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Reproductive Female Feeding Strategies in Spiny Forest-Dwelling Lemur catta in Southern and Southwestern Madagascar: How Do Females Meet the Challenges of Reproduction in this Harsh Habitat?
Abstract
The spiny forest ecoregion of southern and southwestern Madagascar is characterized by low annual rainfall, high temperatures, short-stature xeric vegetation and lack of canopy. Lemur catta is often the only diurnal primate persisting in this habitat. For reproductive females living in spiny forests, gestation and early-to-mid lactation periods occur during the dry season when food resources are limited. We conducted a between-site comparison of variables important to the feeding ecology of reproductive female L. catta inhabiting spiny forest at 3 sites: Berenty spiny forest (BSF), Cap Sainte-Marie (CSM) and Tsimanampesotse National Park (TNP). We hypothesize that the ability for pregnant and lactating females to adequately obtain plant foods high in protein, low in fiber and with a high water content is crucial to their survival and successful reproduction in spiny habitat. We found favorable or relatively equal protein-to-fiber ratios in plant foods most frequently consumed by reproductive females, and preferred foods contained high water content. Some overlap in preferred plant species at the 3 sites suggests important plant foods for reproductive females inhabiting spiny forests. We suggest that choosing foods high in protein, relatively low in fiber and with high water content are behavioral adaptations allowing female L. catta to reproduce and survive in this habitat. © 2015 S. Karger AG, Basel.
... Solving the challenges faced in locating, acquiring, and processing a nutritionally balanced diet can act as a strong selective pressure impacting a species' morphology, sensory ecology, dietary adaptations , habitat use and ranging (Matsuda et al. 2009;Behie and Pavelka 2015), reproductive strategies (Gould et al., 2015), and population density and group size (Hanya & Chapman 2013;Ma et al., 2017). In the case of frugivorous primates, factors such as patch productivity, patch distribution, and whether individual trees of the same species fruit synchronously or asynchronously, play a critical role in foraging decisions (Garber, 1989;. ...
The black or Myanmar snub-nosed monkey (Rhinopithecus strykeri) was discovered in the Gaoligong Mountains of northeastern Kachin state, Myanmar in 2010, and was subsequently found in the mountains of northwestern Yunnan, China in 2011. Across these regions, there were an estimated 14-15 sub-populations with approximately 950 individuals in total (10 sub-populations with 490-620 individuals in China, and 4-5 sub-populations with 260-330 individuals in Myanmar). However, teams of people conducting field surveys and camera trap studies, of which I was part, only confirmed five sub-populations with 400 individuals on the Sino-Myanmar border from data collected 2012-2017. Based on approximately two years field searching, I and my colleagues discovered one sub-population (Luoma population) in the Gaoligong Mountains and conducted another 203 days of field observation to collect dietary data. I also conducted cafeteria feeding trials with 600 wild plant species on two captive individuals housed at Yaojiaping Wildlife Rescue Centre in the Gaoligong Mountains National Nature Reserve. I found that R. strykeri can potentially consume 593 items from more than 170 food plants of trees, bushes, and herbs representing 76 genera and 41 plant families, as well as 15 species of lichen. Among these food items and species, 14 plant species and four lichen species also are consumed by the wild monkeys as well. The food plants mainly distribute in intact sub-tropical evergreen broadleaf forests and hemlock-broadleaf mixed forests at an altitude of 2200-3000 m. Based on interview surveys, camera trap records, and habitat distribution modelling, I confirm this is the main elevational range used by R. strykeri. Nutritional studies and comparisons of 100 leaf items the monkeys selectively consumed (n = 70 plant species) with the nutrient content of 54 leaf items (n = 48 plant species) the monkeys’ avoided in spring and autumn reveal that R. strykeri preferentially select leaves high in moisture (77.7%), crude protein (21.2%), total nonstructural carbohydrates (34.9%) and phosphorus (0.37%) while tending to avoid foods with a neutral detergent fibre content close to 35%. Foods selected in autumn were characterized by a higher amount of metabolisable energy than those rejected (1350 kJ/100g vs. 1268 kJ/100g). Random Forests modeling, an ensemble learning method, indicated that foods consumed during the two seasons were selected primarily based on their proportion of moisture, crude protein, neutral detergent fibre, metabolisable energy, phosphorus and total nonstructural carbohydrates. This nutritional profile is similar to other snub-nosed monkeys. Using interview-based survey data and MAXENT modelling of R. strykeri along the Sino-Myanmar border, I found that R. strykeri may inhabit a range from E98°20′–98°50′ to N25°40′–26°50′. Within this range, high-quality habitat at 1420 km2, medium-quality habitat at 750 km2, and low-quality habitats at 1410 km2. Only 13.9% of the highly suitable habitat (medium + core habitat) for R. strykeri falls within protected areas in China. Approximately 2.6% of the entire habitat has been lost in the past 15 years, 96% of which has been in Myanmar. Two national parks (Imawbum National Park in Myanmar and Nujiang Grand Canyon National Park in China) are therefore proposed for saving this species. Lastly, for structuring a systematic transboundary conservation network in the highly-biodiverse but poorly-studied Gaoligong Mountains region, I used interview-based survey results (on animal distribution data) of three taxa (Primates, Pheasants and Mishmi Takin) and identified five flagship species (R. strykeri, Hoolock tianxing, Trachypithecus shortridgei, Lophophorus sclateri, Budorcas taxicolor) as surrogates of community biodiversity in the Gaoligong Mountains. After confirming the reliability of species distribution data via selective field surveys, I applied multicriteria decision analysis techniques along with data on habitat suitability (MAXENT Models) to highlight areas for transboundary conservation efforts. My results indicate that approximately 83.4% (10,398.7 km2) of remaining habitat with high conservation value for each of the five flagship species is unprotected. This includes six large zones separated by rivers and human settlements that should be designated as transboundary World Nature Heritage, National Parks, or Wildlife sanctuaries along the northern Sino-Myanmar border. Accordingly, I propose related conservation actions and policies for transboundary conservation in the Gaoligong Mountains along the northern Sino-Myanmar border.
... Before our study, research on L. catta feeding ecology conducted in two of the forest fragments in this region revealed that the fruit and leaves of the exotic Melia azedarach, and fruit of three endemic and three exotic Ficus species were keystone foods for the ring-tailed lemurs in these small forests (Cameron & Gould, 2013;Gabriel, 2013a;Gould & Gabriel, 2015). L. catta is known as an extremely ecologically flexible primate, currently or recently found in seven distinct habitats (Goodman et al., 2006;Gould, 2006;Gould, Kelley, & LaFleur, 2015;Kelley, 2011;LaFleur & Sauther, 2015;Ravoavy, 2013;Sauther et al., 1999), and this species exhibits strong preferences for particular foods specific to each habitat, with little overlap Gould, Power, Ellwanger, & Rambeloarivony, 2011;Kelley, 2011;LaFleur, 2011;Mertl-Milhollen et al., 2003;Sauther, 1998;Simmen et al., 2006). The key food resources for L. catta in these south-central fragments differ completely from that documented in other habitats in which this species is found. ...
