Journal of Toxicology and Environmental Health, Part A, 69:1603–1612, 2006
Copyright© Taylor & Francis Group, LLC
ISSN: 1528–7394 print / 1087–2620 online
DOI: 10.1080/15287390500470718
BROOD PATCHES OF AMERICAN KESTRELS ALTERED BY
EXPERIMENTAL EXPOSURE TO PCBS
Sheri A. Fisher1, Gary R. Bortolotti1, Kim J. Fernie2, David M. Bird3,
Judit E. Smits4
1
Department of Biology, University of Saskatchewan, Saskatoon,
Saskatchewan
2
Environment Canada, Burlington, Ontario
3
Avian Science and Conservation Centre, McGill University,
Ste. Anne de Bellevue, Quebec
4
Department of Veterinary Pathology, University of Saskatchewan,
Saskatoon, Saskatchewan, Canada
Captive breeding (n = 25 pairs) and nonbreeding (n = 25) American kestrels were exposed to
a mixture of polychlorinated biphenyls (PCBs) (Aroclor 1248:1254:1260) through their diet of
day-old cockerels. Kestrels ingested approximately 7 mg/kg body weight each day of PCBs, and
this dosage resulted in environmentally relevant total PCB residues in eggs (geometric mean of
34.1 μg/g). An equal number of unexposed birds served as controls. Bare areas of skin known
as brood patches function during incubation to warm eggs; therefore, brood patch size could
potentially influence hatching success, or patches may be a confounding factor in the relationship between poor incubation behavior and hatching failure observed in birds in toxicological
studies. Exposure to PCBs altered the size of brood patches in American kestrels. PCB-exposed
male and female nonbreeders had two of three brood patches that were larger than those of
control nonbreeders. Breeding males exposed to PCBs had smaller patches than controls,
whereas PCB-exposed female kestrels had one larger and one smaller patch than controls.
Patch sizes were not related to total PCB residue levels in eggs of exposed birds. Brood patches
were not related to various incubation behaviors or hatching success in either control or PCBexposed kestrels.
The function of incubation behavior in birds is to keep the eggs near the
optimal temperature for embryonic development. However, parental attendance is not the only factor influencing the warming of the eggs. Since feathers
are a poor conductor of heat, the development of bare areas of skin, known as
brood patches, aids in transferring the body heat of the incubating parent to the
Received 22 June 2005; accepted 18 August 2005.
The authors thank Jerry Huff for developing the electronic balance and Ian Ritchie for his management
and knowledge of the American kestrels at the Avian Science and Conservation Centre. S. A. Fisher thanks
the University of Saskatchewan for financial support through a graduate fellowship. K. J. Fernie thanks the
University of Saskatchewan for financial support through the Isabel María López Martínez Memorial Scholarship. This study was funded by the National Sciences and Engineering Research Council (to G. R. Bortolotti
and J. E. Smits) and the Canadian Network of Toxicology Centres (to G. R. Bortolotti and J. E. Smits).
Address correspondence to Gary R. Bortolotti, Department of Biology, University of Saskatchewan,
112 Science Pl., Saskatoon, Saskatchewan, Canada S7N 5E2. E-mail: gary.bortolotti@usask.ca
1603
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S. A. FISHER ET AL.
eggs (Bailey, 1952). Most bird species develop brood patches during the breeding season on the ventral thoracic and/or the abdominal region of the body
(Jones, 1971). The skin of these regions undergoes feather loss and there is
increased vascularization, edema, and hyperplasia of the brood patch area
(Bailey, 1952; Jones, 1971). In biparental incubators, both males and females
usually develop brood patches, and the number, placement and development
time of the brood patches vary widely across avian taxa (Bailey, 1952; Jones,
1971).
