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Post-release survival of surf scoters following an oil spill: An experimental approach to evaluating rehabilitation success

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Marine Pollution Bulletin xxx (2012) xxx–xxx

Contents lists available at SciVerse ScienceDirect

Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul

Post-release survival of surf scoters following an oil spill: An experimental
approach to evaluating rehabilitation success
Susan E.W. De La Cruz a,⇑, John Y. Takekawa a, Kyle A. Spragens a,1, Julie Yee b, Richard T. Golightly c,
Greg Massey d,2, Laird A. Henkel e, R. Scott Larsen d,3, Michael Ziccardi d
a

U.S. Geological Survey, Western Ecological Research Center, San Francisco Bay Estuary Field Station, Vallejo, CA 94592, United States
U.S. Geological Survey, Western Ecological Research Center, Sacramento, CA 95819, United States
Department of Wildlife, Humboldt State University, Arcata, CA 95521, United States
d
Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, CA 95616, United States
e
Office of Spill Prevention and Response, California Department of Fish and Game, Santa Cruz, CA 95060, United States
b
c

a r t i c l e

i n f o

Keywords:
San Francisco Bay
Melanitta perspicillata
Sea duck
Wildlife rehabilitation
Oil exposure
Radio telemetry

a b s t r a c t
Birds are often the most numerous vertebrates damaged and rehabilitated in marine oil spills; however,
the efficacy of avian rehabilitation is frequently debated and rarely examined experimentally. We compared survival of three radio-marked treatment groups, oiled, rehabilitated (ORHB), un-oiled, rehabilitated
(RHB), and un-oiled, non-rehabilitated (CON), in an experimental approach to examine post-release survival of surf scoters (Melanitta perspicillata) following the 2007 M/V Cosco Busan spill in San Francisco
Bay. Live encounter-dead recovery modeling indicated that survival differed among treatment groups
and over time since release. The survival estimate (±SE) for ORHB was 0.143 ± 0.107 compared to CON
(0.498 ± 0.168) and RHB groups (0.772 ± 0.229), suggesting scoters tolerated the rehabilitation process
itself well, but oiling result; ed in markedly lower survival. Future efforts to understand the physiological
effects of oil type and severity on scoters are needed to improve post-release survival of this species.
Ó 2012 Published by Elsevier Ltd.

1. Introduction
Birds are often among the most affected vertebrate species in
marine oil spills. For example, avian mortality rates after the
2010 Deepwater Horizon spill in the Gulf of Mexico showed the
greatest increase compared to all other tetrapod vertebrate groups
(Antonio et al., 2011). Such oil spill related mortality not only
causes direct damage but can have profound impacts on marine
bird population demographics (Votier et al., 2005; Henkel et al.,
2012) including restricting survival and population recovery for
many years afterwards, as was the case for sea ducks exposed to
residual oil from the 1989 Exxon Valdez spill in Alaska (Esler
et al., 2000, 2002). Given the large numbers influenced by oiling,
marine birds have been frequent subjects of rehabilitation.
⇑ Corresponding author. Address: U.S. Geological Survey, Western Ecological
Research Center, San Francisco Bay Estuary Field Station, 505 Azuar Drive, Vallejo,
CA 94592, USA. Tel.: +1 707 562 2004; fax: +1 707 562 3001.
E-mail address: sdelacruz@usgs.gov (S.E.W. De La Cruz).
1
Present address: Yukon Delta National Wildlife Refuge, State Highway Box 346,
Bethel, AK 99559, United States.
2
Present address: SAS Institute Inc., 100 SAS Campus Drive, Cary, NC 27513, United
States.
3
Present address: Department of Veterinary Medicine, Denver Zoo, 2300 Steele
Street, Denver, CO 80205, United States.

