Daubentonia Madagascariensis) in Torotorofotsy, Madagascar

Examining the morphological and behavioral paradox of aye-ayes (Daubentonia madagascariensis) in Torotorofotsy, Madagascar

Dissertation

Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy

in the Graduate School of The Ohio State University

Timothy Mikhail Sefczek

Graduate Program in Anthropology

The Ohio State University

2018

Dissertation Committee

W. Scott McGraw, Advisor

Dawn Kitchen

Debbie Guatelli-Steinberg

Kristen Gremillion

Copyrighted by

Timothy Mikhail Sefczek

2018

Abstract

Aye-ayes (Daubentonia madagascariensis) are the most morphologically specialized primates, exhibiting a suite of features that include continuously growing incisors, elongated, clawed digits, large, bat-like ears, and a unique metacarpophalangeal joint in their third digit (Owen 1863; Simons 1995; Soligo 2005). These traits are used in combination to echolocate insect larvae embedded in deadwood, a feeding behavior known as percussive foraging (Erickson 1991, 1995; Erickson et al. 1998). Though aye- ayes were originally thought to be predominantly insectivorous (Petter 1962, 1977), they are seemingly too large (2.6kg) to subsist solely or even largely on invertebrates (Kay

1975). Prior to this study, the only available feeding data were derived from studies conducted on an introduced population from the island of Nosy Mangabe, Madagascar

(Iwano and Iwakawa 1988; Sterling 1993, 1994a), and in a disturbed forest (Ancrenaz et al. 1994). The relevance of these studies for understanding the foraging ecology of natural populations in a undisturbed forest is not clear. The present study is the first to be conducted on the diet of a naturally occurring population of aye-ayes in a undisturbed forest for a full annual cycle.

For this research, I examined the feeding, ranging, and positional behaviors of three aye-ayes, a male, a female and a juvenile over a two-year period in Torotorofotsy, an eastern rainforest of Madagascar. I also examined the developmental behavior of the

ii juvenile. My results indicate that the female preferentially consumed invertebrates, particularly those contained within live trees. Additionally, the diet of the female and her offspring mainly consisted of two resources, invertebrates and seeds of Canarium trees, unlike previous studies which suggested a diet of at least four main resources (Sterling

1993, 1994a).

I found both the female home range (713.6 ha) and the male home range

(1587.5ha) to be larger than previously reported (30-98 ha and 120-974 ha, respectively;

Sterling 1993, 1994; Randimbiharinirina et al. 2018). Furthermore, the female’s home range did not appear to change with seasons. Given the female consumed invertebrates throughout the year, and invertebrates occasionally were 100% of her diet, there is a strong possibility that invertebrates are dispersed throughout the environment and that the aye-aye large home range is needed to locate sufficient quantities of their preferred resource.

The female’s and juvenile’s most frequent positional behavior during locomotion was quadrupedal walking, however they frequently leaped and vertically leaped. This result is surprising given that the aye-aye’s intermembral index is higher than other quadrupedal lemurs, suggesting leaping would not occur frequently (Glander 1994).

During invertebrate foraging, both aye-ayes practiced vertical clinging and, frequently, climb and head-first descent. This is understandable given the aye-aye forelimb musculature is specially adapted for vertical positions requiring powerful manual grasping and elbow and wrist flexion. (Soligo 2005). Both findings suggest the aye-ayes

iii observed in undisturbed forest during this study were using specialized positional behaviors to maximize invertebrate feeding on vertical structures.

Most aspects of infant development were prolonged in free-ranging aye-ayes compared to captive aye-ayes. However, independent feeding developed at approximately the same pace. Aye-ayes have one of the longest juvenile periods in strepsirrhines (Feistner and Ashbourne 1994; Winn 1994) and are able to develop their brain and body throughout their ontogenetic period without experiencing an energetic tradeoff (Barrickman and Lin 2010). It is likely this extended growth period is related to the cryptic nature of their preferred food: invertebrates. The demands of locating and capturing insects using percussive foraging techniques requires a long learning period accompanied by a fully developed brain (Kaufman et al. 2005).

My results provide a baseline for aye-aye behaviors in undisturbed forest.

Establishing behavioral data in a pristine forest is an important first step for conservation

(Sutherland 1998) of this top 25 endangered primate (Randimbiharinirina et al. 2017).

Dedication

To Lucas and Owen. I will always be there to help you the same way you helped me. A promise and a threat.

Acknowledgments

There are many people to thank for their support, assistance and encouragement during this entire process. I want to thank W. Scott McGraw, my advisor, for his enthusiasm in my pursuit of aye-aye research. I might not have made thing easy, but from our first meeting to our last you have been amenable to this study and for that, and many other things, I am grateful. I also want to thank my dissertation committee members, Dawn Kitchen, Debbie Guatelli-Steinberg and Kristen Gremillion. Thank you for your guidance and feedback not only with this dissertation, but also with my development as a scholar.

My dissertation research was possible thanks to the financial support from

Columbus Zoo and Aquarium, Primate Conservation Inc., Sacramento Zoo, Cleveland

Metroparks Zoo, The Ohio State University Alumni Association, and The Ohio State

University Department of Anthropology. In addition, my eternal gratitude to Edward E.

Louis, Jr., Omaha’s Henry Doorly Zoo and Aquarium, and Madagascar Biodiversity

Partnership. This research would not have been possible without them. Lastly, a big thank you to Elise Sefczek for helping me get back and forth to Madagascar on numerous occasions.

I have the utmost appreciation for the work of the Madagascar Biodiversity

Partnership staff and guides. Thank you to Eddy Randriamandimbisoa, Liva

Rajoharison, Stephan Raharison, Luc Rakotobe, Ravaka Andriakotoarifidy, Alain

Randriamanalina, Nirina Ramampiandra, Hoby Rakotondramiarana, and Jonnah

Rakotonirina for helping make me feel welcome and relaxed when in Antananarivo. An enormous thank you to Joseph D. Rabekianja for all his hard work in Andasibe and

Torotorofotsy helping make sure I remained in one piece. This research would not have been possible without the efforts of Harison Razafimahaleo, Dimanche Jeanson, Joseph

Rakotomanana, Marcelin Ravelonjanahary, Honore Randriamaronirina, Olivier

Randrianarison, Harrison Randrianjatovo, Fenonampiana Aimee’ Randriatsimialona,

David Rafaralahy and Gabriel Mamy Manampisoa not only following the aye-aye and recording behaviors, but also making sure I never got lost in the forest. Additional thanks to Domenico Randimbiharinirina, Brigitte Raharivololona, the various darting teams,

Cynthia Frasier, Melissa Hawkins, and Rence Aimee Veloarivony Randrianindrina for their collaborations on everything Madagascar.

My appreciation to my OSU primate people. Noah Dunham, Erin Kane, Ashley

Edes, Dara Adams, Alex Wilkins, Kate Werling, and Jessica Walz thank you all for your shared experiences, the pains and joys. A great thanks to my fellow grad students for all the hours of class time and free time. Thank you to both Laurie Rosenberg and Wayne

Miller for their tireless efforts to ensure that funds were available and used to their fullest extent. An enormous debt of gratitude to Josh Sadvari in the OSU Library Research

Commons for his assistance in explaining how to use ArcGIS and how to make the various maps. I look forward to our future collaborations. A very special holla to Jesse

vii

Goliath who made enough time in the middle of everything for Thundercats …HO! Now we can end with a popsicle.

The biggest thank you goes to my family, immediate and extended. Bob, Donna,

Lisa, Dani, Jason, Mike, Margaret, Bobby, Tristan, and Sawyer thank you all for persevering through an endless barrage of questions, complaints and concerns. My boys

Owen and Lucas, who helped remind me of the bigger picture, and who were young enough to not remember that I left them for months at a time to pursue this research.

Lastly, to my wonderful wife Erin who has suffered through every step of this with me. I am so fortunate to have you in my life. Thank you for caring for our children without me, for foisting them on your parents for a month to visit Madagascar with me, and in general for being the eternal optimist. I love you.

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Vita

2017-2018 Adjunct Professor University of Cincinnati

2015 Adjunct Professor Columbus State Community College

2014-2015 Graduate Teaching Fellow The Ohio State University

2012-2017 Graduate Teaching Associate The Ohio State University

2009 M.A. (Anthropology) San Diego State University

2005 (Anthropology) SUNY at Stony Brook

2004 B.S. (Wildlife Biology) University of Vermont

Publications

2018 Sefczek TM, J Rakotomanana, H Randriamaronirina, and EE Louis, Jr. Unsuccessful predation event of an aye-aye (Daubentonia madagascariensis) by a fosa (Cryptoprocta ferox). Lemur News 21: 8-10.

2018 Sefczek TM, M Ravelonjanahary and EE Louis, Jr. A wild aye-aye (Daubentonia madagascariensis) raids chicken eggs in eastern Madagascar. Lemur News. 21: 10-11.

2017 Sefczek, TM, D Randimbiharinirina, BM Raharivololona, JD Rabekianja and EE Louis, Jr. Comparing the use of live trees and deadwood for larval foraging by aye-ayes (Daubentonia madagascariensis) at Kianjavato and Torotorofotsy, Madagascar. Primates 58: 535-546.

2014 Sefczek TM and NT Dunham. 2014. Forelimb and hindlimb musculature of the crab-eating macaque (Macaca fascicularis). The Ohio State University Knowledge Bank http://hdl.handle.net/1811/65221

2012 Sefczek, T.M., Z.J. Farris, P.C. Wright. 2012. Aye-aye feeding strategies at Ranomafana National Park, Madagascar: An indirect sampling method. Folia Primatologica 83(1): 1-10.

2012 Sefczek, T.M. 2012. Expanding their repertoire: Aye-aye feeding traces in a previously unreported tree genus. Lemur News 16: 27-28.

Fields of Study

Major Field: Anthropology

Table of Contents

Abstract ...... ii Dedication ...... v Acknowledgments...... vi Vita ...... ix List of Tables ...... xiii List of Figures ...... xxiii Chapter 1 Introduction ...... 1 General Methodology ...... 13 Chapter 2 Dietary profile, seasonal resource use, substrate use and food preference of an adult aye-aye (Daubentonia madagascariensis) in Torotorofotsy, Madagascar ...... 20 Introduction ...... 20 Methods...... 33 Results ...... 41 Discussion ...... 54 Conclusion ...... 68 Chapter 3 Home range size and seasonal variations in habitat use by aye-ayes (Daubentonia madagascariensis) in Torotorofotsy, Madagascar ...... 113 Introduction ...... 113 Materials and Methods ...... 126 Results ...... 129 Discussion ...... 135 Conclusion ...... 149 Chapter 4 Positional behavior of an adult female aye-aye (Daubentonia madagascariensis) and a sub-adult male aye-aye in Torotorofotsy, Madagascar ...... 168 Introduction ...... 168 Methods...... 190 Results ...... 198 xi

Discussion ...... 210 Conclusion ...... 233 Chapter 5 Behavioral development of a sub-adult male aye-aye (Daubentonia madagascariensis) at Torotorofotsy, Madagascar ...... 277 Introduction ...... 277 Methods...... 295 Results ...... 298 Discussion ...... 304 Conclusion ...... 319 Chapter 6 Conclusion ...... 328 Bibliography ...... 335 Appendix A. Daily and seasonal count of consumed Canarium seeds, invertebrates, Vakona resource, and water from Ravenala by Tsinjo between January 2016 and December 2017 at Torotorofotsy, Madagascar. Continued table...... 375 Appendix B. Daily and seasonal count of live tree, deadwood and bamboo substrates used by Tsinjo for invertebrate foraging between January 2016 and December 2017 at Torotorofotsy, Madagascar. Continued table...... 380

xii

List of Tables

Canarium fruit, number of Canarium seeds on the ground, and mature flowers on

Ravenala madagascariensis were enumerated along transects during the same period. . 75

Table 2.2 Results of G-test of goodness-of-fit comparing monthly abundance of different resources recorded along transects between January 2016 and December 2017 in

Torotorofotsy, Madagascar. Significant differences between months are highlighted in bold. There was 1 degree of freedom for all tests. Continued table...... 76

Table 2.3 Seasonal totals of food availability recorded along transects between January

2016 and December 2017 in Torotorofotsy, Madagascar...... 78

Table 2.4 Results of negative binomial regression analysis comparing seasonal abundance of different resources recorded along transects between January 2016 and

December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold...... 79

Table 2.5 Results of the negative binomial regression analysis for annual comparison of resource availability along transects between January 2016 and December 2017 in

Torotorofotsy, Madagascar...... 80

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Table 2.6 Monthly dietary profile of Tsinjo during the study period. Records for feeding on Canarium seeds in ripe fruit, Vakona, Ravenala and invertebrate feeding were based on direct observations. All data recorded during follows of Tsinjo between January 2016 and December 2017 at Torotorofotsy, Madagascar...... 81

Table 2.7 Results of tests for differences between the number of Canarium seeds in ripe fruit consumed and number of invertebrates consumed within each month between

January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant results of the negative binomial regression analysis indicating differences within months are highlighted in bold...... 82

Table 2.8 Results of negative binomial regression analysis, which tests whether the amount of each resource changed significantly from one month to the next. Significant differences are indicated with bold text...... 83

Table 2.9 Seasonal dietary profile of Tsinjo during the study period. All dietary data were based on direct observations. All data were recorded during follows of Tsinjo between January 2016 and December 2017 at Torotorofotsy, Madagascar...... 84

Table 2.10 Results of the negative binomial regression analysis comparing consumption of Canarium seeds in ripe fruit to invertebrate consumption each season by Tsinjo between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold...... 85

Table 2.11 Results of negative binomial regression analysis for seasonal comparisons of consumption rates by Tsinjo between January 2016 and December 2017 in Torotorofotsy,

Madagascar. Significant differences between seasons are highlighted in bold...... 86

xiv

Table 2.12 Results of negative binomial regression analysis for comparing annual resource consumption rates by Tsinjo between January 2016 and December 2017 in

Torotorofotsy, Madagascar...... 87

Table 2.13 Monthly number of traces made in live trees, deadwood and bamboo by

Tsinjo for consuming invertebrates between January 2016 and December 2017 at

Torotorofotsy, Madagascar...... 88

Table 2.14 Results of negative binomial regression analysis which tests whether live trees, deadwood and bamboo were used in different proportions within a given month.

Significant differences between months are highlighted in bold...... 89

Table 2.15 Results of negative binomial regression analysis for monthly comparison of substrate use for invertebrate foraging by Tsinjo between January 2016 and December

2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold...... 90

Table 2.16 Seasonal use of live trees, deadwood and bamboo by Tsinjo for consuming invertebrates between January 2016 and December 2017 at Torotorofotsy, Madagascar.

...... 91

Table 2.17 Results of the negative binomial regression analysis comparing use of substrates by Tsinjo within each season from January 2016 to December 2017 in

Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold...... 92

Table 2.18 Results of negative binomial regression analysis for seasonal comparison of substrate use for invertebrate foraging by Tsinjo between January 2016 and December

2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold...... 93

Table 2.19 Results of negative binomial regression analysis for annual comparison of substrate use for invertebrate foraging by Tsinjo between January 2016 and December

2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold...... 94

Table 2.20 Monthly preference indices for resource consumption by Tsinjo between

January 2016 and December 2017 at Torotorofotsy, Madagascar. Values below 1 indicate non-preference for Canarium seeds in ripe fruit...... 95

Table 2.21 Seasonal preference indices for resource consumption by Tsinjo at

Torotorofotsy, Madagascar. Values below 1 indicate non-preference for Canarium seeds in ripe fruit...... 96

Table 2.22 Annual preference indices for resource consumption by Tsinjo at

Torotorofotsy, Madagascar. Values below 1 indicate non-preference for Canarium seeds in ripe fruit...... 97

Table 3.1 The number of GPS points and associated behaviors performed by Tsinjo and

Masy. Data for Masy were collected between January 2014 and December 2017. Data for Tsinjo were collected between January 2016 and December 2017...... 154

Table 3.2 Estimated overall home range sizes for Tsinjo and Masy based on MCP and

KDE methods. KDE is broken down into 95%, 50% and 10% isopleths indicating the size of the area most frequently used, from least to most often...... 155

xvi

Table 3.3 The number of GPS points taken for Tsinjo annually and seasonally, between

January 2016 and December 2017...... 156

Table 3.4 The number of GPS points taken for the various behaviors of Tsinjo each season between January 2016 and December 2017. Infrequent behaviors included copulation, grooming and playing...... 157

Table 3.5 Annual home range sizes for Tsinjo in 2016 and 2017 based on KDE methods.

The 95%, 50% and 10% isopleth values are reported...... 158

Table 3.6 Seasonal home range size estimates between January 2016 and December 2017 for Tsinjo based on KDE methods. The 95%, 50% and 10% isopleth values are reported.

...... 159

Table 4.1 Number of follows conducted each month for Tsinjo and Cobalt in

Torotorofotsy, Madagascar...... 235

Table 4.2 Total occurrences, average distances, and frequency of occurrence for all locomotor behaviors by Tsinjo and Cobalt between May 2017 and December 2017. ... 236

Table 4.3 Number of times observed, average distance, and frequency of each locomotor behavior during travel by Tsinjo and Cobalt between May 2017 and December 2017 in

Torotorofotsy, Madagascar...... 237

Table 4.4 Number of time observed, average duration, and frequency of each foraging behavior by Tsinjo and Cobalt between May 2017 and December 2017 in Torotorofotsy,

Madagascar...... 238

xvii

Table 4.5 Number of times observed, average duration, and frequency of each postural behavior during feeding by Tsinjo and Cobalt between May 2017 and December 2017 in

Torotorofotsy, Madagascar...... 239

Table 4.6 Locomotor behavior and forest strata use during travel by Tsinjo and Cobalt between May and December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a locomotor behavior across the forest strata. Underlined % represents the frequency of each locomotor behavior within a forest stratum. Bold % represents the frequency of locomotor behavior use or stratum use...... 240

% represents the frequency of each locomotor behavior on a single support type. Bold % represents the frequency of locomotor behavior use or support use...... 242

Table 4.8 Foraging behavior and forest strata use by Tsinjo and Cobalt between May and

December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a locomotor behavior across the forest strata. Underlined % represents the frequency of each locomotor behavior within a forest stratum. Bold % represents the frequency of locomotor behavior use or stratum use...... 244

Table 4.9 Foraging behavior and support use by Tsinjo and Cobalt between May and

December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a locomotor behavior across the various supports. Underlined % represents the

xviii frequency of each locomotor behavior on a single support type. Bold % represents the frequency of locomotor behavior use or support use...... 245

Table 4.10 Postural behavior and forest strata use during feeding by Tsinjo and Cobalt between May and December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a postural behavior across the forest strata. Underlined % represents the frequency of each postural behavior within a forest stratum. Bold % represents the frequency of locomotor behavior use or stratum use...... 246

% represents the frequency of each postural behavior on a single support type. Bold % represents the frequency of locomotor behavior use or support use...... 247

Table 4.12 Number of occurrences of a locomotor behavior during travel by Tsinjo between May 2017 and December 2017 in Torotorofotsy, Madagascar. Data are presented according to occurrences within a given forest stratum and on a given support.

Overall occurrences and frequency of observation within a stratum or on a substrate are in bold...... 248

Table 4.13 Number of occurrences of a foraging behavior by Tsinjo between May 2017 and December 2017 in Torotorofotsy, Madagascar. Data are presented according to occurrences within a given forest stratum and on a given support. Overall occurrences and frequency of observation within a stratum or on a substrate are in bold...... 249

xix

Table 4.14 Number of occurrences of a positional behavior during feeding by Tsinjo between May 2017 and December 2017 in Torotorofotsy, Madagascar. Data are presented according to occurrences within a given forest stratum and on a given support.

Overall occurrences and frequency of observation within a stratum or on a substrate are in bold...... 250

Table 4.15 Number of occurrences of a locomotor behavior during travelling by Cobalt between May 2017 and December 2017 in Torotorofotsy, Madagascar. Data are presented according to occurrences within a given forest stratum and on a given support.

Overall occurrences and frequency of observation within a stratum or on a substrate are in bold...... 251

Table 4.16 Number of occurrences of a foraging behavior by Cobalt between May 2017 and December 2017 in Torotorofotsy, Madagascar. Data are presented according to occurrences within a given forest stratum and on a given support. Overall occurrences and frequency of observation within a stratum or on a substrate are in bold...... 252

Table 4.17 Number of occurrences of a positional behavior during feeding by Cobalt between May 2017 and December 2017 in Torotorofotsy, Madagascar. Data are presented according to occurrences within a given forest stratum and on a given support.

Overall occurrences and frequency of observation within a stratum or on a substrate are in bold...... 253

Table 4.18 Pairwise comparison results for distances traveled by Tsinjo while performing positional behaviors during locomotion between May 2017 and December 2017 in

Torotorofotsy, Madagascar. Significant differences between positional behavioral frequencies are highlighted in bold...... 254

Table 4.19 Pairwise comparison results for travel distances covered by Tsinjo during bridging in various forest levels between May 2017 and December 2017 in

Torotorofotsy, Madagascar. N/A indicates the statistical test could not be performed because of tied values. Significant differences between distances within forest levels are highlighted in bold...... 255

Table 4.20 Pairwise comparison results for travel distances covered by Tsinjo during leaping in various forest levels between May 2017 and December 2017 in Torotorofotsy,

Madagascar. Significant differences between forest levels are highlighted in bold...... 256

Table 4.21 Pairwise comparison results for travel distances covered by Tsinjo during vertical clinging and leaping in various forest levels between May 2017 and December

2017 in Torotorofotsy, Madagascar. Significant differences between forest levels are highlighted in bold...... 257

Table 4.22 Pairwise comparison results for travel distances covered by Tsinjo during climbing in various forest levels between May 2017 and December 2017 in

Torotorofotsy, Madagascar. Significant differences between forest levels are highlighted in bold...... 258

Table 4.23 Pairwise comparison results for travelling distances covered by Tsinjo during head-first descent in various forest levels between May 2017 and December 2017 in

Torotorofotsy, Madagascar. Significant differences between forest levels are highlighted in bold...... 259

xxi

Table 4.24 Pairwise comparison results for distances traveled with each positional locomotion behavior performed by Cobalt between May 2017 and December 2017 in

Torotorofotsy, Madagascar. Significant differences between positional behavioral frequencies are highlighted in bold...... 260

Table 5.1 Number of night follows, number of occurrences of each behaviors and monthly percent of overall behaviors by Cobalt between August 2016-December 2017 in

Torotorofotsy, Madagascar...... 322

Table 5.2 Frequency of association (within 5m) between Cobalt and Tsinjo outside of the nest every month from August 2016-December 2017 in Torotorofotsy, Madagascar. .. 323

Table 5.3 Number of resources consumed and rate of consumption per minute for invertebrates in live trees, deadwood, or bamboo, and seeds of Canarium by Cobalt between September 2016 and December 2017 in Torotorofotsy, Madagascar...... 324

Table 5.4 Number of total follows and morning follows, as well as average distances traveled each month by Tsinjo and Cobalt from January 2016 to December 2017 in

Torotorofotsy, Madagascar...... 325

xxii

List of Figures

Figure 1.1 The clawed, elongated digits, large, bat-like ears and metacarpophalangeal joint in the 3rd digit of an aye-aye. Photo by author...... 15

Figure 1.2 Various sized larvae removed from a piece of deadwood in Torotorofotsy,

Madagascar. Photo by author...... 16

Figure 1.3 Location of Torotorofotsy on the island of Madagascar...... 17

Figure 1.4 Part A, B and C The forest at Torotorofotsy, Madagascar. Photos by author. 18

Figure 1.5 Images of various lemurs in Torotorofotsy. From top left to bottom right:

Lepilemur, Indri, Cheirogaleus, Microcebus, Eulemur, Daubentonia, Avahi, Propithecus.

All photos by author...... 19

Figure 2.1 Part A Fruit of Canarium sp.; Part B Feeding traces from aye-ayes in seeds of

Canarium sp. Photos by author...... 98

Figure 2.2 Inflorescence of Ravenala madagascariensis. Photo by author...... 99

Figure 2.3 Tsinjo, the focal animal, gnawing into a live tree in Torotorofotsy,

Madagascar...... 100

Figure 2.4 Location of transects, Canarium trees and Ravenala trees in Torotorofotsy,

Madagascar. The white border is the home range of Tsinjo...... 101

Figure 2.5 Part A and Part B New feeding traces in live trees made by aye-ayes in

Torotorofotsy, Madagascar. Photos by author...... 102

Figure 2.6 New feeding traces in deadwood made by an aye-aye in Torotorofotsy,

Madagascar. Photo by author...... 103

xxiii

Figure 2.7 New feeding traces left in bamboo by an aye-aye in Torotorofotsy,

Madagascar. Photo by author...... 104

Figure 2.8 Old feeding trace left in a live tree by an aye-aye. Photo by author...... 105

Figure 2.9 Monthly consumption of resources by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017...... 106

Figure 2.10 Part A Inferior view of a Vakona tree fed on by Tsinjo; Part B Tsinjo on top of a Vakona tree with view of seeds contained within the fronds. Photos by author. .... 107

Figure 2.11 Seasonal consumption of resources by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017...... 108

Figure 2.12 Annual consumption of resources by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017...... 109

Figure 2.13 Monthly use of substrates for invertebrate foraging by Tsinjo in

Torotorofotsy, Madagascar from January 2016 to December 2017...... 110

Figure 2.14 Seasonal use of substrates for invertebrate foraging by Tsinjo in

Torotorofotsy, Madagascar from January 2016 to December 2017...... 111

Figure 2.15 Annual use of substrates for invertebrate foraging by Tsinjo in Torotorofotsy,

Madagascar from January 2016 to December 2017...... 112

Figure 3.1 The 100% MCP home ranges for Masy (white) and Tsinjo (black) from data points between January 2016 and December 2017...... 160

Figure 3.2 The KDE ranges for Masy (blue) and Tsinjo (orange) from data points between January 2016 and December 2017. Solid black line and dotted white lines represent the 100% MCP home ranges for Tsinjo and Masy, respectively...... 161

xxiv

Figure 3.3 The 2016 KDE home ranges for Tsinjo. The white line represents the 100%

MCP home range. Maps include all data points in 2016 (part A), all points during season

1 of 2016 (part B), all points during season 2 of 2016 (part C), and all points during season 3 of 2016 (part D)...... 162

Figure 3.4 The 2017 KDE home ranges for Tsinjo. The white line represents the 100%

MCP home range. Maps include all data points in 2017 (part A), all points during season

1 of 2017 (part B), all points during season 2 of 2017 (part C), and all points during season 3 of 2017 (part D)...... 163

Figure 3.5 The 2016 KDE home ranges for Tsinjo with feeding points overlaid. The white line represents the 100% MCP home range. Maps include all data points for 2016

(part A), all points during season 1 of 2016 (part B), all points for season 2 of 2016 (part

C), and all points for season 3 of 2016 (part D). In all maps, invertebrate feeding is represented by blue circles and Canarium feeding by green circles...... 164

Figure 3.6 The 2017 KDE home ranges for Tsinjo with feeding points overlaid. The white line represents the 100% MCP home range. Maps include all data points for 2017

(part A), all points in season 1 of 2017 (part B), all points in season 2 of 2017 (part C), and all points in season 3 of 2017 (part D). Invertebrate feeding is represented by blue circles, Canarium feeding by green circles and Vakona feeding by red circles...... 165

(part C), and all points in season 3 of 2016 (part D). Red squares are high-high clusters

xxv and blue squares are low-high outliers. Squares without a fill-in color had no GPS points.

...... 166

(part C), and all points in season 3 of 2017 (part D). Red squares are high-high clusters and blue squares are low-high outliers. Squares without a fill-in color had no GPS points.

...... 167

Figure 4.1 Forest levels recognized in this study...... 261

Figure 4.2 Perch: Tsinjo’s hind limbs hold a branch, while her hands hold a Canarium seed. Photo by author...... 262

Figure 4.3 Tap: Cobalt lightly strikes a branch with his 3rd digit. Photo by author...... 263

Figure 4.4 Gnaw: Tsinjo bites into a live tree. Photo by author...... 264

Figure 4.5 Probe: Tsinjo inserts her 3rd digit in a live tree to forage for invertebrates.

Photo by author...... 265

Figure 4.6 Bi-manual cling: Tsinjo foraging on bamboo, clinging with both hands. Photo by author...... 266

Figure 4.7 Uni-manual cling: Tsinjo holds on with one hand while foraging at a live tree.

Photo by author...... 267

Figure 4.8 Hindlimb suspension: Tsinjo hangs from bamboo with her hindlimbs. Photo by author...... 268

xxvi

Figure 4.9 Quadrupedal suspension: Cobalt hangs from a support by all four limbs.

Photo by author...... 269

Figure 4.10 Number of occurrences of positional behaviors during travel for Tsinjo and

Cobalt between May and December 2017 in Torotorofotsy, Madagascar...... 270

Figure 4.11 Number of occurrences of positional behaviors during foraging for Tsinjo and Cobalt between May and December 2017 in Torotorofotsy, Madagascar...... 271

Figure 4.12 Number of occurrences of postural behaviors during feeding for Tsinjo and

Cobalt between May and December 2017 in Torotorofotsy, Madagascar...... 272

Figure 4.13 Biplot for correspondence analysis of Tsinjo’s support and forest level use during travel. Red triangles signify forest level (US: understory, LC: low canopy, MC: main canopy, HC: high canopy, EM: emergent layer) and blue circles identify support

(TR: trunk, BO: bough, BR: branch, TW: twig, LI: liana and bamboo)...... 273

Figure 4.14 Biplot for correspondence analysis of Tsinjo’s support and forest level use during foraging. Red triangles signify forest level (GR: ground, US: understory, LC: low canopy, MC: main canopy, HC: high canopy) and blue circles identify support (TR: trunk, BO: bough, BR: branch, LI: liana and bamboo)...... 274

Figure 4.15 Biplot for correspondence analysis of Cobalt’s support and forest level use during travel. Red triangles signify forest level (GR: ground, US: understory, LC: low canopy, MC: main canopy, HC: high canopy, EM: emergent layer) and blue circles identify support (TR: trunk, BO: bough, BR: branch, TW:twig, LI: liana and bamboo).

...... 275

xxvii

Figure 4.16 Biplot for correspondence analysis of Cobalt’s support and forest level use during foraging. Red triangles signify forest level (US: understory, LC: low canopy, MC: main canopy, HC: high canopy) and blue circles identify support (TR: trunk, BO: bough,

BR: branch, LI: liana and bamboo)...... 276

Figure 5.1 Occurrences of resting, traveling and feeding behaviors for Cobalt from

August 2016 through December 2017...... 326

Figure 5.2 Number of invertebrates in various substrates (live tree, deadwood and bamboo) and Canarium seeds consumed by Cobalt between September 2016 and

December 2017...... 327

xxviii

Chapter 1 Introduction

This chapter provides an overall project summary and introduces the overarching research questions associated with the study taxon, Daubentonia madagascariensis, the aye-aye. It provides a basic introduction to aye-aye morphology, reviews the handful of field studies conducted on this species, establishes the theoretical foundation for this dissertation, provides a brief overview of the field site and general methodologies, and concludes with brief summaries of each subsequent chapter.

Aye-ayes (Daubentonia madagascariensis) are the most morphologically specialized non-human primates. They exhibit a suite of extreme features that includes continuously growing incisors, elongated, clawed digits, large, bat-like ears, a nictitating membrane, and a unique metacarpophalangeal joint in their third digits (Figure 1.1; Owen

1863; Jouffroy 1975; Cartmill 1979; Martin 1990; Sterling 1993, 1994a; Simons 1995;

Soligo 2005). These traits are used in combination to echolocate insect larvae embedded in woody substrates, a feeding behavior referred to as percussive foraging (Figure 1.2;

Petter 1962, 1977; Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991; Erickson et al. 1998; Dominy et al. 2001). Aye-ayes are clearly adapted to forage for insect larvae and have traditionally been considered predominantly insectivorous strepsirrhines (Owen

1863; Petter 1962, 1977; Gaulin 1979). Among primates, there is a well-established relationship between body size and insectivory (Kay 1975). In general, primates with

1 body masses exceeding 500g are not expected to be primarily insectivorous. The reason is that primates in excess of 500g would have to work too hard at acquiring sufficient insects to meet their energetic requirements. The average body mass of aye-ayes is

2.6kg, which greatly exceeds the 500g threshold (Kay 1975), implying that a) Kay’s threshold does not apply to aye-ayes in the manner it does to other primates, b) the traditional characterization of aye-ayes as predominantly insectivorous is inaccurate, or c) some combination of these.

Recent field data indicates that insectivory in aye-ayes may not be as codified as earlier reports suggest (Iwano and Iwakawa 1988; Iwano 1991; Sterling 1993, 1994a).

Data collected from two field sites reveal that aye-ayes (1) are granivorous, mainly consuming seeds of Canarium sp. (Iwano and Iwakawa 1988, Iwano 1991), (2) preferentially consume nectar from Ravenala madagascariensis trees (Ancrenaz et al.

1994), or (3) consume a combination of structurally defended resources, Canarium seeds and insect larvae, as well as Ravenala nectar and cankerous growths (Sterling 1993,

1994a). There are good reasons to be cautious when exploring elements of aye-aye feeding morphology based solely on these data. Two of the three data sets are derived from studies conducted on an introduced population on the island of Nosy Mangabe,

Madagascar (Iwano and Iwakawa 1988; Iwano 1991; Sterling 1993, 1994a). Before their introduction, aye-ayes were not present on the island, and its lack of predators implies very different selective pressures. The third data set was derived from a three-month study in a disturbed forest, Mananara-Nord Biosphere Reserve (Ancrenaz et al. 1994).

Because this reserve consists of heavily degraded forest adjacent to coconut plantations

2 routinely raided by aye-ayes, the relevance of this study for understanding the foraging ecology of natural populations is questionable.

It is well established that aye-ayes are at least partially insectivorous, but the degree of insectivory and details of dietary ecology in a population ranging in undisturbed forest for at least a full annual cycle are not yet known. Furthermore, we lack important information on 1) the relationship between seasonal shifts in diet and ranging behaviors, 2) the positional behavior of aye-ayes during feeding, foraging, and travel, and 3) the ontogeny of foraging behavior.

For this dissertation, I conducted a 24-month study on aye-ayes in the

Torotorofotsy forest of eastern Madagascar. I collected data on the diet, feeding, ranging and positional behavior of three individuals; two adults, one male and one female, and the female’s male offspring. Due to observational difficulties, the great majority of dietary and feeding behavior were collected on the adult female, who is referred to as Tsinjo.

Data on home range size were collected for both the adult male, known as Masy, and the adult female. Data on nightly path length were collected for the adult female and her offspring, named Cobalt. Seasonal ranging patterns were established for the adult female. Positional behavior data were collected on the adult female and her son.

Developmental feeding behaviors were collected on Cobalt. To better understand the constraints on and covariants with feeding and foraging, I collected data on 1) the types and spatial distribution of resources consumed, 2) the location of feeding sites, 3) the duration of foraging bouts, 4) quantities of items consumed during each bout, 5) the seasonal changes in resource abundance, 6) seasonal changes in ranging, 7) positional

3 behaviors used during travel, and 8) positional behaviors (postural and locomotor) used during feeding. Items 1-6 were collected:

a) in an effort to determine what foods are preferred by aye-ayes

b) if fallback foods (Lambert 2007; Marshall and Wrangham 2007) are a major

component of the aye-aye dietary profile, and

c) to test which resource(s) have the greatest influence on aye-aye ranging

behavior.

This project was undertaken to address the relationship between aye-aye morphology and dietary ecology in a natural population. To date, this study is the first to be conducted on a population in a undisturbed forest for at least two annual cycles, and therefore provides an informed window into the behavior of this enigmatic primate.

In Chapter 2, I explore the feeding behaviors of aye-ayes in undisturbed forest.

Current understanding of aye-ayes’ feeding behaviors is based on an amalgamation of studies in various habitats; data from a undisturbed forest are lacking, resulting in an incomplete behavioral profile. The earliest feeding studies were conducted in disturbed forests adjacent to plantations and characterized aye-ayes as predominantly insectivorous

(Petter 1962, 1977). Kay (1975) examined the molar morphology of aye-ayes and concluded they were adapted for a diet of fruit. In addition, based on his analysis of body size and diet across all primates, Kay (1975) suggested that aye-ayes were too large

(2.6kg) to be predominantly insect larvae predators, raising the possibility of greater dietary breadth in aye-ayes. Additional field studies by Iwano and Iwakawa (1988) and

Sterling (1993, 1994a) leant support to Kay’s hypothesis and established that, in addition

4 to large quantities of larvae, aye-ayes consume significant amounts of Canarium seeds.

As discussed above, the utility of these field studies is limited because of their location and the extent to which aye-ayes utilize invertebrates in their natural habitat is not yet known.

Anthropologists have long been interested in understanding how elements of diet shape aspects of morphology and behavior. A central component of this research is describing how primates value different resources. One such paradigm is the preferred versus fallback scheme (Emlen 1966; Johnson 1980; Stephens and Krebs 1986; Kinzey and Norconk 1990; Leighton 1993; Lambert 2007; Marshall and Wrangham 2007).

Preferred foods are those that are consumed in proportions greater than predicted by their availability, a designation which requires an independent assessment of abundance

(Emlen 1966; Johnson 1980; Stephens and Krebs 1986; Leighton 1993). Such foods are frequently, but not always, easy to acquire and process (Emlen 1966; Johnson 1980;

Stephens and Krebs 1986; Leighton 1993; Marshall and Wrangham 2007). Alternatively, fallback foods tend to be abundant, lower-quality resources that are typically difficult to process due to their mechanical properties (Kinzey and Norconk 1990; Lambert 2007;

Marshall and Wrangham 2007). Certain bodies of theory predict that organisms will ‘fall back’ on such foods when preferred resources are scarce (Lambert 2007; Marshall and

Wrangham 2007; Marshall et al. 2009). This theoretical framework has been used to interpret the anatomy of various primates with some controversy. For example, the elongated hindgut in Callimico goeldii is almost certainly an adaptation for digesting this monkey’s preferred food, fungi (Porter et al. 2008). On the other hand, a single feature

5 can be interpreted in a multitude of ways. For example, the thick enamel in grey-cheeked mangabeys, Lophocebus albigena, has been convincingly argued to be an adaptation to processing fallback items, such hard seeds and bark (Lambert et al. 2004). Alternatively, the thick enamel in sooty mangabeys, Cercocebus atys, is argued to be an adaptation for the routine processing of extremely hard seeds which are consumed year-round and are preferred (McGraw et al. 2014). Sterling and McCreless (2006: 164) claim that aye-ayes are not primarily insectivorous, suggesting instead that insect larvae are consumed when their preferred resources are less available. Thus, in this instance, insect larvae represent a stable resource that is available throughout the year and occurs in high-density patches.

This suggests that invertebrates are a fallback food and that aye-aye feeding morphology was developed in response to the consumption of a fallback resource. This hypothesis is complicated by the fact that invertebrates are a high-energy resource (Sterling 1993,

1994a), which is atypical of most fallback foods (but see McGraw et al. 2014). If insect larvae are the most frequently consumed resource monthly, seasonally and annually, they can be considered preferred. However, if another food item is consumed more often than insects during some part of the year, then Sterling and McCreless’s (2006) conclusion that insect larvae are fallback foods could be supported. I hypothesize that aye-ayes prefer invertebrates but that they supplement their diet with different food items throughout the year. In Chapter 2, I combine data on feeding and seasonal resource availability to test two hypotheses which assess the role of invertebrates in the diet of the adult female aye-aye.

In Chapter 3, I examine the ranging behaviors of an adult male and female aye- aye. To date, there have been two studies examining aye-aye home range size, one on an introduced population on the island of Nosy Mangabe (Sterling 1993, 1994a) and one in the disturbed forest of Kianjavato (Randimbiharinirina et al. 2018). Information on aye- aye home range size in a undisturbed forest is not yet available, which makes any attempt to understand the complexities of aye-aye feeding behavior under natural conditions extremely difficult. In addition, there are as yet no studies on how aye-aye ranging behavior changes seasonally, further complicating attempts to understand the habitat requirements of these endangered primates. Tropical environments are known to vary seasonally with significant differences in rainfall and sunlight impacting floral productivity (MacArthur 1972; van Schaik et al. 1993; van Schaik and Pfannes 2005;

Myneni et al. 2007). One way primates can respond to seasonal fluctuations in resource abundance is by altering their ranging behaviors. Optimal foraging theory is a framework that anticipates an organism’s behaviors when searching for food (MacArthur 1972).

This model predicts and empirical evidence demonstrates that primates can respond the same way to different patterns of resource availability. For example, primates can (1) range further when preferred foods are abundant in order to acquire more of that resource

(Stephens et al. 1986), (2) range further when preferred foods are scarce, in order to locate that food item (Hemingway and Bynum 2005), or (3) maintain a consistent ranging behavior and alter the diet based on approximate availability (Stone 2007). In

Madagascar, forests are asynchronous in floral production, with unpredictable peaks in fruit, flower and leaf production from year to year (Wright 1999). While lemurs are

7 known to increase home range size in periods of preferred food abundance (Richard

1977) and scarcity (Overdorff et al. 1997; Sauther 1998), no lemur is known to maintain a consistent ranging behavior over the course of an entire year (Wright 1999, 2006).

Because invertebrates are available throughout the year (Sterling and McCreless 2006) and may be evenly distributed throughout the environment (Sefczek et al. 2017), I hypothesize that the ranging behavior of aye-ayes will not change significantly over the course of the year because of invertebrate ubiquity. I used GPS data to establish home range size for the adult male and adult female aye-aye. I used GPS data on feeding and ranging in the female to test my hypothesis.

Chapter 4 presents information on the locomotion and posture, i.e. positional behavior, of aye-ayes. Positional behaviors are adaptations that improve a primate’s fitness in their environment (Cant 1992). Positional behavior within a habitat is constrained by body size, and therefore restricts the resources that could be consumed and types of behaviors employed to access them (Fleagle and Mittermeier 1980; Cant

1992). For example, across primates, as body size increases the frequency of leaping decreases while incidences of climbing increase (Fleagle and Mittermeier 1980). Large- bodied primates are more likely to be suspensory and engage in little leaping due to the constraints imposed by habitat and physics, as well as the location of food in arboreal environments. Exceptions to these general principles usually invoke unique morphological adaptations. For example, the Indri, Indri indri, is able to vertically cling and leap because their deep crouching position allows for generation of propulsive forces from the hip rather than the foot (Demes et al. 1996). Most importantly, most studies

8 have shown that there is no association between diet and positional behavior (Fleagle and

Mittermeier 1980). For example, leaping primates are known to be highly insectivorous

(Tarsius, Galago), folivorous (Indri, Colobus), and frugivorous (Propithecus, Pithecia).

In addition, most studies suggest that aye-ayes are generalized arboreal quadrupeds unlikely to leap often (Curtis 1992; Curtis and Feistner 1994; Glander 1994).

To date, only one study has been conducted on aye-aye positional behavior in the wild. That study focused primarily on locomotion and consisted of three-months of observations on a total of five individuals ranging in the disturbed forest of Mananara-

Nord Biosphere Reserve (Ancrenaz et al. 1994). Additional research has been conducted on aye-aye locomotion in captivity (Curtis 1992; Curtis and Feistner 1994). These studies provide a general introduction to aye-aye locomotion and posture; however, in order to fully understand how locomotion during travel and foraging and postures employed during feeding are related to other aspects of aye-aye behavior, it is necessary to examine the behavior of free-ranging animals in a broader ecological context (Ripley

1967). Generating hypotheses for aye-aye positional behavior is complicated by the absence of appropriate comparative models: the aye-aye is a unique primate. However, the overwhelming majority of positional behavior studies of other primates have established that many positional adaptations are most interpretable in terms of feeding constraints (Fleagle 1975). If true, I expect that the overall positional repertoire of this primate is most interpretable in terms of feeding constraints combined with cryptic movement. I hypothesize that aye-ayes in the undisturbed forest of Torotorofotsy,

Madagascar will exhibit locomotor adaptations during travel and foraging and postures

9 during feeding that maximize acquisition of invertebrates while remaining as inconspicuous as possible.

Chapter 5 examines the general behavioral repertoire of a subadult male aye-aye, with the goal of understanding how developing aye-ayes acquire their critical foraging skills. The subadult phase of a primate’s life, specifically that period following weaning and preceding first reproduction, is particularly dangerous because individuals are relatively large-bodied but inexperienced (Jansen and van Schaik 1993; Pereira 1993). It has been argued that this long juvenile period in primates has evolved to provide growing individuals sufficient time to learn how to meet their dietary requirements while avoiding predation threats (Jansen and van Schaik 1993; Kappeler 1998; Ross 1998; Kappeler et al. 2003). According to the ecological risk aversion hypothesis (RAH), primates with ubiquitously distributed resources should start feeding independently at a younger age than those with unpredictable and more patchily distributed resources (Jansen and van

Schaik 1993). The rationale for this prediction is that when a primate’s food is plentiful the stress of weaning is diminished because the potential risk period due to low resource availability is shortened and competition with conspecifics is decreased (Jansen and van

Schaik 1993). Under these conditions, we would expect the young to grow rapidly.

Primates reliant on more patchily distributed resources, which are prone to greater fluctuations in abundance, both temporally and spatially, would be more prone to starvation. Under these conditions, slower growth provides a safety factor in response to potentially volatile food sources (Jansen and van Schaik 1993).

Research suggests that lemurs do not conform to predictions of the RAH. For example, folivorous species, such as Indri indri, develop more slowly than their frugivorous counterparts, such as Eulemur fulvus rufus (Godfrey et al. 2004). It has been suggested that the unpredictable seasonality in Madagascar, which translates to irregular resource abundance, is partially responsible for unusual lemur life histories (Wright

1999). Specifically, lemur life history strategies may be a response to maintaining sustainable populations by maximizing adult female survival and reproductive opportunities (Godfrey et al. 2004: 271). For example, female lemurs with parked or nested infants expend less energy and increase energy intake ultimately resulting in more investment in offspring, compared to alloparenting lemurs that carry young (Tecot et al.

2012).

In addition to the effects of RAH, primates’ enlarged brain size may necessitate an extended developmental period (Charnov and Berrigan 1993; Isler and van Schaik

2006, 2009). One explanation for the relationship between encephalization and prolonged ontogenetic period is that there is a high energetic demand associated with brain growth; consequently, primates will experience an energetic trade-off in maturation to facilitate the demands of growing a larger brain (Charnov and Berrigan 1993; Isler and van Schaik 2006, 2009). Alternatively, it may be that maternal body size and age at maturation determine the rate of brain development in offspring, with larger and older females producing infants with larger brains that develop more quickly (Leigh 2004;

Leigh and Blomquist 2007). A third hypothesis indicates that extractive foraging behaviors are strongly associated with enlarged brains and necessitate protracted

11 developmental periods to learn complicated behaviors (Parker and Gibson 1977, 1979;

Gibson 1986; Reader et al. 2011; Parker 2015). The association between life history and brain size becomes particularly salient for aye-ayes because they have the largest body size of any nocturnal primate and the greatest encephalization quotient of any strepsirrhine (Stephan et al. 1981). Research has indicated that the aye-aye’s enlarged brain is strongly associated with percussive foraging as this behavior necessitates high levels of sensorimotor cognition (Kaufman et al. 2005). Given the unusual ecology of

Madagascar and the extractive foraging behavior of aye-ayes, it is likely that a multitude of factors may be influencing the life history strategy of this lemur.

Only two studies have examined the general behavioral repertoires of non-adult aye-ayes, both of which focused on captive individuals (Feistner and Ashbourne 1994;

Winn 1994). Information on infant development on free-ranging individuals is non- existent. Many studies have shown that captive primates of any species tend to have shorter developmental periods than their wild counterparts (Anderson and Simpson 1979;

Fairbanks and McGuire 1984; Lee 1987). Interestingly, available data suggest that captive aye-ayes have a particularly long period of infant dependency compared to other lemurs studied to date (Feistner and Ashbourne 1994; Winn 1994). If the aforementioned captive versus wild dichotomy holds (Anderson and Simpson 1979; Fairbanks and

McGuire 1984; Lee 1987), then we would expect that free-ranging subadult aye-ayes will have even longer periods of infant growth and development. I hypothesize that aye-aye infant development, specifically related to feeding and foraging, is slower than that of their captive counterparts. I explore the notion that the delayed development of aye-ayes

12 is due to (1) the ubiquity of invertebrates and (2) encephalization because of extractive foraging.

General Methodology

This study took place in the undisturbed forest of Torotorofotsy, Madagascar

(18o52’S, 42o22’E; Figure 1.3), a natural wetland about 1100 ha in size, adjacent to

Mantadia National Park and approximately 10km northwest of the town Andasibe. The forest (Figure 1.4a, 1.4b, 1.4c) is neither a national park or a forest reserve, but rather a community-managed parcel adjacent to several small villages and managed by

MITSINJO, an Andasibe-based organization focused on tourism, research and conservation. Torotorofotsy forest is the most intact wetland in the Andasibe-Mantadia-

Zahamena eastern rainforest corridor, which contains a high level of biodiversity (Dolch et al. 2004; Peck 2004; Wright et al. 2008). The lemur community of Torotorofotsy forest is believed to be intact and contains the following species: Varecia variegata, Indri indri, Propithecus diadema, Hapalemur griseus, Prolemur simus, Eulemur rubriventer,

Eulemur fulvus, Daubentonia madagascariensis, Cheirogaleus major, Cheirogaleus crossleyi, Microcebus lehilahytsara, Lepilemur mustelinus, Avahi laniger, and Allocebus trichotis (Figure 1.5)

Aye-ayes have been studied at Torotorofotsy since approximately 2008 (pers. comm. Edward Louis). It is believed that the forest contains three aye-ayes: one adult male, one adult female and one subadult male. These three individuals are outfitted with radio-collars as part of Madagascar Biodiversity Partnership’s aye-aye research project.

The female, Tsinjo, has been collared since March 2008, with a three-year hiatus (from

2009-2012) during which the collar’s battery became non-functional. The adult male,

Masy, has been collared since January 2012 and the subadult male, Cobalt, since August

2016.

The data presented in this dissertation were collected over a period between

January 2016 and December 2017. Data pertaining to feeding and ranging were collected from January 2016 to December 2017. Data related to infant development were collected from September 2016-December 2017, following Cobalt’s birth in March 2016. Data related to positional behavior were collected between May 2017 and December 2017.

In addition to data I collected, four Malagasy researchers collected data on feeding, ranging and infant development. Two other Malagasy researchers collected data on positional behavior. I conducted a tests of inter-observer reliability to determine the percent of agreement between researchers using the weighted occurrence agreement formula, where C% is the percentage of agreement, A is the number of agreed observations and B is the number of differences in observation (House et al. 1981):

A C%= x100 A+B

The test indicated a 90% agreement rate for the feeding, ranging and development data sets and 93.5% agreement rate for the positional behavior data set. Both of these rates are considered high and I am confident that all members of the project were collecting data in a reliable and consistent manner (House et al. 1981).

Figure 1.1 The clawed, elongated digits, large, bat-like ears and metacarpophalangeal joint in the 3rd digit of an aye-aye. Photo by author.

Figure 1.2 Various sized larvae removed from a piece of deadwood in Torotorofotsy, Madagascar. Photo by author.

Figure 1.3 Location of Torotorofotsy on the island of Madagascar.

B C

Figure 1.4 Part A, B and C The forest at Torotorofotsy, Madagascar. Photos by author.

Figure 1.5 Images of various lemurs in Torotorofotsy. From top left to bottom right: Lepilemur, Indri, Cheirogaleus, Microcebus, Eulemur, Daubentonia, Avahi, Propithecus. All photos by author.

Chapter 2 Dietary profile, seasonal resource use, substrate use and food preference of an adult aye-aye (Daubentonia madagascariensis) in Torotorofotsy, Madagascar

In this chapter, I present feeding data on the female aye-aye, Tsinjo, collected over a period of 24 months. I also present abundance data on the three most commonly referenced resources consumed by aye-ayes, Canarium sp. seeds, Ravenala madagascariensis nectar and invertebrates. Additionally, I present data on Tsinjo’s substrate use, i.e. foraging for invertebrates on live trees, deadwood and bamboo. These data are used to establish the first dietary profile of a free-ranging aye-aye in a undisturbed forest, test whether diet fluctuates seasonally and annually, examine whether aye-ayes have preferred and/or fallback foods, and evaluate the dynamics of insectivory in a primate whose body size exceeds the threshold (Kay 1975) of what a predominantly insectivorous organism should be.

Introduction

An aye-aye (Daubentonia madagascariensis) is a non-sexually dimorphic, medium-sized primate (2.6kg) with dark brown or black fur and a tail that is longer than its body (Owen 1863; Martin 1990). Aye-ayes are the most morphologically specialized primates, with continuously growing incisors, a dental formula of 1.0.1.3/1.0.0.3, elongated, clawed digits, a nictitating membrane, large, bat-like ears and a ball-and- socket 3rd digit metacarpophalangeal joint (Owen 1863; Jouffroy 1975; Cartmill 1979;

Martin 1990; Simons 1995). These features are used to echolocate and extract larvae from live trees, deadwood and bamboo, a feeding behavior known as percussive foraging

(Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991; Sterling 1993, 1994; Erickson et al. 1998; Dominy et al. 2001; Soligo 2005). Because of their unusual morphology and behavior, aye-ayes were initially identified as predominantly insectivorous (Petter 1962,

1977). In his influential study on diet and body size, Kay (1975) established a predictive relationship between body mass and insectivory, arguing that a primate weighing more than 500g could not sustain itself on invertebrates because the energy gained from an average insect was not sufficient to offset the cost of acquiring an insect of average size, which is typically small (Kay 1975). Aye-ayes were mentioned specifically as being too large to be exclusively invertebrate predators, leading Kay and others to speculate that aye-ayes were supplementing their insectivorous diet with other resources (Kay 1975;

Iwano and Iwakawa 1988).

The first study to demonstrate that aye-ayes were, perhaps, not strictly insectivorous was that of Iwano and Iwakawa (1988). These authors established that the aye-ayes under observation were primarily granivorous, consuming large quantities of endosperm from Canarium seeds (Figure 2.1a and 2.1b; Iwano and Iwakawa 1988).

These authors also mentioned that their study animals did consume invertebrates; however, no food intake percentages were reported and their discussion focused primarily on the consumption of Canarium seeds (Iwano and Iwakawa 1988). A second study identified Ravenala madagascariensis nectar (Figure 2.2) as the preferred resource

(Ancrenaz et al. 1994). Here too invertebrates were discussed as having been consumed, but they were not identified as the most frequently consumed food item (Ancrenaz et al.

1994). A third study established that in addition to Canarium seeds, invertebrates and

Ravenala nectar, aye-ayes consume cankers and fungus growing on trees (Sterling 1993;

1994a). This latter study concluded that aye-ayes focused their feeding on structurally defended resources, specifically Canarium seeds and invertebrates, particularly those found in deadwood (Sterling 1993, 1994a). Authors of all these studies witnessed aye- ayes consuming invertebrates; however, these authors also noted that when other foods became available, larvae were bypassed (Iwano and Iwakawa 1988; Iwano 1991; Sterling

1993, 1994; Ancrenaz et al. 1994). This leads to the possibility that aye-ayes are not obligate insectivores.

There are reasons to interpret conclusions from the above studies cautiously. Two of the studies (Iwano and Iwakawa 1988; Sterling 1993, 1994) were conducted on the island of Nosy Mangabe where aye-ayes had been introduced. Aye-ayes on Nosy

Mangabe are not naturally occurring, have no predators, and therefore may be under different selective pressures from those in naturally occurring populations on the main island of Madagascar. The third study (Ancrenaz et al. 1994) was conducted in the heavily disturbed forest in Mananara-Nord Biosphere Reserve. This forest is located adjacent to coconut plantations which aye-ayes are known to raid frequently (Ancrenaz et al. 1994). The relevance of these data for understanding the foraging ecology of natural populations is therefore questionable.

Dietary Switching

Understanding the degree to which aye-ayes utilize invertebrates in their natural habitat is important for determining (a) whether their body size indeed constrains invertebrate consumption (Kay 1975) or, alternatively, (b) if aye-ayes overcome the constraints of body size with specialized morphological and foraging adaptations (Gaulin

1979). In addition, observing aye-ayes in their natural habitat provides for a more

22 accurate assessment of how invertebrate consumption fluctuates relative to the acquisition of other resources. Most primates practice some degree of dietary switching as food availability fluctuates with seasonal changes (Lambert 2002, 2007, 2010).

Sometimes primates will shift between different foods of the same resource type. For instance, Diana monkeys (Cercopithecus diana) will eat different types of ripe fruit as seasons change and availability fluctuates (Kane 2012). Many other primates will switch the type of resource they consume (Lambert 2002; Hemingway and Byman 2005). For example, King colobus monkeys (Colobus polykomos) switch between seeds, young leaves and mature leaves at different times of the year (Dasilva 1994). In order for primates to switch between resources, their feeding morphology (i.e. dental or digestive adaptations) must not limit their ability to process multiple food types.

Ranging and Diet

Primates that practice dietary switching are likely to require large home ranges in order to locate sufficient resources (Lambert 2002, 2007, 2010). This is because, on average multiple food types are likely to be distributed across a wider range of a given habitat. For example, orangutans (Pongo abelii; Pongo pygmaeus) are classic dietary switchers, consuming ripe fruit when available, but switching to leaves and bark during non-fruiting seasons (Kanamori et al. 2010). In order to accommodate this diversity of food and the energetic requirements of their large body size, orangutans have enormous home ranges which average approximately 850 ha for females and 2500 ha for males

(Singleton and van Schaik 2001). Such large home ranges allow orangutans to find enough resources to sustain themselves. Lemurs also practice dietary switching, likely because of the extensive periods of drought and unpredictable seasonality of Madagascar

(Hemingway 1998; Powzyk and Mowry 2003; Schmid and Kappeler 2005). For example, Verreaux’s sifakas (Propithecus verreauxi) will increase their home range when fruit and flower availability peaks (Richard 1977). Given Madagascar’s extreme seasonality and concomitant fluctuations in resource availability, it is reasonable to predict that aye-ayes will also demonstrate some degree of dietary switching throughout the year, and that their ranging behavior is interpretable, in part, because of this dietary strategy.

Categorizing Diet

It is common for primates to consume multiple food types, though most species tend to favor some types over others because of factors which include nutritional elements, abundance, ease of access, temporal and spatial availability (Milton and May

1976; Clutton-Brock 1977; Chivers and Hladik 1980; Harvey and Clutton-Brock 1981;

Garber 1987). Favored resources typically are considered more valuable because they are highly nutritious and easy to process. Researchers have developed several systems to describe the differential consumption of foods with different values, i.e. those that are favored over others. One such classification uses the terms preferred and fallback

(Marshall and Wrangham 2007). A preferred resource should be one consumed more often, or favored, than any other resource in the environment, even when other resources are more prevalent (Emlen 1966; Johnson 1980; Stephens and Krebs 1986). This is because preferred resources are valuable: typically, they are nutritious and easily accessible. For example, orangutans (Pongo pygmaeus) consume ripe fruit preferentially even during periods when ripe fruit is scarce. During those periods of the year when ripe fruit is most abundant, ripe fruit is consumed to the exclusion of all other resources

(Leighton 1993; Knott 1998). In contrast, fallback foods are those an organism can “fall back on” when preferred foods cannot be consumed because they are in short supply or are absent.

Foods in the fallback category are typically characterized by a number of properties. First, they usually have mechanical properties that prevent many organisms from efficiently processing them (Kinzey and Norconk 1990; Lambert 2007; Marshall and Wrangham 2007; Marshall et al. 2009). For example, many resources in tropical rainforests are too tough, too hard, or both, for many consumers to process (Coley and

Barone 1996; Janson and Chapman 1999). Fallback foods also tend to be more abundant both spatially and temporally. One of the reasons contributing to their increased availability is the fact that fewer organisms are able to process them. Given the fact that highly valued, or preferred, foods are prone to more seasonal fluctuations, the majority of an organism’s diet will usually consist of fallback foods when preferred foods are not available (Kinzey and Norconk 1990; Lambert 2007; Marshall and Wrangham 2007;

Marshall et al. 2009). An example of a primate falling back is the ring-tailed lemur

(Lemur catta) at Beza Mahafaly Special Reserve (Sauther and Cuozzo 2009). These lemurs preferentially consume ripe fruits whenever they are available (Sauther and

Cuozzo 2009). When ripe fruit is absent, ring-tailed lemurs fallback on Tamarindus indica fruit which have a tough, protective casing that causes significant dental wear

(Sauther and Cuozzo 2009). Unlike ripe fruit, T. indica fruits are available throughout the year but are only consumed in the absence of preferred ripe fruit, which tend to be easily processed (Sauther and Cuozzo 2009). Whenever preferred ripe fruit is available, it is always selected, i.e. preferred, over T. indica (Sauther and Cuozzo 2009).

Demonstrating preference is not as straightforward as simply identifying the most frequently consumed food. This is because, in order to demonstrate preference, it is necessary to have an independent assessment of availability. For example, if a food is consumed while no other options are available, it is quite possible that the most frequently consumed food is not preferred: the organism in question simply has no choice in what it eats. Therefore, any attempt to demonstrate preference or fallback requires an independent assessment of food types across the habitat.

Complicating the preferred/fallback food paradigm is the nature of primate feeding adaptations. It is well established that elements of diet have selected for multiple aspects of primate morphology (Temerin and Cant 1983). For example, folivorous diets are typically associated with high molar shearing crests to allow for better processing of tough leaves (Kay 1975; Kay et al. 1978). Suspensory locomotion is associated with frugivory and is argued to have evolved to allow primates to (a) maximize their straight- line paths between fruit patches and (b) essentially double their foraging sphere by allowing them to reach food below branches (Temerin and Cant 1983). Longer digestive tracts and associated long transit times allow folivorous primates to more readily break down structural carbohydrates common in lower quality foods such as mature leaves

(Milton 1981). Several authors have attempted to explain different elements of primate morphology as having been selected for by preferred and fallback foods respectively.

Some authors contend that preferred foods select for harvesting adaptations. Harvesting adaptations are those that are used in the detection, location and acquisition of foods prior to ingestion (Marshall and Wrangham 2007; Harrison and Marshall 2011; Rosenberg

2013). These include sensory, cognitive, and positional behaviors (Marshall and

Wrangham 2007; Harrison and Marshall 2011; Rosenberg 2013). For example, callitrichids have secondarily re-evolved claws that allow them to cling to large vertical trunks and access their preferred resource, tree sap (Garber 1980). As noted above, it has been argued that the forelimb dominant locomotion of hominoids, i.e. brachiation, evolved in response to the pursuit and acquisition of ripe fruit on the ends of terminal branches (Temerin and Cant 1983). Multiple studies have shown that forelimb suspension is used most frequently during travel between high quality fruit patches and during foraging within those patches themselves (Fleagle 1976; Mittermeier 1978; Cant

1986).

In contrast to harvesting adaptations, processing adaptations are those that are used during ingestion, mastication and digestion (Marshall and Wrangham 2007;

Harrison and Marshall 2011; Rosenberg 2013). All primates have adaptations for processing food, but some processing adaptations are clearly evolved for the comminution of resources with material properties that make breakdown of a resource particularly challenging. Adaptions in this category are suggested to provide a selective advantage related to the consumption of fallback resources when such resources are characterized by challenging material properties (Marshall and Wrangham 2007;

Harrison and Marshall 2011; Rosenberg 2013). For example, the ripe fruit preferentially consumed by orangutans tends to be soft and easily masticated; specialized molar adaptations, such as thick enamel, are not required to consume these preferred foods

(Vogel et al. 2008; Constantino et al. 2009). However, when ripe fruit is unavailable, orangutans will consume hard seeds, unripe fruit and bark, which are much more challenging to process. It has therefore been argued that the tendency for orangutans to

27 fall back on hard seeds, unripe fruit and bark selected for their thick enamel (Vogel et al.

2008; Constantino et al. 2009). The characteristic thick enamel of orangutans may have been selected to facilitate processing of foods consumed only during short periods of the year when preferred foods are unavailable, i.e. during fallback periods.

It is therefore apparent that certain primates have anatomical configurations which allow them to harvest and process foods otherwise considered low quality because they are structurally defended, mechanically challenging, and/or difficult to process. Primates with such adaptations have an advantage because the foods they can consume are typically spatially and temporally ubiquitous in part because most other organisms find them difficult to process and therefore ignore them. Such primates should therefore not be as susceptible to fluctuations in food availability.

Adaptations that allow an organism to consume resources that others cannot provide a great selective advantage because (1) more food is available and (2) competition for that food is lower because most other organisms lack the necessary processing and digestive adaptations to break these foods down (Wrangham 1980; Isbell

1991). For example, a majority of fungi that grow on trees and fallen logs is, for most neotropical primates, very difficult to orally process and digest. However, Goeldi’s monkeys (Callimico goeldii) have high molar shearing crests which facilitate the fracture of cell walls and an elongated hindgut which allows for increased fermentation and improved nutrient absorption (Porter et al. 2009). Therefore, fungus, which is inaccessible to most other sympatric mammals, is the preferred resource of Goeldi’s monkeys (Porter et al. 2009). Similarly, eastern black and white colobus monkeys

(Colobus guereza) have a folivorous diet that consists mainly of young and mature leaves

(Oates 1977; Oates et al. 1977; Chapman and Pavelka 2005; Harris and Chapman 2007).

