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ORIGINAL RESEARCH
published: 13 February 2020
doi: 10.3389/fpubh.2020.00001
Frontiers in Public Health | www.frontiersin.org 1February 2020 | Volume 8 | Article 1
Edited by:
Jessica Rothman,
Hunter College (CUNY), United States
Reviewed by:
Michele Goldsmith,
Southern New Hampshire University,
United States
Anne Eleanor Russon,
York University, Canada
*Correspondence:
Nancy J. Stevens
stevensn@ohio.edu
Specialty section:
This article was submitted to
Environmental Health,
a section of the journal
Frontiers in Public Health
Received: 09 December 2018
Accepted: 02 January 2020
Published: 13 February 2020
Citation:
Weber A, Kalema-Zikusoka G and
Stevens NJ (2020) Lack of
Rule-Adherence During Mountain
Gorilla Tourism Encounters in Bwindi
Impenetrable National Park, Uganda,
Places Gorillas at Risk From Human
Disease. Front. Public Health 8:1.
doi: 10.3389/fpubh.2020.00001
Lack of Rule-Adherence During
Mountain Gorilla Tourism Encounters
in Bwindi Impenetrable National
Park, Uganda, Places Gorillas at Risk
From Human Disease
Annalisa Weber 1,2, Gladys Kalema-Zikusoka 3and Nancy J. Stevens 2, 4
*
1Applied Research and Evaluation, Division of Global Health Protection, Center for Disease Control, Atlanta, GA,
United States, 2Environmental Studies Program, Voinovich School for Leadership and Public Affairs, Ohio University, Athens,
OH, United States, 3Conservation Through Public Health, Entebbe, Uganda, 4Department of Biomedical Sciences, Heritage
College of Osteopathic Medicine, Ohio University, Athens, OH, United States
Mountain gorillas (Gorilla beringei beringei) are an endangered primate species, with
∼43% of the 1,063 individuals that remain on the planet today residing in Bwindi
Impenetrable National Park (BINP) in southwestern Uganda. These primates are at the
heart of a growing tourism industry that has incentivized their continued protection,
but close proximity between humans and gorillas during such encounters presents
well-documented risks for disease transmission. The Uganda Wildlife Authority (UWA)
has developed rules to help protect the health of the gorillas, limiting each habituated
gorilla group to a single 60 min visit each day by a group of no more than 8 tourists,
and emphasizing that humans maintain a >7 m distance from gorillas at all times. A
number of studies have documented that not all tour groups respect these rules. This
project assesses rule-adherence during gorilla tourism encounters at BINP using both
observational and survey-based data collected during the tourism high season between
May and August, 2014. Observational data from 53 treks reveal that groups of 1–11
tourists engaged in gorilla viewing encounters between 46 and 98 min in duration.
Although 96% of pre-trek briefings conducted by park rangers emphasized the need to
maintain >7 m human-gorilla spacing, the 7m distance rule was violated in over 98% (52
out of 53) of the tours examined in this study. Observational data were collected at 2 min
intervals during gorilla-viewing encounters, documenting the nearest distance between
any tourist and a gorilla (n=1,604), of which 1,094 observations (68.2%) took place at
a distance less than or equal to 7 m. Importantly, the 7 m rule was violated in visits to all
of the gorilla groups habituated during the time of the study. In 224 observations (∼14%,
per 1,604 total), human-gorilla spacing was 3 m or less. Survey data (n=243) revealed
promising opportunities to improve tourist understanding of and adherence to park rules,
with 73.6% of respondents indicating that they would be willing to utilize a precautionary
measure of wearing a face-mask during encounters to protect gorilla health.
Keywords: gorilla, primate, tourism, ecotourism, disease transmission, Uganda, conservation
Weber et al. Tourists Violate Rules During Gorilla-Viewing
INTRODUCTION
Mountain gorillas (Gorilla beringei beringei) are an endangered
primate species found in only two isolated forests of central-
eastern Africa, spanning parts of Uganda, Rwanda, and the
Democratic Republic of the Congo (1). Approximately 43%
of the remaining mountain gorilla population inhabits Bwindi
Impenetrable National Park (BINP)1in southwestern Uganda,
and since 1993, a robust tourism industry has developed around
tourists viewing habituated gorilla groups.
The area around BINP is home to some of the densest human
populations on the continent, for example, the Kisoro district
is home to an average of 354 people per km2(2). With one of
the highest population growth rates in the world [population
net gain of 1 person every 22 s, per (2)], Uganda faces long-
term challenges for balancing the growing needs of the human
population with desired outcomes in great ape conservation.
History of Gorilla Tourism Around BINP
Gorilla-viewing tourism was introduced in 1993 as a potential
solution to multiple problems, to generate revenue for the
Ugandan government from gorilla viewing permits with a
portion invested back into local communities, prioritizing gorilla
conservation and offering continued protection of the Bwindi
forest itself (3–6).
In the 1990’s, approximately 3,000 people visited Bwindi
annually. By 2011, BINP was receiving more than 15,000
tourists each year (7), and the numbers have continued to
rise. Habituation of additional gorilla groups has been justified
by increased tourist demand, and to spread the economic
benefits of employment opportunities (e.g., through gorilla
tourism jobs ranging from guides to porters to workers in the
lodging/hospitality sectors) to more communities residing in
different areas of BINP (Figure 1). The census conducted in
2018 estimated a minimum of 459 gorillas in Bwindi forming
50 family groups (1). In 2014, an estimated 42% of the BINP
gorilla population was visited by the public, with habituation
of 12 groups containing 168 gorillas. Indications from ongoing
census efforts indicate that gorilla numbers in Bwindi remain
stable, and the number of habituated groups had increased to 17
by the end of 2018 (1).
