SHORT COMMUNICATIONS 675
The Condor 104:675–678
q
The Cooper Ornithological Society 2002
INFLUENCE OF BILL SHAPE ON ECTOPARASITE LOAD IN WESTERN SCRUB-JAYS
B
RETT
R. M
OYER
1
,A.T
OWNSEND
P
ETERSON
2
AND
D
ALE
H. C
LAYTON
1,3
1
Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, UT 84112-0840
2
Natural History Museum, University of Kansas, Lawrence, KS 66045
Abstract. Populations of the Western Scrub-Jay
(Aphelocoma californica) have bills specialized for
feeding in their respective habitats. Populations in oak
habitat have hooked bills, whereas those in pinyon
habitat have pointed bills with a reduced maxillary
overhang. Work on other bird species shows that the
bill overhang is essential for efficient preening to con-
trol ectoparasites. Given the importance of this over-
hang, we predicted that louse-infested jays with point-
ed bills would have higher louse loads than those with
hooked bills. We compared the number of lice on 65
pointed-billed (4 infested) and 105 hooked-billed (17
infested) birds. Despite their lower incidence of louse
infestation, pointed-billed birds had significantly more
lice than hooked-billed birds, supporting our predic-
Manuscript received 5 September 2001; accepted 24
April 2002.
3
Corresponding author. E-mail: clayton@biology.
utah.edu
tion. While pointed bills enhance feeding in pinyon
habitat, our results suggest that they may incur a cost
of reduced preening efficiency. Evolution of bill shape
has traditionally been interpreted mainly in terms of
foraging. Our results suggest that selection for efficient
preening may also play an important role.
Key words: Aphelocoma californica, bill shape, ec-
toparasite, lice, preening, Western Scrub-Jay.
Influencia de la Forma del Pico en la Carga de
Ectopara´sitos en Aphelocoma californica
Resumen. Los individuos de distintas poblaciones
de Aphelocoma californica tienen picos especializados
para alimentarse en sus ha´bitats respectivos. Las po-
blaciones de ha´bitats con robles se caracterizan por
picos ganchudos, mientras que las de ha´bitats con pi-
n˜ones tienen picos puntiagudos, con el gancho de la
punta de la maxila reducido. Estudios en otras especies
de aves han mostrado que el gancho del pico es esen-
cial para acicalarse eficientemente y ası´ controlar los
676 SHORT COMMUNICATIONS
ectopara´sitos. Dada la importancia de este gancho, pre-
dijimos que los individuos de A. californica de pico
puntiagudo infestados con piojos de pluma tendrı´an
una mayor carga de ectopara´sitos que aquellos de pico
ganchudo. Comparamos el nu´mero de piojos entre 65
individuos de pico puntiagudo (4 infestados) y 105 de
pico ganchudo (17 infestados). A pesar de la baja in-
cidencia de infestacio´n por piojos, las aves de pico
puntiagudo presentaron significativamente ma´s piojos
que las de picho ganchudo, apoyando nuestra predic-
cio´n. Aunque los picos puntiagudos benefician la ali-
mentacio´n en ha´bitats de pin˜ones, nuestros resultados
sugieren que podrı´an representar un costo reduciendo
la eficiencia de acicalamiento. Por lo general, la evo-
lucio´n de la forma del pico ha sido interpretada tra-
dicionalmente en te´rminos del forrajeo, pero nuestros
resultados sugieren que la seleccio´n para acicalarse efi-
cientemente tambie´n podrı´a tener un papel importante.
The adaptive significance of bill morphology has been
studied extensively in relation to foraging (Grant 1986,
Smith 1987, Benkman and Lindholm 1991, Peterson
1993). Other functions of the bill have received con-
siderably less attention. For example, bills are also im-
portant tools for preening. Daily preening is required
for straightening and oiling feathers and removing dirt
and debris from the body surface (Campbell and Lack
1985). Preening is also critical for defense against ec-
toparasites; birds with experimentally impaired preen-
ing abilities are subject to rapid increases in feather
lice (Brown 1972, Clayton 1991), which can lead to
reduced survival (Clayton et al. 1999) and mating suc-
cess (Clayton 1990). Increases in louse load also occur
on wild birds with minor bill deformities that prevent
full occlusion of the mandibles, which is necessary for
efficient preening (Pomeroy 1962, Clayton et al. 1999).
Many other studies of birds have shown detrimental
effects of other ectoparasites on fitness (Møller et al.
1990, Loye and Zuk 1991, Lehmann 1993, Clayton
and Moore 1997). Since many of these ectoparasites
are controlled by preening, they are potential agents of
selection on bill morphology.
