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In order to better understand the symbiotic relationship of the oxpecker-mammal association and the role that oxpeckers play in controlling their hosts' tick burdens, interactions between yellow-billed oxpeckers (Buphagus africanus) and impala (Aepyceros melampus) were investigated at Matobo National Park, Zimbabwe during the wet and dry seasons. Oxpeckers devoted 30-35% of attendance time to foraging upon impala hosts. The ears were preferred for foraging above all other body regions, and foraging sessions directed to the ears were longer than sessions on other areas, apparently due to high tick infestation on host ears. Two-thirds of adult ticks (mostly the blue tick Boophilus decoloratus) collected from impala females were from the ears, and heavy infestations of immature ticks on the ears were common. The majority of oxpecker foraging (71-74%) was directed to the ear, head, and neck area where impala are unable to self-oral groom. Most adult ticks (75-77%) were found on the ears, head, and neck of sampled impala, indicating that oxpeckers foraged so as to maximize adult tick intake. Adult tick abundance in the vegetation, and presumably on impala, was much greater in the wet season than in the dry season. Oxpeckers spent significantly less time foraging upon impala in the wet season compared with the dry season, reflecting the presumed greater abundance of adult ticks on hosts during this time. Impala hosts tolerated oxpeckers 86% of the time, and 42% of oxpecker-tolerant impala accommodated foraging activity by lowering an ear, inclining the head, or standing still. An interaction was apparent between the tick-removal strategies of oxpeckers and their impala hosts in that impala reduced their grooming rate when oxpeckers foraged upon them to 11-36% of their grooming rate in the absence of oxpeckers, thereby reducing the cost of tick control.
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Afr.
J.
Ecol.
1996,
Volume
34,
pages
54-65
Interactions between impala and oxpeckers at Matobo
National Park, Zimbabwe
MICHAEL
S.
MOORING and PETER
J.
MUNDY
Department
of
Anatomy, Physiology and Cell Biology, School
of
Veterinary Medicine,
University
of
California. Davis, California
95616,
U.
S.
A. and Ornithology Research Unit,
Department
of
National Parks and Wild Life Management, PO
Box
2283,
Buluwayo,
Zimbabwe
Summary
In order to better understand the symbiotic relationship of the oxpecker-mammal
association and the role that oxpeckers play in controlling their hosts’ tick
burdens, interactions between yellow-billed oxpeckers
(Buphugus ufricanus)
and impala
(Aepyceros melumpus)
were investigated at Matobo National Park,
Zimbabwe during the wet and dry seasons. Oxpeckers devoted 30-35% of attend-
ance time to foraging upon impala hosts. The ears were preferred for foraging
above all other body regions, and foraging sessions directed to the ears were
longer than sessions on other areas, apparently due to high tick infestation on host
ears. Two-thirds of adult ticks (mostly the blue tick
Boophilus decolorutus)
collected from impala females were from the ears, and heavy infestations of
immature ticks on the ears were common. The majority of oxpecker foraging
(71-74%) was directed to the ear, head, and neck area where impala are unable to
self-oral groom. Most adult ticks (75-77%) were found on the ears, head, and neck
of sampled impala, indicating that oxpeckers foraged
so
as to maximize adult tick
intake. Adult tick abundance in the vegetation, and presumably on impala, was
much greater in the wet season than in the dry season. Oxpeckers spent signifi-
cantly less time foraging upon impala in the wet season compared with the dry
season, reflecting the presumed greater abundance of adult ticks on hosts during
this time. Impala hosts tolerated oxpeckers 86% of the time, and 42% of oxpecker-
tolerant impala accommodated foraging activity by lowering an ear, inclining the
head, or standing still. An interaction was apparent between the tick-removal
strategies of oxpeckers and their impala hosts in that impala reduced their
grooming rate when oxpeckers foraged upon them to 11-36% of their grooming
rate in the absence of oxpeckers, thereby reducing the cost of tick control.
Key
words:
foraging, grooming, impala, oxpeckers, symbiosis, ticks
RhUllC
Pour mieux comprendre la relation symbiotique de l’association pique-boeufs-
mammifkres et le rdle que jouent les pique-boeufs dans le contr6le des tiques de
leurs hdtes, on a analyse les interactions entre les pique-boeufs
a
bec jaune
Correspondence:
Michael
S.
