First Advisor

Natalie Vasey

Term of Graduation

Winter 2020

Date of Publication


Document Type


Degree Name

Doctor of Philosophy (Ph.D.) in Environmental Sciences and Resources


Environmental Sciences and Resources




Forest canopy gaps -- Madagascar -- Parc national de Masoala, Lemurs -- Behavior -- Madagascar -- Parc national de Masoala, Forest canopy ecology, Ecological disturbances



Physical Description

1 online resource (xiii, 225 pages)


Madagascar is one of Earth's top biodiversity hotspots, with 80% of life on the island considered endemic. Among the endemic species are lemurs, a diverse group of non-human primates. Unfortunately, Madagascar's diversity, including lemurs, is threatened by habitat degradation and loss. Despite intense anthropogenic pressure over the past 50 years, scientists have not detected any lemur extinctions during this period. Some researchers have proposed that lemurs' adaptations to natural disturbances have provided these taxa resiliency against anthropogenic disturbances. Certainly, Madagascar experiences an extreme disturbance regime: the island experiences an average of over three cyclones a year. These cyclones create numerous, small disturbances in the form of tree-fall canopy gaps. Consequently, lemurs have had to adapt to both large-scale and small-scale disturbances. While some research exists on the impact of cyclones on lemur behavior, ecology, and population dynamics, very little is known about how tree-fall canopy gap disturbances affect lemurs. This research was the first to address the role canopy gaps play in the behavioral ecology of lemurs.

Tree-fall canopy gaps are ubiquitous features within Masoala National Park (MNP), Madagascar, home of two closely related frugivorous lemur species: Varecia rubra and Eulemur albifrons. Research on other rain forest mammals suggests that canopy gaps may be ecologically important by contributing to high-density and high-quality food patches. Gaps can increase fruit, flower, and young leaf abundance, and increase protein content of young leaves.

V. rubra and E. albifrons evolved within the same disturbance regime at MNP yet differ in a variety of ways. V. rubra is larger (2.6 - 4.1 kg) and include a greater proportion of fruit in their diet than other lemur taxa. In contrast, the smaller (1.6 - 2.3) E. albifrons has greater dietary flexibility than V. rubra, with fruit making up a smaller proportion of the former's overall diet. V. rubra exhibits a highly dynamic fission-fusion social organization that is dictated by both seasonality and reproduction. They live in communities with 8 to 30 individuals and frequently form subgroups of two to five individuals. E. albifrons lives in small (seven to nine individuals), multi-male, multi-female groups that are cohesive year-round.

Some life history traits also differ strikingly. Female V. rubra give birth to litters of up to five offspring (commonly two or three) that develop rapidly with juveniles reaching two-thirds adult body weight by nine months. Females construct nests where infants are born and remain for the first couple of weeks of their lives. Infants are then carried orally and stashed while females forage. High-fat, high-energy milk provided on schedule allow nursing females to stash young for extended time periods. Adults of both sexes participate in extensive alloparenting. In contrast, female E. albifrons give birth to singletons (less commonly twins) and carry their offspring full-time, providing low-energy, low-fat milk on demand. In fact, females within the genus Eulemur produce some of the poorest quality milk of all primates.

Because V. rubra and E. albifrons have different life history traits, a comparison of their adaptations to the same disturbance regime should provide insight into the interaction between life history strategy, natural disturbance, and ecological adaptations. The goal of my research was to determine the different behavioral responses of V. rubra and E. albifrons to tree-fall canopy gaps given their different ecological and life history characteristics. I asked whether V. rubra and E. albifrons use canopy gaps differently than closed canopy forest, and, if so, how. I hypothesized that canopy gaps would serve as food-rich sites for both species. I also predicted that E. albifrons, with its greater ecological and dietary flexibility, would be more closely associated with the tree-fall canopy gaps than V. rubra. Finally, I hypothesized that canopy gaps would provide high-quality food for both species.

My data provide evidence that V. rubra and E. albifrons tolerate the high rate of disturbance represented by tree-fall canopy gaps, at least during the hot, food-abundant seasons. Using generalized mixed effects models (GLMMs), I found that the difference to the nearest gap was significantly different for E. albifrons, V. rubra, and random transect trees. Compared to transect trees, E. albifrons were closer to canopy gaps than expected; V. rubra were farther from canopy gaps than expected during the early part of the hot, dry season and decreased the distance to the nearest gap throughout the hot, rainy season. These results applied to a period of high fruit availability in the hot seasons following Cyclone Enawo, 2017. During a period of low cyclone activity and corresponding low fruit availability, both E. albifrons and V. rubra maintained proximity near tree-fall gaps; only E. albifrons, however, was closer to gaps than random transect trees. Consequently, the two species do differ in their behavior response to canopy gaps as predicted.

The data also support the hypothesis that tree-fall canopy gaps serve as food-rich sites for frugivorous lemurs. GLMMs of tree and liana young leaves and fruit indicated that proximity to gaps was associated with increased fruit and young leaf abundance. Proximity to canopy gaps increased leaf and fruit abundance during the food-scarce, low cyclone activity period and the food-abundant, recent cyclone activity period, as predicted. Contrary to my hypothesis, however, proximity to tree-fall canopy gaps did not affect the nutritional content of young leaves or fruit. Energy and the percent of nitrogen, crude protein, non-structural carbohydrates, condensed tannins, and polyphenols of food samples were similar regardless of whether the samples were collected from gap edges or closed canopy.

The benefits and potential costs of association with tree-fall canopy gaps are affected by cyclones, food availability, and gap frequency. Whether or not lemurs associated with tree-fall gaps depended on food availability within the forest. In times when food was scarce, both species decreased their average distance from canopy gaps and spent more time traveling to do so. The value of canopy gaps also depended on their number and distribution; when common throughout the forest, the lemurs did not need to actively select gaps to be near and benefit from them. The interannual variation in tree-fall canopy gaps, plant phenology, and lemur food abundance in this study highlight the importance of long-term, multi-year studies for understanding complex relationships between disturbance and lemur ecology. Understanding these relationships is increasingly urgent as climate change is expected to significantly alter the intensity and frequency of tropical storms, the most common cause of canopy gaps.


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