Wild Chimpanzees on the Edge: Nocturnal Activities in

Croplands
Sabrina Krief
1,2
*, Marie Cibot
1,2,3
, Sarah Bortolamiol
1,2,4
, Andrew Seguya
5
, Jean-Michel Krief
2
,
Shelly Masi
1
1UMR 7206 CNRS/MNHN/P7, Eco-anthropologie et dethnobiologie, Hommes, Natures, Societe s, Museum national dhistoire naturelle, Paris, France, 2Projet pour la
conservation des grands singes, Kibale National Park, Fort Portal, Uganda, 3UMR 7179 CNRS/MNHN, Me canismes adaptatifs: des organismes aux communautes, Ecologie
et de gestion de la biodiversite , Muse um national dhistoire naturelle, Paris, France, 4UMR 7533, Dynamiques Sociales et Recomposition des Espaces, Paris Diderot
University, Paris, France, 5Uganda Wildlife Authority, Kampala, Uganda
Abstract
In a rapidly changing landscape highly impacted by anthropogenic activities, the great apes are facing new challenges to
coexist with humans. For chimpanzee communities inhabiting encroached territories, not bordered by rival conspecifics but
by human agricultural fields, such boundaries are risky areas. To investigate the hypothesis that they use specific strategies
for incursions out of the forest into maize fields to prevent the risk of detection by humans guarding their field, we carried
out video recordings of chimpanzees at the edge of the forest bordered by a maize plantation in Kibale National Park,
Uganda. Contrary to our expectations, large parties are engaged in crop-raids, including vulnerable individuals such as
females with clinging infants. More surprisingly chimpanzees were crop-raiding during the night. They also stayed longer in
the maize field and presented few signs of vigilance and anxiety during these nocturnal crop-raids. While nocturnal activities
of chimpanzees have been reported during full moon periods, this is the first record of frequent and repeated nocturnal
activities after twilight, in darkness. Habitat destruction may have promoted behavioural adjustments such as nocturnal
exploitation of open croplands.
Citation: Krief S, Cibot M, Bortolamiol S, Seguya A, Krief J-M, et al. (2014) Wild Chimpanzees on the Edge: Nocturnal Activities in Croplands. PLoS ONE 9(10):
e109925. doi:10.1371/journal.pone.0109925
Editor: Roscoe Stanyon, University of Florence, Italy
Received April 18, 2014; Accepted September 4, 2014; Published October 22, 2014
Copyright: 2014 Krief et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its
Supporting Information files.
Funding: SK received funds from National Museum of Natural History/ATM 16, ANR JC-JC SAFAPE to design and conduct the study. MC received funds from
LabEx BCDIV for her field study. Projet pour la Conservation des Grands Singes funds the Ugandan field team and support logistic management. The funders had
no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* Email: [email protected]
Introduction
Compared to previous centuries, the level of demographic
pressure and the rate of habitat loss for wildlife caused by humans
have dramatically increased [1]. Today anthropogenic activities,
including commercial logging, poaching, mining, illicit trade of
wild animals and agricultural land encroachment are severely
threatening the tropical forests and the survival of fauna, including
great apes, our closest relatives. All great ape species are currently
endangered and have experienced a considerable decline in
population size and range in the recent years [1,2,3,4]. Being
charismatic umbrella species, they are widely claimed to be
instrumental in the conservation of tropical forests and wildlife [5].
This emphasizes the importance of understanding and monitoring
how they react and potentially adapt to different habitat changes.
While humans have been present in primate habitats since the
millennia, the current rate of forest destruction and fragmentation,
is resulting today in prevalent humanwildlife conflicts along
protected area boundaries [6]. This situation is deteriorating
further given average human population growth rates, reaching
nearly double the average of rural growth at the border of some
protected areas [7]. The incursions in human cultivations by forest
mammals, such as elephants and primates, are therefore one of the
most common behavioural responses to both habitat loss and
access to new energy-rich food resources (Africa: [8,9]; Asia:
[10,11]).
Among Primates, chimpanzees are known to be sensitive to
logging due to their territoriality, and their frugivorous diet [12,13]
that leads to a lower flexibility to seasonal fluctuations in fruit
availability [14]. However, chimpanzees have high cognitive
abilities. They enable them to use botanical skills to discover and
exploit fruits in the forest habitat according to dynamical temporal
patterns [15], to access hidden food resources using tools
[16,17,18], to cooperate to achieve a common goal (e.g. hunting,
patrolling: [19,20]) or even to use the pharmacological properties
of plants to self-medicate [21,22,23,24]. Nevertheless, the acqui-
sition and transmission of such techniques and behaviours require
a long period of social learning [18,25,26]. This long time of social
learning might not fit in the rapid changes of environment and of
the local population perception towards chimpanzees which occur
in areas where habitat encroachment within chimpanzee habitat
increases encounters with humans and consequentially chimpan-
zee aggressive behaviour [27]. In Western Uganda, in Bulindi, an
unprotected human-dominated area, several people claimed that
chimpanzees had been deliberately killed to deter crop raiding
PLOS ONE | www.plosone.org 1 October 2014 | Volume 9 | Issue 10 | e109925
[28]. Whether chimpanzees are flexible enough to adapt their
behavioural ecology and ranging patterns to their rapidly changing
habitat and to the changes in the attitudes of local people
regarding crop loss is a major concern for their survival. In such a
fragmented farmforest mosaic (Bulindi), a marked mobility of
chimpanzees between the main forest blocks and thus crossing
anthropogenic habitat is necessary even to feed on wild food [28].