Wildlife rehabilitation plays a prominent public role and commands considerable resources during clean-up efforts after major
marine oil spill events. While rehabilitation of oiled wildlife is
common practice worldwide and mandated in California, its efficacy is often debated (Sharp, 1996; Estes, 1998; Jessup, 1998). Part
of the controversy surrounding this practice centers on the survival
of individuals released to the wild after treatment (Estes, 1998).
Results of studies designed to evaluate avian post-release survival
have been varied (Anderson et al., 1996; Sharp, 1996; Goldsworthy
et al., 2000; Golightly et al., 2002; Altwegg et al., 2008), and several
factors, including species, sex, body condition, degree of oiling,
type of oil, and climatic conditions are known to play a role in survival outcomes (Goldsworthy et al., 2000). Recent advances in
rehabilitative techniques (Mazet et al., 2002) have the potential
to improve post-release survival, and continued experimental
study is needed to evaluate their effects.
On 7 November 2007, the M/V Cosco Busan released 53,569 gallons of bunker oil into San Francisco Bay (SFB), California near the
Oakland-San Francisco Bay Bridge. The surf scoter, (Melanitta
perspicillata), a benthic-foraging sea duck, was the species most affected by the Cosco Busan spill (Hampton et al., 2008). Scoters are
one of the most numerous waterfowl species wintering in this
estuary, and SFB scoters comprise 39% of all those overwintering
along the North American lower Pacific Flyway (1988–2009

0025-326X/$ - see front matter Ó 2012 Published by Elsevier Ltd.
http://dx.doi.org/10.1016/j.marpolbul.2012.11.027

Please cite this article in press as: De La Cruz, S.E.W., et al. Post-release survival of surf scoters following an oil spill: An experimental approach to evaluating rehabilitation success. Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.11.027

2

S.E.W. De La Cruz et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx

average; Accurso, 1992; USFWS, 2009). Scoter species (including
surf, white-winged M. fusca, and black M. americana scoters) in
North America have declined by as much as 50% over the past 30
to 50 years (Hodges et al., 1996; Dickson and Gilchrist, 2002;
Nysewander et al., 2005). Long-lived waterfowl species with low
reproductive potential such as scoters are particularly sensitive
to changes in adult survival (Goudie et al., 1994) and may have
the most difficulty recovering from oil spills (Samuels and Ladino,
1983/1984). Additionally, many sea ducks show high winter site
fidelity and pair on wintering areas; thus, factors that affect
survival rates in SFB could have disproportionate effects on local
subpopulations (Esler et al., 2000).
Following the Cosco Busan spill, more than one thousand oiled
scoters were treated by the Oiled Wildlife Care Network (OWCN)
using a standardized marine bird protocol (OWCN, 2001). Postrehabilitation survival of scoters had not been previously studied
but was of particular interest given that they comprise a significant
component of birds oiled in Pacific coast wintertime spill events
(Savard et al., 1998; Hampton et al., 2003). We used an experimental
approach to design a marked-bird study that compared survival of
scoters externally oiled and rehabilitated (ORHB) with two control
treatment groups: un-oiled, rehabilitated (RHB) and un-oiled, nonrehabilitated (CON). We predicted that oiling and the rehabilitation
process itself could have effects on survival such that CON birds
would have highest survival followed by RHB and then ORHB birds.

2. Methods
2.1. Treatment, radio-marking and data collection
We captured beached, oiled scoters by hand from several locations (Fig. 1) around SFB during 8–21 November 2007. We used
netguns (Coda Enterprises, Inc., Mesa, AZ) from a 4 m Boston Whaler to capture birds in Central and San Pablo Bays during 30
November–16 December 2007 (Fig. 1) for the RHB and CON treatment groups. Captured scoters were placed in holding cages and
brought to a U.S. Geological Survey (USGS) research field station
in Vallejo, California or to the OWCN rehabilitation center in Cordelia, California for processing. We banded, weighed, and measured
each captured scoter. We used a combination of plumage characteristics and cloacal examination to determine sex and bursal
depth measurements to determine age (Mather and Esler, 1999).
Coelomic radio transmitters with external whip antennas (18–
19 g, model A2310, Advanced Telemetry Systems, Insanti, MN,
USA) were surgically implanted (Olsen et al., 1992; Korschgen
et al., 1996; Mulcahy and Esler, 1999) by experienced veterinarians
in juvenile and after-second-year (ASY) male and female scoters.
Implant transmitters were used because they have been shown
to be less disruptive and cause fewer behavioral modifications than
external attachment methods for some wild waterfowl (Rotella
et al., 1993; Hupp et al., 2003). Coelomic implant transmitters
are preferred for scoters relative to other transmitter types when
data are collected over a long period of time (Iverson et al., 2006).
Scoters in ORHB and RHB groups underwent treatment and surgery at the OWCN facility. Birds in both groups were treated following established rehabilitative protocols (OWCN, 2001; Mazet
et al., 2002) that included administration of charcoal and isotonic
fluids, oil removal (ORHB group) and cleaning, assistance with
thermoregulation, diagnostic blood work, rehydration, and nutritional supplementation. After rehabilitative treatments were
administered, scoters in both groups were radio-marked and kept
post-surgery at the facility until their feathers were deemed fully
waterproofed and they exhibited normal buoyancy. Marked scoters in ORHB and RHB that died before release were not included
in the study (N = 6 ORHB, N = 6 RHB). At the USGS field station,

