Prosimians

Question 1

Which viruses can be transmitted from humans to prosimians and cause neurologic disease?

Answer 1

Herpesvirus: Human herpes simplex virus type 1: encephalitis, meningoencephalitis - seizures, ataxia, coma Human herpesvirus-4: Epstein-Barr - unilateral facial paralysis (F8, Path)

Question 2

Name a parasite that can be transmited to lemurs from the ingestion of cockroaches

Answer 2

Physaloptera (stomach roundworms) Gongylonema (esophageal roundworm) also correct though beetles are often cited as the main intermediate host

Question 3

Three black lemurs in the same family group develop swelling of the tarsi and stifles. Radiographs show periosteal new bone along the metaphysis of multiple joints and bloowork reveals an azotemia. What is your primary differential?

Answer 3

Periarticular hyperostosis - genetic proliferative bone disease (F8, Path)

Question 4

In which organ or body system is the most common tumor found in lemurs?

Answer 4

Liver (Path)

Question 5

List 3 potential adverse effects of ketamine when used alone for chemical immobilization of prosimians

Answer 5

Vomiting on recovery, inconsistent sedation, seizures (F8, West)

Question 6

What is the preferred diagnostic sample for encephalomyocarditis virus in prosimians?

Answer 6

Heart (Path)

Question 7

List the two infraorders of order Strepsirrhini

Answer 7

Lemuriformes (lemurs), Lorisidae (Loris, potto, galagos)

Question 8

What dental adaptation is unique to prosimians that are nor present in other primates and which prosimian also lacks this adaptation?

Answer 8

Toothcomb: lower incisors and canines project forward almost horizontally. Not present in aye-aye or tarsiers (F8, Path)

Question 9

Which prosimian has hypsodont incisors

Answer 9

Aye-aye, also lack premolars (F8)

Question 10

Which family of lemurs has a spiral-shaped colon

Answer 10

Indriidae: Indri, woolly lemurs, sifaka (F8, Path)

Question 11

Which prosimian requires dietary vitamin C?

Answer 11

Tarsier (Path)

Question 12

In which group of primates do most species have an estrous cycle

Answer 12

Prosimians (Path)

Question 13

Describe the plica mediana and which non-human primates have it

Answer 13

Cartilagenous sublingua with serrated keratin points used for grooming Present in prosimians except tarsiers, hook shaped in aye-aye (Path)

Question 14

What type of uterus and placentation does a ring-tailed lemur have?

Answer 14

Bicornuate; diffuse epitheliochorial

Question 15

Name the toxin in avocados, 3 parts of the plant that contain the toxin, and 2 clinical signs in an aye-aye

Answer 15

Persin; bark, leaves, skin, pit; pericardial effusion, myocardial pallor and contraction band necrosis (Path)

Question 16

Describe some of the unique anatomic and physiologic characteristics of prosimians.

What is their metabolic rate like?

What is a normal systemic temperature for a lemur and for a loris?

What species undergoes torpor?

What are the two orders and suborders of prosimians?

Answer 16

Physiology (Fowler 8)

• Prosimians have a low basal metabolic rate
• Behaviors such as basking and huddling are related to energy conservation and thermal regulation
• Lemurs are 97-99F and lorises are 95-97F normally
• Dwarf lemurs undergo torpor
• No active mechanism for cooling, so capture and handling during warm weather should be avoided

TAXONOMY (TERIO)

1. Order Strepsirhini
   
   1. Lemuriformes, Madagascar
      
      1. Cheirogaleidae: fork-marked, dwarf, mouse lemurs
      2. Lemuridate: bamboo, ring-tailed, ruffed, true lemurs
      3. Lepilemuridae: sportive lemurs
      4. Indriidae: indris, sifakas, woolly lemurs
      5. Daubentoniidae: aye-aye
   2. Lorisiformes
      
      1. Lorisinae: slow and slender lorises (India, SE Asia, west Indonesia, Africa)
      2. Galagos (bushbabies), Africa
      3. pottos, Africa
2. Order Haplorhini - Tarsiiformes, Southeast Asia
3. 94% of known species listed by IUCN as critically endangered, endangered or vulnerable

Question 17

Describe some of the uniqe prosoimian anatomy.

What is unique about their eyes?

Discuss the scent glands of lemurs and lorises. Where are they located? What is unique about slow loris scent glands?

What is unique about their digits?

What is unique about their himdlimbs?

Answer 17

ANATOMY (TERIO)

1. Eyes
   
   1. Nocturnal species have enormous eyes - rod rich retinas
   2. All but tarsiers have retinal fovea and choroidal tapetum lucidum deep to retinal photoreceptors
      
      1. Riboflavin crystals - golden yellow shine
   3. Blue-eyed-black lemurs are only primate other than humans with blue eyes
2. Accessory intranasal vomeronasal system (Jacobson’s organ) - detect chemical stimuli (pheromones)
3. Scent glands
   
   1. Malagasy lemurs - wrists, inside elbows, genital region, forehead, throat, ventral neck region
   2. Slow loris - brachial glands on medial aspect of forearms in elbow region
      
      1. Secretions mixed with saliva - noxious, malodorous, painful bite wounds, associated with human anaphylaxis
4. Opposable first digits on their fore and hind limbs
   
   1. toilet-claws - blunt end and steeper angle relative to the digit; generally on second pedal digit (Tarsiers: 2nd and 3rd digits)
   2. Long third digit - several species including tarsiers and aye-ayes
   3. Tarsiers: long tarsal bones, fused tibiofibulae
   4. Pottos: vestigial first digit

Question 18

Describe the unique anatomy of prosimians.

What is a toothcomb?

What is unique about aye-aye dentition?

What is the plica mediana?

Describe their GI anatomy.

Male reproductive anaotomy - do they have a baculum? What is unique about the glans of mouse lemurs adn bush babies?

Female reproductive anatomy - what type of uterus and placentation? How is that different from other primates?

What is unique about tarsier ear canals and nutrition?

Answer 18

1. Dental/oral
   
   1. Formulas vary (p.324 list some)
   2. All except tarsiers and aye-ayes: lower teeth are modified into a toothcomb - 6 slender close teeth (mandibular incisors and canines) that tilt slightly forward; typically used for grooming but some use of forage
   3. First mandibular premolars often long and caniniform
   4. Aye-ayes - lack premolars and hypselodont incisors
2. Plica mediana (lytta) - rigid, medial, cartilaginous structure that attaches/supports the ventral sublingua (used to clean hair from the toothcomb)
   
   1. Tip of sublingua splits into serrated keratin lined points - lemurs, lorises, bushbabies (NOT tarsiers)
   2. Aye-aye - plica mediana is hook shaped
3. Gastrointestinal
   
   1. Monogastric
   2. Variation in size, shape of tract, ceca, colon - Cecum larger in folivorous species
   3. Proximal colon - spiral with indris
   4. Appendix absent or insignificant
4. Male Reproductive
   
   1. Boney relatively large penile baculum (exception tarsiers)
   2. Spur-like projections on glans penis - mouse lemurs, bush babies
   3. Accessory sex glands in some neonatal males may be relatively large
5. Female Reproductive
   
   1. Have vulvar labia majora
   2. Large exaggerated pendulous clitoris (not to be confused with penis), some also have small baculum-like intraclitoral boney structure: ring-tailed, black and white ruffed lemurs
   3. Bicornuate uterus
   4. Placentation - adeciduate, diffuse, epitheliochorial
      
      1. Most other primates have simplex uterus and hemochorial placentation
   5. Tarsiers are always exception: long uterus and deciduate, discoidal hemochorial placentation
6. Subscapular glomerulopoesis - premature ring-tailed lemurs
   
   1. Adrenal cortex - fetal zone involudes within a few days of birth in lemurs - associated with immaturity
   2. Exception: black and white lemur
7. More weird things about tarsiers
   
   1. Ossified ear canals
   2. L-gulono-1,4-lactone oxidase (GULU) deficient (acquire vitamin C from diet)

Question 19

Describe the housing, feeding requirements, and general preventative medicine of prosimians.

Answer 19

Housing

• Generally from tropical regions so temperature and humidity should be maintained accordingly
• Photoperiod for nocturnal species
• Adequate vertical structures for leaping and locomotion

Feeding

• Range from insectivores to folivores
• Prosimians are able to synthesize vitamin C endogenously
• Many species do well with commercially prepared primate biscuit base supplemented with other food items

Preventative Medicine

• Vaccinate with rabies, +/- tetanus
• Preship should include testing for salmonella, shigella, campylobacter, yersinia, and TB

Question 20

Describe the restraint and anesthesia of prosimians.

What manual restraint techniques can be employed?

What are the sites for venous access?

Describe intubation of prosimians.

What drug combinations are commonly used?

What species are sensitive to inhalant anesthetics?

What are some common complications with anesthesia?

Answer 20

Restraint

• Control head, arm guards prevent scratches, restrain hind limbs above the knees to avoid injury
• Squeeze cage for larger lemur IM injection

Venipuncture

• Cephalic, external saphenous, jugular, femoral
  
  • External saphenous runs along the caudal aspect of the tibia

Intubation

• Lemurs: epiglottis is long and points dorsally, obstructing visualization of the glottis
• Aye-aye have small mouth opening due to heavy jaw musculature and limited visualization due to long incisors
• Ring-tailed lemurs have narrow opening of the vocal fold
• Guide-catheters are useful in these species
• Short trachea
  
  • <1 kg: urinary catheter
  • 0.75-1.5 kg: 2.5 mm uncuffed
  • 1.5-5 kg: 3-4.5 mm cuffed

Question 21

Describe hemosiderosis in prosimians.

