Fault bars in bird feathers: Mechanisms, and ecological and evolutionary causes and consequences

Abstract

Fault bars are narrow malformations in feathers oriented almost perpendicular to the rachis where the feather vein and even the rachis may break. Breaks in the barbs and barbules result in small pieces of the feather vein being lost, while breaks in the rachis result in loss of the distal portion of the feather. Here, we provide a comprehensive review of 74 papers on fault bar formation in hopes of providing a clearer approach to their study. First, we review the evidence that the propensity to develop fault bars is modified by natural selection. Given that fault bars persist in the face of survival costs, we conclude that they must be an unfortunate consequence of some alternative adaptation that outweighs the fitness costs of fault bars. Second, we summarize evidence that the development of fault bars is triggered by psychological stress such as that of handling or predation attempts, and that they persist because the sudden contractions of the muscles in the feather follicle that control fright moults also causes the development of fault bars in growing feathers. Third, we review external and physiological (e.g. corticosterone) agents that may affect the likelihood that an acute stress will result in a growing feather exhibiting a fault bar. These modifying factors have often been treated as fundamental causes in the earlier literature on fault bars. Fourth, we then use this classification to propose a tentative model where fault bars of different severity (from light to severe) are the outcome of the interaction between the propensity to produce fault bars (which differs between species, individuals and feather follicles within individuals) and the intensity of the perturbation. This model helps to explain contradictory results in the literature, to identify gaps in our knowledge, and to suggest further studies. Lastly, we discuss ways in which better understanding of fault bars can inform us about other aspects of avian evolutionary ecology, such as the physiology of moult, the integration of moult into avian life cycles, and the strategies used to minimize stress during moult. Moreover, the study of fault bars may be relevant to understanding the aerodynamics of flight and the early evolution of flight.

Full text

Biol. Rev. (2016), pp. 000–000. 1
doi: 10.1111/brv.12273
Fault bars in bird feathers: mechanisms,
and ecological and evolutionary causes and
consequences
Roger Jovani1,∗and Sievert Rohwer2
1Department of Evolutionary Ecology, Estaci´on Biol´ogica de Do˜nana (CSIC), Avenida Americo Vespucio s/n, 41092 Seville, Spain
2Department of Biology and Burke Museum, University of Washington, Seattle, WA 98195, U.S.A.
ABSTRACT
Fault bars are narrow malformations in feathers oriented almost perpendicular to the rachis where the feather vein
and even the rachis may break. Breaks in the barbs and barbules result in small pieces of the feather vein being
lost, while breaks in the rachis result in loss of the distal portion of the feather. Here, we provide a comprehensive
review of 74 papers on fault bar formation in hopes of providing a clearer approach to their study. First, we review
the evidence that the propensity to develop fault bars is modified by natural selection. Given that fault bars persist in
the face of survival costs, we conclude that they must be an unfortunate consequence of some alternative adaptation
that outweighs the fitness costs of fault bars. Second, we summarize evidence that the development of fault bars is
triggered by psychological stress such as that of handling or predation attempts, and that they persist because the sudden
contractions of the muscles in the feather follicle that control fright moults also causes the development of fault bars in
growing feathers. Third, we review external and physiological (e.g. corticosterone) agents that may affect the likelihood
that an acute stress will result in a growing feather exhibiting a fault bar. These modifying factors have often been
treated as fundamental causes in the earlier literature on fault bars. Fourth, we then use this classification to propose a
tentative model where fault bars of different severity (from light to severe) are the outcome of the interaction between
the propensity to produce fault bars (which differs between species, individuals and feather follicles within individuals)
and the intensity of the perturbation. This model helps to explain contradictory results in the literature, to identify gaps
in our knowledge, and to suggest further studies. Lastly, we discuss ways in which better understanding of fault bars can
inform us about other aspects of avian evolutionary ecology, such as the physiology of moult, the integration of moult
into avian life cycles, and the strategies used to minimize stress during moult. Moreover, the study of fault bars may be
relevant to understanding the aerodynamics of flight and the early evolution of flight.
Key words: bird flight, feather deformities, perturbations, physiology, stress.
CONTENTS
I. Introduction .............................................................................................. 2
II. Methods .................................................................................................. 3
III. Theoretical framework ................................................................................... 3
IV. Selection and the development of fault bars .............................................................. 3
V. Stressors that trigger the generation of fault bars ......................................................... 5
VI. Follicular mechanisms of fault bar formation ............................................................. 6
(1) Blood pressure ........................................................................................ 6
(2) Musculature contraction ............................................................................. 7
VII. Proximate factors shaping fault bar expression in individuals ............................................ 7
(1) Malnutrition .......................................................................................... 7
(2) Age and sex .......................................................................................... 8
(3) Disease ............................................................................................... 8
* Address for correspondence (Tel: +34 954 466 700; Fax: +34 954 621 125; E-mail: jovani@ebd.csic.es).
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2Roger Jovani and Sievert Rohwer
(4) Corticosterone ........................................................................................ 8
(5) Habitat ............................................................................................... 9
VIII. Overview ................................................................................................. 9
IX. Mechanistic model ....................................................................................... 10
(1) The model ............................................................................................ 10
(2) Empirical findings explained by the mechanistic model .............................................. 10
(3) Knowledge gaps revealed by the model .............................................................. 11
X. Ecological and evolutionary consequences of fault bars .................................................. 11
XI. Conclusions .............................................................................................. 12
XII. Acknowledgements ....................................................................................... 13
XIII. References ................................................................................................ 13
XIV. Supporting Information .................................................................................. 15
I. INTRODUCTION
Stressors produce growth abnormalities in keratin structures
such as beaks, claws, feathers, hairs, hoofs or horns. In
nails, for instance, these growth abnormalities have been
traditionally associated with disease (Han et al., 2000; Ciastko,
2002), or intrusive medical treatments (Deliliers & Monni,
2001; Vassallo et al., 2001). However, they probably have
little or no effect on individual fitness. A different picture
arises when these growth abnormalities are produced in bird
feathers.
Fault bars are feather malformations generated during
feather growth (see pictures in Slagsvold, 1982; Murphy,
Miller & King, 1989; Machmer et al., 1992; Sarasola &
Jovani, 2006; Møller, Erritzøe & Nielsen, 2009). They vary
from slight malformations that are difficult to see to extreme
deficiencies in keratin deposition resulting in missing barbules
and breaks in the feather vane and even the feather rachis
(Riddle, 1908; Roest, 1957; Dawson, Bortolotti & Murza,
2001; Møller et al., 2009; Newton, 2010). Accordingly, many
studies classify fault bars by the severity of damage they
may cause to feathers (often called ‘strength’, e.g. Sarasola
& Jovani, 2006). Here we rank potential damage to feathers
(fault bar severity hereafter) as light, moderate, and severe,
according to how much the feather is weakened by the fault
bar. Light fault bars resemble thin lines crossing the feather
vein and appear, on close inspection, as a slight notch on
the feather surface due to feather malformation (Sarasola
& Jovani, 2006). Such fault bars rarely result in breaks
in the feather vein and damage to the rachis amounts to
only a slight discontinuity on the rachis surface, detectable
by sliding one’s fingernail along the rachis. Moderate fault
bars consist of a conspicuous lack of keratin deposition in
barbs and barbules (Murphy et al., 1989), making the feather
translucent at the fault bar, and sometimes resulting in barbs
that are bent at the fault bar. In this case the rachis often
shows a clear malformation that is easy to see. Severe fault
bars are seen as sections of feather vein a few mm wide that
are free of barbules. Feather barbs often break at these fault
bars, resulting in some loss of feather vein, and the rachis
can also break causing loss of the distal part of the feather
(Riddle, 1908; Roest, 1957; Newton, 2010).
