Biological Conservation 238 (2019) 108238 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Anticoagulant rodenticides in Strix owls indicate widespread exposure in west coast forests T ⁎ J. David Wiensa, , Krista E. Dilionea, Collin A. Eagles-Smitha, Garth Herringa, Damon B. Lesmeisterb,e, Mourad W. Gabrielc,d, Greta M. Wengertc, David C. Simona a U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Corvallis, OR, USA b USDA Forest Service, Pacific Northwest Research Station, Corvallis, OR, USA c Integral Ecology Research Center, Blue Lake, CA, USA d University of California Davis Karen C. Drayer Wildlife Health Center-One Health Institute, Davis, CA, USA e Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR, USA ARTICLE INFO ABSTRACT Keywords: Exposure of nontarget wildlife to anticoagulant rodenticides (AR) is a global conservation concern typically Anticoagulant rodenticide centered around urban or agricultural areas. Recently, however, the illegal use of ARs in remote forests of Barred owl California, USA, has exposed sensitive predators, including the federally threatened northern spotted owl (Strix Brodifacoum occidentalis caurina). We used congeneric barred owls (S. varia) as a sentinel species to investigate whether ARs Northern spotted owl pose a threat to spotted owls and other old-forest wildlife in northern regions of the Pacific Northwest. We Strix varia analyzed the liver tissue from 40 barred owls collected in Oregon and Washington and confirmed exposure to Strix occidentalis caurina ≥1 AR compounds in 48% of the owls examined. Brodifacoum, an extremely toxic second-generation AR, was the most common compound detected (89% of positive cases), followed by bromadiolone (11%), difethialone (11%), and warfarin (5%). Brodifacoum was also detected in one barred owl and one spotted owl opportunis- tically found dead (liver concentrations were 0.091 and 0.049 μg/g, respectively). We found no evidence that exposure varied with proximity to developed and agricultural areas, or among different study areas, age-classes, and sexes. Rather, exposure was ubiquitous, and the rates we observed in our study (38–64%) were similar to or greater than that reported previously for barred owls in California (40%). Together these studies indicate widespread contamination in forested landscapes used by spotted owls and other wildlife of conservation con- cern. Owls collected in older forests may have been exposed via illegal use of ARs, highlighting a mounting challenge for land managers and policy makers. 1. Introduction forest predators like fisher (Pekania pennanti), and the federally threa- tened northern spotted owl (Strix occidentalis caurina; Thompson et al., Secondary poisoning of nontarget wildlife by anticoagulant ro- 2014; Gabriel et al., 2012, 2018; Franklin et al., 2018). Unregulated denticides (ARs) is a global conservation concern. Food production, applications at marijuana cultivation sites have emerged as a primary storage, and transport facilities throughout the world are often ringed source of ARs in forested landscapes of northern California (Gabriel by bait stations containing ARs to prevent damage to products and et al., 2012, 2018), but information on AR exposure in northern spotted structures caused by rodents (Elliot et al., 2016, van den Brink et al. owls and other sensitive wildlife outside of California is lacking. 2018). Indeed, most accounts of AR exposure in wildlife occur in or Northern spotted owls are an old-forest species of significant con- adjacent to agricultural, urban, or suburban settings where use of ro- servation concern. Despite nearly 30 years of protection under the denticides is widespread (Erickson and Urban, 2004; Riley et al., 2007, Federal Endangered Species Act, populations have continued to decline López-Perea and Mateo, 2018). Recently, however, exposure within because of loss of old-forest habitat and, more recently, competition remote forest settings has been documented in northern California, with expanding populations of barred owls (S. varia; Wiens et al., 2014; USA, where the use of ARs associated with the illegal cultivation of Dugger et al., 2016; Lesmeister et al., 2018). Northern spotted owls are marijuana (Cannabis spp.) has contaminated food webs of sensitive potentially at substantial risk to AR exposure as another conservation ⁎ Corresponding author. E-mail address: [email protected] (J.D. Wiens). https://doi.org/10.1016/j.biocon.2019.108238 Received 21 May 2019; Received in revised form 28 August 2019; Accepted 31 August 2019 0006-3207/ Published by Elsevier Ltd. J.D. Wiens, et al. Biological Conservation 238 (2019) 108238 threat because their diet consists largely of small rodents and mammals, Intelligence Center, 2007) and more recent reports (Klassen and and they are most common in remote forests where illegal cultivation of Anthony, 2019) indicated widespread occurrence on public lands in marijuana often occurs (Gabriel et al., 2012, 2018; Franklin et al., each of our study regions. 