THE ANATOMICAL RECORD (2018)

Adaptive Anatomical Specialization of

the Intestines of Alpacas Taking into
Account their Original Habitat and
Feeding Behaviour
ANKE VATER * AND JOHANN MAIERL
Department of Anatomy, Histology and Embryology of the Ludwig-Maximilians-University
of Munich, Veterinärstr.13, 80539, Munich, Germany

ABSTRACT
The gastrointestinal tract of the alpaca (Vicugna pacos) is most efficiently
adapted to its habitat at high altitudes. Alpacas, just like ruminants, feed on
hardly digestible forage. However, it has been demonstrated that the anatomy
of the camelid digestive tract has developed independently of ruminants and
not in homology to them. Despite a long history of domestication and an
increasing number of animals worldwide, little research has been done on the
intestinal anatomy of alpacas. The purpose of this study was to describe the
anatomical features of the alpaca’s intestines and to explain anatomical pecu-
liarities in the context of evolutionary function and morphology. Another goal
of this study was the demonstration of weaknesses of the intestinal anatomy
predisposing alpacas to certain clinical presentations. Six animals were used
for dissection. The basic structure of the intestines was comparable to that in
ruminants. However, a number of characteristic peculiarities were found in
alpacas, like the duodenal ampulla and the proximal and distal loop of the
ascending colon. The jejunum and ileum, unlike those of ruminants, had their
own mesentery largely separated from the ascending mesocolon. The main
blood supply was provided by the cranial and caudal mesenteric artery. The
particular lymph nodes were located along the branches of these two arteries.
The spiral colon seemed to play a major role in intestinal digestion and water
resorption. The size of the distal fermentation chamber allows the presumption
that alpacas belong to the group of animals practicing a fractionated fermenta-
tion in the proximal and distal fermentation chambers. Anat Rec, 2018. © 2018
Wiley Periodicals, Inc.

Key words: topographical anatomy; virtually indigestible for-

ages; distal fermentation chamber; intestinal anatomy

INTRODUCTION healthy animal and indicates potential vulnerabilities

within the intestinal tract. Comparison with the intes-
Examination of the anatomy and topography of the tines of different ruminant species reveals the character-
intestines provides useful insight into the anatomy of a istic adaptation of alpacas to their individual habitats.

Abbreviations: C1 = Compartment 1 of the stomach; CFG = Munich, Veterinärstr.13, 80539 Munich, Germany. Tel.: +49
Centrifugal gyri of the ascending colon; CPG = Centripetal gyri (0) 89/2180–2660. E-mail: [email protected]
of the ascending colon; CS = Concentrate selectors; DFC = Distal Received 11 July 2017; Revised 4 January 2018; Accepted 29
fermentation chamber; GIT = Gastrointestinal tract; GR = Grass January 2018.
and roughage eaters; IM = Intermediate, opportunistic mixed DOI: 10.1002/ar.23863
feeders; SACs = South American camelids Published online 00 Month in Wiley Online Library (wileyonline-
*Correspondence to: Anke Vater, Department of Anatomy, His- library.com).
tology and Embryology of the Ludwig-Maximilians-University of

© 2018 WILEY PERIODICALS, INC.

2 VATER AND MAIERL

TABLE 1. Length specifications of the intestines in total and the small and large intestines of alpacas, llamas
and old-world camelids, as listed by different authors
Species Alpaca Llama Old World Camelids
Author (Gusmán Chaves, 1970) (Lesbre, 1903) (Fowler, 2010) (Lesbre, 1903) (Smuts and Bezuidenhout, 1987)
Total length 22.9 27.7 19.0–19.5 35.0–48.0 59.5
Small intestine 13.4 15.8 11.5–12.0 22.0–25.0 40.0
Large intestine 9.5 11.9 7.6 13.0–23.0 19.5

