Arctic Biodiversity Assessment

528 Arctic Biodiversity Assessment

Protostrongylus stilesi, a lung nematode typical in Dall’s sheep Ovis dalli from the Brooks Range and Alaska Range of the western North American Arctic, and in muskoxen Ovibos moschatus in the Brooks Range and Arctic Coastal Plain of Alaska and Yukon Territories, Canada. Shown is the tail end of an adult male with characteristic copulatory structures which are important in diagnosis of these miniscule parasites. Photo: E.P. Hoberg.

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Chapter 15 Parasites

Lead Authors Eric P. Hoberg and Susan J. Kutz

Contributing Authors Joseph A. Cook, Kirill Galaktionov, Voitto Haukisalmi, Heikki Henttonen, Sauli Laaksonen, Arseny Makarikov and David J. Marcogliese

Contents

Summary ��530 I’ve seen that in caribou. Just a couple of years ago, 15.1. Introduction ��530 » every slice through it, you’d see about 50 little white 15.2. Parasites and their importance in the North ��532 round things. We were wondering what that was, so we 15.3. Status and knowledge ��533 checked it out, and it was a tapeworm. The whole body 15.4. Ecosystem components in the North ��534 was completely filled with tapeworms. Yeah. It’s unbe- lievable how they could actually still move and run and 15.5. Terrestrial ecosystems ��536 15.5.1. Mammals ��536 their whole body just completely filled with tapeworms. 15.5.1.1. Ungulates ��536 Village elder, Sachs Harbour, Canada, as related to S.J. Kutz. 15.5.1.2. Rodents ��538 15.5.2. Terrestrial birds ��539 15.6. Freshwater ecosystems ��539 15.6.1. Fishes ��540 He’s saying that when we go harvesting caribou, moose, 15.6.2. Birds ��541 » whatever, when we’re skinning them, we really watch 15.7. Nearshore and pelagic marine ecosystems ��542 out for all these things. The insides, and that yellow 15.7.1. Fishes ��542 stuff they’re talking about; it’s like a doctor looking at 15.7.2. Seabirds ��543 15.7.3. Marine mammals ��546 things. Like when you take the stomach out, you always look on the inside. You look at the liver; you look in the 15.8. Traditional ecological knowledge on parasites in the North ��547 flesh. Like when they bring the meat home and when 15.9. Conclusions and recommendations ��548 15.9.1. New tool development ��548 the women make dried meat, sometimes they find those 15.9.2. Anticipated important host-parasite assemblages little white like beans in the meat. That’s what we eat, and processes ��550 so when we skin something we have to make sure to Acknowledgements ��551 look at everything – the heart, the lungs, the liver, the References ��551 stomach, the kidney. Village elder, Fort Good Hope, Canada, as related to S.J. Kutz. 530 Arctic Biodiversity Assessment

SUMMARY range for hosts, and emergence of parasites and disease. These facets are essential to our capacity to predict fu- Parasites are among the most common organisms on the ture shifts in ecosystem structure over time, to develop planet, and represent diverse members of all biologi- adaptations, and to mitigate or prevent disease outbreaks cal communities. Parasites tie communities together, among human and wildlife populations. revealing or telling stories about critical connections established by a history of evolution, ecology (food habits, foraging behavior, interactions among host species) and 15.1. INTRODUCTION biogeography (patterns of geographic distribution) for host populations, species, ecosystems and regional faunas Parasites represent in excess of 40-50% of the organisms that constitute the biosphere. As such these organisms on Earth and are integral components of all ecosystems tell us about the processes, biological (e.g. range shifts, (Dobson et al. 2008). Vertebrates and invertebrates are invasion) and physical (e.g. climate variation), that have hosts for complex assemblages of macroparasites (worms determined the patterns of diversity that we observe in and arthropods including insects) and microparasites high latitude ecosystems. (viruses, bacteria, fungi and protozoans) that shape ecosystems, food webs, host demographics and host behav- Parasites can have subtle to severe effects on individual ior (e.g. Marcogliese 2001a, 2005, Hudson et al. 2006, hosts or broader impacts on host populations which may Dobson et al. 2008). Surprisingly, in some ecosystems cascade through ecosystems. Parasitic diseases have dual the biomass of parasites exceeds that of apex predators significance: such as birds and fishes, and these otherwise obscure or- 1. influencing sustainability for species and populations ganisms have extraordinary ecological connectivity with of invertebrates, fishes, birds and mammals, and involvement in over 75% of trophic links within food 2. secondarily affecting food security, quality and avail- webs (Lafferty et al. 2006). A substantial role in nutrient ability for people. cycling and trophic interactions at local to regional scales is evident for these assemblages of parasites (Kuris et al. As zoonoses, some parasites of animals can infect and 2008). cause disease in people and are a primary issue for food safety and human health. Sustainability, security and Parasites are taxonomically complex and diverse, even in safety of ‘country foods’ are of concern at northern high latitude systems characterized by relatively simple latitudes where people maintain a strong reliance on assemblages, and are considerably more species-rich than wildlife species. the vertebrate hosts in which they occur. For example, consider the 62+ described species of helminths, In the Arctic, we often lack baseline and long-term arthropods and protozoans, not to mention viruses and data to establish trends for parasite biodiversity (host bacteria, which circulate in four species of ungulates and geographic distributions or numerical measures of across high latitudes of North America and Greenland abundance and prevalence) in terrestrial, freshwater and (Kutz et al. 2012). Among 19 of 24 species of relatively marine systems, even for the best known host species. specialized auks (seabirds of the family Alcidae) there Absence of biodiversity knowledge has consequences are in excess of 100 species of helminths and arthropods for understanding the role of parasites in an ecosystem, in addition to viruses, bacteria and protozoans (Muz- and patterns of emerging animal pathogens, including zafar & Jones 2004). Among the five species of loons zoonotic diseases, at local to regional scales. There is (Gaviiformes) there are 97 species of helminths and urgent need to incorporate parasitological information among Holarctic grebes (three species of Podiceps), all of into policy and management plans and to emphasize which breed at high latitudes, there are 145 species of awareness of parasitic diseases to wildlife managers, helminths which contrasts with 244 among all podici- fisheries biologists, public health authorities and local pediforms in the global fauna (Storer 2000, 2002). communities. Further, in a single fish species, Arctic char Salvelinus alpinus, there are over 100 known species of helminths Parasitological knowledge can be incorporated into and protozoans (Dick 1984, Wrona & Reist, Chapter policy and management plans through an integration 13). These observations emphasize the broad distribution of field-based survey, local knowledge, development of of parasites across and within ecosystems in terrestrial baselines linked to specimens, archival data resources and aquatic environments. Considerable complexity and to assess change, and models that can predict potential knowledge gaps, however, suggest that it is currently spatial and temporal distribution for outbreaks of disease intractable to develop a synoptic picture for trends in among people or animals. We recommend that parasites abundance or diversity across phylogenetically dispa- be considered particularly as they relate to biodiversity rate assemblages of vertebrate hosts (fishes, birds and and conservation of populations, availability of subsist- mammals) and their parasites extending from regional ence food resources and concerns for food security to landscape scales. As an alternative, we highlight a and food safety (i.e. zoonoses and wildlife population series of exemplars demonstrating the importance of declines caused by parasites). Further, research is neces- parasites both conceptually and functionally as integral sary to demonstrate linkages among climate change, components of high latitude ecosystems. Our discus- environmental perturbation, shifting abundance and sion explicitly explores the distribution of metazoans Chapter 15 • Parasites 531

(helminths) and protozoans circulating in fishes, birds through ingestion of water or forage. In contrast, indi- and mammals, and to a lesser extent some parasites that rect transmission is often related to connections estab- are recognized as zoonotic pathogens; we do not exam- lished through foraging and food habits where preda- ine the diversity and distribution of viruses, bacteria, tors (definitive hosts) are infected through ingestion of parasitic fungi (in animals or plants; but see Dahlberg & prey (intermediate hosts where the parasite develops). Bültmann, Chapter 10), or arthropods in parasitic and Significantly, trophic structure in the Arctic involves an mutualisitc associations. unusually great percentage of predators and relatively fewer herbivores (Callaghan et al. 2004a). Predator-prey Parasites can cause disease and mortality, influence the interactions are among the dominant trophic links in dynamics and regulation of host populations, mediate high latitude systems where small to medium mam- competition among hosts which determines community malian and avian predators often specialize on voles and structure, and in the worst case scenarios contribute to lemmings in terrestrial environments; many shorebirds extinction events for hosts. Circulation of parasites is specialize on aquatic invertebrates in either marine or based on specific pathways that represent links among freshwater habitats (most often terrestrial/freshwater hosts and the environmental settings where they occur in the breeding season and marine in the non-breeding (Fig. 15.1). Some parasites have direct transmission cy- season). Consequently, parasite life cycles and transmis- cles that involve passage between definitive hosts where sion are directly influenced by fluctuations in abundance the adult parasite develops and reproduces. Often, the and density for both predators and prey species. Alter- infective stages will occur free in the environment, natively, indirect life cycles may involve vectors, usu- sensitive to ambient temperature, humidity, salinity and ally biting flies or other arthropods such as ticks, which light (including ultraviolet), and are acquired by hosts disseminate the parasites among hosts. In the Arctic, the

Figure 15.1. Life cycles for parasites. Transmission patterns emphasize the triad of ‘host-parasite-environment’, thus both biotic and abiotic mechanisms and controls serve to determine the occurrence of helminths, arthropods, protozoans and viruses. Indirect cycles involving development of larval stages in intermediate hosts ( IH-1 to IH-3) are typical for most helminth parasites in terrestrial, freshwater and marine systems of the Arctic. The IH(s) in specific cycles are usually invertebrates (arthropods, molluscs, annelids) or occasionally other vertebrates (fishes, birds or mammals) that are important as prey for the definitive or final host. Among helminths, 1-3 intermediate hosts are often required for transmission, and the length of the cycle is characteristic of a particular parasite group. In these cases life cycles describe predictable pathways associated with trophic linkages, and thus parasites serve as ecological indicators for diet or other host activities. Indirect cycles may also involve arthropod vectors ( V-1) that are required for development and transmission of parasites to the final host, usually for macroparasites or microparasites in the blood. Direct cycles involve transmission between definitive hosts, often with infective stages distributed in the environment. Photo: Matakiel Island, Northern Sea of Okhotsk, by E.P. Hoberg.

