PARASITES (Chapter 15)

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

SUMMARY

Parasites are among the most common organisms on the planet, and represent diverse members of all biological communities. Parasites tie communities together, revealing or telling stories about critical connections established by a history of evolution, ecology (food habits, foraging behavior, interactions among host species) and biogeography (patterns of geographic distribution) for host populations, species, ecosystems and regional faunas that constitute the biosphere. As such these organisms tell us about the processes, biological (e.g. range shifts, invasion) and physical (e.g. climate variation), that have determined the patterns of diversity that we observe in high latitude ecosystems.

Parasites can have subtle to severe effects on individual hosts or broader impacts on host populations which may cascade through ecosystems. Parasitic diseases have dual significance:

• influencing sustainability for species and populations of invertebrates, fishes, birds and mammals; and
• secondarily affecting food security, quality and availability for people.

As zoonoses, some parasites of animals can infect and cause disease in people and are a primary issue for food safety and human health. Sustainability, security and safety of ‘country foods’ are of concern at northern latitudes where people maintain a strong reliance on wildlife species.

In the Arctic, we often lack baseline and long-term data to establish trends for parasite biodiversity (host and geographic distributions or numerical measures of abundance and prevalence) in terrestrial, freshwater and marine systems, even for the best known host species. Absence of biodiversity knowledge has consequences for understanding the role of parasites in an ecosystem, and patterns of emerging animal pathogens, including zoonotic diseases, at local to regional scales. There is urgent need to incorporate parasitological information into policy and management plans and to emphasize awareness of parasitic diseases to wildlife managers, fisheries biologists, public health authorities and local communities.

I’ve seen that in caribou. Just a couple of years ago, every slice through it, you’d see about 50 little white round things. We were wondering what that was, so we checked it out, and it was a tapeworm. The whole body was completely filled with tapeworms. Yeah. It’s unbelievable how they could actually still move and run and their whole body just completely filled with tapeworms.
Village elder, Sachs Harbour, Canada, as related to S.J. Kutz.

Parasitological knowledge can be incorporated into policy and management plans through an integration of field-based survey, local knowledge, development of baselines linked to specimens, archival data resources to assess change, and models that can predict potential spatial and temporal distribution for outbreaks of disease among people or animals human. We recommend that parasites be considered particularly as they relate to biodiversity and conservation of populations, availability of subsistence food resources and concerns for food security and food safety (i.e. zoonoses and wildlife population declines caused by parasites). Further, research is necessary to demonstrate linkages among climate change, environmental perturbation, shifting abundance and range for hosts, and emergence of parasites and disease. These facets are essential to our capacity to predict future shifts in ecosystem structure over time, to develop adaptations, and to mitigate or prevent disease outbreaks among human and wildlife populations.

INTRODUCTION

Parasites represent in excess of 40-50% of the organisms on Earth and are integral components of all ecosystems (Dobson et al. 2008). Vertebrates and invertebrates are hosts for complex assemblages of macroparasites (worms and arthropods including insects) and microparasites (viruses, bacteria, fungi and protozoans) that shape ecosystems, food webs, host demographics and host behavior (e.g. Marcogliese 2001a, 2005, Hudson et al. 2006, Dobson et al. 2008). Surprisingly, in some ecosystems the biomass of parasites exceeds that of apex predators such as birds and fishes, and these otherwise obscure organisms have extraordinary ecological connectivity with involvement in over 75% of trophic links within food webs (Lafferty et al. 2006). A substantial role in nutrient cycling and trophic interactions at local to regional scales is evident for these assemblages of parasites (Kuris et al. 2008).

