Preamble - AZA Bat Taxon Advisory Group
Standardized Guidelines for Fruit and Nectar Bat Care
List of Common and Scientific Names , Conservation Status, and numbers of Fruit Bats held in North American Institutions, recorded in ISIS as of Jan 27,2006
Family - Pteropodidae
Scientific Name Common Name USFWS/CITES # Held in N.America
Cynopterus brachyotis Dog-faced fruit bat 19.25.0
Eidolon helvum Straw-colored fruit bat 220.197.18
Epomophorus wahlbergi Wahlberg’s epauletted bat 0.3.0
Pteropus conspicillatus Spectacled flying fox 0.1.0
Pteropus giganteus Indian fruit bat / II 59.66.8
Pteropus hypomelanus Island fruit bat / II 30.63.1
Pteropus poliocephalus Gray-headed flying fox / II 15.19.0
Pteropus pumilus Little golden-mantled fruit bat / II 22.23.0
Pteropus rodricensis Rodrigues fruit bat E / II 137.109.2
Pteropus vampyrus Large fruit bat / II 64.52.0
Pteropus voeltzkowi Pemba fruit bat / II 0.3.0
Rousettus aegyptiacus Egyptian fruit bat 146.156.21; 131 group
Rousettus lanosus Ruwenzori long-haired fruit bat 69.65.5
Family - Phyllostomatidae
Scientific Name Common Name USFWS/CITES # Held in N.America
Anoura geoffroyi Geoffroy’s tailless bat 1.4.0
Glossophaga soricina Long-tongued bat 402 group
Carollia perspicillata Short-tailed fruit bat 57.206.32; 3433 group
Artibeus jamaicensis Jamaican fruit bat 91.102.58; 1647 group
Artibeus lituratus Great Trinidadian fruit bat 2.0.0
Leptonycteris curasoae Southern Long-nosed bat 3.8.1
Abiotic Environmental Variables (address both exhibit and off-exhibit holding)
2 Temperature:
Fruit bats originate from tropical areas and do not tolerate low temperatures for extended periods.1 Although researchers disagree on the optimal temperature in which to house bats, laboratory studies have found that tropical bats do best in temperatures ranging between 70 and 90 degrees Fahrenheit (21-32˚C). According to Wilson (1988), Rasweiler (1975), and Barnard (1991), the ideal temperature is 80 degrees Fahrenheit (27˚C). Bats do best when a constant temperature is maintained.
In outdoor enclosures, supplemental heat is needed for temperatures below 70 degrees Fahrenheit (24˚C) and, in regions where temperatures fall below 50 degrees Fahrenheit (10˚C) for prolonged periods, indoor enclosures are necessary. If heat lamps or brood-rite heaters are used they should be properly shielded from bats so that the animals cannot burn themselves or chew through wires. In addition, we recommend creating multiple paths to heat sources to reduce aggression between bats.
Shaded areas must always be provided in outdoor enclosures (e.g., by use of vegetation, plywood structures, etc.). Shelter from rain & wind is also required.
1. Humidity: There are few data available regarding the proper humidity for bats. Bats appear to do well at relative humidities of 60-90 percent (Rasweiler, 1975; Wilson, 1988). Barnard suggests a relative humidity of 55 – 65% since high humidities can promote the growth of potential pathogens. Low humidity appears to be a problem for some species. To maintain proper humidity, we recommend using mister hoses when temperatures go above 85 degrees (29˚C). Symptoms of low humidity include dry skin or wing membranes and/or cracked nails.
2. Illumination:
1.3.1 Identify light intensity, spectral, and duration requirements.
Because there are few scientific studies describing circadian rhythms of bats, lighting is probably best when it imitates natural photoperiods (Wilson, 1988; Rasweiler, 1975). Fruit bats do well on a 10/12 to 12/10 light/dark cycle (Wilson, 1988; MacNamara et al., 1980), and should never be kept in 24 hour darkness or light.
1.3.2 Address the impact of and need for daily changes in light intensity and seasonal changes in light intensity and duration.
Fruit bats do not need to be kept in a nocturnal exhibit. Many species are diurnal or crepuscular and therefore active during the day. However, many species, especially nectar-feeding bats, are more active at night and managers may prefer reversing the light cycle. Reverse red or blue lighting is acceptable for use for display purposes, as are incandescent or florescent lights (House and Doherty, 1975). If a reversed cycle is used, halogen lights, fluorescent tubes, and blue filters make up a good lighting system. The day cycle lights are fluorescent and the nocturnal lights are halogen with blue filters. Blue light can be used (rather than red) because it simulates the color and intensity of moonlight and does not change the color of the bats. We strongly recommend using a dim/anti-dim cycle to reduce the shock of immediate bright light or complete darkness. During the fruit bat "day" cycle, shaded or darkened areas for roosting should be provided. Access to full sunlight is beneficial for Pteropus and Eidolon. Fruit bats can see most colors of light, including red.
4. Space
1.4.1. Identify what behaviors should be expected based on the behavioral repertoire observed in the wild, which of these behaviors animals of a given size should be able to exhibit within the enclosure/exhibit and how these behaviors influence the size and configuration of enclosures. As appropriate address both horizontal and vertical space as well as the appropriate level of complexity within that space. Adequate space should be evaluated in terms of space that is useable for the taxon.
Fruit bats require ample space to perform normal maintenance behaviors and do best in enclosures large enough to permit free flight (Wilson, 1988). USDA requires that flying mammal species must be provided with sufficient unobstructed enclosure volume to enable movement by flying and sufficient roosting space to allow all individuals to rest simultaneously [AWA Section 13; 9 CFR, Part 3, Section 3.128]. Bats that are unable to fly for a month or more may have muscle atrophy and lose the ability to fly (Wilson, 1988).
Bats maintained for exhibition purposes should be housed in enclosures that promote flight and roosting and allow for a broad spectrum of behaviors such as wing displays, grooming, foraging, and social interactions Enclosures should be eight times the wing span long and four times the wing span wide. .For example, an enclosure housing Island flying foxes (Pteropus hypomelanus), a species with wing spans reaching 3.5 feet (1.07 m), should be at least 28 feet (8.5 meters) long in order to encourage flight. Rectangular, octagonal, doughnut, circular or u-shaped enclosures facilitate sustained flight better than square enclosures, but they are all suitable for fruit bats.
Bats appear to be more comfortable in enclosures above human eye level, and will usually move to the highest point in an exhibit. However, if an enclosure is too high, capturing the bats for veterinary or husbandry purposes may be hindered. Generally, a cage height of six to seven feet (1.83 to 2.13 meters) will suffice for most species. Larger bats, such as the pteropids, could be housed in taller exhibits. In addition, greater space is needed for larger colonies. In free flight enclosures or exhibits where high ceilings make hand capture difficult, it is beneficial to have adjacent holding cages for management purposes.
The following space guidelines give details on the number of bats that can be housed in a space based on wing span and a normal body weight range for the species:
1. Giant bats with a wingspread from 3.5 - 5 feet (800 – 1500 grams)
a. For up to 6 animals, an enclosure 15 feet by 30 feet, 6 feet high or the equivalent area as long as the minimum width is 2.5 times the largest wingspan. For each additional animal, increase the enclosure size by 15 percent of the original floor area.
2. Large bats with a wingspread from 2.5 – 3.5 feet (300 – 800 grams)
a. For up to 6 animals, an enclosure 11 feet by 21 feet, 6 feet high or the equivalent area as long as the minimum width is 2.5 times the largest wingspan. For each additional animal, increase the enclosure size by 20 percent of the original floor area.
3. Intermediate bats with a wingspread from 2 – 2.5 feet (200 - 350 grams)
a. For up to 6 animals, an enclosure 8 feet by 15 feet, 6 feet high or the equivalent area as long as the minimum width is 2.5 times the largest wingspan. For each additional animal, increase the enclosure size by 20 percent of the original floor area.
4. Medium bats with a wingspread from 1.5 - 2 feet (80 - 200 grams)
a. For up to 10 animals, an enclosure 6 feet by 12 feet, 6 feet high or the equivalent area as long as the minimum width is 2.5 times the largest wingspan. For each additional animal, increase the enclosure size by 15 percent of the original floor area.
5. Small bats with a wingspread less than 1.25 feet (< 80 grams)
a. For up to 10 animals, an enclosure 4 feet by 7.5 feet, 6 feet high or the equivalent area as long as the minimum width is 2.5 times the largest wingspan. For each additional animal, increase the enclosure size by 15 percent of the original floor area.
All bat enclosures shall be large enough to permit aerial maneuvering within the enclosure. The width of the unobstructed flight area shall be no less than two times the wingspread of the largest bat in the enclosure, which is the approximate turning radius of the bat to allow for circular flight in the exhibit. For mixed bat species exhibits the space for each species is proportional to the number of bats in that size range and summing the space requirements for each group.
In the course of colony management, medical care may necessitate the use of non-flight cages for bats with fractures or other health problems. A minimal acceptable enclosure height should be no less than one and a half times the bats' body length to avoid contact with fecal matter and spoiled food. The minimal acceptable length and width should be no less than one and a half times the wing span to accommodate wing stretching and static flight behaviors (see Appendix B, Ethogram, for definition of behaviors). Permanent non-flight cages may be necessary for non-flighted bats with health problems that could damage themselves by having too much space.
2. For social species indicate minimum inter-individual distances that must be maintained and that will influence size of space. As appropriate address need for temporary isolation from conspecifics.
Fruit bats vary from being very colonial with roost mates touching each other in the roost as is the case with Egyptian fruit bats (Rousettus aegyptiacus) to more solitary species such as the Little golden-mantled flying fox (Pteropus pumilus), which roosts in small dispersed groups. Inter-individual roosting distances will also vary based on sex, with males requiring more space and females roosting much closer together. Larger fruit bats and flying foxes that are over 200 grams should have a minimum inter-individual distance of one half wing span from roost mates in the roost.
Colonial species of fruit bats may have to be isolated from conspecifics for medical reasons. This separation can be stressful, and where possible this should be avoided. Isolating two bats instead of a single individual will allow for social interaction. Social interaction can also be increased by placing isolated individuals in a howdy cage adjacent to their colony. As an isolated individual improves they may also be placed in their normal enclosure during the day for socialization, but isolated at night to monitor food consumption.
3. Identify appropriate furnishings to accommodate an array of locomotory and foraging behaviors as well as resting and sleeping.
Each enclosure should have perching areas for tree roosting species with natural sunlight or full spectrum lighting whereas crevice or cave-dwelling bat species will require dark areas or night boxes. Each enclosure should allow all bats to roost simultaneously and to seek shelter from the elements. They should also have climbing apparatus to facilitate exercise and landing after flight.
Vinyl coated wire hung on the ceiling provides toeholds for bats. We particularly recommend using 1” x 1” coated wire for larger species and 0.5” x 1” for smaller species, as it mimics the network of branches that bats use for a variety of behaviors including breeding, grooming, displaying, seeking food, roosting, and fleeing from aggressive encounters. Wire ceilings also promote wing walking by the bats and increases activity in the exhibit. Bats can be excluded from selected areas (e.g., over water or food dishes) by adding Plexiglas over the wire to prevent roosting. Endurance net is soft alternate for hard wire for species that may abrade their wing tips on the less flexible material.
Rough, naturalistic branches and vines should be provided as perches to help keep bats' nails from overgrowing. However, there should be no points or sharp edges that could puncture wings. Perches will need to be replaced occasionally; therefore, points of attachment should be designed into the exhibit. Roosting areas such as perches, branches, or boxes should be positioned far enough apart that animals can space themselves out during stress or flight (MacNamara et al,1980). Vines, heavy ropes, or crawl ladders (e.g., wire "ladders" attached to wall) should extend to the ground, especially if the exhibit contains solid or glass side walls. This will aid bats who are trying to move from the floor to ceiling roosting areas, as bats can exhaust and injure themselves attempting to fly up to their roost. Narrow gaps (e.g., one-half centimeter) between pieces of furniture should be avoided because bats can get wings wedged in the gap.
Darkened roost boxes or other visual barriers are recommended to provide animals with an avenue of escape from stressful situations, especially if aggression among individuals is observed (Rasweiler, 1975). Consideration should be given to providing feeding stations accessible from wire walls, vines, or perches; or, with sufficient clearance to allow bats to fly to and away from them.
Nectar feeding bats like to roost in either the open, from the top of the cage, or in roost boxes. Therefore, the top of the enclosure should be mesh and a roost box or two should be provided. Roost boxes should be large enough for all bats to comfortably use and spread out. The construction of roost boxes is important. They should be constructed of nontreated wood. The inside of the front, the top and all four sides should be lined with polyethylene mesh or grooved. The mesh or grooves provide an area for the bats to easily grasp and roost comfortably. It is also necessary to have a long landing platform, which should also be meshed or grooved. No light should be able to penetrate into the roost box. Two roost boxes (35 cm L x 21 cm W x 31 cm H with a landing platform of 12 cm) are suggested for a colony of thirty-three bats. It's necessary for cave-dwelling species such as the Long-tongued bats (Glosophaga sorcina) to have a dark place to retreat.
4. Address the need for and appropriateness of visual, acoustic, and olfactory barriers within the space. Consider options for minimizing “white noise” from systems and the surrounding environment
Animals housed indoors should be protected as far as possible from disturbance by the visiting public. Noise from environmental systems should be kept at a reasonable level. Fruit bats should always be provided with an area in their exhibit where they can retreat and feel safe when disturbed by loud noise, bright lights or any other sudden disturbance.
5. Identify appropriate substrates and nesting/bedding materials if required.
As bats may occasionally descend to the ground, non-abrasive flooring should be used. Natural substrates such as soil, grass, or mulch can be used with low densities of bats. We do not recommend the use of sand or saw dust, as bats may ingest it. Flooring material should be easy to clean and floors should have good drainage. Epoxy-based paints are useful in sealing cement walls and floors.
6. Address mechanisms for the provision of change and variation in the environment.
As with most mammals, exhibit “furniture” should be changed periodically, but not all at the same time. These changes can include cleaning and repositioning of ropes, vines and visual barriers. Environmental enrichment can also be a source of change and variation, and is important for fruit bats. There are several enrichment options such as offering browse, giving the bats olfactory and acoustic stimulation, or adding new props or visual barriers to the enclosure (Atkinson, 1993; LeBlanc, 1999). Refer to Appendix E for a list of forages accepted by captive colonies of fruit bats.
7. Address issues, such as scent marking, that may influence how and how often space is cleaned.
Fruit bats use scent-marking to communicate (Dapson et al., 1977; Gustin and McCracken, 1987; Quay, 1970; Scully et al., 2000), and they will scent mark their enclosure. Frequent disinfection that removes all these scent marks may cause distress or aggression. Basic sanitation procedures should be completed on a daily basis, such as sanitizing the food and water bowls, and removing the food waste and fecal contamination in the enclosure. Appropriate design and building materials for cages will greatly facilitate cleaning and sanitation (see Sections 1.4.9). Raised, wire-floor cages allow feces and contaminated food to fall away from the animals and can facilitate cleaning. Stainless steel dishes are preferable to those made from other materials (e.g. plastic) because stainless steel disinfects well, and is less likely to be broken or scratched.
