Department of Pathology, National Zoological Park
The author is an animal records technician.
Exudativory, or the use of plant gums, saps, resins and occasionally latex as a food source in an animal's diet, has been increasingly documented by field studies performed during the past 40 years (Nash, 1986) (Figure 1). Animals known to eat plant exudates are found among the prosimians, marmosets, tamarins, squirrels, marsupials, old world primates, and birds (Fleagle, 1988; MacDonald, 1984; Post, 1983; Rylands, 1984; Smith, 1982; Wrangham, 1981; Bearder, et al., 1980; Charles-Dominique, 1977; Hausfater, et al. 1976; Izawa, 1975; Kilham, 1975; Tate, 1973; Radman, 1969). A literature search done in 1990 resulted in documentation of exudate-feeding in 45 species of animals (see table 1). However, the degree of dependency of animals on this food source is variable. For example, plant exudates are the major component of the natural diet of the Pygmy marmoset (Cebuella pygmaea) (Fleagle, 1988; Hershkovitz, 1977; Nash, 1986), Fork-marked lemur (Phaner furcifer) and other prosimians (Charles-Dominique, 1980; Oxnard, et al., 1990). These animals are considered pr imary gum-feeders based on their morphological, anatomical, physiological, and behavioral adaptations (Fleagle, 1988). Secondary gum-feeders are species that feed on plant exudates as a response to decreased fruit and flower availability, or climatic changes such as wet or dry seasons. Another factor that influences the degree to which animals rely on plant exudates is whether these exudate sources are water stressed, which results in low exudate production (Garber, 1984a; Nash, 1986; Lacher, et al., 1984). Exudate use also includes animals that ingest them opportunistically when they are found and animals that ingest exudates coincidentally when they eat, or perforate, bark down to the cambium layer during insect- or browse-feeding.
Fig. 1. Black-tailed marmoset licking gum that is
dripping down a tree limb. (Photo by Lee Miller)
Between March 1988 and September 1990, I was a member of a behavioral research project at the Small Mammal House, National Zoological Park (NZP), Washington, D.C. Our objective was to apply the information, documented by field research about gummivory, to the captive management of our Pygmy marmosets, Black-tailed marmosets (Callithrix argentata melanura), and Geoffrey's marmosets (C. geoffroyi). We also offered gum arabic to other animals in the collection such as Lion tamarins (Leontopithecus spp.), Goeldi's monkey (Callimico goeldi), Low's squirrel (Sundasciurus lowi), Sugar gliders (Petarus breviceps), Prevost's squirrels (Callisciurus prevosti), and Cuban hutias (Capromys pilorides). All of these animals, except for the Sugar gliders, were on exhibit during our study. Since our experience is with gum-feeding, I will use the term gummivory, or gum-feeding, to be synonymous with the term exudativory. The following information presents the results of our research experiences, gained knowledge, and the unexpected side benefits we obtained from simulating gummivory in captivity.
Generally, animals that use plant exudates are small bodied, have a high metabolism, and are incapable of storing large amounts of fat. Primary gum-eaters have most, or all, of the following traits: small body size, clawed digits (for vertical clinging at gum sources), long procumbent or semi-procumbent incisors complimented by short lower canines (providing a level gouging/scrapping surface), loss of enamel on the lingual side of the lower incisors complimented by honing upper incisors (providing a sharpening effect that permits gouging or scraping abilities), a V-shaped configuration of the mandibular arch, a long tongue (to reach gums within the plant bark), and an enlarged cecum (to allow for fermentation of the gums) (Fleagle, 1988; Coimbra-Filho, et al., 1978; Rosenberger, 1978; Hershkovitz, 1977).
Gums are a high-energy food source composed mainly of water, complex polysaccharides, calcium, and trace minerals (iron, aluminum, silicon, potassium, magnesium, and sodium) (Nash, 1986). Calcium is important to all animals, especially female callitrichids (tamarins and marmosets) which commonly give birth to twins twice a year. It is during the lactation period that the females are usually impregnated by the male. Therefore, they are developing fetuses while nursing their fast-growing infants, resulting in an increased calcium demand. The calcium-to-phosphorus ratio is high in gums which offsets its ratio in insects, which is low. Because all known wild gummivores also include insects in their diet, combining the two, in captivity, may approach a desired nutritional balance and is recommended to avoid the possibility of nitrogen loss and the loss of protein from the body (Nash, 1986; Garber, 1984a; Sussman, et al., 1984; Coimbra-Filho, et al., 1978; Moynihan 1976).
