Concurrent recall of serially learned visual discrimination problems in dwarf goats (Capra hircus)
Introduction
Mammalian species may be expected to have basic learning and problem-solving methods in common, either as a result of shared evolutionary history or as a result of common adaptive processes to the structure of nature (Macphail and Bolhuis, 2001). Although a variety of experimental tasks have been developed to assess learning and memory function in animals, comparable interspecies tests have not been easy to devise. Multiple-problem discrimination procedures like serial exposure to successive problems have provided valuable approaches for investigating basic learning principles (e.g., the ‘learning to learn’ phenomenon) from a comparative perspective (Thomas, 1986). Furthermore, learning performance in multiple-problem discrimination can serve as a measure for acquisition and retention in comparative studies (Santucci and Treichler, 1990, Treichler et al., 1977). In this approach, which has been referred to as ‘concurrent discrimination’ (Hayes et al., 1953), the trials on a number of different problems are intermixed, either during problem acquisition or during recall of previously learned problems (Thomas, 1996). Applying this approach, animals’ capacity has been tested for retention of information about a large number of object-discriminations over longer time periods (Bakner and Treichler, 1993, Nakagawa, 1992, Treichler, 1984).
In farm animals, most tests of performance in serial (one after the other) or concurrent (at the same time) multiple-problem discrimination have been carried out on horses (Murphy and Arkins, 2007, Nicol, 2002). Various studies reported a significant reduction in the number of trials horses needed to reach a given learning criterion in successive problems, indicating that horses have the ability to use previously learned information to facilitate subsequent learning (Fiske and Potter, 1979, Sappington and Goldman, 1994). Recently, similar results were achieved in dwarf goats (Langbein et al., 2007a). Furthermore, horses, like other Equidae, performed quite well in concurrent discriminations (Thomas, 1986).
Conducting similar studies on the cognitive capacity of other domestic animal species is important for various reasons. Cognitive processes like learning and memory allow animals to display complex adaptive behavior in dynamic environments (Toates, 2004). The behavior of grazing animals is greatly influenced by the way they perceive, process, and memorize information from their environment. Observation of domestic goats under laboratory conditions clearly indicates that they possess excellent vision and readily respond to visual stimuli (Baldwin, 1979, Blakeman and Friend, 1986). Good vision greatly increases wild goats’ chance of survival as they are preyed upon by carnivores and birds of prey in the wild. Furthermore, habitats preferred by feral goats include mountain areas with frequent rocky outcrops and abundant scrubs to use as food and protection (Bullock, 1985). Additionally, goats live in large, complex social groups with a strong linear hierarchy (Langbein and Puppe, 2004), so good visual perception and learning skills would be expected as they are prerequisites for social recognition, as has already been shown in sheep (Kendrick et al., 2001). Feral and wild goats show a highly selective feeding behavior compared to other domestic ungulates (Aldezabal and Garin, 2000). They are able to learn very quickly about spatial and temporal variation of preferred plant species (Provenza et al., 1994). A broader understanding of visual learning abilities, and the memory capacity and stability of goats can help explain the development and stability of learned food preferences in this species.
In farm animal species, a lack of information about learning abilities and memory, or misconceptions about how they learn and adapt their behavior, can result in mismanagement and mistreatment (Held et al., 2002). Another reason for studying learning and memory in farm animals is to evaluate theories relevant to ethical concerns about animal welfare (Croney et al., 2004). Furthermore, understanding the learning flexibility and memory capacity of farm animals is a prerequisite for the future design of species-appropriate devices for cognitive enrichment of housing facilities. As already applied in zoos and recently discussed for farm animals (Bloomsmith et al., 2007, Carlstead and Shepherdson, 2000, Melfi and Thomas, 2005, Swaisgood et al., 2001, Watson et al., 1999), these devices provide long lasting positive effects by combining mental stimulation and a rewarding outcome to facilitate successful coping (Langbein et al., 2004, Puppe et al., 2007). To keep cognitive tasks challenging, they have to be modified and updated regularly, e.g., by varying the rewarded cue (Meehan and Mench, 2007), wherefore knowledge about memory capacity and learning flexibility is essential.
