Herpetologists' League

Diet and Food Preferences of the Tortoises Geochelone carbonaria and G. denticulata in
Northwestern Brazil
Author(s): Debra K. Moskovits and Karen A. Bjorndal
Source: Herpetologica, Vol. 46, No. 2 (Jun., 1990), pp. 207-218
Published by: Herpetologists' League
Stable URL: http://www.jstor.org/stable/3892906
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Herpetologica,46(2), 1990, 207-218
? 1990 by The Herpetologists'League, Inc.

DIET AND FOOD PREFERENCES OF THE TORTOISES

GEOCHELONE CARBONARIA AND G. DENTICULATA IN
NORTHWESTERN BRAZIL
DEBRA K. MOSKOVITS"3AND KAREN A. BJORNDAL2
'Department of Biology, University of Chicago, Chicago, IL 60637, USA
2Center for Sea Turtle Research, Department of Zoology,
University of Florida, Gainesville, FL 32611, USA

ABSTRACT: We present the diet of the two Amazonian tortoises, Geochelone carbonaria and
G. denticulata, based on feeding observations and scat examinations of free-ranging individuals in
the rainforest of Maraci, northwestern Brazil. Fruits were prominent in the diet throughout the
year, but especially in the wet season; flowers were prominent in the dry season. Tortoises consumed
live and dead foliage, stems, fungi, soil, sand, pebbles, and animal matter throughout the year.
To examine the characters potentially associated with observed food preferences, we analyzed
samples of several food and non-food items for nutrient concentrations and fermentability. Typically
eaten foods had high relative abundance and calcium concentrations, while preferred foods had
high fermentabilities, high concentrations of total minerals, nitrogen and phosphorus, and low
calcium to phosphorus ratios. Nutrient profiles for preferred and rejected items were similar, and
nearly converse that of regularly eaten items. Concentrations of the nutrients analyzed cannot be
used to predict diet choice.
Key words: Amazonian rainforest; Diet; Food preference; Geochelone carbonaria; Geochelone
denticulata; Minerals; Nutrient; Tortoise

A NUMBER of studies have attempted to reportedly differ in food preferences (Cas-

