Evolutionary Ecology, 1997, 11, 91–104
Host preferences and behaviour of oxpeckers:
co-existence of similar species in a fragmented
landscape
W A L T E R D. KOENI G*
Museum of Vertebrate Zoology and Hastings Reservation, University of California, 38601 E. Carmel Valley Road,
Carmel Valley, CA 93924, USA
Summary
The host preferences and behaviour of red-billed and yellow-billed oxpeckers (Buphagus erythrorynchus
and Buphagus africanus) were studied at two locations in Kenya and combined with previously published
data from East and South Africa. Red-billed oxpeckers are generally more common and have a greater niche
breadth with respect to host preferences than yellow-billed oxpeckers, possibly due to the behavioural
dominance of the latter. Otherwise, the host preferences are remarkably similar: both prefer larger species
of ungulates and are found predominantly on species with manes. There are also no significant differences
in the time–activity budgets of the two species controlling for site and host species, and differences in the
proportion of time spent on different body parts of hosts are small in absolute magnitude even when
statistically significant. Despite these and other basic ecological similarities, no evidence for competitive
displacement was detected by comparing host preferences in areas of sympatry with areas of allopatry, even
though each species appears to depress the population size of the other when sympatric. Traditional singlecommunity competition theory cannot explain the geographical ecology of these two species. Instead, coexistence appears to be dependent on the patterns of extinction and colonization characterized by
metapopulations distributed among a fragmented habitat.
Keywords: Buphagus africanus; Buphagus erythrorynchus; co-existence; competitive displacement; host
preferences; metapopulation; oxpeckers
Introduction
Red-billed oxpeckers (Buphagus erythrorynchus) and yellow-billed oxpeckers (Buphagus africanus), the world’s only obligate mammal gleaners (Dean and MacDonald, 1981), exhibit a series
of highly derived adaptations for life with large mammals, including short, sharp claws that
facilitate clinging to hides, long stiff tails that can be used as support while clinging onto the
bodies of large mammals, and beaks that are laterally flattened and have a sharp cutting edge
suitable for handling ticks (Attwell, 1966). Except for the differing eye colour of the adults and
pale rump of the yellow-billed oxpeckers, they are easily confused for each other. Even their
social behaviour and breeding biology are similar, both being highly social cooperative breeders
that nest in tree cavities during the rainy season (Stutterheim et al., 1976). Their only
distinguishing morphological features are the slightly larger size (they differ approximately 7% in
wing length) and considerably broader, heavier and less scissor-like bill of the yellow-billed
oxpeckers (Attwell, 1966; Stutterheim et al., 1988).
Surprisingly, these differences have not been found to consistently result in differing host
selection, food preferences or foraging behaviour. Host selection is relatively easy to quantify and
* To whom correspondence should be addressed.
0269–7653
© 1997 Chapman & Hall
92
Koenig
has been examined by several authors. Some (e.g. Stutterheim and Panagis, 1985; Stutterheim et
al., 1988) have found that yellow-billed oxpeckers are more specialized and use a narrower
breadth of hosts than do red-billed oxpeckers. However, overlap is often considerable and studies
have generally found few consistent differences in host selection. Stomach content analyses
performed by Van Someren (1951) and Bezuidenhout and Stutterheim (1980) reported apparent
differences in the tick species utilized by the two species, but this result was not collaborated by
food preference studies performed on captive birds by Stutterheim et al. (1988). On the contrary,
these latter authors found that both species had approximately the same pattern of preference for
different species of ticks and were generally similar in their foraging behaviour, with the
exception of a slightly greater dependence on flies and larger ticks by yellow-billed oxpeckers.
Traditional competition theory predicts that such similar species should not persist sympatrically or, if they do, competitive displacement between them should be significant. In contrast
to the first of these predictions, red-billed and yellow-billed oxpeckers are sympatric throughout
much of East and South Africa (Mackworth-Praed and Grant, 1960), frequently being observed
together not only at the same site but even on the same individual host. Unless oxpeckers differ
in some previously unrecognized way, their co-existence throughout this large area presents an
intriguing and as yet unexplained ecological enigma.
Here I present new data on the behaviour of oxpeckers and synthesize new and existing data
on host preferences with the goal of re-examining the ecological similarity of the two species. I
then test for competitive displacement by comparing host preferences in areas of sympatry and
allopatry. In contrast to the second of the above predictions, these analyses confirm not only that
the two oxpecker species are extremely similar in their foraging ecology, but that no detectable
competitive displacement occurs in areas of sympatry. Finally, I discuss some of the factors that
may promote co-existence between these remarkably similar species.
Methods
Field studies
Field work was carried out at Lake Nakuru National Park and the Masai Mara Reserve, Kenya,
between 26 July and 17 August 1990. I collected three sets of data. Host preferences were
determined by surveying arbitrarily selected areas and counting the number of all potential hosts
present and both the number of oxpeckers on the hosts and the number of hosts with one or more
oxpeckers on them. A total of 11 censuses (25 h) over 6 days at Lake Nakuru and 17 censuses
(63 h) over 10 days at the Masai Mara were performed. The preference indices were determined
by dividing the number of oxpeckers observed on a species of host by the number of hosts
counted and multiplying the result by 1000.
