Long-term data allow ecologists to assess trajectories of population abundance. Without this context, it is impossible to know whether a taxon is thriving or declining to extinction. For parasites of wildlife, there are few long-term data – a gap that creates an impediment to managing parasite biodiversity and infectious threats in a changing world. We produced a century-scale time series of metazoan parasite abundance and used it to test whether parasitism is changing in Puget Sound, USA and, if so, why. We performed parasitological dissection of fluid-preserved specimens held in natural history collections for eight fish species collected between 1880 and 2019. We found that parasite taxa using three or more obligately required host species – a group that comprised 52% of the parasite taxa we detected – declined in abundance at a rate of 10.9% per decade, whereas no change in abundance was detected for parasites using one or two obligately required host species. We tested several potential mechanisms for the decline in 3+-host parasites and found that parasite abundance was negatively correlated with sea surface temperature, diminishing at a rate of 38% for every 1°C increase. Although the temperature effect was strong, it did not explain all variability in parasite burden, suggesting that other factors may also have contributed to the long-term declines we observed. These data document one century of climate-associated parasite decline in Puget Sound – a massive loss of biodiversity, undetected until now.

Specimen selection and collection site history

We focused on the metazoan parasites of eight fish species from Puget Sound, Washington, USA, selecting host species that were well-represented in natural history collections and that encompassed a broad range of trophic levels, body sizes, habitats, functional feeding groups, and vulnerability to human impacts (Supplementary Information Table S1). Specimens were sourced primarily from the University of Washington Fish Collection (UWFC) at the Burke Museum of Natural History and Culture, with additional specimens from other collections to increase temporal scope and resolution (Figure 1b; Supplementary Information Table S2). For each specimen examined, we noted locality data from the natural history collection databases and measured the specimen’s total length (TL) in cm. When the collection location was descriptive but lacked coordinates, we estimated the collection location in decimal degrees using Google Maps.

Parasitological dissections

Each fish was subjected to a comprehensive parasitological dissection (see details in Fiorenza et al. [2020] and Snover et al. [2005]). For each parasite identified, we noted its broad taxonomic grouping (Subclass Copepoda, Subclass Hirudinea, Class Monogenea, Class Trematoda, Class Cestoda, Phylum Nematoda, Class Acanthocephala; Supplementary Information Table S3). For flatworms, we stained and mounted specimens before identification (Cable et al. 1963). For nematodes, we cleared specimens before identification (Cable et al. 1963). We identified each parasite to the finest taxonomic resolution, which in most cases was family or genus level, and classified them into one of two transmission strategies: directly transmitted (i.e., parasites that can be transmitted between conspecific hosts) or complex life cycle (i.e., parasites that are transmitted from one host species to another host species in an obligately required sequence). For complex life cycle parasites, we also estimated the number of obligately required host species based on natural history information (Supplementary Information Table S3). Parasites that were identified to species and found in more than one host were recorded under the same parasite taxon name (e.g., Derogenes varicus). Larval nematodes of the genera Anisakis and Contracaecum are known to be host generalists for their fish intermediate/paratenic hosts (Mattiucci et al. 2006; Kuhn et al. 2013; Shamsi 2019); therefore, even though these worms could not be identified to species, we also recorded these under the same parasite taxon name across host species (i.e., Contracaecum sp., Anisakis sp.). For all other parasites that were not identified to species, we assumed that individuals found in one host were of a different species than those found in another host, and named them accordingly (Sasal et al. 1998; Benesh et al. 2021; e.g., Lepeophtheirus sp. of Walleye Pollock versus Lepeophtheirus sp. of Surf Smelt).

Potential environmental drivers

In a retrospective study like this one, it is not possible to definitively identify the causal drivers of change in parasite abundance. However, we had access to several long-term environmental datasets and sought to assess the correlation between environmental variables and parasite burden. Our environmental datasets included information on sea surface temperature (Wan 2022), heavy metal and organic pollutants (Brandenberger et al. 2008), and fish host density (Greene et al. 2015; Essington et al. 2021) within Puget Sound.

