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Afr.
J.
Ecol.
1990,
Volume
28,
pages
24G249
Differential foraging
of
oxpeckers on impala
in
comparison
with
sympatric antelope species
BENJAMIN L. HART, LYNETTE A. HART
and
MICHAEL
S.
MOORING
Department
of
Physiological Sciences, School
of
Veterinary Medicine, University
of
California,
Davis, Caiifornia
95616,
USA
and Department
of
Animal Physiology, University
of
Nairobi,
Nairobi, Kenya
Summary
Regression analysis performed on published observations of oxpeckers foraging
for ticks on different species of ungulates revealed a significant positive relationship
between number of red-billed oxpeckers per unit body surface area and species-
typical body weight. The relationship suggests that the larger ungulate species
maintain a higher density
of
tick mass per unit surface area. The impala is the
smallest ungulate that oxpeckers are reported to attend.
A
field survey ofattendance
by red-billed oxpeckers on impala and four other sympatric antelope (Thompson’s
gazelle, Grant’s gazelle, Coke’s hartebeest and topi), two of which are larger than
impala, revealed that only impala were attended by oxpeckers. Oxpeckers foraged
upon areas
of
the body that impala cannot reach with their own mouths by oral
grooming. The typical behavioural response of impala
to
oxpecker foraging was
toleration or accommodation. These observations suggest that impala harbour a
greater tick mass per unit body surface area than the other antelopes compared.
This could reflect the fact that impala inhabit wooded areas, reportedly higher
in
tick density than grassland areas inhabited by the other antelopes.
Key
words:
Impala, oxpecker, parasites, antelope, ticks, infestation.
Resume
Une analyse de regression exkcutee
a
partir d’observations publikes de pique-
boeufs cherchant les tiques sur diffkrentes especes d’ongults a reve1C une relation
positivement significative entre les nombres de pique-boeufs
a
bec rouge par unite
de surface corporelle et le poids corporel de l’espece. La relation siuggkre que les
plus grandes especes d’ongules abritent une plus haute densite de tiques par unite
de surface.
L’impala est le plus petit ongule sur lequel on ait rapport6 les ‘services’ des pique-
boeufs. Une etude de terrain sur la presence de pique-boeufs
a
bec rouge sur
l’impala et
4
autres antilopes sympatriques (gazelle de Thompson, gazelle de
Grant, bubale de Coke et topi), dont
2
sont plus grandes que l’impala, montre que
seul l’impala etait assist& par les pique-boeufs. Ceux-ci se nourrissent
a
des endroits
du corps que l’impala ne peut atteindre de sa propre bouche en grooming oral. Le
comportement reponse typique de l’impala
a
la presence des pique-boeufs est fait
de tolerance et d’acceptation. Ces observations suggkrent que l’impala abrite une
plus grande densite de tiques par unite de surface corporelle que les autres antilopes
de l’ktude. Ceci peut refleter le fait que l’impala habite des zones boiskes, bien
connues pour abriter une plus grande densite de tiques que les zones herbeuses
frequentkes par les autres antilopes.
Oxpecker Foraging on Impala
24
1
Introduction
Two species of tick birds are found in Africa: the red-billed oxpecker
Buphagus
erythrorhynchus
(Stanley), and the yellow-billed oxpecker
B.
africuna
(Linnaeus).
The yellow-billed oxpecker, with a broad heavy bill, feeds with a pecking or
plucking action to remove adult ticks and seems to prefer buffalo
(Syncerus cafler
(Sparrman)), black and white rhinoceros
(Diceros bicornis
(Linnaeus) and
Ceratotherium sirnum
(Burchell)), zebra
(Equus
spp.), eland
(Trugelaphus oryx
(Pallas)) and giraffe
(Girafu camelopardalis
Linnaeus), which generally have
moderate to heavy tick loads and large feeding surface areas (Attwell, 1966;
Grobler
&
Charsley, 1978; Hustler, 1987). The red-billed oxpecker, on the other
hand, has a narrower bill that is used in a scissoring action to grasp larval and
nymphal ticks in addition to plucking adult ticks and is typically seen on a wider
range of host species, including the more densely-furred, medium-sized antelope
such as greater kudu
(Tragelaphus strepsiceros
(Pallas)), sable antelope
(Hippotragus niger
Harris), roan antelope
(Hippotragus equinus
(Desmarest))
and the smaller impala
(Aepyceros melampus
(Lichtenstein)) (Atwell, 1966;
Bezuidenhout
&
Stutterheim, 1980; Buskirk, 1975; Mundy, 1983).
