Fault bars timing and duration: the power of studying feather
fault bars and growth bands together
Roger Jovani and Javier Diaz-Real
R. Jovani (jovani@ebd.csic.es) and J. Diaz-Real, Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas (CSIC), Américo
Vespucio s/n, ES-41092 Sevilla, Spain.
Growth bands and fault bars, widespread features of feathers that form during regeneration, have largely been studied
independently. Growth bands result from normal regeneration: each pair of dark/light bands forms every 24 h. Fault bars
are a response to stress during regeneration, creating a translucent line that can break the feather. We studied the relative
position and width of these two structures in feathers of nestling and adult white storks Ciconia ciconia. We first confirmed
that one growth band represents 24 h of feather regeneration. Fault bars did not occur at random within growth bands:
65.7% (in nestlings) and 45.6% (in adults) of them occurred in one out of six defined segments within a growth band,
namely that segment corresponding to the first one-third of night time hours. The width of fault bars relative to growth
bands suggested that fault bars were produced during a median (range) of 7.0 h (2.7–27.0) in nestlings and 3.7 h (1.8–7.9)
in adults. Fault bars were concentrated at feather tips in nestlings, but at central locations in adult feathers. Our results
suggest that, in general, fault bars are a discrete event of a finite duration occurring mainly during the night (particularly
in nestlings). This, along with current knowledge, suggests that acute stressors, rather than chronic ones, are responsible
for fault bar formation. Thus, such acute punctual stressors (a matter of minutes) can have long-lasting (months–years)
physiological effects due to the wing load increase from feather breakage caused by fault bars.
Growth bands are pairs of subtle, alternating, dark/light
bands perpendicular to the feather axis along the entire
length of a feather with an appearance similar to watermarks (Riddle 1907, Michener and Michener 1938, Grubb
2006, Jovani et al. 2011). A growth band forms every 24 h
(less in some cases; Results) during normal feather regeneration. Despite a lack of a 1:1 correspondence between
photoperiod and the light/dark width ratio, the light band
is produced during the night, and the dark band during
the day (Jovani et al. 2011 and references therein). This
circadian origin of growth bands suggests their link to bird
body condition: the better the bird’s nutritional status, the
wider the growth bands (Riddle 1908, Wood 1950, Grubb
1989, 2006).
Fault bars are also widespread in feathers, but indicate
abnormal regeneration (dysmorphogenesis). Like growth
bands, they lie perpendicularly to the feather axis. They can
be as minor as a slight notch on the feather surface (‘light’
intensity) or so severe as an absence of barbules allowing
one to see through the feather (‘medium’ and ‘strong’ intensities, following Sarasola and Jovani 2006). All hypotheses
attempting to explain fault bar origin consider some stressor as the cause. However, they differ on the nature of the
stressor. Malnutrition was independently proposed by
Riddle (1908) and Michener and Michener (1938) as the
cause of fault bars. This idea held until Murphy and King
(1982) did detailed experiments with synthetic food, showing that malnutrition, per se, did not produce fault bars,
but that bird handling during the experiments caused the
fault bars (King and Murphy 1984, Murphy et al. 1988).
More recent studies also have excluded malnutrition as a
cause of fault bars. An experiment with American kestrel
Falco sparverius nestlings showed that food deprivation produced no increase in fault bar number, but nestling handling
did (Negro et al. 1994). Providing captive European starlings Sturnus vulgaris with food and water ad libitum, but
changing the availability of dense shrubs for hiding produced an increased abundance of fault bars in aviaries
without shrubs, also challenging the malnutrition hypothesis (Witter and Lee 1995). However, despite human
handling and failed predation attempts occur in the wild,
it seems highly unlikely that they may account for the
widespread occurrence of fault bars in wild birds. Therefore, a general explanation of the causes producing fault bars
remains elusive. Whatever the cause of fault bars what we do
know is that fault bars often result in partial feather damage or even complete breakage (Sarasola and Jovani 2006).
Broken feathers are not replaced until the next moult (as
opposed to plucked feathers, the replacement of which is
initiated immediately), and experimental reduction of wing
area is known to increase energetic demands resulting in
direct fitness costs as reflected in lower reproductive success
97
(Mauck and Grubb 1995, Velando 2002). Therefore, understanding when and for how long are fault bars produced is
a missing piece of knowledge with implications for our
understanding of bird biology and on the potential implications of fault bars in bird plumage evolution.
