Received: 15 July 2020 Revised: 28 December 2020 Accepted: 4 January 2021

DOI: 10.1002/ar.24588

FULL LENGTH ARTICLE

The topographic and systematic anatomy of the alpaca

stomach

Anke Lisa Vater | Elisabeth Zandt | Johann Maierl

Department of Veterinary Sciences,

Faculty of Veterinary Medicine, Chair of
Anatomy, Histology and Embryology,
Ludwig-Maximilians-University Munich,
Munich, Germany
Correspondence
Anke Lisa Vater, Department of
Veterinary Sciences, Faculty of Veterinary
Medicine, Chair of Anatomy, Histology
and Embryology, Ludwig-Maximilians-
University Munich, Veterinärstr.
13, 80539 Munich, Germany.
Email: a.vater@anat.vetmed.uni-
muenchen.de
Abstract
The gastric anatomy of the alpaca (Vicugna pacos) is adapted to the physiologi-
cal process of ruminating and the degradation of plant cell wall contents to a
great extent. Most alpaca husbandries consist of only few animals and with the
still increasing number of alpacas worldwide the number of persons who are
responsible for these animals is increasing as well. Despite this, little research
has been done with regard to the clinical anatomy of the stomach of alpacas.
Six animals were used for dissection. The vascular system of two alpacas was
injected with latex milk to illustrate the course of the blood supply to the vis-
cera. One stomach was used to prepare formalin-fixed preparations. The stom-
ach consisted of three compartments (C1–C3) and showed two sacculated
areas in C1 and another comb-like system in C2. The compartments were lined
by a smooth mucosa. Only the deep cells of C2 were lined by a papillated
mucosa. The main blood supply was provided by the coeliac artery which was
divided into the hepatic artery and the left gastric artery, supplying abdominal
organs like liver, spleen, pancreas, and the initial part of the duodenum. Liter-
ature research on the llama stomach showed that the alpaca stomachs that
were used resembled each other to a very large degree. The specific design of
the stomach together with its related functions and physiological processes
confirm that the evolution of Tylopoda and Ruminantia took place in parallel
and not in homology.

1 | INTRODUCTION

The examination of the gastrointestinal (GIT) tract of the

Abbreviations: C1, compartment 1 (of the stomach)C2, compartment 2;
C3, compartment 3; DFC, distal fermentation chamber; FS, forestomach
(C1/C2/proximal 4/5 of C3); GIT, gastrointestinal tract; GR, grass and
roughage eaters; HS, hindstomach (last 1/5 of C3); IM, intermediate,
opportunistic mixed feeders; SACs, South American camelids; VFA,
short-chain volatile fatty acids.
Alpaca (Vicugna pacos) and the comparison to the exis-
ting literature about the digestive physiology and anat-
omy of other South American camelids (SACs) and
ruminants forms a basis for a better understanding of the
anatomical particularities of the alpaca. The unique fea-
tures of their GIT allow the adaptation of alpacas to their

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Anat Rec. 2021;304:1999–2013. wileyonlinelibrary.com/journal/ar 1999


2000
special habitat in the high altitudes of the Andean moun-
tains at elevations above 3,800 m (Fowler, 2010) creating
different challenges that affect the animals' GIT. The
semiarid climate in the Altiplano consists of a dry (May
to November) and a wet season (December to April). The
predominant part of the forage consists of fibrous plants
with many structural carbohydrates in the plant cell
walls which are virtually indigestible. During the dry sea-
son the plants become more lignified and are even harder
to digest. Additionally, the water resources decrease to a
minimum (San Martin & Bryant, 1989; San Martín &
Van Saun, 2014).
1.1 | Comparison of Tylopoda to
Ruminantia
Bohlken (1960) already stated that there are fundamental
anatomical differences between the stomachs of
Tylopoda and Ruminantia and concluded that the gross
similarity of the stomachs most certainly was the result
of a parallel development not of a close relationship of
the two groups. Describing the differences between the
gastric anatomy of Tylopoda and Ruminantia he classi-
fied the Tylopoda in the system of the Artiodactyla, com-
paring the stomachs of vicuña, (Vicugna vicugna),
guanaco (Lama guanicoe), and llama (Lama glama) to
that of sheep and domestic ox. He emphasized several
characteristic features that distinguish SAC's from Rumi-
nants, making it very difficult to find homologies
between the two groups: first, the different external seg-
mentation of the gastric sections, in particular, four in
Ruminantia and three in Tylopoda. Second, the typical
glandular sacs, existing only in Tylopoda. Third, the gas-
tric groove, which is marked off by two strong lips in
Ruminantia and by one single lip in Tylopoda. Fourth,
the distinctly different structure of the inner surface of all
the divisions of the stomach.
The fact that the physiology of digestion in the stom-
ach cannot be the same in the two groups was the second
conclusion drawn by the author out of these dissimilar-
ities. Ruminating as a physiological process is closely
connected to the gastric anatomy. In consequence of the
anatomical differences the ability of ruminating must
have been acquired twice in phylogeny (Bohlken, 1960).
With this knowledge the denomination of the different
sections should be clear. In this point we followed
Vallenas, Cummings, and Munnell (1971), who did not
use the nomenclature common for the Ruminant's stom-
ach but defined the three sections of the SAC's stomach
as compartments 1, 2, and 3 (C1, C2, and C3).
Several studies described the gross anatomy of the
stomach of the llama and guanaco in detail:
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VATER ET AL.
Compartment 1, located within the abdominal cavity, is
the biggest of the three compartments, touching the dia-
phragm and the left rib-supported body wall. It reaches
the flank area (Alzola et al., 2004). The cardia is located
on the right side of the cranial sac. On the same side the
caudal sac communicates with the reniform C2.
The smooth-walled C2 has a dorsal lesser curvature and
a ventral greater curvature. A thick-walled, narrow, tubu-
lar passage cranially connects C2 to C3 (Alzola
et al., 2004; Vallenas et al., 1971). C2 is located between
C1 on the left and the liver on the right side (Alzola
et al., 2004).
C3 is a tubular organ with a length of 50–70 cm. Its distal
region merges into the HCL-secreting hind stomach
without any anatomical segregation visible from the out-
side (Heller, Gregory, & von Engelhardt, 1984). Distally it
forms a preterminal sigmoid flexure (Vallenas
et al., 1971).
1.2 | Internal morphology
In the llama a transverse muscular pillar corresponding
to the transverse furrow between the cranial and the cau-
dal sac is found. The ventricular groove consists of a sin-
gle lip, beginning sinistrodorsally of the cardia coursing
caudally to the lesser curvature of C2.
The saccules of the caudal sac are located caudally to
the transverse pillar. Primary, secondary, and tertiary
crests correspond to the grooves visible from the outside.
Generally, the sacculated area of the cranial sac shows a
similar design like the caudal area of sacculations.
In C2 the ventricular groove is located at the lesser
curvature, delimited by a single lip and extending until
the orifice of the tubular passage to C3. The greater cur-
vature and sidewalls of the C2 are partitioned into a
retiform pattern by primary crests and secondary crests,
defining orifices to deep glandular cells or chambers. The
cells are lined by a papillated mucosa and in contrast to
the saccules of C1 the individual cells are not visible from
the outer serosal surface (Vallenas et al., 1971).
The tubular connecting passage from C2 to C3
appears as a continuation of the ventricular groove.
C3 is entirely lined by a glandular mucosa. The
mucosa of the preterminal flexure is thickened and
smooth. The first fifth of the terminal greater curvature is
lined by a thick mucosa, corresponding to the proper gas-
tric glands. Along the lesser curvature in this area the
mucosa in general is thinner, containing the pyloric
glands, which cover the entire pyloric circumference in
the last 5 cm. The entrance to the duodenum is guarded
by a prominent torus pyloricus on the lesser curvature
(Alzola et al., 2004; Vallenas et al., 1971).
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VATER ET AL. 2001