Foliage is a difficult resource for most primates to digest because it is tough and contains high quantities of tannins and alkaloids (Oates et al. 1977). However, the eastern black and white colobus preferentially consumes this resource. This is possible because the high molar shearing crests of black and white colobus effectively fracture the cell walls within these tough leaves (Kay 1975). In addition, the ruminant stomach and elongated digestive tract of black and white colobus improve nutrient absorption and neutralize the chemical properties of mature leaves (Ohwaki et al. 1974; Kay et al. 1976).

Interpreting whether a feature has been selected in response to a fallback or preferred feeding is not necessarily straightforward. Lambert et al. (2004) compared the diets and food material properties of grey-cheeked mangabeys (Lophocebus albigena) and red-tailed monkeys (Cercopithecus ascanius) in Uganda’s Kibale Forest. They determined that, with the exception of a five-month period, the average dietary hardness of the two monkey species did not differ. During the period when preferred, ripe fruit was not available, the grey-cheeked mangabey consumed hard seeds and bark, which were interpreted as their fallback foods (Lambert et al. 2004). Grey-cheeked mangabeys, like all mangabeys (McGraw et al. 2012), have very thick enamel and Lambert et al.

(2004) concluded that thick enamel evolved in response to falling back on hard, low- quality foods. Sooty mangabeys (Cercocebus atys) also have thick enamel and consume hard Sacoglottis gabonesis seeds throughout the year (McGraw et al. 2014). In this scenario, hard foods are preferred and the evolution of thick enamel is plausibly explained as a response to preferred hard object feeding rather than fallback hard object feeding (McGraw et al. 2014). In both instances, it was necessary to collect information

29 on the organism’s diet and resource abundance in order to categorize foods as either preferred, fallback or other (Cock 1978; Stephens and Krebs 1986; Leighton 1993).

Previous Work on Aye-aye Feeding Ecology

There have been two attempts to collect dietary information on aye-ayes for a full annual cycle (Sterling 1993, 1994; Randimbiharinirina et al. 2018). In both cases, dietary profiles were generated; however, resource abundance data were not. Furthermore, both studies cannot be considered representative of free-ranging populations under natural conditions: the first focused on a population of non-native individuals (Sterling 1993,

1994), while the second occurred in a highly-disturbed forest (Randimbiharinirina et al.

2018). Any attempt to draw conclusions about the relationship between diet and morphology from these studies should be done with caution.

Based on existing data, the diet of aye-ayes is believed to consist of large quantities of invertebrates, both in the larval and adult stage. Wood-boring beetle larvae appear to be the invertebrate most often consumed by aye-ayes (Petter 1977; Sterling

1993, 1994a; Randimbiharinirina et al. 2018). It is therefore critical that we understand the distribution, abundance and life cycle of wood-boring beetles. Adult beetles, which consume fruit, leaves, sap and soft bark on saplings, are solitary (i.e. non-social) and tend to be dispersed evenly but widely throughout the environment (Hanks 1999). Different species of beetles use different host trees to deposit their eggs beneath the bark (Hanks

1999). Beetles can oviposit anywhere between one and ten eggs per deposition site within a host (Hanks 1999). Hosts can be healthy, weakened, stressed or dead trees

(Hanks 1999). Eggs can be deposited singularly or in groups and they can be clumped within a substrate or evenly distributed throughout the environment (Isbell 1991; Sterling

1993, 1994a). The larvae that eventually hatch within a host feed on the subcortical tree layers: inner bark, cambium and young xylem, sapwood, heartwood and pith (Hanks

1999). Therefore, to the aye-aye, larvae within a tree are a structurally defended resource because they are protected by the woody covering of live trees, deadwood and bamboo

(Sterling 1993, 1994a).

Available literature suggests that although larval consumption by aye-ayes occurs throughout the year, it varies seasonally (Sterling 1993, 1994a). Sterling and McCreless

(2006: 164) claimed aye-ayes on Nosy Mangabe do not preferentially consume insects but rather use them when other resources, more specifically Canarium and Ravenala, are scarce. This conclusion suggests that invertebrates are a fallback food because they are a stable, ubiquitous resource. If true, this would suggest that the specialized aye-aye feeding morphology evolved in response to consumption of non-preferred or fallback foods. Complicating this interpretation is the realization that invertebrates are high in lipids and proteins, making them a high-energy food item (Sterling 1993, 1994a). These are characteristics not associated with typical fallback foods (Marshall and Wrangham

2007). I suspect that the feeding data from Nosy Mangabe do not accurately reflect aye- aye feeding behavior under natural conditions: the aye-ayes studied by Sterling (1993,

1994a) were an introduced population subject to different ecological pressures than those on the mainland. Therefore, questions about the significance of invertebrates in the aye- aye diet remain, and the characterization of invertebrates as preferred or fallback foods has yet to be properly addressed.

Despite possessing a suite of adaptations clearly designed for the extraction of larvae from woody substrates (see Chapter 1), it is still not known the extent to which

31 aye-ayes rely on an insectivorous diet across a full annual cycle under natural conditions.

Without these baseline data, our ability to relate diet to morphology, even in the most specialized of all primates, is compromised. Determining the feeding repertoire of the aye-aye is the first step towards reconciling the relationship between the aye-aye’s body size, anatomical specializations and foraging behavior.

This Study

I collected feeding data on an aye-aye (Figure 2.3) in a continuous rainforest over a two-year period. These data provide the first feeding profile of a free-ranging individual across at least one annual cycle in a natural habitat. To date, no study has been conducted on the feeding behavior of naturally occurring aye-ayes in a undisturbed forest. Therefore, my goals were to (1) develop a complete aye-aye dietary profile, (2) compare the monthly, seasonal and annual consumption of resources, and (3) evaluate preference for the various resources consumed. I do this by comparing resources consumed each month, season and year with the availability of potential foods each month, each season and each year. My null hypothesis is that there will be no difference in the monthly, seasonal and annual frequencies of resources consumed by aye-ayes in a undisturbed forest. Given that invertebrates are a high-energy resource (Sterling 1993,

1994a), and that aye-aye are adapted for sensory perception and extraction of this resource, my alternative hypothesis is that aye-ayes will consume invertebrates more frequently than any other resource. I predicted:

1) Invertebrates will be the most frequently consumed resource each month, each season

and each year.

2) Invertebrates will be the preferred resource of aye-ayes each month, each season and

each year.

3) Aye-ayes will supplement their diet with different food items throughout the year, but

never in excess of or to the exclusion of invertebrates.

Methods

Field site

I conducted this research from January 2016 to December 2017 in Torotorofotsy

(18o52’S, 42o22’E), Madagascar. Torotorofotsy is a natural wetland about 1100 ha in size, adjacent to Mantadia National Park and approximately 10 km northwest of the town

Andasibe. It is the most intact wetland in the Andasibe-Mantadia-Zahamena eastern rainforest corridor, containing high levels of biodiversity (Dolch et al. 2004; Peck 2004;

Wright et al. 2008). Within Torotorofotsy there are three collared aye-ayes: one adult male, one adult female and one subadult male. These aye-ayes are outfitted with radio- collars as part of Madagascar Biodiversity Partnership’s aye-aye research project

(Sefczek et al. 2017). Because the male aye-aye ranged beyond the boundaries of

Torotorofotsy into territories I did not have permission to enter, this research focuses on the feeding behaviors of the adult female, Tsinjo.

Madagascar has three seasons distinguished on the basis of mean daily temperature and total monthly rainfall (Sterling 1993). The hot/rainy season extends between January and mid-May and is considered season 1. The cold/rainy season extends from mid-May to mid-September and is considered season 2. The hot/dry season extends from mid-September to the end of December and is considered season 3.

(Sterling 1993; Wright 1999; Vasey 2005). These three seasonal designations were used to examine the effects of seasonality on aye-aye feeding behavior and food abundance.

Behavioral Data Collection

In order to collect sustained dietary and foraging data, I conducted six-hour follows, from 18:00-0:00 on Mondays and Wednesdays and from 0:00-6:00 on Tuesdays and Thursdays. Monday and Wednesday follows started when Tsinjo exited her sleeping site. During Tuesday and Thursday follows, I located the focal animal using the radio telemetry system. Follows ended when Tsinjo reached her nest and did not move for an hour. I used the methodology outlined by Sterling (1993) with three researchers, myself and two Malagasy field assistants, following a focal animal. One researcher maintained light contact, defined as keeping the aye-aye within the beam from a head lamp but not closer than five meters. The other two participants positioned themselves in order to follow the animal when it ventured in a new direction (Sterling 1993).

During night follows, I collected data using the continuous focal-animal sampling technique (Altmann 1974). That is, I recorded all elements of feeding behavior from the time a feeding bout commenced until a) feeding stopped, b) visibility became obstructed, or c) Tsinjo locomoted out of sight. I adopted the feeding categories of Sterling (1993,

1994a) to describe the dietary inventory: fruit, flower, leaves, seeds, invertebrates, fungus. Whenever feeding behavior was observed, I recorded the following: 1) resource category consumed, 2) quantity of each resource consumed (see below), 3) duration of feeding bout, defined as the time between the commencement of feeding and when she stopped or visibility became compromised, 4) height, estimated in meters, at which feeding occurred, and, when applicable, 5) the substrate used for invertebrate feeding

(bamboo, deadwood, or species of live tree).

Feeding quantity was assessed the following ways:

1) Invertebrate quantity was based on number of new traces created in a substrate with

each new trace equaling one invertebrate. A trace is the hole made by an aye-aye in a

woody substrate for the purpose of accessing an invertebrate. Whenever I witnessed

Tsinjo create a new trace, I recorded one larvae consumed. It is impossible to

determine how many larvae were extracted from a single trace, so we opted for a

conservative approach and tallied one larvae per trace. Therefore, a 1:1 ratio of new

traces made and larvae removed was assumed as a way to estimate larval

consumption.

2) The number of fruits consumed was assessed by counting the number of fruits being

orally processed or from auditory cues which typically consisted of a seed being

dropped. When processing Canarium fruits, the aye-aye will typically grab one fruit,

carry it to a perch spot on a branch, hold it in both hands and gnaw through the fruit

and into the seed contained within. They will then remove a small portion of the

exocarp and extract the endosperm from inside the seed (Iwano and Iwakawa 1988;

Sterling 1993, 1994a). Once the endosperm is removed, the aye-aye will drop the

food and go back for another fruit.

These data were used to build monthly, seasonal and annual dietary profiles. Monthly

feeding profiles were calculated by summing the total number of food items consumed or

traces created that month during observational periods. The number of nights per month

during which observational periods occurred varied between three and thirteen over the

course of the study period. No attempt was made to adjust monthly, seasonal or annual

feeding profiles based on the number of observational periods; however, it is possible that

monthly, seasonal and annual dietary profiles could have differed with additional

35 observations. Seasonal profiles were compiled by adding the results of monthly or half- monthly (15th of each month) profiles. Three seasons (1: hot/rainy, 2: cold/rainy, 3: hot/dry) each of which contained approximately four months. Annual dietary profiles simply consisted of the data collected over the course of each year. These profiles were then examined within the context of phenological data and data on the relative distribution of resources in the habitat.

Phenological Data Collection

Previous studies have shown that parts of two native trees are critical resources for aye-ayes. Canarium seeds extracted from fruits on trees and Canarium seeds collected from the forest floor are referenced in several studies (Iwano and Iwakawa

1988; Sterling 1993, 1994a; Randimbiharinirina et al. 2018). The nectar collected from the mature flowers of Ravenala madagascariensis are also mentioned in numerous studies as being a particularly significant resource for aye-ayes (Ancrenaz et al. 1994;

Sterling 1993, 1994a; Randimbiharinirina et al. 2018). I attempted to establish an independent measure of abundance of these two resources within Tsinjo’s home range in

Torotorofotsy. Every month, I recorded (1) the abundance of ripe and unripe fruit on all

Canarium trees (2) the number of Canarium seed on the forest floor and (3) the availability of Ravenala madagascariensis flowers within Tsinjo’s home range at

Torotorofotsy. I collected these data along twenty transects (Figure 2.4) that I had established in 2015 as part of a pilot study. Each transect was 10m x 100m (0.1 ha) with starting locations determined using a stratified random sampling technique. I scored flowers on Ravenala trees using a scale of 1-3 (1=absent, 2=mature flowers, 3=old flowers; Sterling 1993) and I estimated abundance of mature Ravenala flowers (i.e. those

36 likely to contain nectar) within Torotorofotsy by counting the number of mature flowers per tree along the transects and then multiplying the area covered by all transects (2 ha) within the entire habitat (1100 ha; Tepedino and Stanton 1982). Although data are not available to determine whether nectar is present in older (past their prime) flowers, I adopted a conservative approach and assumed that nectar was present only in healthy- looking flowers that showed no evidence of withering.

I scored fruit availability on Canarium trees using a scale of 1-3 (1=absent,

2=unripe, 3=ripe; Sterling 1993) and estimated fruit abundance by counting the number of fruits in approximately one quarter of the tree crown, multiplying that number by four, calculating the number along the entire transect and then multiplying that to estimate ripe

Canarium fruit availability for the entire Torotorofotsy forest (Ganzhorn et al. 2011).

Because aye-ayes have been known to forage for Canarium seeds on the forest floor

(Sterling 1993), I recorded seed presence and abundance on the ground. At every

Canarium tree I scored seed presence as 0 (absent or used) or 1 (present and unused). I estimated seed availability by counting seeds in one quarter of the forest floor directly beneath the tree canopy and multiplying that number by four to approximate the number of seeds on the forest floor under the canopy (Ganzhorn et al. 2011). For each transect, the number of seeds on the forest floor was determined by summing all seed counts. I then took these totals from each transect and, using the size of Torotorofotsy forest, extrapolated from the area sampled by the transects to determine the total number of seeds within the entire habitat (Ganzhorn et al. 2011). This information was used to determine the availability of Ravenala flowers containing nectar and Canarium fruits and seeds every month.

Invertebrate Abundance Estimation

Insect larvae are a cryptic resource found in a variety of substrates, including live trees, deadwood and bamboo (Sterling 1993). As discussed by Sefczek et al. (2017), aye- ayes in undisturbed forests utilize live trees for invertebrate foraging more than deadwood. While it is possible to sample invertebrate availability in all substrates potentially bearing invertebrates, this sampling procedure would require destruction of the substrate and removal of a potential food thereby possibly disrupting aye-aye foraging

(Sterling 1993; Sefczek et al. 2017). Fortunately, invasive sampling techniques involving destruction of substrates are not required to estimate invertebrate larvae abundance.

Conner et al. (1994) found that arthropod biomass significantly correlates with foraging traces of woodpeckers, another predator of wood-burrowing insects. Since aye-ayes, like woodpeckers, leave distinctive feeding traces on substrates during invertebrate foraging, it is possible to estimate invertebrate availability by assessing the frequency of new traces along transects (Figures 2.5a and 2.5b, 2.6, 2.7; Farris et al. 2011; Sefczek et al. 2012).

New traces are defined as those that have been sampled with a month of the feeding event. They are easily distinguished from older traces because of changes that occur to the bark and underlying phloem following the gnawing event (Farris et al. 2011; Sefczek et al. 2012). When the bark is removed and the phloem is exposed, it typically remains a lighter color for approximately four weeks. After approximately four weeks, traces begin to show signs of decay, the edges of the exposed bark become less sharp, and the coloration becomes dulled and darkened (Figure 2.8). Additionally, new traces may have the presence of wood shavings from where the aye-aye gnawed into the substrate.

I determined invertebrate abundance using two methods. First, assuming a 1:1 relationship between the number of new feeding traces and the number of larvae 38 consumed, I counted the number of new traces on all 20 transects (2ha) each month and used these totals to approximate the number of invertebrates across the entire habitat

(1100ha). One of the limitations of transect sampling is the possibility that events, particularly rare ones, may be missed (Rushton et al. 2004; Guisan et al. 2006). For example, there were some months when no new traces were encountered on any of the transects despite the fact that we knew Tsinjo was foraging for invertebrates. I therefore also used the frequency of trace manufacturing collected during focal follows (many of which did not occur on the transects) to estimate the frequency of new traces, and thus invertebrates, throughout the entire forest. During each observation follow, I counted the number of traces the focal animal made. I also recorded the GPS location of the animal every 15 minutes. I therefore also used the GPS points to estimate the area of forest used that month. I combined the total number of traces with information on monthly forest use to determine the total number of new traces and, thus, total number of available invertebrates across the entire 1100 ha forest. The estimates of invertebrate availability generated by these two methods were compared for each month and whichever produced the greater quantity was used to calculate preference.

Data Analysis

All statistical tests for this research were performed in R. A Shapiro-Wilk test of normality (α=0.05) showed that data for (1) quantities of resources consumed each month

(W=0.727, df=71, p<0.001) and (2) substrates from which invertebrates were consumed monthly (W=0.820, df=71, p<0.001) were not normally distributed. Data on food availability collected along transects are presented for every month, season and year of the study. Significant differences between months were assessed using a G-test of

39 goodness-of-fit with an expected 1:1 ratio between months, and significant differences between seasons and years were assessed using a negative binomial regression analysis

(α=0.05) or a zero-inflated binomial regression analysis (α=0.05) when there were multiple zero values (March 2016, March 2017, May 2017 and June 2017). I compared the consumption of resources and use of substrates for invertebrate feeding within each month, season and year using negative binomial regression analyses (α=0.05). I executed negative binomial regressions (α=0.05) to examine (A) how quantities of resources consumed changes between months, seasons and years and (B) how quantities of invertebrates removed from the three substrates changes between months, seasons and years. I performed a negative binomial regression analysis (α=0.05) to compare resources consumed and use of substrates for invertebrate feeding by Tsinjo over the course of the entire study.

Canarium seeds and invertebrates constituted approximately 99% of the total diet across the course of the study. A two-item preference index was therefore calculated using the following formula (Cock 1978):

Ne/Ne` Index = N/N`

In this formula, Ne is the number of Canarium seeds consumed, Ne` is the number of invertebrates eaten, N is the total number of Canarium seeds available and N` is the total number of invertebrates available. With this formula, a value between 0-1 indicates a negative preference for Canarium seeds, while a value of 1 or greater indicates a positive preference for Canarium seeds (Cock 1978). I did not calculate preference for Ravenala

40 and Vakona because their use was negligible. I also excluded months when invertebrates were the only resource used.

Results

I followed Tsinjo for a total of 153 nights, averaging 2h 42min per follow (range:

15 min-6 hours; σ=75 min). On average, follows were shorter than six hours. The lengthiest follows, typically commencing at 18:00, were those that began with the focal subject still in her nest. On the nights when she had already left her nest, sampling was shorter because I had to spend considerable time searching for her. The aye-aye day typically finishes between 03:00 and 04:00, when the animal selects that day’s sleeping tree. In addition, the aye-aye’s tendency to forage and travel in a cryptic manner, often high in the canopy or in other areas with poor visibility, contributed to short average night follows.

Food Abundance

In this section, I present data on the availability of each food type assessed (1) monthly, (2) seasonally and (3) annually. I walked the twenty 100m x 10m transects every month for a period of twenty-four months. Over the course of the sampling period,

I recorded a total of 443 new invertebrate feeding traces (Table 2.1). Over the course of the sampling period, I recorded a total of 93,400 ripe Canarium fruits. Over the course of the sampling period, I recorded a total of 26,420 Canarium seeds on the forest floor.

Lastly, over the course of the sampling period, I recorded a total of 498 mature Ravenala flowers.

Table 2.2 presents the results of the G-test of goodness-of-fit which tests for differences in availability of each resource between months. The tests indicated that 41 there were multiple significant differences in monthly availability of ripe Canarium fruits, invertebrates, Canarium seeds and mature Ravenala flowers. There are too many permutations to discuss each in full, however a number of generalizations can be made.

In 2016, ripe Canarium fruit was available only between January and July, whereas the following year, ripe Canarium fruit was available between February and November. The monthly differences in Canarium availability between 2016 and 2017 would result in multiple significant values of the G-test. In 2016, invertebrates, as determined by new traces along the transects, were present each month of the year. However, in 2017, invertebrates, as determined by new traces along the transects, were only present between

March and November.

Table 2.3 presents monthly food availability data (from Table 2.1) grouped into three annual seasons: hot/rainy (season 1), cold/rainy (season 2) and hot/dry (season 3).

Results of the negative binomial regression analyses, which test for seasonal differences in resource availability, are present in Table 2.4. The tests indicated that there were significant differences in the availability of ripe Canarium fruits, invertebrates, Canarium seeds and mature Ravenala flowers in different seasons. In season 2 of 2016, there were significantly fewer ripe Canarium fruits (negative binomial regression: z=-119.6, df=7, p=0<0.001) and invertebrates (z=-5.211, df=7, p<0.001) than during season 1 of 2016.

There was no difference in Canarium seed abundance on the ground between season 1 and season 2 of 2016 (z=-0.014, df=7, p=0.989), but there were significantly less mature

Ravenala flowers in season 2 of 2016 (z=-2.165, df=7, p=0.030). In season 3 of 2016, there were significantly fewer (i.e. none) Canarium seed available (z=-2.880, df=7, p=0.028) compared to season 2 of 2016; however, there was an increase in the number of

42 invertebrates (z=2.703, df=7, p=0.006) and mature Ravenala flowers (z=5.640, df=7, p<0.001) during this same period. The number of ripe Canarium fruit increased significantly between season 3 of 2016 and season 1 of 2017 (z=-2.565, df=7, p=0.042) and between season 1 and season 2 of 2017 (z=12.12, df=7, p<0.001), but significantly decreased between season 2 and season 3 of 2017 (z=-75.35, df=7, p<0.001). The number of mature Ravenala flowers decreased significantly between season 1 and season

2 of 2017 (z=-2.997, df=7, p=0.002). There were also significant decreases in Canarium ripe fruit availability (z=-144.0, df=23, p<0.001), Canarium seed availability (z=-63.95, df=23, p<0.001) and mature Ravenala flowers (z=-6.101, df=23, p<0.001) from 2016 to

2017 (Table 2.5).

Overall Resource Use

Table 2.6 presents and Figure 2.9 depicts dietary information on Tsinjo for every month across the duration of the study. Based on the data collected, 99.6% of Tsinjo’s diet consisted of two resources: Canarium seeds extracted from ripe fruits and invertebrates. Invertebrates were consumed every month during the study, with monthly variation ranging between 9.8% and 100% of the diet. Canarium seeds were eaten during two five-month periods: every month between January and May 2016 and every month between February and June 2017. During these two periods, Canarium seeds within fruit usually composed the majority of the diet (between 67.7% and 90.2% of the diet), except for May 2017 (24.5%) and June 2017 (35.1%) when invertebrates were the most consumed resource (72.8% and 64.9%, respectively). In addition to these two foods,

Tsinjo consumed at least two other resources. In February 2016, she was observed drinking water from Ravenala madagascariensis (3.0% of the diet) and on four occasions

43 in May 2017 she was observed feeding on an unknown resource within a Vakona tree

(Pandanus utilis, Pandanaceae; Figure 2.10a and 2.10b). I speculate that the aye-aye was either feeding on invertebrates within Vakona palm fronds, or was feeding on fruits/seeds contained on top of the fronds. At no point did the use of Vakona or Ravenala trees exceed the use of invertebrates or Canarium seeds.

Resource Use Within Months

Appendix A displays the observed nightly consumption of each resource by

Tsinjo between January 2016 and December 2017. I tested to determine if diet composition (i.e., uniformity) varied within months. For example, does the number of invertebrates consumed within a given month significantly differ from the number of

Canarium seeds in ripe fruit eaten during that same month? Table 2.7 presents the significance values for the negative binomial regression analyses comparing diet composition within each month. During the eight months when Canarium seeds in ripe fruit and invertebrates were the only resources consumed, the negative binomial regression analyses and the zero-inflated negative binomial regression analyses indicated nine significant differences. Canarium seeds in ripe fruit were consumed in significantly greater quantities in January 2016 (z=10.60, df=9, p<0.001), February 2016 (z=8979, df=11, p<0.001), March 2016 (z=3.989, df=5, p<0.001), April 2016 (z=11.18, df=11, p<0.001), May 2016 (z=3.862, df=5, p<0.001), February 2017 (z=13.68, df=12, p<0.001), March 2017 (z=4.651, df=13, p<0.001), and April 2017 (z=9.425, df=5, p<0.001). In May of 2017 invertebrates were consumed in significantly greater amounts than Canarium seeds in ripe fruit (z=-2.022, df=25, p=0.043). During February 2017, when Canarium seeds in ripe fruit, invertebrates and water in Ravenala were all

44 consumed, the negative binomial regression analysis found that Ravenala was the least used resource (z=-3.037, df=11, p=0.002). Similarly, in May 2017, when Tsinjo consumed Canarium seeds in ripe fruit, invertebrates and unknown Vakona resources,

Vakona was consumed significantly less than the other two resources (z=-3.850, df=38, p<0.001).

Resource Use Between Months

Monthly feeding profiles are presented in Table 2.6. I used negative binomial regression analyses to examine how consumption of each resource changed from month to month. For example, I was interested in determining whether the number of invertebrates consumed in June differed from the number of invertebrates eaten in July.

Results of these tests are presented in Table 2.8 with significant differences indicated in bold. Results indicate that the amount of Canarium consumed by Tsinjo significantly decreased from January to February 2016 (z=-3.592, df=8, p<0.001), April to May 2016

(z=-4.435, df=8, p<0.001), February to March 2017 (z=-5.443, df=12, p<0.001) and May to June 2017 (z=2.644, df=16, p=0.008). Tsinjo significantly increased her consumption of Canarium seeds in ripe fruit from February to March 2016 (z=-2.463, df=11, p=0.013), March to April 2016 (z=4.41, df=13, p<0.001), January to February 2017 (z=-

2.827, df=8, p=0.004) and from March to April 2017 (z=3.532, df=9, p<0.001).

Significant differences in monthly invertebrate consumption occurred four times. Tsinjo significantly decreased her consumption of invertebrates from July to August 2016 (z=-

1.959, df=11, p=0.050), and November to December 2016 (z=-3.267, df=11, p=0.001).

She significantly increased her consumption of invertebrates from August to September

2016 (z=3.554, df=11, p<0.001) and from April to May 2017 (z=3.524, df=15, p<0.001).

At no point was the consumption of water from Ravenala or the unknown resource of

Vakona significantly different from the preceding or subsequent month.

Seasonal Resource Use

Madagascar has three seasons: the hot/rainy season (Season 1, January to mid-

May), the cold/rainy season (Season 2, mid-May to mid-September) and the hot/dry season (Season 3, mid-September to December; Sterling 1993; Wright 1999; Vasey

2005). The quantity of Canarium seeds in ripe fruit, invertebrates, unknown Vakona resource, and water from Ravenala madagascariensis consumed during each of these seasons are reported in Table 2.9 and depicted in Figure 2.11. Canarium seeds within fruit comprised more of the diet than invertebrates during the hot/rainy season (season 1) in both 2016 (79.9% and 19.6%, respectively) and 2017 (74.1% and 25.9%, respectively;

Figure 2.11). In the cold/rainy season (season 2) of 2016 and 2017, invertebrates composed more of the diet than any other resource (77.4% and 90.2%, respectively). In the hot/dry season (season 3), invertebrates constituted 100% of the diet in both 2016 and

2017.

Resource Use Within Seasons

Table 2.10 displays the results of the negative binomial regression analyses comparing resource consumption by Tsinjo within each season. Tsinjo consumed significantly greater quantities of Canarium seeds in ripe fruit than invertebrates during the hot/rainy season (season 1) of 2016 (negative binomial regression: z=2.639, df=71, p=0.008). Also during the hot/rainy season of 2016, water from Ravenala madagascariensis was consumed significantly less often than both invertebrates and

Canarium seeds in ripe fruit (z=-5.575, df=71, p<0.001). Though there was no

46 significant difference in resource consumption in season 2 of 2016, the greater quantity of invertebrates consumed compared to Canarium seeds in ripe fruit approached significance (p=0.062). It should be noted that there was only one record of Canarium feeding during that season which may affect the strength of the significance test. No tests were performed during season 3 of 2016 and 2017 because Tsinjo only consumed invertebrates. There was a significant difference in diet in seasons 1 and 2 of 2017.

There were significantly more Canarium seeds in ripe fruit consumed than invertebrates in the hot/rainy season (season 1) of 2017 (negative binomial regression: z=17.14, df=47, p<0.001). There were significantly less Canarium seeds in ripe fruit consumed than invertebrates in the cold/rainy season (season 2) of 2017 (z=-4.308, df=77, p<0.001).

There were also significantly less of the unknown Vakona consumed than either of the two resources during this same season (z=-6.361, df=77, p<0.001).

Resource Use Between Seasons

Seasonal fluctuations in Canarium fruit availability caused significant changes in the seasonal consumption rate of this resource by aye-ayes (Table 2.11). A significant decrease in Tsinjo’s consumption of Canarium seeds within fruit coincided with a change from the hot/rainy season (season 1) to cold/rainy season (season 2) in 2016 (negative binomial regression: z=-2.200, df=42, p=0.027) and in 2017 (z=-2.897, df=49, p=0.003).

Additionally, there was a significant increase in consumption of Canarium seeds in ripe fruit between the hot/dry season of 2016 (season 3), when fruit was unavailable, to the hot/rainy season of 2017 (season 1; z=-4.207, df=47, p<0.001). Tsinjo’s consumption of invertebrates increased significantly from the cold/rainy season (season 2) to the hot/dry season (season 3) of 2016 (z=4.419, df=42, p<0.001) and from the hot/rainy season

(season 1) to the cold/rainy season (season 2) of 2017 (z=2.461, df=49, p=0.013). There was also a significant decrease in invertebrate consumption between the hot/dry season

(season 3) of 2016 and the hot/rainy season (season 1) of 2017 (z=-4.193, df=47, p<0.001), which coincided with the increase in Canarium fruit availability and consumption. At no point were Tsinjo’s consumption of water in Ravenala or the unknown resource in Vakona significantly different between seasons.

Annual Resource Use

As seen in Table 2.6 and Figure 2.12, invertebrates formed the majority of the diet in both 2016 (58.3%) and 2017 (60.1%). Canarium seeds were the second most consumed resource in both 2016 (41.5%) and 2017 (39.4%). Ravenala was a small portion of feeding events in 2016 (0.2%), as was Vakona in 2017 (0.5%).

There was no significant difference in the amount of invertebrates and Canarium seeds within ripe fruit consumed by Tsinjo in either 2016 (negative binomial regression: z=-0.916, df=133, p=0.360) or 2017 (z=-1.246, df=153, p=0.213). When dietary profiles for 2016 and 2017 are compared, there was no significant difference between 2016 and

2017 in Tsinjo’s consumption of Canarium seeds in ripe fruit (negative binomial regression: z=-0.640, df=23, p=0.522) or her consumption of invertebrates (z=0.178, df=23, p=0.859; Table 2.12).

Diet Over the Course of the Study

An examination of the feeding data over the course of the entire study reveals that

Tsinjo consumed significantly greater quantities of invertebrates than Canarium seeds in ripe fruit (negative binomial regression: z=-13.79, df=47, p<0.001). Analyses were not run comparing the use of Ravenala madagascariensis for water or the unknown Vakona

48 resource because these resources were so rarely observed being used. Surprisingly,

Tsinjo was never observed feeding on the nectar of mature Ravenala flowers despite previous reports that this as an important resource (Sterling 1993, 1994; Ancrenaz et al.

1994).

Overall Substrate Use for Invertebrate Foraging

Table 2.13 presents and Figure 2.13 depicts the substrate use for invertebrate foraging by Tsinjo. Throughout the course of the study, I observed Tsinjo consuming invertebrates from three substrates: live trees, deadwood, and bamboo. Overall, live trees were the most commonly used substrate for invertebrate consumption (50.4%), followed by deadwood (39.1%) and bamboo (10.5%). Live tree substrates consisted of between

20.1%-97.9% of the invertebrate feeding. Though deadwood represented as little as 2.1% of invertebrate feeding in August 2016, I witnessed Tsinjo use deadwood more often than live trees on seven occasions: May 2016, September 2016-December 2016, April 2017 and June 2017. At no point was bamboo the most frequently used resource, and on several occasions bamboo was not used by Tsinjo for invertebrate consumption.

Substrate Use Within Months

Appendix B displays the observed nightly use of each substrate for invertebrate foraging by Tsinjo between January 2016 and December 2017. Table 2.14 presents the results of the negative binomial regression analyses which tests whether live trees, deadwood and bamboo were used in different proportions within any given month. Tsinjo foraged for invertebrates significantly more frequently on live trees than on deadwood in

January 2016 (negative binomial regression: z=2.849, df=9, p=0.004), August 2016

(z=3.693, df=11, p<0.001), January 2017 (z=2.950, df=5, p=0.003), March 2017

(z=3.607, df=13, p<0.001) and July 2017 (z=2.993, df=13, p=0.002). With only one exception, live trees were used significantly more than deadwood. However, in

September 2016 Tsinjo foraged for invertebrates on deadwood significantly more than on live trees (z=-2.239, df=11, p=0.025). Tsinjo also foraged for invertebrates significantly more on live trees than on bamboo in November 2016 (z=2.446, df=14, p=0.014),

December 2016 (z=2.135, df=20, p=0.032), March 2017 (z=3.465, df=20, p<0.001), July

2017 (z=4.370, df=20, p<0.001) and August 2017 (z=3.220, df=20, p=0.001). Lastly,

Tsinjo foraged for invertebrates significantly more on deadwood than on bamboo in

November 2016 (z=3.729, df=14, p<0.001), December 2016 (z=2.151, df=20, p=0.031), and July 2017 (z=2.267, df=20, p=0.023).

Substrate Use Between Months

Monthly substrate use is presented in Table 2.13. I used negative binomial regression analyses to test whether each substrate was used in different proportions from one month to the next. Results of these tests are presented in Table 2.15 with significant differences indicated in bold. Results indicated that monthly substrate use during foraging changed significantly eleven times over the course of the study. Tsinjo significantly decreased her live tree invertebrate foraging between January and February 2016

(negative binomial regression: z=-3.707, df=8, p<0.001) and March and April 2017 (z=-

2.173, df=9, p=0.029). She significantly increased her invertebrate foraging from May to

June 2016 (z=2.049, df=5, p=0.040) and from April to May 2017 (z=2.240, df=15, p=0.025). Tsinjo significantly increased her use of deadwood between August and

September 2016 (z=4.059, df=11, p<0.001) and March and April 2017 (z=3.704, df=9, p<0.001). She significantly decreased her use of deadwood from July to August 2016

(z=-2.411, df=11, p=0.015), November to December 2016 (z=-2.072, df=11, p=0.038),

December 2016 to January 2017 (z=-2.695, df=9, p=0.007) and from January to February

2017 (z=-3.332, df=8, p<0.001). Tsinjo only had one significant change in bamboo use: an increase between April and May 2017 (z=-2.296, df=15, p=0.037). There were two occasions where significance was expected, between September/October 2016 and

October/November 2016, but the tests did not yield significant values. This may be due to small sample sizes and multiple zero values.

Seasonal Variations in Substrate Use for Invertebrate Feeding

Table 2.16 presents and Figure 2.14 depicts the seasonal use of substrates for invertebrate consumption. Tsinjo’s use of deadwood was most variable between seasons, ranging anywhere between 63 and 597 invertebrates consumed in a single season.

Tsinjo’s use of live trees was slightly less variable, ranging anywhere between 170 and

424 invertebrates consumed in a season. In the cold/rainy season (season 2) of 2016,

Tsinjo did not consume any invertebrates in bamboo, but the following season consumed

150 invertebrates, the most invertebrates from bamboo in any season over the course of the study. The relative contribution of each substrate to seasonal invertebrate feeding varied greatly as well. Deadwood use during the hot/dry season (season 3) of 2016 represented 58.2% of the invertebrate consumption that season. However, at no other point did it consist of over 50% of the substrate use by Tsinjo during the study. Live trees, on the other hand, typically constituted over 55% of the substrates used for invertebrate foraging. Surprisingly, the lowest count of invertebrates in live trees (170) still contributed to 59% of the invertebrate foraging that season. It was the hot/dry season

51 of 2016, when deadwood and bamboo-use peaked, that live tree use comprised the lowest percentage of the overall invertebrate foraging (27%).

Substrate Use Within Seasons

Table 2.17 displays the results of the negative binomial regression analyses comparing seasonal substrate use for invertebrate foraging by Tsinjo. There were significant differences in substrates used for invertebrate foraging in every season except the cold/rainy season (season 2) of 2016. During the hot/rainy season (season 1) of 2016,

Tsinjo foraged significantly more frequently on live trees than on deadwood (z=2.578, df=47, p=0.009) or bamboo (z=5.289, df=71, p<0.001). She also foraged more on deadwood than on bamboo (z=3.382, df=71, p<0.001). During the hot/dry season

(season 3) of 2016, Tsinjo foraged more on deadwood than on live trees (z=-2.021, df=47, p=0.043) or on bamboo (z=2.804, df=71, p=0.005). In the hot/rainy season

(season 1) of 2017, Tsinjo foraged more on live trees than on bamboo (z=2.809, df=71, p=0.004). During the cold/rainy season (season 2) of 2017, Tsinjo foraged more on live trees than in deadwood (z=2.899, df=51, p=0.003) or bamboo (z=4.350, df=77, p<0.001).

During this season, she also foraged more on deadwood on bamboo (z=2.091, df=77, p=0.036). Finally, during the hot/dry season of 2017, Tsinjo foraged more on live trees than on bamboo (z=3.051, df=80, p=0.002).

Substrate Use Between Seasons

Table 2.18 presents the results of the negative binomial regression analyses for differences in substrate use between seasons (as seen in Table 2.16). There were two significant seasonal changes in substrate use by Tsinjo over the course of the study.

Tsinjo foraged significantly more on deadwood in season 3 than in season 2 of 2016

(negative binomial regression: z=2.479, df=42, p=0.013). However, Tsinjo foraged significantly less on deadwood in season 1 of 2017 compared to the prior season, season

3 of 2016 (z=-3.397, df=47, p<0.001). Once again, I was expecting a significant increase in foraging at bamboo between season 2 and season 3 of 2016; however, the tests did not yield significant values for this period. This may be due to small sample sizes and multiple zero values.

Annual Substrate Use

As seen in Table 2.13 and Figure 2.15, Tsinjo foraged on deadwood (49.7%) more frequently than on live trees (40.1%) in 2016. However, in 2017 Tsinjo used live trees more frequently (60.1%) than deadwood (29.1%). Foraging occurred on bamboo during a small portion of foraging events in 2016 and 2017 (10.2% and 10.8%).

There were significant differences in substrates used for invertebrate foraging within each year. In 2016, Tsinjo used deadwood and live trees in relatively equal amounts (negative binomial regression: z=-0.806, df=133, p=0.420). She did, however, use deadwood significantly more than bamboo (z=4.551, df=200, p<0.001) and used live trees significantly more than bamboo (z=39.32, df=200, p<0.001). In 2017, Tsinjo foraged on live trees more than on deadwood (negative binomial regression: z=3.193, df=153, p=0.001) or on bamboo (z=5.716, df=230, p<0.001). She also foraged on deadwood significantly more than on bamboo (z=3.206, df=230, p=0.001).

When substrate use between years is compared (Table 2.19), the only significant difference was a decrease in foraging on deadwood from 2016 to 2017 (z=-1.964, df=143, p=0.049).

Substrate Use Over the Course of the Study

When the entire data set is considered, Tsinjo did not forage on each of the three substrates in similar proportions. Tsinjo foraged significantly more on live trees than on bamboo (negative binomial regression: z=6.804, df=431, p<0.001). She also foraged significantly more on deadwood than on bamboo (z=5.666, df=431, p<0.001). There was no significant difference between foraging on live tree and deadwood over the duration of the study (z=0.146, df=287, p=0.146).

Preference Indices

Table 2.20 displays the preference indices calculated for each month that both ripe Canarium fruits and invertebrates were available: January-May 2016 and February-

November 2017. This index describes consumption of resources relative to their availability. In every case the monthly index value is below 1 indicating that invertebrates were preferred over Canarium seeds in ripe fruit. A preference for invertebrates over Canarium holds when the data are analyzed seasonally (Table 2.21) and annually (Table 2.22). Thus, despite the fact that the majority of the diet consisted of

Canarium seeds in ripe fruit in season 1 of 2016 and 2017 (Table 2.9 and Figure 2.11), this food cannot be considered preferred when their availability is factored in.

Discussion

The majority of literature on aye-ayes to date suggests they are too large to subsist mainly on invertebrates (Kay 1975; Iwano and Iwakawa 1988; Iwano 1991; Sterling

1993, 1994; Ancrenaz et al. 1994; Sterling and McCreless 2006). This is because the energy gained from an average, small-bodied insect should not be sufficient to offset the cost of acquiring it if the consumer is significantly larger (Kay 1975). Indeed, previous research suggests aye-ayes focused feeding efforts on non-invertebrate food items, such

54 as nectar from Ravenala madagascariensis flowers, seeds of Canarium sp., and plantation crops (Petter 1977; Iwano and Iwakawa 1988; Sterling 1993, 1994; Ancrenaz et al. 1994). However, these studies were conducted either on non-native populations or in heavily degraded habitats. For example, Iwano and Iwakawa (1988) identified

Canarium seeds as the main resource of an introduced population of aye-ayes on the island of Nosy Mangabe. Ancrenaz et al. (1994) found that aye-ayes in a disturbed forest surrounding the Mananara-Nord Biosphere Reserve preferred nectar of Ravenala madagascariensis. In both studies, aye-ayes were limited by the forest size: in one case the forest is on a small island while in the second the forest is surrounded by plantations.

In contrast, Torotorofotsy is a undisturbed forest with little disturbance. The results of my study, which I expand upon below, support Gaulin’s (1979) suggestion that aye-ayes are an exception to Kay’s threshold as they preferentially, and often exclusively, consume invertebrates. Additionally, it appears that aye-ayes are specialists on structurally defended resources, focusing their feeding on Canarium seeds and invertebrates, as suggested by Sterling (1993, 1994a).

Dietary Profile

My first objective was to develop a complete dietary profile for a naturally occurring aye-aye in a undisturbed forest. Over 99% of Tsinjo’s diet consisted of two resources: invertebrates and Canarium seeds. This supports Sterling’s (1993, 1994) conclusion that aye-ayes focus their feeding on these two resources. There were two other resources briefly used by Tsinjo during the study. Six times in February 2016, I witnessed Tsinjo foraging (or drinking) on something near the base of a Ravenala madagascariensis tree fronds. This behavior may have been to access water, as

55 described in previous reports (Sterling 1993; Sefczek et al. 2017). In May 2017, Tsinjo also consumed an unknown resource in a Vakona tree (Pandanus utilis). As suggested by Sefczek and colleagues (2017), the aye-aye ate either seeds atop the palms of Vakona or invertebrates contained within the palms of Vakona. Neither of these resources was eaten in greater quantities than invertebrates or Canarium seeds. Therefore, the discussion of monthly, seasonal, and annual resource consumption will focus on invertebrates and Canarium seeds.

Vakona feeding occurred during the cold/rainy season of 2017, specifically in the month of May. Interestingly, Tsinjo ate this Vakona resource during the pilot study in

May 2015, but not in 2016. According to some reports, the cold/rainy season is typically when resource availability is lowest in Malagasy forests (Sterling 1993; Wright 1999;

Vasey 2005). However, data collected during this study suggest a different pattern.

According to the availability data based on transect sampling, the lowest periods of

Canarium fruit availability (but not invertebrate availability) were during the hot/dry seasons (season 3) in both 2016 and 2017. Moreover, Tsinjo was seen feeding on

Vakona during the cold/rainy season (season 2) of 2017 which my food availability data suggest is the period with the greatest Canarium fruit availability. The Vakona resource may have been consumed during this season (a) because it is only available this time of year, and/or (b) because the aye-aye needed an additional resource during the month of

May, when availability of Canarium seeds in ripe fruit decreased. In other words, although Canarium seeds in ripe fruit were most abundant during the season (season 2) that included May, the abundance of this resource in May itself was the lowest during that season. In fact, Tsinjo only rarely fed on Vakona trees despite encountering them

56 nightly. Since follows in May 2016 were limited to three nights, we may have missed her feeding at Vakona trees during this month. If she did consume Vakona in May of every year, it would indicate a consistent use of this resource during the cold/rainy season. If that were the case, this resource may have had a limited availability at a critical time, specifically when Canarium seeds in ripe fruit were dwindling. Ultimately, the aye-aye may have been switching feeding efforts away from Canarium seeds in ripe fruit during this period.

Monthly Resource Consumption

My second goal was to examine aye-aye resource consumption monthly, seasonally and annually. I predicted that invertebrates would be the most frequently consumed resource every month. Tsinjo consumed invertebrates in greater quantities than Canarium seeds in ripe fruit for 16 of the 24 months. In 14 of the 24 months, invertebrates were the only resource I witnessed Tsinjo consume. Tsinjo consumed more

Canarium seeds in ripe fruit than invertebrates in eight months: between January-May of

2016 and between February-April of 2017. During six of those eight months, Tsinjo consumed Canarium seeds in ripe fruit in significantly greater quantities than invertebrates: January, February, April, and May of 2016, and February and April of

2017. In May of 2017 and June of 2017 fewer Canarium seeds were eaten (129 and 60 seeds respectively) than invertebrates (382 and 111, respectively), with the difference in

May being significant. Based on these results, I rejected my hypothesis that monthly invertebrate consumption would always exceed that of any other resource.

May and June of 2017 were the only two months when Tsinjo consumed more invertebrates than Canarium seeds in ripe fruit. While the difference in May of 2017 was

57 significant, the difference in June of 2017 was not; however, I suspect that if more observations occurred in this month it would have resulted in a significant difference.

The decrease in Canarium seeds in ripe fruit eaten by Tsinjo in May of 2017 coincided with a significant decrease in Canarium fruit availability. In June of 2017, ripe

Canarium fruit became more available; however, Tsinjo still consumed more invertebrates than Canarium seeds in ripe fruit. One possible explanation is that, although there are perhaps as many as 30 species of Canarium trees (Daly et al. 2015), aye-ayes do not feed on all of them and that a general evaluation of Canarium availability may be meaningless if it does not include the Canarium species preferred by aye-ayes.

This is similar to how chimpanzees (Pan troglodytes schweinfurthii) eat one species of fig (Ficus sansibarica) more than another (Ficus vallis-choudae; Reynolds et al. 1998).

Implications for this are discussed further below with the analysis of preference.

Examining significant changes in resource consumption between months, Tsinjo ate significantly fewer Canarium seeds in ripe fruit during February of 2016 than she did in January or March of 2016. She also significantly reduced her feeding on Canarium seeds in ripe fruit during February, March and April of 2017. These decreases in

Canarium seed feeding occurred despite a significant increase in Canarium fruit availability from February to March of 2017. The implication is that consumption of

Canarium seeds in ripe fruit cannot always be predicted from information on the relative availability of ripe Canarium fruit.

The decreases in consumption of Canarium seeds in ripe fruit may be suggestive of increased inter-specific scramble competition (Wrangham 1980; Janson and van

Schaik 1988; Sterck et al. 1997). My data suggest that as soon as Canarium seeds

58 became available Tsinjo immediately begins to feed on them, resulting in an abrupt dietary shift. For example, in January of 2017, when no Canarium fruits were available, her diet consisted of 100% invertebrates. Canarium fruits became available in February of 2017 and Tsinjo reduced her focus on invertebrates and began feeding on Canarium seeds in ripe fruit. Canarium was continually available between February and November of 2017; however, her consumption of this resource declined, perhaps a result of increased inter-specific scramble competition. Canarium fruit is an important resource for at least eight species of lemur (Daly et al. 2010; Wright et al. 2005). Diurnal groups of lemurs in Torotorofotsy, such as Varecia variegata variegata, Eulemur fulvus,

Eulemur rubriventer, and Propithecus diadema, consume ripe Canarium fruit when available (Dew and Wright 1998). Therefore, after a solitary aye-aye’s initial indulgence on Canarium seeds in ripe fruit, the competition for this resource likely increased and the aye-aye was forced to consume less Canarium seeds in ripe fruit as the season progressed and fruits were removed.

Invertebrate consumption significantly increased from August to September of

2016 and from April to May of 2017 and significantly decreased from July to August of

2016 and from November to December of 2016. These changes coincided with significant increases and decreases in deadwood foraging, respectively. Though consumption of invertebrates in live trees also changed significantly, the increases and decreases were not enough to significantly alter the overall invertebrate consumption each month. Deadwood invertebrates were also eaten by aye-ayes every month, but their use was more erratic. Increases in deadwood foraging may be due to increases in invertebrate availability in that substrate category. However, there was not a clear pattern

59 of increase in deadwood foraging from one year to the next. This could indicate that either 1) Tsinjo was fortunate in locating deadwood with high quantities of invertebrates during this time or that 2) invertebrate life cycles were less consistent in Madagascar because of the unpredictable seasonality (Rainio 2009; Cameron and Leather 2012).

Work by Rainio (2009) has shown that tropical beetles populations are sensitive to environmental changes. Therefore, it is likely that unpredictable seasonal fluctuations are indeed disrupting beetle lifecycles and thus larval abundance. Invertebrates in bamboo were frequently absent from the aye-aye’s diet and seemed supplemental to the more consistent live tree and deadwood invertebrate foraging. Randimbiharinirina and colleagues (2018) found that bamboo invertebrates were only consumed in large quantities during the hot/dry seasons, particularly October through December. It is possible invertebrates that use bamboo to house larvae have a stricter seasonality that limits the aye-ayes use of this resource.

Seasonal Resource Consumption

I predicted that invertebrates would be the most frequently consumed resource every season. During the 2016 and 2017 hot/rainy seasons (season 1), January to mid-

May, Tsinjo consumed significantly more Canarium seeds in ripe fruit than invertebrates, a finding that did not support my prediction. However, invertebrates were the most frequently consumed resource for more than half the study period. In the cold/rainy season (season 2; mid-May to mid-September) of 2017, Tsinjo consumed significantly more invertebrates than Canarium seeds in ripe fruit. In the hot/dry season (season 3; mid-September to December) of 2016 and 2017, Tsinjo only consumed invertebrates.

Canarium fruit was available in significantly greater quantities during the cold/rainy season (season 2) of 2017 compared to the hot/rainy season (season 1) of

2017. Over this period, Tsinjo decreased her consumption of this resource, though not significantly. Although Tsinjo consumed Canarium seeds in ripe fruit during this cold/rainy season, she ate significantly greater amounts of invertebrates during this season. I suspect that the increase in Canarium fruit availability from the hot/rainy season of 2017 to the cold/rainy season of 2017 is due, in part, to the unpredictable seasonality of Madagascar (Wright 1999; Vasey 2005). In January 2016, Canarium trees were already producing fruit, however the following year fruit production was delayed

(Table 2.1). Additionally, Canarium trees stopped producing new fruits after July 2016, but in 2017 fruit production continued into November (Table 2.1). As mentioned previously, the increase in invertebrate consumption during the cold/rainy season of 2017 must be examined within the context of variation in Canarium abundance. Although the exact number is unknown, there could be as many as 33 species of Canarium trees in

Madagascar fruiting asynchronously (Daly et al. 2015). Thus, it is possible that Tsinjo uses one species of Canarium tree for fruit and ignores the rest. Future work should focus on exploring the botanical diversity of Canarium and whether aye-ayes prefer certain species over others.

There were two significant changes to seasonal consumption of both Canarium seed and invertebrates. Unsurprisingly, there was a significant increase in Tsinjo’s feeding on Canarium seeds in fruit when shifting from season 3 of 2016 to season 1 of

2017. This was because Canarium fruit was absent in season 3 of 2016 and, therefore, unavailable. Canarium seeds in ripe fruit were available and eaten in season 1 of 2017.

There was also a significant decrease from season 1 to season 2 of 2016 because

Canarium fruit availability decreased or was absent for the remainder of the season and year.

The seasonal increase in Canarium seed consumption between the hot/dry season

(season 3) of 2016 and the hot/rainy season (season 1) of 2017 was accompanied by a significant decrease in invertebrate consumption by Tsinjo. During this period, there was a significant decrease in foraging on deadwood. The significant increase in invertebrate consumption from season 2 (cold/rainy) to season 3 (hot/dry) of 2016 coincided with a significant increase in foraging on deadwood. Foraging on live trees never significantly changed from season to season. Therefore, when Tsinjo consumed more Canarium seeds in ripe fruit, it was her foraging on deadwood that changed while her foraging on live trees remained relatively constant. This suggests that live tree invertebrates are more important to the diets of wild aye-ayes than deadwood invertebrates, as described by

Andriamisedra and colleagues (2015) and Sefczek and co-authors (2017). This conclusion is contrary to suggestions by Petter (1977) and Sterling (1993, 1994). The perceived lack of importance of live trees to aye-aye invertebrate foraging in Petter

(1977) and Sterling (1993, 1994a) may be indicative of the quality of habitat in which those studies occurred. As discussed below, I maintain that when live trees are sufficiently abundant, aye-ayes will extract invertebrates in comparable quantities to those in deadwood. It is also apparent that Canarium seeds may be eaten in different quantities depending on the season, but that invertebrates are relied upon heavily throughout the year.

Differences in spatial patchiness of Canarium seeds in ripe fruit and invertebrates may be one reason why Tsinjo consumed more Canarium seeds in the hot/rainy seasons

(season 1) of 2016 and 2017. A single Canarium tree can produce hundreds, if not thousands of fruits during its fruiting season. Therefore, Canarium trees represent a patchy resource where aye-ayes can spend long periods of time removing seed after seed from ripe fruit. In contrast, larvae can occur singularly or in groups within a woody substrate (Isbell 1991; Sterling 1993, 1994a; Hanks 1999). They can also be clumped, with multiple deposits within a substrate, or evenly distributed throughout the environment, with each woody host holding just one deposited egg (Isbell 1991; Sterling

1993, 1994a; Hanks 1999). Aye-ayes do not likely know how many invertebrates are contained within a substrate, so it is therefore conceivable that Canarium trees represent a more reliable and continually available resource than woody substrates.

Seasonally low availability of invertebrates may be another reason why consumption of Canarium seeds is greater than invertebrate consumption during some seasons. Invertebrate populations are often influenced by climatic fluctuations (Rainio

2009; Cameron and Leather 2012) and it is possible the hot/rainy season (season 1) is a time when invertebrate availability is lowest. If so, then aye-ayes may be compensating for low invertebrate availability by eating large quantities of Canarium seeds in ripe fruit.

Based on measures of feeding traces along transects, invertebrates were available throughout the majority of the year (Table 2.1). However, assessing food abundance in this manner only identifies quantities already consumed and not necessarily the full complement of available invertebrates. Since my invertebrate availability estimates were based on consumed invertebrates as deduced from traces, and invertebrate consumption

63 decreased as Canarium feeding increased, it is not possible to determine if invertebrate consumption dropped because of a lack of availability or due to dietary switching. Future work must identify a reliable method for determining how many invertebrates on average are found in live and deadwood substrates.

Annual Resource Consumption

I predicted that invertebrates would be the most frequently consumed resource each year. In both years, the aye-aye ate more invertebrates than Canarium seeds, but the difference was not significant. Therefore, the data did not support my prediction. My data did not indicate that invertebrates were only consumed when other resources were not available, as suggested elsewhere (Sterling and McCreless 2006). Rather, ingestion of Canarium seeds in ripe fruit and invertebrates were consistent over the two-year study.

Based on my findings, I argue that invertebrates are more important to the aye-aye’s diet than Canarium seeds.

Only one other study has examined temporal changes in aye-aye feeding behavior. Sterling (1993, 1994) found that invertebrate consumption occurred throughout the year, but it peaked during the cold/rainy season and at no time did invertebrates comprise the entire diet. This was not the case in Torotorofotsy. Tsinjo consumed greater quantities of invertebrates in the cold/rainy season (season 2) and the hot/dry season (season 3) in both 2016 and 2017. Moreover, invertebrates were 100% of the diet in 14 of the study’s 24 months, and accounted for approximately 60% of the overall diet.

Additionally, Sterling (1993, 1994) found that aye-ayes used more deadwood than any other substrate when foraging for invertebrates. In Torotorofotsy, live trees were used as frequently as deadwood during invertebrate foraging. In fact, live trees were the more

64 consistently used substrate, as Tsinjo never had significant seasonal or annual fluctuations in her foraging on live trees. As suggested previously (Sefczek et al. 2017;

Randimbiharinirina et al. 2018), the decreased consumption of invertebrates on Nosy

Mangabe (Sterling 1993, 1994a), particularly in live trees, may be due to an overpopulation of aye-ayes on the island. This is discussed in further detail in the conclusion.

Feeding Preference

My third objective was to evaluate preference for the resources consumed. The results supported my prediction that invertebrates would be the aye-ayes preferred resource monthly seasonally and annually. Canarium seeds were never preferred.

Sterling and McCreless (2006) suggested that aye-ayes did not preferentially consume invertebrates; rather, aye-ayes focused on invertebrates when other resources in the environment were scarce. As mentioned previously, preference is a function of consumption relative to availability. Canarium trees can produce hundreds, if not thousands of fruits, whereas hollow chambers in woody substrates hold upwards of ten larvae (Hanks 1999). Therefore, in virtually all cases where ripe Canarium is available,

Canarium seeds in ripe fruit will always represent a larger resource patch than substrates containing invertebrates. It should be again emphasized that I assumed a 1:1 ratio of new traces gnawed and larvae removed, so it is possible Tsinjo removed more than one larvae at a time. It is equally possible that during some foraging bouts she removed no larvae.

Therefore, invertebrate availability may be higher or lower than the estimated values in this study.

Between January and May of each year when most of the Canarium trees fruited, abundance of this resource was far greater than invertebrate abundance. Since Canarium seeds are a fat-rich, high-energy resource (Sterling 1993, 1994), aye-ayes could theoretically subsist only on this food if enough of it is available. In this way, the aye- aye would behave in a manner similar to orangutans when ripe fruit is available and the diet consists of 100% fruit (Knott 1998). Instead, the aye-aye continued to pursue the cryptic, less abundant invertebrate resource during this time. Therefore, though invertebrates did not comprise the majority of the diet during the hot/rainy seasons

(season 1), they were still preferred. Additionally, if Canarium seeds were preferred, aye-ayes would be expected to have consumed this resource in the later months of 2017

(July-November) when some trees were still producing fruit. Instead, the aye-aye almost exclusively consumed larvae despite Canarium seeds being available.

Aye-aye resource preference may be more fine-grained than I assumed. For this study, all Canarium species were considered as one resource and all invertebrates were considered another. The majority of Canarium trees produced fruit during the hot/rainy season from January to mid-May. The only exception was one tree along the transects which provided ripe fruit from May to early November 2017. Asynchronous fruiting in

Canarium was not surprising as it has been suggested that this genus has as many as 33 species in Madagascar, each with their own fruiting pattern (Daly et al. 2015). Despite its extended availability, Tsinjo only consumed Canarium from January 2016 to May 2016 and February 2017 to June 2017. It is possible that the aye-aye may be displaying a preference for seeds of certain species of Canarium, especially those fruiting during the hot/rainy season when Canarium seed feeding was significantly greater than invertebrate

66 consumption. If aye-ayes are foraging for ripe fruit from a specific species of Canarium, this could result in a lower abundance value of this resource and potentially change the values of the preference index. However, these Canarium trees still produce ample fruits in a single canopy and there would likely need to be an extremely low density of this tree species to reach a preference level. Unfortunately, a more fine-grained analysis of

Canarium seed use is impossible without information on the exact number of Canarium species and the fruiting season for each type, both of which are presently unavailable. As mentioned above, future work should be directed at the botanical diversity in the

Canarium genus.

In addition to missing information on Canarium, we lack important information on saproxylic beetle larvae. Information from both Sterling (1993) and the present study indicate that aye-ayes consume different sized larvae (see Figure 1.2). It is reasonable to assume that some of this size difference is attributable to species differences among beetles. If it can be determined that aye-ayes prefer one species of invertebrate over another, then an appreciation of this diversity would most likely result in greater dietary partitioning. Separation of invertebrates into different resource categories would likely result in an even lower population estimate for each species of invertebrate. It would be interesting to determine whether aye-ayes can distinguish between invertebrate types before commencing foraging since invertebrates are contained within a substrate and cannot be identified until they are removed.

Lastly, preference could be skewed if I did not witness aye-aye feeding events on

Canarium trees during non-peak seasons (i.e. cold/rainy and hot/dry). I did not conduct full night follows nor did I observe the aye-aye every night. Therefore, Tsinjo may have

67 consumed Canarium seeds after follows were over or on nights when follows did not occur. However, there were several instances when Tsinjo used the same resource, a

Canarium tree or a substrate for invertebrate foraging, on consecutive nights. It therefore seems unlikely that feeding events at Canarium trees during these periods would have gone unnoticed.

Scale of Dietary Diversity

Over the course of the two-year study, there was no significant difference in the quantity of invertebrates and Canarium seeds in ripe fruit that Tsinjo consumed. Indeed, within both 2016 and 2017, Tsinjo consumed nearly equivalent quantities of both resources. However, because Canarium fruit had a limited availability each year, the quantities of each resource consumed were not proportional within any given season. For example, Tsinjo consumed significantly more Canarium seeds in ripe fruit than invertebrates during the hot/rainy season of 2017. Furthermore, monthly evaluation of dietary composition may not even reflect the pattern of the corresponding season. For example, in January of 2017, Tsinjo’s diet only included invertebrates, even though she ate more Canarium seeds in ripe fruit during the hot/rainy season (season 1) of 2017.

Because the aye-aye can have very different feeding behaviors over short time scales, long-term studies on aye-aye feeding behavior are critical to establish accurate dietary composition.

Conclusion

My findings support Sterling’s suggestion that aye-ayes are specialists on the structurally defended resources of Canarium seeds and invertebrates. They also indicate that aye-ayes overcome their large body size to preferentially consume invertebrates.

Invertebrates are high in lipids and protein, and therefore considered a high-energy 68 resource (Sterling 1993). However, Kay’s threshold indicates that primates over 500g should not be able to sustain themselves on a primarily invertebrate diet (Kay 1975). My findings indicate that the aye-aye is an exception to Kay’s threshold as Tsinjo not only preferentially consumed invertebrates, but sustained herself solely on invertebrates 14 months out of the two-year study. The important question is what makes this possible?

As Gaulin (1979) suggests, the unique morphology and foraging behavior is likely how aye-ayes overcome the limitations of their body size. I maintain that aye-ayes have evolved sensory, positional/postural (discussed in Chapter 4) and processing adaptations for their preferred resource: invertebrates. While sensory and postural adaptations are typically associated with preferred resources, processing adaptations are often associated with fallback foods (Marshall and Wrangham 2007; Harrison and Marshall 2011;

Rosenberg 2013). This means that aye-ayes not only violate Kay’s threshold, but also defy expected associations between processing morphologies and fallback foods. Similar to sooty mangabeys, whose thick molar enamel is used to break open hard seeds

(McGraw et al. 2014), and Goeldi’s monkeys, which have high sheering cusps and an elongated hindgut for breaking down fungus (Porter et al. 2008), the aye-aye’s continuously growing incisors, elongated fingers and specialized metacarpophalangeal joint in the third digit are used to access their preferred resource, namely invertebrates contained within woody substrates. Despite their numerous morphological and behavioral adaptations, the average body size for aye-ayes (2.6 kg) is over five times greater than what a predominantly insectivorous primate should be (Kay 1975). This leads to the possibility that aye-ayes also might possess metabolic adaptations that

69 facilitate insectivory given their large body size. This question is beyond the scope of the current research, but is a hypothesis very much worth pursuing.

Positioning my findings within the broader context of aye-aye feeding research, it becomes apparent that aye-ayes show a high level of flexibility in their diet. There have been three previous studies examining the complete dietary repertoire of aye-ayes: one on the island of Nosy Mangabe (Sterling 1994) and two in disturbed forests (Ancrenaz et al.

1994; Randimbiharinirina et al. 2018). On the 520 ha island of Nosy Mangabe, 95% of the aye-ayes’ diets consisted of four resources, Canarium seeds, invertebrates, Ravenala madagascariensis nectar, and cankerous growths on trees (Sterling 1994). In the disturbed forest surrounding Mananara-Nord Biosphere Reserve, aye-ayes preferentially consumed Ravenala madagascariensis nectar and also ate coconuts and invertebrates

(Ancrenaz et al. 1994). Lastly, in the Kianjavato Classified Forest, another disturbed forest, two male aye-ayes were found to consume invertebrates and Canarium seeds, and to a lesser extent Ravenala madagascariensis nectar (Randimbiharinirina et al. 2018).

