Terrestrial Scavenging of Marine Mammals ... - ACS Publications

Subscriber access provided by La Trobe University Library

Article

Terrestrial scavenging of marine mammals: crossecosystem contaminant transfer and its potential risks to endangered California condors (Gymnogyps californianus) Carolyn M Kurle, Vickie Bakker, Holly Copeland, Joe Burnett, Jennie Jones, Joseph Brandt, and Myra E Finkelstein Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b01990 • Publication Date (Web): 19 Jul 2016 Downloaded from http://pubs.acs.org on July 24, 2016

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 31

Environmental Science & Technology

Terrestrial scavenging of marine mammals: cross-ecosystem contaminant transfer and its potential risks to endangered California condors (Gymnogyps californianus) Carolyn M. Kurle1*, Vickie Bakker2*, Holly Copeland3, Joe Burnett4, Jennie Jones5, Joseph Brandt6, Myra E. Finkelstein7+ 1

Division of Biological Sciences, Ecology, Behavior and Evolution Section, University of California, San Diego, La Jolla, CA, USA, [email protected] 2 Department of Ecology, Montana State University, Bozeman, MT, USA, [email protected] 3 The Nature Conservancy, 258 Main Street, Lander, WY, USA, [email protected] 4 Ventana Wildlife Society, 19045 Portola Dr. Ste. F-1, Salinas, CA, USA, [email protected] 5 National Park Service; Pinnacles National Park, 5000 Highway 146, Paicines, CA, USA, [email protected] 6 United States Fish and Wildlife Service, 2493 Portola Rd. Suite B, Ventura, CA, USA, [email protected] 7 Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA USA, [email protected] *Equal co-first authorship +

Corresponding author: [email protected], 831.459.1249

1 ACS Paragon Plus Environment


Page 2 of 31

1

Abstract

2

The critically endangered California condor (Gymnogyps californianus) has relied intermittently on

3

dead-stranded marine mammals since the Pleistocene and this food source is considered important for

4

their current recovery. However, contemporary marine mammals contain persistent organic pollutants

5

that could threaten condor health. We used stable carbon and nitrogen isotope, contaminant, and

6

behavioral data in coastal versus non-coastal condors to quantify contaminant transfer from marine

7

mammals and created simulation models to predict the risk of reproductive impairment for condors

8

from exposure to DDE (p,p'-DDE), a major metabolite of the chlorinated pesticide DDT. Coastal

9

condors had higher whole blood isotope values and 12 to 100-fold greater mean concentrations of

10

contaminants associated with marine mammals, including mercury (whole blood), sum chlorinated

11

pesticides (comprised of ~95% DDE) (plasma), sum polychlorinated biphenyls (PCBs) (plasma), and

12

sum polybrominated diphenyl ethers (PBDEs) (plasma), than non-coastal condors. The mean plasma

13

DDE concentration for coastal condors was 500±670SD (n=22) versus 25±23SD (n=8) ng/g wet

14

weight for non-coastal condors and simulations predicted ~40% of breeding-age coastal condors have

15

DDE levels associated with eggshell thinning in other avian species. Our analyses demonstrate

16

potentially harmful levels of marine contaminant transfer to California condors, which could hinder

17

the recovery of this terrestrial species.

18 19 20

Introduction Dead-stranded marine vertebrates are a significant nutrient source for terrestrial

21

consumers, and marine-subsidized species exhibit increased population sizes1, 2 and higher

22

survival when terrestrial foods are scarce3. Many avian scavengers feed on marine carcasses

23

along the Pacific coast of North America4, a behavior which may have prevented the extirpation


Page 3 of 31


24

of California condors (Gymnogyps californianus) after the Pleistocene terrestrial megafauna

25

disappeared3, 5. However, marine mammal carcasses can contain high levels of persistent organic

26

pollutants (POPs) such as DDE (p,p'-DDE, a major metabolite of the chlorinated pesticide DDT)

27

and polychlorinated biphenyls (PCBs)6, 7. Thus, the nutritional benefits of marine scavenging

28

may be offset by increased risks of contaminant-related health effects, which is of particular

29

concern for endangered species such as the California condor4, 8.