Brood patch development and incubation behavior are under endocrine
control. In birds that develop brood patches by means of a naturally occurring
molt, patch formation is believed to be dependent on changing hormone
levels, which in turn are influenced by incubation behavior (Jones, 1971;
Goldsmith, 1983). Prolactin is the hormone that is most often identified as
being involved in the onset and maintenance of avian incubation (Rosenblatt,
1984; Silver & Ball, 1989; Maney et al., 1999; Sockman et al., 2000) and
brood patch development in a variety of avian orders (Buntin, 1996). A correlation was found between brood patch size and prolactin levels in female
Harris’ hawks (Parabuteo unicinctus) (Vleck et al., 1991); however, prolactin
alone may not suffice. Japanese quail (Coturnix coturnix japonica) injected
with prolactin and estradiol simultaneously showed feather loss and hyperplasia, whereas estradiol or prolactin injected alone resulted in moderate and significant feather loss, respectively (Höhn, 1981). Generally in females, estrogen
enhances prolactin secretion, and estrogen and prolactin act synergistically to
develop the brood patch (Dawson, 1998), whereas in males, testosterone and
prolactin are responsible (Jones, 1971; Goldsmith, 1983). Feedback from contact with eggs is often believed to be important to patch development (Buntin,
1996; Dawson, 1998).
Polychlorinated biphenyls (PCBs) are known to disrupt the functions of the
endocrine system (Koval et al., 1987). Although exposure to PCBs is known to
alter plasma estradiol and testosterone levels (McKinney & Waller, 1994, 1998),
little information exists regarding PCB effects on prolactin. Prolactin levels in
Sprague-Dawley male rats were not altered when the animals were exposed to
PCB 126 (Desaulniers et al., 1999), but serum prolactin levels were lower in
Wistar rats exposed to the herbicide atrazine (Stoker et al., 1999). The influence
of xenobiotics on brood patch development has yet to be explored. Here studies
examined brood patch size in breeding and nonbreeding American kestrels
(Falco sparverius) and compared patch size between PCB-exposed and control
birds. The potential effects of PCBs may be either direct, that is, on the physiology of patch formation, or indirect by altering incubation behavior, which in turn
could affect patch size. Therefore, incubation behavior was included in our analyses to account for variation in patch size.
As hatching success depends on the thermal environment for the eggs, it
may also be influenced by appropriate brood patch development and function. In previous studies, hatching success of American kestrels was reduced
after exposure to PCBs in the diet and in ovo (Fernie et al., 2001a, 2001b).
PCBS ALTER BROOD PATCHES IN KESTRELS
1605
Here, the potential consequence of variation in the size of brood patches on
hatching success was examined.
MATERIAL AND METHODS
Study Species and Experimental Design
This study was conducted at the Avian Science and Conservation Centre of
McGill University (Quebec, Canada), using American kestrels of known age
(1 to 11 yr) and pedigree. On 17 March 1998, 76 male and 74 female kestrels
were randomly assigned to either control or PCB-exposed groups and placed
into communal flight pens (6 × 6 × 2.5 m), segregated by gender and treatment. The kestrels were fed ad libitum on their typical diet of day-old cockerels.
The care and treatment of the kestrels followed the regulations set forth by the
Canadian Council on Animal Care (Olfert et al., 1993).
By using PCB residue levels found in wild prey species of kestrels (Environment Canada, unpubl. data), and PCB congeners found in tissues and eggs of
wild birds from the Great Lakes region (Braune & Norstrom, 1989; Clark et al.,
1998), a dosing regime was calculated that would generate environmentally
relevant PCB levels (Fernie et al., 2000). Aroclor (Monsanto, St. Louis, MO)
types 1248, 1254, and 1260 were mixed 1:1:1 by weight and dissolved in safflower oil at a concentration of 4.85 mg/g total PCB. Kestrels show a preference
for consuming the heads of cockerels (I. Ritchie, personal communication), so
100-μl aliquots of plain safflower oil or the PCB mixture were injected intracranially into frozen–thawed day-old cockerels, to be fed to control or PCB
groups, respectively. Chronic dietary exposure began on 18 March 1998 and,
for the breeding kestrels, continued until the end of the incubation period
(mean 95 d exposure). The birds consumed approximately 7 mg/kg body
weight/d of PCBs (Fernie et al., 2000; Drouillard et al., 2001). Furthermore,
kestrel eggs averaged 34.1 μg/g (geometric mean) of PCB residues on a wholeegg wet weight basis (Fernie et al., 2000), which falls within the range of those
found in eggs of wild raptors showing decreased reproductive success
(Hoffman et al., 1996; Clark et al., 1998; Valkama & Korpimäki, 1999).