we radio-marked CON scoters within 24 h of capture and kept
them up to 2 h following implant surgeries prior to release. Subcutaneous fluids were administered to CON birds every 4–5 h
throughout the period of captivity to minimize the risk of dehydration. Two CON birds died immediately after surgery and were not
included in the survival analysis. Marked scoters were released in
the northern reach of SFB at the Carquinez Strait in Vallejo (ORHB
and RHB), and from the Hercules shoreline (ORHB, RHB, and CON;
Fig. 1). One marked ORHB scoter that escaped from the rehabilitation facility after processing was subsequently heard in the survey
area and included in our analyses.
We conducted aerial telemetry flights in a fixed-wing aircraft 2–
3 times a week for a total of 34 flights between 16 December 2007
and 7 May 2008 to determine location and status of all marked
birds. We used a left–right switch-box system to isolate signals on
either side of the airplane and determine locations (Gilmer et al.,
1981). Each transmitter was equipped with a mortality sensor that
doubled the pulse rate of the transmitter when motionless for 8 h.
For each survey, we recorded whether a scoter was detected or
not, and whether or not detected scoters were alive or dead. Identified mortalities were confirmed by recovery of the carcass or transmitter. The area monitored included bays and the coastline to the
north and south of SFB from Bodega Bay to Monterey Bay, including
all SFB sub-bays (South, Central, San Pablo, and Suisun), and adjacent wetlands (Fig. 1 inset – see survey area). Transmitters could
be heard from 24 km away at an average flight altitude of 460 m;
therefore, we identified a 24 km buffer zone around the flight path
within which we assumed all transmitters could be heard. California
Department of Fish and Game also conducted three extended telemetry flights along the California coast during March 2008 to listen for
marked birds that might have left the study area. Dates and areas
covered on these flights were: 24 March, Ventura north to Pismo
Beach; 25 March, Pismo Beach north to SFB; 27 March, Point Arena
north to the Oregon border (Fig. 1 inset).
2.2. Data analyses
We used a live encounter – dead recovery model (Burnham,
1993; Cooch and White, 2005) in Program MARK (White and
Burnham, 1999) to estimate winter fates of scoters. This joint model extends standard Cormack–Jolly–Seber models of live capture–
recapture data and estimates additional parameters (Burnham,
1993). The four parameters included in live encounter-dead recovery models are: S (the probability of surviving the interval), r (the
probability of being dead and reported), F (the probability of fidelity to the sampling region or remaining in the sample), and p (the
probability of detection or recapture, conditional on being alive
and in the sampling region) (Cooch and White, 2005). This model
was most appropriate for our data as detection probability (p)
was less than one for individuals across treatments (Murray and
Patterson, 2006). Live encounter-dead recovery models allow for
the assumption that a bird not detected during one time interval
could be either dead or alive and not resighted and does not censor
that individual from the interval (Cooch and White, 2005).
We constructed a series of 14 a priori candidate models which
were designed to evaluate S given all possible combinations of
group and time effects, and we included models with body mass
and sex as covariates. We did not adjust mass for structural size
of each bird, because recent studies have shown little or no
improvement with adjustments over body mass alone to predict
body condition (Schamber et al., 2009). In all models, we set
F = 0.986, based on data from un-oiled, non-rehabilitated surf scoters radio-marked from 2003 to 2005 in which only 2 of 149 individuals permanently emigrated from the study area during
winter (De La Cruz et al., unpublished data). In all models, we assumed r and p varied among treatment groups but not with respect

Please cite this article in press as: De La Cruz, S.E.W., et al. Post-release survival of surf scoters following an oil spill: An experimental approach to evaluating rehabilitation success. Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.11.027

