Partial Altitudinal Migration of a Himalayan Forest Pheasant:
First Insights and Conservation Implications
Dissertation submitted for the degree of Doctor of Natural Sciences
presented by:
Nawang Norbu
at the
Faculty of Sciences Department of Biology
Date of Oral Examination: 10th April 2014 First Supervisor: Prof. Martin C Wikelski Second Supervisor: Prof. Mark van Kleunen
Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-276589
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All descriptions of reality are temporary hypotheses
Siddhārtha Gautama
I wanted to change the world. But I have found that the only thing one can be sure of changing is oneself
Aldous Huxley
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With gratitude to my parents
And with love to the ‘meritorious lion’ and his mother
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TABLE OF CONTENTS
Summary ... 9
Zusammenfasung ... 13
CHAPTER1: Introduction ... 17
CHAPTER 2: Partial Altitudinal Migration of a Himalayan Forest Pheasant ... 23
ABSTRACT ... 25
INTRODUCTION ... 26
MATERIALS AND METHODS ... 30
RESULTS ... 33
DISCUSSION ... 36
Tables and Figures ... 40
References ... 46
Acknowledgements ... 53
CHAPTER 3: Comparing Energy Expenditure and Home Range Sizes Using GPS- Accelerometer Telemetry in A High Altitude Partial Migration System ... 55
ABSTRACT ... 57
INTRODUCTION ... 57
MATERIALS AND METHODS ... 60
RESULTS ... 65
DISCUSSION ... 68
Tables and Figures ... 72
References ... 80
Acknowledgments ... 87
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CHAPTER 4: Seasonal Altitudinal Migration of the Satyr Tragopan (Tragopan
Satyra) in the Bhutan Himalayas: Implications for Conservation ... 89
ABSTRACT ... 91
INTRODUCTION ... 92
MATERIALS AND METHODS ... 95
RESULTS ... 100
DISCUSSION ... 103
Tables and Figures ... 108
References ... 116
Acknowledgments ... 121
CHAPTER 5: General Discussion and Future Directions ... 123
INSIGHTS INTO ALTITUDINAL PARTIAL MIGRATION AND THEIR CONSERVATION SIGNIFICANCE ... 123
FUTURE DIRECTIONS ... 126
References ... 129
Acknowledgement ... 141
Author Contributions ... 143
Curriculum Vitae ... 145
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S ummary
Animal migration is a complex phenomenon exhibited across many taxonomic groups and occurs in every major ecosystem on our planet. Given the sheer number of animals on the move, migration profoundly shapes, alters and regulates our environment.
Though animal migration has been a subject of study for decades, the ultimate drivers and consequences of migration are still not clearly established. Bird migration in particular has received a great deal of attention from biologists. Till date, most studies have focused on long distance, cross continental latitudinal migrants. However, a significant proportion of birds undertake annual migrations along elevational gradients across mountain regions of the world. So far, only a few studies have examined altitudinal migration systems due to which altitudinal migrations remain poorly
understood. This thesis therefore is the first documentation of an altitudinal migration system in the high altitude Himalayas of Bhutan with state-of-the-art accelerometer enabled GPS telemetry.
I present the first detailed patterns for a complex partial altitudinal migration system for the Satyr Tragopans (Tragopan satyra) in the Bhutan Himalayas. Contrary to current perceptions, I found that altitudinal migration is not a simple up-and-down slope movement of individuals by documenting 3 main patterns of migration: 1) crossing multiple mountains; 2) descending/ascending longitudinally; 3) moving higher up in winter and lower down in summer. Migrants departed consistently across the years and much ahead of snowfall suggesting that altitudinal migrations do not occur as a
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response to extreme weather events. I also found that although females are more likely to migrate, no consistent patterns can be established to explain who migrates and who remains resident within sexes and therefore suggest that extant hypotheses consider both inter as well as intra-sexual differences while explaining partial migration systems.
And I provide anecdotal evidence that individuals can switch strategy from being a migrant to becoming a resident.
Within partial migration systems, proximate tradeoffs associated with the decision to either migrate or to remain a resident are not clearly understood. I therefore examined the possible tradeoffs related to migratory decisions in terms of energy expenditure and home range sizes. I found that winter home ranges for residents overlapped with
conspecifics and were significantly larger than migrants whose home ranges occurred at discrete non-overlapping sites. Over the course of a migratory season, I did not find any significant differences between migrants and residents in energy expenditure as measured by dynamic body acceleration (DBA). Nevertheless, for migrants, I noted higher DBA scores and activity states associated with running/flying and walking during migration. Given that an individual’s migratory status does not significantly affect its overall energy expenditure despite manifesting differently in terms of space use, I suggest that fluctuating micro-habitat conditions across time may enable the maintenance of a partial migration system.
Having assessed the patterns of migration and the possible proximate tradeoffs involved in such a system, I next considered the conservation requirements for partial altitudinal migrants. Both migrants and residents occupied forests all year round. Using accelerometer data, I found that migrants walk to-and-fro between summer breeding
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and non-breeding winter grounds taking multiple days and halting along mountain slopes across forested landscapes. I also found that females migrated in a south
easterly direction while males migrated in random directions and that migrants occupied south-east facing slopes, while residents chose to remain on south-west facing slopes. I therefore suggest corridors in ideal situations would need to run in random directions and recommend that protected areas in mountainous regions include different habitat configurations (aspects) in addition to having a representation of all habitat types.
