Use of plumage and gular pouch color to evaluate condition of oil spill rehabilitated California brown pelicans (Pelecanus occidentalis californicus) post-release
Use of plumage and gular pouch color to evaluate condition of oil spill rehabilitated California brown pelicans (Pelecanus occidentalis californicus) post-release
Deborah L. JaquesID 0 1
Kyra L. Mills 1
Barton G. Selby 1
Richard R. Veit 1
Michael H. ZiccardiID 1
0 Pacific Eco Logic , Astoria, Oregon , United States of America, 2 Oiled Wildlife Care Network, Karen C. Drayer Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, Davis, California, United States of America , 3 EH1, San Carlos , California, United States of America, 4 Biology Department, College of Staten Island/City University of New York , Staten Island, New York , United States of America
1 Editor: David Hyrenbach, Hawaii Pacific University , UNITED STATES
Sublethal effects of oil spills may dampen seabird rehabilitation success due to lingering negative impacts of contamination and stress on reproduction and long-term survival. These effects can be difficult to measure while birds are in care as well as once birds are released. Expression of sexually selected traits that are sensitive to condition can provide information on physiological status of birds. We evaluated plumage molt and gular pouch skin color of California brown pelicans (Pelecanus occidentalis californicus) following oil contamination and rehabilitation to test for differences between previously oiled and rehabilitated (post-spill) and presumably uncontaminated pelicans. Post-spill pelicans released with either color leg bands alone, or bands plus harness-mounted satellite GPS tags, were relocated and visually assessed in the field at non-breeding communal roosts and compared to surrounding unmarked pelicans in the general population. Non-oiled pelicans bearing GPS tags were also included in the study. Post-spill pelicans lagged the general population in molt of ornamental yellow crown feathers but hind neck transition into white plumage was not significantly different. Both post-spill and non-oiled pelicans wearing GPS tags had lower gular redness scores than the unmarked, non-oiled population. Pre-breeding gular pouch redness of post-spill pelicans was more strongly influenced by wearing of a GPS tag than a history of oil contamination and rehabilitation. Gular pouch redness of post-spill pelicans in the first 18 months after release was positively correlated with long term survivorship. If gular pouch color is a condition-dependent sexual signal and overall health influences plumage molt progression, our results indicate that many post-spill pelicans marked with bands alone were in relatively good condition going into the next breeding season, but those released with electronic tags experienced additional stress due to wearing the equipment, introducing a confounding variable to the post-release study.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: Funding for this study was provided by
the California Department of Fish and Wildlife?s Oil
Spill Prevention and Administration Fund through
the Oiled Wildlife Care Network (OWCN) at the
Karen C. Drayer Wildlife Health Center, School of
Veterinary Medicine, University of California, Davis.
Post-release studies are collaborative efforts
between the OWCN and appropriate experts, with
funding coming from a reserve within the OWCN
budget. M. Ziccardi and K. Mills are staff members
at OWCN and had roles in project concept and
Wildlife exposed to petroleum products after spill incidents can be negatively affected in
multiple ways. The primary acute impact to these animals is from external contamination by oil and
subsequent hypothermia, increased metabolic effort, and emaciation [
]. Ingestion or
inhalation of polyaromatic hydrocarbons can cause liver and kidney damage, compromised
immune function, and hormone disruption [
2, 5, 6
]. Oil-contaminated seabirds may succumb
immediately to oiling or may endure several days of exposure leading to death if not rescued
and rehabilitated. Capture, washing, handling, and time in captivity can both reverse the
effects of exposure or, possibly compound the initial impacts of oiling [
]. Sublethal effects
of oil spills on seabirds may result in failure to thrive despite plumage restoration and other
rehabilitation efforts [
4, 9, 10
]. Such impacts are difficult to measure once birds are released
but may play an important role in population restoration [
Researchers have used a variety of techniques to track the fate of oiled seabirds following
rehabilitation and release. These include quantifying band recoveries of live and dead birds,
monitoring movement patterns with electronic tracking, and documenting reproductive
9, 10, 14?17
]. Electronic tracking methods have improved knowledge of near-term
postspill bird survival [
]; however, these devices introduce another variable to post-release
Brown pelicans (Pelecanus occidentalis) are a seabird commonly oiled following nearshore
spills in the United States. Survival and dispersal of previously oiled and rehabilitated
California brown pelicans (P. o. californicus) were examined in the early 1990?s by Anderson et al. [
Conventional VHF radiotelemetry and auxiliary color banding were used to track movements
and association with breeding colonies up to two years post-release. None of the previously
oiled pelicans were known to breed and only 9% were detected alive two years after the spill.
Anderson et al. concluded that oiling, and possibly handling stress, resulted in long-term
injury to pelicans, including failure to breed, and lower survival than controls. Those results
supported the supposition that long term sublethal effects of oiling may preclude restoration
of some seabirds to the breeding population. More recently, Miller et al. [
] detected a small
number (approx. 2% of those rehabilitated and released) of color banded Eastern brown
pelicans (P.o. carolinensis) successfully breeding one year after oiling from the Deepwater Horizon
spill. An increasing number of studies have demonstrated that seabird oil spill rehabilitation
efforts can succeed in restoring birds to normal function, but further evidence is
needed?specifically projects that extend beyond acute survival [
Identification of visible external features that indicate physiological responses to
contaminant exposure have helped advance the field of ecotoxicology [
]. Variation in expression
of carotenoid-based colors has been used as a tool for evaluation of contaminant effects and
overall condition of birds [
], but evaluation of plumage and soft-part colors have not
previously been used in studies of post-spill rehabilitated seabirds. Little information is
available on impacts of oil exposure, washing, and rehabilitation on seabird molt and plumage
condition after release, but endocrine disruption or other stressors that affect body condition
could feasibly affect subsequent molt and feather pigmentation. Molt is energetically expensive
(up to 5?30% of daily energy budget) and is generally regulated by photoperiod and hormonal
cycles . Timing and duration of molt can be influenced by factors such as age, sex,
reproductive and nutritional status, geographic origin, and variable environmental conditions [30?
34] complicating application to pollutant studies.
