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Differential patterns in flower feeding by Eulemur fulvus rufus and Eulemur rubriventer in Madagascar.

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American Journal of Primatology 28191-203 (1992)
Differential Patterns in Flower Feeding by €demur fulvus
rufus and Eulemur rubriventer in Madagascar
DEBORAH J. OVERDORFF
Department of Biological Anthropology and Anatomy, Duke University, Durham, North
Carolina
In this paper, I describe the differential patterns of flower feeding observed in rufous lemurs (Eulemur fuluus rufus)and red-bellied lemurs (E.
rubriuenter) in the Ranomafana National Park, Madagascar. Red-bellied
lemurs licked nectar from flowers while rufous lemurs ate all flower parts
from the same flower species. Several hypotheses are examined to explain
the significance of flower feeding in these two species. In many primate
species, flower feeding functions as a keystone resource and/or primates
act as pollinators while feeding on flowers. Although peak flower feeding
occurred during a decline in food availability, fruit was always the preferred food item so that flowers did not function as a keystone resource.
Second, red-bellied lemurs appear to be potentially better pollinators compared to the rufous lemurs because 1)they left flower reproductive parts
intact while feeding, 2) they visited more than one tree or liana of the same
plant species in the same day, 3) pollen was observed on the faces of
individuals as they traveled from plant to plant, and 4) they have a feathered, brush-like tip on their tongue which rufous lemurs lack. Finally, the
difference in flower feeding styles between the lemur species also affected
three aspects of diet: 1) feeding bout duration, 2) the size of feeding subgroups, and 3) return visits to flowering sources. These subtle differences
in diet within food categories can allow these two otherwise similar lemur
species to coexist. 0 1992 Wiley-Liss, Inc.
Key words: prosimian primate, keystone resource, pollination, dietary differences
INTRODUCTION
In this paper, I describe the patterns of flower feeding in two sympatric species
of prosimian primates: the rufous lemur (Eulemur fuluus rufus) and the red-bellied
lemur (Eulemur rubriventer: see Simons and Rumpler, 1988, for nomenclature).
Both lemur species fed on similar flowering plant species but ate flowers in different ways throughout a 13-month study in the Ranomafana National Park,
Madagascar (RNP).
Two hypotheses have been suggested to explain the seasonal importance and
function of flower feeding by non-flying mammals, particularly primates. First,
flowers can function as an alternative food source when other preferred food items
Received for publication September 17, 1991; revision accepted April 15,1992.
Address reprint requests to Deborah J. Overdorff, Dept. of Biological Anthropology and Anatomy, Duke
University, 3705-B Erwin Road, The Wheeler Bldg., Durham, NC 27705.
0 1992 Wiley-Liss, Inc.
192 I Overdorff
are scarce. These resources, such as Ficus species, are often referred to as keystone
resources or keystone mutualists [Terborgh, 1986; Leighton & Leighton, 1983;
Gautier-Hion, 1989; van Schaik & Djojosudharmo, 19901.There are four important
characteristics of keystone resources: they are relatively few in number, phenologically predictable, are expected to produce annually, and are the primary form
of caloric intake in the animal’s diet. Flower nectar, in particular, serves as one
type of critical resource that sustains communities of frugivores during periods of
food scarcity in the Neotropics [Janson et al., 1981; Terborgh, 1986; Terborgh &
Stern, 19871. If flowers function as a keystone resource in RNP, it is expected that
both lemur species will spend the most time flower feeding during periods of
maximum food scarcity.
Second, flower feeding by non-flying mammals has been discussed in regard to
pollination ecology [Carpenter, 1978; Sussman, 1978; Prance, 1980; Janson et al.,
1981; Torres de Assumpacao, 1981; Feinsinger, 19831. Sussman and Raven [19781
described the importance of prosimian primates as pollinators due to the limited
numbers of fruit bats on the island of Madagascar. They listed several floral
characteristics that might attract larger, non-flying mammalian pollinators such
as large, unusually strong flowers, strong floral odors, and copious nectar production. In addition to these characteristics, two questions must be considered to
establish whether or not primates are functioning as pollinators: 1)are the flower’s
reproductive parts destroyed during feeding and 2) is pollen transferred between
plants during the feeding process?
