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Dynamics of the access of captive domestic cats to a feed environmental enrichment item
Applied Animal Behaviour Science 151 (2014) 67–74
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Dynamics of the access of captive domestic cats to a feed environmental enrichment item Juliana Damasceno ∗,1 , Gelson Genaro Programa de Pós-Graduac¸ão em Psicobiologia, Departamento de Psicologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes 3900, Monte Alegre, CEP: 14040-901 Ribeirão Preto, SP, Brazil
a r t i c l e
i n f o
Article history: Accepted 10 November 2013 Available online 18 November 2013 Keywords: Welfare Enrichment Interaction Cats Felids
a b s t r a c t Providing feed enrichment to captive felids that are obligate carnivores is crucial for eliciting natural hunting behaviours. However, studies of the efficacy of enrichment techniques usually analyse the whole group, overlooking the different behaviours of individual animals towards the enriched environment. In this study, we used beef (700 g) suspended by steel cables to achieve feed enrichment in a colony of captive domestic cats (Felis silvestris catus), and we analysed the dynamics and the degree of individual interaction with the enrichment item. The enrichment presentation varied as follows: period (morning or afternoon), quantity of enrichment item (one or three), and presence/absence of the experimenter. The results showed that the cats spent more time interacting with the item in the morning (¯x = 19.23 ± 2.00) than in the afternoon (¯x = 15.80 ± 1.59; P = 0.03). The frequency (¯x = 1.97 ± 0.14; P < 0.05) and the duration (¯x = 20.21 ± 1.86; P < 0.01) of the interactions increased when three items were introduced. With respect to the organisation of access to the item, the individuals in the colony accessed the enrichment item in a predetermined order; some individuals interacted with the item more frequently, others interacted with the item moderately, and some interacted little or did not interact with the item at all. On the basis of the dynamics towards the food item, we identified relevant behavioural characteristics in the colony. This more precise diagnosis showed that a more appropriate arrangement of items within the confined space helped to improve environmental enrichment. Providing captive animals with more balanced conditions ensures that individuals within the same colony interact with and benefit from the enrichment item more equally and efficiently. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Environmental enrichment is crucial to ensure that captive species live in satisfactory psychological and physiological conditions (Carlstead et al., 1993; Ellis, 2009; Swaisgood and Shepherdson, 2005). Many types of stimuli can enrich the environment of felids, including sensory
∗ Corresponding author. Tel.: +55 16 92301490/+55 16 36242871/+55 16 82225745. E-mail address: [email protected] (J. Damasceno). 1 Biologist, MSc degree in Science by Psychobiology Postgraduate Program, Postgraduate student at the PhD level in the area of Psychobiology. 0168-1591/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2013.11.004
(Ellis and Wells, 2008, 2010; Resende et al., 2011; Wells, 2009; Wells and Egli, 2004), social (Crowell-Davis et al., 2004), physical (Rochlitz, 2005), cognitive (Dantas-Divers et al., 2011), and feeding stimuli (Szokalski et al., 2012). Felids are obligate carnivores, and they specialise on a diet of animal flesh and organs (Bradshaw and Cook, 1996; Legrand-Défretin, 1994). However, like any species, their diet depends on factors such as the environment and the availability of resources (Beaver, 2003). In their natural habitat, felids are free to fully express their feeding behaviour through locating, stalking, capturing, and killing prey; these behaviours require time and intense activity of the animal (Shepherdson et al., 1993). On the other
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hand, the artificial and predictable environment of captivity frustrates the natural feeding behavioural repertoire of felids, resulting in abnormal behaviours and physiological disorders (Markowitz, 1982; Mcphee, 2002; Wilson, 1982). To minimise these effects, several studies have examined techniques that stimulate the essential natural feeding behaviour of felids (Szokalski et al., 2012). Strategies include presenting new food items, changing the feeding routine and arrangement, introducing food in objects and providing toys that stimulate hunting behaviour (Ellis, 2009; Law et al., 2001; Overall and Dayer, 2005; Rochlitz, 2002; Szokalski et al., 2012). Resende et al. (2009) showed that felids receiving surprise packages containing crude meat hidden in alfalfa dedicated less time to abnormal behaviour and were more active. Bashaw et al. (2003) observed an increase in the frequency and variety of feeding behaviours and a reduction in stereotypies after introducing live fish and horse bones as food enrichments to captive Sumatran tigers and African lions. To make access to food more difficult for domestic cats, Ellis (2009) suggested strategies such as hiding dry cat food in various places, alternating feeding times and introducing puzzle feeders. Varying the presentation of food tends to stimulate the locomotor, cognitive and hunting behaviours that are crucial to felids. Mellen and Shepherdson (1997) suggested that suspended meat is an effective feed enrichment for felines because it motivates hunting behaviour. The growing population of domestic cats has motivated research into sheltered animal welfare (for review, see Geret et al., 2011; Rochlitz, 1999, 2000). There are many discussions about the solitary or gregarious lifestyle of felids; however, in captivity, they are generally accommodated in groups, pairs or trios, depending on the species (Geret et al., 2011; Law et al., 2001;Mellen and Shepherdson, 1997; Rochlitz, 1999, 2000). This grouping generates social organisation among the individuals, resulting in affinities and antagonisms between them. These relationships can affect access to resources that are often scarce in a confined space (for example: resting, feeding, defecating, and urinating areas) and to new objects or enrichment items (Crowell-Davis et al., 2004; Dantas-Divers et al., 2011). Research into environmental enrichment has focused on groups as a whole, and the results have varied (Ellis, 2009). Baron et al. (1957) found a hierarchical linearity in small groups of cats exposed to their favourite food (raw meat). Leaders were the first to feed, and they fed in larger quantities; subordinate individuals consumed smaller quantities if they were able to reach the item. The necessary investigation of how subgroups of cats use enrichment will promote techniques that will benefit individuals as homogeneously as possible (Ellis, 2009). To analyse individual differences, we investigated the dynamics of the access to a feed enrichment item within a colony of domestic cats and examined the degree of interaction of each individual with the item. We tested the hypothesis that individual cats work towards the new item in a predetermined order and that individuals benefit from enrichment to a different extent.
