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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, United States, 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. 

Abstract Earth is rapidly losing free-living species. Is the same true for parasitic species? To reveal temporal trends in biodiversity, historical data are needed, but often such data do not exist for parasites. Here, parasite communities of the past were reconstructed by identifying parasites in fluid-preserved specimens held in natural history collections. Approximately 2500 macroparasites were counted from 109 English Sole ( Parophrys vetulus ) collected between 1930 and 2019 in the Salish Sea, Washington, USA. Alpha and beta diversity were measured to determine if and how diversity changed over time. Species richness of parasite infracommunities and community dispersion did not vary over time, but community composition of decadal component communities varied significantly over the study period. Community dissimilarity also varied: prior to the mid-20th century, parasites shifted in abundance in a seemingly stochastic manner and, after this time period, a canalization of community change was observed, where species' abundances began to shift in consistent directions. Further work is needed to elucidate potential drivers of these changes and to determine if these patterns are present in the parasite communities of other fishes of the Salish Sea. 

The unusual blue color polymorphism of lingcod ( Ophiodon elongatus ) is the subject of much speculation but little empirical research; ~20% of lingcod individuals exhibit this striking blue color morph, which is discrete from and found within the same populations as the more common brown morph. In other species, color polymorphisms are intimately linked with host–parasite interactions, which led us to ask whether blue coloration in lingcod might be associated with parasitism, either as cause or effect. To test how color and parasitism are related in this host species, we performed parasitological dissection of 89 lingcod individuals collected across more than 26 degrees of latitude from Alaska, Washington, and California, USA. We found that male lingcod carried 1.89 times more parasites if they were blue than if they were brown, whereas there was no difference in parasite burden between blue and brown female lingcod. Blue individuals of both sexes had lower hepatosomatic index (i.e., relative liver weight) values than did brown individuals, indicating that blueness is associated with poor body condition. The immune systems of male vertebrates are typically less effective than those of females, due to the immunocompromising properties of male sex hormones; this might explain why blueness is associated with elevated parasite burdens in males but not in females. What remains to be determined is whether parasites induce physiological damage that produces blueness or if both blue coloration and parasite burden are driven by some unmeasured variable, such as starvation. Although our study cannot discriminate between these possibilities, our data suggest that the immune system could be involved in the blue color polymorphism–an exciting jumping-off point for future research to definitively identify the cause of lingcod blueness and a hint that immunocompetence and parasitism may play a role in lingcod population dynamics. 

Historical data are extremely rare but essential for ascertaining whether contemporary infectious disease burdens are unusual. Natural history collections are a valuable source of such data, especially for reconstructing long timelines of parasite abundance. We quantified the parasites of 109 museum specimens of English sole (Parophrys vetulus), an economically important flatfish, collected from Puget Sound, Washington, over a 90‐year period (1930–2019). We counted nearly 2,500 individual parasites representing 23 distinct species/morphotypes and four broad taxonomic groupings. Of the 12 taxa that were prevalent enough to include in the analysis, nine did not change in abundance over time, two (an acanthocephalan and a trematode) decreased, and one (another trematode) increased. By broad taxonomic grouping, nematodes, trematodes, and leeches exhibited no change over time, whereas acanthocephalans declined significantly. 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.

 

Although parasites are ubiquitous in marine ecosystems, predicting the abundance of parasites present within marine ecosystems has proven challenging due to the unknown effects of multiple interacting environmental gradients and stressors. Furthermore, parasites often are considered as a uniform group within ecosystems despite their significant diversity.

We aim to determine the potential importance of multiple predictors of parasite abundance in coral reef ecosystems, including reef area, island area, human population density, chlorophyll‐a, host diversity, coral cover, host abundance and island isolation.

Using a model selection approach within a database of more than 1,200 individual fish hosts and their parasites from 11 islands within the Pacific Line Islands archipelago, we reveal that geographic gradients, including island area and island isolation, emerged as the best predictors of parasite abundance.

Life history moderated the relationship; parasites with complex life cycles increased in abundance with increasing island isolation, while parasites with direct life cycles decreased with increasing isolation. Direct life cycle parasites increased in abundance with increasing island area, although complex life cycle parasite abundance was not associated with island area.

This novel analysis of a unique dataset indicates that parasite abundance in marine systems cannot be predicted precisely without accounting for the independent and interactive effects of each parasite's life history and environmental conditions.

 

Long‐term datasets are needed to evaluate temporal patterns in wildlife disease burdens, but historical data on parasite abundance are extremely rare. For more than a century, natural history collections have been accumulating fluid‐preserved specimens, which should contain the parasites infecting the host at the time of its preservation. However, before this unique data source can be exploited, we must identify the artifacts that are introduced by the preservation process. Here, we experimentally address whether the preservation process alters the degree to which metazoan parasites are detectable in fluid‐preserved fish specimens when using visual parasite detection techniques. We randomly assigned fish of three species (Gadus chalcogrammus, Thaleichthys pacificus, and Parophrys vetulus) to two treatments. In the first treatment, fish were preserved according to the standard procedures used in ichthyological collections. Immediately after the fluid‐preservation process was complete, we performed parasitological dissection on those specimens. The second treatment was a control, in which fish were dissected without being subjected to the fluid‐preservation process. We compared parasite abundance between the two treatments. Across 298 fish individuals and 59 host–parasite pairs, we found few differences between treatments, with 24 of 27 host–parasite pairs equally abundant between the two treatments. Of these, one pair was significantly more abundant in the preservation treatment than in the control group, and two pairs were significantly less abundant in the preservation treatment than in the control group. Our data suggest that the fluid‐preservation process does not have a substantial effect on the detectability of metazoan parasites. This study addresses only the effects of the fixation and preservation process; long‐term experiments are needed to address whether parasite detectability remains unchanged in the months, years, and decades of storage following preservation. If so, ecologists will be able to reconstruct novel, long‐term datasets on parasite diversity and abundance over the past century or more using fluid‐preserved specimens from natural history collections.