The findings from my PhD thesis challenge many of the assumptions associated with altitudinal migrants and offer new perspectives to our understanding of both altitudinal and partial migration systems. In addition, by demonstrating habitat associations, migratory modes and pathways, the thesis contributes towards helping conserve such magnificent migrations which occur across the mountain regions of our planet. Taking advantage of the advances in accelerometer enabled GPS telemetry, my thesis has demonstrated that it is possible to track individuals and illustrate previously unknown patterns of migration over annual cycles. I recommend that future studies collate data across multiple years measuring explanatory variables associated with habitat quality, fecundity, mortality rates, individual condition and predation pressure, while
simultaneously tracking both migrants and residents. Such a study will contribute
significantly in helping understand and uncover both the proximate and ultimate causes and consequences of migrations
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Z usammenfasung
Tierwanderung ist ein komplexes Phänomen, das in vielen taxonomischen Gruppen und in jedem großem Ökosystem unseres Planeten auftritt. Angesichts der hohen Anzahl von Tieren, die sich ständig bewegen, prägen, verändern und regulieren
Tierwanderungen unsere Umwelt grundlegend. Obwohl Tierwanderungen bereits seit Jahrzehnten erforscht werden, sind die Grundlagen und Auswirkungen bisher noch nicht eindeutig verstanden. Insbesondere der Vogelzug erzielt unter Biologen eine große Aufmerksamkeit. Bis heute befassen sich die meisten Untersuchungen jedoch mit Langstreckenziehern. Ein signifikanter Anteil der Vögeln begibt sich jedoch im Jahresverlauf auf Migrationen entlang von Höhengradienten über die Bergregionen dieser Erde. Bisher gibt es nur wenige Studien zu diesen Höhenmigrationssystemen, weshalb die Tierwanderungen in Höhenlagen weitgehend unverstanden sind. Diese Doktorarbeit ist die erste Dokumentation eines Höhenmigrationssystems in den Höhenlagen des Himalayas in Bhutan mithilfe von von GPS-Telemetrie und hochmodernen Beschleunigungsmessern.
Ich präsentiere die ersten detaillierten Muster des komplexes Höhenteilzugsystems der Satyrtragopane (Tragopan satyra) in der Himalayaregion Bhutan. Indem ich drei
Hauptmigrationsmuster unterscheide, kann ich zeigen, dass, entgegen der bisherigen Annahmen, die Höhenmigration keine einfache Auf-und Abbewegung entlang von Berghängen ist. Die drei Muster sind 1) der Überflug mehrerer Berge, 2) das
longitudinale Auf- und Absteigen sowie 3) der Aufwärtszug im Winter und Abwärtszug
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im Sommer. Die Tatsache, dass die Tiere ihre Migration das ganze Jahr über starteten und auch lange bevor es zu schneien beginnt, legt nahe, dass diese Höhenmigrationen nicht aufgrund von extremen Wetterbedingungen stattfindet. Ebenfalls habe ich
herausgefunden, dass, obwohl die Wahrscheinlichkeit der Migration von Weibchen höher ist, innerhalb der Geschlechter keine einheitlichen Muster gefunden werden können, die erklären, welche Tiere ziehen und welche nicht. Dies deutet darauf hin, dass sowohl inter- als auch intrasexuelle Unterschiede bei der Erklärung dieses Teilzugsystems herangezogen werden müssen. Des weiteren präsentiere ich anekdotische Beobachtungen, die zeigen, dass einzelne Individuen ihre Strategie zwischen Ziehen und Nicht-Ziehen wechseln können.
In Teilzugsystemen sind die proximaten Faktoren für den Kompromiss zwischen der Entscheidung zu ziehen oder zu bleiben noch nicht völlig verstanden. Ich habe daher die für die Zugentscheidung relevanten Tradeoffs in Bezug auf Energieaufwand und Reviere untersucht. Ich habe herausgefunden, dass sich die Winterreviere der
Standvögel überlappen und signifikant größer sind als die klar voneinander getrennten Reviere der Zugvögel. Im Laufe der Zugsaison konnte ich anhand der dynamischen Körperbeschleunigung (dynamic body acceleraction; DBA) der besenderten Vögel keine signifikanten Unterschiede des Energieaufwands zwischen Zugvögeln und Standvögeln nachweisen. Nichtsdestotrotz konnte ich bei den Ziehern höhere DBA-Werte und eine gesteigerte Aktivität im Zusammenhang mit Laufen, Fliegen und Gehen messen. Da der Migrationsstatus eines Tieres seine Raumnutzung, jedoch nicht seinen
Energieverbrauch beeinflusst, gehe ich davon aus, dass sich im Zeitverlauf ändernde Mikrohabitate für die Aufrechterhaltung des Teilzugsystems verantwortlich sind.
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Nach der Untersuchung der Migrationsmuster und der möglichen proximaten Tradeoffs dieses Systems war der nächste Schritt, die Schutzansprüche dieser partiellen
Höhenzieher zu untersuchen. Sowohl die Zieher als auch die Standvögel leben das ganze Jahr über in Wäldern. Mithilfe der Beschleunigungsdaten habe ich festgestellt, dass die Zugvögel zwischen den sommerlichen Brutrevieren und den Winterrevieren mehrere Tage lang gehend zurücklegen und dabei an bewaldeten Berghängen Pausen einlegen. Des weiteren habe ich herausgefunden, dass Weibchen in südöstlicher Richtung migrieren wohingegen die Männchen keine festgelegte Zugrichtung haben.
Die Zugtiere nutzen Berghänge mit südöstlicher Ausrichtung wohingegen die Standvögel auf südwestlich ausgerichteten Berghängen bleiben. Ideale Korridore sollten daher in alle Richtungen gehen und Schutzgebiete in Bergregionen sollten neben allen Habitatsklassen außerdem verschiedene Berglagen berücksichtigen.
Die Ergebnisse meiner Doktorarbeit hinterfragen viele der bisherigen Annahmen zur Höhenmigration und bieten neue Gesichtspunkte sowohl für die Höhenmigration als auch für den Teilzug. Darüber hinaus hilft diese Arbeit beim Schutz solch
außergewöhnlicher Migrationen in den Bergregionen unseres Planeten indem sie
Habitatsansprüche, Migrationsmuster und -wege aufzeigt. Diese Arbeit zeigt außerdem, dass durch die Nutzung von GPS-Telemetrie in Kombination mit
Beschleunigungsmessung einzelne Individuen verfolgt und bisher unbekannte Migrationsmuster im Jahresverlauf aufgezeichnet werden können. Für zukünftige Studien empfehle ich Bewegungsdaten aus mehreren Jahren sowohl von Stand- als auch von Zugvögeln mit erklärenden Variablen wie der Habitatqualität, Fertilität,
Sterberate, der individuellen körperlichen Verfassung der Tiere und der Prädationsrate
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zu verbinden. diese Studien werden entscheidend zum weiteren Verständnis der proximaten und ultimaten Faktoren und Konsequenzen von Tierwanderungen beitragen.
