AJP 305

American Journal of Primatology 41:267–288 (1997)

RESEARCH ARTICLES
Determinants of the Dramatic Seasonal Changes in the
Intake of Energy and Protein by Japanese Monkeys in a
Cool Temperate Forest
NAOFUMI NAKAGAWA*
Department of Liberal Arts, Shion Junior College

Daily intake of gross energy (DGEI) and protein (DGPI) of Japanese mon-
keys in a cool temperature forest were investigated in different four sea-
sons. As a result, dramatic seasonal differences in DGEI and DGPI were
found: DGEI and DGPI in winter were significantly lower than those in
spring and autumn, being only about 17–42% of those in the two sea-
sons. DGEI and DGPI in summer were also lower than those in autumn
and spring, being only about 29–52% of those in the two latter seasons.
Seasonal comparisons of some variables on food qualities revealed that
much lower values of DGEI and DGPI in winter and summer were influ-
enced srongly not so much by the lower calorie and protein content of
food as by the lower speed of dry weight intake. Multiple regression analy-
ses for each food item revealed that the unit weight was a more impor-
tant factor in determining the speed of dry weight intake than was the
speed of unit intake. In addition, the speed of dry weight intake contrib-
uted much more to the speed of calorie and protein intake than did the
content of calorie and protein. Multiple regression analyses, employing
DGEI and DGPI (as dependent variables) and daily mean values of some
variables related to food quality (as independent variables), revealed that
the mean values of speed of calorie and protein intake on food items
eaten in a day could explain 79.0% and 85.9% of the variance in DGEI
and DGPI, respectively. In addition, the mean value of the speed of dry
weight intake of food items eaten in a day can be used to explain 74.3%
and 52.8% of the variance in DGEI and DGPI, respectively. These findings
suggested that not only nutritional content of food but also the speed of dry
weight intake strongly determined the nutritional condition of nonhuman
primates. Am. J. Primatol. 41:267–288, 1997. © 1997 Wiley-Liss, Inc.

Key words: Japanese monkeys; energy intake; protein intake; food

quality; cool temperature forest; multiple regression analysis

*Correspondence to: Naofumi Nakagawa, Dept. of Nursing, Fac. of Nursing, Kobe City College of
Nursing, 3-4 Gakuen-nishimachi, Nishi-ku, Kobe, Hyogo 651-21, Japan.

Received for publication 2 September 1995; revision accepted 5 November 1996

© 1997 Wiley-Liss, Inc.

268 / Nakagawa

INTRODUCTION
Many studies have revealed the seasonal changes of time spent feeding of wild
nonhuman primates recently [e.g., Islam & Feeroz, 1992; Newton, 1992; Kool, 1993;
Dasilva, 1994] and, since the 1970s [e.g., Chivers, 1977; Pollock, 1977]. However, the
calorie and nutrient contents are variable among food items [see reviews by
Waterman, 1984; Garber, 1987]. In addition, time spent feeding cannot be accepted
as an estimate of food intake since feeding rate, or quantity of food ingested per unit
time, may differ considerably among food items, as Hladik [1977] was first to em-
phasize. Several field studies have succeeded in revealing the seasonal changes in
the calorie and/or nutrient intake of wild nonhuman primates, measuring the calo-
rie and nutrient contents and the feeding rate of food items [e.g., Presbytis entellus:
Hladik, 1977; Theropithecus gelada: Iwamoto, 1979; Macaca fuscata: Iwamoto, 1982;
Nakagawa, 1989a; Papio ursinus: Byrne et al., 1993].
On the other hand, calorie and nutrient contents of food items have been
investigated mainly to reveal the determinant factors of food choices in nonhu-
man primates [see reviews by Waterman, 1984; Nakagawa, 1996]. Feeding rate
has recently been investigated to reveal the difference of feeding success among
individuals and groups [e.g., Janson, 1985; van Schaik & van Norodwijk, 1988;
Whiten, 1988] and to test optimal patch use [e.g., Nakagawa, 1990a, b; Grether,
et al., 1992] and optimal food choice [Barton & Whiten, 1994]. However, few
studies have examined systematically the relative importance of time spent feed-
ing, calorie and nutrient contents and feeding rate of food items, which are re-
sponsible for seasonal differences in energy and nutrient intake.
My previous study indicated that the intake of gross energy and protein in
autumn by Japanese monkeys in a cool temperature zone was 2.6 and three
times as large as those in winter, respectively [Nakagawa, 1989a]. Such large
differences of nutritional intake between two seasons appeared to be influenced
not so much by the difference of nutritional content as by that of feeding rate.
Subsequent analysis revealed that interregional (cool temperate vs. warm tem-
perate) differences in the intake of gross energy and protein in autumn and win-
ter were also responsible for those in nutritional content and feeding rate of food
items [Nakagawa, 1989a; Nakagawa et al., 1996].
The first goal of this study was to obtain the data for the other two seasons
(i.e., spring and summer) and to identify differences in daily intake by Japanese
monkeys of gross energy and protein among the four seasons in a cool temperate
region. The second and more important goal was to reveal the relative impor-
tance of some factors responsible for these seasonal differences.

METHODS
Study Area
Kinkazan is a small island of about 10 km2, situated in the northern part of
Japan (38°8´N, 141°4´E). It has a mean annual rainfall of about 1,500 mm and a
mean annual temperature of 11°C. The climate in Japan can usually be divided
clearly into four seasons: a hot summer with considerable rainfall (June to Au-
gust), a cool and dry winter (December to February); and spring (March to May)
and autumn (September to November) with moderate temperatures and rainfall
in both seasons. Although it sometimes snows in winter, Kinkazan Island is sel-
dom covered with snow.
The island is mostly covered with the natural cool temperate forests, which
are dominated by Fagus crenata, Abies firma, and Carpinus tschonoskii, and the
remaining parts are covered by plantations of Pinus thunbergii. Among these
 DGEI and DGPI of Japanese Monkeys / 269

forests there are several patches of grassland, which are dominated by Miscanthus
sinensis, Pleioblastus chino, and Zoysia japonica [Yoshii & Yoshioka, 1949; Kato
& Nishihira, 1972]. They were originally created by wildfires and fallen trees
and developed subsequently as a consequence of the high foraging pressure of
indigenous Sika deer [Yoshii & Yoshioka, 1949; Yoshioka, 1960; Takatsuki, 1989].

Study Animals
The number of Japanese monkeys on the island has increased [Izawa, 1988]
since their daily intake of gross energy and protein was studied during the au-
tumn and winter in 1986–1987 [Nakagawa, 1989a], and there were approximately
280 individuals in six social groups in 1993 [Izawa, 1996]. Reflecting such an
overall increase in population size, the size of the focal social group (A troop) also
increased from 29 individuals in February 1987 to 51 in May 1992 [Takahashi,
unpublished].

Behavior Sampling
All data-sampling procedures were identical to those in the previous study
[Nakagawa, 1989a], as described below.
Focal animals were subject to behavior sampling for entire days during two
periods: 3 days in late summer (18/08/91–20/08/91) and 5 days in late spring (10/
05/92–13/05/92). One fully adult female (Kanako and Sara, respectively) was cho-
sen as the focal animal in each period. The focal animals were of similar body
size and in similar reproductive condition (nonestrous, nonlactating) to the focal
animal (Obi) in the previous study.
During focal sampling a continuous record was made of time associated with
various activities (feeding, foraging, moving, resting, drinking, self-grooming, al-
logrooming, and social activities excluding allogrooming) as well as of intervals
when the animal was out of sight, defined as periods when it was not possible to
determine accurately whether the animal was feeding or performing some other
activity. Food items were also recorded (species and part eaten), as were the
numbers of units of each item consumed by the focal animal in 1 min units es-
tablished randomly during continuous feeding on a particular food item. One unit of
an item was normally one fruit, one leaf, one bud, etc., because the monkeys usually
eat one such discrete unit per bite. However, one unit was strictly defined in the
following three different ways: 1) one fruti, one leaf, one bud, etc., was regarded as
one unit for an item that the monkey always ate as a discrete unit per bite or that
the monkey did not always eat as a fixed number of discrete units per bite; 2) a fixed
number of discrete units was regarded as one unit for an item that the monkey
always ate as a fixed number of discrete units per bite (e.g., seeds in one cluster of
flowers, one cluster of fruits); and 3) a previously fixed length of twig or stem and a
fixed area of bark were, for convenience, regarded as one unit in the case of items for
which the volume per bite could not measured.