In areas where chimpanzee communities inhabit a continuous
forested territory that is bordered by crop fields actively guarded
by humans, such as in Kibale National Park, western Uganda, first
surveys suggest that the boundaries of their territory are perceived
to be risky areas [29,30]. Territoriality in chimpanzee involves the
active defence of their home-range, mates and food resources from
the neighbouring communities during cooperative patrols, that
can sometimes be lethal [16,31]. In Kibale National Park,
chimpanzees are usually considered by local people and prima-
tologists as infrequent crop-raiders [29,32]. This may be either
because they do really avoid such dangerous situations or because
their behaviour might be so efficient as to avoid detection by
humans, thus resulting in underestimation of the events [8,29,33].
At Bossou, chimpanzees seem to perceive the risk of human
confrontation in a similar way as risk of predation consequently
adapting their behavior and feeding strategies accordingly. For
example, adult males who usually take more risk than females
were more likely to crop-raid than females [34]. When feeding on
raided food rather than wild food, chimpanzees vocalized less and
showed higher frequency of signs of anxiety, including rough self-
scratching, in presence of local people [34]. They also tended to
transport crops into the forest to reduce stationing in exposed
areas [34]. In this small community (1214 chimpanzees), the
party size was not significantly different when feeding crops or wild
food but cohesiveness increased during crop-raiding [35].
In Kibale National Park, chimpanzees may also be efficient to
minimize the risk of detection by farmers explaining why there are
considered as infrequent. For instance, in some places, farmers
report that sometimes chimpanzees visit crop fields at full moon to
hide their raid ([36]; Sebitoli Chimpanzee Project, unpublished
data). Chimpanzees, as other ape species are considered as strictly
diurnal (illumination intensity range for feeding activity: 185 lux)
while the illuminance (the measure of the incident light
illuminating a surface), during full moon night amounts to about
0.3 lux [37,38]. Among primates, only a few lemur and monkey
species show cathemerality, thus being active during both the day
and night [39,40,41]. To date, descriptions of night activities in
wild great apes have been rare. They include night feeding
activities on the night of full moon at Gombe [16], mating
behaviour [42], and travelling on moonlit nights at Fongoli,
Senegal [43] and Mahale, Tanzania [44]. Such behaviour has also
been observed in different western gorilla groups in the attempt to
avoid or escape from attacks of another group or lone male (Masi,
pers. observ.).
To test the hypothesis that chimpanzees may have developed
several strategies to survive in highly disturbed habitats and to
avoid detection by humans, including being active during moonlit
nights, we focused our survey on a maize field bordering the
forested area of Sebitoli in the northern part of Kibale National
Park (KNP), Uganda. In a recent review of 33 bibliographic
sources, KNP is classified as highly exposed site to agriculture
among the 27 locations scored and maize as a cause of high
conflict out of the 51 crops eaten by chimpanzees [45]. Most of
the Sebitoli chimpanzee territory (32 out of 39 km of the home
range borders) is surrounded by anthropogenic landscape [46]. In
addition, their home range is crossed by a tarmac road and
experiences a great pressure from poaching: 40% of identified
chimpanzees have limb mutilations most likely due to snares [47].
We used video-trapping method to record their behaviour in a
maize field neighbouring the forested area of their territory. This
non-invasive method can be used day and night with infra-red
light and offers an alternative to traditional field methods based on
direct observation. This method offers systematic recording of
behaviours (1) in locations where chimpanzees may be reluctant to
be followed by researchers due to a fear of meeting farmers, and
(2) during periods where luminosity is too low to enable direct
observations of chimpanzees in the case of unusual activity during
full moon nights [36].
Since crop-raiding is a risky way to access valuable food
resources and behavioural adaptations have been shown elsewhere
[3435], we predict that during crop-raiding chimpanzees would
use characteristic behavioural strategies in order to avoid
detection, particularly:
Hypothesis 1- chimpanzees will show specific group behaviours in
response to a risky situation i.e. a) low rate of incursions, party
composition and progression order into the field biased on adult
males who are more often involved in risky activities, b) small party
size, lower number of individuals may decrease the detectability in
that large community counting about 80 members (the alternative
hypothesis being that larger and more cohesive party will increase
the vigilance [35])
Hypothesis 2- chimpanzees will show specific individual behav-
iours to limit the risk of being detected i.e. cautiousness, vigilance,
being silent and extension of activity during nocturnal periods.
Materials and Methods
1. Study site
Kibale National Park (795 km
2
) is a medium-altitude moist
tropical forest located in Western Uganda. The landscape is a
mosaic of evergreen forest, swamps, regenerating forests from
former exotic softwood plantations within the national park (NP).
The park is surrounded on the outside by smallholder farms, forest
fragments and tea estates [4849]. As a result of land scarcity and
the increasing population (up to 335 ind/km
2
; [50]), agricultur-
alists (Batooro and Bakiga ethnic groups) have been forced to set
up their lands at the edge of the national park.
