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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?

May 2015
Folia Primatologica 86(1-2):16-24

DOI:10.1159/000369580

Source
PubMed

Authors:

Lisa Gould

University of Victoria

Elizabeth A Kelley

Saint Louis Zoo

Marni LaFleur

University of San Diego

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.

Location of the 3 study sites in southern and southwestern Madagascar. NP = National Park. Map data: Google Earth, SIO, NOAA, U.S. Navy, NGA, GEBCO, Landsat.

…

. Years of the studies, data collection hours, mean daytime temperatures, maximum temperatures during the hot early-to-mid lactation period, dominant plant genera and absence/presence of drinking water

…

. Plant species most frequently consumed by females at the 3 sites during reproductive periods

…

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Original Article

Folia Primatol 2015;86:16–24

DOI: 10.1159/000369580

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?

Lisa Gould a Elizabeth A. Kelley b Marni LaFleur c

a University of Victoria, Victoria, B.C. , Canada;

b St. Louis University, St. Louis, Mo. , USA;

c University of Veterinary Medicine, Vienna , Austria

Key Words

Lemur catta · Reproductive females · Feeding strategy · Spiny forest

Abstract

The spiny forest ecoregion of southern and southwestern Madagascar is character-

ized 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 repro-

ductive females living in spiny forests, gestation and early-to-mid lactation periods oc-

cur 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 wa-

ter 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.

Lisa Gould

Department of Anthropology

University of Victoria

Victoria, BC V8W 2Y2 (Canada)

E-Mail Lgould  @  uvic.ca

0015–5713/15/0862–0016$39.50/0

www.karger.com/fpr

E-Mail karger@karger.com

Published online: May 19, 2015

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Reproductive Female Feeding Strategies in Spiny

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Folia Primatol 2015;86:16–24

DOI: 10.1159/000369580

Introduction

The endangered Lemur catta is known for its remarkable ecological flexibility,

an adaptation that arose in response to the extreme climate and food resource sea-

sonality throughout its geographic range [Jolly, 1984; Sauther, 1998; Sauther et al.,

1999; Wright, 1999; Goodman et al., 2006; Gould, 2006]. L. catta is found in 7 dis-

tinct habitats throughout southern, southwest and south-central Madagascar

[Goodman et al., 2006; Gould, 2006; Gould et al., 2015]. One of these, the spiny for-

est/spiny bush, is characterized by sparse ground cover, an absence of canopy with

maximum tree height rarely exceeding 6 m, low rainfall (mean <500 mm/year),

temperatures exceeding 45

 °  C in the hot season and little to no standing water

[Fenn, 2003; Charrier et al., 2007; Tengo et al., 2007; Gould et al., 2011; Kelley,

2011].

Beehner et al. [2006] note that environmental conditions are a key variable in

reproductive success or failure, relating that after droughts and periods of intense

heat in Amboseli, female baboons (Papio cynocephalus) were less likely to conceive

or gestate successfully. Yet for many Malagasy primates, strict reproductive season-

ality means gestating and giving birth during a lengthy dry season [Jolly, 1984;

Wright, 1999], and for L. catta often during drought periods [Gould et al., 1999]. L.

catta births in all southern Madagascar habitats occur in September/October when

food resources are relatively scarce, the hot season sets in, and daily temperatures

begin to increase, often into the >40

 °  C range [Jolly, 1966, 1984; Gould, 1990; Sau-

ther, 1998; Sauther et al., 1999; Gould et al., 2011; Kelley, 2011; LaFleur, 2012]. Fe-

males residing in spiny forest face the challenge of obtaining nutritious foods and

adequate water intake to support sufficient milk production for rapidly growing

offspring in a habitat with no shade, no standing water in most locales, and very

high temperatures during the early-to-mid lactation season [Gould et al., 2011; Kel-

ley, 2011].