Oxpeckers depend on the presence of ticks on domestic and wild ungulates for
the mainstay of their diet (Attwell, 1966; Bezuidenhout
&
Stutterheim, 1980).
Stomach analyses of free-living oxpeckers by Bezuidenhout
&
Stutterheim
(
1980)
revealed that the average bird had approximately
400
ticks in its stomach, and that
captive oxpeckers can consume as many as
7000
larval or 60 adult ticks in 24 hr.
When cattle were experimentally infested with larval ticks, foraging by red-billed
oxpeckers was found to reduce the number
of
ticks by twenty to 99%, depending
on the developmental stage
of
ticks that the birds were allowed to feed upon. The
greatest reduction in ticks occurred when the oxpeckers were allowed to feed on
adult ticks (Bezuidenhout
&
Stutterheim, 1980).
For oxpeckers to continuously associate with an ungulate species the foraging
must be cost effective, that is, there must be enough ticks on the typical host to
support the energy expenditure of first finding the host animal and then searching
for ticks. Several factors would be expected to influence the economic feasibility of
exploiting a given host species. One major influence is host size. Larger ungulates,
which are reported to harbour a larger proportion of adult ixodid ticks than
smaller ungulates (Horak, 1982; Horak
et al.,
1983), would be expected to be more
commonly frequented by oxpeckers than smaller ungulates, which harbour more
larval and nymphal stage ticks. Larger ungulates could attract more oxpeckers per
animal either because they support a greater tick mass per unit body surface area
than smaller ungulates, or because they possess a greater absolute surface area to
forage upon. In addition to host size, ungulate species that inhabit regions of high
tick density where individuals are likely to pick up many ticks should be more
preferred by oxpeckers than ungulates living in a lower tick-density habitat.
Finally, whether an animal tolerates or rejects a tick bird’s foraging actions would
also influence whether animals are attended by tick birds. Members of an ungulate
species that are not customarily attended by tick birds may be intolerant of
a
bird
alighting on them. Assuming that removal of ticks contributes to an animal’s
fitness, one would expect a species whose members typically harbour large
numbers
of
ticks to have evolved behaviour accommodating or facilitating the
foraging patterns of the birds.
242
Table
1.
Body weight and
observed oxpeckers on
ungulates
B.
L.
Hart,
L.
A.
Hart and
M.
S.
Mooring
No.
of
oxpeckers per animal’
Species Body wt
(kg)’
Red-billed Yellow-billed
White Rhino 4125 0.452
Black Rhino
1
I50
0,833
Buffalo 650 0,429
Giraffe 650 0.207
Eland 575
-
Sable 328
-
Zebra 27
1
0.0707
‘Body weight data are from Kudu 234 0.0322
IOxpecker tending data Nyala 104 0.0168
from
Stutterheim
(1980)
and Impala 56 0,00793
Grobler
&
Charsley (1978).
Haltenorth
&
Diller (1980). Wildebeest 214
0.01
12
0.133
0,214
0.0527
0.0677
0.0264
0,0668
0.0109
0.003 19
-
-
-
A
perusal of the literature documenting oxpecker counts on various ungulate
species indicates that larger ungulates attract oxpeckers more frequently than
smaller ungulates (Grobler
&
Charsley, 1978; Stutterheim, 1980; Stutterheim
&
Panagis, 1985). These studies further suggest that oxpeckers forage almost exclus-
ively upon large or medium size ungulates, as smaller species of gazelle
(Gazeflu
spp.), hartebeest
(Alcelaphus buselaphus
Pallas), and topi
(Damaliscus
lunatus
Burchell) are not mentioned in the reports or are mentioned as not being attended
by oxpeckers. An exception to this generalization is impala, a relatively small
antelope attended by oxpeckers in Kenya (Hart
&
Hart, 1988) as well as in Zambia,
Zimbabwe, Botswana and South Africa (Attwell,
1966;
Grobler
&
Charsley, 1978;
Stutterheim, 1980; Stutterheim
&
Panagis, 1985). If the attractiveness of an
ungulate for foraging by oxpeckers is related to body size, and impala are unusual
among smaller ungulates in being attended by oxpeckers, these findings would
suggest that impala harbour more ticks than comparably sized antelope. Heavier
tick loads could be a function of impala habitat preference, social behaviour, and/
or
foraging habits.
