Joseph Brandt

Lead poisoning and the deceptive recovery of the critically endangered California condor.

Endangered species recovery programs seek to restore populations to self-sustaining levels. Nonetheless, many recovering species require continuing management to compensate for persistent threats in their environment. Judging true recovery in the face of this management is often difficult, impeding thorough analysis of the success of conservation programs. We illustrate these challenges with a multidisciplinary study of one of the world’s rarest birds—the California condor (Gymnogyps californianus). California condors were brought to the brink of extinction, in part, because of lead poisoning, and lead poisoning remains a significant threat today. We evaluated individual lead-related health effects, the efficacy of current efforts to prevent lead-caused deaths, and the consequences of any reduction in currently intensive management actions. Our results show that condors in California remain chronically exposed to harmful levels of lead; 30% of the annual blood samples collected from condors indicate lead exposure (blood lead ≥ 200 ng/mL) that causes significant subclinical health effects, measured as >60% inhibition of the heme biosynthetic enzyme δ-aminolevulinic acid dehydratase. Furthermore, each year, ∼20% of free-flying birds have blood lead levels (≥450 ng/mL) that indicate the need for clinical intervention to avert morbidity and mortality. Lead isotopic analysis shows that lead-based ammunition is the principle source of lead poisoning in condors. Finally, population models based on condor demographic data show that the condor’s apparent recovery is solely because of intensive ongoing management, with the only hope of achieving true recovery dependent on the elimination or substantial reduction of lead poisoning rates.

Patterns of mortality in free-ranging California Condors (Gymnogyps californianus).

We document causes of death in free-ranging California Condors (Gymnogyps californianus) from the inception of the reintroduction program in 1992 through December 2009 to identify current and historic mortality factors that might interfere with establishment of self-sustaining populations in the wild. A total of 135 deaths occurred from October 1992 (the first post-release death) through December 2009, from a maximum population-at-risk of 352 birds, for a cumulative crude mortality rate of 38%. A definitive cause of death was determined for 76 of the 98 submitted cases, 70%(53/76) of which were attributed to anthropogenic causes. Trash ingestion was the most important mortality factor in nestlings (proportional mortality rate [PMR] 73%; 8/11), while lead toxicosis was the most important factor in juveniles (PMR 26%; 13/50) and adults (PMR 67%; 10/15). These results demonstrate that the leading causes of death at all California Condor release sites are anthropogenic. The mortality factors thought to be important in the decline of the historic California Condor population, particularly lead poisoning, remain the most important documented mortality factors today. Without effective mitigation, these factors can be expected to have the same effects on the sustainability of the wild populations as they have in the past.

Feather Lead Concentrations and 207Pb/206Pb Ratios Reveal Lead Exposure History of California Condors (Gymnogyps californianus)

Lead poisoning is a primary factor impeding the survival and recovery of the critically endangered California Condor (Gymnogyps californianus). However, the frequency and magnitude of lead exposure in condors is not well-known in part because most blood lead monitoring occurs biannually, and biannual blood samples capture only approximately 10% of a birds annual exposure history. We investigated the use of growing feathers from free-flying condors in California to establish a birds lead exposure history. We show that lead concentration and stable lead isotopic composition analyses of sequential feather sections and concurrently collected blood samples provided a comprehensive history of lead exposure over the 2-4 month period of feather growth. Feather analyses identified exposure events not evident from blood monitoring efforts, and by fitting an empirically derived timeline to actively growing feathers, we were able to estimate the time frame for specific lead exposure events. Our results demonstrate the utility of using sequentially sampled feathers to reconstruct lead exposure history. Since exposure risk in individuals is one determinant of population health, our findings should increase the understanding of population-level effects from lead poisoning in condors; this information may also be helpful for other avian species potentially impacted by lead poisoning.

Eggshell Thinning and Depressed Hatching Success of California Condors Reintroduced to Central California

Abstract. From 1997 through 2010, in collaboration with the National Park Service, we released 84 captivereared California Condors (Gymnogyps californianus) to the wild in central California; from 2006 through 2010 we recorded 16 nestings by nine pairs and recovered eggs or eggshell fragments from 12 nests. Mean thickness of shell fragments, without membrane, was 0.46 mm, 34% lower than the average thickness of 0.70 mm of fragments recovered from nine successful nests in interior southern California, 2007–2009. Hatching success in central California was 20–40%, significantly lower than the 70–80% recorded in southern California. The outer crystalline layer was absent or greatly reduced, as in thin-shelled condor eggs laid in southern California in the 1960s. Shell thickness was not related to egg size. Weight/water loss during incubation in the wild averaged three times greater than the normal rate associated with successful hatching; the rate of loss increased significantly with decreasing shell thickness. At least four failures, three from death of the embryo, we attribute to excessive weight/water loss; two other eggs losing substantial weight hatched successfully after artificial incubation at elevated humidities. DDT/DDE from wastes of a DDT factory discharged into the Southern California Bight had previously caused extensive eggshell thinning and reproductive failures of fish-eating and raptorial birds. Feeding on carcasses of California sea lions (Zalophus californianus), reintroduced condors now occupy a higher level of the food web. Like that of other species previously affected, the thickness of condor eggshells should recover as DDE contamination continues to decline.

Spatiotemporal patterns and risk factors for lead exposure in endangered California condors during 15 years of reintroduction.

