ALTERNATE FORAGING STRATEGIES AND
POPULATION STRUCTURE OF ADULT FEMALE
AUSTRALIAN SEA LIONS
Andrew D. Lowther BSc (Hons)
Submitted in fulfilment of the requirements for the degree of
Doctor of Philosophy
University of Adelaide
Faculty of Science
School of Earth and Environmental Sciences
University of Adelaide
February 2012
TABLE OF CONTENTS
LIST OF TABLES.........................................................................................VI
LIST OF FIGURES.......................................................................................VIII
DECLARATION OF ORIGINALITY..............................................................X
STATEMENT OF CONTRIBUTION…………………………………………...XI
DEDICATION..............................................................................................XII
ACKNOWLEDGEMENTS...........................................................................XIII
ABSTRACT.................................................................................................XVI
CHAPTER 1. GENERAL INTRODUCTION...............................................................1
IMPORTANCE OF ECOLOGY AND GENETICS IN DEFINING
POPULATIONS………………………………………….....................................2
INDIVIDUAL SPECIALISATION IN FORAGING BEHAVIOUR AND
POPULATION STRUCTURE..........................................................................4
THE OTARIIDAE…………………………….....................................................6
AUSTRALIAN SEA LIONS…………………….................................................7
NEED FOR RESEARCH………………………………………………………….8
THESIS AIMS.................................................................................................10
CHAPTER 2. DETECTION OF ALTERNATE FORAGING STRATEGIES IN
AUSTRALIAN SEA LION (NEOPHOCA CINEREA) BREEDING COLONIES USING
STABLE ISOTOPE ANALYSIS................................................................................11
ABSTRACT...............................................................................................................12
INTRODUCTION.......................................................................................................13
MATERIALS AND METHODS...................................................................................17
I
Study sites......................................................................................................17
Sampling – Adult Female Australian Sea Lions..............................................17
Sampling – Pups.............................................................................................18
Isotope Analysis..............................................................................................19
Data Analysis..................................................................................................21
RESULTS..................................................................................................................23
Adult Female Foraging Behaviour..................................................................23
Fractionation of Isotopes from Mother to Pup................................................23
Pup Whisker Isotope Ratios and Intracolony Foraging Ecotype
Frequencies...................................................................................................25
DISCUSSION...........................................................................................................26
Pups as Surrogate Measures of Maternal Foraging......................................27
Intra-Colony Segregation of Maternal Foraging Behaviour...........................29
Conclusion.....................................................................................................32
CHAPTER 3. CREATURES OF HABIT: FORAGING SITE FIDELITY OF ADULT
FEMALE AUSTRALIAN SEA LIONS.......................................................................43
ABSTRACT...............................................................................................................44
INTRODUCTION.......................................................................................................45
MATERIALS AND METHODS...................................................................................49
Study sites and sampling................................................................................49
Data analysis..................................................................................................51
RESULTS..................................................................................................................56
Inshore and offshore foraging ecotype designation........................................56
Stability of foraging behaviour over time.........................................................57
II
Movement patterns of individuals...................................................................58
DISCUSSION............................................................................................................59
Individual long-term specialisation in foraging behaviour...............................61
Ecotype-specific differences in movement behaviour and body condition....63
Seasonality of individual foraging behaviour..................................................64
Conclusions....................................................................................................66
CHAPTER 4. POPULATION STRUCTURE OF ADULT FEMALE AUSTRALIAN
SEA LIONS DRIVEN BY FINE-SCALE FORAGING SITE FIDELITY......................79
ABSTRACT................................................................................................................80
INTRODUCTION.......................................................................................................81
MATERIALS AND METHODS...................................................................................85
DNA Amplification...........................................................................................86
Stable Isotope Analysis..................................................................................87
Data Analysis..................................................................................................87
RESULTS..................................................................................................................90
Mitochondrial DNA control region diversity....................................................90
Strong genetic partitioning among colonies...................................................91
Alternate foraging behaviours........................................................................91
Environmental determinants of genetic structure and foraging behaviour....92
DISCUSSION............................................................................................................93
Matrilineal population structure is unrelated to broad-scale ecological
processes......................................................................................................93
III
Is individual niche-width specialisation driving matrilineal population
structure ?.....................................................................................................95
Future Directions...........................................................................................98
Conclusions..................................................................................................100
CHAPTER 5. GENERAL DISCUSSION.................................................................111
Defining the degree of habitat specialisations………………………………………..112
Stability of individual foraging specialisation over time………………………………113
Individual specialisation as a mechanism to drive population structure……………115
Do adult female Australian sea lions maintain individual foraging specialisation
across generations ?...............................................................................................116
The evolution of a unique life history………………………………………………..…118
Future research and conclusions………………………………………………………123
APPENDIX. MATERNAL STRATEGIES OF THE AUSTRALIAN SEA LION
(NEOPHOCA CINEREA) AT DANGEROUS REEF, SOUTH AUSTRALIA...........125
ABSTRACT..............................................................................................................126
INTRODUCTION.....................................................................................................127
MATERIALS AND METHODS.................................................................................130
Maternal attendance, female body condition and milk collection..................131
Milk composition...........................................................................................132
Pup growth...................................................................................................133
Statistical analysis........................................................................................133
RESULTS................................................................................................................135
Maternal attendance.....................................................................................135
IV
Milk-lipid content...........................................................................................136
Pup growth....................................................................................................137
Comparison between Seal Bay and Dangerous Reef..................................139
DISCUSSION..........................................................................................................139
Maternal Strategy.........................................................................................139
Conclusions..................................................................................................143
LITERATURE CITED..............................................................................................152
V
List of Tables
CHAPTER 2. DETECTION OF ALTERNATE FORAGING STRATEGIES IN
AUSTRALIAN SEA LION (NEOPHOCA CINEREA) BREEDING COLONIES USING
STABLE ISOTOPE ANALYSIS.
