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Circadian rhythms in diet and habitat use in red ruffed lemurs (Varecia rubra) and white-fronted brown lemurs (Eulemur fulvus albifrons).

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 124:353–363 (2004)
Circadian Rhythms in Diet and Habitat Use in Red
Ruffed Lemurs (Varecia rubra) and White-Fronted Brown
Lemurs (Eulemur fulvus albifrons)
Natalie Vasey*
Department of Anthropology, Portland State University, Portland, Oregon 97207-0751
KEY WORDS
daily rhythms; nutrition; thermoregulation; sex differences; reproduction
ABSTRACT
Daily variation in niche use among vertebrates is attributed to a variety of factors, including
thermoregulatory, reproductive, and nutritional requirements. Lemuriform primates exhibit many behavioral and
physiological adaptations related to thermoregulation and
sharp, seasonal reproduction, yet they have rarely been
subjects of a quantitative analysis of circadian (or daily)
rhythms in niche use. In this study, I document daily
rhythms in diet and microhabitat use over an annual cycle
in two sympatric, frugivorous lemurs, Varecia rubra and
Eulemur fulvus albifrons. Data on diet, forest site, and
forest height were recorded at 5-min time points on focal
animals and divided into three time blocks for analysis
(06:00 –10:00 hr, 10:00 –14:00 hr, and 14:00 –18:00 hr). I
employed multivariate tests of independence to examine
daily rhythms in diet and microhabitat use according to
sex, season, and reproductive stage. Throughout the day,
V. rubra is frugivorous and dwells in the upper canopy,
with notable departures (especially for females) during
the hot seasons, gestation, and lactation. E. f. albifrons
has heterogeneous daily rhythms of food choice and microhabitat use, particularly across seasons, and both sexes
are equally variable. These daily rhythms in diet and
microhabitat use appear related to thermoregulatory and
nutritional requirements, seasonal food availability and
circadian rhythms of plant (and possibly insect) palatability, predator avoidance tactics, and in the case of Varecia,
to reproduction. Daily rhythms of food choice in V. rubra
support two previously suggested hypotheses explaining
why primates consume more nonfruit items late in the
day, whereas those of E. f. albifrons are too variable to
lend support to these hypotheses. Am J Phys Anthropol
124:353–363, 2004. © 2004 Wiley-Liss, Inc.
Many organisms vary their diets, microhabitat
use, and activity patterns on a regular schedule
throughout the course of the 24-hr light-dark cycle of
the earth. These outward manifestations of an endogenous, time-measuring function (i.e., “biological
clock”) are referred to as daily, or circadian,
rhythms. In mammals, the suprachiasmatic nucleus
of the hypothalamus is the pacemaker responsible
for daily rhythms in physiology and behavior. However, daily rhythms are not strictly fixed. They respond to environmental stimuli, especially light
(e.g., light-entrainment can lengthen or shorten cycle length from 24 hr), they can be phase-shifted
(e.g., peaks in periodicity can be altered), they have
a mutable genetic basis, and they even respond to
social context and domestication (Plyusnina et al.,
1991; Akiyama et al., 1998; Zordan et al., 2000;
Toma et al., 2000; Suarez et al., 2001).
Some daily rhythms are found across a broad array of vertebrate taxa. For example, feeding, coprophagy, locomotor activity, and thermoregulatory
mechanisms often show regular daily peaks (Salmo
salar (Atlantic salmon), Kadri et al., 1991; Lepus
brachyurus (Japanese hares), Hirakawa, 1994). In
some cases, these daily peaks differ among age-sex
classes (Misgurnus anguillicaudatus (loach fishes),
Naruse and Oishi, 1996) and show seasonal periodicity, referred to as circannual rhythms (Agrionemys
horsfieldi (turtles), Wuntke and Siegmund, 1992;
Cricetus cricetus (European hamsters), Wollnik and
Schmidt, 1995; Cynops pyrrhogaster (Japanese
newts), Nagai and Oishi, 1998; Tiliqua rugosa (Australian sleepy lizards), Firth and Belan, 1998). Reproductive activity can also be subject to circadian
rhythms (e.g., Arvicanthis niloticus (Nile grass rats),
McElhinny et al., 1997; Cynops pyrrhogaster (Japanese newts), Nagai and Oishi, 1998). Daily rhythms
have a more complex basis in some taxa. For exam-
©
2004 WILEY-LISS, INC.
Grant sponsor: Wenner-Gren Foundation; Grant sponsor: Leakey
Foundation; Grant sponsor: National Science Foundation; Grant
sponsor: Primate Conservation, Inc.; Grant sponsor: Boise Fund;
Grant sponsor: Sigma Xi.
*Correspondence to: Natalie Vasey, Department of Anthropology,
Portland State University, Portland, OR 97207-0751.
E-mail: nvasey@pdx.edu
Received 26 September 2002; accepted 6 June 2003.
DOI 10.1002/ajpa.10357
Published online 19 November 2003 in Wiley InterScience (www.
interscience.wiley.com).
