Lactation in Propithecus coquereli in Northwestern Madagascar. Abigail C. ... Adult males had significantly higher cortisol during the earlier lactation stage in.
Maternal Effort, Food Quality, and Cortisol Variation During Lactation in Propithecus coquereli in Northwestern Madagascar
by
Abigail C. Ross
A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Anthropology University of Toronto
© Copyright by Abigail C. Ross, 2017
Maternal Effort, Food Quality, and Cortisol Variation During Lactation in Propithecus coquereli in Northwestern Madagascar Abigail C. Ross Doctor of Philosophy Department of Anthropology University of Toronto 2017
Abstract The duration and quality of the infant care mothers provide is paramount to investigating life history theory. Maternal care is the principal determinant of infant survival and future reproductive success. Lactation is the most energetically expensive activity for mammals, in turn causing lactating females to compensate for drastically greater energy requirements. Lemur reproduction occurs under strict seasonal parameters to cope with harsh climatic conditions. I evaluated maternal behavioral care-giving effort towards infants over 26 postnatal weeks in Coquerel’s sifaka (Propithecus coquereli) (n=10 infants, n=10 lactating females). Secondly, I evaluated the nutritional quality of foods consumed exclusively by lactating females (n=10). Lastly, I examined stress responses across sex and reproductive classes in earlier (weeks 1-12) versus later lactation (weeks 13-24) (n=10 lactating females, n=19 adult males, n=8 non-lactating adult females). I conducted fieldwork over two consecutive birth seasons (2010 and 2011) in Ankarafantsika National Park located in northwestern Madagascar. Earlier lactation occurs during the austral winter, and coincides with the seasonally driest time of the year. I quantified maternal care-giving by measuring infant transport position, carrier identity, and bodily contact. Nutritional food quality was measured by protein, fiber, energy (n=123), and mineral content (n=119). I quantified stress responses to determine how sex and reproductive classes respond to seasonal pressures and lactation by measuring cortisol variation in two lactation stages in ii
lactating females (n=180), adult males, (n=133), and non-lactating adult females (n=62). Infants were more altricial relative to other lemurs of similar body size. Allomaternal care was documented, although mothers were the primary infant transporters. Lactating females most frequently selected foods high in non-protein energy, and regularly selected foods high in available protein and fiber. Lactating females had lower cortisol relative to adult males that approached statistical significance, and significantly lower cortisol than non-lactating adult females. Adult males had significantly higher cortisol during the earlier lactation stage in comparison to the later stage. Understanding the behavioral, nutritional, and endocrinological responses of lactating females provides a comprehensive view of how maternal energetics, infant care, and infant development are dynamically performing during the most energetically constraining time of year in a stochastic environment.
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Dedication To my exceptional father, Bill Ross (1950-2016)—a natural born world shaker.
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Acknowledgments “Words are like eggs: when hatched, they have wings.” “Ny teny toy ny atody: raha foy manana elatra.” ~ Malagasy proverb
Stumbling through all the theoretical, logistical, and statistical tribulations of a PhD program has been a tremendous and an exhilarating challenge. The country of Madagascar is an enchanting and mythical place, though can be frustrating and difficult to traverse. When I was covered in bug bites, weary from chasing sifakas, longing for a hot shower, and ready to jump on the next taxi brousse out of Ampijoroa to feast on a cheeseburger and an ice-cold beer; I would experience a magnificently beautiful thing in the forest, hear booming laugher in the village, or smell the ylang-ylang blossoms before dawn. This is Madagascar to me: the grittiest, yet most rewarding place I have ever been. The memory fills me with a deep, quiet satisfaction. Madagascar can be a sorrowful place, plagued by extreme poverty and disease, ravaged by political and economic instability, and the relentless destruction of its environment. But, it is also filled with a penetrating, vibrant richness and depth. I feel a tugging from within when I think of Madagascar, its people, and its lemurs. It will bring me back. Thank you to the Coquerel’s sifaka groups that let me join and share in their world: Citron (village of Ampijoroa), Fito (seven), Iva (low), Kambana (twins), Mainty (black), Rambo (tail), Vaovao (news), Volo (hair), and Zaza (baby). Your lessons are invaluable to me, both as a scientist and human, and I continue to learn from our time together in the forest.
More organizations and people in Madagascar contributed to this dissertation than I ever could have imagined. I thank the Madagascar Institute for the Conservation of Tropical Environments (MICET) for their logistical assistance ranging from acquiring export permits to finding a FedEx in Antananarivo where I could ship my biological samples. MICET welcomed me amiably into their country and provided tremendous backing throughout my project. My dissertation would not have been possible without their expertise. I thank the director of MICET, Benjamin Andriamihaja, for his gracious support. I also thank Tiana, Benji, Jean, Aja, Iton, Silvan, and David at MICET for their assistance and logistical support.
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I sincerely thank my field assistant, Ravalohery Fara Nomena, for her diligent commitment to the project for 14 months. Nomena and her family welcomed me into their home in Itaosy. Nomena proved invaluable in countless ways and I feel incredibly lucky to have worked with her. Nomena is much more than an excellent field assistant; she is my colleague, close friend, interpreter, and cultural liaison. I admire her patience and skill collecting behavioural data. Nomena’s witty humor never failed to make me laugh and I always enjoyed our conversations in the forest. I owe the success of the project to her perseverance and look forward to working alongside her in the future.
Thank you to Randrianjaka (Njaka) Frankin for his devotion to the project as my park guide for 14 months. Njaka has an amazing ability to find sifakas in the forest and went far beyond the call of duty to help both Nomena and myself. He was never late once during the entire project. In fact, I remember Njaka calling my name from outside the tent to wake me up after sleeping through my alarm on several occasions. Njaka’s wife was pregnant with their second child and I recall communicating to him through a series of hand gestures and terrible Malagasy-English to take time off when the baby was born. Nomena chimed in to clarify and Njaka just smiled, shaking his head. Months later, he received a phone call while we were following a sifaka group in the forest to say that his wife was in labor. He told me that he would finish his work for the day and then go see his wife in Ambohimanga, the adjacent village to Ampijoroa. He was back working the next morning. He climbed the trees to collect my plant samples and learned the local tree names from his father, Zama, and other park guides. Chapter 3 would not have been possible with him. Njaka takes tremendous pride in everything he does, including my project and I will forever be grateful for his hard work.
Thank you to Ang and her family for providing nutritious food every day for Nomena, Njaka, and myself. Ang’s kind smile greeted us each morning with hot coffee gave us the energy we needed before heading into the forest. Ang gave us hardboiled eggs for breakfast every Sunday and even delivered potage to my tent when I sick.
Thank you to Madagascar National Parks, Ankarafantsika National Park, Ministere de l’Environnement et des Forets, Ecole Normale Supérieure, Parc Zoologique et Biologique de Tsimbazaza, and Missouri Botanical Gardens. These organizations granted me permission to vi
conduct research in their country and helped me navigate through Madagascar. The assistance of each organization was paramount to the execution of my project on the ground. A special thank you to Lalao Andriamahefarivo, Herisoa Manjakahery, and Faranirina Lantoarisoa at Missouri Botanical Gardens in Antananarivo for their help exporting my plant samples.
I sincerely thank Rakotondradona Remi, Director of Ankarafantsika National Park, for his support of my project. Thank you to Razaiarimanana Jacqueline and Rakotoarimanana Justin for their assistance and daily problem-solving skills. Ankarafantsika National Park was a wonderful place to work and call home because of the support from each of you. Thank you, Travis Steffens, Keriann McGoogan, Kim Valenta, Sharon Kessler, Danielle Levesque, Alida Hasiniaina, and Razafitsalama Mamy for your friendship and remarkable support in the field. We shared many incredible experiences together in a short time, and I am fortunate to have gained lifelong friends and colleagues.
Thank you to my supervisor Dr. Shawn Lehman for his academic and personal support during the last eight years. Shawn offered guidance and help when I needed it, but perhaps most importantly, he gave me the freedom to construct and implement my own project. Shawn taught me how to be an independent field scientist and trusted in my abilities even when I did not. His confidence in me instilled confidence in myself. Shawn went to bat for me on numerous occasions; his loyalty and dedication to his students is exceptional.
Thank you to the Smithsonian Conservation Biology Institute, Conservation Ecology Center, Nutrition Lab, National Zoological Park for allowing me to visit your lab for a summer. An enormous and gracious thank you to Dr. Mike Power. I first met Mike in 2007 when he graciously invited me to his lab to assay Goeldi’s monkey milk. I have been under his wing since that time. I have gained an incredible arsenal of knowledge from his expertise. Mike is an exceptional scientist and an extraordinary person to learn from. His tenacity is inspiring and his enthusiasm for science is infectious. Mike enjoys chatting with students, and continually blows my mind with his impromptu remarks about nutritional science. I am brimming with new ideas, reevaluating old thoughts, and delving into new topics of inquiry after every one of our conversations.
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I thank Dr. Joyce Parga for her assistance constructing my ethogram and extremely helpful suggestions for collecting behavioural data. I found Joyce’s approachability and encouragement so warm when I entered the Ph.D. program. Her courses and frequent emails tremendously expanded my knowledge of lemur reproduction and were essential to the formation of chapter 2. She continues to be a great mentor. I wish her happiness and success in Los Angeles.
Thank you to my committee members: Drs. Julie Teichroeb, Michael Schillaci, Rebecca Stumpf, and Becky Raboy for their revisions and thoughtful insight from the conception of my project to its conclusion. You each challenged the parts of my dissertation that needed more attention. Your contributions significantly improved all my chapters, my ability to think as a scientist, and will make future publications more successful.
Thank you, Michael, Jakubasz and Michael Maslanka at the Department of Nutrition, Smithsonian National Zoological Park. Your assistance started in Madagascar during the shipment of my samples and continued through my lab visit. I truly value my experience at the nutrition lab and gained an instrumental skill set because of your knowledge and thoughtful teaching. Thank you to Dr. Christina Petzinger for your assistance with my plant samples. You were a great resource for me in the lab and taught me a great deal about nutritional assays. A colossal thank you to the nutrition lab interns: Dr. Cari Lewis, Nicole Johnson, Jessica Cooper, Katie Murtough, and DaeKyu Lee. Your hard work and countless hours spent in the lab were profoundly appreciated. The meticulousness and perseverance with which you approached my nutritional assays extended far beyond your responsibilities and demonstrated true passion.
Thank you to Dr. Toni Ziegler, the Wisconsin National Primate Research Center, and Assay Services for acquiring my import permits, opening your lab to me, and conducting my cortisol assays. A very special thank you to Dan Wittwer for teaching me how to run the cortisol assay from start to finish. My first day in the lab Dan asked if I knew the difference between a beaker and a graduated cylinder; and when I responded, “Uh,” Dan knew he had his hands full. Dan is a delightful, easygoing teacher and an absolute pleasure to learn from. His sarcastic humor sustained me while hand grinding 412 fecal samples. He was determined to teach me how to successfully use a multichannel pipette, even after several failed attempts. Toni and Dan
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continued to answer questions long after I left the lab. Their immense dedication to the success of my cortisol assays will always be remembered.
Thank you to my incredible parents, Bill Ross (1950-2016) and Sue McCausland, for their unyielding love and support. You both taught me to reach for the stars, and to always follow my heart. I am lucky enough to still believe that anything is possible because of your parenting. Thank you for letting me play in the mud and eat boxelder bugs. I would not have discovered my passion for animals and the outdoors without your guidance. Dad, one of the last things you told me was how proud you were. I miss you always. I know as I write these words that your advice to me now would be: take it easy, and just be happy.
Erik, you are an endless source of love and support. Your steadfastness and perceptivity in all things lifts me. Thank you. From going to the Sadie Hawkins dance senior year of high school together, it took travelling half away around the world for us to find each other again.
Thank you to my little sister, Caitlin Ross, for always having my back. You are the best teacher I know. I hope that I can motivate and inspire students in the way you do. Thank you to my grandparents, Ed and Renee Ross (1921-2015). Your support over the years enabled me to pursue my passions. I am forever grateful. Thank you to Bob Lund for always lending an ear. Your esteemed insight has been, and continues to be, a vital influence in my individual and professional development. Thank you to Ron and Vickie Lund for your support, encouragement, and kind words that prevailed even during the toughest of times. Thank you to my dear friends Lisa Fischer, Melisa Smith, Jenny Kalousek, Ellie Pedersen, and Kate Nash for believing in me, providing much needed comic relief, and giving me perspective. I am lucky to have each of you in my life. Thank you to my three furry felines, Miel “Big Boy Roy” (2004-2014), Macko, and Baloo for their companionship and affection during the many hours spent on the computer.