Drouillard et al. (2001) present a toxicokinetic model of PCBs in our kestrels.
Kestrels that were genetically unrelated within the past 7 generations were
paired on 21 April 1998 (control n = 25 pairs; PCB n = 25 pairs). Each of the
pairs was placed into an outdoor breeding pen (2.3 × 0.9 × 3.6 m), which contained wooden and rope perches, a one-way glass window for observation,
and a nesting box (0.3 × 0.3 × 0.4 m). The 24 females and 26 males that
remained unpaired, hereafter “nonbreeders,” remained in the communal
flight pens. The nonbreeder pens were located in a building 25–50 m from the
breeding pens, and had large screened windows to allow for natural photoperiod. Wing chord measurements for both breeders and nonbreeders were
taken on 20 April to determine the size of each bird (Wiebe & Bortolotti,
1993). The nonbreeding kestrels were captured on 17 June for measurement
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S. A. FISHER ET AL.
of brood patches. Twenty-four PCB-exposed and 25 control breeding pairs
were captured, weighed, and measured during the incubation period 15 d
after clutch completion. The brood patches of the PCB-exposed breeders
were measured between 22 May and 22 June, with a median date of 9 June.
Control breeders were measured between 21 May and 17 June, with a
median date of 1 June. Brood patches were found by having one person hold
the kestrel and gently blow on the ventral surface to reveal the lack of feathers
and edematous skin. A water-wetted cotton ball was used to brush feathers
aside so that a second person could measure the length and width of the patch
to the nearest millimeter with a ruler. As the shape of a brood patch was oval,
the two measurements were transformed into an area using the equation for
the area of an ellipse. Despite variation in the literature over whether kestrels
develop only a central brood patch, or two patches on the breast (Bailey,
1952; Willoughby & Cade, 1964; Bird, 1988), our findings concur with those
of Wiebe and Bortolotti (1993) that American kestrels develop three brood
patches, one on the central abdominal region and one on each side of the
breast: the central (CBP), left (LBP), and right (RBP) brood patches. Female
American kestrels develop brood patches before and during egg laying,
whereas males typically develop patches after clutch completion, and patches
of females are larger than those of males (Willoughby & Cade, 1964; Wiebe &
Bortolotti, 1993).
The incubation period was defined as the time from the completion of the
clutch to the hatching of the first egg or until 28 d after clutch completion for
pairs that failed to hatch any egg. A custom-built electronic balance system
was used to monitor incubation behavior. A wooden incubation box was
mounted onto a balance. Electrical impulses from the balance, impulses that
were proportional to the mass of the contents of the box, were recoded on a
microchip once every min, 24 h/d. These mass data allowed us to identify
both the presence and the gender of the adults (as females are heavier than
males) (Fisher, 2002; Fisher et al., 2006). Twenty electronic balances were
randomly assigned to PCB-exposed or control pens. Every 5 d during the incubation period, balances were switched between pens of the same treatment
group, providing for an increased sample size (PCB-exposed, n = 23; control,
n = 23) (further details in Fisher, 2002, and Fisher et al., 2006).
Data Analysis
The potential effect of PCB exposure was investigated for right and left
patches combined (R + LBP) and CBP. The abdominal and breast patches
were investigated separately because they may show different patterns of variation, as not all wild male kestrels developed CBPs (Wiebe & Bortolotti, 1993).
The total brood patch area (TBP) was calculated by summing the three patch
areas. The TBP variable was deemed important in trying to relate brood
patches to hatching success.