Table 1: Foraging behaviour of 15 adult female Australian sea lions instrumented
between January 2008 and July 2009.....................................................................34
Table 2: Mean foraging trip and isotope ratio parameter values for alternate foraging
ecotypes of adult female Australian sea lions across all colonies...............35
Table 3: Mean stable isotope ratios from whiskers and blood serum for adult female
Australian sea lions and their pups...........................................................................35
Table 4: Mean isotope values and proportional representation of each ecotype at (a)
Lilliput I., (b) Blefuscu I. and (c) Olive I. from pup whiskers......................................36
CHAPTER 3. CREATURES OF HABIT: FORAGING SITE FIDELITY OF ADULT
FEMALE AUSTRALIAN SEA LIONS.
Table 1: Colony-level mean δ13C and δ15N ratios for serially-subsampled vibrissae
from 20 adult female Australian sea lions across the South Australian range of the
species.......................................................................................................................68
Supplementary Table 1: Descriptive statistics for a) movement and b) dive behaviour
calculated from a randomly-selected foraging trip for 20 adult female Australian sea
lions tracked at seven colonies in South Australia between October 2006 and June
2009...........................................................................................................................69
Supplementary Table 2: Adult female Australian sea lion deployment and sampling
data. Twenty adult females were sampled between October 2006 and June
2009..........................................................................................................................70
Appendix I: Values for (Seasonal) Autoregressive Integrated Moving Average
(SARIMA) models fitted to 14 adult female Australian sea lions with >18 isotope
values........................................................................................................................71
VI
CHAPTER 4. POPULATION STRUCTURE OF ADULT FEMALE AUSTRALIAN
SEA LIONS DRIVEN BY FINE-SCALE FORAGING SITE FIDELITY
Table 1: Characterisation of fifteen Australian sea lion breeding colonies in South
Australia by foraging ecotype using δ13C and δ15N present in pup whiskers..........102
Appendix 1. Median breeding date of colonies sampled…………………………….103
Appendix 2. Haplotype frequency of colonies sampled throughout the South Australian
range………………………………………………………………………………………………104
Appendix 3. Pairwise genetic differences between colonies………………………..105
Appendix 4. Pairwise genetic difference P-values……………………………………106
APPENDIX. MATERNAL STRATEGIES OF THE AUSTRALIAN SEA LION
(NEOPHOCA CINEREA) AT DANGEROUS REEF, SOUTH AUSTRALIA
Table 1: Summary of foraging trip duration, attendance bout duration and proportion
of time spent ashore for individual lactating Australian sea lions in days................145
Table 2: Maternal body length, body condition index and milk-lipid levels of adult
female Australian sea lions during the first two months of lactation at Dangerous
Reef. ‘-‘ indicate milk samples not obtained...........................................................146
Table 3: Summary of linear regressions of mass on age for 18 individual pups
weighed three or more times at Dangerous Reef during the 2006-07 breeding
episode....................................................................................................................147
Table 4. Comparison of maternal strategy data between Seal Bay (Kangaroo Island)
and Dangerous Reef colonies. ...............................................................................148
VII
List of Figures
CHAPTER 2. DETECTION OF ALTERNATE FORAGING STRATEGIES IN
AUSTRALIAN SEA LION (NEOPHOCA CINEREA) BREEDING COLONIES USING
STABLE ISOTOPE ANALYSIS.