identify factors important in the selection
of diets (reviewed in Pyke, 1984). For her-
bivores, it is increasingly recognized that
concentrations of specific nutrients in po-
tential foods may play a more significant
role than energy content in determining
diet choice (Belovsky, 1981; Bryant and
Kuropat, 1980; Owen-Smith and Novellie,
1982). Generalistherbivoresmust select an
appropriately balanced diet from a wide
array of possible food items.
The foraging behavior, ecology, and
population sizes of the two tortoises, Geo-
chelone carbonaria (Spix)and G. denticu-
lata (Linne)-large, ectothermic herbi-
vores living in the relatively benign
environment of the tropical rainforest-
might be considerably affected by the
availability of key nutrients. Yet the diets
of the two tortoises are poorly known. In-
formation on free-ranging individuals is
limited to brief notes in the literature,
which were summarized by Pritchardand
Trebbau (1984). In captivity, the species
3 Present Address: Division of Birds, Field Museum
of Natural History, Chicago, IL 60605, USA.
207
taiio-Mora and Lugo-Rugeles, 1981; Fre-
tey, 1977), although these differences may
be due to individual variation.
In this paper, we present data on the
diet of G. carbonaria and G. denticulata
in the rainforest of Marac'a, in Roraima,
northwestern Brazil, based on feeding ob-
servations and scat analysis. Nutrient com-
position of some of the items regularly eat-
en, preferred, or rejected by the tortoises
was determined. We examine seasonal
changes in diet and food availability and
discuss potential characters associated with
the observed food preferences.
MATERIALS AND METHODS
Field Work
Field work was carried out at Ilha de
Maraca, a 110,000 ha island reserve ad-
ministered by SEMA (Secretaria Especial
do Meio Ambiente), situated in the rain-
forest-savanna ecotone of northern Rorai-
ma, Brazil. The patchy habitat composi-
tion of the 570 ha study site is roughly 85%
forest and 15% open swamps or savanna
(Moskovits, 1988). Both species of Geo-
chelone used all habitat types. Between
208 HERPETOLOGICA
March 1981 and November 1982, 227 in-
dividuals (285 captures) were marked and
measured. Of these, 56 (20 male, 25 female
G. carbonaria; eight male, three female G.
denticulata) were radiotracked or trailed
for a total of 1442 tortoise-days (Moskovits
and Kiester, 1987). Location and activity
of the tortoises were checked at least once
daily (0600-1830 h), and active tortoises
were followed until lost from sight. Indi-
rect evidence was obtained from trailed
routes (e.g., partially eaten fruit, dug-up
soil). Feeding observations (direct and in-
direct) were recorded on 132 occasions (95
for G. carbonaria, 37 for G. denticulata):
110 in the dry (Aug-Mar) and 22 in the
wet (Apr-Jul) season. Samples of foods
were collected for identification, and, when
possible, larger samples were collected for
nutrient analyses (see below).
Tortoise scats found along routes of
trailed individuals or next to tortoises en-
countered, or collected while keeping tor-
toises overnight for processing, were in-
dividually picked and searched for
recognizable items. Most seeds recovered
from the 43 scats examined were matched
with those of fruits in the forest at the time.
Other seeds and animal parts were iden-
tified in museums and herbaria. Due to
wide variation in degree of food digestion,
retrieved items were not quantified. The
few items digested beyond recognition
were not further analyzed. Several of the
seeds recovered were planted to test for
viability.
Estimates of Fruit Availability
Fruit availability was estimated by the
spatial and temporal frequency with which
fruits were encountered along two census
trails (2 km each). In the 25 samples taken
over 18 mo in the field (one sample per 3
wk), 5 m wide strips were surveyed to the
left or right of the designated trails (chosen
at random with respect to habitat or mi-
crohabitat types). The side surveyed was
switched every 50 m. Each tree encoun-
tered in fruit was recorded, and the total
number of fruits on the tree and the pro-
portion apparently ripe were estimated.
Specimens of plants that we collected were
sent to the herbarium at the Instituto Na-
[Vol. 46, No. 2
cional de Pesquisas Amazonicas (INPA),
in Manaus, for identification. The presence
of flowers along these trails was noted, but
quantities were not estimated, and trees
were not measured.
Enclosure Observations
Observations were made on eight tor-
toises (three male, three female G. car-
bonaria; one male, one female G. denticu-
lata) held captive for up to 20 days during
both wet and dry seasons. The 400 m2 out-
door enclosure had red clay soil and was
at the savanna-forest ecotone. Captive tor-
toises were fed large quantities of the fruits
and flowers available in the field, and fresh
water was supplied daily.
Items consistently refused by the tor-
toises and not observed in the diet of free-
ranging individuals were considered "non-
foods." Preference for different foods was
easier to distinguish in the enclosure, where
tortoises chose certain foods and ate them
first or exclusively. Preference levels were
subjectively categorized as: items refused
or parts of foods not eaten (non-foods);
items eaten often or in moderation (i.e., in
amounts smaller or proportional to their
abundance in the study area); and items
highly preferred (i.e., eaten immediately
when available or presented in captivity,
seen eaten simultaneously by several tor-
toises in the field, or found in higher con-
centration in tortoise scats than in the for-
est).
Analyses of Nutrient Composition
and Fermentability
Thirty-three food and non-food items
were collected in sufficient quantity to be
analyzed for nutrient composition and fer-
mentability. These samples were sun-dried
in the field, and were redried in the lab-
oratory at 60 C to constant mass (approx-
imately 24 h). Dried samples were ground
through a 1 mm screen in a Wiley mill. A