1.3 | Greater omentum
In comparison to ruminants the greater omentum of
camelids is smaller.
It is attached to the lesser and greater curvature of C2
and C3 and along the visceral (right) surface of C1. The
epiploic foramen is located ventrally of the liver near the
entrance of the caudal vena cava on its passage through
the liver (Fowler, 2010).
1.4 | Digestive physiology
Different aspects of the digestive physiology, as well as
histochemical and biochemical mechanisms appearing in
the GIT tract, were investigated by different authors.
Here again, the existing literature deals primarily with
the llama and guanaco and therefore the physiological
processes in llamas are often extrapolated to alpacas.
particles are collected in the central part of C1. This pro-
cess and the separation of small and large particles are
continuously repeated during the motility cycles. The
large particles are retained in C1. In the llama the reten-
tion time of fluids (approximately 10 hr) is markedly
shorter than that of particles (about 25 hr). So the larger
particles are retained in the center of C1, whereas small
particles and fluids are mainly collected in C2 and are
transported into C3 (Heller et al., 1984).
The goal of our study was to give a detailed macro-
scopic description of the alpaca's gastric anatomy and to
point out potential differences between alpacas and
llamas to their individual feeding behaviors. According to
these characteristics we tried to classify the two species to
an appropriate morphophysiologic feeding type. We com-
pared the process of ruminating between SACs, especially
of alpacas and ruminants in close connection to their
respective gastric design.

2 | MATERIALS AND METHODS

1.5 | Motility and movements of the
ingesta 2.1 | Material and anatomical dissection

Several authors described the forestomach (FS) motility
of SACs (Ehrlein & von Engelhardt, 1971; Heller
et al., 1984; Vallenas, 1965; Vallenas & Stevens, 1971; von
Engelhardt & Holler, 1982). The llama's stomach shows a
characteristic pattern of contractions (motility cycle) (von
Engelhardt & Holler, 1982). Ingesta in the dorsal portions
of C1 are rather dry, whereas the contents in the ventral
region of the cranial sac, in the glandular sac region and
in C2 are semifluid to watery. The motility pattern of the
FS results in a very effective mixing of the ingesta with
fluid and microorganisms (Ehrlein & von
Engelhardt, 1971; Lechner-Doll et al., 1995). During the
contraction of muscular ridges in the caudal portion of
C1, fluid with contents of nutrients is squeezed out of the
solid ingesta and pressed into the relaxing ventral sac-
cules and into C2. The rather solid ingesta with the large
Two male and four female Alpacas aged from 6 months
to 18 years were used for the anatomical preparations
(Table 1). All animals were euthanized for reasons not
related to the digestive apparatus/system. The time
between euthanasia and dissection of the animals used
was between 8 and 24 hr.
2.1.1 | Euthanasia
The animals were euthanized by veterinarians at the ani-
mals' home stable or in the Clinic for Ruminants,
Oberschleissheim. All animals were injected with pento-
barbital (Euthadorm®, 400 mg/ml; CP-Pharma 31303
Burgdorf; 1–2 ml/10 kg/BW) via the jugular vein. The
alpacas were transported to the dissection hall (of

TABLE 1 Breed, sex, age, weight, and reason of euthanasia of the individual animals

Breed Sex Age Weight (kg) Reason for euthanasia

Huacaya Female 3.5 years 55 Mandibular neoplasia
Huacaya Male Adult (exact age unknown) 72 Aggressiveness
Huacaya Female 20 years 44 Death of old age and emaciation
Huacaya Female 6.5 months 25 Suspicion of endoparasites (no apparent abnormalities
of the GIT and the ingesta during dissection)
Suri Male 18 years 40 Acute blindness
Huacaya Female 5 years 52 Weakness and recumbency

