Comp. BIochem Physiol. 1976, Vol 53A, pp. 123 to 127.

Pergamon Press Printed m Great Br:tain

A COMPARISON OF INTESTINAL AMINO ACID

ABSORPTION IN VARIOUS AVIAN AND
MAMMALIAN SPECIES
JOSEPH LERNER* AND F. H. KRATZER
Department of Avian Sciences, University of Californm,
Davis, CA 95616, U.S.A.

Abstract--I. The intestinal absorption of amino acids in various avian species, the rat and the mouse
was studted by a tissue-accumulation procedure.
2. The orders of initial (one-rain) rates for methionine, lysine, proline, aspartic acid and glycme,
as well as the methionme/lysine, proline/glycine and proline/asparUe acid ratios of rates vaned between
species and within breeds of the domestic fowl.
3. At one extreme, the methionine/lysine ratios were 11'4 and 10.5 in the tinamous and quail, respect-
ively, and 1.46 and 1.92 in the turkey and mouse, at the other
4. Proline/glycine ratios ranged from 1.0 in the chicken, turkey and quail to 2.06 in the mouse.
5. Proline/aspartic acid ratios ranged from I'0 in the chicken, turkey and quail to 3.08 in the mouse.
6. The results are discussed in terms of the current models which assume uptake to be regulated
at the gene level.
7. The observed absorption patterns and ratios probably reflect expression of specific genotypes
found in the various species.

INTRODUCTION (Rattus norvegicus, Sprague-Dawley strain); mouse (Mus

musculus, crossbred strata).
T I E XNTr.STINALabsorption of amino acids in the The tissue handling and manipulations involved in the
domestic fowl and in various mammals has been preparation and incubation of mtestinal segments have
characterized in a number of in vitro studies. Analysis been described (Miller et al., 1974) and were modified in
has been made on the kinetics a n d specificity limits the current study. A portion of intestine on eltber side
of transport, on the ability of various regions of the of the yolk stalk (midgut), except where otherwise noted,
gut to accumulate these nutrients, a n d on develop- was excised and immersed m physiological saline (room
ment of the transport mechanisms with respect to age temperature). The intestine was stripped of mesentery and
of the animal (Miller et al., 1973; Miller et al., 1974; fatty tissue, cut lengthwise and thoroughly washed of
adherent digestive contents. It was then washed in pre-
Lerner et al., 1974). In the present investigation we viously gassed (O2:CO2, 95:5, by vol) physiological saline
have compared the initial rates of amino acid absorp- maintained at 37°C and cut into sections weighing ap-
tion in the intestines of a number of normal strains proximately 50 mg. The sections were individually preincu-
of chickens, in lines possessing inherited metabolic bated in test tubes containing 2 ml of Krebs-Henseleit
diseases, in various avian species, some being close buffer at 37°C. The tubes were fitted with capillary tubing
relatwes within the family Phasianidae, and in the rat (0.048" outer dia x 0.030" inner dia) which served to oxy-
and mouse. The results show that some major differ- genate and mix the buffer. Incubations were performed by
ences occur in absorptive ability even between closely adding 3 ml of Krebs-Henseleit buffer containing L-
[14C]amino acid (New England Nuclear Corp., Boston)
related species, and that differences occur within
and 1 mM unlabeled amino acid to the preincubatlon tube.
strains of a single species. After 1 rain the reaction was terminated by pouring the
tube contents onto a funnel (maintained under suction)
and simultaneously washing the tissue with physiological
MATERIALS A N D M E T H O D S saline. The hssue was then rolled on towel paper and sub-
Maturing or adult ammals of both sexes were used as sequently shaken 1 hr in a 2-ml portion of 2'5% trichloro-
a source of intestinal tissue and were fed standard stock acetic acid. A l-ml aliquot of the clarified extract was
diets. The following species were used: chickens (Gallus assayed for tracer by standard liquid scintillation counting
domesticus) of several breeds which included a Barred Ply- techniques. The extracted gut segments were rolled on
mouth Rock × Rhode Island Red hybrid, Line 200 New towel paper and wet tissue weights were taken. Uptake
Hampshire (control) chickens, Line 304 New Hampshire was expressed in terms of/,moles of amino acid accumu-
chickens with inherited muscular dystrophy, ichthyotic lated per g tissue in 1 rain and was corrected for the non-
chickens, White Leghorn hens, scaleless chickens and day- specific entry and diffusion by subtracting the rate of entry
old chicks (White Leghorn); turkey (Meleagris gallopavo); of 0-6 mM [t4C]/~-alanine in the presence of 100 mM pro-
quail (Corturnix coturnix japonica); chukar partridge (Alec- line. ~-Alanine uptake under these conditions was found
toris oraeca); ring-necked pheasant (Phasianus colchicus); to be nonsaturable in the avian (Miller et aL, 1974). Speci-
starling (Sturnus ouloaris); tinamous (Eudromia elegans); rat ficity studies m the rat with prolin¢ and fl-alanine strongly
suggest that fl-alanine transport can be blocked by excess
proline (Daniels et al., 1969a; Daniels et al., 1969b). The
* On sabbatical leave from the Department of Biochem- correction factors were: 0.015; 0.019; 0"028; 0.015; 0.012;
istry, University of Maine, Orono, ME 04473, U.S.A. and 0.017 /amoles fl-alanine/g x rain for hybrid, New
123
124 JOSEPH LERNER AND F . H . KRATZER