portion of each sample was dried at 105
C to determine percent dry matter and
then ashed in a muffle furnace for 3 h at
500 C to determine percent organic matter
and ash (an estimate of total mineral con-
tent). In vitro organic matter digestibility,
or fermentability, was determined using
June 1990] HERPETOLOGICA
the Tilley and Terry (1963) method as
modified by Moore and Mott (1974). This
analysis consists of a 48 h incubation under
CO2 at 39 C with an inoculant of rumen
fluid (from a fistulated steer) followed by
a 48 h acid-pepsin treatment to remove
undigested microbes. The percent of or-
ganic matter that disappears during the 96
h is the fermentability of the sample.
Percentage of cell walls (cellulose, hemi-
cellulose, lignin and cutin, or neutral de-
tergent fiber ash-free) was measured by
the Van Soest technique (Goering and Van
Soest, 1970) with decalin and sodium sul-
fite omitted (Golding et al., 1985). Amylase
was used in the determination of cell walls
when necessary (Robertson and Van Soest,
1977). Percentage of cell contents (starch,
soluble sugars, protein) was determined by
subtracting percent cell walls from percent
organic matter. Analyses for percentages
of acid detergent fiber (a sub-fraction of
cell walls which is approximately equal to
the cellulose and lignin content), cellulose,
potassium permanganate lignin, and cutin
followed Goering and Van Soest (1970).
Percent concentrations of total (Kjeldahl)
nitrogen, phosphorus, and calcium were
measured with a block digester (Gallaher
et al., 1975) and an automated Technicon
analyzer (Hambleton, 1977). Replicates of
all analyses were acceptable within 1%rel-
ative error.
Statistical Analyses
Diet components were not distributed
normally in either the foraging observa-
tions (FO) or the scat samples (SC). There-
fore, comparison tests were performed on
ranks (Wilcoxon scores, equivalent to the
Wilcoxon rank-sum test for two levels and
the Kruskal-Wallis test for n levels; SAS
Institute Inc., 1987). Nutrient composi-
tions of the different preference levels were
also compared with non-parametric tests
(Wilcoxon and median scores; SAS Insti-
tute Inc., 1987). Nutrient profiles for the
different classes are presented as propor-
tional departures from the overall sample
median. Spearman rank correlation (r,;
SAS Institute Inc., 1987) were used to ana-
lyze the relationships among the different
nutrient concentrations measured.
209
TABLE 1.-Items recorded in the diet of Geochelone
carbonariaand G. denticulata.
Fruits.-Spondias lutea (Anacardiaceae), Anacardium gigantea (An-
acardiaceae), Annona sp. 1 (Annonaceae), Annona sp. 2 (Annona-
ceae), Duguetia surinamensis (Annonaceae), Philodendron sp. (Ara-
ceae), Bromeliad sp. (Bromeliaceae), Trattinnickia ravifolia
(Burseraceae), Licania kunthiana (Chrysobalanaceae), sp. (Lecythi-
daceae), Myriaspora egenensis (Melastomataceae), Bagassa guianen-
sis (Moraceae), Brosimum potabile (Moraceae), Ficus sp. (Moraceae),
Passiflora coccinea (Passifloraceae), Passiflora vespertitio (Passiflora-
ceae), Mauritia flexuosa (Palmae), Desrnoncus polyacanthus (Palmae),
Duroia eriopila (Rubiaceae), Genipa americana (Rubiaceae), Guet-
tarda argentea (Rubiaceae), Posoqueria sp. (Rubiaceae), Pradosia sp.
(Sapotaceae), Richardella (surinamensis) (Sapotaceae), Pouteria hirta
(Sapotaceae), Ecclinusa bacuri (Sapotaceae), Clavija sp. (Theophras-
taceae).
Flowers.-Jacaranda copaia (Bignoniaceae), Cochlospermum orino-
cense (Cochlospermaceae), Mauritia flexuosa (Palmae).
Miscellaneous.-mushrooms (several species); Maximilliana (palm) frond
base; unidentified grasses, live leaves, vine stems, roots; sand, soil,
pebbles; tortoise scat.
Animal matter.-snails (at least 2 species); ants (several species); ter-
mites; beetles (assorted body parts recovered); butterflies (wings re-
covered); Euglossine bees; snakes (ventral scales recovered); lizards;
birds (leg of Psarocolius viridis recovered); agouti; peccary; deer
carcasses.
Too few scats of G. denticulata were
collected for statistical comparisons be-
tween species or sexes, and seasonal com-
parisons were only possible for G. carbo-
naria. Juveniles were not included in any
of the analyses.
RESULTS
Seasonal Diet and Food Preferences
The diverse diet of Geochelone carbo-
naria and G. denticulata at Maraca' con-
sisted of various vegetative and reproduc-
tive plant parts (grasses, leaves, vines, roots,
bark, fruits, and flowers), fungi (several
gilled and woody mushrooms), animal
matter (vertebrate carrion, insects, snails),
soil, sand, and pebbles (Table 1). The pro-
portions of these various food items in the
diet differed markedly when based on for-
aging observations (FO) or on scat exam-
ination (SC) (Table 2). Although fruit
ranked highest in both categories, flowers,
which ranked second highest in foraging
observations, were never detected in the
visual examination of scats. In contrast, an-
imal matter (both vertebrate and inver-
tebrate) was recovered from nearly half of
the scats examined, but was observed eaten
only once in the field (one male G. car-
bonaria feeding on an agouti carcass).
Vegetative plant parts (grasses, leaves, leaf
litter, bark) also were detected more easily
in scats than in field observations.
Diet composition did not differ signifi-
TABLE 2.-Food categories in the diet of Geochelone carbonaria (C) and G. denticulata (D), grouped by: (a) sex
(b) season (D = dry, W = wet). For each food category, percent of foraging observations (FO) is presented first, fo
(in parentheses). n = total number of observations or scats (pooled over all individuals). Note that scats contained
up to 100. The two highest entries in each row are boldfaced for FO and underlined for SC. For the pooled da
significantly for all food categories (Wilcoxon scores range from 5.3-48.8, df = 1, 0.0001 < P < 0.02). For G.
significantly (W scores from 15.6-20.1, df = 1, P < 0.001).
(a) Grouped by species (SP) and sex (SX)
SP SX n Fruit Flower LV' DV2 Fungi Soil."

