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An analysis of chewed food particle size and its relationship to molar structure in the primatesCheirogaleus medius andGalago senegalensis and the insectivoranTupaia glis.

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An Analysis of Chewed Food Particle Size and Its Relationship
to Molar Structure in the Primates Cheirogaleus medius
and Galago senegalensis and the
lnsectivoran Tupaia glis
WENDY SUE SHEINE AND RICHARD F. KAY
Department ofAnatomy, Duke University Medical Center, Durham, North Carolina 27710
KEY WORDS Lemuridae
Dentitions
- Lorisidae . Tupaiidae - Digestion
- Molar tooth structure
ABSTRACT
The chewed food particle size and shearing capacity of the lower
molars of two primate species, the fat-tailed dwarf lemur, Cheirogaleus medius
and the bushbaby Galago senegalensis, and an insectivoran, the tree shrew,
Tupaia glk, were compared. Differences in the shearing design of the lower
molars correlate strongly with the chewed food particle size in these species: the
greater the shearing capacity, the smaller the chewed food particles.
These three species are of comparable size but differ greatly in diet in the wild.
C. medius primarily eats fruit and nectar, while G. senegalensis and T.glis are
largely insect-eaters. The lower molars of G. senegalensisand T! glisshow a much
greater shearing capacity than do those of C. medius. The average length of
chewed food particles of C. medius is significantly larger than that of G.
senegalensis, while that of T.glis is intermediate between the two primates but is
closer to that of G. senegalensis.
Our findings that insect-eating species grind their food more finely than do
fruit- and resin-eating species can be correlated with digestibility of foods: finely
chewing foods such as fruits which are low in relatively undigestible cell wall
components would not greatly improve their digestibility, so a highly efficient
food processing apparatus would be less important to the animal's survival.
Insect-eaters much more finely chew their foods, implying that there is some constituent of insect bodies difficult to digest, and that grinding increases its
digestibility. We suggest that this constituent is chitin.
Considerable attention has recently 'been
given to differences in the functional organization of the primate dentition and its relevance to feeding behavior (e.g., Kay, '73, '75,
in press; Kay and Hylander, in press;
Hylander, '75; Zingeser, '73; Rosenberger and
Kinzey, '76). However only Walker and Murray ('72, '75) actually attempted to establish
some link between molar structure and size of
chewed food particles in primate species with
different diets. In this paper we attempt to
refine and extend their analyses on the
assumption that the most meaningful way to
characterize the biological role of the dentiAM. J. PHYS. ANTHROP., 47: 15-20.
tion, and particularly the triturition mechanism, is t o determine the particle size of
chewed foods. Of particular concern here is
identifying dental parameters which can be
correlated with particle size or shape so that
one can assign a "triturition efficiency" rating
to a particular molar shape or construction.
(Kay ('73, '75) and Kay and Hylander (in
press) showed that there are major differences
between the molar shapes of insectivorous
and frugivorous mammals and inferred that
these differences are related to the efficiency
of digestion. We present evidence to support
this notion.
15
16
WENDY SUE SHEINE AND RICHARD F. KAY
TABLE 1
Size (in mm) of food particles in the feces of three species studied. N is the number of particles measured, X is the mean,
M is the median, S.D. is the standard deuiutwn, SK is the skewness
Length
R
N
Species
Cheirogaleus medius
Galago senegalensis
Tupaia glis
1,000
1,000
1,000
1.54
0.67
0.98
Breadth
SD
SK
x
M
SD
SK
1.32
0.51
0.72
2.73
3.60
1.79
0.81
0.30
0.50
0.63
0.25
0.39
0.63
0.22
0.37
1.90
3.66
1.82
M
1.15
0.54
0.78
TABLE 2
Mean second lower molar dimensions in the three species studied
M2
Species (sample size)
length
Paracristid
obliquecristid
Cheirogaleus medius (2)
Galago senegalensis (5)
npaiaglis (4)
2.22
2.22
3.29
0.58
0.94
0.99
1.29
1.04
1.75
MATERIALS AND METHODS
Three mature Cheirogaleus medius, the fattailed dwarf lemur, six Galago senegalensis,
the bushbaby, and two Tupaia glis, the tree
shrew were used in an experiment to determine the size of chewed food particles. The
choice of animals was based on an approximate equivalence of body size (to minimize
the effects of allometry) and diversity of diet
in the wild. Galago senegalensis and Tupaia
glis are primarily insectivorous while Cheirogaleus eats much more fruit and resin. A relatively rigid food with a high cellulose fraction,
carrots, was chosen as the experimental food
on the assumption that the chewed particles
would be easily recognizable on the basis of
color, and that the cellulose fraction, being
virtually undigestible in small animals, would
be minimally altered after swallowing. Most
important, this food is eaten by virtually all
captive primates facilitating future species
comparisons.