Nutritional Analysis
Fourteen of the 26 items eaten by the focal animal in spring and six of the
16 items eaten in summer (18/08/91) were collected in the field immediately af-
ter behavioral sampling at each period, and the fresh weights per unit were de-
termined. These samples were brought back to the laboratory and preserved in the
freezer. Before nutritional analysis, samples were defrosted, dried to constant weight
in an vacuum dryer at a temperature of about 80°C, weighed, and milled.
270 / Nakagawa

Nutritional contents of the samples were analyzed by the method described

by Ichinose and Matsui [1975]. Crude protein was determined by the Kjeldahl
method for total nitrogen, and the value for total nitrogen was multiplied by
6.25. Ether extract (primarily lipid) was quantified by the Soxhlet method. Crude
fiber was obtained from the remnants left after boiling in acid and alkali, and
crude ash was obtained from the ignition loss. A value for nitrogen-free extract
(soluble carbohydrate) was estimated by subtracting the weights of the above
four components from the total sample weight. The calorie content was calcu-
lated by multiplying each weight (grams) of carbohydrate (crude fiber plus soluble
carbohydrate), crude protein, and lipid by 4.15, 5.65, and 9.40 [Maynard et al.,
1979], respectively.

Estimation of Daily Intake of Gross Energy and Protein and Statistical

Analysis for Comparisons Among Seasons
Daily gross energy intake (DGEI) and daily gross protein intake (DGPI) of
the focal animal during each sampling day d was estimated from the following
equations, respectively:

DGEI d(kcal/day) = ∑ UTWTi × SPUTi × CALCON i × FTi,d (1a)

DGPI d(g/day) = ∑ UTWTi × SPUTi × PROCONi × FTi,d (2a)

In these equations UTWTi (unit weight) is the average unit weight on a dry
weight basis of food item i (g/unit), SPUTi (speed of unit intake) is the mean
number of units of item i consumed by the focal animal per minute (units/min),
CALCONi (calorie content) is the calorie content, on a dry weight basis, of food
item i (kcal/g), PROCONi (protein content) is the protein content on a dry weight
basis of food item i (g), and FTi,d (feeding time) is the number of minutes spent
feeding on food item i on sampling day d. Three additional variables were de-
fined as follows: SPDWi (speed of dry weight intake, g/min) = UTWTi × SPUTi;
SPCALi (speed of calorie intake, kcal/min) = SPDWi × CALCONi; SPPROi (speed
of protein intake, g/min) = SPDWi × PROCONi.
Except on 19–20/08/91, the focal animal was followed almost completely
about from 0430 in spring and 0500 in summer, when the focal animal began
to move, to 1900 in spring and 1830 in summer, when she stopped moving.
The time out of sight was only about 13 min for 18/08/91 during the above
active time. In addition, food items for which nutritional data were available,
including estimated values (shown as e in Table Ia and Ib), accounted for
98.34% and 95.02% of the total observed feeding time in spring and in sum-
mer, respectively (see Tables Ia, Ib). Therefore, DGEI and DGPI were assumed
to be accurate except in the case of 19–20/08/91. These values for autumn and
winter also could be estimated precisely for similar reasons [for details see
Nakagawa, 1989a]. However, the time out of sight amounted to 90 min on 19/
08/91, and the focal animal ceased all activity after 1530 because of heavy
rains on 20/08/91. The data from these 2 days were also analyzed but sepa-
rately from the main results.
One-way ANOVA was used to examine the daily differences in DGEI and
DGPI among three seasons with balanced data (5 days each). Summer, with
only 1 full day’s data, was excluded. Scheffe’s test was used as a multiple
comparison test. The statistical procedures were performed using the HALBAU
statistical package.
TABLE Ia. Details of Each Food Item Eaten in Spring
Speed of Speed of Speed of Speed of
unit dry Calorie Crude calorie protein
Unitb intake weight content protein intake intake
Part weight (unit/ intake (g/ (kcal/ content (kcal/ (g dw/ Feeding time (min) DUR DW
Species name eatena (g dw) min) min) dw) (%) min) min) 10 May 11 May 12 May 13 May 15 May (%)c (%)d

Prunus x yedoenis YFr 0.0200f 41.38 0.8277 4.342 20.10 3.594 0.1664 70.33 48.63 100.17 0.00 31.40 12.80 16.67
Berberis thunbergii Fl 0.0048f 49.68 0.2385 4.642i 17.93 i 1.107i 0.0428i 147.52 230.52 52.77 161.35 51.25 27.40 10.29
Ylf 0.0070f 102.23 0.7156 4.464i 13.04 i 3.194i 0.0933i 65.87 28.17 54.50 67.55 51.68 11.40 12.84
Zelkova serrata LfBu 0.0249f 42.06 1.0474 4.410 28.75 4.619 0.3011 0.00 0.00 46.17 32.15 100.20 7.60 12.53
Ylf 0.0108f 63.83 0.6894 4.384 29.62 3.022 0.2042 183.15 47.43 95.78 29.07 10.50 15.58 16.91
Mlf 0.0238f 56.52 1.3452 4.358 24.57 5.862 0.3305 0.00 0.00 39.77 7.88 0.00 0.34 0.71
Zanthoxylum Fl 0.0089g 40.18 0.3576 4.484 29.41 1.603 0.1052 23.95 13.88 0.00 2.73 46.58 4.51 2.54
pipertium Ylf 0.00 0.00 18.78 0.00 0.67 0.03
Viburnum dilatatum Ylf 0.0132f 48.35 0.6382 4.608i 21.34 i 2.941i 0.1362i 49.95 0.00 0.00 48.97 19.45 5.18 5.20
Acer japonicum FlBu 0.0164f 49.35 0.8093 4.658 33.19 3.770 0.2686 0.00 98.03 3.22 0.00 0.00 6.89 8.78
Ylf 0.0482f 44.29 2.1346 4.377 16.88 9.343 0.3603 0.00 6.62 63.83 3.77 49.67 2.68 9.01
Symplocos chinensis Ylf 0.0120f 45.38 0.5445 4.145 22.15 2.257 0.1206 0.00 0.00 2.90 0.00 0.00 0.37 0.32
Rosa multiflora Sh 0.1526h 6.00 0.9156 4.188 15.83 3.834 0.1449 0.00 0.00 8.63 0.93 17.27 0.78 1.13
Wisteria floribunda FlBu 0.00 0.00 0.22 0.00 0.00 0.17
Zoysia japonica Ylf 0.0111e,g 27.90 0.3097e 3.731e 14.79 e 1.155e 0.0458e 0.00 0.00 4.02 10.18 7.53 0.75 0.37
Celastrus orbiculatus Ylf 0.00 0.00 0.00 16.23 0.00 0.69
Rubus microphyllus Fl 0.0124f 34.00 0.4216 4.344 11.11 1.830 0.0468 0.42 0.00 0.00 0.00 21.57 0.94 0.62
Lonicera japonica Ylf 0.00 0.00 0.00 0.00 4.38 0.19
Pourthiaea villosa Ylf 0.0427f 27.70 1.1828 4.338 21.97 5.131 0.2599 0.00 0.00 0.00 0.00 26.33 1.12 2.09
FlBu 0.00 0.00 0.00 0.00 1.68 0.07
Ixeris stlonifera All 0.00 0.00 0.00 1.27 0.00 0.05
Fraxinus lanuginosa Ylf 0.00 0.00 0.00 0.00 4.30 0.18
Fl 0.00 0.00 0.00 0.00 2.27 0.10
Aralia elata Gum 0.00 0.00 0.00 0.00 1.22 0.05
Mushrooms All 0.00 0.00 0.08 0.00 1.28 0.06
Soil 0.02 1.03 0.2 0.00 0.18 0.07
a
All, parts, Fl, flower; FlBu, flower bud; LfBu, leaf bud; Mlf, mature leaf; Sh, shoot; Ylf, young leaf.
b
One unit of an item was defined as described in Methods.
c
Percentage of time spent feeding on each food item relative to total feeding time for 5 sampling days.
d
Percentage of dry weight intake for each food item relative to the total dry weight intake for 5 sampling days.
e
Estimated values based on data observed in winter [Nakayawa, 1989a] were applied.
f
One fruit, leaf, bud, etc., was regarded as one unit for an item that the monkey always ate as a discrete unit per bite or that the monkey did not always eat as a fixed
DGEI and DGPI of Japanese Monkeys / 271

number of discrete units per bite.

