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Health surveillance of a potential bridge host: Pathogen exposure risks posed to avian populations augmented with captive-bred pheasants

Augmentation of wild populations with captive-bred individuals presents an inherent risk of co-introducing novel pathogens to naïve species, but it can be an important tool for supplementing small or declining populations. Game species used for human enterprise and recreation such as the ring-necked pheasant ( Phasianus colchicus ) are commonly raised in captivity and released onto public and private wildlands as a method of augmenting naturalized pheasant populations. This study presents findings on pathogen exposure from three sources of serological data collected in California during 2014–2017 including (a) 71 pen-reared pheasants sampled across seven game bird breeding farms, (b) six previously released pen-reared pheasants captured at two study sites where wild pheasants occurred and (c) 79 wild pheasants captured across six study sites. In both pen-reared and wild pheasants, antibodies were detected against haemorrhagic enteritis virus (HEV), infectious laryngotracheitis (ILT), infectious bursal disease virus (IBDV), paramyxovirus type 1 (PMV-1) and Pasteurella multocida (PM). Previously released pen-reared pheasants were seropositive for HEV, ILT, and PM. Generalized linear mixed models accounting for intraclass correlation within groups indicated that pen-reared pheasants were more than twice as likely to test positive for HEV antibodies. Necropsy and ancillary diagnostics were performed in addition to serological testing on 40 pen-reared pheasants sampled from five of the seven farms. Pheasants from three of these farms tested positive by PCR for Siadenovirus, the causative agent of both haemorrhagic enteritis in turkeys and marble spleen disease of pheasants, which are serologically indistinguishable. Following necropsy, owners from the five farms were surveyed regarding husbandry and biosecurity practices. Farms ranged in size from 10,000 to more than 100,000 birds, two farms raised other game bird species on premises, and two farms used some form of vaccination. Biosecurity practices varied by farm, but the largest farm implemented the strictest practices.

California

Diseases of amphibian eggs and embryos

Amphibians generally are prolific egg producers. In tropical and semi-tropical regions, deposition of eggs may occur year-round or may coincide with rainy seasons, while in temperate regions, deposition of eggs usually occurs immediately after emergence from hibernation. Numbers of eggs produced by each species may vary from a few dozen to thousands. Accordingly, some eggs may be infertile and wastage of embryos is to be expected. Fertility, viability and decomposition of eggs and embryos must be considered before it is assumed that diseases are present. An important consideration in the evaluation of egg masses is the fact that some will contain infertile and non-viable eggs. These infertile and nonviable eggs will undergo decomposition and they may appear similar to eggs that are infected by a pathogen. Evaluation of egg masses and embryos for the presence of disease may require repeated observations in a given breeding season as well as continued monitoring of egg masses during their growth and development and over successive breeding seasons. Amphibian eggs rarely are subjected to a comprehensive health (diagnostic) examination; hence, there is scant literature on the diseases of this life stage. Indeed, the eggs of some North American amphibians have yet to be described. Much basic physiology and normal biomedical baseline data on amphibian eggs is lacking. For example, it is known that the aquatic eggs of some species of shrimp quickly are coated by a protective and commensal bacterium that effectively impedes invasion of the eggs by other environmental organisms and potential pathogens. In the absence of this bacterium, shrimp eggs are rapidly killed by other bacteria and fungi (Green, 2001). The possibility that amphibian eggs also have important symbiotic or commensal bacteria needs to be investigated. Furthermore, the quantity and types of chemicals in the normal gelatinous capsules of amphibian eggs have scarcely been examined. Abnormalities of the female oviduct, either due to infectious disease, nutritional status, hormonal imbalances, or sublethal intoxications, could affect the quality of secreted gelatinous capsules on eggs, thus rendering an egg mass susceptible to other stressors. Diseases of amphibian eggs and embryos presented in this chapter are Lucke frog herpesvirus Ranavirus (iridovirus) infection Bacteria Watermold infection (saprolegniasis) Algae Microsporidia

Book chapter

Genetic variation underlying resistance to infectious hematopoietic necrosis virus in a steelhead trout ( Oncorhynchus mykiss ) population

Understanding the mechanisms of host resistance to pathogens will allow insights into the response of wild populations to the emergence of new pathogens. Infectious hematopoietic necrosis virus (IHNV) is endemic to the Pacific Northwest and infectious to Pacific salmon and trout ( Oncorhynchus spp.). Emergence of the M genogroup of IHNV in steelhead trout O. mykiss in the coastal streams of Washington State, between 2007 and 2011, was geographically heterogeneous. Differences in host resistance due to genetic change were hypothesized to be a factor influencing the IHNV emergence patterns. For example, juvenile steelhead trout losses at the Quinault National Fish Hatchery (QNFH) were much lower than those at a nearby facility that cultures a stock originally derived from the same source population. Using a classical quantitative genetic approach, we determined the potential for the QNFH steelhead trout population to respond to selection caused by the pathogen, by estimating the heritability for 2 traits indicative of IHNV resistance, mortality ( h 2 = 0.377 (0.226 - 0.550)) and days to death ( h 2 = 0.093 (0.018 - 0.203)). These results confirm that there is a genetic basis for resistance and that this population has the potential to adapt to IHNV. Additionally, genetic correlation between days to death and fish length suggests a correlated response in these traits to selection. Reduction of genetic variation, as well as the presence or absence of resistant alleles, could affect the ability of populations to adapt to the pathogen. Identification of the genetic basis for IHNV resistance could allow the assessment of the susceptibility of other steelhead populations.