354
N. VASEY
ple, foraging peaks in Amblyrhynchus cristatus (Galapagos marine iguanas) appear to be governed by a
combination of circadian as well as circatidal
rhythms (Wikelski and Hau, 1995), while coprophagy in Octodon degus (the degu), an herbivorous
Chilean rodent, is governed by both a circadian
rhythm of nocturnal coprophagy and a digestive
physiology requiring continuous intake into the gastrointestinal (GI) tract and a constant rate of output
from the colon (Kenagy et al., 1999).
There is every reason to suspect that wild primates express daily rhythms in some ecological variables, but few such rhythms have been documented.
One study of Colobus badius, an anthropoid primate, showed a link between feeding and thermoregulation tied in with seasonal shifts. These African colobine monkeys remained high in the canopy
all day in the cold season, but regularly descended
lower in the forest canopy to feed in the morning and
evening during the hot dry season, thereby avoiding
high temperatures and circumventing thermal
stress (Clutton-Brock, 1973). A study of two Malagasy lemurs, Lemur catta and Eulemur fulvus rufus,
showed that daily activity rhythms were related to
behavioral thermoregulation. In cooler regions of
Madagascar, both species sunned themselves early
in the morning after experiencing cool nighttime
temperatures, whereas in warmer regions of Madagascar, both species rarely sunned themselves, and
feeding bouts occurred in the earlier, cooler hours of
the day in L. catta (Sussman, 1974, 1975). Where
the two species were sympatric, resting and feeding
peaks differed between them, thereby contributing
to niche separation (Sussman, 1974, 1977). Lastly,
the two species differed in their daily rhythms of
forest strata use, whether in allopatry or sympatry
(Sussman, 1974).
Lemurs exhibit many behavioral and physiological adaptations related to thermoregulation (e.g.,
sunning, torpor, and seasonal fattening) and photoperiodically cued seasonal reproduction (Van Horn,
1980; Rasmussen, 1985). Thus it seems highly likely
that predictable daily rhythms should form part of
their behavioral and ecological profile. Yet daily
rhythms have rarely been studied in lemurs (Sussman, 1974, 1975; Freed, 1986). In recent studies
examining interspecific and intraspecific patterns of
niche separation in Varecia rubra and Eulemur fulvus albifrons (two closely related, frugivorous, sympatric lemurs), I found that multiple factors influenced niche use, including seasonal differences in
climate and food availability, thermoregulatory
needs, reproductive patterns, nutritional needs, and
predator avoidance tactics (Vasey, 2000, 2002; for
revised taxonomy, see Groves, 2001; Vasey and Tattersall, 2002). Given this intra-annual variation,
daily rhythms in diet and microhabitat use in these
two lemurs are unlikely to be homogeneous throughout the day and from season to season, but rather
should reflect species-specific thermoregulatory, reproductive, and nutritional requirements in addi-
tion to predator-avoidance tactics (niche use hypothesis 1).
A more specific set of predictions can be proposed
concerning daily rhythms in diet. It has been a challenge to explain daily rhythms in this niche parameter fully, because its underlying adaptive basis has
been difficult to identify. Many wild primates consume more fruit in the early part of the day and
diversify their diets in the later part of the day
(reviewed in Clutton-Brock, 1977). Leaves, in particular, are fed upon late in the day by many primates (reviewed in Chapman and Chapman, 1991).
A variety of hypotheses have been offered to explain
this phenomenon, e.g., diet hypothesis 1: feeding on
fruit early in the day may provide quick energy after
nighttime rest when food energy is depleted (Clutton-Brock, 1977; Raemakers, 1978); and diet hypothesis 2: there may be an advantage to consuming
leaves late in the day because, being naturally high
in fiber and secondary compounds, nutrients in
leaves can be slowly extracted during nighttime inactivity (Milton, 1979; Glander, 1982).
Hypotheses 1 and 2 concerning diet do not conflict
with each other, yet Ganzhorn and Wright (1994)
observed that neither is sufficient in the case of
Aotus, the night monkey, whose leaf-eating peaks
late in the day at the start of its nocturnal activity
cycle. Their phytochemical study of Malagasy lemur
food plants indicated that soluble carbohydrates in
leaves increase throughout the day, whereas protein
content does not vary much. They therefore suggested that by eating leaves late in the day, primates may be optimizing their energy intake by
acquiring proteinaceous leaves while they are also
highest in carbohydrate value (diet hypothesis 3).
Hence, when to eat leaves may be, in some measure,
dictated by circadian rhythms of plant palatability.
This hypothesis, unlike earlier ones, takes into account the need for primates to acquire dietary protein.
