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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
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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
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Abstract
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The critically endangered California condor (Gymnogyps californianus) has relied intermittently on
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dead-stranded marine mammals since the Pleistocene and this food source is considered important for
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their current recovery. However, contemporary marine mammals contain persistent organic pollutants
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that could threaten condor health. We used stable carbon and nitrogen isotope, contaminant, and
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behavioral data in coastal versus non-coastal condors to quantify contaminant transfer from marine
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mammals and created simulation models to predict the risk of reproductive impairment for condors
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from exposure to DDE (p,p'-DDE), a major metabolite of the chlorinated pesticide DDT. Coastal
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condors had higher whole blood isotope values and 12 to 100-fold greater mean concentrations of
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contaminants associated with marine mammals, including mercury (whole blood), sum chlorinated
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pesticides (comprised of ~95% DDE) (plasma), sum polychlorinated biphenyls (PCBs) (plasma), and
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sum polybrominated diphenyl ethers (PBDEs) (plasma), than non-coastal condors. The mean plasma
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DDE concentration for coastal condors was 500±670SD (n=22) versus 25±23SD (n=8) ng/g wet
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weight for non-coastal condors and simulations predicted ~40% of breeding-age coastal condors have
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DDE levels associated with eggshell thinning in other avian species. Our analyses demonstrate
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potentially harmful levels of marine contaminant transfer to California condors, which could hinder
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the recovery of this terrestrial species.
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Introduction Dead-stranded marine vertebrates are a significant nutrient source for terrestrial
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consumers, and marine-subsidized species exhibit increased population sizes1, 2 and higher
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survival when terrestrial foods are scarce3. Many avian scavengers feed on marine carcasses
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along the Pacific coast of North America4, a behavior which may have prevented the extirpation
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of California condors (Gymnogyps californianus) after the Pleistocene terrestrial megafauna
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disappeared3, 5. However, marine mammal carcasses can contain high levels of persistent organic
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pollutants (POPs) such as DDE (p,p'-DDE, a major metabolite of the chlorinated pesticide DDT)
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and polychlorinated biphenyls (PCBs)6, 7. Thus, the nutritional benefits of marine scavenging
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may be offset by increased risks of contaminant-related health effects, which is of particular
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concern for endangered species such as the California condor4, 8.
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Nearly extinct in the 1980’s8, the condor population has increased through intensive
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recovery efforts, surpassing 400 birds by 2016, ~half of which are in the wild and associated
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with release sites in California, Arizona, and Baja California, Mexico. The condor population is
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not self-sustaining and poisoning from feeding on carcasses contaminated with lead-based
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ammunition is the primary threat preventing its recovery9, 10. Condors that feed along the coast
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are thought to be at lower risk of lead poisoning and we have found that coastal behavior is
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positively associated with a condor’s survival11. However, eggshell thinning and reduced
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hatching success, likely due to DDE exposure from feeding on beach-cast marine mammals,
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particularly California sea lions (Zalophus californianus; CASLs), was recently identified in
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coastal breeding condors and could prove an additional threat to condor population health12.
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Condor lead exposure is well documented9, 13-15, but data on exposure to DDE and other POPs
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are limited, despite their potential to affect condor recovery8.
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The majority (>95%) of the US population of CASLs breeds on the Channel Islands,
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California16. Nearby waters and sediments were contaminated with PCBs and DDTs discharged
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by several companies from the 1940’s-1970’s, with Montrose Chemical Corporation expelling
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over 2000 metric tons of DDTs17. Elevated contaminant levels persist around these islands18, 19
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and CASLs continue to exhibit high levels of DDTs, the majority of which is DDE7, 20.
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To investigate the potential risk of marine mammal feeding behavior to condor health we:
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(a) measured the stable carbon (δ13C) and nitrogen (δ15N) isotope ratios in condor whole blood
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samples and muscle from potential diet items to estimate the degree to which condors fed on
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marine mammals, (b) evaluated relationships between marine-associated contaminant (e.g.,
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PCBs, DDE) concentrations in condors and their observed feeding and spatial behavior, and (c)
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predicted current flock-wide DDE exposure levels and potential reproductive risks using
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simulation models. Our findings inform future management of condors by providing a
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comprehensive assessment of contaminant transfer from feeding on dead-stranded marine
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mammals while highlighting the broad influence of persistent pollutants in the marine
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environment including cross-ecosystem risks to terrestrial endangered species.
