Prosimians


Chapter 36

Prosimians



Cathy V. Williams



Biology


Prosimian primates are composed of lemurs, lorises, pottos, and galagos. The classification of primates remains somewhat controversial, and taxonomic structure continues to be revised as the increasing amount of genetic information is reconciled with earlier methods of classifications based on morphology and fossil records. Most authorities now follow a systematic arrangement in which the primates are divided into two suborders: (1) Strepsirhini (i.e., the tooth combed primates), and (2) Haplorhini, which includes the tarsiers, monkeys, apes, and humans. The Strepsirhine group is further divided into two infraorders: Lorisiformes and Lemuriformes. The infraorder Lorisiformes includes all the extant African and Asian species of lorises, pottos, and galagos, which are represented by nine genera and 18 species of small-bodied, nocturnal primates.28 The infraorder Lemuriformes is composed of five families endemic to Madagascar: (1) Lemuridae (bamboo lemurs, ring-tailed lemurs, true lemurs, and ruffed lemurs), (2) Indriidae (indri, sifakas, and woolly lemurs), (3) Cheirogaleidae (mouse lemurs, dwarf lemurs, and fork-marked lemurs), (4) Lepilemuridae (sportive lemurs), and (5) Daubentoniidae (aye-aye).


Lemurs are found in a wide range of ecologic niches in Madagascar, including the low to high altitude tropical rain forests on the east coast, the dry deciduous forests of the west, and the spiny deserts of the south. Lorises are native to Southeast Asia and the tropical forests of India and Sri Lanka, and galagos (bush babies) and pottos are distributed throughout Africa south of the Sahara.28


Over the last 2000 years, at least 17 species of lemurs have become extinct, and the ranges of most extant species have decreased dramatically, largely because of human activity. All prosimian species are threatened to various degrees in the wild. All members of the family Lemuridae as well as Nycticebus sp. (slow lorises) are listed in CITES Appendix I by the International Union for the Conservation of Nature (IUCN). Galagos, pottos, and the slender loris (Loris tardigradis) are listed in CITES Appendix II.18 Habitat destruction is the largest threat; however, hunting for bush meat and capture for sale in the pet trade also contribute to their declining numbers.


Many species are not represented in captivity or are present in only very small numbers. Of the lemur species displayed in zoos, Lemur catta (ring-tailed lemur) are most numerous followed by Varecia (ruffed lemurs) and Eulemur (true lemurs or black and brown lemurs). Increasingly, Propithecus (sifaka) and Daubentoina (aye-aye) are found on display in North American and European zoos as better husbandry and feeding programs for these species are developed. Galagos, although not present in zoos in large numbers, are often used in research settings.



Unique Anatomy


Considerable anatomic variations exist among prosimian primates. Adult weights range from 30 grams (g) for the smallest mouse lemur (Microcebus myoxinus) to more than 8 kilograms (kg) for the largest lemur species.24 Table 36-1 contains biologic information on prosimian species commonly kept in captivity.



All prosimians, with the exception of aye-aye (Daubentonia), have tooth combs, an adaptation in which the lower incisors together with the lower canine teeth project forward almost horizontally. The tooth comb is used for mutual grooming and self-grooming. The typical dental formula for prosimians is 2/2, 1/1, 3/3, 3/3, although exceptions exist. In the aye-aye, the dental formula is 1/1, 0/0, 1/0, 3/3. The aye-aye incisors are long, laterally compressed, and continuously growing as in rodents. The roots of the lower incisors are extensive and form a half circle within the mandible, extending caudally into the coronoid process. Sifakas (Propithecus) have one less lower incisor (dental formula 2/1, 1/1, 2/2, 3/3), and sportive lemurs (Lepilemur) lack upper incisors entirely (dental formula 0/2, 1/1, 3/3, 3/3).17


Lorisiform prosimians are small bodied and nocturnal. All have large eyes and superior night vision. Galagos are very active animals and move quickly through forests by leaping from branch to branch. Their body structure is lighter compared with those of lorises and pottos. Hindlimbs are noticeably longer than their forelimbs, and tails are long. In contrast, all limbs of lorises and pottos are of approximately equal length, and tails are short. Locomotion in these species is slow and deliberate. The first digits of both the forelimbs and the hindlimbs of prosimians are opposable to the remaining digits. The second digit of the hindlimb has a claw, which is used for grooming, and all other digits have nails as in other primates.


