Tracy Allison M, Pagenkopp Lohan Katrina M, Carnegie Ryan B, McCollough Carol B, Southworth Melissa, Ogburn Matthew B
Institute of Marine and Environmental Technology, University of Maryland Baltimore County, 701 E. Pratt Street, Baltimore, MD, United States; Department of Marine Biotechnology, University of Maryland Baltimore County, 701 E. Pratt Street, Baltimore, MD, United States; Department of Microbiology & Immunology, University of Maryland Baltimore School of Medicine, 701 E. Pratt Street, Baltimore, MD, United States; Smithsonian Environmental Research Center, 647 Contees Wharf Rd, Edgewater, MD, United States.
Smithsonian Environmental Research Center, 647 Contees Wharf Rd, Edgewater, MD, United States.
J Invertebr Pathol. 2024 Nov;207:108201. doi: 10.1016/j.jip.2024.108201. Epub 2024 Sep 23.
Co-infecting parasites modify infection outcomes in the wild. However, it is unclear how multiple environmental factors influence co-infection. The Chesapeake Bay metapopulation of the eastern oyster, Crassostrea virginica, provides an opportunity to test the importance of co-infection across heterogeneous environments because multiple parasites infect oysters across a broad salinity gradient. This study leverages Maryland and Virginia oyster monitoring for a large-scale survey of four co-infecting organisms, including two tissue parasites and two shell bio-eroding parasites. We diagnosed infection in 440 oysters across 16 paired harvested and unharvested reefs and tested the importance of co-infecting organisms for each parasite relative to environmental conditions, host traits, and marine spatial management. Microscopic visual methods were used to diagnose prevalence and intensity of tissue infections with Perkinsus marinus (the causative agent of dermo disease) and Haplosporidium nelsoni (the causative agent of MSX disease). Macroscopic visual methods were used to diagnose prevalence and intensity of shell infections with Cliona boring sponges and blister-inducing Polydora worms. For the three oyster parasites that were detected [H. nelsoni infections were absent in all oysters], salinity was the overall strongest predictor, corresponding to bay-wide patterns of parasite prevalence and/or intensity. Despite high environmental and spatial variation, co-infections corresponded to altered prevalence and/or intensity for all three oyster parasites. The correlational patterns suggest that P. marinus acts as a lynchpin in co-infection, as its intensity increased with Cliona sponge prevalence and P. marinus co-infection predicted higher Polydora blister intensity. Oyster shell height, reef habitat, and harvest status also predicted parasite prevalence and intensity, further reflecting the multivariate drivers of infections in this system. Unharvested reefs had greater vertical habitat structure and higher intensities of Cliona sponge infections, but no differences in the prevalence of any of the three parasites. Spatial patterns unexpectedly show that reef-level predictors of parasite patterns were more important than differences between tributaries. This correlational survey provides novel insights through the statistical relationships between the three oyster parasites, environmental conditions, host traits, and human resource management. New and more detailed scenarios are needed to expand disease ecological theory to encompass co-infection in anthropogenically impacted wildlife populations.
共同感染的寄生虫会改变野生环境中的感染结果。然而，尚不清楚多种环境因素如何影响共同感染。切萨皮克湾东部牡蛎（Crassostrea virginica）的复合种群提供了一个机会，可用于测试在异质环境中共同感染的重要性，因为多种寄生虫在广泛的盐度梯度范围内感染牡蛎。本研究利用马里兰州和弗吉尼亚州的牡蛎监测数据，对四种共同感染的生物进行大规模调查，其中包括两种组织寄生虫和两种侵蚀贝壳的寄生虫。我们诊断了16对已收获和未收获礁石上440只牡蛎的感染情况，并测试了相对于环境条件、宿主特征和海洋空间管理而言，共同感染生物对每种寄生虫的重要性。使用显微镜视觉方法诊断马里兰帕金虫（Perkinsus marinus，引起皮疽病的病原体）和纳尔逊单孢子虫（Haplosporidium nelsoni，引起MSX病的病原体）的组织感染率和感染强度。使用宏观视觉方法诊断钻孔海绵（Cliona）和引起水泡的多毛类蠕虫对贝壳的感染率和感染强度。对于检测到的三种牡蛎寄生虫[所有牡蛎均未检测到纳尔逊单孢子虫感染]，盐度是总体上最强的预测因子，与全湾范围内的寄生虫感染率和/或感染强度模式相对应。尽管环境和空间变化很大，但共同感染对应于所有三种牡蛎寄生虫的感染率和/或感染强度的改变。相关模式表明，马里兰帕金虫在共同感染中起关键作用，因为其感染强度随着钻孔海绵感染率的增加而增加，并且马里兰帕金虫的共同感染预示着更高的多毛类蠕虫水泡强度。牡蛎壳高度、礁石栖息地和收获状态也可预测寄生虫感染率和感染强度，进一步反映了该系统中感染的多变量驱动因素。未收获的礁石具有更大的垂直栖息地结构和更高的钻孔海绵感染强度，但三种寄生虫的感染率没有差异。空间模式出乎意料地表明，寄生虫模式的礁石水平预测因子比支流之间的差异更重要。这项相关调查通过三种牡蛎寄生虫、环境条件、宿主特征和人力资源管理之间的统计关系提供了新的见解。需要新的、更详细的情景来扩展疾病生态学理论，以涵盖受人为影响的野生动物种群中的共同感染。