Indirect = Transmission by predator-prey cycles Invertebrate and/or vertebrate IH-2 intermediate hosts (IH) IH-1 Indirect Cycles Tapeworms (1-2 IH) Digenean ukes (1-3 IH) Nematodes (1-2 IH) Acanthocephalans (1-2 IH) Tissue-cyst protozoans (1 IH) Vertebrate Final Hosts IH-3 Direct Cycles Nematodes Monogenean ukes Intestinal protozoans Vector/ Indirect Viruses Nematodes Blood protozoans Viruses V-1 532 Arctic Biodiversity Assessment ambient environmental setting (temperature, humid- key to the present’, with history providing a pathway ity, seasonality, geography, host diversity, density and or analogue for predicting how complex host-parasite abundance) dramatically influences the survival, devel- systems will respond in a regime of accelerated environ- opment, abundance and distribution of parasites and mental change over time (Hoberg 1997). related disease in space and time (e.g. Kutz et al. 2005, Hoberg et al. 2008a, Kutz et al. 2009a, Laaksonen et al. 2010a, Kutz et al. 2012). 15.2. PARASITES AND THEIR Parasites have predictable associations with their hosts IMPORTANCE IN THE NORTH and consequently serve as indicators of ecological structure, biogeography and history in complex biological sys- Across the North, parasites are important as evidenced tems (e.g. Hoberg 1996, Marcogliese 2001a, Nieberding by their ecological connectivity among hosts, at local & Olivieri 2007, Hoberg & Brooks 2008, 2010, Morand landscape scales and more broadly across regional & Krasnov 2010). As succinctly outlined by Marcogliese communities. Parasites can be a concern for humans as (2001a): “… Parasites may be excellent indicators of bio- zoonotic organisms (transmissible from animals to hu- diversity. This idea follows from the very nature of para- mans often through consumption of wild food resources site lifecycles. Many parasites have a variety of intermedi- or ‘country foods’) (e.g. Gyorkos et al. 2003, Polley & ate hosts and often depend on predator-prey interactions Thompson 2009, Davidson et al. 2011) and as agents for transmission. A single parasite in its host reflects the of disease in populations of wild fish, birds or mam- presence of all the hosts that participate in its life cycle. mals that are the foundations of subsistence foodwebs. All the parasite species occurring in the host (the parasite Although parasites are important components of ter- community) reflect the plethora of life cycles represented restrial, freshwater and marine systems in the Arctic, by the different parasites and all the associated intermedi- these organisms have not often been included in general ate and definitive hosts. In this way parasites are indica- assessments of biodiversity at high latitudes (Marcogliese tive of food-web structure, trophic interactions, and 2001a, Hoberg et al. 2003, Kutz et al. 2009b, Gilg et al. biodiversity. … They thus reflect long-term persistence 2012). This situation may reflect the insularity or isola- and stable interactions in the environment.” tion that separates different disciplines of the biological sciences and until recently sporadic communications In northern systems, studies of parasite diversity di- among parasitologists, disease specialists and a broader rectly complement our knowledge about the historical community of ecologists, wildlife and fisheries biolo- processes that have served to determine the structure gists. Further, a sustained history for parasitological of faunas, and the role of episodic shifts in climate that studies in high latitude systems has been limited to have influenced dispersal, isolation and speciation during relatively few scientists in Europe, Russia and North the late Tertiary and Quaternary periods, approximately America over the past century. These factors have in- 3-3.5 million years ago to present (e.g. Rausch 1994, teracted to hinder both the development of information Hoberg et al. 2003, Cook et al. 2005, Hoberg 2005a, and the subsequent dissemination of knowledge to wider Zarlenga et al. 2006, Waltari et al. 2007a, Koehler et al. audiences beyond those working directly with parasites 2009). Contemporary diversity in aquatic and terrestrial and pathogens. environments has largely been determined by events that unfolded during the Pleistocene. For example, Climate change and associated ecological perturbations most groups of parasites now distributed in terrestrial are modifying the structure of terrestrial, freshwater mammals across the circumpolar region had origins in and marine systems across high latitudes of the North Eurasia and secondarily expanded into North America and globally (e.g. Callaghan et al. 2004a, Hoberg et al. during glacial stages coinciding with lowered sea-levels 2008b, Kutz et al. 2009a, Burrows et al. 2011). These that exposed the Bering Land Bridge, the primary path- changes have an effect on patterns of distribution, timing way linking Siberia and Alaska (Rausch 1994, Waltari et of migrations and seasonal development of vertebrates, al. 2007a, Hoberg et al. 2012). Alternating episodes of invertebrates and their parasites. Although we recognize rapid climate change from glacial to interglacial cycles and predict direct and indirect impacts to terrestrial, resulted in expansion, geographic isolation and diversi- freshwater and marine systems, parasites and associated fication in diverse host-parasite systems, both between disease have seldom been considered in the ‘equations’ Siberia and Alaska, and also within North America and for environmental change (e.g. Post et al. 2009, Gilg et Greenland (e.g. Stamford & Taylor 2004, Waltari et al. al. 2012). Parasites are critical components of these eco- 2007a, Shafer et al. 2010, Galbreath & Hoberg 2012). In systems, influencing the dynamics for host populations parallel to terrestrial and freshwater systems, patterns of and a range of interactions from competition to preda- diversity are also reflected in the history and distribution tion (Marcogliese 2001a, Bustnes & Galaktionov 2004, of parasite faunas in marine birds, mammals and fishes Kutz et al. 2009b). that were influenced by isolation or expansion between the North Atlantic and North Pacific basins through the Climate and environmental change are accelerating in Arctic Ocean and Bering Strait (e.g. Polyanski 1961a, northern ecosystems (Callaghan et al. 2004a, Gilg et al. Hoberg 1995, Hoberg & Adams 2000, Briggs 2003). 2012). These perturbations (particularly in patterns of These observations highlight the idea that the ‘past is the temperature in aquatic environments, and temperature Chapter 15 • Parasites 533 and humidity in terrestrial systems) have a direct influ- time series of biological collections and surveys at local ence on the occurrence of parasites and the potential to regional scales (e.g. Haukisalmi & Henttonen 1990, for emergence of diseases. Temperature, however, is 2000, Marcogliese 2001a). only one of a myriad of interacting biotic and abiotic mechanisms that directly and indirectly determine the distribution, abundance and potential impact of parasites 15.3. STATUS AND KNOWLEDGE (Marcogliese 2001a). Knowledge of parasite diversity in the Arctic expanded Cumulative (long term) processes and extreme (short in the 1800s coincidental with the earliest biological term) events influence the occurrence of parasites collections in Eurasia and North America. Studies were (Marcogliese 2001a, Hoberg et al. 2008a). Further, usually local and opportunistic, often with minimal atmospheric-oceanic oscillations (shifts between warm samples providing an incomplete glimpse of parasite and cold conditions over periods of months to years and diversity among vertebrate and invertebrate hosts in decades) on varying temporal and spatial scales can also terrestrial, freshwater and marine systems. A process of influence the structure of parasite and host communities discovery emphasized taxonomy and the identification and patterns of disease over broad geographic regions and characterization of diverse macroparasites (less often (Mouritsen & Poulin 2002a, Hoberg 2005b). microparasites), but usually in the absence of an ecosystem approach or historical and biogeographic context. Many northern parasites are adapted to cold environments and have short transmission windows. Long term A more comprehensive view of parasite diversity did processes such as 1 °C increases in global temperature can not emerge until the late 1940s and 1950s as cadres reduce generation times, increase developmental rates and of scientists began to systematically explore northern broaden seasonal windows for transmission. In contrast, environments. These studies may be best exemplified extreme weather events can result in the explosive emer- by the relatively comprehensive attempts to document gence of disease leading to morbidity and mortality at and characterize parasite diversity across Siberia and regional and local scales (Ytrehus et al. 2008, Laaksonen et the northern regions of the former Soviet Union. For ex- al. 2010a). Amplification of parasite populations respond- ample, the series of All Union Expeditions to such areas ing to either cumulative or extreme events may lead to as Kamchatka (317th) and Chukotka (318th) in the 1960s cascading effects within ecosystems, ultimately affecting provided the basis of our initial in-depth view of parasite biodiversity for both free-living and parasitic species (Kutz distributions among birds, mammals and some fishes in et al. 2005, 2009a, Galaktionov et al. 2006, Marcogliese these regions through examination of representative and 2008). Concurrently, northern range expansion for many large series of host specimens (e.g. Spassky et al. 1962, vertebrate species will create new opportunities for ex- 1963). These and other field surveys led to consider- posure of naïve host populations to an array of pathogens able knowledge about helminth parasite faunas circulat- (Brooks & Hoberg 2006, 2007, Reist et al. 2006, Lawler ing across tundra, nearshore and marine environments et al. 2009, De Bruyn 2010, Gilg et al. 2012). Interacting (Belogurov 1966) among shorebirds (Scolopacidae and with overall habitat change and other biotic and abiotic Charadriidae) (e.g. Belopol’skaya 1953, 1980, Bondar- variables, disease is one outcome that can directly influ- enko & Kontrimavichus 1999) and in marine birds such ence the availability of food resources on which northern as auks, gulls and seaducks (Belopol’skaya 1952, Galak- communities depend. The role of anthropogenic introduc- tionov 1996a), which collectively dominate avian diversi- tion, establishment and invasion of parasites into the north ty at high latitudes. These further served as the basis for also cannot be discounted given the degree of globaliza- comprehensive monographs exploring parasite diversity tion and connectivity that now influences the distribution in avian, mammalian and piscine taxa, particularly in the of free-ranging and domestic animals and their pathogens Russian literature (e.g. Bykhovskaya-Pavlovskaya et al. (e.g. Hoberg 2010). 1962, Spasskaya & Spassky 1977, 1978, Ryzhikov et al. 1978). In Alaska at this time, studies of parasite faunas, Consequently, parasites must be explored in the context of principally among mammals and birds, were driven by 1. ecosystem function, stability and sustainability, Robert L. Rausch and his colleagues and presented in a 2. emerging pathogens that may directly influence sub- long series of papers in Studies on the Helminth Fauna of sistence foodwebs and food security at high latitudes Alaska. For the most part, however, multi-taxon surveys under a regime of environmental perturbation, and that were both geographically extensive and site inten- 3. potentially threatened components of northern sys- sive were without counterpart in either northern Eurasia tems that may lack a capacity for adaptation to shifting or North America until the current era of biodiversity environmental conditions, or may be eliminated inventory (Cook et al. 2005). through competition with new invaders (e.g. Kutz et al. 2004, 2009a, Tryland et al. 2009, Laaksonen et al. Coincidental with expanding interest in wildlife para- 2010a). sites, the implications of pathogens and disease for people were receiving attention (e.g. Rausch 1972, 1974). This Ecosystem assessments and the role of complex inter- focus began to examine the interaction between indig- acting factors which may influence patterns of host and enous peoples, subsistence food chains and the cultural parasite abundance can only be explored through long- aspects of parasite transmission and disease (e.g. Rausch 534 Arctic Biodiversity Assessment

1951, Babbot et al. 1961, Cameron & Choquette 1963). Bering Sea and Sea of Okhotsk (e.g. Belopol’skaya 1952, The role of humans in introductions and dissemination Threlfall 1971, Hoberg 1992, 1996, Galaktionov 1996a, of parasites was revealed by the metazoan and protozoan 1996b, Muzzafar 2009). Some of these large collections faunas demonstrated on Iceland (Skirnisson et al. 2003). provide the opportunity for direct comparisons of ecological conditions that characterized systems 30-50 Classical and elegant research in parasitology conducted years ago, relative to contemporary environments, and at high latitudes has emphasized parasites transmissible thus can reflect the results of accelerated perturbation to people (e.g. Rausch 1967, 1974, 2003), however, over time. Parasites are particularly sensitive indicators much remains to be revealed about the extremely diverse of ecological conditions, migration pathways and habitat world of parasitic organisms. For example, new species use because their transmission is often directly linked and genera of macroparasites continue to be discovered to the food habits and foraging behaviour of hosts (e.g. across the circumpolar region. These include assem- Dogiel 1964, Hoberg 1996, 1997, Marcogliese 2001a, blages of tapeworms in such reasonably well studied host Muzzafar 2009). groups as arvicoline rodents (voles and lemmings) (e.g. Rausch 1952, Haukisalmi et al. 2001, 2002, 2006, 2009, Similar inventories, however, are reasonably rare across Wickström et al. 2003, Cook et al. 2005, Makarikov Arctic latitudes. Essentially there are few comprehensive et al. 2011). Additionally, among ungulates including historical baselines (derived from comparable sampling muskoxen Ovibos moschatus, moose Alces americanus and standards) against which to measure trends for changing caribou Rangifer tarandus, new stomach and lungworms patterns of distribution, host associations or numerical are being identified and described (e.g. Hoberg et al. occurrence of most parasites (and diseases) in free-rang- 1995, 1999, Kutz et al. 2007, Laaksonen et al. 2010b). ing and domestic animals or in people (Appendix 15.1). Substantial new information about host and geographic Indeed, we continue to have an incomplete picture of distribution has also emerged reflecting recent programs diversity, host associations and distribution for parasites for parasitological surveillance and monitoring in terres- in vertebrates and invertebrates in northern regions. trial systems (e.g. Kutz et al. 2001b, Hoberg et al. 2002, Faunal checklists can be assembled from a distributed 2008b, Jenkins et al. 2005, Laaksonen 2010, Laaksonen literature for parasites in many species of fishes, birds et al. 2010a). These studies have demonstrated the need and mammals, but these are not always appropriate as for broad integrated approaches which increasingly rely temporal and spatial baselines. Further, there is relative- on both comparative morphological and molecular data ly little ongoing survey-based collecting that will allow to understand patterns of cryptic parasite diversity (re- direct comparisons with the contemporary historical lated species of parasites that cannot be easily identified records that document faunal structure during the past based on morphology) in the North (Hoberg et al. 2003, 30-50 years, which now appears to be a critical period Haukisalmi et al. 2009, Pérez-Ponce de León & Nadler with respect to environmental perturbation in northern 2010). Accurate documentation of diversity (the spe- systems. This situation heightens the need for active col- cies of parasites, how they are related, which hosts they laborations among field biologists, including parasitolo- infect, where they occur geographically and measures of gists, vertebrate biologists, wildlife disease specialists numerical abundance and population genetic diversity) and local communities. are the foundations for understanding and recognizing changing patterns of distribution and the emergence of disease. Further, different species of parasites behave 15.4. ECOSYSTEM COMPONENTS IN in a variety of ways relative to hosts and environmental settings, thus clear definitions of diversity provide THE NORTH important information for predicting the outcomes of environmental change in these systems (e.g. Marcogliese Assemblages of microparasites and macroparasites are 2001a, Albon et al. 2002, Kutz et al. 2012). associated with vertebrate host groups in terrestrial, freshwater and marine systems across the circumpolar Large scale or synoptic biological collections linked to North. Diversity and abundance of parasites is parti- assessments of ecology, biogeography and phylogeogra- tioned among the approximately 200 species of birds phy in some regional settings such as Beringia (the cross- numbering more than 100 million individuals, 100 roads of the northern continents linking North America species of mammals and respectively about 127 (incl. the and Eurasia) have been ongoing over the past decade (e.g. sub-Arctic) and 250 species of fishes in freshwater and Hoberg et al. 2003, Cook et al. 2005). Additionally, dur- marine systems in the Arctic (Callaghan et al. 2004b, ing the International Polar Year (2007-2008) a broad- Reist et al. 2006, Mecklenberg et al. 2011, Ganter & based and standardized project exploring health of rein- Gaston, Chapter 4, Christiansen & Reist, Chapter 6, deer and caribou was initiated under the CircumArctic Hodkinson, Chapter 7). In addition, a considerable array Rangifer Monitoring & Assessment Network (CARMA). of invertebrates (among approximately 4,750 species in In contrast to terrestrial systems, time sensitive inven- terrestrial and freshwater habitats, and 5,000 in marine tories and baselines for parasites in marine birds (pri- environments) may serve as intermediate hosts. As a marily auks, gulls and some waterfowl) have resulted generality, species richness for macroparasites declines from collections in the Arctic Ocean (White Sea), the on a gradient from south to north in terrestrial (Hoberg region adjacent to Greenland and in the North Pacific/ et al. 2012), freshwater (Belopol’skaya 1959, Shulman Chapter 15 • Parasites 535