g
For the flower of Zanthoxylum piperium, one unit was one cluster of flowers. For leaves of Zoysia japonica, one unit was three leaves.
h
For shoots of Rosa multiflora, one unit was a 12 cm long piece of shoot.
i
Saitoh [unpublished].
TABLE Ib. Details of Each Food Item Eaten in Summer
Speed of Speed of Speed of Speed of
unit dry Calorie Crude calorie protein
Unitb intake weight content protein intake intake
Part weight (unit/ intake (g/ (kcal/g content (kcal/ (g dw/ Feeding time (min) DUR DW
Species name eatena (g dw) min) min) dw) (%) min) min) 18 August 19 August 20 August (%)c (%)d
272 / Nakagawa

Paederia scandens Mlf 0.0040f 28.80 0.1152 4.171 17.48 0.480 0.0201 33.28 35.70 22.42 9.57 2.68
Celastrus orgbiculatus Sh 2.17 7.78 16.17 0.62
Zanthoxylum piperitus Mlf 0.0225f 16.67 0.3751 4.296 16.49 1.612 0.0619 40.87 35.07 71.02 11.75 10.72
Fr 0.0301 g 20.20 0.6081 4.424 13.95 2.690 0.0848 1.87 9.72 10.62 0.54 0.80
Stephanandra incisa Se 0.0309g 24.00 0.7416 5.514 9.19 4.090 0.0682 86.25 31.43 16.05 24.95 44.99
Mlf 0.00 4.75 0.00 0.00 0.00
Symplocos chinensis Mlf 0.0470f 10.78 0.5067 4.178 14.06 2.117 0.0712 68.63 15.87 29.12 19.74 24.32
Amphicarpaea Mlf 0.0072f 9.99 0.0719 4.261 19.55 0.306 0.0141 61.60 64.30 14.25 17.72 3.10
edgeworthii
Berberis thunbergii Mlf 0.0070e,f 91.00 0.6370e 4.463e 13.04 e 2.843e 0.0831e 20.30 21.10 25.55 5.84 9.04
Rubus microphyllus Mlf 0.75 0.47 0.00 0.22
Torreya nucifera Se 8.08 0.00 0.00 2.32
Sdl 0.6 0.00 0.97 0.17
Ixeris stlonifera All 0.0025e,f 45.88 0.1147 e 4.240e 18.37 e 0.486e 0.0211 e 12.52 9.78 5.03 3.60 1.01
Ixeris debilis All 0.0025e,f 45.88 0.1147 e 4.240e 18.37 e 0.486e 0.0211 e 4.55 0.00 0.00 1.31 0.36
Viburnum dilatatum YFr 0.0102e,f 20.58 0.2099e 4.450e 5.94e 0.934e 0.0125e 0.00 45.75 5.83 0.00 0.00
Smilax china Fr 0.00 1.43 2.70 0.00
Mushrooms All 5.33 6.85 6.70 1.53
Unidentified insects All 0.40 0.00 0.73 0.12
Soil 0.00 0.22 0.00
Crickets All 0.1780e,f 5.370e 65.23 e 24.00 h 9.00h 13.00 h 2.99
a
All, all part; Fr, fruit; Mlf, mature leaf; Sdl, seedling; Se, seed; Sh, shoot.
b
One unit of an item was defined as described in Methods.
c
Percentage of time spent feeding on each food item relative to the total feeding time on 18 August 1991.
d
Percentage of dry weight intake for each food item relative to the total dry weight intake on 18 August 1991.
e
Estimated values based on data from Spring (Table Ia) or from winter [Nakayawa, 1989a] were applied. The values for Cryllacris japomica [Iwamoto, 1982] were applied for
crickets.
f
One fuit, leaf, bud, etc., was regarded as one unit for an item that the monkey always ate as a discrete unit per bite or that the monkey did not always eat as a fixed number
of discrete units per bite.
g
For fruits of Zanthoxylum piperitus, one unit was one cluster of fruits. For seeds of Stephanandra incisa, one unit was seeds in one cluster of flowers.
h
The number of crickets eaten in a day.
 DGEI and DGPI of Japanese Monkeys / 273

Analysis of Factors Responsible for Seasonal Differences in

DGEI and DGPI
Three different approaches were used to elucidate the factors responsible for
seasonal differences in DGEI and DGPI.
The first approach involved comparisons among seasons of the daily mean
values of the following seven variables for food items eaten on each sampling day
d: UTWTd, SPUTd, CALCONd, PROCONd, SPDWd, SPCAL d, SPPROd. The com-
parisons among three seasons were also performed by the one-way ANOVA and
Scheffe’s multiple comparison test with the HALBAU package.
The second approach was to examine the factors that strongly influenced
DGEI and DGPI using multiple regression analysis with the Stat123/Win statis-
tical package.
From equations 1a and 2a, DGEI and DGPI for sampling day d were ex-
pected to approximate the following equations, respectively:

DGEId ~
– UTWT d × SPUTd × CALCONd × FTd × NO d, (1b)
DGEId ~ – SPDWd × CALCON d × FTd × NOd, (1c)
or DGEId ~
– SPCAL d × FTd × NOd. (1d)

DGPId ~
– UTWTd × SPUTd × PROCON d × FT d × NOd, (2b)
DGPId ~ – SPDWd × PROCON d × FTd × NOd, (2c)
or DGPId ~
– SPPROd × FTd × NOd. (2d)

In all these equations UTWT d, SPUTd, SPDWd, CALCON d, PROCON d,

SPCALd, and SPPROd are the daily mean values of UTWTi, SPUTi, SPDWi,
CALCONi, PROCONi, SPCALi, and SPPROi for each food item eaten on each
sampling day d, respectively, FTd is the daily mean number of minutes spent
feeding on each food item that was eaten on each sampling day d, and NO d is the
number of food items on each sampling day d. Food items that were eaten but
not included in calculations of DGEId and DGPId were excluded from the calcula-
tion of these daily mean values and NOd.
The linear relationships between DGEId, DGPI d (dependent variables), and
several predictor independent variables could be described by the multiple re-
gressions when the above equations were log-transformed as follows:

logDGEId ~
– logUTWTd + logSPUTd + logCALCONd + logFTd + logNO d, (1b´)
logDGEId ~ – logSPDWd + logCALCONd + logFTd + logNO d, (1c´)
or logDGEId ~– logSPCALd + logFTd + logNOd. (1d´)

logDGPId ~
– logUTWTd + logSPUTd + logPROCONd + logFTd + logNO d, (2b´)
logDGPId ~ – logSPDWd + logPROCONd + logFTd + logNO d, (2c´)
or logDGPId ~
– logSPPROd + logFTd + logNOd. (2d´)