Mooring,
Department of Biological
Sciences,
University
of
Alberta,
0
1996
East African
Wild
Life Society.
Edmonton, Alberta
T6G
2EI, Canada.
Interactions between impala and oxpeckers
55
(Buphagus ufricanus)
et les impalas
(Aepyceros melampus)
au Parc National de
Matobo, au Zimbabwe, en saison sbche et en saison des pluies. Les pique-boeufs
consacraient de
30
a
35%
de leur temps d’attention
a
se nourrir sur des impalas.
11s preferaient les oreilles a toute autre partie du corps et le temps consacre
a
se
nourrir sur les oreilles Ctait plus long que sur toute autre partie du corps, ceci
&ant dti semble-t-il
a
un plus haut degrC d’infestation des oreilles des hates par
les tiques. Les deux tiers des tiques adultes (surtout la tique bleue
Boophilus
decoloratus)
recoltkes sur les impalas femelles provenaient des oreilles, et de
fortes infestations des oreilles par des tiques immatures sont communes. La plus
grande part des recherches de pique-boeufs (71
a
74%) se faisait au niveau des
oreilles, de la t&te et du cou, la
ou
les impalas sont incapables de se toiletter
eux-mbmes. On trouvait la plupart des tiques adultes (75 a 77%) sur les oreilles,
la t&te et le cou des animaux analyses, ce qui indique que les pique-boeufs se
nourrissaient a ces endroits pour maximaliser la prise de tiques adultes.
L’abondance de tiques adultes dans la vegetation, et probablement sur les
impalas, etait bien plus grande pendant la saison des pluies que pendant
la
saison
sbche. Les pique-boeufs passaient significativement moins de temps a se nourrir
sur les impalas en saison des pluies qu’en saison seche, ce qui refletait
l’abondance probablement plus grande de tiques adultes sur leurs hdtes pendant
cette saison. Les impalas hdtes toleraient
la
prCsence des pique-boeufs 86% du
temps, et 42% des impalas consentants facilitaient l’activite de nourrissage en
abaissant l’oreille, en baissant la tete ou en restant tranquilles. I1 semblait donc
exister une interaction entre les strategies des pique-boeufs pour enlever les tiques
et les impalas hates, en ceci que les impalas rkduisaient leur temps de toilettage
jusqu’
a
64
a
89% de ce qu’il aurait CtC en l’absence de pique-boeufs, ce qui rCduit
d’autant le coat du contrdle des tiques.
Introduction
The association between oxpeckers
(Buphagus
spp.) and their mammalian hosts
in Africa is well known, and recent evidence indicates that this relationship
may be among the best examples of symbiosis between terrestrial vertebrates
(Breitwisch, 1992). Current evidence points to fitness benefits from the associ-
ation for both oxpecker and host. By removing ticks, oxpeckers gain the major
food item in their diet (Attwell, 1966; Bezuidenhout
&
Stutterheim, 1980), and
hosts are helped in controlling tick infestations that may lead to mortality or
morbidity (Lightfoot
&
Norval, 1981; Norval
et al.,
1988; Hart, 1990). One
would therefore expect to see oxpeckers foraging
so
as to optimize tick intake,
and hosts tolerating or accommodating oxpecker foraging when threatened by
ticks. Previous studies have tended to examine oxpecker biology and host
selection in isolation from the host animal and have not taken into consideration
the interaction that takes place in a symbiotic relationship.
A prime factor influencing oxpecker foraging behaviour would be tick
abundance, which varies seasonally and affects the tick burdens on host animals
(Mulilo, 1985; Kaiser, Sutherst
&
Bourne, 1991). For example, oxpeckers should
be able to forage more quickly and efficiently during the wet season, when
environmental tick challenge and host tick loads are typically greatest (Mooring,
Mazhowu
&
Scott, 1994), than during the dry season, when they may have to
spend more time foraging for sparsely distributed ticks on hosts. Host factors
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East African
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J.
Ecol.,
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M.
S.
Mooring and
P.
J.