To date, our understanding of daily rhythms in
primate diets is based on field studies of anthropoid
primates (see above references). On what basis
might we expect dietary diversification late in the
day in lemurs? Phytochemical work on lemur food
plants indirectly suggests such a pattern (Ganzhorn
and Wright, 1994). Direct observations that formed
part of a field study of V. rubra and E. f. albifrons
also suggest that lemurs might share this pattern
with other primates (Vasey, 2000). Females of both
species simultaneously diversify their diets with
more seasonally available low-fiber, high-protein
plant foods (young leaves, flowers) during the hot
seasons and during costly reproductive stages (gestation and lactation), whereas males do not. In addition, V. rubra shows pronounced sex differences in
diet during costly reproductive stages, with females
acquiring more low-fiber, high-protein plant foods
than males. E. f. albifrons shows far fewer sex differences in diet (Vasey, 2002). These interspecific
and intraspecific patterns have been attributed to
CIRCADIAN RHYTHMS IN V. RUBRA AND E. F. ALBIFRONS
differing energetic investments in reproduction between the two species and between the sexes. Sex
differences in diet cannot be attributed to body-size
dimorphism or male dominance, because most lemurs are monomorphic in body size (Kappeler,
1991), and none show male dominance (reviewed in
Wright, 1999). The relatively pronounced seasonal
shifts in diet for V. rubra females and their sharp
dietary sex differences function in tandem with their
higher energetic investment in reproduction (Vasey,
2000, 2002). Relative to E. f. albifrons, Varecia has a
shorter gestation, larger, heavier litters, more concentrated milk, and nonclinging, rapidly growing
altricial young that are kept in nests or stashed
(Foerg, 1982; Rasmussen, 1985; Pereira et al., 1987;
Young et al., 1990; Tilden and Oftedal, 1997; Vasey,
unpublished findings).
In their quest for high-protein foods, could the
behavior of these lemurs, and of females in particular, be explained by hypotheses 1–3, described
above? This would be cost-efficient, especially for a
primate with relatively high reproductive investment such as V. rubra. If daily peaks in consumption
of high-protein, nonfruit items occur, we would predict such peaks to occur late in the day, to be more
pronounced in females (especially Varecia), and to
occur during costly reproductive periods (i.e., during
gestation and lactation) or when such foods are
abundant (diet: prediction 1). This study, in which
sex, season, and reproductive state are partitioned,
allows a controlled examination of the influences on
daily rhythms of food choice and microhabitat use.
METHODS
Study site
The study site is located in the Masoala National
Park in northeastern Madagascar in a region of
primary lowland coastal rain forest known locally as
Andranobe. Average annual rainfall over the course
of the study was 5,110.26 mm. Average monthly
temperature maxima ranged from 22.5–31.6°C, and
average monthly temperature minima ranged from
19 –23.5°C. There are four distinct seasons: 1) hot
rainy (January–March), 2) transitional cold (April–
May), 3) cold rainy (June–August), and 4) hot dry
(October–December). Assessments of plant phenology from northeastern Madagascar indicate that
fruit, flowers, and young leaves are more abundant
in the hot seasons, with additional increases in
flower and young leaf availability at the end of the
cold rainy season (Andrianisa, 1989; Rigamonti,
1993). Increases in flower and young leaf availability therefore occur during the earlier parts of gestation and lactation (see Table 1 in Vasey, 2002).
Reproductive stages of V. rubra were highly synchronized among individuals in the study community: individuals mated in July and gave birth at the
very end of October (Vasey, 1997a). Reproductive
stages of E. f. albifrons females within the study
group were more protracted but still synchronous:
355
females gave birth in mid-October and early December (Vasey, 1997a). At 4 months of age, infants of
both species were largely weaned (Vasey, unpublished findings). “Nonreproductive” throughout the
text refers to the period of the year when adult
females were neither pregnant nor lactating. For
both species, births occur when seasonal food availability and diversity are increasing. More extensive
descriptions of the study site, region, climate, food
availability, and reproductive schedules can be
found in Vasey (1997a,b, 2000, 2002).
Study population and data collection
At Andranobe, V. rubra lives in large multimalemultifemale communities with a fission-fusion type
of social organization, whereas E. f. albifrons lives in
small, cohesive multimale-multifemale groups (Vasey, 1997a). Data were collected on adult animals on
5– 8 consecutive days per species per month over 12
consecutive months (January–December 1994), with
the help of two field assistants who assisted with
animal tracking. Focal animal observation periods
lasted from 8 –13 hours, depending upon seasonal
differences in day length and time needed to locate
animals at dawn. V. rubra was observed for 672 hr
(5 乆, 463 hr; 3 么, 209 hr) during 78 focal animal
observation periods, and E. f. albifrons was observed
for 619 hr (4 乆, 410 hr; 2 么, 209 hr) during 64 focal
animal observation periods. Observations were
made on one community of V. rubra and on one
group of E. f. albifrons. To facilitate location of animals at the beginning of each observation period,
three V. rubra (2 乆 and 1 么, each from a separate
core group within the community) and one E. f.
albifrons (么) were fitted with radio collars manufactured by Telonics (Mesa, AZ). An additional E. f.
albifrons individual (乆) was fitted with a nylon collar without a transmitter.
At 5-min fixed-interval time point samples (Crook
and Aldrich-Blake, 1968; Altmann, 1974), I recorded
diet and habitat use for the following variables: food
item consumed (fruit, flowers, mature leaves, young
leaves, and miscellaneous); estimated height of focal
animal from the ground in 5-m increments; and
forest site (ground, trunk, major branch, crown, liana, or liana within tree crown). Tree height and
crown diameter estimates were made visually and
were periodically verified for accuracy, using a clinometer.