The equations for multiple regressions were obtained from these log-trans-
formed variables, but the extent of the contribution of the variables to each re-
gression was different. Therefore, stepwise multiple regression analysis (forward
selection method) was carried out to assess the relative importance of these vari-
ables and to allow us to focus on a smaller number of important variables that
might predict DGEI and DGPI. In this analysis, the predictor that showed the
274 / Nakagawa

highest correlation with dependent variables (DGEI or DGPI) was added first in
step 1. Thereafter, each predictor with an elevated correlation was added, one by
one, at each step. No further steps were included when the added predictor vari-
able had an F ratio of less than 4.0.
The third approach was to examine the extent of contributions of UTWTi and
SPUTi to SPDWi, of SPDWi and CALCONi to SPCALi and PROCONi to SPPROi,
using stepwise multiple regression analysis with the Stat123/Win statistical pack-
age. The relationships among these variables are shown by the following equations:

SPDW i = UTWTi × SPUT i (3)

SPCALi = SPDWi × CALCONi (4)
SPPRO i = SPDWi × PROCONi. (5)

The linear relationships between dependent variables and independent vari-

ables could be described by multiple regressions when the above equations were
log-transformed as follows:

logSPDWi = logUTWTi + log SPUTi (3´)

logSPCALi = logSPDWi + logCALCONi (4´)
logSPPROi = logSPDWi + logPROCONi (5´)

Stepwise multiple regression analysis (forward selection method) was car-

ried out to assess the relative importance of each of two independent variables
on each dependent variable in each equation. In this analysis, the independent
variable that showed higher correlation with the dependent variable was added
first in step 1. Food items for which the data included estimated values (shown
as e in Tables Ia, Ib and in Appendix 1a, 1b) for the above variables were ex-
cluded from the analysis that involved all the above equations. Moreover, food
items for which the unit was defined as a previously fixed length of twig or stem
and a fixed area of bark were also excluded from the analysis with equation 3´.
Therefore, 42 and 46 food items were used for analysis with equation 3´ and with
equation 4´ and 5´, respectively.

RESULTS
Food Composition in Spring and Summer
The food composition and quality of each of the food items in spring and
summer are shown in Tables Ia and Ib, respectively.
The focal animal was observed eating 26 food items in spring. The flowers of
Berberis thunbergii accounted for the highest consumption (27.40%) and the young
leaves of Zelkova serrata for the second highest (15.58%) in terms of the percent-
age of total time spent feeding (DUR%). In terms of the percentage of total dry
weight (DW%), the young leaves of Zelkova serrata and the young fruit of Prunus
x yedoensis accounted for the highest consumption (about 17% each). Young leaves
and leaf buds accounted for 44.99% of DIR and for 58.90% of DW. The daily
mean value for total time spent feeding was about 7 h 50 min (54.6% of total
active time), and that for total dry weight intake was 298 g.
The focal animal was observed eating 16 food items on 18/08/91 (summer).
The seeds of Stephanandra incisa were associated with the highest consumption
in terms of both DUR% (24.95%) and DW% (44.99%). Leaves of herbaceous plants
(Amphicarpaea edgeworthii, Paederia scandens, Ixeris spp.) accounted for 32.2%
of DUR and 7.15% of DW. Total time spent feeding was about 5 h 48 min (43.4%
 DGEI and DGPI of Japanese Monkeys / 275

of total active time), excluding time spent foraging on mushrooms and crickets
(54 min), and total dry weight intake was only 143 g.

Seasonal Differences in DGEI and DGPI

Figure 1 shows seasonal differences in daily gross energy intake (DGEI), in
daily gross protein intake (DGPI), and in the variables related to DGEI and DGPI.
DGEI and DGPI in each season are shown in Figure 1a, b, respectively. The
mean values (± SD) of DGEI and DGPI in spring were 1,327.23 (± 259.23) kcal
and 67.97 (± 14.56) g, respectively. By contrast, DGEI and DGPI on 18/08 (sum-
mer) were only 694.73 kcal and 19.86 g, respectively.
The DGEIs in spring and autumn were about 2.5 times that in winter, and
these differences were statistically significant (spring vs. winter, F(2,12) = 14.68,
P = 0.0006; autumn vs. winter, F(2,12) = 19.66, P = 0.0002; Scheffe’s test after
ANOVA: F(2,12) = 42.95, P < 0.0001). There was no significant difference in DGEIs
between spring and autumn (F(2,12) = 0.36; P = 0.703).
By contrast, large and significant differences in DGPIs among these three
seasons were found (spring vs. winter, F(2,12) = 42.64, P < 0.0001; autumn vs
winter, F(2,12) = 7.73, P = 0.0070; spring vs. autumn, F(2,12) = 14.06, P = 0.0007;
Scheffe’s test after ANOVA: F(2,12) = 42.95, P < 0.0001).
Summer, with only 1 full day of data, was excluded from the above statisti-
cal tests. Given that DGEI and DGPI on 19–20/08 were also small (397.73 kcal
and 378.38 kcal for DGEI, 11.46 g and 12.92 g for DGPI, on respective days),
those on 18/08 do not seem to be extremely low for summer. The DGEI in sum-
mer appears to be a similar low value to that in winter and to be much lower
than that in spring and autumn, while the DGPI in summer appears to be inter-
mediate between autumn and winter.

Factors Underlying Seasonal Differences in DGEI and DGPI

First approach. Because DGEI and DGPI were estimated from the fol-
lowing variables related to food item i, namely, UTWTi, SPUTi, SPDWi, CALCONi,
PROCONi, SPPROi, FT i (see equations 1 a and 2a in Methods), the daily mean
values for these variables for food items eaten on each sampling day d (UTWTd,
SPUTd, SPDWd, CALCONd, PROCON d, SPCALd, SPPROd, FTd) and the number
of food items eaten on each sampling day d (NOd) were expected to contribute
strongly to the seasonal differences in DGEI and DGPI (see equations 1b–d and
2b–d in Methods). From a comparison of these values among seasons, as shown
in Figure 1c–k, the factors underlying the seasonal differences in DGEI and DGPI
were examined in turn. Neither FTd nor NOd differed significantly among the
three seasons (ANOVA, F(2,12) = 1.19, P = 0.3382 for FTd, F(2,12) = 1.90, P =
0.1914 for NO d) (Fig. 1d, e). Thus, they did not explain seasonal differences in
DGEI and DGPI.
Values of SPCALd in spring and autumn were significantly higher than that
in winter (spring vs. winter, F(2,12) = 5.94, P = 0.0161; autumn vs. winter, F(2,12)
= 10.25, P = 0.0025 spring vs. autumn, F(2,12) 0.59, P = 0.5720; Scheffe’s test
after ANOVA: F(2,12) = 11.18, P = 0.0018), but there was no significant differ-
ence between spring and autumn in SPCALd (Fig. 1c). Both SPDWd and CALCONd,
which are determinants of SPCALd, in spring and autumn, were also signifi-
cantly higher than those in winter (for SPDWd, spring vs. winter, F(2,12) = 5.17,
P = 0.0241; autumn vs. winter, F(2,12) = 8.19, P = 0.0057; Scheffe’s test after
ANOVA: F(2,12) = 9.14, P = 0.0039; for CALCONd, spring vs. winter, F(2,12) =
276 / Nakagawa

Fig. 1. Seasonal differences in daily intake of gross energy (a) and protein (b) and in daily mean values for
the variables related to food items eaten on each sampling day (c–k). The variable on y axis of the graph
situated in root of an arrow is potentially determinant factors for that situated in point of an arrow. *P <
0.05; **P < 0.01; ***P < 0.001. Summer was excluded from ANOVA and application of Scheffe’s test because
only data from 1 full day were available.
 DGEI and DGPI of Japanese Monkeys / 277