Figure 1: Map of Australian sea lion (Neophoca cinerea) breeding colonies sampled
in South Australia from January 2008 to July 2009...................................................37
Figure 2: Dendrogram based on optimal clusters selected from the maximum-value
Bayesian Information Criteria model of hierarchical agglomerative clustering for
means of dive depth, distance from shore at the foraging trip inflection point and
whisker δ13C / δ15N ratios (leave-one-out cross validated classification success =
93.3%).......................................................................................................................38
Figure 3: Linear regression of (a) pup whisker and (b) capillary blood serum isotope
ratios on maternal values...........................................................................................39
Figure 4: Isotope biplots for pups from Lilliput Island (n=43), Blefuscu Island (n=52)
and Olive Island (n=97)..............................................................................................40
CHAPTER 3. CREATURES OF HABIT: FORAGING SITE FIDELITY OF ADULT
FEMALE AUSTRALIAN SEA LIONS.
Figure 1: The endemic Australian sea lion is distributed from Kangaroo Island in
South Australian through to The Abrolhos Islands in Western Australia.................72
Figure 2: Dendrogram displaying alternate foraging ecotypes of 20 adult female
Australian sea lions sampled between June 2006 and Jun 2009 at seven breeding
colonies in South Australia.......................................................................................73
Figure 3: Representative tracking data from 20 adult female Australian sea lions
tracked at a) The Nuyts Archipelago b) West Waldegrave c) Liguanea Island and d)
The Pages Islands and Seal Slide...........................................................................74
VIII
Figure 4: δ13C and δ15N isotope plots for serially subsampled adult female Australian
sea lion vibrissae (3mm segments) from (a) Lilliput Is., (b) Blefuscu Is., (c) Olive Is.,
(d) West Waldegrave,(e) Liguanea, (f) Seal Slide and (g) The Pages Is................76
CHAPTER 4. POPULATION STRUCTURE OF ADULT FEMALE AUSTRALIAN
SEA LIONS DRIVEN BY FINE-SCALE FORAGING SITE FIDELITY.
Figure 1: (a) Locations of sampled (N=17, pie charts) and unsampled (N=6, green
circles) Australian sea lion breeding colonies along the South Australian coast. (b)
Genetic Landscape Surface (GLS) of individual pairwise genetic distances..........107
Figure 2: Plot of Slatkins Linearised Φst on geographic distance............................109
Figure 3: Isotope biplots of δ13C and δ15N values for 15 colonies sampled
highlighting inter-colony variation in the expression of alternate foraging
ecotypes..................................................................................................................110
APPENDIX. MATERNAL STRATEGIES OF THE AUSTRALIAN SEA LION
(NEOPHOCA CINEREA) AT DANGEROUS REEF, SOUTH AUSTRALIA
Figure 1: Location of the current study at Dangerous Reef in the Spencer Gulf, and
Seal Bay (Kangaroo Island) where a similar study was conducted 16 years earlier.
Bathymetry to 100m is shown. Depth increases rapidly towards 100m in the
immediate vicinity of Seal Bay whereas potential foraging habitat within the Spencer
Gulf rarely exceeds 40m.......................................................................................149
Figure 2: Plots of estimated milk-lipid levels among female Australian sea lions
against adult female a) length and b) mass. Milk-lipid levels were significantly
negatively related to maternal length and mass....................................................150
Figure 3: Plots of (a) estimated pup growth rates and (b) mass at 90 days against
predicted values generated by GLM modeling of maternal length and proportion of
time spent ashore. Maternal length and the proportion of time spent ashore positively
influence pup growth rates and masses at 90 days...............................................151
IX
Declaration of originality
In presenting this thesis in fulfilment of the requirement for doctoral degree at the
University of Adelaide, I affirm that this work is original and has not been submitted
for a higher degree to any other university or institution and consent for this thesis to
be made available to the University of Adelaide library, subject to the provisions of
the Copyright Act 1968. The following summarises my contribution to the
publications involving data analysis included in this thesis.
Signature:
Date: 24/1/2012
Mr Andrew Lowther
X
Statement of contribution
Chapter 2: Detecting alternate foraging ecotypes in Australian sea lion (Neophoca cinerea) colonies using stable
isotope analysis.
Lowther, A.D. and Goldsworthy, S.D. (2010). Detecting alternate foraging ecotypes in Australian sea
lion (Neophoca cinerea) colonies using stable isotope analysis. Marine Mammal Science 27(3): 567-586
Conception: 90%, Data Collection: 100%, Analysis: 100%, Writing: 95%
Chapter 3: Creatures of habit: foraging habitat fidelity of adult female Australian sea lions.