C M 22 (16) 68.2 (81.3) 13.6 (0) 9.1 (81.3) 0.0 (43.7) 4.6 (18.7) 0.0 (43.7)
C F 70 (17) 40.0 (70.6) 27.1 (0) 21.4 (64.7) 2.9 (35.3) 4.3 (17.7) 4.3 (41.2)
C J 3 (5) 66.7 (60.0) 0.0 (0) 0.0 (60.0) 33.3 (60.0) 0.0 (0.0) 0.0 (100.0)
C 95 (38) 47.4 (73.7) 23.2 (0) 17.7 (71.1) 3.2 (42.1) 4.2 (15.8) 3.2 (50.0)
D 37 (5) 46.0 (60.0) 29.7 (0) 8.1 (80.0) 5.4 (80.0) 0.0(40.0) 10.8 (20.0)
(b) Grouped by species (SP) and season (SN)
SP SN n Fruit Flower LV, DV2 Fungi Soil,

C D 76 (27) 40.8 (63.0) 29.0 (0) 15.8 (66.7) 4.0 (44.4) 5.2 (11.1) 2.6 (51.9)
C W 20 (11) 70.0 (100.0) 0.0 (0) 25.0 (81.8) 0.0 (36.4) 0.0 (27.3) 5.0 (45.5)
D D 36 (3) 41.7 (33.3) 30.6 (0) 8.3 (100.0) 5.6 (66.6) 0.0 (33.3) 11.1 (0.0)
D W 2 (2) 100.0 (100.0) 0.0 (0) 0.0 (50.0) 0.0 (100.0) 0.0 (50.0) 0.0 (50.0)
LV = live vegetative plant parts: leaves, stems, roots.
2DV = dead leaves (leaf litter) and bark.
Soil = soil + sand + pebbles.
VERT = vertebrates.
INV = invertebrates.
ANIM = any animal part (vertebrate or invertebrate).
June 1990] HERPETOLOGICA 211

a. Fruit: 1 = eaten
=
3
CI 30
2 possibly eaten
co 3 = not eaten
._ Flower:
0 20

Z 10

~b.
30
-a

4.0
co 20
E

0.O
M J J A S O N D J F M A M J J A S 0
1981 -- 1982
WET DRY WET DRY
FIG. L-(a) Phenology of fruiting and flowering trees. Fruits are grouped as eaten (1), possibly eaten (2),
or not eaten (3) by Geochelone. (b) Estimated number of ripe fruits (total over all trees censused) present
per sample.