Habitat fragmentation is an increasingly serious issue affecting primates in most regions where they are found today. Populations of Lemur catta (ring-tailed lemur) in Madagascar's south-central region are increasingly restricted to small, isolated forest fragments, surrounded by grasslands or small-scale agriculture. Our aim was to evaluate the potential for population viability of L. catta in nine forest fragments of varying sizes (2-46 ha, population range: 6-210 animals) in south-central Madagascar, using a set of comparative, quantitative ecological measures. We used Poisson regression models with a log link function to examine the effects of fragment size, within-fragment food availability, and abundance of matrix resources (food and water sources) on L. catta population sizes and juvenile recruitment. We found a strong association between overall population size and (a) fragment size and (b) abundance of key food resources Melia azedarach and Ficus spp. (per 100 m along transect lines). Juvenile recruitment was also associated with fragment size and abundance of the two above-mentioned food resources. When the largest population, an outlier, was removed from the analysis, again, the model containing fragment size and abundance of M. azedarach and Ficus spp. was the best fitting, but the model that best predicted juvenile recruitment contained only fragment size. While our results are useful for predicting population presence and possible persistence in these fragments, both the potential for male dispersal and the extent of human disturbance within most fragments play crucial roles regarding the likelihood of long-term L. catta survival. While seven of the nine fragments were reasonably protected from human disturbance, only three offered the strong potential for male dispersal, thus the long-term viability of many of these populations is highly uncertain.
... especially A. ascendens and A. procera are dominant trees in forest stands providing several ecosystem services. Abundant scientific literature reported their consumption by folivorous lemurs to supply protein and non-protein energy nutrient, fiber and water [2][3][4] but also their use as sleeping sites [5]. Alluaudia procera (Figure 1) is among extracted forest products used as fuel wood, making house and furniture [6,7]. ...
Drug resistance is a major obstacle in antibiotic and antitumor chemotherapy. In response to the necessity to find new therapeutic strategies, plant secondary metabolites including essential oils (EOs) may represent one of the best sources. EOs in plants act as constitutive defenses against biotic and abiotic stress, and they play an important role in the pharmacology for their low toxicity, good pharmacokinetic and multitarget activity. In this context, natural products such as EOs are one of the most important sources of drugs used in pharmaceutical therapeutics. The aim of this paper was to identify the chemical composition of the essential oil of Alluaudia procera leaves, obtained by hydrodistillation and analysed by gas chromatography-mass spectrometry, and to verify its biological activities on acute myeloid leukemia cancer cell HL60 and its multidrugresistant variant HL60R and the Gram-positive Staphylococcus aureus exhibiting multi-antibiotic resistance. We speculate that cytotoxic and antibiotic effects observed in the tested resistant models may be due to the coordinate activities of forty compounds detected or to the C16 macrocyclic lactones which are the major ones (30%). Our data confirm the possibility of using EOs as therapeutic strategies in resistant models is due to the heterogeneous composition of the oils themselves.
... 9-019-00717 -0) contains supplementary material, which is available to authorized users. (Matsuda et al. 2009;Behie and Pavelka 2015), reproductive strategies (Gould et al. 2015), and population density and group size (Hanya and Chapman 2013;Ma et al. 2017). In the case of fruiteating primates, factors such as patch productivity, patch distribution, and whether individual trees of the same species fruit synchronously or asynchronously, play a critical role in foraging decisions (Garber 1989;Chapman et al. 2012). ...
Since its initial discovery in 2010 in the Gaoligong Mountains on the Sino–Myanmar border, there remains no direct information on the feeding habits of the black snub-nosed monkey (Rhinopithecus strykeri). This species is on the verge of extinction, with an estimated remaining population of < 400 individuals. Due to difficulties in following these monkeys across steep mountainous terrain, during 203 observation days (September 2015–January 2017) we recorded 80 h of behavioral records of a wild population (Luoma group). Our preliminary results identified 14 plant species and four lichen species consumed by the monkeys. In addition, we provided the only two captive individuals of this species with a cafeteria diet composed of > 600 wild-collected plant species that were gathered from known R. strykeri habitats to determine which plant species and food items were considered palatable. Our results indicate that the captive monkeys freely consumed young and mature leaves, fruits/seeds, buds, flowers, twigs, and bark from 170 different species of trees, bushes, and herbs representing 76 genera and 41 plant families, as well as 15 species of lichen. All foods consumed by the wild monkeys were also consumed by the captive individuals. Food plants consumed by R. strykeri were found principally in intact subtropical evergreen broadleaf forests and hemlock-broadleaf mixed forests at an altitude of 2200–3000 m. Strict enforcement of habitat protection and access to resources across this elevation zone appear to be essential for the conservation and survivorship of this critically endangered primate.
... The amount of time subjects spend eating is included as a predictor variable in the analysis since this behaviour is linked to cortisol output in an array of species, including ring-tailed lemurs [Cavigelli, 1999;Weingrill et al., 2004;Pride, 2005;Emery Thompson et al., 2010]. The ability of L. catta to survive in diverse ecological habitats has been attributed to their 'intelligent' feeding behaviour, emphasizing the significance of this behaviour for the species [Gould et al., 2015]. A positive correlation between time spent feeding and fGC levels is predicted (P5f) as a reflection of increased feeding competition. ...
In ring-tailed lemurs, Lemur catta, the factors modulating hypothalamic-pituitary-adrenal (HPA) activity differ between wild and semi-free-ranging populations. Here we assess factors modulating HPA activity in ring-tailed lemurs housed in a third environment: the zoo. First we validate an enzyme immunoassay to quantify levels of glucocorticoid (GC) metabolites in the faeces of L. catta. We determine the nature of the female-female dominance hierarchies within each group by computing David's scores and examining these in relation to faecal GC (fGC). Relationships between female age and fGC are assessed to evaluate potential age-related confounds. The associations between fGC, numbers of males in a group and reproductive status are explored. Finally, we investigate the value of 7 behaviours in predicting levels of fGC. The study revealed stable linear dominance hierarchies in females within each group. The number of males in a social group together with reproductive status, but not age, influenced fGC. The 7 behavioural variables accounted for 68% of the variance in fGC. The amounts of time an animal spent locomoting and in the inside enclosure were both negative predictors of fGC. The study highlights the flexibility and adaptability of the HPA system in ring-tailed lemurs.
... Lemur catta (ring-tailed lemur) is a cathemeral species characterized by seasonal fluctuations in olfactory behavior, group dispersal, tolerance level, and reproduction [58], [78], [79], [93][94][95][96][97]. Lemur catta has a steep, consistent, highly transitive and cohesive hierarchy (sensu Norscia and Palagi [56]), with females dominant over males [58], [59], [78], [98][99]). ...
