Myra E. Finkelstein

Severity of the Effects of Invasive Rats on Seabirds : A Global Review

Invasive rats are some of the largest contributors to seabird extinction and endangerment worldwide. We conducted a meta-analysis of studies on seabird-rat interactions to examine which seabird phylogenetic, morphological, behavioral, and life history characteristics affect their susceptibility to invasive rats and to identify which rat species have had the largest impact on seabird mortality. We examined 94 manuscripts that demonstrated rat effects on seabirds. All studies combined resulted in 115 independent rat-seabird interactions on 61 islands or island chains with 75 species of seabirds in 10 families affected. Seabirds in the family Hydrobatidae and other small, burrow-nesting seabirds were most affected by invasive rats. Laridae and other large, ground-nesting seabirds were the least vulnerable to rats. Of the 3 species of invasive rats, Rattus rattus had the largest mean impact on seabirds followed by R. norvegicus and R. exulans; nevertheless, these differences were not statistically significant. Our findings should help managers and conservation practitioners prioritize selection of islands for rat eradication based on seabird life history traits, develop testable hypotheses for seabird response to rat eradication, provide justification for rat eradication campaigns, and identify suitable levels of response and prevention measures to rat invasion. Assessment of the effects of rats on seabirds can be improved by data derived from additional experimental studies, with emphasis on understudied seabird families such as Sulidae, Phalacrocoracidae, Spheniscidae, Fregatidae, Pelecanoididae, Phaethontidae, and Diomedeidae and evaluation of rat impacts in tropical regions.

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.

Albatross species demonstrate regional differences in North Pacific marine contamination

Recent concern about negative effects on human health from elevated organochlorine and mercury concentrations in marine foods has highlighted the need to understand temporal and spatial patterns of marine pollution. Seabirds, long-lived pelagic predators with wide foraging ranges, can be used as indicators of regional contaminant patterns across large temporal and spatial scales. Here we evaluate contaminant levels, carbon and nitrogen stable isotope ratios, and satellite telemetry data from two sympatrically breeding North Pacific albatross species to demonstrate that (1) organochlorine and mercury contaminant levels are significantly higher in the California Current compared to levels in the high-latitude North Pacific and (2) levels of organochlorine contaminants in the North Pacific are increasing over time. Black-footed Albatrosses (Phoebastria nigripes) had 370-460% higher organochlorine (polychlorinated biphenyls [PCBs], dichlorodiphenyltrichloroethanes [DDTs]) and mercury body burdens than a closely related species, the Laysan Albatross (P. immutabilis), primarily due to regional segregation of their North Pacific foraging areas. PCBs (the sum of the individual PCB congeners analyzed) and DDE concentrations in both albatross species were 130-360% higher than concentrations measured a decade ago. Our results demonstrate dramatically high and increasing contaminant concentrations in the eastern North Pacific Ocean, a finding relevant to other marine predators, including humans.

Evaluating the Potential Effectiveness of Compensatory Mitigation Strategies for Marine Bycatch

Conservationists are continually seeking new strategies to reverse population declines and safeguard against species extinctions. Here we evaluate the potential efficacy of a recently proposed approach to offset a major anthropogenic threat to many marine vertebrates: incidental bycatch in commercial fisheries operations. This new approach, compensatory mitigation for marine bycatch (CMMB), is conceived as a way to replace or reduce mandated restrictions on fishing activities with compensatory activities (e.g., removal of introduced predators from islands) funded by levies placed on fishers. While efforts are underway to bring CMMB into policy discussions, to date there has not been a detailed evaluation of CMMBs potential as a conservation tool, and in particular, a list of necessary and sufficient criteria that CMMB must meet to be an effective conservation strategy. Here we present a list of criteria to assess CMMB that are tied to critical ecological aspects of the species targeted for conservation, the range of possible mitigation activities, and the multi-species impact of fisheries bycatch. We conclude that, overall, CMMB has little potential for benefit and a substantial potential for harm if implemented to solve most fisheries bycatch problems. In particular, CMMB is likely to be effective only when applied to short-lived and highly-fecund species (not the characteristics of most bycatch-impacted species) and to fisheries that take few non-target species, and especially few non-seabird species (not the characteristics of most fisheries). Thus, CMMB appears to have limited application and should only be implemented after rigorous appraisal on a case-specific basis; otherwise it has the potential to accelerate declines of marine species currently threatened by fisheries bycatch.