S.E.W. De La Cruz et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx

3

Fig. 1. Map of San Francisco Bay and surrounding coast showing capture locations and the extent of shoreline oiling due to the M/V Cosco Busan oil spill (taken from California
Department of Fish and Game, Office of Spill Prevention and Response). The inset figure shows the survey area (shaded) flown during each of 31 telemetry flights over the
survival study period. Lines along the coast show the starting points, extent and dates of three flights conducted in March to look for marked scoters that had left the study
area.

to time, because neither mortality nor detection was variable
across encounter occasions. We evaluated appropriate null models,
including a no effects model, and models to test our assumptions
about r, p, and F. Age was not included as a covariate in any model,
since most of the marked individuals were adults (Table 1). We
incorporated encounter data from 31 telemetry flights spanning
16 December 2007 to 7 April 2008 in our candidate models. Data
obtained from three flights after 7 April were not included in our
analyses, as earlier work showed the mean departure date of satellite-marked scoters for spring migration was 10 April (De La Cruz
et al., 2009), and we assumed birds missing after that date could
have begun migration. We chose to use the mean spring migration
date as a more conservative cut-off date for our study as compared
to the beginning of migration in early March (De La Cruz et al.,
2009), because known mortalities occurred throughout March.
We did not use a fixed post-surgical period for censoring birds
(commonly 1–2 weeks for recovery in implant studies) because
ORHB and RHB birds were held for an indefinite period until they
regained their waterproofing, whereas CON birds were released

within hours of surgery (Table 1). Due to lack of statistical power,
we did not include post-surgery recovery time or total time in captivity as covariates in our models.
Within Program MARK, we constructed models with the design
matrix tools and logit-link function and calculated parameter estimates and variances for each model. We assessed goodness-of-fit
using the most general model having adequately estimated parameters by applying the median ĉ approach in MARK, in which we
simulated data with a range of overdispersion parameter (c) values, obtained a deviance ĉ for each of the simulated data sets,
and used logistic regression to identify the c which caused median
deviance ĉ to equal the observed ĉ. We used this estimated value
(ĉ = 1.13, SE = 0.01) to compute quasi log-likelihood values
(Burnham and Anderson, 2002). We used Quasi-Akaike’s Information Criterion with a second-order bias correction (QAICc; Burnham
and Anderson, 2002) to compare among models and estimated
model fit based on values of QAICc, the number of parameters
(K), and the deviance. Models were ranked and compared with
DQAICc and QAICc weights, where DQAICc estimated relative

Please cite this article in press as: De La Cruz, S.E.W., et al. Post-release survival of surf scoters following an oil spill: An experimental approach to evaluating rehabilitation success. Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.11.027

4

S.E.W. De La Cruz et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx

Table 1
Sample size by sex and age, and means (SE) and ranges of mass, capture, surgery, and release dates for radio-marked surf scoters from each treatment group (ORHB = oiled,
rehabilitated; RHB = un-oiled, rehabilitated; CON = un-oiled, non-rehabilitated). All dates are expressed as ordinal dates.
Treatment group

Sex/agea
Male
HY

a
b
c

Total N

Release mass (g)

Capture date

Surgery date

Release date

Recovery
timeb

Time in
captivityc

844.4 (14.8)
695–975
861.3 (19.7)
790–1020
1003.8 (26.6)
820–1280
912.8 (16.2)
695–1280

317.3 (0.8)
312–325
342.5 (1.3)
334–347
348.8 (0.2)
348–350
337.8 (1.9)
312–350

337 (0.6)
334–343
348.9 (1.2)
340–353
350.2 (0.1)
349–351
345.6 (0.9)
334–353

352 (1.3)
345–365
357 (1.4)
347 – 365
350.6 (0.1)
350–351
352.7 (0.7)
345–365

15 (1.0)
9–24
8.1 (0.7)
5–12
0.3 (0.1)
0–1
7.2 (0.9)
0–24

34.8 (1.9)
20–51
14.5 (0.7)
11–18
1.7 (0.1)
1–2
15.3 (2.0)
1–51

Female
AHY

HY

AHY

ORHB

2

5

0

11

18

RHB

1

7

0

7

15

CON

0

11

0

11

22

OVERALL

3

22

0

29

55

HY = Hatch year, designates a bird hatched during the summer prior to the study. AHY = After hatch year, designates a bird older than one year.
Recovery time = mean (SE) and range of time in days between surgery and release.
Time in captivity = mean (SE) and range of total time in days between intake and release.