However despotic a social group may be, managing conflicts of interest is crucial to preserve
group living benefits, mainly based on cooperation. In despotic groups, post-conflict
management via reconciliation (the first post-conflict reunion between former opponents)
can occur, even if conciliatory rates are considerably different. Lemur catta is defined as a
despotic species because groups are characterized by a strict linear hierarchy maintained
by the adult females (the dominant sex) mainly via aggression. Reconciliation was reported
in one out of four captive groups of L. catta. Here we investigate which variables influence
the occurrence of reconciliation in these despotic groups. We analyzed 2339 Post Conflict
(PC)-Matched Control (MC) observation pairs, collected on eight groups (five in the Berenty
forest, Madagascar; three hosted at the Pistoia Zoo, Italy). Since L. catta is characterized
by steep female dominance but shows female-female coalitionary support, we expected to
confirm the presence of reconciliation in the study species. Consistently, we found reconciliation
in one captive group and two wild groups, thus providing the first evidence of the presence
of this phenomenon in wild L. catta. Moreover, because this species is a seasonal
breeder (with mating occurring once a year), we expected seasonal fluctuations in reconciliation
levels. Via a GLMM analysis using data from all wild groups and on a captive group followed
for more than one year, we found that season (but not rank; individuals’ identity, sex,
and age; or group identity) significantly affected individual reconciliation rates, and such
rates were lowest during the mating period. Thus, reconciliation can be present in groups in
which dominants strongly influence and limit social relationships (steep dominance hierarchy)
except when the advantages of intra-group cooperation are overcome by competition,
as occurs in seasonal breeders when reproduction is at stake. We conclude that in despotic
social groups in which c
... For example, spiny forest ring-tailed lemurs appear to have feeding strategies that maintain protein resources during lactation irrespective of the type of spiny forest habitat. Gould et al. [2015] find that despite differences in plant species across 3 different spiny forest habitats, reproductive female ring-tailed lemurs maintain high protein-to-fibre ratios for preferred plant foods. Certain ring-tailed lemur habitats do appear to have protein advantages, however, as seen by LaFleur and Sauther [2015] who note that, compared to spiny forests, ring-tailed lemurs living in gallery forests dominated by Tamarindus indica (an important food in some gallery forest habitats) ingest higher crude protein, which could be at the potential expense of higher fibre content in their diets. ...
For over 50 years, ring-tailed lemurs have been studied continuously in the wild. As
one of the most long-studied primate species, the length and breadth of their study is
comparable to research on Japanese macaques, baboons and chimpanzees. They are
also one of the most broadly observed of all primates, with comprehensive research
conducted on their behaviour, biology, ecology, genetics, palaeobiology and life history.
However, over the last decade, a new generation of lemur scholars, working in conjunction
with researchers who have spent decades studying this species, have greatly
enhanced our knowledge of ring-tailed lemurs. In addition, research on this species has
expanded beyond traditional gallery forest habitats to now include high altitude, spiny
thicket, rocky outcrop and anthropogenically disturbed coastal forest populations. The
focus of this special volume is to ‘re-imagine’ the ‘flagship species of Madagascar’, bringing
together three generations of lemur scholars.
A key aspect of a primate’s ecology is its food source, the very nature of which is spatially and seasonally dependent and may be affected by anthropic pressures. One of the most endangered, yet best-studied, strepsirrhine primates is the ring-tailed lemur (Lemur catta), a species that has experienced significant human-induced habitat loss over many decades. To help understand feeding variability across time and space, I present a literature review of plant species (and parts) fed on by ring-tailed lemurs at nine sites in Madagascar: Ambatotsirongorongo, Andringitra Massif, Anja Reserve, Antserananomby, Berenty Reserve, Bezà Mahafaly Special Reserve, Cap Sainte-Marie, Tsaranoro Valley Forest, and Tsimanampetsotsa National Park. I gathered literature using keyword searches on Google Scholar (https://scholar.google.com/) and verified scientific names using the “Catalogue of the Plants of Madagascar” (http://legacy.tropicos.org/Project/Madagascar). From 24 studies, I identify 221 genera and 241 species of consumed plants, with 92 genera and 70 species consumed at two or more sites. Based on the available distribution data, 63% of species are endemic and 22% native. Sixty-seven plants are known only by Malagasy common names and excluded from analyses. When authors identify the plant tissue consumed, 52% of species in the diet are represented by a single tissue type, typically leaves (mature and immature) or fruit (ripe or unripe). This review highlights the importance of studying multiple populations when creating dietary summaries of species and should prove valuable to those exploring ecological trends and habitat use by ring-tailed lemurs.
The ring-tailed lemur (Lemur catta) was once widely distributed throughout the south-central, far south, and southwest regions of Madagascar. This species is known for its marked ecological plasticity and ability to survive in a variety of habitats. Over the past decade, however, habitat destruction, forest fragmentation, hunting for subsistence or the illegal bushmeat trade, and live capture for the illegal pet trade have increased, resulting in extirpation or drastic reduction of populations throughout its geographic range. Recent mining activities in one region have resulted in further serious threats to remaining populations. In this paper, we discuss (1) population numbers and information on population extirpations, gathered over approximately the past six years, to illustrate the alarming decline of this well-known lemur, and (2) how the formerly accepted geographic range of L. catta now requires considerable revision. Population information was collected via on-the-ground surveys and censuses, or from reports by researchers at 34 sites where L. catta is or was recently present. Only three sites are known to contain populations of more than 200 animals. At 12 sites, populations number 30 or fewer individuals, and at 15 sites, L. catta has been recently extirpated, or populations are highly precarious and may become extinct in the very near future. Populations at three previously designated range limits have been extirpated. Many populations are surviving in small, isolated forest fragments, allowing for no male dispersal. With an estimate of just 2, 000-2, 400 individuals remaining in Madagascar, this iconic lemur may well become extinct in the wild in the near future, or at the very least, exist at only two or three widely dispersed sites.
Although Lemur catta has been the subject of detailed behavioral and ecological field studies at a few localities in the southern portion of Madagascar and is certainly one of the best known of the island’s primates, little has been published about its distribution and the range of habitats it uses. The major exception to this point is a recent assessment of the geographical extent of this species overlaid on anthropogenic habitat degradation. Lemur catta is often associated with being a denizen of gallery forests of the southern spiny bush. This is natural as the vast majority of information on the life history of this taxon comes from long-term studies at Berenty and the Réserve Spéciale de Beza Mahafaly and concerns mostly troops living in this forest type. However, as discussed below, this species is the least forest-dwelling of the extant species of lemurs and occurs in a wide range of habitats in the southern third of the island, and the current categorization of certain life-history parameters may be slightly exaggerated given the intensive focus on gallery forest zones. In this contribution, we address four principal points concerning Lemur catta: (1) its current distribution; (2) geographic range associated with limitation of freshwater sources; (3) aspects of the ecology of the Andringitra high mountain population; and (4) a biogeographic scenario to explain its current distribution.
We addressed the issue of female social dominance as an adaptive response to seasonal energy stress in white sifakas living in a fragment of Didiereaceae forest of southern Madagascar. We tested whether female and male sifakas would exhibit different activity budgets, food choices and energy input given harsh ecological constraints that prevail in such xerophytic ecosystems. Behavioural data were obtained on 2 groups (including 8 focal individuals) during a 2-month study in the late wet season. We analysed forest composition, based on a sample of more than 1000 trees, shrubs and lianas, and phenology through a regular survey of 479 tagged individuals. Males and females were mostly feeding on mature leaves of common plant species, to which they added a range of minor food items. The activity budgets (5-min scan interval) did not differ significantly between sexes. In contrast, marked differences of food intake (using a quantitative method) were observed: we evaluated that females consumed daily 30-40% more food than males while the ranking of preferred foods remained globally similar between sexes. Ad libitum records confirmed female dominance over males in a feeding context, although few aggressive events were recorded. We conclude that (1) time sampling methods may not be appropriate to assess food intake because ingestion rates likely vary among individuals and (2) high food intake of adult females relative to males during the early gestation period is uncoupled with immediate physiological needs and may reflect a sex-specific fattening strategy allowing females to increase their reproductive success.