Hampshire, White Leghorn, dystrophic, scaleless and ich-
thyotic chickens, respectively; 0"030; 0"041; 0"049; 0.020;
0.019; 0.019; 0"026; 0"037; and 0"012 /amoles/g × min for
the chick, starling, mouse, rat, pheasant, partridge, tina-
mous, quaff and turkey, respectively; 0.015; 0.018; 0.031;
0.031; 0.085 /anoles/g x rain for the proximal jejunum,
ileum, caecum, colon and serosal muscle (jejunum-ileum)
in hybrid chnekens, respectively.
The tissue-accumulation method was justified as an indi-
cator of absorption by the ,ntestmal brush border epithe-
lium in two ways Absorption by the serosal muscles alone
was assessed by scraping the mucosa from underlying
muscle in jejunal-ileal segments (hybrid chickens) and incu-
bating the serosa with 0"6 mM am,no acnds Serosal tnssue
weights were 1/4 of whole tissue weights. The uptake
values were: 0"004+_ 0.001 ; 0.006+_.0.004; 0;
0.005 + 0"001 ; 0-004 + 0.001 /amoles/g whole tnssue x min
for lysine, methionme, aspartie acnd, glycine and prohne,
respectively. Compared with absorpt;on in whole gut seg-
ments, these rates were 0-6% of normal entry values
Absorption by the ehmken caecum was studied. The
uptake values were: 0.001 + 0.001; 0.002_ 0-002; 0;
0.002 + 0.001 ; 0"013 + 0.005 /~moles/g x min for lysine,
methionine, aspartne acid, glycine and proline, respectively.
These values demonstrate that specnfic,site medmted trans-
port by the serosa was absent in a region of the gut which
ns known to lack carrier-mediated, epithelial absorption
(Holdsworth & Wilson, 1967; Lerner et al., 1974).
Comparison of absorption between species was accom-
plished by (I) analysis of spec,fic orders of uptake for a
series of amino acids which were assigned with the aid
of a paired-difference test, and by (2) analys,s of ratnos
of absorption rates. Direct comparison of absorptnon rates
between species was avoided because of the likelihood that
the absorptive surface area per g tissue may vary between
them.
RESULTS
Intestinal absorption rates and calculated ratios of
these rates for five amino acids which were selected
as representatives of the various chemical classes are
reported in Table I. Methionine was absorbed fastest
when compared with other substrates in all avian and
Table 1-.I~T~Id~
mammalian species tested. The sequence, meth-
ionine > lysine > proline = aspartic acid = glycine,
was found in two stratus of chickens, the hybrid and
the New Hampshire, the turkey, and possibly the
starling, although data obtained for the latter species
was characterized by high variability which made
comparisons of the individual rates difficult. The same
order was also observed in the more proximal and
more distal regions of the small intestine and in the
colon of the hybrid birds. The absorption patterns
for other types of chickens used in this study varied
from this sequence only in the placement of a single
amino acid, either proline, aspartic acid, or glycine.
Thus, the order in Leghorn and ichthyotic chickens
was methionine > lysine > prohne = glycme > as-
partic acnd. Relatively low absorption of aspartic acid
was found, in addition, in the rat and mouse, whereas,
in the chick its uptake was high. For this reason the
sequence in the chick (methionine > lysine > aspartic
acid > proline = glycine) was found to differ from the
absorption patterns of the older chickens.
Compared with normal New Hampshire birds, the
dystrophic strain (methionine > lysine > proline =
aspartic acid > glycine) was less efficient in absorbing
glycine. The sequence, methionine > lysine > proline
> glycine --- aspartic acid, was common to scaleless
chickens and the pheasant. Relatively high proline
rates were observed also in the partridge (methionine
> proline = lysine > glycme = aspartic acid), the
rat (methionine > lysme = proline > glycine >
aspartic acid), and the mouse (methionine > lysine
= proline > glycine > aspartic acid). The sequence
in the quail (methionine > proline = glycine =
aspartic acid = lysine) was essentially identical to
that of certain breeds of the chicken and the turkey
with the exception of the relatively impaired lysine
absorption. This impairment was present, though
much less pronounced, in the partridge. The tinamous
absorbed most amino acids too slowly to assign an
order, although methionine uptake was substantially
higher than that of the other compounds tested.
A~SO~IO,~ OF 9 ( I , 0 ACID~ I~ A V I ~ AHD NA~HALIAN SE~CIES