17.15, P = 0.0003; autumn vs winter, F(2,12) = 31.92, P < 0.0001; Scheffe’s test
after ANOVA: F(2,12) = 34.23, P < 0.0001). By contrast, there was no significant
difference between spring and autumn in either SPDW d or CALCONd (F(2,12) =
0.35, P = 0.7139 for SPDWd; F(2,12) = 2.27, P = 0.1455 for CALCONd) (Fig. 1g,
h). In addition, UTWTd and SPUTd were related to SPDWd. UTWTd in autumn
was significantly higher than that in spring and in winter (autumn vs. spring,
F(2,12) = 4.40, P = 0.0369; autumn vs. winter, F(2,12) = 4.12, P = 0.0436; Scheffe’s
test after ANOVA: F = 5.68, P = 0.0184). However, SPUT d in spring was signifi-
cantly higher than in autumn or in winter (spring vs. autumn, F(2,12) = 62.77, P
< 0.0001; spring vs. winter, F = 49.60, P < 0.0001; Scheffe’s test after ANOVA:
F(2,12) = 75.43, P < 0.0001) (Fig. 1j, k). The significantly higher values for UTWT d
in autumn and for SPUTd in spring contributed to the higher values for SPDWd
than in winter. Higher values for CALCONd, as well as the higher values for
SPDWd, contributed to significantly higher values of SPCALd in spring and
autumn than in winter, as reflected by higher DGEIs in these seasons than
that in winter.
Although summer was excluded from the above statistical tests, the values
for variables in summer, apart from CALCONd, were similar to those in winter.
CALCONd in summer appeared to be similar to that in spring and autumn. How-
ever, the lower value of SPDWd in summer, resembling that in winter, should
contribute strongly to SPCALd and reflect the lower DGEI in summer.
SPPRO d in spring was significantly higher than that in autumn and in win-
ter (spring vs. autumn, F(2,12) = 39.25, P < 0.0001; spring vs. winter, F(2,12) =
73.49, P < 0.0001; Scheffe’s test after ANOVA: F(2,12) = 78.71, P < 0.0001). SPPROd
in autumn was also significantly higher than that in winter (F(2,12) = 5.33, P =
0.0221) (Fig. 1f). PROCONd, which was one of the determinants of SPPROd, in
spring was significantly higher than that in autumn and in winter (spring vs.
autumn, F(2,12) = 114.14, P < 0.0001; spring vs. winter, F(2,12) = 137.08, P <
0.0001; Scheffe’s test after ANOVA: F(2,12) = 168.18, P < 0.0001) (Fig. 1i). The
values of SPDWd, which were additional determinants of values of SPPROd, in
spring and autumn, were significantly higher than that in winter (Fig. 1h) as a
consequence of higher SPUTd and UTWTd, respectively (Fig. 1j, k). Then, in spring,
the highest value for PROCONd among the three seasons and the significantly
higher value for SPDW d than that in winter contributed together to the highest
value of SPPROd and, ultimately, of DGPI among the three seasons. In autumn,
the significantly higher value of SPDWd than that in winter, in the absence of a
significant difference in PROCONd, resulted in the second highest value for
SPPRO d and ultimately in the second highest DGPI among the three seasons.
In summer, which was excluded from the above statistical tests, PROCON d
was somewhat higher than that in autumn and winter. Since SPDW d was much
lower than that in autumn, SPPROd and ultimately DGPI appeared to be inter-
mediate between autumn and winter.
Second approach. The results of multiple regression analysis, employing
all the variables in equations 1b´–d´ and 2b´–d´, are shown in equations 1b´´–d´´
and 2b´´–d´´, respectively, in Table II. All the regressions were highly significant
(P < 0.001) with 87.2–93.0% and 89.0–91.1% of the variances in DGEI and DGPI,
respectively.
The results of stepwise multiple regression analysis are summarized in Table
III. Among predictor variables shown in equation 1b´´, CALCONd was the most
important and could explain 61.7% of the variance in DGEI (adjusted R2 = 0.590;
P < 0.001). When UTWTd and SPUTd were added into the regresion in that or-
der, the adjusted R2 was increased to 0.683 and then to 0.818, respectively (P <
TABLE II. Results of Multiple Regression Analysis, Employing All the Variables in Equations 1b´´–d´´, and 2b´´–d´´
Regression equations R2 Adjusted R2

1b´´ logDGEI d = 0.28 log UTWTd *** + 0.54 logSPUTd* + 5.62 logCALCON d *** + 1.10 log FTd ** + 1.60 logNOd * – 4.36** 0.930*** 0.896

1c´´ logDGEI d = 0.65 log SPDWd*** + 4.39 logCALCONd ** + 0.91 logFT d* + 1.17 logNO d* – 2.32 0.914*** 0.883

1d´´ logDGEI d = 0.84 logSPCALd *** + 0.95 logFTd* + 0.97 logNO d + 0.13 0.872*** 0.841

2b´´ logDGPId = 0.34 logUTWTd ** + 0.14 logSPUTd + 1.79 log PROCONd * + 1.47 log FTd + 1.40logNO d – 0.46 0.890*** 0.835

2c´´ logDGPId = 0.86 log SPDWd *** + 1.29 logPROCONd *** + 1.10 logFTd + 0.83 logNO d + 0.14 0.911*** 0.877

2d´´ logDGPId = 1.01 logSPPROd *** + 0.69 log FTd + 0.15 logNOd + 1.34 0.908*** 0.885

*P < 0.05.
**P < 0.01.
***P < 0.001.
TABLE III. Stepwise Multiple Regression Analysis of the Contribution of Certain Variables to Daily Gross Energy Intake (DGEI) and
Daily Gross Protein Intake (DGPI)
Independent
Independent variable
variable added Partial Cumulative excluded at
Step at each step F Regression equation obtained at each step R2 adjusted R2 last step Patial F

logDGEI d dependent variable

For equation 1b´´
1 CALCONd 22.59 8.71 logCALCONd – 2.57 0.617* 0.59
2 UTWTd 5.12 7.32 logCALCONd + 0.15 log UTWTd – 1.45 0.725* 0.683
3 SPUTd 10.57 5.48 log CALCONd + 0.27 log UTWT d + 0.72 logSPUT d – 1.19 0.854* 0.818 FTd 0.9
For equation 1c´´ NOd 0.04
1 SPDW d 40.49 0.93 logSPDWd + 3.20 0.743* 0.725
2 CALCONd 9.53 0.66 logSPDWd + 4.60 log CALCONd + 0.20 0.852* 0.829 FTd 1.9
NOd 0.04
For equation 1d´´
1 SPCAL d 52.7 0.89 logSPCALd + 2.63 0.790* 0.775
2 FTd 4.35 0.83 logSPCALd + 0.39 logFTd + 2.00 0.843* 0.819 NOd 2.79
log DGPId as dependent variable
For equation 2b´´
1 PROCONd 20.68 1.78 logPROCONd + 3.00 0.600* 0.571
2 UTWTd 13.9 2.02 logPROCONd + 0.33 log UTWTd + 3.75 0.806* 0.777
3 FTd 5.52 1.96 logPROCONd + 0.30 log UTWTd + 0.67 log FTd + 0.25 0.867* 0.834 NOd 2.2
SPUTd 0.26
For equation 2c´´
1 PROCONd 20.96 1.80 logPROCONd + 3.00 0.600* 0.571
2 SPDW d 1.38 logPROCONd + 0.92 log SPDWd + 2.86 0.851* 0.828
3 FTd 1.35 logPROCONd + 0.84 log SPDWd + 0.61 log FTd + 1.79 0.902* 0.878 NOd 0.95
For equation 2d´´
1 SPPROd 85.05 1.07 logSPPRO d + 2.71 0.859* 0.849 6.88
2 FTd 6.88 1.02 logSPPRO d + 0.601log FTd + 1.64 0.908* 0.893 NOd 0.03