What are the typical clinical signs?

What stain is used to confirm cases?

What are some potential sequelae?

Answer 21

1. Hemosiderosis (iron overload) - intracellular accumulation of iron in the absence of other tissue damage
   
   1. Common in captive setting, severity varies (somewhat species dependent)
   2. Diet possible etiology - uncommon in animals less than 6 months old
   3. First accumulates in duodenum/small intestine followed by storage in liver/spleen/marrow
   4. HE: intracytoplasmic brown granular to globular material that stains blue (Prussian blue)
   5. Severe cases - gross brown discoloration of intestinal mucosa
   6. Hemochromatosis - fibrosis, hepatocyte necrosis, hepatocyte fatty degeneration, bile duct hyperplasia, nodular regeneration (much less common)
   7. Humans - risk factor for neoplasia; similar associations suggested, but not confirmed
   8. “Recent studies of multiple lemur species have not found a relationship between clinical disease and excessive hepatic hemosiderosis or high liver iron concentrations (up to 12,800 ppm dry weight)”

Question 22

What are some common causes of dental disease in prosimians? What types of dental issues are seen?

What species of prosimians commonly have choleliths? What is their composition? What are typical clinical signs and lesions associated with theri cholelithiasis?

Answer 22

1. Dental disease - severe dental calc, gingivitis, periodontitis, tooth wear/fracture/loss, abscesses
   
   1. Common in captive lorises (pygmy and slow) and Senegal bushbabies
   2. Wide band of bright pink to red discoloration and swelling of gingival margin
   3. Facial swelling in more severe cases; extension to ocular/CNS structures - encephalitis
   4. Concurrent factors: diet, trauma, genetics, infectious (Sebaldella termitidis, Trueperella pyogenes)
   5. Slow loris diets with high fruit proportion compared to plant exudates (gums)
2. Choleliths
   
   1. Low frequency reports in several species (greater galago, black lemur, slender loris)
   2. Group of slender lorises - 11-13 years old; CS: absent, inappetence, emaciation, abdominal pain, lethargy, vomiting
   3. One or numerous stones, up to 1 cm diameter in gallbladder; composed of cholesterol
   4. Tissue changes: none to thickening of the gallbladder wall with marked cystic dilation of the gland, mild, multifocal, lymphoplasmacytic inflammation, and occasional intrahepatic, periductular fibrosis

Question 23

Describe the following toxicities in prosimians.

What is the cause of bald lemur syndrome? What are the typical lesions?

What is teh mechanism of toxicity of solanine (nightshade)? What are the typical signs?

What is the toxic principle of avocado? Where on the plant is it found? What are the typical signs?

Answer 23

1. Seasonal alopecia (bald lemur syndrome) - wild ring-tailed lemurs in dry season
   
   1. Consumption of mimosine (plant amino acid) of Leucaena leucocephala tree (plant native to Americas - Mexico, CA, northern SA that was introduced in 1990s for domestic ruminant food source)
   2. Highest concentration in seeds, mature leaves/stems, 5-10% dry weight is toxic
   3. Alopecia, poor bcs/weight, infertility
   4. Severe cases - death, infant mortality
   5. Over 50% of diets for some groups May-September
   6. Skin: orthokeratotic hyperkeratosis, follicular arrest with the majority of hairs in the telogen (resting) phase of the hair growth cycle
   7. Mechanism not understood completely - maybe inhibition of DNA, RNA, protein synthesis
2. Plants with solanine (nightshade family)
   
   1. toxic glycoalkaloid that inhibits cholinesterase enzymes including acetylcholinesterase
   2. Termination of synaptic transmission at neuromuscular junctions
   3. GI and nervous system primarily - vomiting, diarrhea, cardiac dysfunction, respiratory depression, muscle tremors, paralysis, death
   4. Severe hemorrhagic enteritis and typhlitis
3. Avocado
   
   1. Infrequent cause of death in captive aye-ayes
   2. Persin (toxin) - leaves, bark, pits, skin, and possible fruit
   3. Pericardial effusion, myocardial pallor, acute myocardial contraction band necrosis
   4. Massive catecholamine release and stressors may play role
   5. Can detect toxin in stomach contents

Question 24

Describe the degenerative diseases of prosimians.

Where does amyloid B protein deposit in mouse lemurs? What disease is this similar to?

What type of joint diseases are common?

Answer 24

AGE-RELATED/DEGENERATIVE

1. Cataracts: Causes - metabolic, traumatic, heritable, degenerative, secondary to infectious/inflammatory disease
2. Amyloid-B (AB) peptide (human Alzheimer’s) - plaques in brain of mouse lemurs
3. Joint diseases
   
   1. Less common in prosimian than other old world primates
   2. Osteoarthritis more common in captive than free-ranging
   3. Erosions in articular cartilage of metacarpal and metatarsal joints, knee, elbow, but typically limited to a single joint

Question 25

What are the two common renal diseases of prosimians?

What animals do they typically affect?

What are the typical lesions?

What are two unique presentations of GI disease in prosimians?

Which species are affected?

What clinical signs are usually associated?

Answer 25

1. Chronic renal disease
   
   1. Common in middle aged to older animals; severity varies
   2. interstitial fibrosis, cystic tubules, and nonsuppurative, interstitial or tubulointerstitial inflammation, glomerulonephritis, enlarged or shrunken, fibrotic (sclerotic) glomeruli, adhesions between bowman’s capsule layers
2. Polycystic nephropathy - adult slender lorises
   
   1. Kidneys have undulating capsular surfaces that correspond to underlying cortical cysts
   2. lymphocytic and histiocytic interstitial nephritis, proliferative or membranous glomerular changes
3. Necrotizing enterocolitis and typhlitis
   
   1. ring-tailed, red-ruffed, and mongoose lemurs
   2. abdominal pain, lethargy, anorexia, potential hx of diarrhea
   3. Mucosal to transmucosal necrosis of SI, cecum, LI
   4. Unsuccessful attempts to ID a specific infectious cause; Ischemia has been proposed as a factor
4. Gastric pneumatosis (emphysematous gastritis, pneumatosis cystoides internalis)
   
   1. black and white ruffed lemurs, red-ruffed lemurs, and a slow loris
   2. focal or regionally extensive expansion of the gastric submucosa by large, multifocal to coalescing, cyst-like spaces
   3. Gastric wall gas expansion may be radiographically apparent
   4. CS: absent, lethargy, weakness, inappetence, vomiting, weight loss, sudden death
   5. Cause not identified

Question 26

What prosimian species is commonly affected by pyogranulomatous osteomyelitis? How do those animals present and what lesions are appreciated? How can they be managed?

What prosimian species is commonly affected by periarticular hyperostosis? What is it associated with? What type of lesions may occur?

Answer 26

1. Multifocal pyogranulomatous osteomyelitis - captive red-ruffed lemurs
   
   1. Lameness, skeletal muscle atrophy
   2. Rad: multifocal lytic lesions with cortical thickening and sclerosis in the diaphysis of the long bones of the fore and hind legs
   3. Early - woven trabecular bone, neutrophilic inflammation, small foci of necrotic trabecular bone to more severe - necrotic bone, decreased trabecular production, chronic inflammation
   4. Clinical signs may resolve with NSAIDS
   5. Unknown cause
2. Periarticular hyperostosis (PH) - black lemurs associated with chronic renal disease
   
   1. Proliferative, periosteal, new bone formation primarily associated with metaphysis
   2. Advanced cases - periarticular osteophytes, cartilage degeneration

Question 27

What are some of the most common neoplastic diseases affecting prosimians?

Answer 27

NEOPLASTIC

1. The most common tumors occur in the liver
   
   1. Hepatocellular tumors more common than biliary
   2. Carcinomas more common than adenomas
   3. Metastases relatively common, often involve lung; reports in stomach, heart, kidney, mediastinum
   4. Adenomas - composed of a proliferation of well-differentiated hepatocytes
   5. Inflammation is not common
2. Lymphoma relatively common
3. Leukemia relatively common

Question 28

What are some of the natural herpesviruses of prosimians?

What happens with human herpes simplex is transmitted to prosimians?

What are the typical clinical signs?

What are the classic lesions and inclusion bodies?

Answer 28

1. Herpesviruses:
   
   1. tarsier (TsyrHVL), aye-aye (DmadHVL)
   2. Interspecies transmission of human herpes simplex virus type 1 (HSV-1) can cause significant disease in prosimians (similar to gorillas)
   3. Herpesvirus encephalitis and meningoencephalitis
      
      1. black and white ruffed, ring-tails, and pottos
      2. CS: lethargy, weight loss, decreased coordination, lameness, paralysis, seizures, ptyalism, death
      3. Gross lesions absent to multifocal hemorrhage or malacia
      4. Hypereosinophilic necrotic neurons, malacia, demyelination, intranuclear eosinophilic viral inclusions (Type A – alphaherpesvirus)

Question 29

What virus is associated with hepatitis in lemurs? What are the typical clinical signs and lesions?

What parovovirus affects prosimians? What lesions are observed with infection?