2. Methods This study was approved by the Ethics Committee on Animal Use of the Campus of the city of Ribeirão Preto, University of São Paulo (USP), Brazil, and it complied with the ethical principles of animal experimentation (protocol number 10.1.650.53.8). 2.1. Study site The study was conducted in a shelter/cattery (owned cats permanently held in an outdoor enclosure) located in the city of Ribeirão Preto, state of São Paulo, Brazil. The 1250 m2 shelter was enclosed with grids and nets; it contained cemented and grassy areas with dispersed vegetation and trees. The experiments reported here were conducted in cattery III; its total area of 112.41 m2 comprises 97.09 m2 of floor and 15.32 m2 of vertical space (shelves, tables, swings, suspended beds). On this premises, 3.22 m2 was available to each animal, which is higher than the area recommended by Rochlitz (2002). Within the space described above, 12.09 m2 was a covered area used as a dormitory, which contained 20 basket beds and two feeders. The animals were fed with dry cat food and water ad libitum, supplied once a day. The environment was cleaned daily by a worker with water, and when necessary, a veterinary cleaning product, Herbalvet TA® , consisting of benzalkonium chloride (Ouro Fino, Cravinhos, São Paulo, Brazil), was used for disinfection. A veterinary doctor carried out parasitic and clinical control as well as vaccination against rabies and other diseases specific to felines. 2.2. Subjects The cat colony included 35 neutered adult individuals, 23 females and 12 males, of undefined breed. No new individuals had been introduced into the group during the previous 4 years, indicating that the social structure of the colony was stable. The animals had daily contact with humans, including handlers, veterinarians, cleaning staff and owners of the shelter. Individual cats had records with their name, identification number (corresponding to hair colour and sex), and two photographs (one of the face and one of the right side of the body). During the observations, the animals were identified on the basis of their registration and their marking patterns. In the results and discussion sections, individual cats will be represented by their registration numbers. 2.3. Feed enrichment Feed enrichment consisted of 700 g of beef (sirloin) suspended 30 cm above the ground by a steel cable (this height enabled the cats to reach the meat), and it was available to the colony for 2 h on a daily basis. The food was presented via a system of steel cables located outside of the premises, and all of the individuals had equal opportunities to approach the meat. Experimenters were absent so that they did not inadvertently favour the approach of a certain individual to the enrichment item,
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and when experimenters were present, it was in a controlled manner. The nutritional needs of the cats were met by regular feeding (dry cat food) ad libitum in the feeders throughout the experiments; therefore, the sole purpose of the enrichment was to create a stimulating environment. 2.4. Presence of experimenter In order to verify whether the presence of a person known by the animals could affect the behaviour of individuals in the colony, the first author of the article was present in the experiments in a controlled manner. This controlled manner meant that the author intervened during the experiments only when the methodology required that presence, with alternating trials with her presence and her absence performed randomly. The entire protocol is detailed in Section 2.5. It is important to emphasise that the author is familiar to the animals and has daily contact with them for 3 years and was responsible for tasks such as cleaning the shelter, medically treating the animals, and applying regular and planned environmental enrichment, as well as general feeding. 2.5. Procedures The behaviours were video recorded in real-time (30 frames/s), 2 h per trial, with a mini-camera Intelbras® Vm 300 (Intelbras SA, São José, Santa Catarina, Brazil), and the images were recorded on Sony® DVDs (Sony Electronics, San Diego, CA, USA) for subsequent analysis. We tested the following arrangements in the trials conducted in this study:
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ANP3, ANA1, or ANA3. The trials were carried out in triplicate, totalling 24 trials. The enrichment item was removed at the end of each trial. Observations were performed according to Altmann (1974), using the focal sampling method to analyse how individuals interacted with the item. The following behavioural categories were noted: Interaction with the enrichment item—when the cat touched the item (beef) with the front paw or the mouth. Aggression—when a cat strikes with a paw, bites, or engages in real duels with another cat (Bonanni et al., 2007). We used the data to design a new experiment and observed how the colony behaved towards the enrichment item after the removal of the eight most interactive individuals, which were selected on the basis of the frequency of interaction with the enrichment item. The individuals that lay statistically above the mean (Wilcoxon test, P < 0.05) were designated most interactive. The MA1 (morning, absence of experimenter, one item) trial arrangement was chosen because after analysing the results (from previous experiments) we identified no significant difference in the interaction of the animal during the presence of the experimenter, and there is greater interaction of the animals in the morning. The factor “one item” was chosen because, in a new experiment without the more interactive cats, we investigated whether the absence of those most interactive animals induced levels of interaction in other cats similar to the presence of three items. This new trial was renamed experiment MA1B. The investigated categories and sampling methods were the same as those used in the previous trials.
2.6. Data analysis (1) Presence (P) or absence (A) of the experimenter: For the trials accomplished in the presence (P) of the experimenter, the first author entered the premises exactly halfway through the trial (at 1 h after the start of the observation), but did not interact with the individuals. The experimenter suspended the item 1.20 m above the ground, i.e., out of the reach of the animals, for 30 s, and then returned it to the previous position for possible subsequent interaction. (2) Variation in the number of enrichment items: one (1) or three (3) items were presented to the colony. In the situation involving three items and the presence of the experimenter, all of the items were simultaneously suspended 1.20 m above the ground. (3) Period of item presentation: Morning (M), from 7:30 h to 9:30 h or afternoon (AN), from 13:30 h to 16:30 h. Because cats tend to be more active during twilight periods, at dawn and dusk (George, 1974; Langham, 1992), the periods were selected to verify whether the degree of interaction with the enrichment item varied in periods of intense (early morning) and little (early afternoon) feline activity. The trials were randomly ordered by means of a draw; the arrangements varied as follows (according to period, morning or afternoon; presence or absence of experimenter; number of items): MP1, MP3, MA1, MA3, ANP1,
The significance level was set at P < 0.05 (˛=0.05), and all of the data correspond to the mean (¯x) and standard error of the mean. The unpaired student’s t-test was used to compare how the arrangements (morning vs. afternoon, presence vs. absence of the experimenter, and one item vs. three items) affected the frequency and duration of aggression. The Wilcoxon test was used to compare the general mean of the colony with the mean values obtained for each individual regarding their interaction with the enrichment item in terms of frequency, duration, and latency. For each trial, we quantified the mean durations, frequencies and latencies of interactions with the enrichment item for each individual belonging to the colony. We also determined the general mean of the colony for each variable. Using the Wilcoxon test, we compared each individual value with the general mean of the colony, which helped identify the degree of interaction with the enrichment item for each individual relative to the whole group. The Spearman correlation coefficient was employed to verify whether latency correlated with frequency of interaction with the item. The Mann–Whitney non-parametric test was used to compare the data from MA1 and MA1B (in terms of interaction with the item).
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Table 1 Mean ± SEM for duration and frequency of interaction with the enrichment item and frequency of aggression during the 24 experimental days. Arrangement
Morning Afternoon Presence Absence One item Three items
Mean ± SEM
19.23 ± 2.00 15.80 ± 1.59 16.26 ± 1.65 18.74 ± 1.95 13.27 ± 1.51 20.21 ± 1.86
Behaviour categories Interaction with the enrichment item
Aggression
Duration (min)
Frequency
Frequency
P
t
n
Mean ± SEM
P
t
n
Mean ± SEM
P
t
n
0.03*
2.45
1.13
312
1.05
324
0.06
1.89
0.81
0.25
0.01*
8.42
0.05*
2.99
0.42 ± 0.09 0.32 ± 0.06 0.38 ± 0.07 0.36 ± 0.08 0.47 ± 0.09 0.27 ± 0.05
0.30
1.39
1.77 ± 0.15 1.64 ± 0.12 1.86 ± 0.14 1.55 ± 0.13 1.43 ± 0.14 1.97 ± 0.14
0.27
0.12
148 162 163 147 124 186
0.05*
2.05
P: values obtained by Student’s t-test comparing the mean interaction with the enrichment item and aggression in the different arrangements − morning vs. afternoon, presence vs. absence of the experimenter, and one item vs. three items; n corresponds to the number of interactions with the item. * Indicates individuals that were significantly different (P < 0.05).
