Long-term change in the burden of anisakid nematode parasites for marine mammal hosts

Abstract

Many marine mammal populations are failing to rebound despite legal protections; in this dissertation, I explore whether rising rates of parasitism may be placing an increasing energetic burden on already precarious host populations. Gastrointestinal parasites of the family Anisakidae are commonly found during necropsies of marine mammals. Anisakids have complex life cycles, requiring multiple intermediate hosts, including invertebrates, fishes, and cephalopods, to reach their definitive marine mammal hosts. These parasites have long been assumed to have only mild impacts on host health, but recent research suggests that the seriousness of these infections has been overlooked, with health effects ranging from energy loss and reduced immune system function to gastritis and ulceration in the gastrointestinal tract. Anisakid abundance in intermediate fish hosts is increasing globally. In some regions, increases in anisakids in fish have been linked to increasing marine mammal definitive host abundance. With legislation prohibiting their exploitation, many marine mammal populations have been able to recover to historic abundances, potentially increasing anisakid transmission in their ecosystems. However, other marine mammals have lagged in their recovery. As some marine mammal species increase, they may be increasing the burden of parasitism on more vulnerable species, essentially engaging in “apparent competition.” In this dissertation, I assess how anisakid abundances have changed in important prey species both globally and in the North Pacific, what factors may drive these changes, and estimate infection rates in a population of endangered killer whales. In Chapter 1, I used a meta-analytic dataset of anisakid abundance in fish and cephalopod species to assess how anisakid abundance has changed globally in important marine mammal prey species over the past few decades. However, this dataset does not include data from the marine-mammal-rich Northeast Pacific. In Chapter 2, I use museum specimens of ecologically important fish prey species collected in Puget Sound, Washington, USA, from 1920–2018 to determine how anisakid abundances have changed over time in relation to possible definitive host and environmental drivers. Museum collections lack adult salmon specimens, a common prey item for many marine mammals in this region. In Chapter 3, I use a novel data source, archived canned salmon, to assess changes in anisakid abundance in four species of Alaskan salmon from 1979–2021. Finally, in Chapter 4, I test for parasitism among southern resident killer whales, a highly endangered marine mammal population whose range includes Alaska and Puget Sound; I also assess whether infections are correlated with poor body condition. Taken together, these four chapters reveal recent increases in anisakids both globally and regionally in the Northeast Pacific. In Puget Sound, this increase coincides with and may be caused by increasing marine mammal abundances. Furthermore, southern resident killer whales face a high burden of anisakids, which may be putting additional energetic stress on this already vulnerable population. My findings reveal a changing landscape of infection risk, which could represent an increasing threat to vulnerable marine mammal populations in Puget Sound, Alaska, and beyond.