Sebright (1826) seems to have been the first to discuss
fault bars in his treatise on falconry, but Riddle (1907,
1908) and Duerden (1909) undertook the first serious
investigations of the formation of fault bars. Since then,
fault bars have attracted the attention of bird keepers (Ward
& Slaughter, 1968; Taylor, 1991), veterinarians (Hudelson &
Hudelson, 1995; Beynon, Forbes & Harcourt-Brown, 1996;
Koutsos, Matson & Klasing, 2001; Koski, 2002; Rubinstein
& Lightfoot, 2012) and ornithologists (e.g. Slagsvold, 1982;
Murphy, King & Lu, 1988; Gombobaatar, Yosef & Birazana,
2009; Yosef, Gombobaatar & Bortolotti, 2013; Eggers &
Low, 2014; Jovani, Montalvo & Sabat´
e, 2014). Most research
has focused on identifying the external and physiological
factors that may stimulate the formation of fault bars and the
proximate mechanisms by which the fault bars are generated
during feather growth. More recently, a few studies have
investigated how fault bar frequencies have been moulded
by natural selection.
Fault bars are oriented approximately perpendicular to the
rachis (Riddle, 1908; Prum & Williamson, 2001; Maderson
et al., 2009) and run parallel to the alternating light/dark
feather growth bands that can be seen in some feathers and
that usually record 24 h of feather growth (Brodin, 1993;
Jovani & Diaz-Real, 2012). This leaves little doubt that they
are generated by some trauma or perturbation affecting the
collar cells of the feather follicle that generate the complex
structure of growing feathers. This review shows that fault
bars are costly and that the propensity of follicles to create
fault bars can be reduced by natural selection. However, fault
bars are still widespread in birds, thus challenging us to ask
why they exist at all. We suggest that fault bars are a harmful
by-product of some other adaptation carrying benefits that
outweigh the costs of fault bars, as in the classic case of sickle
cell anaemia conferring resistance to malaria in humans who
are heterozygous for sickling (Ferreira et al., 2011). The aim
of this review was to identify these other adaptations and to
synthesize past research on fault bars by organizing them
into a theoretical framework.
A recent review convincingly suggested that feather holes
0.5–1 mm in diameter (also called ‘fault spots’ by Murphy
et al., 1989) may be related to fault bars (V ´
ag´
asi, 2014).
Previously, these holes were attributed to chewing lice (e.g.
Møller, 1991). V´
ag´
asi et al. (2011) found a positive correlation
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Fault bars in bird feathers 3
between the abundance of fault bars and feather holes
among great tits (Parus major), but the same team (Pap
et al., 2007) found these malformations to have different
spatial distributions along the wing feathers within birds.
This may suggest that fault bars and feather holes have
different causes or that feather holes are less harmful and
thus that their position along the wing of birds has been
less shaped by natural selection. Pale bands, varying from a
few millimetres to centimetres in width (see Murphy et al.,
1988, 1989) are sometimes treated as fault bars. However,
Murphy et al. (1988) found that synthetic diets deficient in
sulfur-containing amino acids produced these pale bands
without generating fault bars. Experimental studies in barn
owls (Tyto alba) (Roulin et al., 2008) and feral pigeons (Columba
livia) (Jenni-Eiermann et al., 2015) report increases in the
frequency of pale bands in corticosterone-implanted birds
(see Fig. 3 in Jenni-Eiermann et al., 2015), but they did
not report the formation of fault bars. Although fault
bars and pale bands are both feather malformations, they
appear to have different proximal causes; thus, we advocate
treating fault bars, feather holes, and pale bands as different
phenomena (Pap et al., 2007; V ´
ag´
asi, 2014), while we
encourage studying them simultaneously.
II. METHODS
We found relevant papers on fault bars by searching ISI
Web of Knowledge and Google Scholar for word combinations
such as fault bars, feather marks, fret marks, hunger traces,
hunger faults, starvation marks, segmented dysplasia, stress
bar, stress band or hunger streaks, and by snowballing, i.e.
following references found in the papers we were reviewing.
For each paper treating the formation of fault bars we noted
the suggested cause or correlated factor (e.g. malnutrition,
disease, age, sex), and the quality of the evidence provided.
Evidence was considered ‘speculative’ in the absence of
empirical data, ‘anecdotal’ when observations and analyses
were few and when experiments lacked controls, ‘correlative’
when the occurrence of fault bars was related to potential
causative factors, and ‘experimental’ when experimental and
control treatments were reported.
We found 74 papers reporting 179 tests of hypotheses:
3.4% were speculative, 19.0% anecdotal, 60.3% correlative
and 17.3% experimental (Table 1). A detailed account of
each study is provided as online Supporting Information
(Appendix S1), and synthesized in Table 1, and see online
Tables S1 and S2.
III. THEORETICAL FRAMEWORK
The available literature identifies a number of potential
stressors causing fault bars, many potential factors related to
the abundance of fault bars, and two mechanistic hypotheses
on how fault bars are generated by the collar cells of the
feather follicle during feather growth. The likelihood of
fault bars forming varies according to differences between
feathers and feather tracts within individuals, differences
among individuals related to age, habitat, and other factors,
and differences among species. The temporal scale for factors
that have been related to fault bar formation has also varied
from seconds (handling), to hours (rain), days (malnutrition),
months (disease), years (age), and beyond (natural selection).
Past studies often seem to have mixed apples and oranges,
emphasizing the need for a unifying framework to organize
information on fault bar formation and persistence and,
hopefully, to move this field forward.
We suggest that fault bar production should be studied
on a time scale equivalent to the production of one fault
bar in a particular feather follicle at a given moment. We
further suggest that future studies clearly distinguish between
(i) ultimate, evolutionary factors that shape the a priori
propensity of an active feather follicle to generate a fault bar
in response to a stressor; (ii) specific perturbations (stressors)
that trigger the production of a fault bar at a particular
moment; (iii) the mechanical or physiological mechanisms
by which the feather collar cells actually generate a fault bar;
and (iv) proximate factors that change the a priori propensity
of fault bar generation at the individual level according to
physiological and environmental factors.
We begin with a review of the literature on fault bars
organized as suggested above. Next we present a mechanistic
model linking these various levels of organization. Finally,
we finish by discussing the link between fault bars and other
physiological and life-history attributes of birds.
IV. SELECTION AND THE DEVELOPMENT OF
FAULT BARS
The evidence that the propensity to develop fault bars can be
modified by natural selection is strong, but mostly indirect.
To be modified by natural selection, this propensity must
be heritable, variable between individuals, and have fitness
consequences.
As far as we are aware, only one experimental study
demonstrates heritability of the propensity to develop fault
bars. This study cross-fostered nestling barn swallows (Hirundo
rustica) to evaluate the effects of vitamin E supplementation
and brood size manipulation on nestling development (de
Ayala, Martinelli & Saino, 2006). Neither of the two
experimental treatments affected the incidence of fault bars
in these nestlings, but the nest of origin had a strong and
statistically significant effect on the incidence of fault bars in
the rectrices of nestlings. This suggests that the propensity
to develop fault bars has a heritable, genetic component,
although maternal effects through the eggs cannot be
excluded. Long-term fault bar pedigree studies (e.g. with
an animal model approach) are encouraged to disentangle
the environmental and genetic factors contributing to the
formation of fault bars.
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4Roger Jovani and Sievert Rohwer
Table 1. Summary of the studies providing evidence for the different ultimate and proximate factors related to fault bar formation,
as well as the mechanisms proposed and the stressors investigated. Proximate factors are variables differing between populations
(e.g. habitat) or individuals (e.g. body size) within populations. Note that a single study can contribute to more than one hypothesis.