3. Results 3.1. Interaction with the feed enrichment item Of the 35 individuals belonging to the colony, only 26 interacted with the enrichment item (beef) in the first experiment. Therefore, the data below correspond to these 26 interactive individuals. The durations of interaction differed significantly between the periods (morning, x¯ 19.23 ± 2.00 min; afternoon, x¯ 15.80 ± 1.59 min.; t = 2.45; P = 0.03). The Student’s t-test revealed that the frequency and duration of interactions were significantly different in the presence of one item and three items (t = 2.99; P < 0.05 and t = 4.82; P < 0.01, respectively, Table 1). In addition to exhibiting increased frequencies and durations of interaction, nine individuals who had not interacted with the enrichment when only one item was present interacted when three items were present in the environment; these animals were 4.7, 2.6, 10.4, 4.15, 3.2, 27.1, 20.2, 2.3 and 29.1. During the interaction with enrichment, few instances of aggression were recorded. Among this small observed frequency, with only one item displayed (¯x = 0.47 ± 0.09), even when three items were introduced (¯x = 0.27 ± 0.05)
aggressions were reduced to a greater extent, as shown by the t-test (t = 2.05, P < 0.05). The general mean of the colony for the duration of interaction with the enrichment item during the 2-h time trial was x¯ = 8.67 ± 0.05 (min). Comparing each individual with the general mean of the colony, we verified that six individuals were above the mean, seven were within the mean, and 13 were below the mean (Fig. 1). When the latency of interaction with the enrichment item was measured (Fig. 2), the general mean of the colony was x¯ = 29.83 ± 1.91 (min). Five individuals had latency significantly below the mean, showing that most of the time, they were among the first to interact with the enrichment item. The frequency of interaction with the enrichment item for each individual along the 24 trials furnished a general mean value equal to x¯ = 1.70 ± 0.10 for the colony (represented by the line in Fig. 3). Seven individuals were significantly above the mean 6 were within the mean, and thirteen were below the mean. Latency and frequency of interaction with the enrichment item correlated negatively (Fig. 4), i.e., less latent individuals interacted with the enrichment item more frequently. According to the Spearman correlation coefficient
Fig. 1. Mean ± SEM of duration of interaction with the enrichment item for each individual of colony during the 2 h of observation. An asterisk (*) indicates individuals that were significantly different (P < 0.05) than the general mean of the colony (represented by the line).
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Fig. 2. Mean ± SEM of latency of interaction with the enrichment item throughout the 2 h of observation, during the 24 days of the experiment. An asterisk (*) indicates individuals that were significantly different (P < 0.05) than the general mean of the colony (represented by the line).
Fig. 3. Mean ± SEM of total frequency of interaction with the enrichment item for each individual during the 24 days of the experiment. An asterisk (*) indicates individuals that were significantly different (P < 0.05) than the general mean of the colony (represented by the line).
(r = −0.7052, P < 0.01), a rise in frequency should be accompanied by decreased latency. 3.2. Ranking within the colony Taking together the frequency, latency, and duration data obtained from the analysis of interaction with the enrichment item, we added the scores for each individual and proposed an interaction ranking (Table 2). 3.3. Experiment MA1B
Fig. 4. Spearman correlation (r = −0.7052; P < 0.01) between latency and frequency of interaction with the enrichment item for each individual in the colony throughout the 24 trials.
For this experiment, we removed the eight most interactive individuals. We analysed the same behavioural categories (aggression and interaction with the enrichment item) and the variables of duration and frequency. Removing the most interactive individuals significantly increased the mean frequency (MA1 x¯ = 1.19 ± 0.27; MA1B¯x = 5.80 ± 4.24; U = 88; P < 0.01) and duration (MA1¯x = 4.41 ± 0.40 (min.); MA1B x¯ = 6.61 ± 1.17 (min.); t = 2.08; P = 0.04) of interaction with the enrichment item
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Table 2 Ranking of individual cats according to the total scores for interaction with the enrichment item. Ranking of colony for interaction with the enrichment Variables
Sex
Frequency
Duration
Latency
Ranking
2.19 8.5 3.6 4.2 8.23 22.1 2.10 8.17 8.7 2.13 17.2 8.24 9.1 2.20 4.15 4.7 15.1 4.38 10.4 2.6 20.2 1.3 3.2 27.1 2.3 29.1
M M F M M F M F M M F F F F F F F F F F F M F F M M
1 3 2 4 6 5 11 8 7 9 10 13 14 12 21 17 16 15 20 19 24 18 22 23 25 26
1 4 3 5 2 7 6 8 10 13 11 9 12 14 24 20 15 16 21 19 23 17 18 22 25 26
3 1 5 2 9 6 8 11 12 7 14 17 16 18 4 13 21 22 15 19 10 23 20 24 25 26
1st 2nd 3rd 4th 5th 6th 7th 8th 9th 9th 10th 11th 12th 13th 14th 15th 16th 17th 18th 19th 19th 20th 21st 22nd 23rd 24th
The rectangle highlights the individuals that dominated access to the item and were removed for the MA1B (morning, absence of the experimenter, one item, second experiment without the eight most interactive individuals) trial.
when compared with MA1, as attested by the Student’s t-test and Mann–Whitney test respectively (Fig. 5). We also observed that, out of the 27 individuals that participated in the new experiment (35 from the colony without the eight most interactive), some animals, which had not interacted with the enrichment item in the first experiment began to do so in this new test (MA1B).
4. Discussion To determine how individual cats accessed the enrichment item, we provided the colony with a small number of items (one or three) in relation to the total number of cats. We observed that 26 of the 35 animals interacted with the item throughout the entire study. In the wild, felids are intensely active at twilight, the beginning of the morning or evening (George, 1974; Langham, 1992). In a recent paper, Quirke and O’Riordan (2011) noted increased exploratory and other types of behaviour, and reduced inactivity, when cheetahs (Ancinonyx jubatus) were fed between 9:00 h and 13:00 h instead of at 16:00 h. Here, cats interacted with the enrichment item significantly longer during the early morning (7:30 h to 9:30 h) compared with the early afternoon (13:30 h to 15:30 h), suggesting that enrichment should be applied to felids during the periods of greater activity (early
Fig. 5. Mean ± SEM of (A) frequency and (B) duration of interaction with the enrichment item. MA1 (morning, absence of experimenter, one item, first experiment with the most interactive individuals) vs. MA1B (morning, absence of experimenter, one item, second experiment without the most interactive individuals) during the 3 days of experimentation.