Observations of foraging behaviour were made by watching focal birds and following them for
up to 25 min. Watches were terminated if the focal bird switched host species, but were
continued even if the bird changed hosts as long as the new host was of the same species. In
some cases, when more than a single bird was on a host at the same time, it was not always
possible to be certain that the same individual was being followed the entire time. However, once
an individual was chosen, it was followed as long as possible. Watches were made through
binoculars from a vehicle situated as close as possible.
Two mutually exclusive types of data were taken during separate behavioural watches. During
time–activity budget watches, I recorded the time spent in major activities including eating,
preening, vigilance behaviour, flying and being sedentary (the sum of all sitting, preening and
vigilance behaviour). During host watches I recorded two sets of data: (1) the number of
oxpeckers on the host and (2) where on the host the bird was located. The latter categories
included head, neck, front, undersides, back, tail, sides and rump. In both cases, data were
Co-existence of oxpeckers
93
recorded in real time onto a portable laptop computer using a modified event-recorder program,
stored on cassettes and later transferred to a personal computer where the time spent on each
activity or on each part of the hosts was determined for each watch. The proportions of time
spent in different activities were arcsin transformed prior to analysis. A total of 100 time–activity
budget watches (48 at Lake Nakuru and 52 in the Masai Mara) totalling 754 min of observations
(mean ± SD 5 7.5 ± 4.9 min) and 108 host watches (29 at Lake Nakuru and 79 in the Masai
Mara) totalling 761 min of observations (mean ± SD 5 7.0 ± 4.3 min) were taken. Watches were
considered independent and analysed using analysis of variance.
Synthesis with prior work
In order to gain a more comprehensive perspective on the foraging preferences of the two species
of oxpeckers, I summarized previously published studies on oxpecker host use, including all
studies reporting the number and species of oxpeckers observed on hosts. The studies were
divided according to the oxpeckers present; the species were considered sympatric if both were
observed regularly, while a species was considered allopatric at sites where . 98% of all
sightings were of that taxon. Four studies were performed in areas where only red-billed
oxpeckers occurred, three where only yellow-billed oxpeckers were present and four (six for
niche breadth, see below) where the species were sympatric.
Following Grobler and Charsley (1978), a host preference index (PI) was calculated for each
oxpecker–host combination according to the formula PI 5 (n oxpeckers/n hosts) × 1000. Neither
PI nor log-transformed PI values (ln[PI 1 1]) were normally distributed when non-hosts
(potential hosts that were never observed being used by oxpeckers) were included (Kolmogorov–
Smirnov tests for normality, all p , 0.001). This result was not unexpected given that the
number of non-hosts is potentially large. Excluding non-hosts, however, the log-transformed PI
values were normally distributed (Kolmogorov–Smirnov tests, two-tailed p . 0.8 for both
species). Consequently, the log-transformed PI values (henceforth ‘log-PI’) were averaged over
all appropriate studies for statistical analyses.
Estimates of the niche breadth were calculated from oxpecker occurrence data on different
species of hosts. Two additional studies recording oxpecker associations but not host numbers
were included along with the studies used to calculate the host preferences. Breadth was
calculated using the Shannon–Wiener index, B 5 2 ∑pia ln(pia), where pia is the proportion of
oxpeckers of species i associated with host species a and B is summed over the hosts. The niche
breadths of the two species were only compared within studies, thus circumventing the
shortcomings of this index (Colwell and Futuyma, 1971).
The characteristics of the hosts were measured or obtained from the literature in order to test
for correlates of the oxpecker preferences. Host mass data were taken from Skinner and Smithers
(1990) and Kingdon (1982) by averaging the mid-point of the size ranges given for males and
females; more exact values were not possible because no study has recorded oxpecker use by host
sex. The relative host area was estimated as (mass)0.67. The foraging mode and habitat distribution
for bovids were taken from the figure presented by Kingdon (1982, p. 21). Three dominant
foraging modes were recognized: folivore/frugivores, mixed feeders and grazers. The habitat
distribution was based on Kingdon’s (1982) categorization of the use of eight habitats by bovid
hosts according to their wetness or dryness; the wettest habitat (forest) was given a value of 1,
while the driest habitat (subdesert) was given a value of 8.
The body hair length of potential hosts was taken from Skinner and Smithers (1990). Based on
both preserved material and the illustrations in Dorst and Dandelot (1969), potential hosts were
divided according to whether or not they possessed manes, defined as areas of significantly longer
hair occurring along the nape or front of the neck or along the centre of the back or chest.
94
Koenig
In one study (Grobler and Charsley, 1978), estimates of the actual number of hosts present in
the population were available. In the other studies, the relative host abundance was estimated by
the total number of host individuals of each species sighted during censuses.