Lowther, A.D., Harcourt, R.G., Hamer, D. and Goldsworthy, S.D. (accepted). Creatures of habit:
foraging habitat fidelity of adult female Australian sea lions. Marine Ecology Progress Series.
Conception: 100%, Data Collection: 90%, Analysis: 100%, Writing: 95%
Chapter 4: Population structure of adult female Australian sea lions is driven by fine scale foraging site fidelity.
Lowther, A.D., Harcourt, R.G., Goldsworthy, S.D. and Stow, A. (accepted). Population structure of adult
female Australian sea lions is driven by fine scale foraging site fidelity. Animal Behaviour .
Conception: 90%, Data Collection: 90%, Analysis: 100%, Writing: 95%
Appendix I: Maternal strategies of the Australian sea lion Neophoca cinerea at Dangerous Reef, South
Australia.
Lowther, A.D. and Goldsworthy, S.D. (2011). Maternal Strategies of the Australian sea lion at
Dangerous Reef, South Australia. Australian Journal of Zoology 59: 54-62.
Conception: 70%, Data Collection: 100%, Analysis: 100%, Writing: 80%
Co-authorship was offered to people who assisted me with this project. S. Goldsworthy was involved in the initial
conception of this research and provided general supervision. R. Harcourt and A. Stow provided general
supervision and commented of manuscript drafts. D. Hamer provided a subset of telemetry data for Chapter 3.
By signing this declaration, all co-authors give their consent to allow each published or accepted paper to be
included in this thesis.
Signature:
Date: 16/11/11
A/Prof Simon Goldsworthy
Signature:
Date: 16/11/11
Prof Robert Harcourt
Signature:
Date: 16/11/11
Dr Adam Stow
Signature:
Date: 16/11/11
Mr Derek Hamer
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Dedication
To Brian, Jemma, Charlie, Jessica and Jimmy. My family who silently put up with my
seven year journey of reinvention and gave me their unconditional support
throughout. I am sorry for what this has done.
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Acknowledgements
This body of work started out as a neatly conceptualised plan to be completed in 3,5
years. As Sun Tzu states in his book ‘The Art of War’, ‘no plan ever survives first
contact’. The unique and enigmatic animal I chose to study ensured not only the
initial plan but also plans B, C and D fell by the wayside. As Australian sea lions all
along the southern coastline of Australia battered my efforts to understand them, the
support and guidance of several people kept me true to the cause. Although I will list
a few here, there are doubtless many who I will fail to mention – my omissions are
accidental and unintentional.
Firstly to my principal supervisor Associate Professor Simon Goldsworthy; you left
me be when I needed to figure things out but you offered direction and ‘out-of-thebox’ ideas when I hit the wall. The support you offered in securing funding,
establishing the list of contacts I needed to get through the mammoth amount of
fieldwork required to complete this work and your positive and constructive criticism
of manuscript drafts will be forever appreciated. To Professor Rob Harcourt; as well
as the timely and insightful advice on manuscript drafts, your involvement in various
aspects of fieldwork ranging from recapturing GPS transmitters to posing in photos
on Western Australian roadsides will always be remembered. To Professor Stephen
Donnellan and Dr Adam Stow; molecular ecology is as much an art-of-interpretation
as it is a science, and your guidance and input on all things genetics were greatly
appreciated.
My sincere and heartfelt gratitude to the staff of the Department of Environment and
Natural Resources all along the Spencer Gulf and western Eyre Peninsula: Brett
Dalzell, Robbie Sleep and Mark Anderson in particular were fundamental in making
this work possible. The Ceduna State Emergency Services Marine Rescue unit
headed up by the unflappable and salty Peter Codrington were invaluable
particularly when nobody else would come out to remove us from distant islands in
questionable seas. Andrew Geering and Airborne Solutions gave me the ability to
access islands that would have otherwise remained unsampled.
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Fieldwork is not a one-person job; Kristian Peters, Ian Jupp, Sam Blight, Carly
Wishart, Magali Agreil, Andrew Dawson, Kym Collins, Heidi Ahonen, Ben Pitcher
and many many others made this body of work possible.
The Australian sea lions made every effort to keep their secrets hidden and without
their unwitting cooperation we would still be none-the-wiser. There are several
people who without their guidance and training I would have been hopelessly
unprepared for the vagaries of Australian sea lion work. Al Baylis, for teaching me
how to milk a seal. Derek Hamer for the technicalities of animal capture and
restraint, as well as which brandy to take into the field. Kristian Peters, for a wide
range of expertise; from how much glue is the right amount to use on a transmitter to
how best to cook abalone.