Brown pelicans gradually develop definitive adult plumage over a period of 3?5 years and
are sexually monomorphic [34, 35]. Adults have a complex annual molt cycle that results in
radically different seasonal appearances of the head and neck [34?36]. Adult head and neck
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feathers are generally replaced in the late summer-fall as part of the prebasic molt . Faded
dark hindneck feathers are replaced with white feathers, creating a gray appearing hindneck
during the transition. Around the same time, yellow feathers begin to grow into the white or
speckled crown until the crown is completely yellow and the neck is white in definitive basic
plumage. As part of the prealternate molt later in winter, dark brown-black feathers return to
the hindneck and crest. The crown?s golden hue may intensify during this time, creating
dramatic contrast with the dark hindneck during the courtship period. The yellow crown is thus
an ornamental feature that is present in both basic (non-breeding) and alternate (breeding)
plumage [37, 38]. The crown transitions to white specked with brown during the nesting
season and the brown neck plumage becomes faded and worn by the end of the typical
Both sexes of California brown pelicans (hereafter ?pelicans?) develop a red gular pouch
prior to the breeding season, when the dull grayish gular pouch blooms with redness
proximally . The pouch is multi-layered, including a highly vascular muscle layer and
sub-epithelial melanocyte layer . Pouch redness is thought to indicate hormonal activity and
breeding readiness . Red gular sac color in the great frigatebird (Fregata minor) during the
breeding season has been related to a combination of carotenoids, hemoglobin, and increased
blood flow . The specific physiological and biochemical mechanisms surrounding display
of gular redness have not been described for pelicans but are likely similar to frigatebirds.
Coloration has been found to indicate health and fitness in many species of birds [42, 43].
Carotenoid pigments are acquired by diet and typically give a red, orange, or yellow hue [29,
44, 45], such as the pelican?s pre-breeding crown and gular pouch colors. Expression of
carotenoid colors for sexual signaling is thought to have evolved as an honest advertisement of
individual quality since there are physiological costs associated with using these valuable
antioxidants for display [43, 46, 47]. The outward expression of sexual characteristics can be a
particularly sensitive and readily observable indicator of physiological responses resulting
from stressful events [
]. Carotenoid-based coloration has been found to have a negative
relationship to environmental toxins . For example, Perez et al. [
experimental and field evidence that during the courtship period, the red spot (a carotenoid-based
signal) in yellow-legged gull (Larus michahellis) beaks was smaller in birds exposed to
polyaromatic hydrocarbons compared to those that were not exposed. Similarly, the hue and
brightness of skin colors of kittiwakes during the breeding season showed a negative relationship to
endogenous pollution levels .
We designed a study to test the null hypothesis that post-spill pelicans observed in the wild
would not differ visually from conspecifics with respect to their outward physical appearance.
Here, we provide a field-based comparison of molt progression in the head and neck, and
expression of redness in the gular pouch between previously oiled/rehabilitated pelicans and
the general, presumably never oiled, wild population. We further report on unexpected
differences between post-spill pelicans bearing electronic tags versus post-spill birds released with
only leg bands, and the relationship of gular color to known survival amongst rehabilitated
Materials and methods
To further improve estimates of seabird recovery following oiling, the Oiled Wildlife Care
Network (OWCN), a program led by the School of Veterinary Medicine at the University of
California at Davis, initiated a study to track rehabilitated brown pelican movement patterns and
survival following the May 2015 Refugio Beach Oil Spill near Santa Barbara California using
Global Positioning Satellite platform transmitter terminal (GPS-PTT) tags . We developed
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this field investigation as a companion to the remote tracking project. We assumed that
adequate numbers of post-spill pelicans could be located with the aid of recent position data from
the transmitters and that measures of field observable characteristics, including plumage
transitions and gular pouch color, could provide an independent measure of post-spill pelican
health in the wild. Non-breeding brown pelicans spend much of their daily time budget
onshore at traditional coastal communal roosts [51, 52] where, in certain settings and with
appropriate techniques, they can be observed closely without causing disturbance. Surveys at
breeding colonies were not feasible for this study due to potential disturbance and remote
nesting locations .
The Refugio Beach Oil Spill occurred on 19 May 2015, in Santa Barbara County, California,
USA at 34.46? N, 120.09? W (Fig 1). The spill affected over 100 miles of coastline with oil
sheen and tar balls persisting on the water for several weeks. Brown pelicans contaminated
with crude oil from the spill were captured with hand nets 1?10 days after the initial event.
The extent of oiling on individuals in the study was variable (2?100%) and the duration of
exposure was unknown but ranged from 2 to as many as 15 days. The birds were washed,
rehabilitated and released approximately 3?5 weeks after oiling just outside the spill zone . All
released pelicans (N = 42) were outfitted with aluminum federal bands and field-readable
green color leg bands. Thirty-three of the birds were aged as adult based on typical after third
year (ATY) plumage [34, 35]. Of these, a subset of 12 adults were fitted with GPS-PTT devices
(65g solar units from GeoTrak Inc, Apex, North Carolina). Transmitters were attached
backpack style with Teflon ribbon harnesses (Fig 2) [
]. Eight additional adult pelicans that
did not appear to have been directly exposed to oil were captured in early July 2015 by baiting
near the spill site and fitted with the same GPS-PTT tags for comparative studies of movement
patterns. These control birds were released within hours of capture. Electronic tagging
equipment and procedures are further described in Lamb et al. [
Work was completed in accordance with all appropriate State, Federal and university
regulations and policies including the U.S. Geological Survey Bird Banding Laboratory with
Federal Master Bander permit #23539, the U.S. Fish and Wildlife Service Scientific Collection
Permit #MB191637-0, and the California Department of Fish and Wildlife Scientific Collection
Permit #SC-003855. All procedures were conducted under University of California at Davis
Institutional Animal Care and Use Committee Protocol #18823. Brown pelicans are protected
under the Migratory Bird Treaty Act.
Field reconnaissance was initiated approximately three months after release of the
previously oiled birds. Data collection on plumage and color comparisons took place primarily
from September 2015?March 2016. Field work occurred in seasonal sessions of 7?10 days
and ranged along the coast from Grays Harbor, Washington, USA (46.54?N, 124.06?W) to
Ojo de Liebre, Baja California Sur, MX (27.50?N, 113.57?W; Fig 1). Permission to access Naval
Base Ventura County lands was granted by Martin Ruane (U.S. Navy) and access to A?o
Nuevo Island Reserve was provided by Patrick Robinson (U.C. Santa Cruz). All other field
locations were open to the public. Pelican roost site atlases were used to help plan search effort
within a region and surveys took place from both ground and small boats. The basic survey
strategy was non-intrusive searches and observations of post-spill and control transmitter
pelicans at non-breeding communal roosts and fish handling areas, with initial effort focused on
regions where GPS positions indicated past occurrence of electronically tagged birds. After
transmissions ceased and/or these birds moved out of the study range, search effort was
focused on large roost sites where leg-banded pelicans were most likely to be detected. For the
duration of the study, another observer conducted routine kayak-based searches for banded
pelicans at major harbor breakwater roosts in Central California nearly weekly, without
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Fig 1. Refugio oil spill site and distribution of post-spill pelican field sightings. Locations of Refugio spill green
banded pelican sightings from August 2015 through November 2016 are shown (N = 190 sightings). North and south
limits of field surveys are indicated by triangles. Base map credit: Esri, HERE, Garmin, OpenStreetMap contributors,
and the GIS users community.
consideration of the electronic tracking data. Both observers photographed post-spill pelicans
with high resolution DSLRs and image stabilizing telephoto lenses.