Details for each specific test within each study can be found in the online Supplementary Information. Study categories are described
in Section II
Effect: NO Effect: YES
Speculative Anecdotal Correlative Experimental Total Speculative Anecdotal Correlative Experimental Total
Grand
total
Ultimate issues
Genetic factors 1122
Inter-feather differences 1 1 6 13 19 20
Interspecific differences 22 44
Risk of feather damage 222
Species aerial foraging 111
Species aerial sexual displays 1 1 1
Species diet 1 1 1
Species domestication 1 1 1 1 2
Species flight 111
Species hybridization 1 1 1
Species migration 111
Species predation pressure 111
Species sexual dichromatism 1 1 1
Survival 1 1 5 5 6
Total 0 2 5 0 7 1 10 25 1 37 44
Proximate factors
Age 1 1 1 13 14 15
Arrival date 1 1 1
Body condition 2 2 1 1 2 4
Bodysize 11 112
Breeding effort 1 1 1
Broodsize 11 112
Clutch size 1 1 1
Colony size 111
Corticosterone 1 1 4 4 5
Cost of ornaments 2133
Crowding 1 1 1
Disease 1 1 2 1 4 1 6 8
Egg size 1 1 1
Fluctuating asymmetry 1 1 1
Habitat 2 2 6 6 8
Hatching date 1 1 1
Hour 121 44
Interspecific competition 111
Inter-individual differences 111
Laying date 111
Malnutrition 1 3 10 14 1 7 1 4 13 27
Need for fast moult 1122
Nestling rank 1 1 1 1 2
Other feather defects 1 3 4 1 1 2 6
Plumage features 1 1 2 2 3
Sex 6 6 5 5 11
Total 0 3 28 12 43 3 12 48 7 70 113
Mechanisms
Follicle nutrition 111
Follicle collapse 1 1 1
Musculature contraction 1 1 1 1 2 3
Total 0 0 0 1 1 2 2 0 0 4 5
Stressors
Altrazine (herbicide) 1 1 1
Environmental change 111
Food unpredictability 111
Handling 2 2 1 1 5 7 9
Psychological stress 222
Weather 1 1 2 1 1 3
Total 031 15021 91217
Grand total 0 8 34 14 56 6 26 74 17 123 179
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Fault bars in bird feathers 5
Although evidence is limited (and more longitudinal
studies are encouraged), individuals have been shown to
vary in their likelihood of developing fault bars across
successive moults. Thus, American kestrels (Falco sparverius)
varied consistently across years in the numbers of fault bars
they developed, suggesting variation among individuals in
the propensity to develop fault bars (Bortolotti, Dawson &
Murza, 2002). If these differences have a genetic component,
as the barn swallow study suggests, then the propensity to
develop fault bars could be modified by selection.
The fitness costs of fault bars seems clear. Feathers break
at fault bars and broken feathers are generally not replaced
until the next scheduled normal moult of the feather. Thus,
the fitness consequences of broken feathers could last up to
several years in large birds with incomplete moults (Rohwer
et al., 2009). Reductions in wing area increase wing loading,
which reduces flight performance (Velando, 2002; Navarro
& Gonz´
alez-Solís, 2007). Fitness costs of fault bars have been
shown in several studies. Each fault bar in the rectrices of
both willow tits (Poecile montana) and crested tits (Lophophanes
cristatus) was associated with a 5% reduction in survival
(Eggers & Low, 2014). Three other studies reported higher
mortality among birds with more fault bars. Juvenile great
tits with more fault bars were significantly less likely to be
recaptured than those with fewer fault bars (Pap et al., 2007).
Juvenile Siberian jays (Perisoreus infaustus) with more fault bars
in their primaries were more likely to be killed by predators
in their first winter (Griesser, Nystrand & Ekman, 2006).
Finally, feathers of prey species taken by goshawks (Accipiter
gentilis) and sparrowhawks (Accipiter nisus)weremorelikely
to contain fault bars than were netted individuals of those
same prey species, suggesting that individuals with more fault
bars were more susceptible to predation (Møller et al., 2009);
measures of condition were not related to numbers of fault
bars in the 47 prey species they examined. It is important
to note that none of these studies distinguishes between the
direct cost of fault bars and the alternative that fault bars
merely identify individuals in poor condition that were less
likely to survive for reasons unrelated to the fault bars in their
plumage. That would require experiments.
Current evidence suggests that natural selection shapes
the propensity of feather follicles to develop fault bars at
two levels: between bird species, and according to feather
position within individual birds. Bird species differ greatly in
their abundance of fault bars (Taylor, 1991; Freed, Medeiros
& Bodner, 2008; Møller et al., 2009). For instance, nestlings of
many species have more fault bars than adults (e.g. Jovani &
Tella, 2004; Eggers & Low, 2014), but there are species, such
astheEuropeanpiedflycatcher(Ficedula hypoleuca), where
nestlings are largely free from these malformations (Kern
& Cowie, 2002). These differences in fault bar propensity
among species seem to be related to species characteristics
that make fault bar expression more or less penalized by
selection. For instance, ostrich (Struthio camelus) farmers find
it difficult to produce wing feathers without fault bars,
presumably because flightlessness makes the expression of
fault bars less costly in ostriches (Duerden, 1909). More
recently, Møller et al. (2009) found that birds that fly differ
greatly in fault bar prevalence and abundance, with species
that suffer higher predation pressure or that have longer
migrations showing fewer fault bars. From these results
they concluded (p. 343) that ‘ ... developmental control or
susceptibility to stress can change when intensity of natural
selection changes’.
Differences in fault bar abundance between feathers
within individuals (even contiguous feathers of the same
feather track) also suggest that natural selection has shaped
the propensity to develop fault bars. Thus, fault bars are
symmetrically distributed in the left and right rectrices of
juvenile ospreys (Pandion haliaetus; Machmer et al., 1992) and
juvenile barn swallows (Serrano & Jovani, 2005). Because
juvenile rectrices grow simultaneously and, thus, experience
the same stressors, the left–right symmetry in the distribution
of fault bars in the tail clearly shows that the propensity to
develop fault bars differs between contiguous feather follicles.
These differences presumably result from selection opposing
fault bars in feathers where breaks in the vein or rachis would
affect fitness more seriously (e.g. by being more important
for flight).
This ‘fault bar allocation’ hypothesis is supported in studies
reporting that rectrices regularly have more fault bars than
remiges (Slagsvold, 1982; Bortolotti et al., 2002; Sarasola &
Jovani, 2006), and inner remiges more than outer remiges
(Murphy et al., 1989; Jovani & Blas, 2004; Pap et al ., 2007;
Jovani et al., 2010). Relative to rectrices and secondaries
selection apparently has suppressed the occurrence of fault
bars in the primaries, perhaps because they experience
greater strain during flight (Jovani & Blas, 2004). In both
raptors and cranes fault bars are less common in primaries
than in rectrices or secondaries but they are more likely to
result in feather breaks in the primaries when they occur
there (Sarasola & Jovani, 2006; Jovani et al., 2010). This
pattern suggests that natural selection has suppressed the
production of fault bars in feathers where damage would
seriously lower survival. Indeed, Pap et al. (2007) found that
juvenile great tits were less likely to be recaptured if they had
more fault bars in their primaries but not if they had more
in their secondaries and tertials.
V. STRESSORS THAT TRIGGER THE
GENERATION OF FAULT BARS
Fault bars are a punctuate phenomenon, thus it seems
logical to suspect that fault bars are triggered by some factor
occurring during a short period of time or, at least, that the
processes that produce fault bars occur during a short time
in the follicle collar of a growing feather.
