Infertility in Female Llamas

David E Anderson, D.V.M., MS, Diplomate ACVS
College of Veterinary Medicine
The Ohio State University, Columbus, Ohio

Many veterinarians and owners of llamas do not feel comfortable working with females that do not become pregnant after breeding. This may be because breeding management and reproductive physiology in llamas differs significantly from cattle, sheep, goats, and horses. Llamas breed sitting in sternal recumbency and are induced ovulators (ovulating only after transcervical stimulation). Despite these differences, veterinarians should approach the diagnosis of infertility in llamas from a "warm blooded mammal" standpoint. After ruling out common problems, more species specific problems can be investigated.

BODY CONDITION SCORING FOR BREEDING STOCK

Llamas' reproductive efficiency can suffer from poor body condition as do all livestock species. Poor body condition refers to extremely thin or extremely fat animals. I find the body condition scoring system of 1 to 10 useful (1=emaciated, 10=fat). I like to see breeding females have a body condition score of 5 or 6.

MANAGEMENT OVER-INTERVENTION

Although free range breeding is the most efficient and reliable breeding method, this management style does not allow for specific identification of the sire (if more than one male runs with the herd) and, most importantly, does not allow for close estimation of the expected parturition (criation) date. Therefore, most breeders choose to use "hand breeding". Hand breeding refers to housing males in individual pens and bringing receptive females to the male for breeding. In most cases, copulation is not specifically observed, rather breeding behavior is evaluated to determine if copulation occurs. Over-eager personnel may interfere with the normal breeding behavior of males and females (particularly juveniles), resulting in incomplete or shortened copulation. If this is repeated, libido may be permanently altered.

ENVIRONMENTAL CONDITIONS

Most llamas are adapted to environmental conditions found at high altitudes (in the Alto Plano of the Andes Mountains) where extreme hot temperatures are rare. Therefore, heat stress has become a cause of great concern for owners of llamas in North America. Heat stress will decrease the likelihood of successful conception in females and may cause temporary sterility in males. Because llamas are not seasonal breeders, many owner-breeders have begun to artificially impose a late fall or spring breeding schedule. I feel that this is a desirable goal. The gestational length of llamas is 10 to 14 months (average ~11 months); therefore, crias will be born during mild temperatures. Management during hot months should include shearing all animals prior to the onset of hot weather, adequate shade, high ventilation (including the use of fans), access to cool water (child pools are useful for wading), and use of wet sand pits.

SEXUAL MATURITY CONSIDERATIONS

Llamas are increasingly pushed to breed early in life. Optimally, females should be 2 to 3 years old before their first breeding. However, breeders often enter females into the breeding pool at 14 to 18 months old. This practice is usually successful, but sexual immaturity should be evaluated in young females failing to conceive. I usually base a diagnosis of sexual immaturity on a finding of ovarian inactivity. Ovarian inactivity may be assessed by serial rectal palpation (every 1 to 2 weeks over 30 days), transrectal ultrasound examination, laparoscopic examination of the ovaries, or measurement of blood hormone levels at regular intervals. My recommendation has been to wait at least 6 months prior to trying to re-breed.

BREEDING BEHAVIOR AND RECEPTIVITY TO THE MALE

Llamas have follicular waves approximately every 11 days. When follicles reach maturity, the female is receptive to males and will "submit" to being bred. If breeding is not done, the follicles will regress in favor of another "wave". If breeding is successful, ovulation will occur and progesterone will be maintained. While progesterone is high (>2 ng/ml), the female will "spit-off" males. Owners often use these behaviors as evidence of pregnancy or failure to conceive. I have seen many cases of llamas and alpacas that were presumed pregnant because the female was not receptive to the male. When these animals are ultimately found not to be pregnant, it is assumed that they suffered early embryonic death or abortion. I have examined several females that were behaviorally pregnant for >15 months and were found to be open. Also, I have pregnancy tested several females that were re-bred because of receptivity to the male despite being in mid-gestation. Females that are chronically receptive or not receptive without an appropriate pregnancy status should be examined for ovarian and hormonal abnormalities.

DISEASES OF THE VAGINA, CERVIX, AND UTERUS

The first step in a breeding soundness examination is to determine anatomic normalcy. Persistent hymen, double cervix, inpatient cervix, segmental aplasia of the uterus, and uterus unicornis are occasionally encountered. These animals are immediately removed from the breeding program and neutered.
Vaginoscopic examination is performed with the animal restrained in a camelid chute or against a solid barrier. A small vaginal speculum is inserted and the vagina inspected. The cervix is readily identified at the cranioventral vaginal vault. Then, rectal palpation is performed, if possible. The cervix, uterus, and ovaries are palpable. Alternatively, transrectal ultrasonography is performed. Fluid accumulation in the uterus may be interpreted as pregnancy, endometritis, metritis, or mucometra. Mucometra implies that an anatomic defect is present and hysterectomy may be the treatment of choice. If pregnancy has been ruled-out for accumulations of small volumes of fluid, then uterine culture and biopsy are indicated. I use 3 mg of ECP to provide for relaxation of the cervix (requires 24 to 36 hours). Then, I perform transcervical uterine biopsy. The biopsy is cultured and submitted for histopathologic examination.

In my experience, endometritis is relatively common in llamas. When I find endometritis (discharge from the cervix or upon uterine biopsy), I place an indwelling uterine catheter and perform twice daily uterine lavage. After the catheter has been removed, I recommend 10 to 14 days sexual rest, and then re-enter the animal into the breeding pool. One common question is "When do we re-bred after criation?". Some studies have shown that the optimal time to re-bred is 14 to 21 days after parturition. Llamas bred <14 days and >21 days had lower conception rates.

DISEASES OF THE OVARY AND OVIDUCT

In my experience, diseases affecting the ovaries and oviducts are uncommon. This may mean that I am not diagnosing these problems, or that we have not exerted so much pressure for production that they have become a problem. The most common problems I have seen are ovarian inactivity and ovarian hypoplasia. Rarely, I have diagnosed obstruction of the oviduct and hydrosalpinx has been reported to occur, but we may miss some of these cases because the diagnostic tests are invasive. My approach to evaluation of the reproductive soundness of the ovary is to examine the behavioral breeding history, perform rectal palpation if possible, perform transrectal ultrasonography, and perform hormonal assays (progesterone, estrogens). If the status of the ovaries is in question, I recommend that laparoscopic examination of the ovaries be performed. The patency of the oviduct may be assessed by normograde flushing of the oviduct via laparotomy or a BSP test may be performed. Unfortunately, interpretation of the BSP test is still uncertain. If oviductal flushing is performed, this procedure must be done with extreme caution because the fimbria and oviducts are easily traumatized.