Mundy
such as habitat preference, body mass, group size, and hair length may interact
to make a host more or less attractive to oxpeckers by influencing host tick
burden and oxpecker foraging efficiency. Host response to oxpeckers would also
play a role in host selection. There are two ways that a potential host can
respond to an oxpecker that attempts to land and forage: it can reject the
oxpecker, for example by swinging the head or jumping, or it can tolerate its
presence. Toleration can be expressed either by the host acting indifferently, or
by the host accommodating the bird’s foraging efforts by making certain body
regions accessible (such as by lifting the tail or lowering the ears) or by standing
still during foraging sessions. Typical host response probably plays an important
role in which host species oxpeckers learn to prefer or avoid.
In controlled experiments with cattle, oxpeckers removed 95.7-99.9%
of
adult
ticks and 21-90%
of
larvae and nymphs (Bezuidenhout
&
Stutterheim, 1980).
While oxpeckers are presumably as effective in removing ticks from wild hosts, it
must be remembered that some wild hosts have their own behavioural strategies
for controlling ticks. Impala
(Aepyceros melampus
Licht.) exhibit well-developed
self-grooming behaviour (Hart
et
al.,
1992) as well as a unique form of reciprocal
allogrooming (Hart
&
Hart, 1992; Mooring
&
Hart, 1992a, 1993) that appears to
function primarily to remove ticks before they can attach and engorge. In
Zimbabwe, tick challenge was the primary determinant of impala grooming rate
(Mooring, 1995), and territorial males that engaged in reduced grooming during
the breeding season harboured more ticks than females (Mooring
&
Hart, 1995).
Impala are unusual in being the smallest antelope regularly attended by
oxpeckers, suggesting that impala may harbour more ticks than comparably-
sized antelope that are not attended (Hart, Hart
&
Mooring, 1990). Grooming,
as well as toleration or accommodation of oxpeckers, may be behavioural
strategies used by impala to cope with increased exposure to ticks in their brushy
ecotone habitat. If both impala grooming and oxpecker foraging function to
remove ticks, one might expect an interaction effect whereby impala with
access to oxpeckers reduce their grooming in order to reduce the cost of tick
control.
Investigation into these questions is important not only for better under-
standing of the biology
of
the oxpecker-mammal symbiosis, but also for
improved conservation and management of wildlife populations. Serious tick
problems exist in many national parks and game farms in Africa where limited
area, overstocking, and historical events have allowed excessive buildup of tick
populations (Norval
&
Lightfoot, 1982). One promising management approach
for the control of ticks is the introduction of oxpeckers to problem areas in order
to naturally regulate tick burdens on wild hosts (Mundy, 1983; White, 1990;
Cole, 1992). Little field research has attempted to assess the effectiveness of
oxpeckers in controlling ticks on wild animals, and information of this sort can
contribute to the successful use of oxpeckers as management tools.
The purpose of this study was to investigate the effect of tick challenge upon
the foraging behaviour of oxpeckers, and the response
of
impala
to
oxpecker
foraging. The study involved observations of oxpecker foraging, impala groom-
ing, and typical impala response to oxpeckers during two seasons of the year in
which tick challenge differed. In order to assess tick challenge, both vegetational
sampling and sampling of impala tick loads were undertaken.
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Wild
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Interactions between impala and oxpeckers
57
Materials and methods
Study site
The study was conducted within the Whovi Wilderness Area (game park) of
Matobo National Park (20"30'S, 28'30'E). Matobo has been the site of several
previous studies of oxpecker biology and host preference (Dale, 1992a, b;
Grobler, 1976, 1979; Grobler
&
Charsley, 1978;
P.
J. Mundy, unpubl. data).
Field work was carried out from 20 October to 26 November 1992, and from
3
March to
10
April 1993, periods that corresponded to the late hot-dry (dry)
season and late warm-wet (wet) season, respectively. Yellow-billed oxpeckers
(B.
africanus
L.) at Matobo were descended from 47 birds re-introduced to the
game park in 1975 (Grobler, 1976). The population flourished and in 1990 were
estimated to number around
200
birds (Dale, 1992a). A small population of
red-billed oxpeckers
(B.
erythrorhynchus
Stanley) also exists at Matobo, repre-
senting
14Y0
of the total oxpecker population (unpubl. data). Observations were
focused primarily upon the yellow-billed oxpecker.