In summary, growth bands and fault bars in feathers
reflects normal and abnormal feather regeneration, respectively. Until now, the two have been studied as independent
sources of information: growth bands as proxies of feather
growth rate (Grubb 2006), and fault bars about stressors
(Bortolotti et al. 2009). Also, studies trying to understand
the very nature of these structures have focused on one
or the other structure (Murphy and King 1991, Jovani
et al. 2011), but rarely on both (Riddle 1907, 1908). We
propose that studying growth bands and fault bars together
could provide a new way to study the potential intimate
relationship between the two (Riddle 1907, 1908), answer
basic questions on fault bar formation, and provide new
information on avian biology. Specifically, our questions
were 1) do fault bars occur randomly within growth bands,
and if not, when are they most abundant within the circadian formation of growth bands? 2) When are fault bars
produced during feather regeneration? 3) How wide are
fault bars relative to growth bands? 4) If phenomena in these
contexts differ between nestling and adult birds.
When are fault bars formed?
We cut off the third scapular feather from a sample of
100 nestlings. Also, during our incursions into the colony
in June 2003, we collected from the ground freshly moulted
primary, secondary and scapular wing feathers. These
were considered to be adult feathers (see detailed justification in Jovani and Blas 2004). In the laboratory, we selected
feathers having at least one fault bar within a conspicuous
growth band (i.e. sometimes growth bands were difficult
to detect in some feather portions). To quantify this, we
partitioned the growth band into six imaginary, equallysized, arbitrary segments perpendicular to the longitudinal feather axis (Fig. 1). The first feather portion grown is
the tip. Within growth bands, the dark section is produced during the day and the light section during the night
(Introduction). Therefore category 4 (Fig. 1) roughly corresponds to the hours after sunset (Riddle 1907, 1908).
(a)
Growth band
1
2
3
4
5
6
Methods
Does one growth band equal 24 h?
We tested whether white storks conform to the general
rule (Jovani et al. 2011) that one growth band is produced
every 24 h during feather regeneration. This was an important prerequisite to the study as a few exceptions to the
rule have been found (Langston and Rohwer 1996, Kern
and Cowie 2002). On 3 June 2006 we measured the
third scapular (see a detailed schematic of feather position in
Jovani and Blas 2004) of nine nestlings with a ruler (nearest 1 mm). We repeated the measurement at the same time
eight days later and then cut off the feather at its base. In
this way, we calculated the average daily growth rate of
the feather as (second measure – first measure)/8. Later in
the laboratory, we measured a median (range) of 4 (2–6)
growth bands with a caliper (nearest 0.01 mm) directly
from the feather as closely as possible to the cut base to
compare the mean width of the growth bands with the daily
feather elongation. Our expectation was that the width
of the growth bands was equal to the daily growth rate of
feathers.
98
Fault bar
Feather growth direction
(b)
sunset
75
% fault bars
We employed feathers from nestling and adult white
storks Ciconia ciconia, an especially suitable species by virtue of its long feathers with abundant fault bars (Jovani
and Blas 2004) and conspicuous growth bands of considerable width. Field work was performed during the
2003 breeding season at the Dehesa de Abajo site (Puebla
del Río, Sevilla, SW Spain; 37°13′N, 6°09′W), where
ca 250 pairs of white storks nest colonially on wild olive
trees (see further details in Jovani and Blas 2004, Jovani and
Tella 2004).
50
25
0
1
2
3
4
5
6
Position within growth band
Figure 1. (a) Diagram showing the six arbitrary segments designated to record the position of fault bars within growth bands. A
pair of dark-light bands comprises a growth band. Because feathers
grow from the tip to the proximal feather section, and the light
sections are produced during the night, a fault bar in growth band
positions 1–3 is produced during the day, and one occurring
in position 4 would be produced in the first hours of the night. In
(b) it is shown the proportion of fault bars occurring in each of the
six arbitrary segments within growth bands of nestlings (white bars)
and adults (black bars).
