Order: Artiodactyla
Family: Camelidae

1) General Zoological Data

Camelidae are thought to have originated in North America (Nowak, 1999; Tibary, 1997) but disappeared there approximately 10,000 years ago. The Bactrian camel and the dromedary are the largest of these species, and they are confined to Asia/Africa. They hybridize freely to produce the "Tulu". The large camels are widely used as pack animals, and for races, especially the dromedary. Hybrids of these two species are fertile. The wild Bactrian camel of the Gobi desert has been markedly reduced in numbers in recent years (Hare, 1997). It is smaller than the Bactrian (two-humped) camel seen in zoos, and grayer. With RFLPs of Bactrian camels, Vidal-Rioja et al. (1994) assessed their relation to the South American camelids. The common ancestor was estimated to have existed 5-10 MYA and some hybridization profiles were completely identical, others differed. The llama was believed to have differentiated from guanaco ancestors; the vicuña was found to be quite species-specific in these studies, perhaps further justifying its separation from Lama. These studies suggested that alpaca might have derived from hybridization between guanaco and vicuña. The study of the full sequence mtDNA (of the cytochrome b gene) by Stanley et al. (1994) confirmed the diversification of camelids that had been suggested from fossil records. In addition to these considerations, there are numerous "breeds" of dromedary, listed comprehensively by Tibary (1997).

The South American camelidae also hybridize freely, and the hybrids are fertile as well (Gray, 1972). The original wild South American camel may have been the guanaco, of which several subspecies are now recognized. Whether the vicuña should be assigned as subspecies of the llama is disputed.

The most remarkable hybridization of a female dromedary with semen from a guanaco was reported by Skidmore et al (1999). Despite numerous attempts, only one live offspring was obtained. Hybridization in the other direction, while successful with pregnancies resulting, did not yield a live calf. These authors estimated that effective reproductive isolation between these species had existed for at least 11 million years, thus making this artificial hybrid all the more remarkable.

Aside from their long necks, fine wool, specific hoof structure, and ruminant three-chambered stomachs, camelidae are especially noteworthy because of their oval erythrocytes. These red blood cells are also enormously expansible. In sections they appear similar to sickle cells of humans.

All of these animals are widely distributed in zoological parks, except for the uncommon vicuña. Its precarious status in Peru was well detailed by Hoffman (2001).

Bactrian camel: Adult weight is 300-690 kg; gestational length 360-440 days; usually a single young, very rarely twins; newborn weight is 37 kg; placental weight 4.2 kg; life expectancy is 50 years.

Dromedary: Adult weight is 300-560 kg; gestational length 350-404 days; usually single offspring weighing 26-45 kg; rare twins occur but they usually abort.
Guanaco: Adult weight is 100-120 kg; gestational length is 345-360 days; single young weigh 8-15 kg; longevity is 28 years.

Llama: Adult weight is 130-155 kg; length of gestation is 342-355 days; life span is at least 20 years; twins occur occasionally, with rare freemartinism. Neonatal weights are 8.6 - 14.9 kg (mean 11.98 kg). Placental weight is 0.74 - 1.4 kg (mean 1.0 kg). Size of placenta: 196-280 x 23 - 40 cm.

Alpaca: Adult weight is 55-65 kg; length of gestation is 342-345 days; neonatal weight is 8-9 kg; single young are born, but twins are often conceived. One placenta obtained weighed 1.5 kg (see below).

Vicugna: Adult weight is 35-65 kg; gestational length is 330-350 days; single young weigh 4-6 kg; life expectancy is more than 28 years in captivity.

A comprehensive and superbly illustrated review of all aspects on Camelidae has been published by Tibary (1997). I owe much information to this author, as well as some of the illustrations. Fowler (1998) has produced a comprehensive review of "Medicine and Surgery of South American Camelidae" and he has kindly provided slides of llama placentas.

