ArticlePDF Available

Seasonal Feeding Ecology of Ring-Tailed Lemurs: A Comparison of Spiny and Gallery Forest Habitats

Authors:

Abstract

Although Lemur catta persists in many habitat types in southern Madagascar, its ecology has been primarily studied within gallery forests. We compare plant food selection and properties for ring-tailed lemurs in the spiny and gallery forests over the synchronized lactation period (September to March) that includes both the dry and wet seasons. We found no significant habitat-specific differences in the type of plant part consumed per month (i.e. flower, fruit, leaf) or between the intake of soluble carbohydrates. However , the presence and use of Tamarindus indica plants appear to elevate protein and fiber intake in the gallery forest lemurs' diets. Protein is especially important for reproductive females who incur the added metabolic costs associated with lactation; however, fiber can disrupt protein digestion. Future work should continue to investigate how variations of protein and fiber affect ring-tailed lemur dietary choice and nutrient acquisition.
Original Article
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
Seasonal Feeding Ecology of Ring-Tailed
Lemurs: A Comparison of Spiny and Gallery
Forest Habitats
Marni LaFleur a Michelle L. Sauther b
a Institut für Populationsgenetik, University of Veterinary Medicine, Vienna , Austria;
b Department of Anthropology, University of Colorado, Boulder, Colo. , USA
Key Words
Madagascar · Plant foods · Habitat types · Bezà Mahafaly Special Reserve ·
Tsimanampesotse National Park · Macronutrients · Plant chemistry
Abstract
Although Lemur catta persists in many habitat types in southern Madagascar, its
ecology has been primarily studied within gallery forests. We compare plant food selec-
tion and properties for ring-tailed lemurs in the spiny and gallery forests over the synchro-
nized lactation period (September to March) that includes both the dry and wet seasons.
We found no significant habitat-specific differences in the type of plant part consumed
per month (i.e. flower, fruit, leaf) or between the intake of soluble carbohydrates. How-
ever, the presence and use of Tamarindus indica plants appear to elevate protein and fiber
intake in the gallery forest lemurs’ diets. Protein is especially important for reproductive
females who incur the added metabolic costs associated with lactation; however, fiber
can disrupt protein digestion. Future work should continue to investigate how variations
of protein and fiber affect ring-tailed lemur dietary choice and nutrient acquisition.
© 2015 S. Karger AG, Basel
Introduction
Lemur catta (the ring-tailed lemur) is a remarkably flexible edge or weed species
[Sussman, 1977; Gould et al., 1999; Sauther et al., 1999] that persists in a variety of
habitats in southwestern Madagascar including spiny and xerophytic forests, gallery
and deciduous forests, anthropogenically induced savanna, scrub and brush land,
rocky outcrop vegetation, and the mesic high-altitude forests of the Andringitra
mountain range [Goodman et al., 2006]. Each of these habitat types likely presents
Marni LaFleur
Institut für Populationsgenetik
University of Veterinary Medicine, Vienna
Veterinärplatz 1 , AT–1210 Wien (Austria)
E-Mail marni.lafleur @ gmail.com
© 2015 S. Karger AG, Basel
0015–5713/15/0862–0025$39.50/0
www.karger.com/fpr
E-Mail karger@karger.com
Published online: May 19, 2015
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
26 LaFleur /Sauther
unique challenges in terms of finding food, water and shelter. Given that a few stud-
ies have now focused on ring-tailed lemur’s ecology in non-gallery-forest habitats
[Gould et al., 2011; Kelley, 2013; Gabriel, 2013], it is now possible to compare across
habitats to better understand how proximate variables affect ring-tailed lemur behav-
ior, nutrition and, ultimately, fitness [Gould, 2006].
Ring-tailed lemurs are opportunistic frugivores/folivores, and although they
consume varied and diverse plant-based foods throughout the year, their diet at a
given time tends to be dominated by a few species [Sauther, 1994, 1998]. Forests in
southern Madagascar are extremely seasonal, and animals must cope with a long dry
season, wherein food resources are scarce. Female ring-tailed lemurs are in the late
gestation and early lactation periods in the dry season, and thus have the added met-
abolic burden of reproduction when food resources are already low [Jolly, 1984; Sau-
ther, 1994, 1998].
In two different forest types (spiny and gallery), we examined the feeding behav-
ior of ring-tailed lemurs and the nutritional content of their plant foods to understand
relationships between habitat type and (1) plant food species and plant part con-
sumed, and (2) plant content of macronutrients (crude protein, soluble carbohy-
drates) and fiber (acid-detergent fiber, ADF). We predicted that gallery forest lemurs
would have access to higher-quality plant foods including young leaves, fruits and
flowers, and that both plant parts and the overall nutritional content of their plant
foods would be higher in soluble carbohydrates and crude protein, but lower in ADF.
We made these predictions knowing that when compared to spiny forests, gallery
forests have higher precipitation (and related net primary productivity), and support
higher densities of lemurs [see Kelley, 2013, and references therein], which suggests
a better-quality resource base.
Methods
Study Sites
The Tsimanampesotse National Park, TNP (24.09° S, 43.83° E; 5 km inland from the Mo-
zambique Channel) and Bezà Mahafaly Special Reserve, BMSR (23.67° S, 44.60° E; 140 km inland
from the Mozambique Channel) are both on the Mahafaly Plateau of southwestern Madagascar.
Both sites are highly seasonal with the vast majority of rainfall occurring between November and
April. In this paper, we compare data collected between September and March.
Tsimanampesotse National Park. Data were collected between 2010 and 2011 in the dry spiny
dwarf forests that do not have canopy cover (M.L.). Annual rainfall is usually under 300 mm, and
the dry season may be longer than that of the BMSR [Donque, 1975]. The following plant families
are most common at TNP: Euphorbiaceae, Didiereaceae, Bombacaceae and Fabaceae. Tamarind
trees are present at TNP, but at a low density, and the ring-tailed lemurs do not use tamarind re-
sources to the same extent as they do in gallery forest habitats as the trees are not asynchronous
and thus only provide fruits or leaves during discrete periods at TNP [LaFleur, 2012].