The purpose of this paper is to describe the different patterns of flower feeding
observed in red-bellied lemurs and rufous lemurs. How flowers were consumed and
seasonal patterns of flower feeding will be described. The hypothesis that flowers
function as a keystone resource will be evaluated in conjunction with data collected
on seasonal phenology patterns. Next, the possible role of either lemur species as
a potential pollinator also will be discussed in regard to previously described pollination behavior in prosimian primates. Finally, I will discuss how the different
flower feeding styles between the two lemur species affected other aspects of diet
such as feeding bout duration, subgroup size, and return visits to flowering resources.
MATERIALS AND METHODS
The socio-ecology of red-bellied lemurs and rufous lemurs was studied for 13
months from July 1988 through August 1989. The study site was located in the
RNP, a large (40,000 ha), southeastern stretch of rainforest in Madagascar located
between 47”18’-47”37’ and 21”02-21”-05 S. RNP is a continuous stretch of forest
ranging from montane cloud forest (1,500 m) to lowland rainforest (500 m). The
site for this study, known as Vatoharanana, was approximately 5 km south of the
Duke research station. The Vatoharanana forest is a high montane rainforest
(1,125 m) with an annual rainfall of 2,300 mm during the study period. This region
supports ten other sympatric species of primates in addition to the two study
species.
Two groups of red-bellied lemurs and one group of rufous lemurs were followed
at least 8 days a month from dawn to dusk from July 1988 through August 1989
with the help of a field assistant. A second rufous lemur group was followed
throughout the study on an opportunistic basis. Over 3,000 hours of data were
collected and data are presented from the period of August 1988 through August
1989.
I used a combination of focal animal and all occurrence data [Altmann, 19741
to collect data on the feeding patterns of each lemur species. An adult male and
Flower Feeding in Two Prosimian Primates / 193
female focal animal in a study group were followed on each sampling day and focal
samples were balanced between all adult individuals in each study group. Individuals were marked with colored collars and pendants or radio collars. As animals
were captured, body measurements [Glander et al., in press] were collected and
each animal’s age was estimated on dental wear. Other unusual external characteristics were noted during the capture process. Photographs were also made of
each animal’s face when captured.
Each time a focal animal initiated a feeding bout, four types of data were
recorded: the type of food eaten, the duration of each feeding bout, the number of
food items eaten (or flowers licked) by the focal animal, and the average number
of individuals feeding simultaneously with the focal animal (subgroup size). The
type of food item eaten by the focal animal was categorized as fruit (ripe or unripe),
leaves (new or mature), or flowers (flower eaten or nectar licked).
Prior to the study, I decided that a feeding bout would be defined as a flower
eating or nectar licking bout when the focal animal spent more than 50% of the
time either licking or eating flower parts. Neither lemur species, however, mixed
flower feeding styles during the study. In cases where a focal animal ate flowers,
it was noted (visually or by examining flowers dropped by the focal animal)
whether or not the reproductive parts were destroyed. Diet then was analyzed by
calculating the percentage of observed time feeding (overall and monthly) in each
food category. Plants were collected and pressed for identification. Fruits, leaves,
and corolla lengths were measured during the plant collection process.
The crown volume for each flowering plant that each lemur species fed in was
calculated for every tree over 5 cm diameter a t breast height (DBH). This was
calculated by visually estimating crown radius (m), crown depth (m), crown shape
(circular, cylindrical, triangular, dome), and measuring DBH. If the flowering
plant was a liana, the area covered by the liana was estimated using the same
technique. Each tree or liana also was given a unique identification number and
was mapped on a two-dimensional map of the study site.
A visit to a flowering plant was defined as one or more feeding bouts within
the same tree of liana. A return visit was calculated only when animals traveled
away from the plant to another location and then returned at some later time.
Neither lemur species returned to the same flowering resource in the same day, so
return time was calculated in days.
Seasonal patterns in weather and food availability were quantified by measuring daily rainfall, temperature, and forest phenology. At the beginning of the
study, a sample of 104 trees, representing 26 plant species that the animals were
known to feed in (which included the top 10 species in both lemur’s diets), were
monitored for fruiting, flowering, and new leafing patterns. All trees in the sample
were checked for the presence of fruit, flowers, and new leaves twice a month. The
presence or absence of each reproductive part was recorded using a scale of zero
(none present) to five (full crown) and was referred to as the amplitude score.
Flower, fruit, and new leaf availability index was calculated for each sampling
period using the following formula:
s
FA
CV*(A/5)
=
1=0
where FA = flower availability (m3),i = the ith tree in sample, s = total number
of trees in sample, CV = crown volume, and A = amplitude score.