2) General Gestational Data

Camelidae are seasonal breeders (Sghiri & Driancourt, 1999), and "reflex ovulators" (Shalash & Nawito, 1964). This is further detailed in the section on endocrinology below. Since many animals are now being bred by assisted reproductive technology (ART), oocyte retrieval and their maturation have been of interest. These parameters were critically assessed by Abdoon (2001). Semen storage and acquisition are described by Bravo et al. (2000a). The growth of the alpaca embryo and fetus can now also be followed by transrectal ultrasonography (Bravo et al., 2000b). This has led to the more frequent identification of twin gestations; frequently, however, one twin is lost spontaneously. Embryos can first be detected on day 22 following ovulation. Gazitua et al. (2001) provided data for an accurate determination of llama and alpaca fetal age. Amoroso (1952) and others have suggested that the diffuse epitheliochorial placentation of camelidae is most similar to that of the pig.

3) Implantation

Early blastocysts of camelidae are spherical. In time, however, they elongate enormously, as is illustrated by Tibary (1997). Fixation to the uterus of the elongate blastocyst (that has lost its zona pellucida) begins on day 20 after fertilization of camels. Implantation occurs around day 30. In alpaca and llama, implantation may be somewhat earlier, on days 20-22, according to Tibary (1997). A majority of implantations occurs in the left uterine horn, although ovulation occurs equally commonly in right and left ovaries (Ghazi et al., 1994; Skidmore et al., 1996; Tibary 1997; Sumar, 1999). Embryos placed into the right horn subsequently migrate to the left horn. The fetus lies in the left horn, but the chorion and the large allantoic sac extend early into the other uterine horn. By day 14 after copulation, the trophoblast has come to be closely approximated to the uterine epithelium, with microvillous interdigitations between the two epithelia having become well developed by day 25. Thus, a diffuse epitheliochorial placenta develops. The trophoblast is mostly unicellular, with the exception of numerous irregularly-spaced multinucleated trophoblastic giant cells. Skidmore et al. (1996) found these giant cells to be located over the mouths of glands in their young, implanted, specimens that were fixed in situ. They did not know their function. Gorkhovskii et al. (1975), however, stated that the giant cells were polyploid due to endomitosis and speculated that they had an endocrine function. Our studies also show numerous multinucleated trophoblastic giant cells. They were frequently, but not always, located at the tips of villi in the delivered placentas. Indeed, many trophoblastic cells have multiple nuclei, while others have enlarged nuclei. Klisch et al. (2005) have done additional studies and showed conclusively that the giant cells derive by mitotic polyploidization and are indeed polyploid cells.

Abd-Elnaeim et al. (1999) provided an even more detailed examination of the early stages of trophoblastic contact. They differentiated areas of much microvillous interdigitation as well as areas of "smooth adhesion". In later stages, grooves and ridges form in the allantochorion and endometrium that provide folds and greater surface exchange areas.

Skidmore et al. (1996) published an excellent study of the early dromedary placental development with precise dating of their specimens (14-56 days after ovulation). This publication also provided some outstanding macroscopic photographs of the implanted placenta and fetus. At 14 days, the trophoblast was extremely attenuated and closely applied to the endometrial epithelium. By day 25, the trophoblast has become much taller and allantoic blood vessels are evident. These studies identified syncytial cells by day 35 - so-called giant cells - that lay opposite the endometrial glandular openings. The authors presented additional findings that convincingly demonstrate the origin of the giant cells from fusion of trophoblastic epithelium. The formerly larger yolk sac had nearly totally regressed by day 56 when both uterine horns were filled with membranes. In the 56-day specimen, the authors found the earliest development of "areolae", regions of active endometrial secretion, with modification of the trophoblastic cover, a feature seen in pigs and other species. Unlike the findings in the pig, these areas allow the development of trophoblastic giant cells. Clear evidence of protein uptake was not present. In a detailed study with vascular injection of plastics, Abd-Einaeim et al. (2003) found the vascular arrangement of maternal and fetal vessels similar to that of pig areolae. Skidmore et al. (1996) emphasized that the giant cells of camelidae are different from those found in rodents, and that they are also unlike the binucleate cells of ruminant placentas. The function of these giant cells is still uncertain. They persist to term and do not posses the cytological machinery needed for steroid or protein secretion.

