FUNGI (Chapter 10)

Lead Authors:  Anders Dahlberg and Helga Bültmann 

Contributing Authors: Cathy L. Cripps, Guðríður Gyða Eyjólfsdóttir, Gro Gulden, Hörður Kristinsson and Mikhail Zhurbenko

SUMMARY

Golden coloured blackening waxcap.Photo: Flemming Rune Fungi are one of the most species-rich groups of organisms in the Arctic. While the occurrence, distribution and ecology for lichenized fungi (lichens) are reasonably well known, less is known about non-lichenized fungi (normally just called fungi), including lichenicolous fungi (fungi living on lichens) and in particular, microfungi. The known number of fungal species in the Arctic is presently about 4,350, of which 2,600 are macrofungi and 1,750 are lichens, the rest are microfungi. The fungi have largely a cryptic life form and have therefore not been exhaustively inventoried. Hence, total fungal-species richness in the Arctic may exceed 13,000. Local species richness is typically high and can be very high, e.g. about 50 lichen species on less than 1 m². Most species appear to be present throughout the Arctic, and they also occur in alpine habitats outside the Arctic, particularly in the northern hemisphere. Few fungi are endemic to the Arctic. Of the lichens, 143 species are listed as Arctic endemics, but it is likely that the major part will prove to be synonyms of other species.

Fungi are pivotal in Arctic terrestrial food-webs. Mycorrhizal, saprotrophic and pathogenic fungi drive nutrient and energy cycling, and lichens are important for primary production. Reindeer lichens Cladonia subgenus Cladina spp. form dominant vegetation types in many areas and function as keystone species.

As for other inconspicuous organism groups, it is obviously desirable to gain a better knowledge of the identity, occurrence and functions of fungal species, and particularly the large number of unrecorded species (mainly microfungi). An evaluation of the conservation status of Arctic fungi is feasible, and the mapping of rare and endemic species is necessary. Enhanced monitoring and functional research would enable more accurate prediction of how fungal diversity and the ecosystem functions of fungi will develop with climate change.

Effects of climate change on diversity of Arctic fungi are predicted to be gradual but radical over time, due to changes in vascular plant flora and vegetation, especially the expansion of shrubs. Most fungal species associate with living or dead parts of specific vascular plants and will respond directly to changing composition, abundance and location of the vegetation. Similarly, terricolous lichen communities will be affected by increased competition from vascular plants. The changing vegetation will transform the fungal diversity and thereby affect ecosystem services provided by fungi, such as plant’s uptake of nutrients, decomposition and long-term carbon sequestration in soil, although unknown how and to what degree. The conservation status of Arctic fungi is predicted to scarcely be affected within the next decades but greatly changed over the long term.

I want to tell you something I learned about plants from the late Kakkik that I tried myself. My sister’s late husband used to know about nirnait, caribou lichen, the plants that caribou eat. They are long and you pull them out. They tend to grow in swampy areas. I boiled them when all the people in our camp were sick. I was the only one up and about when we were living in a fishing camp. My mother had been admitted to the hospital and we were waiting for her return in August. Six of my family members were sick in bed. I boiled some caribou lichen in a pot for a long time, following my brother in-law’s advice. He told me to stop boiling them when the water turned black. I waited for them to cool down and I gave each sick person some to drink. The next day, they were all up and about. It looked like the cough syrup in a bottle. Aalasi Joamie in Joamie et al. 2001.

INTRODUCTION

Fungi are an extraordinary group of organisms. They constitute a large portion of Arctic biodiversity and are essential in the functioning of Arctic terrestrial ecosystems. A substantial part of the fungi is lichenized and generally termed lichens. The remaining part of the fungi is in general terms just called fungi and will here be referred to as fungi. Given favorable weather conditions, some may produce short-lived, sometimes prominent, sporocarps (mushrooms), but predominantly, and for many species exclusively, they exist as cryptic and hidden mycelia in e.g. soil and in living or dead insect or plant tissues. The most well-known group of fungi in the Arctic is the lichenized fungi (lichens) because they grow on substrate surfaces and often contribute conspicuously, and colorfully, to Arctic vegetation. This is particularly apparent in the high Arctic and in reindeer lichen-dominated vegetation types in the sub-Arctic.

Here we review the knowledge and status of Arctic macroscopic fungi, i.e. visible sporocarps of fungi, and lichens. Microfungi constitute the most species-rich fungal group in the Arctic, but are only briefly mentioned due to scarcity of knowledge.

CONCLUSIONS AND RECOMMENDATIONS

Fungi is a key group of organisms with high species richness and large significance for ecosystem processes in the Arctic. Except for macrolichens, however, their presence and significance has often been overlooked and poorly appreciated in the Arctic, despite being species rich, abundant and pivotal in carbon and nutrient cycling. Distributional and ecological knowledge is reasonably good for macrolichens but sparser for fungi and microlichens.

Even with these caveats, present knowledge largely enables us to predict the future of Arctic fungi. The unavoidable greening of the Arctic will steadily and significantly affect the distribution and abundance of fungi, as habitat conditions gradually transform the distribution and abundance of plants. This change is in progress already, but studies of Arctic soil fungal communities imply that the response as yet is relatively slow (Timling & Taylor 2012). Therefore, we judge that these changes will only rarely affect their conservation status in the immediate future. However, over time the effects of climate change and subsequently transformed vegetation will have profound effects on the distribution and composition of fungi and consequently also their ecosystem functions. Most of the species are circumpolar and also distributed outside the Arctic. However, a large proportion of them are confined to Arctic-alpine habitats of which the greater part is located within the Arctic and few are true Arctic endemics.

The following actions would enable a more thorough analysis of the status and trends of Arctic fungi.

• Long-term funding is necessary to maintain and train Arctic specialists in mycology and lichenology and to ensure research and monitoring to take place.
• The identity and taxonomy of species with unclear status (e.g. poorly known fungi and potentially endemic lichens) should be critically examined. The large potential of fungal analysis of deep sequenced environmental samples will largely benefit by clarified fungal taxonomy.
• A checklist for Arctic fungi should be compiled.
• The knowledge of distribution and ecology for all fungi, but in particularly for non-lichenized fungi, should be improved.
• Conservation status should be assessed for Arctic lichens and fungi, preferentially at both the Arctic and global scales.
• Long-term monitoring within representative Arctic habitats would enable us to document and follow fungal species shifts over time.
• Analyses of how vegetation changes may, based on knowledge of fungal ecology, predict potential habitats for fungi in space and time.
• Efforts to analyze the effects of slowly shifting fungal communities on ecosystem processes such as nutrient cycling and carbon fluxes are needed.
• Analyses of how the supply of reindeer food lichen communities will alter due to vegetation change should be conducted in order to better predict future conditions for populations of reindeer/caribou.

MICROORGANISMS (Chapter 11)

Lead Author:  Connie Lovejoy

SUMMARY

Microorganisms. Photo: Connie Lovejoy

Microbes, defined here as Bacteria, Archaea and singlecelled Eukaryota (protists) are ubiquitous and diverse members of all biological communities. In marine and many freshwater systems, photosynthetic microbes form the base of the food chain supporting higher trophic levels. Among the photosynthetic species are biologically diverse small flagellates that also graze on bacteria and other protists and hence are functional heterotrophs at times. Strictly phagotrophic protists are also diverse and contribute to the complexity of microbial food webs, with a multitude of trophic interactions. The fate of Arctic primary production emerges from the assembly of the entire microbial community. Heterotrophic bacteria break down fixed organic carbon and recycle nutrients, while other bacteria and Archaea with diverse metabolic capacities are active in the remineralization of carbon, nitrogen and other elements. There is a lack of longterm comprehensive baseline data on microbial biodiversity in terrestrial, freshwater and marine systems that largely impedes understanding ecosystem structure and resilience over both local and regional scales.