The organisations and funding bodies were key to making this research possible all
deserve thanking. SARDI Aquatic Sciences, the University of Adelaide, the
Australian Marine Mammal Centre, Holsworth Wildlife Research Endowment, Wildlife
Conservation Fund and Sea World Research and Rescue Foundation all contributed
to the study of an Australian icon.
Although I was immersed in Australian sea lions continuously for the best part of five
years I never lost sight of their unique attributes and enigmatic characters. They are
still the most attractive otariid out there, and they still have many secrets left to
discover.
XIV
“Caveo !Hic Svnt Leones”
[“Caveo ! Hic sunt leones” is a Latin expression and literally means ‘Beware ! Here be lions’. It can be
found written on uncharted territories of old maps and was used by the early geographers for
unknown and unexplored territories they imagined as populated by savages, wild animals and other
dangers. It was generally placed at the edges of their known world.]
XV
ABSTRACT
Otariid seals pose several challenges in collecting behavioural data due because of
the geographical decoupling of breeding habitat (terrestrial) and foraging grounds
(aquatic). Additionally, life history traits such as breeding chronology and moult state
constrain the temporal window over which data can be collected. Expensive
telemetry devices coupled with logistical difficulties and the biology of animals often
limits the ability to answer questions concerning the role of seasonal or life-history
differences in foraging ecology. However, quantifying individual behavioural
specialisations such as foraging behaviour that may impede gene flow is an
essential prerequisite to understanding population structure.
Several unusual life history traits of the IUCN Red Listed (threatened) Australian sea
lion Neophoca cinerea are interesting from an ecological, evolutionary and
conservation standpoint. Australian sea lions are endemic to the southern and
western coastline of Australia, distributed over approximately 70 breeding colonies
with 86% of all breeding occurring in South Australia. Most notably, a unique
17.5month breeding chronology and asynchronous breeding between spatially-close
colonies has been proposed to be an adaptive response to a low-quality foraging
environment that has little or no seasonality. Contrary to this, recent studies suggest
at least the South Australian range of the species is a region replete with mesoscale
areas of seasonally rich productivity, further supported by the presence of large
numbers of other top marine predators and the largest volume fishery in Australia. In
the face of this contradiction, the ecological determinants of population structure
clearly have yet to be identified. To address these key knowledge gaps, this study
explored the population structure and foraging behaviour of adult female Australian
XVI
sea lions at seventeen of the largest breeding colonies across the South Australian
range.
A novel screening technique which employed δ13C and δ15N present in the whiskers
of wholly milk-dependent pups was developed and validated as a proxy for maternal
values. Mother-to-pup fractionation was quantified, with a δ15N enrichment of
+1.92‰ (blood) and +1.27‰ (vibrissae). Subsequent large-scale sampling of >50%
of all pups born on each colony suggested a degree of ecological partitioning over a
spatial scale never previously described for otariids.
Isotope ratios of serially-subsampled vibrissae from 20 adult female Australian sea
lions across seven breeding colonies revealed individual long-term temporal
consistency in both foraging site (offshore vs inshore) and prey selection.
Furthermore, dive and movement parameters did not differ between alternate
foraging ecotypes, suggesting that the alternate foraging strategies of adult female
Australian sea lions were temporally persistent and unrelated to phenotypic variation.
Finally, individual foraging specialisation and matrilineal pop ulation structure were
integrated by obtaining isotope and mitochondrial DNA (mtDNA) samples from over
50% of all pups born at each of 17 breeding colonies in order to characterise
foraging ecotype composition and matrilineal population structure. Alternate foraging
ecotypes were present at almost every colony with no evidence to support particular
mitochondrial lineages were restricted to specific foraging ecotypes. Spatial analysis
of molecular data identified three putatitive clusters of colonies that share multiple
haplotypes being interspersed with 9 singleton breeding sites, with genetic structure
becoming more apparent at colonies closer to deep water. Colonies with little or no
similarity in mtDNA haplotype composition were more likely to breed asynchronously
XVII
irrespective of the geographic distance between them. Contrary to expectations, the
propensity for individual animals to forage offshore was unrelated to the proximity of
breeding colonies to deep water.
This study adds considerable knowledge to our current understanding of Australian
sea lion foraging behaviour and highlights the inappropriateness of making broadscale inferences about foraging ecology or population structure in this species.
Individual foraging specialisation may act as an ecological barrier to migration, with
individuals only able to disperse to colonies within range of preferred fine-scale
foraging habitat where they have appropriate hunting skills.
XVIII