4) General Characterization of the Placenta

The unusual placentas of the camelidae have been well described by Fowler & Olander (1990). These authors also provided the weights for llama placentas as being 0.7-1.4 kg (mean 1 kg). The placenta of a Bactrian camel that I observed recently weighed 4,260 g, measured 207 cm in length and 60 cm in greatest width. The umbilical cord was 63 cm long. Another placenta of a Bactrian camel weighed 7,250 g, measured 240x35 cm in dimensions and 0.3 cm in thickness. Its umbilical cord was 51 x 5 cm and covered with dark skin-like squamous tissue. A large fragment of brown hippomanes was present as well. The placenta of a term alpaca became available through the courtesy of Dr. Michelle Kutzler at Oregon State University. The 10 year-old female had delivered five previous offspring; the current placenta weighed 1,500 g, the neonate was 8 kg; the dam weighed 95 kg and the gestation was 11 months and 11 days long.

The placentas of all camelidae are thin and completely covered by villi. Separate cotyledons do not exist, although discrete "papillary excrescences" are apparent in scanning EM photographs (Fowler, 1990). These photographs of scanning EM show clearly that there are round, nodular groupings of villi, interspersed by relatively avillous regions. Such an area is shown in one of the following photographs. The placenta of all camelids is epitheliochorial and non-invasive. Fowler & Olander (1990) considered the focal areas of "folded papillation" to correspond to placentomes of other species.

5) Details of fetal/maternal barrier

Many details of the fine structure of camelid placentas have been described in the previous section. It therefore does not need to be repeated here. There are some additional details worthy of note, however. Ghazi et al. (1994) found binucleate as well as mononucleate trophoblast in their electron microscopic study. These were not detailed in an earlier fine-structural analysis of the alpaca placenta by Steven et al. (1980). Moreover, Skidmore et al. (1996) are adamant that the giant cells that they described, are different from the characteristic ruminant binucleate cells. There is no doubt, however, that in the mature camelid placenta some binucleated cells exist. I also interpret them as being different from the distinct binucleate cells of the usual ruminant placenta. For one thing, they are not so distinctly different from the remainder of trophoblast. More likely they are intermediates to the more common multinucleated giant cells. This is so, as they often also they contain three or four nuclei before they become the true, easily distinguished multinucleated cells. These features are shown in the subsequent photographs. Capillaries deeply indent the two epithelial layers (Steven et al., 1980), thus reducing the distance between the two circulations to as little as 2 microns. The rich vascularization of the trophoblastic epithelium is very striking in all camelid placentas. Several authors have commented on this phenomenon and speculated that it is beneficial to fetal development at high altitude. Nevertheless, it also occurs at sea level and in Old World camels, and is thus not necessarily induced by low ambient oxygen pressures.

Mossman (1987) described PAS-positive "absorptive" trophoblastic regions. Tibary (1997) mentioned the existence of a "diffuse" syncytial epithelium. That has not been my experience, nor is it mentioned in other publications. In fact, the detailed electron microscopic study by Steven at al. (1980) identified the trophoblast as being single-layered and covered with microvilli. The fetal endothelium was described as being extremely attenuated. The microvilli are in close contact with the microvillous surface of the uterine epithelium. On delivery, separation of the placenta occurs at this interface, thus, this is a non-deciduate placentation. In fact, the trophoblast of delivered camelid placentas is often cuboidal and, in other regions it is cylindrical with vacuolar cytoplasm.

Jones et al. (2000) showed that there is great variation in the glycosylation of the placental surfaces, inferring that this has significance in the prevention of interspecific breeding. They showed that the sialic acid components of camelidae differs significantly from those of equid species.

After describing the appearance of the dromedary placenta during the first one-half of pregnancy, van Lennep (1963) reported on its appearance during the second half of gestation. The material was well preserved and came from animals harvested in Australia. He described the extremely complex branching of villi and three types of trophoblastic cells: Cuboidal, tall columnar, and giant cells. Frequent intermediates between the first two types occurred. There were fewer giant cells than present in the first trimester placentas. They possessed a brush border and were indented by fetal capillaries.