1961) and marine (Delyamure 1955, Table 15.1. Characteristics of Arctic host-parasite systems. Polyanski 1961a, Rohde 2005) environments, although exceptions are Biological characteristics: strongly influenced by Arctic environments apparent for some host and parasite Relatively low diversity; abundance and diversity for parasites are correlated with that for the host group. Levels of species richness and diversity in high latitude systems are substantially groups that attain maximum diversity lower relative to temperate and boreal zones. This appears to be a generality across parasite and abundance at high latitudes. This faunas in fishes, birds and mammals. trend reflects an interaction of histori- Domination by limited number of taxonomic groups that may occur at high levels of abun- cal processes, ecosystem structure, dance. host-group diversity, and patterns of Numerous migratory host species and populations; avian species with long distance migration distribution, abundance and density in terrestrial, freshwater and marine environments; some mammals particularly caribou, oc- for vertebrates (and invertebrate prey casionally lemmings, some marine mammals; anadromus and diadromus fishes. and vectors) on landscape to regional Often high density aggregations of hosts during breeding season (e.g. colonially nesting birds) scales. Migration further influences and some through the year (e.g. caribou), influencing parasite abundance and transmission. patterns of diversity, and this is mani- Some species fluctuate in abundance on annual or longer cycles; includes vertebrate host spe- fested at varying spatial scales from cies and invertebrate vectors. landscape for rodents, to regional for Extreme seasonality in distribution and abundance; brief pulses of primary/secondary produc- some ungulates, and intercontinental tivity; prolonged winter. for some birds. For example, among Short trophic links; synchronicity in production cycles, occurrence of susceptible hosts, narrow the helminth faunas associated with transmission windows. charadriiform shorebirds, species of Diversity influenced strongly by secondary productivity; shifting abundance for invertebrate parasites may be partitioned on winter- intermediate hosts and vectors. ing or breeding grounds or on migra- Diversity partitioned on spatial patterns reflecting local to regional conditions. tion corridors that extend from the Arctic deep into the Southern Hemi- Historical characteristics influencing diversity sphere (e.g. Belopol’skaya 1953, 1959, Episodic climate change and habitat perturbation coinciding with glacial/interglacial cycles. 1963, Dogiel 1964). Thus, northern Recurrent (episodic) expansion (geographic colonization/range shifts), isolation, fragmentation parasite faunas are characterized by of host/parasite populations. low diversity and are to some degree Spatial heterogeneity; mosaics of suitable habitat for species persistence, driving speciation constrained by biotic and abiotic mech- and distribution of cryptic species. anisms that define species occurrences Refugial effects; residual isolation related to vagility (ability to disperse and velocity of disper- and associations (Tab. 15.1). sal). Complex patterns of species overlap (sympatry) and patterns of parasite exchange (host In a simplistic sense, the biogeography switching) among respective groups. and evolution of circumpolar assem- Prominent biotic filters; constraints leading to loss of diversity due to limited resilience/toler- blages of hosts and parasites reflects ances/thresholds for development and survival in ephemeral, cold and xeric environments. a history of recurrent climatologi- Prominent abiotic filters; constraints related to temperature, precipitation and humidity (ter- cal and environmental perturbation restrial); temperature, ice cover, salinity, water flow and availability, circulation, UV exposure, extending over the past 3-3.5 million etc. (aquatic). years. The history is one of episodic geographic expansion (and contraction) Adaptations in Arctic parasite systems in the ranges for vertebrate hosts and Rapid development of larval-infective stages tied to seasonality (response to ephemeral parasites. The processes have directly conditions). determined patterns of geographic in- Prolonged development tied to sitting and waiting for suitable conditions (multi-year cycles); vasion, and the potential that parasites timing of development and dispersion of larval infective stages often reflects seasonal abun- have periodically colonized new host dance of definitive hosts (migratory marine birds and shorebirds); responses to temperature species or host groups (e.g. Kontrima- with developmental thresholds and tolerances also linked to ephemeral conditions. vichus 1969, Hoberg & Adams 2000, Continuous transmission through all seasons, reduced arrested development (ungulate Hoberg et al. 2012). The important nematodes). implication here is that mechanisms Resilience of eggs/larvae to adverse environmental conditions. that have historically served to deter- Synchronicity in larval availability/infectivity coinciding with vulnerable spectrum of host mine parasite diversity are equivalent population (e.g. nestling and fledgling birds; young of the year ungulates; pre-migratory to those processes in ecological time salmonids). that involve invasion, breakdown of Long life span as adult parasites, large size, high fecundity; multi-year infections; broad ecological isolation and shifts in distri- dissemination of larval stages in environment (e.g. lungworms and some gastrointestinal bution for parasites and host-parasite nematodes in ungulates). assemblages (Hoberg & Brooks 2010). Short life span as adults, rapid development, small size, great abundance, but low fecundity; Northern host-parasite assemblages absence of free-living larval stages; prolonged survival in intermediate hosts (e.g. trematodes including species of Microphallus and Gymnophallus and cestodes such as Microsomacanthus have origins and have diversified in in charadriiform shorebirds, gulls and waterfowl). a crucible defined by environmental Geographically partitioned faunas; specific wintering and breeding/nesting ground parasite change on evolutionary and ecological faunas in migratory birds. scales (Hoberg & Brooks 2008). 536 Arctic Biodiversity Assessment

A history of ecological perturbation and faunal inter- could not successfully colonize high latitudes, or which change is an underlying theme as we summarize obser- were secondarily eliminated historically through local vations for a limited number of exemplars representing or regional extinction associated with rapid climate each of these systems. Our focus necessarily involves and environmental change. Beyond these longitudinal host groups of some importance in subsistence and patterns, a latitudinal gradient has been secondarily those which may be significant for circulation of some superimposed, which is consistent with north-south zoonotic organisms. The exemplars also are indicative of and south-north expansion, isolation and diversification the patchy nature of the data available for host-parasite particularly in North America during the Pleistocene systems at high latitudes where comparable sampling and Holocene (Galbreath & Hoberg 2012). Patterns of regimes are generally not available for all vertebrates diversity also reflect a mosaic structure resulting from throughout the circumpolar zone. Notably many records recurrent episodes of geographic colonization by hosts for the occurrence of parasites in fishes, birds or mam- and parasites at intercontinental, regional and landscape mals relate only to the original description, and thus our scales over extended time frames. Mosaics are complex context for understanding broader distributions is often admixtures of species and populations that result from limited. Unlike free-living fishes, birds and mammals, invasion and faunal interchange, both general phenomena parasites are inherently more difficult to count and are in evolutionary and ecological time (Hoberg et al. 2012). not easily amenable to annual census activities that may Collectively, diversity gradients and mosaics provide a define trends in populations for vertebrates. Further, not context to understand contemporary distributions for all Arctic vertebrates and free-living invertebrates have many parasite assemblages and the possible outcomes of been extensively surveyed for parasites, and this gap in natural and anthropogenic disturbance in northern ter- knowledge suggests that we still do not recognize some restrial systems, and may have broader generality. systems that may be particularly important indicators of environmental change in the North. Emphasis on a series 15.5.1.1. Ungulates of keystone species in respective ecosystems, however, serves to clearly demonstrate the substantial importance Ungulates, including caribou and reindeer are keystones of parasites in the Arctic and highlights the need for of terrestrial ecosystems throughout the Arctic, and are more comprehensive surveys. the core of subsistence food chains in many regions (e.g. Vors & Boyce 2009). Nematode parasites are a common and dominant group among ungulates across high 15.5. TERRESTRIAL ECOSYSTEMS latitude systems, occurring in the gastrointestinal system (e.g. Halvorsen & Bye 1999, Hoberg et al. 2001, Albon As mentioned above, terrestrial host-parasite systems at et al. 2002, Kutz et al. 2004, 2012) or in pulmonary high latitudes are characterized by low diversity (species (lungs) and extrapulmonary sites (musculature, thoracic, richness) relative to those in the boreal and temperate abdominal, peritoneal sites) of their hosts (e.g. Lank- zones, consistent over all with a latitudinal gradient that ester 2001, Hoberg et al. 2002, Laaksonen et al. 2010a, to some degree coincides with patterns of species-rich- 2010b). Among these, the protostrongylids and filarioids ness and abundance for vertebrate hosts (Callaghan et al. may be most sensitive to climate change (e.g. Kutz et 2004a). Due to differences in vagility, some mammalian al. 2001a, 2005, Laaksonen et al. 2010a). These para- parasite faunas appear to be more strongly partitioned sites interact with an array of factors including weather geographically than those among avian hosts. Latitude, events, contaminants and human disturbance that alone however, is only one component that serves to deter- or in concert directly influence ungulate biology (Gunn mine general patterns of parasite distribution. & Irvine 2003, Kutz et al. 2004, 2012). Consequently, development of new baselines for distribution and abun- 15.5.1. Mammals dance (and a capacity to predict and monitor changes in abundance) can contribute directly to a more robust un- Across terrestrial habitats in the Arctic there are about derstanding of health and sustainability among ungulate 65 species of terrestrial mammals (Reid et al., Chapter populations. 3). Diversity of parasite faunas in terrestrial systems, particularly among mammals, is a legacy of recurrent Protostrongylidae is a prominent family of nematodes or episodic expansion during the Pliocene and Pleisto- common in ungulates across the circumpolar region cene from Eurasian areas of origin, eastward into North (Boev 1975). Life cycles are complex involving adult America (Waltari et al. 2007a, Hoberg et al. 2012). As a nematodes in ungulates and infective larvae in gastro- consequence of geographic expansion, however, longi- pod (slugs or snails) intermediate hosts (e.g. Kutz et al. tudinal and latitudinal gradients in diversity appear to 2001a). Development of larvae is temperature depend- be a further generality for many helminth groups among ent occurring more rapidly under warmer conditions up ungulates, rodents, carnivores and lagomorphs. Species to a threshold of 21 °C. For example, research on the richness within respective helminth groups is greatest lungworm Umingmakstrongylus pallikuukensis of muskoxen in Eurasia, lesser in North America, and minimal in the produced models suggesting that climate warming Arctic; or alternatively there is a gradient with a gap in northern Canada has resulted in a shift (or tipping at high latitudes (Appendix 15.2). The gap of mini- point) for the transmission of this parasite from a two mal diversity represents those parasite groups which to a one year life cycle (Kutz et al. 2005). Concurrently, Chapter 15 • Parasites 537 the total number of larvae available to infect muskoxen ranges, specific host associations, prevalence of infection increased under these warming conditions, contributing and identity of the species remain poorly resolved. In to heightened infection pressure and parasite abundance. light of the significant disease associated with filarioids Further, apparent geographic expansion for this lung- in Fennoscandia, and recent anecdotal reports in Alaska worm north from the central mainland onto the Arctic of individual cases of disease (K. Beckmen, pers. com.), islands has been demonstrated by recent field collections these may be parasites of special interest that warrant of muskoxen (S.J. Kutz, M. Dumond & E.P. Hoberg, enhanced surveillance under current conditions of cli- unpubl. data). These interacting factors for rapid parasite mate warming. development, increasing levels of infection and changing geographic distribution are those often associated with Among tissue dwelling and pulmonary nematodes it emergence of disease driven by parasites in ungulate appears that infections are often cumulative with age of populations (Kutz et al. 2012). hosts, and lifespan for individual worms may extend over periods of years (Bylund et al. 1981, Hoberg et al. 1995). Other protostrongylid species are expected to be af- Both of these factors have implications for dissemina- fected in a similar manner under a regime of accelerated tion, invasion (colonization of new geographic areas) and warming and environmental change (Jenkins et al. 2006, emergence of disease (Hoberg 2010, Kutz et al. 2012). Hoberg et al. 2008a). For example, during unusually Development of parasitic stages in the intermediate hosts warm years in Norway, severe outbreaks of disease asso- or vectors is also strongly defined seasonally and by ciated with the protostrongylid Elaphostrongylus rangiferi temperature (Bylund et al. 1981, Handeland & Slettbakk were seen in reindeer (Handeland & Slettbakk 1994). 1994, Kutz et al. 2005, Laaksonen et al. 2010a). The Detailed empirical data and model-based research has widespread distribution of both pulmonary and gastro- not been done on the majority of the other protostron- intestinal nematodes in conjunction with patterns of life gylids, but the influence of climate, and both cumula- history indicates the potential for considerable effects on tive and extreme events, on patterns of distribution and host populations through mortality and reduced fecun- emergence are readily apparent (Hoberg et al. 2008a). dity (Albon et al. 2002, Gunn & Irvine 2003, Hoberg et al. 2008a, Kutz et al. 2009a, 2012, Laaksonen et al. Despite the fact that protostrongylids are common and 2010a). The role of parasites at the ecosystem and re- pathogenic parasites found in keystone ungulates, and gional level, however, including the widespread declines are among the best studied parasites of large mammals, in populations of Barren Ground caribou (Vors & Boyce considerable knowledge gaps remain about their diver- 2009) has not been explored. Significantly, heightened sity and ecology in the Arctic. This was exemplified by thermal stress for muskoxen and caribou (Ytrehus et al. the original discovery of Umingmakstrongylus in the late 2008, Campos et al. 2010) will coincide with conditions 1980s (Hoberg et al. 1995) and most recently by recog- of increasing temperature and humidity that are suitable nition of an apparently new species of protostrongylid, for rapid amplification of parasite populations linked to based on DNA sequences of larvae, in caribou, moose reductions in development time for larval stages (e.g. and muskoxen across the North American Arctic (Kutz Hoberg et al. 2008b). Thus, trends for expansion of et al. 2007). Adults of this previously unknown lung- parasite populations (abundance and infection pressure), worm were collected for the first time in 2010, and are increasingly coincidental with adverse thermal condi- under evaluation (G. Verocai, S.J. Kutz & E.P. Hoberg, tions for hosts represent opposing trajectories where unpubl. data). synergy between these feedback loops ultimately may pose threats to continuity for populations of muskoxen at Filarioid nematodes in ungulates across the Holarctic landscape to regional scales. include species of Setaria, Onchocerca and Rumenfilaria. In contrast to protostrongylids, these parasites are all trans- A primary management implication of parasites among mitted by biting flies (mosquitoes and black flies) (e.g. ungulates may be the northward expansion of free Bylund et al. 1981, Nikander et al. 2006). In Fennoscan- ranging species in otherwise natural ecosystems and dia, Setaria tundra is associated with outbreaks of disease of domestic stock in agricultural systems, both lead- and substantial mortality events in reindeer and Eurasian ing to eventual encroachment on Arctic environments elk Alces alces, and is a direct threat to sustainability and (Hoberg et al. 2008a, 2008b, Kutz et al. 2009a, 2012). food security (Laaksonen 2010, Laaksonen et al. 2010a); Translocations, introductions and ongoing expansion of Rumenilaria andersoni was only recently documented in free ranging species including reindeer and muskoxen Finnish populations of reindeer (Laaksonen et al. 2010b), may already have influenced parasite distribution across and although it may be geographically widespread at high the Arctic (e.g. Hoberg et al. 1999, Hoberg et al. 2002). latitudes of North America, accurate data for distribu- Thus, a process to identify environmental and manage- tion are lacking (Kutz et al. 2012). Emergence of disease ment factors that may enhance (or reduce) transmission attributable to S. tundra is driven directly by climate of parasites and diseases is needed. Knowledge of para- and short-term events of extreme weather (summer site diversity provides a measure for understanding the temperatures averaging above 14 °C in two consecutive drivers for emergence of disease and predictive power years and apparently in conjunction with high humid- that can contribute to management decisions (e.g. Laak- ity). In North America, these parasites are known to sonen et al. 2010a). In this manner, parasites are integral be present among caribou and moose, but geographic to understanding faunal diversity across Arctic systems. 538 Arctic Biodiversity Assessment

