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Ecology of Lemur catta at the Tsimanampetsotsa National Park, Madagascar: Implications for female dominance and the evolution of lemur traits


Abstract and Figures

Lemurs are an ancient, extant primate radiation and have a number of traits (e.g. female dominance, low basal metabolic rate, weaning synchrony, cathemerality) which are unusual when compared to other primates, or even other mammals. The Energy Conservation Hypothesis (ECH) posits that the lemur traits are part of an adaptive complex selected to enable lemurs to conserve and extract energy from their seasonally and stochastically resource-poor environments. Data were collected on two groups of ring-tailed lemurs in the dry spiny forests of the Tsimanampetsotsa National Park, Madagascar, and tested aspects of the ECH through the following hypotheses: 1) ring-tailed lemur foods are seasonally and stochastically limited, 2) ring-tailed lemur nutrients and/or calories are seasonally and stochasically limited, 3) ring-tailed lemurs use behavioral mechanisms to save energy, and 4) the dry season is differentially stressful for female ring-tailed lemurs. Results from these data suggest that ring-tailed lemur plant foods, nutrients, and calories are seasonally and stochastically limited. Males appear to use behavioral strategies to conserve energy and females appear differentially stressed by the harsh conditions of the dry season. This study also documented extensive cathemeral activity in the ring-tailed lemurs, which may function to increase food intake, and limit thermoregulatory stress during hot days and cool nights. The aforementioned results are consistent with ECH, indicating that the lemur traits are an adaptive response to the environmental pressures of Madagascar. Furthermore, since dominance facilitates a feeding advantage for female lemurs, this trait likely allows for costly mammalian reproduction during times of predictable resource scarcity.
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B.Sc., University of Victoria, 2004
M.Sc., University of Victoria, 2008
A thesis submitted to the Faculty of the Graduate School of the presented to the
University of Colorado Boulder in partial fulfillment
of the requirements for the degree of
Doctor of Philosophy
Department of Anthropology
This thesis is entitled:
Ecology of ring-tailed lemurs (Lemur catta) at the Tsimanampetsotsa National Park,
Madagascar: Implications for female dominance and the evolution of lemur traits
written by Marni LaFleur
has been approved for the Department of Anthropology
Michelle Sauther, committee chair
Herbert Covert, committee member
Frank Cuozzo, committee member
Matt Sponheimer, committee member
Dennis, Van Gerven
The final copy of this thesis has been examined by the signatories, and we
find that both the content and the form meet acceptable presentation standards
of scholarly work in the above mentioned discipline
ACU protocol # 1002.09
LaFleur, Marni (Ph.D., Anthropology)
Ecology of ring-tailed lemurs (Lemur catta) at the Tsimanampetsotsa National Park,
Madagascar: Implications for female dominance and the evolution of lemur traits
Thesis directed by Associate Professor Michelle L. Sauther
Lemurs are an ancient, extant primate radiation and have a number of traits (e.g. female
dominance, low basal metabolic rate, weaning synchrony, cathemerality) which are unusual
when compared to other primates, or even other mammals. The Energy Conservation Hypothesis
(ECH) posits that the lemur traits are part of an adaptive complex selected to enable lemurs to
conserve and extract energy from their seasonally and stochastically resource-poor
environments. Data were collected on two groups of ring-tailed lemurs in the dry spiny forests of
the Tsimanampetsotsa National Park, Madagascar, and tested aspects of the ECH through the
following hypotheses: 1) ring-tailed lemur foods are seasonally and stochastically limited, 2)
ring-tailed lemur nutrients and/or calories are seasonally and stochasically limited, 3) ring-tailed
lemurs use behavioral mechanisms to save energy, and 4) the dry season is differentially stressful
for female ring-tailed lemurs. Results from these data suggest that ring-tailed lemur plant foods,
nutrients, and calories are seasonally and stochastically limited. Males appear to use behavioral
strategies to conserve energy and females appear differentially stressed by the harsh conditions
of the dry season. This study also documented extensive cathemeral activity in the ring-tailed
lemurs, which may function to increase food intake, and limit thermoregulatory stress during hot
days and cool nights. The aforementioned results are consistent with ECH, indicating that the
lemur traits are an adaptive response to the environmental pressures of Madagascar.
Furthermore, since dominance facilitates a feeding advantage for female lemurs, this trait likely
allows for costly mammalian reproduction during times of predictable resource scarcity.
For Sid, the lemur that never really had a chance, but slipped through my fingers anyhow.
I am deeply sorry and will forever cherish your tooth comb garlic kisses.
This dissertation nearly killed me. Literally. A number of times. As a direct result of this
work, I endured the following: inappropriate sinus tachycardia; dengue fever and associated
delirium followed by seven months of "break bone" symptoms; malaria; mononucleosis; separate
episodes of calcium and magnesium deficiencies, both severe enough to be conducive with heart
failure; three fractured molars; heat upwards and beyond 50°C for months on end; several
unidentifiable intestinal parasites; a few bouts of food poisoning; countless frightening rashes
and inexplicable blisters; a handful of jagged limestone-induced scars; being stuck for the better
part of five days in nowhere Madagascar, in a vehicle short a transmission, in the middle of a
cyclone; and for lack of a better description, the plagues of mosquitoes, whose memory will
forever give me chills. That being said, I am fortunate to of had these opportunities and that I
lived to tell the stories, and am indebted to so many people who helped along way...
To my academic advisor:
Many thanks to Michelle Sauther. You are not only an outstanding and prolific scholar,
but an exceptional advisor, and you truly went above and beyond for me. Without your patience,
enthusiasm, mad editing skills, and dedication to my success, I would not be where I am today. I
am forever indebted for all of the time and energy you bestowed on me, and can only think to
repay this service through paying it forward.
To my academic committee:
Thank you to the "beloved" Dennis Van Gervan. I have learned so much from you and
am grateful to have been given free reign with the Nubian collection. Driving around 1000 year-
old dead people for x-rays really is a once (or twice) in a lifetime opportunity. Though you are an
extraordinary educator, I am most grateful for your friendship, kindness, and wisdom. I am
certain that I would not be where I am today without your advice, honesty, and sense of humor.
In your own words, "it's not dead babies and it's not cancer, so don't worry about it." True dat.
Thank you to Herbert Covert for challenging me to think critically, and letting me know
that it is ok to love dinosaurs, orangutans, and freezers full of dead things. I admire your
conservation work and hope to someday make a difference in primate conservation, as you do.
Thank you to Matt Sponheimer for taking the time to review my work and give insightful
feedback. You are likely the most intelligent person I have ever or will ever encounter, and in
addition to being a tiny bit frightened of your genius, I am truly honored to of had you as a
And many more thanks to Frank Cuozzo for your detailed reviews and insightful
suggestions, of much of my work, particularly pertaining to lemur prehistory. I am grateful for
your insight, knowledge, and time, though cannot forget what you did to Gary. Those were some
of the most frightening 3 minutes of my life.
And my unofficial mentors:
To Darna Dufour, for taking an interest in me, even through my "I'm not an
Anthropologist" academic coming-of-age phase. I am grateful for your ear, advise, and to know
that I am not the only one to have had field disasters. You survived a plane crash, for goodness
sake. I also admire your dedication to teaching and will keep many of the thing you taught me
through to the next phase in my career as an Anthropologist.
To Nayuta Yamashita (Instit für Population Genetik, Veterinary Medicine University
Vienna), for laughing with and at me, for always having candy in the field, AND for the human
skeleton. You are awesome! Oh, and for your advice and thoughtful review of my methods and
written work. Next time I get hit with a plague of mosquitoes, I will heed your advice, and head
for the beach. On an unrelated note, don't think for a second that I've forgotten about your
involvement in the Gary fiasco.
Thank you to Joerg Ganzhorn (Department of Zoology, University of Hamburg) for your
advice and generosity with reference to plant nutritional analyses, and also Irene Tomaschewski
for performing said analyses.
Also thanks to Jacky Youssouf (Département de Sciences Biologie, Université de
Toliara). Where to even begin. Jacky, you saved me from so many cestodes and literally
welcomed me into your home. I am so grateful for the cultural experiences you've awarded me
and your ability to laugh at anything. The dictator, the driver, the extortion. I am proud to be
your colleague and look forward to seeing you many times again.
And to Rokiman Letsara (Botanical and Zoological Park Tsimbazaza and the California
Academy of Science) thank you for your persistence at door 7, facilitation of this research and
your vast knowledge of the plants of Madagascar.
Thanks also to Chia Tan for inviting me into the San Diego Zoo Global world, and
encouraging and helping me start my academic career.
And all others:
Thank you to the government of Madagascar, Madagascar National Parks and the
University of Toliara, Madagascar, for granting me permission to work at Tsimanampetsotsa
National Park.
And to those that accompanied me in the trenches: Meghan Hoopes, Bronwyn McNeil,
Lanto, and Bakira Ravorona. I still can't believe that you stuck with me through the tortures of
this expedition, and am so thankful for your companionship and ability to laugh. Additionally,
thank you to the Beza Mahafaly animal darting team (Enafa Efitroaromy, Edidy Ellis, and
Elahavelo) and the Tsimanampetsotsa National Park ecological monitoring team (Razanajafy
Olivier, Lauren, Stephan), and local experts Fiti and Francisco. Also thank you to the village of
Efotsy for welcoming me into your world and homes. And thank you to Jason Hale for you help
in getting me set up in Madagascar and for keeping me in contact with the outside world during
ridiculous emergencies. Thanks to Denise Gabriel, for your commiseration and friendship, both
in Madagascar and beyond. Marriage proposals wouldn't be nearly as fun without you.
Thanks to Lisa Gould for introducing me to lemurs, primatology, and deli. Your
dedication and love of these animals encouraged me to pursue my dream of being a
primatologist. And I love kugel.
Thanks to all my lemur peeps, in no particular order: Teague O'Mara, Stephanie
Meredith, Elizabeth Kelley, Brandie Littlefield, James Loudon, Jim Millette, Krista Fish, Andrea
Gemmill, Andy Fogel, Brian Gerber, Jennifer Prew, Megan Shrum, Nicholas Ellwanger, Emily
Mertz, and Paul Sandberg.
Thank you to my dear friend and colleagues, without whom my life would be much less
rich: Michaela Howells, Richard Bender, Morgan Seamont, Marnie Thomson, Rachel Flemming,
and Jordan Steininger, Michelle Graves, and Charlie Jordan.
Many thanks to my parents (Michael and Donna LaFleur), and grandparents (Fred and
Patricia LaFleur, Laurie Zona, Audrey and George Aspin), and extended family, for thinking the
world of me, and in turn, awarding me the strength to endure the challenges of this project.
Thank you to Sam, Kitty LaFleur, Stretch, Gary, Minnie (Jelly), Winnie (Fish), Coco,
Daisy, Baby, Lisa (aka Pig), Dude, Tiny, Trash, Issac, Newton, Kizzi, Jesse, Honey, Peppermint
Pattie, most of all Amy, and all the other animal companions that instilled and inspired me with
empathy, curiosity and wonder.
And thank you to "my" lemurs! You tolerated me, despite my being an overly annoying
bipedal omby. I am so privileged to of been privy to the soap opera that is your daily life. I will
always treasure and miss your company.
Finally, a special thank you to Ron Mombourquette for encouraging me to achieve
dreams I didn't even realize I had, waiting for me, and tolerating scary things in the freezer. For
being home team. I love you dearly and look forward to spending the duration of my days with
This Project was generously funded by: National Science and Engineering Research
Council of Canada (Post Graduate Scholarship 296264), National Science Foundation (Doctoral
Dissertation Research Improvement Grant 1028708), National Geographic Society (Committee
for Research and Exploration Grant 88011), American Society of Primatologists (Small Research
Grant), University of Colorado Boulder Graduate School (Beverly Sears Graduate Student
Grant), University of Colorado Boulder Museum of Natural History (Clark Scholarship Fund),
University of Colorado Boulder Department of Anthropology (Pre-dissertation research grant,
Quintana Award, Haskell-Houghtelin Scholarship Fund), National Aboriginal Achievement
Foundation (Post Secondary Bursary), Native American Resource Advisory Group and the
Denver Museum of Nature & Science's Department of Anthropology (American Indian or
Alaskan Native Scholarship Award), and the Ron Mombourquette Scholarship Fund.
Focal animal name, group, sex, and if female, if infant present.........................
Day and Night animal activity scores from scan sampling with percentage of
time spent engaging in each activity...................................................................
Day and night animal location scores from scan sampling with percentage of
time spent in each location.................................................................................
Chi-square, Cramer's V, and Contingency Coefficient C as percent of max
("C") values for between and within group variation in day and nighttime
active lemur behaviors (locomote, feed/forage, groom, other)...........................
Chi-square, Cramer's V, and Contingency Coefficient C as percent of max
("C") values for between and within group variation in day and nighttime
lemur locations....................................................................................................
Pearson's correlation between lemur nighttime activity levels and daytime
high temperature, nighttime high temperature, and moon illumination..............
Linear regression of lemur nighttime activity levels with daytime temperature
maximum, nighttime temperature maximum, and moon illumination.............
Pearson's correlation between lemur nighttime activity levels and daytime
activity budget categories (feed/forage, locomote, sit/stand/rest, other).............
Linear regression of lemur nighttime activity levels with daytime activity
budgets (feed/forage, locomote, sit/stand/rest)...................................................
Pearson's correlation between lemur daytime activity budgets (feed/forage,
locomote, sit/stand/rest)......................................................................................
Amount of rainfall at TNP between September 2010 and March 2011..............
Percentage of tree coverage on phenological transect lines during the study
Percentages of plant species and plant part that contributed 1% or more of the
total amount consumed by ring-tailed lemurs during each complete month of
the study period...................................................................................................
Activity budgets (average percentage of daytime observation) for lemurs
sexes, all animals across the dry and wet seasons, and lemur groups.................
Student's T-test for differences in the mean amount of time spent in each
activity category by female and male lemurs, all lemurs between the dry and
wet season, and the ILove and Vintany lemur groups........................................
Activity budgets (average percentage of daytime observation) by lemur sex in
both seasons.........................................................................................................
Student's T-test for differences in the mean amount of time spent in each
activity category by lemur females and males in the dry and wet seasons.........
Student's T-test for differences in the mean amount of time spent in each
activity category during the dry and wet season by female and male lemurs.....
ILove and Vintany groups average distance traveled per day (meters) and
number of adults in group during the dry and wet seasons, along with
maximum day distance (meters) and home range size (km2) throughout the
study period.........................................................................................................
Average daily intake by season, sex and group of macronutrient and non-
nutrient (g/day), protein to fiber ratio, and energy (kcal/day).............................
Statistical results from the Independent Student's T-test between sexes,
seasons, and group for the consumption of macronutrients (g/day), non-
nutrients (g/day), the protein to ADF ratio, and energy (kcal/day).....................
Average nutrients, non-nutrients, and calories consumed per day for female
and male ring-tailed lemurs during the dry and wet seasons..............................
Statistical results from the Independent Student's T-test between seasons, and
for female and male animals for the consumption of macronutrients (g/day),
non-nutrients (g/day), the protein to ADF ratio, and energy
Statistical results from the Independent Student's T-test between sexes in the
dry and wet seasons, for the consumption of macronutrients (g/day), non-
nutrients (g/day), the protein to ADF ratio, and energy (kcal/day).
Percentages of nutrients and non-nutrients in parts from the flowers of A.
Usage of fat stores during the dry season by adult ring-tailed lemurs................
Lemur strategies to maximize fitness in the energy poor environments of
Madagascar. As presented by Wright, 1999............................................................
Relative location of Tsimanampetsotsa National Park in Madagascar....................
Location of Tsimanampetsotsa in relation to the Beza Mahafaly Special Reserve,
Berenty Private Reserve, and Cap Sainte Marie, in southwestern Madagascar......
Map of Tsimanampetsotsa National Park with reference to the base living camp..
Examples of habitat zones at the Tsimanampetsotsa national park, including a)
zone 1 (near) and zone 2 (distant), b) zone 2, c) zone 3, and d) zone 4..................
The cliff face where the ILove group sleeps and one of the ILove group females
on a rocky outcrop of the cliff.................................................................................
The large Ficus tree where the Vintany group sleeps with western view of the
tree, with the tree's aerial roots extending into the sink hole and the eastern view
showing the tree's breadth (~22m)...........................................................................
Vintany group drinking sites, including male descending Ficus megapoda aerial
roots, and group members drinking (nervously) in the sink hole below their
sleeping tree.............................................................................................................
ILove group drinking sites, including the group drinking in the Mitoho cave, and
group members entering the Mitoho cave...............................................................
Nighttime activity levels in the ILove and Vintany groups from September to
Male ring-tailed lemur in the momma baobab tree at 12:09am on March 20,
Camera trap photos taken near animals sleep sites. Clockwise from top left: IG
members during daylight at 6:02pm, IG mother and offspring during the night at
11:51pm, VG animal after dark at 8:50pm, and VG animals before daylight at
Average nighttime activity levels with nighttime temperature ...............................
Nighttime activity levels and regression lines with the following daytime
activities: a) Feed/forage, b) Locomote, c) Other, d) Sit/stand/rest.........................
Correlations and best fit lines within daytime activities, including: a) feed/forage
and locomote, b) feed/forage and other, c) feed/forage and sit/stand/rest, d)
locomote and other, e) locomote and sit/stand/rest, and f) other and sit/stand/rest.
Daytime "other" activities females and males in the dry and wet seasons..............
Remains of L. catta infant a) as encountered with dorsal surface untouched, b)
ventral surface after flipping carcass over, c) puncture wounds on side of torso....
Map of the trajectory of Cyclone Bingiza...............................................................
Availability of fruits, flowers, and young leaves during the study period...............
Photos taken of the same areas (angles vary somewhat) during the dry season
and wet season.........................................................................................................
Availability of T. indica and F. megapoda foods....................................................
Ficus megapoda fruits.............................................................................................
Percentage of plant food and part consumed each month (species contributing <
2% per month removed)..........................................................................................
Activity budgets (average percentage of observed time) of female ring-tailed
lemurs in the dry and wet seasons...........................................................................
Activity budgets (average percentage of observed time) of male ring-tailed
lemurs in the dry and wet seasons...........................................................................
Significant differences between time average feeding (average hours/day) for
female and male lemurs in the wet and dry seasons................................................
Aerial satellite map displaying the Vintany and ILove groups semi-overlapping
home ranges.............................................................................................................
Average amount of fiber (g/day)consumed by ILove and Vintany groups.............
Average number of calories (kcal/day) for lemur sexes in dry and wet seasons.....
Average intake of protein and ADF (g/day) for lemur sexes in the dry and wet
Average coat condition for females with and without infants, and males...............
Average coat condition of females with infants, 5Head, and males........................
Female ring-tailed lemur ("The Patient") and her offspring from the ILove group
on a) November 10, 2010, b) February 9, 2011, c) March 9, 2011, and d) April 2,
Male ring-tailed lemur ("Tumor") from the Vintany group on a/b) November 11,
2010, c) March 29, 2011, and d) April 6, 2011.......................................................
Baobab (A. rubrostipa) flower entire (above) and dissected (below) with flower
parts labeled: a) sepals, b) petals, c) stigma and style, d) anther filaments, and e)
anther tube................................................................................................................
Caterpillars that were consumed by lemurs and the D. floribunda trees, which
the caterpillars fed on.
Flowers from N. mahafaliensis, and A. comosa demonstrating the small size of
the flowers................................................................................................................
Dry season activity budgets for ring-tailed lemurs in different locations of spiny
Wet season activity budgets for ring-tailed lemurs at TNP and Cap Sainte Marie
spiny forest...............................................................................................................
Results and conclusions of previous research examining nutrition in lemurs.........
Ficus megapoda fruits in a) a portion of a heavily fruiting tree, b) a cluster of
unripe fruits from the tree and b) fruit and seed remains in feces of L. catta..........
Weaning synchrony as a strategy of lemur infants, along with adaptive strategies
of female and male ring-tailed lemurs.....................................................................
CHAPTER 1: Introduction to Lemur Traits and Primate Socioecology
This is the first study to document Lemur catta (ring-tailed lemurs) behavioral ecology in
an intact spiny forest habitat. The vast majority of our knowledge on L. catta comes from gallery
forest, where Tamarindus indica (tamarind) trees dominate the landscape. When they co-exist in
this way, T. indica is a fallback and commonly used resource for L. catta, and we thus have very
little information on ring-tailed lemurs in areas that are not dominated by tamarind trees. To date,
only three studies have examined L. catta outside of gallery forests; two were in highly
anthropogenically-degraded habitats, and the third was in the unusual high-altitude mountain
range ring-tailed lemur population of Andringitra. This study provides new comparative data,
and is of special interest in that it was collected on populations living within spiny forest habitat
which may be the original habitat for this species. Thus, studying ring-tailed lemurs in an intact
spiny forest offers the best possible opportunity to understand their adaptations, and
subsequently understand the flexibility of the species.
Data were collected on two groups of L. catta over a consecutive nine month period at
the Tsimanampetsotsa National Park (TNP), in southwestern Madagascar. This time period
encompassed the latter portion and peak of the long annual dry season and the following short
wet season. Additionally, during the study period Cyclone Bingiza occurred and resulted in
heavy rains and a flash flood at TNP. Throughout the study, behavioral data were collected
during the day and night. These data, along with camera trap photos, nutritional analyses of ring-
tailed lemur plant foods, and assessments of stress, were used to test aspects of the Energy
Conservation Hypothesis, including female dominance.
