(Advances in Parasitology 79) D. Rollinson and S.I. Hay (Eds.) - Advances in Parasitology-Academic Press (2012) PDF

SERIES EDITORS
D. ROLLINSON S.I. HAY

Department of Zoology, Spatial Epidemiology and Ecology Group,
The Natural History Museum, Tinbergen Building, Department of Zoology,
London, UK University of Oxford, South Parks Road,
d.rollinson@nhm.ac.uk Oxford, UK
simon.hay@zoo.ox.ac.uk
EDITORIAL BOARD
M. G. BASÁÑEZ R. E. SINDEN
Reader in Parasite Epidemiology, Immunology and Infection Section,
Department of Infectious Disease Department of Biological Sciences,
Epidemiology, Faculty of Medicine Sir Alexander Fleming Building, Imperial
(St Mary’s campus), Imperial College, College of Science, Technology and
London, UK Medicine, London, UK
S. BROOKER D. L. SMITH
Wellcome Trust Research Fellow and Johns Hopkins Malaria Research Institute
Reader, London School of Hygiene and & Department of Epidemiology, Johns
Tropical Medicine, Faculty of Infectious Hopkins Bloomberg School of Public
and Tropical Diseases, London, UK Health, Baltimore, MD, USA
R. B. GASSER R. C. A. THOMPSON
Department of Veterinary Science, The Head, WHO Collaborating Centre for
University of Melbourne, Parkville, the Molecular Epidemiology of Parasitic
Victoria, Australia Infections, Principal Investigator, Envi
ronmental Biotechnology CRC (EBCRC),
N. HALL School of Veterinary and Biomedical
School of Biological Sciences, Bio Sciences, Murdoch University, Murdoch,
sciences Building, University of Liver WA, Australia
pool, Liverpool, UK
X. N. ZHOU
R. C. OLIVEIRA Professor, Director, National Institute
Centro de Pesquisas Rene Rachou/ of Parasitic Diseases, Chinese Center
CPqRR - A FIOCRUZ em Minas Gerais, for Disease Control and Prevention,
Rene Rachou Research Center/CPqRR - Shanghai, People’s Republic of China
The Oswaldo Cruz Foundation in the
State of Minas Gerais-Brazil, Brazil
Advances in
PARASITOLOGY
VOLUME
79
Edited by
D. ROLLINSON
Department of Zoology,
The Natural History Museum,
Cromwell Road,
London, UK
S. I. HAY
Spatial Epidemiology and Ecology Group,
Tinbergen Building, Department of Zoology,
University of Oxford, South Parks Road,
Oxford, UK
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CONTRIBUTORS
Kimberlee B. Beckmen
Alaska Department of Fish and Game, Division of Wildlife Conservation,
Fairbanks, AK, United States
Doug D. Colwell
Agriculture and Agri-food Canada, Lethbridge, Alberta, Canada
Joseph A. Cook
Museum of Southwestern Biology and Department of Biology, University
of New Mexico, Albuquerque, NM, USA
Bart Currie
Menzies School of Health Research, Casuarina, NT, Australia
Julie Ducrocq
Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta,
Canada
Brett T. Elkin
Environment and Natural Resources, Government of Northwest
Territories, Yellowknife, Northwest Territories, Canada
Katja Fischer
Queensland Institute of Medical Research, Herston, Queensland, Australia
Kurt E. Galbreath
Department of Biology, Northern Michigan University, Marquette, MI, USA
Stephen E. Greiman
Department of Biology, University of North Dakota, Grand Forks, ND, USA
Ken Hashimoto
Chagas Disease Control Projects, Japan International Cooperation Agency,
Central America
Bryanne M. Hoar
Canada
ix
x Contributors
Eric P. Hoberg
US National Parasite Collection, Animal Parasitic Diseases Laboratory,
Agricultural Research Service, USDA, Beltsville, MD, USA
Deborah Holt
Menzies School of Health Research, Casuarina, NT, Australia
David Kemp
Queensland Institute of Medical Research, Herston, Queensland, Australia
Susan J. Kutz
Canada
Ian Maudlin
Division of Pathway Medicine and Centre for Infectious Diseases, School
of Biomedical Sciences, College of Medicine and Veterinary Medicine, The
University of Edinburgh, Edinburgh, UK
Lydden Polley
Western College of Veterinary Medicine, University of Saskatchewan,
Saskatoon, Saskatchewan, Canada
Vasyl V. Tkach
Jefferson A. Vaughan
Guilherme G. Verocai
Canada
Susan C. Welburn
Division of Pathway Medicine and Centre for Infectious Diseases, School
of Biomedical Sciences, College of Medicine and Veterinary Medicine, The
University of Edinburgh, Edinburgh, UK
Kota Yoshioka
Chagas Disease Control Project, Japan International Cooperation Agency,
Managua, Nicaragua
CHAPTER 1
Northern Host–Parasite
Assemblages: History
and Biogeography on the
Borderlands of Episodic Climate
and Environmental Transition
Eric P. Hoberg*, Kurt E. Galbreath†, Joseph A. Cook‡,
Susan J. Kutz§, and Lydden Polley¶
Contents 1.1. Introduction 3

1.2. Northern Systems and Parasites – Setting the Stage 7
1.2.1. Developing knowledge of parasite diversity
in the North 9
1.2.2. Towards an integrated picture of parasite diversity 10
1.3. An Historical (Physical–Biological) Setting for the Arctic 12
1.3.1. Exploring the Beringian connection 15
1.4. Faunal Structure – Evidence for Northern Connections 17
1.4.1. Faunas associated with terrestrial Carnivora 17
1.4.2. Faunas associated with Lagomorpha 34
1.4.3. Faunas associated with Rodentia 39
1.4.4. Faunas associated with Artiodactyla 48
1.4.5. Human interfaces and occupation of the North 56
* US National Parasite Collection, Animal Parasitic Diseases Laboratory, Agricultural Research Service,
USDA, Beltsville, MD, USA,
† Department of Biology, Northern Michigan University, Marquette, MI, USA,
‡ Museum of Southwestern Biology and Department of Biology, University of New Mexico,
Albuquerque, NM, USA,

§ Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada,
¶ Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan,
Canada
Advances in Parasitology, Volume 79 © 2012 Elsevier Ltd.

ISSN 0091-679X, http://dx.doi.org/10.1016/B978-0-12-398457-9.00001-9 All rights reserved.
1
2 Eric P. Hoberg et al.
1.5. Biodiversity – History in a Complex Northern Fauna 60

1.5.1. General biogeographic patterns 63
1.5.2. Mechanisms of faunal expansion in space and time 66
1.5.3. An integrated model for diversification –
contributions from the North 69
1.5.4. Mosaic faunas – consequences of episodic
geographic expansion 70
1.5.5. Stories that parasites reveal 74
1.6. Tools for Biodiversity Discovery 76
1.7. Problems and Challenges to Be Resolved 79
Acknowledgements 81
References 81
Abstract Diversity among assemblages of mammalian hosts and parasites in

northern terrestrial ecosystems was structured by a deep history of
biotic and abiotic change that overlies a complex geographic arena.
Since the Pliocene, Holarctic ecosystems assembled in response to
shifting climates (glacial and interglacial stages). Cycles of episodic
dispersal/isolation and diversification defined northern diversity
on landscape to regional scales. Episodes of geographic expansion
and colonisation linked Eurasia and North America across Beringia
and drove macroevolutionary structure of host and parasite asso-
ciations. Asynchronous dispersal from centres of origin in Eurasia
into the Nearctic resulted in gradients in parasite diversity in the
carnivoran, lagomorph, rodent and artiodactyl assemblages we re-
viewed. Recurrent faunal interchange and isolation in conjunction
with episodes of host colonisation have produced a mosaic struc-
ture for parasite faunas and considerable cryptic diversity among
nematodes and cestodes. Mechanisms of invasion and geographic
colonisation leading to the establishment of complex faunal as-
semblages are equivalent in evolutionary and ecological time, as
demonstrated by various explorations of diversity in these high-
latitude systems. Our ability to determine historical responses
to episodic shifts in global climate may provide a framework for
predicting the cascading effects of contemporary environmental
change.
Geography to a large extent determines climate and, in combination

with climate, provides the matrix within which ecosystems exist,
function and evolve.
David M. Hopkins, in Paleoecology of Beringia (1982).
The distributions of species that currently occur in the Arctic rep-
resent a snapshot of a dynamic and ongoing process driven by
historical climate changes….
Terry V. Callaghan et al. (2004c).
Northern Host–Parasite Assemblages 3
There are still some areas in the Arctic, especially in North America,
where it is possible to define natural parasite-host relationships, or
at least to gain an understanding of such relationships before the
arrival of Europeans.
Robert L. Rausch (1974).
1.1. INTRODUCTION
The Earth’s northern circumpolar regions present landscapes of outstand-

ing beauty, incomparable fauna and flora and small, widely dispersed
human settlements. These are integrated biological systems, where peo-
ples of great resilience remain culturally close to the land and dependant
on an array of natural resources, while living with the extremes of short
summers and long cold winters (Rausch, 1951; Anisimov et al., 2007). The
North encompasses those regions extending from the borders of the Sub-
arctic (above 50°N) to beyond the Arctic Circle (north of 66°33′N) (Fig. 1.1).
The latter marks the approximate limit for the current northern treeline
and the circumpolar zone characterised seasonally by periods of constant
polar night or midnight sun. Treeless tundra habitats dominate the Arctic
where the average temperatures for the warmest month do not exceed
10°C; mean annual temperatures for the western subregions of the Arctic
range from −20 to +12°C with minimal precipitation varying from 5 to
150mm (Callaghan et al., 2004e). The Arctic transitions into more south-
erly Subarctic environments dominated primarily by taiga forests and a
more complex mosaic of habitats defined by latitude and altitude.
Northern ecosystems were formed by complex abiotic and biotic
mechanisms in a crucible driven by episodic climatological processes
and environmental perturbation extending across the late Pliocene and
Quaternary during the past 3–5 million years (Myr) (e.g. Hopkins et al.,
1982; Andersen and Borns, 1994 Dynesius and Jansson, 2000; Jansson and
Dynesius, 2002; Callaghan et al., 2004a,c; Hewitt, 2004a,b). Contemporary
patterns of faunal complexity reflect extinction events largely coincidental
with the thermal maximum that signalled the termination of continental
glaciation only 10 thousand years ago (Ka) (e.g. Barnosky et al., 2004).
Consequently, northern biotas are typically characterised as relatively sim-
ple, low-diversity assemblages with short trophic linkages, few pathogens
and limited resilience or capacity for adaptation to environmental change
(e.g. Callaghan et al., 2004a) (Table 1.1). A gradient of declining diversity
with increasing latitude (from taiga forests to polar deserts) is also accom-
panied by a shift or increase in dominance for some species, which may
be manifested seasonally or annually (e.g. Callaghan et al., 2004b). High-
latitude biotas are now at their minimal extent relative to patterns of diver-
sity and geographic distribution that characterised faunas during the mid
to late Pleistocene (e.g. Guthrie, 1984; Callaghan et al., 2004a).
FIGURE 1.1 Boundaries and definitions for the Arctic and Subarctic regions according to
the Programme for the Conservation of Arctic Flora and Fauna (CAFF), shown in polar
projection. Boundaries can be defined by the isotherms, habitat, latitude or geopolitical
zones. Source map was developed by cartographer Philippe Rekacewicz (UNEP/GRID-
Arendal) and is made available by CAFF at http://maps.grida.no/go.graphic/definitions
_of_the_arctic. (For color version of this figure, the reader is referred to the web version
of this book.)
At high latitudes, vulnerable systems of low diversity continue to

undergo significant and in some instances accelerating change due
largely to human activity, both local and distant. These perturbations
have the potential for broader impacts at a global scale (Callaghan
et al., 2004a,d; Anisimov et al., 2007; Lawler et al., 2009; Post et al.,
2009). Increasingly, substantial discussion has focused on the status and
future of northern ecosystems, but these assessments have been limited
TABLE 1.1 Defining characteristics for northern systems with respect to physical
and biological attributes (Irvine et al., 2000; Callaghan et al., 2004c,2004e; Hoberg
et al., 2008b)
Arctic Subarctic
Latitude > 66° 33′N > 50° N

Temperaturea < 10°C (mean summer) May exceed + 30°C
(maximum summer)
average low near −40°C
Small variation in extremes Great variation in
extremes
Precipitation Primarily snow (< 25cm) Snow and rain
(+ 40–45 cm)
Vegetation Shrub-tundra, tundra, polar Taiga, steppe, tundra
desert
Latitudinal treeline, microhabi- Mosaics based on altitude
tat mosaics and latitude
Permafrost Present Present or absent
Diversity 75 species terrestrial mammals ± 250 species terrestrial
mammals
Vulnerability Habitat loss through climate Habitat perturbation
change through climate change
Responses (1) Populations at environmental extremes of distribution
in the Arctic (latitude, or altitude, mosaics within land-
scapes) respond to amelioration of physical conditions
such as limitations imposed by temperature through the
potential to expand based on both functional and numeri-
cal mechanisms?
(2) Populations at environmentally benign boundaries in the
Subarctic or with more southern distributions tend to be
constrained by competition with more responsive species,
and amelioration may drive shifts in distribution, devel-
opment of new ecotones, new patterns of sympatry and
displacement?
a Temperatures represent baselines from decades around 1980–1999.
to free-living organisms. Parasitism, pathogens and diseases have not

yet been an integral component of this discourse (Kutz et al., 2009a).
Parasites represent in excess of 40–50% of the organisms on Earth and
complex assemblages of macroparasites (helminths and arthropods) and
microparasites (viruses, bacteria and protozoans) shape ecosystems, food
webs, host demographics and behaviour (e.g. Marcogliese, 2005; Hudson
et al., 2006; Dobson et al., 2008). In some ecosystems, the biomass for
macroparasites exceeds that for apex predators such as birds and fishes,
suggesting a substantial role for otherwise obscure organisms at local to
regional scales (Kuris et al., 2008). Parasites can cause disease and mortal-
ity may influence the dynamics of wildlife populations and, in the worst-
case scenarios, contribute to extinction events.
Parasites are ubiquitous and diverse members of all biological commu-
nities including those at high latitudes. All animals in circumpolar regions
are susceptible to infection by characteristic assemblages of macroparasites
and microparasites. Parasites can have subtle to severe effects on individual
hosts or broader impacts on host populations that may cascade through
ecosystems. Parasitic diseases have dual significance: (1) influencing sus-
tainability for species and populations of diverse invertebrates, fishes, birds
and mammals and (2) secondarily affecting food security, quality and avail-
ability for people. Additionally, as zoonoses, some parasites can infect and
cause disease in people and are a primary issue for food safety and human
health (e.g. Kutz et al., 2009b; Jenkins et al., 2011). Sustainability, security
and safety of ‘country foods’ are of concern at northern latitudes where
people maintain a strong reliance on wildlife species. The potential signifi-
cance of zoonoses is magnified in the North by the intimate linkage between
wildlife and people. Subsistence food chains depend on the harvesting of
free-ranging mammals, birds and fish for food, fibre and other animal prod-
ucts. Understanding the role and influence of parasites in northern systems
emerges from explorations of history, biogeography and the intricate eco-
logical linkages among fishes, birds, mammals, domesticated species and
people in the context of broader global connections (e.g. Hoberg, 2010).
Despite the extreme environmental conditions in the North, the triad of
host, parasite and environment remains the key determinant of the profile
of parasitic infections and disease in people and animals. Parasites circulate
through pathways that link the host and environmental setting. Some para-
sites 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
and humidity, and are then acquired through ingestion of water or forage.
In contrast, indirect transmission is related to trophic connections between
predators (definitive) and prey (intermediate hosts where the parasite
develops) or may involve vectors, usually biting flies or other arthropods,
that disseminate the parasite between hosts. In the Arctic, the ambient envi-
ronmental setting (temperature, humidity, seasonality, geography, external
stressors), and life history traits and ecology of hosts (migration, hiberna-
tion, food habits, foraging behaviour, age and immunological status, etc.)
dramatically influence the survival, development, abundance and distribu-
tion of parasites and related disease in space and time (e.g. Kutz et al., 2004,
2005; Hoberg et al., 2008a,b; Kutz et al., 2009b; Laaksonen et al., 2010).
1.2. NORTHERN SYSTEMS AND PARASITES – SETTING

THE STAGE
Parasites are important components of terrestrial, aquatic and marine

systems in the Arctic but seldom are included in general assessments of
biodiversity at high latitudes (Hoberg, 1996; Hoberg and Adams, 2000;
Hoberg et al., 2003; Kutz et al., 2009a). Climate change and associated eco-
logical perturbations are modifying the structure of terrestrial, aquatic and
marine systems across high latitudes of the north (e.g. ACIA, 2004; Rausch
et al., 2007; Hoberg et al., 2008a; Kutz et al., 2009b). Patterns of distribu-
tion, timing of migrations and seasonally defined windows that determine
the life histories for a diverse assemblage of vertebrates, invertebrates and
their parasites are under dynamic change (Callaghan et al., 2004d; Lawler
et al., 2009). As we recognise and predict direct and indirect impacts to
terrestrial, aquatic and marine systems (e.g. Lawler et al., 2009; Post et al.,
2009), parasites and associated diseases should also be considered in the
‘equations’ for environmental change. Acclerating environmental pertur-
bation in northern ecosystems (particularly patterns of temperature and
humidity acting on habitat and distribution vertebrate and invertebrate
species) (ACIA, 2004) has a direct influence on the occurrence of parasites
and the potential for emergence of disease (Kutz et al., 2004, 2009a).
Cumulative (long-term) processes and extreme (short-term) events influ-
ence the occurrence of parasites and may mediate functional and numerical
responses that determine distribution (Hoberg et al., 2008b). Many northern
parasites are adapted to cold environments and short transmission win-
dows. Long-term processes such as incremental increases in global temper-
ature acting on regional and landscape scales can reduce generation times,
increase developmental rates and broaden seasonal windows for transmis-
sion (Hoberg et al., 2001; Kutz et al., 2005; Jenkins et al., 2006; Kutz et al.,
2012). In contrast, extreme weather events can result in the explosive emer-
gence of disease leading to mortality and morbidity at regional and local
scales (Ytrehus et al., 2008; Laaksonen et al., 2010). Significantly, extreme
events may emerge from patterns that are cumulative and established over
multiple years such as mortality events linked to the nematode Setaria in
reindeer that require successive seasons of atypically high temperatures as a
driver of population amplification (Laaksonen et al., 2010).
Amplification of parasite populations responding to either cumulative
or extreme events creates a background for cascading effects within ecosys-
tems that ultimately affects biodiversity for free-living and parasitic species
(Kutz, et al., 2005; Galaktionov et al., 2006; Kutz et al., 2009b). Concurrently,
northern range expansion for many vertebrate species will create new
opportunities for exposure of naive host populations to an array of patho-
gens (Brooks and Hoberg, 2006, 2007; Lawler et al., 2009; De Bruyn, 2010).
Interacting with overall habitat change and other biotic and abiotic factors,
disease can have an influence on the availability of food resources on which
northern communities are dependent. Consequently, parasites must be
explored (1) in the context of ecosystem function, stability and sustainabil-
ity; (2) as emerging pathogens that may directly influence subsistence food
webs and food security at high latitudes under a regime of environmen-
tal perturbation and (3) as potentially threatened components of northern
systems that may lack a capacity for adaptation to shifting environmental
conditions or may be eliminated through competition with new invaders
(e.g. Kutz et al., 2004, 2009b; Tryland et al., 2009; Laaksonen et al., 2010).
What had been a pursuit driven by curiosity has now gained currency
as a cornerstone in discussions about the fate of ecosystems and species
under a regime of accelerated climate change in northern systems. There
is an urgent need to document biodiversity for assemblages of proto-
zoan and helminth parasites at regional to local scales and particularly
those that are recognised and potential zoonoses (e.g. Rausch, 1972, 1974;
Polley and Thompson, 2009). Concurrently, northern systems can serve
as models for change and cascading impacts on diversity as environmen-
tal perturbation expands (e.g. Hoberg, et al., 2008a,b; Kutz et al., 2009b).
Parasites have consequences for sustainability of tundra and high-latitude
ecosystems, wildlife populations, patterns of potential extinctions and
ultimately human occupation in the North where indigenous cultures
are dependent on subsistence food chains (Rausch, 1951; Callaghan et al.,
2004a; Brook et al., 2009) (Table 1.2).
TABLE 1.2 Why study parasites in the North?

General phenomena
• Ecological/historical indicators – the stories that parasites relate about the
biosphere in a continuum from evolutionary to ecological time (Brooks and
McLennan, 1993; Hoberg, 1997a)
• General models for transmission and disease explored in relatively low-diversity
systems (e.g. Irvine et al., 2000; Kutz et al., 2005; Laaksonen et al., 2010)
• Invasion biology in evolutionary and ecological time (Hoberg, 2010)
Environmental perturbation
• Unprecedented acceleration of environmental change in high-latitude
systems relative to the Pleistocene (ACIA, 2004; Callaghan et al., 2004a)
• Necessity to understand host–parasite systems in a regime of accelerated
change (e.g. Hoberg et al., 2008a; Kutz et al., 2009b)
• Analogues for prediction about processes and impact (indirect and direct)
of environmental change (Hoberg, 1997a; Brooks and Hoberg, 2006)
• Ecosystem sustainability
• Food safety and security in high-latitude communities (Bradley et al., 2005)
1.2.1. Developing knowledge of parasite diversity in the North

Knowledge of parasite diversity in the North extends into the 1800s
coincidental with the earliest biological collections in Eurasia and North
America. Studies were usually local, idiosyncratic and opportunistic,
often with minimal samples providing an incomplete glimpse of parasite
diversity among a limited spectrum of vertebrate and invertebrate hosts
in terrestrial, aquatic and marine systems. A process of discovery empha-
sised taxonomy and the identification and characterisation of diverse
macroparasites and microparasites, but usually an ecosystem approach or
historical and biogeographic context was lacking.
A more comprehensive view of parasite diversity did not emerge until
cadres of scientists initiated explorations for pathogens and disease among
wildlife and at the interface for people and northern environments (e.g.
Rausch, 1972, 1974). Beginning nearly 70 years ago, a succession of parasi-
tologists and ecologists examined the triad of host–parasite environment
to advance our understanding of the structure and function of northern
host–parasite systems. Early investigations are exemplified by pioneer-
ing survey and inventory to document diversity in the Brooks Range and
other regions of Alaska in the late 1940s (e.g. Rausch, 1951, 1952, 1957,
1994) and across Eurasia and the Russian Arctic (e.g. Kontrimavichus,
1969; Gvozdev et al., 1970; Boev, 1975; Priadko, 1976; Ryzhikov et al.,
1978, 1979). These studies established models and baselines for defining
the structure and nature of diversity. Further, they began to recognise the
relationship of indigenous peoples on the land and their interactions with
and dependence on wildlife, through culture and subsistence food webs,
that served as determinants of parasitic infection and diseases (e.g. Babbot
et al., 1961; Cameron and Choquette, 1963; Rausch, 1951). Classical and
elegant research in parasitology has been conducted at high latitudes, par-
ticularly that emphasising parasites transmissible to people (e.g. Rausch,
1967, 2003a). Despite a century of field-based survey and inventory, how-
ever, much remains to be revealed about the extremely diverse world of
parasitic organisms (e.g. Hoberg et al., 2003; Cook et al., 2005).
A morphologically based view of diversity that established the founda-
tions for understanding species associations and distributions (e.g. Rausch,
1952, 1957, 1976, 1994) is now increasingly complemented by molecular
approaches and discovery of considerable unrecognised diversity (both
species and populations) among most major groups of macroparasites
(e.g. Hoberg et al., 2003; Cook et al., 2005; Kutz et al., 2007; Koehler et al.,
2009; Lavikainen et al., 2010). For example, new species and genera of
macroparasites are being discovered in such reasonably well-studied host
groups as arvicoline rodents (e.g. Rausch, 1952; Haukisalmi et al., 2001,
2002; Wickström et al., 2003; Cook et al., 2005; Haukisalmi et al., 2006, 2009;
Makarikov, 2008), ungulates (Hoberg et al., 1995, 1999; Kutz et al., 2007) and
carnivores (Lavikainen et al., 2010, 2011; Haukisalmi et al., 2011), and sub-
stantial new information about host occurrence and geographic distribu-
tion has emerged (e.g. Kutz, et al., 2001b; Hoberg et al., 2002b; Jenkins, et al.,
2005; Galbreath, 2009; Durette-Desset et al., 2010; Laaksonen et al., 2010;
Galbreath and Hoberg, 2012). Broad integrated approaches have demon-
strated the need for both comparative morphological and molecular data
to understand patterns of cryptic parasite diversity in the North (Hoberg
et al., 2003; Pérez-Ponce de León and Nadler, 2010; Haukisalmi et al., 2011).
In the Arctic, although we have a developing understanding of spe-
cies richness and host associations, we generally lack long-term and com-
prehensive baselines for parasite biodiversity in terrestrial, aquatic and
marine systems, even for the best known host species. Absence of detailed
knowledge of parasite biodiversity has consequences for understanding
faunal structure, the role of parasites in ecosystems and patterns of emerg-
ing animal and zoonotic diseases at local to regional scales. We urgently
need to incorporate parasites into policy and management plans and to
emphasise that parasitic diseases be on the agenda for wildlife managers,
fisheries biologists and local communities. Parasitological knowledge can
be incorporated into policy and management plans through an integra-
tion of field-based survey and local knowledge, development of baselines
linked to specimens, digital data resources to assess change and predictive
spatial–epidemiological models (Hoberg et al., 2003; Marcogliese, 2005;
Waltari and Perkins, 2010). We recommend that parasites be integrated
in the broader equations for wildlife management, particularly issues
about the sustainability of wildlife populations and subsistence food
webs including concerns for food security and food safety (zoonoses and
human pathogens) (Kutz et al., 2009b). Further, an evidence-based process
is necessary to demonstrate a clear link between climate change, environ-
mental perturbation and emergence of parasites and disease that are the
foundations for robust projections about dynamic shifts in ecosystems in
the next few decades (e.g. Hoberg et al., 2008a,b; Kutz et al., 2009b).
1.2.2. Towards an integrated picture of parasite diversity

We provide an overview of the key elements of northern landscapes, with
emphasis on high latitudes of the Nearctic (northern Canada and Alaska)
and adjacent regions of the Palaearctic (Russian Far East). In describing
the origins, history and current diversity for assemblages of mammalian
hosts and parasites, we articulate a relatively comprehensive picture for
terrestrial systems to understand faunal structure and assembly in the
North. Employing specific exemplar systems, we address the physical
and biotic processes that have served as determinants of parasite faunal
diversity in space and time. These are the foundations in part for more
detailed discussion of ungulate parasite faunas (Kutz et al., 2012) and are
relevant to the range of zoonoses circulating among free-ranging hosts

and people (e.g. Bradley et al., 2005; Jenkins et al., 2011). Related papers
can emphasise contemporary diversity, the dynamics of infection and dis-
ease, patterns of emergence for pathogens, population-level effects, pro-
cesses for geographic invasion from the south and the potential impact of
parasites alone and in combination with other stressors on human health
and on the sustainability of wildlife in northern ecosystems.
Exemplar systems in the North also afford the opportunity to exam-
ine conceptual issues of coevolution, historical ecology, biogeography and
invasion biology as generalities in parasite faunal diversity (e.g. Hoberg
and Brooks, 2008, 2010). A range of host–parasite assemblages illustrate
some of the current and possible future shifts in parasite and host ecology
resulting from anthropogenic change in the North. The approaches and
investigative tools used to explore these shifts are reviewed.
In a pragmatic sense, integrated studies outlined here contribute to
resolution of real-world issues in animal and human health and decisions
in wildlife management and conservation biology. Integration is essen-
tial in serving to elucidate the role of parasites, parasitism and disease
as influential factors among populations of keystone mammals, such as
ungulates, on which northern communities are dependant. We emphasise
the necessity for using systematics, biodiversity and biogeographic and
phylogeographic information as critical foundations for placing parasites
within a broader context linking host ecology and the environment (e.g.
Hoberg, 1997a,b; Avise, 2000; Brooks and Hoberg, 2000). In recent years,
the recognition of accelerating perturbation in the North, particularly
that resulting from rapid climate change, has increased these efforts (Cal-
laghan et al., 2004d; Post et al., 2009). Further, a more relevant approach to
key issues is now facilitated by the collaborative involvement of northern
communities in the development and implementation of new strategies
for the cooperative management of wildlife resources to ensure sustain-
ability in an uncertain future (e.g. Brook et al., 2009; Kutz et al., 2009b).
Beyond the functional aspects of disease and other more subtle effects
on host biology, parasites are elegant indicators of ecological structure, bio-
geography and history in complex biological systems (e.g. Brooks, 1985;
Hoberg, 1997a; Marcogliese, 2005; Nieberding and Olivieri, 2007; Waltari
et al., 2007a,b; Hoberg and Brooks, 2008, 2010; Morand and Krasnow, 2010).
Understanding parasite biodiversity contributes to addressing several fun-
damental questions about the biosphere: (1) How have faunas been struc-
tured over time? (2) Are there general rules for assembly of faunas, and are
there primary drivers for diversification in complex associations? and (3)
Can insights from historical systems (as analogues) be used in expanding
our basis for prediction related to processes and outcomes in contemporary
systems? A subset of parasite-centric questions can be further explored:
(1) How do we explain host and geographic distributions of parasites? and
(2) What are the ecological, historical and evolutionary determinants of

parasite diversity?
In northern systems, studies of parasite diversity directly complement
our knowledge about the historical processes that have served to struc-
ture faunas and the role of episodic shifts in climate that have influenced
patterns of dispersal, isolation and speciation during the late Tertiary and
Quaternary (e.g. Rausch, 1994; Hoberg, 2005a; Hoberg et al., 2003; Cook
et al., 2005; Zarlenga et al., 2006; Waltari et al., 2007a,b; Koehler et al., 2009).
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 may respond in a regime of accelerated environmen-
tal change over time. Integration of historical processes into predictions
about a future of environmental perturbation, biotic change and shifting
patterns of species diversity is requisite (Hoberg, 1997a; Waltari et al.,
2007b; Provan and Bennet, 2008; Galbreath et al., 2009). In a fundamental
sense, history sets the ground rules for understanding the structure of fau-
nas and the interplay of events on varying temporal and spatial scales that
have been determinants of diversity.
1.3. AN HISTORICAL (PHYSICAL–BIOLOGICAL)

SETTING FOR THE ARCTIC
History and climate interact across geography as determinants of faunal

structure, an observation that emphasises the significance of drivers in evo-
lutionary time as foundations for contemporary biodiversity (Table 1.3).
Over the past 3–5 Myr of the Pliocene and Quaternary, northern systems
have been under dynamic change and these perturbations have influenced
faunas and floras on regional to landscape scales (e.g. Schweger et al., 1982;
Dynesius and Jansson, 2000; Jansson and Dynesius, 2002; Callaghan et al.,
2004a; Brochmann and Brysting, 2008; Post et al., 2009; Sandel et al., 2011).
This important role for climate represents a central axiom that underlies
our understanding of origins and patterns of diversity among complex
host–parasite systems at high latitudes across the Holarctic (e.g. Hoberg,
1992; Rausch, 1994; Hoberg et al., 2003; Waltari et al., 2007b).
Over the past 40–50 Myr, the Holarctic region linking Eurasia, the
Nearctic and Greenland represented a largely contiguous landmass with
interconnected habitats extending across high latitudes (e.g. Matthews,
1979). Substantial intercontinental expansion of mammalian faunas from
Eurasia into North America occurred near the Palaeocene–Eocene bound-
ary, about 55 million years ago (Ma), but this relatively deep history of
colonisation appears to have had minimal influence on contemporary pat-
terns of diversity in the Nearctic (e.g. Bowen et al., 2002; Beard, 2002). The
structure of contemporary faunas did not emerge until after the Miocene
TABLE 1.3 Generalities for structure and assembly of a complex northern fauna
Biological characteristics
• Extremes of seasonality/brief pulses of productivity, prolonged winter
• Low-diversity systems – both hosts and parasites
• Short trophic links
• Domination by limited number of taxonomic groups
• Fluctuations in abundance/population density for some host groups
○ Fluctuations in parasite abundance?
• Dense aggregation of hosts during breeding/calving
• Cryptic diversity in some parasite groups
• Adaptations for survival, resilience, transmission of parasites (taxon specific)
○ Longevity, large size, high fecundity, + rapid development, inhib-
ited development (or reduction in arrested development), multi-
year cycles, continuous transmission through winter
Historical characteristics
• Episodic climate and habitat perturbation
• Recurrent (episodic) expansion, isolation, fragmentation
• Spatial heterogeneity (refugia)
• Refugial effects, residual isolation related to vagility
• Prominent biotic filters – constraints leading to loss of diversity due to
limited resilience/tolerances/thresholds for development and survival in
cold, xeric environments
• Prominent abiotic filters – constraints related to temperature, precipitation
and humidity
(based on Hoberg et al., 2003; Callaghan et al., 2004a; Shafer et al. 2010)
(between 23 and 5.3Ma) as otherwise equitable climatological conditions

across the region began a gradual cooling trend that culminated in the
inception of major cycles of glaciation of the Northern Hemisphere near
3.5Ma in the late Pliocene (between 5.3 and 2.6Ma) (Andersen and Borns,
1994). Subsequent to the late Pliocene, northern ecosystems developed
under a regime of dynamic climate change and episodic perturbations
of both the physical landscape and a complex biota leading to consider-
able transformation and turnover for ecological structure (e.g. Hopkins,
1959; Guthrie, 1990; Jansson and Dynesius, 2002; Callaghan et al., 2004a,d;
Guthrie, 2006). Over time through the Pleistocene (2.6Ma to 10Ka), the
fauna became increasingly Arctic-adapted and constrained by low tem-
perature and humidity.
Glaciation and vast ice sheets were the dominant theme for circumpo-
lar habitats above 60°N during the late Quaternary that encompasses the
Pleistocene and Holocene (e.g. Callaghan et al., 2004a) (Fig. 1.2). In excess of
20 glacial–interglacial cycles have been identified across the 2.6 Myr of the
FIGURE 1.2 Polar projection of the geographic distribution of continental glaciers and
glacial refugia in the Holarctic region during the last glacial maximum about 18Ka show-
ing the position of Beringia and the Bering Land Bridge. Major continental ice masses are
shown in grey, and the extent of exposed continental shelf is stippled. The Arctic Circle
(66º33′N) is indicated with a dotted line. Substantial refugial zones were present in (1)
Beringia and peripheral habitats at high latitudes of North America and eastern Eurasia,
(2) isolated zones between or within the Cordilleran and Laurentide ice sheets, including
the ice-free corridor that developed at the end of the Pleistocene, (3) along the western
coastal zone, including the Alexander Archipelago and Queen Charlotte Islands, and (4)
in periglacial habitats south of the ice sheets. This figure was produced based on infor-
mation presented by Pielou (1991), Dyke et al. (2004), Harington (2005) and Shafer et al.
(2010) and modified from Hoberg et al. (in press-a).
Pleistocene; during the late Pliocene and early in the Pleistocene, these oscil-
lations occurred on roughly 41 thousand year (Kyr) cycles, which shifted to
100 Kyr episodes after about 800Ka (Muller and MacDonald, 1997; Jansson
and Dynesius, 2002). During recurrent glacial maxima, substantial reduc-
tions in sea level (−120m lower than contemporary levels) exposed areas
of continental shelf allowing biotic expansion between Eurasia and North

America (Hopkins, 1959). Continental glaciation partitioned habitats, partic-
ularly in the Nearctic. Glaciation was not universal and critical ice-free zones,
or refugia with considerable implications for faunal structure and continuity
(Fig. 1.2), existed in high latitudes of Asia and North America (e.g. Haring-
ton, 2005; Shafer et al., 2010). In North America, refugial zones occurred at
varying temporal and spatial scales including habitats north and south of
the Laurentide–Cordillera ice sheets, at fine scales in the borderlands of these
continental glaciers, along the northwestern coastal zones and apparently in
the high Arctic (Rand, 1954; Callaghan et al., 2004a; Shafer et al., 2010).
1.3.1. Exploring the Beringian connection

Cyclical processes for alternating episodes of glacial advance and reces-
sion had a pervasive influence on the distribution and structure of floras
and faunas across the region (e.g. Andersen and Borns, 1994; Jansson and
Dynesius, 2002; Abbott and Brochmann, 2003). Drivers for diversity and
structure across the circumpolar north are exemplified by processes iden-
tified in Beringia and adjacent regions of the Nearctic where the dynamics,
patterns and consequences of episodic change are particularly evident at
both intercontinental and regional–intracontinental scales (e.g. Fedorov
and Stenseth, 2002; Galbreath and Cook, 2004; Galbreath et al., 2009;
Shafer et al., 2010). The geographic limits of Beringia have been defined
in a variety of ways to emphasise different geologic and biogeographic
aspects of the region spanning eastern Siberia and northwestern North
America (Harington, 2005) (Fig. 1.3). As first envisioned by Hultén (1937),
who described the region based on phytogeographical evidence, Beringia
encompassed the area between Russia’s Lena River (125°E) and Canada’s
Mackenzie River (130°W). Later authors distinguished between broad and
narrow geographic designations. For example, Yurtsev’s ‘Megaberingia’
(1974) and Sher’s ‘Beringida’ (1984) placed the western boundary of the
region at the Taimyr Peninsula (100°E) or further west, but both authors
also described more narrowly delineated Beringian zones centred around
the Bering Isthmus and Strait. The Great Beringia concept of Yurtsev
(1974) places the western boundary at the Kolyma River (160°E), which
is consistent with a growing body of comparative phylogeographic evi-
dence showing genetic discontinuities in the same area (Hewitt 2004a,b).
Beringia, as a faunal province during the Pleistocene, was thus the
nexus or crossroads for the northern continents. Steppe landscapes dur-
ing glacial maxima were a filter bridge for biotic expansion out of Eurasia
for a diverse terrestrial fauna (Hopkins, 1959, 1967; Kontrimavichus, 1976;
Hopkins et al., 1982; Pielou, 1991; Sher, 1999; Waltari et al., 2004, 2007b;
Elias and Crocker, 2008) and for human colonisation of North America
(Dixon, 2001; Hoffecker et al., 1993). Further, Beringia served as the primary
FIGURE 1.3 Geographic region of the Bering Land Bridge and maximal extent of Late
Pleistocene glaciations in Beringia about 18Ka (from Galbreath and Cook, 2004). The
Kolyma Uplands are a putative historical barrier that may have further defined the
borders of western Beringia. During episodic glacial stages from the Pliocene through
the termination of the Pleistocene, Beringia served as the gateway for expansion by a
terrestrial biota from Eurasia into North America.
intersection for marine exchange between the Atlantic and Pacific basins
via the Arctic Ocean during interglacial periods (e.g. Vermeij, 1991; Hoberg,
1992). This province has been critical for the origins and maintenance of
an arctic-adapted fauna, as a primary dispersal corridor and as a source
region that has influenced the continuity of the Holarctic biota (Guthrie and
Matthews, 1971; Hopkins et al., 1982; Rausch, 1994; Hoberg, 1995; Sher,
1999; Repenning, 2001; Hoberg, 2005a; Waltari et al., 2007b).
Episodic faunal expansion, geographic colonisation and cycles of isola-
tion have occurred at different modes and tempos extending from the late
Tertiary through the Quaternary in response to fluctuations in climate and
shifts in environmental and ecological structure (e.g. Hoberg, 1992; Rausch,
1994; Hoberg, 1995; Lister, 2004; Waltari et al., 2004, 2007b; Hoberg 2005a;
Galbreath, 2009; Koehler et al., 2009). Biotic expansion in terrestrial systems
has been predominately asymmetrical, involving eastward dispersal from
Eurasia into the Nearctic as evidenced by diverse assemblages of mammals
(soricomorphs to ungulates) and their associated micro- and macroparasite
faunas (Waltari, et al., 2007b). Ecologically and phylogenetically disparate
terrestrial faunas including nematodes in lagomorphs and artiodactyls
(Hoberg, 2005a; Durette-Desset et al., 2010), helminths inhabiting carni-
vores (Rausch, 1994; Zarlenga et al., 2006; Koehler et al., 2009; Haukisalmi
et al., 2011), the cestodes infecting arvicoline rodents and Ochotonidae
(Haukisalmi et al., 2001; Wickström et al., 2003; Cook et al., 2005; Haukisalmi
et al., 2006; Galbreath, 2009; Galbreath and Hoberg, 2012; Makarikov et al.,
in press) all exhibit general patterns of episodic biotic expansion and iso-
lation between the Palaearctic and Nearctic (and at fine intracontinental
scales) at specific times during the late Tertiary and Quaternary (Fig. 1.4).
Adjacent Beringian marine biotas exhibit complementary patterns linking
the Atlantic, Arctic and North Pacific basins within similar temporal limits
(e.g. Hoberg, 1992, 1995; Hoberg and Adams, 2000; Hoberg et al., 2003).
1.4. FAUNAL STRUCTURE – EVIDENCE FOR NORTHERN

CONNECTIONS
Beringian parasite assemblages, both marine and terrestrial, represent

elegant exemplars for exploring the intricacies of geographic colonisa-
tion in shallow evolutionary time (Hoberg, 1992, 1995; Rausch, 1994;
Haukisalmi et al., 2001; Hoberg et al., 2003; Wickström et al., 2003; Cook
et al., 2005; Haukisalmi et al., 2006; Zarlenga et al., 2006; Waltari et al.,
2007b; Galbreath, 2009; Koehler et al., 2009). It is evident, however, that
considerably broader phylogeographic inference has been achieved
for recognised mammalian host groups than for many of the specific
host–parasite assemblages (Waltari et al., 2007b; Shafer et al., 2010).
In northern systems, much remains to be discovered relative to basic
issues of biodiversity (species richness and distribution) and the struc-
ture and development of faunal associations (Hoberg et al., 2003; Cook
et al., 2005; Waltari et al., 2007b). We explore a series of four exemplar
assemblages that represent phylogenetically and ecologically disparate
mammalian groups and their parasites in terrestrial environments to
demonstrate general and specific patterns for the history of faunal asso-
ciations.
1.4.1. Faunas associated with terrestrial Carnivora

• The parasite groups: Cestoda – Cyclophyllidea, Taeniidae (Taenia,
Echinococcus); Diphyllobothriidea (Diphyllobothrium); Nematoda –
Ascaridida (Baylisascaris, Toxascaris); Strongylida, Ancylostomatoidea
(Uncinaria), Molineoidea (Molineus); Enoplida, Dioctophymatoidea
(Soboliphyme), Trichinelloidea (Trichinella) (Table 1.4).
• The host groups: Carnivora – Canidae (Canis, Vulpes), Felidae (Lynx),
Mustelidae (Mustela, Martes, Gulo), Ursidae (Ursus).
• Taxonomy for hosts is consistent with Wilson and Reeder (2005). Tax-
onomy for nematodes is consistent with Anderson (2001); for cestodes,
it is based on Kahlil et al. (1994) with modifications proposed by Kuchta
et al. (2008).
FIGURE 1.4 History for geographic expansion by phylogenetically disparate host–

parasite assemblages from Eurasia to the Nearctic through the Beringian region
superimposed on a view of the circumpolar region during maximum reduction in sea
level. Geographical colonisation in terrestrial systems and faunas was asymmetrical
and characterised by episodic expansion in the amphiberingian region that extended
temporally from the Pliocene through the Pleistocene. These events directly influenced
patterns of diversity and occurrence for some helminth taxa among terrestrial
(carnivorans, lagomorphs, rodents, artiodactyls and soricomorphs) and marine mammals
(pinnipeds). The history for most host–parasite assemblages in terrestrial systems relates
to origins in Eurasia and eastward expansion across Beringia into the Nearctic region
(indicated by the directionality of the solid arrows); there is minimal evidence for a west-
ward pattern of expansion or interchange (dotted arrows). The distribution of marine
systems complements those on land, where Beringia and the land bridge alternately
served as pathway or as a barrier to biotic expansion depending on prevailing climate
and sea levels. Map projection and figure is modified from Hoberg and Brooks (2010).
Contemporary groups and species with protracted histories in north-

ern systems are recognised within four clades of terrestrial carnivorans
(Kurtén and Anderson, 1980); a subclade containing Felidae and Hyaeni-
dae (feliforms) are the sister of subclades (caniforms) including Canidae,
Ursidae + Pinnipedia and Mustelidae + Procyonidae (Bininda-Emonds
et al., 2007; Nyakatura and Bininda-Emonds, 2012). Eurasian associations,
extending to the Oligocene (34–23Ma) and Eocene (56–34Ma) and earlier,
are noted for groups that are now distributed at high latitudes of North
America and the Holarctic (Kurtén and Anderson, 1980; Beard, 2002). The
Tertiary history for carnivorans has been strongly influenced by patterns
of episodic extinction, turnover and ecological replacement (Van Valken-
burgh et al., 2004). Some carnivorans, particularly canids, radiated exten-
sively in the Nearctic, but only Caninae persisted to the present and their
history extending into the Holocene links Eurasia and North America.
Multiple expansion events (both among and within certain taxa) into the
Nearctic (and to a lesser extent the Palaearctic) during the Miocene, Plio-
cene and Pleistocene established the distributions for modern taxa and
extant species assemblages (e.g. Kurtén and Anderson, 1980; Waits et al.,
1998; Vilà et al., 1999; Stone and Cook, 2002; Johnson et al., 2006; Waltari
et al., 2007b; Koepfli et al., 2008; Aubry et al., 2009); notably, Hyaenidae
also expanded from Eurasia into North America but the family is poorly
represented in the fossil record.
Events of geographic colonisation involve a number of host genera,
but relatively few species now have Holarctic distributions; the latter
include ermine (Mustela erminea), least weasel (M. nivalis), wolverine
(Gulo gulo), Arctic fox (Vulpes lagopus), red fox (V. vulpes), wolf (Canis
lupus), brown bear (Ursus arctos) and polar bear (U. maritimus). Helminth
parasite faunas encompass elements that are both specific to particular
carnivoran groups and shared based on biogeographic history, ecologi-
cal similarity, foraging behaviour and guild associations (e.g. Kontrima-
vichus, 1969; Rausch, 1994; Hoberg, 2006). Faunal structure is further
influenced by the timing, extent and number of expansion and isola-
tion events primarily during the Pliocene and Quaternary (Vilà et al.,
1999; Waltari et al., 2007b) within this phylogenetically and ecologically
disparate assemblage of Carnivora (e.g. Bininda-Emonds et al., 2007;
Koepfli et al., 2008; Nyakatura and Bininda-Emonds, 2012). Further,
changing patterns of diversity, degrees of sympatry, extinctions and fau-
nal turnover among carnivoran hosts as exemplified at intercontinental
scales and regionally in eastern Beringia may have also influenced the
occurrence of various parasite taxa (Youngman, 1993; Rausch, 1994; Van
Valkenburgh et al., 2004). In a contemporary setting, distributions and
ecological characteristics, particularly prey species and foraging pat-
terns, for carnivorans and their assemblages of parasites are among the
primary determinants or limiting factors for a number of potential and
TABLE 1.4 Species diversity and biogeography for exemplar helminth parasites among Carnivora in the Arctic and Subarctic, exploring
20
assemblages influenced by episodic climate change and geographic expansion in the Pliocene and Quaternary. Species richness is reflected
for global diversity, distributions across the Holarctic and those that are endemic to either the Nearctic or the Palaearctic
Parasite taxon Host association Distribution Species diversitya Processesb
Eric P. Hoberg et al.

Eucestoda/Taeniidae
Taenia spp. Mustelidae, Canidae, Holarctic/Beringian (45G/15H/5N/25P) GE, HC
Felidae, Ursidae (9 amphiberingian)
Echinococcus spp.c Canidae Holarctic/Beringian (10+G?/2H?/0N/6+P) GE
Eucestoda/Diphyllobothriidae
Diphyllobothrium spp. Canidae/Ursidae Holarctic/Beringian (50+G/11+H/3+N/16+P) GE, HC
Eucestoda/Mesocestoididae
Mesocestoides spp. Carnivora Holarctic/Beringian (12+G/2H/3N/8P) GE, HC
(2 amphiberingian)
Nematoda/Trichostrongylina
Molineus sp.d Mustelidae/Canidae/ Holarctic/Beringian (16+G/1H/3N/5P) GE, HC
Ursidae
Nematoda/Strongylina
Uncinaria spp. Ursidae/Canidae Holarctic/Beringian (14+G/3H/2N/4P) GE, HC
Nematoda/Ascaridoidea
Baylisascaris spp. Canidae/Mustelidae/ Holarctic/Beringian (7+G/2H/3N/1P) GE
Ursidae
Toxascaris Carnivora Holarctic/Beringian (3+G/1H/0N/2P) GE
Nematoda/Trichinelloidea
Trichinella spp. Carnivora Holarctic/ Beringian (12G/1H/2N/8P) GE, HC
Nematoda/Dioctophymatoidea
Soboliphyme spp.e Mustelidae Holarctic Beringian (9G/2H/0N/7P) GE, HC, R
a Species diversity relative to regions: G = global, H = Holarctic, N = Nearctic, P = Palaearctic.
b Processes include geographic expansion = GE; host colonisation = HC; refugial effects = R.
c Echinococcus systematics remain in flux. There are 10 putative species recognised. Two endemic species are distributed in the Neotropical region; no species are
known to be endemic to North America. Aside from the Holarctic E. multilocularis and ‘E. granulosus’ all other known species occur in the Old World (see Nakao
et al., 2007).
d Primary diversity for Molineus is found in the tropics of southern Asia and in the Neotropical region. The single Holarctic species has a broad distribution among
carnivorans.
e T he genus Soboliphyme includes nine species, eight of which occur as parasites in soricomorphs; S. baturini is the only species in carnivore definitive hosts and is one
of two Holarctic species (Koehler et al., 2009).
Northern Host–Parasite Assemblages

21
recognised zoonotic protozoans, tapeworms and nematodes that can

circulate in human hosts (e.g. Rausch, 1956, 1994; Rausch and Fay, 2011).
Mustelids have a relatively long trans-Beringian history with successive
expansion events into the Nearctic occurring over extended time frames
and during different intervals beginning in the late Miocene (Kurtén and
Anderson, 1980; Koepfli et al., 2008). Diversification and assembly of the
extant high-latitude fauna, composed of weasels (Mustela spp.), fisher (Mar-
tes pennanti), wolverine and martens (Martes spp.), have resulted from a
minimum of four independent events of geographic colonisation into North
America during the Pliocene and Pleistocene. Refugial effects in periglacial
habitats north and south of the Laurentide–Cordillera systems and in the
western coastal zone along with patterns of secondary expansion appear
as important determinants for diversification and distribution among two
species of martens, M. americana and M. caurina, in North America (Stone
and Cook, 2002; Stone et al., 2002). Martens demonstrate distinct patterns
of divergence between continental and coastal refugial populations. In con-
trast, there is only one species of wolverine across the Holarctic. In North
America, genetic divergence, although minimal, indicates endemic wolver-
ine populations occupying Southeast Alaska, the Kenai Peninsula and the
central Canadian Arctic, reflecting dispersal from Beringia following the
termination of the Pleistocene (Tomasik and Cook, 2005). Weasels (Mustela
spp.) represent yet another expansion event into North America from the
Palaearctic across Beringia (Fleming and Cook, 2002).
Felids have a deep history across the Holarctic, initially being recog-
nised in the faunas of Eurasia and North America near the Eocene–
Oligocene boundary (Kurtén and Anderson, 1980). Contemporary felid
lineages, however, have initial origins linked to Eurasia and the divergence
of large cats, with this region serving as a source area for later colonisation
of Africa and the Nearctic (Johnson et al., 2006). Expansion across Berin-
gia occurred in the Miocene (about 8.0–8.5Ma) leading to establishment
and radiation of three extant lineages (ocelot, lynx and puma), only one
of which (Lynx) has had continuity at high latitudes (Johnson et al., 2006).
Secondarily, North America served as a centre of diversification for felids,
with dispersal events into South America (ocelot), and Eurasia (cheetah,
lynx) during the Pliocene. Large cats in the Panthera lineage, including
lions, attained exceptionally broad geographic distributions in the Pleisto-
cene, which extended from South America to Eurasia and Africa across the
Bering Land Bridge (Kurtén and Anderson, 1980). Panthera leo persisted in
Beringia late into the Wisconsinan and would have represented an impor-
tant component of a complex fauna of mega- and mesocarnivores. The
contemporary Lynx canadensis occurs across the boreal forest zones of the
Nearctic and is sporadically present on the tundra coinciding with periods
of high abundance for snowshoe hare (Lepus americanus) (MacDonald and
Cook, 2009).
Canidae arose in the Eocene–Oligocene of North America and Eurasia

and radiated extensively through the Miocene with considerable diversity
now characterising the global fauna (Nowak, 1999; Bardeleben et al., 2005).
Beringia figured prominently as a gateway into the Nearctic and in some
cases downstream to the Neotropical region, although only three species
among the Caninae or true dogs and foxes now occur at high latitudes
(Kurtén and Anderson, 1980). Broad distributions in the Holarctic are known
for grey wolf (C. lupus), red fox (V. vulpes) and Arctic fox (V. lagopus). Domestic
dogs (C. lupus familiaris) are also considered within this assemblage.
Although wolves appeared in North America by 2Ma, the grey wolf
(as a putative descendant of C. etruscus) has origins in Eurasia about
700Ka with first occurrences in the Nearctic via the Bering Land Bridge
by the middle Pleistocene (Kurtén and Anderson, 1980; Vilà et al., 1999).
Wolves were well represented among carnivore faunas of eastern Berin-
gia as highly vagile predators capable of dispersing over considerable
distances (Guthrie, 1968a). There is evidence of multiple expansion
events from Eurasia into North America during glacial stages over the
late Pleistocene, with ranges subsequently extending far to the south
during interglacials (Vilà et al., 1999). Notably, wolf populations occupy-
ing former coastal refugial zones are genetically distinct from those with
broader continental distributions, indicating effective barriers to gene
flow over the late Pleistocene (Weckworth et al., 2005). Recurrent pat-
terns for episodic expansion, however, have often obscured population
structure and history and constitute factors that likely influenced species
and genetic diversity for parasites associated with these large carnivores.
Dogs at high latitudes are initially recognised in fossil assemblages dat-
ing to near 20Ka in eastern Beringia (e.g. Kurtén and Anderson, 1980).
Red fox, in contrast, initially arrived in North America during the
Illinoian glaciation (130–200Ka) or earlier. During the Sangamon, interglacial
(110–130Ka) foxes occurred in forested habitats at temperate latitudes with
isolated populations, leading to discrete eastern and western clades, dis-
tributed south of the Laurentide during the Wisconsinan (about 110–12Ka)
(Aubry et al., 2009). Foxes representing this early colonisation of North
America became extinct in Beringia and were later replaced by those of
Eurasian origin during the middle Wisconsin. In North America, foxes now
occur as isolated populations of disparate ages and ancestry: (1) endemic
populations (montane and eastern subclades) and their descendents that
have been resident since at least the Illinoian and (2) a Holarctic lineage
composed of populations with Eurasian ancestry that expanded into east-
ern Beringia during the Wisconsinan and eventually south and east as far as
Alberta and the Northwest Territories at the termination of the Pleistocene
(Aubry et al., 2009). Further, foxes have been extensively translocated in the
last century such that populations may now include admixtures (mosaics)
of exotic introduced animals and endemics at some localities. These patterns
may have particular implications for the distribution of such zoonotic para-
sites as Echinococcus multilocularis and Taenia crassiceps. For example, it is not
clear whether or not all red foxes (irrespective of ancestry and origin) (1) are
equally susceptible to infections by these taeniids, (2) have been components
of larger assemblages of canid hosts and parasites or (3) if secondary contact
and host switching have occurred over time.
Arctic foxes are related to an assemblage of red fox-like canids with ori-
gins in Eurasia during the Villafranchian (1–3Ma, bordering the late Plio-
cene and lower Pleistocene). These foxes secondarily expanded across the
circumpolar region during the Wisconsinan (Kurtén and Anderson, 1980;
Rausch, 1994; Bardeleben et al., 2005) and are highly adapted to harsh
frigid and xeric conditions that characterise high-latitude tundra, coastal
and pack ice habitats. In contrast to a broad assemblage of terrestrial mam-
mals, glacial events in the Quaternary did not serve as isolating mecha-
nisms for Arctic fox (Dalén et al., 2005). Foxes were isolated in response
to warming conditions and persisted in high Arctic refugia during the last
interglacial (Sangamon, ending about 117Ka) and subsequently underwent
rapid population and geographic expansion to become widely distributed
in Wisconsinan time across the circumpolar region. Extensive contempo-
rary gene flow is related to long-range dispersal in circumpolar habitats
for arctic fox and little population differentiation has been demonstrated
(Dalén et al., 2005). Across this region, two ecotypes are recognised includ-
ing a ‘lemming’ morph that targets Lemmus and Dicrostonyx as primary
prey (Eurasia, North America, Canadian Archipelago and East Greenland)
and ‘coastal’ adapted forms (Svalbard, Iceland, west Greenland) that for-
age nearshore on birds, eggs and carrion. Such differences in foraging and
distribution may influence the patterns of occurrence of E. multilocularis
and its relationship to potential human infections (Henttonen et al., 2001).
The bears, Ursidae, have a complex history linking Eurasia and North
America, with evidence of multiple expansion events into the Nearctic over
the late Tertiary and Pleistocene (Talbot and Shields, 1996a; Yu et al., 2004).
Tremarctine bears (species of Tremarctos and Arctodos) radiated in North
America but are now represented only by the spectacled bear (T. ornatus)
in South America. Ursine bears radiated initially in the Palaearctic and
include three species (black bear, Ursus americanus; brown bear, U. arctos,
and polar bear, U. maritimus) with independent histories in North America
(Kurtén and Anderson, 1980). Tremarctine and ursine bears would have
been contemporaneous and sympatric at localities in Beringia and south of
the Laurentide during the Pleistocene (Kurtén and Anderson, 1980).
Black bears have origins in Eurasia during the Pliocene, and U. ameri-
canus was widely distributed in North America by the mid-Pleistocene in
localities south of the Laurentide (Kurtén and Anderson, 1980). Contem-
porary black bears appear to be immigrants from the south, arriving in
the former Beringian refugium and at higher latitudes in North America
during the Holocene (Guthrie, 1968a). Distinctive lineages for coastal (SE
Alaska) and continental populations are now recognised (e.g. MacDon-

ald and Cook, 2009), consistent with an extended history of occupation in
nearshore refugia during the Pleistocene (Heaton and Grady, 2003).
Brown bears have origins in Eurasia during the Villafranchian but are
not seen in eastern Beringia and North America until the early Wisconsinan,
although this species may have been more widespread to the south of the
Laurentide prior to the late glacial stages of the Pleistocene (MacDonald
and Cook, 2009). The distribution of genetic diversity for brown bears in
the Nearctic is consistent with a complex history involving multiple expan-
sion events across Beringia and patterns of refugial isolation during glacial
maxima (Heaton and Grady, 1993; Waits et al., 1998; Heaton and Grady,
2003). Similar to black bears, there has been recognition of genetically dis-
tinct coastal and continental populations of brown bear in North America,
highlighting the importance of former refugial zones in the Alexander
Archipelago of SE Alaska (Talbot and Shields, 1996b; Waits et al., 1998).
Polar bears are closely related to brown bears, and it was thought that
origins extended no deeper than the late Pleistocene about 150 Ka (Shields
and Kocher, 1991; Lindqvist et al., 2010). Revision of this date toward the
middle Pleistocene near 600 Ka (Hailer et al., 2012) now suggests that diver-
gence from a common ancestor with brown bears may be related to expan-
sion of perennial sea ice in the Arctic Ocean about 700 Ka (Herman and
Hopkins, 1980). Thus the structure and linkages within the Arctic Ocean
ecosystem were firmly established at that time. Further, a history of diver-
sification extending to the middle Pleistocene implies these highly adapted
Arctic marine carnivores have persisted across multiple glacial-interglacial
cycles through the late Quaternary. as is apparent for some other high
latitude mammals (Lister, 2004). These bears are highly vagile, obligate car-
nivores (usually apex predators of marine mammals) primarily associated
with open ice pack and high-latitude tundra environments around the cir-
cumpolar region. Individuals are wide ranging over long distances, as indi-
cated by minimal differentiation among populations around the Arctic basin
(e.g. Peatkau et al., 1999). Similar to Arctic foxes, extensive travel by polar
bears may serve to mediate gene flow for some parasites, such as Trichinella
nativa, that circulate in an assemblage of high-latitude carnivores in marine
and terrestrial environments. Interestingly, the helminth fauna of polar
bears is limited, reflecting to some extent a specialized diet of pinnipeds
and carrion, and a relatively extended association with offshore marine
environments over the terminal Quaternary.
1.4.1.1. Trichinella and carnivorans

Species of Trichinella circulate in sylvatic cycles among guilds of mesocarni-
vores (felids, canids and mustelids), ursids, some pinnipeds and an array of
omnivorous prey species including rodents and soricomorphs in the Palaearc-
tic and Nearctic (Pozio 2005; Pozio et al., 2009). Carnivory and scavenging
FIGURE 1.5 Biogeographic history for species of Trichinella (T1–T12), following origins in
Eurasia and periods of expansion through Beringia and other regions. The current species
phylogeny for Trichinella is mapped to show the history of distribution (modified from
Pozio et al., 2009). A single species, T. nativa (T2), has a Holarctic distribution, whereas
two others endemic to North America (T. murrelli – T5, and T6) have origins subsequent
to episodes of geographic colonisation by carnivores from Eurasia during the Pleisto-
cene. The occurrence of T12 is attributed to trans-Beringian expansion with felids into
South America during the Miocene. These patterns demonstrated for Trichinella serve
as a primary exemplar for the process of geographic invasion and its influence on faunal
structure and diversification in a variety of other host–parasite assemblages in phyloge-
netically diverse mammals in terrestrial systems.
represent the primary routes for transmission and have been central to pro-
cesses of diversification associated with patterns of host switching and geo-
graphic colonisation. Among encapsulated forms, there are currently nine
designated genotypes or named species (Pozio et al., 2009). Biogeography
and radiation for species of Trichinella in carnivoran (feliforms and caniforms)
and other mammalian hosts have involved high-latitude regions of the Hol-
arctic since the Miocene (Zarlenga et al., 2006; Pozio et al., 2009). Following
initial diversification in Eurasia, four discrete events for biotic expansion into
the Western Hemisphere occurred across the Bering Land Bridge (Fig. 1.5)
influencing five species among the nine recognised genotypes: (1) through the
Nearctic to the Neotropical region during the late Miocene with an early felid
lineage prior to the emergence of the Panamanian Isthmus resulting in the T12
genotype; (2) multiple isolation events in North America from an Holarctic
assemblage near the Pilocene–Pleistocene boundary (2.5–3.0 Ma) leading to T.
murrelli (T5, in temperate to boreal zones) and later divergence of T. nativa (T2,
southern limit defined by the January – 4°C isotherm) and the genotype T6
(boreal to Subarctic) near 400–500Ka and (3) origin of the genotype T9 in Japan
either by expansion from the Nearctic or by peripheral isolation within the
crown group of Trichinella. The contemporary distribution for Trichinella nem-
atodes in mustelids, ursids, canids and other carnivores provides evidence
for the role of extensive host switching (driven by the dynamics of foraging
guilds) and episodic expansion out of Eurasia (Zarlenga et al., 2006; Pozio
et al., 2009). Temporal estimates for arrival of mustelids, some canids and bears
in the Nearctic, as outlined previously, appear to coincide with the history for
diversification of this assemblage of Trichinella at high latitudes. Geographic
distributions and patterns of speciation were further determined by refugial
effects at inter- and intracontinental scales (e.g. relative to the Laurentide and
Cordillera ice masses) (Pozio et al., 2009). Mosaic faunas are apparent where
species resulting from independent processes of geographic colonisation dur-
ing the Quaternary are circulating in sympatry following secondary expan-
sion in the Holocene across regional settings and at some localities.
At high latitudes, the freeze-resistant T. nativa is the primary source for
infections in people, through consumption of bears and walrus (Odobenus
rosmarus), although a broad array of mammals may be infected (Dick and
Pozio, 2001). Polar bear, wolverine and Arctic foxes may be particularly
important in maintaining a broad geographic range for the parasite. Genetic
structure for T. nativa may parallel that demonstrated among the highly
vagile hosts involved in circulation, where considerable levels of gene flow
mediated by polar bears and Arctic foxes in the circumpolar region would
be predicted.
Historically, Trichinella has been part of the landscape in northern sys-
tems, representing a primary zoonotic parasite possibly recognised since
arrival of the first human immigrants from Eurasia. For example, tradi-
tionally in Alaska, meat from bears is not consumed raw but is always
cooked due to the threat of infection by these nematodes (Rausch, 1972).
Accelerated climate change in northern systems is now predicted to drive
shifts in the distribution of Trichinella spp. as the structure of marine food
chains is altered over time leading perhaps to increased levels of exposure
to infections for people (Rausch et al., 2007).
1.4.1.2. Soboliphyme baturini in Mustelidae

Among nine species of Soboliphyme, seven occur as parasites of soricomorph
definitive hosts (both shrews, Soricidae, and moles, Talpidae) from Eurasia,
whereas single species occur, respectively, in a soricid from the Nearctic and
in small to medium carnivorans from northeastern Eurasia and northwestern
North America (Ribas and Casanova, 2006; Karpenko et al., 2007; Koehler
et al., 2007). A broad distribution in Palaearctic soricomorphs appears consis-
tent with radiation for this parasite group in Eurasia, with secondary expan-
sion into North America during the Pliocene and Quaternary.
Soboliphyme baturini, a characteristic large nematode occurring in the stom-

ach of mustelids, and occasionally other mesocarnivores, is a primary para-
site among species of Martes with a geographically widespread range centred
on the amphiberingian region (landmasses encompassing greater Beringia
in the Nearctic and Palaearctic) (Kontrimavichus, 1969; Koehler et al., 2007).
Transmission is dependent on a complex lifecycle involving oligochaete first
intermediate hosts, and soricomorph, or less often arvicoline, paratenic hosts
(Karmanova, 1968; Karpenko et al., 2007; Koehler et al., 2007).
The history for S. baturini contrasts with species of Trichinella in that a
narrow spectrum of congeneric host species has been involved in bioge-
ography and evolution of the assemblage. Gene flow, patterns of isolation
and population structure are mediated by relatively few host species for S.
baturini, whereas guild dynamics and a phylogenetically disparate array of
carnivorans and omnivores with varying levels of vagility characterise Trich-
inella (Zarlenga et al., 2006; Koehler et al., 2009). Soboliphyme baturini provides
insights about geographic expansion and isolation as drivers for the Nearctic
fauna. Phylogeographic analyses exploring sequence data from multigene
systems demonstrated a relatively shallow history with minimal diversifi-
cation (Koehler et al., 2009). Population structure revealed for parasites is
related to geographical and physical events rather than cospeciation linked
to hosts and host phylogeny (Koehler et al., 2009; Hoberg et al., in press a).
Subsequent to an origin in Eurasia, geographical expansion and col-
onisation by S. baturini extended eastward across Beringia into Alaska
with the ancestor of M. caurina + M. americana as early as 1Ma during a
middle Pleistocene glacial cycle (Stone et al., 2002; Koepfli et al., 2008).
As of the late Pleistocene, coincidental with the early maximum of the
terminal Wisconsin glacial cycle 65–122Ka, these two species of martens in
North America were distributed south of the Cordillera and Laurentide in
western (M. caurina) and eastern (M. americana) refugia (Stone et al., 2002).
Although host speciation occurred over this million years of divergence,
similar patterns for diversification of Soboliphyme are not recognised, and
the associations of S. baturini with M. caurina and M. americana represent a
complex temporal and spatial mosaic.
Phylogenetic and phylogeographic structure for Soboliphyme is consis-
tent with geographic colonisation from Eurasia across Beringia and an ini-
tial north to south expansion with sequential isolation in insular (SE Alaskan
archipelago) and coastal refugial zones extending along the western shore
of North America. Relatively extensive genetic diversity in coastal popula-
tions of S. baturini indicates an extended period of geographic occupation
and persistence of the assemblage in putative ice-free refugial zones for hosts
and parasites leading up to the terminal Wisconsinan (Koehler et al., 2009).
Parasite populations in the coastal zone are represented by a mosaic of older
endemics (with extensive and local genetic variation), more recently derived
colonisers (where genetic diversity is not strongly partitioned geographi-
cally), and translocated or introduced populations that have discordant
histories relative to geography (Hoberg et al., in press-a). In these instances,

parasites serve as robust indicators with genetic signals that demonstrate
complex histories for persistence of endemic populations, secondary zones of
contact and the influence of anthropogenic translocation on faunal structure.
1.4.1.3. Taenia tapeworms and carnivorans

Species of Taenia are obligate parasites of carnivores and depending on
the species involved have rodents, lagomorphs or ungulates as interme-
diate hosts; complex life cycles are directly defined by predator–prey rela-
tionships (Loos-Frank, 2000; Hoberg, 2006). Approximately 45+ species
occur in the global fauna, with 13 distributed at high latitudes among
mustelids, canids, felids and ursids across the Holarctic (e.g. Rausch,
1994, 2003b; Lavikainen et al., 2010, 2011; Haukisalmi et al., 2011). Sys-
tematics for Taenia is in a state of flux, with increasingly robust sampling
now becoming available that will support testing of current phylogenetic
hypotheses (e.g. Hoberg, 2006; morphological) based on multi-locus
molecular data (e.g. Lavikainen et al., 2008).
Among mustelids, four species of Taenia occur in Martes spp. (T. interme-
dia across the Holarctic; T. martis in Eurasia), G. gulo (T. twitchelli, Holarctic)
and Mustela spp. (T. mustelae, Holarctic) (Rausch 1977, 1994, 2003b). Excluding
T. mustelae, these species form a subclade of taeniids that primarily occur in
mustelid hosts (Hoberg, 2006). Taenia intermedia is a typical tapeworm among
Pacific and American marten and fisher from North America and in sable from
eastern Siberia. Taenia twitchelli is a specific cestode of wolverines and exhibits
an amphiberingian distribution linking the Nearctic and Palaearctic. Coinci-
dental with the host group, these distributions demonstrate a history of inde-
pendent expansion across Beringia from Eurasia with subsequent isolation in
the Nearctic during the Pliocene and Pleistocene. More broadly, the host distri-
butions reflect a deep coevolutionary association as suggested by sister group
relationships linking the Procyonidae, Mustelidae and their specific species of
Taenia (e.g. Hoberg 2006; Bininda-Emonds et al., 2007; Nyakatura and Bininda-
Emonds, 2012). In contrast, as the putative basal species in the genus, T. muste-
lae has broader host associations including martens and small mustelids such
as ermine, least weasel and mink (Neovison vison). An extensive range across
the Holarctic suggests a deep history extending to the Pliocene and some
level of host switching reflecting the importance of guild dynamics among an
assemblage of small carnivores as a determinant of parasite distribution.
Among canids, species of Taenia are characteristic in wolves
(T. hydatigena, T. krabbei with ungulate intermediates) and in both Arctic
fox and red fox (T. polyacantha, T. crassiceps with rodent intermediates). At
high latitudes, T. krabbei is also found in Arctic fox in both Greenland and
Svalbard. Holarctic distributions for these assemblages were apparently
attained during the Pleistocene following expansion across Beringia and
circumpolar habitats.
Considering foxes, T. polyacantha includes Eurasian (T. p polyacantha,

south of the tundra zone in red fox) and circumpolar subspecies (T. p. arctica,
Holarctic in Arctic fox and uncommon in red fox) (Rausch and Fay, 1988).
In the Nearctic, T. p. arctica is not found south of the tundra zone in red fox
(Rausch and Fay, 1988), thus it would not be expected in endemic mon-
tane or eastern clade foxes. This geographic pattern suggests that Arctic fox
and lemmings may maintain this cestode at high latitudes in the Nearctic.
This pattern may contrast with the distribution of T. crassiceps that is more
widespread in red foxes at boreal latitudes in North America. This taeniid is
known in Arctic fox and has been documented in eastern clade red fox, but
not apparently in montane foxes. Interestingly, constraints on distribution
for these taeniids may be linked to ranges occupied by arvicoline rodents
as intermediate hosts, and post-Pleistocene expansion at high latitudes may
have been initially limited by voles and lemmings (Myodes rutilus and Lem-
mus trimucronatus) and the availability of deglaciated habitats (Rausch, 1994).
Holarctic ranges for T. krabbei and T. hydatigena are likely constrained
by the temporal limits for expansion into Beringia and North America by
an assemblage involving wolves and primary ruminant (cervid) interme-
diate hosts (Rausch, 1994). Sympatry for constituents of this host assem-
blage probably extends to 2Ma in North America (Guthrie and Matthews,
1971) such that these cestodes could have become broadly established
prior to or early in the Pleistocene. The history is obscured by the unre-
solved status for T. krabbei and the recognition of multiple cryptic spe-
cies that may be widely distributed at high latitudes in canids and ursids
(Lavikainen et al., 2010, 2011). At high latitudes in the absence of wolves,
Arctic fox serve as primary definitive hosts for T. krabbei.
Ursids had not been considered as hosts for characteristic taeniids or
other cyclophyllidean tapeworms (Abuladze, 1964; Rausch, 1994). Reports
of infections by Taenia were generally limited to species such as T. krabbei or
T. hydatigena that typically circulate between canid definitive and ungulate
intermediate hosts. A putative cryptic species, similar to T. krabbei, was ini-
tially demonstrated based on sequence data from mitochondrial DNA for
cysticerci in moose (Alces alces) from Fennoscandia (Lavikainen et al., 2010).
Recently described as T. arctos, it has been shown to circulate in brown
bear (U. arctos) from both Fennoscandia and Alaska (Haukisalmi et al.,
2011; Lavikainen et al., 2011). Brown bears and moose (Alces americanus)
are relatively late immigrants across Beringia into the Nearctic during the
ultimate Wisconsinan glaciation (Kurtén and Anderson, 1980), and this
expansion may account for the apparent Holarctic distribution of this
species of Taenia. Such a distribution is consistent with radiation for Taenia
among Eurasian carnivorans prior to expansion into North America. The
occurrence of T. arctos in black bears or polar bears is unknown.
Current evidence suggests that only taeniids in mustelids show strong
evidence of associations linked to cospeciation. More generally, it appears
that geographic colonisation and guild dynamics related to common prey

species for canids, felids, hyaenids and ursids account for parasite diversi-
fication and distribution among assemblages of large carnivores (Hoberg,
2006). Taenia would have had a complex history in northern environ-
ments due to extensive levels of sympatry and episodes of synchronicity
among a diverse assemblage of carnivorans in the Pliocene and Pleisto-
cene (Guthrie, 1968a). Host switching among carnivorans within guilds
has been postulated as a primary mode for diversification among these
tapeworms where patterns of diversity may be related to the relative size
spectrum and foraging behaviour of definitive hosts. For example, arrays
of closely related species circulate through rodent intermediate hosts and
occur in mustelids, small canids and felids; similar relationships are also
apparent for transmission through ungulates including moose and cari-
bou for species of Taenia that occur in megacarnivores such as wolf, bear
and large cats (Hoberg, 2006; Haukisalmi et al., 2011).
1.4.1.4. Echinococcus spp. among canids

At high latitudes, there are two species of the taeniid Echinococcus that,
respectively, circulate in obligate predator–prey cycles among small
canids and arvicoline rodents (E. multilocularis) and among wolves (and
dogs) and ungulates including moose and caribou (tentatively, the cer-
vid strain of E. granulosus, G-8, or E. canadensis) (Rausch, 1967; Thompson
et al., 2005; Nakao et al., 2007).
The distribution of E. multilocularis reflects the intricate history of
V. vulpes in North America, although V. lagopus may have had an over-
riding role in distribution, particularly at high latitudes in the circumpo-
lar zone. Based on analyses of mitochondrial loci, recognised northern
Eurasian and North American partitions for E. multilocularis appear to
reflect distributions dating to the ultimate Sangamon interglacial, coincid-
ing with eastward expansion across Beringia during the Illinoian glacial
stage (Nakao et al., 2009). Secondarily, populations were isolated north
and south of the Laurentide with E. multilocularis persisting in Arctic fox
(St Lawrence Island samples and N1 haplotype) and possibly in the
eastern subclade of red fox during the Wisconsinan glacial maximum
(N2 haplotype); red foxes representing this early colonisation of North
America became extinct in Beringia and were later replaced by those of
Eurasian origin in the Wisconsinan. Shallower histories for populations
of E. multilocularis found in Eurasia and the amphiberingian region may
be linked to this later expansion and to the continuity of red fox across
the Palaearctic and a subsequent invasion of Beringia (A2 and A4 hap-
lotypes) (see Nakao et al., 2009). Such a history in the Beringian region
modifies the current narrative and would account for the distribution of
parasite haplotypes including endemic Alaskan and Asiatic populations
on St Lawrence Island, Alaska (Nakao et al., 2009). Such is also concordant

with the history for both Arctic fox and red fox, but corroboration requires
more comprehensive sampling across the range of E. multilocularis.
In North America, post-Pleistocene expansion to the north and west
from southern refugia involving an initial small population of parasites in
red fox may account for the apparent genetic uniformity for these cestodes
in temperate North America, although this region has yet to be adequately
sampled (Nakao et al., 2009). These populations of red fox, however,
appear to be beyond the historical limits of the endemic eastern subclade
(Aubry et al., 2009) and may also reflect interactions with introduced foxes
imported during the 1800s (Rausch, 1994). Genetic uniformity also does not
exclude the hypothesis for a recent introduction of E. multilocularis estab-
lishing the central North American focus with subsequent and ongoing
geographic expansion over the past few hundred years (Rausch, 1985). In
contrast, southward postglacial expansion of red fox out of eastern Berin-
gia into Yukon Territory and British Columbia may have been blocked by
taiga forest habitats, where the parasite apparently does not occur (Rausch,
1967). The history and biogeography for E. multilocularis would be expected
to parallel that of T. crassiceps and T. polyacantha that circulate among foxes
and arvicoline rodent intermediates (Rausch, 1994). Interestingly, a recent
discovery of E. multilocularis in British Columbia, representing the west
central European population, indicates a very recent introduction and
establishment of this taeniid in contemporary time by jump dispersal and
appears to be unrelated to deeper historical processes (Jenkins et al., 2012).
Arctic fox, however, may be most critical as a determinant of high-
latitude distributions. Consequently, there may be different expectations
for population structure in E. multilocularis associated with red fox in
contrast to Arctic fox. The latter would be predicted to show signatures
of extensive gene flow across the broad geographic range where arvico-
lines are present (Rausch, 1994). Complex historical interactions involving
temporal shifts or episodes of sympatry for foxes and arvicoline rodents
including species of Microtus, Myodes and Lemmus have determined the
distribution of the parasite in space and time. Voles may be the limiting
factor in determining local occurrence and transmission (e.g. Henttonen
et al., 2001), but definitive hosts with varying levels of vagility and dif-
ferential responses to glacial maxima would either mediate isolation (red
fox) or gene flow (Arctic fox).
Recurrent expansion in conjunction with high mobility may confound
recognition of the history for E. granulosus (genotypes G-8 and G-10)
(Lavikainen et al., 2003; Thompson et al., 2005) and the assemblage of
carnivores (primarily wolf) and cervids that perpetuate transmission in
northern environments. Genetic sampling has thus far been insufficient
to either document the geographic range or the host associations and
identity for Echinococcus circulating among wolves, caribou, moose and
related cervids or infer the relationship for populations across the Arctic
and extending to temperate latitudes in North America and Eurasia.
1.4.1.5. Diphyllobothrium spp

Among the approximately 50 recognised species of Diphyllobothrium,
relatively few are known to occur at high latitudes (Scholz et al., 2009).
Considering Alaska and the Canadian Arctic, six species (D. alascense,
D. dalliae, D. dendriticum, D. lanceolatum, D. latum and D. ursi) are likely
to circulate among terrestrial carnivores and all except D. alascense also
occur in people (Rausch et al., 1967; Rausch and Hilliard, 1970). Although
a detailed phylogeny for Diphyllobothrium has yet to be developed, it is
likely that most of these species had extended histories at high latitudes
during the Pleistocene. As a potentially zoonotic assemblage, diphyllo-
bothriids have been associated with people coincidental with the earli-
est incursions out of Eurasia into North America and in conjunction with
diets rich in both freshwater and anadromous fishes that serve as inter-
mediate and paratenic hosts (e.g. Rausch et al., 1967; Rausch and Hilliard,
1970; Scholz et al., 2009). Diphyllobothrium latum, however, appears to be
primarily a parasite of people and its historical occurrence at high lati-
tudes may reflect both late Pleistocene expansion across Beringia and later
anthropogenic introductions with Europeans establishing focal distribu-
tions in the eighteenth century (Rausch and Hilliard, 1970).
At northern latitudes, particular species of Diphyllobothrium in terres-
trial carnivores circulate in freshwater (D. latum, D. dalliae, D. dendriticum),
marine (D. alascense, D. lanceolatum) or freshwater/marine cycles (D. ursi).
Additional species, including D. pacificum, D. stemmacephalum, D. fayi, D.
hians and D. cordatum are characteristic of marine mammals (either pinni-
peds or cetaceans) and potentially may be available in terrestrial systems
through anadromous fishes or exploitation of marine fishes in estuarine
environments (Rausch and Adams, 2000; Rausch, 2005; Scholz et al., 2009;
Rausch et al., 2010). Diphyllobothrium and related diphyllobothriids (e.g.
Diplogonoporus, Pyramicocephalus) appear to have a long and complex his-
tory with arctoid carnivorans and cetaceans, in part involving Beringia
and the Arctic basin with connections through Bering Strait minimally
over the past 4–5 Myr (Hoberg and Adams, 2000). Resolution of this his-
tory and connections to the global fauna remains obscured by the absence
of comprehensive phylogenetic studies among this group of cestodes.
1.4.1.6. Other helminths among carnivorans

Other helminth taxa, including an assemblage of nematodes, are well rep-
resented among carnivorans in the circumpolar region, and it is apparent
that some components of these faunas have histories of expansion across
Beringia from Eurasia during the Pleistocene (e.g. Rausch et al., 1979).
Host distributions in most cases also suggest deep associations and early
diversification with feliforms and caniforms, and some level of host col-
onisation is also postulated where single species may be shared among
ecologically similar carnivores. Comprehensive and detailed phylogenetic
studies are lacking, however, and robust hypotheses for host association
and biogeography remain to be defined. Examples include the ascarids
Baylisascaris, with species distributed among mustelids, mephitids, ursids
and felids, or Toxascaris occurring among canids, ursids and felids. Among
the strongyles, species of Molineus (Molenioidea) also have Holarctic dis-
tributions and broad associations among multiple carnivoran groups.
Considering other strongyles, hookworms (Ancylostomatoidea) includ-
ing species of Uncinaria in ursid hosts have been explored to some degree in
the amphiberingian region (Rausch et al., 1979). Three species (U. rauschi,
Nearctic; U. yukonensis, Holarctic, and U. skrjabini, Palaearctic) are currently
recognised in brown bears and black bears (Wolfgang, 1956; Olsen, 1968).
It is postulated that U. yukonensis originated in eastern Eurasia, expanded
with U. arctos across Beringia in the late Pleistocene and secondarily colo-
nised U. americanus in North America during the Holocene (Rausch et al.,
1979). It is possible that U. rauschi represents an earlier event of geographic
colonisation by bears and hookworms into North America from Eurasia.
Uncinaria skrjabini may actually be a characteristic parasite in some muste-
lids and its occurrence in ursine hosts may be attributable to colonisation
(Kontrimavichus, 1969). It is apparent that species assemblages of para-
sites circulate among diverse arrays of carnivoran hosts as exemplified by
studies of faunal structure for parasites of black bears from North America
or circumpolar mustelids (e.g. Kontrimavichus, 1969; Pence et al., 1983;
Koehler et al., 2007).
1.4.2. Faunas associated with Lagomorpha

• The parasite groups: Cestoda – Cyclophyllidea, Anoplocephalidae
(Mosgovoiya, Schizorchis); Nematoda – Strongylida, Trichostrongylina
(Heligmosomoidea – Ohbayashinema; Molineoidea – Murielus, Graphi-
diella, Rauschia; Trichostrongyloidea – Obeliscoides); Metastrongylina
(Protostrongylus). Oxyuroidea, Heteroxynematidae (Cephaluris, Labios-
tomum). Taxonomy is consistent with Boev (1975); Durette-Desset et al.
(1994); Anderson (2001) and Chilton et al. (2006) (Table 1.5).
• The host groups: Lagomorpha – Ochotonidae (Ochotona spp.); Lepori-
dae (Lepus spp.)
• Taxonomy for lagomorphs consistent with Wilson and Reeder (2005).
Lagomorphs, Leporidae and Ochotonidae diversified initially in Eurasia
during the Oligocene and later attained Holarctic distributions estab-
lished across Beringia during the late Tertiary (Dawson, 1967); no species
in these groups have Holarctic ranges. A number of apparent sister groups
among the helminths (e.g. Anoplocephalidae – Schizorchis and Mosgovoiya;

Trichostrongylina – Murielus, Rauschia + Nematodiroides; Oxyuroidea –
Dermatoxys, Cephaluris and Labiostomum) indicate deep coevolutionary
associations for assemblages of parasites in Leporidae and Ochotonidae
(e.g. Gvozdev, et al., 1970; Quentin, 1975).
Pikas include 30 extant species, but only Ochotona collaris and O. princeps
occur in the Nearctic and represent initial expansion into North America
during the late Pliocene (Smith et al., 1990; Yu et al., 2000). Transcontinental
distributions for Trichostrongylina (Ohbayashinema, Murielus, Graphidiella),
Oxyuroidea (Labiostomum and Cephaluris) and Anoplocephalidae (Schizor-
chis) involving phylogenetically diverse and divergent species of Ochotona
are consistent with a deep history of association linking localities in the
Palaearctic and Nearctic over the late Tertiary and Pleistocene (Galbreath,
2009; Galbreath and Hoberg, 2012; Durette-Desset et al., 2010). The his-
tory of these parasite taxa is complex and intricate with most representing
strongly host-specific helminths limited to Ochotona (Gvozdev, 1962; See-
see, 1973). For example, Ohbayashinema appears associated with an early
event of host colonisation in Eurasia following the divergence of Lepori-
dae and Ochotonidae; these nematodes have affinities with Citellinema in
sciurids or Heligmosomoides in arvicolines (Durette-Desset et al., 2010). In
contrast, both Murielus and Schizorchis appear to have deeper coevolution-
ary histories with patterns of divergence linked to the common ancestor
for the Leporidae + Ochotonidae (Rausch, 1994; Hoberg 2005a).
The helminth fauna of pikas was initially assembled in Eurasia from
phylogenetically disparate sources over an extended time frame since
the mid Tertiary. Geographic expansion from Eurasia and colonisation
across Beringia and south into the Nearctic occurred under the influence
of episodic climate change and cyclical habitat modification during the
past 2Myr (Hoberg, 2005a; Galbreath, 2009). Refugial habitats in North
America were important in the maintenance of complex parasite assem-
blages and in the generation of considerable cryptic diversity across most
parasite groups (Galbreath, 2009; Galbreath and Hoberg, 2012).
Although the helminth fauna characteristic of pikas is relatively
diverse (e.g. Rausch, 1994; Hoberg, 2005a; Hoberg et al., 2009; Galbreath,
2009; Durette-Desset et al., 2010; Galbreath and Hoberg, 2012), few para-
site taxa are distributed at higher latitudes, particularly in the Nearctic.
Comparisons of the sister species O. collaris (Subarctic) and O. princeps
(Temperate) in western North America indicate the complete absence of
trichostrongyline nematodes at higher latitudes in the former host (Gal-
breath, 2009; Galbreath and Hoberg, 2012). Further, there are no unique
species of pinworms and only one endemic cestode at higher latitudes
such that the fauna mostly represents a subset of the parasite species that
are characteristic of the southern O. princeps. Following the initial estab-
lishment of pikas in North America, these small lagomorphs became
36
TABLE 1.5 Species diversity and biogeography for exemplar helminth parasites among Lagomorpha in the Arctic and Subarctic, exploring
assemblages influenced by episodic climate change and geographic expansion in the Pliocene and Quaternary. Species richness is reflected for
global diversity, distributions across the Holarctic and those that are endemic to either the Nearctic or the Palaearctic
Eucestoda/Anoplocephalidae
Schizorchis spp.c Ochotonidae Holarctic/disjunct (10+G/0H/5N/5P) (2, east GE, R
and west Beringia)
Mosgovoyia Leporidae Holarctic/disjunct (5G/2H/1N/2P) GE
Murielus spp. Ochotonidae Holarctic/disjunct (3G/0H/1N/2P) GE
(absent from Beringia)
Obeliscoides Leporidae Holarctic (3G/0H/1N/2P) GE
Graphidiella spp. Ochotonidae Holarctic/disjunct (4G/0H/1N/3P) GE
Ohbayashinema spp. Ochotonidae Holarctic/disjunct (6G/0H/2N/4P) GE, R
Rauschia spp. Leporidae Holarctic/disjunct (5G/0H/2N/3P) GE
Trichostrongylus spp.d Bovidae/Cervidae, Holarctic (30+G/0H/7N/23P) GE, HC
Leporidae, Rodentia
Nematoda/Metastrongylina
Protostrongylus spp. Leporidae Holarctic (6G/1H/1N/4P) GE
Nematoda/Oxyuroideac
Cephaluris spp. Ochotonidae Holarctic – disjunct (10+G/1H/3N/6P) GE, R
Labiostomum (Eugenuris) Ochotonidae Holarctic – disjunct (10+G/0H/4N/6P) GE, R
Labiostomum (Labiostomum) Ochotonidae Holarctic – disjunct (7+G/0H/3N/4P) GE, R
c Diversity includes undescribed species (Hoberg et al., 2009; Galbreath and Hoberg, 2012).
d Nearctic Trichostrongylus are primarily in rodent or leporid definitive hosts.

37
extinct in Beringia but were continuous in habitats south of the Lauren-

tide. Subsequent expansion from southern refugia (leading to the origin
of O. collaris) along with local extinction for the trichostrongylines are
implicated as major influences on patterns of current diversity in the Sub-
arctic (Galbreath, 2009; Galbreath and Hoberg, 2012). Thus, parasites tell
us a story that is counter to the usual narrative for Beringian biogeogra-
phy, indicating a greater role for dispersal from temperate North America
into Beringia prior to the terminal Wisconsinan as a driver for diversity in
northern systems.
Considering Leporidae, four species of hare occur at high latitudes
across the Holarctic and include Lepus timidus (snow hare – Palaearctic),
Lepus othus (Alaska hare – western Alaska), L. arcticus (Arctic hare, north-
eastern Arctic Canada and Greenland) and L. americanus (snowshoe hare
– widespread in Subarctic to Arctic North America) (MacDonald and
Cook, 2009; Waltari and Cook, 2005). An Arctic clade of leporids includes
L. townsendii (white-tailed jackrabbit of western temperate North Amer-
ica) with L. othus, L. arcticus and L. timidus (Halanych et al., 1999). Lepus
americanus is sister of a western American clade of Lepus (Halanych et al.,
1999) and is infected with Protostrongylus boughtoni, Obeliscoides cuniculi
and species of Rauschia probably throughout the geographic range occu-
pied in North America. None of these parasites is known in the Alaska
hare or Arctic hare that are parapatric with L. americanus in some parts of
its range (MacDonald and Cook, 2009). Another lungworm, Protostrongy-
lus cf. pulmonalis, occurs in some populations of Alaska hare and also in
Lepus townsendi (white-tailed jackrabbit) at temperate latitudes of west-
ern North America but is absent in L. americanus (Boev, 1975; E.P. Hoberg
and E. Waltari, unpublished data). Protostrongylus pulmonalis has a broad
host and geographic range in the Palaearctic but, in North America, is
represented by disjunct and putatively discrete populations north and
south of the former Laurentide glaciation suggesting a complex pattern
of refugial isolation and parasite extinction (E.P. Hoberg and E. Waltari,
unpublished data).
Obeliscoides, Protostrongylus, and Rauschia appear to have ancestral
ranges in the Palaearctic including L. timidus and other Eurasian lepo-
rids. Current host and geographic associations suggest multiple events
of expansion between Eurasia and North America, although direction-
ality remains equivocal (Waltari and Cook, 2005); secondarily, isola-
tion occurred north and south of continental glaciers in the Nearctic
for this fauna in leporids. Absence of lungworms and other strongyles
in L. arcticus appears consistent with loss of parasites in a high Arctic
refugium for hosts during the terminal glacial stages of the Pleistocene
(Waltari and Cook, 2005). Similar to the pattern of parasite diver-
sity in O. collaris, the reduced fauna may reflect limitations imposed
by extreme environments and/or demographic and founder effects
involving small initial host populations and geographic colonisation

on the periphery of northern ranges.
1.4.3. Faunas associated with Rodentia

• The parasite groups: Cestoda – Cyclophyllidea, Anoplocephalidae
(Anoplocephaloides, Diandrya, Macrocephaloides, Marmotocephala (=Sciuro-
taenia), Paranoplocephala, Paranoplocephaloides, Parasciurotaenia); Hyme-
nolepididae (Arostrilepis); Nematoda – Strongylida, Trichostrongylina,
Heligmosomoidea – (Citellinema, Heligmosomoides, Heligmosomum);
Oxyuroidea (Citellina). Taxonomy is consistent with Durette-Desset
et al. (1994), Anderson (2001), Chilton et al. (2006) and Haukisalmi
(2009) (Table 1.6).
• The host groups: Rodentia – Cricetidae, Arvicolinae (Dicrostonyx, Lemmus,
Myodes, Microtus, Phenacomys, Synaptomys), and Neotominae (Pero-
myscus); Sciuridae, Sciurini (Tamiasciurus), and Marmotini (Marmota,
Spermophilus). Taxonomy is consistent with Wilson and Reeder (2005).
Rodents are the most diverse group of mammals and occur globally in a
variety of ecosystems, although many genera and species exhibit specific
habitat associations. As a consequence, these small mammals are critical
indicators of environmental structure in evolutionary and ecological time
(e.g. Hoffmann, 1981; Repenning, 2001). Although the earliest rodents
appear in the Palaeocene (65–55Ma) of North America, the structure of
contemporary faunas has largely been determined since the mid Tertiary
and has been strongly influenced by expansion events from Eurasia
into the Nearctic that continued through the Quaternary. The primary
Holarctic and North American taxa are represented by Cricetidae (130
genera and 681 species notably including Arvicolinae and Neotominae)
and Sciuridae (51 genera and 278 species notably including Sciurinae
and Marmotini) (Musser and Carleton, 2005; Thorington and Hoffmann,
2005). In our discussion, we focus on a limited number of exemplars
among the rodents where both host and parasite biogeographic history
has been examined.
Rodent helminth faunas have been explored in considerable detail
across higher latitudes of the Holarctic (e.g. Rausch, 1952, 1957; Durette-
Desset, 1968, 1971; Durette-Desset et al., 1972; Rausch and Rausch, 1973;
Ryzhikov et al., 1978, 1979). Faunas exhibit complex patterns of geographic
and host colonisation and regional extinction with limited evidence of
diversification through extensive cospeciation (Haukisalmi et al., 2008).
Holarctic distributions are linked to dispersal events across Beringia from
the Pliocene into the Quaternary (Rausch, 1994).
Cricetid rodents have a long history of connections between Eurasia and
the Nearctic. Among these, the Arvicolinae and their helminths are among
the most informative exemplars for revealing historical patterns and
40
TABLE 1.6 Species diversity and biogeography for exemplar helminth parasites among Rodentia in the Arctic and Subarctic, exploring assem-
blages influenced by episodic climate change and geographic expansion in the Pliocene and Quaternary. Species richness is reflected for global

diversity, distributions across the Holarctic and those that are endemic to either the Nearctic or the Palaearctic
Eucestoda/Hymenolepididae
Arostrilepis spp.c Arvicolinae Holarctic/Beringian (13G/2H/4N/7P) GE, HC, R
(+Geomyidae) (5 amphiberingian)
Eucestoda/Anoplocephalidae
Anoplocephaloides spp.c Arvicolinae Holarctic/Beringian (10G/2H/3N/3P) GE, HC, R
(3 amphiberingian)
Diandrya Sciurinae Nearctic/Beringian (1N) GE, HC
Paranoplocephala spp. Arvicolinae (+Sciurinae) Holarctic/Beringian (35G/8H/13N/14P) GE, HC, R
(15 amphiberingian)
Paranoplocephaloides spp. Arvicolinae Holarctic (2G/0H/1N/1P) GE
Parasciurotaenia Sciurinae Palaearctic (1G/0H/0N/1P) HC
Marmotocephala spp. Sciurinae Holarctic/Beringian (2G/1H/0N/1P) HC
(1 amphiberingian)
Microcephaloides spp.c Arvicolinae Holarctic/Beringian (9G/0H/6N/3P) GE, HC, R
(+Geomyidae)
Eucestoda/Catenotaeniidae
Catenotaenia spp. Muridae, Cricetidae, Holarctic/Beringian (22+G/2H?/5N12P) GE, HC
Arvicolinae, Mamotinae
Citellinema spp. Sciuridae Holarctic (10+G/0H/5N/5P) GE
Heligmosomoides spp.d Arvicolinae Holarctic/Beringian (36+G/1H/17N/19P) GE, HC, R
(other Cricetidae
Geomyidae)
Trichostrongylus spp.e Bovidae/Cervidae Lepori- Holarctic (30+G/0H/7N/23P) GE, HC
dae, Rodentia
Nematoda/Oxyuroidea
Citellina spp. Sciuridae Holarctic (11+G/0H/2N/9P) GE, HC
c Species richness for Arostrilepis, Anoplocephaloides and Microcephaloides includes undescribed diversity in each genus.
d Heligmosomoides includes nominal species and subspecies (see Asakawa, 1988).
e Nearctic Trichostrongylus are primarily in rodent or leporid definitive hosts.