2. Study subjects
Since 2009, the Sebitoli Chimpanzee Project monitors daily the
extreme north community of chimpanzees (Pan troglodytes
schweinfurthii) of the NP. We adhered to the research protocols
defined by the Administration of Kibale National Park and all
research was approved by the Museum national dhistoire
naturelle. Data of this study refers to the period from the 5
th
to
24
th
February 2013, where a camera trap was placed at the border
of their home range during the period of maize crop maturity. At
this date, 72 chimpanzees were individually recognised out of an
estimated number of 80 individuals. Twenty-six of them present
hands, feet or limb deformities or scars resulting from being
trapped in poaching snares. Eight are missing entire segment(s) of
limb(s). Since 2009 ad libitum daily observations records and GPS
waypoints of contacts with chimpanzees were used to determine
the home range of the Sebitoli community by the method of
Minimum Convex Polygon [51], estimated to be 25 km
2
.
3. Video-trap recording
During our routine chimpanzee monitoring in the North-
Western part of the territory of Sebitoli chimpanzees (Figure 1),
Nocturnal Activities of Wild Chimpanzees
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we regularly found maize remains (corn and stems) associated with
chimpanzee footprints and faeces along a 2 meters wide per 2
meters deep trench, that was dug by the Uganda Wildlife
Authority to prevent elephant from incurring and destroying the
crops. At the time of the study, the efforts by the local communities
to protect such crop fields were fairly significant: day and night
guarding of the field by sleeping in a hut situated in the maize field
(surface =17,838 m
2
calculated from GPS records; Garmin 450) at
35 meters from the trench where chimpanzee food remains were
found and maintenance of the trench. However, in a location
along the maize field, the two sides of the trench were bridged
horizontally by a single fallen trunk (Acanthus pubescens species,
diameter at breast height =0.11 m). The maize food remains were
often found piled up in front of the trunk showing that this point
was the main and preferred access. According to footprints and
feeding remains, the alternative of this direct access was a 100-
meter diversion to access the crop, even though it cannot be
excluded that some individuals may access the field in other ways
thus the observed party size may have been underestimated. We
placed on this bridge a HD video-trap (Bushnell Trophy Cam HD
Max) with a day/night autosensor (motion sensor reaching out to
60 feet or beyond and IR flash i.e. a LED night vision flash that
sends a burst of Infrared Energy which is invisible to the human
eye and an adjustable Passive Infra Red (PIR) motion detector,
with no-glow black LEDs) and sound recordings. The settings were
the following: high definition video of 12806720 pixels, video
length of 30 seconds, trigger interval of 1 second, and low PIR.
The video-trap started recording digital pictures when motion is
sensed at a distance up to 18 m. For the study period, night is
defined as the period between sunset and sunrise i.e. from 19:07 to
7:01 during the study period and at this location [52]. To better
categorise nocturnal activities, we also consider the period of
twilight defined as the illumination produced by sunlight scattering
in the upper atmosphere. Twilight occurs between dawn and
sunrise and between sunset and dusk. While several twilights are
defined according to the position of sun below the horizon, we use
in this study the nautical twilight, which is considered as complete
darkness (sun is less than 12u below the horizon). In the studied
area, twilight is short (crepuscular period is briefest at the Equator)
and always last less than one hour [53].
Infrared images are automatically recorded at night as well as
during daytime if the light is low due to rainy or cloudy weather.
The camera was fixed on a tree facing the small maize field on the
forest side at 3.5 m from the trench. On recorded clips, we can
clearly see the behaviour of the chimpanzees in the forest along the
trench and on the fallen tree. They were not visible while inside
the maize field, however as the maize is growing less than 2 m
along the trench, the chimpanzees that crossed the fallen tree were
entering the maize field. We identified the individuals visible in
each 30 second-clip. However, we were not able to identify all
individuals because recognition of chimpanzees that were not
facing the video trap was difficult especially in the infra-red
images. Finally we defined as full moon days, the days when the
moon is completely illuminated, visible from sunset to sunrise and
illuminance is about 0.3 to 1 lux. As opposite during new moon
days, the moon is not visible or in his first visible crescent
(illuminance is about 0.0001 lux). During first and third quarter
lunar phases, 50% to 99% of the disc is visible and illuminance is
about 0.01 lux (see Fig. 2) [54].
4. Video analysis
At the party level (hypothesis 1), a crop-raiding event started
when the first chimpanzee was recorded entering the field after at
least three hours without clip records and it ended when the last
chimpanzee of the party (visible from the clip) was recorded
leaving the field. At each event of crop-raiding, the party size
(number of different individuals recorded by the clips), the party
composition and the order of individuals crossing the bridging tree
while entering and leaving the maize field were determined
whenever possible. The composition of the entering party
sometimes differed from the leaving one as individuals may enter
or leave without being recorded on the video-clips.
At the individual level (hypothesis 2), a visit to the maize field
started when the chimpanzee entered the maize field by coming
down from the fallen trunk and ended when the individual
climbed again onto the fallen tree to return towards the forest.
However, not all the chimpanzees visible on the video-clips
entered the maize field (at least using the fallen tree), with some of
them staying at the forest edge, sitting or travelling along the
trench or on the fallen trunk.