Answer 29

1. Acute viral hepatitis
   
   1. Associated with hepadenovirus-like particles in two black and white ruffed lemurs
      
      1. lethargy, weakness, sudden collapse, anemia, icterus
      2. hypoteinemia, bilirubinemia
      3. Livers enlarged, mottled light tan, soft
   2. Partially double stranded, partially single-stranded circular DNA
   3. asymptomatic, hepatitis, hepatic necrosis, degeneration, benign hepatomas, hepatocellular carcinoma
   4. Viral inclusions typically not seen
2. Parvovirus (nonenveloped)
   
   1. Slow loris parvovirus 1 (S1.L-PV-1) - infected animal had persistent viremia
      
      1. developed histiocytic sarcoma
      2. Splenomegaly, mottled liver, lymphadenomegaly (pancreatic, mediastinal)
      3. Mitotic figures common
      4. PCR positive samples from liver, spleen, kidney, lung, intestine, serum, and whole blood

Question 30

What is the natural reservoirs of encephalomyocarditis virus?

What are the typical clinical signs in infected prosimians?

What are the associated lesions on gross and histologic examination?

Answer 30

1. Encephalomyocarditis viruses (EMCV)
   
   1. Nonenveloped, single-stranded, Picornaviridae
   2. Rodents (especially mice and rats) natural hosts and reservoirs
   3. Asymptomatic; sudden death or short period of weakness and lethargy prior to death
   4. encephalitis, paralysis, myocarditis, diabetes, orchitis, reproductive disorders
   5. Infection: shed in urine or feces; consumption of contaminated food/water/carcass
   6. Captive outbreaks in Italy, Australia, and US in multiple lemur species
   7. Heart usually most affected and preferred for diagnostic sample (but can be isolated from other tissues and feces)
   8. cardiomegaly, myocardial pallor, epicardial petechial or ecchymotic hemorrhage, pulmonary congestion, hemorrhage, edema, hydropericardium (serous/serofibrinous/serosanguineous), thoracic effusion, ascites
   9. Myocardial necrosis, cardiomyocyte hydropic degeneration, multifocal lymphoplasmacytic epi- and/or myocarditis +/- neutrophilic inflammation or necrotizing vasculitis
   10. Less common - neuronal necrosis, satellitosis, perivascular meningeal hemorrhage

Question 31

What are some of the most common bacterial enteric pathogens of prosimians?

What bacterial infections may result in septicemia?

What bacterial infection can result in necrotizing bronchopneumonia?

What tick borne pathogen affects lemurs? How is it transmitted? What clinical signs does it cause?

What two species of mycobacteria have been reported in lemurs?

How is tularemia transmitted to proximians and how does it affect them?

Answer 31

BACTERIAL

1. Several bacteria described in captive prosimians with enteric disease (Campylobacter jejuni, Yersinia, E. coli, S. typhimurium, Shigella, Klebsiella, C. difficile); many in feces of free-ranging lemurs
2. Bacterial septicemia cases - Citrobacter, S. typhimurium
3. Fibrinous and necrotizing bronchopneumonia - Klebsiella pneumonia or mixed infections in collared lemur and slow lorises
4. Ehrlichiosis
   
   1. Tick-borne; gram-negative, obligate intracellular proteobacteria
   2. E. chaffeensis:
      
      1. US south-central and mid-Atlantic
      2. Lone star tick (Amblyomma americanum) nymphs and adults transmit
      3. White-tailed deer is main reservoir
      4. Affected lemurs: anorexia, lethargy, fever, lymphomegaly; thrombocytopenia and leukopenia (lymphopenia, neutropenia), hyperbilirubinemia, azotemia, proteinuria
      5. Ehrlichia morulae identified in lymphocytes and monocytes from ln aspirates; morula-like inclusions in leukocytes, PCR
5. Mycobacteriosis (acid-fast bacilli, granulomatous inflammation)
   
   1. M. tuberculosis:
      
      1. ring-tailed, ruffed, black and mongoose lemurs
      2. Pulmonary infection most common, but other sites include intestines, thoracic cavity, liver, spleen, mesenteric ln
   2. M. xenopi:
      
      1. Captive black and white ruffed lemur
      2. Similar lesions
6. Tularemia
   
   1. Francisella tularensis - gram negative coccobacillus
   2. Rodent and rabbit carriers
   3. Systemic disease described in captive ring-tailed and black and white ruffed lemurs
   4. Marked splenomegaly, microabscess formation in liver and spleen (nodular aggregates of neutrophilic inflammation with central necrosis and intralesional bacteria), bronchopneumonia
   5. Confirm diagnosis with culture
   6. Antibiotics and rodent control helpful

Question 32

Describe the fungal infections that affect prosimians.

What fungus affects ring-tailed lemurs in teh SW US? What is the typical lesions associated with that disease?

What is the dermatophyte of prosimians? What are the typical clinical signs and lesions?

Answer 32

FUNGAL

1. Coccidioidomycosis (valley fever, San Joaquin Valley fever) - captive ring-tailed lemur
   
   1. Only in Western hemisphere; caused by C. immitis or C. Posadasii
   2. Dimorphic, saprophytic fungi - mycelia in warm arid regions of SW US, Mexico and parts of Central and South America
   3. Inhalation of spores, primary infection usually in lungs but can occur through breaks in skin; can develop into disseminated disease
   4. Granulomatous or pyogranulomatous inflammation and/or abscess formation
   5. characteristic intralesional coccidioidal spherules with or without endospores
2. Dermatophytosis - Trichophyton mentagrophytes
   
   1. Crusting dermatitis and alopecia in skin around mouth, eyes, neck, forefoot; thickened perineal skin
   2. lymphoplasmacytic perivascular dermatitis with folliculitis, furunculosis, and intralesional fungal hyphae
   3. Coquerel’s sifaka
   4. intra/interspecies or zoonotic transmission is concern

Question 33

Describe the nematode parasites that commonly affect prosimians.

How is gonglynoma transmitted? What lesions does it cause?

What are some complications with physaloptera infections?

What clinical signs may occur with Spirocerca lupi infection?

What are the lesions associated with baylisascaris procyonis infection?

Answer 33

1. Gongylonema sp - threadlike nematodes of birds and mammals transmitted by insects (beetles, cockroaches)
   
   1. Tongue or esophagus; adult worms in superficial stratified squamous epithelium of mucosa and form serpiginous tracts
   2. One publication reports association with squamous cell carcinoma in a black & white ruffed lemur (vari)
2. Physaloptera spp
   
   1. Stomach of captive prosimians
   2. Occasional cause mild or significant disease - gastritis in ruffed lemur; black lemur died due to gastric perforation and suppurative peritonitis (P. sibirica) kd
3. Spirocerca lupi - aortic aneurysm formation, rupture and death
4. Baylisascaris procyonis - encephalitis from migration of larvae
   
   1. Black and white ruffed lemurs - malacia with gitter cells in multiple brain sites; characteristic parasites only seen in one animal
   2. white -headed lemurs: granulomatous meningoencephalitis; white matter necrosis associated with larvae; intralesional larvae found in lungs, kidney, spleen, heart, jejunum

Question 34

Describe the cestodes that affect prosimians.

What causes cysticercosis? What is the normal definitive adn intermediate hosts?

What causes hydatid cysts?

Answer 34

1. Cysticercosis - fluid filled bladder containing a single attached inverted scolex (caused by larval Taenia)
   
   1. Carnivore definitive host, rodent intermediate host
   2. 2 ring-tails in Europe, a black lemur in the US, red ruffed lemur case
      
      1. First ring tail: multiple, septated fibrous cysts containing myriad cysticerci in the subcutis and peritoneal cavity
      2. Second: two large, intraabdominal cysticerci associated with severe fibrinosuppurative peritonitis
      3. Black lemur: a large, fluctuant swelling in the subcutis over the back; with similar lesions in abdomen and thorax (replaced a portion of lung lobe)
      4. Source not identified
2. Hydatid cysts produced by larval cestodes of Echinococcus - greater galago, ring-tailed lemur
   
   1. Large fluid-filled cysts with outer membrane and inner germinal epithelium from which brood capsules containing one or multiple, small inverted scolices form and remain attached or bud off and float freely within the cyst
   2. Galago - abdominal distension
   3. Lemur - 7 cm diameter cyst in caudal thorax caused displacement of herat and right lung lobe atrophy; another large cyst in liver
   4. Both animals wild caught

Question 35

Describe the protozoal parasites of prosimians.

What is a common fatal systemic infection caused by a protozoa in prosimians? What lesions does it cause?

What protozoa caused encephalitis? What are teh typical lesions and clinical signs? How is it transmitted?

Answer 35

Protozoan Parasites

1. Toxoplasma gondii
   
   1. Fatal systemic infection with mononuclear cell infiltrates and intracellular tachyzoites, parenchymal cysts
   2. Placentitis, abortion, disseminated fetal infection, neonatal death in pregnant animals
2. Amoebic encephalitis
   
   1. Life threatening disease for humans and non-human primates
   2. Death of black and white ruffed lemur - necrotizing meningoencephalitis due to Acanthamoeba T4 genotype; sudden onset of lethargy, recumbency and seizures
   3. Neutrophilic leukocytosis and lymphopenia
   4. Hemorrhage, necrosis, inflammatory lesions in frontal and parietal lobes of cerebrum with intralesional double-layered amoebic cysts and trophozoites
   5. PCR confirmed organism
   6. Water most likely source of infection
3. Cryptosporidiosis
   
   1. free ranging and captive lemurs and captive sifakas
   2. No clinical signs to mild anorexia, lethargy and abdominal bloat +/- diarrhea
4. Plasmodium - several sp. reported in wild lemurs, but clinical disease has not been described
5. Trypanosoma cruzi - asymptomatic infection in captive and free-ranging ring-tailed lemurs; other species in collection of captive lemurs were seropositive
6. Giardia
7. Entamoeba

Question 36

What ectoparasite commonly affecte Senegal bushbabies? What are the typical lesions like?