Comparative and experimental studies show that
particular features of bill shape, such as the maxillary
overhang, are critical for parasite control. For example,
comparative analyses of 52 species of Peruvian birds
demonstrated a significant negative correlation be-
tween louse abundance and the degree to which the
upper mandible overhangs the lower mandible (Clay-
ton and Walther 2001). This correlation suggests that
species of birds with relatively long bill overhangs are
better at controlling lice by preening. (Extreme over-
hangs, such as the hooked bills of raptors and parrots,
are adaptations mainly for feeding and do little to im-
prove preening efficiency). A relationship between
length of the bill overhang and louse abundance has
also been confirmed by experiments in which removal
of the (1–2 mm) overhang of Rock Doves (Columba
livia) triggers a dramatic increase in louse abundance
(Moyer et al., in press).
A bill shape that enhances feeding efficiency may
compromise preening efficiency. Murray (1990) sug-
gested that birds with smaller bills can remove ecto-
parasites better than birds with elongated or special-
ized bills. Clayton and Walther (2001), however, found
no relationship between bill size and louse load. The
apparent reason is that birds with long bills compen-
sate by scratching more with their feet (Clayton and
Cotgreave 1994). Scratching is another effective de-
fense against ectoparasites that most birds rely upon
for controlling ectoparasites on regions they cannot
preen, such as the head (Clayton 1991). Birds with
inefficient preening may also compensate by using oth-
er defenses such as sunning and dusting behavior (Mo-
yer et al., in press). If compensatory defenses are not
as efficient as preening, however, inefficient preeners
may still have more ectoparasites than birds with ef-
ficient bills.
Populations of the Western Scrub-Jay (Aphelocoma
californica) have bills specialized for feeding in their
respective habitats (Peterson 1993, Bardwell et al.
2001). Scrub-jay populations in oak habitat have rel-
atively deep, hooked bills, whereas those in pinyon
habitat have relatively shallow, pointed bills with a
reduced maxillary overhang. The pointed morphology
allows birds to insert the bill into pinyon cones to re-
move pine seeds with a forceps-like action (see Fig. 7
of Peterson 1993). This maneuver is more difficult
with a hooked bill (Peterson 1993). Bardwell et al.
(2001) experimentally confirmed that scrub-jays with
pointed bills are more efficient at harvesting pinyon
seeds than are jays with hooked bills. The relatively
long, slender shape of the pointed bill significantly en-
hanced feeding efficiency, although the bill overhang
had no measurable effect on efficiency. Since jays with
pointed bills have a reduced bill overhang, we pre-
dicted that they would have more lice than jays with
hooked bills. To test our prediction we analyzed louse
load data from 170 freshly collected jays (Peterson
1990, 1992, 1993).
METHODS
Scrub-jays (65 pointed-billed, 105 hooked-billed) were
collected at 10 sites (4 pinyon, 6 oak) across the west-
ern United States. Pointed-billed birds were collected
from Yavapai County, Arizona (n
5
22 birds), Clark
(n
5
23) and Lander (n
5
11) Counties, Nevada, and
Tooele Co., Utah (n
5
9). Hooked-billed birds were
collected from Monterey (n
5
21), Orange (n
5
16),
Kern (n
5
19), Contra Costa (n
5
19), and Trinity (n
5
15) Counties, California, and Benton Co., Oregon
(n
5
15; see Peterson 1990, 1992 for more information
on sampling localities). Sites with mixed habitats (e.g.,
Edwards Plateau of Texas) and those near zones of
contact between differentiated forms (e.g., northeastern
California) were excluded from the analysis (Pitelka
1951).
Louse loads were measured using post-mortem ruf-
fling (Clayton et al. 1992, Clayton and Drown 2001).
Freshly killed birds were bagged individually and then
sealed in an airtight container for 10–15 min with a
cotton wad soaked in ethyl acetate. The plumage was
then ruffled over a piece of white paper for at least 60
sec, with each major body region (wings, head, un-
derparts, upperparts) ruffled for at least 15 sec. Lice
were preserved in 70% ethanol, and later identified and
counted. Values reported below are means
6
SE.
SHORT COMMUNICATIONS 677
FIGURE 1. Relationship of bill morphology to mean
(
6
SE) number of lice recovered from infested West-
ern Scrub-Jays (Aphelocoma californica) by post-mor-
tem ruffling. Profiles (to scale) of pointed and hooked
bills traced from Peterson (1993,
q
University of Chi-
cago Press, used with permission).
RESULTS
Three species of lice were found on the scrub-jays:
Philopterus crassipes, Myrsidea sp., and Brueelia de-
ficiens. The three species were pooled for the analyses
in order to investigate how bill shape affected the over-
all louse community. Louse prevalence was 12% (21
of 170 jays had lice). The proportion of pointed-billed
birds with lice (4 of 65; 6%) was smaller than the
proportion of hooked-billed birds with lice (17 of 105;
16%; Fisher’s exact test, P
5
0.06). Despite the small
number of samples, infested birds with pointed bills
had significantly more lice (5.0
6
2.7) than did those
with hooked bills (1.7
6
0.2; Mann-Whitney test, Z
5
1.9, P
5
0.05). Figure 1 shows the relationship of bill
morphology to louse loads among infested birds.