Two-tailed statistical tests were used whenever possible and p , 0.05 was considered
significant.
Results
Host preferences
The results of the host preference surveys at Lake Nakuru and in the Masai Mara are presented
in Table 1. Only red-billed oxpeckers were present at Lake Nakuru, while both red-billed and
yellow-billed oxpeckers were common in the Masai Mara. Six species of potential hosts were
present at both sites. The correlation between the PI values for red-billed oxpeckers at the two
sites was positive but not significant (rs 5 0.75, n 5 6, p , 0.10). With the larger sample of
all 12 potential hosts observed in the Masai Mara, the correlation between the PI values of the
two species of oxpeckers was highly significant (rs 5 0.71, n 5 12, p , 0.01).
In order to examine in greater detail the similarities and contrasts in host preferences by the
two species occurring in allopatry and sympatry, these results were combined with host
preference data from prior studies. The mean log-PI values for all potential hosts recorded for
both species of oxpeckers are summarized in Table 2 along with data on the physical
characteristics of the hosts.
The host preferences of the two species of oxpeckers are highly correlated whether or not nonhosts are included (Fig. 1); the slope of the regression line being , 1 indicates that on average
red-billed oxpeckers are more common than yellow-billed oxpeckers on any particular species of
host. The patterns of association between the host preferences and potential hosts are also
virtually identical. There is no association between the foraging mode used by the bovids and
either the mean PI index for either species (Kruskal–Wallis tests: red-billed, x22 5 0.7, n 5 17,
Table 1. Host preferences of red-billed (RBO) and yellow-billed (YBO) oxpeckers at Lake Nakuru National
Park (LN) and the Masai Mara Reserve (MM), Kenya
n hosts
Host
LN
Cape buffalo
Giraffe
Common waterbuck
Sitting
Standing
Warthog
Impala
Zebra
Blue wildebeest
Elephant
Thompson’s gazelle
Grant’s gazelle
Hartebeest
Topi
64
5
1261
228
954
531
295
–
–
–
52
–
–
–
n RBO
MM
25
58
6
–
–
31
726
3398
4674
18
277
5
29
355
LN
MM
70
4
72
53
26
24
7
–
–
–
0
–
–
–
11
11
0
–
–
1
11
25
5
0
0
0
0
0
n YBO
Preference index
MM
RBO(LN)
RBO(MM) YBO
1094
200
57
233
27
45
24
–
–
–
0
–
–
–
440
190
1
–
–
32
15
7
1
0
0
0
0
0
7
9
0
–
–
0
0
31
11
0
0
0
0
0
1 , associations observed during study but not during censuses. For scientific names of hosts, see Table 2.
280
155
0
–
–
0
1
9
2
0
0
0
0
0
Co-existence of oxpeckers
95
Table 2. Host preferences of red-billed (RBO) and yellow-billed (YBO) oxpeckers
Mean log-PI
Host
Body mass
(kg)
Hair length
(mm)
Mane
RBO
YBO
Eland Taurotragus oryx
Giraffe Giraffa camelopardalis
Roan Hippotragus equinus
Sable Hippotragus niger
Cape buffalo Syncerus caffer
Kudu Tragelaphus strepsiceros
Zebra Equus burchelli
Nyala Tragelaphus angasi
Impala Aepyceros melampus
White rhinoceros Ceratotherium simum
Blue wildebeest Connochaetes taurinus
Warthog Phacochoerus aethiopicus
Common waterbuck Kobus ellipsiprymnus
Bushbuck Tragelaphus scriptus
Duiker Sylvicapra grimmia
Steinbok Raphicerus campestris
Lechwe Kobus leche
Reedbuck Redunca arundinum
Oribi Ourebia ourebi
Hartebeest Alcelaphus buselaphus
Topi Damaliscus lunatus
Thompson’s gazelle Gazella thomsoni
Grant’s gazelle Gazella granti
Hippopotamus Hippopotamus amphibius
Elephant Loxodonta africana
570
1010
270
228
504
111
308
85
48
1875
215
68
210
43
20
11
96
45
14
136
133
21
55
1406
3900
14
10
35
40
50
20
9
34
50
–
60
29
41
24
15
30
62
18
25
27
9
NA
NA
–
–
Yes
Yes
Yes
Yes
No
Yes
Yes
Yes
No
No
Yes
Yes
Yes
Yes
No
No
No
No
No
No
No
No
No
No
No
6.62
5.61
5.30
4.95
4.72
4.48
3.37
2.88
2.58
2.23
2.16
1.15
0.81
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
5.90
5.11
5.20
2.25
4.86
2.69
3.29
–
0.85
5.58
2.67
1.65
0.00
–
0.00
0.00
0.00
0.00
–
0.00
0.00
0.00
0.00
0.00
0.00
Data from Grobler and Charsley (1978), Grobler (1980), Stutterheim (1980), Stutterheim and Panagis (1985), Hustler
(1987), Dale (1992), Mooring and Mundy (1996b), and this study; values are means from all relevant studies. Body mass
data from Skinner and Smithers (1990) and Kingdon (1982). NA, not available.
ns; yellow-billed, x22 5 0.2, n 5 15, ns) or whether the species is used as a host or not (x2
contingency tests: red-billed, x22 5 1.7, n 5 17, ns; yellow-billed, x22 5 1.0, n 5 15, ns).
