The Open Ornithology Journal, 2010, 3, 41-71

41Open Access

How Birds Combat Ectoparasites
Dale H. Clayton*,1, Jennifer A. H. Koop1, Christopher W. Harbison1,2, Brett R. Moyer1,3 andSarah E. Bush1,4
1

Department of Biology, University of Utah, Salt Lake City, UT 84112, USA; 2Current address: Biology Department,
Siena College, Loudonville, NY, 12211, USA; 3Current address: Providence Day School, Charlotte, NC, 28270, USA;
4
Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas 66045, USA
Abstract: Birds are plagued by an impressive diversity of ectoparasites, ranging from feather-feeding lice, to featherdegrading bacteria. Many of these ectoparasites have severe negative effects on host fitness. It is therefore not surprisingthat selection on birds has favored a variety of possible adaptations for dealing with ectoparasites. The functional significance of some of these defenses has been well documented. Others have barely been studied, much less tested rigorously.
In this article we review the evidence - or lack thereof - for many of the purported mechanisms birds have for dealing withectoparasites. We concentrate on features of the plumage and its components, as well as anti-parasite behaviors. In somecases, we present original data from our own recent work. We make recommendations for future studies that could improve our understanding of this poorly known aspect of avian biology.

Keywords: Grooming, preening, dusting, sunning, molt, oil, anting, fumigation.
INTRODUCTION

2) Mites and ticks (Acari): many families [6-9].

As a class, birds (Aves) are the most thoroughly studiedgroup of organisms on earth. Nevertheless, the adaptivefunction of many intriguing features of avian morphology,
physiology, and behavior are still uncertain. Some of thesefeatures are thought to play a role in defense against harmfulectoparasites. Examples include the pectinate middle claw ofmany birds, the strange odors of some birds, and the odd"maintenance" behaviors, such as sunning, anting or dusting,performed by many birds. In this article we review the ways
in which birds are thought to combat ectoparasites. We pay
particular attention to possible anti-parasite features of theplumage itself, as well as various forms of anti-parasite behavior. Although the immune system also plays an importantrole in defense against some ectoparasites, such as bloodfeeding mites [1], we do not cover immune defenses in thisreview. Instead, we refer readers to other papers in this volume, and recent reviews of immunology published elsewhere, e.g. [2] and [3].

3) Leeches: four families [10].
4) Fungi: keratinophilic and cellulose decomposing forms[11].
5) Bacteria: several unrelated groups that decompose feathers [12].
Relatively little was known about the impact of ectoparasites on non-game wild birds until about 25 years ago, whenornithologists began to take a strong interest in parasites.
One catalyst was Hamilton and Zuk's influential 1982 [13]paper arguing that the elaborate visual and acoustic displaysof many birds evolved as a result of parasite-mediated sexual
selection. Since then, dozens of papers testing the impact ofparasites on wild birds have been published. For reviews,
including the topic of sexual selection, which we will notcover here, see [3, 14-21].

1) Insects: Four orders, including lice (Phthiraptera), fleas(Siphonaptera), true bugs (Hemiptera), and flies (Diptera)[5].

These studies confirm that many ectoparasites are potent
agents of selection on birds, affecting both the survival andreproductive components of avian fitness. Not surprisingly,
therefore, birds appear to have evolved a wide variety ofdefenses for controlling ectoparasites. Moyer and Clayton[22] provided a succinct review of defenses involving plumage as a barrier, and antiparasite behaviors of birds. Since
their review, several dozen new papers have been publishedwith information pertinent to these kinds of defenses. We
review these papers below, and in some cases we reportoriginal data relevant to purported defenses.

*Address correspondence to this author at the Department of Biology, University of Utah, Salt Lake City, UT 84112, USA; Tel: 801-581-6482;
Fax: 801-581-4668; E-mail: clayton@biology.utah.edu

We consider ectoparasites to include taxa that spend at
least some of their life cycle in close association with thehost, as opposed to more ephemeral "parasites", such as
mosquitoes. We do not cover defenses aimed primarily at

In the classic work Fleas, Flukes and Cuckoos, Rothschild and Clay [4] catalogued the incredibly rich diversityof parasitic organisms inhabiting birds, including groups as
different as viruses, fungi, bacteria, protozoa, worms andarthropods. The major groups with ectoparasitic forms are as
follows:

1874-4532/10

2010 Bentham Open42 The Open Ornithology Journal, 2010, Volume 3these ephemeral species, such as fly repelling behavior, defensive sleeping postures, microhabitat choice, territoriality,and "selfish herd" effects. For reviews of these topics see
Lehane [23], Hart [24] and Weldon and Carroll [25].
We use parasite load in reference to any of the following
more precise measures: richness (the number of species ofparasites present); prevalence (the fraction of parasitizedindividuals in a host population); intensity (the number ofindividual parasites in an infested host); abundance (thenumber of individual parasites in a host, regardless of infestation). Hence, mean intensity is the average number of individual parasites across infested hosts in a population, andmean abundance is the average number of parasites acrossall host individuals, regardless of infestation. For further
details see Bush et al. [26].
PLUMAGE AS A BARRIER
Most ectoparasites are in contact with the plumage, atleast some of the time. Some ectoparasites, such as feather
lice (Phthiraptera: suborder Ischnocera), are in contact withthe plumage all of the time. Indeed, they even feed on feathers, which are digested with the aid of endosymbiotic bacteria [27]. It is therefore reasonable to expect that some chemical or mechanical features of the plumage may have evolved
to deter ectoparasites, similar to the many features of foliage
known to deter herbivorous insects [28]. Plumage related
defenses might include feather molt, analogous to the abscission of plant leafs reducing infestations of leaf miners andother endophytic and sessile herbivorous insects (reviewed
in Stiling et al. [29]).
Feather Molt
Conventional wisdom has it that feather molt helps reduce ectoparasite loads [5]. Indeed, molt presumably does
help birds jettison immobile parasites, such as fungi and bacteria that live in the plumage. Burtt and Ichida [30] showedthat the abundance of feather-degrading bacteria fluctuates
seasonally, with the smallest infestations in the autumn,
which is consistent with this hypothesis. But it remains unclear whether molt plays an important role in controlling
more mobile parasites, such as mites and lice.
Records of lice on molted feathers suggest that molt may
indeed reduce arthropod ectoparasite loads [31]. Post andEnders [32] attributed the low prevalence of lice on Sharptailed Sparrows (Ammodramus caudacutus), compared to
Seaside Sparrows (A. maritimus), to the fact that the former
molt twice a year, while the latter molt once a year. Several
researchers have carried out longitudinal studies in which
they documented an apparent reduction in ectoparasite load
over the course of the host’s molting period [33]. Baum [34]reported an 85% drop in the abundance of lice on molting
Eurasian Blackbirds (Turdus merula). Markov [35] observed
a decrease in the number of ectoparasites on European Starlings (Sturnus vulgaris) during the autumn, and argued thatfeather molt caused this decrease. However, Boyd [36] suggested that seasonal changes in climate were actually responsible for the autumn reductions. Changes in climatic factors particularly ambient humidity - are known to have a significant impact on ectoparasite abundance, at least in the case oflice [22, 37, 38].

Clayton et al.

A recent longitudinal study of ectoparasite loads on
House Finches (Carpodacus mexicanus) indicates that therelationship between molt and ectoparasite abundance can becomplicated [39]. The results of this study show that theabundance of two species of feather mites (Strelkoviacarus
sp. and Dermoglyphus sp.) increased, rather than decreased,
during the molting season. The louse Menecanthus alaudae
also increased during the molting season on male House
Finches. The authors argued that the energetic cost of molt
reduced the amount of energy birds could expend on activities such as preening, leading to an increase in ectoparasites.
The authors also compared the ectoparasite loads of birds invarious degrees of molt. Molting males had more feather
mites than non-molting males, whereas the number of mites
on molting vs. non-molting females did not differ significantly. In addition, the study showed that molting males had
more lice than molting females. The authors suggest thatthese patterns are driven by the additional energetic costs
associated with the possession of showy plumage in males.
Moyer et al. [40] conducted an experimental test of the
impact of molt on ectoparasites. The authors manipulated
photoperiod to trigger early molt in captive Rock Pigeons(Columba livia) infested with lice. They then tracked theabundance of lice on molting and non-molting (control) birds
over the course of several weeks. Visual examination of lice
on different body regions indicated that feather molt reduced
louse abundance. However, body washing, a more robust
method of quantifying lice [41], showed that molt did not, infact, reduce the abundance of lice. Two factors caused visual
examination to underestimate the number of lice on the molting birds. First, molt replaced worn feathers with new, lush
plumage that obscured lice during visual examination. Second, lice sought refuge inside the sheaths of newly developing feathers, where they could not be seen. The illusion of
reduced louse abundance documented by Moyer et al. [40]calls into question observational studies documenting apparent reductions in lice during molt. This may also be true forother ectoparasites.
A few studies of molt have used methods for quantifying
ectoparasites that are more rigorous than visual examination.
For example, Chandra et al. [42] fumigated Common Mynas(Acridotheres tristis), ruffled their plumage, and quantified
the lice. McGroarty and Dobson [43] used body washing todetermine the number of lice on House Sparrows (Passer
domesticus). Both studies showed a reduction in louse abundance in late summer, coincident with the postnuptial molt of
the host. However, experimental manipulations are stillneeded to establish molt as the cause of these decreases,
rather than some third factor that covaries with both molt andectoparasite reductions. One such factor could simply betransmission of lice from parent to offspring birds. Lice typically move in large numbers from parent birds to their offspring at the end of the breeding season, leading to a decrease in the abundance of lice on adult birds around thetime of molt [44-47]. Dispersal of lice to juveniles could also
explain why fewer newly deposited feather louse eggs arefound on adult feathers near the end of the host’s breeding
season [48].
Host physiological constraints may give many ectoparasites time to circumvent molt, which tends to be a gradualprocess in most birds because thermal insulation and aerody-How Birds Combat Ectoparasites

namic efficiency are both compromised in proportion to thenumber of missing feathers [49, 50]. Energy is also required,of course, to create each new feather [51]. Feather quality
can be inversely proportional to the rate of molt, further suggesting constraints on rapid molt [52]. If feathers are lost
gradually, then it may be possible for ectoparasites to avoid
feathers that will soon be molted. A survey of feather mite
distributions on the flight feathers of molting passerines
shows that mites can, in fact, avoid molting feathers [53].
Similarly, mites that live inside the quills of feathers (Syringophilidae) are known to abandon the old feathers in favor of
new ones before the old ones molt [54, 55].
Two mechanisms have been proposed to explain how
ectoparasites detect and avoid molting feathers [56]. The“vibration” hypothesis proposes that the cue used by the ectoparasites is the vibration caused by rocking of the oldfeather as it is pushed out of a follicle by the newly emerging
feather. The “window” hypothesis proposes that ectoparasites on sequentially molting flight feathers can detectchanges in movement or airflow caused by absence of theadjacent, molted feather. Pap et al. [57] addressed both hypotheses in a clever experiment. To test the window hypothesis they removed the sixth primary feather from nonmolting Barn Swallows (Hirundo rustica). To test the vibration hypothesis they cut part way through the shaft of thesixth primary feather of the opposite wing to simulate vibration in a molting feather. The simulated window did notcause mites to leave the adjacent (seventh) primary on thefirst wing, suggesting that the vibration hypothesis might be
the correct explanation. Unfortunately, the authors did notreport whether mites left the partially cut sixth primary on
the opposite wing, nor did they report the number of mites
on the fifth primary, which is one place the mites would be
expected to move in response to vibration. The authors didnote a decrease in the number of mites on the eighth primary,
but the relevance of this observation is unclear. Interestingly,
experimental birds with pulled or cut feathers had significantly fewer mites on the flight feathers than did control
birds at the end of the experiment. The authors suggested
that the mites may have moved from flight feathers onto
body feathers to escape molt, but there were no data withwhich to test this hypothesis.
Jovani et al. [56] also evaluated the two hypotheses using
mites on Barn Swallows. As in many birds, there is a timelag between molting of a primary feather, which creates awindow, and hypothesized vibration in the adjacent feather
before that feather also molts. Jovani et al. [56] found thatmites stayed on feathers near the window for a long time,
moving only when the feather was nearly ready to drop. As
in the case of Pap et al.'s study [57] this observation suggeststhat vibration may be a more important cue than the appearance of a window. However, additional experimental manipulations of cues that ectoparasites could use to detect molt
are needed for a more complete understanding of this question.
Feather Toughness
Feathers containing melanin—the pigment typically responsible for brown, gray or black colors [58]—are moreresistant to mechanical abrasion than feathers without melanin [59, 60]. This toughness makes melanin rich feathers