Contaminant‐associated alteration of immune function in black‐footed albatross (Phoebastria nigripes), a North Pacific predator

Environmental pollution is ubiquitous and can pose a significant threat to wild populations through declines in fitness and population numbers. To elucidate the impact of marine pollution on a pelagic species, we assessed whether toxic contaminants accumulated in black-footed albatross (Phoebastria nigripes), a wide-ranging North Pacific predator, are correlated with altered physiological function. Blood samples from adult black-footed albatrosses on Midway Atoll, part of the Hawaiian (USA) archipelago, were analyzed for organochlorines (e.g., polychlorinated biphenyls [PCBs] and chlorinated pesticides), trace metals (silver, cadmium, tin, lead, chromium, nickel, copper, zinc, arsenic, selenium, and total mercury), and a sensitive physiological marker, peripheral white blood cell immune function (mitogen-induced lymphocyte proliferation and macrophage phagocytosis). We found a positive significant relationship between organochlorines, which were highly correlated within individual birds (p < 0.001, r > 0.80, Spearman correlation for all comparisons; PCBs, 160 +/- 60 ng/ml plasma [mean +/- standard deviation]; DDTs, 140 +/- 180 ng/ml plasma; chlordanes, 7.0 +/- 3.6 ng/ml plasma; hexachlorobenzene, 2.4 +/- 1.5 ng/ml plasma; n = 15) and increased lymphocyte proliferation (p = 0.020) as well as percentage lymphocytes (p = 0.033). Mercury was elevated in black-footed albatrosses (4,500 +/- 870 ng/ml whole blood, n = 15), and high mercury levels appeared to be associated (p = 0.017) with impaired macrophage phagocytosis. The associations we documented between multiple contaminant concentrations and immune function in endangered black-footed albatrosses provide some of the first evidence that albatrosses in the North Pacific may be affected by environmental contamination. Our results raise concern regarding detrimental health effects in pelagic predators exposed to persistent marine pollutants.

