A. Keith Miles

Effects of urbanization on carnivore species distribution and richness

Abstract Urban development can have multiple effects on mammalian carnivore communities. We conducted a meta-analysis of 7,929 photographs from 217 localities in 11 camera-trap studies across coastal southern California to describe habitat use and determine the effects of urban proximity (distance to urban edge) and intensity (percentage of area urbanized) on carnivore occurrence and species richness in natural habitats close to the urban boundary. Coyotes (Canis latrans) and bobcats (Lynx rufus) were distributed widely across the region. Domestic dogs (Canis lupus familiaris), striped skunks (Mephitis mephitis), raccoons (Procyon lotor), gray foxes (Urocyon cinereoargenteus), mountain lions (Puma concolor), and Virginia opossums (Didelphis virginiana) were detected less frequently, and long-tailed weasels (Mustela frenata), American badgers (Taxidea taxus), western spotted skunks (Spilogale gracilis), and domestic cats (Felis catus) were detected rarely. Habitat use generally reflected availability for most species. Coyote and raccoon occurrence increased with both proximity to and intensity of urbanization, whereas bobcat, gray fox, and mountain lion occurrence decreased with urban proximity and intensity. Domestic dogs and Virginia opossums exhibited positive and weak negative relationships, respectively, with urban intensity but were unaffected by urban proximity. Striped skunk occurrence increased with urban proximity but decreased with urban intensity. Native species richness was negatively associated with urban intensity but not urban proximity, probably because of the stronger negative response of individual species to urban intensity.

Mercury correlations among six tissues for four waterbird species breeding in San Francisco Bay, California, USA†

Despite a large body of research concerning mercury (Hg) in birds, no single tissue has been used consistently to assess Hg exposure, and this has hampered comparisons across studies. We evaluated the relationships of Hg concentrations among tissues in four species of waterbirds (American avocets [Recurvirostra americana], black-necked stilts [Himantopus mexicanus], Caspian terns [Hydroprogne caspia; formerly Sterna caspia], and Forsters terns [Sterna forsteri]) and across three life stages (prebreeding adults, breeding adults, and chicks) in San Francisco Bay, California, USA. Across species and life stages, Hg concentrations (least square mean +/- standard error) were highest in head feathers (6.45 +/- 0.31 microg/g dry wt) and breast feathers (5.76 +/- 0.28 microg/g dry wt), followed by kidney (4.54 +/- 0.22 microg/g dry wt), liver (4.43 +/- 0.21 microg/g dry wt), blood (3.10 +/- 0.15 microg/g dry wt), and muscle (1.67 +/- 0.08 microg/g dry wt). Relative Hg distribution among tissues, however, differed by species and life stage. Mercury concentrations were highly correlated among internal tissues (r2 > or = 0.89). Conversely, the relationships between Hg in feathers and internal tissues were substantially weaker (r2 < or = 0.42). Regression slopes sometimes differed among species and life stages, indicating that care must be used when predicting Hg concentrations in one tissue based on those in another. However, we found good agreement between predictions made using a general tissue-prediction equation and more specific equations developed for each species and life stage. Finally, our results suggest that blood is an excellent, nonlethal predictor of Hg concentrations in internal tissues but that feathers are relatively poor indicators of Hg concentrations in internal tissues.

BALD EAGLES AND SEA OTTERS IN THE ALEUTIAN ARCHIPELAGO: INDIRECT EFFECTS OF TROPHIC CASCADES

Because sea otters (Enhydra lutris) exert a wide array of direct and indirect effects on coastal marine ecosystems throughout their geographic range, we investigated the potential influence of sea otters on the ecology of Bald Eagles (Haliaeetus leucocephalus) in the Aleutian Islands, Alaska, USA. We studied the diets, productivity, and density of breeding Bald Eagles on four islands during 1993-1994 and 2000-2002, when sea otters were abundant and scarce, respectively. Bald Eagles depend on nearshore marine communities for most of their prey in this ecosystem, so we predicted that the recent decline in otter populations would have an indirect negative effect on diets and demography of Bald Eagles. Contrary to our predictions, we found no effects on density of breeding pairs on four islands from 1993-1994 to 2000-2002. In contrast, diets and diet diversity of Bald Eagles changed considerably between the two time periods, likely reflecting a change in prey availability resulting from the increase and subsequent decline in sea otter populations. The frequency of sea otter pups, rock greenling (Hexagammus lagocephalus), and smooth lumpsuckers (Aptocyclus ventricosus) in the eagles diet declined with corresponding increases in Rock Ptarmigan (Lagopus mutus), Glaucous-winged Gulls (Larus glaucescens), Atka mackerel (Pleurogrammus monopterygius), and various species of seabirds during the period of the recent otter population decline. Breeding success and productivity of Bald Eagles also increased during this time period, which may be due to the higher nutritional quality of avian prey consumed in later years. Our results provide further evidence of the wide-ranging indirect effects of sea otter predation on nearshore marine communities and another apex predator, the Bald Eagle. Although the indirect effects of sea otters are widely known, this example is unique because the food-web pathway transcended five species and several trophic levels in linking one apex predator to another.

