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Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet

01 Dec 1980-Journal of Morphology (J Morphol)-Vol. 166, Iss: 3, pp 337-386
TL;DR: Three categories of dietary adaptation are recognized according to the distinctive structural and biochemical features of animal matter, fruit, and leaves respectively, and the predominance of only one in the diets of most species.
Abstract: Three categories of dietary adaptation are recognized--faunivory, frugivory, and folivory--according to the distinctive structural and biochemical features of animal matter, fruit, and leaves respectively, and the predominance of only one in the diets of most species. Mammals subsisting mainly on animal matter have a simple stomach and colon and a long small intestine, whereas folivorous species have a complex stomach and/or an enlarged caecum and colon; mammals eating mostly fruit have an intermediate morphology, according to the nature of the fruit and their tendency to supplement this diet with either animal matter or leaves. The frugivorous group are mostly primates: 50 of the 78 mammalian species, and 117 of the 180 individuals included in this analysis are primates. Coefficients of gut differentiation, the ratio of stomach and large intestine to small intestine (by area, weight, and volume), are low in faunivores and high in folivores; the continuous spread of coefficients reflects the different degrees of adaptation to these two dietary extremes. Interspecific comparisons are developed by allowing for allometric factors. In faunivores, in which fermentation is minimal, the volume of stomach and large intestine is related to actual body size, whereas these chambers are more voluminous in larger frugivores and mid-gut fermenting folivores; fore-gut fermenters show a marked decrease in capacity with increasing body size. Surface areas for absorption are related to metabolic body size, directly so in frugivores; area for absorption is relatively less in larger faunivores and more in large folivores, especially those with large stomachs. Indices of gut specialization are derived from these regressions by nonlinear transformation, with references to the main functional features of capacity for fermentation and surface area for absorption. These are directly comparable with the dietary index, derived from quantitative feeding data displayed on a three-dimensional graph, with all species within a crescentic path from 100% faunivory through 55--80% frugivory to 100% folivory, perhaps illustrating, at least for primates, the evolutionary path from primitive insectivorous forms through three major ecological grades.

Summary (2 min read)

COMPARATI VE ANATOMY 0~' T il E GASTRO-I NTESTINAL TRACT

  • Variation in h istological s tructure effects divisions into stomach , .~mall intestine (duodenu m, jejunum, ileum), and large intestine (caecum and colon).
  • The latter are made from relaxed guts immersed in wate r a nd positioned io s how the ma in featu res clearly; a complete reconstruction , impossi ble by photograph, is ach ieved by moving parts of the tract wh ile drawi ng, and adjusting the d imensions of each region after dissection and meas urement.

Frug iuores

  • All frugivores supple ment thei r diets wit h varying a mou nts of insects and/or leaves, but have no distinctive st ructural specialization in the g ut, al thoug h its morphology may show considerable vari ation between species.
  • Among a rtiodactyls, the pigs have a stomach that is clearly di vided into zones, and in some cases into compa rtments; they have an especially long sma ll intestine, a IMge caecum, and a relatively complex colon, so that the whole tract is about 20 times body length.
  • Ma rmosets show some elongation of the fundus, whereas those of cebids are more specia lized with a globular fundus, conical body, a nd cyli ndrical pylorus.
  • 6l, Lemur, a nd callitrichids, a nd cebids and most cata rrhines otherwise have three, except for gibbons with fow <H ill , '58).
  • The capacious colon of gibbons <Fig. 10) is ind icative of consideta ble leaf co ntent in the diet and its potent ia l for ferme ntation.

Folivores

  • Sirenia ns, such as the dugong, ha ve a complex two-ch a mbered stomach, with one part fulfi lling the role of the duodenum ; t hey a lso have a very wide caecum (Grasse, '55) .
  • The stomach leads into a long intesti ne with a wide caecum.
  • These sa cculations are produced by the reduction of longi tudinal muscle into two or more bands (taen ia).
  • The artiodactyl ruminants are well known for their fo ur-chambered stomach (Comline et al. , '68) , which is dominated by the vast rumen, divided into dorsal and ventral sacs by muscular pillars, and covered by kera t inized sq uamous epithelium with papillae of varying size and shape (Fig. 16 ).

Methods

  • One-hundred forty-eight specimens were caught in their natura l habitat by hun ters dur ing pes t cont rol opera t ions or by local people for food; 29 a n ima ls, mos tly pr imates, died in captiv ity, from illness or old age.
  • Specimens were weighed intact, which was not a lways possible in the fie ld, and their lengths were measured from bregma to ischium a nd from tip of nose to base of tail.
  • Upper left, t he stomach (part1ally d1stended w1th wat er) displayed to show the large sac, the gastr ic tube (on t he n ght), and the pylorus (lower left).
  • Thus, volumes have been recalcu lated along these lines <Table 4), yielding values one-third less on average.
  • The categories of "fa univore," "f1 ug ivore," a nd "fo livore" a re esta blished a ccord ing to str uct ural disconti nui ties, and at this stage they can be no more tha n suggest ive of diet.

CO EFFICIENT of GUT DIFFERENT IATI ON

  • Nevertheless, these crude a rcal measures seem to prov ide the best ind icators of dietary ada ptation.
  • Correlations within each g rou p, however, a re less close tha n in the analys is of volumes, and ca lcula tion of the 95'# confidence interva ls produces extens ive overla p between the difTerent regression lines.