I had the good fortune to obtain the slides of a delivered, full-term neonatal alpaca placenta from Dr. Hailu Kinde (UC Davis, CA). These slides are somewhat remarkable in having regions of much more solid trophoblast. I assume these areas to correspond to the round nodules seen by scanning EM and described above. Moreover, the well-fixed organ has numerous multinucleate trophoblastic cells, alternating with single-nucleated trophoblastic cells. "Typical" binucleate cells (as seen in other ungulates) were not found.

6) Umbilical cord

The umbilical cord of camelidae is long; Tibary (1997) stated lengths up to 110 cm. The most recent placenta of a Bactrian camel that I have observed had a 63 cm long umbilical cord. It had four blood vessels and a large allantoic duct. Elastic tissue preparations by Ghazi et al. (1994) showed few such fibers in the blood vessels. The epithelium lining the allantoic duct is transitional (urothelial) or, occasionally, squamous in nature. Numerous small blood vessels are found throughout the cord substance, some with much musculature. There are many, usually clockwise spirals of the umbilical cord. The photograph of an immature llama fetus depicted by Fowler & Olander (1990) had a few cord spirals. The cord of llamas is 30-50 cm long and 2-3 cm in diameter (Fowler & Olander, 1990).

7) Uteroplacental circulation

I know of no studies, other than the anatomical descriptions of female genitalia published by Tibary (1997).

8) Extraplacental membranes

The yolk sac placenta was examined by Shagaev & Baptidanova (1976). They identified the yolk sac at 22-24 days of conception, and the yolk sac placenta at 27-28 days. Their study indicated that it "functions for a long time". This contrasts with the description of Skidmore et al. (1996) who depicted only a small remnant of yolk sac by day 56 in the dromedary.

The camelid amnionic and allantoic membranes are constructed as they are in most other mammals. There are no "free" membranes, as the entire placenta is covered with villi and trophoblast. Hippomanes are commonly found in the allantoic sac. The most unusual feature of camelid placentas is the presence of an "epidermal membrane" (also called "fourth" membrane). It is composed of squamous cells only, adheres to the mucocutaneous junctions of the fetus, and it is presumed to be a derivative of the squamous surface of the embryo. It dries quickly after birth, is fragile and has an unknown function (Fowler & Olander, 1990; Fowler, 1998). It is more of a pseudomembrane, as it has no connective tissue. The amnion has small foci of squamous metaplasia. Steven et al. (1980) described the alpaca amnionic epithelium as being composed of stratified squamous epithelium, six to eight cells thick. It is not clear, however, whether this applies to the actual amnion or to the "fourth" membrane, as these authors did not describe the latter. Most likely, the fourth membrane was studied by these authors electronmicroscopically. There is no decidua capsularis.

9) Trophoblast external to barrier

There is no uterine invasions of trophoblast.

10) Endometrium

The histologic parameters of the reproductive tracts of female llamas were presented in great detail by Tibary (1997), and also by Feder et al. (1999). The camelid placenta is adeciduate.

11) Various features

There is neither a subplacenta nor are there metrial glands.

12) Endocrinology

Camelidae are "induced ovulators", i.e. only after mating is the follicle released, and only then is impregnation possible (see review by Sumar, 1999). Another useful review of camel reproduction that discusses endocrine findings is by Al Eknah (2000). Zhao et al. (2001) fractionated the proteins of seminal plasma from Bactrian camels; they identified a distinct LH-releasing activity in the "third of five fractions" of the semen that they held responsible for ovulation. There was no response of FSH secretion by any of the seminal fractions. In other studies, these authors measured LH and FSH in pregnant camel sera. They thus identified a significant LH peak on the day of insemination, with a gradual fall during pregnancy. The South American camelidae have been shown to be susceptible to superovulation with pFSH and eCG, with successful fertilization following (Correa et al., 1997). Tibary (1997) presented much of the endocrine patterns of camelidae.