Comparisons to the general population were made at the same place and time by evaluating
the five nearest neighbors surrounding a marked focal bird. The ?general population? consisted
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Fig 2. Configuration of GPS-PTT tags on brown pelicans observed in the field. Dorsal (A) and ventral (B) views
shown on Z11, 17 March 2016, after about 9 months of wearing the equipment.
of unmarked, presumably never oiled or rehabilitated pelicans. Focal birds included any
individual in one of the following three groups; 1) previously oiled pelicans released with color
band-only, 2) previously oiled pelicans with band plus GPS-PTT, and 3) non-oiled pelicans
with band and GPS-PTT. Plumage aspect and soft-part color characteristics were based on
classifications in Schreiber et al. .
Molt phase and color assessments were limited to adult birds and focused on three distinct
and readily visible body parts?the hind neck, the crown feathers, and the gular pouch. These
features were visually scored using a combination of direct field observations and digital
photographs. The hind neck and crown were categorized as either in a definitive plumage aspect
or transitioning between states . An ordinal grading system was developed (Fig 3) resulting
in five different potential scores for the neck molt index (NMI) and four for the crown molt
index (CMI). We did not attempt to discern differences in yellow crown feather hue but simply
the occurrence of yellow feathers. Data for crown and neck analyses were restricted to
September 15-December 15, 2015. A third ordinal grading system, the gular redness index (GRI) was
based primarily on visual estimation of spatial extent of red in the pouch (0?3) using data
collected during September 15-March 21, 2016 (Fig 4). Plumage and color were scored only by
the primary observer to reduce potential bias. Occurrence of wetted plumage and shivering
was also noted in the field, which can be normal in some circumstances but can also indicate
structural failure of plumage and a need to produce endogenous heat [
Surveys of banded pelicans to document survival continued through the summer of 2018
and each post-spill bird was photographed. A separate analysis of post-spill survival of the
Refugio incident pelicans, incorporating demographic and biomedical factors, is planned .
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Fig 3. California brown pelican crown and nape index scoring system. The scores shown were the numbers used for
the crown and neck molt indices (CMI and NMI).
Statistical analyses were conducted using R package v. 3.5.1(R Core Team 2018) [
Pelicans were assigned to four different groups as follows: post-spill rehabilitated birds without
GPS-PTT tags; post-spill birds with GPS-PTT tags, non-oiled pelicans with GPS-PTT tags; and
the general population of wild, non-oiled, unmarked pelicans. Loglinear analyses were used to
test for interactions between factors. These analyses included a date factor to incorporate
variation in plumage and color over the sampling period. Data were binned into three sampling
periods as follows (Sep-Oct, Nov-Dec, and Feb-Mar). The effects of oil and GPS-PTT were
modeled separately. In addition, the association between highest GRI observed during 2015?
2016 and survival of post-spill birds, was tested using Spearman rank correlation. The survival
index was the number of days elapsed between release and latest observation in the field,
including detections in 2018.
Most of the Refugio post-spill pelicans (79%) were re-sighted at least once following release. By
September 2017, 220 sightings of 33 birds were documented (mean = 6.7 sightings/bird,
Fig 4. California brown pelican gular pouch scoring system. The gular redness index (GRI) was based primarily on
extent of red; other characteristics that typically accompany each score are also included here.
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range = 1?45, SD = 9.2). Frequent surveys of large communal roosts resulted in a greater
number of visual encounters of target animals than did attempts to relocate electronically tagged
pelicans based on GPS-PTT data feeds showing past positions. Sightings of the post-spill birds
were most common in summer and fall (especially July-October) and relatively rare during
late winter-spring (Fig 5) when pelicans generally retreat to offshore islands in the breeding
]. Tracking data showed that all of the electronically tagged post-spill pelicans moved
out of the zone affected by the spill during summer and fall 2015- some as far north as Oregon,
and most retreated south into Mexico during winter .
Most visual sightings of post-spill birds occurred over 300 km north of the spill region in
Central California (Fig 1). This was due to a combination of focused survey effort at two
harbor roosts where there were exceptionally large concentrations of pelicans and favorable
bandsighting conditions. We counted as many as 2,800 and 3,900 pelicans at two key breakwater
roosts, in Pillar Point and Alameda harbors, respectively, during the summer of 2016, while as
few as zero occurred in late winter-early spring surveys. Band sightings indicated high
turnover of individuals and suggested a well-mixed migratory population, although a few birds
were resident to the area during much of the non-breeding season.
Plumage of post-spill band-only pelicans appeared normal with respect to waterproofing
and overall integument condition (e.g., none were observed with saturated wet plumage or
seen shivering), while four of the 12 pelicans seen wearing transmitters were observed
shivering (two post-spill, two control). Plumage disruption around the harness was generally visible
around the ventral surface (Fig 2B) and excessive preening around the straps was observed,
but not quantified for this study. Ultimately, four pelicans were encountered alive that had
shed their transmitters but retained leg bands.
Fig 5. Field encounters of post-spill brown pelicans by season (2015?2016). Data are separated for previously oiled
birds released with only leg bands (BAND), equipped with GPS-PTT transmitters (PTT) and birds that shed
transmitters but retained bands (PTT LOST). N = 190 sightings of 33 individual post spill birds of all ages.
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During the mid-September?December sampling period, nearly all non-oiled pelicans
(98%) displayed solid yellow crown plumage (Fig 3). Emergence of yellow crown feathers was
more variable and lagging in the post-spill group (Fig 6); 71% of post-spill birds had solid
yellow crowns and the remainder were transitional or entirely lacking yellow feathers. Loglinear
analysis incorporating non-oiled pelicans bearing GPS-PTT tags indicated that both previous
oiling/rehabilitation and equipment burden significantly influenced emergence of yellow
feathers in the crown (Table 1, p < 0.001).