Answer 36

Ectoparasites

1. Demodex - host specific, over proliferation
   
   1. Captive Senegal bushbabies
   2. Raised nodules with thick waxy white material and papules on haired and unhaird surfaces of ear pinnae or rarely on legs
   3. Mites present on histology

Question 37

A recent sutdy evaluated the behavioral responses of lemurs to different food enrichment devices.

What devices did they test?

How did the lemurs respond?

Answer 37

Shapiro, M. E., Shapiro, H. G., & Ehmke, E. E. (2018). Behavioral responses of three lemur species to different food enrichment devices. Zoo biology, 37(3), 146-155.

Abstract: Environmental enrichment is a tool used to promote the welfare and well‐being of captive animals by encouraging the display of species‐specific behaviors and reducing the stress or boredom induced by captive environments. Lemurs are highly endangered, yet few studies have analyzed the behavioral impacts of enrichment on captive populations. We studied the impacts of two novel enrichment devices on three lemur species (ring‐tailed lemurs [Lemur catta], red‐ruffed lemurs [Varecia rubra], and Coquerel’s sifaka [Propithecus coquereli]) to determine both the overall and species‐specific impacts of enrichment on lemur behavior. We recorded lemur behavior using the continuous sampling method to obtain behavior duration and analyzed our results using ANOVA Repeated Measures. Results showed enrichment effectiveness differed for each species and that different enrichment devices had varying impacts on lemur behavior across all species. We attributed the differences in species‐specific responses to the unique locomotor patterns and methods of diet acquisition of each species, and the variances in behavioral responses across all species to the characteristics of each device. Our study highlights the importance of species‐specific enrichment and encourages further research in this field in order to maximize the positive effects of enrichment, which in turn has the potential to affect the overall well‐being of captive populations.

• Ring‐tailed lemurs, red‐ruffed lemurs, and Coquerel’s sifaka looking at three treatments/enrichment and time spent interacting with device
  
  • Food bowl (control)
  • Bottle feeder (enrichment)
  • Hanger (enrichment)
• Bottle feeder was most effective device for ring-tailed lemurs
• Hanger was most effective device for red-ruffed lemurs
• Bottle feeder and hanger were both effective for Coquerel’s sifaka
• Results indicate that the most effective enrichment device for one species may not be the most effective enrichment device for another species
• Enrichment devices significantly increased average duration of locomotion
  
  • Hanger was most effective for increasing locomotion
  • Enrichment devices significantly decreased average duration of resting compared to food bowl
• No significant impact of enrichment or species by enrichment on stereotypic behavior
• Juveniles spent significantly more time locomoting while adults spent more time resting

Question 38

A recent study investigated causes of mortality for teh coquerel’s sifaka.

What age group had the highest mortality rate? What were the four main causes?

For other animals, what were the most common diseases?

Answer 38

Cassady, K., Cullen, J. M., & Williams, C. V. (2018). Mortality in coquerel’s sifakas (propithecus coquereli) under human care: a retrospective survey from the duke lemur center 1990–2015. Journal of Zoo and Wildlife Medicine, 49(2), 315-323.

Abstract: Coquerel’s sifakas (Propithecus coquereli) are diurnal, folivorous lemurs native to Madagascar and one of only two members of the genus Propithecus currently housed in human care settings outside of Madagascar. This species has a lifespan of approximately 30 yr but minimal information exists regarding morbidity and mortality in human care settings. In this retrospective study, medical records, postmortem exam, and autopsy reports from 56 animals housed at the Duke Lemur Center from 1990 to 2015 were evaluated. Mortality assessments included age, sex, time of year, histopathological findings, major organ system impacted, and etiological factors. Mortality was most prevalent among adults greater than 2 yr of age (42.9%) and neonates less than 7 days of age (30.4%). The top four morphological diagnoses accounted for 51.7% of all deaths and included stillbirths (19.6%), enteritis-colitis (12.5%), failure to thrive (10.7%), and systemic protozoal infections (8.9%). The two most commonly affected organ systems in animals over 7 days of age were multisystem disease (30.8%) and the gastrointestinal system (28.2%). Infections were the most common etiology with bacterial being the most prevalent followed by protozoal infections. The results provide insight into common causes of mortality of this species and can be used to guide management of this endangered primate and improve longevity in human care settings.

• Introduction:
  
  • Coquerel’s sifakas – diurnal lemur native to Madagascar.
• M+M:
  
  • Retrospective 56 animals, 1990-2015.
• Results/Discussion:
  
  • No significant difference in mortality based on sex.
  • Adults and perinatal group majority of deaths.
    
    • Perinatal deaths were within the first 3 days of life. Most stillbirths.
  • Number of infections attributed to protozoa or amoeba remarkable with small sample size.
    
    • This species may be particularly susceptible.
    • Systemic infections due to Acanthamoeba, Naegleria, Toxoplasmosis, Neospora in 5 animals, Cryptosporidium in 4 others.
    • Toxoplasmosis not a major contributor to mortality in this study.
  • Primary cardiac dz not identified in any animal. Contrasts with great apes.

Question 39

A recent study described the health assessment of wild brown lemurs on Mayotte Island.

What is the history of this group of lemurs?

What were some of the common findings on examination?

What bacterial, viral, and parasitic pathogens were appreciated in this assessment?

Answer 39

Quintard, B., Lefaux, B., Lécu, A., Niphuis, H., Roux, P., & Ortiz, K. (2019). Biomedical evaluation of a brown lemur (Eulemur fulvus spp.) population from Mbouzi islet, Mayotte island. Journal of Zoo and Wildlife Medicine, 50(3), 650-658.

Abstract: The brown lemur population (Eulemur fulvus spp.) in Mbouzi islet is not native, and was introduced in 1997. Since then, the population has grown. In 2012 the National Council for Protection of Nature of Mayotte requested to remove this population of lemurs from Mbouzi, as they were suspected to be a threat to the protected endemic flora of the islet. The Association Francophone des Vétérinaires de Parcs Zoologiques (French-speaking Zoo Veterinarians Association, AFVPZ) was asked to conduct a biomedical evaluation of the population. Fifty-two animals were captured, anesthetized, and weighed. They all underwent a general physical examination. Feces were sampled for bacterial and parasitological screening. Hair was sampled for genetic studies and blood was sampled for hematology, biochemistry, viral serology, and haemoparasitology. Results showed that three individuals had a positive feces culture for Salmonella enterica and six had Lemuricola or Callistoura parasite infestations. Blood analyses for hematology and biochemistry showed 46 animals with elevated transferrin, 42 with low ferritin levels, 19 with hyperglycemia, and 10 with neutrophilia. Finally, 10 were positive for Toxoplasma serology, one was positive for α herpesvirus, five for pox virus, five for simian virus 40, and two for flavivirus. This publication reports the first complete biomedical evaluation of lemurs on Mayotte Island.

• Introduction:
  
  • Brown lemurs introduced on Mayotte Island (Comoros - Island Nation north of Madagascar) from Madagascar, now integrated into local ecosystem.
  • Potential threat to endemic flora, full biomedical evaluation of the population performed.
  • Human interaction is common in this group – banana feeding twice a week ~15yrs.
• Results/Discussion:
  
  • All masked down with iso for PE, sample collection.
  • 31% had significant hair loss on hands, forearms, tail, one had lice, some dental dz. Hair loss attributed to nutritional deficiency. Zinc, protein, iron and vit B deficiencies have been associated with alopecia in primates.
  • NSD for any of the hematologic values between sexes.
  • Toxoplasmosis titers positive in 10/52 individuals. No felids present on the island, so exposure is likely to be anthropogenic.
  • Only oxyurids on fecals i.e. Lemuricola spp and Callistoura spp parasites, no hemoparasites found.
  • 3 positive salmonella enterica enterica fecal culture. One Ab positive for HSV1. 10% Ab positive for pan polyomavirus. 5 animals Ab positive for poxvirus.
  • All animals hyperglycemic, attributed to stress of capture. Potential for developing DM.
  • Iron overload possible in this group due to low ferritin and elevated transferrin saturation percentage.
• Takeaway: Impact of human activity likely resulting in poor hair coat condition, teeth status, and iron metabolite levels in this population. May also be reason for the HSV1 positive animal and exposure to toxoplasmosis in this population.

Question 40

A recent study investigated two lemur species residing near an active mine site in Madagascar.

What was their general health like?

What differences in trace minerals were present in these animals versus animals at a more pristine location?

Answer 40

Junge, R. E., Williams, C. V., Rakotondrainibe, H., Mahefarisoa, K. L., Rajaonarivelo, T., Faulkner, C., & Mass, V. (2017). Baseline health and nutrition evaluation of two sympatric nocturnal lemur species (Avahi laniger and Lepilemur mustelinus) residing near an active mine site at Ambatovy, Madagascar. Journal of Zoo and Wildlife Medicine, 48(3), 794-803.