41
processes of dispersal and diversification. Over the Pliocene and Pleis-

tocene, 16 arvicoline genera encompassing 5 distinct faunas have been
involved in expansion, primarily asymmetrical, from Eurasia into North
America (Conroy and Cook, 1999; Repenning, 2001). Episodes for expan-
sion and isolation correlate with cyclical periods of glaciations; the first
North American glacial episode occurred around 2.65Ma (Pliocene),
and the first of the classical sequences (Nebraskan) is calibrated near
650–850Ka. Multiple events for geocolonisation from Eurasia are brack-
eted by these time frames and later into the Pleistocene: (1) bog lemmings,
Synaptomys (=Mictomys) at 2.65Ma; (2) Phenacomys at 2.5Ma; (3) Microtus at
2.5Ma in Beringia (1.7Ma south of Laurentide) and later at 300Ka; (4) the
ancestor for Lemmus is known about 2.5Ma in west and east Beringia; Lem-
mus and Dicrostonyx are known since about 1Ma in Beringia from Eurasia,
and for these lemmings, contemporary ranges do not extend to regions
south of the former Cordilleran and Laurentide glaciations, although
southern refugial distributions are postulated (Guthrie, 1968b; Guthrie
and Matthews, 1971; Repenning, 2001; Fedorov and Goropahsnaya, 1999;
Fedorov et al., 1999, 2003; Fedorov and Stenseth, 2002), and (5) Red-backed
voles (Myodes) are recognised near 850Ka in Beringia (Repenning, 2001).
It is evident that distinct faunas were partitioned in space and time over
the past 5Ma, influenced by dispersal events (inter- and intracontinental)
strongly correlated with specific climatological episodes (Conroy and
Cook, 1999, 2000; Repenning, 2001).
A complex biogeographic history also coincided with a rapid radiation
for voles and lemmings across circumpolar habitats (Conroy and Cook,
1999, 2000; Repenning, 2001; Cook et al., 2004; Galbreath and Cook, 2004).
Most palaeolineages retain extant descendants, although relatively few
genera and species are now found at Subarctic to Arctic latitudes (e.g. in
the contemporary fauna, 53% are strictly temperate, 33% temperate to
Subarctic and 13% Arctic) (Repenning, 2001). These observations have
suggested that dispersal events for rodents on intercontinental scales coin-
cided with temperate climates (or habitats) in Beringia. The corollary is
that faunal structure evident in contemporary systems resulted from an
exchange of temperate faunas that are now absent in Beringia but with
distributions now extending into more southern latitudes in both Eurasia
and North America (Repenning, 2001). Although multiple genera are Hol-
arctic in distribution, most of these taxa have disjunct ranges with large
gaps at high latitudes. Only three species of arvicolines, Myodes rutilus,
Microtus oeconomus and Lemmus sibiricus, have continuous distributions
that span Beringia (Rausch, 1994). These distributions and their interpreta-
tion represent part of the apparent habitat paradox (i.e. at what point were
temperate habitats continuous across the land bridge?) for Beringia during
glacial stages. Habitat structure is critical either in impeding or in facilitat-
ing intercontinental expansion and may have significance for the question
of whether greater Beringia was primarily a continuous steppe at higher

latitudes or a complex mosaic of xeric and mesic microhabitats (Guthrie,
2001; Elias and Crocker, 2008). It is apparent that these heterogeneous
environments linking Eurasia and North America were intermittently
of high productivity and capable of supporting a diverse assemblage of
mammals (Guthrie, 1982, 1984, 1990, 2001; Repenning, 2001).
Phylogeographic breaks observed across the Kolyma uplands near the
western boundary of Beringia for multiple arvicoline host taxa (Microtus
oeconomus, Lemmus spp., Dicrostonyx spp.) possibly correspond to his-
torical barriers due to past (intermittent) glaciations reinforced by habitat
structure during interglacials (e.g. xeric environments as ecological barri-
ers) (Galbreath and Cook, 2004). These relationships point to both glacial
(ice masses) and interglacial (habitat refugia) drivers that have influenced
isolation and diversification for arvicoline hosts (Conroy and Cook, 2000;
Repenning, 2001). Thus, among rodents, apparently it is expansions of
Subarctic to temperate habitats (not arctic habitat) that has facilitated the
majority of intercontinental faunal exchange. This association seems also
to apply to large ungulates associated with Beringian and periglacial habi-
tats of the Pleistocene (Guthrie, 2001).
In contrast to cricetids, the sciurid rodents have a substantially deeper
history across the Northern Hemisphere with apparent origins in the
Nearctic prior to expansion and radiation in Eurasia (Kurtén and Ander-
son, 1980). The divergence of ground squirrels (Spermophilus with 38 spe-
cies total/25 North American/1 Holarctic) and marmots (Marmota with 14
species/6 North American) is estimated near 9–10Ma and a complex his-
tory across Beringia is evident (Steppan et al., 1999; Galbreath et al., 2011).
Overall the structure of contemporary diversity among rodents repre-
sents a process of dynamic faunal assembly over time, reflecting the inter-
play between persistence and turnover (Repenning, 2001). Distributions
for various taxa resulted from complex interactions between climatic oscil-
lations (e.g. glacial/interglacial and stadial/interstadial cycles that influ-
enced habitat, and pathways for expansion) and life history parameters
(e.g. vagility and persistence in evolutionary and ecological time). Under
this model, tundra-adapted (Arctic) faunas that have persisted within
Beringia throughout the Quaternary are represented by the lemmings,
Dicrostonyx and Lemmus (Fedorov and Goropahsnaya, 1999; Fedorov et al.,
1999, 2003). These contrast with transient faunas moving through Beringia
as they track temporal shifts in suitable habitat. Such movements have
resulted in Boreal/Subarctic disjunct distributions exemplified by spe-
cies of Myodes and Microtus (Repenning, 2001). This mosaic of persistent
and transient rodent assemblages has in turn been an important driver for
parasite faunal structure.
Cestode faunas in northern rodents are dominated by two fami-
lies, Anoplocephalidae and Hymenolepididae (Taeniidae that occur as
etacestodes are excluded here). Collectively these taxa represent the most
m
diverse helminth groups among any of the terrestrial mammals at high
latitudes with distributions extending south into the Nearctic and Eurasia.
This may reflect host group diversity for cricetids (Arvicolinae with 28 gen-
era and 151 species) and sciurids (Marmotini with 6 genera and 92 species),
although a disproportionate representation of cestodes is apparent at higher
latitudes particularly among arvicolines. Histories for these respective ces-
tode groups among arvicolines are postulated to represent independent
radiations following single basal colonisation events from Lagomorpha for
anoplocephalines and from Soricomorpha for the hymenolepidid Arostril-
epis in the Palaearctic (Wickström et al., 2005; Haukisalmi et al., 2010).
Among the anoplocephalines, diversity is manifested by a relatively
large number of related genera (7) and species (estimated + 60) partitioned
primarily among Holarctic cricetids (Arvicolinae/voles and lemmings)
and sciurids (Marmotini/marmots and ground squirrels) and some
Nearctic geomyids (pocket gophers) (Gvozdev et al., 2004; Haukisalmi
et al., 2002, 2004; Wickström et al., 2005; Haukisalmi et al., 2006, 2008,
2009; Haukisalmi, 2009). Further, in this assemblage multiple cryptic spe-
cies have been demonstrated within A. dentata (4 spp.), Microcephaloides
variabilis (6), Paranoplocephala omphalodes (4) and possibly P. macrocephala
(Haukisalmi et al., 2004, 2008, 2009). Species of Paranoplocephala are pri-
marily parasites of Microtus voles, with relatively fewer species occur-
ring among lemmings or the red-backed voles (Wickström et al., 2003;
Haukisalmi et al., 2006).
Phylogenetic relationships among species of Paranoplocephala, Anoplo-
cephaloides, Microcephaloides and other genera remain enigmatic, but avail-
able evidence suggests a period of explosive radiation leading to multiple
parasite lineages coinciding with events for host diversification extend-
ing into the Pliocene (Conroy and Cook, 1999, 2000; Cook et al., 2005;
Haukisalmi et al., 2006). A single colonisation event is evident among
early arvicolines, but arvicolines have served as a source for colonisation
and subsequent diversification of cestodes among other rodent groups
(Haukisalmi et al., 2004; Haukisalmi, 2009). In the Nearctic, these have
included parasites of geomyids (Microcephaloides and Paranoplocephala),
marmots (Diandrya and Marmotocephala) and other sciurids (some species
of Paranoplocephala). Interestingly, Diandrya composita resulted from colo-
nisation of Nearctic marmots from arvicolines, probably Dicrostonyx lem-
mings during the Pleistocene (Wickström et al., 2005). The cestode faunas
of Eurasian and Nearctic marmots are distinct with no genera or species
that are shared (Rausch, 1994).
Rausch (1994) reviewed the status of helminth faunas of large rodents
in the Beringian region and described a history of expansion between
the Palaearctic and Nearctic. In contrast to arvicolines, helminth diver-
sity is minimal in sciurids and few cestodes are considered typical or are
widespread (Ryzhikov et al., 1978, 1979). Among cestodes, these include

the anoplocephalids Parasciurotaenia, and Ctenotaenia and the catenotaeniid
Catenotaenia primarily in Eurasia, Marmotocephala with a limited Eurasian–
Beringian range and Diandrya in the Nearctic. Nematode faunas are
dominated by spirurids such as Rictularia and Mastophorus and oxyurids
represented by Citellina and Syphacia. The historical biogeography of these
groups has not been examined in detail. Parasites may be particularly rare
among arboreal sciurids in contrast to marmots and ground squirrels.
Pervasive patterns of host and geographic colonisation and rapid
generic- and species-level diversification characterise the history of the
arvicoline clade of anoplocephaline cestodes (Wickström et al., 2001, 2003;
Haukisalmi et al., 2004; Wickström et al., 2005). These shifts were played
out against climatic oscillations and episodes of environmental perturba-
tion during the late Pliocene and Pleistocene, factors considered as criti-
cal drivers for diversification in complex host–parasite assemblages (e.g.
Hoberg and Brooks, 2008, 2010).
In contrast, hymenolepidids are represented by the genus Arostrilepis
where there are now 13+ recognised species-level lineages within what had
historically been recognised as A. horrida, a single widespread and morpho-
logically variable species (Hoberg et al., 2003; Cook et al., 2005; Makarikov,
2008; Makarikov and Kontrimavichus, 2011; Makarikov et al., 2011, in press;
K.E. Galbreath and E.P. Hoberg, unpublished data). Among these, seven are
limited to the Palaearctic, two are Beringian/Holarctic and four are endemic
to the Nearctic. The limits for diversity and species richness for Arostrilepis
remain to be clearly defined and, for example, may include additional spe-
cies in arvicolines (Myodes andersoni and M. smithii) from Japan (Asakawa
et al., 2002). These distributions and apparent host associations reflect a
deep history with arvicolines extending into the Pliocene of Eurasia. Such
is indicated by conspecificity of Arostrilepis in Lemmus and Synaptomys, the
occurrence of an endemic species in Myodes gapperi and multiple species par-
titioned between Microtus spp. and Myodes spp. in the Nearctic and eastern
Palaearctic (Cook et al., 2005); multiple expansion events from the Palaearc-
tic are evident for both hosts and parasites. For example, an initial colonisa-
tion of North America is indicated for the precursor of M. gapperi in the late
Pliocene/early Pleistocene, whereas the distribution of the Holarctic M. ruti-
lus was established during Wisconsinan time of the late Pleistocene (Cook
et al., 2004). Further, three species of tapeworms, respectively, in Geomyidae
(pocket gophers, Thomomys), Neotominae (deer mice, Peromyscus) and Sciu-
ridae (Tamiasciurus) indicate a role for host colonisation from arvicolines in
diversification of Arostrilepis in North America (Makarikov et al., in press).
Cestode faunas among arvicolines have responded to micro-refugial
events (Anoplocephaloides spp., Microcephaloides spp. and Paranoplocephala
spp.) and larger scale patterns of regional isolation (Arostrilepis spp.).
Striking differences in faunal diversity (generic and species richness)
may be attributable to life history, patterns of abundance and dispersion

(homogeneous vs. discontinuous or patchy distributions geographically
and within hosts at specific localities) and effective population size
(Hoberg et al., 2003; Cook et al., 2005). This contrast in diversity is notable,
however, given the apparent equivalent age of association for these dispa-
rate cestode groups in rodents.
Several explanations may be explored for divergent patterns of diver-
sity among these tapeworm assemblages. For example, are there differences
in historical centres and the timing of diversification for anoplocephalines
and Arostrilepis? (1) Did Arostrilepis initially radiate in central Eurasia and
secondarily expand across Beringia into the Nearctic? (2) Did diversifi-
cation for Anoplocephaloides, Paranoplocephala and related genera initially
occur through regional isolation and secondarily by local geographic iso-
lation on near landscape scales? (3) How have faunas been influenced by
single or multiple events for expansion, establishment and isolation at
intercontinental, intracontinental and landscape scales? (4) Sciurids are
older but helminth diversity is generally lower than that seen in arvico-
lines; does this pattern reflect the role of timing for host colonisation in fau-
nal assembly (e.g. late in the evolution of marmots or ground squirrels)?
Life history also contributes to differences in cestode diversity. Species
of anoplocephalines are not regionally widespread; although occasionally
locally abundant, distributions are generally heterogeneous and patch-
ily distributed with few individual worms within hosts and few infected
voles (or lemmings) at local scales (Haukisalmi et al., 2008). These fac-
tors suggest an interaction between small effective population size (and
founder events) for parasites in the context of patterns of local geographic
isolation. The patchy and unpredictable distributions for some anoplo-
cephalines on fine spatial scales may increase the potential for extinction
events over evolutionary time; for example, there are no species of Micro-
cephaloides known across the expanse of Siberia from the Ural Mountains
to the Russian Far East (V. Haukisalmi, Personal Communication). In
contrast, species of Arostrilepis generally are regionally widespread (with
some exceptions) and homogenous in distribution with often large num-
bers of worms within hosts and many infected individuals and species of
arvicolines at local scales. For Arostrilepis, this pattern would suggest sub-
stantially larger effective populations that would be less strongly influ-
enced by fine scale isolation and partitioning of habitats (Hoberg et al.,
2003). Although Arostrilepis is regionally abundant, species have yet to be
discovered in the Fennoscandian sector of the western Palaearctic.
Considering heligmosome nematodes, the genus Heligmosomoides is
primarily associated with the arvicolines (also occurring in Muridae, Sciu-
ridae and other Cricetidae) and includes about 36 species, of which 14 or
15 occur in the Nearctic; a single species, H. hudsoni is Holarctic in distri-
bution (Durrette-Desset, 1968, 1971; Rausch and Rausch, 1973; Asakawa,
1988). Origin and diversification of this fauna is related to independent

events of biotic expansion from the Palaearctic since the early Pleistocene
and a history of cospeciation with voles and lemmings (Durette-Desset,
1968; Durette-Desset et al., 1972; Asakawa, 1988). Distributions of spe-
cies among other cricetids are attributed to a history of independent host
switches and diversification, primarily in the Nearctic (Durette-Desset
and Kinsella, 2007).
Aside from the heligmosome nematodes among arvicolines (e.g.
Durette-Desset et al., 1972; Ryzhikov et al., 1979), cestodes are the only
apparently high diversity groups of metazoan parasites occurring at high
latitudes. Haukisalmi et al. (2006) summarised the structure of the arvi-
coline cestode fauna in Beringia and recognised four primary sources or
distributions for species of Paranoplocephala: (1) Holarctic species, (2) wide-
spread Nearctic species, (3) east Beringian endemics and (4) a single species
with a Palaearctic western Beringian distribution. Among the estimated 35
species of Paranoplocephala, the eastern Beringian fauna (13 species) was an
admixture of Nearctic and Holarctic species. A greater number of endemics
occur in the western Eurasian fauna, which appears to parallel diversity
observed for tapeworms in Leporidae, although these latter assemblages
are older than those in arvicolines (Wickström et al., 2005; Haukisalmi et al.,
2006). These distributions are also similar to host and geographic associa-
tions demonstrated for the heligmosomes and suggest the generality of
the drivers and biogeographic relationships linked to arvicolines. There is
evidence of cospeciation (often associated with colonisation as a precur-
sor) for species in Lemmus, Dicrostonyx, Microtus and Myodes (Wickström
et al., 2003; Haukisalmi et al., 2006). Additionally, colonisation of emergent
arvicoline lineages appears as a primary mode of diversification among
species of Anoplocephaloides (Haukisalmi et al., 2009).
Patterns evident among either anoplocephalids or hymenolepidids
indicate (1) multiple historical events of intercontinental geographic
expansion spread over extended time frames spanning the late Pliocene
and Pleistocene, (2) episodic expansion and contraction of ranges during
glacial and stadial cycles and (3) recurrent fragmentation of host–parasite
assemblages where small effective population size for isolated parasite
populations would constitute drivers for divergence and allopatric specia-
tion (Haukisalmi and Henttonen, 2001; Haukisalmi et al., 2001; Wickström
et al., 2001, 2003; Haukisalmi et al., 2006, 2009). Associations reflect some
instances of cospeciation, although host colonisation and subsequent par-
asite speciation may have occurred as a consequence of isolation of sym-
patric host populations in refugial zones of varying extent and duration.
The temporal faunal mosaic with overlapping elements established across
Beringia over extended time frames indicates the potential for complex
assemblages of hosts and parasites developed through zones of primary
and secondary contact (Hoberg and Brooks, 2008, 2010).
1.4.4. Faunas associated with Artiodactyla

• The parasite groups: Nematoda – Strongylida, Trichostrongylina
(Molineoidea – Nematodirinae; Trichostrongyloidea – Ostertagiinae);
Metastrongylina (Dictyocaulidae, Protostrongylidae); Spirurida
(Filarioidea). Taxonomy is consistent with Durette-Desset et al. (1994),
Anderson (2001) and Chilton et al. (2006) (Table 1.7).
• The host groups: Artiodactyla – Cervidae (Capreolinae – Alces, Odocoi-
leus, Rangifer; Cervinae – Cervus); Bovidae (Antilopinae – Saiga; Bovi-
nae – Bison; Caprinae – Oreamnos, Ovibos, Ovis). Taxonomy consistent
with Wilson and Reeder (2005) and Hernández Fernández and Vrba
(2005).
Although characterised by relatively low diversity, some pecoran rumi-
nants (for example, caribou and reindeer) and their parasites are promi-
nent members of high-latitude communities across the circumpolar region
(e.g. Halvorsen, 1986; Hoberg et al., 1995, 1999; Halvorsen and Bye, 1999;
Irvine et al., 2000; Hoberg et al., 2001; Hoberg, 2005a; Kutz et al., 2012).
Diversification among the ruminants has been strongly influenced by epi-
sodes of climatological variation and habitat perturbation extending from
the Oligocene to middle Pliocene (Hernández Fernández and Vrba, 2005).
Distributions for those species now occurring at high latitudes were deter-
mined predominantly during the Pliocene and Pleistocene coincidental
with cycles of glaciation and a series of independent expansion events
from Eurasia into North America during the Miocene, Pliocene and Pleis-
tocene (e.g. Guthrie, 1968a; Guthrie and Matthews, 1971; Kurtén and
Anderson, 1980; Guthrie, 1982; Webb, 2000). Patterns of geographic colo-
nisation for ungulate assemblages indicate differential and independent
events during successive glacial stages in the Pleistocene and account for
most extant diversity (excluding Antilocapridae and Camelidae) (Hernán-
dez Fernández and Vrba, 2005). Members of Cervidae and Caprinae are
dominant in the North American fauna.
Across northern habitats of the Nearctic and Palaearctic in the late Ter-
tiary and Pleistocene, a widely distributed assemblage of ungulates was
characterised by greater diversity and more extensive sympatry relative
to faunas in the Holocene (Guthrie, 1982; Vereschagin and Baryshnikov,
1982; Guthrie, 1984, 2006). At maximum levels of diversity near the ter-
mination of the Pleistocene, this assemblage included bovids (Bison spp.,
Bos, Saiga, species of Ovis and Ovibos), cervids (Cervus, Rangifer and Alces),
antilocaprids and camelids (Kurtén, 1968; Kurtén and Anderson, 1980).
More extensive sympatry and higher diversity in a regime of environ-
mental perturbation are consistent with drivers for host colonisation by
parasites (e.g. Hoberg and Brooks, 2008; Hoberg, 2010). In contrast, near
the termination of the ultimate glacial cycle, habitat disruption resulted in
range restriction, limited sympatry and extinction (Guthrie, 1984).
TABLE 1.7 Species diversity and biogeography for exemplar helminth parasites among
ungulates in the Arctic and Subarctic, exploring assemblages influenced by episodic
climate change and geographic expansion in the Pliocene and Quaternary. Species
richness is reflected for global diversity, distributions across the Holarctic and those
that are endemic to either the Nearctic or the Palaearctic
Marshallagia Bovidae/ Holarctic (12+G/1H/1N/10P) GE, HC, R
spp. Cervidae
Orloffia spp. Bovidae/ Holarctic (3+G/0H/1N/2P) GE
Cervidae
Ostertagia Bovidae/ Holarctic (12+G/1H/1N/10P) GE
spp. Cervidae
Teladorsagia Bovidae/ Holarctic (3+G/1H/0N/2P) GE, R
spp. Cervidae
Trichostron- Bovidae/ Holarctic (30+G/0H/7N/23P) GE, HC
gylus spp.c Cervidae
Leporidae,
Rodentia
Nematodirus Bovidae/ Holarctic (50+G/7H/7N/26P) GE, HC
spp. Cervidae
Nematodirella Bovidae/ Holarctic (6G/3H/1N/2P) GE, HC
spp. Cervidae
Nematoda/Metastrongylina
Dictyocaulus Bovidae/ Holarctic (7G/1H/0N/6P) GE
Cervidae
Protostrongy- Caprinae Holarctic (23G/0H/3N/20P) GE
lus spp.
Parela- Cervidae Nearctic (3G/0H/3N/0P) GE, HC, R
phostrongy- (Caprinae) (2 eastern Beringia)
lus spp.
Varestrongy- Cervidae Holarctic (9G/0H/2N/7P) GE, HC
lus spp. (Caprinae)
Nematoda/Filarioidead
Onchocerca Cervidae Holarctic (17+G/0H/1N/16P) GE
spp.
Rumenfilaria Cervidae Holarctic (1H) GE
Setaria spp. Bovidae, Holarctic (47+G/0H/3N/44P) GE, HC
Cervidae
c Nearctic Trichostrongylus are primarily in rodent or leporid definitive hosts.
d Filarioid diversity also includes species distributed outside of the Palaearctic region in the Old World.
In the Nearctic, the earliest cervids are recognised in the fossil record
about 5Ma (Webb, 2000) although divergence and diversification among
Cervinae and Capreolinae had ensued in the early Miocene near 23Ma
(Hernández Fernández and Vrba, 2005). Early diversification within
Odocoileini and Rangiferini also may have occurred in the Palaearctic.
Odocoileini, Rangiferini, Cervini and Alceini have had independent tra-
jectories in North America, representing successive waves of expansion
and establishment (Webb, 2000).
Reindeer (Eurasia) and caribou (North America) are the most promi-
nent of the high-latitude cervids. Rangifer represents a Beringian endemic
over the past 2 Myr that initially diversified in this region with second-
ary isolation north and south of the continental glaciers in the Nearc-
tic (Guthrie and Matthews, 1971; Flagstad and Røed, 2003; Cronin et al.,
2005; McDevitt, et al., 2009). During the late Pleistocene, a continuous
population occurred across Beringia and Eurasia. Additionally, one
or more discrete refugial populations existed south of the Laurentide
in North America. Isolation resulted in barren-ground ecotypes in the
north and woodland forms in the south with secondary contact occur-
ring along ecotones through expansion in postglacial time (Flagstad and
Røed, 2003). During the Wisconsinan, southern caribou populations were
in sympatry with Odocoileus and other ruminants. Notably, reindeer and
caribou are highly vagile, migratory and have the capacity to disperse
over large distances. In contrast, moose (or elk, Alces) was widespread
in northern Eurasia from the middle to late Pleistocene (Kurtén, 1968;
Kurtén and Anderson, 1980) but arrived in the Nearctic only about 15Ka
and did not attain a broad range in North America until the Holocene
(Guthrie, 1968a; Kurtén and Anderson, 1980; Hundertmark et al., 2002;
Lister, 2004). Historically, moose occurred at low densities and were the
least common ungulate within the Pleistocene assemblage of Beringia
(Guthrie, 1968a).
Diversification within Caprinae (containing Caprini and Rupicaprini)
extends to 14Ma in Eurasia (Hernández Fernández and Vrba, 2005). Cap-
rini (Ovis spp.) and Rupicaprini (Oreamnos) are not known in the Nearc-
tic until Nebraskan to Kansan time about 600–300Ka. Pachycerine sheep
initially became established in North America at this time, followed by
expansion to the south tracking deglaciation during the Yarmouth inter-
stadial about 300–200Ka (Kurtén and Anderson, 1980). Ovis nivicola in
Siberia and Ovis canadensis + O. dalli resulted from this sequential history
of expansion and isolation. Populations of bighorn and Dall’s sheep have
not apparently been in contact since the mid-Pleistocene about 250Ka
(Loehr et al., 2006). Populations of O. canadensis in the southern Rocky
Mountains assumed their current range with northward dispersal into the
western Cordillera starting near 15Ka (Geist, 1985). Dall’s sheep are recog-
nised in Beringia initially in the Sangamon and survived the ultimate
Pleistocene glaciation in this region and in isolated refugial zones situated

between the Laurentide and Cordilleran ice masses in British Columbia
and the Mackenzie Mountains (Worley et al., 2004; Loehr et al., 2006). Con-
tact apparently occurred between populations of O. canadensis and O. dalli
in the British Columbian refugium, although the former did not survive
the terminal Pleistocene in the Subarctic (Loehr et al., 2006). This complex
history has implications for helminth faunas distributed in wild sheep and
mountain goats extending into the Subarctic and Arctic (e.g. Hoberg et al.,
1999; Hoberg, 2005a).
Mountain goats, Oreamnos americanus, have a biogeographic history
that parallels that of Ovis spp. in North America with discrete northern
and southern subspecies and evidence of isolation in a northern refugium
in British Columbia (Harington, 1971; Shafer et al., 2011). In contrast, mus-
koxen, Ovibos and Symbos, expanded into Beringia during Kansan time
(900–700Ka) and occurred in periglacial habitats south of the Laurentide
and in Beringia during the penultimate glacial stages; Ovibos moschatus
survived the Pleistocene across the Holarctic, but in the Holocene became
extinct in the Palaearctic, and were widely extirpated in Alaska and Can-
ada during the nineteenth century. Muskoxen expanded from the central
Canadian Arctic into Greenland only in the mid Holocene about 4.5Ka
(contrasting with caribou that were present during the last interglacial
stage) (Campos et al., 2010). Other bovids that were transiently present
in northern latitudes of the Pleistocene included Saiga tatarica and species
of Bison and Bos, the sole representatives, respectively, of the Antilopinae
and Bovinae (Kurtén and Anderson, 1980; Harington, 1990; Harington
and Cinq-Mars, 1995).
The northern nematode fauna in ungulates has its origins in Eurasia.
Greatest diversity of nematode groups in central Eurasia indicates early
radiations, already associated with development of distinct faunas includ-
ing representatives of Strongylina (Strongyloidea), Trichostrongylina
(Nematodirinae – Nematodirus and Nematodirella, Ostertagiinae – Marshallagia,
Teladorsagia, Ostertagia, Orloffia) and Metastrongylina (Dictyocaulidae –
Dictyocaulus; Protostrongylidae – Protostrongylus, Umingmakstrongy-
lus, Varestrongylus and Parelaphostrongylus) (Boev, 1975; Hoberg, 2005a).
Expansion into the Nearctic occurred as a series of independent events at
intercontinental scales with distributions secondarily influenced by epi-
sodes of intracontinental isolation in the late Tertiary and Pleistocene. In
this regard, Beringia and associated refugial systems appear as the centre
of evolution for an Arctic-adapted nematode fauna in ungulates with spe-
cific tolerances for transmission in extreme environments characterised by
seasonally low temperatures and varying degrees of desiccation. The late
geographic colonisation of the Nearctic in evolutionary time, however,
is consistent with the relatively limited number of genera and species of
nematodes represented among ruminants at high latitudes of this region
(e.g. Hoberg, 2005a). Further, groups such as the Haemonchinae, Coo-

perinae and Trichostrongylinae are either absent or poorly represented
in the endemic Nearctic fauna, apparently reflecting the cold insular and
xeric habitats and sharply defined seasons that constituted a filter on dis-
tribution (e.g. Hoberg et al., 2004; Hoberg, 2005a; Hoberg et al., 2008a).
For example, Ashworthius, Mazamstrongylus, Orloffia and Trichostrongylus
have Holarctic distributions but are confined to temperate latitudes, with
reduced diversity in the Nearctic, and are not represented in the high-
latitude fauna (Hoberg, 1996; Hoberg et al., 2001, 2002a).
Initial radiation of Nematodirinae, including Nematodirus, occurred in
Eurasian Caprinae during the middle to late Miocene, with subsequent
colonisation of cervids consistent with the high diversity for this genus in
the Palaearctic (Hoberg, 1997b, 2005a). Other than those species that have
been translocated with domestic ruminants, there are few that occupy
Holarctic ranges (Hoberg et al., 2008b). Distinct assemblages of species
occur in Cervidae and Caprinae, indicative of discrete events for geo-
graphic colonisation (Hoberg, 2005a). In parallel, species of Nematodirella
were influenced by multiple dispersal events across Beringia with Cervi-
dae and Bovidae (Lichtenfels and Pilitt, 1983; Hoberg, 2005a).
Metastrongyline nematodes were also influenced by independent
expansion from Eurasia and isolation in North America among both Cap-
rinae and Cervidae (Carreno and Lankester, 1994; Hoberg et al., 1995; Car-
reno and Hoberg, 1999). Low species diversity characterises these groups.
For example, a single species of Dictyocaulus (D. eckerti) appears to be
distributed at high latitudes in caribou/reindeer and muskoxen (Divina
et al., 2002; Höglund et al., 2003). This association initially suggests arrival
in North America linked to such late colonisers as moose near the termi-
nation of the Pleistocene. A consistent 4% divergence in the internal tran-
scribed spacer region 2 (ITS-2) of ribosomal DNA for specimens attributed
to D. eckerti in the Nearctic and Palaearctic, however, suggests a longer
period of isolation (E. Hoberg and A. Abrams, unpublished data).
Among other metastrongylines, the protostrongylid lungworms
are represented by three genera, Protostrongylus (among wild sheep),
Umingmakstrongylus (in muskoxen) and Varestrongylus (in caribou,
moose and muskoxen). Diversity for the lungworms, particularly spe-
cies of Protostrongylus, is greatest among Eurasian Caprinae, reflect-
ing the centres for origin and radiation of these parasites (Boev, 1975;
Carreno and Hoberg, 1999). Distribution of genera and species in the
Nearctic all reflect a complex history of geographic and host colonisa-
tion extending from the Pleistocene to recent events reflecting ongoing
ecological shifts at high latitudes (Hoberg et al., 2002b, Hoberg, 2005a;
Jenkins, 2005; Kutz et al., 2007). Species of Protostrongylus in wild sheep
are components of a broader Holarctic–Eurasian assemblage, and
distributions in North America may reflect expansion with ancestral
species of Ovis (Jenkins, 2005). Unlike Parelaphostrongylus or Varestrongylus

where gene flow for parasites may be mediated by several host species,
lungworms such as P. stilesi circulate almost solely within Ovis, and at
lower latitudes in Ovis and Oreamnos. The limited vagility and isola-
tion demonstrated for populations of O. dalli would be predicted to
drive considerable structure in parasites isolated both within mountain
systems and on high-altitude sky islands. For example, partitioning of
local parasite populations would be predicted by distance across the
Brooks Range, Alaska Range (from the Chugach to near the Lake Clark
region), isolated mountain blocks in the Alaskan interior (Yukon Char-
ley and White Mountains) and across the Richardson Mountains and
Mackenzie Mountains of Canada (e.g. Loehr et al., 2006: E.P. Hoberg
and K. Beckmen, unpublished data). Additionally, contemporary range
expansion and host switching for P. stilesi was documented in a zone
of contact for Dall’s sheep and muskoxen in Alaska and the potential
for reciprocal exchange of parasites between subspecies of Ovibos at the
Mackenzie River ecotone has been predicted (Hoberg et al., 2002a; Kutz
et al., 2004).
Considering other lungworms, Umingmakstrongylus has been regarded
as a relictual genus now endemic to the Central Arctic of Canada where it
appears as a host-specific parasite in muskoxen (Kutz et al., 2001a). Although
currently geographically limited, U. pallikuukensis may have had a more
extensive geographic distribution prior to extinction and extirpation of mus-
koxen populations in both Eurasia and North America (Hoberg et al., 1995;
Campos et al., 2010). In contrast, a single species attributable to Varestrongylus
appears to be widespread at high latitudes from Alaska to Labrador (Kutz
et al., 2007). A primary host association with cervids (caribou) and second-
ary host switching to muskoxen in zones of recent contact has been postu-
lated for this undescribed species. Similar to other protostrongylids, species
of Varestrongylus are prominent parasites of Eurasian ungulates (Boev, 1975).
Protostrongylid muscleworms include the elaphostrongylines and
genera restricted to either the Palaearctic (Elaphostrongylus; except for
E. rangiferi introduced to Newfoundland) or the Nearctic (Parelaphostrongylus)
(Lankester, 2001). The subfamily radiated principally with cervid hosts,
underwent expansion into the Nearctic with Odocoileini and subsequently
diversified among species of Odocoileus south of the Laurentide ice (Platt,
1984; Carreno and Lankester, 1994). At high latitudes of the Nearctic, two
species, Parelaphostrongylus andersoni (in caribou) and P. odocoilei (in wild
sheep, mountain goats and woodland caribou) are currently known. Evi-
dence for south to north expansion tracking continental deglaciation either
in the post-Pleistocene or in an earlier interglacial is seen in the distribu-
tions of Parelaphostrongylus odocoilei in Dall’s sheep, mountain goats and
woodland caribou (Kutz et al., 2001b; Jenkins et al., 2005) and P. andersoni,
which is widely distributed among subspecies and herds of Rangifer
tarandus (Lankester, 2001; Asmundsson et al., 2008). Both species are pri-
mary parasites among species of Odocoileus at temperate latitudes but
through northward geographic expansion and host switching now have
considerably more extensive ranges in North America extending into the
Subarctic and Arctic. The distribution of P. odocoilei excludes the Brooks
Range of Alaska and the Richardson Mountains of the Yukon and North-
west Territories suggesting relatively recent expansion and host switching
from mule deer or black-tailed deer in zones of contact following degla-
ciation of the Cordillera. Alternatively, data from phylogeographic studies
using mitochondrial cytochrome oxidase I (COI) may indicate two centres
of diversity, with (1) a southern population primarily in O. hemionus and
(2) a northern population coinciding in part with the former Mackenzie
refugium that was intermittently present on the northern margin of the
Cordillera during the last glacial maximum (I. Asmundsson, E. Hoberg,
A. Abrams and E. Jenkins, unpublished data) (Worley et al., 2004; Loehr
et al., 2006; Shafer et al., 2010). Such a partition in COI would be consistent
with a pattern of earlier isolation in contrast to expansion and host coloni-
sation from deer during the Holocene. Complex patterns of biogeography
may relate to development of independent contact zones for hosts both in
the unglaciated coastal zone extending on the western margin of the Cordil-
lera and in continental refugial zones between the Cordillera and Lauren-
tide (e.g. Shafer et al., 2010). Philopatric behaviour of thinhorn sheep and
limited postglacial expansion from refugia may further explain the absence
of parasites at higher latitudes.
In contrast to P. odocoilei, populations of P. andersoni appear to be
poorly differentiated, and there is no strong genetic signal demonstrat-
ing isolation north and south of the continental glaciation (E. Hoberg
and I. Asmundsson, unpublished data). A postulated host switch from
white-tailed deer to caribou in a southern refugium during the ultimate
glaciation, subsequent postglacial expansion and a shift from woodland
to barren-ground caribou in the Holocene is consistent with this distribu-
tion. Additionally, expansion during the Holocene explains the apparent
absence of these parasites in once continuous populations of barren-
ground caribou and reindeer, which extended from Beringia into Eurasia
during the late Pleistocene.
Refugial effects are evident in the distributions of both gastrointestinal
and pulmonary parasites in ungulates. Complexes of putative cryptic spe-
cies such as those apparent in Teladorsagia and possibly other Ostertagiinae
including Marshallagia spp. among free-ranging Caprinae are consistent
with a history of range fragmentation and recurrent isolation for hosts and
host species across the late Pleistocene (Hoberg et al., 1999; Hoberg et al.,
in press-b). Thus, T. boreoarcticus in muskoxen represents a member of a
complex that may include additional species in Ovis dalli, O. canadensis
and Oreamnos americana. The distribution for a recently recognised species
of Marshallagia in mountain goats (see Lichtenfels and Pilitt, 1989) appears
to be consistent with a history of refugial isolation and contact with

wild sheep in the late Pleistocene (Hoberg et al., in press-b; Shafer et al.,
2010, 2011).
In contrast, Ostertagia gruehneri is not predicted to demonstrate a signal
for refugial isolation in reindeer and caribou. This ostertagiine is one of
few Holarctic species and may not be strongly differentiated at the popu-
lation level in the Palaearctic and Nearctic in parallel to phylogeography
for its primary Rangifer hosts. Further, extensive mixing of barren-ground
and woodland caribou populations following deglaciation would also
suggest associated patterns of gene flow for parasites. It is not known,
however, whether populations of this ostertagiine are partitioned with
respect to identified herds or ecotypes of caribou in the Nearctic. These
hypotheses remain to be examined based on phylogeographic compari-
sons of parasite populations.
Data for the distribution of filarioid nematodes including species of
Rumenfilaria, Setaria and Onchocerca at high latitudes are patchy and incom-
plete. These vector-borne nematodes appear most often in association with
cervids including caribou and moose in North America (Dieterich and
Luick, 1971). Diversity in these genera across the high latitudes is poorly
understood and it is not clear if single species are widespread in the Hol-
arctic (e.g. Becklund and Walker, 1969; Nikander et al., 2006); for example,
the conspecificity of Setaria tundra in the Palaearctic and S. yehi in the Nearc-
tic, which circulate primarily in cervids, remains unresolved. Further, pub-
lished records of Rumenfilaria in North America are limited to the original
description, although these nematodes are likely to have a broad distribu-
tion coincidental with moose definitive hosts (Lankester and Snider, 1982).
Confounding challenges to understanding historical associations and
the development of faunal structure emerge from cryptic species and
hidden diversity. The latter is an issue of incomplete or insufficient sam-
pling of the northern ungulate fauna (Kutz et al., 2012). It is demonstrated
by the discovery of one new genus and two species of protostrongylids
(Hoberg, et al., 1995; Kutz et al., 2007), and two species of ostertagiines
(Hoberg et al., 1999; Hoberg et al., in press-b). Further, considerably
broader geographic distributions discovered for such protostrongylids as
P. odocoilei in Dall’s sheep and woodland caribou demonstrate the need
for extensive survey and inventory (Kutz et al., 2001b; Hoberg et al., 2003;
Jenkins et al., 2005; Hoberg et al., 2008a). Hidden diversity in conjunction
with assemblages of cryptic species (Pérez-Ponce de León and Nadler,
2010), as revealed among the ostertagiine nematodes, serve to confuse
explanations about the origins and distributions of parasite diversity
in space and time (e.g. Hoberg et al., 1999, 2001). As shown in northern
systems, the effects of refugia and peripheral isolation of host and para-
site populations may be especially pervasive and definition of these pro-
cesses will remain elusive in the absence of fine scale phylogeographic
approaches (e.g. Waltari et al., 2007b; Shafer et al., 2010).
Translocations of reindeer and muskoxen over the past century may

also have an influence on species diversity and population structure for
nematode faunas in ungulates (MacDonald and Cook, 2009; Rausch and
Baldwin, 2002). These may have resulted in introductions for parasites of
muskoxen or reindeer into high-latitude systems in Alaska and Canada
from various sources in eastern Eurasia, Fennoscandia and Greenland with
the development of mosaic faunas at some localities during the past 100
years (Hoberg et al., 1999; Hoberg, 2010; Kutz et al., 2012). Consequently,
there is a need for population-level assessment of all constituents of this
diverse parasite fauna. For example, preliminary data for Teladorsagia nem-
atodes in an introduced population of muskoxen near Aklavik, Northwest
Territories, Canada, revealed a low level of divergence in the ITS-2 region
of ribosomal DNA relative to those parasites in an historically endemic and
isolated host population (E. Hoberg, K. Galbreath and S. Kutz, unpublished
data). The basis for this genetic variation remains unknown, however, and
sampling has been insufficient to completely explore these relationships.
As historical analogues for understanding environmental change,
certain nematodes among ungulates have already been demonstrated as
robust indicators of the role of climatological processes as determinants
of distribution (e.g. Kutz et al., 2005; Jenkins et al., 2006; Hoberg et al.,
2008b). Distributions of protostrongylids appear strongly tied to ambi-
ent temperature and controls on development for larval stages as dem-
onstrated for Umingmakstrongylus and some species of Parelaphostrongylus
and Protostrongylus. Responses associated with thresholds for develop-
ment, temperature tolerances and resilience are critical limiting factors
for distribution and persistence, both historically and in ecological time
(e.g. Hoberg, 2005a). Understanding these physical controls on distribu-
tion provides insights about faunal structure through the Pleistocene and
a baseline for predicting the outcomes of ecological perturbation in the
current regime of climate warming. The latter has been shown associated
with tipping points in development and changes in transmission dynam-
ics for U. pallikkuukensis among muskoxen in the Central Canadian Arc-
tic and may be a driver for ongoing range expansion for parasites in the
region (Kutz et al., 2005; Hoberg et al., 2008b; Kutz et al., 2012).
1.4.5. Human interfaces and occupation of the North

Palaeolithic hunter-gatherers were present near the Arctic Circle in Sibe-
ria by about 40Ka and subsequent human expansion into high latitudes
of western Beringia during the late Pleistocene about 32Ka was the pre-
cursor for occupation of the Western Hemisphere following the peak of
the last glacial maximum (18–22Ka) (Hoffecker et al., 1993; Dixon, 2001;
Goebel et al., 2008; O’Rourke and Raff, 2010). Multiple expansion events
following different pathways may have led to (1) occupation of the Pacific
coastal zone near 14–13.5Ka, (2) dispersal across near coastal zones of the
low Arctic to eastern North America by 14Ka, (3) colonisation of interior
North America via the deglaciated ice-free corridor after 11Ka and (4) col-
onisation of the Aleutian archipelago after 7–8Ka (Dixon, 2001; O’Rourke
and Raff, 2010; Balter, 2012). Although people had been distributed across
high-latitude environments of the Old World, occupation of Beringia,
secondary colonisation of North America and most recently Greenland
occurred sequentially and over an extended time frame from 15 to 4.5Ka
(Dixon, 2001; Goebel et al., 2008).
Pathways for human migration appear initially to be linked to the Ber-
ing Land Bridge. A marine route would provide access to uninterrupted
intertidal zones connecting Eurasia and North America that may have
also included coastal refugial habitats of southeastern Alaska where inver-
tebrates, fishes and marine mammals and birds represent potential prey
(Heaton et al., 1996; Dixon, 2001). In contrast, a terrestrial route would have
facilitated access to assemblages of large mammals, migratory waterfowl
and anadromous fishes as potential prey (Yesner, 2001; Guthrie, 2006). Ter-
restrial- versus marine-oriented migration routes, and later regions occu-
pied by indigenous populations, would influence sources and availability
of potential food, prevailing foraging industries and relative exposure to
different parasite groups (Rausch, 1974).
Arrival of people at high latitudes of the Nearctic about 15Ka altered
the interface for parasites, pathogens and disease in humans, associated
commensals such as dogs and potentially some assemblages of free-
ranging mammals (Rausch, 1972). People influenced parasite diversity
through (1) introduction or facilitation of new geographic distributions
for specific human pathogens (e.g. Enterobius vermicularis and D. latum);
(2) occupation of new ecological settings resulting in exposure to zoonotic
infection from novel assemblages of vertebrate and invertebrate hosts and
parasites, facilitated by local subsistence food chains, water contamina-
tion or proximity, and (3) direct and indirect effects on ecosystem structure
that determined the continuity and persistence of particular assemblages
of hosts and parasites.
Immigrants to North America in the late Pleistocene and early Holo-
cene would have had a long historical association with parasites acquired
through local foraging and the dynamics of food chains (Babbot et al.,
1961; Cameron and Choquette, 1963; Rausch, 1974; Bouchet et al., 1999).
Marine foraging industries would lead to exposures for tapeworms such as
Diphyllobothrium and Diplogonoporus (from marine fishes), intertidal dige-
neans including Cryptocotyle, Stictodora (and other heterophyids), Micro-
phallus and Maritrema (intertidal demersal fishes and mollusks), anisakine
nematodes including Anisakis, Pseudoterranova and Contracaecum (from
pelagic marine fishes and anadromous fishes), the muscle dwelling Trichi-
nella (from polar bears, walrus and beluga) and possibly acanthocephalans
in the genera Corynosoma and Bolobosoma (marine fishes). Aquatic food

resources, and specifically both freshwater and anadromous fishes, are
a source for Diphyllobothrium, Schistocephalus, Nanophyetus and Metorchis.
Terrestrial food sources would be associated with infections from Trichi-
nella (brown bears and black bears) and the apicomplexan Toxoplasma gon-
dii (ungulates, carnivores). These latter parasites are often associated with
marine or terrestrial apex predators exploited in subsistence food chains
(e.g. Jensen et al. 2010).
Local contamination of village sites, specifically by working, or sledge
dogs has represented a substantial source for infections by tapeworms and
nematodes (Rausch, 1974; Rausch and Fay, 2011). For example, zoonotic
infections attributable to E. multilocularis and E. granulosus were facilitated
by significant fecal contamination in permanent villages that were increas-
ingly occupied (in Alaska) after the late1800s. The latter parasite also has
had a strong association with either ungulate hunters or reindeer herd-
ers across the north, in situations characterised by uncontrolled access by
dogs to carcasses of cervid intermediate hosts in conjunction with poor
sanitation (Rausch, 1967). In contrast, the transmission of E. multilocularis
in rodent–canid assemblages was enhanced by synanthropic cycles (dogs
and commensal voles) and development of hyperendemic foci for human
infection in permanent village sites (Rausch and Fay, 2002). Circulation of
these taeniids increasingly contrasted with the historical situation where
people encroached but did not substantially disrupt the structure of natu-
rally occurring host–parasite assemblages (Rausch, 1972). Further, histori-
cal levels of infection pressure for E. multilocularis (and E. granulosus) in
people may have been reduced by a typically nomadic life style where
excessive fecal contamination by dogs in food or water resources would
have been minimised (Rausch, 1951, 1972, 1974).
Infections by the ascaridoid, Toxascaris leonina, are also maintained
in the same synanthropic foci as those of E. multilocularis where levels
of infection among dogs and voles (and contamination) in village sites
may exceed that observed under natural conditions in wild canids (Salb
et al., 2008; Rausch and Fay, 2011). Toxascaris leonina is a prevalent para-
site in either foxes or dogs at high latitudes and may circulate through
arvicoline rodents as intermediate/paratenic hosts. Infections by larval
T. leonina are considered to be the source of eosinophilia observed in people
on St Lawrence Island, Alaska, and perhaps other areas of the north. The
advent of motorised transportation replacing sledge dogs in the 1960s
and 1970s has led to a reduced potential for human infection by both
Echinococcus and Toxascaris in northern villages (Rausch and Fay, 2011).
Considering helminth zoonoses in general, humans have been primar-
ily dead-end or terminal hosts for parasites circulating in free-ranging
or commensal mammals and other vertebrates. In this sense, humans
only rarely contributed directly to local or regional maintenance of these
parasites, where infections were a consequence of passive behaviour linked

to foraging, food habits or exposure by contact or contamination in the
absence of sanitation (Cameron and Choquette, 1963; Jenkins et al., 2011).
An exception may be D. latum that appears to be dependant on humans for
perpetuation of transmission in Alaska (Rausch and Hilliard, 1970).
Species of Diphyllbothrium circulate in strictly aquatic (piscivorous birds
or mammals as definitive hosts), marine (pinnipeds, cetaceans and fishes)
or aquatic/marine cycles (Rausch et al., 2010). In the north, human infec-
tions by particular species are linked to these pathways (Rausch and Hill-
iard, 1970). The earliest documented association with people is from Peru
about 4.5Ka, representing infection by species circulating in pinnipeds.
These cycles are likely the sources of infection of early immigrants into
North America during the Quaternary (Bouchet et al., 1999). This contrasts
with humans as primary hosts such as that implied for D. latum in con-
temporary Alaska (Rausch et al., 1967). Did D. latum expand across Berin-
gia with early human inhabitants of high latitudes or did it arrive later to
become established in focal localities associated with European exploration
and settlement, particularly Russian expansion in the 1700s (Rausch, 1974)?
Transmission pathways represent continuous associations for humans
and pathogens that have extended since initial occupation through the
Holocene to the present (Rausch, 1974). Infection routes for human-associ-
ated pathogens, which characterised the last 10,000 years, have been rapidly
modified over the past century. Among the estimated 4 million residents
of the circumpolar north, indigenous peoples now represent only about
10% of the total population at high latitudes, signifying a demographic
shift to relative dominance by those arriving from the outside (Anisimov
et al., 2007). Shifts from nomadic to sedentary life styles may have initially
increased infection pressure for some synanthropic assemblages of para-
sites (Rausch, 1951, 1972, 1974). Alteration in diets away from subsistence
resources and traditional foods has also reduced levels of infection in
some situations but concurrently has raised new challenges and problems
for health of native peoples. Food security and availability may be increas-
ingly challenged by new patterns of infection and abundance for parasites
and diseases in traditional food animals including muskoxen and caribou
(Hoberg et al., 2008b; Kutz et al., 2009b). Changing demographics have
substantially altered historical linkages for transmission and patterns of
infection pressure for parasites and pathogens at the animal–human inter-
face. Ironically, some infections of Diphyllobothrium now reported in west-
ern Europe are attributed to the importation of salmon from other regions
of the world (Scholz et al., 2009).
As people became mediators of ecosystem structure through local and
regional hunting and fishing practices, there would have been an emerg-
ing influence on species diversity, abundance, distribution and continu-
ity of parasite assemblages, not simply zoonoses. For example, parasite
faunal diversity would have been directly influenced by late and post-
Pleistocene megafaunal extinctions, some of which have been attributed
to human hunting or to interactions between anthropogenic causes and
climate change (Barnosky et al., 2004; Guthrie, 2006; Lorenzen et al., 2011;
Waters et al., 2011). Further, in contemporary time, human-mediated
translocation, introduction and establishment of hosts and parasites over
the past century have altered the distributions for helminths and other
pathogens in some carnivores and ungulates (Hoberg, 2010; Hoberg et al.,
in press-a). The impact of resulting mosaic faunas remains to be identified
(Hoberg et al., 2008a; Hoberg, 2010).
1.5. BIODIVERSITY – HISTORY IN A COMPLEX

NORTHERN FAUNA
There is a generality for low diversity in terrestrial host–parasite systems at

high latitudes. Although at first these patterns are intuitive, closer inspec-
tion has some interesting implications that are connected to a history of
expansion from Eurasia into North America and further south into the
Neotropical zone. Essentially, there is a longitudinal gradient in diversity,
an historical legacy of recurrent or episodic geographic expansion and col-
onisation, which appears in most complex host–parasite systems. Species
richness within respective helminth groups is greatest in Eurasia, less in
North America and minimal in the Arctic, or alternatively, there is a gra-
dient with a gap at high latitudes (Fig. 1.6). The gap of minimal diversity
represents those taxa that could not successfully colonise high latitudes
or that because of thresholds and tolerances and narrow resilience were
secondarily eliminated through local or regional extinction in regimes of
rapid environmental change (e.g. Barker et al., 2011). The gradient empha-
sises the ancestral centre of origin for the fauna (Eurasia) and the historical
processes that have been at play in determining diversity downstream.
Aside from the longitudinal gradient, there is a secondary latitudinal
gradient with greatest diversity (for the few Holarctic groups) in temper-
ate latitudes in either Eurasia or North America. For example, there are
15 genera of Ostertagiinae circulating in ungulate hosts globally. Of these,
only 3 genera and 3 or 4 species occur in the Subarctic and Arctic, 2 gen-
era are Holarctic but with a gap at high latitudes and 10 are Old World
(Palaearctic and African). Patterns extend to the species level (Table 1.7),
and for Marshallagia, there is 1 Holarctic species across temperate to high
latitudes, 1 North American and 10 Eurasian species (Hoberg et al., in press-
b). In Ostertagia, only O. gruehneri occurs across the Arctic; one species is
endemic to North America, there are no species shared across regions and
the greatest diversity (about 10 species) is observed in Eurasia. Teladorsagia
boreoarcticus is probably Holarctic, and no other species (of which there
are two additional congeners) occur outside of a history of introduction
FIGURE 1.6 Distribution of helminth faunal diversity and gradients in species richness
resulting from episodic expansion and isolation across Eurasia and North America through
the Beringian region. Among most helminth groups, diversity (species richness) is greatest
in Eurasia (++++), minimal at high latitudes (few Holarctic species +/−) and is reduced in
the Nearctic (++). These patterns, or longitudinal/latitudinal gradients, reflect the down-
stream influence of eastward geographic colonisation over time from regions of ancestral
origin (Eurasia) to secondary centres of diversification (North America). Consequently,
expansion and geographic colonisation across Beringia set the stage for later diversifica-
tion within helminth groups in both the Nearctic and the Neotropical regions.
in North America. Among the nematodirines, there are 6 Holarctic species

of Nematodirus at high latitudes, about 7 from the Nearctic and Neotropi-
cal regions and about 40 restricted to the Palaearctic including those that
have been globally disseminated with movement of domestic artiodactyls
(Kulmamatov, 1974; Hoberg, 2005a). Additionally, in the realm of ungulate
parasites, many simply never colonised North America coincidental with

their hosts, including gastrointestinal parasites such as Haemonchus, Coo-
peria and Spiculopteragia and protostrongylids represented by Cystocaulus,
Muellerius and others. Intercontinental expansion in the middle to late
Pliocene with cervids may be indicated by the occurrence of Mazamstron-
gylus and Ashworthius in Eurasia and the Western Hemisphere (but not in
the Arctic) under the influence of relatively equitable climate factors and
warm conditions at high latitudes (Hoberg et al., 2004; Robinson, 2011). In
contrast, the distributions for Ostertagia, Teladorsagia, Marshallagia and the
nematodirines were not strongly influenced by climate filters related to
cold and xeric environments later in the Pleistocene.
Considering otherwise Holarctic groups, a gradient for downstream
diversity is also represented among parasites in rodents, lagomorphs and
carnivores and serves to highlight the history of episodic expansion link-
ing ancestral centres of diversification in Eurasia with secondary zones in
North America (Tables 1.4–1.6). A reduction in diversity with geographic
colonisation also indicates the predominant eastward direction for expan-
sion during the Pleistocene (Rausch, 1994; Waltari et al., 2007b). Limited
diversity and the historical mechanisms involved emphasise the unique
nature and relative simplicity of northern host–parasite systems. Further,
and secondarily in some systems, a latitudinal gradient has been superim-
posed, which reflects north–south and south–north expansion, isolation
and diversification particularly in North America (Galbreath and Hoberg,
2012). Among pikas, these patterns for recurrent expansion and isola-
tion have resulted in the origins of substantial diversity in most helminth
groups that secondarily emerged following geographic colonisation from
Eurasia; to some degree, a contrast with a general pattern was observed in
other host–parasite assemblages (Table 1.5).
The apparently unique distribution of diversity downstream from
Eurasia and across Beringia was initially recognised in the history of arvi-
coline rodent faunas (Repenning, 2001). A general or replicated pattern for
species richness now seems evident for complex biological systems across
this geographic arena. We introduce the new term – ‘trans-Beringian
disjunct distribution’ – for biotic assemblages with largely boreal temper-
ate to Subarctic ranges that retain some limited diversity in Beringia or
high latitudes. The most diverse components of these assemblages are
in temperate Eurasia and temperate North America. Such patterns are
best exemplified among helminth groups in ungulates, rodents and lago-
morphs under the influence of (1) rapid expansion tracking suitable habitat
through Beringia during the Pliocene and Pleistocene; (2) exclusion, extir-
pation or local extinction in east and west Beringia during glacial maxima
and (3) limited postglacial expansion returning to Beringian latitudes as a
function of specific tolerances, developmental thresholds and other biotic
(e.g. distribution of potential intermediate hosts) and abiotic parameters.
Thus, there is an apparent interplay between vagility and specialisation

and episodic climatological processes as determinants of species ranges in
these assemblages (Dynesius and Jansson, 2000).
1.5.1. General biogeographic patterns

A history of episodic expansion and isolation under variable regimes of
climate defined by glaciations and interglacial stages, with the origin and
dissolution of refugial zones, emerges as a central driver for patterns of
distribution and diversification of the northern fauna (e.g. Dynesius and
Jansson, 2000; Jansson and Dynesius, 2002; Shafer et al., 2010). Encom-
passed within this rather general framework, specific examples or models
for these and related processes are evident, constituting a pathway for
exploring the relative roles and interactions of different biogeographic
determinants in space and time.
(1) The standard Beringian model: a) Geographic colonisation of eastern
Beringia from Eurasia across the land bridge coincidental with glacial
maxima during the Pleistocene (or prior to the Pliocene–Pleistocene
boundary); b) subsequent interglacial vicariance of Beringian faunas at
Bering Strait and c) interglacial expansion south into North America,
subsequent vicariance north and south of the Laurentide–Cordillera
with post-Pleistocene expansion to varying extent as a function of refu-
gial effects. Interestingly, the strong phylogeographic discontinuity pre-
dicted at Bering Strait appears shifted westward towards the Kolyma
highlands of Chukhotka near the periphery of western Beringia (e.g.
Galbreath and Cook, 2004); this pattern is emerging as a generality for
a number of mammaliam groups and presumably their parasites.
(2) North American regional southern refugia: During the last glacial,
maximum forested refugial zones (eastern and western) have been
inferred south of the Laurentide. Postglacial expansion in the early
Holocene from south to northwest is postulated from eastern refugia
in North America (e.g. Rangifer, Martes americana, Myodes voles, black
bears, tree squirrels, red fox). Distributions are consistent with early
expansion and occupation of North America by a number of discrete
mammalian lineages by the mid-Pleistocene, followed by extirpa-
tion of high-latitude populations in eastern Beringia or the Arctic.
For example, the history of Soboliphyme in martens exemplifies this
complex process for hosts and parasites (Koehler et al., 2009).
(3) Repopulation of eastern Beringia from Eurasia: Extirpation of some
lineages or populations of mammals in eastern Beringia was followed
in a number of cases by expansion secondarily from Eurasian sources
during glacial maxima. This pattern is exemplified by both caribou/
reindeer and red foxes and some arvicoline rodents and their para-
sites. Thus, Eurasian and Beringian populations were continuous and
contrast with those expanding from the south, tracking deglaciation

in post-Pleistocene environments. This suggests that many taxa and
species or populations of parasites that are considered to be wide-
spread in the Nearctic from temperate to Subarctic and Arctic lati-
tudes may not be closely related, and some will have greater affinities
to faunas now isolated across Bering Strait in eastern Eurasia.
(4) Return to Beringia: Patterns involve expansion into North America by
the mid-Pleistocene or earlier, occupation of temperate latitudes dur-
ing a subsequent interglacial and isolation and extirpation of northern
populations during the next glacial cycle in the absence of expansion
from Eurasia into eastern Beringia. In this model, repopulation of Berin-
gia occurs from southern refugia prior to the Wisconsinan or ultimate
glaciation, with lineage continuity and diversification encompassing
multiple glacial–interglacial cycles. North American pikas and the
diversification of O. princeps and O. collaris and their complex helminth
fauna are consistent with this scenario (Galbreath and Hoberg, 2012);
additionally, shrews of the species complex represented by Sorex cinereus
demonstrate this association (Demboski and Cook, 2003; Hope, 2011).
(5) Pleistocene (Wisconsinan) expansion from Eurasia: These taxa
represent late arrival on the Beringian scene and include moose, the
northern lineage of red fox and some wolves. In these situations, host
taxa are expected to have parasites with greater affinities to Eurasia
than to North America. Postglacial expansion has been variable, with
moose, for example, coming to occupy the entire breadth of North
America in the Holocene.
(6) Western coastal refugial zones: Distinct glacial refugial zones on the
outer coast of British Columbia and Alaska are consistent with iso-
lation and diversification of hosts and parasites in western insular
habitats. Coastal refugial patterns have been demonstrated for bears,
wolves and Pacific martens (Heaton et al., 1996; Cook et al., 2006;
Hoberg et al., in press-a).
(7) Macro- and micro-refugial effects: Habitat structuring and partition-
ing during both glacial maxima and under special circumstances for
particular taxa under interglacial regimes serve to influence patterns
of isolation and diversification for complex host–parasite systems.
Most clearly defined for glacial stages, refugial zones may be large
such as that encompassing Beringia or at very small spatial scales such
as those associated with periglacial habitats (Shafer et al., 2010, 2011).
Isolation in interglacial refugial zones at extreme high latitudes often
in archipelagos (responses related to range contraction during warm
periods) followed by population and geographic expansion during
glacial advances represent special cases for Arctic fox and polar bear.
(8) Radiations and bottlenecks: Pliocene/Pleistocene radiations are appar-
ent for a number of host–parasite assemblages, often followed by local or
regional extinction events or bottlenecks of differing scope and intensity
near the Pleistocene/Holocene transition, particularly among carnivores

and ungulates. Radiations appear to have been influenced by vagility,
gene flow and scales of isolation. The distribution of endemic faunas
reflects the interaction of these factors relative to host group: (1) arvi-
coline parasite faunas exhibit endemism at local to regional scales, (2)
lagomorphs at local to regional scales and (3) carnivores and ungulates
at regional to intercontinental scales. These associations reflect scales of
relative vagility and further may indicate the velocity for expansion and
contraction during range shifts (e.g. Sandel et al., 2011; Arenas et al., 2012).
(9) Beringia as a pass-through for neotropical faunas: Beringia was the
gateway for terrestrial expansion from Eurasia into North America, and
for some taxa, geographic colonisation was not limited to the Nearctic. For
example, felids arrived and diversified initially in South America prior
to the emergence of the Panamanian Isthmus near 8Ma, an event that
may also be linked to the early diversification of Trichinella nematodes
(Johnson et al., 2006; Pozio et al., 2009). In contrast, neotropical distribu-
tions for some ungulate parasites, including Nematodirus and Mazamas-
trongylus, were only established following multiple expansion events
across Beringian and into South America with subsequent host switch-
ing (from cervids to camelids) after 3Ma (Hoberg, 2005a). Likewise, the
underrepresentation of endemic Taenia in the Neotropical region relates
to patterns of expansion across Beringia for canids and felids and even-
tual passage into South America in the late Pliocene and Pleistocene
(Webb and Marshall, 1981; Marshall et al., 1982; Rossin et al., 2010).
(10) Dynamic and episodic invasion: It is evident that expansion events
have had considerable complexity in space and time. Considering the
phylogenetic range of these host–parasite assemblages, geographic
colonisation has occurred over varying spatial and temporal scales.
Respective host groups have been influenced by episodic expansion
(contraction) and isolation on different trajectories (e.g. Sandel et al.,
2011; Arenas et al., 2012). Parasite diversity is influenced under sce-
narios for host expansion and establishment (demographic effects for
hosts), recurrent patterns (origin, number and extent of expansions,
synchronic events), propagule size (abundance and intensity of infec-
tions and numbers of infected hosts disseminating parasites, host den-
sity and dispersion) for invading parasites, and life history constraints
(facilitators and buffers) (Hoberg and Brooks, 2008; Hoberg, 2010).
(11) Faunal mosaics for hosts and parasites: Mosaic structure
(addressed in detail below) or faunal admixtures result from recur-
rent or episodic events of expansion and isolation under a dynamic
for taxon pulses (Hoberg and Brooks, 2008, 2010). Most host–
parasite assemblages in the north represent mosaics assembled over
extended time frames since the late Pliocene and through the Quater-
nary and some with anthropogenic influences in the Holocene (e.g.
Hoberg, 2005a, 2010; Hoberg et al., 1999, in press-a).
1.5.2. Mechanisms of faunal expansion in space and time

The complexity of processes for faunal expansion serves as a determinant
of geographic and temporal continuity for assemblages of parasites across
phylogenetically disparate host groups (Hoberg, 2005a). Mechanisms of
invasion and geographic colonisation leading to establishment of com-
plex faunas are equivalent in evolutionary and ecological time (Hoberg
and Brooks, 2008, 2010; Hoberg, 2010). This point is emphasised by the
observation of gradients in diversity that are apparent downstream from
Eurasian centres of origin for many assemblages.
Gradients result from invasion in evolutionary and ecological time
and may be manifested as both microevolutionary (population genetics
and diversity) and macroevolutionary (higher taxon, generic and species
richness) phenomena (e.g. Avise, 2000; Torchin et al., 2003). Depletion of
genetic diversity moving away from an ancestral centre is a characteristic
signature of geographic colonisation involving populations and species.
Anthropogenic introductions of hosts or host groups in contemporary
time may also be expected to lead to selective loss of diversity for associ-
ated parasite faunas (Torchin et al., 2003). These are generalities across a
continuum for host–parasite assemblages in source (ancestral areas) and
recipient regions under the influence of episodic expansion and invasive
processes (Hoberg and Brooks, 2010). Thus, from a macroevolutionary
perspective, for nearly every helminth group with origins in Eurasia, the
diversity downstream (following eastward expansion across Bering Land
Bridge) is substantially reduced in the Nearctic. Considerable diversity in
Eurasia is followed (temporally and spatially) by often complete absence
at high latitudes but with considerably lower levels of species richness
distributed at boreal/temperate latitudes in North America. Under a
regime of episodic expansion, both environmental filters (resilence and
tolerance) and temporal dimensions (relative timing of expansion) can
be invoked to explain resulting patterns of diversity. There are few Hol-
arctic species but also few endemics in the Nearctic resulting from post-
expansion isolation and diversification for helminths among lagomorphs
(to some degree excluding Ochotona with a relatively deep history in the
Nearctic), rodents, carnivorans and ungulates. These generalities remain
to be explored for the diverse faunas associated with soricomoprhs across
the Holarctic region (e.g. Kinsella and Tkach, 2009; Binkienė et al., 2011).
Diversity and its association with episodic invasion further establish the
importance of the Berinigian model where recurrent climatological and
environmental processes serving as determinants of faunal diversity can
be defined in space and time.
In northern systems, intercontinental and intracontinental expansions
have been associated with permissive environmental regimes, host–parasite
assemblages that are sufficiently resilient, and which have developmental
tolerances that fall within climatological extremes of temperature and

humidity. Establishment subsequent to colonisation follows from interact-
ing factors that include the temporal limits for natural dispersal, founder
effects, life history and transmission dynamics, generation time, and initial
population density, abundance and spatial distributions (heterogeneous/
homogenous) for hosts and parasites (Hoberg, 2010). Further, there is a
relationship between dispersal ability (vagility) and refugial history (Shafer
et al., 2010; Sandel et al., 2011; Arenas et al., 2012).
Competitive effects may also be a component of structure for these
faunas. Lafferty (2010) commented on microevolutionary phenomena
related to the relative timing and sequential acquisition of pathogens in
the context of mixed infections in individual hosts. In these instances, the
sequence of exposure in multi-pathogen infections was to some degree
a determinant of successful establishment and persistence by respective
pathogens. It is possible that this dynamic also plays out in a macroevo-
lutionary arena where episodic expansion (multiple events of geographic
colonisation) over time could lead to differential infection pressure and
exposures during the development of multi-species assemblages. Com-
petitive interactions by parasites during faunal assembly could conceiv-
ably serve to either limit or facilitate establishment in new geographic
localities, host species and populations over time.
The mode and tempo for biotic expansion further serve to determine
the ultimate structure of complex host–parasite assemblages. Initially
discussed with reference to population biology and genetic diversity as
a legacy of Pleistocene climate cycles (Hewitt, 1996), contrasting mecha-
nisms for expansion can also influence macro-scale structure for parasites
across continents, regions and landscapes (Hoberg, 2005a). Extensive and
slow rates of expansion involving a substantial representation of hosts
and parasites (both species and populations) across geographically broad
fronts (phalanx) may facilitate establishment over time, maintain diversity
in newly established populations and minimise heterogeneity and pat-
terns of peripheral isolation. In contrast, rapid expansion involving small
populations or segments of larger populations (pioneer) may result in
patchy distributions, founder events, local isolation and varying degrees
of diversification or extinction on landscape scales. Historically, indepen-
dent events of parasite dispersal are consistent with pioneer processes
where bottlenecks and peripheral isolation may be prominent. Alternat-
ing or episodic regimes for climate and habitat perturbation during the
Quaternary interact with the mode and tempo for recurrent expansion
(and contraction) events that have differentially influenced parasite faunal
diversity among mammalian hosts (Hewitt, 1996; Hoberg, 2005a).
Various invasion buffers, developmental and behavioural, also influ-
ence the potential outcomes for expansion and establishment of faunal
complexes. Temporal buffers are an intricate interaction of host-centric
and parasite-centric factors that facilitate continuity of assemblages in

new environmental settings (Hoberg, 2010). Temporal buffers broaden
or extend the time frame under which expansion and introduction may
result in establishment geographically or in new hosts. For example,
extended windows for establishment result from the following: (1) great
host longevity, demographics related to population density and size and
high vagility (e.g. ungulates); (2) recurrent patterns of expansion for host–
parasite assemblages; (3) phalanx dispersal including large numbers on
broad fronts; (4) parasite longevity through indirect cycles over extended
time frames where parasites may be sequestered or live in either defini-
tive or intermediate hosts; (5) parasite longevity in direct cycles where
larvae may exist in arrested stages (e.g. ostertagiines); (6) patterns of inde-
terminate growth and high fecundity (e.g. Umingmakstrongylus); (7) multi-
year life spans (coinciding with host) also leading to high fecundity over
long durations (years) and (8) suitable ecological assemblages or guilds
(Hoberg, 2010; Kutz et al., 2012).
These temporal buffers contrast with factors that result in a limited
or finite window for establishment: (1) limited host longevity, demo-
graphics, low vagility; (2) sporadic or limited expansion; (3) small to
medium mammals and short determinate life spans (e.g. arvicolines,
lagomorphs, mesocarnivores); (4) pioneering expansion involving het-
erogeneity, low numbers, patchy distributions; (5) limited parasite lon-
gevity with determinate life spans, limited fecundity and free-living
stages with limited tolerance and resilience (environmental susceptibil-
ity) (Torchin et al., 2003).
Biotic expansion is further influenced by the presence of environmen-
tal filters that may facilitate or inhibit establishment. Chief among these
were shifts near the Pliocene–Pleistocene boundary (and subsequently in
the Quaternary) between relatively warm to cold and harsh environments
that interacted with tolerances and thresholds for parasite development
and host distribution (e.g. Lister, 2004). Fragmentation of habitats, hetero-
geneity and the distribution of complex and ephemeral refugial zones fur-
ther influenced the potential for persistence of host–parasite assemblages
(Shafer et al., 2010). The directionality of expansion and patterns of diver-
sity in source and recipient regions interact with these filters. Patterns
of absence are attributable in part to biological filters acting on different
components of complex parasite faunas over time. For example, differ-
ential representation of parasite taxa and high-latitude gaps in Holarctic
distributions act as controls on expansion and establishment across Bering
Land Bridge. Alternation of mesic–xeric habitats, which may determine
the distributions for both tundra–steppe floras and an assemblage of mam-
mals (Guthrie, 2001; Galbreath and Cook, 2004; Elias and Crocker, 2008),
would have also directly controlled parasite biogeography. Contemporary
and accelerated climate warming may result in less severe environmental
filters (Callaghan et al., 2004b) allowing northward expansion of some

parasites and host–parasite assemblages (Hoberg et al., 2008b; Kutz et al.,
2009b; Kutz et al., 2012).
1.5.3. An integrated model for diversification – contributions

from the North
Host switching and geographical dispersal of parasites are common phe-
nomena, occurring on many temporal and spatial scales (Hoberg and
Klassen, 2002; Hoberg, 2005b; Nieberding and Olivieri, 2007; Nieberd-
ing et al., 2008; Hoberg and Brooks, 2008, 2010). Diversification involves
both coevolution and colonisation to explain complex host–parasite
associations. Across the expanse of earth history, the major radiations in
host–parasite assemblages have been preceded by ecological disruption,
ecological breakdown and host switching (Hoberg and Brooks, 2008).
A context for host colonisation is defined by the concept of ecological fit-
ting emerging from phylogenetically conservative capacities for host util-
isation (Janzen, 1985; Brooks and Mclennan, 2002; Agosta and Klemens,
2008; Agosta et al., 2010). Most observed host–parasite associations can be
explained by an historical interaction of taxon pulses (cyclical episodes of
expansion and isolation in geographic range) (Erwin, 1985; Halas et al.,
2005), ecological fitting (defining the potential for events of host colonisa-
tion and initial host range) and oscillation (episodes of increasing host
range alternating with isolation in particular hosts) (Janz and Nylin,
2007). This cyclical process sets the stage for codiversification during peri-
ods of relative stability, punctuated by host switching during episodes of
regional to global environmental disruption and climatological change
(Hoberg and Brooks, 2008, 2010).
Taxon pulses represent repeated episodes of expansion/isolation
occurring in response to climate oscillations. Pulses of expansion result
in episodic and extensive faunal overlap through time and a mosaic
assembly for faunal structure. These signatures contrast with patterns of
synchronic divergence for multiple taxa in response to single or unique
isolation events (=vicariance) (see Halas et al., 2005; Folinsbee and Brooks,
2007). The primary drivers for diversification and faunal assembly irre-
spective of host and parasite taxa are most often associated with several
distinct expansion events in space and time at either intercontinental or
intracontinental scales (Hoberg and Brooks, 2010). Taxon pulses result in
faunal mosaics for parasites structured on varying spatial and temporal
scales and relative to the composition and ecological associations of host
taxa. Vicariance does not result in mosaics.
Major episodes of environmental change appear to be the main drivers
for both persistence and diversification of host–parasite systems, creating
opportunities for host switching during periods of geographic expansion
and allowing for cospeciation and coadaptation during periods of rela-

tive stasis and geographic isolation (Brooks and Hoberg, 2008; Hoberg
and Brooks, 2008, 2010). The patterns and dynamics of contemporary
host–parasite associations emerge from an evolutionary context in which
geographic distributions and environment play a key role (e.g. Vrba,
1985) and represent a manifestation of the general evolutionary model
for the ‘sloshing bucket’ where ecological perturbation represents a pri-
mary driver for diversification (Eldredge, 2008; Brooks and Hoberg, 2008;
Hoberg and Brooks, 2008). Hierarchical scale and extent (magnitude) of
perturbation may be critical factors in determining outcomes for biotic
systems and a continuum linking diversification, turnover and extinc-
tion. Much of what we observe today in northern systems is a legacy of
a tumultuous evolutionary history emerging from ecological perturba-
tion at varying spatiotemporal scales. The Arctic represents a particularly
powerful and tractable exemplar system for exploring these interacting
processes.
The generality for taxon pulses as drivers or determinants of faunal
structure in shallow evolutionary and ecological time is revealed in the
Beringian region. Initially, this nexus for Eurasian and Nearctic faunas
was emergent through much of the Tertiary, serving as a primary path-
way for interchange of terrestrial faunas during times of relatively equi-
table climate culminating in the Pliocene. As a crossroads for the northern
continents, Beringia strongly influenced patterns of distribution and
speciation, alternately serving as a barrier or pathway for expansion of
marine and terrestrial faunas and as a centre for diversification over the
past 4–5 Myr (Hopkins, 1959; Sher, 1999). The episodic nature of intersta-
dial–stadial cycles, numbering 20 events during the late Pliocene/Quater-
nary, together with patterns of biotic expansion and isolation at inter- and
intracontinental scales and formation/dissolution of intermittent refugia
have had pervasive effects on the history (speciation, extinction) and dis-
tribution of a complex mosaic of host–parasite systems from the Holarctic
to the Neotropics (e.g. Rausch, 1994; Hoberg et al., 2003; Hoberg, 2005a;
Cook et al., 2005; Dragoo et al., 2006; Zarlenga et al., 2006; Koehler et al.,
2009; Pozio et al., 2009) (Fig. 1.4).
1.5.4. Mosaic faunas – consequences of episodic

geographic expansion
The dynamics of taxon pulses or recurrent patterns of geographic
expansion and isolation in conjunction with episodic host colonisation
results in a mosaic structure for parasite faunas. Geographic expansion
and host colonisation appear to be pervasive mechanisms in driving the
structure of host and parasites associations (Hoberg and Klassen, 2002;
Hoberg and Brooks, 2008, 2010) and have been identified as important
macroevolutionary determinants for patterns of diversity in northern

systems.
Mosaics were originally discussed in the context of invasion biology
related to faunal (regional – interspecific) or populational (landscape –
intraspecific) admixtures of endemic and introduced species brought into
contact and sympatry by anthropogenic translocation and introduction
(e.g. Hoberg et al., 1999, 2008b; Hoberg, 2005a, 2010). Mosaic structure,
however, is a fundamental phenomenon, an observation that emerges
from the idea that processes serving as determinants of complex parasite
faunas are equivalent in evolutionary and ecological time (Hoberg and
Brooks, 2008, 2010). A conceptual linkage to the original terminology for
coevolutionary mosaics as established by Thompson (2005) is also evi-
dent. Mosaics are further consistent with the sloshing bucket model of
evolution with respect to the diversification and maintenance of intricate
faunal assemblages linking ecological and evolutionary hierarchies (e.g.
Eldredge, 2008; Brooks and Hoberg, 2008).
Faunal mosaic structure results from recurrent biotic expansion that
drives the potential for geographic colonisation by hosts and parasites
and possibly secondary host colonisation over extended time frames.
Consider the timing of expansion, arrival and establishment for dispa-
rate elements of a fauna within the context of host ecology and bioge-
ography (sympatry, temporally and spatially, is necessary as a driver of
switching). Trophic linkages, food webs and guilds in conjunction with
ecological fitting establish the potential for switching (e.g. Hoberg and
Adams, 2000; Brooks and Hoberg, 2008). Switching is maximised among
ecologically similar assemblages in proximity or contact and where host
resources (for parasites) are plesiomorphic. Notably, these patterns are
exemplified for Taenia, Trichinella and Soboliphyme among terrestrial car-
nivores (e.g. Hoberg, 2006; Zarlenga et al., 2006; Koehler et al., 2007, 2009;
Pozio et al., 2009); tetrabothriid tapeworms among pinnipeds (Hoberg
and Adams, 2000); nematodirines and protostrongylids among ungulates
(Hoberg et al., 2002b; Hoberg, 2005a); nematodirines and heligmosomes
among lagomorphs (Hoberg, 2005a; Durette-Desset et al., 2010) and anop-
locephalines in rodents and lagomorphs (Haukisalmi et al., 2001, 2006,
2009; Wickström et al., 2005).
1.5.4.1. Defining mosaic structure in space and time

Mosaic structure constitutes a continuum resulting from large-scale
(regions and faunas) to fine scale (landscapes and populations) processes
acting on the distribution of diversity. Consequently, mosaics are mani-
fested spatially and temporally and can involve multi-taxon and interspe-
cific associations in addition to intraspecific and populational interactions
(Hoberg et al., 1999, 2008b; Hoberg, 2010). Mosaics result from faunal
interchange and invasion, both general phenomena in evolutionary and

ecological time (e.g. Marshall et al., 1982; Vermeij, 1991; Hoberg and
Brooks, 2010; Hoberg, 2010).
Faunal and regional mosaics may result from expansion over one-time
land connections, as exemplified in South America with the emergence of
the Panamanian Isthmus that involved complex assemblages of mamma-
lian taxa beginning about 3Ma (Marshall et al., 1982). Unique or one-time
events contrast with episodic processes that bring faunas, congeneric spe-
cies or populations into recurrent contact on varying temporal and spa-
tial scales, as demonstrated in Beringia and the amphiberingian region
over the past 3–5Ma. These latter exchanges ultimately served as determi-
nants of contemporary biotic structure in assemblages of mammals and
parasites of the Holarctic and downstream into the Neotropical zone (e.g.
Hoberg 2005a; Pozio et al., 2009). On northern regional scales, postglacial
expansion out of refugial centres leading to secondary contact or colonisa-
tion also is a driver of mosaic structure (Shafer et al., 2010; Galbreath and
Hoberg, 2012; Hoberg et al., in press-a). Within this general framework,
several classes of mosaics can be defined.
Macroevolutionary faunal mosaics. These are temporal mosaics (ver-
tical or chronological) representing disparate assembly correlated with dif-
ferential expansion and establishment over time. Discrete episodes (taxon
pulses) for host expansion/colonisation lead to historical mosaics com-
posed of elements representing associations and faunas of disparate age.
Episodes involving taxon pulses influence the arrival times for diverse
assemblages representing different taxonomic groups and multiple spe-
cies. Vertical mosaics contribute to the large patterns for diversity and
faunal structure (intercontinental, continental, regional) in the context of
environmental and biotic filters and constraints. These faunal associations
involve species diversity and mechanisms that emphasise interspecific
variation and sympatry. Examples are in the occurrence of assemblages
composed of species groups of disparate age across particular host groups.
Hierarchies are of disparate ages and phylogenetically diverse (consider
comparisons for ungulates, arvicolines or Ochotona) where specific struc-
ture for particular host–parasite assemblages is nested within larger fau-
nal associations. Mosaics contrast with mechanisms derived from simple
vicariance (e.g. Hoberg and Brooks, 2008, 2010) where all elements of a
fauna undergoing simultaneous, large-scale and permanent isolation
would be predicted to be of equivalent age. That such mosaics appear to
be common suggests that vicariance may not always have strong explana-
tory power (Hoberg and Brooks, 2008, 2010).
Horizontal or geospatial mosaics. Spatial mosaics nest within
temporal associations reflecting patterns of assembly correlated with
geography and the geographic extent of expansion or invasion. Refu-
gial effects are emphasised as are primary and secondary patterns
of geographic colonisation as a manifestation of taxon pulses. These

mosaics denote persistent or recurrent refugia in space and time that
is a generality for late Pleistocene environments across the circumpo-
lar region, but of particular significance in trans-Beringian faunas and
in the Nearctic (Galbreath, 2009; Shafer et al., 2010). Related to this is
the concept of habitat heterogeneity and ‘refugia within refugia’ during
particular glacial stages (e.g. Shafer et al., 2010, 2011).
Microevolutionary population mosaics. Landscape scale mosaics
involving populations, emergent from deeper historical processes and asso-
ciations, are manifested by spatial heterogeneity at the intraspecific level
that may be ephemeral in space and time (Thompson, 2005). Population
mosaics are hierarchical and nested within larger temporal and horizontal
structure for host–parasite assemblages. At a microevolutionary scale, these
associations reflect local phenomena and represent the potential for recipro-
cal coadaptation (a microevolutionary counterpart of cospeciation that is not
generally a driver of diversification) and may be tied to transient outbreaks
of disease on landscape scales (Hoberg and Brooks, 2010; Hoberg, 2010).
Anthropogenic invasion mosaics. These mosaics represent the out-
come of processes in ecological time where admixtures of endemic and
introduced species (or populations) result from human-mediated trans-
location and introduction of otherwise non-indigenous taxa (Hoberg,
2010). Such mechanisms not only can influence faunal diversity across
regions but also may extend to the population level on landscape scales
(Thompson, 2005). Primary examples emerge from the interface for natu-
ral and managed systems and are most evident among nematode para-
site assemblages in ungulates (Hoberg et al., 1999, 2008b; Hoberg 2010).
In instances where translocation is used to reintroduce host populations,
as has occurred for some mesocarnivores and ungulates, there is also the
potential for development of mosaics that may have implications in con-
servation biology (Hoberg et al., in press-b).
Contemporary invasion mosaics. Invasions played out in ecological
time may reflect accelerated expansion resulting in rapid and changing
patterns of distribution for host–parasite assemblages. Invasion mosa-
ics involving faunas, species or populations may result from shifts in
distribution mediated by accelerated climate warming and habitat per-
turbation (Parmesan, 2006; Post et al., 2009; Lawler et al., 2009) with the
development of new ecotones and patterns of infection. For example,
substantial northward expansion is projected for assemblages of nema-
tode parasites in ungulates, bringing temperate and high-latitude faunas
into contact (Hoberg et al., 2008a,b; Kutz et al., 2009b; De Bruyn, 2010;
Kutz et al., 2012).
Outcomes for faunal mixing, which apply generally in evolutionary
and ecological time, include (1) faunas that remain discrete in respec-
tive endemic and newly arrived hosts; (2) parasite species that remain
discrete, but faunal structure reflects reciprocal exchange (or unidirec-

tional host colonisation) often at ecotones; (3) hybridisation or introgres-
sion and (4) displacement of an endemic fauna. Processes may be played
out over extended spatiotemporal scales from primary intercontinental
events to regions and landscapes in ecological time and in instances of
postglacial expansion from refugial centres and development of second-
ary contact zones for hosts and parasites. Our developing understanding
of the historical origins and complex structure for mosaics is essential in
formulating predictions about responses to environmental perturbation in
northern systems.
1.5.5. Stories that parasites reveal

Phylogenetics has become the foundation for exploring complex associa-
tions and patterns of diversification, providing a pathway and context
for discovery (e.g. Brooks, 1979, 1981; Brooks and McLennan, 2002; Page,
2003; Hoberg 2005b; Hoberg and Brooks, 2008; Nieberding et al., 2008).
Hierarchical order reveals historical relationships and most critically con-
strains the range of explanations for the structure, biogeography and his-
torical ecology of complex host–parasite systems (Hoberg, 1997a, 2005b);
inference emerges from complex data sets combining morphological and
molecular attributes. Phylogenies are the tapestry to elucidate interactions
related to speciation processes, coevolution, colonisation and extinction,
faunal structure and the environment and ecological continuity across
temporal and biogeographic scales.
The past century has been dominated by coevolutionary thinking
with respect to questions about diversity and faunal structure. Processes
for diversification were most often linked to cospeciation and asso-
ciation by descent between host and parasite lineages (summarised in
Klassen, 1992; Brooks and McLennan, 1993, 2002; Paterson and Banks,
2001; Page, 2003). Extensions of this paradigm for ‘maximum cospecia-
tion’ included formalised assumptions about the evolutionary similarity
of parasite species in phylogenetically related hosts. Thus, faunas should
be of relatively uniform age with respect to the host groups that they
inhabit, and single species were often considered to be geographically
widespread. Following from these observations, common parasite spe-
cies should also occur in both domestic and free-ranging hosts as an
evolutionary legacy of diversification. For example, this was reflected
in concepts for the apparently widespread distributions of nematode
species in broad arrays of ungulate hosts but is also more generally
applicable (e.g. Hoberg et al., 1999).
The coevolutionary reality, however, was discovered to be rather dif-
ferent and considerably more intricate (e.g. Hoberg and Klassen, 2002)
with the idea of pervasive cospeciation giving way to a mechanistically
complex picture of diversification often driven by host and geographic

colonisation on varying spatial and temporal scales linking evolutionary
and ecological time (e.g. Hoberg and Brooks, 2008, 2010). The number of
studies demonstrating a prominent signal of cospeciation in helminth
parasite systems is vanishingly small and these often involve microevo-
lutionary processes of coadaptation rather than macroevolutionary driv-
ers for diversification over time (Nieberding et al., 2008). This observation
is increasingly consistent with diverse assemblages that have so far been
explored in northern systems and globally. Examples of cospeciation are
the exception and where such associations are identified, these are most
often nested within hierarchies originally established through processes
for colonisation (e.g. Wickström et al., 2005; Haukisalmi et al., 2010). Fur-
ther, corroboration of the rarity of association by descent as a driver for
speciation emerges and concurrently identifies processes of colonisation
as substantial contributors to diversification on varying scales (Hoberg
and Klassen, 2002; Hoberg and Brooks 2008, 2010).
In northern systems, colonisation processes are particularly evident
among unrelated mammalian groups – e.g. soricomorphs and arvicolines
in diversification of hymenolepedids (Haukisalmi et al. 2010), or among
particular host groups such as arvicolines with diversification of Paranop-
locephala and Anoplocephaloides (e.g. Haukisalmi et al., 2009). Colonisation
has been the precursor for major radiations by parasite groups in diverse
host taxa and has influenced species-level diversification within nearly all
helminth groups that have been explored (e.g. Hoberg and Brooks, 2008).
Further, there are very few widespread species of parasites and consid-
erably greater diversity in many helminth taxa than previously consid-
ered. For example, the Holarctic tapeworm, Arostrilepis horrida, has now
been demonstrated to represent over 13 species-level lineages distributed
among species of cricetid rodents from Eurasia and North America (Cook
et al., 2005; Makarikov et al., in press). Additionally, considerable diver-
sity is now recognised among anoplocephaline tapeworms where mul-
tiple species complexes have been demonstrated (Haukisalmi et al., 2004,
2008, 2009). Although specificity is often apparent in these assemblages,
diversification was driven to some degree by colonisation events of vari-
ous host taxa.
Parasites reveal a nuanced history for the structure and diversity of
faunal assemblages (Hoberg, 1995, 1997a; Hoberg and Brooks, 2008;
Koehler et al., 2009; Nieberding and Olivieri, 2007; Nieberding et al., 2008;
Hoberg et al., in press-a). Concerted or synchronic expansion and isolation
may result in general patterns of distribution and broad regional struc-
ture as exemplified by vicariance among single or multiple taxa linked
to unique events. In contrast, asynchronous expansion leads to idiosyn-
cratic patterns established at regional to local scales for multiple taxa over
extended time frames (Hoberg and Brooks, 2010). These patterns reflect
episodic processes and responses to differential gradients, habitat and

biotic filters that are unlikely to be temporally uniform but are event spe-
cific in space and time. Dispersal or expansion has been a primary initiator
for biotic structure played out in a dynamic environment of change and a
physical mosaic of heterogeneous habitats (Guthrie, 2001, 2006). Processes
in Beringia and northern systems in general emphasise the importance
of ephemeral associations for host and parasite taxa. In these situations,
parasites may reveal transient historical zones of contact for host species
or populations that otherwise remain cryptic and not immediately identi-
fied (e.g. Hoberg, 1995; Koehler et al., 2009; Galbreath and Hoberg, 2012).
Although we regard episodic dispersal/isolation as a defining process
for the northern fauna, the degree to which expansion events (within a
specific time frame) are synchronous across all groups of mammalian taxa
is unknown. For example, Repenning (2001) suggested that geographic
expansion (across Beringia from the Palaearctic) among arvicoline rodents
was confined to periods early in major glacial cycles and then later dur-
ing the peaks of minor glacial advances (stadials) as a function of habitat
structure and temperature. This may contrast with either ungulates or
carnivores that may not have been as strongly limited by habitat require-
ments and would be expected to have greater vagility.
Current diversity in northern systems represents the outcome of inter-
actions of biotic and abiotic factors that have unfolded in a complex geo-
graphic arena since the Pliocene. Biogeographic and phylogeographic
inference has identified multiple sources for faunal assemblages, under
the influence of recurrent expansion events from Eurasia, and regional
to local effects involving local extinctions and patterns of repopulation.
Both geographic colonisation and in situ speciation have contributed to
the structure and diversity of the northern fauna. In the Nearctic, an inter-
play of processes through the Quaternary in association with Beringian
environments has facilitated both diversification and dissemination of a
speciose and complex parasite fauna linked to mammalian hosts (Rausch,
1994; Cook et al., 2005; Waltari et al., 2007b). Faunal structure represents
the accumulation of species over time and development of spatial and
temporal mosaics resulting from episodes of biotic expansion involving
phylogenetically disparate or homologous assemblages.
1.6. TOOLS FOR BIODIVERSITY DISCOVERY
Explorations of parasite faunal diversity in northern systems and other

regions of the globe are dependent on the availability of sophisticated
tools and resources for biodiversity informatics (Table 1.8). Although
methodological approaches in phylogeography and biogeography have
grown increasingly robust (Avise, 2000; Nieberding et al., 2008; Galbreath
TABLE 1.8 Field-based and analytical tools for the discovery of biodiversity in
northern host–parasite systems
Definitions of parasite diversity

• Geographically extensive and site intensive sampling/ecosystem-level
investigations
• Integrative species-level identifications with morphological and molecular
data
• Species concepts linked to phylogeny and hypothesis testing
• Explorations of cryptic diversity among species
• Phylogeography and population-level approaches
• Molecular-based prospecting for diversity
• Patterns of host and geographic associations on regional to landscape scales
• Genealogical, ecological and numerical diversity
Articulation of historical baselines

• Archival, specimen-based museum resources for morphology and
phylogeography
• Informatics resources for the distribution of diversity linked to collections
• Host–parasite phylogenetic frameworks
• Historical ecology, biogeography/phylogeography to define abiotic and
biotic components of faunal structure and assembly
• Definition of abiotic and biotic drivers of distribution/diversification in
evolutionary/ecological time
Linkage to contemporary systems

• Geographic information system applications
• Geographic modelling (e.g. ecological niche modelling) to explore
determinants of distribution over time
• Environmental effects and constraints on distribution
○ Thresholds/developmental rates/environmental resilience and
tolerances
• Historical analogues for prediction of change in complex systems
○ Responses related to climate and habitat perturbation
○ Invasion biology in evolutionary and ecological time
• Surveillance networks and monitoring
and Hoberg, 2012), we are still fundamentally limited by the quality, scope
and depth of archival biological collections that document patterns of
diversity. Specimens remain the most critical self-correcting records for
biodiversity and in conjunction with baselines from survey and inven-
tory give us a glimpse of faunal structure within particular time frames
(e.g. Hoberg et al., 2003; Hoberg et al., 2009; Kutz et al., 2012). Biodiversity
baselines that combine specimen-based records with informatics about
geographic distribution and host associations are fundamental to tracking

complex host–parasite systems in space and time. Archival resources are
the synergistic tools that link synoptic and strategic field collections with
informatics emanating from phylogenies, history, biogeography, ecology
and population structure. Modern biodiversity assessment is integrative
and relies on the unification of methods and interpretations derived from
molecular and morphologically based approaches (Brooks and Hoberg,
2000, 2006; Cook et al., 2005; Criscione et al., 2005; Koehler et al., 2009).
Archives and biodiversity baselines become the primary tools for
understanding the structure of the biosphere (Brooks and Hoberg,
2000; Hoberg, 2002; Hoberg et al., 2003; Cook et al., 2005; Hoberg et al.,
2008a,b, 2009). The need for integrated approaches combining compara-
tive morphology remains as a foundation or anchor for determination
of morphospecies and combined with phylogeography and population
genetics provides recognition of occurrence of cryptic species and species
complexes (Criscione et al., 2005; Kutz et al., 2007; Pérez-Ponce de León
and Nadler, 2010). Further, site-intensive and geographically extensive
sampling with a shift to application of molecular epizootiological probes,
which to some extent replace laborious necropsy procedures, can greatly
facilitate our capacity for monitoring and tracking changes in geographic
ranges, patterns of host associations and transmission (Hoberg et al., 2001;
Jenkins et al., 2005; Kutz et al., 2007; Asmundsson et al., 2008). By exten-
sion, there is a need to explore population genetics/phylogeography as
a basis to identify geographic sources for faunas, histories for natural
expansion, historical introductions and interactions at ecotones (Koehler
et al., 2009; Hoberg et al., in press-a).
Our current understanding of the general patterns of parasite biodi-
versity in northern systems is emerging from large-scale or synoptic bio-
logical collections linked to assessments of ecology, biogeography and
phylogeography in some regional settings such as Beringia (e.g. Hoberg
et al., 2003; Cook et al., 2005). Additionally, during the International Polar
Year, a broad-based and standardised project exploring health of reindeer
and caribou was initiated under the CircumArctic Rangifer Monitoring
and Assessment Network (Kutz et al., in press). Similar inventories, how-
ever, are underrepresented across Arctic latitudes. Essentially, there are
few comprehensive historical baselines (derived from comparable sam-
pling standards) against which to measure trends for changing patterns
of distribution, host associations or prevalence and abundance of most
parasites (and diseases) in free-ranging and domestic animals or in people
in a regime of accelerated climate change. Indeed, we continue to have an
unbalanced or incomplete picture of diversity, host associations and distri-
bution for parasites in vertebrates and invertebrates in northern regions.
Collections establish the linkage between historical process in evolution-
ary and ecological time (Hoberg et al., 2009).
Systematics also remains as a primary cornerstone. Specimens, associ-

ated data and permanent collections provide a solid foundation for sys-
tematics research through creation of an empirical record that validates
our understanding of the biosphere. The specimen-linked record, how-
ever, is patchy, and despite an extensive published record derived from
survey and inventory (e.g. Rausch, 1952; Gvozdev et al., 1970; Boev, 1975;
Priadko, 1976; Ryzhikov et al., 1979; Govorka et al., 1988; Rausch, 1994),
relatively few vouchers from field collections of terrestrial mammals
now exist in major museum collections in North America or Eurasia. The
importance of having access to well-documented and representative col-
lections of great geographic scope and taxonomic depth is readily appar-
ent (Hoberg et al., 2009).
1.7. PROBLEMS AND CHALLENGES TO BE RESOLVED
A century or more of focused investigations in the North leaves many

unresolved questions that are critical for understanding the outcomes
of environmental change and socioeconomic forcing in these systems.
Considerable unknown diversity remains to be discovered. We have
highlighted this through a number of new genera and species complexes
discovered among ungulates over the past decade (e.g. Umingmakstron-
gylus pallikuukensis, Teladorsagia boreoarcticus and species of Marshallagia
and Varestrongylus) as well as recognition of new or expanded geo-
graphic ranges or host associations for parasites (Parelaphostrongylus
odocoilei, Protostrongylus stilesi). Considerable diversity has also been
discovered among the parasites of arvicoline rodents (e.g. species of
Paranoplocephala and Anoplocephaloides along with new assemblages of
genera and species of Arostrilepis). Further, a unified picture of dynamic
and episodic expansion as the driver for patterns of diversity is now
well established.
There are consequences to unknown diversity, particularly evident
in the potential for emerging diseases and the interface of this phenom-
enon with rapid climate change and environmental perturbation (e.g.
Brooks and Hoberg, 2006, 2007; Hoberg et al., 2008a, 2008b; Kutz et al.,
2009b, 2012). In this regard, we continue to have minimal information for
a number of potential helminth pathogens among ungulates including
filarioids such as Setaria, Rumenfilaria and Onchocerca, lungworms such
as Dictyocaulus and gastrointestinal nematodes including an array of
ostertagiines and nematodirines (Kutz et al., 2012). In some cases where
we have established the limits for diversity among morphospecies of
zoonotic pathogens such as Echinococcus and Trichinella, distributions
and genetic structure remain to be resolved (Rausch, 1967; Thompson
et al., 2005; Nakao et al., 2009).
The importance of understanding northern systems is indicated by

their value as historical models to recognise and define processes involved
in faunal assembly and biodiversity (Waltari et al., 2007a,b; Waltari and
Perkins, 2010; Galbreath and Hoberg, 2012). In northern systems and adja-
cent regions, dispersal, episodic geographic colonisation, host switching,
range fragmentation and isolation of host–parasite populations at inter-
and intracontinental scales have been universal drivers for diversification
through the late Tertiary and Quaternary. Our ability to explore historical
responses to episodic shifts in global climate provides a window or ana-
logue for predicting the cascading effects of rapid environmental change
in contemporary systems. Historically, invasive faunas characterise the
Arctic, and processes of invasion and colonisation, both primary and sec-
ondary effects, have been substantial drivers. We have the opportunity to
reveal microevolutionary phenomena played out on a macroevolutionary
landscape that creates the backbone for faunal structure.
Pervasive host colonisation historically is the precursor that sets the
stage for host switching driven by contemporary ecological perturbation
and predicts major changes in current high-latitude systems. The maps
will be redrawn for many complex host–parasite assemblages over the
coming century. We can use history to define links across Quaternary,
contemporary and future systems and climate states where equivalent
processes have been in play and will continue to be forces that shape eco-
systems and faunas:
• Development of novel and transitional environments, rapid change
• Changing geographical distributions for environments
• Rapid changes in faunal distributions
• Development of secondary contact zones and/or new associations for
host groups
• Accelerated host switching
• Mosaic faunal structure
• Mosaic patterns for ephemeral emergence of diseases in space and
time.
As we have discussed in detail elsewhere, the issue of emergent and inva-
sive pathogens represents a component of the biodiversity crisis linked to
an absence of a comprehensive global taxonomic inventory for parasites
(Brooks and Hoberg, 2006). On broad global scales, there are cascading or
attendant threats to natural systems, human populations, conservation,
agriculture and the global economy. Continuity for ecological and evo-
lutionary mechanisms is universal and emphasises associations for pro-
cesses (biotic expansion, translocation, faunal disruption, establishment,
host switching) and outcomes (faunal structure, emergence of diseases).
Incorporation of historical mechanisms to understanding past and current
faunal structure signals a need to shift from a response-based stance rela-
tive to emerging diseases to a discovery (prediction) -based stance (Brooks
and Hoberg, 2007; Hoberg and Brooks, 2008, 2010; Agosta et al., 2010). The
Arctic is but one piece of a larger interconnected global puzzle.
The Arctic, an obscure place beyond the far horizon for most people, has
also held the imagination of many as an extreme and challenging environ-
ment where highly adapted societies have lived for millennia, but where
European and western exploration seldom ventured until the last 200–300
years (e.g. Lopez, 1986; Berton, 1988; Krupnick, 1993). Faunal diversity in
the North represents interactions at a complex interface linking natural pro-
cesses in evolutionary time with events that have unfolded in ecological time
since the earliest human occupation of high-latitude systems. Consequently,
people are an integral part of the equation for understanding the past and
present and in determining a pathway to the future for these fragile biotas.
ACKNOWLEDGEMENTS
Our exploration of diversity builds on a rich history of research dealing with the northern
fauna and the processes that serve to structure complex biological systems. We are indebted
to Robert L. Rausch and Virginia R. Rausch for their friendship, insights and guidance over
many years of our work in Alaska, the Canadian Arctic and Siberia. David M. Hopkins served
as a critical mentor for E.P.H. and J.A.C. in all things Beringian and introduced us to an intri-
cate historical picture for the north. Appreciation is extended to Vytus Kontrimavichus and
Svetlana Bondarenko who provided a gateway to Chukhotka through the Institute for Bio-
logical Problems of the North in Magadan during the early 1980s. Steven O. MacDonald has
made a huge impact on our integrated field expeditions, as have a large number of Russian
collaborators. A decade of field studies and collaborations with Heikki Henttonen, Voitto
Haukisalmi and Lotta Hardman (Wickström) of the Vantaa Forest Research Center contrib-
uted substantially to our understanding of high-latitude diversity. Further, we thank Alas-
dair Veitch, Richard Popko and Brett Elkin of the Government of the Northwest Territories
(GNT) at Norman Wells and Yellowknife, NT, for their critical contributions to mammalian
parasitology and the opportunity to have interesting experiences in small fixed wing air-
craft on the borders of the Arctic Circle. Our original work in the central Canadian Arctic on
ungulate parasites was greatly facilitated by John Nishi, formerly of the GNT at Coppermine
(now Kugluktuk, Nunavut). Lastly, this view of the biosphere and synergy of geo-expansion,
episodic events and invasion biology was catalysed over the past decade through discussions
and collaborations with Daniel R. Brooks, now at the University of Nebraska-Lincoln. This is
a contribution of the Beringian Coevolution Project, a multi-national research collaboration to
explore diversity across the roof of the world, supported by grants from the National Science
Foundation (DEB 0196095 and 0415668) to J.A.C. at the Museum of Southwestern Biology,
University of New Mexico, and E.P.H. at the US National Parasite Collection.
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CHAPTER 2
Parasites in Ungulates of Arctic
North America and Greenland:
A View of Contemporary
Diversity, Ecology, and Impact
in a World Under Change
Susan J. Kutz*, Julie Ducrocq*, Guilherme G.
Verocai*, Bryanne M. Hoar*, Doug D. Colwell†,
Kimberlee B. Beckmen‡, Lydden Polley§,
Brett T. Elkin¶, and Eric P. Hoberg^

2.1.1. The Arctic 101
2.1.2. Parasites in a changing Arctic 102
2.2. Arctic Ungulate Hosts 103
2.2.1. Caribou – Rangifer tarandus ssp. 103
2.2.2. Muskoxen – Ovibos moschatus ssp. 107
2.2.3. Moose – Alces americanus ssp. 108
2.2.4. Dall’s Sheep – Ovis dalli dalli 112
2.2.5. Other ungulate hosts 113
* University of Calgary, Faculty of Veterinary Medicine, Calgary, Alberta, Canada,

† Agriculture and Agri-food Canada, Lethbridge, Alberta, Canada,
‡
Alaska Department of Fish and Game, Division of Wildlife Conservation, Fairbanks, AK, United
States,
§
University of Saskatchewan, Western College of Veterinary Medicine, Saskatoon, Saskatchewan,
Canada,
¶
Environment and Natural Resources, Government of Northwest Territories, Yellowknife, Northwest
Territories, Canada,
^ US National Parasite Collection, Animal Parasitic Diseases Laboratory, Agricultural Research Service,
USDA, Beltsville, MD, USA

99
100 Susan J. Kutz et al.
2.3. Nematodes 113

2.3.1. Nematodes of the gastrointestinal tract 113
2.3.2. Lung and tissue nematodes: Protostrongylidae
and Dictyocaulinae 139
2.3.3. Other tissue nematodes: Onchocercidae 160
2.4. Cestodes 165
2.4.1. Ungulates as Intermediate hosts: Taeniidae 165
2.4.2. Ungulates as definitive hosts: Anoplocephalidae 171
2.4.3. Emerging issues and knowledge gaps
for the Cestoda 173
2.5. Trematodes 173
2.5.1. Family Fasciolidae 174
2.5.2. Family Paramphistomidae 176
2.6. Protozoa 177
2.6.1. Protozoa of the gastrointestinal tract 177
2.6.2. Tissue and blood protozoa: the Sarcocystidae,
Trypansomatidae and Babesiidae 183
2.7. Arthropods 198
2.7.1. Diptera 200
2.7.2. Phthiraptera 204
2.7.3. Acari 207
2.7.4. Crustacea, Pentastomida 209
2.7.5. Emerging issues and future research
for the Arthropoda 210
2.8. Discussion 210
2.8.1. Parasites alive and well in arctic ungulates 210
2.8.2. Parasite biodiversity 211
2.8.3. Characteristics of arctic parasites: New insights 212
2.8.4. Exploring characteristics of arctic
parasites in a broader framework 217
2.8.5. Changing polar environments and host–parasite
interactions 218
2.8.6. Directions forward 220
2.8.7. Conclusions 223
Acknowledgements 224
References 225
Abstract Parasites play an important role in the structure and function of

arctic ecosystems, systems that are currently experiencing an un-
precedented rate of change due to various anthropogenic pertur-
bations, including climate change. Ungulates such as muskoxen,
caribou, moose and Dall’s sheep are also important components of
northern ecosystems and are a source of food and income, as well
as a focus for maintenance of cultural traditions, for northerners.
Parasites of ungulates can influence host health, population dynam-
ics and the quality, quantity and safety of meat and other products
of animal origin consumed by people. In this article, we provide a
Parasites in Ungulates of Arctic North America and Greenland 101
contemporary view of the diversity of nematode, cestode, trema-

tode, protozoan and arthropod parasites of ungulates in arctic and
subarctic North America and Greenland. We explore the intricate
associations among host and parasite assemblages and identify key
issues and gaps in knowledge that emerge in a regime of accelerating
environmental transition.
List of acronyms
State or province or Country
AK Alaska (state of the USA)
GL Greenland
NL Newfoundland/Labrador
NT Northwest Territories (territory of Canada)
QC Québec (province of Canada)
NU Nunavut Territory (territory of Canada)
YT Yukon Territory (territory of Canada)
2.1. INTRODUCTION
2.1.1. The Arctic

The Earth’s northern circumpolar regions present landscapes of stunning
natural beauty – windswept tundra in the north, boreal coniferous forests
to the south, mountains, glaciers and ice sheets. Small, isolated settlements
are scattered throughout and are inhabited by people of great resilience
who maintain close ties to the land. The northern climate is extreme – long
cold winters, short cool summers and, at higher latitudes, months of con-
tinuous darkness in winter and of continuous sunlight in summer. These
regions also support a unique fauna and flora and provide many valuable
non-renewable resources for the world.
In the Nearctic, Alaska (AK), Yukon (YT), Northwest Territories (NT),
Nunavut (NU) and Greenland occupy almost eight million square kilome-
tres of the Earth’s surface (almost sixteen times the size of France), yet they
are home to less than one million people. Approximately three quarters of
these northern people live in Alaska and one quarter of the total popula-
tion are aboriginal, with Greenland (88%) and Nunavut (84%) having the
highest, and Alaska (15%) the lowest, proportions.
For many northerners, especially aboriginal peoples, wildlife (mam-
mals, birds and fish) are important sources of food through subsistence
hunting, generate economic activity through sport hunting and tour-
ism and are vital for the maintenance of many cultural traditions. For
example, in the NT, approximately 40% of the residents aged 15 years
and above hunted or fished during 2008 and in almost 30% of house-
holds >50% of the food consumed had been acquired by hunting or fish-
ing (Anonymous, 2009).
This circumpolar ecosystem has been shaped over time by a variety of
complex biotic and abiotic processes. It continues to undergo significant,
and in some instances, accelerating change, much of which results from
human activity, both local and distant, and which has the potential for
global impact (IPCC, 2007).
2.1.2. Parasites in a changing Arctic

Parasites are important components of the arctic ecosystem, influencing
health and sustainability of wildlife populations and the health and well-
being of the people who depend on wildlife. Beginning in the 1940s, a succes-
sion of parasitologists and ecologists have explored parasitism in the Arctic
and advanced understanding of the structure and function of northern host–
parasite systems (Rausch, 1974; Hoberg et al., 2012). In recent years, the rec-
ognition of rapid change in the North has increased these efforts.
Accelerated climate warming and perhaps other anthropogenic land-
scape perturbations are having measurable biological impacts on the
Arctic, including the ecology of ungulates and host–parasite interactions
(IPCC, 2007; Kutz et al., 2009a; Post et al., 2009). Ungulates are impor-
tant components of any ecosystem, serving as food for various carnivores,
omnivores and scavengers. They also influence the abundance and diver-
sity of vegetation and affect soil quality (Danell et al., 2002; Bruun et al.,
2008). In the Arctic, ungulates are important sources of food and income
as well as a focus of traditional activities for indigenous peoples (AMAP,
2002; Nancarrow and Chan, 2010). Additionally, they provide an impor-
tant habitat for various helminth, protozoan and arthropod parasites
(Hoberg et al., 2008a; Kutz et al., 2009b).
Parasites can cause significant clinical and subclinical disease in wild-
life and consequently influence the dynamics and trajectory of wildlife
populations (Hudson and Dobson, 1997; Hudson and Greenman, 1998;
Irvine et al., 2000). The biodiversity, abundance and impacts of macro and
micro parasites in arctic wildlife are highly sensitive to climate and cli-
mate change as well as to other anthropogenic disturbances at the land-
scape level (Kutz et al., 2009a,b; Laaksonen et al., 2010a). The current rate
of climate and landscape change in the Arctic is expected to alter host–
parasite interactions and is a significant concern for the sustainability of
arctic ungulates (Hoberg et al., 2008b; Kutz et al., 2009a; Polley et al., 2010).
In addition to direct effects on host populations, changes in parasitism
in wildlife can also have significant impacts on the people who depend
on wildlife. Parasites can affect the quality, quantity and safety of meat
and other products of animal origin consumed by people and changes in
parasite biodiversity and/or in associated disease processes can influence
nutrition, activity levels and the sustainability of cultural activities for

northern aboriginal peoples (Davidson et al., 2011).
Although parasitism is often portrayed as a negative process, parasites
play important roles and provide unique insights into the historical and
current status and health of ecosystems. They reflect trophic interactions
in food webs, are often in themselves an important food source in an eco-
system and may modulate the effects of contaminants in hosts (Lafferty
et al., 2008; Johnson et al., 2010). Parasites can provide information on
the presence of, and direct or indirect interactions with, sympatric spe-
cies as well as temporal and spatial patterns of habitat use (Hoberg, 2010).
Healthy ecosystems typically have a diverse assemblage of parasites,
reflecting diversity of definitive and intermediate host species and vec-
tors. Detection of the ‘normal’ complement of parasites can be indicative
of a healthy ecosystem (Hudson et al., 2006). Conversely, detection of non-
endemic/invasive parasites or a depauperate parasite community can
suggest otherwise. Contemporary arctic host–parasite assemblages have
been strongly influenced by dynamic shifts in climate and invasive pro-
cesses, particularly over the Pleistocene. Parasites can thus also reflect and
provide insights into host evolutionary history and the complex historical
interactions that have structured ecosystems in space and time (Hoberg
and Brooks, 2008; Hoberg et al., 2012c).
To use parasites as indicators, and to track and predict changes in
parasitism and animal health, comprehensive data on parasite biodiver-
sity, distribution and lifecycles are required (Hoberg et al., 2003; Hoberg
and Brooks, 2008; Hoberg et al., 2008b). Although considerable progress
in defining the diversity and ecology of parasites of arctic ungulates has
been made, there remain substantial knowledge gaps. In this chapter, we
review the current known biodiversity, ecology and impacts of parasites
in arctic ungulates of North America, including Greenland. We identify
knowledge gaps and emerging issues and suggest future research direc-
tions. We define ‘arctic’ ungulates as those species naturally and consis-
tently found in the subarctic and arctic regions as outlined by Conservation
of Arctic Flora and Fauna (CAFF) (Fig. 2.1) and focus on caribou (Rangifer
tarandus ssp.), muskoxen (Ovibos moschatus ssp.), moose (Alces americanus
ssp.) and Dall’s sheep (Ovis dalli dalli).
2.2. ARCTIC UNGULATE HOSTS
2.2.1. Caribou – Rangifer tarandus ssp.

Caribou and reindeer are widespread and abundant across the North
American (Figs. 2.2a–c), European and Asian Arctic regions, with a global
population of 3.8 million individuals and an estimated North American
FIGURE 2.1 Map of the North American Arctic showing important political and
geographic boundaries, including definition of the Subarctic, low and high Arctic. The
latter information adapted from Conservation of Arctic Flora and Fauna (CAFF, 2010).
Map created by N. Pamperin, Alaska Department of Fish and Game.
population of approximately 1.5 million (Geist, 1998; Vors and Boyce,

2009; Russell and Gunn, 2010). Through subsistence harvests, sport hunt-
ing and tourism, caribou are important sources of food and income for
northern aboriginal people as well as a key focus for many traditional
activities (Ferguson and Messier, 1997; Jean and Lamontagne, 2004). Meat
replacement value for a caribou carcass in the North American Arctic is
estimated to be between C$500 and 1,000 and represents a market of tens
of millions of dollars per year (Usher, 1976; Ashley, 2000; Tesar, 2007).
Several subspecies and ecotypes of caribou are recognized in North
America (Banfield, 1961; Miller, 1998); however, the current classification
is likely to be modified by recent genetic studies (McDevitt et al., 2009;
Courtois et al., 2010; Festa-Bianchet et al., 2011). Here, we include all extant
Rangifer subspecies living in the high, low and subarctic and define them
based both on ecotype and current subspecies designation. This includes
the migratory barren-ground caribou (R. t. groenlandicus) occurring in
several disjunct populations in Greenland and across most of the main-
land tundra in NU and NT, Canada; forest and migratory Grant’s caribou
(R. t. granti) in YT and AK; forest (boreal) and mountain dwelling wood-
land caribou (R. t. caribou) throughout the boreal forest and mountain
regions and migratory woodland caribou in northern Quebec (QC) and
Parasites in Ungulates of Arctic North America and Greenland
FIGURE 2.2 Distribution of caribou in (A) Canada and Alaska, USA (ecotypes indicated).
105
FIGURE 2.2—cont’d (B) Greenland. (C) An adult male Dolphin-Union caribou. Canada/
Alaska map created by N. Pamperin and J. Wells, Alaska Department of Fish and Game.
Greenland map adapted from that by Christine Cuyler, Greenland Institute of Nature.
Caribou photograph by S. Kutz. (For color version of this figure, the reader is referred to
the web version of this book.)
Labrador; Peary caribou (R. t. pearyi) on the arctic islands and introduced
Eurasian semi-domesticated reindeer (R. t. tarandus) in western AK, near
Tuktoyaktuk, NT, and in various locations in Greenland.
Caribou in North America are thought to have been isolated in two
separate glacial refugia during the terminal Pleistocene. Rangifer t. pearyi,
R. t. groenlandicus and R. t. granti originated from the Beringian–Eurasian
lineage and R. t. caribou originated from the North American lineage
which was isolated south of the ice sheets and then rapidly spread north
and west across the boreal region in the Holocene (Flagstad and Røed,
2003; Cronin et al., 2005; Røed, 2005; McQuade-Smith, 2009). The historical
biogeography of Rangifer species, together with differences in ecology
among ‘ecotypes’, and multiple introductions and subsequent move-
ments of Eurasian reindeer in the late 1800s and early 1900s (Siem, 1913),
no doubt has had an important influence on the contemporary parasite
fauna (Lankester and Fong, 1989; Hoberg et al., 2012c).
Migratory caribou herds naturally undergo substantial cyclic fluctua-
tions with more than a 10-fold change in population size (Bergerud, 2000;
Couturier et al., 2004). Additive anthropogenic stressors and direct mor-
tality, such as hunting and injury loss, as well as industrial development,
roads, climate change and disease, are thought to have significant impacts
and may exacerbate the episodic population fluctuations (Forchhammer
et al., 2002; Kutz et al., 2009b; Vors and Boyce, 2009; Russell and Gunn,
2010; Festa-Bianchet et al., 2011).
Pronounced population cycles are not recognized for woodland cari-
bou but significant declines in population size and range for this subspe-
cies have been attributed mainly to anthropogenic disturbance and habitat
loss (Vors et al., 2007; Festa-Bianchet et al., 2011; Wasser et al., 2011). For
Peary caribou on the high arctic islands, periodic events of icing of the
snow surface, which prevent access to food, are considered a major cause
of starvation-related mortality (Miller and Barry, 2009). Peary caribou and
woodland caribou are considered ‘endangered’ or ‘threatened’ across most
of their range and barren-ground caribou are listed as ‘of special concern’,
by the Species at Risk Act in Canada (http://www.sararegistry.gc.ca/).
2.2.2. Muskoxen – Ovibos moschatus ssp.

Muskoxen are the second most abundant ungulate in the Arctic and, as with
caribou, they serve as an important source of subsistence food and income
for aboriginal people, the latter through commercial and sport hunting and
sale of fibre (qiviut) (Nuttal et al., 2010). Unlike caribou, they are relatively
sedentary animals and do not undergo extensive seasonal migrations.
There are two recognized subspecies of muskoxen, both of which have
been influenced by historical extinction and extirpation as well as recent
patterns of introduction. Ovibos moschatus moschatus is endemic on main-
land NT and NU whereas the ‘island’ or ‘white-faced’ muskox, O. m. war-

dii, has ranged historically across most of the arctic islands and eastern
Greenland (Fig. 2.3a–c) (Campos et al., 2010). There are approximately
105,000 naturally occurring individuals in the NT and NU (Anonymous,
2011b). They are most abundant on Victoria and Banks Islands, Canada,
and have been harvested commercially at these locations since the mid-
1970s to provide meat and fibre for sale to the public (Gunn et al., 1991b).
The population in east Greenland is over 10,000 (C. Cuyler, pers. comm.).
In addition to these naturally occurring populations, a number of trans-
located herds are established in AK, YT, northern QC and west Greenland.
Ovibos m. wardi herds in AK and YT resulted from a series of translocation
events that began in 1930 with 34 muskoxen from east Greenland brought to
Fairbanks, AK, via the Copenhagen Zoo. In 1935–1936, 31 muskoxen from
Fairbanks were introduced to Nunivak Island, AK in the Bering Sea. These
animals thrived and created a source population of animals that have since
been transplanted to various locations around AK (Paul, 2009). Today, there
are approximately 4750 muskoxen in AK (Harper, 2009). Range expansion
of a population introduced to northeast AK has resulted in approximately
150–200 muskoxen in YT and NT west of the Mackenzie River (Gunn et al.,
1991b; Reynolds, 1998; ADFG, 2011b; Anonymous, 2011a,b).
Ovibos m. wardi were also introduced to northern QC in 1967. Fifteen
muskoxen were translocated from Ellesmere Island (NU) and held cap-
tive near Kuujjuaq as an agricultural initiative (Le Hénaff and Crête, 1989).
Between 1973 and 1983, this herd was gradually released from captive
management and the free-ranging population has grown in size to approx-
imately 1500–2000 individuals ranging mainly between the communities
of Kuujjuaq and Tasiujaq, QC and gradually expanding into Labrador
(Chubbs and Brazil, 2007).
Twenty-seven muskox calves from east Greenland were translocated
to the Kangerlussuaq region in west Greenland from 1962–1965 via the
Copenhagen Zoo. This population subsequently served as the source pop-
ulation for several more translocations in west Greenland (Clausen, 1993)
(Fig. 2.3b). These series of translocations and introductions (in Greenland,
Alaska and Canada) has likely influenced the diversity and distribution
of parasites in muskoxen, and perhaps sympatric species, in the Arctic
(Hoberg et al., 1999; Kutz et al., 2007).
2.2.3. Moose – Alces americanus ssp.

