The giant anteater (Myrmecophaga tridactyla) is one of the most distinctive animals of South America. In northern Argentina it is found in forests, savannahs, and grasslands. It is listed as Vulnerable in the IUCN Red List of Threatened Species. The present study was conceived as a husbandry tool for individuals of this species in zoos. The research was developed at CRET (Temaikèn Center of Species Reproduction) and consisted in elaborating the behavioral repertoire of a group of three adult females from April 2009 to April 2010. A total of 122 h of behavioral observations were made by the naked eye at a distance of 1–5 m through a metallic mesh, five times a week, with focal animal ad libitum sampling from 9:00 to 18:00 hr. A diagram of the exhibit was confected to ease the data collecting process. To facilitate the description of the behavioral acts, an identification of the different physical characteristics of each individual was conducted along with the segmentation of the body. During the 12 months of observations, 38 behavioral acts were defined, which were then grouped into eleven categories. Finalization of data collection was based on the saturation curve; the first asymptote was reached at 35 h, while the final one, which remained constant, was reached at 52 h and contained the 38 behavioral acts registered in the ethogram.
INTRODUCTION
Ethology is traditionally known as the study of natural animal behavior. Martin & Bateson (1986) specifically define the purpose of ethology as the study of the biological function of behavior, in the attempt to understand the purpose of behavior in its natural context. Lorenz (1993) discusses the significance of field and captive studies arguing that the comparison between the two is one of the basic tools of ethology, as stimuli are reduced and, therefore, some behaviors will be missing in captive conditions. Furthermore, an elevated threshold exists in captivity, meaning that more stimuli will be needed to trigger a specific behavior. Thus in captivity behaviors may be missing, but no behaviors will appear that do not already occur in nature.
Ethology can also provide key information for designing appropriate enclosures, since to study an animal, is actually to study a portion of nature that was separated from its environment. Lorenz (1993) recommends to never undertake a study without knowing the ethogram of the species and basic information on its ecology. Any project that involves the captive maintenance of animal groups should assign part of its resources to structuring an ethogram.
About the ethogram
Fagen (1978) defines a behavioral repertoire as a group of mutually exclusive and collectively exhaustive acts of an animal or species. Laffitte de Mosera & Caprio (1980) define ethogram as a precise description of animal activity, meaning a thorough description of the observable behaviors in the animal that constitutes the initial phase (observation) of the ethological method.
For Lehner (2003) an ethogram is a group of wide descriptions of the behavioral patterns characteristic of a species. This author clarifies that it is the result of many hours of observations, in some cases of sound recordings, and descriptions, and that it must be the starting point of any ethological research. According to Lehner (2003) the questions that an ethologist tries to answer about the behavior are: what happens (description), when does it happen (temporal component), how (motor patterns), and why (motivational and ecological adaptation of behavior). Martin & Bateson (1986) define it as a catalog of descriptions of discrete behavioral patterns, typical of the species-object, that form the basic behavioral repertoire of the species.
In all cases, the following characteristics should be highlighted:
The elaboration sequence
An ethogram is a list of acts of behavior, it is what the observer considers implied in what he is observing (Lahitte et al., 1993). Since an act of behavior comes from a specimen-environment relationship, the inventory of behavioral acts is consequently a list of the different ways that the observed specimens relate to one another and with their environment. The procedure is to observe and record, after the reading and analysis of those records, a description of the behavioral acts is elaborated, they are then grouped by affinities, differences, functionality, structure, etc. For each category of records, a group of acts can be defined that covers and summarizes them. When the observations that originated the records are presumed complete, meaning such an outlook that more observation time will not add records that do not fall into any of the already defined acts, then it is considered that the list of definitions is an ethogram, a complete list of behaviors of that species. Once this list of behaviors is completed, it remains incorporated into the conceptual framework and it starts being employed as a tool.
Having concluded this introduction, and with the ethological framework established, an ethogram is presented of the giant anteater (Myrmecophaga tridactyla) in captivity, conceived as a tool for the management of individuals of this species in zoos. The giant anteater is one of the most distinctive animals of South America. It has been recorded from Honduras in Central America, south through South America to the Gran Chaco region of Bolivia, Paraguay, and Argentina (Superina et al., 2010). In Argentina its geographical range has been diminishing within the last century, being found presently in the forests of the province of Misiones, savannahs, grasslands, and forests of Formosa and Chaco, and in the woods of the drier Chacoan region including the east of Salta, Jujuy, and north of Santiago del Estero (Pérez Jimeno & Llarín Amaya, 2007; Pautasso et al., 2009). In Argentina the species is categorized as In Danger (EN, in Spanish EP) (Díaz & Ojeda, 2000), and globally it is considered as Vulnerable (Miranda & Medri, 2010).
Myrmecophaga tridactyla is locally uncommon to rare. Habitat loss, roadkills, and wildfires are substantially affecting the wild populations and have led to a continuing decline in mature individuals (Superina et al., 2010).