morning, for example), to stimulate natural behaviours more effectively. The presence of the experimenter on the premises for 30 s (when the experimenter suspended the item and repositioned it for interaction with the animals) did not affect the interactions of the individual cats with the enrichment item. This may be due to methodology that allowed momentary interruption (of only 30 s) of the animals that were interacting with the item at the moment. Regardless, the presence of a human did not affect the interaction of the animals with the enrichment items in our study; human contact is crucial for satisfactory management and constitutes fundamental enrichment for captive cats (Geret et al., 2011; DeLuca and Kranda, 1992; Rochlitz, 2002). The number of items (one or three) significantly affected the durations and frequencies of interactions with the enrichment item(s). This result emphasises the need to consider the quantity of enrichment items to benefit as many individuals as possible (Dantas-Divers et al., 2011). Compared to trials that involved only one item, the presentation of three items increased the durations and frequencies of interactions and significantly reduced aggression, which was already low because the colony was stable at the time of our study. In a study of a stable colony of domestic cats that was similar to our study, Dantas-Divers et al. (2011) found no relationship between agonistic behaviour and the use of environmental enrichment or food (i.e., a puzzle feeder). These authors concluded that aggressive behaviour is linked to stress and emotional
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states such as fear, anxiety and pain rather than behaviours that indicate social position in the group or priority access to resources. Within the same colony, cats have distinct preferences in terms of environmental conditions, activity levels and social interactions with the other cats and humans (Bradshaw et al., 2000; Crowell-Davis et al., 2004; Geret et al., 2011). Studies aimed at identifying the individual differences within the colony assist in understanding the overall needs for the care of the group. Bradshaw et al. (2000) described the differing preferences shown by domestic cats for new food. Feaver et al. (1986) used a qualitative evaluation method to detect individual differences in two laboratory cat colonies, and Ellis (2009) stated that it is necessary to assess individual differences when applying behavioural enrichment to cats to ensure that the largest number of cats benefit from the stimuli. In this study, we verified whether these individual differences really existed within the target cat colony by observing how individual cats worked towards a certain enrichment item. Some of the cats interacted with the enrichment item more frequently, whereas others interacted with the item moderately. Two hypotheses can be proposed for why the animals did not interact with the item at all: first, because they were not interested in the food (Bradshaw et al., 2000) or second, because the other individuals prevented their access to the item (Dantas-Divers et al., 2011; Durr and Smith, 1997; Knowles et al., 2004). The cats that interacted with the item more intensely showed a higher frequency and duration of interaction and a lower latency than the mean value obtained for the colony; in other words, they monopolised the item. The negative Spearman correlation between frequency and latency corroborated these observations: the lower the latency for interaction with the enrichment item is, the higher the frequency of interaction with it. The individuals that interacted with the item more promptly also interacted more frequently, indicating that animals that did not have access to the enrichment item were somehow unable to work towards the item due to a monopoly held by the most interactive individuals. We also noted a significantly increased frequency and duration of interaction with the enrichment item in MA1B, compared with trial MA1. Therefore, the absence of the most interactive animals provided other individuals with more opportunities to interact with the item. An increase in interaction when we introduced three items instead of one item, which demonstrates that more animals can interact with the enrichment item in the presence of a higher number of items or in the absence of monopolising individuals, had also observed. Taken together, these observations dismiss the previous hypothesis that cats do not interact with the item because they are not interested in the food. In fact, our findings, that some cats had little or no interaction with the enrichment item, reinforce the assumption that some individuals restrict the access of other animals to the item (Baron et al., 1957; Knowles et al., 2004) and confirm our hypothesis that colonies have a pre-determined order to enrichment access. A stable social environment does not imply stability in the differences among individuals; a dominating animal
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does not dominate all types of situations or activities (Durr and Smith, 1997). Individuals’ dominance, monopolisation or priority to access resources has been studied and exhibits a complex structure. By analysing parameters of subtle agonistic behaviour, Knowles et al. (2004) observed a complex ordering of animals’ access to a food bowl. While determining the overall ranking of the colony, regarding interaction with enrichment, we observed that top-ranked individuals dominated the interaction with enrichment. To ensure adequate management and welfare of confined animals, it is fundamental to understand how individuals behave socially and how relationships among animals affect their access to resources (Dantas-Divers et al., 2011). Thus, by introducing feed enrichment, we identified how the group organises access to the food resource and how some individuals can monopolize the enrichment. Because of the difficulty of finding more than one colony under the same composition, housing and social stability conditions, which are fundamental aspects for the replication of the study, the group we examined proved to be satisfactory for achieving the proposed goals, and this supposition is supported by the statistical evidence we have presented. Continuing along these lines, future studies should focus on the methodology of applying environmental enrichment in confined animal groups. Such methodology is essential for ensuring that the techniques used are effective and appropriate to benefit individuals in a homogeneous and balanced way. 5. Conclusion Within confined spaces, captive domestic cats follow a priority order to access resources such as environmental enrichment items. Certain individuals monopolise the resource, limiting the approach of other animals to the item. Therefore, we suggest that making a larger number of items available throughout the premises enriches large colonies more appropriately and facilitates more equal access to the enrichment. When implemented with careful methodology and detailed knowledge about behavioural differences within species, feed enrichment can be an efficient strategy to promote natural behaviour, which is essential for animals living in confined or restricted environments. Acknowledgements The authors would like to thank the owners of the shelter/cattery for providing the animals and study site, MSc. and PhD. César Augusto Sangaletti Terc¸ariol for the statistical analyses, and the Coordination for the Improvement of Higher Education Personnel (Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior—CAPES) for financial support. References Altmann, J., 1974. Observational study of behavior: sampling methods. Behaviour 49, 227–267. Baron, A., Stewart, C.N., Warren, J.M., 1957. Patterns of social interaction in cats (Felis domestica). Behaviour 11, 56–66.