I sincerely thank Drs. Leila Porter, Dan Gebo, and Mitch Irwin. Leila was my M.A. supervisor and Dan was on my thesis committee at Northern Illinois University. Leila and Dan prepared me for the rigors of a Ph.D. program, and continued to lend an ear when I moved back home to Rockford, Illinois to write my dissertation. Leila’s gentle way of teaching opened the discipline of Biological Anthropology to me. She is a remarkable person and mentor. Leila helped me ix
pinpoint my research interest in maternal-infant relationships. Her patient and nurturing way of engaging with students while being a compelling and scrupulous professor is an unmatched combination of traits I have encountered in academia. I truly admire Leila’s teaching style and it is my aim to exemplify what I learned from her moving forward in my career. Dan’s challenging courses were invigorating and innovative and developed my critical thinking and writing skills. His leadership encouraged me to apply for Ph.D. programs. Thank you, Dan, for offering to listen to apprehensions I had during my writing stage. Leila and Dan were both integral to my development as a graduate student and transition into becoming a professional primatologist. Thank you to Mitch for being my lemur mentor close to home. Your thoughts and guidance have been immensely valuable.
Thank you to Bill Buhl, my incredible high school biology teacher who first sparked my interest in science. Bill invited me to join his class trip to the Galápagos Islands when I was an undergraduate living in Madison. It was on that trip where I decided I would major in Anthropology. I am indebted to Bill for his encouragement throughout the years.
Thank you to my funding agencies for their generous contributions, including the Department of Anthropology and the Department Graduate Fellowships and Awards Committee Research Funds- University of Toronto, School of Graduate Studies Research Travel Grant- University of Toronto, Primate Conservation, Inc. Research Grant, American Society of Primatologists Conservation Committee Small Grant, The Explorers Club Exploration Fund, Edward and Renee Ross Charitable Foundation, Department of Anthropology Fellowship- University of Toronto, Faculty of Arts and Sciences Fellowship- University of Toronto, and support from S. Lehman's NSERC.
Thank you to the University of Toronto for providing a vivacious community in which to learn and an exceptional, enriching academic atmosphere. Thank you to the statistical consulting service at Northern Illinois University for their patience and mathematical wizardry with chapters 2 and 4. Thank you to digital cartographers, Erik Lund and Charlie Lunn, of Rockford Map Publishers for their ardent interest in nature that inspired them to create all the maps used in my dissertation. The maps were an integral component to my project and will be continue to be valuable to future research in Ankarafantsika National Park. x
Table of Contents Abstract
ii
Dedication
iv
Acknowledgments
v
Table of Contents
xi
Chapter 1: Introduction
1
1.1. Influences on animal life histories
1
1.1.2. Inherited environmental effects model
1
1.1.3. Maternal and allomaternal care
2
1.1.3.1. Lactation
4
1.2. Strepsirhines
5
1.2.1. Strepsirhine phylogeny
5
1.2.2. Conservation research justification
6
1.2.3. Propithecus spp. socioecology
7
1.2.3.1. Infant mortality
8
1.2.3.2. Seasonality in dry deciduous forests
9
1.3. Maternal effects model
9
1.4. Dissertation objective
10
1.4.1. Research hypothesis
11
1.5. Maternal behavioral care-giving background
11
1.5.1. Female social dominance
11
1.5.2. Basal metabolic rates during reproduction
12
1.5.3. Infant growth rates
12
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1.5.4. Maternal body mass
13
1.5.5. Lactation and phenotypic plasticity
14
1.5.6. Infant behavior research justification
14
1.6. Maternal behavioral care-giving predictions
15
1.7. Nutritional food quality background
15
1.7.1. Propithecus spp. diet
16
1.7.2. Protein-to-fiber ratios
17
1.7.3. Gross energy
18
1.8. Nutritional food quality predictions
18
1.9. Stress response background
19
1.10. Temporal cortisol variation predictions
19
1.11. Dissertation overview
20
1.12. References
24
Chapter 2: Maternal Effort in Propithecus coquereli in Ankarafantsika National Park, Northwestern Madagascar
30
2.1. Abstract
30
2.2. Introduction
31
2.3. Methods
36
2.3.1. Study site and species
36
2.3.2. Data collection
38
2.3.3. Sampling methods
39
2.3.4. Data analysis
40
2.4. Results
41
2.4.1. Infant transport position: Ventral
41
2.4.2. Infant transport position: Dorsal
42
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2.4.3. Infant transport position: Independent
42
2.4.4. Comparison of infant transport positions from 1-26 weeks postnatal
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2.4.5. Infant carriers
43
2.5. Discussion
46
2.6. Author note on publication
53
2.7. References
54
Chapter 3: Nutritional Food Quality of Foods Exclusively Selected by Propithecus coquereli Lactating Females
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3.1. Abstract
87
3.2. Introduction
88
3.3. Methods
95
3.3.1. Study site and species
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3.3.2. Botanical and biotic variable collection
96
3.3.3. Botanical processing and preservation
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3.3.4. Macronutrient and micronutrient assays
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3.3.5. Laboratory drying and grinding
98
3.3.6. Crude protein determination
99
3.3.7. Neutral detergent fiber and acid detergent fiber determination
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3.3.8. Total mineral (ash)
100
3.3.9. Gross energy determination
100
3.3.10. Data analysis
100
3.4. Results
101
3.4.1. High available protein foods: Cluster 1
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3.4.2. High fiber foods: Cluster 2
101
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3.4.3. High non-protein gross energy foods: Cluster 3
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3.4.4. Mineral (ash) content
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3.4.5. Frequency of ingestion index
102
3.5. Discussion
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3.5.1. High available protein foods: Cluster 1
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3.5.2. High non-protein gross energy foods: Cluster 3
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3.5.3. High fiber foods: Cluster 2
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3.6. References
111
Chapter 4: Cortisol Variation Across Sex and Reproductive Classes in Propithecus coquereli
131
4.1. Abstract
131
4.2. Introduction
131
4.3. Methods
138
4.3.1. Study site and species
138
4.3.2. Fecal collection and preservation
140
4.3.3. Dried feces sample preparation
141
4.3.4. Cortisol steroid extraction and recovery
141
4.3.5. Cortisol steroid validation
141
4.3.6. Enzyme immunoassays (EIA)
142
4.3.7. Data analysis
142
4.4. Results
143
4.4.1. Lactating females
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4.4.2. Adult males
144
4.4.3. Non-lactating adult females
144
4.4.4. Comparison across sex/reproductive classes
144
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4.5. Discussion
145
4.6. References
152
4.7. Appendix
170
Chapter 5: Conclusions and Future Directions
180
5.1. Theoretical significance
180
5.2. Summary of findings
181
5.3. Future directions of study
189
5.4. Conservation implications
191
5.5. Evolutionary implications
195
5.6. References
197
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List of Tables Chapter 1: Introduction
1
Table 1.1. Gross milk composition in mammals
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Table 1.2. Gross milk composition in primates
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Chapter 2: Maternal Effort in Propithecus coquereli in Ankarafantsika National Park, Northwestern Madagascar
30
Table 2.1. P. coquereli group size and composition including infants season 1
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Table 2.2. P. coquereli group size and composition including infants season 2
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Table 2.3. P. coquereli focal data collection columns
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Table 2.4. P. coquereli ethogram
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Table 2.5. P. coquereli behavioral focal hours
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Table 2.6. P. coquereli infant birth months
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Table 2.7. Mixed effects linear regression comparison of infant position
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Table 2.8. Mixed effects linear regression comparison of infant carrier identity
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Table 2.9. Poisson regression considering number of occurrences mothers initiated and broke infant contact
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Table 2.10. Poisson regression considering number of occurrences infants initiated and broke mother contact
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Chapter 3: Nutritional Food Quality of Foods Exclusively Selected by Propithecus coquereli Lactating Females
87
Table 3.1. Identification of assayed foods selected by lactating P. coquereli
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Table 3.2. Available protein, neutral detergent fiber (NDF), acid detergent fiber (ADF), non-protein gross energy (NPGE), and mineral (ash) values of foods selected by lactating P. coquereli
120
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Table 3.3. Nutrient profile of high available protein foods consumed by lactating P. coquereli
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Table 3.4. Nutrient profile of high neutral detergent fiber (NDF) foods consumed by lactating P. coquereli
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Table 3.5. Nutrient profile of high acid detergent fiber (ADF) foods consumed by lactating P. coquereli
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Table 3.6. Nutrient profile of high non-protein gross energy foods consumed by lactating P. coquereli
127
Table 3.7. Nutrient profile of minerals (ash) in foods consumed by lactating P. coquereli
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Table 3.8. Frequency of ingestion index (FOI)
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Chapter 4: Cortisol Variation Across Sex and Reproductive Classes in Propithecus coquereli
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Table 4.1. P. coquereli fecal samples collected by individual sex/reproductive class and data collection season
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Table 4.2. Comparison of cortisol in P. coquereli by individual sex/reproductive class and lactation phase from 1-24 weeks postnatal
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Table 4.3. Comparison of cortisol in P. coquereli by individual sex/reproductive class from 1-24 weeks postnatal
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Table 4.4. Mixed effects linear regression of cortisol in P. coquereli by individual sex/reproductive class and lactation phase from 1-24 weeks postnatal
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Table 4.5. Mixed effects linear regression estimates of cortisol in P. coquereli by individual sex/reproductive class and lactation phase from 1-24 weeks postnatal
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Table 4.6. Comparison of P. coquereli fecal cortisol and P. verreauxi fecal corticosterone
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Chapter 5: Conclusions and Future Directions
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180
List of Figures Chapter 1: Introduction
1
Figure 1.1. Inherited environmental effects model: components of offspring phenotype Chapter 2: Maternal Effort in Propithecus coquereli in Ankarafantsika National Park, Northwestern Madagascar
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30
Figure 2.1. Ankarafantsika National Park, northwestern Madagascar
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Figure 2.2. Percentage of time P. coquereli infants spent ventrally on all carriers
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Figure 2.3. Percentage of time P. coquereli infants spent dorsally on all carriers
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Figure 2.4. Percentage of time P. coquereli infants spent independently
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Figure 2.5. Percentage of time P. coquereli infants spent ventrally, dorsally, and independently
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Figure 2.6. Percentage of time P. coquereli infants spent carried by mothers
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Figure 2.7. Percentage of time P. coquereli infants spent carried by adult males
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Figure 2.8. Percentage of time P. coquereli infants spent carried by adult females
80
Figure 2.9. Percentage of time P. coquereli infants were transported by mothers, adult males, adult females, and independent
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Figure 2.10. Occurrences of infant contact initiated by P. coquereli mothers
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Figure 2.11. Occurrences of infant contact broken by P. coquereli mothers
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Figure 2.12. Occurrences of mother contact initiated by P. coquereli infants
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Figure 2.13. Occurrences of mother contact broken by P. coquereli infants
85
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Figure 2.14. Occurrences of infant contact initiated/broken by P. coquereli mothers and mother contact initiated/broken by infants Chapter 3: Nutritional Food Quality of Foods Exclusively Selected by Propithecus coquereli Lactating Females Figure 3.1. Ankarafantsika National Park, northwestern Madagascar Chapter 4: Cortisol Variation Across Sex and Reproductive Classes in Propithecus coquereli
86
87 130
131
Figure 4.1. The hypothalamic-pituitary-adrenal (HPA) axis, negative feedback response to chronic and acute stress, and effects of stressors on bodily processes
162
Figure 4.2. The biological response of animals to stress
163
Figure 4.3. Ankarafantsika National Park, northwestern Madagascar
164
Figure 4.4. Cortisol concentrations in P. coquereli lactating females
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Figure 4.5. Cortisol concentrations in P. coquereli adult males
166
Figure 4.6. Cortisol concentrations in P. coquereli adult non-lactating females
167
Figure 4.7. Average cortisol in P. coquereli by sex/reproductive class
168
Figure 4.8. Cortisol comparison across sex/reproductive classes and lactation phases
169
Chapter 5: Conclusions and Future Directions
xix
180
List of Appendices Appendix 1 P. coquereli fecal field collection and cortisol concentrations
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170
Chapter 1 Introduction “All who live under the sky are woven together like one big mat.” “Tsihy be lambanana ny ambanilantra.” ~ Malagasy proverb
1.1. Influences on animal life histories Life history studies investigate individual variation in genotypic and phenotypic fitness through adaptations and constraints (Stearns 1992). Darwinian natural selection causes evolutionary changes in populations and produces adaptations. Adaptations allow an organism to survive and reproduce in its environment. “An organismal character constitutes an adaptation if it performs a function that is of utility to the organisms possessing it and if the character evolved by natural selection for that particular function” (Larson and Losos 1996, p. 187). Constraint is defined as a phylogenetically dependent state where each developmental stage hinges on the previous stage (Oster and Alberch 1982). Non-human primate life history models are predominately constructed using climatically stable or cyclic environments and have not considered the evolutionary responses or adaptive processes at work in erratic environments like Madagascar, where unpredictable intra- and inter-annual rainfall results in irregular and highly seasonal food abundance and distribution (Dewar and Richard 2007; Dunham et al. 2011; Wright 1999). Consequently, life history models are not designed for stochastic environments and maternal behavioral and ecological responses to stochastic environments are not represented in contemporary life history theory.