Two subspecies of moose are found in the North American Arctic (Fig. 2.4a
and b). East of the Mackenzie Mountains are Alces a. andersoni and in and
to the west of the mountains is the much larger subspecies A. a. gigas (Bow-
yer et al., 1998; Hundertmark and Bowyer, 2004). Approximately 275,000
moose are found in arctic North America with the vast majority of these
FIGURE 2.3 Distribution of muskoxen in (A) North America.
FIGURE 2.3—cont’d (B) Greenland. Translocations of muskoxen to east Greenland indi-

cated. ©. (C) Adult male muskoxen, O. m. wardi, from Victoria Island, Nunavut. Canada/
Alaska map created by N. Pamperin and J. Wells, Alaska Department of Fish and Game.
Greenland map adapted from that by Christine Cuyler, Greenland Institute of Nature.
Muskox photograph by S. Kutz. (For color version of this figure, the reader is referred to
the web version of this book.)
FIGURE 2.4 (A) Distribution of moose in arctic and subarctic North America, (B) Alaskan
moose (A. a. gigas). Map created by N. Pamperin and J. Wells, Alaska Department of Fish
and Game. Moose photograph by J. Jemison, Alaska Department of Fish and Game. (For
color version of this figure, the reader is referred to the web version of this book.)
(~200,000) in AK; 65,000 in YT and 10,000 in NT and NU (Franzmann and

Schwartz, 1998). Moose are not present in Greenland. There have been
moose translocations within AK (Paul, 2009) but no introductions of moose
into northern Canada or AK.
Although primarily forest dwelling, both subspecies are found along
rivers and lake shores on the tundra extending north to the arctic coast.
Moose are an extremely important source of food for people in the boreal
forest regions across northern Canada and AK (Lynch, 2006; Larter, 2009).
FIGURE 2.5 (A) Distribution of Dall’s sheep in arctic and subarctic North America,
(B) Adult male Dall’s sheep. Map created by N. Pamperin and J. Wells, Alaska Department
of Fish and Game. Photograph by S. Arthur Alaska Department of Fish and Game. (For
2.2.4. Dall’s Sheep – Ovis dalli dalli

Dall’s sheep are common, occurring in disjunct populations throughout
the mountainous regions of AK and the western Canadian Arctic and Sub-
arctic (Fig. 2.5b) (ADFG, 2011a; Anonymous, 2011c; ENR, 2011). There are
approximately 45,000 in NU and NT and 50,000–64,000 in AK. They are
absent from the Arctic islands and Greenland. In general, populations are
healthy and stable across their range. Dall’s sheep have not been translo-
cated within the Canadian North and only a single unsuccessful introduc-
tion has occurred in AK (Paul, 2009). There is some subsistence hunting
of Dall’s sheep as well as a strong recreational-hunting industry that pro-
vides significant income to the northern economy (e.g., ENR, 2011).
2.2.5. Other ungulate hosts

Mountain goats (Oreamnos americanus) just barely extend into the subarc-
tic in southern AK, and the Mackenzie Mountains, NT and southern YT,
Canada. Population numbers are low and these animals are not used to
any significant extent for food or sport hunting. Mountain goats have a
distributional history in western North America, which parallels that of
wild sheep, with both being represented by strongly disjunct populations
across mountainous terrain (Loehr et al., 2006; Shafer et al., 2011). Com-
pared to other arctic ungulates, these ranges indicate relatively limited
vagility, which may be expected to have an influence on the distribution
of parasites (Hoberg et al., in press-a).
Wood bison (Bison bison athabascae), introduced plains bison (Bison bison
bison), mule deer (Odocoileus hemionus), Sitka black-tailed deer (Odocoileus
hemionus sitkensis), occasionally white-tailed deer (Odocoileus virginianus) and
elk (Cervus elaphus) are found in the Subarctic as defined by CAFF and have
distributions that are either parapatric (with minimal overlap) or have some
degree of sympatry with the arctic ungulate species described above. These
other bovids and cervids are more typical of temperate ecosystems. Although
introduced elk populations are established in southern and central YT, these
will not be considered in detail in this chapter. They are, however, potentially
important in the context of ecological perturbation and northward range
expansion and invasion for assemblages of hosts and parasites (e.g. Hoberg
and Brooks, 2008; Kutz et al., 2009b; deBruyn, 2010; Hoberg, 2010).
2.3. NEMATODES
Nematodes are important parasites in ungulates globally (Anderson,
2000). Nematodes of the orders Strongylida, Oxyurida, Trichocephalida
and Spirurida are found in ungulates of Arctic North America and more
broadly across the Holarctic region (Priadko, 1976). Species among these
orders are found in a variety of developmental stages in almost all host
tissues and maintain a diversity of lifecycles.
2.3.1. Nematodes of the gastrointestinal tract

Gastrointestinal nematodes of arctic ungulates are referred to three orders,
including Strongylida, Oxyurida and Trichocephalida. The strongyles,
or bursate nematodes, are the most diverse and abundant. Among the
stronglyes, members of the subfamilies Ostertagiinae and Nematodiri-
nae are dominant in terms of taxonomic and numerical diversity (Hoberg
et al., 2001) (Fig. 2.6). Species richness in these groups is the greatest in the
Palaearctic coinciding with a Eurasian centre of origin for the fauna and
declines on a longitudinal gradient from west to east into North America
FIGURE 2.6 Gastrointestinal nematodes reported from ungulates of arctic North

America, including Greenland. Nomenclature is consistent primarily with Anderson
(2000), with some modifications within the Strongylida (Hoberg and Lichtenfels, 1994;
Durette-Desset al., 1994, 1999; Carreno and Hoberg, 1999; Chilton et al., 2006).
(Hoberg et al., 2012c). Adult nematodes of most species, including both
males and females, generally can be identified on the basis of morphology
(e.g. Lichtenfels and Pilitt, 1983a; Lichtenfels and Hoberg, 1993). In contrast,
diagnostics at the generic and species level for eggs and larvae remains
problematic but is increasingly being addressed through application of
DNA-based techniques (reviewed in Lichtenfels et al., 1997; Dallas et al.,
2000a,b). Integrated methods incorporating both morphological characters
for adults and molecular sequence data for adults and larvae are now con-
sidered standard in conducting survey and inventory and for exploring the
occurrence of cryptic diversity in ungulate nematode faunas (e.g. Hoberg
et al., 2001; Leignel et al., 2002; Jenkins et al., 2005a).
(a) Host and Geographic Range. Knowledge of the diversity and host and
geographic distributions of gastrointestinal nematodes in ungulates of
arctic North America and Greenland is based primarily on cross-sectional
and opportunistic studies focussed on a single host species or at a single
location (e.g. Gibbs and Tener, 1958; Nielsen and Neiland, 1974; Samuel
and Gray, 1974; Fruetel and Lankester, 1989; Korsholm and Olesen, 1993;
Simmons et al., 2001). Ostertagiines (species of Teladorsagia, Ostertagia and
Marshallagia) and Nematodirines (species of Nematodirus and Nematodire-
lla) are found in mixed species infections in individual hosts across most of
their range whereas the occurrence of Oxyuridae and Trichuridae is more
variable among regions and host species. Many of these parasites can infect
a variety of ungulate species but their relative abundance differs across

hosts and geographic regions. For abomasal nematodes, Ostertagia grueh-
neri is most common in caribou; Teladorsagia boreoarcticus is most common
in muskoxen and Marshallagia cf. marshalli is most common in Dall’s sheep
(Nielsen and Neiland, 1974; Fruetel and Lankester, 1989; Hoberg et al., 1999;
Simmons et al., 2001). In caribou and muskoxen, Marshallagia tends to be
restricted to the mountainous regions and arctic islands and is uncommon
on the mainland tundra. For the Nematodirinae, species diversity and abun-
dance tend to be greater in muskoxen and Dall’s sheep compared to caribou
and moose (Nielsen and Neiland, 1974; Hoberg et al., 2001). One exception
may be the Kangerlussuaq-Sisimiut caribou herd of west Greenland where
faecal examinations revealed an unusually high prevalence of nematodirine
eggs in adult females (J. Steele, S. Kutz, C. Cuyler, unpubl. data).
(b) Ecology. The ostertagiine and nematodirine nematodes infecting
northern ungulates have direct life cycles. Adults live in the gastrointesti-
nal tract and eggs are shed in the host’s faeces. Larval development to the
infective third stage (L3) occurs in the external environment and develop-
ment and survival rates are related to climatic condition (O’Connor et al.,
2006). Development of larvae to the infective stage may occur before
(Nematodirinae) or after (Ostertagiinae) hatching from the egg. For the
Trichuridae, the infective larva remains in the egg. Infective larvae (or
eggs with L3) are passively ingested by the final hosts during grazing.
Eggs and/or larvae of some species in domestic ungulates can persist in
the environment over winter if not ingested by a host within the first year
(O’Connor et al., 2006). Once ingested, larvae pass through the digestive
tract until they reach their final location in either the abomasum or the
intestine. Here, the larvae migrate into the mucosa where they develop to
a fourth larval stage (L4). Development to adults is typically completed
in the lumen. Under certain environmental and/or host conditions, the
L4 of several ostertagiine nematodes may undergo inhibited develop-
ment in the mucosa, delaying the completion of their life cycle for several
months (Eysker, 1993; Sommerville and Davey, 2002).
(b) Impacts. The impacts of gastrointestinal nematodes on wildlife
species are relatively unstudied, but they can negatively influence body
condition, physiology (notably reproductive success) and behaviour of
free-ranging ungulates (Albon et al., 2002; Stien et al., 2002; Morgan et al.,
2005). In domestic livestock, ostertagiine and nematodirine nematodes
are significant pathogens and can cause subtle to severe disease with
impacts on food intake, nutrient absorption and body condition, ulti-
mately reducing overall productivity (Holmes, 1987). Some of the most
severe disease impacts result from parasites migrating from the mucosa
to the lumen of the gastrointestinal tract during development and tran-
sition from parasitic larvae to adult stages (Myers and Taylor, 1989).
The Trichuridae tend to be parasites of young animals and can cause
significant diarrhoea in heavily infected domestic livestock. The Oxy-

uridae do not appear to cause significant production loss in domestic
livestock.
2.3.1.1. Subfamily Ostertagiinae
Nomenclature and Taxonomy

Trichostrongyline nematodes of the subfamily Ostertagiinae are
common abomasal parasites of arctic ungulates. Challenges associated
with defining species limits within this group have hindered the under-
standing of the geographic patterns and host associations of these par-
asites (Dróżdż, 1995). In parallel to most helminth groups, numerous
generic and species designations have been assigned over time and eval-
uation of the literature requires a knowledge of these synonymies. This
problem is heightened among the ostertagiines because polymorphism
(multiple morphologically distinct forms within a species) occurs among
adult males in five of 15 genera of the subfamily (Dróżdż, 1995; Hoberg
et al., 2009). For example, historically for some species, discrete differ-
ences in structural characters of the genital cone and spicules resulted in
identification of individuals as different nominal species, often in separate
genera (Gibbons and Khalil, 1982). Only later was it recognized that these
morphological differences defined the major and minor morphotypes of
single species (Dróżdż, 1995). Since the recognition of polymorphism in
the 1970s, the phenomenon has been extensively corroborated based on
cross-breeding experiments, morphology, ecological studies and DNA
sequence data (Daskolov, 1974; Dróżdż, 1974; Lancaster and Hong, 1981;
Lichtenfels and Hoberg, 1993; Dróżdż, 1995; Hoberg et al., 1999, 2001).
Major morphotypes are defined by their numerical dominance (relative to
minor morphotypes) within infrapopulations of single hosts and appear
to represent a balanced polymorphism (Daskolov, 1974; Dróżdż, 1974;
Dróżdż, 1995), although seasonal variation in relative abundance has been
noted (e.g. Hoberg et al., 1999). The recognition, application and misap-
plication of polymorphism among males have considerably confused the
taxonomy and description of ostertagiinae genera and species over the
past century (Dróżdż, 1995; Hoberg et al., 1999). Several arctic osterta-
giines, including species of Ostertagia, Teladorsagia and Marshallagia, are
polymorphic (Table 2.1) (Lichtenfels and Pilitt, 1989; Lichtenfels et al., 1990;
Hoberg et al., 1999; Hoberg et al., in press-a,b). Throughout the chapter,
we adopt the following convention for naming these polymorphic species.
When it first appears in the text, the latin binomials are presented for each
morphotype, with the major morph given first, for example, Marshallagia
marshalli/M. occidentalis, Teladorsagia circumcincta/T. trifurcata/T. davtiani
or T. boreoarcticus f. major/f. minor A/f. minor B in the standard notation
TABLE 2.1 Major and minor morphs for ostertagiines recovered from arctic host species
Major morphotype Minor morphotype
Marshallagia marshalli M. occidentalis

Marshallagia lichtenfelsi f. minor
Ostertagia gruehneri O. arctica
Teladorsagia boreoarcticus f. minor A, f. minor B
T. circumcinctaa T. trifurcata/T. davtiani
a Is
included here for completeness; however, most, if not all records likely represent T. boreoarcticus or
an as yet unidentified species (Hoberg et al., 1999, 2001, 2012a, 2012b).
currently adopted (Dróżdż, 1995; Hoberg et al., 1999). Following this first
appearance in the text, we dispense with the exhaustive listing and use
only the nominal major morphotype to designate the species.
Another more general issue that affects our understanding of diversity
for trichostrongyloids is the presence of cryptic species (Pérez-Ponce de
Leon and Nadler, 2010). An example is T. boreoarcticus described from mus-
koxen of the central Canadian Arctic in 1999 (Hoberg et al., 1999). Prior to
the description of this species, all arctic specimens of Teladorsagia were iden-
tified as T. circumcincta or one of its minor morphotypes, which are common
parasites of domestic sheep (Hoberg et al., 2012b). Teladorsagia circumcincta
was considered to represent a morphologically variable taxon with a con-
siderable host range and broad geographic distribution and as such was
an example of a widespread species (Hoberg et al., 1999). This species and
T. boreoarcticus are similar in appearance but can be distinguished on the
basis of morphological characteristics and mitochondrial DNA and it is now
known that Teladorsagia sp. in muskoxen across their North American range
is T. boreoarcticus (Hoberg et al., 1999). The discovery of T. boreoarcticus may
indicate the occurrence of a taxonomically diverse complex of cryptic spe-
cies within Teladorsagia circulating in domesticated and free-ranging ungu-
lates. The species limits for this complex have yet to be adequately explored
(Hoberg et al., 1999; Leignel et al., 2002; Hoberg et al., 2012b) but have
fundamentally changed our understanding of the history, structure and
diversity of ungulate helminth faunas in the Holarctic region (e.g. Hoberg
et al., 2008a; Hoberg, 2010). Another cryptic species within the Teladorsagia
complex has also been proposed at temperate latitudes (Leignel et al., 2002;
Grillo et al., 2007) and species complexes may also exist for Marshallagia in
North American ungulates (Lichtenfels et al., 1997; Hoberg et al., 2012a).
2.3.1.1.1. Ostertagia gruehneri/O. arctica

(a) Host and Geographic Distributions. Across the Holarctic region, O. grueh-
neri is the most common gastrointestinal nematode of all subspecies of
Rangifer with prevalence approaching (Table 2.2) 100% both within and
TABLE 2.2 Gastrointestinal nematodes reported from ungulates of arctic North

America, including Greenland. The range of prevalence reported is indicated below the
parasite name. Only prevalence estimates based on sufficient sample sizes are included.
Data compiled from available published and grey literature.
Host, Parasite
(range of prevalence) Herd, region or nearest place name
Caribou
Marshallagia marshalli AK Not specifieda; Fairbanksb
NT Banks Islanda,b
NU Dolphin-Unionc; Kugluktuka
GL Kangerlussuaq-Sisimiutd
Ostertagia gruehneri AK Not specifiede; Spruce Creek, Mulchatna,
Northern Alaska Peninsulab
YT Chisanaf
NT Beverlye,g;Bathursth
NU Kugluktuka; Dolphin-Unionc;
Not specifiede; Bathurst Islandb
GL Akia-Maniitsoqi
Teladorsagia boreoarcticus AK Golovinj; Unalakleet j; Mulchatna,
Northern Alaska Peninsulab
YT Chisanaf
NT Banks Islandk; Hope Lakej; Bathursth
NU Dolphin-Union k; Kugluktukb
Teladorsagia circumcinctaw AK Not specifiedl
NT Beverlyg
NU Dolphin-Unionc
GL Kangerlussuaq-Sisimiute
Nematodirella AK Not specifiedm; Egavik, Kivalina,
longissimespiculata Fakotna, Round Upb
NT Beverlyg
Nematodirus tarandi AK Takotnab
NT Beverlyg
Skrjabinema tarandi AK Arctic Slope; Barrow; Brooks Rangen
NT Beverlyg,n
Dall’s sheep
Cooperia spp. AK Granite Mountainso
Marshallagia marshalli - AK Dry Creek, Kenai Peninsula, Interioro;
(18–100%) Not specifiedu
NT Central Mackenzie Mountainsp
Ostertagia gruehneri NT Central Mackenzie Mountainsp
Ostertagia gruehneriy (8%) AK Dry Creek, Interioro
TABLE 2.2 (continued)
Host, Parasite
Teladorsagia circumcincta ## AK Dry Creek, Interior, Kenai Peninsulao
(2–67%)
Nematodirella species AK Dry Creeko
Nematodirus archari or AK Dry Creeko,q; Kenai Peninsulao
N. andersoniy (58–82%) NT Central Mackenzie Mountainsp
Nematodirus davtiani AK Dry Creek, Kenai Peninsulao
(48–77%) NT Central Mackenzie Mountainsp
Nematodirus oiratianus AK Dry Creek, Kenai Peninsulao;
(13–65%) Not specifiedv
NT Central Mackenzie Mountainso
Nematodirus spathiger AK Dry Creek, Kenai Peninsulao
(38–83%) NT Central Mackenzie Mountainsp
Skrjabinema sp. (19,100%) AK Windy Gap, South Central; Dry Creek,
Kenai Peninsulao
Skrjabinema ovis NT Central Mackenzie Mountainsp
Trichuris sp. (25–85%) AK Windy Gap, South Central; Dry
Creek, Granite Mountains, Kenai Pen-
insulao
Trichuris schumakovitschi NT Central Mackenzie Mountainsp
Moose
Nematodirella alcidis AK Not specifieda,m; Palmerb
Muskoxen
Marshallagia marshalli AK Not specifieda,m,u
NT Banks Islandb
NU Devon and Ellesmere Islandsr; Victoria
Islandc
Marshallagia species AK Nunivaks
NU Bathurst Islands
Teladorsagia boreoarcticus AK Barter Islandj
(100%) NT Banks Islandb,h
NU Cox Lake and Rae River near Kugluk-
tuk; Victoria Island (Ekalluk River) j;
Ellesmere Islandj,r
Teladorsagia circumcincta ## NU Thelont; Victoria Islandd
Nematodirella sp. NU Cox Lake near Kugluktukc; Ekalluk
River, Victoria Islandb
Nematodirella alcidis AK Nunavik Islandb
NU Kugluktuka; Victoria Islanda
(continued)
Host, Parasite
Nematodirella gazelli NU Bathurst Islandm,s
Nematodirella longissimespiculata AK Barter Islanda; Collegem
NT Banks Islandb
NU Thelon Game Sanctuaryt
Nematodirus helvetianus AK Collegeb
NT Banks, Islandb
NU Banks Devon and Ellesmere Islandsb,r
Nematodirus tarandi AK Nunavik Islandb; Collegeb
NT Aklavikb
NU Rae River and Cox Lakeb; Ekalluk Riverb
a Hoberg et al. (2001).
b USNPC, (2011).
c Hughes et al. (2009);
d Korsholm and Olesen (1993).
e Lichtenfels et al. (1990).
f Hoar et al. (2009).
g Fruetel and Lankester (1989).
h B. Hoar, J. Invik, S. Kutz, E. Hoberg (unpubl. obs.).
i J. Steele, S. Kutz, C. Cuyler, E. Hoberg (unpubl obs.).
j Hoberg et al. (1999).
k Hoberg et al., (2012b).
l Becklund (1962).
m Lichtenfels and Pilitt (1983a).
n Schad (1959).
o Nielsen and Neiland (1974).
p Simmons et al., (2001).
q Rickard and Lichtenfels (1989).
r Webster and Rowell (1980).
s Samuel and Gray (1974).
t Gibbs and Tener (1958).
u Lichtenfels and Pilitt (1989).
v Lichtenfels and Pilitt (1983b).
w Teladorsagia circumcincta is an apparent misidentification in the Dolphin-Union Herd and should be
referred to T. boreoarcticus (Hoberg et al., in pressb). Other populations of T. circumcincta reported in

northern ungulates (with the possible exception of Greenland) are considered to be T. boreoarcticus
or may be included in a putative complex of species circulating in free-ranging ungulates, which
excludes T. circumcincta (Hoberg et al., 1999, 2001, 2012b).
x Records attributed to Nematodirus archari in Dall’s sheep may be referred to another species endemic
to North America, N. andersoni according to Durette-Desset and Samuel (1989). Additional studies
are required to establish if N. archari is a Holarctic species (Rickard and Lichtenfels, 1989).
y Nielsen and Neiland (1974) originally reported O. ostertagi in Dall’s sheep from Dry Creek, AK.
These specimens were re-determined as O. gruehneri by E.P. Hoberg and A. Abrams. All northern
records of O. ostertagi in isolated populations of free-ranging hosts are likely referable to O. grueh-
neri.
across most caribou and reindeer herds examined (Bye and Halvorsen,
1983; Bye, 1987; Bye et al., 1987; Irvine, 2000; Irvine et al., 2001; Hrabok
et al., 2007; Hoar et al., 2009). The ubiquitous nature of O. gruehneri in Rangi-
fer may reflect the biogeographic history for these cervids and particularly
the history of expansion for host populations linking Eurasia and North
America, as well as expansion in the Nearctic (Hoberg et al., 2012b).
Ostertagia gruehneri does appear to be absent from one natural popu-
lation of caribou in Greenland. In a small survey of the Kangerlussuaq-
Sisimiut caribou herd in west Greenland, O. gruehneri was not found and
other ostertagiines, Teladorsagia sp. (reported as T. circumcincta but may be T.
boreoarcticus or both) and Marshallagia sp. appeared to dominate the aboma-
sal fauna (Korsholm and Olesen, 1993). Recent post-mortem data support
this pattern and also demonstrate that O. gruehneri is present in the Akia-
Maniitsoq caribou herd immediately to the south of, but physically isolated
from, the Kangerlussuaq-Sisimiut herd (J. Steele, S. Kutz, C. Cuyler unpub.
obs.). Environmental conditions in the Kangerlussuaq region are relatively
mild and generally seem to be suitable for development of O. gruehneri. The
absence of the parasite in this herd may be because it did not establish with
the founding animals or because transmission was not sustained during
periods of low host density. The west Greenland caribou herds were estab-
lished by sporadic natural colonization events by only a few animals, and
these populations have undergone periodic crashes (Meldgaard, 1986; Jep-
sen et al., 2002; Cuyler, 2007). Ostertagia gruehneri is also absent in introduced
reindeer in Iceland where the contemporary parasite fauna consists almost
exclusively of species originating from domestic livestock (Gudmundsdottir,
2006).
Ostertagia gruehneri occurs in muskoxen but at a much lower prevalence
and intensity than in caribou or reindeer (S. Kutz, E. Hoberg, unpubl. obs.).
In Dall’s sheep, O. gruehneri is uncommon, with sporadic, low-intensity
infections reported primarily in the summer (Nielsen and Neiland, 1974;
Simmons et al., 2001). Unusually high counts of ‘strongyle-type’ eggs were
observed in summer faecal surveys of one population of Dall’s sheep from
the Richardson Mountains, NT (Table 2.3). These eggs were not identified
to species but most likely are either O. gruehneri or T. boreoarcticus. There
is substantial sympatry with large numbers of caribou from the Porcupine
herd as well as with a small population of muskoxen. Spill-over of O. grueh-
neri from caribou, or T. boreoarcticus from muskoxen, is possible. Notably,
a high abundance of strongyle-type eggs has not been reported from other
Dall’s sheep populations sympatric with woodland caribou (Table 2.3).
(b) Ecology. Egg production for O. gruehneri in Rangifer is highly sea-
sonal with faecal egg counts in captive and wild reindeer and caribou
increasing in the spring, remaining high throughout the summer and then
tapering to very low or negative egg counts from late fall through to the
spring (Irvine, 2000; Irvine et al., 2000; Hoar et al., 2009,2012a). On the
TABLE 2.3 Prevalence (%) and intensity of eggs (epg) or oocysts/gram (opg) faeces of parasites
detected in faecal samples from North American arctic ungulates from July 2000 to July 2010a
Number of fecals collected each

season Marshallagia sp.
Prov/
Herd or location State N totalb Winter Spring Summer Fall % Range epg
Caribou
Banks Island NT 341 122 78 141 57.5 1–65
Sahtu NT 109 73 35 1 0 NA
Chisana Herd YT 158 158 5.4 1–83
Beverly/Qamanirjuaq NT 25 25 0 NA
NU
Bluenose East NT 51 20 0 NA
NU
Bluenose West NT 10 10 0 NA
Cape Bathurst NT 37 37 2.7 77
Dall’s Sheep
Mackenzie Mountains NT 482 66 194 68 154 86.1 1–117
Richardson Mountains NT 262 2 177 60.3 1–111
Sheep Mountain YT 9 9 89.0 1–38
Ivaavik YT 6 6 83.0 2–43
Tombstone Park YT 1 1 0 NA
Moose
Various places AK 26 6 4 9 0 NA
Mackenzie Mountains NT 4 4 0 NA
Sahtu NT 36 27 9 11.1 1–27
Central YK 27 17 10 29.6 2–16
Yukon YK 24 0 NA
Muskoxen
Ellesmere Island NU 4 4 25.0 4–4
Thelon NU 2 0 NA
Victoria Island NU 28 28 42.9 1–2
Banks Island NT 262 72 10.3 1–13
Sahtu NT 8 8 50 1–3
North YT 19 10 9 0 NA
a Samples were frozen at −20°C and analyzed by modified Wisconsin double-centrifugation sugar
flotation technique (specific gravity 1.26) at the University of Saskatchewan (January 2000–August 2005) and
University of Calgary (September 2005–December 2010). Samples collected as part of a wildlife parasitology col-
laborative monitoring program with the wildlife departments of the governments of the Northwest Territories,
Nunavut and Yukon, US Department of Agriculture, and Universities of Calgary and Saskatchewan.
b In some cases, season of faecal collection was not specified and ‘N’ total is greater than the sum of seasonal ‘N’.
c Includes genera of Trichostrongylinae that produce typical ‘strongyle’ egg. Most likely represents a mixture
of Ostertagia gruehneri and Teladorsagia boreoarcticus, the former most common in caribou and the latter most
common in muskoxen.
Anoplocephalid
Strongyle eggsc Nematodirinae Trichuris sp. Skrjabinema sp. eggs Eimeria spp.
Range Range Range Range Range Range

% epg % epg % epg % epg % epg % opg
23.8 1–19 15.5 1–46 0 NA 0 NA 39.3 1–170 16.4 1–2000

31.2 1–46 6.4 1–7 0.9 1–1 0.9 1–1 0.9 25 8.3 2–1000
60.8 1–247 0 NA 0 NA 9.5 1–7 12.2 2–63 4.7 1–236
8.0 1–1 0 NA 0 NA 0 NA 0 NA 8.0 8–28
5.9 1–4 0 NA 0 NA 0 NA 7.8 17–677 5.9 2–11
0 NA 0 NA 0 NA 0 NA 0 NA 0 NA
0 NA 5.4 4–77 0 NA 0 NA 8.1 39–139 0 NA
1.9 1–23 78.4 1–205 55.6 1–602 2.3 1–105 11.2 1–634 89.4 1–5000
53.8 1–321 62.6 1–207 40.1 1–97 3.8 1–161 24.4 1–3000 70.2 1–6000
0 NA 89.0 1–7 78.0 1–22 0 NA 0 NA 100 5–1000
83.0 1–15 83.0 5–26 67.0 8–40 0 NA 0 NA 50 558–1500
100 3–3 100 11–11 0 NA 0 NA 0 NA 100 13–13
0 NA 25.0 1–39 0 NA 0 NA 2.8 76–76 0 NA
0 NA 18.5 1–4 0 NA 0 NA 3.8 14–14 0 NA
0 NA 79.2 1–41 0 NA 0 NA 16.7 6–247 0 NA
100 24–59 100 1–16 0 NA 0 NA 50 1–6 100 153–704

50 1–1 0 NA 0 NA 0 NA 50 26 0 NA
0 NA 28.6 1–8 0 NA 0 NA 0 NA 96.4 1–325
76.3 1–2236 62.2 1–603 0 NA 0 NA 25.6 1–3745 59.5 1–17,500
87.5 14–66 37.5 1–3 0 NA 0 NA 0 NA 25.0 500–750
57.9 1–187 68.4 1–14 5.3 1–1 0 NA 10.5 7–18 47.4 1–40
Canadian mainland tundra, eggs deposited from early June through to

early August can develop to L3 within 3–4 weeks, but exceptionally high
mid-summer temperatures (>30°C) may delay development (Hoar et al.,
2012b). Although eggs do not survive freezing (deBruyn, 2010), there is
high overwinter survival of both L2 and L3 on the tundra (Van der Wal
et al., 2000; Hoar et al., 2012b).
Inhibition seems to be a key characteristic of the life history of O. grueh-
neri in barren-ground caribou. Extremely high rates of inhibition were
observed in wild barren-ground caribou and in reindeer experimentally
infected with L3 cultured from a barren-ground caribou source (Hoar et al.,
2012a). Inhibition may be an important strategy of O. gruehneri in barren-
ground caribou, enhancing survival and transmission of the parasite in a
harsh arctic environment where the primary host is migratory. Propensity
for inhibition appears to differ across different ecotypes or subspecies of
caribou and reindeer (Leader-Williams, 1980; Bye and Halvorsen, 1983;
Irvine et al., 2000; Hrabok et al., 2006a; Hrabok et al., 2007) and may be
a more common feature linked to migratory behaviour of caribou and
highly seasonal environments (Hoar et al., 2012a). Relatively long pre-
patent periods (PPP) for this family of parasites were observed in three
muskoxen infected with O. gruehneri L3 from woodland caribou (two
muskoxen infected with 2500 L3 each on June 7, monitored daily; PPPs 87
and 93 days) and barren-ground caribou (one muskox infected with 7000
L3 in January, monitored weekly; PPP 61 days) (S. Kutz, B. Hoar, L. Polley,
B. Wagner, unpubl. obs.). It is unknown if this reflects a normal maturation
rate (no inhibition) for this parasite in muskoxen or if the larvae under-
went a short period of inhibition first.
(c) Impacts. In reindeer, high intensities of infection with O. gruehneri
(>5000 adult nematodes/host) can lead to decreased food intake, weight
loss and reduced pregnancy rates (Arneberg et al., 1996; Arneberg and
Folstad, 1999; Stien et al., 2002).
Using mathematical models, Albon et al. (2002) demonstrated the
potential role of O. gruehneri in stabilizing population cycles in Svalbard
reindeer. Svalbard is an excellent study site to investigate the impact of
O. gruehneri on its host population because the parasite assemblage of the
reindeer is simple, dominated by O. gruehneri and M. marshalli and the rein-
deer have no competitors or predators on the archipelago. It is likely that
O. gruehneri plays a role in the population dynamics of other reindeer and
caribou populations but establishing such a link is difficult because of con-
founding factors, including predation, competition, hunting, development
and resource exploration and extraction.
2.3.1.1.2. Teladorsagia boreoarcticus

(a) Host and geographic distributions. Teladorsagia boreoarcticus was origi-
nally described as a dimorphic ostertagiine infecting muskoxen and cari-
bou from the central Canadian Arctic and low Arctic islands primarily in
the region adjacent to Kugluktuk, NU (Hoberg et al., 1999). Subsequently,
a second minor morphotype designated as T. boreoarcticus minor B was
described based on specimens from Victoria Island and Banks Island, NU
and NT, although this form has yet to be demonstrated in mainland pop-
ulations (Hoberg et al., 2012b). The morphological similarity of T. boreo-
arcticus to T. circumcincta, a cosmopolitan nematode of domestic sheep,
and the possibility of a cryptic species complex of Teladorsagia partitioned
among free-ranging northern ungulates complicates a clear understand-
ing of diversity and host associations (Hoberg et al., 1999; Hoberg et al.,
2012b). Prior to the description of T. boreoarcticus, Teladorsagia specimens
isolated from caribou, muskoxen and Dall’s sheep in the North American
Arctic and from mountain goats in western Canada and the US were iden-
tified as T. circumcincta. It is now known that those from muskoxen and
caribou across Canada are T. boreoarcticus (Hoberg et al., 1999). A recent
study of gastrointestinal parasites of caribou and muskoxen in the cen-
tral Canadian Arctic reports T. circumcincta, not T. boreoarcticus, from both
host species (Hughes et al., 2009) but this is considered a misidentifica-
tion (Hoberg et al., 2012b). Unresolved is the identity of Teladorsagia sp.
reported from a small number of muskoxen in an introduced population
near Kangerlussuaq, west Greenland. These animals originated from a
natural population in east Greenland and spent time in the Copenhagen
Zoo before arriving at their final destination (Clausen, 1993). Korsholm
and Olesen (1993) reported T. circumcincta in these muskoxen. Although T.
boreoarcticus would be expected in the source population, it is possible that
the animals may have become infected with T. circumcincta in the Copen-
hagen Zoo and maintained that parasite following introduction. Sympat-
ric caribou of the Kangerlussuaq-Sisimiut herd are also host to Teladorsagia
cf. boreoarcticus (J. Steele, S. Kutz, E. Hoberg, C. Cuyler unpubl. data).
The possibility of multi-species infections of Teladorsagia in Greenland is
consistent with the development of mosaic faunas that may be mixtures
of endemic and introduced species (Hoberg et al., 2012a; Hoberg, 2010;
Hoberg et al., 2012c).
Teladorsagia boreoarcticus is by far the dominant abomasal nematode
of free-ranging muskoxen and is also reported in woodland and bar-
ren-ground caribou and reindeer (Hoberg et al., 1999; Hoar et al., 2009;
deBruyn, 2010). Prevalence and intensity in caribou is generally low, but
woodland caribou can maintain T. boreoarcticus in the absence of musk-
oxen (Hoar et al., 2009; deBruyn, 2010). Adults of T. cf. boreoarcticus, but
not O. gruehneri, were found in two of the now extirpated caribou in Banff
National Park, AB (latitude 51° 8’ 60 N) (deBruyn, 2010), demonstrat-
ing a broad latitudinal distribution for T. boreoarcticus. Teladorsagia sp. is
uncommon in Dall’s sheep and the few reports of T. circumcincta (and
morphotypes) in this host, and the more common reports in mountain
goats (Cowan, 1951; Kerr and Holmes, 1966; Nielsen and Neiland, 1974;
Samuel et al., 1977), may be T. boreoarcticus or involve undescribed species
in a broad complex that remains to be fully characterized (Hoberg et al.,
1999).
The complexity associated with defining species limits and diver-
sity within Teladorsagia (and the identification of T. boreoarcticus) clearly
indicates the potential outcomes of incorrect identifications: (i) errone-
ous interpretations about evolutionary history and host associations (e.g.
Brooks and Hoberg, 2006) and (ii) assumptions about life-history char-
acteristics that may not be applicable to the parasite species in question.
Although the extent of this assemblage in free-ranging hosts across the
Holarctic remains unresolved, current evidence suggests that T. circum-
cincta sensu stricto, T. boreoarcticus and a putative array of cryptic species
have been on divergent evolutionary trajectories for a considerable period
of time (Hoberg et al., 1999; Leignel et al., 2002). This has implications for
parasite development and behaviour in an array of free-ranging ungulate
hosts at high latitudes.
(b) Ecology. Preliminary investigations on the ecology of T. boreoarcticus
have revealed some key features of this parasite’s life cycle. Based on
faecal surveys of free-ranging populations in northern Canada, there is
a seasonal pattern of egg production with high egg counts throughout
the summer and very low egg production during the winter (S. Kutz,
B. Wagner, L. Polley unpubl. obs.; Samuel and Gray, 1974), a similar pat-
tern to that of O. gruehneri. Eggs can hatch after short periods of freezing
(1–2 weeks at zero to −20°C) (S. Kutz, B. Wagner, L. Polley unpubl. obs.)
but freeze tolerance of larval stages has not been investigated. In prelimi-
nary laboratory studies, eggs developed to L3 within 8–11 days on the
laboratory countertop (estimate 20–22°C) (S. Kutz, B. Wagner, L. Polley
unpubl. obs.).
The life cycle of T. boreoarcticus has been completed experimentally
in three captive muskoxen (S. Kutz, B. Wagner, L. Polley unpubl. obs.).
Eggs originated from free-ranging muskoxen on Banks Island. One
male castrate muskox was experimentally infected with L3 cultured
from eggs that had been frozen for 1–2 weeks. Approximately 950 L3
were given by stomach tube on 21 June and the muskox did not shed
eggs until the following spring, on 11 March. Two female muskoxen
were each experimentally infected with 23,000 L3 of T. boreoarcticus
on 7 September of the same year and did not shed eggs until 24 May.
These results suggest a strong tendency towards larval inhibition and
are particularly surprising for the muskox infected in June when nor-
mal maturation of the parasite would have been expected. One domes-
tic sheep infected with 23,000 L3 on 7 September shed small numbers
of strongyle eggs intermittently from 5 October to 1 March, when egg
production increased significantly for a few weeks and then dropped
abruptly (S. Kutz, J. Heath, B. Wagner, L. Polley unpubl. obs.). Data

from free-ranging muskoxen indicate that larval inhibition occurs in the
wild. Emergence of larvae from the abomasal mucosa occurs in May
and causes significant pathology including inflammation and oedema
(Kutz et al., 2004b).
(c) Impacts. Teladorsagia boreoarcticus may play an important ecological
role in the population health of muskoxen. High intensities of infection
and abomasitis occur in muskoxen on arctic islands in Canada (Tessaro
et al., 1984; Wobeser, 1984; Blake, 1985; Rowell, 1987; Kutz et al., 2004a) and
it has been suggested that infections in muskoxen may contribute to pop-
ulation cycling through impacts on host body condition and reproduction
(Kutz et al., 2004a).
2.3.1.1.3. Marshallagia marshalli/M. occidentalis

(a) Host and Geographic Distributions. Species of Marshallagia are poly-
morphic abomasal parasites of ungulates across the Holarctic region
(Boev et al., 1963; Hoberg et al., 2001). The species in muskoxen, cari-
bou and Dall’s sheep across their range has been identified as M. mar-
shalli, a presumptive Holarctic species, but may represent a component
of a broader cryptic complex (Lichtenfels and Pilitt, 1989; Hoberg et al.,
2012a). In caribou and muskoxen from Canada and Greenland, M. mar-
shalli appears to be more common in relatively xeric areas, including
alpine regions and on the high arctic islands, compared to the low-lying
mainland (Table 2.2). Marshallagia marshalli is present in the Kanger-
lussuaq caribou and muskox herds of west Greenland but absent from
the Akia–Maniitsoq caribou immediately to the south (Korsholm and
Olesen, 1993; Steele et al., 2012). Marshallagia marshalli is the dominant
abomasal nematode in Dall’s sheep across their range. A previously
unknown species of Marshallagia was recently identified in mountain
goats from the western cordillera of North America and appears to be
specific to this host species and common across its range (Hoberg et al.,
2012a.). The northern extent of the range for this species remains unde-
fined, although it is likely to be in sympatry with populations of M.
marshalli in areas where Dall’s sheep and mountain goats are in contact
(Hoberg et al., 2012a).
(b) Ecology. Marshallagia marshalli has a direct life cycle with second-
stage larvae hatching from eggs and developing to L3 in the environment
(Anderson, 2000). Freeze-tolerant eggs make it well suited for the Arctic.
In a preliminary study, Marshallagia eggs collected from Dall’s sheep in the
Richardson Mountains, NT, remained viable after being frozen at −10 to
−20°C for at least 8 months (S. Kutz, J. Heath, B. Wagner, L. Polley unpubl.
obs.). These eggs were isolated and cultured according to Hubert and Ker-
boeuf, (1984) and L3 were recovered after 13–14 days on the laboratory
countertop (estimate 20–22°C). A captive Dall’s × Stone (Ovis dalli stonei)
sheep hybrid infected with 2700 L3 cultured from these eggs became
patent at 29 days post-infection (S. Kutz, J. Heath, B. Wagner, L. Polley
unpubl. obs.).
Egg production of Marshallagia has a seasonal pattern that is the reverse
of that for O. gruehneri and T. boreoarcticus; for muskoxen and Svalbard
reindeer, it is higher in the winter/spring than in the summer months
(Samuel and Gray, 1974; Irvine et al., 2000) (Table 2.3). Winter transmis-
sion is reported for reindeer (Halvorsen et al., 1999; Irvine et al., 2001) and
saiga antelope (Morgan et al., 2006) and is probable for muskoxen, caribou
and Dall’s sheep.
(c) Impacts. Marshallagia spp. are common, and sometimes numeri-
cally dominant, members of the gastrointestinal parasite fauna of arctic
ungulates. Despite this, very little is known about the life history or
host impacts of this genus. In studies in AK and the Mackenzie Moun-
tains, NT, in the 1970s, adult parasite counts in Dall’s sheep ranged to
>2000 but most animals tended to have <1000 adult worms (Nielsen
and Neiland, 1974; Simmons et al., 2001). The infection intensity of
adult Marshallagia in Dall’s sheep ewes of the Mackenzie Mountains,
NT, was negatively correlated with both host body condition and
pregnancy rates (S. Kutz, N. Simmons, A. Veitch, L. Polley, E. Hoberg
unpubl. obs.). The impacts of M. marshalli in muskoxen and caribou
remain unknown.
2.3.1.2. Subfamily Nematodirinae

Nematodirines are nematodes of the small intestines of ruminants and
lagomorphs (Hoberg, 2005). The subfamily includes species of two gen-
era, Nematodirus and Nematodirella, which are widespread in arctic ungu-
lates and well adapted to life at these latitudes (Tables 2.2, 2.3).
Host and Geographic Distributions. A minimum of nine species of
nematodirines has been reported in free-ranging arctic ungulates from
North America and Greenland (Table 2.2). There remain some inconsisten-
cies in the definitive identification of species in this group. For example,
Nematodirus archari and N. oiratianus, both species recognized in Eurasia,
have been reported from Dall’s sheep (Nielsen and Neiland, 1974) while
other studies identify N. andersoni and N. oiratianus interruptus in bighorn
and thinhorn sheep of North America, suggesting that the geographic and
host associations for these species be re-evaluated (Lichtenfels and Pilitt,
1983b; Durette-Desset and Samuel, 1989; Rickard and Lichtenfels, 1989).
Similarly, in moose, both Nematodirella alcidis and N. longissemispiculata are
commonly reported across most of this host’s range (reviewed in Fruetel
and Lankester 1988). The latter species probably represents a misidenti-
fication in this host and in most cases is likely N. alcidis (Lichtenfels and
Pilitt, 1983a). Lastly, records of N. helvetianus in muskoxen may be in need
of examination, assuming that this nematodirine is primarily associated

with domesticated cattle and has been widely transported globally with
their translocation.
Muskoxen have a diverse nematodirine fauna, including those found
in both in moose and caribou, Nematodirella alcidis, N. longissimespiculata
and Nematodirus tarandi, as well as Nematodirella gazelli, and Nematodirus
helvetianus (although see comment above re: N. helvetianus). Absent from
the reported muskox fauna are those species found in Dall’s sheep (N.
oiratianus/O. interruptus, N. spathiger, N. andersoni/archari and N. davtiani).
This may only reflect that muskox populations sympatric with Dall’s
sheep have not been sampled as opposed to a host barrier. Both N. filicol-
lis and N. spathiger, parasites typical of domestic sheep, are reported from
muskoxen sympatric with domestic sheep in Norway (Alendal and Helle,
1983), and it follows that muskoxen are likely suitable hosts for the nema-
todirines in Dall’s sheep.
In contrast to muskoxen, the reported diversity of nematodirines in
caribou and moose is low. For caribou, Nematodirella longissemispiculata
and Nematodirus tarandi are most commonly reported, along with Nema-
todirus skrjabini, which may be a synonym of N. tarandi (Dikmans, 1935a;
Bergstrom, 1983; Lichtenfels and Pilitt, 1983a; Fruetel and Lankester, 1989;
Hoberg et al., 2001). The low diversity may reflect true species barriers
and/or sampling limited primarily to barren-ground and island cari-
bou populations. The gastrointestinal nematode fauna in the boreal and
mountain woodland caribou ecotypes of the arctic and subarctic is known
only through faecal examinations (Table 2.2) (e.g. Hoar et al., 2009; John-
son et al., 2010), which have not allowed differentiation among species
of nematodirines. Some of these caribou populations are sympatric with
Dall’s sheep and/or mountain goats and all are likely to have greater sym-
patry with moose than do their barren-ground cousins. Captive caribou
do harbour a greater diversity of nematodirines (Fruetel and Lankester,
1989), supporting the hypothesis that the apparent low diversity in wild
sampled caribou may reflect a combination of ecological isolation and
insufficient sampling.
(b) Ecology. Nematodirines are core components of the ungulate para-
site fauna in arctic and boreal ecosystems in the Holarctic and are well
adapted to the environmental conditions at these latitudes (Hoberg, 2005).
Larvae develop to the infective L3 within eggs. These eggs are resistant
to extreme freezing events, freeze–thaw cycles and desiccation, but direct
sunlight and high temperatures may be detrimental (Marquardt et al.,
1959; van Dijk and Morgan, 2008).
Nematodirella alcidis is common in moose from temperate regions but
its abundance and distribution in the Arctic and Subarctic are not well
described. In temperate regions, prevalence ranges from 47 to 100% and
infection intensity is typically quite low (Fruetel and Lankester, 1988).
In northwestern Ontario, 19 of 20 moose were infected with N. alcidis

with an average infection intensity of 111 ± 54. Regardless of the time of
year sampled, only 21% of the N. alcidis population were mature adults
and a large proportion of the remaining specimens were ‘short’ L4. The
authors suggested that this may indicate arrested development for this
species where inhibited larvae may serve as a reservoir to replace adult
nematodes and ensure that eggs are produced throughout the year
(Fruetel and Lankester, 1988). In this and other studies, there was no dif-
ference between adult and young moose with respect to prevalence or
intensity of infection. This pattern is in contrast to that of N. longissemi-
spiculata in caribou where large numbers of nematodes, the majority of
which are sexually mature, are found in the duodenum of calves in their
first summer. Calves produce eggs through the winter and are free of
infection the following spring (Fruetel, 1987). Infection of adult caribou
with N. longissemispiculata is rare, although it is seen in males during the
rut. Additionally, nematodirine eggs were common in approximately
50% of adult female caribou of the Kangerlussuaq-Sisimiut herd of west
Greenland but have not been identified to species (Steele et al., 2012).
Eggs and infective larvae of N. alcidis and N. longissemispiculata can sur-
vive freezing and desiccation and may live for extended periods in the
environment (Fruetel, 1987) (Fruetel and Lankester, 1988). In muskoxen,
adult animals commonly shed eggs of Nematodirines and egg produc-
tion tends to increase in the summer and drop off in the fall (Samuel and
Gray, 1974) (Table 2.3).
Observations on larval development for Nematodirus spp. in domes-
tic animals provide some additional insights into the ecology of these
parasites. Hatching of nematodirines occurs within a temperature range
specific to the species (11–17°C for N. battus but 6–20°C for N. filicol-
lis) and, depending on species and geographic location, chilling may be
important to trigger hatching. For example, for N. battus, the proportion
of eggs that hatch without chilling (i.e. in the fall) decreases at more
northern latitudes (van Dijk and Morgan, 2008; van Dijk and Morgan,
2010). In the Arctic, it is hypothesized that hatching of nematodirines
should be triggered by an extended period of chilling (i.e. the winter)
as opposed to no chilling (i.e. hatching in the summer/fall) (van Dijk
and Morgan, 2010). Hatching after chilling would synchronize appear-
ance of the majority of the L3 in the spring and allow for transmission
throughout the short arctic summer. This strategy may be better than fall
hatching for two reasons: 1) the survival of L3 that hatch after chilling is
greater than those that have not been chilled (i.e. fall) (van Dijk and Mor-
gan, 2010) and 2) L3 hatching from eggs at the end of a short arctic sum-
mer would have a very narrow window for transmission and may not
survive the subzero winter temperatures (van Dijk and Morgan, 2010).
However, in southern Greenland, Nematodirus spp. of sheep, including
N. spathiger, N. helvetianus and N. abnormalis, may hatch within a month

of deposition in the first summer. Development and hatching in this
environment is not synchronous and may extend over 37 months (Rose
and Jacobs, 1990). Although at high latitude, coastal southern Greenland
has a relatively mild maritime climate and the epidemiology of parasites
in this environment may not reflect what occurs in a more ‘arctic’-type
environment.
Differences in development and hatching strategies among Nematodi-
rus species infecting a single host may provide a competitive advantage
of one species over another depending on ambient conditions (van Dijk
et al., 2009) and may partition parasite species over time and space. Those
with a lower hatching threshold may be available to infect hosts earlier in
the spring while those with a higher hatching threshold may not be avail-
able until later in the summer. For example, the developmental threshold
for N. helvetianus is 3°C whereas development for N. spathiger does not
occur below 6–7°C (Rose and Jacobs, 1990). Understanding development
thresholds and ranges, as well as triggers for hatching, is important as
these are key factors influencing the timing and intensity of host exposure
and, consequently, the timing and severity of disease. Additionally, such
information is essential to understand individual species responses to cli-
matic conditions and climate change.
(c) Impact. Nematodirus spp. can cause significant disease in domestic
livestock, particularly young animals (Samizadeh-Yazd and Todd, 1979
), but little is known about the impacts of this group of nematodes in
arctic ungulates. Nematodirella longissemispiculata was reported from the
duodenum and anterior jejunum of a wild muskox and was associated
with enteritis characterized by ‘petechial haemorrhages, some denuding of the
mucosa and a quantity of mucus in the lumen. In addition reddish plaque-like
areas were observed on the walls of the duodenum in the area where these worms
were found. Microscopic examination…presence of a granulomatous-type lesion’
(Gibbs and Tener, 1958). In caribou, pathology caused by this species is
likely limited to calves (Fruetel, 1987). High infection intensities with N.
helvetianus, N. longissemispiculata, and other gastrointestinal nematodes
in captive muskoxen in Norway were considered, along with other para-
sites, as a possible cause of the poor body condition of animals on the
farm (Alendal and Helle, 1983). Nematodirella alcidis in moose is reported
from the anterior third of the small intestine but pathology and clinical
disease in this host are not known (Threlfall, 1967; Fruetel and Lankester,
1988). In Dall’s sheep, Nematodirus species may be partitioned in the small
intestine (Nielsen and Neiland, 1974) and species-specific differences in
impacts might be expected. Data collected from Dall’s sheep in the Mack-
enzie Mountains, NT, in 1971–1972 suggest a trend for higher infection
intensities with Nematodirus spp. in non-pregnant compared to pregnant
ewes and in ewes in poor body condition compared to those in very good
condition (Simmons et al., 2001).
2.3.1.3. Subfamily Oxyurinae
2.3.1.3.1. Skrjabinema spp.

(a) Host and Geographic Distributions. Species of Skrjabinema are pinworms
of the large intestine and caecum. Based on faecal and post-mortem
examinations, Skrjabinema spp. are present at low to moderate prevalence
and intensity in Dall’s sheep and mountain goats, are rare in caribou and
absent from moose and muskoxen (Tables 2.2 and 2.3) (Cowan, 1951; Kerr
and Holmes, 1966; Samuel et al., 1977; Simmons et al., 2001). Skrjabinema
ovis is common in Dall’s sheep and infection intensities are generally low,
ranging from 1 to 60+ worms (Nielsen and Neiland, 1974; Simmons et al.,
2001). Skrjabinema may be underdiagnosed in arctic ungulates as egg shed-
ding can be low and intermittent and few parasitological studies have
included thorough examinations of the large intestines and caecum.
(b) Ecology. Oxyurids are directly transmitted parasites. In most host
species, gravid females migrate to the anus of the host and deposit eggs
in the perianal region whence the eggs can be shed in the faeces or, once
infective, can be transmitted directly between hosts. Development to the
infective stage is species dependent and can take hours to days.
(c) Impacts. The Oxyuridae in domestic ungulates are believed to be
generally benign with few symptoms (Bowman et al., 2003), but their
effects in free-ranging species remain unexplored.
2.3.1.4. Subfamily Trichurinae
2.3.1.4.1. Trichuris spp.

(a) Host and Geographic Distributions. Species of Trichuris are extremely
uncommon in free-ranging caribou and muskoxen but are found in almost
all surveyed populations of Dall’s sheep (Nielsen and Neiland, 1974; Sim-
mons et al., 2001) (Tables 2.1 and 2.2). The species present in Dall’s sheep is
believed to be T. schumakovitschi. In faecal surveys of Canadian muskoxen,
Trichuris spp. were found at a low prevalence on the mainland but were
completely absent from over 1000 faecal samples examined from Banks
Island, NT (Table 2.2). Interestingly, Capillaria sp., a parasite common in
reindeer in the Palaearctic (Hrabok et al., 2006a), is absent from sampled
populations of free-ranging caribou and muskoxen in North America and
Greenland (Table 2.3) although it was detected in a captive herd of rein-
deer in Alberta (S. Kutz, unpubl. data).
(b) Life Cycle. Trichuris spp. are directly transmitted nematode para-
sites of the large intestine and caecum. The L1 is the infective stage and
remains within the egg, which is extremely resistant to environmental

conditions. This resistance, particularly to desiccation, may be one of the
factors allowing these parasites to survive in the Arctic.
(c) Impacts. The effects of Trichuris spp. infections on free-ranging arctic
ungulates are not known but low-intensity trichurid infections in captive
muskox calves are often associated with diarrhoea (Seidel and Rowell,
1996).
2.3.1.5. Emerging issues and knowledge gaps

The gastrointestinal nematode fauna of arctic ungulates is generally sparse
with the most species diversity represented by the nematodirines, parasites
well adapted to arctic climates. In recent years, considerable progress has
been made in defining the diversity and host and geographic ranges of the
Trichostrongylina in the arctic ungulates of North America, although much
remains to be done. Fundamental to this progress is recognition of cryptic
species complexes (e.g. T. boreoarcticus and Marshallagia spp.) and the use
of integrated methods that combine diagnostic morphological characters
and DNA-based analyses to develop and refine descriptions and phylog-
enies. Importantly, archived specimens deposited in museum collections
(e.g. Nematodirella, Teladorsagia) have aided in confirming or re-determining
the identity of several species, as well as confirming the presence of cryptic
species (Lichtenfels and Pilitt, 1983a; Hoberg et al., 1999). These collections
are particularly relevant for arctic parasites because of the cost and logistics
of collecting material in the field and the challenges of obtaining specimens
from host species that have become endangered or threatened.
Overall, the trichostrongyline parasites in arctic ungulates appear to
have broad host ranges but there are host-specific patterns of abundance.
For the nematodirines in particular, the role of host species barriers ver-
sus ecological barriers to infection requires further investigation. Examin-
ing the patterns of host and geographic distribution, and perturbations
of these patterns, may provide novel insights into mechanisms of para-
site invasion and establishment (Hoberg et al., 2012). For example, the
presence of large numbers of ‘strongyle’ type eggs in Dall’s sheep in the
Richardson Mountains is unusual and may reflect the unique interactions
of sheep with muskoxen and caribou in this region. The absence of O.
gruehneri, the most common abomasal parasite of Rangifer, from caribou
colonizing parts of Greenland is particularly surprising and may reflect
unique patterns of host and parasite dispersal into these regions, includ-
ing severe host, and perhaps parasite, bottlenecks. Further exploration of
animal movements, natural and anthropogenic, ecological and species
barriers and successes and failures of parasite colonization events will
contribute to theory on parasite invasion and establishment and provide
insight into the potential for new parasite invasions in the Arctic (Hoberg,
2010; Hoberg et al., 2012).
Transmission dynamics of gastrointestinal nematodes will be influ-
enced by the rapidly changing arctic environment (Hoberg et al., 2008b;
Kutz et al., 2009a,b). In general, warmer and longer summers are antici-
pated to facilitate parasite development and transmission, whereas
extreme temperatures may have negative impacts (Kutz et al., 2009b; Hoar
et al., 2012b). The effects of changing winter conditions are currently spec-
ulative – shorter winters may decrease propensity for larval inhibition,
increased snow cover that insulates parasites may improve parasite sur-
vival whereas increased freeze–thaw cycles will reduce parasite survival.
Some endemic parasites may be better equipped to cope and take advan-
tage of changing conditions (e.g. nematodirines), whereas others (perhaps
ostertagiines) may not.
There is growing evidence that, at least for some species, the free-liv-
ing stages of parasites in the North may have sufficiently broad thermal
tolerances (e.g. O. gruehneri) and/or flexibility in development strategies
(e.g. nematodirines and O. gruehneri) to persist under these changing con-
ditions (van Dijk and Morgan, 2010; Hoar et al., 2012b). Larval inhibition
within the host and overwintering of eggs and larvae in the environment
are important strategies for overcoming adverse environmental condi-
tions and can synchronize parasite development with the availability of
susceptible hosts, such as spring-borne young (Eysker, 1993; Sommerville
and Davey, 2002; Cattadori et al., 2005). The different propensity for larval
inhibition in O. gruehneri across its geographic range and in different sub-
species of Rangifer likely reflects selective strategies associated with cli-
matic conditions and host behaviours (Hoar et al., 2012a). Such plasticity
within the species may allow it to maximize its fitness (i.e. transmission)
under a variety of climatic conditions.
Similarly, research on species of Nematodirus in domestic livestock
suggests that selection can drive adaptations in patterns of egg hatching
under different climatic or latitudinal gradients (van Dijk and Morgan,
2010) such that these nematodes may be very well equipped to survive
climate change in the Arctic. The nematodirines are a core, diverse and
neglected yet potentially pathogenic component of the gastrointestinal
parasite fauna of arctic ungulates. An understanding the ecology of these
parasites under the current climate warming conditions is of considerable
importance for the health of arctic ungulates and may provide a novel
insight into the epidemiology of nematodirines in domestic species. These
arctic species remain essentially untouched by the selection pressures of
the livestock production industry and may provide a simpler model for
exploring concepts of importance for nematodirines of domestic host spe-
cies.
Invasions of new hosts or parasites to the Arctic may result from a

variety of factors including natural range expansion through gradual
movements or stochastic events, translocation associated with agriculture
or conservation efforts, or anthropogenic change including climate and
landscape perturbation (Kutz et al., 2009b; Hoberg, 2010; Hoberg et al.,
2012). The gastrointestinal nematode fauna of temperate free-ranging
ungulate species in Canada is considerably more diverse than that of arc-
tic ungulates, the former consisting of a mosaic of endemic and introduced
parasites (Table 2.4) (Hoberg et al., 2001,2008a; deBruyn, 2010). There is
evidence that, given appropriate conditions, some of these species may
be able to invade and persist in high latitude ecosystems (e.g. Waller and
Chandrawathani, 2005; deBruyn, 2010).
Trichostrongylus axei is one such parasite that may have already estab-
lished successfully at arctic latitudes. Trichostrongylus axei is not known
as part of the typical endemic fauna of arctic ungulates in North America
or Greenland but it has been reported from a variety of arctic ungulates
in captivity at southern latitudes and in Fennoscandia, as well as in
domestic sheep in Greenland (Alendal and Helle, 1983; Rose et al., 1984;
Bye, 1987; Bye et al., 1987; Fruetel and Lankester, 1989). It was recently
found in an introduced population of elk in the Yukon (deBruyn, 2010).
Although the original source of T. axei in this population is not known
(i.e. introduced or naturally present in endemic YT ungulates), its pres-
ence in the elk years after their translocation indicates that it is currently
able to circulate in this northern environment. It is a host generalist
and likely to spill-over to moose and caribou in the region, if it has not
already.
A second genus of considerable concern is Haemonchus. Some species
of Haemonchus are pathogenic abomasal nematodes of domestic sheep and
cattle that can spill-over into wild ungulates and cause significant disease
(Hoberg et al., 2004). Both H. contortus and H. placei have been reported
in wild deer from western Canada (Table 2.4)(deBruyn, 2010). Species of
Haemonchus and H. contortus are considered tropical parasites and the
free-living stages are susceptible to both cold and dry conditions and
require a mean monthly temperature of 18°C to persist (Gordon, 1948;
Hoberg et al., 2004). These attributes may explain the absence of endemic
species in North America and current geographic limits of introduced
species in the boreal and temperate zones (Hoberg et al., 2012c). Thus, the
establishment of H. contortus above the Arctic Circle in Sweden is unusual,
although these populations are limited to domestic sheep under intense
management and confinement (Waller and Chandrawathani, 2005). A
high propensity for larval inhibition in the abomasal mucosa, in con-
junction with animal husbandry practices, appear to be key features that
allow it to persist in domestic livestock at these latitudes (Waller et al.,
2004). Semi-domesticated reindeer in Finland have been experimentally
136
Susan J. Kutz et al.
TABLE 2.4 Some gastrointestinal nematode species reported from cervids in western Canada. Adapted from deBruyn (2010)
Parasitee Woodland caribou Mule deer White-tailed deer Black-tailed deer Elk Moose
Abomasum
Haemonchus contortus ABf
Heamonchus placei AB, SK
Marshallagia marshalli AB AB
Mazamastrongylus odocoilei SK AB, SK
Orloffia bisonis (Syn. Ostertagia bisonis) ABa ABa
Ostertagia gruehneri/O. arctica AB, BC
Ostertagia mossi/O. dikmansi SK
Ostertagia ostertagi ABa ABa
Ostertagia sp. ABb
Spiculopteragia boehmi AB AB AB
Teladorsagia boreoarcticus AB, BC
Teladorsagia circumcincta BC AB, BCa,d
Trichostrongylus axei ABa ABb
Small intestine
Cooperia oncophora (Syn. C. surnabada) AB, ABa ABb
Nematodirella alcidis ABb ABb
Nematodirella longissimespiculata ABc
Nematodirus helvetianus AB, ABa ABb
Nematodirus odocoilei AB, BC AB, BCa,d
Nematodirus spathiger AB
Skrjabinema ABb
Trichostrongylus colubriformis AB
Trichostrongylus longispicularis ABb
a Stock (1978).
b Stock and Barrett (1983).
Parasites in Ungulates of Arctic North America and Greenland

c Samuel et al. (1976).
d Walker and Becklund (1970).
e Among the Ostertagiinae, only names for the major morphotype for polymorphic species are included.
f AB = Alberta, BC = British Columbia, SK = Saskatchewan.
Records are from DeBruyn (2010) unless otherwise indicated.
137
infected with H. contortus (Hrabok et al., 2006b) and Haemonchus sp. has
also caused acute disease and death of muskoxen in captivity (Durrell
and Bolton 1957) (MacDonald et al., 1976). The absence of H. contortus
in Greenland sheep may suggest that it was not present in the original
sheep brought to Greenland in 1906 and 1915 from the Faroe Islands and
Iceland (Rose et al., 1984). The fact that Haemonchus is currently absent
from Iceland sheep supports this contention (Gudmundsdottir, 2006).
Whether Haemonchus spp., if introduced, could be maintained in the Arc-
tic by populations of wild ungulates in the absence of domestic livestock
or confinement farming is unknown. If established at arctic latitudes,
Haemonchus could become a serious cause of morbidity and mortality in
wild ungulates.
Spiculopteragia boehmi is another potentially pathogenic, invasive para-
site of note. It is a Eurasian abomasal nematode of red deer that was trans-
located to North America (and globally) and is now found in wild deer
and elk in geographically disjunct regions of western Canada and the USA
(deBruyn, 2010; Rickard et al., 1993). Spiculopteragia is well established in
game ranched reindeer, and probably elk (C. elaphus), in western Canada
and appears to have significant impacts on body condition of these ani-
mals (S. Kutz, unpubl. obs). Range expansion into temperate caribou
populations is expected but establishment at arctic latitudes is uncertain
(deBruyn, 2010).
Gastrointestinal nematodes are well established as production limit-
ing parasites in domestic species and are increasingly recognized as hav-
ing a role in the health and population dynamics of free-ranging hosts
(Hudson and Greenman, 1998; Hudson et al., 1998; Albon et al., 2002).
While our knowledge of the diversity of gastrointestinal nematodes of
arctic ungulates has improved substantially, our knowledge of the ecol-
ogy and impacts of this group of parasites remains superficial for almost
all species except O. gruehneri. For some of these parasites, even the very
basics of the life cycle remain unknown. For the rest, knowledge of the
life cycle and potential impacts is limited to what has been learned from
a few pilot studies or extrapolated from related parasites of domestic
species.
As parasites with considerable plasticity and resilience in their
responses to climatic conditions, some gastrointestinal nematodes of arc-
tic ungulates are likely to continue to thrive under ongoing climate change
(e.g. Nematodirines, Marshallagia), while others may not be as success-
ful (e.g. Teladorsagia, Ostertagia). The transmission dynamics and relative
abundance and impacts of these parasites will be sensitive to shifts in
diversity, abundance and behaviour of host communities, as well as to
invasions of new hosts and parasites. Extirpation of endemic faunas may
be a result of competition with such invasive parasites. Parasite-mediated
competition among hosts may also occur. A knowledge of how historical
ecological conditions have structured the parasite communities and how

parasites currently circulate among hosts will allow us to anticipate how
these communities may respond to invasions of southern hosts and para-
sites and ultimately how that will influence the health and sustainability
of wildlife populations.
2.3.2. Lung and tissue nematodes: Protostrongylidae and

Dictyocaulinae
The Protostrongylidae are pathogenic nematodes of free-ranging and
domestic ungulates and lagomorphs around the world. Higher taxonomy
for this group was established by Boev (1975), Kontrimavichus et al. (1976)
and Carreno and Hoberg (1999). Species of four subfamilies are known
in ungulates across North America (Fig. 2.7). Those that live as adults in
the lungs belong to the subfamilies Muelleriinae, Protostrongylinae and
Varestrongylinae, and those that live as adults in the skeletal muscles or
central nervous system are referred to the Elaphostrongylinae. At high
latitudes of Canada and AK, various protostrongylid species occur in bar-
ren-ground, Grant’s, and woodland caribou, thinhorn sheep, moose, mus-
koxen, and mountain goats (Table 2.5). Protostrongylids have not been
reported from caribou or muskoxen in Greenland; however, Muellerius
sp. (Muelleriinae) is reported from domestic sheep in southern Greenland
(Rose et al., 1984). Parasite species diversity, prevalence, and abundance
vary with host and geographic location.
Among protostrongylid species with lung-dwelling adults, eggs pro-
duced by the females hatch to release first-stage larvae (L1) that move up
FIGURE 2.7 Tissue and lung Strongylida reported from ungulates of arctic North
America, including Greenland.
TABLE 2.5 Tissue and blood nematodes reported from ungulates of arctic North Amer-
ica, including Greenland. Data compiled from available published and grey literature
Host and parasite species State/ province Herd, region or nearest place name
Caribou
Parelaphostrongylus AK Mulchatnaa; Northern Alaska Penin-
andersoni sulaa
YT Porcupinea; Chisanaa
NT Cape Bathursta; Tsiigehtchica; Blue-
nose Westa; Beverlyb
QC/NL Rivière-aux-Feuillesc; Rivière
Georgea,b; Mealy Mountainsa
Parelaphostrongylus NT Hay Riverd
odocoilei
Varestrongylus sp. n. AK Northern Alaska Peninsula, Mulchatnaa
YT Porcupinea
NT Beverlya; Bluenose Easta; Cape
Bathursta; Godlin Lakesa
NL Mealy Mountainsa
Dictyocaulus eckertiae AK Western Arctic, Northern Alaska Pen-
insula and Kenai Peninsulam
QC/NL Rivière Georgee
GL AM herdf
Onchocerca cervipedis AK Mulchatnag
Setaria yehi AK College and Cantwellh (in reindeer,
originally from Nome)
NT Not specifiedi
Dall’s sheep
Parelaphostrongylus AK Central Alaska Ranged; Chugach
odocoilei Mountainsd; Wrangel Mountainsd
YT Farod; Kluane National Parkd; St. Elias
Mountainsd
NT Mackenzie Mountainsd,j
Protostrongylus stilesi AK Alaska Ranged,k; Baird Rangel; Brooks
Rangel; Chugach Mountainsl; Wran-
gel Mountainsd
YT Anvil Mountainsd; Ivaavik National
Parkd; St. Elias Mountainsd
NT Mackenzie Mountainsd,j
Moose
Varestrongylus sp. n. AK Tlikakila River, Lake Clark National
Preservea
Host and parasite species State/ province Herd, region or nearest place name
Dictyocaulus eckerti AK Palmerm
Onchocerca cervipedis AK Tok Rivern; Palmern
YT Variouso
NT Mackenzie Mountains, Mackenzie
Valley p
Setaria yehi AK Unspecifiedi; Fairbanksq; Delta Junc-
tionq
Rumenfilaria andersoni AK Interior including Fairbanks, Tanana
Flats, Kuskokwim River, Seward
Peninsulaq
Muskoxen
Umingmakstrongylus pal- NT Sahtu Settlement Regionr
likuukensis NU West of Kugluktuks,t; Victoria Island
(Lady Franklin Point) u
Varestrongylus sp. n. YT Firth Riverk
NT Aklavika
NU Cambridge Bay v; Thelon Game Sanc-
tuarya
Protostrongylus stilesi AK Eastern North Slopew
YT Northern Yukon x
NT Big Fish River (near Aklavik)y
Dictyocaulus eckerti NU Kitikmeot region z
QC Kuujjuaqaa
Dictyocaulus sp.ae AK Eastern North Slopew
NT Banks Islandab
NU Bathurst Islandac; Thelonad
a Kutz et al. (2007). p S. Kutz, C. Tobac, G. Verocai (unpubl. obs.).
b Lankester and Hauta (1989). q Quist and Beckmen (2011).
c Asmundson and Hoberg (pers. comm.). r S. Kutz, A. Veitch, R. Popko (unpubl. data).
d Jenkins et al. (2005a). s Gunn and Wobeser (1993).
e Fruetel and Lankester (1989). t Hoberg et al. (1995).
f C. Cuyler, R. White, S. Kutz (unpubl. data). u S. Kutz, K. Orsel, G. Verocai (unpubl. obs.).
g G. Verocai, K. Beckmen(i), Hoberg v G. Verocai, S. Kutz, S. Checkley (unpubl. data.).
(unpubl. data). w Afema (2008).
h Dieterich and Luick, (1971). x S. Kutz (unpubl. data).
i Becklund and Walker (1969). y Hoberg et al., (2001).
j Kutz et al. (2001d). z Hoglund et al. (2003).
k Neiland (1972). aa USNPC, 2011.
l Jenkins et al. (2007). ab M. Branigan (unpubl. data).
m K. Beckmen (unpubl. data). ac Gibbs and Tener (1958).
n K. Beckmen, G. Verocai, E. Hoberg (unpubl. data). ad Samuel and Gray (1974).
o P. Merchant (pers. comm). ae Reported as D. viviparus but most likely D. eckerti.
the respiratory tree, are swallowed and passed in the faeces. The adults
of tissue-dwelling species (Elaphostrongylinae) produce eggs that are
deposited in the blood stream and transported to the pulmonary vas-
culature where hatching releases the L1. These migrate into the alveoli,
then follow the same route as larvae of the lung-dwelling species and are
passed in the faeces. First-stage larvae of genera within the Muelleriinae,
Elaphostrongylinae and Varestrongylinae have kinked tails with small
dorsal spines (dorsal-spined larvae – DSL). It is not possible to reliably
differentiate among these genera on the basis of larval morphology alone
(Hoberg et al., 2005); therefore, DNA-based methodologies are required
for definitive identification (Huby-Chilton et al., 2006; Kutz et al., 2007).
The L1 of the Protostrongylinae have straight spike tails, lack dorsal
spines and also cannot be reliably distinguished morphologically at
either the generic or species level (e.g. Boev, 1975). In general, L1 of north-
ern protostrongylids can survive well in the often-harsh external environ-
ment and are characterized by a degree of freeze tolerance but repeated
freeze–thaw cycles, shifts in humidity and exposure to high temperatures
will reduce viability (Forrester and Lankester, 1998; Shostak and Samuel,
1984; Lorentzen and Halvorsen, 1986).
Gastropod intermediate hosts, which are invaded by L1 from ungu-
late faeces, are required for continuation of the life cycle for all Proto-
strongylidae (Anderson, 2000). Development to the infective third-stage
larvae (L3) is completed through a variety of terrestrial and aquatic
gastropod species, but there is a certain degree of host specificity. Lar-
val development rates and success within the intermediate host vary
depending on both parasite and gastropod species and are temperature
dependent. Mammalian hosts become infected when they ingest gas-
tropods harbouring L3 or L3 that have spontaneously emerged from
the gastropods and are present in the environment (Anderson, 2000;
Kutz et al., 2000b).
Adults, eggs and L1 of lung-dwelling species and eggs and L1 of tissue-
dwelling species can cause significant pulmonary damage, notably local-
ized or multifocal granulomatous pneumonia. Moreover, the developing
larvae and adults of species of the Elaphostrongylinae can cause myositis
and neurological disease, with particularly severe disease in ‘aberrant’
host species (Anderson, 2000; Lankester, 2001; Jenkins et al., 2005b).
2.3.2.1. Subfamily Protostrongylinae

The Protostrongylinae is a diverse group of parasites with a cosmopolitan
distribution in ungulates and lagomorphs, although the greatest diver-
sity is seen in Eurasia (Boev, 1975). Several species have been reported in
cervids and bovids from North America, including Orthostrongylus mac-
rotis in mule deer, Protostrongylus frosti in bighorn sheep and P. coburni in
white-tailed deer from northeastern USA (Dikmans, 1935b); only P. stilesi

and P. rushi are present in arctic and subarctic regions.
2.3.2.1.1. Protostrongylus stilesi

Protostrongylus stilesi is a small (males 17.55–20.79mm in length, female
length not established) (Hoberg et al., 2002) and slender lung nematode
found in the lung parenchyma of wild sheep and mountain goats from
North America.
(a) Host and Geographic Distributions. Protostrongylus stilesi is common
in bighorn (Ovis canadensis), Stone’s and Dall’s sheep and mountain goats,
across their ranges (Neiland, 1972; Uhazy et al., 1973; Pybus et al., 1984;
Kutz et al., 2001d; Jenkins et al., 2005a). Based on post-mortem examina-
tions together with faecal surveys where L1 were presumed to be P. stilesi
(P. rushi, although less likely, was not ruled out), prevalence ranges from
50 to 100% in thinhorn sheep herds and 50 to 78% in mountain goat herds
(Jenkins et al., 2006b).
Protostrongylus stilesi is also present at low intensities in an introduced
population of muskoxen (O. m. wardi) that are sympatric with Dall’s sheep
in northern YT and northwestern NT (Hoberg et al., 2002), and L1 typical
of Protostrongylus sp. are present in introduced muskoxen that are sym-
patric with Dall’s sheep in western AK (L. Adams, K. Beckmen, unpubl.
obs.). The occurrence of P. stilesi in muskoxen is considered a recent host
switch associated with anthropogenic breakdown of ecological barriers in
conjunction with climate change (Hoberg et al., 2002). Following histori-
cal extirpation, muskoxen were introduced to the Arctic Coastal Plain of
AK in the late 20th century. Later expansion of this population to the east
along the northern shoulder of the Brooks Range has resulted in intermit-
tent sympatry with Dall’s sheep and consequent infection with P. stilesi.
Although infections in muskoxen become patent, larval shedding is low
and it is unknown whether P. stilesi would be maintained in the absence of
Dall’s sheep (Hoberg et al., 2002; Kutz et al., 2004b).
(b) Ecology. The life cycle of P. stilesi is similar to other pulmonary
protostrongylids. Larvae of bighorn sheep origin developed to L3 within
11–60 days in several gastropod genera, including Pupilla, Vallonia, and
Vertigo (Pillmore, 1956; Monson and Post, 1972) and those of Dall’s sheep
origin developed to L3 within 34 days in experimentally infected wild-
caught pupillid snails (Vertigo and Columella spp.) at room temperature
(mean 22°C) (E. Jenkins and J. Skific pers. comm.). Emergence of small
numbers of L3 from gastropod intermediate hosts occurs and although
it is not considered an important feature of the parasite’s epidemiology
in bighorn sheep (Monson and Post, 1972), it may be more important in
the Arctic, extending transmission into winter. Third- and fourth-stage
larvae have been recovered from foetuses and neonatal bighorn lambs,
suggesting that transplacental transmission occurs (Forrester and Senger,

1964; Hibler et al., 1972). The prepatent period in a single experimentally
infected Dall’s sheep was 45 days (E. Jenkins and J. Skific pers. comm.)
and the finding of P. stilesi adults in Dall’s lambs as young as two months
suggests either infection very early in life or that transplacental transmis-
sion might also occur in thinhorn sheep (Jenkins et al., 2007). First-stage
protostrongylid larvae, not identified to subfamily, were also observed in
the bronchi of a wild Dall’s foetus from AK at the end of April (K. Beck-
men, K. Burek, unpubl. obs.). These may be a result of haematogeneous
spread of L1 from the dam, which is unlikely in the case of the Protostron-
gylinae but perhaps more likely for Parelaphostrongylus odocoilei or a patent
infection with species of either genus.
In Dall’s sheep in the Mackenzie Mountains, NT, larval production
tends to be seasonal, with prevalence lowest in August and increasing
through the fall and intensity also increasing through fall and winter and
peaking in the spring (annual range of 32–1075 LPG) (Jenkins et al., 2006b).
Development and transmission of P. stilesi under arctic conditions have
not been investigated in any detail; however, using a degree–day model
for protostrongylid development (Kutz et al., 2002), Jenkins et al. (2005b)
suggested that L3 might not develop in a single summer at arctic latitudes.
The authors hypothesized that freeze tolerance of L1, overwintering of
larvae in gastropods, transplacental transmission and L3 emergence may
all contribute to the persistence of this parasite at arctic latitudes (Jenkins
et al., 2006b).
(c) Impacts. In naturally infected Dall’s sheep, P. stilesi can cause severe
verminous lesions in the lung parenchyma associated with adults, larvae
and eggs. Grossly, there are firm, pale, coalescing lesions of 5–70mm in
diameter primarily along the caudodorsal border of the diaphragmatic
lobe, but also in other lobes, and it is estimated that, in heavy infections,
up to 36% of the lung volume can be compromised (Neiland, 1972; Kutz
et al., 2001d). Histologically, there are focal aggregations of inflammatory
cells surrounding adult nematodes and immature stages, as well as fibro-
sis, bronchiolar hyperplasia and mild fibrino-haemorrhagic exudate (Kutz
et al., 2001d). In muskoxen, lesions are located in the caudodorsal and dia-
phragmatic surfaces of diaphragmatic lobes, are round to oval (3–5mm),
tan to red brown, extending into the lung parenchyma and contain adults,
ova and larvae of the parasite. Histologically, adults are confined to alveo-
lar parenchyma and surrounded by mild to focally marked lymphocyte/
macrophage infiltrate (Hoberg et al., 2002). Pathology is not described in
mountain goats.
The effects of P. stilesi in Dall’s sheep at a population level remain
unknown. Historically, P. stilesi was considered an important pathogen in
bighorn sheep and linked to the lungworm–pneumonia complex. Subse-
quent studies suggest, however, that while lungworms might predispose
to other pneumonias, their effects on the individuals and populations of

this host species may be more subtle and indirect (Festa-Bianchet, 1991).
Of possible significance with respect to Dall’s sheep is that, across their
central and southern range, they may be co-infected with the muscleworm
P. odocoilei. Eggs and larvae of P. odocoilei cause significant pulmonary
damage and co-infections could result in additive or synergistic pulmo-
nary damage (Kutz et al., 2001d; Jenkins et al., 2007).
2.3.2.1.2. Protostrongylus rushi

Adults of P. rushi are larger (males 18–32mm, females about 38mm in
length) than P. stilesi and are found in the trachea, bronchi, and larger bron-
chioles. Protostrongylus rushi has been reported in a Dall’s sheep from the
YT based on a single museum specimen (CMNP 1988-0522) (Kutz et al.,
2001d) and in mountain goats at Mt. Juneau and adjacent to Haines, AK
(USNPC 100426, 105139). It also occurs in bighorn sheep from the Cana-
dian Rocky Mountains (Uhazy et al., 1973) and mountain goats from cen-
tral BC (Jenkins et al., 2004). However, the true geographic range of this
parasite in the Arctic remains unknown. Although adults of P. stilesi and
P. rushi are easily differentiated, the L1 are morphologically very similar
and require DNA-based analyses for identification (e.g. Kutz et al., 2007).
Further survey and inventory are necessary to determine the geographic
distribution of P. rushi in Dall’s sheep and mountain goats and its potential
significance in these caprines.
2.3.2.2. Subfamily Muelleriinae

Members of the Muelleriinae are a monophyletic group of typically cyst-
forming lungworms of the Caprinae and include the genera Muellerius,
Cystocaulus, and Umingmakstrongylus (Carreno and Hoberg, 1999). Uming-
makstrongylus pallikuukensis is the only species of the subfamily endemic to
North America. Muellerius capillaris is a cosmopolitan parasite of domes-
tic sheep and goats that was introduced to North America with domestic
livestock (Anderson, 2000) and has since spilled over to bighorn sheep
(Pybus and Shave, 1984; Ezenwa et al., 2010). Species of Cystocaulus have
distributions in Eurasia and although this genus is the sister of Umingmak-
strongylus, it has not been reported in North America.
2.3.2.2.1. Umingmakstrongylus pallikuukensis

Umingmakstrongylus pallikuukensis is a large (males up to 22cm and females
to 65cm long), cyst-forming, pulmonary nematode specific to muskoxen
(Kutz et al., 1999). It was first discovered west of Kugluktuk, NU, in 1988
(Gunn and Wobeser, 1993; Hoberg et al., 1995).
(a) Host and Geographic Distributions. In the late 1990s, U. pallikuuken-

sis was present at near 100% prevalence in muskoxen on the western
Canadian mainland between the Mackenzie and Coppermine rivers and,
despite extensive survey, was not found in muskox populations elsewhere
(Gunn and Wobeser, 1993; Hoberg et al., 1995; Kutz, 2000). Recently, it has
been detected on Victoria Island, NU, and east of the Coppermine River,
suggesting significant range expansions (S. Kutz, K. Orsel, M. Dumond,
G. Verocai unpub. obs.). It has not been found in sympatric caribou and
did not establish in experimentally exposed Dall’s/Stone’s sheep hybrids
or domestic sheep (Kutz et al., 1999 ; Kutz et al., 2004a).
(b) Ecology. Umingmakstrongylus pallikuukensis follows a typical proto-
strongylid life cycle with temperature dependent development in gastro-
pod intermediate hosts. In the core of the parasite’s range on the Canadian
mainland, the meadow slug, Deroceras laeve, appears to be the most abun-
dant intermediate host but larvae can also develop to L3 in at least two
(Catinella sp. and Euconulus fulvus) of the five terrestrial species and one
(Aplexa hypnorum) of the four aquatic species present in the area. The lar-
val development period in experimentally exposed D. laeve ranges from 9
days at 23.4°C, to 42 days at 11.5°C (Kutz et al., 2001c; Kutz et al., 2002) and
the prepatent period (PPP) in experimentally infected captive muskoxen
is 91–95 days (Kutz et al., 1999).
Umingmakstrongylus pallikuukensis appears to be an exceptionally well
adapted, single host, arctic parasite: it is large, long lived (at minimum two
years and likely much longer) and highly fecund (up to 3 million L1/day
in experimentally exposed muskoxen with adult parasite burdens similar
to those observed in the field); L1 are resistant to freezing and desicca-
tion and develop rapidly and efficiently in a gastropod intermediate host
species that is relatively abundant and vagile; up to 100% of L3 emerge
from the gastropods suggesting the possibility of year-round transmission
and infection accumulates with age and causes minimal inflammatory
response in muskoxen (Kutz et al., 1999; Kutz, 2000; Kutz et al., 2001b).
Where it is present, prevalence approaches 100% in the affected popu-
lation and calves are infected in their first summer (Gunn and Wobeser,
1993; Kutz et al., 2001b).
The restricted geographic distribution of U. pallikuukensis likely reflects
a history of near extirpation of muskoxen in the early 1900s as well as
limiting historical climatic conditions (Hoberg et al., 1995; Hoberg et al.,
2008a). Empirical models suggest that between 1973 and 2002, concurrent
with regional warming, larval development within the intermediate host
reached a tipping point, shifting from a two- to one-year period. This
shift in development rate would have a considerable influence on infec-
tion pressure and transmission dynamics and range expansion under
the current regime of climate warming was predicted (Kutz et al., 2005).
Consequently, the recent finding of U. pallikuukensis on Victoria Island,
a large arctic island separated from the mainland by Coronation Gulf,

is a substantial range expansion (Kutz et al., 2009b). A broadened range
reflects a permissive climate, presence of suitable gastropod intermediate
hosts and an event for expansion and establishment most likely medi-
ated through infrequent muskox movement between the mainland and
the island.
(c) Impacts. Adult parasites inhabit spherical to ovoid grey–brown
cysts of up to 4cm in greater diameter, containing up to… 5–7 adult
worms. Cysts are located throughout the lung parenchyma and some are
easily visible and palpable. Histologically, cysts consist of a wall of con-
nective tissue surrounding adult worms, together with numerous eggs,
L1 and amorphous debris (Hoberg et al., 1995; Kutz et al., 1999). Some
cysts are calcified, which is thought to indicate long-standing infection
and some contain no adult parasites. There is little inflammatory reaction
outside the region directly adjacent to the cysts. Cysts appear to accumu-
late with age and naturally infected older bulls may contain up to 250
(Gunn and Wobeser, 1993). On radiographic examination cysts are vis-
ible as opacities and are also clearly evident on computed tomography
(Kutz et al., 1999).
The population-level impacts of an endemic infection with U. palli-
kuukensis, or the introduction to a naive population such as that on Vic-
toria Island, remain poorly understood. There are anecdotal reports of
epistaxis in free-ranging muskoxen that have been stressed by running,
and one infected captive muskox demonstrated epistaxis when restrained
on a bovine examination tilt table. Conceivably, the parasites may have
significant energetic costs for heavily infected muskoxen and the pathol-
ogy may lead to exercise intolerance and increases in susceptibility to
predation.
2.3.2.3. Subfamily Varestrongylinae

The Varestrongylinae is composed of a number of species within the gen-
era Varestrongylus and Pneumostrongylus. These are small lungworms typi-
cally found in the terminal bronchioles of cervids and bovids across the
Holarctic (Boev, 1975). In North America, two species are known, V. alpe-
nae in white-tailed deer and a recently discovered species, Varestrongylus
sp. n., in caribou, muskoxen and moose; only the latter species is reported
from the Arctic (Kutz et al., 2007).
2.3.2.3.1. Varestrongylus sp. n.

Varestrongylus sp. n. is a miniscule lungworm (1–2cm) found deep in the
airways or parenchyma of the lungs. Taxonomic description of this para-
site is in progress (G. Verocai, E. Hoberg, M. Simard, S. Kutz, unpubl. obs.).
(a) Host and geographic distributions. Varestrongylus sp. n. has a broad

host and geographic range, naturally infecting muskoxen (O. m. moscha-
tus and O. m. wardi), woodland, Grant’s and barren-ground caribou, and
rarely, moose across most of arctic and subarctic North America (Kutz
et al., 2007). Unidentified DSL previously found in woodland caribou in
several Canadian provinces may also be from this species (Lankester et al.,
1976; Gray and Samuel, 1986; Lankester and Fong, 1998; Kutz et al., 2007)
but further investigations are required.
Varestrongylus sp. n. occurs in co-infections with Parelaphostrongylus
andersoni in some barren-ground caribou herds and with P. odocoilei in
woodland caribou from western Canada (Kutz et al., 2007). Co-infections
with P. stilesi in muskoxen are probable (Hoberg et al., 2002; L. Adams, K.
Beckmen, unpubl. obs.), as are co-infections with U. pallikuukensis; how-
ever, the latter would be difficult to detect. The substantial lesions caused
by U. pallikuukensis may obscure the more subtle changes caused by the
Varestrongylus. Similarly, molecular detection based on DSL from faeces
may be confounded by massive larval production from U. pallikuukensis,
which may obscure the less abundant L1 of Varestrongylus (Kutz et al.,
2007).
(b) Ecology: Varestrongylus sp. n. follows the typical protostrongylid life
cycle. It was found in a naturally infected slug, Deroceras laeve, from the
NT (Kutz et al., 2007) and in preliminary studies developed to L3 in both
D. laeve and Deroceras reticulatum (G. Verocai, S. Kutz unpubl. obs.). The
prepatent period, pathology and impacts of this parasite in its hosts are
not known: gross lesions have not been observed in lungs from a small
number of naturally infected muskoxen and caribou (G. Verocai, S. Kutz
and M. Simard unpubl. obs.).
2.3.2.4. Subfamily Elaphostrongylinae

The Elaphostrongylinae consist of two genera with a minimum of six
species, two of which occur in arctic ungulates of North America. Spe-
cies of the genus Parelaphostrongylus are native to North America whereas
Elaphostrongylus is a Palaearctic genus. A single species, E. rangiferi, intro-
duced to northeastern North America through reindeer translocations
from Eurasia is restricted to Newfoundland (Lankester, 2001).
2.3.2.4.1. Parelaphostrongylus andersoni

Parelaphostrongylus andersoni is a muscle-dwelling nematode of white-
tailed deer (O. virginianus) and caribou, with males measuring 19–23mm
and females around 30–35mm. It can cause significant muscular and pul-
monary disease in these hosts. Despite this pathogenicity and its broad
distribution, little is known about the ecology and impacts at the popula-
tion level in its main arctic host, the caribou.
(a) Host and Geographic Distribution: White-tailed deer are considered

the primary hosts, with caribou colonized by host switching during the
Pleistocene (Carreno and Lankester, 1994; Asmundsson et al., 2008). Adult
nematodes were first found in caribou from central and eastern Canada,
including Newfoundland and it was presumed that DSL in caribou across
their range were P. andersoni (Lankester and Hauta, 1989; Lankester and
Fong, 1998; Ball et al., 2001). Recent molecular identification of DSL in
several barren-ground and woodland caribou herds has confirmed the
presence of P. andersoni and supports the hypotheses that this parasite
has a continuous distribution in barren-ground caribou across their arctic
range (Kutz et al., 2007). Despite sympatry of infected caribou herds with
various populations of muskoxen, moose and Dall’s sheep, P. andersoni
has not been detected in these other ungulate species (Jenkins et al., 2005a;
Kutz et al., 2007).
(b) Ecology: The life cycle of P. andersoni is typical of protostrongylids.
Parelaphostrongylus andersoni successfully developed to L3 in gastropod
intermediate hosts Triodopsis sp. and Mesodon sp. within 3–4 weeks under
laboratory conditions at 20–26°C (Pybus and Samuel, 1984a; Lankester
and Hauta, 1989) and was reported from wild Mesodon spp. and D. laeve
(Lankester and Fong, 1998; Anderson, 2000). In these studies, however,
larval identity was not confirmed using DNA-based techniques. Deroc-
eras laeve is considered one of the most important natural intermediate
hosts for P. andersoni in Newfoundland (Lankester and Fong, 1998) and is
found across most, if not all, the mainland North American caribou range
(Pilsbry, 1946; Kutz et al., 2000b; Grimm et al., 2009). Emergence of L3
from gastropods has not been investigated for P. andersoni. The prepatent
period in a single experimentally infected female caribou calf given 385
L3s was 66 days (Lankester and Hauta, 1989) and was within the range of
that reported for other cervid hosts (49–75 days) (Prestwood, 1972; Pybus
and Samuel, 1984b; Lankester et al., 1990). The migratory path of P. ander-
soni within the ungulate host has not been fully described.
The patent period for P. andersoni in experimentally infected caribou
and white-tailed deer appears to be quite short. In the only experimen-
tally infected caribou calf (given 295 L3 followed by 85 L3 14 days later),
Lankester and Hauta (1989) reported a low peak of 124 LPG of faeces two
weeks after patency (66dpi) followed by a significant drop to 7 LPG of
faeces by 32 days after patency. A similar pattern was observed in white-
tailed deer, with larval shedding peaking in 2–8 weeks post-patency
and then declining (Nettles and Prestwood, 1976; Pybus and Samuel,
1981). Higher larval output, longer peaks (12 weeks post-patency) and
longer periods of patency were observed in white-tailed deer fawns
experimentally infected with higher doses of L3 (1,000L3) (Pybus and
Samuel, 1984b). A short patency for P. andersoni in caribou was sup-
ported by data from naturally infected caribou in Newfoundland, where
its co-occurrence with E. rangiferi and a putative cross-immunity seem

to decrease larval output of both elaphostrongylines. Also, in two cari-
bou herds in which P. andersoni occurred alone, larvae were found only
in small faecal pellets considered to be from calves and yearlings, and
larger pellets were DSL-negative (Ball et al., 2001). These data support
the fact that P. andersoni has a short patency period in caribou and is pri-
marily in young animals, although association of faecal pellet size with
caribou age should be interpreted cautiously. Notably, L1 of P. andersoni
have been confirmed based on molecular sequence data in adult barren-
ground caribou from several different herds (Kutz et al., 2007; G. Verocai,
S, Kutz, unpubl. obs.).
(c) Impacts: Adult nematodes, eggs and larvae of P. andersoni can cause
significant pathology in the skeletal muscles and lungs, respectively, and
clinical signs can be severe. Adult nematodes are found predominantly in
the skeletal muscles, typically in the longissimus dorsus and psoas, but
can also be found in other muscles and fat (Prestwood, 1972; Nettles and
Prestwood, 1976; Pybus and Samuel, 1981; Lankester and Fong, 1998).
Gross pulmonary lesions associated with the presence of eggs and L1
include petechial haemorrhages and whitish nodules and are similar to
those found in white-tailed deer (Lankester and Hauta, 1989; Lankester
and Fong, 1998). In naturally and experimentally infected caribou, lesions
associated with adult parasites include diffuse haemorrhage in the region
of the lower neck and back, tight muscles and fasciitis (Lankester and
Hauta, 1989).
In deer experimentally infected with a large number of L3 (5000), clini-
cal signs include included pain in the loin muscles, reluctance to stand,
weakness, marked discomfort in walking and falling to the ground fol-
lowing light pressure on the loin muscles (Nettles and Prestwood, 1976).
Based on clinical signs in experimentally infected deer, this degree of
pathology probably compromises the mobility in naturally infected
caribou. Moreover, co-infections with other common pulmonary nema-
todes such as Varestrongylus and Dictyocaulus might have an additive or
synergistic effect leading to more severe verminous pneumonia.
2.3.3.4.2. Parelaphostrongylus odocoilei

Parelaphostrongylus odocoilei is a muscle-dwelling protostrongylid common
in subspecies of O. hemionus (mule, Columbian black-tailed and Sitka black-
tailed deer) and Dall’s and Stone’s sheep and is occasionally reported from
mountain goats, bighorn sheep and woodland caribou (Table 2.5). The adult
nematodes have a size range from 24 to 33mm for males and 44 to 56mm
for females and typically occur in skeletal muscles, primarily of the back,
hind limbs, forelimbs and trunk but can be found elsewhere (Hobmaier
and Hobmaier, 1934; Pybus and Samuel, 1984b; Kutz et al., 2001d).
(a) Host and Geographic Distributions: Parelaphostrongylus odocoilei was

described originally in mule deer and it occurs in this species through-
out western North America from California to southeastern AK (Hobma-
ier and Hobmaier, 1934; Brunetti, 1969; Platt and Samuel, 1978; Samuel
et al., 1985; Lankester, 2001; Mortenson et al., 2006). It is common and
widespread in thinhorn sheep south of the Arctic Circle with prevalence
approaching 100% in most infected populations (Jenkins et al., 2005a).
It has not been found in Dall’s sheep from the Richardson Mountains
(YT, NT) or the Brooks Range (YT, AK) despite extensive faecal surveys
(Jenkins et al., 2005a ; Jenkins et al., 2007) (E. Hoberg, I. Asmundsson,
K. Beckmen unpubl. obs). It occurs in mountain goats in BC, NT and AK
(Jenkins et al., 2004). DSL are also reported from this host in AB and Wash-
ington State, USA, but have not been conclusively identified (Pybus and
Samuel, 1984a).
The distribution of P. odocoilei in caribou is less well understood and
there exist only two confirmed reports. A single DSL in a woodland caribou
from the Hay River region, NT, was identified as P. odocoilei by molecular
characterization (Jenkins et al., 2005a) and adult nematodes were recov-
ered from skeletal muscles of mule deer experimentally infected with DSL
from faeces of mountain woodland caribou from Jasper National Park,
AB (Gray and Samuel, 1986). These authors hypothesized that it could be
well established in other woodland caribou populations sympatric with
mule deer in AB and BC but to date this has not been confirmed despite a
moderate level of surveillance using DNA-based techniques (Kutz et al.,
2007; G. Verocai, S. Kutz unpubl. obs.).
Moose can be experimentally infected with P. odocoilei (Platt and Sam-
uel, 1978), but the parasite has not been found in faecal surveys of moose
sympatric with infected deer and/or thinhorn sheep in the YT, the Sahtu
Settlement Region NT, northeastern BC, or AK (Kutz et al., 2007). Parela-
phostrongylus odocoilei has not been reported in muskoxen, but nowhere is
this potential host sympatric with infected Dall’s sheep or mule deer.
(b) Ecology: The life cycle of P. odocoilei is similar to that of other tissue-
dwelling protostrongylids. Adults in the skeletal muscles are closely asso-
ciated with blood and possibly lymphatic systems, where females deposit
eggs that are carried to the lungs. A number of different arctic gastropod
species have been reported naturally or experimentally infected with lar-
vae of P. odocoilei, including D. laeve, Catinella spp. and Euconulus cf. fulvus,
but not members of the Pupillidae (Jenkins et al., 2006a) (Lankester, 2001).
As with many other protostrongylids of northern ungulates, D. laeve is
considered the most important intermediate host because of its abun-
dance, susceptibility and higher prevalence of infection in nature, when
compared to other gastropods (Samuel et al., 1985). In the laboratory,
development in D. laeve occurs in as few as 10 days at approximately 24°C
and L3 can develop within a single summer in experimentally infected D.

laeve in the Mackenzie Mountains, NT (Jenkins et al., 2006a).
Emergence of L3 from D. laeve occurs in the laboratory with approxi-
mately one-third of the total larvae emerging from days 22 to 60 post-infec-
tion at room temperature. Emerged L3 survive up to six months in darkness
in water at near-freezing temperatures. Emergence also occurs to a lesser
extent in Catinella sp. (Jenkins et al., 2006a). Emerged L3 might play an impor-
tant role in overwinter transmission when gastropods are not available, as
postulated for U. pallikuukensis (Kutz et al., 2000b; Jenkins et al., 2006a).
The prepatent period in three Stone’s sheep and two thinhorn hybrids
(O. d. stonei × O. d. dalli) each given 200 L3 from a Dall’s sheep source
ranged from 68 to 74 days (Jenkins et al., 2005b), up to 1–3 weeks longer
than that reported for mule and black-tailed deer infected with deer-source
P. odocoilei (Pybus and Samuel, 1984b). Larval shedding early in patency
was high, peaking at 14,000–30,000 LPG between 95 and 109dpi. Larval
counts remained high (1700–4800 LPG of dry faeces) and patency lasted
for a minimum of 180dpi at which point the animals were removed from
the study (Jenkins et al., 2005b).
In the Mackenzie Mountains, NT, larvae of P. odocoilei were present in
84–100% of Dall’s sheep faeces sampled from March 2000 to April 2003.
Intensity ranged from 141 to 1350 LPG through the year with larval pro-
duction peaking from March through May. There was no evidence of
age-related immunity (Jenkins et al., 2006b). Experimentally infected
D. laeve maintained in natural conditions in the Mackenzie Mountains
yielded high numbers of L3 by August–September. It is hypothesized
that the majority of transmission might happen on the winter range,
with infection of gastropods once they emerge from hibernation in
spring and definitive host infection when the sheep return during fall
(Jenkins et al., 2006b).
The apparent absence of P. odocoilei in Dall’s sheep and other potential
host species from the Richardson Mountains and Brooks Range may result
from a combination of historical, climatic, physical and species barriers.
The parasite does not appear to have expanded from refugial habitats with
its hosts at the termination of the Pleistocene, a factor which may explain
current absence at high latitudes north of the Alaska Range (Schafer et al.,
2010; Hoberg et al., 2012). Outcomes using a degree–day model for devel-
opment in gastropod intermediate hosts suggest that temperature-related
constraints on development might limit establishment of P. odocoilei in
naïve Dall’s sheep populations at the northern extent of their range (Jen-
kins et al., 2006b). Under current climate warming scenarios, however, the
‘Arctic-adapted’ characteristics of P. odocoilei, including freeze tolerance of
free-living stages, high prevalence and larval production in Dall’s sheep,
larval emergence, high establishment and development rates in gastropod
intermediate hosts, could allow it to persist if introduced into currently

non-endemic areas.
Introduction of P. odocoilei to the northern sheep ranges is unlikely to
be mediated through movement of sheep. Dall’s sheep are restricted to
mountain ranges and are not likely to disperse across vast expanses of tun-
dra or forest to colonize new mountain habitats, a hypothesis supported
by evidence of population fragmentation found in phylogeographic stud-
ies (Loehr et al., 2006). Caribou in contrast are much more vagile and
conceivably could bridge the gap between mountain ranges during their
annual migrations and introduce the parasite to Dall’s sheep and muskox
populations further north. The potential suitability of caribou as mainte-
nance hosts for this parasite, however, remains enigmatic (see previous
discussion). Muskoxen conceivably could also serve a role in maintenance
and expansion of P. odocoilei between mountain ranges and Dall’s sheep
populations but susceptibility of this species is unknown. Considerably
more research is needed to understand the ecology and transmission
dynamics of P. odocoilei in this system and the potential for it to emerge
further north.
(c) Impacts: Parelaphostrongylus odocoilei is a significant pathogen in
Dall’s sheep, causing parasitic pneumonia and sporadic mortality events
in the wild (Jenkins et al., 2007), as well as weight loss, muscle atrophy
and neurological disease following experimental infection (Jenkins et al.,
2005b). The neurological symptoms developed two weeks before patency
and included ataxia of the hind legs, loss of conscious proprioception
and hyperaesthesia, all of which resolved at patency. Pybus and Samuel
(1984a,b) found adult nematodes and eggs in epidural fat of the spinal
cord in deer and Jenkins et al. (2005b) detected eosinophilic pleocytosis
and antibody to Parelaphostrongylus spp. in the cerebrospinal fluid of the
experimentally infected animals, suggesting that this parasite migrates
through the central nervous system of thinhorn sheep. Haematogeneous
spread of eggs and larvae of P. odocoilei to the lungs during patency causes
significant pulmonary pathology manifested as a disseminated granulo-
matous pneumonia.
The neuromuscular pathology caused by P. odocoilei may enhance sus-
ceptibility to predation or accidents (e.g. falling off cliffs in the sheep’s
natural habitat) for animals with moderate to heavy natural infections
(Jenkins et al., 2005b). Importantly, the parasite is quite small and dif-
ficult to detect, so mortality events associated with the adult stages may
be misdiagnosed as accidents or predation. Pulmonary failure due to P.
odocoilei was the cause of mortality in a 10-month-old, naturally infected
Dall’s lamb (S. Kutz, E. Jenkins, B. Elkin, A. Veitch unpubl. data) and
was a contributing factor in the deaths of other thinhorn sheep in the
wild (Jenkins et al., 2007). In Dall’s sheep, P. odocoilei commonly co-
occurs with P. stilesi, a pulmonary protostrongylid (Jenkins et al., 2006a).
These two species cause very different pulmonary pathology: P. odocoilei

diffuse granulomatous pneumonia and P. stilesi locally severe granulo-
matous pneumonia usually in the caudodorsal regions of the lungs. Co-
infections, therefore, might lead to additive pathology and more severe
disease.
2.3.2.5. Emerging issues and knowledge gaps for the Protostrongylidae
2.3.2.5.1. Potentially invasive protostrongylids

In addition to the protostrongylid fauna discussed above, there are a num-
ber of potentially invasive species at temperate latitudes. Shifts in climate
and landscape structure, changes in arctic ecosystems, translocations of
domestic species and translocations/reintroductions of, and invasions by,
free-ranging hosts, might facilitate northward range expansion of some of
these species (e.g. Kutz et al., 2009a,b; Hoberg, 2010). Among the species
of protostrongylids that are likely to invade and have significant conse-
quences are O. macrotis (Protostrongylinae); M. capillaris (Muelleriinae);
Varestrongylus alpenae (Varestrongylinae) and Parelaphostrongylus tenuis
and Elaphostrongylus rangiferi (Elaphostrongylinae).
Orthostrongylus macrotis is found in the trachea and bronchi of mule and
black-tailed deer and pronghorn (Antilocapra americana) in the western US
and southwestern Canada (Boddicker and Hugghins, 1969; Greiner et al.,
1974; Pybus, 1990; Belem et al., 1993). It is also reported rarely from moose
(Samuel et al., 1976) and elk (Honess and Winter, 1956). Northward range
expansion of mule deer may bring this parasite into sympatry with ungu-
lates in subarctic and arctic environments (deVos and McKinney, 2007;
Wilson, 2009). The literature on this lungworm is sparse and consequently
its ecology, pathology and impacts on hosts, as well as its potential for
invasion into northern ungulates, are unknown.
Muellerius capillaris is an important lung nematode of domestic sheep
and goats. It has spilled over to bighorn sheep in some regions of Canada
and the United States (Ezenwa et al., 2010). It has not been reported in
free-ranging Dall’s sheep or muskoxen from North America but is found
in muskoxen in Norway (S. Kutz, B. Ytrehus, G. Verocai, unpubl. obs.).
Suitable gastropod species are present in the Arctic and Subarctic to sup-
port development of M. capillaris, and this parasite has a lower thresh-
old for development but it has a degree–day requirement similar to U.
pallikuukensis (Kutz et al., 2001c). It is likely, therefore, that if introduced,
environmental conditions and intermediate host diversity and abun-
dance would be suitable for establishment of M. capillaris. Ongoing and
new commercial or hobby farming activities of sheep adjacent to muskox,
Dall’s sheep or mountain goat range could lead to spill-over of this para-
site to free-ranging hosts.
Varestrongylus alpenae. This is a pulmonary lungworm of white-tailed

deer in the eastern USA and southeastern and southcentral Canada, co-
occurring with P. tenuis and P. coburni (Dikmans, 1935b; Cheatum, 1951;
Gray et al., 1985). This species was linked to fatal pneumonia white-tailed
deer in northwestern USA (Cheatum, 1951). The susceptibility of arctic
ungulates to this parasite is not known; examination of woodland caribou
and moose in central and eastern Canada that are sympatric with infected
white-tailed deer may provide new insights.
Parelaphostrongylus tenuis. This is also a parasite of white-tailed deer
and causes severe neurologic disease in several other ungulate species,
including reindeer, caribou and moose (Lankester, 2001). This species is
widely distributed in white-tailed deer throughout eastern North Amer-
ica; in Canada, the western limit of its range is eastern Saskatchewan.
Parelaphostrongylus tenuis is considered a significant factor for failure of
caribou reintroductions in eastern Canada and Minnesota, USA, where
caribou were placed in areas sympatric with, or previously occupied by,
white-tailed deer (Trainer, 1973; Dauphiné Jr., 1975; Pitt and Jordan, 1994).
Climate and landscape changes are leading to a northward range
expansion of white-tailed deer and their parasites (Thompson et al., 1998;
Côté et al., 2004; Latham et al., 2011) but the potential for P. tenuis to sur-
vive and be transmitted at northern latitudes is currently unknown. This
will depend on both deer ecology and densities since white-tailed deer
are requisite for its maintenance (all other cervids are essentially dead-
end hosts or produce very few larvae that subsequent transmission is
unlikely), as well as the ability of larvae to develop and survive in subarc-
tic and arctic environments. Parelaphostrongylus tenuis is a risk to existing
woodland caribou and moose populations elsewhere in eastern Canada
(Lankester et al., 2007) and investigation of host–parasite dynamics at the
interface of these species may provide additional understanding of poten-
tial risks and implications for invasion of the Arctic.
Elaphostrongylus rangiferi. This is a common parasite of wild and semi-
domesticated reindeer (Rangifer tarandus tarandus) in Palaearctic regions
(Fennoscandia and Russia). It causes cerebrospinal elaphostrongylosis
(CSE) in Rangifer and experimentally infected moose (Lankester, 1977;
Lankester and Northcott, 1979; Stéen et al., 1997; Lankester and Fong,
1998). It is a probable cause of a similar clinical disease in muskoxen in
Norway (Holt et al., 1990).
Elaphostrongylus rangiferi was introduced into Newfoundland with
infected reindeer from Norway in 1908 and is now well established in
woodland caribou across the island. Despite several opportunities for
translocation of E. rangiferi to North America with multiple other rein-
deer introductions (e.g. Lankester and Fong, 1989) the parasite has not
been detected in extensive faecal-based geographic surveys of caribou
and muskoxen on most of Canada’s mainland (Huby-Chilton et al., 2006;
Kutz et al., 2007; G. Verocai, E. Hoberg, I. Asmundsson, S. Kutz unpubl.

obs.). Nor has it been detected in western AK, where the majority of the
introduced reindeer from Russia and Norway were established and are
now maintained as a commercial livestock activity (Oleson, 2005; Finstad
et al., 2006). Clinical disease has not been detected in the semi-domesti-
cated reindeer or adjacent free-ranging caribou herds; however, clinically
affected animals may quickly succumb to predation and with abundant
scavengers and a rare human presence carcasses are unlike to be detected.
Even the semi-domesticated reindeer are free ranging over a wide geo-
graphic, sparsely populated area and are rarely observed except during
brief annual handlings for deworming. There have also not been any spe-
cific survey with subsequent larval identification for protostrongylids in
this area, so the presence of E. rangiferi associated with reindeer herds in
AK cannot be ruled out.
The possibility remains that E. rangifer has established elsewhere in
North America but remains undetected. Deroceras laeve is a suitable inter-
mediate host (reviewed in Lankester, 2001) and is common and wide-
spread across most of mainland arctic and subarctic Canada (Pilsbry,
1946). The L1 are freeze tolerant, and no clear decrease in larval survival
was observed in larvae held at −20°C (Lorentzen and Halvorsen, 1986).
Preventing its establishment in arctic North America, however, may be a
relatively high threshold temperature as well as a high number of degree
days required for development compared to other arctic protostrongylids
(Halvorsen and Skorping, 1982; Kutz et al., 2001c).
In order for invasive protostrongylids to successfully establish at sub-
arctic and arctic latitudes, suitable climatic conditions and adequate num-
bers and density of suitable intermediate and definitive hosts are critical,
as is a sufficient founding parasite population. These requirements will
differ among species, but some of the parasite characteristics that might be
important for establishment include freeze tolerance of immature stages,
overwintering ability (transposition of the barrier posed by harsh winter
conditions), broad host range, high larval production, and long lifespans.
This is applicable to other species in other nematode families and virtually
any other metazoan parasite.
2.3.2.5.2. Advances in the identification of parasites and infected hosts

Biodiversity survey and inventory have resulted in significant advances
in a knowledge of the distribution of Protostrongylidae species infect-
ing ungulates in high latitudes of North America (Hoberg et al., 1995;
Kutz et al., 2001b; Jenkins et al., 2005a; Kutz et al., 2007; Hoberg et al.,
2008b). Less than two decades after the recognition of a new genus of
protostrongylid in muskoxen from the Central Canadian Arctic (Hoberg
et al., 1995), the definition of new host and geographic ranges for two
other protostrongylids and discovery of yet another previously unknown
species that is widespread through northern North America (Kutz et al.,

2001d; Hoberg et al., 2002; Kutz et al., 2007) show us that there remains
much to be revealed. Recent and substantial advances in the knowledge
of protostrongylid faunas are partially due to the development and use of
molecular techniques that permit species identity based on single L1s in
faeces. These methods supplant laborious bioassay trials and equivocal
assessments of larval morphology, which were impediments to definitive
identification of parasites and infected hosts (Jenkins et al., 2005a; Huby-
Chilton et al., 2006; Kutz et al., 2007). Importantly, previous records of
protostrongylids not validated with either adult specimens or sequencing
of larval DNA remain suspect. Application of molecular-based diagnos-
tics has already facilitated large-scale studies, both geographically exten-
sive and site intensive, on parasite biodiversity which have eliminated
the need for necropsy and examination of adult nematodes (Jenkins et al.,
2005a; Kutz et al., 2007; Asmundsson et al., 2008). The development and
application of new and affordable molecular diagnostics approaches that
permit rapid identification of high numbers of protostrongylid larvae has
immediate value for screening ungulate populations prior to management
and conservation activities such as translocations.
2.3.2.5.3. Ecology
In general, protostrongylid species appear highly adapted to inhospitable arc-
tic environmental conditions. Arctic adaptations include a series of ecologi-
cal traits such as cold and freeze tolerance in both L1 and L3, emergence of L3
from the gastropod host, extended patency (e.g. U. pallikuukensis, P. odocoilei)
and cumulative infections in some species of long-lived hosts. Not all arctic
protostrongylids display all of these traits but they persist nonetheless. For
example, despite a relatively short period of patency and low larval produc-
tion, P. andersoni has a vast geographic range across the mainland Arctic and
Subarctic. Its distribution mirrors that of its only known arctic host, the cari-
bou. Strategies used by this parasite that allow it to persist across such a large
area in a single host species, when the closely related elaphostrongyline,
P. odocoilei, cannot, may be linked to a combination of historical host–parasite
associations and colonization events as well as tolerance and resilience to
contemporary ecological conditions (e.g. Hoberg et al., 2012c).
The protostrongylid species in arctic ungulates appear to have varying
degrees of host specificity, ranging from apparently absolute with U. pal-
likuukensis, parasitic only in muskoxen, to generalists such as P. odocoilei
which is found naturally infecting caribou, Dall’s sheep and mountain goats
and experimentally can infect moose. In some cases when obvious ecologi-
cal barriers have been removed, such as when muskoxen were introduced
or expanded onto Dall’s sheep range, parasites have successfully colonized
new hosts (e.g. P. stilesi in muskoxen, although persistence in muskoxen
in the absence of sheep has not been demonstrated). In other cases where
there are no obvious ecological barriers, parasites retain apparent host

specificity. For example, despite caribou being sympatric with Dall’s sheep
and muskoxen across large parts of their range, P. andersoni has not been
detected in these latter two species (see also Asmundsson et al., 2008). Some
of these species cross taxonomic boundaries of hosts, infecting both cervids
and bovids (e.g. P. odocoilei, Varestrongylus) while others remain within sub-
family or family boundaries (e.g. Protostrongylus in Caprinae, P. andersoni
in cervids). In the case of moose, this species appears to be an accidental
host, only naturally and rarely infected with Varestrongylus sp. n. in the Arc-
tic. Understanding how this mosaic of protostrongylids circulates among
arctic ungulates requires an integrative approach examining deep histori-
cal events of host and parasite colonization of North America, population
genetics and phylogenetic and phylogeographic studies of the parasites
and contemporary ecological studies (e.g. Hoberg et al., 2012b).
A major and essential component of the protostrongylid life cycle that
remains poorly defined for the Arctic is the ecology of the gastropod inter-
mediate hosts. The literature on arctic gastropods is sparse and limited to
a few species distributions (Pilsbry, 1946; Kutz et al., 2000b; Grimm et al.,
2009). This aspect of the life cycle has the potential to be very dynamic and
responsive to climate, with changing temperature and hydrological condi-
tions in the Arctic likely to have substantial impacts on the biodiversity
and population dynamics of gastropods. The role of aquatic gastropods
as intermediate hosts deserves further investigation. These intermediate
hosts may become increasingly important under climate change scenarios
where a warmer environment together with increased precipitation and
flooding events may favour parasite species capable of infecting aquatic
gastropods (reviewed in Morley, 2010). Intricately linked to studies on gas-
tropods are those on host movement, habitat use and grazing behaviour.
Such knowledge provides information on environmental contamination
and sources and rates of exposure. Understanding this complexity may
help tease out some of the ecological features which determine apparent
host and geographic distributions.
Climate change is a major feature of arctic landscapes and protostron-
gylids are repeatedly demonstrated as being highly responsive to climate
warming (Handeland and Slettbakk, 1994; Ball et al., 2001; Jenkins et al.,
2006b). Current climate warming conditions are likely to decrease devel-
opment times and increase survival rates for protostrongylids endemic
to ungulates in the North, extend the period of the year when parasite
transmission is possible and lead to expansion of geographic ranges of
endemic and invasive protostrongylids (Kutz et al., 2005; Hoberg et al.,
2008a, 2008b; Kutz et al., 2009b). Disease outbreaks may be triggered by
unusually warm summers such as has occurred in reindeer in northern
Europe infected with E. rangiferi (Handeland and Slettbakk, 1994) or by
invasions of new protostrongylids into naïve host populations (Ball et al.,

2001).
Mechanistic models have been developed and validated for predicting
the development and response to climate of two key arctic protostrongylids
(U. pallikuukensis and P. odocoilei) in gastropods on the tundra. These have
served as useful tools for examining the past, current and future distribu-
tion of these parasites and can provide an insight into the ecology of other
protostrongylids if basic life cycle information (development thresholds
and heating constants) is available. These models require further develop-
ment to move into a more quantitative predictive realm that will allow
identification of the key stages of the life cycle that are sensitive to change.
2.3.2.5.4. General effects

Protostrongylids can cause significant multi-systemic pathology. Exacer-
bating the effects on the individual is the fact that caribou, muskoxen,
Dall’s sheep and mountain goats are each susceptible to at least three
separate species of protostrongylids, and co-infections with at least two
species are confirmed in all hosts. While the basic pathology has been
described for most (but not all) northern protostrongylids, the potential
additive effects of co-infections require further investigation. Similarly,
while there is a small literature that demonstrates potentially subtle pop-
ulation-level effects of protostrongylids in bighorn sheep and snowshoe
hares (Festa-Bianchet, 1991; Murray et al., 1997), the role of protostron-
gylids in the population dynamics of arctic ungulates in North America
is yet to be examined.
2.3.2.6. Subfamily Dictyocaulinae
2.3.2.6.1. Dictyocaulus spp.