There are also no significant correlations between the mean PI values and either hair length or
habitat (Table 3). However, correlations between the host preferences and both host mass (Table
3) and relative surface area (Fig. 2) are generally significant for both species.
A second factor significantly correlating with host preferences is whether or not a potential host
possesses a mane (Fig. 3). With the exceptions of the common waterbuck for yellow-billed
oxpeckers and bushbucks for both species, all potential hosts with manes are used by oxpeckers.
Conversely, no potential hosts without manes are used except for Cape buffaloes, impalas and
rhinoceroses. In ANCOVAs, using log-PI as the dependent variable, the presence or absence of
a mane as the main factor and the relative host area as a covariate, the presence of a mane is
highly significant (p , 0.01 for both species) after controlling for relative body surface area.
Together, these two variables explain 41% of the variance in mean host preference for red-billed
oxpeckers and 36% for yellow-billed oxpeckers. Eliminating the three very large, hairless species
of pachyderms (elephants, rhinoceroses and hippopotamuses) increases the proportion of variance
explained to 68% for red-billed oxpeckers and 73% for yellow-billed oxpeckers.
96
Koenig
Figure 1. Host preferences for red-billed versus yellow-billed oxpeckers. Spearman rank correlation for all
data, rs 5 0.92 (n 5 22 species of hosts, p , 0.001) and excluding non-hosts, rs 5 0.67 (n 5 12, p
, 0.02). The regression line (y 5 0.85x 1 0.13) is shown.
There was no correlation between the PI values of yellow-billed oxpeckers and the estimated
number of hosts present in the population for the one study for which these data were available
(rs 5 0.05, n 5 15, ns including all potential hosts; rs 5 2 0.44, n 5 10, ns excluding nonhosts). This fails to support the hypothesis that oxpeckers prefer commoner hosts. Additional
support for this conclusion comes from correlations between the PI values and relative host
abundance as measured by the total number of hosts observed within a particular study. Of the
15 total data sets available (eight for red-billed and seven for yellow-billed oxpeckers), eight yield
positive and seven negative correlations (binomial test, p . 0.5).
Although host abundance does not appear to correlate with the oxpecker preferences, data from
Lake Nakuru suggest that host behaviour may influence host selection by oxpeckers, at least in
some cases. Red-billed oxpeckers were over eight times more likely to be observed on common
waterbucks at this site if the hosts were sitting than if they were standing (Table 1), a highly
significant difference (contingency test using the number of waterbuck observed with one or more
oxpeckers in attendance; x21 5 53.9, p , 0.001).
Foraging behaviour
Results of three-way ANOVAs testing for behavioural differences observed during time–activity
budget watches according to species (red-billed or yellow-billed oxpecker), location (Lake
Table 3. Spearman rank correlations (n species of hosts) between the physical characteristics of potential
hosts and the mean PI values of red-billed (RBO) and yellow-billed (YBO) oxpeckers
All species
Host mass
Host hair length
Habitat
Excluding non-hosts
RBO
YBO
RBO
YBO
0.51 (25)**
0.02 (20)
0.04 (17)
0.54 (22)**
2 0.10 (17)
0.16 (15)
0.52 (13)
2 0.42 (12)
0.33 (8)
0.87 (11)***
2 0.42 (10)
0.60 (7)
Habitat data from Kingdon (1982); positive values indicate a preference for hosts living in drier habitats.
* p , 0.05, ** p , 0.01, *** p , 0.001 (two-tailed).
Co-existence of oxpeckers
97
Figure 2. The relationship between relative host surface area (mass0.67) and mean log-PI values for (a) redbilled oxpeckers (all data, rs 5 0.51, n 5 25, p , 0.01; excluding non-hosts, rs 5 0.52, n 5 13, p 5
0.07) and (b) yellow-billed oxpeckers (all data, rs 5 0.54, n 5 22, p , 0.01; excluding non-hosts, rs 5
0.87, n 5 11, p , 0.001). Values for elephants (E), white rhinoceroses (R) and hippopotamuses (H) are
labelled.
Figure 3. Mean (± SE) log-PI values for oxpeckers depending on whether hosts possess a mane or not. For
red-billed oxpeckers, n species 5 25 (14 no mane and 11 mane) and for yellow-billed oxpeckers, n species
5 22 (13 no mane and nine mane). The differences are significant for both species (Mann–Whitney Utests, both p , 0.01).
98
Koenig
Nakuru or Masai Mara) and host (buffalo, giraffe, impala, warthog, common waterbuck, blue
wildebeest or zebra) generally found significant differences between locations and among hosts,
but yielded no significant differences between the two species of oxpeckers in any aspect of their
time–activity budgets after controlling for these two variables.