Gums from woody plants are reportedly available year round and are constant in their location (Bouchardet de Fonseca, et al., 1984; Ramirez, et al., 1978). This aspect allows marmosets, which are capable of eliciting gum flow, to be non-seasonal breeders and to subsist in small home ranges. Some tamarin species have been noted by field researchers to travel in association with marmosets and parasitize their gum sites.
It has been suggested that gums are an integral link in the food chain of gummivores (Soini, 1982). Some insects (moths, butterflies, ants) are attracted to the gum sites, while other insects simply get stuck in the sticky substance. These insects are often preyed upon by lizards and frogs. Gum-eaters prey on all of these animals, which reduces the amount of time and energy exerted in procuring animal protein in their diet. Gum-feeding typically occurs at the lower levels of the forest canopy (about 3 meters from the ground) where fruits and flowers are usually absent (Ramirez, 1978; Moynihan, 1976). The ability to subsist at this level lessens competition with other forest animals, which are predominantly frugivores or foliavores (Fleagle, 1988).
Gum-feeding is more than just another feeding strategy. It is the merging of the nutritional, ecological, behavioral, and evolutionary traits which allows species that are capable of using this resource to coexist in the wild.
Captive marmosets will instinctively gouge holes in exhibit furniture, despite the fact that they do not receive a food reward. Offspring of captive-born parents also gouge wood throughout their lives. The instinct to retain this behavior is so strong that infant marmosets in captivity demonstrate substrate "mouthing" behavior the prerequisite to gouging behavior as early as 3 weeks of age in Pygmy marmosets and at 5 weeks in Black-tailed marmosets (person. observ.).
In 1988, we began our research project by offering gum-feeders based upon McGrew's suggested artificial gum-feeder for marmosets (McGrew, 1986). These gum-feeders consisted of eight dowel segments with four drilled-out circular cavities (gum reservoirs) that were stacked onto a threaded, metal rod, secured with wing nuts, and wired onto the existing cage furniture. The marmosets not only accepted and fed from these gum-feeders, but became possessive of them when replacement was needed. Although the artificial feeders functioned, there were technical drawbacks. They required shop fabrication and needed to be soaked in water weekly because the dowel was very hard and dry. They were also unnatural in appearance, time-consuming to fill (filling with gum, feeder assembly, and installation of four feeders took approximately 2.5 hours per day), and they required weekly replacement. We abandoned this type of gum-feeder after 2 months and substituted natural branches for the dowel (gum reservoirs were simply holes drilled into the branch). Not only was this type of feeder accepted but it served as additional cage furniture that functioned as pathways and perches for the animals. This type of feeder provides the animals with a naturally textured substrate, is readily obtained, requires no assembly, and if hard wood is used, needs less frequent replacement (our hard wood feeders have been in place for 5 years). Filling these feeders can be accomplished in 5 to 10 minutes (Peterson, et al., 1988).
The following year we expanded the natural-branch idea to the use of floor-to-ceiling-length tree limbs, oriented in vertical and diagonal positions (Figure 2). This additional length of the feeders allowed us to provide eight feeding sites (gum reservoirs) in three locations on each feeder near the top, in the middle, and near the bottom.
Fig. 2. Black-tailed marmoset waiting for the keeper to
fill holes on tree limb with gum arabic. (Photo by Lee Miller)
Using checksheets and 45 trained volunteer behavior watchers, we observed for signs of differences in vertical versus diagonal preference, hard wood versus soft wood feeders, and preference of depth and dimension of drilled holes.
We also experimented with presenting the gum arabic/water solution in a rodent water bottle with a sipper tube (do not use tubes with a ball-bearing). We offered this modified gum-feeder in three ways: 1) inserted through one of our feeders, with the stem protruding; 2) hidden inside a piece of cork bark, with the stem protruding; and 3) affixed directly onto the wiring of a holding cage. The third method could be used for an animal that has been separated for health reasons or because of preshipment. It could also be used for enrichment in a laboratory situation where individual housing may be necessary for compliance with research protocol. Our objective was to make the gum available ad libitum, in hopes that the marmosets would teach us how often they use it.