A three-way analysis of variance (ANOVA) was initially conducted for each
brood patch variable with treatment, gender, and breeding status (breeder or
PCBS ALTER BROOD PATCHES IN KESTRELS
1607
nonbreeder) as factors. As breeding status and gender were found to have significant interactions (Table 1), separate one-way ANOVAs were performed on
both breeding and nonbreeding males and females. For nonbreeders, an analysis of covariance (ANCOVA) was conducted for each gender, with treatment
as a factor and wing chord length, age, and mass as potential covariates. When
a covariate was found to be nonsignificant, it was removed and the ANCOVA
was run again, always keeping treatment in the model. For breeding birds,
similar ANCOVAs were performed, but including clutch completion date as
another potential covariate. Clutch completion date was previously shown to
be affected by PCB exposure in this study (Fernie et al., 2001a) and has an
important influence on incubation behavior (Fisher et al., 2006).
Each patch variable was examined in relation to the following incubation
behaviors: the percent of day each gender spent in the nest, average recess
length, number of recesses, number of nest switches, the average length of an
incubation bout, and the number of incubation bouts each gender performed
(PCB = 23 nests, control = 23 nests). These variables were chosen because
they (1) relate to the time eggs were covered by an incubating adult, (2) were
found to affect hatching success (Fisher et al., 2006), and (3) are likely correlated with levels of prolactin (Schoech et al., 1996). Behavioral variables were
transformed when they did not meet the assumptions for analysis of variance.
Since PCB-exposed kestrels were more likely to have their complete clutch fail
TABLE 1. Initial Three-Way ANOVA Results for Each Brood Patch Variable, With Treatment, Gender, and
Breeding Status as Factors
Brood patch
Central
Right + left
Total
F
Treatment
Gender
Status
Treatment × gender
Treatment × status
Gender × status
Treatment × gender × status
Treatment
Gender
Status
Treatment × gender
Treatment × status
Gender × status
Treatment × gender × status
Treatment
Gender
Status
Treatment × gender
Treatment × status
Gender × status
Treatment × gender × status
0.11
34.72
23.97
0.65
9.21
3.03
0.69
3.15
85.20
4.30
2.87
1.61
5.30
5.17
1.07
86.48
15.46
2.44
5.87
6.04
1.29
p
.74
.00
.00
.42
.00
.08
.43
.08
.00
.04
.09
.21
.02
.03
.30
.00
.00
.12
.02
.02
.26
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S. A. FISHER ET AL.
(Fernie et al., 2001a) and were less efficient incubators (Fisher et al., 2006),
the control and PCB-exposed groups were examined separately. Examining
each gender separately, ANCOVAs were conducted for each brood patch with
behavioral variables as potential covariates. Since clutch completion date had
an effect on incubation behavior (Fisher et al., 2006), it was also included as a
potential covariate.
To determine whether brood patch size was related to the degree of PCB
contamination, total PCB residues in eggs were compared to brood patches
with Pearson’s product moment correlations. For details regarding egg collection and PCB residue analyses, see Fernie et al. (2000).
Kestrels that have larger brood patches should be able to cover more of
the clutch, thereby making incubation more efficient and potentially increasing hatching success. Because hatching success should be related to egg
contact with all brood patches, only TBP was analyzed. To determine if brood
patch size influenced hatching success, an ANOVA was performed for
both males and females with hatching success as a category: no (0%), moderate (1–74%), and high (75–100%) hatching success. The criterion for significance was set at p < .05.
RESULTS
Nonbreeding Kestrels
Females had larger brood patches than males (Tables 1 and 2). Nonbreeding male kestrels exposed to PCBs had a significantly larger R + LBP (F1,24 =
4.76) and TBP (F1,24 = 5.1) compared to control males (Table 2). It was not
possible to detect a treatment effect for the CBP of males. A similar trend was
found in nonbreeding females, where PCB-exposed birds had significantly
larger patches than controls for CBP (F1,21 = 5.44) and TBP (F1,22 = 4.94), but
not for R + LBP (Table 2).