Habituating wild gorillas has been encouraged for both
conservation and research purposes. The decision to habituate
a gorilla group usually weighs costs and benefits (8–10).
Benefits beyond revenue generation include protection of gorillas
and their habitats, daily monitoring to identify any gorilla
health issues, and facilitation of detailed research on behavior
and ecology offering enhanced understanding of population
dynamics including births, deaths, and dispersal patterns [e.g.,
(4,11,12)]. Costs of habituation include reduced avoidance of
humans (13), potentially increasing the likelihood of crop raiding
and/or susceptibility to poaching [e.g., (14–16)], and increased
risk of disease spread by close proximity with humans and
livestock (5,7,17–25). This risk is intensified by the high number
1Bwindi Impenetrable National Park General Management Plan, 2014-2023. www.
ugandawildlife.org.
FIGURE 1 | Study location: Bwindi Impenetrable National Park, Uganda. Stars
indicate locations of trekking trail heads.
of international visitors, generating potential for exposure to
foreign infections to which local humans and great apes lack
resistance (21,26–31).
Gorillas, Disease, and the 7 m Distance
Rule
It has been well-documented that the profitable gorilla tourism
industry promoted to facilitate continued protection of gorillas
increases health risks by bringing thousands of people into close
contact with endangered apes (7,17,18,21,32–39). Indeed, the
close genetic relationship that gorillas share with humans renders
them highly susceptible to human-borne illnesses, to which they
have limited or no immunity (17,21,22,35). For example,
Graczyk et al. (34) reported on five juvenile gorillas from a
habituated group in Bwindi, suffering from highly contagious
scabies, similar to infections found in human populations
surrounding the park. And in the early 2000’s, western lowland
gorilla populations decreased by a third after an outbreak of the
Zaire strain of the Ebola virus (40), with additional concern raised
by the potential for disease transmission between chimpanzees
and gorillas (41). Increased contact between humans and
wildlife intensifies the transmission of anthropozoonotic diseases
and parasites (34), making tourists, along with high human
population density around BINP habitats, a profound threat to
the survival of mountain gorillas (5).
Infectious diseases (of which respiratory diseases are the
most common) result in 20% of sudden deaths in mountain
gorillas (20). Concern that apes are particularly susceptible
to human respiratory infections has been well-documented
[e.g., (22)], and studies have explored risks inherent in
human-gorilla interactions [e.g., (5,42,43)]. Three respiratory-
disease outbreaks among habituated chimpanzee populations
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
within Cote D’Ivoire were traced back to two common
human paramyxoviruses, through tissue sampling of deceased
chimpanzees (19), and an outbreak of the respiratory disease
human metapneumovirus (HMPV) was conclusively linked to
the death of a female mountain gorilla in Virunga National Park
that ultimately died of bacterial pneumonia, followed by the
death of her infant likely due to neglect (20).
Diseases that spread from humans to gorillas without
prolonged or direct physical contact are of grave concern,
namely respiratory infections that are transmitted through the air
(35,38). Pneumonia, measles, tuberculosis, influenza, and RSV
(respiratory syncytial virus) infections are considered particularly
dangerous (21). Habituated gorilla groups face potential exposure
to nearly 50,000 visitor-hours per year at Bwindi should all 17
currently-habituated groups eventually be trekked at full capacity
of 8 one-hour visitors per day, not to mention exposure to
trackers, guides, guards, doctors, and rangers. Put another way,
tourism exposes habituated gorillas to more humans per year
than would visit an average person’s house throughout an entire
lifetime (44).
In order to mitigate health risks to both gorilla and human
populations, the Uganda Wildlife Authority has developed rules
to help protect the health of the gorillas, limiting each habituated
gorilla group to a single 60 min visit per day by a group of no
more than 8 tourists (with the insistence that sick individuals
do not trek), and emphasizing that humans maintain a >7 m
distance from gorillas at all times. Of concern is how consistently
these rules are applied (5,37,42,45,46). For example, Adams
et al. (47) reported that although 69% of tourists visiting
chimpanzee populations were aware that ill individuals should
abstain from chimpanzee treks, 17.7% of people engaging in
the treks had symptoms of active infections. And a full 25% of
tourists surveyed during a study in 2011 admitted willingness
to trek gorillas at Bwindi while ill, noting reluctance to give up
an expensive experience and challenges with rescheduling (5).
The same study documented that only about 51% of tourists
at that time reported they were willing to don protective face-
masks to protect gorilla populations from human-transmitted
diseases. Sanbrook and Semple (42) reported that gorillas and
humans interacted in closer proximity than the stipulated 7 m,
for example as close as 2.8 m. A study conducted in 2011
reported instances of direct contact between humans and gorillas,
including those who reported being ill (5). Not all guides are
equally versed in the rationale behind the rules for safely leading
tourists groups, which can result in irregular enforcement of park
regulations (48).
The rationale for the minimum-distance rule that human-
gorilla proximity should never be closer than 7 m relates to the
particular susceptibility of gorillas to airborne infections, and
the fact that a sneezed droplet containing infectious particles
can cross a distance of 6 m in a controlled indoor environment
(49,50). The degree of potential disease or infection exposure is
related to the probability of contact between an infected human
and a gorilla, exposure duration, and the infectivity factor of
the source, a function of the germ carrier’s status, the stage
of the infection, and the source’s behavior, such as uncovered
coughs and sneezes (44). Even light wind can substantially boost
travel distance for aerosol particles, influencing exposure risk for
gorillas dramatically if the wind is blowing in the direction of the
gorillas (44).
Are Masks a Potential Solution?
One way to reduce the amount of disease-carrying aerosol
particles released into the atmosphere is to introduce a
rule requiring tourists to wear protective face-masks during
the tourism experience. Indeed, wearing protective masks is
considered best practice among scientists working in primate
conservation (19,21,51) and this measure is already in place in
The Democratic Republic of the Congo, where tourists regularly
wear protective face-masks during gorilla tourism encounters.
