Historical ecology of marine and freshwater parasites

The history of medical science teaches us that epidemics of infectious disease can smolder for years, unnoticed. HIV spilled over from primates to humans in the early 1900s in central Africa, but wasn’t recognized by physicians until it was described in 1981 in North American patients. For decades, it spread across the globe, killing millions of people, going entirely unrecognized by modern medicine.

Today, a similar story may be unfolding in ocean ecosystems. Recent decades have brought explosions of infectious disease among marine organisms, including die-offs of sea stars on the west coast of North America, endangered black abalone in California’s Channel Islands, sea urchins in the Caribbean, and pilchards in Australia. These events appear to be increasing in frequency and magnitude. As in the case of HIV, we must ask: where did these infections come from, when did they appear on the scene, and how has their frequency and severity changed over time?

Whether and why wildlife disease is on the rise are questions of profound importance for ecology, conservation, and human society, but they are also notoriously troublesome questions to address. To understand temporal patterns in disease prevalence requires that we contrast contemporary conditions against appropriate baseline data, which can be difficult to come by. Some attempts to assess change in marine disease over time have made use of meta-analysis, but this approach can reach back only a few decades, to the publication dates of the earliest papers systematically catalogued in research databases. By the middle of the 20th century, ocean ecosystems had already been radically altered by fishing, climate change, biological invasions, and other forces. If marine disease is on the rise, we will need more than a few decades of data to detect it.

Our lab is working to “turn back the clock” – to generate primary data on the dynamics of marine disease over long time profiles and at unprecedented temporal, spatial, and taxonomic resolutions. We have several funded projects that tackle this problem.

How? In the basements of thousands of museums around the world, biological collections languish. An underutilized resource, museum specimens are a repository of information on historical disease assemblages, and perhaps our only means of reconstructing these assemblages. Many disease agents are preserved alongside their vertebrate and invertebrate hosts, whether pickled in ethanol or formalin. Our preliminary dissections at the California Academy of Sciences (San Francisco, CA), the Smithsonian Institution’s National Museum of Natural History (Washington, DC), and the UW Fish Collection have confirmed that delicate parasites are preserved and detectable, even in decades-old specimens (Figure 1). We are using these resources to develop time profiles of disease agent abundance and diversity, encompassing more than 130 years and bracketing major turning points in the history of ocean ecosystem degradation. This approach will be a first step toward developing an unbiased, empirical estimate of historical rates of marine disease – data that can be used to test whether the perceived rise in marine disease is real or an artifact of improved observation and reporting.

Figure 1. (a) Specimens in the Ichthyology Collection at the California Academy of Sciences, San Francisco, CA. (b) Some metazoan parasites recovered from dissections of Atlantic cod (Gadus morhua) and spiny dogfish (Squalus acanthias) at the Smithsonian Institution’s National Museum of Natural History in Washington, DC.

Testing whether and why parasite burdens have changed in Puget Sound, WA. A University of Washington Innovation Award and a Sloan Research Fellowship are allowing our our team to reconstruct over one century of change in parasite burden for eight fish host species of Puget Sound. In collaboration with Luke Tornabene (UW), we are extracting information on historical marine diseases from the biological collections of the UW Fish Collection and other museums across the country. The project will provide the world’s first glimpse of disease dynamics in a “pristine” ocean, and will indicate whether Puget Sound is experiencing a rising tide of disease. Our preliminary data (from one of the eight host species, English sole [Parophrys vetulus]) indicate that, of 12 parasite taxa detected, nine did not change over time, two (an acanthocephalan and a trematode) decreased, and one (another trematode) increased. The diverging patterns among parasite taxa suggest a double-edged sword of responses to long-term ocean change: some parasites might be on the rise, while others are declining. This suggests both mounting risks of parasitism from some parasite species, and an alarming loss of parasite biodiversity for other parasite species.

Figure 2. Change in abundance over time for parasites with >5% prevalence. The y-axis is proportional parasite abundance (predicted number of parasites per millimeter of fish length). The predicted fit of the generalized linear mixed model is depicted by the solid black line and the 95% confidence interval is depicted by the gray band. Data points are the raw data representing abundance adjusted for host length for each individual. Green dots indicate models that were P > 0.05; navy and bright blue dots indicate models that were significantly declining or increasing (P < 0.05), respectively. (a) Copepoda sp, (b) Oceanobdella pallida, (c) Trematoda sp 3, (d) metacercaria sp 1, (e) Clavinema mariae, (f) Cucullanus annulatus, (g) Contracaecum sp, (h) Capillaria parophysi, (i) Spirurida sp 1, (j) Echinorhynchus spp, (k) Opecoelidae sp 1, (l) metacercaria sp 2. Reproduced from Welicky et al. 2021.