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CHAPTER 1 : I ntroduction
Animal migration is a complex phenomenon exhibited across many taxonomic groups (Dingle & Drake 2007; Wilcove & Wikelski 2008) and occurs in every major ecosystem on our planet. Given the sheer number of animals on the move, migration profoundly shapes, alters and regulates our environment. While migration influences ecosystem functions (Post et al. 1998; Brodersen et al. 2008; Brodersen, Nicolle & Nilsson 2011), migration itself occurs in response to changing environmental conditions (Alerstam, Hedenstro & Åkesson 2003; Dingle & Drake 2007) while also being genetically
controlled to some extent (Pulido, Berthold & van Noordwijk 1996; Pulido 2007, 2011).
As such, migration as a tactic elucidates mechanisms by which organisms interact with their environment (Bowlin et al. 2010) and can therefore help in understanding how an organism responds to its environment (Schwenk et al. 2009).
Though animal migration has been a subject of study for decades, the ultimate drivers and consequences of migration are still not clearly established. Bird migration in
particular has received a great deal of attention from biologists (Berthold 2001; Newton 2008). Till date, most studies have focused on long distance, cross continental
latitudinal migrants. However, a significant proportion of birds across mountain regions of the world undertake annual migrations (Stiles 1988; Powell & Bjork 1995; Burgess &
Mlingwa 2000; Chaves-Champos, Arevalo & Araya 2003; Faaborg et al. 2010) along elevational gradients. So far, only a few studies have examined altitudinal migration systems (Dixon & Gilbert 1964; Loiselle & Blake 1991; Blake, Stiles and Loiselle 1993;
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Cade & Hoffman 1993; Powell & Bjork 1994, 1995; Chaves-Champos et al. 2003; Hahn et al. 2004; Boyle 2008, 2010; Laymon 2009; Mackas et al. 2010; Boyle, Norris &
Guglielmo 2010; Boyle, Conway & Bronstein 2011a; Hess et al. 2012) and therefore altitudinal migrations remain poorly understood. The ability of animals to use gradients provided by elevational changes along mountains is of course not restricted to birds alone. Evidence has been presented that altitudinal gradients have been used since the time of the dinosaurs (Fricke, Hencecroth & Hoerner 2011), and animals from all major taxonomic groups from butterflies (Shapiro 1974) to bats (McGuire & Boyle 2013) to giant tortoises (Blake et al. 2012) engage in altitudinal migrations.
Mountains regions which host such altitudinal migrations are also important harbours of life and cover an estimated 24.3% of the world’s land surface area (Kapos et al. 2000).
However, rapid climate change (Noguesbravo et al. 2007) will significantly impact mountain regions and species therein are predicted to be profoundly impacted by such changes (Inouye et al. 2000). Mountain regions also continue to be subjected to
anthropogenic pressure (Blyth et al. 2002) and will be significantly impacted by forest cover loss (Hansen et al. 2013). Studies on altitudinal migration will therefore also contribute to the understanding of mountain ecosystems and their conservation.
Many of the hypotheses related to bird migration have so far been only tested in long distance cross continental migratory systems (Berthold 2001; Newton 2008). An examination of whether the theories which have been propounded to explain long distance bird migration equally apply to birds which migrate short distances over altitudinal gradients have not received adequate attention (see exceptions Boyle &
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Conway 2007; Boyle 2008, 2010; Gillis et al. 2008; Boyle et al. 2010, 2011b; Mackas et al. 2010).
Most migration systems – altitudinal ones included – can be partial migration systems where only a portion of the population migrates. Partial migration systems are
considered to be an intermediate state between complete sedentariness and complete migratoriness (Berthold 2001). Such systems therefore offer the opportunity to examine tradeoffs involved in migration and the factors involved in determining migrants and residents. Classically, 3 main hypotheses have been evoked to help explain partial migration (Ketterson & Nolan 1976). However, empirical evidence remains contradictory and appears to differ across species and regions (Chapman et al. 2011). As such, the ultimate mechanisms that drive individual differences remain controversial (Chapman et al. 2011).
In general, the phenomenon of migration is under increasing stress (Wilcove 2008a; b;
Wilcove & Wikelski 2008) and undergoing severe decline. Given these challenges and recognizing our lack of knowledge on altitudinal migrants, it appears imperative that attention be paid to understanding altitudinal migration systems. Recent developments in the field of GPS and accelerometer based telemetry (Cooke, Hinch & Wikelski 2004;
Cooke et al. 2013; Wilson et al. 2006; Wilson, Shepard & Liebsch 2007) allows the inference of behavior and the calculation of energy expenditure in free living wild animals. Such a system enables us to measure individual tradeoffs in addition to helping discover and illustrate previously unknown migration patterns and habitat requirements of migrants. Such information will help us better conserve migratory species (Cagnacci et al. 2010).
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This thesis examines, for the first time, a partial altitudinal migration system with high resolution accelerometer enabled GPS telemetry in the Himalayas, an important yet relatively understudied part of the world.
In Chapter 2, the discovery of a partial altitudinal migration system for the Satyr
Tragopan (Tragopan satyra) in the Himalayas is presented. In addition to showing the complex patterns of migration, I conduct the first tests for classical hypotheses and their applicability to our observations. I examine whether extreme weather related events drive altitudinal migrations and also assess whether altitudinal migration is a simple up- and-down slope movement between summer breeding grounds to non-breeding winter grounds. I also report on migration timing, duration, distance traversed and fidelity to breeding areas.
Although, partial migration systems are ubiquitous (Chapman et al. 2011), tradeoffs in partial migration systems remain poorly understood and the proximate consequences of individual decisions have not been examined. In Chapter 3, I compare differences in energy expenditure and home range sizes between migrants and residents using accelerometer enabled GPS telemetry across a migratory season with an aim to ascertain tradeoffs between different strategies.
Given continuing anthropogenic pressure related to forest cover loss (Hansen et al.
2013) and climate change (Inouye et al. 2000); altitudinal migrants may be at risk. In Chapter 4, I examine the conservation requirements of altitudinal migrants. I assess the mode of migration, distance travelled and the direction of travel. I also examine habitat
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use and landscape configuration requirements for altitudinal migrants. I use the findings to discuss conservation requirements of seasonal altitudinal migrants in montane
environments.