At Berenty Reserve, Madagascar, we have set up a main study area of 14.2 ha to study the demographic changes of ring-tailed lemurs for 11 years from 1989 to 2000. We also have set up a broader study area of 30.4 ha to study the environmental changes, including the main study area. In the main study area, due to the social changes such as troop divisions and evictions, the number of troops increased from three to six. Consequently, home range size of a troop decreased. In the broader study area, there were 475 large trees belonging to 14 species and 9 families. The most abundant species was kily (Tamarindus indica) (n=289), the second benono (Acacia rovumae) (n=74), the third voleli (Nestina isoneura) (n=66). These three species accounted for 90.3 % of all large trees. Population density of large trees was 15.6 per ha, and that of idly trees was 10.3 per ha. In 1989, 12.7 kily trees existed per ha within the main study area of 14.2 ha.In 2000, we re-measured the size of kily trees. Within the main study area of 14.2 ha, the density of idly trees decreased to 11.2 per ha. This decrease was due to the number of dead kily trees exceeded the number of newcomers. In contrast, the number of ring-tailed lemurs over one-year old increased from 63 in 1989 to 89 in 2000. As a result, the number of kily trees per animal was decreased from 2.8 to 1.8. Among troops, there was a great variation in the number of idly trees per animal. Troop CX occupied the richest area (4.7 kily trees/animal), and Troop T2 ranged the poorest area (0.6 kily trees/animal). On the other hand, the amount of kily fruits may fluctuate by each individual tree, area, and year. For example, the harvest of idly fruits was very poor in 2000, and the abundance score of kily fruits for Troop CX was lower than average score of the main study area. The number of brown lemurs (Eulemur fulvus) was also increasing. Since brown lemurs' feeding habits were very similar to ring-tailed lemurs, it is likely that both the within species and inter-species competitions are becoming intense for ring-tailed lemurs.
Feeding strategy and social dominance in female sifakas (Propithecus v. verreauxi) living
in a Didiereaceae forest in southern Madagascar. We addressed the issue of female social dominance as
an adaptive response to seasonal energy stress in white sifakas living in a fragment of Didiereaceae forest of
southern Madagascar. We tested whether female and male sifakas would exhibit different activity budgets,
food choices and energy input given harsh ecological constraints that prevail in such xerophytic ecosystems.
Behavioural data were obtained on 2 groups (including 8 focal individuals) during a 2-month study in the
late wet season. We analysed forest composition, based on a sample of more than 1000 trees, shrubs and
lianas, and phenology through a regular survey of 479 tagged individuals. Males and females were mostly
feeding on mature leaves of common plant species, to which they added a range of minor food items. The
activity budgets (5-min scan interval) did not differ signifi cantly between sexes. In contrast, marked differences
of food intake (using a quantitative method) were observed: we evaluated that females consumed daily
30-40% more food than males while the ranking of preferred foods remained globally similar between sexes.
Ad libitum records confi rmed female dominance over males in a feeding context, although few aggressive
events were recorded. We conclude that (1) time sampling methods may not be appropriate to assess food
intake because ingestion rates likely vary among individuals and (2) high food intake of adult females relative
to males during the early gestation period is uncoupled with immediate physiological needs and may
refl ect a sex-specifi c fattening strategy allowing females to increase their reproductive success.
Folivorous primate biomass has been shown to positively correlate with the average protein-to-fiber ratio in mature leaves of tropical forests. However, studies have failed to explain the mismatch between dietary selection and the role of the protein-to-fiber ratio on primate biomass; why do not folivores always favor mature leaves or leaves with the highest protein-to-fiber ratio? We examined the effect of leaf chemical characteristics and plant abundance (using transect censuses; 0.37 ha, 233 trees) on food choices and nutrient/toxin consumption in a folivorous lemur (Propithecus verreauxi) in a gallery forest in southern Madagascar. To assess the nutritional quality of the habitat, we calculated an abundance-weighted chemical index for each chemical variable. Food intake was quantified using a continuous count of mouthfuls during individual full-day follows across three seasons. We found a significant positive correlation between food ranking in the diet and plant abundance. The protein-to-fiber ratio and most other chemical variables tested had no statistical effect on dietary selection. Numerous chemical characteristics of the sifaka's diet were essentially by-products of generalist feeding and "low energy input/low energy crop" strategy. The examination of feeding behavior and plant chemistry in Old World colobines and folivorous prosimians in Madagascar suggests that relative lack of feeding selectivity and high primate biomass occur when the average protein-to-fiber ratio of mature leaves in the habitat exceeds a threshold at 0.4. Am. J. Primatol. © 2013 Wiley Periodicals, Inc.
Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered "strictly diurnal". We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010-April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25 % of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5 % of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53 % nighttime, 43 % daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.
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.
Data are presented on ring-tailed lemur feeding ecology and resource use at the Beza Mahafaly Special Reserve in southwestern Madagascar. The phenological availability of food resources was sampled monthly from 199 trees and 31 species. Results indicate that Lemur catta feeding ecology is finely tuned to the seasonal nature of specific food resources. Key species provide important food items during critical periods of the reproductive cycle. During a drought year, mortality for mothers and infants increased dramatically, providing indirect evidence that this species is highly dependent on the phenological reliability of food resources. These results indicate that in such highly seasonal habitats, the loss of any key species could have enormous impact on ring-tailed lemur demography and survival.
This is the first study to document the natural history of Lemur catta, ring-tailed lemurs, outside of gallery forest environments: in xerophytic Didiereaceae-Euphorbia, bush habitat that represents over 90% of this species' potential range. Moreover, this study is the first to document ring-tailed lemurs, or any primate species for that matter, as cactus dwellers. Data were collected for 15 consecutive months on two different troops in the Cap Sainte-Marie (CSM) area, which is Madagascar's southernmost region. All-day follows, nutritional analyses, and health assessments were the methods used to test hypotheses on the following themes: a) behavioral flexibility, b) ecology, health, and nutrition, c) the shared use of space with humans, and d) the utilization of nonnative species. Significant findings include: extremely large home ranges, highly social and spatially cohesive (juvenile centered) groups, coexistence with Antandroy villagers, and diverse diets comprised of native species despite the population's adaptation to Opuntia monacantha and Opuntia stricta. Based on these findings, I suggest that L. catta have historically been present in the CSM region, but that this population likely persists here today only because of the presence of Opuntia.
Recent results have suggested that the biomass of folivorous arboreal primates per unit area in Africa and Asia is positively
correlated with the average quality of leaves, expressed as the ratio of protein to fiber concentrations in a given forest.