Although only about half of tourists surveyed in 2011 reported
that they would be willing to don a protective facemask to
protect gorillas (5), additional data are required to revisit whether
mask-wearing presents a viable solution for mitigating disease
transmission in BINP at this time.
Objectives of This Study
Existing research on gorilla tourism suggests that additional data
are also needed in order to better assess whether irregularities
in rule adherence occur that could intensify risk of human-
gorilla disease transmission risk during tourism encounters. As
previously noted, BINP rules stipulate that only 8 tourists may
trek a particular gorilla group each day, with tourism encounters
limited to 60 min, and human-gorilla spacing >7 m. Based on
previous studies and our own observations, we hypothesize
tourists will break the 7 m rule by coming in closer contact with
gorillas during their trek, regardless of being briefed beforehand
to maintain this distance. In 2014, our team set out to explore 7 m
rule adherence in gorilla tourism encounters at Bwindi, recording
also the number of tourists per trekking group and the duration
of the gorilla viewing encounter. Possible explanations for 7 m
rule violations include that tourists may be unaware of the rule,
they may violate the 7 m rule accidentally, they may choose to/be
encouraged to move closer than 7 m to better view the gorillas,
and/or habituated gorillas may themselves approach tourists.
This study documents adherence to Uganda Wildlife Authority
gorilla-trekking rules and regulations during tourism encounters
in BINP through the evaluation of field-based observations of
informational briefings and subsequent tourist—gorilla spacing,
together with a questionnaire survey administered to explore
tourist perception and attitudes about disease transmission and
prevention measures.
STUDY SITE AND METHODS
Study Site
Bwindi Impenetrable National Park (BINP) is located in
southwest Uganda in eastern Africa (Figure 1). The area has
received focused governmental protection since 1932, and by
1964, the reserve was given added protection as an animal
sanctuary in order to protect the mountain gorillas living within
the area. It was officially gazetted as a national park in 1991, with
regulated gorilla trekking commencing in April 1993.
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
Data Collection
Data collection for this study was conducted in BINP by
accompanying tourist groups during their pre-trek briefings and
gorilla viewing visits, and included the following observations:
number of tourists per group, number of individuals per
trek (including tourists, guides, guards, porters, researchers),
content of pre-trek briefings by BINP staff (specifically, whether
or not the 7 m distance rule was explicitly noted by park
staff, and whether human–gorilla disease transmission risks
were discussed), duration of “gorilla hour” viewing encounter
(according to the rules of BINP, once tour groups have trekked
to the location of a habituated gorilla group, the amount of
time tourists are allowed to spend viewing gorillas is limited
to 60 min), duration of trek (which varied depending on
starting point, local topography, and distance from gorilla group;
trek here is defined as the travel from park headquarters
to the gorilla viewing area, plus the “gorilla hour,” plus the
travel back to the park headquarters), and estimated distances
between gorillas and humans during the viewing encounters
(including tourists and park staff). Occasionally the number of
non-tourists (tourists, guides, guards, porters, and researchers)
accompanying the group fluctuated during an experience; these
cases were recorded as missing data. Data were collected by
AW during 53 separate gorilla trekking tourism encounters,
sampling visits to all 12 gorilla groups habituated at the time
of the study, with densest sampling focused on the three most-
frequented Buhoma groups: Habinyanja group (n=15 treks),
Mubare group (n=14 treks), and Rushegura group (n=
12 treks).
During all gorilla tourism encounters, scan estimates of
human-gorilla proximity were conducted at 2 min intervals
recording the smallest distance between any one human and any
one gorilla in the tourism encounter. Human-gorilla distances
recorded during 2-min scans were placed into 11 distance
categories: <1, 1.1–2, 2.1–3, 3.1–4, 4.1–5, 5.1–6, 6.1–7, 7.1–8,
8.1–9, 9.1–10, and >10 m, as human–gorilla spacing could not
be accurately estimated at a distance over 10 m due to dense
vegetation in the study area. Prior to the study, the estimation
of vertical, horizontal, and oblique distances were practiced
and independently validated in habitats of differing complexities
using calibrated measurement distances to ensure validity and
reliability of distance estimates in the variable habitats of the
gorilla groups visited by the tourist groups. It was occasionally
necessary to shift position in order to record the distances
between humans and gorillas through the obscuring vegetation.
Occasionally it was not possible to record an observation due
to movement patterns of the tourists/tourist group and/or
obscuring vegetation; those cases were recorded as missing data.
At no time did we violate the 7 m rule ourselves in collecting the
data for this study.
Assessing Adherence to the “7 m
Distance” Rule
Data on human-gorilla spacing were organized based on the
date of the trek and the name of the gorilla group visited. The
number of 2-min scan observations of human-gorilla spacing
were summed by distance categories and divided by the total
number of observations in that trek to obtain proportional
data for each distance category. The time at first 7 m distance
violation from the beginning of each gorilla encounter was
recorded. The number of sequential distance violations in a
given gorilla-viewing encounter was calculated as a proxy for
duration of violation. When the distance between humans and
gorillas dropped to 3 m or less, it was recorded, whether or not
it coincided with 2 min scan observations. It was also noted
whether it was a human that closed the distance from a gorilla,
or vice-versa, for comparison with such close interactions as
recorded by Sanbrook and Semple (42).
Because we hypothesized a greater opportunity for rule
violations in groups with more tourists, and that tourists trekking
for longer to view a given gorilla group might feel more entitled
to move closer to the gorillas, Spearman rank correlations were
calculated to assess relationships between the proportion of 7 m
rule violations out of the total observations in a given trek
and the following variables: number of tourists per trekking
group, and duration of the trek (significance levels set at p=
0.05). Linear logistic regression models using a quasi-binomial
family to account for over-dispersion of proportional data were
run through the statistical analysis platform R to examine the
relationship between the response variable (proportion of rule
violations out of the total observations in a given trek) and
the following predictor variables: number of tourists in trekking
group, and duration of the trek.