Dictyocaulus spp. are large (up to several centimetres long) white nema-
todes found typically with a dorsal distribution in the bronchi and bron-
chioles of the lungs. A number of species are found in a broad range of
free-ranging ungulate hosts across the Holarctic (Hoglund et al., 2003).
There are varying degrees of host specificity.
(a) Host and Geographic Distributions: At least one species – Dictyocaulus
eckerti – is recorded in moose and caribou in AK, and muskoxen from the
Kitikmeot region of NU and northern QC. Dictyocaulus viviparus has been
reported from muskoxen on the arctic islands and mainland NT and NU,
Canada, as well as AK but these records should be considered suspect
(Table 2.5) (Gibbs and Tener, 1958; Samuel and Gray, 1974; USNPC, 2011).
Records of D. viviparus have often been based uncritically on adult and/or
larval morphology and in light of recent genetic and morphological work
it is more likely that these are D. eckerti (Divina et al., 2000; Hoglund et al.,
2003). There are no published reports for Dictyocaulus in Dall’s sheep or

mountain goats but D. filaria has been reported in bighorn sheep from the
USA (USNPC, 2011). In Greenland, Dictyocaulus sp. was observed in one
of five caribou calves of the Akia-Maniitsoq herd examined in April 2008
(C. Cuyler, S. Kutz, unpubl. data).
(b) Ecology: Adult nematodes produce eggs that pass up the trachea
and, depending on the species, larvated eggs or larvae are excreted in the
faeces. The life cycle is direct and infection is by ingestion of infective L3.
The development from eggs or L1 in the environment is temperature and
humidity dependent. Data on larval development in the environment are
not available for D. eckerti, but for D. filaria of domestic sheep, develop-
ment of L1 to infective L3 in northeast England took approximately 4–9
days in spring and summer, 1.5–4 weeks in autumn and 5.5–7 weeks in
winter (Gallie and Nunns, 1976). The persistence of Dictyocaulus in musk-
oxen as far north as Bathurst Island at 75° latitude (Samuel and Gray, 1974)
suggests that it can develop to infective L3 in the short high arctic summer.
Extended survival of L3 in the arctic environment is unlikely. Whether dis-
persal of the infective larvae of Dictyocaulus spp. in the Arctic is facilitated
by spores of the faecal fungus Pilobolus released from the sporangia, as
occurs for at least some species (e.g. D. viviparus in cattle) (Eysker, 1991),
is not known.
Inhibited development is an important phenomenon in the life cycle
of D. filaria, with a large proportion of the eggs and larvae ingested in
the autumn inhibiting until the following spring (Ayalew et al., 1974). A
similar pattern of inhibition is expected for Dictyocaulus in muskoxen.
In commercial muskox harvests on Banks Island, NT, adult nematodes
are most common in yearling animals in early winter (typically Novem-
ber) and are rare or absent in February (M. Branigan, pers. comm), sug-
gesting that Dictyocaulus at this latitude may overwinter as inhibited
larvae.
(c) Impacts: In general for Dictyocaulus spp., developing pre-adult lar-
vae, adults, eggs and hatched larvae can cause significant pulmonary dam-
age and respiratory disease in their hosts. In muskoxen on Banks Island,
NT, Dictyocaulus infections were associated with emaciation and mortal-
ity in yearlings on at least one occasion (Gunn et al., 1991b). Dictyocaulus
eckerti can also cause significant disease in reindeer and histopathological
findings in this host are consistent with those described in domestic live-
stock (Rahko et al., 1992).
The biodiversity of Dictyocaulus circulating in ungulates at high lati-
tudes remains poorly defined. There exist only a few patchy reports where
species identifications have been confirmed in North America. Where this
has occurred, the species has been designated as D. eckerti, refuting previ-
ous records of D. viviparus. Anecdotal evidence suggests that Dictyocaulus
may be a significant cause of morbidity and mortality of young muskoxen
FIGURE 2.8 Tissue and lymphatic Spirurida reported from ungulates of arctic North
America, including Greenland.
and perhaps also caribou. That it persists in the harsh high Arctic environ-
ment in low-density host populations is perhaps surprising and further
exploration of the ecology of the free-living and parasitic stages of this
parasite is warranted.
2.3.3. Other tissue nematodes: Onchocercidae

There is a minimum of three genera of Onchocercidae nematodes circulat-
ing in ungulates of arctic Canada and AK; none have been reported from
Greenland (although see Fielden, 1877) (Fig. 2.8). Depending on genus
and species, adult nematodes may be found in the abdominal cavity, con-
nective tissue or lymphatic system of their hosts, whereas larval forms
are found in the blood or lymph. These larval forms, named microfilariae
(L1), are typically transmitted by haematophagous dipteran insect inter-
mediate hosts in which development to infective L3 occurs.
2.3.3.1. Subfamily: Setariinae
2.3.3.1.1. Setaria spp.

Setaria spp. are robust nematodes 10–90mm long and 1–3mm thick found
in the peritoneal cavity of a variety of ungulates (Becklund and Walker,
1969; Laaksonen et al., 2007). Two species have been identified in North
American wild ungulates: S. yehi and S. labiatopapillosa. Setaria yehi is con-
sidered distinct from S. tundra, the main species parasitizing cervids in
Fennoscandia (Becklund and Walker, 1969). According to Nikander et al.
(2007), however, the morphological differences between these nominal
species are less than the intraspecific variation demonstrated within S.
tundra. The potential synonymy for S. yehi and S. tundra requires further
exploration; the occurrence of a single holarctic species may be consistent
with the recent history for moose or caribou at high latitudes (Rehbinder
et al., 1975; Laaksonen et al., 2007; Nikander et al., 2007; Hoberg et al.,
2012).
(a) Host and Geographic Distributions. Setaria yehi is found in cervids
across a broad geographic range, documented in reindeer, caribou and
moose from AK and caribou in the NT (Table 2.5) (Becklund and Walker,
1969; Dieterich and Luick, 1971; A. Quist, K. Beckmen unpubl. obs.). Setaria
labiatopapillosa is typically a parasite of bovids but has been reported from
caribou and moose at temperate latitudes (Becklund and Walker, 1969;
USNPC, 2011); at least some of the records from moose may actually be of
S. yehi. There are no reports of Setaria in muskoxen, Dall’s sheep or moun-
tain goats but S. labiatopapillosa has been reported from bighorn sheep
(Becklund and Walker, 1969), indicating that North American caprines
may harbour Setaria species. Setaria sp. are also common in wood bison in
the NT (B. Elkin, unpubl. obs.).
(b) Ecology: The ecology of S. yehi in the Arctic has not been investigated.
A series of studies on S. tundra, however, provide valuable insight into
the ecology of these species in ungulates at arctic and subarctic latitudes.
Adult nematodes live in the peritoneal cavity and produce microfilariae
that circulate in the blood stream (Laaksonen et al., 2009b). Haematopha-
gous insects including mosquitoes (Culicidae, especially Aedes spp. for S.
tundra) and horn flies (Haematobia spp.) are intermediate hosts (Laaksonen
et al., 2009a). Development of microfilariae to L3 in the insect is tem-
perature dependent and for S. tundra takes 14 days at 21°C but does not
occur at a mean temperature of 14.1°C (Laaksonen et al., 2009a). Animals
are exposed to S. tundra during the summer and the prepatent period in
reindeer is approximately four months, with microfilaria first detected in
calves in early November. Thus, in arctic environments, animals infected
one summer will not contribute to transmission until the following year.
Patterns of microfilariae in the peripheral blood vary with age, sea-
son and activity levels. Prevalence and density of microfilariae tend to
be higher in calves than in adults for S. tundra in reindeer and moose
(Laaksonen et al., 2007; Laaksonen et al., 2009b) and similar results were
reported for Setaria sp. in black- and white-tailed deer from southern lati-
tudes of North America (Weinmann et al., 1973; Prestwood and Nettles,
1977). Density of microfilaria in the peripheral blood is the highest dur-
ing the summer. Microfilarial density also increases with host activity and
may enhance transmission during periods of insect harassment, when
hosts are more active due to the discomfort caused by bites and presence
of insects (Laaksonen et al., 2009b). In six captive reindeer, microfilariae-
mia peaked from June to mid-September, then decreased and disappeared
by January (n = 3) or remained very low until the following summer (n = 3),
suggesting a one-year lifespan for the adult parasite and/or evidence of
acquired immunity. Patterns of disease outbreaks in reindeer in Finland –
emerging initially in the south and then moving to the north while disease
in the south decreased – also support an acquired immunity in reindeer.

There is no evidence for transplacental transmission in reindeer.
Moose sympatric with infected reindeer populations have a very low
prevalence of S. tundra (1.4–1.8%) suggesting that they are not good hosts
for this parasite (Laaksonen et al., 2007; Laaksonen et al., 2009b). However,
in some regions of AK, S. yehi appears to be well established in moose with
prevalence of microfilariae up to 100% (A. Quist, K. Beckmen unpubl.
obs.).
Setaria is highly sensitive to climatic conditions and disease outbreaks
and range expansions of S. tundra in Fennoscandia are linked to unusu-
ally warm climatic conditions. In Finland, disease outbreaks in reindeer
have occurred following two consecutive summers with warmer than
average temperatures. Models developed to describe these outbreaks
suggest that disease emergence results from increased development
rates and abundance of the parasites in vectors as well as the herding
behaviour and habitat use of the reindeer (Laaksonen et al., 2009a; Laak-
sonen et al., 2010a).
(c) Impacts: Unlike the situation in Fennoscandia with S. tundra, S.
yehi does not currently seem to be an important cause of morbidity
and mortality in wild caribou of North America. Clinical disease is not
reported in caribou and it was not found in post-mortem examinations
of several hundred wild caribou during International Polar Year activi-
ties (S. Kutz and CARMA, 2011). In AK, infections of 5–20 adult S. yehi
in captive adult reindeer caused a mild to moderate peritonitis but no
clinical signs (Dieterich and Luick, 1971). In contrast, and much more
recently, intense inflammation, a secondary bacterial peritonitis and
mortality in nine free-ranging moose calves were attributed to migrat-
ing S. yehi and massive numbers of microfilaria (A. Quist, K. Beckmen
unpubl. obs.).
2.3.3.2. Subfamily Onchocercinae
2.3.3.2.1. Onchocerca spp.

In North America, Onchocerca cervipedis (syn. Wehrdikmansia cervipedis),
commonly known as ‘legworm’ or ‘footworm’, is a common parasite of
cervids, including moose and woodland caribou of the boreal regions of
AB, BC and southern AK (Ritcey and Edwards, 1958; Williams and Babero,
1958; Low, 1976; Samuel et al., 1976). Adult nematodes range from 5.5 to
6cm (males) and 1.8 to 2.0cm (females) and are found in nodules within
subcutaneous tissues (Wehr and Dikmans, 1935). Parasite identification
is based mainly on gross morphology and the presence of subcutaneous
nodules containing intra-lesional adult nematodes and/or microfilariae
(Samuel et al., 1976). In Eurasia, Onchocerca skrjabini (Synonym O. tarsi-
cola), is present in reindeer and moose (Bylund et al., 1981). Nodules in

reindeer are mainly present under the skin of the muzzle, hocks and to
a lesser extent elsewhere on the body including the brisket and shoulder
(Lisitzin, 1964).
(a) Host and Geographic Distributions. Until recently, there were only
anecdotal reports of O. cervipedis in moose from AK and the YT (Table 2.5)
(P. Merchant, pers. comm.) Recent findings, based on combined parasite
identification, including molecular and histopathological methods, have
confirmed that O. cervipedis occurs in moose and Grant’s caribou from
AK and moose from the NT (G. Verocai, K. Beckmen, S. Kutz, E. Hoberg
unpubl. obs.). The occurrence of this parasite in muskoxen, Dall’s sheep
and mountain goats is unknown. Onchocerca cervipedis may be much more
widespread in ungulates of arctic North America, however, and the need
for targeted survey is apparent.
(b) Life Cycle: The microfilariae produced by female parasites remain in
the skin and are ingested by the vectors during feeding. Blackflies (Dip-
tera: Simuliidae) act as intermediate hosts, with microfilariae developing
to L3. Pledger (1978) demonstrated that Simulium decorum and Simulium
venustum serve as intermediate hosts of O. cervipedis in northeastern AB,
although other simuliids were found feeding on moose. Intermediate
hosts species involved in the epidemiology of this parasite in high lati-
tudes of North America are not known but species that serve as interme-
diate hosts in AB, and related species, are widely distributed in AK, YT,
NT and NU (Currie, 1997; Currie and Adler, 2000; Currie, 2006; Adler and
Currie, 2008).
(c) Impacts: Oncocherca cervipedis rarely causes significant clinical signs.
There are occasional reports of massive infections resulting in swelling,
ulceration and hoof damage in Odocoileus spp. (Rush, 1935; Herman and
Bischoff, 1946). De Nio and West (1942) postulated that clinically affected
animals would be more susceptible to predation and an easier target to
hunters. In contrast, in moose and caribou, this parasite is generally found
along the metatarsus and metacarpus (DeNio and West, 1942). Clinical
disease has not been described in caribou but infections in moose from
YT were associated with open sores in the lower legs (P. Merchant, pers.
comm.). The impacts of O. cervipedis on cervid populations in high lati-
tudes of North America are unknown. Some species of Onchocerca can be
zoonotic, and a recent study reported that Onchocerca jakutensis, a species
that normally infects wild cervids from Eurasia, causes nodular dermato-
logical disease in people (Koehsler et al., 2007).
2.3.3.3. Subfamily: Splendidofilariinae
2.3.3.3.1. Rumenfilaria andersoni

Rumenfilaria are nematodes located in the subserosal lymphatic vessels or
veins of the rumen. Males are up to 62mm long and females up to 205mm
long and may be visible to the naked eye in older and/or thin animals
(Lankester and Snider, 1982; Laaksonen et al., 2010b).
(a) Host and Geographic Distributions: Rumenfilaria andersoni was first
described in moose from northwestern Ontario in 1982 (Lankester and
Snider, 1982) and until recently was only known from the original descrip-
tion. Surveys have now detected microfilariae consistent with R. andersoni
in the blood of up to 70% of Alaskan moose (A. Quist, K. Beckmen unpubl.
obs.). Rumenfilaria has not been documented in muskoxen, Dall’s sheep,
mountain goats or caribou from North America. Rumenfilaria andersoni
tends to be common in other regions where there has been targeted sur-
vey, for example, in Finland (Laaksonen et al., 2010b), and the absence of
reports in caribou, and perhaps other ungulates, in arctic North America
may reflect a lack of search effort as opposed to true absence. Conspeci-
ficity of populations in Fennoscandia and North America remains to be
determined.
Life Cycle: Microfilariae are easily detected in the blood of infected ani-
mals (Laaksonen et al., 2010b), and based on what is known for related
genera it is probable that transmission is by haematophagous arthropods.
Impacts: Adults obstruct the lymphatic vessels of the rumen leading
to dilatation, lymphaedema, lymphangitis, granulomatous inflammation
and fibrosis (Laaksonen et al., 2010b). The occurrence of clinical disease in
wild ungulates remains unknown.
2.3.3.4. Emerging issues and knowledge gaps for the Onchocercidae

Until recently, the Onchocercidae were a completely neglected compo-
nent of the helminth fauna of arctic ungulates of North America. Recent
mortality events for moose calves in AK, new observations of Onchocerca
in moose and caribou in northern Canada and major mortality events in
Fennoscandia linked to S. tundra highlight the possibility that these could
become, or may be becoming, important emerging pathogens under cur-
rent scenarios for climate change. In particular, the work in Fennoscandia
has demonstrated that these parasites are highly responsive to climatic
conditions and that small changes in summer temperatures can lead to
significant disease outbreaks. Members of the Onchocercidae are also
important pathogens of humans in the tropics and knowledge gained from
studying their ecology in the Arctic may provide insights into manage-
ment of this group of parasites in other regions (Laaksonen et al., 2010a;
Davidson et al., 2011). Further research on the biodiversity, definitive host
FIGURE 2.9 Cestoda reported from ungulates of arctic North America, including Greenland.
TABLE 2.6 Cestodes reported from ungulates of arctic North America, including
Greenland. The range of prevalence reported is indicated below the parasite name. Only
prevalence estimates based on sufficient sample sizes are included. Data compiled from
available published and grey literature
Host, Parasite Herd, region or nearest place name
Caribou
Echinococcus granulosus AK Not specifieda; Teshekpuk, Northern Alaska
(1.3-20%) Peninsula, Mulchtna, Western Arcticb
NT Mackenzie Deltac–e; Beverlyf
QC/NL Rivière Georgeg
Taenia hydatigena (15- AK Teshekpukb; Not specifieda,c,h
60%) NT Mackenzie Deltac,e; Beverlyf
NU Kitimeot Regioni
QC Rivière-aux-Feuillesj
Taenia krabbei AK Northwest, Southcentral, Interiork
Taenia cf. krabbei AK Teshekpuk, Northern Alaska Peninsula, Mul-
(13–20%) chatnab, Not specifieda,h
NT Mackenzie Deltae,w
NU Kitikmeot Regioni
QC Rivière-aux-Feuillesj
GL Kangerlussuaql
Moniezia cf. expansa GL Kangerlussuaql
Avitellina arctica NT/NU Thelon Game Sanctuarym
QC Rivière Georgen
Dall’s sheep
Taenia hydatigena (35%) AK Not specifiedh
NT Mackenzie Mountainso
Moniezia sp. (10–16%) NT Mackenzie Mountainso
Host, Parasite Herd, region or nearest place name

Moose
Echinoccocus granulosus AK South Centralp; Tanana Flats, Fairbanks, Palmerb
(24%) NT Mackenzie Mountainsq
Taenia arctos AK Interior and South Centralk
Taenia krabbei AK Interiork
Taenia cf. krabbei AK Not specifiedh
NT Mackenzie Mountainsq
Muskoxen
Echinoccocus granulosus NT/NU Thelon Game Sanctuaryr
Taenia cf. hydatigena AK Not specifiedh
NT/NU Not specifiedq; Thelon Game Sanctuaryr
GL Hurry Inlets
Taenia cf. krabbei AK Not specifiedh
GL Kangerlussuaqt
Taenia sp. NU Ellesmere Islandu
GL east Greenlandv
Anoplocephalidae egg NU Bathurst Island and Devon Islandu,w
Moniezia expansa NU Ellesmere Islandq; Thelon Game Sanctuaryr
Moniezia sp. AK Nunivak Islandw
NU Ellesmere Islandx
a Hadwen (1922). m Gibbs (1960).
b K. Beckmen (unpubl. data). n USNPC, (2011).
c Broughton et al. (1967). o Simmons et al., (2001).
d Sweatman and Williams (1963). p Rausch (1959).
e Choquette et al. (1957). q S. Kutz, C. Tobac (unpubl. obs.).
f Thomas (1996). r Gibbs and Tener (1958).
g Parker (1981). s Alendal and Helle (1983).
h Dieterich (1981). t Raundrup et al. (2012).
i Gunn et al. (1991a). u Webster and Rowell (1980).
j Ducrocq and Lair (2007). v Fielden (1877).
k Lavikainen et al. (2011). w Samuel and Gray (1974).
l Clausen et al. (1980). x Tener (1954).
and geographic range of Onchocercidae in arctic ungulates, together with

research on the life cycle, intermediate host species, transmission patterns
and response to climate change are required (Fig. 2.8).
2.4. CESTODES
The cestodes present in arctic ungulates are from two families, the Tae-
niidae, for which ungulates are intermediate hosts, and the Anoploce-
phalidae, for which ungulates are definitive hosts. Members of Taeniidae
include species of Taenia and Echinococcus, whereas the Anoplocephalidae
is represented by Moniezia, Avitellina and perhaps Thysanosoma (Figure 2.9,
Table 2.6).
2.4.1. Ungulates as Intermediate hosts: Taeniidae

2.4.1.1. Subfamily Taeniinae
2.4.1.1.1. Taenia hydatigena, Taenia krabbei and Taenia arctos
(a) Host and Geographic Distributions. The three species of Taenia recognized
at high latitudes in North America, T. hydatigena, T. krabbei and Taenia arc-
tos all have apparently Holarctic distributions in arctic ungulates, canids
and ursids (Table 2.6) (Loos-Frank, 2000; Haukisalmi et al., 2011). Larvae
are simple cysticeri that commonly occur in the liver and omentum, or
elsewhere in the peritoneal cavity (T. hydatigena) or in the heart, tongue,
oesophagus and skeletal musculature, and less commonly the brain
(T. krabbei and T. arctos) (Broughton et al., 1967; Choquette et al., 1957;
Gibbs and Eaton, 1983; Lavikainen et al., 2011).
Taenia krabbei is often listed as a subspecies of T. ovis, a designation now
refuted by molecular evidence (Lavikainen et al., 2010). A recent report of T.
ovis krabbei in a muskox from west Greenland (Raundrup et al., 2012) should
be referred to T. cf. krabbei; however, it is also possible that this represents T.
arctos instead (see Haukisalmi et al., 2011). Taenia arctos is morphologically
similar to, but genetically distinct from, T. krabbei. It was recently described
to be circulating in moose from AK and Finland and brown bears (Ursus
arctos) in Finland (REFS) (Haukisalmi et al., 2011; Lavikainen et al., 2011).
Consequently, all previous species-level identifications of T. krabbei require
re-evaluation by both morphological and molecular criteria to establish
identity. In particular, current records of T. krabbei in non-canid hosts may
not represent this species (e.g. Rausch, 1994; Hoberg et al., in press-a). Taenia
arctos and T. krabbei are considered phylogenetically quite distant, with the
former as a putative sister species to T. solium and T. krabbei as a sister to T.
multiceps. Since both species had been reported to infect moose, previous
records of T. krabbei in these intermediate hosts should be revisited (Lavi-
kainen et al., 2011). We refer historical records of T. krabbei as tentative and
use the designation of T. cf. krabbei in further discussions below. We treat T.
hydatigena similarly, since limited morphological and molecular confirma-
tion of species identity in arctic ungulates has been done.
Taenia cf. hydatigena is reported in caribou, muskoxen, moose and Dall’s

sheep across their arctic ranges (Table 2.6) (Gibbs and Tener, 1958; Tener,
1965; Webster and Rowell, 1980). Taenia cf. krabbei is known in caribou,
moose and muskoxen but has not been reported in Dall’s sheep. Taenia
arctos was recently described to be circulating in moose and brown bears
(Ursus arctos) from AK and Finland (Haukisalmi et al., 2011; Lavikainen
et al., 2011). Taenia parenchymatosa, a taeniid typical in Eurasian reindeer,
was reported in the liver of reindeer from Alaska (Pushmenkov, 1945 cited
in Choquette et al., 1957) and was probably introduced with these cer-
vids from Chukotka in the last century. It is unknown as to what extent
this parasite established in North America. Infections may be pathogenic
as indicated experimentally where one reindeer died following rupture
of the liver (Pushmenkov 1945 cited in Choquette et al., 1957; Jones and
Pybus, 2001).
(b) Ecology: Taenia spp. have a predator–prey life cycle with adult ces-
todes occurring in the small intestines of carnivores or omnivores and lar-
val stages found as cysts in tissues of herbivore hosts (Loos-Frank, 2000;
Jones and Pybus, 2001). Infection of the definitive hosts is by ingestion of
protoscolices from cysticerci in infected ungulates, and intermediate hosts
are infected by ingestion of eggs from the faeces of carnivores. Transpla-
cental transmission of T. cf. hydatigena was observed in a wild muskox
foetus on the mainland of western Nunavut, Canada (S. Kutz, J. Nishi
unpubl. data). Taeniid eggs are robust, can survive for extended periods
(>200 days) at cool temperatures (Gemmel, 1977) and are likely to per-
sist for extended periods in the Arctic. Infection prevalence and intensity
increases with age for T. cf. hydatigena in moose and caribou (Addison
et al., 1979; Thomas, 1996, although see Pollock et al., 2009) and for
T. cf. krabbei (possibly T. arctos) in moose (Addison et al., 1979). Viable and
degenerate cysts are found across a wide age range of animals, suggesting
both a finite lifespan for the cysticerci as well as ongoing infection (Addi-
son et al. 1979). In caribou, prevalence of T. cf. hydatigena tends to decrease
from December to March (Thomas, 1996).
A series of experiments on T. cf. krabbei and T. hydatigena by Sweatman
and Henshall (1962) provide some important insights into characteristics
of the lifecycles of Taenia spp. in the context of arctic systems. For T. cf.
krabbei, the prepatent period in two dogs given cysticerci that originated
from reindeer from northern Canada was 34 and 37 days. This is short
compared to that for T. ovis in the same study (~60 days) (Sweatman and
Henshall, 1962). The prepatent period of Echinococcus multilocularis is
similarly short (Rausch and Schiller, 1956) and Sweatman and Henshall
(1962) suggested that both these species appeared to have evolved at high
latitudes and that the short prepatent periods could be adaptations to the
short arctic summers, allowing carnivores to maximize egg production
during the seasonal period when successful transmission to the interme-
diate host is more likely. These species have extended histories at high lati-
tudes (e.g. Hoberg et al., 2012 ) and have been influenced by increasingly
cold environments since the Pliocene.
Establishment of cysticerci of T. cf. krabbei as adult cestodes in experi-
mentally infected dogs was high, with 7 of 7 cysticerci maturing to adult
worms in one dog. An average of 9.2–9.3 proglottids, with an average of
19,300 eggs each, were shed per day throughout patency that lasted at least
131 days. Ten sheep, seven goats, one domestic calf and two pigs were
refractory to experimental infection with T. cf. krabbei of reindeer origin,
suggesting host specificity of this parasite (Sweatman and Henshall, 1962).
Sweatman and Plummer (1957) conducted similar studies on the life
history of T. hydatigena. The prepatent period in dogs experimentally
infected with cysticerci from sheep or moose was 51–76 days and patency
lasted 4.5–11.5 months. During that time, proglottids were excreted regu-
larly with one dog infected with five worms excreting an average of 3.7
proglottids per day. Excreted proglottids contained from 6000–23,000 eggs
and some remained active for a day or so post-excretion and were highly
mobile, moving up to three feet from the faeces (Sweatman and Plum-
mer, 1957). In contrast to T. krabbei, T. hydatigena of moose origin, passaged
through a dog, was infective to domestic sheep, suggesting no species bar-
riers between the sylvatic and domestic cycle for this species (Sweatman
and Plummer, 1957).
In contrast to domestic sheep, cysticerci in moose, reindeer and mus-
koxen can mature in the parenchyma of the liver (Choquette et al., 1957;
Sweatman and Plummer, 1957; Gibbs and Tener, 1958). Cysticerci in the
liver parenchyma of moose remain viable for up to 48 hours at subzero
temperatures in northern Ontario, considerably longer than those on the
liver surface or in the omentum. Thus, development to mature, viable cys-
ticerci deep in the hepatic parenchyma may be a mechanism that enhances
transmission potential during the arctic winter in the sylvatic cycle (Sweat-
man and Plummer, 1957).
Adult stages of both T. cf. hydatigena and T. cf. krabbei have been
reported in domestic dogs (Canis familiaris), wolves (Canis lupus), coy-
otes (Canis latrans), red fox (Vulpes vulpes) and arctic fox (Vulpes alopex)
(Kapel and Nansen, 1996; Lavikainen et al., 2011). Taenia cf. krabbei has
also been reported in black (Ursus americanus), brown (U. arctos) and polar
(U. maritimus) bears (Choquette et al., 1969; Pence et al., 1983; USNPC,
2011). To date, T. arctos has been described only from brown/grizzly bears
(Haukisalmi et al., 2011) but previous records of T. krabbei in ursids need to
be revisited. It is probable that the contribution of each intermediate and
definitive host species to the circulation of these cestodes in arctic environ-
ments differs. For example, in west Greenland and Svalbard where wolves
are absent and domestic dogs are few, it is the arctic fox that is responsible
for maintaining T. krabbei (Bye, 1985; Kapel and Nansen, 1996; Stien et al.,
2010) whereas wolves may play a more important role elsewhere.
(c) Impacts: Taenia species are relatively common in arctic ungulates at
low intensities and in general do not seem to cause significant pathology.
There are, however, occasional hunter reports of animals in poor condi-
tion that are severely affected with T. cf. krabbei (Kutz, 2007). Migrations
of T. hydatigena through the liver can also cause tissue damage (Sweatman
and Plummer, 1957). In cross-sectional studies, there was no relationship
between the number of cysts of T. cf. hydatigena in the livers of caribou
and kidney fat index (Pollock et al., 2009) and no detectable impact of
T. cf. hydatigena or T. cf. krabbei on body condition in moose (Addison
et al., 1979).
Taenia hydatigena, T. krabbei and T. arctos are not known zoonoses; how-
ever, T. krabbei and T. arctos are sister species of T. multiceps and T. solium,
respectively, both of which can infect people, leading to uncertainty con-
cerning the zoonotic potential for these arctic taeniids (Lavikainen et al.,
2008). Meat or livers with high intensities of cysticerci may be discarded
by harvesters (Kutz, 2007; B. Elkin, S. Kutz, unpubl. obs.).
2.4.1.2. Subfamily Echinococcinae
2.4.1.2.1. Echinococcus granulosus

(a) Host and Geographic Distributions: Echinococcus granulosus occurs in
the larval stage (hydatid cysts) in the lungs of reindeer, caribou, moose
and muskoxen across North America (Table 2.6) (Gibbs and Tener, 1958;
Rausch, 1967; Choquette et al., 1973; Barrett and Dau, 1981; Rausch,
2003). It is reported in mountain goats from temperate regions (Foreyt
et al., 2009) but has not been found in Dall’s sheep nor is it known from
Greenland (OIE, 1998; Smith, 1957 in Rausch, 2003). Two strains circulate
in ungulates of arctic Canada, G8 and G10, and these differ from other
forms of E. granulosus with respect to pathogenicity to people, infectiv-
ity to domestic ungulates, serology and genetics (reviewed in Thompson,
2008). Whether these strains represent a different species of Echinococcus,
that is, E. canadensis, is unresolved (Thompson, 2008; Knapp, 2011).
(b) Ecology. Wolves (Canis lupus) are the primary definitive hosts in the
Arctic and coyotes (Canis latrans) and domestic dogs can also be infected
(Rausch, 2003). The prepatent period is 56–65 days in dogs, maximum egg
production occurs as early as 76 days post-infection, and the lifespan of the
adult parasite is 8 months to a year (Sweatman and Williams, 1963; Rausch,
1993). Individual dogs can acquire hundreds to tens of thousands of adult
parasites following ingestion of hydatid cysts (Rausch, 1993). Ungulates
are infected by ingestion of eggs from the faeces of infected canids. Like
species of Taenia, these eggs can persist in the environment under cool
moist conditions (Gemmel, 1977). In caribou and moose prevalence, inten-

sity and cyst size increase significantly with age and up to 167 cysts have
been reported in a single moose (Addison et al., 1979; Thomas, 1996). Echi-
nococcus granulosus is zoonotic, and exposure to faeces from infected dogs
that have consumed cysts in wild game is a potential risk in arctic com-
munities (Choquette et al., 1973; Rausch, 2003; Himsworth et al., 2010).
Skinning wolves and foxes are also potential zoonotic risks for trappers.
(c) Impacts. In arctic ungulates, hydatid cysts are found predominantly
in the lungs and less frequently in the liver where they are usually abnor-
mal and sterile (Rausch, 2003; Broughton et al., 1967). In moose, they can
also occur in the spleen, heart or kidneys (Addison et al., 1979). Thomas
(1996) was unable to detect a significant impact of E. granulosus on preg-
nancy, weight or kidney fat in caribou although there were trends towards
poorer body condition and lower pregnancy rates. Infection in moose may
lead to increased mortality; those with high burdens of cysts in their lungs
are more susceptible to hunting and predation than are those with low
burdens or no infection (Rau and Caron, 1979; Joly and Messier, 2004). The
impacts in other arctic ungulates are unknown.
2.4.2. Ungulates as definitive hosts: Anoplocephalidae

2.4.2.1. Subfamilies Anoplocephalinae and Thysanosomatinae
2.4.2.1.1. Moniezia, Avitellina, Thysanosoma

(a) Host and Geographic Ranges: Moniezia and Avitellina are large, long ces-
todes reaching several metres in length and found in the small intestine of
ruminants. Eggs of anoplocephalid tapeworms have been recovered from
faeces of muskoxen, Dall’s sheep, caribou and mountain goats through-
out most of their range (Table 2.6). Adult specimens of Moniezia expansa
have been reported from muskoxen in NU and NT (Gibbs and Tener, 1958;
Tener, 1965; Samuel and Gray, 1974). Anoplocephalid eggs are present in
the faeces of muskoxen in Nunavik, QC, and may differ morphologically
from those recovered from muskoxen in the western Canadian Arctic
(S. Kutz, M. Simard, unpubl. data). Thysanosoma actinoides and M. expansa
are reported in moose from temperate regions of North America (Samuel
et al., 1976; Stock and Barrett, 1983; Hoeve et al., 1988) and anoplocephalid
eggs are common in moose from the arctic and subarctic regions (Table 2.6).
Moniezia sp. is reported from Dall’s sheep of the Mackenzie Mountains
(Simmons et al., 2001) and M. benedeni, Avitellina sp. and Thysanosoma acti-
noides are reported in mountain goats from western Canada (Cowan, 1951;
Samuel et al., 1977).
The diversity of anoplocephalid cestodes in subspecies of Rangifer is
not well documented in North American and Greenland. Avitellina arctica
was reported in a caribou from the Thelon Game Sanctuary, NT (Gibbs,
1960) and the Rivière-George caribou herd in QC in 2006 (USNPC, 2011)

and is commonly reported from reindeer in Eurasia. Several species of
Moniezia including M. benedeni, M. taimyrica and M. rangiferina have been
described in reindeer from Russia, Norway and South Georgia Island
(Semenova, 1967; Zelinskii, 1973; Leader-Williams, 1980; Bye, 1985); how-
ever, there are no confirmed reports of Moniezia sp. in free-ranging arctic
and subarctic North American caribou. Diversity of anoplocephalids, and
particularly species of Moniezia at high latitudes, requires further inves-
tigation including the application of new molecular-based methods to
unequivocally resolve identity and host associations for these otherwise
widespread species.
(b) Ecology. Anoplocephalids have an indirect life cycle. Eggs in the fae-
ces of infected ungulate definitive hosts are ingested by arthropod inter-
mediate hosts where they develop to the infective cysticercoid stage. The
life cycle is completed when cysticercoids are ingested by the definitive
hosts. Moniezia spp. are generally transmitted by oribatid mites (Samuel
and Gray, 1974; Elliott, 1986; Denegri, 1989; Xiao and Herd, 1992) and in
Russia Avitellina arctica develops in at least two species of Collembola,
Onychiurus taimyricus and O. furcifera (Kozlov, 1986). Development to fully
formed cysticercoids is temperature dependent, for example, ranging
from 27 (28°C) to 97 (18–20°C) days for M. expansa in oribatid mites (Nar-
sapur and Prokopic, 1979). The long development time at these relatively
warm temperatures (18–20°C) is perhaps surprising for an arctic parasite
and suggests that climatic conditions may play an important role as deter-
minants of geographic range and epidemiology of this group of parasites.
Anoplocephalids are generally parasites of young animals and are
uncommon in adults (Kirilenko, 1975; Bye, 1985). There is some evidence
of host specificity, for example, A. arctica does not infect ‘horned’ species
that are sympatric with infected cervids in Russia (Gibbs, 1960). Similarly,
caribou that are sympatric with infected muskoxen in the Thelon Game
Sanctuary, NU, were infected with A. arctica while M. expansa was identi-
fied from muskoxen (Gibbs and Tener, 1958; Gibbs, 1960).
(c) Impacts. Anoplocephalid tapeworms can cause diarrhoea and
reduced weight gain in domestic lambs (Narsapur, 1988). In reindeer in
Russia, A. arctica causes sufficient pathology in calves to warrant treatment
and M. baeri, M expansa and M. benedeni are reported to cause unthriftiness
and emaciation (Polyanskaya, 1961; Kirilenko, 1975). For muskoxen, there
is some evidence of pathology induced by Moniezia spp. Translocated
muskox calves that grazed on pasture previously occupied by domestic
sheep and cattle in Iceland died with heavy tapeworm infections and
scouring in captive muskoxen in Norway was attributed to Moniezia spp.
(Samuel and Gray, 1974). The specimens of Moniezia were not identified to
species in either of these cases.
TABLE 2.7 Trematodes reported from ungulates of arctic North America, including
Greenland. The range of prevalence reported is indicated below the parasite name. Only
prevalence estimates based on sufficient sample sizes are included. Data compiled from
Host and Parasites Herd or location
Caribou
Fascioloides magna QC Rivière-aux-Feuillesa; Rivière Georgeb–d
(15–60%)
Paramphistomum cervi AK Cantwelle; Northern Alaska Peninsula, Mulchatnaf
Muskoxen
Fascioloides magna (87%) QC Kuujjuak, Tasiujaqg
Moose
Paramphistomum cervi AK Anchorageh; Fairbanks, Tanana Flatsf
a Ducrocq and Lair (2007).
b Choquette et al. (1971).
c Parker (1981).
d Lankester and Luttich (1988).
e Dieterich, (1981).
f K. Beckmen (unpubl. obs.).
g M. Simard (pers. comm.).
h USNPC, (2011).
FIGURE 2.10 Trematoda reported from ungulates of arctic North America, including
Greenland.
2.4.3. Emerging issues and knowledge gaps for the Cestoda

Cestoda, although widespread in ungulates of arctic North America and
Greenland, are not well characterized. Recent phylogenetic work on the
taeniids, together with discovery of a new species of Taenia circulating in
moose across the Holarctic, highlights the possibility of additional cryptic
species and complexes circulating in ungulates from the Arctic and Sub-
arctic (Lavikainen et al., 2008; Lavikainen et al., 2010; Haukisalmi et al.,
2011; Lavikainen et al., 2011).
Similarly, for the anoplocephalids, the Russian literature suggests that
there may be considerable hidden diversity within Moniezia, that anoplo-
cephalids may have significant impacts on their hosts and that they may
be influenced by climate changes (Priadko, 1976; Narsapur and Prokopic,

1979). That there has been no recent work on biodiversity or impacts of
this family in North America is perhaps surprising. Further characteriza-
tion of the cestode fauna of arctic ungulates is warranted and will strongly
benefit from molecular approaches in defining species limits, diversity and
epidemiological patterns. There is also a need to more critically explore
the impacts of these parasites in arctic hosts, their potential zoonotic risk,
particularly for taeniids, and how they circulate among the various defini-
tive and intermediate hosts.
2.5. TREMATODES
The trematode fauna of ungulates in arctic North America is very

simple, consisting of only two known species: Fascioloides magna, the
giant liver fluke, and Paramphistomum cervi, the rumen fluke (Table 2.7,
Figure 2.10). Both parasites require aquatic snails as intermediate hosts for
transmission.
2.5.1. Family Fasciolidae

2.5.1.1. Subfamily Fasciolinae
2.5.1.1.1. Fascioloides magna

(a) Host and Geographic ranges: The arctic distribution of F. magna is limited
to caribou and muskoxen from northern Quebec and Labrador (Choquette
et al., 1971; Lankester and Luttich, 1988; Pollock et al., 2009: M. Simard
pers. comm) (Table 2.7). Both hosts become patent and prevalence is high,
often approaching 100%. Moose are dead-end hosts for F. magna (Pybus,
2001), and it has not been reported in mountain goats or Dall’s sheep nor
has it been reported in Greenland.
(b) Ecology: Aquatic snails of the family Lymnaeidae are intermediate
hosts for F. magna (Pybus, 2001; Králová-Hromadová et al., 2011). Lym-
naeid snails are present across the Arctic (Hershey, 1990) and various
stages of the parasite have been demonstrated to overwinter in snails
(Pybus, 2001). In caribou, prevalence and intensity tend to increase
with age (Lankester and Luttich, 1988). The life cycle in muskoxen is
undescribed.
(c) Impacts: Fascioloides magna causes substantial liver pathology
in normal and aberrant hosts (Pybus, 2001). In caribou, adult flukes
are associated with lesions that include fibrous capsules typically con-
taining two flukes and copious amounts of viscous grey–brown/black
fluid. Migrating immature flukes are associated with blood filled tun-
nels up to 1.5cm wide (Lankester and Luttich, 1988). Similar lesions are
present in muskoxen (CCWHC, 2011). Despite the significant hepatic
damage, there is no evidence that F. magna has negative effects on
body condition of caribou (Lankester and Luttich, 1988; Pollock et al.,
2009). In moose, the flukes do not mature and the continued migra-
tion of immature flukes through the liver can lead to mortality (Pybus,
2001). Flukes also did not mature in three bighorn sheep experimentally
infected with 50 or 100 metacercariae. All three sheep died from the
effects of the flukes within 104–197 days post-infection. Post-mortem
findings included multifocal pyogranulomatous hepatitis, necrotiz-
ing haemorrhagic pneumonia, pleuritis and peritonitis (Foreyt, 1996).
Three, 18 and 21 flukes were recovered from the sheep indicating a
low lethal dose. A similar outcome might be expected in other bovids,
specifically Dall’s sheep and mountain goats. The introduction of
F. magna into areas where hosts had not been previously exposed is
related to mortality events in European cervids (Balbo et al., 1989;
Slavica et al., 2006).
Fascioloides magna is present in wild cervids of northern BC, AB and
SK (Wobeser et al., 1985; Pybus, 2001) but its distribution is patchy. Range
expansion for this parasite has been associated with natural migration
or translocation of infected hosts into non-endemic areas (Wobeser et al.,
1985; Pybus, 2001; Slavica et al., 2006; Králová-Hromadová et al., 2011).
Development in snail hosts is temperature dependent which may limit its
northward range expansion; however, it is well established in arctic Que-
bec, and the ability to overwinter in snails may facilitate its maintenance
in this environment.
2.5.2. Family Paramphistomidae

2.5.2.1. Subfamily Paramphistominae
2.5.2.1.1. Paramphistomum spp.

(a) Host and Geographic ranges: Paramphistomum spp. are rumen flukes that
are pear-shaped worms characterized by a large terminal ventral sucker.
Numerous genera and species within the Paramphistominae have been
described but the genus was redefined and restricted with only nine spe-
cies being retained (Eduardo, 1982). In North America, P. cervi is reported
in Alaskan caribou and moose (Dieterich, 1981; USNPC, 2011; K. Beckmen,
unpubl. data) and P. cervi and P. liorchis are known in moose from temperate
Canada (Lankester et al., 1979; Kennedy et al., 1985). Paramphistomum has
not been observed in muskoxen, Dall’s sheep or mountain goats. Param-
phistomum leydeni is documented in reindeer from Eurasia (Nikander, 1992).
(b) Ecology: The life cycle of species of Paramphistomum requires aquatic
snail intermediate hosts of which members of the Lymnaeidae and Planor-
bidae are suitable (DeWaal, 2010). Miracidia develop in eggs, hatch, infect
aquatic snails and develop to cercaria. This process is temperature depen-
dent, and in one experimental study on P. cervi, miracidia developed in 20
days in eggs maintained at 20°C but did not hatch at temperatures below
13°C. When infected snails were maintained at 20°C, cercaria were shed by
50 days post-infection (reviewed by Lankester et al., 1979). Snails can shed
cercariae for up to one year (Dinnik and Dinnik, 1957). Based on the sea-
sonal variation in size of adult P. cervi throughout the year, Lankester et al.
(1979) proposed a one-year life cycle for parasites in moose from Ontario.
Animals are infected in the summer and flukes mature by the following
spring, breed and die by autumn. Maturation of flukes in moose appears
to be much slower than that in cattle, sheep and roe deer in Germany and
may be related to changing seasonal diet as well as a strategy to synchro-
nize egg production with availability of intermediate hosts in the summer
(Lankester et al., 1979). In moose in Ontario, prevalence increased from
calves (14%) to yearlings (50%) to adults (82%) (Lankester et al., 1979).
Little is known about the effects of rumen flukes in wild cervids.
Heavy infections have been noted in severely debilitated adult moose and
caribou in AK (K. Beckmen, unpubl. obs.). There is one report of severe
denudation of rumen villae in heavily infected moose calves (Seyfarth,
1938 cited in Lankester et al., 1979). In general, clinical signs are uncom-
FIGURE 2.11 Protozoa reported from ungulates of arctic North America, including
Greenland.
mon in domestic livestock but juvenile parasites in the small intestine may
cause a severe enteritis and profuse diarrhoea (DeWaal, 2010).
The host and geographic distribution of Paramphistomum flukes in
ruminants from the Canadian and Greenlandic Arctic remains virtually
unexplored, and the life cycle and effects are not well understood. Some
features of the life cycle for P. cervi, hatching only over 13°C, and long
development time for cercaria at 20°C in the snail intermediate hosts may
limit the abundance and distribution of this parasite at northern latitudes
(note though Paramphistomum spp. are widespread in reindeer of the Rus-
sian taiga). Species of Paramphistomum are typically considered parasites
of tropical regions, and recent increased occurrence in domestic livestock
at more northern latitudes (DeWaal, 2010) may reflect changes in geo-
graphic distribution, perhaps linked to climatic changes. Further survey
and inventory in the Arctic should be pursued.
2.6. PROTOZOA
Arctic ungulates are host to a broad array of gastrointestinal and tissue

protozoa (Figure 2.11).
2.6.1. Protozoa of the gastrointestinal tract

2.6.1.1. Family Hexamitidae
2.6.1.1.1. Giardia duodenalis
Giardia is a genus of intestinal protozoa that infects a variety of vertebrate
hosts, including people and wildlife (Thompson, 2004). Giardia duodenalis
(synonyms: G. intestinalis and G. lamblia) infects a wide range of free-rang-
ing and domestic animals, and people (Thompson, 1998). A minimum of
seven assemblages (A–G) and many subgroups are recognized (Thomp-
son, 2004; Lasek-Nesselquist et al., 2010). Some subgroups of assemblage
A and B are zoonotic (Sprong et al., 2009). Other assemblages (C–G) are
considered host specific and non-zoonotic (Lebbad et al., 2010).
(a) Host and Geographic Distributions: Giardia species are reported with a
patchy distribution and low prevalence and intensity in caribou and Dall’s
sheep from North America (Table 2.8) (Samuel and Gray, 1974; Roach
et al., 1993; Siefker et al., 2002; Kutz et al., 2008; Kutz et al., 2009c). Giardia
duodenalis assemblage A is common in muskoxen on Banks Island, NT,
(Kutz et al., 2008) but absent from over 200 muskoxen tested on Victoria
Island, NT and NU (S. Kutz, J. Wu, S. Checkley, M. Dumond unpubl. obs.).
In a broad survey of frozen faeces from 520 barren-ground caribou from
twelve herds in North America, only seven sample(s) tested by immuno-
fluorescent antibody (Waterborne Inc.) were positive for Giardia (S. Kutz
TABLE 2.8 Gastrointestinal protozoa reported in ungulates of arctic North America,

including Greenland. The range of prevalence reported is indicated beside the parasite
name. Herds or locations where the parasites were tested for but were absent are
indicated by a ‘0’ following the location/herd with the number of animals tested
following in parentheses. Data compiled from available published and grey literature
Host and parasite species

Caribou and reindeer

Cryptosporidium sp. (1.3–12%) AK Teshekpuk and Western Arctica
NT South Slave regionb; Banks Islandc
Giardia sp. (3%) AK Teshekpuk and Western Arctica
NT Banks Islandc
Eimeria sp. YT Chisanad
NT South Slaveb
Moose
Cryptosporidium sp. AK Colville River area 0(32) a
Giardia sp. AK Colville River area 0(32) a
Muskoxen
Cryptosporidium sp. NT Banks Island 0(72) e
Giardia duodenalis Assemblage A NT Banks Islande
Eimeria sp. NU Devon Islandf
Eimeria moshati (75–100%) AK Nunavik Islandg
E. faurei (43–100%) NU Bathurst Islandg
E. ovina (93–100%) QC Kuujjuaq and Tasiujaqg
Eimeria granulosa (21 and 24%) AK Nunavik Islandg
NU Bathurst Islandg
Eimeria oomingmakensis (14.3%) NU Bathurst Islandg
Dall’s sheep
Cryptosporidium spp. YT Not specified 0(5) h
Giardia (40%) YT Not specifiedh
Eimeria ahsata NT Mackenzie Mountainsi,j
Eimeria crandallis NT Mackenzie Mountainsi,j
Eimeria dalli AK Kenai Peninsulak
NT Mackenzie Mountainsi,j
Eimeria ninakohlyakimovae NT Mackenzie Mountainsi,j
Eimeria parva NT Mackenzie Mountainsi,j
a Siefker et al. (2002). i Uhazy et al. (1971).
b Johnson et al. (2010). j Simmons et al., (2001).
c Nagy et al. (1998). k Clark and Coldell (1974).
d Hoar et al. (2009).
e Kutz et al. (2008).
f Samuel and Gray (1974).
g Duszynski et al. (1977).
h Roach et al. (1993).

and CARMA, unpubl. obs). Giardia was not found in a survey of 92 cari-
bou from two herds in western Greenland (S. Kutz, C. Cuyler, unpubl.
obs.) nor is it reported for other Greenland wildlife, but it was found in
Greenlandic people (Babbott et al., 1961; Krasilnikoff and Gudmand-
Hoeyer, 1978). Giardia sp. have not been documented in moose from the
North American Arctic but are reported in moose from northern Saskatch-
ewan (Heitman et al., 2002) and G. duodenalis assemblage A are reported
from moose in Norway and Sweden and in reindeer in Norway (Heitman
et al., 2002; Siefker et al., 2002; Hamnes et al., 2006; Lebbad et al., 2010).
(b) Impacts: Clinical disease associated with Giardia spp. has not been
described in free-ranging arctic ungulates. In people and domestic ani-
mals, clinical signs can include diarrhoea, dehydration, abdominal pain
and weight loss (Thompson, 2004; Collinet-Adler and Ward, 2010). In
cattle, Giardia spp. infections and disease mainly affect calves and can
decrease herd performance (Naciri et al., 1999; Olson et al., 2004).
(c) Ecology: Giardia is typically considered a waterborne parasite but
transmission may be equally likely through contaminated vegetation
(Thompson, 2004). Giardia cysts are immediately infective and in general
are thought to be environmentally resistant (Thompson, 2004) but mul-
tiple freeze–thaw cycles may cause high mortality (Robertson and Gjerde,
2004; Robertson and Gjerde, 2006).
The high prevalence of G. duodenalis in muskoxen on Banks Island, NT,
demonstrates that it is capable of persisting in a true arctic environment.
The mechanisms for this persistence are unknown but could include over-
winter survival in both the hosts and the environment; cysts are docu-
mented in muskox faeces in winter (Kutz et al., 2008).
It is enigmatic that Giardia appears to be absent from muskoxen on the
adjacent Victoria Island while it is so well established on Banks Island.
Muskoxen on these islands presumably originated from a common Berin-
gian population; however, they have undergone bottlenecks in more
recent times (Gunn et al., 1991b) that may have led to regional extirpa-
tion of Giardia in small sub-populations. Recognizing that the source of
infection could be people, the historical movements of Inuit, whalers and
explorers, and more recently tourists, must also be considered. A point
source introduction of Giardia by people to Banks Island, with subsequent
establishment and spread in the muskox population, is plausible. Con-
temporary ecological conditions on the islands also differ, with histori-
cally a higher density of muskoxen on Banks Island and perhaps a higher
concentration of animals around key water and food sources such as river
valleys.
Our understanding of the epidemiology and transmission pathways
for Giardia spp. on Banks Island and elsewhere in the Arctic is limited by
patchy surveys and absence of ecological studies. Of particular interest is
the potential interaction among people, wildlife and domestic animals for
the circulation of Giardia in northern ecosystems (Kutz et al., 2008; Kutz

et al., 2009c). Giardia occurs in people, particularly the young, in arctic
communities (Babbott et al., 1961; Eaton and White, 1976) and has been
isolated from water sources for rural villages in Alaska (Pollen, 1996). Fur-
ther survey and strain characterization, in animals and people, are essen-
tial to better understand the ecology and potential impacts of this zoonotic
pathogen in wildlife and people in the Arctic.
2.6.1.2. Family Cryptosporidae
2.6.1.2.1. Cryptosporidium spp.

Cryptosporidium spp. are gastrointestinal protozoa that are important
causes of diarrhoea in people and a wide variety of animals (Fayer et al.,
2010). There are multiple species and genotypes and a range of host speci-
ficities.
(a) Host and Geographic Distribution: Cryptosporidium spp. are occasion-
ally reported from muskoxen and caribou in the North American Arctic
and Subarctic (Table 2.8). They were not detected in over 80 caribou from
the Kangerlussuaq-Sisismiut and Akia-Maniitsoq caribou herds of west
Greenland (S. Kutz, C. Cuyler, unpubl. obs.) nor in faecal surveys from
moose in AK or Dall’s sheep in the YT (Roach et al., 1993; Siefker et al.,
2002; Kemper et al., 2004; Kutz et al., 2008). However, clinical disease asso-
ciated with Cryptosporidium was recently observed in one of two orphaned
moose calves in AK (K. Beckmen, R. Gerlach, unpubl. obs.) (Table 2.8).
A novel caribou genotype was reported from one herd of caribou in AK
(Siefker et al., 2002) and the isolates from the AK moose calves are cur-
rently being described (L. Ballweber, K. Beckmen, unpubl. obs.).
(b) Ecology: Based on fairly extensive faecal survey, Cryptosporidium is
not a common parasite of caribou, moose or muskoxen. Freezing can kill
Cryptosporidium spp. oocysts in laboratory conditions (Fayer et al., 2000)
and in colder aquatic and terrestrial environments; thus, transmission
may be temperature limited in the Arctic (Robertson and Gjerde, 2004;
Robertson and Gjerde, 2006).
(c) Impacts: Cryptosporidium is generally considered a disease of neo-
natal and young animals and tends to be self-limiting in immunocom-
petent hosts (Naciri et al., 1999; Hamnes et al., 2006; Petry et al., 2010).
Clinical disease in wild arctic ungulates, other than a single moose calf
in AK, has not been reported, but Cryptosporidium spp. infection was the
cause of severe diarrhoea and lethargy in captive muskox calves in Sas-
katchewan, Canada (Western College of Veterinary Medicine, Saskatoon,
Saskatchewan medical records). The caribou genotype described from
AK is closely related to C. andersoni, an abomasal species associated with
decreased milk production and lower weight gains in cattle (Ralston et al.,
2011); similar effects may be anticipated in caribou (Siefker et al., 2002).
2.6.1.3. Family Eimeriidae
2.6.1.3.1. Eimeria spp.

The Eimeriidae consists of a broad diversity of protozoal parasites of the
gastrointestinal tract. There have been some recent advances in knowl-
edge of species diversity in the Palaearctic ungulates, but little is known
about the ecology of this group of parasites in arctic ungulates.
(a) Host and Geographic Distributions: Eimeria species are found in almost
all examined caribou, muskoxen and Dall’s sheep populations throughout
their ranges in North America, including Greenland (Tables 8, 11). There is
a minimum of six species of Eimeria described from muskoxen and three
from Dall’s sheep (Uhazy et al., 1971; Clark and Coldell, 1974; Duszynski
et al., 1977; Korsholm and Olesen, 1993).
Perhaps surprisingly given the presumed host specificity of most
Eimeria species, three species from muskoxen, E. granulosa, E. ovina and
E. faurei, are also reported from bighorn sheep (Duszynski et al., 1977).
The species of Eimeria in caribou of North America and Greenland have
not been identified, but Eimeria mayeri (prevalence 2.6%; n = 195), E. ran-
giferis (1.0%; n = 195) and E. hreindryria (1.8%; n = 56) have been described
in Icelandic reindeer (Gudmundsdottir and Skirnisson, 2005; Gudmunds-
dottir and Skirnisson, 2006), and E. arctica, E. mühlensi, E. tarandina and
Isospora rangiferis (the latter species identification may be suspect) have
been described in Russian reindeer (Yakimoff 1936, 1937 and 1939, cited
by Gudmundsdottir and Skirnisson, 2006). There are no reports of Eimeria
species in moose from northern BC, YK and NT but Eimeria sp. and associ-
ated diarrhoea in calves is a chronic problem in a captive, research herd of
moose in AK (K. Beckmen, unpubl. obs.) and E. alces has been described in
Russian moose (Soshkin, 1997).
(b) Ecology: Eimeria spp. of arctic ungulates have a direct life cycle
with oocysts shed in faeces, sporulation in the environment and infec-
tion through ingestion. In muskoxen, Eimeria oocysts are present in the
faeces year round, including throughout the winter (Table 2.11). Samuel
and Gray (1974) reported increased shedding of oocysts from muskoxen
in the high Arctic from March to June. At least some species of Eimeria
from muskoxen are freeze tolerant and sporulate after several months
storage at −20°C (R. Rember, S. Kutz, E. Greiner, unpubl. obs.). Sporula-
tion after extended freezing at −7°C or colder is rare for most Eimeria
spp. (Landers, 1953; Marquardt et al., 1960; Rind and Brohi, 2001) but
ability to withstand freezing may be related to environmental conditions
under which the species exist. For example, Landers (1953) demonstrated
sporulation of three species of Eimeria (E. arloingi, E. ninakohlyakintovi and

E. parva) from domestic sheep in Wyoming after freezing at −19 to −25°C
as well as repeated freeze–thaw cycles. These temperatures were simi-
lar to the extreme minimums for that region in winter. Other Eimeria of
cattle, E. bovis and E. zuernii sporulated after 24h of freezing at −20°C but
not when maintained for a longer time period (Rind and Brohi, 2001).
Freeze tolerance for Eimeria spp. from caribou and Dall’s sheep has not
been investigated.
The abundance of Eimeria spp. is low in barren-ground caribou but
quite high in both muskoxen and Dall’s sheep and the parasites tend
to be present year round in these latter species (Table 2.11). Such differ-
ences may reflect the different behaviour of these host species. Barren-
ground caribou have massive home ranges, migrate over vast distances
(over 1000 km) and are moving constantly throughout the summer
(Nagy et al., 2005). This behaviour may remove caribou spatially from
contaminated regions and reduce opportunities for exposure to infec-
tive oocysts. In contrast, muskoxen and Dall’s sheep are more seden-
tary with much smaller home ranges and a build-up of the parasites
in their immediate environment and ongoing exposure may be more
likely.
(c) Impacts: Clinical disease associated with Eimeria spp. is not common
in free-ranging arctic ungulates. The highest oocyst count reported in fae-
cal surveys of >1000 Dall’s sheep, caribou, moose and muskoxen in north-
ern Canada is 17,500 oocysts per gram (opg) of previously frozen faeces in
a muskox from Banks Island (NT) (Table 2.2). Oksanen et al. (1990) found
up to 350,000 Eimeria opg of faeces in reindeer calves and suggested that
clinical disease would be related to higher numbers of oocysts (>800,000
opg faeces) (Oksanen et al., 1990). In Greenland, extremely high oocyst
counts (up to 990,000 opg) were recorded from calves during a mortality
event. The proximate cause of mortality was an E. coli septicaemia and the
role of Eimeria was not determined (Clausen et al., 1980).
(d) Issues and future research: Knowledge of Eimeria spp. in ungulates
of arctic North America is limited to primarily cross-sectional faecal sur-
veys and a few species descriptions. Survey data, a few case reports, and
preliminary laboratory experiments suggest differing patterns of infec-
tion and abundance among host species, possibly significant pathology
and arctic adaptations such as sporulation of oocysts after freezing. New
DNA-based technologies and morphological studies, together with fur-
ther observational (seasonal faecal surveys and characterization of para-
site diversity and abundance among host species and age/sex classes) and
experimental research are necessary to describe the species diversity, host
range, ecology and significance of Eimeria in the Arctic.
2.6.2. Tissue and blood protozoa: the Sarcocystidae,

Trypansomatidae and Babesiidae
2.6.2.1. Family Sarcocystidae
Besnoitia tarandi, Neospora caninum, Sarcocystis spp. and Toxoplasma gondii
are tissue-dwelling obligatory intracellular parasites of a variety of ver-
tebrate species, including arctic ungulates. The life cycle of these Sarco-
cystidae family members typically relies on predator–prey linkages with
predators as the definitive hosts. For some of these species, however,
vertical and horizontal transmission in the absence of definitive hosts
is possible. Diagnosis is by histological identification of cysts, immuno-
histochemistry, DNA-based techniques or serological tests (Dubey and
Odening, 2001; Leighton and Gajadhar, 2001).
2.6.2.1.1. Besnoitia tarandi

Besnoitia tarandi is a tissue cyst-forming parasite first described in Alaskan
reindeer in 1922 (Hadwen, 1922). Cysts are located in the skin, subcutane-
ous tissue, conjunctiva, sclera, periosteum of long bones and skull, muscle
fascia, testicles and occasionally other soft tissues (Ayroud et al., 1995;
Wobeser, 1976). There are three other species of Besnoitia reported from
‘large mammal’ hosts and these include B. besnoiti, primarily from cattle,
B. bennetti primarily from domestic equids, and B. caprae primarily from
goats (Olias et al., 2011). No significant genetic differences between B.
tarandi and B. besnoiti were identified in one study, but morphological and
biological differences suggested that further investigation with more pre-
cise genetic markers is needed (Olias et al., 2011). Subsequent work sug-
gests the utility of microsatellite markers in discriminating among such
taxa. Significant sampling has identified a stable multilocus genotype
for B. tarandi across the Arctic not precisely replicated in any of several
specimens of B. besnoiti heretofore examined (B. Rosenthal, pers. comm.).
Broader application of this and related methods might prove useful in
determining the duration and consequences of evolutionary differentia-
tion between these and related parasite taxa.
(a) Host and Geographic Distributions: Besnoitia tarandi has a circumarctic
distribution in Rangifer. In North America, it is present in semi-domestic
reindeer and free-ranging woodland and migratory barren-ground cari-
bou populations from AK to Labrador (Table 2.9). Prevalence on the main-
land tends to be higher than on nearby arctic islands and it is absent from
Greenland (Gunn et al., 1991a; Ducrocq, 2011). Rangifer species are the pri-
mary intermediate hosts; however, it has also been reported in muskoxen
on mainland Nunavut, Canada, but not in over 100 muskoxen sampled
on Victoria Island immediately to the north (Gunn et al., 1991a; J. Wu, S.
Kutz, S. Checkley, unpubl. obs.). It also occurs in reindeer in Fennoscan-
dia and Russia (Nikolaevskii, 1961; Rehbinder et al., 1981; Dubey et al.,
TABLE 2.9 Tissue and blood protozoans reported from ungulates of arctic North
America, including Greenland. The range of prevalence reported is indicated below the
parasite name. Only prevalence estimates based on sufficient sample sizes and reliable
diagnostic techniques were included (e.g. data from cursory visual assessment for Sar-
cocystis and Besnoitia were excluded but histological assessment included). Locations/
herds where the parasites were tested for but were absent are indicated by a ‘0’ follow-
ing the location/herd and sample size ‘n’ following in parentheses. Data compiled from

Caribou or reindeer (rd)

Besnoitia tarandi (5–78%) AK Variousa; Western Arctic or Teshepukb;
Porcupinec
NT Mackenzie River Delta (rd) d; Not
specified(rd) e; Cape Bathurstf; Bluenose
Westc
NU Bathurstc; Dolphin-Uniong; Southampton
Islandc
QC Riviere-aux-Feuillesc; Riviere Georgec
Sarcocystis sp. (37.5–100%) AK Adak, Delta, Izembek, Nelchina, Porcupine,
Western Arctic, Wrangell Mountain h,
Variousa,b,i
NT Bluenose West n
NU Victoria Islandg; Bathurstc
QC Riviere George and Feuillesc; Goose Bay and
Hopedalej
Toxoplasma gondii AK North Slope and Alaska Peninsulak; Various,
(0.7–62.5%) Porcupine, Western Arcticl
YT Chisanam
NT Bluenose and Beverly n; southern NTac
NU Bathurst, Dolphin-Union, and North Baffin
Islandn
QC Riviere George and Feuilleso,p
GL Akia-Maniitsoq 0(49); Kangerlussuaq-
Sisimiut 0 (50) q
Neospora caninum AK North Slope and Alaska Peninsulak;
(1.4–15.7%) Porcupine, Western Arctic, Variousl
YT Chisanam
NT Bathurstr
Trypanosoma sp. AK Fairbanks (reindeer from Nome) a
YT Porcupineab
NT South Slaveac
NU Bathurstab
GL Akia-Maniitsoq, Kangerlussuaq-Sisimiutab
(continued)

Dall’s sheep
Sarcocystis spp. (14–77.4%) AK Alaska Range, Brooks Range, McCumber
Creek, Sheep Creek, Tok, Wrangell
Mountainsh; Variousi
NT Mackenzie Mountainss
Toxoplasma gondii (6.9%) AK Interiork
Neospora caninum AK Various 0 (52) b
Trypanosoma sp. NT Mackenzie Mountainsae
Moose
Sarcocystis spp. AK Interior, Holitna River and Nelchina,
McKinley Park, Seward Peninsula, Stikine
River, Unit 13, White Riverh; Variousi
Toxoplasma gondii AK North Slope, Interior and South Central
(1.3–22.7) regionsk; South Central and Interior
regions 0(201)l
Neospora caninum (0.5–2.5) AK South Central and Interior regions 0(201)l;
Not specifiedt
NT Mackenzie Valley Sahtu Settlement Regionu
Trypanosoma sp. AK Not specifiedad
Muskoxen
B. tarandi (32%) NU Kugluktukg; Victoria Island 0(153)v
Sarcocystis spp 80% AK Nunivak Islandh
NT Banks Islandw
NU Ellesmere Islandx
Toxoplasma gondii NT Victoria Island (Holman)y
(4.6–40%) NU Kugluktuk and Victoria Island (Cambridge
Bay)y
Neospora caninum (6–8%) AK Eastern North Slopeb; Not specifiedt
NU Victoria Island (Cambridge Bay)v
a Hadwen (1922).
b Beckmen (2010).
c Ducrocq and Lair (2007), J. Ducrocq, S. Lair, CARMA (unpubl. obs).
d Choquette et al. (1967).
e Lewis (1992).
f Larter (1999).
g Gunn et al. (1991a).
h Neiland (1981).
i Dau (1981).
j Khan and Evans (2006).
k Zarnke et al. (2000).
l Stieve et al. (2010).


m M. Oakley, S. Kutz, R. Farnell (unpubl. obs.).
n Kutz et al. (2001d).
o Leclair and Doidge (2001).
p McDonald et al. (1990).
q P. Curry, Susan Kutz, 2012 S. Kutz, C. Cuyler (unpubl. obs.).
r P. Curry, S. Kutz, CARMA (unpubl. obs.).
s Kutz et al. (2001a).
t Dubey and Thullez (2005).
u C. Kashivakura, S. Kutz, A. Veitch, J. Invik (unpubl. obs.).
v J. Wu, S. Kutz, M. Dumond, S. Checkley (unpubl. obs.).
w Tessaro et al. (1984).
x Samuel and Gray (1974).
y Kutz et al. (2000a).
aa Kingston et al. (1982).
ab D. Schock, S. Kutz, CARMA (unpubl. obs.).
ac Johnson et al. (2010).
ad Kingston (1985).
ae S. Kutz, A. Veitch (unpubl. obs.).
2004; Ducrocq, 2011), and the status of free-ranging reindeer from Iceland
is unknown (R. Thorarinsdottir pers. comm.).
Diagnosis in free-ranging ungulates is typically through gross and his-
tological examination. In caribou, histological evaluation of skin from the
mid-cranial metatarsus for cysts provides a sensitive measure for preva-
lence and intensity of infection (Ducrocq et al. 2012). In the live animal,
hosts with high infection intensities can be identified by visual observation
of parasitic cysts on the ocular conjunctiva but this method significantly
underestimates the true prevalence (sensitivity of 0.29 and specificity of
0.98) (Ducrocq, 2011). A commercial serological assay is available for B.
besnoiti in domestic livestock (Schares et al., 2011) but has not been vali-
dated for B. tarandi or arctic ungulates.
(b) Ecology: The transmission cycle for Besnoitia spp. remains poorly
understood (see Olias et al. 2011 for a review). Feline definitive hosts
have been confirmed for some of the Besnoitia spp. that have small animal
intermediate hosts (e.g. B. darlingi, B. wallacei, B. oryctofelisi, B. neotomofe-
lis); definitive hosts have not been identified for those with large animal
intermediate hosts (B. besnoitia, B. benneti, B. tarandi) (Olias et al., 2011;
Basso et al., 2011). Specifically for B. tarandi, experimental infections of a
limited numbers of dogs, domestic cats, raccoons and an arctic fox were
unable to establish these species as definitive hosts (Glover et al., 1990;
Ayroud et al., 1995; Dubey et al., 2004). Possible alternate definitive hosts
that are present across the range of most affected herds include arctic fox
(Vulpes lagopus), wolverine (Gulo gulo), lynx (Lynx lynx) and wolf (Canis
lupus).
Transmission of Besnoitia sp. by insect vectors has also been hypoth-

esized and tabanids, mosquitoes, tse tse and stable flies were experimen-
tally demonstrated to be competent for mechanical transmission of B.
besnoiti among cattle and between cattle and rabbits (Bigalke, 1968; Olias
et al., 2011). Epidemiological evidence for B. tarandi supports the possibil-
ity of vector-borne transmission but does not rule out carnivore defini-
tive hosts. A study of risk factors associated with B. tarandi infection in
two herds in QC, Canada, demonstrated that the prevalence and inten-
sity of Besnoitia cysts in the metatarsal skin increased from summer to fall
of the same year suggesting summer transmission (Ducrocq, 2011). This
could have occurred as a result of vector-borne transmission but could
also be explained by the presence of a definitive host, which may be more
abundant, and contribute to more environmental contamination on the
summer range compared to the winter range. Vector-borne transmission
was also hypothesized in an outbreak in captive zoo animals that demon-
strated similar temporal patterns of occurrence (Glover et al., 1990).
Importantly, transmission of Besnoitia sp. through insects and defini-
tive hosts are not exclusive of each other. Other modes of transmission
have also been suggested, including migratory birds and the possibility
that large mammals are aberrant hosts and the parasite is really main-
tained by small mammalian intermediate hosts (Olias et al., 2011). The
finding of Besnoitia cysts in tundra mice sympatric with infected reindeer
herds is interesting and raises a question as to how Besnoitia may be circu-
lating in these tundra systems (Nikolaevskii, 1961).
In a recent study of North American migratory caribou herds, Besnoitia
prevalence, based on histological examination of metatarsal skin, was esti-
mated between 5.5 and 44.2% and maximum cyst density was 13.1 cysts/
mm2 (Ducrocq, 2011). Prevalence in males was higher than in females, and
prevalence of infection increased in the first years of life and then decreased
with age (Ducrocq, 2011). Decreases in B. tarandi cyst density over the win-
ter were observed and may be the result of either the elimination of B.
tarandi cysts from the dermis during the winter, or of a lower winter sur-
vival rate of caribou heavily infected by B. tarandi (Ducrocq, 2011). Com-
plete cyst elimination, however, is not known for other Besnoitia sp. and
there is little evidence to support this from histological examination of
more than a thousand caribou where only a few necrotic cysts with associ-
ated inflammatory cells were observed (Ducrocq, 2011).
Although B. tarandi has a wide geographic distribution, significant dis-
ease outbreaks in free-ranging caribou have only been reported recently in
the Rivière-George and Rivière-aux-Feuilles caribou herds in QC and Lab-
rador, Canada (Kutz et al., 2009b; Ducrocq, 2011). The cause of this disease
emergence is not understood, but possible hypotheses include a recent
introduction of B. tarandi to a naïve population, changing environmental
conditions that have allowed increased transmission rates or an increase
in animal susceptibility. Prior to 2007, there was only a single report of

Besnoitia in caribou in QC and this was in 1960 from a herd of unknown
geographical origin (CCWHC, 2011). There were no subsequent records
in the Canadian Cooperative Wildlife Centre (CCWHC) database until
2007 when clinical besnoitiosis emerged in the Quebec herds (Ducrocq
and Lair, 2007). Although the CCWHC data are based on passive surveil-
lance, Besnoitia is routinely reported as an incidental finding in caribou
in other regions of arctic North America and previous lack of detection
in QC suggests absence or very low prevalence. Besnoitia tarandi isolates
from North America apparently do not differ genetically from those in
Fennoscandia (B. Rosenthal, pers. comm.) and may have been introduced
relatively recently to North America through multiple reindeer importa-
tions, primarily to AK, at the turn of the 20th century. Alternatively, this
uniformity may reflect the continuous distributions for Rangifer between
Eurasia and Beringia most recently during the Pleistocene and rapid geo-
graphic expansion in North America during the Holocene. The Rivière-
George and the Rivière-aux-Feuilles herds originate from the North
American lineage, south of the glaciers during the last ice age, and are
physically separated from other migratory caribou herds by Hudson Bay.
Thus, these herds may have been isolated from Besnoitia in both evolution-
ary and ecological time.
(c) Impacts: Clinical signs caused by B. tarandi in caribou range from
asymptomatic to significant clinical illness (Wobeser, 1976; Rehbinder
et al., 1981; Ducrocq and Lair, 2007). Severe pathology in captive caribou,
reindeer and mule deer (O. hemionus) was observed in an outbreak at the
Winnipeg Zoo where the naive status of the animals may have contrib-
uted to the severity of the infection (Glover et al., 1990). Alopecia, skin
thickening, decreased mobility and resistance to movement are reported
for captive and free-ranging caribou with high infection intensities (Wobe-
ser, 1976; Rehbinder et al., 1981; Ducrocq, 2011), and this may increase
susceptibility to predation and reduce thermoregulatory abilities. In
males, B. tarandi cysts can cause severe inflammation and obstruction of
blood vessels in the pampiniform plexus of the testicles (Choquette et al.,
1967; Wobeser, 1976; Ayroud et al., 1995). Decreased or impaired fertil-
ity is reported in bovine and caprine besnoitiosis and this may also be
the case in Rangifer (Kumi-Diaka et al., 1981; Njenga et al., 1999). Testicu-
lar pathology can alter testosterone levels, causing antler malformation
and abnormalities (Blake et al., 1998) that may influence social interac-
tions (Clutton-Brock, 1982) and reproductive success (Thomas and Barry,
2005). Velvet retention and broken antlers have been reported in caribou
infected with Besnoitia (Rehbinder et al., 1981; Ducrocq and Lair, 2007) and
further investigation of this association is warranted. Given the impact on
both survival and reproductive success, this parasite may play an impor-
tant role in population dynamics. Recent population surveys have shown
substantial declines in the Rivière-aux-Feuilles and Rivière-George herds

within the past decades and the potential contribution of Besnoitia to these
declines is not known.
Besnoitia infection in muskoxen is rare but can cause severe pathology
including laminitis and ulcerative dermatitis (Gunn et al., 1991a). Limited
data suggest that infection in muskoxen is more prevalent on the main-
land compared to on arctic islands (Gunn et al., 1991a; J. Wu, S. Kutz, M.
Dumond, S. Checkley unpubl. obs.). The role of caribou in the epidemiol-
ogy of the parasite in muskoxen and other contributing factors for trans-
mission to muskoxen remain unknown.
(d) Issues and future research: Besnoitia tarandi is a common and wide-
spread parasite among subspecies of Rangifer across most of the Arctic.
Recent emergence of this parasite as a significant disease-causing agent
was surprising and highlighted the fact that we know very little about
its life cycle and epidemiology. The emergence of disease in Canadian
caribou coincided with emergence of B. besnoiti and associated disease
in domestic and wild animals in Europe (Mehlhorn et al., 2009), perhaps
raising the question of the possibility of a larger scale driver for the ecol-
ogy of this group of parasites. The lifecycles and epidemiology for both
B. tarandi and B. besnoiti remain virtually unknown, yet given the genetic
similarity between these two species, it follows that information gained
from one may guide the understanding of the other.
Priorities for future research on B. tarandi should include establishing
the parasite’s life cycle, likely a challenge considering that the life cycle of
B. besnoiti, a species with a much higher profile, has not yet been deter-
mined. Experimental studies together with epidemiological modelling
applied to existing data (e.g. Ducrocq, 2011) can be used to elucidate the
lifecycle of this parasite, evaluate the relative contribution of different
transmission pathways and understand the potential impacts of chang-
ing environmental conditions and animal communities on transmission
and disease. Apparent differences in disease occurrence and severity in
caribou and muskoxen across the Arctic, possibly related to differences
between individual hosts and/or host population susceptibility, and eco-
logical conditions, require further exploration. Impacts on individuals,
and how these translate to population-level effects, are important.
2.6.2.1.2. Neospora caninum

Neospora caninum is best known as a parasite of agricultural economic
importance, causing abortion and neonatal mortality in cattle (Dubey
et al., 2007; Andreotti et al., 2010). In livestock, it is transmitted horizon-
tally through a canid-ungulate predator–prey life cycle and vertically
from mother to foetus. Its occurrence and potential significance in wildlife
are increasingly recognized.
(a) Host and Geographic Distributions: Caribou, muskoxen and moose

seropositive for Neospora caninum are reported from AK, YT, NT and NU
(Table 2.9) but the parasite has not yet been isolated from these species.
None of 52 Dall’s sheep tested in AK between 1998 and 2004 were sero-
logically positive (K. Beckmen, unpubl. obs.). Wolves (n = 324, 9.0%) and
coyotes (n = 12, 16.7%), but not red foxes (n = 9), were seropositive in one
survey in AK (Stieve et al., 2010).
(b) Life Cycle: Canids are definitive hosts for N. caninum and a wide
variety of ungulates serve as intermediate hosts. Dogs and wolves are con-
sidered natural hosts, coyotes are demonstrated as suitable hosts experi-
mentally and N. caninum DNA, but not viable organisms, has been isolated
from the faeces of free-ranging coyotes and foxes (McAllister et al., 1998;
Gondim et al., 2004; Wapenaar et al., 2006; Dubey and Schares, 2011).
Seropositivity in remote caribou, moose and muskox populations in
various remote locations across the Arctic (Table 2.9), and competency
of wolves and coyotes as definitive hosts, provides compelling evidence
that N. caninum is a common parasite of sylvatic systems, perhaps pri-
marily, with spill-over to domestic agricultural systems. In many regions
of NT and NU, there are currently no domestic livestock and previous
introductions were limited to very few animals that were maintained in
the settlements by missionaries or traders for very short periods. Histori-
cally, working sled dogs may have been important in the life cycle as they
travelled extensively on the land and were fed wild game. Today, there are
very few working dogs and although these and non-working dogs are still
fed wild game (Salb et al., 2008; Brook et al., 2010), dog travel ‘on the land’
is not as common and opportunities for significant environmental con-
tamination may not be substantial. The few dogs that are brought into the
communities are typically small breeds that are (i) unlikely to have been
exposed to N. caninum previously and (ii) are unlikely to have any signifi-
cant travel outside the northern communities and limited opportunities,
therefore, to be a source of N. caninum for wildlife. Seropositive dogs have
been detected in two northern communities where wild game is a large
component of the diet for more than half of the dogs (Salb et al., 2008).
In caribou from YT and AK, there was no difference in Neospora serop-
revalence between calves and animals aged one year or older, suggesting
transplacental transmission (Stieve et al., 2010). Such a transmission route
may be important in maintaining the parasite under sub-optimal climatic
conditions and in regions with low densities of definitive and/or interme-
diate hosts. In one serological study on moose, exposure to Neospora was
detected but not common (Table 2.9) (Stieve et al., 2010). The low preva-
lence in moose was attributed to their feeding habits: they tend to browse
and eat aquatic vegetation, which could limit exposure to oocysts from
carnivore faeces (Stieve et al., 2010).
(c) Impacts: Clinical signs associated with N. caninum have not been
reported in arctic ungulates, but this may reflect a lack of detection rather
than an absence of disease. The parasite was the cause of mortality in
a wild Californian black-tailed deer fawn (O. h. columbianus), causing
lesions in the lungs, liver and kidney (Woods et al., 1994), and transpla-
cental infection with N. caninum was reported in a stillborn captive Eld’
deer (Cervus eldi siamensis) in Europe (Dubey et al., 1996). In domestic
cattle, N. caninum reduces fertility and causes abortion (Dubey and Lind-
say, 1996; Andreotti et al., 2010) and similar impacts are hypothesized in
free-ranging cervids (Dubey et al., 1996). There is anecdotal evidence that
Neospora may be linked to abortion in captive reindeer. Ninety-two per-
cent seroprevalence for Neospora was observed in a captive reindeer herd
approximately five months after a severe late-term abortion storm. Of the
39 animals (25 females, 14 males) in the herd, only three (two males, one
female) were found to be seronegative (Curry, 2010). The herd also had
a history of multiple pasture intrusions by coyotes during the summer
preceding the abortion storm. Unfortunately, no sera were available from
before the abortion storm to evaluate Neospora exposure (S. Kutz, K.
Orsel, P. Curry unpubl. obs.). Also, seroprevalence for Neospora was 15.8%
in adult females of a declining woodland caribou herd in the YT where
poor early calf survival was considered a major cause of the decline (M.
Oakley, S. Kutz, A. Seller, R. Farnell unpubl. obs.). There were anecdotal
reports of a late-term foetus/stillborn calf and additional weak calves in
the herd in the same year, but the potential contribution of Neospora was
not determined.
(d) Issues and future research: Serological investigation for N. caninum
in arctic ungulates has only been done in recent years and the full extent
of its host and geographic distribution in the Arctic is not well defined.
Isolation of the parasite from definitive and intermediate hosts should
be a priority in order to further characterize and compare these isolates
to those circulating in domestic cycles. It is probable that N. caninum has
reproductive impacts on caribou and other arctic ungulates that could
lead to substantially reduced productivity (i.e. abortion and stillbirths)
but low detectability of carcasses, thus resulting in ‘silent’ population
declines.
Finally, the relative role of different definitive host species (coyotes,
wolves and perhaps foxes and domestic dogs) as well as the contribution
of vertical transmission to maintenance of the parasite in wild host popu-
lations in the Arctic requires further exploration. Climate and landscape
change-related shifts in carnivore communities, such as northern range
expansion of coyotes, may alter the transmission dynamics of the para-
site depending on relative suitability of each of these definitive hosts. The
potential role of red and arctic foxes should also be considered.
2.6.2.1.3. Toxoplasma gondii

Toxoplasma gondii is a pathogenic tissue cyst-forming protozoan with a
global distribution (Dubey and Beattie, 1988). It can cause abortions, foe-
tal abnormalities and neurological disease in a wide range of intermedi-
ate hosts, including people (Dubey and Beattie, 1988). Felids are the only
known definitive hosts for T. gondii but there is a broad range of inter-
mediate hosts (Sibley et al., 2009). Infection of intermediate hosts can be
through ingestion of sporulated oocysts that are shed in the faeces of felids,
transplacental transmission or carnivory. Toxoplasma gondii cysts develop
predominantly in neural and muscular tissues of intermediate hosts. Most
T. gondii isolates can be genotyped into three major clonal lineages (types
I, II, and III) (Sibley et al., 2009).
(a) Host and Geographic Distributions: Toxoplasma gondii appears to be
well established in the Arctic. It has been reported from a variety of terres-
trial and marine mammals and birds, as well as people, around the Arctic
(Table 2.9) (McDonald et al., 1990; Oksanen et al., 1998; Zarnke et al., 2000;
Kutz et al., 2001a; Dubey et al., 2003; Prestrud et al., 2010; Stieve et al.,
2010; Elmore et al., 2011).
Seropositive barren-ground and woodland caribou, muskoxen, Dall’s
sheep and moose are reported from AK to Labrador and from the subarctic
to the arctic islands but not in Greenland (Table 2.9). Similar to Neospora,
the actual parasite has not yet been isolated from arctic ungulates. Prev-
alence of infection in muskoxen and caribou decreases at higher lati-
tudes, from the mainland to the Arctic Archipelago (Kutz et al., 2001a),
and a similar latitudinal gradient is reported for polar bears on Svalbard,
Norway (Jensen et al., 2010). The lineages circulating in North American
arctic ungulates have not been defined.
(b) Ecology: The transmission of T. gondii in Arctic ungulates remains
somewhat enigmatic. Domestic cats are rare and those that are present are
almost exclusively indoors (Prestrud et al., 2010; Stieve et al., 2010). Thus,
with the possible exception of occasional environmental contamination
from kitty litter (e.g. landfills or sewage), it is unlikely that the domestic
cat contributes significantly to the life cycle of the T. gondii in the Arctic
(Zarnke et al., 2000; Prestrud et al., 2010). Lynx (Lynx canadensis) are pres-
ent in the low Arctic and the Subarctic and seroprevalence for Toxoplasma
in this species ranges from 15% to 44% in AK, NT, BC and QC (Zarnke
et al., 2000; (Labelle et al., 2001; Philippa et al., 2004; S. Kutz, R. Mulders,
B. Elkin, JP Dubey, unpubl. obs.). Thus, lynx may serve as definitive hosts
in these regions.
The presence of seropositive caribou and muskoxen on arctic islands
where domestic and wild felids are absent suggests an alternate mode of
transmission at higher latitudes. On the arctic island of Svalbard, a high sero-
prevalence in arctic foxes in the absence of definitive hosts is attributed to pre-
dation on infected migratory geese (Jensen et al., 2010; Prestrud et al., 2010).
Reindeer have been known to eat lemmings, and active or passive exposure
to cysts through contaminated vegetation or ingestion of carrion may be pos-
sible sources of infection for arctic ungulates (Oksanen et al., 2000). Vertical
transmission, as can occur in domestic goats and sheep (Dubey, 1982; Rodger
et al., 2006; Camossi et al., 2010), is another potentially very important means
of infection in arctic ungulates that may allow persistence of Toxoplasma for
multiple generations in the absence of a definitive hosts.
Seroconversion to Toxoplasma gondii increases with age in many wild
animal species (polar bears, arctic fox, wolves and cervids) indicating
cumulative exposure or age-dependant behaviours (Kutz et al., 2000a;
Prestrud et al., 2007; Ankerstedt et al., 2010; Jensen et al., 2010; Jokelainen
et al., 2010). Risk factors for T. gondii exposure in arctic ungulates remain
undefined, but for other species variations in diet and behaviour are
important (Aubert et al., 2010; Jensen et al., 2010).
(c) Impacts: Overt disease caused by T. gondii has not been reported in
free-ranging arctic ungulates, but clinical disease is observed in captive
settings. Two experimentally infected reindeer developed signs of depres-
sion, decreased appetite and haemorrhagic diarrhoea leading to fatal
enteritis in one animal (Oksanen et al., 1996). Transplacental transmission
of T. gondii and subsequent abortion have been reported for a captive mus-
kox and a captive reindeer (Crawford et al., 2000; Dubey et al., 2002). The
impacts of Toxoplasma at the population level remain unknown; however,
if abortion/stillbirth is a consistent feature of this parasite in arctic ungu-
lates, then it may have a significant impact on populations by reducing
lifetime reproductive success. As with Neospora, such an impact would be
subtle and difficult to detect (poor calving rates but no visible carcasses
littering the tundra) yet could have major consequences for population
growth and/or stability.
Toxoplasma in subsistence species may pose a significant zoonotic risk
to aboriginal people, particularly with some traditional food preparation
methods where meat is eaten raw or undercooked and cysts may not be
inactivated. In the past, when wild game formed the core of the diet, pri-
mary exposure to cysts in meat probably occurred at a young age and con-
tinued throughout life. More recently, consumption of wild game is not as
common or consistent, and for some may occur only on special occasions,
meaning that many individuals may not be exposed to the parasite until
later in life. Such shifts in behaviour could increase the chances of primary
exposure occurring during pregnancy with subsequent risk of congenital
toxoplasmosis.
(d) Issues and future research: Although T. gondii may be an important
pathogen of wildlife and people in the Arctic its transmission and impacts
in arctic ungulates, and potential transmission risks from ungulates to peo-
ple, are very poorly understood. In particular, its presence at high arctic
latitudes in the absence of typical definitive hosts suggests alternate trans-
mission pathways that need to be explored (Prestrud et al., 2010). To fur-

ther elucidate the life cycle of T. gondii in the Arctic, parasite isolation and
genotyping, together with studies on virulence and ecology are needed.
Such activities will also provide an insight into the worldwide circulation
of strains and their virulence (Aubert et al., 2010; Prestrud et al., 2010).
Recent evidence from the marine system suggests that T. gondii is
increasing in prevalence (Jensen et al., 2010). Similar studies tracking
trends of T. gondii in arctic ungulates do not exist, although widespread
survey did occur during International Polar Year (Parkinson, 2008).
Emerging threats that may shift the transmission dynamics for T. gon-
dii include a growing human presence in the Arctic that is coupled with
increased environmental contamination through sewage, including bal-
last from cruise ships, waste disposal and increased numbers of domestic
cats (Prestrud et al., 2010). Additional threats under a warming climate
include northern range expansion of possible definitive hosts such as lynx
and cougars (Felis concolor) (Anderson et al., 2010).
2.6.2.1.4. Sarcocystis spp.

(a) Host and Geographic Distributions: Sarcocystis spp. are common in Dall’s
sheep, caribou, moose, muskoxen, and mountain goats in the North
American Arctic, and were detected by gross examination in caribou of
Greenland (Orsel, Cuyler pers. comm). Species diversity in the Nearctic
is poorly defined (Table 2.9), with only Sarcocystis alceslatrans and S. ovalis
described in moose from AB, Canada (Colwell and Mahrt, 1981; Dahlgren
and Gjerde, 2008). The biodiversity of this genus is much better described
for arctic ungulates of the Palaearctic. Sarcocystis ovalis, as well as S. alces,
S. scandinavica and S. hjorti have been described in moose in Norway, and
S. gruehneri, S. rangi, S. tarandivulpes, S. hardangeri, S. rangiferi and S. tarandi
have been described in reindeer in Norway and Iceland (Gudmundsdottir
and Skirnisson, 2006; Dahlgren and Gjerde, 2007; Dahlgren et al., 2008a).
The extent of these species in ungulates of arctic North America is not
known.
(b) Ecology: Sarcocystis spp. use carnivore definitive hosts and herbivore
intermediate hosts. Sexual reproduction occurs in the gastrointestinal tract
of the definitive hosts, and asexual reproduction in the vascular endothe-
lium of the intermediate hosts, leading to tissue cysts in skeletal and car-
diac muscle and the nervous system (Herbert and Smith, 1987). A single
intermediate host can be infected by several different species of Sarcocystis
at the same time (Dubey and Odening, 2001; Dahlgren and Gjerde, 2007).
Canids are definitive hosts of S. alceslatrans found in North American
moose and of at least two and three of the species found in Norwegian
moose and reindeer, respectively (Fayer et al., 1982; Colwell and Mahrt,
1983; Dahlgren et al., 2008b; Dahlgren and Gjerde, 2010a). Potential defini-
tive hosts in the North American Arctic include arctic and red foxes,
wolves, coyotes, black bears, grizzly bears, cougars, lynx, wolverine and
dogs (Neiland, 1981; Mahrt and Colwell, 1980; Dau, 1981; Foreyt, 1989;
Khan and Evans, 2006; Dahlgren and Gjerde, 2010b) Avian scavengers
such as corvids, which are common in the Arctic, may also act as definitive
hosts for some species (Gjerde and Dahlgren, 2010). Sarcocystis spp. in arc-
tic ungulates are not considered zoonotic, but this aspect of their biology
has not been adequately investigated (Tessaro et al., 1994).
(c) Impacts: The impact of Sarcocystis for most arctic ungulates has not
been investigated, but clinical disease associated with Sarcocystis spp. has
been reported in other naturally and experimentally infected cervid spe-
cies. A captive white-tailed deer died, after a week of lethargy, from an
acute necrotizing pneumonia caused by Sarcocystis sp. infection (Duncan
et al., 2000). In Oregon, an epizootic in free-ranging mule deer fawns
reduced growth rate (Dubey and Kistner, 1985). Experimental infections
of elk fawns with Sarcocystis spp., including S. sybillensis and S. wapiti,
resulted in weight loss (Foreyt et al., 1995) and experimental infections
of mule deer fawns with S. hemionilatrantis led to anorexia, weight loss,
pyrexia, weakness and death (Hudkins and Kistner, 1977).
In semi-domestic reindeer, infection with Sarcocystis is a cause of
meat condemnation in Fennoscandia and thus a source of production
loss (Dahlgren and Gjerde, 2007). Changes in protein, moisture and fat
content, as well as increased bacterial contamination, were reported for
buffalo meat infected with sarcocysts (Mostafa and Yasein, 2010), but no
changes in meat quality were reported for bovine meat infected with S.
cruzi (Daugschies et al., 2000). To date, Sarcocystis infection has not been a
cause of meat condemnation in commercial caribou harvests in northern
Canada (B. Elkin, unpubl. obs.).
(d) Issues and future research: The knowledge on Sarcocystis spp. in
ungulates of arctic North American and Greenland is scant. The zoonotic
potential and effects of Sarcocystis spp. on the quality and safety of meat
from game animals in the Arctic is of considerable local importance and
requires further work. The biodiversity, life cycles, host specificity and
impacts are poorly described. Similarly, the potential impacts and conse-
quences of northern range expansion of definitive and intermediate host
species and their Sarcocystis spp. require exploration.
2.6.2.2. Family Trypanosomatidae
2.6.2.2.1. Trypanosoma spp.