ANOVAs testing for differences in where on hosts oxpeckers foraged revealed that red-billed
oxpeckers foraged more on the heads of hosts while yellow-billed oxpeckers foraged more on
their sides and undersides. However, even though these differences were statistically significant,
they were all small in absolute magnitude, with the mean percent time spent by the two species
on these three body parts differing by only 4–6%.
Niche breadth and competition
The niche breadth of the two oxpecker species based on host associations for each of six studies
carried out in areas of sympatry are presented in Table 4. In all six sites, the niche breadth of redbilled oxpeckers was greater than that for yellow-billed oxpeckers (binomial test, p , 0.04).
I tested for competition between the oxpecker species in two ways. First, I looked for
differences in the population sizes potentially attributable to the other species by comparing the
total abundance of both species of oxpecker, measured as the total number of birds seen divided
by the total number of potential hosts observed, in sympatric and allopatric sites. Abundance by
this measure was significantly greater for both species when allopatric (Mann–Whitney U-tests:
red-billed, n1 5 n2 5 4, z 5 2.02, p , 0.05; yellow-billed, n1 5 4, n2 5 3, z 5 2.12, p
, 0.05). I also compared the abundances of oxpeckers on a particular host species in areas
where the two species were sympatric compared to allopatric. A total of 20 such comparisons
could be made, 11 for red-billed and nine for yellow-billed oxpeckers. Abundance was less in
sympatry for 17 out of 20 (85%) comparisons (binomial test, p , 0.01), including eight out of
11 (73%) comparisons involving red-billed oxpeckers and all nine comparisons involving yellowbilled oxpeckers. Together, these two tests support the hypothesis that population sizes of both
species are depressed in sympatry, as expected if competition between them is considerable.
Given their ecological similarities and the apparent competition between the two species of
oxpeckers suggested by the above analyses, competitive displacement between them would be
expected. To test for this, I compared log-PI values of oxpeckers on hosts from studies where the
two species were allopatric with those from studies where they were sympatric. Competitive
displacement predicts two patterns. First, when the two species are correlated against each other,
there should be positive correlations between the log-PI values of one species and those of the
other when each is allopatric but not when they are sympatric. Second, when each species is
compared to itself, there should be only weak correlations between the log-PI values when the
species is allopatric compared to when it is sympatric with the other species.
Table 4. Niche breadth (Shannon–Wiener Index) of red-billed (RBO) and yellow-billed (YBO) oxpeckers
studied in areas of sympatry
RBO
YBO
Locality
Reference
2.11
1.62
1.46
1.72
1.57
1.48
2.08
0.21
1.02
1.43
0.67
1.19
Zambia
Botswana
Zimbabwe
Zimbabwe
Botswana
Kenya
Attwell (1966)
Buskirk (1975)
Hustler (1987) (Sinamatella)
Hustler (1987) (Robins)
Stutterheim and Panagis (1985)
This study
Co-existence of oxpeckers
99
Figure 4. The relationship between the mean log-PI values for red-billed versus yellow-billed oxpeckers
when (a) in allopatry (all data, rs 5 0.85, n 5 15, p , 0.001; excluding non-hosts, rs 5 0.65, n 5 11,
p , 0.05) and (b) in sympatry (all data, rs 5 0.80, n 5 18, p , 0.001; excluding non-hosts, rs 5 0.61,
n 5 11, p , 0.05). The value for white rhinoceroses (R) is labelled.
Neither of these predictions were supported (Figs 4 and 5). Correlations of the host preferences
between the two species were significant in both areas of sympatry and allopatry (Fig. 4) and the
correlations were significant between the log-PI values of both species when allopatric and when
Figure 5. The relationship between the mean log-PI values when sympatric with the other oxpecker species
versus when allopatric for (a) red-billed oxpeckers (all data, rs 5 0.82, n 5 11, p , 0.01; excluding nonhosts, rs 5 0.79, n 5 10, p , 0.05) and (b) yellow-billed oxpeckers (all data, rs 5 0.90, n 5 11, p ,
0.01; excluding non-hosts, rs 5 0.88, n 5 10, p , 0.01).
100
Koenig
sympatric with the other species (Fig. 5). These analyses suggest that the host preferences of
oxpeckers are not significantly affected by the presence of the other species.
Discussion
Host preferences
Oxpeckers of both species prefer larger hosts and, with few exceptions, are restricted to hosts
with manes. These two variables alone explain between one-third and three-quarters of the
variance in host preferences. Given that the mix of hosts present in a site can have an important
influence on oxpecker behaviour, as indicated by the changes in host use following the removal
of a particular host species (Dale, 1992), these proportions are extremely high. The host
preferences do not correlate with host diet, habitat preferences, body hair length or host
abundance.
