1 Introduction

Chimpanzees (Pan Troglodytes) have long been subjects of extensive research due to their genetic and phenotypic similarities to humans (Padrell et al. 2020). However, this profound interest in chimpanzees has led to their exploitation in entertainment industries or by private owners. Some European countries have imposed complete (e.g., Scotland, Belgium, Sweden) or partial (Spain) bans on wild animals in circuses, whereas other countries have abstained from any regulation pertaining to animal use for entertainment (e.g., Italy, France) (Eurogroup for Animals 2021). Despite bans on the import of exotic animals, the illegal wildlife trade still thrives, and among apes, the live trade of chimpanzees dominates the market, with an estimated annual global market value from US$1.6 million to US$6.4 million (Arcus Foundation 2021; Feliu et al. 2022). Private owners often acquire these illegally traded chimpanzees as pets, housing them under inadequate conditions, with minimal exposure to other chimpanzees (Freeman and Ross 2014). When the chimpanzees reach maturity, the owners frequently seek to part with them, as they can no longer confine the animals in small cages nor control their behavior (Feliu et al. 2022).

Chimpanzees exploited as pets or entertainers typically endure unfavorable living conditions, including housing in unsuitable environments, temporary or permanent social isolation from conspecifics, and inadequate diets, to name a few. Consequently, they tend to develop and exhibit abnormal behaviors (Figure 1), that is, behaviors that deviate from the norm for wild chimpanzees and may be associated with psychiatric disorders described in humans such as anxiety, depression, and posttraumatic stress disorder (Brüne et al. 2006). Rehabilitation of these individuals is a protracted process, and they likely require long-term specialized care (Crailsheim et al. 2020; Feliu et al. 2022). Thus, the relocation of chimpanzees to primate sanctuaries provides them with a safe and supportive environment where individuals can live in a social space with conspecifics and receive professional care. In this context, the Fundación MONA (Fundaciónmona.org 2023) is a wildlife sanctuary located in Northern Spain that has been rescuing and rehabilitating chimpanzees and Barbary macaques since 2001. The center is part of the European Alliance of Rescue Centers and Sanctuaries (EARS.org). At MONA, the treatment of primates is guided by four principles, which include (1) the provision of suitable housing, social interaction, and (2) species-appropriate activities, (3) knowledge of individuals' histories, and (4) minimal human interaction—only arranged visits and veterinary support (Llorente et al. 2015). MONA offers an ideal setting for an observational, noninvasive behavioral investigation that respects the chimpanzees' welfare, as there are few human visitors, and even those visitors were shown to have minimal impact on the animals' behavior. For instance, a study by López-Álvarez et al. (2019) found that human visits only had a minor effect on the chimpanzees' daily routines, primarily leading to increased human interaction behaviors—91.9% of which were positive or neutral, such as the chimpanzees closely observing visitors.

The impact of past negative events on chimpanzee behavior has been previously investigated, revealing varied outcomes based on different stressors and communities (Brüne et al. 2006; Bloomsmith et al. 2006). Captive-born chimpanzees may experience an environment with more external stimuli and peers' social interactions, and develop enhanced social skills compared to their wild-caught counterparts (Davenport, Rogers, and Rumbaugh 1973; Llorente et al. 2015; Crailsheim et al. 2020). However, an early study by Suomi, Harlow and Kimball (1971) on rhesus macaques showed that individuals born and reared in laboratory settings under socially restrictive conditions displayed higher levels of rocking, self-biting, and self-clasping compared to individuals caught from the wild within their first 2 years of life. While the specific dynamics of laboratory-born rhesus macaques raised in partial isolation may differ from those of chimpanzees born and raised in captivity under non-laboratory conditions, it is important to acknowledge that captivity conditions can sometimes be associated with social deprivation. Therefore, some captive-born chimpanzees, particularly those raised in inadequate facilities and in isolation, could also experience more social deprivation, lacking access to appropriate peer interactions.