MATERIALS AND METHODS
The present study was conceived as a husbandry tool for individuals of this species in zoos. The research was developed at CRET (Temaikèn Center of Species Reproduction), and consisted in elaborating the behavioral repertoire of a group of three adult females from April 2009 to April 2010, including a full year cycle of climatic seasons. A total of 122 h of behavioral observations were made by the naked eye at a distance of 1–5 m through a metallic mesh, five times a week (Monday—Friday), four times a day with focal animal ad libitum sampling (Altmann, 1974), during 12 months from 9:00 to 18:00 hs. A diagram of the exhibit (FlG. 1) was confected and divided into sections to ease the data collecting process during the observations. To facilitate the description of the behavioral acts, a description of the different physical characteristics of each individual was conducted along with the segmentation of the body to identify them (FlG. 2). A climatic description was used as a reference applied in the observations.
FIGURE1.
Diagram of the exhibit where the giant anteaters (Myrmecophaga tridactyla) were housed during the study. A reference scale, keys, dimensions, and sections are provided.
The three females were differentiated by fur color, size, and the difference in the anteaters' characteristic diagonal shoulder stripe in their fur, which is on both lateral sides of the torso. One of the females had lighter brown colored fur and the diagonal stripes were less defined. The second female had darker black fur and the diagonal stripes were more defined. The third female was larger in size, with brown fur, and presented defined diagonal stripes; also, her tail was longer than average.
Finalization of data collection was based on the saturation curve (Lehner, 2003) which consists of creating a graph showing the number of observed behaviors versus the number of observations until an asymptote is reached. When a constant asymptote is reached, more observations will not show new behavioral acts; this implies that even if the data collection is expanded, the observed behaviors will still be applicable to the same group of behavioral descriptions already found.
RESULTS
Displacement of the body segments
As shown in TABLE 1, the body segments were divided into head, torso, tail, and anterior and posterior limbs, and their displacement was described vertically and horizontally.
Behavior
During the 12 months of observations, 38 behavioral acts were defined, which were then grouped into 11 behavioral categories described in TABLE 2. A description of all specific behaviors recorded during the behavioral observation sessions are shown in the behavioral ethogram in TABLE 3. All behaviors were coded for frequency (total number of occurrences).
TABLE 1.
Description of the displacement of the giant anteaters' (Myrmecophaga tridactyla) body. The body is segmented into head, torso, tail, and anterior and posterior limbs. The displacements are described both vertically and horizontally.
TABLE 2.
Description of the 11 behavioral categories that include the 38 specific behaviors observed in giant anteaters (Myrmecophaga tridactyla).
TABLE 3.
Description of each specific behavior recorded during the behavioral observation sessions in giant anteaters (Myrmecophaga tridactyla). Each behavioral act is listed within its behavioral category and has been coded.
CONTINUED
CONTINUED
FIGURE3.
Giant anteater (Myrmecophaga tridactyla) standing with all four limbs on the ground, with both head and tail in the same longitudinal axis as the torso.
FIGURE4.
Giant anteater (Myrmecophaga tridactyla) sitting and interacting with enrichment object, with both anterior limbs extended and posterior limbs flexed.
FIGURE5.
Giant anteater (Myrmecophaga tridactyla) laying, the tail covers the body, the head is lifted from the ground, and the eyes are open.
FIGURE6.
Giant anteater (Myrmecophaga tridactyla) investigating in the vegetation, the snout is touching the substrate.
FIGURE7.
Giant anteater (Myrmecophaga tridactyla) sniffing tree logs, the head is tilted below the longitudinal body axis and reaches the logs with its snout.
FIGURE8.
Giant anteater (Myrmecophaga tridactyla) digging the ground with its claws. One anterior limb digs while the animal introduces its tongue in the hole it created.
FIGURE9.
Giant anteater (Myrmecophaga tridactyla) eating from an enrichment nutrient source, the snout is in contact with the nutritional source and the tongue is seen.
FIGURE10.
Giant anteater (Myrmecophaga tridactyla) eating from an enrichment termite mound. The head is above the longitudinal body axis and the snout is in contact with the nutritional source.
FIGURE11.
Giant anteater (Myrmecophaga tridactyla) scratching its back. The animal is in a sitting position using one anterior limb to scratch itself and the other anterior limb to support its body weight.
Data collected
FIGURE 15 shows the number of new and accumulated behaviors versus the number of observation sessions. The first asymptote was reached at 35 h, there was a second one at 46 h, and the final asymptote, which remained constant, was reached at 52 h and contained the 38 behavioral acts registered in the ethogram.
There were many changes in the behavior of the females throughout the seasonal changes. The investigative and feeding behavior increased during the rainy season and on average, the anteaters were most active during the afternoons versus in the mornings. The heat of the summer with 30–35 °C was when the anteaters were most active. The captive facility where this research was conducted is outside the giant anteater' s natural distribution, which possibly affected the behaviors the animals displayed.