Cytochrome P4501A biomarker indication of oil exposure in harlequin ducks up to 20 years after the Exxon Valdez oil spill.

Hydrocarbon-inducible cytochrome P4501A (CYP1A) expression was measured, as ethoxyresorufin-O-deethylase (EROD) activity, in livers of wintering harlequin ducks (Histrionicus histrionicus) captured in areas of Prince William Sound, Alaska, USA, oiled by the 1989 Exxon Valdez spill and in birds from nearby unoiled areas, during 2005 to 2009 (up to 20 years following the spill). The present work repeated studies conducted in 1998 that demonstrated that in harlequin ducks using areas that received Exxon Valdez oil, EROD activity was elevated nearly a decade after the spill. The present findings strongly supported the conclusion that average levels of hepatic EROD activity were higher in ducks from oiled areas than those from unoiled areas during 2005 to 2009. This result was consistent across four sampling periods; furthermore, results generated from two independent laboratories using paired liver samples from one of the sampling periods were similar. The EROD activity did not vary in relation to age, sex, or body mass of individuals, nor did it vary strongly by season in birds collected early and late in the winter of 2006 to 2007, indicating that these factors did not confound inferences about observed differences between oiled and unoiled areas. We interpret these results to indicate that harlequin ducks continued to be exposed to residual Exxon Valdez oil up to 20 years after the original spill. This adds to a growing body of literature suggesting that oil spills have the potential to affect wildlife for much longer time frames than previously assumed.

Gene transcription in sea otters (Enhydra lutris); development of a diagnostic tool for sea otter and ecosystem health

Gene transcription analysis for diagnosing or monitoring wildlife health requires the ability to distinguish pathophysiological change from natural variation. Herein, we describe methodology for the development of quantitative real‐time polymerase chain reaction (qPCR) assays to measure differential transcript levels of multiple immune function genes in the sea otter (Enhydra lutris); sea otter‐specific qPCR primer sequences for the genes of interest are defined. We establish a ‘reference’ range of transcripts for each gene in a group of clinically healthy captive and free‐ranging sea otters. The 10 genes of interest represent multiple physiological systems that play a role in immuno‐modulation, inflammation, cell protection, tumour suppression, cellular stress response, xenobiotic metabolizing enzymes, antioxidant enzymes and cell–cell adhesion. The cycle threshold (CT) measures for most genes were normally distributed; the complement cytolysis inhibitor was the exception. The relative enumeration of multiple gene transcripts in simple peripheral blood samples expands the diagnostic capability currently available to assess the health of sea otters in situ and provides a better understanding of the state of their environment.

Differential Gene Expression Induced by Exposure of Captive Mink to Fuel Oil: A Model for the Sea Otter

Free-ranging sea otters are subject to hydrocarbon exposure from a variety of sources, both natural and anthropogenic. Effects of direct exposure to unrefined crude oil, such as that associated with the Exxon Valdez oil spill, are readily apparent. However, the impact of subtle but pathophysiologically relevant concentrations of crude oil on sea otters is difficult to assess. The present study was directed at developing a model for assessing the impact of low concentrations of fuel oil on sea otters. Quantitative PCR was used to identify differential gene expression in American mink that were exposed to low concentrations of bunker C fuel oil. A total of 23 genes, representing 10 different physiological systems, were analyzed for perturbation. Six genes with immunological relevance were differentially expressed in oil-fed mink. Interleukin-18 (IL-18), IL-10, inducible nitric oxide synthase (iNOS), cyclooxygenase 2 (COX-2), and complement cytolysis inhibitor (CLI) were down-regulated while IL-2 was up-regulated. Expression of two additional genes was affected; heat shock protein 70 (HSP70) was up-regulated and thyroid hormone receptor (THR) was down-regulated. While the significance of each perturbation is not immediately evident, we identified differential expression of genes that would be consistent with the presence of immune system-modifying and endocrine-disrupting compounds in fuel oil. Application of this approach to identify effects of petroleum contamination on sea otters should be possible following expansion of this mink model to identify a greater number of affected genes in peripheral blood leukocytes.

Invertebrate mercury bioaccumulation in permanent, seasonal, and flooded rice wetlands within California's Central Valley