Most pelicans (93%) in the non-oiled general population had definitive basic white neck
plumage during the sampling period (Fig 3), although some (~ 6%) had progressed further,
into prealternate and alternate phase dark hindneck plumage by mid-December. The
postspill group lagged slightly behind the general population in molt of the hindneck, and none of
the post-spill birds acquired the dark alternate phase hindneck by mid-December (Fig 7).
Replacement of overall body plumage apparently also lagged in some cases but was not
quantified (Fig 8). Loglinear analysis indicated that neither previous oiling/rehabilitation or the
burden of GPS-PTT tags significantly influenced the molt progression of the neck in this study (Z
= -0.65, p = 0.5 and Z = -0.99, p = 0.3, respectively).
Pelicans began to display red pouches at nonbreeding roosts by mid-September 2015, and
red pouches were observed through March 2016. Expression of redness in the non-oiled/
unmarked population was variable each month within the sampling period but scores tended
to be highest in November-February (Fig 9). Previously oiled pelicans and non-oiled
GPS-PTT-bearing birds were less likely to express gular redness than the general population.
Although both factors (oil and PTT) significantly influenced gular redness according to
Fig 6. Crown scores compared for non-oiled and oiled pelicans, showing monthly mean and standard deviation.
The oiled group includes pelicans released with band-only and GPS-PTT tags (N = 21). The non-oiled group includes
only unmarked pelicans (N = 135) and does not include pelicans bearing PTT tags. Data are from September
15-December 15, 2015. Statistical analysis results are presented in Table 1.
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Effect of Oil on Crown
Effect of PTT on Crown
loglinear analysis (Table 2), the effect of wearing a GPS-PTT was more significant (p < .001).
Pelicans wearing electronic tags were more likely to have a GRI score of zero than other
groups. For example, in November-December, only 13% of PTT-bearing birds (N = 8) had
any discernable trace of pouch redness, while 66% of the post-spill birds released with bands
only and 93% in the unmarked non-oiled group showed redness in the pouch (Table 3).
Sightings of banded birds through summer 2018 indicated high survival rates of the Refugio
post-spill pelicans overall; at least 60% (25 of 42 pelicans) were alive one year after release and
43% (18 pelicans) were seen alive three years after the spill. Long-term survival of adult
postspill birds was positively correlated with the highest GRI score documented in the first 18
months after oil exposure (Fig 10; S = 138.7, rS = 0.796, p < 0.001). None of the birds with
gular scores of zero (no redness in the pouch) were encountered >247 days post-release. Gular
redness scores of zero were also associated with known mortality. Of four confirmed pelican
mortalities in this study, three were seen alive in the field during the period of expected pouch
redness, and all had a score of zero. Three of the pelican carcasses were GPS-PTT-bearing and
found by searching in areas where electronic signals suggested lack of normal movement (one
previously oiled, two non-oiled). The fourth carcass was from a color band-only bird and
found incidentally by a member of the public.
We developed a novel approach to evaluating condition of California brown pelicans in the
field following oil spill rehabilitation and release. We found that it was possible to locate
adequate samples of post-spill birds without the aid of electronic tracking devices, although it
required a lot of survey effort at roost sites that were both heavily used and conducive to close
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Fig 7. Hindneck scores compared for non-oiled and oiled pelicans, showing monthly mean and standard deviation. The oiled group includes pelicans released with
band-only and GPS-PTT tags (N = 21). The non-oiled group includes only unmarked pelicans (N = 135) and does not include pelicans bearing GPS-PTT tags. Data are
from September 15-December 15, 2015. Differences in neck molt between groups were not significant according to loglinear analysis (see text).
observations. Our results suggest that there were subtle lingering physiological effects of
pollution exposure and rehabilitation in the first year after the spill that caused significant
differences in crown and gular pouch appearance, contrary to the null hypothesis.
Conditiondependent signals represent the sum of environmental pressures on an animal [
]. In this
case, the burden of wearing electronic transmitters appeared to be a hindrance to recovery of
previously oiled, rehabilitated pelicans and confounded the results of the study. While
GPS-PTT tagged birds survived and initially appeared to move normally [
], there was
evidently ongoing stress that resulted in a general failure to express gular redness prior to the
breeding season for both oiled and non-oiled birds bearing the tags. We recommend that a
similar study be repeated without the additional variable of electronic transmitters and with a
focus on documenting gular pouch redness in the pre-breeding phase.
Although our results were unexpected with regard to the strong influence of the GPS-PTT
], broad literature reviews have concluded that transmitters negatively affect most
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Fig 8. Mid-November brown pelican plumage aspect comparison, lagged versus typical. This example shows lagged molt of a post-spill bird
carrying a GPS-PTT tag photographed 6 months after the spill (A) versus seasonally typical molt status in a post-spill bird marked with
bandonly, photographed 18 months after the spill (B).
aspects of bird behavior and ecology to some degree and may bias resulting data [
Kesler et al.  found that mallards (Anas platyrhynchos) fitted with dummy transmitters
attached with Teflon ribbon harness had lower body mass than controls without equipment.
Fitted mallards also tended to avoid water, presumably due to greater energetic expenditure to
thermoregulate in cold weather and compromised feather insulation caused by the equipment.
In our study, one of the equipment-related stressors for pelicans was likely similar bodily heat
loss due to plumage disruption around the chest harness and transmitter (see Fig 2B); an issue
that may have become aggravated over time.
The fact that there was no discernible difference in plumage quality with respect to
waterproofing between previously oiled pelicans marked with leg band-only and the general
population was an important finding. Current rehabilitation methods include techniques to ensure
that plumage integrity is restored through washing and self-preening and are not released
until the birds have met restored waterproofing criteria [
]. This is a major advance
compared to the early days of seabird oil-spill rehabilitation, when plumage restoration seemed
impossible to achieve [
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Fig 9. Gular redness scores for non-oiled, previously oiled, and non-oiled GPS-PTT bearing pelicans. Shown are medians, quartiles, and outliers across months.
Sample sizes are as follows: non-oiled (N = 135), oiled (N = 17), non-oiled with GPS-PTT (N = 9). Data are from September 15, 2015-March 21, 2016.