15.5.1.2. Rodents six species at Kilpisjärvi (M. glareolus and M. schisticolor Rodents are abundant components of circumpolar eco- are absent), providing a powerful framework for com- systems, and at high latitudes the fauna is dominated by parative parasitological studies. Although all host species the arvicolines (voles and lemmings) which overall has have been studied for helminths since the late 1970s, 28 genera and 151 species in the Northern Hemisphere; efforts for extended time series have focused on M. with eight genera and approximately 20 species restricted glareolus at Pallasjärvi, a key indicator species in western to the Arctic (Reid et al., Chapter 3). Species of Arvicola, Eurasian boreal zone (Haukisalmi & Henttonen 1990). Myodes, Microtus, Dicrostonyx, Lemmus and Synaptomys are Deep time-series data from M. glareolus have been the typical of this fauna. Rodents are of critical importance basis for assessing patterns of seasonal and long-term in Arctic ecosystems as the dynamics and occurrence of population dynamics of cestodes and nematodes, with both avian and mammalian predators are often linked particular reference to varying strategies of ‘common’ to the cyclical abundance of lemmings and voles (Cal- and ‘rare’ species (Haukisalmi & Henttonen 2000). laghan et al. 2004a). Voles and lemmings serve as both intermediate and definitive hosts for a diverse assemblage Annual and seasonal monitoring has revealed, for of macroparasites and microparasites (e.g. Rausch 1952, example, that the populations of ‘common’ helminths Gubanov & Fedorov 1970, Egorova & Nadtochii 1975, of Myodes glareolus are regulated interactively with host Ryzhikov et al. 1978, 1979, Shakhmatova & Yudina density (with a lag) and in conjunction with climatic 1989, Yushkov 1995, Haukisalmi & Henttonen 2000, factors, particularly precipitation (Haukisalmi & Hent- Laakkonen et al. 2002). For macroparasites, distinct tonen 1990). Because the trapping sites at Pallasjärvi are latitudinal and longitudinal gradients for species rich- situated in all main habitat types (with replicates), it has ness are apparent (Hoberg et al. 2012) (Appendix 15.2). been possible to study certain spatial aspects of helminth Helminth parasites in voles and lemmings are indicators ecology as well. One of the most interesting findings of historical and ecological connections in circumpolar is that some of the ‘rare’ species occur predictably in environments (reviewed in Hoberg et al. 2012). Predator- certain spatially limited, temporally persistent ‘foci’ prey cycles for helminths that are mediated through voles (Haukisalmi & Henttonen 1999). Additionally, they and lemmings are also the basis for circulation of some occur almost exclusively in old, overwintered (soon- zoonotic tapeworms, including the taeniid, Echinococ- to-die) animals, particularly females in mid and late cus multilocularis, which is the causative agent of alveolar summer (Haukisalmi & Henttonen 2000). Without this hydatid disease in people (Rausch 1967, 1995, Shakhma- knowledge, they would easily be missed in normal short- tova & Yudina 1989, Yushkov 1995). The biogeographic term surveys. Of further significance, the composition history and contemporary dynamics of vole and lemming of rodent communities has undergone rather dramatic populations thus strongly influence the distribution of changes (besides lemming peaks) during recent decades, complex parasite faunas in northern environments. with faunal turnover and replacement over periods of years (H. Henttonen, unpubl. data). Such perturbations Parasite distribution in arvicolines depends on internal have not had any noticeable effects on helminth faunal host factors, particularly immunity, and permissive envi- diversity, and parasite assemblages have to some degree ronments where conditions of temperature and humidity been maintained continuously with little modification. are suitable for development and survival of infective An exception to this trend may be represented by the stages (Callaghan et al. 2004a). Factors of climate and appearance of a single nematode species (the heligmo- weather further act as determinants of distribution and some, Carolinensis minutus) associated with Microtus agrestis abundance of invertebrates such as soil mites, insects at Pallasjärvi (V. Hauksalmi & H. Henttonen, unpubl. and gastropods that serve as intermediate hosts and are data). Such data would be hard to gather without prop- essential for transmission. Aside from intrinsic host erly designed long-term monitoring. Although these factors, the timing of precipitation in early summer was studies in Finnish Lapland are rare in the Arctic, they shown to be most critical in influencing the prevalence should nonetheless be a model for exploring the dynam- of infection for tapeworms and nematodes infecting ics of host-parasite systems in small mammals at multiple Myodes voles in sub-Arctic Finnish Lapland (Haukisalmi sites throughout the Arctic. & Henttonen 1990). A consequence of climate warming may be fragmenta- As an example of the dynamics of rodent-parasite tion of rodent populations through interactions with systems, these observations emerged from two long- expanding ranges for arvicolines, other rodents, and term programs for monitoring of host populations in their parasites from the south (Callaghan et al. 2004a). northern Finland, at Pallasjärvi in the north boreal The dynamics for these processes may be complex, zone and Kilpisjärvi in the sub-Arctic zone that respec- with patterns of local extinction, faunal mixing through tively extend to 1970 and 1946. Arvicoline diversity in geographic colonization and potential host switching these areas is high, eight species occurring at Pallasjärvi by parasites. In this regard, ecological perturbation has (European water vole Arvicola amphibious, Norway lem- been among the primary mechanisms driving changes in ming Lemmus lemmus, bank vole Myodes glareolus, gray faunal structure and species richness in these northern red-backed vole M. rufocanus and northern red-backed faunas (reviewed in Hoberg et al. 2012). In both evolu- voleM. rutilus, wood lemming Myopus schtisticolor, field tionary and ecological time, phylogeographic structure, vole Microtus agrestis and tundra vole M. oeconomus) and including patterns of cryptic speciation for macropara- Chapter 15 • Parasites 539 sites, has resulted from episodes of range expansion and tebrate prey species. Thus, patterns of abundance and contraction; such structure is often evident for parasites diversity for potential prey can strongly influence the even when not reflected in the history for particular host distribution and composition of helminth faunas. groups or species. As an example of diversity, the parasite faunas of rock Extensive collections from long term monitoring at ptarmigan Lagopus muta include 40 species of micro- various localities has served to confirm the outcomes parasites and macroparasites globally. In Iceland, these of environmental perturbation during the late Pleisto- are represented by 16 species of endo- and ectoparasites cene, particularly glaciations and post-glacial expansion, which contrasts with 21 and 26 found in the Nearctic on the distributions of some parasites (Haukisalmi & and Palearctic, respectively (Skirnisson et al. 2012). A Henttonen 2001). For example, we have been able to notable absence in Iceland is digenean flukes that require confirm that some of the otherwise ubiquitous helminths molluscan intermediate hosts for transmission and hae- are missing in Fennoscandia. Throughout the Holarctic, matozoans that require blood-feeding Culicoides midges. species of Lemmus have four main helminths (species or a Reduced diversity appears to have been further influ- group of closely related species): Arostrilepis spp., Paranop- enced by founder events related to the original coloniz- locephala fellmani and related species, Anoplocephaloides ers of Iceland from Greenland (Skirnisson et al. 2012). lemmi (actually two species) and Heligmosomoides spp. (probably two species). Of these, only P. fellmani occurs Currently, haematozoan parasites of birds appear to be in the Norway lemming in Fennoscandia; Arostrilepis is virtually absent from high latitude (tundra) habitats, also absent in other Fennoscandian rodents. In contrast, although sampling has been relatively minimal (e.g. Ben- cestodes of the genus Arostrilepis are known in arvicolines nett et al. 1992). Their absence has been attributed pri- (Arvicola, Dicrostonyx, Lemmus, Microtus and Myodes) in the marily to the paucity of appropriate arthropod vectors region immediately adjacent to Fennoscandia including and suitable environmental factors that are necessary Karelia, and European Russia (Mozgovoi et al. 1966, for transmission. Although most avian hosts are migra- Yushkov 1995). tory, seasonal arrival on the nesting grounds does not appear to be commonly associated with establishment Faunal mixing, range shifts and establishment of parasite and dissemination of vector-borne parasites in the Arctic populations are also potentially influenced by human region. In the Canadian Arctic, it appears that haema- activities in the Arctic. For example, introductions of tozoans are mostly restricted to areas on the periphery the sibling vole Microtus levis to Svalbard facilitated the of forest and forest-tundra habitats, and are less abun- establishment of Echinococcus multilocularis for the first dant or absent to the north. The genus Leucocytzoon is time in the archipelago (Henttonen et al. 2001). Al- an exception (Simulidae, or black-fly vectors), however, though the tapeworm may have been present in transient and the species L. simondi may be particularly abundant Arctic fox Vulpes lagopus, it had not become established extending into the Arctic and substantially north of due to the absence of a primary arvicoline intermediate the tree-line (Valki uˉ n as 1997). Latitudinal shifts in the host. This example demonstrates that the distribution of treeline may lead to northward expansion and concomi- this tapeworm is likely limited by that of its required in- tant changes in abundance and density of blood-feeding termediate hosts, rather than extensive ranges occupied blackflies and other dipterans that are recognized vec- by highly vagile foxes that disperse over considerable tors. Such climate-mediated shifts in habitat structure distances in the Arctic. Thus, changing abundance and may promote invasion and dissemination of these proto- distribution of voles and lemmings may contribute to a zoans, which are a common component of avian parasite broadened range for this zoonotic taeniid. faunas and often significant pathogens at temperate to boreal latitudes (Bennett et al. 1982, Valki uˉ n as 1997). 15.5.2. Terrestrial birds Loss of habitat and habitat restrictions, shifts from Birds that occupy predominantly terrestrial habitats tundra to forest habitats and structural changes related year round are poorly represented in the Arctic. They to productivity are expected to influence the distribu- include limited numbers of passerines, birds of prey, tion of parasites at all geographic scales. Ongoing shifts owls and grouses, all of which constitute groups that are in species distributions of avian hosts may be predicted widespread in the Northern Hemisphere (Callaghan et to influence the ranges occupied by various host-parasite al. 2004b, Ganter & Gaston, Chapter 4). Most of these assemblages with the consequent development of new species are short range migrants, with occurrences in faunal associations through geographic and host coloniza- the Arctic limited to relatively narrow seasonal windows tion (e.g. Callaghan et al. 2004c, Lawler et al. 2009). during the summer breeding season. Consequently, the affinities of parasite faunas in the assemblage of landbirds are strongly tied to boreal and temperate environments. 15.6. FRESHWATER ECOSYSTEMS Helminth faunas for raptors are usually linked to the cyclic abundance of lemming populations and transmission Vertebrate faunas associated with freshwater environ- pathways involving carnivory. In contrast, the faunas ments in the Arctic are dominated by birds and fishes, circulating among other landbirds involve both direct with relatively few mammals restricted to these habitats transmission and indirect cycles using various inver- (e.g. Callaghan et al. 2004b, Wrona et al. 2006, Ganter 540 Arctic Biodiversity Assessment

& Gaston, Chapter 4, Wrona & Reist, Chapter 13). switching leading to a broadened array of species infect- Parasites in birds and fishes are represented by diverse ed. Such faunal modifications can come about through assemblages of protozoans and helminths (and other anthropogenic mechanisms (e.g. fisheries management, macroparasites), with the latter often cycling through introductions and hatcheries) (e.g. Petrushevski 1961) aquatic invertebrates including insects, annelids and or through expansion driven by either natural events or molluscs. Overall, freshwater systems are highly sensi- those facilitated through external environmental factors tive to water levels, ice cover, flow rates and changing (e.g. Marcogliese 2001a). An example of the former is patterns of primary and secondary productivity that the continuing invasion of the monogenean fluke, Gyro- influence ecosystem structure and potential prey diver- dactylus salaris, in populations of Atlantic salmon Salmo sity and abundance for both fishes and birds (Marcogliese salar from northern Norway (Johnsen & Jensen 1991). 2001a, Ganter & Gaston, Chapter 4). These factors In contrast, changing water conditions (increasing are central to the continuity of parasite life cycles and temperature) in the Yukon River, Alaska and adjacent potential for transmission. Climate change in freshwater Bering Sea have been implicated in the emergence of the systems may be manifested by a number of interacting protozoan Ichthyophonus in Chinook salmon Onchorhynchus factors (Schindler & Smol 2006) of relevance for parasite tshawytscha (Kocan et al. 2004). diversity among both birds and fishes: 1. shifts in development for invertebrates that involve Pacific salmon Onchorhynchus spp. are keystone species tipping points or transitions in life history from involved in nutrient cycling and transport across ecosys- multi-year to single year (e.g. steps of entire years, not tem boundaries, with particular importance in ripar- weeks and months), ian habitats (Gende et al. 2002, Naimann et al. 2002). 2. loss of cold-water refugia leading to extirpation of They are also critical in commercial and subsistence fishes when tolerances and resilience are exceeded, fisheries. Disruption of salmon populations by natural 3. changing distribution of wetland habitats, and anthropogenic drivers can have substantial cascad- 4. northward extension of the ranges for many inverte- ing effects in aquatic and adjacent terrestrial systems. brate species, and In this regard, Ichthyophonus spp., poorly understood 5. higher diversity for fish and invertebrate faunas. protozoan parasites that infect marine and anadromous fishes across the Holarctic, may be of particular concern 15.6.1. Fishes (Kahler et al. 2007). Ichthyophonus hoferi, a pathogen of Chinook salmon from the Yukon River drainage of Arctic and sub-Arctic freshwater systems support ap- North America, has rapidly emerged over the past 30 proximately 127 species of fishes including some spe- years (Kocan et al. 2004, Zuray et al. 2012). Substantial cies complexes, notably among the char and whitefishes pre-spawn mortality for adult fish poses serious implica- (Christiansen & Reist, Chapter 6). The fauna is domi- tions for subsistence and commercial fisheries and can nated to some degree by diadromous species primarily ultimately limit the sustainability of salmon populations salmon and whitefishes that move between freshwater in the Yukon system (Kocan et al. 2004). Further, the and marine environments; cyprinids (minnows) are also parasite directly affects palatability and suitability of speciose whereas the fauna includes limited numbers of infected salmon as food. The presence of Ichthyophonus in sticklebacks, sculpins, perches and other fishes. Parasite the Yukon reflects either a relatively recent introduction faunas include species of microparasites and macro- or invasion or emergence of an endemic pathogen driven parasites that circulate solely in freshwater, in addition by changing environmental regimes in the Bering Sea. to those that are disseminated through dispersal from The origins of this parasite in salmon remain obscure, adjacent coastal seas and involve fishes as both definitive although genetic data suggest a shift from other fish spe- and intermediate hosts (Shulman 1961, Bykhovskaia-Pav- cies in the marine or aquatic environment (e.g. Pacific lovskaya et al. 1962). In the circumpolar region of Russia herring Clupea pallasi) with potential amplification in the (either Arctic Russia or the Russian north, dependent Yukon system being linked to increasing water tempera- on the extent beyond the strict definition of the Arctic tures (Criscione et al. 2002). Cascading effects of this in our report) in excess of 222-300 species of protozans, pathogen in the Yukon ecosystem may be substantial, helminths, crustaceans and other parasites have been particularly if parasites cause significant fish mortality, documented in freshwater habitats and fishes (Shulman ultimately limiting reproductive success for salmon. Sig- 1961, Rumyantsev 1984). Interestingly, many species of nificant reductions in major populations of anadromous fishes occupy broad Holarctic ranges at high latitudes, fishes can have substantial impacts on nutrient cycling contrasting with the fish parasite fauna in which diver- in riparian and adjacent terrestrial habitats (Schinlder sity is often partitioned regionally and geographically & Smol 2006). Potential consequences also include rein the Palearctic and Nearctic (Shulman 1961, Carney duced ecosystem sustainability and direct influences on & Dick 2000). Patterns of distribution for parasites of subsistence and commercial fisheries (Kocan et al. 2004, freshwater fishes are treated in more detail by Wrona & Bradley et al. 2005). Reist (Chapter 13). Current predictions suggest that fishing practices, Parasite assemblages in freshwater fishes are influenced eutrophication and temperature increases may have the by changes in ecological structure linked to expansion most profound effects on parasite faunas among Arctic of geographic range, habitat perturbation and/or to host freshwater fishes (Marcogliese 2001a, 2008, Wrona Chapter 15 • Parasites 541