The Open Ornithology Journal, 2000, Volume 3

43

more resistant to wear and tear, and may also deter featherfeeding ectoparasites. Two studies suggest that melanin canlimit damage by feather feeding lice [61, 62]. Kose and colleagues [61] surveyed feather damage in Barn Swallow (Hirundo rustica) populations and found that the holes chewed
by lice were significantly more likely to occur in the white(melanin-free) spots on the tail feathers, compared to black(melanin-rich) regions of the tail. The authors conducted alouse-preference trial in vitro and found that the lice preferred to be on white portions of the tail feathers. Unfortunately, recent evidence indicates that the louse genus studied
by Kose et al. [61] is not the one that creates holes in thefeathers, thus bringing into question the relevance of theirexperiment. Kose et al. [61] studied preferences of the louse
Machaerilaemus malleus (synonym: Hirundoecus malleus),in the family Menoponidae, whose members often feed onblood and feathers [63]. The holes in Barn Swallow tailfeathers appear to be caused by members of the genus
Brueelia [64], in the family Philopteridae, whose members
typically feed on feathers and dead skin. The experiments
performed by Kose et al. [61] need to be repeated using
Brueelia.
Experiments conducted by Bush et al. [65] indicate thatmelanin does not have an effect on feather-feeding lice fromRock Pigeons. The authors captured pigeons of different
color morphs ranging from white to black. Feather-feeding
lice (Columbicola columbae, and Campanulotes compar)
were fed feathers from these birds in vitro. After two weeks,
there was no significant difference in the amount of feather
material consumed, nor in the survival of lice on featherswith different amounts of melanin. Additional experimentswith C. columbae showed that there was no significant difference in reproduction of lice on white vs. black feathers,
nor did the lice exhibit a preference for different coloredfeathers.
Melanized feathers may be more resistant to featherdegrading bacteria (FDB). Three studies have addressed thisquestion by exposing Bacillus licheniformis, a common
strain of FDB, to melanized and unmelanized feathers. Goldstein et al. [66] suggested that melanized feathers resisted
degradation by FDB; however, this study was performed
without adequate controls or replicates [67]. In contrast,
Grande et al. [68] found that FDB actually degraded melanized feathers faster than unmelanized feathers; however, in
this study feather degradation was scored visually, which
may be problematic because color could bias human perception of degradation. In an attempt to remedy these shortcomings, Gunderson et al. [67] conducted an experiment where
goose feathers were inoculated with B. licheniformis. They
found that melanized feathers had lower bacterial densities,
degraded more slowly, and had less degradation than unmelanized feathers, indicating that melanin does, in fact,
deter at least one strain of FDB in vitro.
Many species of birds have melanic morphs, and the darker
morphs typically live in more humid regions – a pattern
known as Gloger’s rule [69]. Burtt and Ichida [70] hypothesized that this pattern may be driven by FDB, which thrive inhumid conditions. They compared the degradation rates of B.
licheniformis isolated from darkly colored Song Sparrows(Melospiza melodia) from a humid region and more lightly
colored Song Sparrows from an arid region. By growing

44 The Open Ornithology Journal, 2010, Volume 3these bacterial isolates on chicken feathers under “common
garden” laboratory conditions, the authors showed that thebacteria from the humid region degraded feathers faster thanbacteria from the arid region. Burtt and Ichida [70] suggested
that Song Sparrows in humid regions (where bacteria do
better) evolved more melanin because of increased pressure
from the more detrimental strain of B. licheniformis.
In another study, Cristol et al. [71] inoculated the feathers of live birds with B. licheniformis to test the impact ofsunning behavior on FDB. They noticed that darkly colored
European Starlings (Sturnus vulgaris) had far less damage
than more lightly colored Northern Cardinals (Cardinalis
cardinalis). However, as the authors themselves point out,
these data are only suggestive, since the experiments withstarlings and cardinals were run at different temperatures,
humidities, and for different lengths of time.
In summary, studies with B. licheniformis [70, 71] suggest that melanin may be an important defense against FDB.
However, experiments manipulating bacteria in vivo on lightand dark birds are needed for a more convincing test of thishypothesis, as well as to test the fitness consequences of
FDB for birds [72]. Moreover, studies are needed to understand how melanin affects bacterial communities. Interactions between bacteria could alter how we interpret the roleof melanin as a bacterial defense. Experiments done in vivo
should, if possible, incorporate whole communities of FDB,
not just B. licheniformis, which is often studied because it
can be cultured in vitro. Work is also needed to elucidate theprecise mechanism(s) by which melanins deter bacteria [67].
It is entirely possible that an antibacterial role of melanin
could have more to do with its influence on the avian immune system [3] than it's influence on feather hardness (seeother articles in this volume).

Clayton et al.

This hypothesis has been tested most thoroughly in Crested
Auklets (Aethia cristatella) (Fig. 1), which emit a pungent
citrus-like odor that humans can detect at a considerable distance from breeding colonies [82]. Douglas et al. [83] identified the odor constituents as a series of short-chained, saturated and monounsaturated aldehydes, which are corrosive
irritants that are volatile and reactive. The authors suggested
that the citrus odor might repel ectoparasites since two of the
major constituents, hexanal and octanal, are known arthropod repellents.
Douglas et al. [84] tested the effect of synthetic versionsof auklet odorant compounds on two genera of auklet lice
(Austomenopon sp. and Quadraceps sp.). Lice exposed to
1μl of either octanal or Z-4-decanal became moribund inseconds. In contrast, when Douglas et al. [85] exposed Rock
Pigeon lice (Columbicola columbae and Campanulotes compar) to fresh auklet feathers placed in covered petri disheswith lice, or to fresh auklet carcasses sealed in beakers withlice, there was no effect on parasite survival. Douglas et al.
[85] also compared the relative abundance of lice on Crested
Auklets to lice on Least Auklets (A. pusilla), which do notemit a noticeable odor (the birds were from the same mixed
breeding colony). They found that Crested Auklets actually
had significantly more lice than Least Auklets, even after
controlling for a difference in host body size.
Douglas et al. [84] also tested the effect of synthetic versions of auklet odorant compounds on two species of ticks.
Laboratory reared ticks (Amblyomma americanum) were
exposed to octanal on an artificial host consisting of filter
paper attached to a heated, rotating drum. Ticks detached

FEATHER TOXINS
Toxins in the plumage of some birds may help combat
ectoparasites [25, 73]. The best-known example is batrachotoxins in the feathers and skin of several species in the New
Guinea passerine genera Pitohui and Ifrita [74, 75]. Batrachotoxins, which are also found in the skin of poison dart
frogs, (Phyllobates spp.) are thought to play a role in deterring predators. Experimental evidence suggests that the toxins also deter ectoparasites [76-78]. Dumbacher [78] conducted a series of in vitro trials in which he exposed feather
lice from a variety of bird species to feathers of Pitohui andother non-toxic birds. He found that lice avoid feeding or
resting on Pitohui feathers when they are given a choice.
Lice on Pitohui feathers also show higher mortality than lice
on non-toxic feathers. Since batrachotoxin detrimentallyaffects a wide variety of invertebrates [78], it may deter
other ectoparasites in addition to lice. Interestingly, a surveyof 30 New Guinea passerine genera showed that Pitohuis
had the lowest tick loads [79]. Another study showed that thefamily Pachycephalidae, which includes the genus Pitohui,
has comparatively few arthropod-vectored haematozoan
parasites [80].
Odorous Feathers
At least 80 genera of birds in 17 orders produce odorsthat humans can readily detect [81]. It is possible that one
adaptive function of such odors is to combat ectoparasites.

Fig. (1). Crested Auklets (Aethia cristatella), such as the one shown
here, emit a citrus-like odor that may deter ectoparasites. Photo by
Hector Douglas.

How Birds Combat Ectoparasites

significantly faster from artificial hosts treated with 10%
octanal than from artificial hosts treated with ethanol. Ticks
were also exposed to a synthetic cocktail designed to mimic
the diverse chemical composition of auklet odorant. Ticks
challenged with this cocktail (40% octanal, 21% hexanal, 8%Z-4 decenal, 3% decanal, 7% hexanoic acid, and 3% octanoic acid) showed a dose dependent response. Ticks exposed
to at least a 10% dilution of the cocktail remained attached tothe artificial host for a shorter period of time than controls.
Douglas et al. [84] also conducted experiments with Ixodes
uriae, the tick found on Crested Auklets in nature. The results were similar to the experiments conducted with A.
americanum. Moreover, when these ticks were placed in avial with 5μl octanal, they became moribund within an hour.
In another study involving I. uriae ticks, Douglas [86]quantified the relative odor emissions from 57 live Crested
Auklets. Interestingly, the individual with the lowest emission level was infested with 14 ticks. Only one other bird
was infested (with two ticks), out of 96 birds surveyed in thesame breeding colony. In contrast, Hagelin [87] found noevidence that I. uriae ticks are repelled by fresh Crested
Auklet feathers placed in petri dishes, compared to feathersof Least Auklets or Parakeet Auklets (A. psittacula), neitherof which emit a noticeable odor.
Hagelin and Jones [81] have argued that the repellency
studies conducted by Douglas et al. [84] used synthetic compounds that exceed natural concentrations (c.f. those measured in auklet odorant by Hagelin et al [88]). In response,
Douglas [89] argued that Hagelin et al.’s study underestimated the quantity of volatiles in auklet feathers because thesamples were kept under suboptimal conditions, during
which time they may have degraded (and see Hagelin [90]).
Douglas [91] published data indicating that naturalconcentrations of auklet odor are, at least in some cases,
greater than those published by Hagelin et al [88]. He also
conducted in vitro experiments with ticks (A. americanum)
exposed to low doses (0.5% and 1%) of a synthetic cocktail.
Douglas [91] argued that these doses simulate natural conditions because the 1% solution exposed ticks to lower concentrations of octanal than he isolated from the crown and napefeathers of Crested Auklets. Locomotion of ticks at bothdoses in this study was significantly less than that of controls, and there was evidence of paralysis in some of the ticks
exposed to the 1% treatment. These results suggest that thecompounds in Crested Auklet odorant do have the potential
to deter ticks. What is needed for a more definitive study, if
possible, is a test of the impact of the odorant on ticks undernatural conditions in the field. Ideally, this test would involve some kind of experimental manipulation of odorantlevels. Tests for an impact of odorants on ectoparasites inother groups of birds are also needed.
Uropygial Oil
Most birds have a nipple-like uropygial (preen) gland on
their rump. They squeeze this protuberance with their bill
during preening and spread its oil throughout the plumage.
The oil is known to help maintain plumage strength andflexibility, but it has long been thought that the oil may also
deter ectoparasites [77, 92, 93]. Uropygial oil could combat
ectoparasites by reducing their mobility on feathers or skin.
If the oil coats the exterior of a parasite, or at least plugs the

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spiracles (breathing holes) of arthropod parasites, it mightalso suffocate them [94]. In some species of birds the oil isassociated with noxious or repellent odors, which could conceivably affect ectoparasites [73].
Moyer et al. [94] tested whether preen oil helps Rock
Pigeons combat feather lice. They compared the survival oflice raised in an incubator on feathers treated with uropygial
oil to the survival of lice on control feathers without oil.
They found that lice on oiled feathers died more rapidly thancontrols. They also compared the population dynamics oflice on captive pigeons with intact uropygial glands to liceon pigeons with their glands surgically removed. Removal of
the gland had no significant effect on louse populations overa period of four months (about 5 louse generations). Thisfinding suggests that birds do not “fumigate” themselveswith preen oil, despite the fact that the oil does, in fact, havethe capacity to kill lice when applied in vitro [94].
Uropygial oil may inhibit the growth of certain pathogenic bacteria and fungi that inhabit the plumage of birds[11,95-99]. Jacob et al. [99] demonstrated that constituentsof Pelecaniform uropygial oil, applied in vitro, have a dosedependent inhibitory effect on Gram-positive bacteria andfungal dermatophytes (Trichophyton sp., Microsporum
gypseum). The Red-billed Woodhoopoe (Phoeniculus purpureus), like other species of woodhoopoes, emits a malodorous secretion from its uropygial gland [73]. Law-Brown[98] identified 17 chemical constituents found in the uropygial oil of this species. Using disc-diffusion assays, shetested the in vitro activity of each constituent against 13
pathogenic bacterial strains (e.g., Salmonella enteritidis,
Staphylococcus aureus, and Streptococcus faecalis), andagainst a strain of the feather-degrading bacterium Bacillus
licheniformis [30]. Seven of the constituents significantly
inhibited bacteria, suggesting that uropygial oil has the potential to combat bacterial infections and concommitantfeather degradation.
Interestingly, most of the chemical constituents of theuropygial oil of Red-billed Woodhoopes are synthesized by
yet another bacterium, Enterococcus phoeniculicola, which
lives in the bird’s uropygial gland. Law-Brown [98] treatedthe glands of this species with an antibiotic, and then compared the chemical composition of their uropygial oil to thatof untreated controls. Her results showed that only two of 17
constituents were still present following antibiotic treatment.
Furthermore, the ones that remained in the oil (e.g., cholesterol) were present at elevated levels, suggesting they wereno longer metabolized in the absence of the bacteria. This
pioneering study is the first to document a bacterial symbiont
that metabolizes constituents of uropygial oil.
Uropygial oil affects different strains of parasitic bacteria
and fungi in different ways. Pugh and Evans [96] tested theimpact of European Starling (Sturnus vulgaris) “feather fats”
on four species of keratinophilic fungi. They made the interesting observation that, while sporulation of Chrysosporium
keratinophilum increased, the same oils inhibited the growthof Arthroderma quadrifidum, A. uncinatum and Ctenomyces
serratus. Pugh [11] found that the feather fats of Blackbirds(Turdus merula) inhibited the growth of C. serratus, while
stimulating the growth of A. curreyi. In a similar study, Bandyopadhyay and Bhattacharyya [100] tested the effects ofuropygial oil on several fungal species cultured from the skin