Evaluating the Knowledge, Perceptions
and Attitudes of Tourists Toward the Rules
of BINP
For each trek, we documented content of the mandatory pre-
trek briefing provided by the staff of BINP, namely: (1) whether
the 7 m distance rule was mentioned in the briefing (yes or no),
and (2) whether human–gorilla disease transmission risks were
discussed (yes or no).
Subsequent to the gorilla-viewing encounters, tourists were
asked to complete a voluntary five question survey. The
questionnaire gathered yes/no data on tourist knowledge and
attitudes regarding ecotourism rules relating to health and safety,
including (1) whether tourists believed they were educated about
the 7 m rule, (2) whether they believed that they maintained
a 7 m distance from the gorillas, (3) whether they thought
that such a rule was necessary, (4) whether the rule detracted
from their tourism experience, and (5) whether or not they
would be willing to wear a protective face-mask during gorilla
viewing to prevent transmission of infections. A smaller number
of tourists responded to the fifth and final question as it was
added to the survey partway into the study at the request of
coauthor GKZ; every participant who received this question
on the survey provided a yes/no response. The survey was
administered in English, by far the most widely spoken language
among tourists in the study, hence a notable limitation of the
present study is that it only examines responses of English-
speaking tourists. Only adults 18 years and older were asked to
complete survey questionnaires.
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
Aggregate data on self-reported knowledge and attitudes
were gathered from tourist survey responses and discussed
in the context of observed nearest human-gorilla distances
during the study, as well as with percentages of pre-trek
“rules and regulations” briefings delivered by BINP staff that
addressed the 7 m rule and risks of human-gorilla disease
transmission, in order to explore the need for improved
communication about safe tourist-gorilla spacing during gorilla-
viewing treks.
RESULTS
Tourist Informational Briefings by Park
Staff
Gorilla trek observations were conducted 53 times between 25
May and 8 August 2014. Pre-trek briefings were delivered in
English and varied notably in length and content, generally
providing information on the history of the park, the history
of gorilla habituation, rules that tourists are expected to follow
during the trekking experience, and the reasons why the rules
are in place. The overwhelming majority of pre-trek briefings
examined in this study, 96.2% (51/53) indicated the rule of
maintaining a distance of at least 7 m from the gorillas at all times,
and 81.1% (43/53) discussed the risk of disease transmission
between humans and gorillas in close proximity (Table 1 and
Figure 2A).
Evaluating Adherence to the “7 m
Distance” Rule and Instances of Close
Proximity
Of the 53 tourism encounters examined in this study, only a
single trek lacked violations of the 7 m distance rule by any tourist
for the entirety of the gorilla viewing experience (Table 1 and
Figure 2B). Of the 1,604 nearest-neighbor observations, 1,094
observations took place at a distance less than or equal to 7 m, i.e.,
31.8% of observations were in accordance with the 7 m distance
rule, and 68.2% of observations violated the 7 m distance rule
(Figure 2C). In all observations in the study, tourists were the
closest humans to the gorillas, although guides were often very
near the closest tourist, moving vegetation away from the line of
sight or pointing to the nearest gorilla.
Notably, 277 all-occurrence observations recorded human–
gorilla spacing at a distance of 3 m or less, 224 of these
observations occurring at 2 min sampling intervals. Of these
violations, 165 instances (59.6%) were initiated by gorillas, and
112 instances (40.4%) were initiated by tourists; of the latter,
some instances were facilitated by guides, in order to obtain
a clear line of sight for photography. Human–gorilla spacing
at <3 m was recorded during tourism encounters with eight
of the 12 gorilla groups habituated at the time of the study,
including five groups trekked only once or twice during the study
(Table 1). Human–gorilla spacing at <3 m was not observed
during treks with the following groups: Oruzogo (3 treks),
Nkuringu (1 trek), Nshonge (1 trek), and Busingye (1 trek),
although the 7 m rule was violated in all of the treks with those
four groups (Table 1).
Number of Tourists per Group, Duration of
Trek, and Duration of “Gorilla–Hour”
Viewing Experience
The number of tourists per gorilla encounter averaged 7 (sd
=2, range =1 tourist−11 tourists), with the total number of
people per trek including park staff averaging just over 16 (sd
=4.15, range =7–23 people). Overall trek durations (trekking
to and from gorilla viewing position plus gorilla viewing time)
were highly variable across tourist groups, averaging 229 min
(sd =72.07, range =89–411 min). In this study, the actual
amount of time tourists spent viewing gorillas also varied. The
average “gorilla hour” was 66 min in duration (sd =9.44, range
=46–98 min).
Spearman rank correlation analysis revealed a weakly positive
but non-significant relationship (rs=0.15; p=0.269) between
the proportion of rule violations in a given trek and the
number of tourists within that trekking group, and a marginally
significant negative relationship between the proportion of
rule violations in a given trek and duration of the time
spent trekking to the gorilla-viewing location (rs= −0.27;
p=0.052). No significant predictors of rule violations were
recovered by logistic regressions performed in R predicting the
response variable (proportion of rule violations out of the total
observations in a given trek), based on number of tourists per
trekking group and duration of the trek to the gorilla-viewing
location (Supplementary Table).
Timing and Duration of 7 m Rule Violation
During Tourism Encounters
During the 52 encounters with 7 m rule violations, the first
violation of the 7 m distance rule occurred on average 9.8 min
into the encounter (sd =13.8 min; range =0–46 min), with
considerable variation in the time until and duration of rule
violations in the different gorilla groups observed (Figure 3A).