Here, we compare variables related to feeding ecology and nutrient consump-

tion in reproductive female L. catta inhabiting spiny forest at three sites in southern

Madagascar. We ask: how do females cope with the nutritional and hydration de-

mands of gestation and lactation in spiny forest habitat? Malagasy primate diets

tend to be fibrous [Wright, 1999], and fiber consumption can inhibit protein uptake

[Chapman et al., 2002]; however, protein requirements increase during reproduc-

tive periods [Lee, 1996; Jessop, 1997]. In gallery-forest-dwelling L. catta and Eule-

mur mongoz , reproductive females tend to seek out high-protein foods [Sauther,

1994; Curtis, 2004], and in Varecia rubra, pregnant and lactating females consume

foods with a higher protein-to-fiber (P/F) content [Vasey, 2002]. Thus, we predict

that (1) foods most frequently consumed by reproductive females in our sample will

exhibit a high P/F ratio, and (2) lactating females will consume foods containing a

higher water content compared to those eaten in the early gestation period, given

the above-mentioned environmental conditions in spiny forest habitat during the

birth season. We also examine between-site differences in P/F ratios and water con-

tent of most frequently consumed foods, and between-site overlap in frequently

consumed plant species that can be considered important in meeting reproductive

demands, e.g. high P/F ratio and high water content.

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18 Gould  /Kelley  /LaFleur 

Methods

Study Sites

Research was conducted by L.G. at Berenty spiny forest (25°01′13 S, 46°18′23 E; hereafter

referred to as BSF), by E.A.K. at Cap Sainte-Marie (CSM; 25°30′59 S, 45°07′92 E) and by M.L. at

Tsimanampesotse National Park (TNP; 24°03′24 S, 43°46′43 E; fig.1 ). See table1 for mean and

maximum daily temperatures, rainfall and dominant vegetation at the study sites.

Data Collection and Analysis

Continuous-time focal animal data [Altmann, 1974] were collected on all adult females in

2 troops at BSF (n = 6) and CSM (n = 9) during the early gestation season, (June/July) and the

early-to-mid lactation period (September/October), and on adult females in 3 groups during the

early-to-mid lactation period at TNP (n = 13). See table1 for study dates and the number of focal

animal hours collected. Detailed data collection methods used for each study can be found in

Gould et al. [2011], Kelley [2013] and LaFleur et al. [2013].

Fig. 1. Location of the 3 study sites in southern and southwestern Madagascar. NP = National

Park. Map data: Google Earth, SIO, NOAA, U.S. Navy, NGA, GEBCO, Landsat.

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Reproductive Female Feeding Strategies in Spiny

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DOI: 10.1159/000369580

All plant food items consumed by each focal animal were recorded, as well as time spent

feeding on each plant food, and plant food species were identified (1) via a herbarium at the

Berenty field site, (2) at Missouri Botanical Gardens, St. Louis, for CSM plants, and (3) by botanist

Bakira Ravorona for TNP plants. Multiple samples of all plant parts ingested were collected from

the same feeding sites on the same days that they were consumed, and samples were shade-dried

for nutrient analysis. Food intake rates per minute were calculated for each animal thus: total

number of items of each plant food consumed/total minutes focal animal spent feeding.

Nutritional assays for protein and acid detergent fiber content of plant foods consumed by

the lemurs were conducted by (1) Smithsonian National Zoological Park nutrition laboratory

(BSF samples), (2) Dairy One Forage Laboratory, Ithaca, N.Y. (CSM) and (3) University of Ham-

burg, Department of Zoology (TNP). We calculated P/F ratios for the 4 or 5 most frequent-

ly consumed plant foods in each reproductive season thus: percent protein (dry matter per

gram) – percent fiber (dry matter per gram)

The water content of most frequently consumed plant foods at BSF and CSM was deter-

mined by calculating the mean wet weight of 20 samples of a specific food item, then drying

samples thoroughly and calculating the mean dry weight.

Wet weight – dry weight = water content in grams. Water content data of top plant foods

were not collected at TNP.

L.G.’s research at BSF complied with protocols approved by the University of Victoria’s Ani-

mal Care Committee. E.A.K.’s research was conducted with Institutional Animal Care Committee

approval from the Saint Louis Zoo and Washington University, and Institutional Animal Care Com-

mittee approval was obtained from the University of Colorado Boulder in the case of M.L.’s research.

R e s u l t s

P/F Ratios

The plant foods most frequently consumed by females at BSF during the early

gestation period all exhibit a higher P/F content as compared to CSM ( table2 ). One

CSM plant, Paederia foetida , was especially high in protein ( table2 ). Comparing P/F

ratios between the 2 sites, the plant foods most frequently consumed by females at

BSF exhibited significantly higher P/F ratios compared with those consumed at CSM

during the early gestation period (Mann-Whitney: U = 18, p = 0.05).