Data analysis
I pooled time-point samples for all focal animals
for each species, following recommendations by
Leger and Didrichsons (1994). For analysis of daily
rhythms in diet, forest sites, and forest heights, frequencies were calculated based on the number of
scores for each variable category (e.g., forest site:
ground, trunk, crown, or liana) divided by the total
number of records for that variable subdivided by
sex, season, and time block. For dietary data, I also
356
N. VASEY
subdivided time-point data by reproductive stage.
For females in the latter analyses, I included data
only for those who were reproductively active during
the study period (i.e., those who were either gestating or lactating; V. rubra, n ⫽ 4; E. f. albifrons, n ⫽
2). As E. f. albifrons females showed less reproductive synchrony, data collected during different, but
overlapping, sets of months were included in each
reproductive stage for each respective female. All
time points that fell within the following time blocks
were used for analysis regardless of the total length
of observation period: 06:00 –10:00 hr (morning), 10:
00 –14:00 hr (midday), and 14:00 –18:00 hr (late afternoon/early evening, i.e., late in the day).
Bivariate and multivariate analyses of frequencies were used to examine the extent of association
between each variable and their respective number
of categories (or states). In effect, these analyses test
for significant departures from an independent assortment of variables, an expectation of independence being the null hypothesis. I report the Cochran-Mantel-Haenzel (CMH) statistic for analyses of
multiway contingency tables, and the Mantel-Haenzel (MH) chi-square statistic for two-way tables
(Bishop et al., 1975), using standard notation for
significance levels (*P ⬍ 0.05; **P ⬍ 0.01; ***P ⬍
0.001; Sokal and Rohlf, 1981). Statistical tests were
run using the SAS System for Windows, release 6.12
(1989 –1996, SAS Institute, Cary, NC). For further
details on the study population and on data collection and analysis, see Vasey (2000).
RESULTS
Daily feeding rhythms
V. rubra. V. rubra feeds on fruit more than on any
other item in every time block in every season. Furthermore, time spent feeding on each food item is
similar from time block to time block on an annual
basis, across seasons, within seasons, and between
sexes (Table 1, Fig. 1a). The only departure from this
overall pattern is that males feed significantly more
often on flowers late in the day during the hot dry
season (31% of time points, n ⫽ 21; Table 1 contains
sample sizes, statistics, and significance levels for
analyses done on combined sex and on divided sex
data).
As with seasonal data, time spent feeding on each
food item is similar from time block to time block
across reproductive stages. Importantly however,
there are differences within stages and according to
sex (Table 2). Late in the day, V. rubra supplements
its diet with more flowers and foliage (especially
young leaves) during gestation and lactation (Fig.
2a). When these data are divided by sex, males contribute significantly to increased flower intake late
in the day during gestation (25%, n ⫽ 20). However,
only females consume young leaves late in the day
during gestation (3%, n ⫽ 8) and lactation (17%, n ⫽
30; Table 2 contains sample sizes, statistics, and
significance levels for analyses done on combined
sex and on divided sex data). In fact, males were
rarely ever recorded eating foliage.
E. f. albifrons. For E. f. albifrons, time spent feeding on each food item is similar from time block to
time block on an annual basis and within each season. There are departures from independent assortment across seasons by sex, but these departures do
not show an increase in nonfruit consumption exclusively late in the day (Table 1, Fig. 1b). Females are
responsible for a morning peak in flower feeding in
the cold rainy season (19%, n ⫽ 22), and they also
consume more flowers late in the day in the hot dry
season (44%, n ⫽ 34), whereas males eat more miscellaneous items (mainly faunal material) in the
morning during the hot rainy season (30%, n ⫽ 10).
Thus, seasonal data show sex-specific peaks in consumption of nonfruit items both in the morning and
late in day, and these peaks occur during seasonal
food abundance as well as seasonal food scarcity. As
with seasonal data, time spent feeding on each food
item in each time block differs across reproductive
stages by sex, but there is no uniform pattern of
nonfruit consumption late in the day (Table 2; Fig.
2b). During lactation, females eat more young leaves
midday (23%, n ⫽ 11) and more flowers late in the
day (42%, n ⫽ 14), whereas during periods of female
gestation, males eat more flowers late in the day
(24%, n ⫽ 18).
Daily rhythms of forest site use
V. rubra. V. rubra is primarily a crown dweller all
day long in every season, particularly during the
cold seasons. Significant departures from this heavy
use of tree crowns occur within the hot seasons
according to sex (Table 1, Fig. 1c). At midday in the
hot rainy season, females in particular spend more
time on major branches (乆, 7.5%, n ⫽ 42 vs. 么,
3.75%, n ⫽ 7), and use more crown lianas (乆, 7%,
n ⫽ 41 vs. 么, 1%, n ⫽ 2). In the hot dry season,
females spend more time than males on crown lianas in the morning (乆, 13.5%, n ⫽ 57 vs. 么, 2.75%,
n ⫽ 6) and on lianas outside of tree crowns late in
the day (乆, 3%, n ⫽ 15 vs. 么, 1%, n ⫽ 2).
