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

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.

Full text

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
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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].
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Lemur catta Seasonal Habitats and Feeding
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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
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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).
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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
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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.
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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).
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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.
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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.
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Folia Primatol 2015;86:25–34
DOI: 10.1159/000369581
34 LaFleur  /Sauther 
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