We recorded the behaviour of each visible chimpanzee
(identified or not) in all clips. A clip in which n chimpanzees are
visible produces n individual sessions lasting from 19 to 309. The
set of clips nu1 to NuX will thus provide a total of N=n
1
+n
2
+.+
n
X
individual sessions. We counted the occurrence and the
duration of each possible behaviour linked to anxiety, vigilance or
to reduction of the risk of detection for each visible individual:
gentle and rough self-scratching (as described in [55])
scanning behaviours such as (i) guarding (standing in a
quadrupedal posture for more than five seconds without
moving [56]), (ii) bipedal position, (iii) arboreal scanning
behaviours (i.e. climbing up in a tree bordering the targeted
crop and watching in the direction of the field)
defecation and its consistency: diarrhoea can be induced by
fear and is used as an index of anxiety [57]
vocalisations produced, associated behaviours and context
(locomotion, feeding and social contexts)
vigilance or waiting time at the edge of the forest before/after
crossing the trench
locomotion type (suspensory or quadrupedal arboreal locomo-
tion used on the bridging tree) while the journey for crossing
and its duration to either go into or come back from the field:
the time each individual took to cross the trench from one end
to the opposite side of the bridging tree.
5. Data analysis
The data set allowed only basic non-parametrical statistical
approach because many observations did not enable reliable
identification of individual chimpanzees. While the video-trap only
captured the chimpanzees using the same access to the field and in
some occasion do not record the full party, we compared the
median of the party size during crop raiding and during feeding
acitivities in the forest, this last one calculated under the
chimpanzee habituation between February 3
rd
2009 and February
9
th
2013. It corresponds to the maximum number of chimpanzees
observed during a feeding bout (N=1 417; 61 577 minutes,
mean =43 minutes, SD=65 min). A feeding bout was considered
to start when at least a chimpanzee consumed a wild food item
and ended when all the party members stopped eating. To
compare the median of the feeding party size during crop raiding
events and during usual feeding in the forest we used a Chi-Square
test. To test for any sex/age differences in the diurnal or night time
durations (i.e. time spent into the maize field) we used Mann
Whitney U test since comparisons were made among different
individuals: e.g. in the suitable data available data on a whole
Nocturnal Activities of Wild Chimpanzees
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Figure 1. Uganda-Kibale National Park-Sebitoli area, home-range and maize field monitored (location of the guarding huts, the
fallen tree and the video-trap).
doi:10.1371/journal.pone.0109925.g001
Figure 2. Number of clips and number of individual sessions recorded by the video-trap from the 5th to the 25th of February 2013
according to lunar phases during this period.
doi:10.1371/journal.pone.0109925.g002
Nocturnal Activities of Wild Chimpanzees
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crop-raiding visit of an identified individual individuals who
made the night visits to the maize field were not always the same
individuals who made the day-time visits. For the same reason we
used the same test to compare the speed of suspensory locomotion
during night and day visits. To compare the occurrence of the
behavioural signs of vigilance and anxiety between day and night
incursions we used Wilcoxon exact test comparing the frequency
of each behaviour per minute of video record in the two conditions
(night and day).
Results
1 Hypothesis 1: developing group specific behaviours to
avoid detection in response to a risky situation
1.1 Infrequent incursions into the maize field. During
the 20 days of the study, a total of 14 crop-raiding events were
recorded by the activation of the video-trap. Images of wild
animals (chimpanzee, civet, red tail monkey) were captured in 122
clips of 30 seconds each during seven days and included 120 clips
of chimpanzees for a total of 60 min of records. During the first
part of the study period (February the 7
th
the 10
th
), crop-raiding
events occurred at least once a day (71 clips out of 120), and later,
visits were spaced every one or two days (Figure 2).
1.2 Crop-raiding in small parties. In the 14 journeys in
which the number of chimpanzees entering or leaving the maize
field was determined, the median of the party size was 8.20
chimpanzees (range: 317 individuals), thus more than double the
median of the party size (3 chimpanzees; range: 130 individuals)
of the same community during feeding activities in the forest
(measured from 1 417 observations of 61 577 minutes).
1.3 High ranking males leading the activities. The 120
clips of chimpanzee records provided 354 individual sessions.
Those individual sessions in which sex and age class of individuals
can be identified (330 out of 354) showed the presence of all age/
sex classes (n of sessions for adult males: 56, adult females: 144,
sub-adult females: 12, sub-adult males: 12, juveniles: 61, infants:
45) with a proportion not significantly different from the usual
party composition of Sebitoli community during feeding bouts
(Figure 3, Chi-Square =0,232, df =5, P=0.999). In the 277
individual follows in which we were able to determine the exact
identity of the individual (N
individual
=29; mean number of clips/
individual =9.60; range: 139), mean time in the videos/
individual =49050 (89259280), 139 observations correspond to
females (559470), 138 to males (1h00210) and 134 correspond to
chimpanzees going into the field, 119 coming back from the field,
24 being along the trench. Vulnerable individuals such as females
with clinging infants (N=3, respectively in 39, 5 and 2 clips) and
severely mutilated individuals were recorded on clips, these
include two individuals missing feet (19240 on 6 clips and 590 in
3), a female missing four fingers to the left hand (39030 in 10 clips)
and a juvenile with an unconsolidated broken leg (139170 in 33
clips). Mainly females led the party entering the maize field (five
out of seven crop-raiding events).
