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The Pathophysiology, Ecology and Epidemiology of

Haemonchus contortus Infection in Small Ruminants
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DOI: 10.1016/bs.apar.2016.02.022
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The Pathophysiology, Ecology

and Epidemiology of
Haemonchus contortus Infection
in Small Ruminants
R.B. Besier*, 1, L.P. Kahnx, N.D. Sargison{, J.A. Van Wykjj
*Department of Agriculture and Food Western Australia, Albany, WA, Australia
x
University of New England, Armidale, NSW, Australia
{
University of Edinburgh, Midlothian, United Kingdom
jj
University of Pretoria, Hatfield, South Africa
1
Corresponding author: E-mail: R.B.Besier@murdoch.edu.au
Contents
1. Introduction 2
2. Occurrence and Importance 3
2.1 Geographical distribution 3
2.1.1 Tropical and subtropical climates 4
2.1.2 Warm temperate regions 4
2.1.3 Cool temperate regions 5
2.1.4 Arid regions 5
2.2 Economic significance 6
3. Pathogenesis and Disease 7
3.1 Pathophysiology and pathogenesis 7
3.2 Clinical signs of disease 9
4. Ecology 12
4.1 Controlled environment studies 13
4.1.1 Moisture requirements for egg development and survival 13
4.1.2 Moisture requirements for the survival of infective larvae 16
4.1.3 Temperature requirements for the development of eggs to infective larvae 16
4.1.4 Temperature requirements for the survival of infective larvae 17
4.1.5 Intraspecific differences in critical requirements 18
4.1.6 Other environmental factors 19
4.2 Ecological investigations in the field 19
4.2.1 Tropical and subtropical climates 20
4.2.2 Warm, temperate and Mediterranean climates 22
4.2.3 Cool, temperate climates 23
4.2.4 Arid regions 24
4.2.5 Effect of microclimatic factors on larval development 25
4.2.6 Lateral and vertical migration of infective larvae 26
Advances in Parasitology, Volume 93

© 2016 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2016.02.022 All rights reserved. 1
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2 R.B. Besier et al.
5. Epidemiology 28
5.1 Tropical and subtropical regions 28
5.2 Warm, temperate climates 33
5.3 Cool temperate climates 34
5.4 Arid climates 35
6. Prediction of the Occurrence of H. contortus 36
6.1 Predictive models 36
6.2 Potential effects of climate change 37
7. Conclusions 38
References 39
Abstract
The parasitic nematode Haemonchus contortus occurs commonly in small ruminants,
and it is an especially significant threat to the health and production of sheep and goats
in tropical and warm temperate zones. The main signs of disease (haemonchosis) relate
to its blood-feeding activity, leading to anaemia, weakness and frequently to deaths,
unless treatment is provided. Due to the high biotic potential, large burdens of
H. contortus may develop rapidly when environmental conditions favour the free-living
stages, and deaths may occur with little prior warning. More chronic forms of haemon-
chosis, resulting in reduced animal production and eventually deaths, occur with
smaller persistent infections, especially in situations of prolonged, poor nutrition. The
global distribution of the main haemonchosis-endemic zones is consistent with the
critical requirements of the egg and larval stages of H. contortus for moisture and
moderate to relatively warm temperatures, but the seasonal propensity for hypobiosis
(inhibition of the fourth-stage larvae within the host) largely explains the common,
though sporadic, outbreaks of haemonchosis in arid and colder environments. The
wide climatic distribution may also reflect the adaptation of local isolates to less favour-
able ecological conditions, while an apparent increase in the prevalence of outbreaks in
environments not previously considered endemic for haemonchosis e especially cold,
temperate zones e may be attributable to climatic changes. Although the risk of
haemonchosis varies considerably on a local level, even where H. contortus is endemic,
the extensive range of ecological investigations provides a sound basis for predictions
of the relative geographical and seasonal risk in relation to climatic conditions.
1. INTRODUCTION
Haemonchus contortus is a highly pathogenic helminth, primarily of
small ruminants, with a global distribution. Due to its blood-feeding behav-
iour and the potential for the rapid development of large burdens, it is a
frequent cause of mortalities in sheep, goats and occasionally other
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Haemonchus contortus Infection in Small Ruminants 3
ruminants, and is the most important parasite of livestock in warm climatic

regions, and arguably on a global basis.
Although considered primarily a parasite of tropical and summer rainfall
zones, the ecological adaptability of H. contortus afforded by its high level of
genetic polymorphism and high biotic potential has seen it become increas-
ingly important over a wide range of climatic zones. The possible further
increase in its geographical range, especially due to climate change, could
lead to an increased prevalence of haemonchosis in presently low-risk areas.
In conjunction with an increasing severity of anthelmintic resistance, this
would further add to the costs of livestock production, and the necessity
to develop new and sustainable preventative strategies. This chapter reviews
the effects of H. contortus on host animals, and the ecological factors that
determine the occurrence and impact of H. contortus, as the basis for under-
standing its changing distribution and seasonality, and for developing control
strategies.
2. OCCURRENCE AND IMPORTANCE