46 The Open Ornithology Journal, 2010, Volume 3

Clayton et al.

of white leghorn fowl. They found that surgical removal of
the uropygial gland led to an increase in the populations ofall but one species of fungi.
Shawkey et al. [101] suggest that uropygial oil might
benefit birds by promoting the growth of bacteria or fungithat out compete or otherwise exclude more virulent microbes. The authors identified 13 bacterial isolates from thefeathers of wild house finches (Carpodacus mexicanus), andmeasured the feather-degrading activity of each. They tested
the effects of uropygial oil on the survival and growth ofeach strain through a disc-diffusion assay. They found thaturopygial oil inhibited the growth of three feather degradingstrains, including Bacillus licheniformis, but it had less of aneffect on more benign strains. Future studies should aim toclarify the impact of uropygial oil on bacterial and fungal
strains both in isolation, and in the context of the full microbial community.
Feather mites may have an entirely different relationshipwith uropygial oil. Blanco et al. [102] suggested that feather
mites are commensals, or even mutualists, rather than parasites. The main food resource of certain feather mites is uropygial oil on the feathers. Along with the oil, the mites consume microbes such as fungi and bacteria [9]. If these microbes include forms that are dangerous to the bird, the consumption of uropygial oil by feather mites may be beneficial
to the host [103, 104]. This interesting hypothesis should betested experimentally.
BODY MAINTENANCE BEHAVIOR
Grooming behavior, defined as preening and scratchingcombined [105], is known to be critical for defense against
ectoparasites [5, 24]. Preening is of two types: self-preening(Fig. 2a) and allopreening (Fig. 2b). Water bathing, dusting,sunning, anointing and cosmetic behaviors may also play arole in ectoparasite defense. Below we review the evidence
relevant to each of these behaviors, as well as the evidence
relevant to the different types of grooming.
Grooming: Self-Preening
Preening is the most common defensive behavior thatbirds use against ectoparasites. Preening involves the birdpulling its feathers between the two mandibles of the bill, or
nibbling the feathers with the bill tips. Birds can spend asignificant portion of their daily time budget preening; e.g.
Losito et al. [106] showed that juvenile mourning doves
spend up to 23% of their time preening. This is a considerable amount of time and energy, given that the cost of preening can be about twice the basic metabolic rate [107]. Crolland McLaren [108] documented a nearly 200% increase in
the metabolic rate of preening Thick-billed Murres (Urialomvia), compared to resting individuals. The increase washigher than that associated with either feeding (49%) or diving (140%).
Many studies have shown that preening is a critical defense against ectoparasites. The defensive role of preening
was initially suggested by natural “experiments” in whichbirds with bill deformities have very high ectoparasite loads[4, 5, 31, 34, 36, 109-113]. For example, Clayton et al. [113]observed that among 150 wild Rock Pigeons, the three individuals with the most feather lice all had minor bill deformi-

Fig. (2). (a) Preening Black Swan (Cygnus atratus). Photo by Noodle Snacks (commons.wikimedia.org). (b) Allopreening between
Magellanic Penguins (Spheniscus magellanicus). Photo by Andreas
Edelmann (fotolia.com).

ties. One of the deformed individuals had more than 10,000
lice, compared to a mean of 631 lice on birds without deformities. Of course, birds with deformed mandibles may
have other problems, such as impaired foraging ability,
which could contribute to increases in ectoparasite load
[114-117]. Therefore, a rigorous test of the role of preening
in ectoparasite control requires an experimental approachthat alters only preening efficiency.
Early such tests impaired preening crudely by clippingca. 1 cm from the upper mandible of domestic chickens or
pigeons, leading to dramatic increases in ectoparasite load
[118-121]. Subsequent tests impaired preening in a less invasive way, using poultry “bits,” which are small, C-shaped

How Birds Combat Ectoparasites

pieces of metal or plastic. Bits are inserted between the upper and lower mandibles and crimped slightly in the nostrils
to prevent dislodging, but without damaging the tissue. They
create a 1-3 mm gap between the mandibles that impairs theforceps-like action of the bill required for efficient preening.
Bitting triggers a dramatic increase in feather louse populations on pigeons [112, 113, 122, 123]. This increase is notdue to side effects of bits, such as an impact on feeding, because pigeons feed on whole grain (corn, peas, etc.) that canbe picked up despite the small mandibular gap created by thebits. Clayton and Tompkins [123] showed that bits have noeffect on the survival or reproductive success of (unparasitized) Rock Pigeons, compared to non-bitted controls.
The importance of preening for ectoparasite control isalso apparent from comparative studies. The size of the billoverhang varies markedly across species of birds (Fig. 3).
For example, Clayton and Walther [124] compared the diversity of lice among 52 species of Peruvian birds belonging
to 13 families. Phylogenetically independent comparisonsrevealed a significant negative correlation between louse
abundance and degree to which the upper mandible (maxilla)
overhangs the lower mandible. This correlation suggests thatbirds with slightly longer overhangs are better at controlling

The Open Ornithology Journal, 2000, Volume 347lice by preening. Extreme overhangs, such as the hooked
bills of raptors and parrots, are adaptations for feeding that
do not enhance preening efficiency [124].
Clayton et al. [125] demonstrated how the maxillary
overhang functions to control lice. Experimental removal of
the tiny (1-2 mm) overhang (Fig. 3e,f), triggered a dramaticincrease in louse population size (Fig. 4a). Regrowth caused
the louse populations to subsequently crash (Fig. 4a). In aseries of measurements using magnetic transducers glued tothe mandibles of birds, the authors showed that the lower
mandible moves forward during preening (Rock Pigeon
preening at 1/4th actual speed, Rock Pigeon preening at
1/24th actual speed) (suppl 1). This forward motion, which
was remarkably fast, at up to 31 times per second, created ashearing force against the overhang that damaged the lice
(Fig. 4b-e). Without the maxillary overhang, birds were unable to generate this force. Additional experiments showedthat removal of the overhang had no impact on feeding efficiency, suggesting that the overhang is a specific adaptationfor ectoparasite control. Overhangs longer than a mean of
1.5mm broke significantly more often than shorter overhangs, further suggesting that stabilizing selection favors
overhangs of intermediate length. Considering the criticalFig. (3). Natural and experimentally induced variation in the bill overhang. Within the family Charadriidae, the Black-bellied Plover (Pluvialis squatarola) has a pronounced overhang (a), whereas the Black Oystercatcher (Haematopus bachmani) lacks an overhang (b). Within thespecies Western Scrub-Jay (Aphelocoma californica), populations living in scrub oak have a pronounced overhang (c), whereas those living
in pinyon pine have no overhang (d). Rock Pigeons (Columba livia) have a pronounced overhang (e), which Clayton et al. [125] trimmed
using a Dremel® rotary tool (f). Trimming is a harmless procedure, and the overhang regrows in 1-2 weeks. The results of trimming areshown in Fig. (4). Photos by C. Beittel.

48 The Open Ornithology Journal, 2010, Volume 3

a

* *
*
** ** *

600

Number of lice

500
400
300
200
100
0

Clayton et al.

Interestingly, a negative correlation between length of thebill overhang and ectoparasite abundance is also apparent
among populations within species. Populations of the Western Scrub-jay (Aphelocoma californica) have bills specialized for feeding in their respective habitats [126, 127].
Scrub-jays in oak habitat have hooked bills (Fig. 3c),whereas the bills of populations in pinyon habitat are pointed(Fig. 3d). Moyer et al. [128] quantified lice on 170 freshlycollected jays and found a significant relationship between
bill morphology and louse load. Although louse prevalence
was low, infested birds with pointed bills had significantly
more lice than infested birds with hooked bills. More recent
work using better methods of quantifying parasites further
suggests that lice also exert stabilizing selection on the billmorphology of jays (Fig. 5).
Grooming: Allopreening

0

4

8

12 16 20 24 28 32 36

Census week

b

c

0.5mm

d

e

Fig. (4). (a) Mean (± 1 SE) number of lice on 26 adult pigeons in
an experiment to test the impact of the bill overhang on preening
efficiency. The overhangs of all birds were trimmed for 17 weeks;
at week 18 (arrow), half the birds (orange triangles) were allowed
to regrow their overhangs, while the remaining half (blue squares)
continued to be trimmed weekly. Data were analyzed using a 2(treatment: trim, regrow) X 11 (post-treatment census) ANOVA
with repeated measures on the second factor (census). There weresignificant overall effects of treatment (P = 0.003) and census (P <0.0001), and a significant interaction (P < 0.0001). Birds allowed toregrow their overhangs had significantly fewer lice than trimmed
birds at each of the final eight censuses = weeks 22-36 (Protected t> 1.97, df = 240, *P < 0.001). (b) SEM of an undamaged louse(Campanulotes compar), compared to lice that have had most of
their legs removed (c), or been decapitated (d), or lacerated (e) bybirds with normal overhangs. Reprinted from Clayton et al. [125].

importance of the maxillary overhang for controlling lice,
Clayton et al. [125] concluded that the adaptive radiation ofbeak morphology in birds should be re-assessed with bothfeeding and preening in mind.

In addition to preening themselves, birds sometimes "allopreen" one another (Fig. 2b). Allopreening helps reduce
ectoparasites on the head and neck, which are impossible toself-preen. Allopreening is a widespread behavior observedin many species of birds [129]. It is most common between
courting and mated individuals, and between parents andtheir offspring. Harrison [129] argued that allopreening
serves mainly a social function, such as reinforcement of thepair bond, and is of little or no importance for ectoparasite
control. However, subsequent studies indicate a role for allopreening in parasite control [130-133]. Radford and Du Plessis [134] suggested a dual function for allopreening in theGreen Woodhoopoe (Phoeniculus purpureus). Allopreeningof the head and neck regions occurs at similar rates fordominant and subordinate individuals, suggesting a hygienic
function. However, allopreening of self-accessible body regions, such as the wings, back or breast, are influenced bygroup size and dominance status, suggesting a social function.
Among the most convincing demonstrations of the importance of allopreening for controlling parasites is Brooke’s[131] study of tick-infested Macaroni Penguins (Eudyptes
chrysolophus). Brooke reported that individual birds, which
could only self-preen, had two to three times more ticks thanpaired birds, which engaged in frequent allopreening. The
ticks were found mainly on the head and neck, suggestingthat the larger numbers on unpaired birds were due to thelack of allopreening, rather than inefficient self-preening. It
is important to keep in mind, however, that the author could
not control for possible covariates of tick load, such as genetic resistance. Such resistance, if present, might have contributed to the low tick loads of some individuals, as well as
to their ability to attract mates. Hence, inability to attract
mates could lead to a spurious inverse correlation between
tick load and allopreening. A more rigorous test of the roleof allopreening requires analysis of covariation between allopreening and parasite load [cf. 135] or - even better - experimental manipulation of allopreening and its impact on
ectoparasites.
Grooming: Scratching
Scratching with the feet is an important means of controlling ectoparasites on regions that cannot be self-preened,such as the head. Birds with a deformed or missing foot of-How Birds Combat Ectoparasites

The Open Ornithology Journal, 2000, Volume 3

Un-infested Scrub-jays
Infested Scrub-jays

Number of birds

a 14
10
6
2
0

0.5

1.0

1.5

2.0

2.5

Birds may use scratching to compensate for a lack ofother methods of ectoparasite control. The unpaired penguinsin Brooke’s [131] study spent significantly more timescratching than did paired individuals with access to allopreening. Scratching also appears to compensate for inefficient preening in species with unwieldy bills. Clayton and
Cotgreave [105] reported that long-billed species average
16.2% of their grooming time scratching, compared to 2.3%
in short-billed species. In a series of paired taxonomic comparisons, long-billed species scratched significantly morethan short-billed taxa. In another comparative study, Clayton
and Walther [124] investigated the relationship of relative
foot length and toenail flange width to the louse loads of
Peruvian birds, but neither feature was correlated with louse
species richness or abundance.
The efficiency of scratching for ectoparasite control may
be enhanced by the presence of a comb-like pectinate claw
on the middle toes of some birds (Fig. 6) [136-138]. But thepossible ectoparasite control function of this “louse comb”
has long been controversial [139]. Other possible functions
include a role in feeding [140], removal of stale powder
down from the plumage [141], or straightening of rictal bristles [137, 142]. To our knowledge, however, none of thesefunctional hypotheses, including ectoparasite control, hasever been tested. Even the distribution of the pectinate claw
among bird taxa has not been carefully documented.