The Mann-Whitney U test or the Kruskall-Wallis test [Sokal & Rolf, 19811was
used to test for differences in length of flower feeding bouts and flowering resource
size within and between lemur species. Spearman’s rho was used to test the rela-
194 I Overdorff
Fruit
Flower
New leaves
2000
5e
I000
0
0
1988
1989
Fig. 1. Fruit, flower, and new leaf availability from August 1988 through August 1989.
tionship between flower resource size and the number of individuals feeding, and
percentage of time observed feeding on flowers with food availability.
RESULTS
Pheno1ogy
Seasonal fruiting, new leafing, and flowering patterns were observed during
the study (Fig. 1). Fruit availability peaked from August through October and
again in February but was lowest from April through June 1989. New leaf availability peaked in May. Finally, two distinct peaks in flower availability occurred
in August 1988 and a smaller peak was observed in November-December 1988.
Flower Feeding Patterns
Red-bellied lemurs and rufous lemurs fed on flowers throughout the year for a
total of 8.2 hours and 7.9 hours, respectively. Flower feeding constituted the smallest proportion of either lemur species’ diet relative to other food categories (fruit
and leaves) and both lemur species were highly frugivorous year round (Fig. 2).
Both lemur species fed on a total of 18 flowering plant species. Table I lists
each of these species and their corolla lengths. Seven of these plant species were
exploited by both lemurs species and accounted for over 50% of the time spent
feeding on flowers (red-bellied lemurs 64%; rufous lemurs 93%).
Flowers were eaten most often in December and January (Fig. 3). Red-bellied
lemurs also spent a comparable percentage of time eating flowers from an unidentified species of Sterculiaceae in August 1989. Flower feeding was not correlated,
however, with flower availability (red-bellied lemur r, = .12, n.s., rufous lemur rs
= .13, n.s.1 but coincided with the drop in fruit availability and occurred prior to
the peak in new leaf availability.
There was a significant difference in how red-bellied lemurs and rufous lemurs
exploited flowers although they ate flowers from many of the same plant species
a t the same time of year. Neither lemur species mixed flower feeding styles while
feeding; flowers were either eaten or licked. Red-bellied lemurs spent 86% (n = 62)
of the time licking flower nectar and 14% (n = 10) of the time feeding on flower
parts of Vosauoraka. In contrast, rufous lemurs spent 31% (n = 24) of their time
licking flower nectar and 69% (n = 75) of the time eating flower parts.
Both lemur species destroyed flower parts from all but two flowering species,
Strongylodon sp. and Sterculiaceae, regardless if flowers were licked or eaten.
Neither lemur species destroyed the flowers of Strongylodon sp. while the redbellied lemur was the only lemur species that did not destroy Sterculiaceae flow-
Flower Feeding in Two Prosimian Primates I 195
loo
80
-$
60
$
40
1
Ruious lemur
Q Red-bellied lemur
0,
c
a
20
0
FR
LE
FL
OTHER
Fig. 2. Overall composition of diet for rufous lemurs and red-bellied lemurs based on percentage of observed
time feeding in each food category. FR = fruit; LE = leaves; FL = flowers; OTHER = Miscellaneous foods (dirt,
insects, bark, etc.).
TABLE I. Scientific Names of Flowering Plants Eaten by Red-Bellied and Rufous
Lemurs From August 1988 Through August 1989*
Family
Acanthaceae
Cunoniaceae
Guttiferae
Guttiferae
Elaeocarpaceae
Lauraceae
Leguminosae
Papilonoidae
Fabaceae
Loranthaceae
Melastomataceae
Rutaceae
Sapindaceae
Sterculiaceae
Genus and species
RL
Veletra
Maka
Kimba ran0
Kimbaletika
Vanana
Tavolorano
H
T
T
T
T
T
E
E
E
E
L
E
Strongylodon sp.
Vahimberena
Vahimbomena
Tongalahy
Kalamasambarika
Anakatsimba
Fanjavala
Haftra blanche
Hadjavaka
Hazoharaka
Lambinanala
Unknown
Vosavoraka
L
L
E
E
E
E
E
E
E
E
E
E
-
***
Bakerella sp.
Medinilla sp.
Toddalia asiatica
Macphersonia sp.
***
***
***
***
***
Type
Ruellia sp.