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Legarnd-Defretin, V., 1994. Differences between cats and dogs: a nutritional view. Proc. Nutr. Soc. 53, 15–24. Markowitz, H., 1982. Behavioral Enrichment in the Zoo. Van Nostrand Reinhold, New York. Mcphee, M.E., 2002. Intact carcasses as enrichment for large felids: effects on on- and off exhibit behaviors. Zoo Biol. 21, 37–47. Mellen, J.D., Shepherdson, D.J., 1997. Environmental enrichment for felids: an integrated approach. Int. Zoo Yb. 35, 191–197. Overall, K.L., Dyer, D., 2005. Enrichment strategies for laboratory animals from the viewpoint of clinical veterinary behavioral medicine: emphasis on cats and dogs. ILAR J. 46, 202–216. Quirke, T., O’Riordan, R.M., 2011. The effect of a randomized enrichment treatment schedule on the behavior of cheetahs (Acinonyx jubatus). Appl. Anim. Behav. Sci. 135, 103–109. Resende, L.S., Remy, G.L., Ramos Jr., V.A., Andriolo, A., 2009. The influence of feeding enrichment on the behavior of small felids (Carnivora: Felidae) in captivity. Zoologia 26, 601–605. Resende, L.S., Gomes, K.C.P., Andriolo, A., Genaro, G., Remy, G.L., Ramos Júnior, V.A., 2011. Influence of cinnamon and catnip on the stereotypical pacing of oncilla cats (Leopardus tigrinus) in Captivity. Appl. Anim. Welf. Sci. 14, 247–254. Rochlitz, I., 1999. Recommendations for the housing of cats in home, in catteries and animal shelters, in laboratories and veterinary surgeries. J. Feline Med. Surg. 1, 181–191. Rochlitz, I., 2000. Recommendations for the housing and care of domestic cats in laboratories. Lab. Anim. 34, 1–9. Rochlitz, I., 2002. Comfortable quarters for cats in research institutions. In: Reinhardt, V., Reinhardt, A. (Eds.), Comfortable Quarters for Laboratory Animals. Animal Welfare Institute, Washington DC, pp. 50–55. Rochlitz, I., 2005. A review of the housing requirements of domestic cats (Felis silvestris catus) kept in home. Appl. Anim. Behav. Sci. 93, 97–109. Shepherdson, D.J., Carlstead, K., Mellen, J.D., Siedensticker, J., 1993. The influence of food presentation on the behaviour of small cats in confined environments. Zoo Biol. 12, 203–216. Szokalski, M.S., Litchfield, C.A., Foster, W.K., 2012. Enrichment for captive tigers (Panthera tigris): current knowledge and future directions. Appl. Anim. Behav. Sci. 139, 1–9. Swaisgood, R.R., Shepherdson, D.J., 2005. Scientific approaches to enrichment and stereotypes in zoo animals: what’s been done and where should we go next? Zoo Biol. 24, 499–518. Wells, D.L., Egli, J.M., 2004. The influence of olfactory enrichment on the behaviour of black-footed cats. Felis nigripes. Appl. Anim. Behav. Sci. 85, 107–119. Wells, D.L., 2009. Sensory stimulation as environmental enrichment for captive animals: a review. Appl. Anim. Behav. Sci. 118, 1–11. Wilson, S.F., 1982. Environmental influences on the activity of captive apes. Zoo Biol. 1, 201–209.
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Dynamics of the access of captive domestic cats to a feed environmental enrichment item Juliana Damasceno ∗,1 , Gelson Genaro Programa de Pós-Graduac¸ão em Psicobiologia, Departamento de Psicologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes 3900, Monte Alegre, CEP: 14040-901 Ribeirão Preto, SP, Brazil
a r t i c l e
i n f o
Article history: Accepted 10 November 2013 Available online 18 November 2013 Keywords: Welfare Enrichment Interaction Cats Felids
a b s t r a c t Providing feed enrichment to captive felids that are obligate carnivores is crucial for eliciting natural hunting behaviours. However, studies of the efficacy of enrichment techniques usually analyse the whole group, overlooking the different behaviours of individual animals towards the enriched environment. In this study, we used beef (700 g) suspended by steel cables to achieve feed enrichment in a colony of captive domestic cats (Felis silvestris catus), and we analysed the dynamics and the degree of individual interaction with the enrichment item. The enrichment presentation varied as follows: period (morning or afternoon), quantity of enrichment item (one or three), and presence/absence of the experimenter. The results showed that the cats spent more time interacting with the item in the morning (¯x = 19.23 ± 2.00) than in the afternoon (¯x = 15.80 ± 1.59; P = 0.03). The frequency (¯x = 1.97 ± 0.14; P < 0.05) and the duration (¯x = 20.21 ± 1.86; P < 0.01) of the interactions increased when three items were introduced. With respect to the organisation of access to the item, the individuals in the colony accessed the enrichment item in a predetermined order; some individuals interacted with the item more frequently, others interacted with the item moderately, and some interacted little or did not interact with the item at all. On the basis of the dynamics towards the food item, we identified relevant behavioural characteristics in the colony. This more precise diagnosis showed that a more appropriate arrangement of items within the confined space helped to improve environmental enrichment. Providing captive animals with more balanced conditions ensures that individuals within the same colony interact with and benefit from the enrichment item more equally and efficiently. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Environmental enrichment is crucial to ensure that captive species live in satisfactory psychological and physiological conditions (Carlstead et al., 1993; Ellis, 2009; Swaisgood and Shepherdson, 2005). Many types of stimuli can enrich the environment of felids, including sensory
∗ Corresponding author. Tel.: +55 16 92301490/+55 16 36242871/+55 16 82225745. E-mail address: [email protected] (J. Damasceno). 1 Biologist, MSc degree in Science by Psychobiology Postgraduate Program, Postgraduate student at the PhD level in the area of Psychobiology. 0168-1591/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2013.11.004
(Ellis and Wells, 2008, 2010; Resende et al., 2011; Wells, 2009; Wells and Egli, 2004), social (Crowell-Davis et al., 2004), physical (Rochlitz, 2005), cognitive (Dantas-Divers et al., 2011), and feeding stimuli (Szokalski et al., 2012). Felids are obligate carnivores, and they specialise on a diet of animal flesh and organs (Bradshaw and Cook, 1996; Legrand-Défretin, 1994). However, like any species, their diet depends on factors such as the environment and the availability of resources (Beaver, 2003). In their natural habitat, felids are free to fully express their feeding behaviour through locating, stalking, capturing, and killing prey; these behaviours require time and intense activity of the animal (Shepherdson et al., 1993). On the other
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hand, the artificial and predictable environment of captivity frustrates the natural feeding behavioural repertoire of felids, resulting in abnormal behaviours and physiological disorders (Markowitz, 1982; Mcphee, 2002; Wilson, 1982). To minimise these effects, several studies have examined techniques that stimulate the essential natural feeding behaviour of felids (Szokalski et al., 2012). Strategies include presenting new food items, changing the feeding routine and arrangement, introducing food in objects and providing toys that stimulate hunting behaviour (Ellis, 2009; Law et al., 2001; Overall and Dayer, 2005; Rochlitz, 2002; Szokalski et al., 2012). Resende et al. (2009) showed that felids receiving surprise packages containing crude meat hidden in alfalfa dedicated less time to abnormal behaviour and were more active. Bashaw et al. (2003) observed an increase in the frequency and variety of feeding behaviours and a reduction in stereotypies after introducing live fish and horse bones as food enrichments to captive Sumatran tigers and African lions. To make access to food more difficult for domestic cats, Ellis (2009) suggested strategies such as hiding dry cat food in various places, alternating feeding times and introducing puzzle feeders. Varying the presentation of food tends to stimulate the locomotor, cognitive and hunting behaviours that are crucial to felids. Mellen and Shepherdson (1997) suggested that suspended meat is an effective feed enrichment for felines because it motivates hunting behaviour. The growing population of domestic cats has motivated research into sheltered animal welfare (for review, see Geret et al., 2011; Rochlitz, 1999, 2000). There are many discussions about the solitary or gregarious lifestyle of felids; however, in captivity, they are generally accommodated in groups, pairs or trios, depending on the species (Geret et al., 2011; Law et al., 2001;Mellen and Shepherdson, 1997; Rochlitz, 1999, 2000). This grouping generates social organisation among the individuals, resulting in affinities and antagonisms between them. These relationships can affect access to resources that are often scarce in a confined space (for example: resting, feeding, defecating, and urinating areas) and to new objects or enrichment items (Crowell-Davis et al., 2004; Dantas-Divers et al., 2011). Research into environmental enrichment has focused on groups as a whole, and the results have varied (Ellis, 2009). Baron et al. (1957) found a hierarchical linearity in small groups of cats exposed to their favourite food (raw meat). Leaders were the first to feed, and they fed in larger quantities; subordinate individuals consumed smaller quantities if they were able to reach the item. The necessary investigation of how subgroups of cats use enrichment will promote techniques that will benefit individuals as homogeneously as possible (Ellis, 2009). To analyse individual differences, we investigated the dynamics of the access to a feed enrichment item within a colony of domestic cats and examined the degree of interaction of each individual with the item. We tested the hypothesis that individual cats work towards the new item in a predetermined order and that individuals benefit from enrichment to a different extent.
