Influences on Lactation Length and the Timing of Weaning Events in Colobus Vellerosus

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2016-01-29 Influences on Lactation Length and the Timing of Weaning Events in Colobus vellerosus

Crotty, Angela

Crotty, A. (2016). Influences on Lactation Length and the Timing of Weaning Events in Colobus vellerosus (Unpublished master's thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/26523 http://hdl.handle.net/11023/2800 master thesis

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UNIVERSITY OF CALGARY

Influences on Lactation Length and the Timing of Weaning Events in Colobus vellerosus

Angela M. M. Crotty

A THESIS

SUBMITTED TO THE FACULTY OF GRADUATE STUDIES

IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE

DEGREE OF MASTER OF ARTS

GRADUATE PROGRAM IN ANTHROPOLOGY

CALGARY, ALBERTA

JANUARY, 2016

Abstract

I explored variation in maternal investment strategies. I investigated whether infant sex, food availability, female feeding competition or infanticide risk influenced lactation length, the context of nursing cessation and the extent to which mothers can simultaneously gestate and lactate in a wild colobine. I combined long-term records and new observations of Colobus vellerosus. I extracted 40 nursing cessations, 13 exact lactation lengths, and 26 durations between nursing cessation and subsequent births. The independent variables did not influence lactation length, and nursing cessation did not differ by infant sex or cluster with food availability. Lactation length, maternal age, infant sex, infanticide risk, feeding competition, and potential infant handlers available did not influence the duration length to the next birth. This study eliminated some potential variables that may have explained nursing cessation and lactation length variation in our species, although it is evident that other underlying factor(s) are causing the variation.

Acknowledgements

I am forever fortunate and grateful for my supervisor Dr. Pascale Sicotte, for taking a shot on a rough-around-the-edges Maritimer like myself. From your trust and often tedious investment, I have gained invaluable work ethic, courage and the confidence to achieve anything.

I am also thankful to Drs. Linda Fedigan, Warren Wilson, Peter Dawson and Steig Johnson for taking the time and consideration to serve as my proposal and/or defense committee members.

Thank you to the Ghanaian Wildlife Division and the people of Boabeng and Fiema for allowing me to live and conduct research in their beautiful forest. I am incredibly fortunate for the funding provided by the Graduate Research Scholarship, University of Calgary Research

Committee scholarship and the Department of Anthropology and Archaeology. An enormous thank you to the Department of Anthropology and Archaeology, specifically the wonderful staff

(Monika Davison, Julie Boyd and Courtney Wright) running the administration for solving any unforeseeable problems I had without a hitch. Thank you to Dr. Fernando Campos for sharing your R genius, Dr. Tak Fung for solving my mixed model confusion and Dr. Urs Kalbitzer for advice.

This project would not have been possible without the generous access to the long-term

BFMS records collected by Dr. Eva Wikberg, Lisa MacDonald, Josie Vayro and Stephanie Fox.

I vividly remember how difficult it is to collect every piece of data, and I appreciate you sharing your hard work with me. To my Canadian field assistants Bethany Hansen and Rebecca

Ollenberger – you two are an inspiration in work ethic, determination, and positive attitude. I am forever grateful to you two for keeping me from becoming malnourished, picking off ants and saving me from falling over. If given the chance, I would choose you again. To my two

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Ghanaian assistants, Robert Korangteng and Charles Kodom, I appreciate your endless work ethic, jokes, Twi lessons and friendship.

I am forever indebted to Josie Vayro for her patience, tips and life-long friendship. I am eternally grateful that we sat beside one another in the van so many years ago – it has ‘mostly’ been a pleasure. Thank you to my University of Calgary network, especially Monica Myers,

Stephanie Fox and Mackenzie Bergstrom for your friendship, wine/beer and assistance whenever asked.

Ultimately, none of this would have been imaginable or achievable without the help of my loving “loan shark” parents, brothers and life-long friends that have all stuck it out with me.

Thank you for the never failing encouragement, love and the perspective you gave when things seemed tough.

Dedication

To the wonderful people of Boabeng and Fiema: thank you for teaching me the true meaning of hard work, happiness and life in general. If the world were as generous, welcoming and appreciative as you are, it would be a beautiful place.

Table of Contents Abstract ...... ii Acknowledgements ...... iii Dedication ...... v Table of Contents ...... viii Table of Figures ...... ix

CHAPTER ONE: OVERVIEW ...... 1 1.1 Introduction ...... 1 1.2 Literature review ...... 2 1.2.1 Constraints on Lactation length ...... 2 1.2.2 Primate lactation ...... 3 1.2.3 Weaning age as a life history variable ...... 5 1.2.4 Colobine life history characteristics ...... 7 1.2.5 Factors influencing intra-specific variation in lactation length ...... 10 1.2.5.1 Food availability and group size as influential factors ...... 10 1.2.5.2 Infanticide as an influential factor ...... 13 1.2.5.3 Simultaneous gestation and lactation ...... 16 1.3 Thesis aims ...... 18 1.3.1 Hypotheses and predictions ...... 18 CHAPTER TWO: METHODS ...... 22 2.1 Study Site ...... 22 2.2 Study Species ...... 22 2.3 Data Collection ...... 24 2.3.1 Demographic data table and study subjects ...... 24 2.3.2 Phenological Data ...... 25 2.4 Data Analysis ...... 26 2.4.1 Analysis Part One: Factors influencing lactation length ...... 26 2.4.1.1 The effect of sex ...... 27 2.4.1.2 The effect of male group composition ...... 27 2.4.1.3 The effect of adult female group size ...... 27 2.4.2 Analysis Part Two: Analyzing the Context of Nursing Cessation ...... 28 2.4.3 Analysis Part Three: Duration between nursing cessation and subsequent birth ...... 31 2.4.3.1 The correlation between lactation length and duration to the next birth ...... 32 2.4.3.2 The effect of sex on duration to the next birth ...... 32 2.4.3.3 The effect of maternal age on duration to the next birth ...... 32 2.4.3.4 The effect of male group composition on duration to the next birth ...... 32 2.4.3.5 The effect of female group composition on duration to the next birth ...... 33 2.4.3.6 The association between duration to the next birth and the number of available potential infant handlers ...... 33 vi

2.4.3.7 The influence of food availability on duration to the next birth ...... 33 CHAPTER THREE: RESULTS ...... 36 3.1 Lactation length ...... 36 3.1.1 Description of lactation length ...... 36 3.1.2 The effect of sex on lactation length ...... 38 3.1.3 The effect of male group composition ...... 39 3.1.4 The effect of adult female group size ...... 40 3.2 Context of nursing cessation ...... 42 3.2.1 Annual distribution of nursing cessation events ...... 42 3.3 Nursing cessation events in relation to the subsequent birth ...... 43 3.3.1 Description of nursing cessation in relation to the subsequent birth and gestation ..... 43 3.3.2 Sex differences in duration to the next birth ...... 44 3.3.3 The effect of maternal age on duration to the next birth ...... 45 3.3.4 The effect of male group composition to the next birth ...... 46 3.3.5 The effect of adult female group size ...... 47 3.3.6 The association between duration to the next birth and the number of potential infant handlers available ...... 47 3.3.7 The effect of food availability on duration to the next birth ...... 48 CHAPTER FOUR: DISCUSSION ...... 51 4.1 Summary of key results ...... 51 4.2 Lactation length in Colobus vellerosus ...... 52 4.3 Counter-strategy to infanticide hypothesis ...... 54 4.4 The food availability hypothesis ...... 56 4.5 Simultaneous gestation and lactation ...... 57 4.6 Directions for future research ...... 58 4.7 Conclusion ...... 59

REFERENCES ...... 60 REFERENCES FOR TABLE 1.0 ...... 72

APPENDIX: DATA TABLES FOR ANALYSES...... 75 A.1. Lactation length data ...... 75 A.2. Individuals for the analysis of the context nursing cessation events ...... 76 A.3. Data set for lactation length and duration to next birth correlation ...... 77 A.4. Data set for duration to next birth analyses...... 78

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List of Tables

Table 1.0. Life history and reproductive parameters of African and Asian colobines ...... 9

Table 2.1. Duration to next birth sample sizes in four food availability contexts ...... 35

Table 3.1. Description of the durations in each of the four food availability contexts ...... 49

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List of Figures Figure 2.1. Mean Phenological Scores per Plant Part 2014/2015 ...... 29

Figure 3.0. Lactation length sample with and without outlier ...... 37

Figure 3.1. Normality deviation distribution Q-Q plot of lactation length ...... 38

Figure 3.2. Lactation length by sex ...... 39

Figure 3.3. Lactation length by adult male group composition ...... 40

Figure 3.4. Lactation length by adult female group size ...... 41

Figure 3.5. Nursing cessation circular histogram ...... 42

Figure 3.6. Raw nursing cessation circular distribution by sex ...... 43

Figure 3.7. Nursing cessation-subsequent birth duration in days by sex ...... 44

Figure 3.8. Boxplot of the duration to next birth of young and old mothers ...... 45

Figure 3.9. Duration to next birth in uni-male and multi-male groups ...... 43

Figure 3.10. Scatterplot illustrating of number of adult females and duration ...... 46

Figure 3.11. Scatterplot illustrating potential infant handlers and duration ...... 47

Figure 3.12. Duration to next birth in different food availability contexts! ...... 48

Chapter One: Overview

1.1 Introduction

Life history characteristics are a species-specific suite of mean ages and durations of life stages, determined by reproductive trade-off decisions (Fisher 1930), sources of extrinsic mortality such as predation and infanticide (Promislow & Harvey 1990; Charnov 1993), and phylogenetic constraints (Hayssen 1993). While the evolutionary history of a species does create phylogenetic limitations to the amount of variation possible within life history characteristics, inter-individual variation does occur. Inter-individual variation in life history characteristics are the result of different trade-off “decisions” that have evolved to maximise reproductive success in response to varying ecological and social pressures (Fisher 1930; Harvey & Read 1988; Smith

1988; Lee 1996; van Schaik & Isler 2012). Inter-individual variation in the length of lactation and the timing of nursing cessation events are the result of maternal decisions to terminate or increase the investment in their offspring. These investment decisions are the result of a combination of factors including infant nutritional demands, maternal energetics (such as simultaneous gestation and lactation), as well as ecological (e.g., food availability) and social pressures (e.g. infanticide and group size/composition) (Lee 1996; Ross & Jones 1999).

The focus of this thesis is to investigate maternal investment strategies in a population of wild primates by exploring the variation in lactation length and the timing of nursing cessation events, and by attempting to link these data to the social and ecological context of the mothers and their infants at the time. The aim of the literature review is to provide information on the topic of primate lactation, and to explore possible explanations for intra-specific variation in

lactation length and the timing of nursing cessation. In the following paragraphs, I first describe the maternal energetic constraints of lactation, and how primate lactation, specifically lactation in colobines, differs from other mammals. I also discuss the past difficulties of characterizing weaning age as a standard life history characteristic, predominately because of the issues around the definition of what weaning is. These difficulties have resulted in a lack of systematic data collection on the topic of weaning, which in turn, limits our ability to conduct cross-species comparisons. Weaning age, or the age of infant independence, is not often used as a life history characteristic despite its potential usefulness (Lee 1996; Borries et al. 2014). I then describe some of the factors known to influence the inter-individual variation in lactation patterns within and between primate populations. Lastly, I outline the aim of this thesis, as well as my hypotheses and predictions.