Weinmannaia bojeriana
Symphonia sp.
Mammea zambo
Slonea rhodantha
Ravensara sp. 2
***
***
***
***
Vernacular
***
***
P
O
T
L
T
T
T
T
T
m
'I'
= liana; 0 = orchid; P = parasite; T = tree; *** = unidentified; RL
red-bellied lemur; E = eat flower; L = lick nectar.
"Size determined by averaging corolla lengths (n = 10 for each species).
*H = Herb; L
=
RB
Size
mma
4.0
2.0
15.0
4.0
25.0
20.0
80.0
10.0
15.0
25.0
2.0
5.0
60.0
10.0
15.0
4.0
E
7.0
8.0
rufous lemur; RB
=
ers. The faces of both lemurs species also were covered with pollen after nondestructive flower feeding on these two plant species. There were, however, two
levels of flower destruction: 1)either whole flowers including reproductive parts
were eaten, 2) only flower petals were removed and eaten leaving reproductive
parts intact. In all cases, rufous lemurs engaged only in the first type of destruction
by eating petals and all reproductive parts while red-bellied lemurs only knocked
off or ate flower petals.
Red-bellied lemurs and rufous lemurs licked nectar most often from Strongylodon sp. (31% and 43% of the time, respectively). Strongylodon sp. flowers were
irregular with a tubular shape. Nectar collected in a shallow, reservoir or basin at
the base of the tube, near the receptacle (Fig. 4).As they licked nectar, the focal
animal tipped the bottom of the reservoir toward their face, moved the tip of their
snout into the reservoir, and licked nectar.
196 I Overdorff
+ Rufous lemur
1988
198%
Fig. 3. Percentage of time red-belliedlemurs and rufous lemurs were observed flower feeding each month from
August 1988 through August 1989.
Fig. 4. Two examples of Strongylodon sp. flowers drawn to approximately two-thirds size. Note the bulbous
reservoir at the base of the flower which collects nectar.
There was no significant difference in the mean corollar length of flowers
consumed or licked by either lemur species (mean = 2.0 cm, SD = 1.9 cm). The
range in flower size was the same for both lemur species (0.4cm to 8.0 cm).
Strongylodon sp. and Sterculiaceae were the two largest flowers used by both
lemur species (80 mm and 60 mm, respectively, table I). Strongylodon sp. flowers
also emitted a strong smell and petals were leathery to the touch. These two flower
species also were the largest in the sample when compared to flowers that were not
used by rufous and red-bellied lemurs (Us = 306, Z = -2, P < .05).
Differences in the length of all flower licking bouts and flower eating bouts
were tested within and between lemur species. There was no difference in the
length of flower feeding bouts when flowers were licked or eaten within lemur
species although licking bouts tended to last longer than bouts where flowers were
eaten (Table 11). There also was no significant difference in the length of flower
licking or flower eating bouts between lemur species although red-bellied lemur
flower feeding bouts were slightly longer and more variable in length than rufous
lemur bouts.
Flower Feeding in Two Prosimian Primates / 197
TABLE 11. Mean Bout Length of Bouts When Flowers Were Licked and When Flowers
Were Eaten (in Minutes) bv Red-Bellied and Rufous Lemur*
~~~~~
Lick
Red-bellied lemur
Rufous lemur
Eat
Mean
SD
N
Mean
SD
N
7.1
5.6
8.2
6.1
62
24
5.5
4.1
16.3
3.8
10
75
*No significant difference.
Rufous lemurs exploited flowers from larger resources than red- bellied lemurs
(H = 43.4, P < .001, Table 111)and subgroup size was correlated with the size of the
flowering plant (r, = .67, P < .01). Larger subgroups of rufous lemurs also were
observed in flowering plants where flowers were licked than in plants where
flowers were eaten (Table IV). The largest flowering resources used by rufous
lemurs were located on the edges of their 100 ha home range and included species
from which rufous lemurs ate flowers (Ravensara sp. 2) or licked nectar (Strongylodon sp.).
In contrast, there was no difference in the number of red-bellied lemurs feeding in flowering plants where flowers were licked or eaten because the whole
group usually fed simultaneously. Both lemur species, however, fed longer in
larger flowering resources, and the relationship was stronger for rufous lemurs
(red-bellied lemurs rs = .43, P < .01; rufous lemurs r, = .70, P < .OOl).