Diseases of Aquatic Organisms

Emergence of MD type infectious hematopoietic necrosis virus in Washington State coastal steelhead trout

Infectious hematopoietic necrosis virus (IHNV) occurs in North America as 3 major phylogenetic groups designated U, M, and L. In coastal Washington State, IHNV has historically consisted of U genogroup viruses found predominantly in sockeye salmon Oncorhynchus nerka . M genogroup IHNV, which has host-specific virulence for rainbow and steelhead trout O. mykiss , was detected only once in coastal Washington prior to 2007, in an epidemic among juvenile steelhead trout in 1997. Beginning in 2007 and continuing through 2011, there were 8 IHNV epidemics in juvenile steelhead trout, involving 7 different fish culture facilities in 4 separate watersheds. During the same time period, IHNV was also detected in asymptomatic adult steelhead trout from 6 coastal watersheds. Genetic typing of 283 recent virus isolates from coastal Washington revealed that the great majority were in the M genogroup of IHNV and that there were 2 distinct waves of viral emergence between the years 2007 and 2011. IHNV type mG110M was dominant in coastal steelhead trout during 2007 to 2009, and type mG139M was dominant between 2010 and 2011. Phylogenetic analysis of viral isolates indicated that all coastal M genogroup viruses detected in 1997 and 2007 to 2011 were part of the MD subgroup and that several novel genetic variants related to the dominant types arose in the coastal sites. Comparison of spatial and temporal incidence of coastal MD viruses with that of the rest of the Pacific Northwest indicated that the likely source of the emergent viruses was Columbia River Basin steelhead trout.

Washington

Evaluating management alternatives for Wyoming elk feedgrounds in consideration of chronic wasting disease