When disinfectants are used to clean dishes or exhibits, it is critical to rinse them well, as disinfectants may be toxic to bats (Wilson, 1988). Appropriate disinfectants include diluted Clorox (1:30 dilution) or quartenary ammonium compounds, although the latter does not kill certain strains of pseudomonas. Ensure that all organic material is removed before applying disinfectants. Allow adequate contact time (> 15 minutes), scrub in disinfectant well, then rinse thoroughly. Do not expose bats to noxious vapors in enclosed, poorly ventilated areas or allow bats to have contact with disinfectants.
Pest Control
A good pest control program should be in place and be maintained and monitored continuously.
The best control is to exclude pests. Cleanliness in and near bat enclosures is of the utmost importance. Be sure the area around bat enclosures is free of places that harbor pests. Seal all cracks and holes into the exhibit. Glue boards and snap traps can be used but must be shielded from bats. Cockroaches are commonly found in and around fruit bat exhibits. Several methods for controlling cockroach populations are available. Pyrethrin-based insecticides and diatomaceous earth can be used with care. Narrow-mouthed beer or soda bottles partially filled with fruit juices can be used as traps. Tracking powder (e.g., Sevin Dust) has been used by some institutions to control ants. However, we do not recommend it because bats will frequently descend to the floor of the exhibit and can be adversely affected by the dust.2 Snakes can be a problem for small bats, especially in outdoor exhibits. Wire with small openings (e.g., one inch by one-half inch) will exclude most, but not all, snake species. For outdoor exhibits where snakes may present a problem, additional barriers may be needed.
There are no special concerns or requirements for sewage disposal; however, requirements can vary by region and managers should be aware of local regulations.
1.4.8 Identify number of air or water changes/hour required
A highly efficient ventilation system is necessary to avoid the buildup of unpleasant odors, especially in enclosures housing large colonies. A suggested rate of air change for larger colonies is six to ten exchanges per hour with 25% fresh air. Because of the bacteriological breakdown of bat guano, it is important that air leaving bat exhibits, especially that from large colonies, be vented outside and not re-circulated or ducted into a public area (Wilson, 1988).
1.4.9 Identify necessary measures for safety and containment.
In general, enclosure surfaces should be smooth and non-porous, and all surfaces with which bats will come into direct contact should be non-abrasive. Wall and floor surfaces must be able to withstand a great deal of hosing and should be appropriately sealed. Galvanized steel cages and wire should be avoided because bat urine corrodes tinned surfaces and may cause zinc toxicity if ingested (Wilson, 1988). Therefore, if an enclosure contains wire, we recommend using vinyl coated, Teflon sprayed, or non-galvanized wire3. Polyethylene mesh and polypropylene knitted netting (Endurance® netting)4 are also excellent caging material (Barnard, 2006). The size of the openings in wire or mesh should be small enough to prevent animals from pushing a wing, wrist or foot through it, but not so fine that animals' claws get stuck in the mesh (Wilson, 1988).
Enclosures with glass fronts present no special problems, although it may be necessary to tape or soap the windows for a few days after animals are newly introduced to alert animals to the presence of the glass. Piano wire has been used as a public barrier on some fruit bat exhibits, with plastic coated wire being the easiest to clean. The disadvantages of piano wire include bats getting caught in wire, especially when they are new to the exhibit, and urine and fecal material passing through to the public viewing area. To minimize the second problem, place roosts at the two ends of the exhibit, on sides adjacent to piano wire front. The bats will fly back and forth between the roosts (in front of the viewing public) and, because bats tend to defecate while turning at the ends of the exhibit, the amount of fecal material that is passed through the piano wire front will be minimized.
For exhibits that are constructed as "bat caves” (e.g., the shot Crete wet mix design), the vault must be semi-rough to facilitate roosting. Also, it is important to create many small concave pockets in the vault to offer multiple territories and visual barriers favorable to the establishment of a social structure such as harems. Finally, the vault must be uneven and characterized by many elevation levels to simulate a natural environment.
For outdoor exhibits, use of a double enclosure will reduce the possibility of escape. This is mandated by the Lacey Act for Pteropus species. The second enclosure should be more than two inches from the first enclosure to minimize the risk of a bat's foot reaching through the first enclosure and getting entangled with the second. Use small wire openings (one-half inch by one half inch) or a Plexiglass barrier for pest control (see Section 1.4.7). Thin wire (e.g., chicken wire) should be avoided as it may damage feet, especially with heavier bats (e.g., larger Pteropids).
1.4.10 Address issue of transport, identifying (in accordance with IATA)
Most bats can be shipped communally. Mothers with nursing infants should not be shipped. Some international shipments may require use of a lift-out internal cage so that bedding and fruit can be destroyed at the port of entry. Crates should be designed so that there is no leakage (e.g. of urine or feces) from the crate during shipment. Check with customs before shipping and prepare the crates prior to shipment.
Zoos must follow IATA standards for all importations. Once within the United States, IATA standards are still recommended by the Center for Disease Control (CDC), the United States Department of Agriculture (USDA) Animal and Plant Health Inspection Service (APHIS), and United States Department of Interior (USDI). However, the "secondary enclosure" technique, described under Megabats, below, will be permitted (CDC and USDI, pers. comm.). Check with appropriate agencies prior to shipment.
United States Regulations: A Centers for Disease Control (CDC) permit is required to import fruit bats into the United States and to ship bats between states5. (See Appendix E for copy of permit). In 1995, CDC developed more stringent guidelines, so be sure to check with them prior to shipping bats.
Canadian Regulations:
a) Shipments from the United States. There are no restrictions for bats being imported from the United States; however, shipments require a health certificate and permission from the Canadian Department of Interior.
b) Other foreign importation. According to Section Ten of the Animal Health Regulations, administered by Agriculture Canada, an import permit must be issued by the Animal Health Division of the Food Production and Inspection Branch of Agriculture Canada prior to importation. To receive the permit, an application form must be completed by the importer and submitted to the appropriate regional office. Upon their arrival in Canada, the bats will be confined for a thirty day quarantine period in a previously approved area. If there is no health problem after this period, the quarantine will be ended. Appendix D contains a copy of the import permit application form (AGR 1551).
The introduction provides a table of bat species listed as endangered by the United States Fish and Wildlife Service and CITES that can be referenced for shipping information.
1.4.10.1 Type of transport container:
The containers shown in Appendix C meet the requirements of the International Air Transport Association (IATA). They are strong enough to withstand the rigors of air transport, and they include appropriately constructed inner and outer components.
1. Megabats. Pteropus species must be transported in double cages. A vari-kennel with an internal wire cage works well. Line the vented sides and the door with a breathable, opague material like shade cloth or cheese cloth. This provides the bats with some privacy but still allows for air flow. Care should be taken that there are no frayed edges in the material used for privacy with which the bats could become entangled. Crates should be large enough so that when bats are hanging their faces do not reach the floor.
2. Microbats.6 Microbats such as Glossophaga soricina, Carollia perspicillata, and Artibeus jamaicensis can be transported in quart-sized cardboard cartons. These containers, which can be purchased from paper goods companies, measure about four and one-quarter inches (10.8 cm) in diameter at the top, three and one-half inches (8.9 cm) in diameter at the bottom, and are six inches high. They should be moisture-resistant and have slip-on lids. To give the bats something to hang on to, line the interior by stapling in one-eighth inch (3.2 mm) square mesh plastic aquaculture Netting. Punch air holes in the sides with a cork borer. Up to three Carollia sized bats can fit in one carton. Fourteen of these cardboard cartons can be placed inside a screen-lined cardboard mouse shipping cage (with the partitions removed). For extra protection, the mouse cages can be placed inside a strong protective container constructed of one inch (2.5 cm) square, hollow aluminum tubing that is lined on the sides with one-quarter inch (6.2 mm) galvanized wire mesh and has a plywood roof and floor.
1.4.10.2 Appropriate size of transport container
See 1.4.10.1and Appendix C
1.4.10.3 Provision of food and water during transport
The bats should have access to food prior to shipment and it should not remain in the containers for more than 15 hours.
1.4.10.4 Provision of bedding or substrate in transport container
Avoid using aromatic substrates such as pine bark or cedar chips because these materials may cause respiratory distress to the occupants. Kraft paper (50 lb) can be used to line the transport container.
1.4.10.5 Mechanism(s) for separating animal from urine and feces during transport
Some international shipments may require use of a lift-out internal cage so that bedding and fruit can be destroyed at the port of entry. Crates should be designed so that there is no leakage (e.g. of urine or feces) from the crate during shipment.
1.4.10.6 Identify appropriate temperature range during transport
Bats should be shipped when environmental temperatures correspond to a given species’ thermal requirement. Although some airlines will allow animal shipments when temperatures range between 7.2º C and 29.4º C (45º F - 85º F) , regardless of the season, others find it easier to refuse shipments during summer and winter months. When temperatures are close to the allowable limits, it may be necessary to include heating or cooling packs (e.g., Hot Rod( warm packs or Uline( cold packs) within a transport container.
When transporting bats by automobile during hot weather, NEVER leave them in a parked car during rest stops unless the air conditioner is running. When transporting tropical species in winter, the heater should be left on. Many animals have died in vehicles during transport because simple precautions were not taken.
1.4.10.7 Consider appropriate light levels and how to minimize noise during transport.
The appropriate transport container for shipping bats will have low light and minimize outside noise. The mesh sides and door of a Vari-kennel transport container should be covered with a breathable, opaque material to allow for ventilation, to reduce light levels in the container and to give the bats privacy.
When fruit bats are shipped, a polite request to the airline staff to place live animals in locations where loud noises are at a minimum and away from any other live animal shipments in the cargo hold is advised.
1.4.10.8 Address appropriate group size or need for separation of individuals during transport
Most bats can be shipped communally. Mothers with nursing infants should not be shipped.
When a group of bats of the same species is being shipped, the sexes should be separated. In some cases, juveniles may have to be separated from adults. When transporting more than one species at the same time, a separate container should be available for each species. Up to five adult Rodrigues fruit bats (Pteropus rodricensis) can be shipped in an intermediate vari-kennel (0.8 m x 0.56 m x 0.58 m), if the group is compatible. Three Large flying foxes (Pteropus vampyrus) can be shipped in a large vari-kennel (0.91 m x 0.62 m x 0.66 m).
1.4.10.9 Consider need for handler/veterinarian access to animal during transport
Transport periods that are greater than 15 hours in length should be accompanied with food and water instructions. In these cases it may be necessary to make arrangements with a zoological facility close to the lay-over points prior to shipping for food and water provisions. A contact number for the closest zoological facility should be provided and after 15 hours the animals should be checked on by trained professionals. If needed, food and water should be provided.
1.4.10.10 Consider maximum duration of transport allowable before temporary transfer to “normal housing” is required.
Bats should not remain in the containers for more than 24 hours.
1.4.10.11 Address appropriate timing of release, size and type of enclosure at transport destination
Follow quarantine guidelines as required (see Section 3.2.1) and reintroduction guidelines (see Section 5.3). Shipping crate should be placed directly into the quarantine space and the animals allowed to exit on their own volition and at their own pace.
5. Water
1. For aquatic or semi-aquatic organisms identify acceptable water quality parameters (pH, turbidity, salts, turnover rates, filtration, disinfection, bacterial count, acceptable chemical residuals, etc).
2. For terrestrial and semi-aquatic organisms address appropriate means of presentation of water, and appropriate placement of water sources, acceptable bacterial levels, mineral levels, temperature as appropriate
3. Address issues of depth and need for variation in depth and/or current
Water sources should be checked for chemical residues, bacterial counts, mineral levels and salts. Because water requirements are unknown for bats (Racey, 1970), water should be offered at all times, even though some species (e.g., nectar-feeding bats) may rarely be seen drinking. Some naturalistic bat exhibits have running sources of water such as waterfalls and pools. This kind of water source is greatly used by Microchiropteran bats that glide over the water surface for a drink. Care should be taken that fecal material and discarded pieces of food do not accumulate in these areas, and the water source should be shallow enough to allow animals an easy method of removing themselves from these features. Misters provide opportunities for bats that are kept in outdoor exhibits to cool off if the temperature goes over 29.4 °C (85 °F).
1. Biotic Variables
1. Food and Water
1. Identify appropriate containers and protocols for the provision of food and water
Standard glass, plastic, or ceramic bowls should be used for food and water bowls. Several sources of water (e.g., bowls, pools, mister hoses, etc.) should be provided and water should be changed daily. Large colonies and exhibits housing mixed bat species or aggressive animals will need a greater number of water sources. Some of the larger fruit bat species are capable of learning to drink from watering devices fitted with tubes. These devices have the advantage of not becoming soiled by urine and feces. Some species or individuals may not be able to utilize these devices, so bat caregivers need to monitor the situation to verify that all bats are using them successfully. To minimize contamination of water sources by urine and feces, place water source beneath areas of smooth ceiling where bats cannot hang.
For nectarivorous bats, dietary presentation is almost as important as the diet itself. Nectar solution can be offered in a variety of hummingbird feeders. It is important to take into consideration when choosing a feeder whether or not it will be accommodating and easily used by the nectar-feeding bat. The feeder must not have bee guards or obstructions around the opening. The opening must also be as close as possible to the nectar itself to ensure that the bat will be able to reach the fluid with its tongue. The daily feeders used at OBC and Biodome are, respectively, the Little Beginner Hummingbird Feeders by Perky-Pet Products Co. (2201 South Wabash street, Denver, Co 80231. U.S.A.) and the Oriole Feeders by Opus Incorporated (P.O. Box 525, Bellingham, MA, 02019. U.S.A.). Open-topped feeders, such as a plate with an extension in the middle hung from the ceiling, are favorites among the bats.
Yet another form of presentation includes open shallow dishes placed in hanging baskets. More unique forms of presentation are a good source of daily enhancement but this should be done with extra nectar so that it is guaranteed that the entire population receives enough to eat each night. This can be done by using hummingbird feeders in the shape of artificial flowers placed in a pot. Drowning is an important factor to consider when contemplating various ideas of presenting food to smaller bats. To deter drowning, it is helpful to place a variety of marbles in the open dishes to allow an area for footing should an individual accidentally fall into the dish.
2. Identify appropriate foodstuffs (see below) and feeding schedules
One daily feeding is sufficient for most species. Large colonies, however, should be fed more frequently to ensure that all individuals will have access to food. Over feeding can cause obesity in the colony, and this must also be monitored.
For nectarivorous bats, the liquid diets have a tendency to sour or ferment when left out overnight especially in warm environments. The bats must be fed at the end of the light cycle to minimize fermentation of the food prior to feeding.
3. Address the provision of variability in food type and presentation (e.g. spatial and temporal dispersal of food resources)
Large fruit bat colonies may require twice a day feedings to ensure that all individuals will
have access to food. Captive fruit bats also require enrichment which can be offered to provide variability in food type such as browse and flowers in addition to novel fruit items. This enrichment can be presented so that bats have both a spatial and temporal dispersal of food resources in their enclosure.
For nectarivorous bats, the feeders and fruit skewers should placed as far apart as possible as well as in a different locations on a daily basis so that the bats are forced to actively forage as they would in nature. There has been some territorial behaviors observed so it's important to have the nectar and fruit as spread out as possible to ensure adequate consumption by each individual.