Vegetational tick sampling
Vegetational sampling for ticks was performed by drag and removal plot
sampling. Drag sampling captured receptive ticks of all life stages, adults and
immatures, while removal plots captured adult ticks only, both receptive and
quiescent. All sampling was done in the vicinity of Mpopoma Dam in areas
frequented by impala. Four drag sites were sampled per week, two each
in
grassland and open woodland, with two
50
m replicates dragged per site. Four
10 m
x
10
m removal plots were sampled, two per week, in grassland and open
woodland habitats. Ticks were stored in 70% alcohol and later counted and
identified at the Tick Research Unit, Veterinary Research Laboratory, Harare.
Further details
of
the sampling methods are given in Mooring (1995) and
Mooring
et al.
(1994).
Sampling impala tick burden
Taking advantage of a population reduction exercise performed by the Depart-
ment of National Parks in November 1992, it was possible to sample
8
female
and
11
male adult impala. Estimates of relative tick burden were obtained by
using a patch sampling method whereby all adult ticks were removed from the
ears, face, neck, and foreleg on one side of the midline, and the perianal region,
according to the method described by Mooring
&
Hart (1995). All ticks were
later identified by the Tick Research Unit, Veterinary Research Laboratory,
Harare.
Observations
of
oxpeckers and impala
Observations were focused primarily upon the yellow-billed oxpecker, with the
red-billed variety only rarely observed. Behavioural observations
of
oxpeckers in
the presence of impala were conducted at Mpopoma Dam using a 15-60 x
telescope and recording into a portable computer. Focal oxpecker observations
and scan sampling methods (Altmann, 1974) were employed to record foraging
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J.
Ecol.,
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58
M.
S.
Mooring and
P.
J.
Mundy
and other attending behaviours. A total of
99
focal sessions comprising 28.4 h of
observations were completed.
Oxpecker ‘attendance’ of an impala host referred to the total time that
oxpeckers spent upon a particular animal. Attending oxpeckers could engage in
a variety of behaviours, the most typical ones being perching and foraging by
means of the scissoring or plucking techniques (see Bezuidenhout
&
Stutterheim,
1980,
for a full description of behaviours). Foraging technique, host body region
foraging was directed to, the amount of time spent actively foraging on different
body areas, and total attendance time were recorded during continuous obser-
vations, and activity budgets were calculated by scan sampling at 2-min intervals.
Also recorded was the age class (adult or immature) and flock size of oxpeckers,
and the impala herd size. Oxpecker ages were determined by bill colour
according to Stutterheim, Mundy
&
Cook (1976).
When oxpeckers alighted upon an impala and attempted to forage, the
response of the host (rejection, toleration, accommodation) was recorded. The
proportion of impala that rejected oxpeckers’ attempts to land and forage was
recorded by counting overt responses by the host (swinging or shaking of the
head, jumping, running away) as rejections; all cases of attendance of less than
10
s
duration were omitted. An accommodation response was recorded when the
impala lowered an ear, inclined its head, or stood still in response to oxpecker
foraging. If the host initially tolerated the bird and allowed it to forage, and later
rejected it, the host response was classified as toleration.
Host grooming behaviour was recorded when oxpeckers were attending
impala. Impala oral groom by combing the pelage with their incisor-canine teeth
and scratch groom with the hoof of the hindleg. Self-oral grooming is directed to
all parts of the body except the head and neck, while allogrooming and
scratching are directed to the head and neck area which the animal cannot reach
by self-oral grooming. Each oral combing or scratching movement was recorded
as an ‘episode’, with a connected series of episodes constituting a ‘bout’. Data on
the grooming behaviour of female impala when oxpeckers were absent was
collected as part
of
another study conducted at the same site and during the same
time frame, using the methods of this study; these data are cited from Mooring
(1995).
Results
Vegetational tick sampling
To
estimate tick density in the vegetation, 64 drag replicates and 16 removal
plots were sampled in the dry and wet seasons in grassland and woodland
habitat. No adult ticks were recovered from vegetational sampling during the dry
season, while in the wet season an average
of
1.0 adult tick per
50
m
drag and 24
adult ticks per removal plot were collected (Mann-Whitney; drags: 2~3.6,
PcO-0003; removal plots: 2=3.2,
P<O.OOl).