Because of their small size and often large populations, microbes in principle may have global distributions as they are transported by moving masses of air and water. Microbial communities are strongly selected for by their immediate environment, and successful global transport will be influenced by the ability of organisms to remain viable during transport between favorable environments. Species are more likely to have geographically restricted distributions if they lack a dormant stage or are specialists, and if their preferred environments are rare and distant from each other. Local communities may also resist invasions in the absence of physical or ecological perturbations that would give invading species or ecotypes an advantage. In the absence of ice cover, increased light availability and increased water column stratification can influence microbial community structure, affecting both phototrophic and heterotrophic species. Both the duration of the productive season and the species composition of protists have implications for higher food webs, thus ecosystem services by microbes are of direct relevance to wildlife and fisheries biologists as well as local communities. In addition, microbial community interactions largely determine the efficacy of the biological carbon pump.

The diversity of heterotrophic protists and other microbes is largely unknown, since for the most part they cannot be identified morphologically. Hence, sound historical records are lacking. New tools are being used to identify these heterotrophs from their DNA and RNA collected from the environment. Even among larger species of phytoplankton, cryptic species have been identified from DNA sequences. The small sub-unit ribosomal RNA (SS rRNA) gene is the most common target for gene surveys and enables the identification of microbes at the level of genus and even species and ecotype for some groups. In addition, genomic and transcriptomic signatures of microbes from the Arctic will provide valuable insight into the resilience and capacity of Arctic ecosystems. The recent rapid advances in sequencing technology will enable the expansion of microbial surveys, facilitating the integration of microbial biodiversity data into coupled biogeochemical climate models. Further, monitoring could provide the means to test whether there are linkages between climate change, environmental perturbation and the emergence of southerly species, enabling robust projections about dynamic shifts in ecosystem structure over time. For these reasons there is an urgent need to increase knowledge of microbial communities at the finest taxonomic and functional levels.

INTRODUCTION

Microbes represent the majority of biodiversity on Earth and are integral components of all ecosystems. In terms of numbers, microbes also dominate with c. one million cells per milliliter (ml) of seawater and most freshwaters. Marine sediments host an even more impressive number of bacterial cells per ml (in the order of 1 billion). Sea ice also harbors distinct microbial communities that live within brine channels and at high local concentrations (Deming 2002). Distinct communities can be found attached to the bottom of first year ice and occurring in surface melt ponds (Mundy et al. 2011). Concentrations of bacteria in Arctic soils are less than in temperate soils, but can still reach substantial numbers in key microhabitats (Yergeau et al. 2010, Wilhelm et al. 2011). Although heterotrophic protists and other microbes are the primary drivers of marine food webs and play key roles in freshwaters and soils, they are rarely included in general assessments of biodiversity (Archambault et al. 2010).

As reported in other chapters, climate and environmental change is rapidly reshaping northern ecosystems. These perturbations include the loss of summer ice, changes in the annual production cycle and changes in the depth of the most biologically active layers in both pelagic water columns and soils. Such environmental changes will have a direct effect on visible animals and plants (Falk-Petersen et al. 2009) and also have direct impact on the microbial food webs that support higher trophic levels.

In addition, as mentioned in other chapters, terrestrial and aquatic habitats merge over much of the sub-Arctic and Arctic. Distinct ponds and lakes are formed in polygons and runnels surrounding polygons within the permafrost and in the high Arctic water increasingly remain as ice over the year. Deeper lakes are also scattered throughout the Arctic, and the microbial community structure of ponds and lakes is influenced by their depth, catchment area, orientation and underlying basin geology. Freshwater microbes are poorly studied with only sporadic reports of species. Most surveys of soil microbes have focused on disturbed sites with few reports on the microbes from pristine regions (Steven et al. 2008a, Martineau et al. 2010, Niederberger et al. 2010, Wilhelm et al. 2011). In this chapter, I provide a brief summary of existing knowledge, identify key gaps and suggest strategies for monitoring microbial biodiversity.

CONCLUSIONS AND RECOMMENDATIONS

Sensitive areas and hotspots

In the terrestrial and freshwater habitats, areas identified either as sensitive or as hotspots for animals and plants should also be considered as microbiologically significant regions. In addition, unique or rare habitats such as saline springs should be protected to preserve unique biomes and specialized microbiota. In coastal and oceanic regions, areas where mammals and birds congregate should also be monitored. For example, marine productivity is related not only to the quantity of photosynthetic biomass produced but also the quality. In oceanic regions, the diversity and stability of microbial food webs dictates lipid concentrations in the zooplankton that support higher trophic levels. As longer ice free periods become the norm, microbial food chains are predicted to lengthen, and less energy will be available to the highest trophic levels in the oceans (Lovejoy 2011). Such changes will also have major impacts on benthic communities and on the carbon and nutrient cycling that occurs in the benthos (see also Josefson & Mokievsky, Chapter 8). The potential loss of multiyear ice as a habitat and changes in the duration and type of sea ice with different communities (Comeau et al. 2012b) will have consequences for biodiversity and carbon cycling. More research is needed to better estimate which com communities may be lost as a result of the loss of summer sea ice. These changes are likely to have significant effects on the diversity and functioning of Arctic ecosystems. In terrestrial based systems, increased liquid water, higher temperatures and longer growing seasons will affect all biological activity, and northward expansion of species can be expected. Although at present much of the Arctic appears poor in life, microbial communities are active and complex, and ‘non-hot spot’ regions need to be monitored as well as highly productive regions in order to anticipate new distributions and community associations. Microbes will respond to ecosystem changes much sooner than higher plants and invertebrates and are thus sensitive indicators of directional changes.

Key knowledge gaps and recommendations

Ecosystem assessments and the role of complex interacting factors, which may influence ecological patterns, can only be explored through long time series of biological collections and surveys at local to regional scales. The only open-ocean long-term observatory in the Arctic is HAUSGARTEN, coordinated by the Alfred Wegener Institute for Polar and Marine Research (Soltwedel et al. 2005; see also Josefson & Mokievsky, Chapter 8). The Arctic is vastly under-sampled and heterotrophic protists, Bacteria and Archaea play a critical role in ecosystem support. Currently, there are only a small handful of researchers interested in microbial biodiversity and how it directly relates to ocean ecosystem function. There is a need to foster greater interest in microbial ecology among Arctic researchers. Microbial communities must be included in any Arctic monitoring effort aimed at understanding biodiversity and ecosystem function.

TERRESTRIAL ECOSYSTEMS (Chapter 12)

Lead Authors: Rolf A. Ims and Dorothee Ehrich

Key Contributing Authors: Bruce C. Forbes, Brian Huntley, Donald A. Walker and Philip A. Wookey 

Contributing Authors Dominique Berteaux, Uma S. Bhatt, Kari A. Bråthen, Mary E. Edwards, Howard E. Epstein, Mads C. Forchhammer, Eva Fuglei, Gilles Gauthier, Scott Gilbert, Maria Leung, Irina E. Menyushina, Nikita Ovsyanikov, Eric Post, Martha K. Raynolds, Donald G. Reid, Niels M. Schmidt, Audun Stien, Olga I. Sumina and Rene van der Wal

SUMMARY

Photo: Susan Morse

The Arctic tundra biome is geographically restricted to a strip around the margins of the Arctic Ocean. A key force determining the tundra biome’s zonal structure is the bottom-up effect of decreased vegetation productivity and complexity with increasing latitude. Accordingly, there are trends of decreasing diversity within and among trophic guilds of consumers with increasing latitudes. Low food web complexity in the northern parts of the biome is also due to island biogeographic features, as large parts of the high Arctic are located on islands. Similarly, a substantial proportion of the high biodiversity of low Arctic zones stems from ‘spillover effects’ from sub-Arctic ecosystems. Historic processes have also contributed to shaping the current large-scale Regional provinces in terms of Arctic species communities. At sub-regional scales the terrestrial Arctic harbors diverse mosaics of communities that are structured by gradients and disturbances in climate, substrate, hydrology and cryosphere that form unique patterns of within – and among – community diversity. Hot spots of high regional diversity are currently found in some old, topographically and geologically complex regions.