*P < 0.001.
280 / Nakagawa

0.001). Among predictors shown in equation 1c´´, SPDWd was the most impor-
tant and could explain 74.3% of the variance in DGEI (P < 0.001). When the
second most important predictor, CALCONd, was entered, the adjusted value of
R2 increased to 0.829 (P < 0.001). Among predictor variables shown in equation
1d´´, SPCALd was the most important and could explain 79.0% of the variance in
DGEI (adjusted R2 = 0.775; P < 0.001). When FTd was entered, the adjusted
value of R2 increased to 0.819 (P < 0.001). These analyses revealed that 1) SPDWd
contributed to DGEI much more than did CALCONd, 2) between UTWTd and
SPUTd, which were determinants of SPDWd, the contribution of the former to
DGEI seemed to be larger than that of the latter, and 3) the contributions of FTd
and NOd to DGEI were negligible.
With respect to predictors of DGPI in equation 2b´´, PROCONd was the most
important predictor and could explain 60.0% of the variance in DGPI (P < 0.001).
When the second (UTWTd) and third (FTd) most important predictors were added,
the adjusted values of R2 increased to 0.777 and then to 0.834, respectively (P <
0.001). Among predictor variables shown in equation 2c´´, PROCONd, SPDWd,
and FTd were the most important variables, in that order, and the cumulative
adjusted values of R2 were 0.571, 0.828, and 0.878, respectively (P < 0.001). Addi-
tionally, only SPDWd could explained 52.8% of the variance in DGPI (P < 0.001).
Among predictor variables shown in equation 2d´´, SPPROd and FTd were impor-
tant variables, in that order. In contrast to the results of the analysis of DGEI,
FTd contributed significantly to DGPI, whereas the contribution of NOd was still
negligible. However, the contribution of FTd was the least important in any analy-
sis of contributors to DGPI, and all the regressions, even if FTd was excluded,
were still highly significant (P < 0.001) accounting for 80.6–85.9% of the vari-
ance in DGPI. By contrast to the result that CALCONd contributed to DGEI less
than did SPDWd, PROCONd contributed to DGPI more than did SPDWd.
Third approach. As a result of stepwise regression analysis, UTWTi en-
tered equation 3´ first (regression equation: logSPDWi = 0.607logUTWTi + 0.747)
and explained 57.1% of the variance in SPDWi (P < 0.001). SPDWi entered equa-
tion 4´ first (regression equation: logSPCALi = 0.997logSPDWi + 0.634) and ex-
plained 98.6% of the variance in SPCALi (P < 0.001). On the other hand, SPDWi
entered equation 5´ first (regression equation: logSPPROi = 0.854logSPDWi
– 0.947) and explained 60.5% of the variance in SPPROi (P < 0.001).

DISCUSSION
Seasonal Differences in DGEI and DGPI
The dramatic seasonal differences in DGEI and DGPI were found: DGEI and
DGPI in winter were significantly lower than those in spring and autumn, being
only about 17–42% of those in the two latter seasons. DGEI and DGPI in sum-
mer were also lower (but no statistical analyses were undertaken) than those in
autumn and spring, being only about 29–52% of those in the two latter seasons.
The DGEI in summer appears to be a similar low value to that in winter, while
the DGPI in summer appears to be intermediate between autumn and winter.
DGPI in spring was significantly higher not only than that in winter but also
than that in autumn, while DGEI in the spring was similar to that in autumn.
Nakagawa [1989a] calcualted the energy and protein balances in winter at
–231 kcal and –19 g, respectively, while those in autumn were +221 kcal and +5
g, respectively. He used the following values in these calculations: 1) digestibility
at 55% [Iwamoto, 1978], 2) urinary energy at 4% of gross energy [Nagy & Milton,
 DGEI and DGPI of Japanese Monkeys / 281

1979], 3) protein intake requirement at 2.54 g/day/kg body weight [Robbins &
Gavan, 1966], and 4) the energy requirement estimated with the methods of
Coelho [1974] and Coelho et al. [1976]. However, all these values seemed to be
lacking in reliability: digestibility differs among food items and negatively corre-
lates with the fiber content [Iwamoto, 1988]; the work of Robbins & Gavan [1966]
was in a very short study [Oftedal, 1992]; and the energy requirement estimated
with the methods of Coelho and his colleagues seemed to be underestimated
[Iwamoto, 1988]. Digestion tests, using many foods with various nutrient con-
tent, should be conducted, and regression coefficients between digestibility and
fiber content should be calculated to precisely estimate the digestible energy, as
Iwamoto [1988] attempted. On the other hand, the precise measurement of the
energy requirement, using the doubly labeled water method [Nagy & Milton,
1979], also should be conducted. At present, few data based on the methods as
described above are still available. Therefore, energy balances and protein bal-
ances were not examined in this study.
However, the seasonal differences in DGEI and DGPI found in this study are
supposed to roughly reflect the seasonal differences of actual nutritional condi-
tions. Agetsuma and Nakagawa [in preparation] showed seasonal variation of
time spent in each activity and time spent feeding on each food category of Japa-
nese monkeys in Kinkazan based on 20 half-month data sets. Total time spent
feeding was longest in late winter/early spring and late summer, the shortest in
mid-summer. Total time spent moving showed the almost reverse trend. Herbs,
barks, and buds, with a lower speed of energy intake, were the main food catego-
ries in late winter/early spring, while fruits, seeds, and/or leaves, with a higher
speed of energy intake, were the main categories in other seasons. As the opti-
mal foraging model predicted [Norberg, 1977], Japanese monkeys will save the
foraging cost (e.g., moving time) even if energy gain is restricted under poor
nutritional conditions, although they will increase time spent feeding, to some
extent, even on foods with a low speed of energy intake, to get enough energy. As
the nutritional conditions improve, they will increase the foraging cost to get
more energy. Given that time spent feeding and moving reflected the actual
nurtitional conditions as described above, seasonal changes in DGEI and DGPI
found in this study are supposed to roughly reflect those of actual nutritional
conditions because seasonal changes in DGEI and DGPI corresponded to those
in time spent feeding and moving, although these values should not be regarded
as representatives of each season but those of more limited periods (i.e., late
spring, late summer, late autumn, and late winter).
Although no quantified data on seasonal changes in energy and nutrient in-
take by Japanese monkeys in the other cool temperate regions of Japan are avail-
able, the main characteristics of seasonal changes in their food habits seem to be
qualitatively similar to those in Kinkazan Island. Young leaves and flowers are
eaten in spring, leaves and stems of grasses and herbs are eaten in summer,
fruits and seeds are eaten in autumn, and buds and barks are eaten in winter
[Suzuki, 1965; Wada & Ichiki, 1980; Nakagawa, 1989a, b; Agetsuma & Nakagawa,
in preparation]. In one of the cited studies, Wada and Ichiki [1980] concluded
that “food quality in autumn is the best, followed by that in spring, summer, and
winter, in that order’’ on the snowy Shiga Heights, although their conclusion was
based on limited quantified data about food quality. The results of the present
study tend to support their speculative conclusions with respect to calories.
Given the above-mentioned similarities in food habits and food quality be-
tween Kinkazan and Shiga Heights, the results obtained in the present study
may be applicable for the most part to the monkeys in other cool temperate
282 / Nakagawa

regions of Japan, although, at least in winter, the food environment on

Kinkazan Island is considered to be better than that in snowy regions [for
details see Nakagawa, 1989a].