1.2 Literature review

1.2.1 Constraints on Lactation length

Female mammals are energy and time constrained for much of their reproductive lives

(Hayssen 1993; Ross & Jones 1999; van Schaik & Isler 2012). Energy is primarily allocated to reproductive processes during this period, thereby limiting the amount of energy available for individual body maintenance, repair and other physiological processes (Ross & Jones 1999; van

Schaik & Isler 2012). Maternal investment in mammals is the energy that mothers direct to their current offspring and can be divided into two phases: pre-natal, which includes gestation, and post-natal, which includes lactation (Boyce 1988; Altmann & Samuels 1992; Langer 2008). The mammalian post-natal phase is the most energetically expensive period of a female’s lifetime

(Boyce 1988; Altmann & Samuels 1992). The energetic costs of lactation are further exacerbated

by infant carrying, a form of infant care found in most diurnal primates (Altmann 1980; Altmann

& Samuels 1992; Ross 2001). Mothers employ several strategies to compensate for the increased energy expenditure associated with lactation. For example, by increasing foraging time to gain more energy (Altman 1980; Dunbar & Dunbar 1988; Koenig et al. 1997), reducing activity levels in efforts to conserve energy (Barrett, Halliday & Henzi 2006), using sources of stored energy (Knotts 1998), receiving allocare from conspecifics (Mitani & Watts 1997), and by readjusting their time budgets to accommodate nursing (Hayssen 1993). These strategies may result in a reduction of the amount of time available for social interactions (Altman 1980;

Barrett, Halliday & Henzi 2006). Human females also use strategies to cope with the high energetic cost of lactation, particularly by increasing food intake, reducing activity, and using stored energy (Piperata 2009). The strategy favoured to offset the energetic demands of lactation may result from the interactions between maternal age and/or experience (Promislow & Harvey

1990; Fairbanks 1993; Johnson 2006), group dynamics (Palombit et al. 2000; Henzi & Barrett

2003), the availability of potential infant handlers (Mitani & Watts 1997), and food quality and/or availability within the habitat (Barrett, Halliday & Henzi 2006). The use of different strategies to counterbalance the energy expenditures of lactation may result in variation in infant survival and reproductive rates between mothers (Brockman & van Schaik 2005; Emery

Thompson 2013). Amongst primate mothers, the quality and quantity of maternal investment is highly variable (Oftedal 1984).

1.2.2 Primate lactation

Across mammals, the length of lactation positively correlates with maternal mass

(Hayssen 1993). Maternal mass and the amount of energy available determine the pace of infant

growth from birth to nutritional independence (Charnov & Berrigan 1993; Ross & Jones 1999).

Infant suckling rates are highest in the first months of life, which is the most crucial infant growth period, and then begin to slowly decline until complete cessation (Gomendio 1989).

Lactation length and the duration of infant dependence is longer in primates compared to other mammals, even when controlling for maternal mass (Nicolson 1987; Hayssen 1993; Kappeler et al. 2003). The longer length of lactation observed in primates may be due to additional time required for neurological development, learning foraging techniques and/or social navigation

(Hayssen 1993; Ross & Jones 1999).

Lactation length and weaning age vary considerably within primates (Harvey 1990).

Phylogeny and, by extension, maternal mass set a species-specific weaning weight threshold, or an optimal point at which an infant can be successfully weaned (Bowman & Lee 1995). Intra- specific variation from this constant may be a function of individual rearing strategies (Ross

1991). The composition of maternal milk is an evolved result of the species-specific compromise between maternal nutritional stress and optimal infant growth and development needs (Prentice

& Prentice 1995). In humans, breast milk varies both over time and between women (Emmett &

Rogers 1997). Variation in lactation length and the timing of nursing cessation may be due to maternal decisions to terminate investment based on infant nutritional demands, infant growth rates and ecological and/or social pressures (Oftedal 1984; Lee 1996; Ross & Jones 1999), or potentially the beginning of the mother’s investment in the next offspring (Trivers 1972, 1974;

Fairbanks 1993). The extent to which mothers can vary on the early to late weaning continuum within a species is unknown, though ultimately the extent of variation is constrained by phylogeny.

1.2.3 Weaning age as a life history variable

Weaning is not often considered a standard life history characteristic due to its unclear

definition (Lee 1996; Borries et al. 2014). Indeed, because it can be conceptualized as either a

process or as an event, definitions have often varied between studies. Ambiguity, or difficulties

in the definition of the notion of weaning has resulted in a lack of consistency between studies,

thereby limiting the potential for cross-species comparisons (Lee 1996; Borries et al. 2014).

Weaning has previously been defined using three perspectives. First, from a theoretical

perspective, it is defined as the process of a gradual decline in maternal investment, indicating a durational behaviour with an end point (Altmann 1980; Dunbar & Dunbar 1988; Lee 1996).

Second, from an infant growth and maternal energy perspective, infants have been considered weaned following either: i) the point of peak lactation or the maximum lactation threshold

(Borries et al. 2014); or ii) by infant weight (e.g., one-third of adult weight, Charnov & Berrigan

1993; 3-4 times birth weight, Bowman & Lee 1995; Hayssen 1993); each of which indicate a specific, yet likely different point in time. Lastly, it has also been defined as the end of infancy or the beginning of nutritional independence (Borries et al. 2014), again measured as a specific moment in time. Each definition derives from a different perspective with a different set of initial questions and provides different avenues regarding the appropriate approach to studying weaning in wild primates.

Various measures have been used to assess weaning as either a process or a point in time,

although each is problematic. First, some researchers have focused on the onset and/or the

intensity of mother-infant conflict (Trivers 1974; Altmann 1980; Barrett et al. 1995), although

weaning is not the only possible cause of mother-infant conflict (Lee 1996). Others have focused

on infant age: at the eruption of the M1 molar to establish the onset of weaning (Schultz 1935) or

the age at which the infant can survive without its mother (Lee 1996), or the age at which the mother resumes cycling (Lee et al. 1991; Koenig et al. 1997). Lastly, the age of first solid food ingestion has been proposed as a proxy for the onset of weaning. This is indeed a measure that can be observed. However, it is clear, particularly in species with multi-season lactation, that there is a substantial time lag between the age of first solid food ingestion and complete nursing cessation (e.g., years in Pan troglodytes, discussed in Borries et al. 2014; Pongo pygmaeus wurmbii, van Noordwijk, Kuzawa, van Schaik 2013 & van Noordwijk et al. 2013). Additionally, an infant’s attempts at solid food ingestion may indicate food sampling, rather than feeding for energetic benefits (Lee 1996; Watts 1985). All these measures are difficult to obtain in practice, and they are not necessarily indicative of the cessation of lactation.

Borries and colleagues (2014) have recently advocated for the consolidation of research methods in efforts to fully understand weaning, and to ultimately establish the “end of infancy” as a life history characteristic. They proposed the use of the measure “nipple contact cessation”, or the last date observed where an infant had the nipple in its mouth, which presumably should be associated with the cessation of nursing. This is a reliable behavioural trait, and a measureable indicator of infant independence and the end of maternal investment, although it may not, in reality, coincide with the complete cessation of milk transfer. The infant age on the last date observed suckling does not significantly differ from the ages of other weaning proxies such as the M1 molar eruption, mother cycle resumption and mother re-conception (discussed in Borries et al. 2014). This measure should be used with caution, as the presence of suckling is not entirely indicative of milk transfer. Indeed, “nipple in the mouth” may not be a behaviour used only for nutritional purposes, as it can also be used for comfort suckling, and maternal protection from predators via close proximity (Lee 1987; Borries et al. 2014). In favor of this measure, however,

is the recent finding (through fecal isotope analysis), that even low nursing rates supplement an infant’s diet to some extent (Reitsema 2012). In conclusion, using cessation of nipple contact as a measure to gauge maternal investment and nursing cessation is both cost and time efficient, and seems to be a useful measure that is also biologically meaningful.

1.2.4 Colobine life history characteristics

Relative to frugivores (and controlling for body size), folivorous primates have slow life histories with longer gestation and lactation lengths (Lee 1999; van Schaik & Isler 2012).

However, it is unclear if this results from a folivorous diet and/or from an arboreal lifestyle, as these two factors are both associated with lower mortality rates and slower life history trajectories (Charnov 1991; Ross 1992; Borries et al. 2011; van Schaik & Isler 2012). This trend is associated with a low maternal metabolic rate and an increase in the amount of time required for the growth of infant teeth and/or specialized stomachs (Ross 1992; Borries et al. 2011). As in many other mammals, maternal milk in colobines acts as a buffer to the quality, quantity and toxicity of adult foods (Pond 1977; Langer 2008). Furthermore, colobine digestive tracts require the slow inoculation and colonization of microbes to enable effective fermentation and digestion of fibrous plant cell material (Langer 2003). Therefore, to enable a functional digestive system in colobine infants, a long lactation period is required for the chamber growth within the sacculated stomach (Langer 2003). The transition from milk to solid food, or the "mixed-feeding phase", is particularly difficult in infants of folivorous species because they transition from an easily digestible fibre-free diet to a highly fibrous diet (Edwards et al. 2006). In this phase, infants develop a microbial population that requires the slow introduction of plant-based foods (Langer

2008), and this development impacts the optimal time of nursing cessation (Edwards et al. 2006;

Borries et al. 2011).

A large range of variation exists within the colobinae subfamily in regards to female reproductive strategies and the amount of time mothers invest into lactation (Table 1.0). Species range from seasonal to aseasonal breeders, which can even vary intra-specifically (e.g., Colobus polykomos; DaSilva 1989). Lactation length also varies considerably throughout the colobinae subfamily both within and between species (Table 1.0). Few studies have exhaustively explored the causal factors of the variation at the population level, although it is likely due to the availability of high quality food (Lee et al. 1991), group dynamics, and maternal condition

(Janson & Verdolin 2005; van Noordwijk et al. 2013), or a combination of these factors.

Table 1.0 Life history and reproductive parameters of African and Asian colobines Species Common Birth Season; Gestation IBI Lactation Name Peak Length (d) Length (d) Colobus angolensis Angola Black & Aseasonal1 No data No data No data White Colobus Colobus guereza Eastern Black & Aseasonal2 1583,4 265 m 3346 White Colobus 21.53 m 3907 25.28 m 17.57 m

Colobus polykomos Western Black Varies by site10 1707 5847 3657 & White 18610 2410 m Colobus 12.57 m Colobus santanas Black Colobus Seasonal11 19512 No data 48013 Procolobus badius Western Red Aseasonal; 17015 29.47,17 m 773.815 Colobus bimodal birth 5.257, 16 m peak14

Procolobus verus Olive Colobus Seasonal18 16919 No data 36519 Nasalis larvatus Proboscis Aseasonal; 16620,3 5493, 20 2813, 20 Monkey bimodal birth peak32 Pygathrix nemaeus Red-shanked No data 21021 49521 33021 Douc Langur Semnopithecus Hanuman Seasonal22 19923 51123 38923 entellus Langur 211.524 17.23,7 m 41625 16825 32.47,26 m

Semnopithecus Purple-faced Seasonal33 20027 71427 22827 vetulus Langur 197.528 23.5 7,28m Trachypithecus Dusty Leaf Seasonal29 15229 73129 m 36529 obscurus Monkey Trachypithecus Phayre's Leaf Aseasonal, birth 205.330 22.37,31 m No data phayrei Monkey peaks31 m Indicated results were reported in months; 1 Fimbel et al. 2001, n=300; 2 Oates 1977, n=80; Struhsaker & Leland 1979; Harris & Monfort 2006, n=10; 3 Harris & Monfort 2006, n= 4; 4 Dunbar 1984; Godfrey et al. 2001; Lee et al. 1991, cited in van Schaik & Isler 2012; 5Korstjens et al. 2002, n=5; 6 Cited in van Schaik & Isler 2012; 7 Napier & Napier 1967; Rowell & Richards 1979, n=16 intervals from 4 females; Chapman, Walker & Lefebvre 1990; 8 Oates unpublished data n=<5 cited in Struhsaker & Leland 1987; 10 Sabater Pi 1973; 11 Harvey & Clutton-Brock 1985 (cross-species comparison); 12 Struhsaker & Pope 1991, n=16; 13 Struhsaker 1975 unpublished data, n= >20, published in Struhsaker & Leland 1987; 14 Struhsaker 1975, n= >20; 15 Starin 1988, n= 4; 16 Starin 1991; 17 Oates 1994; 18 Korstjens 2001, n=6; 19 Godfrey et al. 2001 (primate cross-species comparison); Gorzitze 1996, n=2; 20 Lippold 1981, n=2 captive, Harvey & Cluttonbrock 1985; Lee 1999; Lindenfors 2002; 21 Borries et al. 2001 n=17 gestations, n= 72 IBI, n=23 lactation lengths; 22 Sommer et al. 1992, n=32 pregnancies, n=28 IBI; 23 Ziegler et al. 2000, n=9; 24 Koenig et al. 1997, n=23; 25 Borries & Koenig 2000; 26 Godfrey et al. 2001; Lee et al. 1999; Lekagul & Mcneely 1977; 27 Rudran 1973; 28 Badham 1967, captive n=2; Godfrey et al. 2001; Struhsaker 1987; 29 Borries et al. 2011, n=40 IBI; 30 Lu 2009; Lu et al. 2010, n=7; 31 Boonratana 1993; 32 Harms 1956; 33Jay 1965.