Since we have previously shown (Jovani et al. 2011) that
the ratio of dark/light width is independent of photoperiod,
the transition between the light and the dark portion is
more difficult to allocate to a particular moment of the
day. When a fault bar occupied more than one category we
recorded the category best describing the midpoint of the
fault bar. We inspected feathers by holding them by the calamus with the dorsal side inclined at ca 20–45° towards natural indirect sunlight. Fault bars were identified and classified
as light, medium or strong following Sarasola and Jovani
(2006). Independent of fault bar strength, we selected examples for which we could record fault bar position within the
growth band with confidence. We found at least one such
fault bar in 55 of the 100 nestling feathers.
In nestlings, 83.3% of fault bars were scored medium or
strong (n 114 fault bars, n 55 feathers), but only 29.3%
were so in adults (n 58 fault bars, n 26 feathers). In nestlings, fault bar intensity was not related to position within the
growth band (PROC FREQ, c2 10 11.00, p 0.357, n 105
fault bars); there was not a large enough sample size to test this
in adults. Also, the proximity of the fault bar to the feather tip
was not related to its position within the growth band (PROC
CORR, Spearman r 20.151, p 0.125; n 105 fault
bars). Therefore, we pooled fault bars of different strengths
when analysing their position. Overall, we located the position
within growth bands of 105 fault bars from nestlings (n 55
feathers) and 57 fault bars from adults (n 26 feathers). Moreover, from the 55 nestling feathers we calculated feather length
and the distance of each fault bar to the tip (whether or not
the fault bar was used to study its position within the growth
band). The same analysis was done for 36 adult scapular feathers. We divided each feather into 25 mm sections starting from
the tip (i.e. 0–25, 26–50, etc.). For each section, we calculated
the proportion of feathers with at least one fault bar in the
section. This variable was compared between ages along the
feather with a generalized linear model with binomial probability distribution (PROC GENMOD). We also tested whether
the number of fault bars differed between ages and feather sections with a generalized linear model with Poisson probability
distribution (PROC GENMOD). Only feathers long enough
to be contributing to a given feather section were used in the
calculations; i.e. a 0 meant that the feather had no fault bar in
the section, given that the feather was long enough to potentially have a fault bar in the section.
For how long do fault bars form?
From these same feathers (cut scapulars from 100 nestlings and
adult feathers collected from the ground) we selected mediumstrong fault bars (following Sarasola and Jovani 2006) to measure the time elapsed during fault bar formation because they
reflect a clear period of dysmorphogenesis. Because light fault
bars are merely a simple pinch on the feather surface, comparing their width with that of medium-strong fault bars would
be misleading. Moreover, we only studied fault bars that had
at least one growth band nearby easy to measure and representative of the feather portion in which the chosen fault bar
occurred. Since we confirmed that white storks follow the
general rule that one growth band corresponds to 24 h of
feather regeneration (Results) we estimated the number of
hours elapsing during fault bar formation as (maximum fault
bar width/mean growth band width) 24 h. To do so, we
measured the maximum width of these fault bars along the
long feather axis as well as the mean width of adjacent growth
bands with a calliper (nearest 0.01 mm). Overall, for 50 nestling feathers we measured widths of 95 fault bars and a median
(range) of 3 (1–8) growth bands around them. The same was
done for 17 fault bars from 14 adult feathers; median (range)
growth bands measured 3 (2–6). SAS 9.2 (SAS Inst.) was
used for all analyses (used SAS procedures are indicated at
first appearance). We used unequal variance t-tests following
Ruxton (2006) when appropriate.
Results
Does one growth band equal 24 h?
For the third scapular of nine nestlings the mean (SD, range)
growth rate was 5.6 (1.2, 4.0–7.1) mm d21, and the mean
width of growth bands was 6.0 (1.1, 3.7–7.6) mm d21.
That is, mean growth band width was only 0.4 mm wider
than the growth rate of the feather, a non-significant difference (PROC TTEST, two independent samples Satterthwaite t-test, t15.97 20.89, p 0.386), and there was no
systematic difference between growth band width and daily
feather growth rate within feathers (paired t-test, t8 0.90,
p 0.393). The alternative hypothesis would be that two
growth bands (two pairs of light-dark growth bands) are
produced every day, according to previous findings in laysan albatross Phoebastria immutabilis (Langston and Rohwer
1996) and nestling pied flycatchers Ficedula hypoleuca (Kern
and Cowie 2002). In our specific case, the average growth
band would be 5.6/2 2.8 mm wide, but growth bands
clearly departed from this ‘one growth band 12 h’ hypothesis (one-sample t-test, t8 8.75, p 0.0001).