Overhang length (mm)b 625
Number of lice

49

125

25

One of us (BRM) recently examined 1421 study skins forpectinate claws in the collection of the Division of Birds,
National Museum of Natural History, Washington DC. At

5

0
0

0.5

1.0

1.5

2.0

Overhang length (mm)Fig. (5). Overhang lengths of Western Scrub-jays, in relation toectoparasite abundance. Jay specimens (n = 57) were collected in
2002-03 at five localities in Utah and Nevada (Utah: Oquirrh
Mountains, n = 8; Lookout Pass, n = 4; La Sal National Forest, n=
6, Stansbury Mountains, n = 2; Nevada: vicinity of Austin, n = 37).
Bills were measured with calipers and the number of lice on eachbird was determined using the body washing method [41]. Panel (a)shows the distribution of overhang length (mean of three measurements per bird) across all 57 birds, as well as across the 20 birds(35%) that were infested with lice. Factors other than preening,such as ambient humidity, are known to influence the prevalence offeather lice on Western Scrub-jays [38]. Nevertheless, of the twenty
birds that had lice, those with intermediate overhangs had the fewest lice (Fig. 5b; quadratic regression R2 = 0.30, P< 0.05). This
intriguing relationship suggests that lice exert stabilizing selection
for intermediate overhang length, presumably because intermediate
overhangs are best at controlling lice (cf. Clayton et al. [125]). An
experimental test of this hypothesis is needed.

ten have large numbers of ectoparasites (and their eggs) concentrated around the head and neck [112]. The obvious explanation is that, although birds can preen themselves while
standing on one leg, they cannot scratch themselves. Although the precise impact of scratching on ectoparasites has
not been measured, scratching is known to kill or damage
fleas on domestic chickens (Suter cited in Marshall [5]).

Fig. (6). Variation in the structure of the pectinate claw, ranging
from (a) the coarsely serrated claw of the American Dipper (Cinclus mexicanus) to (b) the finely serrated claw of the Magnificent
Frigatebird (Fregata magnificens). Photos by C. Beittel.

50 The Open Ornithology Journal, 2010, Volume 3

least one representative species from each of 118 (82%) of
the 144 bird families recognized by Sibley and Ahlquist[143] was selected (haphazardly), and all of the claws of one
male and one female specimen were examined under 6x
magnification. Skins of species noted in the literature to havea pectinate claw were also examined [138, 144-146] . A
pectinate claw was considered to be present if any portion of
any claw was serrate. If a pectinate claw was detected in agiven family during the initial survey, at least one representative species from every available genus in this family was
subsequently examined to assess within family variation (5males and 5 females were examined when possible).
Most birds lack a pectinate claw. Only 17 of 118 families
contained individuals with pectinate claws (Table I), and of
the Passeriformes, only dippers (Cinclidae) had them (Fig6a). The claw has probably evolved repeatedly, given its
scattered distribution across bird families. It is also variable
within families; only a minority of genera possess it withinmost of the 17 families. For example, a pectinate claw ispresent in one of four genera of Heliornithidae, two of 12
genera of Scolopacidae, four of six genera of Glareolidae,
four of 16 genera of Laridae, and one of ten genera of Threskiornithidae (Table I).
In addition to within-family variation, we discovered
within-species variation in pectinate claws. In 15 species
some individuals had the claw, while others lacked it (TableI). This intraspecific variation did not appear to be related tothe sex, geographic distribution, or season in which the bird
was collected. We did not examine variation in relation to
the bird’s age, but this would also be interesting to explore.
The structure of the pectinate claw varied considerably
among taxa. Pectinations ranged from scalloping, as in theAmerican Dipper (Cinclus mexicanus) (Fig. 6a), to fine serrations, as in the Magnificent Frigatebird (Fregata magnificens) (Fig. 6b).
Serrations on some pectinate claws are somewhat similar
to the teeth of combs designed to remove human head lice.
Clay [138] believed that species with pectinate claws might
be more efficient at removing lice from the head by scratching. She predicted that birds with pectinate claws would beparasitized by fewer species of head lice than those species
without pectinate claws. We tested Clay’s hypothesis using
an analysis that compared the species richness of head lice
on birds with pectinate claws to that of sister taxa without
pectinate claws. We selected 14 phylogenetically independent comparisons of bird species with and without pectinate
claws. We then asked a louse taxonomist colleague to tallythe number of species of head lice known from each speciesof bird using Price et al. [63]. Because louse species richness
is influenced by sampling effort, we corrected for this factor
as described in Walther et al. [147].
Our analysis revealed no significant difference in thenumber of species of head lice on birds with and without
claws (Wilcoxon signed-rank test on residuals, T = 24.5, P =0.15). In eight of the 14 comparisons, the species with thepectinate claw had fewer (residual) species of head lice, andin five comparisons the reverse was true (one tie). In retrospect, it is unclear why one should necessarily expect a negative correlation between the pectinate claw and louse species
richness, or a positive correlation. If richness decreases onbirds that evolve pectinate claws, then selection maintaining

Clayton et al.

the claw would be relaxed, leading to disappearance of theclaw. Hence, this comparative analysis is perhaps not themost convincing test of the hypothesis that pectinate claws
help to control ectoparasites.
We have also investigated the relationship between louse
abundance and pectinate claw morphology within species.
We used 24 road-killed Barn Owls (Tyto alba) salvaged bycolleagues along highways in southern Idaho. We counted
the number of teeth on the pectinate claw of each foot (Fig7a), and we measured the length and width of each claw's
flange. The number of lice on each owl was quantified using“body washing” [41]. Fourteen (58%) of the owls had lice,
but one was missing the pectinate claw on one foot. Since we
could not be sure whether this was natural, or a consequenceof post-mortem road damage, this individual bird was excluded from the analysis.
There was no significant difference in the number ofteeth or the length or width of the flange, between infested
and uninfested owls (n = 23, df = 1, P > 0.27). Similarly,
there was no significant relationship between the abundanceof lice on infested owls, and the mean number of teeth perclaw (Fig. 7c). Finally, there was no relationship between
louse abundance and mean claw length (n = 13, R2 = 0.006,
P = 0.81), or width (n = 13, R2 = 0.02, P = 0.63). The resultsof this study indicate that natural variation in the size andshape of the pectinate claw does not correlate with louse
prevalence or intensity, at least in the case of Barn Owls
from southern Idaho.
In summary, these comparative and correlational studies
indicate that the pectinate claw plays no role in parasite control. However, a more definitive test would be to conduct anexperiment in which parasite populations are monitored on
birds with normal claws, versus birds from which the pectinations have been removed, perhaps by filing them off.
There are several common species that could be used for thisexperiment, such as Cattle Egrets (Bubulcus ibis) (Table I).
Bathing
Another form of maintenance behavior practiced by mostbirds is bathing in water.
Rothschild and Clay [4] wrote, "Bathing in water anddust and the subsequent preening helps the bird to rid itself
of parasites." However, we are not aware of any evidence
suggesting that water bathing has a detrimental effect on
ectoparasites. If anything, it might be expected to have apositive effect, given that high humidity favors ectoparasites
ranging from feather lice [37] to bacteria [70]. It is conceivable that substances detrimental to ectoparasites might bedissolved in some water sources, but we know of no support
for this speculation.
Dusting
Members of at least a dozen orders of birds are known toengage in dusting (Table II), during which fine dirt or sandis ruffled through the plumage [148-150] (Fig. 8). Dusting
appears to remove excess feather oil that can cause mattingof plumage [151-153]. It is also thought to help control ectoparasites. Several mechanisms for such control have been
proposed, including (1) reducing feather lipids upon whichsome ectoparasites feed [152]; (2) directly dislodging para

How Birds Combat Ectoparasites

Table I.

The Open Ornithology Journal, 2000, Volume 351

Occurrence of Pectinate Claws Among 1421 Study Skins of Birds Representing 278 Species in 250 Genera (118 Families,
23 Orders). Species with Pectinate Claws are in Boldface. Presence (+) or Absence (-) of a Maxillary Overhang on the Billis also Indicated in the Final Column; Lack of a Symbol Means the Species was not Checked for an Overhang. Classification and Nomenclature Follow Sibley and Monroe [252]Higher Taxa

Bird Species# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Struthioniformes
Struthionidae

Ostrich, Struthio camelus

0/2 (0)+Rheidae

Greater Rhea, Rhea americana

0/2 (0)+Casuariidae

Dwarf Cassowary, Casuarius bennetti

0/2 (0)+Emu, Dromaius novaehollandiae

0/2 (0)+Brown Kiwi, Apteryx australis

0/2 (0)+Variegated Tinamou, Crypturellus variegatus

0/2 (0)+Elegant Crested-Tinamou, Eudromia elegans

0/2 (0)Grey-headed Chachalaca, Ortalis cinereiceps

0/2 (0)Blue-knobbed Curassow, Crax alberti

0/2 (0)Brown-collared Brush-turkey, Talegalla jobiensis

0/2 (0)

Green Peafowl, Pavo muticus

0/2 (0)Spruce Grouse, Dendragapus canadensis

0/2 (0)Ruffed Grouse, Bonasa umbellus

0/2 (0)Wild Turkey, Meleagris gallopavo

0/2 (0)+Numididae

Crested Guineafowl, Guttera pucherani

0/2 (0)+

Odontophoridae

Northern Bobwhite, Colinus virginianus

0/2 (0)+Anhimidae

Southern Screamer, Chauna torquata

0/2 (0)+Anatidae

Emperor Goose, Anser canagica

0/2 (0)+Common Teal, Anas crecca

0/2 (0)

Barred Buttonquail, Turnix suscitator

0/2 (0)+Indicatoridae

Lesser Honeyguide, Indicator minor

0/2 (0)+

PicidaeBlack-cheeked Woodpecker, Melanerpes pucherani

0/2 (0)Greater Flameback, Chrysocolaptes lucidus

0/2 (0)-

Lybiidae

Green Barbet, Stactolaema olivacea

0/2 (0)+Ramphastidae

Yellow-eared Toucanet, Selenidera spectabilis

0/2 (0)+

Apterygidae
Tinamiformes
Tinamiidae

Craciformes
Cracidae

Megapodiidae++

Galliformes
Phasianidae+

Anseriformes

Turniciformes
Turnicidae
Piciformes

Galbuliformes

52 The Open Ornithology Journal, 2010, Volume 3

Clayton et al.
Table 1. Contd….