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CHIVERS D.J. & HLADIK C.M. (1980) Morphology of
the gastrointestinal tract in primates : Comparisons with
other mammals in relation to diet. Journal of Morphology,
166 : 337-386.
Flattened pieces of intestinal tract
in a dissecting tray, for the actual
measurement of mucosal area.

338
DAVID
J.
CliiVERS
AND
C.
M.
HLADIK
'67) showed
intere
s
ting
relation
ships
among
p
rimates,
but
data
on
diet
were st i
ll
inade-
tjuate.
Our
aim
s in
this
paper
arc
I l to
de
scribe
var
i
ous
fea t
ure
s
of
gut
moq
>
ho
l
ogy
with
g
reater
pr
ecision
and
quantificntio
n,
21
to
pre
sent
da
tn from
our
field
and
labor
atory
studies, 3) to account
fo
r
allomet
ric factors in
the
discu
ss
ion of intcrspecific differences,
an
d
4 l
to compm·c
these
dat
n
on
morpholo
gy
wi
th
what
is now
kn
own nb
out
the f
ee
ding ecol
ogy
of
the
spec
ies concerned.
The
com
bination
of
data
on
pr
imates
wi
th
tho
se on domestic
and
othe
r
mamm
als is use-
ful, becau
se
it
allows n g
roup
of closel
y-related
species
with
considcrnble di
ctnry
fl
exibility to
be con
tra
sted
with
others
which h
ave
become
hi
g
hly
specialized for
mark
edly differ
ent
di
ets.
While
the
st
ru
c
ture
of
the
gastro-intestinal
tract
is f
ai
r·l
y homogeneous
nmong
the
differ
-
ent or
der
s
of
mamm
als,
there
have
been
pm·
-
al
lel
d evelop
m
cnL~
of
different
par
ts
of
the g
ut
in
various
evol
ut
i
onary
lineages.
These
re
fl
ect
ada
p
tations
to differe
nt
food
s, which
can
be
classified
into
t
hr
ee major groups, according
to
str
uctur·e
and
biochemical co
mp
osition, a nd
the
r
es
ultin
g
di
ges
tiv
e r
equir
eme
nt
s:
1>
"
An
i
ma
l
matt
e r
,"
incl u
din
g
inverte-
brates,
fish,
and
other
small
vertebr
·ates
from
the
secon
dar
y production
of
t
he
ecosystem,
which
pro
vide sources
of
protein
and
fat
th
at
a re
eas
ily digested a nd, therefore, require a
re
l
ative
ly
sho
rt
and
simple g
ut.
21
"
F'
rui
ts," incl uding
um
·i
pe (e.g., flowers)
and
ripe (
fl
eshy) pm·ts, seeds,
an
d tubers -
most ly
the
reprodu
ct
ive p:u ts
of
pl
ant
s -
which
<We
fo
ods
contain
ing short-cha in
sugars
that
are
hydrolyzed
r-ap
idly in
tracts
of
lar
ge
inte
s
tina
l
area
fo
r
rapid
abso
rption and im-
medi
ate
use.
3)
"
Leave
s,'' i
ncludin
g young
and
matur·c
leaves,
grasse
s,
ste
m
s,
as
well
as
ba
rks and
gums - the
vegetative
pa
rt
s
of
plants
- which
a rc foods us
uall
y containing
pr·
o
tein
and
long-
chain
suga
rs
that
require fer·mentation in
an
enla rged stomach
or
large
inte
s
tine.
According to
the
predominant
item
s co
n-
sumed,
thre
e categories
of
diet
ary
adaptation
may
be
recognized, a
nd
in
th
is
pape
r
they
a re
ref
erred
to
hereafter
as
(aunivore, {rugivore,
and
(olivore
respect
ively (recognition
of
insec-
tivore,
camivo
re, and herbivor·e, wi
th
their
taxonomic
and
ot
he
r conn
otation
s,
contr
i
bute
s
littl
e to
thi
s ana ly
sis
).
Th
ese categor·ies rep-
re
se
nt
a g
rada
ti
on,
for a
gene
r
alize
d
mam
mal,
from
food
s
that
a re rel
ative
ly difficult
io
col-
lect
but
ea
sy to dige
st
(
prey
),
th
r
oug
h
th
o
se
av
ai
lable in limited
qu
a n
tity
(f
ruit), to t hose
t
ha
t
are
widely
ab
und
an
t
bui
rela
tiv
ely
diffi-
cult to di
gest
(leaves).
He
nce
the
need
fo
r
marked
diff
ere
ntia
ti
on
of
feeding
st
r
ategy
a nd
gui
morphology. A
class
ification in
term
s
of
three
di
eta
ry
grades
(H
iadik
, '7
8al
,
wi
th
ap-
pr·opri
ate
subdivision
s,
allows
greate
r
fl
exibil-
ity, a nd
seems
to
re
p
rese
nt successive evolu-
ti
onary
stages
of
greate
r
admixture
of
the
diflerent
types
of