Data analysis (850 observation hours) revealed that the Pygmy marmosets (1.1.2, 1.1, 1.1) [Ed. Note: the first digit indicates the number of male animals, the second digit indicates the number of females, and the third, if present, indicates that the sex is unknown] used all gum sites on all feeders provided to them regardless of position, type of wood, or depth and dimension of drilled gum holes. The Black-tailed marmosets (1.1.2) demonstrated a preference for gum sites that were mid to upper level on vertical feeders. The Geoffrey's marmosets (1.1) used all feeders and feeding sites provided to them regardless of orientation, type of wood, or hole dimension.
The Pygmy marmosets shared feeders and even feeding sites without conflict. Over time, the Black-tailed marmosets became territorial over the feeders and a pronounced hierarchy system emerged within the family. The male Geoffrey's marmoset hung back and allowed the female first access to the gum sites. This behavior has been documented in some species of wild prosimians (Charles-Dominique, 1977).
One observation consistent among our marmoset species was that the use of soft wood feeders stimulated more scent marking and gouging behavior which resulted in marked damage to the feeders as well as to the existing cage furniture.
By providing gum feeders in vertical and diagonal orientations, we had unintentionally provided the marmosets with the opportunity to employ their widely recognized abilities as vertical clingers and leapers. When eating gum from the feeders, the marmosets often fed from an upside-down, clinging position a posture not seen at other times. Gouging on feeders and eating gum from them required the marmosets to use muscles that are not used when locomoting quadrupedally on horizontal vines and branches the typical exhibit furnishings provided in captive settings (Newman, et al., 1990; Garber, 1984b).
1.) Increased animal activity level: The marmosets immediately come down to the feeders while the keeper is injecting the gum into the drilled holes via a syringe. They would also return to the feeders, at various times in the day, to scrape off and eat the dried gum overflow that adhered to the feeders' bark. This replicates the feeding pattern of their counterparts in the wild (Fleagle, 1988).
2.) Increased animal visibility: The Pygmy marmosets in all three exhibits will come within 2-3 inches of a caretaker while the gum is injected into the drilled holes, while the four Black-tailed marmosets and both Geoffrey's marmosets will eagerly eat the gum arabic directly from a syringe (Newman, et al., 1990). This simplifies the task of performing daily head counts of these animals.
3.) Close proximity to exhibit animals allows for health observations: Since the marmosets either eat the gum directly from a hand-held syringe or come within inches of the caretaker, we have been able to detect early signs of pregnancy and detect and monitor minor injuries (cuts, scratches) and dental problems that do not require immediate treatment. We used the gum-filled syringe to encourage our young Black-tailed marmosets to stretch out for sex confirmation. We also used the gum-filled syringe to administer antibiotics to our adult, female Black-tailed marmoset who was diagnosed with a flagyl parasite infection (Figure 3). She refused her medication, even when hidden in her favorite food items, but accepted it when it was mixed into the gum arabic solution (Kelly, et al., 1989) and offered to her in the familiar syringe. Feeding gum arabic has proven to be a useful tool for animal caretakers to keep abreast of their animals' general health. The aspects of close proximity to the animals with its resulting observational benefits can be performed without physical manipulation or stress to the animals (Newman, et al., 1990).
Fig. 3. A female Black-tailed marmoset is being given an
antibiotic gum arabic solution without being removed from
her family, who are watching the procedure. (Photo by Lee Miller)
4.) Visitor experience enhancement: Throughout our study, all of the gum-feeders were positioned near the public viewing side of each exhibit. The public responded to our gum-feeding project with interest and enthusiasm, and countless questions about the animals. It is exciting for zoo visitors to see a captive animal active and interacting with its environment. Other visitors appreciated the opportunity to get close-up photographs of the animals engaging in a natural behavior.
In the summer of 1989, we offered floor-to-ceiling-length wood feeders to a mixed bachelor group of Golden Lion tamarins (Leontopithecus rosalia) and Golden-headed Lion tamarins (L. r. chrysomelas) that were exhibited outdoors. The feeders became a source of interest and stimulation for the tamarins. Use of these feeders again illustrated species-specific behavior responses.