Higher Taxa

Bird Species# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Galbulidae

Great Jacamar, Jacamerops aurea

0/2 (0)+

Bucconidae

White-whiskered Puffbird, Malacoptila panamensis

0/2 (0)+Helmeted Hornbill, Buceros vigil

0/2 (0)White-crowned Hornbill, Aceros comatus

0/2 (0)+UpupidaeEurasian Hoopoe, Upupa epops

0/2 (0)+Phoeniculidae

White-headed Woodhoopoe, Phoeniculus bollei

0/2 (0)+

Diard’s Trogon, Harpactes diardii

0/2 (0)+

Coraciidae

Purple-winged Roller, Coracias temminckii

0/2 (0)+

Leptosomidae

Courol, Leptosomus discolor

0/2 (0)+

Momotidae

Turquoise-browed Motmot, Eumomota superciliosa

0/2 (0)+Todidae

Broad-billed Tody, Todus subulatus

0/2 (0)+Dacelonidae

Laughing Kookaburra, Dacelo novaeguineae

0/2 (0)+

Cerylidae

Belted Kingfisher, Megaceryle alcyon

0/2 (0)+

Meropidae

Madagascar Bee-eater, Merops superciliosus

0/2 (0)+Blue-naped Mousebird, Urocolius macrourus

0/2 (0)+

Cuculidae

Large Hawk-cuckoo, Cuculus sparverioides

0/2 (0)+

Opisthocomidae

Hoatzin, Opisthocomus hoazin

0/2 (0)+Common Kaka, Nestor meridionalis

0/2 (0)+

ApodidaeWhite-throated Swift, Aeronautes saxatalis

0/2 (0)+Hemiprocnidae

Grey-rumped Treeswift, Hemiprocne longipennis

0/2 (0)+Black-hooded Sunbeam, Aglaeactis pamela

0/2 (0)-Knysna Turaco, Tauraco corythaix

0/2 (0)+Barn Owl, Tyto alba

12/12 (100)+Oriental Bay-Owl, Phodilus badius

3/3 (100)

Bucerotiformes
Bucerotidae

Upupiformes

Trogoniformes
Trogonidae
Coraciiformes

Coliiformes
Coliidae
Cuculiformes

Psittaciformes
Psittacidae
Apodiformes

Trochiliformes
Trochilidae
Musophagiformes
Musophagidae
Strigiformes
Tytonidae

How Birds Combat Ectoparasites

The Open Ornithology Journal, 2000, Volume 3

53

Table 1. Contd….
Higher Taxa

# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Eastern Screech-Owl, Otus asio

0/2 (0)+Great Horned Owl, Bubo virginianus

0/2 (0)

Short-eared Owl, Asio flammeus

0/10 (0)Aegothelidae

Australian Owlet-Nightjar, Aegotheles cristatus

0/2 (0)+

Podargidae

Tawny Frogmouth, Podargus strigoides

0/10 (0)+Batrachostomidae

Philippine Frogmouth, Batrachostomus septimus

0/2 (0)+

Steatornithidae

Oilbird, Steatornis caripensis

0/2 (0)+Nyctibiidae

Great Potoo, Nyctibius grandis

0/2 (0)+Eurostopodidae

Great Eared-Nightjar, Eurostopodus macrotis

10/10 (100)+Caprimulgidae

Short-tailed Nighthawk, Lurocalis semitorquatus

9/9 (100)

Common Nighthawk, Chordeiles minor

10/10 (100)Band-tailed Nighthawk, Nyctiprogne leucopyga

5/5 (100)

Nacunda Nighthawk, Podager nacunda

10/10 (100)Paraque, Nyctidromus albicollis

10/10 (100)Common Poorwill, Phalaenoptilus nuttallii

10/10 (100)Ocellated Poorwill, Nyctiphrynus ocellatus

2/2 (100)

Whip-Poor-Will, Caprimulgus vociferus

10/10 (100)Standard-winged Nightjar, Macrodipteryx longipennis

2/2 (100)

Rock Pigeon, Columba livia

0/2 (0)

Pied Imperial-Pigeon, Ducula bicolor

0/2 (0)+Eurypygidae

Sunbittern, Eurypyga helias

0/2 (0)+OtididaeBlack-bellied Bustard, Eupodotis melanogaster0/2 (0)+

GruidaeCommon Crane, Grus grus

0/2 (0)+

Heliornithidae

Limpkin, Aramus guarauna

0/2 (0)+African Finfoot, Podica senegalensis

4/4 (100)

Masked Finfoot, Heliopais personata

0/4 (0)Sungrebe, Heliornis fulica

0/10 (0)Psophiidae

Grey-winged Trumpeter, Psophia crepitans

0/2 (0)+

Cariamidae

Red-legged Seriema, Cariama cristata

0/2 (0)+

Rhynochetidae

Kagu, Rhynochetus jubata

0/2 (0)+RallidaeKing Rail, Rallus elegans

0/2 (0)+Giant Coot, Fulica gigantea

0/2 (0)Strigidae

Bird Species+

Columbiformes
Columbidae

Gruiformes+

54 The Open Ornithology Journal, 2010, Volume 3

Clayton et al.
Table 1. Contd….

Higher Taxa

# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Brown Roatelo, Mesitornis unicolor

0/2 (0)+

Pteroclidae

Lichtenstein’s Sandgrouse, Pterocles lichtensteinii

0/2 (0)+Thinocoridae

Grey-breasted Seedsnipe, Thinocorus orbignyianus

0/2 (0)+Pedionomidae

Plains-Wanderer, Pedionomus torquatus

0/2 (0)+Scolopacidae

Common Snipe, Gallinago gallinago

0/10 (0)Jack Snipe, Lymnocryptes minimus

0/10 (0)Black-tailed Godwit, Limosa limosa

10/12 (83)Long-billed Curlew, Numenius americanus

0/21 (0)Upland Sandpiper, Bartramia longicauda

0/10 (0)Greater Yellowlegs, Tringa melanoleuca

0/2 (0)Lesser Yellowlegs, Tringa flavipes

0/10 (0)Terek Sandpiper, Tringa cinerea

0/10 (0)Black Turnstone, Arenaria melanocephala

0/10 (0)Short-billed Dowitcher, Limnodromus griseus

0/11 (0)Surfbird, Aphriza virgata

11/17 (65)

Red Knot, Calidris canutus

0/10 (0)Ruff, Philomachus pugnax0/10 (0)Red-necked Phalarope, Phalaropus lobatus

0/10 (0)Rostratulidae

Greater Painted-Snipe, Rostratula benghalensis

0/2 (0)+

Jacanidae

Wattled Jacana, Jacana jacana

0/2 (0)+Chionididae

Snowy Sheathbill, Chionis alba

0/2 (0)+Burhinidae

Double-striped Thick-knee, Burhinus bistriatus

0/2 (0)+Beach Thick-knee, Burhinus giganteus

0/15 (0)Black Oystercatcher, Haematopus bachmani

0/2 (0)-American Avocet, Recurvirostra americana

0/2 (0)+

Killdeer, Charadrius vociferus

0/2 (0)

Northern Lapwing, Vanellus vanellus

0/14 (0)+Crab Plover, Dromas ardeola

7/10 (70)+

Crocodile-bird, Pluvianus aegyptius

0/4 (0)Three-banded Courser, Rhinoptilus cinctus

7/7 (100)Cream-colored Courser, Cursorius cursor

10/11 (91)

Indian Courser, Cursorius coromandelicus

2/2 (100)

Collared Pratincole, Glareola pratinicola

10/19 (53)Oriental Pratincole, Glareola maldivarum

10/12 (83)

Mesitornithidae

Bird Species

Ciconiiformes

Charadriidae

Glareolidae++

How Birds Combat Ectoparasites

The Open Ornithology Journal, 2000, Volume 3

55

Table 1. Contd….
Higher Taxa

Bird Species# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Australian Pratincole, Stiltia isabella

0/5 (0)South Polar Skua, Catharacta maccormicki

0/12 (0)Pomarine Jaeger, Stercorarius pomarinus

0/2 (0)Long-tailed Jaeger, Stercorarius longicaudus

0/10 (0)Black Skimmer, Rynchops niger

0/12 (0)-Laughing Gull, Larus atricilla

0/12 (0)+Sabine’s Gull, Xema sabini

0/10 (0)Gull-billed Tern, Sterna nilotica

0/10 (0)Caspian Tern, Sterna caspia

0/10 (0)Black-naped Tern, Sterna sumatrana

9/10 (0)Black Tern, Chlidonias niger

0/10 (0)Large-billed Tern, Phaetusa simplex

0/10 (0)Brown Noddy, Anous stolidus

16/20 (80)Black Noddy, Anous minutus

0/2 (0)Blue Noddy, Procelsterna cerulea

9/10 (90)Common White-Tern, Gygis alba

0/10 (0)Inca Tern, Larosterna inca

6/7 (86)

Dovekie, Alle alle

0/10 (0)Razorbill, Alca torda

0/2 (0)

Pigeon Guillemot, Cepphus columba

0/10 (0)Tufted Puffin, Fratercula cirrhata

0/2 (0)

Osprey, Pandion haliaetus

0/2 (0)+Mississippi Kite, Ictinia mississippiensis

0/2 (0)+

Cooper’s Hawk, Accipiter cooperii

0/2 (0)

Sagittariidae

Secretary-Bird, Sagittarius serpentarius

0/2 (0)+Falconidae

Crested Caracara, Polyborus plancus

0/2 (0)+American Kestrel, Falco sparverius

0/11 (0)White-tufted Grebe, Rollandia rolland

7/8 (88)

Australasian Grebe, Tachybaptus novaehollandiae

7/7 (100)

Least Grebe, Tachybaptus dominicus

10/10 (100)Pied-billed Grebe, Podilymbus podiceps

12/12 (100)Western Grebe, Aechmophorus occidentalis

12/12 (100)Red-tailed Tropicbird, Phaethon rubricauda

0/12 (0)White-tailed Tropicbird, Phaethon lepturus0/10 (0)Northern Gannet, Morus bassanus

9/9 (100)

LaridaeAccipitridae

Podicipedidae

Phaethontidae

Sulidae

+

+

+

+

+

56 The Open Ornithology Journal, 2010, Volume 3

Clayton et al.
Table 1. Contd….

Higher Taxa

Bird Species# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Masked Booby, Sula dactylatra

2/2 (100)

Brown Booby, Sula leucogaster11/11 (100)Anhinga, Anhinga anhinga

10/10 (100)Oriental Darter, Anhinga melanogaster2/2 (100)

Little Cormorant, Phalacrocorax niger

2/2 (100)

Brandt's Cormorant, Phalacrocorax penicillatus

10/10 (100)Neotropic Cormorant, Phalacrocorax brasilianus

2/2 (100)

Double-crested Cormorant, Phalacrocorax auritus

10/10 (100)Great Blue Heron, Ardea herodias

12/12 (100)Cattle Egret, Bubulcus ibis

13/13 (100)Chinese Pond-Heron, Ardeola bacchus

10/10 (100)Yellow-crowned Night-Heron, Nyctanassa violacea

10/10 (100)Black-crowned Night-Heron, Nycticorax nycticorax

10/10 (100)Boat-billed Heron, Cochlearius cochlearius

10/10 (100)Bare-throated Tiger-Heron, Tigrisoma mexicanum

10/10 (100)White-crested Bittern, Tigriornis leucolophus

2/2 (100)

Zigzag Heron, Zebrilus undulatus

1/1 (100)

Stripe-backed Bittern, Ixobrychus involucris

4/4 (100)

Great Bittern, Botaurus stellaris

8/8 (100)

Scopidae

Hamerkop, Scopus umbretta

10/10 (100)+Phoenicopteridae

Greater Flamingo, Phoenicopterus ruber

0/12 (0)+Threskiornithidae

White Ibis, Eudocimus albus

0/10 (0)White-faced Ibis, Plegadis chihi

12/12 (100)Plumbeous Ibis, Theristicus caerulescens

0/5 (0)Buff-necked Ibis, Theristicus caudatus

0/9 (0)

Green Ibis, Mesembrinibis cayennensis

0/10 (0)Hadada Ibis, Bostrychia hagedash

0/12 (0)Wattled Ibis, Bostrychia carunculata

0/5 (0)Spot-breasted Ibis, Bostrychia rara

0/1 (0)

Bald Ibis, Geronticus calvus

0/2 (0)

Sacred Ibis, Threskiornis aethiopicus

0/10 (0)Straw-necked Ibis, Threskiornis spinicollis

0/5 (0)White-shouldered Ibis, Pseudibis davisoni

0/13 (0)Giant Ibis, Pseudibis gigantea

0/4 (0)

Crested Ibis, Nipponia nippon

0/6 (0)Anhingidae

Phalacrocoracidae

Ardeidae

-

+

-

+

How Birds Combat Ectoparasites

The Open Ornithology Journal, 2000, Volume 3

57

Table 1. Contd….
Higher Taxa

Bird Species# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Roseate Spoonbill, Ajaia ajaja

0/12 (0)Shoebill, Balaeniceps rex

2/2 (100)

American White Pelican, Pelecanus erythrorhynchos

3/11 (27)