4. Address opportunities for animals to process food in ways similar to their wild counterparts, and consider mechanisms that enable animals to work for food
All fruit bat species should be given whole fruit or nectar and allowed to process food in ways similar to their wild counterparts as part of their enrichment program. Bats can also be challenged to fly to feeding areas and to utilize their wings and feet to obtained food resources such as Large flying foxes (Pteropus vampyrus) pulling up weighted plastic chain to reach novel food items (Sequin et. al. 2000).
2. Social Considerations
1. Group Composition, including as appropriate
1. Suggested age and sex structure of social group
All fruit bat species maintained in North America can be maintained in single sex groups. Male bachelor groups of fruit bats as with most mammals will have higher levels of aggression than single sex female groups. In single sex groups of any size or sex, there may be minor dominance struggles, especially among males. A common behavior that can be observed is male on male mounting as part of normal dominance behavior.
Bats that are part of an organized breeding program will require facilities to house multiple males, and the breeding group, This does not necessitate that every zoo must maintaining all three types of colonies (Male and female single sex groups and a breeding colony), but rather zoos should trade animals to coordinate breeding programs. A sex ratio of 1.6 or 2.10 is suggested, since problems with aggression can occur with maintaining too many males in a colony such as decreased reproduction and males pulling infants off dams. A sex ratio of 3.12 Long-tongued bat (Glossophaga soricina) is suggested for breeding with this nectar-feeding species.
Fruit bats are long lived in comparison to similar sized mammals, and breeding plans should focus on maintaining healthy populations with appropriate age pyramids. Elderly male fruit bats may have difficulty competing with younger males in single sex groups, and may have to be maintained is single sex groups with males of a similar age class.
2. temporary isolation of parturient females and young, or of males, and corresponding adequate and appropriate space for animals when removed
Some fruit bat species have a post-partum estrus, and reproduction will occur if the breeding males are not removed. Fruit bat species can breed even if they are housed in an enclosure that is too small for them to fly. Parturient females should be left in maternity colonies, and males should be returned to a bachelor group. Appropriate care must be taken in removing breeding males from the colony, so as not to stress pregnant females or dams with pups, which can cause abortions. Introductions of new bats into a maternity colony should also be avoided for two to three months, to allow for a close bond to form between the dam and pup, and to minimize aggressive encounters between newcomers and very young pups. If breeding males or parturient females have to be temporarily isolated, then follow the space guidelines in section 1.4.1.
3. Seasonal separation of sexes, or for those species that are truly solitary (=social interactions are primarily limited to courtship and care of dependent offspring), seasonal introduction of sexes
See Section 4, Reproduction, for more detailed information.
Wild bats are seasonal breeders, the timing of which is mostly species specific. However, seasonality decreases in captivity, especially in indoor enclosures. Seasonality will also differ in different climates.
Although male bats will attempt to copulate throughout the year (Martin et al., 1986), the highest copulation activity in bats is during the mating season. When not in season, females will avoid copulation and will generally fly away from interested males.
During their breeding season, males tend to become more territorial and aggressive. Many, if not most, fruit bats form harems. In some species, males will be seen hovering around a receptive female, showing interest by hooking the female with their thumbs. They will also "hook” another male with a thumb to try to dislodge them and thereby keep them away from the female. The colony hierarchy does not always hold for breeding, so do not assume that the dominant male is the sire. Also, multiple males will breed one female so paternity in multiple male groups can be difficult to ascertain.
Courtship in some of the larger bat species often involves male initiated allo-grooming, especially around the genital area, followed by much bickering and then mating. Females are generally resistant; they may fly to get away from an interested male. Females may choose with whom they mate; however, more research needs to be done in this area.
4. nursery groups (groups of mothers with most recent young)
Typically, parenting is done by the female. Allo-parenting is rare, but has been documented in dog-faced fruit bats (Cynopterus brachyotis), straw-colored fruit bats (Eidolon helvum) and Little-golden-mantled flying foxes (Pteropus pumilus). In the wild it is quite common to find maternity colonies of many bat species, and zoos could replicate this behavior by removing males after birth. Mothers carry and hold their infants in a variety of positions including front and back. They will also "park" the infants for various lengths of time, especially during weaning and parent feeding time (the length of time infants are parked appears to be species specific). Should the infant fall or get knocked down, mother bats will pick their infants off the floor. In one case, a female Large flying fox (P. vampyrus) at the Lubee Bat Conservancy had a pup that died overnight, and the dam would carry the dead pup in her wings, and attempt to get the pup to nurse by pushing the pup to the nipple until she lost her grip on the pup and it fell. This same dam vocalized for her pup over a twenty-four hour period, and would investigate other pups in the enclosure that made contact calls.
In large colonies of fruit bats or in crowded enclosures with other bat species, it has been noted that lone infants that get separated from their dams become vulnerable. In overcrowded situations, maternal neglect is not uncommon. Infanticide has been noted in fruit bat colonies, and while the causes are unknown, it does not appear to be directly related to overcrowding or an improper sex ratio (Carroll, 1988).
5. forced “emigration” of adolescents
In captivity, young male fruit bats must be removed before they reach sexually maturity. This date varies on the species maintained, but in general it is several months after weaning. For the larger fruit bats (e.g., Pteropus spp.) males may reach sexual maturity at twelve months while females may reach sexual maturity when they become two years of old. Smaller species are weaned and reach sexual maturity in less than six months. Be sure that juveniles are eating solid foods and drinking water before removing them from the dam. Mother-juvenile fights are common, especially during weaning, with the pup frequently trying to nurse its dam and then being rebuffed. Pups will form lasting bonds with other bats in their crèche, and it is important to keep them in these groups, especially when moving young males into older bachelor groups. Female pups can stay in the maternity colony longer, and only need to be removed just prior to introducing the breeding male for another round of breeding.
6. multigenerational groups (e.g. many primates, elephants)
Multigenerational single sex colonies may be formed in the wild such as male bachelor groups and female maternity groups in fruit bats. In captivity, they can be maintained in single sex groups.
7. groups deriving from cohorts (e.g., dolphin male pairs)
Young fruit bats that were creched together as pups may form long lasting bonds. Similar-sex bats can be moved to single sex groups as part of normal population management.
8. all male groups
All fruit bat species maintained in North America can be maintained in single sex groups. Male bachelor groups of fruit bats as with most mammals will have higher levels of aggression than single sex female groups. In single sex groups of any size or sex, there may be minor dominance struggles, especially among males. A common behavior that can be observed is male on male mounting as part of normal dominance behavior.
9. daily and life stage variation in patterns of social affiliation
Bat behavior is formed largely through observational learning. Young bats are generally poor flyers and will often crash into things as they learn how to fly. Static flying is common among infant and juvenile bats (Carroll, 1979). Pups are very playful, and their need for environmental enrichment is great (see Section 5.7). At weaning, a pup will first learn to eat solid food by licking its mother's lips as she is feeding. Up to a year of age, pups will return to their mother's nipple when they are frightened. Occasionally, a female will have an older pup on one nipple and a younger pup on the other. Hall and Richards (2000) suggested that adult male flying foxes also have a role in guiding weaned juveniles towards food resources in the wild.
2.2.2. Group Size, including
1. minimum and optimum group sizes
Because the majority of bat species are social, we recommend that no bats be maintained singly. The only exception to this recommendation is if an animal requires special medical care. The ideal number of individuals and sex ratio of bat colonies will be species specific and will depend largely on the size of the enclosure. If bat densities are too high or low, the resulting stress may lead to detrimental physiological and/or behavioral changes (Rasweiler, 1975). While managers should observe colonies for excessive fighting and potential injuries, squabbles among bats are common in the wild and in captivity and often result in harmless wing tears that heal quickly and are of little concern. (For more information on wing tears, see Section 3.2.2). To help avoid undue fighting among animals, be sure to place sufficient feeding and roosting stations in the enclosure (see Section 1.4.3 for additional information on avoiding aggression).
2. inter-individual distances required
2. Conspecific groups, consider the need for/influence of adjacent groups, or similar taxa, on territorial species
In general, bats do very well in mixed species exhibits, including housing bats with other bat species and bats with other taxa. The primary concern with maintaining multiple bat species is ensuring that the nutritional and spatial needs of each species are taken into consideration. Enclosure size, environment (e.g., most appropriate feeding time and light cycle), and species variability are important factors. It is also critical to offer enough food dishes of appropriate sizes to minimize competition. Ideally, mixed species exhibits would house multiple colonies rather than a colony of one species and one or two individuals of another (although this combination has worked well in some instances). The size of the bat species may be a factor; however, more information is needed. There are no documented cases of successful breeding between species in zoos, but in Australia, Grey-headed flying foxes (Pteropus poliocephalus) have been observed to hybridize with Black flying foxes (Pteropus alecto) in captivity (Luckoff pers. comm.).
3. Mixed species groups
1. identify appropriate species (consider relative size, diet, mode of defensive behavior, potential for hybridization, potential for disease transmission)
2. identify key environmental elements for each species
3. identify interspecific inter-animal distances required
4. address appropriateness of single-sexed groups
There is tremendous potential to increase the amount of space available to bats in zoos and make exhibits more exciting by maintaining bats with other taxa. There are several potential problems that should be taken into consideration before implementing a mixed taxa exhibit such as looking at disease issues that could cross species, a lack of adequate space, competition and aggression between species, and provision of enough food and a proper diet. An additional concern when housing bats with terrestrial omnivores and carnivores is that they may consume incapacitated bats that fallen to the ground. For more information on using bats in mixed species exhibits, see Riger, Bear-Hull and Harmon (2001).
Bats in the genus Pteropus are prone to henipaviruses, and should not be exhibited with primates, swine or hoofstock. Salmonella can also be a zoonotic disease threat with mixed species, and veterinarians should screen animals for disease issues prior to managers mixing different species. Managers should also avoid mixing bat species with species that require heavy bedding material that would be soiled by bat guano, and create a possible culture for Histoplasmosis. Bat species that are slated for possible reintroduction should also be excluded from mixed species exhibits to minimize the risk of transferring captive wildlife diseases to wild populations. The AZA Bat TAG suggests not mixing mega and microbat species, and to mix bat species based on region, such as Asian flying foxes or South American fruit bats.
Rodrigues fruit bats (Pteropus rodricensis) have been successfully exhibited with the following species, but it can be aggressive so any mixed species exhibits should be closely monitored:
Riverbanks Zoo – red billed hornbill Tockus erythrorhynchus
Brookfield Zoo – Prevost’s squirrel Callosciurus prevosti, giant Asian squirrel
Ratufa bicolor, small-clawed otter Ablonyx cinerea, boobook owl Ninox
novaeseelandiae, Matschie’s tree kangaroo Dendolagus matschiei, brush-tailed bettong Bettongia penicillata
Lubee Bat Conservancy - Pteropid bats: Pteropus pumilus, Pteropus hypomelanus, Pteropus vampyrus, Pteropus giganteus, Pteropus conspiculattus, and Petaurus breviceps.
Oregon Zoo – Straw colored fruit bat Eidolon helvum, Egyptian fruit bat
Rousettus aegyptiacus, Jamaican fruit bat Artibeus jamaicensis
Philadelphia Zoo – Rousettus aegyptiacus
Organization for Bat Conservation – Short tailed fruit bat Carollia perspicillata,
Jamaican fruit bat Artibeus jamaicensis, Straw colored fruit bat Eidolon helvum, Egyptian fruit bat Rousettus aegyptiacus, Ruwenzori fruit bat Rousettus lanosus
Disney’s Animal Kingdom – Victoria crowned pigeon Goura victoria, Jungle
fowl Gallus sp., Pteropus vampyrus
❖ Additional species not mentioned above: Malayan tapir Tapirus indicus, white-handed gibbon Hylobates lar, Brush-tailed porcupine Atherurus africanus, lesser bushbaby Galago senegalensis (Riger et al. 2001).
4. Introductions
Identify appropriate introduction techniques and strategies for conspecifics, and heterospecifics as appropriate
See section 5.3 for more information on introductions of conspecifics.
2.2.6. Human-animal interactions
1. identify acceptable forms of human/animal interaction keeping in mind that animals should not show fear or aggression during routine care, and interactions viewed by the public should not encourage public interactions with wild animals
All fruit bats will show stress when approached by a handler, and then try to escape. Stress levels are greater for animals housed in small enclosures that have no room to escape. (For additional information on the effects of stress see Widmaier and Kunz, 1993). When captured, most bats will immediately urinate and defecate and many will try to bite. Vocalizations may accompany any of these behaviors. Many large bat species will shiver and head bob when stressed. Long-term stress may cause anorexia. Some bats, especially the micro fruit bats (e. g., Glossophaga soricina), may go into stress-induced torpor. White-lines bats (Vampyrops helleri) and Long-tongues bats (Glossophaga soricina) will exhibit the following behaviors when food deprived: unfolding of the wings, no attempt to fly when approached or prodded, and no audible noises emitted (Rasweiler, 1973).
2. Address both animal and keeper safety
In most States, a bat that bites a human must be killed to test it for rabies. For this reason, we recommend that the public not have direct contact with bats. Only trained and qualified personnel should handle bats. In addition, all personnel who come into contact with bats should be immunized against rabies and have titers tested regularly. All bat bites should be reported to County public health officials, per state guidelines.
Bats potentially are vectors of zoonotic diseases that can be passed to humans (see Constantine, 1988). Consult your local health department for additional information on health issues with bats. Rabies and histoplasmosis are outlined in more detail below:
1. Rabies:
This virus manifests in itself in two forms: furious rabies and paralytic (or dumb rabies). Furious rabies is characterized by agitation, thrashing, biting, and viciousness. Paralytic rabies is characterized by apathy, depression, disorientation, and ends with coma and death by respiratory failure. The furious form is rarely found in bats, and "outbreaks" of rabies in bat colonies is extremely rare. Contrary to common belief (even by medical "experts"), bats are not asymptomatic carriers of rabies. The statistics for the percentage of bats that contract rabies varies depending on region and type of sampling technique used for testing. No matter what the region or species, certain precautions should be taken to protect animal handlers from contracting this disease.
a. All personnel working with bats should be vaccinated against rabies.
b. Personnel should have their rabies titers checked every one to two years and be vaccinated as necessary.
c. The potential for bites should be minimized by wearing gloves, having only trained personnel handle the animals, and by anesthetizing even for routine handling.
d. Establish a bite protocol, and record all bites, even if the skin is not broken.
e. Minimize the number of personnel in contact with the bats.
f. Greatest care must be taken with new, wild-caught imports.
2. Histoplasmosis: Histoplasmosis (Histoplasmosis capsulatum) is an airborne fungus that affects the lungs of mammals. It is contracted from breathing dust in enclosed areas such as caves or mines which contain infected bird or bat guano. The fungus occurs primarily in the Mississippi Basin of the United States, the tropics and subtropics.
The risk of catching histoplasmosis from a captive colony of bats is small because these colonies rarely reach the large numbers needed for the build-up of the fungus, and fecal material is removed on a regular basis (i.e., not allowed to accumulate).