Table 1. Years of the studies, data collection hours, mean daytime temperatures, maximum temperatures during

the hot early-to-mid lactation period, dominant plant genera and absence/presence of drinking water

BSF CSM TNP

Data collection years and hours of focal

animal data collected on reproductive

females

September/October 2006

(131 h)

June/July 2007 (69 h)

September/October 2007

(39 h)

June/July 2008 (27 h)

September/October 2010

(60 h)

Gestation mean daytime temperature 23.5 ° C 29.7 ° C No data

Early-to-mid lactation mean daytime

temperature + maximum recorded

36 ° C (max. 43.7°) 34.1 ° C (max. 46.7°) 34.8 ° C (max. 39.4°)

Dominant plant genera Alluaudia, Euphorbia,

Gyrocarpus, Salvadora

Euphorbia, Opuntia,

Alluaudia, Aloe Euphorbia, Alluaudia,

Adansonia, Ficus,

Gyrocarpus

Drinking water source within home

range?

Closest 3 km

Closest 33 km

Yes

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20 Gould  /Kelley  /LaFleur 

No significant differences in P/F ratios were found when comparing most fre-

quently consumed plant foods across the 3 sites during the early-to-mid lactation

period (Kruskal-Wallis: χ

2 = 0.88, d.f. = 2, p = 0.64; table2 ). 80% of most commonly

consumed plants at BSF, and 60% of those at CSM and TNP, had a high P/F content

(50% or greater).

Water Content

A between-site comparison (BSF and CSM) of water content of most frequently

consumed plant foods revealed no significant difference in either period (early gesta-

tion: U = 13.5, p = 0.76; early/mid lactation, U = 20, p = 0.08), nor did we find any

within-site, between-season differences (BSF, U = 23, p = 0.28; CSM, U = 20.5, p =

0.06.). However, at CSM, there is a trend towards greater water content in plants con-

sumed during the early-to-mid lactation period.

Table 2. Mean P/F ratios and water content of the most frequently consumed plant species during reproductive

periods

Study

site

P/F ratios of most frequently consumed plant species Water content of most frequently consumed plant species, %

early gestation period early/mid lactation period early gestation period early/mid lactation period

BSF Paedera foetida YL 0.86 Gyrocarpus americanus FR,

YL 1.37

Paedera foetida 60% Gyrocarpus americanus

76%

Mixed vine YL 1.13

Tamarindus indica FR, YL 1.7

Mixed vine 41%

Tamarindus indica 88.5%

Metaporana parvifolia YL

1.08

Seyrigia gracilis YL 0.4 Metaporana parvifolia 25% Seyrigia gracilis 76%

Agave sisalana pulp 1.02 Alluaudia procera YL 0.5 Agave sisalana 86% Alluaudia procera 72%

Salvadora angustifolia FL 0.9 Salvadora angustifolia

60%

mean = 1.02 mean = 0.97

CSM Opuntia stricta FR 0.17 Opuntia stricta FR 0.17 Opuntia stricta 82% Opuntia stricta 85%

Opuntia monocantha

FR 0.3

Aloe vahombe LV 0.99 Opuntia monocantha 85% Aloe vahombe 91%

Paederia foetida YL 1.03 Phyllanthus amarus FR 1.51 Paederia foetida 69% Phyllantus amanu 69%

Metaporana sp. YL 0.54 Alluaudia procera LV 0.84 Metaporana sp. 53% Alluaudia procera 82%

Grewia cyclea FR 0.18 Grewia cyclea 25%

mean = 0.44 mean = 0.88

TNP Neobeguea mahafaliensis FL,

YL 0.97

Gyrocarpus americanus FR,

LV 1.29

Olax androyensis FR 1.28

Ficus marmorata FR 0.17

Diospyros manapetsae FR 0.18

mean = 0.78

Nutrition data for TNP collected only during early/mid lactation, and water content data were not collected at this site.

YL = Young leaves; FR = fruit; LV = mature leaves; FL = flowers.

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Diet Overlap between Sites

We found some overlap in the 5 most frequently consumed plant species at CSM

and BSF during the early gestation period, with 2 species, P. foetida and Metaporana

parvifolia, consumed in relatively high proportions at both sites ( table3 ). During the

early-to-mid lactation period, Alluaudia procera was a commonly consumed species

at both BSF and CSM, and Gyrocarpus americanus was an important species for fe-

male L. catta at BSF and TNP ( table3 ). No overlap in top food plant species was found

between CSM and TNP.