The three groups trekked most frequently in this study were
Habinyanja group (n=15 treks), Mubare group (n=14 treks),
and Rushegura group (n=12 treks). Of these, encounters
with the Mubare group (habituated in 1993) tended to have
the highest percentage of nearest-neighbor observations with
human-gorilla spacing that violated the 7 m rule, at over
85% of the total observations across treks. Next highest was
Rushegura group (habituated in 2002) with 76% of observations
comprising 7 m distance violations, followed by Habinyanja
group (habituated in 1999), with over 58% of the total
number of observations of the group comprising 7 m distance
violations (Table 1).
Once the 7 m distance between humans and gorillas was
breached, the duration of the violation varied from 2 to 70 min
(some also violating the gorilla viewing duration of 60 min).
The 70-min violation occurred during an encounter with the
Mubare group, during which all 2 min sampling observations
recorded human-gorilla spacing at a distance <7 m. On average,
the duration of time when tourists were positioned <7 m to the
gorillas during the “gorilla hour” viewing experiences sampled in
this study was 43.5 min (Figure 3B).
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
TABLE 1 | Data collected during gorilla tourism encounters in BINP.
Date Group 7 m rule
brief
Disease-risk
brief
Trek duration Visit duration #Tourists Total # people Under 7 m? Under 3 m?
May 25, 2015 Oruzogo No No 173 60 7 13 Yes No
May 26, 2015 Oruzogo Yes Yes 150 66 7 13 Yes No
May 27, 2015 Kyagurino Yes No 185 66 5 11 Yes Yes
May 28, 2015 Oruzogo Yes Yes 148 65 7 13 Yes No
May 30, 2015 Bitukura Yes No 220 67 8 13 Yes Yes
May 31, 2015 Kyagurino Yes No 258 58 4 11 Yes Yes
June 2, 2015 Habinyanja Yes No 307 81 8 13 Yes Yes
June 3, 2015 Mubare Yes Yes 154 83 6 12 Yes Yes
June 4, 2015 Habinyanja Yes No 259 76 8 18 Yes Yes
June 5, 2015 Rushegura Yes No 246 84 6 21 Yes Yes
June 7, 2015 Habinyanja Yes Yes 167 68 8 NA Yes Yes
June 8, 2015 Mubare Yes Yes 182 69 8 19 Yes Yes
June 12, 2015 Bweza Yes Yes 209 58 7 16 Yes Yes
June 13, 2015 Mishaya Yes Yes 375 70 8 17 Yes Yes
June 14, 2015 Nkuringo Yes Yes 235 65 4 9 Yes No
June 16, 2015 Rushegura Yes Yes 215 64 1 6 Yes Yes
June 17, 2015 Habinyanja Yes Yes 244 78 7 19 Yes Yes
June 18, 2015 Mubare No No 206 80 4 13 Yes Yes
June 19, 2015 Mubare Yes Yes 267 67 7 13 Yes Yes
June 20, 2015 Mubare Yes Yes 181 46 8 18 Yes Yes
June 21, 2015 Habinyanja Yes Yes 197 61 8 18 Yes Yes
June 22, 2015 Mubare Yes Yes 210 60 8 19 Yes Yes
June 24, 2015 Habinyanja Yes Yes 202 98 8 18 Yes Yes
June 25, 2015 Habinyanja Yes Yes 249 65 6 11 No No
June 26, 2015 Mubare Yes Yes 178 62 11 23 Yes Yes
June 27, 2015 Rushegura Yes Yes 285 69 8 18 Yes Yes
June 28, 2015 Mubare Yes Yes 212 71 8 20 Yes Yes
June 29, 2015 Rushegura Yes No 293 56 5 15 Yes Yes
July 1, 2015 Nshongi Yes Yes 325 73 2 7 Yes No
July 2, 2015 Kahungye Yes Yes 338 68 8 13 Yes No
July 3, 2015 Busingye Yes Yes 325 71 3 7 Yes No
July 4, 2015 Habinyanja Yes Yes 89 54 7 NA Yes Yes
July 5, 2015 Habinyanja Yes Yes 220 58 8 NA Yes Yes
July 6, 2015 Mubare Yes Yes 213 79 8 20 Yes Yes
July 8, 2015 Rushegura Yes Yes 349 65 7 17 Yes Yes
July 9, 2015 Mubare Yes Yes 158 67 10 17 Yes Yes
July 22, 2015 Rushegura Yes Yes 101 54 8 21 Yes Yes
July 23, 2015 Rushegura Yes Yes 231 64 8 22 Yes Yes
July 24, 2015 Habinyanja Yes Yes 338 66 8 18 Yes Yes
July 25, 2015 Habinyanja Yes Yes 97 71 8 17 Yes Yes
July 26, 2015 Mubare Yes Yes 267 69 8 17 Yes Yes
July 27, 2015 Habinyanja Yes Yes 168 66 8 18 Yes No
July 28, 2015 Rushegura Yes Yes 411 66 8 21 Yes Yes
July 29, 2015 Mubare Yes Yes 219 60 6 NA Yes Yes
July 30, 2015 Rushegura Yes Yes 282 61 8 18 Yes Yes
August 1, 2015 Mubare Yes Yes 286 87 10 21 Yes Yes
August 2, 2015 Habinyanja Yes Yes 130 76 8 21 Yes Yes
August 3, 2015 Rushegura Yes No 231 54 8 19 Yes Yes
August 4, 2015 Rushegura Yes Yes 257 66 8 18 Yes Yes
August 5, 2015 Mubare Yes Yes 204 71 8 20 Yes Yes
August 6, 2015 Habinyanja Yes Yes 279 64 8 19 Yes Yes
August 7, 2015 Rushegura Yes Yes 105 54 8 19 Yes Yes
August 8, 2015 Habinyanja Yes Yes 295 61 8 18 Yes Yes
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
FIGURE 2 | Rule adherence information and behavior during gorilla viewing. (A) Percentage of treks in which tourists were informed by guides of the 7 m rule and the
importance of maintaining that distance to protect gorillas from disease transmission. (B) Percentage of treks with rule adherence vs. violations (n=53 treks).
