Pan Africa News, 27(2):16–20 (2020)

Note

COVID-19 and chimpanzees from a field perspective:
Mitigation measures, ecological and economical situation after
four months in Sebitoli, Kibale National Park, Uganda
Sabrina Krief 1, 2 , Chloé Couturier 1, 2, 3, Julie Bonnald 1, 2, 4, John Paul Okimat 2,Edward Asalu 5 & Jean-Michel Krief 2✉

1 UMR 7206 CNRS/MNHN/P7, Eco-anthropologie, Hommes et Environnements, Muséum national d’Histoire naturelle, Muséede l’Homme, 17 place du Trocadéro, 75016 Paris, France
2 Great Ape Conservation Project (GACP), Sebitoli Research Station, Kibale National Park, Fort Portal, Uganda
3 Fondation Nicolas Hulot pour la Nature et l’Homme, 6 rue de l’Est, 92100 Boulogne-Billancourt, France
4 Kinomé, Campus du Jardin d’Agronomie Tropicale de la ville de Paris, 45 bis avenue de la Belle Gabrielle, 94736 Nogent surMarne cedex, France
5 Uganda Wildlife Authority, Uganda(✉E-mail: sabrina.krief@mnhn.fr)

INTRODUCTION

The SARS-CoV-2 outbreak has led to the confinementof about two-thirds of the world’s population (Bates et al.
2020). The emergence of the virus seems to be related tothe increase in the interaction between wild animals andhumans. Two main drivers have been proposed to explainit (1) the encroachment of human activities into wild areas and forests, and (2) the (legal and illegal) expanding
international market of bushmeat and live wild animals
from tropical and sub-tropical areas for food and traditional medicine, sold in unsanitary conditions (Volpato etal. 2020). While the biology underlying susceptibility toSARS-CoV-2 infection remains to be fully elucidated, it is
now well-established that the virus infects the endothelial
cells in targeting the angiotensin-converting enzyme-2(ACE2) receptor. Apes exhibit the same set of amino-acidresidues in ACE2 as humans, making them highly susceptible to SARS-CoV-2 (Melin et al. 2020).
With the restriction of national and internationaltraffic to limit the virus transmission, many benefits
were expected for wildlife from this “anthropause,” as aconsequence of reduced habitat disturbance (Rutz et al.
2020). However, the reverse also has been noticed in someplaces, with an increase in poaching and illegal activities(Rutz et al. 2020). Besides the dramatic consequences onhuman health of Coronavirus disease 2019 (COVID-19),
this unique case of global reduction of human mobility
and activities may be viewed as an opportunity to better estimate both positive and negative effects of humanimpact in different ecosystems and on different species(Bates et al. 2020).
Before the COVID-19 pandemic, Sebitoli chimpanzees living in the north of Kibale National Park (Uganda)
experienced a high level of pressure from human activities, such as intensive agriculture, road traffic and related
pollution (Cibot et al. 2015; Bortolamiol et al. 2016; Kriefet al. 2014; 2017; 2020; Spirhanzlova et al. 2019). They
also were indirect victims of wire snares set by poachers
to catch duikers for bushmeat (Cibot et al. 2016). During
the COVID-19 pandemic, the Sebitoli Chimpanzee
Project (SCP) monitored the direct and indirect consequences of COVID-19 in terms of health, environment
and the economy in order to mitigate them. Based on ourpreliminary results, we propose perspectives for researchers and conservationists on possible tools and measures

to protect great apes and their habitats in the contexts ofsuch pandemics.

STUDY SITE

The home range of the Sebitoli chimpanzee community covers 25 km2 in the far north of the Kibale National
Park, Uganda (795 km 2; 0°13′ to 0°41′N and 0°19′ to30°32′E). Since 2008, SCP has monitored daily this community of about 80 chimpanzees. In 2020, before thepandemic, SCP consisted of 25 Ugandan field assistants
working to: collect scientific data, conduct anti-poaching
operations, implement education and community-based
programmes, and maintain the trail systems, managed
by one of us, JPO, coordinator. During the lockdown decided by the Ugandan government and Uganda Wildlife
Authority, eight of the assistants were confined in theNational Park, i.e. they did not have contact with thepopulation outside of the research station. Food wasordered and delivered at the gate of the station and communication between France (direction of the project) andUgandan team was maintained daily with social networks
and weekly with visioconferences.