It has progressively become warmer. I recall that only in our traditional area did the trees occur, but when I returned there via plane last year, a lot more of the tundra was inundated with trees, small mind you, but they have moved north and east. The area we used to inhabit has been overgrown with vegetation, mainly shrubs and small trees. It has become almost like a mini-forest where we used to have our main camp. We visited the site in 2000 and it was almost unrecognizable due to all of the growth that occurred during our absence. I think this is due to a shorter spring, a longer summer and longer frost free falls. Utok; Elders Conference on Climate Change 2001.

The architecture of tundra food webs is modulated by inter-specific interactions within and between trophic levels. Herbivores can regionally exert strong top-down controls on tundra vegetation, whereas predators often control small mammal herbivores and the reproductive success of ground nesting birds. Multi-annual, cascading bottom-up and top-down interaction cycles mediated by lemming populations are crucial for the maintenance of terrestrial Arctic biodiversity in many tundra ecosystems. Functional traits of plants in interactions with below-ground microbial communities and herbivores maintain essential roles in the regulation of the global climate system through controls on fluxes of greenhouse gasses (GHG) and heat fluxes between the earth surface and the atmosphere. Changes to the composition of terrestrial biodiversity may determine whether the Arctic will become a source or a sink for GHGs in a warming climate.

Climate is historically and currently the most important driver of change of Arctic terrestrial ecosystems, through alteration of coastal sea ice, glaciers, snow and permafrost, changed seasonality and extreme events. At present, a second emerging driver is an increased footprint of human presence within the Arctic. Currently, the most profound ecosystem impacts include (1) increased plant biomass due to growth of tall woody plants that cause lower albedo and possibly enhance GHG emissions and thereby accentuating the Arctic amplification of climate change, (2) collapsed cycles of lemmings and emergent Outbreaks of insect herbivores and plant pathogens with cascading impacts on food webs and ecosystem functioning, and (3) increasing abundance of boreal and human commensal species impacting Arctic endemics as predators or competitors. Recommended actions to conserve Arctic terrestrial ecosystems under the impacts of climatic change and other anthropogenic stressors include conservation of topographically diverse areas with landscape-scale ‘buffer-capacity’ to maintain cold refuges in a warmer climate and of remote high Arctic islands that are the most physically protected from species invasions from the south and human presence. Prudent management of Arctic herbivores such as reindeer Rangifer tarandus, using their capacity for shaping vegetation on landscape scales, may be considered for counteracting encroachment of tall woody vegetation that otherwise will eliminate tundra habitats, while avoiding the negative impacts of herbivore overabundance that have been documented in some regions.

A key message from the present assessment is that essential attributes of terrestrial Arctic biodiversity, some of which have global repercussions, are ultimately dependent on how interactions within ecological communities and trophic webs are impacted by rapidly changing external drivers. Consequently, research, monitoring and management ought to be properly ecosystem-based. Because ecosystems are structurally and functionally heterogeneous across the tundra biome and may also be subjected to external drivers of different strengths, new ecosystem-based observatories that include state-of-the art research, often combined with adaptive management, should be widely distributed across the circumpolar Arctic. Model-based predictions about how Arctic species and ecosystems will respond to the substantial climate change currently projected for the Arctic have limited powers to accommodate surprises in terms of novel climates and ecosystems that may rapidly emerge. New efforts urgently need to be deployed to enable well designed real-time observations as a basis for empirically based documentation and understanding of cause-effect relationships of future ecosystem changes in the terrestrial Arctic.

INTRODUCTION

The Arctic tundra biome is characterized by low-growing vegetation composed of low shrubs, sedges, grasses, forbs, lichens and mosses (bryophytes) that grow beyond the northern climatic limit of trees (see Section 2 in Meltofte et al., Introduction for this assessment’s definition of the Arctic). A polar view of the biome from space reveals that the continental portion of the Arctic tundra occupies a thin strip of land between the Arctic Ocean and the boreal forest (Fig. 12.1). Eighty percent of the lowland portion of the Arctic lies within 100 km of seasonally ice-covered seas. The biome essentially owes its existence to cold sea breezes that keep the temperatures during the growing season below that required for tree growth. One fifth of the total coastline of the world, or about 177,000 km, occurs in the Arctic, a biome that comprises only about 5% of the Earth’s terrestrial surface. Three main aspects of the extensive Arctic coastlines make the tundra biome extremely vulnerable to climate warming: (1) the strong climatic influence of the nearby sea ice, (2) narrow bioclimate zonation associated with these coastlines, and (3) extensive lowland plains near most of the Arctic coast (CAVM Team 2003).

In terms of climate, the Arctic tundra can be viewed as a strongly oceanic-influenced biome, but one that varies considerably in the degree of maritime expressions of cloudiness, fog, humidity and equitable temperatures, because the Arctic Ocean is covered by ice to a varying extent during the winter and summer. The longevity of the ice near the coast in summer strongly affects summer land temperatures and local continentality of the climate as well as the diversity of organisms and total productivity of the land (Bhatt et al. 2010). Steep temperature gradients occur inland from these coastlines resulting in extraordinarily long and narrow ecological transition zones with several bioclimate subzones compressed near the coast. Permafrost strongly affects the ecosystems of most of the biome, but is not a condition that defines the biome, as permafrost also extends far into the boreal forest in continental areas of Siberia and North America. On the other hand, there are portions of coastal tundra with no or only discontinuous permafrost (Callaghan et al. 2004a, AMAP 2011). 

The integrity of terrestrial Arctic ecosystems, as shaped by biotic and abiotic processes, is ultimately conditional on low primary productivity resulting from short and cool summers that restrict plant growth and metabolic activity of other poikilothermic1 organisms, such as bacteria, fungi and invertebrates. The low productivity at the base of trophic chains restricts secondary productivity and the complexity of food webs and decomposer webs. Tundra food webs are usually composed of only three major trophic levels: plants, herbivores and predators (Krebs et al. 2003, Ims & Fuglei 2005). The structure of decomposer webs, in which cryptic microbial communities and soil faunas play a central role, is considerably less known (Callaghan et al. 2004b), but may be more complex than the more conspicuous food webs composed of green plants and macroscopic animals (see Hodkinson, Chapter 7). Terrestrial food webs also include fewer trophic levels than, for instance, aquatic ecosystems in the Arctic (Wrona & Reist, Chapter 13, Michel, Chapter 14), although high Arctic limnic systems may be as simple as their terrestrial counterparts (van der Wal & Hessen 2009, Wrona & Reist, Chapter 13).

Although Arctic tundra ecosystems have a simple trophic structure, often with relatively low species richness within each trophic level, other structural features of biodiversity can be remarkably complex. Spatial variability in temperature, winds, precipitation, hydrology, cryosphere and soil chemistry creates gradients and complex mosaics of abiotic conditions that shape the composition of species assemblages (i.e. ecological communities) at multiple spatial scales. For this reason, a spatially hierarchical approach to characterize biodiversity patterns in terms of differences in species assemblages as functions of abiotic controlling factors from local to circumpolar scales appears to be particularly applicable to Arctic tundra. In terms of ecosystem functions, and the biotic and abiotic processes that shape these functions, tundra ecosystems are no less diverse than other ecosystems. Some of the ecosystem functions are crucial for the livelihood of local people, such as locally produced food, while others have essential roles in the global climate system, such as controls of exchange of heat and GHG.

In this chapter we start with a review of present knowledge of how natural abiotic and biotic factors shape biodiversity in terms of ecosystem structure, processes and functions within the tundra biome (Section 12.2). This provides the background for assessing past and present trends in terrestrial Arctic Biodiversity, and the drivers of such trends (Section 12.3). Towards the end of the chapter we provide a synthesis of the assessment’s key findings (Section 12.4) before we conclude with a set of recommendations on how policy makers, managers and ecosystem scientists could act on these findings (Section 12.5).