Bezà Mahafaly Special Reserve. Data were collected in the riverine forests of Parcel 1 during
1987–1988 (M.L.S.). This region has an average annual rainfall of 470 mm [Ratsirarson and Rich-
ard, 2010]. BMSR habitats contain high, closed canopy forest, which abuts the ephemeral Saka-
mena River, and are dominated by Fabaceae (particularly Tamarindus indica ) as well as trees
from the families Meliaceae, Salvadoraceae and Rubiaceae. The dry season dramatically reduces
food availability [Sauther, 1998; Yamashita, 2002; Whitelaw, 2010]. This habitat is dominated by
T. indica which is a particularly important resource for these ring-tailed lemurs as the trees pro-
duce leaves, flowers and fruits year-round and asynchronously [Sauther et al., 1999; Yamashita,
2002, 2008; Sauther and Cuozzo, 2009].
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Lemur catta Seasonal Habitats and Feeding
27
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
S t u d y S p e c i e s
Lemur catta is a semiterrestrial, group-living species with strict female dominance [Jolly,
1966]. It exhibits restricted seasonal reproduction with an annual mating period in April or May,
depending on locality. Infants are born from late September through early October, and repro-
ductive females lactate during the later portion of the dry season and well into the wet season
[Sauther et al., 1999].
Behavioral Data Collection
Diurnal scan sampling data [Altmann, 1974] were collected at 5-min intervals for all visible
adult animals in the focal group. At BMSR, all focal animals (n = 16 from 2 groups) had existing
nylon collars with unique tags [see Sussman et al., 2012]. At TNP, 6 ring-tailed lemurs from 3
distinct social groups were captured and fitted with radio tracking collars (MOD-080 transmitter
configuration, Telonics Inc.) [for protocol, see Sauther and Cuozzo, 2008]. In total, the TNP adult
focal animals ranged between 19 and 22 individuals from 2 groups (M.L. was unable to habituate
the third group).
Plant Food Data
When individual lemurs were feeding, the plant species and part were noted. Representative
plant foods were collected and dried in the shade (TNP) or in a Coleman camp oven (BMSR), be-
fore being transported to the Department of Animal Ecology and Conservation at Hamburg Uni-
versity in Germany for chemical analyses. Assays of each plant include analyses of crude protein,
soluble carbohydrates and ADF (analytical procedures as per those outlined by Ganzhorn [1988]).
Abiotic Data
We measured the millimeters of rainfall daily at BMSR (September to March 1987–1988)
and TNP (September to March 2010–2011).
Data Analyses
We compared the most frequently consumed plants and plant parts at each study site for each
month of both studies. Of the top 5 most frequently consumed plant foods per month at each site,
we created an index of each nutritional component measured using the following formula:
nutritional content index = ∑
foods 1–5 (percent of top 5 foods consumed · percent of content
in food).
We used a 1-way ANOVA to detect significant differences between the two habitats with
regard to the proportions of plant parts (i.e. leaf, flower, fruit) selected by focal animals, the nu-
tritional content for plant parts (leaves, flowers, fruits) and the overall nutritional content (crude
protein, soluble carbohydrates) or fiber indices of the plant foods. ADF content was not obtained
for T. indica fruits because of methodological problems with the samples. In order to account for
the fiber content present in tamarind fruits, we carried out calculations using the literature value
of 7.6% [Gould et al., 2011]. For all tests, significance was set at the α 0.05 level using a 2-tailed
distribution with values approaching p = 0.05 (e.g. p = 0.051) being rounded down [Weiss, 2011].
R e s u l t s
The BMSR received about twice the amount of precipitation of TNP during the
study periods (BMSR = 506.7 mm, TNP = 232.9 mm; fig.1 ). Moreover, the BMSR
received at least some precipitation in 7 of the 8 months studied, while the TNP only
received rain in 4 of the 8 months.
We compared approximately 10,000 scan sample scores at each field site between
the months of September and March. All plant foods consumed by the ring-tailed le-
murs were noted, and the 5 most frequently consumed foods per month are compared
here. Comparison of gallery (BMSR) and spiny (TNP) forest ring-tailed lemur plant
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
28 LaFleur /Sauther
food species, plant part, percentage of top 5 foods, plant nutritional properties (crude
protein, carbohydrates and ADF) and the total percentage of the diet that the top 5
foods constitute for that month are presented in table1 . We found no significant site-
specific differences in the type of plant part consumed per month (flower f = 3.998,
d.f.
total
= 13, p = 0.069; fruit f = 4.054, d.f.
total
= 12, p = 0.067; leaf f = 0.198,
d.f.
total
= 12, p = 0.664). In addition, we found no site-specific differences in the nutrient
value of plant parts used (protein f = 0.654, d.f.
total
= 5, p = 0.659; carbohydrate f = 1.146,
d.f.
total
= 5, p = 0.345; ADF f = 0.960, d.f.
total
= 5, p = 0.449). Of the top 5 foods consumed,
at the species level only Gyrocarpus americanus was found in each habitat, and at the
genus level, only Talinella was common to both the gallery and spiny forest ( table1 ).
BMSR TNP
Sep Oct Dec Jan Feb MarNov
Total rainfall (mm)
16.5
6.3
88.5
16
136.6
76.5 80.5
134.1 132.8
0
50.5
0
1.3 0
Fig. 1. Precipitation during the study periods (BMSR 1987–1988, TNP 2010–2011).
BMSR TNP
Sep Oct Dec Jan Feb MarNov
Crude protein (%)
28
13
32
20
27
12
21
13
23
17
41
10
21
16
Fig. 2. Index of crude protein in the top 5 plant foods (see Methods for nutritional index formula).