1.1.2. Inherited environmental effects model Inherited environment effects are defined as, “components of an offspring’s phenotype that are derived from the parent, apart from nuclear genes” (Rossiter 1996, p. 451). Thus, inherited environmental effects result from a combination of intrinsic and extrinsic factors, including parental environment, and interactions between parental environment and parental genotype (Rossiter 1996). Inherited environmental effects are represented in abiotic, nutritional, and a variety of other ecological characteristics occurring in the parental environment (Rossiter 1996). For example, food quality and other seasonal features (e.g., hormonal stress responses) are 1
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environmental variables that contribute to inherited environmental effects (Rossiter 1996). These variables are permanent components of species’ environments, and thereby reflective of ecological and evolutionary processes at work (Rossiter 1996). Distinguishing inherited genotypic effects from observable phenotypic effects is problematic because a multitude of interrelated factors selectively act on offspring success (Lacey 1998; Rossiter 1996). The inherited environmental effects model is derived from a genetics model of inherited environmental effects, with the inclusion of offspring environmental variability (Eisen and Saxton 1983), and further addition of variability within the parental environment; thus comprising a comprehensive model of the genotypic and phenotypic effects selecting on offspring phenotype (Rossiter 1996) (Figure 1.1). My dissertation primarily addresses parental performance phenotype (source 4; Figure 1.1) (measured by maternal behavioral care-giving effort and temporal variation in cortisol concentrations across sex and reproductive classes); and parental environment (source 5, Figure 1.1) (measured by the nutritional food quality of foods consumed by lactating females). Inherited environment effects select on offspring phenotype by the, “contribution of the parental performance phenotype to offspring phenotype due to parental performance genotype; contribution of the parental environment; interaction between parental and offspring environment; interaction between parental environment and offspring genotype; and covariance between parental performance genes expressed in the parental and subsequent generations” (Rossiter 1996, p. 454-55) (see sources 4-8, Figure 1.1).
1.1.3. Maternal and allomaternal care Maternal care behavior is defined as the amount of time mothers engage in infant care-giving, and the quality and duration of this care (Pryce 1995). Parental investment in their offspring is a function of balancing maternal reproductive costs while maximizing infant care and survivability without impeding future female reproductive success (Trivers 1974). The typical, albeit not universal, mammalian parental investment pattern shows a positive correlation between body mass and reproductive function, which is often used to quantify maternal health (Clutton-Brock 1991; Dobson and Michener 1995; Lewis and Kappeler 2005b; Richard et al. 2000). Other proxies used to determine maternal health include hormonal stress responses (see Abbott et al. 2003; Bales et al. 2005; Beehner and McCann 2008; Boonstra et al. 1998; Brockman et al. 1998; Brockman et al. 2009; Busch and Hayward 2009; Casolini et al. 1997; Creel et al. 2002; Gould et al. 2005; Ostner et al. 2008; Saltzman and Abbott 2009; Setchell et al. 2008), and the nutritional
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quality of foods consumed by mothers also reflect maternal health and are effective temporal measures of how mammals respond to their environments (see Burgess and Chapman 2005; Chapman et al. 2003; Ganzhorn 2002; Gould et al. 2011; Milton 1979; Norscia et al. 2006; Sauther and Cuozzo 2009). Mammalian maternal care is unique in that milk is the exclusive nutritional source available to infants until the introduction of solid foods, thereby requiring mothers to participate in care-giving for varying, though comparatively long, durations relative to other animal classes (Clutton-Brock 1991).
Maternal care is augmented with allomaternal care in some primate taxa (Hrdy 1976). Allomaternal care is an assortment of different behaviors used by non-mothers, in part, to reduce the energetic burden on lactating females (Ross and MacLarnon 2000). These behaviors can be divided in three broad categories: infant transport, babysitting, and energy transfer (reviewed in Tecot et al. 2013). The presence of allomaternal care is prevalent in the order Primates, though the form and frequency of allomaternal care is decidedly variable across taxa (Ross and MacLarnon 2000). Allomaternal caregivers are defined as nonbreeding (e.g., juveniles) or reproductive individuals that decide to expend energy on infants other than their own (Solomon and French 1997). Allomaternal care is typically thought to be adaptive to both mothers and caregivers, but it also poses risks. For example, infants may be injured due to mishandling by inexperienced caregivers, nursing time may be reduced, or mothers may decrease time spent foraging to increase vigilance while other caregivers are watching infants (reviewed in Tecot et al. 2013). Given these potential risks, the benefits of allomaternal care must be considered high for species to partake and include: shorter interbirth intervals, faster infant growth, improved predator protection for infants, thermoregulation, and increased breeding opportunities for males (reviewed in Tecot et al. 2013). Allomaternal may be particularly advantageous in difficult environments such as Madagascar (Wright 1999), where alleviating energetic stress may have immediate benefits for mothers and infants in times of extreme environmental instability. There is evidence of allomaternal care in numerous lemur taxa, though longitudinal data is severely lacking, including: fat-tailed dwarf lemur (Cheirogaleus medius), black lemur (Eulemur macaco), mongoose lemur (Eulemur mongoz), red-bellied lemur (Eulemur rubriventer), eastern lesser bamboo lemur (Hapalemur griseus), ring-tailed lemur (Lemur catta), silky sifaka (Propithecus candidus), diademed sifaka (Propithecus diadema), golden-crowned sifaka (Propithecus tattersalli), Verreaux’s sifaka (Propithecus verreauxi), and Coquerel’s sifaka
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(Propithecus coquereli). In contrast to previous studies focused on haplorhines, there was no relationship found between allomaternal care and faster infant growth or shorter interbirth intervals in a comparative phylogenetic study of 23 lemur species (Tecot et al. 2012). Infant parking and nesting were related to faster life histories, as parking and nesting both positively correlated with fetal and postnatal growth rates (Tecot et al. 2012). The authors of this study suggest that lemurs may have already reached maximal growth rates, and decreased interbirth intervals may not increase rates of reproduction given that lemurs are strict seasonal breeders (Wright 1999, Tecot et al. 2012). It is likely that ecological variables (e.g., food quality and abundance) influence the expression of allocare in lemurs.
1.1.3.1. Lactation Lactating mothers represent a unique study opportunity because lactation is the single most energetically expensive activity in which mammalian mothers engage (Tardif 1994). In the case of some primates, the twofold cost of carrying infants while simultaneously lactating further amplifies this already high energetic cost (Bales et al. 2000; Tardif 1994). The exact selective pressures involved in the origin and evolution of mammalian lactation have not been identified (Sellen 2009), although the emergence of lactation as an exclusively mammalian strategy has undoubtedly caused the emergence of life history traits and evolved parental-infant relationships unique to mammals (reviewed in Dall and Boyd 2004). Within mammals, the Primates Taxonomic Order is distinguished by exceptionally extended life history traits including prolonged gestation length, reduced litter size, and delayed infant independence. Primate lactation strategies are characterized by extended length and frequency of nursing, and large milk volume (Oftedal 1984; Power et al. 2002). Milk is composed of dry matter (total solids), fat, protein, sugars, and ash (minerals). Early lactation is distinguished by changing milk composition prior to mid-lactation, and includes colostrum and transitional milk (Oftedal and Iverson 1995). Mid-lactation is operationally defined as the period of maximal lactation performance, and is more energetically constraining than early and late lactation (Iverson and Oftedal 1995). Late lactation is characterized by declining milk yields and mixed feeding, where infants are simultaneously consuming solid foods and milk (Iverson and Oftedal 1995). The nutrient composition of mammalian milk is exceedingly variable (Table 1.1), with primates generally producing relatively low quality, dilute milks in comparison to other mammals (Oftedal 1984; Power et al. 2002; Tardif et al. 2001; Tilden and Oftedal 1997). Dilute milk has
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high water content, thereby having high sugar and low fat and energy content (M. Power, pers. comm.). Fat is the most variable nutrient, ranging from 0.2% in black rhinos (Diceros bicornis) to 60% in hooded seals (Cystophora cristata) (reviewed in Iverson and Oftedal 1995).
Milk nutrient composition is influenced by divergent infant behavioral care strategies (Tilden and Oftedal 1997). Dilute milk is typically found in genera with continual nipple access with infants that suckle frequently in comparison to higher fat, energy dense milks found in genera with less frequent nipple access (Ben Shaul 1962; Oftedal and Iverson 1995). Even though primates typically have dilute milk, there is significant variation in milk nutrient composition between closely related genera, most notably between lemurs and lorises, that is unrelated to body mass (Table 1.2) (Tilden and Oftedal 1997). Infants have restricted nipple access when they are “parked” and left alone in comparison to infants that are continually carried and therefore ingest a greater milk volume per suckling bout while suckling less frequently, in turn requiring more energy dense milk opposed to carried infants that ingest smaller volumes of dilute milk more frequently (Table 1.2) (Tilden and Oftedal 1997). Infants habitually nurse (and have easier access to nipples) in the ventral position compared to the dorsal position (reviewed in Tecot et al. 2013), though this measure cannot be used as a reliable measure of milk intake since young infants may not suckle while in the ventral position (Cameron 1996).
1.2. Strepsirhines 1.2.1. Strepsirhine phylogeny Madagascar reached its current geographic position 430km east of Mozambique approximately 120 million years ago (MYA), and separated from the Indian subcontinent between 80-90 MYA (Masters et al. 2006). The majority of wildlife in Madagascar evolved under geographically isolated conditions, thereby resulting in exceptionally high numbers of endemic taxa. Estimates of species richness reveal that 92% of vascular plants, excluding ferns, and 84% of land vertebrates are endemic to the island (Goodman and Benstead 2005). The Primates Order is divided into two taxonomic suborders, the Strepsirhini and Haplorhini. Phylogenetic evidence demonstrates the Strepsirhini and Haplorhini clades spilt 87 MYA (Perelman et al. 2011). Within Strepsirhini, the ancestors of Lemuriformes (Malagasy lemurs) / Chiromyiformes (Malagasy aye-aye) and Lorisiformes (lorises, galagos, pottos) spilt 68.7 MYA, with the origins
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of these infraorders estimated at 58.6 MYA and 40.3 MYA, respectively (Perelman et al. 2011). There are four taxonomic families of Lemuriformes found singularly in Madagascar: Cheirogaleidae, Lepilemuridae, Lemuridae, and Indriidae. Lemuriformes first evolved 38.6 MYA, and remain partially phylogenetically unresolved due to current taxonomic debates at the subspecific level (Perelman et al. 2011). Chiromyiformes are represented by the single genus Daubentonia, and diverged from a common Lemuriformes ancestor (Perelman et al. 2011). Considering the four families within Lemuriformes, the Lemuridae emerged first, and subsequently the Indriidae, with a monophyletic lineage spilt that occurred 32.9 MYA, and resulted in the formation of the two sister lineages Lepilemuridae and Cheirogaleidae (Perelman et al. 2011). Indriidae contains three genera: Indri, Avahi, and Propithecus. Within Propithecus, the diademed sifaka (Propithecus diadema) is the eastern geographic type and Verreaux’s sifaka (Propithecus verreauxi) is the western geographic type, with the P. verreauxi clade subsequently splitting into verreauxi-deckeni-coronatus in southwestern Madagascar and the coquerelitattersalli clade in the northwest (Mayor et al. 2004; Pastorini et al. 2001). Previous studies of Coquerel’s sifaka (Propithecus coquereli) in Ankarafantsika National Park (ANP) (Richard 1974; Richard 1976; Richard 1978; Richard 1985; Richard 1987) classified it as P. verreauxi prior to the taxonomic elevation of P. coquereli to a separate species (Mayor et al. 2004).
1.2.2. Conservation research justification There has been an 80% reduction of forested habitats during the last 50 years in Madagascar (Harper et al. 2007). Dry deciduous forests are one of the most degraded biomes in the world as a result of large-scale logging operations (Ganzhorn et al. 2001). Only 3% of dry deciduous forest cover remains in Madagascar and ANP is one of the largest existing deciduous forest blocks (Ganzhorn et al. 2001; Smith 1997). Unregulated use of natural resources in the forms of slash-and-burn agriculture, hunting, logging, fuel wood collection, and seasonal dry forest burning for cattle pasture coupled with rapid population growth are the primary causes of deforestation in Madagascar (Kull 2000).
P. coquereli is classified as an endangered species on the International Union for Conservation of Nature (IUCN) Red List. This lemur is confined to two protected areas in northwest Madagascar, the Bora Special Reserve and ANP. The highest P. coquereli densities occurring in the dry deciduous forests of Ankarafantsika region (Mittermeier 2010). An estimated population
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of approximately 47,000 P. coquereli currently live in ANP (Kun-Rodrigues et al. 2014). Density estimates range from 5-100 individuals/km2, with habitat quality (i.e., negative effects of roads and forest edges) as the principal factor for this high variability (Kun-Rodrigues et al. 2014). An estimated 5 individuals/km2 presently exist in Ampijoroa (Kun-Rodrigues et al. 2014), in comparison to an estimated 60-75 individuals/km2 in the 1980s (Albignac 1981). Ampijoroa is a village within ANP and includes its surrounding regions. This is a rapid decrease of more than 90% of the P. coquereli population in Ampijoroa during the last 30 years (KunRodrigues et al. 2014). Hunting pressure on P. coquereli have increased dramatically during recent years in ANP because their relatively large body size produces greater protein yields relative to other sympatric lemurs (Gerardo and Goodman 2003). Adult P. coquereli weigh between 3.7-4.3kg, with a head-body length of 42-50cm, and total length of 93-110cm (Kappeler 1991; Ravosa et al. 1993; Tattersall 1982). Additionally, human migration influxes have decreased protection previously provided by region-specific food taboos (Gerardo and Goodman 2003).