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Methods
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Study area and species
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All condors are assigned an ID (Studbook number) and are of known sex due to their
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intensive management as an endangered species. We studied free-flying condors associated with
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two flocks: southern California ("non-coastal"), managed by the USFWS Hopper Mountain
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National Wildlife Complex, and central California ("coastal"), managed by Ventana Wildlife
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Society and Pinnacles National Park. The latter moves between the Big Sur coast and inland
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regions, whereas the former remains inland. Personnel maintain set locations where terrestrial
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animal carcasses are placed ("proffered feeding stations") to facilitate monitoring. Coastal
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condors are observed feeding on dead-stranded marine mammals along Big Sur12, whereas
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southern, non-coastal condors are not considered to feed on marine mammals. Ranges of coastal
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condors during the study period (2009-2013) overlap with our dead-stranded marine mammal
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sampling locations and are distinct from non-coastal condor ranges (Supplemental Information;
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Figure S1).
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Sample collection
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Condor blood samples were collected opportunistically during routine health monitoring
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from 2009–2012 and condors sampled appeared to be in good body condition. All samples were
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used for stable isotope analysis and a subset of these were analyzed for contaminants (Table S1).
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Blubber samples (~5 grams) for contaminant analysis were collected from dead-stranded marine
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mammals in Monterey County, California from 2008–2012. Muscle samples for stable isotope
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analysis were collected from dead-stranded marine mammals and wild, non-proffered and
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domestic, proffered terrestrial carcasses in central and southern California from 2010–2012.
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Marine mammal blubber (n=17 organochlorines, n=7 PBDEs) and condor plasma samples (n=33
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organochlorines, n=13 PBDEs) were analyzed for contaminants, condor whole blood samples
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(n=68) were analyzed for total mercury, and diet item muscle (n=60) and condor whole blood
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samples (n=83) were analyzed for stable isotope ratios (Supplemental Information; Tables S1,
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S2, S3).
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Sample analysis (see also Supplemental Information).
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Plasma and blubber samples were analyzed for 54 congeners of PCBs, 26 chlorinated
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pesticides including the seven metabolites of DDT, and 27 congeners of PBDEs (Table S4) at the
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California Department of Fish and Wildlife Water Pollution Control Laboratory. Condor whole
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blood was analyzed for total mercury by Eurofins Frontier Global Sciences, Inc., Bothell,
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Washington on a Tekran 2600 Flow Injection Mercury System (FIMS). Condor whole blood and
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diet item muscle samples were analyzed for their δ13C and δ15N values using a Carlo Erba
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CE1108 elemental analyzer interfaced via a CONFLO III device to a Thermo-Electron Delta
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Plus XP mass spectrometer at the Stable Isotope Laboratory at the University of California Santa
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Cruz Department of Earth and Marine Sciences.
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Condor daily observational data for the coastal flock Condors were monitored on a near-daily basis via visual observation at proffered feeding
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stations or elsewhere, aided by detection of signals from radio (VHF) and/or GPS transmitters.
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Daily observational data consisted of 31,985 records of birds, documenting sightings in coastal
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Big Sur, inland in Pinnacles, and at proffered feeding stations. Observations were also made
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opportunistically of condors feeding on dead-stranded marine mammals in Big Sur from 1999–
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2013.
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Spatial analysis.
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We quantified space use with hourly GPS (PTT-100 50 g Solar Patagial Argos/GPS;
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Microwave Telemetry, Inc.) locations from 01/01/2003–7/31/2013, 0500–2000 PST, equaling
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867,498 locations from 90 unique condors. We summarized geographic ranges for coastal and
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non-coastal flocks using 99% fixed kernel density estimates from 2009–2013, concurrent with
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the time period of condor tissue sample collection (Figure S1), using ArcMET (Movement
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Ecology Tools for ArcGIS)21. To investigate fine-scale patterns of coastal foraging, we ran a
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separate 99% fixed kernel density estimate for all locations within 1.5 km of the coast for the full
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dataset (55,012 locations from 37 unique condors), binning results into equal-area quantiles.
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Statistical Analysis.
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Coastal vs. non-coastal condors. Statistical tests of contaminant and stable isotope data
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were performed in R (version 3.0.2, R Core Team, 2013). Stable carbon and nitrogen isotope
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turnover from blood in birds has been shown to be complete at ~30 days22-24, whereas
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methylmercury concentrations in avian blood decrease by ~90% within 30 days of exposure25.
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We considered blood samples from the same individual independent as all samples were
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collected at intervals greater than or equal to approximately one year and no condors had more
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than one sample taken for organochlorine or PBDE analysis (Table S1). Only quantifiable
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compounds were used for determining the sum chlorinated pesticides, sum PCBs, or sum
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PBDEs; if all compounds within a group (e.g., PCBs) were not quantifiable, half the detection
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limit of a single compound was used as follows: p,p'-DDE was used for sum chlorinated
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pesticides, PCB 153 for sum PCBs, and PBDE-47 for sum PBDEs (Supplemental Information).