Plumage phase differences between oiled and non-oiled birds could indicate stressors
associated with oil exposure, rehabilitation, and/or tracking equipment. A wide range of
debilitating sublethal impacts following oil exposure have been previously described [
4, 8, 13, 26
impacts on subsequent feather replacement have not been specified. Our finding that
postspill pelicans moved through the prebasic hindneck plumage transition (from brown to white
feathering) at a rate insignificantly different from the general population indicated that this
molt process proceeded normally despite the trauma of the spill event.
Sexual signals, including plumage colors that depend on antioxidants such as carotenoids,
offer a more sensitive measure of the immunological and nutritional state of animals, since
bodily antioxidants tend to be directed to other functions related to survival at the expense of
the expression of the sexual traits [
]. The less frequent occurrence of yellow crown
plumage observed in post-spill pelicans in this study seemed to indicate such a trade-off, but we
could not determine if lack of yellow was due to lagging molt or absence of pigmentation in
emerged feathers. In addition, brown pelican head rubbing on the uropygial gland may
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Effect of oil on gular redness
Effect of PTT on gular redness
increase the crown?s golden appearance due to adventitious coloring from the sebaceous oils
after yellow feathers have emerged [34, 35]. It seems important to note that some of the
behaviors we observed in the field suggested that the backpack transmitters may have obstructed
normal access to the preen gland by the head, which could result in a less intense yellow hue to
the crown and represent another negative impact. Color deficiencies in ornamental plumage
Gular redness index scores (GRI) are shown for all previously oiled pelicans (OIL) and those bearing electronic tags
(PTT) across binned months, where 0 = no OIL or no PTT, and 1 = previously oiled, or bearing PTT, respectively.
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Fig 10. Gular pouch redness index and number of days that previously oiled pelicans were known to survive
postrelease. Gular redness index (GRI) is the highest score observed in the field (0?3) in the first 18 months after oil
contamination; ?Survive? is the number of days elapsed between the last sighting of the bird and its release date
following rehabilitation. All data (N = 16) are from ATY pelicans. GRI and the survival index were positively correlated
(S = 138.7, rS = 0.796, p = 0.0002).
may affect mate acquisition and subsequent breeding success . Future field researchers
may be able to improve methodology by using calibrated photographs and spectrometers to
distinguish variation in the crown?s yellow hue .
If one assumes that the red gular pouch provides a positive measure of health in the
California brown pelican, our results suggest that, although not equal to the general population, the
post-spill birds released with only bands were in relatively good condition going into the first
breeding season after the spill, that numerous complex interacting physiological mechanisms
were functioning, and that many of these birds could afford the additional costs of color
]. Developing and maintaining bright gular coloration in the brown booby (Sula
leucogaster) apparently incurs oxidative costs for both sexes . Perhaps most importantly,
our finding that post-spill pelicans with redder pouches tended to be encountered at a higher
rate in subsequent years suggests that gular color may also predict overall survival. Parasite
load, nutritional status, and immunocompetence are some of the possible links between
survival and color of a dynamic avian integument feature [
]. The gular pouch will probably
reflect a pelican?s current condition better than plumage color during the pre-breeding season.
Dey et al. [
] found that a bare-part ornament was a more reliable status signal than plumage
color in a cooperatively breeding bird and recommended an increased focus on bare-parts to
expand understanding of animal communication.
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Relationships between body condition, integument color, and breeding success are
relatively well-known for several seabird species but are not fully understood in the brown
pelican. Investigation of the underlying mechanisms surrounding gular pouch color expression
and how it relates to pelican fitness would increase the utility of using pouch color in future
studies. In the sexually dimorphic great frigatebird, for example, the male displays a bright
red inflated throat pouch during courtship that rapidly fades to orange at the onset of
incubation. Astaxanthin, a carotenoid pigment, has been found in very high concentrations in
the outer dermal layer of the pouch . The spectral pattern of color and the
vascularization of the pouch suggests that along with carotenoids, increased blood flow and the
presence of hemoglobin may contribute substantially to the overall coloration of the pouch
during the display period . Variation in displaying male frigatebird pouch color has
been positively correlated to breeding success [
]. The blue and green gular skin color in
both sexes of breeding brown boobies is thought to be due to a combination of structural
color mechanisms and allocation of carotene pigments . Males expressing greener gular
color were found to have increased parental investment in chicks [
]. Kittiwakes in
good body condition displayed brighter carotenoid based integument colors around the
eye, gape and tongue, than those in poor condition . Pouch color of other brown pelican
subspecies varies but none are typically red [35, 36] adding interest to questions
surrounding color mechanism and signaling function of the gular pouch in this species.
Targeted field surveys with large sample sizes and from wide geographic ranges are also
needed to better establish or update baseline patterns and variation in molt and seasonal color
change for California brown pelicans. Schreiber et al.  noted that there were many
questions surrounding brown pelican molt, including how food supply, region of residence, age,
sex, and the interaction between these and other factors, may affect feather replacement; these
questions also apply to gular pouch color. For example, we found that gular pouch redness
occurred three months earlier than previously described [34, 35]. We saw many birds with red
pouches by September at nonbreeding communal roosts, where pouch displays are often used
in social interactions .
Chronology and outcome of annual breeding effort can affect timing of avian molt [34, 38]
but it is not clear how that may have factored into our study results. During the period 2014?
2016 there was unprecedented breeding failure throughout much of California brown pelican
range due to environmental conditions [
]. Electronic tracking results  suggest that
pelicans oiled in the Refugio spill included birds from Mexican breeding colonies that had failed
or forgone breeding in 2015, and were migrating north along the California coast when caught
in the spill. Although pelicans with GPS-PTT tags visited breeding colonies in 2016, none were
known to successfully breed .
Despite the challenges, field tracking and visual assessment of plumage and gular pouch
color of marked brown pelicans has good potential for future ecotoxicology and post-release
studies. The expression of gular pouch redness likely plays a role in behavioral ecology at
nonbreeding communal roosts, as well as breeding colonies, and may provide a valuable window
into many aspects of California brown pelican health and fitness. This study also serves as a
reminder to use caution when interpreting data based on animals bearing a significant
equipment burden and will hopefully help encourage development of improved remote tracking
techniques for brown pelicans.
S1 Fig. Crown and nape sampling by bird type, 2015.
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S2 Fig. Gular pouch sampling by bird type, 2015?2016.
S1 Datafile. Data used to test for correlation between gular redness and days of known
Assistance was provided by C. Fiorello and C. Clumpner (Oiled Wildlife Care Network), M.