The size of the brood patch was not related to mass, age, or length of the
wing chord in nonbreeding male kestrels. A significant relationship was found
between wing chord and the CBP for females (F1,21 = 8.74), where larger birds
had a greater CBP area, but not for the R + LBP and TBP. A significant association was found between age and the R + LBP (F1,22 = 5.08) and the TBP
(F1,22 = 3.83), where older birds had larger patches. An association between
age and the size of the CBP was not detected. No relationship existed
between brood patch sizes and mass in females.
Breeding Kestrels
Female kestrels had larger brood patches than males (Tables 1 and 2). The
CBP (F1,46 = 3.49), R + LBP (F1,45 = 4.82), and TBP (F1,45 = 5.06) were markedly smaller in PCB-exposed males than in controls (Table 2). Control females
had a significantly larger CBP (F1,46 = 4.71) but a smaller R + LBP (F1,46 =
5.01) than PCB-exposed females, which resulted in no difference in TBP area.
PCBS ALTER BROOD PATCHES IN KESTRELS
1609
TABLE 2. Central (CBP), Right Plus Left (R + LBP), and Total Brood patch (TBP) Areas (mm2) of Breeding
and Nonbreeding American Kestrels, From Control (CTL) and PCB-Exposed Groups
Brood patch
Status
Treatment
Gender
n
CBP
R + LBP
TBP
Breeder
PCB
CTL
PCB
CTL
PCB
CTL
PCB
CTL
M
M
F
F
M
M
F
F
24
25
24
25
13
13
12
12
454 ± 144.3a
562 ± 255.1b
699 ± 169.2a
806 ± 262.5b
424 ± 81.6a
389 ± 68.8a
609 ± 158.2a
471 ± 87.8b
728 ± 186.3a
874 ± 309.4b
1382 ± 306.6a
1193 ± 227.1b
887 ± 137.7a
734 ± 197.7b
1155 ± 50.7a
1051 ± 211.7a
1182 ± 268.3a
1436 ± 487.1b
2081 ± 399.7a
2000 ± 402.3a
1312 ± 237.9a
1123 ± 237.9b
1764 ± 376.1a
1522 ± 248.6b
Nonbreeder
Note. Values are mean ± SD. Values marked with superscript a are significantly different (p < .05) from
those marked with b for the comparison of PCB-exposed and CTL kestrels for each patch variable within
each gender and status group as summarized from the text.
Brood patch size was not related to age, wing chord, or clutch completion
date for breeding males; however, heavier males had significantly larger R + LBP
(F1,45 = 5.59), but mass was not related to the CBP or TBP. A positive
relationship existed between female mass and brood patch size for the CBP
(F1,46 = 6.7) and TBP (F1,45 = 5.58), but not for R + LBP. No association was
found between brood patch size and age, wing chord, or clutch completion date.
No association was found between total PCB residue levels in eggs and the
size of the CBP, R + LBP, or TBP for either males (n = 19) or females (n = 19).
When examining incubation behavior in relation to brood patch size,
covariates previously found to affect patch size were included in the analysis.
No effect of incubation behavior was found on the size of any brood patch for
either males or females from PCB-exposed or control groups.
Total brood patch size was not related to hatching success in PCB-exposed
males and females, or in control males and females.
DISCUSSION
Hatching Success
Kestrels are small-bodied birds with relatively large eggs and a large clutch
size for a raptor, and they appear to have difficulty in covering their entire
clutch (Bortolotti & Wiebe, 1993). Eggs are often partially or totally exposed
even when the parent is in a tight incubating position (Bortolotti & Wiebe,
1993). Since females are unable to warm all the eggs at once, certain eggs may
not get enough heat to survive. Although larger brood patches should be more
effective in providing heat necessary for embryonic development, thereby
influencing egg viability, hatching success was not related to brood patch size in
either PCB-exposed or control birds. Similarly, Wiebe and Bortolotti (1993)
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S. A. FISHER ET AL.
found that hatching success was independent of brood patch size in wild
kestrels. The reduced hatching success of PCB-exposed kestrels (Fernie et al.,
2001a) was partly related to inefficient incubation behavior (Fisher et al., 2006),
but from this study there seems to be no confounding influence of brood patch
size. Studies of wild birds are needed before one might conclude that the
response to PCBs, as shown here, is unimportant to hatching success. Future
research should also consider the possibility that incubation behavior may compensate for poor patch development, and thus limit the impact on eggs.