2. Methods This study was approved by the Ethics Committee on Animal Use of the Campus of the city of Ribeirão Preto, University of São Paulo (USP), Brazil, and it complied with the ethical principles of animal experimentation (protocol number 10.1.650.53.8). 2.1. Study site The study was conducted in a shelter/cattery (owned cats permanently held in an outdoor enclosure) located in the city of Ribeirão Preto, state of São Paulo, Brazil. The 1250 m2 shelter was enclosed with grids and nets; it contained cemented and grassy areas with dispersed vegetation and trees. The experiments reported here were conducted in cattery III; its total area of 112.41 m2 comprises 97.09 m2 of floor and 15.32 m2 of vertical space (shelves, tables, swings, suspended beds). On this premises, 3.22 m2 was available to each animal, which is higher than the area recommended by Rochlitz (2002). Within the space described above, 12.09 m2 was a covered area used as a dormitory, which contained 20 basket beds and two feeders. The animals were fed with dry cat food and water ad libitum, supplied once a day. The environment was cleaned daily by a worker with water, and when necessary, a veterinary cleaning product, Herbalvet TA® , consisting of benzalkonium chloride (Ouro Fino, Cravinhos, São Paulo, Brazil), was used for disinfection. A veterinary doctor carried out parasitic and clinical control as well as vaccination against rabies and other diseases specific to felines. 2.2. Subjects The cat colony included 35 neutered adult individuals, 23 females and 12 males, of undefined breed. No new individuals had been introduced into the group during the previous 4 years, indicating that the social structure of the colony was stable. The animals had daily contact with humans, including handlers, veterinarians, cleaning staff and owners of the shelter. Individual cats had records with their name, identification number (corresponding to hair colour and sex), and two photographs (one of the face and one of the right side of the body). During the observations, the animals were identified on the basis of their registration and their marking patterns. In the results and discussion sections, individual cats will be represented by their registration numbers. 2.3. Feed enrichment Feed enrichment consisted of 700 g of beef (sirloin) suspended 30 cm above the ground by a steel cable (this height enabled the cats to reach the meat), and it was available to the colony for 2 h on a daily basis. The food was presented via a system of steel cables located outside of the premises, and all of the individuals had equal opportunities to approach the meat. Experimenters were absent so that they did not inadvertently favour the approach of a certain individual to the enrichment item,
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and when experimenters were present, it was in a controlled manner. The nutritional needs of the cats were met by regular feeding (dry cat food) ad libitum in the feeders throughout the experiments; therefore, the sole purpose of the enrichment was to create a stimulating environment. 2.4. Presence of experimenter In order to verify whether the presence of a person known by the animals could affect the behaviour of individuals in the colony, the first author of the article was present in the experiments in a controlled manner. This controlled manner meant that the author intervened during the experiments only when the methodology required that presence, with alternating trials with her presence and her absence performed randomly. The entire protocol is detailed in Section 2.5. It is important to emphasise that the author is familiar to the animals and has daily contact with them for 3 years and was responsible for tasks such as cleaning the shelter, medically treating the animals, and applying regular and planned environmental enrichment, as well as general feeding. 2.5. Procedures The behaviours were video recorded in real-time (30 frames/s), 2 h per trial, with a mini-camera Intelbras® Vm 300 (Intelbras SA, São José, Santa Catarina, Brazil), and the images were recorded on Sony® DVDs (Sony Electronics, San Diego, CA, USA) for subsequent analysis. We tested the following arrangements in the trials conducted in this study:
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ANP3, ANA1, or ANA3. The trials were carried out in triplicate, totalling 24 trials. The enrichment item was removed at the end of each trial. Observations were performed according to Altmann (1974), using the focal sampling method to analyse how individuals interacted with the item. The following behavioural categories were noted: Interaction with the enrichment item—when the cat touched the item (beef) with the front paw or the mouth. Aggression—when a cat strikes with a paw, bites, or engages in real duels with another cat (Bonanni et al., 2007). We used the data to design a new experiment and observed how the colony behaved towards the enrichment item after the removal of the eight most interactive individuals, which were selected on the basis of the frequency of interaction with the enrichment item. The individuals that lay statistically above the mean (Wilcoxon test, P < 0.05) were designated most interactive. The MA1 (morning, absence of experimenter, one item) trial arrangement was chosen because after analysing the results (from previous experiments) we identified no significant difference in the interaction of the animal during the presence of the experimenter, and there is greater interaction of the animals in the morning. The factor “one item” was chosen because, in a new experiment without the more interactive cats, we investigated whether the absence of those most interactive animals induced levels of interaction in other cats similar to the presence of three items. This new trial was renamed experiment MA1B. The investigated categories and sampling methods were the same as those used in the previous trials.
2.6. Data analysis (1) Presence (P) or absence (A) of the experimenter: For the trials accomplished in the presence (P) of the experimenter, the first author entered the premises exactly halfway through the trial (at 1 h after the start of the observation), but did not interact with the individuals. The experimenter suspended the item 1.20 m above the ground, i.e., out of the reach of the animals, for 30 s, and then returned it to the previous position for possible subsequent interaction. (2) Variation in the number of enrichment items: one (1) or three (3) items were presented to the colony. In the situation involving three items and the presence of the experimenter, all of the items were simultaneously suspended 1.20 m above the ground. (3) Period of item presentation: Morning (M), from 7:30 h to 9:30 h or afternoon (AN), from 13:30 h to 16:30 h. Because cats tend to be more active during twilight periods, at dawn and dusk (George, 1974; Langham, 1992), the periods were selected to verify whether the degree of interaction with the enrichment item varied in periods of intense (early morning) and little (early afternoon) feline activity. The trials were randomly ordered by means of a draw; the arrangements varied as follows (according to period, morning or afternoon; presence or absence of experimenter; number of items): MP1, MP3, MA1, MA3, ANP1,
The significance level was set at P < 0.05 (˛=0.05), and all of the data correspond to the mean (¯x) and standard error of the mean. The unpaired student’s t-test was used to compare how the arrangements (morning vs. afternoon, presence vs. absence of the experimenter, and one item vs. three items) affected the frequency and duration of aggression. The Wilcoxon test was used to compare the general mean of the colony with the mean values obtained for each individual regarding their interaction with the enrichment item in terms of frequency, duration, and latency. For each trial, we quantified the mean durations, frequencies and latencies of interactions with the enrichment item for each individual belonging to the colony. We also determined the general mean of the colony for each variable. Using the Wilcoxon test, we compared each individual value with the general mean of the colony, which helped identify the degree of interaction with the enrichment item for each individual relative to the whole group. The Spearman correlation coefficient was employed to verify whether latency correlated with frequency of interaction with the item. The Mann–Whitney non-parametric test was used to compare the data from MA1 and MA1B (in terms of interaction with the item).