Health Risks from Lead-Based Ammunition in the Environment

Lead is one of the most studied toxicants, and overwhelming scientific evidence demonstrates that lead is toxic to several physiological systems in vertebrates, including the nervous, renal, cardiovascular, reproductive, immune, and hematologic systems (Health Risks from Lead-Based Ammunition in the Environment—A Consensus Statement of Scientists 2013). Furthermore, there is no level of lead exposure in children known to be without adverse effects [Centers for Disease Control and Prevention (CDC) 2012a, 2012b]. In light of this evidence, there is an urgent need to end a major source of lead for animals and humans: spent lead bullets and shotgun pellets. Notably, production of lead-based ammunition in the United States accounted for > 69,000 metric tons consumed in 2012; this is second only to the amount of lead used to manufacture storage batteries (U.S. Geological Survey 2013). However, there are few regulations regarding the release of lead into the environment through discharge of lead-based ammunition. For other major categories of lead consumption, such as lead batteries and sheet lead/lead pipes, environmental discharge and disposal are regulated. Therefore, lead-based ammunition is likely the greatest largely unregulated source of lead that is knowingly discharged into the environment in the United States. In contrast, the release or distribution of other major sources of environmental lead contamination (e.g., leaded gasoline, lead-based paint, lead solder) have been substantially regulated and reduced since the mid-1970s (Health Risks from Lead-Based Ammunition in the Environment—A Consensus Statement of Scientists 2013). There is a national discussion—polarized at times—of the health risks posed to humans and wildlife from the discharge of lead-based ammunition. To inform this discussion, a group of 30 nationally and internationally recognized scientists with expertise regarding lead and environmental health recently collaborated to create an evidence-based consensus statement (Health Risks from Lead-Based Ammunition in the Environment—A Consensus Statement of Scientists 2013) supporting the reduction and eventual elimination of lead released to the environment through the discharge of lead-based ammunition. The discharge of lead bullets and shotgun pellets into the environment poses significant health risks to humans and wildlife. The best available scientific evidence demonstrates that the discharge of lead-based ammunition substantially increases environmental lead levels, especially in areas with higher shooting activity (U.S. Environmetal Protection Agency 2012) and that the discharge of lead-based ammunition poses risks of elevated lead exposure to gun users (National Research Council 2012). When lead-containing bullets are used to shoot wildlife, they can fragment into hundreds of small pieces, many of which are small enough to be easily ingested by scavenging animals or to be retained in meat prepared for human consumption (Hunt et al. 2009; Knott et al. 2010; Pauli and Burkirk 2007). Consequently, lead-based ammunition may be a significant source of lead exposure in humans that regularly ingest wild game (Hanning et al. 2003; Johansen et al. 2006; Levesque et al. 2003; Tsuji et al. 2008). In addition, lead pellets and fragments have been reported in gastrointestinal tracts of hunters who consume meat from animals shot with lead-based ammunition (Carey 1977; Reddy 1985). The use of lead pellets in shotgun shells for hunting waterfowl posed a serious threat to wetland birds, and secondarily to bald eagles, in the United States, leading to the U.S. Fish and Wildlife Service’s 1991 nationwide regulations requiring use of nontoxic shotgun pellets for hunting waterfowl (Anderson 1992). However, lead poisoning from ingestion of spent lead-based ammunition fragments continues to pose a particularly serious health threat for scavenging species. These lead-containing fragments remain the principal source of lead exposure to endangered California condors and continue to prevent the successful recovery of these birds in the wild (Church et al. 2006; Finkelstein et al. 2012; Green et al. 2008; Parish et al. 2009; Rideout et al. 2012; Woods et al. 2007). Other wildlife species, such as golden eagles, bald eagles, ravens, turkey vultures, and pumas, are also exposed to the fragments of spent lead ammunition (Burco et al. 2012; Clark and Scheuhammer 2003; Craighead and Bedrosian 2008; Cruz-Martinez et al. 2012; Fisher et al. 2006; Kelly and Johnson 2011; Stauber et al. 2010; Wayland and Bollinger 1999). No rational deliberation about the use of lead-based ammunition can ignore the overwhelming evidence for the toxic effects of lead, or that the discharge of lead bullets and shot into the environment poses significant risks of lead exposure to humans and wildlife. Given the availability of non-lead ammunition for shooting and hunting (Thomas 2013), the use of lead-based ammunition that introduces lead into the environment can be reduced and eventually eliminated. This seems to be a reasonable and equitable action to protect the health of humans and wildlife.

Linking cases of illegal shootings of the endangered California condor using stable lead isotope analysis

Lead poisoning is preventing the recovery of the critically endangered California condor (Gymnogyps californianus) and lead isotope analyses have demonstrated that ingestion of spent lead ammunition is the principal source of lead poisoning in condors. Over an 8 month period in 2009, three lead-poisoned condors were independently presented with birdshot embedded in their tissues, evidencing they had been shot. No information connecting these illegal shooting events existed and the timing of the shooting(s) was unknown. Using lead concentration and stable lead isotope analyses of feathers, blood, and recovered birdshot, we observed that: i) lead isotope ratios of embedded shot from all three birds were measurably indistinguishable from each other, suggesting a common source; ii) lead exposure histories re-constructed from feather analysis suggested that the shooting(s) occurred within the same timeframe; and iii) two of the three condors were lead poisoned from a lead source isotopically indistinguishable from the embedded birdshot, implicating ingestion of this type of birdshot as the source of poisoning. One of the condors was subsequently lead poisoned the following year from ingestion of a lead buckshot (blood lead 556 µg/dL), illustrating that ingested shot possess a substantially greater lead poisoning risk compared to embedded shot retained in tissue (blood lead ~20 µg/dL). To our knowledge, this is the first study to use lead isotopes as a tool to retrospectively link wildlife shooting events.

The potential for biodiversity offsetting to fund invasive species eradications on islands

N.D. Holmes,∗ ¶ G.R. Howald,∗ A.S. Wegmann,∗ C.J. Donlan,†‡ M. Finkelstein,§ and B. Keitt∗ ∗Island Conservation, 2161 Delaware Ave Suite A, Santa Cruz, CA 95060, U.S.A. †Advanced Conservation Strategies, Via Agusta 12, Cordoba 14011, Spain ‡Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 15853, U.S.A. §University of California at Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, U.S.A.

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.