In Chapter 5, I discuss key findings from my thesis and recommend areas of further investigation which will help enhance our understanding of migration in general and altitudinal migration in particular.
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CHAPTER 2 : P artial Altitudinal Migration of a Himalayan Forest Pheasant
Nawang Norbu1, 2, 3, Martin C Wikelski2,3, David S Wilcove4, Jesko Partecke2, Ugyen1, Ugyen Tenzin1, Sherub1, Tshering Tempa1,5
PLoS One 8: e60979
1 Ugyen Wangchuck Institute for Conservation and Environment, Lamai Gompa, Bumtang, Bhutan, 2 Max-Planck Institute for Ornithology, Radolfzell, Germany, 3 International Max-Planck Research School for Organismal Biology, University of Konstanz, Germany, 4 Woodrow Wilson School of Public and International Affairs, Princeton University, New Jersey, USA, 5 College of Forestry and Conservation, University of Montana, USA
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25 ABSTRACT
Altitudinal migration systems are poorly understood. Recent advances in animal telemetry which enables tracking of migrants across their annual cycles will help
illustrate unknown migration patterns and test existing hypotheses. Using telemetry, we show the existence of a complex partial altitudinal migration system in the Himalayas and discuss our findings to help better understand partial and altitudinal migration. We used GPS/accelerometer tags to monitor the migration of Satyr tragopan (Tragopan satyra) in the Bhutan Himalayas. We tagged 38 birds from 2009 – 2011 and found that tragopans are partially migratory. Fall migration lasted from the 3rd week of September till the 3rd week of November with migrants traveling distances ranging from 1.25 km to 13.5 km over 1 to 32 days. Snowfall did not influence the onset of migration. Return migration started by the 1st week of March and lasted until the 1st week of April.
Individuals returned within 4 to 10 days and displayed site fidelity. One bird switched from being a migrant to a non-migrant. Tragopans displayed three main migration patterns: 1) crossing multiple mountains; 2) descending/ascending longitudinally; 3) moving higher up in winter and lower down in summer. More females migrated than males; but, within males, body size was not a factor for predicting migrants. Our observations of migrants traversing over multiple mountain ridges and even of others climbing to higher elevations is novel. We support the need for existing hypotheses to consider how best to explain inter- as well as intra-sexual differences. Most importantly, having shown that the patterns of an altitudinal migration system are complex and not a simple up and down slope movement, we hope our findings will influence the way
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altitudinal migrations are perceived and thereby contribute to a better understanding of how species may respond to climate change.
INTRODUCTION
Animal migration is a complex phenomenon exhibited across many taxonomic groups (Dingle & Drake 2007; Wilcove & Wikelski 2008) and has been a subject of study for decades due to its prevalence across taxa and its importance in the life history of organisms (Dingle 1996). Migration as a tactic also elucidates mechanisms by which organisms interact with their environment (Bowlin et al. 2010) and as such is important in understanding an organism’s response to its environment (Schwenk et al. 2009).
However, given that the phenomenon of migration is increasingly under stress (Wilcove 2008a; b; Wilcove & Wikelski 2008), it is important to better understand aspects and systems which have not yet received adequate study.
Bird migration in particular has received a great deal of attention from biologists
(Berthold 2001; Newton 2008). In addition to long distance, cross continental latitudinal movements, many birds also undertake annual migrations along elevational gradients in montane environments (Stiles 1988). So far, only a few studies have focused on
altitudinal migration systems (Dixon & Gilbert 1964; Loiselle & Blake 1991; Blake, Stiles and Loiselle 1993; Cade & Hoffman 1993; Powell & Bjork 1994, 1995; Chaves-
Champos, Arevalo & Araya 2003; Hahn et al. 2004; Boyle 2008a, 2010; Laymon 2009;
Mackas et al. 2010; Boyle, Norris & Guglielmo 2010; Boyle, Conway & Bronstein 2011a;
Hess et al. 2012) and have mostly been viewed as individuals moving from higher
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elevations to more favorable lower elevations and vice-versa in response to fluctuating environmental conditions such as availability of food (Loiselle & Blake 1991; Blake, Stiles and Loiselle 1993; Chaves-Champos et al. 2003; Boyle 2010; Boyle et al. 2011a), changes in weather (Boyle et al. 2010), or trade-offs between survival and predation risks (Boyle 2008a). However, very few studies have examined these in detail (Dixon &
Gilbert 1964; Cade & Hoffman 1993; Chaves-Champos et al. 2003; Hahn et al. 2004;
Laymon 2009); and very little is known about altitudinal migration patterns (but see Hess et al. 2012 and Powell & Bjork 1994, 1995).
It has been suggested that most migrations may in fact be partially migratory systems (Chapman et al. 2011a), where only a fraction of the population migrates (Chapman et al. 2011b; Shaw & Levin 2011). This has been found to be true also for altitudinally migrating tropical birds (Boyle 2008b; Boyle et al. 2010, 2011b; Mackas et al. 2010). In such cases, where a population is partially migratory, emphasis has been placed on determining differences between migrants and non-migrants (Cristol, Baker & Carbone 1999; Bell 2005; Boyle 2008b). Three main hypotheses have been used to explain partial migration (albeit these hypotheses were initially formulated to explain differential migration): the dominance hypothesis (Gauthreaux 1978), the body-size hypothesis (Ketterson & Nolan 1976; Ketterson & Nolan 1983), and the arrival time hypothesis (Ketterson & Nolan 1976). Here, we consider only the body size and the arrival time hypotheses, given difficulties of measuring dominance in the field.
The body size hypothesis predicts that smaller individuals will migrate once food availability declines or due to intolerable colder temperatures. Here, two main
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mechanisms are invoked. One is food availability, where it is assumed that bigger individuals would be better able to compete for food or have greater fasting ability during times of food scarcity. The other mechanism is the ability to withstand
temperature changes, where larger individuals, who have lower surface area to volume ratio, are better able to withstand colder temperatures and therefore remain sedentary (or migrate if it becomes too hot (Alonso et al. 2009)). This differential ability to thermo- regulate based on size has also been stated as the thermal tolerance hypothesis (Calder 1974). Most studies in the temperate zone tend to support the body size hypotheses (Lundberg 1985). However, recent studies from the neo-tropics (Boyle 2008b; Jahn et al. 2010) have shown that bigger individuals are more likely to migrate, highlighting the need to re-interpret prevailing hypotheses based on site and social system specific conditions (reviewed by (Chapman et al. 2011a)).