cantly between species (Table 2; P > 0.1 of the multi-seeded Duguetia were re-
for the nine food categories in FO; SC not covered simultaneously. Of six species re-
tested). Within species, the only sex dif- trieved from scats and planted, four ger-
ference detected was the higher consump- minated successfully.
tion of fruit by male than by female G. In the rainyseason,when fruitingpeaked
carbonaria (significant for FO only, x2- in both volume and number of species (Fig.
5.5, df = 1, P = 0.02). la,b), fruits made up over 70%of the feed-
Seasonal differences, testable for G. car- ing observationsand were present in 100%
bonaria only, were pronounced in the con- of the scats examined. During this season,
sumption of fruit and flowers. Fruit con- large fruits (such as Duguetia surinamen-
sumption was considerably higher in the sis, Richardella surinamensis?, Pouteria
wet than in the dry season (x2 = 5.4, df- hirta) or smallerfruitsin large-canopytrees
1, P = 0.02 for both FO and SC), while (Spondias lutea, Pradosia sp.) were widely
flowers were observed eaten only in the available (present in 43% of the 40, 100-
dry season. m blocks censused; Moskovits, 1985).
Fruits (27 identified and at least four The rich, oily fruit of the palm Mauritia
unidentified species) were the major item flexuosa was available in the forest and was
consumed. They comprised nearly half of consumed by the tortoises throughout the
the feeding observations for both species year (Fig. 2). Tortoisesoften ate the fruits
and were recovered from over 60% of all of two species, Bagassaguianensis(Mora-
scats examined (Table 2). Up to five dif- ceae) and Myriaspora egenensis (Melas-
ferent species of fruit were retrieved from tomataceae), which were rare in the study
a single fecal sample, and up to 34 seeds area. Only one tree of Myriaspora and
of the single-seeded Spondias lutea (xt = three trees of Bagassa were found in the
8.6 g, single fruit wet weight) and 40 seeds study track, and neither was present along
212 HERPETOLOGICA [Vol. 46, No. 2

MONTHSIN FRUIT (OR FLOWER) 1

FAMILY GENUS SPECIES -wet season f----dry season -wet season-Fdry season-
__________________________________________ May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct
FRUITS
Anacardiaceae Spondias lutea
Annona sp*1
Annonaceae Annona sp.2
Duguetia surinamensis
Araceae Philodendron sp.
Bromeliaceae - sp.
Burseraceae Trattinnickia ravifolia

Chrysobalanaceae Licania kunthiana

Lecythidaceae _ sp.
Melastomataceae Myriaspora egenensis
( Bagassa guianensis
Moraceae Brosimum potabile
Ficus sp.
Passiflora coccinea
Passif loraceae Passiflora vespertilio

Palnae Mauritia flexuosa

Duroia eriopila
Rubiaceae Genipa americana
Guettarda argentea
(Pradosia sp.
Richardella (surinamensis)
Sapotaceae Pouteria hirta

Ecclinusa bacuri
Theophrastaceae Clavija sp.

FLOWERS
Bignoniaceae Jacaranda copaia
Cochlospermaceae Cochlospermum orinocense
Palmae Mauritia flexuosa J ,_ ,

FIG. 2. -Phenology of the important species of fruits and flowers eaten by Geochelone. Hatched lines
represent fruits that were probably unripe.