CONCLUSIONS AND RECOMMENDATIONS

Status and trends: Implications for the future

The Arctic tundra biome is a bio-climatically defined zone, the integrity of which is ultimately conditional on cold climates. Based on an extensive peer-reviewed literature, the present assessment testifies to the fact that all aspects of tundra ecosystems and their embedded biodiversity are shaped by past and current climates, although in conjunction with other environmental factors. This also means that future climate warming – in combination with other drivers of change – will fundamentally alter Arctic biodiversity. Indeed, our review of contemporary trends demonstrates that the tundra ecosystems have already changed as a result of recent climate warming as well as by intensified human land-use, including industrial development in certain areas.

Concerning the impacts of drivers of change in general and those related to climate warming in particular, the present assessment arrives at the following conclusions:

• Impacts of change are often indirect, both in the abiotic and biotic domains of tundra ecosystems.
• In the abiotic domain, climate warming exerts some of its most profound impacts through second-order disturbances in the cryosphere, such as ground surface icing (ROS) and permafrost thaw, or through drought-related increase of tundra fires.
• In the biotic domain, pervasive driver-impacts are mediated both by bottom-up and top-down cascades in trophic webs. Both types of cascades have recently been found ultimately to harm species endemic to the Arctic such as lemming-dependent predators and grazing-sensitive cryptogams.

Concerning the functioning of tundra ecosystems, new insights have emerged about the essential but complex roles of terrestrial Arctic biota in the evolution of regional-global climates:

• Ecosystem structure in terms of the composition of species guilds, communities and trophic webs may determine whether the terrestrial Arctic will become a future sink or source for GHGs, and whether it will strengthen or weaken the Arctic amplification of climate warming.
• The set of species traits that dominate in an ecological community is important for overall ecosystem functionality, implying that the processes involved in the global C cycle are not independent of the species (and functional traits) involved.
• An important overall message is that ‘the Devil is in the details’ regarding how terrestrial Arctic biodiversity interacts with climate change, which is indeed an argument for emphasizing Arctic biodiversity in climate research.

The tundra biome’s geographic configuration alone, as an irregular and in places very narrow strip of low-lands squeezed in between boreal forest and the Arctic marine environment, implies that the whole biome is vulnerable to climate change-related ‘edge effects’; i.e. species invasions from sub-Arctic Ecosystems (e.g. northward expansion of forests) and marine encroachment (erosion of coastlines and rising sea levels). Considering paleoecology, the whole biome can already be considered a refugium. Moreover, certain tundra subzones and regions may be particularly sensitive and vulnerable:

• The high arctic subzone A should be considered to be endangered. It is currently restricted to a very small area, about 2% of the non-glaciated terrestrial Arctic, mostly islands surrounded by perennial sea ice. An increase in July mean temperature of only 1-2 °C will permit the introduction of prostrate shrubs, sedges and other temperature-limited species. Disappearing sea ice may also change the levels of marine nutrient and production subsidies to the otherwise extremely nutrient/production limited high Arctic terrestrial food webs.
• The low Arctic subzones (D and E) are particularly vulnerable to increased pressures from range-expanding species with current strongholds in the sub-Arctic. Reported cases include boreal shrubs and trees, outbreaks of insect defoliators and meso-predators. ‘Human commensal’ meso-predators may also be synergistically enhanced by intensified land-use and expanding infrastructure/industries.
• Steppe-tundras that currently are confined to a few regions with continental climate and calcareous substrate are expected to be strongly affected by increased humidification of the climate and acidification of the substrate.

Conservation and management actions

The Arctic tundra biome is still characterized by relatively pristine ecosystems over large areas compared with other biomes on Earth. However, the impact of ongoing and future climate change is expected to be huge and represents the single most severe threat to terrestrial Arctic ecosystems. Moreover, there is significant spatial overlap with other stressors indicating that we must pay special attention to potential synergies. Area protection (reserves and national parks) will be an important means for preserving Arctic biodiversity in the era of climate change, especially since it will act to diminish synergistic impacts of local anthropogenic stressors and climatic warming. With regards to climate warming, there are certain biogeographical features that will make some areas particularly valuable for protection:

• Topographically diverse areas with mountain ranges that include landscape-scale climatic gradients may have ‘buffer-capacity’ to maintain cold refuges in a warmer climate.
• Remote high Arctic islands that are far north of southern bioclimate subzones and boreal ecosystems, and where Arctic marine waters will serve at least as a partial barrier (‘filter’) to invasions from the south. 

However, regardless of how remote and well-protected, no Arctic reserves or national parks will be immune to the impact of climate change. To conserve Arctic biodiversity it may be necessary to implement active management actions especially within protected areas:

• Encroachment of tall shrubs and trees into tundra can be counteracted, with the added benefit that plant community diversity can be maintained under future warming, by management of large herbivores as shown by recent research in Fennoscandia and Greenland. Such management needs to consider both the positive and negative effects of increasing grazing pressures, other ecological effects of high herbivore densities (e.g. subsidies to meso-predators) and the economies of local people (see Huntington, Chapter 18).
• Certain boreal species expanding their range northwards and anthropogenically introduced invasive species may be controlled locally in the manner currently attempted with meso-predators in northern Fennoscandia.
• Increasing populations of human commensal species should be counteracted, for instance by effective waste management associated with human settlements or encouragement of hunting.

Indeed, in a much warmer climate, a network of ‘Arctic parks’ which are actively managed to maintain ecosystem processes that are representative of the main geographic regions and sub-zones of the tundra biome may be the only way to conserve terrestrial Arctic biodiversity in the future. 

Needs for area- and ecosystem representative measurements

Over most of the Arctic, it will continue to be easier (and cheaper) to detect changes from space than on the ground. Thus, remote sensing and technological advances to improve it will undoubtedly be important for monitoring the terrestrial Arctic, and Arctic ecologists ought to be in the forefront of the application of such technologies. However, although we may be able to detect changes in gross ecosystem properties from space, we need to be on the ground to explain and manage those changes. Moreover, most of the biodiversity and many of the factors that drive its dynamics will remain unseen from space regardless of future improvements in remote sensing technologies.

Ground-based measurements currently have very poor geographical coverage considering the vast spatial extent of the tundra biome and the large spatial heterogeneity in its habitats and biota. This heterogeneity must be accounted for, if we are to obtain robust estimates of status and trends, for instance by means of meta-analysis (e.g. Elmendorf et al. 2012). To do this, research and monitoring efforts need to become much more area representative than is now the case. This means that many more long-term sites ought to be established, with the demand that sampling design, measurement methods and criteria for classifications are harmonized among sites.

Those processes that exceed the spatial scale of small plots or include ecosystem components dominated by microbial communities and invertebrates are currently underrepresented in terrestrial Arctic reSearch and monitoring. Both of them are, however, critically important for understanding the important biogeochemical and biophysical processes coupling the tundra ecosystem to the climate system. These problems of lack of area and ecosystem-representativeness are acute challenges that need to be addressed in the upcoming CBMP (see Box 1.4 in Meltofte et al., Chapter 1).

Needs for ecosystem-based approaches

A key message emerging from this assessment is that essential attributes of Arctic biodiversity, some of which have global repercussions, are ultimately dependent on how interactions within ecological communities and trophic webs are impacted by external drivers. This provides a compelling argument for research, monitoring and management of Arctic terrestrial biodiversity to adopt ecosystem-based approaches. At present, however, there are very few sites in the Arctic where long-term projects are explicitly ecosystem-based. This state of affairs must be improved, and CBMP ought to play a key role by helping to orchestrate an area-representative, circumpolar network of ecosystem-based monitoring sites.

The planning of a future network of ecosystem-based programs should strive to harmonize monitoring design and measurement protocols and to accommodate a common set of ‘essential biodiversity variables’ (Pereira et al. 2013). However, the fact that the ecosystems are structurally and functionally heterogeneous across sub-zones and regions of the tundra biome, as well as partly subjected to different external drivers of change, implies also a need for site-specific efforts to focus on site-specific processes and components of the ecosystem. Ecosystem-based monitoring should be guided by the best empirical knowledge and most plausible hypotheses regarding key drivers, processes and trends in the focal ecosystem (Lindenmayer & Likens 2009). In order to be relevant to stakeholders, managers and policy makers, those drivers and components of the ecosystem that actually can be amenable to actions in ecosystem-based management ought to be given particular attention in monitoring programs (Westgate et al. 2013).