Parasites are taxonomically complex and diverse, even in high latitude systems characterized by relatively simple assemblages, and are considerably more species-rich than the vertebrate hosts in which they occur. For example, consider the 62+ described species of helminths, arthropods and protozoans, not to mention viruses and bacteria, which circulate in four species of ungulates across high latitudes of North America and Greenland (Kutz et al. 2012). Among 19 of 24 species of relatively specialized auks (seabirds of the family Alcidae) there are in excess of 100 species of helminths and arthropods in addition to viruses, bacteria and protozoans (Muzzafar & Jones 2004). Among the five species of loons (Gaviiformes) there are 97 species of helminths and among Holarctic grebes (three species of Podiceps), all of which breed at high latitudes, there are 145 species of helminths which contrasts with 244 among all podicipediforms in the global fauna (Storer 2000, 2002). Further, in a single fish species, Arctic char Salvelinus alpinus, there are over 100 known species of helminths and protozoans (Dick 1984, Wrona & Reist, Chapter 13). These observations emphasize the broad distribution of parasites across and within ecosystems in terrestrial and aquatic environments. Considerable complexity and knowledge gaps, however, suggest that it is currently intractable to develop a synoptic picture for trends in abundance or diversity across phylogenetically disparate assemblages of vertebrate hosts (fishes, birds and mammals) and their parasites extending from regional to landscape scales. As an alternative, we highlight a series of exemplars demonstrating the importance of parasites both conceptually and functionally as integral components of high latitude ecosystems. Our discussion explicitly explores the distribution of metazoans (helminths) and protozoans circulating in fishes, birds and mammals, and to a lesser extent some parasites that are recognized as zoonotic pathogens; we do not examine the diversity and distribution of viruses, bacteria, parasitic fungi (in animals or plants; but see Dahlberg & Bültmann, Chapter 10), or arthropods in parasitic and mutualisitc associations.

He’s saying that when we go harvesting caribou, moose, whatever, when we’re skinning them, we really watch out for all these things. The insides, and that yellow stuff they’re talking about; it’s like a doctor looking at things. Like when you take the stomach out, you always look on the inside. You look at the liver; you look in the flesh. Like when they bring the meat home and when the women make dried meat, sometimes they find those little white like beans in the meat. That’s what we eat, so when we skin something we have to make sure to look at everything – the heart, the lungs, the liver, the stomach, the kidney. Village elder, Fort Good Hope, Canada, as related to S.J. Kutz.

Parasites can cause disease and mortality, influence the dynamics and regulation of host populations, mediate competition among hosts which determines community structure, and in the worst case scenarios contribute to extinction events for hosts. Circulation of parasites is based on specific pathways that represent links among hosts and the environmental settings where they occur (Fig. 15.1). Some parasites have direct transmission cycles that involve passage between definitive hosts where the adult parasite develops and reproduces. Often, the infective stages will occur free in the environment, sensitive to ambient temperature, humidity, salinity and light (including ultraviolet), and are acquired by hosts through ingestion of water or forage. In contrast, indirect transmission is often related to connections established through foraging and food habits where predators (definitive hosts) are infected through ingestion of prey (intermediate hosts where the parasite develops). Significantly, trophic structure in the Arctic involves an unusually great percentage of predators and relatively fewer herbivores (Callaghan et al. 2004a). Predator-prey interactions are among the dominant trophic links in high latitude systems where small to medium mammalian and avian predators often specialize on voles and lemmings in terrestrial environments; many shorebirds specialize on aquatic invertebrates in either marine or freshwater habitats (most often terrestrial/freshwater in the breeding season and marine in the non-breeding season). Consequently, parasite life cycles and transmission are directly influenced by fluctuations in abundance and density for both predators and prey species. Alternatively, indirect life cycles may involve vectors, usually biting flies or other arthropods such as ticks, which disseminate the parasites among hosts. In the Arctic, the ambient environmental setting (temperature, humidity, seasonality, geography, host diversity, density and abundance) dramatically influences the survival, development, abundance and distribution of parasites and 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).