The extant lemurs of Madagascar represent a primate radiation dating to at least the Eocene
epoch (e.g. Yoder, 2004; Karanth et al., 2005). Within strepsirrhine primates (Lemuriformes and
Lorisiformes), the lemurs (including the recently extinct "giant" forms), show the greatest
variability in body size, activity patterns, feeding modes, locomotion styles, and social patterns
(Scheumann et al., 2007). Several lemur features are puzzling as they demonstrate a very
different adaptive pattern when compared to haplorrhine primates (van Schaik and Kappeler,
1996). For example, female dominance over males is extremely rare within mammalian social
systems (Ralls, 1976; Kappeler, 1993), but is the norm within the lemurid primates (Kappeler,
1991, 1993). Factors favoring the evolution of female dominance have yet to be fully identified
despite learned debate spanning more than two decades (see Pochron and Wright, 2005;
Dunham, 2008). Understanding female dominance in lemurs is of particular interest because,
unlike the few mammalian species showing female dominance, including hyenas (Crocuta
crocuta [Kruuk, 1972]) and mole rats (Heterocephalus spp. [Sherman et al., 1991]), lemur
females (with the exception of some mouse lemurs [e.g. Smith and Jungers, 1997]) do not have a
size advantage over males and thus dominance is maintained socially rather than physically. In
fact, uncovering the reasons for female dominance in lemurs has been deemed the “holy grail” of
lemur research (Pochron and Wright, 2005). The predominant explanation in the current
literature, the “Energy Conservation Hypothesis” (ECH), suggests that lemur female dominance
results from an adaptation that allows females feeding priority, which counteracts high
reproductive costs, along with seasonal and stochastic scarcity of food resources (Jolly, 1984;
Young et al., 1990; Wright, 1999; Pochron et al., 2003). The ECH is a viable hypothesis, but has
yet to be fully tested and may contain incorrect information regarding some so-called “lemur
As described, the ECH for female dominance in lemurs has four key assumptions. Namely, it
assumes that 1) lemur food resources are seasonally (and stochastically) limited, 2) a reduction in
food availability results in a reduction in nutrient or caloric intake for lemurs, and that this
reduction of nutrient or caloric intake is 3) stressful for all lemurs, but 4) particularly stressful for
female lemurs who have the increased metabolic demands of gestation and lactation. This project
examines the effects of season, sex and reproductive state on feeding behavior, nutrition, and
stress on ring-tailed lemurs, in order test the aforementioned assumptions of ECH.
Lemur catta is an ideal species for testing the ECH as males and females are monomorphic in
body size (Kappeler, 1991), females have strict dominance over males in all feeding and social
situations (Jolly, 1966, 1984, 1998), and they have strict reproductive synchrony (Jolly, 1966).
Additionally, L. catta is a monotypic species that up until only about 2000 years ago had been
evolving for tens of millions of years within an environment free of humans and other major
mammalian groups (Burney, 1987; Martin, 2000; Roos et al., 2004; Yoder and Yang, 2004).
These traits render ring-tailed lemurs an ideal species for making direct comparisons between
individuals, and understanding differences between sexes (see Gould, 2006). Moreover, TNP is
an excellent site for testing the ECH because not only is it a good example of dry spiny habitat to
which L. catta is proposed to be adapted (Goodman et al., 2006), it is also a large intact forest
parcel, with few anthropogenic effects or invasive plant foods (Sussman et al., 2003). Gould
(2006) noted that these conditions are optimal for understanding evolution and adaptation in L.
Most of our knowledge of ring-tailed lemurs and how they differ in response to
environmental variability, comes from the Beza Mahafaly Special Reserve or the Berenty Private
Reserve, which are both highly fragmented and patchily degraded forest habitats, that are
dominated by tamarind trees (See Gould et al., 1999; Sauther et al., 1999; Jolly et al., 2002;
Cuozzo and Sauther, 2006; Koyama et al., 2006). As such, we know very little about ring-tailed
lemur ecology outside gallery forest habitats (Gould, 2006). Though it is unclear when tamarind
trees were introduced to Madagascar (Sauther and Cuozzo, 2009), when present, tamarind trees
have a huge impact on ring-tailed lemur feeding ecology (Sauther, 1998; Yamashita, 2002;
Simmen et al., 2006; Sauther and Cuozzo, 2009). In fact, L. catta in gallery forests spend 35-
60% of their time feeding on tamarind fruits and leaves (Mertl-Milhollen et al., 2003), and
Yamashita (2002, 2008) suggested that in gallery forests all other foods should be considered
secondary to tamarind. Only two studies have observed L. catta in spiny environments, which
are not dominated by tamarind trees, but in both cases the habitats were highly fragmented and
affected by anthropogenic disturbance (Gould et al., 2011; Kelly, 2011). Additionally, although
the ecology of L. catta has been briefly examined within the high-altitude populations of
Andringitra (Goodman et al., 2006), the habitat of Andringitra is very different than what we
believe ring-tailed lemurs are adapted to, and presents an entirely different suite of challenges to
the ring-tailed lemurs residing there. Studying ring-tailed lemurs within a near pristine spiny
forest habitat not dominated by tamarind trees provides insight into their ecology and behavior in
their “natural” environment, meaning the habitat in which ring-tailed lemurs likely evolved and
were living in up until human-induced alterations greatly changed much of Madagascar’s
landscape (Goodman et al., 2006).
Rationale for Research
Unusual “lemur traits” include female dominance, targeted female-female aggression, lack of
sexual dimorphism, sperm competition coupled with male-male aggression, high infant
mortality, cathemerality, and strict seasonal breeding (Wright, 1999; Figure 1.0), and
understanding the causal mechanisms of such traits has driven the research of many
primatologists. Van Schaik and Kappeler (1996) noted distinct differences between gregarious
lemurs and haplorrhine primates in several social, demographic, morphological and ecological
features. Both ECH (Wright, 1999) and the evolutionary disequilibrium hypothesis (EDH) (van
Schaik and Kappeler, 1996) have been presented to account for lemur traits. EDH argues that all
extant lemur species were nocturnal and monogamous until the arrival of humans on Madagascar
approximately 2000 years ago. Moreover, EDH states that the ensuing rapid ecological changes
and extinctions of Madagascar's megafauna (both giant lemurs and large-bodied predatory
raptors) reduced interspecific competition and predation pressure for surviving smaller-bodied
lemurs, which opened up niches that modern diurnal lemurs are now exploiting. Characteristics
such as monomorphism and female dominance are not seen as adaptations to current
environments, but rather to ecological pressures present before the onset of the Holocene. For the
purposes of this manuscript, all mention of the EDH will refer the hypothesis as specifically
defined and proposed by van Schaik and Kappeler (1996) to account for the unusual traits found
in lemurs.
Figure 1.0. Lemur strategies to maximize fitness in the energy poor environments of
Madagascar. As presented by Wright, 1999.
There are several lines of evidence which suggest that lemurs are not in the type of
evolutionary disequilibrium described by van Schaik and Kappeler (1996). The following three
points outline the current evidence contrary to van Schaik and Kappeler's EDH.
First, EDH says that predator pressure is reduced for diurnal lemurs, because of the recent
extinction of the large-bodied diurnal birds of prey (Stephanoaetus maheryi). However, extant
endemic predators such as the harrier hawk (Polyboroides radiatus) are a real threat to diurnal
lemurs, as they are subject to significant predation events that rival those of nocturnal lemurs
(Wright et al., 1997; Karpanty, 2006; Brockman et al., 2008). Also, ring-tailed lemurs at the
Beza Mahafaly Special Reserve are frequent prey victims of a number of species, including wild
cats (e.g. Brockman et al., 2008; Sauther et al., 2011), and some evidence suggests that predation
may be occurring both day and night, given the recovery of fresh lemur remains, and eye witness
accounts, at various times during the day (Sauther et al., 2011). Furthermore, since there was also
a giant fossa (Cryptoprocta spelea) until about 2000 years ago, which was a large as 20kg
(Goodman et al., 2004), by van Schaik and Kappeler's reasoning, we should expect that lemurs
experience reduced predation pressure by modern fossa, which is simply not the case (Hawkins,
2003; Karpanty, 2003, 2006). It is more parsimonious to assume that the extinction of giant
lemurs and their giant predators were coupled, and lemurs today are subject to predation by their
extant predators, as we know they are.
Second, EDH predicts that cathemeral lemurs would have visual anatomy similar to that
of nocturnal lemurs, given that they would have only recently diverged from their fully nocturnal
lifestyle. Nocturnal species tend to have features that enhance visual sensitivity, such as
increased size and curvature of cornea and lens, well-developed tapetum lucidum (a reflective
layer which increases light available to receptors), and an increase in the proportion of rods to
cones (Detwiler 1939, 1940, 1941; Walls, 1942; Prince, 1956; Duke-Elder, 1958; Tansley,
1965). By comparison, diurnal species typically have anatomical eye specializations that increase
acuity, and may include area centralis (an area with a high density of receptors which increase
acuity), reduction in the size and curvature of the cornea and lens, decreased retinal summation,
and an increase in the proportion of cones to rods (Detwiler, 1939, 1940, 1941; Walls, 1942;
Prince, 1956; Duke-Elder, 1958; Tansley, 1965). However, cathemeral lemurs have visual
anatomy specializations, which differ from those of diurnal or nocturnal primates (Kirk, 2006).
Moreover, eye morphology in cathemeral Eulemur are very similar to that found in other non-
primate cathemeral mammals (Kirk, 2006). That is, cathemeral animals tend to have eye
adaptations that are almost half-way between that of diurnal and nocturnal animals, such as
poorly developed tapetum lucidum and area centralis, intermediate size and roundness of the
cornea and lens, and intermediate proportion of rods compared to cones (Kirk, 2006). These
unique cathemeral lemur eye specializations along with the convergence of traits with other
cathemeral animals suggest this visual anatomy is adaptive (Kirk, 2006). Kirk (2006) further
suggests that the common ancestor of Eulemur was characterized by cathemerality, during the
time period of 8-12MYA. Additionally, using phylogenetic analyses, Griffin et al. (2012)
suggested that Eulemur share a cathemeral common ancestor 9MYA, and that the common
ancestor of strepsirrhines was nocturnal. None of the aforementioned data is compatible with van
Schaik and Kappeler's (1996) EDH.
Third, genetic analyses suggest a common ancestry of diurnal or cathemeral indriids and
lemurids from between 32 and 32MYA, which implies that modern cathemeral and diurnal
lemurs did not share a nocturnal common ancestor, and therefore ruling out the possibility of a
recent (2000 years before present) nocturnal common ancestor (Roos et al., 2004). Though the
culmination of these findings does not completely discount the possibility that some modern
lemurs are in a state of evolutionary disequilibrium, the current evidence provides no support and
indicates that this is not a promising direction for future research for understanding lemur traits.
Alternatively, ECH (Wright, 1999) does appear to be a promising direction in lemur
research for understanding unusual lemur traits. In fact, this hypothesis has become normalized
as the driving force in lemur adaptations though it has yet to be adequately scientifically tested
(Dunham, 2008). ECH posits that the majority of lemur traits are either adaptations to conserve
energy (e.g. low basal metabolic rate (BMR), torpor, sperm competition, small group size,
seasonal breeding) or to maximize the use of scarce resources (e.g. female dominance,
cathemerality, territoriality, fibrous diet, weaning synchrony) (Wright, 1999). Again, though
prevalent throughout the literature, some of these suggested lemur traits or adaptations may not
be truly representative of lemurs. For example, low basal metabolic rate is cited as an energy-
conserving trait of lemurs, and is prevalent throughout the literature (Richard and Nicol, 1987;
Young et al., 1990; Wright, 1999; Tilden, 2008). Daniels (1984) demonstrated that some three
individual Eulemur had BMRs just 28% of that predicted from the Kleiber relationship for same-
sized mammals. However, Kappeler (1996) showed that reduced BMR is a characteristic of the
strepsirrhine primates, rather than being uniquely lemur. In a recent review of BMR in primates,
Harcourt (2008) also showed (using data from Genoud [2002] and White and Seymour [2003])
that strepsirrhines indeed have lower BMR when compared to haplorrhine primates, but that
lemur BMRs are not significantly lower than that of other strepsirrhine primates. That being said,
low BMR may very well be an important trait in lemurs, however, the extent to which this trait is
a result of phylogenetic inertia is unknown. Though, from the current body of literature, you
would presume that the this trait had been extensively tested and studied.
Costs of reproduction for female lemurs are also unclear, despite being mentioned frequently
in the literature as though these costs are well understood. Some researchers argue that lemur
females have unusually high costs of reproduction (Jolly, 1984; Richard and Nicol, 1987; Young
et al., 1990), while others say that female lemurs invest less than expected into reproduction
(Wright, 1995; Tilden and Oftedal, 1997; Wright, 1999; Tilden, 2008). Young et al. (1990) posits
that female lemurs have a high rate of prenatal maternal investment (as measured by average
neonate weight gain per day gestation) when compared to other strepsirrhine primates. However,
Kappeler (1996) argued that postnatal growth rates, which represent the bulk of maternal
investment, do not differ among lemurs and lorises, and concluded that lemur females do not
invest significantly more energy in reproduction than other strepsirrhine primates. Wright (1995)
stated that lemur females may invest less in reproduction when compared to other primates, as
lemurs have low-quality milk and lower infant birth weights. However, subsequent research has
shown that milk quality is not universally low in lemurs, but rather, milk is more dilute in
primate mothers whose infants “ride” rather than “park” (Tilden and Oftedal, 1997; Tilden,
2008). Furthermore, while lemur neonates weigh an average of 9% of maternal body mass,
neonate weight in galagos is about 7% of maternal weight (Izard and Nash, 1988) and a mere 3%
in lorises (Zimmermann, 1988). These data suggest that low milk quality and low neonate body
weight are not idiosyncrasies of lemurs.
Wright (1995, 1999) also suggested that females invest little in their young because infant
mortality is inordinately high and further maternal investment would not result in increased
survivorship. As evidence, Wright (1999) cites infant mortality rates of 40-80% for L. catta and
notes that these are twice the infant mortality rates of studied monkey populations. However, the
L. catta mortality rates cited by Wright, which neared 80%, were in the reproductive season
following a 2-year massive drought in southern Madagascar, and that during this time mortality
rates were elevated throughout the entire population, not just within infants (Gould et al., 1999).
As would be expected, primate populations experiencing natural disasters show increased
mortality (Pavelka et al., 2007), so this is not a peculiarity of lemurs. What about the lower end
(i.e. 40%) Wright (1999) cited for lemur infant mortality? Semi-free-ranging ring-tailed lemurs
experience infant mortality rates of 28.6% (Parga and Lessnau, 2005), which is lower than their
wild counterpart, but is likely due to food provisioning and protection from predators. Infant
mortality rates for wild non-lemur strepsirrhine primates are largely lacking from the current
literature, however wild haplorrhine primates show the following infant mortality rates: Saimiri
oerstedi 50% (Boinski, 1987), Semnopithecus entellus 50% (Borries, 1997), Callithrix spp. >
50% (Ross et al., 2007), Gorilla beringei beringei 27% (Robbins et al., 2007). Given the data at
hand, it does not seem that lemur infant mortality rates are elevated per se, and thus increased
infant mortality should not be interpreted as a trait unique to lemurs. However, it is important to
consider the effects of frequent natural disasters on lemur evolution. In sum, no current evidence
sufficiently demonstrates that lemur females have unusually high or low costs of reproduction,
and thus low maternal investment, as currently measured, should not be interpreted as an energy-
conserving strategy of lemurs.
If natural disasters are more prevalent in Madagascar and these disasters affect both infant
and adult survivorship, selection is likely to shape traits that enable survival in unpredictable
environments. The ECH has not been adequately been tested and remains promising in our
understanding of lemur evolution. Understanding exactly how the environment shapes female
dominance in lemurs will provide a powerful framework for understanding whether and how
lemurs are adapted to conserve and extract energy.
Review of pertinent literature
The following review is primarily based on data and theories from the order Primates.
The majority of information specific to lemurs and ring-tailed lemurs will be addressed in
subsequent chapters.
Social Groups
Animal survival in a given habitat is dependent on their ability to find suitable and
sufficient food resources. Acquiring and processing resources requires time and thus the number
of animals in a group is limited by their ability to maintain nutritional requirement within a
reasonable time frame (Dunbar et al., 2009). Increased group size leads to increased feeding
competition between individuals (Wrangham, 1980; Terborgh and Janson, 1986), which at least
within primates, negatively affects fecundity (Dunbar, 1980, 1988; Hill et al., 2000). There is a
trade off, however, between increased feeding competition and avoiding predation, since chances
of any one animal being preyed upon decreases with larger group sizes (Hamilton, 1971). Hence,
large group size is indirectly limited by fecundity, yet social groupings are maintained through
the benefits of predator evasion (van Schaik, 1989; Hill and Lee, 1998).
The primate "ecological model" was proposed by Wrangham (1980), and later expanded
upon by van Schaik (1989), Isbell (1991) and Sterck et al. (1997). This model posits that female
gregariousness within primates creates feeding competition both within and between groups
(Crook and Gartlan, 1966; Terborgh and Jansen, 1986; Isbell, 1991), but as we would predict,
group living is beneficial to females through predation avoidance (van Schaik and van Hooff,
1983; Isbell, 1994; Boinski and Chapman, 1995) and possibly through infanticide prevention
(Sommer, 2000; van Schaik and Janson, 2000; but also see Bartlett et al., 1993; Sussman et al.,
1995). The types of feeding competition delineate the distribution of females, and in turn their
social relationships (Wrangham, 1980). Males, on the other hand, are primarily affected by
mating competition and the distribution of receptive females (Emlen and Oring, 1977;
Vehrencamp and Bradbury, 1978; Stephens and Crebs, 1986).
Food resources, as described by Wrangham (1980) are either large and clumped, and
therefore defendable, or small and dispersed, and thus not defendable. Primates with defendable
food resources, such as fruits, likely have larger group sizes, are female bonded, and the social
relationships are well defined (Wrangham, 1980). This is because females use cooperative
defenses to protect food resources, and social ranking to distribute them. Conversely, primates
with non-defendable foods, such as dispersed insects or certain leaves, likely have smaller group
sizes, do not have female cooperative relationships, are not female bonded, and have very
loosely defined social relationships (Wrangham, 1980). This is because foods cannot be
defended against other groups or individuals. Relatedness within groups facilitates female
bonding, and dictates male philopatry (Wrangham, 1980). Groups with female, and/or male and
female philopatry have low relatedness, which does not generally lend to strong female bonds
(Wrangham, 1980).
Predation is likely a major factor shaping morphology and behavior in primates (see
Alexander, 1974; Clutton-Brock and Harvey, 1977; Cheney and Wrangham, 1987; Boinski et al.,
2000; Miller, 2000), and as mentioned, in the formation of social groups (see Jarman, 1974;
Busse, 1977; Anderson, 1986, but see Stanford, 1998, 2002). However, the effect of predation
on primates is notoriously difficult to understand given the elusiveness of predators, the rarity or
potential randomness of attacks, and lack of empirical evidence (Isbell, 1994; Boinski and
Chapman, 1995; Janson, 1998; Treves, 1999, Boinski et al., 2000; Treves, 2000). Furthermore,
although mounting anecdotal data exists, contextual information surrounding predation events
are often missing. Information such as predator attack strategy, prey age, sex, and status, along
with microhabitat type, and behavior of victims or survivors have been noted as crucial in
advancing our knowledge of the effects of predation on primate evolution (Miller and Treves,
2006). Also, existing anecdotal evidence has been criticized because it sheds little light on prey
vulnerability, and because even those predation events that are actually witnessed could be
random with regards to the prey genotype and/or phenotype (Miller and Treves, 2006).
The most direct method to explore the impact of predation on primates is to study the
predators themselves, which reveals prey profiles for each predator (Janson, 1998). Then by
combining prey profiles with demographic data of both predator and prey, we can assess
predation rates (Karpanty, 2006). With predation rates, we can compare across individuals,
populations and species of primate, with the intention of understanding the degree to which
predation influences life history of the individual or shapes the phylogeny of a species (Hart,
2000). Though effective, it can be difficult to determine predation rates in primate populations,
as predators are elusive by nature and may alter their behavior in the presence of researchers. A
few studies have looked directly at primate predators, and have greatly improved our knowledge
on the topic. The majority of this small body of work has come from the nest observations of
predatory birds, radio tracking terrestrial predators, and collection and examination of bird
regurgitory pellets or mammalian predator scat. Mitani et al. (2001) collected prey remains from
under the nest of two pairs of crowned hawk-eagles (Stephanoaetus coronatus), along with
census data on prey species at Kibale National Park. They found that monkeys were the primary
prey of the eagle and that the eagles were preferentially selecting male redtail monkeys. Sanders
et al. (2003) had similar findings at Ngogo, within Kibale National Park, and note that primates
composed 81% of the crowned haw-eagles' diet. In addition to collecting prey remains, Karpanty
(2006) observed diurnal raptors (Polyboroides radiatus and Accipiter henstii) at Ranomafana
National Park in Madagascar. She found predation rates on lemurs to be significant, and
suggested that raptor predation may depress the intrinsic growth rates and carrying capacity of
some of the lemurs at the site. In their work, Zuberbuhler and Jenny (2002) radio tracked
leopards in order to understand leopard predation on primates in the Tai Forest. They also
examined leopard scat samples and found that monkeys constituted a large portion of the diet.
Interestingly, Zuberbuhler and Jenny (2002) found that leopard predation was positively
correlated to prey density, which suggests that leopards hunt according to abundance. Dollar
(2006) analyzed scat samples from fossa (Cryptoprocta ferox) and found that rather than being
“lemur specialists” (Wright et al., 1997), fossa are flexible foragers that include a number of non-
lemur prey in their diets. These few studies have vastly improved our knowledge on predation
rates within primate communities, and similar studies have been deemed a priority in future.