While studying the energetic and nutritional demands of
moulting in the white-crowned sparrow (Zonotrichia leucophrys
gambelii), King & Murphy (1984) and Murphy et al . (1988)
made a serendipitous discovery: fault bars were created on
the days when they handled the birds, in both control and
experimental birds. They concluded that: ‘We think that the
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6Roger Jovani and Sievert Rohwer
weight of evidence strongly favors the shock of handling as
the cause of fault bars in captive birds, and presumably some
similar shock (such as flight from a predator) causes them
in free-living birds’ (King & Murphy, 1984, p. 169). Later
experiments confirmed these results, and led the authors to
suggest that fault bars are a mild form of the response to
shock that produces fright moult, the instantaneous shedding
of feathers when birds are stressed such as during a predatory
event (Murphy et al., 1988, 1989).
The link between being restrained by a researcher, or a
similar stress such as a failed predation event, and fault bar
formation is supported by other studies. Negro, Bildstein
& Bird (1994) found that hand-reared nestling American
kestrels developed more fault bars than parentally reared
nestlings, irrespective of whether hand-reared nestlings were
fed ad libitum or not. While this does not discount other factors
(and note that food delivered by parents to naturally reared
nestlings was not manipulated), this study suggests that the
psychological stress of not being with their parents and being
handled by researchers contributed to the formation of fault
bars. Whitmore & Marzluff (1998) found a similar result (but
including an effect of malnutrition) in hand-reared corvids of
three species.
Other psychological factors have been studied as causes
of fault bars. In an interesting experiment using captive
European starlings (Sturnus vulgaris) Strochlic & Romero
(2008) compared controls (no stress) with three experimental
stress groups: 30 min of chronic stress four times a day, acute
stress of being handled for 30 min, and chronic stress with
food restriction. Although controls and stress groups did
not differ significantly in numbers of fault bars on a single
rectrix (P=0.08), the chronic and acute stress treatments
had three to fivefold more fault bars than the controls; non
significance may have resulted from small sample sizes. A
recent study of house sparrows (Passer domesticus) showed
higher stress responses (corticosterone levels) in young birds
than in adults when they were handled by researchers and
that the stress response of young birds declined as they grew
(Lendvai et al., 2015). This is interesting because young birds
consistently have more fault bars than adults (see Section
VII.2), which, again, is consistent with fault bars having
a psychological cause. Overall, current evidence suggests
that handling, and other similar acutely frightening stressors,
like predation attempts, are powerful triggers of fault bar
production. In fact, even predation exposure without actual
predation attempts has been related to fault bar formation
(see Section VII.5).
VI. FOLLICULAR MECHANISMS OF FAULT BAR
FORMATION
A major gap in our understanding is that we do not know
how fault bars are generated in growing feathers by the
feather follicle (Prum & Williamson, 2001; Maderson et al.,
2009). Whether fault bars are created by some mechanical
force, or by a change in the physiology of the follicle collar
cells, or by a combination of the two is unclear.
(1) Blood pressure
Riddle (1907, 1908) suggested that fault bars are formed by
reduced blood pressure in the follicle collar during the first
hours of night. He suggested that this reduced nutrition to
the growing feather, resulting in reduced keratin deposition
and a fault bar. Riddle tested this hypothesis by starving
captive birds, and treating them with amyl nitrite and other
substances thought to decrease blood pressure, but support
was ambiguous. Duerden (1909) proposed an alternative, also
based on blood pressure. Rather than positing a shortage
of nutrients (a physiological cause), he suggested that a
reduction of blood pressure inside the developing feather
during the early hours of the night would cause mechanical
collapse of the feather follicle, like sucking a blocked straw,
resulting in the generation of a fault bar. Duerden (1909,
p. 479) thought that reduced blood pressure was sufficient
to mechanically collapse the sheath of the growing feather:
‘From long observation every farmer [of ostriches for the
production of feathers] knows, even before the plumes
unfold, that bars will be present wherever the outer sheath is
indented, while if the sheath is smooth all the way the feathers
will be faultless’. Note, however, that these indentations in
the feather sheath could equally be the result of muscles in
the feather follicle suddenly contracting during the stress of
being handled or frightened by a predator, both of which
cause fault bar formation (see Section 5).
These blood pressure-related hypotheses suggest that fault
bars are mainly generated in the early part of the night when
blood pressure is reduced; thus, no more than one fault bar
should be generated every 24 h, implying that consecutive
fault bars in the same father should be separated by the
length of feather grown during 24 h (i.e. the width of a
pair of light–dark growth bands). Riddle (1907, 1908) and
Duerden (1909) reported this to be the case, as did Jovani
& Diaz-Real (2012); however, the latter authors found that
many fault bars developed at other hours, particularly in
adult birds. Murphy et al. (1989) assessed the blood pressure
hypothesis more directly by showing the night-time blood
pressure reduction to be slight and unlikely to be sufficient
to collapse the feather follicle and induce a fault bar. Thus,
the hypothesis of reduced blood pressure has little empirical
support. However, the possibility that fault bars are mostly
generated during certain parts of the diel cycle (e.g. during
the first hours of the night in white stork, Ciconia ciconia,
chicks: Jovani & Diaz-Real, 2012) merits further study as
it may facilitate understanding the proximal mechanisms of
fault bar formation.
From an evolutionary perspective, reductions in blood
pressure could generate fault bars if the reduction in blood
pressure was an adaptive response to stressors. For example,
cold stress might reduce peripheral blood flow and pressure
to conserve heat and lower the cost of feather production.
However, the ‘musculature contraction’ hypothesis (see
Section VI.2) is more likely because predation attempts
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Fault bars in bird feathers 7
can cause fault bars to form (King & Murphy, 1984; Murphy
et al., 1988) and the mere sight of a hawk raises blood pressure
in turkeys (Krista et al., 1981), rather than lowering it.
(2) Musculature contraction
King & Murphy (1984) and Murphy et al. (1988) suggested
that fault bars are created by a sudden contraction of
the musculature around the soft feather follicle during
feather growth (Homberger & de Silva, 2003; Maderson
et al., 2009). King & Murphy (1984) cite Dathe (1955) to
support this notion, but the latter author could not decide
if the feathers lost in fright moults were lost by sudden
contraction or relaxation of these muscles. We assume that
strong contractions are the underlying mechanism because
feathers are also attached to the skin by connective tissue that
would prevent them from being extruded solely by relaxation
of the muscles surrounding the follicle.
King & Murphy (1984) noted that the nonstriated muscles
surrounding the feather follicle were probably powerful
enough to crimp the feather sheath and cause the generation
of a fault bar. In experimental oil-filled feather follicles
inserted into the sockets of plucked feathers pressures
generated by the stimulation of these muscles averaged
2.4-fold above baseline pressure and, in some experiments,
reached fourfold above baseline (Peterson & Ringer, 1968).
Murphy et al. (1989, p. 1317) conclude that ‘fault bars may
result from unusual contractions of feather muscles that are
normally inhibited while a feather is growing and its sheath
is soft’. These muscle contractions could also account for the
indented sheaths in the feathers of ostriches always resulting
in fault bars (Duerden, 1909).
The beauty of the suggestion by Murphy et al. (1989),
that fault bars are generated by involuntary contractions of
these feather muscles, is that they attribute these sudden
contractions to an alternative fitness benefit, fright moults,
which clearly seem to benefit birds escaping from predators
(Dathe, 1955; H¨
oglund, 1964). Consideration of genetic
correlations as the cause of maladaptive traits did not
characterize thinking when Riddle (1908) and Duerden
(1909) were writing, but it is clear that Murphy et al. (1989)
were thinking in these terms in their interpretation of the
development of fright bars. Thus, they posit that the loss of
feathers in fright moult and the involuntary development of
fault bars during the growth of feathers were both caused by
contractions of the muscles surrounding the feather follicle.
