Animal personality, defined as behavioral differences between individuals that are consistent over time and across contexts [1
], is one of the most emerging subjects in behavioral research [2
]. Many authors agree to consider differences in animal personality as the result of adaptive evolutionary processes [3
] and to occur in a wide range of taxa [4
]. Moreover, recent findings suggest that individuals differ consistently in their behavioral tendencies and that the behavior in one context is correlated with the behavior in multiple other contexts [6
]. Research into animal personality has grown over the last decade as its relevance to animal health and welfare has become more apparent [7
]. Personality has been used also for aspects of captive management, including decreasing stress [8
], increasing positive health outcomes [9
], successful breeding, also in terms of infant survival [10
]. For wildlife management, determining inter-species differences in the personality traits of communally housed animals could be of great help to optimize the use of resources, in order to improve animal welfare [12
]. In group-living species, integrated decisions made by individuals result in collective behaviors [13
], which may, in turn, influence interactions between individuals and shape the resulting social system [14
]. There is evidence that animal groups may exhibit coordinated behavior and make collective decisions based on simple interaction rules [2
]. It has been described that in a flock or a colony; birds tend to exhibit behavioral synchrony, maintaining similar behavior at approximately the same time throughout the group [15
]. Within-group responsiveness provides important benefits for individual group members, allowing for cohesion and consensus to form in movement decisions [2
], predator avoidance [17
] and resource exploitation [18
]. In addition, wild penguins have exhibited within-group synchrony: rockhopper (Eudyptes chrysocome
) and Adélie (Pygoscelis adeliae
) penguins synchronized their diving to increase fishing success [19
], and cooperative foraging has been reported for African penguins (Spheniscus demersus
], while little penguins (Eudyptula minor
) display group behavior arriving at the colony and departing to sea, as a predator avoidance strategy [18
]. What about captivity? Some of the behaviors manifested in captive animals may be a consequence of regimented schedules, since captive animals are usually managed at a specific time and place, and fed with similar food items [15
To date, the link between social behaviors expressed by groups and personality remains poorly explored. Recent studies on wild birds have suggested that individual-level personality traits influence the individual degree of use of social information, attraction to conspecifics, and attitude to act as leaders/followers [2
]. At the population-level, Kurvers et al. [21
] demonstrated that the use of social information in natural populations of barnacle geese decreased with increasing boldness, indicating that personality differences can affect behavioral decisions related to spatial distribution and group formation processes. Michelena et al. [16
] investigated the links between animal personality and the individual and collective decision-making processes in groups of sheep. They noticed that shy individuals were found to have a higher social attraction parameter and graze closer to others.
Does interspecific group life impact on the expression of personality traits on communally housed species? There are no data published on this subject. In this work, we wanted to verify the hypothesis that the penguins of three different species, despite being hosted in common in a dedicated enclosure, express different traits of the personality, and if it is possible to trace, for some traits, a profile that characterizes the species. For this purpose, we have considered three species of penguins, housed together at Royal Zoological Society of Scotland (RZSS) Edinburgh Zoo, Scotland, UK. The exhibit houses a colony of gentoo penguins (Pygoscelis papua
), a bachelor group of king penguins (Aptenodytes patagonicus
) and a small colony of northern rockhopper penguins (Eudyptes moseleyi)
. In the International Union for Conservation of Nature (IUCN) Red List of threatened species, gentoo penguins are classified as least concern, with a wild population estimated number of mature individuals of 774,000 and a population trend referred as stable. Gentoo penguins have a circumpolar breeding distribution that ranges in latitude from the Fish Islands on the Antarctic Peninsula (66°01′ S) to the Crozet Islands (46°00′ S). The three most important locations, containing 80% of the global population, are the Falkland Islands (Malvinas), the South Georgia and the South Sandwich Islands) and the Antarctic Peninsula (including South Shetland Island) [22
]. King penguins are also classified as least concern, with a wild population trend referred as increasing; they breed on various sub-Antarctic islands, in the French Southern Territories, Prince Edward Islands (South Africa), Heard Island and McDonald Islands, Macquarie Island (Australia), with small colonies on the Falkland Islands (Islas Malvinas), in southern Chile and in South Sandwich Islands [22
]. Regrettably, northern rockhopper penguins are classified as endangered, with a wild population estimates number of mature individuals of 480,600 and a population trend referred as decreasing. Approximately, 85% of the northern rockhopper penguin global population is found in the Atlantic Ocean, breeding at the Saint Helena, Ascension and Tristan da Cunha UK Overseas Territories. The remaining 15% of the population is found in the Indian Ocean on Amsterdam and St Paul islands (French Southern Territories) [22
According to the Zoological Information Management System (ZIMS), the online database of wild animals maintained in captivity; there are currently 954 recorded gentoos individuals (intended as Pygoscelis papua species), housed in 36 zoological institution around the world (17 European, 15 North American, 3 Asian and Auckland Zoo), 532 king penguins individuals recorded, housed in 34 Zoos (15 European, 7 Asian, 11 north American and Auckland Zoo), and only 155 northern rockhoppers, individuals, housed in 10 institutions (6 European, 1 African and 3 north American).