Habitat and Feeding Behavior • “grass and roughage eaters” (GR): adapted to fibrous for-
The following paragraph describes the individual habi- age, rich in plant cell walls (cellulose, hemicellulose);
tat and feeding behavior of llamas and alpacas, which is e.g. cattle, sheep
directly connected with the peculiarities of the species’ • “concentrate selectors” (CS): adapted to easily digestible
intestinal anatomy. forage, rich in plant cell contents (solubles); e.g. moose,
In South America, alpacas live mainly in the Altiplano
at altitudes above 3,800 m in a semi-arid climate consist-
roe deer
ing of a long dry season (May to November) and a shorter • “intermediate, opportunistic mixed feeders” (IM): adapted
wet season (December to April) (Fowler, 2010). As a to a mixed diet, but avoiding fibers for as long as possible
result of these climatic conditions, alpacas are forced to (opportunistic foraging); intermediate between GR and
forage high amounts of fibrous plants with many struc- CS; e.g. goat, red deer
tural carbohydrates in the plant cell walls that are hard
to digest. Throughout most of the year, i.e. during the dry IM and CS are characterized by a fractionated fermen-
season, the plants become more lignified making them tation in a proximal fermentation chamber (PFC, rumi-
even harder to digest. In addition, the animals are forced noreticulum) and a distal fermentation chamber (DFC,
to store fat deposits during the wet season that can be cecum and colon), which are both well developed in these
mobilized during the lean times of the dry season when two groups. GR, in contrast, have a very large PFC and a
vegetation is sparse and of poor nutritional quality less developed DFC (Hofmann, 1989).
(Fowler, 2010). According to Sumar (2010), SACs can also be classified
During the wet season, which is also the growing sea- under the intermediate feeders.
son, alpacas prefer mainly tall grasses, forbs and leaves, Anatomy of the gastrointestinal tract of SACs.
whereas during the dry season, they feed mainly on short Most of the existing literature describes general ana-
grasses. Llamas (Lama glama), however, prefer taller tomical aspects of the gastrointestinal tract of llamas,
and coarser bunch grasses (more lignified), even in the guanacos and SACs.
rainy season (San Martin and Bryant, 1989). The intestines of camelids consist of a small and a
In addition, water resources are very scarce in the large intestine. The lengths of the bowel sections are
semiarid climate, which is why South American camelids listed in Table 1.
(SACs) need to handle very economically with their water The duodenum begins with a prominent dilatation, the
balance. For example, camelids are extremely good at duodenal ampulla, and winds around toward the caudodor-
reabsorbing water from their spiral colon (Whitehead, sal abdominal wall caudoventral to the liver and encircles
2013). Over 25% of the water entering the colon is the mesentery root. The subsequent, strongly tortuous
absorbed before defecation (compared to 10% in cattle) jejunum is located in the right caudal part of the abdomen.
and pelleted feces already begin to form in the spiral It is followed by the short ileum, which joins the large
colon (Cebra, 2014). intestine at the ileocolic junction. The relatively small
cecum lies near the linea alba, its blind end mostly
directed toward the pelvic cavity (Lesbre, 1903; Vallenas,
Morphophysiological Feeding Types 1991; Fowler, 2010). According to Fowler (2010) and Cebra
It is important to know as much as possible about the (2014), the ascending colon consists of a proximal loop, a
digestion of the animals and to identify their appropriate spiral loop and a distal loop, whereas Lesbre (1903)
morphophysiological feeding type. This knowledge is described the proximal loop as being part of the spiral loop
instrumental in improving the animals’ correct feeding (Lesbre, 1903). The spiral loop is mostly located in the
and welfare in captivity (Stangassinger, 2007).When midventral abdomen and has five centripetal (CPG) and
wrongly fed especially in areas with high-quality forages five centrifugal (CFG) loops (Van Hoogmoed et al., 1998;
and no lean times, alpacas often have problems of obesity Fowler and Bravo, 2010; Stieger-Vanegas and Cebra,
(Fowler, 2010; Sumar, 2010). The same objective of the 2013). Cebra (2014), on the other hand, reported an incon-
process of rumination of SACs and ruminants—successful sistent location of the spiral colon, caused by the long mes-
fermentation of plant cell wall materials—should allow entery. The transverse colon passes from right to left,
comparison and classification of the gastrointestinal cranial to the cranial mesenteric artery and continues as
tract and feeding behavior of SACs into the morphophy- the descending colon and rectum and finally ends in the
siological feeding types for ruminants described by Hof- anus (Fowler, 2010). The jejunum, ileum, cecum and
mann (1989). ascending colon are supplied with blood by branches of the
Hofmann divided ruminants into three different over- cranial mesenteric artery, while the descending colon and