1.2.5 Factors influencing intra-specific variation in lactation length

1.2.5.1 Food availability and group size as influential factors

The length of lactation may be environmentally sensitive (Lee et al. 1991). In many primate species, maternal condition and female foraging strategies influence lactation length and the timing of nursing cessation (van Noordwijk et al. 2013). Individuals experience longer gestation, longer lactation lengths, and longer inter-birth intervals when they have less access to high quality resources (Semnopithecus entellus, Borries et al. 2001; Papio ursinus, Cheney et al.

2006; Trachypithecus leucocephalus, Zhao et al. 2008; reviewed in Asquith 1989). Limited access to high quality food requires mothers to invest longer in their current offspring and thereby delay investing in future reproduction (Lycett et al. 1998; Emery Thompson et al. 2012).

Females can adjust their level of maternal investment in response to the availability of quality food (Chlorocebus pygerythrus, Hauser & Fairbanks 1988). For example, during periods of low food availability lactation length may extend to allow infants to reach their optimal weaning weight (Lee et al. 1991; Lycett et al. 1998; Zhao et al. 2011). Aseasonal breeders may benefit from delaying weaning by lengthening lactation until a period of high food availability. Such a choice may result in higher infant survival without substantially decreasing a mother’s fitness relative to other females in the population. This is in contrast to a seasonal breeder, for whom delayed weaning would result in a missed breeding season (Altmann 1980; Smith 1988; Zhao et al. 2011; Beehner & Lu 2013).

In an alternative scenario, periods of low food availability could lead to a reduction of maternal care and investment in infants, in an effort to maintain maternal weight for future reproduction (Fairbanks & McGuire 1995). For example, mothers may increase nipple and proximity rejections during low food availability, resulting in high infant distress, particularly

when there is a lack of available weaning foods and/or an infant is too young to forage independently (Altmann 1980; Hauser & Fairbanks 1988; reviewed in van Noordwijk et al.

2013). The energetic costs of lactation are more substantial during low food availability periods because females experience greater metabolic loads and cannot gain enough energy from foraging to sustain themselves and a growing offspring (Clutton-Brock et al. 1989). This energetic cost can result in low milk quality (Roberts et al. 1985), and slow infant maturation rates (Semnopithecus entellus, Borries et al. 2001). For example, in humans low maternal nutritional status has been shown to result in a decreased milk volume and a lower fat content in milk (discussed in Emmett & Rogers 1997). Furthermore, potentially mothers may reach peak lactation earlier (van Noordwijk et al. 2013). In some species, low food availability results in longer recuperation periods before cycle resumption (Pan troglodytes, Emery Thompson et al.

2012). This is further evident when comparing the life history characteristics of wild populations and captive groups, where captive primates demonstrated faster rates of reproduction and infant growth (Papio cynocephalus, Altmann et al. 1981; Chlorocebus pygerythrus, Garcia et al. 2009;

Pan troglodytes, discussed in, Emery Thompson 2013; reviewed in Asquith 1989, Bolter &

Zihlman 2011). Additionally, the mother’s age may determine the strategy used (Promislow &

Harvey 1990; Johnson 2006). As maternal age increases, the value of each offspring should also increase due to the declining number of potential future offspring (Johnson 2006). Mothers seem to adjust their level of maternal care facultatively because of the relationship between food quantity, maternal condition and potential future reproductive opportunities (Hauser & Fairbanks

1988; Borries et al. 2001).

Variation in lactation length and the timing of nursing cessation may be the result of the intensity of feeding competition experienced by mothers. It was previously assumed that

folivorous primates did not experience scramble competition to the same extent as frugivorous species, as leaves were thought to be a non-contestable resource that were both uniformly distributed and of low quality (Isbell 1991; Sterck et al. 1997). In the last two decades, studies of folivorous primates have demonstrated that folivores do indeed experience scramble competition, which translates into lower feeding efficiency in larger groups, and thus lower energetic intake, in larger groups (Chapman et al. 1995; Janson & Goldsmith 1995; Chapman &

Chapman 2000; Koenig 2000; Saj & Sicotte 2007; Snaith & Chapman 2007; Teichroeb & Sicotte

2009). In some cases, contest competition is documented in some colobine species (Colobus polykomos and Procolobus badius, Korstjens et al. 2002; Colobus vellerosus, Wikberg et al.

2013). New findings also highlight that colobine females living in large groups experienced low reproductive rates. For example, these females gave birth to slower developing infants who weaned at an older age and, as a result, these females experienced longer inter-birth intervals

(Borries et al. 2008). Similar group size effects influence female reproductive rates in other primate and mammal species as well (Sterck et al. 1997; Takahata et al. 1998; Lindstrom 1999; van Noordwijk & van Schaik 1999; McComb et al. 2001; Altmann & Alberts 2003; Kumar

2005; Therrien et al. 2008). However, in some species reproductive rates are more strongly influenced by group dynamic elements such as the number of males residing in the group (e.g.,

Gorilla beringei beringei, Stokes et al. 2003; Robbins et al. 2007) and the availability of allocare. In some species, mothers experienced shorter inter-birth intervals when they resided in a group with many potential infant handlers available (discussed in Mitani & Watts 1997). The is likely because when allocare is available, females are able to increase their foraging rates, which results in faster infant growth rates, thereby ultimately providing a fitness advantage to the mother (Stanford 1992). Yet, the variation in lactation length within populations may be the

combined result of the availability of high quality food as well as group size and composition, which in turn influences both an individual’s access to food and foraging rates.

1.2.5.2 Infanticide as an influential factor

Females can also adjust their maternal investment strategies in response to the social environment, particularly in response to male reproductive strategies such as infanticide (van

Schaik & Janson 2000; Crockett & Janson 2000; Borries et al. 2001). Male infanticide is a sexually selected strategy whereby males kill unrelated infants to induce accelerated estrous in females, thereby increasing the infanticidal males’ chances of siring the next offspring (Hrdy

1974, 1977). It occurs in species where lactation is longer than gestation, females experience lactational amenorrhea (van Schaik 2000; van Schaik & Janson 2000; Borries et al. 2001) and where male tenure is brief (Hrdy 1974; Chapman & Hausfater 1979), regularly contested, and group takeovers are frequent (Teichroeb et al. 2012; Sicotte et al. 2015).

Primate groups experience varying levels of infanticide risk depending on factors such as male and female reproductive strategies, population density, population structure, and particularly the number of extra-group males in the population (Crockett & Janson 2000; Janson

2000; Steenbeek & van Schaik 2001; Teichroeb et al. 2012). Infanticide generally occurs following male takeovers in uni-male and multi-male groups, or following rank changes within multi-male groups (Borries 1997; Teichroeb et al. 2009, 2012; Zhao et al. 2011; reviewed in:

Struhsaker & Leland 1987; van Schaik & Janson 2000; van Schaik et al. 2005; Palombit 2012).

Groups containing a high number of females have been suggested to be more susceptible to male immigration attempts and takeovers, and as a result are more prone to be the target of infanticide attempts (Theropithecus gelada, Dunbar 1984; Semnopithecus entellus, Borries 1997; Alouatta

seniculus, Crockett & Janson 2000; Colobus vellerosus, Teichroeb et al. 2011). Multi-male groups in some species are argued to be composed of lower quality males who are unable to prevent takeovers, resulting in a higher risk of takeover and infanticide, relative to uni-male groups (Colobus vellerosus, Teichroeb & Sicotte 2010, Teichroeb et al. 2012, Sicotte et al.

2015). However, it has also been argued that multi-male groups experience a lower risk of infanticide because in the event of the death or disappearance of the alpha male, within group males can rise in the hierarchy and defend infants with whom they may have some level of paternity certainty (Gorilla beringei beringei, Robbins 1995; Procolobus rufomitratus, Leland et al. 1984; see Borries 1997; Borries & Koenig 2000). The pattern of male emigration seems to determine whether multi-male groups are associated with a high or low level of infanticide risk

(Broom et al. 2004). In addition, the rate of male incursions and inter-group encounters may be an additional measure of infanticide risk, because during male incursions, males are assessing the fighting abilities of their opponents (Teichroeb et al. 2011). The number of adult males and females residing in a group thus seems to be an important influence on the group’s inherent level of infanticide risk.

Male infanticide is obviously very costly for mothers. Females have evolved counter- strategies to offset the reproductive costs of male infanticide (Hrdy 1977; Ebensperger 1998;

Palombit 2012). Proposed female counter-strategies to male infanticide include: polyandrous mating (Hrdy 1979; van Schaik 2000), post-conceptive mating (Hrdy 1979; Vayro in prep), maternal aggression against infanticidal males (e.g., female-female coalitions to intra- and extra- group; van Schaik 2000) and associating with defender males (Borries 1997; Saj & Sicotte

2005). Another way in which mothers can cope with male infanticide risk is by modulating their investment toward infants. For instance, mothers can adjust their investment by abruptly weaning

their infants during high-risk situations, such as following a group takeover (Zhao et al. 2011;

Beehner & Lu 2013), or by having shorter overall lactation lengths in groups with an on-going infanticide risk. Delayed weaning during high infanticide risk situations is costly because the infant remains at risk longer (Borries & Koenig 2000; Sicotte 2000). Early and abrupt weaning may be a useful strategy because it reduces infant vulnerability by either allowing the mother to become receptive earlier (Beehner & Lu 2013) or if nipple contact cessation acts as a signal of cycle resumption to infanticidal males (Zhao et al. 2011). In a few species, abrupt weaning has been observed and may potentially act as a female counter-strategy (e.g., Chlorocebus pygerythrus: Fairbanks & McGuire 1987; C. vellerosus: Teichroeb & Sicotte, 2008a; Gorilla gorilla beringei: Watts 1989, Sicotte 2000; Papio hamadryas: Colmenares & Gomendio 1988;

Spermophilus columbianus: Dobson, 1990; T. leucocephalus: Zhao et al. 2011; discussed in

Beehner & Lu 2013). In some cases, females have weaned infants abruptly following group takeovers (Chlorocebus pygerythrus, Fairbanks & McGuire 1987; anecdotal evidence in Colobus vellerosus, Teichroeb & Sicotte 2008a, Teichroeb et al. 2009; Trachypithecus leucocephalus,

Zhao et al. 2011). In the presence of an immediate infanticide threat, counter-strategies may be limited by the infant’s age; for example an infant may be too young to become independent

(Sterck et al. 2005; Teichroeb et al. 2009; Zhao et al. 2011). In the event that an infant is too young to wean abruptly, mothers may either increase their protectiveness (reviewed in Palombit

2012) and/or shorten the overall lactation length resulting in early weaning (Beehner & Lu

2013). Lactation length variation between groups may potentially be the result of mothers facultatively adjusting their maternal investment levels in response to the threat of infanticide.

Situations of high stress such as group takeovers may have shaped females’ physiological and

behavioural responses, and may contribute to an accelerated development and earlier weaning age (Palombit 2012; Allen-Blevins et al. 2015; Bădescu et al. accepted).

1.2.5.3 Simultaneous gestation and lactation

The maternal investment conflict between current and potential future offspring may influence the length of lactation (Trivers 1972, 1974). Primate females experience postpartum lactational amenorrhea, although the length of this phase is variable (van Schaik 2000b). It is unclear whether cycle resumption triggers the weaning process or if a decrease in suckling reallocates energy into cycle resumption. In humans, a decrease in the frequency of suckling correlates with a decrease in the mother’s prolactin levels, which triggers cycle resumption

(reviewed in Ellison 1995).