It is important to realize, however, that the majority of research looking at primates and
their predators has examined predation risk rather than rate. Predation risk aims to understand a
primate’s perception of the chance of being taken by a predator (Hill and Dunbar, 1998; Janson,
1998; Miller, 2002). As Hill and Dunbar (1998) noted, predation risk could also be seen as a
primate’s perception of the likelihood of encountering a predator. This perception is likely to
affect a primate anti-predator behavior, namely vigilance, which has been extensively discussed
elsewhere (see Hill and Dunbar, 1998). Additionally, perceptions of risk are likely to include
memory of past predation attempts and present ecological variables (e.g. canopy cover, refuge
availability, presence of neighboring primate groups, visibility, etc.), which can convolute our
understanding of both the proximate and ultimate factors of the effects of predation on primate
societies (Hill and Dunbar, 1998).
Recently, researchers examining primate anti-predator behavior have moved away from
studies of vigilance and focused on how predation risk influences foraging behavior. Optimally
finding food while avoiding becoming someone else’s food can be a difficult balance, as
behaviors that increase foraging may also increase the risk of being preyed upon (Janson, 2000).
For example, although increased inter-individual distance while foraging can increase food
consumption, it also increases chances of predation (Cords, 2002). “Predator sensitive foraging”
looks at the behaviors primates use when foraging, which minimize chances of predation.
Social and environmental factors are important influences in primate predator sensitive
foraging (Lima and Dill, 1990; Miller, 2002). Other than group size, further social factors
affecting predator sensitive foraging include group composition, cohesion, centrality, and rank.
Adult or sub-adult males often play a protective role in their groups, and therefore having more
or less males would likely increase or decrease group safety (Lima and Dill, 1990). Similarly,
physical locations of group members affect individual safety. Individuals with close neighbors
and whose physical location is near the center of the group are less likely to be targeted by
predators; however, foraging efficiency is negatively correlated with increasing neighbors and
centrality (Miller, 2002). Social rank influences on predator sensitive foraging are complicated
(Miller, 2002; Sterck, 2002). For example, in sexually dimorphic species, higher-ranked
individuals may be larger, and thus somewhat less vulnerable to predation, which allows them to
engage in riskier foraging behaviors. However, lower-ranked individuals may also engage in
risky foraging behaviors, which are motivated by restricted access to high-quality foods. Overall,
higher-ranked individuals have greater freedom regarding their foraging strategy, as they can
choose their location within the group (Miller, 2002).
The environment a primate lives in also influences predator sensitive foraging. Though
habitat type is determined, primates can choose on which substrate and at what time they forage
(Miller, 2002; Sauther, 2002). Predation risk is generally greater in open areas, since individuals
are exposed to both aerial and terrestrial predators (Sauther, 2002; Sterck, 2002). However, with
increased visibility, primates can also detect predators sooner, which may not be the case in
dense forest cover, where range of sight and sound are restricted (Garber and Bicca-Marques,
2002; Miller, 2002). Though more data on predator-prey interactions are needed to fully
understand the complex interactions, the type and hunting style of each predator likely influence
risk-factor in open versus closed habitats. Additionally, primates can alter the risk-factor
associated with behaviors perceived as risky, such as foraging in an open environment. Larger
group size or increased ability to detect predators may decrease predation risk. Or, increased risk
may be ignored if the reward is high (as in crop raiding) and/or individuals are particularly
nutrient depleted (Saj et al., 1999).
Given the necessary social and environmental factors, polyspecific associations may also
be employed in primate predator sensitive foraging (Miller, 2002). Primate species may forage in
groups with other primates, as in Saguinus (Garber and Bicca-Marques, 2002), or with ring-
tailed lemurs and Verreaux's sifaka (Sauther, 2002), or they may forage with non-primate
animals, such as the coupling of baboons and gazelles (Devore and Hall, 1965) or langurs and
deer (Newton, 1985). In cases where the species’ diets differ, costs of foraging in the larger
group are greatly off-set. Moreover, given that species’ can interpret each others’ alarm systems,
predator detection is likely significantly increased (Zuberbuhler, 2002).
The balance between finding food resources and avoiding predators is multifactorial and
dependent upon social and environmental factors, but also individual choices. If predation
accounts for a significant number of deaths in wild primates, we expect selection to favor traits
which minimize predation events in an individual’s life. Future work examining the
“synecological” relationships of primates and their predators that include predation rates,
predation risk, and experimental manipulation are likely to yield valuable information on the
proximate and ultimate affects of predation on primates (Colquhoun, 2006).
Feeding and Nutritional Ecology
Like activity pattern, adaptations to feeding may affect variables such as physiology,
morphology, ontogeny, and ecology on individual, population and community levels (e.g. Oates
et al., 1990; Fleagle et al., 1991; Ross, 1992; Leigh, 1994; Altmann, 1998; McGraw, 1998). In
fact, diet has been called the single most important parameter underlying behavioral and
ecological differences in primates (Oates, 1987; Fleagle, 1988).
Primates require the full suite of nutrients that are necessary for most mammals, which
include both macronutrients (carbohydrates, proteins, fats, water) and micronutrients (minerals
and vitamins) (Oftedal and Allen, 1996). With a few exceptions (Tarsius spp. [e.g. MacKinnon
and MacKinnon, 1980] and Loris spp. [e.g. Nekaris and Rasmussen, 2003]), wild primates derive
the majority of their nutritional and energetic requirements from plant parts including: fruits (ripe
and unripe), seeds (immature and mature), leaves (all development phases), petioles, corms,
rhizomes, bark, flowers, nectar, sap, and gum (Lambert, 2007). Plant foods contain both nutrients
(feedants) and non-nutritive components (antifeedants). Feedants are desired nutrients such as
protein and carbohydrates, while antifeedants are non-nutritious and may include components
that reduce quality (fiber), and/or interfere with digestion (e.g. secondary compounds, toxins)
(Wrangham et al., 1998). Primate food selection is thus influenced by both nutrients required for
survival, but also chemicals and compounds that may interfere with nutrient absorption or even
be poisonous (Wrangham et al., 1998).
Relative levels of feedants (e.g. protein) and antifeedants (e.g. fiber) are often used as a
measure of dietary quality (Waterman and Kool, 1994), often by way of the protein to acid
detergent fiber ratio (protein:ADF). Protein is an integral part of the primate diet because it
provides the nitrogenous building blocks essential for DNA replication, body growth and
maintenance, and regulation of body functions (Ullrey et al., 2003). Protein is found in high
concentrations in young leaves, flowers, some fruits and seeds (Waterman and Choo, 1981;
Waterman et al., 1981). Non-structural carbohydrates are the primary source of energy for most
primate species (Ullrey et al., 2003; Danish et al., 2006). Non-structural carbohydrates are a
quick energy source, as they absorbed directly through the gut lining and into the bloodstream
(Ullrey et al., 2003; Danish et al., 2006). Non-structural carbohydrates are found in high
concentrations in fruits, nectars, flowers and some young leaves. Fats are also important in the
primate diet, as they particularly rich energy source and because fats can be stored for later use
(Ullrey et al., 2003; Danish et al., 2006). Fats can be found primarily in seeds, but also in non-
plant primate foods such as insects and small vertebrate prey (Ullrey et al., 2003). Water is also
an important macronutrient as it carries other nutrients throughout the body and is required for
cell regulation (Bosco et al., 2001). Primates require water intake daily, which can be found
directly in tree holes or streams, or indirectly in plant parts such as pulpy fruits and succulent
leaves (Glander, 1978).
Micronutrients, such as some vitamins and minerals, are also essential for body
development, growth, and maintenance and healing (National Research Council, 2003;
Windmaier et al., 2004). For example, calcium and magnesium are required for bone growth and
maintenance, and for function of muscles and nerves (National Research Council, 2003;
Windmaier et al., 2004). Potassium is also necessary for nerve function and is important in
maintaining normal body blood pressure (National Research Council, 2003; Windmaier et al.,
2004). Similarly, sodium regulates body fluid volume and concentration (National Research
Council, 2003; Windmaier et al., 2004). Vitamins, such as niacin, folic acid, and ascorbic acid
are also important in body function and are integral to processes ranging from cell division to
building fat, muscle, and bone to oxygen transport and red blood cell generation (National
Research Council, 2003; Windmaier et al., 2004). Micronutrients are found in plant foods, but
can also be found in earthy deposits such as clay and soil (Mahaney et al., 1993).
Antifeedants are components of foods that do not contribute to body nourishment. Fiber,
a structural carbohydrate, is the primary antifeedant consumed by most primates, as it is present
in all plant foods (Van Soest, 1994; Conklin-Brittian et al., 1998). Fiber content is inversely
related to digestibility (Van Soest, 1994), as high fiber levels can also interfere with fat and
protein absorption (Ullrey et al., 2003). Mature leaves, unripe fruits, and plants such as bamboos
are particularly fibrous, and should be avoided by primates who do not have specializations to
ferment or otherwise deal with high fiber content (Yeager et al., 1990; Milton, 1993). In addition
to fiber, secondary compounds can interfere with digestion and/or absorption on nutrients.
Secondary compounds that primates commonly encounter include tannins and alkaloids. Tannins
bind to proteins and thereby reduce the digestibility of the protein, while alkaloids act as toxins
and disrupt metabolic processes (Lambert, 1998). Although some primates have evolved
adaptations to deal with specific secondary compounds (e.g. Hapalemur spp., Tan, 1999;
Glander et al., 1989), many largely circumvent ingesting significant quantities through diet
diversification or avoiding foods high in secondary compounds (Fashing et al., 2007). Primates
are highly selective feeders who discriminate finely between plant food species and parts
(Milton, 1980; Glander, 1982); these foraging decisions can often be attributed to relative
compositions of both feedants and antifeedants (Wrangham et al., 1998).
Sex based dietary differences are found throughout the primate order. Gautier-Hion et al.
(1980) demonstrated that intraspecific sex differences in diet can be even greater than
interspecific differences. To illustrate, while gestating or lactating, female cercopithecines
(Cercopithecus nictitans, C. pogonias, and C. cephus) chose protein-rich foods such as foliage
and insects, while non-reproductive females and males chose foods lower in protein (Gautier-
Hion et al., 1980). Increased protein intake has been observed in reproductive females in a
variety of other primate speciesincluding: (e.g. Indi indri [Pollock, 1977], L. catta [Sauther,
1994], Varecia variegate rubra and Eulemur fulvus albifrons [Vasey, 2002]), (e.g. Cercocebus
albigena [Waser, 1977], C. sabaeus [Harrison, 1983], Cebus olivaceaus [Fragaszy, 1986;
Robinson, 1986], Saimiri oerstedi [Boinski, 1987], Cebus capucinus [Rose, 1994], and Pongo
pygmaeus [Fox et al., 2004]). In addition to protein, reproductive females from a number of
genera show dietary shift towards a higher quality diet that is low-fiber and rich in minerals
(Waterman and Choo, 1981; Waterman et al., 1983; Sauther, 1994, 1998; Curtis, 2004). Since
food is essential for reproduction and survival, natural selection is expected to exert a strong
influence on foraging decisions (Pyke et al., 1977; Stephens and Krebs, 1986; Garber, 1987; ;
Richard et al., 2000; Lewis and Kappeler, 2005). Females able to maximize energy intake or
optimize the mix of nutrients consumed are likely to have higher reproductive output and success
(van Noordwijk and van Schaik, 1987; Altmann, 1991; van Noordwijk and van Schaik, 1999;
Dufour and Sauther, 2002). Strong selective pressure on adaptive traits, such as female food
choice, can provide important insight into primate evolutionary ecology (Altmann, 1998; Milton,
The "Madagascar traits"
Madagascar's flora and fauna are unlike anywhere else on earth (Yoder and Nowak,
2006). It is characterized by high levels of endemicity and broad diversity from a select few
orders, including lemurs, tenrecs, carnivores, and rodents (Goodman et al., 2003; Yoder et al.,
2003). Within the diverse species of Madagascar, it is common to find unusual traits. For
example the Madagascar giant jumping rat (Hypogeomys antimena) weighs in at over 1kg, and is
a herbivore in which pair-bonded parents' cooperatively rear a single infant every two years
(Eisenberg and Gould, 1970; Stephenson and Racey, 1997). Compare this with Madagascar's so-
called "common" tenrec (Tenrec ecaudatus), which weighs up to 2kg and whose females are
nearly semelparous yet have up to 32 infants at once (Sommer, 1997). And of course, the lemurs,
are noted for their suite of unusual traits which are outlined throughout this manuscript.
Madagascar's unusual animals along with their unusual life history traits and adaptations
have been largely attributed to its environmental properties. Long isolation, low colonization,
chance dispersion, strong seasonality, poor soils, and frequent natural disasters have all been
proposed to account for the peculiarities found on Madagascar. However, with nearly all of these
traits we can find examples of similar situations outside of Madagascar which have not resulted
in flora and fauna remotely similar to those in Madagascar as we know it.
In addition, as suggested by Richard and Dewar (2007), given current evidence no other
land mass appears to have the same levels of hyper-variability in rainfall and frequent yet
unpredictable natural disasters including cyclones and droughts. In its "Natural Disaster
Hotspots" document, the World Bank (2005) states that Madagascar is at high risk of human
mortality because it is prone to multiple hazards including overlapping regions with drought and
cyclones. Severe droughts are common in the arid regions of the south and southwest, and may
even be cyclical, but droughts also affect the eastern rainforests (Gould et al., 1999). Drought
results in high canopy tree mortality, tree reproductive failure, fruit crop failure and a decrease in
young leaf production. Storms and cyclones also frequent the island, with an average of seven
major events per year (Donque, 1975; Ganzhorn, 1995). Cyclone activity can result in
defoliation, complete tree knockdowns, canopy destruction, landslides and flooding (Ganzhorn,
1995). Southern portions and highlands of Madagascar also experience cold temperatures and
frost resulting from annual Antarctic storms in June through August (Terborgh, 1983).
Moreover, destructive hailstorms in these regions are often lethal to vegetation, which have little
frost tolerance. Dewar and Richard (2007) deemed the environment of Madagascar
“hypervariable” and demonstrated that intra- and inter-annual rainfall patterns throughout
Madagascar are unpredictable. Unpredictable rainfall along with frequent yet unpredictable
natural disasters result in unpredictable phenological patterns, which Dewar and Richard (2007)
argue has shaped the evolution of distinctive features of the lemurs and other mammalian fauna
on Madagascar.
In vertebrates, exposure to a stressor (a noxious or unpredictable stimulus) elicits a stress
response, which can be defined as the physiological, hormonal and/or behavioral changes that
enable the animal to cope with a stressor (Romero, 2004). Physiological stress involves a cascade
of neurological, hormonal and immunological responses that promote energy mobilization and
behavioral responses to environmental changes and challenges (Sapolsky, 1992). One
physiological stress response increases the release of catecholamine (the sympathetic “fight-or-
flight” hormone), which is followed by an increase in secretion of glucocorticoid (GC) hormones
into the bloodstream (Sapolsky, 1992). Many studies have used elevated GC, including cortisol
levels, as a measure of stress in animals (Sapolsky, 1992; Wingfield and Romero, 2001). Cortisol
functions to redirect energy from long-term storage to immediate use (Sapolsky et al., 1992), and
thus has an associated metabolic cost. Chronic elevation of GC can suppress the immune system,
somatic cell growth, and/or sexual maturation, which can in turn alter life-history patterns and
lower reproductive success (Sapolsky, 1992). Additionally, since chronic elevation in GC is a
significant predictor of early adult mortality, relative GC levels can serve as a proxy for fitness
(Romero and Wikelski, 2001; Pride, 2005).
GC levels are strongly influenced by ecological, social, and physiological variables
(Cheney and Seyfarth, 2009). Many studies of mammals have shown that fGC (fecal
glucocorticoid) levels are elevated during winter months, and during times of food or water
scarcity (reviewed by Wingfield and Ramenofsky, 1999; Romero, 2002). Additionally, in species
organized into dominance hierarchies, rank and aggressive interactions can elevate fGC (Creel,
2001; Abbott et al., 2003). Moreover, animals experiencing periods of elevated metabolic and
energetic demands, such as costly reproductive periods in female mammals, also show increased
fGC (Pepe and Albrecht, 1995; Wingfield and Ramenofsky, 1999; Romero, 2002).
While short-term (hourly) stressors are measured through fGC levels, longer-term stress
or general health can be measured through an animals’ coat condition (Berg et al., 2009). Like
fGC levels, coat condition can be affected by a plethora of factors, such as reproductive
condition (Davis and Suomi, 2006), nutritional deficiencies (Isbell, 1995; Gerold et al., 1997),
social stress (Isbell, 1995; Roloff et al., 1998; Steinmetz et al., 2006), parasites and skin diseases
(Roloff et al., 1998; Steinmetz et al., 2006), and over-grooming (Reinhardt, 2005). However, hair
loss related to nutritional deficiencies and/or general stressors tends to be bilaterally
symmetrical, and results in an overall shaggy, dry, and dull appearance (Steinmetz et al., 2005).
Isbell (1995) noted that wild vervet monkeys (Cercopithecus aethiops) exhibited significant hair
loss on an annual basis and attributed this loss to both nutritional and social stressors. In these
cases, poor coat condition correlated with low food availability and low social rank (Isbell,
This project compares adult male and female ring-tailed lemurs from two social groups in an
endemic, non-disturbed xerophytic habitat during portions of southern Madagascar's distinct wet
and dry seasons, to test some of the assumptions made by ECH with relation to the effect of
fluctuations in resource availability on activity, behavior, nutrition, and stress in ring-tailed
lemurs. Specific hypotheses include:
1. Lemur foods are seasonally and stochastically limited.
2. Lemur nutrients and/or calories are seasonally and stochasically limited.
3. Lemurs use behavioral mechanisms to save energy.
4. The dry season is differentially stressful for female lemurs.
Lemur traits are hypothesized to be part of an adaptive complex selected to help lemurs
conserve energy in their seasonally and stochastically resource-poor environments. Female
dominance and associated niche partitioning between the sexes may facilitate lemur energy
conservation and frugality, which act to offset costs of reproduction in females. By integrating
ecological, behavioral, nutritional, and biological data collected on wild ring-tailed lemurs in the
spiny forest habitat at TNP, my aim is to understand the extent that male and female lemurs are
constrained by seasonal fluctuations in resources availability. Data here is compared with data
from localities where ring-tailed lemurs have been extensively studied, namely the Beza
Mahafaly and Berenty Reserves, as well as recent research from degraded spiny forest habitats,
in order better understand how the environment has shaped adaptations in this species. This will
be the first project to examine ring-tailed lemurs in a largely undisturbed spiny forest habitat, and
provides the framework to better understand ring-tailed lemur ecology in all other habitat types.
Outline of Dissertation
To avoid unnecessary duplication of methodological and theoretical content, this
dissertation is arranged as a monograph. The following briefly outlines the content of the
subsequent chapters. In chapter two I describe the study site and methods used. Chapter three
examines the nighttime behavior of ring-tailed lemurs. Nighttime activity was not expected to be
part of the behavioral repertoire of these ring-tailed lemurs, however, since it was noticed early
in the study period (through camera trap photos) and is likely to be of significant importance to
this research and in understanding the adaptations of ring-tailed lemurs, it has been included in
this manuscript. Chapter four encompasses the climate and weather conditions of southern
Madagascar and TNP, along with plant phenology and plant food use by focal animals during the
study period. Chapter five outlines ecology of ring-tailed lemurs at TNP including activity
budgets, diet and nutrition, and stress. Finally, chapter six examines the implications of this
research for understanding ECH, and its account of the unusual traits found in lemurs, including
female dominance.
Chapter 2: Methods
Study Site
Data were collected at the Tsimanampetsotsa National Park (TNP), in southwestern
Madagascar (24°03’-24°12’S, 43°46’-43°50’E), between September 2010 and April 2011.
Figures 2.1.-2.3. show the geographical locations Tsimanampetsotsa National Park, including
base camp for this project, and locations of other ring-tailed lemur research locations discussed
frequently throughout this manuscript. Tsimanampetsotsa represents the western most
escarpment of the limestone Mahafaly Plateau. This area is highly seasonal, and is subject to
high winds, frequent droughts and cyclones (Andriatsimietry et al., 2009). The majority of
rainfall occurs between late December and February, with total rainfall rarely exceeding 400 ml
per year (Donque, 1975). The dry season is long with average durations of nine to eleven months
(Donque, 1975). Temperatures can be extreme, with daytime highs of well over 40°C, although
mean daily temperatures range between 22.5°C and 35.8°C. Lake Tsimanampetsotsa occupies
45000 hectares of protected RAMSAR wetlands, and the park is another 43200 hectares of land
protected by Madagascar National Parks.
Vegetation at Tsimanampetsotsa is characterized as dry, spiny, and xerophytic. It can be
further divided into four zones (Figure 2.4.). The first zone consists of the land surrounding the
lake, which is sparsely populated, but contains stands of invasive Casuarina equisetifolia, and
patches of Acrostichym aureum and Cyperus sp. (Mamokatra, 1999). The second zone lies at the
foot of the Mahafaly Plateau, where the forest ranges from partially canopied fruit trees (Ficus
megapoda, Tamarindus indica, Salvadoria angustifolia, etc.) to degraded scrub and areas of
induced desertification. In general, these fruit trees are found near ephemeral or permanent water
sources, such as springs and seeps, along the border of the limestone plateau. The third zone is
the Mahafaly Plateau, and is populated by open-canopied dwarf flora, primarily from the
families Euphorbiaceae, Didiereaceae, Bombaceae, and Fabaceae (Mamokatra, 1999). The fourth
and eastern most zone emerges where the limestone gives way to red clays and flora and are
composed of spiny bush formations with dominant plant families from Didiereaceae,
Euphorbiaeceae, and Burseraceae (Mamokatra, 1999). The plateau area is a relatively narrow
formation, running north-south, and found between the lake margin and the vast "eastern zone."