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Table 1 Mean ± SEM for duration and frequency of interaction with the enrichment item and frequency of aggression during the 24 experimental days. Arrangement
Morning Afternoon Presence Absence One item Three items
Mean ± SEM
19.23 ± 2.00 15.80 ± 1.59 16.26 ± 1.65 18.74 ± 1.95 13.27 ± 1.51 20.21 ± 1.86
Behaviour categories Interaction with the enrichment item
Aggression
Duration (min)
Frequency
Frequency
P
t
n
Mean ± SEM
P
t
n
Mean ± SEM
P
t
n
0.03*
2.45
1.13
312
1.05
324
0.06
1.89
0.81
0.25
0.01*
8.42
0.05*
2.99
0.42 ± 0.09 0.32 ± 0.06 0.38 ± 0.07 0.36 ± 0.08 0.47 ± 0.09 0.27 ± 0.05
0.30
1.39
1.77 ± 0.15 1.64 ± 0.12 1.86 ± 0.14 1.55 ± 0.13 1.43 ± 0.14 1.97 ± 0.14
0.27
0.12
148 162 163 147 124 186
0.05*
2.05
P: values obtained by Student’s t-test comparing the mean interaction with the enrichment item and aggression in the different arrangements − morning vs. afternoon, presence vs. absence of the experimenter, and one item vs. three items; n corresponds to the number of interactions with the item. * Indicates individuals that were significantly different (P < 0.05).
3. Results 3.1. Interaction with the feed enrichment item Of the 35 individuals belonging to the colony, only 26 interacted with the enrichment item (beef) in the first experiment. Therefore, the data below correspond to these 26 interactive individuals. The durations of interaction differed significantly between the periods (morning, x¯ 19.23 ± 2.00 min; afternoon, x¯ 15.80 ± 1.59 min.; t = 2.45; P = 0.03). The Student’s t-test revealed that the frequency and duration of interactions were significantly different in the presence of one item and three items (t = 2.99; P < 0.05 and t = 4.82; P < 0.01, respectively, Table 1). In addition to exhibiting increased frequencies and durations of interaction, nine individuals who had not interacted with the enrichment when only one item was present interacted when three items were present in the environment; these animals were 4.7, 2.6, 10.4, 4.15, 3.2, 27.1, 20.2, 2.3 and 29.1. During the interaction with enrichment, few instances of aggression were recorded. Among this small observed frequency, with only one item displayed (¯x = 0.47 ± 0.09), even when three items were introduced (¯x = 0.27 ± 0.05)
aggressions were reduced to a greater extent, as shown by the t-test (t = 2.05, P < 0.05). The general mean of the colony for the duration of interaction with the enrichment item during the 2-h time trial was x¯ = 8.67 ± 0.05 (min). Comparing each individual with the general mean of the colony, we verified that six individuals were above the mean, seven were within the mean, and 13 were below the mean (Fig. 1). When the latency of interaction with the enrichment item was measured (Fig. 2), the general mean of the colony was x¯ = 29.83 ± 1.91 (min). Five individuals had latency significantly below the mean, showing that most of the time, they were among the first to interact with the enrichment item. The frequency of interaction with the enrichment item for each individual along the 24 trials furnished a general mean value equal to x¯ = 1.70 ± 0.10 for the colony (represented by the line in Fig. 3). Seven individuals were significantly above the mean 6 were within the mean, and thirteen were below the mean. Latency and frequency of interaction with the enrichment item correlated negatively (Fig. 4), i.e., less latent individuals interacted with the enrichment item more frequently. According to the Spearman correlation coefficient
Fig. 1. Mean ± SEM of duration of interaction with the enrichment item for each individual of colony during the 2 h of observation. An asterisk (*) indicates individuals that were significantly different (P < 0.05) than the general mean of the colony (represented by the line).
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Fig. 2. Mean ± SEM of latency of interaction with the enrichment item throughout the 2 h of observation, during the 24 days of the experiment. An asterisk (*) indicates individuals that were significantly different (P < 0.05) than the general mean of the colony (represented by the line).
Fig. 3. Mean ± SEM of total frequency of interaction with the enrichment item for each individual during the 24 days of the experiment. An asterisk (*) indicates individuals that were significantly different (P < 0.05) than the general mean of the colony (represented by the line).
(r = −0.7052, P < 0.01), a rise in frequency should be accompanied by decreased latency. 3.2. Ranking within the colony Taking together the frequency, latency, and duration data obtained from the analysis of interaction with the enrichment item, we added the scores for each individual and proposed an interaction ranking (Table 2). 3.3. Experiment MA1B
Fig. 4. Spearman correlation (r = −0.7052; P < 0.01) between latency and frequency of interaction with the enrichment item for each individual in the colony throughout the 24 trials.
For this experiment, we removed the eight most interactive individuals. We analysed the same behavioural categories (aggression and interaction with the enrichment item) and the variables of duration and frequency. Removing the most interactive individuals significantly increased the mean frequency (MA1 x¯ = 1.19 ± 0.27; MA1B¯x = 5.80 ± 4.24; U = 88; P < 0.01) and duration (MA1¯x = 4.41 ± 0.40 (min.); MA1B x¯ = 6.61 ± 1.17 (min.); t = 2.08; P = 0.04) of interaction with the enrichment item
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Table 2 Ranking of individual cats according to the total scores for interaction with the enrichment item. Ranking of colony for interaction with the enrichment Variables
Sex
Frequency
Duration
Latency
Ranking
2.19 8.5 3.6 4.2 8.23 22.1 2.10 8.17 8.7 2.13 17.2 8.24 9.1 2.20 4.15 4.7 15.1 4.38 10.4 2.6 20.2 1.3 3.2 27.1 2.3 29.1
M M F M M F M F M M F F F F F F F F F F F M F F M M
1 3 2 4 6 5 11 8 7 9 10 13 14 12 21 17 16 15 20 19 24 18 22 23 25 26
1 4 3 5 2 7 6 8 10 13 11 9 12 14 24 20 15 16 21 19 23 17 18 22 25 26
3 1 5 2 9 6 8 11 12 7 14 17 16 18 4 13 21 22 15 19 10 23 20 24 25 26
1st 2nd 3rd 4th 5th 6th 7th 8th 9th 9th 10th 11th 12th 13th 14th 15th 16th 17th 18th 19th 19th 20th 21st 22nd 23rd 24th
The rectangle highlights the individuals that dominated access to the item and were removed for the MA1B (morning, absence of the experimenter, one item, second experiment without the eight most interactive individuals) trial.
when compared with MA1, as attested by the Student’s t-test and Mann–Whitney test respectively (Fig. 5). We also observed that, out of the 27 individuals that participated in the new experiment (35 from the colony without the eight most interactive), some animals, which had not interacted with the enrichment item in the first experiment began to do so in this new test (MA1B).