the fruit census trails. Groups of 2-5 in- bright yellow Cochlospermum orinocense
dividuals fed simultaneously under trees made up 30% of all flowers observed eaten.
(Bagassa) bearing ripe fruit, even though Yet the visually very similar Allamanda
individuals of Geochelone were generally cathartica (Apocynaceae) was never seen
solitary animals. Tortoises also aggregated eaten in the field and was rejected in cap-
under Genipa americana bearing ripe tivity (Table 3). The small and fragrant,
fruit. Fruits not seen eaten by tortoises, and orange-yellow flowers of Mauritia palms
considered unlikely items in their diet (type were available over much of the year (Fig.
"3" in Fig. 1), were generally non-fleshy 2), but were observed eaten only during
and wind-dispersed or too large and hard the dry season.
for tortoises to consume. Several species of mushrooms were eat-
Flowers constituted close to 30% of the en readily by the tortoises. Often the fungi
feeding observations during the dry season were recovered seemingly intact from tor-
for both species of Geochelone. The flow- toise scats. Mushrooms were considerably
ering peak at Marac'a occurred in the mid- more conspicuous in the forest during the
dle to late dry season (Fig. 1), when the rainy season, but tortoises were observed
fruits in the forest were generally small or eating them only during the dry season
present singly or in small clusters. Three (Table 2). No seasonal difference was ev-
species (Table 1) comprised over 72% of ident from the scat data. Also consumed
the flower feeding observations, and the year-round were live grasses, leaves, stems,
June 1990] HERPETOLOGICA
vines, and roots,and dead leaves, bark,soil, eral concentrations. They were relatively
sand, and pebbles. Scat reingestion was ob- abundant and high in Ca concentration
served once in the enclosure.
Feeding Behavior
When feeding in patches of dense fruit
or flowers, tortoises did not systematically
eat the firstitem encountered.Instead,they
zig-zagged back and forth, holding their
heads low and sniffing loudly. They often
took only a few bites of a fruit or flower
that they later returned to eat whole, and
when eating leaves, they generally bit and
rejected several before swallowing one.
This same pick-and-choosebehaviorwas
displayed in the enclosure, even when the
tortoiseswere presented non-naturalfoods
(e.g., banana, papaya). Captive tortoises
often ate two or more items simultaneous-
ly, taking a few bites from each and
switching frequently. Individual prefer-
ences varied among the tortoises tested,
but all ate meat first when presented with
a variety of items. Large live grubs were
consumed immediately when presented to
one captive individual.
The tortoises swallowed most of their
foods whole in the field, only occasionally
using their forelimbs to help tear larger
items. However, in captivity, they manip-
ulated the foods in their mouths until seeds
or hard items were ejected. They did not
swallow the seeds or bones as they did in
the field. Both species showed keen dis-
criminating capabilities in captivity, com-
ing directly to a favored item from as far
as 20 m away and learning to avoid per-
manent obstacles(such as a dividing fence)
along the way.
Nutrient Analyses
Nutrient analyseswere performed on 12
rejected, 18 regularlyeaten, and three pre-
ferred items. Of the variables considered
(Table 3), median values differed signifi-
cantly for abundance, fermentability, cell
wall (cellulose, hemicellulose and lignin),
nitrogen (N) concentration,phosphorus(P)
concentration, and calcium (Ca):P ratios
(Fig. 3). The foods regularly eaten seem
"poor"in quality, with high cell wall con-
centrations (especially cutin), low fer-
mentability, and low N, P, and total min-
213
with high Ca:P ratios. In contrast, pre-
ferred foods had low Ca concentrations
and Ca:P ratios, low cell wall concentra-
tions, high fermentability, and high N, P,
and total mineral concentrations (Fig. 3).
Surprisingly, items preferred and rejected
were similar in nutrient composition. This
may be, in part, because regularly eaten
foods analyzed were mostly fruits (16 of
18 items), while those preferred or rejected
were mostly flowers (two of three and nine
of 12, respectively).
DISCUSSION
Land turtles are primarily opportunistic
feeders, their diets often reflecting season-
al and regional availabilities of food (e.g.,
Hansen et al., 1976; Klimstra and New-
some, 1960; Luckenbach, 1982). However,
turtles are capable of discriminating colors
and of feeding selectively in their envi-
ronment (e.g. Macdonald and Mushinsky,
1988; Quaranta and Evans, 1949; Swing-
land and Frazier, 1979). In a study in Flor-
ida, Gopherus polyphemus were consid-
ered intermediate between foraging
specialists and generalists (Macdonald and
Mushinsky, 1988).
In Marac'a, the two species of Geoche-
lone ate primarily fruits throughout the
year. They heavily supplemented their diet
with flowers in the dry season, and with
animal matter, live and dead vegetative
plant parts (leaves, vines, roots, leaf litter),
fungi, soil, sand, and pebbles year-round.
Species and sex differences were not de-
tected, except for a higher overall con-
sumption of fruit by male than by female
G. carbonaria (significant in FO only). Sea-
sonal differences, analyzable only for G.
carbonaria, were pronounced in fruit and
flower consumption, and reflected overall
availability in the forest. The pronounced
differences between foraging observations
and scat examinations suggest that the diet
information presented here is preliminary.
Given both the complexity of the rainfor-
est and its ample food abundance, and the
broad diet of the Geochelone, additional
food items should be identified with fur-
ther study.
TABLE 3.-Nutrient composition (%) of items rejected (R), accepted (A), and preferred (P). Abundance categories a
and 2 = abundant. Fermentability is expressed as % organic matter; the other variables are % dry matter. ADF