lapping groups of morphophysiological feeding types: rectum are supplied by the caudal mesenteric artery.
 THE INTESTINAL ANATOMY OF ALPACAS 3
Several studies have dealt with the radiological exami- TABLE 2. Breed, sex, age, weight and reason of
nation of the gastrointestinal tract of llamas and alpacas: euthanasia of the individual animals
Timm et al. (1999) investigated the abdomen of neonatal
llama crias with normal and contrast-enhanced Reason for
Breed Sex Age Weight euthanasia
radiography.
Cebra et al. (2002) described the transabdominal, Huacaya Female 3.5 years 55 kg Mandibular
ultrasonographic appearance of the viscera of llamas and neoplasia
alpacas. Van Hoogmoed et al. (1998) and Stieger-Vanegas Huacaya Male adult 72 kg Aggressiveness
(exact age
and Cebra (2013) examined the gastrointestinal tract of
unknown)
alpacas and llamas using contrast-enhanced computed Huacaya Female 20 years 44 kg Death of old age
tomography and Anderson et al. (1996) described laparo- and emaciation
scopic approaches to the llama’s abdomen and its normal Huacaya Female 6.5 months 25 kg Suspicion of
laparoscopic anatomy. Endoparasites
(no apparent
abnormalities
Diseases of the GIT of the GIT and
Diseases of the gastrointestinal tract are one of the the ingesta
main reasons for veterinary diagnostics and therapy in during dissection)
Suri Male 18 years 40 kg Acute blindness
SACs and account for one of the main causes of death in Huacaya Female 5 years 52 kg Weakness and
camelids (Shapiro et al., 2005; Theuß et al., 2014). In the recumbency
past, most efforts to reduce these fatalities focused on the
medical control of gastric ulceration (Cebra et al., 1998).
However, ulcerative diseases are responsible for less than
a third of all fatal outcomes attributable to gastrointesti- Fixation
nal diseases in llamas and some of these deaths could Before dissection, the arterial vascular system of the
have been prevented by surgical intervention not only in animals was injected with a 50% alcohol–water solution
the gastric region but also in the intestines, for example via the right common carotid artery. The animals as well
via surgical removal of an intestinal trichophytobezoar as the extracted organs were stored in a 10% NaCl solu-
(Kennel and Wilkins, 1992). tion to which 0.005% formaldehyde was added, and refrig-
The aim of this study was first to work out a systematic erated at 4  C during the dissection period.
first basis of the topography and morphology of the abdo-
men of the alpaca and then zoom in on the intestines in
an attempt to find correlations between anatomy and Preparation of the Arterial Vascular System
digestive physiology. with Latex Milk
In two animals, the arterial vascular system was
MATERIALS AND METHODS injected with latex milk (La-Gum, 25,335 Elmshorn).
Material About 600 mL of red latex milk was injected into the
right common carotid artery. In one of the animals, the
Two male and four female Alpacas aged from 6 months right femoral artery was ligated, while in the other ani-
to 18 years were used for anatomical preparations. All mal both femoral arteries were ligated before injection to
animals were euthanised for reasons which did not influ- ensure enough pressure being built up so that even the
ence our results (Table 2). None of the animals showed smallest vessels of the organs were injected. The animals
apparent abnormalities during dissection. were then cooled down to 4  C for 3 days allowing the
latex milk to harden.
Euthanasia
The animals were euthanised by veterinarians at the Photographic Documentation
animals’ home stable or in the Clinic for Ruminants, An SLR camera (Olympus® Digital ED with an
Oberschleissheim. Animals were injected with pentobar- Olympus® Zuiko Digital ED 14–42 mm f3.5–5.6 lens and an
bital (Euthadorm, 400 mg mL−1®; CP-Pharma 31,303 Olympus® Zuiko Digital 35 mm f3.5 macro lens; Olympus
Burgdorf; 1–2 mL/10 kg/BW) via the jugular vein. The Deutschland, 20,097 Hamburg) was available. A polarizing
alpacas were transported to the dissection hall (of the filter (Hama®,86,653 Monheim, PL CIR  58 (IV) and  52)
chair of anatomy, histology and embryology of the LMU) was used to avoid highlights on the preparations.
in left lateral recumbency. The pictures were taken in front of a black foil and
using a tripod.
Anatomical Dissection Images were edited afterwards with Adobe® Photo-
shop® (Dublin 24, Republic of Ireland).
The usual methods and instruments of preparation
were used. First, the topography of the abdominal and
RESULTS
pelvic cavity was examined, photographed and documen-
ted. In different animals, various approaches to the The (small + large) intestines of the alpaca had a mean
abdominal cavity were selected in such a way that pic- length of 21.60  2.82 m (Table 3). The small intestine
tures were taken from the ventral view as well as from began with the duodenum at the pylorus, followed by the
the right and the left lateral view. Then the stomach and jejunum and ileum. Its mean diameter ranged from
intestines were removed for individual examination. 1.4  0.3 to 2.7  0.3 cm depending on the bowel’s section.
4 VATER AND MAIERL