2.1 Geographical distribution
The requirement of warm and moist environmental conditions for
the free-living stages of H. contortus governs the parasite’s geographical
and seasonal distributions. The prevalence of H. contortus and disease in
grazing animals is therefore particularly high in the tropical climatic zones
of both hemispheres, between latitudes 23.5 N and S (O’Connor et al.,
2006). However, H. contortus has proven to be remarkably adaptable
over a wide range of environments (Waller and Chandrawathani, 2005),
due to its high biotic potential which allows it to take advantage of
short periods which are favourable for the development of its free-living
stages, and the survival ability of the relatively robust infective third-stage
larvae (summarized in Table 1), and specific adaptive mechanisms, such as
hypobiosis of the fourth-stage larvae. Genetic differences in environmental
tolerance arising as a consequence of a high level of polymorphism may
confer a selective advantage to particular strains in the face of climate
change. Hence, H. contortus occurs in almost all regions where small rumi-
nants are raised, with the potential for outbreaks of haemonchosis, regard-
less of the climatic zone.
Due to its clinical and economic significance H. contortus is probably the
most studied of ruminant helminths, and the many ecological and
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epidemiological studies constitute a vast literature that defines its ecological

adaptability across many different environments. In this chapter, the distri-
bution of H. contortus is considered largely in relation to the availability of
moisture (rainfall) and the typical temperature range in different types of
environments, namely tropical, subtropical, temperate (warm and cool)
and arid regions (summarized in Table 2). Although information is not avail-
able from some regions, taken as a whole, the studies detailed in the
following sections provide an indication of the prevalence of H. contortus
and the severity of haemonchosis in a range of environments.
2.1.1 Tropical and subtropical climates

Due to continually high temperatures, most locations within these climatic
zones consistently support the larval development of H. contortus, and the
presence of this nematode relates almost entirely to rainfall. In the wet tro-
pics and equatorial zones, infective larvae are present on pasture essentially
throughout the year, and haemonchosis is a significant constraint to the
raising of small ruminants (eg, Barger et al., 1994; Chandrawathani, 2004;
Dorny et al., 1995). These regions include tropical Africa, South-East
Asia, tropical Pacific Island countries, Central America and countries in
the northern parts of South America and the Caribbean.
In subtropical and similar environments, seasonal variations in rainfall
largely determine whether H. contortus is a continual or, alternatively, a
routine seasonal threat, as generally high temperatures maintain the potential
for rapid population development. However, there is extensive variation in
the risk for haemonchosis throughout this zone, depending on the relative
length of dry seasons, and, in some cases, on the effects of altitude in moder-
ating temperatures (eg, Githigia et al., 2001; Shillhorn Van Veen, 1978). In
markedly seasonal climates with long and hot dry seasons, during which there
is negligible external survival of infective larvae, hypobiosis of the fourth-stage
larvae (Gibbs, 1986; Michel, 1974) allows H. contortus to survive until more
favourable conditions resume. Regions included are to the north and south
of the true tropics in Africa, Asia and the Americas, including some southern
regions of the USA, central and southern India and the north of Australia.
2.1.2 Warm temperate regions

Haemonchus contortus is a significant seasonal threat in the warmer temperate
climatic zones, as temperatures are sufficiently high to permit development
for several months of the year, and winters not sufficiently severe for a pro-
longed, restrictive effect on infective larvae. The major restrictions are
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seasonally dry conditions or droughts, although winter temperatures typi-

cally limit egg development for part of the year, particularly when combined
with altitude. The severity is greatest in summer rainfall regions (Swan,
1970; Veglia, 1915), and whether larval development is constant or sporadic
throughout summer depends mostly on the pattern of rainfall. In predom-
inately winter rainfall areas in this zone, haemonchosis usually occurs more
sporadically but is still a seasonally endemic threat, also depending on the dis-
tribution of summer rainfall. Where significant small ruminant populations
occur, affected regions extend from the tropics to around 35 N and S,
including in southern Africa, much of eastern Australia, parts of southern
USA, mid-regions of South America, southern Asia and Mediterranean
climatic zones in both hemispheres.
2.1.3 Cool temperate regions

Outside the major endemic zones, longer periods of cold conditions restrict
the annual availability of H. contortus, although seasonally dry conditions are
usually less important, as the infective larvae can survive for relatively long pe-
riods. Haemonchosis may be a significant annual, although short lived, threat
where summer temperatures are sufficiently high and sustained, including lat-
itudes >35 S in the southern hemisphere, and >45 N in Europe and north-
ern America and Asia. The risk diminishes as latitude increases, with only
sporadic outbreaks where specific circumstances favour H. contortus develop-
ment. In colder zones, H. contortus is generally of minor and brief significance,
and its annual survival usually associated with hypobiosis (Gibbs, 1986). How-
ever, there are concerns regarding an increasing importance of H. contortus in
regions in which development is constrained to short periods in summer, such
as in northern Europe, Scandinavia and Canada (Waller and Chandrawathani,
2005; Rinaldi et al., 2015). The climate change trends are likely to extend the
range of H. contortus and other parasites (Van Dijk et al., 2010) in all environ-
ments where cold or dry conditions might limit its present significance.
2.1.4 Arid regions