2018). As a wide-ranging, federally protected species with dwindling numbers, however, it is challenging to directly measure the level of 2.2. Barred owl removal experiment and specimen collection threat ARs may pose. Studies in California have begun to address this issue by using ecologically similar barred owls as a surrogate species for Barred owls were removed from habitats and territories historically inferring exposure in sympatric spotted owls (Gabriel et al., 2018), as used by spotted owls as part of a broad-scale experiment to determine if these two species compete for space, habitat, and small mammal prey reducing populations of invasive barred owls can improve population (Wiens et al., 2014). trends of threatened spotted owls (Diller et al., 2016; Wiens et al., The rapid expansion of barred owls into the Pacific Northwest has 2019). Barred owls identified during population surveys were removed motivated conservationists, researchers, and land managers to develop using 12-gauge shotguns loaded with non-toxic shot (Diller et al., 2014; broad-scale approaches to mitigate the negative effects of competition Wiens et al., 2019). Removals occurred primarily in the non-breeding with barred owls on spotted owls (Long and Wolfe, 2019). As part of season (Sep–Apr) to avoid collecting owls with dependent young. Lethal this effort, removal experiments were initiated to determine if reducing removal and scientific collection of barred owls was approved by the numbers of barred owls can benefit declining populations of spotted Institutional Animal Care and Use Committee at Oregon State Uni- owls (Diller et al., 2014, 2016; Wiens et al., 2018, 2019). Barred owl versity (Protocols 4728, 5067), and completed under Federal Fish and removal experiments have been replicated in a variety of forest con- Wildlife Permit MB14305B-0 and Washington (HENSON 18-261) and ditions occupied by spotted owls in the Pacific Northwest, which offers Oregon (MB14305B-5) State Scientific Collection Permits. an opportunity to extend the initial work of Gabriel et al. (2018) to We recorded the coordinates of the collection location, sex, and age broader portions of the northern spotted owl's geographic range. This is of all individual barred owls. We determined sex of barred owls based relevant because clandestine marijuana operations also occur in on vocalizations and morphometric measurements and verified those forested landscapes of Oregon and Washington (Klassen and Anthony, determinations in the lab through examination of sex organs. We 2019) and the illegal use of ARs at these sites may represent a wide- classified all barred owls as either adults (≥3 years old) or subadults spread, albeit little studied, conservation concern to old-forest wildlife. (1–2 years old) based on the presence of distinctive juvenile (first-year) We investigated AR exposure in barred owls collected during re- flight feathers and molt characteristics observed under ultraviolet light moval experiments in Oregon and Washington during 2015–2017. Our (Weidensaul et al., 2011 ; Wiens et al., 2018, 2019). In addition, we objectives were to examine the prevalence of exposures relative to those used site-specific detection histories from survey and removal activities recently reported for northern California by Gabriel et al. (2018), and to to classify individual owls as either territorial residents (previously determine whether exposure was occurring across a larger portion of established owls collected at the beginning of the removal study) or spotted owl's geographic range. We also investigated: 1) the extent of new colonizers (owls collected at sites after the original occupants had AR exposure within and among different study regions, and 2) possible been removed). Territorial residents were well-established owls (pri- intrinsic and extrinsic sources of variation in exposure (e.g., proximity marily adults) with home ranges averaging 450–700 ha in size (Wiens to forest-urban interface, sex, age class, and territorial status of in- et al., 2014), whereas newly established colonizers (primarily sub- dividuals). Our test sample included barred owls removed from adults) were likely to have wide-ranging movements prior to collection, breeding territories simultaneously co-occupied by spotted owls, which and thus may have a greater risk of exposure to ARs as they dispersed provided an indicator of the threat of exposure to spotted owls re- across urban