(C) Observations of nearest human-gorilla spacing collected at 2 min intervals, shown by distance category.
Tourist Perceptions and Attitudes About
Gorilla Tourism Encounters
Of the 379 tourists accompanied during the study, approximately
64% elected to complete post-trek surveys, yielding a total of
243 surveys included in the study. Not all survey respondents
answered every question; results are depicted in Table 2 and
Figure 4. Of the 239 respondents to the first question, 211
responded that they were aware of the 7 m distance rule, and
28 reported that they were not. Of the 235 respondents to the
second question, 52 responded that they believed they kept a 7 m
distance from gorillas, whereas 183 responded that they had not.
Of the 243 respondents to the third question, 192 reported that
they believed that it is necessary to maintain a 7 m distance from
the gorillas, 41 reported that they did not believe it was necessary,
and 10 responded that they were unsure. Of the 235 respondents
to the fourth question, 50 thought that the 7 m rule detracts
from the visitor experience, 185 did not feel that maintaining a
7 m distance from gorillas would detract from the experience,
and 5 respondents were unsure. Because the fifth question was
added in partway through the study, only 142 people received
it in their survey and all responded; 106 reported that they
would be willing to wear a face-mask to protect the health of the
gorillas whereas only 36 reported that they would be unwilling to
do so.
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
FIGURE 3 | Timing and duration of 7 m rule violations for human-gorilla spacing during this study, by gorilla group and year of habitation. (A) Average time in minutes
until first 7 m rule violation during an hour-long viewing experience, as a function of gorilla group. (B) Average duration in minutes of 7 m rule violations during an
hour-long viewing experience, as a function of gorilla group.
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
TABLE 2 | Survey questionnaire questions and responses.
Question NYes No Maybe Missing % Yes % No % Maybe % Missing
(1) Did you know about the rule limiting
human–gorilla proximity to 7 m?
239 211 28 0 4 88.28 11.72 0 1.67
(2) Do you think a 7 m distance was maintained
between yourself a n d the gorillas?
235 52 183 0 8 22.13 77.87 0 3.40
(3) Do you think it is necessary for people to ma
intain a dista nce of 7 m from the gorillas? 233
233 192 41 10 10 82.40 17.60 4.29 4.29
(4) Do you think the 7 m distance rule detract s from
the gorilla-viewing experience?
235 50 185 5 8 21.28 78.72 2.13 3.40
(5) Would you be willing to wear a face-mask during
the gorilla-viewing experience?
142 106 36 0 0 74.65 25.35 0 0
FIGURE 4 | Tourist responses to survey items on study questionnaire. (Q1)
Did you know about the rule limiting human-gorilla proximity to 7 m? (Q2) Do
you think a 7 m distance was maintained between yourself and the gorillas?
(Q3) Do you think it is necessary for people to maintain a distance of 7 m from
the gorillas? (Q4) Do you think the 7 m distance rule detracts from the
gorilla-viewing experience? (Q5) Would you be willing to wear a face-mask
during the gorilla-viewing experience? (in these charts, green indicates “yes,”
orange indicates “no,” gray indicates “maybe/uncertain,” and black indicates
no answer).
DISCUSSION
Improving Tourist Knowledge, Perceptions,
and Attitudes About Behavior During
Gorilla Encounters
Our study hypothesized that the 7 m distance rule would not be
uniformly and consistently followed during tourism encounters
at BINP. Based on data from 53 gorilla viewing tourism treks
incorporating all habituated gorilla groups at the time of the
study, our hypothesis was supported. The 7 m distance rule was
only upheld in 2% (1/53) of treks in this study, whereas in 98% of
treks tourists came into closer contact than 7 m, breaking the rule,
in 67 observations (∼4% of 1,604 observations) within a meter
of gorillas.
For gorilla encounters, the pre-trek briefing at park
headquarters is important, because it is the only formal
opportunity for an explicit discussion regarding rules and
regulations of BINP available to shape tourist knowledge and
attitudes about the experience. Although 51 out of 53 pre-trek
briefings (96.2%) included information regarding the importance
of maintaining a distance of 7 m from the gorillas, over 11% of
tourists reported after the trek that they had been unaware of
the 7 m rule (Table 2). Several potential reasons could explain
why an individual tourist could embark upon a trek without
knowing about the 7 m distance rule and its critical role in
protecting the health of gorillas. It is possible that some tourists
may have missed all or part of the pre-trek briefing. Even if
they were present at a pre-trek briefing where this information
was provided, tourists may not retain information from the
briefing due to distraction; the morning briefing takes place at
park headquarters, where it is often noisy and crowded, and
filled with many people and vehicles. Moreover, the briefing
takes place outside in a somewhat dispersed setting. There is
the potential for a language barrier to impact understanding
of rules related to human-gorilla spacing, and this could be
explored in future studies. Although the all-Ugandan BINP
staff are fluent in English, most tourists were international and
some speak English as a second language or not at all. There
is also the simple possibility that tourists are not attentive
during the briefing, or that they are not accurately self-reporting
their knowledge.
When tourists were asked whether they perceived that it
is necessary to maintain a 7 m distance from gorillas, 16.9%
of respondents answered “no” and an additional 4.12% of
respondents indicated that they were unsure. This finding may
reflect that not all morning briefings in this study mentioned
the risk of disease transmission between humans and gorillas
that can occur in close proximity between the two species.