Leon et al. (1990) were among the first to record a rise of progesterone levels 5 days after mating, and the fall of progesterone that occurs shortly before parturition. They observed a 350 day length of gestation. The changes that occur in endocrine patterns after mating were recorded by Aba et al. (1995) and, in alpacas, by Raggi et al. (1999). They observed LH concentration and PGF2 alpha to be significantly elevated immediately after copulation, with progesterone first observed to rise on day 4. Luteolysis was due to PGF2 alpha, usually after 8 days of the existence of a corpus luteum. Skidmore et al. (1998) made further observations on the effect of prostaglandins. Skidmore et al. (1996), as well as Zhao et al. (1998), measured progesterone and estrogens during pregnancy. The placenta is said to have the ability to aromatize androgen precursors. Ratto et al. (1997) detailed the ovarian response of llamas to treatment with pFSH (superovulation).

Bravo et al. (1992) examined the pituitary response to repetitive copulation and GnRH injections in South American camelidae. Only the first copulation, or GnRH injection, yielded an ovulatory response. In a later publication (Bravo et al., 1996) these investigators showed that serum relaxin concentration is a "superior indicator of pregnancy after the second month". They also identified two peaks of estrone sulfate in urine. The source of relaxin was identified by Hombach-Klonisch et al. (2000) as coming from ovarian luteal cells and endometrium; the trophoblast and the placental giant cells did not contain the hormone expression.

Nasr et al. (1996) examined the influence of carazolol on placental separation. Normally, this occurs in 49 hours. With administration of the drug it was reduced to 33 hours.

13) Genetics

All camelidae have 74 chromosomes with a very similar morphology (Benirschke, 1967; Hungerford & Snyder, 1966). Hybridization of DNA on chromosomes, especially the satellite regions and C-band, by Vidal-Rioja et al. (1987), showed significant homologies among New World camelids. Detailed studies of mtDNA by Quan et al. (2000) of domesticated Bactrian camels led the authors to suggest that two major genotypes can be differentiated. Lin et al. (2001) examined the interspersed repetitive elements (SINE) of camelids, compared these with 14 other orders, and suggested from the results that camels were the first to branch from the original stock of camelidae, to be followed by vicuñas and llamas. Rieder et al. (2000) showed that genetic markers of New World camelids exist that allow identification of individuals and differentiation among breeds.

X-monosomy in an infertile llama with infantile reproductive organs was reported by Hinrichs et al. (1997). Other intersex states are listed under the section of pathology below. Freemartinism with XX/XY blood chimerism in fraternal twins was described in a llama by Hinrichs et al. (1999). The animal had hypoplastic external genitalia.

14) Immunology

Because of the high neonatal mortality from infectious diseases of camels, Kamber et al. (2001) studied the immunoglobulin G (IgG) supply by colostrum to newborns. The colostrum was found to have higher IgG concentrations than that of horse and cattle. The conclusion was reached that low intake of colostrum rather than low IgG was responsible for the neonatal mortality.

The immunoglobins of camelidae are unusual in that the antibody molecules lack light chains, being composed solely of heavy chains (Muyldermans, 2001; Spinelli et al., 2001).