Until now, the vast majority of learning studies have routinely involved training single individuals to perform a limited number of trials per day, organized in separate sessions while separated from their social group and normal housing. However, both separation-related stress and changing the context between the periods of acquisition and retention can impair learning performance (Mendl, 1999, Sondergaard and Ladewig, 2004, Thomas et al., 1985). With this study on serial as well as concurrent multiple-problem discrimination in group-housed dwarf goats, we wanted to broaden the insight into cognitive abilities of animals such as learning flexibility (replacing former cues by new cues), memory capacity (number of cues which can be stored at any one time), and retention time (for how long several cues can be concurrently recalled) under non-laboratory and more naturalistic conditions. We used an experimental approach where the animals could learn individually while remaining in their familiar environment and normal social settings. This was achieved by integrating a fully automated learning device into the animals’ home pen. With this experimental design, we wanted to overcome the restrictions of previous learning studies as described above. As the learning device was accessible all day, the animals could decide themselves when to learn and for how long at all stages of the experiment. There was no restriction on individuals with regard to the number of visits to or trials at the learning device or with regard to the overall amount of reward an animal could gain. Furthermore, with such a learning device, we were able to test the individual learning behavior of a large number of animals simultaneously.
Section snippets
Animals and housing
The subjects of this study were eight female Nigerian dwarf goats (Capra hircus, mean age 132 days at the start of the experiment), from a line bred at our institute for over 10 years. The animals were group-housed in an indoor pen (12 m2), which contained straw litter, a wooden two-floor climbing rack, a hayrack (hay ad lib.), and a round feeder to deliver concentrate (300 g per day/animal). The learning device was installed in a separate compartment inside the pen. The device was accessible to
Shape similarity
The mean SSIM between pairs of shapes over all discrimination problems was 0.502 (±0.046) as analyzed by pairwise comparison of shapes within each problem. The lowest mean SSIMs were found in P3 (0.443) and in P8 (0.444), indicating a higher level of similarity between the shapes in those two problems. The lowest SSIMs were found between S+ and S−1 (0.390) in P3 and between S+ and S−3 (0.375) in P8. The highest mean SSIM was found in P9 (0.583), indicating a low level of similarity between the
Discussion
The aim of the study was to broaden the knowledge of cognitive and learning abilities of animals by studying a non-showpiece species in learning research. Our experimental setup enabled us to investigate individual learning performances under normal housing conditions and social settings. This setup should sufficiently mimic a naturalistic learning situation in domestic animals to satisfy the criticisms of learning research expressed by cognitive ethologists (Ristau, 2001). Dwarf goats were
Acknowledgements
The authors would like to thank D. Sehland for excellent technical care, data collection, and primary processing of raw data. Our very special thanks go to F. Robert Treichler, two anonymous referees, and J.S. Katz for their constructive revision of previous versions of this manuscript. Further thanks go to Christian Wallraven for his assistance with the Perceptual Feature Toolbox. Finally, we are greatly indebted to H. Erhard, D.L. Thomson, and Christine Baes for correcting the English style
References (59)
- et al.
Browsing preference of feral goats (Capra hircus L.) in a Mediterranean mountain scrubland
J. Arid Environ.
(2000) - et al.
Long-term spatial memory in clark nutcracker, Nucifraga columbiana
Anim. Behav.
(1992) Operant studies on shape discrimination in goats
Physiol. Behav.
(1979)- et al.
Visual discrimination at varying distances in Spanish goat
Appl. Anim. Behav. Sci.
(1986) - et al.
Addressing nonhuman primate behavioral problems through the application of operant conditioning: is the human treatment approach a useful model?
Appl. Anim. Behav. Sci.
(2007) - et al.
Use of cues by grazing animals to locate food patches: an example with sheep
Appl. Anim. Behav. Sci.
(1997) - et al.
Analysing dominance relationships by sociometric methods—a plea for more standardised and precise approach in farm animals
Appl. Anim. Behav. Sci.
(2004) - et al.
Visual discrimination learning in dwarf goats and associated changes in heart rate and heart rate variability
Physiol. Behav.
(2004) - et al.
The impact of acoustical secondary reinforcement during shape discrimination learning of dwarf goats (Capra hircus)
Appl. Anim. Behav. Sci.
(2007) - et al.
The challenge of challenge: can problem solving opportunities enhance animal welfare?
Appl. Anim. Behav. Sci.
(2007)