Abstract

Three species of lemur—ring-tailed lemurs (Lemur catta), black-and-white ruffed lemurs (Varecia variegata variegata), and blue-eyed black lemurs (Eulemur macaco flavifrons)—have been managed in a free-ranging setting on St. Catherine’s Island over the last 15 years. Review of lemur health records and the preventive medical program resulted identification of the morbidity and mortality causes reported in this study.

Introduction

St. Catherines Island (SCI) is a barrier island off the coast of Georgia. The island has many different habitats including freshwater and saltwater marsh, deciduous and evergreen forest, palmetto scrub, and open savannah. The island is separated from the mainland by 6 km of tidal marsh and river. There are approximately 14 miles of beach on the eastern side of the island.

In 1974, the Wildlife Survival Center was established on SCI with the mission to promote captive reproduction of endangered animals outside of the traditional zoological setting. This was a partnership between the SCI Foundation and the Wildlife Conservation Society. Species of prosimians that have been managed on SCI over the last 15 years include ring-tailed lemurs (Lemur catta), black and white ruffed lemurs (Varecia variegata variegata), blue-eyed black lemurs (Eulemur macaco flavifrons), black lemurs (Eulemur macaco macaco), and crowned lemurs (Eulemur coronatus). The large habitats and isolation of the island have allowed for the development of various free-ranging prosimian projects. Ring-tailed lemurs, black-and-white ruffed lemurs, and blue-eyed black lemurs have been managed successfully in a free-ranging setting. Six ring-tailed lemurs were first introduced onto SCI in 1985. The population has grown to up to 80 ring-tailed lemurs, which have established up to four distinct free-ranging troops. The free-ranging ring-tailed lemur program has provided researchers an excellent opportunity to conduct behavioral and conservation-oriented research. Additionally, the lemurs have been instrumental in several of our local and international training and education programs. St. Catherines Island was one of the two sites used as a “boot camp” for training black-and-white ruffed lemurs to forage and climb trees prior to being sent over to Madagascar as part of the Betampona Restocking Project.

Preventive Medicine Program

The preventive medicine program for lemurs on SCI includes an annual physical examination and diagnostic workup under isoflurane anesthesia, including a complete blood count, serum chemistry profile, serum banking, periodic serology and disease screening, fecal examination for parasites and culture for enteric bacterial pathogens, whole-body radiographs, tuberculin testing, external parasite collection and identification, and paternity testing. Dental prophylaxis, fipronil application, changing radio collars, and vaccination for rabies and tetanus are also performed. Additionally, various methods of identification (transponder, ear tag, colored cat and radio collars) are placed at this time.

Morbidity and Mortality

Trauma

Various forms of trauma were the most common problem observed in the free-ranging ring-tailed lemurs. Documented injuries have included lacerations, bite wounds, leg and tail fractures, and occasional head and vertebral fractures. Vertebral and skull fractures have required euthanasia. The following are a list of orthopedic injuries that have been documented predominantly in the ring-tailed lemurs and less commonly in the other two species: pelvic fractures (two) and coxofemoral luxations (two), cruciate and other stifle ligament injuries (three), bilateral elbow luxation with olecranon fracture (one), ulnar fractures (two), humeral fractures (three) (one of these involved the growth plate of the proximal humerus), clavicle fracture (one), tibial fracture (one), radial/ulnar fracture (one), femur fractures (two), and a metacarpal fracture (one). A fractured patella occurred in a blue-eyed black lemur and a fractured tuber calcaneus occurred in a black-and-white ruffed lemur. The majority of these fractures were successfully repaired utilizing a variety orthopedic techniques including using various types of pinning techniques, cerclage and Kirschner wires, bone plating, interlocking nails, and external skeletal fixation. Cage rest was used to treat less severe fractures.