1.2.3. Propithecus spp. socioecology Propithecus spp. social groups are flexible in terms of composition and size, with the average size ranging between five to six individuals (Kubzdela 1997; Lewis and van Schaik 2007; Richard 1974; Richard 1985). Larger numbers of Propithecus females in social groups increases feeding competition while negatively influencing reproduction (Kubzdela 1997). Social relationships between males in adjacent groups is the primary factor contributing to their reproductive access to females, rather than relationships between males and females (Young et al. 1990). Females encourage subordinate males to enter social groups to increase mating choice, vigilance, and facilitate intergroup hostility (Richard 1985). “Bet-hedging” is a biological strategy that assists in mothers achieving the balance between selfpreservation and providing infant care (Stearns 1976). “Bet-hedging” specifically refers to a collection of life history traits where higher infant mortality rates, often more typical in unstable environments, drive females to reproductively invest less per gestation event (Stearns 1976). Females live longer in these environments, and by doing so have increased rates of reproduction over a longer duration, thereby increasing the probability that some infants will survive unstable environmental conditions and eventually reproduce (Stearns 1976; Stearns 1992). Propithecus
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spp. females are considered exemplary “bet-hedgers” by displaying unusually “slow” life histories (Richard et al. 2002). P. verreauxi females only reach sexual maturity after five years, relatively late in life, and often do not reproduce until six years of age, with females reproducing and living longer than expected compared to mammals of similar body size (Richard 1976; Richard et al. 2002). The energy conservation hypothesis emerged from Stearn’s (1972) work and proposes that less postnatal maternal investment is present in lemurs relative to other nonhuman primates, resulting in lemur mothers reserving energetic resources for subsequent births due to high infant mortality (Jolly 1966; see Wright 1999).
1.2.3.1. Infant mortality Infant and juvenile primates typically experience higher mortality rates relative to breeding adults as they become less dependent on mothers and more self-reliant; for example, heightened predation risk and foraging incompetence are two risk factors contributing to higher mortality rates in young primates (Janson and van Schaik 2002). Ring-tailed lemurs (Lemur catta) and P. verreauxi infants incur higher mortalities within the first postnatal year in comparison to gregarious anthropoids of similar body size (reviewed in Gould et al. 2003). Only 52% of P. verreauxi infants survive the first postnatal year and fatalities occur primarily during the wet season or shortly after birth, although no significant seasonal pattern has been detected (Richard et al. 2002). This is a high infant mortality rate relative to 29% in white-faced capuchins (Cebus capucinus) (Fedigan et al. 1996) or 16-19% in red howler monkeys (Alouatta seniculus) (Crockett and Rudran 1987), especially given the low reproductive output in Propithecus social groups of one infant per female every two years (Richard et al. 2002). L. catta infant mortality increased from 52% in a non-drought year to 80% during a drought year and 20% of all adult females in Beza-Mahafaly Reserve perished during this time, demonstrating that increased environmental stress on mothers contributes to high lemur infant mortality (Gould et al. 1999; Gould et al. 2003). The L. catta population in Beza-Mahafaly Reserve recovered quickly postdrought as L. catta females reproduce annually, have high annual birth rates (.80-.86), and reach sexual maturity earlier (between two to three years of age) than Propithecus spp. (Gould et al. 1999; Gould et al. 2003).
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1.2.3.2. Seasonality in dry deciduous forests Propithecus spp. infants in western dry forests are born during the dry season months in the austral winter (June-August) and weaned during the subsequent wet season (January-February) (Lewis and Kappeler 2005b; Young et al. 1990). Two strategies have been proposed to explain the variation seen in the timing of reproduction in primates. The first strategy suggests that females conceive during intervals of high or low food availability, and subsequently resources are the most abundant during the second half of lactation (van Schaik and van Noordwijk 1985), which is the most energetically expensive component of reproduction (Oftedal 1993; Tardif et al. 2001; Trivers 1974). In the second strategy, females conceive during a peak in food abundance and store energy reserves until mid-lactation, which occurs during periods of decreased food availability (van Schaik and van Noordwijk 1985). P. verreauxi females cannot employ the second strategy given that they lose 18% of their body mass during the dry season and hence cannot store sufficient fat reserves for periods of decreased seasonal food availability (Lewis and Kappeler 2005b). P. verreauxi follows the first reproductive strategy, where the birth season coincides with periods of reduced food availability, and the most energetically costly portion of lactation corresponds with greater food availability (Lewis and Kappeler 2005b; Young et al. 1990). This trade-off allows mothers to have the greatest access to food resources when experiencing the greatest level of energetic cost. Subsequently, early infant development occurs when resources are the scarcest and infants become independent from their mothers during periods of high food availability. Given differences in reproductive physiology, males and lactating females likely physiologically respond differently to seasonal constraints. Males also face energetic constraints during this time due to reduced food availability. Additionally, the risk of infanticide increases when dependent infants are present, and resident males must protect infants from immigrant males during lactation. Consequently, these factors may induce an elevated stress response in males during lactation. In contrast, lactating female may experience a reduced stress response relative to adult males to more successfully care for infants, though may also have an overall greater stress response during earlier lactation opposed to later lactation.
1.3. Maternal effects model The maternal effects model postulates that the quality of the physical environment and caregiving a mother provides influences the development and fitness of her offspring (see Bernardo
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1996; Cheverud and Wolf 2009; Galloway 2005; Inchausti and Ginzburg 1998; Kirkpatrick and Lande 1989; Lacey 1998; Maestripieri 2009; Maestripieri and Mateo 2009; Mateo 2009; McGinley et al. 1987; McLaren 1981; Mousseau and Fox 1998; Rossiter 1994; Willham 1972). Until recently, consideration of maternal effects had been largely absent from life history studies (Roosenburg 1996), which were primarily evaluated from a genetic, inherited perspective instead of examining the role of acquired environmental effects in maternal performance and subsequent effects on offspring (Bernardo 1996; Cheverud 1984; Rossiter 1998). Assessing maternal effects quantifies individual differences across generations over time, in turn measuring the rapidity and intensity of natural selection (Mateo 2009; Stearns 1976). Postnatal maternal effects directly influence offspring outside of the womb, whereas prezygotic (e.g., offspring genotype) and prenatal (e.g., placenta) maternal effects are mediated through the mother’s physiology (Rossiter 1998). Documenting significant changes in maternal care-giving behavior without solely capturing individual maternal behavioral variation has been successful in recent mammalian studies (Champagne et al. 2003; Fairbanks and McGuire 1995), which is of particular importance given the small sample sizes characteristic of many field studies. Studies of postnatal maternal effects provide data on intergenerational phenotypic plasticity since mothers quickly respond to environmental cues thereby influencing their immediate offspring, in turn influencing the subsequent generation (Bernardo 1996). Maternal effects are more relevant in mammalian evolutionary dynamics relative to any other taxa due to the extensive care-giving provided by mothers that influences offspring even after weaning (Reinhold 2002).
1.4. Dissertation objective My study examines maternal behavior, food nutrient composition, and stress responses in P. coquereli, an endangered lemur species belonging to the taxonomic family Indriidae, that inhabits a localized geographic range in the tropical dry deciduous forests in northwestern Madagascar. The objective of my dissertation is to quantify P. coquereli maternal care-giving behavioral effort from birth until six and a half months postnatal concurrently with measuring food nutrient values and identifying nutrient selection profiles in lactating females and temporal cortisol variation in lactating females compared to other group members (adult males and nonlactating adult females). I will demonstrate how mothers balance their nutritional needs and physiological responses with providing infant care during the seasonally energetically depletive
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lactation period. This will advance current discussions in evolutionary anthropology on maternal care-giving and its potential effects on offspring development.
1.4.1. Research hypothesis The inherited environmental effects (Rossiter 1996) and maternal effects models (Bernardo 1996) served as the theoretical foundation from which I formulated the hypothesis that I tested. My dissertation tests the following hypothesis and eleven related predictions established a priori: H1: P. coquereli mothers experience greater postnatal reproductive stress, which is measured by behavioral care-giving effort, nutritional food quality, and cortisol stress responses (see predictions below) during early/earlier-mid lactation (designated as 1-12 weeks postnatal) (MayAugust) in comparison to later-mid/late lactation (designated as 13-26 weeks postnatal) (September-December) due to the increased energetic costs of lactation while simultaneously caring for dependent infants during the driest seasonal months in the austral winter when food quality is low. H0: There is no difference in the postnatal reproductive stress P. coquereli mothers experience during early/earlier-mid lactation (designated as 1-12 weeks postnatal) (May-August) in comparison to later-mid/late lactation (designated as 13-26 weeks postnatal) (SeptemberDecember).
1.5. Maternal behavioral care-giving background 1.5.1. Female social dominance Propithecus spp. live in matrifocal groups and females outrank males in feeding priority (Richard 1974; Richard 1985). Female social dominance is a result of the high energetic cost of reproduction (Jolly 1984) and females often synchronize reproduction with the most favorable environmental conditions (Lewis and Kappeler 2005b; Young et al. 1990). Gestation length is approximately 163 days and females give birth to single offspring (Petter-Rousseaux 1962). One infant is born per female, with an interbirth interval of 24 months which is only reduced to one year if the neonate dies, indicating that reproduction is too energetically expensive to occur annually (Richard et al. 2002). All-parental behavior occurs (Richard 1974; Richard 1985), but in a captive study on a single P. coquereli infant, the infant spent the most time on mother’s
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relative to other group members, and the least time with immigrant males and subordinate females (Grieser 1992).
1.5.2. Basal metabolic rates during reproduction Females in species expressing female social dominance, particularly in Propithecus spp., metabolically invest more in neonates per day of gestation in comparison to male dominant or co-dominant strepsirhines (Young et al. 1990). Basal metabolic rate (BMR) measures the rate at which energy is depleted by an organism, excluding the influence of environmental or behavioral effects. BMRs are more difficult to quantify in primates than in other mammals because primates respond aversively to stressful conditions and capture of wild primates is necessary in order to measure BMR via oxygen consumption (Genoud 2002). The positive relationship between lemur BMR and prenatal maternal investment (measured as average daily maternal energy output) supports the prediction that lemurs have high prenatal investment in neonates for their BMR (Young et al. 1990). Thus, high prenatal investment appears to have contributed to the evolution of female dominance in lemurs, but other selective pressures also influenced its emergence since female dominance is not a characteristic exclusive to taxa with low BMRs (Young et al. 1990). Body mass is the primary determinant of mammalian BMRs, but there is also considerable mass-independent variability, demonstrating that physiological and environmental adaptations clearly play a role in accurately assessing BMRs and their rate of change under variable conditions (Genoud 2002). Haplorhines typically have higher BMRs than strepsirhines (reviewed in Harcourt 2008). Lemurs have low BMRs relative to haplorhines that elevate during reproduction (Richard and Nicoll 1987). The unpredictable climate in Madagascar (see Dewar and Richard 2007) has been used as the principal explanation for low BMRs in lemurs, but low BMRs are more widespread among African strepsirhines than previously thought and further studies are needed to test whether lemurs do indeed have a lower relative BMR for their body mass than other strepsirhines (Harcourt 2008).
1.5.3. Infant growth rates Strepsirhines produce neonates with smaller body mass and rapid postnatal growth rates of shorter durations in comparison to haplorhines (Leigh and Terranova 1998; Leutenegger 1973). Lemurs are generally sexually monomorphic in body size and the selective pressures
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contributing to the lack of dimorphism are both ontogenetic and environmental (Leigh and Terranova 1998). There is a lack of sex difference in most lemur postnatal growth rates, a trait referred to as bimaturism (Leigh and Terranova 1998, but see Tennenhouse 2016). The similar growth rate between sexes is unexpected given high rates of intermale competition and seasonal breeding in lemurs (Kappeler 1993; Mass et al. 2009; Richard 1991). The extent of bimaturism can be influenced by seasonality, photoperiod sensitivity of ontogeny, and female reproductive synchrony (Leigh and Terranova 1998). Ontogenetic adaptations to seasonal food abundance and quality is the primary restraint on bimaturism because male growth is limited as a result of decreased food abundance and quality during the dry season (Leigh and Terranova 1998). Lemur infants are still relatively altricial despite rapid postnatal growth (Jolly 1984). Accelerated postnatal growth is related to the rapid or concentrated milk nutrient transfer that is needed to wean infants more quickly (Power et al. 2002).