Discussion

L. catta females are considered ‘income breeders’ [Gould et al., 2003] and must

rely on resources obtained from the environment rather than on body fat during re-

productive periods. In an arid, hot spiny forest habitat with little shade, how do fe-

males maintain sufficient body condition (e.g. nutrients and water) to support both

pregnancy and milk production? Mean P/F ratios of most commonly consumed

foods at our sites exceed the means (0.21–0.48) found in lemur plant foods in dry de-

ciduous and gallery forest habitats in Madagascar [Ganzhorn, 1992; Simmen et al.,

2014]. P/F ratios of the most frequently consumed plants were more favorable at BSF

compared to those at CSM during the early gestation season; however, the mean P/F

ratio for that period at CSM (0.44) is on the higher end of those reported by Ganzhorn

[1992] and Simmen et al. [2014]. At all sites, mean P/F ratios of preferred plant foods

were high during the early-to-mid lactation period (range 0.78–0.97), thus lactating

female protein absorption was likely not adversely affected by fiber consumption at

the onset of milk production.

Table 3. Plant species most frequently consumed by females at the 3 sites during reproductive periods

BSF CSM TNP

Most frequently consumed plant species: early gestation period

Paederia foetida (30%)*Opuntia stricta (20%)

Metaporana parvifolia (18.3%)*Opuntia monocantha (16.7%)

Agave sisalana (7.1%) Paederia foetida (14.3%)*

Mixed vine leaves (6.5%) Metaporana parvifolia (12%)*

Grewia cyclea (7.1%)

Most frequently consumed plant species: early-to-mid lactation period

Gyrocarpus americanus (33%)*Opuntia stricta (25.6%) Neobeguea mahafaliensis (56%)

Tamarindus indica (19%) Aloe vahombe (14.6%) Gyrocarpus americanus (29.5%)*

Seyrigia gracilis (15%) Phyllanthus amarus (9.6%) Olax androyensis (10%)

Alluaudia procera (13%)*Alluaudia procera (7.3%)*Ficus marmorata (4%)

Salvadora angustifolia (10%) Gymnosporia linearis (5.5%)

Values in parentheses represent percentages of diet devoted to consumption of these plants. Species

marked with asterisks were consumed by reproductive females at >1 site.

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22 Gould  /Kelley  /LaFleur 

While L. catta females produce comparatively dilute milk [Tilden and Oftedal,

1997; Power et al., 2006; Hinde et al., 2011], they likely produce large quantities to

nourish and hydrate infants in spiny forest habitat. The mean annual rainfall at gallery

forest sites in south and southwest Madagascar ranges from 580 to 700 mm/year

[Koyama et al., 2006; Sussman et al., 2012]; however, rainfall in spiny forest habitat

averages less than 500 mm/year [Tengo et al., 2007; Kelley, 2011]. Furthermore, health

assessment of the CSM population in 2007 revealed low hydration levels [Kelley,

2011]. Negus and Berger [1987] note that for many mammals inhabiting xeric envi-

ronments, temporal availability of water can regulate reproductive timing. Yet for L.

catta at BSF and CSM, external water sources only become available at the onset of the

rainy season, which corresponds to the mid-to-late lactation period when weanlings

begin to eat solids. To compensate, L. catta females in xeric spiny habitat focus on

plant foods high in water content during the hot early-to-mid lactation period even

though some (e.g. Opuntia ) exhibit relatively unfavorable P/F concentrations. Al-

though not statistically significant, the water content of top food plant species at both

CSM and BSF was never less than 60% in the hotter early-to-mid lactation period com-

pared with plants consumed during the cooler early gestation months, which could be

as low as 25% ( table2 ). At CSM, frequent consumption of Opuntia , Aloe and Alluau-

dia, all exceptionally high in water content, can be viewed as key to reproductive fe-

male hydration in a markedly open habitat with no canopy whatsoever.

At both BSF and CSF, pregnant females consumed P. foetida and M. parvifolia

frequently. Both plants produce young leaves in the early gestation period, which are

easy to access, grow in abundance and are high in protein. Lactating females at BSF

and CSM frequently consumed A. procera leaves. A. procera is a deciduous succulent,

with leaves and flowers high in water content ( table2 ), thus a useful resource when

temperatures rise during the early lactation period. G. americanus was preferentially

consumed by females at BSF and TNP, and exhibited markedly high P/F ratios and

high water content. All of these plant species can be considered important to the body

maintenance of L. catta females when pregnant and lactating.