Numerous collapsed “sinks” which can contain some plants that rely on a minimum of
ephemeral water sources mark the plateau.
Figure 2.1. Relative location of Tsimanampetsotsa National Park in Madagascar.
Figure 2.2. Location of Tsimanampetsotsa in relation to the Beza Mahafaly Special Reserve,
Berenty Private Reserve, and Cap Sainte Marie, in southwestern Madagascar.
Figure 2.3. Map of Tsimanampetsotsa National Park with reference to the base living camp.
Figure 2.4. Examples of habitat zones at the Tsimanampetsotsa national park, including a) zone
1 (near) and zone 2 (distant), b) zone 2, c) zone 3, and d) zone 4. Photos a and b courtesy of
Sauther, 2012.
Study animals and data collection
Ring-tailed lemurs are endemic to southwestern Madagascar and are currently listed as
vulnerable to extinction, with declining population numbers (Mittermeir et al., 2006). Males and
females have an average body weight of 2.2-2.7kg (Tattersall, 1982; Sauther et al., 2006),
although the body weights of TNP animals may be lower than this range. Dutton et al. (2003)
anesthetized 20 free ranging animals (10 females and 10 males) and note an average weight of
1.99 kg ± 0.342kg, and minima and maxima weights of 1.15kg and 2.45kg, respectively. Ring-
tailed lemurs are the most terrestrial of the lemurs, spending up to one half of their foraging time
on the ground (Sauther, 1994; Sauther et al., 1999). They live in multi-male multi-female social
groups ranging from approximately 9-22 individuals (Sussman, 1977). They are a remarkably
plastic “edge” or “weed” species (Sussman, 1977; Gould et al., 1999; Sauther et al., 1999) and
their diet is classified as opportunistic frugivoure/folivore (Sauther et al., 1999). Their gut
morphology includes a simple stomach, moderate length small intestine, a well-developed
ceacum and intermediately long colon (Campbell et al., 2000). These morphological adaptations
allow for at least some microbially assisted fiber fermentation (Campbell et al., 2000).
Lemur catta are found in a variety of habitat types including: spiny and xerophytic
forests, gallery and deciduous dry forests, anthropogenically induced savannah, scrub and brush
land, and the mesic high altitude forests of the Andringitra mountain range (Sussman, 1977;
Goodman and Langrand ,1996; Goodman and Rasolonandrasana, 2001; Sussman et al., 2003;
Pride, 2005; Goodman et al., 2006). Ring-tailed lemurs are the only large-bodied lemurs present
in the northern portion of TNP, where this study was conducted. However, there are unconfirmed
reports of Verreaux's sifaka (Propithecus verreauxi) being found 20km south of the study area,
where the spiny forest canopy consists of larger and taller vegetation. The Vintany (n= 12-14
adults,7 sub-adults and 4-7 infants) and ILove (n= 9-10 adults, 7 sub-adults, and 4-5 infants)
groups were the focus of this research. Individual animals were identified by unique markings,
scars, mask shapes, or in the case of the collared individuals (detailed below) by their collars.
Animals, along with the names I used to identify them, age class, sex, and group are detailed in
Table 2.1. These two groups inhabited similar, overlapping home ranges that included areas
between the habitat zones 2-4. Both groups' sleeping sites were on the Mahafaly Plateau (Zone
3). The Vintany group (VG) slept in a large Ficus tree (Figure 2.5), whereas the ILove group
(IG) slept in small communal caves on the face of a 20 meter high limestone cliff (Figure 2.6).
The Vintany group fissioned near the end of the dry season, after core females in Vintany
targeted aggression towards three specific adult females in the group. The three females left the
Vintany group and were called the "Soccer Moms" once they began sleeping and spending days
away from the main group. I was unable to reliably find and follow the Soccer Mom group, but
did occasionally see then during the wet season when the two groups encountered one another.
Additionally, Figures 2.7-2.8 shows two of the places where the animals drink water, which is
available year-round.
Table 2.1. Focal animal name, group, sex, and if female, if an infant was noted and survived.
Infant survive
(yes/no), death
1 or 2
Pinky (collar)
The Patient
1 or 2
Momma Bear
No, Sept
300 (collar)
Mom 2
Sore leg girl
No, Dec
Mutant Mom
340 (collar)
Soccer Moms
Tina Greyface
Soccer Moms
Soccer Moms
No, Nov
4, 6
ILove, Vintany
1 or 2
1 or 2
Short-tail 2
ILove, Unknown
George Clooney
David Greybum
Figure 2.5. The cliff face where the ILove group sleeps (top left) and one of the ILove group
females on a rocky outcrop of the cliff (bottom right).
Figure 2.6. The large Ficus tree where the Vintany group sleeps with (top left) western view of
the tree, with the tree's aerial roots extending into the sink hole and (bottom right) the eastern
view showing the tree's breadth (~22m).
Figure 2.7. Vintany group drinking sites, including male descending Ficus megapoda aerial
roots (top left), and group members drinking (nervously) in the sink hole below their sleeping
tree (bottom right).
Figure 2.8. ILove group drinking sites, including the group drinking in the Mitoho cave (top
left), and group members entering the Mitoho cave (bottom right).
With the assistance of a local Malagasy lemur darting team, six female animals from
three distinct social groups were captured and fitted with radio tracking collars. Animals
captured were fitted with VHS radio collars (MOD-080 transmitter configuration, Telonics Inc.)
because during preliminary observations the animals were noted to be quiet and cryptic when
moving, and thus difficult to continuously follow. We used the same veterinary protocols that
were used during ring-tailed lemur captures at TNP in 2006 (see Sauther and Cuozzo, 2008) and
at Beza Mahafaly since 2003 (e.g. Miller et al., 2007). Two of the groups (ILove and Vintany)
were easily habituated to my presence within two weeks, while I was not able to habituate the
third group (Akao). The Vintany and ILove groups had previous exposure to tourists, as some
trails and the camping site are within their home ranges. Akao seemed differentially affected by
the capture process and were extremely wary of human presence both before and after capture.
Even with collared animals, I was unable to get within a reasonable viewing distance of the Akao
group and chose to stop trying to following them after 5 months. During the study, one female's
collar fell off and after the study 3 other females were recaptured to have their collars removed.
The darting team was not able to find the Akao group in order to remove their collars.
Behavioral Sampling
I collected 526 hours of focal animal data in the daytime and 67 hours of scan data at
night. Additionally, my assistants collected 275 hours of scan data in the daytime. Nocturnal
observations were not part of the original data collection plan, but early on in the study I noted
nocturnal lemur activity on camera trap photos, and decided to additionally observe the animals
at night. These data were collected during weeks bracketing full moons, between 8pm and 1am,
in October, November, and December 2010, and March 2011. Increased moon illumination aided
in my ability to observe animals in the dark. During the day, continuous, known-animal focal
follows were conducted with the objective of sampling one animal daily. If the animal was lost
for more than 30 minutes, however, I would switch to another animal. Scan data (Altmann,
1974), were collected at 5 minute intervals with the goal of including 10 adult animals in every
scan. Dominance rank and changes in rank were noted for each focal animal, based on approach
retreat repeated interactions (Hausfater, 1975). For a few animals, it was difficult to decipher
their exact rank, and in these instances I used relative rank instead (e.g. low). Photographs and
scores of coat and tail condition were taken at the beginning of every month (or when
encountered, as in the case of the Soccer Moms) as per the methods outlined by Berg et al.
(2009), where coat score of 0= good, 1= rough, 2= holes, 3= ragged, 4= sheared, and 5= bald;
and tail score of 0= good, 1= pointy, 2= thin, 3= ragged or whorled, 4= sheared, and 5= bald.
GPS position was recorded several times per day throughout the study period. Later, these data
were entered into Google Earth © (2012) in order to generate home range maps, and then data
were transferred to the online Earth Point © (2012) software (, in
order to calculate ranging areas.
During the day, animal locations were noted as being on or off the ground, and if off the
ground, I recorded if they were in a shrub, tree, or other area. Animal location scores at night
were categorized slightly differently, and included the following: tree/cave, ground/cliff, or
other. Location data for "tree" and "cave", and "ground" and "cliff" were combined, because they
served the same or comparable purposes to the animals. For example, the large Ficus tree and
caves were sites for sleeping, while the ground and cliff were areas of travel between the
sleeping spot and other destinations (primarily feeding trees).
Camera trap photos of lemurs at night serve as a proxy for nighttime activity levels
(Griffitths and van Schaik, 1996). These both contribute to our knowledge of cathemeral lemurs,
and provide valuable unbiased information on the nocturnal behavior of these L. catta groups
(Griffitths and van Schaik, 1996). Cameras were stationed near the two lemur groups sleeping
sites (n=2-5), and along forest paths (n=1-3). The number and position of cameras in use varied
from time to time, as lemurs would change ranging patterns, which required camera reposition
trials, or because cameras required repairs. Resultant photos were reviewed for presence of one
or more animal. Lemur nighttime photos were categorized by lemur group, and then a average
nighttime photo rate was calculated as per the following formula (Griffitths and van Schaik
Average nighttime photo rate per day= Number of nighttime photos in one day per lemur group
Number of cameras per day
Similarly, the average lemur nighttime photo rate per month was calculated as per the following
Average nighttime photo rate per month =Number of nighttime photos in one month per lemur group
Number of days per month*number of cameras per day
Following the methods of van Schaik and Griffiths (1996), only the first of consecutive
photos containing one (or more than one) of the same individual(s) was included in the data. A
lapse of 5 minutes was used to delineate each photo event. Using only the first photo and
delineating a time period between photos aids in achieving statistical independence (Griffitths
and van Schaik, 1996). Colors of photographs varied according to light conditions. During the
day, photos are in full color; during dawn and dusk, photos are in grey scale; and at night, photos
are in black and white.
Activity patterns and feeding behavior
Focal animal data were used to calculate daytime activity budgets. These data were
combined into the following categories: feed/forage, locomote, sit/stand/rest, and other
(vigilance, groom, displace(d), scent mark, stink fight). These categories aid in not only
understanding feeding activity, but also activities that vary according to their approximate
energetic costs, such as moving or not moving. Average percentages of time spent in each
behavioral category were obtained and summed according to animal sex and group, and season.
Conversely, activity data from group scan sampling were used to calculate activity budgets and
animal locations between the day and night. Similarly, average percentages of time spent in each
behavioral category and location were summed according to day or night time, and group.
During focal follows, if an animal was feeding, the plant and plant part were noted.
Usually, plant samples were collected at the same time and place where the animal was feeding,
but this was not always possible. Given the variation that can occur between plant samples, I
aimed to collect samples which best represented what an animal was eating and this was
generally done within 24-hours of the feeding bout. A local Malagasy botanist later identified
plants and samples were dried in the shade. Plants, such as Aloe divaricatha or Euphorbia
stenoclada, that were succulent or particularly resistant to desiccation were sliced into thin strips
that promoted drying. Exudate from E. stenoclada was collected by cutting small areas of the
terminal tips of branches and catching the liquid in a glass jar. The jar was then kept in the shade
until the liquid exudate had evaporated and a powder remained. Caterpillars used as lemur foods
were also collected. These were cut in half and then left to dry in the shade. Once dry, all foods
were weighed and an average weight was calculated. The number of plant samples weighed to
produce an average weight depended on the type of sample, and on the amount of variation
between sample weights. Variation was largest in very small foods (those weighing <0.01 grams
per unit), such as flowers from Neobeguea mahafaliensis, and so 100 individual flowers were
weighed to produce an average weight per flower. With larger foods (those weighing >0.10
grams per unit) that had less variation between samples, such as young red leaf bundles leaves
from Neobeguea mahafaliensis, 10 individual leaf bundles were weighed to produce and average
weight per unit. Dry, weighed plant samples were stored in the shade, in zip lock bags with silica
Diet and Nutrition
All nutritional analyses were conducted at the Department of Animal Ecology and
Conservation of Hamburg University. A total of 80 food samples (79 plant, 1 insect) were
analyzed. The food samples included: 28 fruits or parts of fruit, 24 types of leaves, 20 flowers or
flower parts, 5 non-leaf non-reproductive plant parts, and two exudates. Samples were ground to
pass through a 2mm sieve, and dried again (at 50-60°C) before laboratory analyses. Crude lipid
(referred to hereafter as fat) content was determined by extraction using petroleum ether,
followed by evaporation of the solvent. The amount of nitrogen was determined using the
Kjeldahl method and 6.25 was used as the factor converting nitrogen to crude protein (referred to
hereafter as protein). Soluble carbohydrates and procyanidin condensed tannins were extracted
with 50% methanol. Concentrations of soluble sugars (referred to hereafter as sugar) were
determined as the equivalent of galactose after acid hydrolization of the 50% methanol extract.
Concentrations of procyanidin condensed tannin (referred to hereafter as tannin) were measured
as equivalents of quebrancho tannin (Oates et al., 1977), and polyphenole following Folin-
Ciocalteau (Bollen et al., 2004; Stolter et al., 2009). Neutral and acid detergent fibers (referred to
hereafter as NDF and ADF, respectively) (Goering and van Soest, 1970; van Soest, 1994;
modified according to instructions for the use in "Ankom fiber analyzer") were analyzed.
In order to estimate the amount an animal consumed during a day, I multiplied the
number of bites in each feeding bout by the average weight of the item eaten (Watts, 1984;
Oftedal, 1992; Rode et al., 2006). I then summed the daily total of amount eaten by an animal for
all foods and divided that total by the amount of time taken to consume the foods, to obtain a
feeding rate per hour (Rothman et al., 2011). The feeding rate per hour was then multiplied by
the average time spent feeding per day for the subgroup, such as females in the dry season
(LaFleur and Gould, 2009; Gould et al., 2011). It was essential to calculate feeding rates in this
way because the amount of focal data was not equally distributed between animals (Schulke et
al., 2006).
Calories per macronutrient were calculated by multiplying the percentage of
macronutrient in a food by the amount consumed and the following nutritional constants: protein,
4 kcal/gram; sugar 4 kcal/gram; and fat, 9 kcal/gram. Total calories per feeding bout were
obtained by adding together the calories from each of the constituent macronutrients, as seen in
the following formula:
Calories (kcal)
Amount consumed (grams)
[(% protein*4) + (% fat*9) + (% sugar*4)]
Calories from each feeding bout per animal per day were added together in order to
generate total calories. Total calories were divided by time taken to consume the foods and
multiplied by the average time spent feeding per day, as outlined and explained above. For
comparative purposes, nutrients, non-nutrients, dietary quality and calories consumed per day
were averages for each subgroup of interest, such as males.
Environmental Abiotic data
Percentage of moon illuminated for the southern hemisphere was taken from the United
States Naval Observatory Astronomical Applications Department website (NMOC, 2011).
Temperature and humidity absolute and average minimums and maximums, along with
millimeters of rainfall, were taken daily at base camp. These data, can be found in Appendix 1.
During this study temperatures at base camp ranged from 10.4°C to 41.9°C, however
temperatures can be significantly higher in certain areas of the forest. Much of the dwarf spiny
forest is on the Mahafaly limestone plateau, and in addition to there being no protective tree
canopy, solar radiation reflects intensely from the dark grey limestone formations. Though I was
not able to constantly measure spiny forest temperatures, I did occasionally take readings, the
highest of which was 53°C. For the purposes of this research, the dry season began at the onset
of the study (Sept 1, 2011) and ended at the onset of the seasonal rains (December 22, 2010).
The wet season began with the onset of seasonal rains (December 23, 2010), and ended when the
study ended (April 7, 2011). The "wet" season was extended until the end of the study period,
because at this time standing water was still abundant throughout the habitat and the vast
majority of trees were foliated. It is also of note that on February 14 2011, Cyclone Bingiza
collided with southwestern Madagascar and brought heavy rains (~125mm) and a flash flood to
Environmental biotic data
Phenological data were collected once per month. Nine line plots were established, by an
expert Malagasy botanist, within each of the representative zones (2-4) of the animals' home
ranges. To do this, a line of 25m was established and then any woody tree or shrub within 1
perpendicular meter of the line was marked with a numbered tree tag. Presence and abundance of
mature leaves, young leaves, flowers, and fruits (along with ripeness) were record. Additionally,
all Tamarindus indica and Ficus megapoda trees (which had a diameter at breast height of 10 cm
or larger) within the lemurs' home ranges were monitored (for leaves, flowers, fruits, and fruit
ripeness), as tamarind is an important food in other habitats of ring-tailed lemurs, and figs
appeared to be an important lemur food source during this study.
Predator presence was measured through camera trap photos, nest monitoring, and
opportunistically collected predator scats. One point was used to score a predator photo or scat
on the day it was taken or collected. Points were tallied monthly to create an estimate of predator
presence. Predator scores were categorized according to the activity pattern of the predator,
where P. radiatus and Canis familiaris are diurnal, Felis sylvestris is nocturnal, and C. ferox is
Data Analyses
Chi-square was used to assess variation between and within groups' day and nighttime
activities, as the data are of nominal level. Sample sizes of these data were large (e.g. 4000),
which can increase the power of chi-square (and thus artificially decreasing the p-value). As
such, Cramer's V was used for determining strength of association within "significant" Chi-
square data and the Contingency Coefficient C was also used in to compare "percent of max"
between data. In these instances, findings were only considered significant when Chi-square p-
values were equal to or less than 0.05, Cramer's V was greater than or equal to 0.15 (strong or
very strong association), and the Contingency percent of max suggested a meaningful
Linear regression and Pearson's correlation were used to assess variation between the
number of photos taken after dark in a time period (day or month) and the following independent
variables: predator presence, day length, temperature maximum and minimum, humidity
maximum and minimum, rainfall, phenology (including total phenological availability, plant part
availability and fig fruiting patterns), and nightly moon illumination. Additionally, the
relationships between nighttime activity and daytime activity budgets (feed/forage, locomote,
sit/stand/rest, other), and relationships between the daytime activity independent variables were
analyses using linear regression and Pearson's correlation. Data that may measure the same
variables twice, such as rainfall and phenology, were examined separately.
The Student's T-Test was used to analyze differences in the mean between seasons, lemur
sexes and groups for activity patterns and plant part eaten, daily intake of nutrients (protein,
sugar, fat), non-nutrients (tannin, polyphenole, NDF, ADF), dietary quality (protein:ADF), and
calories. For the dependant variables in this chapter and in Chapter 5, numerical codes were used
in place of words when analyzing differences between sex (female=1, male=2), season (dry=1,
wet=2), and group (ILove=1, Vintany=2). Therefore, the direction of t reflected that of the
coding. For example, a negative t between sexes would imply that males had a higher value for a
given variable, when compared to females.
Once again, the Student's T-test was used to assess variation in the means between coat
and tail scores between sexes and seasons. Since results from the condition of coat and tail
condition were not significantly different (i.e. a individual with a coat score of 3 also had a tail
score of 3), only the data for coat condition are presented.
Values of p that were less than or equal to 0.05 were considered significant and marked
with an asterisk. SPSS 19.0 was used for all statistical analyses.
CHAPTER 3: Cathemeral activity in wild ring-tailed lemurs
Adaptations to diurnal or nocturnal living are vast, and may affect variables such as life
history, diet, sociality, morphology, predator and prey dynamics, and sensory functioning (see
Enright, 1970; Terborgh and Jackson, 1986; Jacobs, 1993; Rydell and Speakmen, 1995). It
would thus seem unlikely that primates, or any mammal, would be active both during the day
and night, given that day-active adaptations may hinder an animal during the night, and vice-
versa (Charles-Dominique, 1975; Aschoff et al., 1982; Halle, 2006). Although it is rare for
primates to exhibit cathemeral activity patterns, one haplorrhine genus, Aotus (Wright, 1989;
Fernandez-Duque, 2003), and two strepsirrhine genera, Eulemur and Hapalemur (Curtis and
Rasmussen, 2002, 2006) are currently regarded as cathemeral.
The Lemuriformes offer an excellent opportunity to understand factors that may drive
cathemerality, given that lemurs are a monophyletic group exhibiting the three main activity
patterns, namely they can be nocturnal, diurnal, or cathemeral (Tattersall, 1982; Donati and
Borgognini-Tarli, 2006). Additionally, since cathemerality is, by comparison, found in many
species of Malagasy primates, it seems likely that Madagascar has or had some environmental
properties favoring flexible activity patterns (Tattersall, 1982). Dewar and Richard (2007)
deemed the environment of Madagascar "hypervariable," due to its seasonality, unpredictability
and frequent tropical cyclones. We thus know that the environment is unpredictable and that
some lemurs use flexible activity patterns, however, teasing apart environmental factors
promoting cathemeral activity patterns in lemurs have proved rather arduous (Curtis and
Rasmussen, 2002). Some of the difficulties lie in the impracticality of monitoring animal's
behavior over 24-hour periods, and our own shortcomings in the nocturnal environment (Curtis
and Rasmussen, 2002). Additionally, ever changing environmental factors can make
understanding cause and effect factors complex (Curtis, 2006). Various models have even been
proposed to account for cathemerality in different species and habitat types in Madagascar, yet
what we are learning from these explanatory models is that there likely is no one-size-fits-all
proximate or ultimate answer as to why cathemerality exists in lemurs (see Rasmussen, 1999;
Curtis and Rasmussen, 2002; Curtis, 2006). Despite the difficulties associated with cathemeral
research in lemurs, activity patterns are of basic importance in understanding adaptations behind
primate radiations (Donati and Borgognini-Tarli, 2006), and should remain a priority in lemur
evolutionary biology.