Two host species stand out as being anomalous in terms of their use by oxpeckers relative to
that expected based on their size and mane morphology. White rhinoceroses are perplexing
because they, but neither elephants nor hippopotamuses, are common hosts, particularly for
yellow-billed oxpeckers. A second species whose use is anomalous are impalas, the only
maneless antelope used regularly as a host. Size offers no resolution, as impalas are the smallest
ungulate used by oxpeckers (Table 2). Hart et al. (1990) examined oxpecker use of impalas with
this anomaly in mind and suggested that impalas harbour a greater tick mass per unit body
surface area than other antelopes, possible due to their greater use of wooded areas. Although I
found no relationship between habitat use by antelopes and attendance by oxpeckers (Table 3),
the possibility that impalas are used as hosts because of an unusually high incidence of tick
infestation remains untested.
At least three overlapping causes appear to be important in determining these preferences. Most
critical is the density and availability of ticks. Assuming that their larger surface area allows for
a greater total number and possibly increased density of ticks (Olubayo et al., 1993), this factor
could explain the preference for larger species of hosts. It could also explain preferences for hosts
with manes if manes tend to be infested with high densities of easily-removed ectoparasites. I
know of no data addressing this hypothesis, although observations confirm that oxpeckers spend
much of their foraging time on body parts, such as manes, that hosts are unable to groom selforally (Mooring and Mundy, 1996a).
The second factor that may be important in determining oxpecker host preferences is the ability
to detect and hide from predators. When alarmed, oxpeckers line up along an animal’s back and
produce a distinct hissing call (Mackworth-Praed and Grant, 1960). The preference of oxpeckers
for ungulates with manes could reflect in part a greater ability to effectively hide behind these
structures, which are generally located in the same area that these birds congregate when alarmed.
Predation could even explain their preference for larger hosts to the extent that avian predators
might be less likely to disturb or attempt to catch them when on larger, less vulnerable hosts.
Finally, there are several lines of evidence to suggest that host behaviour plays a role in
determining preferences. Red-billed oxpeckers at Lake Nakuru were over eight times more likely
to be observed on sitting compared to standing waterbuck (Table 1). The grooming behaviour
varies significantly between and even within species of African ungulates (Hart et al., 1992) and
may influence the density of ticks and thus oxpecker preferences. Differences in host tolerance
independent of tick density per se may also influence oxpecker preferences (Attwell, 1966;
Watkins and Cassidy, 1987; Mooring and Mundy, 1996b). However, hosts generally appear to
ignore oxpeckers attending them; only occasionally are behaviours observed that can be
Co-existence of oxpeckers
101
interpreted as either discouraging or facilitating oxpeckers (for a possible example of the latter,
see Breitwisch (1992)).
Interspecific differences and similarities
Yellow-billed oxpeckers have bills that are broader and heavier compared to the more scissor-like
bills of red-billed oxpeckers (Attwell, 1966). Yellow-billed oxpeckers are also slightly larger and
behaviourally dominant (Stutterheim et al., 1988), although interspecific interactions are not
frequent in the wild. These morphological differences are correlated with quantitative differences
in foraging behaviour, with red-billed oxpeckers ‘scissoring’ (sweeping their head along a host’s
body while rapidly opening and closing their bill) more frequently than yellow-billed oxpeckers
(Neweklowsky, 1974; Stutterheim et al., 1988). However, these morphological and behavioural
differences are not known to correlate with any significant difference in food preferences
(Stutterheim et al., 1988).
The results presented here support the conclusion that ecological differences between the
species are minimal. Red-billed oxpeckers are generally more common on a particular species of
host, use a wider diversity of hosts and, thus, have a greater niche breadth than yellow-billed
oxpeckers (Table 4), as previously suggested by Stutterheim and Panagis (1985) and Stutterheim
et al. (1988). Otherwise, the host preferences and behaviour of the two species while foraging on
hosts are remarkably similar and I found no evidence of competitive displacement (Figs 4 and 5)
despite evidence that each species depresses the population size of the other. Other key aspects
of their biology are similar as well: both are cooperative breeders, both are secondary hole nesters
that breed in tree cavities and both breed during the rainy season (Stutterheim et al., 1976;
Stutterheim, 1982). As surmised as early as Attwell (1966), oxpeckers appear to be an example
of two co-existing species making the same demands on their habitat.
Geographical ecology and co-existence of oxpeckers
The similarity of these two species raises two basic questions about their geographical ecology.
First, how do they persist in sympatry over such a wide area of East and South Africa and yet
exhibit no evidence of competitive displacement? Second, what explains the much larger
distribution of yellow-billed oxpeckers whose range, unlike red-billed oxpeckers, extends far into
West Africa?
One complication is that recent faunal changes may have obscured otherwise important
differences between these species. Most obviously, the eradication of game throughout much of
Africa has resulted in widespread declines in oxpecker populations that may have altered
ecological interactions between them. Population changes in particular host species may also be
important. For example, the white rhinoceros, a species which has been recently driven nearly to
extinction in much of Africa, is a preferred host of yellow-billed oxpeckers but only occasionally
used by red-billed oxpeckers (Table 2), a difference particularly evident when the two species are
sympatric (Fig. 4). Assuming this difference held when rhinoceroses were common, foraging
differences between the oxpeckers may have once been considerably more pronounced than they
are today. Although it is not possible to reject this hypothesis entirely, local co-existence between
the two oxpecker species is not new: numerous cases of both species feeding together extending
back as far as 1951 are reported by Attwell (1966). This suggests that the ecological similarity
and local co-existence of oxpeckers is neither a recent nor a temporary phenomenon.