2002
the Chair of Anatomy, Histology and Embryology of the
LMU) in left lateral recumbency.
2.1.2 | Anatomical dissection
Using the usual methods and instruments, the dissection was
carried out. First, the topographical anatomy of the abdomi-
nal and pelvic cavity was examined, photographed, and
documented. In different animals various approaches to the
abdominal cavity were selected and therefore pictures were
taken from the ventral view as well as from the right and
the left lateral view. Then the stomach and the intestines
were removed for individual examination.
2.1.3 | Fixation
Before dissection, the arterial vascular system of the spec-
imen was injected with a 50% alcohol–water solution via
the right common carotid artery. The animals as well as
the extracted organs were stored in a 10% NaCl solution
with an added amount of 0.005% formaldehyde and
refrigerated at 4 C during the dissection period.
2.1.4 | Preparation of the arterial
vascular system with latex milk
In two animals, the arterial vascular system was injected
with latex milk by injecting about 600 ml of red latex
milk into the right common carotid artery. In one of the
animals, the right femoral artery was ligated, in the other
animals, both femoral arteries were ligated before injec-
tion to ensure enough pressure being built up. In this
way even the smallest vessels of the organs were injected.
All animals were then cooled down to 4 C for 3 days for
the latex milk to harden.
2.1.5 | Frozen preparations of the
saccule complexes of the stomach
For producing these preparations the first compartment
of the stomach was fixed in 5% formaldehyde solution in
the desired position for 3 days. Afterward it was frozen at
−18 C and sawed into pieces.
2.1.6 | Photographic documentation
An SLR camera (Olympus® Digital ED with an Olympus
Zuiko Digital ED 14-42 mm f3.5-5.6 lens and an Olympus
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VATER ET AL.
Zuiko Digital 35 mm f3.5 macro lens) was used. A polar-
izing filter (hama® PL CIR Ø 58 (IV) and Ø 52) reduced
highlights on the preparations.
The pictures were taken in front of a black foil and
using a tripod.
For editing the pictures afterward, the computer pro-
gram Adobe® Photoshop® was used.
3 | RESULTS
The stomach of the alpaca consisted of three compart-
ments (C1, C2, and C3), which mainly lay in the abdo-
men but were also extending into the intrathoracic
portion of the peritoneal cavity.
3.1 | External morphology
The cardia was located on the dorsal surface of C1 at the
level of the ventral transverse furrow, slightly asymmetri-
cally on the right side.
Separated by a semicircular ventral transverse furrow,
which was limited to the ventral and lateral walls of the
stomach into a smaller cranial and a larger caudal sac,
the balloon-like C1 (Figure 1) was about 50 cm long.
Each sac showed a defined region of saccular-like bulges.
The saccule complex of the cranial sac (Figures 1
and 2) was located at its cranial aspect beneath the adhe-
sion surface of C1 to the diaphragm pillars, extending
ribbon-like from the right to the left and touching the
diaphragm. Its longitudinal axis measured 30 cm and its
width ranged from 2 cm on the left to 10 cm on the right.
In contrast to the remaining smooth surface of the cra-
nial sac of C1 in this region the individual saccules were
F I G U R E 1 Left lateral view of C1. C1, C3—Compartments
1, 3. 1—Cranial sac of C1; 2—caudal sac of C1; 3—cranial
sacculated area; 4—caudal sacculated area; 5—ventral transverse
furrow

VATER ET AL.
F I G U R E 2 Right lateral view of C1. C1, C2, C3—
Compartments 1, 2, 3; DA, duodenal ampulla. 1—Cranial
sacculated area of C1; 2—caudal sacculated area of C1; 3—cardia;
4—attachment line of the greater omentum (clarified by a
black line)
not definable from outside, however, the entire complex
was prominent.
In the caudal sac (Figures 1 and 2) there was the
larger region of these saccules, situated on the visceral
surface directly caudal to the ventral furrow and in close
vicinity to C2. Stretching on a width of about 17 cm, dor-
sally the saccules began 6–7 cm below the cardia. This
saccule region extended ventrally to the left stomach wall
and decreased in its width, so that it had an almost trian-
gular shape. The various saccules were separated by deep
prominent grooves into single saccules, pairs of two or
groups of three. The line of attachment of the greater
omentum separated this saccule complex into a cranial
and a caudal part, so that the caudal part lay within the
omental bursa.
Equipped with a smooth-walled surface, C2
(Figure 2) was kidney-shaped with its greater curvature
directing ventrally and its lesser curvature dorsally.
The last compartment (C3) (Figures 1, 2, and 3a) had
an elongated and tubular form with a smooth wall as
well. C2 and C3 were connected by a narrow 2.5 cm wide
canal (Figure 3a, CT) before C3 enlarged to a sac-like oral
bend. After that, it turned caudally into its straight por-
tion, which was 10 cm in diameter. With its greater cur-
vature directing ventrally and its lesser curvature facing
dorsally, C3 ended in the pyloric part, which formed a
dilated loop, pointing cranially again.
The whole stomach was covered by peritoneum apart
from an area at the dorsal aspect of C1. This area was
attached to the diaphragm and the sublumbar region as
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2003
far as the mesentery root at the level of the third lumbar
vertebra.
3.2 | Internal morphology
The inner lining of C1 (Figures 4 and 5) was a smooth
mucosa without any papillae but some irregular mucosa
folds.
The bottom of C1 (Figure 4) was characterized by a
2–3 cm wide transverse pillar, corresponding to the ven-
tral transverse furrow. Forming the cranial and dorsal
border of the orifice from C1 to C2, the pillar was semi-
circular shaped with its right branch running dorsally.
Furthermore, the transverse pillar was the cranial
border of the caudal saccule complex (Figure 4). Smaller
gastric pillars were placed in right angles to it and ran in
caudal direction becoming thinner and lower in the end.
These 13–14 pillars in turn were intersected by even
smaller folds building openings to a comb-like system
corresponding to the saccules visible from the outside
(Figures 6 and 7).
The saccule complex in the cranial sac of C1 was of
similar structure. Again 13–14 main pillars, running dor-
soventrally, were intersected with smaller ones, forming
the orifices to the saccules. The orifices were arranged in
rows of four in the middle and in rows of two or in a sin-
gle row at the right and left end of the saccule complex.
Lying dorsocranially of the larger saccule complex the
aperture from C1 to C2 was 7 cm long and 4 cm wide
(Figure 5). The surface of the smaller curvature of C2 was
covered by a smooth mucosa. In the area of its greater
curvature there were about six to seven semicircular pil-
lars intersected by additional right-angled pillars, also
leading into a comb-like system. The surface of this area
was occupied by numerous short papillae, except the pil-
lars, which were covered by a smooth mucosa again
(Figure 5).
Having its origin on the left side of the cardia the gas-
tric groove continued to the entrance of C2 and ran along
the right side of the lesser curvature of C2, so that the
access to the sulcus was located medially. It consisted of
a single lip and was about 16 cm long and 0.2 cm deep.
This lip ended directly behind the passage to the con-
necting tube to C3 displaying a smooth mucosa without
any folds.
The initial bend and the straight part of C3
(Figure 3b) were lined by a smooth mucosa folded in low
longitudinal ridges. Only a small area of the lesser curva-
ture of C3, directly distal to the connecting piece, showed
a comb-like surface, limited by shallow rims. The longitu-
dinal folds abruptly ended before the caudal loop of C3.
The greater curvature of this loop was lined by a thick