Harris and L. Henkel (California Department of Fish and Wildlife, Office of Spill Prevention
and Response), R. McMorran (U.S. Fish and Wildlife Service), R. Golightly (Humboldt State
University), and the International Bird Rescue (IBR) staff at the Los Angeles Oiled Bird Care
and Education Center. The U.S. Geological Survey Bird Banding Laboratory and the South
Carolina Fish and Wildlife Research Institute provided technical resources. Additional
logistical assistance and site access was provided by M. Ruane (Ventura Naval Air Weapons Station),
L. Feeney, (Golden Gate Audubon Society), M. Parker and J. Howard (Center for Ecological
Studies), D. Mazurkewicz (National Park Service), Patrick Robinson (U.C. Santa Cruz), and
the Port of Ventura. A. Esiner (USDA Wildlife Services), Tiffany Shepherd (Naval Base
Coronado), J. Manley (Institute for Wildlife Studies), Michelle Maley (Naval Base Point Loma), and
Marie Malloy (Wildlife Assist) assisted with carcass search and retrieval. We thank D.W.
Anderson (U.C. Davis emeritus) for valuable input and encouragement throughout.
Conceptualization: Deborah L. Jaques, Kyra L. Mills, Michael H. Ziccardi.
Data curation: Deborah L. Jaques.
Formal analysis: Deborah L. Jaques, Richard R. Veit.
Funding acquisition: Michael H. Ziccardi.
Investigation: Deborah L. Jaques, Barton G. Selby.
Methodology: Deborah L. Jaques, Barton G. Selby, Richard R. Veit.
Project administration: Deborah L. Jaques, Kyra L. Mills, Michael H. Ziccardi.
Resources: Deborah L. Jaques, Barton G. Selby.
Software: Deborah L. Jaques.
Supervision: Kyra L. Mills.
Visualization: Deborah L. Jaques.
Writing ? original draft: Deborah L. Jaques.
Writing ? review & editing: Deborah L. Jaques, Kyra L. Mills, Barton G. Selby, Richard R.
Veit, Michael H. Ziccardi.
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18 / 20
Saks L, Ots I, H?rak P. Carotenoid-based plumage coloration of male greenfinches reflects health and
immunocompetence. Oecologia. 2003; 134(3):301?7. https://doi.org/10.1007/s00442-002-1125-z
Dauwe T, Eens M. Melanin-and carotenoid-dependent signals of great tits (Parus major) relate
differently to metal pollution. Naturwissenschaften. 2008; 95(10):969?73.
https://doi.org/10.1007/s00114008-0400-1 PMID: 18506415
McGraw KJ, Hill G. Mechanics of carotenoid-based coloration. Bird coloration. 12006. p. 177?242.
Payne RB. Mechanisms and control of molt. Avian biology. 1972; 2:103?55.
Hahn T, Swingle J, Wingfield J, Ramenofsky M. Adjustments of the prebasic molt schedule in birds.
Ornis Scandinavica. 1992:314?21.
Dawson A. Control of the annual cycle in birds: endocrine constraints and plasticity in response to
ecological variability. Philos Trans R Soc Lond B Biol Sci. 2008; 363(1497):1621?33. Epub 2007/12/01.
https://doi.org/10.1098/rstb.2007.0004 PMID: 18048294; PubMed Central PMCID: PMCPMC2606722.
Freed LA, Cann RL. Changes in timing, duration, and symmetry of molt of Hawaiian forest birds. PLoS
One. 2012; 7(1):e29834. https://doi.org/10.1371/journal.pone.0029834 PMID: 22279547
Pyle P. Identification guide to North American birds. Part II.: Slate Creek Press, Point Ryes Station,
Schreiber R, Schreiber E, Anderson D, Bradley D. Plumages and molts of Brown Pelicans. Natural
History Museum of Los Angeles County Contributions to Science. 1989;(402).
Shields M. Brown Pelican: Pelecanus occidentalis: American Ornithologists? Union; 2002.
Humphrey PS, Parkes KCJTA. An approach to the study of molts and plumages. 1959; 76(1):1?31.
Amadon DJTC. Avian plumages and molts. 1966; 68(3):263?78.
McSweeney T, Stoskopf MK. Selected anatomical features of the neck and gular sac of the brown
pelican (Pelecanus occidentalis). The Journal of Zoo Animal Medicine. 1988:116?21.
Schreiber RW. Maintenance behavior and communication in the Brown Pelican. Ornithological
Juola FA, McGraw K, Dearborn DC. Carotenoids and throat pouch coloration in the great frigatebird
(Fregata minor). Comp Biochem Physiol B Biochem Mol Biol. 2008; 149(2):370?7. Epub 2007/11/24.
https://doi.org/10.1016/j.cbpb.2007.10.010 PMID: 18035568.
Hill GE, McGraw KJ. Bird coloration: mechanisms and measurements: Harvard University Press; 2006.
Hill GE, McGraw KJ. Bird coloration: function and evolution: Harvard University Press; 2006.
Brush AH. Avian pigmentation. Chemical zoology. 1978; 10:141?61.
Goodwin TW. The biochemistry of the carotenoids. 2nd ed. London; New York: Chapman and Hall; 1980.
Zahavi A. Mate selection?a selection for a handicap. Journal of theoretical Biology. 1975; 53(1):205?
14. PMID: 1195756
Montoya B, Valverde M, Rojas E, Torres R. Oxidative stress during courtship affects male and female
reproductive effort differentially in a wild bird with biparental care. J Exp Biol. 2016; 219(Pt 24):3915?26.
Epub 2016/11/02. https://doi.org/10.1242/jeb.141325 PMID: 27802141.
Buchanan KL. Stress and the evolution of condition-dependent signals. Trends in Ecology & Evolution.
Ble? vin P, Tartu S, Angelier F, Leclaire S, Bustnes JO, Moe B, et al. Integument colouration in relation to
persistent organic pollutants and body condition in arctic breeding black-legged kittiwakes (Rissa
tridactyla). Science of the Total Environment. 2014; 470:248?54. https://doi.org/10.1016/j.scitotenv.2013.09.
049 PMID: 24140695
Lamb J, Fiorello C, Satg e? Y, Mills K, Ziccardi M, Jodice P. Movement patterns of California brown
pelicans (Pelecanus occidentalis californicus) following oiling and rehabilitation. Marine Pollution Bulletin.