1.5.4. Maternal body mass Numerous parental and environmental sources considered within the inherited environmental effects model are responsible for the quality and duration of prezygotic, prenatal, and postnatal investment in offspring. Reproductive females must acquire and retain sufficient resources to sustain pregnancies and subsequently provide behavioral and nutritional care of infants. Maternal body mass is clearly a vital indicator of pre-and postnatal infant growth and thus is pertinent to infant survivorship and future fecundity (see Altmann and Alberts 2005; Leigh and Terranova 1998; Tardif and Bales 2004). Interestingly, the duration of lactation in large-bodied mammals is weakly correlated with both maternal and neonatal body mass and appears more dependent on overall maternal health (Lee et al. 1991). Lactation duration cannot be attributed to a single source, but rather results from a combination of individually specific physiological and seasonally contingent variables. Weaning age is reflective of environmental quality, where earlier weaning can result from a mother’s inability to sustain lactation due to low environmental quality (Lee et al. 1991). Conversely, high milk nutrient transfer resulting from greater food quality can cause weaning weight to be reached more rapidly than in lower quality environments, in turn facilitating earlier weaning (Lee et al. 1991).
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1.5.5. Lactation and phenotypic plasticity The Callitrichidae are a classic primatological example of coping with the energetic costs of lactation with phenotypic plasticity. Phenotypic plasticity is operationally defined as the genotypic capability to produce alternative morphological, physiological, or behavioral states in response to the surrounding environment (West-Eberhard 1989). Callitrichids, excluding Goeldi’s monkey (Callimico goeldii), experience severe energetic constraints due to biannual twin births, and combat this cost with reduced maternal behavioral care and high rates of paternal care, where fathers are the primary carriers from the time infants are only a few days old (Tardif et al. 1993). In contrast, C. goeldii underwent a reduction in litter size which enables mothers to delay the onset of paternal carriage and extend weaning age, thus demonstrating divergent behavioral strategies in closely related callitrichid species (Ross et al. 2010). Wied’s marmoset (Callithrix kuhlii) mothers that conceived early in their postpartum phase significantly reduced behavioral investment in infants, by carrying less and rejecting infants more frequently to conserve energy for the subsequent litter (Fite et al. 2005). In regards to this study, paternal care in P. coquereli has only been measured in a captive setting (Bastian and Brockman 2007), and longitudinal data on the quality, duration, and variability of allomaternal care in wild. P. coquereli infant carriage have not been available until my dissertation.
1.5.6. Infant behavior research justification Although behavioral development in Propithecus spp. infants has been examined in prior studies, circumspection must be exercised due to the lack of longitudinal studies, noncontinuous data, or small sample sizes in two wild studies (n=3 in Jolly 1966; n=9 in Richard 1976) and two captive studies (n=1 in Eaglen and Boskoff 1978; n=2 in Grieser 1992). Propithecus spp. infants are carried until approximately six months after birth, coinciding with the weaning process (Jolly 1966; Richard 1976). Although P. verreauxi infants began to taste solid foods one to two weeks following birth, infants often tasted foods not consumed by adults and consumed foods exclusively eaten by group members by five months postnatal (Richard 1976). Unexplained variation exists in documenting infant development. Sequences of independent locomotive behavior were first observed at fifteen days (Richard 1976) in comparison to two months postnatal (Jolly 1966).
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1.6. Maternal behavioral care-giving predictions The maternal effects model (Bernardo 1996) and the numerous supported energetic constraints associated with lactation serve as the theoretical underpinnings for my predictions on maternalinfant relationships. I predict that the duration, frequency, and type of P. coquereli maternal infant carriage will decrease as infants increase in age, as evidenced by strepsirhine growth rates. Infants become less dependent on their mothers over time for their transport and nutritional needs. I predict P. coquereli mothers will be the principal infant behavioral care-givers as evidenced by high prenatal maternal investment that has contributed to the evolution of female feeding priority and dominance in some lemur species, thus enabling mothers primary access to higher quality food resources. I propose that lactating females sufficiently offset the high energetic costs of lactation and infant care without comprising their current or future reproductive success. P1. Maternal behavioral care-giving effort will decrease as P. coquereli infants increase in age as measured by infant transport position (ventral, dorsal, independent). Infants will spend the greatest duration in the ventral position, followed by the dorsal position, and the least duration independently from carriers from birth until weaning (twenty-six weeks postnatal). P2. P. coquereli mothers will provide the majority of infant behavioral care-giving relative to adult males and non-mother adult females as measured by the frequency and duration of infant carriage from birth until weaning. P3. Infant contact initiated by P. coquereli mothers will decrease while infant contact broken by mothers will increase as infants age. P4. Contact with mothers initiated by P. coquereli infants will decrease while contact with mothers broken by infants will increase as infants age.
1.7. Nutritional food quality background Food selection, foraging ability, and thermoregulation are influenced by food quality, thereby contributing to the amount of available energy mothers can invest in infant care-giving while maintaining their own nutritional needs (Lee and Bowman 1995; Stearns 1977). Few studies have examined nutritional food quality specifically during lactation in non-human primates. Lactation increases the quantity of amino acids needed to energetically sustain females, in turn significantly increasing protein requirements (Jessop 1997). Non-human primate nutritional
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models are often rooted in human nutritional models, and therefore do not accurately represent protein sources available to wild primates (Oftedal 1991). Protein, the primary nutrient involved in mammalian reproductive function, requirements increase by more than 1/3 during early lactation in humans (Oftedal 1984; Cameron 1996; Tilden and Oftedal 1997; Power et al. 2002). Protein requirement guidelines are primarily based on captive animals that experience reduced activity, fewer nutritional demands, and environmental stress in comparison to wild animals. There is a lack of agreement over the amount of protein needed to sustain wild mammals during gestation and lactation, in part because the laboratory and statistical significance of protein is a measure of total protein, which does not accurately reflect the biological significance of the food item since the amount of available protein is unknown (Gogarten et al. 2012; Oftedal 1991).
1.7.1. Propithecus spp. diet Propithecus spp. have highly seasonal diets and are primarily folivore-frugivores, with flowers and bark being consumed in smaller quantities during certain times of the year (Hemingway 1998; Irwin 2008b; Lewis and Kappeler 2005a; McGoogan 2011; Norscia et al. 2006; Richard 1974). In terms of digestive anatomy, P. coquereli has a relatively long, spiraled colon and large, sacculated caecum (Campbell et al. 2004), and are classified as caeco-colic fermenters since either the caecum or colon is the primary fermentation chamber (Lambert 1998). This fermentation type decreases the amount of protein available prior to digestion and therefore, best suits taxa that consume digestible compounds (Alexander 1993). The large quantities of leaves consumed by P. coquereli are higher in insoluble fiber than other plant parts (Lambert 1998). P. verreauxi select foods primarily based on nutritional quality throughout the year, with protein and sugar consumption the highest when more fruit and flowers are consumed during wet season months (Norscia et al. 2006). The greatest diversity in foods consumed by P. diadema occurred during the calendar months when leaf consumption was greatest, suggesting that Propithecus spp. can afford to be more selective when better quality foods are seasonally available; either because higher quality foods fulfill nutritional requirements more quickly than lesser quality foods, or to avoid secondary compounds that can inhibit digestion or be toxic in larger quantities (Irwin 2008b). P. diadema consume markedly more fruits and seeds during the wet season, and shift to consuming greater quantities of leaf buds and flowers during the dry season (Irwin 2008b). P. coquereli follows a similar pattern of feeding predominantly on mature leaves and dormant buds during the dry season and shift to young leaves, fruit, and flowers during the wet
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season (Richard 1974). P. coquereli consumed bark throughout the dry season, but did not consume dead wood; the opposite pattern was found during the wet season, although insectivorous behavior was not observed while groups consumed bark (Richard 1974). A more recent long-term study of the same species found that both dead and alive wood was consumed throughout the year (McGoogan 2011). This same study found that P. coquereli adult females spent significantly more time feeding than adult males, though this may be due to the group sex ratio of one male to four females (McGoogan 2011). Plant parts consumed by P. coquereli are spatially auto correlated and likely related to the synchronous patterns of fruiting and flowering characteristic of Madagascar (McGoogan 2011).
1.7.2. Protein-to-fiber ratios Protein-to-fiber ratios often determine leaf choice, with primates preferentially consuming leaves with a high protein-to-fiber ratio (Milton 1979). Trees along habitat edges receive more sunlight than trees closer to the forest interior, and can result in leaves that occur on habitat edges having higher protein-to-fiber ratios (Ganzhorn 1995a). Protein-to-fiber ratios and food consumption have been primarily examined in New World monkeys (Milton 1979) and colobines (Chapman et al. 2004; Gogarten et al. 2012), and have recently been evaluated in L. catta (Gould et al. 2011) and P. coquereli (McGoogan 2011). P. coquereli groups occupying home ranges closes to habitat edges showed no difference in the nutritional quality of foods consumed relative to forest interior groups (McGoogan 2011). All groups consumed foods high in crude protein and high protein-to-fiber ratios (McGoogan 2011). Gestating and lactating females forage less and consume leaves higher in protein relative to other group members to conserve metabolic expenditures (in callitrichids, Goldizen 1987; Price 1991; in lemurs, Sauther 1994; Vasey 2002). Conversely, Gould et al. (2011) found no differences in nutrient intake between gestating and lactating L. catta in comparison to conspecifics. Instead, the study found that early gestating females spent a greater amount of time feeding than during the period of early/mid-lactation (Gould et al. 2011). Young leaves consumed by colobines were found to have more overall protein, were consumed more frequently, had higher protein-to-fiber ratios, and were more digestible than mature leaves (Chapman et al. 2004).
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1.7.3. Gross energy The term gross energy refers to the measurement of energy released after heat combustion in a laboratory setting, and is exclusively dependent on the nutrient composition of a food (Maynard and Loosli 1965b). Accordingly, a gross energy value is analogous to the energetic density of a food (Hinde and Milligan 2011), with high fat foods having higher gross energy values than carbohydrates, and high protein foods typically having moderate gross energy values (Maynard and Loosli 1965b). Metabolizable energy is a term used to describe the energy remaining after digestion and absorption, excluding indigestible material. Digestion is the chemical breakdown of food into usable compounds. Absorption is the transfer of these digested compounds across the gastrointestinal tract into the bloodstream. Metabolizable energy measures the absolute energy consumed by an animal, whereas gross energy measures the total caloric content of the food item. Thus, considering metabolizable and gross energy in tandem more accurately assesses the biological significance of foods, rather than considering either energy measure independently. All L. catta group members consume foods with significantly higher gross energy during early gestation than during early/mid-lactation, but no sex differences were found, which is likely due to extreme climatic events like cyclones (Gould et al. 2011). An alternative explanation is that males experience nutritional duress after mating competition, and require foods with higher nutritional value during the early gestation period (Gould et al. 2011). P. coquereli spent most of their annual activity budget consuming foods high in gross energy (Acacia spp.) and high protein-to-fiber ratios (McGoogan 2011). The nutritional quality of foods selected by lactating P. coquereli females was unknown prior to my dissertation.
1.8. Nutritional food quality predictions I predict that P. coquereli mothers will select relatively high quality foods, which I define as foods high in available protein, low in fiber, high in non-protein gross energy, or high in minerals. My prediction is based on the theoretical groundwork of optimal foraging theory (Stephens and Krebs 1986), nitrogen maximization (Mattson 1980), fiber limitations (Milton 1979), and energy maximization models (Schoener 1971). P4. P. coquereli lactating females will select foods high in available protein. P5. P. coquereli lactating females will select foods high in minerals. P6. P. coquereli lactating females will select foods low in fiber.
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P7. P. coquereli lactating females will select foods high in non-protein energy.
1.9. Stress response background Variation in human maternal care is influenced by endocrinological fluctuations that determine a mother's attachment to her infant (Fleming et al. 1997). Socioendocrinology studies indicate that hormonal fluctuations are strongly associated with seasonality, sociality, reproductive function, and offspring development (e.g., Beehner and McCann 2008; Boonstra et al. 1998; Brockman et al. 2009; Gould et al. 2005). Glucocorticoids are steroid hormones that regulate glucose metabolism in the adrenal cortex, and are released into the bloodstream in response to acute stressors. Stress does not necessarily incite negative responses since energy is made available at critical moments, thereby improving biological fitness (Keay et al. 2006). Cortisol is a glucocorticoid that suppresses the immune system under chronic conditions. Distinguishing between stress and distress is essential when evaluating stress responses. This distinction can be measured as the biological cost of the stress to the animal, and is present under acute and chronic circumstances (Moberg 2000). It is not the amount of stress an animal experiences that is quantified when glucocorticoids such as cortisol are measured, but more accurately the stress response of the animal to its environment during a particular time (Busch and Hayward 2009). Climatic instability, food quality and availability, reproduction, infant presence, and predation pressure all produce elevated glucocorticoid levels in non-human primates (e.g., Abbott et al. 2003; Bales et al. 2005; Brockman et al. 2009; Fichtel et al. 2007a; Girard-Buttoz et al. 2009; Gould et al. 2005; Ostner et al. 2008; Rangel-Negrín et al. 2009; Saltzman and Abbott 2009; Setchell et al. 2008; Ziegler 2000). For example, P. verreauxi males experience an elevated stress response when infants are present in comparison to when infants are absent from groups (Brockman et al. 2009). Infant presence coincides with elevated infanticide risk during the lactation period from immigrant males while infants are still dependent on their mothers for milk (Brockman et al. 2009). Temporal variation in P. coquereli stress responses within or between sexes and reproductive classes have not been studied prior to my dissertation.