Species also vary in their ability to become pregnant while lactating. In the case of seasonal breeding primates, females must reach a minimum condition threshold prior to conception (Brockman & van Schaik 2005) and use stored nutrients to support their current reproductive effort (Richard et al. 2000). These limitations exclude seasonal breeders from simultaneously gestating and lactating. In these species, the optimal strategy for individuals is to cluster their reproductive events such as ovulation, conception, birth and peak lactation, to periods of peak or high food availability (reviewed in: van Schaik & van Noordwijk 1985;

Brockman & van Schaik 2005; Janson & Verdolin 2005; Emery Thompson 2013; e.g., Saimiri sciureus, Baldwin 1968; Semnopithecus entellus; Borries 1997). Individuals who deviate from the optimal birth and weaning times risk missing the narrow time-to-conception window

(Brockman & van Schaik 2005) and thereby also risk increasing the rate of infant mortality

(Tecot 2010).

In the case of aseasonal breeding species, or income breeders, current energy intake is used to fuel reproduction and they require more energy intake for both subsistence and prolonged reproductive efforts (e.g., seen in multi-season lactators), making a capital breeding strategy energetically insufficient (Emery Thompson 2013). Income breeding females exhibit flexible reproductive timing, conception rates, and investment levels because they are not constrained by an optimum birth timing, but instead are predominantly constrained by maternal condition, and by extension, the availability of quality food items (Lee 1996; Brockman & van Schaik 2005). In these species, maternal condition before cycling is the most crucial factor influencing reproduction (Janson & Verdolin 2005). It is possible for primates to resume cycling while lactating if the following conditions are met: mothers provide a conservative investment level throughout lactation (van Noordwijk et al. 2013), infants begin to supplement their diets early within the lactation phase, thus allowing mothers to resume cycling (Langer 2008), and lastly, habitat food abundance is high prior and during cycle resumption (Ellison 1995; Brockman & van Schaik 2005; Janson & Verdolin 2005). If a female meets these conditions, it is possible that she can resume cycling, and then gestate a new infant while lactating for her previous infant.

Because of these circumstances, females are able to begin allocating energy to reproduction during the lactation phase. In these species, complete nursing cessation (“true weaning”) may not fully occur until the subsequent offspring is born (discussed in Lee 1996; e.g.,

Trachypithecus phayrei crepusculus, Borries et al. 2014; Pongo pygmaeus wurmbii, van

Noordwijk, Kuzawa & van Schaik 2013, van Noordwijk et al. 2013; Colobus vellerosus, Vayro in prep). Few studies have investigated the contexts, influential factors and the extent to which mothers are able to gestate and lactate simultaneously. It is possible that inter-individual variation in lactation length observed in some species may be the result of whether the mother

has become pregnant during the lactation period, in which case the pregnancy would place an energetic constraint on the length of lactation possible.

1.3 Thesis aims

The aim of this thesis is to describe the variation in lactation lengths observed in a population of wild colobus monkeys. It will also explore the potential causal factors of this variation. The intention is to expand on the work of Dr. Sicotte’s previous MA student Lisa Macdonald, by exploring the context and temporal distribution of lactation cessation. Additionally, I aim to contribute data to further develop methods to investigate nursing cessation in non-human primates, ultimately in an effort to both help strengthen its position as a life history characteristic and standardize measures of nursing cessation in primate field studies.

In the next paragraphs, I will present the hypotheses that I will investigate in this thesis, as well as my predictions.

1.3.1 Hypotheses and predictions

The infanticide counter-strategy hypothesis

Female ursine colobus could increase infant survival, and hence their reproductive success, if they were able to modulate their maternal investment strategies in the presence of infanticide risk

(Trivers 1974; Hrdy 1977). In our population, groups experience a different inherent risk of infanticide in response to male group composition (Teichroeb et al. 2012). Indeed, in our study population, prime males residing in uni-male groups are of higher quality than those in multi- male groups, because they are able to deter takeovers and frequently win inter-group encounters

(Teichroeb et al. 2012). Therefore, for the female residents, multi-male groups are of a higher

inherent risk of infanticide relative to uni-male groups. In the presence of infanticide risk, females should shorten lactation length (i.e., shorter than mean population length) relative to those in low infanticide risk conditions, thereby lessening infant vulnerability, increasing infant survival and bringing females back into estrus sooner. I predict:

A. Females residing in multi-male groups will have shorter lactation lengths relative to

those in uni-male groups because extra-group males often target multi-male groups,

and males residing in multi-male groups tend to be of lower quality than those in uni-

male groups (Crockett & Janson 2000; Teichroeb et al. 2012; Sicotte et al. 2015).

B. Mothers residing in groups with a high number of females will wean their infants

earlier relative to those in groups with a low number of adult females, because groups

with a high number of females are more attractive to immigrant males, making the

females in these groups experience a higher risk of infanticide (Theropithecus gelada,

Dunbar 1984; Semnopithecus entellus, Borries 1997; Alouatta seniculus, Crockett &

Janson 2000; Colobus vellerosus, Teichroeb et al. 2011).

C. Male infants will wean earlier than females because males develop faster (i.e. they

transition to a black and white coat earlier; Bădescu et al. accepted), and are more

often the target of infanticidal adult males (Teichroeb & Sicotte 2008).

Additionally, theoretically males commit infanticide as a strategy to induce accelerated estrous in females, in efforts to increase their own reproductive success (Hrdy 1974, 1977). Our data now suggests that simultaneous gestation and lactation does occur in Colobus vellerosus, and so the two phases (gestation and lactation) are not necessarily discrete reproductive phases.

In this thesis, I will present the cases that we have that seem to indicate that simultaneous gestation and lactation is indeed quite frequent in our population. If the simultaneous gestation

and lactation constitutes a counter-strategy against infanticide, I expect that mothers residing in groups with an on-going risk of infanticide begin to gestate sooner during lactation relative to mothers residing in lower risk groups.

The food availability hypothesis

Food availability and by extension, the level of female feeding competition, may influence the length of lactation and the timing of nursing cessation. Infants weaned during periods of high food availability can more easily and successfully transition to independent foraging (Lee 1996). In periods of low food availability, infants experience slower overall growth rates, possibly due to low milk quality (Lee 1996; Borries et al. 2008) and have difficultly independently foraging due to scarce resources once they are weaned (Lycett et al.

1998). If females modulate their lactation length and cessation timing in response to food availability, I predict:

A. Nursing cessation will temporally cluster to periods prior to or during the

months with the highest abundance of quality food items, so that infants can

transition to independent foraging faster, and females can easily acquire energy

required for future reproduction.

B. The length of lactation will be longer in groups with a high number of females

because females will suffer the effects of scramble feeding competition.

Indeed, when scramble feeding competition is high, mother’s feeding

efficiency will decrease, which may lead to lower milk quality, thereby

resulting in slower infant development (Lindstrom 1999; Borries et al. 2008;

Therrien et al. 2008; Lowther & Goldsworthy 2011).

Additionally, we expect that mothers will experience shorter intervals between nursing cessation and the subsequent birth, if the nursing cessation occurs during high food availability periods. The high availability of quality food within the environment may accommodate or lessen the energetic costs of a growing foetus and a nursing infant. We also expect that intervals will be longest when mothers wean their infant during low food availability because they are unable to maintain both gestation and lactation when access to quality food items is low.

This thesis obviously has a limited scope. I did not investigate questions that relate to the process of weaning from a behavioural perspective. Instead, I have chosen to explore the final moments of maternal investment (nursing cessation), and whenever possible, to investigate the length of the maternal investment itself. In addition, due to the long lifespan of Colobus vellerosus, I was unable to investigate the long-term fitness benefits of different maternal investment strategies, lactation lengths or contexts of nursing cessation.

Chapter Two: Methods

2.1 Study Site

Boabeng-Fiema Monkey Sanctuary (BFMS) is a 192ha (1.9km2) dry semi-deciduous forest fragment surrounded by farmland, in the Brong-Ahafo region of Ghana, West Africa (Hall

& Swaine 1981; Fargey 1992). BFMS is located within a constellation of riparian forest fragments, ranging in size from 3 to 55 ha, some of which also contain ursine colobus. Some of these fragments connect to each other (Wong & Sicotte 2006; Kankam & Sicotte 2013). The annual rainy season is March-October and the dry season is November and February (Fargey

1992; Saj & Sicotte 2007). Two diurnal primate species (Colobus vellerosus and Cercopithecus campbelli lowei) live sympatrically within the sanctuary and local religious taboos culturally protect each species (Fargey 1992; Saj et al. 2005; 2006; Saj & Sicotte 2013). BFMS currently does not contain any potential predator species that could prey on adult monkeys in these two species (MacIntosh & Sicotte 2009; Teichroeb & Sicotte 2012).

2.2 Study Species

Ursine colobus (Colobus vellerosus) is a diurnal and arboreal colobine living in Africa

(Saj & Sicotte 2013), with an annual diet composition of 74% young and mature leaves (Saj et al. 2007). Group size is variable, ranging from 6-38 individuals per group (Saj et al. 2005; Wong

& Sicotte 2006; Kankam et al. 2013). Groups are primarily female philopatric (Teichroeb et al.

2009). Males systematically disperse from their natal group (Teichroeb et al. 2009; Teichroeb et al. 2011). Facultative female dispersal occurs (Teichroeb et al. 2009) and this leads to adult females living in social contexts where their access to female kin varies (Wikberg et al. 2012,

Wikberg et al. 2014). Social groups are not static and range in composition from uni-male/multi-

female to multi-male/multi-female (Saj et al. 2005; Teichroeb et al. 2011; Teichroeb et al. 2013).

All male bands (AMB) do occur (Saj & Sicotte 2005; Sicotte et al. 2007). Extra-group males put

considerable pressure on bi-sexual groups and often takeover the groups (Sicotte et al. 2015).

Infanticide regularly occurs following a takeover (Teichroeb & Sicotte 2008). Multi-male groups

face a higher infanticide risk, arguably because they are composed of lower quality males who

are unable to prevent takeovers; resulting in a higher risk of takeover and infanticide, relative to

uni-male groups (Teichroeb et al. 2012) Females generally experience scramble competition for

food (Teichroeb & Sicotte 2009), and exhibit low rates of aggression (Saj et al. 2007). In some

circumstances however, contest competition for food does occur, and leads to the establishment

of individualistic dominance hierarchies that vary in their degree of strength depending on group composition, group size and the availability of concentrated, high-quality resources (i.e., egalitarian to despotic; Wikberg et al. 2013).

Colobus vellerosus exhibit white pelage on the underside of the tail base, which is used to

determine the sex of individuals. Females have white pelage that is broken at the perineum and

males have a white pelage that is continuous across the perineum (Saj & Sicotte 2013). Infants

experience natal coat color changes during the first year, transitioning from a white coat to a

black and white coat (MacDonald 2011; Bădescu et al. accepted). Infant handling occurs often

in this species (Brent et al. 2008), with white infants handled the most particularly by kin, and

male infants are handled more than female infants (Bădescu et al. 2015). Previous research has

reported that infant weaning age varies across and within groups, ranging from 420-539 days

(60-77 weeks) (MacDonald 2011).

2.3 Data Collection

2.3.1 Demographic data table and study subjects

In Colobus vellerosus the length of lactation often spans more than one year (and so more than one research season), therefore it was necessary to compile long-term data to be able to capture the individual’s date of birth and the date of nursing cessation in our dataset. I used the terms nursing cessation as opposed to weaning (as cited throughout the literature), because it more clearly describes the final moments of maternal investment from a maternal perspective, whereas the term weaning is both difficult to measure and may describe a process rather than an end point. In this study, the exact nursing cessation date was the last date observed suckling when followed by two consecutive weeks of no observed suckling, as recommended by Borries et al. 2014. Whenever possible, suckling was determined by the presence of infant jaw movements which has been shown to indicate milk transfer (Macdonald 2011). We chose this method to study nursing cessation because it was both practical to collect during my field season and also easily extracted from the long-term data.