The animals were food deprived for about 12
hours prior to the experimental procedure.
Then they were placed in wire bottomed cages
and fed pieces of carrot cut into 1 mm X 10
mm x 25 mm slices. No other foods were presented for the duration of the experimental
procedure. Ad lib feeding continued for 48 to
72 hours. Feces were collected at 12-hour
intervals and preserved in 10% formalin.
Feces analysis was undertaken rather than
analysis of stomach contents due to the difficulty of stomach pumping operations with
small animals (see note added in proof).
A sample of feces was placed in a tray of
water and shaken gently to separate the particles. The particles were spread on a gridded
Hypocristid
0.64
0.70
1.39
Postmetacristid
0.54
1.10
1.12
Preentccristid
0.47
0.82
1.09
filter paper mounted in a Buchner funnel connected t o a filter flask and vacuum. The sides
of the funnel were washed with water to
insure that all particles rested on the paper. After suction, the paper was removed
with forceps and placed under a microscope
equipped with a calibrated reticle. Two
linear dimensions were measured on each carrot particle-the maximum length and the
maximum breadth orthogonal to the long axis
of the particle.
The total shearing capacity of the postcanine dentitions of each species was estimated by measuring the summed lengths of
the M2 shearing blades, the cristid obliqua,
post-hypocristid, protocristid, pre-entocristid,
and postmetacristid. M, was chosen because
its structure is usually representative of that
of the postcanines as a whole (Kay, "73, '75).
RESULTS
A. Behavioral observations
The feeding behaviors of the three species
were very similar. Each animal picked up a
carrot slice in its hand and conveyed it to its
mouth. The slice was often held and visually
inspected, especially by C.medius and G. senegalensis. A bite was taken by inserting the
slice into the side of the mouth in the
postcanine region. In most instances the
chunk bitten off was masticated thoroughly
and swallowed before another bite was taken.
Often during chewing the animal held the remainder of the carrot slice in one or both
hands. We have very little quantitative data
on the number of masticatory cycles each species took for a comparable sized carrot slice.
However, a small number of chewing counts
CHEWED FOOD PARTICLE SIZE
17
A
B
C
Fig. 1 Lateral views of the lower P,-MBof A, Galago senegalensis (left P,-MJ anterior to the left, M, length
= 2.22 mm; B, Cheirogaleus medias, right P,-M, anterior to the right, M2length = 2.22 mm; C, f i p a t a g h (left
P,-MJ anterior to the right, Mzlength = 3.29 mm. By comparison with Galago and Tupaia, the molars of
Cheirogaleus have low cusps and short shearing blades.
did not reveal apparent contrasts among the
species.
B. Chewed food particle size and shape
The mean of the maximum dimension of the
chewed carrot particles recovered in feces
(table 1) differ significantly. (Probabilities in
students t test are p < <0.001.) Although
skewed distributions are not legitimately
testable with students t, the deviation of the
probabilities is probably negligible with such
large sample sizes. Cheirogaleus medius had
the longest food particles, Galago senegalensis
the smallest, with Tupaia glis food particles
intermediate in size but closer to G.senegalensis. The mean breadth of food particles of
Cheirogaleus medius is significantly larger
than those of other species (p<<O.OOl).
Tupaia glis food particle breadths are significantly larger than those of Galago senegalensis.