Of the adult ticks collected by drag
samples, 90% were the brown ear-tick
Rhipicephalus appendiculatus
Neumann
and 6% were the red-legged tick
R.
evertsi
Neumann, while 72%
of
larvae were
the blue tick
Boophilus decoloratus
(Koch). Removal plot sampling of adult ticks
collected 97%
R. appendiculatus
and 3%
R. evertsi.
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African
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Interactions between impala and oxpeckers
59
Impala tick burden
The adult ticks collected from the nineteen culled adult impala
(8
females,
11
males) that were patch-sampled for relative tick burden were
B.
decoloratus,
79%;
R.
evertsi,
14%; and
R.
appendiculatus,
6%. Of a total of 205 ticks removed
from female impala, 67.3% were on the ears. The remainder of the ticks collected
were distributed throughout the body (face, 5.9%; neck, 3.4%; foreleg, 16.1%;
tail, 7.3%). There was no difference in the number
of
ticks removed from males,
and the proportion
of
ticks infesting the combined ear, face, and neck area was
very similar (females, 77%; males, 75%). Although immature ticks were not
collected, it was noted that 9 of the 19 adults sampled (47%) had heavy to very
heavy infestations of larval and nymphal ticks in the ears.
Observations
of
oxpeckers
Mean
(
f
SE)
oxpecker flock size per impala herd was 2.3
(
f
0.2) in the dry
season and
3.4
(
f
0.3)
in the wet season, ranging between
1
and
9
oxpeckers. The
average number of oxpeckers attending a single impala was 1.5
(
f
0.1) in both
seasons, although as many as 6 oxpeckers were observed upon one impala at a
time. The longest time
of
continual attendance on the same host was 26 min (dry
season) and 20 min (wet season). The number of oxpeckers attending an impala
herd was positively correlated with the size of the herd (Spearman:
r,=0*88,
Z=2.3, PC0.02). Oxpecker flock size did not increase in the same proportion as
the increase in impala herd size, however, as reflected in fewer oxpeckers per host
animal in larger herds.
The foraging behaviour of oxpeckers typically seen on impala is depicted in
Fig. 1, as well as a typical accommodation response of impala. The percentage of
attempts by oxpeckers to land and forage upon impala that were tolerated (not
rejected) by the host was
84%
in the dry season and 89% in the wet season (not
significantly different), or a mean of 86%. For those impala that tolerated
oxpecker foraging activities, the percentage that accommodated oxpeckers by
lowering an ear, inclining the head, or standing still to facilitate foraging efforts
was 55%
(N=
161) in the dry season and 20%
(N=
103) in the wet season, or a
mean of 42%. From the scan samples, the percentage of attendance time that
oxpeckers devoted to foraging was 31% (N=609) in the dry season and 29%
(N=278) in the wet season (not statistically different), which was a mean of 30%.
Based on continuous time sampling of oxpeckers upon hosts, the percentage of
attendance time devoted to foraging was
38%
in the dry season and 33% in the
wet season, or a mean of 35%. The percentage of time on a host that oxpeckers
devoted to perching from scan samples was 49% and 55% for the dry and wet
seasons, respectively, and did not differ between seasons.
The body areas
of
impala that were foraged upon by oxpeckers in the two
seasons are displayed in order of decreasing preference in Fig. 2. The ears were
the single most preferred foraging site, being utilized for up to 50% of foraging
time. In addition, during the dry season oxpeckers spent more time per foraging
session on the ears compared with all other areas (mean
f
SE:
ears=35
f
2
s,
all
other areas= 19
f
1
s),
which was highly significant (Wilcoxon: 2=6.3,
P<O*OOOl). In the wet season, oxpecker sessions on the ears were also signifi-
cantly longer (Z=2*0,
PcO.05).
The head (excluding the ears) was the next most
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Ecol.,
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M.
S.
Mooring
and
P.
J.
Mundy
Fig.
1.
Typical accommodation
behaviour is demonstrated by a
female impala lowering its ear in
order
to
facilitate foraging by a
red-billed oxpecker. Drawn by
Emma Mooring from a
photograph.
preferred body site after the ears, followed by the neck area. Oxpeckers
concentrated their foraging efforts on the ears, head, and neck, accounting for
71%
of oxpecker foraging in the dry season and
74”/0
in the wet season.