The magnitude of climate warming in the Arctic during the present century may become as extreme as 10 °C. However, the projected temperatures and precipitation patterns vary so much between different models and geographic regions (Overland et al. 2011, Xu et al. 2013) that one may question the value of the many attempts now taken to derive explicit model-based predictions about how Arctic species and ecosystems will respond. Moreover, the combination of unprecedented rates of climate change, abnormal levels of other stressors, evolution of novel climates Williams et al. 2007) and ecosystem structures (Macias-Fauria et al. 2012) accentuate the possibility that present knowledge about past changes, contemporary ecosystems states and trends may have little bearing on what will become the future states of terrestrial high latitude ecosystems (Post 2013b). In such a dire situation it becomes crucial to establish flexible observation systems to enable real-time detection, documentation and understanding of cause-effect relations (Ims et al. 2013). The framework of adaptive monitoring as proposed by Lindenmayer et al. (2010) may be particularly suitable in the context of ecosystems as likely to be prone to uncertainties and surprises as those currently located in the terrestrial Arctic.

FRESHWATER ECOSYSTEMS (Chapter 13)

Lead Authors:  Frederick J. Wrona & James D. Reist 

Contributing Authors: Per-Arne Amundsen, Patricia A. Chambers, Kirsten Christoffersen, Joseph M. Culp, Peter D. di Cenzo, Laura Forsström, Johan Hammar, Jani Heino, Risto K. Heikkinen, Kimmo K. Kahilainen, Lance Lesack, Hannu Lehtonen, Jennifer Lento, Miska Luoto, Philip Marsh, David J. Marcogliese, Paul A. Moquin, Tero Mustonen, Terry D. Prowse, Michael Power, Mila Rautio, Heidi Swanson, Megan Thompson, Heikki Toivonen, Vladimir Vasiliev, Raimo Virkkala and Sergey Zavalko

SUMMARY

Photo: Patrick J. Endres

The Arctic contains an abundant and wide range of freshwater ecosystems, including lakes, ponds, rivers and streams and a complex array of wetlands and deltas. This broad range of freshwater ecosystem types contains a multitude of habitats of varying ecological complexity and supports a diversity of permanent and transitory organisms adapted to living in an often highly variable and extreme environment. Moreover, these habitats and species provide important ecological and economic services to northern peoples through the provision of subsistence foods (fish, aquatic birds and mammals), serve as seasonally important transportation corridors (e.g. ice roads), and are ecologically and culturally important habitat for resident and migratory aquatic species.

The Arctic region is currently undergoing significant and rapid environmental and socio-economic change, which in turn will have profound effects on the distribution, abundance and quality of freshwater ecosystems, their associated habitats and related biological and functional diversity. Climate change has been identified as the prominent environmental driver affecting Arctic freshwater ecosystems and their related biological and functional diversity, although other significant drivers and environmental stressors are increasing in relevance (e.g. point and non-point pollution, increased impoundment/diversion of freshwater, enhanced mining and
oil and gas activities and anthropogenic introduction of invasive species).

As a result, biodiversity within Arctic freshwater ecosystems is being rapidly altered by natural and anthropogenic drivers. Hence, a parallel understanding of functional diversity (food web structure and complexity, productivity, carbon and nutrient dynamics) is required to develop and implement appropriate conservation and management measures to ensure healthy and functioning ecosystems. Together these observations also contribute to understanding of the factors promoting services provided by freshwater ecosystems.

There have been changes to the permafrost: In the past ten years several lakes have disappeared both from the taiga and tundra area where we have our reindeer migration. Lakes have become rivers and drained out. You can see this in the tundra, but even more in forested areas. This impacts the fishing for sure. One of the lakes drained, and the fish got stuck on the bottom and died of course. Wetlands and marshes are deeper or are not so solid. Close to the rivers like Chukatsha, there are depression faults and holes in the ground. The marshlands cannot be used for reindeer travelling anymore. Dmitri Nikolayevich Begunov, a Chukchi reindeer herder from the Cherski town in Lower Kolyma in north-eastern Russia
(Mustonen 2009).

Currently, knowledge of Arctic freshwater ecosystems and related biodiversity is limited with large spatial gaps particularly in remote areas. The development of appropriate knowledge of reference states is critical to assess the variability and significance of change. Significant knowledge gaps remain in our understanding of how biodiversity contributes to, and how changes affect, freshwater ecosystem function and services. More systematic process-based studies are required to better understand the abiotic and biotic controls on ecosystem properties and to obtain a predictive understanding of how ecological communities are structured in response to changing anthropogenic and environmental drivers.

Future conservation and protection of Arctic freshwater ecosystems and their associated biodiversity requires appropriate long-term monitoring and associated process- based research across relevant spatial and temporal scales. Actions taken must be adaptive and responsive to new information in a rapidly changing Arctic.

INTRODUCTION

Freshwater ecosystems are abundant and diverse throughout the circumpolar region and include lakes, ponds, rivers, streams and a wide range of wetland complexes (Usher et al. 2005, Wrona et al. 2005, 2006a, Vincent & Laybourn-Parry 2008). The Arctic contains some of the world’s largest rivers and associated deltas (e.g. the Lena, Ob, Yenisei, Mackenzie), largest and deepest lakes (e.g. Great Bear Lake, Great Slave Lake and Lake Taymyr), numerous permanent and intermittent streams and rivers draining mountains, highlands and glaciated areas, and a myriad of smaller permanent and semi-permanent lakes, ponds and wetlands. In some regions of the Arctic, lake, pond and wetland complexes can cover > 80% of the total land area (Wrona et al. 2005, 2006a, Pienitz et al. 2008, Rautio et al. 2011).

This broad range of freshwater ecosystem types contains a multitude of habitats of varying complexity, which in turn support a diversity of permanent and transitory organisms adapted to living in an often highly variable and extreme environment (Rouse et al. 1997, Usher et al. 2005, Wrona et al. 2005, Prowse et al. 2006b, Rautio et al. 2008, Heino et al. 2009, Moss et al. 2009, Schindler & Lee 2010). In addition, high-latitude freshwater systems are of regional and global significance by serving as important tele-connections and providing feedbacks with climate and ocean systems, being critical habitat and/or refugia for unique species and communities, acting as significant sources and/or sinks of CO₂ and methane, and serving as transecosystem integrators and links of nutrient, organic matter and freshwater transport and f lux between the terrestrial and marine systems (Wrona et al. 2005, AMAP 2011b, Prowse et al. 2011c).

The Arctic region is currently in a period of major and rapid environmental and socio-economic change, which in turn will have profound effects on the distribution, abundance and quality of freshwater ecosystems and their associated habitats and biological and ecological diversity (Wrona et al. 2005, CAFF 2010, AMAP 2011b). While climate change is a key environmental driver affecting freshwater ecosystems and associated biota in the Arctic region and has received a significant amount of attention (ACIA 2005a, 2005b, IPCC 2007, Heino et al. 2009, AMAP 2011b, Rautio et al. 2011, Culp et al. 2012), a number of other significant drivers and environmental stressors are also increasing in relevance in their potential for affecting freshwater ecosystems and related biodiversity. These include, for example, point and non-point pollution (e.g. long-range aerial transport of contaminants; AMAP 2003, 2011a, Macdonald et al. 2005, Wrona et al. 2006b), altered hydrologic regimes related to increased impoundment/diversion of freshwater (Prowse et al. 2006a), water quality changes from landscape alterations (e.g. mining, oil and gas exploration) (AMAP 2008) and biological resource exploitation (e.g. subsistence and commercial fisheries). Furthermore, increased access to the north via land and sea transport including for example, the proliferation of roads in northern Canada and Russia, opens up efficient new dissemination pathways for invasive species (AMAP 2011b; see also Lassuy & Lewis, Chapter 16). Collectively, these drivers/stressors will often synergistically contribute to the alteration and/or degradation of biological diversity at the species, genetic and habitat- ecosystem levels (Pimm et al. 1995, ACIA 2005, Wrona et al. 2005, IPCC 2007, CAFF 2010).