2004
F I G U R E 3 External (a) and internal (b) morphology of C3. CT, Connection tube; DA, duodenal ampulla. 1—Initial bend of C3; 2—
straight part of C3; 3—caudal loop of C3; 4—torus pyloricus
mucosa, folded like a cratered landscape with countless
depressions. The mucosa of the lesser curvature and the
pyloric circumference was considerably thinner again. A
prominent torus pyloricus and a significant constriction
separated the C3 from the duodenum.
3.3 | Topographic position
Being the largest part of the stomach, C1 extended with
its longitudinal axis from the diaphragm at the level of
the sixth to seventh intercostal space to the fourth to fifth
lumbar vertebra (Figure 8). It occupied almost the entire
left side of the abdominal cavity but also crossed the
median plane to the right with its parietal surface being
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VATER ET AL.
oriented toward the left, ventral, and dorsal body wall.
The visceral surface faced to the right and was closely
related to C2, C3, and the liver, which separated it from
the right body wall (Figure 9). Caudally it mainly lay next
to intestinal loops of the small and large intestines
(Figures 8 and 9).
C2 was located caudoventrally to the cardia between
C1 on the left and the liver on the right within the vesti-
bule of the omental bursa. It extended in an area between
the seventh to the ninth rib. Its greater curvature pointed
ventrally, its lesser curvature dorsally, while its oral part
lay directly caudal to the larger glandular region of C1.
The elongated and tubular-shaped C3 was located
on the right side of C1 as well (Figures 8 and 9). Its ini-
tial tight connecting piece first ran cranially up to the
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VATER ET AL. 2005

F I G U R E 4 Compartment 1: internal morphology. C2, Compartment 2. 1—Cranial sac of C1; 2—caudal sac of C1; 3—cranial sacculated
area; 4—cardia; 5—ventral transverse pillar; 6—primary crests; 7—secondary crests; 8—tertiary crests

F I G U R E 5 Gastric groove (C1 and C2 were turned inside out; contour of C2 clarified by a black line). C1, C2—Compartments 1, 2. 1—Cranial
sac of C1; 2—caudal sac of C1; 3—cranial sacculated area; 4—caudal sacculated area; 5—ventral transverse pillar; 6—cardia: 7—singular lip
limiting the gastric groove; 8—lesser curvature of C2; 9—greater curvature of C2; 10—connecting tube between C2 and C3
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2006 VATER ET AL.

F I G U R E 6 Preparations of frozen sections of the caudal saccular region of C1. (a) Oblique view with cutted saccules, (b) top view of the
saccules. 1—Primary crests; 2—secondary crests; 3—tertiary crests; 4—ventral transverse pillar

F I G U R E 7 Preparations of frozen sections C2. (a) Transverse section; (b) transverse and longitudinal section. 1—Lesser curvature of C2;
2—primary crests; 3—secondary crests

diaphragm before dilating and turning caudoventrally,
with its straight part resting on the ventral body wall
turning dorsally again at the level of the fifth lumbar
vertebra and ending in a sigmoid loop. In part, the liver
separated C3 from the right body wall and loops of the
duodenum lay between the end loop of C3 and the
right body wall in some animals. In the other animals
the small intestine was located only caudal to the
stomach.
3.4 | Greater and lesser omentum of the
stomach
The stomach was fixed in the abdominal cavity by the
esophageal embedding in the diaphragm, the fixation
of the cranial portion of the duodenum, and by the
mesentery of the stomach itself. The mesentery con-
sisted of the greater omentum and the lesser
omentum.
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VATER ET AL. 2007

F I G U R E 8 Right lateral view of the abdomen. C1, C3, Compartments 1 and 3 of the stomach; DC, descending colon; DP, diaphragm; J,
Jejunum; L, liver; L1–L7, lumbar vertebra 1–7; rK, right kidney; T6–T12, thoracic vertebra 6–12

F I G U R E 9 Left lateral view of the viscera of the abdomen. AC, Ascending colon; C1, C3—compartments 1 and 3 of the stomach; DP,
diaphragm; L, lung; R5, R12—Ribs 5 and 12; S—spleen

2008
The line of attachment of the greater omentum at the
dorsal abdominal wall started at the esophageal hiatus,
running along the adhesion area of the stomach to the dia-
phragmatic pillars (Figure 10). On the left-hand side, it
inserted at the visceral surface of C1 in a V-shaped course.
Dividing the saccular complex of the caudal sac into a cra-
nial and caudal portion it subsequently rose dorsally again.
There it passed to the mesentery of the spleen and inserted
at the hilus of the spleen. The most caudal point of attach-
ment was the mesocolon descendens on the level of the
caudal end of the left pancreatic lobe. Running to the
medial side of C2 on the right-hand side, it inserted at the
greater curvature of C2 and C3 and along the cranial and
descending portion of the duodenum. The omental bursa
had a small dimension. It was fit against the compartments
of the stomach very tightly and was not visible when open-
ing the abdominal cavity.
The lesser omentum consisted of the hepatogastric
and hepatoduodenal ligament, both originating from the
visceral surface of the liver. The hepatogastric ligament
was attached to the esophageal hiatus at its cranial
aspect, to the lesser curvature of C2 and C3, and the
hepatoduodenal ligament to the initial part of the duode-
num. As a result, C2 was located within the vestibule of
the omental bursa recess which was dorsally closed
through the adhesion zone of the caudal vena cava to the
dorsal body wall. Being 4 cm long and 2 cm wide the
ovally shaped epiploic foramen was located caudal to the
liver between the caudal vena cava dorsally and the
V. portae ventrally on the level of the first lumbar
vertebra.
FIGURE 10 (a) Lesser omentum and (b) greater omentum
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VATER ET AL.
3.5 | The vessels of the stomach
3.5.1 | The arterial supply to the
stomach
The arteries of the stomach originated from the coeliac
artery (Figure 11), which came from the abdominal aorta
on the level of the third lumbar vertebra directly cranial
to the cranial mesenteric artery. Close to its origin the
coeliac artery is divided into the hepatic artery (c) and
the left gastric artery (b), supplying the liver, the spleen,
the pancreas, and the initial part of the duodenum.
The splenic artery (h) came from the hepatic artery
close to its origin, gave off the pancreatic branch (i) to
the pancreas, and continued to the spleen.
The hepatic artery supplied the gastroduodenal artery
(j), which divided into the cranial pancreaticoduodenal
artery (k) to the initial part of the duodenum and the
right gastroepiploic artery (l) to the greater curvature of
C2 and C3. Giving off a branch for the ventral aspect of
the caudal flexure of C3 the right gastroepiploic artery
ran along the greater curvature of C3 supplying it with
many small vessels.
Shortly before reaching the liver, the hepatic artery
(c) gave off the right gastric artery (m) which divided cra-
nial of the terminal flexure into two parallel vessels run-
ning along the lesser curvature of C3.
After originating from the coeliac artery, the left gas-
tric artery supplied a big vessel, which divided into two
branches for the first compartment (d, e). These branches