Due to the requirement for moisture for development of the free-living
stages, haemonchosis is of relatively lesser importance in arid zones, but out-
breaks occur in hotter climates where brief seasonal rainfall permits rapid larval
development. This may occur routinely due to the maturation of hypobiotic
larvae after annual dry seasons, such as in southern and sub-Saharan Africa
(Shillhorn Van Veen and Ogunsusi, 1978; Vercruysse, 1985; Viljoen, 1969)
and the Middle East (Altaif and Issa, 1983), or rarely following unusually
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protracted periods of rainfall, such as in the dry inland of northern Australia

(De Chaneet and Mayberry, 1978). In many situations, H. contortus infection
probably persists only because anthelmintic treatment is rarely considered
justified, although it may be a threat on irrigated pastures in these zones (Altaif
and Yakoob, 1987; Pullan and Megadmi, 1983). There are few instances
where arid conditions occur in colder climates, but the dual pressures of
extremely dry conditions and low temperatures would severely restrict the
expansion of H. contortus populations (Viljoen, 1969).
2.2 Economic significance

Haemonchosis is recognized as the most economically important parasitic
nematode in its main endemic zones (McLeod, 2004; Perry et al., 2002),
chiefly due to the common occurrence and potential for heavy mortality
rates in small ruminants. Animal losses vary greatly between regions, years
and seasons, depending on environmental conditions and the effectiveness
of control measures, including the impact of anthelmintic resistance. The
immediate economic impact is greatest when animals are managed under
intensive commercial conditions in endemic areas. However, the losses
experienced in traditional livestock systems when small numbers of animals
are run under extensive conditions are proportionately greater at particular
times, and often exacerbated by periods of poor nutrition and the limited
availability and affordability of anthelmintics, as well as anthelmintic resis-
tance (Vatta and Lindberg, 2006).
In a study in an H. contortus endemic area in New South Wales, Australia,
annual mortalities in Merino ewes of >10% were largely attributed to hae-
monchosis on farms with relatively unplanned control practices (Kelly et al.,
2010), although there was a large between-year variation. The mean annual
cost of AUD 11.00/head was associated chiefly (80%) with ewe deaths but
included the control measures (anthelmintics and diagnostic tests) required
to treat and prevent haemonchosis. The impact of chronic H. contortus infec-
tion is difficult to assess, as it is most significant in extensive grazing situations
where routine monitoring is rarely conducted, but Qama et al. (2012) attrib-
uted substantial loss to the reduced value of animal production, and Fabiyi
(1987) reported substantial losses due to mixed helminth infections in a
number of African countries, mostly related to H. contortus. In many cases,
mortalities eventually occur after some months of infection and in associa-
tion with poor nutritional conditions (Allonby and Urquhart, 1975).
Anthelmintic resistance is well established in all major zones endemic for
H. contortus, often precluding the use of entire anthelmintic groups, thus
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exacerbating the costs and complexity of control (chapter: Diagnosis,

Treatment and Management of Haemonchus contortus in Small Ruminants
by Besier et al., 2016; chapter: Anthelmintic Resistance in Haemonchus con-
tortus: History, Mechanisms and Diagnosis by Kotze and Prichard, 2016).
3. PATHOGENESIS AND DISEASE

3.1 Pathophysiology and pathogenesis
Haemonchus contortus is by far the most pathogenic of the common
nematodes of small ruminants, due to its blood-feeding activity and its ca-
pacity for rapid population increases during periods and under conditions
favouring the development of the free-living stages. The pathophysiology
of haemonchosis and associated clinical signs are chiefly linked to the
anaemia that develops as a consequence of the blood-feeding activity of
the parasite (Dunn, 1978; Levine, 1980; Urquhart et al., 1996). Blood loss
commences with the development of the fourth-stage larvae (M€ onnig,
1950; Veglia, 1915), with anaemia being first detectable 10e12 days after
infection (Dargie and Allonby, 1975; Hunter and McKenzie, 1982). Indi-
vidual adult worms are estimated to remove 30e50 mL of blood per day
(Clarke et al., 1962; Dargie and Allonby, 1975), and a daily blood loss of
30 mL has been reported in sheep 11 days after infection with 10,000 infec-
tive larvae of H. contortus (see Albers and Le Jambre, 1983). The severity of
disease in the host is closely related to the number of H. contortus larvae that
establish, as there is a strong correlation between blood loss and the number
of adult worms (Le Jambre, 1995). The outcome of H. contortus infection
therefore depends largely on the rate of intake of infective larvae, the ability
of the host to reject them and the capacity to replace lost blood.
Depending on the intensity of infection and the host response, haemon-
chosis has been categorized into a continuum of three general syndromes:
hyperacute, acute and chronic (Dunn, 1978; Urquhart et al., 1996). In
the relatively rare hyperacute form, massive blood loss from infection
with as many as 30,000 H. contortus causes a haemorrhagic gastritis, in
addition to terminal anaemia (Dunn, 1978). Deaths occur suddenly with
no premonitory signs of disease, but with signs of severe anaemia in many
of the survivors. The diagnosis is obvious at necropsy due to very large
numbers of worms of different developmental stages, and numerous obvious
haemorrhages on the mucosal surface.
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In acute haemonchosis, significant anaemia develops over a relatively