3. Henipavirus: This virus genus in the family Paramyxoviridae, contains two members, Hendra virus (originally Equine morbillivirus, EMV) and Nipa hvirus. They are characterized by their natural occurrence in Pteropid fruit bats (flying foxes), and their recent emergence as zoonotic pathogens capable of causing illness and death in domestic animals and humans. Hendra virus was discovered in September 1994 when it caused the deaths of thirteen horses, and a trainer at a training complex in Hendra, a suburb of Brisbane in Queensland, Australia. A serosurvey of wildlife in the outbreak areas showed that pteropid fruit bats had a 47% seroprevalence for the virus. Virus isolations from the reproductive tract and urine of wild bats indicated that transmission to horses may have occurred via exposure to bat urine or birthing fluids (Halpin et al, 2000). Nipah virus was identified in 1999 when it caused an outbreak of neurological and respiratory disease on pig farms in peninsular Malaysia, resulting in 105 human deaths and the culling of one million pigs (Field et al., 2001). Flying foxes are unaffected by Hendra or Nipah virus infection. Bats in the genus Pteropus should not be mixed with hoofstock, swine or primates.
3. Health and Nutrition
3.1. Diet
1. Identify existing standards for nutrient requirements for all life stages if available
Foraging Ecology
Currently, it appears that the majority of data about foraging ecology is a description of the bats' feeding or foraging habits in the wild. Some studies have involved collecting and analyzing food items for various nutrients (Morrison, 1978; Morrison, 1980; Thomas, 1984). Others examined excreta or stomach contents of bats in the wild (Stellar, 1986; Thomas, 1984). Each of these methods has its limitations and none quantitatively defines the daily nutrient requirements of fruit bats. Thus to date, there is little information available that describes the nutrient levels required by fruit bats. The only fruit bats for which estimates of nutrient requirements have been made are in the suborder Megachiroptera (Stellar, 1986; Thomas, 1984). Few, if any, quantitative nutrient requirement data for frugivorous Microchiroptera are available.
Many species regularly consume fresh green forages; however, the extent to which forages contribute to overall nutrition is unknown (Kunz and Ingalls, 1994; Kunz and Diaz, 1994; Marshall, 1985). Additionally, fruit and nectar-eating bats can consume other plant parts including flowers,
bracts, nectar, and pollen (Law, 1992; Lowry, 1989; Marshall, 1983). Since fruit is not a rich source of protein, bats can consume protein rich plants and insects, especially during pregnancy, to meet their protein requirements (Courts, 1998). Diets in the wild are influenced by seasonal availability, and this can also be modeled in captivity.
Section adapted from Dempsey, J. 2004. Fruit bats: Nutrition and dietary husbandry. Fact Sheet 014. Nutrition Advisory Group Handbook.
Digestive Tract Morphology and Physiology
Fruit bats are highly efficient in extracting the liquid portion of chosen foods. They have fewer teeth than insectivores,10 and their teeth are broad and relatively flat for crushing fruits, allowing the bats to squeeze out and swallow the juices.23 The fibrous portion remaining is much reduced in moisture and is spit out in tightly compressed pellets (ejecta). Seeds also may be swallowed, but many of those from figs appear to pass whole into the feces.23,48 To meet nutrient needs, daily food intakes (on a wet basis) range as high as 2.5 times body mass.14,15,16,26,31,48,63, 70 These large volumes of food are processed through the digestive tract rapidly, with transit times ranging from 15-100 min.30,48,69
The gastrointestinal tract of the fruit bat species that have been studied is highly modified compared to bat species with other feeding strategies. The stomach is large and more complex, the small intestine is long and convoluted, the cecum is absent, and the large intestine is short and nearly indistinguishable from the small intestine.30,68,69 There appear to be no areas of fermentation analogous to the rumen of ruminants, and significant concentrations of gastrointestinal fermenting anaerobes have not been found.30 Rather, it is thought that the enlarged, complex stomach and long, convoluted intestine provide the space and surface area required for digestion and absorption of nutrients from the large volumes of liquid consumed.
Nutrient Content of Foods
Upon comparison with established nutrient requirements of other mammals and the foods needed to provide them, fruit, when consumed alone, would seem to constitute an inadequate diet. Analyses of most cultivated fruits indicate that the concentrations of many nutrients are quite low. However, there are few documented analyses of the nutrients in wild fruit species, and A. jamaicensis has been reported to feed on fruits from over 70 genera.23 Thus, it may be important to distinguish between cultivated and wild fruits. Limited compositional data on proximate fractions and minerals in both are presented in Tables 1 and 2. The cultivated fruits listed tend to be lower in fiber, ash, and calcium (dry basis), with some higher in moisture, than the listed wild fruits.8,19,25,31,59,60,66 Comparisons between cultivated and wild fruits in concentrations of vitamins could not be made because published vitamin values for wild fruits were not found.
Fruit bats in the wild appear to meet their nutrient needs by consuming large quantities of a
mixture of native fruits, with some consumption of flower parts, leaves, and insects.
2,11,12,21,23,28,33,34,36,37,38,46-49,61,78 In captivity, fruit sources are limited to those that are cultivated and readily available. As a consequence, it may be important to ensure that all essential nutrients are supplied by using other nutritionally complete foods. To formulate such foods, it is important to know which nutrients are essential to fruit bats and in what amounts they should be supplied.
Table 1. Comparison of the macronutrient composition of cultivated and native fruits. Expressed on a dry matter basis
|Fruit Type |Moisture % |Gross Energy |Protein |Nitrogen |Fat |
| | |Kcal/g |% |% |% |
|Cultivated a,b | | | | | |
|Apple |84.50 |0.03 |0.05 |4.5 |0.02 |
|Banana |74.30 |0.02 |0.08 |11.9 |0.04 |
|Cantaloupe |89.78 |0.11 |0.17 |21.5 |0.04 |
|Orange |86.80 |0.30 |0.11 |7.6 |0.04 |
|Native | | | | | |
|Fig (F. pertusa)c ripe fruit |77.20 |0.74 |0.12 |56.60 |0.03 |
|Fig (F. trigonata)cunripe |83.70 |0.74 |0.23 |49.9 |0.10 |
|fruit | | | | | |
|Fig (Belize native)d |72.08 |2.04 |0.18 |58.1 |-- |
|Fig (Indonesia native)e |-- |1.21 |0.33 |65.7 |-- |
|Fig (Uganda native)e |-- |1.52 |0.18 |94.7 |-- |
A Data from Pennington and Church.60
B Fruit without skin or peel, includes seeds.
C Data from Edwards.19 N=3 for F. pertusa, N=1 for F. trigonata.
D Data from Silver et al.66 Samples were pooled from multiple Ficus sp., N=5.
E Data from O’Brien et al.59 Indonesia N=20, Uganda N=10.
Nutrient Requirements
Despite differences in diet and feeding strategy among mammals, most species that have been studied appear to have similar qualitative nutrient needs for normal tissue metabolism. Presumably, these similarities also apply to fruit bats. Approximately fifty nutrients have been identified as dietary essentials for mammals. That is, they must be obtained from the diet or through the activity of gastrointestinal microbes because they cannot be endogenously synthesized in quantities appropriate to meet animal needs.72
Water
Water is the easiest and least expensive nutrient to provide in captivity. A supply of water is crucial due to its involvement in a variety of essential functions within the body. The need for liquid water is influenced by variables such as ambient air temperature and humidity, solar and thermal radiation, metabolic rates, and food composition and intake.64 Fruit bats have been maintained in laboratory settings on mixed fruit diets without free access to liquid water and appear to obtain the water they need from their high-moisture fruit diet and presumably from water released during metabolism of absorbed energy sources (metabolic water). However, many species have been observed to actively consume water both in captivity and in the wild. Wild species of Pteropus on oceanic islands have been observed consuming sea water, and their kidneys appear well-adapted to excreting salt.29 Therefore, considering the limited food choices and, in some cases, fluctuating environmental conditions, it is prudent to provide ad libitum access to fresh water in captivity.
Protein and amino acids
Proteins contain nitrogen, are major constituents of the animal body, and are vital to all tissues. Amino acids are the functional building blocks of proteins, and animals with relatively simple stomachs and little or no capacity for fermentation require a dietary source of 10-12 amino acids that cannot be synthesized metabolically at an adequate rate (dietary essentials).64,72 Essential amino acid requirements for bat species are not known nor has the amino acid composition of many foods consumed by bats been determined, although Herbst26 has reported relative concentrations of arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, and valine in fruit pulp protein of four plant species (Cecropia peltata, Chlorophora tinctoria, Ficus ovalis, and Piper amalogo). It is not known whether the amino acid composition of protein in juice squeezed out of the pulp and swallowed by fruit bats is the same as that in the pulp.
Fruit, as the only food item, is considered by many researchers to constitute an inadequate diet because of its low protein content when compared to other plant and animal food sources, although the quality of that protein is relevant to such a conclusion. It has been argued that both pteropodid and phyllostomid fruit bats must supplement their fruit diets with relatively higher protein items, including a more complementary array of amino acids, such as might be found in insects,48 pollen,35 or leaves32,33,38,78 in order to meet protein needs. However, other researchers maintain that fruit bats can meet their protein requirements exclusively with fruits,9,15,26,67,70 and fruit bats (Carollia brevicauda and Sturnira ludovici) in Costa Rica showed a strong preference for fruit (Acristus arborescens) that was not infested with insect larvae.20 Further, it has been proposed that most fig wasps will have departed figs by the time they become ripe and are consumed by bats, and residual corpses are unlikely to contribute significantly to protein intake.8
Recent research supports the latter hypothesis, at least for maintenance of adults. These studies have been conducted using diets that approximate the protein concentration of fruits (both cultivated and wild) or by using wild fruits alone, thus suggesting that fruit bats have the ability to meet their protein requirements for maintenance on very low protein diets. This may be accomplished in part through minimal nitrogen excretion,31 and by adjusting dry matter intake to meet protein needs, regardless of dietary energy concentration.63 A diet containing about 9% crude protein (DM basis) was consumed by captive fruit bats (Pteropus hypomelanus, P. pumilus, P. vampyrus) at 28% of body weight on an as fed basis or 7% as dry matter.16 Studies of the protein needs of A. jamaicensis (phyllostomids) weighing 39-50 g found that 0.28-0.30 g/day were required for adult maintenance, or about 5% of dietary dry matter.48,63 In another study, adult A. jamaicensis bats weighing 36.8 g achieved nitrogen balance at protein intakes of 0.17 g/day on a “high-energy” diet and 0.46 g/day on a “low-energy” diet.15 Maintenance protein requirements for adult Carollia perspicillata (phyllostomids) were estimated to be 0.14 g/day.14 Adult Rousettus aegyptiacus (pteropodids) weighing 144-157 g achieved nitrogen balance at protein intakes of 0.36-0.83 g/day.15,31 It should be noted that when stable-N isotope analyses were used to quantify the relative importance of plants (fruits) and animals (insects) as sources of assimilable N for five species of free-ranging frugivorous New World bats (Artibeus jamaicensis, Uroderma bilobatum, Dermanura phaetis, Sturnira lilium, and Carollia brevicauda), fruits were by far the most important throughout the year. However, at the end of the rainy season and beginning of the dry season, there was a trend in all species for a decline in the relative proportion of plant protein in the diet, and in some individuals of S. lilium and C. brevicauda, insects became a significant source of protein. It was suggested that fruit bat species may vary in their foraging strategy, with some relying almost entirely on fruits throughout the year, whereas others may switch to insects when fruits are less abundant.27
It is difficult to estimate exact requirements because quite different diets have been used in published studies, and the factors to convert nitrogen to protein may have, in some cases, been incorrect.9,26,43 Assuming appropriate amino acid concentrations in the protein, 4-6% protein in the dry matter consumed and digested appears sufficient for maintenance. Requirements for reproduction or growth may be higher but have not been experimentally determined. Presumably, the essential amino acid composition of dietary proteins as compared to amino acid needs would influence the amounts of protein required for any of the above functions.
Energy
Digestible energy and metabolizable energy are terms used to describe an animal’s energy needs and to characterize the usable energy concentrations in food fed to that animal. Because animal species vary in the way they digest and metabolize nutrient sources, the digestible energy or metabolizable energy concentration in a food varies with the gross energy of that food, the amount of food consumed, and the digestive and/or metabolic abilities of the animal to which the food is fed. A more complete description of energy terms can be found in a National Research Council publication.52
Due to their high concentrations in fruit, carbohydrates are quantitatively important sources of energy in the diets of fruit bats. Dietary fat is a potentially important source of energy, as well, but generally is a minor constituent of high-sugar fruits. Protein in the diet also can be broken down for energy, but that is probably minimal on low-protein diets in which the balance of essential amino acids is just adequate to meet amino acid requirements. Fruit bats presumably have no difficulty meeting energy needs during periods of food abundance because they consume large amounts of high carbohydrate fruits, both in captivity and in the wild. There
is controversy among researchers whether or not fruit bats must “over-ingest” energy in order to meet protein requirements. This is due to the relatively high energy:protein ratio of most fruits. High food (and energy) intakes were necessary to meet protein needs in pteropodids (Epomops buettikoferi, Micropteropus pusillus, and Pteropus poliocephalus) when fed some low-protein fruits but not when fed others.67,70 Carollia perspicillata (phyllostomids) did not need to consume excessive energy to meet maintenance protein needs if appropriate wild foods were available and selected.26 Estimates of metabolizable energy requirements for adult maintenance of A. jamaicensis have been made by a number of researchers, and range from 12 to 34.3 kcal/day.15,48,63 The intermediate value of 17.2 kcal/day found by Reiter63 is equivalent to 43.9 kcal of metabolizable energy/100 g body mass/day (mean body mass 39.2 g) or a metabolizable energy density in ingested dry matter of 3.16 kcal/kg, a metabolizable energy concentration found in many domestic fruits.
Estimates of metabolizable energy requirements for adult maintenance of C. perspicillata weighing 18.5 g were 16.1 kcal/day/bat14 and were 40.1 kcal/day for R. aegyptiacus with a mean body mass of 144 g,31 or 76.3 to 91.9 kcal/day for R. aegyptiacus with a mean body mass of 156.7 g.15
Care must be taken when interpreting published data on energy requirements of fruit bats because species, experimental diets, and levels of permitted activity varied appreciably among studies. Basal energy expenditures of bats appear to vary with species (particularly body mass and foraging and roosting behavior), sexual dimorphism in body mass, precision of body temperature regulation, tendency to enter torpor, and the environmental circumstances within which they evolved.40,41 In addition, both dietary digestibility and metabolizability have usually been estimated rather than directly determined. Some fruit bats eating very low protein diets may consume large amounts of food to meet protein requirements, thus elevating energy intakes. Researchers generally have noted little change in body mass, but studies of changes in body composition appear not to have been made. With respect to energy needs for flight, requirements are surely higher than for resting, and the amount of flight activity required in the wild will vary with food abundance and distribution. In captivity, it is likely that energy requirements for resting and for flight can be met by offering ad libitum quantities of nutritionally appropriate food.