VATER ET AL.
F I G U R E 1 1 Arteries and lymphonodi of the three
compartments of the stomach. a—Coeliac artery; b—left gastric
artery, c—hepatic artery; d, e, f—branches for C1; g—branches for
the caudal sacculated area; h—lienal artery; i—pancreatic branch;
j—gastroduodenal branch; k—cranial pancreaticoduodenal artery;
l—right gastroepiploic artery; m—right gastric artery; n—branch
for the caudal sacculated area; o—oesophageal branch; p, q—
branches for the cranial C1; r, s—arteries for C2; t—left
gastroepiploic artery
supplied the various regions of C1 partly building
anastomoses.
One of these branches passed into the left gas-
troepiploic artery (t). After continuing along the greater
curvature, it anastomosed with the right gastroepiploic
artery (l).
The truncus of the left gastric artery (b) ran cranially,
supplying an esophageal branch (o), a branch for the cra-
nial saccules of C1 (p, q), one for C2 (r), and finally
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2009
divided into two branches. These continued on the dorsal
curvature of C3 (b), where they anastomosed with the
two branches of the right gastroepiploic artery (l).
3.5.2 | The venous drainage of the
stomach
The veins, draining the stomach, the spleen, and the ini-
tial part of the duodenum, ran parallel to their respective
arteries and are named according to these. They all
joined in the portal vein, which entered the porta of the
liver.
4 | DISCUSSION
The purpose of our study was to give a detailed insight
into the macroscopic anatomy and topography of the
stomach of the alpaca and to allow the comparison to the
gastric anatomy of the llama and other ruminating spe-
cies. This detailed macroscopic description of the stom-
ach together with its associated structures (vessels, lymph
nodes) should help veterinarians and surgeons to make
correct diagnoses and to improve suitable treatments for
the GIT tract.
4.1 | Theoretical implications
To the authors' knowledge, most of the literature deals
with the anatomy of SACs and camelids in general and
not with the specific situation of the alpaca. This, how-
ever, is necessary as alpacas belong to an own genus dif-
fering in their habitat and feeding behaviors.
Furthermore, the existing literature mostly describes
only single aspects of the gastric anatomy of SACs, how-
ever, not in a functional unit together. The present study
gives a comprehensive overview of the stomach together
with its associated structures and its topography.
To the authors' knowledge, there exists no work
describing the alpaca's stomach systematically.
4.1.1 | Comparison to ruminants
Furthermore, this study draws comparisons to the gastric
anatomy of ruminants and is taking into account the differ-
ent digestive physiology. San Martín and Van Saun (2014)
already reported that due to the lack of sound knowledge
about the GIT anatomy and digestive physiology of SACs,
feeding practices or medical treatments are often extrapo-
lated from other ruminant species.