differences between the top ranked model and each of the other
models, and QAICc weights indicated the support for a model relative to the others in the candidate set. Additionally, we calculated
evidence ratios (w1/wj), where w1 was the weight of the top ranked
model and wj was the weight of lower ranked models in the candidate set (Burnham and Anderson, 2002).
We also examined beta values (b), standard error (SE), and confidence intervals for variables of interest in the most parsimonious
model that included those variables. Beta values are modelestimated slopes, interpreted on the basis of direction and their
effect size relative to associated variation. Based on Esler and
Iverson (2010), we used a criterion of SE bi < bi to identify variables
that had a potential biological relationship with survival. We used
model averaging across the candidate model set to generate cumulative winter survival, detection, and recovery estimates for each
treatment group. We used the variance–covariance matrix generated in MARK to calculate standard errors by the delta method
(Williams et al., 2002; Powell, 2007), as well as confidence intervals in R (version 2.13.0; R Development Core Team, 2011).

3. Results
We released 55 radio-marked scoters in SFB between 11 and 31
December 2007 (Table 1). Capture dates for RHB and CON scoters
overlapped each other but were later than those of ORHB scoters
(Table 1). The range of surgery and release dates overlapped among
all three treatment groups (Table 1). The average number of days
between surgery and release (recovery time) and in captivity were
longest for ORHB, versus RHB and CON birds (Table 1). We recorded 687 aerial telemetry locations during the survival study.
Of these, 132 locations were from ORHB, 255 from RHB, and 300
from CON scoters. All locations were obtained within the surveyed
study area (Fig. 1 and inset), and no marked scoters were detected
during the three extended coastal flights conducted by California
Department of Fish and Game in March (Fig. 1 inset).
Among the 14 candidate models we evaluated to explain variation in scoter survival, the best-supported model (QAICc = 1119.47,
wi = 0.31) indicated S varied as a function of treatment group and
followed a consistent trend over encounter occasions, and that p
and r also varied among groups (Table 2). The evidence for this
model was only 1.17 times higher than the second highest ranking
model (QAICc = 1119.78, wi = 0.27), which specified S varied as a
function of treatment group, and had no time trend. Weights for
models ranked 3rd (wi = 0.17) and 4th (wi = 0.12) indicated weaker
support for the additive effects of treatment group and body mass
(1.87 times lower) or treatment group and sex (2.59 times lower).

The beta estimates for release mass in model 3 (0.004, Table 2) and
sex in model 4 (0.468, Table 2) were equal to or less than their
associated standard errors (0.004 and 0.606, respectively) and their
95% confidence intervals both overlapped zero, indicating a lack of
meaningful effects. We found little support for any of the remaining models (wi 6 0.05), including the no effects model (Table 2,
model 7) which had an evidence ratio 25.15 times lower than
the highest ranking model.
We averaged across all models (Burnham and Anderson, 2002)
to determine cumulative winter estimates of S, p, and r for each of
the three treatment groups. Cumulative survival curves plotted
over all encounter occasions (Fig. 2) demonstrated low initial survival for ORHB scoters compared to other groups and a steep decline over encounter occasions, while survival for RHB and CON
groups displayed a more gradual decline. The resulting estimates
for S (± standard error, 95% confidence intervals) were 0.143
(±0.107, 0.032–0.636) for ORHB, 0.772 (±0.229, 0.427–1.000) for
RHB, and 0.498 (±0.168, 0.254–0.977) for CON (Fig. 2). Model averaged estimates of p and r followed a similar trend among treatment
groups. Estimates of p were 0.727 (±0.038, 0.646–0.795) for ORHB,
0.823 (±0.024, 0.770–0.866) for RHB, and 0.769 (±0.023, 0.721–
0.811) for CON. Estimates for r were 0.205 (±0.112, 0.063–0.498)
for ORHB, 0.843 (±0.379, 0.019–0.999) for RHB, and 0.603
(±0.230, 0.187–0.909) for CON.