In the following sections we summarize the current state of knowledge on the relative importance of the past, present and projected environmental and anthropogenic drivers in affecting the status, patterns and trends in ecosystem/habitat, structural and functional diversity of Arctic freshwater systems. In some circumstances it is difficult to fully adhere to the strict definition of the Arctic used in this assessment (see Section 2 in Meltofte et al., Introduction), as certain freshwater systems (notably the large rivers that discharge to the Arctic Ocean) cross several ecozones and related latitudinal and temperature gradients given the scale of their contributing drainage area. Such systems are used as key examples of how Arctic freshwater and habitat quality, quantity and related biodiversity can also be significantly affected through direct linkages to environmental and anthropogenic drivers and ecological processes that are extraneous to the Arctic per se.

Through the use of pertinent case studies and examples, we will provide an ecosystem-based, community or food web perspective on how key environmental and anthropogenic drivers in the Arctic, operating singly or in combination, affect the distribution and abundance of freshwater ecosystem types, their related habitats, and structural and functional ecological properties.

In the final section of the chapter we provide perspectives on current and proposed approaches for the conservation and protection of Arctic freshwater biodiversity, identify knowledge gaps and challenges, and forward recommendations on the future directions of monitoring and assessment of aquatic biodiversity in a rapidly changing Arctic.

CONCLUSIONS AND RECOMMENDATIONS

Arctic freshwater ecosystems are undergoing rapid eronmental change in response to the inf luence of both environmental and anthropogenic drivers. Primary drivers affecting the distribution, abundance, quality and hence diversity of freshwater lentic and lotic ecosystems and associated habitats include climate variability and change, landscape-level changes to the cryospheric components (i.e. permafrost degradation, alterations in snow and ice regimes), and changes to ultraviolet radiation (UVR). Key secondary environmental and anthropogenic drivers that are gaining circumpolar importance in affecting Arctic freshwater ecosystem quantity and quality include increasing acidification and pollution from deposition of industrial and other human activities (wastewater, release of stored contaminants, long-range transport and biomagnification of pollutants), landscape disturbance from human development (dams, diversions, mining, oil and gas activity, population increase) and exploitation of freshwater systems (fisheries, water withdrawals).

Changes in the magnitudes, duration and interactions among environmental and anthropogenic drivers will have profound effects on the distribution and abundance of Arctic freshwater ecosystem types, the quantity and quality of their habitats, and associated structural and functional biodiversity. In response to the observed and projected types and magnitudes of changes in environmental and anthropogenic drivers affecting the Arctic ecozone, freshwater ecosystem diversity (i.e. the range and types of freshwater systems), related changes to associated freshwater habitats, and corresponding faunal biodiversity will be affected at local, regional and circumpolar scales. Given the levels of ecological complexity and associated uncertainty with linking changes in physico-chemical factors to biological interactions, quantifying and monitoring changes in beta and gamma diversity in relation to changes in key drivers will be fundamental to the conservation and management of Arctic freshwater ecosystems and their biota.

Similarly, the biodiversity within freshwater ecosystems is being rapidly altered by natural and anthropogenic drivers, thus a parallel understanding of functional diversity (food web structure and complexity, productivity, carbon and nutrient dynamics) is required to develop and implement appropriate conservation and management measures to ensure continued ecosystem services. Together these observations also contribute understanding of factors promoting services provided by freshwater ecosystems.

Currently, knowledge of Arctic freshwater ecosystems and related biodiversity and stability is very limited due to a paucity of long-term monitoring sites resulting in large spatial and temporal time-series gaps particularly in remote areas. In the face of a rapidly changing Arctic, developing appropriate knowledge of reference states will be critical to assessing the variability and significance of change.

Significant gaps also remain in our understanding of how biodiversity contributes to, and how changes affect, freshwater ecosystem functions. The future conservation and protection of Arctic freshwater ecosystems and their associated biodiversity requires appropriate long-term monitoring across relevant spatial and temporal scales.  An important step to improving efforts in this area has been the approval for implementation of the circumpolar freshwater biodiversity monitoring plan developed by the Arctic Council Conservation of Flora and Fauna (CAFF) working group and its Circumpolar Biodiversity Monitoring Program (CBMP). The Arctic Freshwater Biodiversity Monitoring Plan (Culp et al. 2012) details the rationale and framework for improvements related to the monitoring of freshwaters of the circumpolar Arctic, including ponds, lakes, their tributaries and associated wetlands, as well as rivers, their tributaries and associated wetlands. The plan also provides Arctic countries with a structure and a set of guidelines for initiating and developing monitoring activities that employ common approaches and indicators.

Process-based studies are required to better understand the abiotic and biotic controls on ecosystem properties and to obtain a predictive understanding of how ecological communities are structured in response to changing anthropogenic and environmental drivers. Given the complex interactions between the abiotic and biotic drivers affecting rapid change in the Arctic, trans-disciplinary approaches will be instrumental in identifying and understanding key processes (Hodkinson et al. 1999).

Most analyses of status and trends of biodiversity and its change have been linked to the monitoring and assessment of species richness. Standard species-based approaches may misrepresent true structural and functional diversity and thus ecosystem stability and resilience in the face of change. Future assessments of biodiversity and its changes must also include consideration of ecosystem and functional attributes using both empirical and experimental approaches. There is also an identified need to develop integrated biological/hydro-ecological models (in particular regarding changes in cryospheric components) to predict freshwater biodiversity responses to a changing climate (Hodkinson et al. 1999, Prowse & Brown 2010b, 2010c, AMAP 2011b).

• The establishment of a long-term, circumpolar network of integrated freshwater research observatories and monitoring sites is required to achieve the above goals. The focus should be inclusive of biodiversity in ecosystems, biota and key physical and chemical drivers, as well as anthropogenic inf luences, across appropriate spatial scales.

Rapid Arctic change is outpacing present capacity for Arctic freshwater conservation and management. More over, spatial displacement of key habitats, rapid shifts in the nature of processes and colonization by southern biota all indicate that static approaches are insufficient to understand and manage these complex systems. Given the large spatial scale of potential changes in Arctic freshwater ecosystems (e.g. losses, shifts amongst types, productivity changes), systematic wide scale observations are required.

• Accordingly, management actions for conservation and protection of Arctic freshwater ecosystems must be adaptive in nature and the development of novel approaches is required.

Development of appropriate wide-scale and focal-point approaches to monitoring is required. These could include, for example, genomics-based diversity assessment, space-based remote sensing, networks of automated sensors systems operating at varying spatial and temporal scales, and inter-disciplinary transfer of key approaches. In addition, community-based monitoring can be an effective method to provide continuous data from remote inhabited areas. Such work could range from simple observation and documentation to the collection of samples including tissue samples taken from harvested species by subsistence hunters and fishers.

Freshwater ecosystems serve as trans-ecosystem integrators (e.g. linking terrestrial, freshwater and oceanic environments) of multiple environmental and anthropogenic drivers and stressors. In particular lakes act as sentinels and integrators of biological, geochemical and ecological events occurring in catchments and in lacustrine environments (Schlinder 2009). Ecological transtion zones within and between ecosystems concentrate key processes, drivers and diversity, thus are focal areas of rapid ecosystem change and thus represent ‘hot spots’ ideal for early warning.

• Consideration should be made of using basin or ‘catchment-based’ integrative approaches (e.g. Schinder 2009, Schindler & Lee 2010) for the development of appropriate monitoring and research programs that could link individual, population, community and ecosystem responses to changes in environmental and anthropogenic drivers. In addition, such an integrated approach will allow for the assessment of the current state of ecosystem health and cumulative impacts associated with biodiversity change.