This hypothesis has been tested in different forests of Madagascar. Leaf selection of all folivorous femus species was studied
in relation to leaf chemistry. Except for two populations ofLepilemur subspecies all other folivorous lemur species (including two other subspecies ofLepilemur) select leaves with high concentrations of easily extractable protein or low concentrations of fiber, or both. This confirms
the prominent role of these two components in leaf selection by folivorous lemurs. The average quality of mature leaves in
a given forest, expressed as the ratio of protein to fiber concentrations, is positively correlated with the biomass of folivorous
lemurs. This confirms the hypothesis tested and suggests rather uniform selection processes for arboreal folivorous primates
across the world.
The Beza Mahafaly Project in southwestern Madagascar was founded in 1975. It was established as a collaborative effort among
the University of Madagascar (now University of Antananarivo), Washington University, Yale University, and the local communities
for long-term training and research, biodiversity conservation, and socioeconomic development. Beza Mahafaly consists of two
noncontiguous forest parcels separated by 10 km that became a protected area (Réserve Spéciale) in 1986: an 80-ha gallery
forest and a 520-ha xerophytic spiny forest. The region has a diversity of habitats and a very diverse and highly endemic
flora and fauna, including four species of lemurs found in or near the reserve. The ringtailed lemur (Lemur catta) and Verreaux’s sifaka (Propithecus verreauxi) have been the subject of our long-term research. In this chapter we highlight some of the results of this research. Our
multidisciplinary studies illustrate the feasibility of collecting long-term data on careers of individual animals and of
obtaining large samples on numerous animals, across numerous social groups, in relatively isolated breeding populations. Thus,
we can provide insights into many of the demographic, socioecological, anthropogenic, and epidemiological factors that shape
the local ringtailed lemur and sifaka population. Here we summarize how ringtailed lemur demographic structure is affected
by climatic perturbations (drought); how aspects of general health (parasite loads and dental health) are directly related
to habitat, dietary, and anthropogenic factors; how tight birth seasonality in sifaka can elicit stress responses in males
associated with increased male aggression, group takeovers, and infanticide risk; how life history schedules are related to
evolutionary responses to extreme climatic fluctuations; and how directional selection among sifaka males leads to longer,
stronger legs, but not to increase in male body mass relative to females.
We examine demographic patterns from a long-term study (1987–1996) of the population of ring-tailed lemurs in the Beza-Mahafaly Special Reserve, in southwestern Madagascar. In particular, we focus on the effects that a severe drought in 1991 and 1992 had on the population. The population of adult animals peaked in 1991 but decreased rapidly during the subsequent drought and immediate postdrought years. In the 1992 birth season (and second year of the drought) infant mortality reached 80%, and 20.8% of all adult females in the reserve died. The following year, adult female mortality reached a high of 29.9%. Juvenile mortality in 3 intensively studied groups was 57% during the second year of the drought. We compare these data with infant, juvenile, and adult female mortality in non-drought years. We are not able to calculate adult male mortality, as they often emigrate from the reserve to the adjacent forest; however, in the same 3 intensively studied groups, 89% of the males disappeared during the 2 immediate postdrought years. By 1996, the population had begun to recover after the decline that correlated with the drought conditions. Annual reproduction, high birth rates (.80–.86 annually), early sexual maturity, and dietary adaptability may be contributing factors to the recovery. Effects of and recovery from this type of natural disaster in the Beza Mahafaly ring-tailed lemur population parallel responses of some species of macaques and baboons with respect to the adaptability of edge species.
The biomass of arboreal folivorous primates in Africa and Asia is related to an index of mature leaf quality: the ratio of protein-to-fiber concentration. Investigations have considered variation in folivore biomass and forest composition among sites separated by hundreds or thousands of km. However, large variation in folivore abundance has been documented over much smaller spatial scales. We quantify the degree to which the average protein-to-fiber ratio of mature leaves of the 20 most abundant tree species predicts the biomass of western red colobus (Piliocolobus trephosceles) and black-and-white colobus (Colobus guereza) over very small spatial scales. Four sites within Kibale National Park, Uganda, varied markedly in forest structure. Colobine biomass varied among sites from 191 to 2675 kg/km2 and was related to the average protein-to-fiber ratio of mature leaves of the 20 most abundant tree species at each site. We examined the generality of the relationship between protein-to-fiber ratios and colobine abundance by adding our biomass and leaf chemistry values to previously published values to produce 9 comparable sites. At these locations, colobine biomass varied from 84 to 2675 kg/km2 (mean biomass among sites = 910 kg/km2), and mean protein/fiber ratios varied from 0.167 to 0.577. Colobine biomass was related to the protein-to-fiber ratios of mature leaves (R
2 = 0.616, P = 0.012).
Strong resource seasonality in Madagascar has led to the evolution of female feeding priority and weaning synchrony in most lemur species. For these taxa, pregnancy/early lactation periods coincide with low food availability, and weaning of infants is timed with increased resources at the onset of the rainy season. Reproductive females experience high metabolic requirements, which they must accommodate, particularly when food resources are scarce. Female ring-tailed lemurs (Lemur catta) residing in spiny forest habitat must deal with resource scarcity, high temperatures (∼36-40°C) and little shade in early to mid-lactation periods. Considered "income breeders," these females must use resources obtained from the environment instead of relying on fat stores; thus, we expected they would differ from same-sized males in time spent on feeding and in the intake of food and nutrients. We investigated these variables in two groups (N = 11 and 12) of Lemur catta residing in spiny forest habitat during early gestation and early to mid-lactation periods. Focal animal data and food plant samples were collected, and plants were analyzed for protein, kcal, and fiber. We found no sex differences for any feeding or nutrient intake variable for the top five food species consumed. Females in early gestation spent more time feeding compared with early/mid-lactation. Physiological compensation for spiny forest-dwelling females may be tied to greater time spent resting compared with gallery forest conspecifics, consuming foods high in protein, calories, and water, reduced home range defense in a sparsely populated habitat, and for Lemur catta females in general, production of relatively dilute milk compared with many strepsirrhines.
Environmental conditions are a key factor mediating reproductive success or failure. Consequently, many mammalian taxa have breeding seasons that coordinate critical reproductive stages with optimal environmental conditions. However, in contrast with most mammals, baboons (Papio cynocephalus) of Kenya reproduce throughout the year. Here we depart from the typical approach of evaluating seasonal effects on reproduction and engage in a more fine-grained analysis of the actual ecological conditions leading up to reproduction for females. Our aim was to determine how environmental conditions, in combination with social and demographic factors, might mediate baboon reproduction. The data set includes all female reproductive cycles from multiple baboon groups in the Amboseli basin between 1976 and 2004. Results indicate that after periods of drought or extreme heat, females were significantly less likely to cycle than expected. If females did cycle after these conditions, they were less likely to conceive; and if they did conceive after drought (heat effects were nonsignificant), they were less likely to have a successful pregnancy. Age also significantly predicted conceptive failure; conceptive probability was lowest among the youngest and oldest cycling females. There was also a trend for high ambient temperatures to contribute to fetal loss during the first trimester but not other trimesters. Finally, group size and drought conditions interacted in their effects on the probability of conception. Although females in all groups had equal conception probabilities during optimal conditions, females in large groups were less likely than those in small groups to conceive during periods of drought. These results indicate that in a highly variable environment, baboon reproductive success is mediated by the interaction between proximate ecological conditions and individual demographic factors. Copyright 2006.