4. Discussion
We used live-encounter dead-recovery models to evaluate survival (S) in light of detection (p), recovery (r), and site fidelity (F)
rates of marked scoters in each of our three treatment groups.
We found strong support for models that indicated winter survival
of scoters differed among treatment groups in our study, and was
lowest for ORHB birds. Contrary to our predictions, we found that
survival was not negatively influenced by the rehabilitation process itself, as evidenced by the fact that RHB birds had higher survival than CON birds. In addition, the highest ranked model
indicated that mortality was likely to occur early in the study for
ORHB birds. Small sample sizes resulted in overlap of 95% confidence intervals among groups; however, the cumulative model
averaged survival estimate for ORHB (0.143) was substantially
lower than that of both RHB (0.772) and CON (0.498) scoters.
Likewise, estimates for reporting of dead scoters (r) and detection of live scoters (p) also differed among groups in our top models and were lowest for ORHB birds. In particular, the low estimate
of r for ORHB scoters (0.205) reflects a large number of birds that
either died and were not reported or disappeared early in the

Please cite this article in press as: De La Cruz, S.E.W., et al. Post-release survival of surf scoters following an oil spill: An experimental approach to evaluating rehabilitation success. Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.11.027

5

S.E.W. De La Cruz et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx

Table 2
Ranking of models used to estimate winter fates of surf scoters in a live encounter – dead recovery analysis. The best-fitting model is that with the lowest QAICc value and support
for each model is indicated by difference in its QAICc value from the best model (DQAICc) and its QAICc weight.
a

Model rank

Model Description

1
2
3
4
5
6
7
8
9
10
11
12
13
14

{S(g + T)p(g)r(g)F(0.986)}
{S(g)p(g)r(g)F(0.986)}
{S(g + weight)p(g)r(g)F(0.986)}
{S(g + sex)p(g)r(g)F(0.986)}
{S(gT)p(g)r(g)F(0.986)}
{S(T)p(g)r(g)F(0.986)}
{S(.)p(.)r(.)F(.)}
{S(.)p(g)r(g)F(0.986)}
{S(.)p(.)r(.)F(0.986)}
{S(t)p(g)r(g)F(0.986)}
{S(g + t)p(g)r(g)F(0.986)}
{S(gt)p(g)r(g)F(0.986)}
{S(gt + weight)p(g)r(g)F(0.986)}
{S(gt + sex)p(g)r(g)F(0.986)}

QAICc

DQAICc

QAICc
weight (wi)

Evidence
ratios

Model
likelihood

Number of
parameters (K)

QDeviance

1119.47
1119.78
1120.73
1121.37
1123.41
1124.01
1124.41
1125.26
1125.92
1151.32
1180.96
1264.83
1267.14
1274.16

0
0.31
1.26
1.90
3.93
4.53
4.93
5.79
6.45
31.84
61.48
145.36
147.67
154.68

0.31
0.27
0.17
0.12
0.04
0.03
0.03
0.02
0.01
0
0
0
0
0

–
1.17
1.87
2.59
7.14
9.64
11.78
18.09
25.15
–
–
–
–
–

1.00
0.86
0.53
0.39
0.14
0.10
0.08
0.06
0.04
0
0
0
0
0

10
9
10
10
12
8
4
7
3
37
39
99
100
100

1099.17
1101.53
1100.42
1101.07
1098.97
1107.81
1116.35
1111.11
1119.89
1073.28
1098.47
1035.65
1035.28
1042.30

a
Key to Model Description notation: S = survival probability, p = detection probability, r = recovery probability, F = probability of fidelity to study area (set at 0.986 for all
models). Tested effects are in parentheses for each parameter – g = treatment group effect, t = time effect over encounter occasions, T = time effect follows a trend over
encounter occasions. ‘‘*’’ indicates an interactive effect, while ‘‘+’’ indicates an additive effect. In Models 3 and 13 release mass was considered as a covariate for survival and
in Models 4 and 14 sex was a covariate of survival.

