PBPrimate BiologyPBPrimate Biol.2363-4715Copernicus GmbHGöttingen, Germany10.5194/pb-2-21-2015Dry season drinking from terrestrial man-made watering holes in
arboreal wild Temminck's red colobus, The GambiaHillyerA. P.alisonhillyer@yahoo.co.ukArmstrongR.KorstjensA. H.https://orcid.org/0000-0002-9587-4020Faculty of Science and Technology, Bournemouth University,
Dorset, UKCentre for Wildlife Conservation, University of Cumbria,
Cumbria, UKA. P. Hillyer (alisonhillyer@yahoo.co.uk)12June201521212421December201411May201512May2015This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://pb.copernicus.org/articles/2/21/2015/pb-2-21-2015.htmlThe full text article is available as a PDF file from https://pb.copernicus.org/articles/2/21/2015/pb-2-21-2015.pdf
Like most arboreal primates, red colobus monkeys obtain most water from
plants in their diet, licking their body or drinking occasionally from
standing water in tree holes. Terrestrial drinking is not normally reported
for arboreal primates. Here we report observations of terrestrial drinking
from man-made watering holes by Temminck's red colobus (Piliocolobus badius temminckii) in Abuko Nature Reserve and Bijilo Forest Park, The
Gambia. Colobus drinking behaviour in Abuko has been reported previously by
Starin (1991, 2002), mostly involving juveniles or lactating females; water
was most commonly obtained by licking water from the body and leaves or
obtained from tree holes. Some juveniles were seen drinking from swampy
ground and puddles in the dry season, but otherwise the only terrestrial water
body available to colobus during the study by Starin contained crocodiles, a
known predator of red colobus at the site. Our observations show that shallow
man-made watering holes that have since been created and do not harbour
predators were used by different age classes. We discuss some of the
implications of this behaviour for this endangered subspecies and report on
the trend of increasing temperatures in The Gambia.
Introduction
Observations of primate drinking behaviour are not regularly reported, but
terrestrial drinking events by arboreal primates do represent an interesting
behaviour considering the risk of predation and increased parasite–disease
risk associated with terrestriality, especially standing water. Arboreality
can help to evade soil-transmitted endoparasitism (Loudon and Sauther, 2013).
Parr et al. (2013) reported that white-faced capuchins (Cebus capucinus) were more likely to be infected with Strongyloides
sp.
during the dry season when the monkeys descend to the forest floor to drink.
Terrestrial drinking in most arboreal primate species is not reported;
however, there are notable examples: mantled howler monkeys (Alouatta palliata) came to the ground to drink from standing water in Costa Rica
during exceptionally dry conditions (Gilbert and Stouffer, 1989), and
Geoffroy's spider monkeys (Ateles geoffroyi) in Costa Rica are known
to drink from water holes (Chapman, 1988).
Here we report preliminary observations of an arboreal primate, Temminck's
red colobus (Piliocolobus badius temminckii), drinking from man-made
terrestrial water holes during the dry season in Abuko Nature Reserve and
Bijilo Forest Park, The Gambia. Prior to this study Temminck's colobuses were
recorded to drink occasionally in Abuko Reserve (Starin, 1991, 2002);
drinking was reported mostly in lactating females and juveniles and to occur
more in the wet (4/12 months: June–October) compared with the dry season
(8/12 months: October–June) during a 5-year study from 1978 to 1983 and a
further 6-month study in 1996. It is not known whether sampling effort was
equally distributed in the dry and wet seasons. Starin followed a focal
group, which had a natural water pool (0.8 % of the reserve area) within
their territory, but it was (and still is) inhabited by crocodiles, a known
predator of the colobus. The group were never seen to drink from the pool, but
juveniles were seen drinking from swampy ground and puddles
(5 × 7 cm) in the dry season.
Terrestrial drinking could be influenced by various factors such as absence
of predation pressure, group competition influencing spatial–temporal use of
home range, climate and habitat–dietary change related to water requirement.
In this paper we report drinking events from two different populations of
P. b. temminckii collected either via direct observation or camera
trapping and will discuss the data together with climate–temperature data
(since 1970).
MethodsStudy sites and species
Data were collected on Temminck's colobus groups in two isolated populations:
Abuko Nature Reserve (ANR) (13∘23′45′′ N,
16∘38′44′′ W) and Bijilo Forest Park (BFP)
(13∘25′58′′ N, 16∘43′35′′ W), The Gambia. Both ANR
and BFP are protected reserves and listed as two of the most important sites
for the subspecies (Butynski et al., 2013). Permits were obtained from the
Forestry Department to work in BFP and the Department of Parks and Wildlife
Management in ANR. P. b. temminckii is an endangered subspecies of
the western red colobus (P. badius); endemic to West Africa, it is
found in southern Senegal, The Gambia, Guinea-Bissau, NW Guinea and Sierra
Leone. The subspecies' range is considerably fragmented: the northern
boundary has retreated, and many populations exist in isolation (Galat et al.,
2009).