Both lemur species ate more flowers per minute compared to the number of
flowers licked each minute (Table V). The number of flowers consumed or licked
also was negatively correlated with the size of the flower and did not matter how
the flower was eaten (r, = -0.8, P < .001).
Return trips to flowering resources where both lemur species licked nectar
occurred within 1or 2 days. Both species consistently returned within a day to the
same Strongylodon sp. liana (n = 6). In contrast, rufous lemurs did not return to
plants where they had consumed flowers until 14 days or more had passed (Fig. 5).
Differences were observed, however, between lemur species in the number of
plants of the same flowering species visited daily. Red-bellied lemurs only once
visited multiple Sterculiaceae trees in the same day. Rufous lemurs however,
visited multiple plants of different species within a single day (Table VI).
Morphology
As animals were weighed and processed, other researchers (Powzyk pers.
comm., Merelender, pers. comm.) and I noted a distinct difference between redbellied lemur and rufous lemur tongues. Red-bellied lemur tongues were feathered
or brush-like in appearance on the tip while rufous lemur tongues were rounded
and smooth (Fig. 6). This pattern was confirmed by checking photos of captured
individuals and individuals of each species housed a t the Duke University Primate
Center.
DISCUSSION
Red-bellied lemurs and rufous lemurs fed on flowers in different ways
throughout this study. Red-bellied lemurs primarily licked nectar from flowers
while rufous lemurs mainly consumed flowers by eating flower buds, petals, and
reproductive organs. Flower feeding, particularly nectarivory, is not uncommon in
primates and has been documented in many Neotropical primate species [Prance,
1980; Janson et al., 1981; Terborgh, 1983, Terborgh & Stern, 1987; Garber, 19881
198 I Overdorff
TABLE 111. Mean Size of Flowering Resources Where Flowers Were Eaten or Licked
by Red-BelliedLemurs and Rufous Lemurs
Lick
Red-bellied lemur
Rufous lemur*
Eat
Mean
SD
N
Mean
SD
N
65.6 m3
557.2 m3
91.4m3
104.3m3
62
24
7.6 m3
359.0m3
2.3 m3
403.6m3
10
75
*H = 43.4, P < .001.
TABLE IV. Mean Number of Individuals Feeding Per Bout (Subgroup Size) in
Tree or Lianas Where Flowers Were Eaten or Licked by Red-Bellied Lemurs and
Rufous Lemurs
Lick
Red-bellied lemur
Rufous lemur
Eat
Mean
SD
N
Mean
SD
N
2.6
7.0
0.6
1.4
62
24
2.8
4.7
0.8
2.6
10
75
TABLE V. Number of Flowers Eaten or Licked Per
Minute by Red-Bellied Lemurs and Rufous Lemurs
Eat
Mean
SD
n
Range
Lick
Mean
SD
n
Range
Red-bellied lemur
Rufous lemur
15.2
1
-
4.3
3.0
6
1.4-10.0
1.1
2.0
9
0.2-6.0
0.5
0.3
3
0.3-0.7
and other prosimian primates (Gatago crassicaudatus, Coe and Issac [19651;Lemur
mongoz, Tattersall and Sussman [19751; Sussman and Raven [19781; L. f. mayottensis, Tattersal 119791; Varecia variegata, White, pers. comm.). Very few of these
studies, however, have described flower feeding behavior and the seasonal patterns of flower feeding in detail.
Primatologists have provided two explanations for flower feeding behavior
regarding the proximate function of flower feeding and its possible evolutionary
function. The proximate explanation for flower feeding is that primates are satisfying an immediate nutritional need resulting from a seasonal shortage in other
critical food items. Flower nectar can be an important source of essential nutrients,
such as sucrose and proteins, when other food items are unavilable. For example,
nectarivory was observed most often during the dry season when only 10% of the
trees produced fruit in the Manu National Park, Peru [Terborgh & Stern, 19873.
In this study, however, flowers do not function as keystone resources based on
the seasonality of flower feeding, the amount of flowers present in the diet, and
phenological patterns. Red-bellied and rufous lemurs devoted the most time flower
feeding during a decline in fruit availability, not when fruit was most scarce. Fruit
Flower Feeding in Two Prosimian Primates I 199
(A) Rufous lemur
t
!c
t
Flowers licked
Flowers eaten
.