There is a growing recognition and concern regarding the lack of understanding of the potential loss or gain of species and the consequent implications for associated ecosystem function (e.g. Hooper et al. 2005, Vaughn 2010). Given the functional importance of biota living in aquatic environments and the difficulties associated with cataloging their diversity and distribution, innovative approaches and studies must be taken along a range of spatial, temporal and organizational (e.g. system-based and species-based) scales to better understand the connections (e.g. the necessity of obtaining an improved mechanistic understanding of the individual effects and interactions among environmental stressors/drivers on all trophic levels and related ecosystem structure and function; see Bordersen et al. 2011). In addition, in a rapidly changing Arctic, there is a need to be aware of and to develop ways to detect and understand possible ecological ‘surprises’, which are unexpected findings or outcomes that are well outside what is expected to happen or not happen (Lindenmayer et al. 2010).

• Research involving a range of comparative short- and long-term field-based empirical studies, field experiments (including experimental manipulations) and laboratory experiments should be conducted to investigate and better understand the linkages and effects of biodiversity on ecosystem function and, consequently, on the ecological goods and services that Arctic freshwater ecosystems provide.

MARINE ECOSYSTEMS (Chapter 14)

Lead Author:  Christine Michel 

Contributing Authors: Bodil Bluhm, Violet Ford, Vincent Gallucci, Anthony J. Gaston, Francisco J. L. Gordillo, Rolf Gradinger, Russ Hopcroft, Nina Jensen, Kaisu Mustonen, Tero Mustonen, Andrea Niemi, Torkel G. Nielsen and Hein Rune Skjoldal

SUMMARY

Harbour seal Photo: Stefan Schejok, Shutterstock.com

Arctic marine ecosystems host a vast array of over 2,000 species of algae, tens of thousands of microbes and over 5,000 animal species, including unique apex species such as the polar bear Ursus maritimus and narwhal Monodon monoceros, commercially valuable fish species, large populations of migratory birds and marine mammals, and some of the largest colonies of seabirds on the planet. Current estimates also suggest that many species are yet to be discovered.

The marine Arctic is characterized by a wide range of and large variability in environmental conditions. The Arctic Ocean has the most extensive shelves of all oceans, covering about 50% of its total area. It comprises diverse ecosystems such as unique millennia-old ice shelves, multi-year sea ice, cold seeps and hot vents, and their associated communities.

The Arctic is undergoing major and rapid environmental changes including accelerated warming, decrease in sea ice cover, increase in river runoff and precipitation, and permafrost and glacier melt. These changes together with new opportunities for economic development create multiple stressors and pressures on Arctic marine ecosystems.

All Eskimos (Siberian Yupik) emphasize their connection with the sea – boys have dreams of becoming hunters. The sea gives birth to our whole life … Tatyana Achirgina in Novikova (2008).

Throughout the Arctic, ecosystem changes are already being observed. Changes in the distribution and abundance of key species, range extensions and cascading effects on species interactions are taking place, influencing Arctic marine food web architecture. Unique habitats such as ice shelves and multi-year ice are rapidly shrinking.

With continued warming and sea ice decline, measures should be put in place to monitor areas of particular biological significance and uniqueness in support of preservation and protection measures. Moreover, the complexity and regional character of Arctic ecosystem responses to environmental changes calls for the establishment of long-term marine ecosystem observatories across the Arctic, in support of sustainable management and conservation actions.

INTRODUCTION

Arctic marine ecosystems are important constituents of global biodiversity. Arctic marine ecosystems are habitats to a vast array of over 5,000 animal species and over 2,000 species of algae and tens of thousands of microbes (see Josefson & Mokievsky, Chapter 8, Daniëls et al., Chapter 9 and Lovejoy, Chapter 11). The marine Arctic also provides habitat for large populations of marine mammals and birds (see Reid et al., Chapter 3 and Ganter & Gaston, Chapter 4), some of which form colonies that are among the largest seabird colonies on the planet. The unique characteristics of Arctic marine ecosystems also contribute directly to global diversity. For example, Arctic sea ice ecosystems support biodiversity at various scales ranging from unique microbial communities to apex predator species such as the polar bear Ursus maritimus and walrus Odobaenus rosmarus whose ecology is closely associated with the sea ice environment.

Indirectly, the Arctic Ocean plays a key role in shaping the global biodiversity of marine and terrestrial ecosystems as it plays an essential role in the Earth climate system. The Arctic Ocean also influences marine ecosystems of the Atlantic Ocean directly, as waters and sea ice exiting the Arctic Ocean affect the physical, chemical and biological characteristics of the North Atlantic. Conversely, the Arctic Ocean receives waters from the Pacific and Atlantic Oceans, and therefore Arctic marine ecosystems are influenced by global changes that influence biodiversity in these oceans.

The Arctic is subject to rapid environmental changes. The current increase in global temperature is most rapid in the Arctic, with a predicted summer temperature increase of up to 5 °C over this century (IPCC 2007), and surface water temperature anomalies as high as 5 °C recorded in 2007 (Steele et al. 2008). Arctic sea ice, a key defining characteristic of the Arctic Ocean, is declining faster than forecasted by model simulations (in Meltofte et al., Chapter 1), with the potential for a summer ice-free Arctic within the next few decades (Stroeve et al. 2007, Wang & Overland 2009). The effects of these and other environmental changes (e.g. changes in freshwater input, shoreline erosion) on Arctic marine ecosystems are already documented (e.g. Wassmann et al. 2010, Weslawski et al. 2011). These changes, together with increased economic interest and development in the Arctic, put pressure on the biodiversity of Arctic marine ecosystems and on the species that inhabit them.

CONCLUSIONS AND RECOMMENDATIONS

Vulnerabilities, adaptation and looking forward

As primary production fuels marine food webs through its transfer to pelagic and benthic organisms, regional increases in primary production may be expected to augment the production of fish and shellfish species, some of which have commercial value. Recent increases in primary production associated with changes in sea ice cover on two geographically opposed shelves, the Beaufort and Laptev shelves, have been linked to observed/ modeled increases in the sedimentation of organic material (Lalande et al. 2009, Lavoie et al. 2009). In addition, studies from Arctic areas (Svalbard) suggest that benthic biota respond to fluctuations in regional climate patterns (Beuchel et al. 2006). Enhanced environmental forcing leading to warmer winters with less sea ice, earlier onset of melting and increased precipitation in Kongsfjorden during the decade 1993-2004 (Svendsen et al. 2002) may have benefited the brown algae Desmarestia sp. due to the increased availability of light and nutrients (Beuchel & Gulliksen 2008). These results point to changes in marine ecosystem architecture and biodiversity on Arctic shelves, where sea ice cover is in a state of transition.

At the same time, recent studies indicate that the increased freshwater content in the Arctic Ocean, through the effect of stratification on plankton community structure (Li et al. 2009), decreases the efficiency of transfer of organic material in Arctic marine food webs (Kirchman et al. 2009, Cai et al. 2010). Therefore, an increase in overall production in the Arctic Ocean may not necessarily lead to more abundant harvestable species, as the composition of communities largely determines the fate of material in marine systems. Recent modelling also highlights the regional character of ecosystem responses to climatic forcing (Slagstad et al. 2011).

The response of Arctic marine ecosystems to on-going changes depends on complex interactions between community structure, trophic interactions, species-specific adaptation and fitness in regard to environmental conditions, superimposed upon anthropogenic stressors that often have a strong local influence. The cumulative effects of the thinning of the ice pack, its enhanced export in relation to atmospheric circulation patterns, and warmer ocean temperatures may continue to alter Arctic sea ice and associated ecosystems dramatically. How these and other emergent environmental and anthropogenic forcings will affect ecosystem biodiversity in the marine Arctic, and in downstream marine systems, is unknown.