Brown Pelican, Pelecanus occidentalis

11/11 (100)+Turkey Vulture, Cathartes aura

0/2 (0)+Andean Condor, Vultur gryphus

0/2 (0)White Stork, Ciconia ciconia

0/9 (0)Lesser Adjutant, Leptoptilos javanicus

0/2 (0)Magnificent Frigatebird, Fregata magnificens

12/12 (100)Great Frigatebird, Fregata minor

10/10 (100)Gentoo Penguin, Pygoscelis papua

0/12 (0)Jackass Penguin, Spheniscus demersus

0/2 (0)Red-throated Loon, Gavia stellata

0/7 (0)Arctic Loon, Gavia arctica

0/6 (0)Common Loon, Gavia immer

0/12 (0)Yellow-billed Loon, Gavia adamsii

0/4 (0)Southern Fulmar, Fulmarus glacialoides

0/2 (0)Juan Fernandez Petrel, Pterodroma externa

0/2 (0)Common Diving-Petrel, Pelecanoides urinatrix

0/2 (0)+Black-footed Albatross, Diomedea nigripes

0/2 (0)+Light-mantled Albatross, Phoebetria palpebrata

0/2 (0)

Leach’s Storm-Petrel, Oceanodroma leucorhoa

0/2 (0)+Acanthisittidae

Rifleman, Acanthisitta chloris

0/2 (0)+

Pittidae

Ivory-breasted Pitta, Pitta maxima

0/2 (0)+EurylaimidaeDusky Broadbill, Corydon sumatranus

0/2 (0)+Philepittidae

Velvet Asity, Philepitta castanea

0/2 (0)+Tyrannidae

Highland Elaenia, Elaenia obscura

0/2 (0)+Black-necked Red-Cotinga, Phoenicircus nigricollis

0/2 (0)+

Rufous-tailed Plant-cutter, Phytotoma rara

0/2 (0)+Sharpbill, Oxyruncus cristatus

0/2 (0)+Long-tailed Manakin, Chiroxiphia linearis

0/2 (0)+Thamnophilidae

Black-backed Antshrike, Sakesphorus melanonotus

0/2 (0)+

Furnariidae

Azara’s Spinetail, Synallaxis azarae

0/2 (0)+Long-billed Woodcreeper, Nasica longirostris

0/2 (0)+Pelecanidae

Ciconiidae

Fregatidae

Spheniscidae

GaviidaeProcellariidae

+

+

+

+

+

+

Passeriformes

58 The Open Ornithology Journal, 2010, Volume 3

Clayton et al.
Table 1. Contd….

Higher Taxa

Bird Species# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Rhinocryptidae

Moustached Turca, Pteroptochos megapodius

0/2 (0)+

Climacteridae

White-throated Treecreeper, Cormobates leucophaeus

0/2 (0)+Menuridae

Superb Lyrebird, Menura novaehollandiae

0/2 (0)+

Rufous Scrub-bird, Atrichornis rufescens

0/2 (0)+Ptilonorhynchidae

Green Catbird, Ailuroedus crassirostris

0/2 (0)+Meliphagidae

Wattled Honeyeater, Foulehaio carunculata

0/2 (0)+

Irenidae

Golden-fronted Leafbird, Chloropsis aurifrons

0/2 (0)+Vireonidae

Yellow-throated Vireo, Vireo flavifrons

0/2 (0)+

Corvidae

Daurian Jackdaw, Corvus dauuricus

0/2 (0)+

Raggiana Bird-of-Paradise, Paradisaea raggiana

0/2 (0)+Grey Currawong, Strepera versicolor

0/2 (0)+Dusky Wood-Swallow, Artamus cyanopterus

0/2 (0)+Black-hooded Oriole, Oriolus xanthornus

0/2 (0)+Bar-bellied Cuckoo-Shrike, Coracina striata

0/2 (0)+

Square-tailed Drongo, Dicrurus ludwigii

0/2 (0)+Magpie-Lark, Grallina cyanoleuca

0/2 (0)+White Helmetshrike, Prionops plumatus

0/2 (0)+

Rufous Vanga, Schetba rufa

0/2 (0)+

Coral-billed Nuthatch, Hypositta corallirostris

0/2 (0)+Callaeatidae

Kokako, Callaeas cinerea

0/2 (0)+Bombycillidae

Palmchat, Dulus dominicus

0/2 (0)+Grey Silky-Flycatcher, Ptilogonys cinereus

0/2 (0)+

Cedar Waxwing, Bombycilla cedrorum

0/2 (0)+White-throated Dipper, Cinclus cinclus

3/15 (20)Brown Dipper, Cinclus pallasii

3/22 (14)American Dipper, Cinclus mexicanus

10/20 (50)

Swainson’s Thrush, Catharus ustulatus

0/20 (0)White-bellied Short-wing, Brachypteryx major

0/2 (0)+Red-winged Starling, Onychognathus morio

0/2 (0)+Grey Catbird, Dumetella carolinensis

0/2 (0)+Wood Nuthatch, Sitta europaea

0/2 (0)+Wallcreeper, Tichodroma muraria

0/2 (0)+Eurasian Tree-Creeper, Certhia familiaris

0/2 (0)+Cactus Wren, Campylorhynchus brunneicapillus

0/2 (0)+African Penduline-Tit, Anthoscopus caroli

0/2 (0)+Cinclidae

Muscicapidae

Sturnidae

Sittidae

Certhiidae

Paridae+How Birds Combat Ectoparasites

The Open Ornithology Journal, 2000, Volume 3

59

Table 1. Contd….
Higher Taxa

# With Claw/

Bill Overhang# Examined (%)

Present (+), Absent (-), or
Unexamined ( )Carolina Chickadee, Parus carolinensis

0/2 (0)+Aegithalidae

Bushtit, Psaltriparus minimus

0/2 (0)+

Hirundinidae

Caribbean Martin, Progne dominicensis

0/2 (0)+Pycnonotidae

Red-whiskered Bulbul, Pycnonotus jocosus

0/2 (0)+

Zosteropidae

White-breasted White-eye, Zosterops abyssinicus

0/2 (0)+Sylviidae

Gray’s Warbler, Locustella fasciolata

0/2 (0)+Ferruginous Babbler, Trichastoma bicolor

0/2 (0)+Brown Parrotbill, Paradoxornis unicolor

0/2 (0)+

Stripe-sided Rhabdornis, Rhabdornis mysticalis

0/2 (0)+

Wrentit, Chamaea fasciata

0/2 (0)+

Alaudidae

Austral-Asian Lark, Mirafra javanica

0/2 (0)+

Nectariniidae

Yellow-sided Flowerpecker, Dicaeum aureolimbatum

0/2 (0)+Purple-throated Sunbird, Nectarinia sperata

0/2 (0)+Russet Sparrow, Passer rutilans

0/2 (0)+

Yellow Wagtail, Motacilla flava

0/2 (0)+

Alpine Accentor, Prunella collaris

0/2 (0)+White-breasted Negrofinch, Nigrita fusconota

0/2 (0)+Iiwi, Vestiaria coccinea

0/2 (0)+

Nashville Warbler, Vermivora ruficapilla

0/2 (0)+

Grass-green Tanager, Chlorornis riefferii

0/2 (0)+

Swallow Tanager, Tersina viridis

0/2 (0)+Grey-bellied Flower-piercer, Diglossa carbonaria

0/2 (0)+Rose-breasted Grosbeak, Pheucticus ludovicianus

0/2 (0)+

Audubon’s Oriole, Icterus graduacauda

0/2 (0)+

Passeridae

Fringillidae

Bird Species

sites [154, 155]; (3) plugging parasite spiracles (breathing
pores), leading to poor respiration; and (4) abrading the cuticle, leading to desiccation [132,149]. Desiccation is an intriguing possibility, given that inert dusts, such as volcanicash, are known to kill insects by abrading their cuticles [156,157]. Surprisingly, however, no rigorous test of this hypothesis has been conducted. Indeed, to our knowledge, nodirect test of the impact of dusting behavior on ectoparasites
has ever been performed. Such a study is feasible because
many birds dust readily in captivity [153, 158-161]. It should
be possible to "seed" parasite-free birds with identical numbers of parasites, such as feather lice, and then provide experimental birds with containers of dust. It might even be
possible elicit dusting behavior in control birds by providingthem a substance that is known to be harmless to ectoparasites.
Sunning
At least 50 families of birds are known to adopt stereotyped
postures and expose themselves to solar radiation, which is

known as “sunning” [162] (Fig. 9). Sunning is thought tocontrol ectoparasites, either by killing them directly or byincreasing their vulnerability to preening as they try to escape from the heat [163]. Sunning has intriguing parallels to“behavioral fever,” which is when ectothermic animals exploit warm microclimates to combat parasites [164-166]. For
example, in response to bacterial infections, Desert Iguanas(Dipsosaurus dorsalis) move to warm microclimates andgenerate a 2˚C fever, which increases their survival [167].
Goldfish (Carassius auratus) increase their survival in theface of bacterial infection by frequenting warm water, which
elevates their body temperature [168].
In warm environments many birds sun to the point ofapparent hyperthermia [163, 169-172]. Some birds sun when
it is hottest outside, not when it is coolest, suggesting thatsuch sunning has little or nothing to do with conserving body
heat. For example, Black Noddies (Anous minutus) in tropical Australia sun most frequently during periods of hightemperature rather than low temperature [163], and several
species of swallows sun only on hot summer days [172 -60 The Open Ornithology Journal, 2010, Volume 3

Clayton et al.

Table II.

Examples of Birds Known to Dust; from Moyer and
Clayton [22]STRUTHIONIFORMESSTRIGIFORMESSTRUTHIONIDAESTRIGIDAE

Ostrich (Struthio)

Owl

RHEIFORMESCAPRIMULGIFORMESRHEIDAECAPRIMULGIDAE
Rhea (Rhea)

Nightjar

FALCONIFORMESCOLIIFORMESACCIPITRIDAE

COLIIDAE

Hawk
FALCONIDAE
FalconMousebird
CORACIIFORMESMOMOTIDAEGALLIFORMESPHASIANIDAE

MotmotMEROPIDAE

Grouse (Lagopus)
Bobwhite (Colinus)

Bee-eater
CORACIIDAE

Fowl (Gallus)
Quail (Coturnix)

RollerUPUPIDAE

Partridge (Alectoris)
Pheasant (Chrysolophus, Phasianus)

HoopoeBUCEROTIDAEGRUIFORMESTURNICIDAE
Buttonquail

Hornbill
PASSERIFORMESALAUDIDAECARIAMIDAE
Seriema

Lark
TROGLODYTIDAE

OTIDIDAE

Wren
Bustard

CHARADRIIFORMESTHINOCORIDAE
Seedsnipe

Fig. (7). Barn Owls (Tyto alba) have a pectinate claw on their middle toe (a, photo by S. Bush), which is used in scratching (b, photoby Mike Read, naturepl.com). One adaptive function of this claw
may be to remove ectoparasites. We studied natural variation inlouse load and pectinate claw morphology of Barn Owls fromSouthern Idaho. (c) The relationship between the number of lice
and the mean number of teeth per claw is not significant (n = 13, R2= 0.01, P = 0.72).

COLUMBIFORMESCOLUMBIDAE
Dove
PTEROCLIDIDAE
Sandgrouse

TIMALIIDAE
Wrentit (Chamaea)
EMBERIZIDAE
Sparrow (Spizella, Pooecetes)
ICTERIDAE
Grackle (Quiscalus)
PLOCEIDAE
Sparrow (Passer, Petronia, Montifringilla)
GRALLINIDAE175]. Both noddies and swallows pant during these sunning
episodes, indicating heat stress.

Chough (Corcorax)

How Birds Combat Ectoparasites

The Open Ornithology Journal, 2000, Volume 361

Fig. (8). Southern Ground-hornbill (Bucorvus leadbeateri) dusting itself. Photo by T. Laman (naturepl.com).

Fig. (9). White-rumped Shama (Copsychus malabaricus) sunning itself. Photo by Michael Luckett (fotolia.com).