We examined methylmercury (MeHg) bioavailability in four of the most predominant wetland habitats in Californias Central Valley agricultural region during the spring and summer: white rice, wild rice, permanent wetlands, and shallowly-flooded fallow fields. We sampled MeHg and total mercury (THg) concentrations in two aquatic macroinvertebrate taxa at the inlets, centers, and outlets of four replicated wetland habitats (8 wetlands total) during two time periods bounding the rice growing season and corresponding to flood-up and pre-harvest (96 total samples). In general, THg concentrations (mean+/-standard error) in Notonectidae (Notonecta, back swimmers; 1.18+/-0.08 microg g(-1) dry weight [dw]) were higher than in Corixidae (Corisella, water boatmen; 0.89+/-0.06 microg g(-)(1)dw, MeHg: 0.74+/-0.05 microg g(-)(1)dw). MeHg concentrations were correlated with THg concentrations in Corixidae (R(2)=0.80) and 88% of THg was in the MeHg form. Wetland habitat type had an important influence on THg concentrations in aquatic invertebrates, but this effect depended on the sampling time period and taxa. In particular, THg concentrations in Notonectidae, but not Corixidae, were higher in permanent wetlands than in white rice, wild rice, or shallowly-flooded fallow fields. THg concentrations in Notonectidae were higher at the end of the rice growing season than near the time of flood-up, whereas THg concentrations in Corixidae did not differ between time periods. The effect of wetland habitat type was more prevalent near the end of the rice growing season, when Notonectidae THg concentrations were highest in permanent wetlands. Additionally, invertebrate THg concentrations were higher at water outlets than at inlets of wetlands. Our results indicate that although invertebrate THg concentrations increased from the time of flood-up to draw-down of wetlands, temporarily flooded habitats such as white rice, wild rice, and shallowly-flooded fallow fields did not have higher THg or MeHg concentrations in invertebrates than permanent wetlands.

Polycyclic aromatic hydrocarbon exposure in Steller's eiders (Polysticta stelleri) and harlequin ducks (Histronicus histronicus) in the Eastern Aleutian Islands, Alaska, USA

Seaducks may be affected by harmful levels of polycyclic aromatic hydrocarbons (PAHs) at seaports near the Arctic. As an indicator of exposure to PAHs, we measured hepatic enzyme 7-ethoxyresorufin-O-deethylase activity (EROD) to determine cytochrome P4501A induction in Stellers eiders (Polysticta stelleri) and Harlequin ducks (Histronicus histronicus) from Unalaska, Popof, and Unga Islands (AK, USA) in 2002 and 2003. We measured PAHs and organic contaminants in seaduck prey samples and polychlorinated biphenyl congeners in seaduck blood plasma to determine any relationship to EROD. Using Akaikes information criterion, species and site differences best explained EROD patterns: Activity was higher in Harlequin ducks than in Stellers eiders and higher at industrial than at nonindustrial sites. Site-specific concentrations of PAHs in blue mussels ([Mytilus trossilus] seaduck prey; PAH concentrations higher at Dutch Harbor, Unalaska, than at other sites) also was important in defining EROD patterns. Organochlorine compounds rarely were detected in prey samples. No relationship was found between polychlorinated biphenyl congeners in avian blood and EROD, which further supported inferences derived from Akaikes information criterion. Congeners were highest in seaducks from a nonindustrial or reference site, contrary to PAH patterns. To assist in interpreting the field study, 15 captive Stellers eiders were dosed with a PAH known to induce cytochrome P4501A. Dosed, captive Stellers eiders had definitive induction, but results indicated that wild Stellers eiders were exposed to PAHs or other inducing compounds at levels greater than those used in laboratory studies. Concentrations of PAHs in blue mussels at or near Dutch Harbor (approximately 1,180-5,980 ng/g) approached those found at highly contaminated sites (approximately 4,100-7,500 ng/g).

Predator Removal and Nesting Waterbird Success at San Francisco Bay, California

Abstract The efficacy of long-term predator removal in urbanized areas is poorly understood. The impact of predation on ground-nesting waterbirds, as well as predator abundance and composition in predator removal versus non-removal or reference sites were examined at South San Francisco Bay. The success of natural nests and predator activity was monitored using track plates, trip cameras, wire haircatchers and simulated nests. Removal sites had higher nest densities, but lower hatching success than reference sites. Predator composition and abundance were not different at the removal and reference sites for any predator other than feral Cat (Felis domesticus). Striped Skunk (Mephitis mephitis) comprised the majority (84%) of predators removed, yet remained the most abundant predators in removal and reference sites. Urban environments provide supplemental food that may influence skunks and other nest predators to immigrate into vacancies created by predator removal. Based on the findings from this study, predator removal should be applied intensively over a larger geographic area in order to be a viable management strategy for some mammalian species in urbanized areas.

Cytochrome P4501A biomarker indication of the timeline of chronic exposure of Barrow's goldeneyes to residual Exxon Valdez oil.

We examined hepatic EROD activity, as an indicator of CYP1A induction, in Barrows goldeneyes captured in areas oiled during the 1989 Exxon Valdez spill and those from nearby unoiled areas. We found that average EROD activity differed between areas during 2005, although the magnitude of the difference was reduced relative to a previous study from 1996/1997, and we found that areas did not differ by 2009. Similarly, we found that the proportion of individuals captured from oiled areas with elevated EROD activity (≥ 2 times unoiled average) declined from 41% in winter 1996/1997 to 10% in 2005 and 15% in 2009. This work adds to a body of literature describing the timelines over which vertebrates were exposed to residual Exxon Valdez oil and indicates that, for Barrows goldeneyes in Prince William Sound, exposure persisted for many years with evidence of substantially reduced exposure by 2 decades after the spill.