1.10. Temporal cortisol variation predictions My predictions are formulated from the cortisol-adaptation (Bonier et al. 2009b) and brood-value hypotheses (Heidinger et al. 2006). I predict P. coquereli mothers and adult males will have
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significantly higher fecal cortisol levels during early/earlier-mid lactation, coinciding with the peak of the annual dry season, in comparison to later-mid/late lactation when food quality and abundance begins to improve. Infant births occur during the peak of the austral winter when food quality in the forest is the lowest, risk from immigrate males is intensified, infants are the most altricial, and lactation constraints are the highest. Since Propithecus spp. have a low reproductive output, this makes the reproductive value of infants relatively high (see Heidinger et al. 2006) in comparison to species that produce more offspring during the course of a lifetime. This, in turn, incites a decreased stress response for mothers to successfully care for their infants and prepare for future pregnancies. I predict that P. coquereli mothers will have significantly lower fecal cortisol levels relative to adult males and non-lactating adult females. P9. P. coquereli lactating females will have significantly higher fecal cortisol levels during early/earlier-mid lactation relative to later-mid/late lactation. P10. P. coquereli adult males will have significantly higher fecal cortisol levels during early/earlier-mid lactation relative to later-mid/late lactation. P11. P. coquereli lactating females will have significantly lower fecal cortisol levels relative to adult males and non-lactating adult females during both lactation phases.
1.11. Dissertation overview Chapters 2 through 4 are presented as independent manuscripts. Chapter 2 assesses P. coquereli maternal behavioral care-giving effort in their infants from birth until 26 weeks postnatal. Chapter 3 examines nutritional food quality and the biological significance of foods selected by lactating females. Chapter 4 investigates temporal variation in cortisol across different sex and reproductive classes during lactation. Chapter 5 draws conclusions and offers insights from the preceding four chapters and provides directions for future research.
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Table 1.1. Gross milk composition in mammals Genus & species N DM CP (%) (%)
Fat (%)
Sugar (%)
Ash (%)
Hooded seala (Cystophora cristata)
15
69.8
4.9
61.0
1.0
n/a
Domestic doga (Canis familiaris)
25
22.7
7.5
9.5
3.8
1.1
Humanb (Homo sapiens)
n/a
12.4
0.9
3.8
7.0
0.02
Common marmosetc (Callithrix jacchus)
46
13.9
2.7
3.5
7.4
n/a
Ring-tailed lemurd (Lemur catta)
1
10.9
2.0
1.8
8.1
n/a
DM dry matter, CP crude protein a Data from Oftedal and Iverson (1995) b Data from Hambraeus (1984) c Data from Power et al. (2002) d Data from Tilden and Oftedal (1997)
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Table 1.2. Gross milk composition in primates Genus & species N DM CP (%) (%)
Fat (%)
Sugar GE C/P (%) (kcal/g)
Female body mass (kg)
Black-and-white ruffed lemur (Varecia variegata)
5a
14.0a
4.2a
1.3a
7.7a
0.84a
P
3.5c
Common brown lemur (Eulemur fulvus)
6a
9.6a
1.3a
0.9a
8.5a
0.49a
C
2.3c
Sunda slow loris (Nycticebus coucang)
4a
16.3a
3.9a
7.0a
6.6a
1.1a
P
0.6c
Bolivian squirrel monkey (Saimiri boliviensis)
16b
16.6b
3.7b
5.0b
6.9b
0.91b
C
0.7c
DM dry matter, CP crude protein, GE gross energy, C/P carry or park infants a Data from Tilden and Oftedal (1997) b Data from Milligan et al. (2007) c Data from Smith and Cheverud (2002)
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Figure 1.1. Inherited environmental effects model: components of offspring phenotype
The components of offspring phenotype expressed in time t, deriving from the direct contribution of nuclear genes by one parent, a time-lagged presentation of the parental environment (Em), a time-lagged expression of parental performance genes and their interactions with the parental environment to produce the parental performance phenotype (Pm), plus the offspring’s own environment (Eo). For simplicity of presentation, G indicates additive genetic effects with dominance and epistasis assumed to be negligible. The numbered sources indicate possible routes of contribution to the offspring phenotype; Source 8 is any genetic covariance (cov) between genes expressed in two generations such as covGm Go or cov(GmEo)(G0Eo) (figure and description taken from Rossiter 1996)
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Chapter 2 Maternal Effort in Propithecus coquereli in Ankarafantsika National Park, Northwestern Madagascar “Behave like the chameleon: look forward and observe behind.” “Mitondra tena tahaka ny tanalahy: mijery eo aloha sy mandinika ny aoriana.” ~ Malagasy proverb
2.1. Abstract Lactation is the most energetically expensive activity in which mammals participate. Lactating females face energetic constraints absent in non-lactating conspecifics and in turn, must compensate for substantially higher energy requirements during the lactation process. Extended durations of infant transport are widespread throughout the taxonomic order Primates while rare considering the class Mammalia. Infant transport is also an energetically costly mammalian activity seen predominately in primates, yet few primatologists examined this behavior in detail. I evaluated Coquerel’s sifaka (Propithecus coquereli) maternal behavioral care-giving effort in Ankarafantsika National Park, northwestern Madagascar from 1-26 weeks postnatal (n=10 mothers with infants) and compared it to non-mothers (n=19 adult males, n=8 adult females without infants). Maternal behavioral care-giving and the quality of the environment mothers provide directly influences infant development and future reproductive success. The volatile climate and extreme seasonality characteristic of Madagascar coupled with the associated costs of lactation and infant transport gives rise to a large energetic challenge faced by P. coquereli mothers. I measured infant transport position (ventral, dorsal, independent), the duration of infant transport by carriers (mothers, adult males, adult females), and the frequency of infant bodily contact between mothers and their infants for 678 focal hours of observation over two consecutive birth seasons (2010 and 2011). Infant transport position was used as a proxy for development. Infants spent significantly more time in the ventral transport position than either dorsally or independently. Mothers were the primary infant transporters. Adult males and females that were not mothers both participated in infant transport, but for significantly less time than mothers. Infants initiated and broke bodily contact with mothers more frequently than mothers initiated and broke contact with their infants. P. coquereli infants continued to be transported 26% of the time by the 26th postnatal week. This clearly
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demonstrates that P. coquereli infants are more altricial relative to other lemurs of comparable body size and dependent on their mothers for longer durations than suggested by previous studies. P. coquereli mothers were the primary infant behavioral care-givers and must employ alternative behavioral, physiological, or nutritional strategies to offset the associated energetic costs of lactating while transporting infants in a harsh environment.
2.2. Introduction Mammalian parental care is long in duration and infants are more altricial than in other animal classes (Clutton-Brock 1991). Nonetheless, long-term infant transport is uncommon in most mammals while frequent in primates (Ross 2001a). Lactation is the single most energetically costly activity for mammals (see Oftedal 1984), followed by infant transport, though lactation is considerably more costly than transport (Altmann and Samuels 1992; Dewey 1997; Nievergelt and Martin 1999; Tardif et al. 1993). Lactation increases daily energy expenditures up to 150% in mammals, with mean caloric intake during lactation increasing 66-188% (reviewed in Gittleman and Thomspon 1988; Lee et al. 1991). This striking rise forces lactating females to compensate for substantially higher energy requirements by utilizing stored energy (e.g., fat reserves), increasing energy consumption (e.g., food), reducing energy invested in physiological states (e.g., basal metabolic rate), or reducing energy in behavioral activities (e.g., infant transport).
The maternal effects model proposes that the care mothers provide their offspring determines how offspring respond to their physical environment (e.g., Bernardo 1996). Maternal care includes all prezygotic, prenatal, and postnatal investment in offspring that is either expressed through a genetic, physiological, behavioral, or environmental condition (Rossiter 1996; Wade 1998). Mammalian research on maternal effects has primarily focused on ungulates (e.g., Cameron and Linklater 2000) and within the non-human primates, the cercopithecines (e.g., Altmann 1988). Lactation is divided into two phases when infants: (1) are exclusively dependent on milk nutrients and (2) rely on a combination of milk nutrients and solid food (Langer 2008). Maternal effects both directly and indirectly effect offspring phenotype, the observable traits of an organism, with a combination of parental and environmental sources selecting on offspring phenotype. These parental and environmental sources are either genotypic or phenotypic and are collectively referred to as the inherited environmental effects model (Eisen and Saxton 1983;
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Rossiter 1996). Thus, maternal effects are a component of the inherited environmental effects model. Nongenetic maternal effects influence individual adaptations to environmental conditions and contribute to evolutionary changes in resident populations (reviewed in Maestripieri and Mateo 2009).
Environmental quality is a source included within the inherited environmental effects model that plays a significant role in the structure, quality and duration of maternal-infant relationships (Rossiter 1996). The dynamic relationship between the expression of parental effects and environmental quality exists irrespective of the additional variables contributing to offspring phenotypic expression, is species dependent, and seasonally variable (Rossiter 1996; Rossiter 1998). For instance, the quality and duration of parental care invested in human offspring is influenced by environmental risk factors, such as famine and warfare (Quinlan 2007; Quinlan et al. 2003). When these human risk factors increase, maternal care investment decreases (Quinlan 2007). Human mothers with low socioeconomic status, and thus more restricted access to resources, have been found to wean high-risk infants (defined as infants with lower birth weights in poorer physical condition) more rapidly than healthy infants to maximize the potential reproductive value of future healthy infants (Bereczkei 2001). This life history trade-off supports that mothers do not invest care in high-risk infants because they offer little inclusive fitness in comparison to healthy infants that have a greater chance of survival and eventually producing their own offspring. These studies demonstrate that human parental care patterns are directly affected by environmental quality and contingent on resource stability.
The quality of maternal care infant receive may partly reflect infant sex. The Trivers-Willard (TW) model is a classic life history model which predicts maternal health is the primary determinant of sex ratio variation, and that individual females will produce biased birth sex ratios (BSRs) favoring the sex benefiting most from increased parental care (Trivers and Willard 1973). The T-W model has not always been supported when applied to primate taxa (reviewed in Richard et al. 1991), thereby demonstrating that the evolutionary factors selecting biased BSRs cannot be solely attributed to maternal health and care-giving, but must expanded to consider additional beneficial elements. The local resource competition hypothesis (LRC) is a competing hypothesis to the T-W model proposing that BSRs will favor the dispersing sex due to intrafemale competition in female philopatric groups, which is most palpable when resource
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competition is high and unstable (Hamilton 1967; Silk 1984). Another competing model to the TW model is the local resource enhancement (LRE) model, which suggests that BSRs in cooperatively breeding species will favor the more effective helper sex to maximize infant caregiving (Pen and Weissing 2000).
Resource instability in mammals besides humans has been shown to negatively influence maternal care. For example, variability in Long-Evans rat (Rattus norvegicus) litter size, sex, and weaning weight does not alter individual maternal care behavior across multiple litters when resource access is constant and only changes when resources are unstable (Champagne et al. 2003). Bonnet macaque (Macaca radiata) mother-infant relationships are more negatively influenced by resource unpredictability than a constant state of decreased food availability (Rosenblum and Andrews 1994). In the same study, captive infants that experienced a combination of high (food was sparse and patchily distributed) and low (food was abundant and readily distributed) foraging demands, had fewer positive interactions with their mothers and displayed greater emotional distress than infants raised exclusively in the lower quality, higher foraging demand environment where food was sparse and patchily distributed (Rosenblum and Andrews 1994). Thus, resource instability affects gestational development and is also a driving factor in the quality of postnatal care mothers provide.
In contrast to the T-W model, the LRC and LRE models focus on broader scale genetic and ecological processes rather than exclusively on maternal body condition during conception to determine the causes of preferred BSRs (Silk and Brown 2008). A review of BSRs in 102 primate species found BSRs are not related to the magnitude of sexual dimorphism present in dimorphic species, and thus BSRs do not reflect differences in the costs of behavioral care-giving between male and female offspring since BSRs would be expected to be skewed in favor of the less costly sex (most typically females due to their smaller body size) (Silk and Brown 2008). The same study found that female dispersing species had female-biased BSRs (Silk and Brown 2008). Cooperatively breeding species had male-biased BSRs, which followed predictions, given that males are typically more invested in behavioral care-giving than females in cooperatively breeding species (Silk and Brown 2008). These findings support predictions from the LRC and LRE models and demonstrate that examining BSRs on a population level in comparison to individualized responses recommended by the T-W model will assist in isolating
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the causes of preferred BSRs and encourage interspecific comparisons.