& Reist, Chapter 13). Impacts of climate change are vertebrates in freshwater/terrestrial habitats and are expected to be profound and will involve both direct and subsequently exposed to a considerably different parasite indirect effects on parasite diversity, faunal structure fauna (e.g. Bondarenko & Kontrimavichus 2006). Thus, (turnovers) and abundance and, in synergy with anthro- parasites often can be indicators of geographic origins pogenic factors, can be expected to influence host popu- for different species or populations of hosts at varying lations. Northward expansion along rivers and through spatial and temporal scales (Bondarenko & Kontrima- lakes for southern fish species (for example yellow perch vichus 1999). Irrespective of latitudinal and geographic Perca flavescens) and invertebrates of importance for trans- partitioning, many species of tapeworms and flukes have mission may lead to introductions of parasite species longitudinally broad ranges across the Holarctic, or at previously unknown in the North (Reist et al. 2006). the continental scale (e.g. Belopol’skaya 1979, 1980, In contrast, species of fishes endemic to the Arctic may 1983). These patterns of distribution, particularly for undergo range reductions leading to extirpation of both breeding ground faunas would be expected to be modi- hosts and arrays of parasites in sensitive biological sys- fied by northward expansion of some species of boreal tems (Wrona & Reist, Chapter 13). shorebirds in both Eurasia and possibly North America (Ganter & Gaston, Chapter 4). Further, northern mi- 15.6.2. Birds grants come into contact with different spectrums of parasites, which circulate independently among resident Waterfowl, cranes, shorebirds, gulls and loons are avian faunas established in tropical and Southern Hemi- dominant and often abundant in freshwater, wetland and sphere environments. estuarine habitats of the Arctic (Ganter & Gaston, Chap- ter 4). Macroparasite faunas among this assemblage of Consequences of seasonal shifts in phenology, including phylogenetically disparate birds are often diverse and to early migration and nesting in conjunction with geo- some degree specialized with host associations linked to graphic expansion in ranges, may be seen in perturba- particular avian taxa and ecological settings (e.g. Spass- tions in the timing and synchronicity of food availability kaya & Spassky 1978, Wong & Anderson 1990, Storer for breeding birds and fledglings (Ganter & Gaston, 2000, 2002, Bondarenko & Kontrimavichus 2006). Chapter 4). Synchronicity determines parasite transmission where the presence of a susceptible host population All birds associated with freshwater habitats are migrato- coincides with the availability of primary invertebrate ry, and in contrast to terrestrial birds, none are residents prey serving as intermediate hosts (Marcogliese 2001a). in the North throughout the year. Further, in contrast Mismatches in the arrival and breeding activities for to terrestrial birds, migration is often long-range and birds and the seasonal timing of production cycles that may involve intercontinental or global connections with determine the critical availability of invertebrate prey passage deep into the Southern Hemisphere for some may be expected to disrupt patterns of parasite diversity. species (Ganter & Gaston, Chapter 4). Seasonal migra- This may be reflected through loss of typical parasites, tion to overwintering areas in the South or breeding and or declines in their abundance and prevalence and could nesting areas in the North follows traditional flyways also extend across migration corridors and staging areas. generally using a series of historically predictable staging Asynchrony may also drive shifts to alternative prey areas. These patterns of distribution and seasonal move- species that result in exposures to a broader spectrum ment have a considerable influence on the occurrence of parasites. Examination of these postulated outcomes and diversity of helminth faunas among northern birds. is dependent on the availability of baselines for parasite For example, among the helminth faunas associated with diversity at varying geographic scales (Appendix 15.1). shorebirds (Scolopacidae and Charadriidae), species of parasites may be partitioned in space and time with Migration may also play a role in the distribution of specific assemblages linked to transmission on winter- some zoonotic parasites including Toxoplasma gondii in ing or breeding grounds or on migration corridors (e.g. the Arctic, which may have been introduced from more Belopol’skaya 1953, 1959, 1963, Dogiel 1964, Wong southerly latitudes (Prestrud et al. 2007). Toxoplasma & Anderson 1990). Considerable turnover in parasite gondii is a protozoan parasite that now occurs globally, diversity may occur between wintering and breeding and the disease toxoplasmosis has been reported from habitats, which for shorebirds reflect shifts from marine an extraordinary diversity of vertebrate hosts including to freshwater/terrestrial food resources (Anderson & humans (Dubey & Beattie 1988). The parasite is now Wong 1992, Wong & Anderson 1993). well documented in terrestrial and aquatic ecosystems of the Arctic, but the mechanisms for apparent introduc- In the case of acuarioid nematodes and other macropara- tion and dissemination remain largely enigmatic (Jensen sites acquired on marine wintering and staging areas, et al. 2010); both marine and terrestrial pathways appear the occurrence of these parasites in birds during pas- to be involved. For example polar bears Ursus maritimus sage reflects the diversity and abundance of crustaceans, and their primary prey including ringed seals Pusa hispida polychaetes and molluscs, and consequently, the struc- and bearded seals Erignathus barbatus appear to have had ture and ecological integrity of coastal and intertidal increasing levels of infection over the past decade, and systems where transmission occurs. On arrival to tundra the parasite is also common in Arctic foxes, wolverines environments in the Arctic, birds exploit a broad array Gulo gulo and even some ungulates (Kutz et al. 2012). of dipterans, coleopterans, annelids and other macroin- On Svalbard it has been postulated that the parasite may 542 Arctic Biodiversity Assessment be maintained by periodic introductions associated with species, one Baltic species, two cosmopolitan species, 17 migratory barnacle geese Branta leucopsis (Prestrud et al. brackish and freshwater species and 37 marine species 2007). A shift in the distribution and abundance of this with unknown distributions (Polyanksi 1961a). Parasites parasite and broad dissemination within this ecosystem provide information on their host habitats and diets, and may have accompanied population increases for geese consequently Polyanski (1961b) recognized distinct host and greater diversity of terrestrial birds arriving in Sval- complexes based on their parasite fauna. In the Barents bard that serve as prey for both Arctic foxes and bears Sea, fishes could be grouped into benthic and small fish (Prestrud et al. 2007, Jensen et al. 2010). consumers, littoral and coastal species, plankton feeders and migratory fishes, whereas in the Bering Sea they A mosaic of trends and responses is apparent, and the were categorized as exclusive planktivores, piscivores avian parasite faunas at high latitudes will ultimately also feeding on plankton, strict piscivores and benthi- reflect the cumulative environmental processes that vores. Taxonomically different species with similar diets influence diversity across considerable latitudinal and share parasites, while taxonomically related hosts with geographic gradients. For migratory species (and their different diets also have different parasites. Generally, parasites) there will be synergy with impacts manifested the Barents Sea parasite fauna consists of a mixture at lower latitudes (Gilg et al. 2012, Ganter & Gaston, of species of Arctic origin with those from the boreal Chapter 4). The effects of climate change and eutrophi- North Atlantic (Polyanski 1961a). The proportion of cation in freshwater habitats may be additive (Mar- Arctic-boreal parasites varies geographically within cogliese 2001a, 2008). Loss and restrictions of habitat, the Barents Sea and also among the host complexes particularly diminished tundra habitat for shorebirds and mentioned above. The far-eastern seas are considered a waterfowl, shifts from open tundra to closed and heavily distinct biogeographic region, but at the same time the forested zones, and structural changes related to produc- Bering Sea also shares parasites with the White Sea, the tivity are among the factors that will modify complex Barents Sea and the North Atlantic (Polyanski 1961a). host-parasite systems. Parasites are important components of the mosaic of environmental change. It has Perhaps the best-studied marine fish globally occurring been observed, with respect to avian taxa, that “Species in sub-Arctic or Arctic waters is the Atlantic cod Gadus respond individualistically to environmental variables morhua. As with marine fishes, few parasites are restrict- such as temperature, moderated by species assemblages, ed to northern latitudes. These include a few ciliates, competitors, facilitators, food, pests and parasites, and monogeneans, a cestode, a protist and a leech. However, potential immigrant species” (Callaghan et al. 2004b). cod are infected with numerous Arctic-boreal parasites, which do not extend into southern waters. These include 16 protists and myxozoans, four monogeneans, 11 dige- 15.7. NEARSHORE AND PELAGIC neans, at least 10 nematodes, three acanthocephalans, one leech and three copepods (Hemmingsen & MacKen- MARINE ECOSYSTEMS zie 2001). As with other hosts, certain other cosmopolitan parasites are also found in northern waters. 15.7.1. Fishes It has long been recognized that parasites can provide Marine fishes in the Arctic include nearly 250 recog- information on stock delineation (biological tags) for nized species (Christiansen & Reist, Chapter 6). As with fisheries management (Polyanski 1961b, Margolis 1965). other vertebrate taxa, our knowledge of parasites of ma- Consequently, our knowledge of parasites of marine rine fishes is fragmentary and incomplete. Historically, fishes in North America is largely confined to the sub- the most complete information stems from the former Arctic, and often restricted to commercial species such Soviet Union, with very broad host species coverage, as Pacific halibut Hippoglossus stenolepis and rockfishes whereas in North America, the best-studied hosts are Sebastes spp. off the Alaskan coast (Blaylock et al. 1998, anadromous fishes. Moles et al. 1998), and Greenland halibut Reinhardtius hippoglossoides and roundnose grenadier Coryphaeno- Most of the work in the former Soviet Union has been ides rupestris off Labrador (Zubchenko 1981, Arthur & concentrated in the Barents Sea, the White Sea and Albert 1994). Typically, these types of studies include the Bering Sea, where parasites have been surveyed sub-Arctic or Arctic waters only if the range of these in at least 46 species of marine fishes. Parasites tend commercial species extends into those waters. In a geo- to be most diverse in the Barents Sea and least diverse graphically extensive study, Blaylock et al. (1998) noted a in the White Sea, apparently reflecting its relatively typically sub-Arctic parasite fauna in Pacific halibut from young biogeographic history (Polyanski 1961a). A total northern latitudes. In European waters, parasites have of 146 parasite species have been found in the Barents been used to examine cod stocks in sub-Arctic waters Sea including 28 sub-Arctic species, 27 Arctic-boreal off Iceland, coastal Norway and the Barents Sea (Hem- species, 58 boreal species, five cosmopolitan species, mingsen & MacKenzie 2001). In addition, parasites have 10 freshwater and estuarine species, and 18 species of been used to determine the freshwater origins of Pacific unknown affiliation. In contrast, in the White Sea there salmon (Margolis 1965, Urawa et al. 1998). They also are 100 parasite species including 10 Arctic species, have been used to separate sea-run Arctic char from 11 Arctic-boreal species, 17 boreal species, five Pacific freshwater forms in Norway (Kennedy 1978), Greenland Chapter 15 • Parasites 543