Trypanosoma spp. are blood-borne protozoans that parasitize a wide range
of vertebrates globally. They are transmitted by blood-feeding arthropods.
In tropical regions some species, for example, T. congolense, and T. cruzi can
cause severe clinical disease in livestock and people, respectively, whereas
those species in ungulates of temperate and arctic North America are not
considered significant pathogens.
(a) Host and Geographic Distributions. Trypanosoma spp. are widespread
and common in free-ranging ungulates in North America (Kingston, 1981).
They have been morphologically identified as T. cervi, but differences in
biology and infectivity for different hosts, together with absence of molec-
ular characterization of the parasite from various hosts, raises some uncer-
tainty as to whether more than one species circulates in cervids across North
America. Trypanosoma cf. cervi have been detected in the blood of reindeer,
woodland caribou, moose (culture and PCR) and Dall’s sheep in AK, NT,
NU and Greenland (Table 2.9) (Bequaert, 1942; Kingston, 1981 ; Kingston
et al., 1982; Kingston et al., 1985; Lefebvre et al., 1997; Johnson et al., 2010).
Trypanosoma sp., consistent with T. cervi, was detected in a mountain goat
from Montana (Kingston, 1985) and, using amplification and sequenc-
ing of a 550 base pair segment of the 18SrRNA gene, Trypanosoma sp. has
been found in mule deer (SK), ranched elk (AB), Rocky Mountain bighorn
sheep (BC) and wood bison (NT) (D. Schock, S. Kutz unpubl. obs., methods
as per Noyes et al., 1999). Based on blood cultures or microhaematocrit
centrifugation concentration, the prevalence of Trypanosoma sp. in free-
ranging caribou is quite high 72–84% (Lefebvre et al., 1997; Johnson et al.,
2010). There are no reports in muskoxen, which might reflect a lack of sur-
veillance, or could be real and reflect reduced rates of attack on muskoxen
by potential vectors. Trypanosoma sp. in caribou is morphologically similar
to T. cervi, but experimental exposure of two elk to trypanosomes from
Alaskan reindeer did not result in infection (Kingston et al., 1982).
(b) Ecology. In North America, Trypanosoma spp. have been isolated
from deer flies, ticks (Amblyomma americanum) and horse flies (reviewed in
Lefebvre et al. 1997). At least 33 species of tabanid flies are reported in the
Arctic (Teskey, 1988) although the species transmitting Trypanosoma in this
region are unknown. Trypanosoma spp. are present in Greenland where
arthropod diversity is likely quite poor, and investigation of potential vec-
tors in this relatively simple system may provide valuable insight into
transmission (D. Shock, S. Kutz, C. Cuyler unpubl. obs.). Transplacental
transmission of T. cervi in mule deer is documented, but the frequency and
significance of this mode of transmission is not known (Kingston, 1982).
Prevalence of infection appears to be seasonal in reindeer and elk with
highest prevalence based on direct examination, not culture, during mid-
summer and much lower prevalence in the mid to late autumn (Kingston,
1981; Kingston et al., 1982). This summer peak may coincide with vector
abundance and thus enhance opportunities for transmission.
(c) Impacts. No clinical disease has been reported associated with Try-
panosoma in arctic ungulates or wild North American cervids (Kingston
et al., 1982; Kingston and Nikander, 1985).
2.6.2.3. Invasive protozoa

Babesia spp. are apicomplexan protozoans transmitted by ticks, and in the
mammalian hosts, they invade red blood cells to replicate. Natural infec-
tions with Babesia have not been reported in free-ranging arctic ungulates
of North America or Greenland; however, natural infections with Babesia
and significant disease are common in eastern Russia (Rehbinder, 1990).
Babesia odocoilei has been reported from captive woodland caribou, farmed
reindeer and captive muskoxen in the USA (Holman et al., 1994; Holman
et al., 2003; Schoelkopf et al., 2005). It is transmitted by Ixodid ticks but
other possible vectors have been hypothesized in Russia (Zhilyaev, 1977).
In its mammalian hosts, Babesia spp. can cause intravascular hae-
molysis, anaemia, haemoglobinuria and occasionally a secondary toxic
nephritis (Petrini et al., 1995). It almost invariably causes severe disease
in captive Rangifer, with all cases of untreated babesiosis reported in
North American acute and fatal (Holman et al., 1994; Schoelkopf et al.,
2005; Bartlett et al., 2009). It is not known if subclinical babesiosis occurs
in caribou and reindeer (Schoelkopf et al., 2005), as has been observed in
farmed elk (Gallatin et al., 2003) and free-ranging white-tailed deer (Hol-
man et al., 1994; Petrini et al., 1995; Holman et al., 2000). Two acute, fatal
cases of babesiosis have been reported in muskoxen in a zoo in Minnesota.
Babesia odocoilei was identified in these animals using DNA-based tech-
niques (Schoelkopf et al., 2005). There are no published reports of Babesia
in Dall’s sheep, mountain goats or moose (Fig. 2.11).
FIGURE 2.12 Arthropoda reported from ungulates of arctic North America, including
Greenland.
TABLE 2.10 Arthropod parasites in ungulates of arctic North America, including

Greenland. Data compiled from available published and grey literature
Host and Parasite species Location Herd, region or nearest place name
Caribou or reindeer
Hypoderma tarandi AK, NT, All sampled herds and locationsa–g (Note:
NU latitudinal gradient – reduced prevalence at
higher latitudesc)
YT Porcupineb,e, Chisanae
QC/NL Rivière-George herdb,i
GL Kangerlussuaq-Sisimiutb,j,k; Akia-Maniitsoqb
Cephenemyia trompe AK Western Arcticb,d; Mulchatnad, Northern
Alaska Peninsulad, Nelchinad, Teshepukd;
Various tundral
NT Bathurstb
NU Baffin n, Keewatinl; Bernard Harborl
GL Kangerlussuaq-Sisimiutb,j; Akia-Maniitsoqb
Bovicola sp. NT Bluenose Easto
Solenoptes tarandi AK Anaktuvuk Pass of Brooks Range and Utukok
River south of Barrowa
Chorioptes texanus NT Mackenzie Delta reindeerp
Dermacentor albipictus YT Variousq
NT Woodland caribou North Slavef,q
Linguatula arctica AK Unimak Islandr
NU Baffin Islandn
Dall’s sheep
Bovicola jellisoni AK Kenai Peninsulas
Melophagus ovinus AK Unspecifiedt; Chugach Mtnsd; Alaska Ranged
Moose
Dermacentor albipictus YT Variousq
NT Sahtu, South Slave, Deh Chof,q
Muskoxen
Hypoderma tarandi AK Seward Peninsulad
NU Victoria Islandg,h
QC Kuujjuaqu
a Weisser and Kim (1973).
b CARMA, (2011).
c Thomas and Kiliaan (1990).
d K. Beckmen (unpubl. data)
e S. Kutz, M. Oakley (unpubl. data).
f B. Elkin (unpubl. obs.).
g Hughes et al. (2009).
h Gunn et al. (1991a).
i Parker (1981).
j Korsholm and Olesen (1993).
(continued)

k Clausen et al. (1980).
l Bennett and Sabrosky (1962).
m Downes et al. (1985).
n Ferguson (2003).
o C. Kashivakura, B. Kenny, G. Verocai, S. Kutz, A. Veitch (unpubl. obs.).
p Sweatman (1958).
q Kutz et al., (2009b).
r Murie (1926).
s Kim (1977).
t Bequaert (1942).
u M. Simard, S. Kutz (unpubl. obs.).
Despite its potential importance as a significant cause of morbidity

and mortality in caribou and muskoxen, there are no published studies
on Babesia in wild caribou or other arctic ungulates in North America.
The ixodid tick, Dermacentor albipictus, is found on moose and wood-
land caribou in the subarctic (Kutz et al., 2009b) but is a one-host tick
and its competence as a vector for Babesia is unknown. Ixodes scapularis,
the known vector of B. odocoilei, is common in white-tailed deer in tem-
perate regions. In Canada, the currently non-contiguous ranges of this
tick are expanding but the northern boundaries of their range are still a
considerable distance from the Subarctic and Arctic (Steiner et al., 2008;
Ogden et al., 2009). Thus, although white-tailed deer are expanding
their range northwards and may eventually become an important res-
ervoir for B. odocoilei species in the North (Waldrup et al., 1990), it may
be some time before this tick species and Babesia appear in subarctic and
arctic regions.
2.7. ARTHROPODS
The known diversity of ectoparasites of arctic ungulates is relatively simple

and includes only one or two representatives in each of the following fami-
lies: the Oestridae (bots), the Linognathidae and Trichodectidae (lice), the
Psoroptidae (mites) and Ixodidae (ticks), and the Lingulatidae (Fig. 2.12,
Table 2.10). In addition, a number of flies, including members of the Mus-
cidae, such as moose flies (Haematobosca alces), members of the Tabanidae
such as horse flies, members of the Hippoboscidae such as the sheep ked
(Melophagus ovinus) (Bequaert, 1942) and members of the Simulidae and
Culicidae (blackflies and mosquitoes, respectively) are reported across
much of the Arctic but are not discussed here. Caribou have the greatest
diversity of ectoparasites whereas muskoxen have the least and appear to
be primarily accidental hosts.
2.7.1. Diptera
2.7.1.1. Family Oestridae
The Oestridae, nose/throat bots (Cephenemyia trompe) and warbles (Hypo-
derma tarandi) are the most abundant and extensively studied ectoparasites of
arctic ungulates. They are parasites primarily of Rangifer spp. and rarely infest
other ungulate species. They have a Holarctic distribution and are found in
most, but not all, extant Rangifer populations. It is thought that both species
were introduced to west Greenland with reindeer imported from Norway in
1952 (Clausen et al., 1980). Also, the presence of C. trompe on Baffin Island,
NU, appears to be a more recent phenomenon with it first detected on the
southern part of the island in 1997 (Ferguson, 2003). Both species are absent
from translocated reindeer populations in Iceland and South Georgia Island.
Adults of Hypoderma and Cephenemyia are large, robust flies character-
ized by a dense covering of golden and black hairs (Colwell et al., 2006) in
patterns that make them Batesian mimics of several species of bumble bee
(Nilssen et al., 2000; Anderson, 2006). Mimicry of bumblebees presumably
protects the flies from predation by birds (Anderson, 2006). Adults are non-
feeding and must complete all activities using fat reserves built up during
larval development within the host. Females are strong fliers, capable of
flight speeds between 29 and 36km/hr and theoretical flight distances of
up to 330 km (based on flight mill studies) (Nilssen and Anderson, 1995).
First instars are small, translucent white, muscomorph larvae (≈1mm
in length), uniformly covered with small spines (H. tarandi) or slightly
dorso-ventrally flattened and covered with a number of thin spines pri-
marily on the ventral and lateral surfaces (C. trompe). The first instars of H.
tarandi grow to approximately 1cm in length during development beneath
the skin. Second instars are translucent white of up to 1.5cm in length with
widely disbursed short spines on all body surfaces. Third instars are large
(up to 3cm in length) creamy white with all body surfaces having short,
stout, sparsely distributed spines (Colwell et al. 2006). As third instars
near completion of their development, the cuticle becomes increasingly
melanized and mature third instars are almost completely black.
Third instars that have exited the host bury themselves in the sur-
face litter prior to pupariation. These larvae and the puparia are likely to
encounter freezing temperatures and presumably exhibit cold hardiness
similar to other oestrids (Nilssen, 2006). Development within the pupar-
ium is highly temperature dependent, occurring from 10°C to 35°C with
the maximum development rate at approximately 25°C and not increas-
ing between 25°C and the upper limit (Nilssen, 2006). Overall duration of
the pupal period will range from 7 to 80 days. This exquisite temperature
dependence will result in dramatic variation in the timing of adult fly
eclosion between regions and years with differing temperature regimes.
Harassment by oestrid flies can reduce feeding time and lead to

reduced feed intake, reduced summer weight gain, decreased lactation,
reduced calf weights and poorer overall condition that may influence
reproductive success for reindeer (Weladji et al., 2003). The effect of larval
stages on the host, particularly for C. trompe, is less well understood.
2.7.1.1.1. Cephenemyia trompe

(a) Host and Geographic Ranges. Cephenemyia trompe is found throughout
most of the Holarctic, coincident with the distribution of Rangifer. It is con-
sidered host specific to Rangifer although there are reports of this species
from Odocoileus hemionus in central Ontario, (Bennett and Sabrosky, 1962).
Larvae have been reported from most subspecies of Rangifer (Table 2.10).
(b) Ecology. Cephenemyia trompe are ovoviviparous and females emerge
from the puparia with a compliment of 500–1500 fully developed eggs
(Anderson, 2006). Males aggregate at ecologically characteristic sites, usu-
ally treeless hilltops (Downes et al., 1985; Anderson, 2006) to await pass-
ing females with which to mate. Newly mated females rest for several
days, in order for the larvae to develop within a specialized segment of the
oviduct. When larval development is complete, the females must quickly
search for a suitable host as they do not feed and do not supply nutrient to
their larvae. Individual caribou respond to fly approach by dropping their
head to get their nose as close to the ground as possible which may pre-
vent the accurate deposition of larvae. Harassment by adult Cephenemyia
is thought to induce stress responses similar to those induced by blood-
feeding flies. The fly activity period in southern YT extends from June
through August (Downes et al., 1985). Temperature, wind and cloud cover
are the prime regulators of fly activity with the flies remaining inactive
during cool, windy and inclement weather (Anderson and Nilssen, 1996).
In the YT, males were active at temperatures >6°C (Downes et al., 1985).
Females approach the host from below the head and forcibly eject
small groups of first instars precisely on to the upper lip of reindeer hosts
(Anderson and Nilssen, 1990). Larvae migrate along the roof of the mouth
or tongue to the upper respiratory tract where first instar development
is completed. Second instars move to the pharyngeal region where they
develop within the retropharyngeal recesses or pouches. Third instar
development takes place in the same region and at the completion of this
last stage the larvae are coughed up by the host and expelled. The rate
of larval development may be affected by crowding in the host, where
at high intensities development may not be synchronous (Nilssen and
Haugerud, 1994). This often leads to hosts with all three larval stages
present simultaneously. In general, the second instars are first present in
mid-January and third instars will be found from early March. Departure
of third instars from the host begins in late April and may continue until
late June (Nilssen and Haugerud, 1994).
(c) Impacts. Larviposition behaviour alters the normal activity patterns

of caribou (Hagemoen and Reimers, 2002; Anderson, 2006) resulting in
reduced grazing time (Colman et al., 2003) and increased energy expendi-
ture associated with avoidance behaviours. Coupled with the harassment
by Hypoderma tarandi, these flies are a major factor in reduced summer
weight gain, which is crucial to fertility and winter survival, and can have
serious consequences for caribou populations (Hughes et al., 2009). A
model quantifying weather conditions suitable for fly activity has been
developed (Weladji et al., 2003) and could prove useful for predicting the
impact of these flies on caribou at various localities. The impact of larval
stages of Cephenemyia in caribou is not known.
2.7.1.1.2. Hypoderma tarandi

(a) Host and Geographic Distributions. Rangifer spp. are the primary hosts for
H. tarandi although there are a few reports of larvae found in muskoxen
in QC and NU and a moose in Sweden (Zumpt, 1965; Gunn et al., 1991a;
Agren and Chirico, 2005; M. Simard, S. Kutz, unpubl. obs.). Host selection
by ovipositing H. tarandi has not been extensively studied, but indications
from other species in the genus suggest that a combination of visual, olfac-
tory and chemosensory evaluations by the fly restrict the host range. For
example, female cattle grubs, H. lineatum, are very selective as to the diam-
eter of hair shaft to which they will attach eggs (Jones, 2000). The ability of
first instars of H. tarandi to penetrate and survive in hosts other than caribou
is likely limited based on the observation that H. lineatum larvae are inca-
pable of penetrating >1–2mm into mouse skin (D. Colwell unpubl. obs.)
and by failure of the same species to either penetrate or survive in goats
under experimental conditions (Colwell and Otranto, 2006). However, ovi-
position and limited larval survival does occur in non-primary hosts, as
exemplified by H. lineatum infestations in bison and horses (Scharff, 1950).
(b) Ecology. Hypoderma tarandi are oviparous and females emerge from
the puparia with a fully developed set of eggs (300–800/ female, Ander-
son, 2006) and are thus ready to mate almost immediately. Males, which
tend to emerge a few days ahead of females, aggregate at ecologically char-
acteristic sites, usually flat graveled areas with sparse plant growth located
along rivers or streams (Anderson, 2006). Mating occurs at these sites and
females depart in search of suitable hosts. Three factors affect oestrid fly
activity with the requirement that ambient temperature be >10°C, wind
or air speed be <6m/s and cloud cover be <40%. These factors have been
used to successfully predict insect harassment (Moerschel, 1999; Weladji
et al., 2003). Females land on the host and thrust their ovipositors into the
pelage, to near the skin surface, where eggs are attached individually to
the hair shaft using ‘glue’ that reduces loss of the eggs. Development of
larvae within the eggs takes place within 7–10 days and larvae migrate
quickly to the skin surface. Larvae penetrate the skin and reside in the
subcutaneous tissues where they become surrounded by a granuloma

referred to as a ‘warble’. Unlike the species that infest cattle, H. tarandi first
instars do not undergo migrations in the connective tissues deep within
the body. The warble provides a nutrient-rich environment where the lar-
vae complete three instars prior to exiting the host. Larval departure from
the host generally begins in early May and is complete by early to mid-July
(Nilssen and Haugerud, 1994; Nilssen, 2006). Larvae that have exited the
host and the puparia are likely to encounter freezing temperatures; they
presumably exhibit cold hardiness similar to other oestrids (Nilssen, 2006).
(b) Impacts. Adult and larval stages may impact the health of cari-
bou. Individual animals respond to oviposition activities by vigorous
leg stamping, presumably to deter or dislodge the flies. This harassment
is thought to induce stress responses similar to those induced by blood-
feeding flies. Additional impact on the host results from the developing
larval stages during winter. The cost to the host results from the energy
cost of development and maintaining the granuloma (warble) surround-
ing the larvae as well as the cost associated with the development and
maintenance of an immune response (e.g. antibody production). Research
on west Greenland caribou suggests that infestation with H. tarandi is a
significant drain on the energy budget of the host and could threaten the
survival of calves and severely reduce fat deposition in pregnant cows
(Cuyler, et al. 2012) and work on Dolphin-Union caribou, NU, suggests
that increasing warble burdens are negatively associated with the likeli-
hood of pregnancy (Hughes et al., 2009). In other natural systems, it has
been demonstrated that in a situation where food resources are restricted
the larvae can have a major impact on host survival (Milton, 1996). These
observations suggest that, together, adult and larval stages of oestrid flies
may have substantial impact on caribou populations in the Arctic.
Hypoderma tarandi is becoming of increasing concern as a zoonosis
(Lagace-Wiens et al., 2008); in people, it can cause a serious ophthalmo-
myiasis interna, which often leads to loss of the eye. While the condition
has been reported throughout the range of H. tarandi, there is an increasing
occurrence in the Canadian Arctic. Larvae recovered from affected individ-
uals have been early first instars, but the actual mode of infestation is not
clear. Possible routes include oviposition on the human subjects by errant
flies or accidental transfer of newly hatched larvae from the hide of caribou.
2.7.2. Phthiraptera
Blood-feeding and chewing lice are described from caribou, Dall’s sheep
and mountain goats but not from muskoxen or moose (Durden, 2001).
There is, however, little information available on the specific features of
their biology, epizootiology and impact on their hosts. In addition, there
are few published data on the prevalence and intensity of infestation for
any of these hosts. The following details on biology are derived from
information on lice affecting domestic livestock (Price and Graham, 1997).
2.7.2.1. Family Linognathidae
2.7.2.1.1. Solenopotes tarandi

(a) Morphology. Sucking lice are small (usually 1–2mm in length), often blue or
blue–grey in colour, with narrow, pointed heads. They have highly adapted
legs with tarsi modified for grasping hairs on the host’s body. These grasping
‘claws’ help the lice hold their position close to the skin while feeding.
(b) Host and Geographic Distributions. The distribution of S. tarandi is
presumably Holarctic as the original description of this species was from
reindeer in Sweden and it was subsequently identified in barren-ground
caribou in AK (Weisser and Kim, 1973). Solenoptes sp. has not been reported
in moose, muskoxen or Dall’s sheep in the North American Arctic.
(c) Life Cycle. Lice are hemi-metabolous insects with incomplete meta-
morphosis, that is, nymphal stages appear superficially similar to the
adult stages. All life cycle stages are closely associated with their hosts
and they will not survive off the host for long periods. Transmission of
lice occurs by direct contact, although transfer between hosts can occur on
inert objects. Young animals may become infected through transfer from
their dams within a short time after birth.
Both sexes are obligate blood feeders, using small, highly modified
mouthparts that are concealed within the head capsule to obtain numerous
small meals from capillaries in the upper layers of their skin. Data from cattle
feeding species suggest females lay 2–6 eggs per day, which are attached to
the host hair shafts (D. Colwell, unpubl. obs). Eggs complete embryonation
and hatch within 8–11 days of deposition. Lice have three nymphal stages,
which bear a morphological similarity to the sexually mature adult stage.
Each nymphal stage will take 2–4 days to complete. Louse development rate,
at all stages, is highly temperature dependent but is optimal at a narrow tem-
perature range. Temperatures >41°C and 46 °C are lethal for eggs and adults,
respectively, of Linognathus vituli of cattle. Optimal development takes place
between 33 °C and 37 °C. Lice therefore show a seasonal periodicity with
very low numbers in the summer when conditions are hot. Populations begin
to increase as temperatures and solar radiation decline, reaching maximum
levels in late winter. Lice preferentially occupy sites where the host is unable
to groom effectively, but the distribution will become more generalized as
the pelage become thicker during fall and winter.
Knowledge on the ecology of S. tarandi from caribou is limited. In one
study, 36 and 74 lice were found exclusively on the head, predominantly
around the ears and cheeks and anterior part of the neck of two of three cari-
bou sampled in AK in June 1971. With the exception of H. tarandi, no other
ectoparasites were recovered from total hide digests of these animals (Weisser
and Kim, 1973). The authors suggested that the predilection for the head
region could be due to the microclimate in this region. Fur on the head is
much shorter than on most of the rest of the body and lacks the dense under-
fur, thus providing a unique temperature and humidity regime that may be
preferred by the lice (Weisser and Kim, 1973). Predilection for the head may
also be a result of the difficulty in individuals grooming that region effectively.
(d) Impacts. Generally, lice do not cause severe problems in large ungu-
late hosts and given the limited literature available it does not appear that
the blood-feeding lice are of serious concern in ungulates in the Arctic.
Rare cases of host disease have been noted in non-arctic ungulates (Foreyt
et al., 1986) where a species of louse has switched host species.
2.7.2.2. Family Trichodectidae
2.7.2.2.1. Bovicola spp.

(a) Morphology. Chewing lice (Bovicola tarandi, Bovicola jellisoni and Bovic-
ola oreamnidis) are generally small, <2mm in length. These lice are highly
mobile, usually brown or reddish-brown in colour with a characteristi-
cally dorso-ventrally flattened body and broad, rounded head.
(b) Host and Geographic Distributions. Bovicola tarandi are described from
woodland caribou and reindeer, suggesting a Holarctic distribution (Low,
FIGURE 2.13 Dall’s sheep ewe with fur loss. Sheep Mountain, Yukon Territory Canada.
(photograph by S. Kutz, 7 May 2006). (For color version of this figure, the reader is
referred to the web version of this book.)
1976). Bovicola jellisoni is described as infesting Dall’s sheep (Kim, 1977)

but was originally described from bighorn sheep (Emerson, 1962).
(c) Life Cycle. These lice feed on dead skin cells, hair and oil secretions,
which they abrade from the surface using their chewing mouthparts. There
may be some abrasion of the upper skin layers and there has been demon-
stration that sheep develop antibodies to salivary sections of Bovicola ovis
(James et al., 1998). Sex ratios are highly female biased and parthenogenesis
is a common occurrence in many species (Price and Graham, 1997). Females
deposit less than one egg per day. Embryonation is completed in 7–10 days
producing nymphs, which molt three times before reaching sexual matu-
rity. As with the sucking lice, development is highly regulated by tempera-
ture with a narrow range for optimal development and survival. Chewing
lice can survive off the host for up to two weeks under ideal conditions.
Transmission of lice occurs by direct contact, although phoretic transfer of
chewing lice between hosts by flies occurs occasionally (Mertins et al., 2011).
Bovicola jellisoni was described from two of three Dall’s ewes collected
27 April 1971 from the Kenai Peninsula, AK. One animal had 18 lice, and
the second had approximately 19,300 lice, with 85% of the population dis-
tributed on the sides and belly and 13% around the anus (Kim, 1977). A
high proportion (88%) of the louse population were nymphs, 9% female
adults, and the sex ratio was 3:1 female:male.
(d) Impacts. Chewing louse populations tend to be small on individual
hosts and they have little impact on the host, although there are descrip-
tions of hair loss associated with louse infestation on horses (Larsen et al.,
2005). Occasional reports of hair loss on Dall’s sheep occur (Figure 2.13)
(R. Popko, Mackenzie Mountains, pers. comm.; S. Kutz, Sheep Mountain
Yukon, unpubl. obs.), but aetiology has not been determined. Reports of
skin lesions and hair loss in caribou, with the exception of those associated
with Besnoitia are not common (Kutz, 2007).
There is concern that the potential exists for severe impact on naive
hosts when lice are exchanged between host species that have only
recently come into contact. A severe hair loss syndrome has been described
in black-tailed deer resulting from the transfer of Tricholipeurus parallelus
from white-tailed and mule deer (Bildfell et al., 2004; Foreyt et al., 2004).
On black-tailed deer, the populations of T. parallelus were uncharacter-
istically high and the severity of hair loss lead to death in some cases.
Whether the syndrome was the result solely of the lice or a combination of
factors is not entirely clear, but the consequences for the affected deer were
serious. The problem has become of more concern with the report by Mer-
tins et al. (2011) describing the impact of Bovicola tibialis, a louse brought
to North America with Dama dama (fallow deer), on native species of deer.
It appears that the louse has switched to several native cervids with some
ease and is causing severe hair-loss syndrome in many populations and
is thought to be impacting the well-being of the affected populations. A
potential explanation of the hair-loss syndrome could be the exposure to a

new allergen produced by lice to which the host was not adapted. Pfeffer
et al. (2010) have described an allergen produced by sheep lice (Bovicola
ovis) that is responsible for small reactions seen on the skin of infested
sheep and on non-adapted hosts the reactions could be more severe.
2.7.3. Acari
2.7.3.1. Family Psoroptidae
2.7.3.1.1. Chorioptes spp.

(a) Morphology. Chorioptes mites are very small, adults being approximately
0.5mm long. The body is oval with legs bearing single stalked pulvilli that
terminate in a cup-like structure.
(b) Host and Geographic Distributions. Chorioptes texanus is considered
to be relatively non-host specific and capable of infesting a wide range of
wild cervids and domestic livestock. It has been reported from reindeer
(Rangifer tarandus) in Canada (Sweatman, 1958), where it was collected
from the ears, but the distribution is likely Holarctic. Chorioptes has not
been reported from moose in North America, but Chorioptes texanus was
reported from moose in Poland (Kadulski, 1996) and a previously unchar-
acterized pathogenic species has been described from the outer ear canals
of moose in Sweden (Hestvik et al., 2007). Chorioptes sp. was observed from
the lower legs of captive muskoxen (B. Wagner, S. Kutz, unpubl. obs.).
(c) Life Cycle. The life cycle comprises five distinct stages, including
egg, larva, protonymph, tritonymph and adult. Based on information
from C. bovis of domestic livestock, the entire life cycle requires from 19 to
28 days to complete on the host (Baker, 1999). Larval and nymph stages
feed on skin debris.
(d) Impacts. In moose, Chorioptes sp. causes significant epidermal and
dermal inflammatory lesions in the outer ear canals (Hestvik et al., 2007).
In captive muskoxen pruritus, mild scaling and hair loss were observed
on the lower legs (S. Kutz, unpubl. obs.). In cattle, an allergic dermatitis
occurs occasionally leading to focal hair loss around the tail-head while in
other domestic animals the predilection site varies (Yeruham et al. 1999).
2.7.3.2. Family Ixodidae
2.7.3.2.1. Dermacentor albipictus

(a) Morphology. These are medium-sized ticks (3–6mm long) with eyes,
festoons (folds in the posterior margin of the idiosoma), short mouth-
parts and palps with a rectangular basis capitulum. Members of this
Family are characterized by the presence of a dorsal shield, or scu-
tum, which covers nearly all of the body of males but is confined to the
anterior portion in females and immature stages. The openings of the
respiratory system are associated with near tear-drop-shaped spiracular
plates (also known as stigmal plates) that are characteristic for the spe-
cies (Gregson, 1956).
(b) Host and Geographic Distributions. Dermacentor albipictus is broadly
distributed in temperate North America and is reported from a wide
range of hosts including moose, woodland caribou, mountain goat and
bighorn sheep (Allan, 2001). Recently, D. albipictus appears to be expand-
ing its geographic range north in moose, woodland caribou and elk in
NT and YT, and the potential invasion of barren-ground caribou herds
is a significant concern under current climate warming conditions (Kutz
et al., 2009b).
(c) Life Cycle. Dermacentor albipictus is a one-host tick with all blood-
feeding stages occurring on the same host. Gravid females, once having
mated on the host, drop off in April and March. Oviposition begins in
June. Survival of females, eggs and larvae is reduced by exposure to high
temperatures (Drew and Samuel, 1985). Larvae develop over the course of
the summer and may enter a diapause. Diapause is influenced by photope-
riod (Wright, 1969; Wright, 1971) and larvae are found questing at the tips
of vegetation in September and October (Drew and Samuel, 1985). There
is a high degree of cold tolerance in the larvae allowing persistence during
often hostile periods (Gregson, 1956; Samuel and Welch, 1991). Once on
the host, larvae feed and nymphs can be found within three weeks. This
latter stage does not feed until some time later, often January (Drew and
Samuel 1985). The feeding can take place over a long period, extending
to March, in northern latitudes (Samuel and Barker, 1979). Adult ticks are
found on hosts from March through early June.
(d) Impacts. Feeding by D. albipictus has a range of effects on the host
that may be linked to the host susceptibility, grooming behaviour and
intensity of infection. Moose tend to have the highest burdens, infested
by many thousands of ticks (Samuel and Welch, 1991), caribou and elk
can have moderate infections, and deer tend to support very few ticks
(Welch et al., 1990). The feeding activity of ticks induces an intense itch-
ing that stimulates grooming activity. The grooming can result in dra-
matic hair-loss in some host species such as moose, which can culminate
in adverse effects leading to death. Moose die-offs have been associated
with heavy infestations (Allan, 2001). Other species show only mild alo-
pecia.
High intensities of infestation of captive reindeer and woodland cari-
bou are associated alopecia, although the confined nature of the animals
may have contributed to the high tick burdens (Welch et al., 1990; Kutz
et al., 2009b). Small numbers of winter tick have also been reported from a
few free-ranging woodland caribou in northern AB and NT (Welch et al.,

1990; Kutz et al., 2009b).
2.7.4. Crustacea, Pentastomida

2.7.4.1. Family: Linguatulidae
2.7.4.1.1. Linguatula arctica

(a) Morphology. Adult females are large (6–13cm long), dorso-ventrally flat-
tened with numerous pseudo-segments (annuli). In the anterior half, the
annuli are broader than in the caudal half giving the parasites a paddle-
shaped appearance (Riley et al., 1987; Nikander and Saari, 2006). Males
are smaller (3–4cm long) with a slightly smaller number of annuli. The
number of annuli is a diagnostic feature used to separate L. arctica from
the common species infecting canids L. serrata (Riley et al., 1987).
(b) Host and Geographic Distributions. The sinus worms have been
thought of as primarily parasites of semi-domesticated reindeer in the
Palaearctic; however, there are two reports from North America. It was
reported from a caribou (misidentified as L. serrata, a cosmopolitan par-
asite of carnivores) on Unimak Island, the easternmost Aleutian island
in Alaska (Murie, 1926), and more recently from Baffin Island caribou
(Ferguson, 2003). Based on oral histories from indigenous hunters,
Ferguson (2003) suggests that the sinus worms were present on Baffin
Island prior to the introduction of Norwegian reindeer in 1921. These
reports may suggest a Holarctic distribution for the parasite, but the
apparent discontinuous distribution across the North American Arctic
is enigmatic.
(c) Life Cycle. The reindeer sinus worm has a direct life cycle; an
unusual feature for this group that often utilizes intermediate hosts for
the completion of larval development. Adult sinus worms are found in
the nasal cavity of their hosts where they produce embryonated eggs that
are shed from the host in mucous. The eggs are immediately infective to
grazing calves.
(d) Impacts. Most infections with the sinus worm are found in calves
and animals under two years of age suggesting the development of pro-
tective immunity (Riley et al. 1987). There has been no reported effect
on infected animals (Haugerud, 1989) despite the presence of significant
pathology in some animals.
2.7.5. Emerging issues and future research for the Arthropoda

With the exception of the Oestridae, the diversity, host and geographic dis-
tribution and impacts of ectoparasites in ungulates of the North American
Arctic are very poorly defined, consisting primarily of a few case reports
from a few hosts and locations. Caribou appear to have the most and mus-
koxen the least diverse faunas.
The majority of research on host–parasite interactions and on biology
of adult stages has been conducted in the Palaearctic, primarily with the
semi-domesticated reindeer hosts (e.g. C. trompe, H. tarandi and L. arctica).
For the oestrid flies, there is a paucity of data on the biology of the pupal
stages and their response to changes in environment, for example, studies
of the freeze tolerance of mature third instars and pupae are needed. In the
case of H. tarandi, variation in the susceptibility of the various subspecies of
caribou present in North America requires research particularly in light of
the demonstration by Rødven et al. (2009) that the intensity of infestation
was higher in lighter coloured individuals (Nørwegian et al., 2009).
The effects of lice and mites on arctic ungulate hosts remain unknown.
Evidence of high infestation intensities (e.g. B. jellisoni in Dall’s sheep),
hair loss of unknown etiologies, and recent recognition of Chorioptes as an
important pathogen in Scandinavian moose suggest that these parasites
may play an important role in host health.
The lifecycles and transmission dynamics of all the ectoparasites
described above are limited or accelerated by ambient climatic conditions,
in particular temperature and relative humidity, but also wind speed
and cloud cover. Defining current faunal diversity, including host and
geographic distributions, together with establishing thermal tolerances,
thresholds and tipping points, are essential steps to understanding the
potential response of these host–parasite systems to ephemeral climatic
events and long-term climate trends.
2.8. DISCUSSION
2.8.1. Parasites alive and well in arctic ungulates

We have defined and reviewed patterns of biodiversity for a complex, suc-
cessful and geographically widespread parasite fauna in caribou, mus-
koxen, Dall’s sheep and moose of the North American Arctic, including
Greenland. At minimum, this fauna consists of 60 described species of
helminths, arthropods and protozoans yet there remains considerable
undescribed biodiversity and probable cryptic species complexes. For the
few parasites that have been studied in some detail, there is strong evi-
dence that they can have significant impacts on individual health and host
population dynamics. Most of these arctic parasites are highly responsive
to climate and climate change and many have important consequences for
the safety, security (sustainability and availability of wildlife populations)
and quality of country foods on which many northern aboriginal peoples
continue to depend. So what have we learned and where do we need to

go?
2.8.2. Parasite biodiversity

It is abundantly clear that, despite the fact that ungulate species are charis-
matic components of northern ecosystems, there remain many basic ques-
tions regarding the biodiversity and faunal structure for their parasites.
Much of the endemic fauna across the high latitudes of the Nearctic was
established through geographic expansion and colonization from Eurasia
under the influence of various biotic and abiotic filters ovet the last 3 mil-
lion years (Hoberg et al., 2012). This historical perspective sets the stage
for understanding the current diversity and also provides a foundation to
explore biological systems under dynamic change. We are now defining
the faunal assembly and patterns of distribution, recognizing that species
richness tends to decrease at high latitudes and on a west to east gradient,
perhaps coinciding with expansion and invasion from Eurasia into North
America.
Recent and ongoing descriptions of new species and cryptic com-
plexes, diagnoses of new genera and definition of new host or geographic
distributions highlight the significant but hidden diversity of helminths
(Hoberg et al., 1995, 1999; Kutz et al., 2001d; Hoberg et al., 2002; Kutz
et al., 2007; Laaksonen et al., 2010b; Haukisalmi et al., 2011; Hoberg et al.,
in press-a,b) and enteric and tissue cyst-forming protozoans (Gudmunds-
dottir and Skirnisson, 2005; Gudmundsdottir and Skirnisson, 2006; Dahl-
gren et al., 2008a; Kutz et al., 2008; Kutz et al., 2009c) in arctic ungulates.
Although diversity for ectoparasites has been explored minimally, hidden
diversity is probable. Ectoparasites may be highly responsive to climatic
changes and also can be important vectors or intermediate hosts for a vari-
ety of pathogens; thus, there is some urgency to understand this fauna
much better in an Arctic undergoing substantial climate change.
Essential to documenting biodiversity are permanent specimen-based
and archival collections that provide historical baselines for contempo-
rary systems and allow comparison across regions and over time (Hoberg
et al., 2003, 2009). Museum archival collections (specimens and associated
informatics) are the critical foundations for documenting change in north-
ern systems (Hoberg, 2010). Importantly, archival collections are ‘self-cor-
recting’ records, that is, specimens can be re-examined and identifications
re-determined as new information and new technology develops. Such
collections have been essential for redescriptions of species, identification
of cryptic species, and correction of historical records (e.g. Hoberg et al.,
1999; Lichtenfels and Pilitt, 1983a). They have also been key resources for
the development of this manuscript where specimens from previously
published records could be re-examined and reported with the most up to

date taxonomic designations.
2.8.3. Characteristics of arctic parasites – New insights

Parasites of ungulates in the Arctic demonstrate a variety of attributes
that facilitate their persistence in an environment characterized by high
seasonality, extremes of climate and weather (temperature and humidity),
and a generally low abundance and diversity of hosts that varies over
space and time. These factors have operated over both evolutionary and
ecological time, playing critical roles in structuring of the contemporary
parasite fauna (Hoberg, 2012b). Freeze tolerance, arrested development,
overwintering in/on the hosts, large size and high fecundity, long life
spans and defined seasonal characteristics are some of the features that
have ensured the success and often extensive distributions of arctic para-
sites.
2.8.3.1. Freeze tolerance

A key feature of many arctic parasites is their ability to withstand extended
freezing events. Nematodirines and Marshallagia have eggs that are resis-
tant to environmental extremes and subzero temperatures for extended
periods. Both L2 and L3 of O. gruehneri have high overwinter survival on
the arctic tundra. For at least some of the protostrongylids, for example,
U. pallikuukensis and P. odocoilei, both the first-stage larvae in the environ-
ment and developing larvae in gastropod intermediate hosts are able to
overwinter at subzero temperatures; this is predicted also for P. stilesi and
P. andersoni. The cysticerci of T. hydatigena mature within the liver paren-
chyma of arctic ungulates, thus surviving subzero ambient temperatures
longer than more superficial cysticerci that are typical in domestic animals
infected with this cestode. This feature is not described in domestic hosts
and may indicate a behavioural adaptation to subzero temperatures in
sylvatic cycles. At least some species of Eimeria from muskoxen have the
ability to sporulate after extended freezing, an uncommon characteristic
for the Apicomplexans. Freeze tolerance for a number of other parasites
including the tissue forming protozoans (Besnoitia, Toxoplasma, Sarcocystis
and Neospora) and the pupae of Hypoderma and Cephenemyia is unknown
but would certainly be an advantage in the arctic environment.
2.8.3.2. Arrested larval development

Whereas some parasites are able to overwinter in the environment, oth-
ers use a different strategy to survive the extreme cold. Observational
and experimental data demonstrate that arrested larval development is a
dominant feature of the lifecycles for both O. gruehneri and T. boreoarcticus.
Similarly, observational data suggest that Dictyocaulus in muskoxen may

overwinter as fourth-stage larvae in the lungs of calves or yearlings. In
these situations, arrested development over the winter effectively main-
tains the parasites during extended periods of poor environmental condi-
tions and in a hypobiotic state, which conceivably minimizes the energetic
costs to the hosts during periods of possible nutritional stress. Inhibited
development may thus reduce parasite-mediated morbidity and mortal-
ity that would be detrimental to persistence of these directly transmitted
helminths.
Nematodirus alcidis in moose, however, appears to maintain an arrested
larval population throughout the year and this may serve as a ready reser-
voir to replenish the adult population (Fruetel and Lankester, 1988). Such
a strategy may be particularly important in environments where exposure
to infective larvae is erratic and unpredictable, for example, where host
density is low or climatic conditions are variable.
2.8.3.3. Seasonality
Several arctic parasites display very strict seasonal patterns that coincide
with features of host lifecycles and appear to promote their persistence
in the Arctic. For example, the arrested development of O. gruehneri lim-
its egg production, and subsequent availability of infective larvae, to the
spring and summer, a time when parasites are most likely to develop in
the external environment and be transmitted within migratory caribou
populations. In addition, adult nematodes persist in the abomasa of cari-
bou throughout the winter but are not gravid during this time. Quiescence
of these adult nematodes may minimize the parasite cost to the host at
a time when any eggs produced would not likely survive. Preliminary
studies on T. boreoarcticus suggest similar patterns.
2.8.3.4. Prepatent periods, fecundity and lifespans

Prepatent periods in arctic helminth parasites differ across taxa and many
appear to be finely tuned to the seasonality of the arctic environment. The
short prepatent period for Taenia krabbei in the definitive host is considered
a potential adaptation to the short summers, where high rates of predation
on ungulate intermediate hosts during the summer would then lead to
egg production throughout the summer (Sweatman and Henshall, 1962).
In contrast, P. cervi, the rumen fluke, and S. tundra, the peritoneal nema-
tode, have very long prepatent periods where infection in one summer
results in peaks in eggs/microfilaria production the following summer
when arthropod intermediate hosts are available and transmission is
most likely to succeed.
Several arctic-adapted nematode parasites tend to have long prepatent
periods, are larger in body size and longer lived than their temperate and
southern relatives. For example, U. pallikuukensis, which appears to have

indeterminate growth (Kutz et al., 1999), is very large-bodied and long
lived relative to other Muelleriinae lungworms (Hoberg et al., 1995; Kutz
et al., 2001b). Similarly, specimens of T. boreoarcticus are generally consid-
erably larger than those of the closely related T. circumcincta (Hoberg et al.,
1999). Jacobs and Rose (1990) observed large T. circumcincta in domestic
sheep in Greenland and, through experimental studies and cross-infec-
tions, concluded that the large size was more likely a result of environ-
TABLE 2.11 Checklist of parasites confirmed from ungulates of arctic North America,
including Greenland. ‘X’ indicates parasite present in the host in the Arctic and/or
Subarctic
Caribou
Type of Parasite (reindeer) Dall’s sheep Moose Muskoxen
Nematoda (enteric) (15)

Trichostrongylina
Ostertagia gruehneri X X X
Teladorsagia boreoarcticus X X X
Marshallagia marshalli X X X
Nematodirella sp. X
Nematodirella alcidis X X
Nematodirella longissimespiculata X X
Nematodirella gazelli X
Nematodirus archari/andersoni X
Nematodirus davtiani X
Nematodirus helvetianus X
Nematodirus oiratianus/o. interruptus X
Nematodirus spathiger X
Nematodirus tarandi X X
Oxyurina
Skrjabinema tarandi X
Skrjabinema ovis X
Trichinellina
Trichuris spp. X X
Trichuris schumakovitschi X
Total species 15 7 10 1 9
Nematoda (tissue)
Metastrongylina
Dictyocaulus sp. X X
Dictyocaulus eckerti X X
Parelaphostrongylus andersoni X
Parelaphostrongylus odocoilei X X
(continued)
ment 2.11
TABLE in the(continued)
host (in particular, low host immunity) rather than a species
Caribou
Protostrongylus stilesi X X
Protostrongylus rushi X
Varestrongylus sp. nov. X X X
Umingmakstrongylus pallikuukensis X
Spirurina
Rumenfilaria andersoni X
Setaria sp. X
Setaria yehi X X
Onchocerca cervipedis X X
Cestoda
Taenia hydatigena X X X X
Taenia krabbei X X
Taenia arctos X
Echinococcus granulosus X X X
Anoplocephalidae X X X X
Avitellina sp.
Avitellina arctica X
Moniezia sp. X
Moniezia benedeni
Moniezia expansa X
Trematoda
Fascioloides magna X X
Paramphistomum sp. X X
Protozoa (gastrointestinal)
Giardia sp. X X
Giardia duodenalis assemblage A X
Cryptosporidium sp. X X X
Eimeria sp. X X X
E. ahsata X
E. crandallis X
E. dalli X
E. faurei X
E. granulosa X
E. moshati X
E. ninakohlyakimovae X
E. oomingmakensis X
E. ovina X

Caribou
E. parva X
Protozoa (tissue) (5)
Besnoitia tarandi X X
Neospora caninum X X X
Sarcocystis spp. X X X X
Toxoplasma gondii X X X X
Trypanosoma sp. X X X
Arthropod ectoparasites
Cephenemyia trompe X
Hypoderma tarandi X X
Melophagus ovinus X
Bovicola tarandi X
Bovicola jellisoni X
Solenoptes tarandi X
Chorioptes texanus X
Dermacentor albipictus X X
Linguatula arctica X
Total parasite species 60 35 26 18 31
difference from T. circumcincta elsewhere. It is possible that large size may

be a product of both parasite intrinsic characteristics (e.g. genetics) and
host factors. Certainly, reduced host immunity may be an important fac-
tor for arctic ungulates, in particular muskoxen, which appear to be par-
ticularly susceptible to most parasites and parasite-induced disease (e.g.
Alendal and Helle, 1983).
The lifespans of for both O. gruehneri and T. boreoarcticus appear to be
extended, at least two years, an exceptionally long time for this subfamily
of nematodes. Larvae ingested one summer mature the following spring,
produce eggs throughout the summer and persist in the host through the
following winter. Whether they then die or continue to produce eggs the
next summer remains uncertain; however, evidence from experimental
infections suggests that adults of O. gruehneri may survive and produce
eggs for at least two summers. Two reindeer experimentally infected with
a low dose of O. gruehneri and with very minimal opportunity for re-infec-
tion had similar egg counts for two consecutive summer seasons (Hoar
et al., 2012a).
In general, for nematodes, prepatent period is frequently positively
correlated with body size and body size is positively correlated with
egg production (Gemmill et al., 1999; Rowe et al., 2008). Large size and
longevity in the Arctic may allow pulses of high egg/larval production
over short seasonal periods but multiple years. Multi-year lifespans may
ensure maintenance of the parasites over years where environmental con-
ditions are inadequate to support development in the environment or
when host densities or behaviour reduce transmission potential. Indeter-
minate growth, large body size and extended fecundity for infections in
highly vagile ungulates are expected to be correlated with a capacity for
invasion and geographic colonization (Hoberg, 2010; Hoberg, in press b).
2.8.3.5. Generalist life history

Another mechanism for survival in the arctic environment may be a
propensity for a generalist life history. The ability to parasitize several
different host species may provide a buffer if one species declines or is
seasonally unavailable. In our study, of 60 parasites that were identified
to the species level, 26 are able to parasitize more than one species of arc-
tic ungulate (Table 2.11). Caribou, however, generally the most abundant
ungulate across the Arctic, may maintain a few more host-specific para-
sites. For example, Besnoitia, Hypoderma, and Cephenemya, are essentially
host specialists. Although they spill-over into muskoxen on occasion, it is
highly unlikely that they could be maintained in this host.
2.8.4. Exploring characteristics of arctic parasites in a broader

framework
Our review has highlighted that differences among arctic ungulate spe-
cies or ecotypes may be very important determinants of parasite com-
munity diversity and transmission patterns. For example, transmission
of parasites among the highly vagile, migratory caribou may differ sub-
stantially from patterns among the highly philopatric Dall’s sheep. Even
within a host species, biodiversity of parasites and patterns of transmis-
sion are likely to differ, for example, between relatively solitary, low-den-
sity and non-migratory Peary and boreal woodland caribou compared
to migratory barren-ground caribou. As our knowledge of the biodiver-
sity and distribution of parasites among these hosts expands, we can
use meta-analyses to explore how host behaviour and ecology influence
parasite distributions within the relatively simple arctic ecosystem. Such
new investigations should include landscape level assessments of genetic
diversity using appropriate fine-scale markers to explore patterns of
istorical and contemporary isolation and expansion for both hosts and
h
parasites.
Similarly, we are also at a point where broader comparisons among
parasites of arctic, temperate and tropical systems are needed. In particu-
lar, phylogenetically corrected meta-analyses comparing parasite life-his-
tory patterns and characteristics such as direct versus indirect lifecycles,
arrested development, freeze tolerance, body size, length of prepatent
periods and patency, accumulation of parasites and patterns of age preva-
lence/intensity, host associations and host specialists versus generalists
across broad latitudinal gradients are now becoming possible. Such com-
parisons will provide new insights into host–parasite associations and
adaptations and potential responses to different climatic conditions and
environmental perturbations. Clearly, essential for such meta-analyses is
an understanding of diversity and history for ungulate parasite faunas
both in the Arctic and in temperate and tropical zones.
An exciting area of research that remains virtually unexplored in the
Arctic is the biomass of parasites in the ecosystem and their role in food
webs. Parasites are responsible for a complex array of linkages within the
arctic food web (Kutz, 2012) and understanding how they cycle nutrients
through the environment and the relative importance of this in an arc-
tic ecosystem that is nutrient poor compared to a tropical or temperate
system is an important issue. For example, the biomass of warble larvae
in caribou is substantial. These larvae are composed entirely of nutrients
derived from the caribou host. When they pupate in the environment they
may become important components of the food chain as prey for rodents,
birds and other invertebrates, thus translating caribou biomass into a
potentially wide array of terrestrial vertebrates and invertebrates.
2.8.5. Changing polar environments and host–parasite interactions

Polar environments today are changing at an unprecedented rate in
response to climate change and effects of these changes are now evident in
the biosphere (Callaghan et al., 2004; Post et al., 2009). Accelerated climate
change and extreme weather events are influencing the ecology, impacts
and geographic distribution of endemic parasites in the Arctic (Kutz et al.,
2005; Hoberg, 2010; Laaksonen et al., 2010a) and leading to the expand-
ing ranges and emergence of new parasites at high latitudes (Kutz et al.,
2009b).
Responses of host–parasite systems to climatic changes will vary and
will be linked to the specific history of faunal assembly, species diversity,
life-history characteristics, and particular tolerances, thresholds and resil-
ience of parasites and hosts (e.g. Kutz et al., 2009b; Hoberg et al., 2008a;
Hoberg et al., 2012). For example, we may expect arthropod transmitted
parasites to respond rapidly, and for the most part positively, to warming
climatic conditions (e.g. Laaksonen et al., 2010a) whereas directly trans-

mitted parasites may be positively or negatively influenced depending
on their thermal tolerances (Kutz et al., 2009b; Hoar et al., 2012b). Addi-
tionally, parasites transmitted by gastropod, and perhaps arthropod,
intermediate hosts may be sheltered from climatic extremes because of
behavioural thermoregulation by these intermediate hosts and therefore
will respond to a warming climate in a more moderated manner (Kutz
et al., 2009b).
Photoperiod at arctic latitudes may be an important factor influencing
the phenology of parasites (Hueffer et al., 2011). While warming climate
may push the potential for more rapid development rates, photoperiod
may temper these responses. For example, the diapause, and consequently
the questing by larvae of the tick D. albipictus, is strongly influenced by
light regime. Under a constant photoperiod of 8h, larvae attached to hosts
at 4 weeks post hatching whereas larvae maintained at 12 and 16 hours
remained in diapause for 10 and 12 weeks, respectively (Wright, 1969,
1971). Thus, photoperiod has a significant impact on larval questing and,
depending on how climate and photoperiod interact, may limit, or accel-
erate, range expansion of this parasite at in the Arctic. Further exploration
of the interaction between climate and photoperiod with respect to para-
site transmission dynamics is important at high latitudes where both these
abiotic features have a very broad range.
2.8.5.1. The breakdown of ecological barriers

Episodic changes in climate and habitat have historically influenced the
assemblage of arctic ungulates and their parasites (Hoberg, in press b).
Ongoing and increasing anthropogenic changes in the Arctic, including
rapid climate warming, landscape perturbation associated with human
activities and animal translocations, can lead to the breakdown of ecologi-
cal barriers that previously may have separated different host species and/
or restricted the movement of parasites either within the North or between
temperate and arctic species (Hoberg, 2010; Hoberg et al., 2012). Such inva-
sions could lead to shifts in parasite communities and parasite transmis-
sion pathways (e.g. through new intermediate/definitive host species
and/or vectors). Given the general pattern for low host specificity among
parasites of arctic ungulates, emergence of new host–parasite interactions
are expected. This is exemplified by muskox translocation and subsequent
expansion leading to sympatry with Dall’s sheep and infection of musk-
oxen with P. stilesi acquired from sheep. With northward range expansion
of southern host and parasite species, disease emergence in naive northern
species and parasite-mediated competition are potential outcomes. Impor-
tantly though, invasion and establishment of new parasites under warm-
ing climatic conditions is not a foregone conclusion. For each individual
parasite species, numerous ecological conditions, including but not limited

to sufficient densities and spatio-temporal distributions of definitive and
intermediate hosts, suitable climate and appropriate thermal tolerances of
the parasite, need to be met before an invasion could succeed.
Other climate-related changes that may influence the parasite fauna, and
subsequently the health and sustainability of wildlife populations, include
increased colonization of northern regions by people and their domestic
animals and thus the potential for rapid invasions by new parasites. Tour-
ism and dumping of ballast water may also influence systems by introduc-
ing new parasites, such as Giardia, which may be transmissible to wildlife.
2.8.5.2. Loss of parasite biodiversity

Another important potential outcome of climate change for parasites in
the Arctic that has received little attention is that of parasite extinctions. As
environmental conditions change and southern species invade, competi-
tion among invasive and endemic parasite species could lead to displace-
ment, extirpation and even extinction of arctic-adapted parasite species.
Similarly, if arctic host species are threatened by extinction, co-extinction
of any host-specific parasites is a reality. Globally, despite the fact that
many host-specialist parasites are anticipated to go extinct with the extinc-
tion of their hosts, there is currently only one parasite listed on the IUCN
red list – the pygmy hog sucking louse (Hematopinidae: Haematopinus oli-
veri) (Whiteman and Parker, 2005). Loss of endemic parasites may reduce
cross-immunity to invasive species and would reduce interspecific com-
petition for invading parasites; thus, it may facilitate establishment of new
parasites. Such losses would also have downstream effects on food webs
as well as consequences for host health. Finally, extirpation of endemic
parasite species would remove a key element of biodiversity and a win-
dow into the evolutionary past of their hosts (Brooks and Hoberg, 2000;
Hoberg et al., 2003, in press b; Whiteman and Parker, 2005).
2.8.6. Directions forward

In the last 15 years, there has been substantial progress in understanding
the biodiversity and ecological interactions of parasites in arctic ungulates
yet there remain significant knowledge gaps. The relative simplicity of the
Arctic makes it extremely enticing to explore host–parasite interactions
much more thoroughly – a perhaps tangible and achievable goal.
2.8.6.1. Climate change

Climate-driven emergence of new parasites and parasite-induced disease
syndromes in the Arctic have heightened our awareness of the sensitiv-
ity of these systems and the value of the Arctic as a model system for
i nvestigating the impacts of climate change (Hoberg et al., 2003; 2008a;
Kutz et al., 2009b). The development of empirical models for the transmis-
sion patterns of protostrongylids has provided predictive tools for antici-
pating potential effects of climate change on distribution and transmission
rates of this group of parasites (Kutz et al., 2005;Jenkins et al., 2006b). Simi-
larly, the determination of a temperature ‘tipping point’ for emergence of
Setaria has provided a measurable climate indicator that can be used to
predict disease outbreaks for this parasite (Laaksonen et al., 2010a). Ini-
tial research on impacts of directly transmitted nematodes suggests that
responses to climate change may differ substantially from those of the
indirectly transmitted protostrongylids and upper temperature thresh-
olds may become important (Kutz et al., 2009b; Hoar et al., 2012b).
An additional consideration is that directional climate change results in
cumulative or incremental processes over a range of time periods (years to
decades) and on regional scales. These processes may interact with extreme
or idiosyncratic (short-term) climatic events, which can influence the emer-
gence of pathogens and disease across landscapes (Hoberg et al., 2008a).
Further modelling of these systems, integrating climate-related impacts on
free-living parasite stages, together with life-history parameters of para-
sites and hosts, is essential for better understanding potential similarities
and differences in the response of these systems to a shifting climate.
2.8.6.2. Parasite ecology

Limiting our understanding of the ecology of parasites in Arctic ungulates
is our incomplete understanding of many of their lifecycles. In some cases,
transmission pathways remain completely unknown and we currently
draw on what is known for related species to infer possible transmis-
sion routes. For example, Besnoitia may have two divergent transmission
routes – through arthropod vectors or through carnivore definitive hosts
– and the response of the host–parasite system to a changing landscape
will differ depending on the transmission route. For other parasites, the
basic transmission cycle may be known; however, the specific develop-
ment and survival parameters, thermal tolerances, thresholds and tipping
points, and alternate, intermediate, and paratenic hosts and vectors are
undescribed. Clearly, knowledge of the transmission route(s), biotic and
abiotic factors influencing the success of these routes and relative contri-
bution of different pathways when they exist is necessary to understand
the drivers of disease and anticipate pathogen impacts under a changing
landscape and different climate scenarios.
2.8.6.3. Impacts
The consequences of parasite infections and the emergence of parasitic dis-
eases for the sustainability of arctic ungulates are still not well understood.
As we look further and in more depth, however, there is increasing evi-

dence to suggest that these changes may be detrimental to individuals
and host populations (Jenkins et al., 2005b; Irvine, 2006; Laaksonen et al.,
2010a). The studies that have provided the most robust information on
impacts on individuals have been those that are longitudinal experimental
studies where parasites have either been removed (i.e. Svalbard reindeer)
or animals have been experimentally exposed (e.g. P. odocoilei). Coupling
these studies with modelling of host population dynamics (e.g. Svalbard)
has provided an insight into potential impacts at the population level.
While experimental manipulations are extremely useful for explor-
ing impacts of parasites on individuals and populations, the frequently
complex logistics and finances have limited the number of such studies
on free-living populations. Also, the components of host–parasite rela-
tionships generating disease are often complex and intricately linked. It
is important to recognize that sometimes the parasites’ adverse effects on
hosts are not obvious and frequently can be very difficult to detect and
quantify. Also, most ungulates are infected with multiple genera and spe-
cies, and synergies among these might be important in generating disease.
In fact, most data on host–parasite systems in arctic ungulates comes
from cross-sectional post-mortem examinations. Despite inherent con-
straints, such studies can be particularly valuable when they are large,
standardized, and repeated on a regular interval to monitor changes over
time and over geographically disparate regions (e.g. Nielsen and Neiland,
1974; Simmons et al., 2001; Kutz et al., 2012). Data from these studies can
provide robust measures of parasite diversity trends, associations with
other biotic and abiotic conditions and host factors (e.g. population size,
trajectory, demographics, sympatric species). They can also help to iden-
tify associations between parasite diversity and abundance and indicators
of host health, age, sex, pregnancy and other physiological parameters.
While it is difficult to irrefutably determine cause and effect, such studies
can lead to important insights and can be used to recognize new ecological
processes and generate new hypotheses.
2.8.6.4. Monitoring programs

Key to successful, monitoring programs are standardized protocols, effi-
cient field techniques, reliable laboratory assays, user-friendly centralized
and comprehensive databases that have adequate and long-term IT sup-
port, and physical archives of whole specimens and specimen DNA (e.g.
Hoberg et al., 2008a). Additionally, it is crucial that any data released be
sufficient to allow meaningful comparisons within and between studies,
for example, date of sampling (to allow for possible seasonal effects), host
age or age class (to allow for age effects), and sample history (to allow for
storage effects such as freezing). For arctic ungulates, the CircumArctic
Rangifer Monitoring and Assessment network (CARMA) developed such

protocols for Rangifer sampling during International Polar Year (Kutz
et al., 2012). Different levels of field sampling protocols with an increasing
degree of complexity were designed depending on the expertise of the
collector (from lay person through to experienced wildlife disease experts)
and protocols were made publically available on a website. Techniques for
sampling were refined to facilitate scientifically robust and comprehen-
sive sampling. For example, Nobuto filter paper strips were validated for
infectious disease serology and then implemented in the field, thus remov-
ing the need for whole-blood collection and serum separation under field
conditions (Curry 2010; Curry et al., 2011). Application of these protocols
during defined time period across circumpolar Rangifer herds has led to
a much deeper insight into the parasite biodiversity in the Holarctic and
has provided a relatively comprehensive baseline (S. Kutz, J. Ducrocq and
CARMA, 2011, unpubl. obs.). Perhaps limiting the potential future value
of these collections is the absence of a single centralized database that
can manage the data long term, limited capacity of some museums for
archiving specimens and no central repository for archiving of parasite
DNA. The most appropriate collections will involve a large number of
specimens subsampled for both definitive morphospecies identification
and molecular characterization tied to informatics resources for phylog-
eny, ecology and biogeography (Hoberg et al., 2003).
2.8.7. Conclusions
In this review, we have highlighted the current state of knowledge of the
contemporary parasite fauna infecting arctic ungulates of North Amer-
ica and Greenland. Contemporary systems do not exist in an historical
vacuum and understanding the structure of these systems in ecological
time has been, and continues to be, guided by a robust historical founda-
tion. Parasites are key components of arctic ecosystems, bridging trophic
levels and influencing the health and dynamics of wildlife populations.
Although much has been learned, many knowledge gaps remain, related
particularly to parasite faunal structure, the dynamics of the complex
interactions within and among parasite and host communities (includ-
ing invasive fauna) and the population-level impacts on free-ranging
ungulates.
Of equal importance, however, is the very real fact that ungulates play a
key role in the lives of northern aboriginal peoples and changing host–par-
asite dynamics across the North may negatively impact northern residents.
Parasite-mediated population declines could limit availability of arctic ungu-
lates for subsistence or commercial use. Parasitism in individual animals
may be a food safety concern (e.g. Toxoplasma), decrease the quality of the
hides (e.g. warbles) and the meat (e.g. decrease body condition and reduce
amount of highly valued fat), and may make meat aesthetically unpleasing
(e.g. animals with high intensities of Taenia cysts are often discarded) (Kutz
et al., 2009b). In a land where the individual hunter must serve as his/her
own meat inspector, emergence of new disease syndromes can w significant
concerns and uncertainties, resulting in the loss of confidence in country
foods, the loss of cultural traditions, and a reduction in community health.
Arctic ecosystems are undergoing significant perturbations, many of
which have the potential to affect ungulates and other wildlife. Critical
among these is climate warming, which is more marked in the Arctic than
in many other areas of the world. The possible consequences of this warm-
ing for the health and sustainability of the region’s wildlife and people are
difficult to detect, measure and predict. We can take a lesson from the past
across the Arctic, a region strongly influenced by episodic shifts in climate
and where host–parasite systems have diversified under cycles of dynamic
and rapid change. Invasions, accompanied by geographic and host colo-
nization have shaped the structure of diversity that we have documented.
We anticipate that such processes will continue to have a substantial influ-
ence on high latitude systems. Further, it is possible that some effects of
new climate regimes might be mediated through parasites, for many of
which host and geographic distributions, transmission, abundance and
health impacts depend on local and regional environmental conditions.
ACKNOWLEDGEMENTS
Numerous people have contributed to this manuscript. Thanks go the CARMA network, in
particular the wildlife disease experts, wildlife biologists and managers, and the community
members who have collaborated on much of the work presented in this manuscript; Dean
Brown, Sylvia Checkley, Patricia Curry, Nathan deBruyn, Maëlle Gouix, Jesse Invik, Cyntia
Kashivakura, Lynn Klassen, Alessandro Massolo, Karin Orsel, Karin Seeger, Rene Span, Jillian
Steele, Jian Wang, Brent Wagner, Jessica Wu, Jayninn Yue and many others who contributed
to scientific discussions, sample processing and the smooth operations of the Kutz labora-
tory at the University of Calgary Faculty of Veterinary Medicine, and at the Western College
of Veterinary Medicine, University of Saskatchewan; Mathieu Dumond, Luigi Torretti and
Jorgan Bolt (Government of Nunavut); Alasdair Veitch, Richard Popko, Marsha Branigan,
Jan Adamczewski and John Nagy (Government of the NT); Philip Merchant, Michelle Oak-
ley, Rick Farnell, Rick Ward (Yukon Government), and Manon Simard (Nunavik Research
Centre, Quebec) who have contributed many samples and dynamic discussions over the
years; Nathan Pamperin, Jeff Wells and many others with the Alaska Department of Fish and
Game who contributed information and images for this work. We also thank Patricia Pilitt
and Arthur Abrams, Associate Curators at the US National Parasite Collection, ARS, USDA
Beltsville for their contributions to the morphological and molecular characterization of vari-
ous nematode parasites from northern ungulates over the past decade.
Grants to S. Kutz and associated laboratory members contributed to the work that is
presented in this manuscript: NSERC Discovery, NSERC Northern Supplement, NSERC Spe-
cial Opportunities grants; Environment Canada International Polar Year funding; Alberta
Innovates; University of Calgary; Sahtu Renewable Resources Board; Cumulative Impacts
onitoring Program, NWT; Alberta Conservation Association – Grants in Biodiversity; W.

M
Garfield Weston/Wildlife Conservation Society; Northern Scientific Training Program; Arctic
Institute of North America Grant in Aid and Nassivik Centre for Inuit Health. Further, and in
part, this is a contribution of the Beringian Coevolution Project a multi-national research collab-
oration to explore diversity across the roof of the world supported by grants from the National
Science Foundation (DEB 0196095 and 0415668) to J.A. Cook at the Museum of Southwestern
Biology, University of New Mexico and to E.P. Hoberg at the US National Parasite Collection.
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CHAPTER 3
Neorickettsial Endosymbionts
of the Digenea: Diversity,
Transmission and Distribution
Jefferson A. Vaughan, Vasyl V. Tkach
and Stephen E. Greiman

3.2. Taxonomy and Phylogeny of Neorickettsia 256
3.2.1. Systematic position of Neorickettsia 256
3.2.2. Taxonomy and phylogenetic interrelationships
among species of Neorickettsia 258
3.3. Ecology and Transmission of Neorickettsiae 260
3.3.1. Neorickettsia helminthoeca and SPD 261
3.3.2. EFF agent 265
3.3.3. Neorickettsia sennetsu and Sennetsu fever 267
3.3.4. Neorickettsia risticii and PHF 270
3.3.5. SF agent 275
3.3.6. Rainbow trout agent 275
3.3.7. Neorickettsia sp. from needlefish in Cambodia 276
3.3.8. Catfish agents 276
3.4. Geographic distribution of Neorickettsia 277
3.5. Phylogenetic associations between
Neorickettsia and Digenea 283
3.6. Advances in genomics and molecular biology
of Neorickettsia 285
3.7. Gaps in current knowledge and future perspectives 287
References 289

253
254 Jefferson A. Vaughan et al.
Abstract Digeneans are endoparasitic flatworms with complex life cycles

and distinct life stages that parasitize different host species.
Some digenean species harbour bacterial endosymbionts known
as Neorickettsia (Order Rickettsiales, Family Anaplasmataceae).
Neorickettsia occur in all life stages and are maintained by verti-
cal transmission. Far from benign however, Neorickettsia may also
be transmitted horizontally by digenean parasites to their verte-
brate definitive hosts. Once inside, Neorickettsia can infect macro-
phages and other cell types. In some vertebrate species (e.g. dogs,
horses and humans), neorickettsial infections cause severe disease.
Taken from a mostly parasitological perspective, this article sum-
marizes our current knowledge on the transmission ecology of
neorickettsiae, both for pathogenic species and for neorickettsiae
of unknown pathogenicity. In addition, we discuss the diversity,
phylogeny and geographical distribution of neorickettsiae, as well
as their possible evolutionary associations with various groups of
digeneans. Our understanding of neorickettsiae is at an early stage
and there are undoubtedly many more neorickettsial endosymbi-
oses with digeneans waiting to be discovered. Because neorickett-
siae can infect vertebrates, it is particularly important to examine
digenean species that regularly infect humans. Rapid advances in
molecular tools and their application towards bacterial identifica-
tion bode well for our future progress in understanding the biology
of Neorickettsia.
3.1. INTRODUCTION
Today, biologists, healthcare professionals and veterinarians are well

aware that blood-sucking arthropods can serve as biological vectors of
disease. Fewer realize that endoparasitic helminths can also act as vec-
tors of animal and human infectious diseases. However, examples of this
have been known for a long time. Three of the earliest known examples
include turkey blackhead disease caused by a flagellated protist Histomo-
nas meleagridis transmitted, among other ways, by a nematode Heterakis
gallinarum (Graybill and Smith, 1920; Tyzzer, 1934; Ruff et al., 1970); swine
influenza caused by a virus that can also be transmitted by a parasitic
nematode, Metastrongylus apri (Lee, 1971; Shope, 1941, 1943), and salmon
poisoning disease (SPD) caused by a bacterium transmitted by a digenean
Nanophyetus salmincola (Lee, 1971; Philip, 1955).
Transmission of bacterial diseases by digenean parasites was almost
simultaneously and independently discovered on the opposite sides of
the globe during the mid-1950s. In North America, Philip et al. (1953,
1955) found that a lethal dog disease previously well known as ‘salmon
dog poisoning’ is caused by a rickettsial agent transmitted by an intestinal
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution 255
fluke N. salmincola. Meanwhile, Japanese researchers (Fukuda et al., 1954;

Misao and Kobayashi, 1954) discovered that a previously known disease
of unknown aetiology, the Sennetsu fever, is also caused by a new rickett-
sial agent associated with flukes. Philip et al. (1953) erected a new genus,
Neorickettsia, for this new bacterium species.
The genus Neorickettsia (Family: Anaplasmataceae) comprises a small
group of obligate intracellular bacteria normally endosymbiotic within
digeneans. Digenean life cycles are complex and typically involve several
stages parasitizing different host species. Neorickettsiae persist within all
stages of the fluke and thus are maintained through vertical transmission.
Under certain circumstances, adult flukes may pass their neorickettsial
endosymbionts to the vertebrate definitive hosts. Once inside, neorickett-
siae invade and multiply within the cells of the vertebrate. In some ver-
tebrates, neorickettsial infections of macrophages, monocytes and other
cells types lead to severe, sometimes fatal, disease. Currently, there are at
least seven species/genotypes of Neorickettsia and four distinct diseases
attributed to Neorickettsia.
With a few exceptions, studies of Neorickettsia have been traditionally
carried out by bacteriologists, medical and veterinary researchers, while
helminthologists have rarely participated in these research endeavours.
Despite the in-depth research published on different aspects of molecu-
lar biology, immunology, diagnostics and treatment of neorickettsiae and
neorickettsial diseases, the quantitative aspects of transmission of these
bacteria and their ecological and evolutionary interrelationships with
their invertebrate and vertebrate hosts have received much less attention.
Neorickettsia transmission systems are inextricably intertwined with com-
plex multihost life cycles of digeneans. Thus, full elucidation of the trans-
mission patterns of these neglected, but potentially widespread diseases
will require equal participation of helminthologists, rickettsiologists, epi-
demiologists and vector biologists.
Recent progress in molecular techniques, particularly the polymerase
chain reaction (PCR) and DNA sequencing, has made possible the efficient
and reliable detection of Neorickettsia at every step of their circulation,
whether in the digenean host of the neorickettsiae or in the invertebrate
and vertebrate hosts of the digenean. The same technology also allows
for reliable identification of the digeneans, regardless of the stage of their
development. Increasing number of Neorickettsia DNA sequences in the
GenBank and other internationally accessible public databases have facili-
tated rapid comparisons of genotypes discovered in different parts of the
world. Phylogenetic reconstructions of Neorickettsia have revealed new
lineages, in some cases potentially new species. Recent publication of
complete genomes of two Neorickettsia species opens new possibilities for
studies of their evolution and phylogeny, metabolism and treatment of
diseases caused by these bacteria.
Several significant reviews have been published on different aspects

of Neorickettsia and neorickettsial diseases. These reviews usually covered
Neorickettsia as a part of a larger discussion of diseases caused by various
groups within the Anaplasmataceae (Rikihisa, 1991, 2003, 2010; Walker
and Dumler, 1996; Rikihisa et al., 2005) or focused on particular species
of Neorickettsia of veterinary importance (Mulville, 1991; Palmer, 1993;
Madigan and Pusterla, 2000; Headley et al., 2011).
This article primarily focuses on the current knowledge of the trans-
mission ecology, diversity, phylogeny and distribution of neorickettsiae.
We are not covering pathology and therapy, diagnostics and immunology
of neorickettsial diseases nor do we review recent advances in biochemis-
try and molecular biology (comparative genomics and proteomics) to any
significant extent. Readers primarily interested in these topics may refer to
the reviews mentioned above or other relevant publications (e.g. Cordes
et al., 1986; Brouqui and Raoult, 1990; Barnewall et al., 1999; Zhang et al.,
1997, 1998; Rikihisa, 2003; Rikihisa et al., 2004; Hotopp et al., 2006; Lin
et al., 2009; Gibson et al., 2010, 2011).
3.2. TAXONOMY AND PHYLOGENY OF NEORICKETTSIA
3.2.1. Systematic position of Neorickettsia

The classification of rickettsiae and other intracellular bacteria was tra-
ditionally based on biological, morphological or immunological charac-
teristics. Introduction of DNA sequencing has dramatically changed the
field. Among other findings, molecular phylogenies have led to a reor-
ganization of the order Rickettsiales into two families, Rickettsiaceae
and Anaplasmataceae (Dumler et al., 2001). This revision was based
primarily on phylogenetic analyses of 16S ribosomal RNA (rRNA) and
groESL gene sequences. Secondary characters included outer membrane
protein sequences (amino acid or gene sequences) and biological char-
acteristics such as morphology, host cell tropism, disease ecology and
clinical presentation. Neorickettsia is one of the four generally accepted
genera belonging to the family Anaplasmataceae, namely Anaplasma,
Ehrlichia, Wolbachia and Neorickettsia (Dumler et al., 2001; Taillardat-
Bisch et al., 2003; Rikihisa, 2010; Fig. 3.1). Recent publications (Seng
et al., 2009; Rikihisa, 2010) suggest the existence of three to five addi-
tional genera in the family (Fig. 3.2), some of which are not formally
described yet.
All Anaplasmataceae are obligate intracellular bacteria that grow
within membrane-bound vacuoles of host cell origin (=morulae). The gen-
era Anaplasma and Ehrlichia are exclusively tick borne and include species
of medical or veterinary importance. Aegyptianella is also considered by
FIGURE 3.1 Phylogenetic interrelationships among the Anaplasmataceae based on

Bayesian analysis of partial 16S rRNA sequences. (For color version of this figure, the
reader is referred to the web version of this book.)
some as another valid genus of the Anaplasmataceae (e.g. Rikihisa, 2010),

although in our analysis based on partial ribosomal 16S sequences, Aegyp-
tianella clustered together with members of Anaplasma (Fig. 3.1). Both
are transmitted horizontally from tick to vertebrate to tick and vertical
transmission plays little role in their natural cycle. The genus Wolbachia
infects the ovaries of many species of arthropods and filariid nematodes
and is transmitted exclusively through vertical transmission. There are no
known vertebrate hosts of Wolbachia.
The most genetically divergent genus is Neorickettsia with all species
apparently endosymbiotic in digenean flukes. Neorickettsia are unique
among the Anaplasmataceae in that both vertical transmission and hori-
zontal transmission (at least from fluke to vertebrate) have been docu-
mented (Cordy and Gorham, 1950; Gibson et al., 2005). Neorickettsia can be
grown in vitro within certain cell types (e.g. macrophages and monocytes)
of various vertebrate species (e.g. mouse, dog and human).
FIGURE 3.2 Phylogenetic position of the new genotypes of Neorickettsia and two
putative new genera of Anaplasmataceae found by Seng et al. (2009) in the tract of fish
in Southeast Asia (adapted after Seng et al., 2009, with permission).
3.2.2. Taxonomy and phylogenetic interrelationships among

species of Neorickettsia
Presently, there are three published named species and four genotypes
of Neorickettsia, four of which cause distinct diseases, including a human
disease (Table 3.1). In addition, we have recently identified two more
genotypes from digeneans parasitic in North American catfishes (V.V.
Tkach, J.A. Schroeder and J.A. Vaughan, unpublished data; Fig. 3.3).
The separation between species in literature is based primarily on levels
of 16S rRNA sequence divergence (Dumler et al., 2001; Stackebrandt
et al., 2002). Biological differences among the neorickettsial species
are borne out by the fact that different species produce clinical illness
within certain vertebrate species but not in others. At the same time,
different species demonstrate antigenic relatedness, as evidenced by
immunological cross-protection conferred between different neorickett-
sial species. For example, N. sennetsu causes clinical illness in humans
but not horses. However, when horses are inoculated with N. sennetsu,
they become immune against challenge with N. risticii, a species nor-
mally pathogenic to horses (Rikihisa and Jiang, 1988).
Currently, the taxonomy and principles of species differentiation
among Neorickettsia species are far from being stable and universally
agreed upon. For instance, multiple neorickettsial infections in digene-
ans from Korea identified as N. risticii (Chae et al., 2003; Park et al., 2003)
TABLE 3.1 Neorickettsia species/genotypes described in literature and diseases caused by them
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution

Neorickettsia Vertebrates Neorickettsia Vertebrate cell type
species/genotypes Disease affected by disease localization infected Geographic distribution First described
Neorickettsia Sennetsu Humans, rodents Lymph nodes Monocytes, Japan, Malaysia, Laos, Fukuda et al.
sennetsu fever (exp.) endothelium Thailand (1954)
SF agent Not known Mice (exp.), dogs Not known Macrophages Japan Fukuda et al.
(exp.) (1973)
Neorickettsia Salmon Canids Lymph nodes Macrophages North America (Pacific Philip et al.
helminthoeca poisoning slope of Cascade (1953)
Mountains), Brazil
EEF agent Elokomin Bears, dogs (exp.) Lymph nodes Macrophages Northwestern USA Farrell et al.
fluke fever (1973)
Neorickettsia Potomac Horses Large colon Glandular epithelia, USA, Brazil and South Holland et al.
risticii horse fever macrophages, Korea (1985c)
monocytes
Rainbow trout Not known Not known Not known Not known USA – northern Cali- Pusterla et al.
agent fornia (2000)
Neorickettsia sp. Not known Not known Intestine Not known Cambodia Seng et al.
from needlefish (2009)
259
FIGURE 3.3 Phylogenetic tree of currently known species and genotypes of Neorickettsia
resulting from Bayesian analysis of partial 16S rRNA sequences.
may not belong to this species. Based on the levels of sequence homology
of 16S gene provided by these authors, their isolates are more closely
related to the ‘rainbow trout’ genotype of Neorickettsia reported from
North America and, thus, may belong to a phylogenetic lineage different
from that of N. risticii. Although Chae et al. (2003) did not present a phy-
logenetic tree and did not submit sequences to a publicly accessible data-
base, their work demonstrate the potential of finding additional forms
in eastern and southeastern Asia. Our preliminary sampling and screen-
ing of a variety of digenean taxa from North America (V.V. Tkach, J.A.
Schroeder and J.A. Vaughan, unpublished data; Fig. 3.3) demonstrate
that novel lineages of Neorickettsia may exist in other parts of the world
as well.
3.3. ECOLOGY AND TRANSMISSION OF NEORICKETTSIAE
There are four distinct diseases described in the medical/veterinary lit-

erature attributable to Neorickettsia; SPD, Elokomin fluke fever (EFF),
Sennetsu fever and Potomac horse fever (PHF; Table 3.1). The causative
agents for these diseases are generally regarded as separate species based
on differing pathologies, serology, antigenic profiles and DNA sequence
analyses. In addition, there are at least five other species/genotypes of
neorickettsial endosymbionts whose pathogenicity to humans or other
vertebrates is not known. The discovery of non-pathogenic Neorickettsia

genotypes resulted largely from ecological studies targeting the patho-
genic species. For example, studies on sennetsu fever discovered the SF
(abbreviated from Stellantchasmus falcatus) agent and ecological studies on
N. risticii discovered the neorickettsiae provisionally designated as rain-
bow trout agent, catfish agent 1, catfish agent 2 and undefined N. risticii-
like agents.
3.3.1. Neorickettsia helminthoeca and SPD

It was common knowledge among native Americans and white settlers
along the Pacific coast of northern California, Oregon and Washing-
ton that if dogs were allowed to eat the dead or dying ‘spawned out’
salmon, the dogs were likely to become very ill and die. It was assumed
that the fish contained a toxin that was somehow poisonous to dogs,
foxes and coyotes – but not to other fish-eating carnivores such as rac-
coons or mink. Thus, the affliction got its name ‘salmon poisoning of dogs’.
Symptoms include rapid onset of fever and weight loss, accompanied
later by vomiting and black, bloody diarrhoea. If left untreated, death is
almost certain (90% mortality rate) within 2 weeks after onset. Because
of the extreme severity of this disease, concern about SPD among vet-
erinarians and dog owners in the Pacific Northwest persists to the pres-
ent day.
As early as in 1911, Pernot (1911) demonstrated that SPD was not due
to a toxin but instead was caused by an infectious agent. Blood from sick
dogs was injected into healthy dogs. After an incubation period of 2–4 days,
injected dogs developed symptoms characteristic of salmon poisoning.
Serial injections of blood from these dogs into naive dogs also produced
disease with similar symptoms and incubation periods. Furthermore,
the few dogs that managed to survive their illnesses were immune to the
effects of subsequent injections. However, the exact aetiology of the infec-
tion remained unknown until Donham (1925) made a key observation. He
reported that autopsied dogs that died of SPD all harboured minute adult
digenean flukes (later identified as N. salmincola by Chapin, 1926). Don-
ham correctly surmised that the afflicted dogs had acquired their adult
flukes by ingesting fluke cysts (=metacercariae) found in the flesh and
internal organs of local salmonid fish. Furthermore, he speculated that
presence of the fluke was a necessary component of contracting the dis-
ease. Simms et al. (1931a, b, 1932) demonstrated conclusively that metacer-
cariae and adult flukes of locally collected N. salmincola caused SPD when
fed or injected into dogs. They suspected that the infection was rickettsial
or haemosporidian in origin. Their hypothesis was confirmed when Cordy
and Gorham (1950) described intracytoplasmic rickettsial-like organisms
in reticuloendothelial cells from Giemsa-stained lymph node impression
smears taken from a dog that died of salmon poisoning. Philip et al. (1953)
named the agent N. helminthoeca in recognition that it was a new type of
rickettsia and that digeneans were essential to their transmission.
During the 1950s and 1960s, two main groups of researchers studied
the disease. Researchers at Oregon State University (Millemann et al.,
1964; Millemann and Knapp, 1970; Gebhardt et al., 1966; Baldwin et al.,
1967; Nyberg et al., 1967 Schlegel et al., 1968) conducted ecological stud-
ies on the digenean parasite and its intermediate and definitive hosts. At
the National Institutes of Health Rocky Mountain Laboratory in Hamilton
MT, C.B. Philip and his colleagues performed studies on the transmis-
sion and pathology of the aetiology agent (Philip at al., 1954a, b; Philip,
1955). From the work of these and others, it is now known that the disease
agent, N. helminthoeca, is found in all life stages of the digenean parasite,
N. salmincola (Fig. 3.4 for fluke life cycle; Bennington and Pratt, 1960).
FIGURE 3.4 Circulation of Neorickettsia helminthoeca (white dots) through life cycle
of its digenean host, Nanophyetus salmincola. Images by T. Dieter (snail) and T. Saxby
(trout), Integration and Application Network, University of Maryland Center for Environ-
mental Science (ian.umces.edu/imagelibrary/). Images of raccoon and dog are from the
clipart library sold with CorelDraw X4 software package. (For color version of this figure,
the reader is referred to the web version of this book.)
In nature, dogs acquire infections by consuming fish containing N. sal-

mincola-infected metacercariae. When dogs eat infected fish, the ingested
fluke metacercariae mature to adults deep within the mucosa of the upper
portion of the small intestine. Adult worms begin producing eggs in 5–10
days, which corresponds closely to the normal prepatent period of SPD
symptoms in dogs. The mechanism by which neorickettsial organisms are
transferred from the developing fluke to intestinal tissues and into macro-
phages of the dog is unknown. If left untreated, most dogs die within 6–10
days after onset of clinical symptoms. During the rapid course of disease,
gross pathology is largely restricted to the visceral lymph nodes, which
present as enlarged and fleshy, often with areas of haemorrhage and necro-
sis. The relatively mild pathology induced by SPD belies its severe and
lethal consequences, suggesting that N. helminthoeca possesses a highly
potent virulence factor(s) (Philip et al. 1954a). Yet, experimental infections
with SPD fail to produce more than a transient fever in other non-canid
mammals, including raccoons, bears, mink, bobcats, domestic cats, guinea
pigs, rats, mice or hamsters (Cordy and Gorham 1950, Simms et al. 1931b;
Simms et al., 1932). Humans can be infected with the fluke (Eastburn et al.
1987; Harrell and Deardorff 1990) but are apparently refractory to the dis-
ease. Philip (1955) infected himself by eating raw metacercarial-infected
trout, samples of which produced a fatal infection when fed to a dog. He
suffered no ill effects, but some parasites did attain maturity as evidenced
by the appearance of a few eggs in his stool 10 days after ingestion of the
raw fish.
Indeed, because of the unique pathogenicity of SPD against canids,
wildlife biologists have investigated the feasibility of using fish from SPD-
endemic regions as a possible alternative to traditional poisoned baits to
control coyotes, Canis latrans (Foreyt and Thorson, 1982, Foreyt et al., 1987;
Green et al., 1986; Foreyt and Gorham, 1988). Dogs, foxes and coyotes that
recover from SPD, either naturally or via antibiotic therapy, are immune
to subsequent infection (Simms et al. 1931a). However, the flukes in their
intestines continue to harbour infectious neorickettsiae and convalescent
dogs may continue to shed neorickettsia-infected fluke eggs in their faeces
(Philip et al 1954b).
In the laboratory, SPD has been transmitted experimentally from dog
to dog by intra-peritoneal injection of blood or lymph node homogenates
prepared from sick dogs (pre-patent period = 2–4 days; Philip et al. 1954b).
During experiments to determine if SPD could be transmitted among
dogs by direct contact, Bosman et al. (1970) successfully infected dogs via
aerosolization and enemas of lymph node suspensions and rectal mucosa
homogenates. This indicated that in theory, SPD could be communicable.
However, contagious infection within a natural setting is probably rare
because Sims (1932) reported that over the course of 7 years, over 100
susceptible dogs were maintained in kennels together with dogs infected
with SPD and in no instance was SPD transmitted to susceptible dogs by

such contact. This is in spite of the fact that SPD-stricken dogs produce
vomit and diarrhoea.
SPD has also been transmitted experimentally from fluke to dog by
intra-peritoneal injection of whole and macerated adult flukes (pre-patent
period = 6–7 days) and of snail tissue containing rediae (pre-patent period
of 28–33 days; Philip et al. 1954a). The disease was also successfully trans-
mitted by injecting dogs with fluke eggs homogenized in glass tissue
grinder – but not with intact eggs – indicating that infectious neorickett-
siae are contained within the interior of the unembryonated N. salmincola
eggs but not on the exterior surfaces of the egg shells (Nyberg et al. 1967).
This was conclusive proof that N. helminthoeca is transmitted transovari-
ally to successive generations of digeneans.
Until recently, SPD was considered to be restricted exclusively to west-
ern United States and Canada, ranging from the Pacific coast westward
to the Cascade Mountains and longitudinally from southern Vancouver
Island (Booth et al. 1984) to the Sacramento River of northwest Califor-
nia (Sykes et al. 2010). However, N. helminthoeca has also been confirmed
recently in south-central Brazil using immunological and molecular tech-
niques (Headley et al 2004, 2009). This indicates that there is an alternative
life cycle for SPD and that it is more widespread than previously appreci-
ated. The fluke species responsible for SPD transmission in Brazil remains
unknown. In North America, SPD is only transmitted by N. salmincola.
Thus, the geographic distribution of SPD is constrained by the distribu-
tion of N. salmincola that is in turn determined solely by the distribution
of the fluke’s first intermediate host, Juga silicula (Family: Pleuroceridae).
This snail species (sometimes referred to as Oxytrema silicula) is common
in streams and rivers of the Pacific Northwest but is found nowhere else
(Bennington and Pratt 1960). Although J. silicula serves as a host to several
other digenean species (including Acanthatrium oregonense, which har-
bours a different Neorickettsia species – see N. risticii below), the asexual
development and production of cercariae by N. salmincola can only occur
in this snail species (Millemann and Knapp 1970).
Juga silicula snails become infected after N. salmincola eggs hatch and
miracidium penetrates the snail. Over several months, digenean rediae
within the snail undergo numerous asexual generations and eventually
produce thousands of stub-tailed xiphidiocercariae, which are shed into
the surrounding water. Presumably, the neorickettsiae proliferate in tan-
dem with their larval digenean hosts within the snail. Upon contact with
salmonid fish, the xiphidiocercariae of N. salmincola rapidly penetrate
the skin and move into muscle and viscera of the fish where they encyst
and enter the metacercaria stage. Salmon generally acquire N. salmincola
metacercarial parasites during their years as young fish in freshwater.
Neorickettsiae within N. salmincola metacercariae have been shown to remain
viable for at least 3 years during the oceanic phase of the salmon life cycle
(Farrell et al. 1964). Thus, dogs can acquire SPD by eating fingerlings,
smolts or ocean-caught adult fish (Millemann et al. 1964). Cooking or
freezing (–20°C, 24h) the fish kills both the parasite and the neorickettsial
endosymbiont, although SPD has been reportedly transmitted through
smoked (kippered) salmon (Farrell et al. 1968, 1974). Nanophyetus salmin-
cola metacercariae have been found naturally infecting other types of fish
besides salmonids (e.g. shiner, sculpin and lamprey) and N. salmincola
cercariae have been demonstrated experimentally to penetrate and form
metacercariae in even more fish species and even a salamander (Gebhardt
et al., 1966). Thus, the potential for canids to contract SPD goes beyond
just eating raw salmon or trout.
Adult N. salmincola flukes have been found to occur naturally in the
intestines of 12 species of mammals and 3 species of piscivorous birds in
western Oregon, USA (Schlegel et al. 1968). However, parasite loads in
many of the species were low. Raccoons and spotted skunks were con-
sidered to be the principal definitive hosts of N. salmincola based on their
abundance, their propensity to eat fish and defecate in or near the water
and the high prevalence (100% and 75%, respectively) and intensities of
fluke infections (average of 57,571 and 2613 flukes per animal, respec-
tively) in these species. Although raccoons do not become clinically ill
with SPD, Philip (1955) reported that a suspension of ca. 500 adult N.
salmincola flukes taken from a raccoon at necropsy caused a characteris-
tic fatal infection of SPD when injected into a dog. Thus, neorickettsial
endosymbionts retain their viability within adult flukes, regardless of
whether the fluke parasitizes a neorickettsia-susceptible canid or a neor-
ickettsial-refractory non-canid host. This indicates that raccoons and pos-
sibly many other vertebrate species, contribute to the natural cycling of N.
helminthoeca, and dogs, although victims of disease, are not required for
maintenance of the neorickettsiae.
Interestingly, a close relative of N. salmincola, namely N. schikhobalowi,
infects fish-eating mammals, including humans, living alongside the
Amur and Ussuri Rivers of southeastern Siberia. The ecology of the fluke
is similar to its sister species in the Pacific Northwest, yet SPD is not
known in the region and the local dogs eat raw fish and carry adult flukes
in their intestines (Filimonova, 1963). This suggests that Asian species of
the Nanophyetus fluke do not harbour neorickettsiae or if they do, they
harbour a different species of Neorickettsia that is non-pathogenic to dogs.
3.3.2. EFF agent

In 1973, Farrell and colleagues published a series of papers describing what
they designated as a second neorickettsial agent transmitted by the same
fluke vector, N. salmincola (Farrell et al., 1973; Sakawa et al., 1973; Kitao
et al., 1973). Their original purpose was to determine if black bears, Ursus
americanus (proven earlier to be refractory to SPD), could act as the natural
reservoirs of SPD. Metacercarial-infected trout were fed to six captive bears,
four of which developed fever, anorexia and ‘lassitude’. Upon autopsy, the
sick bears had swollen mesenteric lymph nodes suggestive of salmon poi-
soning. Three of the bears had detectable rickettsial bodies in lymph node
impression smears. Upon injection of individual lymph suspensions from
five autopsied bears into groups of four to six dogs each, 72% of the dogs
developed low-grade fever and diarrhoea for 4–12 days but did not die.
Serial passage of blood during the febrile state into fresh dogs produced
similar, mild symptoms. When convalescent dogs were then fed metacer-
caria-infected trout 3 months later, 87% died of SPD. Because the clinical
symptoms differed and there was lack of conferred immunity between the
two diseases, Farrell et al. named the disease ‘Elokomin fluke fever’ (EFF)
because the source of the infective trout was the Elokomin River, a tribu-
tary of the Columbia River near its mouth in Washington state. Later stud-
ies confirmed that EFF agent was immunologically distinguishable from
both N. helminthoeca and N. sennetsu (see below) by complement fixation
(Sakawa et al., 1973), immunofluorescent antibody tests and live animal
challenges (Kitao et al., 1973). Farrell et al. (1973) considered EFF and
N. helminthoeca to be a disease complex and indeed the EFF agent has been
provisionally designated as N. elokominica in the Merck Veterinary Manual.
No further work has been published on the EFF agent. Recently, how-
ever, Gai and Marks (2008) reported salmon dog poisoning in two cap-
tive sun bears (U. malayanus) that developed disease upon eating fresh
trout wild caught in Northern California. Both bears developed symp-
toms (vomiting, diarrhoea, anorexia and lethargy) consistent with those
observed in dogs sick with SPD. Foecal samples from sick bears contained
eggs of N. salmincola, the fluke responsible for transmission of SPD. The
authors concluded that the disease was SPD. It can be the case consid-
ering that sun bears as a species presumably have not had exposure to
N. helminthoeca throughout the course of their evolution and may not
have well-pronounced immunity to this disease agent. At the same time,
as mentioned above, it has been experimentally proven that black bears
native to the region do not develop such severe disease upon exposure to
N. helminthoeca. The symptoms described by Gai and Marks (2008) are also
strongly reminiscent of the symptoms described by Farrell et al. (1973) for
the EFF. Thus, it cannot be excluded that the disease described by Gai and
Marks (2008) could have actually been EFF. Since no DNA sequences were
obtained in either case, it is difficult at present to judge on the identity of
these diseases and their respective agents. Regardless, feeding raw salmo-
nid fish from SPD-endemic areas to various species of bears (e.g. sun bears
and polar bears) remains an important veterinary concern for zoos that
maintain captive bears (Bourne et al., 2010).
3.3.3. Neorickettsia sennetsu and Sennetsu fever

About the same time that early studies on SPD were conducted in the
United States, Japanese scientists were investigating the cause of an acute,
incapacitating rickettsial mononucleosis of humans that had a variety of
local names – Sennetsu, Hyuga or Kagami fevers – endemic to Miyazaki
Prefecture in western Kyushu, Japan (Fukuda et al., 1954; Misao and
Kobayashi, 1954, 1955; Misao and Katsuta, 1956). Symptoms include
high fever, enlarged postauricular and posterior cervical lymph nodes,
malaise, anorexia and peripheral blood mononucleosis. Hepatospleno-
megaly occurs in some patients. Disease lasts up to 2 weeks; fatalities
are unknown (Misao, Katsuta, 1956; Tachibana, 1986). Epidemiological
studies suggested that the disease is acquired by eating raw grey mullet
fish (Mugil cephalus) infected with metacercariae (Fukuda, 1958). When
96 human volunteers ate metacercaria-infected raw mullet captured from
the Oyodo River, 5 of the volunteers developed clinical symptoms of the
disease (Fukuda et al., 1962). The agent was named Neorickettsia (formerly
Ehrlichia) sennetsu. Neorickettsia sennetsu was isolated from patients and
later from fish, but it was never isolated from metacercariae, nor was the
fluke host ever identified. Later, the agent of this disease was reported
from patients in Malaysia (Holland et al., 1985b; Ristic, 1990; Weiss et al,
1990). Monkeys, rodents and dogs can be successfully infected experimen-
tally and develop multiple symptoms and enlarged lymph nodes (Fukuda
et al., 1954; Ohtaki and Shishido, 1965; Holland et al., 1985b). Interestingly,
the disease has not been reported from Japan for a long time. However,
N. sennetsu was successfully propagated in primary canine blood mono-
cyte cultures that allowed to develop an immunological test that revealed
numerous N. sennetsu infections among patients with fevers of unknown
origin in Malaysia (Holland et al., 1985b).
A recent study (Newton et al., 2009) revealed that a high seropreva-
lence of N. sennetsu (17% of 1132 patients) occurs in Vientiane municipality
and Savannakhet Province in Laos. Newton et al. (2009) concluded that
sennetsu neorickettsiosis is a common infection in Laos. The same study
showed a 4% seroprevalence in patients in Thailand. It should be noted
that only 1 of 91 buffy coat samples from patients with non-malarious
undifferentiated fever was PCR positive for N. sennetsu. Sequences of PCR
products of three different genes obtained from the human patient sample
were 100% identical to previously published sequences of N. sennetsu
strain Miyayama. Newton et al. (2009) considered it possible that at least
some of the seropositive samples found in their survey resulted from
exposure to organisms closely related to N. sennetsu, but not N. sennetsu.
Laos is a country where raw fish is commonly consumed and fish-borne
intestinal and hepatic digenean infections are prevalent (Chai et al., 2005b,
2007; 2009a, b; Hortle, 2007; Sayasone et al., 2009a, b; Andrews et al., 2008;
TABLE 3.2 Species diversity and worm burden of digenean-infected people living
within two known Neorickettsia sennetsu endemic regions of Laos, 2002–2004
Prevalence of infection (%), mean intensity of infection
Species composition Vientiane (n = 18) Savannakhet (n = 29) Total (n = 47)
Opisthorchis viverrini 100%, 26 76%, 35 70%, 30

Haplorchis taichui 89%, 10 69%, 11 63%, 11
H. pumilio 6%, 1 10%, 18 7%, 9
H. yokogawai 11%, 31 7%, 1 7%, 7
Centrocestus caninus 17%, 1 0%,0 5%, 1
Echinostomatidae spp. 0%, 0 10%, 23 5%, 23
Prosthodendrium 28%, 2 41%, 10 30%, 6
molenkampi
Phaneropsolus bonnei 0%, 0 10%, 8 5%, 8
Dual infections (two 44% 34% 38%
digenean species)
Polyparasitism (three or 44% 31% 36%
more digenean spp.)
(data from Chai et al., 2005b, 2007)
Rim et al., 2008; Table 3.2). Therefore, Newton et al. (2009) screened local
fish for Neorickettsia using standard and real-time PCR (RT-PCR) targeting
the 16S rRNA gene. After screening 238 samples and impressive 88 fish
species including 10 fish species most commonly consumed in and around
the Laos capital Vientiane, Newton et al. (2009) discovered Neorickettsia
infections in three fish species, namely the dwarf snakehead fish (Channa
gachua), the croaking gourami (Trichopsis vittata) and the climbing perch
(Anabas testudineus). While the sequences from the first two fishes were
significantly different from the sequence of N. sennetsu (92.2% and 95.8%
homology), the sequence from A. testudineus showed 99.1% homology with
the previously published sequence of N. sennetsu strain Miyayama. The
results were confirmed with RT-PCR using two additional genes frequently
used in Neorickettsia systematics, namely gltA and Omp85. Newton et al.
(2009) presented a phylogenetic analysis showing that the samples from
the human patient and A. testudineus clustered together with N. sennetsu.
Sequences from the other two fish species (C. gachua and T. vittata) were
positioned basal to all Neorickettsia. These recent findings of up to four new
forms of Anaplasmataceae in fish from the same region by Newton et al.
(2009) and Seng et al. (2009) clearly indicate that there is yet much to be
learnt about these bacteria, their diversity and diseases caused by them.
Coincidentally with the study of Newton et al. (2009), scientists in
the Korean–Laos Cooperation Project on Parasite Control in Lao PDR
conducted extensive parasitological surveys along the Mekong River,
including four villages in Vientiane and four villages in Savannakhet

Province (Chai et al., 2005a, b, 2007). Their survey revealed that 62% of
1580 examined people had active digenean infections. Combining the anti-
Neorickettsia serology and the digenean prevalence data suggests that 27%
of the digenean infections that occurred in Vientiane and Savannakhet
Provinces during 2001–2003 could have resulted in neorickettsioses – i.e.
17% overall anti-sennetsu seropositivity (Newton et al., 2009) divided by
62% overall digenean parasitism (Chai et al., 2005b,s 2007). It means that
over a quarter of all food-borne digenean infections in these two Laotian
provinces could have resulted in neorickettsioses.
The Korean–Laotian collaborative study found at least seven digenean
species present and 75% of infected people were parasitized by more than
one digenean species (Table 3.2). Most infected people harboured a few
dozen flukes, while some others harboured hundreds, even thousands.
Although the relative contribution of species varied by location, three spe-
cies dominated in all locations – a liver fluke, Opisthorchis viverrini (Opis-
thorchiidae) and two intestinal flukes, Haplorchis taichui (Heterophyidae)
and Prosthodendrium molenkampi (Lecithodendriidae). The first two are
acquired from eating raw fish (Chai et al., 2009b). The third species,
Pr. molenkampi, uses dragonfly nymphs as second intermediate host
(Manning and Lertprasert, 1973). Taking into account that insects are
known to host other species/genotypes of Neorickettsia, it cannot be
excluded that arthropods may represent another potential source of
human neorickettsial infections. Considering the extremely widespread
consumption of raw or undercooked fish products in the region, as well as
common use of various invertebrates (crustaceans, insects and molluscs)
as food (Chai et al., 2005a, b; Hortle, 2007), human neorickettsioses are
probably more common in this part of the world than currently known.
Nearly nothing is known about distribution of N. sennetsu among
mammals other than humans, with the exception of a single report from
rodents in Japan (Fukuda et al., 1962). Taking into account the known
pathogenicity of N. sennetsu in some non-human mammals resulting
from experimental infections (see above), it cannot be excluded that this
agent may cause disease in wild animals as well. Unfortunately, our
knowledge of the ecology of N. sennetsu and other related genotypes is
rather marginal. The thorough study done by Newton et al. (2009) that
resulted in multiple records of Neorickettsia in fish did not incriminate
any digenean species. Considering the extremely diverse traditional
diets in the region, more Neorickettsia transmission pathways are possible
than merely through fish. The case of N. risticii that can infect a variety
of digeneans having diverse life cycles (see Section 3.3.4 of this review),
from entirely aquatic to entirely terrestrial, provides a clue that the cir-
culation of Neorickettsia in nature may be more flexible than we currently
appreciate.
3.3.4. Neorickettsia risticii and PHF

In the late 1970s, a mysterious, summertime illness of horses appeared
in the rural counties of Maryland and Virginia surrounding Washing-
ton, DC. Clinical symptoms varied, but usually included fever (often
biphasic), depression, anorexia and colitis (inflammation of large colon),
accompanied by acute diarrhoea (Holland et al., 1985c; Rikihisa, 1991).
In severe cases, horses exhibited laminitis. Pregnant mares often aborted
(Coffman et al., 2008, Long et al., 1995). If left untreated, overall mortality
approached 30% (Cordes et al. 1986). The clinical term for this condition
is equine monocytic ehrlichiosis but because the initial cases occurred in
horses pastured close to the Potomac River, the disease became known
as ‘Potomac horse fever’ (PHF). Stools from diarrhoeic horses contained
the infectious agent and, when fed to susceptible horses, could produce
PHF (Biswas et al., 1994, Palmer and Benson, 1994). However, the highly
seasonal occurrence of the disease, coupled with the fact that susceptible
horses stabled with sick horses rarely acquired PHF, suggested that PHF
was not a communicable disease but instead was a vector-borne disease.
The causative organism was initially placed in the genus Ehrlichia
(Holland et al., 1985a, c; Rikihisa and Perry, 1985). This led to some early
confusion regarding the transmission of PHF because Ehrlichia are known
to be tick borne. However, vector competence studies at the time failed to
incriminate local tick species in the transmission of the PHF (Hahn et al.,
1990, Levine et al., 1990).
The source of PHF remained enigmatic for years, until advances in molec-
ular biology transformed bacterial systematics in the early 1990s. When
Yasuko Rikihisa and her team at Ohio State University applied molecular
methodology to the study of ehrlichial diseases, they not only accelerated
the development of accurate diagnostic tools for PHF (Messick and Riki-
hisa, 1992a, b; Barlough et al., 1997, Mott et al., 1997a, b; Pusterla et al., 2006)
but importantly, their efforts as well as others, allowed for the phylogenetic
reconstruction of the Rickettsiales (Pretzman et al., 1995; Dumler et al., 2001;
Inokuma et al., 2001). As a result of this landmark accomplishment, it became
evident that the PHF agent was phylogenetically closer to the fluke-borne
agents of SPD, sennetsu fever and the SF agent than it was to tick-borne
ehrlichiae. This proved to be a textbook example of the utility of systemat-
ics and phylogenetics in resolving pressing practical questions related to a
new emerging disease and it provided the clue that enabled the University
of California (UC) Davis veterinarian team of John Madigan and colleagues
to begin to put the pieces of the PHF puzzle together (Dumler, 2000).
Using PCR technology, the UC Davis team isolated N. risticii DNA
from small pleurocercid snails ( Juga spp.) collected in the streams of an
endemic area (Barlough et al., 1998; Reubel et al., 1998). When cercariae
and sporocysts from fluke-infected snails were inoculated into horses, the
horses became ill with PHF (or Shasta River crud, as it is known locally;
Madigan et al., 1997). Neorickettsia risticii were recovered from buffy
coats of the sick horses (Pusterla et al., 2000a, c), satisfying Koch’s postu-
lates. Further studies elucidated the ecology of PHF in northern Califor-
nia (Pusterla et al., 2000a, c, 2003; Chae et al., 2000, 2002) and in central
Pennsylvania (Mott et al., 2002; Gibson et al., 2005; Gibson and Riki-
hisa, 2008). Transmission cycles in these areas involve several fluke spe-
cies that use river snails (e.g. Juga) as the first intermediate host, aquatic
insects (e.g. caddisflies and mayflies) as the second intermediate host and
insectivorous birds and/or bats as the definitive hosts (Fig. 3.5). Within
PHF-endemic areas, rates of N. risticii infection in intermediate hosts of
digeneans were high. In northern California, up to 26% of the snails har-
bouring larval digeneans tested PCR positive for N. risticii DNA (Pusterla
et al., 2000a, c). Likewise in central Pennsylvania, 5 of 42 pools (12%) of
cercariae and sporocyts collected from snails tested PCR positive for
N. risticii DNA, as did 2 of 10 pools (20%) of adult mayflies and 3 of 8 pools
(38%) of adult caddisflies (Mott et al., 2002).
To determine if metacercaria-infected insects harboured viable N. risticii,
two horses were fed pools of field-collected caddisflies that had tested
positive for N. risticii. Six to 11 days later, both horses became neorick-
ettsemic and clinically ill with PHF (Mott et al., 2002). Therefore, trans-
mission in these areas supposedly occurs when horses somehow swallow
insects containing metacercariae. This could occur in a variety of ways –
either through consuming insects while grazing, eating insect-contami-
nated hay, or by drinking insects that have been attracted at night to lights
over watering troughs and fell in the water (Farren, 2007). It is also pos-
sible that horses may acquire PHF by drinking water containing cercariae
shed by snails. To the best of our knowledge, this potential transmission
route has not yet been tested experimentally.
At least two different genera of adult flukes (Acanthatrium sp., Lecithoden-
drium sp.) parasitizing bats and swallows were found to harbour N. risticii
DNA (Pusterla et al., 2003; Gibson et al., 2005; Gibson and Rikihisa, 2008).
Importantly, unparasitized tissues (liver and spleen) from the definitive hosts
also contained N. risticii DNA (Pusterla et al., 2003), suggesting that insec-
tivorous birds and bats may act as natural vertebrate reservoirs of N. risticii.
However, several reports indicate that enzootic transmission cycles of
N. risticii are not necessarily restricted to lotic (i.e. riverine) ecosystems or
to a single type of digenean life cycle (Table 3.3). For example, Barlough
et al. (1998) reported detecting 16S rRNA sequence of N. risticii from a pool
of Stagnicola (Lymnaeidae) snails in Oregon. Stagnicola are common inhab-
itants of ponds and lakes throughout North America and are hosts to repre-
sentatives of many digenean families (Schell, 1985). On the shores of Lake
Merin, Uruguay, Dutra et al. (2001) found a significant clustering of cases
of PHF (=churrido equino) in horses that were regularly pastured in the
low marshy fields bordering the lake (36 per 1000 horse years) compared to
the horses pastured in rice plain fields (3 per 1000 horse years). In our pre-
liminary surveys, N. risticii DNA was isolated from two different species of
cercariae shed from Helisoma trivolis snails (Planorbidae) collected at Lake
FIGURE 3.5 Circulation of Neorickettsia risticii (white dots) involving lecithodendriid

digeneans (e.g. Acanthatrium spp.) and horses as a dead-end host. Images of snail and
fish are by T. Dieter and T. Saxby, Integration and Application Network, University of
Maryland Center for Environmental Science (ian.umces.edu/imagelibrary/). Images of
animals are by T. Dieter (snail, mayfly larva), T. Saxby (bat, horse) and K. Kraeer and L.V.
Essen-Fishman (mayfly adult), Integration and Application Network, University of
Maryland Center for Environmental Science (ian.umces.edu/imagelibrary/). (For color
version of this figure, the reader is referred to the web version of this book.)
Itasca, MN, USA (Table 3.3). Taken together, these observations indicate
that natural transmission of N. risticii may also involve lentic (=lake and
pond) ecosystems.
Moreover, N. risticii DNA has been recovered from an adult dicrocoe-
liid fluke parasitisizing a small passerine bird in North Dakota, USA (V.V.
Tkach, J.A. Schroeder and J.A. Vaughan, unpublished data). This is sig-
nificant because all dicrocoeliid flukes utilize land snails or slugs as their
first intermediate hosts and terrestrial invertebrates (usually arthropods)
as second intermediate hosts (Yamaguti, 1975; Schell, 1985). In addition,
we (V.V. Tkach, J.A. Schroeder and J.A. Vaughan, unpublished data) have
recently detected by PCR and sequenced N. risticii in digeneans with fully
aquatic life cycles, namely Alloglossidium corti (parasite of catfishes; Table 3.3)
and Heronimus mollis (parasite of freshwater turtles; Table 3.3). The for-
mer uses arthropods as second intermediate hosts, while the latter does
not have a second intermediate host and metacercariae remain within the
snail until eaten by a turtle. Thus, N. risticii is present in various digenean
groups having all of the main types of life cycles typical of freshwater/
terrestrial ecosystems (Fig. 3.6). Thus far, N. risticii has not been reported
from marine or estuarine environment. These findings demonstrate the
great plasticity of N. risticii circulation pathways in nature (Fig. 3.6). All
this indicates that enzootic transmission cycles of PHF occur even in many
ecosystems, even fully terrestrial ecosystems, which explains how horses
FIGURE 3.6 Generalized circulation pathways of Neorickettsia risticii based on life

cycles of its currently known digenean hosts. (For color version of this figure, the reader
is referred to the web version of this book.)
contract PHF in pastures far removed from rivers, streams, lakes or ponds.
Thus, the risk of horses contracting PHF may be more widespread than
previously recognized.
We are not aware of any studies demonstrating the presence of adult
flukes in horses that have contracted PHF. Indeed, the digenean fauna of
horses is generally very poor, and thus far, none of the digenean species
from which N. risticii DNA has been recovered belonged to groups that
can develop to the adult stages in horses. Thus, it appears that digenean
metacercariae do not need to complete development to the adult stage in
order to pass the infection to horses. Unlike the situation with SPD and
dogs, horses can truly be considered ‘dead-end hosts’ for PHF transmis-
sion. It remains unknown whether all species of N. risticii-infected meta-
cercariae ingested by a horse can lead to PHF or whether only certain
species or groups of digeneans can successfully transmit their neorickett-
sial endosymbionts before being destroyed in the horse’s digestive system
or expelled with the droppings.
A commercial vaccine for PHF based on the type strain, N. risticii Illi-
nois, became available in the late 1980s. However, soon afterwards, cases
of vaccine failures began to surface (Vemulapalli et al., 1995, Dutta et al.,
1998), suggesting that there were other, naturally occurring strains of
N. risticii that could infect horses but were different antigenically from the
strain upon which the vaccine was based. Various studies have supported
the idea of strain variation within N. risticii. In an early study examin-
ing this issue, Chaichanasiriwithaya et al. (1994) compared Western blot
and monoclonal antibody reactivity profiles of nine isolates collected in
Ohio and Kentucky from horses experiencing acute, naturally acquired
PHF. Three of the horses represented cases of ‘vaccine failure’ as they had
been vaccinated against PHF 6 months earlier and had high levels of anti-
N. risticii antibodies. From this relatively small sample size from a rela-
tively narrow geographic region, Chaichanasiriwithaya et al. (1994) found
three immunologically distinct N. risticii ‘sero-groups’. More recently,
Gibson et al. (2011) reported a strong geographic clustering among various
N. risticii isolates collected in the United States with respect to the pre-
dicted amino acid sequences of several proteins, including two external
loops of the major immunodominant surface-expressed protein, p51. The
cause of such variation is not known but is unlikely to be the result of
selective pressure placed on the bacteria by humoral responses of infected
horses. Neorickettsia are intracellular and horses represent a dead-end for
further Neorickettsia transmission. Rather, Gibson et al. (2011) speculated
that strain variation in N. risticii may be related to the specific type of dige-
nean harbouring the endosymbiont. The data provided by Gibson et al.
(2011) support earlier suggestions by Barlough et al. (1998) and Reubel
et al. (1998) that N. risticii actually constitutes a collection of strains that
may differ in the digenean hosts, snail ecology and virulence to horses.
As more information regarding strain variation accumulates over

broad geographic regions and the principal digenean hosts involved in
local transmission are identified, it may be possible to detect patterns
in digenean/endosymbiont strain associations and thereby define site-
specific ecologies of transmission. If such associations exist and can be
mapped out, then preventive strategies can be tailored to specific regions
to limit horse exposure to N. risticii-infected metacercariae and thus reduce
the administration of ineffectual vaccines or the over reliance on antibiot-
ics to prevent and treat PHF (Kanter et al., 2000).
3.3.5. SF agent

During the search for the agent of sennetsu fever, another neorickettsial
agent was discovered in S. falcatus metacercariae infecting grey mullet and
has been consistently found during at least 17 years of regular studies
(Fukuda et al., 1973; Fukuda and Yamamoto, 1981). The agent has become
known as ‘SF agent’ (short for ‘Stellantchasmus falcatus agent’) and differs
from N. sennetsu in western blot profiles probed with anti-SF sera, clinical
and pathologic responses of mice and 16S rRNA sequence comparisons
(Wen et al., 1996). The SF agent is not known to cause disease in humans
or in experimentally infected monkeys. It produces splenomegaly and
lymphadenopathy when injected into mice but produces only mild clini-
cal symptoms in dogs (Shishido et al., 1965; Hirai, 1966; Fukuda and
Yamamoto, 1981; Tachibana, 1986; Rikihisa, 1991; Wen et al., 1996). This
genotype of Neorickettsia can be maintained by mouse passages in labora-
tory (Fukuda and Yamamoto, 1981). Its digenean host, S. falcatus has a
snail/fish/mammal type of life cycle associated with lotic/estuarine habi-
tats. When ingested by humans, S. falcatus metacercariae are able to mature
to the adult stage in the intestine (Katsuta, 1931; Seo et al., 1984). Infection
with this small heterophyid fluke is of minor medical concern, causing
only mild intestinal discomfort and occasional diarrhoea (Seo et al., 1984).
Despite the wide geographic range of this fluke species (Japan, Korea,
Southeast Asia, Hawaii, Australia, Egypt, Palestine and Israel according to
Katsuta, 1931; Pearson, 1964; Chai and Sohn, 1988), SF agent has only been
recorded from Japan (Fukuda et al., 1973; Wen et al., 1996). It is not known
if it may inhabit other digenean species or other vertebrate animals.
3.3.6. Rainbow trout agent

During the studies to elucidate the ecology of PHF in California, 35 rain-
bow trout were collected from the Shasha River in a PHF-endemic area.
Neorickettsial DNA was recovered from three species of adult digenean
parasites collected from the gall bladder and intestine of the trout (Crep-
idostomum, Creptotrema, Deropegus spp.) and from the eggs of a blood fluke
(Sanguinicola sp.) recovered from gill capillaries (Pusterla et al., 2000b).
Neorickettsial DNA was also recovered from unparasitized fish tissues,
which may have represented either neorickettsial infection of host blood/
tissue or infection by undetected blood fluke eggs. Sequences of the ampli-
cons of 16S rRNA gene obtained from fish tissue and flukes were identical
to each other and very close to the sequences of members of Neorickettsia.
At the same time, they were distinct enough from N. risticii, N. sennetsu,
SF agent and N. helminthoeca (95–96% sequence homology) to suggest
that the ‘rainbow trout agent’ is a previously unrecognized genotype of
Neorickettsia. Nothing is known about its pathogenicity in fish or in verte-
brates that eat fish.
3.3.7. Neorickettsia sp. from needlefish in Cambodia

Seng et al. (2009) studied frozen fish and fish-based ingredients imported
from Thailand, Vietnam and Cambodia to Asian markets in Marseille,
France. They examined fish digestive tracts for parasitic worms and subse-
quently extracted DNA from digestive tracts. For detection of Anaplasma-
taceae, they used PCR with primers specific for the 16S rRNA and citrate
synthase genes of this group of bacteria. Three different forms of Ana-
plasmataceae were determined in the fish digestive tracts. Based on the
level of the sequence homology, the authors suggested that two of them
represented new genera within the Anaplasmataceae, while the third rep-
resented a new species of Neorickettsia. To define specific and generic lev-
els of sequence divergence in the Anaplasmataceae, the authors chose a
threshold of 97% identity among homologous 16S rRNA gene sequences
generated from each isolate. In a phylogenetic tree of the Anaplasmata-
ceae, the three genotypes all clustered together with Neorickettsia. The
two new genera were basal to all Neorickettsia, while the third belonged
to the clade containing the rainbow trout agent (Fig. 3.2). The new Neor-
ickettsia sp. was found in a freshwater needlefish Xenentodon cancila from
Cambodia. No digeneans were found in the needlefish, thus, the potential
circulatory pathway of these neorickettsiae remains unknown.
3.3.8. Catfish agents

Recently, we isolated two genotypes of Neorickettsia from different dige-
neans parasitic in catfishes in the United States (V.V. Tkach, J.A. Schro-
eder and J.A. Vaughan, unpublished data). These genotypes showed high
sequence homology (95–98%) with members of Neorickettsia and belonged
to two different clades within the genus (Fig. 3.3). One of them was
obtained from a gorgoderid digenean, Phyllodistomum lacustri, found in
the bladder of a stonecat catfish (Noturus flavus) and tentatively called cat-
fish agent 1. The other was obtained from an allocreadiid digenean, Megal-
ogonia ictaluri, found in the intestine of channel catfish (Ictalurus punctatus)
and tentatively called catfish agent 2. The former genotype seems closest
to N. helminthoeca, while the latter clustered with the published sequence
of the rainbow trout agent (Fig. 3.3). These findings, combined with dis-
coveries of the ‘EFF agent’ and rainbow trout agent, suggest that a rela-
tively diverse Neorickettsia species/genotype complex exists in digenean
parasites of North American freshwater fish.
These forms deserve more detailed studies, especially in view of the fact
that the catfish agent 2 was recovered from a digenean species parasitic in
the channel catfish – an important fish species that is raised commercially
and packaged for sale and consumption throughout the United States and
elsewhere. Worldwide, the channel catfish production has increased steadily
and has reached well over 450,000 tons per year according to Food and
Agriculture Organization fishery statistics (http://www.fao.org/fishery/
culturedspecies/Ictalurus_punctatus/en). Therefore, while the public health
importance of this and other poorly characterized Neorickettsia genotypes
is unclear, these discoveries nevertheless indicate that, even in the United
States, neorickettsiae occur dangerously close to the human food chain.
3.4. GEOGRAPHIC DISTRIBUTION OF NEORICKETTSIA
There are reports of confirmed or probable neorickettsial infections from

all continents, with N. risticii being by far the most widely distributed
and most frequently reported species of Neorickettsia (Dumler et al., 2005).
However, the majority of these reports including all information available
from Europe, Africa, Australia, as well as some Asian (e.g. India) and South
American (e.g. Venezuela) countries is based exclusively on serological test-
ing of horses without further evidence from either PCR/sequencing or cul-
turing the bacteria. In most cases, the vaccination or relocation histories of
serologically positive horses were not known or reported. Clearly, serolog-
ical tests have limitations and depend on previous exposure whether from
natural infections or vaccinations. Madigan et al. (1995) provided convinc-
ing evidence of high rate of false-positive results when the most common
serological diagnostic tool, the indirect fluorescent antibody (IFA) test, was
used to diagnose PHF in California. Later, Mott et al. (1997a) compared rel-
ative sensitivity and usability of IFA versus nested PCR while concurrently
culturing bacteria in the majority of samples. At the time, horses with sero-
logic evidence of prior exposure to PHF were found throughout the United
States, Canada and Europe, and seroepidemiological studies reported high
seroprevalences of horses that lacked clinical symptoms of PHF. However,
culture of N. risticii was rarely done and most of the diagnoses were based
on IFA testing. Mott et al. (1997a) emphasized that IFA testing at a single
time point is useless as a surveillance tool for detecting PHF in vaccinated
horses and expressed the same concern as Madigan et al. (1995) regarding
the reliability of reports based on serological evidence alone. Mott et al.
(1997a) concluded that the PCR test was as accurate and sensitive as cul-
turing and has an advantage over the IFA test because it is independent
of the past vaccination history of a horse. Therefore, in this section and on
the map in Fig. 3.7, we consider only data resulting from application of
PCR/sequencing techniques or culturing of the bacteria. Exceptionally, we
consider a few cases when sufficient vaccination/relocation histories were
reported for individual serologically positive horses.
Even after applying the stricter criteria outlined above, N. risticii
remains the most widely distributed species/genotype of Neorickettsia
(Fig. 3.7; Tables 3.1 and 3.3). It is broadly distributed throughout North
America and was recently reported from Brazil and Uruguay (Fig. 3.7).
Korean researchers (Chae et al., 2003; Park et al., 2003) also reported N. ris-
ticii from larval stages of several digenean species in the Republic of Korea.
However, the relatively high level of 16S sequence divergence between
Korean isolates and those from the United States suggests that the species
identity of the Korean genotype should be considered with some caution
(see discussion in Section 3.2.2 of this review). In any case, one or another
Neorickettsia species is certainly distributed in the Republic of Korea.
Another species of Neorickettsia that seems to be rather broadly distrib-
uted is N. helminthoeca that was long known to cause dog disease in the
Pacific northwest of the United States but then was found in other parts of
the western coast of North America, from British Columbia to California
(Booth et al., 1984; Sykes et al., 2010) as well as in Brazil (Headley et al.,
2004, 2009). The third named Neorickettsia species, N. sennetsu, is the most
widely distributed member of the genus in Asia and was found so far in
Japan, Malaysia, Laos and Thailand. All remaining five Neorickettsia geno-
types have very limited distribution and have been found in a single geo-
graphical area each (Fig. 3.7), either in North America, Japan or Southeast
Asia. Invariably, these genotypes have been discovered as a by-product of
studies targeting pathogenic species.
Thus, the known confirmed distribution of Neorickettsia is very uneven
from the geographical viewpoint. If we use the conservative approach out-
lined above, well-documented information on Neorickettsia is lacking from
Africa, Australia, Europe, most of South America, most of Asia and nearly
all island countries. In our opinion, this patchy distribution reflects a lack
of studies and insufficient knowledge rather than the true absence of Neor-
ickettsia from most regions of the planet. As far as we are aware, there were
no studies focusing on finding Neorickettsia anywhere in Africa or Austra-
lia. At the same time, already proven Neorickettsia symbiosis in representa-
tives of all major phylogenetic lineages of the Digenea (see Section 3.5 of
this review) suggests that these bacteria may likely be widely distributed
geographically. It is probably not accidental that the species with widest
distribution are those of significant veterinary or medical importance. It
FIGURE 3.7 Geographic distribution of known species and genotypes of Neorickettsia. Records based solely on serological diagnostics are not
included. (For color version of this figure, the reader is referred to the web version of this book.)
279
TABLE 3.3 Known digenean hosts of Neorickettsia species/genotypes their natural definitive hosts and geographic origin of Neorickettsia-
280
positive samples
Neorickettsia Digenean genus Digenean

species Digenean family and species definitive host Life cycle Country Reference
Jefferson A. Vaughan et al.