Parasites have predictable associations with their hosts and consequently serve as indicators of ecological structure, biogeography and history in complex biological systems (e.g. Hoberg 1996, Marcogliese 2001a, Nieberding & Olivieri 2007, Hoberg & Brooks 2008, 2010, Morand & Krasnov 2010). As succinctly outlined by Marcogliese (2001a): “… Parasites may be excellent indicators of biodiversity. This idea follows from the very nature of parasite lifecycles. Many parasites have a variety of intermediate hosts and often depend on predator-prey interactions for transmission. A single parasite in its host reflects the presence of all the hosts that participate in its life cycle. All the parasite species occurring in the host (the parasite community) reflect the plethora of life cycles represented by the different parasites and all the associated intermediate and definitive hosts. In this way parasites are indicative of food-web structure, trophic interactions, and biodiversity. … They thus reflect long-term persistence and stable interactions in the environment.”

rectly complement our knowledge about the historical processes that have served to determine the structure of faunas, and the role of episodic shifts in climate that have influenced dispersal, isolation and speciation during the late Tertiary and Quaternary periods, approximately 3-3.5 million years ago to present (e.g. Rausch 1994, Hoberg et al. 2003, Cook et al. 2005, Hoberg 2005a, Zarlenga et al. 2006, Waltari et al. 2007a, Koehler et al. 2009). Contemporary diversity in aquatic and terrestrial environments has largely been determined by events that unfolded during the Pleistocene. For example, most groups of parasites now distributed in terrestrial mammals across the circumpolar region had origins in Eurasia and secondarily expanded into North America during glacial stages coinciding with lowered sea-levels that exposed the Bering Land Bridge, the primary pathway linking Siberia and Alaska (Rausch 1994, Waltari et al. 2007a, Hoberg et al. 2012). Alternating episodes of rapid climate change from glacial to interglacial cycles resulted in expansion, geographic isolation and diversification in diverse host-parasite systems, both between Siberia and Alaska, and also within North America and Greenland (e.g. Stamford & Taylor 2004, Waltari et al. 2007a, Shafer et al. 2010, Galbreath & Hoberg 2012). In parallel to terrestrial and freshwater systems, patterns of diversity are also reflected in the history and distribution of parasite faunas in marine birds, mammals and fishes that were influenced by isolation or expansion between the North Atlantic and North Pacific basins through the Arctic Ocean and Bering Strait (e.g. Polyanski 1961a, Hoberg 1995, Hoberg & Adams 2000, Briggs 2003). These observations highlight the idea that the ‘past is the key to the present’, with history providing a pathway or analogue for predicting how complex host-parasite systems will respond in a regime of accelerated environmental change over time (Hoberg 1997).

CONCLUSIONS AND RECOMMENDATIONS

New tool development

Knowledge of parasite diversity, particularly definitive identification, geographic distribution and host association, is critical as a foundation for understanding the potential for pathogen dissemination and disease (Brooks & Hoberg 2000, 2006, Hoberg 2010). Achieving this goal requires field-based research, networks with local capacity, scientific and local community engagement, coordination and collaboration to facilitate collections, plus methodologies that provide timely or rapid identification of parasites. Parasite collection and identification has often been a laborious process dependent on special expertise and knowledge of specific taxonomic groups. Collections were often logistically difficult (e.g. ungulates or marine mammals) where the necessity of field-based necropsy to recover adult parasites often limited the geographic scope and numbers of host specimens that could be examined. Molecular-based methods increasingly complement microscopic identification, and such approaches for the first time provide a means for geographically extensive and site-intensive sampling for parasite diversity that does not always have to rely directly on necropsy (e.g. Jenkins et al. 2005, Kutz et al. 2007). These and other non-invasive, ‘field-friendly’ methods enhance data and sample collection and storage by hunters, substantially increasing the capacity to rapidly assess diversity and epidemiology of parasites across large landscapes and regions (e.g. blood filter-paper; Curry 2009), and fecal sampling for parasitic eggs and larvae in conjunction with DNA amplification and sequencing (Jenkins et al. 2005, Huby-Chilton et al. 2006, Kutz et al. 2007, DeBruyn 2010). Additionally, definitive identification of many microparasites such as species of Giardia, Toxoplasma, Besnoitia and others is not feasible in the absence of molecular methodology (e.g. Criscione et al. 2002, Polley & Thompson 2009). The latter is increasingly important in identifying the sources and pathways for human infection from stages of parasites acquired through water or food contamination mediated by wildlife (Polley & Thompson 2009).