Traditional competition theory predicts that ecologically similar species should co-exist
precariously at best (Gause, 1971; MacArthur, 1972). More recently, metapopulation models (e.g.
Hanski and Gyllenberg, 1993) have been developed to account for the regional co-existence of
species in patchy environments (reviewed by McLaughlin and Roughgarden (1993)). Such models
102
Koenig
are particularly appropriate here given that oxpeckers are primarily dependent on large ungulate
herds concentrated in relatively small reserves scattered throughout their range.
Although there are insufficient data on both the frequency of extinctions or recolonizations of
oxpeckers within patches and patch-occupancy frequencies of either species to test such models
directly, indirect evidence is consistent with metapopulation dynamics playing an important role
in the geographical ecology of oxpeckers. For example, Slatkin’s (1974) model (extended by
Hanski (1983)) of two species competing in an environment consisting of many identical patches
predicts that the abundance of each species should be reduced in areas of sympatry compared to
allopatry, as found here.
These models also suggest, in contrast to traditional competition models, that there need not be
a clear priority effect and that one species may be able to invade a region occupied by the other
regardless of the effects each has on the other’s colonization and extinction rates. There is
evidence from both reintroductions and natural reinvasions consistent with the lack of a priority
effect in oxpeckers. For example, red-billed oxpeckers translocated to an area in Zimbabwe
already occupied by yellow-billed oxpeckers have persisted (P.J. Mundy, personal communication). Particularly relevant are observations on the recent reinvasion by yellow-billed oxpeckers
into Kruger National Park, where they had formerly become extinct (Whyte et al., 1987). Despite
red-billed oxpeckers being present in large numbers throughout the area, yellow-billed oxpeckers
penetrated 130 km into the park within 10–12 years of colonization and were found on 63% of
buffalo herds recorded within this range. This example also illustrates both extinction and
recolonization events by oxpeckers within habitat patches, as expected by species whose
distributions are influenced by metapopulation dynamics.
Conclusion
The remarkable ecological similarity of oxpeckers combined with the apparent lack of
competitive exclusion or competitive displacement in areas of sympatry demonstrate that
traditional single-community competition theory is insufficient to explain their distributional
ecology. Instead, the geographical ecology of these two species is consistent with the hypothesis
that metapopulation structure facilitates their regional co-existence. What remains unexplained by
current metapopulation models is the extensive degree of their local co-existence (Hanski and
Ranta, 1983; McLaughlin and Roughgarden, 1993) and the extensive allopatric range of yellowbilled oxpeckers in West Africa, where to date no studies have been conducted. Also needed are
data on the changes in the species of oxpeckers present within localities in order to determine the
time scale over which co-existence persists; populations becoming locally extinct and recolonizing over relatively short time scales would provide important support for the hypothesis that
metapopulation dynamics explain their co-existence. Although numerous questions remain,
oxpeckers offer a unique challenge to current ideas concering the evolutionary ecology of coexisting species.
Acknowledgements
I thank P.J. Mundy for information regarding oxpecker translocations in Zimbabwe, M. Mooring
for preprints of his work on oxpeckers, Randy Breitwisch, Nils Chr. Stenseth and the reviewers
for comments on the manuscript and the Florida State Museum of Natural History, the University
of Montana Zoological Museum and the California Academy of Sciences for access to specimens
under their care. Janis Dickinson, Kay Holekamp, Laura Smale and Oscar Wambuguh assisted
my work in the Mara in various ways. Field work for this study was supported by a grant from
the American Philosophical Society.
Co-existence of oxpeckers
103
References
Attwell, R.I.G. (1966) Oxpeckers, and their associations with mammals in Zambia. Puku 4, 17–48.
Bezuidenhout, J.D. and Stutterheim, C.J. (1980) A critical evaluation of the role played by the red-billed
oxpecker Buphagus erythrorhynchus in the biological control of ticks. Onderstepoort J. Vet. Res. 47,
51–75.
Breitwisch, R. (1992) Tickling for ticks. Nat. Hist. March, 56–63.
Buskirk, W.H. (1975) Substrate choices of oxpeckers. Auk 92, 604–6.
Colwell, R.L. and Futuyma, D.J. (1971) On the measurement of niche breadth and overlap. Ecology 52,
567–76.
Dale, J. (1992) The effect of the removal of buffalo Syncerus caffer (Sparman 1779) on the host selection
of yellow-billed oxpeckers Buphagus africanus Linnaeus 1766 in Zimbabwe. Trop. Ecol. 5, 19–23.
Dean, W.F.J. and MacDonald, I.A.W. (1981) A review of African birds feeding in association with
mammals. Ostrich 52, 135–55.