Fig. 2. Cumulative survival probability curves for 55 radio-marked San Francisco Bay surf scoters in treatment groups ORHB, RHB, and CON during winter 2007–2008. Curves
are determined based on model-averaging across all candidate models. Numbers along the x-axis represent 31 telemetry flights taken over the course of the study period to
collect encounter data on scoters.

study, and this parameter had a strong influence on cumulative
estimates of S. High initial post-release mortality has been reported in marking studies of un-oiled scoters (Iverson et al.,
2006) and in studies of other oiled and rehabilitated species such
as common murres (Uria aalge; Newman et al., 2004). In these
studies, early mortality was attributed to capture and handling
stress. Given the much higher survival rate of RHB birds that
underwent treatments similar to ORHB birds, this explanation
seems less likely in our study; however, we did not directly evaluate capture and handling time as covariates in our models.
While differences among groups for estimates of p were smaller
than for r, ORHB birds were detected less frequently. This may have
occurred if ORHB behavior differed from other groups. For example, birds that spent more time near sheltered or covered areas
or that were diving more frequently might have had a higher likelihood of being missed during aerial telemetry flights. Behavior

results for these treatment groups (Golightly et al., 2011) indicated
that ORHB scoters were found closer to shore than RHB and CON
birds, but there were no differences in dive frequency or duration
among the groups. On the basis of our previous work, we chose to
hold the fourth parameter in our model, fidelity (F), constant at
0.986 for all groups. It is conceivable that this estimate was too
conservative if prey or habitat conditions related to oiling in SFB
caused birds to emigrate in higher numbers than in a typical year.
However, we found no evidence for emigration from the study area
based on coastal flights conducted in March prior to the onset of
spring migration.
The covariates of sex and release mass (Models 3 and 4) had little influence on survival. This differs somewhat from the results of
Goldsworthy et al. (2000), who found that both sex and release
mass significantly affected post-release survival of little penguins
(Eudyptula minor). Over a 20 month period, male little penguins

Please cite this article in press as: De La Cruz, S.E.W., et al. Post-release survival of surf scoters following an oil spill: An experimental approach to evaluating rehabilitation success. Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.11.027

6

S.E.W. De La Cruz et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx

were more likely to survive than females, and the probability of
survival increased by 10% with every 127 g increase in release
mass (Goldsworthy et al., 2000). Incorporating a larger sample size
to better examine the effect of these parameters may be valuable
for scoters, especially since sea duck population dynamics are
particularly sensitive to adult female survival (Goudie et al.,
1994; Esler et al., 2000). Ranges for recovery time and total time
in captivity were distinct among treatment groups; however, we
lacked the statistical power to evaluate them as covariates in our
survival models. Scoter species respond poorly to long periods of
captivity (Rosenberg and Petrula, 2000; Richman and Lovvorn,
2008), so time spent in rehabilitation may negatively impact survival. However, RHB scoters had the highest survival of any group,
yet they spent an intermediate time in recovery and total captivity
compared to the other two treatment groups. This suggests that
extended rehabilitation time itself may not have negatively influence ORHB survival; however, additional work focused on time
in captivity is needed to fully understand its effect.
The cumulative winter survival estimate for RHB birds was similar to that of Harlequin ducks (Histrionicus histrionicus), another
sea duck species, marked on un-oiled areas of Prince William
Sound, Alaska (0.837, Esler et al., 2000; Esler and Iverson 2010),
while CON scoter survival was markedly lower. Supplemental
feeding and extended care of RHB birds could have had beneficial
results, such as improving immune function or waterproofing,
which resulted in higher survival for this group. In addition, CON
scoters were marked in a separate facility by a different surgical
team, which could have had some bearing on their differential survival. However, scoters in all groups were marked using a standard
protocol (Olsen et al., 1992; Korschgen et al., 1996; Mulcahy and
Esler, 1999) that has proven successful in several other studies of
non-oiled surf scoters conducted by various teams across the Pacific coast (e.g. Iverson et al., 2006; Kirk et al., 2008; De La Cruz et al.,
2009; Takekawa et al., 2011); therefore, the marking procedure itself is unlikely to be the source of differences among groups. Marking diving birds with transmitters can influence their descent
speed and dive durations (Latty et al. 2010), and thus may also
have an effect on their survival. In our study, birds from each group
were marked with the same transmitter type to ensure transmitters effects were applied equally to all groups and were not likely
to have caused the survival differences we detected among groups.
The cumulative survival rate of ORHB scoters was lower than
those reported for other species in recent studies (Anderson
et al., 2000; Golightly et al., 2002; Newman et al., 2004) that evaluated use of rehabilitation techniques instituted by OWCN in 1994
(Mazet et al., 2002). Anderson et al. (2000) found that oiled and
rehabilitated American coots (Fulica americana) had a cumulative
survival rate of 49%, while survival of a non-oiled, non-rehabilitated
control group was one and a half times higher at 76%. Golightly
et al. (2002) concluded that 100% of oiled and rehabilitated
Western gulls (Larus occidentalis) treated in 1997 after the Torch/
Platform Irene spill survived to 183 days after release, and that
survival did not differ among this group and rehabilitated and
non-rehabilitated control groups. Newman et al. (2004) studied
survival of oiled and rehabilitated common murres and found that
68% survived at least 80 days after release; however, only 7% of
common murres survived until 142 days. Reasons for the differences seen among these studies may be species-specific, as postrelease survival is highly variable among species (Russell et al.,
2003). For instance, penguins have higher post-rehabilitation survival (Morant et al., 1981; Underhill et al., 1999) than other species,
including sea duck species like the white-winged scoter (Sharp,
1996).
Avian post-rehabilitation survival may also depend on several
other factors, including degree of oiling, type of oil, and climatic
conditions (Goldsworthy et al., 2000), that we did not evaluate in