The implication is that inhibition of this muscular contraction
cannot be complete in those species where fright moult
generates a fitness benefit that exceeds the fitness cost of
fault bars generated by sudden stressors that cause the
contraction of these muscles while feathers are growing.
This is consistent with their strong experimental evidence
that handling stress causes fault bars and, further, does so
much more frequently in naïve than habituated birds (King
& Murphy, 1984; Murphy et al., 1988). However, Murphy
et al. (1989) also acknowledge Riddle’s (1908) circumstantial
evidence that unsuccessful begging or foraging, odd smells,
and food adulterants may also stimulate formation of fault
bars. We consider these other factors as general stressors
affecting the propensity to develop fault bars, rather than
stimuli that might cause contractions of the feather muscles.
To test the idea that fault bars are an unfortunate
consequence of the ability to undergo fright moults, we
need experiments exploring whether artificial stimulation
of the follicular muscles can produce fault bars in growing
feathers, and whether the stimulus needed to generate these
contractions varies according to differences among species in
their propensities to undergo fright moults. The latter could
be investigated by relating the frequency of fault bars seen in
rectrices to the index of the propensity to show fright moults
developed by Møller, Nielsen & Erritzøe (2006), which is
simply the difference in the force required to pluck rump
feathers compared to feathers from the upper back or breast.
That rectrix feathers are frequently lost in fright moults (Juhn,
1955; Møller et al., 2006) and that they regularly have far
more fault bars than remiges (Møller et al., 2009) is consistent
with fright moults and fault bars having a common cause
that inversely links their fitness costs and benefits.
VII. PROXIMATE FACTORS SHAPING FAULT
BAR EXPRESSION IN INDIVIDUALS
So far, we have established two general principles. First,
species and feather groups differ in their propensity to
develop fault bars in ways that suggest adaptive responses
to the survival costs imposed by fault bars; and second, the
immediate stressor triggering the formation of a fault bar
seems to be some form of acute fear. Below we review a
series of proximate factors that can modify the propensity
for an acute stressor to trigger the formation of a fault bar
in a growing feather. Much of the earlier literature treating
these factors has not distinguished between treating them
as fundamental causes of fault bars and treating them as
modifiers of the propensity to produce fault bars. Thus we
emphasize that we are treating these factors as modifiers
of the likelihood that a follicle will produce a fault bar in
response to a triggering stress. These modifying factors may
be intrinsic, such as sex, age or developmental history, or
extrinsic, such as food availability, disease or habitat features,
but there is little evidence that they are able to generate fault
bars in the absence of a triggering stimulus.
(1) Malnutrition
Malnutrition was likely the first factor to be related to fault
bars (Sebright, 1826), leading to fault bars being called
‘hunger traces’ or ‘hunger streaks’. Riddle’s (1907, 1908)
pioneering studies suggested that malnutrition was a key
factor in explaining fault bar formation, with the result that
it has been examined in no less than 27 studies, 14 of which
are experimental (Table 1). While some evidence supports
this hypothesis (e.g. Waite, 1990), 10 out of 14 experimental
tests of hunger as a proximate modifier of the propensity
to develop fault bars failed to induce fault bar formation
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8Roger Jovani and Sievert Rohwer
through food restriction or malnutrition (Table 1; e.g. King
& Murphy, 1984; Murphy et al., 1988; Negro et al ., 1994;
Searcy, Peters & Nowicki, 2004). Thus, current empirical
evidence fails to show that malnutrition strongly modifies the
propensity for fault bars to form.
Related to malnutrition is general body condition.
Although current evidence (Table 1) does not suggest
condition to be strongly correlated with the propensity
to develop fault bars, body condition cannot be ruled
out completely. Condition, measured as mass corrected
for size, was related to fault bar frequency in American
kestrels (Bortolotti et al., 2002). Fault bar abundance has
also been related to features linked to differences in body
condition among individuals, such as nestling rank or
number of nestlings in a brood (Machmer et al., 1992;
Gombobaatar et al., 2009), or co-occurrence with other kinds
of feather defects (Harrison, 1963) or feather secondary
sexual characters (V´
ag´
asi, Pap & Barta, 2010; V´
ag´
asi et al.,
2012). Further, individuals with better developed sexual
ornaments often have fewer fault bars (Møller, 1989, 1994;
Blanco & de la Puente, 2002; but see Andersson, 1994),
which is consistent with those individuals being in better
condition. Interestingly, five out of six studies have shown
that individuals with more fault bars have lower survival
(Table 1). While fault bars may directly explain lower survival
in some cases by impairing flight and the ability to escape
predators, it is perhaps more likely that fault bars merely
identify lower quality individuals that would be less able to
escape predators, even without fault bars. Only experiments
can sort this out.
(2) Age and sex
While sex does not appear to affect fault bar formation,
age is strongly associated with fault bar frequency (Table 1).
Younger birds consistently have more fault bars than older
conspecifics, both across individuals (Slagsvold, 1982; Blanco
& de la Puente, 2002; Jovani & Blas, 2004; Jovani et al., 2014)
and within individuals developing from nestling to adult
plumage (Pap et al., 2007; Leloutre, Gouzerh & Angelier,
2014). Indeed, age even affects the development of fault bars
within developing nestlings, as studied by the position of fault
bars along growing feathers (Machmer et al., 1992; Jovani &
Tella, 2004; Jovani & Diaz-Real, 2012). Jovani & Tella (2004)
found an exponential decrease in fault bar formation during
nestling growth, which paralleled the increase in survival
of nestlings with age; young that are less able to confront
environmental perturbations produce more fault bars.
(3) Disease
Disease also predicts differences in the propensity to develop
fault bars in some studies. Male house sparrows with
many fault bars had relatively larger bursas of Fabricius,
which indexes the severity of parasite infections (Møller,
Kimball & Erritzøe, 1996). Similarly, Freed et al. (2008)
found more fault bars in individuals infected with chewing
lice in nine avian species. Jovani et al. (2014) found a clear
correlation between Campylobacter enteric bacterial infection
and fault bar abundance in feral pigeons, suggesting either
a causal relationship or (more likely) a higher propensity
to develop fault bars among physiologically compromised
birds. Manniste & Horak (2014) reported similar results
for captive greenfinches (Carduelis chloris) that died from
Trichomonas infections.
A study by Romano et al. (2011) is possibly the
most interesting. They treated nestling barn swallows
with bacterial lipopolysaccharide (LPS), thus simulating a
bacterial infection without the detrimental costs of actual
infections and found both the prevalence and abundance
of fault bars to be about twice as high in experimental
than in control nestlings. Moreno-Rueda (2010) found that
LPS-injected birds had a slower moult speed than controls,
thus suggesting a link between LPS injection and feather
regeneration physiology. Because LPS, per se, could not
explain the production of fault bars, he suggested that the
higher corticosterone titres associated with LPS treatment
(Owen-Ashley et al., 2006) might be responsible for the
additional fault bars because high corticosterone levels have
been related to reduced feather quality (see Section VII.4).
(4) Corticosterone
Corticosterone, the predominant avian glucocorticoid and
a hallmark of the adrenocortical response to stress in birds
(Blas, 2014), has attracted substantial attention in relation
to feather moult physiology (e.g. Romero, Strochlic &
Wingfield, 2005; DesRochers et al., 2009; Almasi et al ., 2012;
Jenni-Eiermann et al., 2015). Corticosterone has complex,
contrasting and even opposing effects when related to food
intake and feather growth. For instance, Patterson et al.