Factors Underlying the Seasonal Differences in DGEI and DGPI

From comparisons of calorie and protein contents, speed of dry weight in-
take, and unit weights of food items in autumn and winter, Nakagawa [1989a]
concluded that lower values of DGEI and DGPI in winter appeared to be strongly
influenced not only by the lower calorie and protein content of food but also by a
lower speed of dry weight intake, which was derived partly from the smaller unit
weights of the food items eaten in winter, as compared to those in autumn. Us-
ing a different and more elaborate analytical method, as well as additional data
for spring and summer, the author obtained similar results in the present study.
Moreover, new findings were also obtained. Although the higher speed of dry
weight intake in spring was derived not from greater unit weight but from higher
speed of unit intake, multiple regression analysis for each item revealed that the
unit weight was a more important factor in determining the speed of dry weight
intake than the speed of unit intake. In addition, the speed of dry weight intake
contributed much more to the speed of calorie intake than did the calorie con-
tent. Wrangham et al. [1993] have reported similar results: the speed of wet
weight intake and the speed of calorie intake from the digestible carbohydrates
of six species of fruits eaten by frugivorous animals (e.g., Pan troglodytes) were
significantly and positively correlated with the wet weight of fruit. Data on 23
species of fruits eaten by Macaca fascicularis from van Schaik & van Norodwijk
[1987] were analyzed with the same stepwise regression analysis as that of this
study, and it also indicated log-formed unit weight entered the equation first and
explained 41.9% of the variance in log-formed speed of dry weight intake (P <
0.001). With respect to the speed of protein intake, the speed of dry weight in-
take was a more important factor in determining the speed of protein intake
than was protein content. Data on 38 food items of Papio anubis from Barton
and Whiten [1994] also indicated log-formed speed of dry weight intake entered
the equation first and explained 71.8% of the variance in log-formed speed of
protein intake (P < 0.001). These findings that the speed of dry weight intake,
and especially its determinant factor, namely, unit weight, was a conspicuous
predictor of the speed of calorie and protein intake may generalize to many spe-
cies of nonhuman primates.
The importance of the speed of calorie and protein intake is supported by
the following results from the present study. The mean values for speed of
intake of calorie and protein from food items eaten in a day predicted 79.0%
and 85.9% of the variance in the daily intake of gross energy and protein,
respectively. This result means that the daily intake of gross energy and pro-
tein could be estimated approximately only from the data related to the qual-
ity of food items (unit weight, speed of unit intake, content of calories and
protein) even if the time spent feeding on each food item and the number of
items eaten in a day were unknown. Moreover, even if no nutritional data on
food items (contents of calories and protein) are available, the mean value of
the speed of dry weight intake of food items eaten in a day can be used to
predict 74.3% and 52.8% of the variance in the daily intake of gross energy
and protein, respectively.
Some regressions obtained from the present study seem not to be appli-
cable to different-sized primates since chimpanzees, for example, can harvest
 DGEI and DGPI of Japanese Monkeys / 283

same sized fig fruits at a higher rate than smaller frugivorous animals
[Wrangham et al., 1993]. The method used for processing food items (e.g.,
with or without the use of cheek pouches) is also considered to influence the
speed of intake. However, the variables related to food quality considered in
the present analysis are sure to be suitable for the relative and rough com-
parisons of nutritional conditions in one species (e.g., interseasonal compari-
sons [Nakagawa, 1989a; present study] and interregional comparisons
[Nakagawa, 1989a; Nakagawa et al., 1996]). Therefore, data on the speed of
dry weight intake or at least the unit weights of food items should also now
be collected for different primate species; previous studies on feeding ecology
in nonhuman primates have focused on the nutritional content of food items
[e.g., Milton, 1979; Oates et al., 1980; McKey et al., 1981; Davies & Bennett,
1988; Rogers et al., 1990]. These data are being accumulated for various taxa
of nonhuman primates [e.g., Alouatta seniculus: Gaulin & Gaulin, 1982; Cebus
apella: Janson, 1985; Papio cynocephalus: Stacey, 1986; Shopland, 1987;
Macaca fascicularis: van Schaik & van Noordwijk, 1987; Gorilla gorilla
beringei: Watts, 1988; Papio anubis: Barton & Whitten, 1994]. Unfortunately,
however, few data are available to examine the generality in the regressions
that predict the nutritional intake with the speed of dry weight intake [but
see Barton & Whiten, 1994]. In future, the regression coefficients between
nutritional intake and variables related to food quality and those among these
each variable are expected to calculate for as many as primate species as
possible. Then, comparison of regression obtained among species can perhaps
reveal generality and speciality in feeding strategies among species.

CONCLUSIONS

1. In Japanese monkeys inhabiting a cool temperate forest, daily intake of

gross energy (DGEI) and protein (DGPI) in winter and summer were much lower
than those in autumn and spring.
2. Such lower values of DGEI and DGPI in the two former seasons were
influenced strongly not so much by the lower calorie and protein contents of food
as by the lower speed of dry weight intake.
3. This finding suggested that not only nutritional content of food but also
their speed of dry weight intake strongly determined the nutritional condition of
nonhuman primates.

ACKNOWLEDGMENTS

I am deeply indebted to Dr. Akio Maekawa, Dr. Tadahiro Tadokoro and their
technical assistants at the Tokyo University of Agriculture, who kindly under-
took the nutritional analysis of food items eaten in spring. I am also indebted to
Dr. Chiemi Saitoh at Tokyo University, who generously permitted use of her unpub-
lished data on nutritional content of food items eaten in spring. I am also grateful to
the District Forestry Office in Ishinomaki for providing excellent facilities during
the field work.
This study was financed in part by the Cooperative Research Fund of the
Primate Research Institute, Kyoto University, and in part by a special grant in
aid from Shion Junior College.
284 / Nakagawa
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APPENDIX Ia. Details of Each Food Item Eaten in Autumn*
Speed of Speed of Speed of Speed of
unit dry Calorie Crude calorie protein
Unitb intake weight content protein intake intake
Part weight (unit/ intake (g/ (kcal/ content (kcal/ (g dw/ Feeding time (min) DUR DW
Species name eatena (g dw) min) min) dw) (%) min) min) 22 Nov. 23 Nov. 24 Nov. 29 Nov. 30 Nov. (%)c (%)d

Rubus microphyllus Mlf 0.0128f 38.20 0.4890 4.436 14.62 2.169 0.0715 3.93 0.00 5.20 5.45 0.00 0.64 0.46
Lonicera japonica Fr 0.0340f 18.00 0.6120 4.540 11.25 2.779 0.0689 0.00 3.15 0.00 0.00 0.00 0.14 0.12
Mlf 0.0313f 25.90 0.8107 4.279 13.44 3.469 0.1090 7.55 19.50 37.75 14.50 20.48 4.35 5.23
Berberis thunbergii Fr 0.0202f 45.28 0.9148 4.513 11.26 4.128 0.1030 0.00 0.00 0.00 8.42 0.00 0.37 0.50
Rosa multiflora Fr 0.0319f 36.63 1.1684 4.280 8.28 5.001 0.0967 0.00 0.00 46.92 15.82 2.58 2.85 4.93
Mlf 0.00 0.00 0.00 0.00 3.68 0.16
Viburnum dilatatum Fr 0.0130f 46.15 0.5999 4.450 5.94 2.670 0.0356 0.00 30.95 17.18 0.00 21.40 3.03 2.69
Torreya nucifera Se 0.0886f 5.70 0.5048 5.284 17.33 2.668 0.0875 13.65 0.00 5.92 68.63 0.83 3.88 2.90
Clematic apiifolia Se 0.0108g 27.53 0.2973 4.819 18.98 1.433 0.0564 47.13 84.85 94.88 0.00 0.00 9.90 4.36
Oplismenus All 0.0184f 10.22 0.1881 3.888 6.29 0.731 0.0118 2.37 13.63 0.00 39.85 1.95 2.52 0.70
undulatifolius
Malus tschonoskii Fr 1.2781f 3.42h 4.3747h 4.680 1.06 20.475h 0.0464h 33.28 h 0.00h 0.00h 24.55 h 22.25 h 3.72 23.79
2.66h 3.3975h 15.902h 0.0360h 2.67h 0.00h 0.00h 2.60h 0.00h
Carpinus tschonoskii Se 0.0102f 55.80 0.5692 4.741 15.78 2.699 0.0898 313.32 248.17 248.17 241.63 324.12 63.04 53.14
Perilla frutescens Se 17.50 16.05 16.05 8.32 0.00 1.86
Quercus serrata Se 7.57 0.00 0.00 25.08 4.60 1.62
Viscum album Fr 0.0253e,f 19.91 0.5038e 4.443e 8.95e 2.238e 0.0451e 1.85 2.53 1.95 5.83 0.00 0.53 0.40
Schisandra repanda Fr 0.0253f 32.70 0.8273 4.443e 8.95e 3.675e 0.0740e 0.00 0.00 0.00 14.57 0.00 0.64 0.78
Fagus crenata Se 0.00 0.00 0.00 3.10 0.00 0.14
Boehmeria spicata Se 0.00 0.00 0.00 0.87 0.00 0.04
Trifolium spicata Mlf 0.00 0.00 0.00 0.00 2.17 0.09
Ganoderma lucidum All 0.00 0.00 0.00 0.00 5.27 0.23
Coriolus versicolor All 0.00 0.00 0.00 0.45 0.60 0.05
Seaweed 0.00 0.00 0.00 0.00 4.22 0.18
Soil 0.00 0.00 0.00 0.00 0.00 0.03
*
All data from Nakagawa [1989a].
a
All, all parts; fr, fruit; Mlf, mature leaf; Se, seed.
b
One unit of an item was defined as described in Methods.
c
Percentage of time spent feeding on each food item relative to the total feeding time for 5 sampling days.
d
Percentage of dry weight intake for each food item relative to the total dry weight intake for 5 sampling days.
e
Estimated values based on mean values for other fruits eaten in autumn were applied. The value for unit weight of fruits of Schisandra repanda was applied to that for
fruits of Viscum album.
f
One fruit, leaf, bud, etc., was regarded as one unit for an item that the monkey always ate as a discrete unit per bite or that the monkey did not always eat as a fixed
number of discrete units per bite.
g
For seeds of Clematic apiifolia, one unit was seeds in one flower.
h
The speed of unit intake differed between feeding in the tree (upper numbers) and feeding on the ground (lower numbers). Whereas both values were used for estimations of
DGEI and DGPI, only the values for feeding in the tree were used as the values for variables related to food quality, and thte total feeding time wasused for the variable
related to feeding time in the analysis for factors responsible for seasonal differences in DGEI and DGPI.
APPENDIX Ib. Details of Each Food Item Eaten in Winter*
Speed of Speed of Speed of Speed of
unit dry Calorie Crude calorie protein
Unitb intake weight content protein intake intake
Part weight (unit/ intake (g/ (kcal/ content (kcal/ (g dw/ Feedtime (min) DUR DW
Species name eatena (g dw) min) min) dw) (%) min) min) 21 Feb. 22 Feb. 23 Feb. 24 Feb. 25 Feb. (%) c (%)d

