Camelid placentation; the llama

Keywords: Llama, camelid, placenta, anatomy, parturition.

Note: The term chorioallantois is commonly accepted and is seldom hyphenated i.e. chorio-allantois. However, terms such as chorio-amnion and amnio-allantois are not commonly used. Therefore they have been hyphenated in this entry to clarify their composition.

Placentation in the llama (and all camelids) is a source of fascination for those who are familiar with the placentation of horses and cattle. In a manner of speaking, it is a hybrid of both, yet distinctly different. The camelid chorion is similar to that of horses i.e. diffuse and epitheliochorial. Although the two look similar macroscopically, llamas have small, rugaevilli (squat projections with folded or ridged surfaces) rather than the microcotyledons seen in horses. The superficial appearance of a llama placenta is seen below. Note too, how small areas of the chorion are devoid of rugaevilli. Local absence of microcotyledons is a common feature of equine placentation as well. In both horses and camelids, these are normal and probably occur where the chorion has folded on the endometrial surface.

Fig 1. Image size: 1122 x 791px

The internal structure of camelid placentation (illustrated in the next image) is very different to that of horses. In horses, the amnion is separated from the chorion completely i.e. it is "a balloon within a balloon". The fetus lies within the central balloon (the amnion) tethered to its inner surface by the intra-amnionic cord. The central "balloon" is then tethered to the chorion by the continuation of the umbilical cord (minus the urachus) i.e. the extra-amnionic cord. See this entry and another, illustrating the equine anatomy elsewhere in LORI. Readers will note that the allantois in horses lines the space surrounding the amnion, separating it completely from the chorion. This explains why there is no such structure as an amnio-chorion in horses. Yet, that label appears in the image of the llama placenta shown above. This is because the allantois in camelids lies adjacent to the amnion; it does not surround it. This is similar to the situation in cattle where the allantois also lies adjacent to the amnion and does not surround it either. In both camelids and cattle therefore, there is a section of the amnion that lies against the chorion and this is the amnio-chorion. See figure 2

Fig 2. Image size: 2732 x 1835 px.

During foaling and calving, the chorioallantois ruptures and a large amount of fluid escapes from the vulva before the amnion appears at the vulva lips.  This is because the chorioallantois abuts the internal cervical os in horses and cattle. Although the chorion also lies against the internal cervical os in camelids, it is the amnion, not the allantois, that lies adjacent the chorion in this area. See figure 2. Therefore, when the chorion ruptures in camelids, the allantois does not rupture at the same time. As a result, large volumes of allantoic fluid are not discharged before the amnion become visible at the vulva lips. Instead, the allantois its bypassed by the fetus in its amnion although a large area of the amnion is still attached to the allantois over an area known as the amnio-allantois. See figure 2. The transparent amnion pushes through the cervix and soon appears at the vulva lips, the fetus visible within.

After the fetus has been born, the bluish allantoic fluid can be seen within the chorion, at the vulva lips, yet to be expelled. The allantois is visible through the wall that was formed by the fusion of the amnion and allantois i.e. the membrane mentioned in the previous paragraph, the amnio-allantois (see Fig 2&3).

Below, a dead fetus (washed and devoid of its epidermal membrane) placed within the opened placenta to show the relationship between the fetus and the fetal membranes:

Fig 3. Image size: 990 x 616 px.

Notes  Although ovulation occurs with equal frequency from both ovaries, the fetus almost always lies in the left uterine horn (see figures 2 & 3). Also, camelids are like horses, with the vast majority of births in cranial, longitudinal presentation and dorso-sacral position. Normal posture is the same as for cattle and horses.  In brief, parturition takes place in the morning and the female usually stands throughout second stage. Second stage is usually completed within 20 minutes but takes significantly longer in primipara. The placenta is usually expelled with the chorion on the outside but occasionally, inside out.  As for all herbivores, hippomanes are occasionally found within the allantois. Although there is one report of hippomanes in the amnion, this seems unlikely; perhaps a feature of errant handling of fetal membranes during inspection.

Selected references

Fowler M.E. and Olander H.J.  1990. Fetal membranes and ancillary structures of llamas (Lama glama) Am.J. Vet. Research. 51: 1495-1500

Fowler M.E. 2011. Medicine and Surgery of Camelids.  John Wiley & Sons. ISBN: 0470961694, 9780470961698

Morton. W.R.M. 1961 Observations on the full term foetal membranes of three members of the camelidae (Camelus dromidarius L. Camelus bactrianus L. and Lama glama L)

J. Anatomy 95: 200-209

Epidermal membrane (epithelion) on a llama cria

Keywords: Llama glama, llama, epidermal, camel, membrane, neonate, camelid

In both old and new world camelids, neonates are covered by a thin membrane at birth. This is most commonly referred to as the epidermal membrane (EM) but in piglets where it is also present (see Pearson, M.J. et al. 2015) it has been referred to as an epithelion. The latter term is certainly not commonly used, either with regard to pigs or when discussing camelid reproduction.

The image below shows the thin EM, partially covering the body of a cria. During late gestation the EM is relatively thick, becoming thinner towards term. At term it is thin, friable and easily brushed off by the neonate itself during vitalization.  It was only because this fetus died during or shortly after birth, that the EM was partially intact.

Image size: 2000 x 1400 pixels

Below, a term male llama delivered per vagina. Death due to dystocia. A good example of the EM in a fresh state.