Excluding the study by Ancrenaz and colleagues (1994) which was conducted in a forest adjacent to coconut plantations, it appears that as forest patch size increases, dietary breadth decreases. It should be noted that the differences in dietary composition of aye- ayes in Nosy Mangabe, Kianjavato and Torotorofotsy may vary because of qualitatively different habitats. Nosy Mangabe is off the northeast coast of Madagascar, while

Torotorofotsy is in the east and Kianjavato is in the southeast. Nevertheless, all three forests are tropical rain forests with similar resources available to aye-ayes, specifically

Canarium seeds in ripe fruit, nectar from Ravenala madagascariensis flowers, and invertebrates. On the 520 ha island of Nosy Mangabe, aye-aye diets included four

70 resources. In the disturbed forest of Kianjavato, approximately 4,725ha, aye-ayes consumed three resources. In Torotorofotsy, a 1,100 ha forest adjacent to the 9,875 ha forest of Mantadia National Park (Shyamsundar and Kramer 1997), over 99% of the aye- aye’s diet was composed of just two resources, invertebrates and Canarium seeds.

Unfortunately, undisturbed forests such as Torotorofotsy are increasingly rare due to deforestation and agricultural expansion (Chapman et al. 2006). Forest degradation and loss of critical resources can prove untenable for most primate (Harcourt and Doherty

2005). For example, cao vit gibbons (Nomascus nasutus; Fan et al. 2011), redtail monkeys (Cercopithecus ascanius; Rode et al. 2006), bearded saki monkeys (Chiropotes sp.; Benchimol and Peres 2014), Moore’s woolly lemurs (Avahi mooreorum; Sawyer et al. 2017) and Masoala sportive lemurs (Lepilemur scottorum; Sawyer et al. 2017) have lower population sizes in heavily disturbed habitats because their primary resources are scarce and therefore difficult to obtain. However, insectivorous primates, such as the

Dian’s tarsiers (Tarsius dianae; Merker and Muhlenberg 2000) and Javan slow lorises

(Nycticebus javanicus; Rode-Margono et al. 2014), occur in higher densities in disturbed habitats. In fact, it appears that insectivorous primates generally have a high threshold for environmental disturbance (Johns and Skorupa 1987). Aye-ayes are also capable of adjusting to habitat degradation by decreasing home ranges and increasing dietary breadth. Preliminary observations suggest that aye-ayes in Kianjavato may have a higher population density than those at Torotorofotsy (Edward Louis, pers. comm.). The ability of the highly morphologically specialized aye-aye to survive in disturbed forests is a testament to its adaptive capacity.

Not only are aye-ayes able to consume different resources depending upon their environment, they also appear able to survive even when their preferred resource is available in limited quantities. We know that aye-ayes have the largest distribution of any lemur species across the island of Madagascar and can occur in undisturbed forests, disturbed forests, and near plantations (Petter 1962, 1977; Ganzhorn and Rabesoa 1986;

Simons 1993; Sterling 1993, 1994; Ancrenaz et al. 1994). Because previous studies were conducted on either introduced populations or populations in disturbed habitats, invertebrates were identified as a less valued resource in the aye-aye’s diet (Iwano and

Iwakawa 1988; Ancrenaz et al. 1994; Sterling 1993, 1994a). I have shown that an aye- aye in a undisturbed forest preferentially, and often exclusively, consumes invertebrates, frequently from live trees. In fragmentary forests, especially along plantations (Petter

1977; Ancrenaz et al. 1994), aye-ayes will consume fewer invertebrates and supplement with Ravenala madagascariensis nectar or plantation crops (Ancrenaz et al. 1994;

Randimbiharinirina et al. 2018). In disturbed forests adjacent to plantations, aye-ayes decrease the quantity of invertebrates consumed throughout the year, to the point where they raid crops more frequently than they consume invertebrates (Petter 1977; Ancrenaz et al. 1994). In Kianjavato, where the forest patches are larger but still disturbed, aye- ayes consume invertebrates primarily from deadwood, and supplement the diet with

Ravenala madagascariensis nectar (Randimbiharinirina et al. 2018). As demonstrated here and elsewhere (Andriamisedra et al. 2015; Sefczek et al. 2017), aye-ayes in a undisturbed forest will utilize live trees more than any other substrate for invertebrate foraging.

What is clear from these studies is that the substrates aye-ayes feed on are largely a function of the degree of habitat disturbance associated with the study site. Foraging on live tree invertebrates is compromised by forest degradation due to the obvious reduction in live trees that accompanies deforestation. Moreover, it is likely that overall invertebrate abundance and species richness in tropical forests decreases when large- diameter trees are removed, as is the case in temperate forests (Grove 2002). Given these assumptions, reports of aye-aye using deadwood as their main substrate for invertebrate feeding (Petter 1977; Sterling 1993, 1994; Ancrenaz et al. 1994) and relying on Ravenala or Canarium as preferred resources (Iwano and Iwakawa 1988; Ancrenaz et al. 1994) may in fact be due to aye-ayes missing a critical resource, namely invertebrates in live trees.

I determined that aye-ayes at Torotorofotsy focus on invertebrates and Canarium seeds, a finding similar to that of Sterling at Nosy Mangabe (Sterling 1993, 1994).

However, Sterling and McCreless (2006) claimed that invertebrates were consumed when other resources, especially Canarium fruit, became less available. In other words, invertebrates at Nosy Mangabe were fallback foods (sensu Marshall and Wrangham

2007) for aye-ayes. I believe the dietary profile of aye-ayes at Nosy Mangabe has been effected by the size of the study site. It may be that there is an unusually high density of aye-ayes on the 520 ha island and that aye-ayes may not be able consume this resource as frequently as they would under more pristine conditions (further discussion can be found in chapter 3). When female aye-ayes are not as spatially confined, their dispersed polygyny social system guarantees a home range with a steady supply of invertebrates. If it is true that the number of aye-ayes on Nosy Mangabe is abnormally high, and that the

73 size of the female’s home ranges on this island are a small fraction of what they are at

Torotorofotsy, then the number of invertebrates contained within a typical Nosy Mangabe aye-aye home range would be depleted rapidly. As a result, the diets of Nosy Mangabe aye-ayes must contain greater quantities of alternatives, in this case Canarium seeds in ripe fruit, Ravenala madagascariensis nectar and cankerous growths (Sterling 1993,

1994a). In contrast, female aye-ayes at Torotorofotsy are not constrained by other females, their home ranges are enormous, and they do not appear to be ‘falling back’ on invertebrates. Indeed, this resource is the preferred and often sole food used throughout the year. Future studies can test this by recolonizing forests with endemic tree species and examining if/how aye-ayes’ feeding behavior changes with respect to invertebrate consumption.

Table 2.1 Monthly assessments of food availability during the study period, January 2016 through December 2017, in Torotorofotsy, Madagascar. Invertebrate abundance was determined by counting the number of feeding traces along transects. Number of ripe Canarium fruit, number of Canarium seeds on the ground, and mature flowers on Ravenala madagascariensis were enumerated along transects during the same period.

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Annual Totals Invertebrates 25 26 32 23 10 2 6 16 32 12 60 14 258 Ripe 12500 15200 16200 7500 6500 7000 4900 0 0 0 0 0 69800 Canarium Fruit 2016 Canarium 450 720 1250 6900 2750 2400 2100 2000 0 0 0 0 18570 Seeds Mature 66 53 4 0 0 0 0 6 21 43 62 63 318 Ravenala Flowers Invertebrates 0 0 16 12 36 19 20 25 22 15 20 0 185 Ripe 0 2500 4800 2800 900 4000 3000 4000 900 400 300 0 23600 Canarium Fruit 2017 Canarium 0 100 400 1100 2850 1000 500 300 900 500 200 0 7850 Seeds Mature 27 49 22 27 0 4 0 14 4 6 15 12 180 Ravenala Flowers

Resource Total for Sampling Period Invertebrates 443 Ripe Canarium Fruit 93,400 Canarium Seeds 26,420 Mature Ravenala Flowers 498

Table 2.2 Results of G-test of goodness-of-fit comparing monthly abundance of different resources recorded along transects between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant differences between months are highlighted in bold. There was 1 degree of freedom for all tests. Continued table.

Ripe Canarium Invertebrates Canarium seeds Mature Fruit Ravenala Flowers G-value p-value G-value p-value G-value p-value G-value p-value Jan/Feb 2016 263.5952 <0.001 0.0196 0.888 62.87285 <0.001 1.423 0.232 Feb/Mar 2016 31.8525 <0.001 0.6218 0.430 144.3608 <0.001 50.052 <0.001 Mar/Apr 2016 3269.569 <0.001 1.4793 0.223 4313.461 <0.001 N/A N/A Apr/May 2016 71.4894 <0.001 5.2626 0.021 1844.253 <0.001 N/A N/A May/Jun 2016 18.5227 <0.001 5.822 0.015 23.80475 <0.001 N/A N/A Jun/Jul 2016 372.5361 <0.001 2.0929 0.147 20.0148 <0.001 N/A N/A Jul/Aug 2016 N/A N/A 4.7165 0.029 2.43926 0.118 N/A N/A Aug/Sep 2016 N/A N/A 5.4367 0.019 N/A N/A 8.8258 0.002 Sep/Oct 2016 N/A N/A 9.4331 0.002 N/A N/A 7.7189 0.005 Oct/Nov 2016 N/A N/A 34.9323 <0.001 N/A N/A 3.4571 0.062 Nov/Dec 2016 N/A N/A 30.7991 <0.001 N/A N/A 0.008 0.928 Dec 2016/Jan 2017 N/A N/A N/A N/A N/A N/A 14.81 <0.001 Jan/Feb 2017 N/A N/A N/A N/A N/A N/A 6.4604 0.011 Feb/Mar 2017 737.149 <0.001 N/A N/A 192.744 <0.001 10.53 0.001 Mar/Apr 2017 532.565 <0.001 0.5733 0.448 339.696 <0.001 0.511 0.474 Apr/May 2017 1023.846 <0.001 12.557 <0.001 802.91 <0.001 N/A N/A

Continued

Table 2.2 Continued

Ripe Canarium Invertebrates Canarium seeds Mature Fruit Ravenala Flowers G-value p-value G-value p-value G-value p-value G-value p-value May/Jun 2017 2119.043 <0.001 5.3415 0.020 926.788 <0.001 N/A N/A Jun/Jul 2017 143.347 <0.001 0.0256 0.872 169.899 <0.001 N/A N/A Jul/Aug 2017 143.347 <0.001 0.5567 0.455 50.534 <0.001 N/A N/A Aug/Sep 2017 2119.043 <0.001 0.1916 0.661 313.948 <0.001 5.883 0.015 Sep/Oct 2017 197.354 <0.001 1.332 0.248 115.893 <0.001 0.4027 0.525 Oct/Nov 2017 14.3347 <0.001 0.7167 0.397 132.828 <0.001 0.3984 0.045 Nov/Dec 2017 N/A N/A N/A N/A N/A N/A 0.334 0.563

Table 2.3 Seasonal totals of food availability recorded along transects between January 2016 and December 2017 in Torotorofotsy, Madagascar.

Season 1 Season 2 Season 3

Invertebrates 106 34 118 Ripe Canarium Fruit 51400 18400 0 2016 Canarium Seeds 9320 9250 0 Mature Ravenala Flowers 123 6 189 Invertebrates 28 100 57 Ripe Canarium Fruit 10100 11900 1600 2017 Canarium Seeds 1600 4650 1600 Mature Ravenala Flowers 125 18 37

Table 2.4 Results of negative binomial regression analysis comparing seasonal abundance of different resources recorded along transects between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold.

Ripe Invertebrates Canarium Ravenala Canarium seeds Fruit Season 1/Season 2 2016 p<0.001 p<0.001 p=0.989 p=0.030 Season 2/Season 3 2016 p=0.028 p=0.006 p=0.998 p<0.001 Season 3 2016/Season 1 2017 p=0.042 p=0.070 p=0.158 p=0.109 Season 1/Season 2 2017 p<0.001 p=0.066 p=0.276 p=0.002 Season 2/Season 3 2017 p<0.001 p=0.225 p=0.256 p=0.328

Table 2.5 Results of the negative binomial regression analysis for annual comparison of resource availability along transects between January 2016 and December 2017 in Torotorofotsy, Madagascar.

Ripe Canarium Invertebrates Canarium Ravenala Fruit seeds 2016/2017 p<0.001 p=0.373 p<0.001 p<0.001

Follows Canarium seeds in Invertebrates Vakona/Ravenala ripe fruit Count Percentage Count Percentage Count Percentage January 2016 5 300 79.4% 78 20.6% 0 0.0% February 2016 4 170 85.0% 24 12.0% 6 3.0% March 2016 8 267 77.6% 77 22.4% 0 0.0% April 2016 7 291 83.1% 59 16.9% 0 0.0% May 2016 3 84 67.7% 40 32.3% 0 0.0% June 2016 3 0 0.0% 72 100% 0 0.0% July 2016 7 0 0.0% 109 100% 0 0.0% August 2016 7 0 0.0% 48 100% 0 0.0% September 2016 7 0 0.0% 169 100% 0 0.0% October 2016 8 0 0.0% 409 100% 0 0.0% November 2016 5 0 0.0% 319 100% 0 0.0% December 2016 7 0 0.0% 161 100% 0 0.0% 2016 Totals 71 1112 41.5% 1565 58.3% 6 0.2%

January 2017 3 0 0.0% 52 100% 0 0.0% February 2017 6 400 86.8% 61 13.2% 0 0.0% March 2017 8 309 77.6% 89 22.4% 0 0.0% April 2017 4 184 90.2% 20 9.8% 0 0.0% May 2017 13 129 24.5% 382 72.8% 14 2.7% June 2017 5 60 35.1% 111 64.9% 0 0.0% July 2017 7 0 0.0% 144 100% 0 0.0% August 2017 8 0 0.0% 180 100% 0 0.0% September 2017 7 0 0.0% 107 100% 0 0.0% October 2017 9 0 0.0% 208 100% 0 0.0% November2017 6 0 0.0% 117 100% 0 0.0% December 2017 6 0 0.0% 178 100% 0 0.0% 2017 Totals 82 1082 39.4% 1649 60.1% 14 0.5%

Table 2.7 Results of tests for differences between the number of Canarium seeds in ripe fruit consumed and number of invertebrates consumed within each month between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant results of the negative binomial regression analysis indicating differences within months are highlighted in bold.

p-value January 2016 <0.001 February 2016 <0.001 March 2016 <0.001 April 2016 <0.001 May 2016 <0.001 February 2017 <0.001 March 2017 <0.001 April 2017 <0.001 May 2017 0.043 June 2017 0.642

Canarium Invertebrates Vakona Ravenala Jan/Feb 2016 p<0.001 p=0.078 N/A p=0.998 Feb/Mar 2016 p=0.013 p=0.489 N/A p=0.997 Mar/Apr 2016 p<0.001 p=0.976 N/A N/A Apr/May 2016 p<0.001 p=0.747 N/A N/A May/Jun 2016 p=1 p=0.270 N/A N/A Jun/Jul 2016 N/A p=0.603 N/A N/A Jul/Aug 2016 N/A p=0.050 N/A N/A Aug/Sep 2016 N/A p<0.001 N/A N/A Sep/Oct 2016 N/A p=0134 N/A N/A Oct/Nov 2016 N/A p=0.559 N/A N/A Nov/Dec 2016 N/A p=0.001 N/A N/A Dec 2016/Jan 2017 N/A p=0.486 N/A N/A Jan/Feb 2017 p=0.004 p=0.060 N/A N/A Feb/Mar 2017 p<0.001 p=0.747 N/A N/A Mar/Apr 2017 p<0.001 p=0.229 N/A N/A Apr/May 2017 p=0.495 p<0.001 p=0.998 N/A May/Jun 2017 p=0.008 p=0.871 p=0.998 N/A Jun/Jul 2017 p=0.993 p=0.487 N/A N/A Jul/Aug 2017 N/A p=0.505 N/A N/A Aug/Sep 2017 N/A p=0.189 N/A N/A Sep/Oct 2017 N/A p=0.199 N/A N/A Oct/Nov 2017 N/A p=0.423 N/A N/A Nov/Dec 2017 N/A p=0.301 N/A N/A

Canarium Invertebrates Vakona/Ravenala Count Percentage Count Percentage Count Percentage Season 1 2016 1028 79.9% 252 19.6% 6 0.5% Season 2 2016 84 22.6% 288 77.4% 0 0.0% Season 3 2016 0 0.0% 1018 100.0% 0 0.0% Season 1 2017 1022 74.1% 357 25.9% 0 0.0% Season 2 2017 60 7.9% 682 90.2% 14 1.9% Season 3 2017 0 0.0% 610 100.0% 0 0.0%

p-value Season 1 2016 0.008 Season 2 2016 0.062 Season 3 2016 N/A Season 1 2017 <0.001 Season 2 2017 <0.001 Season 3 2017 N/A

Table 2.11 Results of negative binomial regression analysis for seasonal comparisons of consumption rates by Tsinjo between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold.

Canarium Invertebrates Vakona Ravenala Season 1/Season 2 2016 p=0.027 p=0.213 N/A p=0.998 Season 2/Season 3 2016 p=0.266 p<0.001 N/A N/A Season 3 2016/Season 1 2017 p<0.001 p<0.001 N/A N/A Season 1/Season 2 2017 p=0.003 p=0.013 p=0.995 N/A Season 2/Season 3 2017 p=1 p=0.446 p=0.994 N/A

Table 2.12 Results of negative binomial regression analysis for comparing annual resource consumption rates by Tsinjo between January 2016 and December 2017 in Torotorofotsy, Madagascar.

Canarium Invertebrates 2016/2017 p=0.522 p=0.859

Table 2.13 Monthly number of traces made in live trees, deadwood and bamboo by Tsinjo for consuming invertebrates between January 2016 and December 2017 at Torotorofotsy, Madagascar.

Follows Live Tree Deadwood Bamboo Count Percentage Count Percentage Count Percentage January 2016 5 66 84.6% 12 15.4% 0 0.0% February 2016 4 11 45.8% 4 16.7% 9 37.5% March 2016 8 50 64.9% 27 35.1% 0 0.0% April 2016 7 42 71.2% 17 28.8% 0 0.0% May 2016 3 15 37.5% 25 62.5% 0 0.0% June 2016 3 45 62.5% 27 37.5% 0 0.0% July 2016 7 60 55.0% 49 45.0% 0 0.0% August 2016 7 47 97.9% 1 2.1% 0 0.0% September 2016 7 34 20.1% 135 79.9% 0 0.0% October 2016 8 112 27.4% 166 40.6% 131 32.0% November 2016 5 72 22.6% 240 75.2 % 7 2.2% December 2016 7 74 46.0% 75 46.6% 12 7.4% 2016 Totals 71 628 40.1% 778 49.7% 159 10.2%

January 2017 3 37 71.2% 15 28.8% 0 0.0% February 2017 6 51 83.6% 6 9.8% 4 6.6% March 2017 8 82 92.1% 4 4.5% 3 3.4% April 2017 4 6 30.0% 14 70.0% 0 0.0% May 2017 13 196 51.3% 115 30.1% 71 18.6% June 2017 5 39 35.1% 57 51.4% 15 13.5% July 2017 7 124 86.1 % 18 12.5% 2 1.4% August 2017 8 108 63.5% 47 27.7% 15 8.8% September 2017 7 53 49.5 % 34 31.8% 20 18.7% October 2017 9 141 67.8% 67 32.2% 0 0.0% November2017 6 65 55.6% 52 44.4% 0 0.0% December 2017 6 88 49.5% 41 23.0% 49 27.5% 2017 Totals 82 990 60.1% 479 29.1% 179 10.8% OVERALL 153 1618 50.4% 1257 39.1% 338 10.5%

Table 2.14 Results of negative binomial regression analysis which tests whether live trees, deadwood and bamboo were used in different proportions within a given month. Significant differences between months are highlighted in bold.

Comparison of Live Comparison of Live Comparison of Tree and Deadwood Tree and Bamboo Deadwood and Bamboo January 2016 p=0.004 N/A N/A February 2016 p=0.304 p=0.878 p=0.553 March 2016 p=0.317 N/A N/A April 2016 p=0.427 N/A N/A May 2016 p=0.508 N/A N/A June 2016 p=0.672 N/A N/A July 2016 p=0.794 N/A N/A August 2016 p<0.001 N/A N/A September 2016 p=0.025 N/A N/A October 2016 p=0.354 p=0.837 p=0.756 November 2016 p=0.096 p=0.014 p<0.001 December 2016 p=0.935 p=0.032 p=0.031 January 2017 p=0.003 N/A N/A February 2017 p=0.159 p=0.116 p=0.808 March 2017 p<0.001 p<0.001 p=0.788 April 2017 p=0.082 N/A N/A May 2017 p=0.211 p=0.059 p=0.374 June 2017 p=0.587 p=0.243 p=0.101 July 2017 p=0.002 p<0.001 p=0.023 August 2017 p=0.089 p=0.001 p=0.066 September 2017 p=0.484 p=0.258 p=0.541 October 2017 p=0.354 N/A N/A November 2017 p=0.660 N/A N/A December 2017 p=0.399 p=0.648 p=0.890

Table 2.15 Results of negative binomial regression analysis for monthly comparison of substrate use for invertebrate foraging by Tsinjo between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold.

Live Tree Deadwood Bamboo Jan/Feb 2016 p<0.001 p=0.578 p=0.996 Feb/Mar 2016 p=0.263 p=0.189 p=0.997 Mar/Apr 2016 p=0.880 p=0.844 N/A Apr/May 2016 p=0.716 p=0.373 N/A May/Jun 2016 p=0.040 p=0.955 N/A Jun/Jul 2016 p=0.184 p=0.957 N/A Jul/Aug 2016 p=0.393 p=0.015 N/A Aug/Sep 2016 p=0.402 p<0.001 N/A Sep/Oct 2016 p=0.089 p=0.919 p=0.998 Oct/Nov 2016 p=0.969 p=0.251 p=0.060 Nov/Dec 2016 p=0.061 p=0.038 p=0.670 Dec 2016/Jan 2017 p=0.828 p=0.007 p=0.997 Jan/Feb 2017 p=0.084 p<0.001 p=0.997 Feb/Mar 2017 p=0.699 p=0.386 p=0.563 Mar/Apr 2017 p=0.029 p<0.001 p=0.997 Apr/May 2017 p=0.025 p=0.361 p=0.037 May/Jun 2017 p=0.555 p=0.304 p=0.186 Jun/Jul 2017 p=0.209 p=0.091 p=0.060 Jul/Aug 2017 p=0.667 p=0.334 p=0.116 Aug/Sep 2017 p=0.149 p=0.619 p=0.834 Sep/Oct 2017 p=0.250 p=0.459 p=0.275 Oct/Nov 2017 p=0.442 p=0.853 N/A Nov/Dec 2017 p=0.469 p=0.255 p=0.998

Table 2.16 Seasonal use of live trees, deadwood and bamboo by Tsinjo for consuming invertebrates between January 2016 and December 2017 at Torotorofotsy, Madagascar.

Live Tree Deadwood Bamboo Count Percentage Count Percentage Count Percentage Season 1 2016 180 71.4% 63 25.0% 9 3.6% Season 2 2016 170 59.0% 118 41.0% 0 0.0% Season 3 2016 278 27.2% 597 58.2% 150 14.6% Season 1 2017 219 61.5% 102 28.7% 35 9.8% Season 2 2017 424 63.0% 174 25.9% 75 11.1% Season 3 2017 347 56.9% 194 31.8% 69 11.3%

Table 2.17 Results of the negative binomial regression analysis comparing use of substrates by Tsinjo within each season from January 2016 to December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold.

Comparison of Live Comparison of Live Comparison of Tree and Deadwood Tree and Bamboo Deadwood and Bamboo Season 1 2016 0.009 <0.001 <0.001 Season 2 2016 0.433 N/A N/A Season 3 2016 0.043 0.212 0.005 Season 1 2017 0.175 0.004 0.103 Season 2 2017 0.003 <0.001 0.036 Season 3 2017 0.119 0.002 0.051

Table 2.18 Results of negative binomial regression analysis for seasonal comparison of substrate use for invertebrate foraging by Tsinjo between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold.

Live Tree Deadwood Bamboo Season 1/Season 2 2016 p=0.525 p=0.195 p=0.995 Season 2/Season 3 2016 p=0.376 p=0.013 p=0.266 Season 3 2016/Season 1 2017 p=0.546 p<0.001 p=0.127 Season 1/Season 2 2017 p=0.078 p=0.394 p=0.417 Season 2/Season 3 2017 p=0.390 p=0.870 p=0.907

Table 2.19 Results of negative binomial regression analysis for annual comparison of substrate use for invertebrate foraging by Tsinjo between January 2016 and December 2017 in Torotorofotsy, Madagascar. Significant differences between seasons are highlighted in bold.

Live Tree Deadwood Bamboo 2016/2017 p=0.090 p=0.049 p=0.977

Table 2.20 Monthly preference indices for resource consumption by Tsinjo between January 2016 and December 2017 at Torotorofotsy, Madagascar. Values below 1 indicate non-preference for Canarium seeds in ripe fruit.

Preference Index Value January 2016 0.007 February 2016 0.010 March 2016 0.006 April 2016 0.013 May 2016 0.003 February 2017 0.019 March 2017 0.012 April 2017 0.039 May 2017 0.014 June 2017 0.003

Table 2.21 Seasonal preference indices for resource consumption by Tsinjo at Torotorofotsy, Madagascar. Values below 1 indicate non-preference for Canarium seeds in ripe fruit.

Preference Index Value Hot/Rainy (Season 1) 2016 0.008 Cold/Rainy (Season 2) 2016 0.001 Hot/Dry (Season 3) 2016 0.000 Hot/Rainy (Season 1) 2017 0.015 Cold/Rainy (Season 2) 2017 0.002 Hot/Dry (Season 3) 2017 0.000

Table 2.22 Annual preference indices for resource consumption by Tsinjo at Torotorofotsy, Madagascar. Values below 1 indicate non-preference for Canarium seeds in ripe fruit.

Preference Index Value 2016 0.002 2017 0.006

Figure 2.1 Part A Fruit of Canarium sp.; Part B Feeding traces from aye-ayes in seeds of Canarium sp. Photos by author.

Figure 2.2 Inflorescence of Ravenala madagascariensis. Photo by author.

Figure 2.3 Tsinjo, the focal animal, gnawing into a live tree in Torotorofotsy, Madagascar.

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Figure 2.4 Location of transects, Canarium trees and Ravenala trees in Torotorofotsy, Madagascar. The white border is the home range of Tsinjo.

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Figure 2.5 Part A and Part B New feeding traces in live trees made by aye-ayes in Torotorofotsy, Madagascar. Photos by author.

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Figure 2.6 New feeding traces in deadwood made by an aye-aye in Torotorofotsy, Madagascar. Photo by author.

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Figure 2.7 New feeding traces left in bamboo by an aye-aye in Torotorofotsy, Madagascar. Photo by author.

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Figure 2.8 Old feeding trace left in a live tree by an aye-aye. Photo by author.

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Figure 2.9 Monthly consumption of resources by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017.

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Figure 2.10 Part A Inferior view of a Vakona tree fed on by Tsinjo; Part B Tsinjo on top of a Vakona tree with view of seeds contained within the fronds. Photos by author.

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Figure 2.11 Seasonal consumption of resources by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017.

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Figure 2.13 Monthly use of substrates for invertebrate foraging by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017.

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Figure 2.14 Seasonal use of substrates for invertebrate foraging by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017.

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Figure 2.15 Annual use of substrates for invertebrate foraging by Tsinjo in Torotorofotsy, Madagascar from January 2016 to December 2017.

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Chapter 3 Home range size and seasonal variations in habitat use by aye-ayes (Daubentonia madagascariensis) in Torotorofotsy, Madagascar

In this chapter, I present ranging data on both the male and female aye-aye, Masy and Tsinjo, collected over a period of 24 months. I establish a home range size for both individuals using the Minimum Convex Polygon method. I also examin how seasonal shifts in resource availability change the ranging behavior of the female using the Kernel

Density Estimates method. These data are used to establish the home ranges of free- ranging aye-ayes and test whether ranges change in a predictable, seasonal manner.

Introduction

Aye-ayes (Daubentonia madagascariensis) have the largest home ranges of any extant lemur species (Sterling 1993, 1994a; Randimbiharinirina et al. 2018). The first study to examine aye-aye home ranges was conducted on the island of Nosy Mangabe

(Sterling 1993, 1994a). Sterling (1993, 1994a) found that female territories were between 30-40 ha and male home ranges were between 125-250 ha. A more recent study in the disturbed forest of Kianjavato in southeastern Madagascar found that a single female’s home range was 98 ha and male home ranges were between 821 ha and 973 ha

(Randimbiharinirina et al. 2018). As discussed in Chapter 2, the aye-ayes in both of these forests are adapting to different selective pressures than aye-ayes in a undisturbed forest.

On Nosy Mangabe, aye-ayes are not naturally occurring, lack predators, and may be over-populated. These factors have resulted in aye-ayes on the island consuming more variety of resources than the aye-ayes at Torotorofotsy (see Chapter 2). In Kianjavato,

113 the aye-ayes are adapted to a heavily disturbed forest which again results in a diet that includes resources that are not consumed by aye-ayes in Torotorofotsy. Since home range size is related to an organism’s diet (McNab 1963), and aye-ayes from these other studies have a different dietary composition than the aye-aye in Torotorofotsy, the previous data on home range size may not be applicable to our understanding of the ecology of naturally occurring populations. That is, aye-ayes in a undisturbed forest likely need larger habitat sizes given their strong reliance on invertebrates.

Home Range, Body Size and Diet

Diet and body size are correlated with the size of an organism’s territory (McNab

1963). More specifically, as body size increases, resources should become larger, dietary diversity will broaden and home range size will ultimately expand (McNab 1963). As an organism’s body size increases, the size of their resources should also increase to make sure sufficient energy is consumed per each unit of food (McNab 1963). Normally, we would not expect a large-bodied primate (over 500g) to sustain itself on insects, which are typically small, because the energy gained from an average insect should not be sufficient to offset the cost of acquiring them (Kay 1975). If a large-bodied organism is able to persist on invertebrates, it has to be very efficient in its foraging for them (McNab

1963; Gaulin 1979). Primates bigger than 500 g should consume fruits or leaves in greater quantities instead of invertebrates (Kay 1975). In addition to having larger food items, large-bodied organisms will also typically increase their home range size (McNab

1963). By having bigger home ranges, a large-bodied organism is more likely to locate sufficient quantities of resources within its territory to sustain itself (McNab 1963). In fact, primates with large territories often have diets that incorporate significant amounts

114 of fruit (frugivores) or invertebrates (omnivores) because these resources tend to be highly dispersed and unpredictable, thus necessitating a greater area to procure sufficient food items (McNab 1963; Milton and May 1976; Janson and Chapman 1999). What is more, large-bodied organisms with big home ranges will typically diversify their diet in an effort to locate a variety of resources throughout their habitat and improve foraging efficiency (McNab 1963).

In general, most primates exploit an array of resource types, consuming some combination of leaves, fruit, insects, gums or other foods (Garber 1987; Sussman 1987;

Chapman and Chapman 1990). However, one type of resource is usually consumed in greater quantities than others (Garber 1987; Sussman 1987). The distribution and availability of this resource type will often directly influence a primate’s ranging behavior (Oates 1987; Janson and Chapman 1999; Buzzard 2006). Folivores tend to have small home range sizes because resources are easily obtained and ubiquitous (Janson and

Chapman 1999). For example, black and white colobus monkey (Colobus guereza) home ranges are approximately 12 ha, which is comparatively small given their body size

(Chapman and Pavelka 2005). Alternatively, with food items such as invertebrates or fruit, which are not evenly distributed spatially or temporally in the environment, i.e. patchy, primates will typically necessitate large home ranges to locate sufficient resources to maintain homeostasis (Janson and Chapman 1999). For example, the frugivorous collared mangabey (Cercocebus torquatus), with a body size similar to black and white colobus, has a home range size of 247 ha (Mitani 1989). Of course, while primate dietary diversity should expand with home range (McNab 1963), the availability of resources is seasonally dependent based on climatic fluctuations (van Schaik et al.

115

1993). This means that dietary inclusion or exclusion will likely change with seasonal changes in resource abundance.

Seasonality in the Tropics

Most primates live in the tropics where resources vary seasonally (van Schaik et al. 1993; van Schaik and Pfannes 2005; Myneni et al. 2007). Though tropical rainforests do not experience dramatic climatic fluctuations, there are significant differences in rainfall and sunlight that impact floral productivity (MacArthur 1972; van Schaik and

Pfannes 2005). Seasons in the tropics are differentiated by annual peaks in rainfall or irradiance (MacArthur 1972; van Schaik and Pfannes 2005). In tropical environments, production of young leaves (flushing), flowers and fruit vary with seasonal fluctuations in rainfall and sunlight (van Schaik et al. 1993; van Schaik and Pfannes 2005). Though there is some temporal association between flushing, flowering and fruiting, seasonal timing for each phase can be evaluated separately (van Schaik et al. 1993; van Schaik and

Pfannes 2005).

Seasonal increases in rainfall after droughts are associated with both flushing and, to a lesser extent, flowering of plants (van Schaik et al. 1993; van Schaik and Pfannes

2005). This means that production of young leaves and flowers are strongly associated with the change from dry to rainy seasons (van Schaik and Pfannes 2005). When a distinction is made between dehiscent fruits and succulent fruits, seasonal peaks in abundance have been recognized (van Schaik and Pfannes 2005). Succulent fruits associated with tropical environments are typically abundant during rainy seasons (van

Schaik and Pfannes 2005). Therefore, the abundance of some resources, such as young leaves, nectar and ripe succulent fruit, peak during the hot, rainy season. Because

116 tropical environments exhibit relatively stable climatic conditions, these foods are rarely absent from tropical forests, even during less productive seasons (Wright 1999; 2006).

However, typically there are seasonal peaks in floral production which can result in a patchy distribution of flowers in some habitats.

Temporal patchiness, the seasonal fluctuation in resource availability, is one way that foods can vary within an environment. Resources can also be spatially patchy, occurring in unevenly distributed clumps (Charles-Dominique 1995). If resources are spatially patchy, a primate must remember the location of these items to successfully reach the resource before its competitors (Temerin and Cant 1983; Charles-Dominque

1995). Some resources, such as succulent fruit, can be both spatially and temporally patchy. Others, such as young leaves, are usually temporally but not spatially restrictive.

The spatial patchiness of fruits and not of leaves is why there are differences in the home range sizes of frugivores compared to folivores (Milton and May 1976; Janson and

Chapman 1999). However, regardless of the predominant type of resource consumed, primates will experience some temporal and/or spatial patchiness to their food supply and will ultimately need to adapt accordingly.

Optimal Foraging Theory

Optimal foraging theory (OFT) predicts that an organism will forage in the most economical fashion (Emlen 1966; MacArthur and Pianka 1966). Each organism has its own energetic costs of obtaining resources, including time spent searching, handling, pursuing, capturing and consuming a food item (Pyke 1984; Stephens and Krebs 1986).

According to OFT, a primate should select the resources that maximize their energetic gain and minimize their costs (Pyke 1984; Stephens and Krebs 1986). To that end,

117 organisms should expand their dietary breadth as the availability of resources decreases

(Emien 1966; MacArthur and Pianka 1966). Since most primates are omnivorous, it is difficult to apply OFT because each resource will have different energetic costs and benefits (Clutton-Brock 1977; Garber 1987). However, primates will still display some optimal foraging behaviors (Garber 1987; Sayers et al. 2010). For example, as seasons shift and resource availability changes, Himalayan langurs (Semnopithecus entellus) broaden their diet during periods of food scarcity (Sayer et al. 2010).

OFT originally predicted that all organisms should have similar optimal behaviors

(Emien 1966; MacArthur and Pianka 1966). However, optimal behaviors will differ depending on the life history strategies of an individual organism (Wrangham 1980;

Hixon 1982). Therefore, organisms are said to adopt one of two different optimal strategies: 1) time minimizer or 2) energy maximizer (Schoener 1971, 1983; Hixon

1982). A time minimizer will try to consume their required energy as quickly as possible so as to allow time for other behaviors (Schoener 1971; Hixon 1982). For example, squirrel monkeys (Saimiri sciureus) experienced seasonal changes to their dietary composition, but did not change their home range size or daily travel lengths (Stone

2007). Stone (2007) suggested the squirrel monkeys were attempting to consume enough energy to perform their regular daily activities and not expend additional energy on resource acquisition. On the other hand, an energy maximizer will devote as much time as possible to consuming resources, thus optimizing energetic input to meet any metabolic demands (Schoener 1971; Hixon 1982). For example, moustached (Saguinus mystax) and saddle-back tamarins (S. fuscicollis) will remember which trees have low food rewards and avoid them (Garber 1987). Their travel distances will increase, but

118 they will maximize their energy gain by feeding at trees that provide a higher energetic yield (Garber 1987). The way a primate responds to seasonal fluctuations in resource abundance will largely depend on which strategy it adopts.

Changes in Ranging Behavior

The most noticeable behavioral response of primates to food patchiness is a change in their ranging patterns in response to fluctuating availability of the main resource type they consume (Janson and Chapman 1999). Altering daily path lengths and home range size allows primates to adjust energy expenditure to compensate for changes in food availability. Primates have multiple ranging behavioral responses to changes in resource availability (Oates 1987; Hemingway and Bynam 2005). Some primates will increase travel distances in search of preferred resources when availability of these items is high, bypassing non-preferred foods (Stephens et al. 1986). For example, western gorillas (Gorilla gorilla gorilla) will increase their daily path length in order to consume more of their preferred resource (fruit) when it is available in large quantities (Doran-

Sheehy et al. 2004). Propithecus verreauxi also increase their daily path length to consume more fruits and flowers when these resources are at their peak availability

(Richard 1977).

Alternatively, some primates will increase travel when preferred foods are scarce in order to locate sufficient resources (Hemingway and Bynum 2005). For example, spectral tarsiers (Tarsius spectrum) will increase their nightly path length during periods of low abundance of their preferred resource, a practice that helps them through lean times (Gursky 2000). Similarly, several lemur species, such as Lemur catta (Sauther

1998) and Hapalemur griseus (Overdorff et al. 1997), are known to increase travel times

119 during periods of preferred resource scarcity (Hemingway and Bynum 2005; Schmid and

Kappeler 2005). This increase in travel may be due to a scarcity of preferred foods within the primate’s current home range (Hemingway and Bynum 2005). Ultimately, by increasing daily path length, these primates will simultaneously increase home range size to locate additional types of resources (Hemingway and Bynum 2005).

Other primates have consistent ranging behavior throughout the year. Squirrel monkeys maintain their daily travel distance by foraging on high-density, available resources, whether they are preferred or not (Stone 2007). Though lemurs have a variety of behavioral adaptations for coping with seasonality, lemurs do not maintain consistent ranging behavior throughout the year (Wright 1999, 2006). These three behavioral responses (increasing ranging, decreasing ranging and maintaining a consistent range) demonstrate how primates alter their ranging behavior as food patchiness fluctuates; though behavioral responses are varied, they are strongly tied to resource consumption

(Hemingway and Bynum 2005).

Madagascar Seasonality

Malagasy forests are more asynchronous in production of leaves, flowers and fruit than other topical forests (Wright 1999). In Madagascar, there are three distinct seasons: hot/rainy (January to mid-May), cold/rainy (mid-May to mid-September) and hot/dry

(mid-September to December) (Sterling 1993, 1994; Wright 1999, 2006; Vasey 2005).

Floral resource peaks in Madagascar can be unpredictable (Wright 1999). For example,

Canarium sp., a genus of tropical and subtropical trees with approximately 32 species native to Madagascar (Daly et al. 2015), produces fruits on an alternate year cycle

(Overdorff 1993; Hemingway 1995; Wright 2006). Dry periods in Madagascar can last

120 upwards of six months, a dramatic enough climatic shift causing some foods, such as

Canarium fruit, to be unavailable for extended periods (Wright 1999, 2006). This means that unlike some primates that consume one resource category throughout the year (e.g.

Cercopithecus diana, Kane 2012), few lemur species can rely primarily on one food type year-round (Wright 2006). Therefore, it has been argued that most lemurs have evolved morphological and/or behavioral specializations to cope with extensive periods of resource scarcity (Overdorff 1993; Wright 1999, 2006).

Aye-aye Home Range and Diet

As described in chapter 2, two resources comprise the diet of an aye-aye in

Torotorofotsy: invertebrates and Canarium seeds in ripe fruit. Since invertebrates and

Canarium fruit are considered highly dispersed and unpredictable, and because aye-ayes are relatively large-bodied (2.5 kg), aye-ayes should have large home ranges in order to procure enough of either or both of these resources (Milton and May 1976; Janson and

Chapman 1999). Indeed, aye-ayes have the largest home ranges of any extant lemur species. On the island of Nosy Mangabe males range between 125 ha and 215 ha while females have home ranges approximately 30 ha to 40 ha (Sterling 1993, 1994a). In

Kianjavato, male home ranges were between 822 ha and 974 ha and a female territory was at least 98 ha (Randimbiharinirina et al. 2018).

Surprisingly, aye-ayes do not appear to follow other expectations for a large- bodied organism (McNab 1963). For instance, large-bodied predators with big home ranges typically have a diverse diet and include larger food items as a way of improving foraging efficiency (McNab 1963). The aye-ayes on Nosy Mangabe have some dietary diversity, including Canarium seeds in ripe fruit and on the forest floor, Ravenala nectar,

121 larvae and cankerous growths on trees (Sterling 1993, 1994a). The aye-ayes in

Kianjavato have larger home ranges than those on Nosy Mangabe, but less dietary variety, consuming Canarium seeds in ripe fruit, Ravenala nectar and invertebrates

(Randimbiharinirina et al. 2018). In Torotorofotsy, two items comprise 99% of the diet,

Canarium seeds in ripe fruit and invertebrates (see Chapter 2). Not only is the dietary breadth relatively limited, but the main resource item, invertebrates, remains a small food unit.

As discussed previously, Kay’s threshold predicts that aye-ayes should not be able to sustain themselves on invertebrates (Kay 1975). Yet it appears that within

Torotorofotsy, the female aye-aye was preferentially and often exclusively consuming invertebrates. In order for an animal as large as the aye-aye to mainly feed on invertebrates, it has to be highly efficient at foraging for this resource (McNab 1963;

Gaulin 1979). Optimal foraging is at least partially a function of home range use (Emien

1966; MacArthur and Pianka 1966) and organisms should adjust their home range size to either minimize their time feeding or maximize their energetic gains (Schoener 1971;

Hixon 1982). The two previous studies on aye-aye home range sizes yielded drastically different results (Sterling 1993, 1994a; Randimbiharinirina et al. 2018). Additionally, neither study examined how seasonality influences aye-ayes ranging behaviors.

Therefore, it is important to examine seasonal and annual habitat use within

Torotorofotsy to interpret which optimization strategy aye-ayes employ.

Possible Aye-aye Strategies

Based on findings in Chapter 2, invertebrates are the resource most likely to influence a female aye-aye’s ranging behavior because they are preferred. Invertebrates

122 are available year-round (Sterling 1993, 1994a; Randimbiharinirina et al. 2018; see

Chapter 2) and appear to be evenly distributed throughout the environment in a undisturbed forest (Isbell 1991; Sefczek et al. 2017). However, as beetles only oviposit upwards of ten eggs within a single depositing site (Hanks 1999), invertebrates would likely represent solitary food items or at best a small patch. Therefore, the large-bodied aye-aye most likely consumes large quantities of invertebrates to meet its metabolic needs and would therefore need a large home range to locate sufficient quantities of this resource (Milton and May 1976). Additionally, since this resource is widely distributed at all times of year, it is likely that a solitary aye-aye maintains a consistently large home range regardless of season (Milton and May 1976). In this scenario, aye-ayes would be energy maximizers as they would constantly be searching for and consuming invertebrates to meet their energetic demands (Schoener 1971; Hixon 1982).

Alternatively, during the hot/rainy seasons (season 1) the aye-aye in

Torotorofotsy consumed more Canarium seeds from ripe fruit than invertebrates (see

Chapter 2). Canarium seeds are known to be unpredictable in availability, with trees producing fruits on an alternate year cycle and having extended periods of unavailability

(Overdorff 1993; Hemingway 1995; Wright 1999, 2006). However, Canarium trees also produce thousands of fruits in a single fruiting season (see Chapter 2) meaning they are a large patch resource for aye-ayes to exploit. Since aye-ayes consume large quantities of

Canarium seeds during the hot/rainy season (season 1), they may not need to maintain large home ranges throughout the year. Instead, aye-ayes may adjust home range as shifts in Canarium seed availability occurs (Olupot et al. 1997). As Canarium seeds are not the preferred food, aye-ayes would not be expected to increase home range size and

123 bypass invertebrates for this resource (Stephens et al. 1986). Instead, aye-ayes will likely reduce their territory because they can consume multiple seeds from a single tree, decreasing the necessity of traveling greater distances in search of additional resources

(Norscia et al. 2006). During periods of decreased Canarium fruit availability and increased invertebrate consumption, such as the hot/dry season (season 3), aye-ayes would likely increase their travel distances, and ultimately their overall home range size

(Wright 1999, 2006; Hemingway and Bynum 2005; Schmid and Kappeler 2005; Vasey

2005). In this scenario, when Canarium fruit is available, aye-ayes would likely be time minimizers, consuming large quantities of Canarium seeds in ripe fruit when available and spending less time foraging for other resources (Schoener 1971; Hixon 1982). Then, when Canarium fruits are unavailable, aye-ayes become energy maximizers as they focus on invertebrate consumption (Schoener 1971; Hixon 1982).

Though Chapter 2 has shown that aye-ayes exclusively eat invertebrates, their preferred resource, for the majority of a year, it is not entirely clear how aye-ayes are able to sustain themselves on such a small-packaged food item. Without relating feeding data to ranging behavior, we cannot hope to understand how aye-ayes are able to violate

Kay’s threshold. As previously discussed, home range size is correlated with diet

(McNab 1963). The diets of aye-ayes in Kianjavato and Nosy Mangabe included more types of resources (i.e. Ravenala madagascariensis nectar and cankerous growths on trees) than the diet of the Torotorofotsy aye-aye, as described in Chapter 2 (Sterling 1993,

1994a; Randimbiharinirina et al. 2018). Additionally, invertebrate feeding at Kianjavato and Nosy Mangabe was more frequent at deadwood substrates than live trees (Sterling

1993, 1994a; Randimbiharinirina et al. 2018). If invertebrates are more clumped in

124 deadwood than in live trees as has been reported elsewhere (Isbell 1991; Sterling 1993,

1994a; Hanks 1999), and clumped resources cause differential optimization of feeding behaviors (Emien 1966; MacArthur and Pianka 1966), then home range size and habitat use of these aye-ayes might not be reflective of behaviors in a pristine environment.

Determining how aye-ayes in a undisturbed forest utilize their habitat seasonally and annually can help us (1) understand the aye-aye’s optimization strategy and (2) elucidate how aye-ayes sustain themselves on invertebrates despite their large body size.

This study

I collected home range data on two aye-ayes in a undisturbed forest over a two- year period. These data provide the first estimates for home range size and use of free- ranging individuals in a undisturbed forest. To date, no study has examined the seasonal ranging patterns of a free-ranging aye-aye. Therefore, my goals were to (1) determine the home range size of a male and female aye-aye in a undisturbed forest and (2) examine the relationship between diet and ranging behavior seasonally and annually for the female aye-aye. I do this by comparing the locations of each resource the aye-aye consumed to the approximated habitat use of the aye-aye each season and each year. My null hypothesis is that there will be no difference in the seasonal and annual areas of the forest the aye-aye uses. Given that invertebrates are the preferred resources and are ubiquitously distributed throughout the environment in small patches (see Chapter 2), my alternative hypothesis is that aye-ayes will alter their home range use seasonally and annually. I predicted:

1) Aye-ayes will have larger home ranges in undisturbed forest than estimates from

previous studies at Nosy Mangabe and Kianjavato

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2) Seasonal and annual habitat use by the aye-aye will be related to invertebrate, not

Canarium seed, feeding.

3) Aye-ayes will use different portions of their home range each season and year.

Materials and Methods

Study Sites

I conducted research from January 2016 to December 2017 in Torotorofotsy (18º

46’S and 48º 25’ E), Madagascar. Torotorofotsy is a natural wetland about 1100 ha in size, is adjacent to Mantadia National Park, and roughly 10 km northwest of the town

Andasibe. This forest is the most intact wetland in the Andasibe-Mantadia-Zahamena eastern rainforest corridor, containing high levels of biodiversity (Dolch et al. 2004; Peck

2004; Wright et al. 2008). Within Torotorofotsy there are three collared aye-ayes: one adult male, one adult female and one subadult male. These aye-ayes are outfitted with radio-collars as part of Madagascar Biodiversity Partnership’s aye-aye research project

(Sefczek et al. 2017). Because the subadult male will only range within his mother’s territory, this research focuses on the ranging behaviors of the adult male, Masy, and the adult female, Tsinjo. Masy ranged beyond the boundaries of Torotorofotsy into habitat I did not have permission to access. Therefore, his data will be used only to estimate total home range size. The analysis of seasonal and annual variations in home range size and resource use will focus on the behaviors of Tsinjo.

Based on average daily temperature and monthly rainfall, there are three distinguishable seasons in Madagascar (Sterling 1993). Season 1, also known as the hot/rainy season, extends between January and mid-May. Season 2, referred to as the cold/rainy season, extends from mid-May to mid-September. Season 3, the hot/dry season, extends from mid-September to the end of December (Sterling 1993; Wright

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1999; Vasey 2005). These three seasonal designations were used to examine the effects of seasonality on aye-aye ranging behavior.

GPS Data Collection

In order to collect continual ranging data, I conducted six-hour follows from

18:00-0:00 on Mondays and Wednesdays and from 0:00-6:00 on Tuesdays and

Thursdays. Monday and Wednesday follows commenced at the sleeping site of the animal. During Tuesday and Thursday follows, I located the focal animal using the radio telemetry system. These follows ended when the animal reached its nest and did not move for an hour. I used the methodology outlined by Sterling (1993) with three researchers, myself and two Malagasy field assistants, following a focal animal. One researcher maintained light contact, defined as keeping the aye-aye within the beam from a head lamp but not closer than five meters. The other two participants positioned themselves to follow the animal when it ventured in a new direction (Sterling 1993).

During night follows, I collected data using instantaneous focal-animal sampling

(Altmann 1974). That is, every 15 minutes I recorded the GPS location of the animal and the behavior the animal was performing. Behaviors included resting, traveling, feeding, and self-grooming. I also recorded the GPS location of every feeding event and the food item consumed. Because Masy was frequently out of the Torotorofotsy forest, the locations of daytime nest sites were opportunistically recorded to help estimate home range size. I also used unpublished data collected between July 2014 and December

2015 to estimate Masy’s home range. By recording GPS points during night follows and at daytime nest locations, I estimated the home range size of both aye-ayes (Muller 1999;

Dammhahn and Kappeler 2005; Lahann 2008; Biebouw 2009). These data were used to

127 create home range maps for the male and female aye-ayes. In addition to the overall home range size of both aye-ayes, I created seasonal and annual home range maps for the female, Tsinjo. Annual home ranges simply consisted of the GPS locations collected over the course of each year. Seasonal home ranges were compiled by examining the

GPS locations for the three seasons (1: hot/rainy, 2: cold/rainy, 3: hot/dry), each of which contained approximately four months of data points. These seasonal and annual ranges were then compared to the seasonal and annual locations of feeding sites for each resource.

Data Analysis

I performed spatial analyses for both aye-ayes using the Home Range Tools

(HRT) add-in for ArcGIS 10.2 (Rodgers et al. 2015). I used the Multiple Convex

Polygon (MCP) method to estimate home range sizes for both the female and male aye- aye. MCPs are created by using the most peripheral GPS points collected to create a polygon (Mohr 1947). While home range sizes with MCP are usually determined by removing the 5% of data points farthest from the mean, I retained 100% of data points to identify the maximum home range size for both individuals (White and Garrott 1990).

In addition, I used the Kernel Density Estimation method (KDE), with an adaptive kernel and least squares cross validation for bandwidth selection, to assess seasonal and annual habitat use by Tsinjo across the two-year study. KDE uses the data points to make inferences about the probable home range size. This can potentially result in larger ranges than the MCP value because of the smoothing effect of the bandwidth; however, size estimations are still statistically robust (Worton 1989). I determined utilization distribution by setting isopleth levels at 95%, 50% and 10%. By doing this, I could

128 examine where the highest frequencies of habitat use, i.e. 10% isopleth level, occurred each season. This allowed me to determine if there were any seasonal patterns to

Tsinjo’s movement. Typically, repetitive data points are eliminated from home range studies to fix autocorrelation problems (Swihart and Slade 1985a, 1985b). However, to improve accuracy of density estimates of points, independent observations were not necessary (Swihart and Slade 1997; DeSolla et al. 1999). Instead, I used the adaptive method with least-squares cross validation (Worton 1989).

Finally, I used the grid-cell method (GCM), running global spatial autocorrelation analyses (α=0.05) and creating local hotspot maps, to determine if areas of the home range used seasonally and annually were significantly clustered. GCM works by superimposing a grid over an area and numerating the number of times an animal enters one of the cells on the grid (Stark et al. 2017). Based on GCM for orangutan home ranges (Singleton and van Schaik 2001), I used 100 m x 100 m cell measurements for the fishnet on hotspot maps to avoid over- or under-estimation of range sizes. GCM maps produce high-high and low-low clusters indicating areas high or low use, as well as high- low and low-high outliers, where data point frequencies within the cell do not match the surrounding areas. The GCM allowed me to estimate habitat utilization seasonally and annually.

Results

I collected 900 GPS points for Tsinjo and 132 GPS points for Masy (Table 3.1).

Over half of Tsinjo’s GPS points (453) were taken during feeding events. While all of

Tsinjo’s GPS points were collected between 2016 and 2017, most of Masy’s GPS points were collected in 2014 (54) and 2015 (45). Only 37 of the 132 GPS points for Masy were collected between 2016 and 2017. Thus, Masy’s data were only considered for the 129 overall home range estimates but could not be used for annual and seasonal breakdowns of home range use.

Overall Home Range Size

Table 3.2 presents and Figure 3.1 displays the 100% MCP home range estimates for Tsinjo, 713.6 ha, and Masy, 1587.5 ha. This follows the trend of previous aye-aye studies with the male home range being larger than the female (Sterling 1993, 1994a;

Randimbiharinirina et al. 2018). This is expected given the aye-ayes dispersed polygynous social system (Sterling 1993; Sterling and Richard 1995). The ranges for both the male and female are much greater than those reported from Nosy Mangabe

(Sterling 1993, 1994a) or Kianjavato (Randimbiharinirina et al. 2018).

Table 3.2 also presents and Figure 3.2 depicts the KDE home range estimates for both aye-ayes. Tsinjo’s 95% isopleth was calculated at 474.8 ha, her 50% was 223.1 ha, and her 10% was 11.8 ha over the course of the study. This means that although the majority of Tsinjo’s activities over the course of the study occurred in an 11.8 ha territory, she occupied a much larger home range. It is important to point out that while the KDE method typically produces larger home ranges than those estimated using the

MCP method, Tsinjo’s 95% isopleth for the overall KDE range was smaller. This is likely because MCP only considers the furthest GPS points when making its polygon while KDE evaluates based on frequency of points in a given area. During 2016,

Tsinjo’s home ranges were smaller and the GPS points were more concentrated. This probably skewed the data, leading to a smaller estimated home range size. The difference in size between Tsinjo’s MCP and KDE home range will be evaluated further in the discussion.

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Masy’s KDE was larger than Tsinjo’s for both 95% and 10% isopleths (1020.5 ha and 23.2 ha, respectively), however the 50% isopleth was only 179.1 ha (Figure 3.2).

While Masy’s home ranges are larger than Tsinjo’s, it is likely his MCP and KDE values are smaller than his actual home range. Most of Masy’s data points were collected when he ventured into the Torotorofotsy study site, but he spent the majority of the study outside of this forest and in Mantadia National Park or further east near the mining site.

The GPS points are only from a small portion of Masy’s total territory; therefore, his

MCP and KDE ranges are likely even bigger than I found.

Annual Home Range Sizes

To explore annual changes in habitat use, I compared Tsinjo’s data points from

2016 and 2017. Table 3.3 presents the seasonal and annual number of GPS points collected for Tsinjo and Table 3.4 displays the number of GPS points taken for various feeding events each season and year. I collected 426 GPS points in 2016 and 474 GPS points in 2017 (Table 3.3); of these points, 227 were invertebrate feeding sites in 2016 and 195 in 2017 (Table 3.4). This means that over 50% of the GPS points in 2016 and just over 40% of the GPS points in 2017 were from invertebrate feeding. Though the percentage of data points for feeding decreased in 2017, feeding was still the most frequent behavior recorded when taken GPS location. This is to be expected as all GPS points of feeding locations were recorded but all other GPS points were taken in 15 minute intervals.

Table 3.5 presents and Figures 3.3A and 3.4A display the annual KDE estimated home range of Tsinjo in 2016 and 2017. In 2016, the 95% isopleth covered 407.1 ha of

Tsinjo’s territory, while in 2017 the 95% isopleth incorporated 775.3 ha (Table 3.5,

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Figure 3.3A, Figure 3.4A). As seen in Figures 3.5A and 3.6A, I then overlaid annual feeding points on the KDE ranges to display what type of resources was being consumed and from which part of the forest it was being removed. This permitted me to assess whether there was a pattern to aye-aye’s habitat use. Feeding on invertebrates occurs throughout the home range, with a high concentration in the 10% isopleth areas (Figures

3.5A and 3.6A). Feeding on Canarium seeds was absent in the 10% isopleth, but present in the 50% and 95% isopleths for 2016 (Figure 3.5A). This means that the most frequently used areas were not concentrated on Canarium feeding but rather invertebrate feeding. In 2017, invertebrate feeding was again widespread throughout the habitat, with a heavy concentration in the 10% and 50% isopleth areas (Figure 3.6A). Canarium feeding was very common in the 10% isopleth region (Figure 3.6A).

The results from the annuals KDE maps suggests that in 2016 the Canarium seed feeding was less of a focus than in 2017, when Canarium feeding sites were more prevalent in the most frequently used area. Invertebrate feeding seems to occur throughout the home range, suggesting invertebrates are ubiquitous and widely dispersed.

Their heavy concentration in the 10% isopleth ranges for both 2016 and 2017 suggests that aye-ayes spend a large portion of their time in pursuit of invertebrates within a relatively confined vicinity.

Seasonal Home Range Sizes

To explore seasonal changes in habitat use, I compared Tsinjo’s data points from each of the three seasons in 2016 and 2017. Table 3.3 presents the seasonal and annual number of GPS points collected for Tsinjo and Table 3.4 displays the number of GPS points taken for various feeding events each season and year. The most GPS points

132 collected were during season 2 of 2017 (213) followed by season 3 of 2016 (181; Table

3.3). While the majority of data points were taken during feeding behaviors, there was an increase in GPS points taken during traveling in season 2 and season 3 of 2017 (Table

3.4). This suggests that Tsinjo was spending more time moving throughout her environment as the study progressed. As discussed below and in Chapter 5, this is likely due to the development of her offspring.

Table 3.6 presents and Figures 3.3 B through D and 3.4 B through D display the seasonal KDE estimated home ranges of Tsinjo. The hot/rainy season (season 1) of 2017 had the biggest 95% isopleth (527.0 ha; Table 3.6; Figure 3.4 B). The smallest 95% isopleth occurred during the hot/rainy season (season 1) of 2016 (170.6 ha; Table 3.6;

Figure 3.3B). In fact, with the exception of the 95% isopleth for season 2 of 2017 and season 3 of 2016, the home range estimates at all levels (95%, 50%, and 10%) of 2017 were larger than those of 2016 (Table 3.6). This suggests that Tsinjo had a bigger home range in 2017 than in 2016. This will be discussed in more detail later.

In figures 3.5 B through D and 3.6 B through D, I overlaid the seasonal feeding points on the respective seasonal KDE ranges to display what type of resources were being consumed and from which part of the forest they were being removed. This helped me explore if there was a seasonal pattern to aye-aye’s habitat use. In all seasonal maps, invertebrate feeding locations occurred throughout the home range, with high concentrations in the most frequently used areas of the habitat (i.e. the 10% isopleth).

Canarium feeding was absent in the hot/dry season (season 3) of both 2016 and 2017

(Figure 3.5 D and 3.6 D), which aligns with feeding behaviors described in Chapter 2.

Canarium feeding did occur in the cold/rainy seasons (season 2) of 2016 and 2017, but

133 was only in the 95% isopleth and 50% isopleth respectively (Figures 3.5 C and 3.6 C).

Canarium feeding mostly occurred during the hot/rainy seasons (season 1). In 2016,

Canarium feeding was infrequent in the most frequently used parts of the forest (10% and

50% isopleths; Figure 3.5 B), but in 2017 the majority of the Canarium feeding occurred within the 50% isopleths (Figure 3.6 B).

As seen in the annual KDE range maps, invertebrate feeding occurs every season and throughout the home range. It appears that in the hot/rainy seasons (season 1) invertebrate feeding is more concentrated in Tsinjo’s most frequently used areas (10% and 50% isopleths), but becomes more dispersed in the subsequent two seasons each year. Season 1 is also when the Canarium feeding is most frequent. Canarium feeding is prevalent in the 50% isopleth ranges during this season, particularly in 2017 (Figure 3.6

B). This could indicate that during the hot/rainy season (season 1) Tsinjo is traveling less and spending more time in the vicinity of Canarium trees. This behavior was previously suggested by Sefczek and colleagues (2012) when examining aye-aye traces in

Ranomafana National Park. Yet, invertebrate feeding locations are constantly heavily concentrated in the 10% isopleths for each season. Therefore, it seems more likely that, as with the results from the annual KDE ranges, aye-ayes spend a large portion of their time in pursuit of invertebrates within a relatively restricted area.

Spatial Analysis of Home Range Use

Figures 3.7A and 3.8A depict the most frequently used areas of Tsinjo’s habitat in

2016 and 2017, respectively. The global spatial autocorrelation showed that the GPS points were significantly clustered in both 2016 (Moran’s Index: 0.350, p<0.001) and

2017 (Moran’s Index: 0.354, p<0.001).

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Figures 3.7B (season 1), 3.7C (season 2) and 3.7D (season 3) display the most frequently used areas of Tsinjo’s habitat each season in 2016. Global spatial autocorrelations for season 1 of 2016 (Moran’s Index: 0.310, p<0.001), season 2 of 2016

(Moran’s Index: 0.161, p<0.001) and season 3 of 2016 (Moran’s Index: 0.333, p<0.001) were all significantly clustered.

Figure 3.8B (season 1), 3.8C (season 2) and 3.8D (season 3) show the most frequently used areas of Tsinjo’s habitat each season in 2017. Global spatial autocorrelations for season 1 of 2017 (Moran’s Index: 0.212, p<0.001), season 2 of 2017

(Moran’s Index: 0.398, p<0.001) and season 3 of 2017 (Moran’s Index: 0.189, p<0.001) were all significantly clustered.

For the seasonal and annual maps of 2016 and 2017, the clustering correlates with the 10% and 50% isopleths of the KDE maps (Figures 3.2 and 3.4). High percentages of habitat use by Tsinjo are represented by the 10% and 50% areas of the KDE maps. These areas were used more than any other part of the home range during the respective seasons.

Discussion

Aye-ayes are known to have large territories, but the home range size and associated diets vary greatly. Sterling (1993, 1994a) found that female aye-ayes on Nosy

Mangabe had home ranges ranging between 30 and 40 ha while males home ranges varied between 125 and 250 ha. Four resources comprise over 90% of the diet for these aye-ayes: Canarium seeds, Ravenala madagascariensis nectar, insect larvae and cankerous growths on trees (Sterling 1993, 1994a). Canarium seeds and Ravenala nectar are the most frequently used resource by aye-ayes on Nosy Mangabe while invertebrates are only eaten when these resources are unavailable (Sterling 1993, 1994a; Sterling and 135

McCreless 2006). In the disturbed southeastern forest of Kianjavato, the territory of one female was 90 ha and the territories of two males were 821 ha and 973 ha, respectively

(Randimbiharinirina et al. 2018). The aye-ayes in Kianjavato ate three types of resources: Canarium seeds, Ravenala nectar and invertebrates (Randimbiharinirina et al.

2018). However, unlike on Nosy Mangabe, invertebrates were eaten in greater quantity than either of the other two resources (Randimbiharinirina et al. 2018). My findings in

Chapter 2 reveal that an aye-aye in undisturbed forest decreased its dietary breadth even further, with Canarium seeds in ripe fruit and invertebrates comprising over 99% of the diet. The home ranges are also very different, with a male covering at least 1587.5 ha and a female occupying a 713.6 ha territory. Typically, large-bodied organisms are expected to (a) not rely predominantly on invertebrates and (b) increase dietary breadth as home range expands (McNab 1963; Kay 1975). However, as aye-aye territory size increases, diet appears to narrow and become more focused on invertebrates.