Mammalian mothers are typically the primary infant care-givers since infants rely on mothers for milk, but allomaternal care is present within mammals, and is more common, albeit highly variable, within primates than earlier understood (see Bales et al. 2000; Chism 2000; Fite et al. 2005; Goldizen 1987; Gould 1992; Morland 1990; Roberts et al. 2001; Ross and MacLarnon 2000; Schradin and Anzenberger 2001a; Schradin and Anzenberger 2001b; Zahed et al. 2008). Allomaternal care is a collection of care behaviors including infant transport, infant guarding, babysitting, and energy transfer by non-mothers (reviewed in Tecot et al. 2013) used, in part, to reduce the energetic burden on lactating females (see Ross and MacLarnon 2000 Table 2.1 for a list of proximate, adaptive, and nonadaptive determinants of allocare). Infant carrying is the second most energetically costly activity within this list (Altmann and Samuels 1992) and is associated with elevated nutritional and predation risks (Schradin and Anzenberger 2001a). Lemur allomaternal studies are alarmingly few (reviewed in Tecot et al. 2013, but see Baden 2011), due partly to lower documented incidences within lemurs, and fewer lemur postnatal behavioral studies in comparison to callitrichids and cercopithecines. There is no relationship between allomaternal care and offspring sex in golden lion tamarins (Leontopithecus rosalia), but there was a significant relationship between the number of allocare-care givers and the number of surviving infants (Bales et al. 2002). Callitrichid infants grow rapidly and solid food provisioning by group members is critical to infant survivability (Bales et al. 2002). Verreaux’s sifaka (Propithecus verreauxi) tertiary (exclusively reproductive individuals) sex ratios are nearly equal, in contrast to many haplorhines that have female-biased tertiary sex ratios (Richard et al. 1991). Interestingly, the P. verreauxi secondary (at birth) sex ratio is skewed, which suggests a disparity in sex survivability that results from higher mortality rates in reproductive females (Richard et al. 1991). Longitudinal data in the wild on carrier identity and duration of P. coquereli infant transport have not been available until my dissertation.
Lemur reproductive events occur under fixed seasonal parameters as a response to restricted food availability and quality (see Tecot 2010; Wright 1999). Madagascar is characterized by erratic rainfall patterns that have caused the evolution of unique tree phenology and unpredictability in food abundance and distribution (Dewar and Richard 2007), including the Mahajanga province where data for my dissertation were collected. Thus, fruiting is restricted to a brief number of
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calendar months (reviewed in Dewar and Richard 2007), thereby requiring P. coquereli to rely on alternative, less energy dense resources (e.g., leaves) during the majority of the year (McGoogan 2011). P. verreauxi males and females undergo seasonal changes in body mass, weighing the least during the middle to end of the dry season, with females experiencing greater changes in body mass than males (Richard et al. 2000). P. verreauxi females with higher body mass during the mating season had a greater number of births the subsequent season opposed to females that weighed significantly less and gave birth to fewer infants (Richard et al. 2000).
P. verreauxi reproductive females experience punctuated intervals of high mortality because of the high energetic costs of reproduction together with extreme seasonality on Madagascar (Richard et al. 1991). Cyclones and rainfall levels have adverse effects on Milne-Edwards’ sifaka (Propithecus edwardsi) reproductive rates (Richard et al. 2002). The number of P. edwardsi infants per female per year surviving to one postnatal year is negatively related to cyclone presence during gestation (Dunham et al. 2011). The number of drought months infants experience during the first postnatal year are also negatively associated with survival, demonstrating that lemur reproductive success is contingent on climatic events (Dunham et al. 2011). Maternal dental senescence and rainfall influences P. edwardsi infant survival, with older mothers requiring more daily precipitation to sustain dependent infants during lactation (King et al. 2005). Lactation also increases demands to water balance (Gittleman and Thomspon 1988), a cost that is especially pronounced in species living in xeric habitats (Soholt 1977) such as P. coquereli.
Propithecus spp. have unsealed vulvas in contrast to other Malagasy strepsirhines and exhibit concealed ovulation, a character present in many primate genera (Brockman et al. 1998). Females undergo single 0.50 to 0.96-hour estrus periods during the three-month breeding season (Brockman and Whitten 1996). Due to the short duration of estrus, Many female strepsirhines display estrous asynchrony within the seasonal synchrony of estrus, which increases mate choice by reducing female-female competition for mates, although males also successfully mate guard females and harass mating pairs irrespective of social status (Sauther 1991). Propithecus spp. polyandrous mating may be a strategy to confuse paternity, thereby decreasing the risk of infanticide (Wright 1995; but see Erhart and Overdorff 1999). However, monoandrous and polyandrous matings both result in conception and thus the function of polyandry is not a
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strategy exclusively used to decrease infanticide (Brockman and Whitten 1996). A 10 to 15-day elevation in estradiol distinguish behavioral estrus and increased progesterone levels determine conception one to three days’ post-estrus, with estradiol levels characteristic of the gestational phrase present between 42 to 45 days after conception (Brockman and Whitten 1996).
Maternal behavioral care-giving effort is a nongenetic maternal effect that I define as the frequency and duration of infant transport by P. coquereli mothers in comparison to adult males and non-mother adult females. My dissertation tests the hypothesis that P. coquereli mothers experience greater postnatal reproductive stress, which is measured by behavioral care-giving effort, nutritional food quality, and cortisol stress responses during early/earlier-mid lactation (designated as 1-12 weeks postnatal) (May-August) in comparison to later-mid/late lactation (designated as 13-26 weeks postnatal) (September-December) due to the increased energetic costs of lactation while simultaneously caring for dependent infants during the driest seasonal months in the austral winter when food quality is low. This chapter examines P. coquereli maternal behavioral care-giving effort by addressing four predictions under this hypothesis. P1. Maternal behavioral care-giving effort will decrease as P. coquereli infants increase in age as measured by infant transport position (ventral, dorsal, independent). Infants will spend the greatest duration of time in the ventral position, followed by the dorsal position, and the least duration independent from carriers from birth until weaning (twenty-six weeks postnatal). P2. P. coquereli mothers will provide the majority of infant behavioral care-giving effort relative to adult males and non-mother adult females as measured by the frequency and duration of infant carriage from birth until weaning. P3. Infant contact initiated by P. coquereli mothers will decrease while infant contact broken by mothers will increase as infants age. P4. Contact with mothers initiated by P. coquereli infants will decrease while contact with mothers broken by infants will increase as infants age.
2.3. Methods 2.3.1. Study site and species I conducted this study from Ampijoroa Forestry Station in Ankarafantsika National Park (ANP) located in the Mahajanga Province in northwestern Madagascar (Figure 2.1). The
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Ankarafantsika region (135,000 ha) was first established as two protected areas in 1927 and recognized as a national park in 2003. Ampijoroa is situated in the southwestern portion of ANP. The Marovoay area (38,000 ha) found within the Ankarafantsika region is the second largest producer of rice, the primary subsistence crop, in Madagascar (Alonso and Hannah 2002). The GPS coordinates of the research base camp are 16°18’31” South, 46°48’49” East and is 88m above sea level. ANP is characterized as a dry deciduous forest with an exceptionally pronounced dry season (Alonso and Hannah 2002; Du Puy and Moat 1996). Forested areas surrounding Ampijoroa are experiencing anthropogenic disturbance from slash and burn agriculture, fire, relatively high volumes of human traffic, unregulated presence and herding of domestic cattle, bushmeat hunting, and hole digging for Dioscorea maciba tuber extraction (Alonso and Hannah 2002; Crowley et al. 2012; Gerardo and Goodman 2003). The underlying geological formation in the Ankarafantsika region is composed of sandstones and the study area sits atop a sandstone plateau between 310-340 m above sea level (Du Puy and Moat 1996; Lourenço and Goodman 2006). Soils are either red, speckled or white, with red soil containing the highest water content and white sand the lowest (Crowley et al. 2012). Red soil most often occurs in the forest edge and in the savannah itself, though is also present in the forest interior and is presumably more nutrient dense due to its higher water content than forest interior quartz white sands (Crowley et al. 2012). Many trees grow in nutrient poor, acidic white sands and a thick layer of loose sand is present on the soil surface as a result of sandstone erosion (Du Puy and Moat 1996; Lourenço and Goodman 2006). Flora are speciose and the forest understory is moderately thick with sparse leaf litter (Lourenço and Goodman 2006) Annual precipitation in ANP ranges from 1100-1600 mm, with the majority of rainfall occurring in January and February and a period of extreme desiccation from May to September in which there is very little rainfall (Rendigs et al. 2003). Average daily temperatures range from 16°C during the dry season to 37°C in the wet season (Rendigs et al. 2003). Vertebrates have varied adaptive responses to cope with the austral winter including torpor or hibernation and flora are resilient to desiccation (Lourenço and Goodman 2006; Rendigs et al. 2003). There are eight extant lemur species in ANP including: Coquerel’s sifaka (Propithecus coquereli), common brown lemur (Eulemur fulvus), mongoose lemur (Eulemur mongoz), western woolly lemur (Avahi occidentalis), lesser dwarf lemur (Cheirogaleus medius), Milne-Edwards' sportive lemur (Lepilemur edwardsi), Gray mouse lemur (Microcebus murinus), and the golden-
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brown mouse lemur (Microcebus ravelobensis) (Alonso and Hannah 2002). The International Union for Conservation of Nature estimates that the P. coquereli has experience rapid population declines of more than 50% during the last 30 years primarily due to habitat loss (Andrainarivo 2008, accessed 17 November 2013) and more recently, hunting for human consumption (Gerardo and Goodman 2003). The slow life histories exemplified by Propithecus spp. increases extinction risk (Purvis et al. 2000) and amplifies the devastating impact of hunting given Propithecus spp. do not reproduce until later in life, have interbirth intervals of every other year, and only one infant is present per social group (Pochron et al. 2004; Richard et al. 1991). An estimated population of ~47,000 P. coquereli currently live in ANP (Kun-Rodrigues et al. 2014). Density estimates range from 5-100 individuals/km2, with habitat quality (i.e., negative effects of roads and forest edges) as the principal factor for this high variability (Kun-Rodrigues et al. 2014). An estimated 5 individuals/km2 presently exist in Ampijoroa (Kun-Rodrigues et al. 2014), in comparison to an estimated 60-75 individuals/km2 in the 1980s (Albignac 1981). This is a rapid decrease of more than 90% of the P. coquereli population in Ampijoroa (KunRodrigues et al. 2014).
This chapter examines the duration and frequency of P. coquereli maternal behavioral effort from infant birth (referred to as week 1 postnatal) until 26 weeks postnatal. Infant transport position, infant carrier identity, and infant bodily contact between mothers and their infants were used as the measures of maternal behavioral effort and compared with non-mothers.
2.3.2. Data collection Data were collected for a total of 14 months between June-December 2010 and 2011. A previously established research trail system in Jardin Botanique A (JBA)(see Rendigs et al. 2003 for a detailed site description) and the tourist trails identified as the “Coquereli circuit” were used to initially locate P. coquereli groups. I, along with 1-2 research assistants, collected data on ten habituated P. coquereli groups. The principal investigator trained assistants in focal animal sampling techniques and inter-observer reliability diagnostic tests were performed with assistants once per month for the duration of this study. Inter-observer reliability was performed a total of five times approximately every three months and was calculated using a Kappa coefficient as the measure of agreement between observers following Lehner (1996), where Po = observed proportion of agreements and Pc = chance proportion of agreements:
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Kappa = (Po - Pc) (1 - Pc)
The Kappa statistic was applied separately to infant position (85% agreement between observers), infant carrier (80% agreement between observers), and infant bodily contact between mothers and infants (87% agreement between observers).
Seven P. coquereli groups were studied in season 1 and three groups were studied in season 2 for 26 consecutive weeks. Attempts to locate additional groups with infants in season 2 were unsuccessful and likely due to Propithecus spp. interbirth interval length of every other year. An 8th group was located in season 1, but the infant disappeared during the 3 rd observation week and was presumed dead. Thus, the infant mortality rate during this study was only 9%. Early/earliermid lactation was designated from May to August and later-mid/late lactation from September to December. P. coquereli groups were considered habituated when no alarm calling occurred after researcher presence was detected. Phenotypic variations (e.g., tail length and shape, facial features) were used to differentiate between individuals. Group composition remained constant in all groups throughout both seasons (Tables 2.1, 2.2). A total of 47 individuals composed the ten groups (mothers n=10, infants n=10, adult males n=19, adult female, non-mothers n=8). The mean group size including infants for seasons 1 and 2 were 4.9 ± 0.9 and 4.3 ± 0.6, respectively for a mean group size of 4.6 ± 0.8 individuals.
2.3.3. Sampling methods Each P. coquereli group was followed for one day per week using ten minute continuous focal sampling (Altmann 1974) to collect infant carrier and transport position data for 6 hours beginning at dawn after groups were located in their sleeping trees. All-occurrence sampling (Altmann 1974) was used to collect data on bodily contact between mothers and infants. The number of occurrences where mothers initiated and broke bodily contact with infants and the numbers of occurrences where infants initiated and broke bodily contact with mothers (adopted from Bardi et al. 2003; Hinde and Atkinson 1970) were recorded simultaneously with infant carrier and position (see Tables 2.3, 2.4 for focal data columns and ethogram). The focal animal was alternated weekly between mothers and infants for a total of 678 focal hours (see Table 2.5
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for focal hours by group and individual). Adult females were established as mothers when infants were first seen attached on the nipple prior to the first focal follow by the principle investigator. Nursing behavior was not recorded because suckling duration cannot be distinguished from time spent on the mother (Cameron 1998; Cameron et al. 1999).