All food particle lengths and breadths are
right-skewed (table 1).In recognition of this,
the shape of each particle was separately calculated as a ratio of length to breadth. Then
the ratios were averaged. Thus the ratios
presented cannot be calculated from the mean
particle length and breadth in table 1. The
shapes of the chewed food particles of the species are also significantly different (p< 0.01).
Galago senegalensis particles are 2.66 times as
long as they are wide, Cheirogaleus rnedius
particles are 2.09 times as long as they are
broad. Tupaia glis particles are intermediate
in shape (2.19).
The functional design of the second molars
of the species studied (representative of the
triturition mechanism as a whole) are quite
different (table 2, figs. 1 A-C). The second
molars of Cheirogaleus medius have low cusp
relief compared with those of Galago senegalensis and Tupaia glis. The crests (which
function as shearing blades) are in general
shorter and less trenchant: the sum of the five
measured crests divided by tooth length is
1.43 for Cheirogaleus, compared with 2.10 for
Galago senegalensis and 2.02 for Tupaia glis.
Irrespective of diet, the total M2 shearing
blade length of primates (estimated by summing the length of the same 5 crests used in
table 2) is negatively allometric with respect
to M2 length (log, total shearing = 0.34 +
0.91 log, M 2length for 41 species of non-cecopithecid primates) (Kay, unpublished data).
18
WENDY SUE SHEINE AND RICHARD F. K A Y
In other words, smaller primates have proportionally longer shearing blades than large primates. This allometric effect must be taken
into account in comparisons of the molar
shearing capacity of species with different
sized molars (Kay, '75). From the equation, an
"average" primate with a tooth lengthened
the same a s G. senegalensis would have a
summed M, shearing blade length of 2.91
mm. Galago senegalensis has 160% of the expected shearingcrest length for a primate with
its M, length, Cheirogaleus medius has 109%
and the insectivoran, Tupaia glk, is intermediate with 145% compared with the primate
model.
The differences in the shearing design of the
second lower molars correlate strongly with
the size of chewed food particles in these comparably sized mammals: the greater the
shearing capacity, the smaller are the food
particles.
DISCUSSION
We have shown that the three species
studied differ significantly in the size and
shape of the food particles in their feces. This
observation can be accounted for in several
ways. In terms of oral food preparation, either
the teeth of some of the species are more efficient in reducing food particle size, or some
species simply chew the foods more finely
than others. The data in table 2 illustrates
that there are major differences in the shapes
of the molars and t h a t those species with bett e r developed shearing blades also have
smaller food particles in their feces. We have
not investigated whether some species are
chewing comparably sized items more times
than other species. This may be a very important consideration, particularly when the species differ in body size.
The possibility must also be considered that
the size of food particles in the feces may not
be solely a reflection of differences in oral food
preparation. One way to approach this
problem would be to extract and analyze the
food particles immediately after swallowing.
However, this imposes some amount of risk to
the survival of the subjects, some of which are
endangered in the wild. The other way to
minimize post-oral food particle size change is
to select foods unlikely to be significantly
digested. We chose carrots, which have a high
cellulose fraction, because there is little
likelihood t h a t the species could efficiently
process it. For precisely the opposite reason,
chitin was unacceptable, because, as we will
mention below, we strongly suspect t h a t
chitin is relatively highly digestible in some
primate species. Carrots have the additional
advantage as a n experimental food because
their cellulose constituent may closely approximate the physical constancy of chitin,
t h e s t r u c t u r a l component of insect exoskeleton.
The frugivorous species used in this study
chews its foods more coarsely than do the
more insectivorous ones. The diet of Cheirogaleus medius in the wild is principally fruit and
nectar although they will accept and eat
insects and mammals, a t least in captivity
(Petter, '62). Judging from stomach contents,
Zhpaia glis eats a variety of insects as well a s
some fruit (Medway, '66). Galago senegalensis
appears to be much more insectivorousinsect fragments were found in abundance in
all stomach contents of wild collected specimens examined by Haddow and Ellice ('64),
although vegetable matter was also present.
Booth ('60) confirms that they eat mainly
insects.