The arrival time hypothesis (Ketterson & Nolan 1976) posits that individuals which establish territories during the breeding season will be less likely to migrate. The hypothesis further predicts that in cases where territorial individuals do migrate, they migrate shorter distances than individuals who do not need to establish territories (i.e., females in our case) resulting in differential migration. Availability of food and declining temperatures at limited breeding grounds are invoked as the underlying driving
mechanisms.
Studies so far offer mixed support for the current hypotheses (Chapman et al. 2011a).
Recent telemetry techniques (e.g., gps-tracking) which allow researchers to track animals throughout their annual cycle may enable better testing of extant hypotheses
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and also illustrate hitherto unknown patterns of migrations. Unfortunately, most
altitudinal migration studies so far have used telemetry only to a limited extent (Cade &
Hoffman 1993; Powell & Bjork 1994, 1995; Chaves-Champos et al. 2003; Hahn et al.
2004; Laymon 2009; Hess et al. 2012) even though these systems occur over
comparatively smaller geographic space and are therefore more feasible study systems.
In addition to contributing to a better understanding of migration ecology, telemetry data are also crucial to ensuring the adequate conservation of species that undertake such migrations (Powell & Bjork 1995). Since mountain systems will witness faster rates of warming (Nogués-Bravo et al. 2007), altitudinal migration systems across the world’s mountains (Faaborg et al. 2010) may be affected in novel and unpredictable ways (Inouye et al. 2000). Most species of birds in the Himalayas (including Bhutan) are considered to be altitudinal migrants (Grimmett, Inskipp & Inskipp 1999). Yet, to our knowledge, there are no studies on altitudinal migration of birds employing telemetry in the Himalayas.
We used state-of-the-art GPS/accelerometer tags to monitor migration in a high altitude pheasant, the Satyr tragopan (hereafter referred to as tragopan/s) in the Bhutan
Himalayas. We present results for fall migrations for 2009, 2010, 2011 and return migrations for 2011 and 2012. We documented the existence of a complex partial altitudinal migration system. Our results offer partial support for the arrival time hypothesis. Within males, we refute the body size and the thermal tolerance hypotheses. We discuss implications of our findings within the broader context of helping understand altitudinal and partial migration.
30 MATERIALS AND METHODS
Study Area
Tragopans were studied in Thrumshingla National Park (Figure 6) of Bhutan (27° 22'46'' N, 91°01'46''E). Elevation in the study area ranged from 1500 masl to 4500 masl and temperatures ranged from a maximum of 25 °c to a minimum of -8 °c. The area has four distinct seasons with most rainfall occurring between the months of May to August as part of the Asian monsoons. The study area is mostly conifer forests dominated by fir (Abies densa) with rhododendron understory at higher elevations (>3000 masl) transiting to mixed conifer forests (2400 – 3000 masl) comprising of spruce (Picea spinulosa), hemlock (Tsuga dumosa) and larch (Larix griffithii). Below 2400 masl, conifer forests give way to conifer-broadleaf mixed forests, and to cool broadleaved forests comprising mostly of oak (Quercus glauca and Q. lamellosa). There are also a few patches of open grazing areas used by nomadic cattle herders in the region.
Study Species
The Satyr tragopan (Tragopan satyra) is a pheasant species endemic to the central and eastern Himalayas covering the countries of Nepal and Bhutan. They are also found in the state of Arunachal Pradesh in India, and some lower valleys of Xizang in China (Sibley & Monroe 1990). Only an estimated 20,000 individuals (about 6000 – 15000 adults) are extant in the wild (BirdLife International 2012). The tragopans are classified as Near Threatened by the IUCN (IUCN 2008) and listed on Appendix III of CITES (www.cites.org). Such listings while important may not adequately reflect the actual
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threat to a species. In many parts of its range, it has been suggested that the tragopans face increasing threats from habitat loss, forest fires and poaching (BirdLife International 2012).
Adult male tragopans weigh from 1.3 to 2.1 kgs, while females weigh from 1 to 1.3 kgs.
They are omnivorous and feed on seeds, fresh leaves, moss, bamboo shoots, berries and insects (BirdLife International 2012). Adults perform elaborate courtship displays and breeding starts from April and lasts till June. About 3 – 5 eggs are laid per clutch which are then incubated for about 28 days (BirdLife International 2012). Little is known of the biology of tragopans in the wild, and although it has been noted that tragopans are altitudinal migrants (Grimmett et al. 1999), no studies so far have investigated this phenomenon.
We trapped tragopans in 2009, 2010 and 2011 using neck noose traps laid along known haunts following ridges which we barricaded with bamboo and other shrub species. We flushed tragopans towards traps during early mornings and evenings. All animal
trapping were approved by the Ministry of Agriculture and Forests in Bhutan. In 2009, in order to reduce any handling related fatality given that these pheasants were trapped for the first time, all captured pheasants were released immediately after attaching GPS tags. Pheasants captured in 2010 and 2011 were weighed (to the nearest gm) and measurements were also taken of tarsus length (mm) and beak size (mm).
GPS Tags and Data Acquisition
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We used GPS/accelerometer tags (www.e-obs.de, Munich, Germany) to record the location (GPS) and activity (accelerometer) of our tragopans. Tags with harnesses weighed 45 gms. These tags save the recorded data (i.e., location, elevation, date, time and acceleration) onboard to be remotely downloaded via a handheld base station after the tragopan is relocated via the tag VHF radio pulse (ping). To help locate tagged birds, tags were programmed to ping once every 2 seconds for 2 hours every day.