Prefer- Abun- Ferment- Organic Cell

ence dance ability matter contents Cell walls ADF Cellulose Lignin Cutin Ni

Fruit (unripe)
Aegiphila membranacea R 1 46.6 91.9 43.5 48.3 37.3 22.1 10.8 4.7
Duguetia surinamensis R 1 27.4 96.9 22.7 74.3 55.2 33.3 15.7 6.3
Gustavia augusta R 0 46.7 95.5 44.4 51.4 34.8 21.6 10.1 3.1
Flower
Allamanda cathartica R 2 63.3 93.9 66.0 29.8 20.7 13.6 4.8 1.2
Genipa americana R 1 56.0 94.7 56.0 40.0 33.0 15.3 15.5 3.3
UT 1 R 1 63.3 94.6 60.3 34.9 24.7 11.7 11.7 1.9
UT 2 R 1 85.8 94.9 78.0 17.6 10.8 6.8 2.7 0.9
UT 3 R 1 61.3 92.1 65.7 29.5 21.1 13.0 4.8 1.0
Ul 4 R 1 72.4 94.7 74.4 20.9 13.9 9.0 2.2 2.4
Ul 5 R 1 31.8 95.9 52.7 44.9 28.5 8.5 14.5 6.4
UT 6 R 1 63.9 96.0 76.7 19.9 13.2 6.8 3.3 3.4
UT 7 R 1 - 97.1 67.2 30.5 17.5 9.5 5.9 2.4
Stem
Ul vine A 2 55.7 78.4 30.7 56.9 45.6 22.1 14.0 4.0
 TABLE 3.-Continued.
Prefer- Abun- Ferment- Organic Cell
ence dance ability matter contents Cell walls ADF Cellulose Lignin Cutin Nit

Fruit (ripe)
Bagassa guianensis A 0 51.9 91.2 47.9 50.9 43.7 13.1 11.2 14.3
Duguetia surinamensis A 1 31.0 96.4 24.6 72.3 53.4 30.4 15.6 7.4
Ecclinusa guyanensis A 2 12.2 97.9 19.1 81.4 73.5 20.7 6.8 45.2 0
Genipa americana A 2 52.7 95.3 38.5 57.0 44.3 29.8 11.1 3.3
Genipa a. (rind) A 2 75.4 95.9 67.6 28.3 24.2 16.5 6.3 1.2 0
Geophila gracilis A 2 50.9 90.9 38.3 53.5 43.0 3.4 7.7 11.2 2
Guettarda argentea A 0 36.9 94.8 37.9 58.6 46.6 21.4 10.2 14.7 0
Ficus sp. A 1 42.0 95.4 34.7 61.5 42.3 18.3 11.7 12.1
Mauritia flexuosa A 2 20.7 94.9 37.7 59.3 46.1 21.8 8.6 13.4 0
Mauritia f. (seed coat) A 2 65.4 94.8 41.1 54.8 38.5 31.4 6.4 1.3 0
Myriaspora egenensis A 0 66.9 96.2 66.5 30.2 25.9 7.3 7.6 11.0 1
Passiflora sp. A 2 43.3 94.1 30.2 64.1 47.3 27.3 13.5 6.6 2
Philodendron sp. A 1 76.5 93.7 71.7 22.1 15.4 6.9 6.1 2.3 1
Spondias lutea A 2 20.2 95.6 21.1 75.6 64.9 40.4 12.7 11.2 0
UT 1 A 0 35.1 96.6 37.7 60.3 53.7 16.9 9.5 26.9 1
UT 2 A 1 29.3 97.6 32.1 66.4 54.5 20.8 10.6 22.7 1
Flower
Passiflora sp. A 2 56.9 92.4 53.2 41.6 19.0 9.1 5.2 4.7 3
Flower
Jacaranda copaia P 1 65.4 96.1 60.4 37.0 24.9 9.0 6.4 8.7 2
Cochiospermum orino- P 1 62.1 91.8 58.2 36.0 26.9 13.4 9.6 3.2 2
cense
Fungus
Ul mushroom P 1 58.7 80.0 45.8 42.4 25.8 11.5 6.2 1.9 5
216 HERPETOLOGICA [Vol. 46, No. 2

ITEMS
Eaten regularly Preferred Rejected

++ Abundance
++ Fermentability
* % Organic matter-
% Cell contents -
** ++ % Cell wall -
* ++ % Cellulose -
% Lignin -
** + % Cutin -

** + % Nitrogen -
% Minerals -
** ++ % Phosphorus -
% Calcium
** + CA:P

-1 0 1 -1 0 1 -1 0 1

Departure from overall sample median (%)

FIG. 3.-Nutrient composition profile. Levels of significance in comparison of medians: Wilcoxon scores
(rank sums) * = P < 0.05, ** P < 0.01; median scores (number of points above the median) + = P <
0.05, ++ = P< 0.01.