While adaptive reasons have been proposed to account for cathemerality in all primates
(see Overdorff, 1988; Enqvist and Richard, 1991 Overdorff and Rasmussen, 1995; Curtis and
Rasmussen, 2002), non-adaptive explanations have also been proposed to account for this in
lemurs (van Schaik and Kappeler, 1996). Possible (non-mutually exclusive) ultimate
environmental factors favoring flexible activity patterns include: thermoregulatory benefits
(Curtis et al., 1999), predator avoidance (Overdorff, 1988; Curtis et al., 1999), competition
minimization (Curtis, 1997; Rasmussen, 1999; but see Overdorff, 1993) and nutritional needs
(Engqvist and Richard, 1991; Wright, 1999; Tarnaud, 2006). Alternatively, for lemurs,
cathemerality has been suggested to be a non-adaptive transitional state or evolutionary
disequilibrium, wherein nocturnal animals are in the process of becoming diurnal, resulting from
relaxed selection pressure of diurnal living following the relatively recent mass extinctions of
large diurnal raptors (van Schaik and Kappeler, 1996). The following will expand on
aforementioned proposed adaptive and non-adaptive hypotheses accounting for cathemerality.
Primates, as with other mammals, employ physiological means of thermoregulation
(Heldmaier and Steinlechner, 1981; Ellison et al., 1992; Haim et al., 1995). For example, fur and
fat act as insulators over long periods, and vasoconstriction and vasodilatation conserve or
dissipate heat, respectively, during the short-term (e.g. Romanovsky, 2007). Physiologically,
some nocturnal lemurs show torpor, seasonal fattening, and heterothermy (Petter-Rousseaux,
1980; Fietz and Ganzhorn, 1998; Giroud et al., 2010), yet limited shiver and sweat responses
(Aujard et al., 1998). All lemur species that have been tested show lower than expected basal
metabolic rates (BMR) as per the Kleiber equation (Jolly, 1984; Perret et al., 1998; Richard and
Dewar, 1991; Wright, 1999; Richard et al., 2000; Genoud, 2002; Simmen et al., 2010). However,
it has been debated as to whether reduced BMR is a phylogenetic trait shared with other
strepsirrhine primates (e.g. Müller, 1985; Genoud, 2002), or if low BMR is an adaption to
Madagascar's feast/famine environment (Richard and Dewar, 1991; Wright, 1999; Schmid and
Stephenson, 2003). While more data are needed to understand if low BMR is a trait unique to
lemurs, we do know that some lemurs have extremely low BMR. For instance, the BMR of E.
fulvus is just 28-56% of the expected rate (Daniels, 1984). Low BMR, in this case, is coupled
with a near constant and relatively high body temperature which ranges from 38.4-39.4°C
(Daniels, 1984; Erkert and Cramer, 2006). Low BMR indicates a capacity for temperature
regulation, while a high body temperature disallows a reduction in body temperatures during
cool periods or times of inactivity (Daniels, 1984; Müller, 1985). For E. fulvus the resultant
"thermoneutral zone," or temperature range wherein animals expend little or no energy to
maintain their body temperature, lies between 22°C and 30°C (Daniels, 1984; Erkert and
Cramer, 2006). The thermoneutral zone of L. catta is unknown, however, BMR in L. catta is just
26-37% of that predicted (McNab in Simmen et al., 2010), and body temperature ranges from
36.9-38.9°C (Teare, 2002; Dutton et al., 2003). Given that ring-tailed lemurs are primarily
adapted to the hot dry forests of southern Madagascar (although overnight temperatures can be
low in the austral winter) (Goodman et al., 2006), while Eulemur are adapted to the cool eastern
humid forests of northern Madagascar (see Tattersall and Sussman, 1998), we might expect the
thermoneutral zone of ring-tailed lemurs to be slightly higher than that of Eulemur spp., however
this prediction does require testing to be confirmed.
Behavioral means of thermoregulation can both increase or decrease body temperature.
Ring-tailed lemurs are well known for their sunning behavior, which acts to increase body
temperature on cool days (Jolly, 1966). Other behavioral mechanisms used by lemurs that
increase body temperature may include postures that decrease surface area (and reduce heat
dissipation), and social thermoregulation, such as huddling (Jolly, 1966). For example, Eulemur
collaris spends significantly more time in huddle or curled positions during the cold season of
the tropical wet forests of Saint Luce (Donati et al., 2011). Conversely, behavioral mechanisms
used to decrease body temperature (or prevent over-heating) include postures that increase
surface area (and increase heat dissipation) (Donati et al., 2011). During the hottest periods of the
day, L. catta rest in the shade in prone positions and hug onto the bases of cool trees or rocks.
Animals also lick their hands and feet, and pant, all of which aid in heat reduction through
dissipation (Jolly, 1966). Each of the aforementioned behaviors helps maintain optimal body
temperatures, while minimizing use of comparatively energetically expensive physiological
Some lemurs also adjust activity patterns as a behavioral mechanism minimizing energy
required for thermoregulation (see Curtis et al., 1999; Curtis, 2006). In the reed beds of lake
Alaotra, H. alaotrensis avoids activity in particularly high daytime temperatures, and instead
increases nighttime activity (Mutschler, 2002). Alternatively, in the deciduous forest of
Anjamena and Kirindy, E. mongoz (Curtis et al., 1999) and E. rufus (Donati et al., 1999;
Kappeler and Erkert, 2003) increase nighttime activity during low nighttime temperatures (e.g.
11°C [Kappeler and Erkert, 2003], 18°C [Curtis et al., 1999]). Limiting activity in high
temperatures minimizes heat stress, while increasing activity during cool periods induces heat
production generated through movement (Curtis et al., 1999). In these instances, cathemerality
may be a behavioral mechanism that helps reduce thermoregulatory costs associated with heat or
cold stress (Curtis et al., 1999). Though a contributing factor for some cathemeral lemurs, other
cathemeral lemurs nocturnal activity levels are not related to thermoregulatory benefits (e.g. E.
macaco [Andrews and Birkshaw, 1998], E. fulvus [Donati and Borgognini-Tarli, 2006], E.f.
collaris [Tarnaud, 2006]). Thus, although thermoregulation may help explain some variation in
lemur activity patterns, it cannot solely explain the variation.
Anti-predator strategy
Predation is a major force in shaping primate evolution (see van Schaik and van Hoof,
1983; Andrewartha and Birch, 1984; Anderson, 1986; Cheney and Wrangham, 1987; Isbell,
1994; Stanford, 2002). Yet, there is a longstanding debate as to the extent to which lemurs
experience predation, particularly predation from aerial predators (van Schaik and Kappeler,
1996; Kappeler, 1997; Wright, 1999). It has been suggested that extant lemurs are subject to
relatively low levels of predation, especially aerial predation, due to the mass extinction of large-
bodied diurnal raptors that occurred about 2000 years ago (van Schaik and Kappeler, 1996).
There is mounting evidence, however, which demonstrates that lemurs are subject to significant
predation from diurnal raptors (Karpanty 1999, 2003, 2006). Additionally, lemurs are under
threat of predation from their most formidable endemic predator, the fossa (Cryptoprocta ferox)
(Hawkins, 2003; Colquhoun, 2006). Data on animal location (i.e. ground, low canopy, high
canopy) in several Eulemur species may demonstrate a strategy for avoiding predation by diurnal
raptors (Andrews and Birkinshaw, 1998; Overdorff, 1988; Curtis et al., 1999; Donati et al., 1999;
Rasmussen, 2005; Gould and Sauther, 2006), and for avoiding predation by cathemeral fossa
(Kohncke and Leonhardt, 1986; Dollar et al., 1997; Hawkins, 2003). These lemurs exploit the
upper layer of the forest during the night, while using the middle to lower layers during the day
(Overdorff, 1988; Curtis et al., 1999; Donati et al., 1999; Rasmussen, 2005). Feeding and
traveling in the mid to low forest during the day may help evade detection from raptors (Curtis,
2007); while, feeding and traveling in the high canopy may help avoid detection from terrestrial
predators, particularly the fossa (Hawkins, 2003), but also forest cats. The fossa is adept in the
trees, but has difficulty in the highest canopy due to its body size (Hawkins, 2003). Though it
may be the case that lemurs are less likely to attract fossa at night if they are in the high canopy,
fossa are cathemeral (Colquhoun, 2006), which would put lemurs at greater risk of detection by
fossa during the day. Aside from location, lemurs may use cathemerality as a mechanism of
temporal crypsis, wherein predators are unable to focus efforts on a particular time for capturing
prey (Colquhoun, 2006). Predation is an important factor in lemur ecology, however, it is once
again central to note that although predation appears to play an key role in the cathemerality of
some lemurs, other lemurs with known reduced predation threat also maintain cathemeral
activity patterns (Tarnaud, 2006). Thus, predation cannot solely account for variation in these
activity patterns.
Avoidance of competition
Though interspecific competition is intrinsically linked to niche differentiation, the
relationship between cathemerality and resource competition remains the most ambiguous to
date (Curtis and Rasmussen, 2006). Rasmussen (1999) showed that E. fulvus fulvus and E.
mongoz in a seasonal dry forest of northeastern Madagascar had overlapping core home ranges,
along with preferred sleeping trees and diet. In this case, we would expect that species would
favor the reduction of interspecific competition through temporal shifts (Rasmussen, 1999).
However, these species groups actually displayed higher than expected encounter rates, many of
which were neutral or positive, even in feeding contexts (Rasmussen, 1999). Additionally, the
importance of competition in cathemeral activity patterns is less understood in communities that
do not contain congeners (Curtis and Rasmussen, 2006). Given that L. catta is the sole species of
the Lemur genus and that the present research took place in an area without intraspecific
competitors, the avoidance of competition and its potential role in cathemeral activity will not be
further addressed here.
Metabolic and dietary needs
Seasonal and stochastic fluctuations in food availability pose a significant problem to
Malagasy primates (Richard and Dewar, 2007). Tattersall and Sussman (1975) linked the
nocturnal feeding of E. mongoz to the temporally available nectar from Ceiba pentaandra
flowers. Furthermore, Andrews and Birkshaw (1998) found that the presence of particular foods,
both during the day and night can help explain activity patterns. Yet, others have found few or no
associations between temporal availability of food and diurnal or nocturnal behavior (Overdorff
and Rasmussen, 1995; Colquhoun, 1998; Curtis et al., 1999; Rasmussen, 1999; Tarnaud, 2006).
Rather than specific foods, Enqvist and Richards (1991) proposed that during times of fruit
scarcity lemurs may include more fibrous leaves in their diets, thus requiring a 24-hr clock to
maximize food spacing and digestive capacity. Results on this hypothesis are contradictory.
Tarnaud (2006) found that E. f. mayottensis females increased their leaf consumption during the
daytime, when activity was extended through the night (Tarnaud, 2006). However, Curtis et al.
(1999) found no relationship between fibrous diets and nighttime activity. As noted, some
variation in cathemeral activity patterns may be explained by dietary needs, however diet cannot
solely explain this variation.
Transition between nocturnal and diurnal niche
van Schaik and Kappeler's (1996) EDH argues that cathemeral lemurs are in a transitional
state between nocturnal and diurnal lifestyles. However, since EDH was covered in Chapter 1 of
this dissertation, and EDH does not appear to be a fruitful direction for elucidating causal
mechanisms of lemur traits, it will not be further explored here.
Cathemerality in Lemur catta
Although L. catta is considered "strictly diurnal" (Jolly, 1966; Sauther et al., 1999) there
are anecdotal (Jolly, 1966; Sauther, 1989) and/or limited empirical (Traina, 2001; Parga, 2011)
data suggesting a flexible activity pattern in this species. Jolly (1966) and Sauther (1989) have
noted nocturnal yapping (a call in response to a potential predator) by L. catta at both Berenty
Private Reserve and Beza Mahafaly Special Reserve. Researchers at Beza Mahafaly Special
Reserve have recently noted that when the moon was full (or near full) ring-tailed lemurs slept
near heavily fruiting tamarind (Tamarindus indica) in camp and then fed on those fruits during
the night (Sauther, pers. obs.). Traina (2001) found that the nighttime activities of L. catta at
Berenty included feeding, grooming, traveling, playing, mating, and fighting. Parga (2011) used
GPS during a brief, one-week study of five, semi-captive, provisioned L. catta on St. Catherines
Island, Georgia, USA, and found that animals did range between the hours of 1900 and 0530.
Most recently, in July of 2011, ring-tailed lemurs at Beza Mahafaly Special Reserve were
observed by local villagers engaging in crop raiding behaviors during the full moon (Enafa, pers.
comm.). Albeit limited, these observations suggest that wild, free-ranging, and captive ring-tailed
lemurs engage in some degree of cathemeral activity. Interestingly, L. catta may also have the
patterns of eye morphology commonly found in cathemeral animals. In fact, they have both a
well-developed tapetum lucidum and area centralis, which means that ring-tailed lemurs have
both visual sensitivity for nighttime activity and visual acuity for daytime activity (Rohen and
Castenholtz, 1967; Starck, 1995). Lemur catta is regarded as an extraordinarily flexible primate
in many aspects (e.g. habitat type, feeding behavior, sleep sites) (Goodman et al., 2006; Gould,
2006; Jolly et al., 2006; Sussman et al., 2003) and cathemeral behavior may represent another
way in which this species is adaptable. Cathemerality in L. catta may thus play a key role in our
understanding of adaptations enabling flexibility in this species.
Accounting for cathemeral activity in lemur behavior and ecology is an extremely
important aspect of future lemur studies, including that of L. catta. Nocturnal data are largely
missing in all but a few studies in species of Hapalemur and Eulemur, which has likely created a
bias towards daytime activities in many lemur study species (Curtis and Rasmussen, 2002).
Curtis and Rasmussen (2002) point out that many lemur research projects aimed at
understanding "seasonal stress" likely provide inaccurate activity budgets and feeding data, given
that nocturnal data are under-represented or absent. Nocturnal data of cathemeral lemurs could
have a huge impact on our understanding lemur adaptations, including the 'holy grail' of lemur
research, namely, understanding why female lemurs are dominant to males (Pochron & Wright,
Due to the nature of the study, data collection is biased towards daytime activities, and
cannot account for all lunar phases or time periods. This schedule allowed for clearest
observation of nighttime activities, and continuation of the larger research project. However,
through animal observations, use of camera traps, and examination of prey remains, some insight
into what animals were doing during nocturnal activities is provided. Results demonstrate that L.
catta are in fact cathemeral, point to some of the proximate variables promoting cathemeral
behavior, suggest ultimate benefits of cathemerality, and compares this research with the current
literature on cathemerality in the Lemuridae.
Animal data
Cathemeral activity occurred throughout the study period (Figure 3.1). Animal activity
and location scores from scan samples are presented in Tables 3.1 and 3.2, respectively.
Table 3.1. Day and Night animal activity scores from scan sampling with percentage of time
spent engaging in each activity.
Day: percentage of time
in each activity
Night: percentage of time
in each activity
Feed or Forage
Table 3.2. Day and night animal location scores from scan sampling with percentage of time
spent in each location.
Day: percentage of time
at location
Night: percentage of
time at location
Average number of photos taken
per camera trap night
Figure 3.1. Nighttime activity levels in the
ILove and Vintany groups from September to
All Chi-square values examining day and night animal activities, and animal day and
night animal locations were significant (Table 3.3-3.4). Data with Cramer's V values that were
strong or very strong are considered significant, while those with none or weak relationships
were considered not significant. The Contingency Coefficient C (reported as percentage of max)
reflect findings similar to those of Cramer's V, namely that there were much stronger
relationships between day versus night activities or locations, when compared to within the day
or night. There were significant differences in animal behavior and location between the day and
the night, however, there were no significant differences found between animals groups.
Table 3.3. Chi-square, Cramer's V, and Contingency Coefficient C as percent of max ("C")
values for between and within group variation in day and nighttime active lemur behaviors
(locomote, feed/forage, groom, other).
Cramer's V
All animals day versus night
VG day versus night
IG day versus night
VG day versus IG day
VG night versus IG night
Table 3.4. Chi-square, Cramer's V, and Contingency Coefficient C as percent of max ("C")
values for between and within group variation in day and nighttime lemur locations.
All animals day versus night
Very Strong
VG day versus night
Very Strong
IG day versus night
Very Strong
VG day versus IG day
VG night versus IG night
Both groups of lemurs ranged extensively throughout the day (2018m on average, as
presented in Chapter 5). Nighttime ranging, on the other hand, was restricted. Most animals
stayed within a 100m circumference of their group's sleep site. That being said, on two occasions
I saw lone males leave their group at night, and have one camera trap photo (Figure 3.2) of a
male in the "momma" baobab tree which is farther than 100m from either of the groups sleep
Figure 3.2. Male ring-tailed lemur in the momma baobab tree at 12:09am on March 20, 2011.
Camera trap data
The camera traps stationed near animal sleeping sites resulted in 1314 unique lemur
photographs from 422 camera trap days. Of these photos, 387 were at night (Figure 3.3).
Figure 3.3. Camera trap photos taken near animals sleep sites. Clockwise from top left: IG
members during daylight at 6:02pm, IG mother and offspring during the night at 11:51pm, VG
animal after dark at 8:50pm, and VG animals before daylight at 4:48am.
Nighttime Activity
Significant correlations were found between nighttime activity levels and daytime
temperature maximum, nighttime temperature maximum, and to a lesser extent, amount of
nighttime moon illumination (Table 3.5). Furthermore, linear regression showed significant
relationships within the aforementioned variables (Table 3.6). In other words, the lemurs
increased their nighttime activity levels when a) it had been hot during the day, or b) was warm
during the night (Figure 3.4), and/or c) when there was greater moon illumination, although this
was marginal. High daily and nightly temperatures explained about 20% of the variation in
nighttime activity levels, while increased moon illumination explained about 2%. No significant
associations were found between nocturnal activity and day length, rainfall and/or phenology, or
predator presence. However, the events surrounding the death of a predated ring-tailed lemur
infant will be detailed below.
Table 3.5. Pearson's correlation between lemur nighttime activity levels and daytime high
temperature, nighttime high temperature, and moon illumination.
p-value (1-tailed)
Daytime temperature
Table 3.6. Linear regression of lemur nighttime activity levels with daytime temperature
maximum, nighttime temperature maximum, and moon illumination.
p-value (1-tailed)
Daytime temperature, nighttime temperature, and
Average temperature (°C)
Average nighttime activity levels
Figure 3.4. Average nighttime activity levels with
nighttime temperature
Nighttime Activity Levels
Minimum temperature (C°)
Pearson's correlation shows positive relationships between average monthly nighttime
activity levels and daytime activities of feed/forage and sit/stand/rest, while negative correlations
between average nighttime activity levels and daytime activities of locomotion and "other"
(Figure 3.5, Table 3.7). Similarly, linear regression showed significant relationships between the
amount of lemur nighttime activity and daytime activity budgets (Table 3.8). Additionally, there
were significant correlations found within the daytime activity categories (independent variables)
(Figure 3.6, Table 3.9).
Figure 3.5. Nighttime activity levels and regression lines with the following daytime activities:
a) Feed/forage, b) Locomote, c) Other, d) Sit/stand/rest.
Table 3.7. Pearson's correlation between lemur nighttime activity levels and daytime activity
budget categories (feed/forage, locomote, sit/stand/rest, other).
p-value (1-tailed)
Table 3.8. Linear regression of lemur nighttime activity levels with daytime activity budgets
(feed/forage, locomote, sit/stand/rest).
p-value (1-tailed)
Figure 3.6. Correlations and best fit lines within daytime activities, including: a) feed/forage and
locomote, b) feed/forage and other, c) feed/forage and sit/stand/rest, d) locomote and other, e)
locomote and sit/stand/rest, and f) other and sit/stand/rest.
Table 3.9. Pearson's correlation between lemur daytime activity budgets (feed/forage, locomote,
Feed/forage, locomote
Feed/forage, other
Feed/forage, sit/stand/rest
Locomote, other
Locomote, sit/stand/rest
Other, sit/stand/rest
Daytime activities that were considered "other" are further detailed in Figure 3.7. Only
males engaged in stink fighting, as we know, and scent marking was significantly correlated to
males (Pearson's= 0.900, N=4, p=0.050), when compared to females. No other significant
differences were found in these data.
Figure 3.7. Daytime "other" activities females and males in the dry and wet seasons.
Female dry
Vigilance 15%
Groom 22%
Scent mark 35%
Misc 18%
Female wet
Vigilance 3%
Groom 5%
Displace(d) 50%
Scent mark 18%
Misc 24%
Male dry
Vigilance 1%
Groom 6%
Scent mark,
stink fight 68%
Misc 7%
Male wet
Groom 9%
Displace(d) 3%
Scent mark,
stink fight 72%
Misc 16%
Predation of an infant ring-tailed lemur
On October 26, 2010, a 3-4 week old dead infant L. catta was found under the Vintany
sleep tree. Given the state of decay, the infant had likely died the previous day (Figure 3.8). The
ventral surface of the infant's torso was absent and it was not possible to determine its sex. There
were two puncture wounds on the infant's neck, with a distance of 16mm between them. This
infant was probably killed (or at least bitten by) either an ampaha or a fossa, given that either of
these animals can have an inter-canine distance of 16mm (Sauther, unpublished data).