The time that oxpeckers spent foraging per host was
72%
longer in the dry
season than in the wet season, with oxpeckers devoting
a
mean
(
&
SE)
of
1.65
(
f
0.13)
min foraging per host in the dry season compared with
0.96
(
f
0-1 1)
min during the wet season (Mann-Whitney:
Z=3.6, P<0.0004).
Because the
percentage of attendance time spent foraging did not change between seasons
(mean=
3O-35%;
see above), the time that oxpeckers spent attending impala was
also greater in the dry season than in the wet season,
4.4
(
f
0.3)
min per host
compared with
2.9
(
f
0.3)
min
(Z=3.4,
P<0.0007).
Impala significantly decreased their rate of self grooming during the time
when oxpeckers were in attendance on them. Table
1
compares grooming by
impala when oxpeckers were in attendance with grooming by impala in the
absence of attending oxpeckers. In the dry season, grooming rates when
oxpeckers were attending were
64790/0
lower than when oxpeckers were absent;
in the wet season, grooming rates with oxpeckers attending were
79-89%
lower
than in the absence of oxpeckers. These differences were highly significant in
both seasons (Mann-Whitney test, Table
1).
Discussion
Yellow-billed oxpeckers at Matobo foraged
30-350/0
of the time that they
attended impala, and this percentage remained consistent throughout the year.
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Interactions between impala and oxpeckers
6
1
50
L
40
.I
F
0
Host
body
areas
Fig.
2.
The body areas
of
impala that were foraged upon by oxpeckers during the dry season
(October-November
1992;
solid bars) and the wet season (March-April
1993;
cross-hatched bars) at
Matobo National Park. Body areas are: ears, head, neck, hindleg, tail, rump, back, foreleg, belly,
perineum, flank, shoulder, and chest.
Table
1.
Grooming per h (mean
f
SE)
of impala when oxpeckers
were in attendance compared to grooming rate of female impala
when oxpeckers were not in attendance at Matobo National Park,
and
Z-
and P-values for Mann-Whitney comparisons
Oxpeckers Oxpeckers
Grooming per h present absent
Z
P
Dry
season
Self-oral bouts
2.68
(
f
0.70) 7.48
(
f
1.20) 3.4 0.0006
Self-oral episodes
36
(
f
12) 99
(f
18) 3.2
0.001
Scratch bouts
0.39
(+0.17) 2.03 (zkO.32) 4.1
0.0001
Scratch episodes
12(f5) 51 (f9) 3.8 0.0002
Wet
season
Self-oral
bouts
3.89
(
f
0.91) 17.82
(
f
1.88) 5.8
0.0001
Self-oral episodes
45
(
f
12) 282
(
f
48) 5.6
0.0001
Scratch bouts
0.62
(
+
0.32) 3.39
(
f
0.52) 4.1 0.0001
Scratch episodes
6(+3) 70
(
f
13) 4.2 0.0001
For their part, impala hosts tolerated the foraging attentions of oxpeckers
86%
of
the time.
Of
tolerating impala,
42%
exhibited active accommodation behaviour
(lowering an ear, inclining the head, or standing still), while the remaining
58%
were indifferent to the attentions of the birds.
A
high toleration of oxpeckers and
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J.
Ecol.,
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62
M.
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Mooring and
P.
J.
Mundy
pronounced accommodation movements by impala to facilitate foraging efforts
was also reported for red-billed oxpeckers in East Africa (Hart
et
af.,
1990).
Oxpeckers were attracted to larger groups of impala insofar as there was a
positive correlation between impala herd size and oxpecker flock size. This
makes sense in terms of foraging economy because the larger the host group size,
the more oxpeckers that can be supported. The fact that oxpecker flock size
increase was not proportional to the increase in impala herd size (i.e. there were
fewer oxpeckers per impala in larger groups) suggests that one benefit to
oxpeckers
of
larger herds would be increased numbers of hosts per oxpecker by
means of a dilution effect. Although the dilution effect of grouping generally
benefits ungulate hosts by reducing the per capita risk of predation or parasitism
from flying insects in larger groups (Mooring
&
Hart, 1992b), in this case impala
in
larger herds were at a disadvantage because each impala received less foraging
attention from oxpeckers than they would have in a smaller herd.