Among Malagasy prosimians, members of the Cheirogaleidae, Lepilemuridae, and Daubentoniidae are nocturnal as is the genus Avahi in the Indriidae family. The remaining species exhibit either diurnal or cathemeral activity patterns. All species have long tails, with the exception of Indri, which has a short rudimentary tail. With extremely well-developed hindlimbs, sifaka, Indri, Avahi, and Lepilemur are vertical clingers and leapers. The remaining lemur species move quadrapedally along tree limbs or leap from branch to branch.28


Although all prosimians are monogastric, the length of the intestinal tract as well as the size and conformation of the cecum and large bowel vary, depending on the species. In general, the more folivorous a species, the larger is the cecum and the more pronounced is the ability to use microbial fermentation to derive energy from fibrous diet items. In members of the Indriidae family, the proximal colon forms a spiral and is located in the right anterior quadrant of the abdomen adjacent to the body wall.17



Special Housing Requirements


Prosimians originate from tropical environments and may be maintained in outdoor enclosures year-round in mild climates. In temperate climates, enclosed environments with supplemental heat should be provided for diurnal lemurs when temperatures drop below 4.5° C to 7° C (40° F–45° F). Nocturnal prosimians are typically housed in indoor environments with temperatures controlled between 21° C to 27° C (70° F–80° F). Adequate shade should be provided in outdoor enclosures.


The size and design of enclosures for prosimians depends on the species, group size and social dynamics, and the reproductive status of individuals. Nocturnal prosimians are generally solitary in nature, although some may tolerate living with related individuals or a member of the opposite sex in captivity. Diurnal lemurs are social and should be housed with a compatible cage mate or social group. Flexible enclosure designs that allow physical separation of group members while maintaining visual contact are preferable, as individuals may require temporary separation for medical or behavioral management. Choosing flooring substrates and cage furniture materials that are sanitized or replaced easily is important for minimizing environmental pathogen loads. Branches and perches are added to maximize the use of vertical and horizontal space. For sifakas, adequate vertical structures are required to accommodate their vertical leaping form of locomotion. Enclosures for multimember groups should contain multiple feeding stations to prevent dominate animals from monopolizing food. The addition of visual barriers allows subordinate animals the option of moving out of sight of dominate individuals and decreases tension and fighting.


Nocturnal species are usually maintained under reversed light cycles for display and to allow husbandry staff to readily monitor behavior and activity. It is important to provide nest boxes or chambers for seclusion when desired. Aye-ayes should be provided with appropriate material to weave nests.



Special Physiology


Prosimians have a low basal metabolic rate compared with other mammals of similar body size.34 Behaviors such as basking and huddling are related to energy conservation and thermal regulation. Rectal temperatures of lemurs and bush babies range between 36° C to 37° C (97° F–99° F), with that of lorises somewhat lower between 35° C to 36° C (95° F–97° F).25,47 Dwarf lemurs (Cheirogaleus) and, to a lesser degree, mouse lemurs (Microcebus) undergo periods of torpor or hibernation during seasons of the year when food and water are scarce in their native environment. While in torpor, core body temperatures decrease and often match ambient temperatures for prolonged periods of time and metabolic rates slow dramatically. Body temperatures well below 27° C (80° F) are not uncommon in dwarf lemurs during torpor.9


Prosimians have no active mechanism for cooling, and temperature regulation is accomplished by limiting activity, seeking cool locations during hot weather, and licking hands to generate evaporative cooling. Capture and handling during warm weather should be done early when outdoor temperatures are cool or in temperature controlled environments.



Feeding


Feeding strategies in prosimians range from primarily insectivorous for some species of galagos to highly folivorous for members of the Indriidae family. Bamboo lemurs are highly specialized, and bamboo composes 90% to 95% of food consumed in the wild. The ability to successfully maintain many prosimian species in good health in captivity depends, in large part, on providing diets that closely resemble the gross composition of wild diets. The National Resource Council’s Nutrient Requirements of Nonhuman Primates contains a summary of differing prosimian feeding strategies.26 A notable exception between prosimian and anthropoid primates is the former’s ability to synthesize vitamin C endogenously.27


Many prosimians do well with diets composed of commercially prepared primate biscuits as a base. Folivorous lemurs such as sifakas and bamboo lemurs require high-fiber biscuits designed for leaf-eating primates, whereas the frugivorous ruffed lemurs are better adapted to biscuits designed for old-world monkeys with intermediate fiber levels. Ring-tailed, black, and brown lemurs do well on biscuits with either moderate or high levels of fiber.