Documentation of parasite diversity is a continuum that includes:

• targeted taxonomic studies on single parasite species and simple case reports in individual hosts,
• surveys for parasites in single host species at a limited spectrum of localities,
• survey and inventory at the ecosystem level based on standardized and comprehensive sampling protocols implemented on broad geographic scales, and
• integrated inventory for hosts and parasites with application of population genetic approaches and phylogeography to explore relationships at fine temporal and spatial scales (see Cook, Chapter 17).

Ecosystem approaches for survey (and surveillance) are necessary as the distribution of a parasite is generally broader than the distribution of disease (Audy 1958), and outbreaks may represent geographic (and host) mosaics that are ephemeral in space and time (Thompson 2005, Hoberg 2010). Geographic coverage from local landscapes to regions is thus a foundation for establishing patterns of abundance and circulation for parasites. Further, such surveys should contribute directly to the development of archival biological collections (parasites, hosts, tissues and biodiversity informatics) held in museum repositories as a baseline for diversity and faunal structure (Fig. 15.2) (Brooks & Hoberg 2000, Hoberg et al. 2003, 2009).

The Beringian Coevolution Project (BCP), initiated in 1999, represents a primary model for integrated survey and inventory of northern fauna (Hoberg et al. 2003, Cook et al. 2005). The BCP was designed to:

• provide a detailed and geographically widespread resource of museum specimens from key high-latitude areas that had not been inventoried,
• develop a comparative framework for Beringia to examine the history of host-parasite systems that are phylogenetically and ecologically disparate, providing the basis for detailed studies in coevolution and historical biogeography,
• explore large-scale physical (climate variation) and biotic forces that have structured high-latitude biomes, including drivers of intercontinental faunal exchange across the North, and
• build a spatial and temporal foundation at fine scales for investigations of Arctic biodiversity by identifying regions of endemism and contact zones between divergent lineages while exploring fundamental mechanisms that determined faunal diversity within complex biotic systems.

The BCP has resulted in extensive archival collections of host and parasite specimens, including whole vouchers, tissues and DNA products from approximately 18,000 small mammals (primarily rodents, soricomorphs, lagomorphs and mustelids representing 80 species and 31 genera, with additional materials from high latitude ungulates) across 250 sites spanning > 100° longitude and > 25° latitude in Siberia, Alaska and Canada. Specimens and information are housed in permanent museum repositories including the Museum of Southwestern Biology, University of New Mexico, the University of Alaska Museum of the North and the US National Parasite Collection (Cook et al. 2005). A crucial foundation and unique baseline of information for hosts and parasites is emerging and under current evaluation for basic research and conservation in the face of changing climate and increasing anthropogenic impacts at high latitudes (Arctos 2012).

In parallel, the International Polar Year (2007-2008) provided the opportunity to focus on health, status and population trends for caribou and reindeer through the CircumArctic Rangifer Monitoring & Assessment Network (CARMA). From 2007 to 2009, this network developed and implemented standardized sample and data collection protocols to evaluate the body condition, demographics and health of multiple herds in North America, Greenland and Russia. CARMA also built on existing programs (Brook et al. 2009) to develop training materials to facilitate hunter-based health monitoring for caribou. Development of locally supported, effective and efficient monitoring programs that can provide long-term data are dependent on assessing protocols and by adapting methods that are most appropriate at the community level across region.

Another mechanism for ongoing parasite monitoring is through local programs. For example, due to food safety issues, the Nunavik Trichinellosis Prevention Program was established in Kuujjuaq, Quebec (formerly Fort Chimo) by the Nunavik Research Centre (Proulx et al. 2002). This program serves to monitor prevalence, intensity and geographic distribution of Trichinella in walrus from Nunavik. Such a program may have general applicability across the Arctic given ongoing perturbation at the ecosystem level and projected changes for the distribution of Trichinella in marine mammals (Rausch et al. 2007).