(B) Red-bellied lemur
10 1
0
1
2
3
4
5
6
7
8
9 1 0 1 1 12 1 3 1 0 1 5 1 6 1 7 1 8 1 9 2 0 2 1 22
Days between visits
Fig. 5. Number of return visits in days by (A) rufous lemurs and (B)red-bellied lemurs to flowering resources
where flowers were licked or eaten.
TABLE VI. Number of Patches Visited in the Same Day of the Same Flowering Plant
Species by Red-Bellied Lemurs and Rufous Lemurs
Plant suecies
~~
~
Date
Number visited
12/6/88
2
9/5/88
1/3/84
1/5/89
2
~
Red-bellied lemur
Strongylodon sp.
Rufous lemur
Sterculiaceae
Symphonia sp.
Rauensara sp.
Strongylodon sp.
12/16/88
12/1/88
12/2/88
3
3
2
2
2
also remained the preferred food item throughout the study [Overdoe, 19911.
Flowers did not constitute a substantial part of either lemur’s diets at any time
compared to some primate species such as mangabeys [Cercocebus a1bigena, Waser,
19771 or vervet monkeys [Cercopithecus aethiops, Whitten, 19881. Finally, ongoing
phenological sampling at Ranomafana indicates that fruiting and flowering patterns are unpredictable from year to year so that flowering resources are not
consistently reliable [Overdoe, 19911.
The evolutionary explanation for flower feeding is that some primate species
200 I Overdorff
A
B
Fig. 6. These two drawings depict the brush-like feathered tongue of the red-bellied lemur in proportion to the
animal's head (A) and in detail (B).
function as pollinators while feeding on flowers [Prance, 1980; Janson et al., 1981;
Torres de Assumpacao, 19811. This hypothesis is particularly relevant to prosimian
primates due to the low abundance of fruit bats on Madagascar [Coe & Issac, 1965;
Sussman & Raven, 1978; Sussman, 19781. Superficially, it appears that neither
lemur species consistently functioned as a pollinator of all flowering species visited
because they systematically destroyed flowers during flower feeding (when flowers were eaten or licked), and they did not consistently transfer pollen between
plants.
Strongylodon sp. was the only exception to this pattern and possessed several
characteristics, such as flower size, smell, and copious nectar, that would attract
potential mammalian pollinators [Carpenter, 1978; Sussman & Raven 1978; Faegri & van der Pijl, 19791.Neither lemur species destroyed the reproductive parts of
this flower, it was the largest flower visited by both lemur species, and it exuded
the strongest floral odor compared to other flowering species collected. Although
the amount of nectar produced daily was not measured, this species was the only
flower used by lemur species that had a tubular shape and a reservoir in which
nectar collected (Fig. 4).
Pollen also was observed on the faces of both lemur species as they traveled
between Strongylodon sp. and Sterculiaceae plants. Both lemur species, particularly rufous lemurs, visited more than one plant of both of these plant species in
the same day, although rufous lemurs destroyed Sterculiaceae flowers. Consequently, these two plant species are the strongest candidates for pollination by
red-bellied lemurs and rufous lemurs based either on the lack of destruction during
flower feeding andlor the possible transfer of pollen via the face from plant to
plant.
Of the two lemur species, however, the red-bellied lemur appears to be a more
efficient pollinator compared to the rufous lemur based on the behavioral and
Flower Feeding in Two Prosimian Primates / 201
morphological evidence. First, although red-bellied lemurs did not leave flowers
intact while feeding, they licked flower nectar without damaging reproductive
parts. In contrast, rufous lemurs completely destroyed flowers including reproductive parts while feeding on flowers. Second, the feathered or brush-like aspect of
red-bellied lemur tongues is very similar to morphological adaptations observed in
birds [Chruchill & Christensen, 19701 and bats that enables them to extract nectar
and pollen more efficiently [Faegri & van der Pijl, 19791.
This is only preliminary evidence, however, and warrants further investigation. Differences in these plant species’ flowering morphology and the seasonal
timing of inflorescenses needs to be examined in areas where either one or neither
lemur species exists and compared to patterns observed in RNP. The number of
flowers per plant, petal strength, nectar content, and nectar production also needs
further investigation.