Oplismenus All 0.0184f 16.78 0.3088 3.888 6.29 1.201 0.0194 109.22 132.23 209.77 265.38 259.87 43.72 42.92
uadulatifolius
h
Zanthoxylum Br 0.0128 27.70 0.3545 4.206 11.10 1.491 0.0393 12.10 24.10 4.63 6.68 46.25 4.20 4.73
piperitum Bu 0.0053f 27.83 0.1475 4.323 16.77 0.638 0.0247 6.32 0.58 58.65 102.50 39.98 9.31 4.37
Tw 0.0190h 16.67 0.3167 4.222 9.27 1.337 0.0294 19.42 10.40 7.28 1.28 21.92 2.70 2.72
Zoysia japonica Mlf 0.111 g 35.40 0.3929 3.731 14.79 1.466 0.0581 0.00 156.37 0.00 0.00 0.00 7.00 8.75
Carpinus tschonoskii Se 0.0075f 30.60 0.2295 4.181 5.33 0.960 0.0122 3.27 29.93 39.77 27.07 46.77 6.57 4.80
Castanea crenata Bu 0.0055f 26.38 0.1451 4.392 7.73 0.637 0.0112 51.70 0.00 0.00 31.85 0.00 3.74 1.73
Se 0.00 0.00 0.55 0.00 0.00 0.02
Celastrus orbiculatus St 33.17 42.55 0.00 0.00 0.00 3.39
Celtis sinensis Br 0.0467h 19.11 0.8992 3.992 7.38 3.562 0.0658 41.83 33.63 0.00 0.00 0.00 2.38 9.58
Schizophragma Bu 0.0106f 46.43 0.4922 4.117 8.05 2.026 0.0396 17.25 0.00 20.58 0.00 16.70 2.44 3.82
hydrangeoides
Grass (Ixeris deblilis, All 0.0025f 45.88 0.1147 4.243 18.37 0.487 0.0211 19.03 5.67 0.42 21.93 3.53 2.27 0.83
Ixeris, stlonifera,
Trifolium repens,
Chamaele
decumbens)
Callicarpa japonica Br 0.0298e,h 21.30 0.6347e 4.099e 9.24e 2.602e 0.0586e 15.57 0.00 2.88 20.78 8.65 2.14 4.33
Lonicera japonica Mlf 0.0067g 7.25 0.0486 4.279 13.44 0.208 0.0065 35.33 0.00 0.00 0.00 0.00 1.58 0.24
Rhus ambigua Br, Br 0.00 34.43 34.43 0.00 0.00 1.54
Symplocos chinensis Br 0.0298e,h 30.90 0.9207e 4.099e 9.24e 3.774e 0.0851e 0.00 0.00 0.00 0.00 30.55 1.37 4.00
Cornus kousa Bu 0.0212f 35.00 0.7420 4.295 9.45 3.187 0.0701 0.00 18.27 18.27 0.00 2.87 0.95 2.23
Trachelospermum Mlf 0.0187f 35.17 0.6576 3.984 6.21 2.620 0.0408 0.00 16.78 16.78 0.00 0.00 0.75 1.57
asiaticum
Euonymus fortunei Mlf 0.00 6.25 6.25 8.50 0.37 0.68
Fraxinus lanuginosa Br 0.00 0.00 0.00 0.00 12.50 0.56
Cornus macrophylla Bu 0.0112f 24.30 0.2722 4.257 9.63 1.159 0.0262 2.52 0.00 0.00 9.63 0.00 0.54 0.47
Sagina maxima All 0.3686f 4.98 1.8350 2.605 4.83 4.781 0.0886 0.00 0.00 0.00 0.00 0.00 0.50 2.91
Coriolus versicolor All 0.00 4.98 4.98 0.00 0.00 0.22
Soil 0.50 0.00 0.00 1.20 0.42 0.16

(continued)
 288 / Nakagawa

APPENDIX Ib. Detals of Each Food Item Eaten in Winter* (continued)

Speed of Speed of Speed of Speed of
unit dry Calorie Crude calorie protein
Unitb intake weight content protein intake intake
Part weight (unit/ intake (g/ (kcal/ content (kcal/ (g dw/ Feedtime (min) DUR DW
Species name eatena (g dw) min) min) dw) (%) min) min) 21 Feb. 22 Feb. 23 Feb. 24 Feb. 25 Feb. (%) c (%)d
Torreya mucifera Sdl 0.90 0.00 0.00 0.00 0.00 0.04
Ilex macropoda Br 0.00 0.00 0.00 0.00 0.58 0.03
Rubus microphyllus Bu 0.00 0.00 0.00 0.00 0.57 0.03
Not identified 0.00 1.27 1.27 0.33 0.00 0.15
*
All data from Nakagawa [1989a].
a
All, all parts; Br, Bark; Bu, bud; Mlf, mature leaf; Se, seed; Sdl, seedling; St, stem; Tw, twig.
b
One unit of item was defined as described in Methods.
c
Percentage of time spent feeding on each food item relative to the total feeding time for 5 sampling days.
d
Percentage of dry weight intake for each food item relative to the total dry weight intake for 5 sampling days.
e
Estimated values based on mean values for other types of bark eaten in winter were applied.
f
One fruit, leaf, bud, etc., was regard as one unit for an item that the monkey always ate as a discrete unit per bite or that the moinkey did not always eat as a fixed number
of discrete units per bite.
g
For leaves of Zoysia japonica, one unit was three leaves. For leaves of Lonicera japonica, one unit was one cluster of leaves.
h
For barks, one unit was an area of 1 cm2 of bark. For twigs of Zanthoxylum pipertum, one unit was a 1 cm long piece of twig.