In a mixed species enclosure, animals are far more intermingled than they would be in the wild and have a limited area in which to maintain different territories. Therefore, we wanted to evaluate whether, in these three species of communally housed penguins, it was possible to highlight specie-specific personality traits, despite the influence of forced cohabitation.
The scope of this project was:
To provide a preliminary evaluation for the personality traits obtained by the questionnaire filled by the keepers;
To investigate if personality traits vary in a sample of three species of communally housed captive penguins;
to investigate if it is possible to identify specie-specific personality trends.
2. Materials and Methods
2.1. Subjects and Housing
The subjects included in the study are briefly described in Table S1
. In total, 43 penguins, randomly selected among the colony housed at RZSS Edinburgh Zoo, Scotland, UK, were considered: 21 northern rockhopper (Eudyptes Moseley
, 11 m and 10 f); 14 gentoo penguins (Pygoscelis papua
, 7 m and 7 f) and 9 king penguins (Aptenodytes patagonicus
, all males).
The Edinburgh Zoo ‘Penguins Rock’ is the refurbished enclosure opened in 2013. It is 85 m long, 30 meters wide and is equipped with a 65-meter-long pool, which is 3.5 m deep at the deepest point. The pool is freshwater, and holds approximately 1.2 million liters of water, filtered via a filtration system. ‘Penguins Rock’ is one of the largest outdoor penguin exhibits in Europe and it hosts a colony of 129 penguins. There is no foliage incorporated into the enclosure, to eliminate the risk of aspergillosis spores affecting the birds. The kings and gentoos are housed together all year round, while northern rockhopper penguins are separated off, in February, and are moved to a smaller ‘creche’ enclosure, attached to the main exhibit, for their breeding season.
The penguins are fed 3 times a day (first thing in the morning, between 2:30 p.m. and 4 p.m. and between 4:30 p.m. and 5:45 p.m.). The breeding gentoos are also given an extra feed before 1 p.m. The penguins are all hand-fed: this allows keepers to have a close visual health check every day on the birds (look inside beaks, look at toenails, eyes, and feather condition) in order to verify the health conditions and plan timely veterinary medical interventions. If necessary, medical treatments are administered hidden into the gills of the fish and then hand-fed to that penguin. In the colony there are also some old age penguins, which need daily diet supplementation. Enrichments are given regularly according to a scheme.
2.2. Personality Assessment
With the purpose of evaluating personality, we decided to acquire trait-rating assessment from the people who know the animals best (zoo keepers). Following the protocol from Chadwick [8
], questionnaires were given to the two keepers who have regular interactions with the penguins, to rate the personality traits of the animals they attend. The test required that the keepers, who both expressed their assessment on all the animals in the study, did not consult during the compilation of the questionnaires. The first part of the questionnaire presented some questions related to keeper’s work, to their interests for the birds (in particular penguins), and to the perception that they have of the personality influence on the animals’ behavior and health. In order to describe penguin behavioral and personality aspects, in the second part of the questionnaire were included 31 adjectives (Table S2
), which were rated on a scale of 1 (trait never exhibited) to 12 (trait always exhibited), depending on how well they described each penguin [23
]. Two keepers completed the questionnaires for each animal.
2.3. Statistical Analysis
Concordance between keepers. Inter-rater reliability (IRR) was calculated for each personality trait as Cronbach’s alpha (CA) (SPSS ver. 24 for Windows). IRRs were calculated separately for each species, and then, in the rockhopper and gentoo penguins, repeated separately for females and males. Only traits with an IRR > 0.5 for at least two species were used in subsequent analyses.
Personality traits. The considered variables were analyzed through descriptive statistics; for each variable, the first, the third quartile, the median value were calculated and then represented by box and whiskers plots (Jamovi for Windows, 0.9.6, Jamovi Computer Software, https://www.jamovi.org/
). The box-whisker plots were performed for the three species and the gender.