Tags deployed in 2009 were programmed to take a GPS reading every 2 hours from 0400 hrs to 2200 hrs. Given battery power constraints; tags in 2010 were programmed to take only 2 GPS readings everyday at 0600 hrs and 1400 hrs; while in 2011 tags were programmed to take 3 GPS readings everyday at 0800 hrs, 1400 hrs and 2000 hrs. In order to optimize battery performance, tags were further programmed with GPS
‘give up times’ of 2 minutes, after which the tag does not try to obtain a GPS fix for that particular location.
Distance and Duration of Migration
We classified all birds which showed distinct summer and winter ranges (birds staying more than a month at a given location) as migrants and the rest as residents. We measured migration distance using the ‘show elevation profile’ tool in Google Earth 5.2 as the distance between the location on the day when migration was initiated to the first location of the day when migration was terminated. Total number of migration days was calculated as difference between the date of initiation of migration and the date of cessation of migration.
33 Temperature Profile
Temperature loggers (HOBO ©) were placed at 2900 masl (summer range) and 1700 masl (assumed winter range) during 2009. In 2010, after ascertaining winter ranges for 2 migrating birds, additional loggers were deployed at 2700 masl and 2300 masl.
Loggers were programmed to record temperatures averaged across every 20 minutes at a sampling interval of 10 seconds. Gain in temperatures were calculated as the difference between the average temperature at 2900 masl on the day when migration was initiated and the temperature at 2300 masl on the day when migration was
terminated.
Statistical Analyses
We used body mass (kg) and a body size index (mass [kg]/tarsus length [mm]) and developed a logistic regression model with a logit link function in R (http://www.r- project.org; version 2.15.1) to test whether an individual’s migratory status was related to its body mass and size index. All other statistical tests were also performed in R.
RESULTS
We tagged 38 birds over three years (2009, 2010, 2011). We obtained complete
downward migration data for 14 birds, return migration data for 5 birds, and data for 10
34
birds that did not migrate. We lost 14 birds. See Table 1 and Supplementary Table. All data have been archived at Movebank.org.
Patterns of Migration
We determined 3 main patterns of migration (Figure 1 and 2). Of the 14 migrants, five (3 females and 2 males) descended and returned longitudinally along mountain slopes (i.e., traveled parallel to the mountain ridges). Seven birds (5 females and 2 males) crossed over multiple mountain passes to and from their wintering grounds.
Surprisingly, two birds (1 female and 1 male) actually migrated to higher elevations during winter and later returned to their breeding grounds at lower elevations.
Who Migrates?
Females were significantly more likely to migrate than males (n=24, Fisher’s exact test, p = 0.047) and males were significantly heavier than females (n=20, t= –9.8707,
p=0.000). Within males (n=11, 4 migrants and 7 non-migrants), neither body mass nor an index of body size [body mass (kg)/tarsus length (mm)] were significant predictors for male migratory status (Table 2 and Figure 3).We did not carry out a similar analysis for females (n=9) as we had body mass data for only one sedentary female (Figure 3).
Distance and Duration of Migration
Duration of fall migration did not differ between sexes (n=14, t=-0.7461, p=0.4739) and ranged from 1 day (for an individual descending down a mountain) to 32 days (for an
35
individual who crossed multiple mountains) with a mean of 12 (± 7.07) days for females and 8.8 (± 10.02) days for males. Distance migrated ranged from 1.25 km to more than 13.5 km and did not differ between sexes (n=14, t=-0.0238, p=0.9815) with a mean distance of 6.91 (± 3.16) km for females and 6.87 (± 3.71) km for males. Elevation differences between summer and winter grounds ranged from a gain of 920 masl (individuals descending to lower altitudes) to a loss of 190 masl (individuals ascending to higher elevation sites). There was no elevation change for one female migrant. We found no difference between males and females in terms of elevation change (n=14, t=- 0.4071, p=0.6937). See Figure 4.
Out of the 5 birds (1 female and 4 males) for which we obtained data for return
migration, 4 individuals (3 females and 1 male) returned within 4 days with one female taking upto 10 days. All returning birds displayed fidelity to their breeding sites.
Timing of Migration
Birds began their fall migration as early as the 3rd week of September with some leaving as late as the 3rd week of November (Figure 5a) with a median departure date of 26th October (n=14) for all years combined. While average daily temperatures at our study site decline gradually after August, departure dates were much ahead of snowfall events in the area (Figure 5b) which occur starting from late December and lasts till mid-March. Birds started to return between the first week of March and the first week of April following increasing temperatures beginning in mid-February (Figure 5b).
36
Other Observations: Do Migrants Remain Migrants?
In 2011, we recaptured one male bird which had been tagged in 2010. While it migrated in 2010, it did not do so in 2011. We found that the bird had gained weight (2010 = 1.46kg; 2011 = 1.68kg), increased its beak size (2010 = 15mm; 2011 = 16mm) and also increased the length of its tarsus (2010 = 63mm; 2011 = 74mm).
DISCUSSION
To our knowledge, this is the first time an altitudinal migration system has been documented with high resolution GPS telemetry in the Himalayas. By tracking individuals throughout an annual migratory cycle, we confirmed that tragopans are partial altitudinal migrants. We show that migrants moving to lower/higher elevations do so by either traversing parallel to mountain ridges or by crossing multiple mountain passes. Unexpectedly, we also found that migrants move up to higher elevations in winter. Blue grouse (Cade & Hoffman 1993) have also been found to move higher up during winters. Our results challenge the conventional notion that altitudinal migrants move to lower elevations during winter and vice-versa. Also, the complex movement patterns demonstrate that altitudinal migration is not a simple up and down-slope movement.
Our clear female biased migration system lends support to the arrival time hypothesis (Ketterson & Nolan 1976; Morbey, Coppack & Pulido 2012) which predicts that territorial males are less likely to migrate so as to maintain their territories for the coming breeding season. However, while the hypothesis further predicts that the sex which maintains
37
territories (i.e. males in our case) should travel shorter distances than the one that do not maintain territories (in our case, females); we found no difference between migratory males and females in terms of distance traveled or elevation changes between summer and winter. Other studies investigating the arrival time hypothesis have produced
inconsistent patterns. For example, male Blue Grouse (Dendragapus obscurus) (Cade
& Hoffman 1993) moved farther than females, whereas female Spruce Grouse
(Canachites canadensis) (Herzog & Keppie 1980; Schroeder & Braun 1993) traveled farther than males. One way of testing the arrival time hypothesis has been the
measurement of return dates to breeding sites where it is predicted that the sex which maintains territories will arrive earlier. While we found no return migration date
differences between males and females, we refrain from making interpretations given our small sample sizes (4 females, 1 male). Others have reported that male Spruce Grouse (Herzog & Keppie 1980) and Blue Grouse (as cited in Herzog & Keppie 1980) return earlier to their breeding grounds. Additional data on spring arrival dates would enable us to better test this hypothesis.