this study. Ingestion of petroleum hydrocarbons has a wide variety
of documented physiological effects on birds, including anemia
(Leighton et al., 1983), endocrine dysfunction (Peakall et al.,
1981), poor condition (muscle and lipid catabolism – Oka and
Okuyama, 2000) and immunosuppression (Rocke et al., 1984) that
may be delayed or not apparent externally (Khan and Ryan, 1991).
Blood health indices may help determine the extent of physiological damage a bird has sustained and guide treatment. Newman
et al. (2004) showed that some of these indices, including lower total inorganic phosphorous concentration, higher creatine kinase
activity, and higher fibrinogen concentrations, were associated with
decreased survival in common murres. Inclusion of these parameters in more extensive survival analyses on rehabilitated scoters
may help identify health parameters most important to this species.
Scoters spend three-quarters of their annual cycle migrating
and wintering in estuaries and nearshore marine environments
where the potential for them to experience acute mortality or
long-term demographic effects (e.g. Henkel et al. 2012) due to oil
spills is high. When scoters undergo rehabilitation as a result of
an oil spill, post-release studies can provide information needed
to improve treatments, make damage assessments, and ultimately
weigh the costs and benefits of rehabilitation. It is difficult to
determine the fate of oiled, wild birds that remain at sea and are
not subject to treatment (Ford et al. 1987; Piatt et al. 1990); however if we assume that oiled, non-rehabilitated birds suffer 100%
mortality, our data suggest that rehabilitation increased winter
survival by 14.3%. Furthermore, our results demonstrate that unoiled scoters can tolerate modern rehabilitation techniques well.
Given this, survival of rehabilitated oiled scoters, and perhaps
many marine bird species, is likely dependent on several factors related to type of oil, severity of oiling, and species specific physiological effects. Identifying the most influential of these factors is
the future challenge for rehabilitative programs.
Acknowledgements
This study was funded by the Oiled Wildlife Care Network
(OWCN) at the University of California, Davis. OWCN personnel
were directly involved in the rehabilitative care and radio-marking
of scoters, but did not participate in data collection, analyses or
interpretation. All capture, handling, and marking of scoters was
carried out under the guidance and approval of the U.S. Geological
Survey, Western Ecological Research Center, Animal Care and Use
Committee with permits from California Department of Fish and
Game (SC-004857 and SC-003855), U.S. Fish and Wildlife Service
(MB-102896-0), and USGS Bird Banding Laboratory (BBL-22911).
We are grateful for the comments of D. Esler, M. Ricca, and an
anonymous reviewer, which helped to improve this manuscript.
We thank E. Palm, M. Wilson, J. Shinn, S. Rhoades, L. Terrazas, A.
Schultz, H. Robinson, and pilot B. Van Wagenen for assistance with
scoter capture and marking, data collection, and data entry, as well
as P. Gibbons, DVM, for his veterinary expertise. We acknowledge
the assistance of Advanced Telemetry Systems for rapidly producing implant transmitters following the spill. Any use of trade, product, or firm names in this publication is for descriptive purposes
only and does not imply endorsement by the U.S. government.
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