Why should insect-eaters chew their food
more finely than comparably sized fruiteaters? Our proposed explanation requires a
review of some factors of carbohydrate digestion.
Vegetable substances may be divided into
two fractions, t h a t contained in cell walls and
that in the metabolically active part of the
cell (Van Soest, '66). Cell contents (mainly
lipids, sugars, organic acids, starch, nonprotein nitrogen, soluble protein, and pectin)
are virtually completely and rapidly digestible by mammals as are some cell wall constituents such as attached protein. Some additional cell wall constituents are undigestible
in mammals: lignin, lignified nitrogen compounds, keratin and silica (Van Soest, '66).
Finally the digestibility of the hemicellulose
and cellulose component of the cell wall
depends on the presence of intestinal microorganisms capable of producing the appropriate
enzymes (Van Soest, '661, and varies according to the physical and chemical environment
for digestion, the length of the period of time
allowed for digestion, and the relative surface
area to volume ratio of the ingested food particles (McLeod and Minson, '69).
The importance of food particle size for
digestibility is illustrated by data abstracted
from the work of McLeod and Minson (fig. 2).
They show that: As food particle size is decreased, digestion is speeded and the total
digestibility of the food (related to the percent
of structural carbohydrate) increases slightly.
19
CHEWED FOOD PARTICLE SIZE
ultimate digestibility:
2
particle
i size(crn1
0
Fig. 2 The effects of food particle size on the rate of digestion. The food particle size is plotted against standardized in vitro digestibility at 48 hours for four plant species. For example, if 0%of food a was digested in 48
hours with a particle size of 2 cm, then 11%was digested in 48 hours with a particle size of 1 cm and 18%with a
particle size of 0.4 cm. Data from McLeod and Minson (‘691.
Plant species: a, Chloris gayana;b, Cenchrus ciliaris;
c, Digitaria spp.; d, Sataria spp. End point or “ultimate” digestibility is taken for 0.4 mm particl size for 72 hours.
The higher the ultimate digestibility of the
food, the less is the effect of reducing particle
size. Foods a and b in figure 2 are 56 and 55%
digestible and the effect of reducing particle
size is quite large. For foods c and d with much
higher digestibility the effect of reducing particle size is much less. Since the ultimate
digestibility of the foods is related to the percent of cell-wall constituents they contain
(Van Soest, ’66) it is clear that reducing the
particle size of foods is a more important factor in digestibility among animals which eat
high cell-wall constituent foods like leaves,
bark, buds and grasses than among those
which eat foods low in that fraction. This suggestion is supported by Walker and Murray’s
(’75) demonstration that leaf-monkeys grind
their foods like leaves, bark, buds and grasses,
more finely than do fruit-eating ones.
Our findings show that insect-eating species more finely grind their foods than fruit
and resin-eating species. Finely grinding
fruits and gums generally low in cell wall
components would not greatly improve a species’ digestive efficiency.
Soft material such as fruits could be
crushed to extract the nutritive elements;
finely subdividing fruit would not be necessary. The low-cusped dentition of a fruit-eater
such as Cheirogaleus medius would be wellsuited t o rupturing plant cell walls without
necessarily reducing particle size. Conversely
we conclude that there must be some constituent of insect bodies, analogous to the plant
cell-wall constituent, which becomes more
digestible when it is more finely ground. We
suggest that that constituent is chitin.
Chitin is a polysaccharide with physical and
chemical properties similar to those of cellulose (Wainright e t al., ’76). Although we know
of no data on the in vivo digestibility of chitin
in mammals, the digestive enzyme chitinase
has been isolated from the digestive tracts of
several mammals including the lorisoid primate Perodicticus potto which eats insects and
is not found in species which rarely feed on
insects (Goffart, ’76; Jeuniaux, ’63). (Jeuniaux considered and eliminated the possibility that the production of chitinase is stimulated by the presence of chitin and retarded
by its absence in the gastrointestinal tract.)
We hypothesize, on the basis of our findings
20
WENDY SUE SHEINE AND RICHARD F. K A Y
and those of Jeuniaux, first, that chitin digestion must occur in many small primates and
tree shrews, and second, that chewing insect exoskeleton more finely increases its
digestibility for small insectovirous mammals.