(2014) found more corticosterone in feathers of nestling
Caspian terns (Hydropogne caspia)fedad libitum compared to
conspecifics ingesting only two-thirds the amount of food,
while Will et al. (2014) found higher feather corticosterone
in food-restricted rhinoceros auklets (Cerorhinca moncerata)
that were hand-reared or manipulated in the field. Almasi
et al. (2012) found corticosterone implants to reduce feather
growth rate in nestling barn owls, resulting in shorter
wing lengths at fledging. Similarly, Romero et al. (2005)
found that corticosterone-implanted European starlings grew
feathers more slowly than controls. DesRochers et al. (2009)
found that both endogenous (experimentally increased by
psychological stress) and exogenous (increased with implants)
sources of corticosterone reduced feather quality in European
starlings, particularly in rectrices. However, Fairhurst et al.
(2014) found a negative correlation between corticosterone
levels and the formation of fault bars in wild common
redpolls (Acanthis flammea); moreover, feathers with higher
corticosterone levels had wider growth bands and those
birds had redder plumage, both of which may suggest that
corticosterone enhances food finding and the mobilization
of body stores for feather growth.
Much less is known about the role of corticosterone in the
production of fault bars (Table 1). Using radioimmunoassay,
Bortolotti et al. (2009) found more corticosterone in feather
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Fault bars in bird feathers 9
segments with one or more fault bars than in adjacent
feather segments without fault bars. Also, Patterson et al.
(2014) showed corticosterone levels to be higher in the
distal parts of feathers, which grow first, in Caspian tern
chicks, a pattern that is consistent with fault bars being
more frequent in the distal parts of the feathers in nestling
raptors and storks (Machmer et al., 1992; Jovani & Tella,
2004; Jovani et al., 2014). Among other physiological actions,
elevated plasma corticosterone levels are known to increase
protein catabolism (Blas, 2014), potentially reducing keratin
synthesis during feather growth, which could lead to fault
bar formation. Fokidis et al. (2012) found that captive
curve-billed thrashers (Toxostoma curvirostre) provided with
an unpredictable food supply elevated their initial (baseline)
plasma corticosterone, but decreased their stress-induced
levels (in response to 30 min of handling and restraint)
compared to control birds with constant access to food.
Interestingly, birds in the variable-feeding group developed
five times more fault bars, which may suggest that baseline,
but not stress-induced, corticosterone elevations induced
fault bar formation.
Overall, corticosterone is a promising candidate
mediator between environmental perturbations (e.g.
weather, predation risk, actual predation attempts) and other
proximate factors of fault bar production (e.g. age, disease).
However, much more research is needed to understand the
role of the hypothalamic–pituitary–adrenal axis on feather
development in general, and on fault bar formation in
particular. For example, no study has tested the effects
of other avian hormones involved in the adrenocortical
response to stress [e.g. corticotropin-releasing hormone
(CRH), arginine vasotocin (AVT), adrenocorticotropic
hormone (ACTH)] on fault bar formation (J. Blas, personal
communication). Some of these hormones could have a more
direct role in fault bar production than corticosterone, such as
disrupting cell membrane physiology, which might not allow
the accumulation of keratin, or altering cell to cell adhesion
in the follicle collar, which could induce keratinocytes to
separate during feather generation and create a fault bar.
Again, the evolutionary interpretation of a potential role
of corticosterone in the production of fault bars would be
that increases in blood titres of corticosterone are a beneficial
stress response, and that fault bars are either the unavoidable
consequence of this stress response or that reduced keratin
deposition mediated by corticosterone is a stress response
that lowers energy consumption by processes such as feather
growth that are not vital in an emergency situation. More
studies on the role of corticosterone on the formation of fault
bars are strongly encouraged.
(5) Habitat
Habitat features may also change fault bar propensity. In a
fully crossed experimental design Witter & Lee (1995) found a
higher occurrence of fault bars in captive European starlings
housed in cages without cover; treatments were cages with
or without vegetation cover and food positioned near or far
from the cover. The authors suggested that the perceived risk
of predation in the habitat was behind fault bar abundance.
In addition, differences have been reported between habitats
in six out of eight correlative studies on fault bar occurrence
(Table 1), and most of these studies argued that habitat
resources (mainly food) were behind these results. While food
differences may actually be a causal factor in some of these
studies (e.g. Blanco, Laiolo & Fargallo, 2014), we are more
inclined towards the interpretation of Witter & Lee (1995)
that psychological stress linked to reduced vegetation cover
and increased risk of predation may underlie these results.
In fact, correlative studies seem to support this hypothesis
because birds carried more fault bars in regenerating forests
(Sodhi et al., 2005), in habitats with less vegetation cover
(Griesser et al., 2006; Eggers & Low, 2014), and in more
fragmented habitats (Sodhi, 2002). Similarly, Fokidis et al.
(2012) found that the same amount of food delivered to
captive birds increased the number of fault bars if it was
delivered in an unpredictable way. It would appear that
psychological factors, and not resource abundance, per se,
could explain the differences between habitats.
VIII. OVERVIEW
So many specific factors affect the expression of fault bars
that a brief overview of some of the more important trends
in Table 1 seems merited. Concerning ultimate, selective
factors, differences between feather tracts in the prevalence
of fault bars have been recorded in 19 of 20 studies,
strongly attesting to selection having modified the propensity
of different feather groups to form fault bars. The high
prevalence of fault bars in the rectrices is consistent with
predation attempts being the primary stressor causing their
formation and the rectrices often being ejected in fright
moults. There is a surprising shortage of studies reporting
species differences (N=4) and relating fault bar prevalence
with species predation pressure (N=1); however, five of six
studies have found individuals with more fault bars to be less
likely to survive. Concerning proximate factors that modify
the likelihood that a stressor will result in the formation of
a fault bar, age is the only clearly confirmed factor, with 14
of 15 studies showing young birds to have more fault bars
than adults. However, three additional contingencies have
reasonable cross-study support for affecting the likelihood of
fault bar expression: corticosterone, disease, and habitat. Sex
and malnutrition have been addressed in good numbers of
studies but neither factor seems clearly associated with fault
bar formation. Table 1 also clearly demonstrates the serious
shortage of studies treating the specific follicular mechanism
that generates fault bars in growing feathers. Current
understanding suggests that the most likely mechanism
is strong contraction of the follicular muscles associated
with fright stress, but this awaits further study. Finally, of
the specific stressors that may generate fault bars, only
handling stress has been reasonably well studied, with seven
of nine studies finding an effect of observer handling, which
presumably resembles the stress of a predation attempt.
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10 Roger Jovani and Sievert Rohwer
Fig. 1. Model of the interaction between propensity of a feather
follicle to produce fault bars (x-axis), the strength of the stressor
(plotted lines) and the resulting fault bar severity (y-axis). Note
that the x-axis may account for different scales (differences in
fault bar propensity between feathers, individuals or species).
Fault bar propensity is shaped by ultimate (see Section IV)
and proximate (see Section VII) factors. See Section IX for
explanation of numbers (1–4) and letters (A, B).
IX. MECHANISTIC MODEL
(1) The model
Below, we propose a way to use our classification of factors
behind fault bar formation (propensity shaped by ultimate
and proximate causes, and stressors) to build a model of
their formation (Fig. 1). This approach aims to explain the
formation of a fault bar of a particular severity (y-axis) as a
function of the interplay between the likelihood of producing
a fault bar by a given feather follicle (x-axis) and the strength
of the perturbation producing the fault bar (curves within
Fig. 1). It is important to note that the x-axis in Fig. 1
applies to a particular feather follicle that is generating a new
feather. As stated above, this propensity has been shaped
through evolution according to the species and according
to the feather group and the position of the follicle within
the feather group. Moreover, this propensity is fine-tuned
by proximal factors affecting the individual bird (e.g. age,
disease, habitat). Thus, the x-axis of Fig. 1 could be equally
used to understand differences in fault bar occurrence among
the feathers either of an individual bird (e.g. from proximal
to distal wing feathers), or among birds within species (from
diseased to healthy individuals), or among species (from
resident to migrant species; see Møller et al., 2009). The
model was built taking into account the following biological
facts.