Before beginning my 2014 field season, I compiled a long-term demographic data table from pre-existing data from the population at the Boabeng-Fiema Monkey Sanctuary. Previous researchers collected observational data during their field seasons from 2003 to 2013. The dataset included infant birth and nursing cessation dates in eight groups, totalling 110 infant records. The amount of information available per infant, as well as its precision, varied considerably. I aimed to compile the following information (whenever available): date of birth

(exact and approximate dates), date first observed, group at birth, mother identification, mother’s parity status, and date of nursing cessation (range of approximation if not exact). Individuals

with missing characteristics were included in the data table if they could potentially contribute to future analyses outside of the scope of this project.

From this long-term data, I was able to calculate 13 exact lactation lengths (see Appendix

A.1.) and also extract 40 infants in seven groups with an exact date of nursing cessation

(Appendix A.2.). Exact dates were those documented within 0-3 days of the birth or nursing cessation. Additionally, I was able to extract 26 cases with a known date of nursing cessation for one infant and an exact date of birth of the mother’s subsequent infant (see Appendix A.3. &

A.4.). Individuals included in this study are from my 2014 field season and from data collected during the field seasons of Eva Wikberg, Lisa Macdonald, Josie Vayro and Stephanie Fox. The individuals in my sample do not represent every nursing cessation event that occurred within the study period, but instead represent a small subset of individuals with all the appropriate information required for the analyses. Since there is no reason to assume a bias towards a certain group, individual or characteristic of the individuals, this data set is likely a random and representative sample of our BFMS study groups. For each data point, group composition and food availability during the lactation and nursing cessation were known. Nursing cessation dates were collected in three ways: by previous researchers using proximity data from scan samples and ad libitum data where the infant was last observed nursing, by myself during my field season, or by research assistants Robert Korangteng and Charles Kodom while collecting long- term data from November 2014 to November 2015.

2.3.2 Phenological Data

To assess food availability, phenological data of the top 10 colobus food items were collected bi-weekly along two routes. One route covered one group’s range (RT), and the second

route contained the remaining three groups ranges (SP, WT and WW). T. Saj, J. Teichroeb and

E. Wikberg previously chose these phenology routes by randomly selecting 3-5 trees per large tree species within the study groups’ home ranges. All phenology data collected during my study was with the assistance of Tony Dassah (TD). TD has assisted in the collection of BFMS phenological data with all previous researchers, which helps maintain a level of consistency between projects. Phenological data continued to be collected until May 2015 by TD with the assistance of RK and CK.

We documented phenological data of 165 trees. We walked the routes between 9 am – 12

pm. First, flower, fruit and seedpod availability were recorded as a raw count, and leaf

availability was recorded as bare, mid-full, or full. Then young leaf, mature leaves, flower buds,

flowers, unripe fruits, ripe fruits, unripe seed pods, and ripe seed pods availability was recorded

on a scale of 0 to 4 where 0=0%, 1=1-25%, 2=25-50%, 3=50-75%, and 4=75-100%.

2.4 Data Analysis

2.4.1 Analysis Part One: Factors influencing lactation length

I used two datasets to investigate lactation length and the context of nursing cessation.

For part one, I used 13 infants in five groups with exact birth and nursing cessation dates. Using

these individuals, I was able to calculate an exact lactation length in days. Group composition

(number of females, number of males) and infant sex were known for all 13 cases.

Generally, a multivariate analysis should be used to disentangle the effects of several test

variables on the dependent variable. Multivariate analyses require more independent test subjects

(such as lactation lengths) relative to test variables. Due to the limited sample size, a multivariate

analysis was not statistically appropriate for our dataset; therefore we have chosen several

univariate analyses.

2.4.1.1 The effect of sex on lactation length

I compared lactation length (in days) between male and female infants. I tested the effect of infant sex on lactation length using a Mann-Whitney U test. The sample included 6 female infants and 7 male infants.

2.4.1.2 The effect of male group composition on lactation length

I tested the effect of male group composition on lactation length. I categorized groups as

either uni-male (N = 8) or multi-male (N = 5). Multi-male groups were any group containing

more than one male, regardless of the number of males. Each group remained in their category

throughout each lactation length. A Mann-Whitney U test (MWU #2) compared the lactation

length of infants in uni-male and multi-male groups. Both Mann-Whitney U tests in analysis part

one are two-tailed with a Bonferroni correction, and results are considered significant if p <

0.025.

2.4.1.3 The effect of adult female group size on lactation length

To determine if the number of adult females in a group influenced the length of lactation,

I categorized groups as containing a low (≤ 4; N = 4), medium (5-6, N = 5) or high number of

females (7 females; N = 4). Three groups were created because the sample contained more

individuals who resided in groups with ≥ 5 adult females. Each group remained in their category

throughout each lactation length. A Kruskal-Wallis H test was run to test the association between

the length of lactation in groups in relation to the number of adult females.

2.4.2 Analysis Part Two: Analyzing the Context of Nursing Cessation

I combined individuals with an exact length of lactation (N = 13) to those with exact

nursing cessation dates but unknown birth dates (N = 27) to explore the context in which

mothers wean their infants. In this analysis, the duration of lactation is not important, but rather it

is the timing of nursing cessation that is used in the analysis, in relation to the context at that time. Every individual used to analyze the context of nursing cessation, have an exact date of nursing cessation with an accuracy of 0-3 days (N = 40).

First, I investigated if the timing of nursing cessation coincided with the availability of

high quality food items. I took several steps to investigate if nursing cessation link to the

availability of high quality food items. First, I categorized months as possessing a “high” and

“low” amount of quality foods. Dr. Tania Saj investigated food availability at BFMS during her

PhD research in 2000-2001. She concluded that late December to March contained the highest

availability of high quality food items (flowers, fruits, seedpods and young leaves) (Saj 2005).

To determine whether this trend continued to present day, I used phenological data from my field

work (May 2014 to April 2015) to calculate mean monthly plant part availability (Figure 2.1.),

then compared the scores to same eleven months from Dr. Saj’s records using paired sample t-

tests. I conducted an eleven-month comparison (as opposed) to a 12-month comparison because

the 2000-2001 records did not include the month of December. The paired T-tests showed no

significant difference in mean monthly phenology scores in flowers, seedpods, young leaves or

mature leaves between 2000/2001 and 2014/2015 (FL: t = .209; p = .839; SP: t = -.827; p = .430;

Figure 2.1. Mean Phenological Scores per Plant Part 2014/2015 Phenology dates: May 2014- April 2015 FL = Flower; FR = Fruits + Seeds; SP = Seedpods; YL = Young Leaves; ML = Mature Leaves; High food (HQ) quality months demarcated by blue box.

YL: t = 1.223; p = .252; ML: t =1.128; p = .289), however, the fruit availability had significantly decreased (t = 8.157; p = < 0.0005). The peak in fruit availability remained within the high quality months. It thus suggests that there is consistency in the temporal pattern of food availability at the site throughout the long-term data, thereby eliminating the necessity to test phenology scores for all long-term field seasons. I have thus categorized January, February and

March as high quality food months, due to the high amount of available fruit, flowers, seedpods, and young leaves, all of which are preferred colobus food items (Saj & Sicotte 2007a).

Depending on seasonal availability, C. vellerosus prefer to eat seeds and unripe fruit, which has been observed in other colobus species (Saj & Sicotte 2007). Mature leaves are a food

type that contain high tannin levels and a low protein-to-fibre ratio, making them both a less preferred and low quality food item because of low digestibility (Milton 1979; McKey et al.

1981; DaSilva 1992; Mowrey et al. 1996; Davies et al. 1999; Saj & Sicotte 2007a). Therefore,

April to December are categorized as low quality food months, because primarily only mature leaves are available (Saj & Sicotte 2007 a, b). To determine if mothers prefer to wean infants during months with the presence of high quality food items, I used circular statistics and the

Rayleigh test to assess the uniformity of the nursing cessation events distribution. If females wean infants in relation to the abundance of high quality food items, one would expect a non- uniform or concentrated distribution of nursing cessation to the months with the highest abundance of quality food (January, February and March).

Circular statistics analyze the distribution of data that can be converted into points on the circumference of a circle (Pewsey et al. 2013). Circular variables differ from linear variables because 0° does not represent a true zero but also represents 360°, which is close to both 355° and 5°. In the present analysis, the circular axis was equally divided into 12 sections of 30°, each representing a month of the year. I converted nursing cessation dates into degrees and plotted them on the circumference. The Rayleigh uniformity test assessed the probability of data points evenly distributed throughout the year (Batschelet 1981; Pewsey et al. 2013). Primate studies assessing the annual distribution of events (e.g., birth, mating) using circular statistics commonly use the mean vector length r in circular statistics, which measures the unevenness of events throughout the year (Janson & Verdolin 2005). In this analysis, r was not calculated because it is more appropriate for studies with larger sample sizes, because the r-value increases as the sample size decreases, which in this study could have prematurely indicated nursing cessation

seasonality when potentially none exist. All circular statistics were completed in R 3.2.0 GUI

1.65 Mavericks build (6931).

2.4.3 Analysis Part Three: Duration between nursing cessation and subsequent birth for the same mother

I used two datasets to analyze the relationship between my independent variables (infant

sex, maternal age, male/female group composition, number of potential infant handlers present

and food availability), and the duration between the date of nursing cessation and the subsequent

birth (herein as duration to the next birth). From our sample of infants with exact nursing

cessation dates (N = 40), we have a subset, for which we have the exact known birth date of the

subsequent infant of the mother (N=26). This allowed me to calculate an exact duration (in days)

between the nursing cessation of infant 1 and the birth of infant 2 for a given mother. First, to

investigate the relationship between lactation length and duration to the next birth, I used eight

individuals with known exact lactation lengths and the duration to the next birth. Second, I

explored the influence of the independent variables (infant sex, food availability for the nursing

cessation month and group composition) on duration to the next birth (N = 26).

Generally, a multivariate analysis should be used to disentangle the effects of several test

variables on the dependent variable. Multivariate analyses require more independent test subjects

(such as duration to next birth) relative to the independent variables. Due to the limited sample

size, a multivariate analysis was not statistically appropriate for our dataset; therefore I have

chosen several univariate analyses. I was able to test the influence of birth and nursing cessation

month food availability on duration using three GMM’s.

2.4.3.1 The correlation between lactation length and duration to the next birth

To test the association between exact lactation length and duration to the next birth,

I used a Spearman’s rank-order correlation on eight individuals.

2.4.3.2 The effect of sex on duration to the next birth

I tested the effect of the first infant’s sex on the duration to the next birth (N = 26). The set of individuals included ten female infants and sixteen male infants. I compared durations to the next birth in male and female infants using a Mann-Whitney U test.

2.4.3.3 The effect of maternal age on duration to the next birth

To test for the effect of maternal age, I categorized mothers as either young (<10 years of age, N

= 10) or old (≥ 10 years of age, N = 17) at the time of the infant nursing cessation event. I used a

Mann-Whitney U test to compare duration to the next birth of young and old mothers.

2.4.3.4 The effect of male group composition on duration to the next birth

I tested the effect of male group composition on duration to the next birth. I categorized groups as either uni-male (N = 16) or multi-male (N = 10). The duration to the next birth of uni- male and multi-male groups was compared using a Mann-Whitney U test. All Mann-Whitney U tests in analysis part three are two-tailed with a Bonferroni correction, and results are considered significant if p < 0.0167.

2.4.3.5 The effect of female group composition on duration to the next birth

Female group size in the sample ranged from 3-7 (range 3-7; 3 AF = 3; 4 AF = 4; 5 AF =

8; 6 AF = 4; 7 AF = 7). I tested the association between female group size and the duration to the

next birth (N = 26) with a Spearman’s rank-order correlation.

2.4.3.6 The association between duration to the next birth and the number of available potential infant handlers

I defined the number of potential handlers as the number of non-mother adult females and

sub-adult females residing in the group at the time of the nursing cessation. The number of

potential handlers within groups ranged from 5 to 10 individuals. I tested the relationship

between duration and the number of potential infant handlers available using a Spearman’s rank-

order correlation.

2.4.3.7 The influence of food availability on duration to the next birth

I ran three mixed models to understand the influence of food availability on duration in

IBM SPSS Statistics 22 (‘genlinmixed’ function). Mixed models were appropriate for these

analyses because it can control for repeated measures by setting them as a random effect. The

duration dataset contained 21 distinct mothers ID with 5 of the mothers having two distinct

durations to the next birth (i.e., neither infant 1 or 2 were repeated), for a total of 26 durations.