Differences in traits by species: In order to evaluate differences between species, every species was analyzed for the aforementioned variables; the differences between species were calculated using the Kruskal-Wallis nonparametric test, followed by Steel-Dwass-Critchlow-Fligner test for multiple comparisons (Jamovi for Windows). The statistical significance was set at p < 0.05. Species were also compared for each personality trait using a generalized linear model (GLM) in R. Normality of residuals was confirmed for all behavioral traits using the R plot function.
Gender differences: for rockhopper and gentoo penguins a glm was used to investigate the effects of gender, species and their interaction in a 2-way ANOVA design.
Multivariate analysis of personality variables: a multivariate Multiple Factor Analysis (MFA) was applied to the variables (R for Windows, https://cran.r-project.org/bin/windows/
) to visualize the differences among species.
2.4. Ethical Statement
All keepers gave their informed consent for inclusion before they participated in the study. The study was conducted in accordance with the Declaration of Helsinki, and the protocol, by its nature, did not require the approval of the Ethics Committee of the Royal Zoological Society of Scotland.
In past years, personality assessment through keeper ratings has been criticized for being too subjective, anthropomorphic and not scientific [25
], since keepers use their impression and knowledge to judge the animals and their behaviors [27
]. In the scientific literature, an increasing body of evidence indicates that keeper ratings are both reliable and valid, and there is also little evidence supporting the contention that ratings are tainted by anthropomorphism [29
]. Kwan et al. [30
] found that the raters were not projecting their characteristics onto their pet dogs, and Weiss et al. [31
] found no differences between ratings of chimpanzee personality obtained from American and Japanese observers, indicating that there was no influence of the cultural backgrounds and of the experiences of raters. Observer ratings have been used in assessing the welfare and personality of farm animals [32
] and the personality of companion animals [33
]. In the same way, keeper ratings can be used to investigate the welfare and personality of zoo animals [23
]. A fundamental condition in personality studies is that the assessment of personality traits must be both reliable and valid [25
]. Raters scoring the animals must agree in their assessments, and this agreement must be confirmed by testing inter-rater reliability [37
]. Therefore, it is fundamental that people who provide ratings for each animal do it independently and do not confer on their answers [25
]. According to that, the experimental setting of our study required that the keepers did not consult during the compilation of the questionnaires, this was designed to provide an assessment of the behavioral characteristics of each individual. The analysis of the questionnaires filled out by the keepers showed an intraclass correlation coefficient which allow to further elaborate the data, since a moderate agreement between the two evaluators was highlighted.
The results obtained in the present study have shown that the keepers knew every penguin very well, and they were able to consistently evaluate their behavioral characteristics [23
]. This data is useful to underline the importance of the professional figure of the zookeeper, which has prominent responsibilities in the daily welfare of the animals [29
In our study, we aimed to analyze the differences in the expression of personality traits of three penguin species housed within the same enclosure, in a controlled environment. The results we obtained indicated that six of the 31 personality traits considered presented statistically significant differences between the species involved. These data point out that the three species of penguins, despite living in close contact, sharing the same enclosure and the same management procedures permanently (or for most of the year), maintain, at least for some personality traits, a species-specific behavioral individuality. Our finding is in accordance with what has been observed by Foerder et al. [15
] in an observational study of a colony of 65 penguins of two different species, chinstrap (Pygoscelis antarctica
) and gentoo (Pygoscelis papua
) housed in the same environment in the Central Park Zoo (USA). Foerder results indicated that the penguins, despite showing a behavioral synchronism and despite the restrictions imposed by captivity, maintained a behavioral species separation.
In the last year, space in zoos is becoming more limited by the necessity to increase individual enclosure size: maintaining more than one species in a single enclosure zoo may increase the conservation return on the infrastructure [39
]. Moreover, it has been highlighted that mixing species in an enclosure is a mean to increase social complexity, which is a paramount aspect of enrichment for many species [40
]. However, this choice also has its downsides: changes in conspecific and species composition can also be a cause of stress. Unlike the domesticated farm animals, zoo animals have not been selected for adaptation to captive condition: conversely, strenuous efforts are implemented specifically to raise animals that behave as similar as possible to their wild living conspecific [40
]. The awareness that the cohabitation of the species involved in this study does not induce the flattening of the expressions of the behavioral traits it could be an excellent index of well-being, which would also be interesting to investigate in other respects.
In these colonies, where different species live together, it would be interesting to evaluate the existence of a link between expression of personality traits and the choice of the reproductive partner, the effectiveness of parental care, and the survival of newborns, topics particularly delicate, especially in species considered vulnerable from the conservation point of view.
This approach could be useful in one of the central missions of the modern zoo: to conserve endangered species through captive reproduction and to educate the visitors to conservation issues.