Captive chimpanzees can be housed in a wide range of contexts, often dictated by human use or circumstances. These contexts include zoos, research laboratories, sanctuaries, and private ownership settings, and each context presents unique challenges for the animals' welfare and behavioral development (Bradshaw et al. 2008; Llorente et al. 2015). In the current study, we focus on rescued chimpanzees who were previously housed as pets or entertainers. We categorized the subjects as “entertainment” if they had been primarily involved with circuses and/or commercial agencies; and “pet” if they had been kept in human households for exclusively private purposes (‘entertainment’ animals may also have been housed in the trainer's house during youth).

The distinction between the effects of experience as pet and entertainment chimpanzees remains unclear. Both groups are highly exposed to humans, a factor known to elevate stress levels in captive settings, and reduce behavioral diversity (Freeman and Ross 2014; Jacobson et al. 2017; Kühl et al. 2019). Previous research suggests that performer chimpanzees may exhibit higher behavioral competence correlated to the enriched environments they inhabit and the potential for conspecific housing (Freeman and Ross 2014; Llorente et al. 2015). However, they also might be subjected to a stricter training routine than pet animals, including negative reinforcement, such as training chimpanzees to avoid interactions with whips or sticks to increase the frequency of desired behaviors in a circus show (Iossa, Soulsbury, and Harris 2009).

Although Baker (2000) found no difference in the levels of abnormal behaviors exhibited by old versus younger captive chimpanzees, more recent literature indicates that older captive chimpanzees display more abnormal behaviors than their younger counterparts (Neal et al. 2019b). Moreover, Veenema et al. (1997) recorded a significant increase of stress-related behaviors with age in long-tailed macaques housed in captivity. However, these do not represent analyses of the influence of the duration of inadequate treatment experiences on such behaviors in chimpanzees. Reimers, Schwarzenberger and Preuschoft (2007) demonstrated that the duration of deprivation impacts former laboratory chimpanzees' personalities and coping strategies. Indeed, the individuals who were isolated earlier in life and for a longer period showed a higher stress response during rehabilitation, suggesting that former pet and entertainer chimpanzees could show a similar pattern.

Extensive research underscores the importance of a social environment for typical chimpanzee development during infancy, emphasizing the need for a mother figure, whether human or conspecific, in early development (Bloomsmith et al. 2006; Botero, MacDonald, and Miller 2012; Ongman et al. 2013; Maki, Fritz, and England 1993). Particularly, captive chimpanzees who underwent an early impoverished rearing have been shown to develop stereotypic behaviors, including rocking and self-clasping, and cognitive and social deficits that persisted after many years of environmental enrichment and social group maintenance (Menzel, Davenport, and Rogers 1963; Davenport 1963; Turner, Davenport, and Rogers 1969; Davenport, Rogers, and Rumbaugh 1973). Moreover, early responsive care, supporting the development of species-typical socio-emotional and communicative skills, was found to positively impact the emotional and cognitive development of captive chimpanzees (van Ijzendoorn et al. 2009).

Early social deprivation has been directly linked to heightened anxiety levels in chimpanzees (Ortín et al. 2019; Ferdowsian et al. 2011), marmosets (Cinini et al. 2014), and rhesus macaques (Kempes et al. 2008). Additionally, studies demonstrated the advantages of housing larger groups of chimpanzees together to reduce aggression and anxiety-related behaviors (Neal Webb, Hau, and Schapiro 2019a; Baker and Easley 1996; Baker 2004). Together, this evidence highlights the lasting effects of disrupted social experiences and the critical role of group dynamics in mitigating those effects and promoting well-being.

The current research aims to add to existing literature on abnormal behavior in chimpanzees by providing a more detailed description of how early life experiences impact the current behaviors of rescued chimpanzees, especially by examining the link between their age at rescue and their social condition pre-rescue, as well as the explicit comparison of pet and entertainment chimpanzees. Indeed, the comprehensive array of information available on the chimpanzees' past allowed us to perform an examination of the diverse factors contributing to abnormal behavior, whereas previous research often lacked such detailed data about the animals' history.