Home Range Size

My first goal was to determine the home range size of a male and female aye-aye in undisturbed forest. I predicted that the home range of aye-ayes in undisturbed forest would be larger than previous estimates that were based on aye-ayes from Nosy Mangabe and Kianjavato. The male aye-aye’s (Masy) home range was 1587.5 ha based on the

100% MCP, and 1020.5 ha based on the 95% KDE. Since Masy ranged beyond our permitted research area, I was not able to collect consistent GPS points throughout his territory; it is therefore possible his home range is even bigger than that reported here.

The female aye-aye’s home range was 713.6 ha based on the 100% MCP, and 474.8 ha

136 based on the 95% isopleth for KDE. Thus, my prediction that aye-ayes in Torotorofotsy would have the largest home range size yet reported is supported.

The size difference between the male and female home range is likely due to aye- ayes having a dispersed polygyny, or noyau, social system (Petter 1977; Sterling 1993).

In a dispersed polygyny system, female dispersal is based on resource availability, while males attempt to monopolize reproductive opportunities by overlapping with multiple females (Dammhahn and Kappeler 2009). Therefore, females will have smaller, non- overlapping home ranges so as to defend resources from other females, while males will have larger territories that overlap with home ranges of other individuals in order to increase rates of encounters with estrous females (Dammhahn and Kappeler 2009). In

Torotorofotsy, Masy traveled well beyond the boundaries of Tsinjo’s territory and often didn’t return for weeks or months at a time. It is possible his absence, particularly in the early part of 2016, was due to the presence of Tsinjo’s offspring Cobalt. Female primates cannot ovulate while they are nursing and since aye-aye offspring can remain with a female for at least 14 months (Feistner and Ashbourne 1994; Winn 1994), Cobalt’s presence may have been enough for Masy to avoid roaming in Tsinjo’s territory for an extended period of time. Future research should examine how many female territories are incorporated within a male’s territory and if male habitat use is related to females in estrous.

When reviewing the overall home range size (Table 3.2) of the female aye-aye,

Tsinjo, there is a big difference between the 100% MCP home range (713.6 ha) and the

95% isopleth for KDE home range (474.8 ha). There are two reasons for this striking difference: 1) home range size is calculated differently when using MCP and KDE and 2)

137 the birth of Cobalt, Tsinjo’s offspring, skewed the 2016 KDE estimate. MCP provides an estimated range based on the available data points without expanding the given data set

(Worton 1989). In contrast, KDE uses GPS points to calculate a probable range that is potentially greater than the area based solely on known localities from the data (Worton

1989). Therefore, even though the MCP estimates Tsinjo’s home range to be 713.6 ha, it is possible her home range is much greater. This may seem a moot point given the overall KDE home range was calculated as smaller than the MCP; however, the 95% isopleth for the KDE in 2017 was greater (775.3 ha) than the MCP estimate (713.6 ha).

The 95% isopleth for the KDE in 2016 was only calculated to be 407.1 ha which probably resulted in an overall estimate of 474.8 ha, which is smaller than the MCP or

2017 KDE values. There may be a behavioral explanation for the disparity between the

KDE estimates.

The differences in 95% isopleths for the 2016 and 2017 KDE home range estimates, and ultimately the small home range size for the entire study, are likely due to

Tsinjo’s care of her offspring, Cobalt. Cobalt was born in February 2016 and remained with Tsinjo throughout the rest of the study. When they forage, female aye-ayes with newborns tend to park their infants in trees rather than carry them while they search for food (pers. obs.). This practice continues until developing infants have acquired enough foraging skills to sustain themselves (Kappeler and Ross 2001). During the period infants are parked, mothers interrupt their foraging bouts and return to the nest in order to nurse their offspring. This practice of maintaining close proximity to the infant temporarily constrains the foraging territory to a small portion of the home range

(Kappeler 1998; Ross 2001). Therefore, Tsinjo used a smaller portion of her home range

138 during the first year of the study because she was caring for a parked infant. New-born infants in captivity were found to rely solely on their mother’s milk during their first 20 weeks of life and intermittently nurse up to a year after birth (Feistner and Ashbourne

1994; Winn 1994). Thus, Tsinjo’s increased use of her home range in 2017 is likely due to Cobalt’s increased independence, while the smaller 2016 and overall KDE estimates are likely skewed due to Tsinjo’s decreased ranging and increased infant care. I discuss

Cobalt’s ranging and feeding behaviors further in Chapter 5. To date, no study has examined the home range size of females with offspring, therefore it is impossible to determine if this fluctuation in territory is normal.

As suggested in Chapter 2, the difference between the home range size presented in this study and those from earlier reports may be due to differences in habitat quality.

The island of Nosy Mangabe is approximately 500 ha in size and contains at least seven aye-ayes (Sterling 1993, 1994). It is possible that the small home ranges of Nosy

Mangabe aye-ayes is due to over-crowding. With too many aye-ayes on the island and non-overlapping female home ranges as part of their social organization, territories become smaller and diets broaden in order to locate sufficient resources within their space. This may be why only the aye-ayes on Nosy Mangabe have been reported to consume Canarium seeds that have fallen to the ground (Sterling 1993, 1994a).

Kianjavato is a disturbed habitat consisting of multiple patchy forests

(Randimbiharinirina et al. 2018). The forest patches are surrounded by agricultural subsistence farm land and coffee plantations (Randimbiharinirina et al. 2018). Aye-ayes in Kianjavato have been observed traveling several kilometers across rice fields in one night to move between forest patches (Edward Louis Pers. Comm.). Though aye-ayes

139 can travel via terrestrial quadrupedalism (Curtis 1992; Sterling 1993), the absence of continuous canopy may be enough to limit the aye-aye’s home range size in this disturbed forest. Since Torotorofotsy is undisturbed forest adjacent to Mantadia National

Park, aye-ayes have the opportunity to disperse further while remaining in the canopy.

Continuous trees allow aye-ayes to use their most common form of locomotion, arboreal quadrupedalism (Curtis 1992; Ancrenaz et al. 1994). The positional behavior of aye-ayes during locomotion will be explored further in Chapter 4. Aye-ayes in Torotorofotsy were never seen in non-forested areas and, presumably, had no reason to move along the ground for an extended distance. In other words, aye-ayes are adaptable enough to utilize terrestrial habitat when necessary, but will primarily remain in the canopy when possible.

Future research should explore how reforestation affects (a) the home range size and (b) dietary breadth of aye-ayes in a disturbed forest.

To summarize the home range analysis: (1) home ranges of the male and female aye-ayes of Torotorofotsy were determined to be significantly larger than those reported from any previous study and, perhaps even greater than that reported here, (2) the home range use of the adult female was largely dependent upon the presence of a nursing offspring.

Annual Relationship Between Diet and Ranging

My second objective was to examine the relationship between diet and ranging behavior. I predicted that annual habitat use by the female aye-aye would be related to invertebrate feeding, not Canarium seed feeding. Based solely on the number of GPS points taken in 2016 and 2017 (Table 3.3), Tsinjo had more GPS points for invertebrate feeding (227 and 195 GPS points, respectively) than Canarium trees (13 and 15 GPS

140 points, respectively). In 2016 (Figure 3.5A), the most frequently used portion of Tsinjo’s territory, i.e. the 10% isopleth of the KDE map, included invertebrate feeding locations but no Canarium feeding sites. In fact, only three of Tsinjo’s thirteen Canarium feeding sites occurred within the 50% isopleth of the KDE home range for 2016. However, in

2017 (Figure 3.6A), the 10% isopleth for the KDE incorporated six of the fifteen

Canarium feeding locations. Half of the Canarium feeding locations were included in the 50% isopleth. Therefore, my prediction that the annual aye-aye home range would be related to invertebrates and not Canarium seeds was supported in 2016 but not supported in 2017. Because there was no difference in the amount of Canarium seeds in ripe fruit consumed in 2016 compared to 2017 (see Chapter 2), I expected the resource consumption to have a similar influence on the ranging behavior for both years. An examination of the seasonal differences in KDE ranges and Canarium feeding behavior may help to elucidate the differences in annual feeding on Canarium seeds.

In 2016, the hot/rainy season (season 1) was the only period when Canarium seeds in ripe fruit were consumed (see Chapter 2). The 2016 annual map (Figure 3.5A) shows that none of the Canarium feeding locations occurred within the 10% isopleth, the most frequently used portion of the habitat. During the hot/rainy season of 2016 (Figure

3.5B), one Canarium feeding location occurred within the 10% isopleth. This suggests that the aye-aye did not focus her ranging behavior on Canarium availability during this season or year. Alternatively, in 2017, Canarium seeds in ripe fruit were eaten in both the hot/rainy season (season 1) and the cold/rainy season (season 2). The annual map for

2017 (Figure 3.6A) shows there were six Canarium feeding locations within the 10% isopleth. This could suggest that Tsinjo focused her feeding on this area because

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Canarium seeds were abundantly available there. However, if this were the case, we would expect her to return to this area every season when Canarium was available, i.e., when Canarium feeding occurred, it would happen within this 10% isopleth. That she did not suggests (see figures 3.6B, C, D) that the Canarium feeding in the annual 10% isopleth could be coincidental and that feeding in this location had as much to do with invertebrates as it did with Canarium.

In summary, aye-aye annual ranging behavior at Torotorofotsy appears to be directely related to invertebrate feeding and is influenced little by the distribution of

Canarium. Future research should examine if aye-ayes in non-undisturbed forests and with broader diets still focus their annual ranging behaviors on invertebrate foraging.

Seasonal Relationship Between Diet and Ranging

I predicted that the seasonal habitat use of the female aye-aye would be related to invertebrate feeding but not Canarium seed feeding. In every season, there were more invertebrate feeding locations than Canarium feeding locations within the female’s home range (Table 3.4). Based on the rarity that Canarium feeding locations were recorded in the cold/rainy seasons (season 2) of 2016 and 2017, and the complete absence of

Canarium feeding in the hot/dry seasons (season 3) of 2016 and 2017, invertebrate feeding was the resource most likely correlated with home range use at those times. As previously described, the hot/rainy seasons (season 1) of 2016 (Figure 3.5B) and 2017

(Figure 3.6B) had one and two Canarium feeding locations within the 10% isopleths (2.1 ha and 11.3 ha, respectively). The 50% isopleths (2016: 32.7 ha; 2017: 114.2 ha) show three and ten Canarium feeding locations in 2016 and 2017, respectively. This may suggest that Canarium feeding was at least partially correlated with the aye-aye’s habitat

142 use, especially during 2017. In 2016, the majority of invertebrate feeding locations were located within the 10% and 50% isopleths. Again, this might be due to the presence of the infant Cobalt. More specifically, if Tsinjo was unable to range as far as she normally would because of her parked infant, she might have compensated by consuming as many invertebrates as possible within the small area (2.1 ha). During the hot/rainy season

(season 1) of 2017, when Cobalt was more independent, Tsinjo’s invertebrate feeding remained higher than Canarium feeding in the 10% and 50% isopleths, but feeding sites were more widely dispersed. This is likely because the range was greater so she fed across a bigger area. In many instances, there were invertebrate feeding locations in close proximity to Canarium feeding locations (Figure 3.5 A, B, C and Figure 3.6 A, B,

C). As described in Chapter 2, even though Canarium seeds in ripe fruit were eaten in greater quantities during this season, Tsinjo still consumed invertebrates. If she focused her ranging behavior on the location of Canarium trees, it would be expected for there to be more Canarium feeding locations within the 10% isopleths. Since that is not the case,

I support my prediction that invertebrates are the main food source that drive seasonal habitat use. It should be noted that Canarium feeding locations are often within the 50% isopleths for season 1 of 2016 and 2017, suggesting that Tsinjo is frequently ranging around these trees during the hot/rainy season. It is possible that in forests where invertebrate assemblages are less evenly dispersed and aye-ayes use Canarium trees more regularly, aye-aye home ranges may correlate more closely with this resource.

The 2016 hot/rainy season (season 1) and cold/rainy season (season 2) were the smallest 95% isopleths, 170.6 ha and 204.5 ha respectively (Table. 3.6). The hot/rainy season (season 1) and hot/dry season (season 3) of 2017 were the largest 95% isopleths at

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527.0 ha and 487.3 ha, respectively (Table 3.6). As previously mentioned, Tsinjo’s home range size was smaller in 2016 than in 2017, probably because of her parked infant.

There is a clear increase in home range sizes across the three seasons of 2016, with the last season having the greatest home range for the year. This is likely due to Cobalt growing older and becoming more independent. In fact, Cobalt’s first observed feeding events occur in September of 2016, approximately 20 weeks after his April birth.

In both years, there was an increase in home range size from the cold/rainy season

(season 2) to the hot/dry season (season 3). In 2017, there was a decrease in home range size during the cold/rainy season, considered the winter months in Madagascar (Wright

1999, 2006; Vasey 2005). Season 2 of 2017 had the most GPS data points of any season

(Table 3.3), so the small area was not due to data deficiency. It is possible Tsinjo decreased her home range size during this season in response to low invertebrate availability. The 10% isopleth during the cold/rainy season (season 2) of 2017 (5.2 ha) was smaller than hot/rainy season (season 1; 11.3 ha) and hot/dry season (season 3; 13.8 ha) of 2017. This raises the possibility that Tsinjo’s decreased home range is associated with a seasonal change in invertebrate availability. During the cold/rainy season of 2017

(season 2), Tsinjo fed at a Canarium tree once and consumed an unknown resource from

Vakona trees on four different occasions. Vakona feeding was only witnessed during this period and one other time, during the cold/rainy season of the 2015 pilot study. It seems likely that Tsinjo was not only decreasing her home range size during the 2017 cold/rainy season, but was also expanding her diet to include a resource not typically used.

Immediately following the cold/rainy season, there was an increase in the KDE home range sizes as the aye-aye transitioned to the hot/dry season (season 3). Simultaneously,

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Tsinjo exclusively consumed invertebrates during this hot/dry season (season 3) of 2017.

As preferred resources become scarce, an organism will often consume food items it would normally reject (Barrette et al. 2010). Though invertebrate assemblages appeared to increase from season 1 to season 2 in 2017 (see Chapter 2, Table 2.3), estimates of invertebrate abundance were likely not reflective of the actual availability in the environment (as discussed in Chapter 2). Therefore, it is possible that invertebrate resource availability increased between season 2 and season 3 of 2017 and the aye-aye expanded her home range in search of this resource. Since aye-ayes in disturbed forests have broader diets and may not preferentially consume invertebrates (Sterling 1993,

1994a; Ancrenaz et al. 1994), future studies should establish if aye-ayes in these locations alter their territories seasonally.

Annual Habitat Use

My third prediction was that Tsinjo would not use her home range uniformly during each year. In 2016, the 95% isopleth was 407.1 ha and in 2017 it was 775.3 ha

(Table 3.5). Therefore, while her use of the home range changed between years, it is not clear if the size of the home range size itself decreased during 2016. As already discussed, I believe the annual range use differed due to the birth and slow development of Tsinjo’s offspring Cobalt. Cobalt was born in 2016 and remained parked in a nest until August 2016 (see Chapter 5). Mothers that park infants typically have smaller ranges because they are constantly returning to a nest to care for their young (Kappeler

1998; Ross 2001). As 2016 progressed Tsinjo’s 95% isopleths increased from 170.6 ha in season 1 to 296.7 ha in season 3 (Table 3.6). By the time Cobalt was one year old and more independent, Tsinjo’s 95% isopleth in season 1 of 2017 was 527.0 ha (Table 3.6).

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Thus, it seems likely that Tsinjo’s home range use was smaller in 2016 because of

Cobalt’s dependence on her for parental care. Cobalt’s development is discussed further in Chapter 5. Future research should investigate how aye-aye mothers maintain territory boundaries when ranging territories decrease while caring for a nested infant.

Comparison of the 2016 and 2017 grid-cell maps (GCMs; Figure 3.7A and 3.8A) reveals that there was minimal overlap in the portion of the home range Tsinjo used most frequently each year. Therefore, my prediction that the aye-aye would use different portions of her habitat each year is supported. I believe Tsinjo used different portions of her habitat each year in order not to deplete invertebrate populations. Up to ten larvae can be oviposited into a substrate (Hanks 1999); this results in a significantly smaller patch size than other resources, such as fruit or leaves in a tree. Additionally, there is significantly less invertebrate than floral biomass available for consumption (Wilbur et al.

1974). Thus, aye-ayes will systematically use their habitat in order to have continuous access to their preferred resource. Furthermore, the dispersed polygyny system is critical to this foraging strategy because non-overlapping female home ranges minimize competition over invertebrates, thereby ensuring a protected and reliable supply

(Wrangham 1980). This point is discussed further below. It should be noted that

Tsinjo’s home range was larger than any previously reported female aye-aye territory. It is possible that other females used Tsinjo’s home range to feed on invertebrates; however, based on previous studies that have demonstrated the non-overlap of female home ranges (Sterling 1993, 1994a), this seems unlikely. Future research should examine if any overlap occurs in female aye-aye home ranges in undisturbed forests.

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Seasonal Habitat Use

My third prediction also stated that Tsinjo would not use her home range uniformly during each season. In 2016, Tsinjo’s 95% isopleths for season 2 (204.5 ha;

Table 3.6) and season 3 (296.7 ha) were more than half the size of her entire home range during that year (95% isopleth: 407.1 ha; Table 3.5). Similarly, the 95% isopleths for season 1 (527.0 ha) and season 3 (487.3 ha) of 2017 were also greater than half of her entire home range during that year (95% isopleth: 775.3 ha). Only the home ranges of season 1 of 2016 and season 2 of 2017 did not equal more than 50% of the total home range size for the respective years. The decrease during season 1 of 2016 is likely due to the birth of Cobalt, as Tsinjo would be expected to decrease her home range while caring for her parked infant (Kappeler 1998; Ross 2001). It is possible that the decreased home range during season 2 of 2017 was due to depleted availability of invertebrates as described above. Indeed, if there were a decline in invertebrate availability during this time, it would help to explain the brief expansion of Tsinjo’s diet to include the Vakona resource. Unfortunately, there is no reliable method for estimating invertebrate abundance. Thus, the reason for Tsinjo’s decrease in home range use during this season remains elusive. Because of this decrease in home range use during season 2 of 2017, I failed to support my prediction that aye-ayes would maintain a similar home range use across seasons. Future research should explore if aye-ayes that prefer seasonally available resources, such as those in Mananara Nord Biosphere Reserve that prefer nectar from Ravenala madagascariensis flowers (Ancrenaz et al. 1994), have even greater variability in their seasonal home range use.

Examining potential correlations between GCMs and KDE maps may help elucidate differences in habitat use. The GCMs (Figure 3.7 and 3.8) visually depict the 147 frequency that an animal uses portions of its home range. As such, it can identify tendencies for the study subject to home-in or cluster at specific regions within the home range. We can compare these clusters to the 10% and 50% isopleths generated from the

KDE to determine if these differences in habitat use are random or are significantly different. The 10% isopleths (Figure 3.3 B through D and Figure 3.5 B through D) between seasons show noticeable differences in the most frequently used areas. In fact, the 10% isopleths shifts from west to east and slightly south to north as the seasons progress, suggesting that Tsinjo was shifting her home range use in this manner. This pattern is not as obvious in the larger KDE isopleths (50% and 95%) for habitat use probably because she ranged over a large area and because so much of her home range was not used frequently. However, it might suggest that within the overall territory, most of Tsinjo’s activity occurred within a relatively confined area, i.e., the 10% isopleth.

Once Tsinjo left an area, she tended to not return to that location until the rest of her territory was explored. I therefore support my prediction that aye-ayes would use different areas of their home range in each season. As discussed below, it is possible

Tsinjo was using different portions of her environment each season as a way of sampling her territory and allowing invertebrate populations to recover (Chapman 1988). Other studies have demonstrated that primates are good stewards of their habitat and will allow highly-prized fruiting trees to recover before depleting the resource again (Chapman

1988; Garber 1989; Chapman 1990; Chapman et al. 1995; Janson 1998; Cunningham and

Janson 2007; Valero and Byrne 2007; Tombak et al. 2012; Shaffer 2014). Future research should investigate the frequency with which aye-ayes revisit different portions of their home range.

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Conclusion

The presence of Cobalt appears to have dramatically altered Tsinjo’s ranging behavior, as would be expected from a species that parks their infants (Kappeler 1998;

Ross 2001). This point is well illustrated by the ranging data from 2016, the year Cobalt was born. In that year, Tsinjo’s home range use, as illustrated by the overall KDE estimate (Figure 3.2) was significantly smaller than the MCP home range. I suspect this reduction in home range use is attributable to Tsinjo maintaining close proximity to her parked Cobalt so that she could frequently return to the nest during her foraging bouts in order to nurse. I assume that Tsinjo’s ranging behaviors in 2017 are similar to how she would behave as a solitary individual because Cobalt was older, more independent, and likely not requiring as much maternal care (Feistner and Ashbourne 1994; see Chapter 5).

Therefore, looking solely at her annual and seasonal home range use in 2017, it appears that Tsinjo was behaving as an energy maximizer. Her 10% isopleth for the 2017 home range size (25 ha) was bigger than the total home range size of other large lemur species such as Lemur catta (7.4 ha) and Propithecus verreauxi (7.6 ha; Harvey and Clutton-

Brock 1981). From one season to another she used different portions of her habitat, but it appears that invertebrates were the resource associated with the most heavily used portions of her territory (i.e. the 10% isopleth). Since aye-ayes spend most of their time feeding and traveling (Table 3.1; Randimbiharinirina et al. 2018), and not performing other behaviors, energy maximization is the most likely pattern of optimization (Schoener

1971; Hixon 1982). If Tsinjo were a time minimizer, she would most likely have spent more time eating Canarium fruits during the hot/rainy season (season 1) and spent less time consuming invertebrates (Schoener 1971; Hixon 1982). Indeed, time minimizers will consume the necessary resources as quickly as possible in order to spend more time 149 performing other, non-feeding behaviors (Schoener 1971; Hixon 1982). Instead, season 1 of 2017 had the largest estimated 95% isopleth and there was still ample invertebrate feeding (Table 3.6). Additionally, her second largest home range occurred in season 3 of

2017, when invertebrates were the only resource consumed. Therefore, Tsinjo is likely maximizing her energetic intake by consuming large quantities of invertebrates.

Aye-ayes were predicted to be too large to subsist on invertebrates without incorporating other resources into their diet (McNab 1963; Kay 1975). While the aye- ayes in this study did include Canarium seeds in their diet, it would be a stretch to call them primarily frugivorous, as suggested by Kay (1975). Indeed, invertebrates were often the only resource aye-ayes consumed. In order to meet their metabolic needs, aye- ayes likely have to continuously consume invertebrates. Fortunately, invertebrates appear to be ubiquitous in undisturbed forests (Hanks 1999; Sefczek et al. 2017), allowing aye-ayes to continuously consume them. In order for sustained feeding on invertebrates to occur, aye-ayes must have a relatively high success rate at acquiring this resource in whatever section of the forest they occupy. Thus, it follows that (1) aye-ayes must use their range in a systematic manner to ensure they do not deplete the invertebrate population beyond a point where it can replenish and (2) aye-ayes must maintain non- overlapping home ranges to make sure they are not foraging in habitats where invertebrates have already been removed.

To the first point, all Tsinjo’s 10% isopleths are associated with invertebrate consumption. Undisturbed forest have greater invertebrate species richness and abundance, particularly in live trees, than do disturbed forests (Hanks 1999; Sefczek et al.

2017). If a home range were large enough, aye-ayes could continuously forage for

150 invertebrates and not need to expand diet. Tsinjo was clearly focusing her feeding efforts in different portions of her habitat with each subsequent season. It is therefore reasonable to conclude that this constant rotation through her habitat, driven by the search for invertebrates, allows her to sustain herself on this resource without depleting it.

Conversely in disturbed forests where invertebrate assemblages are less diverse, less abundant (Grove 2002; Latchat et al. 2007), and more concentrated in deadwood than live trees (Jabin et al. 2004; Bouget et al. 2013), aye-ayes may need to expand their diet to incorporate resources such as Ravenala nectar out of necessity. If they do not, they risk over-harvesting the invertebrate population. Similarly, if aye-ayes on Nosy Mangabe are over-populated, as previously suggested (Randimbiharinirina et al. 2018; see Chapter

2), they may need to focus feeding efforts on other resources and expand their dietary breadth as a way of compensating for small home range sizes with minimal invertebrates available.

The dispersed polygyny system of aye-ayes is likely related to invertebrate consumption. Females in a noyau social system should maintain non-overlapping home ranges so they can monopolize resources and improve individual fitness (Wrangham

1980). When a resource is distributed throughout the environment and continuously available, a primate can be territorial (Emlen and Oring 1977). Territoriality allows an organism to minimize the competition for resources and better estimate when a patch is replenished for improved food intake (Charnov et al. 1976). If invertebrates are evenly dispersed throughout the habitat but occur in small clumps (Andriamisedra et al. 2015;

Sefczek et al. 2017), and if aye-ayes are energy maximizers that must continuously consume invertebrates, venturing into an area that is already depleted of this resource will

151 adversely affect the aye-aye. This is particularly true of females that need the security of resource availability for the added energetic costs of gestation and lactation (Wrangham

1980). Therefore, by maintaining non-overlapping home ranges, females can ensure they have access to an ample supply of invertebrates and can consistently meet their energetic demands.

Lastly, it has been suggested that primates have developed large brains to help them remember when and where resources are located and to minimize search time

(Milton 1981). For instance, the moustached tamarins and saddle-back tamarins remember when nectar from one species of tree becomes available and where the most successful feeding sites are located (Garber 1989, 1993). Indeed, many species of primates will visit the same trees every year during the same season because they have learned it is a reliable resource during that time (Janson 1985; Garber 1989, 1993; Garber and Paciulli 1997; Gibeault and MacDonald 2000; Hemingway and Bynum 2005; Valero and Byrne 2007; Erhart and Overdorff 2008; Janmaat et al. 2013). Since Madagascar’s seasons vary in duration and intensity (Wright 1999), temporal fluctuations in resource availability may be too difficult to predict. If foods do not have a discernable pattern of peaks and troughs, there would be less benefit to remembering when and where successful feeding events took place. This may partially explain why lemur brains have remained so small. However, in the case of the aye-aye, their brain size is relatively large. Since invertebrates are available throughout the environment and throughout the year, they can and do feed anywhere in their home range. Yet, Tsinjo doesn’t appear to revisit the same locations from one year to the next. She may be using her territory in a systematic manner, never revisiting the same location multiple seasons in a row, but there

152 does not appear to be any temporal component to her territory use. Therefore, aye-aye brain size is likely encephalized because of their percussive foraging behavior and the need for processing large amounts of sensory information (Kaufman et al. 2005), and less so in relation to spatial memory. I conclude that the large brain of the aye-aye has less to do with spatial memory and mental maps, and much more to do with the demands of extractive foraging. This is discussed further in Chapter 5.

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Table 3.1 The number of GPS points and associated behaviors performed by Tsinjo and Masy. Data for Masy were collected between January 2014 and December 2017. Data for Tsinjo were collected between January 2016 and December 2017.

Behavior Masy Tsinjo Copulating 0 2 Feeding (Invertebrates) 23 422 Feeding (Canarium) 8 28 Feeding (Vakona) 0 3 Grooming 0 8 Nest 18 70 Playing 0 3 Resting 9 110 Traveling 77 254 TOTAL 135 900

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Table 3.2 Estimated overall home range sizes for Tsinjo and Masy based on MCP and KDE methods. KDE is broken down into 95%, 50% and 10% isopleths indicating the size of the area most frequently used, from least to most often.

Masy Tsinjo MCP 1587.5 ha 713.6 ha KDE 95% 1020.5 ha 474.8 ha 50% 179.1 ha 223.1 ha 10% 23.2 ha 11.8 ha

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Table 3.3 The number of GPS points taken for Tsinjo annually and seasonally, between January 2016 and December 2017.

Year/Season Number of GPS Points 2016 Hot/rainy season 140 2016 Cold/rainy season 105 2016 Hot/dry season 181 Total for 2016 426 2017 Hot/rainy season 105 2017 Cold/rainy season 213 2017 Hot/dry season 156 Total for 2017 474

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Table 3.4 The number of GPS points taken for the various behaviors of Tsinjo each season between January 2016 and December 2017. Infrequent behaviors included copulation, grooming and playing.

Invertebrate Canarium Vakona Nest Rest Travel Infrequent Feeding Feeding Feeding Behaviors 2016 Season 1 64 12 0 10 8 45 1 Season 2 56 1 0 10 17 18 3 Season 3 107 0 0 8 29 34 3 Totals 227 13 0 28 54 97 7 2017 Season 1 46 14 0 10 9 25 1 Season 2 85 1 3 18 28 77 1 Season 3 64 0 0 14 19 55 4 Totals 195 15 3 42 56 157 6

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Table 3.5 Annual home range sizes for Tsinjo in 2016 and 2017 based on KDE methods. The 95%, 50% and 10% isopleth values are reported.

KDE KDE KDE 95% 50% 10% 2016 407.1 ha 97.1 ha 10.1 ha 2017 775.3 ha 203.7 ha 25.0 ha

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Table 3.6 Seasonal home range size estimates between January 2016 and December 2017 for Tsinjo based on KDE methods. The 95%, 50% and 10% isopleth values are reported.

Season KDE KDE KDE 95% 50% 10% 2016 Hot/rainy season 170.6 ha 32.7 ha 2.1 ha 2016 Cold/rainy season 204.5 ha 41.8 ha 3.0 ha 2016 Hot/dry season 296.7 ha 55.4 ha 3.7 ha 2017 Hot/rainy season 527.0 ha 114.2 ha 11.3 ha 2017 Cold/rainy season 277.1 ha 56.2 ha 5.2 ha 2017 Hot/dry season 487.3 ha 130.4 ha 13.8 ha

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Figure 3.1 The 100% MCP home ranges for Masy (white) and Tsinjo (black) from data points between January 2016 and December 2017.

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(A) (B)

Figure 3.3 The 2016 KDE home ranges for Tsinjo. The white line represents the 100% MCP home range. Maps include all data points in 2016 (part A), all points during season 1 of 2016 (part B), all points during season 2 of 2016 (part C), and all points during season 3 of 2016 (part D).

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(A) (B)

Figure 3.4 The 2017 KDE home ranges for Tsinjo. The white line represents the 100% MCP home range. Maps include all data points in 2017 (part A), all points during season 1 of 2017 (part B), all points during season 2 of 2017 (part C), and all points during season 3 of 2017 (part D).

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(A) (B)

Figure 3.5 The 2016 KDE home ranges for Tsinjo with feeding points overlaid. The white line represents the 100% MCP home range. Maps include all data points for 2016 (part A), all points during season 1 of 2016 (part B), all points for season 2 of 2016 (part C), and all points for season 3 of 2016 (part D). In all maps, invertebrate feeding is represented by blue circles and Canarium feeding by green circles.

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(A) (B)

Figure 3.6 The 2017 KDE home ranges for Tsinjo with feeding points overlaid. The white line represents the 100% MCP home range. Maps include all data points for 2017 (part A), all points in season 1 of 2017 (part B), all points in season 2 of 2017 (part C), and all points in season 3 of 2017 (part D). Invertebrate feeding is represented by blue circles, Canarium feeding by green circles and Vakona feeding by red circles.

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(A) (B)

Figure 3.7 The 2016 grid-cell maps for Tsinjo. The black line represents the 100% MCP home range and the white line represent the KDEs of 2016. Maps include all data points in 2016 (part A), all points in season 1 of 2016 (part B), all points in season 2 of 2016 (part C), and all points in season 3 of 2016 (part D). Red squares are high-high clusters and blue squares are low-high outliers. Squares without a fill-in color had no GPS points.

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(A) (B)

Figure 3.8 The 2017 grid-cell maps for Tsinjo. The black line represents the 100% MCP home range and the white line represent the KDEs of 2017. Maps includes all data points in 2017 (part A), all points in season 1 of 2017 (part B), all points in season 2 of 2017 (part C), and all points in season 3 of 2017 (part D). Red squares are high-high clusters and blue squares are low-high outliers. Squares without a fill-in color had no GPS points.

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Chapter 4 Positional behavior of an adult female aye-aye (Daubentonia madagascariensis) and a sub-adult male aye-aye in Torotorofotsy, Madagascar

In this chapter, I present positional behavior data on a female aye-aye, Tsinjo, and her offspring, Cobalt, collected over a period of eight months. I collected locomotor data during travel and during foraging and postural data during feeding on the two individuals.

I also collected information on forest level and substrate use by the two aye-ayes. These data are used to test established relationships between positional behavior and maintenance activities, evaluate what resources influence postures used during feeding, and test the relationship between positional behavior, strata use and substrate use.

Introduction

Prior research suggests that aye-ayes (Daubentonia madagascariensis) forage at every level of the forest (Sterling 1993, 1994a). On the forest floor, aye-ayes extract invertebrates from downed deadwood and eat Canarium seeds that have fallen to the ground (Sterling 1993, 1994a). In the understory and low canopy, these lemurs remove larvae from live trees, bamboo and snags (Sterling 1993, 1994a; Sefczek et al. 2017;

Randimbiharinirina et al. 2018). In the main and upper canopy, this species is known to harvest invertebrates from live or dead branches and boughs, remove nectar from flowers of Ravenala madagascariensis, and consume Canarium seeds in ripe fruit (Iwano and

Iwakawa 1988; Sterling 1993, 1994a; Ancrenaz et al. 1994; Sefczek et al. 2017;

Randimbiharinirina et al. 2018). Invertebrates are the only resource available at all forest levels and, as discussed in Chapter 2, invertebrates are the preferred resource of aye-ayes.

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Given their reliance on invertebrates, aye-ayes need to be adept at moving through every forest stratum.

Based on the ranging behavior results presented in Chapter 3, the aye-aye is an energy maximizer. Aye-ayes require a large home range to harvest sufficient quantities of invertebrates to support their body size. As a medium-sized organism, aye-ayes (2.5 kg) should expand their diet to improve foraging efficiency in a large home range

(McNab 1963). Aye-ayes, however, do not conform to this expectation (see Chapter 3).

Additionally, aye-ayes are presumably too large to sustain themselves on invertebrates

(Kay 1976); yet they violate this relationship as well (see Chapter 2). In order for a 2.5 kg organism to be able to subsist on invertebrates in an expansive territory, it must be a highly efficient forager (McNab 1963; Gaulin 1979). Since invertebrates occur at all forest levels and appear to be evenly dispersed (i.e., not clumped) throughout the environment (Sefczek et al. 2017), aye-ayes must be able to efficiently acquire them wherever they occur. It is therefore reasonable to expect that aye-ayes will possess adaptations that maximize efficient location and acquisition of their preferred food

(Temerin and Cant 1983).

Harvesting and Processing Adaptations

The demands of acquiring and consuming different kinds of resources are selective pressures acting on all primates (Temerin and Cant 1983). In response to these pressures, primates have evolved a myriad of specialized morphological adaptations to better compete for resources. These features are typically divided into two categories: processing adaptations and harvesting adaptations (Marshall and Wrangham 2007;

Harrison and Marshall 2011; Rosenberg 2013). Processing adaptations are used to ingest,

169 masticate and digest resources and are among the most recognizable feeding adaptations

(Marshall and Wrangham 2007; Harrison and Marshall 2011; Rosenberg 2013). For example, frugivores possess broad incisors to maximize fruit intake per bite (Hylander

1975), while folivores have high cusps and sheering crests on their molars to help break the tough cell walls of leaves (Kay 1975).

Harvesting adaptations include sensory, cognitive and positional (locomotor and postural) behaviors that help in the detection, location, and acquisition of food items prior to ingestion (Fleagle 1976a; Cant 1992; Doran 1992; Marshall and Wrangham 2007;

Harrison and Marshall 2011; Rosenberg 2013). These adaptations may be less obvious than processing adaptations because they do not necessarily directly interact with the resource (Marshall and Wrangham 2007; Harrison and Marshall 2011; Rosenberg 2013).

In other words, while processing adaptations involve direct manipulation of a food item, harvesting adaptations help the primate interact with the environment around the resource. For example, although the diagnostic shoulder morphology of a frugivorous hylobatid does not physically contact highly prized figs, it has been argued that suspensory locomotion evolved in frugivores because it (a) maximizes travelling efficiency between fruiting trees by allowing animals to better travel in a straight line between clumped and distant resource (i.e., fruit) and (b) helps them access fruits above and below the ends of terminal branches, essentially doubling their foraging sphere

(Temerin and Cant 1983). To cite another example, it has been argued that the secondarily-derived claws of the callitrichids allow these primates to cling to large vertical trunks while they forage on tree sap (Garber 1980, 1984, 1992). It is doubtful that these small-bodied primates would be able to position themselves on large diameter

170 trunks and feed on exudate without claw-like nails; however, the morphological specialization of callitrichids that enable this dietary strategy never actually contacts the tree gum itself (Garber 1980, 1984, 1992). Though the way these adaptations assist a primate in obtaining resources may be subtle, they are no less important to a primate’s feeding ecology.

Locomotor and Postural Behaviors

Locomotor and postural behaviors improve a primate’s fitness by, among other things, providing increased access to resources within the environment (Ripley 1967;

Cant 1992). Locomotor behaviors are those that shift the primate’s center of gravity and involve spatial displacement, i.e., moving the entire body from one position to another

(Prost 1965; Napier 1967; Ripley 1967). Locomotor behaviors include quadrupedal walking, quadrupedal running, suspension, leaping, vertical clinging and leaping, climbing, head-first descent, rump-first descent, sideways descent, etc. (Fleagle 1976a;

Hunt et al. 1996). These behaviors can be categorized by the maintenance activity during which they are performed (Prost 1965; Napier 1967; Ripley 1967). For example, a primate can locomote very quickly from one end of its home range to another, i.e., it can travel. Alternatively, a primate can move more slowly within a single tree while searching for food, i.e. it can forage (Prost 1965; Napier 1967; Ripley 1967). The goals, habitat features, and respective end points of travel versus foraging differ significantly, and considerable research has shown that frequencies of individual locomotor behaviors differ depending on whether the primate is travelling or foraging (Fleagle 1976a, 1976b;

Mendel 1976; Morbeck 1977; Mittermeier 1978; McGraw 1996, 1998a, b).

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Postural behaviors are the array of behaviors and limb configurations a primate employs during periods when not spatially displacing its body, i.e., when it is stationary

(Prost 1965; Napier 1967; Ripley 1967). Postural behaviors include perching, sitting, standing, clinging, laying down, etc. (Fleagle 1976a; Hunt et al. 1996). These behaviors can be used by a primate to configure or position its body during rest, socializing, and feeding bouts (Prost 1965; Napier 1967; Ripley 1967). Postural behaviors have not received nearly as much attention as locomotor behaviors; however, it has been established that several idiosyncratic postures are associated with specialized maintenance activities (McGraw 1998; McGraw and Daegling 2012). For example, the clinging to tree trunks by callitrichids is an adaptive postural behavior which allows these small-bodied and clawed primates to gnaw into bark to stimulate sap production (Garber

1980, 1984, 1992). Together, locomotor and postural behaviors constitute the domain of positional behavior.

Primates display a dazzling array of positional behaviors and there are multiple factors that have shaped the positional behavior of this group (Napier 1967; Napier and

Napier 1967; Fleagle 1984; Schmidt 2010; Fleagle and Lieberman 2015). Variation in the size, location and density of arboreal supports (i.e. trunks, boughs, branches, twigs, lianas, etc.) are some of the architectural elements of habitat a primate must navigate in order to acquire sufficient resources (Fleagle 1976a; Cant 1992). Over time, the successful negotiation of these habitat elements has shaped the post-cranial morphology of primates (Napier 1967) and physical anthropologists have long been interested in establishing relationships between specific elements of habitat use, positional behavior, and their morphological correlates (Ripley 1967; Fleagle 1976a, b; Temerin and Cant

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1983; McGraw 1996). Locomotor and postural behaviors provide a selective advantage if they improve a primate’s ability to acquire resources within an environment (Ripley

1967; Fleagle 1984; Cant 1992). By evaluating the contexts during which locomotor and postural behaviors are most frequently performed by free-ranging primates, we can better understand the selective factors that shaped their morphology (Ripley 1967; Fleagle

1976a; Mittermeier 1978; Cant 1986). The relationships established in extant taxa can then be used to infer the behavior of extinct forms (Kay and Covert 1984; Rosenberg

1992; Ross 1996; Plavcan et al. 2002).

Morphological Adaptation

When locomotor or postural behaviors are chronically performed or are critical to fitness, they will directly influence a primate’s morphology (Fleagle 1976a; Hunt et al.

1996). In other words, the anatomical configuration of a primate should be adapted to help maximize the occurrence of locomotor and postural behaviors and ultimately improve the fitness of the primate in its natural environment (Ripley 1967; Fleagle

1976a; Cant 1992; Hunt et al. 1996). For example, Presbytis obscura and P. melalophos are sympatric species of leaf monkeys with different locomotor tendencies (Fleagle

1976b). P. obscura relies upon quadrupedal locomotion to travel along large boughs while P. melalophos typically leaps and uses forelimb suspension to travel along smaller supports (Fleagle 1976b). These species differences in locomotor tendencies are reflected in the respective morphologies: P. obscura has shorter forelimbs and hindlimbs that facilitate arboreal quadrupedalism while P. melalophos has longer hindlimbs for enhanced propulsion during leaping. P. melalophos also has a rounded, globular humeral head for better range of motion in the shoulder during suspension (Fleagle 1976b). Other

173 well-known examples between anatomy and inferred locomotion in extant taxa include: intermembral indices in three types of leapers (Oxnard et al. 1981), hindlimb reduction and forelimb elongation in vertical climbers (Jungers 1978), and specializations of the hand and wrist in knuckle-walkers (Tuttle 1967).

Body Size and Positional Behavior

There is no greater constraint on primate locomotion than body size (Fleagle and

Mittermeier 1980; Fleagle 1984; Jungers 1984). A primate’s body size can frequently restrict its ability to perform individual locomotor and/or postural behaviors (Fleagle and

Mittermeier 1980; Cant 1992). For instance, leaping is generally rare in large-bodied primates because larger primates are more likely to suffer injury or death as a result of awkward landings or falls. In addition, due to scaling factors, the energy required to propel a large primate is proportionally much greater than that required by a small primate. Furthermore, a large bodied primate is more likely to encounter discontinuities in a canopy that can be crossed by bridging or climbing because of its longer appendages and trunk length (Cartmill and Milton 1977; Fleagle and Mittermeier 1980; Cannon and

Leighton 1994). In contract, a small-bodied primate moving through the same forest is likely to encounter more gaps that can only be crossed using leaping (Cartmill and Milton

1977; Fleagle and Mittermeier 1980; Cannon and Leighton 1994). Consequently, large- bodied primates tend not to leap often and instead travel quadrupedally or using climbing and/or suspension (Fleagle and Mittermeier 1980). Small-bodied primates such as tarsiers (Tarsius sp.; 113-142g), do not require as much energy to move their mass and can derive ample leaping propulsion from their hindlimbs, particularly if they are elongated (Napier and Walker 1967). In addition, due to their diminutive stature, small-

174 bodied primates encounter a greater number of gaps requiring leaping that do not appear as gaps to large-bodied primates (Fleagle and Mittermeier 1980). Thus, leaping is more frequently used for crossing gaps in the canopy pathways (Fleagle and Mittermeier

1980).

The array of supports a primate uses is also restricted by body size (Napier 1962;

Cartmill and Milton 1977; Fleagle and Mittermeier 1980; Cannon and Leighton 1994;

McGraw 1998a). Multiple studies have shown that there is a strong relationship between body size and support size across the primate order (Napier 1967; Cartmill 1974; Fleagle

1976a; Fleagle and Mittermeier 1980; Cant 1992). Within a tree, supports can be delineated into four general types: trunks, boughs, branches and twigs (Fleagle 1976a).

Trunks are the principle and most stable support available within a forest (Fleagle 1976a;

Cant 1992). Boughs represent slightly smaller, but still typically stable supports extending outwards from the trunk (Fleagle 1976a). Branches are still smaller and less stable supports often originating on boughs, while twigs are the weak, readily deformed distal ends of branches (Grand 1972; Fleagle 1976a; Cant 1992). Trunks and boughs are relatively stable and strong supports; therefore, most any primate, regardless of body size, can use them without concern of the support breaking under the tension of their weight

(Fleagle and Mittermeier 1980; Cant 1992). However, these supports usually have large diameters and, when vertically oriented, require an organism to possess either long arms and large grasping hands or specialized clawed digits to resist gravitational pull as they move their mass along the support (Cartmill 1974; Jungers 1978). Branches and twigs, on the other hand, are thinner and less rigid than boughs and trunks (Grand 1972; Fleagle

1976a; Fleagle and Mittermeier 1980; Cant 1992). When most arboreal mammals use

175 these supports, some amount of downward bending of the branch or twig is expected

(Grand 1972; Cant 1992). The amount of deformation depends upon the weight of the organism, with too much mass resulting in the support reaching its structural breaking point (Grand 1972; Cant 1992). Small-bodied primates typically do not have enough mass for twigs and branches to reach a critical breaking point. Consequently, small- bodied primates should be able to use nearly any support in an environment (Fleagle and

Mittermeier 1980). However, many of the same branches and twigs used by small- bodied primates are likely to break under the weight of a large-bodied primate (Fleagle and Mittermeier 1980). Therefore, large-bodied primates should preferentially use large supports, such as boughs, because they are stronger and not likely to deform under the weight of a primate (Cartmill and Milton 1977; Cant 1992; McGraw 1998a). When a large bodied primate uses smaller supports, it should distribute its weight over several of them to lessen the deformative effects of their mass on each one (Fleagle and Mittermeier

1980).

Most resources consumed by arboreal primates are located at the terminal ends of branches and twigs in the periphery of tree crowns (Cartmill 1972; Fleagle 1976a;

Sussman 1991). Most arboreal primates must therefore deal with the challenges of safely acquiring resources from small, flexible supports in the periphery of the canopy (Fleagle

1976a; McGraw 1998a, 1998b). Primates of different body sizes have solved this problem in different ways. Large-bodied primates are unable to position themselves on top of single twigs on the edges of tree crowns, so they must either distribute their weight across multiple twigs or suspend themselves below these small supports in order to feed

(Napier 1962; Cartmill and Milton 1977; Fleagle and Mittermeier 1980; Cannon and

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Leighton 1994; McGraw 1998b). Because of the branch to body size ratio, there are more supports that appear large to a small-bodied primate and therefore a greater number of supports that can facilitate quadrupedal locomotion including in the terminal branches of tree crowns. For this reason, most small-bodied primates are quadrupedal and suspensory locomotion is comparatively rare because it is not required (Napier 1962;

Cartmill and Milton 1977; Fleagle and Mittermeier 1980; Cannon and Leighton 1994;

McGraw 1998).

Locomotion of any type involves movement; however, the motivation for and end points of different kinds of movement result in different locomotor strategies. This is the reason why we examine locomotion in the context of different maintenance activities

(defined in methods). Generally speaking, when primates travel they chose routes that facilitate rapid movement between locations which are often between distant points in their home range, e.g., between patches. The start and end points of a locomotor bout during travel are therefore often much more general (e.g., that portion of any home range, sleeping tree, etc.) compared to a foraging bout (e.g., the fruit at the end of a twig;

Fleagle and Mittermeier 1980). In such cases, arboreal primates are more likely to travel along larger supports that facilitate direct and rapid travel through the canopy (Napier

1962; Fleagle and Mittermeier 1980; Cannon and Leighton 1994; McGraw 1998a,

1998b). Foraging, on the other hand, tends to involve endpoints that are closer together and much more specific, i.e., the fruit or leaf at the end of a branch within a patch

(Fleagle 1976a). The respective destinations associated with travel versus foraging therefore lead to several predictions concerning the supports and behaviors associated with each of these maintenance activities.

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There can be exceptions to the aforementioned generalities regarding body size and habitat use, especially if a primate is highly morphologically specialized (Gebo and

Chapman 1995). For example, the large-bodied Indri indri (10-15kg) is able to vertically cling and leap because its deep crouching position allows it to generate a leaping propulsion from its hip joint (Napier and Walker 1967; Pollock 1977; Demes et al. 1996).

Similarly, claws allow the small-bodied callitrichids to grasp large supports, such as tree trunks, better than similarly sized primates that lack claws (Cartmill 1974; Garber 1980,

1991). The prehensile tail of the atelines and Cebus allow these primates to suspend themselves below branches and access resources unobtainable to arboreal quadrupeds and, in the case of Ateles, Lagothrix and Brachyteles, more effectively traverse gaps in the canopy during travel (Mittermeier 1978; Cant 1986; Fontaine 1990; Garber and Rehg

1999). These post-cranial specializations allow certain primates to violate the strict association between body size and habitat use.

Specializations in Aye-aye Morphology

The most recognizable traits of aye-ayes (Daubentonia madagascariensis) are those associated with percussive foraging, specifically the large and flexible ears, continuously growing incisors, and elongated hands with a skeletal 3rd digit that has a metacarpophalangeal ball-and-socket joint (Owen 1863; Jouffroy 1975; Martin 1990;

Simons 1995; Soligo 2005). As described in Chapter 2, percussive foraging involves the echolocation and extraction of invertebrates contained within live trees, deadwood or bamboo (Petter 1962, 1977; Cartmill 1979; Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991; Sterling 1993, 1994; Erickson et al. 1998; Dominy et al. 2001). Based on results from Chapter 2 and previous work on aye-aye feeding behavior (Petter 1962,

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1977; Cartmill 1979; Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991; Sterling

1993, 1994; Erickson et al. 1998; Dominy et al. 2001), there is no question that the aforementioned traits are associated with the extraction of invertebrates. Because of their extreme nature, these traits have been the primary focus of most aye-aye positional behavior studies to date (Oxnard et al. 1990; Goix 1993; Krakauer et al. 2002; Kivell et al. 2010). In the course of these studies, it was determined that the unusual musculoskeletal morphology of its 3rd digit precludes the aye-aye from applying mechanical loads to this finger during locomotion. Consequently, many studies have examined how the aye-aye positions this finger when travelling along supports of varying inclinations (Oxnard et al. 1990; Goix 1993; Krakauer et al. 2002; Kivell et al. 2010).

The aye-aye’s 3rd digit does present an unusual problem during locomotion, but it is not the only peculiar musculoskeletal adaptation the aye-aye possesses. Indeed, the aye-aye has numerous post-cranial features that contribute to it being regarded as the most specialized of all primates (Oxnard 1981; Soligo 2005). In order to understand the adaptive context of these anatomies, it is necessary to observe aye-ayes in their natural habitat (Ripley 1967).

Aye-ayes possess an array of post-cranial features that make their skeleton

‘uniquely different’ from the rest of the entire primate order (Oxnard 1981: 7). One such feature is its intermembral index (IMI). The IMI is the ratio of forelimb to hindlimb length and is known to be a reliable indicator of locomotor tendencies (Napier and Napier

1967; Walker 1974). Leaping primates such as tarsiers and sifakas tend to have low intermembral indices indicating that the hindlimbs are longer than the forelimbs.

Suspensory primates such as hylobatids tend to have high intermembral indices

179 indicating that the forelimbs are longer than the hindlimbs. Quadrupedal primates tend to have intermediate intermembral indices indicating that the forelimb and hindlimbs are similar in length (Napier and Napier 1967; Walker 1974; Fleagle and Meldrum 1988).

The IMI of the aye-aye falls between 77 and 81 (Sterling 1993; Glander 1994). These numbers are within the range associated with quadrupedal primates (Fleagle 2013).

Further examination indicates that the aye-aye IMI is the highest of all quadrupedal lemurs and therefore, based on this metric, one would not expect the aye-ayes to be a frequent leaper (Glander 1994). While early reports suggested that aye-ayes often leaped great distances in the canopy (Petter 1962), recent positional behavior studies of aye-ayes in the disturbed forest of Mananara-Nord Biosphere Reserve (Ancrenaz et al. 1994) and in captivity (Curtis and Feistner 1994) indicate that aye-ayes are predominantly quadrupedal and do not leap often.

Soligo’s (2005) dissection of the upper extremities of an aye-aye helped identify several musculoskeletal adaptations potentially important to aye-aye locomotor and postural idiosyncrasies. The trapezius muscles at the occipital origin and the serratus anterior muscles at the inferior angle of the scapula are particularly robust (Soligo 2005).

Soligo (2005) suggests that these enlarged muscles are used to shift body weight during head-first descent of vertical supports (Soligo 2005). This robust musculature is necessary because aye-ayes are believed to be the largest primate to perform this locomotor behavior (Curtis 1992). The strong trapezius muscles are also used to brace an aye-aye’s head against a substrate while gnawing and when performing percussive foraging (Soligo 2005). Aye-ayes have strong teres major muscles to aid in clinging to and climbing on large, vertical structures (Soligo 2005). Additionally, aye-ayes possess a

180 large pars spinalis portion of the deltoid muscle, which helps to rotate the humerus laterally during invertebrate extraction (Soligo 2005). Lastly, the morphology of the hand is unusual compared to other primates and likely adapted to accommodate the elongated 3rd digit (Soligo 2005). The 3rd digit is lacking many small, intrinsic muscles, like the interossei dorsalis, while the 4th digit is the longest on the hand and contains most of the hand musculature (30-32%; Soligo 2005). The re-distribution of the muscles in the hand is thought to help the aye-aye cling to vertical substrates during percussive foraging (Soligo 2005). Aye-ayes also possess clawed digits, similar to the callitrichids, which may allow them to cling while searching for invertebrates (Soligo 2005).

However, unlike callitrichids, aye-ayes frequently cling one-handed to a substrate while percussive foraging (Soligo 2005; personal observation). The increased musculature in the 4th digit, and proportionally longer hands (Jouffroy et al. 1991) may help aye-ayes to grip vertical substrates (Soligo 2005).

Information from Soligo’s (2005) dissection suggests that the aye-aye possesses at least several post-cranial adaptations that can be linked to specific, highly specialized locomotor and postural behaviors. The ability to descend head-first on a vertical trunk is likely facilitated by the respective configurations of trapezius, serratus anterior and teres major muscles (Soligo 2005). Similarly, the configuration of shoulder (teres major) and intrinsic hand muscles likely facilitates postures such as bi-manual and uni-manual clinging (Soligo 2005). The adaptive significance of these positional behaviors and their underlying morphologies have not yet been thoroughly investigated.

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Previous Work on Aye-aye Positional Behavior

Positional studies are conducted on free-ranging populations to better understand the evolutionary relationship between morphological complexes and the habitats they are adapted to (Ripley 1967). It is undoubtedly the case that aye-aye morphology is associated with its unique positional repertoire which includes routine quadrupedalism, as well as, head-first descent, climbing, and clinging during feeding (Soligo 2005). To date there have been two studies on the positional behavior of wild aye-ayes: a three-month study in a degraded forest in Mananara-Nord Biosphere Reserve (Ancrenaz et al. 1994) and a seven-month study at Aye-aye Island in the Mananara River (Lhota et al. 2009).

The three-month study documented locomotor behavior and established that aye-ayes primarily used quadrupedal locomotion, though no attempt was made to distinguish between locomotion performed during travel and that during foraging (Ancrenaz et al.

1994). Interestingly, these authors noted that aye-ayes leaped across large gaps from quadrupedal take-off positions and vertically clung and leaped between tree trunks, sometimes using three and four trunks in succession (Ancrenaz et al. 1994). The study subjects were observed using a variety of supports across all forest levels (Ancrenaz et al.

1994). The second study was a seven-month study that focused on hand laterality (Lhota et al. 2009). In this study, it was determined that while some individuals displayed a hand preference, there did not appear to be a species-wide pattern of one hand over the other (Lhota et al. 2009). All other positional behavior studies have been conducted on captive aye-ayes (Curtis 1992; Curtis and Feistner 1994; Feistner et al. 1994). The most frequent locomotor activities of captive lemurs were quadrupedalism, followed by climbing and head-first descent (Curtis 1992; Curtis and Feistner 1994). Though leaping was relatively infrequent, aye-ayes were found to be quite adept leapers (Curtis and 182

Feistner 1994). The most frequent postural behaviors of captive aye-ayes were standing, perching and sitting (Curtis 1992; Curtis and Feistner 1994).

To summarize results from free-ranging (Ancrenaz et al. 1994; Lhota et al. 2009) and captive studies (Curtis 1992; Curtis and Feistner 1994; Feistner et al. 1994) conducted to date: (a) aye-ayes do not display a hand preference during feeding, (b) the most frequent aye-aye locomotor behavior is arboreal quadrupedalism, (c) aye-ayes are capable of a wide arrange of locomotor behaviors including head-first descent, rump-first descent, sideways descent, climbing, leaping, vertical clinging and leaping, arboreal quadrupedalism, etc., and (d) of all behaviors in the aye-aye locomotor repertoire, leaping is the least common. Nevertheless, aye-ayes are capable of performing acrobatic leaps across large gaps, including multiple leaps in succession across vertical trunks (Ancrenaz et al. 1994). Thus, aye-ayes are clearly capable of using a multitude of positional behaviors and do not appear to be limit in their ability to adapt to disturbed environments.

The Influence of Habitat on Positional Behavior

Aye-ayes living in undisturbed forest have different selective pressures than those found in disturbed forest. For instance, undisturbed forest has more large diameter trees, more continuous canopy and greater variation in support size and support density than does disturbed forest (Tomlinson and Zimmermann 1978; Grove 2002). Additionally, as described in Chapter 2, the aye-aye’s diet in undisturbed forest differs from that in disturbed forest. In Torotorofotsy, the aye-aye consumed invertebrates, especially those in live trees, more than any other resource. In comparison, in Mananara-Nord Biosphere

Reserve (Ancrenaz et al. 1994) the aye-ayes preferred food was the nectar from mature flowers of Ravenala madagascariensis and invertebrates were typically removed from

183 deadwood. Because aye-ayes in undisturbed forest remove invertebrates more from live trees than deadwood, and since live trees tend to be oriented vertically, aye-ayes in undisturbed forest are expected to perform more vertically oriented positional behaviors during foraging and feeding. Aye-ayes in a disturbed forest, on the other hand, will differ in the frequency that they perform these behaviors because deadwood can be either standing or felled (Sterling 1993, 1994a; Ancrenaz et al. 1994). Therefore, the selective pressures of an undisturbed forest should result in the aye-aye performing positional behaviors in frequencies that differ from those observed in disturbed forest. Without these baseline data on positional behavior in an undisturbed habitat, our ability to understand the relationship between aye-aye morphology and the environment in which it evolved is incomplete. Determining the positional behavior of aye-ayes in an undisturbed forest is the first step towards understanding the selective pressures that influenced aye-aye’s unique post-cranial morphology.

This Study

I collected positional behavior data during travel, foraging, and feeding on two aye-ayes in an undisturbed forest over an eight-month period. These are the first locomotor and postural data of free-ranging aye-ayes in an undisturbed, natural habitat.

My goals were (1) to establish the overall positional repertoire and habitat use profile of a free-ranging aye-aye in an undisturbed forest, (2) to establish the aye-aye’s locomotor repertoire and habitat use profile during travel, (3) to establish the locomotor behaviors and habitat use profile during foraging, and (4) to evaluate the postural repertoire and habitat use profile during feeding. These goals are achieved by collecting positional

184 behavior and habitat use data within the context of several defined maintenance activities designed to test a number of specific hypotheses.

The hypotheses are the following:

HI) Quadrupedalism will be the predominant locomotor behavior for aye-ayes during all activities. Leaping will comprise a minor component of the locomotor repertoire.

Rationale: Aye-ayes in captivity and in disturbed forest used quadrupedal locomotion more than any other locomotor behavior during travel (Curtis 1992; Ancrenaz et al. 1994; Curtis and Feistner 1994). Additionally, the aye-aye IMI is within the range of a quadrupedal primate (Glander 1994). Leaping was the least frequent locomotor behavior by aye-ayes in captivity and was only occasionally performed in disturbed forest

(Curtis 1992; Ancrenaz et al. 1994; Curtis and Feistner 1994). Additionally, the aye-aye

IMI is much higher than other quadrupedal lemurs which suggests leaping should be infrequent (Glander 1994). Large-bodied primates are less likely to leap and more likely to employ other positional behaviors such as bridging or climbing (Fleagle and

Mittermeier 1980). Since aye-ayes are a medium-size lemur species (2.5 kg) leaping should not regularly be used.

HII) Leaping will be more frequent during travel than during foraging.

Rationale: Primates tend to spend less time leaping during foraging than during travel (Fleagle and Mittermeier 1980). Locomotion during travel tends to occur over longer distances on more stable supports and with more generalized endpoints, whereas locomotion during foraging requires more precise movements over shorter distances on less stable supports due to the location of most food within arboreal habitats (Napier

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1962; Fleagle 1976a; Fleagle and Mittermeier 1980; Cannon and Leighton 1994;

McGraw 1998a, 1998b). Since leaping is used to rapidly cover large discontinuities in the canopy, it is more likely to occur during travelling than during foraging (Fleagle and

Mittermeier 1980; Schmidt 2010).

HIII) The locomotor and postural behaviors associated with forelimb anatomical idiosyncrasies, i.e., uni-manual clinging, bi-manual clinging, head-first descent, rump- first descent, sideways descent, and vertical climbing, will occur more frequently during feeding and foraging than during travel.

Rationale: In undisturbed forest, invertebrates are often extracted from trunks of live trees (Sefczek et al. 2017). Given that tree trunks are typically vertically oriented, the aye-aye will frequently have to employ positional behaviors during foraging and feeding that facilitate movement along and clinging to vertical substrates. Aye-aye musculoskeletal morphology is adapted for climbing, clinging and head-first descent

(Soligo 2005). All of these locomotor behaviors occur on substrates with an orientation greater than 45o (Hunt et al. 1996). Since the preferred resource of aye-ayes, i.e., invertebrates, is often located within vertical supports, these forelimb dominated behaviors should be frequently used during foraging and feeding. Travel, on the other hand, can occur along both vertically and horizontally oriented substrates (Fleagle 1976a;

Hunt et al. 1996; Ancrenaz et al. 1994). Quadrupedalism, a locomotor behavior performed on horizontal supports, has previously been reported as the behavior used by aye-ayes most frequently during travel (Curtis 1992; Ancrenaz et al. 1994; Curtis and

Feistner 1994). Therefore, during travel, aye-ayes will use fewer forelimb dominated

186 behaviors because there will be a greater variety of supports that do not require these specializations.

HIV) Quadrupedalism during travel will occur most often in the main canopy and along boughs.

Rationale: When arboreal primates travel, they typically select paths that promote rapid movement between locations (Fleagle and Mittermeier 1980). This is accomplished by using the forest layer with the greatest quantity of large, horizontal supports with minimal gaps through the canopy (Napier 1962; Fleagle and Mittermeier 1980; Cannon and Leighton 1994). The majority of continuous horizontal supports occur in the main canopy (Fleagle 1976a). If the configuration of supports that facilitates quadrupedalism is most common in the main canopy, and if the aye-aye prefers to travel quadrupedally, then quadrupedal locomotion should occur most often in the main canopy and along boughs.

HV) Climbing and head-first descent will occur most often in the understory and along trunks.

HVI) Uni-manual and bi-manual clinging will occur most often in the understory and along trunks.

Rationale: The aye-aye has specialized musculoskeletal morphology in their forelimbs to perform (1) vertically oriented locomotor behaviors, i.e., climbing and head- first descent, and (2) vertically oriented postural behaviors, e.g., uni-manual cling and bi- manual cling (Curtis 1992; Ancrenaz et al. 1994; Curtis and Feistner 1994; Soligo 2005).

The low, main and high canopy have trunks, boughs, branches and twigs that may be oriented vertically, horizontally and obliquely (Fleagle 1976a; Cant 1992; Hunt et al.

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1996). This means that at any canopy level an arboreal primate can select from multiple support types and use a variety of positional behaviors. In the understory, on the other hand, vertical supports are the most dominant support type and positional behaviors would be limited to vertically oriented ones (Fleagle 1976a; Cant 1992). Therefore, the climbing, head-first descent, uni-manual clinging and bi-manual clinging will occur most frequently in the understory, specifically along trunks.

HVII) Travel will occur primarily in the main canopy and along boughs.

Rationale: Regardless of size, arboreal primates should most frequently use large horizontal supports during travel because they provide the most rapid and direct path through the forest (Napier 1962; Fleagle and Mittermeier 1980; Cannon and Leighton

1994). Previous studies have determined that aye-ayes primarily travel via quadrupedal locomotion (Curtis 1992; Ancrenaz et al. 1994; Curtis and Feistner 1994).

Quadrupedalism in medium-sized primates most often occurs along horizontal supports

(Fleagle 1976a) that are large in size and occur frequently (e.g., abundance of boughs;

Cartmill and Milton 1977; Fleagle and Mittermeier 1980; Cant 1992). Since the large horizontal supports (i.e., boughs) are most common in the main canopy (Fleagle and

Mittermeier 1980), this will be the most frequently used stratum and support type used during travel.

HVIII) Foraging will occur primarily in the understory and along tree trunks.

HIX) Feeding will occur primarily in the understory and along tree trunks.