To
obtain a quantitative expression of the relationship between ungulate body
size, surface area and attending preference by oxpeckers we conducted an analysis
using the oxpecker density (‘preference’) values from Stutterheim (1980) for red-
billed oxpeckers and from Grobler
&
Charsley (1978) for yellow-billed oxpeckers.
Preference values (oxpeckers per animal) for various ungulate species are tabulated
in Table
1.
Data on the white rhinoceros were not included in the analysis because
its weight is four times that of the next heaviest species. Stutterheim
&
Panagis
(1985) also reported on number of oxpeckers per animal and their findings were
similar to the two studies we utilized. Published body weights from Haltenorth
&
Diller (1980) were averaged for males and females to obtain mean species mass
(Table 1).
Simple linear regression was performed separately for red-billed and yellow-
billed oxpeckers. We first plotted number of oxpeckers per animal against body
mass. Because larger body mass
is
confounded
by
greater absolute surface area
(and length) available for foraging, the preference values were adjusted to reflect
2
0.6
a,
0
a,
Q
0.4
0.2
t
0
Oxpecker Foraging on Impala
243
8
8
n
AA
8
A,
5
=o.otfi*
*
I
I
I
I
0
200
400
600
800
1000
1200
Species-typical
Mass
(kg)
Fig.
1.
Scatter plot of number
of
red-billed oxpeckers
(0)
and yellow-billed oxpeckers (A) per animal
as
a
function
of
species-typical body mass.
There
is
a
significant positive relationship for red-billed oxpeckers
(y=
-0.1
14+0.001x,
$=0.92, P=0.0002),
but
not
for
yellow-billed oxpeckers
(r’=0.46,
P=0.09).
density of oxpeckers per unit surface area. The number of oxpeckers per animal
was divided by body mass raised to the allometric exponent of
0.67
in order
to
convert mass to relative surface area (Schmidt-Nielsen, 1984). We omitted the
allometric coefficient
(w
10 for the mouse-to-elephant curve) because the calcu-
lations were for comparative purposes only. The adjusted value was then regressed
against body mass. Preference values were similarly converted to oxpeckers per
unit body length by dividing by mass raised to the
0.33
power (Economos, 1983)
and regressed against body mass.
A
scatter plot of oxpeckers per host animal as a function of body mass (Fig.
1)
indicates a positive relationship for red-billed
Cy
=
-0.1
14+
O.OOlx,
r2
=
0.92,
P=
0.0002), but not for yellow-billed oxpeckers
(r2
=
0.46,
P=
0.09).
When the
adjustment was made to hold body surface area constant by dividing by rna~s~’~’,
regression revealed a significant relationship for red-billed
0,
=
-
0.0003
1
+
0-OOOOlx, r2
=0-89,
P=
0-0004; Fig. 2), but not for yellow-billed oxpeckers
(r2=
0.32,
P=
0.19). With oxpecker density adjusted for body length regressed
against body mass, again there was a significant relationship for red-billed
oxpeckers
(y
=
-
0.0085
+
O.O0007x,
r2
=
0.92,
P=
0.0002) but not for yellow-billed
oxpeckers
(r2
=
0.41,
P=
0.12). We conclude that red-billed oxpeckers prefer larger
host species, and that this preference is over and above the factor of greater surface
area and length.
Because
of
this robust relationship between body mass and red-billed oxpecker
attendance, with impala being the smallest antelope species attended, we were
interested in determining if impala were unique among smaller antelope in attract-
ing oxpeckers.