Only P. coquereli groups with infants that were a maximum of four weeks postnatal were followed and only one infant was present in all groups (see Table 2.6 for infant birth months). The same group, Zaza, was followed during seasons 1 and 2 as the season 1 infant was absent from the group and presumed dead at the beginning of season 2 when a newborn infant was present. Groups were first located when no infants were present. These same groups were rechecked weekly until an infant was present (n=9). For example, Group Rambo was first located with no infant present on 05/28/2011, subsequently located on 06/06/2011 with no infant present, and relocated on 06/11/11 with an infant present. Therefore, the infant was a maximum of 5 days old. The number of days that elapsed between the initial and subsequent group locations determined maximum infant age. Age was estimated based on speaking with local guides and comparing relative body size to the other study infants (n=9) by taking photographs of each infant in the instance where the infant was present when the group was first located (n=1).
2.3.4. Data analysis Box and whisker plots illustrating infant transport position and carrier identities were constructed by converting the total weekly focal times (hours: minutes: seconds) for each group and converting it to a percentage. For example, if an infant spent 3:00:00 (the total continuous focal time) ventrally, this was converted by the following formula:
(=hour [3:00:00] +minute [3:00:00]/60+second [3:00:00]/3600).
This value was then converted by the following formula: (=3.00/3*100) to yield a percentage, in this case 100%. Box and whisker plots were created from the average percentage of time for each postnatal week, weekly minimum, first quartile, second quartile (median), third quartile, and weekly maximum. These values were used to create boxes from the 25 th, 50th, and 75th percentiles. Whiskers were created from subtracting weekly minimums from the first quartile and the third quartile from maximums. Data were not available on infant transport by adult
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females in week 26 as no adult females were present in observed groups.
Mixed effects linear regression models in SAS® Version 9.2 were applied to determine the relationship between the independent variable, infant age (1-26 weeks postnatal) and the dependent variable, carrier position (ventral, dorsal, or independent). Mixed effect linear regression models use structured covariance models to show dependence among observations within individuals (SAS/STAT® 2010), and were selected for their robusticity to missing values. Data were log transformed prior to statistical analyses and met the assumption of normality. The covariance structure is applied in repeated measure designs to control for potential observational dependence between individuals. All effects in this model were fixed. Mixed effects linear regression models determined the relationship between infant age and the dependent variable, time spent on carriers (mothers, adult males, adult females). A Poisson regression using a PROC GENMOD procedure designed to fit generalized linear models measured the significance between infant age and the number of occurrences mothers initiated and broke bodily contact with infants, and the numbers of occurrences infants initiated and broke bodily contact with mothers. All analyses were conducted in SAS® Version 9.2. Maps were created in ArcGIS® software version 10.0.
2.4. Results 2.4.1. Infant transport position: Ventral There was a negative relationship between P. coquereli infant age and percentage of time spent ventrally (Figure 2.2). Infants (n=10) were almost exclusively transported ventrally from weeks 1-5 postnatal by all carriers (n=37), with a median above 90% until week 6. The average was 96.69% in week 1 and 6.56% in week 26. Infants consistently spent the most time ventrally during 1-5 weeks postnatal, with the least amount of variation during weeks 1-3 postnatal. The minimum percentage of time infants spent ventrally increased in week 6 relative to weeks 1-5. Weeks 7-15 showed a relatively consistent decrease in time spent ventrally, with weeks 10 and 11 showing greater overall variation than preceding weeks. The mean in week 16 was slightly higher than week 15, but the overall range is comparable. Considerable variation was present during weeks 7-18. Weeks 17-26 showed consistent decreases in time spent ventrally. Min/max variation decreased beginning in week 22.
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2.4.2. Infant transport position: Dorsal There was a positive relationship between P. coquereli infant age and percentage of time spent dorsally on all carriers until week 19 (Figure 2.3). Infants were not transported dorsally in weeks 1-2 postnatal. The average was 0.00% in week 1 and 22.21% in week 26. Infants were transported dorsally in very low percentages (|t|
236.36 -13.19 -52.17 -31.45 -33.93 -23.36 -54.55 -30.36 -14.23 -0.38
10.95 11.48 9.90 10.18 9.81 10.74 9.72 10.05 8.80 8.16
16 16 16 16 16 16 16 16 16 16
21.58 -1.15 -5.27 -3.09 -3.46 -2.18 -5.61 -3.02 -1.62 -0.05
1 km from a nonforest edge) were reduced nearly 80% during the same time span (Harper et al. 2007). The preferred habitat of many lemur species, including Propithecus spp., falls within the core forest range (McGoogan 2011). Recent geospatial analysis predicted that many lemur species will experience substantial reductions in habitat ranges exclusively attributed to climate change (i.e., models do not take into account sociopolitical factors, biotic interactions, etc.) (Brown and Yoder 2015). Appropriate lemur habitat does not exist in many of these geographic areas between the current and future predicted ranges, which will result in lemurs being unable to travel in search of new habitat (Brown and Yoder 2015). Lemur reproduction and infant survival have already been shown to be dependent on climatic variability (Dunham et al. 2011; Gould et al. 1999). Additional environmental pressures caused by climate change in habitats already highly compromised is of great concern, particularly for the health, survival, and relationship between mothers and their infants. A political crisis has plagued Madagascar since a coup d’état occurred in 2009. Since then, the country has experienced a devastating increase in environmental crimes
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including tremendous surges in hardwood timber extraction and illegal bushmeat hunting (Barrett and Ratsimbazafy 2009). The withdrawal of foreign aid along with continued political and socioeconomic instability have only intensified environmental crime and poverty, since little or no governmental regulation is present (Barrett and Ratsimbazafy 2009). Dry deciduous forests are one of the most degraded biomes in the world as a result of large-scale logging (Schwitzer et al. 2013). Less than 3% of the dry deciduous forest cover remains in Madagascar (Smith 1997), and the Ankarafantsika region is the largest remaining dry deciduous forest block (Ganzhorn et al. 2001; Schwitzer et al. 2013). The tree identification of the genera and/or species selected by lactating P. coquereli in chapter three of my dissertation can be implemented as a conservation management tool. The trees selected can be replanted in the Ankarafantsika region to help ensure P. coquereli have adequate resources during the dry season.
The hunting and consumption of bushmeat, the meat derived from wild animals, already has had calamitous ramifications throughout western and central Africa (Walsh et al. 2003). Increased zoonotic disease transmission (e.g., Ebola outbreaks) and predicted species extinctions have been directly correlated with bushmeat hunting and its consumption (Brashares et al. 2001; Chapman et al. 2005; Gillespie and Chapman 2008; Leroy et al. 2004; Rwego et al. 2008). For example, the indri (Indri indri) and diademed sifakas (Propithecus diadema) currently face extirpation in northwestern Madagascar (Jenkins et al. 2011). The demand for bushmeat has recently been on the rise in Madagascar, with disturbingly high consumption rates documented for protected species, including those listed as critically endangered by the IUCN (Jenkins et al. 2011; Randriamamonjy et al. 2015; Razafimanahaka et al. 2012; Schwitzer et al. 2014). Geographic cultural taboos that had previously prevented bushmeat consumption in Madagascar have become futile, and the demand for bushmeat continues to grow with the influx in human migration across the country (Jenkins et al. 2011). Madagascar is one of the poorest countries in the world, with more than 92% of the population living on less than $2 USD per day (World Bank 2013). This staggering statistic makes lemur conservation immensely difficult; however, the promotion of ecotourism, creation of protected areas managed by Malagasy citizens at a community level, and the expansion
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of long-term research presence will assist in decreasing hunting while simultaneously alleviating poverty (Schwitzer et al. 2014).
Bushmeat is often critical food source for the rural poor in continental Africa and Madagascar (Gardner and Davies 2013; Jenkins et al. 2011; Randriamamonjy et al. 2015). Bushmeat markets are both local and commercial; however, a new market has emerged in recent years focused on selling lemur bushmeat as a luxury commodity to consumers in Madagascar (Barrett and Ratsimbazafy 2009; Schwitzer et al. 2014). The transformation from lemurs being hunted on a relatively subsistence-based, local scale to being exploited as a national urban delicacy is particularly concerning given the magnitude at which environmental crime presently occurs. Commercial exploitation is more environmentally harmful than subsistence hunting due to the demand for high meat volume, high commercial prices bushmeat fetches at markets, and infrastructure built in forested habitats to develop and maintain these operations (Alvard et al. 1996; Fa et al. 2003; Fa et al. 1995). Wealth is considered a primary factor influencing bushmeat consumption, as animal protein is typically more expensive than other food items (Fa et al. 2003). Nonetheless, this relationship is not straightforward since local preferences for wild versus domestic meat, access to guns/snares, and employment alternatives for hunters are crucial predictors of bushmeat consumption (Schenck et al. 2006; Wilkie and Carpenter 1999). Hunting bushmeat is less expensive than purchasing domestic meat from local markets, though recent studies agree bushmeat is less preferred by rural Malagasy to domestic meat and fish (Gardner and Davies 2013; Jenkins et al. 2011). It is important to note that this tendency may be changing in accordance with migrations and the trend of bushmeat being viewed as a commercial, luxury commodity. P. coquereli are particularly susceptible to hunting, as their large body size and diurnal activity pattern make easy targets for hunters. Additionally, slow life histories make it very difficult for P. coquereli populations to recover from hunting pressures. Introducing inexpensive, readily available protein substitutes to bushmeat that appeal to urban and rural residents alike, while enforcing wildlife and firearm laws are crucial steps urgently needed moving forward (Gardner and Davies 2013; Jenkins et al. 2011; Randriamamonjy et al. 2015; Razafimanahaka et al. 2012).
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There are many feral dogs living in the forested areas surrounding the village of Ampijoroa. These dogs pose a direct threat to all flora and fauna in Ankarafantsika National Park. I personally witnessed a feral dog attack an adult male sifaka in October 2011. I recommend that all dogs residing in the park be spayed or neutered annually, at minimum. Local dogs could be trained as conservation detection dogs to protect all animals living in the park. Conservation detection dog organizations are currently having success in reducing poaching and illegal wildlife trafficking in other parts of the developing and developed world. Trained professionals should euthanize injured and ill feral dogs.
A three-year emergency plan was developed by the IUCN and collaborating scientists in 2013 for conserving lemurs throughout Madagascar (Schwitzer et al. 2013). Scientists with long-term research projects established in Ankarafantsika National Park outlined their site-specific strategy with recommendations to permanently establish forest wardens, forest agents, researchers, and conservationists in the Ankarafantsika region to promote long-term protection of the ecosystem (Radespiel and Razafindramanana 2013). Advanced training in biodiversity assessment and monitoring by park personnel is another key component to improve patrolling, anti-fire, and anti-poaching efforts in Ankarafantsika National Park (Radespiel and Razafindramanana 2013). Rapid assessment programs, especially in more remote areas of the park, occurring on an annual basis will help monitor species livelihoods (Radespiel and Razafindramanana 2013). Lastly, conservation education programs in villages, and regular meetings with village elders on conservation related issues throughout Ankarafantsika National Park is essential to the success of the lemur conservation plan (Radespiel and Razafindramanana 2013).
5.5. Evolutionary implications Individual variation is the fundamental unit of natural selection, and maternal effort is the primary determinant of offspring fitness (Maestripieri and Mateo 2009). Maternal effects are most relevant in mammalian evolutionary dynamics, and expressly in primates, due to the extensive care-giving influencing offspring even after the weaning process (Reinhold
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2002). However, evaluating maternal effects in an evolutionary and adaptive context has only been considered relatively recently in wild animals (Bernardo 1996). My dissertation examined how lactating P. coquereli behaviorally, nutritionally, and physiologically responded to a stochastic environment. Few studies have focused on the process of transitional feeding in strepsirhines, where infants receive nutrition from milk and solid foods (Sellen 2007). This will advance current discussion in evolutionary anthropology and biology on the importance of maternal care-giving.
The paleobiological record shows evidence of the adaptive significance of hominid maternal care-giving strategies in stochastic environments (Foley 1995). Hominids are specious, suggesting high variability in maternal care-giving strategies relative to modern humans (Anton 2007). Relatively large brain size is a defining characteristic in human evolution and is associated with high metabolic expenditure of maintaining this organ (reviewed in Foley 1995). Increased encephalisation is correlated with this increased energetic demand, thereby requiring mothers to invest in energetically expensive offspring (Foley 1995). My dissertation and future studies of extant lemur maternal-infant relationships will provide insights to early changes in pre-australopithecine maternal life histories and reconstructing ancestral social organization. My research will assist in understanding the emergence of derived human characters. For example, the emergence of bipedality and alloparental care were dependent on hominid weaning strategies (Sellen 2007).
Malagasy strepsirhines are the most basal extant representations of Eocene primates, such that Microcebus spp. are typically considered a living depiction of fossil taxa, as they are most closely representative extant genus to the proposed ancestral weight (10-15 g) of the very first primates that were shrew-sized (Gebo 2004). Some species of subfossil lemurs briefly coexisted with human populations until extinctions resulting from human colonization and overhunting (Burney et al. 2004). Behavioral studies of extant lemurs will serve as models for innovative theories on primate evolution and subfossil lemur extinctions in Madagascar. This study will contribute to the ongoing debate on the evolution of maternal care strategies in early primates and hominids.
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