Although useful for providing enrichment and variety in the diet, provision of commercially available fruits and vegetables should be limited as overconsumption contributes to dental disease, diarrhea, obesity, and diabetes. Cultivated fruits and vegetables contain high levels of sugar and starch and low levels of fiber compared with foods consumed in the wild. Domesticated fruits and starchy vegetables such as potatoes, corn, and grains, are high in simple sugars, and alter microbial populations in the hind gut and should be strictly limited or avoided altogether in the diet of folivorous lemurs. The addition of locally available fresh leaves and browse is essential for folivorous species, whereas including live insects or gums is important for species that have evolved to selectively feed on these items. A simple method to calculate the amount to feed a single animal is 25 grams per day (g/day) per animal of primate biscuit and 35 g/day per animal of fruit-and-vegetable mix per kilogram of ideal body weight.



Restraint and Handling


Because prosimians are relatively small, it is feasible to use manual restraint when performing brief examinations or minor treatments. Handlers should wear arm guards to protect themselves against scratches should an animal grasp the handler’s forearm. Physical restraint of prosimians weighing less than 1 kg involves initially grasping the animal over the back of the neck and around the mandible with a gloved hand to control the head while using a second hand to control the abdomen and back legs.


An animal weighing between 1 and 4 kg is first netted in its enclosure or out of a transport kennel. The head is controlled by placing one hand around the back of the neck with fingers extending around the jaw to secure the head. The second hand is then placed under the mandible to gain full control of the head and neck. The animal is then brought out of the net and allowed to grasp the handler’s arm with front and back limbs (Figure 36-1). If more control is needed, a second handler restrains the hindlimbs above the stifles to prevent injury to the knee joints and extends the legs, while the animal is positioned on either its back or abdomen (Figure 36-2). Squeeze cages may be used to restrain medium to large lemurs for the administration of intramuscular injections.





Chemical Restraint


Dosages of sedatives and immobilization agents are given in Table 36-2 and useful combination regimes in Table 36-3. When chemical restraint is needed to facilitate handling or performance of minor procedures, a range of options, spanning mild sedation to full immobilization, is available. Combining agents takes advantage of the synergistic effects of compounds having differing mechanisms of action.




Although ketamine is frequently used in a wide range of primates, it has a number of undesirable side effects in diurnal lemurs. When used alone, the degree and quality of immobilization is inconsistent, vomiting on induction or recovery is common, and seizures may occur even within normal dose ranges. The disadvantages are mitigated somewhat by combining ketamine with other agents; however, full recovery still requires several hours, which is a distinct disadvantage over other options.45



Anesthesia and Surgery


When general anesthesia is required, it is desirable to give pre-anesthetic medications whenever possible, as this provides a smoother induction and more stable plane of anesthesia while decreasing the amount of other agents needed to maintain a surgical plane of anesthesia. Isoflurane and sevoflurane are suitable inhalation agents for inducing and maintaining general anesthesia in pro­simians. When inducing animals in a chamber or via a mask, sevoflurane is the preferred agent, as it is less irritating to airways, making induction smoother and less objectionable to the patient.


Intubation may be challenging in aye-ayes (Daubentonia), sifakas (Propithecus), and ring-tailed lemurs (Lemur catta) because of the limited visibility of the larynx or the narrow openings between the vocal folds. Intubation is most easily performed in these species by inserting a guide cannula into the trachea and then passing the endotracheal tube over the cannula into proper position. Five-French (5-Fr) polypropylene suction catheters make good guide catheters (Figure 36-3). Once the endotracheal tube is in place the cannula is removed.



Lemurs are highly sensitive to the hypotensive effects of both isoflurane and sevoflurane, so it is important to monitor blood pressure and be prepared to administer intravenous fluids or other supportive measures as necessary when using these agents. Because of their high ratios of surface area to body mass, lemurs develop hypothermia quickly when anesthetized. Heat loss may be minimized by insulating the animals from cold surfaces, providing supplemental sources of warmth, and warming the surgical skin preparation solutions and fluids used for lavage and intravenous administration.



Diagnostics


Performing a complete physical examination and laboratory evaluation are critical for determining the health status of prosimians as in other taxa. Several sites are accessible for collecting blood samples. The femoral vein or artery in the region of the femoral triangle is the easiest site from where samples can be obtained in most prosimians. The main disadvantage with the site is an increased risk of serious bleeding following collection if the phlebotomist inadvertently hits the artery instead of the vein and adequate attention is not paid to hemostasis. This is particularly true for animals that are manually restrained, as blood pressure may be increased secondary to stress associated with handling. The posterior tibial vein, or small saphenous vein, running up the posterior aspect of the hindlimb, is an ideal site for intravenous injections and indwelling catheter placement (Figure 36-4); however, like the cephalic vein, it tends to collapse easily, making it suitable for collecting only small amounts of blood (typically < 1 milliliter [mL]). Jugular veins may be used for blood collection and catheter placement in anesthetized prosimians; however, the short neck length makes this site less desirable.