longer period, but deaths may occur within 4e6 weeks of infection,
depending on the rate of larval intake. H. contortus burdens of 2000e
20,000 worms per sheep may be present (Urquhart et al., 1996), with faecal
worm egg counts (FWECs) of 50,000 eggs per gram (Dunn, 1978). Dargie
and Allonby (1975) defined three stages in the progression of anaemia during
acute haemonchosis, with an initial decrease in packed cell volume (PCV)
over about 6 weeks following infection, and an apparent recovery due to
compensatory erythropoiesis in animals that survived. However, over the
following weeks a dramatic and terminal reduction in PCV can occur due
to exhaustion of the capacity to replace blood cells, due in part to depletion
of the iron reserves. At necropsy, the carcass is pale with marked ascites and
submandibular oedema, reflecting the hypoproteinaemia which also results
from the blood-feeding activity of H. contortus. The blood may be watery
and fail to clot, and the abomasal mucosa is often oedematous with
blood-flecked mucous and obvious signs of parasite attachment. The histo-
pathological changes associated with acute haemonchosis include traumatic
damage to the mucosal surface and evidence of a cellular immunological
response (Hunter and McKenzie, 1982; Silverman and Paterson, 1960).
Infections with smaller but persistent H. contortus burdens have been
characterized as ‘chronic haemonchosis’ (Allonby and Urquhart, 1975;
Dunn, 1978), which may pass unnoticed or become obvious only when
larval intake and, hence, worm burdens increase, or when poor nutritional
conditions reduce the capacity of the host to tolerate the pathogenic effects.
The syndrome was first characterized on the basis of observations made in
Kenya (Allonby and Urquhart, 1975) and in pastoral grazing environments
in Australia, where rainfall is relatively low and variable between seasons,
and small burdens of worms persist (Cobon and O’Sullivan, 1992; De
Chaneet and Mayberry, 1978; Roberts and Swan, 1981). Chronic haemon-
chosis is most common in environments which are marginal for the
development of the free-living stages, or during less favourable periods in
seasonally endemic zones, and is usually accompanied by infections with
other helminths. The chronic form of haemonchosis may also occur where
overt outbreaks are common but partially effective control measures prevent
the emergence of acute haemonchosis.
Nutritional status has a major role in the tolerance of H. contortus infec-
tion, and overt haemonchosis can be precipitated by a reduction in feed
quality. A sharp differential in the tolerance (or resilience) to H. contortus
has been demonstrated in pen-kept sheep on extremely low-protein ratios
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compared with those in groups receiving feed supplements (Abbott et al.,

1986a; Nnadi et al., 2009; Wallace et al., 1996), even though there was
no significant change in worm numbers (Abbott et al., 1986b; Wallace
et al., 1996). Loss of milk production might also be associated with small
but chronic burdens of H. contortus in sheep (Thomas and Ali, 1983) and
goats (Nnadi et al., 2009), and partial agalactia in ewes may add to the less
obvious effects of H. contortus infections by reducing lamb growth. The pro-
duction effects of chronic H. contortus infection in sheep on low planes of
nutrition relate to a negative nitrogen balance (Abbott et al., 1985a;
Rowe et al., 1988), and, to a degree, to inappetance (Abbott et al.,
1985a; Holmes, 1987), as commonly occurs for infections with many tri-
chostrongyle species (Fox, 1997). As expected, the benefits of protein sup-
plementation to enhance the resistance and resilience of sheep against H.
contortus infection is greatest in breeds or individual sheep that are more sus-
ceptible to helminthosis (cf. Abbott et al., 1985b; Kahn et al., 2003; Steel,
2003). In addition, the potential for differences in pathogenicity among
H. contortus strains has been implied by results from a number of studies,
including those of Hunt et al. (2008), who reported both genomic and phys-
iological differences between Australian strains, and also Angulo-Cubillan
et al. (2010) who found differences between Spanish and Scottish strains.
3.2 Clinical signs of disease

The clinical signs of H. contortus infection depend upon the number of
haematophagous adult and larvae present in the abomasum, and the varia-
tion in susceptibility among individual animals and, to an extent, on their
nutritional status. The visible evidence presented to livestock owners and
veterinarians varies considerably both over time and within a flock, and a
classic outline of the progression of haemonchosis from inapparent infection
to the commencement of mortalities was originally described by Clunies-
Ross and Gordon (1936; cited in Georgi, 1974). Detailed descriptions of
the clinical signs (and associated pathophysiology) are available in numerous
veterinary and parasitology texts (eg, Bowman, 2014; Dunn, 1978; Levine,
1980; Taylor et al., 2007; Urquhart et al., 1996).
The principal clinical signs in individual host animals relate almost entirely
to the degree of anaemia associated with the size and duration of H. contortus
infection, but this expression is mediated by a number of factors. No age or
class of animal is specifically associated with haemonchosis, although the dis-
ease is probably most common in lambs that have not acquired natural, pro-
tective immunity against helminths. However, it is also seen in lactating ewes
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and does (presumably under the influence of the peri-parturient relaxation of