METHODS

We adapted the usual protocols to record chimpanzee
behaviour and health and to reduce threats of poaching inaccordance with Uganda Wildlife Authority guidelines.
We set up 14 camera traps at the most commonly-visited
locations (feeding trees and crop-fields) and memory
cards were collected twice weekly for immediate reading. We designed new datasheets: identity of chimpanzees
and when possible, general condition, injuries, respiratory function (sneezing, coughing), locomotion, appetite,
faecal consistency, reproductive status of females werescored. We collected data on illegal activities during antipoaching patrols five days per week. Two teams werededicated to this task during the COVID-19 period, wereas usually only one was active. We counted twice weekly,
the number of vehicles travelling in both directions along
the road inside the protected area. On 19 May and 27
July, 2020, we collected all plastic bottles and other litter
discarded by people from the vehicles along the 4.6 km ofroadsides (4 m each side of the tarmac within the nationalpark).

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Pan Africa News, 27(2):16–20 (2020)
Table 1. Confinement measures and Standard Operating Procedure (SOP) taken in Uganda
Date

Event and measure

18 March 2020

Public gatherings (religious, cultural meeting, school) suspended.

21 March 2020

The first case of COVID-19 recorded at the Entebbe International Airport.

22 March 2020

Travel from abroad suspended except for drivers of cargo trucks (PCR tests done before entering Uganda).
Moto-taxis allowed to carry only food and material. Private cars allowed but to carry no more than three people including, thedriver.

25 March 2020

Communication from Uganda Wildlife Authority management to stop primate research, filming and tourism.

27 March 2020

Public and private transport suspended.

30 March 2020

Total lock-down declared. Curfew 19:00–06:30 hr.

31 March 2020

Private car traffic suspended.

26 May 2020

Private cars allowed to operate from 06:30–19:00 hr in 95 of 135 districts.

4 June 2020

Public transport (bus and minibus) allowed to operate, provided they followed SOPs and only in some districts. No public transport
in border districts.

21 July 2020

30 July 2020

Moto-taxis allowed to carry passengers provided they followed SOPs.
During entire period, cargo trucks continued to operate.
SOP for research activities in UWA estates—Reopening of the Park Area (PA) during COVID-19 pandemic.
i) All researchers coming into the PAs or close proximity of wild animals must wear clean clothing and disinfected footwear prior togoing to the field for data collection.
ii) Every researcher must carry into the field a hand sanitiser.
iii) Time spent conducting research activities near primates shall be limited to a maximum of five hours per designated researchday.
iv) The research team shall comprise a maximum number of three people to ensure safety and health monitoring.
v) A distance of not less than 10 metres from the primates shall be maintained at all times.
vi) A surgical facemask must be worn by anyone coming within 10 metres of primates.

RESULTS

Protecting Sebitoli chimpanzees
and local communities : sensitization by SCP
From 21 April through July
2020, a series of measures wereadopted by the government andUganda Wildlife Authority, modulating the level of human activities
in and around Kibale National
Park (Table 1). Although SCP,
even before the pandemic, had
implemented preventive measuresagainst transmission of human respiratory diseases to chimpanzees(e.g. keeping distance between
observers and apes, wearing surgical masks, using sanitizer, not spitting in the forest...), to reduce anemergent risk of the new coronavirus transmission, SCP initiatedcommunication related to safety
recommendations. The SCP teamdesigned posters using pictograms
to highlight the risks and the measures to reduce them (Figure 1). The
targeted public was: (1) SCP fieldassistants at the research stationand in the forest when authorized
to carry out health monitoring, Figure 1. Posters designed to sensitize SCP staff and local farmers to COVID-19
anti-poaching patrols, and transect
maintenance in the National Park; (2) villagers, especially Indirect monitoring of the chimpanzees using camera
those who neither know how to read nor speak English, traps
Over the first eight weeks, 51 chimpanzees were seen
thus the simplicity and pictorial nature of the messages.

17Pan Africa News, 27(2):16–20 (2020)

Figure 2. Cost of some basic food items eaten locally around the study area before the COVID-19 period and during theCOVID-19 period. Prices are given in Uganda shillings for 1 kg of food except for posho (maize flour, 10 kg).