2010
Clear differences in the gastric and intestinal anatomy
(Vater & Maierl, 2018) together with the individual feed-
ing behavior of SACs make a specific approach to the
GIT anatomy of the alpaca indispensable for correct feed-
ing and treatment.
The main external differences to the ruminant's stom-
ach (Nickel, Schummer, & Seiferle, 2004) were the exter-
nal segmentation of the stomach and the lack of a clear
demarcation between the FS (C1, C2, and the cranial part
of C3 in SACs; rumen, reticulum, and omasum in rumi-
nants) and the HS (caudal part of C3 in SACs; abomasum
in ruminants) and the unique appearance of the areas of
saccules in SACs.
Furthermore, the greater omentum is significantly
smaller in the alpaca showing a completely different line of
attachment on C1 compared to the greater omentum of
ruminants. In contrast to ruminants (Nickel et al., 2004)
there is no omental sling, which separates the intestines
from the body wall.
The internal morphology of the alpaca stomach
shows some fundamental differences to that of rumi-
nants. C1 is only separated into a cranial and caudal sac
but is not divided into dorsal and ventral portions. It is
lined by a smooth mucosa without any papillae. The ven-
tricular groove is limited by a small single lip in contrast
to two lips in ruminants.
In the alpaca, the internal surface of C2 is the only
portion that is partly lined by a papillated mucosa. It also
shows a comb-like system of small ridges just as in the
sacculated areas of C1. A similarity to the ruminants'
stomach is the quite large opening from C1 to C2 like the
opening between the rumen and the reticulum. The car-
dia of the alpaca, however, merges directly and only into
C1 and does not enter the FS at a location corresponding
to the ruminoreticular transition.
As far as the internal surface is concerned, C3 seems
to be separated into two functional units, characterized
by different types of mucosa. The initial oral bend and
the long tubular section are lined by a smooth mucosa
showing a flat longitudinal plication, whereas the caudal
loop of C3 is marked by a noticeable thickening of the
mucosa characterized by countless crater-like depres-
sions. In the alpaca this mucosa—clearly different in
height and color compared to the proximal part—exactly
corresponds to the distal fifth of C3 often considered as a
separate part of the stomach and seen as HS (Luciano,
Reale, & von Engelhardt, 1980; Sumar, 2010; von
Engelhardt & Heller, 1985). In the guanaco it is covered
by fundic epithelium with the typical secretion of
hydrochloric acid and a transition to pyloric epithelium
toward the pylorus (Luciano et al., 1980; von
Engelhardt & Heller, 1985). It may be assumed that the
macroscopic similarity of the mucosa within SACs
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VATER ET AL.
reflects the functional resemblance in terms of secretory
activity. Accordingly, this distal part of C3 is often com-
pared to the abomasum of ruminants (Heller et al., 1984).
In the alpaca, however, there is no anatomical separation
between the HS and the previous section as it is in rumi-
nants (ostium omasoabomasicum).
The external as well as the internal morphology of
the stomach of the alpaca, which fundamentally differs
from that of ruminants, substantiate the first assumption
of Bohlken (1960), that the alpaca as well as the other
three species of SACs developed their gastric anatomy
and their ruminating digestion process in a parallel evo-
lution and not in homology to ruminants.
Bohlken (1960)'s second assumption, that the physiol-
ogy of digestion could not be the same in Tylopoda as in
Ruminantia because the physiological process of rumi-
nating is closely connected to the gastric anatomy, proves
to be true in several anatomical particularities of SACs.
These particularities are related to specific physiological
processes, which are unique in SACs.
Connected to their specific physiological process of
ruminating, the first anatomical difference in SACs is the
existence of glandular mucosa in C1, C2, and the tubular
part of C3, which is characterized by a high absorptive
capacity of the epithelial cells and millions of tubular
glands (Cummings, Munnell, & Vallenas, 1972; Luciano
et al., 1980; Luciano, Voss-Wermbter, Behnke, von
Engelhardt, & Reale, 1979). These facts explain the two
to three times higher absorption rate of VFA, water, and
sodium than in ruminants (Rübsamen & von
Engelhardt, 1979; Vallenas et al., 1973; von Engelhardt &
Sallmann, 1972).
The second difference is the design of the saccules,
which play a significant role in the effective mixing of the
ingesta during the motility cycles of SACs. In contrast to
ruminants the ingesta of SACs is relatively homogenous
and there is no arrangement in layers of fluid, solid, and
gasiform ingesta as it is in ruminants (Fowler &
Bravo, 2010a). The combination of the almost continuous
motility cycles (more frequent than in ruminants) and
the anatomy of the glandular saccules allow a permanent
mixing and squeezing out of the solid ingesta (Ehrlein &
von Engelhardt, 1971; Heller et al., 1984; Vallenas, 1965;
Vallenas & Stevens, 1971; von Engelhardt &
Holler, 1982). Thus there exists an efficient condition for
the high absorptive capacity of the epithelial cells of the
glandular epithelium for a fast absorption of nutrients
(von Engelhardt & Sallmann, 1972). In this way, SACs
seem to compensate the lack of a papillated mucosa and
the, therefore, resulting surface enlargement, like it is in
the FS in ruminants. The effective mixing of the ingesta
allows an even higher amount of absorption of VFA.
According to von Engelhardt, Ali, and Wipper (1979) the

VATER ET AL.
tubular part of C3 is lined by a similar mucosa like the
glandular saccules. This mucosa structure as well results
in high absorptive capacities.
4.1.2 | Comparison to the Lama glama
and classification to a morphophysiologic
feeding type
The external and internal morphology of the alpaca's
stomach resembles that of the llama and guanaco and
that of the old world camelids (Fowler & Bravo, 2010b;
Vallenas et al., 1971). The external segmentation into
three compartments as well as the presence of an area of
saccules in the cranial and caudal sac of C1, respectively,
coincides with the existing literature about the llama and
guanaco stomach.
Being in close connection to the alpacas' feeding
behavior and morphophysiologic feeding type, there are,
however, differences in the proportion of the gastric com-
partments and the intestines between llamas and alpacas.
Overall SACs seem to have a successfully fractionated
fermentation like intermediate, opportunistic mixed
feeders (IM) such as goats (Hofmann, 1989). Vallenas
et al. (1973) already documented an extensive fermenta-
tive activity in C1, C2, the first two-third of C3, in the
caecum and proximal colon. In our previous paper we
showed that the alpaca has a shorter small intestine com-
pared to ruminants, providing more space for both of the
fermentation chambers. The colon coil of alpacas consists
of more centrifugal gyri than that of ruminants, which is
an evidence for species with a better developed DFC
(Hofmann, 1989). Besides this, the jejunum and the
ascending colon have a separated mesentery allowing
greater mobility and development of the ascending
colon's proximal loop (Vater & Maierl, 2018), which may
allow an easier seasonal enlargement of the distal fer-
mentation chamber and thus adaptation to feeding condi-
tions, especially in the dry season. During the dry
season—in the Altiplano between May to November—
the plants become more lignified and are even harder to
digest (Fowler & Bravo, 2010a).
Differences between llama and alpaca exist in the
length of some parts of the bowel. The total length of the
small intestine of the alpaca accords with that of the
llama (Fowler, 2010; Lesbre, 1903). In relation to their
body size, however, alpacas have a longer small intestine
(Vater & Maierl, 2018).
Although llamas prefer to eat tall, coarse bunch-
grasses, highly concentrated of virtually indigestible car-
bohydrates, all over the year and independent of the
season, alpacas are more selective. They prefer as long as
possible leaves, forbs, and short grasses, which are of
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2011
higher content of nutrients. With the plants becoming
more lignified in the dry season, alpacas are, however,
more opportunistic and able to use a wide variety of for-
age types, which is especially important in the dry season
(San Martin Howard, 1987; San Martín & Van
Saun, 2014).
Llamas seem to be even better adapted to an arid cli-
mate than alpacas, which is reflected in the proportions
of their digestive system. The more spacious fermentation
chambers compared to that of alpacas allow a more effi-
cient fermentation of hardly digestible carbohydrates.
Alpacas are able to modify their preferences
according to forage availability during the different sea-
sons (San Martin Howard, 1987). They seem to belong
to the intermediate feeding group more than llamas do.
Different authors stated a higher ability to digest and
lower protein and energy requirements of SACs com-
pared to sheep especially when the forage is of poor qual-
ity (Dulphy, Dardillat, Jailler, & Ballet, 1997; Lemosquet,
Dardillat, Jailler, & Dulphy, 1996; San Martin &
Bryant, 1989). Different factors seem to influence the
digestibility of forage positively. The pH and ammonia
levels are higher in llamas, whereas the VFA concentra-
tions are lower, probably linked to a more rapid absorp-
tion (Rübsamen & von Engelhardt, 1978) and a higher
water turnover. The very stable pH levels of C1 and C2
together with an excellent cellulolytic activity seem to
play a leading role during digestion of plant cell walls
(Dulphy et al., 1997; Lemosquet et al., 1996). The high
volume of buffering substances is related to a rapid turn-
over of the liquid phase, which is connected to abundant
gastric and salivary secretions rich in bicarbonate
(Rübsamen & von Engelhardt, 1979).
4.2 | Practical implications
The specific design of their gastric anatomy predisposes
alpacas for gastric ulcers, which are responsible for 6% of
fatal casualties (Cebra, 2014; Cebra, Tornquist, Bildfell, &
Heidel, 2003; Hughes & Mueller, 2008; Smith, 1989;
Smith, Pearson, & Timm, 1994). Gastric ulcers occur
in all three compartments, mostly, however, in C3
(Fowler & Bravo, 2010b).
The results of the present study show that—as it is in
the llama—there is no anatomical separation between
the FS and the hydrochloric acid-secreting hindstomach
(the distal fifth of C3). Besides this, the emptying of the
stomach happens against gravitation as the distal caudal
loop of C3 is oriented ventrodorsally and the lumen of
the pyloric orifice is quite narrow. These aspects could be
responsible for a reflux of hydrochloric acid contents or
an incomplete emptying during an atonic stomach or an