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Lemur catta Seasonal Habitats and Feeding
29
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
Location/month Plant species Plant part Percent
top 5
foods
Protein,
%
Carbo-
hydrates,
%
ADF,
%
BMSR
September Quisiavanthe papionae flowers 67 18.6 13.7 38.4
Tamarindus indica leaf buds 21 64.1 4.1 50.5
Tamarindus indica fruit 5 12.9 19.3 50.2
Gyrocarpus americanus flowers 4 46.9 7.1 17.0
(proportion Salvadora angustifolia young leaves 3 5.1 4.2 26.9
of total diet = 90%)
October Salvadora angustifolia fruit 55 12.9 15.5 16.1
Tamarindus indica leaf buds 27 22.1 12.7 5.6
Tamarindus indica fruit 12 6.4 1.3 44.2
Hildebrandtia sp. young leaves 3 7.1 9.4 40.2
(proportion Acalypha sp. young leaves 3 20.3 4.2 26.9
of total diet = 84%)
November Salvadora angustifolia fruit 78 64.1 4.1 50.2
Tamarindus indica leaf buds 9 12.9 19.3 50.5
Hildebrandtia sp. leaves 6 56.7 4.7 14.3
Talinella dolphinensis young leaves 4 17.0 4.9 31.7
(proportion Tamarindus indica fruit 4 28.4 5.7 13.2
of total diet = 89%)
December Tamarindus indica fruit 51 8.8 12.3 6.8
Hildebrandtia sp. leaves 28 11.1 15.9 15.8
Corralocarpus greveii young leaves 8 6.4 1.3 44.2
Gloriosa superba leaves, stems 7 15.8 3.5 37.4
(proportion Marsdenia sp. leaf buds 6 20.3 4.2 26.9
of total diet = 75%)
January Talinella dolphinensis fruit 51 64.1 4.1 50.2
Antidesma petiolare fruit 17 56.7 4.7 18.6
Hildebrandtia sp. young leaves 13 24.3 8.8 35.9
Tamarindus indica fruit 10 12.9 19.3 50.2
(proportion Grewia clavata fruit 8 15.4 41.2 8.8
of total diet = 78%)
February Talinella dolphinensis fruit 41 6.4 1.3 44.2
Grewia clavata fruit 36 15.8 3.5 37.4
Tamarindus indica fruit 12 5.4 17.5 25.4
Hildebrandtia sp. leaves 6 15.8 3.5 37.4
(proportion Marsdenia sp. young leaves 6 12.9 19.3 50.5
of total diet = 81%)
March Grewia leucophylla fruit 42 27.4 4.7 18.6
Tamarindus indica fruit 35 9.6 3.5 21.0
Rhynchosia sp. leaves 8 54.4 10.1 31.9
(proportion
of total diet = 70%)
Hildebrandtia sp. young leaves 8 35.0 10.7 20.6
Corralocarpus greveii young leaves 7 15.4 41.2 8.8
Table 1. Comparison of gallery (BMSR) and spiny (TNP) forest ring-tailed lemur plant food spe-
cies, plant part, percentage of top 5 foods, plant nutritional properties (crude protein, carbohy-
drates and ADF) and the total percentage of the diet that the top 5 foods constitute for that month
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
30 LaFleur /Sauther
Table 1 (continued)
Location/month Plant species Plant part Percent
top 5
foods
Protein,
%
Carbo-
hydrates,
%
ADF,
%
TNP
September Neobeguea mahafaliensis flowers 94 5.4 17.5 25.4
Neobeguea mahafaliensis young leaves 3 17.3 0.0 6.0
Ficus marmorata fruit 2 15.8 3.5 37.4
(proportion Diospyros manapetsae fruit 1 14.6 12.0 11.8
of total diet = 100%)
October Gyrocarpus americanus flowers 57 12.3 14.3 18.2
Olax androyensis fruit 15 37.8 22.2 31.7
Neobeguea mahafaliensis flowers 20 56.7 4.7 14.3
Ficus marmorata fruit 6 12.9 19.3 50.5
(proportion Gyrocarpus americanus fruit aril 2 25.3 31.5 33.1
of total diet = 100%)
November Gyrocarpus americanus fruit aril 46 18.3 9.5 17.3
Alluaudia comosa flowers 26 10.8 8.2 33.4
Ficus megapoda fruit 13 26.9 21.1 9.5
Ficus marmorata fruit 8 8.1 14.0 15.9
(proportion Gyrocarpus americanus young leaves 7 16.6 6.8 4.6
of total diet = 90%)
December Alluaudia comosa flowers 45 65.4 14.3 18.2
Ficus megapoda fruit 22 25.3 31.5 33.1
rantsandaka1 flowers 18 12.9 19.3 50.5
Gyrocarpus americanus young leaves 9 27.4 4.7 18.6
(proportion anago1flowers 5 35.0 10.7 20.6
(of total diet = 96%)
January liana2 young leaves 30 5.4 17.5 25.4
rantsandaka1 flowers 23 18.3 9.5 17.3
Xerophita dasyliroides flowers 21 24.8 4.2 17.8
manolosasavy1 fruit 16 9.1 23.7 17.3
(proportion Ximenia perrieri fruit 10 10.8 8.2 33.4
of total diet = 70%)
February Ficus megapoda fruit 59 20.8 8.8 51.3
liana2 young leaves 14 12.9 19.3 50.5
Poupartia minor young leaves 13 39.9 8.9 37.4
Adonsonia rubrostipa flowers 9 56.7 4.7 14.3
(proportion rantsandaka1 flowers 5 9.6 4.3 22.7
of total diet = 95%)
March liana2 young leaves 39 18.3 9.5 17.3
Tallinella grevei fruit 26 16.6 8.3 20.8
Neobeguea mahafaliensis mature leaves 14 12.1 9.6 21.5
Euphorbia stenoclada stem 12 10.4 5.1 16.2
(proportion anago1flowers 9 14.6 12.0 11.8
of total diet = 90%)
1 Scientific name unknown. 2 Several similar species analyzed together.
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Lemur catta Seasonal Habitats and Feeding
31
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
Across all months of the study period, the BMSR lemur plant foods’ protein
index was significantly higher than that of the TNP lemurs (f = 22.330, d.f.
total =
13, p 0.00; fig.2 ). Although the BMSR lemur plant food index of soluble carbohy-
drates was lower than that of the TNP lemurs in each month of the study, these dif-
ferences were not significant (f = 0.409, d.f.
total = 13, p = 0.534; fig.3 ). When using the
literature value of 7.6% ADF for T. indica fruit pulp [Gould et al., 2011], we did find
that the BMSR lemurs’ foods contained significantly more fiber when compared to
the TNP plant foods (f = 4.686, d.f.
total = 13, p = 0.051; fig.4 ). Of note, the very high
content of fibrous food in the BMSR diets occurred in September and October, and
are double (or more) than those of the TNP diet during those months ( fig.4 ).
BMSR TNP
Sep Oct Dec Jan Feb MarNov
Soluble carbohydrates (%)
11
17
6
15
5
25
13 15 16
18
20
23
5
18
Fig. 3. Index of soluble carbohydrates in the top 5 plant foods (see Methods for nutritional index
formula).
BMSR TNP
Sep Oct Dec Jan Feb MarNov
ADF (%)
38
17
30
15
28
25
10
15
19 18
22 23
28
18
Fig. 4. Index of ADF in the top 5 plant foods (see Methods for nutritional index formula).