A
field study was conducted to compare oxpecker attending of
impala with other small or medium sized antelope in the same area. Two of the
species, topi and Coke’s hartebeest, are larger than impala, one species, Grant’s
gazelle
(Gazella granti
Brooke), is about the same size, and one species, Thomson’s
gazelle
(G. thomsoni
Giinther), is smaller (Table
2).
244
B.
L.
Hart,
L.
A.
Hart and
M.
S.
Mooring
,
,
,
,
,
,
0
Species-typical
Mass
(kg)
Fig.
2.
Number
of
red-billed oxpeckers per unit body surface area (number of oxpeckers divided by
masso6’)
regressed against species-typical body mass. The relationship is highly significant
01
=
-0.0003
1
+
O~OOOO~X,
f2
=
0.89.
P=0.0004).
Dashed lines indicate
95%
confidence bands. Species abbreviations are:
I,
impala.
N,
nyala;
W,
wildebeest;
K,
kudu;
Z,
zebra;
G,
giraffe;
B,
buffalo;
R,
black rhinoceros.
Materials
and
methods
The principal study took place in the Mara region (inside and outside of the Masai
Mara Reserve) and on farms in the Lake Naivasha area of Kenya. The species
observed in both areas were Thomson’s gazelle, Grant’s gazelle, impala and Coke’s
hartebeest. Topi were observed in the Masai Mara area only. Impala were also
observed in the Lake Nakuru area as a separate non-comparative project since the
comparison antelope species are not found in Nakuru National Park. Both female
groups, consisting usually of several females and one territorial male, and all-male
bachelor groups were observed for all species.
Impala inhabit open woodland areas and in this study they were observed
mostly at the interface of wooded areas and grassland meadows or plains. The
other antelope inhabit mostly grassland areas, although they were sometimes near
wooded areas. All observations were made from four-wheel-drive vehicles using
binoculars or a spotting scope. Groups
of
either female or male bachelor antelope
were observed at distances of 50-200 m for the presence
of
oxpeckers attending any
animals in the herd. Groups were observed for 5-20 min before concluding that
there were no oxpeckers. The number
of
antelope per herd and the maximum
number
of
oxpeckers seen during the observation period were recorded. Herds
were observed just once on any given day. An attempt was made to observe as
many separate herds of animals as possible in order
to
avoid pseudoreplication
(Machlis
et
al.,
1985).
If
oxpeckers were present, some animals were chosen for
focal observations and the total time spent on the antelope
by
the bird and the body
parts foraged upon were recorded. Any immediate rejection of an oxpecker that
Oxpecker
Foraging on Impala
245
Table
2.
Antelope groups
observed
with foraging oxpeckers in Mara and Lake Naivasha
~~~ ~ ~ ~ ~ ~ ~~~~
Mean
no.
%
of groups with
No. of groups animals per group
one
or more oxpeckers
Species Body wt
(kg)'
Female Male Female Male Female Male
T.
Gazelle
22 63
45
15
15
0
0
G. Gazelle
55
62
34
10
10
0
0
Hartebeest
159 44
17
24
10
0
0
Topi
118
24 2 9
8
0
0
Impala
56
49
68
28
16 13
12
'Body weight data are from Haltenorth
&
Diller
(1980)
alighted upon an antelope (flicking away with muzzle, head toss, jumping) was also
noted.
Both red-billed and yellow-billed oxpeckers are widely sympatric in Kenya, but
the red-billed is by far the most common (Lewis
&
Pomeroy,
1989).
Positive identi-
fication of the species
of
oxpecker, presumed to be red-billed, was often difficult
because of the distances
of
observation, obstruction of the bird's heads by the focal
animal's body and rapid movement
of
the birds. Whenever the bill was seen the
bird was identified as the red-billed oxpecker.
Results
Species-typical body weights, averaged across males and females, number of
groups observed and the mean number of adult animals per group are presented in
Table 2, along with the percentage of groups observed in which at least one
oxpecker was seen attending one or more animals.