Essential fatty acids
Apart from serving as sources of dietary energy and promoting fat-soluble vitamin absorption, fats also provide essential fatty acids (n-6 and n-3 series). The most important dietary fatty acids for the mammal species that have been studied are n-6 fatty acids, such as linoleic and arachidonic, and n-3 fatty acids, such as ∞-linolenic and longer chain fatty acids in this series. Qualitative requirements for essential fatty acids have been demonstrated in a number of mammalian species although quantitative requirements are mostly undefined. Fruit bats are likely to have dietary fatty acid requirements similar to other mammals. The recommendation for most mammals is to include essential fatty acids in the diet at 1-2% of the total metabolizable energy intake, with linoleic acid comprising the largest proportion of the total. However, the amounts of total essential fatty acids and the proportions of each may vary with species, age, and physiologic state.64, 72 Cultivated fruits generally have very low levels of fat and essential fatty acids.60, 73 Essential fatty acid concentrations in the wild fruits eaten by bats are largely unknown.
Vitamins and minerals
Specific vitamin and mineral requirements have not been determined for fruit bats, and there is no
information on the nutrient requirements of their closest taxonomic relatives. Limited data are available on a few primate species.50 The National Research Council (NRC) has established vitamin and mineral requirements for a variety of domestic and laboratory animals.50,53-56 NRC nutrient requirements for rats and mice are shown in Table 3.55 The range in body mass of laboratory rats and mice is similar to that of several species of fruit bats, although relative intakes of dietary dry matter and energy are typically higher for bats. Thus, when nutrient requirements are expressed per unit of dietary dry matter, bats would be expected to consume larger amounts of these nutrients per day than would rats or mice of comparable mass and physiologic state. As a consequence, until specific requirements are determined, diets for captive bats may be presumed sufficient if formulated to provide bioavailable1 vitamin and mineral levels within the ranges of nutrients for the listed laboratory species. It is known that some bat species lack the
ability to synthesize vitamin C and therefore require a dietary source.3 Despite serum levels of 25- hydroxyvitamin D 103 |>28 |>301 |
|Vitamin B12, µg/kg |26 |7 |23 |
|Choline, mg/kg |>980 |>261 |>1,079 |
|Calcium, % |0.85 |0.63 |0.85 |
|Phosphorous, % |0.61 |0.52 |0.58 |
|Magnesium, % |0.17 |0.09 |0.15 |
|Sodium, % |0.19 |0.06 |0.21 |
|Potassium, % |1.16 |0.90 |0.84 |
|Iron, mg/kg |411 |352 |140 |
|Copper, mg/kg |14 |7 |15 |
|Manganese, mg/kg |84 |30 |38 |
|Zinc, mg/kg |90 |29 |78 |
|Iodine, mg/kg |0.98 |0.26 |>0.8 |
|Selenium, mg/kg |0.13 |0.05 |0.28 |
a Fed to Rodriguez fruit bats (Pteropus rodricensis) at Brookfield Zoo for 5 years (Ca phos., dibasic, added at 3 yr).
b Fed to Neotropical fruit bats (Artibeus jamaicensis) at Brookfield Zoo for 5 years.
c Fed to Rodriguez fruit bats (Pteropus rodricensis) at Philadelphia Zoo for 5 years.
d Whole fruits include apple, banana and orange; chopped fruits include apple, banana, blueberries, currants, grapes, mango, and raisins.
e Vegetables (nonstarchy type) consisted of carrots, either steamed or raw.
f Starchy vegetables consisted of sweet potatoes, either steamed or raw.
g Leafy green vegetables included celery, romaine lettuce, and spinach.
h Purina Mills, LLC, 1401 S. Hanley Rd., St. Louis, MO 63144 (800-227-8941).
i Marion Zoological Inc., 2003 E. Center Circle, Plymouth, MN 55441 (800-327-7974).
Summary
Although specific nutrient requirements for frugivorous and nectarivorous bats remain virtually unknown information exists which provides practical guidelines for formulating diets for captive bats. This information must be reviewed critically, applied sensibly, and compared with what is known for other mammalian species until more specific research is conducted. Opportunities for research in bat nutrition abound and, in view of the diversity of species, the information derived would improve not only our understanding of the nutrient requirements and dietary husbandry of bats but also of other species with similar dietary habits and feeding strategies.
(*note- end of section adapted from Nutrition Advisory Group Handbook)
2. Provide sample recommended diet(s) for all life stages based on nutritional requirements and identify body condition norms as determined from wild animals, if possible
PRELIMINARY TARGET NUTRIENT LEVELS (drv matter basis)
Daily Diet
Nutrient Composition
Crude protein (%) 2.0- 15.0*
Fat (%) 5.0-9.0
Vitamin A (IU/g) 4.0- 14.0
Vitamin D2 & D3 (IU/g) 0.2-2.0
Vitamin E (mg/kg) 11.0-56.0
Calcium (%)* * 0.5- 1 .O
Phosphorus (%) * * 0.4-0.9
*Reported levels of protein consumed by free-ranging and captive Megachiropteran and
Microchropteran fruit- and nectar-feeding bats fall in this range (Morrison, 1980; Rasweiler, 1977; Reiter, 1993; Stellar, 1986; Thomas, 1984).
**For Mammals, Calcium:Phosphorus ratios of 1: 1 to 2: 1 are recommended (Robbins, 1993).
Because we have yet to delineate the target nutrient levels, we are providing diets that, on face value, appear to meet the above indicated nutrient levels. No examination of micro-nutrient levels has occurred. These diets have been provided by several institutions that consider their programs successful. Please note that these are presented only as suggestions and have not been subjected to thorough review. To provide suggestions for easily adaptable diets, the data have been modified slightly and presented as food groups rather than specific food items. The total quantity to feed is not given and is dependent on many factors. However, as a rough guideline, an average active adult bat may consume a total of approximately 10- 15% of body weight per day (dry matter basis); or 50-120% of body weight on an as fed basis. If the animal is lactating this may increase to 1.5 times that per day. Care should be taken that the animals do not become obese when fed ad libitum.
Comparison of the Approximate Nutrient Content of Three Working
Diets with Preliminary Target Nutrient Levels (dry matter basis)
Target Zoo Zoo Zoo
Nutrient Levels A B C*
Crude protein (%) 2.0-15.0 12.3 19.0 4.9
Fat (%) 1.0--5.0 7.2 3.0 4.4
Vitamin A (IU/g) 4.0-14.0 26.0 14.9 8.1
VitaminD2& D3
(IU/g) 0.2-2.0 6.2 3.2 0. I**
Vitamin E (mg/kg) 11.0-56.0 133.1 50.2 29.8
Calcium (%) 0.5- 1.0 0.4 0.8 0.1 ***
Phosphorus (%) 0.4-0.9 0.3 0.4 0.1
* Values reported are averages because daily diet composition varies at this Zoo.
**Animals at this facility are housed under full spectrum lights
***Animals have ad libitum access to a mineral wheel
Working Diet Composition
We are aware of a number of nutritional concerns about some of the diets being used in captive feeding regimes today. We hope to address these in the final document.
Food items: The proportions represented below are derived from the three working diets presented above. It is possible to achieve the nutrient levels of the Zoo diets outlined above by offering a diet consisting of the following food items. For adaptability to different institutional situations, we are presenting the diets as food groups in percent to be included in the total diet. This is percent contribution of each item (or food group) by weight, as fed.
COMPARISON OF THE PERCENT CONTRIBUTION OF FOOD GROUPS IN THREE
WORKING DIETS (AS FED BASIS)
Zoo Zoo Zoo
Food group A B C*
Fruit(%) 74.1 16.0 90.4
Vegetables (%) - 7.0 -
Starchy vegetables (%) - 7.0 -
Leafy, green vegetables (%) - 14.0 2.3
Fruit juice/nectar (%) - - 6.5
Water (%) - 41.0 -
Nutritionally complete products (%) 23.3** 7.5*** -
Protein supplements (animal-based) (%) - - 0.7
Home-made protein/ vitamin/mineral
supplements (%) 2.6 4.5 0.1
* Values reported are averages because daily diet composition varies at this Zoo.
**This consists of 14.2% canned primate diet and 9.1% canned feline diet.
*** Total contribution is from high protein monkey chow.
Food groups: The diet can comprise one or more of the following foods in the quantities outlined above.
Fruit: apple, banana, grapes, pear, papaya, dried figs, raisins, melon, kiwi, etc.
Vegetables: carrots, green beans, etc.
Starchy vegetables: sweet potatoes, corn, etc.
Leafy, green vegetables: lettuce, spinach, kale, collard, mustard, etc.
Please notice that all of the working diets outlined above use home-made supplements in conjunction with commercially-made, nutritionally complete products. If one or more of the products are not included in each of the diets as outlined, the diet will no longer reflect the nutrients presented in the previous section. Many of the home-made recipes are difficult, and sometimes expensive, to make. Therefore, in the final nutrition chapter we intend to provide recommendations for use of easily attainable, nutritionally complete diets that will allow formulated diets to meet target nutrient levels.
In addition to specialized housing, Long-tongued bats have specialized dietary requirements. A nutritionally complete diet for nectarivorous bats is composed of a liquid diet of fruit juice/nectar and fresh fruits such as cantaloupe and banana. Table 1 present a successful diet currently in use at the Biodome and the Organization for Bat Conservation’s facility (OBC).
Table 1. Liquid diet for nectarivorous bats
|Food components |Quantity |
|Tropical Passion Oasis unsweetened (Juice)* |960 ml |
|Corn oil |20 ml |
|Purina High Protein Monkey Chow 5045 |15 g |
|Nektar-plus† |55 g |
|Nectar powder mixture |30 g |
Sources of diet components
* A.Lassande Inc., Rougemont (Quebec), Canada
† Nekton, Pforzheim, West Germany
Nectar powder mixture
|Components |Quantity |
|Mixed cereal |500 g |
|Fructose |500 g |
|Powder milk |300 g |
|Wheat germ oil |160 g |
|Vitadol Plus§ |40 g |
§ Upjohn Company, Animal Health Division, Orangeville, Ontario, Canada.
3. As appropriate address the influence of the following variables on dietary requirements
Age (infant, juvenile, reproductive adult, senescent adult, etc.)
body size
reproductive status
seasonal changes in ambient temperature
seasonal changes in body condition
seasonal changes in nutritional requirements
activity levels
health status
4. Address issues of palatability, texture, processing, etc. that will
encourage species-appropriate appetitive behaviors.
Fruit bats squeeze the juices out of their food and spit out the dry, fibrous portion. Blending or puréeing fruits forces the bats to ingest large quantities of fiber that may impair absorption of nutrients (George, 1990). Furthermore, because fruit bats are unable to concentrate the fiber in blended diets, rectal prolapse may occur (Snell, 1994). Trupkiewicz et al. (in prep.) reported frequent rectal prolapses in a zoo colony of Pteropus rodricensis that may have been related to diet.
There remains a large amount of information to be collected in order to finalize recommendations for target nutrient levels and appropriate feeding procedures for Megachiropteran and Microchiropteran fruit bats. Much of this information will become available through our proposed pre-survey and following in-depth survey of diets and feeding practices in institutions currently housing fruit bats. The information still needed includes, but is certainly not limited to, the following: Nutritional deficiencies/toxicities, feeding behavior in captivity, quantities of food to offer (factors include: age, species, size of housing, number in group, etc.), form of diet offered (e.g., chopped vs. whole fruits, etc.), problems with obesity, seasonality (e.g., feeding different diets based on season), feeding schedules, feeding location, use and potential nutrient contribution of fresh green forages and other plant parts (see Appendix F for a partial list of forages accepted by captive colonies of fruit bats), behavioral enrichment for captive fruit bats.
1. Medical management – guidelines should address and specify acceptable husbandry practices for the taxon at different life stages with respect to
1. Quarantine and hospitalization
We strongly recommend consulting with veterinarians and others experienced in quarantine procedures when receiving bats. In addition, the Centers for Disease Control (CDC) can provide quarantine information and recommendations.
Ideally, wild-caught animals should be held for one month prior to shipment from their country of origin. This has the benefit of allowing detection and removal of any sick animals, and it allows the animal to adapt to captivity prior to shipment7. During the holding period prior to shipment, the bats should be examined, preferably by a veterinarian, and treated for ecto- and endoparasites.
When captive- born bats are received from another institution, ideally they should be quarantined for 90 days. However, this may vary depending on the source of animals and their previous standard of care and medical testing. Minimally, they should be quarantined for 30 days. Wild-caught bats arriving from another institution should be quarantined for a minimum of six months. Quarantine conditions should closely mimic the bats' natural ambient conditions (torpor can lengthen the disease incubation time). All bats should be examined as soon as possible after shipment for evidence of disease. An additional exam should be performed before the animals are removed from quarantine. Any bats that die during quarantine must have a complete necropsy (see Section 3.2.2). If a bat dies during quarantine and the cause is unknown, the quarantine period should be extended to allow sufficient time for detection of disease in the remaining animals. All Pteropus species should be screened for henipavirus.
Following completion of quarantine, it is recommended that wild-caught animals placed on exhibit be isolated from other animals for at least one year, and housed in cages that protect the public from bat urine and feces (e.g., plexiglass-fronted cages). Animals to be introduced to a mixed collection should have been in isolation at least one year, and the group should be free of evidence of infectious diseases. It is preferable that animals to be introduced into mixed exhibits be first or second generation removed from wild-caught animals. The same is also true for education animals.
Except for the 90 day quarantine period following receipt of the bats, the other requirements (e.g., one year isolation and first and second generations) can be completed at other accredited facilities.
1. Identify problems arising from isolation of social taxa and suggest possible mechanisms for avoiding these problems
2. Preventive medicine (testing, vaccinations, parasite control, etc.)
Ideally, all bats should be individually identifiable (see Section 5.1) and each bat should have a separate medical records.
Inoculations
Recent studies suggest that captive bats can be vaccinated for rabies (Peters and Isaza, 2005; Lollar, 2004). However, vaccination of insectivorous bats constitutes extra-label use of the rabies vaccine.
Recommended Routine Medical Procedures
Ideally, each bat should be examined once a year. When applicable, this examination could include collection of blood for hematology, plasma biochemical analysis, and plasma for freezing (freezing temperature equals -70˚F). When colony size renders individual exams impractical, a few individuals could be selected from the colony for examination.
Life Span
For their size, bats have very long life spans. Short-tailed leaf-nosed bats (Carollia perspicillata) can live up to 12 years of age, and have a shorter life span than the larger tropical species of megachiroptera. Straw-colored fruit bats (Eidolon helvum) can live up to 22 years and the record age of an Indian flying fox (P. giganteus) is 31 years (Jones, 1982; Richarz and Limbrunner, 1993). More data need to be collected on this issue.
Necropsy Protocol
All bats that die should be necropsied. A gross necropsy alone is inadequate without submission of representative tissues (brain, skeletal muscle, heart, lung, liver, stomach, pancreas, small and large intestines, kidneys, gonads, bone and bone marrow) for pathology. A section of brain from new or wild-caught bats that have died in captivity should always be submitted for rabies testing. Accurate necropsy records should be made and mortality rates should be tracked on a yearly basis (including neonatal deaths).
Parasites
1. Screening. All parasites collected should be submitted for identification. Fecal examination for parasites should be done every six months for individuals and every month on a sample collected from the colony.8 These tests should be performed by people capable of identifying the parasites likely to be found in bats.