foo
d.
COMPARATIVE ANATOMY
0~'
T
il
E GASTRO-
INTESTI
NAL
TRACT
The
structure
of
the
wall
of
the
gasir
o-
in
-
testi
nal
ira
ci
fo
llows a
pattern
common to all
verte
b
rates
:
the
i
nn
er
li
nin
g
of
mucous mem-
brane
is
se
parate
d
by
conn
ective
ti
ss
ue from
a n
oute
r cyl
inde
r
of
ai
l
eas
t two la
ye
rs of
mu
scle.
Variatio
n in histological s
tructur
e
ef
-
fects divisions into stomach,
.~
mall
int
es
tine
(
duode
num,
jejun
um, il
eum),
and
large intes-
tine (
caecum
an
d colon). Bri
ef
ref
erence wi
ll
be
mad
e to
va
rious
co
nfig
ur
ution
s
of
the
mu-
cosa a nd
unde
rlying connec
ti
ve
ti
ss
ue
, which
apparently
assist
di
ges
tion mechanically, by
m i
xing
or slowing the p
assage
of
food
or
by
in
creasi
ng
the
surface ar
ea
for
dige
stion
an
d
ab
so
rption, e.g.,
pa
pi
llae
,
rugae
tfold
sl,
ha us-
trae
<sacc
ulation
sl,
villi.
In this section
we
s
hall
try to identify tho
se
str
ucture
s
re
l
ating
to each
of
ihe
three
main
diet
a
ry
ad
aptations
by
sup
pl
em
enting
pre
-
vious knowledge
with
new
observations.
Th
e
latt
er
ar
e
made
from
relaxed
gut
s i
mmersed
in
wa
ter and pos
it
i
oned
io
show
the
ma
in
featur
es
cl
ear
ly; a c
om
pl
ete
recon
st
ru
ct
ion,
impossible by photog
ra
ph, is achieved by mov-
ing
pa
r
·t
s
of
th
e
tract
wh
ile
drawi
ng,
and
ad
ju
s
tin
g
the
di
men
sions
of
each
reg
i
on
after
dissection
and
meas
urem
e
nt.
Fauniuores
The
ba
s
ic
pattern
of
gut
st
ru
ctu
re
among
faun
ivores consists
of
a simple glob
ular
sto
m-
ac
h,
tortuou
s s mall i
nte
sti
ne, s
hort
conical
caec
um,
and
si
mple smooth-walled col
on
.
Thi
s
pattern
is exhibited by
pr·
i
mates
feed
in
g
main
-
ly
on
inverteb
r
ates,
such
as
Arctocebus (Fig.
1), Lori
s,
and
Tar
si us.
ln
other
mam
mals
ther
e
may
be s
tr
uc
tur
al
speciali
zat
io
n in one direc-
tion
or
an
oth
er.
The small
est
ma
mma
l
ian
gut
known is
fo
und in
the
insectivorous
bat
,
Rh
in
-
opom.e;
it
s
tract
is
on
ly four
·-
fifths
of
body
l
ength
(G
ra
sse, '55
).
Simp
lification
of
the
gut
is ext
reme
in
haemoph
ago
us
bats,
such as
De
smo
du
s,
with
the stom
ach
as
a blind-en
din
g
tu
be
, a
very
short colon, and no caecum. Such
G 'I'
~IOI!PIIOI.OGY
Ai\llDIET
I
~li\~ 1\
I
AI.S
339
redu
cti
ons
are
clear
ly
specia
lizations,
rath
er
th
an
represe
ntin
g t
he
primitive con
dit
i
on
.
Sp
ecia l
izat
ions
of
faun
ivores m
ay
also in-
vol
ve
the
stomach. Some
ani-eating
edent
aL
es
a lso lack a caecum
an
d
th
e
gu
t is
on
ly
seven
time
s
bo
dy
le
n
gth,
but
t
he
sto
mach
co
ntains
a "musc
ular
tooth"
compensating
fo
r
the
lack
of
ora
l
teet
h <
Gra
sse,
'55
).
A s
im
ilar
muscul
ar
specialization is f
ou
nd
in
pholidotcs, such
as
the
termite-eating
pangolin, Manis
(F'
ig.
ll,
s
upp
l
emented
by a
keratinized
area
in
the
pylorus
and
by
the
pr·esence
of
small
stone
s.
Fig.
l.
Gas
tr
o.
in
tcst.inal_ t
rac~
.
of
faunivores, drawn by C.M
.H.,
with accurate scaling of proportions,
main
blood ve
ssels
t.o
show the
d•
spos
1Uon
of
m
esenter
i
es
,
and
convent
ional
shad
in
g
of
lhe
different
morpho
l
o~,
~
cal
~eat.ure
s
.
The angwanttbo,
Ar
ctocebus calabare
ns
is (Specimen
FC,
see
t.ab
le 5) is o
ne
of
the
most unspecia
li
zed
m
term
s
of
morpho
lo
gy.
The
pangolin, M
a11i
s giga11tea I specimen MR,
juve
nile)
is
presented below with
an
open stomach
to
show t
he
muscular ''tooth:''
the
arrow marks the junction
of
il
eum and
co
lon determined
from
microscop
iC
e
xaminatio
n
or
lhe
mucosal w
all
; l
he
extreme l
engt
h
of
lhe
small
inlesli
ne did 'n
ot
a
ll
ow i
tlo
be
drawn
completely unfolded,
as
in
ot
her
dr
awings.