2 Hypothesis 2: specific individual behaviours to limit the
risk of being detected
2.1 Being vigilant. Before entering the field, chimpanzees
displayed scanning behaviours (25 guarding postures, seven
bipedal postures, two arboreal scanning in a high eucalyptus tree
growing at the border of the field; clip S1) (Figure 4) and some
individuals were not entering the field, staying at the edge. While
in the maize field, chimpanzees were sometimes chased by barking
dogs (N=3 clips) or run after by the guardian of the field (N=1),
who threw a branch towards a severely mutilated adult female
who hurried to cross the bridging tree. The screams and barks of
chimpanzees during these events and the records of self-scratching
behaviour and emission of soft/diarrheic faeces (Figure 4) in other
occasions also indicated anxiety and perception of a risky situation.
In twenty-two cases, chimpanzees came back from the field with
ears (one to six pieces) or stems (six pieces) (clip S2) and among the
half of them who were identified, six were females (carrying 14
items), five were males (bringing back nine items). Chimpanzees
rarely transport wild food. Such transport of food items may
indicate that chimpanzees were not ease to consuming crops in the
field and felt at risk by staying in the field.
2.2 Being silent and focused on the risky activity. A total
of 36 events of vocalisations were recorded during 34 clips: grunts
were the most frequent type of vocalisations (5 foodgrunts and 23
social pantgrunts), and louder vocalizations such as whimpering
(N=4), high screams (N=2), panthoots (N=1) and waabark
(N=1) occurred at a lower frequency. All vocalisations, except the
screams and bark, were produced in social or feeding contexts.
Interestingly, other social behaviours, usually absent during tense
or risky situations, have been observed at the border of the trench
such as a copulation, a female-female genital inspection and
genital touching (a sort of greeting also described in Bossou and
Nimbas chimpanzees [58]; clip S3).
2.3 Rushing. In the six events of crop-raiding recorded, in
which we can clearly identified the individuals entering and going
out of the maize field, the raids ranged from a minimum duration
of 79240 to a max of 2h299020. The individual mean duration of
the visits to the maize field was 409090 (19590-2h269390) based on
25 visits of identified chimpanzees going into the field and coming
back. Adult males do not spend a significantly longer time in the
maize field in comparison to adult females (average duration: adult
male =1h259110 (39560-2h289170, N=4), adult females =209510
(19590-1h579130, N=12) Mann Whitney U exact, U=12,
P=0.226). Severely mutilated individuals (three males and one
female) stayed on average 379360 (19590-2h259160) in the field
(N=7 visits). Both male and female chimpanzees visiting the field
plantation were thus neither rushing to consume the maize nor
leaving quickly the forest edging the maize field (average:
females =19410 (50-129540), males =19570 (40-249100) from 21 tree
crossings by 11 different females and 27 for 16 different males
(Mann Whitney U Test, U=281, P=0.958).
2.4 Extension of the period of activity to darkness. Forty
one per cent of chimpanzee clips (N=120) were recorded between
sunfall (7:07pm) and midnight, a time where chimpanzees are
usually resting in arboreal night nests, 19 of them occurring after
twilight. More than one third of nocturnal individual sessions (40
out of 114) occurred after twilight. Identification of chimpanzee at
night in IR images was often challenging (10 night visits out of the
25 in which we can identify the individual both entering and
coming out of the maize garden), however for seven instances the
whole raid occurred for clearly identified chimpanzees after the
sunset (range: 19:2119:48). No clip was recorded before sunrise
(7:01 am), and only a short crop-raiding event (79240) by six
individuals (four adult females and their dependants) occurred
before 12.00 am. All night crop visits occurred during new moon,
at the beginning of quarter moon or end of third quarter, thus
when the night is darker than a full-moon period [53] (Figure 5).
While during the day, chimpanzees generally stopped and sat on
the bridging tree before entering the maize field, during night visits
chimpanzees did not show hesitation and crossed rapidly the
bridge to enter the field, using more frequently suspensory
locomotion (66% vs 41% during daily visits), as opposed to
quadrupedal locomotion during the day (Figure 6). In all
nocturnal visits, even when chimpanzees screamed due to the
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noise of barking dogs, they did not flee from the maize field;
instead they came back into the forest relatively slowly (clips S4,
S5, S6). Adults and sub-adults spent a longer time in the maize
field during night visits than during day light visits (median of the
duration in the field: night =1.120 (N=7), day =0.208 (N=10);
Mann Whitney U Test, U=12, P=0.024). Overall signs of
vigilance and anxiety occurred all at higher frequency during the
day than during night incursions (Figure 3; Wilcoxon exact test,
T+=0, N=5, P =0.043).
Discussion
Contrary to our expectations, despite the fact that crop-raiding
have various costs perceived by the chimpanzees, the Sebitoli
chimpanzees did not use behavioural strategies usually used in
response to a risky situation. Instead, they display an innovative
behaviour, raiding cultivated maize after sunset.