No
oxpecker was ever seen in
association with antelope of any species other than impala. There was no evident
relationship between mean group size and the presence
of
oxpeckers. In the com-
bined Mara and Lake Naivasha areas, 13% of female impala groups
(n
=49)
and
12% of male groups
(n
=
68) had at least one oxpecker attending animals in the
group. In Nakuru Park, 36% of female groups
(n
=
14) and 20% of male groups
(n
=
5)
were attended by at least one oxpecker.
Sixty-three impala served as focal animals for the analysis of the time oxpeckers
spent on the animals and the body parts foraged upon. Of these subjects, three
rejected the oxpecker by shaking or tossing the head or body as soon as the bird
alighted on them. If the oxpecker was not
so
rejected the time spent on an individ-
ual impala ranged from 3 sec
to
21 min, with a median of 2.5 min. The number of
oxpeckers seen foraging on an impala at one time ranged from one to three, with 47
impala attended by one oxpecker (78%), and seven and six impala tended by two
and three oxpeckers, respectively. In one case a bird was seen flying from a giraffe,
upon which it had been foraging, to an impala, and in another instance an oxpecker
flew from an impala to a zebra.
Of
the body parts foraged upon by the birds, the ears, both inside and outside,
were attended the most; this occurred in 72% of the impala observed. Other body
parts attended were the neck, periorbital area and eyelid, face and forehead, base of
246
B.
L.
Hurt,
L.
A.
Hurt
and
M.
S.
Mooring
cd
cd
-
60
-
-
m
0
9
40
0
c
c
c
20
0,
0
a
0
E
FF
N
VA
PT PE
H
I
Body
Part
Fig.
3.
Percent of focal impala in which various body parts were foraged upon at least once by red-billed
oxpeckers. Abbreviations:
E,
ears;
FF,
face and forehead;
N,
neck;
VA,
ventral abdomen;
PT,
perianal and
tail;
PE,
periorbital and eyelid;
H,
base
of
horn;
I,
inguinal area.
horn, ventral abdomen, perianal area and tail, and inguinal area between the hind
legs. Fig.
3
presents the percent of focal impala in which these body parts were
foraged upon at least once.
With oxpeckers foraging on the ears and around the eyes, rather obvious
accommodation movements by the impala were noted. The ears were often held
still while the birds foraged for ticks inside the pinna despite what must have been
uncomfortable stimulation from the oxpecker entering the pinna, sometimes a
distance of half the bird’s body length. The ear was frequently lowered in an
apparent effort to facilitate the bird’s entrance into the pinna or access to the base
of the ear. When oxpeckers tended the areas around the eyes, which also must have
been uncomfortable, the impala closed the eyes, while continuing to allow the birds
to forage on the periorbital area and eyelid. The scissoring action characteristic of
red-billed oxpeckers was performed when the birds foraged on the forehead and
neck. Pecking or plucking movements occurred, however, when the birds foraged
upon the ears, around the eyes, near the horn base, on the ventral abdomen or
around the perianal areas. There were instances when oxpeckers were flicked off
after being allowed to forage on several body parts but these actions were not
classified as rejections.
Discussion
The regression analysis of numbers of oxpeckers per unit of body surface area or
body length reveals a highly significant relationship between species-typical mass
and attending by red-billed oxpeckers even when surface area or length are held
constant, indicating that larger-sized host species are more attractive to red-billed
oxpeckers independent
of
their greater available surface area and length. This
suggests that larger species have more tick mass available per unit of surface area
than smaller ungulates. No relationship was revealed for yellow-billed oxpeckers.
There are undoubtedly other factors such as habitat preference, fur density and
behavioural adaptations that influence species preference by oxpeckers. However,
Oxpecker Foraging
on
Impala
247
body mass (with surface area held constant) accounted for 89% of the variation in
species selection by red-billed oxpeckers. We therefore conclude that red-billed
oxpeckers preferentially attend the larger host species primarily in order to exploit
a higher density of ticks on the large-bodied animals.
By removing large amounts of blood, engorging adult ticks can represent a
substantial drain on body reserves (Little, 1963; Williams, Hair
&
McNew, 1978).