Neorickettsia Troglotrematidae Nanophyetus Marine and Aquatic/ United States Philip et al. (1953)
helminthoeca salmincola freshwater terrestrial
fish
EEF agent Troglotrematidae N. salmincola Marine and Aquatic/ United States Farrell et al. (1973)
freshwater terrestrial
fish
Neorickettsia Dicrocoeliidae Conspicuum sp. Birds Terrestrial United States V.V. Tkach, J.A.
risticii Schroeder and J.A.
Vaughan, unpublished
Echinostomatidae Echinoparyphium Birds Aquatic/ United States V.V. Tkach, J.A. Schroeder
rubrum terrestrial and J.A. Vaughan,
unpublished
Echinostomatidae Echinostoma Mammals Aquatic/ South Korea Park et al. (2003)
cinetorchis (humans) terrestrial
Echinostomatidae Echinostoma Birds and Aquatic/ South Korea Park et al. (2003)
hortense mammals terrestrial
Fasciolidae Fasciola sp. Mammals Aquatic/ South Korea Park et al. (2003)
terrestrial
Heronimidae Heronimus mollis Freshwater Aquatic United States V.V. Tkach, J.A. Schro-
turtles eder and J.A. Vaughan,
unpublished
Lecithodendriidae Lecithodendrium sp. Mammals Aquatic/ United States Pusterla et al. (2003)
and birds terrestrial
Lecithodendriidae Acanthatrium sp. Mammals Aquatic/ United States Pusterla et al. (2003)

(bats) terrestrial
Lecithodendriidae Acanthatrium orego- Mammals Aquatic/ United States Gibson et al. (2005)
nense (bats) terrestrial
Macroderoididae Alloglossidium corti Freshwater Aquatic United States V.V. Tkach, J.A.
fish Schroeder and J.A.
Vaughan, unpublished
Microphallidae Microphallidae sp. Bird or Aquatic/ South Korea Park et al. (2003)
mammal terrestrial
Plagiorchiidae Plagiorchis elegans Birds and Aquatic/ United States S.E. Greiman and V.V.
mammals terrestrial Tkach, unpublished
Schistosomatidae Schistosomatidae Birds and Aquatic/ South Korea Park et al. (2003)
sp. mammals terrestrial
Neorickettsia Not known Not known Not known Not known Japan, Fukuda et al. (1954);
sennetsu Malaisia, Misao and Kobayashi
Laos, (1954)
Thailand
Neorickettsia Gorgoderidae Phyllodistomum Freshwater Aquatic United States V.V. Tkach, J.A.
sp. (catfish lacustri fish Schroeder and J.A.
agent 1) Vaughan, unpublished
Neorickettsia Allocreadiidae Megalogonia ictaluri Freshwater Aquatic United States V.V. Tkach, J.A.
sp. (catfish fish Schroeder and J.A.
agent 2) Vaughan, unpublished
(continued)
281
TABLE 3.3 (Continued)
282
Neorickettsia Digenean genus Digenean
species Digenean family and species definitive host Life cycle Country Reference
Jefferson A. Vaughan et al.

Neorickettsia Not known Not known Freshwater Not known Cambodia Seng et al. (2009)
sp. fish
Neorickettsia Derogenidae Deropegus sp. Freshwater Aquatic United States Pusterla et al. (2000)
sp. (rain- fish
bow trout Allocreadiidae Crepidostomum sp. Freshwater Aquatic United States Pusterla et al. (2000)
agent) fish
Allocreadiidae Creptotrema sp. Freshwater Aquatic United States Pusterla et al. (2000)
fish
Sanguinicolidae Sanguinicola sp. Freshwater Aquatic United States Pusterla et al. 2000
fish
Neorickettsia Heterophyidae Stellantchasmus Mammals Aquatic/ Japan Fukuda and
sp. (SF falcatus (humans) terrestrial Yamamoto (1981)
agent)
reflects the fact that much more resources have been put into studies of
these species. An additional important factor might be the high mobil-
ity of humans and high frequency of relocation of domestic animals that
could facilitate the spread of some of the Neorickettsia genotypes. Available
evidence suggests that PHF was almost certainly historically absent from
North America. Considering the vital importance of horses to the economy
and culture of early settlement of North America, it seems strange that PHF
had never before been diagnosed as a recognizable disease prior to 1970.
It would be difficult to expect that a disease with visible clinical symp-
toms would have gone completely unnoticed for centuries. As it turns out,
N. risticii has been identified as the causative agent for ‘churrido equino’ –
a diarrhoeic disease of horses known for over 100 years in the Lake Merin
region of Uruguay and Brazil (Dutra et al., 2001; Coimbra et al., 2005).
We hypothesize that PHF might have been introduced to North America
from South America relatively recently. Comparative phylogenetic studies
of a greater number of samples from as broad geographic area as possible,
optimally using sequences of several genes, may provide some insight into
this interesting question and either confirm or refute this hypothesis.
Obviously, there are natural causes for differences in the distribution
of various Neorickettsia species/genotypes. For instance, the most widely
spread species, N. risticii, is the only one found so far in flying migratory
vertebrate animals (birds and bats), which may have an impact on the
distribution of their digeneans and digenean endosymbionts. The most
obvious mechanism limiting the geographic distribution of the majority of
Neorickettsia genotypes is related to the specificities of the bacteria to their
fluke hosts on the one hand and of flukes to their intermediate and defini-
tive hosts on the other. Most digeneans are rather tightly ecologically and
evolutionarily associated with their mollusc hosts as well as other host cat-
egories (Yamaguti, 1975; Cribb et al., 2001, 2003). It means that if even one
of the hosts in the digenean complex life cycle has a limited distribution,
it will limit the distribution of the fluke species. Nanophyetus salmincola
is a good example of such dependency due to its high specificity to a mol-
lusc host with a limited geographic distribution (see Section 3.3.1).
As studies of neorickettsiae are undertaken in new regions, we antici-
pate that the known geographic distribution of these endosymbionts will
expand significantly.
3.5. PHYLOGENETIC ASSOCIATIONS BETWEEN

NEORICKETTSIA AND DIGENEA
Neorickettsiae are widely distributed among digeneans. In fact, one or
another species or genotype of these endosymbionts is found in represen-
tatives of all major lineages of the Digenea (Fig. 3.8). Some neorickettsial
FIGURE 3.8 Neorickettsia species/genotype records mapped on the phylogenetic tree

of the digenan families from Olson et al. (2003; published by permission from Elsevier).
Records of Neorickettsia obtained from published data and unpublished data by V.V.
Tkach, J.A. Schroeder and J.A. Vaughan (Table 3.3). A record in Alloglossidium corti is not
shown on the tree because the Allocreadiidae were not included in the phylogenetic
analysis by Olson et al. (2003).
species seem to have a narrow host range, restricted to within a single

family of Digenea (e.g. salmon poisoning, EFF agent and SF agent;
see Fig. 3.8). Other neorickettsial species have been isolated from phy-
logenetically distant digenean families (e.g. rainbow trout agent; see
Fig. 3.8). Neorickettsia risticii displays the broadest digenean host utiliza-
tion, with its DNA having been isolated from an astonishing diversity of
digeneans including a range of families from one of the most basal dige-
nean lineages (Schistosomatidae and Strigeidae) to the most advanced lin-
eages (Lecithodendriidae and Microphallidae). This may indicate that the
neorickettsiae as a group have had a long evolutionary history with Digenea
and suggests that neorickettsiae may be potentially found in many addi-
tional groups of Digenea. At the same time, there is no evidence of clear
coevolutionary relationship between certain digenean lineages and their
bacterial endosymbionts. For example, identical sequences of 16S rRNA
have been obtained from widely divergent digenean taxa. Conversely,
different genotypes producing different pathologies in dogs and bears,
i.e. N. helminthoeca and EFF agent, share the same digenean host species,
N. salmincola.
The exact nature of the endosymbiotic relationship among neorickett-
siae and their digenean hosts at physiological level is currently unclear. It
is likely not obligatory because there is no apparent dependency of digene-
ans on these endosymbionts. Some individuals within the same digenean
species may be infected with neorickettsiae, whereas other individuals are
not. This situation is different, for instance, from the obligatory relation-
ships among Wolbachia and certain species of filariid nematodes (Taylor
et al., 2005; Casiraghi et al., 2005; Ferri et al., 2011; Fischer et al., 2011). The
potential influence of Neorickettsia on their digenean hosts remains practi-
cally unknown and represents one of the most interesting aspects of their
biology.
3.6. ADVANCES IN GENOMICS AND MOLECULAR BIOLOGY

OF NEORICKETTSIA
Most of the advances in our knowledge of the biology, host associations

and distribution of Neorickettsia in the last 15–17 years are intimately
linked to the development of molecular approaches and techniques,
particularly PCR and DNA sequencing. As mentioned before, use of DNA
sequences has revolutionized the systematics and phylogenetics of this
group of bacteria. Although 16S rRNA region remains the primary tar-
get for both diagnostics and phylogenetic analyses (Pretzman et al., 1995;
Dumler et al., 2001; Stackebrandt et al., 2002; Headley et al., 2011), several
other genes have been proposed and used for both diagnostics and phylo-
genetics, e.g. the citrate synthase gene (gltA; Inokuma et al., 2001; Rikihisa
et al., 2004), the RNA polymerase b-subunit (Taillardat-Bisch et al., 2003),

the heat shock protein gene (groESL; Dumler et al., 2001; Rikihisa et al.,
2004; Headley et al., 2011), the p51 gene encoding major antigenic 51-kDa
protein (Rikihisa et al., 2004) and the outer membrane protein Omp85 gene
(Newton et al., 2009). The groESL gene is the second most widely utilized DNA
region utilized in differentiation among lineages and species of Neorickettsia.
With further evolution of PCR technology, use of RT-PCR including
TaqMan probes provided an additional convenient method for quick and
reliable detection of Neorickettsia (Pusterla et al., 2006; Newton et al., 2009).
Complete genomes of several Anaplasmataceae were recently pub-
lished, including two annotated genomes of Neorickettsia, namely N. sennetsu
(Hotopp et al., 2006) and N. risticii (Lin et al., 2009). Hotopp et al. (2006)
conducted a comparative analysis of genomes of 19 obligate and faculta-
tive intracellular pathogenic and endosymbiotic bacteria and discovered
that 176 orthologue clusters (mostly with housekeeping functions) are
conserved across these bacterial lineages. Members of the Anaplasmata-
ceae had significantly higher percentages of their genomes dedicated to
nucleotide biosynthesis, cofactor and vitamin biosynthesis, and protein
synthesis than did free-living α-proteobacteria.
Neorickettsiae have the smallest genome size of all members of the Ana-
plasmataceae examined to date. The annotated genome of N. risticii consists
of 879,977 bp and encodes 38 RNA species and 898 proteins (Lin et al., 2009).
Genome-wide comparison between N. risticii and N. sennetsu showed that
very high percentage (758 or 88.2%) of protein-coding genes is conserved
between N. risticii and N. sennetsu. Moreover, comparison of genes among N.
risticii and other Anaplasmataceae showed that most genes (525 orthologs
generally associated with housekeeping functions) are shared among other
members of major Anaplasmataceae lineages. Besides other obvious poten-
tial uses of this information, it suggests that many more genes are available
for species differentiation and phylogenetic inference in this group than cur-
rently used. On the other hand, Lin et al. (2009) showed that some genes of
N. risticii and N. sennetsu have greater homology to those of α-proteobacteria
than to the same genes in other Anaplasmataceae, including the genes cod-
ing for histone-like HU DNA-binding proteins, adenosine triphosphate syn-
thase subunits, DsbB/D protein and some ribosomal protein subunits.
Certain genes potentially involved in the pathogenesis of N. risticii have
been identified, including those encoding putative outer membrane pro-
teins, two-component systems and a type IV secretion system. The genome
of N. risticii encodes for a fully functional aerobic respiratory pathway but
encodes for only a partial glycolytic pathway. Although N. risticii has lim-
ited ability to synthesize amino acids and lacks many metabolic pathways,
it is capable of making major vitamins, cofactors and nucleotides. Like
in other anaplasmids, the Neorickettsia genome does not encode for pep-
tidoglycan or lipopolysaccarhide synthesis, which are potent stimulants
for the innate immune response in vertebrates and invertebrates. This

may enhance their ability to survive within vertebrate leucocytes.
Lin et al. (2009) have demonstrated that despite parasitizing differ-
ent digenean hosts on different continents, N. risticii and N. sennetsu have
preserved complete genome synteny, although the genome contents were
divergent on proteins with yet unknown functions. They emphasized
that surface-exposed proteins and the unique sets of proteins involved in
pathogenesis identified in their work provide valuable baseline data for
future research on PHF vaccines. Gibson et al. (2010, 2011) followed up on
some of these suggestions in their proteomic analyses of surface proteins
in N. sennetsu and N. risticii, respectively. They confirmed that 51-kDa anti-
gen (P51) was a major surface-exposed outer membrane protein and dem-
onstrated its functional role in the cell, i.e. porin activity. As mentioned in
Section 3.3.4, these data demonstrate patterns of geographical association
for P51 providing baseline information for designing immunodiagnostic
targets for PHF.
It can be anticipated that publication of annotated complete genomes
will foster new in-depth studies of neorickettsial metabolism, pathogen-
esis, antigenic properties, drug and vaccine development, evolution and
phylogeny.
3.7. GAPS IN CURRENT KNOWLEDGE AND FUTURE

PERSPECTIVES
It has been more than 50 years since the discovery that digeneans harbour
bacterial endosymbionts that cause disease in humans and dogs. And yet,
it is safe to say that even now the studies of neorickettsial diversity are in
their infancy. As demonstrated above, only a small fraction of digenean
taxa has ever been examined for the presence of Neorickettsia. Screening a
broad diversity of digeneans around the world will likely reveal numer-
ous new Neorickettsia–digenean host associations and very probably new
species of Neorickettsia. Numerous, in some cases very extensive, collec-
tions of digenean DNA obtained for systematic, ecological, genomic and
diagnostic purposes around the world represent a great underutilized
resource for studies of Neorickettsia. These collections can be rather eas-
ily screened for the presence of neorickettsial DNA, dramatically enhance
our knowledge of these endosymbionts and provide new insights into
evolutionary relationships between neorickettsiae and their digenean and
vertebrate hosts.
It is also certain that the current knowledge of Neorickettsia geographic
distribution is highly incomplete and does not accurately portray the real
picture. Lack of information on Neorickettsia from Africa, Australia, most
of Eurasia and majority of large islands reflects insufficient sampling
rather than true absence of Neorickettsia in these continents and geographi-

cal regions. Recent discoveries of N. sennetsu in Laos, N. helminthoeca in
Brazil and N. risticii in Uruguay indicate that neorickettsiae are more ubiq-
uitous than was previously known. With PCR and sequencing technology
becoming progressively more accessible in many parts of the world, we
anticipate quick expansion of these studies in previously uninvestigated
regions.
Screening digenean groups that include human parasites should be
a priority. Digenean infections of humans are very common and in some
localities, the prevalence of infection can reach nearly 100% (Chai et al.,
2005a, 2007, 2009b). For example, opisthorchiid flukes constitute a large
proportion of human digenean infections in several parts of the world,
yet this important group of digeneans has never been tested for neorick-
ettsiae. The only neorickettsial disease of humans, the Sennetsu fever, is
restricted to a single geographic region. This does not have an adequate
explanation and poses a serious question. If the magnitude of food-borne
digenean infection is so great, why are not more people getting sick with
neorickettsioses? The reasons might be various, ranging from dietary
preferences, dependency of Neorickettsia circulation on certain regionally
distributed definitive or intermediate hosts or improper diagnosis of neor-
ickettisial disease. Perhaps, human neorickettsioses are rare and restricted
to specific regions. Perhaps, there is a certain degree of specificity between
digenean and virulent strains of Neorickettsia. If so, then the prevalence
of neorickettsioses may be associated with the prevalence of only certain
types or species of digenean infections. Alternatively, in the tropics where
diagnostic capabilities may be minimal, neorickettsioses may go undiag-
nosed (e.g. fever of unknown origin) or misdiagnosed as something else
(e.g. dengue). Considering that at least two known Neorickettsia species
are capable of infecting human cell lines in vitro, there is a pressing need
to investigate the prevalence of Neorickettsia infection in digenean species
infecting humans.
Similarly, there are several diseases of wildlife attributable to Neorick-
ettsia. Most likely there are more neorickettsial diseases of wildlife than we
presently know. However, the real scope of neorickettsiosis of wildlife is
difficult to estimate, especially if these diseases are sublethal. Considering
the virulence of neorickettsiae to some wild and experimental animals, the
role of neorickettsioses as a cause of significant mortality and morbidity
among wildlife population diseases might be more significant than cur-
rently appreciated.
Lastly, there is a need to understand both qualitative and quantitative
aspects of Neorickettsia transmission. The notion that there are more dige-
nean taxa that harbour neorickettsiae than is currently known leads to
the conclusion that there are yet unknown pathways of their circulation
and infection of definitive hosts. The discovery of entirely terrestrial and
entirely aquatic circulation pathways for N. risticii, as well as the confir-

mation of neorickettsial infection in blood flukes, already has uncovered
new routes of circulation for these pathogens. We are confident that future
research will reveal additional transmission pathways of neorickettsiae in
nature.
Probably, the largest gap in our knowledge of Neorickettsia biology is
the very limited information available regarding the quantitative aspects
of their perpetuation during the complex digenean life cycles. To persist,
the endosymbionts must survive several developmental processes which
their digenean hosts undergo during a single life cycle. And to proliferate
and prosper, it seems reasonable that the endosymbiont must undergo rep-
lication during those times at which its digenean host is also undergoing
reproduction – asexual in the mollusc and sexual in the vertebrate defini-
tive host. But the efficiency to which bacterial replication keeps pace with
that of its host is not known. Determining the prevalence of Neorickettsia
in different stages of digenean life cycles, from eggs to cercariae, meta-
cercariae and adult worms, is a logical starting point for understanding
this aspect of neorickettsia biology. Horizontal transmission of neorickett-
siae from digeneans to vertebrates occurs naturally and has been shown
experimentally. However, the transmission from neorickettsemic verte-
brates to digeneans or from Neorickettsia-infected digeneans to uninfected
digeneans has not yet been demonstrated. Horizontal transmission may
be a vital part of the circulation and evolution of neorickettsiae because it
may complement vertical transmission and introduce neorickettsial infec-
tions into previously uninfected digenean lineages. Understanding these
fundamental aspects of Neorickettsia biology and transmission will be criti-
cal to understanding the epidemiology and epizootology of the diseases
caused by these bacteria.
ACKNOWLEDGEMENTS
We are grateful to Maksym Tkach who helped to obtain many of the original references used
in this review. This work was supported in part by the grant R15AI092622 from the National
Institutes of Health, USA.
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CHAPTER 4
Priorities for the Elimination
of Sleeping Sickness
Susan C. Welburn and Ian Maudlin

4.2. Risk 301
4.2.1. Vector distribution 301
4.2.2. Disease distribution – two diseases 302
4.2.3. Foci of infection 303
4.2.4. Vector competence – T. b. rhodesiense in tsetse 304
4.2.5. Vector competence – T. b. gambiense in tsetse 305
4.2.6. Reservoirs of infection 306
4.3. Diagnosis and Treatment 308
4.3.1. Treatment – T. b. gambiense sleeping sickness 308
4.3.2. Treatment – T. b. rhodesiense sleeping sickness 309
4.3.3. Diagnostics 310
4.3.4. Diagnosis – T. b. gambiense sleeping sickness 310
4.3.5. Diagnosis – T. b. rhodesiense sleeping sickness 310
4.3.6. Molecular diagnostics 311
4.4. Burden of Disease 311
4.4.1. Hidden burden of disease 313
4.5. Control 313
4.5.1. Origins of epidemics 314
4.5.2. Controlling T. b. gambiense sleeping sickness 316
4.5.3. Tsetse control and T. b. gambiense 318
4.5.4. Controlling T. b. rhodesiense sleeping sickness 321
4.5.5. Tsetse control and T. b. rhodesiense 321
4.6. Discussion 324
References 329
Division of Pathway Medicine and Centre for Infectious Diseases, School of Biomedical Sciences, College
of Medicine and Veterinary Medicine, The University of Edinburgh, Edinburgh, UK

299
300 S. C. Welburn et al.
Abstract Sleeping sickness describes two diseases, both fatal if left un-
treated: (i) Gambian sleeping sickness caused by Trypanosoma
brucei gambiense, a chronic disease with average infection lasting
around 3 years, and (ii) Rhodesian sleeping sickness caused
by T. b. rhodesiense, an acute disease with death occurring
within weeks of infection. Control of Gambian sleeping sickness
is based on case detection and treatment involving serological
screening, followed by diagnostic confirmation and staging. In
stage I, patients can remain asymptomatic as trypanosomes mul-
tiply in tissues and body fluids; in stage II, trypanosomes cross
the blood–brain barrier, enter the central nervous system and, if
left untreated, death follows. Staging is crucial as it defines the
treatment that is prescribed; for both forms of disease, stage II
involves the use of the highly toxic drug melarsoprol or, in the
case of Gambian sleeping sickness, the use of complex and very
expensive drug regimes. Case detection of T. b. gambiense sleep-
ing sickness is known to be inefficient but could be improved by
the identification of parasites using molecular tools that are, as
yet, rarely used in the field. Diagnostics are not such a problem in
relation to T. b. rhodesiense sleeping sickness, but the high level
of under-reporting of this disease suggests that current strategies,
reliant on self-reporting, are inefficient.
Sleeping sickness is one of the ‘neglected tropical diseases’
that attracts little attention from donors or policymakers. Proper
quantification of the burden of sleeping sickness matters, as the
primary reason for its ‘neglect’ is that the true impact of the
disease is unknown, largely as a result of under-reporting. Cer-
tainly, elimination will not be achieved without vast improve-
ments in field diagnostics for both forms of sleeping sickness
especially if there is a hidden reservoir of ‘chronic carriers’. Mass
screening would be a desirable aim for Gambian sleeping sick-
ness and could be handled on a national scale in the endemic
countries – perhaps by piggybacking on programmes committed
to other diseases. As well as improved diagnostics, the search for
non-toxic drugs for stage II treatment should remain a research
priority.
There is good evidence that thorough active case finding is
sufficient to control T. b. gambiense sleeping sickness, as there is
no significant animal reservoir. Trypanosoma brucei rhodesiense
sleeping sickness is a zoonosis and control involves interrupt-
ing the fly–animal–human cycle, so some form of tsetse control
and chemotherapy of the animal reservoir must be involved. The
restricted application of insecticide to cattle is the most promising,
affordable and sustainable technique to have emerged for tsetse
control. Animal health providers can aid disease control by treat-
ing cattle and, when allied with innovative methods of funding (e.g.
public–private partnerships) not reliant on the public purse, this
approach may prove more sustainable.
Priorities for the Elimination of Sleeping Sickness 301
Sleeping sickness incidence for the 36 endemic countries has

shown a steady decline in recent years and we should take advantage
of the apparent lull in incidence and aim for elimination. This is fea-
sible in some sleeping sickness foci but must be planned and paid
for increasingly by the endemic countries themselves. The control
and elimination of T. b. gambiense sleeping sickness may be seen
as a public good, as appropriate strategies depend on local health
services for surveillance and treatment, but public–private fund-
ing mechanisms should not be excluded. It is timely to take up the
tools available and invest in new tools – including novel financial
instruments – to eliminate this disease from Africa.
4.1. INTRODUCTION
Sleeping sickness is one of 13 parasitic diseases affecting the poor in

developing countries that have come to be known as ‘the neglected tropi-
cal diseases’ (NTDs) affecting several hundred million people and kill-
ing at least half a million annually; yet they attract little attention from
donors or policymakers (Molyneux et al., 2005; Molyneux, 2008), hence
the designation ‘neglected’ (Hotez et al., 2009). Recent reviews of sleeping
sickness (also described as Human African trypanosomiasis or HAT – not
a helpful descriptor for, as we shall see, there are two very different forms
of this disease) have dealt with, variously, the trypanosome’s notorious
molecular wiliness in evading the host immune system (Rudenko, 2011),
clinical aspects (Brun et al., 2010; Malvy and Chappuis, 2011), chemother-
apy, drug discovery (Burri, 2010; Jacobs et al., 2011) and related problems
of drug resistance (Barrett et al., 2011) and diagnostics (Chappuis et al.,
2005). We seek here to indicate where resources might best be placed to
move towards the elimination of this peculiarly African disease. To do
this, we have used own experience – based on many years of fieldwork –
leavened by discussions we have had with our valued collaborators. We
are now at the point where innovative solutions are available to impact on
this disease to the extent that elimination is now a realistic aim, targeted
officially at 2020 (World Health Organization, 2012) – more than a century
since the disease was first recognised. Where there are gaps in our tool-
box, we suggest areas of research that could benefit from focus.
4.2. RISK
4.2.1. Vector distribution

To paraphrase Jane Austen: ‘It is a truth universally acknowledged, that a try-
panosome in possession of a human infective genotype, must be in want of a
tsetse fly’. Sleeping sickness is confined to sub-Saharan Africa for the simple
reason that the distribution of its primary host and vector, the tsetse fly, marks
the limits of the disease. Tsetse distribution is dependent on environmental
conditions that define habitats suitable for fly survival. At the edges of the
continental range, maximum mean monthly temperature defines the range
limit of all tsetse species; the Sahel, spanning Africa from the Atlantic Ocean
to the Red Sea, conveniently sets the northern limit of vector distribution and,
to the south, flies do not penetrate far into the Republic of South Africa.
While the northern and southern limits of tsetse are easily recognised
and understood, within the continent tsetse are not evenly distributed.
The 33 species and subspecies of tsetse are grouped into three divisions,
adapted to differing habitats: fusca group (forest habitat), morsitans
group (savannah habitat) and palpalis group (riverine and forest habi-
tats). Until recently, the best available distribution maps of tsetse species
were based on reported surveys of variable quantitative rigour (Ford
and Katondo, 1977). The advent of satellite imagery combined with
sophisticated computer modelling has vastly improved the situation;
the distribution of tsetse species may now be predicted and mapped
with remarkable accuracy by applying a limited set of variables: nor-
malised density vegetation index, temperature, rainfall and humidity
(Rogers and Robinson, 2004).
It is evident from these mapping studies that distribution within tsetse
species is not uniform across ecological zones but rather that species tend
to have wide but geographically discontinuous distributions. This view is
reinforced when we examine tsetse population genetics. All tsetse species
examined show highly structured distinct population clusters (i.e. subpopu-
lations or demes), between which there is little detectable gene flow suggest-
ing that flies have adapted among species to differing environments (Ravel
et al., 2007). This is well illustrated by recent studies of Glossina fuscipes, an
important vector of sleeping sickness across Central Africa, that in fact com-
prises a species complex (Abila et al., 2008; Beadell et al., 2010; Dyer et al.,
2011). Genetic evidence precludes massive exchange of individuals between
any of the tsetse populations sampled to date (Krafsur, 2009). For palpalis
group taxa, Krafsur (loc. cit.) has suggested that seasonal range expansions
and contractions account for a patchwork distribution of demes differenti-
ated by founder effects and genetic drift during the favourable wet season,
followed by concentration in moist refugia during the dry season – hence
the discontinuous distribution of flies we observe today.
4.2.2. Disease distribution – two diseases

Confusingly, sleeping sickness is not a single disease – the term covers two
diseases that present with distinct clinical features (Welburn et al., 2001a).
Gambian sleeping sickness (caused by Trypanosoma brucei gambiense infection)
is a chronic disease with average duration of infection calculated to be around

3 years (Checchi et al., 2008a); Rhodesian sleeping sickness (caused by T. b.
rhodesiense infection) by contrast is acute, death occurring within weeks or
months of infection (Odiit et al., 1997). Both diseases are ultimately fatal if
left untreated. Unfortunately, discussions of sleeping sickness control tend to
elide this distinction and, as we shall see, may have contributed to the pursuit
of inappropriate control strategies, which is why the generic term ‘HAT’ is
best avoided. The most obvious distinction in terms of distribution of the two
diseases is East–West, with a very clear dividing line closely following the
Great Rift Valley (Welburn et al., 2001a).
4.2.3. Foci of infection

The distribution of sleeping sickness is limited by the distribution of the
tsetse belt across Africa. However, as we have seen, the tsetse belt is made
up of many species of tsetse with differing environmental strictures; in
turn these species comprise a patchwork of subpopulations that may be
small in number (Krafsur, 2009). As we might expect, sleeping sickness
in turn is not evenly distributed across the African continent. However,
maps of tsetse and sleeping sickness distribution cannot be simply over-
laid, as sleeping sickness is far more limited in its distribution than its
vector species; a cursory glance at any disease distribution map reveals
a highly discontinuous distribution of reported cases (for the most recent
maps, see Cecchi et al., 2009; Simarro et al., 2010). This patchwork distri-
bution (well illustrated for Cameroon and Gabon by Cattand et al., 2001)
has long been recognised, hence the description ‘historic endemic foci’
(Gouteux and Artzrouni, 2000). This is in sharp contrast to the distribution
of animal trypanosomes that are found across the tsetse belt: Trypanosoma
congolense is found in cattle across Africa from Burkino Faso (Sow et al.,
2006) to Zambia (Van den Bossche et al., 2011), in a range of ecosystems.
The origins of these ancient foci of sleeping sickness defy simple
environmental explanation – they are difficult to define by either habi-
tat restrictions or tsetse species and/or range; they remain enigmatic.
A rough definition of a focus is ‘a zone of transmission to which a geo-
graphical name is given’ (Simarro et al., 2008); an example would be
the Busoga (Uganda) focus of T. b. rhodesiense sleeping sickness. In the
absence of plausible biological definitions, the origins of foci and epidem-
ics are ascribed to historical, multifactorial, socio-economic conditions
(Ford, 1971; Lyons, 1992; Berrang-Ford, 2007; Courtin et al., 2008). The
most plausible biological explanation of the origins of sleeping sickness
foci is given by Krafsur (2009) who suggests that tsetse fly/trypanosome
coadaptations differ from one population cluster to another resulting in
the evolution of complex trypanosome–vector interactions, which may
be very closely defined by habitat and hence geography. Studies of the
population genetics of T. b. gambiense support this view (Krafsur, loc. cit.);

for example, trypanosomes from Guinea and Ivory Coast are highly dif-
ferentiated and are thought to have adapted to different vector species:
Glossina palpalis gambiensis in Guinea and G. p. palpalis in the Ivory Coast
(Koffi et al., 2009).
An analysis of T. b. gambiense sleeping sickness foci in West Africa over
the past 100 years has shown that some historic foci – in Senegal, Mali and
Burkino Faso – have disappeared altogether. More generally, there was a
shift in the last century of endemic foci from North to South of the region
to areas where annual rainfall exceeds 1200mm (Courtin et al., 2008). This
change in distribution of foci is thought to reflect a decline in rainfall in
the periods 1950–1969 and 1970–1989 with consequent effects on tsetse
populations combined with human population pressure and intensifica-
tion of agriculture. By contrast, Moore et al. (2011) suggest that impend-
ing changes in global temperature could affect the distribution of sleeping
sickness, predicting an increase in its extent.
Interestingly, Courtin et al. (loc. cit.) also note a shift over time in the
apparent extent of foci from historically widespread zones to the pres-
ent day ‘small circles’ raising the question of whether the definition of a
‘focus’ has changed over time simply as a result of the precision of modern
mapping techniques. Courtin et al. (loc. cit.) pose a challenging question:
‘does the special distribution of the current foci (i.e. only found in regions
of West Africa with >1200mm rainfall per year) merely mirror the zone
where medical teams monitor the disease effectively?’. There is no doubt
that the spikes in incidence across Africa, we saw in the epidemics of the
1980s–1990s, reflected the reintroduction of monitoring following a period
of neglect (e.g. see Moore and Richer, 2001).
4.2.4. Vector competence – T. b. rhodesiense in tsetse

Naturally acquired infections with sleeping sickness trypanosomes are
rare in tsetse – particularly transmissible (i.e. salivary gland or ‘mature’)
infections. This is well illustrated by G. f. fuscipes dissected before, dur-
ing and after the 1980s T. b. rhodesiense epidemic in Busoga, SE Uganda:
at the height of the epidemic, salivary gland infection rates were found
to be low (0.8% – Okoth and Kapaata, 1986) and not much different
from that of flies in 1976, before the epidemic period (0.5% – Kutuza
and Okoth, 1981). Later, in endemic conditions in the same area, salivary
gland infection rates were not strikingly lower (0.2% – Waiswa et al.,
2006). It must be borne in mind that some (or indeed all) of these sali-
vary gland infections could well have been T. b. brucei (i.e. non-human
infective) rather than T. b. rhodesiense as these two types of infection can-
not be distinguished by microscopy. When the Busoga sleeping sickness
outbreak of the 1980s spreads eastwards into Tororo district, the authors
carried out two surveys of G. f. fuscipes in 1988 and 1990 in Iyolwa sub-
county; a single salivary gland infection was found in each sample (0.1%
in both samples; 1500 flies dissected in total – S.C. Welburn and I. Maudlin
unpublished observations). Both of these infections were subsequently
identified as T. b. rhodesiense by DNA analysis (Hide et al., 1994). Recent
surveys using polymerase chain reaction (PCR) in the Serengeti, Tanza-
nia, have also demonstrated a low prevalence (0.01%) of transmissible
T. b. rhodesiense in tsetse (Auty et al., 2012). We conclude that low mature
infection rates of T. b. rhodesiense observed in tsetse in the field are the
norm across a range of environments, even during epidemic conditions.
4.2.5. Vector competence – T. b. gambiense in tsetse

If the apparently low T. b. rhodesiense mature infection rates in tsetse are
surprising, such rates are highly satisfactory when compared with the
results for T. b. gambiense infections. One of the earliest investigators,
H.L. Duke, was puzzled by the very low infection rates he obtained exper-
imentally in tsetse. Duke (1934) found a single T. gambiense salivary gland
infection (0.02%) in 4272 Glossina palpalis (since renamed G. f. fuscipes) and
found it difficult to reconcile his fly data with the apparent high infec-
tion rates recorded in humans both in Uganda and in West Africa. Indeed,
when Duke’s (1930) work was reviewed, he was at pains to show that
these low infection rates did not indicate dilatoriness on his part. Subse-
quent investigators have also found it difficult to infect tsetse with T. b.
gambiense in the laboratory (Maudlin and Dukes, 1986; Moloo et al., 1986).
Using fresh field isolates of T. b. gambiense, Ravel et al. (2006) were unable
to obtain any salivary gland infections in three of five isolates tested; one
trypanosome isolate did produce a high salivary gland infection rate (6%).
Field data that predate molecular analysis of T. b. gambiense infections
in tsetse are difficult to assess for, as with T. b. rhodesiense, T. b. gambiense
could not be differentiated from the non-human infective species T. b. bru-
cei by microscopy. However, it is worth noting that, in collating data from
various workers in Nigeria and Cameroon (where sleeping sickness was
then endemic), Jordan (1961) showed that ‘T. brucei’ s.l. infection rates (i.e.
salivary gland infections) for all tsetse species were either low (<1.0%)
or non-existent. More recently, in a sample of 1701 G. p. palpalis in Côte
d’Ivoire, only one salivary gland infection was found by microscopy giv-
ing a T. brucei s. l. infection rate of 0.06% (Jamonneau et al., 2004); surveys
in Cameroon identified T. b. gambiense in the midguts of tsetse using PCR
but no mature infections in 4717 flies (Farikou et al., 2010).
It might be thought that PCR techniques would simplify analysis of
tsetse collected in the field but it should be noted that such studies tend to
exaggerate both mature and immature fly infection rates when compared
with microscopy. The presence of trypanosome DNA in a preserved/frozen
fly does not necessarily indicate a mature infection – or even an established

midgut infection – as trypanosome DNA could come from a blood meal
taken just prior to analysis and merely indicate a transitory midgut infec-
tion that the fly will eliminate (Macleod et al., 2007); a salivary gland infec-
tion of T. b. rhodesiense takes, on average, 18 days to mature (Dale et al.,
1995). Contamination with midgut forms during tsetse dissection is almost
impossible to prevent and saliva obtained by encouraging flies to probe
(Majiwa et al., 1994) may also contain regurgitated procyclic (immature)
forms. Farikou et al. (2010) accept that a midgut infection does not indicate
a mature infection that will be transmitted.
4.2.6. Reservoirs of infection

Central to the aim of controlling or indeed eliminating sleeping sickness
must be the understanding that the two forms of disease differ fundamen-
tally in their reservoir hosts. It has long been recognised that the acute
form of sleeping sickness, T. b. rhodesiense, is a zoonotic disease infecting
both humans and wild animals. This was firmly established by Heisch
et al. (1958) who took a natural infection from a bushbuck and infected a
human volunteer. More importantly for present day Africa, in which game
animals are not so prevalent, similar experiments with human volunteers
unequivocally showed that domestic cattle also carried T. b. rhodesiense
(Onyango et al., 1966). Until recently, however, measuring the extent of the
domestic animal reservoir without the use of ‘volunteers’ was not possible
as cattle may also be infected with non-human infective T. b. brucei, indis-
tinguishable from T. b. rhodesiense by microscopy. With the identification of
a molecular marker (SRA gene) for T. b. rhodesiense (Xong et al., 1998), dif-
ferentiation of parasites in animals became possible (Welburn et al., 2001b)
and field surveys revealed that the domestic animal reservoir was the pri-
mary source of human infective trypanosomes for tsetse, with up to 40%
of cattle carrying T. b. rhodesiense in SE Uganda (Fèvre et al., 2001). A recent
survey of 418 wild animals from the Luangwa valley, Zambia, using the
SRA marker gene found 0.5% prevalence for T. b. rhodesiense (Anderson
et al., 2011). This low level is revealing given that wildlife hosts were for
many years regarded as the natural reservoir for T. b. rhodesiense (Heisch
et al., 1958) and is in stark contrast to the situation in SE Uganda where
game animals are no longer common and human infective parasites circu-
late between cattle and man (Batchelor et al., 2009). It follows, in the light
of these data from Uganda, that simply treating infected humans will not
control T. b. rhodesiense sleeping sickness and this is reflected in models
analysing control options (Welburn et al., 2006).
The chronic form of sleeping sickness differs epidemiologically from
the acute form in that T. b. gambiense does not have a significant animal res-
ervoir. van Hoof (1947) showed that T. b. gambiense could be transmitted
cyclically in the laboratory between pigs and human volunteers but there
have been no direct demonstrations of an animal reservoir along the lines
of the T. b. rhodesiense experiments of Heisch et al. (1958). While much
effort has gone into demonstrating T. b. gambiense in various animals using
molecular probes (Herder et al., 2002; Njiokou et al., 2006), it is now gener-
ally accepted that the reservoir for T. b. gambiense sleeping sickness is in
humans, not least because of the lengthy period between infection and
progression to disease in humans; this provides ample time for the disease
to be transmitted to another human host despite the very low risk of tsetse
infection that we have noted. Checchi et al. (2008a) analysed reports of the
progression of T. b. gambiense sleeping sickness and found that the dura-
tion of stage I ranged from a few months to a few years and calculated
a rough estimate of 33 months for the mean total duration of infection.
Checchi et al. (2008b) also examined the role of putative ‘chronic carriers’
in perpetuating transmission and suggest that such carriers could explain
how some sleeping sickness foci are sustained by very few cases (Gout-
eux and Artzrouni, 2000). Kaboré et al. (2011) have provided molecular
confirmation of ‘chronic carriers’; serologically positive subjects that are
apparently negative for parasites by microscopy [and therefore cannot be
treated because of the guidelines (WHO, 1998)] were shown in this survey
from Guinea and Côte d’Ivoire to be carrying T. b. gambiense but at very
low parasitaemia. Further evidence of ‘chronic carriers’ was provided by
Wastling et al. (2011) who, using PCR, found parasite DNA in clinically
unaffected, microscopically aparasitaemic people on the Eastern shores of
Lake Albert, Uganda. Koffi et al. (2006) suggest that there is a ‘long last-
ing human reservoir that may contribute to the maintenance or periodic
resurgences of HAT in endemic foci’, with infections at a level too low
to be picked up by sensitive conventional parasitological detection tech-
niques, and even at the limits of detection by PCR.
Another hidden source of infection of T. b. gambiense may be vertical
transmission of trypanosomes from mothers to offspring. There are few
publications on congenital transmission and it is assumed to be a rare phe-
nomenon. In reviewing the literature from 1933 onwards, Lindner and Pri-
otto (2010) found only 17 cases of certain vertical transmission: 13 cases
with T. b. gambiense and 1 case with T. b. rhodesiense (plus three children of
infected mothers – the children had never entered an endemic country).
These data would indicate that vertical transmission is indeed rare but
there is a serious problem surrounding definition: congenital infection is
usually defined as the diagnosis of sleeping sickness in the newborn of an
infected mother within the first 5 days of life. This cut-off period assumes that,
after 5 days, infections in young children will have come from an infected
tsetse fly rather than the mother. Given the slow rate of development of
T. b. gambiense sleeping sickness, difficulties with diagnostics in rural set-
tings (Radwanska, 2010) and evidence of undetected ‘chronic carriers’
revealed by PCR (Wastling et al., 2011), it seems that this 5-day cut-off
period may be unrealistic. There is evidence from recent surveys to support
this: Eperon et al. (2007) analysed data from Sudanese preschool children
treated between 2000 and 2002 and found that the proportion of children
with stage II sleeping sickness was significantly higher in very young chil-
dren (<2 years); are we to assume that children <2 years are more likely to
be bitten by an infective tsetse fly than older children? Wastling et al. (2011)
found a high proportion of children <12 years positive by PCR in Western
Uganda, again suggesting that younger children are more likely to be bitten
and infected than older people – if not infected congenitally. Khonde et al.
(1997) showed that the risk of sleeping sickness in children was related to
the history of disease in the mother but not in the father, strongly hinting
at maternal transmission. The traditional entomological explanation, based
on the frequency of human–fly contact (Laveissière et al., 1994), is that chil-
dren during the first 2 years of life spend a lot of time with their mother,
and when the mother collects water, the child is exposed to the bites of
riverine tsetse. Daily activities, linked to frequency of human–fly contact,
are usually implicated as important risk factors for sleeping sickness and
responsible not only for higher prevalence rates but also for both spatial
and familial cases clustering (Henry, 1981); again an alternative explanation
for familial clustering could be maternal transmission. Although Gambian
sleeping sickness is more frequently observed in adults than children in
some surveys (Moore et al., 1999), this may simply reflect problems associ-
ated with diagnosis of early stages of T. b. gambiense (Kaboré et al., 2011).
Garcia et al. (2002), in a detailed study of 485 sleeping sickness cases in
Côte d’Ivoire, showed that the age at diagnosis (rather than the mean age
of cases) peaked at <10 years. It may be that there is a silent focus of disease
transmitted congenitally (Wastling et al., 2011) and this could explain the
feature of familial infections that have long been observed within villages
and in T. b. rhodesiense foci (Dukes et al., 1983). In the absence of more
detailed studies of congenital infections, the real risk is unknown (Lindner
and Priotto, 2010).
4.3. DIAGNOSIS AND TREATMENT
4.3.1. Treatment – T. b. gambiense sleeping sickness

As we shall see, control of Gambian sleeping sickness is largely based
on case detection and treatment of the population at risk. This involves
population screening, followed by diagnostic confirmation and staging
(Cattand et al., 2001). Staging is crucial as it defines the treatment that
is prescribed. In stage I, which may last for years (Checchi et al., 2008b),
patients can remain asymptomatic as trypanosomes multiply in tissues
and body fluids; in stage II, trypanosomes cross the blood–brain barrier
and enter the central nervous system (CNS) resulting in various neuro-
logical signs and, if left untreated, death (Brun et al., 2010).
Pentamidine is the drug of choice for treatment of stage I Gambian
sleeping sickness and is generally well tolerated. Melarsoprol, an organo-
arsenic compound, remains the most widely used drug for treatment for
stage II; unfortunately, melarsoprol is a poorly tolerated drug and adverse
reactions are frequent (around 5% suffer an encephalopathic syndrome)
and can be fatal. A new drug, eflornithine (DFMO), is now recommended
by WHO as the first-line treatment for stage II Gambian sleeping sick-
ness as studies have shown that this results in significantly less mortality.
Eflornithine is gradually replacing melarsoprol as the first-line treatment
but treatment with eflornithine is complex lasting 2 weeks, involving four
infusions each day (56 intravenous infusions of >30min over 14 days).
Understandably, adoption of eflornithine has been handicapped by the
demands this treatment makes on rural clinics in both cost and nursing
care; only well-funded non-governmental organisations (NGOs) could
afford to use eflornithine – the kit for two eflornithine treatments weighs
40kg and costs US$ 1420. Despite these constraints, with WHO assistance
with training and drug supplies, by 2009 the proportion of patients treated
with melarsoprol had fallen from 88% to 38% and the use of eflornithine
increased from 20% to 70% (Simarro et al., 2011a).
The complexity of the eflornithine treatment stimulated trials of a therapy
combining nifurtimox (a drug registered for the treatment of Chagas disease)
and eflornithine that could simplify the standard procedure; trials showed
that this nifurtimox–eflornithine combination treatment (NECT) was as safe
to use and as efficacious as eflornithine monotherapy (Priotto et al., 2009).
Kits for four full NECT treatments (costing US$ 1440) have been distributed
by WHO to nine countries and by 2009 were being used in the treatment of
96% of all Gambian sleeping sickness cases (Simarro et al., 2011a).
It is necessary to enter a cautionary note about the emerging problem
of drug resistance. Treatment failures due to melarsoprol drug resistance
in T. b. gambiense first appeared in the 1990s and their incidence rose very
quickly. Selection of resistance to both eflornithine and nifurtimox has
been shown to be relatively easy in the laboratory and reports of treatment
failures with eflornithine monotherapy are emerging in the field (Barrett
et al., 2011). Drug resistance has the potential to undo recent advances in
controlling Gambian sleeping sickness (Simarro et al., 2008).
4.3.2. Treatment – T. b. rhodesiense sleeping sickness

Trypanosoma brucei rhodesiense disease usually presents as an acute
febrile illness with poor demarcation between stages, leading to
death within months. Suramin is used to treat stage I T. b. rhodesiense,
and adverse drug reactions although frequent are usually mild and
reversible. For stage II T. b. rhodesiense disease, when trypanosomes
have crossed the blood–brain barrier, melarsoprol is the only drug in
use and involves lengthy treatment schedules. Adverse reactions to
melarsoprol are frequent and can be life threatening; unfortunately,
the use of efornithine for treatment of T. b. rhodesiense infections is not
advised (Brun et al., 2010).
4.3.3. Diagnostics
As we have seen, staging of sleeping sickness cases determines which
treatment regime is adopted; for both forms of disease, stage II involves
the use of the highly toxic drug melarsoprol or, in the case of Gambian
sleeping sickness, complex drug regimes. It follows that correct diagnosis
is critical.
4.3.4. Diagnosis – T. b. gambiense sleeping sickness

After examination for clinical signs (enlarged cervical lymph nodes,
etc.), the card agglutination test for trypanosomiasis (CATT/T. b. gam-
biense), applied to whole blood, is currently used in most endemic areas.
CATT-seropositive individuals undergo further examination to search for
trypanosomes in the blood, lymph nodes or cerebrospinal fluid (CSF).
Staging relies on examination of the CSF: stage II is defined by the pres-
ence in the CSF of (1) parasites, (2) increase in white blood cell levels or (3)
increased total protein concentration (Chappuis et al., 2005). Despite the
high specificity of CATT, parasitological confirmation – by microscopy
– is required for all CATT-seropositives. The question of treating sero-
logically suspect patients with high CATT titres but without parasitologi-
cal confirmation has long been debated (Simarro et al., 1999) but is only
acceptable in areas of high disease prevalence (>1%) (Malvy and Chap-
puis, 2011). The CATT test, devised 34 years ago (Magnus et al., 1978),
remains the only field assay available for large-scale surveillance but, as
it is based on detection of clone-specific trypanosome antibodies, may not
be reliable in areas where these immunological variants are not present
(Radwanska, 2010). CATT false positives can also occur in patients with
malaria (Magnus et al., 1978).
4.3.5. Diagnosis – T. b. rhodesiense sleeping sickness

There is no equivalent to the CATT test for screening for T. b. rhodesiense
but parasitological confirmation is comparatively simple as trypanosomes
are usually easily seen in thick or thin smears under the microscope. For
staging, examination of CSF follows – as for T. b. gambiense – and deter-
mines which drug regimen is employed.
4.3.6. Molecular diagnostics

Microscopic confirmation of parasites in body fluids of patients remains
the most reliable and convenient diagnostic technique for sleeping sick-
ness suspects and offers many practical advantages when used in rural
areas: easy to use, no cold chain required, high specificity, low cost and
readily available. However, microscopy suffers from lack of sensitiv-
ity and a simple, highly sensitive test that could detect and identify that
trypanosome species is highly desirable. It is estimated that 20%–30% of
patients are missed by the standard parasitological techniques (Robays
et al., 2004) and Kaboré et al. (2011) have shown by molecular methods
that CATT-positive subjects negative for parasites may be carrying T. b.
gambiense at very low parasitaemia.
A range of molecular amplification tests has been developed for
the diagnosis of sleeping sickness, mostly based on the PCR. PCR tests
could, in the right circumstances, replace microscopy as they have been
shown to be sufficiently accurate (Mugasa et al., 2012) and have been
used experimentally to screen CSF (Truc et al., 2012). The problem with
PCR technology is that it is not really practical in rural settings requiring
an uninterrupted electricity supply, cold chain, trained staff and expen-
sive equipment. Isothermal reactions such as loop-mediated isothermal
amplification (LAMP) and nucleic acid sequence-based amplification, that
require less expensive equipment than PCR-based tests, are also under
development (Radwanska, 2010). As there is no equivalent to the CATT
test for Rhodesian sleeping sickness, the discovery of the SRA gene for
human serum resistance in T. b. rhodesiense (Xong et al., 1998) was a break-
through for diagnostics and PCR assays have been developed that can
identify a single trypanosome (Welburn et al., 2001a; Picozzi et al., 2008).
A more formidable problem is the development of a diagnostic tool for
staging sleeping sickness; this would obviate the need for lumbar punc-
tures and, more importantly, aid the critical step of drug choice. Cytokines
and antibodies have been tested as potential biomarkers for CNS infection
but possible interference from other diseases remains an obstacle to prog-
ress (Radwanska, 2010).
4.4. BURDEN OF DISEASE
A WHO Committee estimated in 1998 that 60 million people were at risk

of contracting sleeping sickness in sub-Saharan Africa (World Health
Organization, 1998); the evidence supporting this figure is, however, dis-
putable (Fèvre et al., 2008a). The use of satellite technology has produced
more accurate, localised and hence more useful pictures of populations at
risk. Simarro et al. (2011b) have geo-referenced sleeping sickness records
from six countries in Central Africa (Cameroon, Central African Repub-

lic, Chad, Congo, Equatorial Guinea and Gabon) and by combining these
with human population data have mapped areas according to one of five
risk categories [from very high (>1/100) to very low (1/105 to 1/106)].
Simarro et al. (loc. cit.) calculate that around 3.5 million people are now
at risk in these six countries (8.9% of the population), distributed over an
area of 224,000km2; four very high-risk areas were identified in the Central
African Republic and two in Congo. Risk maps like these could help target
areas for control operations for T. b. gambiense sleeping sickness. We may
need to bear in mind that predicted climate changes in Africa could result
in an increased risk of exposure to sleeping sickness (Moore et al., 2011).
Estimates of the disease situation for the 36 affected countries (World
Health Organization, 2006) showed that the greatest burden of reported
cases was due to T. b. gambiense; for the years 1997 to 2006, there were
36,585, 37,385, 27,862, 25,945, 26,200, 23,832, 19,901, 17,036, 15,651 and
11,382 new cases reported in 24 countries affected. In 2006, 11 of these 24
countries reported no cases. Only three countries reported an average of
>1000 new cases per year: Angola, Democratic Republic of Congo (DRC)
and Sudan together comprising 90% of the total reported T. b. gambiense
cases. Approximately two-thirds of reported T. b. gambiense cases occur
in DRC.
Trypanosoma brucei rhodesiense cases for the same decade were 592,
606, 619, 669, 750, 655, 514, 580, 727 and 486 in 13 affected countries. Only
two countries, Tanzania and Uganda, reported more than 100 new cases
per year, representing around 90% of the total. Five countries reported
no cases over the decade and four reported sporadic cases. Latest sleep-
ing sickness incidence data from WHO for 2010 show a decrease of 28%
from a total (both forms of disease) of 9878 cases in 2009 to 7139 new
cases in 2010 for the 36 endemic countries (http://www.who.int/neg
lected_diseases/disease_management/HAT_cases_drop/en/index.h
tml). Uganda is the only country affected by both forms of disease. For
a detailed breakdown of WHO incidence data for both forms of disease,
see Simarro et al. (2008).
Fèvre et al. (2008a) stress that proper quantification of the burden of
the ‘neglected diseases’ really matters, as the primary reason for their
neglect is that the true impact of the disease on society is unknown. The
overall cost of treating a case of Rhodesian sleeping sickness is estimated
to be around $150 (Fèvre et al., 2008b). Assessing disease burden is a pre-
requisite for planning disease control and the disability-adjusted life year
(DALY) is now a well-established tool for assessing burden (i.e. impact) of
disease. DALYs are useful in comparing the economic burden imposed by
different diseases in order to prioritise health expenditure, for example,
spend/DALY averted. For example, a study of the cost-effectiveness of a
control programme in DRC found that 1408 DALYs has been averted, for
a cost of US$ 17 per DALY averted (Lutumba et al., 2007). These data may
need amending in light of the increased cost of newly introduced NECT
treatments.
4.4.1. Hidden burden of disease

In the context of sleeping sickness, it is important to recognise that WHO
incidence data are based on reported cases; in an African setting, cases that
do not reach a hospital (often for the simple reason that poor people are
unable to afford treatment) are not reported. For example, in Uganda it
is estimated that 92% of deaths from T. b. rhodesiense sleeping sickness go
unreported (Odiit et al., 2005) and in Tanzania 45% (Matemba et al., 2010).
During an outbreak of sleeping sickness in Serere, Uganda, T. b. rhodesiense
cases consumed 30% of in-patient time in the local health centre but mor-
tality due to unreported cases was shown to be the major contributor to
the health burden placed on the local population (Fèvre et al., 2008b). For
T. b. gambiense, cases will inevitably be missed in areas where no active
case detection takes place (Robays et al., 2004). Recent detailed surveys
using PCR have shown that under-reporting of T. b. gambiense – estimated
to be as high as 50% – is a serious issue in DRC (Mumba et al., 2011).
How does sleeping sickness rank in importance when compared with
the other ‘NTDs’ that place a burden on local health services? Sleeping sick-
ness (taking both forms together) was estimated to impose a burden of 1.3
million DALYs (World Health Organization, 2003), ranking around the same
level as schistosomiasis (1.4 million DALYs) and leishmaniasis (1.7 million
DALYs), neither of which are confined to Africa. Obviously, in many sub-
Saharan African countries, the national burden of malaria exceeds by orders
of magnitude that of sleeping sickness and many other neglected infections.
However, because of its high mortality and acute clinical course, T. b. rhod-
esiense, sleeping sickness at a localised level can have a DALY estimate that
is high even in comparison with malaria. Locally, sleeping sickness may
assume much greater economic importance given the necessity for hospi-
talisation and high cost of drugs (Fèvre et al., 2008a). For T. b. rhodesiense
sleeping sickness, hospital-based interventions have been shown to be cost-
effective in rural settings in Uganda, with a mean cost of US$ 8.50 per DALY
averted; compared to treatment of other infectious diseases this has been
shown to be very cost-effective (Fèvre et al., 2008b).
4.5. CONTROL
When considering control options for sleeping sickness, we must bear in

mind the major difference between the two parasites involved: the relative
importance of animal hosts in the maintenance and spread of infection.
We can assume for all practical purposes that T. b. rhodesiense is an infec-

tion primarily of animals that occasionally spills over into humans, while
T. b. gambiense is a human infection that is occasionally seen in animals
(Welburn et al., 2001a). This epidemiological distinction, as we shall see,
is reflected (consciously or subconsciously) in the differing control strate-
gies that have been adopted for the two diseases. Failure to observe this
distinction can, and has, led to the use of inappropriate control strategies
that can prove costly.
4.5.1. Origins of epidemics

The origins of the great epidemics of sleeping sickness in the early part
of the twentieth century were much researched by the Colonial powers
and it was held that these epidemics resulted from people’s new-found
freedom to move around (both within and between countries) – a freedom
conferred by the peace (‘pax Britannica’) the colonial powers had imposed
militarily on African society following the Conference of Berlin (1884) and
the subsequent ‘scramble for Africa’ (Packenham, 1991). In his seminal
work, Ford (1971) turned this generally accepted view on its head and sug-
gested that, rather than peace, the effect of the colonial occupation of Africa
had been to promote discord between people and their environment –
an environment which Ford suggested had been finely balanced. The tides
of disease from 1900 onwards were caused by the shocks an intrusive colo-
nial system had wrought on a previously stable African ecosystem – in
Ford’s words: ‘Bellum Britannica’. The colonial regimes’ introduction of
intensive systems of agriculture for cash crops such as cotton altered, in
Ford’s view, the environment in sub-Saharan Africa – an environment that
millennia had settled in balance. Ford suggested that epidemics of try-
panosomiasis (both human and animal) had their origins in ancient foci of
disease and were triggered by social upheaval that upset the natural eco-
logical balance, resulting in ‘epidemiological disorder’ and inevitably in
epidemics of sleeping sickness. As there was neither effective chemother-
apy nor means of controlling tsetse populations at the time of the great
sleeping sickness epidemics in Uganda and the DRC (c. 1900), attempts to
control the disease were based simply on isolating those thought infected.
The French and Belgian colonial authorities viewed sleeping sickness as
primarily a medical problem and sought medical solutions firstly by iso-
lating those affected by the disease in lazarets; as there was no treatment
for sleeping sickness in the early years of the twentieth century, the lazarets
became prison camps and the patients were left to die. The British authori-
ties in Uganda simply moved the whole population of Busoga away from
the shores of Lake Victoria. Whether these draconian measures led to the
control of these epidemics (which incidentally were of different forms
of disease: T. b. gambiense in DRC and T. b. rhodesiense in SE Uganda) or
whether, as with most epidemics, incidence peaked and fell, we cannot

be sure.
John Ford was an entomologist and the ‘epidemiological disorder’
at the beginning of the twentieth century resulted, in his view, from the
expansion of tsetse populations following on the rinderpest epizootic
between 1896 and 1898. This epizootic resulted in the loss of grazing ani-
mals and was thought to have led to the replacement of grasslands by
bush that was conducive to the spread and growth of tsetse populations
that in turn spread sleeping sickness. There is a problem with this view in
that we now know that the major vector of sleeping sickness in Busoga
(G. f. fuscipes) would have been largely unaffected by the loss of grazing
animals as this fly relies mainly on reptiles, particularly monitor lizards for
its blood meals (Clausen et al., 1998; Waiswa et al., 2006). Reptiles would
not have been affected by rinderpest but we can also assume that not all
cattle were eliminated by the epizootic (Mack, 1970). Host animal elimi-
nation was tried as a tsetse control measure in the past and was found to
be inefficient unless every host animal were eliminated (Hargrove, 2003).
We have more insight into the causes of the T. b. gambiense epidemics
that sprang up at the end of the twentieth century, which were unrelated
to the ‘spread’ of tsetse populations. Rather, these epidemics in Sudan
(Moore and Richer, 2001), north-western Uganda (Paquet et al., 1995), DRC
(Van Nieuwenhove et al., 2001) and Angola (Stanghellini and Josenando,
2001) represented the reawakening of ancient T. b. gambiense foci of infec-
tion that had been kept in check by disease control activities. Surveillance
and active case finding had, however, lapsed during the decades of civil
disturbances in those countries and disease prevalence correspondingly
increased (Van Nieuwenhove et al., 2001; Cattand et al., 2001).
By contrast, the outbreak of T. b. rhodesiense sleeping sickness in Busoga,
SE Uganda, in the 1980s cannot be related to the loss of active case finding
as this strategy had never been the mainstay of disease control in Busoga.
Rather, the disease had been kept under control, after the introduction of
insecticides in the 1950s, by ground spraying (to keep the tsetse population
in check) accompanied by treatment of human cases – largely self-reporting.
The 1980s Busoga epidemic was brought to an abrupt halt by three rounds
of aerial spraying using endosulfan (see Fig. 1 in Welburn et al., 2006). The
epidemic has since spread from north from Busoga to affect the central
areas of Uganda surrounding Lake Kyoga, largely as a result of the move-
ment of cattle carrying T. b. rhodesiense (Batchelor et al., 2009).
Berrang-Ford et al., (2011) suggest that ‘political terror’ was the main
driver of epidemics of the twentieth century. Ford (1971) was the first
to suggest that ‘wars’ were at the root of the problem of sleeping sick-
ness outbreaks but his idea of a war was not the simplistic view of men
wielding Kalashnikovs but a far more nuanced view. While ‘wars’ may
be linked to sleeping sickness epidemics (Kaba et al., 2006), the association
is likely to be correlative rather than causative. It is improbable that the

very rapid surges in incidence of sleeping sickness seen in the twenti-
eth century arose simply from increases in human–fly contact; such dis-
ease spikes would require huge increases in tsetse numbers, given the
very low transmission rates of tsetse. Tsetse population increases of this
order would take several years and would not correlate with short-term
socio-economic turmoil (Hargrove, 2003). Khonde et al. (1995) suggest
that people previously infected by T. b. gambiense develop a very signifi-
cant immunity to the disease. Checchi et al. (2008b) further suggest that
‘chronic carriers’ could play a key role in perpetuating transmission of T. b.
gambiense and might explain how certain foci appear to be extinguished,
only to reawaken mysteriously after several years. Endfield et al. (2009) tell
a story of civil, religious and colonial warfare, drought, famine, flood and
pestilence (plague, smallpox and rinderpest) all preceding the devastating
epidemics of T. b. gambiense and T. b. rhodesiense in 1900–1920. If we accept
the idea of ‘chronic carriers’, then the epidemics of T. b. gambiense seen in
the twentieth century might relate more to periods of famine that would
have affected the immune system of starving people, allowing parasitic
diseases previously held in check (that would include sleeping sickness)
to re-emerge synchronously. There is, however, no evidence of a ‘chronic
carrier’ state in T. b. rhodesiense and it is difficult to relate the epidemics of
this disease to famine, unless suppression of the immune system allowed
infections to establish in people who would normally have resisted T. b.
rhodesiense-infected bites of tsetse.
4.5.2. Controlling T. b. gambiense sleeping sickness

Sleeping sickness incidence data (both forms) from 1900 onwards show
the number of new cases reaching a peak of more than 70,000 in 1930, then
gradually falling to very low levels in 1960. A period of calm in the 1960s
was followed by a surge in incidence from the 1970 to 1997 when new
cases totalled almost 40,000 per annum (Simarro et al., 2008). There has
since been a very encouraging decline in the incidence of T. b. gambiense to
around 11,000 new cases in 2006 (World Health Organization, 2006). After
continued control efforts, the number of cases reported in 2009 dropped
below 10,000 for the first time in 50 years; this trend has been maintained
with 7139 new cases reported in 2010 (WHO estimate that the number of
actual cases – allowing for under-reporting – is currently 30,000; http://www.
who.int/mediacentre/factsheets/fs259/en/).
The French and Belgian colonial authorities viewed sleeping sickness
control as primarily a medical problem and sought medical solutions.
Usable drugs became available in the 1920s: suramin, for stage I, and tryp-
arsamide, an organo-arsenic compound, for stage II. The Francophone
countries of West Africa adopted both drugs to treat Gambian sleeping
sickness. Eugene Jamot who, between 1925 and 1935, treated thousands
of cases in Cameroon and Upper Volta promoted this policy vigorously.
Jamot also understood that passive screening would not solve the problem
of the human reservoir of disease and ‘Jamot’s doctrine’, also adopted by
the Belgian authorities in the Congo, decreed that infected people should
not move but should be treated by mobile medical teams (Stanghellini,
1999). Post 1945, chemoprophylaxis using the less toxic drug pentamidine
(a stage I drug) was introduced; usually two to four doses at 6-monthly
interval injections were given. Mass treatment ‘pentamidinisation’ cam-
paigns were instigated on an unimaginable scale in West Africa. Chemo-
prophylaxis with Lomidine (the French name for pentamidine) became an
annual event in the 1950s along the Congo River, with around a million
people treated on both French and Belgian banks of the river. This tactic
was extended across Francophone West Africa; British colonies in West
Africa also adopted massive pentamidinisation schemes (Waddy, 1970). In
practice, Jamot’s approach was highly effective; by 1965, the incidence of
sleeping sickness in the Francophone countries of West Africa had fallen
to 0.02% (in a survey of almost one million people) compared with, for
example, 0.85% before chemoprophylaxis in the Congo. The aim of the
Colonial regimes was always ‘eradication’ and they were constantly frus-
trated by their inability to achieve this in many disease foci using chemo-
prophylaxis. It is unsurprising that the strategy became very unpopular
with the communities involved and led to treatment avoidance, which, in
turn, made elimination by chemotherapy unrealistic.
If we link the time frame for the introduction of chemotherapy with
incidence data from1930 to 1960, we can see that decline synchronised with
the adoption of the ‘Jamot doctrine’ (Simarro et al., 2008; for a description
of Jamot’s work, see Courtin et al., 2008). However, this strategy is expen-
sive to maintain and requires good logistics; it is unsurprising that there
was a surge in incidence of sleeping sickness from 1970 to 1997 linked to
changes in the priorities of postcolonial governments and knock-on effects
of civil wars in some endemic countries. As health services were restored,
the number of people under active surveillance increased between 1997
and 2006 and the number of new cases decreased (69% reduction) (Simarro
et al., 2008). This was achieved by simply focussing control activities on the
human reservoir of disease and ignoring any putative animal reservoir –
this was considered to have only a minor impact on the transmission of
T. b. gambiense (Simarro et al., 2008). In the absence of an animal reservoir,
it can be seen intuitively that controlling T. b. gambiense sleeping sickness
can be best achieved by removing the human reservoir of disease or –
more difficult – removing the vector and this is borne out by modelling
control options (Welburn et al., 2001a).
Khonde et al. (1995) offer an intriguing insight into the origins of the
very long inter-epidemic periods observed in the twentieth century when
low prevalence rates persisted for several decades despite conditions

favouring human–fly contact in these areas. Khonde et al. (loc. cit.) suggest
that this could be because of the selection of an immune population dur-
ing an epidemic and that it takes several decades for the pool of suscep-
tible individuals to reach sufficient size for the next epidemic to take off.
4.5.3. Tsetse control and T. b. gambiense

In West Africa during the colonial period, chemotherapy – coupled with
active case finding using mobile teams – produced a sharp decline in inci-
dence in Nigeria between 1935 and 1960 with about 500,000 treatments
(Ford, 1971); despite this success, it was still assumed that tsetse control
was a necessary adjunct to sleeping sickness control. An example from
Nigeria illustrates this attitude: the Anchau scheme for rural development
and resettlement was planned in response to an outbreak of sleeping sick-
ness in villages near Zaria (Nash, 1948). Firstly, tsetse flies were removed
from the ‘Anchau corridor’ by clearing riverine vegetation from an area
70 miles long and 10 miles wide; people were then resettled in the centre
of the corridor. Five thousand people were moved from 45 hamlets and
housed in 16 new villages and one town, while a further 60,000 people
were helped by freeing areas of tsetse and providing good wells, schools
and marketing facilities at a cost of US$ 150,000 (equivalent to around
US$ 1.3 million today). Together with mass chemotherapy, the annual inci-
dence of sleeping sickness was reduced from 30% in 1934 to 0.2% in 1946.
The success of this scheme, which we would now consider a community
development project, may have had less to do with the elimination of the
risk of tsetse fly bites and more with general improvements in people’s
health care and welfare that such a scheme promoted. Similar outbreaks
of sleeping sickness were attacked with a mixture of chemotherapy and
tsetse control; for example, an outbreak on the Jos Plateau, where mortal-
ity was linked closely with the density of G. p. palpalis (Ford, loc. cit.). It is
tempting to speculate whether similar success could have been achieved
solely by chemoprophylaxis of people at risk and at less cost. Ford (loc.
cit.) observed that T. b. gambiense was completely eliminated from a clan of
the Tiv people of Nigeria as a result of 2 years (1956–1958) of pentamidine
prophylaxis. Ford (loc. cit.) notes that the withdrawal of the prophylaxis
should have been the signal for reappearance of the disease as close man–
fly contact persisted within the villages of this focus – if there had been an
animal reservoir of T. b. gambiense. However, Ford does not raise the more
interesting question: was tsetse control – a major part of control strategy in
Nigeria – really necessary to remove sleeping sickness foci?
Logic would suggest that in the light of this, and work in other coun-
tries, there is no need to include tsetse control in tactics for controlling
T. b. gambiense. Cattand et al. (2001) argue that for T. b. gambiense – with its
extended asymptomatic preclinical course – the only suitable approach is

active surveillance using mobile teams. Compelling evidence comes from
the work of Simarro and his colleagues in Equatorial Guinea and Angola;
using only surveillance (active and passive) and treatment of all cases
(both parasitological and serological positives) between 1985 and 2004,
the disease was eliminated from Bioko Island, Equatorial Guinea – the last
sleeping sickness case was seen in 1995 (Simarro et al., 2006). While tsetse
control had been used on the island (Simarro et al., 1991), this was aban-
doned as too expensive. Interestingly, Cordon-Obras et al. (2010) recently
found a fly positive for T. b. gambiense (1/259) on Bioko Island; unfortu-
nately, the PCR analysis was based on whole flies so we cannot know if
this was a mature (i.e. transmissible) infection and, as we have discussed
(Section 2.5), this may simply reflect DNA from a recent blood meal that is
unlikely to mature. In the Quicama municipality of Luanda, Angola, the
prevalence of disease was significantly decreased by active surveillance
and treatment without any vector control, which was considered neither
necessary nor feasible at the time (Ruiz et al., 2002). Critics of this approach
would say: (i) the programme in Equatorial Guinea was on an island and
hence a limited exercise and (ii) the programme in Luanda did not achieve
disease elimination. However, Simarro et al. (2011a) clearly think that the
gambiense form of sleeping sickness can be ‘eliminated as a public health
problem’ in many foci by simply implementing active surveillance within
the national health systems of affected countries, always assuming the
costs of such a system are locally sustainable. There are some dissenting
voices however: Robays et al. (2004) analysed data from DRC and found
that using mobile teams for active case detection and treatment strategy
was <50% effective overall, the major problem being attendance rates/
mobile team which averaged 74%. Robays et al. (loc. cit.) conclude that
active screening only leads to reasonable effectiveness if the attendance
rate is sufficiently high, even if other parameters (including diagnostics)
are optimised.
Given the general acceptance of the efficacy of the active surveillance
approach, the widespread adoption of tsetse trapping (baits, etc.) to control
outbreaks of Gambian sleeping sickness in the 1980s might be seen as over-
kill. While insecticide-impregnated targets may indeed be one of the most
effective tools for control of riverine tsetse in West Africa (Rayaisse et al.,
2011), there is an underlying assumption that tsetse control is necessary for
controlling Gambian sleeping sickness (see, e.g. Joja and Okoli, 2001).
In their analysis of T. b. gambiense sleeping sickness foci in West Africa,
Courtin et al. (2008) note that some foci in Senegal, Mali and Burkino Faso
have disappeared altogether, despite the fact that tsetse are still present in
these historic foci.
Interest in removing the vector as a means of eliminating sleeping
sickness from West Africa was stimulated by the success of a large-scale
programme aimed at removing tsetse from the whole of the north of Nigeria
by ground spraying with DDT (dichloro-diphenyl-trichloroethane) and
dieldrin in the 1950s to 1960s (Davies, 1964). This military-style approach,
together with the harsh environmental conditions in northern Nigeria,
where the fly was in any case on the limits of its distribution, favoured
tsetse control, even elimination. However, when this plan was extended
to the middle belt of Nigeria, success proved elusive; the high humidity
favoured year-round tsetse survival and also inhibited the residual activity
of insecticides (Jordan, 1986). Moreover, insecticide-based control schemes
became increasingly difficult to justify with growing environmental mis-
givings. Interest turned to more environmentally friendly technology.
Research on trap development took place in West Africa to deal specifically
with the problem of controlling riverine species of tsetse responsible for
transmitting sleeping sickness (Challier and Laveissière, 1973; Laveissière
and Couret, 1980; Lancien and Gouteux, 1987). These traps were not as
efficient as the baited traps that had proved so efficient in southern Africa
(see below) and much research effort has gone into improving trap effi-
ciency. However, to date, artificial attractants have produced only modest
increases in trap catches of West African riverine tsetse species (Rayaisse
et al., 2010) but have resulted in improvements in the cost-effectiveness
of insecticide-impregnated targets (Rayaisse et al., 2011). Despite much
research effort, it appears that using artificial host odours to raise catches
of riverine species of tsetse significantly beyond that of unbaited traps has
been found to be difficult if not impossible (Torr and Solano, 2010).
It should be noted that the aim of the tsetse control operations in N
Nigeria in the 1950s was not to deal with sleeping sickness but primar-
ily to provide a tsetse-free environment for cattle keepers – the driver
was not human health but animal health. This message appears to have
been forgotten and we continue to see plans to remove riverine tsetse
populations for the purpose of eliminating T. b. gambiense sleeping sick-
ness. Modelling has shown that T. b. gambiense sleeping sickness may
be controlled either by removing the human reservoir of disease or by
removing the vector (Welburn et al., 2001a). Modelling by Artzrouni and
Gouteux (1996) indicates that detection of sick individuals is more effi-
cient than vector control for controlling T. b. gambiense sleeping sickness
in an endemic situation. Simarro et al. (2011a) suggest that resources are
better directed at active surveillance, diagnosis and treatment that can
lead, in the absence of any other intervention including tsetse control, to
reduced T. b. gambiense incidence. Although we have seen that failures
in medical services resulting from civil disruption can quickly lead to
epidemics of T. b. gambiense sleeping sickness, restoration of surveillance
can bring the situation under control without the need for expensive
and hence unsustainable tsetse control campaigns (Robays et al., 2004).
4.5.4. Controlling T. b. rhodesiense sleeping sickness

In the period, between 1997 and 2006, control activities focussing on
the human reservoir of T. b. rhodesiense showed a much smaller shift
in the number of cases (21% reduction) compared with the promis-
ing data for T. b. gambiense. This difference is attributed to the major
role of the animal reservoir in transmission of T. b. rhodesiense (Simarro
et al., 2008). We have seen that in Uganda [which, with Tanzania, is
one of only two countries with an incidence of >100 cases per year
(Simarro et al., loc. cit.)] domestic cattle is now the major reservoir of T. b.
rhodesiense parasites (Fèvre et al., 2001). In this situation, active sur-
veillance and treatment are not sufficient to control the disease as flies
will constantly reinfect people by bringing parasites from infected live-
stock. Welburn et al. (2001a) modelled the various control options for
T. b. rhodesiense sleeping sickness by extending the multi-host model
of African trypanosomiases developed by Rogers (1988). Chemopro-
phylaxis of animals is shown in this model to be an effective option
for T. b. rhodesiense control, as the animal reservoir is a more impor-
tant component of the overall effective reproductive number R0 (i.e.
the number of secondary infections resulting from a primary case in a
population in which some individuals might not be susceptible). How-
ever, vector control is also shown to be effective for T. b. rhodesiense
sleeping sickness control, regardless of the livestock reservoir
(Welburn et al., 2001a).
4.5.5. Tsetse control and T. b. rhodesiense

The introduction of insecticides, post 1945, proved to be a watershed in
approaches to tsetse control. Ground spraying of residual insecticides
was used, indiscriminately at first but then more specifically on the rest-
ing sites of tsetse, at larger and larger scales. The development of these
spraying technologies was not aimed at sleeping sickness but primarily
at trypanosomiasis in livestock, which remains a heavy burden on live-
stock keepers across vast swathes of Africa (Shaw, 2004). It is estimated
that between the 1950s and the 1980s, around 400,000km2 were sprayed
in this way (Allsopp and Hursey, 2004). These spraying operations, while
highly effective in Nigeria, Kenya, Uganda and Zimbabwe, were logisti-
cally complex, labour intensive and hence costly but fell out of favour
largely because of concerns about the environmental damage caused by
the use of organochlorine insecticides such as DDT. However unfash-
ionable, Okoth et al. (1991) found that ground spraying with lambda-
cyhalothrin in Tororo District, Uganda (an eastward extension of the
Busoga focus), effectively reduced the incidence of sleeping sickness for
6 months.
4.5.5.1. Aerial spraying

Ground spraying was superseded by aerial spraying in the 1970s and was
shown to be a very efficient tool, covering large areas without large labour
forces. Non-residual insecticides could be applied by fixed-wing aircraft
as low-dosage aerosols, with five treatments at intervals of 15–20 days (to
ensure treatment of tsetse emerging from pupae in the ground – the pupal
period lasting c. 27 days at 25°C – Hargrove, 2005). This sequential aero-
sol technique (SAT) was employed extensively in Botswana and Zimbabwe
firstly using the organochlorine endosulfan and then synthetic pyrethroids
(Allsopp and Hursey, 2004). Despite the low insecticide dosages used in SAT
and evidence that this technique presents limited environmental risk (Grant,
2001), the widespread use of insecticides for tsetse control fell out of favour
by the end of the 1980s. Aerial spraying was seen at its most impressive in
the Okavango delta, Botswana; aircrafts spraying very low doses of delta-
methrin have eliminated tsetse from an area of over 7000km2 (Kgori et al.,
2006). As we have seen, the 1980s epidemic of T. b. rhodesiense sleeping sick-
ness in Busoga, Uganda, was halted aerial spraying (Welburn et al., 2006).
There is no doubt that aerial spraying can be effective but this approach is
extremely expensive when compared with other technologies (Shaw, 2004).
4.5.5.2. SIT
The sterile insect technique (SIT), involving the release of artificially reared
sterile males, offers an environmentally friendly option for tsetse control
and has been used successfully to eliminate tsetse from Unguja Island,
Zanzibar (Vreysen et al., 2000). However, the use of SIT in African settings
has been criticised on ecological, logistical and cost grounds. Hargrove
et al. (2011) comment that, since SIT is always used together with other
techniques (e.g. targets, insecticide-treated cattle), it simply adds hugely
to operational costs.
4.5.5.3. Bait technology

In an effort to provide greener technologies, research both in Francophone
and in Anglophone Africa turned in the 1970s to the development of
‘bait’ technologies. The use of three-dimensional traps made to resemble
(and even containing) cattle, known to be attractive to tsetse, had been
explored in the 1930s and 1940s; some even incorporated insecticides
(DDT) (Buxton, 1955). These traps were unwieldy and costly and, with
the advent of insecticide ground spraying, were largely abandoned as
impractical. Buxton (loc. cit.) confessed that he had ‘no clear understanding
of what it is that attracts a tsetse towards a trap’ but into this knowledge
gap stepped a small but determined group of scientists in Zimbabwe who
identified the major components that attracted tsetse. Using electrocuting
nets to capture tsetse attracted to oxen, it was possible to remove humans
from the equation, as humans were shown to actually repel savannah

tsetse species, particularly female tsetse. It soon became clear that tsetse
used odour to detect their hosts and that the olfactory stimulus was more
important than the visual; roughly 80% of the flies arriving at an ox could
be attributed to the olfactory stimulus (Vale, 1974). By constructing a pit
large enough to house oxen and using a fan to provide above ground the
olfactory stimulus of the oxen, but without a visual stimulus, it was found
that the catch just kept increasing with numbers of oxen, i.e. odour; with
sufficient cattle, it was possible to catch over 14,000 tsetse flies in a 3-hour
period (Hargrove et al., 1995).
It followed that if the chemicals responsible for olfactory attraction
could be identified, it might be possible, by using them in sufficient quanti-
ties, to attract and kill enough tsetse flies to provide a very efficient method
of tsetse control. Tsetse biology played a part in this thinking: female tsetse
produce only one offspring at a time, at approximately 10-day intervals
and simple calculations have shown that no tsetse population can grow if
the adult female death rate exceeds about 3.5% per day (Hargrove, 2005).
With the huge numbers of savannah flies that could be caught by using
odours, this seemed a very easy target. The quest then centred on sim-
ulating ox odour; carbon dioxide, acetone and 1-octen-3-ol were identi-
fied from cow breath and 4-methylphenol and 3-propylphenol from cow
urine. Artificial baits (odour-baited targets – simplified traps – treated
with insecticide) were then deployed in southern and eastern Africa, not
only to reduce tsetse populations but also to try to eliminate sections of
the savannah fly belt; by the end of the 1980s, aerial and ground spraying
had been abandoned in Zimbabwe and replaced with insecticide-treated
targets (Vale and Torr, 2004).
4.5.5.4. Live baits

It soon became apparent that, when used on a large-scale, artificial baits
were labour intensive and costly; traps/targets, apart from the cost of
manufacture, required regular maintenance and sustainability became
an issue. Ironically, it transpired that treating cattle with insecticide pro-
vided far more effective baits than the artificial types, with the bonus that
artificial odour attractants were not necessary as animals provided them
naturally. Treating cattle with insecticides had been tried as a tsetse con-
trol measure in the 1940s (Whiteside, 1949) but the use of DDT on cattle
proved impractical, as it was not sufficiently persistent and posed eco-
logical problems. With the introduction of new formulations of synthetic
pyrethroids, treating cattle became a practical proposition both in south-
ern (Thomson, 1987; Thompson et al., 1991; Vale et al., 1999) and in West
Africa (Bauer et al., 1992). The main drawback to the universal adoption
by farmers in Africa of cattle as live bait for tsetse/tick control was the
insecticide cost, especially of ‘pour-on’ formulations (Bauer et al., loc. cit.).

However, experiments showed that effective control could be achieved
by treating only the body regions where most tsetse land: the belly and
lower legs of older and larger cattle in a herd (Torr et al., 2001). This
‘restricted application’ technique reduced the costs of treatment by 90%.
While the use of insecticide-treated cattle has its drawbacks [resistance in
tick populations (Eisler et al., 2003) and environmental side-effects (Vale
et al., 2004)], restricted application not only reduced costs but also reduced
environmental risks. The ‘restricted application’ technique has an added
bonus in that it also controls tick-borne diseases that artificial traps and
targets cannot.
Many factors affect the efficacy of using insecticide-treated cattle for
tsetse control (Hargrove et al., 2002) but the most important is the number
of cattle that need to be treated as this affects cost and hence sustainabil-
ity of the control programme. The question also arises as to whether it is
also necessary to treat the animal reservoir of disease at the same time
as spraying cattle – this is an expensive option. Hargrove et al. (in press)
have now modelled this problem and indicate that sleeping sickness may
be controlled by treating only 20% of cattle with insecticides – compared
with the need to treat 65% with trypanocides.
4.6. DISCUSSION
We are in an inter-epidemic period when those concerned with sleeping

sickness control and, more importantly, donors and their advisors may be
(are?) tempted to suggest that we have seen the back of this disease and
seek to move on to more topical issues (Molyneux et al., 2010). Unfortu-
nately, the WHO Global Burden of Disease (GBD) trumps all other con-
siderations in this situation drawing ‘on a wide range of data sources to
quantify global and regional effects of diseases, injuries and risk factors
on population health’; the overall burden of disease is assessed using the
DALY (http://www.who.int/healthinfo/global_burden_disease/en/).
AIDS, TB and malaria, with their huge DALY burden, have unsurprisingly
monopolised the global health agenda; it is a simple matter to consult GBD
tables and allocate resources accordingly. At present, sleeping sickness
incidence reflects naturally low rates of transmission and consequently is
removed from the list of health care priorities – described by Simarro et al.
(2008) as the ‘punishment of success’. Simarro et al. (2011b) question the
use of the DALY in relation to sleeping sickness and describe its use as a
‘tyranny’; they suggest that GBD in DALYs simply justifies the lack of inter-
est of donors when the burden of the disease is decreasing. In parallel with
the difficulties associated with finding resources for disease control, much
needed research to provide new tools to eliminate the disease will similarly
prove increasingly hard. King and Bertino (2008) echo Simarro et al. (loc.
cit.), arguing that underestimation of disease burden is inevitable in sub-
Saharan Africa due to extrapolation from scant data; this means ‘estimates
will be only approximate with a strong tendency towards underestimation
of disease burden’. As we have seen, under-reporting is a significant prob-
lem in estimating the burden of disease of sleeping sickness. For example,
in SE Uganda for every death reported, 12 deaths remain unreported; the
ratio of unreported cases is about 7 unreported to 10 reported so about 60%
of cases are reported (Odiit et al., 2005). Simarro et al. (2011b) suggest that
unless we develop new technologies and apply tools we know can work,
then we will ‘open the door for the re-emergence of the disease’.
It is our view that this seesawing – between heightened states of panic
(during epidemics) and complacency – undermines our ability to elimi-
nate sleeping sickness from Africa. As sleeping sickness is a fatal disease
of normally low prevalence, it should and can be eliminated if we (a) put
to use the effective tools available and (b) concentrate our research efforts
on the development of cheap, simple to use diagnostics and non-toxic
therapies. This will require a sea change, not only in research and develop-
ment but, more importantly, in funding priorities (Molyneux et al., 2010).
However, in order to reverse this attitude of neglect from donors and gov-
ernments, it is incumbent on those involved in research to provide some
guidance for prioritisation.
In this review, we have seen that for T. b. gambiense sleeping sickness
there are serious issues with diagnostics and drugs. The rising costs asso-
ciated with the best available drug therapy (NECT) have brought into
question whether use of this treatment is sustainable and underline the
continued need for new drugs that are simpler to administer and cheaper
than those at present available (Simarro et al., 2012). Solving the problem
of drug resistance is probably the most difficult task given the paucity of
new treatments that have appeared over the past 50 years. Barrett et al.
(2011) warn that if new drugs do not appear soon, there is a risk that the
current downward trend in disease prevalence will be reversed and, as
has happened in the past, the disease will become resurgent, only this
time in a form that resists available drugs.
The search for new diagnostics has been very productive – indeed we
are faced with a plethora of novel diagnostics (Wastling and Welburn,
2011). Despite the enormous technological progress in molecular parasi-
tology in recent years, the most convenient and reliable diagnostic tech-
nique remains observation of trypanosomes in body fluids by microscopy.
As Radwanska (2010) points out, there is a disconnect when it comes to
sleeping sickness diagnosis between (i) the world of modern experimen-
tal laboratories and (ii) field diagnostics, where the only semi-commer-
cial test in use (CATT) was introduced over 30 years ago (Magnus et al.,
1978). Radwanska (loc. cit.) concludes that this lack of progress in field
diagnostics is not due to a lack of scientific interest or research funds, but

mainly from translating basic research into field-applicable diagnostics
(Radwanska, loc. cit.). To bridge this gap, the Foundation for Innovative
New Diagnostics is promoting the development of isothermal diagnostics
for sleeping sickness with the LAMP test looking promising as a tool for
field use (Ndung’u et al., 2010). However, there remain concerns about
the practicality of using LAMP as a diagnostic tool in remote settings:
template preparation, heating blocks, electricity, a cold chain and multi-
ple manipulations (Deborggraeve and Buscher, 2010). There is no doubt
that isothermal DNA amplification techniques have potential as molecu-
lar diagnostics for both forms of sleeping sickness; whether this research
effort will translate into clinical diagnostics or whether they are merely
another addition to an ever-expanding toolbox of molecular assays for
research is unclear.
Diagnostics are central to the control of T. b. gambiense sleeping sick-
ness; as we have seen, the most effective means of control remains active
case finding by mass population screening (Simarro et al., 2011b). To
achieve successful control, this approach is reliant on diagnostic confir-
mation and staging. In rural Africa, due to a lack of hospital infrastruc-
ture, suspects might be subjected to six consecutive diagnostic tests before
being treated in order to confirm their infection status. In practice, the
diagnostic methods used for sleeping sickness confirmation are cumber-
some and inaccurate due to inadequate sensitivity and specificity of cur-
rently available tests (Radwanska, 2010). At present, the identification of
parasites using molecular tools is rarely, if ever, implemented during field
surveys by National Sleeping Sickness Control Programmes (NSSCPs).
The authors have used FTA®cards for over 10 years for the rapid collec-
tion and archiving of a large number of samples from people and cattle
for the molecular diagnosis of T. b. rhodesiense using PCR. While there
are some difficulties in the downstream processing of these cards, we
have developed a best practice protocol for processing from FTA®cards
(Ahmed et al., 2011). A practical solution to accurate field surveys might
be to piggyback sleeping sickness diagnostics on to national programmes
set up to deal with, for example, AIDS. Field samples from surveys would
be placed on FTA®cards, which could then be sent to a central laboratory,
analysed by PCR and the results sent by SMS (as mobile phones are now
readily available in Africa) to field personnel who could proceed with the
appropriate treatment within a few days. Checchi et al. (2008b) suggest
that even a small proportion of ‘silent or chronic carriers’ would decrease
the chances of repeated active case detection campaigns interrupting
transmission; accurate diagnostics, using PCR, would answer the ques-
tion of ‘chronic carriers’ and also ensure that people would not be need-
lessly treated with toxic drugs. To address the problem of ‘silent carriers’,
all admissions to health centres within sleeping sickness endemic foci
should be tested by PCR for trypanosomes – especially newborn infants

(Oba et al., 2011). Problems of under-reporting and accuracy of diagnosis
would also succumb to large-scale, accurate diagnostics, using PCR.
Elimination of T. b. gambiense sleeping sickness remains the stated
ambition of WHO and the necessary prerequisites to achieve this aim have
been outlined by Simarro et al. (2008); much of this turns around infra-
structure and training of NSSCPs which, as NGO inputs have declined,
are responsible once again for national programmes. However, there is the
vexed question of whether elimination of T. b. gambiense sleeping sickness
requires elimination of the tsetse vector of whether active case finding will
achieve this end. There is now quite strong evidence that active case find-
ing is sufficient – where there is no significant animal reservoir to deal
with – and we shall see over the coming years whether this is so. Elimina-
tion will not be achieved without vast improvements in field diagnostics –
what is needed is a simple and reliable test that give a simple yes/no
answer for infection with T. b. gambiense. Given the profusion of putative
molecular tests but lack of application, we should bear in mind Voltaire’s
warning ‘Le mieux est l’ennemi du bien’ (the perfect is the enemy of the
good) or perhaps in more modern terms: ‘done is better than perfect’. We
are left with the – very researchable – question: what level of surveillance
(and at what cost) needs to be maintained to achieve elimination?
Diagnostics are not such a problem in relation to T. b. rhodesiense sleep-
ing sickness, as simple microscopy is usually sufficient (Radwanska, 2010).
However, the level of under-reporting of this disease suggests that current
approaches are insufficient. Mass screening in known hotspots (preferably
by PCR) to deal with the problem of under-reporting would be a desirable
aim and could be handled on a national scale in the endemic countries;
again, piggyback sleeping sickness on national programmes put in place
for other diseases – though we are well aware that this approach pres-
ents difficulties both political and logistical. As with T. b. gambiense sleep-
ing sickness, the search for non-toxic drugs for stage II treatment should
remain a research priority.
All approaches to controlling T. b. rhodesiense sleeping sickness revolve
around a significant animal reservoir. This means interrupting the fly–
animal–human cycle and in practice some form of tsetse control must be
involved. Tsetse populations are, however, extremely resilient; as few as a
dozen female flies, with enough males for insemination, will ensure that
the population will not be eliminated without further control efforts. Har-
grove (2005) has shown that it is necessary to either (i) kill all of the flies in
the initial onslaught using, for instance, protracted ground or aerial spray-
ing operations or (ii) maintain an adult mortality of at least 3.5% per day,
using techniques such as odour-baited targets or insecticide-treated cattle,
until sampling confirms elimination. The use of insecticide-treated cattle
is not a panacea for tsetse control; obviously, this approach is of no use
where there are either no cattle or only patchy distribution of insecticide-

treated cattle (Hargrove et al., 2002). Nonetheless, where tsetse and try-
panosomiasis are a problem, cattle are usually present and the restricted
application of insecticide is the most promising technique (Torr et al.,
2007). Moreover, concurrent treatments with trypanocides offer animal
health benefits unrelated to sleeping sickness, presenting an inducement
to farmers to treat their animals. Most importantly, it has been calculated
that treating livestock to control T. b. rhodesiense sleeping sickness, the cost
per DALY averted can actually be negative because treating cattle will
increase income from livestock and the trypanocidal drugs used on cattle
will also remove the animal reservoir of disease (Shaw, 2004).
The use of insecticide-treated cattle to control tsetse has been a game-
changing innovation as it puts disease control into the hands of farmers
themselves; tsetse control is no longer the sole preserve of government-
or donor-funded, large-scale, operations using costly technology such as
aerial spraying but can be in the hands of smaller scale private or pub-
lic/private enterprises and is therefore far more likely to be sustainable
(Torr et al., 2007). Restricted application technology has brought tsetse
control within the reach of poor farmers in Africa at a cost of around 2
cents US/animal/treatment. This approach can also be used to control
sleeping sickness; a Public Private Partnership (The Stamp Out Sleeping
Sickness campaign: http://www.stampoutsleepingsickness.com/) was
formed (Kabasa, 2007) in response to an emergency situation arising in a
number of districts in Northern Uganda to control the northward spread
of T. b. rhodesiense sleeping sickness (Picozzi et al., 2005). By promoting
the restricted application technique combined with trypanocidal drugs
to control sleeping sickness, this partnership has also improved veteri-
nary services in a very deprived area of Uganda and provided livelihood
opportunities for young veterinarians (Waiswa and Kabasa, 2010). The
long-term success of this independent approach to sleeping sickness con-
trol will depend on farmers getting involved and it is in everyone’s inter-
est to attend to farmers’ attitudes (Morton, 2010; Bouyer et al., 2011). The
privatisation of sleeping sickness control would have been unthinkable a
decade ago, but with the introduction of insecticide-treated cattle, this is
now a viable option and could be expanded by equally innovative fund-
ing options, for example, public–private partnerships, social investment
bonds, etc.
We have been here before – we recognise inter-epidemic periods; we
know that sleeping sickness is extremely resilient and can, in changing cir-
cumstances, come back to shock us in the most aggressive fashion. There
were major outbreaks in the twentieth century across Africa, which provide
good evidence of this. We are now in a position to take advantage of the pres-
ent lull in prevalence and continue with what the French rightly describe as
la lutte (struggle) (Simarro et al., 1991). Before we casually consider disease
elimination, we should recall that strategies to bring this about will now be
planned and paid for increasingly by the endemic countries themselves. We
have seen this reflected in the decline of NGO involvement as local health
services resume surveillance (Simarro et al., 2011a). To apply ‘the last strike
to the dying beast’ will be difficult when relying on overloaded and weak
national health services (Simarro et al., 2011b). However, we should ques-
tion the underlying assumption that sleeping sickness control must always
be a public good with attendant fiscal frailties. As we have seen in Uganda,
animal health suppliers, not reliant on the public purse, are involved in the
control of T. b. rhodesiense sleeping sickness using innovative methods of
funding through a public–private partnership. It is generally assumed that
the control and elimination of T. b. gambiense sleeping sickness will always
be a public good as appropriate strategies depend on local health service
for surveillance and treatment, but there is no need to think that this must
always be so. One approach could be the use of social impact bonds (SIBs),
also referred to as ‘Pay For Success’ contracts (for examples of SIBs, go to http:
//www.socialfinance.org.uk/), to finance sleeping sickness control opera-
tions. Rather than resting on our laurels, we suggest that this is precisely
the time to take up the tools available, invest in new tools (including novel
financial instruments) where necessary, struggle against sleeping sickness
with more – not less – vigour and ensure that we eliminate this disease from
Africa.
ACKNOWLEDGEMENTS
We are grateful for the support of the UK Department for International Development through
their Research into Use Programme and the EU FP7 Integrated Control of Neglected Zoo-
noses programme. The views expressed here are the authors’ own and not necessarily those
of the donors. We would also like to thank Mark Carrington, Paul Coleman, John Hargrove,
Elliot Krafsur and Steven Torr for their helpful advice.
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CHAPTER 5
Scabies: Important Clinical
Consequences Explained by
New Molecular Studies
Katja Fischer*, Deborah Holt†, Bart Currie† and
David Kemp*

5.2. Biology/Clinical Aspects 342
5.2.1. Lifecycle and transmission 342
5.2.2. Clinical presentation 342
5.2.3. Diagnosis 343
5.2.4. Interaction of scabies mites with the host epidermis 344
5.3. Current Strategies to Control Scabies are Inadequate 346
5.4. Tools to Facilitate Research on Scabies 348
5.4.1. A large scabies mite EST database as a valuable
resource of molecular data 349
5.4.2. A porcine system as a model for in vivo studies 351
5.5. Scabies Mite Intestinal Proteins as Targets to Develop
Alternative Therapeutic Intervention 353
5.6. Sar s 3, an Intestinal Scabies Mite Serine Protease
Digesting Epidermal Protein 354
5.7. SsAP, an Aspartic Protease of Scabies Mites 357
5.8. Inactivated Scabies Mite Serine Protease Paralogues
(SMIPP-Ss) Interfere with Human Complement 358
5.9. A Scabies Mite Peritrophin is a Potential Target of Host
Complement 362
5.10. Complement Inhibition by Scabies Mites Promotes
Streptococcal Growth in vitro 364
5.11. Conclusion 365
References 366
* Queensland Institute of Medical Research, Herston

† Menzies School of Health Research, Herston.