Rationale: The aye-aye’s preferred resource, invertebrates in woody substrates, can occur in any level of the forest (Sterling 1993, 1994a). Aye-aye musculoskeletal morphologies are directly related to chronic use of vertical supports (Soligo 2005). Since

188 travel should be more frequent on horizontal supports (Napier 1962; Fleagle and

Mittermeier 1980; Cannon and Leighton 1994), the frequent use of forelimb anatomical idiosyncrasies must be related to another behavior, likely foraging and feeding.

Therefore, aye-ayes should forage and feed along vertical supports more than any other support type. As tree trunks are vertically oriented more often than any other support type and because they are more common in the understory than any other forest stratum

(Fleagle 1976a; Cant 1992), aye-ayes should primarily forage and feed in the understory and on tree trunks.

HX) The supports used during travel will be smaller than those used during foraging and feeding.

Rationale: Most primates use smaller supports for feeding and foraging than for travelling because the majority of resources are located on the ends of terminal branches and twigs in the high canopy levels (Fleagle 1976a). Aye-ayes do not conform to expectations with regard to Kay’s threshold (Kay 1975; see Chapter 2) or with regard to the association between habitat size, body size and dietary diversity (McNab 1963, see

Chapter 3). Therefore, it is quite possible the relationship Fleagle (1976a) proposed between support size and maintenance activity will not apply to this primate. If forelimb anatomical idiosyncrasies are used mostly used during foraging and feeding, aye-ayes should forage and feed more on vertical supports, particularly tree trunks, than on any other support type. If aye-ayes travel primarily via quadrupedal locomotion (Curtis 1992;

Ancrenaz et al. 1994; Curtis and Feistner 1994), and quadrupedalism most often occurs along horizontal supports (Fleagle 1976a), then aye-ayes should travel along horizontal supports, especially boughs and branches, more than any other support type. Since tree

189 trunks are the largest support available on a tree, foraging and feeding should occur on larger supports than travel.

HXI) Aye-ayes travelling in undisturbed forest will use larger supports more often than aye-ayes travelling in disturbed forest.

Rationale: In general, trees in undisturbed tropical forests tend to have a greater abundance of large supports, i.e., boughs (Tomlinson and Zimmermann 1978; Grove

2002). Secondary growth that is the product of forest disturbance contains a much greater abundance of different sized supports, but a dearth of large supports because the highest canopy trees have been felled (McGraw 1996; Di Bitetti et al. 2000). If aye-ayes prefer to travel on large supports, then aye-ayes in disturbed forests will find more preferred supports to travel on.

HXII) Aye-ayes in undisturbed forest will forage and feed more often in lower forest strata than the those in disturbed forest.

Rationale: Results from a previous study indicate that aye-ayes in disturbed forest preferred to feed on Ravenala nectar, located in the highest forest level (Ancrenaz et al.

1994). Aye-ayes in undisturbed forest prefer invertebrates (see Chapter 2), which can occur at any level of the forest (Sterling 1993, 1994a). If aye-ayes in undisturbed forest spend more time feeding and foraging on vertical supports, and vertical supports are most common in the understory (Fleagle 1976a), then aye-ayes in undisturbed forest will forage and feed more often in a lower forest stratum than those in disturbed forest.

Methods

Field Site

I conducted this research from May 2017 to December 2017 in Torotorofotsy

(18o52’S, 42o22’E), Madagascar. Torotorofotsy is a natural wetland, approximately 1100

190 ha in size, and is adjacent to Mantadia National Park, approximately 10 km northwest of the town Andasibe. Torotorofotsy is the most expansive, undisturbed wetland forest in the Andasibe-Mantadia-Zahamena eastern rainforest corridor, and has a high biodiversity

(Dolch et al. 2004; Peck 2004; Wright et al. 2008). Within Torotorofotsy there are three collared aye-ayes: one adult male, one adult female and one subadult. All three individuals are outfitted with radio-collars as part of the Madagascar Biodiversity

Partnership’s aye-aye research project. Unfortunately, the male aye-aye ranged well beyond the boundaries of Torotorofotsy into territories I did not have permission to enter.

Therefore, this research focused on the positional behaviors of the adult female, Tsinjo, and her subadult male offspring, Cobalt.

Locomotor and Postural Behavioral Data Collection

In order to collect locomotor and postural data, I conducted focal follows

Mondays and Wednesdays from 18:00 to 0:00 and Tuesdays and Thursdays from 0:00 to

06:00, alternating the focal animal every Monday and Wednesday. Monday and

Wednesday follows started when Tsinjo or Cobalt exited their sleeping site. During

Tuesday and Thursday follows, I located the focal animal using the radio telemetry system. Follows ended when the focal animal reached the nest and did not move for an hour. I used the methodology outlined by Sterling (1993) which involved three researchers, myself and two Malagasy field assistants, following a focal animal. One researcher maintained light contact, defined as keeping the aye-aye within the beam of a head lamp but not closer than five meters. The other two participants positioned themselves in order to follow the animal when it ventured in a new direction (Sterling

1993).

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During night follows, I collected locomotor data using the continuous focal animal bout sampling method (Fleagle 1976a; Doran 1992). I recorded positional behavior frequencies using a bout sampling scheme modified after Fleagle (1976a). I defined a locomotor bout as a single locomotor behavior bracketed by a different locomotor behavior, a stoppage in locomotion, or an interruption of observation (Fleagle

1976a). I recorded all locomotor behaviors that occurred during two recognized maintenance activities: travel and foraging. Travel is defined as long distance movement between sleeping sites, food sources or both (Fleagle 1976a: 253). Foraging is defined as

‘movement from one feeding posture to another within one food source, during one feeding session’ (Fleagle 1976a: 254). The recognized locomotor behaviors for aye-ayes were: quadrupedal walk, quadrupedal run, leap, vertical clinging leap, bridge, descend vertically head-first, descent vertically rump-first, descend vertically sideways, or climb

(see Hunt et al. 1996 for illustrations).

Quadrupedal walk is defined as slow or medium speed, pronograde locomotion on top of a support that is less than 45o (Hunt et al. 1996: 375).

Quadrupedal run is defined as fast speed, pronograde locomotion with an irregular gate and periods of free flight, on top of a support that is less than 45o (Hunt et al. 1996: 377).

Leaping is a behavior that includes an extended period of free flight, usually across a discontinuity. In primates, most leaps originate with propulsion from the hindlimbs and conclude with the primate touching down on one or more supports using a combination of grasping behaviors (Hunt et al. 1996). Any leap that did not originate from a vertical support was considered a leap.

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Vertical clinging and leaping is a specialized form of leaping behavior that is most often seen in the forest understory where supports (tree trunks) tend to be oriented vertically. At the start of this behavior, the primate’s body is orthograde and the forelimbs and hindlimbs are used to cling to the vertical support. Take off is powered by the hindlimbs and, during the areal phase, the primate typically rotates the body in mid- air in order to position itself for landing (Hunt et al. 1996). It was not possible to reliably and consistently discern how aye-ayes typically landed; however, based on what observations were possible, I suspect in most cases aye-ayes land feet first during vertical clinging and leaping bouts. Vertical clinging and leaping is a highly-specialized locomotor behavior common to many of the lemurs of Madagascar (Napier and Walker

1967).

Bridging is a behavior used to cross small gaps as an alternative to leaping.

During a bridge, a primate uses its feet to grip a support while reaching across the gap to secure supports on the other side. The primate then pulls its body across the open space

(Hunt et al. 1996: 380-381).

Head-first vertical descent is a behavior in which all four limbs are used to progress head-first down a vertical support greater than or equal to 45o (Hunt et al. 1996:

379). Much of the effort employed by the limbs during head-first vertical descent is braking in nature in order to prevent the animal from falling down along the trunk.

Rump-first vertical descent is essentially the opposite of head-first vertical descent; the animal progresses down a vertical support with the torso in an orthograde position using the limbs in an alternating fashion to lower itself down the trunk (Hunt et al. 1996: 379).

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Sideways vertical descent is a behavior in which the animal’s vertebral column is perpendicular to the axis of the support. Using a combination of hand and foot holds, the animal gradually progresses further down the trunk (Hunt et al. 1996: 379).

Climbing is a behavior in which all four limbs are used to ascend a support greater than or equal to 45o (Hunt et al. 1996: 379). Climbing can involve a diversity of limb configurations and movements. The point at which quadrupedal locomotion on inclined supports becomes climbing has been a long-standing debate in primatology (Rose 1973;

Gebo 1992; Moffett 2000).

A locomotor bout commenced when the animal started moving and ended when a) locomotion stopped, b) a different locomotor behavior commenced, c) visibility became obstructed, or d) the focal animal moved out of sight. I recorded the distance the animal covered during each discrete locomotor behavior. I recorded forest level and information on substrate use associated with every discrete locomotor behavior. I used six categories of forest levels (Figure 4.1):

Ground is the floor of the forest.

Understory is the forest level between the ground and the lowest set of branches in the canopy.

I divided the canopy into three different layers:

Low canopy is the bottommost series of branches in the canopy.

Main canopy is the middle and largest layer of the canopy. It is positioned between the low canopy and high canopy. This is the forest stratum where most boughs are found.

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High canopy is the uppermost level of the canopy. This forest level is dominated by branches and twigs.

The emergent layer is comprised of those ‘super trees’ that have managed to extend their canopy layers above the rest of the forest canopy (Cannon and Leighton

1994).

I recognized seven support categories (Fleagle 1976a; Moffett 2000):

Trunk is a single, often vertically oriented support that comprises the axis of a tree.

Bough is a large diameter support (>10cm) that originates from the trunk.

Typically, an organism is unable to fully grasp their hand around this support type.

Branch is a medium diameter support (between 2cm and 10cm) that originates from a trunk or a bough.

Twig is a small diameter support (<2cm) deriving from branches. These are often the youngest shoots and typically the smallest supports on a tree.

Liana is a ‘vine with a woody stem’ (Moffett 2000: 581).

Bamboo is a single shoot of species of woody Poaceae.

Other is any support used that does not fit the above descriptions.

I collected data on the postures used when the aye-ayes were feeding. Postural data were collected during feeding bouts using a bout sampling technique modified after

Fleagle (1976a). I defined a postural bout as a single posture bracketed by a different posture (Fleagle 1976a). A postural bout commenced when the animal started feeding and ended when a) locomotion started, b) a different posture commenced, c) visibility became obstructed, or d) the focal animal moved out of sight. The postural repertoire

195 during a feeding includes: clinging, perching, sitting. When possible, I recorded the duration of each discrete posture used during feeding using a watch or recorded video.

Clinging is a behavior in which the torso is positioned orthograde and parallel to a vertical support, and the hindlimbs are typically in a flexed position while the feet grasp the vertical support (Hunt et al. 1996). One or both forelimbs may be used to secure the primate close to the support and I referred to these behaviors as uni-manual and bi- manual cling.

Perching is a behavior in which most of the animal is positioned on top of a horizontal support. The hindlimbs are used to secure the body’s weight while the animal leans below the support and uses its forelimbs to acquire or process a food item (Curtis

1992).

Sitting is a behavior in which the majority of the weight is born by the ischia while the torso is in a typically orthograde position (Hunt et al. 1996). The limbs can be in a variety of positions during sitting.

During the course of my observations, it became clear that the aye-aye could employ a diversity of food acquisition behaviors associated with a single posture. For example, aye-ayes frequently cling to the trunks of trees using both feet and with one hand grasping the tree bark. During such periods of what I called uni-manual clinging, the aye-aye could perform a number of feeding activities including tapping or probing with the free hand, and smelling the bark’s surface. Aye-ayes also frequently cling bi- manually to tree trunks during which time they might engage in gnawing and/or smelling.

I recognize that the sensory activities occurring during these two types of clinging are critical to understanding the feeding ecology of aye-ayes; however, for the purpose of this

196 chapter, I only recognized the type of manual clinging and did not focus on the feeding activities associated with each of these. Therefore, feeding postures included perching, bi-manual cling, uni-manual cling, hindlimb suspension, quadrupedal suspension, sit and quadrupedal stand (Figure 4.2-4.9; Hunt et al. 1996). Because feeding behaviors can change quickly, I also used a camcorder with infrared lighting to record aye-ayes during foraging and feeding bouts. I then examined the videos to more accurately evaluate feeding behaviors that occurred too quick to record during follows themselves.

Data Analysis

To determine if data were normally distributed, I performed Shapiro-Wilks tests of normality (α=0.05) on multiple data sets for both Tsinjo and Cobalt. Data for Tsinjo and Cobalt were significantly different from a normal distribution for distances covered during locomotion (W=0.8535, df=851, p<0.001; W=0.84782, df=656, p<0.001, respectively) and distances covered during foraging (W=0.89991, df=199, p<0.001;

W=0.87379, df=46, p<0.001, respectively) Therefore, non-parametric tests were used.

Locomotor behaviors used during travel and foraging and postures employed during feeding were observed at nearly every forest stratum. Therefore, I used a Kruskal-

Wallis test (α=0.05) to determine if there were significant differences in the distance associated with each locomotor behavior during travel and foraging across forest levels for both Tsinjo and Cobalt. In the case of a significant difference, I used a pairwise comparison to determine at what forest level distances differed significantly.

To determine which substrates Tsinjo and Cobalt used most frequently at each forest level during foraging and travel, I used a chi-square test (α=0.05) and then a correspondence analysis (CA). The CA is a visual representation of the chi-square test,

197 comparing all substrates and forest levels simultaneously to produce dimensions that explain the majority of the chi-square significance value and determine which categories are most associated with each other.

When determining which positional behavior had the longest average duration, I only compared those behaviors that occurred a minimum of 10 times. Those positional behaviors with fewer occurrences may have longer average durations, but because the sample is small, one very short or very long duration could skew the value.

Results

I followed Tsinjo 37 times from May to December 2017 (Table 4.1). Basic positional behavior data for Tsinjo are presented in Tables 4.2-4.5. During follows, I recorded 1084 locomotor behaviors performed by Tsinjo during travelling and foraging

(Table 4.2). Vertical clinging and leaping (25.4%), leaping (22.6%), and quadrupedal walking (16.6%) were the three most frequent locomotor behaviors performed by Tsinjo.

Of the total number of locomotor behaviors observed, 878 occurred during travel (Table

4.3). Tsinjo’s most frequent locomotor behavior during travel was vertical clinging and leaping (31.3%, Figure 4.10), but quadrupedal running averaged the longest distances per travel bout (3.1 m, Table 4.3). I also recorded 206 locomotor events during foraging

(Table 4.4). Tsinjo’s most frequent locomotor behavior during foraging was head-first descent (35.0%, Figure 4.11), which also averaged the longest distance (2.1 m, Table

4.4). I observed 883 postural behaviors (bouts) during feeding (Table 4.5). Tsinjo’s most frequent postural behavior was bi-manual cling (54.0%, Figure 4.12); however, the posture with the longest average duration was uni-manual clinging (20 s, Table 4.5).

I followed Cobalt 33 times from May to December 2017 (Table 4.1). Basic positional behavior data for Cobalt are presented in Table 4.2-4.5. During these follows, 198

I recorded 709 locomotor behaviors during travel and foraging (Table 4.2). Vertical clinging and leaping (29.5%), leaping (20.7%), and quadrupedal walk (17.3%) were the three most frequent locomotor behaviors performed by Cobalt. Of these locomotor behaviors, I observed 659 locomotor events during travel (Table 4.3). Cobalt’s most frequent locomotor behavior during travel was vertical clinging and leaping (31.7%,

Figure 4.10), but quadrupedal running averaged the greatest distance (3.3 m, Table 4.3).

I also witnessed 50 locomotor events during foraging (Table 4.4). Cobalt’s most frequent locomotor behavior during foraging was head-first descent (48.0%, Figure 4.11), which also averaged the longest distance per bout for behaviors with more than 10 occurrences

(2.3 m, Table 4.4). Lastly, I recorded 240 postural behavior events during feeding (Table

4.5). Cobalt’s most frequent posture during feeding was uni-manual cling (58.8%, Figure

4.12), which also had the longest average duration (88 s) for postures that occurred more than once (Table 4.5).

Quadrupedal Locomotion and Various Leaping Behaviors

During travel, quadrupedal walking was frequently used by both Tsinjo (15.2%) and Cobalt (16.7%), but quadrupedal running was not (1.4% and 2.3%, respectively;

Table 4.3). Vertical clinging and leaping was the most frequent behavior used by Tsinjo and Cobalt during travel (31.3% and 31.7%, respectively), with leaping the second most frequent behavior for both aye-ayes (27.9% and 22.3%, respectively; Table 4.3). Though the frequency of leaping and vertical clinging and leaping was greater than both quadrupedal walking and running, average distances covered during both quadrupedal locomotor behaviors (walk: 2.7 m; run: 3.1 m) were greater than that covered by either leaping behavior (1.9 m each) for Tsinjo (Table 4.3). Cobalt averaged greater distances

199 using quadrupedal running (3.3 m) than using either leaping (2.0 m) or vertical clinging and leaping (1.9 m), though his quadrupedal walking distances (2.0 m) were almost identical to the leaping distances (Table 4.3). These data indicate that during travel

Tsinjo and Cobalt used leaping and vertical clinging and leaping most frequently, but covered greater distances when they moved quadrupedally. There were no instances of leaping during foraging for either Tsinjo or Cobalt (Table 4.4). This is because when both aye-aye leaped, it was to move away from a foraging site, rather than to continue foraging on the same substrate.

Forelimb Dominated Positional Behaviors

Tsinjo and Cobalt performed several forelimb dominated positional behaviors, including uni-manual cling, bi-manual cling, head-first descent, rump-first descent, sideways descent and climbing. Uni-manual and bi-manual cling were used only during feeding and were exclusively postural behaviors. These two behaviors comprised 99.5% and 99.6% of all feeding behavior postures for Tsinjo and Cobalt, respectively (Table

4.5). During travel, forelimb dominated behaviors represented 21.1% and 25.8% of the overall locomotor behaviors for Tsinjo and Cobalt, respectively (Table 4.3). During foraging, forelimb dominated behaviors represented 77.2% and 74.0% of the locomotor behaviors for Tsinjo and Cobalt, respectively (Table 4.4). This indicates that the clear majority of aye-aye foraging and feeding activity documented in this study involves significant exertion of the forelimb musculature including: flexion, extension and both internal and external rotation. In contrast, the locomotor behaviors employed during travel do not appear to include as many extreme forelimb dominated activities.

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Stratum and Substrate Use: Locomotion During Travel

The frequencies that Tsinjo and Cobalt engaged in each locomotor behavior during travel at each forest level are presented in Table 4.6. Tsinjo and Cobalt used the main canopy most frequently when travelling (45.4% and 50.6%, respectively). Leaping and vertical clinging and leaping were the most frequently used locomotor behaviors during travel (Table 4.6). Tsinjo leaped and vertically clung and leaped most often in the main canopy (41.5% and 47.3%, respectively) and in nearly equal proportions within that stratum (28.6% and 29.1%, respectively; Table 4.6). Both types of leaping performed by

Cobalt occurred most often in the main canopy (vertical cling and leap: 55.8%, leap:

47.6%) though vertical clinging and leaping occurred more frequently than leaping in that stratum (34.9% and 21.0%, respectively; Table 4.6). During travel, almost every other locomotor behavior performed by Tsinjo and Cobalt occurred in the main canopy more than in other strata (Table 4.6). The exceptions for Tsinjo were: bridging, quadrupedal running, quadrupedal suspension, and sideways descent. The exceptions for Cobalt were: climbing and quadrupedal running. For Tsinjo, bridging occurred most often in the understory, quadrupedal running occurred in equal proportions in both the high canopy and main canopy, quadrupedal suspension was more frequent in the low canopy than the main canopy, and sideways descent occurred in equal proportions in the understory and main canopy. For Cobalt, climbing occurred in equal proportions in the high canopy and main canopy while quadrupedal running was more frequent in the high canopy than the main canopy. Thus, leaping and vertical clinging and leaping were the most frequently performed locomotor behaviors during travel.

The frequencies that Tsinjo and Cobalt engaged in each locomotor behavior during travel on each support are presented in Table 4.7. For both Tsinjo and Cobalt, the 201 most frequently used supports were trunks (50.7% and 51.5%, respectively), followed by branches (22.8% and 20.5%, respectively; Table 4.7). For both study subjects, vertical clinging and leaping and leaping occurred most frequently on trunks (Tsinjo: 68.7% and

50.2%, respectively; Cobalt: 64.0% and 50.3%, respectively). Though trunks are typically oriented vertically, there were many trees in Torotorofotsy whose trunks were inclined at various angles, including many at angles less than 45o. Both study animals seemed to prefer these oblique trunks for travel in the main canopy and when they moved on them they tended to do so quadrupedally. Tsinjo performed quadrupedal walking along branches (36.1%) and non-vertical trunks (33.8%) in nearly equal proportions, and less often on boughs (8.3%). Cobalt walked quadrupedally on non-vertical trunks

(40.0%) more than on branches (23.7%) and boughs (4.5%, Table 4.7). Thus, trunks, especially inclined ones, were the most frequently used support type for travel.

Stratum and Substrate Use During Foraging

The frequencies that both study animals foraged at each forest level are presented in Table 4.8. Tsinjo used the main canopy (33.0%), understory (29.1%) and low canopy

(30.6%, Table 4.8) in nearly equal proportions. Cobalt foraged most often in the main canopy (46.0%), followed by the high canopy (32.0%, Table 4.8). Head-first descent was the most frequently performed locomotor behavior during foraging for both Tsinjo and

Cobalt (35.0% and 48.0%, respectively; Table 4.8). For Tsinjo, climbing was the second most frequent locomotor behavior during foraging (29.1%), followed by quadrupedal walking (22.5%, Table 4.8). Cobalt’s second most frequent locomotor behavior during foraging was quadrupedal walking (26.0%), followed by climbing (20.0%, Table 4.8).

For Tsinjo, head-first descent occurred in similar proportions in the low canopy (34.7%)

202 and main canopy (30.6%), followed by the understory (27.8%). Tsinjo climbed most often in the understory (38.3%), followed by the main canopy (33.3%) and low canopy

(21.7%, Table 4.8). Cobalt descended head-first most often in the main canopy (45.9%) and high canopy (33.3%) and climbed most often in the main canopy (50.0%, Table 4.8).

The frequencies that both study animals foraged on each support type are presented in Table 4.9. Trunks were the most frequently used support during foraging for both Tsinjo and Cobalt (55.8% and 60.0%, respectively), followed by bamboo for Tsinjo

(29.1%) and boughs for Cobalt (14.0%, Table 4.9). Most of the climbing (73.3%) and head-first descent (51.4%) performed by Tsinjo occurred on trunks. Most of the climbing

(70.0%) and head-first descent (66.7%) performed by Cobalt also occurred on trunks.

Thus, the most frequent positional behaviors used by both study animals during foraging were vertically oriented locomotor modes: head-first descent and climbing. Both of these locomotor behaviors occurred most frequently on trunks in the main canopy.

Stratum and Substrate Use: Postures During Feeding

The frequencies that Tsinjo and Cobalt used different postures at each stratum during feeding are presented in Table 4.10. For Tsinjo, bi-manual cling was the most frequent posture (53.5%) followed by uni-manual cling (45.7%, Table 4.10). Cobalt clung uni-manually more often than bi-manually (58.0% and 41.6%, respectively).

Tsinjo’s feeding occurred most often in the understory (41.7%) followed by the main canopy (29.4%) and low canopy (23.8%). Cobalt fed most often in the main canopy

(62.1%) and high canopy (27.6%, Table 4.10). During feeding, Tsinjo used bi-manual and uni-manual cling most often while in the understory (41.7% and 42.5%, respectively;

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Table 4.10). Cobalt used bi-manual and uni-manual cling most often while in the main canopy (60.4% and 63.8%, respectively; Table 4.10).

Postural and support use data during feeding for both aye-ayes are reported in

Table 4.11. Tsinjo and Cobalt fed most often on tree trunks (73.1% and 69.5%, respectively; Table 4.11). During feeding, the most frequently employed postures by both aye-ayes were uni-manual and bi-manual cling (Tsinjo: 45.7% and 53.5%, respectively; Cobalt: 58.0% and 41.6%, respectively; Table 4.11). Both postures were performed most often on tree trunks by Tsinjo (uni-manual: 77.4%, bimanual: 70.7%) and Cobalt (uni-manual: 70.2%, bi-manual: 69.4%, Table 4.11). Tsinjo also used bamboo frequently for bi-manual and uni-manual clinging during feeding (16.6% and

10.4%, respectively; Table 4.11). Thus, Tsinjo and Cobalt most often fed on vertical trunks using one or two-handed clinging postures.

Forest Stratum and Substrate Use by Tsinjo During Travel, Foraging and Feeding

The frequencies that Tsinjo traveled on each support type and at each forest level are presented in Table 4.12. Similarly, the frequencies that Tsinjo foraged and fed on each support type and at each forest level are presented in Tables 4.13 and 4.14, respectively.

During travel, Tsinjo used tree trunks more frequently than any other support type

(50.7%, Table 4.6). Branches (22.8%) and lianas (10.7%) were the other two most common supports used by Tsinjo when travelling (Table 4.6). Tsinjo traveled most often in the main canopy (45.4%), followed by the low canopy (20.9%), high canopy (18.0%) and understory (15.6%, Table 4.12). Only once was Tsinjo observed travelling in the emergent layer.

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There were significant associations between Tsinjo’s support use and forest level use during travel (chi-square test: χ2=168.6186, df=20, p<0.001; Figure 4.13). In other words, the use of a specific support type is associated with a specific forest level. The first dimension of the CA for support use and forest level use explains 88.5% of the chi- square significance value and the second dimension explains an additional 10.6% of the value; thus 99.1% of the associations between forest stratum use and support use by

Tsinjo during travel are represented by this CA (Figure 4.13). Trunks and bamboos were most often used when Tsinjo was in the low canopy and, to a lesser extent, the understory

(Figure 4.13). Boughs and lianas were used most often when she was in the main canopy, with branches being used in similar proportions in the main and high canopy levels (Figure 4.13). Tsinjo only used the emergent layer on one occasion and this appears to be an outlier because its association with the various supports is not as strong as the association between other supports and other forest levels (Figure 4.13).

Collectively, these data suggest that when Tsinjo was travelling in the main canopy she used a combination of horizontal supports (bough and branches) and supports without uniform orientations (lianas). When Tsinjo traveled in the understory and low canopy, she tended to use vertically oriented supports (trunks and bamboo).

Tsinjo foraged most often on trunks (55.8%) followed by bamboo (29.1%, Table

4.13). Tsinjo foraged in the main canopy (33.0%), low canopy (30.6%) and understory

(29.1%, Table 4.13) in similar proportions. Tsinjo was never observed foraging on the ground or in the emergent layer.

There were significant associations between Tsinjo’s support use and forest level use during foraging (χ2=57.8151, df=16, p<0.001; Figure 4.14). That is, the use of a

205 specific support type is associated with a specific forest level. The first dimension explains 87.1% of the chi-square significance value and the second dimension explains an additional 8.1% of the value; thus, 95.2% of the associations between forest stratum use and support use by Tsinjo during foraging are represented by this CA (Figure 4.14).

Trunks and bamboo were most often used when Tsinjo was in the understory, low canopy and main canopy (Figure 4.14). Boughs and branches were used most often when she was in the high canopy and, to a lesser extent, the main canopy (Figure 4.14). Thus,

Tsinjo foraged mostly on trunks and bamboo between the understory and main canopy.

She expanded her support use to include branches and boughs as she foraged in higher strata.

When feeding, Tsinjo used tree trunks most frequently (73.1%), followed by bamboo (13.6%), branches (7.3%) and boughs (4.3%, Table 4.14). Tsinjo fed most frequently in the understory (41.7%), followed by the main canopy (29.4%), the low canopy (23.8%) and the high canopy (5.1%, Table 4.14). Tsinjo was never observed feeding on the ground or in the emergent layer.

Forest Stratum and Substrate Use by Cobalt During Travel, Foraging and Feeding

Data on Cobalt’s support and forest level use during travel are presented in Table

4.15. Cobalt’s support and forest level use during foraging and feeding are presented in

Tables 4.16 and 4.17, respectively.

Cobalt used tree trunks more frequently than any other support during travel

(51.5%, Table 4.9). Branches (20.5%) and lianas (14.3%) were the other two most common supports used by Cobalt when travelling (Table 4.15). Cobalt most often used the main canopy for travel (50.6%), followed by the high canopy (29.0%), and low

206 canopy (12.9%, Table 4.15). Though Cobalt was never observed travelling on the ground, he did use the emergent layer twice.

There were significant associations between Cobalt’s support use and forest level use during travel (χ2=115.7229, df=25, p<0.001; Figure 4.15). In other words, the use of specific support types is associated with a specific forest stratum. While the first dimension of the CA between support use and forest level use only accounted for 78.5% of the chi-square significance value, the second dimension explained an additional 14.4% of the value. Therefore, 92.9% of the associations between forest stratum use and support use by Cobalt during travel are represented by this CA (Figure 4.15). Trunks and boughs were most often used when Cobalt was in the main canopy and, to a lesser extent, in the low canopy (Figure 4.15). Branches and twigs were used most often when he was in the high canopy (Figure 4.15). These data suggest that Cobalt typically traveled in the main and high canopy using a vareity of support types.

When foraging, Cobalt used trunks more often than any other support (60.0%), with boughs (14.0%) the second most frequent support (Table 4.16). Cobalt mainly used the main canopy when foraging (46.0%), followed by the high canopy (32.0%) and low canopy (14.0%, Table 4.16). Cobalt was never observed using the ground or emergent layer when foraging.

There were significant associations between Cobalt’s support use and forest level use during foraging (χ2=47.72102, df=15, p<0.001) with the use of a specific support type associated with a specific forest level (Figure 4.16). The first dimension of the CA for support use and forest level explains 88.1% of the chi-square significance value and the second dimension accounts for an additional 10.5% of the value. Thus, 98.6% of the

207 associations between forest stratum use and support use by Cobalt during foraging are represented by this CA (Figure 4.16). Trunks and bamboo were most often used when

Cobalt was in the main canopy and, to a lesser extent, trunks were also used when Cobalt was in the low canopy (Figure 4.16). Boughs and branches were used most often when he was in the high canopy (Figure 4.16). Thus, these data suggest that when Cobalt was foraging in the main and high canopy, he used a combination of vertical supports (trunks and bamboo) and horizontal supports (boughs and branches). Though infrequent, when he foraged in the low canopy it was typically on trunks.

When feeding, tree trunks were Cobalt’s most frequently used support (69.5%), followed by branches (7.4%), and bamboo (6.6%, Table 4.17). The main canopy was the most frequently used forest stratum for feeding by Cobalt (62.1%), followed by the high canopy (27.6%), and the low canopy (7.0%, Table 4.17). Cobalt rarely fed in the understory and was never observed feeding on the ground or in the emergent layer.

Distances Covered by Tsinjo During Travel

The distances Tsinjo covered with her various locomotor behaviors during travel were significantly different from each other (Kruskal-Wallis test: χ2=155.13, df=9, p<0.001). A pairwise comparison showed that distances covered during vertical clinging and leaping (p<0.001) and leaping (p<0.001) were significantly less than those covered during quadrupedal walking (Table 4.18). Tsinjo also covered significantly less distance using vertical clinging and leaping (<0.001) and leaping (0.002) compared to quadrupedal running (Table 4.18).

The distance covered by a given locomotor behavior varied according to the stratum in which it occurred. For Tsinjo, there were significant differences in the

208 distances covered by bridging (Kruskal-Wallis test: χ2= 9.5508, df=3, p=0.023), leaping

(χ2=20.441, df=3, p<0.001) and vertical clinging and leaping (χ2=13.919, df=3, p=0.003) depending on the forest level. A pairwise comparison showed that, on average, bridging distances (Table 4.19) were greater in the low canopy than in the understory (p=0.019).

Another pairwise comparison showed that, on average, leaping distances (Table 4.20) were greater in the understory than in the main canopy (p=0.001), in the understory compared to the high canopy (p=0.014) and in the low canopy compared to the main canopy (p=0.012). A third pairwise comparison indicated that, on average, vertical clinging and leaping distances (Table 4.21) were greater in the understory compared to the low canopy (p=0.016), main canopy (p=0.004), and high canopy (p=0.020).

Distances Covered by Tsinjo During Foraging

There were significant differences in the distances covered during foraging depending on the forest level. Distances covered during climbing varied significantly with forest level (Kruskal-Wallis test: χ2=11.23, df=3, p=0.010). A pairwise comparison indicated that climbing distances were, on average, greater in the understory than in the main canopy (p=0.036; Table 4.22). There was also a significant difference in the distance Tsinjo covered during head-first descent depending on the forest level

(χ2=9.0108, df=3, p=0.029). A pairwise comparison indicated that distances covered during head-first descent were, on average, greater in the understory than in the main canopy (p=0.018; Table 4.23).

Distances Covered by Cobalt During Travel

The distances Cobalt covered with his various locomotor behaviors during travel were significantly different from each other (Kruskal-Wallis test: χ2=48.121, df=9,

209 p<0.001). A pairwise comparison showed that average distances covered during quadrupedal running were significantly greater than those averaged during quadrupedal walking (p=0.004), vertical clinging and leaping (p<0.001) and leaping (p<0.001; Table

4.24). Cobalt also covered significantly greater distances on average using vertical clinging and leaping compared to head-first descent (p=0.044). Cobalt covered significantly greater distances using vertical clinging and leaping (p=0.004) and leaping

(p=0.039) than climbing (Table 4.24).

The average distance covered by Cobalt during travel via climbing (χ2=8.7093, df=4, p=0.069), descending head-first (χ2=5.6516, df=4, p=0.227), leaping (χ2=3.5592, df=3, p=0.313), quadrupedal running (x2=4.8114, df=3, p=0.186), quadrupedal walking

(χ2=0.86976, df=3, p=0.833), and vertical clinging and leaping (χ2=4.2639, df=3, p=0.234) did not vary according to the stratum in which it occurred.

Differences in Distances Covered by Cobalt When Foraging

The average distance covered by Cobalt during foraging via climbing (χ2=5.1171, df=3, p=0.163), descending head-first (χ2=5.3341, df=3, p=0.149), and quadrupedal walking (χ2=2.2153, df=2, p=0.330) were not significant different in the various forest levels.

Discussion

Aye-ayes appear to violate many of the relationships between body size, diet and foraging ecology that have predictive power with other primates. For instance, insectivorous primates should not exceed 500 g (Kay 1975) yet, on average, aye-ayes weigh 2.5 kg and primarily consume invertebrates. Additionally, organisms with extensive home ranges normally have very diverse diets incorporating multiple resources

(McNab 1963). Aye-aye home ranges can exceed 700 ha, yet over 99% of their diet 210 consists of two resources: invertebrates and Canarium seeds (see Chapters 2 and 3). As has been discussed in Chapters 2 and 3, aye-ayes must be very efficient at locating, harvesting, and consuming invertebrates in order to sustain themselves on a primarily insectivorous diet (Gaulin 1979). Their percussive foraging behavior and the unique morphologies associated with it help to explain the aye-aye’s efficiency. However, these are only part of the overall behavioral and morphological complexity (Soligo 2005) that allow this medium-sized primate to survive on a diet comprised mainly of invertebrates.

The positional repertoire explored here further elucidates the extent to which aye- ayes are specialized to consume primarily invertebrates. Soligo (2005) suggested that the musculoskeletal peculiarities in the aye-aye’s forelimbs (i.e., configurations of trapezius, serratus anterior, teres major and intrinsic hand muscles) were adapted to improve positional behaviors that facilitate acquisition of invertebrates. As I discuss below, based on the positional behaviors of Tsinjo and Cobalt, this appears to be the case. Aye-ayes must travel, forage and feed in nearly every forest stratum because as their preferred food, invertebrates, occurs in discrete patches at all levels of the forest (Sterling 1993,

1994a; Chapter 3). Both Tsinjo and Cobalt used a wide breadth of locomotor behaviors during travel. During foraging they displayed fewer behaviors, most of which involved moving up and down vertical trunks. These behaviors include climbing, head-first descent, rump-first descent, and sideways descent. Feeding postures were even more limited, with two postures, i.e. uni-manual and bi-manual clinging, accounting for over

99% of the maintenance activity. Many of these positional behaviors require the aye-aye to use its peculiar forelimb anatomy (Soligo 2005). Thus, the aye-aye’s invertebrate

211 specializations include not only the percussive foraging adaptations they are so well known for, but also many elements of their positional repertoire.

Locomotor Behavior During Travel and Foraging

My first hypothesis was that quadrupedalism would be the predominant locomotor behavior during all activities and that leaping would comprise a minor component of the locomotor repertoire. For both Tsinjo and Cobalt, the most frequent locomotor behavior was vertical clinging and leaping (25.4% and 29.5%, respectively) followed by leaping (22.6% and 20.7%, respectively; Table 4.2). Quadrupedal walking was the third most common locomotor behavior for both aye-ayes (16.6% and 17.3%,

Table 4.2). Therefore, the data do not support my hypothesis that quadrupedal locomotion will be the most common locomotor behavior. This is unexpected because

(1) the IMI of aye-ayes is greater than that of other leaping quadrupedal lemurs (Glander

1994), (2) Ancrenaz and colleagues (1994) found that quadrupedal walking was the most common form of locomotion for aye-ayes in Mananara-Nord Biosphere Reserve, and (3)

Curtis (1992) had reported that leaping was not a frequent behavior.

Though quadrupedal walking and running were not the most frequent locomotor behaviors, they did average the longest distances covered by Tsinjo (2.5 m and 3.1 m, respectively; Table 4.2). Cobalt averaged the longest distances via quadrupedal running

(3.3 m, Table 4.2). However, his average quadrupedal walking distance (1.4 m) was shorter than his average distance travelled using leaping (2 m) and vertically clinging and leaping (1.9 m, Table 4.2). This means that when Cobalt travelled long distances, he tended to do so using quadrupedal running, which is a pattern that has been documented in many arboreal primates (Fleagle and Mittermeier 1981; Fleagle 1984). When he

212 travelled short distances, his locomotor behavior was more varied. While some of his play behavior may have been misidentified as travel, this does not appear to comprise a majority of the short distance movements. Instead it may be that, as a subadult, Cobalt was not yet capable of sustained, long distance travel. That is, he may have been performing short travel bouts, frequently stopping to rest, forage or feed. When he did travel long distances, it was often at the end of the night when travelling to the next sleeping site. It is likely Cobalt’s quadrupedal walking distances will increase with age.

Between May and December of 2017, Cobalt was over a year old and would consistently travel away from the nesting tree. This means he was traveling between trees, likely using quadrupedal running, and not play moving within a single canopy. However, his travel distances and monthly home range size were smaller than Tsinjo’s until approximately August of 2017 (see Chapter 5). This may indicate that Cobalt’s quadrupedal walking distance were shorter on average because he did not travel as much as Tsinjo until later in the study. Though quadrupedal walking was not the most frequent locomotor behavior for either aye-aye, quadrupedal locomotion may be important for the aye-ayes to cover longer distances.

It should also be noted that bridging might be more frequent than I observed. For

Tsinjo, bridging averaged the shortest distance of all locomotion during travel (0.7 m).

However, Tsinjo used this behavior at nearly every level of the forest, particularly the understory and low canopy. When at lower strata, she would typically grab a neighboring liana, bamboo, or small diameter trunk as supports for bridging. Assuming

Tsinjo was attempting to move as quietly as possible, it is likely she chose to cross small gaps using bridging versus leaping not only because it saved energy but also because it

213 was less noisy. During some follows, there were times when Tsinjo would suddenly leave an area where she had been feeding, and move away very quickly as we scrambled after her. We attempted to keep up and although we assumed from the telemetry data that she was moving, we were not always confident this was the case because, in certain instances, we lost visibility. One hypothesis we can formulate is that the pathways and behaviors Tsinjo chose during travel are those that allowed her to better remain hidden.

Indeed, it was often the rustling of leaves and branches following a leap (versus a more cryptic bridging episode) that would cue me into the animal’s location. While bridging, quadrupedal walking and quadrupedal running behaviors might be more important than these data indicate, this does not detract from the importance of both vertical clinging and leaping and leaping to the aye-aye’s movement through the undisturbed forest. Future research should examine macro-habitat differences to determine what habitat qualities

(i.e. number of large diameter trees, density of trees with >10 cm diameter at breast height, percent canopy cover, etc.) influence the frequencies of the various positional behaviors during aye-aye locomotion.

Leaping During Travel and Foraging

My second hypothesis was that leaping would be more frequent during travel than during foraging. During travel, vertical clinging and leaping and leaping were the two most frequent locomotor behaviors for Tsinjo (31.3% and 27.9%, respectively) and

Cobalt (31.7% and 22.3%, respectively; Table 4.3). These behaviors never occurred during foraging. Therefore, my hypothesis is supported. Vertical clinging and leaping and leaping likely were more efficient forms of locomotion to get from one feeding site to another, as one of these two locomotor behaviors typically occurred following feeding

214 bouts. After removing an invertebrate from a tree, aye-ayes would often leave via leaping or vertical clinging and leaping in order to (a) move to another feeding site within

10 m of their location or (b) start moving through the forest. If the aye-aye started to travel, it would usually leap or vertically leap to another tree, climb to the main canopy and start to walk quadrupedally. There were also several instances when an aye-aye would vertically cling and leap between three to five successive tree trunks before ascending into the canopy. In contrast, leaping and vertical clinging and leaping were never used during foraging. Instead, the aye-aye normally stayed on the same substrate during foraging and then ended the foraging bout with a leap or vertical cling and leap away from the support.

Anatomical studies indicate that aye-ayes have a higher IMI than other quadrupedal lemurs, suggesting that leaping should not be a common behavior (Oxnard

1981; Glander 1994). It is possible the use of the uni-manual clinging posture during feeding (discussed below) necessitates the longer forelimb lengths and that higher IMI is less reflective of locomotion tendencies for this species. Since leaping propulsion is generated from the hindlimbs (Napier and Walker 1967), future research should examine if aye-aye hindlimb musculature is also specialized to accommodate leaping despite their high IMI value.

Forelimb Dominated Positional Behaviors

My third hypothesis was that locomotor and postural behaviors associated with anatomical idiosyncrasies of the forelimbs would occur more frequently during feeding and foraging than during travel. The forelimb dominated locomotor behaviors include head-first descent, rump-first descent, sideways descent, and climbing. The forelimb

215 dominated postural behaviors include uni-manual clinging and bi-manual clinging.

These locomotor behaviors comprised 21.1% of Tsinjo’s overall travel and 25.8% of

Cobalt’s overall travel (Table 4.3). The percentage of forelimb dominated behaviors increased dramatically during foraging and feeding, comprising 77.2% and 99.5% of

Tsinjo’s respective behaviors and 74.0% and 99.6% of Cobalt’s respective behaviors

(Tables 4.4 and 4.5). Therefore, my hypothesis that aye-aye forelimb idiosyncrasies were used more for foraging and feeding than for travel is supported.

As Soligo (2005) suggested, many of the aye-aye’s forelimb peculiarities likely evolved to enable foraging and feeding on invertebrates. Both aye-ayes would typically forage and feed for invertebrates along a vertical support, whether a live tree, deadwood or bamboo. Though most foraging and feeding occurred on tree trunks, even foraging and feeding in the main or high canopy typically was done on vertically oriented branches. Indeed, it was exceedingly rare for either aye-aye to forage along a horizontal support. Furthermore, as will be discussed below, foraging and feeding occurred at nearly every forest level. This usually resulted in the aye-aye searching the length of a tree trunk or snag, continually climbing, clinging, and descending the same tree until it was satisfied that the resources inside were depleted.

The aye-aye’s elongated 3rd digit with a specialized metacarpophalangeal joint, its continuously growing incisors and large, bat-like ears (Owen 1863; Jouffroy 1975;

Cartmill 1979; Martin 1990; Simons 1995) are some of its well-known apomorphies.

Clawed digits, increased musculature in the elongated 4th digit, and robust shoulder and back muscles are all used to support the aye-ayes body weight along a vertical structure

(Soligo 2005). Considering how frequently I observed aye-ayes clinging to a trunk head-

216 down with some or all of the body’s momentum being checked by action of the hindlimbs, it would not be surprising if the aye-aye also possessed specializations of the hindlimb musculature that enable these striking positional behaviors. As proposed in

Chapter 2 and earlier in this chapter, the aye-aye’s total positional repertoire likely evolved to enable the aye-aye to more efficiently locate, harvest and consume invertebrates throughout the habitat, and, in so doing, violate Kay’s threshold (Gaulin

1979).

The aye-ayes in Torotorofotsy ate invertebrates frequently, but it was not their only resource. Canarium seeds in ripe fruit were another important food and were typically consumed between January and May (see Chapter 2). Canarium feeding was only briefly recorded during this positional behavior study: once in the month of May

2017. When Tsinjo fed on a Canarium seed in ripe fruit, she would do so while perched on a bough or branch. Tsinjo would hold the fruit in two hands, gnaw into the fruit and seed, and extract the endocarp by probing with her 3rd digit. Once the endocarp was removed, she would let the seed drop to the forest floor, walk quadrupedally along the support to forage for another fruit, and return to her perch spot to feed again. Though she gnawed and probed like she did when feeding on invertebrates, these behaviors all occurred from a perched position and likely did not require the same use of either the musculature adaptations of the forelimbs or clawed digits that the four clinging positions did. Given that other resources, such as Ravenala nectar (Sterling 1993, 1994a; Ancrenaz et al. 1994; Randimbiharinirina et al. 2018) are included in the diets of aye-ayes in disturbed forests, future research should investigate what behaviors during foraging and feeding are used to access these food items.

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Stratum Use, Support Use and Positional Behaviors

My fourth hypothesis was that quadrupedalism during travel would occur most often in the main canopy and along boughs. For both Tsinjo and Cobalt, quadrupedal walking was practiced most frequently in the main canopy. During quadrupedalism,

Tsinjo most often used branches while Cobalt most often used inclined trunks (Tables 4.6 and 4.7). Therefore, this hypothesis is only partially supported. It is not surprising that aye-ayes use the main canopy for travel, as large, horizontal supports that facilitate rapid locomotion are most available in this stratum (Fleagle and Mittermeier 1980). However, it was unexpected that boughs were not the most frequently used support, and even more surprising that the adult used smaller supports than the subadult. Young and smaller- bodied primates are expected to use a greater variety of supports because they are not as hindered by problems of weight-to-branch size ratios (Fleagle and Mittermeier 1980;

Brezanson 2017). What might account for this contradiction?

I suspect the younger aye-aye used larger supports than the adult for two reasons.

First, because Cobalt was not an adult he may not have been fully confident in his locomotor abilities to use smaller supports. A number of studies on positional behavior ontogeny have shown that support use and positional diversity changes with age (Ripley

1967; Wunderlich et al. 2011; Dunham 2015; Bezanson 2017); however, the positional repertoire typically decreases with age (Bezanson 2017). This is not the case with Cobalt who had less positional variation than Tsinjo. It is possible that a fully developed musculoskeletal anatomy is necessary to perform the vast array of positions an aye-aye typically exhibits, particularly vertically oriented behaviors and that Cobalt has not completely developed his adult physiology. If Cobalt’s locomotor repertoire was not yet fully developed, it would be safer for him to remain on large, stable supports where he 218 could practice his behaviors and become more secure in his locomotion. I will discuss the development of Cobalt’s behaviors further in Chapter 5. Secondly, because Cobalt was younger and often parked at a nesting site, the use of larger supports may have helped him remain cryptic, thus acting as a predator avoidance strategy. When an organism uses smaller supports, there is greater risk of the support bending or breaking

(Grand 1972; Fleagle and Mittermeier 1980; Cant 1992), often creating significant noise and detectable movement as the supports deform. Use of larger supports, on the other hand, could help the young aye-aye remain quiet and attract less attention. Future research should examine at what age an aye-aye starts to use supports of various sizes more consistently.

My fifth hypothesis was that climbing and head-first descent would occur most often in the understory and along trunks. This is because the understory is dominated by vertically oriented supports which require increased amounts of climbing and other vertically directed locomotor behaviors. Furthermore, opportunities for quadrupedalism are similarly limited in the understory. Therefore, this hypothesis was partially supported. During travel, Tsinjo and Cobalt used trunks most often during head-first descent (Table 4.7). Cobalt used trunks most often for climbing when travelling (Table

4.7). When foraging, Tsinjo typically climbed in the understory (Table 4.8). Both aye- ayes foraged most frequently along trunks, usually by climbing or descending head-first

(Table 4.9). Thus, these data support many previous studies that locomotor behaviors are, to a large extent, determined by the support environment (Fleagle 1976b; Charles-

Dominique 1977; Kinzey et al. 1977; Fleagle and Mittermeier 1980, 1981).

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On the other hand, some results did not support my hypothesis. During travel, climbing and head-first descent by both Tsinjo and Cobalt occurred most frequently in the main canopy rather than the understory (Table 4.6). For Cobalt, climbing and head- first descent during foraging also occurred most frequently in the main canopy (Table

4.8). These results are unexpected because most climbing and head-first descent should occur in the understory where most supports are oriented vertically and because there are ample opportunities for quadrupedalism in the main canopy due to the abundance of horizontal supports. When Tsinjo climbed during travel, it tended to occur on branches rather than trunks (Table 4.7). This is because Tsinjo tended to select branches with significant inclinations, possibly related to surprisingly high levels of leaping during travel and the support characteristics that facilitate leaping (Demes et al. 1995). Demes et al. (1995) showed that vertical clingers and leapers used supports that sway when they apply force as these substrates facilitate leaping. It is likely the aye-ayes can similarly deform these inclined branches to assist with leaping behaviors. Finally, head-first descent during foraging was most frequent in the low canopy for Tsinjo (Table 4.8). This is likely a sampling issue and a function of the fact that trunks extend from the understory into the low main canopy. Thus, some of the associations established between locomotion and forest strata in other primate taxa do not apply in this context.

Continuing to explore vertically oriented positional behaviors, my sixth hypothesis was that uni-manual cling and bi-manual cling would most often occur in the understory and along trunks. This is because these two positional behaviors are predicted to be determined by two things, (A) the abundance of invertebrates in vertical trunks and

(B) the positional behaviors required to negotiate these substrates during feeding. My

220 results supported my hypothesis for Tsinjo but not for Cobalt. Tsinjo fed most often on trunks in the understory and when she did, the most frequently employed postures were uni-manual and bi-manual cling (Table 4.10 and 4.11). Cobalt also preferred to feed on trunks; however, the preferred forest level for feeding was the main canopy (Table 4.10 and 4.11). Interestingly, the overwhelming majority of feeding postures employed by

Cobalt were uni-manual and bi-manual cling (Table 4.11). This is surprising given that the main canopy contains so many more horizontal supports which, presumably, eliminates the need for clinging postures. Thus, despite the plethora of horizontal supports, Cobalt appeared to still prefer trunks and vertically-oriented branches. This may suggest that the aye-ayes have evolved to feed in vertically oriented positions. As has been previously suggested, aye-ayes may be filling the ecological niche of a woodpecker on Madagascar, positioning themselves along tree trunks to harvest invertebrates (Petter 1977; Cartmill 1979).

The lesson from evaluating hypotheses five and six is that, vertically oriented positional behaviors are critical because they allow aye-ayes to more efficiently forage and feed on invertebrates. Tsinjo’s preference for vertical trunks in the understory, combined with Cobalt’s preference for similar supports in the main canopy, indicate that aye-ayes are supremely adapted to exploit trunks, regardless of the forest level. Whether occupying the understory or the main canopy, or performing vertically oriented locomotor or postural behaviors, both aye-ayes almost always used trunks. As will be discussed later, Cobalt’s predominant use of the main canopy may be reflective of his youth, i.e., he was not yet confident enough to descend to lower forest levels in order to feed and forage.

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Maintenance Activities, Strata Use and Substrate Use

My seventh hypothesis was that travel would occur primarily in the main canopy and along boughs. Travel by Tsinjo and Cobalt did occur largely in the main canopy

(45.4% and 50.6%, respectively); however, the most frequently used supports during travel by both individuals were trunks and branches rather than boughs (Tsinjo: 50.7% and 22.8%, respectively; Table 4.12; Cobalt: 51.5% and 20.5%, respectively; Table 4.15).

This was the case in the main canopy as well as several other forest levels. Thus, the results did not support my hypothesis. The correspondence analysis (CA) of forest level and support type during travel yielded some strong associations, such as that between high canopy and twigs for both aye-ayes. However, these relationships are not necessarily meaningful because in some cases the sample sizes are extremely low (Figure

4.13 and 4.15). For example, the CA could yield a very strong correspondence between a support and strata level, but if those do not occur often, it may not be biologically relevant. Potentially more important are cases where there are strong associations with large sample sizes or, conversely, large sample sizes but no associations. In the latter case, it is the lack of association that is more informative. For Tsinjo, low canopy, main canopy, bamboo, trunks, boughs and lianas all have weak associations during travel despite being the most frequently used support types and forest levels (Figure 4.13).

Similarly, during travel by Cobalt, there were weak associations involving the main canopy and trunks, the most common stratum and support type (Figure 4.15). These data indicate that these aye-ayes are using a variety of support types in almost every forest level. For Tsinjo, when she occupies the understory, low canopy and main canopy, she uses trunks, bamboo, lianas and boughs. Cobalt uses trunks, boughs, and branches when in the low canopy, main canopy and high canopy. As will be discussed later, Cobalt’s 222 predominant use of the main canopy may be reflective of his youth. I will therefore focus on the behavior of Tsinjo as this is likely more reflective of aye-aye behaviors because

(1) organisms spend much greater time as adults than as juvenile, and (2) the adult post- crania are what we normally look at when evaluating positional behavior and limb anatomy.

Based on the support types and forest levels used during travel, it is evident that

Tsinjo most often used vertically oriented supports, especially in the main canopy where nearly 50% of all observed travel behaviors occurred (Table 4.12). While she travelled mostly along trunks, branches at an angle greater than 45o were also commonly used.

Indeed, travel along vertical supports was not limited to the main canopy. The understory, low canopy and high canopy were all used in relatively similar proportions and, except for in the high canopy, trunks were the preferred support type (Table 4.12).

Therefore, while the aye-aye does typically travel as other primates do, i.e., in the main canopy (Fleagle 1976a; Fleagle and Mittermeier 1980), they are more expansive in their strata and support type use. This of course is exemplified by the fact that they frequently travel along trunks using vertically oriented locomotor behaviors. Indeed, the variation in support use across nearly every stratum may be a strategy for improving foraging and feeding efficiency.

Many primates consume resources that are located in the main and high canopy, thus when they travel to a new resource tree, they select routes between points in a forest which allow the most rapid, uninterrupted movement to a food item (Garber 1980). This is particularly important when feeding on highly clumped and patchy resources, such as ripe fruit, that can be depleted quickly. The aye-aye, on the other hand, prefers a resource

223 that is cryptic, hidden beneath a woody substrate, making this food inaccessible to other lemurs. Despite a lack of inter-specific competition, and even though invertebrates seem to be ubiquitous in the habitat, rapid locomotion between distant feeding locations was still a common occurrence when following Tsinjo. This long-distance travelling may be due to (a) Tsinjo avoiding depletion of invertebrates within a portion of her habitat, (b) difficulty distinguishing between locomotor and foraging events, or (c) invertebrates occurring in non-traditional patches.

Exploring the first possibility, Tsinjo travelled throughout her habitat, consuming invertebrates across her entire range (see Chapter 3). While she occasionally revisited a feeding site on consecutive nights, she did not occupy the same area for longer than two nights before moving elsewhere. Thus, she may have been attempting to avoid depleting resources within a portion of her habitat. However, given the cryptic nature of her preferred resource, it seems unlikely that an organism could determine when this food item would be depleted.

Alternatively, expanding on the second possibility, the high frequency of vertical support use during travel may be a sampling error. Tsinjo seemed capable of travelling quickly while still evaluating the availability of invertebrates within a support.

Therefore, it may be that travelling and foraging occur simultaneously and that distinguishing between the two may not be possible. This begs the question, how do aye- aye know when and where to stop travelling and start foraging/feeding? Unfortunately, this is beyond the scope of this research. Future research should explore the use of visual, auditory and olfactory cues by aye-ayes when travelling to determine how they identify a resource tree.

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The third possibility may be that invertebrates appear ubiquitous but actually occur in a non-traditional patch, i.e., multiple resources located in different trees within a short distance of each other, thus requiring the aye-aye to travel long distances between patches. Patches are typically thought of as a single tree as these can produce multiple fruits, flowers and/or leaves (Garber 1980; Janson and Chapman 1999). Thus, when a primate travels between patches, it is often long distances between individual trees

(Garber 1980; Oates 1987; Janson and Chapman 1999; Buzzard 2006). It is possible that invertebrate patches do not conform to the typical patch pattern, but rather occur across multiple trees within a small area. This would explain why the aye-aye travelled long distances between patches, resulting in a large home range, but fed and foraged across several supports within a short distance of each other. Furthermore, fruits, flowers and leaves are cyclical, meaning food availability within a given tree fluctuates with the seasons (van Schaik et al. 1993; van Schaik and Pfannes 2005). Primates can return to a patch during the appropriate season knowing that resources will again be available

(Garber 1987). Conversely, invertebrates: 1) seem to be available throughout the year, 2) do not occur in large clumps (often fewer than 10 in a tree), and 3) might not reuse the same host tree. By using multiple support types and inclinations throughout all forest levels, aye-aye may be increasing the likelihood of encountering an embedded larva during travel. Future research should examine how invertebrates are dispersed throughout the forest to determine if they are truly ubiquitous or patchy.

My eighth hypothesis was that foraging would occur primarily in the understory and along trunks. Ultimately, the data supported my hypothesis for Tsinjo (Table 4.13;

Figure 4.14) but not for Cobalt (Table 4.16; Figure 4.16). Tsinjo foraged on trunks in

225 relatively equal proportions in the understory, low canopy and main canopy, while Cobalt most frequently foraged along trunks in the main canopy (Tables 4.13 and 4.16). Results from the correspondence analysis provide additional information. For Tsinjo, the associations between bamboo, trunks and forest stratum were not strong, though trunks and bamboo were more closely related to the use of the understory, main canopy and low canopy than any other stratum (Figure 4.14). The CA for Cobalt’s foraging, on the other hand, showed a strong association between trunks and the main canopy (Figure 4.16).

This indicates that both aye-ayes spent most of their time foraging on trunks; however, while Cobalt concentrated his foraging in the main canopy, Tsinjo would search the length of trunks from the understory into the main canopy. I will discuss this in conjunction with feeding behaviors in further detail below.

My ninth hypothesis was that feeding would occur primarily in the understory and along trunks. This hypothesis was partially supported. Tsinjo (41.7%, Table 4.14) fed mostly in the understory while Cobalt (62.1%, Table 4.17) fed mostly in the main canopy. Both aye-ayes fed primarily on trunks (73.1% and 69.5%, respectively; Tables

4.14 and 4.17). This phenomenon is interpretable by understanding how aye-ayes feed and forage (explored in hypothesis 8). The fact that Tsinjo foraged in relatively equal amounts in the understory, low canopy and main canopy suggests that invertebrates are evenly dispersed throughout Torotorofotsy. Though Tsinjo fed more frequently in the understory, possibly indicating a greater abundance of invertebrates at that stratum, feeding still occurred in the other strata with some regularity. This underscores the point that Tsinjo was continually searching multiple forest levels for her preferred resource. In other words, Tsinjo explored much of the vertical dimension, from the understory

226 through the main canopy, as well as the horizontal space, e.g., between trees, while searching for invertebrates. This appeared to result in a large amount of ‘wasted’ movement: searching the length and circumference of a trunk with few successful feeding events during foraging. If Tsinjo experienced the most feeding success in the understory she would be expected to focus her foraging efforts in this stratum. Instead, she regularly foraged and fed in the low and main canopy in addition to using the understory. It is likely Tsinjo was maximizing her energetic gain by moving along the length of the trunk and exhausting a host tree before leaving. Future research should explore the metabolic rates of aye-ayes to determine how they are able to maintain positive net energy despite frequent movement during foraging.

Cobalt’s feeding and foraging behaviors did not always align with those of Tsinjo.

While both aye-ayes fed and foraged most frequently on trunks, Cobalt did so more often in the main and high canopy while Tsinjo most frequently used the understory and low canopy. Feeding in the high canopy is typical for most primates, since the majority of resources are located on the terminal ends of branches and twigs (Fleagle 1976a).

However, Cobalt fed more often from trunks, not branches and twigs. Since trunks are more prominent in the lower forest levels, feeding should happen more frequently in these low strata, as it did with Tsinjo. Instead, Cobalt used trunks higher in the forest to feed on invertebrates.

One explanation for this high frequency of feeding and foraging by Cobalt in the main and high canopy is that invertebrates are more prevalent in this level than at any other. However, if that were the case, Tsinjo likely would not have fed as much in the understory. Instead, the frequent use of main canopy by Cobalt may be due to his age.

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Cobalt fed on the same support types as Tsinjo, but at different forest levels. Nocturnal and solitary parked infants are often kept in higher levels of the canopy as an anti- predation strategy (Ebensperger and Blumstein 2006; Tecot et al. 2012). Not only are predation pressures greater along the ground than in the canopy (Janson and van Schaik

1993), but nested, solitary infants will be less conspicuous and thus attract less attention of potential predators (Ebensperger and Blumstein 2006; Tecot et al. 2012). Thus, Cobalt would be expected to spend more time in the main and high canopy because it is a safer location (Janson and van Schaik 1993).

Furthermore, mothers who park their infants will occasionally return to parking sites to check on their offspring (Kappeler 1998; Ross 2001). If Tsinjo was returning to care for Cobalt, she would have had to move into the main canopy to do so. Therefore, the frequency with which Tsinjo foraged in the main canopy may be partially skewed.

That is, she constantly fed and foraged for invertebrates, often in the lower strata, and occasionally returned to the nest site to check on her infant, located higher in the forest.

Alternatively, she often climbed to the top of a tree and perform a contact call, presumably directed at her offspring. This behavior was a better alternative to travelling back to the nest because it allowed Tsinjo to conserve energy, especially later in this study when Cobalt began to travel greater distances. Future research should examine if there is a relationship between maintenance activities, strata use and support use for an adult female aye-aye without an infant, or for an adult male aye-aye.

My tenth hypothesis was that supports used during travel would be smaller than those used during foraging and feeding. Tsinjo and Cobalt both used tree trunks more than any other support during travel (50.7% and 51.5%; Tables 4.12 and 4.15,

228 respectively). Branches were the second most frequently used substrate during travel for both Tsinjo (22.8%) and Cobalt (20.5%). During foraging, Tsinjo and Cobalt used trunks more than any other support (55.8% and 60.0%; Tables 4.13 and 4.16, respectively).

However, whereas Tsinjo’s second most frequently used support for foraging was bamboo (29.1%), Cobalt’s secondary support was boughs (14.0%). The support type most often used by Tsinjo and Cobalt during feeding was trunks (73.1% and 69.5%;

Tables 4.14 and 4.17, respectively). Again, the second most frequently used support during feeding for Tsinjo was bamboo (13.6%), whereas Cobalt’s was branches (7.4%).

In summation, the data did not support my hypothesis because the most frequently used support for travel, foraging and feeding by both aye-ayes was trunks. Indeed, the second most frequently used support by Tsinjo during travelling, foraging and feeding may not have been different either. Though the bamboo diameters were not measured, most bamboo available in the forest was likely under 10 cm in diameter, which is the upper size limit for branches used in this study. Therefore, Tsinjo likely travelled, foraged and fed on similarly sized primary and secondary supports.

Most primates travel along horizontal supports because they are abundant and facilitate rapid locomotion between distant end points (Fleagle and Mittermeier 1980).

When foraging and feeding, the majority of primates use smaller supports because most resources, i.e., fruits, flowers and leaves, are located on the ends of terminal branches and twigs in the high canopy levels (Grand 1972; Fleagle 1976a; Cant 1992). However, as with many other facets of aye-aye ecology, such as the association between habitat size, body size and dietary diversity (McNab 1963; Kay 1975; see Chapter 2 and Chapter 3), relationships between maintenance activities and support characteristics do not conform

229 to expectations. The predominant use of trunks by both aye-ayes for all positional behaviors is likely due to invertebrates being available at every level of the forest

(Sterling 1993, 1994a). Aye-ayes not only have to move horizontally through the forest to reach new feeding sites, but they also must explore the vertical space to maximize their invertebrate consumption. In other words, aye-ayes not only forage and feed on trunks, where most invertebrates appear to be located (Hanks 1999), they may also travel along or between trunks, via climbing, descent, leaping or vertical clinging and leaping, in order to reach the next feeding location.