Niche separation was documented in a year-long study of Varecia variegata rubra and Eulemur fulvus albifrons on the Masoala Peninsula, Madagascar. Feeding trees were measured, and diet, forest height, and forest site were recorded at 5-min time points on focal animals. For time point data, multivariate and bivariate analysis of frequencies was employed to examine how niche dimensions vary between species according to sex, season, and reproductive stage. V. v. rubra feeds in larger trees than E. f. albifrons. V. v. rubra has a diet consisting mainly of fruit, whereas E. f. lbifrons has a more varied diet. V. v. ubra ranges mainly above 15 m in tree crowns, whereas E. f. albifrons ranges mainly below 15 m in a wide array of forest sites. Both species are largely frugivorous, but they harvest fruit in different-sized trees, in different quantities, and in different forest strata. Niche partitioning varies in tandem with seasonal shifts in climate and food availability and with reproductive stages. Seasonal shifts in forest site and forest height use are largely attributed to species-specific tactics for behavioral thermoregulation and predator avoidance. The diet of E. f. albifrons is diverse whether examined by season or reproductive stage. However, females of both species diversify their diets with more low-fiber protein than males during gestation, lactation, and the hot seasons. This pattern is most pronounced for V. v. rubra females and may be directly attributed to high energetic investment in reproduction. These results suggest that niche partitioning may be driven more by the energetic requirements of reproductive females than males.
Based on a year-long field study in northeastern Madagascar, I summarize annual patterns of niche use (food patch size, diet, forest height, and forest site) in two sympatric lemurs, Varecia variegata rubra and Eulemur fulvus albifrons. Furthermore, I examine intraspecific patterns of niche use according to sex, season, and reproductive stage in these two lemurs that differ in terms of energetic investment in reproduction. Lemurs as a group provide a special opportunity to test hypotheses concerning sex differences in niche use. Due to their body size monomorphism and seasonal, synchronous pattern of breeding, it is possible to directly evaluate whether sex differences in diet reflect high energetic investment in reproduction by females. Results confirm the hypothesis that intraspecific variation in niche use (e.g., sex differences, seasonal differences) would be more pronounced in V. v. rubra than in E. f. albifrons, due in large measure to the former's relatively high energetic investment in reproduction: 1a) Dietary sex differences in V. v. rubra are most pronounced during costly reproductive stages and involve acquisition of low-fiber, high-protein plant foods. Females of both species consume more seasonally available low-fiber protein (young leaves, flowers) relative to conspecific males during the hot dry season, but only in V. v. rubra females is this pattern also evident during gestation and lactation. 1b) The diets of female V. v. rubra and female E. f. albifrons are more similar to each other than are the diets of conspecific males and females in the case of V. v. rubra. This is not uniformly the case for female E. f. albifrons. This finding confirms a hypothesis put forward in Vasey ([2000] Am J Phys Anthropol 112:411-431) that energetic requirements of reproductive females drive niche separation more than do the energetic requirements of males. 1c) Both species synchronize most or all of lactation with seasonal food abundance and diversity. E. f. albifrons shows a more protracted period of synchrony, and this may contribute to its wide biogeographic distribution in Madagascar. 2) Sex differences and seasonal differences in microhabitat use reflect intraspecific patterns of thermoregulation, predator avoidance, and in the case of V. v. rubra, reproduction. One important factor selecting for body size monomorphism in lemurs appears to be the tight synchrony between lactation and periods of food abundance afforded by annual, seasonal breeding.
In the dry forest of southern Madagascar, a region of global conservation priority, formally protected areas are nearly totally absent. We illustrate how the continued existence of unique forest habitats in the Androy region is directly dependent on informal institutions, taboos, regulating human behavior. Qualitative interviews to map and analyze the social mechanisms underlying forest protection have been combined with vegetation analyses of species diversity and composition. Of 188 forest patches, 93% were classified as protected, and in Southern Androy all remaining forest patches larger than 5 ha were protected. Eight different types of forests, with a gradient of social fencing from open access to almost complete entry prohibitions, were identified. Transgressions were well enforced with strong sanctions of significant economic as well as religious importance. Analyses of species diversity between protected and unprotected forests were complicated because of size differences and access restrictions. However, since, for example, in southern Androy >90% of the total remaining forest cover is protected through taboos, these informal institutions represent an important, and presently the only, mechanism for conservation of the highly endemic forest species. We conclude that social aspects, such as local beliefs and legitimate sanctioning systems, need to be analyzed and incorporated along with biodiversity studies for successful conservation.
Habitat fragmentation is an increasingly serious issue affecting primates in most regions where they are found today. Populations of Lemur catta (ring-tailed lemur) in Madagascar's south-central region are increasingly restricted to small, isolated forest fragments, surrounded by grasslands or small-scale agriculture. Our aim was to evaluate the potential for population viability of L. catta in nine forest fragments of varying sizes (2-46 ha, population range: 6-210 animals) in south-central Madagascar, using a set of comparative, quantitative ecological measures. We used Poisson regression models with a log link function to examine the effects of fragment size, within-fragment food availability, and abundance of matrix resources (food and water sources) on L. catta population sizes and juvenile recruitment. We found a strong association between overall population size and (a) fragment size and (b) abundance of key food resources Melia azedarach and Ficus spp. (per 100 m along transect lines). Juvenile recruitment was also associated with fragment size and abundance of the two above-mentioned food resources. When the largest population, an outlier, was removed from the analysis, again, the model containing fragment size and abundance of M. azedarach and Ficus spp. was the best fitting, but the model that best predicted juvenile recruitment contained only fragment size. While our results are useful for predicting population presence and possible persistence in these fragments, both the potential for male dispersal and the extent of human disturbance within most fragments play crucial roles regarding the likelihood of long-term L. catta survival. While seven of the nine fragments were reasonably protected from human disturbance, only three offered the strong potential for male dispersal, thus the long-term viability of many of these populations is highly uncertain.
The last decade's lemur research includes successes in discovering new living and extinct species and learning about the distribution, biogeography, physiology, behavior, and ecology of previously little-studied species. In addition, in both the dry forest and rain forest, long-term studies of lemur demography, life history and reproduction, have been completed in conjunction with data on tree productivity, phenology, and climate. Lemurs contrast with anthropoids in several behavioral features, including female dominance, targeted female-female aggression, lack of sexual dimorphism regardless of mating system, sperm competition coupled with male-male aggression, high infant mortality, cathemerality, and strict seasonal breeding. Hypotheses to explain these traits include the "energy conservation hypothesis" (ECH) suggesting that harsh and unpredictable climate factors on the island of Madagascar have affected the evolution of female dominance, and the "evolutionary disequilibrium hypotheses" (EVDH) suggesting that the recent megafauna extinctions have influenced lemurs to become diurnal. These hypotheses are compared and contrasted in light of recent empirical data on climate, subfossils, and lemur behavior. New data on life histories of the rain forest lemurs at Ranomafana National Park give further support to the ECH. Birth seasons are synchronized within each species, but there is a 6-month distribution of births among species. Gestation and lactation lengths vary among sympatric lemurs, but all lemur species in the rain forest wean in synchrony at the season most likely to have abundant resources. Across-species weaning synchrony seen in Ranomafana corroborates data from the dry forest that late lactation and weaning is the life history event that is the primary focus of the annual schedule. Lemur adaptations may assure maximum offspring survival in this environment with an unpredictable food supply and heavy predation. In conclusion, a more comprehensive energy frugality hypothesis (EFH) is proposed, which postulates 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 use of scarce resources (e.g., cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony). Among primates, the isolated adaptive radiation of lemurs on Madagascar may have been uniquely characterized by selection toward efficiency to cope with the harsh and unpredictable island environment. (C) 1999 Wiley-Liss, Inc.