The importance of efforts to improve methodologies that facilitate sample and data collection in the field cannot be overestimated. The Arctic continues to be a logistically challenging region for field biology and assessment of pathogens and the distribution of disease. As much as is possible, knowledge of parasite diversity should be linked directly to specimen-based information. The primary cornerstone will be integrated survey and inventory supporting surveillance (active systems designed to discover general patterns of abundance, prevalence or incidence) and monitoring (ongoing assessments of health status of specific animal populations) (Salman 2003) that contributes to archival collections (parasites, hosts and tissues) as a permanent record of environments in dynamic change (e.g. Hoberg et al. 2008b, Cook, Chapter 17). Such archival resources, as self-correcting records of biodiversity, will be increasingly important in the arenas of ecosystem sustainability, human health and conservation (Hoberg et al. 2003, Koehler et al. 2009, MacDonald & Cook 2009).

Anticipated important host-parasite assemblages and processes

The presence of diverse assemblages of parasites is indicative of a healthy ecosystem (Marcogliese 2005, Hudson et al. 2006). The presence of parasites is an indicator of ecosystem stability and the connections that fishes, birds, mammals and invertebrates have within and across complex foodwebs in aquatic and terrestrial environments (Lafferty et al. 2006, Amundsen et al. 2009). Following from this complex web of interactions, parasites tell stories about where host individuals, populations and species have been (in migration), what they eat and where they spend their time. Consequently, perturbations in ecosystems are often reflected in the diversity and spectrum of parasites that occur at landscape to regional scales (Hoberg 1996, Marcogliese 2001). These relationships serve to indicate the importance of understanding parasite diversity in space and time (Hoberg 1997, Brooks & Hoberg 2000).

The biodiversity crisis is not simply an issue of ecosystem perturbation and species loss, but also one of emerging infectious diseases in both wildlife and people (Daszak et al. 2000, Brooks & Hoberg 2006). Fundamental to either an invasion or emergence of parasites is breakdown in environmental structure or ecological isolation driven by natural or anthropogenic processes (e.g. Elton 1958, Hoberg 2010). Ecological disruption with the development of new borderlands or ecotones is also central to the process for expanding host and geographic ranges for assemblages of parasites. Analogues based on historical processes for episodes of climate change can serve to inform us about how complex host-parasite systems in the Arctic have been structured by events in the Quaternary Period during the last 2.6 million years (e.g. Rausch 1994, Hoberg et al. 2003, 2012). Dispersal, range shifts, colonization of new geographic regions and switching of parasites among host species and within ecosystems are fundamental characteristics of northern systems and these mechanisms are equivalent in evolutionary and ecological time (Hoberg & Brooks 2008, Hoberg et al. 2012). The nature of invasion and emergence, however, suggests that it not always simple to predict how assemblages of hosts and parasites will respond to transitional conditions, particularly those associated with accelerated climate change in contemporary northern systems (Marcogliese 2001a, Hoberg et al. 2008a, 2008b, Kutz et al. 2009a, 2012, Hoberg 2010, Gilg et al. 2012). These factors heighten the need for comprehensive surveys to establish baseline faunal associations for poorly known hosts or among host-groups identified as keystones within specific ecosystems (Appendix 15.1). Application of model-based approaches, particularly ecological niche modelling, in conjunction with detailed records from archival collections can also contribute to an understanding of the consequences of environmental change on the distribution of parasites and disease (e.g. Waltari et al. 2007b, Waltari & Perkins 2010).

Establishing baselines for diversity is central to identifying the role of parasites in an ecosystem, among host groups, host species and populations (Appendix 15.1). Baseline data provide a way to identify trends in host and geographic distribution or abundance, which may reflect changing ecological conditions. There is a distinction between numerical trends (difficult to acquire), versus faunal trends, or evidence of range shifts and development of new host-parasite associations. Both may be indicators of shifting patterns of abundance for host organisms where host density is a factor that directly influences the potential for expansion and successful establishment by parasites (Skorping 1996, Marcogliese 2001a, Hoberg 2010). Consequently, our recommendation is that field biologists exploring populations of fishes, birds or mammals incorporate parasitology as an integral component of their research and management programs. If vertebrate populations are worthy of monitoring because of their perceived and real value, then parasites should concurrently be of equal importance because of what they reflect about the state of the biosphere.