Image size 1692 x 1272 px

The EM is perhaps 1 to 2 mm thick at most. It is comprised of keratin, resembling the epidermis when examined histologically. It contains very few nucleated cells. The EM starts to form early in gestation as an additional layer to the epidermis, being pushed away from the skin as hairs begin to form. By the end of the first trimester to mid gestation, it is obvious on gross examination of the fetus.

Image size: 1200 x 985 pixels

The EM attaches to the mucocutaneous junctions, doing so at the mouth (as shown above), nostrils, eyes, prepuce, vulva and anus. (below). Therefore the functions of these orifices are not impeded by its presence. There is for example, no chance that the EM will cause peripartum asphyxia.

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As is shown below, the EM does not cover the claws either. It is attached only as far distal as the coronary bands.

Image size: 1000 x 492 pixels

In all camelids, amniontic fluid is thought to be less viscous and lubricating than it is in most other animals. This leads to the logical assumption that the EM (which is extremely slippery when wet) assists in lubricating the fetus during its passage through the birth canal.

Selected references

Fowler, M.E. and Olander, H.J. 1990 Fetal membranes and ancillary structures in llamas (Lama glama). Am J Vet Res 51: 1495-1500

Holubar, K. and Schmidt, C. 1994. Dermato-pathologia 1792 and Henry Seguin Jackson (1750?-1816): a bicentennial. J. Royal Society of Medicine. 87:464 (The epithelion is mentioned in this paper)

Merkt. H. et al. 1988. The presence of an additional partial membrane and its function in the newborn guanaco (Lama guanacoe). Theriogenology. 30:437-439

Pearson, M.J. et al. 2015. Gross and histological description of the epidermal membrane found on normal neonatal piglets. Lab animal 44: 445-447

Llama. Male genitalia

Keywords: Llama, camelid, new world, male, penis, genitals, prepuce, testicles, testes

The image shows the genitalia of a newborn male llama.  Note the long inguinal canal.

Image size: 1685 x 973 pixels

The tip of the penis in all camelids is directed caudally, therefore they are retromingent animals. However, the shaft of the penis is directed caudal-to-cranial. After copulation, the penis is withdrawn by retractor penis muscles (see image). Note the use of the diminutive form of testes (testicles) in this image.

The camelid penis is fibro-elastic like that of a bull but its sigmoid flexure is cranial to the scrotum, more like that that of a boar than a bull. In all camelids, the penis ends in a short cartilaginous process. This process is perhaps, essential for cervical penetration and intra-uterine ejaculation, the latter being unique among domestic animals. The cartilaginous process develops with age and was therefore not obvious in this neonate.

Camelid testes are located in a non-pendulous scrotum ventral to the anus.  After experience with other animals, an examiner is struck by how small the testes of new world camelids are in proportional to the body weight of the adult male. In adult male llamas for example, the testes are usually 5.0 to 7.0 cm long and 2.5 to 4.0 cm wide.  Corresponding measurements for alpaca testes are 3.5 to 5.0 cm long and 2.0 to 3.5 cm wide.  Accessory sex glands are palpable transrectally in large males but (like felids) only the prostate gland and a pair of bulbourethral glands are present.

Lymphoma in an alpaca

Keywords: alpaca, camelid, lymphoma

With thanks to Dr Andrea Bourque DVM ACVP for the pathology contribution to this description.

The uterus of a 16 year old alpaca in moderate to poor body condition was submitted for pregnancy diagnosis. Her body weight was 82Kg. Feed intake could not be accurately determined but the animal was reported to lag behind others when the herd was called for feeding. Otherwise, she was bright, alert and responsive and able to rise and ambulate normally. The owners believed that she may be pregnant because a male had been with the herd for an extended period of time.

On transabdominal and transrectal ultrasonic examination, no pregnancy was visible. Instead, large highly echogenic masses were seen to surround the uterus and adnexa. Vacuolated, fluid-filled non-echogenic areas were present within the masses. These are shown here:

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In one cross-section of one of the uterine horns, a solid and vacuolated mass appeared to impinged on the lumen (outlined below). Indeed. later post mortem examination showed this to be case.

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Due to the absence of pregnancy, a strong possibility of neoplasia and the advanced age of the animal, she was euthanized and submitted for postmortem examination. The images below show masses of what appeared to be lymphoma-like tissue in the myometrium and uterine adnexa. The ovaries were not affected. Note the thick mass of tissue being incised; contiguous with, and adjacent to the left uterine horn.

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There was also a large retroperitoneal mass which surrounded (but did not invade) the kidneys and adrenal glands and extended caudally to the pelvic inlet.  It is shown below

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This locally invasive tumor also invaded and markedly expanded the wall of a large segment of distal colon and much of the reproductive tract extending from the mid vagina, encompassing the cervix, uterine body and adjacent uterine horns (sparing the terminal portions of the horns).  Otherwise, neoplastic infiltrates were not seen elsewhere. This distribution was supported by histopathology.  

The microscopic features of this tumor are shown below. 

Image size: 1000 x 753px

Small foci of lytic necrosis and hemorrhage were scattered within the mass. The tumor cells had large round to oval to sometimes reniform nuclei with variably prominent nucleoli, coarsely stippled chromatin, and small amounts of poorly defined, pink-grey, cytoplasm. Anisokaryosis (yellow arrows) was moderate. Mitotic figures (black arrows) were present in very high numbers (approximately 160 in 10 HPF). Occasional binucleate cells were also noted.