resistance; O’Sullivan and Donald, 1973), and occasionally in helmintholog-
ically naive adult animals which have been newly introduced into an H. con-
tortuseendemic zone. In addition to the very marked natural variation in
immunological responses among individuals within a flock or herd, which
can be exploited for the breeding of naturally resistant (Preston and Allonby,
1979; Woolaston and Baker, 1996) or resilient animals (Bissett and Morris,
1996), there is a large variation among breeds in their resistance to haemon-
chosis (Mugambi et al., 1997; Preston and Allonby, 1979), with a significant
advantage to locally adapted breeds (chapter: Diagnosis, Treatment and
Management of Haemonchus contortus in Small Ruminants by Besier et al.,
2016). As indicated above, the nutritional state of affected animals can have
a significant influence on the expression of haemonchosis (McArthur et al.,
2013), as would concurrent infection with other parasites or other diseases.
In hyperacute cases, sudden deaths occur without prior signs to alert an
owner, but the signs of anaemia typical of acute haemonchosis will be
evident in most individuals that survive. These signs include pallor of the
mucous membranes, most readily seen in the conjunctivae. The close rela-
tionship between colour of the ocular membranes and the degree of anaemia
is the basis of the FAMACHA (FAffa MAlan CHArt; Malan et al., 2001) sys-
tem for assessing the risk for haemonchosis in a group of animals, expressed
as a score of 1e5, ranging from a red-pink (normal) colour to an extreme
white in terminal situations (Van Wyk and Bath, 2002). Affected animals
become progressively weaker with increasing blood loss, and may be less in-
clined to move, or spend more time lying down than usual. On driving,
some will collapse and may die, particularly if repeatedly forced to move
(ironically, often for anthelmintic treatment). At this stage, treatment is often
undertaken, but if the disease progresses, the hypoproteinaemia due to blood
loss may lead to general ventral oedema in a proportion of animals. Subman-
dibular oedema (‘bottle jaw’) is also typically seen, although this sign is not
pathognomonic for haemonchosis, and deaths may occur before it develops.
Diarrhoea is not a feature of haemonchosis, and the faeces are typically firm,
scant and may be dark (due to melaena), although haemonchosis may occur
concurrently with infections with other nematodes that do cause diarrhoea
(Eysker and Ogunsusi, 1980). No pain is evident, but a ‘break in the wool’ of
sheep occasionally occurs, with shedding of strands of wool or even the
entire fleece in recovered or chronically affected animals.
Acutely developing outbreaks of haemonchosis are not immediately
associated with observable animal production losses, but, if allowed to
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progress, substantial effects on live-weight gain and (in sheep) wool growth
can occur. Pen studies in New South Wales showed a mean reduction of
38% in animal growth rates after 9 weeks of H. contortus infection in lambs,
which led to clinical haemonchosis, although wool growth loss was not
evident for some weeks, with a mean reduction of only 7% (Albers et al.,
1989). Similarly, in observations on haemonchosis in grazing sheep, also
in New South Wales, no animal production effects were apparent in affected
sheep at the time that mortalities occurred, but with continued infection,
both live-weight gains and wool growth were significantly reduced (Cohen
et al., 1972). However, observations on the animal production implications
for the FAMACHA system indicated that, despite high FWECs of >10,000
eggs per gram in individual sheep, there was little associated reduction in
live-weight, by comparison with sheep drenched at monthly intervals
(Van Wyk, 2008). This information suggests that, if treatment can be pro-
vided when imminent haemonchosis is detected, a significant production
penalty is not inevitable.
In more chronic forms of haemonchosis, signs may be similar to malnu-
trition, seen as weight loss or poor weight gains and general ill-thrift, and a
degree of anaemia in some individuals. Depending on the nutritional status,
minor infections would need to continue for a considerable period before a
significant animal production impact is evident. Barger and Cox (1984)
observed only a small reduction (3%) in the live-weights of yearling sheep
on good pasture over a 12-week period of low-level H. contortus challenge,
and no significant effect on wool production. However, in poorly nourished
animals, chronic H. contortus infection is often associated with a loss in animal
production. In a pen experiment in Indonesia, a daily reduction in live-
weight growth (w30 g per day) was recorded in both sheep and goats
with small burdens of H. contortus (Beriajaya and Copeman, 2006). Similarly,
in pen experiments in the Philippines, Howlader et al. (1997) reported a
reduction of 25% in the growth rates of goats with subclinical haemonchosis.
Losses associated with chronic, subclinical H. contortus infection in grazing
Merino sheep were also reported from an arid environment in inland
Queensland, Australia, with a significant reduction in weight gains and
wool growth in all ages, and a reduction in both the milk yield of ewes
and lamb survival (Cobon and O’Sullivan, 1992). Similarly, continual infec-
tion with moderate worm burdens, predominately H. contortus, led to
reduced live-weight gains in grazing goats in Kenya (Githigia et al.,
2001), with mortalities during seasonal periods of poor nutrition, mostly
in animals with the poorest body condition. As noted previously, it is likely
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that unsuspected chronic haemonchosis occurs relatively common in situa-