Environmental conditions are a key factor mediating reproductive success or failure. Consequently, many mammalian taxa have
breeding seasons that coordinate critical reproductive stages with optimal environmental conditions. However, in contrast
with most mammals, baboons (Papio cynocephalus) of Kenya reproduce throughout the year. Here we depart from the typical approach of evaluating seasonal effects on reproduction
and engage in a more fine-grained analysis of the actual ecological conditions leading up to reproduction for females. Our
aim was to determine how environmental conditions, in combination with social and demographic factors, might mediate baboon
reproduction. The data set includes all female reproductive cycles from multiple baboon groups in the Amboseli basin between
1976 and 2004. Results indicate that after periods of drought or extreme heat, females were significantly less likely to cycle
than expected. If females did cycle after these conditions, they were less likely to conceive; and if they did conceive after
drought (heat effects were nonsignificant), they were less likely to have a successful pregnancy. Age also significantly predicted
conceptive failure; conceptive probability was lowest among the youngest and oldest cycling females. There was also a trend
for high ambient temperatures to contribute to fetal loss during the first trimester but not other trimesters. Finally, group
size and drought conditions interacted in their effects on the probability of conception. Although females in all groups had
equal conception probabilities during optimal conditions, females in large groups were less likely than those in small groups
to conceive during periods of drought. These results indicate that in a highly variable environment, baboon reproductive success
is mediated by the interaction between proximate ecological conditions and individual demographic factors.
Linnaeus' original scientific description of Lemur catta, the ringtailed lemur, was based on a living animal brought to England in 1749. Although there were many brief descriptions of wild ringtailed lemurs, it was not until Jolly wrote her now classic book, Lemur Behavior, that we had our first detailed description of the natural history of these beautiful animals (Fig. 1). Since then, long-term field studies, mainly from two study sites in Madagascar, Berenty and Beza Mahafaly (Fig. 2), as well as studies on forest-living groups in captivity at the Duke University Primate Center in Durham, North Carolina, have greatly expanded our knowledge of the ecology and behavior of this species (Table 1, Box 1). Thirty-five years of research on this species at these various sites indicates that Lemur catta is proving to be every bit as complex in its behavior as are many anthropoid primates. This very complexity has been reflected in the current controversies and questions concerning the ecology and behavior of this species.
The social development of 11 free-ranging infantLemur catta was examined over the first 16 weeks of the infants' lives. By 16 weeks, infants still occasionally suckled and were carried dorsally, but on the whole, they were independent of their mothers. Sex or mother's rank was not found to affect frequency or type of play behavior. Mother's rank had no effect on frequency of maternal rejections, from the nipple or from riding, but female infants were rejected slightly more frequently than males were. Mothers tended to reject infants more severely and more frequently from dorsal riding than from the nipple. Sex and rank differences were not found with respect to behaviors determined as measures of independence; however, lower-ranking infants engaged in significantly more “dependent” behaviors than higher-ranking young did. It may be necessary for the infant of a low-ranking mother to maintain closer proximity to its mother for a longer period of time during infancy because such infants may be subject to abuse by higher-ranking group members and, furthermore, may not be as readily rescued in a stressful or dangerous situation as a higher-ranking infant. Sex was not found to be a factor in terms of measures of dependence. The lack of sex differences in developmental behaviors in this species may be related to female dominance, as well as to the fact that, as adults, both sexes engage in aggressive territorial behavirs.
Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
Large home ranges and extreme flexibility in ranging behaviors characterize most subarid dwelling haplorhines. However, the most comparable extant strepsirhine, Lemur catta, is characterized as having small home ranges with consistent boundaries. Since ranging studies on this species have been limited to gallery forest habitat, the author's goal is to identify ecological factors that affect range use of L. catta in one of the most resource-limited environments of its distribution. To conduct this study, ranging and behavioral data were collected on two nonoverlapping groups through all-day follows in the semidesert scrub environment of Cap Sainte-Marie (CSM), Madagascar. Data were collected from August 2007 through July 2008. Home range areas and day range lengths were generated using ArcGIS® 9.3. Other variables measured were habitat composition, diet richness, daily activity, and microclimate. Home range areas of CSM L. catta were very large relative to those of gallery forest L. catta, and there was great monthly variation. In contrast, day range lengths at CSM were either smaller than or approximated the size of comparative gallery forest groups. Temperature, sunning, and diet richness were associated with day range length for one but not for both groups and appear to be related to energy management needs. Based on these findings, the author suggests that L. catta is capable of extensive behavioral and ranging flexibility in the extremes of its environment. However, physiological constraints impose limitations that can interfere with its ability to adapt to even seemingly minor variations in microclimate and habitat structure within the same site. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.
Hypothesized relationships between milk composition and life history traits were examined by analyzing mid-lactation milks of seven lemurs (Eulemur fulvus, E. macaco, E. rubriventer, E. mongoz, Varecia variegata, Hapalemur griseus, Lemur catta), three bushbabies (Otolemur crassicaudatus, O. garnettii, Galago moholi), and two lorises (Nycticebus coucang, Loris tardigradus); partial data were also obtained for the lemuroid Cheirogaleus medius. There were significant differences in milk composition among species within either Eulemur or Otolemur, but the four genera for which multiple samples were available (Eulemur, Varecia, Otolemur, and Nycticebus) exhibited large composition differences. Eulemur milk was, on average, very dilute (9.9% dry matter) and low in energy (0.49 kcal/g). These milks contained 0.9% fat, 1.2% protein, and 8.4% carbohydrate on a fresh weight basis. Protein energy comprised only about 15% of total milk energy. Varecia had significantly higher dry matter (13.5%), fat (3.2%), protein (4.2%), gross energy (0.80 kcal/g), and protein energy: total energy ratio (28%) than Eulemur. Milks of the lorisoid genera Otolemur and Nycticebus were very similar, and both had significantly higher dry matter (18.3, 16.3%), fat (7.6, 7.0%), and gross energy concentration (1.27, 1.13 kcal/g) than either lemuroid genus. Otolemur milk was higher in protein than Nycticebus milk. We conclude that lorises, bushbabies, and perhaps cheirogaleids produce relatively rich, energy-dense milks in comparison with anthropoid primates. However, dilute milks appear to be uniformly found among species of Eulemur and perhaps in Lemur catta. The milk of Varecia (and perhaps Hapalemur) is intermediate in composition. Differences in milk composition among prosimians may be related to differences in maternal care: prosimians that carry their young during lactation produce more dilute milks than do species which leave their young unattended for prolonged periods. When looking at primates as a whole, however, the picture is somewhat less clear, since the milks of some “parkers” like Varecia do closely resemble those of large anthropoid primates who carry their young. Am. J. Primatol. 41:195–211, 1997. © 1997 Wiley-Liss, Inc.