In addition to the functional explanations behind flower feeding, differences in
flower feeding can be related to differences in overall feeding patterns by redbellied lemurs and rufous lemurs. The bout length, subgroup size, and number of
return visits to the same flowering plant were affected. The difference in bout
length where rufous lemurs and red-bellied ate flowers may have resulted from
differences in group size. As rufous lemur groups were three times larger than
red-bellied lemur groups, they may have depleted a flowering plant more quickly
as more group members fed simultaneously and more flowers were eaten per
minute than licked. Rufous lemurs also consistently visited flowering resources
that were much larger than those used by red-bellied lemurs, perhaps to accommodate the larger group sizes as subgroups size was correlated with flowering
resource size. This trend, however, was restricted to flowering resources and was
not observed in other types of food resources [Overdorff, 19911.
The shorter intervals between trips to plants where both lemur species licked
flowers implies that 1 to 2 days may be sufficient time for nectar to rejuvenate,
provided individuals lick nectar until all flowers are depleted. An alternative
explanation is that red-bellied and rufous lemurs fed only until satiated without
completely depleting the flower of its nectar.
Longer time intervals were observed between return trips to plants where
rufous lemurs ate flower parts. Both lemur species were followed weekly during
this time period so it is unlikely that the return times are an artifact of the data
collection schedule. One consideration is that rufous lemurs depleted all edible
flowers during a visit as they physically removed flowers by eating them. Rufous
lemurs ate eight times as many flowers each bout as they did when licking flower
nectar, but sample sizes were small for each category to be conclusive. A prediction
to be tested in future studies is that 14 days or longer is required for sufficient
flower development in those plant species to warrant a return visit. An another
alternative explanation is that rufous lemurs did not visit these trees more frequently as they were located on the far edge of the group’s home range. Rufous
lemurs typically used a 40 ha core area and only visited far edges of the home
range every 2 to 3 weeks to outlying food sources such as the larger flowering trees
and lianas [Overdorff, 19911. Therefore, the return time may not be a reflection of
how the flowering resource was used, but a consequence of how rufous lemurs use
their home range and what other food items were available to them in the core area
at that time.
The diet, locomotion, habitat preferences (preferred height in the canopy and
substrates used), and overall morphology of these two species is virtually identical
[OverdorfT, 19911. When examined on a finer level, however, subtle differences
emerge in their dietary preferences within food categories as documented in this
202 I Overdorff
paper. They used the same flowering resources but used them in different ways.
This pattern was observed in other food categories as well. Both lemur species, for
example, fed on the same plant species but rufous lemurs ate more mature leaves
and unripe fruits than red-bellied lemurs. It is these subtle differences in diet that
most likely allow these two similar species to coexist within the same habitat
[Schoener, 1974; Sussman, 1972, 1974; Struhsaker, 1975; Struhsaker & Oates,
1975; Oates 1977; Hladik, 19751.
CONCLUSIONS
1. In this study, red-bellied lemurs and rufous lemurs fed on flowers in different ways: red-bellied lemurs primarily licked flower nectar while rufous lemurs
mainly consumed all flower parts.
2. Flowers did not serve as an alternative food source when other resources
were unavailable as both lemur species fed on flowers throughout the year and
fruit remained the primary food item year round.
3. Both lemur species may serve as pollinators for Strongylodon sp. and Sterculiaceae plant species. Red-bellied lemurs, however, appear to be more efficient
pollinators as they did not destroy flower reproductive organs systematically and
had brush-like tongues which may enable them to extract nectar and pollen from
flowers more efficiently.
4. Feeding styles and differences in group size affected the size of flowering
patches visited, the amount of time both species ate flowers, and return trips to
flowering sources.
5. Subtle differences within food categories may allow these two otherwise
similar prosimian primate species to coexist.
ACKNOWLEDGMENTS
I would like to acknowledge the assistance of M. Raymond Rakotoandriana
and M. George Rakotoanrivo of the Department of Water and Forests of Madagascar and M. Berthe Rakotsamimanana and M. Benjamin Andriamihaga of the Ministry of Higher Education in Madagascar. I would like to thank Missouri Botanical
Garden for plant identifications. J. Powzyk is thanked for her drawings of Strongylodon sp. and the red-bellied lemur tongue. This paper was improved by comments
from P.C. Wright, P. Holroyd, C. Hemingway, C.P. van Schaik, F. White, and three
anonymous reviewers. Special thanks go to M.E. Winslett for his patience and field
assistance. The research for this project was funded by National Science Foundation grant BNS-8819559, Wenner-Gren Foundation, Douroucouli Foundation,
Duke Univeristy Travel Award, and National Sigma Xi Grand-in-Aid.
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