TABLE 3. Length (m) and diameter (mm) specifications of the bowel sections

Length (m) Diameter (cm)

Absolute length (m) mean  SD % of the total length mean  SD
Duodenal ampulla 0.1 0.10  0.02 0.5 2.7  0.3
Duodenum 1.0–1.5 1.10  0.22 5.3 1.4 0.3
Jejunum 7.0–15.0 10.70  3.18 49.5 1.8 0.3
Ileum 0.3–0.5 0.40  0.084 1.7 1.8 0.2
Cecum 0.1–0.2 0.19  0.05 0.9 3.8  0.5
Proximal loop of the ascending colon 1.3–1.4 1.37  0.02 6.4
Cecal (orad) 3.6  0.3
Spiral (aborad) 1.6  0.3
Spiral loop of the ascending colon 4.5–6.2 5.15  0.71 23.8 1.1  0.2
Distal loop of the ascending colon 1.3–1.5 1.38  0.07 6.4 1.2  0.2
Transverse colon 0.3–0.5 0.29  0.15 1.3 1.3  0.0
Descending colon 0.5–0.6 0.58  0.02 2.7 1.8  0.2
Rectum 0.3–0.4 0.34  0.22 1.6 3.5  0.3
Total length 18.8–25.5 21.60  2.82

The large intestine started with the cecum, merging into the a festoon. Because of the large stomach, the jejunum was
ascending, transverse and descending colon (Figs. 1–3). mainly located in the right caudal part of the abdomen,
The duodenum was separated from the pyloric region reaching the ventral abdominal wall as well as the dorsal
by a prominent torus pyloricus, followed by a constriction abdominal wall. It surrounded the right kidney and cau-
that significantly reduced the lumen. The duodenum dally reached the pelvic cavity.
started with a sack-like bulge, the duodenal ampulla The last part of the small intestine, the ileum, was
(length: 0.10  0.02 m, width: 2.7  0.3 cm) and had a located at the margin of the long mesentery loop of the
mean length of 1.10  0.22 m (Fig. 3). jejunum. It lay between jejunal loops on top of the ventral
The duodenal ampulla turned into the cranial duodenal abdominal wall. It was attached to the large intestine
flexure at the level of the 1st lumbar vertebra, merging into and its lumen opened via the ileal orifice, located at the
the strongly tortuous descending portion of the duodenum. border between the cecum and the ascending colon. Its
This part of the duodenum ran caudodorsally and lay orad beginning was marked by the ileocecal fold on the
between the first compartment of the stomach (C1) on the gut’s antimesenterial side connecting the ileum and the
left side and the visceral surface of the liver on the right cecum. It had a length of 0.40  0.084 m.
side. It was fixed to the dorsal abdominal wall by a long cra- The cecum was relatively small with a length of
nial mesoduodenum, which reached the middle of the right 0.19  0.05 m and a width of 3.8  0.5 cm. It was located
abdominal wall in four animals. The right lobe of the pan- in the ventral part of the abdomen in the median plane.
creas was embedded in the cranial mesoduodenum. The Its blind end pointed cranially in most of the animals
hepato-pancreatic duct led into the duodenum about 16 cm with slight divergences to the left or right lateral side.
aborad from the duodenal ampulla. It had an intramural The ascending colon emerged from the cecum at the level
course of 30 mm, ending on the major duodenal papilla. of the ileal orifice and had the same diameter as the cecum.
The beginning of the duodenum was connected to the Initially, it formed the almost circular proximal loop of the
liver by the hepatoduodenal ligament, forming the caudal ascending colon (Ansa proximalis coli). This loop framed a
part of the lesser omentum. The descending portion of the double-sided serous membrane, forming the mesentery for
duodenum rose dorsally and passed the cranial mesenteric the following colon coil, to which it was attached. The diam-
root on its right, its mesentery getting shorter. The final eter of the colon coil constantly decreased from
part of the distal portion of the ascending colon (Ansa dis- 3.6  0.3 cm at the proximal loop of the ascending colon
talis coli) was attached to the mesentery of the descending (orad) to 1.6  0.3 cm at the central flexure (aborad) (Flex-
portion of the duodenum and was located between this ura centralis). The colon coil was formed by a long double-
part and the mesenteric root. Caudal to the mesenteric armed loop and consisted of 4 1/2 centripetal and 4 1/2 cen-
root, the descending portion turned into the transverse trifugal loops excluding the proximal loop. The correspond-
portion of the duodenum, heading to the left and leading ing centripetal and centrifugal loops were positioned on top
to the ascending portion of the duodenum. The turning of each other like a pyramid. The central flexure was
point was at the level of the caudal extremity of the right located at the center of the coil and marked the transition
kidney at the 5th lumbar vertebra. This U-shaped part of from the centripetal gyri to the centrifugal gyri.
the duodenum lay directly ventral to the caudal vena cava The colon coil rotated clockwise around its supplying ves-
and the aorta, touching the adrenal glands and kidneys. sels, so that the initial part of the proximal loop of the
The transition into the jejunum was formed by the duode- ascending colon ran dorsally on the right side and turned
nojejunal flexure, which turned ventrally. The ascending around the supplying vessels to the ventral side again.
portion of the duodenum was tightly attached to the des- Because of this rotation the colon coil was directed toward
cending colon on its left side by the duodenocolic fold. the left abdominal body wall in most of the animals. In
The jejunum was the longest part of the intestines with some animals it faced the ventral body wall as well (Fig. 4).
a length of about 10.70  3.18 m. The first section of the The outermost centrifugal gyrus merged into the distal
jejunum was linked to a short mesentery, but the mesoje- loop of the ascending colon which passed to the left side
junum quickly became longer and formed an elongated of the mesentery of the jejunum, forming a final loop
mesentery loop framed by the jejunum and the ileum like there. Then it turned dorsally to the level of the
 THE INTESTINAL ANATOMY OF ALPACAS 5

Fig. 1. Schematic drawing of the intestines, its supplying arteries and lymph nodes. For reasons of clarity only the supplying vessels to the
centrifugal loops of the colon coil are shown. DA, Duodenal ampulla; DLAC, Distal loop of the ascending colon; CFG, Centrifugal gyri; CPG,
Centripetal gyri; PLAC, Proximal loop of the ascending colon. (a) cranial mesenteric artery; (b) caudal pancreaticoduodenal artery with two branches
for the duodenum and one for the jejunum; (c) middle colic artery with two branches for the transverse colon, one branch for the DLAC and one for
the descending colon; (d) jejunal branch; (e) right colic arteries; (f) ileocolic artery, (g) jejunal artery; g1, distal part of the jejunal artery, (h) cecal
artery; (i) ileal artery; (j) colic branches (CPG + PLAC) and right colic arteries (CFG); (k) aorta; (l) caudal mesenteric artery; (m) left colic artery; (n)
cranial rectal artery; (o) left external iliac artery; (p) left internal iliac artery; (q) cranial gluteal artery; (r) vaginal/prostatic artery; (s) caudal gluteal
artery; (t) caudal rectal artery; (u) internal pudendal artery; (v) medial sacral artery.