1. Repeated nocturnal activities outside of moonlit nights
The most surprising innovative behaviour captured on video
traps is undoubtedly the night incursions into the maize field by
Sebitoli chimpanzees. Indeed, chimpanzees preferred to visit the
maize field during late afternoon or after sunset, staying twice as
long in the field at night than during daylight. Some of the raids
started before the sunset and continued after it but several of them
occurred at twilight or even after it, in complete darkness.
Nineteen clips out of 120 were recorded more than one hour after
sunset, i.e. after twilight, when the illuminance is very low (0.0001
Figure 3. Party composition during forest feeding activities and activities at the border of the maize field.
doi:10.1371/journal.pone.0109925.g003
Figure 4. Frequency of signs of anxiety and vigilance in chimpanzees during day and night crop-raiding (occurrence of each
behaviour per minute of video record).
doi:10.1371/journal.pone.0109925.g004
Nocturnal Activities of Wild Chimpanzees
PLOS ONE | www.plosone.org 6 October 2014 | Volume 9 | Issue 10 | e109925
0,1 lux according to lunar phases during the study period [37,38].
No other previous studies reported crop raiding after sunset. In
Bossou, where chimpanzees consume 17 different types of
cultivated foods, no relationship with time of the day has been
recorded [45,59] except for cassava (Manihot esculenta). The
majority of cassava raids occurred during afternoon-time, with a
greater-than-expected frequency [45,59]. This suggests that
cultivated sugar fruits attract chimpanzees who raid any time
during the day, but for cassava, the high frequency at the end of
the day suggests they probably first tried to feed on wild food but
because of food scarcity they were pushed by hunger to take risks
to obtain crops. In Sebitoli, the screams and barks of chimpanzees
during crop-raiding, self-scratching behaviour and emission of
soft/diarrheic faeces indicated anxiety and perception of a risky
situation. Signs of anxiety and vigilance were less frequent after
sunset than during day hours where they seemed tenser. At night,
they also enter quickly into the field using suspensory locomotion
showing less hesitation and do not rush when leaving it.
In fact, chimpanzee nocturnal raids were not marginal during
our study period as 41% of the time spent at the border of the
maize field (N=120 clips i.e. 60 min) occurred during night hours.
To our knowledge, this is the first report of long, repeated and
group night activities by a great ape species outside of moonlit
nights. As of today, the nightlife of chimpanzees has been
neglected and we have probably missed some interesting activities
as night-time lasts around half of each 24 h in the equatorial
regions.
2. Chimpanzees raid in large parties including vulnerable
members
Considering the context of Sebitoli where people are actively
guarding their field at crop maturity, perception of local people
who rarely report chimpanzee incursion and previous surveys
conducted in the area of KNP, the number of 14 crop-raiding
events in a short period of 20 days and the size and the
composition of the parties participating are surprising. However
Figure 5. Time distribution of crop-raiding activities recorded (number of clips and individual sessions) during daylight and night
including twilight and darkness period.
doi:10.1371/journal.pone.0109925.g005
Figure 6. Types of arboreal locomotion used during night and day to cross the trench using the bridging tree to go and come back
from the maize field (occurrence of each behaviour per minute of video record).
doi:10.1371/journal.pone.0109925.g006
Nocturnal Activities of Wild Chimpanzees
PLOS ONE | www.plosone.org 7 October 2014 | Volume 9 | Issue 10 | e109925
the study period is to short to conclude about the frequency of
crop-raiding in Sebitoli and to compare it to other sites like Bossou
where crop raiding bouts range from 5 to 45 per month [34] but
the absence of hesitation to enter the field at night as opposed to a
day-light raid in the same area and behaviour in the neighbouring
community of Kanyawara (Krief pers. observ.) indicates this is
probably usual. During nocturnal activities, chimpanzees most
likely feel more confident in coming out of forested areas to reach
open fields to access highly rewarding food. Contrary to
composition recorded in similar or other risky activities such as
territorial patrols, intergroup conflicts and crop-raiding at other
sites all biased towards males, in the Sebitoli incursions, all age/sex
classes were involved, including females with clinging infants and
severely mutilated individuals [16,34,45,60]. Even though we
acknowledge a small sample size, our data does not show evidence
of specific leading behaviour of the alpha male or high ranking
males to protect the individuals of the party entering into
cultivated land. Adult females were even observed leading the
incursion into the cultivation and the journey back to the forest,
while party composition does not show a sex-ratio biased towards
females.
During crop-raiding, we observed large party size (and this
number is probably underestimated since the bridging tree may
have not been the only way, even though preferential, to access the
maize field), even larger than the habitual party size of the study
community during feeding time. While a large party is more easily
detectable during day, the cost of vigilance for each individual is
likely reduced when travelling with more conspecifics, and during
night when the visibility is reduced, numeric inconvenience is
likely reduced. The fact that chimpanzees carry less maize from
the field to the forest during night means they most likely consume
it directly in the field. Indeed, emission of soft faeces, rough self-
scratching, bipedal positions showed that the border zone slightly
affected chimpanzee behaviour, which was anxious and vigilant,
especially during day. However, they were not avoiding the
location, even when humans were present, and did not really fear
villagers that were guarding their crops, entering when present and
staying close to the border after being chased. Previous surveys in
the same park reported that chimpanzees rarely raid crops unless
wild food availability is low [6]. Wilson et al. [29] considered such
observations as evidence that chimpanzees are sensitive to the cost
of crop-raiding and avoid the risk of being killed by humans. In
contrast with patrols where chimpanzees are usually silent and as
previously observed during crop-raiding for monkeys [29,61],
Sebitoli chimpanzees were not silent and did socially interact at the
border of the field. However, loud calls were rare and the only
male to pant-hoot in the maize field was the higher ranking male
as observed previously during periphery excursions [29]. Actually,
the production of loud calls recorded during excursions (also called
border checking to distinguish them from patrols) was
interpreted as advertising their presence and coalitionary strength
to intimidate neighbours [16,62].