The ears were the single most preferred foraging site for yellow-billed
oxpeckers, representing up to 50% of foraging time on impala. Hart
et
uf.
(1990)
reported similar results for red-billed oxpeckers foraging upon impala in Kenya,
with 34% of foraging directed to the ears, more than any other body part.
At
Matobo, foraging sessions on the ears were also significantly longer than sessions
directed to other body areas. This is of interest in view of the preponderance of
adult ticks (67%) collected from the ears of patch-sampled female impala and the
high percentage of impala with heavy infestations of immature ticks in the ears.
Male and female impala harboured 75-77% of adult ticks on the ear, head, and
neck region, which was where oxpeckers directed
7
1-74% of their foraging
efforts. Impala are unable to reach the ear, head, and neck for self-oral
grooming, which may explain the greater concentration of ticks found on this
region. Although impala direct scratching and allogrooming to the ears, head,
and neck, scratching is unlikely to be as effective in removing ticks as oral
grooming with the teeth (Mooring, 1995), and, because the ears are pliant and
yield to oral grooming, allogrooming is probably less efficient for tick removal
from the ears than is foraging by oxpeckers. Interestingly, red-billed oxpeckers
in
Kenya directed 72% of foraging on impala to the ear, head, and neck (Hart
et
ul.,
1990). This pattern would be adaptive for oxpeckers in terms of optimal foraging
efficiency.
Vegetational tick sampling established that adult tick challenge at Matobo
was considerably greater at the end of the wet season compared with the end of
the dry season. Oxpeckers have been shown to be almost 100% effective in
removing adult stage ticks (Bezuidenhout
&
Stutterheim, 1980), and adult ticks
would be their preferred food items compared with the smaller larval and
nymphal stages. Because engorging adult ticks (especially females) are able to
remove far more blood from the host than immatures, adult ticks represent the
greatest cost of tick infestation to hosts. Oral grooming with the teeth would be
most efficient at removing the larger adults, and previous work has shown that
adult ticks are the primary determinant of impala self-grooming rates (Mooring,
1995).
Female impala observed during the same time frame as part of another study
(Mooring, 1995) exhibited significantly higher rates of self-oral and scratch
grooming during the wet season compared with the dry season (Fig. 3).
0
East
African Wild Life Society,
Afr.
J.
Ed.,
34,
5465
Interactions between impala
and
oxpeckers
63
20
18
16
3
14
8
10
I,
12
ia
9
8
72
5E
=J
3n
SelCOral Bouts Scratch Bouts
%
Scans Grooming
Fig.
3.
Mean
(
f
SE)
self-grooming bouts per
h
and percent scans grooming by impala at Matobo
National Park during the dry season (October-November 1992) (solid bars) and the wet season
(March-April
1993)
(open bars). Data from Mooring (1995).
Presumably, this increase in grooming rate was in response to increased tick
burdens on the impala during the wet season. In support of this, rates of self-oral
grooming and scratching by impala at Kyle Recreational Park in Zimbabwe
were positively correlated with adult tick challenge throughout the year
(Mooring, 1995). Due to the seasonal variation in tick burden on impala hosts,
oxpeckers spent
72%
more time foraging during the dry season compared with
the wet season. It is suggested here that oxpeckers in the low-tick dry season were
forced to spend more time searching for the fewer ticks on their hosts, whereas
in the high-tick wet season they became satiated more quickly by the greater tick
load on impala.
Oxpecker foraging appears to reduce the amount of tick-control grooming
effort needed for impala to avoid excessive infestation. Grooming rate was
reduced during the time that oxpeckers were present upon impala hosts. (Because
impala in the presence of oxpeckers were observed only while the focal oxpecker
attended the host, an average of about
3-4
min,
it
cannot be said if there was a
residual effect whereby grooming rate remained depressed for
a
period of time
after the oxpecker departed.) Grooming is costly to impala in terms of saliva
loss, distraction from vigilance, and attrition of the dental elements (Mooring,
1995),
and oxpeckers are effective in removing ticks from the ears, head, and
neck, areas not efficiently groomed by impala because they are not accessible to
self-oral grooming. Attempting to groom with an oxpecker on the head or neck
might also entail an additional energetic cost to the impala and interfere with
grooming behaviour. When oxpeckers are in attendance, it is probably more
energetically cost-effective from a tick-removal standpoint for impala to reduce
their grooming in favour of tolerating and accommodating the foraging activity
of oxpeckers.