While Tsinjo and Cobalt both predominantly foraged and fed on trunks, there was a difference in their second most frequently used support. Tsinjo used bamboo, which are frequently vertically oriented and medium-size in diameter (greater than 2 cm but less than 10 cm). Cobalt, on the other hand, used boughs which were often horizontally oriented and greater than 10 cm in diameter. Indeed, 84.9% of Tsinjo’s foraging and

86.7% of her feeding occurred along vertically oriented supports, i.e., trunks and bamboo

(Tables 4.13 and 4.14). For Cobalt, only 62.0% of foraging and 76.1% of feeding occurred along these two support types (Tables 4.16 and 4.17). It is possible elements of the full positional repertoire, especially those behaviors involving vertically oriented movements and postures, were not yet fully developed in the sub-adult aye-aye

(behavioral development will be explored further in Chapter 5). This is supported further by considering the difference in understory use by the two aye-ayes. The understory is dominated by vertical supports and fewer horizontal substrates. For this reason, opportunities for quadrupedalism are very limited and the most obvious option for moving between trees at this forest level is to pass between trunks using leaping or

230 bridging, or moving up and down trunks using climbing or various kinds of descent. In nearly all of these cases, the positional behaviors used are those that are vertically oriented in nature.

Tsinjo used the understory during travel (15.6%, Table 4.12), foraging (29.1%,

Table 4.13), and feeding (41.7%, Table 4.14) more frequently than Cobalt (7.2%, 8.0%, and 3.3%, respectively; Tables 4.15, 4.16, and 4.17). It is likely that the younger aye-aye was not confident in its ability to perform vertically-oriented behaviors or could not leap as far and instead remained in the high forest levels which more readily facilitates horizontal behaviors. Future research should examine how long it takes for young aye- aye to become proficient at vertically-oriented locomotor and postural behaviors.

Comparing Disturbed Forest and Undisturbed Forest Behaviors

My last two hypotheses focused on the differences between behaviors in undisturbed forest and disturbed forest and I address them together. Hypothesis eleven was that aye-ayes travelling in undisturbed forest would use larger supports more often than aye-ayes travelling in disturbed forest. Hypothesis twelve was that aye-ayes in undisturbed forest would forage and feed more often in the lower forest stratum than those in the disturbed forest.

Ancrenaz et al. (1994) found that aye-ayes in the disturbed forest of Mananara-

Nord Biosphere Reserve typically used medium (3-10 cm; 42.2%) and small (< 3 cm;

32.2%) supports for their locomotor behaviors (Ancrenaz et al. 1994). Feeding was not observed in the understory and rarely seen in the low canopy (0.8%) or main canopy

(3.1%). Rather, these aye-ayes fed most often in the high canopy (24.2%). The aye-ayes in the undisturbed forest of Torotorofotsy primarily used trunks when travelling (Tsinjo:

231

50.7%, Table 4.12; Cobalt: 51.5%, Table 4.15). Therefore, the hypothesis that aye-ayes in undisturbed forest would use larger supports during travel than aye-ayes in disturbed forest is supported. When feeding, Tsinjo was most often in the understory (41.7%,

Table 4.14); however, Cobalt fed most frequently in the main canopy (62.1%, Table

4.17). Thus, the hypothesis that aye-ayes in undisturbed forest would feed more often in the lower forest levels than aye-ayes in disturbed forest is partially supported.

Ancrenaz and colleagues (1994) clearly indicate that the behaviors of their study subjects at Mananara-Nord Biosphere Reserve were heavily influenced by a reliance on the nectar of Ravenala madagascariensis flowers. Ravenala flowers occur in the high canopy layers which explains why aye-ayes at Mananara-Nord concentrated their locomotor and feeding behaviors in the high canopy. In contrast, the Torotorofotsy aye- ayes prefer invertebrates which are located in tree trunks in nearly every forest level.

Therefore, travel and feeding tends to occur along trunks between the understory and the main canopy where invertebrates are most likely to be encountered. For instance, an aye- aye preferentially feeding on Ravenala flowers may only have to remain in the high canopy to locate its next feeding site. In contrast, an aye-aye that preferentially consumes invertebrates is less likely to remain in one forest layer because its next resource could be in a lower forest stratum.

It has been suggested that aye-aye locomotor diversity helps them access a multitude of resources (Ancrenaz et al. 1994). Based on my findings in Chapter 2 and here, it seems more likely that the locomotor diversity of aye-ayes helps them access a plethora of invertebrates and can be used to access other resources when necessary.

Future research should examine if support and forest strata use change in other forests

232 where (a) invertebrates are not the primary resource or (b) forest composition is significantly different, i.e., the dry western forests of Madagascar.

Conclusion

Though actual frequencies of quadrupedal locomotion may be greater than those reported in this study, vertical clinging and leaping and leaping were very important forms of locomotion for both Tsinjo and Cobalt. This is true not only in the understory, but also in the lower and main canopy. In addition to being contrary to previous findings which suggested that leaping was not a major part of the aye-aye locomotor repertoire

(Curtis 1992; Curtis and Feistner 1994), my results provide an important baseline for comparison across forests. As mentioned in Chapter 2, invertebrate foraging, particularly in live trees, appears to be more important in the undisturbed Torotorofotsy forest than in disturbed forest. It is possible that the lower frequencies of leaping and vertical clinging and leaping reported from other forests is also related to this difference in diet. In

Mananara-Nord Biosphere Reserve, Ravenala madagascariensis nectar was the aye-aye’s preferred resource (Ancrenaz et al. 1994). Ravenala flowers are located in the main or high canopy levels which would explain why aye-ayes focusing on this resource spent more time in the higher levels of the forest (Ancrenaz et al. 1994). Additionally, higher forest levels are characterized by a variety of support types and sizes as well as a generally more continuous support environment (Fleagle 1976a; Cannon and Leighton

1994). This architectural milieu ultimately results in higher frequency of quadrupedal locomotion. In contrast, aye-ayes in Torotorofotsy prefer invertebrates which can be found at all forest levels. Consequently, aye-ayes are more likely to use a greater diversity of locomotor behaviors during feeding and foraging, including leaping and

233 vertically cling and leap, as they search the understory, low and main canopies for their preferred resource.

The frequency that I observed head-first descent and climbing, particularly during foraging, supports the notion that aye-ayes actively search every forest level in order to procure their primary food source. In fact, the wide array of positional behaviors I observed during feeding and foraging are reflective of the fact that invertebrates are not only located in falled tree trunks along the ground. On the contrary, invertebrates at

Torotorofotsy were found at every forest layer and in multiple support types. Cobalt and

Tsinjo located, harvested and extracted invertebrates from all of these forest levels which required a great diversity of positional behaviors. By successfully doing so, they were able to sustain their body size and large home ranges with such a specialized diet (as discussed in Chapters 2 and 3). Even aye-ayes’ quadromanous suspensory positional behavior, which was rarely used, is likely to aid in the search for invertebrates, allowing them to explore underneath branches and boughs. Previous research suggests that aye- ayes are capable of a wide range of positional behaviors which are beneficial in accessing a diverse array of resources (Curtis 1992; Ancrenaz et al. 1994; Curtis and Feistner

1994). The data here highlight how the positional behaviors of the Torotorofotsy aye- ayes help them efficiently locate and consume invertebrates, in particular, rather than a more diverse array of resources. It seems likely that, as human disturbance increased, the aye-aye’s positional repertoire has been repurposed for survival in less pristine habitats, i.e., accessing resources other than invertebrates.

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Table 4.1 Number of follows conducted each month for Tsinjo and Cobalt in Torotorofotsy, Madagascar.

Month Tsinjo Cobalt Follows Follows May 2017 5 4 June 2017 4 2 July 2017 7 5 August 2017 3 7 September 2017 5 2 October 2017 6 4 November 2017 5 4 December 2017 2 5 Total 37 33

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Table 4.2 Total occurrences, average distances, and frequency of occurrence for all locomotor behaviors by Tsinjo and Cobalt between May 2017 and December 2017.

Tsinjo Cobalt

Positional Average Average Frequency Frequency Behavior Occurrences Distance Occurrences Distance (%) (%) (m) (m)

Bridge 25 0.7 2.3% 4 1.5 0.6% Climb 153 2.4 14.1% 77 1.2 10.9%

Head-first 153 2.4 14.1% 118 1.8 16.6% descent

Leap 245 1.9 22.6% 147 2 20.7%

Quadrupedal 12 3.1 1.1% 15 3.3 2.1% run

Quadrupedal 3 2 0.3% 4 1.4 0.6% suspend

Quadrupedal 180 2.5 16.6% 123 1.4 17.3% walk

Rump-first 28 1.2 2.6% 12 1.2 1.7% descent

Sideways 10 1.3 0.9% N/A N/A N/A descent

Vertical leap 275 1.9 25.4% 209 1.9 29.5%

Total 1084 100.0% 709 100.0%

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Table 4.3 Number of times observed, average distance, and frequency of each locomotor behavior during travel by Tsinjo and Cobalt between May 2017 and December 2017 in Torotorofotsy, Madagascar.

Tsinjo Cobalt Travel Occurrences Average Frequency Occurrences Average Frequency Distance (%) Distance (%) (m) (m) Bridge 25 0.7 2.8% 4 1.5 0.6% Climb 93 2.7 10.6% 67 2.4 10.2% Head-first 81 2.7 9.2% 94 2.4 14.3% descent Leap 245 1.9 27.9% 147 2.0 22.3% Quadrupedal 12 3.1 1.4% 15 3.3 2.3% run Quadrupedal 3 2.0 0.3% 5 1.4 0.7% suspend Quadrupedal 133 2.7 15.2% 110 2.0 16.7% walk Rump-first 7 2.7 0.8% 8 2.6 1.2% descent Sideways 4 2.3 0.5% N/A N/A N/A descent Vertical leap 275 1.9 31.3% 209 1.9 31.7% Total 878 100.0% 659 100.0%

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Table 4.4 Number of time observed, average duration, and frequency of each foraging behavior by Tsinjo and Cobalt between May 2017 and December 2017 in Torotorofotsy, Madagascar.

Tsinjo Cobalt Occurrences Average Frequency Occurrences Average Frequency Foraging Distance (%) Distance (%) (m) (m) Climbing 60 2.0 29.1% 10 1.8 20.0% Head-first 72 2.1 35.0% 24 2.3 48.0% descent Quadrupedal 47 1.9 22.8% 13 2.1 26.0% walk Rump-first 21 0.7 10.2% 3 3.3 6.0% descent Sideways 6 0.7 2.9% N/A N/A N/A descent Total 206 100.0% 50 100.0%

238

Table 4.5 Number of times observed, average duration, and frequency of each postural behavior during feeding by Tsinjo and Cobalt between May 2017 and December 2017 in Torotorofotsy, Madagascar.

Tsinjo Cobalt Feeding Occurrences Average Frequency Occurrences Average Frequency Duration (%) Duration (%) (s) (s) Bi-manual 477 16 54.0% 98 55 40.8% cling Perch 3 6 0.4% N/A N/A N/A Quadrupedal 1 40 0.1% 1 120 0.4% suspend Uni-manual 402 20 45.5% 141 88 58.8% cling Total 883 100% 240 100%

239

Travel Understory Low Canopy Main Canopy High Canopy Emergent Layer TOTAL Bridge 12 8 4 1 0 25 (48.0%, 8.8%) (32.0%, 4.3%) (16.0%, 1.0%) (4.0%, 0.6%) (0.0%, 0.0%) 2.8% Climb 18 16 34 24 1 93 (19.4%, 13.1%) (17.2%, 8.7%) (36.6%, 8.5%) (25.8%, 15.2%) (1.0%, 100.0%) 10.6% Head-first Descent 12 20 40 9 0 81 (14.8%, 8.8%) (24.7%, 10.9%) (49.4%, 10.0%) (11.1%, 5.7%) (0.0%, 0.0%) 9.2% Leap 27 55 116 47 0 245 (11.0%, 19.7%) (22.5%, 29.9%) (47.3%, 29.1%) (19.2%, 29.8%) (0.0%, 0.0%) 27.9% Quadrupedal Run 0 0 6 6 0 12 (0.0%, 0.0%) (0.0%, 0.0%) (50.0%, 1.5%) (50.0%, 3.8%) (0.0%, 0.0%) 1.4% Tsinjo Quadrupedal Suspend 0 2 1 0 0 3 (0.0%, 0.0%) (66.7%, 1.1%) (33.3%, 0.3%) (0.0%, 0.0%) (0.0%, 0.0%) 0.3% Quadrupedal Walk 5 26 78 24 0 133 (3.8%, 3.6%) (19.5%, 14.1%) (58.6%, 19.5%) (18.1%, 15.2%) (0.0%, 0.0%) 15.1% Rump-first Descent 1 2 4 1 0 8 (12.5%, 0.7%) (25.0%, 1.1%) (50.0%, 1.0%) (12.5%, 0.6%) (0.0%, 0.0%) 0.9% Sideways Descent 2 0 2 0 0 4 (50.0%, 1.5%) (0.0%, 0.0%) (50.0%, 0.5%) (0.0%, 0.0%) (0.0%, 0.0%) 0.5% Vertical Leap 60 55 114 46 0 275 (21.8%, 43.8%) (20.0%, 29.9%) (41.5%, 28.6%) (16.7%, 29.1%) (0.0%, 0.0%) 31.3% TOTAL 137 (15.6%) 184 (20.9%) 399 (45.4%) 158 (18.0%) 1 (0.1%) 879

Continued

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Table 4.6 Continued

Travel Understory Low Canopy Main Canopy High Canopy Emergent Layer TOTAL Bridge 1 1 2 0 0 4 (25.0%, 2.1%) (25.0%, 1.2%) (50.0%, 0.6%) (0.0%, 0.0%) (0.0%, 0.0%) 0.6% Climb 8 5 26 26 2 67 (11.9%, 17.0%) (7.5%, 5.9%) (38.8%, 7.8%) (38.8%, 13.6%) (3.0%, 100.0%) 10.2% Head-first Descent 7 13 49 25 0 94 (7.5%, 15.0%) (13.8%, 15.3%) (52.1%, 14.7%) (26.6%, 13.1%) (0.0%, 0.0%) 14.3% Leap 8 20 70 49 0 147 (5.5%, 17.0%) (13.6%, 23.5%) (47.6%, 21.0%) (33.3%, 25.7%) (0.0%, 0.0%) 22.3% Quadrupedal Run 1 2 5 7 0 15 Cobalt (6.7%, 2.1%) (13.3%, 2.3%) (33.3%, 1.5%) (46.7%, 3.7%) (0.0%, 0.0%) 2.3% Quadrupedal Suspend 0 0 2 3 0 5 (0.0%, 0.0%) (0.0%, 0.0%) (40.0%, 0.6%) (60.0%, 1.6%) (0.0%, 0.0%) 0.8% Quadrupedal Walk 4 10 57 39 0 110 (3.6%, 8.5%) (9.1%, 11.8%) (51.8%, 17.1%) (35.5%, 20.4%) (0.0%, 0.0%) 16.7% Rump-first Descent 0 0 6 2 0 8 (0.0%, 0.0%) (0.0%, 0.0%) (75.0%, 1.8%) (25.0%, 1.0%) (0.0%, 0.0%) 1.2% Sideways Descent N/A N/A N/A N/A N/A N/A Vertical Leap 18 34 116 40 0 208 (8.7%, 38.3%) (16.3%, 40.0%) (55.8%, 34.9%) (19.2%, 20.9%) (0.0%, 0.0%) 31.6% TOTAL 47 (7.2%) 85 (12.9%) 333 (50.6%) 191 (29.0%) 2 (0.3%) 658

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Table 4.7 Locomotor behavior and support use during travel by Tsinjo and Cobalt between May and December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a locomotor behavior across the various supports. Underlined % represents the frequency of each locomotor behavior on a single support type. Bold % represents the frequency of locomotor behavior use or support use.

Travel Trunk Bough Branch Twig Liana Bamboo TOTAL

Bridge 15 2 5 1 2 0 25 (60.0%, 3.4%) (8.0%, 3.6%) (20.0%, 2.5%) (4.0%, 1.9%) (8.0%, 2.1%) (0.0%, 0.0%) 2.8% Climb 30 6 36 9 10 2 93 (32.2%, 6.7%) (6.4%, 10.7%) (38.7%, 18.0%) (9.7%, 16.7%) (10.8%, 10.6%) (2.2%, 6.9%) 10.6% Head-first 35 2 10 4 24 6 81 Descent (43.2%, 7.8%) (2.5%, 3.6%) (12.4%, 5.0%) (4.9%, 7.4%) (29.6%, 25.5%) (7.4%, 20.7%) 9.2% Leap 123 22 54 16 17 13 245 (50.2%, 27.6%) (9.0%, 39.3%) (22.0%, 27.0%) (6.5%, 29.6%) (7.0%, 18.1%) (5.3%, 44.8%) 27.9% Quadrupedal 2 1 4 2 3 0 12 Run (16.7%, 0.4%) (8.3%, 1.8%) (33.3%, 2.0%) (16.7%, 3.7%) (25.0%, 3.2%) (0.0%, 0.0%) 1.4% Tsinjo Quadrupedal 1 0 2 0 0 0 3 Suspend (33.3%, 0.2%) (0.0%, 0.0%) (66.7%, 1.0%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) 0.3% Quadrupedal 45 11 48 8 19 2 133 Walk (33.8%, 10.1%) (8.3%, 19.6%) (36.1%, 24.0%) (6.0%, 14.8%) (14.3%, 20.2%) (1.5%, 6.9%) 15.1% Rump-first 3 0 0 0 5 0 8 Descent (37.5%, 0.7%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) (62.5%, 5.3%) (0.0%, 0.0%) 0.9% Sideways 3 0 1 0 0 0 4 Descent (75.0%, 0.7%) (0.0%, 0.0%) (25.0%, 0.5%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) 0.5% Vertical 189 12 40 14 14 6 275 Leap (68.7%, 42.4%) (4.4%, 21.4%) (14.5%, 20.0%) (5.1%, 25.9%) (5.1%, 15.0%) (2.2%, 20.7%) 31.3% TOTAL 446 (50.7%) 56 (6.4%) 200 (22.8%) 54 (6.1%) 94 (10.7%) 29 (3.3%) 879

Continued

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Table 4.7 Continued

Travel Trunk Bough Branch Twig Liana Bamboo TOTAL Bridge 2 1 0 0 1 0 4 (50.0%, 0.6%) (25.0%, 2.6%) (0.0%, 0.0%) (0.0%, 0.0%) (25.0%, 1.1%) (0.0%, 0.0%) 0.6% Climb 24 6 18 7 10 2 67 (35.8%, 7.1%) (9.0%, 15.4%) (26.9%, 13.3%) (10.4%, 17.5%) (14.9%, 10.6%) (3.0%, 18.2%) 10.2% Head-first 55 5 10 5 18 1 94 Descent (58.5%, 16.2%) (5.3%, 12.8%) (10.6%, 7.4%) (5.3%, 12.5%) (19.2%, 19.2%) (1.1%, 9.1%) 14.3% Leap 74 11 36 11 13 2 147 (50.3%, 21.8%) (7.5%, 28.2%) (24.5%, 26.7%) (7.5%, 27.5%) (8.8%, 13.8%) (1.4%, 18.2%) 22.3% Quadrupedal 5 3 5 1 0 1 15 Run (33.3%, 1.5%) (20.0%, 7.7%) (33.3%, 3.7%) (6.7%, 2.5%) (0.0%, 0.0%) (6.7%, 9.0%) 2.3% Cobalt Quadrupedal 0 0 2 1 1 1 5 Suspend (0.0%, 0.0%) (0.0%, 0.0%) (40.0%, 1.5%%) (20.0%, 2.5%) (20.0%, 1.1%) (20.0%, 9.1%) 0.8% Quadrupedal 44 5 30 8 21 2 110 Walk (40.0%, 13.0%) (4.5%, 12.8%) (27.3%, 22.2%) (7.3%, 20.0%) (19.1%, 22.3%) (1.8%, 18.2%) 16.7% Rump-first 2 1 2 0 3 0 8 Descent (25.0%, 0.6%) (12.5%, 2.6%) (25.0%, 1.5%) (0.0%, 0.0%) (37.5%, 3.2%) (0.0%, 0.0%) 1.2% Sideways N/A N/A N/A N/A N/A N/A N/A Descent Vertical 133 7 32 7 27 2 208 Leap (6.4%, 39.2%) (3.3%, 17.9%) (15.4%, 23.7%) (3.3%, 17.5%) (13.0%, 28.7%) (1.0%, 18.2%) 31.6% TOTAL 339 (51.5%) 39 (6.0%) 135 (20.5%) 40 (6.0%) 94 (14.3%) 11 (1.7%) 658

243

Table 4.8 Foraging behavior and forest strata use by Tsinjo and Cobalt between May and December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a locomotor behavior across the forest strata. Underlined % represents the frequency of each locomotor behavior within a forest stratum. Bold % represents the frequency of locomotor behavior use or stratum use.

Foraging Understory Low Canopy Main Canopy High Canopy TOTAL Climb 23 13 20 4 60 (38.3%, 38.3%) (21.7%, 20.6%) (33.3%, 29.4%) (6.7%, 26.7%) 29.1% Head-first Descent 20 25 22 5 72 (27.8%, 33.3%) (34.7%, 39.7%) (30.6%, 32.4%) (6.4%, 33.3%) 35.0% Quadrupedal Walk 1 15 26 5 47 Tsinjo (2.1%, 1.7%) (32.0%, 23.8%) (55.3%, 38.2%) (10.6%, 33.3%) 22.8% Rump-first Descent 11 9 0 1 21 (52.4%, 18.3%) (42.8%, 14.3%) (0.0%, 0.0%) (4.8%, 6.7%) 10.2% Sideways Descent 5 1 0 0 6 (83.3%, 8.4%) (16.7%, 1.6%) (0.0%, 0.0%) (0.0%, 0.0%) 2.9% TOTAL 60 (29.1%) 63 (30.6%) 68 (33.0%) 15 (7.3%) 206 Climb 2 1 5 2 10 (20.0%, 50.0%) (10.0%, 14.3%) (50.0%, 21.7%) (20.0%, 12.5%) 20.0% Head-first Descent 2 3 11 8 24 (8.3%, 50.0%) (12.5%, 42.8%) (45.9%, 47.8%) (33.3%, 50.0%) 48.0% Cobalt Quadrupedal Walk 0 2 6 5 13 (0.0%, 0.0%) (15.4%, 28.6%) (46.1%, 26.1%) (38.5%, 31.2%) 26.0% Rump-first Descent 0 1 1 1 3 (0.0%, 0.0%) (33.4%, 14.3%) (33.3%, 4.4%) (33.3%, 6.3%) 6.0% Sideways Descent N/A N/A N/A N/A N/A TOTAL 4 (8.0%) 7 (14.0%) 23 (46.0%) 16 (32.0%) 50

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Table 4.9 Foraging behavior and support use by Tsinjo and Cobalt between May and December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a locomotor behavior across the various supports. Underlined % represents the frequency of each locomotor behavior on a single support type. Bold % represents the frequency of locomotor behavior use or support use.

Foraging Trunk Bough Branch Twig Liana Bamboo TOTAL Climb 44 2 4 0 1 9 60 (73.3%, 38.2%) (3.3%, 14.3%) (6.7%, 44.5%) (0.0%, 0.0%) (1.7%, 14.3%) (15.0%, 15.0%) 29.1% Head-first 37 5 2 0 2 26 72 Descent (51.4%, 32.1%) (6.9%, 35.7%) (2.8%, 22.2%) (0.0%, 0.0%) (2.8%, 28.6%) (36.1%, 43.3%) 35.0% Quadrupedal 21 6 3 1 3 13 47 Tsinjo Walk (44.7%, 18.3%) (12.8%, 42.9%) (6.4%, 33.3%) (2.1%, 100%) (6.4%, 42.8%) (27.6%, 21.7%) 22.8% Rump-first 8 1 0 0 1 11 21 Descent (38.0%, 7.1%) (4.8%, 7.1%) (0.0%, 0.0%) (0.0%, 0.0%) (4.8%, 14.3%) (52.4%, 18.3%) 10.2% Sideways 5 0 0 0 0 1 6 Descent (83.3%, 4.3%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) (16.7%, 1.7%) 2.9% TOTAL 115 (55.8%) 14 (6.8%) 9 (4.4%) 1 (0.5%) 7 (3.4%) 60 (29.1%) 206 Climb 7 1 0 0 2 0 10 (70.0%, 23.3%) (10.0%, 14.3%) (0.0%, 0.0%) (0.0%, 0.0%) (20.0%, 40.0%) (0.0%, 0.0%) 20.0% Head-first 16 3 2 1 2 0 24 Descent (66.7%, 53.3%) (12.5%, 42.8%) (8.3%, 40.0%) (4.2%, 50.0%) (8.3%, 40.0%) (0.0%, 0.0%) 48.0% Quadrupedal Cobalt 5 2 3 1 1 1 13 Walk (38.5%, 16.7%) (15.4%, 28.6%) (23.0%, 60.0%) (7.7%, 50.0%) (7.7%, 20.0%) (7.7%, 100.0%) 26.0% Rump-first 2 1 0 0 0 0 3 Descent (66.7%, 6.7%) (33.3%, 14.3%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) 6.0% Sideways N/A N/A N/A N/A N/A N/A N/A Descent TOTAL 30 (60.0%) 7 (14.0%) 5 (10.0%) 2 (4.0%) 5 (10.0%) 1 (2.0%) 50

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Feeding Understory Low Canopy Main Canopy High Canopy TOTALS Bi-manual Cling 196 116 129 29 470 (41.7%, 53.4%) (24.7%, 55.5%) (27.4%, 50.0%) (6.2%, 64.4%) 53.5% Perch 0 0 6 0 6 (0.0%, 0.0%) (0.0%, 0.0%) (100.0%, 2.3%) (0.0%, 0.0%) 0.7% Tsinjo Quadrupedal Suspend 0 0 1 0 1 (0.0%, 0.0%) (0.0%, 0.0%) (100.0%, 0.4%) (0.0%, 0.0%) 0.1% Uni-manual Cling 171 93 122 16 402 (42.5%, 46.6%) (23.1%, 44.5%) (30.4%, 47.3%) (4.0%, 35.6%) 45.7% TOTALS 367 (41.7%) 209 (23.8%) 258 (29.4%) 45 (5.1%) 879 Bi-manual Cling 6 13 61 21 101 (5.9%, 75.0%) (12.9%, 76.5%) (60.4%, 40.4%) (20.8%, 31.3%) 41.6% Perch N/A N/A N/A N/A N/A Cobalt Quadrupedal Suspend 0 0 0 1 1 (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) (100%, 1.5%) 0.4% Uni-manual Cling 2 4 90 45 141 (1.4%, 25.0%) (2.9%, 23.5%) (63.8%, 59.6%) (31.9%, 67.2%) 58.0% TOTALS 8 (3.3%) 17 (7.0%) 151 (62.1%) 67 (27.6%) 243

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Table 4.11 Postural behavior and support use during feeding by Tsinjo and Cobalt between May and December of 2017 in Torotorofotsy, Madagascar. Italicized % represents the frequency of a postural behavior across the various supports. Underlined % represents the frequency of each postural behavior on a single support type. Bold % represents the frequency of locomotor behavior use or support use.

Feeding Trunk Bough Branch Twig Liana Bamboo TOTAL

Bi-manual 332 24 26 2 8 78 470 Cling (70.7%, 51.6%) (5.1%, 63.2%) (5.5%, 41.3%) (0.4%, 100.0%) (1.7%, 61.5%) (16.6%, 65.0%) 53.5% Perch 0 1 5 0 0 0 6 (0.0%, 0.0%) (16.7%, 2.6%) (83.3%, 7.9%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) 0.7% Tsinjo Quadrupedal 0 1 0 0 0 0 1 Suspend (0.0%, 0.0%) (100.0%, 2.6%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) 0.1% Uni-manual 311 12 32 0 5 42 402 Cling (77.4%, 48.4%) (3.0%, 31.6%) (8.0%, 50.8%) (0.0%, 0.0%) (1.2%, 38.5%) (10.4%, 35.0%) 45.7% TOTAL 643 (73.1%) 38 (4.3%) 63 (7.3%) 2 (0.2%) 13 (1.5%) 120 (13.6%) 879 Bi-manual 70 6 7 8 4 6 101 Cling (69.4%, 41.4%) (5.9%, 60.0%) (6.9%, 38.9%) (7.9%, 53.3%) (4.0%, 26.7%) (5.9%, 37.5%) 41.6% Perch N/A N/A N/A N/A N/A N/A N/A Cobalt Quadrupedal 0 0 1 0 0 0 1 Suspend (0.0%, 0.0%) (0.0%, 0.0%) (100.0%, 5.5%) (0.0%, 0.0%) (0.0%, 0.0%) (0.0%, 0.0%) 0.4% Uni-manual 99 4 10 7 11 10 141 Cling (70.2%, 58.6%) (2.8%, 40.0%) (7.1%, 55.6%) (5.0%, 46.7%) (7.8%, 73.3%) (7.1%, 62.5%) 58.0% TOTAL 169 (69.5%) 10 (4.1%) 18 (7.4%) 15 (6.2%) 15 (6.2%) 16 (6.6%) 243

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Travel Ground Understory Low canopy Main Canopy High Canopy Emergent Total Support Layer Use (and %) Trunk 0 106 114 197 29 0 446 (50.7%)

Bough 0 5 13 27 11 0 56 (6.4%)

Branch 0 9 26 106 59 0 200 (22.8%)

Twig 0 1 5 14 33 1 54 (6.1%)

Bamboo 0 5 8 12 4 0 29 (3.3%)

Liana 0 11 18 43 22 0 94 (10.7%)

Total Strata 0 (0.0%) 137 (15.6%) 184 (20.9%) 399 (45.4%) 158 (18.0%) 1 (0.1%) Use (and %)

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Foraging Ground Understory Low canopy Main Canopy High Canopy Emergent Total Support Layer Use (and %) Trunk 0 42 30 36 7 0 115 (55.8%)

Bough 0 1 2 4 7 0 14 (6.8%)

Branch 0 0 1 8 0 0 9 (4.4%)

Twig 0 0 0 1 0 0 1 (0.5%)

Bamboo 0 16 29 14 1 0 60 (29.1%)

Liana 0 1 1 5 0 0 7 (3.4%)

Total Strata 0 (0.0%) 60 (29.1%) 63 (30.6%) 68 (33.0%) 15 (7.3%) 0 (0.0%) Use (and %)

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Feeding Ground Understory Low canopy Main Canopy High Canopy Emergent Total Support Layer Use (and %) Trunk 0 324 158 148 13 0 643 (73.1%)

Bough 0 1 1 27 9 0 38 (4.3%)

Branch 0 0 7 36 20 0 63 (7.3%)

Twig 0 0 1 1 0 0 2 (0.2%)

Bamboo 0 39 42 36 3 0 120 (13.6%)

Liana 0 3 0 10 0 0 13 (1.5%)

Total Strata 0 (0.0%) 367 (41.7%) 209 (23.8%) 258 (29.4%) 45 (5.1%) 0 (0.0%) Use (and %)

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Travel Ground Understory Low canopy Main Canopy High Canopy Emergent Total Support Layer Use (and %) Trunk 0 29 53 190 67 0 339 (51.5%)

Bough 0 1 7 18 13 0 39 (6.0%)

Branch 0 0 5 62 67 1 135 (20.5%)

Twig 0 0 2 12 25 1 40 (6.0%)

Bamboo 0 0 5 5 1 0 11 (1.7%)

Liana 0 17 13 46 18 0 94 (14.3%)

Total Strata 0 (0.0%) 47 (7.2%) 85 (12.9%) 333 (50.6%) 191 (29.0%) 2 (0.3%) Use (and %)

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Foraging Ground Understory Low canopy Main Canopy High Canopy Emergent Total Support Layer Use (and %) Trunk 0 3 5 16 6 0 30 (60.0%)

Bough 0 1 1 1 4 0 7 (14.0%)

Branch 0 0 0 0 5 0 5 (10.0%)

Twig 0 0 0 1 1 0 2 (4.0%)

Bamboo 0 0 0 1 0 0 1 (2.0%)

Liana 0 0 1 4 0 0 5 (10.0%)

Total Strata 0 (0.0%) 4 (8.0%) 7 (14.0%) 23 (46.0%) 16 (32.0%) 0 (0.0%) Use (and %)

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Feeding Ground Understory Low canopy Main Canopy High Canopy Emergent Total Support Layer Use (and %) Trunk 0 5 12 106 46 0 169 (69.5%)

Bough 0 2 2 6 0 0 10 (4.1%)

Branch 0 0 0 6 12 0 18 (7.4%)

Twig 0 0 0 12 3 0 15 (6.2%)

Bamboo 0 1 2 5 8 0 16 (6.6%)

Liana 0 0 0 15 0 0 15 (6.2%)

Total Strata 0 (0.0%) 8 (3.3%) 17 (7.0%) 151 (62.1%) 67 (27.6%) 0 (0.0%) Use (and %)

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Table 4.18 Pairwise comparison results for distances traveled by Tsinjo while performing positional behaviors during locomotion between May 2017 and December 2017 in Torotorofotsy, Madagascar. Significant differences between positional behavioral frequencies are highlighted in bold.

BR CL HD LP QR QS QW SD TD VL BR X <0.001 <0.001 <0.001 <0.001 0.765 <0.001 0.063 <0.001 <0.001 CL X 1.000 <0.001 1.000 1.000 1.000 1.000 1.000 <0.001 HD X <0.001 1.000 1.000 1.000 1.000 1.000 <0.001 LP X 0.002 1.000 <0.001 1.000 0.590 1.000 QR X 1.000 1.000 1.000 1.000 <0.001 QS X 1.000 1.000 1.000 1.000 QW X 1.000 1.000 <0.001 SD X 1.000 1.000 TD X 0.746 VL X

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Table 4.19 Pairwise comparison results for travel distances covered by Tsinjo during bridging in various forest levels between May 2017 and December 2017 in Torotorofotsy, Madagascar. N/A indicates the statistical test could not be performed because of tied values. Significant differences between distances within forest levels are highlighted in bold.

Forest Levels p-value High Canopy vs. Main Canopy 1.000 High Canopy vs. Low Canopy N/A High Canopy vs. Understory 0.771 Main Canopy vs. Low Canopy 0.197 Main Canopy vs. Understory 1.000 Low Canopy vs. Understory 0.019

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Table 4.20 Pairwise comparison results for travel distances covered by Tsinjo during leaping in various forest levels between May 2017 and December 2017 in Torotorofotsy, Madagascar. Significant differences between forest levels are highlighted in bold.

Forest Levels p-value High Canopy vs. Main Canopy 0.280 High Canopy vs. Low Canopy 0.280 High Canopy vs. Understory 0.014 Main Canopy vs. Low Canopy 0.012 Main Canopy vs. Understory 0.001 Low Canopy vs. Understory 0.280

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Table 4.21 Pairwise comparison results for travel distances covered by Tsinjo during vertical clinging and leaping in various forest levels between May 2017 and December 2017 in Torotorofotsy, Madagascar. Significant differences between forest levels are highlighted in bold.

Forest Levels p-value High Canopy vs. Main Canopy 1.000 High Canopy vs. Low Canopy 1.000 High Canopy vs. Understory 0.020 Main Canopy vs. Low Canopy 1.000 Main Canopy vs. Understory 0.004 Low Canopy vs. Understory 0.015

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Table 4.22 Pairwise comparison results for travel distances covered by Tsinjo during climbing in various forest levels between May 2017 and December 2017 in Torotorofotsy, Madagascar. Significant differences between forest levels are highlighted in bold.

Forest Levels p-value High Canopy vs. Main Canopy 0.407 High Canopy vs. Low Canopy 0.407 High Canopy vs. Understory 0.088 Main Canopy vs. Low Canopy 0.559 Main Canopy vs. Understory 0.036 Low Canopy vs. Understory 0.407

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Table 4.23 Pairwise comparison results for travelling distances covered by Tsinjo during head- first descent in various forest levels between May 2017 and December 2017 in Torotorofotsy, Madagascar. Significant differences between forest levels are highlighted in bold.

Forest Levels p-value High Canopy vs. Main Canopy 1.000 High Canopy vs. Low Canopy 1.000 High Canopy vs. Understory 0.512 Main Canopy vs. Low Canopy 0.578 Main Canopy vs. Understory 0.018 Low Canopy vs. Understory 0.578

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Table 4.24 Pairwise comparison results for distances traveled with each positional locomotion behavior performed by Cobalt between May 2017 and December 2017 in Torotorofotsy, Madagascar. Significant differences between positional behavioral frequencies are highlighted in bold.

BR CL HD LP QR QS QW SD TD VL BR X 1.000 1.000 1.000 0.394 1.000 1.000 1.000 1.000 1.000 CL X 1.000 0.039 0.485 1.000 0.390 1.000 1.000 0.004 HD X 0.316 0.379 1.000 1.000 1.000 1.000 0.045 LP X <0.001 1.000 1.000 1.000 0.597 1.000 QR X 0.394 0.004 1.000 1.000 <0.001 QS X 1.000 1.000 1.000 1.000 QW X 1.000 1.000 1.000 SD X 1.000 1.000 TD X 0.343 VL X

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Figure 4.1 Forest levels recognized in this study.

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Figure 4.2 Perch: Tsinjo’s hind limbs hold a branch, while her hands hold a Canarium seed. Photo by author.

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Figure 4.3 Tap: Cobalt lightly strikes a branch with his 3rd digit. Photo by author.

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Figure 4.4 Gnaw: Tsinjo bites into a live tree. Photo by author.

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Figure 4.5 Probe: Tsinjo inserts her 3rd digit in a live tree to forage for invertebrates. Photo by author.

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Figure 4.6 Bi-manual cling: Tsinjo foraging on bamboo, clinging with both hands. Photo by author.

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Figure 4.7 Uni-manual cling: Tsinjo holds on with one hand while foraging at a live tree. Photo by author.

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Figure 4.8 Hindlimb suspension: Tsinjo hangs from bamboo with her hindlimbs. Photo by author.

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Figure 4.9 Quadrupedal suspension: Cobalt hangs from a support by all four limbs. Photo by author.

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300

250

200

150

Occurrences Tsinjo 100 Cobalt

Figure 4.10 Number of occurrences of positional behaviors during travel for Tsinjo and Cobalt between May and December 2017 in Torotorofotsy, Madagascar.

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40 Tsinjo Cobalt Occurrences 30

0 Climbing Head-first Quadrupedal Rump-first Sideways Descent Walk Descent Descent

Figure 4.11 Number of occurrences of positional behaviors during foraging for Tsinjo and Cobalt between May and December 2017 in Torotorofotsy, Madagascar.

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600

500

400

300 Tsinjo

Cobalt Occurrences 200

100

0 Bi-manual cling Perch Quadrupedal Uni-manual cling suspend

Figure 4.12 Number of occurrences of postural behaviors during feeding for Tsinjo and Cobalt between May and December 2017 in Torotorofotsy, Madagascar.

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273

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Chapter 5 Behavioral development of a sub-adult male aye-aye (Daubentonia madagascariensis) at Torotorofotsy, Madagascar

In this chapter, I present feeding, ranging, and locomotor behavioral data on the infant aye-aye, Cobalt, collected over a period of seventeen months. These data are compared to the behaviors of captive infants to assess if a wild aye-aye develops more slowly than his captive counterparts, as seen in other primates. Additionally, I discuss how resources and brain size may influence the duration of an aye-aye’s ontogeny.

Introduction

The social brain hypothesis states that large brains, especially an increase in the size of the neocortex, was selected for in primates to help maintain complex social connections (Dunbar 1998). The neocortex is responsible for sensory perception, spatial reasoning and conscious thought, among other things (Dunbar 1998). Though aye-ayes

(Daubentonia madagascariensis) have the most encephalized brain of any strepsirrhine or nocturnal primate (Stephan et al. 1981), their neocortex size is relatively small

(Kaufman et al. 2005). Instead, the largest portion of the aye-aye’s brain is the frontal cortex, which is involved in motor function, problem solving and memory (Kaufman et al. 2005). It has been suggested that the enlarged frontal cortex of aye-ayes is associated with the processing of large quantities of sensorimotor information (i.e., simultaneous sensory and motor function such as echolocation via tapping) during percussive foraging

(Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991; Erickson et al. 1998; Dominy et al. 2001; Kaufman et al. 2005). Percussive foraging is a behavior performed by aye- ayes when echolocating invertebrates in woody substrates. This behavior requires aye-

277 ayes to process olfactory, visual, auditory and tactile information to successfully remove a larva from its chamber (Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991;

Erickson et al. 1998; Dominy et al. 2001; Kaufman et al. 2005). Given that aye-ayes have a dispersed polygyny social system and social interactions are infrequent (Sterling and Richard 1995), it is more likely that the aye-aye’s enlarged brain is due to ecological factors associated with invertebrate foraging, i.e. echolocation of larvae in woody substrates (Clutton-Brock and Harvey 1980), rather than social factors (Dunbar 1998).

As discussed in Chapter 2, invertebrates are the aye-aye’s preferred resource.

Aye-ayes not only exploit this resource across a large home range (see Chapter 3) but use a wide variety of positional behaviors to access this resource in every level of the forest

(see Chapter 4). Additionally, aye-ayes constantly forage for invertebrates, likely as a way of maximizing energetic gain (described in Chapter 3). Because aye-ayes must efficiently forage on invertebrates to sustain their large body size (McNab 1963; Gaulin

1979), it is not unreasonable to assume that the protracted developmental period of young aye-ayes resulted in, among other things, superior foraging skills that provided a selective advantage in survival that offset their delayed reproductive maturation (Johnson and

Bock 2004; Schuppli et al. 2012). To understand the selective pressures that influence the duration of an aye-aye’s developmental period, we must consider a multitude of factors, including parental care strategies, predation, diet, and brain size (Kappeler 1998;

Ross 1998; Kappeler et al. 2003), and how each one relates to the behavioral development of aye-ayes (Pereira and Fairbanks 2002).

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Life History Theory

An organism’s life history typically refers to their pace of growth and development, rate of reproduction and maximum potential life span (Partridge and

Harvey 1988; Stearns 1992). Life history is an adaptation that provides a species with a selective advantage in their environment by adjusting energetic allocation to growth, reproduction, maintenance and repair to augment fitness (Stearns 1992; van Schaik and

Isler 2012). Indeed, the energy stores of an organism are finite, and any additional energy applied to one process will be reduced from another (van Schaik and Isler 2012).

For example, female rhesus macaques (Macaca mulatta) that mature one year early will experience a reduction of adult lifespan by 11 months (Blomquist 2009). Similarly, female orangutans (Pongo sp.) experience extended periods between ovulation cycles when rearing an offspring (van Noordwijk and van Schaik 2005). In general, mammalian life history follows one of two trajectories: fast or slow (Stearns 1992). Fast life histories

(r-selective) generally means that an animal will develop quickly and reach reproductive age early in life, have a short lifespan, produce multiple offspring in one litter, have few litters in a life span, and typically provide minimal parental care. Organisms that have slow life histories (K-selective) will develop slowly, taking a long time to reach reproductive age, have a long lifespan, produce only a few offspring per litter but have multiple reproductive opportunities, and provide extensive parental care. Though it has been shown that there is no correlation between body size and other life history traits

(Klingenberg and Spence 1997), typically larger animals take longer to grow than smaller organisms and therefore have longer lifespans and fewer offspring (Lindstedt and Clader

1981).

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Since life history characteristics are influenced by multiple external factors, including habitat, resource availability, predation, etc., there is some plasticity in these traits at the individual level (Mousseau and Roff 1987). That is, when an organism is supplied with the proper resources and has minimal predation pressure, it should grow and mature faster, produce more offspring, and live longer than an organism that experiences high ecological stress (van Schaik and Isler 2012). For example, captive orangutans have shorter inter-birth intervals, younger ages at first reproduction and similar life spans as their wild counterparts (Anderson et al. 2008; Wich et al. 2009).

Similarly, provisioned olive baboons (Papio hamadryas anubis) were found to grow almost twice as fast as wild olive baboons (Garcia et al. 2009). This isn’t to say that stressed organisms will not adapt to their environment, rather they will experience more pronounced life history trade-offs. For instance, though offspring of wild olive baboons experienced more stress and grew more slowly than provisioned or captive individuals, there was no difference in their mass at maturity (Garcia et al. 2009). Indeed, the olive baboons of this study possess significant plasticity which allow them to cope with ecological variability to ensure survival of offspring to reproductive age (Garcia et al.

2009). Thus, selection favors traits that can ensure stability in intergenerational population size, rather than those that maximize offspring quantity (Chisholm et al.

1993).

Primates are peculiar among eutherian mammals because they have extraordinarily slow individual growth rates that result in long lifespans with few offspring (Charnov and Berrigan 1993). That is, natural selection has favored the trade- off of low mortality for slow growth rates and low production rates in primates (Charnov

280 and Berrigan 1993: 193). As with other mammals, an individual primate’s developmental trajectory is based on the quality of maternal investment (Lee 1987;

Charnov and Berrigan 1993; Johnson 2003). Lactation production, i.e., milk that is high in fats, protein, calories, etc., from mothers is the main source of energetic derivation for a young primate (Lee 1987; Charnov and Berrigan 1993; Hinde and Milligan 2011).

Young primates that receive high quality maternal investment have a lower mortality rate, reach sexual maturity faster, produce more offspring over their lifetime and live a longer life than a young primate with lower quality care (Lee 1987; Charnov and

Berrigan 1993). For example, in Chacma baboons (Papio hamadryas ursinus) female offspring born of a higher-ranking mother grew and matured faster and produced more offspring in their lifetime than females born of a lower-ranking mother (Johnson 2003).

Of course, as already described, the mother also experiences trade-offs when caring for an infant, delaying ovulation and necessitating increased resource consumption to compensate for the energetic demands of pregnancy and lactation (Lee 1987; Hinde and

Milligan 2011). However, these demands and trade-offs are adaptable and can be altered by the behaviors of the mother, such as her parental care strategy.

Parental Care Strategies

Parental care strategies in primates can be broken down into two categories: absentee or permanent (Kappeler 1998; van Schaik et al. 1999; Ross 2001). Absentee care is when an adult parks their infant in a protective space, such as vegetation, a tree hole or a nest, during active hours of the day or night (Kappeler 1998; van Schaik et al.

1999; Ross 2001). Permanent care is when an infant is carried throughout the environment during active hours (Kappeler 1998; van Schaik et al. 1999; Ross 2001).

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Within these two categories there is further division into non-communal or communal infant care (Kappeler 1998; van Schaik et al. 1999; Ross 2001; Tecot et al. 2012; Baden et al. 2013; Tecot et al. 2013). Non-communal care means the infant’s mother is responsible for all aspects of rearing (van Schaik et al. 1999). Communal care is when members of the community will help rear on another’s offspring by assisting with carrying, protection and/or provisioning (van Schaik et al. 1999; Tecot et al. 2012; Baden et al. 2013).

Absentee Care

Infant parking is believed to be primitive in primates and is most common in strepsirrhines (Kappeler 1998; Ross 2001, 2003; Tecot et al. 2012). Strepsirrhines that use nests typically have altricial young, that is, infants that are born with closed eyes, are unable to grasp, and have difficulty thermoregulating (Blumberg and Sokoloff 1998;

Kappeler 1998; Tecot et al. 2012). These infants are relatively helpless and spend the first several weeks to months of their lives in a nest (Kappeler 1998). Nests retain heat, ultimately helping altricial young thermoregulate (Pereira et al. 1987). Because infants are aided in maintaining homeostasis, they are able to allocate additional energy for growth and development, thus accelerating their maturation (Kappeler 1998; Ross 2001).

When detected by predators, parked infants are easy prey and have high mortality rates because they are unprotected and vulnerable (Ross 2001; Tecot et al. 2012). To minimize predation events, a mother occasionally will carry her infant in her mouth to a new nest, where parking will commence again (Ross 2001). Heavy predation pressures affect primate life history by selecting for rapid growth and development in infants

(Janson and van Schaik 1993). By reaching adulthood more quickly, parked infants

282 minimize the duration of their most vulnerable period of life (Janson and van Schaik

1993). Therefore, because nested infants have high mortality rates (Ross 2001), the post- natal period of growth is rapid to ensure they reach reproductive maturity (Janson and van Schaik 1993; Tecot et al. 2012).

Parking an infant also has energetic benefits and costs for the mother that may influence infant development (Tecot et al. 2012). Generally, absentee mothers, including aye-ayes as demonstrated in Chapter 3, have smaller home ranges and feed for shorter durations than permanent care females because they are constantly returning to the nest to check on their parked young (Kappeler 1998; Ross 2001). However, compared to mothers that carry their infants, those that park offspring do not expend as much energy during foraging because they are not carrying their young (Tecot et al. 2012). Therefore, mothers can maximize their energy intake (Tecot et al. 2012). Simultaneously, mothers that park infants typically have shorter ranges and may have shorter feeding bouts because they are consistently returning to a nest to care for their young (Kappeler 1998;

Ross 2001). It has been suggested that mothers who park their infants can maximize energy consumption and provide higher energetic investment to offspring, i.e., higher quality milk production, than mothers that carry infants because they alleviate the constant stress of carrying and protecting young (Tilden and Oftedal 1997; Hinde and

Milligan 2011; Tecot et al. 2012).

Permanent Care

Permanent care, involving the carrying of an infant during all activities, is argued to be a derived behavior in primates, exhibited more commonly in haplorrhines (Kappeler

1998; van Schaik et al. 1999; Ross 2001, 2003). Carried infants are typically precocial,

283 meaning at birth they can grasp with hands and feet, open their eyes, and can thermoregulate (Kappeler 1998). Because these infants are less helpless than altricial young, they will ventrally or dorsally grasp onto the torso of their mother as she travels away from sleeping locations daily (Kappeler 1998). However, these infants must expend energy for clinging as well as maintaining homeostasis; therefore, the energy allocated to growth and development may be limited during a protracted maturation

(Ross 2001).

Infants with permanent care are in constant contact with an adult (Kappeler 1998).

This means there is consistent vigilance against predation on behalf of the infant.

Because carried infants have continuous protection, their mortality rates are low

(Charnov 1993; Janson and van Schaik 1993; Ross 2001). However, because they are in contact, and therefore competition, with conspecifics, especially adults, the risk of starvation increases (Janson and van Schaik 1993). In these circumstances, infants are predicted to have protracted growth and development (Janson and van Schaik 1993).

This delayed maturation takes advantage of the safety of the subadult phase, when predation pressures are reduced because of interactions with conspecifics, and diffusing the cost of maturation across a longer juvenile period, thereby increasing the likelihood of an infant successfully reaching adulthood (Janson and van Schaik 1993).

Since carried young are constantly with an adult, their mothers can range further in search of food and feed for longer durations than parking mothers (Kappeler 1998;

Ross 2001). Yet infant carrying can be energetically expensive to mothers in terms of transportation, locating resources, and avoiding predators (Schradin and Anzenberger

2001; Tecot et al. 2013). Though females that carry infants have higher energetic costs

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(Schradin and Anzenberger 2001; Tecot et al. 2013), slow maturation of carried infants disperses the energetic demands of parental investment across a longer period (Janson and van Schaik 1993).

Non-communal and Communal Rearing

In addition to being parked or carried, infants can be non-communally or communally reared. Non-communal rearing means that the mother provides the majority of, if not all, parental investment (Kappeler 1998; van Schaik et al. 1999; Ross 2001,

2003). Non-communal infant rearing is typically associated with a nocturnal lifestyle because it is easier for mothers to travel and remain cryptic during the night when an infant is parked in a nest (Ross 2001, 2003; Tecot et al. 2012). Nocturnal and solitary young are typically hidden, making them more difficult for predators to find

(Ebensperger and Blumstein 2006). However, despite being less conspicuous, non- communally parked offspring have a high likelihood of mortality when detected by predators because they will be the solely targeted individual for predation (Ross 2001).

As discussed previously, greater predation pressures likely result in selection for rapid growth and development (Janson and van Schaik 1993).

Communal rearing, or allocaretaking, is when other adults within the group help care for infants that are not their own through protection, transportation or provisioning

(Kappeler 1998; van Schaik et al. 1999; Ross 2001, 2003, Tecot et al. 2012; Baden et al.

2013). Communal infant rearing is common in diurnal species because resources are easier to locate and predators are more easily avoided during daylight hours (Ross 2001,

2003; Tecot et al. 2012). Furthermore, allocaretaking alleviates the strain of infant care for the mother, as other individuals share the stress (Mitani and Watts 1997). As already

285 discussed, when mothers experience less stress, there can be greater investment in offspring (Tecot et al. 2012). As a result, communally reared offspring have faster growth and development than non-communally reared counterparts, whether parked or carried (van Schaik et al. 1999; Ross 2003; Tecot et al. 2012).

Ecological Risk Aversion

Ecological factors, such as predation and diet, are also integral to the speed of development in subadult primates. The ecological risk aversion hypothesis (RAH) postulates that predation pressure and resource competition can select for either an accelerated or delayed maturation of young primates (Janson and van Schaik 1993). As described above, high infant mortality rates due to predation should result in a shortened subadult period (Janson and van Schaik 1993). Conversely, if infant mortality rates are low, young primates should delay maturation (Janson and van Schaik 1993).

In relation to diet, the subadult period following weaning and preceding first reproduction is particularly dangerous because individuals are relatively large-bodied but inexperienced (Janson and van Schaik 1993; Pereira 1993). Long juvenile periods are suggested to reduce the threat of extended periods of resource depression (Janson and van

Schaik 1993; Kappeler 1998; Ross 1998; Kappeler et al. 2003). For example, frugivores may be prone to starvation because they rely on a spatially and temporally patchy resource. Fluctuations in food abundance also increase intraspecific competition for resources. These factors result in frugivorous young experiencing high levels of stress during weaning (Janson and van Schaik 1993). Ultimately, young frugivorous primates should develop slowly to minimize the effects of a potentially volatile resource (Janson and van Schaik 1993). On the other hand, folivores have ubiquitously distributed

286 resources that are plentiful, both spatially and temporally (Janson and van Schaik 1993).

With short periods of low resource availability, intraspecific competition will be minimal

(Janson and van Schaik 1993). Therefore, offspring of folivorous species should experience rapid growth and start feeding independently at a young age because there is diminished stress associated with weaning (Janson and van Schaik 1993).

Haplorrhines in general conform to the predictions of the RAH (Leigh 1994).

Folivorous species of Colobinae, Alouatta, Hylobates, Gorilla and Pan all have rapid growth and short subadult periods (Leigh 1994). Comparatively, non-folivorous species of Papio, Macaca, and Cercopithecus all have a protracted ontogeny (Leigh 1994).

However, there are exceptions, such as Saimiri sciureus, which are frugivorous and insectivorous (Stone 2007). Though individuals of this species have slow infant growth, it is not due to anti-predation benefits or risk of starvation. Instead Stone (2007) suggests the protracted period of growth may be related to learning intricate social behaviors.

Studies on strepsirrhine development and behavior have shown that lemurs do not necessarily conform to the expectations of the RAH as it relates to diet (Wright 1999;

Godfrey et al. 2004; Tecot et al. 2012). For example, folivorous lemurs, such as Indri and Propithecus, while displaying faster dental development, will grow and mature more slowly than their frugivorous counterparts, Eulemur, Varecia, and Lemur (Godfrey et al.

2004). The unpredictable seasonality in Madagascar, which translates to irregular resource abundance, is partially responsible for unusual lemur life histories (Wright

1999). Lemurs may be undergoing selective pressures to maintain sustainable population sizes by maximizing adult female survival and reproductive opportunities (Godfrey et al.

2004: 271). For example, the frugivorous Varecia variegata variegata maximizes

287 energetic gains and minimizes energy expenditure by not carrying infants (Tecot et al.

2012). The result is the Varecia infants have higher maternal energetic investment than carried lemur young and reach adulthood more quickly (Tecot et al. 2012). Thus, the

Varecia population remains stable because of the accelerated infant development

(Godfrey et al. 2004; Tecot et al. 2012). On the other hand, the folivorous indri and sifakas carry their offspring (Pollock 1975; Klopfer and Boskoff 1979). These primates expend more energy daily and females with offspring have low net energy gain (Janson and van Schaik 1993; Godfrey et al. 2004). Ultimately, these infants have a protracted growth rate because the quality of maternal investment is lower than for parked infants

(Janson and van Schaik 1993; Godfrey et al. 2004). With protracted developmental periods, infants remain with adults and protected from predators resulting in high survival rates and stable populations (Godfrey et al. 2004).

Brain Size and Life History

There has also been significant attention to the relationship between encephalization and a prolonged ontogeny (Charnov and Berrigan 1993; Leigh 2004;

Isler and van Schaik 2006, 2009; Leigh and Blomquist 2007). In general, primates are characterized as having large brain to body size ratios compared to other mammals. One theory is that large brains require high energetic demands (Charnov and Berrigan 1993;

Isler and van Schaik 2006, 2009). This means that primates will experience a protracted developmental period as energy is diverted from maturation and instead focused on growing the large brain (Charnov and Berrigan 1993; Isler and van Schaik 2006, 2009).

An alternative theory suggests that brain development does not actually influence body development and does not directly affect life history (Leigh and Blomquist 2007;

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Barrickman and Lin 2010). Rather, it is suggested that the maturation rates of mothers provide a selective advantage for pre- or post-natal brain development of offspring (Leigh

2004; Leigh and Blomquist 2007). That is, females that delay maturation, and are typically large-bodied, will be able to provide significant investment in the prenatal brain growth of offspring because they can sustain the associated energetic demands (Leigh

2004; Leigh and Blomquist 2007). Conversely, early maturation in females is typically linked to post-natal brain development in infants (Leigh 2004; Leigh and Blomquist

2007). This is because the energetic demands of the offspring may be diffused via alloparenting or independent foraging by the offspring and are not necessarily the sole responsibility of the mother (Leigh 2004; Leigh and Blomquist 2007).

A third theory suggests that the prolonged developmental periods are necessary for learning complex behaviors, particularly those associated with extractive foraging, i.e., removal of a resource from a hidden or protective substrate (Parker and Gibson 1977,

1979; Gibson 1986; Reader et al. 2011; Parker 2015). When a primate relies on resources that may be hidden or cryptic, they must learn how to locate and remove food in an efficient manner (Parker and Gibson 1977, 1979; Gibson 1986). For instance, members of the family Hominoidea, especially Pan sp. and Pongo sp. which are known to be extractive foragers, have prolonged periods of development, and have large brain to body size ratios (Reader et al. 2011; Parker 2015). Therefore, extractive foraging is strongly correlated with enlarged brain sizes and prolonged ontogeny (Reader et al. 2011;

Parker 2015).

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Aye-aye Development

Evaluation of life history patterns is particularly salient for aye-ayes as they are the largest bodied nocturnal primate and have the greatest encephalization quotient of any strepsirrhine (Stephan et al. 1981). When examining parental care strategies, most primates that infant park are small bodied and produce multiple offspring (Kappeler

1998; Ross 2001, 2003). However, aye-ayes do not conform to these typical characteristics as they are large bodied and only produce a single young at a time

(Feistner and Ashbourne 1994; Winn 1994; Glander 1994; Kappeler 1998; Ross 2001,

2003). Infant parking is also associated with rapid post-natal development (Kappeler

1998; Ross 2001). Studies on aye-aye development, generated from captive populations, suggest they have a slower growth rate than other lemurs (Feistner and Ashbourne 1994;

Winn 1994). For instance, wild precocial young of Lemur catta are capable of proficient locomotion at one to two months of age and wild altricial young of Varecia variegata at two to three months (Klopfer and Boskoff 1979; Pereira et al. 1987). Captive aye-ayes, on the other hand, do not become proficient at traveling until approximately three months and do not display a full range of locomotion until nine months (Pereira et al. 1987;

Feistner and Ashbourne 1994; Winn 1994). Additionally, wild Lemur catta start weaning at 70 days and consume solid foods at 84 days (Klopfer and Boskoff 1979), whereas captive aye-aye infants start weaning around 90-118 days (Feistner and Ashbourne 1994;

Winn 1994).

According to the RAH, if a primate species’ main resource fluctuates dramatically, young primates should develop more slowly (Janson and van Schaik 1993).

Conversely, those primates that rely on a continuously available resource should have young that develop more quickly (Janson and van Schaik 1993). As discussed in Chapter 290

2, the preferred food of aye-ayes is invertebrates, a continuously available resource; therefore, according to the RAH, aye-ayes should develop more quickly. However, as already mentioned, lemurs do not appear to follow the predictions of the RAH, with frugivorous lemurs developing more quickly than their folivorous counterparts (Godfrey et al. 2004; Tecot et al. 2012). Instead, infant development rates may be related to population stability (Godfrey et al. 2004; Tecot et al. 2012). Because aye-ayes only produce one offspring per birth, maintaining a stable population would likely necessitate slower development to ensure survival of offspring. That is, delayed maturation may help the infant to learn how to navigate periods of low resource availability, thus minimizing the adverse effects of intraspecific competition it will experience as an independent adult (Godfrey et al. 2004). This of course is contrary to the predictions for absentee parental care, already discussed, but aligns with the rate of development for captive aye-ayes (Feistner and Ashbourne 1994; Winn 1994).

The association between life history and brain size is particularly relevant to aye- ayes because they are the largest nocturnal primate and have the greatest encephalization quotient of any strepsirrhine (Stephan et al. 1981). The aye-aye’s enlarged brain is adapted for high levels of sensorimotor cognition, necessitated by their percussive foraging behavior (Kaufman et al. 2005). As described in Chapter 2, percussive foraging is where aye-ayes use their adaptations to echolocate and extract larvae contained within a woody substrate (Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991; Sterling

1993, 1994; Erickson et al. 1998; Dominy et al. 2001). Primates that employ extractive foraging techniques, such as Pan or Pongo do when foraging for termites and ants, are thought to have evolved large brains as a selective advantage for harvesting a cryptic

291 resource (Reader et al. 2011; Parker 2015). Of course, large brain sizes require a longer developmental period because of the energetic demand associated with developing and maintaining this energetically expensive organ (Dunbar 1998). Alternatively, the delayed development of a species may be selectively advantageous to ensure pregnant females can sustain the energetic demands of rapid pre-natal brain development (Leigh 2004;

Leigh and Blomquist 2007). Since extractive foraging behaviors select for enlarged brain size and slow developmental rates in young primates (Reader et al. 2011; Parker 2015), this could be an explanation for the delayed maturation of young aye-ayes, as described in captivity (Feistner and Ashbourne 1994; Winn 1994).

It is likely that a multitude of factors may be influencing the life history pattern of aye-ayes; however, our ability to understand aye-aye development is hindered by the dearth of behavioral research on young aye-ayes. To date, there have been three studies on the development of captive aye-aye infants, all of which suggest that aye-ayes have a longer period of infant dependency than other lemurs (Feistner and Ashbourne 1994;

Glander 1994; Winn 1994). However, infant developmental periods in captivity may not be characteristic of rates of ontogeny in naturally occurring populations as captive primates tend to develop more quickly than wild ones (Anderson and Simpson 1979;

Fairbanks and McGuire 1984; Lee 1987; Altmann and Muruthi 1988). Information about infant behavior in free-ranging aye-ayes is limited and questionable. For instance, Petter

(1965) described an aye-aye infant clinging to its mother’s fur during travel; however, captive aye-aye infants were described as altricial, carried in their mother’s mouth as they were unable to cling, and parked in a nest (Feistner and Ashbourne 1994 Kappeler 1998;

Ross 2001, 2003).

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Several studies have shown that captive primates tend to develop more quickly than their wild counterparts because provisioning and lack of predation create optimal conditions for accelerated development (Anderson and Simpson 1979; Fairbanks and

McGuire 1984; Lee 1987; Altmann and Muruthi 1988). For example, captive infant owl monkeys (Aotus sp.) were completely weaned by four to five months while their wild counterparts were still attempting to nurse at eight months old (Rotundo et al. 2005).

Similarly, captive baboons (Papio sp.) grew at twice the rate of wild baboons (Altmann and Alberts 1987). Lemurs also develop more slowly in the wild than in captivity. Wild blue-eyed black lemur infants (Eulemur flavifrons) began eating solid foods around ten weeks, while captive infants feed on solid foods around six weeks (Volampeno et al.

2011). Captive black and white ruffed lemur infants (Varecia variegata) were noted to leave nest boxes around three weeks, first experimented with solid foods between five and seven weeks and were weaned at around six months (Brockman et al. 1987).

Conversely, wild black and white ruffed lemurs started traveling independently between two and three months of age, experimented with solid foods around two months old and were still occasionally nursing between 7-8 months old (Morland 1990).

Since primates develop more quickly in captivity than in the wild, the actual developmental time for wild aye-ayes may be even longer than that of captive aye-ayes.

For example, aye-aye infants in captivity first emerge from a nest around 56-60 days

(Feistner and Ashbourne 1994; Winn 1994). These nests are located on the ground and infants can crawl out of the nest, though they have minimal locomotor coordination

(Feistner and Ashbourne 1994; Winn 1994). In the wild, aye-aye nests are on average

17m high (Sterling 1993), meaning when infants leave, they need to have sufficient

293 motor control to securely move along branches. Captive infants are not capable of locomotion along branches until 64-81 days of age, well after they initially leave their nest (Feistner and Ashbourne 1994; Winn 1994). This could translate to wild aye-ayes emerging from their nests even later than reported in captivity. Therefore, the duration of delayed maturation may be much longer than what other lemurs display. Without accurate information on the behavioral development of wild aye-aye offspring, it is impossible to gauge what selective pressures influence the life history strategy of this species.