tions where small burdens are maintained for some months due to limited
larval intake or where partially effective treatment prevents its overt expres-
sion, and that the expression of clinical signs is largely nutritionally mediated.
4. ECOLOGY
The geographical and seasonal distributions of parasitic nematodes
with a free-living component of the life cycle is determined by the effects
of the external environment on the development of eggs through the first-
to third-larval stages, and by the survival of the infective larvae on herbage
(Crofton, 1963; Levine, 1980). For each species, a critical minimum require-
ment for moisture within the faecal pellet and on the herbage determines the
viability of the egg and various larval stages, and development between these
stages occurs at an increasing rate as temperature increases from a minimum
value over a defined range. In general, trichostrongyle eggs either develop to
infective larvae relatively rapidly (within one or more days) or die before
reaching this stage (Crofton, 1963; Levine, 1980; Stromberg, 1997; Veglia,
1915). In contrast, the infective larvae are considerably resilient, and can sur-
vive on pasture for periods of some months, provided that temperatures are
not extreme and moisture is sufficient (O’Connor et al., 2006).
Due to its importance, H. contortus is probably the best studied nematode
of ruminants in relation to ecological factors that determine the viability of
the egg and larval stages. In comparison with other trichostrongyles, such as
Teladorsagia circumcincta and Trichostrongylus colubriformis, the free-living stages
of H. contortus have a more stringent requirement for moisture, a lower toler-
ance of low temperatures, and a greater requirement for and tolerance for
warm temperatures (O’Connor et al., 2006). Investigations to establish crit-
ical values for the development and survival of free-living stages include
in vitro laboratory studies, in which eggs isolated from host faeces or larvae
at various stages can be exposed to controlled environmental conditions, and
field plot studies to indicate the integrated effects of ecological factors,
mostly climatic measurements. Further studies, utilizing grazing animals to
sample pasture contaminated at defined times provide a basis for explaining
the epidemiology of infections in different locations. In all cases, compari-
sons among studies must be interpreted with caution, due to differences
in observation intervals and other procedural variations, and particularly in
relation to older studies, the sensitivity of technology used to measure
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environmental variables, as well as for estimations of egg and larval numbers.

The possibility of between-strain variation cannot be discounted as an expla-
nation of varying results, because evidence from direct comparisons suggests
that adaptive responses occur in relation to environmental variation
(Crofton and Whitlock, 1965; Le Jambre and Whitlock, 1976).
4.1 Controlled environment studies

In general, in vivo investigations with the free-living stages of nematodes
indicate the critical range of values for key factors, principally moisture
and temperature, and thus the absolute environmental boundaries for the
occurrence of a particular species. While observations within individual
studies extend only over a predetermined set of values and usually for a single
variable, taken together, numerous studies provide a comprehensive indica-
tion of the specific ecological requirements. A summary of the critical values
for environment variables is provided in Table 1.
4.1.1 Moisture requirements for egg development and survival

Early investigations established the critical requirement for moisture for
development beyond the egg stage, and that embryonated H. contortus
eggs are considerably more resistant to desiccation than eggs that have not
commenced development (Berberian and Mizelle, 1957; Shorb, 1944b;
Veglia, 1915). Most H. contortus eggs die if allowed to desiccate, but the sur-
vival period increases as the relative humidity or faecal moisture content
(FMC) increases (Berberian and Mizelle, 1957; Rose, 1963; Waller and
Donald, 1970), and once eggs have embryonated they hatch rapidly when
exposed to moisture (Silverman and Campbell, 1959; Waller and Donald,
1970). Desiccation tolerance appears to be determined largely by the perme-
ability of the exterior egg membrane to water, as Waller and Donald (1970)
found structural differences between the membranes of T. colubriformis and
H. contortus that related to the greater survival of T. colubriformis eggs at
low humidity values.
The interactions between moisture and temperature for H. contortus egg
development are evident from experiments in which temperature and rela-
tive humidity were cycled; over the relatively high temperature range of
20e35 C, no eggs developed at low humidity levels (70e85%), but most
eggs produced infective larvae at 100% relative humidity (Hsu and Levine,
1977). However, the period of time for which eggs were exposed to low
humidity was critical, as substantial development occurred provided that
low humidity (70%) was maintained for only 12 h before an increase to
Table 1 Effects of environmental factors on the free-living stages of Haemonchus contortus under controlled conditions (Section 4.1)
14
Aspect investigated Environmental factor Optimal conditions (key references) Limiting conditions (key references)
Development and Moisture Relative humidity 100% at 20e35 C Relative humidity <85% in faecal
survival of eggs (in faecal pellets) (Hsu and Levine, pellets at 20e35 C (Hsu and Levine,
(unembryonated) 1977) 1977; Misrah and Ruprah, 1973a;
‘Moist faeces’ (Rose, 1963) Shorb, 1944a,b)
‘Dry air, unshaded’ (Veglia, 1915)
Development and Moisture ‘Shaded faecal pellets’ in dry air Relative humidity <88% at 20 C
survival of eggs (development and survival) (Veglia, (Waller and Donald, 1970)
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(embryonated) 1915)
Dry faecal pellets at room temperature
(survival) (Silverman and Campbell,
1959)
Survival of eggs Low temperature 0e4 C (<10 days) (Shorb, 1944a,b; <0 C (Jasmer et al., 1986; Rose, 1964;
(unembryonated) Silverman and Campbell, 1959; Todd et al., 1976b)
Smith-Bujis and Borgesteede, 1986)
Survival of eggs Low temperature 0e4 C (2 months) (Silverman and <0 C (Rose, 1964; Todd et al., 1976b)
(embryonated) Campbell, 1959; Todd et al., 1976b;
Veglia, 1915)
Development of eggs to Temperature (no Rapid development, high proportion Slow development, low proportion of
infective larvae moisture restriction) hatch: w15 C: 4e12 days (Misrah hatch: <8 C, no development
and Ruprah, 1973a; Rose, 1964; (Crofton and Whitlock, 1965;
Veglia, 1915) 22e25 C: 3e7 days Silverman and Campbell, 1959;
(Berberian and Mizelle, 1957; Hsu Veglia, 1915)
and Levine, 1977; Rose, 1964; 10 C: w2e4 weeks (Veglia, 1915)
R.B. Besier et al.