340
DAVID J . CHIVERS AND
C.
M. IILADIK
Ln
cetaceans the stomach
ha
s tht·ee main
compar
tments
(
Harri
son
et
al., '
70
).
Th
e first
and
la
rgest is covered
by
folds
of
th
ic
k,
ke
ra-
tinized ep
it
he
lium
,
the
second by
sp
ir
ally ar-
ran
ge
d folds of
th
ick, gl
andular
ep
ith
elium
(
making
a dit·ect cha
nn
el a l
ong
t
he
le
ss
er
c
urva
tu
re
),
an
d the thit
·d
,
tubu
l
ar
compat·i-
m
ent
ha
s a simple pyloric muco a
an
d str·ong
s
phincten;
at
both
ends, e.g.,
the
porpoise
Phocaerw
CFig.
2
).
The s
mall
inte
stin
e,
start-
in
g from a dil
ate
d
duodenum
, is
very
l
ong
(about 1
500
cm
l;
the
t·e is no caecum a nd a
very s
hort
colon (only 10 cm, identified u
nd
er
th
e dissecting microscope by
th
e
abrupt
tran-
sition from vill i to
crypts
).
In
the lnscctivora the sim
pl
e s
tomac
h is
followed by a very s
hor
t small
inte
s
tine
and,
usuall
y,
no caecum- as i
ll
u
stra
ted by Polo·
mogale Wig. 3l, which is
ad
a
pt
ed f
or
feed
in
g
on
fres
hwater
fi
sh
and
cr
u
stacea
ns.
1n
Sorex
the
tr
act
is only 2.6 ti mes body l
en
g
th,
an
d
s
ome
faeces
arc
r
cingc
sted to
permit
a second
oppo
rtun
ity
fo
r digestion. This phenomenon
of
re
fl
ection CCrowct
·o
l
l.
, '
52
) helps to explain
the
re
du
ct
ion in
gu
t size as a
phy
siologicaVbehav-
ioral speciali
za
tion.
1n
one species of Tenre
c,
which
eat
s
foo
ds
ot
h
er
than
insects,
th
e
tract
may
be seven
tim
es
bo
dy l
en
gth.
Tr
ee
shrews,
Tupaia, which also s
upplement
their
inverte-
brate
diet
with
fr
uit,
have
a slightly
la
r
ger
colon
than
other
in
se
c
tiv
ores
and
a s
mall
caecum C
Gra
ss
e, '55). Some rodents subsist on
a
diet
composed e
nt
ir·ely
of
ins
ects
or o
th
er
animal prey.
In
the
African murid Lophuro-
mys,
for example, speciali
zat
ion to such a di
et
includes a c
han
ge
in
the
di
s
tribut
ion of
ga
s
tric
glands CGenest-Vill
ard
, 1968).
Ot
her
mamma
ls, such as s
ome
fee
din
g on
ver
t
eb
rat
es, show no obv ious speciali
zatio
n. ln
fi
ss
ipedes, fot· e
xample,
th
e stomach is simple,
the sma
ll
int
es
tin
e fou r to six
time
s body
len
gt
h,
the
caecum s
mall
or
ab
se
nt,
and
the
colon re
du
ced, as shown in the Viverridae
by
the
African linsang Poiarw !Fig. 3) and
the
mong
oo
se
Atilax
,
and
in
th
e
Fe
lidae by
the
golden cat P
rof
elis
cF'i
g. 4).
The
s
hape,
i
nter-
n
al
features, a nd relative s
i7..C
S
of
fun
dus and
pyl
oru
s vary slightly
among
such
mammal
s,
as
de
scribed by E
ll
enbet·ger a nd
Baum
('21)
and illus
tra
te
d here by
th
e domestic dog,
Can
-
is
!Fig. 5).
Frugiuores
This
grou
p con
tai
ns most
pr
i
ma
te
s,
but
none
of
th
em s
ub
si
sts
en
tir
ely on fruit. All f
rug
i-
vo
res s
up
pl
em
en
t th
ei
r
diets
wit h
varying
amoun
ts
of insec
ts
and/or le
ave
s, but have no
dis
tinctive
str
uctural
spec
ia
li
zatio
n
in
the
gut,
al
though
its
morphology m
ay
show cons
ider
-
ab
le vari
at
ion
between
species.
Some
Car
nivora also
have
thi
s mixed
diet
,
but
r
etai
n
the
st
ructur
al fe
at
ur
es
of
fauni-
vore
s,
e.g., t
he
palm
civet
Nandi
nia
feeds
heavily
on
fruit
(Cha
rle
s-Dominiq
ue
, '78),
bu
t
h
as
no caecum and a
red
uced colon
CFig
. 6).
Myoxid
rode
nt
s al
so
have
no c
ae
cum
<
Gra
s
se
, '55), a
nd
their
pred
atio
n on birds,
as
a s
upplement
to seeds and fruit,
pla
ces
them
on the
border
between
fa
uni
vo
res and fmgi-
vores. In
the
st
om
ac
hs of cr
icet
ine rode
nts,
the
fundus a nd
en
larged
car
dia!
gla
nd
reg
ion
vary
in
th
ei
dim
ension
s,
sepa
rat
ed by a fold
of
varyi
ng shape (
Carleto
n ,
'73
).
In
f
ru
givorous
ba
ts
the
sto
mach is rel
at
ively complex,
wit
h
a distinct
ca
r
dia
! r
eg
ion, a long pyl
or
ic
diver-
ticulum
fo