30

Nearly extinct in the 1980’s8, the condor population has increased through intensive

31

recovery efforts, surpassing 400 birds by 2016, ~half of which are in the wild and associated

32

with release sites in California, Arizona, and Baja California, Mexico. The condor population is

33

not self-sustaining and poisoning from feeding on carcasses contaminated with lead-based

34

ammunition is the primary threat preventing its recovery9, 10. Condors that feed along the coast

35

are thought to be at lower risk of lead poisoning and we have found that coastal behavior is

36

positively associated with a condor’s survival11. However, eggshell thinning and reduced

37

hatching success, likely due to DDE exposure from feeding on beach-cast marine mammals,

38

particularly California sea lions (Zalophus californianus; CASLs), was recently identified in

39

coastal breeding condors and could prove an additional threat to condor population health12.

40

Condor lead exposure is well documented9, 13-15, but data on exposure to DDE and other POPs

41

are limited, despite their potential to affect condor recovery8.

42

The majority (>95%) of the US population of CASLs breeds on the Channel Islands,

43

California16. Nearby waters and sediments were contaminated with PCBs and DDTs discharged

44

by several companies from the 1940’s-1970’s, with Montrose Chemical Corporation expelling

45

over 2000 metric tons of DDTs17. Elevated contaminant levels persist around these islands18, 19

46

and CASLs continue to exhibit high levels of DDTs, the majority of which is DDE7, 20.



47

Page 4 of 31

To investigate the potential risk of marine mammal feeding behavior to condor health we:

48

(a) measured the stable carbon (δ13C) and nitrogen (δ15N) isotope ratios in condor whole blood

49

samples and muscle from potential diet items to estimate the degree to which condors fed on

50

marine mammals, (b) evaluated relationships between marine-associated contaminant (e.g.,

51

PCBs, DDE) concentrations in condors and their observed feeding and spatial behavior, and (c)

52

predicted current flock-wide DDE exposure levels and potential reproductive risks using

53

simulation models. Our findings inform future management of condors by providing a

54

comprehensive assessment of contaminant transfer from feeding on dead-stranded marine

55

mammals while highlighting the broad influence of persistent pollutants in the marine

56

environment including cross-ecosystem risks to terrestrial endangered species.

57 58

Methods

59

Study area and species

60

All condors are assigned an ID (Studbook number) and are of known sex due to their

61

intensive management as an endangered species. We studied free-flying condors associated with

62

two flocks: southern California ("non-coastal"), managed by the USFWS Hopper Mountain

63

National Wildlife Complex, and central California ("coastal"), managed by Ventana Wildlife

64

Society and Pinnacles National Park. The latter moves between the Big Sur coast and inland

65

regions, whereas the former remains inland. Personnel maintain set locations where terrestrial

66

animal carcasses are placed ("proffered feeding stations") to facilitate monitoring. Coastal

67

condors are observed feeding on dead-stranded marine mammals along Big Sur12, whereas

68

southern, non-coastal condors are not considered to feed on marine mammals. Ranges of coastal

69

condors during the study period (2009-2013) overlap with our dead-stranded marine mammal


Page 5 of 31


70

sampling locations and are distinct from non-coastal condor ranges (Supplemental Information;

71

Figure S1).

72

Sample collection

73

Condor blood samples were collected opportunistically during routine health monitoring

74

from 2009–2012 and condors sampled appeared to be in good body condition. All samples were

75

used for stable isotope analysis and a subset of these were analyzed for contaminants (Table S1).

76

Blubber samples (~5 grams) for contaminant analysis were collected from dead-stranded marine

77

mammals in Monterey County, California from 2008–2012. Muscle samples for stable isotope

78

analysis were collected from dead-stranded marine mammals and wild, non-proffered and

79

domestic, proffered terrestrial carcasses in central and southern California from 2010–2012.

80

Marine mammal blubber (n=17 organochlorines, n=7 PBDEs) and condor plasma samples (n=33

81

organochlorines, n=13 PBDEs) were analyzed for contaminants, condor whole blood samples

82

(n=68) were analyzed for total mercury, and diet item muscle (n=60) and condor whole blood

83

samples (n=83) were analyzed for stable isotope ratios (Supplemental Information; Tables S1,

84

S2, S3).