The temperature and pollutant datasets reflect prevailing conditions in Puget Sound that might have affected all hosts and parasites, while fish density data reflect conditions pertaining primarily to parasites within that fish host. Data on sea surface temperature were from a continuous record (1921–2019) collected at Race Rocks lighthouse (Wan 2022); we extracted average monthly sea surface temperature in degrees Celsius, discarded any year in which more than one month was missing data (n = 4 of 98 years), and obtained an annual average for each year. For each host individual, we matched the year of the host’s collection to the corresponding year from the temperature dataset. Data on pollutants were from a continuous record (1774–2005) obtained by coring Puget Sound sediments (Brandenberger et al. 2008), which yielded values for the concentration of lead, arsenic, zinc, nickel, vanadium, chromium, copper, barium, and beryllium in micrograms per gram of sediment, as well as concentrations of lignin and soil biomarkers, which indicate inputs of terrestrial organic matter. We extracted annual values for each variable from two cores taken near Tacoma and Seattle, WA in Puget Sound (PS-1 near Tacoma = 47.347167, -122.409667; PS-4 near Seattle = 47.614967, -122.449017; Brandenberger et al. 2008), averaged values within each year across the two cores, and interpolated among years to bridge temporal gaps. Some of the 12 pollutant variables were collinear with one another (Supplementary Information Figure S3), so we performed a principal components analysis to reduce the dimensionality of the pollutant dataset and found that the first two principal components explained 74% of variation (Supplementary Information Figure S4). To account for annual measurement error, we ran a LOESS smoother on each principal component and then matched the year of each host individual’s collection to the corresponding year from the first and second principal components.

We also had access to data on the density of the fish hosts for six of the eight host species we examined: G. chalcogrammus, H. colliei, M. productus, and P. vetulus from Essington et al. [2021] and C. pallasii and H. pretiosus from Greene et al. [2015]. Data from Essington et al. [2021] were annual projections of density based on historical data collected from 1946 to 1977, while data from Greene et al. [2015] were estimates of catch per unit effort (CPUE) for various Puget Sound basins sampled between 1972 and 2011. For Greene et al. [2015], estimates were averaged across basins within each year to obtain an annual estimate of abundance across Puget Sound. For each fish species’ time series, we interpolated among years to bridge temporal gaps and matched the year of each host individual’s collection to the corresponding year from the host density dataset, matching host species to corresponding parasites (i.e., P. vetulus density was recorded for P. vetulus parasites only).

Literature cited

• Brandenberger, J. M. et al. Reconstructing trends in hypoxia using multiple paleoecological indicators recorded in sediment cores from Puget Sound, WA. National Oceanic and Atmospheric Administration, Silver Spring, MD (2008).
• Benesh, D. P., Parker, G. A., Chubb, J. C. & Lafferty, K. D. Trade-offs with growth limit host range in complex life-cycle helminths. Am. Nat. 197, E40–E54 (2021).
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• Mattiucci, S. & Nascetti, G. Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13, 99–113 (2006).
• Sasal, S., Desdevises, Y. & Morand, S. Host-specialization and species diversity in fish parasites: Phylogenetic conservatism? Ecography 21, 639–643 (1998).
• Shamsi, S. Parasite loss or parasite gain? Story of Contracaecum nematodes in antipodean waters. Parasit. Epi. Cont. 4, e00087 (2019).
• Snover, A. K., Mote, P. W., Whitely Binder, L. C., Hamlet, A. F. & Mantua, N. J. Uncertain future: climate change and its effects on Puget Sound. Climate Impacts Group, Center for Science in the Earth System, Joint Institute for the Study of the Atmosphere and Oceans, University of Washington (2005).
• Wan, D. 2022. British Columbia Lightstation Sea-Surface Temperature and Salinity Data (Pacific), 1914-present. https://open.canada.ca/data/en/dataset/719955f2-bf8e-44f7-bc26-6bd623e82884. Accessed 13 Dec 2022.

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