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
32 LaFleur /Sauther
Discussion
The feeding ecology of the ring-tailed lemur has been largely typified by data from
gallery forest habitats. However, this species persists in a suite of habitat types [Good-
man et al., 2006] and is able to adjust to significant environmental perturbations [Gould
et al., 1999; LaFleur and Gould, 2009]. Comparative feeding ecology data from non-
gallery-forest habitats that are now emerging [Gould et al., 2011; LaFleur, 2012; Cam-
eron and Gould, 2013; Gabriel, 2013; Kelley, 2013; LaFleur et al., 2014] are important for
understanding the remarkable ecological flexibility of L. catta. Furthermore, given the
rapid rates of land conversion and forest loss occurring in Madagascar [see Schwitzer et
al., 2014], it is important that we understand variables that determine whether ring-
tailed lemurs can persist over the long-term in highly disturbed or marginal habitats.
The gallery and spiny forest ring-tailed lemurs varied considerably regarding pre-
ferred plant species. Of the top 5 foods consumed at both sites, only one, G. america-
nus , was common to both. Nonetheless, we found no significant differences between
the type of plant part selected (leaves, flowers, fruits). This is reminiscent of Sussman’s
[1987] ‘species-specific’ dietary pattern concept, where he posits that each primate
species has particular dietary preferences due to their morphological and physiological
traits, which then affect taste preference, food processing and digestion. As such, while
particular plant species may be different, conspecifics will utilize similar numbers and
proportions of particular food items. Such dietary flexibility indicates that ring-tailed
lemurs may be able to persist in a wide range of habitat types because they are mor-
phological and physiological generalists, and are able to exploit seasonally available
resources regardless of the particular plant species present.
Although the plant parts consumed by gallery and spiny forest lemurs were sim-
ilar, the top 5 foods emphasized by the BMSR gallery forest ring-tailed lemurs were
significantly higher in crude protein and ADF (especially during the birth months of
September and October; fig.4 ), but not different in soluble carbohydrates, when com-
pared to the top 5 food resources for the spiny forest lemurs, a pattern consistent
across all months ( fig.2 ). Tamarind trees occur in high densities in riverine forests,
and only rarely in spiny forest (such as where there is accessible underground water)
[Sussman and Rakotozafy, 1994; LaFleur, 2012]. Moreover, because tamarind trees
produce leaves and fruits asynchronously at BMSR, they provide a reliable fallback
resource across normal, noncyclone years [Sauther and Cuozzo, 2009; LaFleur and
Gould, 2009]. Indeed during every month of our study at BMSR, tamarind leaf buds
or fruits were among the top 5 foods and provided between 5.4 (fruit) and 64.1% (leaf
buds) crude protein ( table1 ). The increased ADF intake at BSMR was also likely pri-
marily driven by the ingestion of tamarind fruits (50% ADF), young leaves (51%
ADF) and to some extent flowers ( table1 ). Lastly, since the leaves and fruits of tama-
rind trees are not particularly high in carbohydrates (4 and 19%, respectively), the
gallery forest lemurs did not have access to a higher sugar content by way of tamarind
foods. In sum, during this research, the BMSR lemurs may have a nutritional tradeoff
in that they accept high fiber values in order to access high protein levels from tama-
rind. Conversely, the overall lower protein density at TNP may be a function of low
densities of tamarind trees, and/or low rainfall in spiny forest habitats [Donque,
1975]. However, the aforementioned claims need to be explored further, including
how both of these factors influence infant survivorship and subsequent reproduction,
and whether sex differences in diet are apparent.
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Lemur catta Seasonal Habitats and Feeding
33
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
What then is the limit to ecological flexibility in L. catta ? Ring-tailed lemurs are
able to persist in highly degraded and fragmented areas and habitats where plant
foods are of poor quality [e.g. Kelley, 2011; Gould and Gabriel, 2014]. They also live
in the most arid habitats in Madagascar, where low precipitation limits forest pri-
mary productivity, and food resources are low in quantity. Ring-tailed lemurs are able
to exploit seasonally available resources regardless of the particular plant species pres-
ent, which indirectly implies that they are physiological and morphological general-
ists. They do however need some areas of refuge (e.g. trees, shrubs, caves), in addition
to sufficient food resources, although they can cope with variations in macronutrient
(crude protein) and fiber (ADF) content within their foods. Long-term viability of
ring-tailed lemurs in extremely isolated or altered habitats is not yet known, but pop-
ulations are likely to be more affected by genetic bottlenecks [Parga et al., 2012] and
inability to disperse across discontinuous habitat than by diet, given their ability to
exploit similar plant parts, yet persist on differing macronutrient contents.
Acknowledgments
M.L.S. thanks Robert Sussman, Dr. Benjamin Andriamihaja, Armand Rakotozafy, Pete
Philipson, Behaligno and the late Pothin Rakotomanga and Madame B. Rakotosamimananana
for their help with facilitating her project. Her work was supported by the National Science Foun-
dation, the Fulbright Collaborative Grant, the Leakey Foundation, Sigma Xi, the Boise Fund and
the National Geographic Society.
M.L. thanks Dr. Youssouf Jacky Ibrahim Antho and Rokiman Letsara for their help with
facilitating her project. Her work was supported by the National Science and Engineering Re-
search Council of Canada, the National Science Foundation, the American Primatological As-
sociation and the National Geographic Society.
We also thank the government of Madagascar, University of Toliara, University of Anta-
nanarivo, and the lemurs.
References
Altmann J (1974). Observational study of behavior: sampling methods. Behaviour 49: 227–267.
Cameron A, Gould L (2013). Fragment-adaptive behavioural strategies and intersite variation in the ring-
tailed lemur (Lemur catta) in south-central Madagascar. In Primates in Fragments: Complexity and
Resilience (Marsh LK, Chapman CA, eds.), pp 227–243. New York, Springer.
Donque G (1975). Contribution Géographique à l’Etude du Climat de Madagascar. Tananarive, Nouvelle
Imprimerie des Arts Graphiques.
Gabriel DN (2013). Habitat use and activity patterns as an indication of fragment quality in a strepsirrhine
primate. International Journal of Primatology 34: 388–406.
Ganzhorn JU (1988). Food partitioning among Malagasy primates. Oecologia 75: 436–450.
Goodman SM, Rakotoarisoa SV, Wilm L (2006). The distribution and biogeography of the ringtailed le-
mur (Lemur catta) . In Ring-Tailed Lemur Biology (Jolly A, Koyama N, Rasamimanana H, Sussman
RW, eds.), pp 3–15. New York, Springer.
Gould L (2006). Lemur catta ecology: what we know and what we need to know. In Lemurs: Ecology and
Adaptation (Gould L, Sauther ML, eds.), pp 255–274. New York, Springer.