lded back on itsel
f,
an
d a la
tera
l
"caec
um
";
the
tru
e
caecum
is
pr
esent
in sev-
er
al
ge
nera (G
ra
sse, '55).
Among a rtiodactyl
s,
th
e pi
gs
h
ave
a
sto
m-
ach
th
at is cle
ar
ly di
vi
ded
in
to zones,
and
in
some cases i
nto
compa
rtm
ent
s;
they
ha
ve
an
especially l
ong
small in
te
s
tin
e, a I
Mge
cae-
cum,
and
a
relatively
complex colon, so
that
the
whole
tract
is
about
20
time
s body len
gt
h.
These
elaborations •·elate to the inclusion
of
mots
and
ot
her
vegetative
par
ts
of
plants
in
th
eir di
et.
Gut
str
ucture
is more homo
ge
neo
us
among
fru
givorous
pr
im
ate
s (Figs. 7, 8, 9). The
sto
m-
ach is
essentia
lly simple a nd globular in
struc
-
ture
(Hill, '58). Marmos
ets
show some elon-
gation
of
the
fundus, wh
erea
s those
of
cebids
are
more specialized
with
a gl
obula
r fundus,
co
ni
ca
l
bo
dy, and cyli
ndri
cal pylorus. Alouat-
ta
, wh ich also
eats
man
y l
eave
s
C4
<YY
o
of
diet
by
weight
, Hla
dik
and
Hl
adik,
'69), shows
the
g
eate
st complexity,
with
a capacio
us
gl
obula
r
s
ac
, na rrowing towards
the
ben
t t
ubu
l
ar
py-
l
ow
s,
which is
gu
arded by s
tron
g pillars;
ru-
gae
radi
ate
from
the
cardia
and
ru
n longi
tu
-
dinal
ly
within
the
body. Ateles, which is one
of
the
most frugivorous a
nd
swallo
ws
many
stones,
ha
s a n e
nlat
·ged J -shaped stom
ac
h.
Old
World
pr
im
ate
s,
other
than
colobine monke
ys,
h
ave
a s
in
gle smooth-walled sac;
amo
ng
the
a pes
it
is
mor
e
globular
and
man-li
ke
in gib-
bons, even m
ore
globul
ar
in
gor
illas, and more
el
ongated
in c
himp
anzees
and
or
a
ngutan
s
(Hill, '58).
Th
e duo
denum
is commonly C-s
haped
,
in
cont
rast to
th
e
elongated
U-s
hape
of
other
ma
mm
als; in s
ome
ce
bid
s a nd all
catarrh
ines
it is
rett
·o
pe
riton
ea
l.
Th
e caecum is l
ar
ge
in
frugivorous
pro
simians, s
hort
an
d wide
in
GUT
\IOili'II
OI.OGY AND
DII
·:
T I
~11\
,
\
1
~1
1\
I.
S
3
41
marmosets,
and
hook-s
hape
d
in
cebids; in ca-
ta
rrh
ines
the
base is globulat·,
the
body sho
rt
and c
apac
iou
s,
and
the
apex
blu
nt
a
nd
conical,
wi
th
a
te
rmin
al
ven
n iform appendix in hom-
inoids IHill '58!.
Th
e colon is simple and s
trai
g
ht
in cebids
such as
Saimi
ri;
there
is a tt·ansvet
-s
e colon in
Cebus
an
d Aotus, and a r
ight
colon as wel l in
C
a/lic
ehus, Cacajao, and Pithecia.
Furth
er
elongation
(a
nd folding) occurs in callitrichids,
Logolhrix, a nd a ll
ca
ta
nhine
s <Hill, '
58
).
T
aenia
coli (redu
ct
ion
of
l
ongitudina
l muscle
into
band
s) m·e lac
kin
g
in
Saimir
i, Cebus, a
nd
most pros
imian
s, but
there
may
be one
or
tw
o
in
Nycti
cebus, Perodicticus
CFi
g. 6l, L
emur
,
and
callitr
ichids, and cebids
and
most
cata
r-
rhine
s
otherwi
se
ha
ve
thr
ee, exce
pt
for gib-
bons
with
fow· <Hill, '58
).
The ansa coli loop
in
the
tran
sve
se
co
lon is common
in
prosi-
mian
s <Pig. 6l;
this
pa
rt
of
th
e colon is
al
so
l
on
g and
dependent
in
ape
s.
The
capacious
co
lon
of
gibbons <Fig. 10) is indi
cat
ive
of
con-
side
able leaf con
te
nt
in
the
diet
and
its po-
te
ntial f
or
f
er
me
ntat
ion.
Fig. 2
..
Th
e _compound s
tomac
h
of
the h
arbor
I
>Orpoi
S(l,
Pl
wcae
na
p
lr
ocaena
(035
), is shown open a nd
flaU
.e
noo m a d1s
sect
mg t
ra
y.
The
oesophagus (cent.er) le
ad
s
right
into
the
fi
rst
compartment
, which in
tu
rn
opens
mto
the glandular c
hamb
er
<lo
wer
);
the
fi
rst s phincter, 01
>e
n
ing
into
t
he
pyl
oric
tu
be, is just
vi
sible
Oo-:ve
r
centc
rl l
ea
dmg up to
the
pyloric sphin
cte
r and thence into the duodenal dive
rt
iculu
the
mu
co
sal folds
wh1ch
~un
the
_l
ength
of
t
he
intestine,
ca
n be seen (upper left
).
Photo by D.J.C. and D
epartmen
t
of
Anatomy'
Ca
mbr1d
ge
Umver
sty. '