Two lines of evidence are consistent with the hypothesisthat sunning helps control ectoparasites. Blem and Blem[172] compared the rate of sunning in Violet-green Swallows(Tachycinete thalassina); experimentals were fumigated toremove ectoparasites, while controls were not. Fumigatedbirds sunned less frequently than controls [172], suggestingthat the motivation to sun decreases with a reduction in ectoparasite load. Moyer and Wagenbach [163] exposed lice,
placed on model Black Noddy wings, to sun and shade. The
duration of exposure was typical of those sunning bouts, andthe temperature of the model wings did not exceed that of
the wings of actual sunning noddies (temperature was measured from a distance with an infrared thermometer). Significantly more lice died in the sun than in the shade.
Although this work suggests that one adaptive functionof sunning is ectoparasite control, additional research isneeded to determine exactly how effective sunning is forcontrolling different parasites, and under different conditions. For example, it would be interesting to explore
whether sunning by birds with dark plumage is more effec-

62 The Open Ornithology Journal, 2010, Volume 3tive than sunning by birds with light plumage. Preliminary
work by one of us (BRM) indicates that dark feathers heat up
more rapidly, and to a higher temperature, than white feathers when exposed to the sun. Furthermore, Rock Pigeon
wing lice abandon interbarb refuges of dark feathers sooner
than those on white feathers when exposed sunlight. It is
tempting to speculate that one cost associated with the evolution of light colored plumage might be that light coloredbirds have more difficulty controlling ectoparasites by sunning.
Anointing
Another hypothesized defense against ectoparasites isanointing behavior, during which birds and mammals"...apply scent-laden materials to their integument" [25]. A
particularly intriguing form of anointing is "anting" behavior, during which birds crush and smear ants on their feathers(active anting), or allow ants to crawl through the plumage(passive anting) [176-181] (Fig. 10). Anting has been re-

Clayton et al.

ported in over 200 bird species, most of them Passeriformes[24, 182, 181]. The fact that birds ant exclusively with antsthat secrete formic acid, or other pungent fluids, suggeststhat anting may kill or deter ectoparasites.
Among the most compelling observations suggesting arole of anting in parasite control is Dubinin's [183] accountof anting Meadow Pipits (Anthus pratensis) (cited in Kelso
and Nice, [179]). Dubinin observed four pipits grasping
Wood Ants (Formica rufa) in their bills and rubbing themthrough their plumage. He collected these birds shortly
thereafter and examined them along with several other pipits
that had not been seen anting. The wing feathers of theanting birds were splotched with liquid that Dubinin presumed to be formic acid. Feather mites (Pterodectes spp.) on
these birds were actively moving across the feathers, and alarge proportion of the mites in the moist regions of thefeathers were dead. In contrast, mites on the four non-anting
birds were positioned between the feather barbs and wereundisturbed. More than 25% (163 of 642) of live mites taken

Fig. (10). Jay (Garrulus glandarius) anting. Ants (arrows) crawling on the primaries. Photos by A. Cooper (naturepl.com).

How Birds Combat Ectoparasites

The Open Ornithology Journal, 2000, Volume 3from the anting birds died within 12 hr, compared with lessthan 1% (5 of 758) of those taken from the non-anting birds.
Dubinin’s observations are consistent with the hypothesisthat anting helps control ectoparasites. However, Dubinin's
work certainly does not represent a rigorous test of the hypothesis.

Ectoparasite abundance was quantified on all birds using
the visual examination method [41] both the day before fieldtrials started, and again three days after the conclusion of the
field trials. The three-day interval allowed birds time topreen dead or damaged ectoparasites, while allowing parasites time to return to normal plumage microhabitats prior to
the second visual census. All feather mites visible on eachprimary and secondary feather of each outstretched wing, as
well as mites on the tail feathers, were counted with the aidof a 2x magnifying headset. All of the mites were Pteronyssoides truncates. Lice were quantified by tallying only thoseobserved during timed visual counts of specific body regions, including the crown, face, gulum, breast, pectoral region, nape, back (60 s each), as well as the flank and rump
(30 s each). Four species of lice were observed: Menacanthus eurysternus, Myrsidea cucullaris, Brueelia nebulosa,and Sturnidoecus sturni. Parasite counts were done "blind" totreatment by using VicksTM Vaporub in the nostrils of theperson doing the parasite counts. A few birds escaped ordied over the course of the experiment, which left complete
data sets for 25 of the 32 birds (14 experimentals and 11 controls).
Despite the fact that experimental birds anted extensively
over the three day field trials, there was no significant impactof anting on mites (Fig. 11a), nor on lice (Fig. 11b). Since
the post-treatment census occurred three days after the final
day of formic acid exposure, there should have been ample
time for any effect of acid on parasites to occur. In vitro
studies show that formic acid kills more than 90% of ectoparasites within 15 minutes [177]. In addition to comparing the number of ectoparasites on birds, the condition of allof the lice was noted, as well as a haphazard sample of 25
mites on each wing of each of 14 birds (under magnification). All of the parasites appeared to be in good condition.

AntingControl

Number of mites

a 500
400
300
200
100
0

b

14
12

Number of lice

Clayton and Wolfe [181] provided a brief synopsis of theresults of a field experiment designed to test the impact ofanting by European Starlings (Sturnus vulgaris) on feather
mites and lice. The experiment was conducted using 32 wildcaught birds, half of which were placed in cages(0.8x0.8x0.9 m) directly over natural Wood Ant (Formicarufa) trails, while the other half (controls) were placed in
identical cages adjacent to ant trails ([184]; Bennett et al.
unpublished ms). The bottomless cages allowed birds directaccess to ants on the ground. The lower portions of the cages
were coated with FluonTM, a Teflon-coated liquid that dries
to a film ants cannot cross, thus preventing them fromswarming up the cage and disturbing the bird. Experimental
birds (over ant trails) were observed in frequent anting behavior over the course of the field trials, which lasted threedays (birds were removed from the field enclosures at night).
By the end of the field trials, experimental birds had plumage that smelled strongly of formic acid. In contrast, control
birds did not have access to ant trails and they seldom engaged in anting-like behavior. They did not smell of formic
acid at the end of the field trials.

63

10
8
6
4
2
0

Before Treatment

After Treatment

Fig. (11). Mean (± SE) number of (a) feather mites and (b) lice on
European Starlings (Sturnus vulgaris) before and after experimental
birds were allowed to engage in anting behavior. There was no
significant relationship between anting and either mite or louseloads.

These observations indicate that anting has little or no effecton mites or lice, at least on starlings. Interestingly, the number of mites and lice actually increased between the first andsecond visual censuses, presumably as a result of improvement on the part of the observer, and/or displacement of ectoparasites from refugia where they may have been hiding
prior to the initial census and field procedures. It would be
worthwhile repeating this experiment using birds that are
euthanized and washed after the experiment in order to obtain more accurate estimates of total ectoparasite abundance[41].
Ehrlich et al. [185] proposed that anting behavior helps
control harmful plumage bacteria or fungi. In a series of inhibition trials, Revis and Waller [186] tested polar and nonpolar ant secretions, as well as pure formic acid, for bactericidal and fungicidal effects. Although the formic acidstrongly inhibited all bacteria and fungal hyphae tested, concentrations of formic acid approximating those actuallyfound in the bodies of formicine ants did not have an effect.

64 The Open Ornithology Journal, 2010, Volume 3

Clayton et al.

There was also no detectable effect of hexane ant-chemical
extracts, nor ant suspensions in deionized water, on plumage
microbes. These results suggest that anting is unlikely tocontrol microbes. Nevertheless, an "in vivo" experiment,
analogous to the one with starlings described above, isneeded for a more definitive test.
Birds also anoint themselves with a bizarre list of otheritems, including millipedes [187, 188], caterpillars [189],
garlic snails [190], bombardier beetles [191], citrus fruits[192, 193, 194], walnut juice [195], flowers [196, 197], lawnchemicals [198] and even mothballs placed in gardens torepel vegetarian pests [199-201]. Many of these items reportedly have anti-parasite properties [201], but few carefultests have been carried out.
Clayton and Vernon [194] performed one such test. The
authors observed a Common Grackle (Quiscalus quiscula)anointing itself with half a lime fruit. The bird pecked at thefruit repeatedly, then preened itself while holding pieces oflime in its bill. The authors subsequently tested the effect oflime on pigeon lice in the lab. Although lime juice had noeffect, exposure to vapor from the lime rind rapidly killed
the lice. This result is not surprising, given that lime peelcontains D-limonene, a monoterpene present at high concentrations in the peel oil of many citrus fruits, and which is
known to be toxic to a wide variety of arthropods [194].
Nevertheless, the hypothesis that birds use citrus peel, or anyof the other substances listed above, as a means for actuallycontrolling their ectoparasites is still in need of in vivo testing. Experiments using parasitized captive birds engaging in
anointing behavior would be informative.

Fig. (12). Bearded vultures (Gypaetus barbatus) stain their plumage with soil rich in iron oxide; captive birds without access to such
soil have white underparts. Photo by Richard Bartz (commons.wikimedia.org).

Cosmetic behavior
At least 13 bird families are known to apply "cosmetic"
substances to their bodies [202]. The function of this cosmetic behavior is largely unknown, but some examples suggest that the behavior may help combat ectoparasites. For
example, Bearded Vultures (Gypaetus barbatus) stain theirplumage with soils that are rich in iron oxide Fig. (12), [203,204]. They either rub their plumage in dry red soil, or rub
damp red soil into their plumage following a bath. Vultures
spend as much as an hour applying the soil [204]. Captive
Bearded Vultures return to their nests following episodes ofsoil bathing and rub their newly stained feathers on eggs andoffspring [205]. Frey and Roth-Callies [203] [cited in Negro
et al. [204]] tested for an effect of iron oxide on lice, butthere was no significant difference in the survival of lice
exposed to a suspension containing iron oxide vs. water controls. Arlettaz et al. [205] argued that, since Bearded Vultures are often the last species to feed upon carcasses, they
may also be exposed to dangerous quantities of bacteria left
behind by earlier scavengers. The oxidative properties iniron oxide rich soils may reduce the negative effects of suchbacteria on egg development and nestling growth [205].
However, experimental tests are needed to investigate theeffects of iron oxides on bacterial strains.

any effect on ectoparasites has not been tested. Other speciesof birds, such as Cinnamon Bitterns (Ixobrychus cinnamomeus) and Night Herons (Nycticorax nycticorax), apply
powder down - specialized feathers that degrade into a powder - to their head and neck regions [207, 208]. The powder
down alters the color of these regions, suggesting an intraspecific signaling function. However, since these are also theareas that the bird cannot reach with its bill to preen, it isconceivable that the application of substances to these regions could also help deter parasites. No test of this hypothesis has been conducted.

In a recent review of cosmetic coloration, Delhey andcolleagues [202] describe two other kinds of cosmetic behavior that might deter ectoparasites. Shortly before breeding,the Japanese Crested Ibis (Nipponia nippon) secretes a black
substance from the skin of its head and neck, which is thenpreened into the plumage [206]; whether this substance has

Parasite transmission is often more efficient in dense hostpopulations [210]. For this reason, antisocial behavior, suchas territoriality, may provide benefits in terms of defense
against ectoparasites [211]. Similarly, in colonial species,
nesting in smaller colonies can help control ectoparasites
because parasite load is proportional to colony size [212].

NEST MAINTENANCE BEHAVIOR
In addition to combating ectoparasites on their bodies,birds must defend themselves from parasites in their nests.
Parasites such as fleas, flies, true bugs, and some mites
spend portions of their life cycle in the nest material andmake brief forays onto nestlings and parents to feed [5]. It is
not uncommon for such parasites to kill nestlings or fledglings [45, 209]. Birds have several kinds of nest maintenancebehavior that may deter ectoparasites.
Territoriality and Colony SizeHow Birds Combat Ectoparasites

Nest Site Avoidance
The most effective defense against nest parasites may be
to simply avoid them in the first place. A number of studies
have shown that birds can detect and avoid nesting (androosting) sites containing ectoparasites [24, 212-221]. For
example, Oppliger et al. [214] experimentally investigatedthe effects of the hematophagous Hen Flea (Ceratophyllus
gallinae) on nest-site choice in the Great Tit (Parus major).
When offered a choice between adjacent nest boxes, one
flea-infested and one flea-free, significantly more Great Tits
chose parasite-free boxes.
Cliff Swallows (Hirundo pyrrhonota) show a similar
preference for uninfested nests. Brown and Brown [212]noted that during the early spring, overwintering fleas (Ceratophyllus celsus) and Swallow Bugs (Oeciacus vicarius)congregate in plain view at the entrances of old swallow
nests. This location is a good position from which to infest
swallows that enter the nest, or even swallows that come too
close to inspect the nest opening, allowing the fleas to leap
onto such birds. When they return from the wintering
grounds, Cliff Swallows often hover a few centimeters infront of old nests, rather than entering them. This behavior
appears to allow the birds to safely inspect the nest opening
for ectoparasites [212].
Another way in which birds can avoid ectoparasites is bychoosing to breed when fewer ectoparasites are present atnest sites. For example, Great Tits delay reproduction tominimize infestations by Hen Fleas [222], which - like swallow fleas - overwinter in the nest cavity. If a host does not
use the cavity, the fleas emigrate [223]. Hence, by delaying
reproduction, birds can reduce exposure to fleas. In an experimental test of this delayed-reproduction hypothesis, Oppliger et al. [214] found that Great Tits whose nest boxes
were infested with fleas started laying eggs 11 days later
than birds occupying uninfested nest boxes.
Nest Sanitation
In some cases, birds are known to engage in nest "sanitation" behavior [24]. Female Great Tits and Blue Tits (Parus
caeruleus) exhibit this behavior, which Christe et al. [224]described as "a period of active search with the head dug into
the nest material." It is unclear whether this kills or simply
disperses ectoparasites, but female Great Tits devote significantly more time to sanitation in flea-infested nests than in
uninfested nests [224]. Similarly, female Blue Tits spend
more time in sanitation of nests infested with blowfly (Protocalliphora) larvae [225] or fleas [226] than in uninfested
nests [225]. Another form of nest sanitation is to clean out
nests that have been used before; for example, male House
Wrens (Troglodytes aedon) remove old nest material fromtheir nest boxes prior to each reproductive bout. Pacejka etal. [227] showed that this behavior effectively reduces theabundance of mites (Dermanyssus) in the nest.
Nest Fumigation
An interesting purported adaptation for controlling ectoparasites in nests is the use of aromatic vegetation to fumigate the nest [24, 25, 73, 181, 228]. Clark and Mason [229]
showed that European Starlings (Sturnus vulgaris) selectspecies of plants that contain volatile chemicals with antibac-