In this study, we investigated the correlation between chimpanzees' individual history and abnormal behavior observed in the study period, addressing key questions regarding the impact of origin, early history, age at rescue, and social conditions before rescue. Based on the previously presented literature, we predicted that wild-born chimpanzees would spend more time displaying abnormal behavior than their captive-born counterparts, whereas former pet chimpanzees were expected to show more abnormal behavior compared to those involved in entertainment. We also predicted that the duration of inappropriate conditions would correlate with abnormal behavior, especially in older captive chimpanzees; and that social rearing would mitigate the display of abnormal behaviors compared to chimpanzees raised in isolation.

Beyond enhancing our understanding of abnormal chimpanzee behavior, this research has broader implications for animal welfare, emphasizing the need to raise awareness about the consequences of exploiting wild primates for entertainment or private ownership. Overall, our study provides valuable insights into how rescued chimpanzees' behavior may be impacted by past inadequate living conditions, highlighting the importance for sanctuaries and zoos to consider each individual's previous history to better support their physical and mental wellbeing post-rescue.

2 Methods

3 Results

3.2 Social Housing Can Mitigate the Percentage of Scans Spent Displaying Abnormal Behavior in Older Rescued Animals

The analysis of the interaction effect of the age at rescue and the chimpanzees' previous social conditions revealed that for individuals who grew up surrounded by peers, the percentage of scans spent displaying abnormal behavior did not differ based on the age at which they were rescued (slope = −0.004, std error: 0.01), whereas chimpanzees who were isolated beforehand showed an increase in the percentage of scans spent displaying abnormal behavior with the increase of age at rescue (slope = 0.18, std error: 0.05). The model revealed a statistically significant difference (F_1, 4 = 11.98, p = 0.03), and the residuals were normally distributed (W = 0.90, p = 0.23) (Figure 2). The full model output is presented in Table S2.

4 Discussion

We explored the connection between individual histories of chimpanzees at the MONA sanctuary and the manifestation of abnormal behaviors during the study period. Our results showed that social isolation before rescue significantly increased the percentage of scans spent displaying abnormal behavior in chimpanzees rescued later in life. Moreover, this effect could be almost entirely mitigated if these animals were held in social groups before their rescue (Figure 2). This aligns with existing research suggesting that prolonged exposure to trauma has lasting effects on chimpanzee behavior (Kalcher et al. 2008; Kalcher-Sommersguter et al. 2013), which have been compared with complex posttraumatic stress disorder (C-PTSD) in humans with behaviors such as social withdrawal and self-harm (Ferdowsian et al. 2011; Herman 1992; Dyer et al. 2009; Lopresti-Goodman, Kameka, and Dube 2012; Bradshaw et al. 2008; Cantor and Price 2007). The implications of this finding reinforce the well-established importance of socialization during infancy (Lopresti-Goodman, Kameka, and Dube 2012; Crailsheim et al. 2020; Kalcher-Sommersguter et al. 2015; Snyder et al. 1984) and adolescence (Reddy, Sandel, and Dahl 2022) for animal psycho-social development.

Our study did not find differences in abnormal behavior among wild- or captive-born individuals. This partly contradicts prior expectations that the higher level of social capacities shown by captive chimpanzees may correlate with less time spent displaying abnormal behavior and highlights the nuanced nature of individual experiences. One potential reason for the lack of observed differences is that we did not have information on the age at which the wild-born chimpanzees were captured and placed in captivity, which may be a critical factor in understanding behavioral differences between these groups. Likewise, our data showed no differences between abnormal behaviors displayed by pet versus entertainment chimpanzees. A possible explanation arises from the labeling of individuals based on their primary roles as either pets or entertainers, whereas the practical reality is that most animals were involved in both capacities to some degree, complicating the clear differentiation of the influence of the two categories. Alternatively, the lack of observed differences between pet and entertainment chimpanzees may be attributed to both conditions being equally detrimental, leading to uniformly poor outcomes. While some of our comparisons did not reach statistical significance, certain trends may still be biologically meaningful. Notably, previously isolated chimpanzees displayed abnormal behaviors approximately 10 times more frequently than their previously peer-housed counterparts. This difference, although not statistically significant, could reflect the long-term impact of early-life social deprivation. These results underscore the complexity of factors contributing to abnormal behavior (Birkett and Newton-Fisher 2011; Nash et al. 1999; Goodall 1986; Whiten et al. 1999; Hook et al. 2002) and highlight the need for individualized care.