DISCUSSION
These data are consistent with the prediction that jays
with pointed bills are less efficient at preening than
jays with hooked bills. This is not to say that individ-
uals with pointed bills are completely incapable of
controlling their louse loads. We excluded an infested,
pointed-billed jay from our analyses because it was
missing the entire distal half of its lower mandible.
This bird, which was completely incapable of preen-
ing, had nearly twice as many lice (n
5
22) as the next
most infested bird in our study.
Factors in addition to bill morphology could con-
ceivably have contributed to the difference in louse
loads of pointed-billed and hooked-billed birds. For
example, several studies have shown that large-bodied
species of birds have more lice than small-bodied spe-
cies, presumably because large-bodied hosts represent
more abundant resources for lice (Gregory 1997, Ro´z-
sa 1997, Clayton and Walther 2001). The same rela-
tionship may hold within species, with larger-bodied
populations or individuals having more lice. However,
body size could not have confounded the results of the
present study. Infested pointed-billed birds were sig-
nificantly smaller (n
5
4, mean
5
79.3
6
2.7 g) than
infested hooked-billed birds (n
5
17, mean
5
93.7
6
2.4 g; Mann-Whitney test, Z
5
2.4, P
,
0.05). In short,
small jays actually had more lice than large jays.
Ambient humidity is another factor that can influ-
ence louse abundance. Moyer et al. (2002) showed that
wild birds in arid habitats have significantly fewer lice
than do conspecifics in humid habitats. To confirm hu-
midity as the causal agent, they conducted an experi-
ment with captive Rock Doves in which they manip-
ulated ambient humidity. Louse infestations decreased
dramatically on birds kept at low humidity, compared
to birds at high humidity. The pinyon habitat of scrub-
jays with pointed bills was significantly drier (mean
relative humidity
5
35%, range 20% to 47%, n
5
4)
than that of the oak habitat in which the hooked-billed
birds were collected (mean
5
62%, range 39% to 76%,
n
5
6; comparison of National Weather Service av-
erage humidity near each site during the months of
sampling: Mann-Whitney test, Z
5
2.0, P
,
0.05). The
risk of infestation was lower in pinyon habitat. Only
6% of jays (4 of 65) were infested in pinyon habitat,
whereas 16% of jays (17 of 105) were infested in oak
habitats.
The fact that infested pointed-billed birds had sig-
nificantly more lice than infested hooked-billed birds,
despite the former having smaller body size and living
in more arid habitat, emphasizes the critical role of the
bill overhang in preening for louse control. While
Bardwell et al. (2001) demonstrated that the pointed
bill shape of scrub-jays enhances feeding efficiency in
pinyon habitats, our results suggest that pointed-billed
birds incur a cost in terms of reduced preening effi-
ciency.
The mean difference in lice on pointed- versus
hooked-billed birds was only 3.3 lice. Could such a
small difference have fitness consequences for the
host? This is indeed possible for two reasons. First, the
data shown are subsamples of lice removed by post-
mortem ruffling, which gets only a fraction of the lice
on a bird (Clayton and Drown 2001). We estimated the
total number of lice to be at least five times higher
than the subsamples, which would be a mean of about
25 lice on pointed-billed and 8 lice on hooked-billed
jays. This threefold difference could well translate into
a significant difference in the energetic costs and fit-
ness consequences of feather damage from lice (Booth
et al. 1993, Clayton et al. 1999). Second, lice can vec-
tor pathogens and endoparasites (Saxena et al. 1985,
Clayton and Adams, in press); all else being equal, the
probability of infection by such agents increases with
louse load.
Bill shape has traditionally been interpreted mainly
in terms of foraging. Our results suggest that selection
for efficient preening may also play a role in the evo-
lution of bill shape. Research comparing the feeding
and preening efficiencies of captive birds with differ-
ent bill shapes could help determine the extent to
which the evolution of bill shape has been governed
by a feeding-preening tradeoff, rather than by trophic
selection alone.
678 SHORT COMMUNICATIONS
The work on jays was supported by grants to ATP
from NSF (BSR-8700850), the National Geographic
Society, Field Museum of Natural History, and the
Hinds Fund of the University of Chicago. DHC was
supported by an NSF CAREER award (DEB-
9703003), and BRM was supported by grants from
Sigma Xi and the Frank M. Chapman Memorial Fund
of the American Museum of Natural History. We thank
C. W. Benkman, J. Burtt, B. A. Walther, G. E. Wool-
fenden, and an anonymous referee for helpful com-
ments on the manuscript. We are grateful to R. D. Price
for identifying and counting the lice.
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