The first mixed model (MM #1) tested whether the food availability during the month of

nursing cessation influenced the length of duration to the next birth. I applied the same food

availability periods as previously (e.g., high food availability as January, February and March;

low food availability as April to December). Of the 26 durations, 6 nursing cessation events

occurred during high food availability (HW), and 20 during low food availability (LW). In MM

#1, food availability during the month of nursing cessation was the fixed effect variable. The second mixed model (MM #2) tested whether the food availability at the time of the subsequent birth influenced the length of duration. For this model, 11 births occurred in high food availability (HB) and 15 births occurred in low food availability (LB).

The third mixed model (MM #3), attempted to analyze the influence of both the nursing cessation and birth month food availability on the length of duration. The nursing cessation of infant one and the birth of infant two creates a difficult statistical challenge in regards to food availability because each event may occur in different food availability contexts. Using the previous high vs. low food availability categorization, four separate food availability contexts were created (see Table 2.1): 1) wean in high food availability, subsequent birth in high food availability (HW-HB; N = 4); 2) wean in high food availability, subsequent birth in low food availability (HW-LB; N = 2); 3) wean in low food availability, subsequent birth in high food availability (LW-HB; N = 7); 4) wean in low food availability, subsequent birth during low food availability (LW-LB; N = 13). The third model (MM #3) assessed the influence of food availability context on the length of duration, with food availability context as the fixed effect variable. All mixed models are two-tailed with the Bonferroni correction, and results are considered significance if p <0.0167.

Table 2.1. Duration to next birth sample sizes in four food availability contexts BIRTH High food availability at Low food availability at birth of infant 2 (HB) birth of infant 2 (LB) High food availability at HW - HB HW - LB nursing cessation of N = 4 N = 2 infant 1 (HW) Low food availability at LW - HB LW - LB WEAN WEAN nursing cessation of N = 7 N = 13 infant 1 (LW)

Chapter Three: Results

3.1 Lactation length

3.1.1 Description of lactation length

I used thirteen infants with an exact date of birth and date of nursing cessation to

determine lactation length. The range in lactation length was 275-640 days (39.3- 91.4 weeks;

365 day range). The mean lactation length was 409.8 days (58.5 weeks SE 27.4; SD 98.9 days)

with a median length of 436 days (62.3 weeks; IQR 116 days).

We opted to exclude the longest lactation length (mother infant dyad XY-X6 of 640

days). Case 13 represents XY’s first lactation length (discussed at length in the discussion), this point is substantially higher than all other lactation lengths within the sample (Figures 3.0 & 3.1), and it is statistically a mild outlier above the upper inner fence (UIF = Q3 + 3*IQR (116) = 633 days). We do not believe that this case represents a typical lactation length; therefore we have excluded it in the following analyses (e.g., 3.1.2-3.14).

The range in lactation length without the outlier was 275-472 days ([39.3-67.4 weeks] N

= 12). The mean lactation length was 394.5 days ([56.4 weeks] SE 20.8, SD 72.1), with a median

length of 430 days ([61.4 weeks] IQR 136.3).

Figure 3.0. Lactation length sample with and without outlier Case 13 of 640 is a statistical mild outlier (upper inner fence = 633, upper outer fence = 807) and therefore excluded from the sample.

Figure 3.1. Normality deviation distribution Q-Q plot of lactation length Data point #13 indicates the dyad XY-X6 relative to the remaining lactation length sample (points 1-12).

3.1.2 The effect of sex on lactation length

Lactation length in female infants ranged from 275-459 days (39.3-65.6 weeks; mean

390.3 days [55.6 weeks] SD 69.9, SE 28.5; median 412.5 days [58.9 weeks]; IQR 115.6; N = 6)

(Figure 3.2). Male infant lactation length ranged from 284-640 days (40.6-67.4 weeks; mean

398.7 days [57 weeks] SD 80.8, SE 33; median 433.5 days [61.9]; IQR 158.6; N = 6). I used a

Mann-Whitney U test to explore sex differences in lactation length and the difference was not significant (U= 14.5, z = -.930, p = 0.352).

Figure 3.2. Lactation length by sex females: mean 390.3, SD 69.9, SE 28.5; median 412.5, IQR 115.6; range 275-459, N = 6; males: mean 398.7, SD 80.8, SE 33; median 433.5, IQR 158.6, range 284-472, N = 6; MWU U= 14.5, z = -.930, p = 0.352

3.1.3 The effect of male group composition

Of the twelve lactation lengths, seven infants were weaned in uni-male groups (mean

367.9 [52.6 weeks]; SD 76, SE 28.7; median length 389 days [55.6 weeks]; IQR 154; range 275-

443) and five in multi-male groups (mean 431.8 days [61.7 weeks]; SD 51.7, SE 23.1; median length 459 days [65.6 weeks]; IQR 81; range 345-472 [49.3-67.4 weeks]) (Figure 3.3). The

Mann-Whitney U test showed no significant difference in lactation length of uni-male and multi- male groups (U = 7, z = -1.708, p = 0.088).

Figure 3.3. Lactation length by adult male group composition Uni-male: mean 367.9 days; SD 76, SE 28.7; median 389 days; IQR 154; range 275-443, N = 7; multi-male: mean 431.8; SD 51.7, SE 23.1; median 459, IQR 81, range 345-472, N = 5; MWU U = 7, z = -1.708, p = 0.088).

3.1.4 The effect of adult female group size

The length of lactation in groups with a low number of females ranged from 284-438 days ([40.6-62.6 weeks], mean 370.3 days [52.9 weeks]; SD 78.7, SE 45.4; median 389 days

[55.6 weeks]; N = 3), a medium number of females lactation length ranged from 310-472 ([44.3-

67.4weeks]; mean 424 days [60.6 weeks]; SD 65.2, SE 29.2; median 443 [63.3 weeks]; IQR

92.5; N = 5) and groups with a high number of females ranged from 275-459 ([39.3-65.6 weeks], mean 375.8 days [53.7 weeks]; SD 82.4, SE 41.2; median 384.5 days [54.9 weeks]; IQR 157.8;

N = 4)(see Figure 3.4). The Kruskal-Wallis H test showed that there was no significant difference found between the three group categories (χ2 = 2.162, df = 2, p = .339).

Figure 3.4. Lactation length by adult female group size Low: mean 370.33 days, SD 78.7, SE 45.4, median 389 days, range 284-640, N = 3; medium: mean 424 days, SD 65.2, SE 29.2, median 443, IQR 92.5, N = 5; high: mean 375.8 days, SD 82.4, SE 41.2; median 384.5 days, IQR 157.8, N = 4; Kruskal-Wallis H test (χ2 = 2.162, df = 2, p = .339).

3.2 Context of nursing cessation

3.2.1 Annual distribution of nursing cessation

The monthly distribution of forty nursing cessations is illustrated in Figure 3.5. Nursing

cessation was observed in all 12 months of the year. The distribution of events was uniform and not clustered within the months with high or low food availability (Rayleigh test: Z = 0.2052; p =

.1863, N = 40). The distribution of nursing cessation was also uniform when analyzed by sex

(males: Rayleigh test: Z = .3022, p = .1221 N = 23; females: Z = .0894, p = .8762, N = 17)

(Figure 3.6).

Figure 3.5. Nursing cessation circular histogram Nursing cessation dates (N = 40) plotted on a circular representation of a year. The bar indicates the number of nursing cessation events per month with January to March (royal blue) as high food quality months and April to December (light blue) as low food quality months. Rayleigh test of uniformity (Z = 0.2052; p = .1863) shows that nursing cessation dates are not clustered.

Figure 3.6. Raw nursing cessation circular distribution by sex Nursing cessation dates per month by sex, with female infants in orange and male infants in blue. Rayleigh test of uniformity showed nursing cessation events were not clustered when analyzed separately by sex (males: Rayleigh test: Z = .3022, p = .1221 N = 23; females: Z = .0894, p = .8762, N = 17).

3.3 Nursing cessation in relation to the subsequent birth

3.3.1 Description of nursing cessation in relation to the subsequent birth and gestation

Of the twenty-six durations to the subsequent birth, the range was 0-114 days (0-16.3 weeks), with a mean difference of 57 days ([8.1 weeks], SD 35.3, SE 6.9), and a median difference of 58 days (8.3 weeks; IQR 55.5). In regards to gestation (approximately 6 months,

Vayro in prep), mothers range in their ability to simultaneously nurse and gestate for the entirety of their gestation, although mothers seemed to wean their infants when they were 4.1 months pregnant.

Eight individuals with exact lactation lengths and exact durations to the subsequent birth were analyzed using Spearman’s rank-order correlation. There was no significant relationship between the length of lactation and duration to the birth of the next offspring (r = .333, N = 8, p

= .420).

3.3.2 Sex differences in duration to the next birth

The duration to the next birth following the nursing cessation of a male infant ranged from 0-114 days (0-16.3 weeks; mean 57.7 days [8.2 weeks]; SD 39.1, SE 9.8; median 47 days

[6.7weeks]; IQR 67.6; N = 16). Female infants ranged from 7-106 days (1-15.1 weeks; mean

55.9 days [8 weeks]; SD30.3, SE 9.6; median 52.5 days [7.5 weeks]; IQR 38.75; N = 10) (Figure

3.6). The duration to the next birth of male infants (N = 16) and female infants (N = 10) were analyzed using a Mann-Whitney U test, which showed no significant difference in duration to the next birth after nursing cessation male or female infants (U = 76.5, z = -.185, p = .854).

Figure 3.7. Nursing cessation-subsequent birth duration in days by sex Males: 0-114 days, mean 57.7 days, SD 39.1, SE 9.8, median 47 days, IQR 67.6, N = 16; females: 7-106 days, mean 55.9 days, SD30.3, SE 9.6, median 52.5 days, IQR 38.75, N = 10; MWU U = 76.5, z = -.185, p = .854

3.3.3 The effect of maternal age on duration to the next birth

Of the 26 durations to the next birth, young mothers weaned 9 infants and older mothers weaned 17 infants (Figure 3.7). Durations to the next birth of young mothers were slightly longer than those of older mothers (young: mean 60.3 days [8.6 weeks], SD 37.7, SE 12.6, median 59

[8.4 weeks], IQR 73.5, range 7-106 days [1-14.1 weeks], N = 9; old: mean 55.2 days [7.9 weeks], SD 35.1, SE 12.6, median 58 days [8.3 weeks], IQR 44, range 0-114 days [0-16.3], N =

17). The Mann-Whitney U test showed this difference was not significant (U= 71, z = -.297, p =

.767).

Figure 3.8. Boxplot of the duration to next birth of young and older mothers Young mothers: mean 60.3 days, median 59 days, IQR 73.5, range 7-106 days, N = 9; old mothers: mean 55.2 days, SD 35.1, SE 12.6, median 58 days, IQR 44, range 0-114, N = 17; U= 71, z = - .297, p = .767

3.3.4 The effect of male group composition to the next birth

The duration to the next birth of uni-male groups (N = 16) and multi-male groups (N =

10) were analyzed using a Mann-Whitney U test. There was no significant difference between the two group compositions (uni-male: mean 57.4 days [8.2 weeks], SD 37.7, SE 9.4, median

58.5 [8.4 weeks], IQR 69.8; multi-male: mean 56.3 days [8 weeks], SD 33, SE 10.4, median 53

[7.6 weeks], IQR 47.8, range 0-112 [0-16]; U = 78, z = -.105, p = .916) (Figure 3.8).

Figure 3.9. Duration to next birth in uni-male and multi-male groups uni-male: mean 57.4 days, SD 37.7, SE 9.4, median 58.5, IQR 69.8, range 3-114, N = 16; multi-male: mean 56.3 days, SD 33, SE 10.4, median 53, IQR 47.8, range 0-112, N = 10; MWU U = 78, z = -.105, p = .916

3.3.5 The effect of adult female group size

The Spearman’s rank-order correlation found no significant correlation between the

duration to the next birth and number of adult females residing in the group at the time of nursing

cessation (N = 26, rs = -.022, p = .915) (Figure 3.9).

120!

100!