The Golden-headed Lion tamarins stripped off the bark over the gum sites to gain access to the gum that had been injected into the holes, whereas the Golden Lion tamarins were observed probing the gum-filled holes and then eating the gum from their fingers. The Golden-headed Lion tamarins also returned to the feeders later and stripped off additional bark from over the gum holes to gain access to any gum residue. At no time did we observe conflicts between the tamarin species over the gum (Kelly, et al., 1989).
When we injected the gum into a wide, circular depression on one of the feeders, both species of tamarins were observed using their cupped hand to scoop up the gum and eat it. This is the same method used in the wild to obtain rainwater from the cups of bromelids.
Our trial with Goeldi's monkey was limited to an individual female that was housed with our Black-tailed marmosets during our initial study in 1988. She did taste, and, on occasion, eat some of the gum, but she did not demonstrate strong attraction to it as did the marmosets and tamarins. We believe she was simply mimicking the Black-tail's responses to the gum. We have since learned that wild Goeldi's are not known to eat gums from woody plants, but do eat a sticky gum substance found on seed pods.
We were disappointed by our results with the Low's squirrel and the Sugar gliders. We offered a natural wood gum-feeder to a Low's squirrel and although the gum always disappeared, we never actually saw the squirrel using the feeder. It has been our experience that Low's squirrels are typically shy and secretive. The Sugar gliders (family group of five), however, stripped off large areas of bark from the feeders but ignored the gum sites. Further literature searches suggest they were probably searching for insects under the bark. Providing natural branches to Sugar gliders, even without gum, provides a stimulus to them which increases their activity level. Although both of these species are documented gum-eaters (MacDonald, 1984; Smith, 1982), the types of gum utilized by animals vary among species because of differences in geographic ranges and environmental factors. We used acacia gum extract in our trials which may not be the type of gum eaten by Low's squirrels and Sugar gliders.
One pair of Prevost squirrels in our study ate gum from the feeders as well as directly from the syringe. We do not place emphasis on their acceptance of the gum-feeders since this particular pair of squirrels were hand-raised and seek human interaction. The other pair of Prevost squirrels (parent-raised) in our study showed little-to-no interest in the gum or the feeders.
The responses of the Cuban hutias were surprising. Our four hutias were recently acquired, wild-caught animals. We do not have any documentation of gum-feeding in this species, but based on our theory that wood-eating species ingest gums, we offered the gum to them. The hutias, especially the females, ate the gum directly from the syringe but at no other time would they allow us close proximity to them. We have noticed that the females in all the trials, especially when pregnant, are usually the first animals to come for the gum.
Although we did not intentionally include Acouchis (Myopracta pratti) in our gum-acceptance trials, we learned that some acouchis will eat gum. The pair of acouchis housed in our mixed Geoffrey's and Pygmy marmoset exhibit began eating any gum that accidently landed on the floor. One of these acouchis would eat the gum directly from the syringe and would stand up on its hind legs, waiting to be fed the gum.
All of the above animals, except for the Low's squirrel and the Sugar gliders, would come surprisingly close to keepers feeding gum or they would accept hand-feeding via the syringe. This provided us with the same side benefits previously listed for the marmosets.
We also placed natural wood gum-feeders in some of our indoor mixed-species exhibits. The feeders became a source of interest and activity to the gum-eating species as well as to the non-gum-eating species. Curiosity was stimulated and intra- and inter-species activities resulted, thus creating a more interesting environment for the animals.
Our research project has shown that natural branch gum-feeders can be used to simulate gummivory in captivity for a variety of animals. Use of natural branches/tree limbs is an inexpensive, readily available, and low maintenance method of providing environmental enrichment in an artificial setting. Simulating gummivory in captivity can be accomplished with minimal time investment and energy demand on the part of animal caretakers.
Modern zoos are attempting to exhibit animals in naturalistic settings. Ideally, the goal should be to exhibit animals in a naturalistic setting that stimulates behavioral interactions between the animals and their environment. We feel our natural branch gum-feeders help accomplish this goal.
When captive environments lack stimulus, animals are deprived of the opportunity to engage in some of their natural behaviors, which may be replaced by atypical behaviors characterized by excessive inactivity, grooming, and/or sleeping (Schoenfield, 1989). Duplicating natural habitats as much as possible in captivity encourages animals to use their innate behaviors (Hancocks, 1980).