339
340 Katja Fischer et al.
Abstract In 2004, we reviewed the status of disease caused by the scabies

mite Sarcoptes scabiei at the time and pointed out that very little
basic research had ever been done. The reason for this was largely
the lack of availability of mites for experimental purposes and, to
a degree, a consequent lack of understanding of its importance,
resulting in the trivial name ‘itch mite’. Scabies is responsible for
major morbidity in disadvantaged communities and immunocom-
promised patients worldwide. In addition to the physical discom-
fort caused by the disease, scabies infestations facilitate infection
by bacterial pathogens such as Streptococcus pyogenes and Sta-
phylococcus aureus via skin lesions, resulting in severe downstream
disease such as in a high prevalence of rheumatic fever/heart dis-
ease in affected communities. We now have further evidence that
in disadvantaged populations living in tropical climates, scabies
rather than ‘Strep throat’ is an important source of S. pyogenes
causing rheumatic fever and eventually rheumatic heart disease. In
addition, our work has resulted in two fundamental research tools
that facilitate much of the current biomedical research efforts on
scabies, namely a public database containing ~45,000 scabies mite
expressed sequence tags and a porcine in vivo model. Here we will
discuss novel and unexpected proteins encountered in the data-
base that appear crucial to mite survival with regard to digestion
and evasion of host defence. The mode(s) of action of some of
these have been at least partially revealed. Further, newly discov-
ered molecules that may well have a similar role, such as a family
of inactivated cysteine proteases, are yet to be investigated. Hence,
there are now whole families of potential targets for chemical in-
hibitors of S. scabiei. These efforts put today’s scabies research in a
unique position to design and test small molecules that may spe-
cifically interfere with mite-derived molecules, such as digestive
proteases and mite complement inhibitors. The porcine scabies
model will be available to trial in vivo treatment with potential
inhibitors. New therapies for scabies may be developed from these
studies and may contribute to reduce the spread of scabies and the
subsequent prevalence of bacterial skin infections and their devas-
tating sequelae in the community.
5.1. INTRODUCTION
Scabies, caused by the ectoparasitic mite Sarcoptes scabiei, has been recog-
nised as a disease of the skin for at least 3000 years (Burgess, 1994). It is
commonly known by the trivial name the ‘itch mite’. However, infestation
with the ‘itch mite’ can be far from trivial and studies of the molecular
biology of the mite, which have only recently become possible, have
started to shed light on mechanisms that underlie this.
Scabies: Important Clinical Consequences Explained by New Molecular Studies 341
Scabies is common among many different species of animals, with

over 100 known mammalian hosts (Bornstein, 2001). It was considered
likely that zoonotic transmission to humans could be a common mode
of spread of the infestation (reviewed in Walton et al., 2004c) and the
possibility that dogs were a source of infestation in disadvantaged com-
munities in Australia was studied in depth (Walton et al., 1997, Walton
et al., 1999). This study employed a number of microsatellites and con-
vincingly demonstrated that mites from the same hosts were genetically
more similar to each other than mites from different hosts, regardless of
their geographical origin. Specifically, scabies mites from a human in Aus-
tralia were more similar to mites from humans in Panama than to mites
from a dog within the same house. The study was subsequently extended
and confirmed using further microsatellites as well as mitochondrial DNA
sequences with similar results (Walton et al., 2004b). In conjunction with
small complementary DNA (cDNA) libraries constructed using messen-
ger RNA from S. scabiei var. vulpes (Mattsson et al., 2001; Ljunggren et al.,
2003) and var. hominis (Harumal et al., 2003), this work clearly delineated
the start of systematic genome-based work on scabies mites.
Organisms that have been much more widely studied than S. scabiei
are the house dust mites Dermatophagoides pteronyssinus, Dermatophagoides
farinae and Euroglyphus maynei. These mites are non-parasitic; however,
their diet is largely dead skin flakes shed by animals including humans
and as such have a similar source of nutrition to scabies mites. However,
they have been studied to a considerably greater extent than scabies mites
due to their role as important causes of asthma. Consequently, the ques-
tion of whether homologues of house dust mite allergens occur in scabies
mites provided one possible start point in the examination of expressed
sequence tags (ESTs) generated from the cDNA libraries; indeed, homo-
logues of most house dust mite allergens were present. To enable further
comparison, we also generated a relatively small EST data set from D.
pteronyssinus. These presented some fascinating similarities and, in some
cases, differences. The differences reveal critical unexpected aspects that
may well underlie the successful host–parasite relationship.
In this review, we will first discuss aspects of the biology of scabies
coming from a wealth of clinical studies that convince us that the term
‘itch mite’ trivialises an important disease. Together with this, we will
also describe some advances in experimental methodology that should be
advantageous in future studies. We will then devote most of this review
to describing specific molecules many of which appear to be the homo-
logues of house dust mite allergens, and in particular molecules that have
diverged in sequence and function from them, apparently acquiring some
quite novel functions during this process. It is this latter set of molecules
that puts scabies mites into an entirely new and unexpected perspective.
5.2. BIOLOGY/CLINICAL ASPECTS
5.2.1. Lifecycle and transmission

The scabies mite S. scabiei is a member of the class Arachnida, subclass Acari,
order Astigmata and family Sarcoptidae. Scabies mites are obligate para-
sites that burrow into the skin of their host, reproducing and laying eggs in
the burrows. Adult female mites are approximately 0.2–0.5 mm long and
0.2–0.4 mm wide with adult male mites about two-thirds of the size of the
female mites (Arlian, 1989). Adult female mites burrow into the upper
epidermis of the host at the rate of approximately 0.5–5 mm per day lay-
ing one to three eggs per day. The eggs hatch out into six-legged larvae,
then moult progressively into eight-legged protonymphs, tritonymphs
and then adult males and females. The process from egg to adult takes
approximately 14 days, while the average life span of the mites is around
30–60 days (Alexander, 1984).
Transmission of scabies mites between hosts is largely via direct skin
contact, while there is conflicting evidence regarding the role of fomites.
Early human experimentation indicated that fomites were not likely to
contribute significantly to transmission, with only two cases of scabies
recorded in volunteers from 63 experiments involving exposure to the
bedding or clothing of infested patients (Mellanby, 1941). However, it was
noted that blankets were considered by some at the time as the chief means
of transmission, particularly in the Army (Mellanby, 1941). Further human
experimentation resulted in only four cases of scabies from 272 volunteers
who got into warm beds recently vacated by infested patients (Mellanby,
1944). Scabies mites have greatest survival away from a host in conditions
of low temperature and high relative humidity. Mites have been shown
to remain infective after up to 36h away from the host at 22–24°C and
40–80% relative humidity, with the time taken for subsequent penetration
into the skin as a function of the time off the host (Arlian et al., 1984a,
Arlian et al., 1989). Female tritonymphs have been reported to survive
as long as 19 days at 10°C and 97% relative humidity (Arlian et al., 1989).
This survival coupled with the recovery of live mites from the homes of
scabies cases (Arlian et al., 1988) indicates that fomites may have a role
in transmission. It is likely that direct skin contact is the most important
mode of transmission in cases of ordinary scabies, while fomites may also
play a role in transmission from crusted scabies cases, in which extremely
high numbers of mites are present (Section 5.2.2).
5.2.2. Clinical presentation
Two major forms of scabies are recognised. In most cases, infestation results
in ordinary scabies in which the mite burden is low (approximately 10–15
mites). Severe itching and prutitic, erythematous, papular and vesicular
lesions are often associated with the burrowing mites. In addition, a more
generalised rash may also appear on other areas of the body which appear
unrelated to mite activity and may result from an allergic sensitivity or
auto-sensitisation reaction due to cell-mediated or circulating immune
complexes (reviewed in Arlian, 1989). The most common sites of mite bur-
rows are the webs of the fingers, the volar aspect of the wrists and arms
and the extensor of the elbows. Less common areas of infestation include
the soles of the feet, the buttocks and genitals and the area surrounding
the nipples (Mellanby, 1977b, Alexander, 1984).
The symptoms of scabies infestation are reported to take 4–8 weeks
to develop (Mellanby, 1977a) consistent with a delayed hypersensitivity
reaction. Thus, infested individuals may be contagious for a considerable
period before a diagnosis is made. A reaction occurs much more quickly
with subsequent infestations with symptoms generally appearing in
24–48 h, and spontaneous recovery from these subsequent infestations can
occur. Experimental re-infestation was only successful in 40% of patients
who had been previously infested (Mellanby, 1944). There is evidence
that this observed protection is due to a Th1 cell-mediated response (Lalli
et al., 2004, Roberts et al., 2005, Walton et al., 2008).
A severe and debilitating form of the disease known as crusted sca-
bies can also occur in which extremely large numbers of mites are present.
Patients characteristically develop hyperkeratotic skin crusts that often
involve extensive areas of the skin. Thousands of mites per gram of skin
have been reported in crusted scabies cases (Currie et al., 1995), and as
such, these patients are extremely infectious. Crusted scabies is caused by
the same variety of mites that causes ordinary scabies and progression to
this form of the disease is uncommon. Crusted scabies can be associated
with underling immunodeficiency; however, cases in immunocompe-
tent individuals are also seen (reviewed in Walton et al., 2004c). Cluster-
ing within families indicates that genetic predisposition may be a factor
in some cases (Roberts et al., 2005). Crusted scabies patients have been
shown to have extremely high levels of total immunoglobulin (Ig) E and
IgG and a skewed Th2 response to infestation (reviewed in Walton, 2010).
5.2.3. Diagnosis
Scabies can be a difficult disease to diagnose as the clinical presentation
can mimic that of other skin conditions including dermatitis, eczema,
impetigo and the allergic reaction to other organisms such as lice, fleas
and bedbugs (Alexander, 1984). The identification of mite burrows in the
host epidermis is often used for diagnosis; however, burrows can be scarce
and difficult to locate on many patients with the unaided eye. Definitive
diagnosis of scabies infestation can be made by the microscopic identifi-
cation of mites, eggs or faecal pellets in scrapings of skin from suspected
cases. The sensitivity of this technique is also low, particularly in cases of

ordinary scabies in which the mite burden is low. As a result, diagnosis
is often made purely on a clinical and epidemiological basis (Walton and
Currie, 2007).
Immunodiagnostic tests for the diagnosis of scabies in animals have
been developed using whole mite extract from dog mites (var. canis) or pig
mites (var. suis) and evaluated for use in the diagnosis of scabies in animals
including dogs (Bornstein et al., 1996, Curtis, 2001, Lower et al., 2001), foxes
(Bornstein et al., 1995) and pigs (Bornstein and Wallgreen, 1997, Hollanders
et al., 1997, Jacobson et al., 1999, Van Der Heijden et al., 2000). Little work
has been done to assess the usefulness of these enzyme-linked immuno-
sorbent assays (ELISAs) for the diagnosis of scabies in humans. A serologi-
cal survey of indigenous people in peninsula Malaysia showed that 25%
produced a positive polyvalent response to the var. canis antigen, much
higher than the <1% who demonstrated clinical symptoms, leading to the
suggestion that continuous exposure to dog scabies mites was providing
cross-protection against scabies in humans (Normaznah et al., 1996). A var.
vulpes whole mite extract ELISA showed only 48% sensitivity for diagnosis
in humans, compared to 80% in pigs and 84% in dogs (Haas et al., 2005). An
ELISA based on whole mite extract of var. hominis mites would be extremely
difficult to develop due to the lack of an in vitro culture system and thus a
reliance on mites from human patients as the source of antigen. Recently,
ELISAs have been developed using recombinant S. scabiei var. hominis anti-
gens. An ELISA based on part of a glycine-rich protein was shown to have
100% sensitivity and 97% specificity in both chamois and deer (Casais et al.,
2007) but was not evaluated for diagnosis in humans. Several other var.
hominis molecules have been shown to be recognised by sera from infested
humans (Walton et al., 2010), with an apolipoprotein showing particular
promise as a serodiganostic antigen in humans ( Jayaraj et al., 2011).
5.2.4. Interaction of scabies mites with the host epidermis

Scabies mites burrow into the human epidermis and are widely thought
to reside in the lower stratum corneum with their gnathosoma embed-
ded into deeper layers of the epidermis (Alexander, 1984; Christopherson,
1986) (Fig. 5.1). Recent work has also provided evidence of the presence
of scabies mites in the stratum granulosum (Levi et al., 2011). Studies sug-
gest that fluid from deeper epidermal layers seep into the mite burrows
providing a source of nutrition and water to the mites. This also allows
soluble mite antigens from saliva, faeces and other body secretions to dif-
fuse into the dermis and stimulate an immune and inflammatory response
by the host (Arlian, 1989). This promotes the diffusion and deposition of
complement C3 and circulating antibodies in the dermoepidermal junc-
tion, in the vicinity of the mites (Frentz et al., 1977, Hoefling and Schroeter,
FIGURE 5.1 A female scabies mite burrowing in the upper epidermis. Coloured arrows
indicate key mechanisms in scabies and associated bacterial skin infections: : Scabies
mite defence in form of gut and faecal proteins. : Host response (immunoglobulins,
complement, coagulation factors, host proteases). : Bacteria entering the skin. (For
1980, Salo et al., 1982). IgG (Rapp et al., 2006, Willis et al., 2006), IgE
(Walton et al., 2010), C1q (Bergstrom et al., 2009) and C9 (Mika et al., 2011)
have all been localised to the gut of scabies mites in human skin.
Studies using whole scabies mite extract have demonstrated that
S. scabiei are able to influence inflammatory and immune responses by host
cells including keratinocytes, fibroblasts, peripheral blood mononuclear
cells and dendritic cells (Arlian et al., 2003, Arlian et al., 2004, Arlian et al.,
2006, Elder et al., 2006). These studies showed that thus far uncharacter-
ised components of the mite extract favour mite infestation by depressing
the initiation of inflammatory processes and potentially contributing to
the delayed immune response seen clinically. Studies using four S. scabiei
recombinant antigens with homology to well characterised house dust mite
antigens showed increased expression of the Th2 cytokines Interleukin-5
and Interleukin-13 and decreased expression of the Th1 cytokine Interferon-
gamma in crusted scabies patients compared to ordinary scabies patients,
in response to a recombinant S. scabiei cysteine protease (Walton, 2010). The
specific mechanisms of the interaction between scabies mite molecules and

their hosts have only recently begun to be investigated (5, Sections 5.5–5.10).
The secondary infection of scabies lesions with bacteria is very com-
mon. In remote indigenous communities in the Northern Territory of
Australia, infection with group A Streptococcus is the commonest cause
of pyoderma and scabies is thought to underlie 50–70% of these infec-
tions (Van Buynder et al., 1992). The significant sequelae of skin infection
with group A Streptococcus include acute post-streptococcal glomeru-
lonephritis, acute rheumatic fever and rheumatic heart disease, which
occur in extremely high rates in many remote indigenous communities
in Australia (Currie and Carapetis, 2000). Scabies control programs have
demonstrated a reduction in the rate and severity of pyoderma as a result
of community-wide scabies treatment, in the absence of antibiotic treat-
ment (Carapetis et al., 1997, Wong et al., 2001, Lawrence et al., 2005). This
indicates that scabies mite burrows provide a favourable environment for
the growth of these bacteria, and the secretion and excretion of mite prod-
ucts into the burrow are likely to play a role in this. One possible mecha-
nism for this has now been elucidated in which scabies mite-inactivated
proteases interfere with complement activation thus providing a favour-
able environment for the growth of group A Streptococcus (Section 5.10).
5.3. CURRENT STRATEGIES TO CONTROL

SCABIES ARE INADEQUATE
Many therapies have been used for the treatment of scabies; however,
some have lost favour due to limited efficacy or unpleasant side-effects
including neurotoxicity or severe skin irritation (reviewed in Mounsey
et al., 2008). The current first-line therapeutic agents for the treatment of
scabies are broad spectrum agents that kill arthropods via interfering with
the nervous system or muscle function. Permethrin is the treatment of
choice in many areas and is used as a 5% cream that is applied all over the
body from the neck down. However, permethrin is generally not recom-
mended for children under 2 months of age where crotamiton is usually
preferred (Ewald, 2010), despite evidence indicating that the clinical effi-
cacy of crotamiton may be low (Taplin et al., 1990, Amer and El-Gharib,
1992). Oral ivermectin has been shown to be an effective treatment for
scabies and is used in many endemic areas, including remote indigenous
communities in northern Australia, for the treatment of crusted scabies
(Currie et al., 1995, Huffam and Currie, 1998). However, due to a lack of
safety data, ivermectin is currently not used in pregnant women and chil-
dren under 15kg, the latter of which are a major target group in many
community-based control programs. The roles of permethrin and iver-
mectin in treatment of cases of ordinary and crusted scabies and their
contacts were recently summarised (Currie and McCarthy, 2010).
A number of community control programs have been undertaken,

with mixed success. One program conducted in a remote indigenous
community in the Northern Territory of Australia used a combination of
annual mass community treatment with topical permethrin, coupled with
public health education and environmental initiatives (Wong et al., 2001).
The prevalence of scabies was shown to be reduced 15 months after the
intervention (Wong et al., 2002). Similarly a program of active screening
and treatment with topical permethrin reduced the prevalence of scabies
from 29% to less than 10% over 2 years in another remote indigenous com-
munity (Carapetis et al., 1997). However, a subsequent program monitor-
ing prevalence rates over 3 years showed that despite a drop in the rate
of infected scabies from 3.7% to 1.5%, no change in the overall prevalence
of scabies was achieved (Andrews et al. 2009). The limited sustainability of
this intervention may have been confounded by the low initial prevalence
observed (16%), the reintroduction of scabies through population mobil-
ity, poor compliance with the unsupervised treatment and the possibility
of emerging drug resistance. Supervised treatment with oral ivermectin
may be a suitable alternative to topical permethrin for such programs and
has been successfully used for a mass community treatment program in
the Solomon Islands (Lawrence et al., 2005). The 3-year program showed
a reduction in scabies from 25% to less than 1%. A similar approach is now
being trialled in a remote indigenous community in Australia, driven by
a community desire to reduce the disease burden due to both scabies and
strongyloidiasis (Kearns et al., 2009).
Emerging resistance of scabies mites to current treatments is of growing
concern. In vitro resistance of scabies mites (Currie et al., 2004, Mounsey
et al., 2009) as well as clinical treatment failure of scabies in humans
(Currie et al., 2004, Van Den Hoek et al., 2008) and dogs (Terada et al.,
2010) has now been reported for ivermectin. A pH-gated chloride channel
that is likely the primary target of ivermectin and a P-glycoprotein that
may also play a role in the development of resistance have been identified
in scabies mites (Mounsey et al., 2006, Mounsey et al., 2007). This evidence
of increasing tolerance raises concerns as to the sustainability of the use
of ivermectin for the treatment of severe crusted scabies in endemic areas
and for community-based control programs. Likewise, increasing in vitro
tolerance of scabies mites to permethrin has also been reported (Walton
et al., 2000). A single nucleotide polymorphism was identified in perme-
thrin-tolerant scabies mites in a region of the voltage-sensitive sodium
channel gene where mutations have been shown to result in pyrethroid
resistance in a number of other arthropods (Pasay et al., 2008). In addi-
tion, a significant increase in the expression of glutathione S-transferase
genes has been shown in permethrin-tolerant human scabies mites and
permethrin-resistant dog scabies mites (Mounsey et al., 2010b).
A number of alternative treatments for scabies have been proposed
including tea tree oil (Walton et al., 2004d), aloe vera (Oyelami et al., 2009)
and eugenol-based compounds (Pasay et al., 2010). However, in the face

of this emerging resistance of scabies mites to ivermectin and permethrin,
there is an urgent need to develop specific therapies for the treatment of
scabies. This requires a more detailed understanding of mite biology and
of specific host–parasite interactions.
5.4. TOOLS TO FACILITATE RESEARCH ON SCABIES
Two fundamental research tools have facilitated much of the current bio-
medical research efforts on scabies, namely a large EST data set and an
in vivo model (Fig. 5.2).
FIGURE 5.2 Conceptual framework outlining the project aims of our research. SM
(scabies mite), HDM (house dust mite).
5.4.1. A large scabies mite EST database as a valuable resource of

molecular data
Until 2000, the scarcity of molecular data on scabies was largely due to
the difficulty in obtaining mites. The majority of scabies cases have low
parasite burdens that do not provide sufficient material for most labora-
tory work, and an in vitro culture system or a tractable animal model did
not exist. An EST data set of approximately 1000 sequences was generated
from cDNA extracted from scabies mites of the red fox and a number of
molecules were identified including a homologue of the house dust mite
allergen paramyosin (Mattsson et al., 2001, Ljunggren et al., 2003).
Subsequently, cDNA libraries using mites available from the bedding
of a crusted scabies patient were generated. These libraries were of suf-
ficient quality for a major sequencing project (Fischer et al., 2003a, Fischer
et al., 2003b, Harumal et al., 2003) resulting in a data set of over 40,000 STs.
Analysis of this EST data set has had a considerable impact, providing for
the first time a substantial amount of molecular data on this parasite and
securing a solid base for recombinant biology. It has facilitated the explo-
ration of an increasing number of scabies mite proteins that may be novel
targets to develop alternative therapeutics.
To further explore the biology of the scabies mite, our group is work-
ing towards establishing the genome sequence of S. scabiei. Attempts to
estimate the S. scabiei genome size accurately using flow cytometry have
been hampered by the small numbers of cells that could be isolated as
single cells from egg or whole-body preparations. The small size of scabies
mites of 0.2–0.5mm does not allow tissue dissections and thus it is difficult
to obtain homogenous cell preparations. Similar difficulties were reported
in Metaseiulus occidentalis, where flow cytometry failed to resolve genome
size, with estimates ranging from 35 to 160Mbp, depending on the age
of the eggs used (Jeyaprakash and Hoy, 2009). An alternative approach
utilising quantitative PCR (qPCR) was suggested to be particularly use-
ful for organisms where the genome size is expected to be small and the
availability of genetic material is limited (Jeyaprakash and Hoy, 2009).
Based on the method of Wilhelm et al. (2003), this method has proven
reliable for a number of species, including Saccharomyces cerevisiae, Xiphor-
phours maculaus, Homo sapiens (Wilhelm et al., 2003), Musca domestica and
Drosophila melanogaster (Gao and Scott, 2006). Very recently, qPCR was used
to estimate the genome size of S. scabiei, Psoroptes ovis and D. pteronyssinus,
which were calculated as approximately 100, 86 and 150Mbp (females)
or 220Mbp (males), respectively (Mounsey et al., 2012). The estimate of
100Mbp for S. scabiei is consistent with other evidence suggesting a small
genome size, including that the nuclei are very small in comparison to
nuclei from mosquito cell lines, and the average size of introns identified
TABLE 5.1 Novel S. scabiei gut excretory proteins identified from EST database
350
Name Protein family Function Targeted host proteins Reference
Sar s 3 Catalytically active serine Cleaves ingested skin Filaggrin (Beckham et al., 2009)
Katja Fischer et al.

protease proteins
SsAP Aspartic protease Cleaves ingested Haemoglobin, serum Unpublished
plasma proteins albumin, fibrinogen and
fibronectin
SMIPPS-I1 Inhibit lectin, c lassical Bergstrom et al. (2009)
SMIPPS-D1 and a lternative
Catalytically inactive serine pathways of C1q, mannan-binding lectin
SMIPPS-B2
proteases (>33 identified) complement (MBL), properdin
SMIPPS-G2 Mika et al. (in review)
SMIPPS-G4 activation
SMSB3 Inhibit lectin, classical C2, C8, Factor D Mika et al. (in review)
Serpins (six identified)
SMSB4 and alternative path- C1, C2, C3, C4, Factor B,
ways of complement Factor D, properdin
activation
SsPTP1 Peritrophin (one of several Inhibits lectin pathway MBL Mika et al. (in press)
identified) of complement
activation
Sar s 1c Catalytically active cysteine Cleaves complement C3 and C5 Holt et al. (2004)
protease (one of five components
identified)
SMIPPC 1-5 Multiple catalytically inac- Not defined Not defined Holt et al. (2004)
tive cysteine proteases
GST Glutathione S-transferase Play role in pesticide None Molin and Mattsson (2008)
(six identified) detoxification and Mounsey et al. (2010b)
is 140bp. This small genome size puts S. scabiei at the lower end within the
Acari, where genome size ranges from 2671Mbp (approximately 2.73pg)
for the Ixodidae (Geraci et al., 2007) to about 90Mbp for the two-spotted
spider mite Tetranychus urticae (Hanrahan and Johnston, 2011) and the
phytoseiid mite M. occidentalis (Jeyaprakash and Hoy, 2009). These estima-
tions provide an encouraging starting point for future genome sequencing
efforts.
5.4.2. A porcine system as a model for in vivo studies

Scabies is a highly host-specific parasite (Walton et al., 2004a), pro-
ducing only a transient, self-limiting reaction in its non-preferred
host (Orkin, 1985). To date no method has been established to main-
tain viable, propagating mites separated from the host for longer than
48hs. A trans-species animal model (dog mites on rabbits) (Arlian et al.,
1984b) has been useful for initial studies, and valuable insights into the
immunopathogenesis of scabies have been gained by utilising S. scabiei
var. canis whole mite antigen extracts in studies in rabbits, mice and
humans (Arlian et al., 1996, Arlian et al., 2003, Arlian et al., 2006). How-
ever, this is a mismatched host–parasite system and there are difficulties
in transfer between laboratories. Hence, it was essential to investigate
other possible models. Several mouse/group A Streptococcus models
are available including a human xenograft mouse model for pyoderma
(Scaramuzzino et al., 2000). Extensive trials to experimentally infest
multiple mouse breeds with scabies mites from humans, pigs and dogs
were undertaken; however, an infection with scabies mites could not
be established even in immune-deficient Rag1−/− mice crossed with
Dystrophin-deficient mdx mice, which lack the ability to groom. Pigs
on the other hand naturally develop a manifestation of scabies closely
resembling human crusted scabies (Van Neste and Staquet, 1986). An
experimental pig model has recently been developed (Mounsey et al.,
2010a). High mite numbers (>6000 mites/gskin) and prolonged infesta-
tion times (6–12 months) are achieved by treatment with the immune-
suppressor dexamethasone, which promotes infection by depressing
lymphocyte and antibody production and inflammation. Only mild,
controlled side-effects of the dexamethosone treatment were observed.
Moreover, in most recent experimental groups, some of the pigs devel-
oped crusted scabies in the absence of immunosuppression, if the ini-
tial mite load used for infection was high (unpublished data). This
observation reinforces the relevance of the porcine model to explore
the pathogenesis of crusted scabies. Most importantly, porcine innate
immunity is very comparable to that in humans. The experimental
progress in the development of the pig model of scabies is summarised
in Table 5.2.
TABLE 5.2 Development of an animal model for scabies, 2004–2009
Duration of
Number Source of Dexamethasone Mites per infection
Year of pigs infection treatment 4 cm2 skin (weeks)
2004 1 Natural None 0 0

2004 5 Natural None 19 8
2004 4 Natural 0.01mg/kg, 50 10
injection,
1 per week
2006 4 Natural 0.01 mg/kg, 150 12
injection,
3 per week
2006 3 Passaged Pretreated, 300 12 (60)
0.1 mg/kg,
injection,
3 per week
2007 4 Passaged and Pretreated, 500 40*
boosted 0.1 mg/kg,
oral, 3 per
week-daily
2007 3 Passaged and Pretreated, >1000 52*
boosted 0.1 mg/kg, oral,
daily
2008 3 Passaged and Pretreated, >10,000 20*
boosted 0.25–0.3 mg/kg,
oral, daily
2009 2 Boosted Pretreated, 100,000 44*
0.2 mg/kg,
oral, daily
2009 3 Passaged and Pretreated, 100,000 14*
boosted 0.2 mg/kg,
oral, daily
The pig appears to be an ideal host to model human scabies infesta-

tion. Apart from the obvious requirement of the parasite propagating to
high numbers in the crusted condition, another genuine advantage of this
model are the outstanding anatomical, physiological, biochemical and
immunological similarities between human and pig skin, which are only
exceeded by non-human primates. The relative thickness and structure of
the dermal and epidermal layers, epithelial regeneration time, the physi-
ology of wound healing, the vasculature and many important biochemi-
cal parameters are very similar between pigs and humans (Sullivan et al.,
2001, Hollander et al., 2003, Steinstraesser et al., 2006). Most antibodies
against human epidermal markers cross-react against porcine antigens
(Vodicka et al., 2005) and human and porcine complement factors func-
tionally interact in vitro (Salvesen and Mollnes, 2009) and in vivo (Jiang
et al., 2010). In contrast, many human and mouse complement factors are
not compatible (Kirschfink and Mollnes, 2003) and mite inhibitory pro-
teins evolved to inhibit human complement likely will not inhibit mouse
complement. Porcine experimental models are well recognised in many
areas (Vodicka et al., 2005), including research on wound repair (Sulli-
van et al., 2001), epidermal drug absorption (Simon and Maibach, 2000,
Cilurzo et al., 2007) and also on complement (Jiang et al., 2010), sepsis and
ischemia/reperfusion injury (Thorgersen et al., 2007). The porcine model
of scabies can be further utilised to advance understanding of the innate
and adaptive immune responses in scabies, by defining the temporal pro-
gression of immunopathologic responses in the mite infested skin. The
existing system likely has the potential to be extended into a pig/scabies/
pyoderma model that allows us to study the effects of mite molecules
within the epidermis on host system (e.g. local complement) and scabies-
associated pathogens. In addition, the in vivo model can be utilised to trial
novel therapeutics in a well-matched host system.
5.5. SCABIES MITE INTESTINAL PROTEINS AS TARGETS TO

DEVELOP ALTERNATIVE THERAPEUTIC INTERVENTION
As is the case for other parasites that ingest host serous material, the mite
gut is likely a vulnerable target. Burrowing scabies mites imbibe epider-
mal protein and plasma, which contain a multitude of diverse host prote-
ases, in particular of the coagulation and complement systems (Fig. 5.1).
There is now considerable data indicating that burrowing scabies mites
have indeed evolved an extensive repertoire of excretory gut proteins
(Holt et al., 2004, Beckham et al., 2009, Bergstrom et al., 2009, Mika et al.,
2011, Mika et al., in review). Figure 3 summarises the immunohistological
localisation in scabies mites of the proteins reviewed in Section 5.6–5.9.
In addition, the mite gut indeed contains ingested epidermal protein and
host plasma components. Some of these have a direct interaction with
mite intestinal proteins. The mite gut protease Sar s 3, for example, cleaves
specifically filaggrin, a major epidermal protein. This is described in detail
in Section 5.6. Mite molecules interfering with the host complement, as
described in Sections 5.8 and 5.9, co-localise with ingested host comple-
ment components. Neoepitope antibodies specific for the human SC5b-9
complex were used to detect membrane attack complex formation in his-
tological sections of scabies mite infested skin (Mika et al., 2011). Interest-
ingly, the levels of membrane attack complex detection did not exceed
background staining while the complement component C9 was strongly

detectable in the mite gut. Evidently, the combined anti-complement
mechanisms present in the mite gut seem to inhibit membrane attack com-
plex formation and thus may prevent complement-mediated gut damage.
It is clear from these localisation studies that essential mite proteins
exist within the mite gut and are also excreted from the gut with faeces
into the epidermis. We propose that an approach that involves inhibiting
the proteins the mite uses to protect itself from host defence as well as
the proteases involved in digestion may lead to the development of novel
therapeutic molecules. A substantial number of proteins are currently
under investigation (Table 5.1). Importantly, mite gut proteases seem to
play a major role in the host–parasite relationship.
5.6. SAR S 3, AN INTESTINAL SCABIES MITE SERINE PROTEASE

DIGESTING EPIDERMAL PROTEIN
Scabies mites reside for most of their lives in burrows they create in the epi-
dermis of its host’s skin to feed and to lay its eggs. While burrowing, mites
are thought to continually feed on constituents of the upmost layer of the
epidermis known as the stratum corneum or cornified envelope (CE). The
CE is formed by flattened dead-cell remnants to create a physical barrier
against the environment. At the molecular level, the CE is formed by pro-
teins, including filaggrin, loricrin, trichohyalin, involucrin, small proline-
rich proteins and keratin intermediate filaments. These components are
highly cross-linked by transglutaminases and an intricate set of insoluble
lipids thereby forming a semi-sealed barrier. The function of the CE is to
exclude foreign substances and harmful organisms, such as viruses, bacte-
ria, and fungi, and to prevent the loss of vital fluids. This system is contin-
uously regenerated by differentiating keratinocytes in a highly organised
process (reviewed in Candi et al., 2005, McGrath and Uitto, 2008).
When female scabies mites burrow into the superficial skin layers, they
move by mechanically disrupting the CE (Van Neste, 1985). Proteases would
be required to digest the ingested skin proteins and perhaps also might play
a role in degrading skin proteins outside of the mite (Fimiani et al., 1997).
Faeces are left behind as the mites tunnel through the epidermis, creating
linear lesions clinically recognised as burrows (Prins et al., 2004). We have
shown that the serine protease from the scabies mite Sar s 3 is localised in
the digestive tract of the mite and in faecal pellets by immunohistochemis-
try (Fig. 5.3). This localisation led to the question as to whether the enzyme
was involved in digesting skin proteins either within the mite or externally.
A recombinant form of the Sar s 3 serine protease was successfully expressed
in a yeast expression system (Beckham et al., 2009). The enzyme was puri-
fied and shown to be active in its mature form with the pro-peptide cleaved.
Data indicated that the pro-peptide of the enzyme is vital for formation of
FIGURE 5.3 Immunohistochemical staining demonstrated intestinal localisation

of mite and host target molecules. In human scabies mite infested skin sections,
antibodies against representatives for each protein family co-localised (in red) with
anti-human IgG antibodies, which were used to label the gut. Epidermal proteins and
components of the host complement were also detected in the gut while membrane
attack complex (MAC) was not detected with a neoepitope antibody. All mite gut
molecules tested to date are as well detected in the mite faeces within the epidermal
burrows (as exemplarily shown for SMIPP-S I1). Shown are sections (1) pre-immune serum,
(2) IgG, (3) SMIPP-S I1 localised to mite faeces, (4) serine protease Sar s 3, (5) aspartic
protease SsAP, (6) SMIPP-I1, (7) serpin B4, (8) peritrophin SsPTP1, (9) cysteine protease Sar
s 1c, (10) complement factor C9, (11) MAC and (12) human filaggrin. (For color version of
this figure, the reader is referred to the web version of this book.)
active enzyme and the current hypothesis is that in the mite the Sar s 3
proenzyme is cleaved by an unknown enzyme in the digestive tract to form
active, mature Sar s 3. The activity and specificity of Sar s 3 were determined
initially using various fluorogenic peptides. These results indicated that Sar
s 3 is trypsin like in its preference. This specificity was further investigated
using phage-displayed peptides, produced after six cycles of screening with

the phage display library. This generated a number of repeated sequences
containing a similar motif: Arg, followed by Ser or Ala, followed by Gly
or Ala. These sequences were further dissected using quenched fluorescent
substrates, followed by liquid chromatography–mass spectrometry. Scan-
ning the human proteome gave a considerable number of hits, but consid-
eration of these suggested four skin-specific proteins, keratin 1, filaggrin,
desmoplakin (isoforms 1 and 2) and envoplakin, as the most likely targets
because of their location within epidermis (Beckham et al., 2009).
Filaggrin was particularly noteworthy as it had multiple predicted
cleavage sites. Filaggrin is a key component of the CE. It is formed from
profilaggrin, a highly phosphorylated, histidine-rich, 500kDa polypeptide
consisting of 10–12 tandemly arranged 35-kDa filaggrin units. The filaggrin
matrix embeds keratin intermediate filaments and subsequently maintains
the epidermal texture (Candi et al., 2005). If there is a reduction or complete
absence of filaggrin, as occurs in heritable skin disorders such as atopic
dermatitis or ichthyosis vulgaris (Nomura et al., 2008), the skin barrier can
become permeable to external factors such as allergens or pathogens. The
precise cleavage of proteins such as filaggrin has been shown to be essen-
tial to proper formation of this vital protective layer (List et al., 2003). The
mechanical disruption and subsequent digestion of the filaggrin matrix by
the scabies mite would be predicted to have similar effects.
To determine whether Sar s 3 could directly degrade filaggrin, a recom-
binant fragment of human filaggrin containing six putative cleavage sites
was treated with the enzyme. While an active site titration method is yet
to be established, unambiguous cleavage was observed. We conclude that
filaggrin is one target of Sar s 3 digestion in the gut of the mite (Beckham
et al., 2009). Disruption of the structure of the filaggrin protein by the Sar
s 3 protease would be expected to substantially disrupt the CE, thereby
rendering patients susceptible to secondary infections, which is in fact the
case (Currie and Carapetis, 2000). Thus, the Sar s 3 protease has emerged
as an excellent candidate for the development of inhibitors to combat the
allergic symptoms engendered in patients infested with scabies mites, as
well as the associated secondary infections.
Sar s 3 is the closest homologue in our EST data set to the group 3 aller-
gens of house dust mites. Unexpectedly, we found a family of at least 33
scabies mite homologues of this sequence all of which were predicted to be
catalytically inactive, due to mutations in the active site (Holt et al., 2003
and Table 5.1). These scabies mite-inactivated protease paralogues – serine
proteases (SMIPP-Ss) are described below (Section 5.8). Similarly, a group
of inactivated cysteine proteases with homology to the group 1 allergens
of house dust mites termed scabies mite-inactivated protease paralogues –
cysteine proteases (SMIPP-Cs) have also been identified (Holt et al., 2004
and Table 5.1) but their function is currently unknown.
5.7. SSAP, AN ASPARTIC PROTEASE OF SCABIES MITES
Aspartic proteases are a class of endopeptidases that generally have a

bi-lobal structure, with each lobe contributing an aspartic acid residue to
the active site of the enzyme. Cathepsin d-like aspartic proteases are mem-
bers of the A1 family of aspartic proteases and are utilised as digestive
enzymes by a range of organisms. Blood-feeding parasites are thought to
use a proteolytic cascade to digest haemoglobin through an acidification
process and cathepsin d-like aspartic proteases play a key role in this pro-
cess in a number of parasites including Plasmodium (Francis et al., 1994),
hookworms (Williamson et al., 2002), Schistosoma (Brindley et al., 2001),
Onchocera (Jolodar et al., 2004) and Haemonchus (Longbottom et al., 1997).
It has been suggested that the host species specificity shown by some
parasitic organisms is due to compatibility between the sequence of the
host molecules and the specificity of the parasite’s proteolytic enzymes
(Brinkworth et al., 2000). The human hookworm Necator americanus and
the dog hookworm Ancylostoma caninum are able to infect their non-
preferred host; however, they are unable to successfully feed, develop and
reproduce. Recombinant aspartic protease from N. americanus (Na-APR-1)
and A. caninum (Ac-APR-1) were each shown to cleave haemoglobin from
their preferred host with at least twice the efficiency of haemoglobin from
their non-preferred host (Williamson et al., 2002). A similar preference for
substrates from the preferred host was also observed for the digestion of
serum proteins and skin macromolecules by Na-APR-1 and Ac-APR-1.
Despite this, the two enzymes have identical residues lining their active
site clefts (Williamson et al., 2003). Molecular models of Na-APR-1 and
Ac-APR-1 indicated that residues in the S3 pocket adopted different con-
formations, likely accounting for the differences in substrate specificity
observed (Brinkworth et al., 2001). Thus, minor amino acid changes or
variations in protein folding even in the absence of sequence differences
can alter enzyme–substrate interactions substantially.
Scabies mites infesting humans and dogs have been shown to be genet-
ically distinct (Walton et al., 1999, Walton et al., 2004a). This is consistent
with evidence of host specificity, with dog mites causing atypical infesta-
tions in humans that appear to be self-limiting (reviewed in Walton et al.,
2004c). Physiological differences in dietary requirements have been pro-
posed as a possible explanation for this observed host specificity (Arlian,
1989). Therefore, digestive enzymes are likely to play a role in this pro-
cess. Recently, aspartic protease activity in whole scabies mite extract has
been shown to be capable of cleaving haemoglobin (unpublished data).
A S. scabiei var. hominis cathepsin d-like aspartic protease sequence was
subsequently identified and termed SsAP-h. It was localised to the gnatho-
soma, gut and faecal pellets of the mite indicating that it is likely involved
in digestive processes (unpublished data). Indeed, the refolded, activated
recombinant SsAP-h was shown to be capable of digesting human haemo-

globin, serum albumin, fibronectin and fibrinogen in vitro (unpublished
data).
Recombinant SsAP-h was shown to be recognised by sera from infested
human patients (unpublished data), as was a human mite apolipopro-
tein (Harumal et al., 2003, Walton et al., 2010). However, while sera from
infested dogs also recognised the human mite apolipoprotein, they failed
to recognise the human mite aspartic protease SsAP-h (unpublished data).
This indicates that there may be differences between the aspartic proteases
of different host-associated mites, which result in the enzyme not being
recognised by the non-natural host. Analysis of the sequence of SsAP-h
revealed eight amino acid differences to a partial aspartic protease sequence
from fox scabies mites (Ljunggren et al., 2003) over the sequence available
(unpublished data). Further analysis of the aspartic proteases from differ-
ent host-associated scabies mites may provide evidence of the role of the
scabies mite aspartic protease in the host specificity of scabies mites.
In addition to their role in host specificity, aspartic proteases are attrac-
tive targets for therapeutic intervention in some parasitic organisms. The
general aspartic protease inhibitor pepstatin A has been shown to decrease
the migration of hookworm larvae through the skin, demonstrating the
essential function of this enzyme (Brown et al., 1999, Williamson et al., 2003).
As a result, the human hookworm aspartic protease Na-APR-1 has been the
focus of vaccine development against hookworm (Loukas et al., 2005, Xiao
et al., 2008, Pearson et al., 2009, Pearson et al., 2010). The development of
specific therapeutics to interfere with the function of the scabies mite aspar-
tic protease may prove to be a useful addition to the currently available
treatments. The inability to propagate scabies mites in vitro precludes the
testing of the phenotypic effect of such inhibitors on scabies mites in vitro;
however, the new porcine model will be a valuable tool in this respect.
5.8. INACTIVATED SCABIES MITE SERINE PROTEASE

PARALOGUES (SMIPP-SS) INTERFERE WITH HUMAN
COMPLEMENT
Any successful pathogen must have a strategy to resist complement-

mediated killing. Complement is a network of approximately 35 proteins
circulating in human plasma and penetrating most tissues including skin.
It is activated immediately upon contact of a microbe with host body flu-
ids. Triggered by immune complexes, carbohydrates or foreign surfaces its
activation proceeds via three cascades: the classical, lectin and alternative
pathways (Ricklin et al., 2010). Activation of any of these pathways leads
to opsonisation and phagocytosis of the target, the release of anaphylatox-
ins, induction of inflammation and the formation of the membrane attack
complex, which forms a pore in the target membrane and leads to cell
lysis. Furthermore, activated complement induces adaptive immunity at
the level of both B cells (Holers and Kulik, 2007) and T cells (Kemper and
Atkinson, 2007). Activated complement causes formation of membrane
attack complexes on the surface of foreign target cells, which are in the
case of the haematophagous parasites the gut epithelium. Hence, mecha-
nisms have evolved that allow (i) digestion of serous components and (ii)
evasion of these host defence factors. The complement system has several
sensory molecules that recognise molecular patterns foreign to its host.
Furthermore, it can be strongly activated by both low-affinity IgM anti-
bodies as well as specific, high-affinity IgG antibodies. Many pathogens
utilise multiple evasion strategies directed at inhibition of complement, as
redundancy and multiplicity are important for immune and complement
evasion (Zipfel et al., 2007). Schistosomes, for example, possess a plethora
of proteins impeding the human complement cascades (Skelly, 2004).
There are no earlier studies for mites but tick gut damage due to
ingested complement was suggested (Wikel, 1979). The protective prop-
erties of antibodies generated against the midgut protein Bm86 as used
in the vaccine against Rhipicephalus microplus, the most important tick
parasite of livestock in the world (Willadsen et al., 1996, De Rose et al.,
1999), rely markedly on complement (Kemp et al., 1989). Vaccination
trials against midgut secreted proteins of the tick Ornithodoros erraticus
have been shown to induce lethal gut damage, also thought to be medi-
ated by complement (Manzano-Roman et al., 2006). There is accumulat-
ing evidence that complement plays a major role in scabies mite biology
(Bergstrom et al., 2009, Mika et al., 2011, Mika et al., in review, in press).
The scabies mite produces at least 33 proteins that are closely related in
sequence to the house dust mite group 3 allergens and belong to the S1-like
serine protease family. The single proteolytically active member of this fam-
ily is Sar s 3 (Section 5.6). All other members in this family identified to date
contain mutations in the conserved active site catalytic triad that render
them proteolytically inactive. These genetically inactivated serine proteases
are thus termed scabies mite-inactivated protease paralogues – serine prote-
ases (SMIPP-Ss). The precise and entire function(s) of the SMIPP-S protein
family remains unclear. It was originally suggested that these proteins may
function by binding and protecting target mite substrates from cleavage by
host immune proteases, thus preventing the host from mounting an effec-
tive immune challenge. Several recombinant SMIPP-S proteins were pro-
duced in Pichia pastoris, following a similar protocol as established for the
active serine protease Sar s 3 (Beckham et al., 2009). Phage-displayed peptide
libraries have been previously used to identify peptide substrates of several
chymotrypsin-like serine proteases (Deperthes, 2002; Hekim, 2006). Since it
was likely that the SMIPP-Ss were inactive due to mutations of their cata-
lytic residues, we tested whether SMIPPs were able to bind 20-mer peptide
substrates fused to the minor coat protein pIII in a phage display library
(Coley et al., 2001). However, screening of the phage display peptide library
with three different SMIPP-Ss did not demonstrate a preference for any of
the amino acid sequences displayed (Fischer et al., 2009). These results were
consistent with structural data, which are outlined below, implying strongly
that SMIPP-Ss do not bind peptides, as might be expected for a catalytically
inactive proteases with an otherwise fully formed active site.
In order to begin to understand the structural basis for SMIPP-S func-
tion, the crystal structures of two SMIPP-S proteins from different clades
within the phylogenetic tree, namely SMIPP-S I1 and SMIPP-S D1, were
solved at 1.85 and 2.0 Å resolutions, respectively (Fischer et al., 2009). Both
structures display the characteristic serine protease fold but with substan-
tial structural variations over much of the molecule. Most strikingly, in
both structures, the mutations in the catalytic triad are combined with
an occlusion of the S1 subsite by a conserved tyrosine residue, located at
approximately position 200 of the amino acid sequence. This structural
blockage of the binding pocket in the SMIPP-Ss was proposed to be due to
the lack of the third disulfide bond, which is present in the proteolytically
active Sar s 3. Attempts to restore function (via site-directed mutagenesis
of catalytic residues as well as Tyr200) were unsuccessful. It was postu-
lated that SMIPP-Ss have lost the ability to bind substrates in a classical
‘canonical’ fashion and instead have evolved alternative functions in the
lifecycle of the scabies mite (Fischer et al., 2009).
Searching for the possible function(s) of the SMIPP-Ss concentrated
on host systems in contact with the scabies mite. Burrowing scabies mites
imbibe epidermal protein and plasma, which contain a multitude of diverse
host proteases, in particular of the coagulation and complement systems.
SMIPP-Ss are able to interact with several complement proteins, which
leads to inhibition of all three pathways of complement. Five recombinant
SMIPP-Ss randomly chosen as examples from multiple clades within the
phylogenetic tree of the SMIPP-S family (Fischer et al., 2009) were each
shown to prevent activation of all complement pathways in an ELISA-
based functional assay (Mika et al., in press). These data were obtained by
testing the SMIPP-Ss in a commercially available system (Wieslab Comple-
ment System Screen Kit, EuroDiagnostica) in which complement activation
was initiated by specific ligands for each pathway. After addition of human
serum, pretreated with the purified recombinant mite proteins, deposited
complement proteins were detected using specific antibodies against the
terminal membrane attack complex (C5b-9). A detailed in vitro study con-
sisting of haemolytic assays, a systematic series of deposition assays and
binding assays assessing individual complement factors revealed that two
representative SMIPP-Ss bound to distinct complement factors, thereby
effectively preventing the activation of all three main complement path-
ways (Bergstrom et al., 2009). Immunohistochemical staining demonstrated
the presence of complement components in the gut of scabies mites

(Bergstrom et al., 2009, Mika et al., 2011). This led to the hypothesis that
SMIPP-Ss minimise complement-mediated gut damage and thus create a
favourable environment for the scabies mites.
Relatively high concentrations of SMIPP-Ss in a micromolar range
were needed to observe a significant complement inhibition in some of
the assays presented in these studies (Bergstrom et al., 2009). Hence, it is
plausible to question their physiological concentration. It is important to
emphasise that all assays reported in this study were done in vitro with
recombinant molecules that were expressed, folded and activated in vitro.
It is likely that only a portion of these preparations of recombinant mol-
ecules are actually biologically active. Furthermore, the concentrations of
SMIPP-Ss or any other proteins in the mite gut are not known at present
and the local concentrations of complement proteins at the sites of mite
infection have also not been determined. However, 33 SMIPPs have now
been identified and since all five of the SMIPP-Ss tested to date show com-
plement-inhibitory functions, it is possible that many of these molecules
inhibit complement synergistically. In addition, another class of scabies
mite complement inhibitors has recently been identified (see below). This
makes it quite plausible that many of these complement-inhibitory mol-
ecules act on several levels of the complement system, accumulating to
high concentrations of anti-complement activities in the confined environ-
ment of the epidermal burrows. Further studies will be needed to assess
the in vivo relevance of SMIPP-Ss in defence against complement. SMIPP-
Ss are present in the gut of the mite and excreted in faeces, hence their
site(s) of action are likely both internal and external to the mite. Internally,
as the gut contains host plasma, complement cascades must be inhibited
in a milieu in which digestion of protein food can occur. This seems to be
an obvious role of the SMIPP-Ss. Externally, the inhibition of complement
may have further consequences for the host. By interfering with host com-
plement, the SMIPP-Ss may effectively enhance the survival of pathogenic
bacteria that colonise the mite burrows. In line with this hypothesis, it
has previously been shown that cysteine proteinases from Porphyromonas
gingivalis degrade complement factors and may provide an advantage to
other periodontal pathogens residing in the same location (Popadiak et al.,
2007). Ultimately, the inhibition of the host complement by scabies mite
products such as the SMIPP-Ss may account significantly for the associ-
ated secondary bacterial skin infections and downstream chronic disease.
It has very recently been shown that scabies mite proteins enhance the
growth of group A Streptococcus in whole blood assays by inhibition of
host innate immunity (Mika et al., in press and Section 5.10).
The X-ray crystal structures of SMIPP-S I1 and SMIPP-S D1 (Fischer
et al., 2009) may provide clues to the mechanisms of complement-binding
activities. Inspection of sequence variability within the SMIPP-S family in
the context of the existing two structures suggests that the family is confor-
mationally diverse and thus likely able to present multiple protein inter-
action-binding sites that could potentially bind a range of complement
proteins. However, the absence of structural information for most comple-
ment proteins precludes modelling of such potential interactions. In search
of structural properties related to this function, the sequence conserva-
tion within the SMIPP-S family was mapped onto both structures (Fischer
et al., 2009). It has been shown that sequence conservation of surface resi-
dues is a robust indicator of functional sites (Armon et al., 2001, Bell and
Ben-Tal, 2003). The low sequence conservation within the SMIPP-S fam-
ily was clearly revealed. When modelling 30 SMIPP-S sequences against
the two observed structures, the highest conservation was found within
the core of the molecule while the majority of surface-exposed regions
showed minor conservation. Despite the overall low conservation of the
SMIPP-S surfaces, a few small areas of relatively high conservation were
observed on the opposite side to the inactivated binding groove (Fischer
et al., 2009). These may be important for function as possible exosites.
Further insights may be obtained by structural characterisation of other
members of the SMIPP-S family, as well as complement-binding studies of
mutants, which can now be rationally guided by the available structural
data. Investigation is underway as to whether mutations in these regions
reduce the ability to bind to complement. Defining the SMIPP-S-binding
sites for the complement factors involved would allow the development
of inhibitory peptides that specifically block complement inhibition by the
mites, thereby allowing the host innate immune system to eliminate mites
and associated bacteria.
As the data described above strongly implicate molecules associated
with proteolytic systems in the mite, scabies mite serine protease inhibi-
tors of the serpin superfamily have also been investigated (Mika et al.,
in review). We propose that, apart from the SMIPP-Ss, scabies mite ser-
ine protease inhibitors may also protect scabies mites from complement-
mediated gut damage.
5.9. A SCABIES MITE PERITROPHIN IS A POTENTIAL TARGET OF

HOST COMPLEMENT
Parasitic invertebrates ingesting vertebrate plasma have evolved additional

strategies to protect themselves from hazardous host molecules consumed
during feeding. An important part of the immediate defence mechanisms
in vertebrate plasma is complement-mediated killing. We reviewed above
data indicating that scabies mites, who feed on skin containing plasma,
produce several proteins that inhibit human complement within the mite
gut. The mites excrete these molecules into the upper epidermis where
they presumably also inhibit complement activity. Mite gut antigens that
initially trigger the complement cascade have not been previously iden-
tified. Peritrophins are major components of the peritrophic matrix often
found in the gut of arthropods. A peritrophin, if abundant in the scabies
mite gut, could be an activator of ingested host complement.
A novel full-length scabies mite peritrophin (SsPTP1) was identified
as a highly abundant molecule in the cDNA library from S. scabiei var.
hominis (Mika et al., 2011). Antibodies against a recombinant SsPTP1 frag-
ment were used to immunohistochemically localise native SsPTP1 in the
mite gut and in faecal pellets within the upper epidermis, co-localising
with serum components such as host IgG and complement. Enzymatic
deglycosylation confirmed strong N- and O-glycosylation of the native
peritrophin. The abundance of SsPTP1 within the mite gut and its high
degree of predicted glycosylation led us to test the possible interaction
between mannan-binding lectin (MBL), the recognition molecule of the
lectin pathway of human complement activation, and native SsPTP1 in
extracts of native total mite protein. MBL is a pattern recognition molecule
specific for mannose, fucose and N-acetyl glucosamine(GlcNAc) (Turner,
1996). It binds to sugar arrays on the surfaces of microorganisms and
invertebrates (Holmskov et al., 1994) but not to most human glycopro-
tein glycans terminating in galactose or sialic acid. MBL thereby triggers
the lectin pathway in the host serum to eliminate microbial and parasitic
intruders (Ricklin et al., 2010).
SsPTP1 was predicted to be strongly glycosylated as the amino acid
sequence outside of the chitin-binding domains was covered with puta-
tive N- and O-glycosylation sites. Scabies mite homogenates were sub-
jected to deglycosylating enzymes to remove N- and O-glycosylation of
the proteins and subsequently separated by SDS-PAGE. In accordance
with the large number of predicted O-glycosylation sites in SsPTP1,
O-glycosylation was shown to be predominant. When blotting onto a
membrane and incubating with 50% normal human serum (containing
all complement factors including MBL), followed by immunodetection of
bound MBL using an anti-MBL antibody, MBL specifically bound to gly-
cosylated SsPTP1. With an average concentration of only ~1.2µg/ml MBL
is relatively scarce in human serum (Arnold et al., 2006). Nonetheless, the
experimental removal of glycans affected the binding of MBL drastically,
indicating that MBL may have bound to SsPTP1 carbohydrates.
Given the millennia of co-evolution between parasites and host,
many pathogens have evolved a range of elaborate counterstrategies to
evade complement (Ricklin et al., 2010). Among the many mechanisms
observed, the capture of complement initiators (such as immunoglobulins)
and the depletion of complement components due to binding to secreted
pathogen molecules have been described for bacteria, viruses, fungi and
parasites (Lambris et al., 2008). Glycoproteins in herpes viruses have Fc
receptor properties and can deplete antibody recognition and activation of

the classical pathway (Favoreel et al., 2003). There is increasing evidence
that microorganisms developed incredible fine-tuning of activation and
inhibition. Viruses ‘voluntarily’ activate complement through surface gly-
coproteins to become opsonised and enter host cells through complement
receptors. At the same time, they keep complement activation in check
by other mechanisms (Lambris et al., 2008). It may be possible that the
scabies mite peritrophin targets MBL in the gut lumen, thereby deplet-
ing it and avoiding membrane attack complex formation on the gut epi-
thelial cells, in addition to the inactivation of complement factors by the
SMIPP-Ss (Bergstrom et al., 2009).
This study added a new aspect to the accumulating evidence that com-
plement plays a major role in scabies mite biology. It identified a novel
peritrophin localised in the mite gut as a potential target of the lectin path-
way of the complement cascade. These initial findings indicate a novel role
of scabies mite peritrophins in triggering a host innate immune response
within the mite gut. It is highly likely that, apart from SsPTP1, other mech-
anisms are leading to complement binding in the mite gut. Elucidating in
depth the molecular mechanisms that are involved in restricting comple-
ment activation within the mite gut and in the infested epidermal tissue
will be vital for developing novel strategies of therapeutic intervention
against scabies and associated bacterial infections.
5.10. COMPLEMENT INHIBITION BY SCABIES MITES PROMOTES

STREPTOCOCCAL GROWTH IN VITRO
Scabies infestations predispose to secondary bacterial skin infestation.

However, the molecular interactions between human host, bacteria and
mites have never been examined. It has been established that a large num-
ber of proteins expressed by scabies mites inhibit all three pathways of
human complement (Section 5.8). These proteins are secreted into the mite
gut and subsequently excreted as components of faeces into mite burrows
in the subepidermis regions of human skin (Figs 5.1 and 5.2). By inference,
suppressed local complement should favour secondary infections by bac-
terial pathogens. Indeed, in tropical settings, association between scabetic
infestation and pyoderma caused by group A Streptococcus has been well
established (Currie and Carapetis, 2000, McDonald et al., 2007, Clucas
et al., 2008, La Vincente et al., 2009, Steer et al., 2009). Globally, group A
Streptococcus-associated diseases affect an estimated 18.1 million individu-
als and account for over 0.5 million deaths per year from all causes of
streptococcal diseases such as rheumatic heart disease, post-streptococcal
glomerulonephritis and severe invasive diseases (Carapetis et al., 2005). In
Australian Aboriginal communities, rheumatic fever and rheumatic heart
disease prevalence was 2% in 2008 (Parnaby and Carapetis, 2010), trans-

lating to the highest incidences reported globally (Carapetis et al., 2007).
Scabies and pyoderma have also been linked with outbreaks of acute post-
streptococcal glomerulonephritis (Clucas et al., 2008, La Vincente et al.,
2009, Marshall et al., 2011). In some remote Aboriginal communities, 63%
and 69% of children had presented with scabies and skin sores, respec-
tively, by 1 year of age (Clucas et al., 2008). Community-wide treatment
of scabies decreases pyoderma (Carapetis et al., 1997, Lawrence et al.,
2005), pointing towards a key role of the mite burrowing in the human
epidermis.
While mechanical infringement of the stratum corneum caused by
mites and host scratching could promote secondary infections of the skin,
molecular host–parasite interactions underlying increased incidence of
streptococcal pyoderma among scabies patients have not been investi-
gated. SMIPP-Ss and more recently scabies mite serine protease inhibi-
tors have been characterised as effective complement inhibitors and are
detected in parasite faeces within the human epidermis. Whole-blood
bactericidal assays employing functional human phagocytes and com-
plement (Lancefield, 1957, Brandt et al., 1996, Carlsson et al., 2003) were
recently utilised to investigate if inactivation of complement pathways by
these complement inhibitors aids in efficient growth of group A Streptococ-
cus. The initial data produced indicate a substantial increase in growth of
group A Streptococcus (Mika et al., in press) in the presence of SMIPP-Ss
and scabies mite serine protease inhibitors, suggesting an efficient inter-
ference with bacterial uptake by human phagocytes. It is intriguing to
consider that the collective complement-inhibitory function of multiple
mite excretory proteins in combination with complement inhibitors pro-
duced by group A Streptococcus (Rooijakkers and Van Strijp, 2007) pro-
motes the survival of bacterial pathogens in the microenvironment of the
epidermal burrows produced by the mites. This molecular link between
complement inhibition by mite proteins and bacterial survival is a novel
aspect of pyoderma pathogenesis that may have important implications
for the development of alternative therapies.
5.11. CONCLUSION
Recent research strongly suggest that the misnomer ‘itch mite’ trivialises
this important disease and that more clinical emphasis should be given
to the role of the mite and to controlling it in tropical settings. Improv-
ing the treatment and management of scabies requires foremost a bet-
ter understanding of the interactions between scabies mites, the bacteria
subsequently infecting the scabies lesions and the host immune system.
The EST data set and the accumulating biochemical and functional data
on mite proteins involved in pathogenesis and parasite survival are fun-

damental to this. Many of the mite proteins currently being investigated
are involved in the host–parasite interface and hence are potential tar-
gets for therapeutic intervention. The design of specific inhibitors of key
mite molecules involved in pathogenic processes is a logical progression.
The recently developed porcine model of scabies should now provide a
suitable platform to confirm in vivo the predominantly in vitro evidence
described here and to test potential treatment options.
ACKNOWLEDGEMENTS
This study was supported by the Australian National Health and Medical Research Coun-
cil through Program Grant 496600, Project Grants 613626 and 545220, and a fellowship to
D. J. Kemp.
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CHAPTER 6
Review: Surveillance of Chagas
Disease
Ken Hashimoto* and Kota Yoshioka†

6.2. Epidemiological Trends 379
6.2.1. South America – INCOSUR 379
6.2.2. Central America – IPCA 382
6.3. Vector Surveillance 386
6.3.1. South America – INCOSUR 386
6.3.2. Central America – IPCA 388
6.3.3. Common structures of vector
surveillance systems 389
6.4. Mechanism of Community-based
Surveillance Systems 391
6.4.1. Five basic functions 392
6.4.2. Stakeholders 393
6.4.3. Evaluation of process and results 394
6.4.4. Mechanism of community-based
surveillance systems in El Salvador and Honduras 396
6.5. Health Systems and Community-based
Surveillance Systems 402
6.5.1. Viewpoints to analyse program integration 403
6.5.2. Integration of community-based
surveillance systems in El Salvador and Honduras 404
6.6. Challenges 409
6.6.1. Challenges for further evolution
of surveillance systems 409
6.6.2. Challenges for regional strategies 411
6.6.3. Development of ecological approach 413
* Chagas Disease Control Projects, Japan International Cooperation Agency, Central America
† Chagas Disease Control Project, Japan International Cooperation Agency, Managua, Nicaragua
375
376 Ken Hashimoto and Kota Yoshioka
6.7. Situations of Other Initiatives 415

6.7.1. Latin America 415
6.7.2. Non-endemic countries 416
6.8. Conclusions 418
Acknowledgments 419
References 419
Abstract After remarkable reduction in prevalence through regional elimination

of domestic vectors, the central challenge of Chagas disease control is
shifting towards interruption of the disease transmission by non-elim-
inable vectors in Latin America. Vector surveillance with community
participation was cost-effective against the eliminable vectors. But
the efforts often failed against the non-eliminable vectors due to lack
of surveillance coverage or sustainability. For instance, in El Salvador
and Honduras, the operational vector control personnel lost access
to many communities under decentralized health systems. To cover
wider areas lastingly, the countries implemented the surveillance sys-
tems involving non-specialists from locally embedded resources, such
as local health services, schools and community leaders. From these
experiences, this paper outlines a common structure of the current
community-based surveillance systems, consisting of five fundamen-
tal sequential functions. To increase scalability and sustainability, four
of the five functions could be delegated to the locally available hu-
man resources, and the surveillance systems can be integrated into the
general health systems. Challenges at national and regional levels are
discussed for further evolution of the surveillance systems.
6.1. INTRODUCTION
Prevalence of Chagas disease or American trypanosomiasis has declined

in Latin America (Moncayo, 2003; Moncayo and Ortiz, 2006; WHO, 2007a;
Moncayo and Silveira, 2009). The affected population reduced from 16–18
million in the 1980s to 8–9 million today (WHO, 1991; PAHO, 2006b).
Along with remarkable progress in the medical knowledge and practice
(Lescure et al., 2010; Rassi et al., 2010; Telleria and Tibayrenc, 2010; Weiss
and Tanowitz, 2011; Weiss et al., 2011), effective interventions have been
implemented mainly to interrupt the disease transmission through vector
and blood transfusion. Much of the efforts and resources were placed on
the vector control, which was responsible for more than 80% of all trans-
mission (Schofield, 1994).
The dramatic reduction in prevalence owes principally to the South
American efforts which reduced the incidence by 70% (Dias, 2007;
Moncayo and Silveira, 2009). Transmission through the main vector,
Review: Surveillance of Chagas Disease 377
Triatoma infestans, was interrupted in Uruguay in 1997, Chile in 1999,

Brazil in 2000–2005 and in extensive areas of Argentina, Bolivia and
Paraguay. The national control programs were coordinated internation-
ally through the regional initiative (Iniciativa de Salud del Cono Sur,
INCOSUR). INCOSUR was established in 1991 between Argentina, Bolivia,
Brazil, Chile, Paraguay and Uruguay, providing opportunities for devel-
opment of technical knowledge and political impulse (e.g. PAHO, 2002).
Key success factors for these countries were availability of the established
technology and strategy, strong leadership at the central level, support-
ive scientific community and feasible, valuable and cost-effective regional
initiative (Yamagata and Nakagawa, 2006).
The vector control strategy in INCOSUR was developed after the
successful malaria control program of the 1950s (Dias, 1991). The strat-
egy consisted of preparatory, attack and surveillance phases. In the
preparatory phase, the national control program determines high-risk
areas through epidemiological and entomological surveys. During the
attack phase, houses in high-risk areas are sprayed with insecticides
to reduce the vector infestation levels. The surveillance phase follows
aiming to minimise the re-emergence of risks by selective insecticide
spraying of reinfested houses. If absence of the vector infestation is
demonstrated for more than three consecutive years under perma-
nent surveillance, the Initiative certified for vector elimination (PAHO,
1994). These certification criteria were developed in South America
(PAHO, 1994) and later adopted in Central America (PAHO, 2003a).
The South American approach was considered to be technically fea-
sible in other regions (Schofield and Dujardin, 1997; Schofield and Dias,
1999). The success of INCOSUR led to establishment of an international
target, ‘elimination of Chagas disease transmission’ at the 51st World
Health Assembly in 1998 (WHO, 1998) as well as foundation of other
regional initiatives. In 1997, the Central American initiative was launched
among Belize, Costa Rica, El Salvador, Guatemala, Honduras, Nicara-
gua and Panama (Iniciativa de los Países de Centroamérica, IPCA). In
the same year, the Andean initiative was formed by Colombia, Ecuador,
Peru and Venezuela (Iniciativa de los Países Andinos, IPA). In 2004, the
Amazon initiative was established for the specific epidemiological and
ecological situations in Bolivia, Brazil, Colombia, Ecuador, French Gui-
ana, Guyana, Peru, Suriname and Venezuela (Iniciativa de los países
Amazónicos, AMCHA).
Recently, Central American countries made progress towards the
common objective. Chagas disease transmission by one of the principal
vectors, Rhodnius prolixus, was interrupted in Guatemala in 2008 and
Honduras and Nicaragua in 2011. Elimination of R. prolixus was also
certified in El Salvador in 2010 and Costa Rica in 2011 based on the vector
control activities from the 1950s to 1970s (IPCA, 2008; IPCA, 2010; IPCA,
2011; Hashimoto and Schofield, 2012). The vector control technology

and strategy developed by INCOSUR were largely applicable to Central
America.
The experience of INCOSUR and IPCA shows that the existing tech-
nology and strategy can achieve elimination of the highly domestic vec-
tors and substantial reduction of other widespread species. However,
elimination or reduction of the vectors is not an end point. Native or
autochthonous species, such as T. infestans in Andean valleys in Bolivia or
T. dimidiata in Central America, are capable of infesting the human dwell-
ings repeatedly even after the massive and multiple insecticide spraying
(Noireau et al., 2005; Hashimoto et al., 2006). The next challenge is to sus-
tain vector surveillance with community participation and retreatment
of any newly detected domestic vectors (Dias et al., 2002; Ramsey and
Schofield, 2003).
The surveillance phase must continue eternally because not all vectors
are eliminable. Indeed, out of the 21 endemic Latin American countries,
none has achieved the complete vector elimination. If the surveillance is
prematurely relaxed, the progressive re-establishment of active transmis-
sion could be the consequence (Dias, 2009). To sustain the surveillance,
three issues are considered essential.
Firstly, although the core surveillance strategies are essentially the
same against eliminable and non-eliminable vectors (i.e. vector report-
ing and retreatment), management of surveillance systems must differ
because of geographical and time scales (Table 6.1). Domestic infesta-
tions of the non-eliminable autochthonous vectors are more extensive
and persistent; thus, the vector surveillance needs be designed to cover
wider geographical areas on a lasting-basis. These scale factors make the
surveillance of non-eliminable vectors even more challenging.
Secondly, the surveillance system should be continually adjusted to
fit into the changeable general health systems. The health sector reform
is an ongoing issue in Latin America under health policies such as
decentralisation and primary health care (PHC). For example, in Bra-
zil, the decentralisation of health systems transformed Chagas disease
control activities from the national program to the municipal programs
TABLE 6.1 Spatial and temporal scale for the surveillance of eliminable
and non-eliminable vectors
Vector Eliminable Non-eliminable
Objective To verify elimination To maintain low house infestation

Target areas Previously infested areas All eligible areas for infestation
End point When the vector is not Not clearly consented or may not
reported for 3 years exist
(Dias, 2009). Each country is required to keep updating the surveillance

s ystem in accordance with changes in the general health systems.
Thirdly, the political is likely to decline in the surveillance phase. The
attained success in the attack phase may generate excessive optimism and
may even disregard the disease and its control among health authorities.
The loss of visibility and priority may be a logical consequence, partic-
ularly in most Latin American health systems that are still disorganised
and overburdened due to insufficiencies of financial and human resources
(Dias et al., 2008). Thinking ahead to low political will, the surveillance
systems should be designed to be functional at a minimal institutional
cost.
To interrupt vector-borne transmission of Chagas disease, the current
technical challenge is to establish scalable and sustainable surveillance
systems. Development of strategies for maintaining surveillance is one of
urgent needs (Lannes-Vieira et al., 2009), even in the areas where the con-
trol of eliminable vector had successfully concluded (Costa and Lorenzo,
2009). Experiences have been documented in a certain level; however,
management and operation of surveillance systems are yet to be studied
in a systematic manner. This paper reviews strategies implemented dur-
ing the surveillance phase in the countries, where the transmission of Cha-
gas disease by the eliminable vectors has been interrupted, and analyses
the factors associated with scalable and sustainable surveillance systems.
Based on the findings, future strategies for the surveillance phase will be
discussed.
6.2. EPIDEMIOLOGICAL TRENDS
6.2.1. South America – INCOSUR

The estimated prevalence remains relatively constant in INCOSUR
(Table 6.2), after interruption of the disease transmission by the prin-
cipal vector, T. infestans. The epidemiological stability is attributable
to the implementation of the surveillance system and screening of all
blood donations in the 1980s and 1990s. In the short term, the general
prevalence may show scarce decrease or even increase depending on the
estimation methods but is expected to decline gradually over the next
decades.
Screening at blood banks for Trypanosoma cruzi antibody prevents
transfusional transmission and offers prevalence data among the donors.
In the INCOSUR countries, all blood donations are screened except those
at non-endemic areas in Southern Chile. The seroprevalence among
blood donors has reduced in the INCOSUR countries in the past two
decades (Table 6.3). This indicator reflects retarded but actual effects of
TABLE 6.2 Estimated number of the infected, prevalence and incidence of Chagas
disease in Southern Cone Initiative, 1975–2005
Number of the infected Prevalence (%) Incidence (%)
Country 1975–1985 2002 2005 2002 2005 2005
Argentina 2,640,000 1,671,164–2,202,898 1,599,864 4.4–5.8 4.13 0.003

Bolivia 1,300,000 1,300,000–2,074,800 619,968.64 19–24 6.752 0.112
Brazil 3,600,000 1,961,000–2,291,341 1,899,467 1.1–1.3 1.02 0.000
Chile 150,000 62,452–93,678 160,233 0.4–0.6 0.99 0.000
Paraguay 397,000 223,860–287,000 150,003 3.9–5.0 2.54 0.015
Uruguay 37,000 3,391–20,346 21,685 0.1–0.6 0.66 0.000
Source: Patterson and Guhl (2010) (1975/1985 data were collated by Strosberg et al. (2007) and the 2005
data were sourced from PAHO (2006b)).
the control interventions, although the results may not be representa-

tive of the general population due to relatively limited access for rural
population to blood banks and filtering of donors from endemic areas at
prescreening interviews.
Acute cases are rarely found after achieving interruption of transmis-
sion by T. infestans. Occasional case reports derive from reinfestation by
T. infestans and lack of community-based surveillance system (PAHO,
2002) as well as oral transmission where infected bugs were accidentally
ground in fresh fruit juice (Pereira et al., 2009). Attempts also began on
surveillance of congenital transmission and chronic cases as the next
challenges (Gürtler et al., 2008; Lannes-Vieira et al., 2010).
The younger generations have shown more evident changes in the
prevalence rates. In Argentina between 1992 and 2003, the seroprevalence
reduced from 6.3% to 2.74% among children under 15 years old from rural
areas and from 11.84% to 5.49% among pregnant women while intradomi-
ciliary vector infestation rates decreased from 6.11% to 0.95% under sur-
veillance (Zaidemberg et al., 2004). In the Oriental Region in Paraguay,
the serological prevalence among children of 1–5 years of age declined
from 0.6% in 2001 to 0.3% in 2008 (PAHO/WHO, 2011). National surveys
in Brazil showed that the seroprevalence among children under 5 years
of age declined from 2.21% in 1975–1980 (Silveira et al., 2011) to 0.03%
in 2001–2008 (Luquetti et al., 2011). In general, the countries with vector
control have shown trends towards progressive reduction in the number
of infected donor candidates and gradual shift of the infected individuals
to older age groups (Coura and Dias, 2009).
Sporadic vector-borne transmission continues to be observed in INCO-
SUR (Table 6.4). Reinfestaion by T. infestans is reported in the Gran Chaco
areas, Andean valleys of Bolivia and Southern Peru, where the wild pop-
ulations of T. infestans is widespread (Ceballos et al., 2011; Noireau et al.,
TABLE 6.3 Screening coverage and prevalence among blood donors in Southern Cone
countries from 1993 to 2009
% of reactive donors for

% of blood donors screened Trypanosoma cruzi
Country 93–95a 01/02a 05b 09c 93–95a 01/02a 05b 09c
Argentina 100 100 100 100 4.92 4.50 3.75 3.08

Bolivia 29.4 86.1 99.3 100 14.79 9.91 8.61 2.62
Brazil na 100 100 100 na 0.61 0.61 0.20
Chile 76.7 75.2 68.7 na 1.20 0.47 0.27 na
Paraguay 87.0 99.8 99.8 100 4.50 0.28 3.30 2.85
Uruguay 100 100 100 na 0.62 0.47 0.26 na
na, data not available.
a Schmunis and Cruz (2005)
b PAHO (2007)
c PAHO (2010a,b,c).
TABLE 6.4 Achievement and current challenges of vector control in Southern Cone
Initiative
Principal
Country vectors Achievementa Current challengesa
Argentina Triatoma Interruption of transmis- Persisting vector-borne

infestans sion in five provinces transmission in 18 other
(2001) and other four endemic provinces
provinces (2011)
Bolivia T. infestans Vector-borne transmission Vector-borne transmission
has declined in past is still active
10 years, with interrup-
tion of transmission in
one department (2011)
Brazil T. infestans Interruption of transmis- Sporadic vector-borne trans-
sion (2006) mission in Amazon region
Chile T. infestans Interruption of
transmission (1999)
Paraguay T. infestans Interruption of Persisting vector-borne
transmission in the east- transmission in Chaco
ern region (2008) region
Uruguay T. infestans Interruption of transmission
(1997)
a WHO/PAHO (2010a), modified by authors to be updated.
2005; Noireau, 2009, Rolón et al., 2011). Morphologically, the wild T. infes-
tans is classified into three forms: dark morph, Mataral morph and common
morph (whose chromatic pattern is similar to that of domestic population).
The dark morph has arboreal habitats in Chaco and the Mataral morph has
rupicolous habitat in Andean valleys. These areas hypothetically consid-
ered to be the origin of T. infestans (Noireau, 2009) and are likely to encoun-
ter difficulties in domestic vector control without adequate surveillance. For
example, in Argentine Gran Chaco where T. infestans has sylvatic colonies
highly connected to domestic or peridomestic conspecifics (Ceballos et al.,
2011), the elimination of T. infestans has failed because of its early domes-
tic reinfestation from peridomestic foci or surrounding infested communi-
ties (Cecere et al., 2006; Gürtler, 1999; Gürtler, 2009). In this area, the first
spraying campaign was conducted in 1985; however, human T. cruzi trans-
mission resurged within 2–3 years because of absence of subsequent effec-
tive surveillance. Renewed intervention in 1992, with community-based
surveillance and selective action control, led to the interruption of human
T. cruzi transmission (Gürtler et al., 2007). Elimination of T. infestans remains
as a challenge in the specific areas in INCOSUR. In addition, secondary
autochthonous vectors such as T. sordida and T. brasiliensis have potentials to
occupy ecological niche of T . infestans after its elimination (Guhl et al., 2009).
6.2.2. Central America – IPCA

Prevalence in Central America started declining effectively after launch-
ing IPCA in 1997. Three species of the vector are considered important
in the region: R. prolixus, T. dimidiata and R. pallescens (Schofield, 2000).
Since the late 1990s, El Salvador, Guatemala, Honduras and Nicaragua
intensified vector control interventions targeting mainly the former two
species and recorded notable progress. By 2005, the community-based
surveillance was in place, but in limited areas of Guatemala. Accordingly,
reduction in seroprevalence in 2005 is mostly attributable to decreased
vector infestation through insecticide spraying campaigns and little to the
subsequent surveillance activities (Table 6.5).
Surveillance of blood transfusion improved and achieved the entire
coverage of screening of T. cruzi antibody in Central America through the
2000s (Table 6.6). The seroreactive rates still do not demonstrate possi-
ble effects of the vector control interventions because the reactive donors
are usually adults and most likely to have been infected before the late
1990s. Seroprevalence in children under 15 years of age, on the other hand,
reduced from 5.0% to 0.4% in Honduras (MoH and JICA, 2011). Yet, peri-
odic evaluation of seroprevalence in younger generations will provide
more analysable information on the impact of the surveillance activities.
In Central America, the strategic focus for surveillance is also placed
on detection of acute cases along with T. dimidiata infestation. El Salvador
TABLE 6.5 Estimated number of the infected, prevalence and incidence of Chagas
disease in Central American Initiative, 1975–2005
Number of the infected Prevalence (%) Incidence (%)
Country 1975–1985 2002 2005 2002 2005 2005
Belize 600 600–650 2001 0.26 0.74 0.009

Costa Rica 130,000 77,786–130,000 23,020 1.9–3.2 0.53 0.001
El Salvador 900,000 192,000–320,750 232,027 2.5–5.0 3.37 0.036
Guatemala 1,100,000 337,008–734,196 249,964 2.8–6.1 1.98 0.017
Honduras 300,000 103,750–300,000 219,969 1.19–1.53 3.05 0.039
Nicaragua 67,000 68,822–176,055 58,621 1.29–3.3 1.14 0.015
Panama 200,000 6000–220,000 194 <0.1–7.59 0.01 0.007
Source: Patterson and Guhl (2010) (1975/1985 data were collated by Strosberg et al. (2007) and the 2005
data were sourced from PAHO (2006b)).
TABLE 6.6 Screening coverage and prevalence among blood donors in Central
America from 1993 to 2009
% of reactive donors for

% of blood donors screened Trypanosoma cruzi
Country 93–95a 01/02a 05b 09c 93–95a 01/02a 05b 09c
Belize na na 100 100 na na 0.45 0.66

Costa Rica 0.0 25.1 100 100 0.80 0.36 0.09 0.42
El Salvador 42.5 100 100 100 1.47 0.3 2.40 1.93
Guatemala 75.0 92.7 100 100 1.40 1.02 1.40 1.75
Honduras 100 100 100 100 1.24 0.87 1.47 1.55
Nicaragua 58.4 95.0 100 100 0.24 0.49 0.90 0.12
Panama 24.0 34.0 97.6 100 0.13 0.9 0.12 0.36
na, data not available.
a Schmunis and Cruz (2005)
b PAHO (2007)
c PAHO (2010a,b,c)
is one of the countries with highest detection rates of acute cases in Latin
America. Annually detected cases ranged from 49 to 264 during 1993–1996
(WHO, 1997a) and continued averaging around 100 through the 2000s
(Ministerio de Salud de El Salvador, 2010; PAHO, 2010b). Blood samples of
clinically suspicious individuals are examined by trained laboratory tech-
nicians at the local health facility for parasitological tests using the centri-
fuge and microscopy. The clinical surveillance is operated by the trained
medical professionals at health facilities for diagnosis and treatment with
participation of the oriented community leaders and householders for

symptom recognition and reference to the local health centers.
The high detection rates in El Salvador in comparison to the neigh-
boring countries are attributable principally to three essential factors.
1) Accessibility to the local health facility: high population density indi-
cates closer distance to the medical service and information.
2) Highly trained professionals at the local health facility: the laboratory
technicians are university graduates. Whole laboratory network has
been trained and equipped for parasitological diagnostic techniques
for acute case detection (Luquetti, 2011).
3) High transmission efficiency of T. dimidiata in the dense housing envi-
ronments (very limited peridomestic areas).
Among the two targeted vectors, the control priority recently shifted
from R. prolixus to T. dimidiata (Table 6.7). Distribution of R. prolixus,
known to have transmission capacity about three times higher than that of
T. dimidiata (Ponce et al., 1995; Schofield, 2000; Paz-Bailey et al., 2002),
was dramatically extracted through massive chemical control operations
in Guatemala, Honduras and Nicaragua (Nakagawa et al., 2003a,b; MoH
and JICA, 2007, 2011; Yoshioka et al., 2011; Hashimoto and Schofield, 2012).
Following recent remarks of interruption of Chagas disease transmission
by R. prolixus in these three countries and elimination of the vector in El
Salvador and Costa Rica, T. dimidiata became recognised as the main vec-
tor in Central America (IPCA, 2011).
Unlike domestic R. prolixus, the habitat of T. dimidiata ranges from
sylvatic conditions to human dwellings, including urban areas (Zeledón
et al., 2005; Guzman-Tapia et al., 2007). Some populations appear to
remain sylvan and others have evidence of migrating between sylvatic
and domestic habitats (Dorn et al., 2006). Reinfestation of houses by
T. dimidiata after insecticide application is well known (e.g. Dumonteil
et al., 2004; Hashimoto et al., 2006). As being extensively distributed, its
elimination is not feasible. Therefore, the control program has strategi-
cally aimed to reduce infestation index below 5% so that the transmis-
sion of Chagas disease would be rare (Yamagata and Nakagawa, 2006;
WHO, 2006). Recently, the IPCA proposed that ‘elimination of domes-
tic colonies’ should be the goal of control of T. dimidiata (PAHO, 2009a;
IPCA, 2011), but feasibility of this goal is yet to be proved theoretically
and empirically. There could be a technical gap between the proposed
goal and available control methods. To fulfil this gap, the IPCA empha-
sises a need to develop innovative control strategies and techniques
(IPCA, 2011).
The experience of vector control program in Guatemala and El Salvador
shows that the multiple spraying in the attack phase reduced drastically
not only R. prolixus but also T. dimidiata (Nakagawa et al., 2003a,b; Hashi-
moto et al., 2006; PAHO, 2010b). House infestation index of T. dimidiata
TABLE 6.7 Achievement and current challenges of vector control in Central America
Country Principal vectors Achievementa Current challengesb
Belize Triatoma Elimination of domestic

dimidiata colonies of T. dimidiata
Costa Rica T. dimidiata Absence of Elimination of domestic
Rhodnius colonies of T. dimidiata
prolixus (2011)
El Salvador T. dimidiata Elimination of Elimination of domestic
R. prolixus (2010) colonies of T. dimidiata
Guatemala R. prolixus, Interruption of a) Certification of
T. dimidiata transmission by elimination of R. prolixus
R. prolixus (2008) b) Elimination of domestic
colonies of
T. dimidiata
Honduras R. prolixus, Interruption of a) Certification of
colonies of
T. dimidiata
Nicaragua R. prolixus, Interruption of a) Certification of
colonies of
T. dimidiata
Panama T. dimidiata, a) Elimination of domestic
R. pallescens colonies of T. dimidiata
b) Strengthening of entomo-
logical surveillance system
for R. pallescens
a WHO/PAHO (2010a)
b PAHO (2009a,b), modified by authors to be updated.
lowered in extensive areas in Central America, although sporadic and clus-

ter infestation of T. dimidiata are still found especially in the southeastern
Guatemala and western El Salvador (MoH and JICA, 2007, 2011; IPCA,
2010; PAHO, 2010b; Manne et al., 2012). Recent seroprevalence among
children under 16 years old ranged from 1.1-1.4% in El Salvador and from
0.03-0.4% in Honduras (PAHO, 2010b; MoH and JICA, 2011; Aiga et al, in
press). Although T. dimidiata is widely distributed, its large genetic varia-
tion can be classified into four taxonomic subgroups (Bargues et al., 2008).
The genetic difference may provide clear understanding of the ecological
pattern and epidemiological role of each subgroup leading to shape more
suitable vector control strategies. Spatial analysis of T. dimidiata is developed
to predict its geographical distribution, but the prediction model may need
to be improved to be put in practical use (Dumonteil and Gourbière, 2004;
Bustamante et al., 2007).
Rhodnius pallescens is present in Panama, Nicaragua and Costa Rica
(Arboleda et al., 2009) and is commonly found in the wild environments
corresponding to the tropical rain forest. The adult population are flying
visitors to the human dwellings and transmit T. cruzi to the inhabitants.
Some trends towards domestic colonisation have also been observed in
the recent years (Zeledón et al., 2006). The control activities are not yet in
place due to lack of adequate technology and strategy.
6.3. VECTOR SURVEILLANCE
6.3.1. South America – INCOSUR

After successful reduction of T. infestans through attack phase, mainte-
nance of surveillance actions became the main challenge in INCOSUR
(e.g. in Brazil: Silveira and Vinhaes, 1999). One of the practical mod-
els for community-based surveillance was developed in Brazil during
the 1980s using triatominae notification posts (Postos de Informação de
Triatomíneos, PITs) (Ministério da Saúde Brazil, 1980; Garcia-Zapata
and Marsden, 1993). Householders in endemic areas deposited vec-
tor bugs found in their houses into the post located in the community.
Institutional personnel from the Ministry of Health (MoH) collected the
bugs and sprayed the reinfested houses on a regular basis. Commu-
nity participation improved efficiency for identifying and treating the
reinfested houses. This model was later implemented in neighbouring
countries, but with slight adjustments, in accordance with the societal
contexts. That is, surveillance systems became more multi-sectoral using
locally embedded resources as intermediate agents to facilitate bug
reporting and collection as well as treatment of infested houses (Table 6.8)
(PAHO, 2003b). In the recent years, due to rare vector infestation and
technological advance, the Chilean MoH set up entomological consult-
ing units, where no intermediate agents are involved but presence of the
suspicious bugs are directly reported by the community via telephone
or email.
In South America, the vector control programs have faced the adminis-
trative and political challenges: 1) loss of political interest in already certif-
icated areas, 2) constant reduction of the technical staff and expertise and
3) difficulties to maintain the activities under restructured health systems
(Dias, 2007). In this context, no country has sufficient vector control tech-
nicians (VCTs) to establish and maintain regular surveillance in all eligible
areas for vector infestation or reinfestatoin.
TABLE 6.8 Responsible actors and intermediate agents for vector surveillance in Southern Cone Initiative
Argentina Bolivia Brazil Chile Paraguay Uruguay
Responsible man- Local Environ- Municipalities Municipal Health PHC Service Departmental Vector
agement unit mental Health headquarter Service Control Program
Unit Center
Intermediate Schools, PHC Schools, com- Schools, com- Schools, Schools, com- Schools, army and
agents (bug agents, community leaders, munity leaders, PHC munity lead- police
report collec- munity leaders, army and police, PIT agents ers, ethnic
tion) sensor boxes ethnic churches, churches,
NGOs, PIT NGOs
Intermediate Information and na Information and na na na
agents (treat- attack posts attack posts
Review: Surveillance of Chagas Disease

ment of infested at distant at distant
houses) community community
PHC, primary health care; NGO, non-governmental organisation; PIT, Posto de Informação de Triatomíneos (triatominae notification post); na, not available.
Source: PAHO (2003b, p. 126, Table 42).
387
As an alternative, inclusive strategy was developed in view of commu-

nity participation. In Argentina, for example, the vertical control program
managed to reduce seroprevalence from 10.1% in 1964 to 1.9% in 1993
among 18- or 20-year-old men drafted into the military service (Segura
et al., 1999). However, the vertical strategy failed to reach and sustain the
surveillance in widespread rural areas. An alternative horizontally struc-
tured control strategy was tested in the Province of Santiago del Estero,
where the PHC agents monitored quarterly the passive detection device
(sensor box). Its cost was five times lower than the vertical surveys by the
entomological technicians (Chuit et al., 1992). Being proved to produce
better impact on house reinfestation and community participation, this
strategy was expanded to broader geographical areas (Chuit et al., 1992;
Segura et al., 1999).
When institutional response to the community bug reports was not fea-
sible in distant rural areas, the community inhabitants were trained and
provided with insecticides and equipment to spray the reinfested houses.
For example, in Brazil, the control program recruited ‘local health agents’
who assumed responsibilities to examine all locally collected insects,
inspect reportedly infested houses, apply insecticides and produce monthly
reports (Bryan et al., 1994). In the county of Mambaí, Brazil, the trained
community leaders served as sprayers in the hard-to-reach localities and
contributed to achieve total spray coverage of the infested houses (García-
Zapata and Marsden, 1993). Later, in 1999, elimination of T. infestans was
confirmed in this county (Silveira et al., 2001). Similar strategy was applied
in the Moreno Department, Argentina, where the trained community lead-
ers stored and distributed the insecticides and equipment to villagers who
were in charge of spraying their houses (Vazquez-Prokopec et al., 2009).
The latter experience showed that the control actions by the villagers were
cost-effective and sufficient to maintain low vector infestation. However,
the villagers could not eliminate T. infestans due to loss of adequate spray-
ing techniques, which demonstrates needs of systematised technical sup-
port for the community sprayers (Vazquez-Prokopec et al., 2009).
6.3.2. Central America – IPCA

Surveillance of T. dimidiata, with development of effective strategy, is the
main challenge for Chagas disease control programs in Central America
(Ponce, 2007). Although the vectors and health systems were different
from INCOSUR, the same model is used for the community-based sur-
veillance systems in Central America. In Guatemala, the vector control
program set up triatominae notification posts in the health centers or in
the communities, visited regularly to collect bug reports and responded
by visiting and spraying the infested houses. Such surveillance system
was also typical of T. infestans in South America. In starting this simple
TABLE 6.9 Responsible actors and intermediate agents for vector surveillance in
Central American Initiative
Guatemala Honduras El Salvador
Responsible Departmental Local Health Departmental Vector

management Vector Control Centers Control Program/
unit Program Health Promotion
Unit
Intermediate Chagas disease Community Health promoters,
agents (bug volunteers, health volun- community health
report collec- community teers, schools, volunteers, schools,
tion) leaders, schools NGOs, NGOs, community
community leaders
leaders
Intermediate Community Community Community sprayers
agents (treat- sprayers health
ment of infested (in trial) volunteers
houses) and sprayers
NGO, non-governmental organisation.
model, Guatemala, El Salvador and Honduras also employed multi-sector

coordination to optimise locally embedded resources, especially schools
and community leaders (Table 6.9). There are no explicitly defined surveil-
lance systems in other Central American countries.
The Guatemalan surveillance model was effective for eliminable R.
prolixus, but not for T. dimidiata, when its infestation occurred repeatedly
and extensively. The vector control programs of Central American coun-
tries had been relatively underfunded from the attack phase but expected
even more limited resource allocation in the surveillance phase for alle-
viated vector infestation. Lack of resources in Guatemala, for example,
scaled down the spray coverage by adjusting the response criteria for the
community bug reports. In Honduras, scarce human resources in the vec-
tor control program after the health system reform during the 1990s, local
health centres became responsible for management of the community-
based surveillance system. In El Salvador, the surveillance activities were
shared between the vector control program and the health promotion
program.
6.3.3. Common structures of vector surveillance systems

To achieve interruption of vector-borne transmission of Chagas disease,
most countries implemented both institutional and community-based
surveillance (PAHO, 2003b). These experiences may be extracted and
explained in terms of three structural models (Fig. 6.1), as described by

WHO (WHO, 1997b):
1) The government control program puts special field inspectors in charge
of surveillance in certain areas.
2) Selected community members are provided with materials and trained
to carry out surveillance, keeping the government control program
informed.
3) As part of the PHC approach, some community members are trained as
health workers and become in charge of surveillance and retreatment,
along with other activities.
The institutional surveillance is characterised by entomological investi-
gation, typically the man-hour bug search by trained VCTs of the MoH.
This standardised entomological investigation allows systematic analysis
with relatively limited bias but is costly. The community-based surveil-
lance shares a common framework, where the bugs are reported from the
community directly or indirectly to the MoH and, in turn, the infested
houses (and surrounding houses if necessary) are sprayed with insecti-
cides. Involvement of the community broadens the coverage of vector sur-
veillance and improves sensitivity to detect bug infestation (Abad-Franch,
2011; Abad-Franch et al., 2011).
Among the community-based approaches, the management unit var-
ied from the departmental vector control program to the local health or
PHC service (Fig. 6.1). This variation is attributable to the organisational
structure resulted from the health system reform or decentralisation.
The central program was downsized, shifting the directive and opera-
tional units towards the peripheric MoH offices or into the municipality
service (Tobar, 2006). The idea of transformation was to respond more
efficiently and effectively to the local needs. However, in many Latin
FIGURE 6.1 Basic structures of three vector surveillance systems: institutional surveillance
(left) and community-based surveillance managed by vector control program (centre) and
by local health service (right).
American countries, these reforms engendered controversial features

including untimely and unfair fiscal and managerial decentralisation
without careful consideration of the local capacity (Marquez et al., 2008).
Many communicable disease control programs were affected by institu-
tional fragmentation, discard of goals, loss of expertise, lack of financial
and human resources and, as a consequence, negative epidemiological
impact (PAHO, 2006c).
Along with the decentralisation, community participation has become
an important tool from the early 1980s for the control of tropical diseases,
such as malaria, lymphatic filariasis, Chagas disease and schistosomiasis
(Manderson et al., 1992). Community surveillance, if properly organised,
saves the authorities much work and money and is likely to improve the
quality of control operations (WHO, 1997b). For Chagas disease vector
control, the community-based surveillance is now recognised as an inter-
national issue (PAHO, 2009a).
Experiences suggest that the Chagas disease surveillance systems have
been developed seeking for organisational consistency with the health sys-
tems and for community’s capability on vector control. Detailed analysis
of these experiences will provide more insights to evolve the community-
based surveillance system for Chagas disease. On the basis of the empiri-
cal knowledge, the next two Sections (6.4. and 6.5.) attempt to describe
internal and external factors which can influence sustainability and scal-
ability of the surveillance systems. In each Section, the experiences from El
Salvador and Honduras will be analysed to draw lessons.
6.4. MECHANISM OF COMMUNITY-BASED SURVEILLANCE

SYSTEMS
In the surveillance phase, the core tasks are to sustain surveillance and
retreat any newly detected domestic vector infestation (Dias et al., 2002;
Schofield et al., 2006). The question is how to keep controlling widespread
and low-intensive vector infestation in the most effective and efficient
manner. Experiences in South American countries suggest that vector con-
trol with community participation has significant and sustainable impact
on vector density and is a politically viable strategy (Bryan et al., 1994).
Once the attack phase is completed and the vector infestation is low, the
community-based surveillance has higher sensitivity for vector detection
than institutional surveillance (Abad-Franch, 2011; Abad-Franch et al.,
2011) and is the most cost-effective option (Vazquez-Prokopec et al., 2009).
Such reasons explain why the community-based surveillance has become
the mainstream. This Section 6.4. will dismantle the community-based
surveillance systems to understand how they can continue functioning
within its structure.
6.4.1. Five basic functions

Effectiveness of community-based surveillance depends on three fea-
tures: 1) a system to receive and acknowledge the householder reports,
2) a system to collate the reports with other information of operational and
epidemiological relevance and 3) capacity to implement selective inter-
ventions in response to the reports of individual and/or clustered infesta-
tion (Schofield et al., 2006). Under this principle, each endemic country
has implemented the community-based surveillance (see Section 6.3.). The
operational process generally involves five key functions (Fig. 6.2):
1) Health promotion with instructive information so that the community
can detect and report bugs or human acute cases.
2) Detection of suspected bugs and acute cases in the community.
3) Report of the suspected bugs and acute cases to the health facility.
4) Analysis and planning at the health facility to carry out responses.
5) Response to the report with residual insecticide spraying, orientating
for house and environmental improvement and/or medication.
The community-based surveillance system keeps working as a continuous
interaction between the MoH and the community. It commences necessar-
ily with heath promotion, so that the community members undertake their
roles of searching for bug and acute cases. Then, the surveillance system con-
tinues by repeating the circular actions from the function 2–5. Yet, in order to
sustain the effectiveness, the system requires constant promotional stimula-
tion and quality management. Only when all five functions keep working in
sequence, it is possible to say ‘the surveillance system in function’.
FIGURE 6.2 Five functions of community-based surveillance system.