80!

60!

40! Duration!to!Next!Birth!(days)! 20!

0! 0! 1! 2! 3! 4! 5! 6! 7! 8! Number!of!Adult!Females!

Figure 3.10. Adult female-duration to next birth scatterplot No correlation between number of adult females within a group at the time of nursing cessation and the duration to the next birth N = 26, rs = -.022, p = .915

3.3.6 The association between duration to the next birth and the number of potential infant handlers available

The Spearman’s rank-order correlation found no significant correlation between the

duration to the next birth and number of available potential infant handlers at the time of nursing

cessation (rs = .053, p = .915; (Figure 3.10)).

120!

100! days)

80! Birth!( 60!

!Next! Male!Infants! 40! Female!Infants! on!to

20! Durati 0! 0! 1! 2! 3! 4! 5! 6! 7! 8! 9! 10! 11! Number!of!Available!Potential!Infant!Handlers!

Figure 3.11. Potential handlers-duration to next birth scatterplot No correlation between the number of potential infant handlers within a group at the time of nursing cessation and duration to the next birth (N = 26, rs = .053, p = .915)

3.3.7 The effect of food availability on duration to the next birth

The mean durations to the next birth for the high food availability during nursing cessation months was 39.8 days ([5.7 weeks] SE 14.2; N = 20), which appears quite different from duration following nursing cessation during low food availability months 62.2 days ([8.9 weeks] SE 7.8; N = 6), however the mixed model showed no statistical difference

(F(1,24)=1.910, p = .180). This may indicate a statistical trend that with a larger sample the food availability during the birth month would have been a significant influencing factor. Models also showed that the food availability during the nursing cessation month had no significant effect on the duration (MM #2: F(1,24)=.021, p = .887), with mean durations in high food availability birth months 55.8 days [8 weeks] SE 10.9; N = 11) vs. low birth months 57.9 days ([8.3 weeks]

SE 9.3; N = 15).

When assessing the four contexts of food availability on duration (see table 3.1 for full description, and figure 3.11), duration to the next birth appeared shorter during high food availability at both birth and nursing cessation (mean 19.5 days [2.8 weeks]). The longest durations were observed following high month food availability at nursing cessation and low birth month food availability (mean 80.5 days [11.5 weeks]), followed by low availability at nursing cessation and high food availability during the birth month (mean 76.6 days [10.9 weeks]). The final mixed model (MM #3) assessed the effect of the food availability context on the duration to the next birth, which was found to have no significant effect on duration

(F(3,22)= 1.671, p = .202). However, again it is likely that this represents a statistical trend and we need a larger sample to achieve lower standard error measures.

Table 3.1. Description of the durations in each of the four food availability contexts BIRTH High food availability at birth of Low food availability at infant 2 (HB) birth of infant 2 (LB) High food HW - HB HW - LB availability at N = 4 N = 2 nursing Range 7 – 40 days [1 - 5.7 weeks] Range 59 – 102 days [8.4 –

cessation of Mean 19.5 days [2.8 weeks] 14.6 weeks] infant 1 (HW) Median 15.5 days [2.2 weeks] Mean 80.5 days [11.5 weeks] Low food LW - HB LW - LB availability at N = 7 N = 13 WEAN WEAN nursing Range 26 – 114 days [3.7 - 16.3 Range 0 – 112 days [0 – 16 cessation of weeks] weeks] infant 1 (LW) Mean 76.6 days [10.9 weeks] Mean 46.9 days [6.7 weeks] Median 80 days [11.4 weeks] Median 53 days [7.6 weeks]

Figure 3.12. Duration to next birth in four food availability contexts No significant effect was found when comparing duration to food availability at the time of nursing cessation (MM #1, p = .180), at the time of the next birth (MM#2, p = .887), or the context of both nursing cessation and birth month (MM#3 p = .202). * H=High food availability, L=Low food availability, W=Nursing cessation event, B=Birth event.

Chapter Four: Discussion

4.1 Summary of key results

Colobus vellerosus infants become nutritionally independent much earlier than originally

documented in the previously tested (small) dataset (39.3 weeks [9.2 months] vs. 62 weeks [14.5

months]). In addition, the range of lactation length variation was much greater than anticipated,

with the shortest and longest lactation lengths differing by one year. The factors that allow some

mothers to wean infants substantially earlier than other mothers remained unclear. In our limited

dataset, the length of lactation was not influenced by infant sex, food availability, female feeding

competition or the risk of infanticide. The timing of nursing cessation was not influenced by the

availability of high quality food items or infant sex. Therefore, we1 were not in a position to

reject either our infanticide counter-strategy hypothesis or our food availability hypothesis.

In this thesis, we presented a new measure of female reproduction, “duration to the

subsequent birth”, which was the number of days between the nursing cessation of one infant and

the birth of the subsequent infant. Duration to the subsequent birth was not significantly

influenced by lactation length, maternal age, infant sex, the level of infanticide risk, intensity of

female feeding competition, or the number of potential infant handlers available. Food

availability during the nursing cessation month and birth month had no significant influence on

the duration to the subsequent birth, although there may be a trend toward shorter durations when

nursing cessation occurs during a period of high food availability. Food availability at the time of

nursing cessation and the food availability of the time of the next birth combined did predict

distinctly different mean lengths per context. Due to the limited sample size and high standard

errors, the four contexts were not statistically significant. However, a statistical trend indicated

1 I have chosen to use “we” oppose to “I” when discussing51 the results of this study. I personally developed and implemented the analyses for this thesis (in conjunction with my supervisor Dr. P. Sicotte), the data that allowed for this study was collect by several researchers since 2006 including Lisa MacDonald, Eva Wikberg,

Josie Vayro and Stephanie Fox.

that mothers might be able to nurse and gestate longer when food availability is high, particularly when food availability is high at nursing cessation.

Lastly, although it is outside of the scope of this project, we determined that the quantity of fruit at BFMS has significantly declined since 2000/2001.

4.2 Lactation length in Colobus vellerosus

Previous MA student Lisa MacDonald showed that lactation length in Colobus vellerosus ranged from 62-77 weeks, with a mean length of 62.5 weeks (N = 2, MacDonald 2011). Using a larger sample size, our study calculated a mean length of lactation at 394.8 days (56.4 weeks; N

= 12). Previously, 434 days (62 weeks) was the earliest observed case of nursing cessation

(MacDonald 2011), although anecdotal observations suggested infants could wean as early 30 weeks (Saj & Sicotte 2005). Our study has shown that an infant may be weaned as early as 39.3 weeks (9.2 months) using exact lactation lengths. Also, using the earliest exact age of nursing cessation, we have expanded the known range of variation in lactation length variation from 17 weeks (Macdonald 2011) to 52.6 weeks. The factors influencing this variation in lactation length remained undetermined. We found no influence of infant sex, food availability, female feeding competition or the risk of infanticide. Potentially, the observed variation may be the result of the contradictory selective pressures of female feeding competition and infanticide risk.

We excluded one outlier from our lactation length analyses (case 13, XY-X6 dyad). We believe this case did not represent a typical lactation (640 days; 91.4 weeks), because it is substantially higher than all other lactation lengths in the sample, and the mother was primiparous. It has been shown that new mothers initially have slow reproductive rates relative to more experienced mothers (Ross & Jones 1999), although some studies have found no

correlation between primiparous mothers and slow initial reproductive rates (Sade 1990); this

trend may occur in Colobus vellerosus at BFMS. However, we have two additional alternative

explanations for this result. First, in case 13 the mother resided in a group composed of only

primiparous mothers, perhaps resulting in no ability to replicate the maternal strategies of more

experienced mothers within the group. Second, within the lactation period, XY may have

become pregnant and then lost the fetus, then continued to nurse the current offspring. If this

were the scenario, it would explain the long length of lactation relative to others in the sample.

Regardless, a sample size of one is too small to speculate about the effect of primiparity at

BFMS, although we aim to explore this in the future.

The length of lactation in colobines is generally slightly longer than one year, with no

clear difference between African and Asian colobine species (see Table 1.0.). We found that the

length of lactation in Colobus vellerosus is within the realm of other colobine species, and is

most similar to Colobus guereza (390 days; Napier & Napier 1967; Chapman, Walker &

Lefebvre 1990) and Colobus polykomos (365 days; Sabater Pi 1973). Colobus vellerosus are

aseasonal breeders, which allows for flexible rearing strategies, specifically in regards to the

length of lactation, which in turn results in variation within populations. The range of lactation

length variation within colobine species is probably under-reported in many cases, because most

researchers publish only the mean length of lactation. This lack of data may slightly skew

comparisons of life history characteristics in some cases. More specifically, when we compared

the extremely high and low cases of lactation length to other colobine species, Colobus

vellerosus was most similar to Nasalis larvatus (280 days; Lippold 1981; Harris & Monfort

2006) and Colobus satanas (480 days; Struhsaker & Leland 1987).

To determine nursing cessation dates, we used the last date observed nursing followed by two consecutive weeks of no observed nursing. This method was advocated by Borries et al.

2014, as a biologically meaningful and a practical measure to obtain information on nursing cessation in field research. This measure does come with two setbacks (fully discussed in Borries et al. 2014). First, using this measure we were unable to determine whether nursing occurred during the night (when researchers were not present), and therefore, our date of nursing cessation may be slightly skewed to an earlier date than in reality. Second, by using a behavioural measure such as the presence of nursing, researchers are unable to extrapolate as to the quantity or quality of the milk transfer occurring. We were aware of both of these setbacks prior to conducting the research for this thesis. We assumed that the presence of nursing (nipple in mouth with jaw movement) indicated the transfer of milk, and therefore a lack of observed nursing was indicative of no milk transfer, and by extension, it demonstrated the end of maternal investment.

4.3 Counter-strategy to infanticide hypothesis

We tested whether mothers altered their maternal investment level in response to the risk of male infanticide. We were unable to support this hypothesis; in fact, there was no support for any of our predictions. Mothers did not wean their infants earlier when residing in multi-male groups, nor did they did they wean sooner when the group they resided in contained a high number of adult females, each context arguably leading to a higher inherent level of infanticide risk (Dunbar 1984; Borries 1997; Crockett & Janson 2000; Broom et al. 2004; Teichroeb et al.

2012). Instead, infants wean at statistically similar ages in uni-male and multi-male groups, and in groups containing a low, medium and high number of adult females. However, interestingly mothers in multi-male groups on average lactated longer than those in uni-male groups, which

entirely contradicted our prediction. We were unsure of an explanation for this trend as it would seem that in multi-male groups, infants remain at risk of infanticide longer than those in uni-male groups. Thus, it would seem that mothers do not utilize early weaning as a counter-strategy to male infanticide risk. However, our sample size might be too small to fully test this. We did not have enough data to test whether mothers abruptly weaned their infants in the context of a male takeover, where the risk of infanticide should be highest, because no takeovers occurred during our sample.

There were no sex differences in infant age at nursing cessation. Male and female infants weaned at similar ages. This contrasts with findings from outside of this thesis which suggested that male infants mature faster, potentially as an adaptation to the risk of infanticide because infanticidal males target male infants more often than female infants (Teichroeb & Sicotte 2008;

Bădescu et al. accepted). If male infants mature faster via rapid coat colors transitions, you would expect this to also be observable via shorter lactation lengths of male infants, in which case maternal investment in males would appear shorter in length. Our results contradict this prediction, which could indicate that the coat color itself may act as a stronger signal of infant dependence to infanticidal males, rather than the presence of suckling. Male infants may visually appear to mature faster, although the level of maternal investment in the form of nursing remains constant regardless of infant sex. With that said, we are unable to test this idea without analyzing the quality and quantity of milk given to each sex, it has often been suggested that male infants receive high quality milk in regards to protein and fat content relative to female infants, indicating a higher initial maternal investment, although for a shorter period of time (Macaca mulatta: Hinde 2007, 2009; Cervus elaphus hispanicus: Landete-Castillejos et al. 2004).