duodenum and ran cranially, connected to the mesenteric passed to the left side cranial to the mesenteric root and
root on its left side and to the descending portion of the merged into the caudally oriented descending colon. The
duodenum on its right side. As the transverse colon, it initial part of the descending colon was connected to the
6 VATER AND MAIERL

Fig. 2. Overview of the intestinal bundle arranged on one level. AC, Ascending colon; C, Cecum; D, Duodenum; DC, Descending colon; DLAC,
Distal loop of the ascending colon; I, Ileum; J, Jejunum; PLAC, Proximal loop of the ascending colon; S, Spleen; SC, Spiral colon.

ascending portion of the duodenum on its right side by parts of the duodenum, the initial part of the jejunum and
the duodenocolic fold and formed a sigmoid flexure. The the pancreas. The next branch was the middle colic artery
descending colon was fixed to the dorsal abdominal wall supplying the transverse colon, the distal part of the
by a short mesentery, which finally became longer again ascending colon and the initial part of the descending colon.
immediately before entering the pelvic cavity, forming Further branches were the 3–4 right colic arteries to
the sigmoid flexure (Ansa sigmoidea). Toward the pelvic the centrifugal gyri of the spiral colon.
cavity the descending colon was surrounded by fat tissue. The next larger branch was the ileocolic artery, passing
The rectum was covered by peritoneum as long as to the proximal loop of the ascending colon. It supplied
6–7 cm from the anus. In Figures 5–7 the topography of 4–5 colic branches for the centripetal gyri of the spiral
the abdominal viscera is shown from the ventral, right colon and the distal part of the jejunal artery. The distal
and left lateral view. part of the jejunal artery gave off the ileal artery to the
Table 3 shows the total lengths and diameters of the ileum and the cecal artery to the cecum. The cranial mes-
bowel sections as well as the mean and standard enteric artery merged into the proximal jejunal artery,
deviations. anastomosing with the distal part of the jejunal artery.
The jejunal artery ran along the jejunum in an arc, sup-
plying numerous short vessels for the jejunum.
Vascularisation of the Intestines
The right colic arteries and the colic branches were
The intestines were mainly supplied with blood by the intertwined in a clockwise direction. The blood supply of
cranial and caudal mesenteric arteries (Fig. 2). Vessels the descending colon and the rectum occurred via the cau-
from a different origin were also found at the beginning dal mesenteric artery, which divided into the left colic
and the end of the gut. The initial part of the duodenum artery and the cranial rectal artery. The very caudal end
was supplied by the gastroduodenal artery, a branch of of the rectum was supplied by the caudal rectal artery.
the coeliac artery, while the very caudal end of the rec- The cranial rectal artery turned caudally to the dorsal
tum was supplied by the caudal rectal artery. side of the rectum and almost reached the anus, supply-
Close to its origin the cranial mesenteric artery gave off ing numerous small vessels to the rectum on its way.
the caudal pancreaticoduodenal artery for the different After delivery of the cranial rectal artery the aorta
 THE INTESTINAL ANATOMY OF ALPACAS 7

Fig. 3. Transition from C3 to the duodenum with the duodenal ampulla from the outside (A) and the same section turned inside out (B). C1, C3,
Compartment 1 and 3 of the stomach; D, Duodenum; DA, Duodenal ampulla.

supplied the left and right external iliac arteries and The venous drainage of the intestines took place via
finally divided into the left and right internal iliac arter- the portal vein. The portal vein collected the blood from
ies and the medial sacral artery. The internal iliac arter- the cranial and caudal mesenteric veins, which received
ies gave off the vaginal/prostatic artery, the caudal their blood from the different veins of the abdominal vis-
gluteal artery and a small caudal rectal artery for the cera. These veins had the same course as their respective
most caudal aspect of the rectum. arteries and were named after these.

Fig. 4. The intestinal bundle with the spiral colon arranged as it would be located in the abdomen: the spiral colon is rotated clockwise around its
supplying blood vessels (Right lateral view). C, Cecum; AC, Ascending colon; CF, Central flexure; D, Duodenum; DLAC, Distal loop of the
ascending colon; I, Ileum; J, Jejunum; P, Pancreas. PLAC, Proximal loop of the ascending colon; S, Spleen; SC Spiral colon.
8 VATER AND MAIERL

Fig. 5. Left lateral view of the viscera of the caudal abdomen. C1, Compartment 1 of the stomach; PLAC, Proximal loop of the ascending
colon; S, Spleen; SC, Spiral colon.