The subject of dental evolution has always
been a major focus of primate paleontology.
Recently, attention has centered on the interpretation of dental trends in biomechanical
terms and, from this, making inferences about
feeding changes in the past. These interpretations are increasingly being based on studies
of how living animals move their teeth, how
forces are transmitted to food and the
implications of this for the organization of
jaw musculature and tooth shape. Implicit in
all this is that the function of the postcanine
dentition is to break down food, increasing its
surface area and facilitating enzymatic processing. This study, to our knowledge, is the
first of its kind to approach the question of
how the dentition actually alters food particle
size in a controlled experimental situation.
When more of this work is done, i t should be
possible to interpret the selective factors
which have influenced dental evolution.
ACKNOWLEDGMENTS
This work was supported by NSF Grant GS43262 to Richard F. Kay.
LITERATURE CITED
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Haddow, A. J., and J. M. Ellice 1964 Studies on bushbabies
(Galago spp.) with special reference to the epidemiology
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521-538.
Hylander, W. L. 1975 Incisor size and diet in anthropoids with special reference to Ceropithecidae. Science,
189: 1095-1098.
Jeuniaux, C. 1961 Chitinase: an addition to the list of
hydrolases in the digestive tract of vertebrates. Nature,
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1963 Chitin et Chitinolyse. Masson, Paris,
180 pp.
Kay, R. F. 1973 Mastication, Molar Tooth Structure,
and Diet in Primates. Ph.D. Thesis, Yale University.
375 pp.
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of Teeth. P. Butler and K. Joysey, eds. Academic Press,
London, in press.
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Arboreal folivores with special reference to Primates and
Phalangeroidea (Marsupialis). In: Arboreal Folivory. G.
G. Mongomery, ed. Smithsonian Inst. Publ., in press.
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in the in uitro digestibility of tropical grasses. J. Brit.
Grassland Sw., 24: 244-253.
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Tioman and Pulau Tulai, Part 2, the mammals. Bull.
National Mus. Repub. Singapore, 34: 9-32.
Petter, J. J. 1962 Recherche3 sur I’kologie e t l’ethologie
des lemuriens Malagaches. Mem. Mus. Hist. Nat. (Paris),
Ser. A: 1-146.
Rosenberger, A. L., and W. G. Kinzey 1976 Functional patterns of molar occlusion in platyrrhine primates. Am. J.
Phys. Anthrop., 45: 281-297.
Van Soest, Peter 1966 Nonnutritive residues: a system
of analysis for the replacement of crude fiber. Jour.
A.O.A.C., 49: 546-551.
Walker, P., and P. Murray 1972 Particle size of stomach
contents a s an indication of energy expenditure proportioning in feeding-foraging activities of selected
Anthropoidea. (Abstract). Am. J. Phys. Anthrop., 37:
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1975 An assessment of masticatory efficiency in
a series of anthropoid primates with special reference to
the Colobinal and Cercopithecinal. In: Primate Functional Morphology and Evolution. R. Tuttle, ed. Mouton,
Hague, pp. 135-150.
Wainwright, S. A,, W. D. Biggs, J. D. Currey and J. M.
Gosline 1976 Mechanical Design in Organisms. Wiley,
New York, 423 pp.
Zingeser, M. R. 1973 Dentition of Brachyteles arachnoides with reference to Alouattine and Atelinine affinities. Folia Primat., 20: 351-390.
Note added in proof: Recently we developed a technique which allows us t o sample stomach contents directly, without harm to the animals. Subjects were
subdued with a small dosage of Ketamine. A flexible tube was passed orally into the stomach. A small volume of water was introduced into the
stomach via the tube, and the stomach contents were withdrawn by exerting gentle pressure on a syringe attached to the free end of the tube.
Our results indicate that the average length of carrot particles is not
significantly altered by the gastrointestinal tracts of the species studied
here. Carrots recovered from the stomachs of G. senegalensis have a mean
particle length of 0.44mm, compared with a mean of 0.67mm in fecal particles. The two lengths are not significantly different.
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