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.

Now, a University of Washington Innovation Award is allowing our our team 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. 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.

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.

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.

Preliminary data. Puget Sound is the jewel of Washington State – an economic, cultural, and aesthetic fulcrum point for the region – but our preliminary work has already demonstrated an alarming trend of increasing infection in the Sound. Clavinema mariae is a nematode parasite of benthic fishes that is common in English sole (Parophrys vetulus). We obtained historical records of its abundance from the literature and from unpublished Washington Department of Fish and Wildlife data, and resampled the same locations using the same methods in 2017, to compare historical and contemporary C. mariae abundance (Figure 2a; Howard et al. in press). We also used our newly developed approach: we examined museum specimens of English sole, collected between 1930 and 2016, for C. mariae burden (Figure 2b; Howard et al. in press). Both the historical data and museum specimen approaches demonstrated increases over time in C. mariae abundance, with robust agreement between the two approaches. In addition to documenting a previously unrecognized eightfold increase in the burden of an economically important parasite, this work demonstrates that parasitological examination of liquid-preserved museum specimens can produce reliable data on long-term trends in parasite abundance, at a much greater temporal resolution (Figure 2b) than is possible to obtain from historical records (Figure 2a).

Figure 2. (a) Historical (1949– 1976) and contemporary (2017) prevalence of Clavinema mariae in English sole at five sites. (b) Abundance of Clavinema mariae in specimens of English sole from the UW Fish Collection, as a function of year of the specimen’s collection. Both plots reproduced from Howard et al. in press.

Our plan of attack. In the next two years, we will museum specimens to (Q1) assess whether there has been a general trend of increasing or decreasing infection among Puget Sound fishes over the past century, (Q2) characterize change in the composition of these parasite assemblages over time, and (Q3) identify the parasite and host traits that predict increasing parasite abundance over time. We have chosen 10 representative host species across the Puget Sound food web (i.e., spanning trophic levels), sourced museum lots of these species from the UW Fish Collection and other nationally recognized natural history collections, and are performing parasitological dissections of these museum specimens. We will use the resulting data to reconstruct trajectories of change for the entire parasite fauna of each species – revealing a century of change in infection for Puget Sound fishes.


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