Gorilla tourism has played a pivotal role in not only fostering the recovery of the endangered mountain gorillas (Gorilla beringei beringei) but also in benefiting coexisting species and local communities. The remarkable success of mountain gorilla tourism has significantly contributed to the conservation efforts within the Greater Virunga Landscape. This is achieved partly by offering economic and social incentives to local populations, thereby reducing their reliance on more invasive and destructive resource extraction practices that could otherwise degrade the habitat and jeopardize the survival of wildlife.

However, gorilla tourism may also pose potential threats to these apes due to the risk of Anthropozoonoses, increased stress levels, and negative impacts on their behaviour. In response to these concerns, the International Union for Conservation of Nature (IUCN) has formulated comprehensive guidelines for great ape tourism aimed at mitigating these risks. These guidelines include prohibiting the participation of individuals exhibiting signs of illness, limiting the number of daily visitors to one group of 8 people (6 tourists and 2 guides) per gorilla group, maintaining a minimum distance of 7 m from the gorillas, and restricting the duration of viewing to one hour.

However, by the end of their gorilla visit, 11 % of tourists remain unaware of the 7-meter guidelines (Weber et al. 2020). Moreover, there is growing evidence to suggest that tourists often spend significantly more time in closer proximity to gorillas than recommended. Additionally, Hanes et al. (2018) reported that out of 136 tourists surveyed, 8 openly admitted to tracking gorillas while feeling ill. Even more concerning, despite being aware of the regulations, 25 % of the respondents indicated that they would still embark on gorilla treks when feeling unwell.

At such close proximity to tourists, it is reasonable to anticipate changes in the behaviour of gorillas. However, the absence of systematic research complicates our ability to ascertain the specific strategies employed by gorillas to cope with (a) the presence of tourists, (b) the distances between tourists and gorilla groups, and (c) the sizes of tourist groups. In particular, it has been observed that short distances to tourists can trigger stress responses and coping mechanisms in macaques, especially when they are in close proximity to large tourist crowds (Maréchal et al. 2016; Marty et al. 2019). Hence, it is plausible to consider that mountain gorillas may employ similar strategies to cope with the pressures of tourist presence.

The primary objective of this study was to explore the behavioural changes in gorillas concerning tourist presence and proximity to tourists. Simultaneously, we aimed to assess the extent to which tourists adhere to the 7-meter rule during gorilla tourism activities. Our specific focus was on understanding how tourists' compliance or non-compliance with this rule might influence gorilla behaviour. Our study focused on identifying behavioural stress indicators and social behaviours among gorillas, with a particular interest in uncovering potential coping mechanisms, such as social buffering. To conduct our research, we embarked on a year-long journey to Bwindi Impenetrable National Park in Uganda, spanning from September 2017 to February 2019. During this time, we closely observed one of the oldest gorilla families that had been habituated to tourist presence. It is worth noting that the majority of this family's members were born after the initiation of the habituation process. Throughout this year-long study, we followed the Rushegura gorilla family, totalling 577 hours' worth of data.

Originally, our study aimed to compare behavioural changes during tourist visits as they related to tourist group size. However, only 4 % of the visits had fewer than 8 people per group, rendering this comparison impractical, and thus, we discarded this approach. The average tourist group size, excluding guides, was 7.7 (± 1.5; N = 297; range: 2-11), while including guides, the mean group size was 13 (± 2.4; N = 297; range: 6-25). The monitoring group size (comprising park staff and researchers exclusively) averaged 5.8 (± 1.8; N = 443; range: 3-11).

Additionally, we initially intended to examine the influence of distances of less than 3 m, 3-7 m, and greater than 7 m to tourists on gorilla behaviour. However, due to tourists spending nearly 60 % of their time within 3 meters of the gorillas, we had to consolidate the categories of 3-7 m and greater than 7 m into a single category (> 3 m) to balance the data between the predictor variables. Specifically, tourist groups spent 59.20 % of their time at distances of < 3 m, 25.63 % at 3-7 m, and 15.17 % at > 7 m away from the focal gorilla, respectively.

Upon analyzing specific behaviours (such as scratching, social interactions, and interactions with tourists), our models have revealed heightened stress indicators during tourist visits and the use of stress alleviation mechanisms.

Percentage of events of all observed types of Human-directed behaviour (agonism, neutral, and avoidance) at the different levels of tourist-gorilla distance, during the tourist visiting hour. A total of 1,120 sessions were recorded in the presence of tourists (182.6 hours).

We found increased self-scratching, particularly among male gorillas who exhibit acute stress when tourists are within a 3-meter proximity. Self-scratching serves as a non-invasive and well-established behavioural proxy for measuring stress. It has been effectively utilized in previous studies involving various wild primate species exposed to tourist crowds and other sources of anthropogenic disturbance. In fact, this method is commonly employed in both captive and wild habitats, including as a dependable measure to evaluate the impact of visitors on anxiety levels in western lowland gorillas (Gorilla gorilla gorilla) in zoos.