Gould L, Gabriel DN (2014). Wet and dry season diets of the Endangered Lemur catta (ring-tailed lemur)
in two mountainous rocky-outcrop forest fragments in south-central Madagascar. African Journal
of Ecology 2014, Early View DOI: 10.1111/aje.12186.
Gould L, Power ML, Ellwanger N, Rambeloarivony H (2011). Feeding behavior and nutrient intake in
spiny forest-dwelling ring-tailed lemurs (Lemur catta) during early gestation and early to mid-lac-
tation periods: compensating in a harsh environment. American Journal of Physical Anthropology
145: 469–479.
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
34 LaFleur /Sauther
Gould L, Sussman RW, Sauther ML (1999). Natural disasters and primate populations: the effects of a
2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in south-
western Madagascar. International Journal of Primatology 20: 69–84.
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: Studies by Women Primatologists
(Small M, ed), pp 197–217, New York, Alan R. Liss.
Kelley EA (2011). Lemur catta in the region of Cap Sainte-Marie, Madagascar: introduced cacti, xero-
phytic Didiereaceae-Euphorbia bush, and tombs. PhD Dissertation. Washington University, St.
Louis.
Kelley EA (2013). The ranging behavior of Lemur catta in the region of Cap Sainte-Marie, Madagascar.
American Journal of Physical Anthropology 150: 122–132.
LaFleur M (2012). Ecology of Ring-Tailed Lemurs (Lemur catta) at the Tsimanampetsotsa National Park,
Madagascar: Implications for Female Dominance and the Evolution of Lemur Traits. Unpublished
doctoral dissertation, University of Colorado, Boulder.
LaFleur M, Gould L (2009). Feeding outside the forest: the importance of crop raiding and an invasive
weed in the diet of gallery forest ring-tailed lemurs (Lemur catta) following a cyclone at the Beza
Mahafaly Special Reserve, Madagascar. Folia Primatologica 80:233–246.
LaFleur M, Sauther M, Cuozzo, F, Yamashita N, Youssouf IAJ, Bender R (2014). Cathemerality in wild
ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap
data and preliminary behavioral observations. Primates 55: 207–217.
Parga JA, Sauther ML, Cuozzo FP, Youssouf Jacky IA, Lawler R (2012). Evaluating ring-tailed lemurs (Le-
mur catta) from Southwestern Madagascar for a genetic population bottleneck. American Journal of
Physical Anthropology 147:21–29.
Ratsirarson J, Richard A (2010). Reinforcing the Community-Based Biodiversity Conservation and Moni-
toring in Southwestern Madagascar. Final Report 2008–2010. Antananarivo, Foundation Tany Meva.
Sauther ML (1994). Wild plant use by pregnant and lactating ring-tailed lemurs, with implications for
early hominid foraging. In Eating on the Wild Side (Etkin NL, ed.), pp 240–256. Tucson, University
of Arizona Press.
Sauther ML (1998). The interplay of phenology and reproduction in ringtailed lemurs: implications for
ringtailed lemur conservation. Folia Primatologica 69(suppl 1): 309–320.
Sauther ML, Cuozzo F (2008). Somatic variation in living, wild ring-tailed lemurs (Lemur catta). Folia
Primatologica 79:55–78.
Sauther ML, Cuozzo FP (2009). The impact of fallback foods on wild ring-tailed lemur biology: a com-
parison of intact and anthropogenically disturbed habitats. American Journal of Physical Anthropol-
ogy 140: 671–686.
Sauther ML, Sussman RW, Gould L (1999). The socioecology of the ring-tailed lemur: thirty-five years of
research. Evolutionary Anthropology 8: 120–132.
Schwitzer C, Mittermeier RA, Johnson SE, Donati G, Irwin M, Peacock H, Wright PC (2014). Averting
lemur extinctions amid Madagascar’s political crisis. Science 343: 842–843.
Sponheimer M, Robinson T, Ayliffe L, Passey B, Roeder B, Shipley L, Lopez E, Cerling T, Dearing D,
Ehleringer J (2003). An experimental study of carbon-isotope fractionation between diet, hair, and
feces of mammalian herbivores. Canadian Journal of Zoology 81: 871–876.
Sussman RW (1977). Distribution of the Malagasy lemurs. 2. Lemur catta and Lemur fulvus in southern
and western Madagascar. Annals of the New York Academy of Science 293: 170–184.
Sussman RW (1987). Species-specific dietary patterns in primates and human dietary adaptations. In The
Evolution of Human Behavior: Primate Models (Kinzey WG, ed.), pp 151–179. Albany, State Uni-
versity of New York Press.
Sussman RW, Rakotozafy A (1994). Plant diversity and structural analysis of a tropical dry forest in south-
western Madagascar. Biotropica 26: 241–254.
Sussman RW, Richard AF, Ratsirarson J, Sauther ML, Brockman DK, Gould L, Lawler R, Cuozzo FP
(2012). Beza Mahafaly Special Reserve: long-term research on lemurs in southwestern Madagascar.
In Long-Term Field Studies of Primates (Kappeler PM, Watts DP, eds.), pp 45–66. Berlin, Springer.
Weiss KE (2011). The 5% solution: how do we make decisions in science? Evolutionary Anthropology 20:
81–84.
Whitelaw DC (2010). Ecological Impacts of Forest Disturbance on Ring-Tailed Lemurs (Lemur catta) in the
Beza-Mahafaly Special Reserve Region: Implications for Conservations in an Altered Landscape . Un-
published doctoral dissertation, University of Colorado, Boulder.
Yamashita N (2002). Diets of two sympatric lemur species in different microhabitats in Beza Mahafaly
Special Reserve, Madagascar. International Journal of Primatology 23: 1025–1051.
Yamashita N (2008). Chemical properties of the diets of two lemur species in southwestern Madagascar.
International Journal of Primatology 29: 339–364.
Downloaded by:
Max Planck Society
195.37.59.2 - 5/22/2015 10:06:59 AM
... indica produce young leaves and fruits asynchronously at BMSR with either T. indica leaf buds or fruit among the top five foods each month and with T. indica leaves providing a key source of crude protein for the lemurs (LaFleur & Sauther, 2015). As such, during the 12 month postcyclone period, there was a near total absence of the ring-tailed lemurs' major fallback species and potentially low protein availability (Rasamimanana et al., 2012;Whitelaw, 2010). ...