Hooded seal pups are suckled for a total of four days; chimpanzees and elephants sometimes are suckled for as long as eight years. This enormous range suggests considerable diversity in reproductive strategies. Lactation represents early maternal effort, whereas weaning is the infant's transition to nutritional independence. Weaning behavior is thus important from two interconnected perspectives: that of the infant during this transition and that of the mother with the cessation of lactation and the resumption of her reproductive capacity. What controls such diversity in the duration of lactation? What are the consequences of this diversity for mothers in terms of reproduction and for infants in terms of their growth and survival? How are differences in lactation reflected in behavioral interactions? The answers to these questions involve consideration of weaning and growth, and have implications for life histories
To understand the evolutionary forces that have shaped primate lactation strategies, it is important to understand the proximate mechanisms of milk synthesis and their ecological and phylogenetic contexts. The lactation strategy of a species has four interrelated dimensions: the frequency and duration of nursing bouts, the period of lactation until weaning, the number and sex ratio of infants that a mother rears simultaneously, and the composition and yield of the milk that mothers synthesize. Milk synthesis, arguably the most physiologically costly component of rearing infants, remains the least studied. Energy transfer becomes energetically less efficient, transitioning from placental support to milk synthesis just as the energy requirements for infant growth, development, and behavioral activity substantially increase. Here we review primate lactation biology and milk synthesis, integrating studies from anthropology, biology, nutrition, animal science, immunology, and biochemistry, to identify the derived and ancestral features of primate milks and enhance our understanding of primate life history.
The last decade's lemur research includes successes in discovering new living and extinct species and learning about the distribution, biogeography, physiology, behavior, and ecology of previously little-studied species. In addition, in both the dry forest and rain forest, long-term studies of lemur demography, life history, and reproduction, have been completed in conjunction with data on tree productivity, phenology, and climate. Lemurs contrast with anthropoids in several behavioral features, including female dominance, targeted female-female aggression, lack of sexual dimorphism regardless of mating system, sperm competition coupled with male-male aggression, high infant mortality, cathemerality, and strict seasonal breeding. Hypotheses to explain these traits include the "energy conservation hypothesis" (ECH) suggesting that harsh and unpredictable climate factors on the island of Madagascar have affected the evolution of female dominance, and the "evolutionary disequilibrium hypotheses" (EVDH) suggesting that the recent megafauna extinctions have influenced lemurs to become diurnal. These hypotheses are compared and contrasted in light of recent empirical data on climate, subfossils, and lemur behavior. New data on life histories of the rain forest lemurs at Ranomafana National Park give further support to the ECH. Birth seasons are synchronized within each species, but there is a 6-month distribution of births among species. Gestation and lactation lengths vary among sympatric lemurs, but all lemur species in the rain forest wean in synchrony at the season most likely to have abundant resources. Across-species weaning synchrony seen in Ranomafana corroborates data from the dry forest that late lactation and weaning is the life history event that is the primary focus of the annual schedule. Lemur adaptations may assure maximum offspring survival in this environment with an unpredictable food supply and heavy predation. In conclusion, a more comprehensive energy frugality hypothesis (EFH) is proposed, which postulates 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 use of scarce resources (e.g., cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony). Among primates, the isolated adaptive radiation of lemurs on Madagascar may have been uniquely characterized by selection toward efficiency to cope with the harsh and unpredictable island environment.
Over 15 field seasons (1987-2001), we collected census and life-history data on a population of individually identified ring-tailed lemurs at the Beza Mahafaly Reserve, Madagascar. No significant difference was found in population size over the study period, though a marked decline in the population occurred following a 2-year drought. The population rebounded rapidly after the immediate postdrought period. There was nearly a complete replacement of individuals over the study period. Average group size is 11.5 animals, and adult male to female sex ratio is 0.92. Most females reproduce annually, and the average fecundity rate is 84.3%. The greatest variability in fecundity is found among old females. We suggest that ring-tailed lemur females follow an "income breeding" strategy, i.e., females use maximum resources during reproduction rather than relying on fat stores, as do "capital breeders." Infant mortality to 1 year of age in a nondrought year is 52%, higher than infant mortality in small to medium-sized anthropoids. The oldest known female was 18 years old in 2001. We suggest that 18-20 years may represent the maximum life-span for wild ring-tailed lemurs. Because males regularly emigrate from the population, we have no data regarding male life-span; however, there is some indication that males do not survive as long as females. Group fission has occurred three times: twice from one parent group living in the driest area of the reserve, with the most dispersed food resources. We suggest that the reproductive strategy that has evolved in this species, wherein females reproduce early in life and annually until old age, is a response to the unusual climate and environmental conditions under which Lemur catta has evolved.
Data collected on the feeding behavior, food intake, and chemical analyses of plant foods were used to document seasonal variation in diet and nutrition in Eulemur mongoz in northwestern Madagascar. E. mongoz conforms to the general Eulemur dietary pattern, with a predominantly frugivorous diet supplemented mainly by leaves, flowers, and nectar. Phytochemical analysis revealed high water contents in all the main plant foods; mature fruit and flowers contained the most water-soluble carbohydrates; immature leaves were richest in protein and essential amino acids; the limiting amino acids in all plant foods were methionine and cystine; ash (mineral) content was highest in petioles and mature leaves; crude lipid content was highest in seeds; and crude fiber content was indistinguishable between immature and mature fruit and leaves. High-fiber foods were eaten during both seasons; the wet season diet was dominated by high-energy foods (mature fruit, nectar, and seeds), while the dry season diet contained foods high in energy (mature fruit and flowers) and high in protein (immature leaves) and minerals (mature leaves and petioles). However, nutrient intake did not vary between seasons, implying that nutrient requirements are met throughout the year. These results suggest we draw more conservative conclusions when interpreting dietary variability in the absence of chemical analysis, and also draw into question the idea that nutritional stress is a factor in the timing of reproduction in lemurs and, by extension, is linked to the prevalence of female dominance and small group size in lemurs.
The puzzle of female feeding priority
- A Jolly
Jolly A (1966). Lemur Behaviour: A Madagascar Field Study. Chicago, University of Chicago Press.
Jolly A (1984). The puzzle of female feeding priority. In Female Primates (Small M, ed.), pp 197-215. New
York, Liss.
The spiny forest ecoregion
- M Fenn
Fenn M (2003). The spiny forest ecoregion. In The Natural History of Madagascar (Goodman S, Benstead
J, eds.), pp 1525-1530. Chicago, University of Chicago Press.
of California San Diego 137.110
- Univ
Univ. of California San Diego
137.110.39.88 -2/2/2017 7:20:06 PM
Folia Primatol 2015;86:16–24
DOI: 10.1159/000369580
Mammalian reproductive physiology: adaptive responses to changing environments
- N Negus
- P Berger
Negus N, Berger P (1987). Mammalian reproductive physiology: adaptive responses to changing environments. In Current Mammalogy (Genoways HH, ed.), pp 149-173. New York, Springer.