Figure 3.8. Remains of L. catta infant a) as encountered with dorsal surface untouched, b)
ventral surface after flipping carcass over, c) puncture wounds on side of torso.
During the entire study period, there were two instances, which I am aware of, when the
Vintany group did not sleep at their usual tree. Those nights were October 25 and October 26,
2010. Instead of their usual sleeping site, the group slept north of camp at the base of the
Mahafaly plateau. Using telemetry, I was able to locate their general location at about 10:00pm
on Oct 25th, but could not pinpoint where exactly the animals were sleeping because of problems
with nighttime visibility and there not being any paths in the vicinity.
There were camera trap images for the Vintany group after dark on October 20-23 and
25, and then not again until November 21, 2010 (27 days later). There were no camera trap
images of predators surrounding the infant's death. Albeit circumstantial, it seems as though a
predator had taken the infant ring-tailed lemur, probably at night, on the evening of October 25,
2010, and that after this event the Vintany group avoided their usual sleep tree for two nights,
and avoided nighttime activities for nearly a month.
This study of wild L. catta at Tsimanampetsotsa National Park, which is part of a long-
term ecological assessment of this lemur population, documents for the first time in a wild ring-
tailed lemur population that ring-tailed lemurs are frequently active during the night, and thus
should be considered cathemeral. During nighttime activity, TNP lemurs engaged in more
feeding behavior and less locomotion when compared to daytime activity. Furthermore, at night,
most animals avoided being on the ground and spent the majority of their active time in trees
within 100m of their usual sleeping spots. The amount of nighttime activity in these two lemur
groups increased with high daily temperatures, nightly high temperatures, and greater moon
illumination, although these three independent variables only explain 26% of the variation.
Significant positive correlations were found between nighttime activity levels, daytime feeding
and daytime resting, while significant negative correlations were found between nighttime
activity levels and daytime locomotion and daytime "other" behaviors. While more data are
needed to completely identify the underlying causes of cathemerality in L. catta, these results
allow for some evaluation of the functional relevance of cathemeral activity in a comparative
Increased moon illumination promotes nocturnal activity in many lemur species from
various habitats (Colquhoun, 1998; Donati et al., 1999, 2001; Olivieri, 2002; Kappeler and
Erkert, 2003; Donati and Borgognini-Tarli, 2006). Moreover, nocturnal activity is highest when
the moon is above the horizon and at its brightest (Kappeler and Erkert, 2003; Donati and
Borgognini-Tarli, 2006). Though moon rise and crest were not considered in this study, available
moon light was significantly related to nocturnal activity, but only marginally. Given that moon
illumination has been suggested to positively affect L. catta activity (Traina, 2001; Parga, 2011),
it is likely that light availability is a factor in L. catta nocturnal activity, however it only accounts
for a small amount of the variation in nighttime activity here.
Ambient temperature also affects nocturnal activity in some lemur species (Overdorff and
Rasmussen, 1995; Colquhoun, 1998; Curtis et al., 1999; Donati et al., 1999; Rasmussen, 1999;
Kappeler and Erkert, 2003; Donati and Borgognini-Tarli, 2006), which may be a means to
minimize thermoregulatory energy requirements (Curtis et al., 1999; Curtis and Rasmussen,
2002). In fact, lemurs have a suite of physiological, behavioral, postural, and social activities,
which appear to function as low-cost themoregulatory mechanisms (Richard and Dewar, 1991;
Morland, 1993; Ostner, 2002). These have been interpreted as adaptations to the distinct
seasonality and unpredictability of resources in Madagascar (Jolly, 1984; Wright, 1999; Dewar
and Richard, 2007). All lemurs that have been studied thus far appear to be hypometabolic
(Daniels, 1984; Genoud, 2002; Simmen et al., 2010), and have limited capacity for sweat or
shiver responses (Aujard et al., 1998). However, low BMR in Eulemur spp. seems to be coupled
with high body temperature (Daniels, 1984; Müller, 1985), which may help explain high levels
of activity in these animals (Donati et al., 2007). If these patterns are also present in other genera
of lemur, such as L. catta, it is likely that lemurs have evolved physiological and behavioral traits
that maintain high body temperatures even with their low metabolic rates (Donati et al., 2011).
High activity levels resulting from a high resting body temperature may help lemurs exploit
scarce and ephemeral resources when they are briefly available.
It has thus been proposed that lemurs should often use behavioral thermoregulation as an
energy efficient way to maintain temperature homeostasis (Morland, 1993). Research here
suggests that cathemerality could represent a behavioral mechanism for thermoregulation. I
noted that during days with hot periods, particularly when temperatures were greater than 45°C,
lemurs spent long periods of time resting in the shade, while panting and licking their hands and
feet, and were subsequently more likely to be active at night. Nighttime activity, in this case,
may have allowed animals to make up for lost feeding or foraging time when conditions were
much more favorable. Ellwanger and Gould (2011) note that activity rapidly declines in L. catta
once ambient temperatures surpass 40°C and suggest that in order to compensate for the lost
feeding time, animals use abbreviated but intense feeding periods in the late afternoon, wherein
feeding rates increase. Data from this study suggests that L. catta increase nighttime activity
during periods with particularly high daytime temperatures (i.e. >40°C). During nighttime active
periods, animals spend the majority of their time feeding (53%), and as such, nighttime feeding
may serve as an additional mechanism for making up for lost feeding time, when daytime
conditions are not optimal. The avoidance of high daytime temperatures and increased nighttime
foraging has also been found in H. alaotrensis (Mutschler, 1999, 2002).
These ring-tailed lemurs were more likely to be active at night when nighttime
temperatures were warmer, and may have been limiting nighttime activity during particularly
cold nights. Huddling and avoidance of activity during overnight cold temperatures have also
been seen in H. g. alaotrensis (Mutschler, 1998) and Aotus aotus azarai (Fernandez-Duque,
2003). However, the opposite case where correlations between low nighttime temperatures and
nighttime activity have been reported in several species of Eulemur (mongoz [Curtis et al., 1999],
rufus [Donati et al., 1999], rubriventer [Overdorff and Rasmussen, 1995]). Donati and
Borgognini-Tarli (2006) note that there seems to be a divide in the activity pattern and level of
seasonality in the habitat. Correlations between increased nocturnal activity and low overnight
temperatures tend to be seen in forests with reduced seasonality and smaller relative annual
temperature fluctuations, whereas the avoidance of activity during cold nights occurs in highly
seasonal habitats where overnight temperature lows can vary by 20°C, as in the current study,
although there are exceptions to this statement (see Curtis et al., 1999).
Nocturnal activity was not directly related to measures of predator presence in this study.
However, measures may not have accurately reflected predator pressure, as other lines of
evidence suggest predation may have played a role in nocturnal activity of L. catta. First, animals
had a marked aversion to traveling on the ground and spend far less time in locomotion at night.
While spending 25% of their travel time on the ground during the day, they spent only 2% of
their time on the ground at night. Ground travel is likely associated with increased predation by
nocturnal cats, and potentially by fossa, and may be why lemurs avoided the ground at night
(Curtis, 2006). Additionally, nighttime activity was comparably low at the beginning of the study
period, which corresponded to the lemur birth season, but increased every month after that, as the
infants increased in size and improved their physical abilities (though nighttime temperatures
were also low at the onset of the study). Infant L. catta are extremely precocial and actively
move about their mother shortly after birth (Sauther, 1989). During the second week of life,
infants engage in exploratory behavior through hopping off the mother and climbing around their
environment (Gould, 1990). This can be a particularly dangerous time for infants, as their
mothers may quickly flee if startled, leaving the exploring infants behind. During this study, a
three week old infant was found dead on the ground at the Vintany group's sleep site. It had only
been dead a few hours and had two puncture wounds on the side of its torso, which were
consistent with the size and shape of either cat or fossa canine teeth (Figure 3.9). Camera trap
photos revealed that animals were up the previous night, but this group was not seen after dark
again until 27 days later. Furthermore, the group did not sleep in their regular sleep tree for two
nights following my finding the dead infant. This was the only known occasion during the study
when Vintany did not sleep in their normal tree. In addition to this infant, the remains of at least
three adult ring-tailed lemur was found in predator scat from within the group’s overlapping
home ranges. Of course, these remains could have been the result of scavenging rather than
direct predation, but the lemurs behavior suggest animals are subject to predation, engaging in
predator avoidance, and that anti-predator behaviors should be explored further in future
The diet hypothesis predicts that cathemerality is an adaptive response that enables
animals to best utilize low-quality food resources during times of scarcity. For this hypothesis to
be true, we would expect to see more cathemeral activity during periods when animals were
eating markedly fibrous foods, or when food resources were most limited. Data presented in
Chapter 5 of this manuscript demonstrates that fiber consumption was higher for both males and
females during the dry season, which corresponds to periods of relatively low nocturnal activity
by these lemurs. Additionally, the TNP ring-tailed lemurs were much more active during the wet
season when foods are more abundant. This pattern of increased nocturnal activity with increased
food abundance, was also found by Kappeler and Erkert (2003) in their work on E. f. rufus in the
dry deciduous forests of Kirindy. Thus, it does not appear that L. catta at TNP increased
nighttime activity in response to highly fibrous foods or scarcity of resources. All observed foods
consumed during nighttime observations, were also consumed during the day, however, it was
not possible to assess rates of feeding or amount consumed at night. Curtis (1999) suggested that
feeding behaviors at night in E. mongoz were not significantly different from their daytime
feeding habits. Since we do not know if feeding behaviors vary between night and day in ring-
tailed lemurs, this should be explored further, as this data could impact the interpretation of
fibrous food consumption. Proximity to food resource seemed to be the most important factor
determining what foods the animals would consume at night. Almost all nighttime observations
of animals were within 100m of their sleep site. Males sometimes went off alone and ranged
further at night (Figure 3.2), but in the vast majority of nighttime observations animals remained
close to their sleeping site. This type of ranging was likely related to predator avoidance, since
there is no continuous canopy and animals have to travel on the ground if they are to range
further. The evidence from other lemur species is mixed on the relative importance of the diet
hypothesis in relation to cathemeral activity. Donati et al. (2009) found that fiber was able to
explain a significant portion of activity variation in E. collaris and E. collaris X E.f. rufus
hybrids, while many other authors have found no such associations (Andrews and Birkinshaw,
1998; Colquhoun, 1998; Curtis et al., 1999; Rasmussen, 1999; Fernandez-Duque, 2003;
Kappeler and Erkert, 2003). With reference to diet, cathemeral lemurs may simply increase their
caloric intake in order to meet (or attempt to meet) their metabolic needs, and are achieving this
through nighttime feeding. Nocturnal activity, however, by their thermoregulatory capacities,
which may explain why animals were not more active at night during the times when foods were
most scarce, and overnight temperatures were lowest. Nighttime feeding and foraging was
positively correlated to daytime feeding and foraging and also resting, while negatively
correlated with locomotion and "other" behavioral categories. These data follow the trends I have
found for activity budgets of male and female ring-tailed lemurs, in that when food is more
plentiful animals feed more and travel less. From an energetic point of view one might predict
that nighttime feeding would be most beneficial to animals when foods were generally scarce
and animals have to travel more and rest less, while feeding during the day. Once again however,
the coincidence of low food availability and low overnight temperatures may impede these ring-
tailed lemurs' ability to feed during the night, though this may also be related to the relative
vulnerability of infants to predation during this time period. Food is often limited for
frugivorous/folivorous lemurs, and fruit abundance is cited as being the primary limiting factor
in L. catta survival (Jolly et al., 2002). Ability to feed at night could be important for gaining fat
during brief periods of food availability, and/or essential for survival during times of food
van Schaik and Kappeler's (1996) evolutionary disequilibrium hypothesis suggests that
cathemerality is not an adaptive trait, but rather part of the transition from a nocturnal to diurnal
lifestyle, resulting from relaxed selection pressure following the extinction of large-bodied
diurnal raptors some 2000 years ago. Existing data on predation rates by diurnal raptors
(Karpanty, 1999, 2003, 2006), eye morphology of cathemeral lemurs (Kirk, 2006), genetic
analyses (Roos et al., 2004), and phylogenetic reconstructions (Griffin et al., 2012) have all
indicated that cathemeral lemurs do not show evolutionary disequilibrium, nor do the data
presented here. Also, pairs of P. radiatus were frequently seen within lemur territory, and two
unsuccessful predation attempts on L. catta individuals were recorded. Lemurs sometimes
reacted strongly (shrieks, alarm barks, moving into trees) to the presence of P. radiatus. When
the groups were in areas of habitat that were dwarf forests or otherwise without canopy, they
would illicit intense and long alarm responses. However, when lemur groups were in or under
large trees, their reaction was very different in that they seldom alarm called, and continued to
feed while frequently glancing at the hawk(s). Sauther (1989) suggested that Harrier hawks
require open spaces in order to predate animals, because of their large wing span. From their
behavioral response to Harrier hawks, it appears as if these lemurs a) recognize Harrier hawks as
a potential predator, and b) assess the level of threat posed by hawks according to micro-habitat.
van Schaik and Kappeler (1996) suggested that lemurs' alarm responses to hawk were
inappropriate in modern times and a relic behavior left over from before the extinction of the
giant crowned eagle, S. mahery. Given that Harrier hawks prey on other large-bodied lemurs
(Karpanty 2002, 2006) and that L. catta appear to react to the level of threat posed by the hawks,
I expect that the current behavioral reactions of lemurs are appropriate. Selection pressure in the
diurnal niche is not likely relaxed, as proposed by van Schaik and Kappeler (1996), and
cathemeral lemurs are not expected to be in a state of evolutionary disequilibrium.
Conditions of Madagascar's habitats are unusually harsh (Wright, 1997; Wright, 1999).
Soils are of poorer quality than most in other primate habitats (Ganzhorn et al., 1999), and tree
growth is slower and fruit production lower than in measured forests in South America and
Africa (Terborgh, 1983; Sorg and Rohner, 1996; Terborgh et al., 1997; Struhsaker, 1997;
Ganzhorn et al., 1999). Additionally, Madagascar is subject to frequent yet unpredictable
cyclones, severe storms, and droughts, and all of Madagascar's forests are seasonal (Donque,
1975; Ganzhorn, 1995; Wright, 1997). For lemurs, the culmination of the aforementioned
conditions result in frequent predictable and unpredictable shortages of foods (Jolly, 1984;
Wright, 1999). Cathemerality could be one of the flexible responses employed by some lemurs,
which enables them to secure resources, such that they meet caloric requirements. One thing is
becoming increasingly clear in the study of cathemerality in lemurs; there is no one universal
factor or mechanism determining cathemeral activity. Rather, cathemerality is an activity pattern
employed by a variety of species, in various habitats, at different times, in response to a host of
ever changing and non-mutually exclusive variables. The task at hand remains to examine more
cathemeral lemur data, tease apart proximate mechanisms, and discover any patterns that may
In summary, I argue that L. catta is in fact cathemeral. Proximate mechanisms promoting
nighttime activity include daytime and overnight temperatures and moon illumination, although
these variables can only explain 26% of the variation in nighttime activity levels. Ultimate
factors of cathemerality likely include thermoregulation and predator avoidance. Food
availability was not found to be an ultimate factor, per se, although I suggest that cathemeral
feeding may allow animals to meet basic caloric needs. If this were true, diet would play an
adaptive role in cathemerality. It remains unlikely that lemur cathemerality is a result of
evolutionary disequilibrium, as proposed by van Schaik and Kappeler (1996). Since unaccounted
nocturnal activities could greatly affect our interpretations of L. catta ecology, future work
should at the very least monitor the amount of time animals are active at night, but we also need
much more data on nighttime behavior, activity budgets, and nutritional profiles. Furthermore,
given the potential importance of cathemerality on lemur ecology, cathemeral behavior should be
investigated further in any species in which occasional flexible diel activity pattern has been
reported. This information would be particularly pertinent for Varecia variegata variegata,
which along with L. catta, has been regarded as diurnal, but has also been reported as nighttime
active (Morland in Hoffmann et al., 1992; Balko in Wright, 1999; Britt in Donati and
Borgognini, 2006). If V.v. variegata was cathemeral along with Eulemur, Hapalemur and now
Lemur, parsimony would predict that the ancestral state of the Lemuridae clade is also
cathemeral. This knowledge could advance our understanding on the evolution of flexible 24-hr
activity patterns in lemurs, and therefore other mammals, given their shared physiology and
Chapter 4: Patterns of climate and weather in southern Madagascar, along with Lemur
catta plant food use.
Strong seasonality, erratic rainfall, frequent cyclones, and cyclical droughts are
characteristic of the climate and weather of Madagascar (Dewar and Richard, 2007). These
climatic events have been suggested as primary proximate mechanisms shaping traits in the
islands' flora and fauna (Dewar and Richard, 2007). For instance, lemur reproduction is timed
such that females are pregnant, and at least begin lactating during the driest parts of the year,
when food resources are reduced (Jolly, 1984; Wright, 1999). During these times, lemur females
rely primarily on small burst of flowers and leaves, and in gallery forests, on tamarind fruits
(Sauther, 1994, 1998). Through synchronous and seasonal reproduction, females begin weaning
their infants at the time of year which coincides with the highest food availability and infants are
thus given the best possible chances of survival during this critical life stage period (Jolly, 1984;
Wright, 1999).
This chapter examines the climate in southern Madagascar and at Tsimanampetsotsa
before and during the time of this research, which then sets the stage for understanding plant
phenology, and whether or not plant foods are seasonally limited for ring-tailed lemurs.
Southern Madagascar climate and weather
Madagascar's climatic features are often regarded as unusual, when compared to other
landmasses, due in part to the island's large size, latitudinal expanse and topographic diversity
(Jury, 2003). Southern Madagascar's climate alternates between a short, hot, wet austral summer
and a long, cool and dry austral winter. Temperatures during austral summer days can be well
over 40°C, while austral winter night temperatures near 0°C. Cyclone season mirrors the austral
summer wherein an average of seven significant storms hit Madagascar every year (based on
data from 1920-1975 [Donque, 1975; Goodman 1995]). On average, 80% of these annual storms
originate in the east and most affect the east coast, however, approximately 20% originate west
of Africa and have the most impact on Madagascar's southwestern coast (Wright, 1999).
Additionally, storms originating in Madagascar's east often continue on a trajectory that includes
the south, although the severity is generally reduced after initial touchdown.
Rainfall in southern Madagascar varies between approximately 300 and 900mm per year,
although these tend to vary greatly. Richard and Dewar (2007) note that rainfall patterns,
particularly those in western Madagascar are unpredictable both inter- and intra-annually. Severe
droughts also occur in Madagascar and some suggest droughts are part of cyclical patterns
(Sauther, 1991; Gould, 1992; Jolly, 1998; Sauther, 1998; Gould et al., 1999). Prior to 1999,
drought years recorded in Betioky (25km southwest of BMSR), include: 1949, 1957, 1959, 1964,
1976, 1982, and 1991-1992 (Gould et al., 1999). Serious drought conditions in southern
Madagascar and El Nino periods appear to occur simultaneously, and droughts also tend to linger
in years after El Nino (Jury, 2003). Furthermore, the International Disaster Database (2012)
suggests that between 1900 and 2012 there were an average of 0.16 droughts per year in
Madagascar. In other words, on average, southern Madagascar can expect a significant drought
once every 6.25 years.
Cyclones in southern Madagascar can result in massive destruction in Madagascar's
forests. In January 2005, cyclone Ernest hit BMSR, and resulted in flooding, defoliation, tree
knock-downs, soil erosion, and a fruiting failure within tamarind trees (LaFleur and Gould, 2009;
Whitelaw, 2010). This storm, and associated reduction in forest foods, appeared to impede the
ability of female ring-tailed lemurs to conceive, and impact the survivorship of infants that were
born (Sauther, unpublished data).
Cyclones, but particularly drought, appear to negatively affect animal survivorship,
through a reduction in water and food resources. Gould et al. (1999) describe the bottleneck
effects of widespread drought on ring-tailed lemur populations, and note that in the second year
of the 1991-1992 drought 80% of all infants and 20.8% of adult females died. Furthermore, in
the following year, 57% of juveniles died and an additional 29.9% of adult females died. It
wasn't until the 4th year following the drought that L. catta populations began to show signs of
recovery (Gould et al., 1999). Southwestern Madagascar's habitat is harsh and difficult to begin
with, but coupled with several annual cyclones and serious droughts which occur approximately
every 6 years, results in an extremely challenging environment to survive in.
Ring-tailed lemur feeding and important foods
The availability of plant foods in southern Madagascar fluctuates dramatically according
to season. Only a select few plant genera have the ability to maintain productivity during the
long dry seasons, and thus there is a significant reduction in plant foods available during dry
periods. However, once seasonal rains commence, many forest plant species are almost
immediately productive and for a period of time there is an abundant and diverse array of plant
foods available.
Ring-tailed lemurs are flexible foragers that consume ripe and unripe fruits, young and
mature leaves, leaf stems, flowers, soil, dead wood, termite casts, insects, and in very rare
occasions, vertebrate prey (Jolly, 1966; Sussman, 1972, 1974; Budnitz and Dainis, 1975;
Sussman, 1976; Sauther, 1992; Rasamimanana and Rafidinarivo, 1993; Sauther, 1998;
Yamashita, 2002; Simmen et al., 2003, 2006). The number of plants species fed on by ring-tailed
lemurs at a given time can be diverse and varies according to time of year and location. For
example, at BMSR, ring-tailed lemurs consume 40 different leaf species, 28 fruit species and 16
flower species, whereas at Berenty, they consume 82 different leaf species, 40 fruits and 38
flowers (Simmens et al., 2006). However, since ring-tailed lemurs use plant resources as they
become available, the total number of species consumed during a given time period tends to be
largely dominated by far fewer species (Sauther 1992, 1998; Simmen et al., 2006). When
accounting for newly introduced species (such as those in the tourist areas of Berenty) and
tamarind, ring-tailed lemur diet tends to focus on 15 or less plant species at a time (Sauther 1992,
1998; Simmen et al., 2006). However, if tamarind and introduced plant species are not present or
not included in this tally, the diet tends to be dominated by three or less species at any one time
(Sauther 1992, 1998; Simmen et al., 2006).