6.4.2. Stakeholders
In its simplest form, the community-based vector surveillance system
could be operated only between those who find bugs and those who treat
them. For example, in Guatemala, the initial surveillance system involved
only the vector control program and the community. This simple design
contributed to find sporadic foci of R. prolixus and provided effective and
timely intervention. However, when the same surveillance system was
addressed for T. dimidiata, whose domestic infestation occurs far more fre-
quently in time and space, the vector control program faced the limitation
in human and financial resources. The same situation happened when the
South American countries embarked on the surveillance against T. infes-
tans in their vast land. Accordingly, the surveillance systems have needed
to involve more stakeholders who can work as intermediate agents bridg-
ing the vector control program and the affected communities.
For instance, the Southern Cone countries involved multi-sectoral
agents, such as municipal governments, primary schools, police and com-
munity leaders. In Central America, the surveillance systems involved
community health volunteers (CHVs), primary schools, rural health pro-
moters (HPs), health center staff, etc. While Guatemala created purpose-
built community volunteers under the vector control program, Honduras
and El Salvador shared tasks of surveillance systems with the existing
human resources at the local health services. To involve such heteroge-
neous stakeholders, the central question becomes how to share the roles
to operate the surveillance systems.
To simplify the discussion, it is possible to classify these stakeholders
into four categories according to their affiliation and technical capacity on
vector control: vector control personnel, local health personnel, selected
community members and community inhabitants (Table 6.10). Among the
five functions of community-based surveillance system, only the function
4 (analysis and planning) must be undertaken by the institutional person-
nel because this task requires capacity on data processing and uniform
decision making. The function 5 (response to report) also requires techni-
cal capacity but these skills are transferrable in case of vector control to
selected community members by training (e.g. García-Zapata and Mars-
den, 1993; Gürtler et al., 2007). Other functions can be readily shared with
community members.
From the logistics viewpoint, the function 5 (response to report) is a
bottleneck of surveillance system. To spray houses in response to bug
reports, the best quality-oriented method is to mobilise trained person-
nel and equipment from the health facility to the community. However,
often this task faces insufficiency in human resources, transportation and
fuel, which implicate more needs to involve stakeholders and to store
equipment close to the community. Training and technical follow-up are
TABLE 6.10 Potential role distribution among four categorised stakeholders to oper-
ate the community-based surveillance systems
Affiliation Ministry of Health Community
Intermediate agents
Selected
Vector control Local health community Community
Category personnel personnel members inhabitants
Technical capacity High >a >a Low
Potential role distribution

1) Health promotion ✓ ✓ ✓
2) Bug/case detection ✓ ✓
3) Bug/case report ✓ ✓ ✓ ✓
4) Analysis and planning ✓ ✓
5) Response to report ✓ ✓ ✓ b
a These stakeholders need special training on vector control before undertaking roles.
b The effectiveness of spraying by community members is disputable.
ecessary because involvement of non-professional personnel or commu-

n
nity members can cause loss of quality and effectiveness (Vazquez-Proko-
pec et al., 2009; Abad-Franch, 2011).
The more stakeholders are involved in the surveillance system, the
higher management capacity is required. As the functions of surveillance
system are distributed among various stakeholders, the manager need to
coordinate them all, integrate fragmented tasks into effect, monitor the
performance and provide solutions to any operational problems. Thus,
the manager holds total responsibility in operation of the community-
based surveillance system. Identification of appropriate managers is one
of the key issues to maintain the surveillance functioning.
6.4.3. Evaluation of process and results

Actions of the community-based surveillance system should be trans-
lated into the impact on the disease transmission levels. The surveillance
systems can be evaluated in three different dimensions: process, output
and outcome (Table 6.11). Evaluation will offer feedback, validating or
invalidating the implemented surveillance models. Scale of such analysis
is adjustable in time and space. Especially, longitudinal epidemiological
study and geographical comparative analysis by using geographic infor-
mation systems (GIS) will be useful.
Operational process of the community-based surveillance system
may be measured using a performance index, developed in Honduras
TABLE 6.11 Indicators to evaluate the community-based surveillance systems
Dimension Indicator
Process Performance index; geographical coverage

Output Number of houses reportedly infested with vectors; percentage
of houses reportedly infested with vectors (denominator: all
houses in areas with the surveillance system); number of acute
cases; response coverage; time lag between report and response
Outcome Infestation index a; colonisation index b; seroprevalence and
incidence
a Infestation index = number of houses infested/number of houses examined × 100; b colonisation
index = number of houses with nymphs/number of houses examined × 100 (Schofield, 2001).
(see Section 6.4.4.5). A checklist of task completeness by various stake-

holders will systematically identify operational pitfalls that influence
the outputs. The results may be utilized to improve performance of the
surveillance system by adjusting details of role distribution and task
contents. Monitoring of performance index will also provide informa-
tion on epidemiological silence and incomplete or delayed response to
the community bug/case reports. Also, the geographical coverage of
the community-based surveillance system ([number of endemic villages
with surveillance system/total number of endemic villages] × 100) is
fundamental to visualise achievement in scaling-up of the surveillance
systems.
The outputs or short-term production of the community-based sur-
veillance systems need be monitored, analyzing the reports and response
results. The number and percentage ([number of reportedly infested
houses/number of all houses in the areas with the surveillance system]
× 100) of bug reports reflect the trends of domestic vector infestation or
level of community participation in searching or reporting bugs to the
health facilities. The number of acute cases referred by the community will
also be a product of the surveillance, where the local laboratorial network
is capable of detecting T. cruzi. Response coverage ([number of report-
edly infested houses (or acute cases) treated by MoH/number of infested
houses (or acute cases) reported by community] × 100) can show the
response capacity of the installed surveillance systems. Time lag between
bug/case reports by the community and institutional response can also be
useful to measure response timeliness by the health facilities.
The outcome or long-term consequences of the surveillance system is
shown as entomological and epidemiological trends. Changes in the per-
centage of reportedly infested houses or acute cases can provide implica-
tion of changes in real house infestation rates and incidence. Although the
analysis may contain methodological irregularity due to dependency on
the individuals’ behaviors, a constant monitoring on these passive indica-

tors is likely to show some trends in a long run. In addition, these limi-
tations may be complemented by conducting institutional entomological
and serological surveys at sentinel or priority communities. Such fixed
point observation will become more feasible with availability of periodic
and earmarked funding.
6.4.4. Mechanism of community-based surveillance systems

in El Salvador and Honduras
El Salvador and Honduras each selected six pilot sites, where the commu-
nity-based surveillance systems were experimentally introduced in 2008.
El Salvador placed the priority on the areas with human acute cases or
with moderated infestation levels of T. dimidiata after residual insecticide
spraying campaigns. Honduras selected areas with history of R. prolixus
or with over 20% of previous house infestation rate of T. dimidiata.
6.4.4.1. Stakeholders
Figure 6.3 shows structure of the local health systems in which multiple
stakeholders of community-based surveillance systems are distributed.
Both countries have structure of three strata: Department Health Office,
Local Health Center and community.
FIGURE 6.3 Structure of local health systems and stakeholders of community-based

surveillance systems in El Salvador and Honduras.
In El Salvador, VCTs are assigned to the Department Health Office. At

Local Health Center level, environmental health technicians (EHTs) are
in charge of water and food safety, excrement sanitation, solid and bioin-
fectious wastes, etc. HPs are official frontline health workers who realize
monthly house visits addressing all kinds of health-related problems. At
the community level, CHVs are organised to assist HPs in all aspects. Pri-
mary schools participate in health promotion and the trained community
sprayers are available in some communities.
In Honduras, the vector control program was integrated into the Envi-
ronmental Health Program during the health system reform of the 1990s.
EHTs became in charge of vector-borne diseases, zoonosis, food and water
safety and basic sanitary issues. EHTs are allocated in all Department
Health Offices and some Local Health Centers. At the Local Health Center,
the chief physician or nurse manages the community-based surveillance
system. At the community level, CHVs bridge the Local Health Center
and the community. Trained community sprayers are available in most
communities with the surveillance system.
6.4.4.2. Role distribution

Table 6.12 shows role distribution within the mechanism of community-
based surveillance systems in El Salvador and Honduras. In both coun-
tries, the managerial and operational tasks are shared among the vector
control personnel, local health personnel, selected community members
and community inhabitants.
In El Salvador, the VCTs at the Department Health Office are respon-
sible for managing and supervising the whole process of the commu-
nity-based surveillance system. In Honduras, the manager is chief
physician or nurse in the Local Health Center, who organises monthly
meetings with CHVs to discuss all relevant health-related issues, includ-
ing surveillance of Chagas disease. The vector control personnel in
Honduras (EHT) is not in principal charge of managing nor operating
the surveillance systems but of providing technical or logistic support
to local health center (e.g. data analysis, planning, training of commu-
nity sprayers, provision of insecticides, maintenance of spraying equip-
ments).
From operational perspectives, key intermediate agents are HPs in El
Salvador and CHVs in Honduras. They are involved in the functions 1, 3
and 5 (health promotion, bug/case report and response to report). Only
in El Salvador, the HPs are expected to be responsible for the function
4 (analysis and planning). Their main strength is homogeneity with the
community since they are recruited among the community inhabitants.
They often have inherent communication skills and are capable of learn-
ing vector control techniques such as spraying.
TABLE 6.12 Mechanism of community-based surveillance systems in El Salvador and

Honduras
Country El Salvador Honduras
Management unit Department Health Office Local Health Center
Functions Stakeholders and roles

1) Health promotion HPs (under VCTs’ CHVs encourage
orientation) encourage community inhabit-
community inhabitants ants to search bugs
to search bugs during irregularly. School
regular house visits. teachers and Health
School teachers orient Center staff help
children annually occasionally
2) Bug/case detection Community inhabitants Community inhabit-
search for bugs and ants search for bugs.
human cases. Schoolchil- Schoolchildren
dren participate participate
3) Bug/case report HPs receive bugs in house Community inhab-
visit and refer suspected itants take bugs
cases to Health Center to Health Center
directly or via CHVs
4) Analysis and planning HPs analyse community Health Center staff
reports to identify analyse community
villages with high vector reports to identify
infestation and human villages with high
cases vector infestation
5) Response to report HPs or EHTs provide CHVs provide 1) house
1) entomological verifica- visit for bug search,
tion, 2) educational advice 2) orientation for
or 3) spraying under super- house improvement
vision of VCTs. Commu- or 3) spraying in
nity sprayers are organised coordination with
if necessary. Physicians EHTs. Community
diagnose and treat the sprayers are organ-
patients if necessary ised if necessary
CHV, community health volunteer; EHT, environmental health technician; HP, health promoter; VCT,
vector control technician.
For the function 1 (health promotion), local primary schools also have a
significant role in both countries. In Central America, the primary schools
are widely distributed even in rural areas with access difficulties. The
primary schools provide a channel through which the information could
be diffused among schoolchildren. In El Salvador, the MoH concluded a
c onvention with the Ministry of Education, so that the curriculum for the
sixth grade of schoolchildren would involve orientation for prevention
and control of Chagas disease. Furthermore, the primary schools annually
celebrate ‘Chagas Day’ (July 9) to intensify promotional activities.
For the function 3 (bug report), the channels of the bug transportation
from the community to the health facility are well defined. In El Salvador,
HPs receive captured bugs during their monthly visits to the houses and
schools, although the villagers also take the bugs to the Local Health Cen-
ters on occasions. In Honduras, CHVs receive bugs and transfer them to
the Local Health Centers.
For the function 5 (response to report), the HPs and CHVs are oper-
ational main actors in each country. When necessary, the community
sprayers are trained and organized to spray more infested houses in both
countries (see Section 6.6.1). To assure the quality of spraying by non-
professional cadres, spraying actions are supervised. In El Salvador, VCTs
lead and supervise HPs in whole process of responsive control activities,
while in Honduras, EHTs provide occasional advice and supervision to
the Local Health Centers.
6.4.4.3. Response criteria

In El Salvador, the local health facility must provide response for every bug
report within according to the national norm 7 days according to the national
norm (Ministerio de Salud de El Salvador, 2011). The response includes
three options: entomological verification, educational advice and spraying.
Criteria to choose one of these response options are not strict in the national
norm. Instead, the decision depends on the HPs’ analysis, taking account of
the availability of materials, time and house infestation levels.
In Honduras, the institutional response involves three activities: house
visit for bug search, orientation for house improvement and spraying.
One of the responses is to be provided to every community bug report.
Although the selection criteria are not strictly defined, insecticide is gener-
ally applied to houses with high bug density or with nymph bug popula-
tions, indicating possibilities of indoor colonisation. If the percentage of the
infested houses exceeds 20% within a community, all houses are eligible for
insecticide spraying. For communities below 20% of house infestation rates,
only infested houses are sprayed (Secretaría de Salud de Honduras, 2010).
6.4.4.4. Emergent cases

In case of emergencies, such as report of human acute cases or R. prolixus,
direct actions are taken by the VCTs in the two countries (Table 6.13). In El
Salvador, VCTs investigate directly the causal environments of acute cases
and spray the infested and neighboring houses. In Honduras, reports of
suspected R. prolixus are dealt with by the departmental coordinator of
TABLE 6.13 Control actions for report of acute cases or Rhodnius prolixus
Functions Stakeholders and roles

4) Analysis and Physicians and laboratories in Departmental EHTs
planning Local Health Center confirm confirm R. prolixus and
acute cases and refer them to the make decisions for
departmental hospital for further response
examinations. Departmental
VCTs immediately investigate
and spray the patient’s house
5) Response to Departmental VCTs carry out Community sprayers
report focal spraying. Physicians carry out the spraying
provide medical treatment under supervision of
EHTs
EHT, environmental health technician; VCT, vector control technician.
EHT by visiting the reported house with the municipal EHT. If the sus-
pected bug is confirmed as R. prolixus, insecticide spraying is organized
immediately by the EHTs with the local community sprayers. Since R. pro-
lixus is subject to elimination, insecticide spraying will cover all houses in
the infested community as well as adjacent communities.
6.4.4.5. Evaluation
Table 6.14 shows output and outcome of the community-based surveil-
lance systems which were implemented in the pilot sites of El Salvador
and Honduras. Although some data are missing in the experimentally
measured output and outcome, the available indicators show its potential
applicability for evaluation of surveillance.
In El Salvador, the response coverage was 100%, but not meaning
that all reportedly infested houses were sprayed. According to national
norm, the response can be any of entomological verification, educational
advice and spraying. As HPs are obliged to visit all houses every month
in their catchment areas for general purpose, automatically HPs visit all
reported houses and can provide at least educational advice. In this case,
the response coverage should be broken down by the types of response.
In Honduras, the time lag between report and response varied from 1
week to 16 months. The quickness of responsive control action depends
on the gravity of the reported problem and on the institutional capacity
of the Local Health Center to organize control actions. The response was
provided individually in a relatively short term in some areas or collec-
tively after accumulating the bug reports for certain periods in others.
TABLE 6.14 Output and outcome of the community-based surveillance systems in

pilot sites, El Salvador and Honduras
Output Number of reported houses Number of reported houses

(2009–2010): (2009–2010): T. dimidiata = 466,
Triatoma dimidiata = n/a, Rhodnius prolixus = 1
acute cases = n/a
Percentage of reportedly Percentage of reportedly infested
infested houses by houses by T. dimidiata
T. dimidiata (2009–2010): (2009–2010): 6.5% (466/7224)
n/a%
Response coverage Response coverage
T. dimidiata: n/a% sprayed T. dimidiata: 63% sprayed
100% visited for education n/a% visited for education
Acute case: 100% sprayed R. prolixus: 100% sprayed
Time lag between report and Time lag between report and
response: T. dimidiata: response: T. dimidiata: 1
1 week ≤; acute case: 24h month≤; R. prolixus: 24h (vector
(house visit), 1 week confirmation), 1 week to 16
(spraying) months (spraying)
Outcome House infestation index for House infestation index for
T. dimidiata: n/a T. dimidiata: n/a
Seroprevalence: n/a Number of communities with
R. prolixus: 24 (2003–2006), 1
(2009–2010)
Incidence: n/a Seroprevalence among children
under 15 years old:
3.1% (130/4162) (2004–2007),
0.4% (15/3611) (2010)
n/a: data not available.
Data source: Ministry of Health in El Salvador and Honduras
Functional performance of the surveillance system was monitored

in the six pilot areas in Honduras, having developed an original mea-
surement checklist. Four administrative levels (central program, depart-
mental health office, municipal health center and community) are to
be evaluated every 6 months whether each accomplished their tasks to
operate the surveillance system. A total of 48 items were answered by
‘yes’, ‘no’ or ‘not apply’, including interrelated (e.g. information flow,
material provision) and independent issues (e.g. risk map update, bug
identification).
FIGURE 6.4 Performance index of the community-based surveillance system in six pilot
sites in Honduras 2009–2010.
This process evaluation allowed visualizing the progress along the

implementation of the surveillance system and identifying specific tasks
to improve. In the six pilot sites of Honduras, the average performance
index gradually increased from 46%, 73%, 77% to 83% through March 2009
to August 2010 (Fig. 6.4). Most difficult challenges were regular updates
of risk map and timely response to the reports. These less achievable tasks
may be simplified, shared with more stakeholders or even eliminated if
possible. The process evaluation can provide opportunities to improve the
performance and motivate the stakeholders, especially when it is comple-
mented with field visits and person-to-person communication to validate
the operational activities.
6.5. HEALTH SYSTEMS AND COMMUNITY-BASED

SURVEILLANCE SYSTEMS
For the community-based surveillance systems to be sustainable and scal-

able, influences from surrounding environments should be examined.
With the health system decentralisation, Chagas disease control program
no longer could maintain itself in a vertical manner, namely, with ear-

marked resources and an independent chain of command. The commu-
nity-based surveillance systems must be administered with influences
from outer environment, that is, general health systems.
Yamagata and Nakagawa (2006) pointed out that integration of the
surveillance activities for T. dimidiata into general local administration is
a key challenge in Central America to cover most geographical areas in a
sustainable basis. Similarly, integration of the vector or case surveillance
into the local health service is recognised as an important future strategy
throughout Latin American countries (Aguilar et al., 2007; Chuit et al.,
1992; Gürtler et al., 2007; Moncayo and Silveira, 2009; Schofield et al.,
2006). With the integration, it is expected that the surveillance 1) would
be expanded to larger geographical areas through existing health
structures and 2) would be sustained as one component of local routine
health services. Central question is how the community-based surveil-
lance systems for Chagas disease can be integrated into the general
health systems.
6.5.1. Viewpoints to analyse program integration

Integration is currently a common interest in the public health. After the
controversy of vertical versus horizontal approach (Oliveira-Cruz et al.,
2003), the integration of disease-specific programs into general health
systems has become one of the main challenges in major communicable
disease control such as HIV/AIDS, tuberculosis and malaria (Atun et al.,
2010a). The benefits of integration are considered to be variable, includ-
ing improvement of effectiveness, efficiency, sustainability, accessibility or
user’s satisfaction (Shigayeva et al., 2010). To facilitate understanding of
the logic and related factors, conceptual and analytical frameworks have
been developed (Atun et al., 2004, 2010b; Coker et al., 2010). So that, the
degree of integration can also be comparatively visualised (Atun et al.,
2009). This Section 6.5. will employ the comparative analysis model con-
structed by Coker et al. (2010) to examine the integration of Chagas dis-
ease community-based surveillance systems into general health systems
(Fig. 6.5).
Linking to the mechanisms to provide interventions, this model
describes six health system functions: 1) stewardship and governance,
2) financing, 3) planning, 4) service delivery, 5) monitoring and evalua-
tion and 6) demand generation. These functions are the focus of analyses
of integration between health systems and disease control programs. In
this model, the term ‘integration’ represents a spectrum of organizational
arrangements related to the funding, administration, organisation, service
delivery and clinical scenarios designed to create connectivity, alignment
and collaboration (Coker et al., 2010). Using six health system functions,
FIGURE 6.5 Comparative analysis model by Coker et al. (2010) applied on Chagas disease
vector surveillance. *Details of health system functions can be found in Atun et al.
(2009, p. 4).
the following section examines the level of integration of Chagas disease

surveillance systems in El Salvador and Honduras.
6.5.2. Integration of community-based surveillance systems in El

Salvador and Honduras
El Salvador and Honduras implemented the community-based surveil-
lance systems on an experimental basis in 2008. Implementation began
with designing of the basic structure and continued with empirical
trials, adjustment and modification of the design to fit into the sur-
rounding environment. By 2010, the surveillance systems became
administrated through the existing local health services in both coun-
tries (Table 6.15).
To develop integrated model of surveillance, participatory approach
was crucial. For example, in El Salvador, role distribution was discussed
among various stakeholders from three administrative levels: Local
Health Center (physicians, nurses, EHTs, HPs and laboratory techni-
cians), Department Health Office (epidemiologists, coordinator of HPs
and VCTs) and the National Vector Control Program (program coordina-
tor). Through the discussions facilitated by Japan International Coopera-
tion Agency (JICA), bug collection and response by HPs were identified as
vital tasks. The identified tasks were aggregated into HPs’ job profiles and
TABLE 6.15 Integration of the community-based surveillance system at operational

level in El Salvador and Honduras
Health system
functions El Salvador Honduras
Stewardship and • Chiefs and HPs of Local • Chiefs of Local Health

governance Health Centers are directly Centers are directly
accountable for perfor- accountable for perfor-
mance of surveillance mance of surveillance
system system
• ETVs are responsible for
training and supervision
of surveillance activities
Financing • Operational activities are • Ordinary operational
financed by regular Health activities are financed by
Center budgets regular Health Center
• Spraying equipments, budgets
insecticides and educa- • For special events such
tional materials for Local as celebration of Chagas
Health Centers are sup- disease day, funds are
plied from Central Chagas negotiated with local
Disease Control Program government budgets,
via Department Health NGOs, etc
Office • Spraying equip-
ments, insecticides and
educational materials for
Local Health Centers are
supplied from Central
Chagas Disease Control
Program via Department
Health Office upon formal
request
Planning • Surveillance actions are • Local Health Centers
integrated into annual analyse data, set priorities
operation plans of the and allocate resources
Health Centers, HPs and in annual action plans
VCTs in coordination with
• HPs analyse bug reports Department Health Office
and plan response with
guidance of VCTs
(continued)
Health system
Service delivery • Regular house visits by • CHVs often take bugs

HPs and occasional house to Local Health Center,
visits by ETVs include when they attend monthly
health education, bug meetings
collection and response • Insecticide spraying
• Community sprayers are organised by Local Health
trained for insecticide Centre staff and CHVs
spraying by HPs and/or at monthly meeting and
VCTs, when necessary carried out by trained
• At Local Health Centers, CHVs or community
spraying equipment and sprayers
insecticide are controlled
• At Local Health Centers,
by HPs (under supervision spraying equipment and
of ETVs) and repaired by insecticide are kept and
VCTs leased out by physicians
• Laboratory technician or nurses and repaired by
at larger Local Health EHTs
Centers diagnose acute • Local Health Centers refer
cases suspected acute cases
• Physicians at Local Health to Department Hospital
Centers provide medical Laboratory
treatment • Physicians at Local Health
Centers provide medical
treatment
Monitoring and • Vector house infesta- • House infestation
evaluation tion, response by health and response data are
education and spraying registered on paper for-
and acute case data are mats at Local Health enter
resisted in the national and shared at monthly
online information system meetings with CHVs
at Local Health Centers • Summarised house
• Surveillance performance infestation and response
of Local Health Center is data are sent monthly to
monitored by Departmen- the Departmental EHTs
tal HPs • Surveillance performance
of Local Health Center is
monitored by Departmental
EHTs
(continued)
Health system
Demand • Bug/case search and • Bug/case search and report

generation report are promoted by are promoted by Local
HPs (with orientation of Health Center staff through
ETVs) during their regular CHVs
house visits • Local Health Centers
• Local Health Centers share relevant information
share relevant information through different local
through different local network
network • Villagers have right and
• Villagers have right and access to insecticide
access to insecticide spraying at Local Health
spraying, diagnosis and Centers
medication with Local
Health Centers
CHV, Community health volunteer; EHT, environmental health technician; HP, health promoter;
NGO, non-governmental organisation; VCT, vector control technician.
monthly data reporting formats. In Honduras, at first, the National Cha-

gas Disease Control Program presented a provisional guideline with role
distribution to the Department Health Offices (director, epidemiologists
and coordinators of EHTs). The departmental coordinator of EHTs in turn
oriented the Local Health Center staff with support of the National Cha-
gas Disease Control Program and JICA. At this point, the management of
the surveillance system was introduced as a part of the routine health ser-
vice. Then, in quarterly workshops, experience-based progress, problems
and lessons were presented and discussed among the multi-level stake-
holders. Through this process, the role distribution became clearly defined
and agreed among the stakeholders.
To strengthen the integration at the operational level, adjustments were
required also at the upper administrative levels. In El Salvador, the com-
munication within Department Health Office was often stagnant nodule.
For instance, occasionally, acute cases reported to the Department Health
Office were not transmitted immediately to the Departmental Vector Con-
trol Unit and so left unattended for vector control actions for some time. At
the departmental level, the Vector Control Unit is administratively posi-
tioned under the Department Health Office, however, technically depends
on the National Vector Control Program. Conserving some vertical cul-
ture even after the health system reform, the Departmental Vector Con-
trol Units tend to respond to the National Vector Control Program rather
than the Department Health Offices. This vertical dependence may have
hindered the horizontal communication. On the other hand, the Health
Promotion Units created after the health system reform are integrated
into the Department Health Offices. Technical coordination between the
Health Promotion and Vector Control Units contributed in improving the
horizontal coordination. When the HPs perceived needs of control actions,
the departmental coordinators of HPs established direct communication
with the Departmental Vector Control Units to obtain technical assistance.
In Honduras, in attempts to integrate the vector surveillance system
into the local health service, the operational responsibility was shifted
from Departmental Health Office to local Health Centers. Initially, the
Departmental Health Offices received and analyzed the community bug
reports. However, the distance between the Departmental Health Offices
and communities created time lag in responding to the reports, leading
to demotivation among the inhabitants and to gradual decrease in the
number of community reports. To shorten the time lag, the Health Cen-
ters were equipped with spraying equipment, insecticide and registry for
community reports and response, and were allowed to make decisions
over institutional response. This transference of responsibility took place
with agreement and support by the director of the Departmental Health
Offices. Provision of the necessary equipment and partial authority to the
Health Centers increased the community reports and response coverage,
as well as ownership of the Health Center staff. The Departmental Health
Office, in turn, took role of supervision in coordination with the National
Chagas Disease Control Program. The operation of vector surveillance
was monitored through the monthly reports from the Health Centers to
the Departmental Health Office and later to the National Chagas Disease
Control Program. Along with the involvement of Heath Centers, the mon-
itoring of work process and quality by upper authorities was necessary.
The performance checklist (see Section 6.4.4.5.) facilitated to standardize
surveillance operations and checkpoints for supervision.
Integration seems critical to increase scalability and sustainability of
surveillance systems, but there is no rule without exceptions. In case of
emergency, such as report of acute cases in El Salvador and R. prolixus in
Honduras, the response needed to be organized vertically. In El Salvador,
the special team was formed among the national and departmental vector
control programs to visit the reported houses for epidemiological causal
investigation. Similarly, in Honduras, the National Chagas Disease Con-
trol Program and the Departmental Environment Health Unit visited the
reported houses for confirmation and technical observation. Such verti-
cal organization enables quick on-the-spot inspection with high expertise,
preventing loss of information, as well as human infection or vector infes-
tation. The community-based surveillance systems should have flexibility
and capability for vertical organization in case of emergency.
6.6. CHALLENGES
6.6.1. Challenges for further evolution of surveillance systems

The surveillance systems should evolve continually to increase the geo-
graphical coverage and sustainability. After the attack phase against
T. infestans in Brazil, the challenges in the surveillance phase were mainte-
nance of political will and community interest, integration of vector con-
trol into other activities and quality assurance at peripheral level (Dias,
1991). These challenges are still relevant today, even when the target vec-
tors are extensively distributed and non-eliminable, as in the case of T.
dimidiata in Central America. In facing the challenges, three key strategies
can contribute through evolution of surveillance systems: involvement of
multiple stakeholders, adjustment of response criteria to the community
bug reports and combination with campaign-style intervention.
6.6.1.1. Multiple stakeholders

Firstly, more stakeholders need be involved at the local health facilities and
at the community to control a lager number of infested houses (Fig. 6.6).
Under decentralized health systems, the number of institutional person-
nel is not sufficient to provide timely control actions to all reportedly
infested houses. Involvement of more locally embedded actors is a key
to increase response coverage of the community-based surveillance sys-
tems. Furthermore, this strategy contributes to reduction of institutional
cost and to increase local awareness of disease prevention. Identification
and involvement of more stakeholders will back up scaling-up of the sur-
veillance systems and enhance sustainability of vector control strategies
(Gürtler, 2009).
FIGURE 6.6 Relationship between coverage of surveillance systems and number of

involved stakeholders.
A concern with involvement of locally embedded actors is quality

of spraying activities, including maintenance of spraying equipment,
adequate use of insecticide and information management. Minimum
quality should be assured systematically because lack of skills in non-
professional sprayers may affect the effectiveness of vector control. Hon-
duras, for instance, experimentally implemented a quality checklist for
community sprayers to monitor 10 technical requirements. Occasional
quality monitoring by the municipal, departmental and central levels
seems to assure the minimum spraying techniques. Conventionally,
the insecticide spraying needs well-trained professional sprayers due
to its specialized and standardized techniques (Schofield, 2001; WHO
1997a,b, 2006, 2007b). Simplification of spraying techniques and tools
may be an innovative leverage to lower technical barriers and increase
response coverage.
6.6.1.2. Response to the community

Secondly, the response to the community bug reports needs to be improved
in terms of cost, coverage and time. The visibility of intervention is cru-
cial to maintain community participation (Manderson et al., 1992). Abad-
Franch et al. (2011) insist on a timely and professional response to every
report and Schofield et al. (2006) propose an annual cycle of selective
interventions in response to the accumulated reinfestation reports. The
former seems unfeasible due to limited institutional resources in Central
American contexts. The latter might discourage community inhabitants
who generally expect immediate spraying by the MoH as a return. There
is a need to set response criteria which strike the supply-demand balance
between institutional available resources and community reports. The
response criteria can be adjusted in three aspects: type of response, target
areas and frequency.
As types of response, insecticide spraying and educational house visit
have been common in El Salvador and Honduras. While insecticide spray-
ing is more effective but costly, educational house visit has been practiced
as an economical alternative. The educational visits may encourage the
community inhabitants and keep the community-based surveillance
active. However, its impact on vector population is uncertain because
the effects of control actions depend largely on residents’ behaviors. Edu-
cational house visits can increase response coverage by involving more
stakeholders and reducing institutional cost, but the long-term effects
should be evaluated in terms of vector infestation and human infection.
Blood sampling to test seropositivity can be an option of response to bug
reports but has never been practiced in Central America.
Target areas can be selected for response. For example, houses infested
with nymphs are eligible of insecticide spraying, while those with adults
are occasionally visited for preventive education and orientation. In

assumption, the nymphs are unable to fly from outside the house and
hence imply the presence of domestic colonisation. These criteria derive
from the regional control objective: elimination of the domestic colonisa-
tion of T. dimidiata. Other criteria can be house infestation levels. For exam-
ple, only when the percentage of reportedly infested houses reaches 20%,
the spraying is programmed in the whole community. Such artificial selec-
tion of target areas may be useful for concentrating resources in high-risk
areas; however, it may leave unattended resurgence of vector-borne dis-
ease transmission in other areas.
Frequency of response can be varied. Immediate response is ideal
but requires individual action to each report, maximising logistic cost.
To economize time and resources, collective response is an option after
accumulating community reports for a determined period. The longer
is the period to accumulate data, the more efficient will be the response
activities. However, delayed response could discourage the community
inhabitants and produce a chance of T. cruzi transmission.
6.6.1.3. Campaign
The third strategy is organisation of annual campaigns. The MoH calls the
communities for intensive bug search and report for a short period and
all reports are responded with insecticide spraying. For example, Para-
guay organised ‘Chagas week’ in five departments in 2009. About 50,000
schoolchildren participated in the bug collection and detected 30 vector
foci, including four of T. infestans (PAHO/WHO, 2011). Similar campaign
was organised in the Department of Jalapa, Guatemala, in 2007, which
discovered two foci of R. prolixus after five years of absence (Nakagawa,
2009). Such campaign-style intervention is effective to update vector
distribution maps in extensive areas as well as to increase community’s
awareness, political attention and accordingly necessary resources, at
least temporally.
6.6.2. Challenges for regional strategies

The regional initiatives have facilitated the progress of Chagas disease
control of the member countries, providing the clear objectives, oppor-
tunities for technical information exchange, monitoring through annual
meetings, evaluation missions and international certifications. While these
technical and political supports should continue, the strategic focus of the
initiatives must be updated towards sustainable control of autochthonous
species and infected human cases.
In 2010, the WHO/PAHO developed a regional strategy and action
plans at the 146th Session of executive committee (WHO/PAHO, 2010a)
and 50th directing council (WHO/PAHO, 2010b). This strategy contains

two general goals: 1) to interrupt domestic vector borne, transfusional and
other types of T. cruzi transmission in all subregions of the America and 2)
to reduce morbidity and mortality by improving access to health services
for infected people and increase the coverage of diagnosis, quality of med-
ical care and timely treatment of cases. Table 6.16 extracts the contents of
the strategy in relation to the vector control. To put the strategy in practice,
four key issues are considered important.
Firstly, to judge interruption of vector-borne transmission, the
active transmission by autochthonous species should be monitored at
the regional level. That is, parasitological data of acute human cases
should also be collected in addition to serological data of chronic cases.
Although serological surveys with younger generation will capture the
trends of recent transmission levels, infection may have occurred at any
moment in the seropositive individuals’ life time. The most recent and
active vector transmission can be detected through acute case, as seen in
the surveillance of El Salvador. The local health service with basic labo-
ratory apparatus and a trained technician can implement parasitologi-
cal tests with little additional cost. Increased coverage of parasitological
diagnosis in endemic areas will provide a more accurate map of the epi-
demiological situation. Combination of parasitological and serological
data can consolidate more evidence-based evaluation by the regional
initiatives.
Secondly, the regional initiative could arrange systematic learning
from experiences of surveillance systems to accelerate scaling-up and
to improve efficiency. Practical knowledge can be documented from
TABLE 6.16 Regional strategy for the control of vector-borne transmission of Chagas
disease
Objective Indicators Tasks
To interrupt the vector- • Indoor infestation • Eliminate allochthonous

borne transmission of index of less than 1% triatominae species
Trypanosoma cruzi in for specific triatominae • Prevent transmission to
intra-domestic areas species human where autochtho-
• Seroprevalence of less nous triatominaes (either
than 1% in children domestic or wild species
under 5 years that have colonized or
• No acute cases due to infested dwellings) are
vector-born transmis- present
sion in intra-domestic
areas
Source: WHO/PAHO (2010a).
s uccessful experiences and can also be shared through the regional meet-
ings. The framework for data collection and analysis (see Tables 6.11 and
6.14) will be useful for comparing and evaluating the surveillance sys-
tems. Furthermore, cross-bordering field visits to the actual practice sites
will allow learning from the key persons on the implicit experiences and
knowledge, not explicitly presented or documented.
Thirdly, decent investment is necessary to achieve the regional goals.
Often, the endemic countries are underfunded to assure the scaling-up of
surveillance systems as well as to carry out outcome evaluations. Once
scalable and sustainable surveillance models are developed at a small scale,
strategic scaling-up plans can become sales products for funders, includ-
ing national political decision makers and external donors. The regional
initiative may facilitate regional funding schemes, bridging the funders
with the prepared countries. Also additional investment could strengthen
cross-broader surveillance where the vector reinfestation is persistent,
especially at the Gran Chaco region between Argentina, Bolivia and Para-
guay and the border area of Guatemala and El Salvador.
Finally, the rule of international certification by the initiatives could
be modified. Where the autochthonous vectors can infest the domestic
areas, the vector-borne transmission can re-emerge anytime after insec-
ticide treatment. Thus, the certification of interrupted transmission
at a certain time point is not guaranteed in the long run. In this case,
the certification rule should admit reversibility; the emitted certifica-
tion can be invalidated in case of recurrence of the disease transmis-
sion. This reversible approach is regulated in the certification rule of
foot-and-mouth disease (Aphtae epizooticae) and may show effects on
retaining the political interest even after the certification. Besides, as
the autochthonous vectors are widespread, country-level certification
is less achievable in the short term, which may discourage the politi-
cal decision makers or funders. To attract more political will and fund-
ing, the unit of certification can be divided into smaller scales, such as
departmental and provincial levels.
6.6.3. Development of ecological approach

Among ecological vector control approaches, house improvement has been
the most common method to reduce domestic vector infestation (Rojas de
Arias, 2001; Cecere et al., 2002; Monroy et al., 2009). Since domestic vector
infestation is associated with cracked mud walls, mud floors and domestic
animals living inside the house (e.g. Bustamante et al., 2009), actions have
focused on removing of these risk factors. The frequently used technique
is wall plastering in such a way to ensure smooth, flat and crack-free walls
(Rojas de Arias et al., 1999; Cecere et al., 2002). In Guatemala, the research-
ers found that the wall plaster with mixture of one part local soil (clay)
and three parts sand is effective for the control of T. dimidiata reinfestation
(Monroy et al., 2009).
However, house improvement is not a magic bullet that can replace
the insecticide spraying. In Bolivia, house improvement alone could not
eliminate domestic vector populations (Guillen et al., 1997). Without
behavioral changes of the residents, physically improved houses could
be repeatedly infested. Behavioral changes are often difficult even within
well-supported programs with a high level of community participation
because not all individuals may comply (Manderson et al., 1992).
For cost-effectiveness, while economical rationale is established for
insecticide-based intervention (Schofield and Dias, 1991), house improve-
ment remains less attractive. In some cases, house improvement was 24
times more costly than insecticide spraying (Rojas de Arias et al., 1999).
The Guatemalan approach above costs around US$ 30.0 per house, while
insecticide spraying costs US$ 8.0 (Monroy et al., 2009). In view of scal-
ability, the house improvement approach seems less scalable because of
high contingency on local context. In each intervention area, it is necessary
1) to identify locally acceptable construction design and technology and
2) to develop strategies to finance local costs (Bryan et al., 1994). Thus, the
house improvement approach is considered costly and difficult to imple-
ment on a large scale (Guillen et al., 1997; Schofield and Dias, 1999).
Indeed, the experience in Venezuela resumes operational obstacles of
house improvement, including limited human and economic resources,
situational and psychosocial factors that lessen local appreciation for the
value of good housing and cumbersome logistics because of widely dis-
persed housing (Bryan et al., 1994). In Guatemala, the VCTs of MoH were
appointed as technical disseminator and logistic coordinator; however,
this task was time-consuming and few houses could be improved. Prog-
ress will largely depend on the availability of local resources and the inter-
est of the community.
Besides house improvement, environmental management is also pro-
posed. In a Costa Rican trial study, all sorts of disorderly objects were
removed from infested peridomestic areas to modify artificial ecotopes
that served as hiding and breeding sites for T. dimidiata (Zeledón and
Rojas, 2006). This approach demonstrated reduction of vector infestation
and was reliable and sustainable after 4–5 years (Zeledón et al., 2008). A
Mexican trial study showed that the cleaning of houses by itself could
reduce vector infestation but not as effectively as insecticide application
(Wastavino et al., 2004).
So far, none of the ecological approaches can control vector infestation
completely. The ecological approach should still be considered comple-
mentary to the conventional insecticide-based approach. For its wider
application, further research is required focusing on not only technical but
also economic and logistic dimensions .
6.7. SITUATIONS OF OTHER INITIATIVES
6.7.1. Latin America

Since establishment of the Andean Initiative IPA in 1997 (see Section
6.1.), Colombia, Ecuador, Peru and Venezuela have made limited prog-
ress in vector control and surveillance. Among four main target vectors:
R. prolixus, R. ecuadoriensis, T. dimidiata and T. infestans (IPA Homepage,
PAHO, 2006a), R. prolixus is epidemiologically the most important species
(Guhl, 2007). Unlike in Central America, R. prolixus is never likely to be
eliminated by house insecticide spraying due to its sylvatic populations
(Sanchez-Martin et al., 2006). On the other hand, T. dimidiata is a viable
candidate for elimination in Ecuador and Northern Peru (Guhl, 2007).
Progress has been made in Colombia and Ecuador in stratifying risks of
vector-borne transmission (Guhl and Vallejo, 1999; Moncayo and Silveira,
2009). Venezuela has successfully reduced vector-borne transmission
but faced the common challenge: maintenance of effective control with
reduced resources and central management (Feliciangeli et al., 2003). In
Peru, the Department of Moquegua was certified for the interruption of
the disease transmission by T. infestans in 2010 (PAHO, 2010 a). In general,
the vector control in the Andean region has progressed slowly and its geo-
graphical coverage is still limited (Guhl, 2007).
In the Amazon region initiative, AMCHA, launched in 2004 by
Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Peru, Suri-
name and Venezuela (see Section 6.1.), 4 triatominae species (R. robustus,
R. stali, Panstrongylus geniculatus and P. herreri) among the 24 reported
are considered as important control candidates because of their domestic
habitat or frequent invasion of human dwellings from sylvatic ecotopes
(Ecosalud/IDRC, 2006). Continuous and low-intensity transmission gen-
erate a hypoendemic pattern with seropositivity rates of about 1%–3%
(Aguilar et al., 2007). General epidemiological surveillance detected sev-
eral acute cases (Coura and Dias, 2009) and focal intensive transmission
with evidences of oral transmission (e.g. urban outbreak in Brazil (Pinto
et al., 2009)). New patterns of land occupation and globalization might
have contributed to the increase of autochthonous human cases since the
1970s (Briceño-León, 2007). Such irregular entomological and epidemio-
logical patterns generate high uncertainty in designing the intervention
strategy and may hinder the control activities. The Amazon initiative is
recognised as being at an initial phase of creating epidemiological and
methodological knowledge (Moncayo and Silveira, 2009). No specific
goals have been established regarding interruption of vector-borne trans-
mission or vector elimination (PAHO, 2009a). Needs for more research
have been repeatedly called out (PAHO, 2005a,b; PAHO, 2006a; Aguilar
et al., 2007; PAHO, 2009a).
In Mexico, there are 30 species of triatominaes among which 9 of

Triatoma genus are considered as important vectors. The major vectors
are distributed mainly in the central and southern states, including the
concentrated distribution of T. dimidiata in Yucatan Peninsula (Cruz-Reyes
and Pickering-López, 2006). Accordingly, prevalence of Chagas disease is
the highest in the Pacific Coast states of the Yucatan Peninsula and in some
areas of the central part of the country (Moncayo and Silveira, 2009). Sero-
prevalence among blood donors is 2.03% in 1978–2004 (Cruz-Reyes and
Pickering-López, 2006) and 0.41% in 2009 (PAHO, 2010c). The coverage of
blood screening increased from 36.34% in 2005 to 82.10% in 2009 (PAHO,
2010c). In spite of approval of mandatory law in 2000 (Guzmán-Bracho,
2001), full screening is not achieved. Control of triatominaes is considered
to have benefited from malaria eradication campaigns with residual insec-
ticide spraying since the 1950s, leading to the certification of absence of
R. prolixus in 2009 (Salazar et al, 2010; Hashimoto and Schofield, 2012). Still,
the Mexican MoH needs to develop the surveillance system to continue
monitoring the areas with the history of R. prolixus and to better under-
stand the endemic situations with other vector species (PAHO, 2009b).
6.7.2. Non-endemic countries

With substantial increase in global human movements, Chagas disease
became an inevitable issue for epidemiological surveillance among coun-
tries outside Latin America. It is estimated that at least 19.2 million Latin
Americans immigrants live in North America, Europe and Asia, of which
more than 436,000 are infected with T. cruzi (Table 6.17). Establishment of the
non-endemic countries initiative was proposed to eliminate the disease by
1) diagnosing, managing and treating patients, including infected new-
borns from congenital transmission, 2) preventing transmission by screen-
ing blood transfusion and organ transplantation, 3) sharing information
about Chagas disease and training health personnel to facilitate diagnosis
and medical care (WHO, 2010).
Among the non-endemic countries, United States records the high-
est number of Latin American immigrants and according Chagas disease
patients. Since 1970s, sporadic Chagas disease cases have been reported,
including imported acute cases and transfusion-related or transplantation-
related cases (Kirchhoff and Neva, 1985; Kirchhoff, 1993; Cimo et al.,1993;
Leiby et al., 1999; Centers for Disease Control and Prevention, 2006, 2007).
In 1987, the first serological survey showed 4.9% prevalence among the
Central American immigrants in the Washington, DC (Kirchhoff et al.,
1987). Canada have also experienced imported cases and transfusion-
related transmission since 1970s (Schipper et al., 1980; Steele et al., 2007).
In Canada, 1.0% of Latin American immigrants were found seropositive in
2007 (Young et al., 2007). Autochthonous vector-borne transmission exists
TABLE 6.17 Estimated number of immigrants, infected population by Trypanosoma

cruzi and patients in need for medical attention
Estimated
Estimated number of
Estimated number of Estimated patients
number of the infected seropositivity with clinical
immigrants by T. cruzi (%) symptoms Year of data
United States 16,689,172 325,671 65,133 2007

Canada 156,960 5553 3.5 2006
15 European 483,074 14,010 2.9 2803 2001–2005
countries
(excluding
Spain)
Spain 1,678,711 86,948 5.2 17,390 2008
Australia 80,522 3088 3.8 2006
Japan 115,606 1510 > 2008
Total 19,204,045 436,780 >
(extracted from Schmunis and Yadon (2010))
in United States but not in Canada. Since the first report in Texas in 1955
(Woody and Woody, 1955), six more cases by vector transmission have
been documented in the Southern states of United States (Dorn et al., 2007;
Navin et al., 1985; Ochs et al., 1996; Schiffler et al., 1984).
As a preventive measure, United States implemented extensive sero-
logical screening for blood donation in 2007, covering 65% of the total
collected blood as of 2010 (Chagas’ Biovigilance Network, 2010). This
has allowed detecting more than 1,500 serologically positive donors in 42
states (Chagas Biovigilance Network, 2011). In Canada, blood screening is
performed selectively on at-risk donors, effectively, descendants of Latin
American immigrants and recent travellers to Central or South American
countries (Canadian Blood Services HP, 2011). United States and Canada
are yet to organize systems and policies for surveillance of congenital
transmission and early case detection. Surveillance may be reinforced
with complete blood screening in the southern region of United States and
joint initiative with Mexico (Sarkar et al., 2010).
In Europe, the following countries are identified as members of the non-
endemic countries initiative: Austria, Belgium, Croatia, Denmark, France,
Germany, Greece, Ireland, Italy, Luxembourg, Netherlands, Norway,
Portugal, Romania, Sweden, Spain, Switzerland and United Kingdom
(WHO, 2010). Chagas disease cases have been reported in 16 European
countries, with more than 4000 laboratory-confirmed cases during the
2000s (WHO, 2010). Since the first case report in Romania in 1975 (Pehr-
son et al., 1981), a few congenital, accidental, transfusional and imported
cases have been reported from Denmark, France, Italy, Spain and Swe-
den (Pehrson et al., 1982; Alvar, 1983; Brisseau et al., 1988; Villalba et al.,
1992; Crovato and Rebora, 1997; Enemark et al., 2000; Lescure et al., 2008).
The seroprevalence of Latin American population ranged from 2.0% to
12.8% in Germany, Italy, Spain and Switzerland (Frank et al., 1997; Jack-
son et al., 2010; Angheben et al., 2011; Flores-Chavez et al., 2011). Chagas
disease vectors have not been reported in Europe. By 2009, 14 countries
have implemented a prescreening questionnaire to exclude at-risk blood
donors. There is a need to improve pharmacovigilance and control of con-
genital or transplantation-related cases (WHO, 2010).
Japan and Australia are also listed for the non-endemic countries ini-
tiative for having the Latin American immigrants and Chagas disease
cases. In Japan, since the first case was confirmed in 1976, several cases
have been sporadically confirmed in the 1990s and 2000s among those
who had lived in Brazil and Bolivia (WHO, 2011). In 2000, a survey con-
ducted in a Japanese immigrant community in an endemic area of Bolivia
showed 24.5% of seropositivity and 13.5% of parasitemia (WHO, 2011).
Brazilian community in Japan was found with 1.9% of seroprevalence
during 2008–2010 (WHO, 2011). Triatominaes are found in Vietnam (T.
rubrofasciata) and in Australia (T. leopoldi) but have not been identified as
vectors for Chagas disease (WHO, 2011).
Currently, Japan and Australia have implemented a prescreening
questionnaire to prevent transfusional transmission (WHO, 2011). Poli-
cies on organ transplantation, congenital infection and promotion of early
diagnosis and treatment are yet to be established, while consultancy is
provided by an non-governmental organisation and universities in Japan
(WHO, 2011). China and Viet Num, in spite of their assumingly increas-
ing immigrants from Latin American, have none of these systems or poli-
cies introduced as of 2011 (WHO, 2011). Pharmacovigilance is currently in
place only in Japan.
6.8. CONCLUSIONS
Surveillance of autochthonous vector-borne transmission is a main chal-

lenge in Chagas disease endemic countries. To achieve interruption of
T. cruzi transmission by the widespread and non-eliminable vectors, the
surveillance systems need be more scalable and sustainable. Understand-
ing of the internal mechanism of the surveillance systems (see Section
6.4.) and the surrounding health system (see Section 6.5.) may provide
the opportunities to improve surveillance strategies. In the decentralised
health systems, especially where the vector control programs have diffi-
culties in dispatching the operational personnel to the communities, four
issues are important.
First, the vector surveillance systems should involve more local stake-
holders, so that more at-risk houses/individuals are reported and treated.
The Ministry of Health could delegate operational tasks to local non-pro-
fessional stakeholders, concentrating institutional resources into mana-
gerial tasks, quality control, data analysis and decision making. Second,
each country should establish reasonable response criteria for community
bug reports. The criteria need to meet the supply-demand balance, that is,
institutional available resources and community bug reports. Third, inte-
gration of the surveillance system into the existing local health service is a
decent option. Adjustments in political, technical, logistical and commu-
nicational dimensions will be a key to integration. Fourth, the functional
model of surveillance systems would be developed through empirical
trials. Discussion of role distribution among stakeholders, involving the
central programs, the local health authorities and locally available agents,
may facilitate development of scalable and sustainable surveillance.
The regional initiatives could reinforce the implementation of surveil-
lance strategies by providing standardized conceptual framework on surveil-
lance systems, including the evaluation indicators and certification criteria as
well as potential funding schemes. Technical and financial efforts need to be
united to reach the international goal ‘intra-domiciliary transmission inter-
rupted in the region of the Americas by 2015’ (WHO, 2012).
ACKNOWLEDGMENTS
The authors acknowledge the efforts by all stakeholders involved in the Chagas disease
control at different parts of the world, to reach the final common goal; elimination of the
disease. This review benefited particularly from experiences of Chagas disease surveillance
implemented by the Ministries of Health in Central and South America, and supported by
JICA, PAHO/WHO, ECLAT and CIDA. Special thanks to Concepción Zúniga of the Ministry
of Health in Honduras, Hector Rámos and Eduardo Romero of the Ministry of Health in El
Salvador, Roberto Savatella of PAHO, Jiro Nakamura and Emi Sasagawa of JICA projects,
and Yoichi Yamagata for revising the drafts.
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INDEX
Note: Page numbers with “f” denote figures; “t” tables.
A moose, 108–111, 111f, 118t–120t, 140t–141t,

Acanthatrium sp., 271 185t–186t, 199t
Acanthatrium oregonense, 264 muskoxen, 103–107, 109f–110f, 118t–120t,
Acari, 207–209 140t–141t, 185t–186t, 199t
Aegyptianella, 256–257 nematodes, 113–165
Aerial spraying, for tsetse control, 322 gastrointestinal, 113–138, 114f,
Alces americanus andersoni, 108–111 118t–120t, 136t–137t
Alces americanus gigas, 108–111 Marshallagia marshalli, 116–117, 124,
Alces americanus ssp., 108–111, 111f 127–128
Alloglossidium corti, 273–274 Marshallagia occidentalis, 116–117,
Amazon region initiative, 415 127–128
American trypanosomiasis. See Chagas Nematodirinae, 114–115, 128–131
disease, surveillance of Ostertagia gruehneri, 117–124
Anabas testudineus, 267–268 Ostertagiinea, 114–128, 123t
Anaplasma, 256–257 Teladorsagia boreoarcticus, 116–117,
Anaplasmataceae, 256–257 124–127
phylogenetic interrelationships, 257f Onchocercidae, 160–165
Ancylostoma caninum, 357 issues and knowledge gaps of, 165
Anoplocephalidae, 171–173 Onchocercinae, 163–164
Antilocapra americana, 154 Splendidofilariinae, 164–165
Aplexa hypnorum, 146 Oxyurinae, 132
Arctic ungulates, 99–252 issues and knowledge gaps of,
alive/well parasites in, 210–211 133–138
arthropods, 198–210, 198f, 199t Trichurinae, 132–133
Acari, 207–209 parasites in, 101–102, 104f
Crustacea, 209 biodiversity, 211–212
Diptera, 200–204 characteristics of, 212–215, 217–218
issues and future research of, 210 checklist of, 215t–217t
Pentastomida, 209 infections, impact of, 221–222
Phthiraptera, 204–207 monitoring programs for, 222–223
caribou, 103–107, 105f–106f, 118t–120t, Protostrongylidae, 139–160, 139f
140t–141t, 185t–186t, 199t Dictyocaulinae, 159–160
cestodes, 165–173 ecology of, 157–158
Anoplocephalidae, 171–173 Elaphostrongylinae, 148–153
Echinococcinae, 170–171 general effects of, 158–159
issues and knowledge gaps of, 173 identification of, 156–157
Taeniidae, 165–171 issues and knowledge gaps, 153–159
changing polar environments and Muelleriinae, 145–147
host–parasite interactions, 218–220 potentially invasive, 153–156
Dall’s sheep, 108–111, 112f, 118t–120t, Protostrongylinae, 142–145
140t–141t, 185t–186t, 199t Varestrongylinae, 147–148
429
430 Index
protozoa, 177–198 Bovicola spp., 205–207

blood, 183–198, 185t–186t geographic distribution of, 205
gastrointestinal, 177–183 hosts, 205
invasive, 177f, 197–198 impacts of, 206–207
tissue, 183–198, 185t–186t life cycle of, 205–206
Arrested larval development, of arctic morphology of, 205
parasites, 212–213 Bovicola tarandi, 205
Arthropods, 198–210, 198f, 199t Bovicola tibialis, 206–207
Avitellina spp., 171–173
ecology of, 172–173 C
geographic distribution of, 171–172
Canidae, 23
hosts, 171–172
Canis latrans, 263
impacts of, 173
Capillaria sp., 132
Card agglutination test for trypanosomiasis
B (CATT), 310–311, 325–326
Babesia odocoilei, 197–198 Caribou, 103–107, 105f–106f, 118t–120t,
Babesia spp., 197 140t–141t, 185t–186t, 199t
Bait technology, 322–323, 328 Carnivora, 17–34
Baylisascaris spp., 33–34 helminth parasites among, 19–22, 20t,
Beringia(n) 33–34
eastern, repopulation of, 63–64 Taenia tapeworms in, 29–31
parasite assemblages, 15–17, 18f Trichinella in, 25–27, 26f
as pass-through for neotropical faunas, 65 Catfish agents, 276–277
return to, 64 Cathepsin d-like aspartic proteases, 357
standard model, 63 Catinella sp., 146
Besnoitia besnoiti, 183–184 Central America, Chagas disease in
Besnoitia caprae, 183–184 epidemiological trends, 382–386
Besnoitia tarandi, 183–190 vector surveillance, 388–389
ecology of, 184–188 Cephenemyia spp., 200
future research of, 189–190 Cephenemyia trompe, 200–202
geographic distribution of, 184 ecology of, 201–202
hosts, 184 geographic distribution of, 201
impacts of, 188–189 hosts, 201
biodiversity, 3–6 impacts of, 202
biographic determinants of, 63–65 Cervus elaphus, 113
of Dictyocaulus spp., 160 Cestodes, 165–173, 166f, 166t–167t
discovery, tools for, 76–79, 77t ‘Chagas Day,’ 398, 399
distribution of, 60, 61f Chagas disease, surveillance of, 376–379
downstream, 62–63 challenges to, 409–414
faunal expansion, mechanisms of, 66–69 campaign, 411
integrated model for, 69–70 development of ecological approach,
latitudinal gradient in, 60–62 413–414
longitudinal gradient in, 60 evolution, 409–411
mosaic faunas. See Mosaic faunas multiple stakeholders, 409–410
parasites reveal, stories for, 74–76 for regional strategies, 411–413
Bison bison athabascae, 113 response to the community, 410–411
Bison bison bison, 113 community-based surveillance systems,
Blood protozoa, 183–198, 185t–186t. See also 391–402
Protozoa basic functions, 392, 392f
Blood-sucking arthropods, 254 in El Salvador and Honduras, 396–402
Bovicola jellisoni, 205–206 evaluation of process and results,
Bovicola oreamnidis, 205 394–396, 395t
Index 431
health systems and, 402–408 Creptotrema, 275–276

performance index of, 402f Crustacea, 209
Stakeholders of MoH and community, Cryptosporidae, 177–183
393–394 Cryptosporidium andersoni, 181
epidemiological trends, 379–386 Cryptosporidium spp., 180–181
Central America – IPCA, 382–386 ecology of, 181
South America – INCOSUR, 379–382 geographic distribution of, 180
situations of other initiatives, 415–418 hosts, 180
Latin America, 415–416 impacts of, 175, 181
non-endemic countries, 416–418
vector surveillance, 386–391 D
Central America – IPCA, 388–389
Dall’s sheep, 108–111, 112f, 118t–120t,
common structures of, 389–391
140t–141t, 185t–186t, 199t
South America – INCOSUR, 386–388
DDT, for tsetse control, 319–324
Channa gachua, 267–268
Departmental Vector Control Units, 407–408
Chemoprophylaxis with Lomidine, for T. b.
Department Health Office, 407–408
gambiense sleeping sickness, 316–317
Dermacentor albipictus, 197–198, 208–209
Chorioptes spp., 207
geographic distribution of, 208
hosts, 208
hosts, 207
impacts of, 208–209
impacts of, 207
life cycle of, 208
life cycle of, 207
morphology of, 208
morphology of, 207
Dermatophagoides farinae, 341
Chorioptes texanus, 207
Dermatophagoides pteronyssinus, 341
Circum Arctic Rangifer Monitoring and
Deroceras leave, 146, 148–149, 156
Assessment network (CARMA),
Deroceras reticulatum, 148
222–223
Deropegus, 275–276
Climate change and host–parasite
Dictyocaulinae, 159–160
interactions, 158, 220–221
Dictyocaulus eckerti, 160
Columella spp., 143–144
Dictyocaulus spp., 150, 159–160
Community-based surveillance systems,
ecology of, 159–160
391–402
basic functions of, 392, 392f
hosts, 159
in El Salvador and Honduras, 396–402,
impacts of, 160
401t
Dictyocaulus viviparus, 160
emergent cases, 399–400
Dieldrin, for tsetse control, 319–320
output and outcome, 400–402
Digeneans, 255, 269
response criteria, 399
and Neorickettsia, phylogenetic associa-
role distribution, 397–399
tions between, 283–285, 284f
stakeholders, 396–397, 396f
Diphyllobothrium alascense, 33
evaluation of process and results,
Diphyllobothrium cordatum, 33
394–396, 395t
Diphyllobothrium dalliae, 33
health systems and, 402–408
Diphyllobothrium dendriticum, 33
integration in El Salvador and
Diphyllobothrium fayi, 33
Honduras, 404–408, 405t–407t
Diphyllobothrium hians, 33
viewpoints to analyse program
Diphyllobothrium lanceolatum, 33
integration, 403–404
Diphyllobothrium latum, 33
Stakeholders of MoH and community,
Diphyllobothrium pacificum, 33
393–394
Diphyllobothrium spp., 33
Community health volunteer (CHV), 399
Diphyllobothrium stemmacephalum, 33
Cornified envelope (CE), 354
Diphyllobothrium ursi, 33
Crepidostomum, 275–276
Diplogonoporus spp., 33
432 Index
Diptera, 200–204 F
Disability-adjusted life year (DALY), Fasciolidae spp., 174–175
312–313, 324–325 Fascioloides magna, 174–175
DNA sequencing, 255 ecology of, 175
E hosts, 174–175
Echinococcinae, 170–171 impacts of, 175
Echinococcus canadensis, 31 Fecundity, of arctic parasites, 213–214
Echinococcus granulosus, 31–33, 170–171 Felids, 22
ecology of, 171 51-kDa antigen (P51), 287
hosts, 170–171 Filaggrin, 356
impacts of, 171 Foci of sleeping sickness, 303–304
Echinococcus multilocularis, 31–32 Freeze tolerance, of arctic parasites, 212
Echinococcus spp., 31–33 FTA®cards, 326–327
Ecology of parasites, 221. See also individual
parasites G
Eflornithine, for T. b. gambiense sleeping Gambian sleeping sickness. See T. b.
sickness, 309 gambiense sleeping sickness
Ehrlichia, 256–257, 270 Gastrointestinal nematodes, 113–138, 114f,
Eimeria spp., 181–183 118t–120t, 136t–137t
ecology of, 182 ecology of, 115
future research of, 183 geographic distribution of, 114–115
geographic distribution of, 181–182 hosts, 114–115
hosts, 181–182 impacts of, 115–116. See also Nematodes
impacts of, 182–183 Gastrointestinal protozoa, 177–183. See also
Eimeriidae, 181–183 Protozoa
Elaphostrongylinae, 148–153 Generalist life history, of arctic parasites,
Elaphostrongylus rangiferi, 155–156, 158 214–215
Electrocuting nets, for tsetse control, Giardia duodenalis, 177–180, 179t
322–323 ecology of, 178
Elk (Cervus elaphus), 113 geographic distribution of, 178
Elokomin fl uke fever (EFF) agent, 265–266 hosts, 178
El Salvador and Honduras, community- impacts of, 175, 178
based surveillance systems in, 396–402, Glaciation, 13–15, 14f
401t, 404–408, 405t–407t Glossina fuscipes, 302
emergent cases, 399–400 gltA, 267–268
output and outcome, 400–402 groESL gene sequence, 256
response criteria, 399
role distribution, 397–399
H
stakeholders, 396–397, 396f
Environmental health technicians (EHTs), Haemonchus contortus, 135–138
397, 408 Haemonchus placei, 135–138
Enzyme-linked immunosorbent assays Haemonchus spp., 135–138
(ELISAs), 344 Haplorchis taichui, 269
Euconulus fulvus, 146 Health Promotion Units, 407–408
Eurasia Health sector reform, 378–379
Pleistocene (Wisconsinan) expansion Health system functions, 403–404
from, 64 Health systems and community-based
repopulation of eastern Beringia from, surveillance systems, 402–408
63–64 integration in El Salvador and Honduras,
Euroglyphus maynei, 341 404–408
Expressed sequence tags (ESTs), 341
Index 433
viewpoints to analyse program integra- impacts of, 209

tion, 403–404 life cycle of, 209
Helisoma trivolis, 271–273 morphology of, 209
Heronimus mollis, 273–274 Linguatulidae, 209
Heterakis gallinarum, 254 Linognathidae, 204–205
Hexamitidae, 177–180 Linognathus vituli, 204–205
Histomonas meleagridis, 254 ‘Local health agents,’ 388
Host–parasite interactions, changing polar Loop-mediated isothermal amplification
environments and, 218–220 (LAMP), for sleeping sickness, 311,
ecological barriers, breakdown of, 325–326
219–220 Lung nematodes, 139–160, 139f. See also
parasite biodiversity, loss of, 220 Nematodes
Human African trypanosomiasis (HAT),
301. See also Sleeping sickness M
Hypoderma lineatum, 202
Marshallagia marshalli, 116–117,
Hypoderma spp., 200
124, 127–128
Hypoderma tarandi, 200, 202–204
hosts, 127
hosts, 202
impacts of, 128
Marshallagia occidentalis, 116–117, 127–128
I geographic distribution of, 127
Ictalurus punctatus, 276–277 hosts, 127
INCOSUR, 376–377, 379–382, 386–388 impacts of, 128
vector control strategy in, 377 Marshallagia spp., 114–117, 133
Invasion of parasites Megalogonia ictaluri, 276–277
dynamic, 65 Melarsoprol
episodic, 65 for T. b. gambiense sleeping sickness, 309
Invasive protozoa, 177f, 197–198. See also for T. b. rhodesiense sleeping sickness,
Protozoa 309–310
IPCA, 378, 382–386, 388–389 Mesodon spp., 149
‘Itch mite,’ 341 Metaseiulus occidentalis, 349–351
Ixodes scapularis, 197–198 Metastrongylus apri, 254
Ixodidae, 208–209 Microtus spp., 32
MoH and community, stakeholders of,
J 393–394
Molecular diagnostics, of sleeping sickness,
Jamot’s doctrine, 316–317 311
Japan International Cooperation Agency Molineus spp., 33–34
(JICA), 404–407 Moniezia baeri, 173
Juga silicula, 264 Moniezia benedeni, 171–173
Moniezia expansa, 171–173
L Moniezia rangiferina, 172
Lagomorpha, 34–39, 36t–37t Moniezia spp., 171–173
Lecithodendrium sp., 271 ecology of, 172
Lemmus spp., 32 geographic distribution of, 171–172
Lemmus trimucronatus, 30 hosts, 171–172
Lifespans, arctic parasites, 214 impacts of, 173
Linguatula arctica, 209 Moniezia taimyrica, 172
geographic distribution of, 209 Moose, 108–111, 111f, 118t–120t, 140t–141t,
hosts, 209 185t–186t, 199t
434 Index
Mosaic faunas, 65, 70–74 Nematodirella alcidis, 128–131

anthropogenic invasion, 73 Nematodirella davtiani, 129
contemporary invasion, 73 Nematodirella filicollis, 129–131
defined, 71–74 Nematodirella gazelle, 129
episodic geographic expansion and, 65, Nematodirella sp., 114–115
70–74 Nematodirella spathiger, 129
geospatial, 72–73 Nematodirinae, 114–115, 128–131
horizontal, 72–73 ecology of, 129
macroevolutionary, 72 geographic distribution of, 128–129
microevolutionary, 73 hosts, 128–129
Mountain goats (Oreamnos americanus), 113 impacts of, 131
Muelleriinae, 145–147 Nematodirus, 114–115
Muellerius capillaris, 154 Nematodirus abnormalis, 130–131
Mugil cephalus, 267 Nematodirus alcidis, 213
Mule deer (Odocoileus hemionus), 113 Nematodirus andersoni, 128–129
Muskoxen, 103–107, 109f–110f, 118t–120t, Nematodirus archari, 128–129
140t–141t, 185t–186t, 199t Nematodirus battus, 130–131
Mustelidae, Soboliphyme baturini in, 27–29 Nematodirus helvetianus, 128–131
Mustelids, 22 Nematodirus longissemispiculata, 128–131
Myodes rutilus, 30 Nematodirus oiratianus, 128–129
Myodes spp., 32 Nematodirus oiratianus interruptus, 128–129
Nematodirus skrjabini, 129
N Nematodirus spathiger, 130–131
Nematodirus tarandi, 129
Nanophyetus salmincola, 254–255, 261–262, Neorickettsia, 254–256
264–265, 283 and digenea, phylogenetic associations
Nanophyetus schikhobalowi, 265 between, 283–285, 284f
National Sleeping Sickness Control ecology and transmission, 260–277
Programmes (NSSCPs), 326–327 future perspectives, 287–289
National Vector Control Program, 407–408 genomics and molecular biology
Necator americanus, 357 advances, 285–287
Neglected tropical diseases (NTDs), 301 geographic distribution of, 277–283, 279f,
Nematodes, 113–165 280t–282t
of gastrointestinal tract, 113–138, 114f, from needlefish, 276
118t–120t, 136t–137t species/genotypes and related diseases,
ecology of, 115 259t
geographic distribution of, 114–115 systematic position, 256–257
hosts, 114–115 taxonomy and phylogenetic interrelation-
impacts of, 115–116 ships, 258–260, 258f
Marshallagia marshalli, 116–117, 124, Neorickettsia elokominica, 258
127–128 Neorickettsia helminthoeca, 258, 266, 276–277
Marshallagia occidentalis, 116–117, and SPD, 261–265
127–128 Neorickettsia risticii, 258–261, 269
Nematodirinae, 114–115, 128–131 generalized circulation pathways, 273f
Ostertagia gruehneri, 117–124 and PHF, 270–275
Ostertagiinea, 114–128, 123t Neorickettsia sennetsu, 258, 278
Teladorsagia boreoarcticus, 116–117, and Sennetsu fever, 267–269
124–127 Neospora caninum, 190–192
lung, 139–160 future research of, 191–192
Oxyurinae, 132 geographic distribution of, 190
issues and knowledge gaps of, 133–138 hosts, 190
Trichurinae, 132–133 impacts of, 191
tissue, 139–160
Index 435
life cycle of, 190–191 Organochlorine endosulfan, for tsetse

Nifurtimox–eflornithine combination control, 322
treatment (NECT), for T. b. gambiense Ornithodoros erraticus, 359
sleeping sickness, 309 Orthostrongylus macrotis, 142, 154
North American regional southern refugia, Ostertagia gruehneri, 114–115, 117–124,
63 133–134
Northern host–parasite assemblages, 1–97 ecology of, 121–124
Beringian parasite assemblages, 15–17, geographic distribution of, 117–121
18f hosts, 117–121
biodiversity. See Biodiversity impacts of, 124
characteristics of, 5t lifespan of, 214
faunal structure, 17–60 Ostertagia spp., 114–117
associated with Lagomorpha, 34–39, Ostertagiinea, 114–128, 123t
36t–37t morphs for, 117t
associated with rodentia, 39–47, 40t–41t nomenclature of, 116
associated with ruminants, 48–56, 49t taxonomy of, 116
associated with terrestrial Carnivora, Ovibos moschatus moschatus, 107–108
17–34 Ovibos moschatus ssp., 103–107, 109f–110f
human interfaces and occupation, Ovibos moschatus wardii, 107–108
56–60 O. virginianus, 148
historical characteristics of, 13t Ovis Canadensis, 143
parasite diversity, 9–12 Ovis dalli dalli, 108–111
physical–biological setting for, 12–17, 13t Ovis dalli stonei, 127–128
problems and challenges to, 79–81 Oxytrema silicula, 264
Noturus flavus, 276–277 Oxyuridae, 114–116
Novel full-length scabies mite peritrophin Oxyurinae, 132
(SsPTP1), 363
nucleic acid sequence-based amplification, P
for sleeping sickness, 311
Paramphistomidae, 176–177
Paramphistomum cervi, 176
O Paramphistomum spp., 176–177
Odobenus rosmarus, 27 ecology of, 176–177
Odocoileus hemionus, 113 geographic distribution of, 176
Odocoileus hemionus sitkensis, 113 hosts, 176
Odocoileus virginianus, 113 Parasite biodiversity, 211–212
Oestridae, 200–204 Parasite diversity, 9–12. See also Biodiversity
Omp85, 267–268 Parasites reveal, stories for, 74–76
Onchocerca cervipedis, 163–164 Parelaphostrongylus andersoni, 148–150,
Onchocerca jakutensis, 164 157
Onchocerca spp., 163–164 ecology of, 149
geographic distribution of, 163 geographic distribution of, 148–149
hosts, 163 hosts, 148–149
impacts of, 164 impacts of, 150
life cycle of, 163–164 Parelaphostrongylus odocoilei, 143–144,
Onchocerca tarsicola, 163 150–153, 157–158
Onchocercidae, 160–165 ecology of, 151–153
Onchocercinae, 163–164 geographic distribution of, 150–151
Onychiurus furcifera, 172 hosts, 150–151
Onychiurus taimyricus, 172 impacts of, 153
Opisthorchis viverrini, 269 Parelaphostrongylus tenuis, 154–155
Oreamnos americanus, 113 Pay For Success contracts, 328–329
436 Index
Pentamidine, for T. b. gambiense sleeping Rhodesian sleeping sickness. See T. b.

sickness, 309, 316–317 rhodesiense sleeping sickness
Pentastomida, 209 Rhodnius pallescens, 386
Phthiraptera, 204–207 Rhodnius prolixus, 377–378, 415–416
Phyllodistomum lacustri, 276–277 Rickettsiaceae, 256
Physical–biological setting, for Northern Rodentia, 39–47, 40t–41t
host–parasite assemblages, 12–17 Rumenfilaria andersoni, 164–165
Pichia pastoris, 359–360 geographic distribution of, 164
Plains bison (Bison bison bison), 113 hosts, 164
Pleistocene impacts of, 165
arctic host–parasite assemblages, 103 life cycle of, 165
expansion from Eurasia, 64 Ruminants, 48–56, 49t
radiations, 64–65
Pliocene radiations, 64–65 S
Pneumostrongylus, 147
Salmon poisoning disease (SPD), 254–255
Polymerase chain reaction (PCR), 255
Neorickettsia helminthoeca, 261–265
Polymerase chain reaction (PCR) test, for
Sanguinicola sp., 275–276
sleeping sickness, 311, 318–319, 326–327
Sarcocystidae, 183–196
Potomac horse fever
Sarcocystis spp., 194–196
Neorickettsia risticii, 270–275
ecology of, 195
Prepatent periods, in arctic parasites,
future research of, 195–196
213–214
Prosthodendrium molenkampi, 269
hosts, 194
α-Proteobacteria, 286
impacts of, 195
Protostrongylidae, 139–160
Sarcoptes scabiei, 340, 342, 349–351
Protostrongylinae, 142–145
Sar s 3, 354–356
Protostrongylus coburni, 142
Satellite technology, 311–313
Protostrongylus frosti, 142
Scabies, 340–341
Protostrongylus rushi, 142, 145
biology/clinical aspects, 342–346
Protostrongylus stilesi, 142, 157
clinical presentation, 342–343
ecology of, 146
diagnosis, 343–344
interaction of scabies mites with the
hosts, 145
host epidermis, 344–346, 345f
lifecycle and transmission, 342
Protozoa, 177–198
complement inhibition by scabies mites,
gastrointestinal, 177–183
364–365
Psoroptidae, 207
current strategies to control, 346–348
Pupilla spp., 143–144
development of animal model for, 352t
Pyramicocephalus spp., 33
Sar s 3, 354–356
Pyrethroids, for tsetse control, 322
scabies mite intestinal proteins, 353–354
scabies mite peritrophin, 362–364
R SMIPP-Ss, 358–362
Rainbow trout agent, 275–276 SsAP, 357–358
Rangifer tarandus caribou, 104–107 tools to facilitate research on, 348–353
Rangifer tarandus granti, 104–107 porcine system, 351–353
Rangifer tarandus groenlandicus, 104–107 scabies mite EST database, 349–351
Rangifer tarandus pearyi, 104–107 Scabies mite-inactivated protease
Rangifer tarandus ssp., 103–107, 105f–106f paralogues – serine proteases
Rangifer tarandus tarandus, 104–107 (SMIPP-Ss), 359–360
Reservoirs, of sleeping sickness, 306–308 Seasonality and arctic partasites, 213
Rhipicephalus microplus, 359 Sennetsu fever, 254–255, 288
Neorickettsia sennetsu, 267–269
Index 437
Sequential aerosol technique (SAT), 322 Soboliphyme baturini

Setaria labiatopapillosa, 161 characteristics of, 28
Setaria spp., 161–163 geographical expansion and colonisation
ecology of, 161–162 of, 28
geographic distribution of, 161 history of, 28
hosts, 161 in Mustelidae, 27–29
impacts of, 163 structure of, 28–29
Setaria tundra, 161–163, 213 Social impact bonds (SIBs), 328–329
Setaria yehi, 161–163 Solenopotes tarandi, 204–205
Setariinae, 161–163 geographic distribution of, 204
Simulium decorum, 163–164 hosts, 204
Simulium venustum, 163–164 impacts of, 205
Sitka black-tailed deer (Odocoileus hemionus life cycle of, 204–205
sitkensis), 113 morphology of, 204
16S ribosomal RNA (rRNA) sequence, 256 South America, Chagas disease in
Skrjabinema ovis, 132 epidemiological trends, 379–382
Skrjabinema spp., 132 vector surveillance, 386–388
ecology of, 132 Species at Risk Act (Canada), 107
geographic distribution of, 132 Spiculopteragia boehmi, 138
hosts, 132 Splendidofilariinae, 164–165
impact of, 132 SsAP, 357–358
Sleeping sickness, 293–337 Stagnicola, 271–273
burden of, 311–313 Stakeholders, 396–397, 396f
hidden, 313 Stamp Out Sleeping Sickness, The, 328
control of, 313–324 Stellantchasmus falcatus, 260–261
origins of epidemics, 314–316 Stellantchasmus falcatus agent (SF agent), 275
T. b. gambiense sleeping sickness, Sterile insect technique (SIT), 322
318–320 Suramin, for T. b. rhodesiense sleeping
T. b. rhodesiense sleeping sickness, 321 sickness, 309–310
tsetse control and T. b. gambiense Swine influenza, 254
sleeping sickness, 318–320
diagnosis of, 310 T
molecular diagnostics, 311
Taenia arctos, 165–170
T. b. gambiense sleeping sickness, 310
T. b. rhodesiense sleeping sickness, 310
Gambian. See T. b. gambiense sleeping
hosts, 165–168
sickness
impacts of, 170
Rhodesian. See T. b. rhodesiense sleeping
Taenia crassiceps, 30, 32
sickness
Taenia hydatigena, 29, 165–170
risk factors associated with, 301–308
disease distribution, 302–303
foci of infection, 303–304
hosts, 165–168
reservoirs of infection, 306–308
impacts of, 165
vector competence, 304–306
Taenia intermedia, 29
vector distribution, 301–302
Taenia krabbei, 165–170, 213
treatment for
T. b. gambiense sleeping sickness,
308–309
hosts, 165–168
T. b. rhodesiense sleeping sickness,
impacts of, 170
309–310
Taenia krabbei, 29
SMIPP-Ss, 358–362
Taenia martis, 29
438 Index
Taenia multiceps, 170 Trematodes, 173–177, 174f

Taenia mustelae, 29 Triatoma brasiliensis, 380–382
Taenia polyacantha, 29–30, 32 Triatoma cruzi, 379–380, 411–412, 416–418
Taenia solium, 170 Triatoma dimidiata, 378, 384–386, 388–389,
Taenia tapeworms, in Carnivorans, 29–31 393, 403, 409–411, 414–416
Taenia twitchelli, 29 habitat of, 384
Taeniidae, 165–171 Triatoma infestans, 376–377, 378–382, 381t,
Taxon pulses, 69–70 386, 388–389, 393, 415
T. b. gambiense sleeping sickness Triatoma sordida, 380
burden of, 311–312 Trichinella, in Carnivorans, 25–27, 26f
contrlling, 316–318 Trichinella murrelli, 25–27, 26f
diagnosis of, 310 Trichinella native, 25–27, 26f
risk factors associated with, 303–304 Trichodectidae, 205–207
staging of, 308–309 Tricholipeurus para, 206–207
treatment for, 308–309 Trichopsis vittata, 267–268
tsetse control and, 318–320 Trichostrongyline nematodes, 116–117
T. b. rhodesiense sleeping sickness Trichostrongylus axei, 135
burden of, 312 Trichuridae, 114–116
controlling, 321 Trichurinae, 132–133
diagnosis of, 310 Trichuris schumakovitschi, 132
risk factors associated with, 303 Trichuris spp., 132–133
treatment for, 309–310 geographic distribution of, 132
Teladorsagia boreoarcticus, 114–117, 124–127, hosts, 132
133, 214 impacts of, 133
ecology of, 126 life cycle of, 132
geographic distribution of, 124–125 Triodopsis spp., 149
hosts, 124–125 Trypanosoma congolense, 303
impacts of, 127 Trypanosoma spp., 196–197
lifespan of, 214 ecology of, 196–197
Teladorsagia circumcincta, 116–117, 124–125, geographic distribution of, 196
214 hosts, 196
Teladorsagia davitiani, 116–117 impacts of, 197
Teladorsagia spp., 114–117 Trypanosomatidae, 196–197
Teladorsagia trifurcate, 116–117 Tsetse
Thysanosoma actinoides, 171–172 control
Thysanosoma spp., 171–173 and T. b. gambiense sleeping sickness,
ecology of, 172–173 318–320
geographic distribution of, 172 and T. b. rhodesiense sleeping sickness,
hosts, 171–172 321–324
impacts of, 173 T. b. rhodesiense infection in, 303
Thysanosomatinae, 171–173 T. b. gambiense infection in, 303–304
Tissue nematodes, 139–160, 139f, 140t–141t. Turkey blackhead disease, 254
See also Nematodes
Tissue protozoa, 183–198, 185t–186t. See also U
Protozoa
Toxascaris spp., 33–34 Umingmakstrongylus pallikuukensis, 145–147,
Toxoplasma gondii, 192–194 157–158, 213
ecology of, 192–193 Uncinaria rauschi, 34
future research of, 194 Uncinaria skrjabini, 34
geographic distribution of, 192 Uncinaria spp., 34
hosts, 192 Uncinaria yukonensis, 34
impacts of, 193–194 Ursus americanus, 265–266
Index 439
V W
Vallonia spp., 143–144 Western coastal refugial zones, 64
Varestrongylinae, 147–148 white-tailed deer (Odocoileus virginianus),
Varestrongylus alpenae, 154 113
Varestrongylus sp. n., 147, 157 Wolbachia, 256, 285
ecology of, 148 Wolves, 23
geographic distribution of, 147 Wood bison (Bison bison athabascae), 113
hosts, 147 World Health Organization (WHO)
Vector control programs, 385t, 386 Global Burden of Disease (GBD), 324–325
Vector control technicians (VCTs), 386, 397,
399–400, 408, 414 X
Vector Control Unit, 407–408
Xenentodon cancila, 276
Vector distribution, of sleeping sickness,
301–302
Vertigo spp., 143–144
V. lagopus, 31–32
V. vulpes, 31–32
CONTENTS OF VOLUMES
IN THIS SERIES
Volume 41 M. Albonico, D.W.T. Cromption, and

L. Savioli
Drug Resistance in Malaria Parasites of
Animals and Man DNA Vaocines: Technology and
W. Peters Applications as Anti-parasite and
Anti-microbial Agents
Molecular Pathobiology and Antigenic J.B. Alarcon, G.W. Wainem and
Variation of Pneumocystis carinii D.P. McManus
Y. Nakamura and M. Wada
Ascariasis in China
P. Weidono, Z. Xianmin and
D.W.T. Crompton
Volume 43
Genetic Exchange in the
The Generation and Expression of
Trypanosomatidae
Immunity to Trichinella spiralis in
W. Gibson and J. Stevens
Laboratory Rodents
R.G. Bell The Host-Parasite Relationship in
Neosporosis
Population Biology of Parasitic
A. Hemphill
Nematodes: Application of Genetic
Markers Proteases of Protozoan Parasites
T. J.C. Anderson, M.S. Blouin and P.J. Rosenthal
R.M. Brech
Proteinases and Associated Genes of
Schistosomiasis in Cattle Parasitic Helminths
J. De Bont and J. Vercruysse J. Tort, P.J. Brindley, D. Knox, K.H. Wolfe,
and J.P. Dalton
Parasitic Fungi and their
Volume 42 Interaction with the Insect
Immune System
The Southern Cone Initiative Against
A. Vilcinskas and P. Götz
Chagas Disease
C.J. Schofield and J.C.P. Dias
Phytomonas and Other Trypanosomatid
Parasites of Plants and Fruit Volume 44
E.P. Camargo
Cell Biology of Leishmania
Paragonimiasis and the Genus B. Handman
Paragonimus
Immunity and Vaccine Development in
D. Blair, Z.-B. Xu, and T. Agatsuma
the Bovine Theilerioses
Immunology and Biochemistry of N. Boulter and R. Hall
Hymenolepis diminuta
The Distribution of Schistosoma bovis
J. Anreassen, E.M. Bennet-Jenkins, and
Sonaino, 1876 in Relation to
C. Bryant
Intermediate Host Mollusc-Parasite
Control Strategies for Human Intestinal Relationships
Nematode Infections H. Moné, G. Mouahid, and S. Morand
441
442 Contents of Volumes in This Series
The Larvae of Monogenea Satellites, Space, Time and the African

(Platyhelminthes) Trypanosomiases
I.D. Whittington, L.A. Chisholm, and D.J. Rogers
K. Rohde
Earth Observation, Geographic
Sealice on Salmonids: Their Biology and Information Systems and Plasmodium
Control falciparum Malaria in Sub-Saharan
A.W. Pike and S.L. Wadsworth Africa
S.I. Hay, J. Omumbo, M. Craig, and
R.W. Snow
Volume 45 Ticks and Tick-borne Disease Systems in
The Biology of some Intraerythrocytic Space and from Space
Parasites of Fishes, Amphibia S.E. Randolph
and Reptiles The Potential of Geographical
A.J. Davies and M.R.L. Johnston Information Systems (GIS) and
The Range and Biological Activity of Remote Sensing in the Epidemiology
FMR Famide-related Peptides and and Control of Human Helminth
Classical Neurotransmitters Infections
in Nematodes S. Brooker and E. Michael
D. Brownlee, L. Holden-Dye, and Advances in Satellite Remote Sensing
R. Walker of Environmental Variables for
The Immunobiology of Gastrointestinal Epidemiological Applications
Nematode Infections in Ruminants S.J. Goetz, S.D. Prince, and J. Small
A. Balic, V.M. Bowles, and E.N.T. Forecasting Diseases Risk for Increased
Meeusen Epidemic Preparedness in Public
Health
M.F. Myers, D.J. Rogers, J. Cox,
Volume 46 A. Flauhalt, and S.I. Hay
Host-Parasite Interactions in Education, Outreach and the Future of
Acanthocephala: A Morphological Remote Sensing in Human Health
Approach B.L. Woods, L.R. Beck, B.M. Lobitz, and
H. Taraschewski M.R. Bobo
Eicosanoids in Parasites and Parasitic
Infections
A. Daugschies and A. Joachim Volume 48
The Molecular Evolution of
Volume 47 Trypanosomatidae
J.R. Stevens, H.A. Noyes, C.J. Schofield,
An Overview of Remote Sensing and and W. Gibson
Geodesy for Epidemiology and
Transovarial Transmission in the
Public Health Application
Microsporidia
S. I. Hay
A.M. Dunn, R.S. Terry, and J.E. Smith
Linking Remote Sensing, Land Cover
Adhesive Secretions in the
and Disease
Platyhelminthes
P.J. Curran, P.M. Atkinson, G.M. Foody,
I.D. Whittington and B.W. Cribb
and E.J. Milton
The Use of Ultrasound in Schistosomiasis
Spatial Statistics and Geographic
C.F.R. Hatz
Information Systems in
Epidemiology and Public Health Ascaris and Ascariasis
T.P. Robinson D.W.T. Crompton
Contents of Volumes in This Series 443
Volume 49 Volume 52
Antigenic Variation in Trypanosomes: The Ecology of Fish Parasites with
Enhanced Phenotypic Variation in a Particular Reference to Helminth
Eukaryotic Parasite Parasites and their Salmonid Fish
H.D. Barry and R. McCulloch Hosts in Welsh Rivers: A Review of
Some of the Central Questions
The Epidemiology and Control of
J.D. Thomas
Human African Trypanosomiasis
J. Pépin and H.A. Méda Biology of the Schistosome Genus
Trichobilharzia
Apoptosis and Parasitism: from the
P. Horák, L. Kolárová, and C.M. Adema
Parasite to the Host Immune
Response The Consequences of Reducing
G.A. DosReis and M.A. Barcinski Transmission of Plasmodium
falciparum in Africa
Biology of Echinostomes Except
R.W. Snow and K. Marsh
Echinostoma
B. Fried Cytokine-Mediated Host Responses
during Schistosome Infections:
Walking the Fine Line Between
Volume 50 Immunological Control and
Immunopathology
The Malaria-Infected Red Blood Cell: K.F. Hoffmann, T.A. Wynn, and
Structural and Functional Changes D.W. Dunne
B.M. Cooke, N. Mohandas, and R.L. Coppel
Schistosomiasis in the Mekong Region:
Epidemiology and Phytogeography
S.W. Attwood Volume 53
Molecular Aspects of Sexual Interactions between Tsetse and
Development and Reproduction in Trypanosomes with Implications for
Nematodes and Schistosomes the Control of Trypanosomiasis
P.R. Boag, S.E. Newton, and R.B. Gasser S. Aksoy, W.C. Gibson, and M.J. Lehane
Antiparasitic Properties of Medicinal Enzymes Involved in the Biogenesis of
Plants and Other Naturally the Nematode Cuticle
Occurring Products A.P. Page and A.D. Winter
S. Tagboto and S. Townson
Diagnosis of Human Filariases (Except
Onchocerciasis)
M. Walther and R. Muller
Volume 51
Aspects of Human Parasites in which
Surgical Intervention May Be
Important
D.A. Meyer and B. Fried Volume 54
Electron-transfer Complexes in Ascaris Introduction – Phylogenies,
Mitochondria Phylogenetics, Parasites and the
K. Kita and S. Takamiya Evolution of Parasitism
D.T.J. Littlewood
Cestode Parasites: Application of In Vivo
and In Vitro Models for Studies of the Cryptic Organelles in Parasitic Protists
Host-Parasite Relationship and Fungi
M. Siles-Lucas and A. Hemphill B.A.P. Williams and P.J. Keeling
Phylogenetic Insights into the Evolution The Mitochondrial Genomics of Parasitic

of Parasitism in Hymenoptera Nematodes of Socio-Economic
J.B. Whitfield Importance: Recent Progress, and
Implications for Population Genetics
Nematoda: Genes, Genomes and the
and Systematics
Evolution of Parasitism
M. Hu, N.B. Chilton, and R.B. Gasser
M.L. Blaxter
The Cytoskeleton and Motility in
Life Cycle Evolution in the Digenea:
Apicomplexan Invasion
A New Perspective from Phylogeny
R.E. Fowler, G. Margos, and
T.H. Cribb, R.A. Bray, P.D. Olson, and
G.H. Mitchell
D.T.J. Littlewood
Progress in Malaria Research: The Case
for Phylogenetics Volume 57
S.M. Rich and F.J. Ayala
Canine Leishmaniasis
Phylogenies, the Comparative Method J. Alvar, C. Cañavate, R. Molina,
and Parasite Evolutionary Ecology J. Moreno, and J. Nieto
S. Morand and R. Poulin
Sexual Biology of Schistosomes
Recent Results in Cophylogeny Mapping H. Moné and J. Boissier
M.A. Charleston
Review of the Trematode Genus Ribeiroia
Inference of Viral Evolutionary Rates (Psilostomidae): Ecology, Life
from Molecular Sequences History, and Pathogenesis with
A. Drummond, O.G. Pybus, and Special Emphasis on the Amphibian
A. Rambaut Malformation Problem
Detecting Adaptive Molecular P.T.J. Johnson, D.R. Sutherland,
Evolution: Additional Tools for the J.M. Kinsella and K.B. Lunde
Parasitologist The Trichuris muris System: A Paradigm
J.O. McInerney, D.T.J. Littlewood, and of Resistance and Susceptibility to
C.J. Creevey Intestinal Nematode Infection
L.J. Cliffe and R.K. Grencis
Scabies: New Future for a Neglected
Volume 55 Disease
S.F. Walton, D.C. Holt, B.J. Currie, and
Contents of Volumes 28–52 D.J. Kemp
Cumulative Subject Indexes for Volumes
28–52
Contributors to Volumes 28–52 Volume 58
Leishmania spp.: On the Interactions they
Establish with Antigen-Presenting
Volume 56 Cells of their Mammalian Hosts
J.-C. Antoine, E. Prina, N. Courret, and
Glycoinositolphospholipid from
T. Lang
Trypanosoma cruzi: Structure,
Biosynthesis and Immunobiology Variation in Giardia: Implications for
J.O. Previato, R. Wait, C. Jones, Taxonomy and Epidemiology
G.A. DosReis, A.R. Todeschini, N. Heise R.C.A. Thompson and P.T. Monis
and L.M. Previata
Recent Advances in the Biology
Biodiversity and Evolution of the of Echinostoma species in the
Myxozoa “revolutum” Group
E.U. Canning and B. Okamura B. Fried and T.K. Graczyk
Human Hookworm Infection in the Volume 61

21st Century
S. Brooker, J. Bethony, and P.J. Hotez Control of Human Parasitic Diseases:
Context and Overview
The Curious Life-Style of the Parasitic David H. Molyneux
Stages of Gnathiid Isopods
N.J. Smit and A.J. Davies Malaria Chemotherapy
Peter Winstanley and Stephen Ward
Insecticide-Treated Nets
Volume 59 Jenny Hill, Jo Lines, and
Genes and Susceptibility to Mark Rowland
Leishmaniasis
Control of Chagas Disease
Emanuela Handman, Colleen Elso, and
Yoichi Yamagata and Jun Nakagawa
Simon Foote
Human African Trypanosomiasis:
Cryptosporidium and Cryptosporidiosis
Epidemiology and Control
R.C.A. Thompson, M.E. Olson, G. Zhu,
E.M. Fèvre, K. Picozzi, J. Jannin,
S. Enomoto, Mitchell S. Abrahamsen
S.C. Welburn and I. Maudlin
and N.S. Hijjawi
Chemotherapy in the Treatment and
Ichthyophthirius multifiliis Fouquet and
Control of Leishmaniasis
Ichthyophthiriosis in Freshwater
Jorge Alvar, Simon Croft, and Piero
Teleosts
Olliaro
R.A. Matthews
Dracunculiasis (Guinea Worm Disease)
Biology of the Phylum Nematomorpha
Eradication
B. Hanelt, F. Thomas, and A. Schmidt-
Ernesto Ruiz-Tiben and Donald
Rhaesa
R. Hopkins
Intervention for the Control of Soil-
Volume 60 Transmitted Helminthiasis in the
Community
Sulfur-Containing Amino Acid
Marco Albonico, Antonio Montresor,
Metabolism in Parasitic Protozoa
D.W. T. Crompton, and Lorenzo Savioli
Tomoyoshi Nozaki, Vahab Ali, and
Masaharu Tokoro Control of Onchocerciasis
Boakye A. Boatin and Frank O.
The Use and Implications of Ribosomal
Richards, Jr.
DNA Sequencing for the
Discrimination of Digenean Species Lymphatic Filariasis: Treatment, Control
Matthew J. Nolan and Thomas H. Cribb and Elimination
Eric A. Ottesen
Advances and Trends in the Molecular
Systematics of the Parasitic Control of Cystic Echinococcosis/
Platyhelminthes Hydatidosis: 1863–2002
Peter D. Olson and Vasyl V. Tkach P.S. Craig and E. Larrieu
Wolbachia Bacterial Endosymbionts of Control of Taenia solium Cysticercosis/
Filarial Nematodes Taeniosis
Mark J. Taylor, Claudio Bandi, and Achim Arve Lee Willingham III and
Hoerauf Dirk Engels
The Biology of Avian Eimeria with Implementation of Human
an Emphasis on their Control by Schistosomiasis Control: Challenges
Vaccination and Prospects
Martin W. Shirley, Adrian L. Smith, and Alan Fenwick, David Rollinson, and
Fiona M. Tomley Vaughan Southgate
Volume 62 Targeting of Toxic Compounds to the

Trypanosome’s Interior
Models for Vectors and Vector-Borne Michael P. Barrett and Ian H. Gilbert
Diseases
D.J. Rogers Making Sense of the Schistosome
Surface
Global Environmental Data for Patrick J. Skelly and R. Alan Wilson
Mapping Infectious Disease
Distribution Immunology and Pathology of Intestinal
S.I. Hay, A.J. Tatem, A.J. Graham, Trematodes in Their Definitive Hosts
S.J. Goetz, and D.J. Rogers Rafael Toledo, José-Guillermo Esteban, and
Bernard Fried
Issues of Scale and Uncertainty in the
Global Remote Sensing of Systematics and Epidemiology of
Disease Trichinella
P.M. Atkinson and A.J. Graham Edoardo Pozio and K. Darwin Murrell
Determining Global Population

Distribution: Methods, Applications
and Data Volume 64
D.L. Balk, U. Deichmann, G. Yetman,
F. Pozzi, S.I. Hay, and A. Nelson Leishmania and the Leishmaniases:
A Parasite Genetic Update and
Defining the Global Spatial Limits of Advances in Taxonomy, Epidemiology
Malaria Transmission in 2005 and Pathogenicity in Humans
C.A. Guerra, R.W. Snow and S.I. Hay Anne-Laure Bañuls, Mallorie Hide and
The Global Distribution of Yellow Fever Franck Prugnolle
and Dengue Human Waterborne Trematode and
D.J. Rogers, A.J. Wilson, S.I. Hay, and Protozoan Infections
A.J. Graham Thaddeus K. Graczyk and Bernard Fried
Global Epidemiology, Ecology and The Biology of Gyrodctylid
Control of Soil-Transmitted Helminth Monogeneans: The “Russian-Doll
Infections Killers”
S. Brooker, A.C.A. Clements and T.A. Bakke, J. Cable, and P.D. Harris
D.A.P. Bundy
Human Genetic Diversity and the
Tick-borne Disease Systems: Mapping Epidemiology of Parasitic and Other
Geographic and Phylogenetic Transmissible Diseases
Space Michel Tibayrenc
S.E. Randolph and D.J. Rogers
Global Transport Networks and
Infectious Disease Spread
A.J. Tatem, D.J. Rogers and S.I. Hay Volume 65
Climate Change and Vector-Borne ABO Blood Group Phenotypes and
Diseases Plasmodium falciparum Malaria:
D.J. Rogers and S.E. Randolph Unlocking a Pivotal Mechanism
María-Paz Loscertales, Stephen Owens,
James O’Donnell, James Bunn, Xavier
Bosch-Capblanch, and Bernard J. Brabin
Volume 63
Structure and Content of the Entamoeba
Phylogenetic Analyses of Parasites in the histolytica Genome
New Millennium C. G. Clark, U. C. M. Alsmark, M.
David A. Morrison Tazreiter, Y. Saito-Nakano, V. Ali,
S. Marion, C. Weber, C. Mukherjee, Volume 67

I. Bruchhaus, E. Tannich, M. Leippe,
T. Sicheritz-Ponten, P. G. Foster, Introduction
J. Samuelson, C. J. Noël, R. P. Hirt, Irwin W. Sherman
T. M. Embley, C. A. Gilchrist, B. J. Mann, An Introduction to Malaria Parasites
U. Singh, J. P. Ackers, S. Bhattacharya, Irwin W. Sherman
A. Bhattacharya, A. Lohia, N. Guillén,
M. Duchêne, T. Nozaki, and N. Hall The Early Years
Irwin W. Sherman
Epidemiological Modelling for
Monitoring and Evaluation of Show Me the Money
Lymphatic Filariasis Control Irwin W. Sherman
Edwin Michael, Mwele N. Malecela- In Vivo and In Vitro Models
Lazaro, and James W. Kazura Irwin W. Sherman
The Role of Helminth Infections in Malaria Pigment
Carcinogenesis Irwin W. Sherman
David A. Mayer and Bernard Fried
Chloroquine and Hemozoin
A Review of the Biology of the Irwin W. Sherman
Parasitic Copepod Lernaeocera
branchialis (L., 1767)(Copepoda: Isoenzymes
Pennellidae Irwin W. Sherman
Adam J. Brooker, Andrew P. Shinn, and The Road to the Plasmodium falciparum
James E. Bron Genome
Irwin W. Sherman
Carbohydrate Metabolism
Volume 66 Irwin W. Sherman
Strain Theory of Malaria: The First 50 Pyrimidines and the Mitochondrion
Years Irwin W. Sherman
F. Ellis McKenzie,* David L. Smith, The Road to Atovaquone
Wendy P. O’Meara, and Eleanor Irwin W. Sherman
M. Riley
The Ring Road to the Apicoplast
Advances and Trends in the Molecular Irwin W. Sherman
Systematics of Anisakid Nematodes,
with Implications for their Ribosomes and Ribosomal Ribonucleic
Evolutionary Ecology and Host– Acid Synthesis
Parasite Co-evolutionary Irwin W. Sherman
Processes De Novo Synthesis of Pyrimidines and
Simonetta Mattiucci and Giuseppe Folates
Nascetti Irwin W. Sherman
Atopic Disorders and Parasitic Salvage of Purines
Infections Irwin W. Sherman
Aditya Reddy and Bernard Fried
Polyamines
Heartworm Disease in Animals and Irwin W. Sherman
Humans
John W. McCall, Claudio Genchi, Laura H. New Permeability Pathways and
Kramer, Jorge Guerrero, and Luigi Transport
Venco Irwin W. Sherman
Hemoglobinases Tracking Transmission of the Zoonosis

Irwin W. Sherman Toxoplasma gondii
Judith E. Smith
Erythrocyte Surface Membrane Proteins
Irwin W. Sherman Parasites and Biological Invasions
Alison M. Dunn
Trafficking
Irwin W. Sherman Zoonoses in Wildlife: Integrating Ecology
into Management
Erythrocyte Membrane Lipids
Fiona Mathews
Irwin W. Sherman
Understanding the Interaction Between
Invasion of Erythrocytes
an Obligate Hyperparasitic
Irwin W. Sherman
Bacterium, Pasteuria
Vitamins and Anti-Oxidant Defenses penetrans and its Obligate
Irwin W. Sherman Plant-Parasitic Nematode Host,
Meloidogyne spp.
Shocks and Clocks
Keith G. Davies
Irwin W. Sherman
Host–Parasite Relations and Implications
Transcriptomes, Proteomes and Data
for Control
Mining
Alan Fenwick
Irwin W. Sherman
Onchocerca–Simulium Interactions and the
Mosquito Interactions
Population and Evolutionary Biology
Irwin W. Sherman
of Onchocerca volvulus
María-Gloria Basáñez, Thomas S.
Churcher, and María-Eugenia
Volume 68 Grillet
HLA-Mediated Control of HIV and HIV Microsporidians as Evolution-Proof
Adaptation to HLA Agents of Malaria Control?
Rebecca P. Payne, Philippa C. Matthews, Jacob C. Koella, Lena Lorenz, and Irka
Julia G. Prado, and Philip J. R. Goulder Bargielowski
An Evolutionary Perspective on
Parasitism as a Cause of Cancer
Paul W. Ewald
Volume 69
Invasion of the Body Snatchers:
The Diversity and Evolution of The Biology of the Caecal Trematode
Manipulative Strategies in Host– Zygocotyle lunata
Parasite Interactions Bernard Fried, Jane E. Huffman, Shamus
Thierry Lefévre, Shelley A. Adamo, David Keeler, and Robert C. Peoples
G. Biron, Dorothée Missé, David Fasciola, Lymnaeids and Human
Hughes, and Frédéric Thomas Fascioliasis, with a Global
Evolutionary Drivers of Parasite-Induced Overview on Disease Transmission,
Changes in Insect Life-History Epidemiology, Evolutionary
Traits: From Theory to Underlying Genetics, Molecular Epidemiology
Mechanisms and Control
Hilary Hurd Santiago Mas-Coma, María Adela Valero,
and María Dolores Bargues
Ecological Immunology of a Tapeworms’
Interaction with its Two Consecutive Recent Advances in the Biology of
Hosts Echinostomes
Katrin Hammerschmidt and Joachim Rafael Toledo, José-Guillermo Esteban, and
Kurtz Bernard Fried
Peptidases of Trematodes Components of Asobara Venoms and

Martin Kašný, Libor Mikeš, Vladimír their Effects on Hosts
Hampl, Jan Dvořák, Conor R. Caffrey, Sébastien J.M. Moreau, Sophie Vinchon,
John P. Dalton, and Petr Horák Anas Cherqui, and Geneviève Prévost
Potential Contribution of Sero- Strategies of Avoidance of Host Immune
Epidemiological Analysis for Defenses in Asobara Species
Monitoring Malaria Control and Genevie`ve Prévost, Géraldine Doury,
Elimination: Historical and Current Alix D.N. Mabiala-Moundoungou,
Perspectives Anas Cherqui, and Patrice Eslin
Chris Drakeley and Jackie Cook
Evolution of Host Resistance and
Parasitoid Counter-Resistance
Alex R. Kraaijeveld and H. Charles
Volume 70 J. Godfray
Ecology and Life History Evolution of Local, Geographic and Phylogenetic

Frugivorous Drosophila Parasitoids Scales of Coevolution in Drosophila–
Frédéric Fleury, Patricia Gibert, Nicolas Parasitoid Interactions
Ris, and Roland Allemand S. Dupas, A. Dubuffet, Y. Carton, and
M. Poirié
Decision-Making Dynamics in
Parasitoids of Drosophila Drosophila–Parasitoid Communities as
Andra Thiel and Thomas S. Hoffmeister Model Systems for Host–Wolbachia
Interactions
Dynamic Use of Fruit Odours to Locate Fabrice Vavre, Laurence Mouton,
Host Larvae: Individual Learning, and Bart A. Pannebakker
Physiological State and Genetic
Variability as Adaptive Mechanisms A Virus-Shaping Reproductive Strategy
Laure Kaiser, Aude Couty, and Raquel in a Drosophila Parasitoid
Perez-Maluf Julien Varaldi, Sabine Patot, Maxime
Nardin, and Sylvain Gandon
The Role of Melanization and Cytotoxic
By-Products in the Cellular Immune
Responses of Drosophila Against
Parasitic Wasps
A. Nappi, M. Poirié, and Y. Carton Volume 71
Virulence Factors and Strategies of Cryptosporidiosis in Southeast Asia:
Leptopilina spp.: Selective Responses What’s out There?
in Drosophila Hosts Yvonne A.L. Lim, Aaron R. Jex, Huw
Mark J. Lee, Marta E. Kalamarz, Indira V. Smith, and Robin B. Gasser
Paddibhatla, Chiyedza Small, Roma
Rajwani, and Shubha Govind Human Schistosomiasis in the Economic
Community of West African States:
Variation of Leptopilina boulardi Success in Epidemiology and Control
Drosophila Hosts: What is Inside the Héléne Moné, Moudachirou Ibikounlé,
Black Box? Achille Massougbodji, and Gabriel
A. Dubuffet, D. Colinet, C. Anselme, Mouahid
S. Dupas, Y. Carton, and M. Poirié
The Rise and Fall of Human
Immune Resistance of Drosophila Hosts Oesophagostomiasis
Against Asobara Parasitoids: Cellular A.M. Polderman, M. Eberhard, S. Baeta,
Aspects Robin B. Gasser, L. van Lieshout,
Patrice Eslin, Geneviève Prévost, Sébastien P. Magnussen, A. Olsen, N.
Havard, and Géraldine Doury Spannbrucker, J. Ziem, and J. Horton
Volume 72 Combating Taenia solium Cysticercosis

in Southeast Asia: An Opportunity
Important Helminth Infections in for Improving Human Health and
Southeast Asia: Diversity, Potential Livestock Production Links
for Control and Prospects for A. Lee Willingham III, Hai-Wei Wu, James
Elimination Conlan, and Fadjar Satrija
Jürg Utzinger, Robert Bergquist, Remigio
Olveda, and Xiao-Nong Zhou Echinococcosis with Particular Reference
to Southeast Asia
Escalating the Global Fight Against Donald P. McManus
Neglected Tropical Diseases Through
Interventions in the Asia Pacific Food-Borne Trematodiases in Southeast
Region Asia: Epidemiology, Pathology,
Peter J. Hotez and John P. Ehrenberg Clinical Manifestation and Control
Banchob Sripa, Sasithorn Kaewkes,
Coordinating Research on Neglected Pewpan M. Intapan, Wanchai
Parasitic Diseases in Southeast Asia Maleewong, and Paul J. Brindley
Through Networking
Remi Olveda, Lydia Leonardo, Feng Helminth Infections of the Central
Zheng, Banchob Sripa, Robert Nervous System Occurring in
Bergquist, and Xiao-Nong Zhou Southeast Asia and the Far East
Shan Lv, Yi Zhang, Peter Steinmann,
Neglected Diseases and Ethnic Minorities Xiao-Nong Zhou, and Jürg Utzinger
in the Western Pacific Region:
Exploring the Links Less Common Parasitic Infections in
Alexander Schratz, Martha Fernanda Southeast Asia that can Produce
Pineda, Liberty G. Reforma, Nicole Outbreaks
M. Fox, Tuan Le Anh, L. Tommaso Peter Odermatt, Shan Lv, and Somphou
Cavalli-Sforza, Mackenzie Sayasone
K. Henderson, Raymond Mendoza, Jürg
Utzinger, John P. Ehrenberg,
and Ah Sian Tee Volume 73
Controlling Schistosomiasis in Southeast Concepts in Research Capabilities
Asia: A Tale of Two Countries Strengthening: Positive Experiences
Robert Bergquist and Marcel Tanner of Network Approaches by TDR in
Schistosomiasis Japonica: Control and the People’s Republic of China and
Research Needs Eastern Asia
Xiao-Nong Zhou, Robert Bergquist, Lydia Xiao-Nong Zhou, Steven Wayling, and
Leonardo, Guo-Jing Yang, Kun Yang, Robert Bergquist
M. Sudomo, and Remigio Olveda Multiparasitism: A Neglected Reality on
Schistosoma mekongi in Cambodia Global, Regional and Local Scale
and Lao People’s Democratic Peter Steinmann, Jürg Utzinger, Zun-Wei
Republic Du, and Xiao-Nong Zhou
Sinuon Muth, Somphou Sayasone, Health Metrics for Helminthic Infections
Sophie Odermatt-Biays, Samlane Charles H. King
Phompida, Socheat Duong,
and Peter Odermatt Implementing a Geospatial Health
Data Infrastructure for Control
Elimination of Lymphatic Filariasis in of Asian Schistosomiasis in the
Southeast Asia People’s Republic of China and the
Mohammad Sudomo, Sombat Chayabejara, Philippines
Duong Socheat, Leda Hernandez, John B. Malone, Guo-Jing Yang, Lydia
Wei-Ping Wu, and Robert Bergquist Leonardo, and Xiao-Nong Zhou
The Regional Network for Asian Studies on the Parasitology,

Schistosomiasis and Other Phylogeography and the Evolution
Helminth Zoonoses (RNAS+): of Host–Parasite Interactions for
Target Diseases in Face of Climate the Snail Intermediate Hosts of
Change Medically Important Trematode
Guo-Jing Yang, Jürg Utzinger, Shan Lv, Genera in Southeast Asia
Ying-Jun Qian, Shi-Zhu Li, Qiang Stephen W. Attwood
Wang, Robert Bergquist, Penelope
Vounatsou, Wei Li, Kun Yang, and
Xiao-Nong Zhou
Volume 74
Social Science Implications for Control
of Helminth Infections in Southeast The Many Roads to Parasitism: A Tale of
Asia Convergence
Lisa M. Vandemark, Tie-Wu Jia, and Robert Poulin
Xiao-Nong Zhou Malaria Distribution, Prevalence, Drug
Towards Improved Diagnosis of Resistance and Control in Indonesia
Zoonotic Trematode Infections in Iqbal R.F. Elyazar, Simon I. Hay, and
Southeast Asia J. Kevin Baird
Maria Vang Johansen, Paiboon Cytogenetics and Chromosomes of
Sithithaworn, Robert Bergquist, and Tapeworms (Platyhelminthes,
Jürg Utzinger Cestoda)
The Drugs We Have and the Drugs Marta Špakulová, Martina Orosová, and
We Need Against Major Helminth John S. Mackiewicz
Infections Soil-Transmitted Helminths of Humans
Jennifer Keiser and Jürg Utzinger in Southeast Asia—Towards
Research and Development of Integrated Control
Antischistosomal Drugs in the Aaron R. Jex, Yvonne A.L. Lim, Jeffrey
People’s Republic of China: Bethony, Peter J. Hotez, Neil D. Young,
A 60-Year Review and Robin B. Gasser
Shu-Hua Xiao, Jennifer Keiser, The Applications of Model-Based
Ming-Gang Chen, Marcel Tanner, and Geostatistics in Helminth
Jürg Utzinger Epidemiology and Control
Control of Important Helminthic Ricardo J. Soares Magalhães, Archie C.A.
Infections: Vaccine Development as Clements, Anand P. Patil, Peter W.
Part of the Solution Gething, and Simon Brooker
Robert Bergquist and Sara
Lustigman
Our Wormy World: Genomics, Volume 75
Proteomics and Transcriptomics in
East and Southeast Asia Epidemiology of American
Jun Chuan, Zheng Feng, Paul J. Brindley, Trypanosomiasis (Chagas Disease)
Donald P. McManus, Zeguang Han, Louis V. Kirchhoff
Peng Jianxin, and Wei Hu Acute and Congenital Chagas Disease
Advances in Metabolic Profiling of Caryn Bern, Diana L. Martin,
Experimental Nematode and and Robert H. Gilman
Trematode Infections Cell-Based Therapy in Chagas Disease
Yulan Wang, Jia V. Li, Jasmina Saric, Antonio C. Campos de Carvalho,
Jennifer Keiser, Junfang Wu, Jürg Adriana B. Carvalho, and Regina C.S.
Utzinger, and Elaine Holmes Goldenberg
Targeting Trypanosoma cruzi Sterol Volume 76

14α-Demethylase (CYP51)
Galina I. Lepesheva, Fernando Villalta, and Bioactive Lipids in Trypanosoma cruzi
Michael R. Waterman Infection
Fabiana S. Machado, Shankar Mukherjee,
Experimental Chemotherapy and Louis M. Weiss, Herbert B. Tanowitz,
Approaches to Drug Discovery for and Anthony W. Ashton
Trypanosoma cruzi Infection
Frederick S. Buckner Mechanisms of Host Cell Invasion by
Trypanosoma cruzi
Vaccine Development Against Kacey L. Caradonna and Barbara A.
Trypanosoma cruzi and Chagas Burleigh
Disease
Juan C. Vázquez-Chagoyán, Shivali Gap Junctions and Chagas Disease
Gupta, and Nisha Jain Garg Daniel Adesse, Regina Coeli
Goldenberg, Fabio S. Fortes, Jasmin,
Genetic Epidemiology of Chagas Dumitru A. Iacobas, Sanda Iacobas,
Disease Antonio Carlos Campos de Carvalho,
Sarah Williams-Blangero, John L. Maria de Narareth Meirelles, Huan
VandeBerg, John Blangero, and Rodrigo Huang, Milena B. Soares, Herbert B.
Corrêa-Oliveira Tanowitz, Luciana Ribeiro Garzoni, and
Kissing Bugs. The Vectors of Chagas David C. Spray
Lori Stevens, Patricia L. Dorn, Justin O. The Vasculature in Chagas Disease
Schmidt, John H. Klotz, David Lucero, Cibele M. Prado, Linda A. Jelicks,
and Stephen A. Klotz Louis M. Weiss, Stephen M. Factor,
Advances in Imaging of Animal Models Herbert B. Tanowitz, and Marcos A.
of Chagas Disease Rossi
Linda A. Jelicks and Herbert B. Tanowitz Infection-Associated Vasculopathy
The Genome and Its Implications in Experimental Chagas Disease:
Santuza M. Teixeira, Najib M. El-Sayed, Pathogenic Roles of Endothelin and
and Patrícia R. Araújo Kinin Pathways
Julio Scharfstein and Daniele Andrade
Genetic Techniques in Trypanosoma
cruzi Autoimmunity
Martin C. Taylor, Huan Huang, Edecio Cunha-Neto, Priscila Camillo
and John M. Kelly Teixeira, Luciana Gabriel Nogueira, and
Jorge Kalil
Nuclear Structure of Trypanosoma cruzi
Sergio Schenkman, Bruno dos Santos ROS Signalling of Inflammatory
Pascoalino, and Sheila C. Nardelli Cytokines During Trypanosoma cruzi
Infection
Aspects of Trypanosoma cruzi Stage Shivali Gupta, Monisha Dhiman, Jian-jun
Differentiation Wen, and Nisha Jain Garg
Samuel Goldenberg and Andrea Rodrigues
Ávila Inflammation and Chagas Disease:
Some Mechanisms and Relevance
The Role of Acidocalcisomes in the Stress André Talvani and Mauro M. Teixeira
Response of Trypanosoma cruzi
Roberto Docampo, Veronica Jimenez, Neurodegeneration and
Sharon King-Keller, Zhu-hong Li, and Neuroregeneration in Chagas
Silvia N.J. Moreno Disease
Marina V. Chuenkova and Mercio
Signal Transduction in Trypanosoma cruzi PereiraPerrin
Huan Huang
Adipose Tissue, Diabetes and Chagas Aaron R. Jex, Huw V. Smith, Matthew
Disease J. Nolan, Bronwyn E. Campbell, Neil
Herbert B. Tanowitz, Linda A. Jelicks, D. Young, Cinzia Cantacessi, and Robin
Fabiana S. Machado, Lisia Esper, B. Gasser
Xiaohua Qi, Mahalia S. Desruisseaux,
Assessment and Monitoring of
Streamson C. Chua, Philipp E. Scherer,
Onchocerciasis in Latin America
and Fnu Nagajyothi
Mario A. Rodríguez-Pérez, Thomas R.
Unnasch, and Olga Real-Najarro
Volume 77
Coinfection of Schistosoma (Trematoda) Volume 78
with Bacteria, Protozoa and
Gene Silencing in Parasites: Current
Helminths
Status and Future Prospects
Amy Abruzzi and Bernard Fried
Raúl Manzano-Román, Ana Oleaga,
Trichomonas vaginalis Pathobiology: Ricardo Pérez-Sánchez,
New Insights from the Genome Mar Siles-Lucas
Sequence
Giardia—From Genome to Proteome
Robert P. Hirt, Natalia de Miguel, Sirintra
R.C. Andrew Thompson, Paul Monis
Nakjang, Daniele Dessi, Yuk-Chien
Liu, Nicia Diaz, Paola Rappelli, Alvaro Malaria Ecotypes and Stratification
Acosta-Serrano, Pier-Luigi Fiori, and Allan Schapira, Konstantina Boutsika
Jeremy C. Mottram
The Changing Limits and Incidence of
Cryptic Parasite Revealed: Improved Malaria in Africa: 1939–2009
Prospects for Treatment and Control Robert W. Snow, Punam Amratia,
of Human Cryptosporidiosis Caroline W. Kabaria, Abdisalan M.
Through Advanced Technologies Noor, Kevin Marsh

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SERIES EDITORS

D. ROLLINSON S.I. HAY

AMSTERDAM • BOSTON • HEIDELBERG • LONDON

525 B Street, Suite 1900, San Diego, CA 92101-4495, USA

First edition 2012

Copyright © 2012 Elsevier Ltd. All rights reserved.

No part of this publication may be reproduced, stored in a retrieval system or

For information on all Academic Press publications

Printed and bound in UK

Contents 1.1. Introduction 3

Albuquerque, NM, USA,

Advances in Parasitology, Volume 79 © 2012 Elsevier Ltd.

1.5. Biodiversity – History in a Complex Northern Fauna 60

Abstract Diversity among assemblages of mammalian hosts and parasites in

Geography to a large extent determines climate and, in combination

The Earth’s northern circumpolar regions present landscapes of outstand-

At high latitudes, vulnerable systems of low diversity continue to

Latitude > 66° 33′N > 50° N

to free-living organisms. Parasitism, pathogens and diseases have not

1.2. NORTHERN SYSTEMS AND PARASITES – SETTING

Parasites are important components of terrestrial, aquatic and marine

TABLE 1.2 Why study parasites in the North?

1.2.1. Developing knowledge of parasite diversity in the North

1.2.2. Towards an integrated picture of parasite diversity

relevant to the range of zoonoses circulating among free-ranging hosts

(2) What are the ecological, historical and evolutionary determinants of

1.3. AN HISTORICAL (PHYSICAL–BIOLOGICAL)

History and climate interact across geography as determinants of faunal

(between 23 and 5.3Ma) as otherwise equitable climatological conditions

of continental shelf allowing biotic expansion between Eurasia and North

1.3.1. Exploring the Beringian connection

1.4. FAUNAL STRUCTURE – EVIDENCE FOR NORTHERN

Beringian parasite assemblages, both marine and terrestrial, represent

1.4.1. Faunas associated with terrestrial Carnivora

FIGURE 1.4 History for geographic expansion by phylogenetically disparate host–

Contemporary groups and species with protracted histories in north-

Parasite taxon Host association Distribution Species diversitya Processesb

Eric P. Hoberg et al.

of two Holarctic species (Koehler et al., 2009).

Northern Host–Parasite Assemblages

recognised zoonotic protozoans, tapeworms and nematodes that can

Canidae arose in the Eocene–Oligocene of North America and Eurasia

Alaska) and continental populations are now recognised (e.g. MacDon-

1.4.1.1. Trichinella and carnivorans

1.4.1.2. Soboliphyme baturini in Mustelidae

Soboliphyme baturini, a characteristic large nematode occurring in the stom-

histories relative to geography (Hoberg et al., in press-a). In these instances,

1.4.1.3. Taenia tapeworms and carnivorans

Considering foxes, T. polyacantha includes Eurasian (T. p polyacantha,

that geographic colonisation and guild dynamics related to common prey

1.4.1.4. Echinococcus spp. among canids

on St ­Lawrence Island, Alaska (Nakao et al., 2009). Such is also concordant

1.4.1.5. Diphyllobothrium spp

1.4.1.6. Other helminths among carnivorans

1.4.2. Faunas associated with Lagomorpha

among the helminths (e.g. Anoplocephalidae – Schizorchis and Mosgovoiya;

Parasite taxon Host association Distribution Species diversitya Processesb

d Nearctic Trichostrongylus are primarily in rodent or leporid definitive hosts.

Northern Host–Parasite Assemblages

extinct in Beringia but were continuous in habitats south of the Lauren-

involving small initial host populations and geographic colonisation

1.4.3. Faunas associated with Rodentia

Eric P. Hoberg et al.

Contents 1.1. Introduction 3

1.5. Biodiversity – History in a Complex Northern Fauna 60

1.2. NORTHERN SYSTEMS AND PARASITES – SETTING

1.2.1. Developing knowledge of parasite diversity in the North

1.2.2. Towards an integrated picture of parasite diversity

1.3. AN HISTORICAL (PHYSICAL–BIOLOGICAL)

1.3.1. Exploring the Beringian connection

1.4. FAUNAL STRUCTURE – EVIDENCE FOR NORTHERN

1.4.1. Faunas associated with terrestrial Carnivora

1.4.1.1. Trichinella and carnivorans

1.4.1.2. Soboliphyme baturini in Mustelidae

1.4.1.3. Taenia tapeworms and carnivorans

1.4.1.4. Echinococcus spp. among canids

on St Lawrence Island, Alaska (Nakao et al., 2009). Such is also concordant

1.4.1.5. Diphyllobothrium spp

1.4.1.6. Other helminths among carnivorans

1.4.2. Faunas associated with Lagomorpha

1.4.3. Faunas associated with Rodentia

widespread (Ryzhikov et al., 1978, 1979). Among cestodes, these include

1.4.4. Faunas associated with Artiodactyla

1.4.5. Human interfaces and occupation of the North

1.5. BIODIVERSITY – HISTORY IN A COMPLEX

Thus, there is an apparent interplay between vagility and specialisation

1.5.1. General biogeographic patterns

1.5.2. Mechanisms of faunal expansion in space and time

1.5.3. An integrated model for diversification – contributions

1.5.4. Mosaic faunas – consequences of episodic

1.5.4.1. Defining mosaic structure in space and time

1.5.5. Stories that parasites reveal

1.6. TOOLS FOR BIODIVERSITY DISCOVERY

1.7. PROBLEMS AND CHALLENGES TO BE RESOLVED

Contents 2.1. Introduction 101

2.3. Nematodes 113

2.1.1. The Arctic

2.1.2. Parasites in a changing Arctic

2.2. ARCTIC UNGULATE HOSTS

2.2.1. Caribou – Rangifer tarandus ssp.

2.2.2. Muskoxen – Ovibos moschatus ssp.

2.2.3. Moose – Alces americanus ssp.