342
DAVIO J . C
l-l
iVERS AND C. M.
II
LADI K
Fig.
3.
Gas
tro-
intc
stinal
tract
of
Potamogale velox (
MXJ
presented
as
in
Figu
re
I ,
with
the
arrow
ma
rking
the
jun
ct
ion
of
small i
nte
st
ine
and
colon. In Poiana riclwrdsoni (MS), to
th
e r i
ght,
the
limit
of
t
he
colon is
cl
early
marked
by a s
hort
caecu
m.
Dr
awin
gs
by
C.
M. H.
Fig. 4. Gas
tro
-
in
tcs
tinal
trac
ts
of
Atilax paludinosus (
MW
) and:
on
the right: Profelis aurata (
MZ
). Draw
in
gs
by
C.M.H.
GUT
MOR
PH
OLOGY
AN
D D I
ET
IN
MAM
M A LS
343
Fig. 5. Internal view
of
the
sto
mach
of
t
he
domestic d
og
, opened
arou
nd
the
greate
r cur
vature
, showing
the
oesop
hageal
o
pe
nin
g
intac
t
(at
top), the
exten
sive folded fu n
dic
region,
and
the
p
aler
pyloric region (lower).
Ph
oto by
Department
of
Anatomy, Cambrid
ge
Un
iversity.
Folivores
Th
e long-ch
ai
n
!3-l
inked
car
b
ohydrates
pre-
do
minant
in
the
leaves, grasses,
stems,
bark
s,
and
gums
co
nsumed by
th
ese
an
ima
ls req
uire
consider
ab
le d
eg
ra
dation
by sy
mb
iotic micro-
bi
al
or
ganis
ms. The m
ost
conspicuous adap-
ta
tions
are
chamb
ers for t he
bacte
rial fermen-
tat
ion
of
cellulo
se
a
nd
f
or
the
abs
or·
ption
of
v
olat
i
le
f
at
ty acids and
othe
r
metabolit
es,
ei
the
r in
the
stomach or in the l
arge
in
testi
ne.
Th
is dichotomy
might
mask
f
urt
her diversifi-
ca
ti
on
as
shown by the expansion
of
the rig
ht
colon
as
well as,
or
instead
of, the caecum,
the
presence
or
ab
se
nce of
cae
c
ot
rophy, and var
i-
at
ion
in
stomach
struct
ure.
T
he
la
rg
e i
nt
esti
ne is
enlar
ge
d
in
th
ose
p
r·osi
mian
s which f
ee
d
on
leave
s
or
gu
ms.
ln
Lepil
emur
a mechani
sm
similar to refection
(
se
e above) allows efficient u
se
of
a
diet
very
high
in
fiber con
te
nt
(Hl
adik
and
Charles
-
D
omini
qu
e,
'
74
).
Th
is c
ase
of
caecotrophy is
un
i
que
among pri
ma
tes, a nd helps to
exp
la
in
why the
small
int
est
i
ne
is
one
of
the
s
hor
test
among
mamma
ls (Fig. 11
).
An
equally
elon-
gate
d and coiled caec
um
is found in Phaner
and
E uoticus. Since gums r·equire
fermenta-
tion for d
igest
i
on
they
ar
e classified
with
fol
-
iv
or
es, a l
ong
with
lndri, which shows s
im
il
ar
f
eat
ur
es (Fig. 11) a nd
is
a tr
ue
folivore.
Th
e
rabb
it provid
es
the
classic case
of
cae-
cotrophy (Mor·ot, 1
88
2;
Ta
ylor,
'4
0).
ln
!ago-
morphs
and
myomor
ph
rod
ents
some faeces
are
r·eingested
after
fer
men
t
ati
on
in
t
he
ca
-
pacious caecum, so
that
metab
olites
from
the