Abstract: Extractive industries can have significant impacts on ecosystems through loss of habitat, degradation of water quality, and direct impact on floral and faunal biodiversity. When operations are located in sensitive regions with high biodiversity containing endangered or threatened species, it is possible to minimize impact on the environment by developing programs to scientifically monitor the impact on resident flora and fauna species in the early phases of operation so that effects can be mitigated whenever possible. This report presents the baseline health, nutrition, and trace mineral evaluation for 33 Avahi laniger (Eastern wooly lemur) and 15 Lepilemur mustelinus (greater sportive lemur) captured and given complete health evaluations that included the measurement of fat-soluble vitamins and trace minerals in addition to routine complete blood counts, serum chemistries, and parasite evaluations. All lemurs appeared healthy on physical examination despite the presence of minor wounds consistent with interspecies aggression in some individuals. Serum chemistry values were within expected ranges for other lemur species; however, A. laniger erythrocytes were significantly smaller than those of L. mustelinus. Serum nickel values were markedly higher than expected in both species, and selenium, copper, and cobalt levels were higher in L. mustelinus compared with A. laniger at the study site, as well as values for I. indri or P. diadema reported from other locations. Endoparasites and ectoparasites were typical of those reported in other wild lemur species, but load and diversity varied between A. laniger and L. mustelinus despite inhabiting the same forest ecosystem. This baseline assessment provides the foundation for ongoing monitoring.

• Eastern wooly lemur and greater sportive lemur
  
  • Small, folivorous, nocturnal lemurs
  • Sympatric in the forests in the Ambatovy region in Madagascar
• M + M
  
  • Anesthetized with telazol
  • PE, CBC/chem, fecal, ectoparasite collection
  • Measurement of vitamins A, E, beta carotene, and 25, hydroxycholecalciferol
  • Serum trace mineral analysis for cobalt, copper, iron, nickel, manganese, molybdenum, selenium, and zinc
• Results/discussion
  
  • Both species appear to be carotenoid non-accumulators
  • A. laniger erythrocytes were significantly smaller than those of L. mustelinus
  • nocturnal L. mustelinus has significantly lower vitamin D than diurnal I. indri and P. diadema
  • L. mustelinus, which sleeps in tree holes during day, had lower vitamin D levels than A. laniger, which sleeps in trees during day.
    
    • Exposure to natural sunlight may contribute to vitamin D generation in both diurnal and nocturnal lemur species
  • Cobalt, copper, selenium, and zinc were all higher in L. mustelinus than in A. laniger
    
    • Differences in serum cobalt and selenium were significant
      
      • Median levels of selenium and cobalt in L. mustelinus far exceeded those of either A. laniger at Ambatovy, I. indri evaluated at Analamazoatra, or P. diadema at Tsinjoarivo
        
        • A. laniger at Ambatovy, and I. indri at Analamazoatra by Junge and Barrett considered selenium deficient if compared to normal from other animals
  • Markedly lower levels of iron and higher levels of nickel and zinc in A. laniger and L. mustelinus
  • No major concerns or signs of illness in animals sampled

Question 41

A recent study described the successful breeding of a pair of Philippine tarsiers.

What is unique about this species diet?

What were the key husbandry paramters for this species?

How were the pair introducted for successful breeding?

Answer 41

Řeháková, M. (2019). Successful breeding attempt of a pair of Philippine tarsier (Tarsius syrichta) in a conservation center in Bilar, Bohol, Philippines and recommendations for tarsier husbandry. Zoo biology, 38(6), 516-521.

Abstract: The Philippine tarsier (Tarsius syrichta) belongs to the least known nocturnal primates. Tarsiers and remaining biodiversity of the Philippines are under tremendous threats from increasing human expansion, with habitat loss and illegal pet trade being the main reasons for tarsier population decline. In addition, even though the attempts were made by western and local facilities, tarsiers have not survived well in captivity. In this paper, I present an example of successful breeding of the Philippine tarsier in captive conditions but in natural climate. As the most important elements of success, I see a large amount of space provided to tarsiers, the climate similar to their natural habitat and the food resembling their natural diet. Our pair of tarsiers were joined during the mating period and held separately outside the mating period, which corresponds with their behavior in the wild and may have played a crucial role in breeding success. Eliminating stress to animals is also important. The study can provide valuable guidelines for other facilities keeping tarsiers in the Philippines and help to improve tarsiers’ welfare and in the future help to establish a viable captive population of the Philippine tarsier that will serve as a backup population and also will decrease demand on tarsiers captured from the wild.

• Philippine tarsiers are an endangered species that have had little success in captivity and captive breeding has been challenging
• Nearly 89% captive‐born T. syrichta did not live beyond the first year and there were no recorded cases of successful second‐ generation reproduction in the Philippine tarsiers
• They are the only strictly carnivorous primates (insects, spiders, crustaceans, small vertebrates)
• Solitary species, seasonal breeders
• This paper describes condition husbandry practices used in a captive pair that bred successfully, conservation center in Bohol, Phillippines
• Temperature and humidity kept at natural conditions (24.3 C and 95.2% respectively)
• Tarsiers given lots of space and sheltered areas
• Given as close to natural diet as possible, many live caught from the wild
• Breeding pair was held together during mating period and separated otherwise
• The first breeding resulted in a suspected stillbirth
• The second a year later was successful

Question 42

A recent study described the breeding of ring-tailed lemurs.

What is the natural social structure of these species?

What is neonatal mortality like?

What social structure in managed setting appears to be key to increasing success?

Answer 42

Breton, G., Thibault, S., Werts, M., & Baudry, E. (2019). Captive ring‐tailed lemur breeding in semi‐free ranging conditions and genetic parentage analysis. Zoo biology, 38(3), 281-291.

Abstract: The ring‐tailed lemur (Lemur catta), one of the most iconic and widely recognized primates in the world, is threatened in its native range and classified as endangered by the International Union for Conservation of Nature. The global conservation strategy for the species includes ex situ conservation efforts led by zoological institutions in the framework of regional captive breeding programs. To maximize the conservation of genetic diversity and optimize breeding programs, an accurate pedigree must be established in captive populations. Our study documents the formation and subsequent monitoring of a large ring‐tailed lemur group in a French zoological institution. Based on staff’s behavioral observations and DNA analyses using 11 microsatellite markers, we were able to document the survival and reproduction rates of the lemurs in this situation and reconstruct the pedigree of infants born in the institution. In total, 22 of the 28 imported animals as well as 4 locally born individuals gave birth to 58 infants of which 28 survived. The consistent genotypes obtained from the 53 sampled animals allowed us to identify 25 of the sires and 27 of the dams for the 28 surviving infants. A total of 12 different females and 14 different males produced the 28 surviving infants, suggesting that no individual dominates reproduction. This pioneering study has practical applications for the captive management of the species, which can be raised to the individual level instead of the group level.

Background

• Ring-tailed lemur - native range Madagascar, endangered IUCN
  
  • Live in multi-male female troops of 6-24 in the wild with core of 2 or 3 related females
  • Aggression within and between troops is common
  • Cause of infant mortality in wild: natural predation, severe drought, infanticide by adult males, female indifference or aggression
  • Live up to 30 yrs in captivity (20 in the wild)
  • Mating season in the wild: mid-April; Parturition late Aug-Oct; gestation 135-141 days
  • Targeted aggression or fissioning begins at critical number of ~7 females

Key Points

• Offspring survival rate to adulthood: 48% (similar to wild 30-51% up to 80%)
  
  • Mortality rate at 3rd month: 46% (cause of death 40.7% disappeared, 15% unidentified conflict, infanticide by black lemurs was noted)
  • 64% births in March, 24% in April, some in Feb and June - shift from wild due to photoperiod difference in the Northern Hemisphere
  • Sex ratio even
• No single male dominance in siring infants with paternity shift over time as younger males aged
  
  • Males gained access to females from 2.5 yrs and started producing surviving infants after age 3 - similar to wild
• Dominant females produced the most infants and oldest females bred throughout entire study period
  
  • All adult females helped to raise young, infants were frequently exchanged leading to dam-infant dyad misidentification by staff
  • Carry their young ventrally until 3 wks when they move to the back and start expanding relationships to other related females and males

Conclusions

• Ring-tailed lemurs have few behavioral and veterinarian problems, excellent breeding success, and thrive in captivity
• Recommend starting a troop with a small number of related females
• Avoid housing with black lemurs due to risk of infanticide of ring-tailed infants
• Recommend giving staff time to gain recognition expertise and allow precise group management so that all individuals can be accurately recognized
• Genetic tracking clearly identified pedigree even between closely related animals
• Encourage other institutions to use genetic methods to document pedigree and aid in studbook management of the ring-tailed lemur, an endangered species

Question 43

A recent paper described an outbreak of Yersinia enterocolitica at the Omaha Zoo.

What is teh most common biotype in animals?

What are the typical clinical signs adn lesions that were described in the lemurs in this study?