... As world climatic perturbations become more frequent and intense, understanding the effects of different extreme weather events on health and physiology is essential for the development of long-term conservation strategies and should be incorporated into any species risk assessment (y Juárez et al., 2013). This is especially critical for the ring-tailed lemur, given that new data on populations indicate a recent, rapid, precipitous drop in numbers across their historical range (Gould & Sauther, 2006;LaFleur & Sauther, 2015). ...
Article
Madagascar is known for its hypervariable climate with periodic droughts and cyclones, but little is known of the impact of such events on lemur physiology. We examined the effects of sequential weather periods, drought, normal, cyclone and post-cyclone, on hair cortisol concentrations (HCC) and body weight in wild ring-tailed lemurs, Lemur catta (n = 185), at the Bezà Mahafaly Special Reserve in southwestern Madagascar. Data were modeled and analyzed by sex, age, and troop. Given the ecological consequences of extreme climatic perturbations, we hypothesized that drought and cyclone would significantly impact lemur HCC. Among adults, drought was associated with higher HCC than other periods and the lowest HCC was associated with the post-cyclone period. Adult females had greater variation in HCC during drought and males had greater variation during cyclone and Post-cyclone periods, suggesting sexes were differentially affected in terms of how individuals responded to extreme weather events. Low HCC in the post-cyclone period followed a 12-month period of reduced availability of primary and fallback food resources. Based on the known extreme and chronic nutritional stress during this time, our results indicate hypocortisolism in the animals included in our analysis. Higher HCC in sub-adults during the cyclone also suggests that immature lemurs may experience extreme weather events differently than adults. Body weight, used as a gauge for environmental stress, was lowest during the post-cyclone for sub-adults, young adults, and adults. Body weight did not differ by sex among adults across any of the weather events. Overall, ring-tailed lemur's HCC appear to be more immediately impacted by drought, or stressors associated with that specific weather event, and influenced by the long-term impact of cyclones on resource availability evidenced by data from the post-cyclone period.
... Thanks to their semi-terrestrial habits, they can forage both on the ground and in the trees (Jolly 1966;Demens et al. 1999) thus showing a high ecological flexibility. L. catta is defined as an opportunistic frugivorous-folivorous species whose diet can also include invertebrates and small vertebrates (Ganzhorn 1986;Rasamimanana & Rafidinarivo 1993;Sauther 1993;Sauther et al. 1999;LaFleur & Sauther 2015). Previous studies highlighted that food resources selected by ring-tailed lemurs vary among different sites and habitats according to seasonal availability (Gould & Gabriel 2015). ...
... They also prey on larvae, locusts, cicadas, and spiders (Sauther 1992), and occasionally birds and chameleons (Sauther 1992;Oda 1996;Ichino & Rambeloarivony 2011). Therefore, the variety of food items included in their diet requires different feeding strategies (Wright 1999) and different levels of manual skills that vary from simple grasping actions for static food to rapid movements for targets in motion, hereinafter defined as "catching" (LaFleur & Sauther 2015;Hansell et al. 2020). As all the other strepsirrhine species, L. catta shows a wholehand power grip with no digit individualisation (Peckre et al. 2019a). ...
... It is unknown whether any remain in the park in 2016. A population of L. catta can still be found at the Tsimanampesotse National Park (LaFleur 2012; Sauther et al. 2013;LaFleur and Sauther 2015), although the total number of animals is unknown, as the park is large and, in places, inaccessible. Part of the population, containing around 80-100 animals, is continually monitored via long-term studies by M. LaFleur, and by M. Sauther and F. P. Cuozzo (Sauther et al. 2013;LaFleur et al. 2014;LaFleur and Sauther 2015). ...
... A population of L. catta can still be found at the Tsimanampesotse National Park (LaFleur 2012; Sauther et al. 2013;LaFleur and Sauther 2015), although the total number of animals is unknown, as the park is large and, in places, inaccessible. Part of the population, containing around 80-100 animals, is continually monitored via long-term studies by M. LaFleur, and by M. Sauther and F. P. Cuozzo (Sauther et al. 2013;LaFleur et al. 2014;LaFleur and Sauther 2015). There are recent reports, however, of infants being taken for the illegal pet trade . ...
Article
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 Didiereoideae are particularly important in this context as their leaves are protected by spines that closely related species from mainland Africa lack (Applequist and Wallace, 2003). This suggests significant predation was experienced by the Madagascan clade (Cooper and Owen-Smith, 1986), even if today they experience only light predation by Lemur catta and Propithecus verreauxi (Norscia and Palagi, 2011;LaFleur and Sauther, 2015). In fact, Hadropithecus is the only species we know that presumably had the capacity and stable isotope compositions to have predated upon these CAM plants regularly (Crowley and Godfrey, 2013). ...
Article
Carbon isotopic analysis has been challenging our ideas about hominin diet for nearly 30 years. The first study in 1994 revealed that Paranthropus robustus from South Africa consumed principally C3 foods (e.g., tree fruits and leaves) but also about 25% C4/CAM resources (e.g., tropical grasses and sedges). This result was largely consistent with morphological and dental microwear evidence suggesting P. robustus had a diet which included hard objects like nuts and seeds. Decades later, however, P. boisei from eastern Africa was shown to have eaten nearly 80% C4/CAM plants like the contemporaneous grass-eating primate Theropithecus. Moreover, dental microwear revealed no evidence of hard object consumption in P. boisei, suggesting a diet of tough foods such as grass or sedge leaf and stem. So Paranthropus presents us with two central problems: 1) Why do dietary proxies suggest different diets for the two robust australopiths despite their morphological congruity; and 2) How could P. boisei have consumed tough foods with teeth that seem unsuited to the task. Here we review these questions and more with a particular focus on new isotopic data from the Omo and insights that can be gleaned from mammals outside the haplorrhine primates. We argue that extant Primates do not capture the ecomorphological diversity of P. boisei and other extinct primates and should not narrowly circumscribe the behaviors we ascribe to extinct taxa. We also discuss possible digestive strategies for P. boisei in light of its morphology, dietary proxy data, food mechanical properties, and comparative data on mammalian digestive kinetics.
... To help understand feeding variability across time and space, I present a literature review of plant species consumed by ring-tailed lemurs from nine study sites in Madagascar. Although other reviews exist (e.g., Goodman et al. 2006;Gould and Gabriel 2015;LaFleur and Sauther 2015;Simmen et al. 2006), this is the most extensive and comprehensive to date with regard to the number of sites examined. The data are from 1974-2016, with the earliest publication (Sussman 1974) including fieldwork from 1969. ...
Article
Full-text available
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.