Species Uptake
~4ole8 • 8-~ • n~Ln';
LysLne Nethlenine Aspa~Lc 01.vcine Prollne Hethionine Proltne Prollne
Acid Lysine ~ ASps~tlC
Aeid
C~lcken, hybr/d° 0.18~±0.018 0.b6~0.0~1 O.OTI~O.OOT O.OTS*O.OOB 0.0T6*0.010 2.53 1.01/ 1.071
" ", proxL~al JeJu.n: l' 0.173t0.019 0.~T0*0.102 0.0T~0.012 0.0~*0.016 0.067±0.019 2.72 0.85/ 0.9~/
" ", 11e~" 0.100~0.008 0.297~0.027 0.057,0.009 0.0~9±0.007 0.052~0.01~ 2.97 1.06/ 0.91/
" "p cOlOni l 0.061+0.027 0.12~0.0~ 0.00~0.001 0.019+0.00~ 0.02]±0.007 1.98 1.101 -
Chicken, ~ev Heapablre 0.268~0.0180.621~0.085 0.1~7,0.019 0 . 1 ~ 0 . 0 1 2 0.150~0.01~ 2.32 1.08/ 1.02/
ChLckee, 1mite LeShorn 0.22~0.029 0.627,0.132 0.059±0.011 0.11~±0.01~ 0.125,0.017 2.75 1.10/ 2.12
Chicken, ~ t r o p t t c 0.160~0.0160.~3~0.0~7 0.0920.013 0.077*0.008 0.10]~0.010 2.TT 1.3~ 1.081
Chicken, scaleless 0 . 1 8 1 ~ 0 . 0 1 20.~67,0.025 0.07~0.009 0.08~*0.007 0.11]~0.011 2.58 1.27 1.53
Chicken, tchthyotlc 0.~18t0.02~ 0.80~0.101 0.115,0.012 0.171±0.023 0.185,0.026 2.53 1.08/ 1.~1
ChLck (dw-old, £e~orn)+ 0.282~0.0~ 0.70~0.099 0.191~0.016 0.138~0.01~ 0o11~0.016 2.~0 0.83/ 0.60
Turkey 0.15~0.01~ 0.23~t0.020 0.0~,0.00~ 0.0~0,0.00~ 0.0~+0.003 1.~ 1.101 1.22/
~u'41°~ 0.081:1:0.026 0.8~0~0.0~8 0.108~0.011 0.121~0.00~ 0.135,0.011 10.5 1.121 1.251
Tlnamotm ~ 0.01~0.00~ 0.18~0.0~5 0.008,0.00~ 0.00~+0.002 0.008*0.005 11.E
l~r~rl~e 0.O63~0.O12 0.369~O.018 O.O~8~O.005 O.0~9.O.OO3 0.080±0.006 5.86 1.63 1.67
~eesent 0.13h±0.032 0.~25,0.056 0.072+0.008 O.O~A~O.O06 0.C9~k0.010 3.17 1.50 1.33
8tarl~n8~ 0.12~±0.035 0.~03~0.08~ 0.072±0.021 0.033~0.011 0.0~8~0.009 3.25 1.~l 0.671
Rat, JeJueu~mmmm O.l~]_tO.02~ O.~O±O.ObO 0.0~,0.006 0.081~0.015 0.1~1~0.013 3.26 1.62 2.98
Nouns+ 0.619±0.087 1.18~t0.238 0.157,0.0~3 0.23~±0.017 0.~8~0.09~ 1.92/ 2.0~ 3.08