(Due & Curtis 1995) and across northern Canada (Dick on parasitism and disease in these regions. As recognized & Belosevic 1981, Bouillon & Dempson 1989, Desdevis- by Polyanski (1961b) and still true today: “The study es et al. 1998). However, Dick (1984) cautions that given of the life cycles of parasites and their seasonal and age the patchy distribution of Arctic char parasites, each dynamics, requires the organization of permanent ‘fixed system must be examined separately, a rather daunting stations’ which can be sampled and investigated directly task. There are some marine parasites of char, however, at sea. To do this it is necessary to set up specialised that are widespread with Holarctic distributions, includ- parasitological laboratories at our marine biological sta- ing a number of trematodes (Brachyphallus crenatus, Dero- tions. ... Ecologo-parasitological investigations should genes varicus, Lecithaster gibbosus, Prosorhynchus squamatus), constitute an inseparable part of the general plan of stud- a cestode (Bothrimonus sturionis) and an acanthocephlan ies of the biology of the sea.” (Echinorhynchus gadi). All of these are generalists, infecting numerous host species in marine waters. 15.7.2. Seabirds Anisakid nematodes are cosmopolitan parasites that Birds are prominent and highly visible residents of infect Arctic and sub-Arctic pinnipeds and whales, with pelagic, nearshore and intertidal ecosystems around larval stages occurring in fishes in those regions as well. the Arctic basin, often occurring as apex predators in Members of two genera in particular are of concern to these marine environments. Although species diversity fisheries. Anisakis spp. are pathogens acquired from eat- is relatively low compared with temperate latitudes, ing raw or undercooked fish, while Pseudoterranova decipi- certain groups including seaducks and other waterfowl, ens is a large, visible nematode which is unappealing to gulls, auks, calidrid sandpipers and their allies attain consumers and reduces fish product quality. Anisakis spp. their maximum diversity in the sub-Arctic and Arctic mature in whales, while P. decipiens (sealworm) uses pin- (Ganter & Gaston, Chapter 4). Complex assemblages nipeds as its definitive host, and both parasites are found of digenean trematodes (flukes), tapeworms and nema- in a large range of fish intermediate and paratenic hosts. todes circulate though birds, molluscan (marine snails, Consequently, these parasites, especially sealworm, have bivalves and cephalopods), crustacean (crabs, amphi- been the subject of intensive investigation for well over pods, euphausiids, etc.) and fish intermediate hosts in three decades in waters off Alaska, Greenland, Norway the pelagic, intertidal and upper subtidal zones, where and in the Bering and Barents Seas, with records as far parasites often serve to structure coastal communities back as the 1930s in Iceland (Platt 1975, 1976, Munger (e.g. Galaktionov 1996a, 1996b, Mouritsen & Poulin 1983, Shults & Frost 1988, Karasev et al. 1996, Ólafs- 2002b, Kuris et al. 2008). In these avian assemblages, dóttir 2001). As a result, these are among the only fish generally pelagic (oceanic) birds such as some auks, a few parasites from the sub-Arctic or Arctic for which there gulls (e.g. the two kittiwake Rissa species) and tubenosed are long-term data to evaluate trends over time. For ex- seabirds support faunas of lower diversity compared ample, in Iceland, there has been a declining trend in the with those in loons, grebes, seaducks and most gulls and abundance of sealworm in cod between 1980 and 1999, terns, which are usually found on neritic (over the con- paralleling reduction in population size for gray seal tinental shelf) and littoral (nearshore and shoreline) habi- Halichoerus grypus definitive hosts, but this trend is not tats (Hoberg 1996). These patterns reflect differences in significant (Ólafsdóttir 2001). Seal numbers alone do not vagility, narrow versus eclectic foraging habits, and for account for high intensities in fishes, and other ecological gulls, grebes and loons, components of the parasite fauna and environmental factors likely are important. Across derived from terrestrial/freshwater systems. Spatially, the North Atlantic sub-Arctic waters, sealworm is more diversity is influenced by a dilution effect of the marine abundant in Icelandic cod compared with those from environment, where oceanic and continental islands rep- Greenland and northern Norway, and this may in part resent foci for parasite transmission and species richness be due to the location of Iceland at the interface of warm diminishes with distance as a trend into pelagic systems and cold water masses (Ólafsdóttir 2001). A series of (Hoberg 1996). studies in cod from the Barents Sea found no difference in abundance or prevalence of Anisakis simplex between The main biodiversity in Arctic seas is associated with the early 1970s and late 1980s, despite major ecosystem insular and mainland coastal waters. The rich and abun- changes over the same time period (Hemmingsen & dant fauna of marine organisms in intertidal and upper MacKenzie 2001). Rokicki (2009) suggests that anisakid subtidal zones attracts huge numbers of marine and nematodes may further increase in abundance as a result coastal birds that feed on these animals. The proximity of climate change. Temperature increases due to climate of all these organisms promotes transmission of complex change could extend the growing season and enhance parasite life cycles involving coastal invertebrates, fish development rates of eggs and larval stages (Marcogliese and birds as intermediate and final hosts. The fauna of 2001a, Rokicki 2009). These responses, however, may the coastal ecosystems of the Arctic seas is especially vary with parasites and their relative adaptation to warm rich in helminths (trematodes, cestodes, nematodes or cold waters (Marcogliese 2001b). and acanthocephalans) of seabirds. In the areas with a relatively milder climate (the White Sea, the Norwegian Clearly, only limited baseline data exist in many parts of Sea, the southwestern part of the Barents Sea, the near- the Arctic and sub-Arctic, and much basic survey work shore zone of Iceland and the north of the Sea of Ok- is required to prepare for climate change and its effects hotsk) trematodes predominate among these helminths, 544 Arctic Biodiversity Assessment as they do in the boreal regions. In the regions with a & Marasaev 1986). Especially dense aggregations of more Arctic climate, there is a clear tendency towards waterfowl, such as the king eider Somateria spectabilis, the a lower species diversity of trematodes, up to their total black scoter Melanitta nigra, the long-tailed duck Clangula disappearance in the high Arctic. This may be condi- hyemalis, the velvet scoter Melanitta fusca and the Stel- tioned on severe environmental conditions in the Arctic ler’s eider Polysticta stelleri, are constantly observed there coastal zone which impede transmission of trematode at the shallows near Dolgii Island during the molting free-living (miracidia and cercariae) larval stages (Galak- period and migration to wintering places (Krasnov et al. tionov & Bustnes 1999). 2004, Sukhotin et al. 2008). The diet of these birds is based on mussels Mytilus edulis, other subtidal molluscs Trematodes that lack free-living larvae in their life and crustaceans, the intermediate hosts of the helminths cycles, such as microphallids of the ‘pygmaeus’ group, parasitic in these birds. Near Dolgii Island these inver- advance further into the Arctic. A representative of tebrates are heavily infected by the larvae of helminths, ‘pygmaeus’ microphallids, Microphallus pseudopygmaeus, is such as the trematodes Micropallus pseudopygmaeus, Tris- the only trematode species recorded in seabirds from the triata anatis, Gymnophallus somateria and Renicola somateria, high Arctic archipelagoes of Novaya Zemlya (northern cestodes Microsomacanthus spp. and acanthocephalan island) and Franz Josef Land (Galaktionov et al. 1993, Polymorphus phippsi parasitic in seaducks (K. Galaktionov, Kuklin & Kuklina 2005). It should be emphasized that unpbl. data). the life cycles of cestodes (Tetrabothriidea, Dilepididae and Hymenolepididae) and acanthocephalans (Polymor- Formation of such local foci of invertebrate infection phus, Corynosoma) parasitizing Arctic seabirds also lack by the larvae of seabird helminths is characteristic of free-living larval stages. the coastal waters of the Arctic seas. The sites of high concentrations of the final hosts (bird colonies, migra- Apart from climatic conditions, expansion of seabird tory aggregations etc.) alternate with vast areas only trematodes into the Arctic was hindered by the cir- sporadically visited by birds. It is worth noting that hu- cumstance that most of them use molluscs belonging to man activity may have an indirect effect on the increase the boreal and Arctic-boreal faunal complex (Littorina, of the infection level in coastal invertebrates. This is Hydrobia, etc.) as first and second intermediate hosts. associated with the anthropogenic concentration of bird These molluscs do not penetrate into the high Arctic. populations. For instance, in northern Norway, gulls Cestodes and acanthocephalans, whose intermediate often gather in fishing ports and fishing farms to feed hosts are crustaceans, are in a different situation. The on offal. This leads to a concentrated distribution of abundance of crustaceans in nearshore ecosystems of the the final hosts, which may, in turn, lead to increased high Arctic enhances successful transmission of these transmission of parasites between hosts. Examinations parasites. Though species composition of cestodes and of intertidal molluscs and crustaceans conducted on the acanthocephalans is lower than in boreal regions, the coast of northern Norway revealed a higher infection infection indices are high. For example, at Franz Josef prevalence of helminth larvae in gulls in places with Land the infection intensity of cestodes Microsomacanthus human activity (fishing ports, fish industry complexes, spp. and the acanthocephalan Polymorphus phippsi in the fish farms) as compared with places untouched by human common eider Somateria mollissima reaches 200,000 and activity (Kristoffersen 1991, Bustnes & Galaktionov 1,200, respectively, in individual hosts. As these para- 1999). Here, populations of invertebrates are constantly sites are pathogenic for seabirds (for review see Gal- subjected to parasitic pressure which may result in aktionov 1996b) they must influence considerably the detrimental effects. Moreover, the invertebrates inhabit- dynamics of their host populations in the Arctic. This ing these sites are also subject to heavy anthropogenic effect was demonstrated in the population of the com- influences such as pollution with hydrocarbons, every- mon eider in the White Sea in a monitoring ornithologi- day wastes etc. Consequently, there is a double pressure cal and parasitological survey of 1935-1985 (Kulatchkova (both parasitic and anthropogenic), which obviously 1979, Karpovich 1987). strengthens pathogenicity at the organismal level and can provoke degeneration of coastal ecosystems near settle- The Arctic is crossed by migratory routes of many spe- ments (Bustnes et al. 2000). cies of shorebirds and waterfowl nesting along the coasts of the polar seas and in the tundra. Each year millions of Species composition and indices of the birds’ infection birds migrate along the coasts and across the open areas with parasites are dynamic and subject to long-term of the Arctic seas (Johnson & Herter 1990, Webster et fluctuations. The latter are determined by changes al. 2002, Alerstam et al. 2007, Ganter & Gaston, Chap- in marine ecosystems caused both by natural and by ter 4). This promotes a broad trans-Arctic transmission anthropogenic causes. An illustrative example is provid- of parasites, whose scale is now difficult to assess due to ed by the studies of parasites of colonial seabirds at the the scarcity of parasitological data from the areas of the sub-Arctic Seven Islands Archipelago (eastern Murman, Siberian seas, the coastal waters of Alaska and the Cana- Barents Sea, 68° 45’ N, 37° 25’ E) where the largest dian Arctic Archipelago. At the sites of mass aggregation bird colonies in the eastern end of the Kola Peninsula of migrating birds, local foci of helminth infection may are situated. Parasitological studies were carried out arise. This was shown in some areas of the southeast- there in 1940-41 by M.M. Belopol’skaya (1952) and in ern part of the Barents Sea (Pechora Sea) (Galaktionov 1991-2000 by a team of researchers (Galaktionov 1995, Chapter 15 • Parasites 545