Answer 43

CLONAL SPREAD OF YERSINIA ENTEROCOLITICA 1B/O:8 IN MULTIPLE ZOO SPECIES

Christie L. Hicks, DVM, Julia E. Napier, DVM, Douglas L. Armstrong, DVM, Lori M. Gladney, Cheryl L. Tarr, PhD, Molly M. Freeman, PhD, and Peter C. Iwen, PhD, D (ABMM)

Abstract: Yersinia enterocolitica (YE) bioserotype 1B/O:8 (YE 1B/O:8) was identified in routine culture of a variety of zoo species housed at Omaha’s Henry Doorly Zoo and Aquarium (OHDZA) from April to July 2011. Animal cases representing 12 species had YE detected from 34 cases during routine fecal monitoring and/or during postmortem examination: Coquerel’s sifakas (Propithecus coquereli, two cases), black & white (BW) ruffed lemurs (Varecia variegata variegata, six cases), red ruffed lemurs (Varecia rubra, seven cases), white handed gibbon (Hylobates lar albimana, one case), black lemurs (Eulemur macaco, three cases), mongoose lemurs (Eulemur mongoz, two cases), African hunting dogs (Lycaon pictus, five cases), agile gibbons (Hylobates agilis, three cases), siamangs (Hylobates syndactylus, two cases), colobus monkey (Colobus angolensis palliates, one case), argus pheasant (Argusianus argus, one case), and orangutan (Pongo pygmaeus, one case). Most species were not symptomatic; however, three symptomatic cases in Coquerel’s sifakas (two) and a white handed gibbon (one) showed clinical signs of diarrhea and lethargy that resulted in death for the Coquerel’s sifakas. One unexpected death also occurred in a BW ruffed lemur. To the authors’ knowledge, this is the first report of YE 1B/O:8 in such a large variety of zoo species. The source of the YE could not be identified, prompting the initiation of a diseases surveillance program to prevent further cases for the species that are sensitive to YE. To date, no additional cases have been identified, thus suggesting a single introduction of the YE 1B/O:8 strain into the zoo environment.

Journal of Zoo and Wildlife Medicine 51(1): 170–176, 2020

Importance: low- not a new species, first report of an outbreak in this many species but has been reported in all of those species previously, good to know the important biotypes

Introduction:

• Yersinia enterocolitica = gram negative coccobacillus
  
  • Six biotypes (1A, 1B, 2, 3, 4, 5) and 60 serotypes
  • Cause of GI disease in humans and many animals (birds, mammals, reptiles)
  • Most common cause of disease in animals = biotype 1B/O:8; biotype 4B/O:3 is an emerging pathogen

Methods/results:

• Study describing the clonal spread of YE biotype 1B/O:8 at a zoo with shedding seen in multiple species
  
  • Detected in 34 cultures from 12 species over about 100 days
  • Several different areas of the zoo
  • Range from asymptomatic shedding - mild disease - acute disease- death
    
    • Most severe in the nonhuman primates
    • Acute death in BW ruffed lemur
      
      • Necropsy lesions: abscesses of the large intestines, lymph nodes, liver
    • Coquerel’s sifaka- presented for dehydration/lethargy, supportive care given but died
      
      • Necropsy lesions: severe necrotizing ulcerative hemorrhagic enteritis; second lemur = liver necrosis, DIC
      • Negative for YE at the time of necropsy?

Discussion:

• Suspect all cases came from a common exposure to a single strain
• Exposure to YE primarily from contaminated food or water
• Zoonotic transfer to/from humans has to be considered during an outbreak

Comments/questions:

• A little confused on what “clonal spread” means in this context- I think it’s just that the same bacterial strain was seen throughout the case outbreak
• Definition found online- Clonal spread of a resistant strain: Under the selective pressure of antibiotics a strain carrying antimicrobial resistance genes may be preferentially selected and transferred within a population.

Question 44

A recent study described a health assessment of black and white ruffed lemurs in madagascar.

Were there any significant differences in values from managed lemurs?

Any differences by sex?

Answer 44

HEALTH ASSESSMENT OF BLACK-AND-WHITE RUFFED LEMURS (VARECIA VARIEGATA) IN RANOMAFANA NATIONAL PARK, MADAGASCAR

Journal of Zoo and Wildlife Medicine 52(4): 1095–1104, 2021

Abstract: The Anthropocene is a major threat to biodiversity worldwide. Human pressures including climate change and emerging infectious diseases are presenting new challenges to wildlife, requiring vigilance and monitoring of wild populations to ensure their persistence. In order to monitor fluctuations in health, baseline data from long-term studies are required. Clinical laboratory data on 80 black-and-white ruffed lemurs (Varecia variegata), derived from the capture of 98 individuals spanning six field seasons are presented. Serum biochemical profiles showed variation between years that remained within published reference intervals for the species, with the exception of total bilirubin in 2008, and creatine kinase and chloride in 2019. Serum trace minerals and fat soluble vitamin values also fluctuated between years and are within ranges seen in other lemur species. These results, combined with previously published data on ectoparasite load and population genetic diversity, suggest that the Mangevo ruffed lemur population is healthy and can provide important and valuable baseline data for comparisons moving forward.

Intro

• Black-and-white ruffed lemur behavioral ecology and genetics have been the focus of longitudinal research in Ranomafana National Park (Madagascar) since 2005. This paper presents the conclusions from health and nutrition assessments of 98 individuals over that time period

M&M

• Lemurs anesthetized using telazol
• PE and tracker tagged, fecal, biochemistry, vitamin and mineral panel

Results and discussion

• N = 80 (39 males, 41 females)
• Body weight and PE parameters did not differ between sexes
• For biochemistry, there is statistically significant variation between years for nearly every parameter measured.
• However, with the exception of three parameters (total bilirubin [T bili] in 2008; chloride [Cl], and creatine kinase [CK] in 2019), all of these results fall within the reference ranges determined for this species in human care
• Results of trace mineral and fat-soluble vitamin analyses–no reference interval available to compared to relatively similar lemur species there are some differences, likely due to diet
  
  • Cu, Fe, Mn and Zn similar. Co higher in other lemur species, Se levels higher in the study population
  • Mo detected some years and not others. Unclear significance.
• When examining sex differences, males and females only differed in their Vitamin D values (lower in females). Suspected to be correlated with pregnancy and parturition but could not be confirmed

Question 45

A recent study investigated wound management of ring-tailed lemur bite wounds.

Where did wounds most commonly occur?

What are some common indicators of pain in lemurs?

What analgesics and antibiotics were commonly used?

Answer 45

J Zoo Wildl Med 2021 52(4): 1263–1269

A RETROSPECTIVE STUDY OF BITE WOUND MANAGEMENT IN RING-TAILED LEMURS (LEMUR CATTA) HOUSED WITHIN FIVE BRITISH ZOOS

Ceccolini ME, Hedley J, Chang Y, and Guthrie A

ABSTRACT: Captive nonhuman primates frequently experience bite wounds inflicted by conspecifics; however, few studies evaluate wound management in these animals. This study evaluates bite wound management in 35 captive ring-tailed lemurs (RTL, Lemur catta) held within five British zoological institutions between 2015 and 2019. Treatments for 152 bite incidents resulting in 211 bite wounds were summarized. Treatment efficacy and potential risk factors for bite wound complications were evaluated for correlations with outcomes. Treatments in the first 48 hours included analgesia alone (54/152; 35.5%); analgesia and antimicrobials (42/152; 27.6%); no treatment (26/152; 17.1%); analgesia, antimicrobials, and wound management under anesthesia (24/152; 15.8%); and antimicrobials alone (6/152; 3.9%). Poor outcomes were observed in RTL in association with 20.4% of wounds (43/211): signs of pain (SOP) after 48 hours were the most common (30/211; 14.2%), followed by signs of infection (SOI, 16/211; 7.6%), wound dehiscence (7/211; 3.3%), and abnormal function or behavior at day 30 (4/ 211; 1.9%). Poor outcomes were more likely with severe bite wounds and bite wounds to the hand or limb (thoracic or pelvic, excluding the hand or foot). Specifically, SOP were more likely to be observed with severe wounds and solitary wounds, and SOI were more likely to be observed with wounds not treated with early antimicrobials. When SOI occurred, most resolved with antimicrobial treatment alone. Early analgesia is recommended for RTL with bite wounds. If SOP persist, multimodal analgesia should be administered. Clinicians should consider withholding antimicrobials for RTL with bite wounds of mild and moderate severity until SOI are observed

Goal: Summarize bite wound management of ring-tailed lemurs held in British institutions over a 5-yr period; evaluate associations between wound factors, treatments, and outcomes; and provide recommendations based on these findings

Key Points:

• Bite wounds from conspecifics are common in captive NHP
  
  • Despite this frequency, literature re: outcomes of bite wound management are limited to single case reports and a study on tetanus management
• Treatments were commonly administered to severe and/or multiple bite wounds
  
  • Wounds to the feet or head, closed wounds, and solitary wounds were treated less frequently
• In humans, bite wounds to the hand are at high risk for infection, tendinitis, and joint stiffness because of the potential involvement of tendons, joint capsules, and bone
• Compared to multiple wound incidents, solitary wounds were more likely to result in SOP
  
  • Licking and overgrooming are potential indicators of pain
  • Meloxicam was the most commonly analgesia used
  • The use of analgesia was not a predictor of wound outcome
• Early antimicrobials were prescribed in almost half of the incidents
  
  • Human inflicted bite wounds are reported to have infection rates of 20–25%
  • The use of prophylactic antimicrobials for bite wounds in humans remains controversial
  • In this study, bite wounds had an overall infection rate of 7.6%
  • 13.3% of wounds untreated and 3.3% of wounds treated developed SOI
  • Although RTL have a large hindgut, diarrhea was not observed despite the frequent use of beta-lactams
• Surgical repair was performed on 51 wounds in this study, including five hand wounds
  
  • Only one on the body developed SOI, suggesting that surgical repair is unlikely to increase risk of infection

TLDR:

• Poor outcomes were uncommon but occurred more w/ severe wounds and bite wounds to the limbs or hands
• SOP were more likely to be observed with severe wounds and solitary wounds
• Although SOI occurred more when early antimicrobials were NOT administered, SOI were uncommon overall, and most resolved once antimicrobials were administered
  
  • Consider withholding antimicrobials for bite wounds of mild to moderate severity until SOI are observed

Question 46

A recent study described vertical transmission of Toxoplasma gondii in red ruffed lemurs.