Dorst, J. and Dandelot, P. (1969) A Field Guide to the Larger Mammals of Africa. Houghton Mifflin,
Boston, MA.
Gause, G.F. (1971) The Struggle for Existence. Dover, New York.
Grobler, J.H. (1980) Host selection and species preference of the red-billed oxpecker Buphagus
erythrorhynchus in the Kruger National Park. Koedoe 23, 89–97.
Grobler, J.H. and Charsley, G.W. (1978) Host preference of the yellow-billed oxpecker Buphagus africanus
in the Rhodes Matopos National Park, Rhodesia. S. Afr. J. Wildl. Res. 8, 169–70.
Hanski, I. (1983) Coexistence of competitors in a patchy environment. Ecology 64, 493-500.
Hanski, I. and Gyllenberg, M. (1993) Two general metapopulation models and the core-satellite species
hypothesis. Am. Nat. 142, 17–41.
Hanski, I. and Ranta, E. (1983) Coexistence in a patchy environment: three species of Daphnia in rock
pools. J. Animal Ecol. 52, 263–79.
Hart, B.L., Hart, L.A. and Mooring, M.S. (1990) Differential foraging of oxpeckers on impala in
comparison with sympatric antelope species. Afr. J. Ecol. 28, 240–9.
Hart, B.L., Hart, L.A., Mooring, M.S. and Olubayo, R. (1992) Biological basis of grooming behaviour in
antelope: the body-size, vigilance and habitat principles. Animal Behav. 44, 615–31.
Hustler, K. (1987) Host preference of oxpeckers in the Hwange National Park, Zimbabwe. Afr. J. Ecol. 25,
241–5.
Kingdon, J. (1982) East African Mammals, Vol. IIIc. Academic Press, New York.
MacArthur, R.H. (1972) Geographical Ecology. Harper & Row, New York.
Mackworth-Praed, C.W. and Grant, C.H.B. (1960) Birds of Eastern and North Eastern Africa, Vol. II (2nd
edn). Longman, London.
McLaughlin, J.F. and Roughgarden, J. (1993) Species interactions in space. In Species Diversity in
Ecological Communities (R.E. Ricklefs and D. Schluter, eds), pp. 89–98. University of Chicago Press,
Chicago, IL.
Mooring, M.S. and Mundy, P.J. (1996a) Interactions between impala and oxpeckers at Matobo National
Park, Zimbabwe. Afr. J. Ecol. 34, 54–65.
Mooring, M.S. and Mundy, P.J. (1996b) Factors influencing host selection by yellow-billed oxpeckers at
Matobo National Park, Zimbabwe. Afr. J. Ecol. 34, 177–88.
Neweklowsky, W. (1974) Beobachtungen an Rotschnabelmadenhackern, Buphagus erythrorhynchus (Stanley). Zool. Garten N.F. 44, 121–43.
Olubayo, R., Jonyo, J., Orinda, G., Groothenhuis, J.G. and Hart, B.L. (1993) Comparative differences in
density of adult ticks as a function of body size in some East African antelope. Afr. J. Ecol. 31,
26–34.
Skinner, J.D. and Smithers, H.N. (1990) The Mammals of the Southern African Subregion. University of
Pretoria, Pretoria.
Slatkin, M. (1974) Competition and regional coexistence. Ecology 55, 128–34.
104
Koenig
Stutterheim, C.J. (1980) Symbiont selection of redbilled oxpecker in the Hluhluwe-Umfolozi game reserve
complex. Lammergeyer 30, 21–5.
Stutterheim, C.J. (1982) Breeding biology of the redbilled oxpecker in the Kruger National Park. Ostrich
53, 79–90.
Stutterheim, I.M. and Panagis, K. (1985) Roosting behaviour and host selection of oxpeckers (Aves:
Buphaginae) in Moremi Wildlife Reserve, Botswana, and eastern Caprivi, South West Africa. S. Afr. J.
Zool. 20, 237–40.
Stutterheim, C.J., Mundy, P.J. and Cook, A.W. (1976) Comparisons between the two species of oxpecker.
Bokmakierie 28, 12–14.
Stutterheim, I.M., Bezuidenhout, J.D. and Elliott, E.G.R. (1988) Comparative feeding behaviour and food
preferences of oxpeckers (Buphagus erythrorhynchus and B. africanus) in captivity. Onderstepoort J.
Vet. Res. 55, 173–9.
Van Someren, V.D. (1951) The red-billed oxpecker and its relation to stock in Kenya. E. Afr. Agricult. J.
17, 1–11.
Watkins, B.P. and Cassidy, R.J. (1987) Evasive action taken by waterbuck to redbilled oxpeckers. Ostrich
58, 90.
Whyte, I.J., Hall-Martin, A.J., Kloppers, J.J. and Otto, J.P.A. de T. (1987) The status and distribution of the
yellowbilled oxpecker in the Kruger National Park. Ostrich 58, 88–90.