There is a complex network
of
relationships between oxpecker, host, and tick
burden, with oxpeckers and hosts benefiting mutually from their association.
Oxpecker foraging is influenced by impala tick load and host response (tolerance
or rejection), and the grooming behaviour of impala is influenced by the
8
East African Wild Life Society,
Afr.
J.
Ecol.,
34,
54-65
64
M.
S.
Mooring
and
P.
J.
Mundy
effectiveness of oxpecker tick removal. From the point of view
of
wildlife
management, the results presented here indicate that impala populations, at
least, would benefit from the presence of oxpeckers, both in terms of more
effective tick control on the ear, head, and neck area, and by reducing the costs
of grooming behaviour. Future studies may reveal similar benefits for other host
species.
Acknowledgments
We thank the Director of the Department
of
National Parks and Wild Life
Management, Zimbabwe, for permission to carry out the study. Chief Ecologist
A.
Conybeare provided assistance
in
initiating the project, and Provincial
Warden
1.
Ncube, Warden N. Rusike, Ranger C. Nott, Major Ncube and the
staff of Matobo National Park fully extended their cooperation. We are grateful
to W. Mazhowu of the Veterinary Research Laboratory Tick Unit for doing the
tick counts and identifications. Special thanks to
A.
Elliot and
I.
McDonald of
Touch the Wild for providing accommodation during October-November
1992.
B.
L.
Hart and an anonymous reviewer made helpful comments on a previous
draft, and E. Mooring assisted in the data analysis and drew the figure. Funding
was provided by NSF Grant BNS
9109039
to
B.
L.
Hart.
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Two species of oxpeckers occur in Rhodesia, Buphagus africanus and B. erythrorhyncus, both of which are now restricted to large game areas and some large ranches. As a conservation measure 47 B. africanus and 12 B. erythrorhyncus were introduced to the Rhodes Matopos National Park from Wankie National Park. The B. africanus have become established and have increased in numbers whereas the introduction of B. erythrorhyncus has been unsuccessful, although at least one pair is still in the release area. Birds were captured on donkeys and then transported directly by air to the Matopos for immediate release. Host selection by the birds is discussed with brief notes on competition from other species.
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Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
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Ticks from cattle were collected for the purposes of quantifying the number of tick species and their relative abundance at Msekera Regional Research Station. Fifteen species were recorded. It was found that although different species of ticks parasitized cattle throughout the year, their peaks of abundance were dependent on the season. The majority of the species had their peaks during the wet season (November to April). Rhipicephalus punctatus (Warburton) was found to be the most abundant species followed by Rhipicephalus appendiculatus (Neumann) and Amblyomma variegatum (Fabricius). Haemaphysalis leachi (Audouin) and Rhipicephalus turanicus (Morel and Vassileades) were least abundant. The findings are discussed in relation to seasonal vector abundance and disease transmission, the problems of chemical control of a multi‐species tick population and climatic influence on general tick population dynamics.
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Tick populations were observed on zebu cattle (Bos indicus) over an 18 month period at Patiko in northern Uganda. Monthly collections were made of all stages of ticks from five cattle and six sheep (Ovis aries). Collections of adults of Rhipicephalus appendiculatus Neumann were also made from the ears of about 30 cattle on several occasions. The species recorded on cattle, in order of decreasing abundance, were R. appendiculatus, Amblyomma variegatum (Fabricius), Boophilus decoloratus (Koch) and R. evertsi evertsi Neumann. Far fewer ticks were collected from the sheep. The adults of R. appendiculatus were randomly distributed over the herd. There was a distinct seasonal incidence of R. appendiculatus and A. variegatum on their hosts, which could be related to rainfall and to the emergence of new cohorts during the long rainy season. In addition, adult females of R. appendiculatus were collected daily off the ears of cattle at Entebbe following an infestation with 200 adult males and females. Measurements of the growth of the ticks were used to define the sizes of ‘standard’ ticks which would complete engorgement in the following 24 h. Such ticks provide a means of sampling to estimate the number of ticks engorging daily. Comparison of the frequency distributions of each stage and species in the Patiko collections were then used to infer the sizes of standard ticks for other species.