Silverman and Campbell, 1959; 40 C: little/no development
Veglia, 1915) 35e37 C: 3 days (Berberian and Mizelle, 1957; Jehan
(Jehan and Gupta, 1974; Silverman and Gupta, 1974; Veglia, 1915)
and Campbell, 1959; Veglia, 1915)
Survival of infective Moisture (desiccated; Relative humidity 60e90%: w20 C: 8 Relative humidity <50%: >w20 C:
larvae <100% relative e36 weeks (Rose, 1963; M€ onnig, few days to 3 weeks (Ellenby, 1968;
humidity) 1930; Todd et al., 1970; Todd et al., Rose, 1963; Todd et al., 1970)
1976a) w30 C: 1e8 weeks (Todd
et al., 1970; 1976a)
Survival of infective Temperature (no Optimum (>20 weeks, relatively high Minimum (<20 weeks, low
larvae moisture restriction) proportion): 5e10 C: >12 months proportion): <0 C: few days (Jasmer
(Boag and Thomas, 1985; Misra, et al., 1987; Rose, 1963; Todd et al.,
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1978; Rose, 1963; Todd et al., 1976b)
1976b) 35e40 C: 1e9 weeks (Jehan and
15e20 C: 32e56 weeks (Boag and Gupta, 1974; Misra, 1978; Sood and
Thomas, 1985; Todd et al., 1976b) Kapur, 1975)
25e30 C: 17e36 weeks (Boag and >40 C: few days (Jehan and Gupta,
Thomas, 1985; Jehan and Gupta, 1974; Misra, 1978; Sood and Kapur,
1974; Rose, 1963; Todd et al., 1975; Todd et al., 1976b; Veglia,
1976b) 1915)
15
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100%. Incubator and small plot studies (Khadijah et al., 2013a,b; O’Connor
et al., 2007a,b, 2008; discussed in the following section) confirm the critical
role of moisture for the development of H. contortus eggs to infective larvae
during the short period of time after they are deposited onto pasture.
4.1.2 Moisture requirements for the survival of infective larvae

The remarkable survival capacity of infective larvae of trichostrongyle nem-
atodes on pasture during dry conditions is a key explanatory feature of the
epidemiology of infections in livestock. It has long been noted that the L3
(infective) larvae are relatively resistant to desiccation, and can survive stor-
age in a dry state on glass slides at room temperature (22e24 C) for
2 months (M€ onnig, 1930; Rose, 1963), provided that the relative humid-
ity is sufficiently high. With a low relative humidity but similar temperature
conditions, the survival is lower. Ellenby (1968) found desiccated infective
larvae of H. contortus to survive in vitro for a maximum of 3 weeks at 47%
relative humidity and a temperature of 18 C. The percentage surviving
declines as the relative humidity decreases (Rose, 1963; Todd et al.,
1970), although survival is closely related to temperature: at 60% relative hu-
midity, survival decreased from 64 days at 20 C, to 8 days at 35 C (Todd
et al., 1976a).
The environmental resistance of the infective larva has long been associ-
ated with the larval sheath, which is retained after the second moult. Ellenby
(1968) showed that exsheathed larvae survived for only a few hours
compared with up to 3 weeks when the sheath was retained. Survival is
also enhanced in faecal pellets, with larvae found to be viable in faeces after
256 days at 20 C and a relative humidity of 60%, compared with only
64 days for desiccated larvae on glass under the same conditions (Todd
et al., 1976a). As well as ensuring the presence of at least some moisture,
the faecal mass may moderate the rate of desiccation of larvae. The require-
ments for moisture to enable the migration of infective larvae from the faecal
mass were reviewed (Van Dijk and Morgan, 2011; see Section 4.2.6).
4.1.3 Temperature requirements for the development of eggs to