From the hepatic hilus the portal vein coursed inside the Two to three cecal lymph nodes were attached to the ileo-
margin of the hepatoduodenal ligament until it reached the cecal fold. Two lymph nodes were located directly under
dorsal aspect of the pancreas. There it parted into the cau- the vessels for the colon coil and one lymph node was hid-
dal mesenteric vein, the lienal vein and the different den inside the colon coil. Two to three caudal mesenteric
branches for the stomach, which ran parallel to their respec- lymph nodes for the drainage of the descending colon
tive arteries. The oval shaped epiploic foramen was located were located around the caudal mesenteric artery.
caudal to the liver between the caudal vena cava dorsally
and the portal vein ventrally at the level of the 1st lumbar
vertebrae. It had a length of 40 mm and a width of 20 mm. DISCUSSION
In this study, we examined the morphology and topo-
graphic anatomy of the abdominal viscera of the alpaca as
Lymph Nodes a functional unit together with their supplying vessels,
The small intestine and the ascending colon were lymph nodes and their anatomical position in relation to
drained by the cranial mesenteric lymph center, which each other. The purpose was to give detailed descriptions of
consisted of the duodenal lymph nodes, the jejunal lymph the intestines, to compare them with the intestines of other
nodes, the cecal lymph nodes and the colic lymph nodes. ruminant species and to find correlations between peculiar-
They were grouped around the branches of the cranial ities of different intestinal sections and feeding behavior.
mesenteric artery. The jejunal lymph nodes occupied the
largest part of the cranial mesenteric lymph center.
Theoretical Implications
Numerous small lymph nodes were located in the mesen-
tery of the most orad part of the jejunum next to the jeju- First, the existing literature mostly describes the anat-
nal wall. Three to four bigger lymph nodes were found in omy of the llama or of SACs in general, although the
the center of the elongated mesentery loop of the jejunum. alpaca and the llama belong to different genera and have
 THE INTESTINAL ANATOMY OF ALPACAS 9

Fig. 6. Ventral view of the abdominal viscera. C, Cecum; C1, C3, Compartment 1 and 3 of the stomach; L, liver; PLAC, Proximal loop of the
ascending colon; SC, Spiral colon.

different habitats and feeding behaviors. To the authors’ To correctly assess the proportions of the mesentery of
knowledge, the topographic anatomy of the intestines of the jejunum and the spiral colon, it should be kept in mind
alpacas in particular has not been described to date. The that the spiral colon is not attached to the jejunal mesen-
present study as such provides in-depth insight into the tery but that it has its own mesentery. Cebra (2014)
anatomical peculiarities of this genus. explained that the long mesenteric attachment of the
Second, our work brings together and completes differ- ascending colon, due to its pendulous nature, is prone to
ent individual aspects of the intestinal anatomy, which, rotate around its root or become entrapped whenever there
in the existing literature were partly incomplete and con- is an unoccupied point in the abdomen, for example the epi-
sidered isolated from one another. Our research presents ploic foramen, a mesenteric rent, a defect in the body wall
a comprehensive overview of the intestines in relation to or diaphragm or a tight band formed by fibrous adhesions.
their supplying blood vessels and their lymphatic system. Third, the findings facilitate a thorough comparison of
The intestines of alpacas have an anatomical topogra- the alpaca’s anatomy with that of the llama, old-world
phy that is similar to that described in previous studies camelids and different ruminants.
about the anatomy of the dromedary (Smuts and Bezui- San Martín and Van Saun (2014) reported that due to
denhout, 1987), the camel (Lesbre, 1903) and SACs the lack of knowledge about the applied digestive anat-
(Vallenas, 1991; McCracken et al., 1999; Fowler, 2010). In omy of SACs, feeding practices were extrapolated from
most aspects the topography also corresponds to the other ruminating species such as cattle and sheep. The
results of the few radiological and laparoscopic studies unique anatomy and metabolism of SACs, however,
(Anderson et al., 1996; Van Hoogmoed et al., 1998; Cebra require a specific approach to correct feeding. Our results
et al., 2002; Stieger-Vanegas and Cebra, 2013). The spiral in connection with some aspects of the digestive physiol-
colon was most often found to be located on the ventral ogy and the feeding behavior described in literature show
abdominal wall (Van Hoogmoed et al. (1998), Stieger- that classification of SACs into a particular group of mor-
Vanegas and Cebra (2013), Fowler and Bravo (2010)), phophysiological feeding behavior according to Hofmann
although Cebra (2014) reported multiple different topo- (1989) is not obvious. SACs share numerous similarities
graphic locations for the spiral colon. In our animals, the with other ruminants, but also show a number of unique
location of the spiral colon varied from the ventral abdo- features in terms of anatomy and metabolism. It is
men to the right dorsal body wall. This variation might equally important to understand that there are even sig-
be explained by the long mesentery and the lack of fixa- nificant differences in feeding behavior between llamas
tion of the spiral colon to the dorsal body wall. and alpacas.
10 VATER AND MAIERL

Fig. 7. Right lateral view of the abdomen. C1, C3, Compartment 1 and 3 of the stomach; D, Duodenum; DC, Descending colon; DP,
Diaphragm; J, Jejunum, K, Kidney; L, Liver, L1, L4, L7, Lumbar vertebra 1, 4 and 7, T6, T9, T12, Thoracic vertebra 6, 9, 12.