4.4 The food availability hypothesis

We did not find evidence to support the food availability hypothesis, which predicted that mothers would wean infants in relation to the availability of high quality food. Given this hypothesis, we expected nursing cessation to cluster either before or during January, February or

March, when food resources are highly available, so infants would be able to transition into independent foragers easier. We found that Colobus vellerosus nursing cessation is uniformly distributed throughout the year, regardless of infant sex. This result is not surprising because

Colobus vellerosus is not a seasonally breeding species, and lactation often spans over one year, so you would not expect a seasonal nursing cessation result. Thus, it is more likely that another selective pressure such as group composition or size, is influencing either the length of lactation and/or the timing of nursing cessation in this species, resulting in the inter-individual variation observed.

The second prediction of the food availability hypothesis was that if food availability, and by extension the feeding competition experienced by mothers, resulted in lower milk quality, we would expect infants residing in groups with a high number of adult females to wean at an earlier age (Lindstrom 1999; Borries et al. 2008; Therrien et al. 2008; Lowther & Goldsworthy 2011).

The level of female scramble feeding competition (as measured by female group size) did not influence lactation length in this study, as weaning age did not significantly correlate with the number of adult females. Thus, the availability of food does not seem to directly influence the length of lactation or the timing of nursing cessation in Colobus vellerosus. However, we did found one curious trend in regards to female group size. We found that females residing the medium sized group experienced the longest lactation lengths relative to both the small and large groups. Potentially, this may be the result of two selective pressures (female feeding competition

and infanticide risk) oppose to one, acting on the length of lactation, although due to the limited sample size, we are unable to test this idea with a multivariate analysis.

4.5 Simultaneous gestation and lactation

From an evolutionary perspective, it is argued that males commit infanticide to induce accelerated oestrous in females (Hrdy 1974, 1977). We have demonstrated that Colobus vellerosus mothers are able to simultaneously gestate and nurse their current offspring. Our unique dataset enabled us to analyze factors that potentially influence the duration between nursing cessation and the birth of the subsequent offspring. Our data showed a large range of variation between the shortest and longest durations to the next birth (0-114 days [0-16 weeks] N

= 26), however we were unable to determine the primary factor influencing this inter-individual variation. There was no effect of maternal age, infant sex, infanticide risk, female feeding competition, or the number of potential infant handlers available. We also found that food availability during the subsequent birth month had no significant effect on duration. Currently, our dataset is too small to fully test the influence of the weaning month food availability.

However, we have demonstrated that high food availability during the weaning month does produce shorter durations to the next birth on average, and a statistical trend toward this did emerged.

Mothers expressed a wide range of inter-individual variation regarding simultaneous lactation and gestation, where some mothers nursed offspring throughout their entire pregnancy.

Based on an approximate 5.75-month gestation length in Colobus vellerosus (Josie Vayro in prep), mothers in the sample on average nursed until the fourth month of gestation (16.6 weeks or up to 67% of gestation period). This may indicate that the variation in lactation length and

duration to the subsequent birth may be the result of different maternal investment strategies during gestation in varying food availability contexts.

4.6 Directions for future research

Based on the findings from this thesis, in the future we aim to explore follow-up avenues, such as the effects of maternal rank, the influence of parity on lactation length, the influence of competing selective pressures specifically female group composition and infanticide risk, and lastly, simultaneous lactation and gestation. We were unable determine maternal dominance ranks for many of the long-term records, therefore, the relationship between rank and maternal investment strategies was not explored. Other studies have demonstrated that high-ranking individuals give birth to heavier infants who experience faster growth rates, and thereby wean earlier, which gives high-ranking mothers a fitness advantage (Papio anubis, Garcia et al. 2009;

Papio ursinus, Johnson 2006; Mandrillus sphinx, Setchell et al. 2001). We hope to be able to assess the impact of maternal rank in the future.

Our conclusions about lactation length may be premature due to the small sample size, particularly in regards to primiparous females. In the future, we aim to explore the relationship between female group size and infanticide risk, because potentially these two pressures are competing with one another, resulting in mothers experiencing longer lactation lengths in medium size female group composition; a scenario we did not anticipate prior to this thesis. In

November 2014, our BFMS team began collecting year-round demographic data at BFMS, which will allow for future analyses with a larger sample size. Additionally, the preliminary work we discussed regarding the relationship between weaning and the subsequent birth will be reassessed in conjunction with hormonal and behavioural data with PhD student Josie Vayro.

More specifically, this work will investigate the frequency of simultaneous lactation and gestation at BFMS, which perhaps may be a strong causal factor of inter-individual variation in lactation length.

Lastly, in this thesis found we found that fruit availability at BFMS had significantly declined in the last 14 years. We are unsure of the causation or ramifications of this decline in regards to female reproduction, but more importantly in regards to population growth and dynamics. We hope to investigate this area at a later date.

4.7 Conclusion

Untangling ecological and social influences from life history characteristics is a difficult endeavour. In this study, we concluded that lactation length is not influenced by infant sex, food availability or the risk of infanticide, at least not in our limited sample. We have found that mothers did not wean their infants in response to the availability of food or by infant sex. Our study has eliminated some potential variables that may have explained the variation observed in lactation length and weaning events in our species. It is evident that other underlying factor(s) are either unknown or may be competing with one another, which has resulted the large range of variation in lactation length at BFMS.

We can now contribute to literature on mammalian life history by providing an accurate lactation length in Colobus vellerosus, using a larger sample size than previously analyzed.

Additionally, we have attempted to use the methods recommended by Borries et al. (2014) to acquire accurate and comparable weaning data for cross-species comparisons, although we are unable to confirm if these dates are indicative of infant nutritional independence without further studies of maternal milk composition.

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APPENDIX A: DATA TABLES

A.1. Lactation length data

Group Infant Mother Infant Date of Date of Lactation Male # Adult ID ID ID Sex1 Birth Weaning Length Group Females (days) Comp.2 DA CP CA F 10-07- 11-04- 275 0 7 2008 2009 WW C7 CR M 23-10- 03-08- 284 0 4 2013 2014 RT BO BE M 10-12- 16-10- 310 0 5 2012 2013 WW CX CR F 06-10- 14-09- 343 0 4 2012 2013 WW WL WE F 28-04- 08-04- 345 1 7 2008 2009 WW CI CH M 20-05- 17-07- 424 1 7 2007 2008 RT B9 BL F 23-05- 02-08- 436 0 5 2013 2014 SP XY XE M 01-07- 11-09- 438 0 3 2007 2008 RT F9 FV M 09-09- 26-11- 443 0 5 2013 2014 WW LS LU M 01-05- 02-08- 459 1 7 2007 2008 SP V8 VE F 06-10- 08-01- 459 1 5 2013 2015 SP S7 SA M 11-09- 27-12- 472 1 5 2013 2014 1 Infant sex where F denotes females and M denotes males 2 Male group composition where 0 denotes uni-male groups and 1 denotes multi-male groups

A.2. Individuals used for weaning event context analysis

Group Infant Mother Infant Date of ID ID ID Sex Weaning WW CI CH M 17-07-2008 NP LR LT M 25-07-2008 WW LS LU M 02-08-2008 SP XY XE F 11-09-2008 RT JI JE M 24-10-2008 NP NP NJ M 29-10-2008 WW JA ML M 30-10-2008 RT FR FI M 13-11-2008 SP VZ VE M 27-11-2008 BS SF SS F 29-11-2008 DA WM WY M 30-11-2008 DA MI MR F 14-01-2009 BS GM GR M 23-01-2009 OD TH TT M 26-01-2009 RT TO TR F 15-02-2009 RT BK BL M 18-02-2009 RT PE PO F 19-02-2009 RT SR SU F 18-03-2009 WW WL WE M 08-04-2009 DA CP CA M 11-04-2009 RT BD BL M 20-04-2013 RT GS TR M 23-05-2013 RT FN FV M 17-06-2013 SP CK CT F 17-08-2013 SP XA XE F 30-08-2013 WW CX CR F 14-09-2013 SP SW SE M 26-09-2013 RT BO BE F 16-10-2013 WW JJ JN F 26-06-2014 RT B9 BL F 02-08-2014 WW C7 CR M 03-08-2014 RT F9 FV M 26-11-2014 RT B5 BE M 26-12-2014 WW B7 BY M 26-12-2014 SP S7 SA M 27-12-2014 SP V8 VE F 08-01-2015 SP C8 CT F 17-01-2015 WW L7 LY F 26-01-2015 WT X6 XY M 05-09-2015 1 Infant sex where F denotes females and M denotes males

A.3. Data set for lactation length and duration to next birth analysis

Group Mother Mother's Infant Infant Date of Lactation Duration to ID ID Age1 ID Sex2 Weaning Length3 Next Birth3 WW CH O CI 1 17-07-2008 424 112 WW LU Y LS 1 02-08-2008 459 95 SP XE Y XY 0 11-09-2008 438 106 WW CR O CX 0 14-09-2013 343 39 RT BL O B9 0 02-08-2014 436 68 WW CR O C7 1 03-08-2014 284 75 RT FV Y F9 1 26-11-2014 443 26 SP SA Y S7 1 27-12-2014 472 24 1 Maternal age categorized as either young (denoted by Y; ≥ 10 years of age) or old (denoted by O; <10 years of age) 2 Infant sex categorized as females (0) and males (1) 3 Data point calculated in days

A.4. Data set for duration to next birth analyses

Group Mother Mother Inf. 1 Date of Duration Infant 2 Date Infant Male Group # Adult # FA ID ID AgeW, O Sex Weaning to Next of Birth 2 ID Composition Females Handlers Context2 BirthD W, 1 W W WW CH O 1 17-07-2008 112 06-11-2008 CM 1 7 10 LWLB NP LT Y 1 25-07-2008 59 22-09-2008 LE 0 6 5 LWLB WW LU Y 1 02-08-2008 95 05-11-2008 LN 1 7 10 LWLB SP XE Y 0 11-09-2008 106 26-12-2008 XS 0 3 4 LWHB RT JI O 0 24-10-2008 47 10-12-2008 JO 1 7 6 LWLB NP NJ O 1 29-10-2008 114 20-02-2009 N9 0 6 5 LWHB WW ML O 1 30-10-2008 0 30-10-2008 MX 1 7 10 LWLB RT FI O 1 13-11-2008 48 31-12-2008 FZ 1 7 6 LWHB SP VE O 1 27-11-2008 104 11-03-2009 VV 0 3 4 LWHB BS SS O 0 29-11-2008 58 26-01-2009 SX 0 6 6 LWHB DA WY O 1 30-11-2008 80 18-02-2009 WB 1 7 8 LWHB OD TT O 0 26-01-2009 7 02-02-2009 TA 0 6 5 HWHB RT TO O 1 15-02-2009 59 15-04-2009 TF 1 7 6 HWLB RT BL O 1 20-04-2013 33 23-05-2013 B9 0 5 4 LWLB RT TR O 0 23-05-2013 34 26-06-2013 T2 0 5 4 LWLB RT FV Y 1 17-06-2013 84 09-09-2013 F9 0 5 4 LWLB WW CR O 0 14-09-2013 39 23-10-2013 C7 0 4 5 LWLB RT BL O 0 02-08-2014 68 09-10-2014 B2 0 5 5 LWLB WW CR O 1 03-08-2014 75 17-10-2014 C2 0 4 6 LWLB RT FV Y 1 26-11-2014 26 22-12-2014 F2 0 5 5 LWHB RT BE O 1 08-12-2014 3 11-12-2014 B6 0 5 5 LWLB WW BY Y 1 26-12-2014 7 02-01-2015 L1 0 4 6 HWHB

SP SA Y 1 27-12-2014 24 20-01-2015 S2 1 5 5 HWHB SP CT Y 0 17-01-2015 40 26-02-2015 C1 1 5 5 HWHB WW LY Y 0 26-01-2015 102 08-05-2015 BY1 0 4 6 HWLB SP XE O 1 28-07-2015 58 24-09-2015 X1 1 5 5 LWLB W Indicates that the data point was extract at the time of the weaning event A Maternal age categorized as either young (denoted by Y; ≥ 10 years of age) or old (denoted by O; <10 years of age) D Data point calculated in days 1 Male group composition where 0 denotes uni-male groups and 1 denotes multi-male groups 2 Food availability context of both weaning and birth month. H=High food availability, L=Low food availability, W=Weaning event, B=Birth event