~8orpt£~ oF amino a¢£ds ~ 8 d e t e x ~ t n e d b y t h e p~ocedures o u t l i n e d I n t h e t e x t . ~ t l v a l u e s r e p r e s e n t t h e neen

S . ~ . N . o r 15 de t e rml n&t t ons on t i s s u e from 3 a n i m a l s , e x c e p t v h e r e o t h e r v i s e i n d i c a t e d . I n c u b a t i o n t ~ e vma i a l e ,
S u b s t r a t e c c ~ c e n t r a t L ~ 8 v e r e 0 . 6 ~4. )Ud-JeJtmtm-proxlaual i l e u m VLS 8 a a p l e d , e x c e p t vhece o t h e r v l s e i n d i c a t e d .

o B a r r e d P1):aouth Rock x M o d e I s l a n d SeA,

• 5 d e t e r m i n a t l o n a ; t i s s u e F r ~ one a n i m a l .
ee 5 determln&tton8; t i s s u e from 2 s ~ t m l l t ,
see 15 d e t e z ~ t n a t i c o s ; t i s s u e f r o a 6 a n i m a l s .
meou 5 d e t e r l i n a t t o u e ; t i s s u e Frcn 3 8 ~ e ,
+ 5 de~erninattoen ; tlenue tron 5 s,nLmols.
I mot eisnlfleent~y different from 1.0 (P • 0.05) uslns s palred-ditTereuce test on tissue ~mu one anln81.
 Intestinal amino acid absorption in various species
Methionine to lysine absorption ratios (M/L) wore
observed to be similar in the various breeds of
chickens and compared closely with the value
obtained in the chick. Likewise, this ratio appeared
to be fairly uniform when measured along the gut
from the region of the proximal jejunum through the
ileum. The colon had a somewhat lower M/L ratio,
although this experiment showed highly variable
rates. M/L values varied widely between species
within the pheasant family, the quail being at one
extreme and the chicken at the other. Considering
all species, M/L values ranged over an order of mag-
nitude, the greatest differences being seen among the
birds, with the quail and tinamous at one extreme,
and the turkey at the other. Mammalian intestine,
in this respect, was similar to the chicken and turkey.
Proline to glycine absorption ratios (P/G) were essen-
tially 1.0 in the various normal lines of chickens, the
chick, iehthyotic chickens and in different regions of
the gut. However, the proline rate was significantly
faster than that of glycine in both scaleless and dys-
trophic birds. In addition to the chicken, both turkey
and quail absorbed proline and glycme at approxi-
mately the same rate. The highest P/G ratios were
noted in the partridge, pheasant, rat and mouse. Pro-
line to aspartic acid absorption ratios (P/A) were
essentially 1.0 in different levels of the gut of hybrid
chickens, in New Hampshire stock, m dystrophic
birds, in the turkey, starling and quail. The high ratios
observed for the Leghorn and ichthyotlc birds reflect
the low aspartic acid rates. Conversely, the signifi-
cantly low ratio in the chick reflects the high aspartic
acid rate. The high P/A ratios found in the scaleless
birds, in the partridge, pheasant, rat and mouse in
conjunction with the high P/G ratios in these species
indicate the effectiveness of these tissues m rapidly
absorbing proline. In this regard, the mammahan spe-
cies were the most efficient.
DISCUSSION
Three strains of chickens used in this investigation
had hereditary diseases. Muscular dystrophy occurs
in New Hampshire chickens homozygous for an auto-
somal recessive gene. Characteristics of this disease
include hypertrophy and later atrophy of the superior
pectoral muscle, which has a higher free amino acid
content, higher fat, and higher lysosomal enzyme acti-
vity than that of normal chickens (Wilson et al., 1965).
Avian ichthyosis is a mutation characterized by exces-
sive keratinization of epidermal structures, severe
limb deformation and dehydration (Sawyer & Abbott,
1974). Scaleless birds have an ectodermal defect which
occurs early m embryogeny and prevents the appear-
ance of all scales as well as most specialized deriva-
tives of scales, including feathers, foot pads and spurs
(Abbott & Asmundson, 1957).
The genetic relatedness of the members of family