Figure 3. Traffic (mean number of pedestrians and vehicles/hour) on the tarmac road from Fort Portal to Kampala
before and during the COVID-19 period.

a total of 612 times. None was diagnosed as showing severe symptoms (sneezing, coughing, apathy), which can
indicate COVID-19. Injuries were observed (see below,poaching section).
Econom ic sit uat ion dur i ng the four months ofCOVID-19 confinement
We made very basic estimates of the economic consequences for local communities, using as a proxy of thecost of living, the price of common foods. Over eightweeks after the traffic was suspended (15 May, 2020), allfood-item prices had increased (Figure 2).
Ecological situat ion during the four months of
COVID-19 confinement
Public transport (by bus, minibus) was almost absent
between 25 March and 4 June, i.e. over more than twomonths (Figure 3).
Despite this substantial reduction of traffic,- A subadult female chimpanzee, CP (Chapati) estimated age of 14 year, was knocked dead by a vehicle on
the tarmac road on 8 May, 2020 (Figure 4). Since 2012,
three Sebitoli chimpanzees were killed on this portion ofroad (Krief et al. 2020).

Figure 4. Chapati, subadult female fatality from a car
accident on 8 May 2020 on the tarmac road crossing theSebitoli chimpanzee home range in Kibale National Park.

- On 27 July, 2020 : 2626 bottles (52 kg) and 26 kg ofother plastic waste were collected with the assistance of
the Uganda Wildlife Authority. Seventy-eight kg of such
litter had accumulated in only 10 weeks (19 May to 27July, 2020) since the last collection during the confinement. Twice as many bottles were collected during theCOVID-19 period (1170/month) compared to a mean number of 601 bottles/month in the four months, at the end of2019 (Table 2; Figure 5).

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Pan Africa News, 27(2):16–20 (2020)
Table 2. Plastic collection along the Fort Portal-Kampalaroad, in the section crossing Kibale National Park and thehome-range of Sebitoli chimpanzees.
Date of plastic
collection

Number of bottles
per monthsince last collection

Number ofplastic bottles

Weight ofplastic (kg)July 2019

3090

92

December 2019

2406

96

601/month

May 2020

1884

70.5

July 2020

2926

78

Total for year

10306

336.5

Table 3. Illegal activities recorded during patrols ofSebitoli Chimpanzee Project in chimpanzee homerange from 25 March – 31 July in 2019 and in 2020 (sinceconfinement was declared in Uganda).
Type of illegal activities

Number of evidences recorded during
patrols from 20 March – 31 July
20192020 (COVID-19)

Debarked trees

122376/month

Firewood collection sites

20281170/month

Piper guineense harvesting

2

13Tree cutting

27

41

Snares

58

64

Total

116

210

Figure 5. Litter collection by Sebitoli Chimpanzee Projectassistants 19 May 2020 on the tarmac road crossing theSebitoli chimpanzee home range in Kibale National Park.

The total number of snares recovered was similar
during a four-month period (25 March to 31 July) in 2019and 2020. Patrols found a mean number of 0.70 snare/
day during the COVID-19 period (64 in 91 working days)
against 0.85/day in 2019 during the same period (58 in 68
working days). However, other illegal activities related toflora increased by a factor of 2.5 in 2020, especially thosethat generate income, such as Piper guineense (13 casesvs 2) and tree cutting for getting bark from medicinaltrees (such as Prunus africana) (22 vs 1) (Table 3). Also,
several observations indicated an increase of illegal activities, including poaching:
One of the camera traps was stolen on 7 May, 2020,
and the presence of dogs attacking chimpanzees in theforest was also observed in camera-traps and reported to
the Uganda Wildlife Authority (two dogs observed in fouroccasions).
We also observed three cases of severe injuries tochimpanzees caused by poaching over the COVID-19 period, while no case had been observed in 2019:
Subadult male GR (17 April, 2020) had a large wound(at least 4 cm) on his left thigh, attributed to a spear;
Infant female, dependant of FR (27 May, 2020) had asevere injury on her right foot from a snare;
Subadult male LK (14 July, 2020) had a severe injury
on his left hand from a snare (Figure 6).