344
0
1\
VIO
J.
C
HIVER
S
AND
C.
M. H
LADI
K
Fig
. 6.
Ga
sL
r
o-i
ntc
stinal Lracts of frugivores.
On
_
the
le
ft.
. fr
om
Perooicticus
poll~
(FM), a frugivorous
pro~hnian
feed
i~g
pa
nl
y on a
nim
al
matLe
r.
On
t
he
righ
L,
Lh
c palm covet, Nandrma bmotata (MY)
os
a
car
mvore feedmg ma
on
ly
on
fruot,
lac
kin
g a caec
um
.
Lhe
ju
ncLion
of
colon
and
small inLcstinc is
marked
by
an
a
rro
w.
Oraw
mgs
by
C.M.II.
herbivorous d
iet
can be absor·bed
in
the
small
in
test
ine.
Th
e caecum is very coiled and el
on
ga
ted in
sp
ecia
lized folivorcs, s
uch
as
th
e
"g
liding"
squirrel
An
omalu
rus
<Fig.
Ill
-e
ven more so
than in
Lepilemur.
Th
e most complex lar
ge
intestine
is found
in
D
endrohyrax
<F
ig. L
2l,
wh
ere
the
fi
r
·st
caec
um
is followed by two more
after
about
20 cm of colon.
With
en
lar
·gement
of
the
colon in ma
mma
ls
the
mig
ati
on of the ileo-caeco-colic
junction
can be traced from
th
e l
eft
cran
ia
l pa rt
of
the
abdominal
cavity
round to
the
right c
audal
as
pect
, so
th
at
th
e
caecum
comes to poi
nt
caudall
y r
ather
than
c
rani
ally (Hill, '58). ln
tho
se
speci
es
with
a
vo
l
uminou
s caecum, how-
ever, cr·ani
al
rotat
ion
ha
s occurred so t
ha
t
it
comes to occ
up
y the
ventra
l p
art
of
the
abd
o-
men, as in the hor
se
(
Fig
. 13). Peri
ss
odactl
ys
an
d proboscids
have
l
ar
ge
co
lic loops in addi-
tio
n to
th
e hu
ge
sacc
ul
ated
caecum for
the
br
ea
kdown
of
their fibrous
diet.
As
in
other
mamm
als which
co
pe
with
this kind of di
et
,
the
hor
se
h
as
a
lar
ge
ar
ea
of
keratini
zed
epit
heli
um
in i
ts
st
omach, which, h
owever
,
r·emains s
imple
(Fig. 14
).
Car
leton ('73) sug-
gests
th
at
the
va
r
ia
ble
co
m ification
of
th
e
stomach lining in
diff
erent species
of
cricetine
ro
dent
s might be
co
rr
elated with
the
amou
nt
of
cellulose
in
the
di
et.
ln
co
ntr
ast
to
peri
ss
od
acty
l
s,
proboscids
ha
ve a
la
r
ge
fo
lded stomach
and
a s
hort
small
in
tes
tine
of
lar
ge
interna
l ar·ea.
Siren
ian
s,
such
as
the
du
gong, have a complex two-cham-
b
ere
d
st
omach, with
one
part
ful
fi
lling
th
e
role
of
the
duodenum
; th
ey
also h
ave
a
ver
y
wide caecum (
Gra
sse, '
55
).
Th
e most el
aborate
tr
ac
ts are f
ound
in tho
se
folivores, usua lly s
ub
si
sti
ng a lmost entirely
on grasses,
wi
th
co
mplex s
tomachs
for bacte-
GUT
J\ IO
I!
I'IIOLOCiY
AN
D D
IE
T I
'I/
~
I
AM~IA
I
.S
345
Fi
g. 7 Gastro-
in
testmal
tracts
of
fr
ug
iv
oro
us monkeys. Above,
the
mangabey
Cercocebus
a/brgena
oFF, Juveni
le
),
an
d below,
the
gue
n
on
Cercopithecus cephus
CF
Dl.
Dr
awings by C.
M.H
.
ria
l ferment
at
ion,
as
exempli
fi
ed
by
th
e a r-
tiod
actyl
rum
ina
nts. Mac
opod ma
supi
als,
so
me
edentate
s,
hippopotami,
ca
mels, and co-
lobine m
onke
ys
show evol
ution
ary
conver-
ge
nce with ru
minants
in the ir ada pt
ati
ons
of
sto
mach
st
ru
cture
fo
r folivory <Moir, '68
).
ln
th
ese
gro
up
s
th
ere
is
act
ua
ll
y a
co
nt
i
nuum
of
diets
from frugivore to foli
vo
r·e,
as
shown
in
the
pr
ece
din
g
sect
ion for pi
gs
and peccari
es
!who
se
stom
ach
s show some s imil
ar
i
ty
to
those
of
r
uminan
ts).
Among
the
ruminant
s,
fo
r
example,
there a re
pur
e fr
ug
ivores, such
as
Cephaloplws
and H
yemoschus
(
chevrotain
),
in
te
rme
dia
te
typ
es
such
as
the
spotted
de
er
Ax
is, a nd p
ur
e fol iv
ore
s,
such
as
Neotragus, or
p
ur
e
herb
ivores, such
as
the
buffalo S
yncerus
(G. Dubost,
per
s. comm.).
These
extremes
of
the
continuum
are
the
mo
st
specialized forms.
Macropod marsupials
ha
ve a long tu
bular
stomach,
sa
ccula
te
d
alo
ng much of
the
gr
eater