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All samples had quantifiable total mercury concentrations. Variables were log-transformed if
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normality and homoscedasticity were improved, and non-parametric equivalents were utilized
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when data did not meet assumptions for parametric analyses.
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Diet of coastal condors. MixSIAR, a Bayesian stable isotope mixing model incorporating
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discrimination factors for condors on known diets26 and the mean (±SD) δ13C and δ15N values
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from condors, marine mammals, and terrestrial proffered and non-proffered mammals, was used
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to estimate proportions of condor diet composed of marine versus terrestrial proffered versus
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terrestrial non-proffered items. We found no differences in the δ13C (t=0.1.99, P=0.77) and δ15N
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(t=1.99, P=0.41) values between sexes, so combined sexes for analyses.
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Behavior affecting contaminant exposure. We assessed whether mercury, PCBs, PBDEs,
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and DDE levels were predicted by condor foraging behavior, focusing on DDE because it is the
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most abundant organochlorine in CASLs7 and associated with reproductive failure in avian
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species27. We considered the cumulative number of observations of condors feeding on marine
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carcasses, overall and in one and three year windows preceding sample collection. Detecting
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non-proffered feeding along a wide coastal area is inherently difficult, so to minimize the
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influence of missing data, we also considered the cumulative number of years an individual was
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a marine mammal feeder prior to and inclusive of sampling year, and counted an individual as a
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marine mammal feeder if it was observed feeding on marine mammals at least once in the year.
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Because gray whales have substantially lower DDE levels than CASLs (this study and7) and
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condors were observed feeding on individual gray whales for several months, we also considered
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observations of marine mammal feeding excluding gray whales. We fit contaminant data to these
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marine feeding observations using linear regression models (Supplemental Information),
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transforming response and predictor variables to improve normality and homoscedasticity and
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standardizing continuous predictor variables to facilitate model convergence. Model selection
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was guided by AICc.
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We used estimated relationships between observed marine mammal feeding and
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measured DDE to estimate DDE levels for all condors in the coastal flock based on observed
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marine mammal feeding behavior from 07/31/2001-07/31/2013, incorporating unexplained
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variance due to residual SE, and summarized results from 1000 replicate runs (Matlab version
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8.1) (Supplemental Information). To investigate the possibility that DDE is affecting
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reproduction, for each simulated run we tracked the proportion of the population that, using a
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plasma DDE to egg DDE conversion factor reported for other raptors28, exceeded two DDE
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thresholds approximately equal to egg concentrations of 5000 ng/g and 15000 ng/g wet weight.
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The lower DDE threshold is associated with 10% and 20% eggshell thinning in bald eagles28 and
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condors29, respectively, whereas bald eagles approached 100% reproductive failure at the upper
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DDE threshold28 (Supplemental Information).
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Results
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δ13C and δ15N and contaminant values
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We found no differences in the δ13C (t=0.1.99, P=0.77) and δ15N (t=1.99, P=0.41) values
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between sexes, so combined sexes for analyses. Coastal condors (n=65) had higher mean (±SD)
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δ13C (-22.1±1.2‰) and δ15N (9.9±1.2‰) values than non-coastal condors (n=18, -23.2±1.2‰
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and 8.0±0.8‰, respectively) and the mean δ13C and δ15N values from marine mammals (n=17, -
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17.3±0.8‰ and 17.1±1.0‰, respectively) were also higher than those from all terrestrial animals
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(n=46, -23.7±2.3‰ and 6.4±1.5‰, respectively) (Figure 1, Table S5), indicating the diet of
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coastal condors is partially marine-derived. The estimated coastal condor diets (means) for
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individual birds ranged from 8-52% marine mammals, 26-53% proffered, and 16-63% non-
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proffered terrestrial items (Table S6), whereas those of non-coastal condors were 28-40%
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proffered and 44-68% non-proffered terrestrial items.
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Coastal condors had 12 to 100-fold greater mean concentrations of mercury, chlorinated
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pesticides, PCBs, and PBDEs than non-coastal condors (all P90% of sum chlorinated pesticides with trans-nonachlor the second most
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abundant chlorinated pesticide detected (~1-4% of sum) (Table S9). PCB153 was a predominant
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PCB congener, accounting for 10-48% of sum PCBs, whereas PBDE-47 was the most abundant
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PBDE congener detected (Table S9). We found strong positive correlations between PBDEs,
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chlorinated pesticides, and PCBs within individual condors (r≥0.951, p