This Study

I examined the behaviors of a naturally-occurring subadult male aye-aye during a seventeen-month period. The data I collected provide the first developmental profile of a free-ranging infant in a natural habitat. To date, no study has been conducted on the behavioral development of a naturally occurring aye-aye in a undisturbed forest.

Therefore, my goal was to estimate the timing of developmental changes during the ontogenetic period of a young aye-aye, including: a) first emergence from his nest, b) commencement of weaning, c) independent feeding becoming the primary form of subsistence, and d) the commencement of adult ranging behaviors. I do this by comparing (1) the frequency of behaviors in the wild infant to results of captive infant studies (Feistner and Ashbourne 1994; Winn 1994) and (2) the monthly ranging behaviors of the young aye-aye to his mother. My null hypothesis is that there will be no difference in the age of emergence from nest, weaning, and feeding on solid foods when comparing the free-ranging infant to the captive infants or between the infant’s and mother’s monthly home range. Given that wild young develop more slowly than their

294 captive counterparts (Anderson and Simpson 1979; Fairbanks and McGuire 1984; Lee

1987; Altmann and Muruthi 1988) and that parked infants remain in a nest so that mothers can forage unencumbered (Kappeler 1998; Ross 2001; Tecot et al. 2012), my alternative hypothesis is that the major behavioral changes in the wild infant aye-aye will occur at later ages than witnessed in captive individuals and there will be a difference between the monthly ranging behavior of the mother and her infant. I predicted:

1) The wild aye-aye will first emerge from his nest at an older age than the captive infants.

2) The wild aye-aye will start weaning at a later age than the captive infants.

3) The wild aye-aye will use solid foods as its primary form of subsistence at an older age than the captive infants.

4) The young aye-aye will never exceed the home range of his mother while still co- nesting.

Methods

Field Site

I conducted this research from August 2016-December 2017 in Torotorofotsy

(18o52’S, 42o22’E), Madagascar. Torotorofotsy is a natural wetland about 1100 ha in size, adjacent to Mantadia National Park and approximately 10km northwest of Andasibe

(Dolch et al. 2004; Peck 2004). It is the most continuous wetland in the Andasibe-

Mantadia-Zahamena eastern rainforest corridor, containing high levels of biodiversity

(Dolch et al. 2004; Peck 2004; Wright et al. 2008). Within Torotorofotsy there are three collared aye-ayes, one adult male, one adult female and one subadult male. These aye- ayes are outfitted with radio-collars as part of Madagascar Biodiversity Partnership’s aye-

295 aye research project (Sefczek et al. 2017). This research focused on the behaviors of the subadult male, Cobalt.

Behavioral Data Collection

In order to collect sustained dietary, foraging and positional data, I conducted six- hour follows, from 18:00-0:00 on Mondays and Wednesdays and from 0:00-6:00 on

Tuesdays and Thursdays. Monday and Wednesday follows started when Cobalt exited his sleeping nest. During Tuesday and Thursday follows, I located the focal animal using the radio telemetry system. Follows ended when Cobalt reached his nest and did not move for an hour. I used the methodology outlined by Sterling (1993) with three researchers following a focal animal: myself and two Malagasy field assistants. One researcher maintained light contact, defined as keeping the aye-aye within the beam from a head lamp but not closer than five meters. The other two participants positioned themselves to follow the animal when it ventured in a new direction (Sterling 1993).

During night follows, I collected data using the time-point sampling (Altmann

1974). That is, every five minutes I recorded all state events including resting, traveling, feeding, foraging, auto-grooming, allo-grooming, suckling, play locomotion, and playing with mother. Whenever these behaviors were observed, I recorded the height, estimated in meters, at which the behavior occurred, the vernacular name of the tree species in which the behavior occurred, and the diameter at breast height of said tree. Whenever

Tsinjo, Cobalt’s mother, was within visual contact, I recorded the distance between the two aye-ayes.

I also recorded elements of feeding behavior from the time a feeding bout commenced until a) feeding stopped, b) visibility became obstructed, or c) Cobalt

296 locomoted out of sight. I adopted the feeding categories of Sterling (1993, 1994a) to describe the dietary inventory: fruit, flower, leaves, seeds, invertebrates, fungus.

Whenever feeding was observed, I recorded the following: 1) resource category consumed, 2) quantity of each resource consumed (see below), 3) duration of feeding bout, defined as the time between the commencement of feeding and when Cobalt stopped or visibility became compromised, 4) height, estimated in meters, at which feeding occurred, and, when applicable, 5) the substrate used for invertebrate feeding

(bamboo, deadwood, or species of live tree).

Feeding quantity was assessed the following ways:

1) Invertebrate quantity was based on number of new traces created in a substrate

with each new trace equaling one invertebrate. A trace is the hole made by an

aye-aye in a woody substrate for the purpose of accessing an invertebrate.

Whenever I witnessed Cobalt create a new trace, I recorded one larvae consumed.

It is impossible to determine how many larvae were extracted from a single trace,

so I opted for a conservative approach and tallied one larvae per trace. Therefore,

a 1:1 ratio of new traces made and larvae removed was assumed as a way to

estimate larval consumption.

2) Fruits consumed were assessed by counting the number being orally processed or

from auditory cues which typically consisted of a seed being dropped. When

processing Canarium fruits, the aye-aye will grab one fruit, carry it to a perch spot

on a branch, hold it in both hands and gnaw through the fruit and into the seed

contained within. They will then remove a small portion of the exocarp and

extract the endosperm from inside the seed (Iwano and Iwakawa 1988; Sterling

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1993, 1994a). Once the endosperm is removed, the aye-aye will drop the food

and go back for another fruit.

Finally, I recorded the GPS location of Cobalt every 15 minutes using handheld Garmin

GPS Map60CS and Map62S units. I used the GPS points to estimate nightly path lengths.

Data Analysis

All statistical tests for this research were performed in R. A Shapiro-Wilk test of normality (α=0.05) showed that data for (1) feeding duration (W=0.67551, df=242, p<0.001), (2) quantities of resources consumed (W=0.653, df=169, p<0.001), and (3) substrates from which invertebrates were consumed (W=0.524, df=254, p<0.001) were not normally distributed. To compare the overall consumption of resources and duration of feeding bouts at each resource, I used a negative binomial regression analysis

(α=0.05). I employed a Mann Whitney U test (α=0.05) to compare mean length of feeding bout times on Canarium seeds in ripe fruit and invertebrates. To compare the total consumption of larvae from the three different substrates, I also used a negative binomial regression analysis (α=0.05). Lastly, I input GPS points into ArcGIS to determine night path lengths for follows lasting longer than 60 minutes.

Results

I followed Cobalt for a total of 102 nights, averaging 2.5 hours per follow (range:

40min-5hours 40min,=69min). Early months of observation were shorter because

Cobalt remained in the nest for extended periods of time. As Cobalt increasingly traveled away from the nest, durations of observations changed. The longest follows typically commenced at 18:00 because observation started while the individual was still in his nest.

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On the nights when Cobalt had already left the nest, sampling was shorter because considerable time was spent searching for him. The aye-aye typically finishes activity between 3:00 and 4:00, when he entered a sleeping nest with his mother. Additionally, aye-ayes tend to forage and travel in a cryptic manner, often high in the canopy or in other areas with poor visibility. This contributed to shorter average night follows.

Lastly, in September 2017, the batteries in Cobalt’s radio collar died, hindering our ability to follow him until a new radio collar was fitted.

Estimated Time of Birth

Tsinjo was documented as pregnant on February 4, 2016, and Cobalt was initially collared on July 29, 2016. By this time, Cobalt weighed 800g. Based on birth weights in captivity (Glander 1994) and birth weights of wild aye-ayes in Kianjavato (unpublished data, Edward Louis pers. comm.), Cobalt was estimated to be born in mid-February 2016.

During the first five and a half months of life, Cobalt was not observed outside of his nest. It is possible he left the nest after Tsinjo had started traveling and I was occupied with observations of the female. Based on reports from captivity (Feistner and

Ashbourne 1994; Winn 1994), aye-aye infants do not leave the nest for the first two months. Therefore, it is also likely that Cobalt wasn’t observed because he did not leave the nest.

Resting Behaviors

Table 5.1 presents and Figure 5.1 displays the frequency of Cobalt’s behaviors between August 2016 to December 2017. Cobalt’s first recorded activity outside of the nest was August 1, 2016, at approximately five and a half months old. During this time

Cobalt rested 8-12m high in various trees, either by himself or with Tsinjo. From August

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2016 through December 2016, when Cobalt was between five and nine months old, resting was his most frequent behavior, with the exception of September 2016 when traveling exceeded resting (Table 5.1). After December 2016, from January 2017-

December 2017, traveling and feeding behaviors increased in frequency and resting was never more frequent than 33% of the time (Table 5.1).

Locomotor Behaviors

Between August and October 2016, Cobalt was developing his locomotor capabilities. During this time, Tsinjo would often return to check on Cobalt, coming within five meters of him (Table 5.2). When Tsinjo would travel beyond five meters,

Cobalt would remain parked near the nest, traveling short distances between trees or play locomoting in the canopy. By November 2016 Cobalt spent approximately one-third of his time traveling, with two exception, December 2016 and February 2017 (Table 5.1).

In December 2016, Cobalt was resting more frequently than any other behavior, while in

February 2017 his most frequent behavior was feeding. Resting frequency in December

2016 may be due to sampling deficiency, as only three nights of data were collected. It is possible Cobalt traveled more frequently during this time but not when I was collecting data. The decrease in travel in February is likely because of an increase in Canarium seed feeding during this month (Table 5.3). Since Canarium trees produce thousands of fruits, it is possible for the aye-aye to remain in one tree for extended periods of time as they consume seeds in ripe fruit.

Distance to Tsinjo

Table 5.2 presents the number of times Tsinjo and Cobalt were in association (i.e. within five meters) outside of the nest over the course of the study. Tsinjo and Cobalt

300 nested together through December 2017. Between August and October 2016, when

Cobalt started performing activities outside of the nest, associations between Tsinjo and

Cobalt increased (Table 5.2). Many of these close associations were during feeding events performed by either Cobalt or Tsinjo. After October 2016, associations between the Tsinjo and Cobalt outside the nest became infrequent until February 2017. During the early days of February 2017 Tsinjo and Cobalt were again in close association as twice they fed on ripe fruit in the same Canarium tree (Table 5.2). In May 2017 Tsinjo and Cobalt were in close proximity at the beginning of the night but quickly dispersed in opposite directions (Table 5.2). During both February and May 2017 Tsinjo nursed

Cobalt outside of the nest (Table 5.1). By June 2017, when the aye-ayes would exit the nest, they would disperse in opposite directions. Except for nesting together, interactions were rare. There were two notable interactions between Cobalt and Tsinjo outside of the nest. Tsinjo would occasionally be within five meters of Cobalt immediately after they exited the nest, but were soon out of visual contact with each other. In July 2017, Cobalt and Tsinjo allo-groomed each other upon exiting the nest, the only time this event was witnessed. Additionally, in September 2017, Cobalt mounted Tsinjo twice in the same night.

Feeding Behaviors

Table 5.3 presents and Figure 5.2 displays the number of invertebrates in various substrates (live tree, deadwood, and bamboo) and Canarium seeds in ripe fruit consumed by Cobalt between September 2016 and December 2017. Apart from suckling, all of

Cobalt’s feeding was done independently of his mother. The earliest feeding behaviors occurred in September 2016, when Cobalt was approximately seven months old, and

301 were associated with invertebrates contained in live trees and deadwood (Table 5.3 and

Figure 5.2). Independent foraging and feeding became a frequent behavior in December

2016, when Cobalt was ten months old. Between December 2016 and December 2017, feeding comprised anywhere between 26.3% and 58.8% of behaviors (Table 5.1). Data from September 2017 are lacking due to the batteries in Cobalt’s collar dying. I never witnessed Cobalt stealing food from Tsinjo, a behavior reported in captive infants

(Feistner and Ashbourne 1994; Winn 1994).

Infrequent Behaviors

Play behavior, whether with Tsinjo or solitary play movement through tree, was most frequent in October 2016. Play was not witnessed with any regularity before or after that month (Table 5.1). Suckling was only witnessed outside of the nest in two months, February and May 2017. Based on reports from capacity (Feistner and

Ashbourne 1994; Winn 1994), it is likely that most of Cobalt’s suckling occurred within the nest when both aye-ayes were out of sight (Table 5.1). There were five rare events that occurred during the entire study. In February 2017, Cobalt was chased by a fosa

(Cryptoprocta ferox; described in Sefczek et al. 2018). In September 2017, Cobalt mounted Tsinjo twice in one night. Finally, in November 2017, Cobalt made two contact calls in one night. Auto-grooming and allo-grooming were both infrequent behaviors outside of the nest. It is possible these behaviors occur more frequently within the nest when aye-ayes are out of sight.

Overall Resource Use

Over the course of the study, there was no significant difference in the quantity of invertebrates and Canarium seeds in ripe fruit that Cobalt consumed (negative

302 binomial regression: z=-0.806, df=169, p=0.420). However, the average time of Cobalt’s feeding bouts at Canarium trees were significantly longer than those at invertebrates

(Mann Whitney U test: W=192.5, df=1, p<0.001). On average, Cobalt consumed more seeds per minute (1.0/min) than he consumed larvae per minute in any of live tree

(0.5/min), deadwood (0.4/min) or bamboo (0.6/min) during feeding bouts (Table 5.3).

When consuming invertebrates, Cobalt consumed significantly more invertebrates in live trees than in deadwood (negative binomial regression: z=4.28, df=169, p<0.001) or bamboo (z=7.191, df=254, p<0.001); he also ate significantly more deadwood invertebrates than bamboo invertebrates (z=3.594, df=254, p<0.001).

Nightly Ranging Distances

Table 5.4 presents the average distances traveled each month, based on half-night follows. Using the GPS points, I calculated that Cobalt averaged 322.7m traveled per half-night (N=97), while Tsinjo averaged 514.5m (N=142). Cobalt’s 18:00-0:00 follows averaged 326.2m (N=57), while his 0:00-6:00 follows averaged 317.8m (N=40). The average distance for Tsinjo during follows from 18:00-0:00 was 592.1m (N=86), while follows between 0:00-6:00 were 393.2m (N=55). Tsinjo almost always ranged further than Cobalt during the study, though there was a noticeable increase in Cobalt’s range starting in August 2017. Between August 2016 and July 2017, Cobalt’s monthly average distances traveled were considerably lower than Tsinjo’s, except for April 2017. The difference in April 2017 ranging distances is likely due to sampling variance, with Cobalt followed twice as much as Tsinjo in this month (Table 5.4). Starting in August 2017,

Cobalt was averaging nearly the same distances as Tsinjo. Ranging data for Cobalt in

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September 2017 are skewed because the batteries in his radio collar died and follows were not possible a portion of this month (Table 5.4).

Discussion

Previous research on captive aye-aye developmental patterns suggests that aye- ayes have a longer developmental period than other strepsirrhines (Feistner and

Ashbourne 1994; Winn 1994; Glander 1994). Based on the behavioral pattern of the male subadult aye-aye from this study, my findings substantiate these results.

Furthermore, this wild offspring appears to take longer than its captive counterparts to develop a full behavioral repertoire and become independent. It is likely this prolonged ontogenetic period in wild aye-ayes compared to captive individuals is due to ecological factors, primarily predation pressures and resource acquisition.

Emergence from Nest

My first goal was to determine the timing of emergence from the nest. I predicted that Cobalt would take longer to emerge from his nest than captive infants took to come out of theirs. The data supported my prediction: Cobalt did remain in the nest longer than was reported in captive aye-ayes. Captive infants first emerged from the nest at 56-

60 days (roughly 2 months), moving along the ground (Feistner and Ashbourne 1994;

Winn 1994), whereas Cobalt emerged from the nest around five and a half months of age.

I saw Cobalt come to the ground twice during the study (see Chapter 4) and both events occurred after he was one year old. It is likely that locomotion along the ground is less frequent for the wild aye-aye because of the greater predation pressures associated with increased terrestrial behaviors (DeVore 1963).

This increased time in the nest could be associated with a decrease in parental care by the mother. Feistner and Ashbourne (1994) noted that the aye-aye mother in their 304 study spent a large portion of her time in the nest box with the infant and did not increase activity until the infant became more mobile. Unlike captive aye-ayes, Tsinjo was not provisioned. She searched for resources and parked the infant in a nest every night

(Table 5.4). It is probable the captive mother’s reduced foraging time translates to increased parental care from the mother to the infant in the nest. While it is unknown what behaviors transpired in the nest, it may be that the greater sociality between mother and infant, i.e., grooming, nursing, playing, etc., has a role in the more rapid develop of the captive aye-aye compared to wild ones (Anderson and Simpson 1979; Fairbanks and

McGuire 1984; Lee 1987; Altmann and Muruthi 1988). For instance, if nests help infants thermoregulate by retaining heat (Pereira et al. 1987), the presence of another individual in the nest should also help the infant maintain homeostasis. However, there are no data either here or in captive studies examining parental care within a nest to substantiate this claim (Feistner and Ashbourne 1994; Winn 1994). Future studies should examine the parent/offspring interactions that occur within the nest to help elucidate the amount of parental care that absentee parents provide both in captivity and in the wild.

Alternatively, free-ranging aye-ayes may necessitate longer development to ensure locomotor competence upon first exiting the nest. As already mentioned, two- month old captive aye-ayes emerge from nests located on the floor and walk along the ground. There were no aye-aye nests located on the forest floor in Torotorofotsy; instead, nests in Torotorofotsy were located anywhere between 8-20m off the ground. Therefore,

Cobalt had to be coordinated enough to move through the canopy without falling. In captivity, stable locomotion, including short leaps and climbing, was not witnessed until

63-90 days after birth, and the subjects practiced quadrupedal locomotion on the ground

305 for at least a week (Feistner and Ashbourne 1994; Winn 1994). Thus, Cobalt’s emergence from the nest may have been delayed because he needed to be more stable in the canopy before locomotion was possible. In fact, as soon as Cobalt was seen outside the nest at approximately 150 days, he appeared to move through the canopy without difficulty. During our focal follows of Tsinjo (see Chapter 2), Cobalt may have been outside performing unstable locomotion. It is equally likely that behaviors were practiced and fine-tuned within the tangled lianas that typically formed a nest. Future research should the explore the activities of a parked offspring prior to their first solo- excursion outside of the nest.

The long duration before the first emergence from a nest may be due to sampling error. Captive mothers are known to carry infants in their mouth to new nests (Feistner and Ashbourne 1994; Winn 1994). Tsinjo frequently used different nests during the study but I never witnessed her carrying the infant into a different nest or noticed the infant out of the nest earlier than August 1, 2016. It is possible the infant emerged from the nest while I was following Tsinjo or that Tsinjo relocated her infant during non- follow nights. Additionally, May and June 2016 were particularly poor months for observation due to inclement weather. Infant relocation may have been frequent during these months as well. Interestingly, I did not observe the infant during July 2016, when observations were more consistent. If the infant was able to move rapidly and make small leaps at 90 days (Winn 1994), I would expect to have witnessed the infant outside of the nest during the month of July 2016. Therefore, it seems likely that Cobalt exited the arboreal nest at a later age than captive aye-ayes because he needed to be physically

306 and mentally mature enough to balance on branches and deal with the demand of stable locomotion immediately upon exiting the arboreal nest.

In addition to emerging from the nest later, Cobalt also played in isolation and with his mother at an older age when compared to captive aye-aye infants. Solitary play behavior includes leaping from branch to branch and quick quadrupedal locomotion over the same series of supports repeatedly (Feistner and Ashbourne 1994; Winn 1994). In captivity, play jumping was initially demonstrated at approximately three months, approximately one month after leaving the nest, and then advanced to jumping at the mother shortly afterwards (Feistner and Ashbourne 1994). Again, I did not observe

Cobalt until he was approximately five and a half months old. I did not witness any play behavior from Cobalt in August or September of 2016, approximately six and seven months old, respectively. However, there was ample playing in October 2016, when

Cobalt was approximately eight months old. Though Cobalt follows a similar trajectory, emergence from nest, solitary play and finally playing with the mother, he displays these behaviors at an older age than the captive aye-aye young. As with emergence from nest, it seems likely the wild aye-aye’s behavioral development occurs later because an arboreal lifestyle necessitates an extended time activities involving locomotion, including play, can be performed with confidence.

Weaning

My second goal was to determine at what age weaning begins for the wild aye- aye infant. Unfortunately, commencement of weaning was indeterminate due to lack of observations for suckling behavior. As with captive studies, it is likely that most suckling occurred inside the nest where aye-ayes were not visible (Feistner and Ashbourne 1994;

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Winn 1994). Suckling by Cobalt was observed three times outside of the nest, twice in

February 2017, when he was 12 months old, and once in May 2017 when he was 15 months old (Table 5.1). It is worth noting that Tsinjo and Cobalt would quadrumanually suspend themselves from a branch when suckling (see Figure 4.8), a previously unreported position for nursing behavior. Since aye-ayes in captivity were completely weaned by 170 days (Winn 1994) and attempts from a yearling were typically rebuffed

(Feistner and Ashbourne 1994), this supports the prediction that wild infants are weaned at a later age then their captive counterparts. Cobalt would occasionally suckle even a full year after birth and much later than the captive aye-ayes that were weaned before six months of age (Table 5.1; Feistner and Ashbourne 1994). This extended period of infant dependence includes the duration of shared nesting. Captive aye-aye infants were removed from their mother between 14 months (male infant; Winn 1994) and 20 months

(female infant; Feistner and Ashbourne 1994) due to increased conflict between the two.

By the end of this study, at approximately 22 months old, Cobalt was still nesting with

Tsinjo. Future studies should follow aye-aye offspring through the entirety of their dependency period to determine at what age young leave the nest.

The extended period during which suckling was allowed by Tsinjo is particularly interesting. Given that provisioned captive females should not have to expend as much energy in foraging for resources, it might be expected that they would permit suckling for a longer time, but this was not the case. Instead, because captive primates are provisioned, they can provide optimal nutrition for infant development, with sustainable and high-quality milk production, thereby improving chances of early weaning (Kennedy

2005; Hinde and Milligan 2011). In contrast, wild primate mothers, such as Tsinjo, are

308 much more active with travel and foraging. Without a consistent source of food, lactation can decrease or become suspended altogether, resulting in suboptimum nutrition for infants and extending the duration of suckling (Kennedy 2005; Hinde and Milligan

2011). Additionally, where captive infants are still provisioned after weaning, wild infants must forage independently and may not acquire sufficient resources to properly sustain their growth. Therefore, wild young are permitted by their mother to suckle at older ages to ensure adequate nutritional intake (Rotundo et al. 2005; Volampeno et al.

2011). Future research should explore how a young aye-aye’s dietary composition, particularly solid vs. liquid ingestion, changes with age.

Alternatively, the shortened suckling period of the captive aye-aye young may have been due to the mother becoming pregnant and giving birth to a second offspring

(Feistner and Ashbourne 1994). In one of the captive studies (Feistner and Ashbourne

1994), the mother became pregnant with another offspring while her initial dependent was approximately one year old. This indicates that captive aye-ayes follow the pattern common in other captive primates wherein optimal conditions, e.g., consistently available food and a lack of predation, causes faster maturation of offspring and a shortened inter- birth interval for the mother (Anderson and Simpson 1979; Fairbanks and McGuire 1984;

Lee 1987). The interactions between the captive aye-aye mother and her first offspring became increasingly aggressive, and the two individuals were separated (Feistner and

Ashbourne 1994). In contrast, Tsinjo and Cobalt were never witnessed to have agonistic behaviors toward each other. As estrous is known to cause conflict between mother and offspring (Kleiman 1979), it is likely that Tsinjo never came into estrous during this study. It is possible that the shorted weaning in captivity is due to captive management

309 teams permitting insemination from a male too early. However, this seems unlikely as most non-human primates are not fertile until offspring are independent (Lee 1987).

Instead, it is probable that the same resource reliability that resulted in shortened suckling and quickened maturation of the captive offspring, also lead to the captive female ovulating sooner. Energetic balance is closely linked to reproduction; therefore, reproductive success should be optimized when conditions are ideal for positive energetic gain, such as those encountered in captivity (Schneider 2004). This would explain why the captive female, no longer energetically hindered by lactation, was able to ovulate despite already caring for a young aye-aye. Future research should determine if wild aye- aye females ovulate while still caring for an offspring over a year old.

Two rare behaviors deserve additional discussion. First, Cobalt was witnessed mounting Tsinjo twice in September 2017, when he was approximately 19 months old.

This behavior was witnessed in captivity as well, when a 17-month old male aye-aye was observed trying to mount his mother and another adult female (Winn 1994). While neither of these occurrences appear to have been successful copulation events, these events suggest a similar timing of sexual development in wild and captive male aye-ayes.

In the case of Cobalt, this did not lead to aggressive behavior from the mother and he continued to nest with her through December 2017. The captive aye-aye was removed from the enclosure with his mother shortly after the mounting event (Winn 1994).

Cobalt’s vocalizations in November 2017 were also rare behaviors. One of the captive infants was recorded using vocalizations within the first week of birth and continuing to use them throughout the study, though with decreasing frequency (Winn

1994). It is possible that Cobalt used vocalizations earlier than initially recorded,

310 particularly while in the nest prior to August 2016. Alternatively, vocalizations may be limited in the wild due to predation pressure. For instance, during and immediately following pursuit by a fosa, Cobalt made no vocalizations (Sefczek et al. 2018). Tsinjo vocalized more than Cobalt, including making contact calls after Cobalt was born.

However, Tsinjo only vocalized on nine of the 153 nights observed, making it a rare event. There is also the potential that aye-ayes, similar to tarsiers, produce vocalizations outside of the range of human hearing (Ramsier et al. 2012). It should be noted that

Cobalt did not respond whenever Tsinjo vocalized, and neither mother nor infant appeared to vocalize frequently during follows. Yet both ended follows at the same, new nest site, despite foraging independently, sometimes over 100m apart. Future research should explore how mother/infant pairs are able to communicate across long distances.

Independent Feeding

My third goal was to determine at what age Cobalt started feeding independently as his primary form of subsistence. Due to infrequent observations of suckling behaviors, it is not possible to pinpoint an age where independent feeding became the main source of nutrient intake. My first observation of feeding behavior by Cobalt was in September

2016 when Cobalt was seven months old. This event involved Cobalt searching for invertebrates in live trees. In January 2017, when Cobalt was 11 months old, he was feeding more frequently than he was resting, a trend that would continue through the rest of the study (Table 5.1). Greater frequency of feeding than resting is indicative of a reliance on solid foods for the majority of nutrient consumption (Feistner and Ashbourne

1994; Winn 1994). Infants in captivity start tap foraging and gnawing behaviors between

2-3 months of age and become proficient at feeding around nine months old (Feistner and

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Ashbourne 1994; Winn 1994). I did not observe Cobalt start practicing feeding behaviors as early as the captive aye-aye infants, likely because he remained in the nest longer.

However, based on the frequency of his feeding and resting behaviors, Cobalt did become proficient at an age similar to that of captive infants. Therefore, I did not support my prediction that wild aye-ayes would develop proficiency in feeding behaviors at an older age than the captive counterparts.

It is possible that Tsinjo’s absentee parenting necessitated Cobalt’s rapid development of feeding behaviors once outside of the nest. Captive infants had consistent parental attention and were noted to steal and beg for food from their parents

(Feistner and Ashbourne 1994; Winn 1994). Though Cobalt was in frequent association with Tsinjo when learning to feed on invertebrates (September-October 2016) and

Canarium seeds in ripe fruit (February 2017), I never saw him steal food from Tsinjo.

Other than these two periods of learning, Tsinjo frequently ventured away from the nest where Cobalt was parked. Therefore, it is likely that stealing and begging were not a viable option for Cobalt to obtain food. Unable to procure solid foods from his mother,

Cobalt may have been forced to develop his feeding behavior quickly once outside of the nest. However, this would suggest he was not obtaining the necessary nutrients from

Tsinjo, which is contrary to suggested benefits of parked infant strepsirrhines (Tecot et al.

2012). Instead, it seems more likely that Cobalt was more coordinated upon exiting the nest, and therefore needed less time to develop foraging behaviors compared to captive aye-aye young. Future research should explore feeding proficiency as a measure of successful invertebrate removal from substrates to determine when aye-ayes become efficient percussive foragers.

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Cobalt consumed only invertebrates and Canarium seeds, a diet similar in breadth to his mother Tsinjo. Cobalt consumed more invertebrates than Canarium seeds over the course of the study, as was also found with Tsinjo (see Chapter 2). Also, like Tsinjo,

Cobalt consumed more invertebrates from live trees than from deadwood or bamboo.

However, he was more efficient at eating Canarium seeds in ripe fruit (1.0/min) than invertebrates in any substrate (live tree: 0.5/min; deadwood 0.4/min; bamboo: 0.6/min).

Unlike Tsinjo, Cobalt was not observed consuming resources from Vakona trees

(Pandanus utilis, Pandanaceae). It is possible Cobalt was not yet familiar with this item as a potential resource. Alternatively, he was gaining enough nutrients from Canarium seeds in ripe fruit and invertebrates to support his body size and does not necessitate the additional food from Vakona trees. Future research should explore if young aye-ayes readily feed on resources other than invertebrates and Canarium seeds, such as Ravenala madagascariensis nectar, or if they start incorporating these resources at older ages and heavier body weights.

Ranging Behavior

My final objective was to determine when infant ranging behaviors reflect those of their adult counterparts. The nightly ranging behavior shows that Cobalt gradually became more confident ranging further from the nest until, at 18 months of age, he was ranging on average almost the same distances as Tsinjo (Table 5.4). By 18 months of age, Cobalt’s feeding and ranging behaviors were similar to that of an adult aye-aye. It is approximately this age, between 14 and 20 months old, that captive aye-ayes were removed from their parents (Feistner and Ashbourne 1994; Winn 1994). While ranging in captive animals cannot be measured the same way as in the wild, the fact that the

313 captive and wild infants displayed adult behaviors at a similar age indicates no difference in development at this point. Therefore, this result does not support my prediction of a later age of development for wild aye-ayes compared to captive aye-ayes. Future research should examine if habitat quality, which ultimately changes home range size

(see Chapter 3), influences the pace of development of young aye-ayes.

Parental Care and Aye-aye Development

Parked infants typically have more rapid post-natal development than carried young (Kappeler 1998; Ross 2001). Parking results in rapid development because absentee mothers maximize their net energy gain while foraging compared to mothers that carry young (Ross 2001, 2003; Tecot et al. 2012). Consequently, parked young received more enriched nutrition from their parent than carried offspring and are subsequently able to develop more quickly (Ross 2001, 2003; Tecot et al. 2012). For example, mother’s milk in strepsirrhines that park their young, such as lorises (Otolemur and Nycticebus), bushbabies (Galago) and fat-tailed dwarf lemurs (Cheirogaleus), has more dry matter, fat, protein and gross energy concentration than that of strepsirrhines that carry their young, like Lemur and Eulemur (Tilden and Oftedal 1997; Hinde and

Milligan 2011). However, aye-ayes do not appear to conform to expectations of a shortened ontogenetic period. Though Tsinjo parked her infant and foraged alone, Cobalt still developed at a slower pace than other species of parked lemurs. For instance,

Lepilemur ruficaudatus infants were found to be weaned, feeding on foliage and roaming independently at around 50 days old (Hilgartner et al. 2008). Cobalt started feeding on solid foods around seven months old and still occasionally sucked over a year after birth.

Since young aye-ayes have a prolonged development, and infant parking should result in

314 a more rapid developmental pace, as it does in other species, the parental care strategy of aye-ayes is probably not as influential on the developmental trajectory of their young as other factors, i.e., RAH or brain development.

RAH and Aye-aye Development

There appears to be some support for a relationship between the ecological risk aversion hypothesis and aye-aye life history. As previously mentioned, the RAH predicts that primates with continuously available foods, such as folivores, should develop more quickly than those primates with resources that have sporadic availability, such as frugivores (Janson and van Schaik 1993). For strepsirrhines, the inverse is actually the case, with folivores developing more slowly than frugivores (Wright 1999; Godfrey et al.

2004; Tecot et al. 2012). Invertebrates appear to be a continuously available resource for aye-ayes (see Chapter 2). Therefore, based solely on resource availability, aye-ayes appear to follow the trend of other strepsirrhines with ubiquitous foods by developing slowly (Wright 1999; Godfrey et al. 2004; Tecot et al. 2012). Perhaps, as discussed earlier, the slow ontogeny is related to population stability (Godfrey et al. 2004; Tecot et al. 2012). Aye-ayes produce one offspring per birth, have a continuously available resource, and therefore maintain a stable population by maximizing parental investment, i.e., suckling, co-nesting and sharing habitat, in order to minimize infant mortality.

In addition to resource availability, the RAH also predicts that predation will influence primate development (Janson and van Schaik 1993). When predation pressure is high, young are expected to develop quickly and limit their time of vulnerability

(Janson and van Schaik 1993). When there is low predation pressure, selection will favor slow development to minimize the effect of competing for resources with adults by

315 diffusing the energetic costs of maturation over a longer time (Janson and van Schaik

1993). In the present case, it is difficult to assess how predation pressure influences aye- aye infant development as only one predation event was witnessed. Even though parked infants have higher mortality rates than carried infants and therefore should develop more quickly (Janson and van Schaik 1993), Cobalt had a very prolonged developmental period. This runs counter to the RAH argument. Cobalt emerged from the nest with a limited array of fully developed positional behaviors. This may help explain the differences in support and strata use by Cobalt and Tsinjo as discussed in Chapter 4. In

February 2017, despite still not ranging the same distances as Tsinjo, his locomotor skills were sufficient to evade a predation event by a fosa. Therefore, his rate of development was fast enough to ensure survival of a predation attempt. Though Cobalt’s developmental trajectory was rapid enough to avoid predation, it is still longer than would be anticipated for a nested infant, based on the expectations of RAH (Janson and van Schaik 1993).

Aye-aye Brain Development

Lastly, the protracted development of aye-ayes may be related to brain development. As previously mentioned, aye-ayes have the largest brain of any strepsirrhine or nocturnal lemur (Stephan et al. 1981). It has been suggested that primates with large brains experience a protracted development so that energy may be focused toward growing a large brain rather than physical maturation (Charnov and Berrigan

1993; Isler and van Schaik 2006, 2009). However, aye-ayes do not experience any trade- offs in the development of their brain and body during their ontogenetic period (Kaufman et al. 2005; Barrickman and Lin 2010). Indeed, aye-aye young experience the most rapid

316 post-natal body and brain growth in their first two months of life (Barrickman and Lin

2010). In other words, aye-aye young do not have prolonged developmental periods to accommodate brain growth, nor do they decrease body growth to compensate for developing their encephalized brain (Barrickman and Lin 2010). There are two possible explanations for why aye-ayes have simultaneous rapid development of brain and body.

One is that aye-ayes experience a trade-off in intestinal development to accommodate brain and body size development (Barrickman and Lin 2010). The expensive-tissue hypothesis suggests that primates offset the metabolic costs of developing encephalized brains by reducing the energetic expenditure of developing another ‘expensive’ organ

(Aiello and Wheeler 1995). Encephalized brains are energetically expensive to develop and typically require that an organism offset the developmental cost by reducing the metabolic expense of developing other tissues (Aiello and Wheeler 1995). Body size is one metabolic process where an organism can reduce energetic demands, along with the heart, liver, kidney and gastro-intestinal tract (Aiello and Wheeler 1995). Aiello and

Wheeler (1995) identify the gastro-intestinal tract as an organ with reduced energetic investment, based on the shortened length, in primates with encephalized brains. A more complex and elongated gut morphology, e.g., the intestinal tract found in folivorous primates, results in a long food transit time (Milton 1981). This is necessary to extract nutrients from difficult-to-digest resources, such as leaves (Chivers and Hladik 1980).

When a primate has a shortened digestive tract, its food transit time is short (Milton

1981). A primate with a short digestive tract and a metabolically expensive brain must have a diet consisting of high-energy, easily processed resources to maintain the energetic demands of its large brain (Aiello and Wheeler 1995). In primates, a short and

317 simple digestive tract is characteristic of insectivores and frugivores because invertebrates and ripe fruit are typically easily digested, high-energy resources (Chivers and Hladik 1980). Since invertebrates are the aye-aye’s preferred resource (see Chapter

2) and invertebrate consumption is typically associated with a short and simple digestive tract (Chivers and Hladik 1980), then, according to the expensive-tissue hypothesis, the reduced metabolic cost of developing a shortened gastro-intestinal tract will benefit the aye-ayes by offsetting the cost of simultaneous rapid development of body and brain size

(Aiello and Wheeler 1995).

Alternatively, the demands of rapidly growing body size and an encephalized brain simultaneously may be entirely met by the energetic gains provided by maternal care (Barrickman and Lin 2010). However, examining the maternal investment in infant development is beyond the scope of this research.

Finally, some have suggested that slow development of large brains is related to learning complex behaviors, particularly extractive foraging activities (Parker and Gibson

1977, 1979; Gibson 1986; Reader et al. 2011; Parker 2015). Learning how to locate hidden or cryptic resources necessitates a protracted development so the young primate can become efficient at finding and feeding on this important resource (Parker and

Gibson 1977, 1979; Gibson 1986). Invertebrates are cryptic because they are hidden within various substrates throughout the forest (Sterling 1993, 1994). Aye-ayes use complex echolocation behaviors (i.e. percussive foraging) to extract invertebrates from a variety of substrates (Petter 1962, 1977; Gibson 1986; Erickson 1991, 1995; Millikan et al. 1991; Erickson et al. 1998; Dominy et al. 2001). Since aye-ayes, such as Tsinjo and

Cobalt consume invertebrates more consistently than any other resource (see Chapter 2),

318 the cryptic nature of this food item necessitates the aye-aye are proficient at the location and extraction of this resource (McNab 1963; Gaulin 1979; Erickson 1991, 1995;

Erickson et al. 1998). As discussed in Chapter 2, aye-ayes must be able to efficiently procure this resource in sufficient quantities to sustain their large body size. It is likely that this ability develops at a young age over a long period of time, while the infant can still supplement their diet by suckling. This is supported by my observation of Cobalt: from September 2016 to January 2017, he gradually increased the frequency of foraging involving echolocation, but still suckled occasionally and as late as May 2017.

Conclusion

The protracted life history of aye-ayes is likely the result of behavioral and physiological development, both of which are directly linked to their unique feeding behavior. Given that aye-ayes have a high basal metabolic rate (Barrickman and Lin

2010), a longer developmental period may allow young aye-ayes to become proficient at locating and extracting invertebrates from the various substrates with the added security of supplemental suckling. This is particularly important since aye-ayes do not experience any trade-offs in the development of their brain and body during their ontogenetic period

(Kaufman et al. 2005; Barrickman and Lin 2010). Furthermore, the prolonged developmental period may be necessary for full development of the aye-aye brain. Aye- ayes have an enlarged frontal cortex and an increased olfactory lobe, both associated with invertebrate foraging (Kaufman et al. 2005). Invertebrates supply ample nutrients for adult aye-ayes to support their high basal metabolic rate (Barrickman and Lin 2010).

However, aye-ayes necessitate large home ranges to acquire sufficient food (see Chapter

3), and, in the case of Cobalt, the juvenile aye-aye do not exhibit an adult ranging behavior until 17 months of age. Therefore, my study of Cobalt suggests that a 319 protracted developmental period is necessary for aye-ayes to develop the behavioral complexities that will help them procure enough invertebrates to sustain themselves as adults.

Knowing that wild aye-aye’s may display an extended juvenile period is important for determining their population size. Based on captive studies, aye-aye infants were removed from the same enclosure as their mothers between 14-20 months (Feistner and Ashbourne 1994; Winn 1994). In one instance, a captive female had a second offspring before her first, a one-year old, was rehoused (Feistner and Ashbourne 1994).

If wild aye-ayes are assumed to have life histories similar to those of captive animals, this might suggest an interbirth interval of one year, with mothers capable of supporting two offspring simultaneously. However, after 22 months, Cobalt was still nesting with

Tsinjo, no aggressive behaviors were witnessed, and Tsinjo was not observed copulating with another male. This may indicate that aye-aye interbirth intervals are greater in wild populations than in captive groups, possibly because wild offspring have a prolonged period of maternal dependence. This maternal dependence likely involves an extended period of lactation for the mother, ultimately compromising her energetic balance and suppressing her ovulation until the current infant is fully weaned (Schneider 2004). Yet, as already discussed, Cobalt appeared to behave as an independent adult, ranging and feeding in a similar manner to Tsinjo, at 17 months, roughly the same age when captive infants were removed from their mothers (Feistner and Ashbourne 1994; Winn 1994).

Nevertheless, Cobalt remained nested with Tsinjo much longer time than expected given his independent behavior. If most aye-aye offspring remain with a female for 22 months or longer, this would result in longer inter-birth intervals for aye-aye females.

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Ultimately, long inter-birth intervals necessitate reduced estimates on population size as the population adds individuals at a slower rate than expected. Determining the actual inter-birth interval is a necessary step in any conservation planning for this species.

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Table 5.1 Number of night follows, number of occurrences of each behaviors and monthly percent of overall behaviors by Cobalt between August 2016-December 2017 in Torotorofotsy, Madagascar.

Month Follows Rest Travel Feed Play Play w/Tsinjo Suckle Grooming Total (Auto/Allo) Count Count % Count % Count % Count % Count % Count % Count % Aug-16 3 35 83.3% 7 16.7% 0 0% 0 0% 0 0% 0 0% 0 0% 42 Sep-16 3 26 39.4% 36 54.5% 4 6.1% 0 0% 0 0% 0 0% 0 0% 66 Oct-16 5 58 40.6% 24 16.8% 18 12.5% 34 23.8% 8 5.6% 0 0% 1 0.7% 143 Nov-16 5 68 45.3% 52 34.7% 28 18.7% 0 0% 0 0% 0 0% 2 1.3% 150 Dec-16 3 44 56.4% 7 9.0% 27 34.6% 0 0% 0 0% 0 0% 0 0% 78 Jan-17 2 0 0% 14 41.2% 20 58.8% 0 0% 0 0% 0 0% 0 0% 34 Feb-17 9 82 25.7% 67 21.0% 161 50.5% 0 0% 2 0.6% 2 0.6% 5 1.6% 319 Mar-17 6 20 9.4% 115 54.0% 78 36.6% 0 0% 0 0% 0 0% 0 0% 213 Apr-17 6 35 21.7% 56 34.8% 70 43.5% 0 0% 0 0% 0 0% 0 0% 161 May-17 14 125 27.0% 209 45.1% 122 26.4% 1 0.2% 0 0% 1 0.2% 5 1.1% 463 Jun-17 4 38 32.5% 40 34.2% 39 33.3% 0 0% 0 0% 0 0% 0 0% 117 Jul-17 7 31 15.8% 83 42.3% 77 39.3% 0 0% 0 0% 0 0% 5 2.6% 196 Aug-17 10 39 19.5% 100 50.0% 57 28.5% 0 0% 0 0% 0 0% 4 2.0% 200 Sep-17 2 4 14.3% 21 75.0% 2 7.1% 0 0% 0 0% 0 0% 1 3.6% 28 Oct-17 6 38 22.0% 85 49.1% 47 27.2% 0 0% 0 0% 0 0% 3 1.7% 173 Nov-17 9 27 14.9% 97 53.6% 57 31.5% 0 0% 0 0% 0 0% 0 0% 181 Dec-17 8 35 12.8% 115 42.2% 118 43.2% 0 0% 0 0% 0 0% 5 1.8% 273

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Table 5.2 Frequency of association (within 5m) between Cobalt and Tsinjo outside of the nest every month from August 2016-December 2017 in Torotorofotsy, Madagascar.

Month Association out of nest (<5m) Aug-16 10 Sep-16 18 Oct-16 20 Nov-16 3 Dec-16 0 Jan-17 0 Feb-17 58 Mar-17 0 Apr-17 0 May-17 5 Jun-17 0 Jul-17 2 Aug-17 0 Sep-17 1 Oct-17 0 Nov-17 0 Dec-17 0

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Month Live Tree Deadwood Bamboo Canarium seeds Count Average Count Average Count Average Count Average Sep-16 11 0.4/min 2 2.0/min - - - - Oct-16 30 0.4/min - - 3 0.3/min - - Nov-16 25 0.4/min 11 0.3/min 4 0.7/min - - Dec-16 31 0.4/min - - 17 0.4/min - - Jan-17 33 0.4/min ------Feb-17 46 0.4/min 47 0.4/min - - 483 0.9/min Mar-17 118 0.7/min 24 0.6/min - - 178 1.5/min Apr-17 29 0.3/min - - 10 0.8/min 167 0.7/min May-17 270 0.9/min 21 0.4/min 1 1.0/min 152 1.3/min Jun-17 38 0.5/min 17 1.0/min - - 80 1.8/min Jul-17 123 0.4/min 1 1.0/min 3 1.5/min - - Aug-17 64 0.4/min 16 0.6/min 7 0.5/min - - Sep-17 2 0.3/min ------Oct-17 62 0.5/min 37 0.5/min - - - - Nov-17 39 0.4/min 34 0.3/min - - - - Dec-17 121 0.4/min 76 0.4/min 33 1.2/min - - TOTAL 1042 0.5/min 286 0.4/min 78 0.6/min 1060 1.0/min

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Table 5.4 Number of total follows and morning follows, as well as average distances traveled each month by Tsinjo and Cobalt from January 2016 to December 2017 in Torotorofotsy, Madagascar.

Month Tsinjo Cobalt Total Number Average Total Number Average Number of of AM Distance Number of AM Distance Follows Follows (m) of Follows (m) Follows Jan-16 5 3 555.3 Feb-16 4 2 517.3 Mar-16 7 4 496.8 Apr-16 7 3 483.1 May-16 3 0 1034.6 Jun-16 3 2 957.0 Jul-16 6 3 372.0 Aug-16 5 1 546.6 2 0 126.7 Sep-16 7 3 512.1 2 0 282.2 Oct-16 7 0 491.4 5 2 86.7 Nov-16 5 2 430.6 5 2 360.7 Dec-16 7 3 239.1 3 0 94.8 Jan-17 3 2 752.3 2 2 282.2 Feb-17 5 2 426.5 8 3 253.4 Mar-17 7 2 527.4 6 3 259.6 Apr-17 3 2 252.7 6 4 382.3 May-17 12 4 546.7 14 5 288.1 Jun-17 4 1 809.8 3 0 153.2 Jul-17 6 1 562.9 7 2 321.6 Aug-17 8 4 381.6 9 6 303.4 Sep-17 7 4 427.7 2 2 158.1 Oct-17 8 3 467.1 6 2 435.6 Nov-17 6 2 659.4 9 4 623.3 Dec-17 6 2 549.2 8 3 438.4

325

250

200

150 Rest Travel Feed

100 NumberOccurrences of

0 1-Jan 1-Feb 1-Mar 1-Apr 1-May 1-Jun 1-Jul 1-Aug 1-Sep 1-Oct 1-Nov 1-Dec

Figure 5.1 Occurrences of resting, traveling and feeding behaviors for Cobalt from August 2016 through December 2017.

326

600

500

400

Live Tree

300 Deadwood Bamboo Canarium seeds

200 Number of Resources NumberResources of Consumed

100

0 1-Jan 1-Feb 1-Mar 1-Apr 1-May 1-Jun 1-Jul 1-Aug 1-Sep 1-Oct 1-Nov 1-Dec

Figure 5.2 Number of invertebrates in various substrates (live tree, deadwood and bamboo) and Canarium seeds consumed by Cobalt between September 2016 and December 2017. 327

Chapter 6 Conclusion

This chapter provides an overview of the results on my research on the aye-aye,

Daubentonia madagascariensis. It provides (1) an overview of the dietary profile, (2) home range estimates, (3) an examination of the various positional behaviors, and (4) a review of the development of a subadult aye-aye. It concludes with suggestions for future research objectives.

My main objective was to determine the significance of invertebrates in aye-aye ecology. Previous research has suggested that either Canarium seeds (Iwano and

Iwakawa 1988; Iwano 1991) or Ravenala nectar (Ancrenaz et al. 1994) are the aye-aye’s most important resource. Invertebrates were implied to be a staple fallback resource for aye-ayes, consumed in significant quantities only when other resources were not available (Sterling and McCreless 2006; Lambert 2007; Marshall and Wrangham 2007).

However, all prior studies were conducted on either introduced populations on the island of Nosy Mangabe (Iwano and Iwakawa 1988; Iwano 1991; Sterling 1993,1994) or in disturbed habitats (Ancrenaz et al. 1994). Primate behavior is known to vary significantly in response to deforestation and reduction in forest size (Irwin 2008; Chaves et al. 2012), so it follows that these earlier results may not reflect the behaviors of populations in undisturbed forest. My research in undisturbed forest indicates invertebrates are not only the preferred aye-aye resource, but that they influence ranging

328 behavior, locomotor behaviors, postural behaviors, and infant development. Thus, invertebrates are significantly more important to aye-aye ecology than previously suggested (Iwano and Iwakawa 1988; Sterling and McCreless 2006).

During the course of this study, both the female and her infant consumed invertebrates more frequently than any other resource. In fact, Tsinjo, the female, not only preferred invertebrates but often consumed them to the exclusion of other resources.

Additionally, live trees were the most frequently used substrate for invertebrate foraging, in contrast to previous reports (Petter 1977; Sterling 1993, 1994). While the aye-ayes consumed Canarium seeds and Tsinjo occasionally ate an unknown resource from

Vakona trees (Pandanus utilis, Pandanaceae), there were no instances of Torotorofotsy aye-ayes consuming Ravenala nectar despite its availability. Given invertebrates are the preferred resource in undisturbed forests, but not in smaller perturbed forests (Sterling

1993, 1994; Ancrenaz et al. 1994; Randimbiharinirina et al. 2018), it is possible that deforestation is negatively influencing invertebrate population density and species richness in disturbed forests (Sefczek et al. 2017). If this is the case, aye-ayes in

Mananara-Nord Biosphere Reserve may preferentially consume Ravenala nectar

(Ancrenaz et al. 1994) out of necessity because of decreased invertebrate abundance. On

Nosy Mangabe, where the population was introduced and predators are absent, aye-ayes may be overcrowded and over-harvesting invertebrate assemblages. Decreased availability of invertebrates throughout the year may require aye-ayes in perturbed areas to consume a greater variety of resources than the aye-ayes in the present study (Sterling

1993, 1994). Because it is assumed that invertebrates are continuously available and

329 widely distributed in undisturbed forest, the ranging behavior of aye-ayes in habitats such as that found at Torotorofotsy is critical to a broader understanding of how they optimally forage and sustain themselves on this food.

The home ranges for the adult male and adult female examined in this study were larger than those reported from previous studies. Earlier reports identified female home ranges of between 30-98 ha and male ranges of between 120-974 ha (Sterling 1993,

1994; Randimbiharinirina et al. 2018). In the undisturbed forest of Torotorofotsy the female’s home range was approximately 713.6 ha and the male’s home range was about

1587.5 ha. Seasonal and annual ranging patterns for the female aye-aye indicated that invertebrates were critical to the aye-aye’s ranging behavior. As observed in the KDE maps, the adult female Tsinjo’s most frequently-used portions of her habitat were those where invertebrate feeding sites were concentrated. Additionally, Tsinjo consumed invertebrates throughout her entire habitat but never used the same portion of her territory in consecutive seasons. Tsinjo’s home range use differed in 2017 than 2016, likely due to the presence of a dependent infant during 2016. During five of the six seasons covered by this study, the female aye-aye consumed only invertebrates and/or Canarium seeds in ripe fruit. The season in 2017 with the most limited range use (season 2) coincided with an increase in dietary breadth, including consumption of a previously unknown Vakona resource. Since invertebrates were the sole resource consumed for the majority of the study, large home ranges were likely needed so Tsinjo could continue to subsist primarily on invertebrates. Tsinjo behaved as an energy maximizer, spending most of her time feeding, foraging or traveling, often in the quest for invertebrates. Invertebrates are a

330 potentially evenly distributed resource (Sefczek et al. 2017) and her systematic ranging behavior throughout her territory may permit invertebrate populations to rebound after feeding bouts. If this is true, the noyau social system and non-overlapping female home ranges (Sterling 1993, 1994) may be necessary to ensure aye-ayes do not visit locations where invertebrates were recently removed by another aye-aye. Knowing that invertebrates can be obtained throughout the forest at any level and in any woody substrate (Sterling 1993, 1994a), an examination of the positional behaviors employed during feeding and foraging may elucidate how aye-ayes maximize energetic gain while locating sufficient quantities of this resource across their territory.

Previous studies on the positional behavior of free-ranging aye-ayes in Mananara-

Nord Biosphere Reserve and of captive aye-ayes found that these lemurs most frequently used quadrupedal locomotion for traveling, rarely leaped, and spent the majority of their time in the highest parts of the canopy on medium and small supports (Curtis 1992;

Ancrenaz et al. 1994; Curtis and Feistner 1994). The most frequent locomotor behaviors used during traveling by the female and subadult aye-aye in Torotorofotsy were leaping and vertical leaping. These individuals typically travelled along trunks in the main canopy. When foraging, they frequently used head-first descent and climbing, frequently along trunks. While the female foraged in the main canopy, low canopy and understory most frequently, the subadult foraged most often in the main and high canopy. Despite concentrating feeding efforts in different forest levels, the female in the understory and the subadult in the main canopy, trunks were the most commonly used support. Both aye-ayes used uni-manual and bi-manual clinging postures most frequently when feeding.

331

This indicates that the aye-ayes in the undisturbed forest are heavily reliant on their specialized musculature morphology, specifically that of the upper extremities (Soligo

2005), while employing a variety of positional behaviors in order to maximize invertebrate extraction. As predicted by Soligo (2005), invertebrate feeding was the activity that required the most frequent use of the aye-aye’s clawed digits and specialized forelimb musculature. Indeed, the diversity of aye-aye positional behaviors is reflective of their use of every forest level in pursuit of invertebrates. In order to develop this full- range of positional behaviors, young aye-ayes likely require an extended period of development.

Aye-ayes have one of the longest juvenile periods of any strepsirrhine (Feistner and Ashbourne 1994; Winn 1994), and have similar rates of brain and body development throughout their ontogenetic period (Barrickman and Lin 2010). The developmental period of a free-ranging aye-aye subadult was longer than that of its captive counterparts, matching results from studies of other primates (Anderson and Simpson 1979; Fairbanks and McGuire 1984; Lee 1987; Altmann and Muruthi 1988). The young male aye-aye at

Torotorofotsy had a delayed age at first emergence from nest, initial feeding behavior, and weaning than the previously studied captive infants (Feistner and Ashbourne 1994;

Winn 1994). The only similarity between wild and captive aye-aye development was in the age of independent feeding which occurred in both contexts at roughly nine to ten months old (Feistner and Ashbourne 1994). The extended ontogenetic period in wild aye-ayes is likely due to 1) the development of their specialized brain for processing large amounts of sensorimotor information when foraging for invertebrates (Kaufman et al.

332

2005), and 2) the development of their full behavioral repertoire which is necessary to efficiently forage for invertebrates. Thus, it appears that nearly every aspect of aye-ayes, morphology, behavior and life history, has evolved to fill the ecological niche of an extractive forager of invertebrates. This species is not too large to subsist on insects (Kay

1975) because it has a multitude of highly specialized morphological, behavioral and life- history adaptations which allow it to efficiently hunt wood-boring invertebrates (Gaulin

1979).

The results presented here provide a baseline for aye-aye behavior in undisturbed forest. However, both the adult male and female examined in this study dispersed beyond the boundaries of Torotorofotsy. The study site at Torotorofotsy and the adjacent

Mantadia National Park are both portions of the extensive corridor of rainforest that runs the length of Madagascar’s eastern border. Therefore, in theory, though these study animals represent a small portion of the larger eastern rainforest population, it is expected that these aye-ayes will disperse and contribute to gene flow (Lindenmayer 1998;

Mittermeier et al. 2005). But there is no guarantee that the forest types within the rainforest corridor will present similar ecological challenges. Consequently, aye-aye behavior may change significantly as a function of habitat type. Future research should examine the variability in aye-aye behaviors throughout the Andasibe-Mantadia-

Zahamena eastern rainforest corridor in order to better understand the adaptability of these lemurs.

Additionally, aye-ayes in the eastern rainforest represent only a fraction of the total distribution of this species on Madagascar. Elsewhere, aye-ayes are known to

333 inhabit a diversity of habitats including the dry forests in the north and west

(Andriamisedra et al. 2015). These individually unique ecosystems have a distinct floral diversity which may result in behaviors different from those documented in

Torotorofotsy. For instance, in a two-month study of feeding traces, Andriamisedra and colleagues (2015) found that aye-ayes used more deadwood than live trees in dry forests but the opposite in eastern rainforests. Furthermore, the baseline of aye-aye behavior I establish here appears to be different from that of aye-ayes reported on in disturbed forests and human modified habitats (Petter 1977; Ancrenaz et al. 1994). Future research should explore the dietary, ranging and positional behavior differences of aye-ayes in varying ecosystems.

334

Bibliography

Aiello LC and P Wheeler. 1995. The expensive-tissue hypothesis: The brain and the

digestive system in human and primate evolution. Current Anthropology 36: 199-

221.

Altmann J. 1974. Observational study of behavior: Sampling methods. Behaviour 49:

227-267.

Altmann J and S Alberts. 1987. Body mass and growth rates in a wild primate population.

Oceologia 72: 15-20.

Altmann J and P. Muruthi. 1988. Differences in daily life between semi-provisioned and

wild-feeding baboons. American Journal of Primatology 15: 213-221.

Ancrenaz M, I Lackman-Ancrenaz and N Mundy. 1994. Field observations of aye-ayes

(Daubentonia madagascariensis) in Madagascar. Folia Primatologica 62: 22-36.

Anderson DM and MJA Simpson. 1979. Breeding performance of a captive colony of

rhesus macaques (Macaca mulatta). Laboratory Animals 13: 275-281.

Anderson HB, ME Thompson, CD Knott and L Perkins. 2008. Fertility and mortality

patterns of captive Bornean and Sumatran orangutans: Is there a species

difference in life history? Journal of Human Evolution 54: 34-42.

Andriamisedra RT, M Aylward, SE Johnson, EE Louis Jr and BM Raharivololona. 2015.

Détermination de quelques aspects de l’écologie de Daubentonia

madagascariensis dans deluxe forêt malgaches: la Réserve Spéciale de Manombo,

Sud-est, et la Forêt de Beanka, Center-oust de Madagascar. Lemur News 19: 44-

50. 335

Baden AL, PC Wright, EE Louis Jr. and BJ Bradley. 2013. Communal nesting, kinship,

and maternal success in a social primate. Behavioral Ecology and Sociobiology

67: 1939-1950.

Barrette M, G Boivin, J Brodeur and LA Giraldeau. 2010. Travel time affects optimal

diet in depleting patches. Behavioral Ecology and Sociobiology 64: 593-598.

Barrickman NL and MJ Lin. 2010. Encephalization, expensive tissues, and energetic: An

examination of the relative costs of brain size in Strepsirrhines. American Journal

of Physical Anthropology 143: 579-590.

Benchimol M and CA Peres. 2014. Predicting primate local extinctions within ‘real-

world’ forest fragments: A pan-neotropical analysis. American Journal of

Primatology 76: 289-302.

Bezanson M. 2017. Primate positional behavior development and evolution. Annual

Review of Anthropology 46: 279-298.

Biebouw K. 2009. Home range size and use in Allocebus trichotis in Analamazaotra

Special Reserve, Central Eastern Madagascar. International Journal of

Primatology 30: 367-386.

Blomquist GE. 2009. Trade-off between age of first reproduction and survival in a female

primate. Biology Letters 5: 339-342.

Blumberg MS and G Sokoloff. 1998. Thermoregulatory competence and behavioral

expression in the young of altricial species-revisited. Developmental

Psychobiology 33: 107-123.

336

Bouget C, L Laurier, B Nusillard and G Parmain. 2013. In search of the best local habitat

drivers for saproxylic battle diversity in temperate deciduous forests. Biodiversity

Conservation 22: 2111-2130.

Brockman DK, MS Willis and WB Karesh. 1987. Management and husbandry of ruffed

lemurs, Varecia variegata, at the San Diego Zoo. II. Reproduction, pregnancy,

parturition, litter size, infant care, and reintroduction of hand-raised infants. Zoo

Biology 6: 349-363.

Buzzard PJ. 2006. Ranging patterns in relation to Seasonality and frugivory among

Cercopithecus campbelli, C. Petaurista, and C. Diana in the Tai Forest.

International Journal of Primatology 27: 559-573.

Cameron KH and SR Leather. 2012. How good are carabid beetles (Coleoptera,

Carabidae) as indicators of invertebrate abundance and order richness?

Biodiversity Conservation 21: 763-779.

Cannon CH and M Leighton. 1994. Comparative locomotor ecology of gibbons and

macaques: Selection of canopy elements for crossing gaps. American Journal of

Physical Anthropology 93: 505-524.

Cant JGH. 1986. Locomotion and feeding postures of spider and howling monkeys: Field

study and evolutionary interpretation. Folia Primatologica 46: 1-14.

Cant JGH. 1992. Positional behavior and body size of arboreal primates: A theoretical

framework for field studies and an illustration of its application. American

Journal of Physical Anthropology 88: 273-282.

337

Cartmill M. 1972. Arboreal adaptations and the origin of the order Primates. In: The

Functional and Evolutionary Biology of Primates. Tuttle RH, ed. Pp: 97-122.

Chicago: Aldine-Atherton.

Cartmill M. 1974. Pads and claws in arboreal locomotion. In: Primate Locomotion.

Jenkins F, ed. Pp: 45-83. New York: Academic Press.

Cartmill M. 1979. Daubentonia, dactylopsila, woodpeckers, and klinorhynchy. In:

Prosimian Biology. Martin RD, GA Doyle and AC Walker, eds. Pp: 655-672.

Pittsburgh, PA: University of Pittsburgh Press.

Cartmill M and K Milton. 1977. The lorisiform wrist joint and the evolution of

“brachiating” adaptations in the Hominoidea. American Journal of Physical

Anthropology 47: 249-272.

Chapman CA. 1988. Patch use and patch depletion by the spider and howling monkeys

of Santa Rosa National Park, Costa Rica. Behaviour 105: 99-116.

Chapman CA. 1990. Ecological constraints on group size in three species of Neotropical

primates. Folia Primatologica 55: 1-9.

Chapman CA and LJ Chapman. 1990. Dietary variability in primate populations.

Primates 31: 121-128.

Chapman CA and MSM Pavelka. 2005. Group size in folivorous primates: Ecological

constraints and the possible influence of social factors. Primates 46: 1-9.

Chapman CA, MJ Lawes and HAC Eeley. 2006. What hope for African primate

diversity? African Journal of Ecology 44: 116-133.

338

Chapman CA, RW Wrangham and LJ Chapman. 1995. Ecological constriants on group

size: An analysis of spider monkey and chimpanzee subgroups. Behavior,

Ecology and Sociobiology 36: 59-70.

Charles-Dominique P. 1995. Food distribution and reproductive constraints in the

evolution of social structure: Nocturnal primates and other mammals. In:

Creatures of the Dark: The Nocturnal Prosimians. Alterman L, GA Doyle and MK

Izard, eds. Pp: 425-438. New York: Plenum Press.

Charnov EL. 1993. Life History Invariants: Some Explorations of Symmetry in

Evolutionary Ecology. Oxford: Oxford University Press.

Charnov EL and D Berrigan. 1993. Why do female primates have such long lifespans and

so few babies? or Life in the slow lane. Evolutionary Anthropology 1: 191-194.

Charnov EL, GH Orlans and K Hyatt. 1976. Ecological implications of resource

depression. The American Naturalist 110: 247-259.

Chaves OM, KE Stoner and V Arroyo-Rodriguez. 2012. Differences in diet between

spider money groups living in forest fragments and undisturbed forest in Mexico.

Biotropica 44: 105-113.

Chisholm JS, PT Ellison, J Evans, PC Lee, LS Lieberman, Z Pavlik, AS Ryan, EM

Salter, WA Stini and CM Worthman. 1993. Death, hope and sex: Life-history

theory and the development of reproductive strategies. Current Anthropology 34:

1-24.

339

Chivers DJ and CM Hladik. 1980. Morphology of the gastrointestinal tract in primates:

Comparisons with other mammals in relation to diet. Journal of Morphology 166:

337-386.

Clutton-Brock TH. 1977. Some aspects of intraspecific variation in feeding and ranging

behaviour in primates. In: Primate Ecology: Studies of Feeding and Ranging

Behaviour in Lemurs, Monkeys and Apes. Clutton-Brock TH, ed. Associated

Press: New York. Pp: 539-556.

Cock MJW. 1978. The assessment of preference. The Journal of Animal Ecology. 47:

805-816.

Cohn JP. 1993. Madagascar’s mysterious aye-ayes. BioScience 43: 668-671.