E. f. albifrons. E. f. albifrons is characterized by
significant heterogeneity in use of forest sites from
time block to time block on an annual basis and
across seasons according to sex. Unlike Varecia,
they also use the ground. Departures from independent assortment are significant for one or both sexes
within every season (Table 1, Fig. 1d). The annual
pattern is due overall to extensive use of crown
lianas in the morning and both crown lianas and
lianas at midday. Additionally, there is substantial
seasonal and intraspecific heterogeneity, such as the
marked use of tree crowns, primarily by females (乆,
92%, n ⫽ 417 vs. 么, 86%, n ⫽ 118), at the expense of
crown lianas in the morning during the hot dry
season, and the decreased use of crown lianas (乆,
4.5%, n ⫽ 16; 么, 2.75%, n ⫽ 6) and a concomitant
—
(68)
—
(78)
—
(97)
19.68***
(199)
0.53
(398)
—
(200)
—
(386)
1.42
(479)
1.26
(466)
—
(278)
—
(483)
0.31
(678)
1.87
(2,132)
MH
0.55
(1,905)
0.07
(1,905)
CMH
—
(401)
—
(409)
—
(516)
0.00
(794)
3.00
(1,235)
—
(647)
0.61
(1,332)
42.69***
(1,442)
4.80*
(1,636)
3.70
(1,056)
0.09
(1,848)
36.91***
(2,236)
6.05*
(7,448)
MH
7.64*
(6,776)
8.10*
(6,776)
CMH
Forest site
Varecia rubra
16.47***
(402)
24.41***
(405)
5.30*
(516)
4.21*
(790)
8.02**
(1,240)
0.00
(636)
20.44***
(1,321)
0.99
(1,425)
0.54
(1,642)
17.31***
(1,041)
21.4***
(1,837)
3.22
(2,215)
15.32***
(7,420)
MH
4.65
(6,735)
5.13
(6735)
CMH
Height
5.43*
(93)
0.01
(69)
3.63
(149)
0.06
(136)
0.18
(104)
0.13
(125)
10.26***
(272)
4.99*
(337)
1.70
(197)
0.15
(194)
1.80
(421)
1.54
(473)
0.88
(1,422)
MH
CMH
15.23***
(1,285)
15.98***
(1,285)
Diet
0.12
(619)
7.45**
(458)
19.33***
(666)
0.03
(452)
4.54*
(625)
2.39
(657)
15.74***
(1,133)
12.84***
(1,285)
2.50
(1,244)
0.26
(1,115)
31.08***
(1,799)
9.82**
(1,737)
19.95***
(6,607)
MH
49.11***
(5895)
48.07***
(5895)
CMH
Forest site
Eulemur fulvus albifrons
0.00
(648)
12.58***
(471)
3.73
(670)
7.55**
(453)
22.21***
(654)
1.19
(677)
6.10*
(1,143)
6.13*
(1,279)
89.99***
(5,995)
87.64***
(5,995)
CMH
Height
14.29***
(1,302)
9.19**
(1,148)
9.15**
(1,813)
11.75***
(1,732)
6.96**
(6,716)
MH
1
d.f. ⫽ 2 for season ⫻ block ⫻ niche variable, d.f. ⫽ 2 for season ⫻ sex ⫻ block ⫻ niche variable, and d.f. ⫽ 1 for all other tests. MH, Mantel-Haenzel chi-square statistic; CMH,
Cochran-Mantel-Haenzel row mean scores statistic. Dashes indicate that tables were not produced because niche variables were so homogeneous that they resulted in multiple column
sum zeros. Sample sizes (n) are indicated in parentheses.
* P ⬍ 0.05.
** P ⬍ 0.01.
*** P ⬍ 0.001.
Hot dry
Cold rainy
Transitional cold
Males
Hot rainy
Hot dry
Cold rainy
Transitional cold
Females
Hot rainy
Season ⫻ sex ⫻ block ⫻ niche variable
Hot dry
Cold rainy
Transitional cold
Hot rainy
Season ⫻ block ⫻ niche variable
Block ⫻ niche variable
Niche variable
Diet
TABLE 1. Intraspecies tests of independence between niche variables and time-blocks by season1
358
N. VASEY
Fig. 1. Time spent during each time block feeding on various food items (a, b), in various forest sites (c, d), and at different forest
heights (e, f), according to season based on combined sex data, for V. rubra (a, c, e) and E. f. albifrons (b, d, f). Time blocks include
morning (06:00 –10:00 hr), midday (10:00 –14:00 hr), and late in day (14:00 –18:00 hr). Table 1 contains sample sizes and statistics for
analyses based on combined sex data (shown here) and for analyses based on divided sex data. Salient percentages from divided sex
analyses are provided in text.