What are the typical presentations associated with toxoplasma infection in lemurs?

How did these cases present? Was treatment effective?

What are the three possible scenarios for reactivation of latent toxoplasma in pregnant lemurs?

Answer 46

OUTCOMES OF TRANSPLACENTAL TRANSMISSION OF TOXOPLASMA GONDII FROM CHRONICALLY INFECTED FEMALE RED RUFFED LEMURS (VARECIA RUBRA)

Geoffrey R. Browning, MS, DVM, Cora Singleton, DVM, DACZM, Dean Gibson, MS, and Ilse H. Stalis, DVM, DACVP Journal of Zoo and Wildlife Medicine, 2021;52(3):1036-1041

Abstract: Ten red ruffed lemurs (Varecia rubra)—two adult females and their eight offspring—were evaluated in this case series. Two adult females were diagnosed with chronic, latent toxoplasmosis based on serologic testing. The first female lemur had two successive pregnancies. The first pregnancy resulted in transplacental transmission of Toxoplasma gondii. The only surviving offspring was diagnosed with congenital toxoplasmosis based on serologic testing and compatible ophthalmic lesions. The two deceased offspring had disseminated nonsuppurative inflammation and intralesional protozoal organisms consistent with T. gondii, which was confirmed by polymerase chain reaction. The second pregnancy did not result in transplacental transmission. The second chronically infected adult female lemur had one pregnancy that resulted in a single stillborn fetus without evidence of transplacental transmission of T. gondii. Treatment with trimethoprim-sulfamethoxazole and folinic acid was administered to the first adult female and one offspring, but no treatment was given to the second adult female. All surviving lemurs had no further complications associated with toxoplasmosis. This case series demonstrates that chronic, latent infection of reproductive female red ruffed lemurs with T. gondii may result in variable outcomes: (1) transplacental transmission with disseminated fetal infection and stillbirth, (2) transplacental transmission with congenital infection and survival, or (3) lack of transplacental transmission and healthy offspring. Information gained from these cases may help guide recommendations for breeding of this critically endangered species.

Key Points:

• Red ruffed lemurs are prosimians native to Madagascar
• Toxoplasma gondii is apicomplexan protozoa
  
  • Felids are definitive hosts – ingestion of sporulated oocysts, intermediate hosts or transplacental transmission can occur
  • Frequently infection is asymptomatic but results in chronic lifelong latency
• Acute disseminated toxoplasmosis and localized (placentitis, stillbirth, disseminated fetal infection) infection reported in ring tailed lemurs
• Case series described outcomes of pregnancies in two latently infected with T gondii.
• Case 1
  
  • Nulliparous female with chronic toxoplasmosis diagnosed based on chronically elevated T gondii IgG and chorioretinal scars
  • 2/3 neonates died secondary to in utero infection with T gondii (reactivation of chronic latent infection occurred during pregnancy with transplacental transmission to the offspring)
    
    • Disseminated lesions in 2 - T gondii protozoa seen in lung, kidney, and adipose tissue. PCR positive placenta and liver.
    • One survived with chorioretinitis alone - surviving neonate diagnosed with congenital latent toxoplasmosis (inactive chorioretinitis and positive IgG) and treated with TMS and folinic acid for 1 year.
      
      • Neonates will have maternal IgG and antibodies, so measurement of IgM and follow-up serology at 6-12 months is recommended to exclude maternal transfer
  • Treated with TMS and folinic acid for 1 year – gave birth 16 mo after treatment ended and 2/4 survived
    
    • No evidence of transplacental transmission based on serology and post mortem exams
• Case 2
  
  • 10 yr old lemur tested positive for T gondii during quarantine evaluation. Two years later animal had a stillbirth. Dam was T gondii positive 1day after parturition but no evidence of toxoplasmosis in the neonate nor placenta.
  • Lemur with chronic latent toxoplasmosis can have first pregnancy free from reactivation and transplacental transmission
• Birth outcomes of two red ruffed lemurs with serologic evidence of chronic latent toxoplasmosis
  
  • Reactivation of latent toxoplasmosis with transplacental transmission and survival of congenitally infected offspring
  • Gestational reactivation of latent toxoplasmosis is NOT universal across successive pregnancies nor individuals
• Previous report of T gondii infection in ring tailed lemur which resulted in reactivation, transplacental transmission and disseminated toxoplasmosis (hepatic necrosis and encephalitis) in all fetuses followed by death in the dam from myocardial toxoplasmosis.
• Recommend minimizing stress during gestation in chronically infected lemurs.
• No definitive reason for lack of reactivation and transplacental transmission of T Gondii in second pregnancy of case 1 and in case 2
• Single episode of gestation reactivation of latent toxoplasmosis does NOT predict future gestational reactivation in red ruffed lemurs
  
  • Reactivation of latent toxoplasmosis may not cause clinical disease in the dam and transplacental transmission is not universally fatal to the offspring.

Take home:

In chronic, latently infected red ruffed lemurs, pregnancy can stimulate reactivation causing

1. Transplacental transmission and fetal death
2. Transplacental transmission and congenital latent toxoplasmosis

Can also have a lack of reactivation of latent toxoplasmosis

Question 47

A recent study described the management of congestive heart failure in a ring-tailed lemur.

What congenital abnormality was detected on echocardiography?

What drugs were used to control the signs of heart failure?

How long was the case successfully managed?

Answer 47

Journal of the American Veterinary Medical Association 257(8): 849-854 2020

Long-term management of congestive heart failure secondary to mitral stenosis in a ring-tailed lemur (Lemur catta)

Shane D. Murphy, DVM, Jessica L. Ward, DVM, Jodi D. Smith, DVM, PhD, Andrew J. Gall, DVM, June E. Olds, DVM (Reviewed by KMT)

Abstract:  

CASE DESCRIPTION: A 15-year-old sexually intact female ring-tailed lemur (Lemur catta) was evaluated for a heart murmur and progressive radiographic cardiomegaly.

CLINICAL FINDINGS: The lemur was clinically normal at the time of initial evaluation. Results of transthoracic echocardiography performed when the animal was anesthetized indicated mitral valve stenosis and severe left atrial dilation. Three months later, signs of left-sided congestive heart failure (CHF; coughing, exercise intolerance, and tachypnea) were observed and confirmed by the presence of radiographic pulmonary edema.

TREATMENT AND OUTCOME: Medical treatment that consisted of aspirin, benazepril, furosemide, pimobendan, spironolactone, and ultimately torsemide in lieu of furosemide successfully controlled the lemur’s clinical signs for 33 months after the development of CHF. Euthanasia was then elected on the basis of perceived poor quality of life because tachypnea became refractory to progressively higher dosages of diuretic. Necropsy confirmed mitral stenosis with severe left atrial dilation and chronic pulmonary congestion.

CLINICAL RELEVANCE: The present report described the long-term medical management of CHF secondary to mitral stenosis in a lemur. Mitral stenosis was suspected to be a congenital defect, similar to the cause of mitral stenosis reported for dogs and cats, rather than to be an acquired change in association with rheumatic heart disease as commonly occurs for people. The lemur’s CHF was well managed for 33 months with treatment, including pimobendan, which was well tolerated. (J Am Vet Med Assoc 2020;257: 849–854)

Key points:

• 15 yo FI RTL presenting with heart murmur (grade 3/6 diastolic, PMI over left apex) and radiographic cardiomegaly, no clinical signs initially, normal CBC/Chem
  
  • First noted incidentally at 4 yo, murmur was noted intermittently during immobilizations throughout life
  • Progressive LA enlargement on radiographs
  • Echocardiogram under anesthesia at 15yo showed mitral valve stenosis and severe LA dilation
• Medications utilized in treatment included aspirin and benazepril initially
• 3 months after echo, lemur developed cough and exercise intolerance à started on pimobendan and furosemide
• Cough recurred and noted increased respiratory effort 10 months later à progressively increased furosemide dosage
• 13 months after presumptive diagnosis of CHF, immobilized again and found progressive disease, increased pimo and started spironolactone as well as activity restriction, free access to air conditioning
• Good clinical control for subsequent 12 months, then increased RR and effort à changed to torsemide from furosemide
• RR was progressively increasing 7 months later, increased torsemide dosage but no clinical improvement
• Lemur was euthanized at 18yo and 33months following initial onset of CH

Question 48

A recent study established baseline values for assessment of heart disease in ring-tailed lemurs.

What imaging modalities were assessed?

What is cardiac troponoin T? What causes elevations?

What is NT-ProBNP? What causes elevations?

