101. Salmon in a warming world: Impact of pathogen infections on juvenile Chinook salmon (Oncorhynchus tshawytscha)
- Author
-
Abdelrazek, Samah
- Subjects
Animal diseases ,Aquatic sciences ,Behavior ,Chinook salmon ,Flavobacterium columnare ,Gene expression ,Temperature - Abstract
There is global concern over fish population declines, particularly for economically and culturally valuable salmonid species. Chinook salmon (Oncorhynchus tshawytscha), the largest in the genus Oncorhynchus, are anadromous salmonids native to the United States Pacific Northwest (PNW). Chinook salmon have declined in abundance and several populations are listed as threatened under the Endangered Species Act. Climate change is projected to have a further, significant impact on Chinook salmon populations, as water reservoir storage decreases, reducing river flows and increasing water temperatures. Sub-optimal water temperature has long been recognized as a key factor influencing disease progression in salmonids, by altering the nature or course of the immune response and increasing infectious agent abundance or virulence, to enhance the likelihood of disease progression. While many opportunistic pathogens may be endemic in a watershed, a disease often only manifests when other factors, such as poor environmental conditions, first compromise the host. Flavobacterium columnare, for example, is a re-emerging bacterial pathogen, especially during summer and early fall, and one of the etiological agents of columnaris disease. During the last two decades, columnaris has become one of the most serious threats to nearly all freshwater fishes including anadromous salmonids. Mitigating the effects of fish diseases requires a thorough understanding of the processes that drive host-pathogen interactions under various environmental conditions. There is a paucity of information on whether the outcomes of infections under various environmental conditions are caused by the environment’s effects on the host, the pathogen, or on both organisms. To address this knowledge gap, the objective of my dissertation was to investigate the context-specific dynamics associated with infectious agents. I used juvenile fall-run Chinook salmon, a species of conservation concern in the California Central Valley, as a sentinel for other runs of Chinook salmon listed as threatened or endangered. The overarching hypothesis of this dissertation was that the host physiological response is associated with the host immune- and stress-response, infection burden, and external stressors (e.g., temperature) that also mediate host-pathogen dynamics. The emphasis of my dissertation was on evaluating host-related factors that influence the outcome of pathogen infections for juvenile Chinook salmon, including tissue damage, the host immune response to prevent, control and eliminate pathogens, and detrimental consequences caused by inflammation, during warming. Many tools have been developed to better understand disease progression mechanisms, which could indicate organismal health status. Insight into which aspects of immunity are recruited can be gained by measuring the direction and magnitude of transcriptional changes in host immune gene regulation and can be paired with the measurement of infection severities in the same tissues (Chapter 1). I examined salmon survival following challenge with F. columnare at two temperatures (14 °C and 18 °C), F. columnare abundance, and transcript abundance of pro-inflammatory, acute phase proteins, anti-inflammatory cytokines, immunoglobulins, and stress-related genes in gills over 16 days. I found that with a temperature rise of 4 °C, F. columnare abundance and prevalence increased. Additionally, data emphasize the significance of timely and balanced immune responses in challenged Chinook salmon. I demonstrated that immune activation at elevated water temperatures that Chinook salmon experience during outmigration (18 °C) appeared to elicit a strong response against infection, as demonstrated by higher transcription levels of immune-related genes. The strong immune response, however, did not result in increased salmon survival, as mortality rates were significantly higher in fish challenged with F. columnare at 18 °C compared to those kept at a cooler temperature, 14 °C. Sub-lethal behavioral effects caused by bacterial infections can have long-lasting repercussions on fish ecological fitness through effects on predator avoidance and foraging success. I, therefore, conducted a study to determine whether F. columnare infection can alter the behavior of juvenile fall-run Chinook salmon. Specifically, I quantified locomotion and anxiety-like behavior. I utilized the open field test to assess locomotion followed by a novel object approach test to quantify anxiety. Additionally, I assessed F. columnare abundance in gills, and changes in expression of genes associated with behavior, in the brain tissue (Chapter 2). The results of this study indicated that: first, whereas challenged fish were less receptive to the presence of the novel object, control fish exhibited a range of behavioral responses. Second, there were significant differences in F. columnare abundance among challenged fish over time, with the pathogen abundance rapidly increasing but also showing potential for recovery over time. Lastly, F. columnare challenge elicited differential expression of behavior-related genes as the F. columnare infection progressed.Lastly, research on host-environment-agent interactions has focused on single pathogen studies. In many systems, however, salmon are exposed to a variety of pathogens, and these multiple exposures may synergize and not result in simple additive effects on the host. Therefore, I determined the prevalence and abundance of pathogens in gill and kidney tissues of fish deployed in the Sacramento River (CA, USA). I further determined consequences of pathogen exposure on salmon histological and physiological responses: expression of immune, stress, and development-related genes (Chapter 3). I found that fall-run Chinook salmon were exposed to multiple potential pathogens when out-migrating from the Sacramento River, with Ceratonova shasta and Parvicapsula minibicornis being the two dominant pathogens. I noted that the presence of specific pathogens in fish tissue does not always imply disease establishment and progression, especially for pathogens that are ubiquitous in the aquatic environment. I detected upregulation of immune and stress-related genes in gills before they were detected in kidneys, suggesting that gill biopsy may be useful for early-warning studies on what could potentially be a non-lethal target tissue. Furthermore, expression of investigated genes was altered following deployment; these responses could potentially represent irreversible impacts on salmon, thus demonstrating the threat of pathogen exposure and disease progression to the outmigrating Chinook salmon population. My dissertation indicates that infectious diseases will likely remain and worsen as a conservation issue as climate change continues to reshape host-pathogen dynamics and will significantly influence fish physiology, behavior, and survival. Combining nonlethal sampling with molecular genetic-based identification techniques opens a wide range of possibilities for creative study plans that could potentially address the true complexity of the host-pathogen dynamic in a warming world. Predicting the trajectory of these dynamics will require the inclusion of greater knowledge and tools (e.g., molecular techniques, histopathology, and behavior testing) outlined in this dissertation and other studies. This dissertation research, however, provides a foundation for future avenues of research investigating host-environment-agent interactions and offers crucial knowledge for future conservation efforts.
- Published
- 2023