The fibrous and virtually indigestible forage available coil serves as a principle delay mechanism. The higher
to SACs during the dry season of the year requires an the number of coils, the longer is the retention time of
adaptation of the gastrointestinal tract similar to that of ingesta in the DFC which is necessary for effective cellu-
ruminants belonging to the category of grass and rough- lolysis (Hofmann, 1989).
age eaters (GR), such as cattle and sheep. One of their Another conspicuous difference in intestinal anatomy
most important digestive tasks is cellulolytic fermenta- between alpacas and that of other ruminants lies in the
tion. GR, in particular cattle, solve this problem by means presence of a separate mesentery for the jejunum and the
of a huge proximal fermentation chamber, the ruminoreti- ascending colon in alpacas, allowing more mobility and
culum. Their distal fermentation chamber (DFC) of GR is development of the proximal loop of the ascending colon
shorter than that in CS and IM because the DFC in GR is and the spiral colon. This specific adaptation also sug-
only used when required (Hofmann, 1989). gests an important role of the DFC for alpacas, may pro-
The forage of SACs in their natural habitat is even vide a better adaptation of the intestines to seasonal
more lignified and more difficult to digest. Moreover, fluctuations of forage quality and may allow an easier
SACs are less selective in their forage than for example seasonal enlargement of the DFC. This fits in with obser-
sheep, which select more easily digestible fibers than vations that SACs exhibit higher digestibility than rumi-
SACs. SACs hence need an additional mechanism to nants when consuming low quality forages, whereas
digest fibrous material. Vallenas et al. (1973) documented digestibility of higher quality forage is similar between
high fermentative activity in C1, C2, and the first 2/3 of SACs and ruminants. The higher digestibility is related
C3 and in the cecum and proximal colon. Our results to a longer retention time of the ingested forages, provid-
show that the ascending colon in particular, representing ing more time for microbial degradation of the cell walls
the DFC in alpacas, is longer than that of cattle and (San Martin and Howard, 1987).
sheep. The colon coil of alpacas consists of 4 ½ CFG and The general structure of the intestines is similar in
CPG, whereas cattle only have 2 ½ to 3 coils each (Nickel alpacas and llamas although there are some differences in
et al., 2004). A higher number of spiral colon coils is a the length of some parts of the bowel. The small intestine of
typical feature of species with a better developed DFC. the alpaca has almost the same total length as that of the
Apart from ensuring propulsion, the tight concentric colon llama (Lesbre, 1903; Fowler, 2010). In relation to their body
 THE INTESTINAL ANATOMY OF ALPACAS 11
size, however, alpacas have a longer small intestine. jejunum or displacement of parts of the jejunum through
Alpacas avoid hard-to-digest fibers for as long as possible, the epiploic foramen, leading to life-threatening conditions
preferring leaves and forbs instead, whereas llamas prefer such as a volvulus with a strangulating ileus. The colon coil
to graze in dry areas dominated by tall and coarse bunch of the ascending colon, which is not directly attached to the
grasses, even during the rainy season. Llamas appear to be dorsal abdominal wall is prone to displacements and tor-
even better adapted to an arid climate than alpacas and sions as well (Cebra, 2014). The only fixed point is a small
their digestive system is better suited to deal with these area next to the transition of the cecum into the ascending
conditions, as also seen in old-world camelids (San Martín colon and the supplying blood vessels. The variable position
and Van Saun, 2014), i.e. a more efficient microbial fermen- of the ascending colon that deviates from lying directly on
tation of hardly digestible carbohydrates and more spacious the ventral abdominal wall or even next to the right latero-
fermentation chambers compared to alpacas. dorsal body wall is also important for abdominal ultra-
Alpacas, however, exhibit the most opportunistic feed- sound examination or for surgical approaches. The long
ing behavior compared to llamas and sheep, preferring mesentery of these intestinal sections also offers advan-
grasses and wetland conditions with more easily digest- tages for the surgeon: it simplifies the systematic investiga-
ible carbohydrates and avoiding fibers for as long as pos- tion of patients suffering from colic diseases as the
sible. They are able to modify their preferences according intestines can easily be displaced from the abdominal cav-
to forage availability and are hence capable of consuming ity. Thus, surgical correction of gastrointestinal lesions can
a wide variety of forage types (San Martin and Howard, be performed more easily. Cebra et al. (2014) showed that
1987). Alpacas as such seem to belong to the intermediate sections of the colon, for example the spiral colon, can be
feeding group more than llamas do. successfully resected.
Comparing alpacas to domesticated ruminants, their Second, distinct sections in the ascending colon, in
feeding behavior resembles that of goats, whose original which the luminal diameter rapidly narrows, are more
habitat was characterized by high altitudes and barren sensitive to invaginations, obstipation through concen-
landscapes with changing forage quality throughout the trated and dry intestinal content or obturations through
year (Hofmann, 1989). Goats have the longest ascending foreign bodies or phytobezoars. These narrow passages
colon (4 CFG and 4 CPG) of all ruminants in relation to are located directly aborad to the prominent torus pylori-
their body size and are best capable of macerating cellu- cus, aborad to the duodenal ampulla, in the transition
lose with the help of microorganisms (Nickel et al., 2004). between the proximal loop of the ascending colon to the
We have shown that the ascending colon with the spiral spiral colon and in the central flexure.
colon is the longest part of the colon in alpacas. Its size cor- Third, the supplying blood vessels of the ascending
relates with its highly important functions. In addition to colon are very long because of the evolutionary extension
functioning as a second fermentation chamber, the ascend- of the ascending colon. Torsions of the colon coil can inter-
ing colon needs to efficiently reabsorb water in the spiral rupt the blood supply, leading to hemorrhagic infarction
colon as an adaptation to the sparse water resources of the of the wall of the intestines.
semi-arid habitat of alpacas (Whitehead, 2013; Cebra,
2014). The longer the spiral colon the more surface and Limitations and future research. There are several lim-
time for water and electrolyte absorption exists (Hofmann, itations to our study.
1989). Formation of pelleted feces starts in the proximal First, we examined the animals solely anatomically.
spiral colon (Fowler, 2010). Camels are able to reduce the For a medical investigation and for a correct diagnosis, in
water content of feces and increase the concentration of particular in animals suffering from colic diseases, an
urine to minimize excretion of vital fluid during heat stress. ultrasound examination is essential, because a rectal
Thus, they are capable of passing completely desiccated examination is not possible due to the size of the animals.
feces when water intake is restricted. The water content of Comparison of anatomical cross sections with ultrasound
the feces of SACs is higher than of that of old-world came- images, which would help veterinary medical students
lids (Fowler, 2010) but SACs may share the ability to con- and practitioners evaluate the health status of an alpaca
trol the water content of their feces. correctly, does not exist. Filling this information gap
should be one of the next steps.
Practical Implications Second, we investigated only the macroscopic and not
the microscopic anatomy due to the fact that our animals
The physiological anatomy and topography of the intes- were not animals for slaughter but animals that had been
tines of the alpaca have a number of weak points which euthanised for medical reasons other than diseases of the
are predispositions to different kinds of gastrointestinal gastrointestinal tract. Thus, the time between death and
diseases and potential causes of colics in camelids dissection of the animals was too long to obtain meaning-
(Whitehead, 2013). ful histological samples.
Cebra et al. (1998) described typical intestinal features of Third, the number of dissected animals was too small
camelids that probably correlate with typical gastrointesti- to permit a real sound statistical analysis of the results.
nal problems observed in these animals. Our results con- However, the results presented in this study provide
firm these features for the alpaca in particular. valuable information on the anatomy of the alpaca that
First, there are the distinctive conditions of the mesen- was not available to date.
tery of the intestines. The jejunum has its own mesentery
and is quite long. Only the beginning and the most aboral
CONCLUSION
part of the jejunum are relatively constant. The remaining
part is variable in its position and loops of the jejunum can The overall intestinal anatomy of the alpaca is similar
be found almost anywhere within the caudal half of the to that of the llama. Differences exist in the length of
abdomen. The long mesentery allows torsions of the some bowel sections, which probably reflect different
12 VATER AND MAIERL