2018; 131:22?31. https://doi.org/10.1016/j.marpolbul.2018.03.043 PMID: 29886941
Briggs KT, Tyler WB, Lewis DB, Kelly PR, Croll DA. Brown Pelicans in central and northern California.
Journal of Field Ornithology. 1983; 54(4):353?73.
Croll DA, Ballance LT, W u?rsig BG, Tyler WB. Movements and daily activity patterns of a Brown Pelican
in central California. Condor. 1986:258?60.
Anderson DW. In my experience: dose-response relationship between human disturbance and Brown
Pelican breeding success. Wildlife Society Bulletin (1973?2006). 1988; 16(3):339?45.
Fiorello C, Jodice P, Lamb J, Satge Y, Mills-Parker K, Jaques D, et al., editors. Post-release monitoring
of oiled brown pelicans from the 2015 Refugio oil spill International Oil Spill Conference Proceedings;
2017: International Oil Spill Conference.
19 / 20
1. Fry DM , Lowenstine LJ . Pathology of common murres and Cassin's auklets exposed to oil . Archives of Environmental Contamination and Toxicology . 1985 ; 14 ( 6 ): 725 - 37 .
2. Leighton FA . The toxicity of petroleum oils to birds . Environmental Reviews . 1993 ; 1 ( 2 ): 92 - 103 .
3. Helm RC , Carter HR , Ford RG , Fry DM , Moreno RL , Sanpera C , et al. Overview of efforts to document and reduce impacts of oil spills on seabirds : John Wiley & Sons, Inc. Hoboken, NJ; 2015 .
4. Troisi G , Barton S , Bexton S. Impacts of oil spills on seabirds: Unsustainable impacts of non-renewable energy . International Journal of Hydrogen Energy . 2016 ; 41 ( 37 ): 16549 - 55 . https://doi.org/10.1016/j. ijhydene. 2016 . 04 .011
5. Eisler R . Polycyclic aromatic hydrocarbon hazards to fish, wildlife, and invertebrates: a synoptic review . Patuxent Wildlife Research Center, Laurel, MD (USA), 1987 .
6. Khan R , Ryan P. Long term effects of crude oil on common murres (Uria aalge) following rehabilitation . Bulletin of Environmental Contamination and Toxicology . 1991 ; 46 ( 2 ): 216 - 22 . PMID: 2018868
7. Aldrich JW . Review of the problem of birds contaminated by oil and their rehabilitation . 1970 .
8. Briggs KT , Gershwin ME , Anderson DW . Consequences of petrochemical ingestion and stress on the immune system of seabirds . ICES Journal of Marine Science . 1997 ; 54 ( 4 ): 718 - 25 .
9. Anderson DW , Gress F , Fry DM . Survival and dispersal of oiled brown pelicans after rehabilitation and release . Marine pollution bulletin . 1996 ; 32 ( 10 ): 711 - 8 .
10. Sharp BE . Post-release survival of oiled, cleaned seabirds in North America . Ibis. 1996 ; 138 ( 2 ): 222 - 8 .
11. Fry DM , Swenson J , Addiego L , Grau C , Kang A. Reduced reproduction of wedge-tailed shearwaters exposed to weathered Santa Barbara crude oil . Archives of Environmental Contamination and Toxicology . 1986 ; 15 ( 4 ): 453 - 63 .
12. Perez C , Lores M , Velando A . Oil pollution increases plasma antioxidants but reduces coloration in a seabird . Oecologia . 2010 ; 163 ( 4 ): 875 - 84 . Epub 2010/06/10. https://doi.org/10.1007/s00442-010-1677- 2 PMID: 20532916 .
13. Fallon JA , Smith EP , Schoch N , Paruk JD , Adams EA , Evers DC , et al. Hematological indices of injury to lightly oiled birds from the Deepwater Horizon oil spill . Environ Toxicol Chem . 2018 ; 37 ( 2 ): 451 - 61 . Epub 2017/10/13. https://doi.org/10.1002/etc.3983 PMID: 29024020 .
14. Giese M , Goldsworthy SD , Gales R , Brothers N , Hamill J. Effects of the Iron Baron oil spill on little penguins (Eudyptula minor) . III. Breeding success of rehabilitated oiled birds . Wildlife Research . 2000 ; 27 ( 6 ): 583 - 91 .
15. Goldsworthy SD , Giese M , Gales R , Brothers N , Hamill J. Effects of the Iron Baron oil spill on little penguins (Eudyptula minor). II. Post-release survival of rehabilitated oiled birds . Wildlife Research . 2000 ; 27 ( 6 ): 573 - 82 .
16. Golightly RT , Newman SH , Craig EN , Carter HR , Mazet JA . Survival and behavior of western gulls following exposure to oil and rehabilitation . Wildlife Society Bulletin . 2002 : 539 - 46 .
17. Altwegg R , Crawford RJ , Underhill LG , Williams ATJ . Long-term survival of de-oiled Cape gannets Morus capensis after the Castillo de Bellver oil spill of 1983 . Biological Conservation. 2008 ; 141 ( 7 ): 1924 - 9 .
18. Newman SH , Golightly RT , Craig EN , Carter HR , Kreuder C. The effects of petroleum exposure and rehabilitation on post-release survival, behavior, and blood health indices: A Common Murre (Uria aalge) case study following the Stuyvesant petroleum spill . Final Report Oiled Wildlife Care Network , Wildlife Health Center, UC Davis, CA. 2004 .
19. De la Cruz SE , Takekawa JY , Spragens KA , Yee J , Golightly RT , Massey G , et al. Post-release survival of surf scoters following an oil spill: an experimental approach to evaluating rehabilitation success . Mar Pollut Bull . 2013 ; 67 ( 1-2 ): 100 - 6 . Epub 2013/01/01. https://doi.org/10.1016/j.marpolbul. 2012 . 11 .027 PMID: 23273616 .
20. Mills KL , Gaydos JK , Fiorello CV , Whitmer ER , Cruz SDL , Mulcahy DM , et al. Post-release survival and movement of western grebes (Aechmophorus occidentalis) implanted with intracoelomic satellite transmitters . Waterbirds . 2016 ; 39 ( 2 ): 175 - 86 .
21. Miller EK , T; Bystrak D ; and Norton T Banded bird reports following the Deepwater Horizon Spill . Proceedings of the 11th International Conference on the Effects of Oil on Wildlife . 2012 .
22. Chilvers B , Morgan K , Finlayson G , Sievwright KJMpb . Diving behaviour of wildlife impacted by an oil spill: A clean-up and rehabilitation success? 2015 ; 100 ( 1 ): 128 - 33 .