A natural experiment to test the influence of climate on temporal change in parasite burdens. A pilot research grant from the Cooperative Institute for Climate,
Ocean, and Ecosystem Studies (CICOES) is helping to launch a project that will exploit spatial variability in warming patterns to isolate the influence of climate on parasites. Sub-regions of the Gulf of Alaska have experienced divergent trajectories of warming and this variability in sea surface temperature across space will allow us to parse the influence of climate on parasite burden. In collaboration with Andrés López (University of Alaska Fairbanks Museum of the North), our team is quantifying change in Gulf of Alaska parasite assemblages by assessing the parasite burden of fish specimens collected at different points in time and space. We have chosen host species that span the Gulf of Alaska food web, and we will source museum lots of these species from the UW Fish Collection, the University of Alaska Fairbanks Museum of the North, and other nationally recognized natural history collections. We will perform parasitological dissections of these museum specimens and use the resulting data to reconstruct trajectories of change for the entire parasite fauna of each fish species. Aggregating across parasite taxa, our team will (Objective 1) assess whether there has been a general trend of increasing or decreasing infection over time, (Objective 2) identify the regions of the Gulf of Alaska that have experienced the most change in infection, and (Objective 3) isolate the potential role of climate warming in these changing infection patterns.

Two natural experiments to test the influence of urbanization and pollution on temporal change in parasite burdens. A CAREER Award from the National Science Foundation’s Division of Environmental Biology is allowing our team to test how urbanization and pollution affect temporal trajectories of change in parasite abundance. By carefully selecting specimens collected before and after the onset of a particular environmental impact (e.g., urbanization, pollutant inputs) in impacted and matched control areas (a before-after-control-impact or BACI design), we can discriminate change caused by the environmental impact from background change. River ecosystems lend themselves to such studies, because riverine fishes are well-represented in natural history collections, providing an ample number of specimens that can be mined for parasitological data (providing continuous data across a broad temporal scope) and, with their directional flow, rivers can serve as their own controls, as long as specimens have been collected both above- and below-stream of the impact under investigation (control/impact). We will begin by focusing on a specific impact – industrial pollution – in a carefully planned natural experiment situated in the US Gulf South region and supported by Hank Bart, Curator of Fishes at the Tulane University Biodiversity Research Institute (TUBRI) (Figure 3).

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Figure 3. Sampling sites and availability of specimens for Project 1. (a) Project 1 study area. (b–c) Maps of sampling locations (white markers = control, grey markers = polluted) and pulp mills (black markers) with plots of specimen availability for (b) Pearl River, LA and (c) Alabama River, AL. For plots, each point is a lot (i.e., a jar of fish) held in the TUBRI Ichthyology Collection, C = control sites, P = polluted sites, and each color is a different fish host species (of the 10 species to be targeted). Dashed line = implementation of the Clean Water Act (CWA) in 1973, light grey shading = before implementation of CWA, dark grey vertical bars = droughts.

We will then test the influence of urbanization, a geographically widespread impact that not only changes water quality, but also increases temperature, causes “flashier” hydrology (i.e., more frequent and rapid changes in streamflow), and simplifies physical habitat of river ecosystems. This second study will be situated in Albuquerque, NM and supported by Tom Turner, Curator of Fishes at the University of New Mexico’s Museum of Southwestern Biology (MSB) (Figure 4). In these two projects, our team will address the following questions: Q1: How has the abundance of parasites in river ecosystems changed over the past half century? Q2: What roles have industrial pollution and urbanization played in shaping change in parasite abundance through time? Q3: How do industrial pollution and urbanization affect the stability (i.e., resistance + resilience) of parasite communities as they experience other disturbances (e.g., drought)? Armand Kuris (UC Santa Barbara) and Maarten Vanhove (Hasselt University) are also collaborators on the project and will participate in data collection.

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Figure 5. (a) Map of Project 2 study area, indicating two regions: “control” = north of dashed line, upstream of the North Diversion Channel (i.e., the Albuquerque outfall that contributes the greatest discharge by volume to the Rio Grande), and “urbanized” = south of dashed line, below North Diversion Channel. (b) Fish specimens available for dissection at MSB from control and urbanized regions. Each point is a lot (i.e., a jar of fish) held at MSB, with size proportional to the number of individual fish in the lot. HA = Hybognathus amarus, PP = Pimephales promelas, and GA = Gambusia affinis. X and Y positions are jittered to allow visualization of overlapping points. Dark grey vertical bar = the 1953–1956 drought.
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