Despite the seasonal changes observed,
the diet of the Geochelone did not solely
reflect abundance in the forest. The tor-
toises frequently ate at least two fruits that
were rare in the study area. They rejected
the flowers of Allamanda cathartica, which
were available simultaneously with, and
closely resembled, the favored flowers of
Cochlospermum orinocense. Further-
more, they consumed flowers of Mauritia
flexuosa only in the late dry season, al-
though the flowers were available through
much of the year (Fig. 2). Both species of
Geochelone also showed keen discrimi-
nating capabilities in the enclosure, often
coming directly to a favored food item.
In the enclosure, where soil was harder
clay and sand was not available, tortoises
did not swallow their foods whole as they
did in the forest. As suggested by many
(e.g., Luckenbach, 1982; Marlow and Tol-
lestrup, 1982; Sokol, 1971), sand may be
important as an abrasive agent enhancing
digestion, and its absence in the enclosure
may have contributed to the observed shift
in behavior.
Given this tendency of the Geochelone
to swallow foods whole, and to frequent
treefalls regularly (ideal environments for
the growth and establishment of seed-
lings), they are probablyeffective seed dis-
persers. This also has been suggested for
Gopherus polyphemus (Macdonald and
Mushinsky, 1988) and Testudo graeca
(Cobo and Andreu, 1988).
A large portion of the diet of the tor-
toises was high in cell wall concentration
(especially cutin), was relatively low in fer-
mentability and cell contents (starch, sol-
uble sugars, protein) and was low in total
mineral concentration. However, these
foods were relatively abundant in the for-
est and were high in Ca concentrations.In
contrast,the few preferred items were low
in cell wall contents, high in cell contents
and fermentability, and high in overall
minerals, P, and total N concentrations.
Items rejected were very similar to the
preferred foods in nutrient composition,
although their total mineral, P, and N con-
centrations were not as high (Fig. 3). This
similarity may have been due, in part, to
the high proportionof flowers represented
in both the non-food and the preferred
samples. The observed tendency for tor-
toises to eat several foods simultaneously
June 1990] HERPETOLOGICA
in captivity, their seemingly haphazard
behavior in the field, and the diversity of
items recovered from single scat samples
may indicate that tortoises reach an ade-
quate balance of nutrients by ingesting a
wide variety of foods.
Based on the nutrient profiles obtained
in this study, concentrations of the nu-
trients analyzed cannot be used to predict
diet choice. Yet three points should be con-
sidered. First, toxic and secondary com-
pounds were not examined in this study,
and they might be important in determin-
ing the diet of the tortoises. It is likely,
however, that fruiting trees have not
evolved specific noxious compounds to de-
ter the tortoises, which are potential seed
dispersers. Second, fermentability, used
here as a relative measure of microbial
degradability of the foods, may not reflect
digestibility in the tortoises' guts. How-
ever, both species of Geochelone rely on
a hindgut microbial fermentation, similar
to the rumen fermentation, to degrade the
cell wall fraction of their diet (Bjorndal,
1989). Third, the relative concentrations
of a nutrient in a series of food items do
not necessarily reflect the relative avail-
abilities of that nutrient in the food items.
Minerals,especially, vary greatly in avail-
ability, and their absorption in the gut is
a complex interaction of the pH, the pres-
ence or absence of other minerals, and the
chemical form of the mineral (Robbins,
1983; Van Soest, 1982). Appropriate data
on relative availabilities, along with nu-
trient analysesof a broadersample of items
regularly eaten, preferred, and rejected,
should help clarify the nutritionalbasis for
food preferences.
Acknowledgments-We thank Dr. P. Nogueira
Neto for SEMA facilities; G. M. de Oliveira, L. Pes-
tana, J. and E. Lima da Silva, and Amazonas for help
in the field; and Dr. P. E. Vanzolini for invaluable
support at every stage. For specimen identifications,
we thank Dr. M. F. da Silva, INPA (plants); Dr. R.
B. Foster, FMNH (seeds); and Dr. J. W. Fitzpatrick,
FMNH (bird parts). J. Moore generously provided
use of his laboratory. A. Bolten, D. F. Stotz, R. D.
Semlitsch, and four anonymous reviewers made valu-
able suggestions on earlier versions of the manuscript.
Grants to DKM from the Chicago Zoological Society,
the Hinds Fund of the University of Chicago, and
the National Academy of Science helped fund the
217
project. Finally, we are deeply grateful to R. Mos-
kovits for her immeasurable assistance in the field.
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Accepted: 28 June 1989
Associate Editor: Raymond Semlitsch