Moreover, it is important to mention that the levels of abnormal behavior recorded for 6 out of the 10 subjects in this study were notably low, with abnormal behaviors observed in fewer than 1% of scans for these individuals. This rate is lower than that reported for other captive chimpanzee population; for example, Wobber and Hare (2011) observed coprophagy and rocking in more than 6% and 4% of the total scans, respectively, in a group of 14 chimpanzees housed in at the Leipzig Zoo.

Overall, our findings provide valuable insights into the intricate relationship between individual life histories and abnormal behavior in chimpanzees. Future research addressing the effectiveness of different enrichment strategies in mitigating abnormal behavior could enhance our understanding and contribute to the well-being of chimpanzees in sanctuary and zoo settings (Llorente et al. 2015; Feliu et al. 2022; van Leeuwen, Bruinstroop, and Haun 2022; Reimers, Schwarzenberger, and Preuschoft 2007; Kranendonk and Schippers 2014). Enrichment has been shown to enhance species-typical behaviors, reduce agonism and stress-related behaviors (Padrell et al. 2021; Bloomsmith and Lambeth 2000; Pomerantz and Terkel 2009; Yamanashi et al. 2016), whereas other studies did not find significant differences in behaviors correlated to enrichment, and highlighted the variation among individuals (Olsen et al. 2020; Greeson et al. 2022).

It is important to interpret our results with caution, because we had a limited sample size of 10 individuals equally divided into two groups. We also acknowledge both limited generalizability of the findings to other captive populations and observer bias as potential limitations of the study. Although observer bias is an inherent risk in observational research, at MONA we implemented a three-step quality control and interobserver reliability testing protocol to reduce to the minimum the influence of observer bias. These factors should be considered when evaluating our conclusions, and future studies should aim to address these limitations by incorporating larger, more diverse samples. Our findings are consistent with existing literature on the matter, but more data are necessary for conclusive inferences about the relationship between abnormal behavior, age at rescue, and sociality before rescue for other chimpanzee groups as well as other primates.

5 Conclusion

Our findings prompt a broader consideration of the implications for primate welfare, urging a comprehensive approach to rehabilitation and care practices in zoos and sanctuaries. Caregivers need to learn to understand the effect of experiences pre-rescue on the individuals' well-being, and how to possibly reduce such impact. For instance, they could pay more attention to the needs of individuals rescued later in life and isolated before rescue, as these chimpanzees may exhibit higher levels of abnormal behavior and face greater challenges in social integration. Additionally, monitoring and supporting their mental health through behavioral assessments and enrichment strategies could help mitigate the effects of previous inadequate treatment and improve their overall quality of life.

Author Contributions

Emma Chen: conceptualization (lead), data curation (lead), formal analysis (lead), investigation (equal), methodology (lead), writing–original draft (lead), writing–review and editing (lead). Giulia Pipolo: formal analysis (supporting), visualization (supporting), writing–review & editing (supporting). Dietmar Crailsheim: data curation (equal), methodology (equal), supervision (equal), writing–review and editing (equal). Juliano Morimoto: formal analysis (supporting), project administration (equal), supervision (equal), writing–review & editing (equal).

Ethics Statement

The collection of data was based purely on behavioral observations and was conducted in accordance with all national and institutional guidelines for the care and management of primates as established by Fundación MONA, the Association for the Study of Animal Behavior/Animal Behavior Society and the Spanish Government (RD 53/2013).

Conflicts of Interest

The authors declare no conflicts of interest.