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Maternal Effort, Food Quality, and Cortisol Variation During Lactation in Propithecus Coquereli in Northwestern Madagascar

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Maternal Effort, Food Quality, and Cortisol Variation During Lactation in Propithecus Coquereli in Northwestern Madagascar 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. iii Dedication To my exceptional father, Bill Ross (1950-2016)—a natural born world shaker. iv 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. v 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.
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