ANR is 106.6 ha in area, composed of gallery forest (16 %), tree and
shrub (56.6 %), savannah and woodland savannah (24.8 %),
crocodile-inhabited freshwater pool (0.8 %) and swamp (0.3 %)
(Starin, 1991). The freshwater pool and swamp is located in the home range of
two colobus groups (most likely to be the area used by Starin's focal group).
Apart from the freshwater pool and swamp there is a man-made pool, situated
in front of a hide in the home range of one group, here named “orphanage
group” (not the focal group during Starin's study). The pool is
approximately 2 m2 and 20 cm deep (if filled to maximum). The pool was
created in 1996 approximately and filled on an ad hoc basis. Green monkeys
(Chlorocebus aethiops sabaeus) frequented the pool to drink. Known
predators in the reserve include West African crocodiles (Crocodylus suchus) and snakes of different species (Starin, 1991). There is an
additional threat from domestic dogs entering the reserve; ANR is surrounded
by towns and agricultural land. The study was carried out between March
and June 2013 (dry season).
Average rainfall (mm) and maximum, mean and minimum
temperatures (degrees Celsius) per month of the year (from 1970 until 2011).
BFP is 51.3 ha in area and comprises a combination of sand dunes, savannah
and rhun palm forest. Possible predators here include snakes and feral dogs.
As in ANR two primate species inhabit this park: green monkeys and Temminck's
colobus. The colobuses in BFP do not flee from tourists and as such can be
regarded as semi-habituated. The forest has no permanent, natural sources of
drinking water; however, in 2009 two concrete-lined “water holes” were
created. Both pools are around 2 m × 3 m and are filled on an
ad hoc basis resulting in water depths of 0–20 cm. The data were collected
in April 2013 in BFP.
Behavioural sampling
Behavioural studies were carried out in ANR but not BFP. Dawn to dusk group
follows were carried out on 42 days (504 h). Most of the colobuses were very
shy and ran from people and as such could be considered unhabituated. One
group near the reserve entrance, named “entrance group” (most likely the
same area used by the focal group in Starin's study) could be considered
semi-habituated as they differed in their reaction to visitors. Five groups
(of an estimated seven groups) were followed; two groups were observed to have a
natural water pool within their range and another group, “orphanage group”,
a man-made water hole within its home range.
Trail camera data
In both ANR and BFP trail cameras were used to monitor activity at water
holes. In ANR, Bushnell “Trophy Camera” model 119437 was used for 4
consecutive days, 24 h a day, placed at approximately 1–2 m height off the
ground with a view of the whole pool. The Bushnell trail camera model is
triggered by movement. The data from BFP were collected with the same camera
model, positioned at 1–2 m height in a position where > 90 % of the
water hole could be monitored, for 10 days, 24 h a day. Typical human
disturbance at the water holes was 1–2 visits per day.
A summary of all drinking events observed (ANR being Abuko Nature
Reserve and BFP being Bijilo Forest Park).
SiteDate and timeDuration (minutes)No. ofindividualsAge and sexANR16 Apr 2013 5:06 p.m.Unknown (encountered bychance and interrupted)53 adults (sex unknown) and2 juvenilesANR18 Apr 2013 approx. 5:00 p.m.Unknown (encountered bychance and interrupted)10Not recordedANR5 May 2013 3:49 p.m.72Adult female with infantBFP18 Apr 201312:58 a.m.3610+Mostly adult females with infants and a few immature individualsBFP21 Apr 2013 2:30 p.m.1810+Mostly females with infants and immature individuals, briefly joined by adult male and what appeared to be 2 immature males; the immature males drank but the adult male did not.BFP21 Apr 2013 3:40 p.m.0.51A subadultBFP24 Apr 2013 9:45 a.m.0.53Adult female with infant and another adult femaleBFP24 Apr 2013 11:07 a.m.1085 adult females and 2 infants and a juvenileClimate data
Temperature and precipitation data were obtained from Yundum Meteorological
Station, 1.25 km from ANR. Mean annual temperature (∘C) and mean
annual precipitation (mm) data were analysed using linear regression analysis
in SPSS 10.0. The dry season is October–June (Starin, 1991); see absence of
rainfall in Fig. 1.
ResultsDrinking observations and trail camera data, Abuko Nature
Reserve
Eight drinking events were observed. Two of the events were seen during dawn
to dusk group follows in ANR; the other events were recorded using trail
cameras. Table 1 summarises all drinking events. On
16 April 2013, while
following the orphanage group, at 5:06 p.m. LT, 3 adults and 2 juveniles of unknown sex were seen drinking from the
man-made pool in their home range. Other juveniles were by the pool, but the
group fled when A. P. Hillyer was noticed. On 18 April 2013 in the late afternoon 10
individuals of unknown age and sex were seen drinking at the pool by a field
assistant. The “orphanage” group had been seen drinking from the pool on
various occasions by the field assistant before the start of this study. The
trail camera further recorded an adult female with an infant at the pool from
3:49 to 3:55 p.m., on 5 May 2013. The female squatted to drink but the
infant was not captured drinking (Fig. 2 in the Supplement).