Large-scale poisoning events are common to scavenging bird species that forage communally, many of which are in decline. To reduce the threat of poisoning and compensate for other persistent threats, management, including supplemental feeding, is ongoing for many reintroduced and endangered vulture populations. Through a longitudinal study of lead exposure in California condors (Gymnogyps californianus), we illustrate the conservation challenges inherent in reintroduction of an endangered species to the wild when pervasive threats have not been eliminated. We evaluated population-wide patterns in blood lead levels from 1997 to 2011 and assessed a broad range of putative demographic, behavioral, and environmental risk factors for elevated lead exposure among reintroduced California condors in California (United States). We also assessed the effectiveness of lead ammunition regulations within the condors range in California by comparing condor blood lead levels before and after implementation of the regulations. Lead exposure was a pervasive threat to California condors despite recent regulations limiting lead ammunition use. In addition, condor lead levels significantly increased as age and independence from intensive management increased, including increasing time spent away from managed release sites, and decreasing reliance on food provisions. Greater independence among an increasing number of reintroduced condors has therefore elevated the populations risk of lead exposure and limited the effectiveness of lead reduction efforts to date. Our findings highlight the challenges of restoring endangered vulture populations as they mature and become less reliant on management actions necessary to compensate for persistent threats.

An analysis of monthly home range size in the critically endangered California Condor Gymnogyps californianus

Summary Condors and vultures comprise the only group of terrestrial vertebrates in the world that are obligate scavengers, and these species move widely to locate ephemeral, unpredictable, and patchilydistributed food resources. In this study, we used high-resolution GPS location data to quantify monthly home range size of the critically endangered California Condor Gymnogyps californianus throughout the annual cycle in California. We assessed whether individual-level characteristics (age, sex and breeding status) and factors related to endangered species recovery program efforts (rearing method, release site) were linked to variation in monthly home range size. We found that monthly home range size varied across the annual cycle, with the largest monthly home ranges observed during late summer and early fall (July–October), a pattern that may be linked to seasonal changes in thermals that facilitate movement. Monthly home ranges of adults were significantly larger than those of immatures, but males and females used monthly home ranges of similar size throughout the year and breeding adults did not differ from non-breeding adults in their average monthly home range size. Individuals from each of three release sites differed significantly in the size of their monthly home ranges, and no differences in monthly home range size were detected between condors reared under captive conditions relative to those reared in the wild. Our study provides an important foundation for understanding the movement ecology of the California Condor and it highlights the importance of seasonal variation in space use for effective conservation planning for this critically endangered species.

Lead Exposure Risk from Trash Ingestion by the Endangered California Condor (Gymnogyps californianus).

Abstract Lead poisoning from ingestion of spent lead ammunition is one of the greatest threats to the recovery of California Condors (Gymnogyps californianus) in the wild. Trash ingestion by condors is well documented, yet the extent that trash presents a lead exposure risk is unknown. We evaluated 1,413 trash items collected from condor nest areas and nestlings in the Transverse Range of Ventura County, California, US, from 2002 to 2008, for their potential as a lead exposure risk to condors. We visually identified 71 items suspected to contain sufficient lead to be of toxicologic concern. These items were leached with weak acid and analyzed for lead. Twenty-seven of the 71 leached items (~2% of the 1,413 items) were “lead containing” based on criteria of a leachate lead concentration >1 μg/mL, with the majority of these items (22; 81% of the 27 lead items) being ammunition related (e.g., spent bullet casings and jacketed bullets). Only three of the 1,413 items collected were lead containing but were clearly not ammunition related; the other two lead-containing items were unidentified. Our results suggest that trash ingestion of nonammunition items does not pose a significant lead exposure risk to the California Condor population in California.

Flight response to spatial and temporal correlates informs risk from wind turbines to the California Condor

ABSTRACT Wind power is a fast-growing energy resource, but wind turbines can kill volant wildlife, and the flight behavior of obligate soaring birds can place them at risk of collision with these structures. We analyzed altitudinal data from GPS telemetry of critically endangered California Condors (Gymnogyps californianus) to assess the circumstances under which their flight behavior may place them at risk from collision with wind turbines. Condor flight behavior was strongly influenced by topography and land cover, and birds flew at lower altitudes and closer to the rotor-swept zone of wind turbines when over ridgelines and steep slopes and over forested and grassland cover types. Condor flight behavior was temporally predictable, and birds flew lower and closer to the rotor-swept zone during early morning and evening hours and during the winter months, when thermal updrafts were weakest. Although condors only occasionally flew at altitudes that placed them in the rotor-swept zone of turbines, they regularly flew near or within wind resource areas preferred by energy developers. Practitioners aiming to mitigate collision risk to this and other soaring bird species of conservation concern can consider the manner in which flight behavior varies temporally and in response to areas of high topographic relief and proximity to nocturnal roosting sites. By contrast, collision risk to large soaring birds from turbines should be relatively lower over flatter and less rugged areas and in habitat used during daytime soaring.

Reply to Comment on "Terrestrial Scavenging of Marine Mammals: Cross-Ecosystem Contaminant Transfer and Potential Risks to Endangered California Condors (Gymnogyps californianus)"

Author(s): Finkelstein, Myra E; Bakker, Victoria J; Copeland, Holly; Burnett, Joe; Jones Scherbinski, Jennie; Brandt, Joseph; Kurle, Carolyn M