What Determines Patch Size?
Little is known of the physiology of brood patches, or how xenobiotics may
impact their development. Complete brood patch development occurred in an
immature nonbreeding common black-headed gull (Larus ridibundus), indicating
that patch formation did not result from contact with eggs (Jones, 1971). Similarly, tactile stimulation is not needed for patch development as observed in
breeding male flycatchers (Empidonax spp.) and black-headed grosbeaks
(Pheucticus melanocephalus) as they do not incubate (Bailey, 1952; Skutch,
1957). On the other hand, no patch development occurred in breeding male or
nonbreeding female Harris’ hawks even though they contributed to incubation
and had elevated prolactin levels (Vleck et al., 1991), and prolactin normally
plays an important role in brood patch development (Jones, 1971; Buntin, 1996).
All of our nonbreeding kestrels developed all three brood patches. At least
one nonbreeding female from each of the control and PCB-exposed groups laid
eggs on the floor of the communal flight pen that were often warm to the touch.
The development of brood patches in those few laying females may not be surprising. However, brood patches of the remaining females and the nonbreeding
males indicate that patch formation is at least independent of incubation behavior. Given that 20% of male kestrels breeding in the wild do not develop a CBP
(Wiebe & Bortolotti, 1993), the formation of all three patches in the nonbreeders in captivity was surprising. Although incubation behavior did not influence
whether patches would develop, breeding status was an important factor.
Breeding females had significantly larger brood patches than nonbreeding
females, and breeding control males had bigger patches compared to nonbreeding controls. However, non-breeding PCB-exposed males had CBPs of similar
size and R + LBPs that were larger than those of the breeders.
Despite the lack of association between brood patch size and total PCB
residues in the eggs, PCB-exposure consistently accounted for variation in
patch size in both male and female kestrels. Nonbreeding kestrels of both genders exposed to PCBs had larger brood patches than respective controls. An
opposite trend was found in PCB-exposed male breeders, which had smaller
brood patches than controls. In the PCB-exposed breeding females, the size of
certain patches were also modified in an inconsistent manner, with one larger
patch and one smaller patch compared to controls. Given what is known
about the role of hormones in the development of brood patches, our results
provide further evidence suggesting that PCBs are endocrine-modulating
PCBS ALTER BROOD PATCHES IN KESTRELS
1611
substances. The facts that effects were found in nonbreeders and that patch
sizes were unrelated to specific behaviors in the breeders suggest a direct
mode of action of PCBs on patch physiology, rather than patch size being an
indirect consequence of incubation behavior. That brood patches of males
and females had very different responses to PCBs is consistent with the gender-specific effects of PCBs previously found on behavior (Fisher et al., 2001;
Fisher et al., 2006), immune function (Smits & Bortolotti, 2001; Smits et al.,
2002), and reproduction (Fernie et al., 2001b) in this study population of
kestrels, and again is consistent with endocrine modulation.
We recommend that ecotoxicologists consider the phenomenon of patch
development, as it has now been shown that brood patches clearly respond to
PCB exposure. In addition to understanding potential negative impacts of
contamination on physiology and reproduction, there are useful applications.
Brood patches may be used as bioindicators of endocrine modulation in
toxicology, just as patch development has been used as an indicator of circulating estrogen levels in physiology (Macdougall-Shackleton et al., 2001). Given
their ease of measure in the laboratory and field, the use of brood patches is particularly advantageous for the study of prolactin modulation, as the alternatives
(i.e., incubation behaviors) are time-consuming, costly, and logistically difficult.
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