Coley PD and JA Barone. 1996. Herbivory and plant defenses in tropical forests. Annual

Review of Ecological Systems 27: 305-335.

Conner RN, SD Jones and GD Jones. 1994. Snag condition and woodpecker foraging

ecology in bottomland hardwood forest. The Wilson Bulletin 106: 242-257.

Constantino PJ, PW Lucas, JJW Lee and BR Lawn. 2009. The influence of fallback foods

on great ape tooth enamel. American Journal of Physical Anthropology 140: 653-

660.

Cunningham E and C Janson. 2007. Integrating information about location and value of

resources by white-faced saki monkeys (Pithecia pithecia). Animal Cognition 10:

293-304.

Curtis DJ. 1992. Substrate use in captive aye-ayes, Daubentonia madagascariensis.

Dodo: Journal of the Wildlife Preservation Trusts 28: 30-44.

340

Curtis DJ and ATC Feistner. 1994. Positional behaviour in captive aye-ayes

(Daubentonia madagascariensis). Folia Primatologica 62: 155-159.

Daly DC, MM Harley, MC Martinez-Habibe and A Weeks. 2010. Burseraceae. In:

Flowering Plants. Eudicots. Kubitzki K, ed. Pp 76-104. Heidelberg, Germany:

Springer

Daly DC, J Raharimampionona and S Federman. 2015. A revision of Canarium L.

(Burseraceae) in Madagascar. Adansonia 37: 277-345.

Dammhahn M and PM Kappeler. 2005. Social system of Microcebus berthae, the

world’s smallest primate. International Journal of Primatology 26: 407-435.

Dammhahn M and PM Kappeler. 2009. Females go where the food is: Does the socio-

ecological model explain variations in social organization of solitary foragers?

Behavioral Ecology and Sociobiology 63: 939-952.

Demes B, WL Jungers, TS Gross and JG Fleagle. 1995. Kinetics of leaping primates:

Influence of substrate orientation and compliance. American Journal of Physical

Anthropology 96: 419-429.

Demes B, WL Jungers, JG Fleagle, RE Wunderlich, BG Richmond and P Lemelin. 1996.

Body size and leaping kinematic in Malagasy vertical clingers and leapers.

Journal of Human Evolution 31: 367-388.

DeSolla SR, R Bonduriansky and RJ Brooks. 1999. Eliminating autocorrelation reduces

biological relevance of home range estimates. Journal of Animal Ecology 68: 221-

234.

341

DeVore I. 1963. A comparison of the ecology and behavior of monkeys and apes. In:

Classification and Human Evolution. Washburn SL, ed. Routledge: New York.

Pp: 301-319.

Dew JL and PC Wright. 1998. Frugivory and seed dispersal by four species of primate in

Madagascar’s eastern rain forest. Biotropica 30: 425-437.

Di Bitetti MS, EML Vidal, MC Baldovino and V Benesovsky. 2000. Sleeping site

preferences in tufted capuchin monkeys (Cebus paella nigritus). American

Journal of Primatology 50: 257-274.

Dolch R, RD Hilgartner, JN Ndriamiary and H Randriamahazo. 2004. The grandmother

of all bamboo lemurs - evidence for the occurrence of Hapalemur simus in

fragmented rainforest surrounding the Torotorofotsy marshes, Central Eastern

Madagascar. Lemur News 9: 24-26.

Dominy NJ, PW Lucas, D Osorio and N Yamashita. 2001. The sensory ecology of

primate food perception. Evolutionary Anthropology 10: 171-186.

Doran DM. 1992. Comparison of instantaneous and locomotor bout sampling methods: A

case study of adult male chimpanzee locomotor behavior and substrate use.

American Journal of Physical Anthropology 89: 85-99.

Doran-Sheehy DM, D Greer, P Mongo and D Schwindt. 2004. Impact of ecological and

social factors on ranging in Western Gorillas. American Journal of Primatology

64: 207-222.

Dunbar DC and GL Badam. 1998. Development of posture and locomotion in free-

ranging primates. Neuroscience and Behavioral Reviews 22: 541-546.

342

Dunbar RIM. 1998. The social brain hypothesis. Evolutionary Anthropology 6: 178-190.

Dunham NT. 2015. Ontogeny of positional behavior and support use among Colobus

angolensis palliatus of the Diani Forest, Kenya. Primates 56: 183-192.

Ebensperger LA and DT Blumstein. 2006. Sociality in New World hystricognath rodents

is linked to predators and burrow digging. Behavioral Ecology 17: 410-418.

Emlen JM. 1966. The role of time and energy in food preference. The American

Naturalist 100: 611-617.

Emlen ST and LW Oring. 1977. Ecology, sexual selection and the evolution of mating

systems. Science 197: 215-223.

Erhart EM and DJ Overdorff. 2008. Spatial memory during foraging in prosimian

primates: Propithecus edwardsi and Eulemur fulvus rufus. Folia Primatologica

79: 185-196.

Erickson CJ. 1991. Percussive foraging in the aye-aye, Daubentonia madagascariensis.

Animal Behavior 41: 793-801.

Erickson CJ. 1995. Feeding sites for extractive foraging by the aye-aye, Daubentonia

madagascariensis. American Journal of Primatology 35: 235-240.

Erickson CJ, S Nowicki, L Dollar and N Goehring. 1998. Percussive foraging: Stimuli

for prey location by aye-ayes (Daubentonia madagascariensis). International

Journal of Primatology 19: 111-122.

Estrada A and R Coates-Estrada. 1996. Tropical rain forest fragmentation and wild

populations of primates at Los Tuxtlas, Mexico. International Journal of

Primatology 17: 759-783.

343

Fairbanks LA and MT McGuire. 1984. Determinants of fecundity and reproductive

success in captive vervet monkeys. American Journal of Primatology 7: 27-38.

Fan PF, HL Fei, MB Scott, W Zhang and CY Ma. 2011. Habitat and food choice of the

critically endangered cal vit gibbon (Nomascus nasutus) in China: Implications

for conservation. Biological Conservation 144: 2247-2254.

Farris ZJ, TL Morelli, T Sefczek and PC Wright. 2011. Comparing aye-aye

(Daubentonia madagascariensis) presence and distribution between degraded and

non-degraded forest within Ranomafana National Park, Madagascar. Folia

Primatologica 82: 94-106.

Feistner ATC and CJ Ashbourne. 1994. Infant development in a captive bred aye-aye

(Daubentonia madagascariensis) over the first year of life. Folia Primatologica

62: 74-92.

Feistner ATC, EC Price and GW Milliken. 1994. Preliminary observations on hand

preference for tapping, digit-feeding and food-holding in captive aye-ayes

(Daubentonia madagascariensis). Folia Primatologica 62: 136-141.

Fleagle JG. 1976a. Locomotion and posture of the Malayan siamang and implications for

Hominoid evolution. Folia Primatologica 26: 245-269.

Fleagle JG. 1976b. Locomotor behavior and skeletal anatomy of sympatric Malaysian

leaf monkeys (Presbytis obscura and Presbytis melalophos). Yearbook of

Physical Anthropology 20: 440-453.

344

Fleagle JG. 1984. Primate locomotion and diet. In: Food Acquisition and Processing in

Primates. Chivers DJ, BA Wood and A Bilsborough, eds. Pp: 105-117. New

York: Plenum Press.

Fleagle JG. 2013. Primate Adaptation and Evolution, 3rd Edition. New York: Academic

Press.

Fleagle JG and DE Lieberman. 2015. Major transformations in the evolution of primate

locomotion. In: Great Transformations in Vertebrate Evolution. Dial KP, N

Shubin and EL Brainerd, eds. Pp: 257-278. Chicago: The University of Chicago

Press.

Fleagle JG and DJ Meldrum. 1988. Locomotor behavior and skeletal morphology of two

sympatric pitheciine monkeys, Pithecia pithecia and Chiropotes satanas.

American Journal of Primatology 16: 227-249.

Fleagle JG and RA Mittermeier. 1980. Locomotor behavior, body size, and comparative

ecology of seven Surinam monkeys. American Journal of Physical Anthropology

52: 301-314.

Fleagle JG and RA Mittermeier. 1981. Differential habitat use by Cebus apella and

Saimiri sciureus in Central Surinam. Primates 22: 361-367.

Fontaine R. 1990. Positional behavior in Saimiri boliviensis and Ateles geoffroyi.

American Journal of Physical Anthropology 82: 485-508.

Ganzhorn J and J Rabesoa. 1986. The aye-aye (Daubentonia madagascariensis) found in

the eastern rainforest of Madagascar. Folia Primatologica 46: 125-126.

345

Ganzhorn JG, SJ Rakotondranary and YR Ratovonamana. 2011. Habitat description and

phenology. In: Field and laboratory methods in primatology: A practical guide,

2nd edition. Setchell JM and DJ Curtis, eds. Pp: 51-68. New York: Cambridge

University Press.

Garber PA. 1980. Locomotor behavior and feeding ecology of the Panamanian tamarin

(Saguinus oedipus geoffroyi, Callitrichidae, Primates). International Journal of

Primatology 1: 185-201.

Garber PA. 1984. Proposed nutritional importance of plant exudates in the diet of the

Panamanian tamarin, Saguinus oedipus goeffroyi. International Journal of

Primatology 5: 1-15.

Garber PA. 1987. Foraging strategies among living primates. Annual Review of

Anthropology 16: 339-364.

Garber PA. 1989. Role of spatial memory in primate foraging patterns: Saguinus mystax

and Saguinus fuscicollis. American Journal of Primatology 12: 203-216.

Garber PA. 1991. A comparative study of positional behavior in three species of tamarin

monkeys. Primates 32:219-230.

Garber PA. 1992. Vertical clinging, small body size, and the evolution of feeding

adaptations in the Callitrichinae. American Journal of Physical Anthropology 88:

469-482.

Garber PA. 1993. Seasonal patterns of diet and ranging in two species of tamarin

monkeys: Stability versus variability. International Journal of Primatology 14:

145-166.

346

Garber PA and JD Pruetz. 1995. Positional behavior in moustached tamarin monkeys:

Effects of habitat on locomotor variability and locomotor stability. Journal of

Human Evolution 28: 411-426.

Garber PA and JA Rehg. 1999. The ecological role of the prehensile tail in white-faced

capuchins (Cebus capucinus). American Journal of Physical Anthropology 110:

325-339.

Garber PA and LM Paciulli. 1997. Experimental field study of spatial memory and

learning in wild capuchin monkeys (Cebus capucinus). Folia Primatologica 68:

236-253.

Garcia C, PC Lee and L Rosetta. 2009. Growth in a colony living Anubis baboon infants

and its relationship with maternal activity budgets and reproductive status.

American Journal of Physical Anthropology 138: 123-135.

Gaulin SJC. 1979. Jarman/Bell model of primate feeding niches. Human Ecology 7: 1-20.

Gebo DL. 1992. Locomotor and postural behavior in Alouatta palliate and Cebus

capucinus. American Journal of Primatology 26: 277-290.

Gebo DL and CA Chapman. 1995. Positional behavior in five sympatric Old World

monkeys. American Journal of Physical Anthropology 97: 49-76.

Gibeault S and SE MacDonald. 2000. Spatial memory and foraging competition in

captive western lowland gorillas (Gorilla gorilla gorilla). Primates 41: 147-160.

Gibson KR. 1986. Cognition, brain size and the extraction of embedded food resources.

In: Primate ontogeny, cognition and social behaviour. Else JG and PC Lee, eds.

Pp: 93-103. Cambridge: Cambridge University Press.

347

Glander KE. 1994. Morphometrics and growth in captive aye-ayes (Daubentonia

madagascariensis). Folia Primatologica 62: 108-114.

Godfrey LE, KE Samonds, WL Jungers, MR Sutherland and MT Irwin. 2004.

Ontogenetic correlates of diet in Malagasy lemurs. American Journal of Physical

Anthropology 123: 250-276.

Goix E. 1993. L’utilisation de la main chez le aye-aye en captivité (Daubentonia

madagascariensis) (Prosimiens, Daubentoniidés). Mammalia 57: 171-188.

Grand TI. 1972. A mechanical interpretation of terminal branch feeding. Journal of

Mammalogy 53: 198-201.

Grove SJ. 2002. Saproxylic insect ecology and the sustainable management of forests.

Annual Review of Ecological Systems 33: 1-23.

Guisan A, O Broennimann, R Engler, M Vust, NG Yoccoz, A Lehmann and NE

Zimmermann. 2006. Using niche-based models to improve the sampling of rare

species. Conservation Biology 20: 501-511.

Gursky S. 2000. Effect of seasonality on the behavior of an insectivorous primate,

Tarsius spectrum. International Journal of Primatology 21: 477-495.

Hanks LM. 1999. Influence of the larval host plant on reproductive strategies of

cerambycid beetles. Annual Review of Entomology 44: 483-505.

Harcourt AH and DA Doherty. 2005. Species-area relationships of primates in tropical

forest fragments: A global analysis. Journal of Applied Ecology 42: 630-637.

Harris TR and CA Chapman. 2007. Variation in diet and ranging of black and white

colobus monkeys in Kibale National Park, Uganda. Primates 48: 208-221.

348

Harrison ME and AJ Marshall. 2011. Strategies for the use of fallback foods in apes.

International Journal of Primatology 32: 531-565.

Harvey PH and TH Clutton-Brock. 1981. Primate home-range size and metabolic needs.

Behavioral Ecology and Sociobiology 8: 151-155.

Hemingway CA. 1995. Feeding and reproductive strategies of the Milne-Edwards’

sifaka, Propithecus diadema edwardsi [dissertation]. Durham, NC: Duke

University.

Hemingway CA. 1998. Selectivity and variability in the diet of Milne-Edwards’ sifakas

(Propithecus diadema edwardsi): Implications for folivory and seed-eating.

International Journal of Primatology 19: 355-377

Hemingway CA and N Bynam. 2005. The influence of seasonality on primate diet and

ranging. In: Seasonality in Primates: Studies of Living and Extinct Human and

Non-human Primates. Brockton DK and CP van Schaik, eds. Pp: 57-104.

Cambridge: Cambridge University Press.

Hilgartner R, D Zinner and PM Kappeler. 2008. Life history traits and parental care in

Lepilemur ruficaudatus. American Journal of Primatology 70: 2-11.

Hinde K and LA Milligan. 2011. Primate milk: Proximate mechanisms and ultimate

perspectives. Evolutionary Anthropology 20: 9-23.

Hixon MA. 1982. Energy maximizers and time minimizers: Theory and reality. The

American Naturalist 119: 596-599.

349

House AE, BJ House and MB Campbell. 1981. Measures of interobserver agreement:

Calculation formulas and distribution effects. Journal of Behavioral Assessment

3: 37-57.

Hunt KD, JGH Cant, DL Gebo, MD Rose, SE Walker and D Youlatos. 1996.

Standardized descriptions of primate locomotor and postural modes. Primates 37:

363-387.

Hylander WL. 1975. Incisor size and diet in anthropoids with special reference to

Cercopithecidae. Science 189: 1095-1098.

Irwin MT. 2008. Diademed sifaka (Propithecus diadema) ranging and habitat use in

continuous and fragmented forest: Higher density but lower viability in

fragments? Biotropica 40: 231-240.

Isbell LA. 1991. Contest and scramble competition: Patterns of female aggression and

ranging behavior among primates. Behavioral Ecology 2: 143-155.

Isler K and CP van Schaik. 2006. Metabolic costs of brain size evolution. Biology Letters

2: 557-560.

Isler K and CP van Schaik. 2009. The expensive brain: A framework for explaining

evolutionary changes in brain size. Journal of Human Evolution 57: 392-400.

Iwano T. 1991. An ecological and behavioral study of the aye-aye (Daubentonia

madagascariensis). African Study Monographs 12: 19-42.

Iwano T and C Iwakawa. 1988. Feeding behaviour of the aye-aye (Daubentonia

madagascariensis) on nuts of ramy (Canarium madagascariensis). Folia

Primatologica 50: 136-142.

350

Jabin M, D Mohr, H Kappes and W Topp. 2004. Influence of deadwood on density of

soil macro-Arthropoda in a managed oak-beech forest. Forest Ecology and

Management 194: 61-69.

Janmaat KRL, SD Ban and C Boesch. 2013. Chimpanzees use long-term spatial memory

to monitor large fruit trees and remember feeding experiences across seasons.

Animal Behaviour 86: 1183-1205.

Janson CH. 1998. Experimental evidence for spatial memory in foraging wild capuchin

monkeys, Cebus paella. Aminal Behaviour 44: 1229-1243.

Janson CH and CA Chapman. 1999. Resources and primate community structure. In:

Primate Communities. Fleagle JG, CH Janson and KE Reed, eds. Pp:237-267.

New York: Cambridge University Press.

Janson CH and CP van Schaik. 1988. Recognizing the many faces of primate food

competition: Methods. Behaviour 105: 165-186.

Janson CH and CP van Schaik. 1993. Ecological risk aversion in juvenile primates: Slow

and steady wins the race. In: Juvenile Primates. Pereira M and L Fairbanks, eds.

Pp: 57-76. New York: Oxford University Press.

Johns AD and JP Skorupa. 1987. Responses of rain-forest primates to habitat disturbance:

A review. International Journal of Primatology 8: 157-191.

Johnson DH. 1980. The comparison of usage and availability measurements for

evaluating resource preference. Ecology 61: 65-71.

351

Johnson SE. 2003. Life history and the competitive environment: Trajectories of growth,

maturation, and reproductive output among chacma baboons. American Journal

of Physical Anthropology 120: 83-98.

Johnson SE and J Bock. 2004. Trade-offs in skill acquisition and time allocation among

juvenile chacma baboons. Human Nature 15: 45-62.

Jones CB. 2006. Flexibility in Primatology: Causes and Consequences. New York:

Springer Science and Business Media, Inc.

Jouffroy FK. 1975. Osteology and mycologists of the lemuriform post cranial skeleton.

In: Lemur Biology. Tattersall I and RW Sussman, eds. Pp: 149-192. New York:

Plenum Press.

Jouffroy FK, M Godinot and Y Nakano. 1991. Biometric always characteristics of

primate hands. Human Evolution 6: 269-306.

Jungers WL. 1978. The functional significance of skeletal allometry in Megaladapis in

comparison to living prosimians. American Journal of Physical Anthropology 49:

303-314.

Jungers WL. 1984. Aspects of size and scaling in primate biology with special reference

to the locomotor skeleton. American Journal of Physical Anthropology 27: 73-97.

Kappeler PM. 1998. Nests, tree holes and the evolution of primate life histories.

American Journal of Primatology 46: 7-33.

Kappeler PM, ME Pereira and CP van Schaik. 2003. Primate life histories and

socioecology. In: Primate Life Histories and Socioecology. Kappeler PM and CE

Pereira, eds. University of Chicago Press: Chicago Pp: 1-20.

352

Kane EE. 2012. The context of dietary variation in Cercopithecus diana in the Ivory

Coast’s Tai National Park [thesis]. Columbus, OH: The Ohio State University.

Kaufman JA, ET Ahrens, DH Laidlaw, S Zhang and JM Allman. 2005. Anatomical

analysis of an aye-aye brain (Daubentonia madagascariensis, Primates: Prosimii)

combining histology, magnetic resonance imaging, and diffusion tensor imaging.

The Anatomical Record Part A 287A: 1026-1037.

Kay RF. 1975. The functional adaptations of primate molar teeth. American Journal of

Physical Anthropology 43: 195-216.

Kay RF and HH Covert. 1984. Anatomy and behaviour of extinct primates. In: Food

Acquisition and Processing in Primates. Chivers DJ, BA Wood and A

Bilsborough, eds. Pp: 467-508. Boston: Springer.

Kay RF, RW Sussman and I Tattersall. 1978. Dietary and dental variations in the genus

Lemur, with comments concerning dietary-dental correlations among Malagasy

primates. American Journal of Physical Anthropology 49: 119-128.

Kay RNB, P Hoppe and GMO Maloiy. 1976. Fermentation digestion of food in the

colobus monkey, Colobus polykomos. Experientia 32: 485-487.

Kennedy GE. 2005. From the ape’s dilemma to the weanling’s dilemma: Early weaning

and its evolutionary context. Journal of Human Evolution 48: 123-145.

Kivell TL, D Schmitt and RE Wunderlich. 2010. Hand and foot pressures in the aye-aye

(Daubentonia madagascariensis) reveal novel biomechanical trade-offs required

for walking on gracile digits. The Journal of Experimental Biology 213: 1549-

1557.

353

Kinzey WG and MA Norconk. 1990. Hardness as a basis of fruit choice in two sympatric

primates. American Journal of Physical Anthropology 81: 5-15.

Kinzey WG, AL Rosenberger, PS Heisler, DL Prowse and JS Trilling. 1977. A

preliminary field investigation of the yellow handed titi monkey, Callicebus

torquatus torquatus, in northern Peru. Primates 18: 159-181.

Kleiman DG. 1979. Parent-offspring conflict and sibling competition in a monogamous

primate. The American Naturalist 114: 753-760.

Klingenberg CP and J Spence. 1997. On the role of body size for life-history evolution.

Ecological Entomology 22: 55-68.

Klopfer PH and KJ Boskoff. 1979. Maternal behavior in prosimians. In: The Study of

Prosimian Behavior. Doyle GA, ed. Academic Press: New York. Pp: 123-156.

Knott CD. 1998. Changes in orangutan caloric intake, energy balance, and ketones in

response to fluctuating fruit availability. International Journal of Primatology 19:

1061-1079.

Krakauer E, P Lemelin and D Schmitt. 2002. Hand and body position during locomotor

behavior in the aye-aye (Daubentonia madagascariensis). American Journal of

Primatology 57: 105-118.

Lahann P. 2008. Habitat utilization of three sympatric Cheirogaleid lemur species in a

littoral rain forest of southeastern Madagascar. International Journal of

Primatology 29: 117-134.

354

Lambert JE. 2007. Seasonality, fallback strategies and natural selection: A chimpanzee

and Cercopithecoid model for interpreting the evolution of Hominin diet. In:

Evolution of the Human Diet: The Known, the Unknown, and the Unknowable.

Ungar PS, ed. Pp: 324-343. New York: Oxford University Press, Inc.

Lambert JE, CA Chapman, RW Wrangham and NL Conklin-Brittain. 2004. Hardness of

Cercopithecines foods: Implications for the critical function of enamel thickness

in exploiting fallback foods. American Journal of Physical Anthropology 125:

363-368.

Latchat T, R Peveling, S Attignon, G Goergen, B Sinsin and P Nagel. 2007. Saproxylic

battle assemblages on native and exotic snags in a West African tropical forest.

African Entomology 15: 13-24.

Lee PC. 1987. Nutrition, fertility and maternal investment in primates. Journal of

Zoology, London 213: 409-422.

Leigh SR. 1994. Ontogenetic correlates of diet in anthropoid primates. American Journal

of Physical Anthropology 94: 499-522.

Leigh SR. 2004. Brain growth, life history, and cognition in primate and human

evolution. American Journal of Primatology 62: 139-164.

Leigh SR and GE Blomquist. 2007. Life history. In: Primates in Perspective. Campbell

CJ, A Fuentes, KC MacKinnon, M Panger and SK Bearder, eds. Pp: 396-407.

New York: Oxford University Press, Inc.

355

Lhota S, T June and L Bartos. 2009. Patterns and laterality of hand use in free-ranging

aye-aye (Daubentonia madagascariensis) and a comparison with captive studies.

Journal of Ethology 27: 419-428.

Lindenmayer DB. 1998. The design of wildlife corridors in wood production forests.

NSW National Parks and Wildlife Service: Sydney.

Lindstedt SL and WA Calder III. 1981. Body size, physiological time, and longevity of

homeothermic mammals. Quarterly Review of Biology 56: 1-16.

MacArthur RH. 1972. Geographical Ecology: Patterns in the Distribution of Species.

Princeton: Princeton University Press.

MacArthur RH and ER Pianka. 1966. On optimal use of a patchy environment. The

American Naturalist 100: 603-609.

Marshall AJ and RW Wrangham. 2007. Evolutionary consequences of fallback foods.

International Journal of Primatology 28: 1219-1235.

Marshall AJ, CM Boyko, KL Feilen, RH Boykott and M Leighton. 2009. Defining

fallback foods and assessing their importance in primate ecology and evolution.

American Journal of Physical Anthropology 140: 603-614.

Martin RD. 1990. Primate Origins and Evolution: A Phylogenetic Reconstruction.

Princeton: Princeton University Press.

McGraw WS. 1996. Cercopithecid locomotion, support use, and support availability in

the Tai Forest, Ivory Coast. American Journal of Physical Anthropology 100:

507-522.

356

McGraw WS. 1998a. Comparative locomotion and habitat use of six monkeys in the Tai

Forest, Ivory Coast. American Journal of Physical Anthropology 105: 493-510.

McGraw WS. 1998b. Posture and support use of Old World Monkeys (Cercopithecidae):

The influence of foraging strategies, activity patterns, and the spatial distribution

of preferred food items. American Journal of Primatology 46: 229-250.

McGraw WS and DJ Daegling. 2012. Primate feeding and foraging: Integrating studies of

behavior and morphology. Annual Review of Anthropology 41: 203-219.

McGraw WS, JD Pampush and DJ Daegling. 2012. Brief communication: Enamel

thickness and durophagy in mangabeys revisited. American Journal of Physical

Anthropology 147: 326-333.

McGraw WS, AE Vick and DJ Daegling. 2014. Dietary variation and food hardness in

sooty mangabeys (Cercocebus atys): Implications for fallback foods and dental

adaptation. American Journal of Physical Anthropology 154: 413-423.

McNab BK. 1963. Bioenergetics and determination of home range size. The American

Naturalist 97: 133-140.

Mendel F. 1976. Postural and locomotor behavior of Alouatta palliate on various

substrates. Folia Primatologica 26: 36-53.

Millikan GW, JP Ward and CJ Erickson. 1991. Independent digit control in foraging by

the aye-aye (Daubentonia madagascariensis). Folia Primatologica 56: 219-224.

Milton K. 1981. Food choice and digestive strategies of two sympatric primate species.

The American Naturalist 117: 496-505.

357

Milton K and ML May. 1976. Body weight, diet and home range area in primates.

Nature 259: 459-462.

Mitani JC and D Watts. 1997. The evolution of non-maternal caretaking among

anthropoid primates: Do helpers help? Behavioral Ecology and Sociobiology 40:

213-220.

Mitani M. 1989. Cercocebus torquatus: Adaptive feeding and ranging behaviors related

to seasonal fluctuations of food resources in the tropical rain forest of south-

western Cameroon. Primates 30: 307-323.

Mittermeier RA. 1978. Locomotion and posture in Ateles geoffroyi and Ateles paniscus.

Folia Primatologica 30: 161-193.

Mittermeier RA, F Hawkins, S Rajaobelina and O Langrand. 2005. Wilderness

conservation in a biodiversity hotspot. International Journal of Wilderness 11:

42-45.

Moffett MW. 2000. What’s ‘up’? A critical look at the basic terms of canopy biology.

Biotropica 32: 569-596.

Mohr CO. 1947. Table of equivalent populations of North American small mammals.

The American Midland Naturalist 37: 223-249.

Morbeck ME. 1977. Positional behavior, selective use of habitat substrate and associated

non-positional behavior in free-ranging Colobus guereza. Primates 18: 35-58.

Morland HS. 1990. Parental behavior and infant development in ruffed lemurs (Varecia

variegata) in a northeast Madagascar rainforest. American Journal of Primatology

20: 253-265.

358

Mousseau TA and DA Roff. 1987. Natural selection and the heritability of fitness

components. Heredity 59: 181-197.

Müller AE. 1999. Social organization of the fat-tailed dwarf lemur (Cheirogaleus

medius) in northwestern Madagascar. In: New Directions in Lemur Studies.

Rakotosamimanana B, H Rasamimanana, JU Ganzhorn and SM Goodman, eds.

Pp: 139-157. Boston: Springer.

Myneni RB, W Yan, RR Nemani, AR Huete, RE Dickinson, Y Knyazikhin, K Didan, R

Fu, RI Negron Juarez, SS Saatchi, H Hashimoto, K Ichii, NV Shabanov, B Tan, P

Ratana, JL Privette, JT Morisette, EF Vermonter, DP Roy, RE Wolfe, MA Friedl,

SW Running, P Votava, N El-Saleous, S Devadiga, Y Su and VV Salomonson.

2007. Large seasonal swings in leaf area of Amazon rain forests. Proceedings of

the National Academy of Sciences 104: 4820-4823.

Napier JR. 1962. Monkeys and their habitats. New Scientist 295: 88-92.

Napier JR. 1967. Evolutionary aspects of primate locomotion. American Journal of

Physical Anthropology 27: 333-342.

Napier JR and Napier PH. 1967. A Handbook of Living Primates. New York: Academic

Press.

Napier JR and AC Walker. 1967. Vertical clinging and leaping- A newly recognized

category of locomotor behaviour of primates. Folia Primatologica 6: 204-219.

Norscia I, V Carrai and SM Borgognini-Tarli. 2006. Influence of dry season and food

quality and quantity on behavior and feeding strategy of Propithecus verreauxi in

Kirindy, Madagascar. International Journal of Primatology 27: 1001-1022.

359

Oates JF. 1977. The Guereza and its food. In: Primate Ecology: Studies of Feeding and

Ranging Behaviour in Lemurs, Monkeys and Apes. Clutton-Brock TH, ed.

Associated Press: New York. Pp:275-321.

Oates JF. 1987. Food distribution and foraging behavior. In: Primate Societies. Smuts

BB, DL Cheney, RM Seyfarth, RW Wrangham and TT Struhsaker, eds. Pp: 197-

209. Chicago: University of Chicago Press.

Oates JF, T Swain and J Zantovska. 1977. Secondary compounds and food selection by

colobus monkeys. Biochemical Systematics and Ecology 5: 317-321.

Ohwaki, RE Hungate, L Lotter, RR Hofmann and G Maloiy. 1974. Stomach fermentation

in East African colobus monkeys in their natural state. Applied Microbiology 27:

713-723.

Olupot W, CA Chapman, PM Waser and G Isabirye-Basuta. 1997. Mangabey

(Cercocebus albigena) ranging patterns in relation to fruit availability and the risk

of parasite infection in Kibale National Park, Uganda. American Journal of

Primatology 43: 65-78.

Overdorff DJ. 1993. Similarities, differences, and seasonal patterns in the diets of

Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park,

Madagascar. International Journal of Primatology 14: 721-753.

Overdorff DJ, SG Strait and A Telo. 1997. Seasonal variation in activity and diet in a

small-bodied folivorous primate, Hapalemur griseus, in Southeastern

Madagascar. American Journal of Primatology 43: 211-223.

360

Owen R. 1863. Monograph on the aye-aye (Chiromys madagascariensis, Cuvier).

London: Taylor and Francis.

Oxnard CE. 1981. The uniqueness of Daubentonia. American Journal of Physical

Anthropology 54: 1-21.

Oxnard CE, RH Compton and SS Lieberman. 1990. Animal Lifestyles and Anatomies:

The Case of the Prosimian Primates. Seattle: University of Washington Press.

Oxnard CE, R German FK Jouffroy and J Lessertisseur. 1981. A morphometric study of

limb proportions in leaping prosimians. American Journal of Physical

Anthropology 54: 421-430.

Parker ST. 2015. Re-evaluating the extractive foraging hypothesis. New Ideas in

Psychology 37: 1-12.

Parker ST and KR Gibson. 1977. Object manipulation, tool use, and sensorimotor

intelligence as feeding adaptations in cebus monkeys and great apes. Journal of

Human Evolution 6: 623-641.

Parker ST and KR Gibson. 1979. A developmental model for the evolution of language

and intelligence in early hominids. Behavioral and Brain Sciences 2: 367-408.

Partridge L and PH Harvey. 1988. The ecological context of life history evolution.

Science 241: 1449-1455.

Peck D. 2004. Madagascar designates its third Ramsar site. Lemur News 9: 3.

Pereira ME and LA Fairbanks. 2002. What are juvenile primates all about? In: Juvenile

Primates: Life History, Development, and Behavior. Pereira ME and LA

Fairbanks, eds. Pp: 3-12. Chicago: University of Chicago Press.

361

Pereira ME, A Klepper, and EL Simons. 1987. Tactics for care of young infants by forest

living ruffed lemurs (Varecia variegata variegata): Ground nests, parking and

biparental guarding. American Journal of Primatology 13: 129-144.

Petter JJ. 1962. Recherches sur l’écologie et l’éthologie des lémuriens malagache.

Mémoires de Museum National d’Histoire Natural 27: 1-46.

Petter JJ. 1965. The lemurs of Madagascar. In: Primate Behavior: Field Studies of

Monkeys and Apes. DeVore I, ed. Pp: 292-319. New York: Holt, Rinehart and

Winston.

Petter JJ. 1977. The aye-aye. In: Primate Conservation. Rainier P III and GH Bourne, eds.

Pp: 37-57. New York: Academic Press.

Plavcan JM, RF Kay, WL Jungers and CP van Schaik. 2002. Reconstructing Behavior in

the Primate Fossil Record. Boston: Springer.

Pollock JI. 1975. Field observations on Indri indri: A preliminary report. In: Lemur

Biology. Tattersall I and RW Sussman, eds. Plenum Press: New York. Pp: 287-

311.

Pollock JI. 1977. The ecology and sociology of feeding in Indri indri. In: Primate

Ecology: Studies of Feeding and Ranging Behaviour in Lemurs, Monkeys and

Apes. Clutton-Brock TH, ed. Pp: 37-69. New York: Academic Press, Inc.

Porter LM, PA Garber and E Nacimento. 2009. Exudates as a fallback food for Callimico

goeldii. American Journal of Primatology 71: 120-129.

362

Powzyk JA and CB Mowry. 2003. Dietary and feeding differences between sympatric

Propithecus diadema diadema and Indri indri. International Journal of

Primatology 24: 1143-1162.

Prost JH. 1965. A definitional system for the classification of primate locomotion.

American Anthropologist 67: 1198-1214.

Pusey AE. 1980. Inbreeding avoidance in chimpanzees. Animal Behaviour 28: 543-552.

Pyke GH. 1984. Optimal foraging theory: A critical review. Annual Review of Ecology

and Systematics 15: 523-575.

Rainio J. 2009. Carabid beetles (Coleoptera, Carabidae) as indicators of environmental

change in Ranomafana National Park, Madagascar [dissertation]. Helsinki,

Finland: University of Helsinki.

Ramsier MA, AJ Cunningham, GL Moritz, JJ Finneran, CV Williams, PS Ong, SL

Gursky-Doyen and NJ Dominy. 2012. Primate communication in the pure

ultrasound. Biology Letters 8: 508-511.

Randimbiharinirina DR, TM Sefczek, BM Raharivololona, YR Andriamalala, J

Ratsimbazafy and EE Louis, Jr. 2017. Aye-aye (Daubentonia madagascariensis).

In: Primates in Peril: The World’s 25 Most Endangered Primates 2016-2018.

Schwitzer C, RA Mittermeier, AB Rylands, F Chiozza, EA Williamson, EJ

MacFie, J Wallis and A Cotton, eds. Pp: 44-46. IUCN SSC Primate Specialist

Group (PSG), International Primatological Society (IPS), Conservation

International (CI), and Bristol Zoological Society, Arlington.

363

Randimbiharinirina DR, BM Raharivololona, MTR Hawkins, CL Frasier, R Culligan,

TM Sefczek, R Randriamampionona and EE Louis, Jr. 2018. Behavior and

ecology of male aye-ayes (Daubentonia madagascariensis) in the Kianjavato

classified forest, southeastern Madagascar. Folia Primatologica 89: 123-137.

Read AF and PH Harvey. 1989. Life history differences among the eutherian radiations.

Journal of Zoology 219: 329-353.

Reader SM, Y Hager and KN Laland. 2011. The evolution of primate general and

cultural intelligence. Philosophical Transactions of the Royal Society B 366:

1017-1027.

Reynolds V, AJ Plumptre, J Greenham and J Harborne. 1998. Condensed tannins and

sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo

Forest, Uganda. Oecologia 115: 331-336.

Richard A. 1977. The feeding behaviour of Propithecus verreauxi. In: Primate Ecology:

Studies of Feeding and Ranging Behaviour in Lemurs, Monkeys and Apes.

Clutton-Brock TH, ed. Pp: 72-96. New York: Academic Press, Inc.

Ripley S. 1967. The leaping of langurs: A problem in the study of locomotor adaptation.

American Journal of Physical Anthropology 26: 149-170.

Robinson BW and DS Wilson. 1998. Optimal foraging, specialization, and a solution to

Liem’s paradox. The American Naturalist 151: 223-235.

Rode KD, CA Chapman, LR McDowell and C Stickler. 2006. Nutritional correlates of

population density across habitats and logging intensities in redtail monkeys

(Cercopithecus ascanius). Biotropica 38: 625-634.

364

Rodgers AR, JG Kie, D Wright, HL Beyer and AP Carr. 2015. HRT: Home Range Tools

for ArcGIS. Version 2.0. Ontario Ministry of Natural Resources and Forestry,

Center for Northern Forest Ecosystem Research, Thunder Bay, Ontario, Canada.

Rose MD. 1973. Quadrupedalism in Primates. Primates 14: 337-357.

Rosenberg AL. 1992. Evolution of feeding niches in New World monkeys. American

Journal of Physical Anthropology 88: 525-562.

Rosenberg AL. 2013. Fallback foods, preferred foods, adaptive zones, and primate

origins. American Journal of Primatology 75: 883-890.

Ross C. 1996. Adaptive explanation for the origins of the Anthropoidea (Primates).

American Journal of Primatology 40: 205-230.

Ross C. 1998. Primate life histories. Evolutionary Anthropology 6: 54-63.

Ross C. 2001. Park or ride? Evolution of infant carrying in primates. International

Journal of Primatology 22:749-771.

Ross C. 2003. Life history, infant care strategies, and brain size in primates. In: Primate

Life Histories and Socioecology. Kappeler PM and ME Pereira, eds. University of

Chicago Press, Chicago. Pp: 266-284.

Rotundo M, E Fernandez-Duque and AF Dixson. 2005. Infant development and parental

care in free-ranging Aotus azarai azarai in Argentina. International Journal of

Primatology 26: 1459-1473.

Rushton SP, SJ Ormerod and G Kerby. 2004. New paradigms for modelling species

distributions? Journal of Applied Ecology 41: 193-200.

365

Sauther ML. 1998. Interplay of phenology and reproduction in ring-tailed lemurs:

Implications for ring-tailed lemur conservation. Folia Primatologica 69: 309-320.

Sauther ML and FP Cuozzo. 2009. The impact of fallback foods on wild ring-tailed lemur

biology: A comparison of intact and anthropogenically distributed habitats.

American Journal of Physical Anthropology 140: 671-686.

Sawyer RM, ZSE Fenosoa, A Andrianarimisa and G Donati. 2017. The effect of habitat

disturbance on the abundance of nocturnal lemur species on the Masoala

Peninsula, northeastern Madagascar. Primates 58: 187-197.

Sayers K, MA Norconk and NL Conklin-Brittain. 2010. Optimal foraging on the roof of

the world: Himalayan langurs and the classical prey model. American Journal of

Physical Anthropology 141: 337-357.

Schmid J and PM Kappeler. 2005. Physiological adaptations to seasonality in nocturnal

primates. In: Seasonality in Primates: Studies of Living and Extinct Human and

Non-human Primates. Brockton DK and CP van Schaik, eds. Pp: 129-156.

Cambridge: Cambridge University Press.

Schmidt M. 2010. Locomotion and postural behaviour. Advances in Science and

Research. 5: 23-39.

Schneider JE. 2004. Energy balance and reproduction. Physiology and Behavior 81: 289-

317.

Schoener TW. 1971. Theory of feeding strategies. Annual Review of Ecology and

Systematics 2: 369-404.

366

Schradin C and G Anzenberger. 2001. Costs of infant carrying in common marmosets,

Callithrix jacchus: An experimental analysis. Animal Behavior 62: 289-295.

Schuppli C, K Isler and CP van Schaik. 2012. How to explain the unusually late age at

skill competence among humans. Journal of Human Evolution 63: 843-850.

Schwitzer C, RA Mittermeier, AB Rylands, F Chiozza, EA Williamson, EJ MacFie, J

Wallis and A Cotton. 2017. Primates in Peril: The World’s 25 Most Endangered

Primates 2016-2018. IUCN SSC Primate Specialist Group (PSG), International

Primatological Society (IPS), Conservation International (CI), and Bristol

Zoological Society, Arlington.

Shaffer CA. 2014. Spatial foraging in free ranging bearded sakis: Traveling salesmen or

Lévy walker? American Journal of Primatology 76: 472-484.

Shyamsundar P and R Kramer. 1997. Biodiversity conservation: At what cost? A study

of households in the vicinity of Madagascar’s Mantadia National Park. Ambio 26:

180-184.

Sefczek TM, ZJ Farris and PC Wright. 2012. Aye-aye (Daubentonia madagascariensis)

feeding strategies at Ranomafana National Park, Madagascar: An indirect

sampling method. Folia Primatologica 83: 1-10.

Sefczek TM, D Randimbiharinirina, BM Raharivololona, JD Rabekianja and EE Louis,

Jr. 2017. Comparing the use of live trees and deadwood for larval foraging by

aye-ayes (Daubentonia madagascariensis) at Kianjavato and Torotorofotsy,

Madagascar. Primates 58: 535-546.

367

Sefczek TM, J Rakotomanana, H Randriamaronirina and EE Louis, Jr. 2018.

Unsuccessful predation event of an aye-aye (Daubentonia madagascariensis) by a

fosa (Cyptoprocta ferox). Lemur News 21: 8-10.

Simons EL. 1993. Discovery of the western aye-aye. Lemur News 1: 6.

Simons EL. 1995. History, anatomy, subfossil record and management of Daubentonia

madagascariensis. In: Creatures of the Dark: The Nocturnal Prosimians.

Alderman L, GA Doyle and MK Izard, eds. Pp: 133-140. New York: Plenum

Press.

Singleton I and CP van Schaik. 2001. Orangutan home range size and its determinants in

a Sumatran swamp forest. International Journal of Primatology 22: 877-911.

Soligo C. 2005. Anatomy of the hand and arm in Daubentonia madagascariensis: A

functional and phylogenetic outlook. Folia Primatologica 76: 262-300.

Stark DJ, IP Vaughan, DA Ramirez Saldivar, SKSS Nathan, and B Goossens. 2017.

Evaluating methods for estimating home ranges using GPS collars: A comparison

using proboscis monkeys (Nasalis larvatus). PLoS ONE 12: e0174891.

https://doi.org/10.1371/journal.pone.0174891

Stephan H, H Frahm and G Baron. 1981. New and revised data on volumes of brain

structures in insectivores and primates. Folia Primatologica 35: 1-29.

Stephens DW and JR Krebs (eds). 1986. Foraging Theory. Princeton: Princeton

University Press.

Stephens DW, JF Lynch, AE Sorensen and C Gordon. 1987. Preference and profitability:

Theory and experiment. The American Naturalist 127: 533-553.

368

Streak EHM, DP Watts and CP van Schaik. 1997. The evolution of female social

relationships in nonhuman primates. Behavioral Ecology and Sociobiology 41:

291-309.

Sterling EJ. 1993. Behavioral ecology of the aye-aye (Daubentonia madagascariensis) on

Nosy Mangabe, Madagascar [dissertation]. New Haven, CT: Yale University.

Sterling EJ. 1994a. Aye-ayes: Specialists on structurally defended resources. Folia

Primatologica 62: 142-154.

Sterling EJ. 1994b. Taxonomy and distribution of Daubentonia: A historical perspective.

Folia Primatologica 62: 8-13.

Sterling EJ and EM McCreless. 2006. Adaptations in the aye-aye: A review. In: Lemurs:

Ecology and Adaptation. Gould L and ML Sauther, eds. Pp: 159-184. New York:

Springer Science and Business Media, Inc.

Sterling EJ and AF Richard. 1995. Social organization in the aye-aye (Daubentonia

madagascariensis) and the perceived distinctiveness of nocturnal primates. In:

Creatures of the Dark. Alterman L, GA Doyle and MK Izard, eds. Pp: 439-451.

Boston: Springer.

Sterns SC. 1992. The Evolution of Life Histories. Oxford: Oxford University Press.

Stone AI. 2007. Responses of squirrel monkeys to seasonal changes in food availability

in an eastern Amazonian forest. American Journal of Primatology 69: 142-157.

Sussman RW. 1987. Species-specific dietary patterns in primate and human dietary

adaptations. In: Evolution of Human Behavior: Primate Models. Kinzey WG, ed.

Pp: 151-179. Albany: State University of New York Press.

369

Sussman RW. 1991. Primate origins and the evolution of angiosperms. American Journal

of Primatology 23: 209-223.

Sutherland WJ. 1998. The importance of behavioural studies in conservation biology.

Animal Behaviour 56: 801-809.

Swihart RK and NA Slade. 1985a. Testing for independence of observations in animal

movements. Ecology 66: 1176-1184.

Swihart RK and NA Slade. 1985b. Influence of sampling interval on estimates of home-

range size. The Journal of Wildlife Management 49: 1019-1025.

Swihart RK and NA Slade. 1997. On testing for independence of animal movements.

Journal of Agricultural, Biological, and Environmental Statistics 2:48-63.

Tecot SR, AL Baden, NK Romine and JM Kamilar. 2012. Infant parking and nesting, not

allomaternal care, influence Malagasy primate life histories. Behavioral Ecology

and Sociobiology 66: 1375-1386.

Tecot SR, AL Baden, N Romine, and JM Kamilar. 2013. Reproductive strategies and

infant care in the Malagasy primates. In: Building Babies: Primate Development

in Proximate and Ultimate Perspective. Clancy KBH, ed. Pp: 321-359. New York:

Springer.

Temerin LA and JGH Cant. 1983. The evolutionary divergence of old world monkeys

and apes. The American Naturalist 122: 335-351.

Tepedino VJ and NL Stanton. 1982. Estimating floral resources and flower visitors in

studies of pollinator-plant communities. Oikos 38: 384-386.

370

Tilden CD and OT Oftedal. 1997. Milk composition reflects pattern of material care in

prosimian primates. American Journal of Primatology 41: 195-211.

Tombak KJ, AJ Reid, CA Chapman, JM Rothman, CA Johnson and R Reyna-Hurtado.

2012. Patch depletion behavior differs between sympatric folivorous primates.

Primates 53: 57-64.

Tomlinson PB and MH Zimmermann. 1978. Tropical Trees as Living Systems. P: 679.

Cambridge: Cambridge University Press.

Tuttle RH. 1967. Knuckle-walking and the evolution of hominoid hands. American

Journal of Physical Anthropology 26: 171-206.

Valero A and RW Byrne. 2007. Spider monkey ranging patterns in Mexican subtropical

forest: Do travel routes reflect planning? Animal Cognition 10: 305-315. van Noordwijk MA and CP van Schaik. 2005. Development of ecological competence in

Sumatran orangutans. American Journal of Physical Anthropology 127: 79-94. van Schaik CP and K Isler. 2012. Life-history evolution in primates. In: The Evolution of

Primate Societies. Mitani JC, J Call, PM Kappeler, RA Palombit, and JB Silk,

eds. Pp: 220-224. Chicago: University of Chicago Press. van Schaik CP and KR Pfannes. 2005. Tropical climates and phenology: A primate

perspective. In: Seasonality in Primates: Studies of Living and Extinct Human and

Non-human Primates. Brockton K and CP van Schaik, eds. Pp: 24-54.

Cambridge: Cambridge University Press.

371 van Schaik CP, JW Terborgh and SJ Wright. 1993. The phenology of tropical forests:

Adaptive significance and consequences for primary consumers. Annual Review

of Ecology and Systematic 24: 353-377. van Schaik CP, MA van Noordwijk and CL Nunn. 1999. Sex and social evolution in

primates. In: Comparative Primate Socioecology. Lee PC, ed. Pp: 204-240.

Cambridge: Cambridge University Press.

Vasey N. 2005. Activity budgets and activity rhythms in red ruffed lemurs (Varecia

rubra) on the Masoala Peninsula, Madagascar: Seasonality and reproductive

energetics. American Journal of Primatology 27: 1535-1550.

Vogel ER, JT van Woerden, PW Lucas, SSU Atmoko, CP van Schaik and NJ Dominy.

2008. Functional ecology and evolution of hominoid molar enamel thickness: Pan

troglodytes schweinfurthii and Pongo pygmaeus wurmbii. Journal of Human

Evolution 55: 60-74.

Volampeno MSN, JC Masters and CT Downs. 2011. Life history traits, maternal

behavior and infant development of blue-eyed black lemurs (Eulemur flavifrons).

American Journal of Primatology 73: 474-484.

Walker A. 1974. Locomotor adaptations in past and present prosimian primates. In:

Primate Locomotion. Jenkins Jr. FA, ed. Pp: 349-381. New York: Academic

Press.

White GC and RA Garrott. 1990. Analysis of wildlife radio-tracking data. San Diego:

Academic Press.

372

Wich SA, RW Shumaker, L Perkins and H de Vries. 2009. Captive and wild orangutan

(Pongo sp.) survivorship: A comparison and the influence of management.

American Journal of Primatology 71: 680-686.

Winn RM. 1994. Preliminary study of the sexual behaviour of three aye-ayes

(Daubentonia madagascariensis) in captivity. Folia Primatologica 62: 63-73.

Worton BJ. 1989. Kernel methods for estimating the utilization distribution in home-

range studies. Ecology 70: 164-168.

Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour

75: 262-300.

Wright PC. 1999. Lemur traits and Madagascar ecology: Coping with an island

environment. Yearbook of Physical Anthropology 42: 31-72.

Wright PC. 2006. Considering climate change effects in lemur ecology and conservation.

In: Lemurs: Ecology and Adaptation. Gould L and ML Sauther, eds. Pp: 385-401.

New York: Springer Science and Business Media, Inc.

Wright PC, BR Andriamihaja and SA Raharimiandra. 2005. Tanaka synecological

relations with lemurs in Southeastern Madagascar. In: Commensalism and

Conflict: The Human-Primate Interface. Paterson JD and J Wallis, eds. Pp: 119-

145. Norman, OK: American Society of Primatologists.

373

Wright PC, SE Johnson, MT Irwin, R Jacobs, P Schlichting, S Lehman, EE Louis JR, SJ

Arrigo-Nelson, JL Raharison, RR Rafalirarison, V Razafindratsita, J

Ratsimbazafy, FJ Ratelolahy, R Dolch and C Tan. 2008. The crisis of the

critically endangered greater bamboo lemur (Prolemur simus). Primate

Conservation 23: 5-17.

Wunderlick RE, RR Lawler and AE Williams. 2011. Field and experimental approaches

to the study of locomotor ontogeny in Propithecus verreauxi. In: Primate

Locomotion: Linking Field and Laboratory Research. D’Aout K and EE

Vereecke, eds. Pp: 135-154 New York: Springer.

374

Appendix A. Daily and seasonal count of consumed Canarium seeds, invertebrates, Vakona resource, and water from Ravenala by Tsinjo between January 2016 and December 2017 at Torotorofotsy, Madagascar. Continued table.

Month Season Canarium seeds Invertebrates Vakona Ravenala Jan-16 S1 2016 0 7 0 0 Jan-16 S1 2016 75 15 0 0 Jan-16 S1 2016 0 24 0 0 Jan-16 S1 2016 143 6 0 0 Jan-16 S1 2016 82 26 0 0 Feb-16 S1 2016 0 15 0 0 Feb-16 S1 2016 90 2 0 0 Feb-16 S1 2016 80 0 0 0 Feb-16 S1 2016 0 7 0 6 Mar-16 S1 2016 133 2 0 0 Mar-16 S1 2016 32 19 0 0 Mar-16 S1 2016 0 29 0 0 Mar-16 S1 2016 41 0 0 0 Mar-16 S1 2016 0 3 0 0 Mar-16 S1 2016 0 5 0 0 Mar-16 S1 2016 61 11 0 0 Mar-16 S1 2016 0 8 0 0 Apr-16 S1 2016 101 16 0 0 Apr-16 S1 2016 0 11 0 0 Apr-16 S1 2016 52 0 0 0 Apr-16 S1 2016 60 0 0 0 Apr-16 S1 2016 78 1 0 0 Apr-16 S1 2016 0 31 0 0 May-16 S1 2016 0 14 0 0 May-16 S2 2016 84 23 0 0 May-16 S2 2016 0 3 0 0

Continued

375

Appendix A Continued

Month Season Canarium seeds Invertebrates Vakona Ravenala Jun-16 S2 2016 0 39 0 0 Jun-16 S2 2016 0 8 0 0 Jun-16 S2 2016 0 25 0 0 Jul-16 S2 2016 0 3 0 0 Jul-16 S2 2016 0 15 0 0 Jul-16 S2 2016 0 56 0 0 Jul-16 S2 2016 0 14 0 0 Jul-16 S2 2016 0 8 0 0 Jul-16 S2 2016 0 13 0 0 Aug-16 S2 2016 0 17 0 0 Aug-16 S2 2016 0 5 0 0 Aug-16 S2 2016 0 10 0 0 Aug-16 S2 2016 0 3 0 0 Aug-16 S2 2016 0 6 0 0 Aug-16 S2 2016 0 7 0 0 Sep-16 S2 2016 0 24 0 0 Sep-16 S2 2016 0 9 0 0 Sep-16 S3 2016 0 70 0 0 Sep-16 S3 2016 0 13 0 0 Sep-16 S3 2016 0 28 0 0 Sep-16 S3 2016 0 25 0 0 Oct-16 S3 2016 0 71 0 0 Oct-16 S3 2016 0 110 0 0 Oct-16 S3 2016 0 15 0 0 Oct-16 S3 2016 0 5 0 0 Oct-16 S3 2016 0 90 0 0 Oct-16 S3 2016 0 58 0 0 Oct-16 S3 2016 0 35 0 0 Oct-16 S3 2016 0 25 0 0 Nov-16 S3 2016 0 116 0 0 Nov-16 S3 2016 0 41 0 0

Continued 376

Appendix A Continued

Month Season Canarium seeds Invertebrates Vakona Ravenala Nov-16 S3 2016 0 58 0 0 Nov-16 S3 2016 0 45 0 0 Nov-16 S3 2016 0 59 0 0 Dec-16 S3 2016 0 16 0 0 Dec-16 S3 2016 0 35 0 0 Dec-16 S3 2016 0 14 0 0 Dec-16 S3 2016 0 10 0 0 Dec-16 S3 2016 0 60 0 0 Dec-16 S3 2016 0 14 0 0 Dec-16 S3 2016 0 12 0 0 Jan-17 S1 2017 0 27 0 0 Jan-17 S1 2017 0 15 0 0 Jan-17 S1 2017 0 10 0 0 Feb-17 S1 2017 122 0 0 0 Feb-17 S1 2017 90 0 0 0 Feb-17 S1 2017 112 0 0 0 Feb-17 S1 2017 57 19 0 0 Feb-17 S1 2017 0 32 0 0 Feb-17 S1 2017 19 10 0 0 Mar-17 S1 2017 47 8 0 0 Mar-17 S1 2017 39 7 0 0 Mar-17 S1 2017 148 9 0 0 Mar-17 S1 2017 75 16 0 0 Mar-17 S1 2017 0 33 0 0 Mar-17 S1 2017 0 2 0 0 Mar-17 S1 2017 0 14 0 0 Apr-17 S1 2017 85 5 0 0 Apr-17 S1 2017 99 14 0 0 Apr-17 S1 2017 0 1 0 0 May-17 S1 2017 0 11 0 0 May-17 S1 2017 111 30 0 0

Continued 377

Appendix A Continued

Month Season Canarium seeds Invertebrates Vakona Ravenala May-17 S1 2017 0 17 0 0 May-17 S1 2017 18 18 0 0 May-17 S1 2017 0 58 0 0 May-17 S2 2017 0 22 1 0 May-17 S2 2017 0 17 9 0 May-17 S2 2017 0 35 4 0 May-17 S2 2017 0 57 0 0 May-17 S2 2017 0 12 0 0 May-17 S2 2017 0 16 0 0 May-17 S2 2017 0 54 0 0 May-17 S2 2017 0 35 0 0 Jun-17 S2 2017 0 68 0 0 Jun-17 S2 2017 60 15 0 0 Jun-17 S2 2017 0 21 0 0 Jun-17 S2 2017 0 7 0 0 Jul-17 S2 2017 0 29 0 0 Jul-17 S2 2017 0 10 0 0 Jul-17 S2 2017 0 7 0 0 Jul-17 S2 2017 0 15 0 0 Jul-17 S2 2017 0 14 0 0 Jul-17 S2 2017 0 18 0 0 Jul-17 S2 2017 0 51 0 0 Aug-17 S2 2017 0 24 0 0 Aug-17 S2 2017 0 42 0 0 Aug-17 S2 2017 0 27 0 0 Aug-17 S2 2017 0 21 0 0 Aug-17 S2 2017 0 6 0 0 Aug-17 S2 2017 0 51 0 0 Aug-17 S2 2017 0 9 0 0 Sep-17 S3 2017 0 4 0 0

Continued

378

Appendix A Continued

Month Season Canarium seeds Invertebrates Vakona Ravenala Sep-17 S3 2017 0 46 0 0 Sep-17 S3 2017 0 10 0 0 Sep-17 S3 2017 0 2 0 0 Sep-17 S3 2017 0 14 0 0 Sep-17 S3 2017 0 19 0 0 Sep-17 S3 2017 0 12 0 0 Oct-17 S3 2017 0 77 0 0 Oct-17 S3 2017 0 22 0 0 Oct-17 S3 2017 0 28 0 0 Oct-17 S3 2017 0 3 0 0 Oct-17 S3 2017 0 10 0 0 Oct-17 S3 2017 0 17 0 0 Oct-17 S3 2017 0 23 0 0 Oct-17 S3 2017 0 28 0 0 Nov-17 S3 2017 0 24 0 0 Nov-17 S3 2017 0 20 0 0 Nov-17 S3 2017 0 23 0 0 Nov-17 S3 2017 0 19 0 0 Nov-17 S3 2017 0 4 0 0 Nov-17 S3 2017 0 27 0 0 Dec-17 S3 2017 0 26 0 0 Dec-17 S3 2017 0 7 0 0 Dec-17 S3 2017 0 31 0 0 Dec-17 S3 2017 0 88 0 0 Dec-17 S3 2017 0 19 0 0 Dec-17 S3 2017 0 7 0 0

379

Appendix B. Daily and seasonal count of live tree, deadwood and bamboo substrates used by Tsinjo for invertebrate foraging between January 2016 and December 2017 at Torotorofotsy, Madagascar. Continued table.

Month Season Live Tree Deadwood Bamboo Jan-16 S1 2016 7 0 0 Jan-16 S1 2016 15 0 0 Jan-16 S1 2016 21 3 0 Jan-16 S1 2016 6 0 0 Jan-16 S1 2016 17 9 0 Feb-16 S1 2016 6 0 9 Feb-16 S1 2016 2 0 0 Feb-16 S1 2016 0 0 0 Feb-16 S1 2016 3 4 0 Mar-16 S1 2016 1 1 0 Mar-16 S1 2016 12 7 0 Mar-16 S1 2016 17 12 0 Mar-16 S1 2016 0 0 0 Mar-16 S1 2016 0 3 0 Mar-16 S1 2016 3 2 0 Mar-16 S1 2016 9 2 0 Mar-16 S1 2016 8 0 0 Apr-16 S1 2016 13 3 0 Apr-16 S1 2016 11 0 0 Apr-16 S1 2016 0 0 0 Apr-16 S1 2016 0 0 0 Apr-16 S1 2016 1 0 0 Apr-16 S1 2016 17 14 0 May-16 S1 2016 11 3 0 May-16 S2 2016 3 20 0 May-16 S2 2016 1 2 0

Continued

380

Appendix B Continued

Month Season Live Tree Deadwood Bamboo Jun-16 S2 2016 12 27 0 Jun-16 S2 2016 8 0 0 Jun-16 S2 2016 25 0 0 Jul-16 S2 2016 3 0 0 Jul-16 S2 2016 15 0 0 Jul-16 S2 2016 13 43 0 Jul-16 S2 2016 11 3 0 Jul-16 S2 2016 8 0 0 Jul-16 S2 2016 10 3 0 Aug-16 S2 2016 17 0 0 Aug-16 S2 2016 4 1 0 Aug-16 S2 2016 10 0 0 Aug-16 S2 2016 3 0 0 Aug-16 S2 2016 6 0 0 Aug-16 S2 2016 7 0 0 Sep-16 S2 2016 5 19 0 Sep-16 S2 2016 9 0 0 Sep-16 S3 2016 2 68 0 Sep-16 S3 2016 8 5 0 Sep-16 S3 2016 10 18 0 Sep-16 S3 2016 0 25 0 Oct-16 S3 2016 49 22 0 Oct-16 S3 2016 1 109 0 Oct-16 S3 2016 2 10 3 Oct-16 S3 2016 5 0 0 Oct-16 S3 2016 18 2 70 Oct-16 S3 2016 9 14 35 Oct-16 S3 2016 6 9 20 Oct-16 S3 2016 22 0 3 Nov-16 S3 2016 0 116 0 Nov-16 S3 2016 0 34 7

Continued 381

Appendix B Continued

Month Season Live Tree Deadwood Bamboo Nov-16 S3 2016 40 18 0 Nov-16 S3 2016 20 25 0 Nov-16 S3 2016 12 47 0 Dec-16 S3 2016 0 16 0 Dec-16 S3 2016 11 18 6 Dec-16 S3 2016 10 0 0 Dec-16 S3 2016 21 33 6 Dec-16 S3 2016 14 0 0 Dec-16 S3 2016 4 8 0 Jan-17 S1 2017 27 0 0 Jan-17 S1 2017 0 15 0 Jan-17 S1 2017 10 0 0 Feb-17 S1 2017 0 0 0 Feb-17 S1 2017 0 0 0 Feb-17 S1 2017 0 0 0 Feb-17 S1 2017 15 0 4 Feb-17 S1 2017 32 0 0 Feb-17 S1 2017 4 6 0 Mar-17 S1 2017 8 0 0 Mar-17 S1 2017 0 4 3 Mar-17 S1 2017 9 0 0 Mar-17 S1 2017 16 0 0 Mar-17 S1 2017 33 0 0 Mar-17 S1 2017 2 0 0 Mar-17 S1 2017 14 0 0 Apr-17 S1 2017 5 0 0 Apr-17 S1 2017 0 14 0 Apr-17 S1 2017 1 0 0 May-17 S1 2017 0 11 0 May-17 S1 2017 19 11 0 May-17 S1 2017 5 5 7

Continued 382

Appendix B Continued

Month Season Live Tree Deadwood Bamboo May-17 S1 2017 0 15 3 May-17 S1 2017 19 21 18 May-17 S2 2017 22 0 0 May-17 S2 2017 10 7 0 May-17 S2 2017 25 10 0 May-17 S2 2017 37 14 6 May-17 S2 2017 3 9 0 May-17 S2 2017 12 4 0 May-17 S2 2017 44 0 10 May-17 S2 2017 0 8 27 Jun-17 S2 2017 24 37 7 Jun-17 S2 2017 6 9 0 Jun-17 S2 2017 9 4 8 Jun-17 S2 2017 0 7 0 Jul-17 S2 2017 27 0 2 Jul-17 S2 2017 10 0 0 Jul-17 S2 2017 7 0 0 Jul-17 S2 2017 10 5 0 Jul-17 S2 2017 14 0 0 Jul-17 S2 2017 18 0 0 Jul-17 S2 2017 38 13 0 Aug-17 S2 2017 17 7 0 Aug-17 S2 2017 14 19 9 Aug-17 S2 2017 7 6 4 Aug-17 S2 2017 19 0 2 Aug-17 S2 2017 4 2 0 Aug-17 S2 2017 38 13 0 Aug-17 S2 2017 9 0 0 Sep-17 S3 2017 0 4 0 Sep-17 S3 2017 20 7 19

Continued

383

Appendix B Continued

Month Season Live Tree Deadwood Bamboo Sep-17 S3 2017 1 8 1 Sep-17 S3 2017 2 0 0 Sep-17 S3 2017 2 12 0 Sep-17 S3 2017 16 3 0 Sep-17 S3 2017 12 0 0 Oct-17 S3 2017 77 0 0 Oct-17 S3 2017 0 22 0 Oct-17 S3 2017 15 13 0 Oct-17 S3 2017 3 0 0 Oct-17 S3 2017 4 6 0 Oct-17 S3 2017 14 3 0 Oct-17 S3 2017 0 23 0 Oct-17 S3 2017 28 0 0 Nov-17 S3 2017 24 0 0 Nov-17 S3 2017 11 9 0 Nov-17 S3 2017 6 17 0 Nov-17 S3 2017 8 11 0 Nov-17 S3 2017 4 0 0 Nov-17 S3 2017 12 15 0 Dec-17 S3 2017 26 0 0 Dec-17 S3 2017 7 0 0 Dec-17 S3 2017 31 0 0 Dec-17 S3 2017 16 23 49 Dec-17 S3 2017 1 18 0 Dec-17 S3 2017 7 0 0

384