We suggest that by choosing plant foods high in protein or with relatively com-

parable P/F content, and having access to water through the hot early-to-mid lacta-

tion period (through foods consumed at BSF and CSM or via cave and sinkhole water

sources at TNP) female L. catta in spiny forest habitat are able to successfully repro-

duce and lactate for rapidly growing infants at the end of a challenging dry season.

One important factor in the evolution of ecological flexibility of L. catta may relate to

female choice of specific plant foods in diverse habitats that will meet reproductive

demands and promote infant survival.

Acknowledgments

Research permission was obtained from the Département des Eaux et Forêts Madagascar

(all authors), as well as the de Heaulme family (L.G.), the MNP team at CSM (E.A.K.) and Mad-

agascar National Parks and University of Toliara (M.L.). Funding was provided by grants from

the Natural Sciences and Engineering Research Council of Canada (L.G.), St. Louis Zoo, Lambda

Alpha, National Science Foundation (NSF-0752334) and Primate Conservation Inc. (E.A.K.),

and a Natural Sciences and Engineering Research Council of Canada postgraduate scholarship,

and grants from NSF (1028708), National Geographic Society, American Society of Primatolo-

gists and University of Colorado (M.L.).

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DOI: 10.1159/000369580

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Feeding ecology and conservation biology of the black snub-nosed monkey (Rhinopithecus strykeri)

Thesis

Full-text available

Jun 2019

Tiger Yang

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.

Lemur catta in small forest fragments: Which variables best predict population viability?

Article

Jan 2020

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.

Essential Oil Composition of Alluaudia procera and in Vitro Biological Activity on Two Drug-Resistant Models

Article

Full-text available

Aug 2019
MOLECULES

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.

First insights into the feeding habits of the Critically Endangered black snub-nosed monkey, Rhinopithecus strykeri (Colobinae, Primates)

Article

Full-text available

Mar 2019
PRIMATES

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.

Patterns of Behaviour, Group Structure and Reproductive Status Predict Levels of Glucocorticoid Metabolites in Zoo-Housed Ring-Tailed Lemurs, Lemur catta

Article

Jan 2016
FOLIA PRIMATOL

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.

The Season for Peace: Reconciliation in a Despotic Species (Lemur catta)

Article

Full-text available

Nov 2015
PLOS ONE

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

Ring-Tailed Lemurs: A Species Re-Imagined

Article

Full-text available

May 2015
FOLIA PRIMATOL

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.

Plant Species Fed on by Wild Ring-Tailed Lemurs (Lemur catta) at Nine Sites

Article

Full-text available

Feb 2021
INT J PRIMATOL

Stephanie L. Canington

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.

Going, going, gone. Is the iconic ring-tailed Lemur (Lemur catta) Headed for Imminent Extirpation?

Article

Jan 2016

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.

The distribution and biogeography of the ring-tailed lemur (Lemur catta)

Article

Full-text available

Jan 2006

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.

Feeding strategy and social dominance in female Sifakas (Propithecus v. verreauxi) living in a Didiereaceae forest in southern Madagascar

Article

Full-text available

Jan 2007
REV ECOL-TERRE VIE

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.

Home ranges of ring-tailed lemur troops and the density of large trees at Berenty Reserve, Madagascar

Article

Full-text available

Jan 2005

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.

Stratégie alimentaire et dominance des femelles propithèque de verreaux (Propithecus v. verreauxi) dans la forêt à Didiereaceae du sud de Madagascar

Article

Full-text available

Jan 2007

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.

Leaf Chemistry as a Predictor of Primate Biomass and the Mediating Role of Food Selection: A Case Study in a Folivorous Lemur ( Propithecus verreauxi)

Article

Full-text available

Jun 2014
AM J PRIMATOL

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 in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: Camera trap data and preliminary behavioral observations

Article

Full-text available

Oct 2013

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.

Lemur catta in small forest fragments: Which variables best predict population viability?

Article

Jan 2020

Lemur traits and Madagascar ecology: Coping with an island environment

Article

Jan 1999
YEARB PHYS ANTHROPOL

Patricia Wright

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.

Patterns of milk composition in prosimian primates

Article

Aug 2006

The ecology of conception and pregnancy failure in wild baboons

Article

Jun 2006

Jacinta C. Beehner

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.