Other orphanage group individuals were seen on various occasions around the
pool in mixed age groups but not drinking. In some cases a potential
drinking event may have been interrupted as a response to the observer.
Trail camera data, Bijilo Forest Park
During the data collection period, the water hole was visited on five occasions
by groups varying in size from a single individual to over 10 individuals
(Fig. 3 in the Supplement). Adult females drank from the pool (whether adult
males drank could not be determined), as did immature individuals; R. Armstrong
categorised groups of juveniles and subadults as one class: immature individuals.
Attendance time at the pools ranged from 0.5 to 36 min. The longest visits
were also the occasions on which most individuals were present (> 10),
whereas the shortest visit involved only a single individual. Colobuses did not
just visit the pools to drink; instead they stayed in the vicinity for some
time and engaged in social behaviour with conspecifics (including play-chases
and soliciting copulation) and green monkeys (play-chases). On
24 April 2013 a group of three colobuses (Table 1) were encountered drinking at the
water hole ad libitum at 9:45 a.m.
Climate data
Mean, minimum and maximum annual temperatures all increased significantly
between 1970 and 2011 (linear regression: df = 1 and 40: mean
temperature R2= 0.607, p< 0.001; Tmin: R2= 0.682, p< 0.001; Tmax:
R2= 0.426, p< 0.001). In contrast, mean annual precipitation
did not change significantly between 1970 and 2011 (R2= 0.48,
P= 0.162). Rainfall and temperature variation (measured as standard
deviation between months over the year) did not change significantly
(rainfall: R1,402= 0.044, p= 0.185; temperature:
R1,402= 0.041, p= 0.199). Temperature and precipitation
values can be seen in Fig. 4 (Supplement).
Discussion
The observations presented here suggest P. b. temminckii will use a
ground pool if available and safe. There are no crocodiles near the man-made
water holes at both sites during the day (they are known to travel in ANR at
night) (I. Jarjou, personal communication, 2013). With reference to ANR, prior
drinking observations reported for Temminckii's red colobus (Starin, 2002)
involved monkeys mostly licking water from leaves, tree bowls or their own
bodies. The only incidences of a terrestrial nature occurred in the dry
season, which involved juveniles sometimes drinking from swampy ground
(number of events unknown) and juvenile/immature individuals drinking on four
occasions from puddles. Contrary to our observations, Starin reported that
adults did not actively seek water nor did the colobus use a water hole.
However, there was no water hole available as a safe drinking resource for
the focal group during her studies. Furthermore, Starin observed a different
group to that which A. P. Hillyer observed drinking. As well as the limited
duration of our study this means a comparison cannot be made. Unfortunately,
there are no prior records of drinking behaviour in BFP.
Provisioning in the form of terrestrial, man-made water holes could pose
risks to the colobus such as increased exposure to disease or predation. They
are least careful when at ground level (Starin, 1991). Of particular concern
here are (1) the presence of domestic dogs in both ANR (Starin, 1991;
A. P. Hillyer, personal observation, 2013) and BFP (R. Armstrong, personal
observation, 2013), which are known to hunt colobus (Galat-Luong and Galat,
2005), and (2) in ANR livestock carcasses (used to feed captive hyenas within
the home range of the orphanage group) were left in contact with the ground, on which the colobus frequently cross. This has implications for colobus
health/survival. An increasing temperature trend was found for the period
1970–2011, but whether this has or will influence terrestrial drinking in
colobus cannot be determined with the present data. As mentioned before, ANR
and BFP are listed as two important sites for Temminck's colobus; the
threats discussed here warrant further long-term investigation.
The Supplement related to this article is available online at doi:10.5194/pb-2-21-2015-supplement.
A. P. Hillyer and R. Armstrong observed the
events in the field. A. P. Hillyer prepared the manuscript with contributions
from R. Armstrong and A. H. Korstjens. A. P. Hillyer and A. H. Korstjens
carried out statistical analyses.
Acknowledgements
The authors are grateful to the Department of Parks and Wildlife Management
and the Forestry Department, The Gambia, for allowing the research at the two
sites. A. P. Hillyer would like to thank Ibou Jarjou for his valuable
knowledge of the colobus in ANR and his assistance in the field. R. Armstrong
would like to thank Sulayman Jobe for his continued support and assistance in
BFP. Thank you to Mr Saikou Kolley, Yundum Meteorological Station. We also
appreciate the suggestions from Jan Gogarten and an anonymous reviewer, which
improved the manuscript. Edited by:
J. Ostner Reviewed by: J. Gogarten and one anonymous referee
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