85

Sample analysis (see also Supplemental Information).

86

Plasma and blubber samples were analyzed for 54 congeners of PCBs, 26 chlorinated

87

pesticides including the seven metabolites of DDT, and 27 congeners of PBDEs (Table S4) at the

88

California Department of Fish and Wildlife Water Pollution Control Laboratory. Condor whole

89

blood was analyzed for total mercury by Eurofins Frontier Global Sciences, Inc., Bothell,

90

Washington on a Tekran 2600 Flow Injection Mercury System (FIMS). Condor whole blood and

91

diet item muscle samples were analyzed for their δ13C and δ15N values using a Carlo Erba

92

CE1108 elemental analyzer interfaced via a CONFLO III device to a Thermo-Electron Delta



Page 6 of 31

93

Plus XP mass spectrometer at the Stable Isotope Laboratory at the University of California Santa

94

Cruz Department of Earth and Marine Sciences.

95

Condor daily observational data for the coastal flock Condors were monitored on a near-daily basis via visual observation at proffered feeding

96 97

stations or elsewhere, aided by detection of signals from radio (VHF) and/or GPS transmitters.

98

Daily observational data consisted of 31,985 records of birds, documenting sightings in coastal

99

Big Sur, inland in Pinnacles, and at proffered feeding stations. Observations were also made

100

opportunistically of condors feeding on dead-stranded marine mammals in Big Sur from 1999–

101

2013.

102

Spatial analysis.

103

We quantified space use with hourly GPS (PTT-100 50 g Solar Patagial Argos/GPS;

104

Microwave Telemetry, Inc.) locations from 01/01/2003–7/31/2013, 0500–2000 PST, equaling

105

867,498 locations from 90 unique condors. We summarized geographic ranges for coastal and

106

non-coastal flocks using 99% fixed kernel density estimates from 2009–2013, concurrent with

107

the time period of condor tissue sample collection (Figure S1), using ArcMET (Movement

108

Ecology Tools for ArcGIS)21. To investigate fine-scale patterns of coastal foraging, we ran a

109

separate 99% fixed kernel density estimate for all locations within 1.5 km of the coast for the full

110

dataset (55,012 locations from 37 unique condors), binning results into equal-area quantiles.

111

Statistical Analysis.

112

Coastal vs. non-coastal condors. Statistical tests of contaminant and stable isotope data

113

were performed in R (version 3.0.2, R Core Team, 2013). Stable carbon and nitrogen isotope

114

turnover from blood in birds has been shown to be complete at ~30 days22-24, whereas

115

methylmercury concentrations in avian blood decrease by ~90% within 30 days of exposure25.


Page 7 of 31


116

We considered blood samples from the same individual independent as all samples were

117

collected at intervals greater than or equal to approximately one year and no condors had more

118

than one sample taken for organochlorine or PBDE analysis (Table S1). Only quantifiable

119

compounds were used for determining the sum chlorinated pesticides, sum PCBs, or sum

120

PBDEs; if all compounds within a group (e.g., PCBs) were not quantifiable, half the detection

121

limit of a single compound was used as follows: p,p'-DDE was used for sum chlorinated

122

pesticides, PCB 153 for sum PCBs, and PBDE-47 for sum PBDEs (Supplemental Information).

123

All samples had quantifiable total mercury concentrations. Variables were log-transformed if

124

normality and homoscedasticity were improved, and non-parametric equivalents were utilized

125

when data did not meet assumptions for parametric analyses.

126

Diet of coastal condors. MixSIAR, a Bayesian stable isotope mixing model incorporating

127

discrimination factors for condors on known diets26 and the mean (±SD) δ13C and δ15N values

128

from condors, marine mammals, and terrestrial proffered and non-proffered mammals, was used

129

to estimate proportions of condor diet composed of marine versus terrestrial proffered versus

130

terrestrial non-proffered items. We found no differences in the δ13C (t=0.1.99, P=0.77) and δ15N

131

(t=1.99, P=0.41) values between sexes, so combined sexes for analyses.