Though generally a trait reserved for species in temperate climates, the vast majority of
lemur reproduction is strictly seasonal, and is induced by changes in photoperiod (van Horn and
Resko, 1977; Petter-Rousseaux, 1980). In some genera, such as those within the Lemuridae,
reproduction in groups is synchronized to within a week or two of surrounding groups (Richard,
1974; Pereira, 1991; Sauther, 1991; Wright, 1995; Pereira, 1998; Wright, 1999). Moreover,
synchronous reproduction is deeply ingrained within lemur life history, and is maintained in
lemurs even when they are in captivity and far from Madagascar, which is not the case for any
other primate group (Rasmussen, 1985).
Lemur catta reproduction is highly tied to seasonal resources within gallery forest
habitats such as BMSR or Berenty (Jolly, 1984; Sauther, 1992; Rasamimanana and Rafidinarivo,
1993; Sauther, 1993, 1998; Sauther et al., 1999: Yamashita, 2002), and females are in late
gestation during the driest parts of the year (July-September), which has correspondingly low
food availability (Sauther, 1994, 1998; Sauther et al., 1999). Furthermore, at Berenty and BMSR
early lactation occurs at the onset of the wet season (October-November) and late lactation and
early weaning occurs well into the wet season (January-April), which is normally associated with
food abundance. At this time, all animals exploit increasing food resources (Sauther, 1994, 1998;
Sauther et al., 1999). Furthermore, weanlings’ chances of autonomous survival are increased
through “weaning synchrony” wherein weaning coincides during the time of year with the most
predictably abundant food resources (Jolly, 1984; Sauther, 1994; Wright, 1999). Reproductive
females in gallery forests rely heavily on a few key species (e.g. Tamarindus indica, Maeurua
filiformis, and Quivisianthe papinae), which tend to be either consistently available or likely to
produce short bursts of large quantities of foods during critical times (Sauther, 1994, 1998;
Sauther et al., 1999).
In the few other habitats where ring-tailed lemurs have been studied, we see similar
trends of reproduction and plant food use. For example, Kelly (2011) found that the diets of ring-
tailed lemurs groups in Cap St. Marie, who's habitat is distinctly populated by stands of Opuntia
monacantha, were similar to gallery forest ring-tailed lemurs' in species diversity, general food
type and composition. Furthermore, these lemurs used the fruits of O. monacantha throughout
the year and were able to sequester both nutrients and important water resources from the fruits.
Gould (2011) noted that in fragmented gallery and spiny forest patches, ring-tailed lemur relied
on a few key species of plants during lean times. Furthermore, many of the plant species used
during the driest times of year are also those used by ring-tailed lemurs in the gallery forests of
BMSR and Berenty including: Gyrocarpus americanus (flowers leaves, fruits), Metaporana
parvifolia (young leaves), Tamarindus indica (fruit, leaves), Alluaudia procera (flowers, leaves),
mixed liana (young leaves), and Salvadora angustifolia (young leaves and flower bundles).
Gallery forest ring-tailed lemurs and tamarind
Tamarindus indica is of particular importance to gallery forest-residing L. catta asyoung
leaves, flowers, and fruits are produced asynchronously throughout the year at riverine gallery
forest habitats (Sauther, 1998), thus making them available year-round for consumption
(Simmen et al., 2006; Irwin, 2008). As a member of the family Fabaceae, tamarind fruits are
protein-dense and provide a rich source of energy (Morton, 1987). Young tamarind leaves and
flowers are also important to L. catta diet as they too provide a readily digestible protein source
(Sauther, 1993; Mertl-Milhollen et al., 2003). Furthermore, tamarind foods usually comprise
upwards of 35-60% of gallery forest ring-tailed lemurs’ diet (Rasamimanana and Rafidinarivo,
1993; Mertl-Milhollen et al., 2003; Soma, 2004; Koyama et al., 2006). Fruits are ripe during the
driest parts of the year and provide high-energy foods to females who are gestating or lactating,
and infants as young as two months feed on and lick tamarind pods (Simmen et al., 2006).
Because of the dietary importance of T. indica to L. catta at the BMSR as well as the large
number of tamarind trees in this forest, Yamashita (2002) suggests that all other foods are
Several authors use the definition of a "fallback food" for any food for which there is a
significant negative correlation between its use and the abundance of other foods (Marshall and
Wrangham, 2007; Marshall et al., 2009; Sauther and Cuozzo, 2009). Fallback foods are often
thought to be influential in primate morphology, and particularly dental morphology, since they
influence adaptive shifts during critical periods (e.g. Lambert et al., 2004; Laden and Wrangham,
2005; Vogel et al., 2008; Strait et al., 2009). Du Puy et al. (2002) suggests that the importance of
tamarind foods to gallery forest ring-tailed lemurs implies an adaptation to consuming a
disproportionate amount of T. indica. However, Sauther and Cuozzo (2004, 2006, 2009)
associate severe and premature dental wear and attrition with tamarind fruit use in ring-tailed
lemurs at Beza Mahafaly. Similar wear and attrition has been found in Berenty ring-tailed
lemurs, where tamarind is also the dominant gallery forest tree species and ring-tailed lemur
fallback food (as noted by Crawford [Sauther and Cuozzo, 2006]). Yamashita's (2008) work
showed that tamarind fruits are the hardest and toughest foods consumed by ring-tailed lemurs at
BMSR, and since the lemurs use their teeth to crack and chew the hard casing of the tamarind
fruits, these data lend further support to Sauther and Cuozzo's (Cuozzo and Sauther 2004, 2006,
2009) linkage of tamarind fruit consumption and the ring-tailed lemurs' dental pathology.
Moreover, this work is further supported by the facts that dental pathologies are not found in the
sifaka (Propithecus verreauxi) at Beza Mahafaly or in ring-tailed lemurs at Tsimanampetsotsa.
The sifaka choose younger, softer fruits, and the Tsimanampetsotsa ring-tailed lemurs only
occasionally consume tamarind fruits (Cuozzo and Sauther, 2004, 2006; Yamashita, 2008;
Sauther and Cuozzo, 2009). Though very important to gallery forest residing ring-tailed lemurs,
the current evidence suggests that the lemurs are not morphologically adapted to consume large
quantities of tamarind, given the detrimental biological effects (but see DuPuy et al., 2002).
The goal of this chapter is to describe the climate and weather patterns bracketing the
study period, and through measures of phenology, to determine if seasonality limits food
resources for ring-tailed lemurs. Seasonal (or stochastic) restriction of resources is the first
assumption of the Energy Conservation Hypothesis that is tested by this research, and
understanding if/how resources are limited to lemurs should provide insight into the unusual
lemur traits, including female dominance.
Climate and weather patterns
TNP generally receives less that 400mm of rain per year, with the majority of rainfall
occurring between late December and February. During the study period, a total of 232.9mm of
rain were measured (Table 4.1). The rain in February coincided with Cyclone Bingiza, which hit
the northeast coast of Madagascar on Feb 14, 2011 and the southwest on Feb 17, 2011 (Figure
4.1). The intensity of the cyclone was dramatically reduced on the west coast, however within a
30 hour period between February 17 and 18, 2011, TNP received more than 125mm of rain. This
rain caused a flash flood at the TNP camp, but did not cause significant tree damage or
defoliation within the study area.
Figure 4.1. Amount of rainfall at TNP between September 2010 and March 2011.
Rain (mm)
Figure 4.1. Map of the trajectory of Cyclone Bingiza (UNCT Madagascar).
Phenology and food availability
Seasonal food availability changed dramatically over the study period (Figure 4.2-4.3;
Table 4.2). At the onset of the study (August of 2010), mature leaf coverage was below 40%, but
at the end of the study period (April 2011) coverage surpassed 80%. Young leaf availability
peaked once (December 2010 through January 2011), while flower availability peaked twice
(once in November 2010 and again in January 2011). Fruit availability also peaked twice, with
some fruits available in November (2010) and others in January through March (2011).
Table 4.2. Average percentage of tree coverage on all phenological transect lines during the
study period.
Mature leaves
Young leaves
Plant part
Percentage of tree coverage
Figure 4.2. Availability of fruits, flowers, young leaves, and leaves
during the study period.
Figure 4.3. Photos taken of the same areas (angles vary somewhat) during the dry season (left)
and wet season (right).
In addition to transects, I monitored all tamarind and fig trees (with a diameter at breast
height over 10cm) within the two focal lemur group’s overlapping home ranges. In total, there
were 59 T. indica and 96 Ficus megapoda trees within this area. With the exception of one
tamarind tree on the Mahafaly plateau (zone 3), tamarinds were only present at the base of the
Mahafaly plateau or "zone two" as described in Chapter 2: Methods. Though T. indica trees in
southwestern Madagascar are generally asynchronous within gallery forests and noted for their
ability to provide gallery forest ring-tailed lemurs with food year-round (Sauther 1992, 1994),
the trees in this study appeared seasonal. During September and October tamarind trees had ripe
fruit and mature leaves (see Figure 4.4). Shortly after there had been 6.3mm of rain in late
October a few tamarind trees produced flowers, but these flowers did not seem to result in any
fruits. By November there were little-to-no fruits remaining and trees rapidly lost all of their
leaves and became completely defoliated. In late December, trees regained their leaves, and these
leaves matured quickly. In late March, flowers began to appear. Trees were not monitored after
the study period, though one would presume after flowering in March and April, fruits would
mature and be again ripe in September. Local people confirmed that synchrony was the normal
pattern for tamarind at TNP.
Ficus megapoda trees were distributed throughout zones 2 and 3 of the lemurs' home
ranges. These trees did fruit asynchronously and provided bursts of ripe fruits throughout the
study period (Figure 4.5). Most notably, the large fig tree that the Vintany group slept in
produced great quantities of fruits during two separate periods, while another fig tree ("Fig 3")
produced a large amount of fruits in late October and early November. These fruiting events
attracted many frugivorous/herbivorous animals including lemur groups, a host of bird species,
tortoises, and insects. When fig trees within the territory produced large quantities of fruits, the
lemur groups would visit the trees several times daily to selectively feed on ripe fruits.
Throughout the study period, there was continuous availability of figs (F. megapoda and F.
marmorata), though the quantity and quality varied.
Figure 4.5. Ficus megapoda fruits.
T. indica flowers
T. indica young leaves
T. indica fruits
F. macropoda fruits
Plant and food part
Availibility (0-1, where 0 is none and 1 is abundant)
Figure 4.4. Availability of T. indica and F. megapoda foods
Foods consumed by focal animals
During the study period, focal ring-tailed lemurs were observed consuming two types of
unidentified insects (one species of large arthropod and one or possibly two species of
caterpillar), along with 69 plant parts originating from 53 known and 7 unknown different plant
species (See Appendix 2 for a complete list). As with previous studies (Sauther 1992, 1998),
animals at TNP consumed foods as they became available, and the composition of the diet varied
from month to month (Figure 4.6). During September to late December the average number of
species consumed per month by focal animals was 6.7, while from January to April the average
number of species consumed per month was 11.1. Plant species and part, and the relative amount
that animals consumed per month are listed in Table 4.3. For each month, the highest percentage
of feeding time was spent on the following: September, Neobeguea mahafaliensis, flowers, 94%;
October, Gyrocarpus americanus, flowers, 57%; November, G. americanus, fruit aril, 43%;
December, Alluaudia comosa, flowers, 44%; January, Pentarhopalopilia madagascariensis and
other species of liana, young leaves, 21%; February, F. megapoda, fruit, 57%; and March, P.
madagascariensis and other species of liana, young leaves, 35%. Of all of the focal feeding data
collected, animals spent 10.9% of their feeding time consuming figs and less than 1% of their
feeding time consuming tamarind foods. Neobeguea mahafaliensis flowers, G. americanus
flowers and fruit arils, and A. cosmosa flowers fit the definition of fallback foods, as the
consumption of these foods negatively correlated to availability of other same type foods. The
use of F. megapoda fruits by ring-tailed lemurs in this study doesn't fit cleanly into any of the
operationalized definitions of food resources, as specified by Marshall and Wrangham (2007).
Figs are almost always available, though the quantity and quality vary. The lemurs over-
exploited F. megapoda fruits when there was one particular tree within their range that had an
enormous amount of ripe fruits. This happened in October when the fruits of Gyrocarpus were
plentiful (although the lemurs only ate the fruit aril of Gyrocarpus and not the entire fruit) but no
other fruits available, in December when few other fruits were available, and in February, which
was one of the months with highest food availability. Though figs tend to be a regular food
source of relatively low nutritional content (see Chapter 5), in times of mast fruiting of one tree,
figs appeared to be a preferred food (October and February), a fallback food (December), and a
staple food in other months. Overall, female lemurs consumed significantly more leaves (t=
6.353, df=2, p=0.0120), when compared to males, and both males and females fed on insects
during the wet season but not the dry (t=-4.556, df=2, p=0.0220). There were no other significant
differences found in the type of food eaten by lemur sexes or groups, or between seasons.
Table 4.3. Percentages of plant species and plant part that contributed 1% or more of the total
amount consumed by ring-tailed lemurs during each complete month of the study period. The
most consumed species per month are in bold.
Adansonia rubrostipa
Alluaudia comosa
Cedrelopsis grevei
Commiphora simplicifolia
Didierea madagascariensis
Diospyros manapetsae
Euphorbia plagiantha
New growth
Euphorbia stenoclada
New growth
Ficus marmorata
Ficus megapoda
Gyrocarpus americanus
Gyrocarpus americanus
Fruit aril
Gyrocarpus americanus
Gyrocarpus americanus
Young leaves
Neobeguea mahafaliensis
Neobeguea mahafaliensis
Neobeguea mahafaliensis
Young leaves
Olax androyensis
madagascariensis and other
species of liana
Young leaves
Poupartia minor
Young leaves
Tallinella grevei
Voharanga madagascariensis
New growth
Xerophyta dasylirioides
Ximenia perrieri
Zygophyllum depauperatum
*Scientific name used unless unknown.
There was a marked lack of both lemur plant foods and non-lemur plant foods during the
dry portion of this study. It appears as though TNP has an even more restricted wet season and
receives less annual precipitation, when compared to the well-studied ring-tailed lemur habitats
in southern Madagascar. The following examines the effects of reduced rainfall on phenology,
and in turn, the effects of low rainfall on ring-tailed lemurs.
During years without disrupting droughts or cyclones, the annual rainy season in southern
Madagascar occurs between November and March (Sussman et al., 2012). At BSMR average
rainfall measures 700mm (Sussman et al., 2012), while data for Berenty range is between 300-
900mm (Jolly et al., 2012). Kelley (2011) notes 695mm of rainfall during a one-year period at
Cap Sainte Marie, but interestingly, this area received rain every single month. Moreover, at all
of these sites infant ring-tailed lemurs are born in late September and early October. At TNP,
infants were also born in late September, but there is a marked decrease, at this site, in the
amount and duration of rainfall. Annual rains begin in December (usually late December) and
cease in February, with most of the year’s total rainfall measuring significantly less than 400mm
(Donque, 1975). Though weather patterns are highly variable, what these sites do have in
common is a generally predictable abundance of food at the onset of lemur infant weaning,
which occurs in January. This pattern of infant weaning with most predictable food resources
appears to be deeply engrained in the life histories of ring-tailed and many other lemur species.
The effects of cyclones and droughts on lemurs depend on the severity and duration of
the storm or drought. During this study, cyclone Bingiza brought a large amount of rain
(125mm) in a short period of time (30hrs), but it did not appear to be physically destructive to
the habitat, or to adversely affect the lemurs. However, the full effects of natural disasters may
not be evident until the years following the event. For example, in 2005, following cyclone
Ernest, massive defoliation and tree knock-downs occurred at BMSR, and for at least seven
months after the cyclone, tamarind trees failed to produce fruits. This cyclone also may have
impacted the ring-tailed lemurs, in that infant survivorship was reduced over the following two
birth years (Sauther, unpublished data). Moreover, during the 1991-1992 severe droughts in
southern Madagascar, Gould et al. (1999) detail significant mortality rates in ring-tailed lemur
females and infants at BSMR. Pavelka et al. (2007) describe similar long-term effects of
hurricanes on howler monkey populations. These authors point out that hurricanes affect the
monkeys' food supply, diet, and activity (Pavelka et al., 2007). Given that these animals continue
to have elevated rates of mortality long after normal patterns of rain ensue, it appears as though
food supply, rather than water per se, most affects survival of these primates following natural
Both lemur plant foods and non-foods were extremely limited during the dry season at
TNP. As we know, ring-tailed lemurs exploit foods as they become available (Sauther 1994,
1998). During the dry season the number of foods available at any one time was low. Neobeguea
provided an incredible 97% (94% flowers, 3% young leaves) of all recorded food items in the
month of September, and there were several days during this month where lemurs did not
consume any other foods. The flowers and leaves from Neobeguea were important to focal
animals for the following reasons: nutritional content, they became foliated and flowered en
masse, and there were few other foods available. Other plant foods that were of particular
importance to ring-tailed lemurs throughout this study included G. americanus, A. comosa, F.
megapoda, and P. madagascariensis and other species of liana. Gyrocarpus was an important
food during November and December and focal animals consumed flowers, fruit arils, and young
and mature leaves. Gould et al. (2011) also noted G. americanus young fruits as a ring-tailed
lemur plant food, but I did not witness any consumption of the actual fruiting body. In fact, focal
animals seemed to go out of their way to discard fruits, while feeding on fruit arils. In the
analyses by Gould et al., (2009), concentrations of condensed tannins found in G. americanus
fruits were more than seven times the concentration found in flowers, fruit arils, or leaves, which
may explain why TNP animals avoided them, although it is unclear why the Berenty animals
would consume the fruits. Alluaudia flowers were an important food source during November
and December, and it is worth noting that the trees were also physically important to focal
animals, in that their umbrella-like shape and thick canopy provided shady refuge for the lemurs
during particularly hot periods when temperatures surpassed 45°C.
As per the definition of Sauther and Cuozzo (2009), N. mahafaliensis, G. americanus,
and A. comosa were all fallback foods to the TNP lemurs, as there were negative correlations
between the intensive use of these species and the abundance of other foods. Ficus sp. were also
important foods during this study as they provided ripe fruits during every calendar month and
were the only species to do so. The relationship of fig fruit use by ring-tailed lemurs at TNP is
somewhat more complicated than that of other foods. The lemurs tend to over-exploit figs when
there was a mast fruiting event of one fig tree within their home range, and their use of these
fruits could be classified as fallback, preferred, or staple, depending on the time period and what
other foods were available. It is also possible that these food classifications are not adequate or
accurate in describing the patterns of use by ring-tailed lemurs. Ficus megapoda fruits are not a
particularly high quality food and may be difficult for the lemurs to digest (see Chapter 5),
however, the ease to which they can be obtained in a heavily fruiting tree appears to be an
attractive quality to the lemurs, and many other species of animal at TNP (birds, tortoises,
insects), regardless of the availability of other fruits, which would not have been as spatially
clumped as the fig fruits. Fig fruits are esteemed for their importance to frugivorous species
world-wide (Terborgh, 1986), and their importance to animals in this research will be addressed
further below. The last foods noted to be an important seasonal resource in this study includes
the young leaves from P. madagascariensis and those from other lianas, which were ample
during both January and March. Though high in fibrous matter, these leaves were an excellent
protein source and contain little secondary compounds, which likely made them attractive, low-
cost food sources. From the aforementioned species, both lianas and G. americanus have been
noted to contribute to the diets of ring-tailed lemurs in other habitats. Gyrocarpus is an important
seasonal food for ring-tailed lemurs at Beza (Sauther, 1998; Yamashita, 2002) and is also
important for the ring-tailed lemurs in spiny forest fragments outside of Berenty (Gould et al.,
2011). Figs are an important component of the Andringitra mountain range ring-tailed lemurs dry
and wet season diets, and they spend 6.6% and 14.0% of their feeding time consuming fruits,
respectively, over these seasons (Simmen et al., 2006). When comparing top quartile or
seasonally important foods from the study period, G. americanus, liana leaves, and fig species
appear to be the only overlapping food species between TNP and all other ring-tailed lemur
study sites.
Ficus spp. have been noted as part of the ring-tailed lemur diet at Beza, Berenty, Cap. St.
Marie, and in the Andringitra mountain range (Simmens et al., 2006). Most of the fruits
consumed in these locations, such as those from F. marmorata, are from small shrub-like bushes,
that don't tend to produce vast quantities of fruits at any one time. Koyoma et al. (2006) note that
F. megapoda occur at Berenty (they include 6 individual trees within their habitat census), but
there is little information on if and in what manner the ring-tailed lemurs use resources from
these trees at Berenty. In this research, lemurs used figs during every month of the study period
and consumed large quantities from F. megapoda, when they were available. During February
2011, F. megapoda constituted 57% of the lemur’s diet. Figs are noted to be depauperate in
Madagascar, which is thought to be one of the factors contributing to Madagascar's low frugivore
diversity, particularly in birds (Langrand, 1990; Mittermeir et al., 1994; Goodman and Ganzhorn,
For the purposes of this research, it is important to know if these figs are endemic to
Madagascar, and if not, the length of time that ring-tailed lemurs and figs have been co-existing.