Disease transmission was mentioned in 43 out of 53 (81%)
tourist briefings. At times, tourists were instructed to maintain a
7 m distance from the gorillas in order to reduce gorilla “stress
and disturbance.” A potential problem with this approach is
that tourists cannot be expected to adequately assess stress in
habituated gorillas, making it a less effective a deterrent than
simply emphasizing risks of disease transmission.
Nonetheless, differences are apparent between information
presented in morning briefings and self-reported tourist
knowledge, attitudes, and perceptions. These differences could
be addressed through more deliberate and consistent messaging
from BINP staff at morning briefings, by updating the gorilla
tracking video shown to tourists before the morning briefing, and
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
by providing written handouts that explain risks and visitor rules.
Developing a set script for staff members could formalize the
morning briefing and help ensure that the “7 m distance” rule and
that risks of disease transmission between humans and gorillas
are clear to all tourists. Indeed this has been suggested in previous
studies [e.g., (5,51)], so it would be interesting to explore why
a set script has not yet been formally adopted. In addition, we
advocate for a second briefing to be instituted immediately before
the tourists begin gorilla viewing (i.e., when they have located
gorillas but before approaching them) in order to emphasize
that the 7 m distance must be maintained between humans and
gorillas at all times, and that this rule is in place to help mitigate
potential disease risk to the endangered gorillas. Increasing the
efficacy of communication between tourists and park staff of
BINP represents an essential yet simple tool for increasing rule
adherence and safe ecotourism practices.
Importantly, even though 88.3% of tourist respondents
indicated that they were aware of the 7 m distance rule, and
79.01% indicated they thought it was important to gorilla
health to maintain that 7 m distance, only 22.1% reported
having maintained a 7 m distance during their own gorilla
viewing experience, indicating a significant disconnect to be
addressed regarding rule adherence and rule enforcement during
gorilla encounters during this study. Rule disregard and lack
of enforcement have been well-documented in gorilla tourism
studies for decades [e.g., (42)]. We recommend that tourist
briefings be clarified and repeated to emphasize the health risks
posed to gorillas by proximity to humans at a distance <7 m, and
that park staff be encouraged and empowered to consistently and
effectively enforce the 7 m rule.
In Reality: Tourists Are Too Close to
Gorillas
Tourist perceptions aside, this study shows that although 96%
of tourists were informed of the 7 m rule preceding their trek,
tourists broke this rule in 98% (52/53) of the treks assessed.
This pattern was consistent across headquarter locations in the
park, throughout the tourist season, and across all gorilla groups.
Rule violations occurred in small and large groups of tourists
(some group sizes also exceeding the rule of 8 tourists per
trek), and in treks of the shortest and longest durations (with
a majority of treks lasting longer than the 60 min stipulated
for gorilla viewing experiences). Notably, 7 m rule violations
often began early during gorilla viewing and persisted without
correction; 7 m violations occasionally persisted for the entire
viewing period. These violations suggest BINP staff and guides
were reluctant to intervene to correct the problems and imply
that some gorillas may be accustomed to close human proximity
such that they do not move away from tourists even when in
proximity close enough for disease transmission (indeed, gorillas
approached humans in over half of the <3 m encounters). It
would be interesting for future studies to explore differences
in rule violations based on the time since habituation and
composition (including number of juveniles) of gorilla groups.
Environmental factors during treks probably also influence
human-gorilla proximity (e.g., steep terrain, narrow pathways,
and key vantage points), as they can at times make it difficult or
impossible for humans to move away from gorillas.
In 81% of morning briefings, tourists were informed of the
health risks of violating the 7 m distance rule, and in most
instances, tourists were briefed that if the distance was closed
by gorillas, it was the tourists’ responsibility to move away to
maintain the minimum 7 m distance. If humans are approached
by gorillas and appear reluctant to increase the distance between
themselves and the animals, then park staff must have strategies
to successfully intervene. Yet park staff are placed in a potentially
difficult position when it comes to enforcing the rules of BINP.
Gorilla trekking is an expensive, rare opportunity, and tourists
who engage in these treks often travel a great distance to do so,
thus they may have expectations and feelings of entitlement that
are unrealistic for a wild animal viewing experience (51). Hence,
Bwindi guides are placed under intense pressure to provide
tourists with an exceptional time-limited viewing experience
of an endangered primate species. Of course, the livelihoods
of Bwindi guides can also be enhanced by tips from tourists,
adding to the pressure of ensuring tourist satisfaction with the
experience, and perhaps generating reluctance about negatively
impacting tourist satisfaction. It would be interesting to explore
variation in guide responses to 7 m rule violations. Some guides
may strive to reinforce the 7 m distance rule, whereas other
guides may be hesitant to interfere with or upset the tourists. The
complexities of economic disparities and inequities in the wildlife
tourism industry have been deeply explored elsewhere [e.g., (52–
61)], but the bottom line is that as gorilla tourism continues
to expand, enforcement of the 7 m rule remains problematic
in long-habituated as well as newly habituated gorilla groups
at BINP.
Mask the Problem?
The tourism industry at BINP continues to present a
conservation paradox, with steady revenue generated through
tourists visiting gorillas a powerful incentive to continue
protecting the habitat and incredible biodiversity found within
the park. But the risk of disease transmission between humans
and gorillas poses a real threat to continued mountain gorilla
survival, and this study demonstrates that tourists are still
generally not adhering to the “7 m distance” rule in place to
protect mountain gorilla health. Gorilla conservation is reliant
upon tourism (11), yet the current gorilla tourism model is still
not ensuring safe human-gorilla interactions.