First, fault bars are not a binary phenomenon (Machmer
et al., 1992). As explained above they are classified according
to their severity as light, moderate and severe, where severe
fault bars often result in breakage of parts or the entire
feather. Although the conceptual diagram shows fault bar
severity as a continuous variable (as it actually is), we also
show severity bins that link to (light, moderate, severe)
categories in earlier literature. Moreover, two thresholds
indicated by dashed horizontal lines are shown in Fig. 1.
Below the lower threshold fault bars would be too mild to be
detected with the naked eye. Above the upper threshold, fault
bars would be so serious that the rachis would immediately
break at the fault bar line.
Second, stressors also are not a binary phenomenon, but
may range from very mild to very strong. For instance, an
interaction with a predator may range from the observation
of a predator flying nearby up to being restrained and injured
by the predator before escaping. Examples of stressors of
different intensities are indicated by the different curves in
Fig. 1, ranging from mild stress events (light lines) up to
strong stress events (dark lines).
Moreover, the diagram is built upon four axioms. Clearly,
stressors apply only to individual birds, but fault bar
propensity (x-axis) varies across different groups of feathers,
as well as different groups of individuals (such as age classes,
or birds in different habitats), and different species sharing
relevant physiological and ecological traits, or selective
history. For simplicity we explain the four axioms used
to frame the model (as numbers in Fig. 1) with reference
to individuals. In the top region of the graph (1), an
extraordinarily strong stressor could produce a severe fault
bar that would break the feather in almost any bird, even
in a bird with a low propensity to develop fault bars. At
the opposite extreme (2), a very weak stressing event would
rarely produce a fault bar, and if so, it would be so mild
that it might not be noticed. The right-hand region of
the graph (3) represents extremely susceptible individuals
that will produce severe fault bars when experiencing even
a mild stress. Finally, the left-hand region of the graph
(4) represents individuals that will not develop fault bars
even when confronted with extremely stressful events. While
theoretically possible, some of these extreme scenarios may
not occur in nature (e.g. extreme fright might kill the bird
before a fault bar can be produced), but including the
extremes makes the diagram general.
(2) Empirical findings explained by the mechanistic
model
The family of curves presented in the figure illustrates how
the feathers of different species may respond differently to
different stressors. Rectangle A, on the right side of the
propensity axis crosses the same four stressor intensity lines
as rectangle B on the left side of the axis, but the severity
of the fault bars produced differs greatly. For example, a
bird in rectangle A could show large differences in the
frequency of fault bars and in the damage they caused
according to stress intensity, while no difference in these
parameters might be found for a bird receiving similar
stressors that fell in rectangle B on the x-axis. Thus, the
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Fault bars in bird feathers 11
failure of an experimental stressor to produce fault bars could
mean either that the species, individual, or feather tract is
not prone to fault bar production, or that the intensity
of the experimental stress was not sufficient to result in
fault bars.
By following one of the mild stress lines from left to
right in Fig. 1, one sees what is often found across feathers
of the same feather tract that are growing simultaneously
and thus simultaneously affected by a given acute stressor.
Many studies report that simultaneously growing nestling
feathers vary in their response to single stress events from
not developing a fault bar to developing a severe fault bar
that breaks the feather (e.g. Jovani & Blas, 2004). Thus,
among feathers of the same individual the entire x-axis can
be involved.
It has also been reported that the same severe stress, such
as capturing and handling a bird, can produce fault bars in
almost any experimental bird (King & Murphy, 1984); this
would correspond to the dark stress lines in Fig. 1, producing
a fault bar even in individuals with low propensity to develop
them. However, it may also be the case that the stress was
actually less severe, but that all experimental birds had a
high propensity for developing fault bars. In fact, Witter
& Lee (1995, p. 306) noted that, while King & Murphy
(1984) considered handling as the cause of fault bars, their
birds were part of a malnutrition experiment, which may
have ‘heightened the sensitivity to handling stress’. Murphy
et al. (1988, p. 1411) later recognized that their experimental
diets deficient in sulfur-containing amino acids may have
increased ‘the likelihood that the shock of handling resulted
in fault-bar formation in some birds’. In other words, they
may have shifted individuals to the right of the x-axis in
Fig. 1, such that even a moderate handling stress produced
fault bars in all birds.
In general, the severity of fault bars is inversely related
to their abundance (Table 2). It could be argued that this
is the direct (linear) consequence of strong perturbations
being less common than lighter ones. However, Fig. 1
suggests that the relationship between fault bar propensity
and realized fault bar severity could be non-linear,
and thus that the abundance of fault bars of different
intensities may not mirror the relative abundance of
perturbation intensities. The frequency distribution of the
stress intensities experienced by birds growing feathers
might be possible to estimate if the model could be
parameterized.
This model also explains why a factor, even if relevant,
may be found to have no effect in correlative or experimental
studies, thus leading to often-contradictory conclusions
among studies. For instance, nestling pied flycatchers have
been reported to lack fault bars while nestlings of other species
are highly prone to fault bars (Kern & Cowie, 2002). This
need not mean that age is unimportant, or that there was a
lack of perturbations. For instance, nestling pied flycatchers
likely have little predisposition to develop fault bars because
they migrate long distances using juvenile flight feathers
(Møller et al., 2009).
(3) Knowledge gaps revealed by the model
Figure 1 highlights information that was not found in our
review of the causes of fault bar formation, thus suggesting
new research avenues. Surprisingly, only a few studies (e.g.
Negro et al., 1994) examined the consequences of different
stress intensities on the formation of fault bars. Further, many
studies focus on factors that modify the propensity to produce
fault bars without also including an intense stressor event,
such as handling, that could be expected to generate the
acute fright that seems required to stimulate the formation
of fault bars.
Perhaps the largest knowledge gap that Fig. 1 highlights
is that no study has addressed how stress intensity and
the propensity to develop fault bars interact to create fault
bars of different severity. An array of factors affecting the
likelihood of fault bars forming in response to acute stress
have been studied, and several of these modifiers were found
to increase the likelihood of fault bars being formed in
one or more studies (Table 1). Nonetheless, most of these
studies focused on only one or a few of these modifiers and
treated them as independent and additive, without looking
for interactions between modifiers that affect the likelihood
of fault bar formation. The relationship between stress
intensity and the development of fault bars could be studied
experimentally by modifying both the intensity of the stressor
and the modifying factors leading to different fault bar
propensities. For instance, an experimental approach could
test the interaction between different stress intensities applied
to individuals with different treatments of corticosterone
implants, and then measure fault bar severity on individuals.
X. ECOLOGICAL AND EVOLUTIONARY
CONSEQUENCES OF FAULT BARS
Plumage is key to understanding avian ecology and evolution
because it serves a diversity of functions, including flight,
signalling, camouflage, and thermoregulation. Because fault
bars may compromise these functions it is not surprising
that current evidence clearly shows that the propensity to
develop fault bars between different feather groups and
between different ecological and life-history categories of
species has been shaped by natural selection. However, the
most fundamental question surrounding the existence of
fault bars is why fault bars are found in most bird species,
given that the propensity for them to form can be lowered
by selection and that they are so clearly costly. Above we
argued that fault bars are likely a harmful by-product of some
other adaptation that carries benefits sufficient to outweigh
their costs. This raises an important and related question.