DISCUSSION

In the Sebitoli area, a strict sanitary protocol was applied for the field team confined in the protected area. The

Figure 6. Subadult male LK severely injured his left handby a snare. Image captured by camera-trap on 14 July2020.

direct effects of COVID-19 on the chimpanzees’ health,as monitored by camera traps, did not reveal respiratory
symptoms. Camera traps enabled us to discover severe
injuries caused by poaching (wires and spear) on Sebitoli
chimpanzees. While the number of snares recovered by
the anti-poaching patrols did not increase compared to thesame period in 2019, damages to the habitat have more thandoubled likely due of loss of revenues in local communities. Despite the fact that public transport was banned,
no detectable positive consequences were noted along
the road inside the park, with a female chimpanzee being
knocked dead and the number of plastic bottles along theroad having more than doubled compared to the period
before the lockdown. Unfortunately, the relaxation of thepressure expected on wildlife did not occur and the indirect effects of COVID-19 on wild chimpanzees and theirhabitat in Sebitoli area seems more negative than positive,in general. This case study in a small part of a protectedarea emphasized: (1) the relevance of camera-traps’ use toreduce proximity with apes in such circumstances, and (2)the importance of strengthening efforts to contain illegalactivities. We suggest that sharing local experiences withother study-sites, harmonizing protocols, and increasing
indirect monitoring of apes’ habitat (e.g. drone, cameratrap) are necessary to be ready to react to future emerging
disease outbreaks.
The potential cascading impacts of COVID-19 from19

Pan Africa News, 27(2):16–20 (2020)
sis and beyond. Nat Ecol Evol 4:1300–1310.

international travel restriction, reduced tourism, local
food insecurity, poverty increase, and funding reduction
due to global economic shrinkage show the importanceof supporting local agencies and civil society. This pointis proposed to IUCN World Congress 2021 in the motion
115 – “Strengthening great ape conservation across countries, in and outside of protected areas, involving local
actors” and shall be also considered to diversify revenueoperating actions from wildlife areas (Lindsey et al.
2020).

https://doi.org/10.1038/s41559-020-1275-6

Melin AD, Janiak MC, Marrone II F, Arora PS, Higham J P
2020. Comparative ACE2 variation and primate COVID-19
risk. BioRxiv. (preprint)
https://doi.org/10.1101/2020.04.09.034967

Rutz C, Loretto MC, Bates AE et al. 2020. COVID-19 lockdown allows researchers to quantify the effects of humanactivity on wildlife. Nat Ecol Evol 4:1156–1159.
https://doi.org/10.1038/s41559-020-1237-z

Spi rhan zlova P, Fi n i J-B, Demenei x B et al. 2019.
Composition and endocrine effects of water collectedin the Kibale national park in Uganda. Environ Pollut
251:460–468.

ACKNOWLEDGMENTS

https://doi.org/10.1016/j.envpol.2019.05.006

We thank the Uganda Wildlife Authority and Uganda
National Council for Science and Technology for authorizing our research in the Kibale National Park. We
are very grateful to all field assistants of the Sebitoli
Chimpanzee Project who were confined at Sebitoli
Station during Covid-19 lockdown, namely, EmmanuelBalinda, Deogratius Kiomuhangi, Joseph Alinaitwe,
Ibrahim Nyakana, Wilson Muzahura, Edward Kalyegira,and Sulaiti Tusabe. We offer profound thanks to Daniela
Zainabu Birungi, Robert Asimwe, and Robert Nyakahuma
for their assistance for the plastic waste collection andto Clovice Alikonyera, Charles Twesige, and PhilipMusinguzi for the road patrols. We are grateful to theFondation Nicolas Hulot pour la Nature et pour l’Homme,
the Fondation Prince Albert II, and the Fonds Françaispour l’Environnement Mondial for financial support. We
deeply thank Kazuhiko Hosaka, Noriko Itoh and WilliamC. McGrew for their valuable comments to improve thismanuscript.

Volpato G, Fontefrancesco MF, Gruppuso P, Zocchi DM,Pieroni A 2020. Baby pangolins on my plate: Possible lessons to learn from the COVID-19 pandemic. J Ethnobiol
Ethnomed 16:19.
https://doi.org/10.1186/s13002-020-00366-4

Received: 13 August 2020
Accepted: 26 October 2020

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