Given the blood
loss
and release of toxic products from engorging ticks, larger
species, with a smaller surface
to
volume ratio, would be expected to tolerate a
higher density of ticks than smaller ungulates.
Absence
of
any sightings of oxpeckers in groups
of
Thomson’s gazelle, Grant’s
gazelle, topi, and Coke’s hartebeest indicate that these small and medium size
antelope are rarely, if ever, attended by oxpeckers. No other report of oxpeckers on
ungulates has mentioned these species as being attended by oxpeckers. In 12-13%
of impala groups which were sympatric with the above antelope, however,
oxpeckers attended one or more group members. At Lake Nakuru Park
2&36%
of
impala groups were attended by oxpeckers. The birds attended primarily the head
and neck of impala. This is in agreement with observations of oxpecker foraging
behaviour by Mengesha (1978).
The consistent sighting of oxpeckers on impala, but not on comparably-sized
or somewhat larger antelope, is an indication that impala typically carry more tick
mass per unit surface area than the comparison species. As mentioned, smaller
ungulates are reported to harbour a greater proportion of larval and nymphal stage
ticks than large ungulates. In particular, MacLeod
et
al.
(1977) and Horak (1982)
have found that impala carry a much smaller proportion of adult ticks than do
cattle. Thus, impala may not harbour a large number of adult ticks, but have more
larval and nymphal ticks than the comparison antelopes of medium size. Perhaps
a relatively heavy load of immature ticks combined with the tendency for impala
to form large, tightly clustered groups (Jarman, 1979) makes impala attractive
foraging subjects for red-billed oxpeckers adapted to collecting immature ticks.
Self-grooming with the mouth and scratching with the hind hooves are com-
monly displayed by
all
antelope species in this study. Oral grooming in cattle has
been shown to be highly effective
in
removing ticks (Bennett, 1969; Snowball,
1956). Undoubtedly this is true in antelope as well. Estimates of oral self-grooming
rates range from
600
to
1000
oral grooms in a 12-hr day for individual Grant’s
gazelle, wildebeest
(Connochaetes taurinus
Burchell) and impala (Hart
&
Hart,
1988). This amount of self-grooming, together with whatever other tick avoidance
behaviour and immune responses may be operating, appears to keep tick loads on
most antelope below the threshold that would attract oxpeckers. Impala, however,
not only self-groom the same as other antelopes, they also engage in reciprocal
mutual grooming of the head and neck, a behaviour not reported in any other
antelope species (Hart
&
Hart, 1988). Just as oral self-grooming in impala removes
ticks from the thorax, abdomen, and legs, mutual grooming undoubtedly func-
tions to remove ticks from the head and neck, which the animals cannot reach with
their own mouths.
Assuming that susceptibility to tick infestation could provide the selection
pressure for reciprocal mutual grooming, both attending by oxpeckers and the
mutual grooming behaviour
of
impala would be an indication that impala acquire
more ticks in their brushy habitat than sympatric antelope do on open grassland.
248
B.
L.
Hart,
L.
A.
Hart
and
M.
S.
Mooring
Woodland areas are consistently reported to support more ticks than open grass-
land (Londt
&
Whitehead, 1972; Norval, 1977; Semtner
&
Hair, 1973). Tolerance
and accommodation of tick birds and reciprocal mutual grooming both appear to
be behavioural strategies utilized by impala to cope with an increased exposure to
ticks.
Acknowledgments
We acknowledge the cooperation of the Kenyan Wildlife Conservation and
Management Department in the Ministry of Tourism and Wildlife. Participants in
the University Research Expeditions Program enthusiastically contributed their
abilities. We thank A.A. Heusner for helpful suggestions regarding the allometric
conversions, and A.A. Heusner and an anonymous reviewer for comments on an
earlier draft. Financial support for BLH and LAH was provided by the University
Research Expeditions Program, University of California, Berkeley.
MSM
was
funded by Sigma Xi, the Scientific Research Society, a University of California,
Davis Graduate Research Award and a Regents Fellowship.
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(Acarina: Ixodidae): Experimental infestations
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Exp. Parasitol.
26,323-328.
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&
STUTTERHEIM, C.J. (1980)
A
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