CIRCADIAN RHYTHMS IN V. RUBRA AND E. F. ALBIFRONS
TABLE 2. Intraspecies tests of independence between diet, time
block, and reproductive stage1
Varecia rubra
Eulemur fulvus
albifrons
MH
MH
Stage ⫻ block ⫻ diet
Gestation
Lactation
Nonreproductive
Stage ⫻ sex ⫻ block ⫻
diet
Females
Gestation
Lactation
Nonreproductive
Males
Gestation
Lactation
Nonreproductive
CMH
3.24
(2,046)
4.82*
(788)
10.53***
(677)
1.52
(581)
CMH
22.64***
(1,014)
0.72
(477)
6.05*
(270)
0.51
(267)
22.64***
(2,046)
(1,014)
3.77
(286)
3.98*
(130)
2.51
(140)
13.41***
(208)
4.34*
(178)
—
(140)
3.84*
(191)
2.52
(140)
0.26
(127)
15–20 m). However, there is enormous heterogeneity in how time is divided between strata from time
block to time block across seasons, within seasons,
and when divided by sex (Table 1, Fig. 1f). This is
particularly true in the morning: E. f. albifrons
spends the largest portion of its time between the
ground and 5 m in the hot rainy season, between
5–10 m in the cold seasons, and between 10 –15 m in
the hot dry season.
DISCUSSION
3.20
0.25
(580)
17.21***
(499)
1.42
(441)
359
d.f. ⫽ 2 for stage ⫻ block ⫻ diet, d.f. ⫽ 2 for stage ⫻ sex ⫻
block ⫻ diet, and d.f. ⫽ 1 for all other tests. MH, Mantel-Haenzel
chi-square statistic; CMH, Cochran-Mantel-Haenzel row mean
scores statistic. Dash indicates that table was not produced because niche variables were so homogeneous that they resulted in
multiple column sum zeros. Sample sizes (n) are indicated in
parentheses.
* P ⬍ 0.05.
** P ⬍ 0.01.
*** P ⬍ 0.001.
1
increase in the use of tree trunks (乆, 8.75%, n ⫽ 30;
么, 6%, n ⫽ 13) late in the day during the cold
seasons (both sexes).
Daily vertical ranging rhythms
V. rubra. V. rubra spends significantly different
amounts of time in each forest level from time block
to time block, yet the pattern is largely similar
across seasons and between the sexes (Table 1, Fig.
1e). In nearly every time block within every season,
V. rubra spends most of its time between 15–20 m,
the second largest bulk of time between 20 –25 m,
and the third largest bulk of time between 10 –15 m.
The transitional cold season illustrates the most
extreme version of this pattern and the most uneven
use of forest levels (e.g., over 80% of time is spent
over 15 m in the morning time block). In the opposite
extreme, during the hot rainy season, V. rubra uses
forest levels more equally in each time block. The
amount of time spent below 15 m in the second and
third time blocks is markedly greater during the hot
rainy season (Fig. 1e).
E. f. albifrons. In each time block, E. f. albifrons
distributes its time relatively evenly in four 5-m
height categories (0 –5 m, 5–10 m, 10 –15 m, and
Sex differences and daily rhythms in
microhabitat use
As predicted, daily rhythms in diet and microhabitat use in V. rubra and E. f. albifrons are not homogeneous throughout the day and from season to season (niche use hypothesis 1). In terms of
microhabitat use, daily rhythms appear linked to
species-specific thermoregulatory requirements,
predator-avoidance tactics, and in the case of Varecia, to reproduction. V. rubra carries out most of its
activities in the crowns of high-canopy trees regardless of time of day or season (Vasey, 2000, 2002), and
this use of high crowns is particularly evident during the morning in the transitional cold season. During the cold seasons the sun appears briefly throughout the day amid torrential rain and fast-moving
clouds, and V. rubra seizes these brief opportunities
to sun itself in open areas in the canopy. Sun bathing occurs exclusively in the exposed upper canopy.
The few departures from this upper canopy usepattern shown in Results are linked to other thermoregulatory needs and to reproductive and predator-avoidance strategies. From midday on in the hot
rainy season, V. rubra descends to lower canopy
levels. These descents illustrate attempts to remain
cool during a season and time of day when ambient
temperature is highest (mean seasonal maximum,
30.25°C). V. rubra rests, drinks from tree holes, and
travels at these lower levels, and as a consequence,
uses major branches more often. Another departure
occurs during the hot dry season, when females use
lianas in the crowns of trees more often than males
in the morning and late in the day. This use of crown
lianas corresponds to the long periods of time females spend in nests after infants are born (November) and in stashing depots thereafter (November–
January), keeping their young warm and nourished.
After approximately 2 weeks of age, infants are
moved to concealed, protected, and supportive spots
in the canopy created by liana tangles or other foliage. Infants are difficult to see and access in such
spots, and are effectively protected against predators and the elements (e.g., heat loss) when left
unattended (Vasey, 1997a, 2000, unpublished findings).