When are fault bars formed?
Fault bars were found in any position within growth
bands, but the first third of the light portion accounted
for 65.7% of the fault bars in nestlings (c2 5 185.46,
p 0.0001) and 45.6% in adults (c2 5 38.05, p 0.0001;
Fig. 1); note that under a perfect even distribution only
16.6% of the fault bars would occur in this position. More
generally, fault bars were highly concentrated in the light
portion of the growth bands of nestling feathers (86.7%;
c 2 1 56.47, p 0.0001), while a slighter bias occurred in
adults (64.9%, c2 1 5.07, p 0.0243; Fig. 1); note that an
even distribution would yield 50%.
Fault bars were more concentrated towards the feather
tip in nestlings, while the probability of harbouring a fault
bar was higher at the central sections of the adult feathers
(PROC GENMOD, feather section age: c29 46.68,
p 0.0001; Fig. 2a). Very similar patterns were found for
the number of fault bars per feather section (feather section age: c2 8 85.33, p 0.0001; Fig. 2b).
For how long do fault bars form?
Nestling fault bars were estimated to be growing during
a median (range) of 7.0 h (2.7–27.0), slightly departing from
99
25
0.8
20
0.6
15
0.4
10
0.2
0.0
(b) 2.5
Mean number of
fault bars
2.0
5
0
10
1.5
8
1.0
6
0.5
Adults
4
226–250
201–225
176–200
151–175
126–150
101–125
51–75
76–100
0–25
26–50
0.0
Feather section (mm; 0=tip)
Figure 2. Occurrence of fault bars at different times during
feather regeneration (the tip is the first part of the feather to regenerate). Proportion (SE) of feathers harbouring at least one fault bar
in each feather section (a). Mean (SE) number of fault bars in each
feather section (b). In both panels, only feathers contributing
to each feather section (not all feathers were of the same length)
were used for the calculations. The number of nestling feathers
(white dots; from left to right) was: 55, 55, 55, 52, 50, 46, 40,
22, 5, and 2; adults (black dots): 36, 36, 36, 36, 36, 35, 22, 8, 1,
and 1.
a normal frequency distribution (PROC UNIVARIATE,
Kolmogorov–Smirnov D 0.103, p 0.014; skewness
2.36; Fig. 3). Excluding the largest value, the distribution did not depart from normal (Kolmogorov–Smirnov
D 0.080, p 0.148; skewness 0.66). Adult fault bars
showed a much reduced range of values, with a median
(range) of 3.7 h (1.8–7.9) and did not depart from a normal
distribution (Kolmogorov–Smirnov D 0.185, p 0.122;
skewness 0.673; Fig. 3). Nestling fault bars were wider
than those of adults (Satterthwaite t-test, t37.123 5.65,
p 0.0001). The same conclusion was obtained when only
scapulars were compared (Satterthwaite t-test, t27.098 4.74,
p 0.0001).
Discussion
Fault bars did not occur randomly within growth
bands, but were highly concentrated at the beginning of
the formation of the light growth band (during the first
hours of the night according to current evidence, see
Introduction). This could be a simple by-product of the
two (the formation of the fault bar and the beginning of the
100
Nestlings
30
Number of fault bars
Proportion of feathers with
at least one fault bar
(a) 1.0
2
0
0
4
8
12
16
20
24
28
Growth time (hours)
Figure 3. Fault bar duration (hours) in nestlings and adults.
formation of the light growth band) being produced simultaneously because of a third causative factor, or it could
denote an intimate developmental connection between
them. Interestingly, one hypothesis posed by Riddle (1907,
1908) suggests that fault bars (particularly his ‘types one and
three’ defects) are the extreme manifestation of the same
underlying phenomenon that also creates growth bands (his
‘fundamental bars’), namely, the circadian fluctuations of
blood pressure. As the lowest pressure in birds was said to
occur in the first hours of the night, if it was especially low
on a particular night, this would produce follicular collapse
and thus a fault bar as the result of defective keratinization.