DISCUSSION
Little background information was available on the specimens used in this research. They were born in the wild and then donated to the Temaikèn Foundation. This lack of background information brings forth a discussion regarding the variations between behaviors in the wild and in captivity. For example, in this study the only laying behavior observed was with the tail folded over the body when sleeping, which helps the anteater conserve the body heat generated by its metabolism and also serves to camouflage the sleeping animal (Shaw & Carter, 1980).
However, observations in natural habitats indicate variations of this behavior depending on ambient temperature (Medri & Mourão, 2005). In a large number of sightings (n=107), giant anteaters were found sleeping with their bushy tails covering their bodies even on days when the temperature exceeded 30 °C, while on a cool sunny morning, when ambient temperature was about 17 °C, the giant anteater was sleeping stretched out flat on the ground exposing the full length of its body to sunlight, a behavior that suggests it was using solar radiation as a source of heat to raise its body temperature (Medri & Mourão, 2005).
FIGURE14.
Giant anteater (Myrmecophaga tridactyla) playing with an enrichment object. The animal is laying on the ground while manipulating the object with its anterior limbs and holding it in place with its posterior limb.
Another finding that shows the variations of giant anteater behavior is the bathing habit. In this research, the animals used the pool to bathe and also enjoyed being hosed down by their keepers as a part of their enrichment. In the wild, bathing in water is rare in mammals that are not semi-aquatic and giant anteaters do not share the physical characteristics of other bathing mammals. However, Emmons et al. (2004) acquired over 70 photos with a camera trap of giant anteaters coming to a watering hole in Parque Nacional Noel Kempff Mercado in Santa Cruz, Bolivia. The photos showed many anteaters arriving dry, then leaving the hole soaking wet (Emmons et al., 2004).
There has been much dispute regarding the climbing behavior of giant anteaters. In this study this specific behavior was only recorded when the animal was motivated to climb with the use of food type enrichment. This behavior was described by the observations of Young et al. (2003), where the ability of both captive and wild giant anteaters to climb termite mounds, trees, and man-made objects was fully described. In both studies, the conclusion reached is that a sufficiently hungry or motivated giant anteater will display the climbing abilities needed to obtain certain goals, such as food.
FIGURE15.
Chart showing the number of new behaviors / accumulated behaviors observed in giant anteaters (Myrmecophaga tridactyla) versus the number of observation sessions. The first asymptote was reached at 35 h, there was a second one at 46 h, and the final asymptote, which remained constant, was reached at 52 h and contained the 38 behavioral acts registered in the ethogram.
Agonistic behaviors recorded in this research and others in captivity seem to be less violent and do not end with serious injuries, as opposed to the fighting behavior that occurs in the wild and which has been described in the scientific literature (Shaw et al. 1987; Rocha & Mourão, 2006; Kreutz et al., 2009). However, some of the aggressive behaviors seen in this study could be associated with reproductive periods when comparing these behaviors with those found in the work of Astwood Romero et al. (2010). Although the study performed by Astwood Romero et al. (2010) is about courtship and mating behaviors of giant anteaters in ex situ conditions, it also includes a basic ethogram with some of the same behaviors recorded in this study, such as climbing, sleeping, smelling, rubbing, running, following, turning, eating, and grooming. The agonistic behaviors displayed by these three females seem to fit some of the courting descriptions of Astwood Romero et al. (2010), and may in fact be a part of a misdirected courtship attempt.
CONCLUSIONS
The results described here are useful for the husbandry of giant anteaters in captivity in order to achieve their welfare. The zookeepers of these animals now have a better understanding of them, accomplishing the goal of this study.
Accomplishing a good management of animal behavior is of utmost importance because it results in sanitary treatments, veterinarian interventions, and handling with higher probabilities of success. This study has helped improve the training techniques used by the keepers of these giant anteaters.
Good management also helps in the conditioning of exhibits and in the possible reintroduction of the animals into their environment, as it allows recognizing when an animal is ready to be released. Based on the results of this study, the three females will be separated from each other and placed in better conditioned exhibits.
Environmental enrichment allows the animals to express species-appropriate behaviors and thus increases the chance of successful reproduction of endangered species, such as the giant anteater. Following the completion of this ethogram a more suitable environmental enrichment program will be put into practice at Temaikèn Zoo to diminish the high frequency of aggression and stereotypies recorded in this study.
ACKNOWLEDGEMENTS
The author is pleased to acknowledge those who made the research possible. Special thanks go out to the supervisor of the work, Florencia Presa, whose guidance and support were key to develop an understanding of the topic. Infinite appreciation to the Temaikèn Foundation for the use of the facilities, and to all the members of the Nutritional Department and the zookeeper staff for their assistance and cooperation throughout the study.