2. Commonly observed parasites and treatments.
a) Ectoparasites: Emtoparasites include mites, lice, chiggers, fleas, ticks and flies (Whitaker, 1988). No ectoparasites should be tolerated and several ectoparasites are potential vectors for blood borne diseases. Imported animals should be examined and treated in the country of origin. Many ectoparasite species will spontaneously leave the wild caught bat. Some ectoparasites spend most of their time in the environment, and therefore any treatment program should include changing props, substrate and so forth, as well as disinfecting, and in large cages, fumigating.
Pest strips work well to deter ectoparasites confined to the host (e.g., mites, chiggers and lice). However, animals in outdoor exhibits (where use of pest strips is not feasible), and those with heavy ectoparasite loads can be treated with ivermectin (200-400 pg/kg PO, IM, SC) every 10 to 14 days for three treatments. Repeated treatment may be necessary to kill the parasites that subsequently hatch from the protected eggs. Ivermectin has a narrow therapeutic index. Care should therefore be taken in calculating dosages. Signs of toxicity range from lethargy and decreased appetite to full paralysis. These signs occur within the first 24 to 48 hours. Treatment is supportive; there is no antidote. Ivermectin for injection must be diluted with propylene glycol, not water. This is because it is an oily substance and does not mix well with water. There is an oral liquid preparation for horses that can be diluted with water and administered orally.
Alternatively, some ectoparasites are susceptible to pyrethrin-based sprays. Take care not to use excessive amounts (e.g., soaking the animal), and do not use in confined, poorly ventilated areas. Rather than spray, it may be better in smaller bats to moisten a towel, and rub into the coat. Whenever using a treatment for the first time, use in a few individuals first and observe.
b) Endoparasites (see Coggins, 1988 and Constantine, 1993):
The major endoparasite of concern is Toxocara pteropodis.
Round worms:
Ivermectin 200 to 400 μg/kg PO. Extreme care must be taken when diluting ivermectin, especially with smaller bats.
Fenbendazole 75 to 100 mg/kg PO, repeat in 10 days.
Tapeworms:
Praziquantel 7.5 to 15 mg/kg IM, PO.
Trematodes:
Prauquantel: high dosages (50 mg/lkg) are not very effective.
c) Hemoparasites: Hemoparasites (Hepatocystis sp.) have been observed in imported Pteropus pumilus from the Philippines. These parasites spontaneously disappeared from the blood over a 12 to 14 month period. No present treatment is recommended.
d) Protozoa: Metronidazole 75 to 100 mg/kg PO.
Behavioral Signs of Illness
Behavioral signs of illness include: decreased appetite, wings constantly wrapped to the body (even when disturbed), lethargy, reluctance to move9, not flying or abnormal flying, and animal found on floor (note: some healthy individuals will sleep on floor or retrieve food from floor).
Common Injuries and Their treatment
1. Band constrictions: Pay attention immediately after placement and check on a periodic basis (see Section 5.1). Remove the band immediately if swelling and/or ulceration occur.
Treat severe injuries with antibiotics.
2. Other thumb injuries (e.g., tom nails, simple fractures or abrasions as a result of contact with rough surfaces): Treat with antibiotics if deemed necessary.
3. Wing tears generally heal well by themselves. Wing tears that involve the leading or supporting wing edges require suturing.
4. Bandaging that incorporates the wing web may obstruct inflow of arterial blood causing subsequent necrosis (i.e., ischemic necrosis).
5. Fractures (wings and legs): Take special care not to pull too hard when removing bats from wire and perches. Rough handling in young bats may cause injuries at growth plates of long bones.
6. Dry skin and feet may be caused by low humidity (see Section 1.2).
7. Wing bone injuries: These injuries need to be carefully evaluated by a veterinarian to determine appropriate treatment.
8. Swollen joints: Swollen joints may be caused by septic (bacterial) arthritis. Treatment is based on culture and antibiotic sensitivity, as well as radiographs to confirm severity of lesions.
9. Infected marking glands on chest: These may respond to antibiotics. In severe cases, it may be necessary to excise the lesion surgically.
10. Torn lower lips. These may need to be sutured.
Physiological Reference Values
1. Heart and respiratory rates: Rapid, except during torpor. 10
2. Hematology and blood reference values: Available data are limited. The TAG encourages zoos to submit data from their collections to ISIS. In addition, more research is required to obtain normal reference values from free-ranging bats. Data that are available are sometimes compromised by poor blood collection and handling techniques. The following tips are recommended to facilitate collection: In a healthy bat, 10% of blood volume can safely be collected. This is approximately 1% of body weight in grams (1 gram = 1 ml). For example, in a
450 gm bat, 4.5 mls of blood can be collected for plasma biochemical determination. Blood should be collected into a heparinized syringe, immediately centrifuged, and the plasma refrigerated prior to analysis.
3. Management of hereditary diseases or disorders
Major Disease Problems and Their Treatments
1. Viral. No treatment is available for viral diseases.
a. Rabies (see Constantine, 1988 and 1993): Rabies is not a major disease problem for bats, although, when contracted, the virus will kill animals. The primary concern is for public health (see Section 2.2.6.2). All bats should be vaccinated for rabies, although this constitutes an extra-label use of the vaccine (Peters and Isaza, 2005; Lollar, 2004).
b. Henipaviruses
c. Other viruses: further research required.
2. Bacterial. Treatment is based on culture and sensitivity.
a. Salmonella
b. Other
Antibiotics used in bats include: fruit-flavored oral preparations, Baytril , Trimethoprimsulfa combination, Amoxicillin, Clavamox, Chloramphenicol palmitate, and Keflin. Injectables include: TMZ, Amikacin, Enrofloxacin.
3. Parasitic (see Section 3.2.2).
4. Nutritional
Diets for long-term maintenance of bats need to be perfected (see Section 3.)
a. Dilated cardiomyopathy - probably vitamin E deficiency.
b. Vitamins C and B 12
c. Metabolic bone disease.
5. Toxic
a. Zinc (galvanized wire)
b. Lead
c. Fluoride - P. rodricensis appears to be sensitive to low level exposure to fluoride. Cumulative effects of fluoride exposure may result in toxicity (J. Trupkiewicz pers. com.). At the Philadelphia Zoo, multicentric hyperostosis (bone lesions) that is consistent with fluorosis has been diagnosed during post-mortem examination of five P. rodricensis. Similar lesions have been identified in other species of captive pteropids exposed to high levels of dietary fluoride (Duncan et al., 1996).
d. Some plants
4. appropriate capture, restraint and immobilization techniques and training for routine and non-routine procedures
Methods of Capture, handling, and restraint
Chiropteran wing bones are delicate and can be easily broken during capture. If using a net, make sure it is wider than the bat's wingspan to avoid damage to wing bones and membranes. Mist nets can also be used to capture bats. Be sure to have experienced personnel and adequate staff on hand when using mist nets. It is important to remove bats from nets immediately so they do not get overly entangled. To remove bats that are hanging on wire or perches, be sure to unhook their nails rather than pulling on the bat. This will avoid injury to toes. In large, free-flight aviaries, it may be useful to erect a food trap. This is accomplished by feeding animals in a small enclosed area on a regular basis so that when it becomes necessary to capture bats, the area can be sealed as the animal is eating.
Appropriate techniques for handling small mammals are generally adequate for bats, although care should always be taken to immobilize the wings. Do not hold any bat by the wing tips during restraint and always fold wings close to the body. To avoid permanent damage, special care should be taken not to hyperextend the joints. While we do not know if holding bats head-up for prolonged periods presents a risk to bats, we recommend trying to hold them head down (or at least horizontally) as a precaution.
It is a good idea to wear a long sleeved shirt and gauntlet gloves11 when handling bats, especially the larger fruit bats. To reduce keeper injuries, welders’ gloves can be useful in handling large fruit bats. However, use of them may cause injuries to the animals. If used, extreme care should be taken not to apply excessive pressure. When weighing fruit bats, place the bat in a cloth bag before putting it on the scale to reduce stress.
Immobilization and Anesthesia
The following recommendations are for a one pound fruit bat. The dose will need to be higher per kilogram for smaller bats and lower per kilogram for larger bats. The preferred method of anesthesia is isoflurane in oxygen. Mask down animal at 5% isoflurane until the animal is relaxed, then decrease to 2.5 %. Maintain oxygen flow at 2 liters per minute. If gas anesthesia is unavailable, a mixture of ketamine and xylazine can be utilized. For 30 minutes of immobilization, combine equal volumes of ketamine (100mg/ml) and xylazine (20mg/ml) to achieve a concentration of 50mg/ml ketamine and 10mg/ml xylazine and administer. Give .2mls/kg of mixture for a 500 gram bat.
5. Management of neonates and geriatric animals
Neonatal Examinations
Births, as well as birthing problems and neonatal deaths, should be recorded. The neonate should be visually assessed soon after birth to make sure it is suckling, has normal activity for its age, and there are no gross congenital abnormalities. Although not practical or advisable for most situations,12 neonatal bats can be examined, weighed and measured immediately after birth and during development. Information from such a procedure can help to establish baseline information for the individual, as well as for the species. Growth curves are invaluable for valuating health status of lactating females and hand-raised bats. For more information on neonatal exams, see Barnard, 1994.
When examining neonates and suckling bats, it is recommended that the mother be anesthetized (see Section 3.2.4) to decrease the likelihood of injury to both parent and pup. The pup can be removed from the nipple by gently placing a smooth probe (e.g., small rubber spatula) at the comer of the mouth of the pup until it releases its grip on the teat. Force should not be used and care should be taken to avoid damaging the milk teeth. Rubber spatulas work well to insure teeth and mouth do not get damaged. The pup is either placed on the mother before recovery, or placed in a small cage with the awake mother. Placement of the pup on the physically restrained mother is stressful, may result in injury, and is generally unnecessary.
6. Management during pregnancy
4. Reproduction
Fruit bats share many of the general reproductive characteristics present in other mammalian species. They reproduce sexually, produce live young, and females nurse pups from one or two mammae located on either side of the thorax. Fruit bats have a rather low reproductive rate, especially considering their size. Most field studies on bats, however, refer to sporadic observation collected only a few times a year. Thus, much of the information on bat reproduction is anecdotal. Some of the information in this chapter was collected through a TAG bat reproduction survey that was sent to all AZA institutions housing bats. Tables 1 and 2, taken from this survey, contain information on development in captive born bats and a summary of bat reproduction data, respectively. For additional information, see Galindo et al, 1995.[pic][pic]
[pic]
[pic]
Age-Specific Fecundity
Generally, females of !arger species do not give birth until they are between one and two years old (Asdell, 1964; Nelson, 1965; Thomas and Marshal, 1984). Pteropus poliocephalus females reach sexual maturity at one and a half years, while males do not reach effective fertilization until they are two and a half years, even though they are considered sexually mature at 18 months of age (Martin et al., 1986). The males of some other Pteropus species also do not reach effective fertilization until two and a half years, even though they are sexually mature at 18 months (Martin et al., 1986). Smaller species are able to reproduce as early as four to eight months of age (Miclkeburgh, et al., 1992; Galindo et al., 1995), with males not becoming mature until between one and two years of age. Cynopterus brachiotis females are sexually mature at four to six months, while the males are mature at one year of age (Heideman, pers. comm., 1992). Many species of fruit bats show a post partum estrus (Galindo et al., 1995; Mickleburgh et al., 1992).
1. Identify seasonal changes in physiology and behavior associated with reproduction and address management implications of such changes
Breeding Seasons
Beck (1973) reports a monoestrous cycle (one single estrus per breeding season [McDonald, 1987) in Pteropus giganteus, polyestrous cycles (multiple estrus cycles per breeding season [McDonald, 1987]) in Rousettus aegyptiacus and three pregnancy peaks per year
in Cynopterus brachyotis. There has been one reported case of possible sperm storage in P.
giganteus in a captive environment, where one female gave birth after nine months of being in a single sex female group (Galindo et al., 1995). In general, larger species of fruit bats seem to be monoestrous, while smaller species are generally polyestrous. In captive Pteropus poliocephalus, mating increases in February, peaking in April (Martin et al., 1986).
Female G. soricina exhibit menstruation and seems to have a reproductive cycle of 22-26 days (Rasweiler, 1972). Mating activity should normally occur during these 3 or 4 weeks. In Central America, Flemming et al. (1972) reported that ovulation and mating may be biannual. Females give birth throughout the year, although the majority of births at the Biodome occur in the warmest period of the year (July and August).
Behavior
Although male bats will attempt to copulate throughout the year (Martin et al., 1986), the highest copulation activity in bats is during the mating season. When not in season, females will avoid copulation and will generally fly away from interested males. As part of the mating ritual, the interested male may flick his wings towards the female and vocalize loudly. He will then attempt to groom the female while he orients himself to her dorsal surface. He will attempt to clasp her with his wings and thumbs, grasping the thickened nape of her neck with his teeth. During a successful copulation, the female cooperates by hanging from the male's legs (Baker, 1991; Martin et al.; West, 1986). Intromission is short and is accompanied by a quick ejaculation (Baker, 1991; Martin et al., 1986). Copulation is generally ventral/dorsal; however, Eidolon helvum have been observed copulating in the ventral/ventral position (Galindo, 1995). 13
Breeding success of G. soricina seems not to be affected by the environment and outside disturbance. Indeed, a few studies showed that G. soricina can mate and conceive despite being housed in small cages and subject to daily handling (Rasweiler 1972, 1974). According to Rasweiler (1974), a low male/female sex ratio may be advisable to ensure an efficient breeding success with G. soricina.
Gestation
As a general rule, bats carry only one young per gestation period. Twining is present occasionally, though survivability of both the pups and the dam is very low. At least one of the pups may need to be hand-raised to relieve the dam of the stress of raising twins. In the wild, however, smaller species such as Artibeus jamaicensis, Eidolon helvum and others have been seen to do quite well with twins (Skinner and Smithers, 1990). Gestation in Pteropodid bats has been estimated at 105 days to 210 days. Examples include Pteropus rodricensis at 140- 180 days, Rousettus aegyptiacus at 105- 107 days, and Epomophorus wahlbergi at 180-210 days (West and Redshaw, 1987; Baker, 1991; Kunz et al., 1994; Carroll, 1988; West, 1985-86; Falanrow, 1988; Sowler, 1984).
Eidolon helvum are essentially monoestrous, and are thought to have two distinct breeding strategies in the wild. One strategy is to have a four month gestation with conceptions in the autumn and births in the spring (Anderson, 1912). Another is to copulate in June or July and, utilizing a delayed implantation strategy, have gestation begin in November, with the young being born between March and April. This strategy usually coincides with the rainy season (Fayenuwo and Halstead, 1974; Funmilayo, 1979; Galindo et al., 1995). Births of Pteropus rodricensis in captivity occur mainly during October through April, with a peak between late March and April. They show synchronized births and can potentially have two birth periods a year with an interval of 260 days (Carroll, 1988).
There are some suggestions that Epomophorus wahlbergi have conceptions that occur from May to December, with the peak occurring May through July. Births peak in November and December (Sowler, 1984), thus making gestation roughly six to eight months. Rousettus aegyptiacus breed two times per year in East Africa and year-round in North Africa (Kingdom, 1974).