Machado et al. (2001) note that the separation of India and Madagascar, which occurred about 80
million years ago, coincided with the timing of the radiation of groups of wasps that pollinate
flowers from the subgenera Urostigma (which includes F. megapoda), Sycomorus, Ficus and
Sycidium. Machado et al. (2001) further state that Ficus and its pollinators could have dispersed
by drifting with the fractured continents or by rafting, and that either scenario is consistent with
the paleontological data (Sahni, 1984; Briggs, 1987). However, both Machado et al. (2001) and
Goodman and Ganzhorn (1997) suggest that the lack of endemism of figs on Madagascar along
with the high levels of endemism of other Malagasy species suggests a relatively recent
introduction. We know that F. megapoda is not one of the historically introduced fig species,
because there have been leaf imprints found in Benenitra, from alongside the Onilahy river
which date to at least the early Quaternary (Perrier de la Bâthie, 1928). Lemurs' historical use of
figs and whether F. megapoda is endemic or an introduced species on Madagascar, would help
in understanding to what degree lemurs have relied on these fruits in the past.
The findings that ring-tailed lemurs exploit available fig fruits is not surprising. What is
surprising is that foods from tamarind trees were infrequently incorporated into the diets of these
animals. There are a few explanations for why the ring-tailed lemurs at TNP use tamarind foods
infrequently. First, in gallery forests, the availability of foods from tamarind trees are
asynchronous (Sauther, 1994). As such, throughout the year, there are almost always tamarind
trees that have young leaves, flowers, and/or fruits available (Sauther, 1994). So, these trees are a
reliable food source for lemurs, even in the dry season. This did not seem to be the case at TNP.
The phenology of tamarind trees at TNP was highly synchronized (Figure 4.3), and although the
lemurs did consume some tamarind foods when they were available, their total amount of
feeding time dedicated to tamarind was < 1%. Second, at TNP figs appeared to be the only
asynchronous food that was available during every month of the study (Figure 4.3). The lemurs
did exploit ripe fig fruits frequently, and spent 16% of the total observed feeding time consuming
figs. Third, fig fruits are substantially easier to process mechanically, compared to tamarind
fruits. Pods of ripe tamarind fruits are very hard and inedible, and biting through this exocarp has
been related to extreme tooth wear in the Beza Mahafaly ring-tailed lemurs (Sauther Cuozzo,
2004, 2006; Yamashita, 2008; Sauther and Cuozzo 2009). Figs, on the other hand, are soft and
fleshy and do not require manipulation prior to being consumed. During the months of Sept-Nov
2010, both tamarind fruits and figs were available in the lemurs home ranges. Animals spent
2%, 6%, and 19% of their feeding time consuming figs during these months, but less than 1% of
their time consuming tamarind fruits, which suggests that the TNP lemurs prefer fig fruits to
tamarind pods. Though the known dates of introduction of F. megapoda and T. indica are
ultimately unknown, given the current evidence, it appears as though F. megapoda has a longer
evolutionary history in Madagascar, when compared to that of T. indica. If TNP is the type of
habitat that ring-tailed lemurs are primarily adapted to, it is possible that when ring-tailed lemurs
dispersed throughout southern Madagascar via river ways (Goodman et al., 2006), they also
acted as seed dispersers for both T. indica and F. megapoda. Both fig and tamarind species need
access to a certain amount of ground water to survive. However, given that Ficus species are less
tolerant of certain soil types (Swagel et al., 1997), it would be much less likely that figs would be
as readily distributed so widely, whereas tamarind is much more tolerant in reference to soil
(Gillman and Watson, 1994). This would help explain the near lack of large fig trees in southern
Madagascar's gallery forest, along with the dominance of tamarind trees. That being said, further
data are needed before we can decide when and how these plant species dispersed in southern
Madagascar. Use of different plant species than previously known for L. catta, exploitation of
figs, and the unusual near exclusion of tamarind foods in the TNP ring-tailed lemurs further
exemplifies the extreme flexibility of this species.
Southwestern Madagascar is highly seasonal, and although weather patterns are erratic
and unpredictable, natural disasters such as cyclones and drought are frequent and common.
Weather patterns directly impact primary productivity, even in dry adapted forests, and limited
or unpredictable primary productivity is thought to be important in the unusual adaptations found
in Madagascar's primates. This research was the first to document ecology of ring-tailed lemurs
in an intact spiny forest. Neobeguea, Alluaudia, and Gyrocarpus, and figs all served as fallback
foods. These ring-tailed lemurs, surprisingly, incorporate very little tamarind into their diets,
which may be because the tamarind trees at TNP are seasonal in leaf coverage, flowering and
fruiting, or because these lemurs have access to figs, which are comparably easier to consume.
Chapter 5: Feeding ecology and nutrition of Lemur catta at the Tsimanampetsotsa National
In Chapter 4 we saw that there are far less of plant foods present during southern
Madagascar's long dry season. The question that still remains, however, is whether this reduction
in overall plant food availability translates into a reduction of nutrients or calories consumed by
lemurs (Yamashita, 2008). Previous research has noted differences between lemur female and
male feeding behavior, such as plant part chosen and/or amount of time spent feeding, and these
differences are thought to reflect the differential reproductive metabolic needs of female and
male lemurs (Sauther 1994, 1998). However, nutritional data have been either lacking or provide
no or weak support for the hypotheses (see Sauther 1994, 1998; Curtis, 2004; Yamashita 2008).
Several authors have suggested that future research should examine gross amount consumed
when comparing dietary components of lemur nutrition (Curtis, 2004; Yamashita, 2008). This
chapter will explore the interspecific response of ring-tailed lemurs to variability in the
availability of plant foods, along with caloric and nutritional profiles, activity budgets, and stress,
in order to understand the degree to which ring-tailed lemurs may partition ecological niches
between the sexes.
Sex based feeding differences
In gallery forest ring-tailed lemurs, both seasonal and sex differences in feeding have
been documented. At Beza, pregnant females consume more flowers and fruits, while males
consume more leaves (Sauther, 1994, 1998). Once lactating, females focus on consuming young
leaves which contain elements that are important for lactation, such as calories, protein, and
calcium, presumably, without large quantities of secondary compounds which can interfere with
digestion (Sauther, 1994, 1998). At Berenty, pregnant females fed heavily on mature tamarind
leaves and unripe tamarind fruit and then once lactating, these same females became increasingly
frugivorous (Rasamimanana and Rafidinarivo, 1993). Unripe tamarind fruits and mature leaves
contain considerable secondary compounds, which we would expect females to avoid, but
Rasamimanana and Rafidinarivo (1993) suggest that in this case, females are exploiting the high
protein content found in these foods.
These sex based differences in food selection and diet are hypothesized to aid females in
securing sufficient resources to feed their rapidly growing young (Lee, 1996; Dufour and
Sauther, 2002; Gould et al., 2003). Protein (or rather, the amino acids found in protein) and
calcium have been noted as particularly important dietary components to reproductive mammals,
as they are required in physiological processes ranging from DNA replication and cell division to
bone deposition and hair growth (Ullrey et al., 2003; National Research Council, 2003). That
being said, the current data on intraspecific lemur nutrition are all but lacking, and for those data
on interseasonal differences in the diets of lemurs that have been explored, the data does not
always support hypotheses proposed based on lemur feeding data. This topic will be further
explored next.
Diet and nutrition
We know that Madagascar's forests are seasonal, particularly in the west and
southwestern dry forests. However, an overall reduction in flora does not necessarily result in a
proportional reduction in lemur plant foods or nutrients, since lemur plant foods are only a subset
of the total plant biomass in the forest, and because lemurs exploit seasonal foods as they
become annually available (Sauther, 1994, 1998). In her analyses of gallery forest lemur (L. catta
and Propithecus verreauxi) nutrition, Yamashita (2008) found that although there was a marked
reduction in food availability in the dry season, nutrient intake (protein, sugars) was balanced
between the wet and dry seasons. Furthermore, Yamashita (2008) notes that although the
quantities of nutrients and contributing plant parts differ throughout the year, neither sifaka nor
ring-tailed lemurs appear to be nutrient starved. Similarly, in her analyses of gallery forest
Eulemur mongoz dietary nutrients (amino acids, lipids, carbohydrates) Curtis (2004) found vast
differences in seasonal food availability, but little interseasonal difference in nutrient intake, and
suggested that the lemurs' nutritional requirements were being met throughout the year. Although
food resources are reduced, these lemurs appear to exploit resources such that their nutritional
requirements are met during the wet and dry seasons (Curtis, 2004; Yamashita, 2008). Through
these data both authors concluded that there was not a maximal exploitation of foods during
periods of abundance, or that seasonality induces nutritional stress (Curtis, 2004; Yamashita,
Although nutrients were balanced between the seasons in the aforementioned studies,
Curtis (2004) and Yamashita (2008) point out that calories are likely not balanced due to the
reduction in overall food intake, along with the visible reduction in lemur body weight during the
dry season. It is also possible that seasonal nutrient differences were not found in these studies
because of the presence of tamarind trees (see Yamashita, 2008). At both of these study sites T.
indica trees are the most common or at least a very common species throughout the habitats. As
such, the aforementioned findings may be more reflective of E. mongoz, L. catta, and P.
verreauxi when consuming a tamarind dense diet, which we know influences feeding patterns in
Gould et al. (2011) examined nutrients and calories for reproductive female and male
ring-tailed lemurs in the gallery and spiny forest fragments surrounding Berenty. This research
spanned approximately two one-month periods during which the female lemurs were in early to
mid lactation (2006) or early gestation (2007) (Gould et al., 2011). These authors found no sex
differences in feeding behavior, nutrients, or calories consumed. In fact, the only significant
difference found by Gould et al. (2011), was that spiny forest females tended to rest more than
gallery forest females. The presence of tamarind fruits in the lemurs' diet may account for some
of the findings, however, Gould et al. (2011) suggest that the lemurs' overall food availability
may have played a role, given that the previous year had lower than average rainfall. LaFleur and
Gould (2009) note an absence of feeding or nutritional differences in the diets of BMSR ring-
tailed lemurs during a complete tamarind fruiting failure and suggest that sex based differences
may cease when foods reach a critical low point. Gould et al. (2011) do not provide phenological
data, and it is therefore difficult to decipher if the ring-tailed lemur plant foods were at critically
low levels.
In the biomedical evaluations of ring-tailed lemurs at Cap Sainte Marie, Kelley (2011)
found no evidence of dehydration or malnourishment in focal animals. These lemurs live in
highly anthropogenically altered habitats, and depend on O. monacantha cactus hedges for both
shelter, food, and water. Interestingly, Kelley (2011) notes that although the sleeping sites of
focal animals were within agricultural fields or gardens, crop raiding was extremely rare.
Furthermore, in contrast to ring-tailed lemurs at BSMR, Kelley (2011) did not witness any
consumption of cooked human foods, cattle forage, or intraspecific coprophagy. We might
expect that lemurs living in highly disturbed areas with would show signs of adverse health, poor
diet, and/or behavioral adaptations to consuming crop or other non-typical foods, as has been
found elsewhere (MeNon and Poirier, 1996, Umapathy and Kumar, 2000; Irwin, 2006), and even
within ring-tailed lemurs (Whitelaw, 2010). Furthermore, it is surprising that studies focused on
nutrition in ring-tailed lemurs, a species for which we have well documented sex and seasonal
dietary differences (Rasamimanana and Rafidinarivo, 1993; Sauther, 1994, 1998; Simmen et al.,
2006; Soma, 2006), have failed to produce significant differences in the nutritional profiles. It is
possible, of course, that feeding differences documented in these animals do not equate to
nutritional differences, even though behavioral data would suggest so. Conversely, it is also
possible that the presence and use of certain foods, such as potentially introduced species such as
T. indica and invasive or sometimes cultivated species like O. monacantha, mask what would be
the "normal" (i.e. what we would expect in the types of habitats that they are adapted to) dietary
profile for ring-tailed lemurs.
Activity patterns and ranging
Seasonal patterns in activity budgets have been found throughout the Malagasy primates
(Wright, 1999; Ganzhorn et al., 2000), including within ring-tailed lemurs (Jolly, 1966; Sussman,
1977; Sauther, 1992; Loudon, 2008; Whitelaw, 2010). These differences have been attributed to
food availability, reproduction, temperature, and sex (Jolly, 1966; Sussman, 1977; Sauther, 1992;
Gould, 2006; Rasamimanana et al., 2006). Gallery forest ring-tailed lemurs tend to rest more
during the dry season, and ring-tailed lemurs in spiny forest fragments tend to rest more than
those in gallery forests (Sauther, 1994; Loudon, 2008; Ellwanger and Gould, 2011).
Furthermore, the amount of time spent resting seems to negatively correlate with the amount of
time spent feeding (Gould, 2006). That being said, reported sex based differences in activity
budget are inconsistent. For example, some authors report no sex differences in the amount of
time spent resting, feeding or locomoting (Simmen et al., 2010; Gould et al., 2011; Kelley, 2011)
while others state that females move and travel significantly more than males (Rasamimanana et
al., 2006). The trend of resting more during the dry season has been interpreted as an energy
effective strategy by ring-railed lemurs, wherein periods of inactivity coincide with periods of
high ambient temperature and low food availability (Sauther et al., 2006; Gould et al., 2011).
Under this reasoning, it is unclear why female lemurs would engage in more active behaviors,
when compared to males. Activity budgets will be examined here, in order to understand the
relative amounts of energy expended by focal animals during different reproductive periods and
Studies of fecal glucocorticoid levels, a common measurement used to monitor stress in
wild animals, have shown that lemur stress varies by species and can be triggered by a variety of
stressors (Cavilgelli 1999; Pride, 2005; Fitchel et al., 2007; Ostner et al., 2008; Starling et al.,
2010). For example P. verreauxi alpha males at Kirindy show significantly elevated fGC levels
in the breeding season, when compared to subordinate males, but during the birthing season, no
rank-related differences are found (Fitchel et al., 2007). Conversely, at the same site, no rank
related differences were found in male Eulemur fulvus rufus, but there is an increase of fCG
during the birthing season (Ostner et al., 2008). In the sifaka, alpha males likely experience
significant stress guarding cycling females during the very short reproductive time period
(Fitchel et al., 2007). In the red-fronted brown lemur, elevated stress during the birthing period
may be in response to threat of infanticide (Ostner et al., 2008). In further comparison, female
ring-tailed lemurs show an increase in fCG levels in response to low rainfall and low tamarind
fruit availability (Cavigelli, 1999), short term food scarcity and large group size (Pride, 2005),
social rank, social instability and aggressive interactions (Starling et al., 2010), and with mating,
pregnancy, and lactation (Cavigelli, 1999; Starling et al., 2010). Given that many of these factors
co-occur (e.g. pregnancy and low food availability), it can be difficult to understand the causal
Coat condition can also be used as a long-term measure of stress, given that prolonged
fGC correlates with poor coat condition (Pride, 2005; Steinmetz et al., 2005). A dull, shaggy, and
dry looking coat in a free-ranging primate is likely an indicator of nutritional or social stress
(Steinmetz et al., 2005). Long-term stress, such as that which is reflected in extended fGC level
elevation or poor coat condition, can be indicators of early adult mortality and ultimately fitness
(Pride, 2005; Romero and Wikelski, 2001). The ring-tailed lemur coat scoring system as outlined
by Berg et al. (2009) was used to assess long-term stress in focal animals of this study, with the
aim of better understanding which of the following stress factors most affected individuals: sex,
reproductive state, dominance rank, and food availability.
Research presented here includes the feeding behavior, nutritional and non-nutritional
components of diet, activity patterns, and estimates of stress from two groups of ring-tailed
lemurs residing at the Tsimanampetsotsa National Park. Data will be used to address the
following questions:
1. Are ring-tailed lemur nutrients or calories seasonally constrained?
2. Do ring-tailed lemurs use behavioral mechanisms to save energy?
3. Is the dry season differentially stressful for female ring-tailed lemurs?
Activity Patterns
The percentages of average daytime activities were calculated from focal animal data
during the dry and wet seasons, and for animal groups and sexes (Table 5.1). Percentages for
sex, season and group were calculated separately after removing any outliers, and thus the total
percentages may differ slightly between categories. Outliers included data points which were
unreasonable (such as daily caloric intake of 1.44Kcal or 4012Kcal) and likely resulting from
measurement error. Significant differences were found for both seasons and sexes. However,
when comparing the ILove and Vintany groups' activities, no significant differences were found
(Table 5.2).
Table 5.1. Activity budgets (average percentage of daytime observation) for lemurs sexes, all
animals across the dry and wet seasons, and lemur groups.
Stink Fight
Misc. (Defecate, drink)
Table 5.2. Student's T-test for differences in the mean amount of time spent in each activity
category by female and male lemurs, all lemurs between the dry and wet season, and the ILove
and Vintany lemur groups.
Misc. (defecate,
N/A= females do not stink fight, only one occurrence of male stink fighting in the dry season.
Data were further categorized according to lemur sex and season, in order to understand
where significant interactions were occurring, if any. Table 5.3 and Figure 5.1a-5.1b show the
percentages of average daytime activities for female and male lemurs in the dry and wet seasons.
Significant differences in these data can be found in Table 5.4-5.5. The percentages of time
spent feeding by lemur sexes in each season, were multiplied the average day length (12hr) in
order to determine differences in the number of hours spent feeding per day (Figure 5.2).
Table 5.3. Activity budgets (average percentage of daytime observation) by lemur sex in both
Female Dry
Female Wet
Male Dry
Male Wet
Stink Fight
Other (Defecate, drink)
NA= females do not stink fight
Figure 5.1.a. Activity budgets (average percentage of observed time) of female ring-tailed
lemurs in the dry and wet seasons.
Females Dry Season
Females Wet Season
Figure 5.1.b. Activity budgets (average percentage of observed time) of male ring-tailed lemurs
in the dry and wet seasons.
Stink Fight
Males Dry Season
Stink Fight
Males Wet Season
Table 5.4. Student's T-test for differences in the mean amount of time spent in each activity
category by lemur females and males in the dry and wet seasons.
Female Dry Wet Seasons
Male Dry Wet Seasons
Stink Fight
Misc. (Defecate,
N/A= females do not stink fight, only one occurrence of male stink fighting in the dry season.
n/a = sample size too small
Table 5.5. Student's T-test for differences in the mean amount of time spent in each activity
category during the dry and wet season by female and male lemurs.
Female Male Dry Season
Female Male Wet Season
Stink Fight
Misc. (Defecate,
N/A= females do not stink fight
n/a= sample size too small
The average and maximum distances traveled per day, number of adults in group, and
total home range sizes of both lemur groups can be found in Table 5.6. Additionally, a map of
the two groups' semi-overlapping home ranges can be found in Figure 5.3.
Table 5.6. ILove and Vintany groups average distance traveled per day (meters) and number of
adults in group during the dry and wet seasons, along with maximum day distance (meters) and
home range size (km2) throughout the study period.
Dry Season
Wet Season
Study period
Adults in
Adults in
Max day
Female Dry
Female Wet
Male Dry
Male Wet
Figure 5.2. Significant differences between time average
feeding (average hours/day) for female and male lemurs in
the wet and dry seasons.
Figure 5.3. Aerial satellite map displaying the Vintany and ILove groups semi-overlapping
home ranges.
Nutritional Intake
From foods consumed by the lemurs, one insect sample and 79 plant samples were
analyzed for their nutritional content. Complete nutrient composition along with specific details
of plant part processing (i.e. seed removal, when appropriate) can be found in Appendix 3. Due
to the abundance and diversity of lianas, which were often intertwined and difficult to
distinguish, samples were combined into "mixed liana." The Pentarhopalopilia liana was
analyzed solely because it was the most commonly consumed liana, and easy to identify given its
five-lobed leaves and distinctive smell. Not all foods were analyzed due to factors such as rarity
of consumption, insufficient sample availability, and sample spoilage. However, nutritional
content of foods from varying phases and time periods were analyzed for 51 species of plant,
which constituted 94.5% of the lemurs' diet.
Focal feeding data yielded feeding rates 76% of the time, as it was not always possible to
count bites or see the focal animal's mouth, even when I knew they were eating. Of the data with
feeding rates, I have nutritional information for 97.5% of the plant foods consumed. Therefore,
the data presented here are likely approximately 27% lower than the average animal daily
intakes. Additionally, these data do not include the amount of food focal animals consumed at
night, which may have been significant. However, assuming that the excluded data are equally
distributed between animals, and that the rates of feeding at night are comparable to those during
the day, the data presented here represent an accurate fraction of the actual average animal daily
The average daily intake and statistical analyses of macronutrients, non-nutrients,
amount, protein to fiber ratio, and energy for each season, sex, and group can be found in Tables
5.7-5.8. In sum, there are significant differences within the following combinations: sexes and
calories consumed; seasons and calories, tannin and the ratio of protein:ADF; and lemur groups
and the amount of NDF and ADF (Figure 5.4). For comparative purposes, I divided the average
number of calories consumed per day by all animals, by the average distance traveled per day in
the dry and wet seasons. The value for the dry season is 0.0776 kcal/m (171.1 kcal/ 2205 m) and
the value for the wet season is 0.129 kcal/m (235.8 kcal/ 1830 m).
Table 5.7. Average daily intake by season, sex and group of macronutrient (g/day), non-nutrient
(g/day), protein to fiber ratio, and energy (kcal/day).
Protein :ADF
Table 5.8. Statistical results from the Independent Student's T-test between sexes, seasons, and
group for the consumption of macronutrients (g/day), non-nutrients (g/day), the protein to ADF
ratio, and energy (kcal/day).