23. Henkel LA , Ziccardi MHJJoF , Management W. Life and Death: How Should We Respond to Oiled Wildlife? 2017 ; 9 ( 1 ): 296 - 301 .
24. Hill GE . Ornamental traits as indicators of environmental health . BioScience . 1995 ; 45 ( 1 ): 25 - 31 .
25. Geens A , Dauwe T , Eens M. Does anthropogenic metal pollution affect carotenoid colouration, antioxidative capacity and physiological condition of great tits (Parus major)? Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2009 ; 150 ( 2 ): 155 - 63 .
26. Perez C , Munilla I , Lopez-Alonso M , Velando A . Sublethal effects on seabirds after the Prestige oil-spill are mirrored in sexual signals . Biol Lett . 2010 ; 6 ( 1 ): 33 - 5 . Epub 2009/09/04. https://doi.org/10.1098/rsbl. 2009 .0567 PMID: 19726443; PubMed Central PMCID : PMCPMC2817249 .
55. Dunstan T. A harness for radio-tagging raptorial birds . Inland bird banding news . 1972 ; 44 : 4 - 8 .
56. Lamb JS , Satge? YG, Fiorello CV , Jodice PGR . Behavioral and reproductive effects of bird-borne data logger attachment on Brown Pelicans (Pelecanus occidentalis) on three temporal scales . Journal of Ornithology . 2016 ; 158 ( 2 ): 617 - 27 . https://doi.org/10.1007/s10336-016-1418-3
57. Evans RM . Cold-induced calling and shivering in young American white pelicans: honest signalling of offspring need for warmth in a functionally integrated thermoregulatory system . Behaviour . 1994 ; 129 ( 1 ): 13 - 34 .
58. Team RC . R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing , Austria, 2015 . ISBN 3-900051-07-0: URL http://www.R-project.org; 2018 .
59. Anderson DW , Anderson I. Distribution and status of Brown Pelicans in the California Current . American Birds . 1976 ; 30 : 3 - 12 .
60. Godfrey J , Bryant D. Effects of radio transmitters: Review of recent radio-tracking studies . Science for Conservation . 2003 ; 214 : 83 - 95 .
61. Barron DG , Brawn JD , Weatherhead PJ . Meta-analysis of transmitter effects on avian behaviour and ecology . Methods in Ecology and Evolution . 2010 ; 1 ( 2 ): 180 - 7 . https://doi.org/10.1111/j.2041- 210X . 2010 . 00013 .x
62. Kesler DC , Raedeke AH , Foggia JR , Beatty WS , Webb EB , Humburg DD , et al. Effects of satellite transmitters on captive and wild mallards . Wildlife Society Bulletin . 2014 ; 38 ( 3 ): 557 - 65 .
63. Mazet JA , Newman SH , Gilardi KV , Tseng FS , Holcomb JB , Jessup DA , et al. Advances in oiled bird emergency medicine and management . Journal of Avian Medicine and Surgery . 2002 ; 16 ( 2 ): 146 - 9 .
64. Blount JD , Metcalfe NB , Birkhead TR , Surai PF . Carotenoid modulation of immune function and sexual attractiveness in zebra finches . Science . 2003 ; 300 ( 5616 ): 125 - 7 . https://doi.org/10.1126/science. 1082142 PMID: 12677066
65. Faivre B , Gre?goire A , Pre?ault M, Ce?zilly F , Sorci G . Immune activation rapidly mirrored in a secondary sexual trait . Science . 2003 ; 300 ( 5616 ): 103 -. https://doi.org/10.1126/science.1082026 PMID: 12677062
66. Alonso-Alvarez C , Bertrand S , Devevey G , Gaillard M , Prost J , Faivre B , et al. An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity . The American Naturalist . 2004 ; 164 ( 5 ): 651 - 9 . https://doi.org/10.1086/424971 PMID: 15540154
67. Alonso-Alvarez C , Galva?n I. Free radical exposure creates paler carotenoid-based ornaments: a possible interaction in the expression of black and red traits . PLoS One . 2011 ; 6 ( 4 ):e19403. https://doi.org/ 10.1371/journal.pone. 0019403 PMID: 21556328
68. Johnsen SJJoEB. How to measure color using spectrometers and calibrated photographs . 2016 ; 219 ( 6 ): 772 - 8 .
69. Alonso-Alvarez C , Bertrand S , Faivre B , Chastel O , Sorci G . Testosterone and oxidative stress: the oxidation handicap hypothesis . Proceedings of the Royal Society of London B: Biological Sciences . 2007 ; 274 ( 1611 ): 819 - 25 .
70. McGraw KJ , Hill GE . Differential effects of endoparasitism on the expression of carotenoid-and melanin-based ornamental coloration . Proceedings of the Royal Society of London B: Biological Sciences . 2000 ; 267 ( 1452 ): 1525 - 31 .
71. Lumpkin DC , Murphy TG , Tarvin KA . Blood parasite infection differentially relates to carotenoid-based plumage and bill color in the American goldfinch . Ecology and evolution . 2014 ; 4 ( 16 ): 3210 - 7 . https:// doi.org/10.1002/ece3.1164 PMID: 25473474
72. Schull Q , Dobson FS , Stier A , Robin J-P , Bize P , Viblanc VA . Beak color dynamically signals changes in fasting status and parasite loads in king penguins . Behavioral Ecology . 2016 :arw091.
73. Dey CJ , Quinn JS , King A , Hiscox J , Dale JJTA . A bare-part ornament is a stronger predictor of dominance than plumage ornamentation in the cooperatively breeding Australian Swamphen . 2017 ; 134 ( 2 ): 317 - 29 .
74. Dearborn D , Ryan M. A test of the Darwin-Fisher theory for the evolution of male secondary sexual traits in monogamous birds . Journal of Evolutionary Biology . 2002 ; 15 ( 2 ): 307 - 13 .
75. Montoya B , Torres R . Male skin color signals direct and indirect benefits in a species with biparental care . Behavioral Ecology . 2014 ; 26 ( 2 ): 425 - 34 .
76. Anderson DW , God??nez- Reyes CR , Velarde E , Avalos-Tellez R , Ram? ?rez-Delgado D , Moreno-Prado H , et al. Brown Pelicans, Pelecanus occidentalis californicus (Aves: Pelecanidae): Five decades with ENSO, dynamic nesting, and contemporary breeding status in the Gulf of California . 2017 .