Kuklin & Kuklina 2005). Over the past 50 years, since to an even greater decrease in the possibility of infection Belopol’skaya’s studies, the numbers of seabirds at the of the second intermediate hosts. Correspondingly, the archipelago and their food composition have changed due probability of the second intermediate host (fish, crusta- to anthropogenic influences. Due to fishery activities, cean, mollusc) containing the infective larvae being eaten the proportions of Atlantic herring Clupea harengus and by the final host (seabird) is infinitesimal. capelin Mallotus villosus have dropped sharply whereas the proportion of sandeel Ammodytes tobianus and also Atlan- In contrast to trematodes, Eastern Murman is not a tic cod, redfish Sebastes spp., goby Myoxocephalus scorpius, boundary for the distribution of the majority of the ces- plaice Pleuronectes platessa and lumpfish Cyclopterus lumpus tode species observed in the Seven Islands Archipelago have increased in the food composition of fish-eating seabirds. They have been found in the gulls and auks of seabirds (Krasnov et al. 1995). The consumption of mol- Greenland, Novaya Zemlya, Franz Josef Land and in the luscs, mainly blue mussels, decreased 2-3-fold. Shifting North Pacific basin and Bering Sea (Markov 1941, Baer prey selection coincided with a dramatic decrease in 1956, Galaktionov et al. 1993, Hoberg 1996). Changes the abundance of mussels (> 90%) in the Barents Sea, recorded in the cestode fauna of the archipelago seabirds reflecting either changing patterns of larval recruitment were not so conspicuous and can be attributed mainly controlled by advection from the Norwegian Sea, or by to changes in their diets. For example, disappearance of shifts between cold and warm water mass regimes. Tetrabothrius jaegerskioeldi and the decrease in the prevalence of the common species T. erostris in gulls may be Most striking in the comparison of the results of 1991- attributable to shifting abundance of fish species. At 2000 survey with those of 1940-41 is the decline in the the same time, the tetrabothriid fauna of kittiwakes species composition of trematodes. In 1991-2000 trema- was supplemented by T. immerinus and Tetrabothrius sp. I, todes in the Seven Islands Archipelago seabirds were whereas the great black-backed gull was demonstrated represented by six species, as compared with 11 record- for the first time to be a host for T. cylindraceus and Tet- ed by Belopol’skaya in 1940-41. It should be emphasized rabothrius sp. I. The increase in the proportion of small that the life cycles of only four of these six species are crustaceans (Mysidacea, Euphausiacea, Calanoidea) in associated with marine ecosystems; the trematodes Dip- kittiwake diet may have caused an increase (from 41% lostomum spathaceum and Plagiorchis laricola use freshwater to 69%) of infection with Alcataenia larina. At the same invertebrates and fishes as intermediate hosts. From the time, this species disappeared from the herring gull richest (nine species, 1940-41) trematode fauna, which helminth fauna, whereas Wardium cirrosa appeared and was that of the herring gull Larus argentatus, such com- infection with Alcataenia micracantha and Microsomacanthus mon species as Microphallus similis and Renicola murmanica ductilis increased. Most probably, these latter shifts were have disappeared. A sharp decrease of Gymnophallus linked to an increase in intertidal and upper subtidal deliciosus prevalence and the total absence of Renicola crustaceans (intermediate hosts for the above cestodes) and Himasthla is likely to be determined by the above- in herring gull diets, as compared with 1940-41. mentioned decrease of bivalves, the intermediate hosts of these trematodes, in the diet of these birds. A similar To sum up, the changes in the helminth fauna composi- explanation does not, however, apply to Microphallus tion of the Seven Islands Archipelago seabirds can be to similis, which in Eastern Murman uses the crabs Hyas ara- a great extent explained by the changes in the numbers neus as the second intermediate host (Uspenskaya 1963). of seabirds and in their diet. To some extent, marine The tendency concerning Cryptocotyle lingua, a common birds forage opportunistically, and prey selection and parasite of gulls, is also obscure. An increased consump- its relationship to parasites reflects shifts in abundance tion of fish (young cod, redfish, goby and plaice), which for fishes or invertebrates that may be available as prey. enter the intertidal and upper subtidal zones, should Consequently, in these cases parasites directly indicate have resulted in an increased prevalence of C. lingua in the structure of foodwebs and the intricate connections gulls, as the aforementioned fishes are intermediate hosts between birds and forage resources (Hoberg 1996, of this parasite. Instead, C. lingua prevalence in gulls was 2005b). much lower in 1991-2000 than in 1940-41. Concurrently, considerable shifts in the structure of Decreased species diversity and prevalence of trematodes host-parasite assemblages in the Arctic seas may also be in seabirds appears to have been promoted also by the re- driven by climatic changes, including variation in ocean- duction in the number of the principal final hosts of these ographic conditions, current regimes and range shifts parasites – the herring gulls, great black-backed gulls for certain crustacean intermediate hosts, particularly Larus marinus and common gulls Larus canus in the archi- euphausiids. For example, shifting abundance of species pelago area (Krasnov et al. 1995). Eastern Murman is the of Alcataenia tapeworms has been linked to differential northeastern boundary of the known distribution area exploitation of euphausiid prey by thick-billed Uria lomvia of most aforementioned trematodes. Their prevalence in and common murres Uria aalge and kittiwakes in the the first intermediate host (molluscs) in this area is thus North Pacific and Bering Sea, and oceanic regime shifts extremely low in comparison with the western parts of (from warm to cold conditions linked to the Pacific the Barents Sea coast (Galaktionov & Bustnes 1996). Its Decadal Oscillation) were implicated as determinants of further decrease in the archipelago area, as a result of the parasite distributions (Hoberg 1996, 2005b). New cur- decrease in the main species of final hosts, should lead rent regimes and watermass structure through the Arc- 546 Arctic Biodiversity Assessment tic basin were identified as drivers in an apparent range 2. higher numbers of infected molluscan hosts will drive expansion from the North Pacific to the North Atlantic expansion of parasite populations in invertebrates and of another species of Alcataenia in murres (Muzaffar et fishes that are primary prey for birds, and al. 2006, Muzzafar 2009). Oceanic colonization was ap- 3. prevalence and abundance of parasites in birds is pre- parently mediated by an expanding range for euphausiid dicted to increase coincidentally with patterns of at- crustacean intermediate hosts of Pacific origin. Estab- mospheric warming and increasing sea temperatures, lishment of these tapeworms appears to have coincided leading to heightened levels of infection for molluscs. with a substantial restructuring of the parasite fauna of these pelagic birds relative to conditions documented in These feedback loops will be further enhanced as the the late 1960s (Threlfall 1971, Muzzafar 2009). As in duration for residency by shorebirds in intertidal zones the Seven Islands Archipelago, it was the presence of a of the sub-Arctic and Arctic broadens seasonally in large scale historical baseline established through prior response to ameliorating conditions linked to climate collections that allowed exploration of faunal change change (Lehikoinen et al. 2004). The ultimate outcome over time in these pelagic systems. of these cascades may be collapse of intertidal communities as parasitism and mortality in molluscan, crustacean These studies clearly indicate that parasites are powerful and piscine hosts disrupts food-web dynamics (Mar- adjuncts to studies of food habits and foraging ecology cogliese 2008). It is essential that monitoring programs among diverse assemblages of hosts. Such is particularly be developed throughout the Arctic basin to follow the evident in the detailed investigations of parasite faunal development of this process that can have profound structure among marine birds in the White Sea region effects on the structure of nearshore ecosystems (Galak- and North Pacific basin. Studies of food habits are often tionov et al. 2006). temporally limited providing a brief glimpse of food selected by birds at a particular moment in time. In 15.7.3. Marine mammals contrast, parasites that circulate among apex predators such as murres and other seabirds facilitate a more nu- Marine mammals are characteristic inhabitants through- anced exploration of trophic ecology. Parasites reveal the out global seas and include approximately 13 species of underlying oceanographic conditions and regime shifts baleen whales, 71 species of toothed whales, 34 species that determine distributions of euphausiids, fishes and of pinnipeds (seals and sea lions), polar bear, sea otter cephalopods (e.g. Ganter & Gaston, Chapter 4) that are Enhydra lutris and the sirenians (Evans & Raga 2001). the foundations for intricate links involved in transmis- Among these, there are 313 species of macroparasites, sion and completion of life cycles. Parasites found in a relatively few protozoans, but a considerable diversity of host are the sum of foraging activity spread over some viruses and bacteria (Aznar et al. 2002). Marine mam- period of time, but generally within a definable spatial mals are locally abundant in circumpolar seas extend- sphere related to prey abundance and distance to colony ing from the northern North Atlantic to the Bering Sea sites (e.g. Hoberg 1996). Thus, knowledge of parasites where overall the fauna is characterized by 22 species of directly complements more targeted studies designed cetaceans (whales), nine pinnipeds (walrus Odobenus ros- solely to reveal the spectrum of prey selected by various marus and seals), and the polar bear (Reid et al., Chapter vertebrate species. 3). At high latitudes, helminth parasite faunas include over 30 species of tapeworms, flukes, nematodes and Climatic effects are also manifested in relatively short thorny-headed worms that have distributions through term events that may represent responses to incremental the Arctic Ocean, with a minimum of 26 in pinnipeds change over time. The process of parasite development and six in cetaceans (Delyamure 1955). Consistent with in intermediate hosts, mostly cold-blooded animals, the latitudinal gradients, this contrasts with boreal seas release of the parasite larvae into the environment and (North Atlantic and North Pacific Oceans) where ap- the process of the host animals’ infection are greatly proximately 35 species parasitize pinnipeds and 49 are influenced by the temperature of the environment known in cetaceans. Patterns of diversity reflect species (Galaktionov et al. 2006, Poulin 2006, Poulin & Mou- richness and abundance for respective host groups. ritsen 2006, Koprivnikar & Poulin 2009, Studer et al. 2010). A highly relevant circumstance in this respect is Original recognition of these gradients has been aug- the fact that parasite transmission in the Arctic regions mented by recent studies. For example, in waters of the is confined to a very short time period, the so-called North Pacific and eastern Arctic Ocean, baseline survey transmission window. Recent studies in the coastal zone data exist for macroparasites in phocids including harbor of the White Sea demonstrated that climate change and seal Phoca vitulina, largha Phoca largha, ringed seals and long-term warming of intertidal systems can drive the ribbon seals Phoca fasciata (Adams 1988, Shults & Frost amplification of parasite populations in both birds and 1988, Hoberg et al. 1991, Measures & Gosselin 1994) molluscan hosts (Galaktionov et al. 2006). and otariids including the Steller’s sea lion Eumetopias jubatus (Shults 1986). Additionally, among cetaceans, Intensified transmission for flukes represents an unfold- twenty-two species of helminths are now known from ing cascade in intertidal systems where the blue whale Balaenoptera musculus, of which 20 occur 1. the seasonal window for infection of molluscan inter- in the Arctic (Measures 1993). mediates will be prolonged, Chapter 15 • Parasites 547

Prominent in these faunas are tapeworms of the genera Although infection pathways through zooplankton and Diphyllobothrium and Anophryocephalus (e.g. Hoberg 1995, fishes are well defined for anisakines and Diphylloboth- Hoberg & Adams 2000, Rausch 2005) and anisakine rium, circulation of Trichinella and either intestinal or nematodes including species of Anisakis, Pseudoterranova, tissue-cyst forming protozoans like Toxoplasma are poorly Contracaecum and Phocascaris (Rokicki 2009). Lungworms understood in marine environments (Forbes 2000, Jens- (Acanthocheilonema spirocauda, Otostrongylus circumlitus) and en et al. 2010). Other disease agents recently detected in heartworms (Filaroides gymnurus, Parafilaroides arcticus) northern marine mammals include Brucella sp. and mor- also have been surveyed in ringed seals from the Cana- billivirus, the latter similar to phocine distemper virus dian Arctic (Bergeron et al. 1997, Gosselin & Measures in walrus (Forbes et al. 2000, Nielsen et al. 2000). 1997, Measures et al. 1997). Species of Diphyllobothrium, Anisakis and Pseudoterranova are recognized as zoonotic parasites in people, and larval stages are acquired from 15.8. TRADITIONAL ECOLOGICAL consumption of infected fishes, with anadromous species having a prominent role (Rausch & Adams 2000). KNOWLEDGE ON PARASITES IN Historic records for the distribution anisakines tend to THE NORTH be strongest for Pseudoterranova spp. in seals, especially in Iceland, because this parasite has been a continuing problem for commercial fisheries (Ólafsdóttir 2001). Liver – if liver good, animal healthy, if bumps on liver animal » is discarded. … You use common sense; you eat what is good In contrast to pinnipeds and cetaceans, polar bears have for you. If it doesn’t look good you don’t eat it. Won’t eat liver if they remarkably few macroparasites other than Trichinella see something on it. nematodes, despite relatively deep temporal origins and expansion into marine environments since the late If we start getting disease in all the wildlife what’s going to hap- Miocene about 4-5 million years ago (Miller et al. 2012), pen? Our age group is still living off the land. Younger generation and a specialized diet of pinnipeds and marine carrion. won’t know anything like that. Go to the store and buy wieners and As polar bears are increasingly displaced from ice-edge sandwiches. They don’t eat the same food as we do. habitats and stranded on shore, shifts in foraging behaviour may be anticipated to lead to exposures for a In the old days there was no study on the animals like caribou and broader spectrum of parasites derived from intertidal moose, but when the elders killed a moose or caribou, they ate the zones (e.g. Laidre et al. 2008). Such dietary shifts may meat and nobody ever got sick from the animal in the old days. be indicated by an array of digenean flukes that circulate They never saw dead animals anywhere. He said you guys are through molluscs and crustaceans in shallow coastal seas studying animals now, but in the old days they had no study on (Rausch et al. 1979). the animals. But he said that when they see animals or they shoot at animals, they know if it’s good or bad, because their ancestors Decreases in sea ice in the Arctic Ocean are predicted used to tell them how to see, so they never did any studies on the to have a pervasive effect on ecosystem structure and animals, but they know what is good and what is not. They just the biology of ice-associated marine mammals, including knew it by heart. If the animal was fat and good to eat, they knew polar bears, walruses, some other pinnipeds and whales it by heart. If the animal was not good to eat, skinny, they knew it. that have considerable importance in subsistence foodwebs (Moore & Huntington 2008). Changes in oceanic Alfred just mentioned that from Alberta and in the North we’re regimes, currents and water-mass structure, associated different because we always have cold weather all the time, and ice conditions, freshwater melt and salinity will drive they have the warm weather and those kinds of spiders (ticks) can modifications in behavior and diets for marine mammals go on anything, can go onto the animals. But here we have cold as distribution and species composition for invertebrate weather and we don’t see that much in the summertime. and vertebrate prey species respond to new environ- (Village elder, Aklavik, Canada, as related to S. J. Kutz). mental conditions (Marcogliese 2001a, Laidre et al. 2008). The degree of sympatry and seasonal overlaps in distributions for cetaceans and pinnipeds are predicted Traditional knowledge held by indigenous peoples to increase, suggesting heightened opportunities for the about parasites in wildlife used for food and materials exchange and dissemination of parasites and pathogens can directly complement scientific baselines (Brook et (Burek et al. 2008). al. 2009). Considerable knowledge is evident in some regions and for some wildlife species, often reflecting Concurrently, accelerated warming in the Arctic may an understanding of potential food safety risks associ- modify the diversity and abundance of parasites associated with a subsistence diet. For example, traditionally ated with these mammals, resulting in greater levels in Alaska meat from bears is not consumed raw but is of exposure for people to zoonotic helminths such as always cooked due to the threat of infection and disease Trichinella nativa, anisakine nematodes and species of posed by Trichinella nematodes (e.g. Rausch 1972). Diphyllobothrium tapeworms and protozoans including Toxoplasma gondii, species of Giardia and possibly Crypto- A more general knowledge about disease processes and sporidium (Marcogliese 2001a, Hughes-Hanks et al. 2005, the impact of parasites is also apparent as demonstrated in Rausch et al. 2007, Burek et al. 2008, Jensen et al. 2010). the NWT of Canada through focus groups and interviews 548 Arctic Biodiversity Assessment about ungulates (Kutz 2007). Participants included elders 15.9. CONCLUSIONS AND and mature hunters and women who had handled hide and RECOMMENDATIONS meat for numerous years. Those among this cohort were familiar with many of the common parasites of caribou, muskoxen and moose. Observations by hunters brought 15.9.1. New tool development an apparently unknown emerging disease – “slimy green/ yellow wet stuff under the skin” – affecting caribou to Knowledge of parasite diversity, particularly definitive the attention of biologists (Kutz 2007). Later reports identification, geographic distribution and host associa- from the field documented the increasing incidence of tion, is critical as a foundation for understanding the this syndrome in harvested caribou (Kutz et al. 2009a). potential for pathogen dissemination and disease (Brooks Parasitic infection was suggested based on the structure & Hoberg 2000, 2006, Hoberg 2010). Achieving this of the lesions, but the cause remains to be determined. goal requires field-based research, networks with local In some cases, the liquefied lesions were found in associa- capacity, scientific and local community engagement, co- tion with the protozoan Besnoitia tarandi and dead larvae ordination and collaboration to facilitate collections, plus of the warble fly Hypoderma tarandi; nematodes were not methodologies that provide timely or rapid identification demonstrated. In Finland a similar syndrome is known in of parasites. Parasite collection and identification has often semi-domestic reindeer and in Eurasian elk, observed in been a laborious process dependent on special expertise conjunction with subcutaneous infections of the filarioid and knowledge of specific taxonomic groups. Collections nematode Onchocerca, where in some areas 100% of ani- were often logistically difficult (e.g. ungulates or marine mals are affected (S. Laaksonen, unpubl. data). mammals) where the necessity of field-based necropsy to recover adult parasites often limited the geographic scope The recent invasion into the northern boreal forest of the and numbers of host specimens that could be examined. NWT by the winter tick Dermacentor albipictus was fur- Molecular-based methods increasingly complement mi- ther confirmed by local hunters who had no prior tradi- croscopic identification, and such approaches for the first tional knowledge of this arthropod parasite in the region time provide a means for geographically extensive and (Kutz et al. 2009a). Interestingly, hunters from several site-intensive sampling for parasite diversity that does not communities indicated that parasitism was normal in the always have to rely directly on necropsy (e.g. Jenkins et animals and kept them healthy, but that animals with al. 2005, Kutz et al. 2007). These and other non-invasive, numerous visible parasites were often “skinnier” than ‘field-friendly’ methods enhance data and sample collec- those without parasites. tion and storage by hunters, substantially increasing the capacity to rapidly assess diversity and epidemiology of Results from these interviews demonstrated that there parasites across large landscapes and regions (e.g. blood is considerable traditional knowledge and local expertise filter paper (Curry 2009), and fecal sampling for para- on the occurrence of specific parasites and disease syn- sitic eggs and larvae in conjunction with DNA amplifica- dromes. It is urgent that such local insights about north- tion and sequencing (Jenkins et al. 2005, Huby-Chilton et ern systems be recorded, given an ageing population al. 2006, Kutz et al. 2007, DeBruyn 2010)). Additionally, and the continuing transition away from lifestyles linked definitive identification of many microparasites such as directly to the environment. Documenting personal species of Giardia, Toxoplasma, Besnoitia and others is not histories and observations from community elders and feasible in the absence of molecular methodology (e.g. others should be a collaborative process between social Criscione et al. 2002, Polley & Thompson 2009). The scientists and biologists who are conversant with para- latter is increasingly important in identifying the sources sites and wildlife diseases (e.g. Kutz 2007). Local knowl- and pathways for human infection from stages of parasites edge provides valuable historical baselines, particularly acquired through water or food contamination mediated in regions and localities lacking scientific collections, by wildlife (Polley & Thompson 2009). surveillance or monitoring, as well as a methodology for contemporary tracking of infectious diseases in wildlife Documentation of parasite diversity is a continuum that (Henri et al. 2010). includes: 1. targeted taxonomic studies on single parasite species Similarly, in aquatic habitats, subsistence fishermen were and simple case reports in individual hosts, the first to recognize an expanding disease syndrome in 2. surveys for parasites in single host species at a limited Chinook salmon on the main stem of the Yukon River in spectrum of localities, Alaska (Kocan et al. 2004). Infections by the enigmatic 3. survey and inventory at the ecosystem level based on protozoan Ichthyophonus hoferi were unknown prior to standardized and comprehensive sampling protocols 1980 in Pacific salmon and were apparently absent from implemented on broad geographic scales, and the Yukon River system. The parasite is now abundant 4. integrated inventory for hosts and parasites with and well established and constitutes a direct influence on application of population genetic approaches and phy- the availability, suitability and palatability of salmon as logeography to explore relationships at fine temporal food (Bradley et al. 2005). and spatial scales (see Cook, Chapter 17). Chapter 15 • Parasites 549