Answer 48

THORACIC RADIOGRAPHY AND TRANSTHORACIC ECHOCARDIOGRAPHY IN CLINICALLY HEALTHY RING-TAILED LEMURS (LEMUR CATTA)

Blandine Houdellier, Laurent Locquet, Jimmy H. Saunders, Bart J.G. Broeckx, Tim Bouts, Pascale Smets

J. of Zoo and Wildlife Medicine, 51(2):308-320 (2020).

Taxonomy: Primates (order) → Lemuridae (family) → Lemur (genus)

Abstract: Cardiac disease has been recognized as a major cause of death in captive nonhuman primates, which necessitates diagnostic (imaging) techniques to screen for and diagnose preclinical and clinical stages of possible cardiac conditions. Echocardiography is currently the most commonly used diagnostic tool for evaluation of cardiac anatomy and function. Complete with thoracic radiography and blood levels of two cardiac biomarkers, N-terminal probrain natriuretic peptide (NT-proBNP) and cardiac troponin T (cTnT), it gives an extensive examination of the cardiorespiratory system. The purpose of this cross-sectional cohort study is to describe normal thoracic anatomy using thoracic radiography, and to provide normal values for echocardiographic measurements in 20 ring-tailed lemurs (Lemur catta). Additionally, cardiac biomarkers were determined. Three radiographic projections of the thoracic cavity and a complete transthoracic echocardiography were performed in 20 clinically healthy ring-tailed lemurs during their annual health examinations. Similar standard right parasternal and left apical echocardiographic images were obtained as described in dogs and cats and normal values for routine two-dimensional (2D-), time-motion (M-) and Doppler mode measurements were generated. Furthermore, a noninvasive smartphone base ECG recording and blood concentrations of cardiac biomarkers were obtained. Other radiographic measurements are provided for the skeletal and respiratory systems such as the trachea to inlet ratio and tracheal inclination. Knowledge of the normal radiographic thoracic and echocardiographic anatomy and function are fundamental for the diagnosis and follow-up of cardiac disease in affected individuals and for species screening, and will be of added value in future research in and conservation of this endangered species.

Key Points:

• Dilated cardiomyopathy, hypertrophic cardiomyopathy, fibrosing cardiomyopathy
• Cardiac troponin T
  
  • intracellular protein,bound to the actin backbone within cardiomyocytes. As cells are damaged, leaks into circulation
  • Gene thought to be highly conserved across sps
  • Elevations = recent damage of cardiomyocytes (and cardiomyopathies)
    
    • cTnT can be elevated from non-cardiac causes (renal failure)
  • Median value for lemurs in this study = 269.7ng/L
• NT-ProBNP below detection for all animals. (could mean test doesn’t work, or healthy animals have low value)
  
  • Increased secondary to myocardial stretch. Helps distinguish between cardiogenic and resp causes of dyspnea
  • Can be elevated w/ renal failure and inflammation not related to heart
• 17 animals had trace valvular regurgitation
  
  • One animal had LV hypertrophy, aortic and tricuspid valve insufficiency, radiographic cardiomegaly
    
    • Cardiac markers were not significantly different for this individual compared to others in group
• Lemurs have clavicles, first lumbar vertebrae had remnants of ribs
• Case report of congestive heart failure in ring-tailed lemurs
• Systolic volume higher in L apical view vs. R parasternal view

Take Home Message: Ring tailed lemurs: Normal thoracic rads, normal echo parameters, cTnT was elevated in all individuals (not different between one individual with cardiac disease and other healthy), NT-proBNP not measurable.

Question 49

A recent study investigated the effects of olfactory stimulation on the behavior of ring-tailed lemurs.

What is the scientific name of this species?

How did the addition of olfactory enrichment change their behavior?

Was a specific scent preferred?

Answer 49

The effects of olfactory stimulation on the behavior of captive ring‐tailed lemurs (Lemur catta).
Baker B, Taylor S, Montrose VT.
Zoo biology. 2018;37(1):16-22.

Ring-tailed lemurs reside in many animal collections worldwide. Lemur welfare may be a cause of concern due to some captive individuals exhibiting stereotypic behavior. Despite these concerns, there has been little exploration of methods of environmental enrichment for ring-tailed lemurs. Olfactory stimulation can enhance captive animal welfare by encouraging species-typical behaviors, enhancing behavioral diversity, and decreasing stereotypic behaviors. We aimed to investigate the effects of olfactory stimulation via lavender, peppermint, coconut, and prey odor upon the behavior of eight captive ring-tailed lemurs. We exposed the lemurs to six individual odor conditions (odor control, novel object control, lavender, peppermint, coconut, and Morio worms) and observed them for 4 hr a day for 3 days with an intervening period of 4 days between conditions. We recorded the lemurs’ behavior under each condition using instantaneous scan sampling. We found significant effects of olfactory stimulation on the ring-tailed lemurs’ behavior in the initial analysis but these did not survive correction for multiple testing. Overall, while our findings are suggestive of a general effect of olfactory stimulation on the captive ring-tailed lemurs they did not indicate a marked influence of olfactory condition. However, further investigation with a larger sample size and more biologically relevant odors may be beneficial to fully examine potential effects of olfactory stimulation in captive lemurs.

Key Points
- Changes found when exposed to any scent but no difference found between scents
- No effect of olfactory stimulation on feeding behavior or one-way grooming
- With scent: higher levels of resting/sleeping behavior, locomotion
- Without scent: more sitting, foraging, drinking, self-grooming, mutual grooming, chasing behavior, scent-marking, vocalization, and vigilance

Conclusions
- Providing olfactory enrichment had a general effect on behavior but no difference found between different scents

Question 50

A recent study investigated the use of lettuce supplementation to promote foraging in red ruffed and black and white ruffed lemurs.

What is the natural diet of these species?
How does what is offered in managed care different?

What was the goal in supplementing lettuce?

What changes in the microbiome were observed?
- What bacteria are present to digest fiber?
- What bacteria interacts with the immune system and is protective against obesity and diabetes?

Answer 50

ZB 2020 39(5) 334-344
Daily lettuce supplements promote foraging behavior and modify the gut microbiota in captive frugivores

Abstract: For captive primates, greater provisioning of leafy greens or foliage can promote natural foraging behavior while boosting fiber intake. Recalcitrant fiber, although minimally available to endogenous metabolism, is readily fermented into nutrients by gut microbes. Whereas most primates in captivity consume fiber‐limited diets and harbor imbalanced gut microbiota compared to their wild conspecifics, the importance of fiber provisioning to primate gut microbiota has predominately been studied in folivores. We, therefore, determined if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores. We provisioned ruffed lemurs (Varecia rubra and V. variegata) with romaine lettuce, on top of the standard dietary fare, for 10 consecutive days. Before and across the period of lettuce supplementation, we collected observational data of animal feeding and fecal samples for microbiome analysis, determined via amplicon sequencing. The ruffed lemurs and their gut microbes responded to lettuce provisioning. In particular, younger animals readily ate lettuce and showed no decline in consumption across study days. When controlling for the effects of host species and social‐group membership, lettuce consumption shifted the composition of the gut microbiome away from each lemur’s own baseline, an effect that became stronger as the study progressed. In the final study days, Ruminococcaceae UCG‐008 and Akkermansia, microbes typically and respectively associated with fiber metabolism and host health, were significantly enriched in the consortia of lettuce‐provisioned subjects. Ultimately, the routine offering of lettuce, leafy greens, or foliage to captive frugivores may benefit animal wellbeing.

Intro
- Among the biggest challenges in zoo welfare and conservation biology is determining the optimal diets to feed endangered wildlife maintained in captivity
- For primates, in particular, a growing concern relates to the discrepancy between dietary plant fibers and sugars
- Whereas recalcitrant plant fibers are abundant in the diets of many wild primates (stemming from their consumption of foliage, and unripe, seedy, or pulpy fruits), captive primates tend to be provisioned with ample orchard produce that has been artificially selected to be sugar dense
- Increased recalcitrant fiber can regulate sugar absorption and modify the gut microbiome
- Goal of this study: to determine if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores

Results
- The ruffed lemurs routinely consumed provisioned lettuce across the study
- older animals consumed lettuce far less frequently than did their younger counterparts.
- Spent more time foraging stalks than leaves
- At the phylum level, the gut microbiome of DLC ruffed lemurs comprised predominantly microbes from Bacteroidetes, Firmicutes, and Proteobacteria, with lesser contributions from Spirochaetes and Verrucomicrobia
- Although all lemurs were fed the same diet, baseline microbiome varied by species
– all red‐ruffed lemurs had greater representation from Bacteroides and an unassigned genus within the Lachnospiraceae family, whereas all black‐and‐white ruffed lemurs had a greater representation of Prevotella 2
- Also found that the lemurs’ gut microbiomes clustered by social group
- When lemur hosts were fed lettuce daily, their gut microbiomes responded, although the effects were minor–no effects on any measure of alpha diversity
- When restricted to to intra‐individual comparisons and controlled for the effects of lemur, social group, and species identities, some patterns emerged
- In the early period, compared to both the baseline and late periods, an unnamed genus from the Tenericutes phylum were enriched in the lemurs’ gut consortia.
- In the late period, compared to both the baseline and early periods, two genera were enriched in the consortia of all supplemented subjects: Akkermansia and Ruminococcaceae UCG‐008

Discussion
- For frugivorous primates in captivity, we show that lettuce can be used as a daily dietary item that functionally serves to boost recalcitrant fiber intake and modify gut microbiome structure.
- Whereas some of the ruffed lemurs’ dominant microbes can be linked to frugivory, like Prevotella that reflects noncellulolytic fiber metabolism,, the abundance of Lachnospiraceae and Ruminococcaceae members highlight the potential for the lemurs’ consortia to metabolize more recalcitrant fibers.
- One such taxon from Ruminococcaceae was enriched in the lemurs’ consortia following consistent lettuce provisioning.
- The other taxon that bloomed as a consequence of prolonged lettuce provisioning, Akkermansia, provides insight into the potential health benefits of lettuce as an enrichment item.
– Akkermansia resides in the mucus layer of the intestines where it interacts with the immune system and affects gut barrier function
– This taxon is known for its inverse relationship with metabolic disorders like host obesity, glucose intolerance, diabetes, and gut inflammation