Given that females are significantly smaller than males, our finding that more females migrated than males also provides support for the body-size hypothesis, which predicts that larger individuals are less likely to migrate. However, a within male investigation finds no support for this hypothesis with both smaller and lager males being equally likely to remain sedentary or to migrate. Also, in addition to smaller individuals
remaining resident year round; a migrant male (1.35 kg) climbed to higher elevations (with presumably colder temperatures) in winter. Also, a female migrant (1.12 kg) climbed to higher elevations in winter. As such, we believe that individuals do not
38
migrate as a consequence of dropping temperature levels and that body size does not determine migrants at the intra-sexual level. Our findings reinforces the need for greater consideration of inter- and intra-sexual differences while testing current hypotheses and we support the need to assess these hypotheses in cases where sexes are of the same size or where females are bigger than males (Chapman et al. 2011a).
We did not investigate food availability in our study system. However food availability has been important in determining upward return migrations (but not the downward fall migrations) for the White-ruffed Manikins (Corapipo altera) (Boyle 2010). In other pheasant species, it has been noted that food may not be an important factor in driving migrations (Cade & Hoffman 1993; Schroeder & Braun 1993). A closer examination of diet preferences, individual foraging strategies, and fluctuations in food availability at both breeding and wintering sites will help clarify the role of food further.
Given that weather determines both food availability and individual thermoregulation, it has been suggested that extreme weather related events (Boyle et al. 2010) drive altitudinal migrations. Our tragopan migrants departed consistently across years after rainfall peaks (July to August) and much ahead of the onset of snow (Figure 5b). As such, we believe that altitudinal migration in our case is not driven by extreme weather events.
All birds for which we have return data displayed site fidelity. These return sites were also in close proximity to sites that were occupied year-round by resident birds. Our field observations suggest that these are preferred breeding areas. As such, we speculate
39
that density of individuals at summer breeding grounds (Lundberg 1987, 1988; Taylor &
Norris 2007) may be influencing migration in relation to the carrying capacity of breeding grounds. Further analysis on movement and activity patterns between migrants and non-migrants may help explain trade-offs in a partial migration system.
Interestingly, one male switched from being a migrant in 2010 to a non-migrant the following year. This provides anecdotal support that migration may be a plastic phenotypic response, where environmental variation can maintain differences in individual strategies (Brodersen et al. 2011). This is contrary to Spruce Grouse where migratory strategies do not change (Herzog & Keppie 1980). Assessing the repeatability of migratory strategy over the lifetime of an individual may help further clarify this
question and provide much needed answers to help address gaps in our current understanding on the role of, and balance between, genetic and environmental influences (Pulido 2011) in partial migration systems.
The ultimate reasons for why some individuals migrate while others remain sedentary are unclear (Chapman et al. 2011a). However, we provide the first tests for a few of the existing hypotheses in a previously unstudied altitudinal migrant from the Himalayas, an important yet relatively understudied part of the world. Our observations of migrants traversing over multiple mountain ridges and even of others climbing to higher elevations is incredibly interesting, but further complicates an already puzzling
phenomenon. We highlight that existing hypotheses will benefit from considering how best to explain inter- as well as intra-sexual differences. Most importantly, having shown that the patterns of an altitudinal migration system are complex and not a simple up and
40
down slope movement, we hope our findings will influence the way altitudinal migrations are perceived and thereby contribute to a better understanding of how species may respond to climate change.
Tables and Figures
Table 1. Number of individuals by year and sex classified as migrants and residents and birds for which data could not be obtained
No of Birds Year
Trapped
Total Birds Tagged
Data for Fall Migration
Data for Spring/
Return Migration
Data for Sedentary Birds
Not Determined/
Birds Lost/
2009 10 (4F, 6M) 2 (1F, 1M) Na 2 (1F, 1M) 6 (2F, 4M)
2010 14 (7F, 7M) 7 (5F, 2M) 0 1 (0F, 1M) 6 (2F, 4M)
2011 14 (4F, 10M) 5 (3F, 2M) 3 (2F, 1M) 7 (1F, 6M) 2 (0F, 2M)
2012 Na Na 2 (2F,0M) Na Na
Total 38 (15F, 23M) 14 (9F, 5M) 5 (4F, 1M) 10 (2F, 8M) 14 (4F, 10M)
Table 2. Model estimates for effect of body mass and body size index (mass/tarsus length) on migratory status of males
Model Std.
Error
z value
Pr(>|z|)
Migratory Status ~ Body Mass (kg) 3.004 -0.874 0.382
Migratory Status ~ Body Mass (kg)/ Tarsus Length (mm) 230.307 -0.737 0.461
41
Figure 1. Migration patterns for 8 individual (different colours) tragopans (A). Arrows show direction of movement, and ‘Summer’ and ‘Winter’ denote summer breeding and
wintering grounds. Elevation profiles (B) for 5 tragopans showing the initiation of migration (closed triangle) and end of migration (closed square). Individuals are identified by small letters ‘a’, ‘b’, ‘c’, ‘d’, ‘e’ on both (A) and (B). Temperature profiles are
for October to December 2009 and January 2010 at 2300 (black line) and 2900 (blue line) masl.
42
Figure 2. No of individuals classified as migrants or residents (Pattern 4). Migrants have been further classified into those crossing multiple mountains (Pattern 1), descending longitudinally (Pattern 2) [i.e. travelling parallel to mountain ridges], and those climbing
to higher elevations in winter (Pattern 3). Hatches indicate elevation change by individuals during fall migration. ‘+200’ denotes individuals who climbed higher in winter.
Figure 3. Relationship of body mass (kg) by sex to migratory status, where ‘0’ is sedentary and ‘1’ is migratory. Filled symbols represent birds tagged in 2010 and open
symbols show birds tagged in 2011.