3. Rapid adaptation to low predation risk and food with
high nutritive value
Although few examples have been identified in primates, the
ability to operate both at night and during the day is common
among mammals [63]. Cathemeral animals are characterized by
an extreme behavioural flexibility, and they may range from
almost full diurnality to almost full nocturnality [63]. Our closest
relative, the chimpanzee, does not show the physical adaptation to
nocturnal activities found in other primate species, such as
prosimians (e.g. large orbits and presence of tapetum lucidum,
the reflective layer behind the retina to enhance available light). It
is likely that in a diurnal species only multiple advantages would
lead it to engage in the risky behaviour of cathemerality. Among
the motivational causes suggested for cathemeral animals, three
main ecological benefits may be the ultimate reasons for the
activity shifts in chimpanzees: predator avoidance, the need to
complement their dietary requirements and heat stress avoidance
[39,40,41,64,65].
With regard to the first hypothesis, just a few predators (e.g.
snakes, humans) might threaten Sebitoli chimpanzees given that
leopards, which are the main nocturnal predator for this species,
are so rare in Kibale NP that they could not represent a threat for
chimpanzees ([36,66], Chapman pers. comm.). Local human
population, Bakiga and Batooro, do not eat chimpanzee meat but
they protect their field with snares and in Sebitoli, chimpanzees
are particularly affected since approximately 40% of the individ-
uals are victims of severe mutilations (Sebitoli Chimpanzee
Project, long term data). Field owners actively guard their cultures,
sometimes resulting in serious injuries to wildlife intruders. The
alpha-male of the Kanyawara chimpanzee community, neigh-
bouring the Sebitoli community, has been severely injured by a
spear [29,30]. Chimpanzees may have adapted ancestral anti-
predatory and patrol behaviour to face new threats (i.e. human
defence of crop fields, highway crossing) by using shift systems in
their activity period and improving cooperative behaviours to
maximise the protection of the party. However, while road
crossing or boundary patrols usually occur during the day, the
nocturnal crop-raiding activity displayed by Sebitoli chimpanzees
emphasizes their high level of flexibility and capacity for rapid
adaptation due to the likely predation by leopards 100 years ago in
Kibale NP making such nocturnal visits risky at that time.
Secondly, such adaptation may provide a significant supplement
to their natural diet adding food of higher nutritional quality (one
ear of maize provides 86 Kcal and is particularly high in
carbohydrate (19.2% compared to the average of 13.9% of 32 wild
fruits from Kibale; [67,68]. The consumption of several ears of
maize represents a high intake, as daily energy intake for Kibales
chimpanzees range from 1206 and 3333 Kcal on estimation [69].
Moreover, as usually in cathemeral species such flexibility may
depend also on seasonal variations in food availability in the forest
and/or seasonality in field cultivation for humans
[41,70,71,72,73]. Therefore, the fact that the maize was mature
when the wild food availability was not high (Intermediate Food
Availability between January and February 2013 calculated after
[46]), may have led hungry chimpanzees to risk more and take the
opportunity of consuming highly nutritive food while caloric intake
was not high during the day.
Interestingly the nocturnal behaviour in Sebitoli chimpanzees
during new moon, first or third quarter (absence of moonlight) was
inconsistent with previous records of cathemeral and nocturnal
primates showing general lunarphilia (cathemeral primates
[41,74], nocturnal primates [75,76], even after other rare
recordings of night activities in other chimpanzee communities
[16,43]. Two alternative hypotheses may be formulated to explain
such peculiar observations. The Sebitoli chimpanzees perform
night crop-raiding during the period of the absence of moon light
in order to be less detectable from humans or simply due to the
maturation stage of the maize that may disappear if they waited
for the full moon.
However, in chimpanzees, the absence of physical and
physiological adaptations to nocturnal vision raises the question
of how they are able to raid crops during dark nights. The high
anthropogenic pressure in the Sebitoli area deeply altered the
canopy and the forest cover. During the 609s and 709s, half of the
trees were destroyed by logging activities in almost the whole
Nocturnal Activities of Wild Chimpanzees
PLOS ONE | www.plosone.org 8 October 2014 | Volume 9 | Issue 10 | e109925
home-range of Sebitoli chimpanzees [48]. Therefore, chimpanzees
live today in a more open habitat with higher light penetration at
night than before and than in other more pristine forests. Such
increased light penetration may encourage them to travel and
forage later after sunset in crop plantations at the periphery of the
Park and to extend their activity over the 12-h gaining access to
higher energy and quality food. Such behaviour is observed in
Eulemur fulvus, mostly diurnal during long days of austral
summer, which becomes as active at night during austral winter
[41].