Ecosystem approaches for survey (and surveillance) are 1. provide a detailed and geographically widespread necessary as the distribution of a parasite is generally resource of museum specimens from key high-latitude broader than the distribution of disease (Audy 1958), areas that had not been inventoried, and outbreaks may represent geographic (and host) mo- 2. develop a comparative framework for Beringia to saics that are ephemeral in space and time (Thompson examine the history of host-parasite systems that are 2005, Hoberg 2010). Geographic coverage from local phylogenetically and ecologically disparate, provid- landscapes to regions is thus a foundation for establishing the basis for detailed studies in coevolution and ing patterns of abundance and circulation for parasites. historical biogeography, Further, such surveys should contribute directly to the 3. explore large-scale physical (climate variation) and bi- development of archival biological collections (parasites, otic forces that have structured high-latitude biomes, hosts, tissues and biodiversity informatics) held in mu- including drivers of intercontinental faunal exchange seum repositories as a baseline for diversity and faunal across the North, and structure (Fig. 15.2) (Brooks & Hoberg 2000, Hoberg et 4. build a spatial and temporal foundation at fine scales al. 2003, 2009). for investigations of Arctic biodiversity by identifying regions of endemism and contact zones between The Beringian Coevolution Project (BCP), initiated in divergent lineages while exploring fundamental 1999, represents a primary model for integrated survey mechanisms that determined faunal diversity within and inventory of northern fauna (Hoberg et al. 2003, complex biotic systems. Cook et al. 2005). The BCP was designed to:

Figure 15.2. A model for integrated survey and inventory to explore diversity in northern host-parasite systems. Ecosystem and multi-species approaches rely on field-based collections of macroparasites and microparasites that result from collaborations among parasitologists, wildlife biologists, ecologists and local communities. Specimens are deposited in archival collections, where geo-referenced data are linked to tissues and vouchers for hosts and parasites, along with their definitive identifications. Biodiversity information becomes the focal point for diagnostics, development of temporal and spatial baselines, and diverse research activities including ecological modeling and prediction in a regime of environmental change. Archives representing specimens and informatics become the baselines to define faunal diversity and against which environmental perturbations may be assessed. As a limited example of integrated and ecosystem level survey in the Bering Sea, counter-clockwise from the top: Steller’s sea eagle Haliaeetus pelagicus, rock sandpiper Calidris ptilocnemis, short-tailed shearwaters Puffinus tenuirostris and lesser numbers of sooty shearwaters Puffinus griseus, rhinoceros auklet Cerorhinca monocerata, crested auklet Aethia cristata, tufted puffin Fratercula cirrhata and black-legged kittiwake Rissa tridactyla. Photos: E.P. Hoberg.

Conservation management

Hosts/pathogens Tissues/vouchers GIS Microparasites Archival Collections Ecological Macroparasites modelling Biodiversity informatics Prediction

Research

GenBank Baselines

Diagnosis 550 Arctic Biodiversity Assessment

The BCP has resulted in extensive archival collections of 2003) that contributes to archival collections (parasites, host and parasite specimens, including whole vouchers, hosts and tissues) as a permanent record of environments tissues and DNA products from approximately 18,000 in dynamic change (e.g. Hoberg et al. 2008b, Cook, small mammals (primarily rodents, soricomorphs, Chapter 17). Such archival resources, as self-correcting lagomorphs and mustelids representing 80 species and records of biodiversity, will be increasingly important in 31 genera, with additional materials from high latitude the arenas of ecosystem sustainability, human health and ungulates) across 250 sites spanning > 100° longitude conservation (Hoberg et al. 2003, Koehler et al. 2009, and > 25° latitude in Siberia, Alaska and Canada. Speci- MacDonald & Cook 2009). mens and information are housed in permanent museum repositories including the Museum of Southwestern Biol- 15.9.2. Anticipated important host-parasite ogy, University of New Mexico, the University of Alaska Museum of the North and the US National Parasite assemblages and processes Collection (Cook et al. 2005). A crucial foundation and unique baseline of information for hosts and parasites is The presence of diverse assemblages of parasites is in- emerging and under current evaluation for basic research dicative of a healthy ecosystem (Marcogliese 2005, Hud- and conservation in the face of changing climate and in- son et al. 2006). The presence of parasites is an indicator creasing anthropogenic impacts at high latitudes (Arctos of ecosystem stability and the connections that fishes, 2012). birds, mammals and invertebrates have within and across complex foodwebs in aquatic and terrestrial environ- In parallel, the International Polar Year (2007-2008) ments (Lafferty et al. 2006, Amundsen et al. 2009). Fol- provided the opportunity to focus on health, status and lowing from this complex web of interactions, parasites population trends for caribou and reindeer through tell stories about where host individuals, populations the CircumArctic Rangifer Monitoring & Assessment and species have been (in migration), what they eat and Network (CARMA). From 2007 to 2009, this network where they spend their time. Consequently, perturba- developed and implemented standardized sample and tions in ecosystems are often reflected in the diversity data collection protocols to evaluate the body condition, and spectrum of parasites that occur at landscape to demographics and health of multiple herds in North regional scales (Hoberg 1996, Marcogliese 2001). These America, Greenland and Russia. CARMA also built on relationships serve to indicate the importance of under- existing programs (Brook et al. 2009) to develop train- standing parasite diversity in space and time (Hoberg ing materials to facilitate hunter-based health monitoring 1997, Brooks & Hoberg 2000). for caribou. Development of locally supported, effec- tive and efficient monitoring programs that can provide The biodiversity crisis is not simply an issue of ecosystem long-term data are dependent on assessing protocols and perturbation and species loss, but also one of emerging by adapting methods that are most appropriate at the infectious diseases in both wildlife and people (Daszak community level across region. et al. 2000, Brooks & Hoberg 2006). Fundamental to either an invasion or emergence of parasites is breakdown Another mechanism for ongoing parasite monitoring is in environmental structure or ecological isolation driven through local programs. For example, due to food safety by natural or anthropogenic processes (e.g. Elton 1958, issues, the Nunavik Trichinellosis Prevention Program Hoberg 2010). Ecological disruption with the develop- was established in Kuujjuaq, Quebec (formerly Fort ment of new borderlands or ecotones is also central to Chimo) by the Nunavik Research Centre (Proulx et the process for expanding host and geographic ranges al. 2002). This program serves to monitor prevalence, for assemblages of parasites. Analogues based on histori- intensity and geographic distribution of Trichinella in cal processes for episodes of climate change can serve to walrus from Nunavik. Such a program may have general inform us about how complex host-parasite systems in applicability across the Arctic given ongoing perturba- the Arctic have been structured by events in the Quater- tion at the ecosystem level and projected changes for the nary Period during the last 2.6 million years (e.g. Rausch distribution of Trichinella in marine mammals (Rausch et 1994, Hoberg et al. 2003, 2012). Dispersal, range shifts, al. 2007). colonization of new geographic regions and switching of parasites among host species and within ecosystems are The importance of efforts to improve methodologies that fundamental characteristics of northern systems, and facilitate sample and data collection in the field cannot these mechanisms are equivalent in evolutionary and be overestimated. The Arctic continues to be a logisti- ecological time (Hoberg & Brooks 2008, Hoberg et al. cally challenging region for field biology and assessment 2012). The nature of invasion and emergence, however, of pathogens and the distribution of disease. As much suggests that it not always simple to predict how assem- as is possible, knowledge of parasite diversity should blages of hosts and parasites will respond to transitional be linked directly to specimen-based information. The conditions, particularly those associated with acceler- primary cornerstone will be integrated survey and in- ated climate change in contemporary northern systems ventory supporting surveillance (active systems designed (Marcogliese 2001a, Hoberg et al. 2008a, 2008b, Kutz et to discover general patterns of abundance, prevalence al. 2009a, 2012, Hoberg 2010, Gilg et al. 2012). These or incidence) and monitoring (ongoing assessments of factors heighten the need for comprehensive surveys to health status of specific animal populations) (Salman establish baseline faunal associations for poorly known Chapter 15 • Parasites 551 hosts or among host-groups identified as keystones Anderson, R.C. & Wong, P.L. 1992. Western Palearctic and Ethio- within specific ecosystems (Appendix 15.1). Application pian species of Skrjabinoclava (Nematoda: Acuarioidea) in Ice- landic shorebirds (Aves: Charadriiformes) en route to breed in of model-based approaches, particularly ecological niche the New World and Greenland. Can. J. Zool. 70: 1861-1877. modelling, in conjunction with detailed records from ar- Arctos 2012. Multi-Institution, Multi-Collection Museum Data- chival collections can also contribute to an understand- base. arctos.database.museum/SpecimenSearch.cfm [accessed ing of the consequences of environmental change on the August 2012] distribution of parasites and disease (e.g. Waltari et al. Arthur, J.R. & Albert, E. 1994. A survey of the parasites of Greenland halibut (Reinhardtius hippoglossoides) caught off 2007b, Waltari & Perkins 2010). Atlantic Canada, with notes on their zoogeography in this fish. Can. J. Zool. 72: 765-778. Establishing baselines for diversity is central to identify- Audy, J.R. 1958. The localization of diseases with special refer- ing the role of parasites in an ecosystem, among host ence to the zoonoses. Trans. Roy. Soc. Trop. Med. Hyg. 52: groups, host species and populations (Appendix 15.1). 309-328. Aznar, F.J., Balbuena, J.A., Fernández, M. & Raga, J.A. 2002. Baseline data provide a way to identify trends in host and Living together: The parasites of marine mammals. In: P.G.H. geographic distribution or abundance, which may reflect Evans & J.A. Raga (eds.). Marine Mammals: Biology and Con- changing ecological conditions. There is a distinction be- servation, pp 385-423. Kluwer Academic, New York. tween numerical trends (difficult to acquire), versus fau- Babbot, F.L. Jr., Frye, W.W. & Gordon, J.E. 1961. Intestinal nal trends, or evidence of range shifts and development parasites of man in Arctic Greenland. Am. J. Trop. Med. Hyg. 10: 185-190. of new host-parasite associations. Both may be indicators Baer, J.G. 1956. Parasitic helminths collected in West Greenland. of shifting patterns of abundance for host organisms Medd. Grønland 124(10): 1-55. where host density is a factor that directly influences the Belogurov, O.I. 1966. Helminth specificity with respect to defini- potential for expansion and successful establishment by tive hosts. Interrelationships of the helminth fauna of the ani- parasites (Skorping 1996, Marcogliese 2001a, Hoberg mals belonging to different orders (by the data collected along the coast of the Okhotsk Sea). Zool. Zhurn. 45: 1449-1454. 2010). Consequently, our recommendation is that field [in Russian] biologists exploring populations of fishes, birds or mam- Belopol’skaya, M.M. 1952. Parasite fauna of marine waterfowl. mals incorporate parasitology as an integral component Scientific Proceedings of the Leningrad University (Uchenie of their research and management programs. If verte- Zapiski Leningradskogo Universiteta) 141, ser. Biol. 28: 127- brate populations are worthy of monitoring because 180. [in Russian] Belopol’skaya, M.M. 1953. Helminthofauna of USSR shorebirds. of their perceived and real value, then parasites should In: A.M. Petrov, (ed.). Contributions to Helminthology to concurrently be of equal importance because of what Commemorate the 75th birthday of K.I. Skrjabin, pp 45-65. they reflect about the state of the biosphere. Izdatel’stvo Akademii Nauk SSSR, Moscow [English Transla- tion, 1966, Israel Program for Scientific Translations, Jerusa- lem] Belopol’skaya, M.M. 1959. The parasite fauna of limnicoline birds ACKNOWLEDGEMENTS along the shores of the Sea of Japan and the Barents Sea. In: Y.I. Polyanski (ed.). Ecological Parasitology, pp 22-57. Leningrad Perspectives presented in this assessment by EPH and University, Leningrad. [in Russian] JAC are a contribution from the Beringian Coevolution Belopol’skaya, M.M. 1963. Helminth fauna of sandpipers in the Project, supported by the National Science Foundation lower region of the Amur in the period of flight and nidulation. Trudy. Gel. Lab. 13: 164-195. [in Russian] (US) (DEB 0196095, 0415668, 1258010 and 1256832). Belopol’skaya, M.M. 1979. Cestodes of waders in the family Dile- SJK was supported in part by the Climate Change Action pididae Fuhrmann, 1907. Vest. Leningrad. Univ. 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