2012
ileus. Due to the lack of a gallbladder, in SACs there is a
continuous flow of bile into the duodenum. In situations
of an atonic intestine or an ileus, it could lead to a reflux
of bile and therefore foster gastric ulcers (Cebra
et al., 2003).
It is very important to avoid acidosis of the FSs
because acidosis is another reason for ulcers. When con-
centrated feed is given—which is not essential for
alpacas—it should be distributed all over the day and
enough roughage should be given in parallel (Cebra
et al., 2003).
4.2.1 | Limitations and future research
There are different limitations in this study.
First, the histological anatomy of the different mucosa
sections was not examined due to the fact that only ani-
mals were used which died or were euthanized (for medi-
cal reasons other than diseases of the GIT tract) and
subsequently donated. Thus the time between death and
dissection was too long to get meaningful histological
samples. The histological morphology and biochemical
processes along the gastric walls in the different compart-
ments of the alpaca should be one of the next research
studies to compare the alpacas' and llamas' digestion in
detail.
Second, the number of animals was too small to pre-
sent profound statistics of the results concerning the mac-
roscopic anatomy of the stomach. However, the results
obtained in this study give valuable information on the
gastric anatomy of the alpaca that has not been available
until now.
5 | C ON C L U S I ON
The gastric anatomy of alpacas resembles in most aspects
that of llamas. However, the differences in the propor-
tions of the stomach and the intestines are explainable
when considering the different feeding behaviors of
llamas and alpacas. Llamas seem to belong rather to the
grass and roughage eaters and alpacas rather to the inter-
mediate feeders. Both camelids have a relatively big distal
fermentation chamber compared to sheep or cattle; how-
ever, the stomach of the alpaca is even bigger than that
of the llama. Together with their feeding behavior, this
explains, their classification as IM.
A C K N O WL E D G E M E N T
The authors wish to thank those animal holders who
donated their euthanized animals for our research project.
They also thank Hannah Schmidt, who professionally
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VATER ET AL.
drew the schematic drawing of the stomach. Open Access
funding enabled and organized by Projekt DEAL.
CONFLICT OF INTEREST
The authors declare no potential conflict of interest.
AUTHOR CONTRIBUTIONS
Anke Vater: Conceptualization; data curation; investiga-
tion; methodology; project administration. Elisabeth
Zandt: Formal analysis; writing-review and editing; for-
mal analysis-supporting; writing-review & editing-
Supporting. Johann Maierl: Conceptualization; investi-
gation; methodology; supervision.
ORCID
Anke Lisa Vater https://orcid.org/0000-0001-7379-7987
RE FER EN CES
Alzola, R. H., Ghezzi, M. D., Gimeno, E. J., Lupidio, M. C.,
Castro, A. N., & Rodriguez, J. A. (2004). Topography and mor-
phology of the llama (Lama glama) stomach. International
Journal of Morphology, 22, 155–164.
Bohlken, H. (1960). Remarks on the stomach and the systematic
position of the Tylopoda. Journal of Zoology, 134, 207–215.
Cebra, C. (2014). Disorders of the digestive system. In C. Cebra, D. E.
Anderson, A. Tibary, R. J. Van Saun, & L. W. Johnson (Eds.),
Llama and Alpaca care (pp. 477–536). St. Louis: W.B. Saunders.
Cebra, C. K., Tornquist, S. J., Bildfell, R. J., & Heidel, J. R. (2003).
Bile acids in gastric fluids from llamas and alpacas with and
without ulcers. Journal of Veterinary Internal Medicine, 17,
567–570.
Cummings, J. F., Munnell, J. F., & Vallenas, A. (1972). The
mucigenous glandular mucosa in the complex stomach of two
new-world camelids, the llama and guanaco. Journal of Mor-
phology, 137, 71–110.
Dulphy, J. P., Dardillat, C., Jailler, M., & Ballet, J. M. (1997). Com-
parative study of forestomach digestion in llamas and sheep.
Reproduction, Nutrition, Development, 37, 709–725.
Ehrlein, H. J., & von Engelhardt, W. (1971). Untersuchungen über
die Magenmotorik beim Lama. Zentralblatt für
Veterinärmedizin, Reihe A, 18, 181–191.
Fowler, M. E. (2010). Medicine and surgery of camelids, (3rd ed.,
pp. 1–644). Ames, Iowa: Wiley-Blackwell.
Fowler, M. E., & Bravo, P. W. (2010a). Feeding and nutrition. In
M. E. Fowler (Ed.), Medicine and surgery of camelids
(pp. 17–58). Ames, Iowa: John Wiley & Sons.
Fowler, M. E., & Bravo, P. W. (2010b). Digestive system. In M. E.
Fowler (Ed.), Medicine and surgery of camelids (pp. 351–402).
Ames, Iowa: John Wiley & Sons.
Heller, R., Gregory, P. C., & von Engelhardt, W. (1984). Pattern of
motility and flow of digesta in the forestomach of the Llama
(Lama guanacoe f. glama). Journal of Comparative Physiology B:
Biochemical, Systemic & Environmental Physiology, 154,
529–533.
Hofmann, R. R. (1989). Evolutionary steps of ecophysiological adap-
tation and diversification of ruminants: A comparative view of
their digestive system. Oecologia, 78, 443–457.