External and Internal Parasites

Cuterebra (warble fly) infestation was a common problem in the free-ranging ring-tailed and black-and-white ruffed lemurs. The species of Cuterebra affecting the lemurs (Cuterebra emasculator fitch) is the same species that infests the native gray squirrel (Sciurus carolinensis). Cuterebra infestations are particularly problematic in juveniles and lower-ranking troop members and may lead to localized abscessation and generalized debilitation. We have removed as many as 13 Cuterebra from an individual lemur. Cuterebra infestations are seasonal, occurring from August to October, with variation in the incidence of Cuterebra infestations from year to year. For example, in 1999 we removed over 150 Cuterebra from ring-tailed lemurs. The next year we decided to set up a controlled study to evaluate potential preventive treatment protocols, and no Cuterebra were observed, even in the control groups. Over the past several years, we have systematically performed annual examinations in June and July and placed fipronil (Frontline®, Merial Limited, Duluth, GA, USA) on a shaved area between the scapulae. In 2003, we were performed annual examinations and applied fipronil in June and July for three troops, and no warble flies were noted for the remainder of the season. One troop received their annual examination in mid-August, and 50% of the lemurs had early stages of warble fly infestation. The adult lemurs receive a cat dose (0.5 ml) of the drug and the juveniles (approximately 4 months of age) receive 0.1 ml of the drug topically. One dose of fipronil has significantly decreased the incidence of Cuterebra infestations.

Low-grade Strongyloides sp. infestations are common; however, clinical disease from this parasite is rare. A 3-day course of fenbendazole (Panacur, 100 mg/ml, Hoechst Roussel Vet, Warren, NJ, USA) at 50 mg/kg of body weight effectively treats this organism.

Infectious Diseases

Previous studies on SCI have isolated a variety of infectious diseases from ticks recovered from various wildlife species. Preliminary serologic studies of lemurs from SCI documented evidence of exposure to Ehrlichia spp. and Rocky Mountain spotted fever (Rickettsia rickettsii) in several lemurs. Attempts to isolate Borrelia burgdorferi (Lyme disease) from 45 skin biopsies taken from ring-tailed lemurs were unsuccessful. Recently, a study was conducted to evaluate evidence of exposure of lemurs residing on SCI to tickborne ehrlichiae.² Fifty-six lemurs of three species were serologically tested for exposure to Ehrlichia chaffeensis and Anaplasma phagocytophilum. Additionally, polymerase chain reaction (PCR) assays for E. chaffeensis, A. phagocytophilum, Ehrlichia ewingii, and Ehrlichia canis were conducted on blood samples from all lemurs. Twenty (38.5%) and 16 (30.8%) had antibodies reactive for E. chaffeensis and A. phagocytophilum, respectively. Two ring-tailed lemurs were PCR- and culture-positive for E. chaffeensis. The study showed that these lemurs have been exposed to or infected with tickborne ehrlichiae, or both, but showed no clinical disease.

Trypanosoma cruzi is endemic in the raccoon population on SCI and other locations in the southeastern United States. Free-ranging lion-tailed macaques and lemurs released on SCI were tested for infection with T. cruzi by a previously described blood culture method.¹ Seven of 11 lion-tailed macaques and one of 19 ring-tailed lemurs had positive cultures. The organism is most likely transmitted by the triatomine bug, Triatoma sanguisuga.

Gastrointestinal disease was a relatively common problem in all of the lemur species residing on SCI. Severe acute fibrinonecrotic enterocolitis was observed in four ring-tailed lemurs, two blue-eyed black, and one crowned lemur. The ileum and cecum were most commonly involved; however, all parts of the small and proximal large intestine were affected by this pathology. The onset of clinical signs was acute and included anorexia, lethargy, abdominal pain, and vomiting. Physical examination often revealed a mid-abdominal mass. Severely gas-distended bowel loops were the most common radiographic signs. Consistent clinical pathology abnormalities included leukocytosis, monocytosis, elevated packed cell volume, hypoproteinemia, hypoalbuminemia, hyperkalemia, and hyponatremia. The problem required immediate medical intervention, which included crystalline and colloidal fluid therapy, broad-spectrum antibiotics, and analgesics. Exploratory surgery was performed in the four ring-tailed lemurs and revealed severe adhesion formation causing the involved gastrointestinal tract to be tightly adhered to itself (mass evident on palpation), peritonitis, abdominal effusion, and varying degrees of devitalized thickened bowel. There was often a foul odor to the abdomen, and obvious perforation was noted in two cases. Two cases required euthanasia during surgery due to the severity and extent of devitalized bowel. Two out of six cases were successfully managed with resection and anastomosis of the affected bowel. Although the etiology is unknown, enrofloxacin (Baytril®, Bayer Health Care LLC, Shawnee Mission, KS, USA) use prior to the onset of clinical signs was noted in three of the six cases. Enrofloxacin had been used 8 months, 5 months, and just prior to onset of clinical signs in the three cases. Histopathology documented severe acute ulcerative, necrotizing gastroenteritis, typhlitis, and colitis. Gram-negative rods predominated with occasional gram-positive rods observed. A mixture of gram-negative bacteria was typically cultured. Feces and tissue submitted for Salmonella, Shigella, Campylobacter, and Yersinia culture were negative in all cases. Clostridium perfringens was cultured from affected gastrointestinal tract tissue in one case. Toxin assays for Clostridium difficile and Clostridium perfringens were negative.