E. f. albifrons carries out its maintenance activities in a wide variety of forest sites and vertical
strata, showing heterogeneity throughout the day
and from season to season. Males and females are
360
N. VASEY
Fig. 2. Time spent during each time block feeding on various food items according to reproductive stage based on combined sex
data. a: V. rubra. b: E. f. albifrons. Time blocks include morning (06:00 –10:00 hr), midday (10:00 –14:00 hr), and late in day
(14:00 –18:00 hr). Table 2 contains sample sizes and statistics for analyses based on combined sex data (shown in this figure) and for
analyses based on divided sex data. Salient percentages from divided sex analyses are provided in text.
equally variable. This pattern of microhabitat use
demonstrates how E. f. albifrons uses its relatively
small home range very thoroughly for a wide variety
of food resources, resting locations, and travel substrates. As with V. rubra, their microhabitat niche
seems well-designed to avoid predators and to meet
thermoregulatory (but not reproductive) requirements. On a regular basis, animals enter crown lianas and lianas for their midday rest period where
they are well-camouflaged, tucked out of sight from
both aerial and ground predators. These sites often
have very restricted arboreal access, requiring the
lemurs to enter and exit the spot single-file using the
single arboreal pathway available. Resting in dense
lianas also protects them from high ambient temperatures (ranging as high as 40.5°C), the cold, the rain,
and the wind. In addition, E. f. albifrons is a “social
thermoregulator;” animals huddle together and
wrap their tails around each other, a behavior never
observed among V. rubra adults (see also Morland,
1993, and Discussion below of nesting in Varecia).
During the one relatively dry season, E. f. albifrons
spends more time in open tree crowns in the morning.
Sex differences and daily rhythms in diet
Daily rhythms in diet for E. f. albifrons do not
show clear support for the prediction that daily
peaks in consumption of high-protein, nonfruit
items would occur late in the day, be more pronounced in females, and occur during costly reproductive periods or when such foods are abundant
(diet: prediction 1). Nor do they show any clear pattern. In E. f. albifrons, both males and females show
peaks in consumption of high-protein, nonfruit
items, and these peaks do not uniformly occur during costly reproductive phases or when such foods
are abundant. Furthermore, such peaks occur in the
morning, at midday, and late in the day. Thus, E. f.
albifrons has a relatively diverse diet throughout
the day, and various daily rhythms in food choice are
evident. Because E. f. albifrons males alone show a
morning peak in consumption of miscellaneous
items (mainly insect material) in the hot rainy season, this could indicate that males have a propensity
for seeking out mobile sources of protein which are
more costly to obtain and process (see also Vasey,
2000; Rose, 1994), and/or that these insects are more
easily digested early in the day. Millipedes, in particular, require extensive preparation time once captured. Even once they are rolled in the hands and
salivated on, presumably to reduce toxicity, they
often still escape uneaten. On the other hand, sexspecific peaks in daily rhythms of nonfruit consumption (including the apparent penchant of E. f. albifrons males for insects) may simply be due to
sampling a species with a highly diverse diet. Daily
rhythms of food choice in E. f. albifrons may in fact
reflect multiple influences in combination: seasonal
patterns of food availability, dietary heterogeneity,
and sex differences (see also Vasey, 2002), in addition to circadian rhythms of plant or insect palatability.
In contrast to E. f. albifrons, daily rhythms in diet
for V. rubra do support prediction 1 concerning diet,
showing a clearly interpretable pattern. High-protein, nonfruit items are fed on late in the day during
costly reproductive phases and when such foods are
abundant. Quantitative analyses presented here indicate that both sexes show this pattern, with males
increasing intake of flowers late in the day during
gestation and the hot dry season (Tables 1 and 2),
and females feeding more often on young leaves late
in the day during lactation (Table 2). These increases correspond to peaks in flower and young leaf
availability during the earlier parts of gestation and
CIRCADIAN RHYTHMS IN V. RUBRA AND E. F. ALBIFRONS
lactation (see Methods). Although the number of
males under observation (3) was smaller than the
number of females (5), the results for males appear
representative, as the frequency distributions for
each male are similar and a large number of time
point records were employed in analyses (Tables 1
and 2).
Young leaves are the most easily digested source
of plant protein in the forest due to their high protein-to-fiber ratio, while flowers contain water, protein (in pollen), and simple sugars (Richard, 1985).
High-protein foods are critical for milk production
and to replace lost energy reserves. Protein requirements of pregnant and lactating primates are estimated to increase 20 – 46% above baseline levels,
and perhaps more in those (like Varecia) that produce rich milk (Oftedal, 1991). However, while nutritional requirements of gestation and lactation adequately explain sex differences in the diet of V.
rubra (see also Vasey, 2002), they do not, by themselves, explain the daily rhythm of leaf-eating in
females. In this regard, my case study from Andranobe (see below) suggests prominent roles for
digestive physiology (diet hypothesis 2), circadian
rhythms of plant palatability (diet hypothesis 3),
and yet a third factor: the thermoregulatory needs of
Varecia infants. All factors indicate that an energy
conservation strategy is at work. High-protein foods
generally require more time for nutrient extraction;
digestion, absorption, transport, and protein synthesis are parts of a lengthy process of creating milk
from leaves (and other plant foods). V. rubra females
may increase intake of high-protein foods late in the
day, which take longer to digest (diet hypothesis 2),
to tide them through the night while they are first
starting to lactate and cannot leave their nestlings
unattended, susceptible to cold and vulnerable to
nocturnal predators. Only mothers were observed
nesting infants, so other group members were not a
source of heat to newborns (see also Morland, 1993,
p. 200). These females may also be optimizing their
energy intake by ingesting leaves at the time of day
when they are highest in carbohydrate value (diet
hypothesis 3).