In those groups of feathers and species where the propensity
to develop fault bars has been reduced (e.g. because of
high predation pressure; Møller et al., 2009), have there
been trade-offs that have compromised fitness as a result of
suppressing the expression of fault bars? For example, if fault
bars are associated with muscle contractions used to expel
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12 Roger Jovani and Sievert Rohwer
Table 2. Percentage of fault bars of different severity. N=number of fault bars inspected
Species Feathers Age Light Moderate Severe NRefs.
White stork (Ciconia ciconia) Wing Adult 72 21 7 235 Jovani & Blas (2004)
White stork (Ciconia ciconia) Wing Nestling 57 27 16 1,120 Jovani & Blas (2004)
Sandhill crane (Grus canadensis) Wing Adult 78 14 7 4,676 Jovani et al . (2010)
Swainson’s hawk (Buteo swainsoni) Wing Unknown 56 35 9 724 Sarasola & Jovani (2006)
Feral pigeon (Columba livia) Wing Adult 69 28 3 2,533 Unpublished raw data from Jovani et al.
(2014)
Feral pigeon (Columba livia) Wing Young 55 42 3 855 Unpublished raw data from Jovani et al .
(2014)
Feral pigeon (Columba livia) Tail Adult 70 29 1 4,803 Unpublished raw data from Jovani et al .
(2014)
Feral pigeon (Columba livia) Tail Young 53 45 2 1,556 Unpublished raw data from Jovani et al .
(2014)
feathers during fright moults, then is it the case that those
species that are less likely to produce fault bars (because
wing gaps reduce flight ability) are less likely to escape when
caught by a predator (i.e. because they cannot undergo fright
moults)?
Because fault bars are only formed when feathers
are growing, strategies to reduce the probability of
encountering certain environmental stressors, and to reduce
individual propensity to fault bars (e.g. improving general
body condition) during moult should be adaptive. While
non-moulting birds reduce their heart and metabolic rate
at night, moulting birds maintain similar rates throughout
the day and night, and are much less responsive when
challenged by a stressor (Cyr, Wikelski & Romero, 2008).
Apparently elevated night-time metabolism keeps feather
growth rate continuously high, which limits time in moult
and damage to growing feathers generated by fault bars.
We also know that corticosterone levels are depressed during
moult compared to during the breeding period (Romero,
Soma & Wingfield, 1998; Cornelius et al., 2011) and this
likely reduces the propensity for acute stressors to generate
fault bars because high corticosterone titres are correlated
(not implying causality) with fault bar formation. Pap et al.
(2007) also suggested that the partial moult of immature
great tits may be an adaptation to replace feathers with more
fault bars. Thus, recently fledged great tits had more fault
bars in their tertials and rectrices when they left the nest
than after they had replaced these feathers in the partial,
post-juvenile moult. Finally, fault bars may influence the
evolution of moult rate because house sparrows whose moult
was accelerated by experimentally reducing day lengths had
more fault bars (V´
ag´
asi et al., 2012).
Fault bars may also give us insight into subtle differences
in the role of feathers in bird flight. While there are
general patterns, such as rectrices having more fault
bars than remiges (see Section IV), fault bar distribution
patterns vary among species (Riddle, 1908). For instance,
a W-shaped distribution pattern of fault bars is found in
the tail of barn swallows (Serrano & Jovani, 2005) and
an inverse V-distribution is found in the tail of ospreys
(Machmer et al., 1992). Such differences suggest that natural
selection has fine-tuned the propensity to produce fault
bars according to functional importance among feathers
within feather tracts. If the distribution of fault bars across
flight feathers informs us about their relative importance
in flight (e.g. Jovani & Blas, 2004), further comparative
studies of fault bar distributions may help understand the
relative importance of different flight feathers across bird
species.
Lastly, Riddle (1908, p. 336) stated that he found fault bars
‘everywhere, indeed, that I have looked for them except in
fossil feathers, artists’ drawings, and journals of ornithology!’
Given that almost all extant bird species have fault bars,
it seems extremely unlikely that fault bars are not present
in fossil feathers. This should be studied by systematically
screening fossil feathers for fault bars and by analysing
the microstructure of fossil feathers to compare them with
non-fossilized feathers with fault bars. We could also study
how fault bars behave during fossilization using current
techniques to simulate feather fossilization (McNamara et al.,
2013). This would allow us to determine whether fault bars
become hidden during fossilization and, if so, to determine
whether the distribution of fault bars along the wing/tail
feathers of primitive birds could inform us about the early
evolution of bird flight.
XI. CONCLUSIONS
(1) This review classifies information from past studies of
fault bars into three functional categories that affect their
expression in growing feathers: selective factors shaping the a
priori propensity that a feather follicle will produce a fault bar,
acute stressors that are capable of triggering the production
of a fault bar during feather growth, and a series of modifying
factors of the likelihood that an acute stressor will trigger
the formation of a fault bar. We present a graphical model
that illustrates how these three factors interact to produce
fault bars of varying severity. Experimental studies aimed
at testing this model with an array of potential stressors are
needed.
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Fault bars in bird feathers 13
(2) Because fault bars are costly, natural selection seems
to have lowered their occurrence when the benefit of the
underlying adaptation that causes them to be formed is
lower than the cost of the feather damage they cause. If,
as we suggest, the general explanation for the persistence
of fault bars is that they are an unfortunate by-product of
some other important adaptation (King & Murphy, 1984),
then testing this by-product hypothesis would seem to be the
most important next step in solidifying out understanding
of fault bars. Are they, in fact, generated because fright
moults serve so effectively in escaping predator attacks,
or is there some other more plausible adaptation that
may be responsible for their persistence in the face of
the high survival costs they impose through damaged or
broken feathers? In short, is this alternative adaptation fright
moult, as King & Murphy (1984) proposed and as we also
suggest to be true, or is it something else? Recognizing and
confirming the validity of this underlying adaptation seems
to be key to satisfactorily understanding why fault bars exist
at all.
(3) If fright moults are the underlying adaptation that
force the existence of fault bars, then we should expect to
see a strong correlation between the incidence of fault bars
and the propensity to undergo fright moults. This prediction
seems well supported by the strong association between
the propensity to lose the rectrices in fright moults (Juhn,
1955; H¨
oglund, 1964; Møller et al., 2006) and the much
higher frequency of fault bars in the rectrices than in the
primaries. It needs to be evaluated further across species
where the costs and benefits of sacrificing the rectrices
to escape predation can be predicted by other life-history
variables, such as residency versus migration and relative
vulnerability to predation. An impediment to such studies
has been the difficulty of assembling comparative data on
differences in the frequencies of fright moult across bird
species. Fortunately, this impediment has been removed by
the valuable index proposed by Møller et al. (2006). Thus it is
now feasible to correlate the propensity of species to undergo
fright moults with the incidence of fault bars in the rectrices,
which can easily be measured in museum specimens or in
netted birds. Such comparative studies should give us more
insight into the validity of the hypothesis that fault bars
have not been eliminated in some avian lineages because the
follicular contractions that make fright moults possible also
generate fault bars in growing feathers.
XII. ACKNOWLEDGEMENTS
R. J. is supported by a Ram´
on y Cajal research contract
(RYC-2009-03967) from the Ministerio de Ciencia e
Innovaci´
on and acknowledges support from the Spanish
Severo Ochoa Program (SEV-2012-0262). David Serrano,
Santi Guallar, Csongor I. V´
ag´
asi and two anonymous
reviewers provided interesting comments on an early
draft of the manuscript. Julio Blas substantially improved
corticosterone-related paragraphs.
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XIV. SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of this article.
Appendix S1. Detailed account of each reviewed study.
Table S1. Summary of the 74 reviewed studies.
Table S2. Synthesis of Table S1 showing, for each analysed
factor, evidence in favour or against an effect of fault bar
formation, broken down into the different approaches.
(Received 9 September 2015; revised 9 March 2016; accepted 14 March 2016 )
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