feeding behaviors and better adaptation of llamas to arid Kennel A, Wilkins J. 1992. Causes of mortality in farmed llamas in
conditions. The intestines of the SACs in general seem to North America. Necropsy findings from the database of a major
be very well adapted to the harsh conditions of the high insurer. Int Llama Assoc 1–3.
Lesbre FX. 1903. Recherches anatomiques sur les camélidés. Lyon:
altitudes of their original habitats in Southern America
H. Georg.
with the long period of low quality forages and poor water McCracken TO, Spurgeon TL, Kainer RA. 1999. Spurgeon’s color
resources. atlas of large animal anatomy: The essentials. Philadelphia:
These anatomical adaptations, however, also cause cer- Wiley-Blackwell.
tain sections of the intestines to be prone to the above- Nickel R, Schummer A, Seiferle E. 2004. Lehrbuch der Anatomie der
mentioned gastrointestinal diseases. Haustiere. Eingeweide Berlin: Parey.
For suitable husbandry, further studies about the phys- San Martin F, Bryant FC. 1989. Nutrition of domesticated South
iology, applied anatomy and the correct feeding of ani- American llamas and alpacas. Small Ruminant Res 2:191–216.
mals in captivity are still necessary. San Martin F, Howard A. 1987. Comparative forage selectivity and
nutrition of South American camelids and sheep. In: Lubbock:
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AUTHORS’ CONTRIBUTION San Martín F, Van Saun RJ. 2014. Applied digestive anatomy and
feeding behavior. Llama and Alpaca Care. St. Louis: W.B. Saun-
AV: dissections, data interpretation, writing of the text.
ders. p 51–58.
JM: critical revision, approval of the manuscript. Shapiro JL, Watson P, McEwen B, Carman S. 2005. Highlights of
camelid diagnoses from necropsy submissions to the Animal Health
ACKNOWLEDGEMENTS Laboratory, University of Guelph, from 1998 to 2004. Can Vet J 46:
317–318.
The authors wish to thank those animal owners who Smuts MMS, Bezuidenhout AJ. 1987. Anatomy of the dromedary.
donated their euthanised animals for the research project Oxford: Oxford University Press.
and they also thank Hannah Schmidt, who drew the sche- Stangassinger M. 2007. Zur Bedeutung der Nahrungsfaser für die
matic drawing of the intestines for them and Alina Niel- Entwicklung und Funktion des Verdauungstraktes beim Wieder-
sen, who digitally edited the sketch. käuer. In: Plitzner C, Kraft M, Windisch W, editors. Austria:
The authors have no conflict of interests to declare. BOKU-Symposium Tierernährung. p 25–32.
Stieger-Vanegas SM, Cebra CK. 2013. Contrast-enhanced computed
tomography of the gastrointestinal tract in clinically normal
alpacas and llamas. J Am Vet Med Assoc 242:254–260.
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