... Ring-tailed lemurs (Lemur catta) are known to consume a wide variety of food items of both plant and animal origin [20][21][22]. Nevertheless, they are considered as opportunistic frugivores/folivores and are highly adaptive to seasonal changes in their diet [23]. ...
Article
Full-text available
The aim of the present study was to assess the occurrence of spontaneous food preferences in zoo-housed ring-tailed lemurs and to analyze whether these preferences correlate with nutrient composition. Using a two-alternative choice test three female and one male Lemur catta were repeatedly presented with all possible binary combinations of 12 types of food which are part of their diet in captivity and found to display the following rank order of preference: apple > sweet potato > melon > beetroot > carrot > egg > eggplant > pumpkin > cucumber > tomato > cabbage > mealworm. Correlational analyses revealed a highly significant positive correlation between this food preference ranking and the total carbohydrate and sucrose contents of the foods (p < 0.01, respectively). No other significant correlations with any other macro- or micronutrient were found. These results suggest that zoo-housed ring-tailed lemurs are not opportunistic, but selective feeders with regard to maximizing their net gain of energy as only the content of carbohydrates, but not the contents of total energy, proteins or lipids significantly correlated with the displayed food preferences. Further, we found that ring-tailed lemurs that were raised on a vegetable-based diet did not significantly differ in their food preferences, and in particular in their predilection for food items high in carbohydrates, from animals that had previously been fed a fruit-based diet. This suggests that the lemurs’ preference for carbohydrate-rich food items may be innate and not affected by experience with different diets.
... 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. ...
Article
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.
... This is predicted to vary depending on group dynamics and environmental factors (Ganzhorn, 1986;Simmen et al., 2006;LaFleur and Sauther, 2015). As they are considered semi-terrestrial, they are known to spend 18-30% of foraging time on the ground, a trait considered unusual in lemurs ( Sauther et al., 1999;Fleagle, 2013). ...
Thesis
Full-text available
Lemurs are naturally endemic to the island of Madagascar. Captive lemur diets generally consist of commercial dry pellets supplemented with vegetables and forages. The dry pellets given are their main source of fibre and are key to ensuring all nutritional requirements are met in a man-made setting. These are often the blandest and least desirable part of the diet, and therefore usually fed first, separately to more palatable foods, and ad lib. Incorrect feeding in captivity for lemurs is a prominent issue seen in many institutions. Enrichment feeds have proven to have a beneficial effect on encouraging natural behaviours, such as grooming and foraging. However, there is minimal research on whether enrichment can be used to affect feed intake. Three species of lemur, the red ruffed lemur (Varecia rubra), the black and white ruffed lemur (Varecia variegate), and the ring-tailed lemur (Lemur catta) were given three different feeding enrichments. Two aims were being investigated: 1) whether presenting dry pellets through enrichment devices changes the overall feed intake in three species of lemur, and 2) whether different enrichment items have different effects on pellet consumption. Results presented no significant change in pellet consumption when fed through enrichment devices for ring-tailed lemurs (p>0.05), which was also the case for both ruffed lemur species (p>0.1). They also distinguished no significant difference between feeding enrichments in pellet intake in any of the three species of lemur. This study helped identify the possibility of using enrichment for pellet consumption in zoos, but showed that the devices used didn’t have a significant enough effect to suggest future implementation of enrichments for the sake of nutrition. Further research is needed to fully understand whether the application of enrichment can be beneficial for encouraging adequate diets in lemurs, and more factors need to be considered, such as species difference in locomotion and enclosure use.
... Lemur catta, the ring-tailed lemur, is a medium-bodied (average body mass 2.2 kg; Smith and Jungers, 1997) largely terrestrial lemurid endemic to Madagascar (Dagosto, 1995;Fleagle, 2013;LaFleur and Sauther, 2015). The locomotor behavior exhibited by L. catta centers on terrestrial quadrupedalism, but arboreal movements are also common especially on large or medium sized supports (Gebo, 1987;Oxnard et al., 1990;Goodenberger et al., 2015). ...
Thesis
Full-text available
For primates, and other arboreal mammals, adopting suspensory locomotion represents one of the strategies an animal can use to prevent toppling off a thin support during arboreal movement and foraging. While numerous studies have reported the incidence of suspensory locomotion in a broad phylogenetic sample of mammals, little research has explored what mechanical transitions must occur in order for an animal to successfully adopt suspensory locomotion. Additionally, many primate species are capable of adopting a highly specialized form of suspensory locomotion referred to as arm-swinging, but few scenarios have been posited to explain how arm-swinging initially evolved. This study takes a comparative experimental approach to explore the mechanics of below branch quadrupedal locomotion in primates and other mammals to determine whether above and below branch quadrupedal locomotion represent neuromuscular mirrors of each other, and whether the patterns below branch quadrupedal locomotion are similar across taxa. Also, this study explores whether the nature of the flexible coupling between the forelimb and hindlimb observed in primates is a uniquely primate feature, and investigates the possibility that this mechanism could be responsible for the evolution of arm-swinging. To address these research goals, kinetic, kinematic, and spatiotemporal gait variables were collected from five species of primates (Cebus capucinus, Daubentonia madagascariensis, Lemur catta, Propithecus coquereli, and Varecia variegata) walking quadrupedally above and below branches. Data from these primate species were compared to data collected from three species of non-primate mammals (Choloepus didactylus, Pteropus vampyrus, and Desmodus rotundus) and to three species of arm-swinging primates (Hylobates moloch, Ateles fusciceps, and Pygathrix nemaeus) to determine how varying forms of suspensory locomotion relate to each other and across taxa. From the data collected in this study, it is evident the specialized gait characteristics present during above branch quadrupedal locomotion in primates are not observed when walking below branches. Instead, gait mechanics closely replicate the characteristic walking patterns of non-primate mammals, with the exception that primates demonstrate an altered limb loading pattern during below branch quadrupedal locomotion in which the forelimb becomes the primary propulsive and weight-bearing limb ¬– a pattern similar to what is observed during arm-swinging. It is likely that below branch quadrupedal locomotion represents a “mechanical release” from the challenges of moving on top of thin arboreal supports. Additionally, it is possible that arm-swinging could have evolved from an anatomically-generalized arboreal primate with tendencies to forage and locomote below branches. During these suspensory bouts, weight would have been shifted away from the hindlimbs towards the forelimbs, and, as the frequency of these bouts increased, the reliance of the forelimbs for weight support would have also increased. This functional decoupling may have released the hindlimbs from their weight-bearing role during suspensory locomotion, and eventually, arm-swinging would have replaced below branch quadrupedal locomotion as the primary mode of suspensory locomotion observed in some primate species. This study provides the first experimental evidence supporting the hypothetical link between below branch quadrupedal locomotion and arm-swinging in primates.