In 1997, several ring-tailed lemurs and black-and-white ruffed lemurs succumbed to gastrointestinal disease and subsequent septicemia. Although a common organism was not isolated in every case, Salmonella sp. was isolated on two occasions and histopathology substantiated this finding. Subsequently, Salmonella and Campylobacter sp. have occasionally isolated from healthy individuals; however, further mortality has not occurred.

Miscellaneous

Miscellaneous medical problems documented in the ring-tailed lemurs include canine tooth fractures with subsequent tooth loss or abscessation, frostbite to tail tips, scent gland abscesses and impactions, suspected snake bite (one), corneal ulcers, medial strabismus, tricuspid insufficiency (endocardiosis) (one), epilepsy (one), intestinal herniation with exposed mucosa and feces coming from hernia site in an infant (surgical repair was successful), femoral vein thrombosis (one), inguinal testicle (one), osteoarthritis (has been an occasional problem in geriatric lemurs, glycosaminoglycans have been administered long term in one animal), fleas (one), ticks (occasionally observed but usually very low in numbers), eosinophilic dermatitis (one), Capillaria hepatica (incidental finding in one animal), cholecystitis (one), bacterial pneumonia (four), pleuritis (two), pulmonary septic thrombosis (one), cardiac septic thrombosis (one), mesothelioma of diaphragm (one), and a subcutaneous lipoma (one).

Causes of morbidity in black-and-white ruffed lemurs documented in this study were asymptomatic salmonella (one), ovarian/uterine bacterial abscess/infection (resolved with surgery), Capillaria (one), heavy tick infestation (one), fractured tuber calcanei (one), low-grade strongyloides (common), dystocia (resolved with C-section), bite wounds, and Cuterebra infestation. Causes of mortality in this lemur species included failure to nurse (five), congenital heart defect (one), cardiomyopathy (three), pneumonia and septicemia caused by Klebsiella (three), bacterial colitis leading to complete obstruction (one), necrotizing gastroenteritis with septicemia (one), renal failure (two), and colonic obstruction with subsequent rupture and peritonitis (one).

Causes of morbidity in blue-eyed black lemurs included abortion/stillbirths (possibly secondary to previous use of Depo-Provera and MGA implants for birth control), vulvar and scrotal ulcers (herpesvirus serology negative, biopsies reveal a pustular to eosinophilic dermatitis), chronic cholangiohepatitis (diagnosed on liver biopsy, elevated alkaline phosphatase, geriatric lemur), patellar fracture (one), and a rectal stricture requiring resection anastomosis with subsequent rectal/vaginal fistula formation. Causes of mortality in this species included acute focally extensive necrotizing enteritis with secondary septicemia (suspected Salmonella) (one), acute focally extensive ulcerative colitis (Clostridium perfringens cultured) (one), abortions/stillbirths (suspect secondary to changes induced by birth control), bite wound to abdomen with penetration into the ileum causing an intestinal abscess, adhesions, peritonitis (one), and hypertrophic osteopathy and chronic renal failure (one).

Acknowledgments

We would like to acknowledge the lemur husbandry and medical staff at the Wildlife Survival Center and the technical staff at the South Carolina Veterinary Referral Center for their assistance over the past several years on various lemur medical and surgical cases.

Literature Cited

1.  Pung, O. J., J. Spratt, C.G. Clark, T. M. Norton, and J. Carter. 1998. Trypanasoma cruzi infection of free-ranging lion-tailed macaques (Macaca silenus) and ring-tailed lemurs (Lemur catta) on St. Catherines Island, Georgia, USA. J. Zoo Wildl. Med. 29(1): 25–30.

2.  Yabsley, M. J., T. M. Norton, M. R. Powell, and W. R. Davidson. 2004. Molecular and serological evidence of tick-borne Ehrlichieae in three species of lemurs from St. Catherines Island, Georgia, USA. J. Zoo Wildl. Med. 35(4): 503–509.