Phasianidae (pheasant, chicken, partridge and quail
in this study) as well as their relationship to the tur-
key (family Meleaffrididae) has been established by
cross hybridization studies. The following crosses
* Some Tinamous of Argentina and Chde, United States
Department of the Interior, Bureau of Sports Fisheries and
Wildlife Report.
125
have been successful: quail x chicken (Wilcox &
Clark, 1961); quail x pheasant (Sarvella, 1971); phea-
sant x chicken and pheasant x turkey (Asmundson
& Lorenz, 1955); turkey x chicken (Oisen, 1960).
Quail could not be crossed with either the turkey
or partridge (Woodard et al., 1973). Of this group,
we suspect that the turkey and quail may represent
genetic extremes.
The starling (family Sturnidae) was chosen as an
example of an avian which possesses an extremely
short digestwe tract and a vestigial caecum. In terms
of body size, it was similar to the quail. The tinamous
(family Tinamidae) is perhaps the most primative liv-
ing bird (Fisher & Peterson, 1964). It is characterized
by its large, multi-pouched caecum and the species
used in this study is a desert bird, living in regions
with as little as 4.5" of rain.*
There is reasonable evidence from competition
studies to suggest that amino acid transport in the
avian small intestine occurs by way of a number of
chemzcal processes with overlapping specificitles. Sys-
tems have been proposed which absorb (I) aliphatic
amino acids (including glycine and imino acids), (2)
aliphatic amino acids and glycine (excluding imino
acids), (3) imino acids and glycme (excluding bulky,
aliphatic amino acids), (4) imino acids (excluding gly-
cme), and (5) cationic amino acids (Miller et al., 1974;
Herzberg et al., 1971; Herzberg & Lerner, 1973;
LaBelle et al., 1971). Acidic amino acid transport has
not been studied in the avian. Neutral amino acid,
basic amino acid and immo-glycine pathways with
overlapping reactivities have also been described in
the rat intestine (Reiser & Christiansen, 1969). Schultz
and coinvestigators (1970) showed that acidic amino
acids enter rabbit ileum via a carrier mechanism,
although earlier work with mammalian intestine
demonstrated that these substances are rapidly trans-
aminated by this tissue 0Vlatthews & Wiseman,
1953). The identification of genetic defects which
result in malabsorption of neutral or basic amino
acids in man provides support for the concept of
separate transport mediators. Thus, in cystinuria
there Is a defect in intestinal absorption of basic
amino acids and cystine in one form of the disease;
in Hartnup disease the transport of tryptophan and
other neutral amino acids is defective, sparing, how-
ever, the absorption of basic amino acids, diearboxy-
lie amino acids, imino acids and glycine; and in cer-
tain forms of imino-glycinuria a gut defect has been
observed for proline and glycine (Rosenberg, 1969).
The indwidual absorption rates measured in this
study must necessarily reflect the sum of activities of
the separate systems by which a given substrate is
transported. Presumably, the presence of a particular
pattern of specific systems is determined genetically,
and that expression of genotype may be influenced
by feedback mechanisms at the transcriptional level
as discussed below. Other factors, perhaps of lesser
quantitative significance, may include the influence of
substrate metabolism and transmembrane electrical
potential difference. Assuming that the primary deter-
minant of the observed rates is the genotype, we may
conclude that even closely related breeds of chickens
are genetically heterogeneous. This deduction should
be valid for the relative placement of as'panic acid,
even if its mode of uptake is by diffusion followed
126 JOSEPH LERNER ^ND F. H. KRATZER
by transamination. In this case, we might postulate
genetic variants in epithelial transaminases. The rela-