15) Pathological features

All authors who discuss the gestational aspects of camelidae are impressed with the frequency of fetal deaths. The reason for these failures is usually obscure. Hanichen & Wiesner (1995) provided an overview of New World camelid deaths in zoos. Gastric phytobezoars, infectious diseases, and foam cell granulomas of the pleura were identified. A statistical survey of camelid deaths in the UK also showed a significant perinatal mortality (Davis et al., 1998). A survey of diseases in Jordanian dromedaries lists a 98% infection with intestinal parasites, 33% nasal myasis, and 44% hydatid cysts (Al-Rawashdeh et al., 2000; see also Elamin et al., 2001 for prenatal infection with hydatid cysts). Sarcoptic mange and trypanosomiasis were similarly frequent. Dromedaries often died from pneumonia and had gastric foreign bodies in 22% of cases. Griner (1983) cautions that phytobezoars, so commonly found in camelidae, should not be mistaken for foreign bodies. He also reported on the frequency of small lipid ?tumors of the liver, additional rare proliferative lesions, and on the occurrence of occasional congenital anomalies. In Ethiopia, Tefera & Gebreah (2001) identified trypanosomiasis, camel pox, skin parasites and balantidiasis as major problems. Testing for antibodies against Brucella on 64 camels yielded negative results (El-Ansary et al., 2001). In California, where numerous llamas are being bred and kept as pets, coccidioidomycosis has been a significant health problem (Fowler et al., 1992). Wright et al. (1998) published the results of a survey among breeders of South American camelids in the UK. Neonatal mortality was a prominent problem for those breeders as well. Acute placentitis due to infection with Encephalitozoon cuniculi has recently been described in an alpaca by Webster et al. (2008). The organisms were confined to the trophoblast, were not found within the prematurely-born fetus, and the placental surface was covered with exudates.

The ovaries of the camelidae are partially enclosed in a bursa. Tibary & Anouassi (2001) identified an unusual "malformation" which they described as hydrobursitis. It is a collection of fluid that envelops the ovary and is responsible for sterility and abortions. Surgical ablation has some beneficial results. A remarkable case of peritonitis in a llama was described by Bedford et al. (1996). In this case, the placenta had entered the peritoneal cavity through a vaginal tear that occurred during delivery.

Kinne & Wernery (2002) studied the prevalence of coccidiosis (largely Eimeria sp.) in a large population of dromedaries in Dubai. They found 60% of camels older than one year had intestinal Eimeria cameli infection. In addition, many animals suffered subsequently enterotoxemia due to clostridia.

Sex reversal of a 74,XX, phenotypically male animal (with testes) was described in a llama by Wilker et al. (1994). In another case (Drew et al., 1999), multiple anomalies were present, a remnant of the Y-chromosome was excluded, and ovarian rather than testicular tissue was present. Lopez et al. (1998) reported another intersex llama with urinary obstruction. Tibary (1997) recorded many additional pathologic conditions of gestation and of the female reproductive tract. These include placentitis due to a variety of organisms. Freemartinism has been referred to above.

16) Physiologic data

Normal biochemical and hematological values of "racing dromedaries" were provided by Mohamed & Hussein (1999). Blood lipids were examined at different ages by Nazifi et al. (2000). There was a significant rise with age of cholesterol, triglyceride and HDL-cholesterol; LDL-cholesterol decreased. Cortisol levels were measured in alpacas around parturition and during weaning by Bravo et al. (2001). They were elevated in newborns and on the day of parturition.

In view of the peculiar nature of the red blood cells of the camelidae, the study by Warda & Zeisig (2000) is especially interesting. They examined the composition of the dromedary red cell membranes. There was 28.8% sphingomyelin, 12% phophatidylcholine, and phosphatidylserine each. Because of the shorter and less saturated fatty acid chains that they identified, the dromedary red cell membranes are more "fluid" than those of human red cells. Perhaps this explains their remarkable stretchability. Omorphos et al. (1989) found that the ellipsoid shape of camel erythrocytes is very stable and that the cytoskeleton differs from that of human red cells. In my experience, camelid red cells may expand with distilled water to 400% before they rupture. Asiatic camels also have a more rapidly moving front of G-6-PD on electrophoresis than the American camelids (Benirschke, 1967).

17) Other resources

Cell cultures of most camelidae can be obtained from the "Frozen Zoo" at CRES through contacting Dr. Oliver Ryder at: oryder@ucsd.edu.

18) Other remarks - What additional Information is needed?

There are only sparse records of the length of umbilical cords and placental weights. The function of multinucleate trophoblast remains unclear. Hormonal assessment of the placenta is incomplete.

Acknowledgement

Most of the animal photographs in these chapters come from the Zoological Society of San Diego. I appreciate also very much the help of the pathologists at the San Diego Zoo. The macroscopic pictures of the various placentas are a gift from Dr. Ahmed Tibary.

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