At Andranobe, lactating females began feeding
extensively on young leaves immediately after giving birth, while newborns were still in the nest.
Mothers left their nestlings for rapid foraging bouts
several times a day during their first week of life
(Vasey, unpublished findings). The last feeding bout
of the day occurred shortly before dusk and ended
with an extensive feed on young leaves growing close
to their nests. Often these were immature liana
leaves growing though the canopy of the very same
trees in which they built their nests. V. rubra give
birth during the hottest, driest time of the year
(October–November), which should ensure that altricial V. rubra infants do not undergo thermal
stress while mothers are away feeding during the
day. However, nighttime temperatures fall regularly (Vasey, 2000), and seasonal weather patterns
361
are not always predictable. In 1994, infants were
born and nested during an unseasonably cold and
rainy week (for climatic data from 1992–1996, see
Vasey, 1997a). One mother showed gross physical
signs of reproductive stress: she became emaciated
and lost much of her lustrous coat while nesting her
newborn twins. She may have used her fur as nesting material, as observed in captivity (Petter-Rousseaux, 1964), though it remains unclear whether
this behavior was an artifact of poor captive management. Regardless of how much climatic conditions fluctuate from birth season to birth season,
this case study illustrates that daily rhythms of food
choice coalesced with digestive, thermoregulatory,
and nutritional requirements, as well as with seasonal peaks in availability of protein-rich plant
foods, to ensure infant survivorship at Andranobe in
1994.
All three hypotheses concerning diet in large measure assume that daily rhythms in diet are dictated
by choice. However, daily variation in diet may also
be governed by shifting food availability during the
course of an organism’s active period and food perception capabilities. For example, if fruit feeding
peaks in the early part of the day, choosy diurnal
frugivores (i.e., many primates) may find less palatable fruit available within their home ranges toward
the end of the day, spurring a daily dietary rhythm
of consuming nonfruit items. In effect, decreasing
food availability throughout the day could spur competition for fruit late in the day. This potential factor
is probably of negligible importance for V. rubra.
Because V. rubra appears to be a predominant frugivore in its biotic community with an exclusive
home range relative to conspecifics (Rigamonti,
1993; Vasey, 1997a), and because females are dominant to males in all contexts in this genus (e.g.,
social, feeding; Morland, 1991; Kaufman, 1991; Raps
and White, 1995), it is likely that any increases in
consumption of nonfruit items by females toward
the end of the day are due primarily to choice and
not to inter- or intragroup competition. In this regard, it is noteworthy that some Varecia females
possess trichromatic vision (those that are heterozygous at the X-linked M/L opsin gene locus), a trait
known only in one other prosimian, Propithecus verreauxi coquereli (Tan and Li, 1999; Jacobs and Deegan, 2003). These females may have an advantage in
the long-range detection of young leaves that flush
red against a background of mature green foliage
(e.g., Dominy and Lucas, 2001) a factor clearly
linked here to their reproductive success.
In summary, daily rhythms in diet and microhabitat use appear related to thermoregulatory and nutritional requirements, seasonal food availability
and circadian rhythms of plant (and possibly insect)
palatability, predator-avoidance tactics, and in the
case of Varecia, to reproduction. V. rubra descends
into the lower canopy during the hot rainy season
when ambient temperature is highest, and females
feed on high-protein leaves late in the day during
362
N. VASEY
lactation and seek out discrete microhabitats for
nesting and stashing infants early and late in the
day in the hot seasons. E. f. albifrons has highly
heterogeneous daily rhythms of food choice and microhabitat use, although midday resting sites are
well-designed for insulation from harsh elements
and predators. Daily rhythms of food choice in V.
rubra support two general hypotheses explaining
why primates consume more nonfruit items late in
the day, whereas those of E. f. albifrons are too
variable to lend support to any such hypotheses. It
was recently demonstrated that vertical stratification, food-patch sizes, and forest-site use separate
the niches of V. rubra and E. f. albifrons more than
do gross dietary categories (Vasey, 2000, 2002). The
differing daily rhythms in diet and microhabitat use
of these two frugivorous lemurs function as yet another set of niche-partitioning parameters.
ACKNOWLEDGMENTS
I thank my Ph.D. committee for guidance with
various aspects of this work, and particularly Bob
Sussman and Alan Templeton for encouraging me to
undertake an analysis of lemur circadian rhythms. I
also thank Urs Thalmann and Bob Sussman for
comments on an earlier version of this paper. I acknowledge the Tripartite Committee of the Malagasy Government for permission to complete this
research under an accord between the Department
of Paleontology and Biological Anthropology, University of Antananarivo and the Department of Anthropology, Washington University.
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