VATER ET AL.
Hughes, K., & Mueller, K. (2008). Pathologic lesions of mycotic
pneumonia in an alpaca following third compartment ulcera-
tion. Journal of Veterinary Diagnostic Investigation, 20, 672–675.
Lechner-Doll, M., von Engelhardt, W., Abbas, A. M., Mousa, H. M.,
Luciano, L., & Reale, E. (1995). Particularities in forestomach
anatomy, physiology and biochemistry of camelids compared to
ruminants. Options méditerranéennes, Serie B: Etudes et
Recherches. Elevage et Alimentation du Dromadaire–Camel Pro-
duction and Nutrition, 13, 19–32.
Lemosquet, S., Dardillat, C., Jailler, M., & Dulphy, J. (1996). Volun-
tary intake and gastric digestion of two hays by llamas and
sheep: Influence of concentrate supplementation. The Journal
of Agricultural Science, 127, 539–548.
Lesbre, F. X. (1903). Recherches anatomiques sur les camélidés (Vol. 8).
Lyon: H. Georg.
Luciano, L., Reale, E., & von Engelhardt, W. (1980). The fine struc-
ture of the stomach mucosa of the Llama (Llama guanacoe).
II. The fundic region of the hind stomach. Cell and Tissue
Research, 208, 207–228.
Luciano, L., Voss-Wermbter, G., Behnke, M., von Engelhardt, W., &
Reale, E. (1979). Die Struktur der Magenschleimhaut beim Lama
(Lama guanacoe und Lama lamae), I. Teil: Vormägen.
Gegenbaurs Morphologisches Jahrbuch, 125, 519–549.
Nickel, R., Schummer, A., & Seiferle, E. (2004). Lehrbuch der
Anatomie der Haustiere. Eingeweide (Vol. 2, 9th ed., pp.1–482).
Berlin: Parey.
Rübsamen, K., & von Engelhardt, W. (1978). Bicarbonate secretion
and solute absorption in forestomach of the llama. American
Journal of Physiology-Endocrinology and Metabolism, 235, E1–E6.
Rübsamen, K., & von Engelhardt, W. (1979). Morphological and
functional peculiarities of the llama forestomach. Annals of Vet-
erinary Research, 10, 473–475.
San Martin, F., & Bryant, F. C. (1989). Nutrition of domesticated
South American llamas and alpacas. Small Ruminant Research,
2, 191–216.
San Martín, F., & Van Saun, R. J. (2014). Applied digestive anatomy
and feeding behavior. In Llama and Alpaca care (pp. 51–58).
St. Louis: W.B. Saunders.
San Martin Howard, F. A. (1987). Comparative forage selectivity and
nutrition of South American camelids and sheep (pp. 1–292).
Lubbock: Texas Tech University.
Smith, B. B., Pearson, E. G., & Timm, K. I. (1994). Third compart-
ment ulcers in the llama. Veterinary Clinics of North America:
Food Animal Practice, 10, 319–330.
19328494, 2021, 9, Downloaded from https://anatomypubs.onlinelibrary.wiley.com/doi/10.1002/ar.24588 by Readcube (Labtiva Inc.), Wiley Online Library on [07/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2013
Smith, J. A. (1989). Noninfectious diseases, metabolic diseases, tox-
icities, and neoplastic diseases of South American Camelids.
Veterinary Clinics of North America: Food Animal Practice, 5,
101–143.
Sumar, J. (2010). Nutrition in camelids (pp. 343–357). Santiago:
World Buiatrics Congress, World Buiatrics Association.
Vallenas, A. (1965). Some physiological aspects of digestion in the
alpaca (Lama pacos). In R. Dougherty (Ed.), Physiology of digestion
in the ruminant (pp. 147–158). Washington, DC: Butterworths.
Vallenas, A., Cummings, J. F., & Munnell, J. F. (1971). A gross study
of the compartmentalized stomach of two new-world camelids,
the llama and guanaco. Journal of Morphology, 134, 399–423.
Vallenas, A., Llerena, L., Valenzuela, A., Chauca, D.,
Esquerrey, J., & Candela, E. (1973). Concentración de ácidos
grasos volátiles a lo largo del tracto gastrointestinal de alpacas y
llamas. Revista de Investigaciones Pecuarias, 2, 3–14.
Vallenas, A. P., & Stevens, C. E. (1971). Motility of the llama and
guanaco stomach. American Journal of Physiology, 220,
275–282.
Vater, A., & Maierl, J. (2018). Adaptive anatomical specialization of
the intestines of alpacas taking into account their original habi-
tat and feeding behaviour. The Anatomical Record, 301,
1840–1851.
von Engelhardt, W., Ali, K., & Wipper, E. (1979). Absorption and
secretion in the tubiform forestomach (compartment 3) of the
llama. Journal of Comparative Physiology, 132, 337–341.
von Engelhardt, W., & Heller, R. (1985). Structure and function of
the forestomach in camelids-a comparative approach. Acta
Physiologica Scandinavica, 124, 85–85.
von Engelhardt, W., & Holler, H. (1982). Salivary and gastric physi-
ology of camelids. Verhandlungen der Deutschen Zoologischen
Gesellschaft, 75, 195–204.
von Engelhardt, W., & Sallmann, H. (1972). Resorption und
Sekretion im Pansen des Guanakos (Lama guanacoe).
Zentralblatt fur Veterinarmedizin Reihe A, 19, 117–132.
How to cite this article: Vater AL, Zandt E,
Maierl J. The topographic and systematic anatomy
of the alpaca stomach. Anat Rec. 2021;304:
1999–2013. https://doi.org/10.1002/ar.24588