Furthermore, by employing both General Linear Models to assess the frequency of pro-social behaviours and utilizing social network analysis with selected metrics like node degree, node strength, and node closeness to thoroughly investigate our hypotheses, our research reveals a consistent pattern. It indicates that gorillas are more inclined to engage in social behaviours and increase cohesion when tourists are present and within 3 m. This behaviour is likely a strategy employed by gorillas to alleviate stress through social buffering, which encompasses their proximity to and interactions with conspecifics, including activities such as grooming, affiliative physical contact, and play.

Additionally, our research findings indicate that gorillas typically respond to close tourist proximity by either engaging in aggressive behaviours or avoiding tourists altogether. Given that tourists often spend the majority of their time in close proximity to gorillas, this presents an imminent risk of potential pathogenic transmission through close physical contact. It is worth noting that animals under stress may have compromised immune systems, further exacerbating this risk. Notably, tourists visiting wild mountain gorillas may not always recognize or admit to experiencing symptoms of illness. Additionally, some tourists could be asymptomatic carriers of diseases, remaining unaware of the potential threat they pose to the vulnerable wild gorilla population.

Furthermore, in the presence of large groups of tourists, with more than eight people per group, tourists tend to cluster together, often at increasingly shorter distances to gorillas. In response to this, gorillas form more cohesive and tightly connected aggregations. In other contexts, rapid transmission of respiratory infections within gorilla groups has been observed, possibly due to the strong social connections between individuals (Morrison et al. 2021). The cumulative effects of shorter distances between potentially infectious humans and more cohesive gorilla aggregations may significantly heighten the risk of cross-species pathogen transmission.

Implications for conservation

Gorilla tourism undoubtedly brings significant benefits to parks and communities across the country, especially those with limited resources. To ensure the continued success of gorilla tourism in a sustainable manner, we recommend revisiting the original regulations that allowed for 6 tourists and 2 guiding park staff per group. Our research findings underscore the critical importance of gorillas being influenced by the proximity of tourists, emphasizing the need for stricter enforcement of the 7-meter rule.

The COVID-19 pandemic may have raised awareness about the potential for new zoonotic diseases among tourists. In addition to the immediate threat to these animals, the potential for repeated infections due to continuous human contact through tourism could lead to the emergence of new virus variants. While recent models suggest that inter-group pathogen transmission is unlikely (Morrison et al. 2021), we propose limiting the number of new habituated gorilla groups or even suspending the habituation of additional groups. This precaution would help ensure that a portion of the wild gorilla population remains free from pathogens and parasites of human origin and preserve their natural social and demographic processes.

With the reopening of the parks and international traveling, wildlife tourism has regained momentum. To ensure a 7-m distance between tourists and gorillas, park staff could enhance their communication efforts by providing more assertive and effective explanations for these regulations. Additionally, ecotourists are inclined to contribute more towards conservation initiatives. Therefore, planning an increase in permit prices could be a viable strategy. This would guarantee (or even increase) enough capital to sustain the activity and benefit the communities while we can work towards ensuring that a portion of the mountain gorilla population remains wild and free.

Raquel F. P. Costa

Adapted from:
Costa, R., Takeshita, R. S., Tomonaga, M., Huffman, M. A., Kalema-Zikusoka, G., Bercovitch, F., & Hayashi, M. (2023): The impact of tourist visits on mountain gorilla behavior in Uganda. Journal of Ecotourism, 1-19. doi.org/10.1080/14724049.2023.2176507
Costa, R. F. P., Romano, V., Pereira, A. S., Hart, J. D. A., MacIntosh, A., & Hayashi, M. (2022): Mountain gorillas benefit from social distancing too: Close proximity from tourists affects gorillas' sociality. Conservation Science and Practice, e12859. doi.org/10.1111/csp2.12859

References
Hanes, A. C. et al. (2018): Assessment of health risks posed by tourists visiting mountain gorillas in Bwindi impenetrable National Park, Uganda. Primate Conservation 32, 123-132
Maréchal, L. et al. (2016): Primates' behavioral responses to tourists: Evidence for a trade-off between potential risks and benefits. Scientific Reports 6, 32465
Marty, P. R. et al. (2019): Time constraints imposed by anthropogenic environments alter social behavior in longtailed macaques. Animal Behavior 150, 157-165
Morrison, R. E. et al. (2021): Rapid transmission of respiratory infections within but not between mountain gorilla groups. Scientific Reports 11 (1), 1-12
Weber, A. et al. (2020): Lack of rule-adherence during mountain gorilla tourism encounters in Bwindi impenetrable National Park, Uganda, places gorillas at risk from human disease. Public Health Frontiers 8 (1), 1-13