Parturition
There is little behavioral change in the weeks and days prior to parturition. Female bats will pant immediately prior to and during parturition. For birthing, she will alternate hanging with all four limbs and clinging to the wire hanging from just her thumbs. In the Pteropodidae, infants are born head first and, as soon as the head is exposed, the female will bring her feet up and catch the pup as it emerges. The Microchiroptera are usually born rump or feet first.
A typical Pteropus birth and placental delivery may last only a few minutes to two hours (Baker, 1991). There are usually few warning signs to show when a female is about to give birth. The first signs are manifested two to three weeks prior to parturition. The bulk of the fetus shifts from its usual sprawled lateral position to a more centralized, ventral position on her abdomen, directly above the vaginal area, which seems to swell slightly. Hours prior to parturition, the expectant mother separates herself from others in the group and starts fanning herself. When she is ready to deliver, she hangs from her thumbs, as though she is attempting to void, and strains hard. As the pup emerges head first, it is positioned so that the wings are folded around the head. There is little blood loss. At the actual moment of birth, the female adopts a horizontal position, grooming and licking the genitalia and the emerging infant (West, 1986). There is usually a pause between expulsion of the head and rest of the body (Martin et al., 1986) which will generally last from ten minutes to several hours (Martin et al., 1986). During this time, the pup has its eyes open, twitches its nose, and occasionally will vocalize. The mother opens up her wings to make a "net" to protect the infant from falling. The offspring hangs on to the mother with its feet and thumbs and is guided to a nipple by the mother. The mother, and occasionally other cage mates, will then eat the placenta (Martin et al., 1986). Kunz et al. (1994) have documented alloparenting in Pteropus rodricensis.
Infant Development
Fruit bats grow and mature quickly. Smaller species of fruit bats are born with their eyes closed and ears folded back, both opening after ten days (Lombard, 1961). Artibeus jamaicensis have an average birth weight of four grams, and wean at an average age of three and a half months (Galindo et al., 1995). All fruit bats are born with some fur, well developed claws to cling to the mother's ventral side, and deciduous recurved milk teeth (West, 1985-86; Nelson, 1965; Pook, 1977). Pteropus rodricensis have short, snubbed muzzles, small wings and large feet (Baker, 1991; West, 1985-86) with a body weight of 45 grams. Forearm length is 43% of adult length (West, 19486). Pteropus poliocephalus are an average of 76 grams at birth (Hood, 1989).
Milk cannot be expressed manually after about six months. However, many species of fruit bats have been seen still on the mother's nipple after one year of age (Galindo et al., 1995; West, 1985-86; Baker, 1991). From observations in the field and in captivity, many species show a post partum estrus (Galindo et al, 1995; Mickleburgh et al., 1992). At birth, G. sorcina males are slightly larger than females (Walker 1975). Nursing lasts approximately 1 month before the young bat can fly.
Neonatal/ Infant Mortality
According to the TAG'S published survey on reproduction of frugivorous bats in North American Zoos (Galindo et al, 1995), 1370 individuals were born within the last ten years in responding institutions. Of those born, 458 (33%) were either stillborn or died before the age of two months. Some of the major causes of neonatal death included: environmental stress (overcrowding, extremes in temperature, capturing for medical procedures), cage mate inflicted trauma, hazards within the enclosure (drowning in pools, eaten by other species housed with the bats), and medical inflictions (cesarean section deaths, infections). The survey also reported that there were higher instances of neonatal deaths in larger species (100 grams and over) to pups born to first time mothers than those born to experienced mothers. Cannibalism was also seen in many instances where overcrowding was an issue. Birthing dams have been seen to partially consume stillborn pups.
In Rodrigues fruit bats, pup mortality was investigated through radiographic analysis, by Cooper and West (1988) who noted a preponderance of cranial injuries, including dislocated mandibular symphyses, and depression fractures of the skull. These injuries are typical of flying fox mothers who immediately reject the pup after birth. First time mothers, obese females, and mothers under stress are more prone to reject pups than well adapted females who have a history of successful births (LeBlanc, pers. comm.).
2. Address hormonal tracking as a mechanism for identifying reproductive state, and assessing feasibility of introduction for solitary species
3. Address timing of introductions for individuals of solitary species
4. Address provision of and describe facilities for parturition and as appropriate, management of females during isolation or denning
5. Address what, if any, circumstances might warrant hand-rearing and identify acceptable hand-rearing and reintroduction protocols
Hand-rearing
Hand-rearing fruit bats is similar to hand-rearing other small mammals. Be sure to wrap the infant in a towel or hang it on a stuffed animal for its comfort and security. Initially, infants should be fed with milk replacer every two hours from six a.m. until midnight. The milk replacer should be a high fat (e.g., 43% dry weight) product that utilizes vegetable oil, not soy14 or butterfat.
Some examples of acceptable formulas are Similac, Puppylac, and Just Born. Feedings can be decreased gradually over time with pureed and then diced fruits being introduced until infants are weaned (large Pteropus species are usually weaned by six months; smaller fruit bats will be weaned earlier). Many suckling fruit bats remain on the nipple until they are weaned and should be given continuous access to a nipple. For additional information on hand-rearing, See Barnard,
1995; Young, 1987; and George, 1988.15
Fostering
The Lubee Bat Conservancy has successfully fostered a Little-golden mantled flying fox pup to its grandmother who was in another enclosure, and lactating. The Durrell Wildlife Conservation Trust has also successfully fostered a Rodrigues fruit bat.
6. Recommend means and duration of contraception for taxon; include all acceptable alternatives and identify the benefits and drawbacks of each
Contraception
Little or no information is available on reversible chemical contraceptive methods in bats.
The most commonly used method of reversible contraception in mammals in AZA institutions are
MGA implants. However, the efficacy of these in bats has yet to be determined. Barnard and
Soloway (1992) describe a method of male castration as a form of irreversible contraception. Recently, Lafortune et al. (2004) showed that vasectomies are possible in bats. Unlike castration, a vasectomy has the potential to be reversed.
Husbandry techniques, such as maintaining single-sex groups, are recommended as the most simple and inexpensive method of contraception. Downfalls such as lack of space to house separate groups of the same species can be overcome. One way to acquire additional space for single sex colonies is to house bats with other taxa (see Section 2.2.4). Another method is for institutions to trade the same species of bat, so each institution receives all of one sex.
5. Behavior management
1. Identify procedures that have been successful in managing the taxon for routine husbandry. Routine husbandry may include such activities as shifting from one area to another, tolerating close visual inspection, tolerating close proximity to caretakers, etc.
Record Keeping
All bats should be included in ISIS records. We further recommend that all neo-natal deaths, stillborns, and aborted fetus' be included in ISIS records. While this is not always an easy task, especially with large colonies of microbats, it is an important tool in determining population demographics.
Individual Identification Methods
All known identification methods have advantages and disadvantages and tend to be species specific. The following is a summary of selected identification methods used in bats (taken from Kunz, in prep.)
1. Transponders. The AZA Chiropteran TAG recommends all fruit bats be permanently identified using the Trovan Electronic Identification System (i.e., transponders), although due to the development of ISO universal readers and transponders other systems such as AVID and Digital Angel (Formerly Destron) are acceptable. 16 To insert a transponder, pinch and pull the skin, insert needle under the skin, and inject transponder right side up. The best placement is in the posterior dorsal region where it will not interfere with movement. Some managers have placed transponders between the shoulder blades; however, this location may interfere with muscles and shoulder blade movements associated with flight. Transponders can migrate, and several observations of the transponders occurring in the patagium have been noted at the Lubee Bat Conservancy, even when they were injected below the scapulas. Advantages of this technique include relative permanence and few health/injury risks. The disadvantage of transponders is that the individual must be in-hand to read the identification.
2. Bead-chain necklace. Many field researchers have used bead-chain necklaces quite successfully and they seem to work well with some species. The advantages of bead-chain necklaces are that they can be seen from a distance and come in many color and/or number combinations. Disadvantages are that beads have been reported to fade, they can break, be abrasive, harbor mites and ticks, food can cake around necklace, and the public sometimes reacts negatively to the "jewelry."
3. Thumb bands. Some species do fairly well with thumb bands, while others, such as Rousettus aegyptiacus and Pteropus rodricensis are able to remove them. Use colored bands17 that are placed on the animal loosely enough to turn easily and not cut off circulation. Aluminum bands are not recommended for fruit bats as they can be compressed if bats chew on them. The advantages of colored thumb bands are that they are fairly easy to read from a distance and there are many color and/or number combinations available. Multicolored band combinations as well as numbered bands should be read from distal end of thumb in toward the wing. Stainless steel bands are also available and work well with some species. However, stainless steel bands cannot be read from a distance (as colored bands can). Therefore, we recommend using transponders for close identification needs and colored bands for remote identification.
4. Forearm bands. Extreme care must be taken when using forearm bands because they can restrict circulation in the propatagium. They may also injure the underlying muscle and tendons if bats chew and bend the band. If used, band combinations or numbers should be read from the distal end of thumb.
5. Ear notching. This technique is not recommended because it disfigures the animal and there are relatively few combinations available.
6. Ear tags. Ear tags can cake with food and can tear out of the ear. In addition, they are difficult to read from a distance.
7. Tattooing Wing tattooing is a short-term identification method because the tattoo does not last long. Another disadvantage is the need to catch the animal in order to read the tattoo. Tattooing of the ear with light colored species such as Egyptian fruit bats (R. aegyptiacus) and Wahlberg’s epauletted fruit bats (Epomophorus wahlbergi) is permanent (LeBlanc, pers. comm.).
8. Freeze branding. This method of identification has not been successful to date.
9. Nail polish. Nail polish, when placed on the individual's back, is fairly useful for short term identification purposes, and many color variations are available. The disadvantage of this method is the frequent need to replace polish. In addition, while nail polish makes for easy identification because it is easy to see, it may be offensive to the visiting public.
All methods of identification, but especially bands, should be checked regularly.
5.2 Identify procedures that have been successful in managing the taxon for non-routine husbandry. Non-routine husbandry includes regular weighing, sample collection, blood pressure monitoring, injections, crating, swimming/climbing into a stretcher, walking into a small stall/funneling space, transport, etc.
See section 3.2.4, and appendix for SOP’s.
5.3 Identify procedures that have been successful in facilitating introductions. These may include separation of individuals from group, stationing, tolerance while feeding, “howdy” units, visitation gates, etc.
Be careful not to overextend quarantine of individual animals or their social behavior may be adversely affected. If possible, quarantine bats in groups rather than singly.
Introducing and removing bats from a colony is generally not problematic. New animals can be introduced immediately into a group rather than maintained in a traditional "howdy" cage (i.e., a small cage placed within the main exhibit cage for the purpose of letting animals become familiarized). However, the use of a howdy cage for introducing a group of bats into a large free-flight exhibit can help new bats get acclimated to the environment and possibly reduce aggression between the new group and established colony. Browse and enrichment can be utilized to offer new animals sanctuary from aggressive cage residents by offering more visual barriers in the enclosure, and distracting current cage residents with food. Other visual barriers that can be utilized are corrugated vinyl roofing, cardboard or cotton bed sheets.
Introducing new bats into an existing colony should take place at the start of a keeper shift, so as to allow maximum observation time. Newly introduced animals should be watched off and on for 24-48 hours to ensure that the animal(s) is eating and has adjusted well. Juvenile and adult bats will frequently perform static flying when placed in a new exhibit as they grow accustomed to the new environment (Carroll, 1978).
The stress of capture of microchiropteran fruit bats (e. g., Carollia perspicillata & and Artibeus jamaicensis) , can induce torpor and/or a period of fasting that can last up to 24 hours. To help prevent this problem, we recommend that removal of individuals be planned for after the normal feeding period.
Initially there will be many confrontations among the bat colony as the group's social structure is challenged and perhaps altered. New males may take over existing males' territories or they will be dominated by the cage residents. Females tend to accommodate to new members more easily than males. Removing bats from colonies causes minimal stress.
If an animal needs to be treated for medical purposes, it is best to provide veterinary care while leaving the animal in the main enclosure. If it is absolutely necessary to remove the animal for treatment, be sure to minimize the amount of time it is separated from the colony and follow recommendations for introductions when reintroducing the animal to the colony. For bats that have to be isolated for protracted periods, their scent marks can be captured by placing a sealed muslin cloth on the ceiling of the isolation cage as a visual barrier, and then moving the scent-marked cloth into the regular pen. Since the scent of this bat was maintained in the enclosure, the bat may have an easier time being reintroduced to its cage mates.
There appears to be no major effect of removing animals from a colony except that, if the individual removed is high ranking in the social order, there may be some jostling while a new hierarchy is established. This may affect reproduction, but usually just for a short time.
If maintaining the colony for genetic management, the breeding male should be removed immediately after the first young are born. If it is known that a female is pregnant, the male can be removed earlier, although care should be taken not to stress the entire colony while attempting to capture males. New males or females being added to the colony should be introduced two to three months after the colony's females give birth. At this stage, the infants will be large enough to fend for themselves should the newcomers act aggressively.
5.4 Identify facility design considerations, husbandry training techniques, and implementation plan that can be used to elicit desired behaviors in a way that is safe for both caretakers and animals.
5.5 Identify those techniques that have been shown to be most effective.
5.6 Identify technical skills and competencies needed by staff
5.7 Appropriate methods of enrichment for the taxon should be identified if not included in categories 1-3 above.
Environmental Enrichment
Environmental enrichment is important for bats, and keepers and managers should spend some time developing new ways to stimulate their bat colonies. Methods of environmental enrichment that are known to be successful include providing naturalistic foods, varying the food presentation, supplying olfactory stimulation, adding props to the enclosure such as ropes, branches, mirrors and so forth, providing adequate flight space, and supplying bats with browse (for additional information on environmental enrichment for fruit bats, see Atkinson, 1993; LeBlanc and Seyjagat, 2000).
Refer to Appendix F for a partial list of forages accepted by captive colonies of fruit bats.
Notes on Individual Species and Unusual Behaviors
Epomophorus wahlbergi will rock back and forth (laterally) with their wings wrapped around them when resting (Wickler and Seibt, 1976).
Rousettus aegyptiacus and other small bats will occasionally sleep on their backs on the floor of the cage (usually propped against a wall).
There are usually high levels of aggression between males in a breeding colony of Cynopterus brachyotis.
In outdoor enclosures (and indoor enclosures where browse is provided), many bat species will crawl to the ground in search of green foliage.
6. Documentation
ENDNOTES (for Nutrition section 3.1 adapted from Nutrition Advisory Group Handbook)
1 Ammerman, C.B., D.H. Baker, and A.J. Lewis (eds.). 1995. Bioavailability of Nutrients for Animals. Academic Press, San Diego, CA.
2 Ange, K.D., S. Rhodes, and S.D. Crissey. 2001. Browse consumption and preference in the Rodriguez fruit bat (Pteropus rodricensis). AAZK Animal Keepers’ Forum 28(12):475-482.
3 Ayaz K.M., E.C. Birney, and R. Jennes. 1976. Inability of bats to synthesize L-ascorbic acid. Nature 260:626-628.
4 Bonaccorso, F.J. 1978. Foraging and reproductive ecology in a Panamanian bat community. Bull. Florida State Mus. Biol. Sci. 24:359-408.