Hematology and common serum biochemistry reference values for various species of captive prosimians are provided in Tables 36-4 and 36-5, respectively. Urine is collected by using standard techniques. Cystocentesis and manual bladder compression are easily performed under manual or chemical restraint. Urethral catheterization is straightforward in males but is somewhat more complicated in females, as the position of the urethral orifice varies, depending on the species. In all members of the Lorisidae, the orifice is at the tip of the clitoris, whereas in lemurs, it is located in different positions between the vagina and the base of the clitoris. Urine specific gravity in healthy lemurs is frequently isosthenuric and not cause for alarm unless other abnormalities are identified on laboratory workup.



TABLE 36-4


Reference Values for Hematologic Parameters for Selected Prosimians Species*












































































































































Parameter Pygmy Slow Loris Greater Bush Baby Ring-Tailed Lemur Black Lemur Ruffed Lemur Aye-Aye Coquerel’s Sifaka
WBC (×103/µL) 13.1 ± 7.5 10.9 ± 5.5 8.63 ± 3.84 8.97 ± 3.58 7.75 ± 3.28 11.91 ± 4.18 7.3 ± 3.0
RBC (×106/µL) 5.7 ± 1.3 8.38 ± 1.26 7.63 ± 0.92 8.42 ± 1.29 9.29 ± 1.12 7.2 ± 0.65 8.26 ± 1.34
HCT (%) 42.4 ± 6.3 46.8 ± 5.4 50.4 ± 6.3 47.3 ± 7.0 49.6 ± 5.9 47 ± 5 41.6 ± 7.2
Hemoglobin (g/dL) 14.5 ± 3.0 15.8 ± 2.0 15.5 ± 1.7 15.1 ± 2.2 15.8 ± 1.9 16.0 ± 1.3 13.8 ± 2.3
MCV (fL) 75.1 ± 13.8 55.1 ± 4.8 65.8 ± 6.4 56.8 ± 6.0 53.5 ± 4.6 66.3 ± 3.7 50.6 ± 3.3
MCH (pg/cell) 26.1 ± 3.0 18.6 ± 1.6 20.3 ± 1.6 17.9 ± 1.4 17.1 ± 1.0 22.2 ± 1.1 16.8 ± 1.1
MCHC (g/dL) 35.0 ± 5.3 34.0 ± 1.5 31.1 ± 2.3 32.1 ± 2.6 32.2 ± 2.6 33.6 ± 1.7 33.2 ± 1.8
Platelets (×103/µL) 341 ± 100 300 ± 153 270 ± 109 205 ± 132 351 ± 149 346 ± 78 377 ± 100
Neutrophils (×103/µL) 3.12 ± 2.20 4.02 ± 4.31 4.34 ± 3.13 4.60 ± 2.33 3.96 ± 1.97 4.36 ± 2.29 4.51 ± 2.44
Bands (×103/µL) 0.3 ± 0.4 0.53 ± 0 0.18 ± 0.18 0.33 ± 0.57 0.27 ± 0.73 0 ± 0 0 ± 0
Lymphocytes (×103/µL) 8.51 ± 4.63 5.31 ± 3.12 3.73 ± 1.99 3.76 ± 2.36 3.18 ± 1.93 6.75 ± 3.45 2.42 ± 1.21
Eosinophils (×103/µL) 0.42 ± 0.39 0.53 ± 0.48 0.35 ± 0.36 0.48 ± 0.5 0.33 ± 0.36 0.14 ± 0.21 0.05 ± 0.07
Monocytes (×103/µL) 0.66 ± 0.80 0.44 ± 0.37 0.37 ± 0.41 0.3 ± 0.21 0.28 ± 0.24 0.56 ± 0.43 0.28 ± 0.22
Basophils (×103/µL) 0.21 ± 0.17 0.08 ± 0.02 0.05 ± 0.06 0.1 ± 0.09 0.05 ± 0.05 0.02 ± 0.05 0.02 ± 0.04

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Aug 27, 2016 | Posted by in EXOTIC, WILD, ZOO | Comments Off on Prosimians
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