43
Figure 4. Boxplots for distance migrated (A), change in elevation (B) and duration of migration (C) by sex (n=24, females = 11 and males = 13).
44
Figure 5. Departure dates for fall migrations for 2009, 2010 and 2011 (A) and return migrations for 2011 and 2012 (B) against temperature profiles. Dashed horizontal grey
lines (B) show snowfall days in the study area.
(A)
(B)
45
Figure 6. Location of Bhutan (A[i]) and Thrumshingla National Park in Bhutan shown in green (A[ii]). Location of study area bounded by rectangular box (A[ii]). Light grey areas
show protected areas in Bhutan and dark grey areas show biological corridors. Land cover, locations for 1 resident (black circles) and migratory routes for 4 migratory individuals (3 females and 1 male [green squares and line] within the study area (B)). A tagged male (C) and a tagged female (D) being released. Travel route of a male migrant
shown in green and female migrant shown in yellow (B) overlaid onto a photograph of the actual mountain location (E).
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53 Acknowledgements
We are grateful to the International Max-Planck Research School for Organismal Biology and the Max-Planck Institute for Ornithology, Radolfzell for funding this work.
We thank Scott La Point for proof reading the manuscript and providing editorial input.
We are also grateful to two anonymous reviewers for their critique and constructive suggestions.
55
CHAPTER 3 : C omparing Energy Expenditure and Home Range Sizes Using GPS-Accelerometer
Telemetry in A High Altitude Partial Migration System
Nawang Norbu1, 2, 3, Joshua Golberg4, Martin C Wikelski1,2
(Target Journal: Biology Letters)
1 International Max-Planck Research School for Organismal Biology, University of Konstanz, Germany, 2 Max-Planck Institute for Ornithology, Radolfzell, Germany, 3 Ugyen Wangchuck Institute for Conservation and Environment, Lamai Gompa, Bhutan 4 College of Forestry and
Conservation, University of Montana, USA
56
57 ABSTRACT
Tradeoffs in partial migration systems, determining the decision whether to stay or to go, remain poorly understood and the proximate consequences of individual decisions have not been examined in detail. Using accelerometer-enabled GPS telemetry, we investigated differences in energetic status and home range sizes for residents and migrants over a migratory season in a partially migratory population of Stayr Tragopans in the Bhutan Himalayas. Winter home ranges for residents overlapped between
conspecifics and were significantly larger than those of migrants whose home ranges were located at discrete non-overlapping sites. Over the course of the entire migratory season, we did not find significant differences between migrants and residents in energy expenditure as estimated by dynamic body acceleration (DBA). Nevertheless, for
migrants, we observed higher DBA scores and activity states associated with
running/flying and walking during migration. We conclude that an individual’s migratory status does not significantly affect its overall energy expenditure status despite
manifesting differently in terms of space use. This may explain the maintenance of a partial migration system within a relatively small geographic area where the better strategy (i.e. of either being resident or a migrant) could be mediated by fluctuating micro-habitat conditions across time.
INTRODUCTION
Most migration systems are cases of partial migration (Chapman et al. 2011) where only a portion of the population migrates (Lundberg 1988). This is also the case in some
58
altitudinal migrants (Gillis et al. 2008; Boyle 2010; Norbu et al. 2013). Though partial migration is ubiquitous and influences ecosystem functioning (Brodersen, Nicolle &
Nilsson 2011), the ultimate drivers and the proximate consequences in terms of energetic status and home range sizes of individuals remain poorly understood.
The rates at which animals expend energy determine important parameters associated with growth, reproduction and acquisition of food amongst others (Berthold, Gwinner &
Sonnenschein 2003; Brown et al. 2004). As such the allocation of energy budgets has proximate consequences on an individual’s life history with ultimate implications for its fitness. Migration has generally been considered as an adaptive strategy wherein an individual seeks to avoid seasonally difficult conditions by travelling to energetically less challenging areas (Klaassen 2003; Fort et al. 2013). It has also been shown that
conditions at non-breeding sites can influence fitness outcomes at the breeding grounds (Marra, Hobson & Holmes 1998). This assumption may hold true for most long distance latitudinal migrants. However, whether wintering sites are also energetically benign in altitudinal migration systems has not been assessed so far.
Very few studies have quantified the energetic costs (Wikelski et al. 2003) associated with migration and the related costs and benefits of remaining resident or adopting migration (Fort et al. 2013). However, migration is perceived as energetically
demanding and costly for individuals who undertake it (Alexander 1998; Wikelski et al.
2003; Newton 2008), although migrants potentially benefit from access to better quality habitats (Fryxell & Sinclair 1988). Within partial migration systems, it is still not clear as to which strategy (i.e. being a resident or a migrant) provides better fitness outcomes
59
and the possibility of a suite of evolutionary stable strategies to exist has been suggested (Newton 2008).
Amongst other aspects, the energetic status of an individual may depend on food availability and amounts of foraging required (Pyke 1984; Murray 1991). Home range sizes have been shown to correlate with the availability of food (Newton 2008). Also in ungulates, it has been shown that home range sizes are larger where habitat conditions are poor (Mysterud 1999). However, it has also been suggested that territory sizes may not necessarily be regulated by food availability (Adams 2001) and can be influenced by the presence of conspecifics in ways other than by pure food competition. Nonetheless, we presume that home range sizes can have a bearing on the energetic status of
individuals through the extent of movement required to meet foraging needs. It is known that for many (but not all) different foraging guilds, a major portion of an animal’s energy expenditure can be attributed to movement (Alexander 2003; Wilson et al. 2006).
The accurate measurement of movement-related energy expenditure in the wild together with estimation of home range sizes is now possible with accelerometer informed GPS telemetry (Cooke, Hinch & Wikelski 2004; Wilson et al. 2006; Wilson, Shepard & Liebsch 2007; Cagnacci et al. 2010; Brown et al. 2013). Animal-attached accelerometers which measure body acceleration over time can provide proxies of energy expenditure and their reliability as indices for energy expenditure has been demonstrated in a wide range of animals (Halsey & White 2010; Halsey, Shepard &
Wilson 2011; Brown et al. 2013).