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19 Sep 2004
TL;DR: Finite functions over hereditarily finite algebraic datatypes are used to implement natural language morphology in the functional language Haskell to make it easy for linguists, who are not trained as functional programmers, to apply the ideas to new languages.
Abstract: This paper presents a methodology for implementing natural language morphology in the functional language Haskell. The main idea behind is simple: instead of working with untyped regular expressions, which is the state of the art of morphology in computational linguistics, we use finite functions over hereditarily finite algebraic datatypes. The definitions of these datatypes and functions are the language-dependent part of the morphology. The language-independent part consists of an untyped dictionary format which is used for synthesis of word forms, and a decorated trie, which is used for analysis.Functional Morphology builds on ideas introduced by Huet in his computational linguistics toolkit Zen, which he has used to implement the morphology of Sanskrit. The goal has been to make it easy for linguists, who are not trained as functional programmers, to apply the ideas to new languages. As a proof of the productivity of the method, morphologies for Swedish, Italian, Russian, Spanish, and Latin have already been implemented using the library. The Latin morphology is used as a running example in this article.

380 citations

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Journal ArticleDOI
23 Mar 1973-Science
TL;DR: The model proposed here promises useful answers in comparisons of living things on both the microscopic and the gross scale, as part of the growing science of form, which asks precisely how organisms are diverse and yet again how they are alike.
Abstract: Arguments based on elastic stability and flexure, as opposed to the more conventional ones based on yield strength, require that living organisms adopt forms whereby lengths increase as the ⅔ power of diameter. The somatic dimensions of several species of animals and of a wide variety of trees fit this rule well. It is a simple matter to show that energy metabolism during maximal sustained work depends on body cross-sectional area, not total body surface area as proposed by Rubner (1) and many after him. This result and the result requiring animal proportions to change with size amount to a derivation of Kleiber9s law, a statement only empirical until now, correlating the metabolically related variables with body weight raised to the ¾ power. In the present model, biological frequencies are predicted to go inversely as body weight to the ¼ power, and total body surface areas should correlate with body weight to the ⅝ power. All predictions of the proposed model are tested by comparison with existing data, and the fit is considered satisfactory. In The Fire of Life, Kleiber (5) wrote "When the concepts concerned with the relation of body size and metabolic rate are clarified, . . . then compartive physiology of metabolism will be of great help in solving one of the most intricate and interesting problems in biology, namely the regulation of the rate of cell metabolism." Although Hill (23) realized that "the essential point about a large animal is that its structure should be capable of bearing its own weight and this leaves less play for other factors," he was forced to use an oversimplified "geometric similarity" hypothesis in his important work on animal locomotion and muscular dynamics. It is my hope that the model proposed here promises useful answers in comparisons of living things on both the microscopic and the gross scale, as part of the growing science of form, which asks precisely how organisms are diverse and yet again how they are alike.

1,147 citations

Journal ArticleDOI
TL;DR: The perissodactyls were the dominant medium to largesized herbivores during the Eocene, and in the early Oligocene a reduction in their diversity coincided with the beginning radiations of the ruminant groups of artiodactylS.
Abstract: There are two main groups of ungulates or hoofed mammals living today, perissodactyls and artiodactyls. They are distinguished by a basic difference in foot morphology, which indicates that the two groups arose independently from a basal "proto-ungulate" stock (the order Condylarthra) in the early Tertiary. This difference involves the axis of symmetry of the foot. In perissodactyls it passes through the third metapodial, while in artiodactyls it passes between the third and fourth metapodials. The perissodactyls surviving today are horses, rhinos and tapirs. The recent artiodactyls are a much larger and more diverse group, broadly covering all "cloven-hoofed" animals such as pigs, hippos, camels, deer, giraffes, antelope, cattle and sheep. The perissodactyls must have evolved by the late Paleocene, as by the early Eocene four out of five of the known superfamilies are already distinguishable (Romer, 1966). Artiodactyls are also seen in the early Eocene (Romer, 1966), but the two major groups of ruminant artiodactyls, the tylopods and the pecorans, do not appear in the fossil record until the late Eocene (Gazin, 1955) (see Fig. 1). The perissodactyls were the dominant medium to largesized herbivores during the Eocene, and in the early Oligocene a reduction in their diversity coincided with the beginning radiations of the ruminant groups of artiodactyls. These latter animals were the dominant medium-sized herbivores throughout the remainder of the Tertiary, at least in terms of species diversity. The perissodactyls originated in North America; the origin of the artiodactyls, whether in North America or in Eurasia, is still in question (Olson, 1971). As the rise of the artiodactyls at the Eocene-Oligocene boundary coincides with the decrease in the diversity of the perissodactyls, theories have been advanced to explain this coincidence in terms of perissodactyls being competitively inferior to artiodactyls. One obvious difference between the two groups is the difference in limb morphology. Although the axis of symmetry of the foot seems an unlikely candidate for conferring a selective advantage, artiodactyls do possess a unique double trochleared tarsal or ankle joint. This structure has been regarded as a key feature of the group and contributory to their evolutionary success, on the grounds that it has enabled artiodactyls to achieve rapid acceleration for predator escape (e.g., Schaeffer, 1947; Romer, 1968; Colbert, 1969). While there is little doubt that this particular adaptation was of value to the artiodactyls themselves, I do not think, however, that it had a great deal to do with the relative competitive efficiencies of these two ungulate groups. For a start, this tarsus appeared in a highly advanced condition in the first artiodactyls in the early Eocene (Schaeffer, 1947) long before their radiation and diversification, and is found in noncursorial as well as cursorial forms. In addition, modern ecological work demonstrates that predation is not necessarily detrimental

559 citations

Journal ArticleDOI
Vance A. Tucker1
TL;DR: The minimum cost of transport for various walking, running and flying animals is functionally related to the type of transport and to body weight, and the same functional relations hold for poikilotherms and homeotherms, and for five or more decades of body weight.

352 citations