Executive Summary The authors used decision and modeling analyses to evaluate management alternatives for a decision on whether to permit Cervus canadensis (elk) feeding on two sites on Bridger-Teton National Forest, Dell Creek and Forest Park. Supplemental feeding of elk could increase the transmission of chronic wasting disease (CWD) locally and disease spread regionally, potentially impacting elk populations over time with wider implications for Odocoileus hemionus (mule deer) and Odocoileus virginianus (white-tailed deer) populations and hunting, tourism, and regional revenue. Supplemental feeding is thought to improve overwinter elk survival and reduce the commingling of elk with cattle during months when brucellosis transmission risk is highest. We worked with the U.S. Department of Agriculture Forest Service to identify their fundamental objectives and associated performance metrics related to this feedground decision. We then developed disease and habitat selection models to quantify the effect of four management alternatives on select performance metrics. The four alternatives were to continue to permit feeding, phaseout permits to feed in three years, permit feeding on an emergency basis, or stop permitting feeding. In this report, we present methods and summarized results on disease and habitat selection models and summaries of other performance metrics analyzed by BIO-WEST, Inc. and Cirrus Ecological Solutions as part of an Environmental Impact Statement. Data from Wyoming Game and Fish Department (WGFD) supported the assumption that supplemental elk feeding allows for larger elk populations in a region. We documented that herd units (HU) without feedgrounds had 23 percent lower densities of elk per area of winter range when compared against HUs with feedgrounds, after accounting for differences in sightability of elk during counts on and off feedgrounds. Thus, throughout our analyses, we assumed feedground closures would reduce elk carrying capacity resulting in an average decline of previously fed elk population segments by 23 percent (5th and 95th percentiles = [11 percent, 35 percent]) by year 20. Most of that decline occurred within the first few years after a feedground ceases to operate. We used a panel of CWD experts to help estimate CWD trans-mission in fed and unfed elk population segments. In aggregate, the expert panel estimated that median values of direct and indirect transmission of CWD are expected to be 1.9 and 4 times higher, respectively, in fed elk populations compared to unfed elk. We used these disease transmission estimates in combination with local elk demographic rates and carrying capacity estimates to project disease and population dynamics. In year 20, we predicted CWD prevalence would increase to 42 percent (5th and 95th percentiles = [29 percent, 55 percent]), and 13 percent (5th and 95th percentiles = [4 percent, 26 percent]) on average for fed and unfed elk population segments, respectively, given a starting prevalence of 1.6 percent. The prevalence estimates for the unfed elk population segments are in the range of previous observations of CWD in elk in the western United States. The average CWD prevalence from 2016 to 2018 in the unfed elk population of Wind Cave National Park in South Dakota was 18 percent overall but up to 30 percent in some regions (Sargeant and others, 2021). Meanwhile, CWD prevalence in the Iron Mountain and Laramie Peak elk herds in Wyoming from 2016 to 2018 was 14 percent and 7 percent, respectively, despite being present since at least 2002 (Wyoming Game and Fish Department, 2020b). From 2016 to 2020, elk that were fed at Dell Creek and Forest Park constituted on average 12–20 percent of the total elk on their respective HUs. As a result, the differences between management alternatives are modest when considering the closure of only one feedground on a HU. The no feeding alternative for Forest Park resulted in a CWD prevalence of 17 percent (SD = 7 percent) in the Afton HU compared to 20 percent (SD = 7 percent) with continued feeding by year 20. In the Upper Green River HU, no feeding on Dell Creek resulted in a CWD prevalence of 27 percent (SD = 6 percent) compared to 30 percent (SD = 5 percent) with continued feeding. In terms of disease-associated mortality, we predicted the closure of Forest Park and Dell Creek feedgrounds would reduce the total number of CWD mortalities by 9 percent in the Upper Green River HU and 26 percent in the Afton HU during the 20-year timespan. Our spatial analyses predicted that management alternative effects vary by HU as a function of private property and other wildlife winter ranges proximity relative to feedground location. The predicted number of elk abortions on private land, as a proxy for brucellosis risk to cattle, may increase by 8–21 percent in the absence of feeding at Dell Creek and Forest Park. Eight feedgrounds are located on Bridger-Teton National Forest, all of which have permits that have expired or will expire prior to 2028. In addition, WGFD could change their management of feedgrounds given new information; therefore, we also assessed the cumulative effects of continued feeding, phaseout, and no feeding management alternatives across five HUs south of Jackson, Wyoming (Afton HU, Fall Creek HU, Piney HU, Pinedale HU, and Upper Green River HU). These five HUs ranged from about 41 to 85 percent of the elk herd using feedgrounds, which corresponded to a CWD prevalence at year 20 of 23–34 percent if all feedgrounds in those five HUs remained open relative to 12 to 14 percent if all feedgrounds were closed. We predicted feedground closures may result in immediate reductions in population size relative to alternatives that continue feeding (for example, continued feeding and emergency feeding alternatives); however, over longer periods of time, CWD-associated mortality leads to larger population reductions. The no feeding alternative resulted in higher elk population sizes compared to the continued feeding alternative after about 10 years of implementation. Delayed action under a phaseout alternative resulted in increasing the CWD prevalence to 20 percent relative to 12 to 14 percent, on average, without feeding on HUs with a large population of fed elk such as the Upper Green River HU. Summarizing our cumulative results across all five of the analyzed HUs, we predicted continued feeding will lead to fewer elk by year 20 (mean = 8,300, standard deviation [SD] = 740) compared to no feeding at U.S. Department of Agri-culture Forest Service sites (10,700, SD = 890). The closure of all feedgrounds was projected to result in the largest elk populations at year 20 (12,500, SD = 980). No feeding at all sites also resulted in the largest cumulative harvest of 57,700 (SD = 2,600) compared to 51,100 (SD = 3,800) for continued feeding at all current feedground sites on the five HUs. Continued feeding also resulted in the lowest brucellosis costs to producers ($194,600, SD = $11,500) compared to no feeding on all feedgrounds ($243,000, SD = $13,700). Assuming moderate reductions in hunter interest because of increasing CWD prevalence in elk, we predicted that no feeding resulted in regional revenues generated by hunting activities of $190 million (SD = $10 million) compared to $173 million (SD = $10 million) for continued feeding over the 20-year timeframe. Recent CWD detections in mule deer and elk in Grand Teton National Park has elevated the importance of the cur-rent decision on whether, and how, to permit elk feeding on Dell Creek and Forest Park and the management of the other feedgrounds. Aggressive male harvest has slowed, but not stopped, the increasing prevalence of CWD in mule deer (Conner and others, 2021). It is unclear whether harvest management can be an effective tool to slow the spread of CWD in elk. There are also no effective treatments or vaccines for CWD, and it is unlikely that any will be developed that can be easily deployed in the near future. Thus, reducing artificial aggregations is one of the few management approaches suggested by the Western Association of Fish and Wildlife Agencies (Almberg and others, 2017). Future surveillance and monitoring can be designed to resolve uncertainties that can improve future decision-making. If feedgrounds close, research could quantify elk population reductions in the absence of feeding, the redistribution of fed elk to other places, or the consequences of elk movement on private property. If feedgrounds remain open, research could assess how rapidly CWD spreads in artificial aggregations of elk; however, surveillance programs would need to be designed with sufficient power to detect initial changes of CWD prevalence. Delaying action on feedground management was projected to be costly. Results of the phaseout alternative relative to the no feeding alternative suggested a 3-year delay was enough for substantial long-term changes in CWD prevalence. The long-term persistence of infectious CWD prions in the environment suggests that feedground management decisions may have long-lasting consequences. Our results indicated tradeoffs in the ability of a management agency to achieve all their objectives, and all management alternatives resulted in significant reductions in elk population size. This report contains the foundational elements for formal decision analysis methods, which can be implemented to help decision makers transparently evaluate the consequences of decision alternatives and identify the set of actions that best achieve agency and stakeholder priorities.

Wyoming