Having the opportunity to demonstrate their natural gum-foraging behavior stimulated some of the animal's other natural behaviors, i.e., compatible sharing of feeders and feeding sites (Pygmy marmosets), methods of food acquisition (marmosets and tamarins, Golden Lion tamarins and Golden-headed Lion tamarins), and territoriality and dominance (Black-tailed marmosets). Providing feeders allowed our captive animals to emulate, to some extent, the behaviors of their wild counterparts. Gum-feeders also served as a source of interest and entertainment for young marmosets (Shepardson 1989).
Providing natural wood gum-feeders to NZP animals resulted in: increased animal activity, increased animal visibility for record- keeping and general health observations, sexing of young animals, early detection of pregnancy, non-stressful medicating of sick animals, and detection and monitoring of minor injuries or dental disorders that do not require immediate medical attention (Figure 4).
Fig. 4. Hand-feeding gum via a syringe provides keepers with
the opportunity to closely examine animals and dispense
medication in a non-stressful manner. (Photo by Lee Miller)
Full-length feeders presented in vertical and diagonal orientations promote and compliment the locomotor abilities of known vertical clingers and leapers. Using the gum-feeders required the animals to use muscles that are not exercised during quadrupedal locomotion (Garber, 1984b). They provided the animals with the opportunity to assume postures not demonstrated prior to the introduction of the feeders, and they increased the amount of available, usable cage space. Simulating gummivory improved the condition of our animals and enhanced the interest and experience of our zoo visitors.
Providing interactive ways for captive animals to gain some control of their environment results in an aesthetic, interesting, potentially educational, and functionally useful exhibit. Attempts at environmental enrichment, such as simulating gummivory, could simultaneously be used to help visually demonstrate the evolutionary niche of various species while illustrating the need to conserve entire ecosystems as well as individual species.
This paper is dedicated to the memory of Yoda, a 4-year-old Black-tailed marmoset who was the catalyst for this research project.
|Prosimians:||Euticus elengatulus - Needle-clawed Galago |
Galago alleni - Allen's bushbaby
G. senegalensis - Senegal bushbaby
G. crassicaudatus - Thick-tailed bushbaby
Galagoides demidovii - Dwarf galago
Perodicticus potto - Potto
Lemur catta - Ring-tailed lemur
L. fulvus - Brown lemur
Microcebus murinus - Mouse lemur
Mirza coquereli - Coquerel's dwarf lemur
Phaner furcifer - Fork-marked lemur
Callithrix argentata melanura - Black-tailed marmoset |
C. a. aurita - Buffy tufted-ear marmoset
C. flaviceps - Buffy-headed marmoset
C. geoffroyi - Geoffrey's marmoset
C. humeralifer - Tassel-ear marmoset
C. jacchus - Common marmoset
C. j. pencillata - Black tufted ear marmoset
Cebuella pygmaea - Pygmy marmoset
|Tamarins:||Saguinus fuscicollis - Saddle-back tamarin |
S. imperator - Emperor tamarin
S. labiatus - Red-bellied tamarin
S. midas - Golden-handed tamarin
S. nigricollis - Black-mantle tamarin
S. oedipus - Cotton-topped tamarin
S. o. geoffroyi - Geoffrey's tamarin
|Squirrels:||Hylopetes spadiceus - Red-cheeked squirrel |
Microsceurus - Pygmy squirrel
Sciurus vulgaris - Red squirrel
Sundasciurus lowii - Low's squirrel
S. tenuis - Slender squirrel
|Old World Monkeys:||Cercopithecus aethiops - Vervet monkey |
Erythrocebus patas - Patas monkey
Papio c. cynocephalus - Yellow baboon
Macaca sylvanus - Barbary macaque
Pan troglodytes - Chimpanzee
|Marsupials:||Gymnobelideus leadbeateri - Leadbeater's possum|
Petaurus australis - Yellow bellied glider
P. breviceps - Sugar glider
|Other Mammals:||Ursus americanus - Black bear |
Loxodonta africana - African elephant (in Amboseli)
|Birds:||Artideotis kori - Kori bustard |
Coua cristata - Crested coua (Madagascar)
Sphyrapicus varius - Yellow-bellied sapsucker
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