Patterns of changing diversity will likely depend on regional characteristics and habitat types, but also on the connectivity of ocean areas with boreal/southern regions. In areas connected to boreal waters, increases in advection can result in the transport of more sub-Arctic species northward. In regions isolated from advection of boreal waters, such as the Canadian Arctic Archipelago, changes in biodiversity may be slower and mainly influenced by local changes. Trans-Arctic migrations from the Pacific to the Atlantic Ocean are likely to occur increasingly, as Arctic sea ice continues to melt and could cause restructuring of marine food webs. The presence of the Pacific diatom Neodenticula seminae in the North Atlantic Ocean in the late 1990s after > 800,000 years of absence, was attributed to increased transport of Pacific waters through the Canadian Archipelago (Reid et al. 2007). Such trans-Arctic expansions are likely to continue, reflecting the influence of the Arctic on global marine biodiversity.

Some unique habitats, species and elements of Arctic marine ecosystems are particularly vulnerable to ongoing changes. The unique habitats associated with Arctic ice shelves that have evolved over thousands of years are eroding and may be irrevocably lost in the current and predicted future climate. Multi-year ice and its associated habitats are at risk of vanishing, with major but largely unknown direct and indirect effects on Arctic marine ecosystem architecture. Ice-associated biodiversity is at risk, with species such as the polar bear exemplifying climate-related impacts on Arctic marine biodiversity.

As changes are occurring in the Arctic, marine species and Arctic residents need to adapt. Hence, much local human transport that hitherto has taken place over ice may now use ships and boats for most of the year, and hunting techniques developed for hunting on ice may be replaced by open water hunting methods. Traditional ways may have to evolve, as expressed by this Inuit hunter:

A buddy of mine is into making little sleds out of aluminum, which you can use as a little kayak or boat. If you’re out on the ice and you have to cross an open lead you can use that. It’s one of the things that can help. I’m going to get one of those. It’s combined as a little sleigh and, if you have to, you can use it as a boat. That’s one way I can adapt.

Species with more plasticity are likely to better adapt to a variable and changing environment than species with narrow tolerances and strict physiology or life history. For example, copepods and krill in the Barents Sea MIZ show marked trophic plasticity, shifting from herbivory during the bloom to omnivory when fresh material is less abundant. Predator fishes such as Atlantic cod also show high feeding plasticity, shifting their prey from fishes to zooplankton in response to changes in abundance. Such flexibility in feeding strategies may provide an advantage in highly variable environments such as the MIZ (Tamelander et al. 2008). Phenotypic plasticity is also expected to dominated responses of marine mammals to climate change in the short term (Gilg et al. 2012). Accordingly, biodiversity can offer functional redundancy and increase the resilience of marine systems to multiple stressors. However, this resilience ultimately depends on the response of each species to individual and combined stressors and the resulting trophic interactions.

Since the Arctic is at the northern limit of distribution of many species, northward range extensions due to a warming climate are likely to shift the balance of species as the sub-Arctic biome takes over the present Arctic and true Arctic species are pushed northwards or go extinct. Such changes, as examplified by shifts in top predator species in Hudson Bay (i.e. killer whales versus polar bears, see Section 14.5.4), will affect ecosystem functioning and transfer pathways. In addition, extensive alterations in the physical and biogeochemical structure of Arctic marine ecosystems are currently taking place, with unknown consequences for these ecosystems and the species that inhabit them. We cannot predict the tradeoffs between the potential loss of unique ecosystems such as ice shelves and the introduction of new species via northwards range extensions and modifications in habitats.

Knowledge gaps and challenges

One of the greatest impediments to understanding the ongoing changes in the biodiversity of Arctic marine ecosystems is the fragmented nature of much of the existing knowledge and the lack of consistent and regular long-term monitoring programs in most Arctic marine regions, including unique or vulnerable ecosystems. A commitment to long-term studies is essential in this regard, and the establishment of the Arctic Marine Biodiversity Monitoring Plan supported by CAFF (Gill et al. 2011) is an important step towards this goal.

The effects of disturbances and stressors on Arctic marine biodiversity are not well understood. The lack of baseline information in many areas, the wide range of ecosystems and the impact of cumulative effects make it difficult to predict the direction of changes. The multiple stressors currently affecting Arctic marine ecosystems operate simultaneously at various temporal and spatial scales, emphasizing the need for local and concerted biodiversity assessment and monitoring. There is also a need to develop indicators that properly reflect the unique characteristics of Arctic marine ecosystems. For example, habitat fragmentation, used as a global biodiversity indicator, could be characterized in the marine Arctic using a variety or combination of indicators including sea ice extent and water mass distribution indices. These physical/chemical indicators could then serve as structuring elements upon which to monitor associated ecosystem biodiversity trends. Shifts in ecosystem structure, species interactions and trophic pathways need to be understood in the context of shortand long-term trends, in order to develop management strategies to maintain the diversity and sustainability of Arctic marine ecosystems. To this effect, it is essential to include biological elements in monitoring programs for the marine Arctic.

To gain new knowledge and make sensible projections about climate impacts on carbon dynamics and sequestering in Arctic marine ecosystems, key organisms from the base of marine food webs need to be considered, parameterized and included in research and modeling efforts We also need to better understand the ecophysiology of key species to be able to better parameterize bulk processes and rates.

We still have a limited inventory and understanding of the current status of Arctic marine diversity, and particularly so for the small microbial communities and benthic invertebrates. There is still much to learn about the biodiversity of extreme habitats and organisms in the Arctic. For example, there is recent evidence of the widespread occurrence of cold seeps in the marine Arctic, but the organisms inhabiting these unique habitats are poorly described. Similarly, unique habitats associated with sea ice and ice shelves are poorly understood and their biodiversity is largely unknown. This special biodiversity in the Arctic presents opportunities for advancements in biotechnology, medical research and even the search for life on other planets. Deep basins of the Arctic Ocean, which were largely inaccessible, are becoming ice-free in summer, bringing new opportunities for research and exploration. As one of the last frontiers on Earth, the marine Arctic still holds many discoveries with respect to the biodiversity of its ecosystems and the species that inhabit them

Key points and recommended actions

The marine Arctic spans a wide range of environmental conditions including extremes in temperature, salinity, light conditions and the presence (or absence) of sea ice, leading to diverse Arctic marine ecosystems. These ecosystems are experiencing rapid changes in their chemical, physical and biological characteristics together with unprecedented socio-economic pressures. Changes in the distribution and abundance of key species and cascading effects on species interactions and the structure and functionality of marine food webs are already observed.

Range extensions are taking place throughout the Arctic, with a northward expansion of sub-Arctic species and a narrowing of Arctic habitats that have existed over millions of years such as multi-year ice and ice shelves. Under current climate scenarios, the loss of these unique ecosystems could be irreversible.

Arctic marine ecosystems are influenced by large-scale processes and their connectivity to the Pacific and Atlantic Oceans. However, the strong regionality in physicochemical conditions and in observed trends and their drivers precludes generalization of ecosystem responses to current and predicted environmental changes.

• With continued warming and sea ice decline, measures should be put in place to monitor areas of particular biological significance and uniqueness in support of preservation and protection measures. One such area is N Greenland and the northeastern Canadian Archipelago, predicted to be the last refuge where multiyear ice and its associated species will persist.
• Establishing a network of long-term biological observatories of marine ecosystems across the Arctic is highly recommended. It is essential that biological communities and ecosystem processes are characterized in conjunction with physico-chemical observations as part of monitoring activities in the Arctic.
• Pan-Arctic coordination of research and monitoring activities, using standardized methods in Arctic oceanography and taking advantage of new technologies, is encouraged in order to document and forecast trends in Arctic marine ecosystem biodiversity.
• Key species at all trophic levels and ecological processes that best allow characterization of marine food webs should be identified and included in future monitoring programs across the Arctic.
• Concerted international efforts and associated national funding programs should be dedicated to better understanding changes in the functioning of Arctic marine ecosystems, including process studies to relate

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

Lung nematode. Photo: Eric Hoberg

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.