The Open Ornithology Journal, 2000, Volume 365

terial and insecticidal properties. The authors found that thehatching success of lice (Menacanthus sp.) and the growth ofseveral strains of bacteria (Streptococcus aurealis, Staphylococcus epidermis, and Pseudomonas aeruginosa) were significantly reduced when exposed to volatiles from plants
preferred by starlings, compared to a random sample ofnearby vegetation. A subsequent study showed that emergence of a mite (Ornithonyssus sylviarum) was significantly
decreased when wild carrot (Daucus carota) or fleabane(Erigeron philadelphicus) was added to the nesting material[230].
A recent study of Bonelli’s Eagles (Hieraaetus fasciatus)
showed that nests with higher percentages of pine greenery
had fewer blow fly larvae (Protocalliphora) and higher host
breeding success [231]. The results of this observational
study are intriguing, but they have not yet been tested byexperimental manipulation. In another study, which did use
an experimental approach, Shutler and Campbell [232],
added yarrow (Achillea millefolium) to the nests of Tree
Swallows (Tachycineta bicolor); this manipulation reduced
the number of fleas in the nest by half, compared to control
nests. However, the authors did not find that the use of green
vegetation and the subsequent reduction in fleas had any
effect on nestling survival or fledgling success. Gwinner et
al. [233] manipulated green vegetation in European Starling(Sturnus vulgaris) nests and found no difference in the number of ectoparasites (mites, lice, fleas) between experimental
and control nests; however, nestlings from nests with vegetation did have higher red blood cell counts and body masses
than nestlings from nests without vegetation. The authors
argued that the vegetation may stimulate the immune systemof nestlings, which could ameliorate the detrimental effectsof blood-feeding ectoparasites, even though it did not change
parasite number, per se. This hypothesis has not been tested.
Yet another recent study, this one with Blue Tits
(Cyanistes caeruleus), showed that in enlarged broods, nestling mass gain was positively affected by the addition ofgreen vegetation [234]. However, there was no difference infledgling body mass between chicks in nests with added
vegetation versus control nests. In conclusion, these various
studies reveal a link between green vegetation and decreased
ectoparasite loads, and a link between vegetation and increased nestling condition. However, there is still no rigorous experimental evidence that fumigation of nests withgreen vegetation actually increases the fitness of birds bydeterring parasites.
Heterospecific Cleaning
Birds can conceivably reduce ectoparasites using what
Hart [24] referred to as "heterospecific cleaning". Both of the
known cases involve nest maintenance. The most remarkable
example was reported in a paper by Smith [235]. He observed that brood parasitic Giant Cowbirds (Scaphidura
oryzivora) are tolerated by some nesting colonies of foster
species, such as Yellow-rumped Caciques (Cacicus cela) andoropendolas (Psarocolius wagleri, P. decumanus, Gymnostinops montezuma). Smith [235] reported that the cost ofbrood parasitism was offset by the fact that the nestling cowbirds remove and consume parasitic botflies (Philornis) fromthe foster parents' offspring, thus enhancing the fledging
success of the foster species. Selection for cowbird egg mim-

66 The Open Ornithology Journal, 2010, Volume 3icry was relaxed under these conditions, explaining a higher
frequency of non-mimetic eggs in colonies parasitized byflies. This "advantage of being parasitized" (by cowbirds)
was reportedly lost in the case of cacique or oropendolacolonies adjacent to large wasp nests, because the wasps
deterred the flies from parasitizing bird nests. In such cases,
cowbirds were not tolerated by the foster species and thefrequency of mimetic eggs was higher. These interactions,which are among the most complex ever documented, needadditional study and confirmation.
Gehlbach and Baldridge [236] reported another form ofheterospecific cleaning. They documented higher growth
rates of nestling Eastern Screech Owls (Otus asio) in nests
with Blind Snakes (Leptotyphlops dulcis). Superficial scars
on the snakes suggested they were transported to the nest by
adult owls, yet not eaten. The authors argued that growth
rates of young in nests containing snakes were higher because the snakes fed on parasitic larvae that are harmful tothe nestlings. However, other factors could covary withsnake presence and owlet growth, e.g., parental hunting ability. An experimental manipulation of snake presence isneeded to test Gehlbach and Baldridge’s [236] hypothesis.
Cleaning of one species of bird by another species,
analogous to the cleaning symbioses of marine fishes, hasalso been suggested. Bowman and Billeb [237] speculated
that the bizarre feeding behavior of “vampire” Sharp-beaked
Ground Finches (Geospiza difficilis), which puncture thepin-feathers of boobies to feed upon their blood, may haveoriginated from finches feeding on the large, numerous hippoboscid flies that plague the boobies. This is an intriguing
idea, but the authors were quick to point out that they did notactually observe finches feeding on hippoboscid flies. We
are unaware of any other documented cases of cleaning interactions between different species of birds.
Nest Desertion
If all else fails, an ultimate strategy for dealing with nest
parasites is simply to abandon the nest, rather than continuing to invest in offspring that may be doomed. Nest desertionin the face of high ectoparasite loads has been documented
for many bird species [45, 212, 214, 238-245]. Duffy [242]showed that argasid ticks (Ornithodoros amblus) cause
large-scale desertion of colonial seabird nesting colonies,
which raises interesting questions. How often do adult birds
desert because they are cutting their losses, versus simply
escaping intolerable irritation? Because short-lived birds
have fewer breeding seasons in which to reproduce, shortlived birds should be slower to abandon their nests thanlong-lived birds, all else being equal. Comparative and experimental studies are needed to investigate how life span
affects the decision to desert nests, in the face of high ectoparasite load.
DISCUSSION
As we have tried to show, birds have an impressive arrayof possible defenses against ectoparasites. Different speciesof birds may use very different combinations of these defenses, but the extent to which this actually occurs is notknown. Most work has focused on demonstrating what thevarious defenses are, and, in some cases, exactly how theyfunction. A more complete understanding of how birds com-

Clayton et al.

bat ectoparasites requires a broader perspective that considers how the different defenses interact, and the relationshipof ectoparasite defense to the many other life history challenges birds face. The optimum strategy undoubtedly depends on various life history tradeoffs. Multiple defenses andhow they interact are also important to document in order tobetter understand the nature of coevolutionary responses tohost defense by the parasites themselves. The evolution ofeffective counterstrategies should be more difficult, all else
being equal, if a host has more than one effective defense
strategy.
Environmental constraints will also limit the defenses
available to different species. Opportunities for sunning are
more limited for birds that live in regions with an average of
300 days per year of rain (e.g., Seattle, Washington), compared to regions with an average of 300 days/year of sun(e.g., Salt Lake City, Utah). Redundant defenses may also be
important in the face of environmental variability. Sunningand dusting may combat similar ectoparasites, but dusting is
an option on a cloudy day, while sunning may be effective inhabitats devoid of dust or loose dirt.
Composition of the ectoparasite community will also
influence the defenses used by a given host. Ectoparasite
species richness and abundance vary markedly among birds,
even within single groups of ectoparasites [124]. Some species of tinamous (Tinamiidae) can be infested with a dozen
species of lice, while ostriches (Struthionidae) have but one
species [5, 63]. Defense strategies against a single species
probably differ from those against a more diverse community. Consistent with this prediction, bird species known tohost more species of lice appear to devote more time tomaintenance behavior than birds with few species of lice[246]. This kind of relationship probably holds for otherkinds of ectoparasites, as well.
Ectoparasite species richness can also vary within a single bird species. Brown and Wilson [247] compared the ectoparasite communities of House Sparrows in Europe andNorth America. They found that 34 of the 69 species of ectoparasites found on the European sparrows were “lost”
when House Sparrows were introduced to North America. It
would be interesting to test whether North American sparrows have lost certain defenses as a result of the reduction in
the richness of their ectoparasite community.
Ectoparasite prevalence also varies across environments.
A worldwide comparison of louse prevalence among 22 species of pigeons and doves (Columbidae) revealed a positive
relationship between louse prevalence and ambient humidity[22]. For example, lice were found on fewer than 3% ofbirds in the Sonoran Desert of Arizona, whereas 92% and100% of birds in Philippine and Peruvian rainforests, respectively, were infested. Moyer et al. [37] showed that pigeonsand doves in arid habitats also have lower louse abundance
than conspecifics in humid habitats. To confirm humidity as
the causal agent, the authors experimentally manipulated theambient humidity of captive feral Rock Pigeons. Louse infestations decreased greatly on birds kept at low humidity,
compared with those at higher humidities.
The "arsenal" of defenses employed by a given bird species will also depend on adaptations that are not immediately

How Birds Combat Ectoparasites

related to parasite control. Ornithologists have traditionallyinterpreted bill shape mainly as it relates to foraging [126,248-250]. However, recent studies (e.g. Clayton et al. [125];Fig. 4) make it clear that selection for efficient preening canalso play a role in the evolution of bill morphology. In environments with high ectoparasite pressure, selection forpreening-efficient bills may be strong. Some species of birds
have foraging ecology that precludes a maxillary overhang(e.g. woodpeckers, hummingbirds, oystercatchers (Fig. 2b),
skimmers, darters, and herons; Table I). These taxa are presumably under selective pressure to evolve other mechanisms for controlling ectoparasites.
Finally, ectoparasite defense may also vary in terms ofinvestment in particular defenses, independent of other defenses. For example, preening birds cannot simultaneously
forage or engage in courtship. Preening also reduces vigilance [251], increasing the risk of predation. Given thesecosts of preening, we predict that birds in areas of low ectoparasite pressure should spend less time preening thanbirds in areas of high ectoparasite pressure. This hypothesis
would be easy to test simply by comparing preening rates ofbirds in different localities (e.g., Clayton and Cotgreave[105]). We expect that tradeoffs of this kind may be common
for many of the different adaptations birds have for controlling ectoparasites.

The Open Ornithology Journal, 2000, Volume 3

SUPPLEMENTARY MATERIAL
Supplementary material is available on the publishers
Web site along with the published article.
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CONCLUSION
Birds have a wide variety of defenses for combating theirdiverse communities of ectoparasites. In some cases there isoverwhelming evidence that a particular trait is important in
ectoparasite defense (e.g., preening). In other cases the purported defense has not been tested (e.g, dusting). In stillother cases, recent evidence suggests that the purported defense may, in fact, have little to do with ectoparasite control(e.g. pectinate claws). Multiple defenses allow birds to target
different types of ectoparasites and to defend themselves in
the face of environmental variability. Birds should also
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ACKNOWLEDGMENTS
We thank Aldo Poiani for inviting us to contribute to thisvolume. We thank A. Smith, P. Angle, D. Brewer, E. Burtt,
P. Coley, M. Cottam, H. Douglas, J. Dean, K. Johnson, A.
Møller, R. Moyle, S. Nelson, N. Newbold, D. Reed, M.
Robbins, A. Rock, A. Smith, J. Weckstein and an anonymous referee for assistance and/or advice regarding different
aspects of this review. We are grateful to J. Belthoff and T.
Boves for access to Barn Owl specimens, and to J. Lokvam
for help interpreting chemical ecology data. The Division ofBirds of the National Museum of Natural History allowed us
access to their skin collection. We are grateful to R. Price fortallying louse species richness for the pectinate claw analysis. We are grateful to A. Farley for assistance preparing themanuscript. This work was supported by grants from Sigma
Xi, the Frank M. Chapman Memorial Fund, and the National
Science Foundation (DEB-9703003, NSF DEB-0344430,
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Accepted: June 11, 2009

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