Article
Full-text available
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.
Article
Full-text available
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.
Article
Full-text available
The carbon-isotope composition of hair and feces offers a glimpse into the diets of mammalian herbivores. It is particularly useful for determining the relative consumption of browse and graze in tropical environments, as these foods have strongly divergent carbon-isotope compositions. Fecal δ13C values reflect the last few days consumption, whereas hair provides longer term dietary information. Previous studies have shown, however, that some fractionation occurs between dietary δ13C values and those of hair and feces. Journal Article
Article
Full-text available
The most threatened mammal group on Earth, Madagascar's five endemic lemur families (lemurs are found nowhere else) (1), represent more than 20% of the world's primate species and 30% of family-level diversity. This combination of diversity and uniqueness is unmatched by any other country—remarkable considering that Madagascar is only 1.3 to 2.9% the size of the Neotropics, Africa, or Asia, the other three landmasses where nonhuman primates occur. But lemurs face extinction risks driven by human disturbance of for-est habitats. We discuss these challenges and reasons for hope in light of site-specific, local actions proposed in an emergency con-servation action plan (2). Political Crisis, Remarkable Threat An International Union for Conservation of Nature (IUCN) Species Survival Commission (SSC) Red List reassessment found that 94% of lemur species are threatened (2) (Fig. S1 and Table S1), up from 74% in 2008, which makes lemurs the most imperiled group of large vertebrates. Although other large mammals are also under pres-sure, for the vast majority of taxa in an entire infraorder (Lemuriformes) to be threatened is new, notable, and disturbing. This reevaluation has resulted from both the deterioration of habitat and the recent application of genetic data to phylogenetic analyses (increasing the number of extant lemur species from 43 to 101) (3), revealing more species with smaller ranges. This unique primate diversity relies on for-est habitats that are shrinking under persistent anthropogenic destruction and disturbance. Remaining intact forest habitat was estimated to cover 92,200 km 2 in 2010, only 10 to 20% of Madagascar's original forest cover and down from 106,600 km 2 in 1990 (4); much of this habitat is inadequately or not at all protected. Habitat and lemur conservation are interdependent: Lemurs have important ecological roles and are essential to maintaining the island's unique forests. Their loss would likely trigger extinction cascades (5). Challenges to in situ lemur conservation are immense. Madagascar is one of the poor-est countries in the world; more than 92% of Malagasy live on less than U.S. $2/day (6). Although there is a paucity of published data compared to other lemur-related subjects, lemur poaching for bushmeat has drastically increased since the onset of the political crisis in 2009 (7, 8). Illegal logging of rosewood and ebony, mining, and slash-and-burn agriculture are all causing lemur population declines, by habitat loss, fragmentation, and alteration. Protected areas have not been spared; for example, armed timber poachers extracting valuable hardwoods targeted Masoala and Marojejy National Parks in the northeast once local law enforcement broke down (9). Foreign demand, as well as political turmoil and corruption, drive these
Article
Full-text available
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.
Thesis
Full-text available
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.
Chapter
Behaviour, diet and population demography were sampled and compared between two forest fragment-living populations of wild ringtailed lemurs (Lemur catta) in south-central Madagascar. Both sites—a fragment in the Tsaranoro Valley near Andringitra National Park, and a more densely populated fragment at Anja, much closer to human habitation—are sacred forests (sites of human burial) surrounded by anthropogenically produced savannah, and are subject to traditional protective prohibitions (fady). Both sites attract tourists, but are operated differently, with Anja receiving considerably more tourists; the resources available to the L. catta also differ at each site, affecting their behaviour. L. catta at Tsaranoro spent more time feeding, and less time resting and engaging in social behaviour than those at Anja, where abundant fruit from introduced trees, as well as plentiful drinking water, are available and resource abundance is relatively higher. Although the fragments are of similar size and were expected to differ little, many significant behavioural and population differences were observed, suggesting the importance of the refinement of rapid assessment techniques for judging the habitat suitability and conservation value of small forest fragments.
Article
For this paper, we sampled a fenced and an unprotected portion of a dry gallery forest (the Beza Mahafaly Reserve) in southwestern Madagascar for structure and floristic composition. Seedling plots were also sampled to assess invasion and regeneration. A total of 923 plants ≥2.5 cm diameter at breast height (DBH) were censused in 25 transects. Sixty-nine species and 43 genera were represented. In plant density, diversity, and size classes of individuals, the forest is similar to many continental tropical dry forests in Africa and the Neotropics. Over 80 percent of those species identified were native, as were 26 percent of the genera. Unlike many insular forests, Beza Mahafaly is not being invaded by fast-growing exotic species. There were no noticable differences in density, diversity, size classes, or proportion of native species between transects within and outside of the protected reserve. Two distinct microhabitats were noticed. Individual plants were more dense on "drier" soils; whereas, large trees ≥25 cm DBH were over twice as frequent on "wetter" soils. The floristic composition also differed, with only two species of tree, Tamarindus indica and Azima tetracantha, being common to both habitats. The distribution and density of lemur populations within the forest appear to be directly related to microhabitat differences.
Article
Lemur catta's ability to consume a wide variety of plant foods is a key to this species' survival in a time of ecological crisis across its geographic range. We examined seasonal diet variability of L. catta groups inhabiting two rocky outcrop fragments in south-central Madagascar: Anja Reserve and Tsaranoro Valley forest. Leaves and fruit of Melia azedarach were a keystone resource for Anja lemurs in wet and dry seasons. At Tsaranoro, L. catta relied on M. azedarach and Ficus spp. in dry season, but during the wet season, neither was a dominant food resource. Top food species at both sites differed markedly from those consumed by L. catta in other habitats. At Tsaranoro, a greater proportion of lemurs engaged in feeding during the dry season compared with wet season. We attribute this to resource scarcity during dry season, when greater feeding effort is needed to maintain energy requirements. Because M. azedarach is ubiquitous throughout Anja Reserve, producing fruit and leaves year-round, Anja lemurs can meet energy requirements with little seasonal adjustment in feeding activity. L. catta's IUCN status has been upgraded to Endangered, thus, greater insight into its diet flexibility and ability to survive on introduced plant species, can inform conservation plans in remaining wild habitats and ex situ programs.