tively high aspartic acid transport rate observed in
the chick as opposed to the older chickens may reflect
either a change in transaminase activity or that of
a membrane carrier. Antonioli & Christensen (1969)
have, in fact, reported findings on differing schedules
of regression of transport systems for lysine and
alanine in maturing mammalian red blood cells. The
low aspartic acid absorption seen in both the Leghorn
and ichthyotic birds probably relates to the fact that
ichthyotic chickens derive from parent Leghorn stock
(U.K. Abbott, personal communication). Although
scaleless birds were derived from New Hampshire
stock, the mutants used in this study had been crossed
with a number of other breeds, and therefore should
not be compared on a disease basis with the normal
New Hampshire line (Abbott & Asmundson, 1962).
The absorption of glycine in dystrophic birds was
significantly lower on a relative basis than in the con-
trol New Hampshire chickens. Peterson et al. (1963)
found that amino acids, such as methionine, aspartic
acid and proline, were increased about 2-fold in
amount as free amino acids in pectoral muscle of dys-
trophic compared to normal New Hampshire birds;
glycine, however, was increased 3-fold. Conceivably,
the high tissue content of glycine might serve as a
repressive signal limiting uptake by a transport sys-
tem which has high specificity for glycine. Studies
nevertheless have not been done to assess the tissue
concentration of glycine in other organs. Chrlstensen
(1973) has reported data on a discrimination against
glycine uptake in fetal guinea pig tissues relative to
the maternal system which disappears rapidly after
delivery. Presumably, the abrupt fall in plasma amino
acids which occurs after delivery might be the stimu-
lus for the rapid postnatal enhancement of glycine
transport. Franchi-Gazzola et al. (1973) discovered
that the capacity to synthesize transport proteins of
the A (alanine-preferring) mediation in chick embryo
heart cells was repressed at the level of transcription
by amino acids pertaining to the A process.
The constancy of the orders of absorption along
the small intestine of the chicken probably means that
the activities and abundance of the individual trans-
port mediators are constant throughout this region
of the gut. These results are at variance with those
of two groups (Baker & George, 1971 ; Schedl et al.,
1968), who contend that the rat and human small
intestines have specific longitudinal distributions of
two distinct membrane carriers.
The low lysme absorption in the quail may perhaps
signify a genetic defect in the basic amino acid carrier
in this organism. As such, the quail may serve as a
model for malabsorption of lysine in the human. In
terms of comparative biochemistry, the quail also
appears to be different from the chicken and pheasant
in its ability to conjugate benzoic acid with the basic
amino acid ornithine (Bunden et al., 1973). The low
lysine absorption in the tinamous is part of a more
general phenomenon of impaired amino acid absorp-
tion.
Striver & Rosenberg (1973) have proposed that
group-specific transport of basic amino acids and cys-
tine in the gut and kidney is catalyzed by a specific
transport protein whose synthesis is controlled by a
single pair of allelic genes. Thus, the combination of
normal and various mutant alleles is expressed in a
variety of phenotypes, characterized by excretion
rates for the amino acids which are normal, slightly
increased, moderately increased, or highly increased.
This type of model would appear to be applicable
in explaining how absorption rates vary between
closely related avians as reported in this study.
Acknowledctements---We are grateful to Leslie Earl,
James Adams, Adnan Miski and Drs. Ursula Abbott and
Hans Abplanaip for their assistance and interest in this
work.
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