4. Discussion To determine how individual cats accessed the enrichment item, we provided the colony with a small number of items (one or three) in relation to the total number of cats. We observed that 26 of the 35 animals interacted with the item throughout the entire study. In the wild, felids are intensely active at twilight, the beginning of the morning or evening (George, 1974; Langham, 1992). In a recent paper, Quirke and O’Riordan (2011) noted increased exploratory and other types of behaviour, and reduced inactivity, when cheetahs (Ancinonyx jubatus) were fed between 9:00 h and 13:00 h instead of at 16:00 h. Here, cats interacted with the enrichment item significantly longer during the early morning (7:30 h to 9:30 h) compared with the early afternoon (13:30 h to 15:30 h), suggesting that enrichment should be applied to felids during the periods of greater activity (early
Fig. 5. Mean ± SEM of (A) frequency and (B) duration of interaction with the enrichment item. MA1 (morning, absence of experimenter, one item, first experiment with the most interactive individuals) vs. MA1B (morning, absence of experimenter, one item, second experiment without the most interactive individuals) during the 3 days of experimentation.
morning, for example), to stimulate natural behaviours more effectively. The presence of the experimenter on the premises for 30 s (when the experimenter suspended the item and repositioned it for interaction with the animals) did not affect the interactions of the individual cats with the enrichment item. This may be due to methodology that allowed momentary interruption (of only 30 s) of the animals that were interacting with the item at the moment. Regardless, the presence of a human did not affect the interaction of the animals with the enrichment items in our study; human contact is crucial for satisfactory management and constitutes fundamental enrichment for captive cats (Geret et al., 2011; DeLuca and Kranda, 1992; Rochlitz, 2002). The number of items (one or three) significantly affected the durations and frequencies of interactions with the enrichment item(s). This result emphasises the need to consider the quantity of enrichment items to benefit as many individuals as possible (Dantas-Divers et al., 2011). Compared to trials that involved only one item, the presentation of three items increased the durations and frequencies of interactions and significantly reduced aggression, which was already low because the colony was stable at the time of our study. In a study of a stable colony of domestic cats that was similar to our study, Dantas-Divers et al. (2011) found no relationship between agonistic behaviour and the use of environmental enrichment or food (i.e., a puzzle feeder). These authors concluded that aggressive behaviour is linked to stress and emotional
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states such as fear, anxiety and pain rather than behaviours that indicate social position in the group or priority access to resources. Within the same colony, cats have distinct preferences in terms of environmental conditions, activity levels and social interactions with the other cats and humans (Bradshaw et al., 2000; Crowell-Davis et al., 2004; Geret et al., 2011). Studies aimed at identifying the individual differences within the colony assist in understanding the overall needs for the care of the group. Bradshaw et al. (2000) described the differing preferences shown by domestic cats for new food. Feaver et al. (1986) used a qualitative evaluation method to detect individual differences in two laboratory cat colonies, and Ellis (2009) stated that it is necessary to assess individual differences when applying behavioural enrichment to cats to ensure that the largest number of cats benefit from the stimuli. In this study, we verified whether these individual differences really existed within the target cat colony by observing how individual cats worked towards a certain enrichment item. Some of the cats interacted with the enrichment item more frequently, whereas others interacted with the item moderately. Two hypotheses can be proposed for why the animals did not interact with the item at all: first, because they were not interested in the food (Bradshaw et al., 2000) or second, because the other individuals prevented their access to the item (Dantas-Divers et al., 2011; Durr and Smith, 1997; Knowles et al., 2004). The cats that interacted with the item more intensely showed a higher frequency and duration of interaction and a lower latency than the mean value obtained for the colony; in other words, they monopolised the item. The negative Spearman correlation between frequency and latency corroborated these observations: the lower the latency for interaction with the enrichment item is, the higher the frequency of interaction with it. The individuals that interacted with the item more promptly also interacted more frequently, indicating that animals that did not have access to the enrichment item were somehow unable to work towards the item due to a monopoly held by the most interactive individuals. We also noted a significantly increased frequency and duration of interaction with the enrichment item in MA1B, compared with trial MA1. Therefore, the absence of the most interactive animals provided other individuals with more opportunities to interact with the item. An increase in interaction when we introduced three items instead of one item, which demonstrates that more animals can interact with the enrichment item in the presence of a higher number of items or in the absence of monopolising individuals, had also observed. Taken together, these observations dismiss the previous hypothesis that cats do not interact with the item because they are not interested in the food. In fact, our findings, that some cats had little or no interaction with the enrichment item, reinforce the assumption that some individuals restrict the access of other animals to the item (Baron et al., 1957; Knowles et al., 2004) and confirm our hypothesis that colonies have a pre-determined order to enrichment access. A stable social environment does not imply stability in the differences among individuals; a dominating animal
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does not dominate all types of situations or activities (Durr and Smith, 1997). Individuals’ dominance, monopolisation or priority to access resources has been studied and exhibits a complex structure. By analysing parameters of subtle agonistic behaviour, Knowles et al. (2004) observed a complex ordering of animals’ access to a food bowl. While determining the overall ranking of the colony, regarding interaction with enrichment, we observed that top-ranked individuals dominated the interaction with enrichment. To ensure adequate management and welfare of confined animals, it is fundamental to understand how individuals behave socially and how relationships among animals affect their access to resources (Dantas-Divers et al., 2011). Thus, by introducing feed enrichment, we identified how the group organises access to the food resource and how some individuals can monopolize the enrichment. Because of the difficulty of finding more than one colony under the same composition, housing and social stability conditions, which are fundamental aspects for the replication of the study, the group we examined proved to be satisfactory for achieving the proposed goals, and this supposition is supported by the statistical evidence we have presented. Continuing along these lines, future studies should focus on the methodology of applying environmental enrichment in confined animal groups. Such methodology is essential for ensuring that the techniques used are effective and appropriate to benefit individuals in a homogeneous and balanced way. 5. Conclusion Within confined spaces, captive domestic cats follow a priority order to access resources such as environmental enrichment items. Certain individuals monopolise the resource, limiting the approach of other animals to the item. Therefore, we suggest that making a larger number of items available throughout the premises enriches large colonies more appropriately and facilitates more equal access to the enrichment. When implemented with careful methodology and detailed knowledge about behavioural differences within species, feed enrichment can be an efficient strategy to promote natural behaviour, which is essential for animals living in confined or restricted environments. Acknowledgements The authors would like to thank the owners of the shelter/cattery for providing the animals and study site, MSc. and PhD. César Augusto Sangaletti Terc¸ariol for the statistical analyses, and the Coordination for the Improvement of Higher Education Personnel (Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior—CAPES) for financial support. References Altmann, J., 1974. Observational study of behavior: sampling methods. Behaviour 49, 227–267. Baron, A., Stewart, C.N., Warren, J.M., 1957. Patterns of social interaction in cats (Felis domestica). Behaviour 11, 56–66.
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