132

Behavior affecting contaminant exposure. We assessed whether mercury, PCBs, PBDEs,

133

and DDE levels were predicted by condor foraging behavior, focusing on DDE because it is the

134

most abundant organochlorine in CASLs7 and associated with reproductive failure in avian

135

species27. We considered the cumulative number of observations of condors feeding on marine

136

carcasses, overall and in one and three year windows preceding sample collection. Detecting

137

non-proffered feeding along a wide coastal area is inherently difficult, so to minimize the

138

influence of missing data, we also considered the cumulative number of years an individual was



Page 8 of 31

139

a marine mammal feeder prior to and inclusive of sampling year, and counted an individual as a

140

marine mammal feeder if it was observed feeding on marine mammals at least once in the year.

141

Because gray whales have substantially lower DDE levels than CASLs (this study and7) and

142

condors were observed feeding on individual gray whales for several months, we also considered

143

observations of marine mammal feeding excluding gray whales. We fit contaminant data to these

144

marine feeding observations using linear regression models (Supplemental Information),

145

transforming response and predictor variables to improve normality and homoscedasticity and

146

standardizing continuous predictor variables to facilitate model convergence. Model selection

147

was guided by AICc.

148

We used estimated relationships between observed marine mammal feeding and

149

measured DDE to estimate DDE levels for all condors in the coastal flock based on observed

150

marine mammal feeding behavior from 07/31/2001-07/31/2013, incorporating unexplained

151

variance due to residual SE, and summarized results from 1000 replicate runs (Matlab version

152

8.1) (Supplemental Information). To investigate the possibility that DDE is affecting

153

reproduction, for each simulated run we tracked the proportion of the population that, using a

154

plasma DDE to egg DDE conversion factor reported for other raptors28, exceeded two DDE

155

thresholds approximately equal to egg concentrations of 5000 ng/g and 15000 ng/g wet weight.

156

The lower DDE threshold is associated with 10% and 20% eggshell thinning in bald eagles28 and

157

condors29, respectively, whereas bald eagles approached 100% reproductive failure at the upper

158

DDE threshold28 (Supplemental Information).

159 160

Results

161

δ13C and δ15N and contaminant values


Page 9 of 31

162


We found no differences in the δ13C (t=0.1.99, P=0.77) and δ15N (t=1.99, P=0.41) values

163

between sexes, so combined sexes for analyses. Coastal condors (n=65) had higher mean (±SD)

164

δ13C (-22.1±1.2‰) and δ15N (9.9±1.2‰) values than non-coastal condors (n=18, -23.2±1.2‰

165

and 8.0±0.8‰, respectively) and the mean δ13C and δ15N values from marine mammals (n=17, -

166

17.3±0.8‰ and 17.1±1.0‰, respectively) were also higher than those from all terrestrial animals

167

(n=46, -23.7±2.3‰ and 6.4±1.5‰, respectively) (Figure 1, Table S5), indicating the diet of

168

coastal condors is partially marine-derived. The estimated coastal condor diets (means) for

169

individual birds ranged from 8-52% marine mammals, 26-53% proffered, and 16-63% non-

170

proffered terrestrial items (Table S6), whereas those of non-coastal condors were 28-40%

171

proffered and 44-68% non-proffered terrestrial items.

172

Coastal condors had 12 to 100-fold greater mean concentrations of mercury, chlorinated

173

pesticides, PCBs, and PBDEs than non-coastal condors (all P90% of sum chlorinated pesticides with trans-nonachlor the second most

180

abundant chlorinated pesticide detected (~1-4% of sum) (Table S9). PCB153 was a predominant

181

PCB congener, accounting for 10-48% of sum PCBs, whereas PBDE-47 was the most abundant

182

PBDE congener detected (Table S9). We found strong positive correlations between PBDEs,

183

chlorinated pesticides, and PCBs within individual condors (r≥0.951, p

Terrestrial Scavenging of Marine Mammals ... - ACS Publications

Recommend Documents