One potential solution to mitigate the present risks is to
introduce a rule requiring tourists to wear protective face-masks
during the gorilla encounter experience to reduce the amount of
disease-carrying aerosol particles released into the atmosphere
(62). In the final survey question “Would you be willing to wear a
face-mask during the gorilla-viewing experience?” the majority of
respondents (73.6%), indicated they would be comfortable with
the introduction of this practice. This figure is important, and
higher than the 51% positive responses from tourists reported
in a 2011 survey (5). Wearing protective masks is considered
best practice among conservation scientists (19,21,51) and is
currently in place in The Democratic Republic of the Congo,
where tourists regularly wear protective face-masks during gorilla
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
tourism encounters. Based on best practice recommendations for
mitigating transmission of respiratory diseases between humans
and great apes (21,51), we recommend here that tourists
be required to use face-masks (e.g., N95 surgical respirator
masks) during gorilla encounters at BINP to reduce the risk of
disease transmission.
Long-Term Strategy: Empowering Guides
and Managing Tourist Expectations
To increase tourist knowledge and promote responsible tourism
practices, sustainable long-term strategies must urgently aim to
improve human–gorilla spacing, empowering guides through
staff training exercises that target and practice strategies for
intervention that maintain a positive tourist experience without
compromising gorilla health. At the time of this study, all
habituated gorilla groups in BINP were exposed to tourists
at a distance <7 m. Shaping tourist expectations and guide
responses to rule violations may benefit from focused mediation
training for staff, including managing tourists from different
cultures. This can help guides to address challenges and better
direct human behavior during gorilla trekking experiences.
Providing additional resources and training to BINP staff can
help improve confidence, empowering staff to better enforce the
“7 m distance,” rule.
Importantly, Macfie and Williamson (51) point out the need
for managing tourist expectations at the outset of a viewing
experience. One approach may be to adjust tourist expectations
about the gorilla tourism experience altogether. For example,
successful conservation of wildlife habitat has been facilitated
by wilderness-style experiences along the Kinabatangan River
in Malaysian Borneo that feature simply the “possibility”
of viewing orangutans (51) (NJS pers. obs.). This raises
the potential for a deliberate gradual shift of the tourism
experience made available by the Uganda Wildlife Authority
to highlight more sustainable and meaningful opportunities
for tourists to “search for” gorillas (for example at a distance
far >7 m), rather than marketing more or less guaranteed
photo opportunities at close range. Notably, orangutan tour
operators rarely guarantee orangutan sightings, but tourists still
visit. Communicating similar expectations to tourists interested
in viewing gorillas could help shift distances back over time,
and in conjunction with such a shift, communications could
emphasize other fauna and flora that may be seen during
treks. Long-term shifts to a less intensive gorilla viewing
experience could not only serve as a sustainable solution
to mitigate diseases spread by close encounters, it may
also reduce gorilla over-habituation, and hence human-gorilla
conflict, as less habituated animals may be less inclined to
venture into areas of human occupation for crop raiding
(51). Long-term strategies can prioritize a more sustainable
experience, where the goal would be “to catch an exciting
glimpse” of the gorillas rather than to spend an hour in
extremely close proximity to them, taking similar pictures over
and over.
Gorilla tourism at BINP has proven successful in protecting
forested habitat and conserving endangered mountain gorilla
populations over the past two decades, at the same time
providing livelihoods and development opportunities for local
communities. As human populations continue to grow and
gorillas become increasingly habituated, however, communities
must adopt new and more effective strategies if they wish
to conserve endangered great ape populations and sustain
gorilla-viewing tourism into the future. Rule violation patterns
documented herein demonstrate that there is room and urgent
need for improvement in mitigating disease risks caused by
tourists visiting the mountain gorilla of BINP. The present
gorilla tourism model as implemented introduces substantial
health risks for the very animals it tries to protect, and
increasing tourist demand is likely to further increase risks
unless substantial actions are taken to mitigate risks of
disease transmission.
DATA AVAILABILITY STATEMENT
All datasets generated for this study are included in the article or
available by request to the correspondent author.
ETHICS STATEMENT
This study was conducted with permission from the Uganda
Wildlife Authority and the Uganda National Council for
Science and Technology in accordance with IRB and IACUC
recommendations of the Ohio University Office of Research
Compliance. All human subjects gave written informed
consent in accordance with the Declaration of Helsinki.
Protocol IRB#19.052 was approved by the Institutional Review
Board Committee in the Ohio University Office of Research
Compliance. Protocol IACUC# 19.049 was approved by the
Institutional Animal Care and Use Committee in the Ohio
University Office of Research Compliance.
AUTHOR CONTRIBUTIONS
NS, AW, and GK-Z contributed to conception and design of the
study. AW carried out the field work. NS and AW analyzed the
data. AW and NS assembled the first draft of the manuscript
and figures.
FUNDING
Graduate student funding for this work was provided to AW
through the Ohio University Voinovich School of Leadership
and Public Affairs. Support for NS was provided by the Ohio
University Heritage College of Osteopathic Medicine.
ACKNOWLEDGMENTS
We thank editor Jessica Rothman and two reviewers who
provided detailed suggestions that substantially improved the
manuscript. We thank G. Dabelko, D. Miles, P. O’Connor,
and E. Wangui for helpful insights that contributed to the
project, E. Wyza with assistance in figure generation, V. Popescu
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Weber et al. Tourists Violate Rules During Gorilla-Viewing
for statistical support. AW acknowledges logistical support
provided by Gorilla Conservation Camp and Conservation
Through Public Health staff during the field study. NS
acknowledges field support provided by the Voinovich School
and laboratory support the Heritage College of Osteopathic
Medicine at Ohio University. This study was conducted in
accordance with recommendations from the Ohio University
Institutional Review Board and IACUC, the Uganda Wildlife
Authority and the Uganda National Council for Science
and Technology.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fpubh.
2020.00001/full#supplementary-material
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Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
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