Our results partially support this hypothesis suggesting a
developmental connection between growth bands and fault
bars. However, frequent fault bar occurrence in locations
other than those predicted by Riddle’s hypothesis suggests
that other processes could be involved. In any case, our
approach comparing growth bands and fault bars promises
to be a suitable way to better understand the potential connection between the two, and suggests that a good starting
point would be to investigate why (developmentally, physiologically, behaviourally, ecologically) the first hours of the
night are so prone to the creation of fault bars.
The relatively good fit of time taken to form a fault
bar to a normal frequency distribution (if we exclude the
single exceptionally wide fault bar; Fig. 2) suggests that it
is a discrete phenomenon. This is interesting because
stressors for birds can span from seconds (escaping from a
predator) or minutes (a severe territorial fight) to hours (an
intense storm), days (the acute stage of parasite infection),
or more. However, our study shows that fault bars either
occur or do not occur, and when they occur they are of a
specific size range, showing a definite mean (Fig. 2). Captive
starlings exposed to 30 min of chronic stress (including
restraint in cloth bag, loud music, human voice, cage moving) four times a day for 20 d, or the same chronic stress
coupled with food deprivation, showed fewer fault bars
than birds exposed to an acute punctual stress consisting of
30 min of restraint in a cloth bag every other day (Strochlic
and Romero 2008). Another study showed that corticosterone levels were higher in feather locations containing a fault
bar than in contiguous locations lacking such (Bortolotti
et al. 2009). Overall, the evidence suggests that fault bars are
not the result of a chronic stress, but that of an acute stressor.
It could thus be speculated that fault bar strength (reflected
in their width) is not related to the duration of the stress, but
rather, to the intensity of the stress (or the intensity of the
response of the bird to the stress).
Broken feathers by fault bars are not replaced until the
next moult (Introduction). Therefore, an acute stress lasting
minutes, or even seconds, could translate into long-lasting
physiological costs over many months or years if this leads
to the formation of a fault bar. This shows the relevance of
further investigating the relationship between stressors and
fault bar formation, and of using the position of fault bars
within growth bands to understand which are these punctual
stressors producing long-lasting flight costs in wild bird.
Fault bars were concentrated in the first third of the light
growth band (Fig. 1). Moreover, we have confirmed here the
‘one growth band 24 h’ hypothesis, and current knowledge
strongly suggests that the light portion is produced during the
night (see details in Jovani et al. 2011). Therefore, fault bar
formation was likely concentrated during the first hours of the
night both in nestlings and adults, but particularly so in nestlings. More generally, fault bars accumulated more often during the night than during the day (particularly in nestlings).
Moreover, nestling fault bars were wider than in adults. This
extends previous studies of the same population where we
found that a) fault bars were more abundant in nestlings, and
that b) nestling mortality was especially high during the first
days of life, sharply declining at older ages when nestlings are
able to thermoregulate (Jovani and Blas 2004, Jovani and Tella
2004). Interestingly, fault bars did not concentrate at the tips
of adult feathers. This shows that accumulation of fault bars on
the tips of nestling feathers (when they are youngest) is not an
artefact implying feather weakness in this feather section and/
or feathers being more prone to dysmorphogenesis. Rather, this
suggests a real connection between stress and fault bar origin.
However, the peak of fault bars in the mid-sections of the adult
feathers is an unexpected result demanding further study.
In conclusion, we have shown that studying the relative position and width of fault bars in the context of growth bands is
valuable in understanding the fundamental nature of both and
can provide new interesting information about avian biology.
Acknowledgements – We are grateful to José Luis Tella for his
support. Julio Blas, Joaquín Lamas, Judit Smits, Gary Bortolotti, José
Luis Tella, Martina Carrete, Raquel Baos, Isa Luque, Mariola Martín,
MaCarmen Roque, Fatima León, Ernesto Fedriani and especially Juan
Manuel Terrero were of great help in the field. Paul F. A. Maderson
made interesting suggestion to an earlier draft of the manuscript. RJ is
supported by a Ramón y Cajal research contract (RYC-2009-03967)
from the Ministerio de Ciencia e Innovación. RJ wants to dedicate
this paper to the memory of Gary Bortolotti. JD-R did this work during a stay at the Estación Biológica de Doñana (CSIC) under an
internship program agreement with the Univ. de Salamanca.
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