Indeed, as for other animal species, cathemerality seems to be
linked to a particular habitat, thus the exceptional nocturnal
activity of chimpanzees may be related to the peculiar feature of
the study area, a region where habitat loss and human population
expansion have resulted in severe encroachment on wildlife
habitat [77,78]. While in South-Western Uganda early agriculture
through forest clearing and environmental degradation started
4800 years ago [79], today the quasi totality of Ugandan forested
areas (98%) are considered as regenerated forests, and the
remaining 2% are planted forest exclusively with introduced
species [80] (e.g. eucalyptus, pines, cypresses [81]). This situation
contrasts with the worlds forests where primary forests (forest of
native species that have no clearly visible indications of recent
human activities) account for 36% and regenerated forests for 57%
of the total forest cover [80]. Additionally, considering the non
negligible amount of crops consumed by chimpanzees, it is urgent
to reconsider fertilizers and pesticides used in crops to avoid
contamination of wild surrounding habitat, soil and sediments and
to promote organic agriculture at the interface with wildlife. The
high frequency of congenital deformities observed in the Sebitoli
chimpanzee community of this study may be related to the
exposure to chemicals while crop raiding [47].
4. Conclusions
Even though the chimpanzees home range has been seriously
damaged and disturbed by both logging activities and significant
human demographic pressure, chimpanzees have shown great
behavioural flexibility including unexpected nocturnal behaviour,
in order to take advantage of the proximity of domestic nutritive
food. The new findings of chimpanzee nocturnal raids can aid to
formulate recommendations to local farmers and Park authorities
in addition to those already listed as best practice guidelines
from IUCN in terms of human-wildlife conflicts [82].
Supporting Information
Clip S1 13/02/2013, 18h019000 (duration 300) (daylight).
In this clip, an individual (not identified) climbs the
eucalyptus tree at the edge of the maize field for
arboreal scanning. An adult male and adult swelling female
cross the tree, both in quadrupedal arboreal locomotion, followed
by another adult male who crosses in suspension. Lastly, SA, a
sub-adult swelling female arrives and stands at the border of the
trench.
(AVI)
Clip S2 13/02/2013, 18h059090 (duration 300) (daylight).
This clip shows an adult male (NE) who comes back from the
maize field with six ears of maize (held by the mouth, by the right
hand and between the left arm and his body), a juvenile male (KI)
sitting on the bridging tree, his mother (KU) and another adult
female (KL) with clinging infant (KR) approaching the bridging
tree from the forest side.
(AVI)
Clip S3 13/02/2013, 18h059450 (duration 300) (daylight).
In this clip the old adult female (KU) touches the genital area of a
female (KL) with clinging infant (KR), a behaviour described as a
sort of greeting [56]. Then KL (with KR carried ventrally) crosses
the bridge in suspension, while KU together with another adult
female climbed the bridging tree where an adult male (NE) and his
juvenile son (KI) are sitting. A juvenile male (UL) faces the camera
trap.
(AVI)
Clip S4 13/02/201320h159270 (duration 300) (night
time, IR image). A chimpanzee coming from the field (with a
maize ear in his mouth) crosses the bridge in quadrupedal arboreal
locomotion and then in suspension to pass around another
individual who is feeding maize (stem and ear) on the bridging
trunk.
(AVI)
Clip S5 13/02/201320h249470 & 20h259230 (duration
26300) (night time, IR image). In these clips, some screams
and waa-barks are emitted, then a mutilated adult chimpanzee
(BM, whose left foot is missing) is coming back from the maize field
followed by four individuals (including one holding a maize ear
with the mouth). Among them ET, the alpha-male is pilo-erected
when crossing in suspension, but then sits across the trench, facing
the maize field.
(AVI)
Clip S6 13/02/201320h249470 & 20h259230 (duration
26300) (night time, IR image). In these clips, some screams
and waa-barks are emitted, then a mutilated adult chimpanzee
(BM, whose left foot is missing) is coming back from the maize field
followed by four individuals (including one holding a maize ear
with the mouth). Among them ET, the alpha-male is pilo-erected
when crossing in suspension, but then sits across the trench, facing
the maize field.
(AVI)
Acknowledgments
Data have been collected in the context of a scientific agreement signed
between National Museum of Natural History, Uganda Wildlife Authority
and Makerere University (SJ44512). We are grateful to Uganda Wildlife
Authority and Uganda National Council for Science and Technology for
authorization to conduct research and to the Museum national dhistoire
naturelle and Projet pour la Conservation des Grands Singes for logistical
assistance to the project. We thank Victoria Whitehead for her invaluable
work for anglicizing this manuscript. Special thanks to the staff of the
Sebitoli Chimpanzee Project and especially to Ugandan assistants for their
fieldwork.
Author Contributions
Conceived and designed the experiments: SK JMK. Performed the
experiments: SK JMK MC. Analyzed the data: SK MC SM. Contributed
reagents/materials/analysis tools: SK JMK AS. Contributed to the writing
of the manuscript: SK MC SB AS JMK SM.
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