5 Bonaccorso, F.J., and S.R. Humphrey. 1979. Population and community ecology. Pp. 409-441 in Baker, R.J., J.K. Jones, Jr., and D.C. Carter (eds.). Biology of Bats of the New World Family Phyllostomatidae, Part III. Mus. Texas Tech. Univ. Spec. Publ. 16.
6 Bradbury, J.W. 1977. Social organization and communication. Pp. 1-72 in Wimsatt, W.A. (ed.). Biology of Bats, Vol. III. Academic Press, New York, NY.
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8 Conklin, N.L., and R.W. Wrangham. 1994. The value of figs to a hind-gut fermenting frugivore: a nutritional analysis. Biochem. Sys. Ecol. 22(2):137-151
9 Conklin-Brittain, N.L., E.S. Dierenfeld, R.W. Wrangham, M. Norconk, and S.C. Silver. 1999. Chemical protein analysis: a comparison of kjeldahl crude protein and total protein ninhydrin using wild, tropical vegetation. J. Chem. Ecol. 25:2601-2622.
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58 Nowak, R.M. 1999. Order Chiroptera. Pp. 253-489 in Walker’s Mammals of the World, Vol. I. Johns Hopkins Univ. Press, Baltimore, MD.
59 O’Brien, T.G., M.F. Kinnaird, E.S. Dierenfeld, N.L. Conklin-Brittain, S.C. Silver, and R.W. Wrangham. 1998. What’s so special about figs: a pantropical mineral analysis. Nature 392:668.
60 Pennington, J.A.T., and H.N. Church (eds.). 1985. Bowes & Church’s: Food Values of Portions
Commonly Used, 14th Ed. J.B. Lippincott Company, Philadelphia, PA. Pp. 74-80, 209, 220.
61 Pope, B. 1998, Insectivory in Rodrigues Fruit Bats (Pteropus rodricensis) as an enrichment. P.3 in Pteropus (Bulletin no.4), Newsl. Lubee Foundation.
62 Rasweiler, J.J. 1986. American leaf-nosed bats. Pp. 638-644 in Fowler, M.E. (ed.). Zoo and Wild Animal Medicine, 2nd Ed. W.B. Saunders Company, Philadelphia, PA.
63 Reiter, J.L. 1993. The Intake of Captive Adult, Male Fruit Bats (Artibeus jamaicensis) Fed Diets of Differing Protein Content. M.S. Dissertation, University of Illinois at Chicago, Chicago, IL.
64Robbins, C.T. 1993. Wildlife Feeding and Nutrition, 2nd Ed. Academic Press, Inc., New York, NY.
65 Shanahan, M., S. So, S.G. Compton, and R. Corlett. 2001. Fig-eating by vertebrate frugivores: a global review. Biolog. Rev. 76:529-572.
66 Silver, S.C., L.E.T. Ostro, C.P. Yeager, and E.S. Dierenfeld. 2000. Phytochemical and mineral
components of foods consumed by black howler monkeys (Alouatta pigra) at two sites in Belize. Zoo Biol. 19:95-109.
67 Stellar, D.C. 1986. The dietary energy and nitrogen requirements of the grey-headed flying fox
Pteropus poliocephalus (Megachiroptera). Aust. J. Zool. 34:339-349.
68 Stevens, C.E., and I.D. Hume. 1995. The mammalian gastrointestinal tract. Pp. 55-58 in Comparative Physiology of the Vertebrate Digestive System, 2nd Ed. Cambridge University Press, New York, NY.
69 Tedman, R.A., and L.S. Hall. 1985. The morphology of the gastrointestinal tract and food transit time in the fruit bats Pteropus alecto and P. poliocephalus (Megachiroptera). Aust. J. Zool. 33:625-640.
70 Thomas, D.W. 1984. Fruit intake and energy budgets of frugivorous bats. Physiol. Zool. 57:457-467.
71 Toddes, B., and J. Trupkiewicz. 2001. Personal communication.
72 Ullrey, D.E., and M.E. Allen. 1986. Principles of zoo animal nutrition. Pp. 516-532 in Fowler, M.E. (ed.). Zoo and Wild Animal Medicine, 2nd Ed. W.B. Saunders Company, Philadelphia, PA.
73 United States Department of Agriculture. 1975. Composition of Foods. Agricultural Handbook No.8. U.S. Dept of Agric., Washington, DC.
74 Wendeln, M.C., J.R. Runkle, and E.K.V. Kalko. 2000. Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32:489-501.
75 Westhuysen, J. van der. 1988. Haematology and iron status of the Egyptian fruit bat, Rousettus aegyptiacus. Comp. Biochem. Physiol. A. Comp. Physiol. 90:117-120.
76 Wilson, D.E. 1979. Reproductive patterns. Pp. 317-318 in Baker, R.J., J.K. Jones, Jr., and D.C. Carter (eds.). Biology of Bats of the New World Family Phyllostomatidae, Part III. Mus. Texas Tech. Univ. Spec. Publ. 16.
77 Wimsatt, W.A. 1986. Vampire bats. Pp. 644-649 in Fowler, M.E. (ed.). Zoo and Wild Animal Medicine, 2nd Ed. W.B. Saunders Company, Philadelphia, PA.
78 Zortea, M., and S.L. Mendez. 1993. Folivory in the big fruit-eating bat, Artibeus lituratus (Chiroptera, Phyllostomidae) in eastern Brazil. J. Trop. Ecol. 9:117-120.
ENDNOTES (for all other sections except Nutrition section 3.1)
1. Only two species, Pteropus poliocephalus and Rousettus aegyptiacus extend from tropical regions into cool temperate regions.
2. At least one zoo has reported bat deaths due to tracking powder (K. Whitman, pas. comm.).
3. Available from Valentine Incorporated. Phone: (800) GET STUFF
4. Netting is available from Endurance Net, Inc. PO Box 127, Roebling, NJ 08554; Phone (800) 808-6387; ; email: EnduranceNet@
5. For more information about CDC permits contact: Department of Health & Human Services, Public Health Service, Center for Disease Control, Office of Biosafety, Atlanta GA 30333. Phone: (404) 329-3883.
6. Microbat shipping information was provided by Dr. John J. Rasweiler, The New York Hospital -
Cornell Medical Center.
7. In addition, if an animal is not adapting to captivity, the possibility of releasing them remains.
8. Ideally, samples should be collected from individuals. In large collections, however, a survey sample number of specimens should be collected.
9. Lethargy and reluctance to move can also be caused by torpor, which is normal for chiropterans.
10. Many factors affect heart rate. It is necessary to calculate respiration for each species. Both heart rate and respiration vary with body size.
11. Gauntlet gloves & capture equipment can be obtained through Fuhrman Diversified, 2912 Bayport Blvd., Seabrook, TX 77586-1501. Phone: (281) 474-1388; email: fdi@
12. It is impractical to attempt to examine neonates of large colonies. In addition, it may lead to mother bats abandoning their infants. This process should only be undertaken when deemed necessary in order to gather specific scientific data for a research program.
13. In addition, some researchers believe that Pteropus pumilus may show lek behavior (R. Spears, pen. comm.). However, there is little evidence to support this claim.
14. Some fruit bat rehabilitators believe that soy-based milk can be lethal to flying foxes (H. Luckoff, pers. corn.)
15. Additional information can be obtained by writing to Susan Barnard, 6146 Fieldcrest Dr. Morrow, GA 30260; Helen George, Wombaroo Food Products, ass Vale Road, Beaumont, Australia 2577. Phone: (044) 65- 1328 and/or Helen Luckhoff, 52 Cardiff Road, Darru, Queensland, Australia 4076.
Teats for handrearing flying foxes can be obtained from: S. Grzegorski, Australian Wildlife Teats, 60 Sutherland St., Calliope, Australia, 4680.
16. Trovan transponders can be obtained by contacting Infopet Identification Systems, Inc., 415 W. Travelers Trail, Burnsville, MN 55337, Phone: (612) 890-2080.
AVID transponders can be obtained by contacting AVID Identification Systems, Inc., 3185 Hamner Ave, Norco, CA 92860-1983, Phone: (951) 371-7505
17. One recommended brand is L&M Bird Leg Bands, Inc. PO Box 2636, San Bernadino, CA 92406, Phone: (909) 882-4649; another is Gey Band & Tag Co, Inc. (now National Band & Tag Co.) PO Box 72430, Newport, KY 41072-0430; Phone: (859) 261-2035; email: tags@; another is A.C. Hughes, 1 High Street, Hampton Hill, Greater London TW12 lNA, U.K. Phone: (081) 797- 1366.
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Definitions
Animal welfare:
The degree to which an animal can cope with challenges in its environment as determined by a combination of measures of health (including pre-clinical physiological responses) and measures of psychological well-being:
• Good health represents the absence of diseases or physical and physiological conditions that result (directly or indirectly) from inadequate nutrition social conditions, or other environmental conditions to which an animal fails to cope successfully.
• Psychological well-being is dependent on there being the opportunity for animals to perform strongly motivated behaviours, especially those that arise in response to aversive stimuli.
• Enhanced psychological well-being is conditional on the choices animal have to respond appropriately to variable environmental conditions, physiological states, developmental stages and social situations, and the extent to which they can develop and use their cognitive abilities.
Stress:
a) A non-specific response of the body to any demand made on it; b) an environmental effect that is likely to or does reduce the Darwinian fitness of the organism; c) the alarm system in a homeostatic organism, d) a cumulative response, the result of an animal’s interaction with its environment.
Eustress:
The outcome when a stressor is met by effective coping strategies and transformed thereby from distress (negative) to eustress (positive).
Distress. The state of being unable to defend against or control effects of an acute or chronic environmental stressor. A stressor may be either physical or emotional.
Suggested Readings
Beckoff, M., ed. 1998 Encyclopedia of Animal Rights and Animal Welfare. Greenwood Press, Westport, Conneticut.
Gibbons, Edward F., Jr., Barbara S. Durrant, and Jack Demarest, eds. 1995. Conservation of Endangered Species in Captivity: An Interdisciplinary Approach. State University of New York Press, Albany, New York.
Kleiman, Devra G., Mary E. Allen, Katerina V. Thompson, Susan Lumpkin, eds. 1996 Wild Mammals in Captivity: Principles and Techniques. University of Chicago Press, Chicago, Illinois.
Moller, Anders P., Manfred Milinski, Peter J. B. Slater, eds. 1998. Stress and Behavior, Advances in the Study of Behavior, vol. 27. Academic Press, San Diego, California.
Norton, Bryan G., Michael Hutchins, Elizabeth F. Stevens, and Terry L. Maple, eds. 1995. Ethics on the Ark. Smithsonian Institution Press, Washington, D. C.
Shepherdson, David J., Jill D. Mellen, Michael Hutchins, eds. 1999. Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, D. C.
Stanford, S. Clare, Peter Salmon, eds. 1993. Stress: From Synapse to Syndrome. Academic Press, San Diego, California.
Veterinary Standards Committee, American Association of Zoo Veterinarians. 1999. Guidelines for Zoo and Aquarium Veterinary Medical Programs and Animal Hospitals.
APPENDIX A
Need to Update: List of Participants
1994 &/or 1995 AZA Chiropteran TAG Mid-year Meetings
The Lubee Foundation, Gainesville, Florida
Keith Atkinson, The Lubee Foundation
Bruce Bohmke, Phoenix Zoo
Bruce Brewer, Brookfield Zoo
Bryan Carroll, Jersey Wildlife Preservation Trust
Michel Delorme, Biodome De Montreal
Jan Dempsey, St. Louis Zoo
Ellen Dierenfeld, Wildlife Conservation Park/ Bronx Zoo
Nina Fascione, Defenders of Wildlife
Adriana Galindo, University of Florida
Tim Gross, University of Florida
Roger Haagenson, Lubee Foundation
Darryl Heard, University of Florida
Scott Heinrichs, Lincoln Park Zoo
Karen Killmar, San Diego Zoo
Tom Kunz, Boston University
Norma Lewis, Birmingham Zoo
Dan Moms, Omaha's Henry Door1 y Zoo
Terry O’Connor, Woodland Park Zoo
Dennis Pate, Metro Washington Park Zoo
Harry Reeve, Busch Gardens Tampa
Peter Riger, Wildlife Conservation Park/Bronx Zoo
Alan Rost, Jacksonville Zoo
John Seyjagat, The Lubee Foundation
Kim Tropea, The Wildlife Conservation Park/Bronx Zoo
Kim Whitman, Philadelphia Zoological Garden
Steven Wing, Folsom Children's Zoo
Roland Wirth, Munchen, Germany
Husbandry Manual Editors (in addition to those at the TAG Meetings):
Sue Barnard, Zoo Atlanta
Sue Crissey, Brookfield Zoo
Brock Fenton, York University
Peter Myroniuk, Melbourne Zoo
Dominic Wormell, Jersey Wildlife Preservation Trust
Janette Young, Jersey Wildlife Preservation Trust
APPENDIX B
PARTIAL ETHOGRAM OF BAT BEHAVIORS
(from Carroll, 1979)
Autogrooming: licking or nibbling the fur or scratching with one hind foot. Forelimbs are not used in grooming.
Allogrooming: seen quite frequently among all sex/age classes, although adult males confine allogrooming to adult females. Involves groomer licking groomee's fur.
Hanging Alert: animal is hanging stationary, but is awake and alert.
Play Chase: seen among immature. Two or more animals fly from one location to another and rapidly leave again.
Play Wrestle: usually seen among immatures. Involves close ventral contact between individuals while giving inhibited bites to neck area of the other animal. More than two animals may be involved.
Roosting: animal is asleep, suspended by one or both feet from a perch.
Scent Marking: rubbing neck and chin glands against perches or the walls of cage. Seen most frequently in adult males.
Static Flying: flapping the wings as if to fly but retaining hold of the perch with the feet. Seen mainly among infants who cannot yet fly.
Walking on the Ground: animal will descend to ground to search for fallen food. Limb sequence is typical for quadrupedal gait and claw of the thumb is used to pull the animal along. While is may be difficult for some species, bats can take off from the ground.
Wing Fan: seen during hanging alert. Is a gentle fanning with half-folded wing, may be thermoregulatory.
Wing Shake: aggressive action. One or both wings held with arms outstretched from the body. Wings shaken with thumb pointing at addressee. Claw can be used in physical encounters and is capable of inflicting injury.
Wing Flick: short flick of the distal half of wing achieved by moving the digits. Seen sometimes during courtship by males.
APPENDIX C
[pic]
Shipping Container: Vari-Kennek (Doskocil) with a wire mesh cage
Large- Pteropus vampyrus (39”L x 26.5”W x 28.5”H)
Medium- Pteropus rodricensis (27”L x 20”W x 19”H)
Small- (19”L x 12”W x 10”H)
[pic]
APPENDIX E [pic][pic]
APPENDIX F
Partial List of Forages Accepted by Captive Colonies of Fruit Bats
alder
ash
aspen
bamboo
banana
beech
black locust
box elder
crabapple
dogwoods
elm
ficus
forsythia
grape
hackberry
honeysuckle (Japanese)
Kentucky coffee tree
kudzu
mangrove (Florida)
maple (not red)**
mulberry (not red)
ornamental pear
poplar (not tulip poplar)
sweetgum
torch ginger
** Although red maple has been fed in some institutions, there have been reports of health incidents possibly related to the ingestion of red maple. Therefore, it is not recommended.
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