infective larvae
Provided that moisture conditions are adequate, eggs of H. contortus survive
and develop between about 10 C and <40 C, with maximum hatching
rates (and mortality) at high temperatures, but greatest survival at low tem-
peratures. Under conditions of extreme cold, freshly passed (unembryo-
nated) eggs in faecal pellets are not viable, surviving for only 24 h at 0 C
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(Jasmer et al., 1986; Shorb, 1944a,b; Veglia, 1915), and for few days at 4e
5 C (Shorb, 1944a,b; Smith-Bujis and Borgesteede, 1986). The longer sur-
vival of embryonated eggs at low temperatures (2 months at 1.1 to 2.2 C;
Silverman and Campbell, 1959) confirm the environmental resistance of this
stage, although this is likely to be of marginal, practical significance, except
where diurnal temperature fluctuations permit sporadic egg development to
infective larvae. H. contortus eggs are significantly less tolerant of cold tem-
peratures than are the eggs of other major trichostrongyles of ruminants
(McKenna, 1998).
The role of temperature in determining H. contortus development rates is
clearly seen in the effects on the time required for egg hatching. At the
minimum hatching temperatures (8e10 C) reported for eggs incubated in
water, first-stage larvae were observed between 5 and 18 days (Berberian
and Mizelle, 1957; Crofton and Whitlock, 1965; Jehan and Gupta, 1974;
Veglia, 1915), but none developed at 7.2 C (Silverman and Campbell,
1959). In contrast, hatching was rapid at high temperatures: 14e16 h at
37 C (Berberian and Mizelle, 1957; Jehan and Gupta, 1974; Veglia,
1915). This temperature is close to the upper limit for hatching, because
at 40 C, little or no egg development occurs (Misra and Ruprah,
1973a; Todd et al., 1976b; Veglia, 1915).
A similar response to temperatures applies to the development of infec-
tive larvae of H. contortus, with an increasingly short period required as
temperatures increase. Silverman and Campbell (1959) reported that infec-
tive larvae appeared after 11 days at 11 C, 5 days at 21.7 C, and 3 days at
37 C. No larvae develop at extreme temperatures (w40 C) (Berberian
and Mizelle, 1957; Jehan and Gupta, 1974; Misra and Ruprah, 1973a;
Silverman and Campbell, 1959; Veglia, 1915). The consensus from these
reports indicates that optimal development with minimal mortality occurs
over the physiological range optimal for most ruminant nematodes (20e
30 C), provided that moisture is not limiting.
4.1.4 Temperature requirements for the survival of infective larvae

Although infective larvae of H. contortus can survive extremes of moisture
conditions, from desiccation to full hydration, this is largely mediated by
temperature, with limitations closely following the requirements for egg
development. Larvae stored in water at <0 survived for only a few days
(Jasmer et al., 1987; Rose, 1963; Todd et al., 1976b), but for some months
at temperatures close to freezing point, although in very small numbers
(Boag and Thomas, 1985; Misra, 1978; Rose, 1963; Veglia, 1915). Survival
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in faecal cultures was longer when larvae were desiccated before storage
(Todd et al., 1976b). The survival of larvae at extremes of high temperature
(in water) was considerably shorter: only 16e33 days at 40 C (Jehan and
Gupta, 1974; Sood and Kaur, 1975).
Provided that moisture is abundant, the range of temperature for larval
survival largely corresponds with that for larval development. Periods
recorded for survival in water at 20 C varied from 140 to 256 days in several
studies (Boag and Thomas, 1985; Jehan and Gupta, 1974; Todd et al.,
1976b), and at 30 C from 91 to 118 days (Boag and Thomas, 1985; Sood
and Kaur, 1975). Although direct extrapolation to field conditions is
tenuous, these findings seem to be consistent with the wide occurrence of
H. contortus in tropical, subtropical and summer rainfall climatic zones.
4.1.5 Intraspecific differences in critical requirements

Reports of differences in egg hatching times between isolates from various
geographical regions when compared under standardiszed conditions sug-
gest the existence of environmentally mediated survival differences. Crofton
and Whitlock (1965) reported a minimum egg hatching temperature of 9 C
for an isolate from the UK, compared with a surprisingly high 15 C for H.
contortus from New York, USA, and maximum hatching temperatures vary-
ing from 36 to 41 C. Similarly, Le Jambre and Whitlock (1976) reported a
variation from 38 to 40 C for New York and Ohio isolates, respectively,
and also related morphological characteristics to temperature preferences.
A more specific link to environment was seen in Australia, where minimum
hatching temperatures varied from >10 C for H. contortus isolates from
warm-climate regions (northern Western Australia and Queensland) to
8 C for those from colder southern locations in Tasmania and southern
Western Australia (Besier, 1992). High-temperature responses also appear
consistent with environmental differences. Although comparisons between
studies must be interpreted with caution, considerable variation in egg-
hatching intervals have been reported, from 3 days for a UK isolate
(Silverman and Campbell, 1959) to 15e16 h for isolates from the USA
and India (Berberian and Mizelle, 1957; Jehan and Gupta, 1974). Similar
variation has been reported for the development of eggs to infective larvae
at high temperatures: 132 h for a US isolate at 37 C (Berberian and Mizelle,
1957) compared with 80 h in an Indian study at the same temperature (Jehan
and Gupta, 1974).
Although further evidence is needed to confirm intraspecific variation in
environmental tolerance, current information would be consistent with an
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adaptation strategy that allows H. contortus to extend its geographical range,

particularly to colder environments, and thus explain the ubiquitous distri-
bution of a species of essentially tropical origin. Phenotypic variation within
H. contortus is also reflected in differences in pathogenicity among isolates
(Hunt et al., 2008; Angulo-Cubillan et al., 2010), suggested to relate to
genomic variability (Hunt et al., 2008), and in the capacity for hypobiosis
from distinct climatic regions (Troell et al., 2006). The report of genes pu-
tatively related to desiccation tolerance (Yang et al., 2015) is consistent with
the proposition of a genetic adaptation to environmental differences.
4.1.6 Other environmental factors

In comparison with the critical role of temperature and moisture, evidence
for effects of other ecological factors is limited. A requirement for adequate
oxygenation of faecal cultures under laboratory conditions has been demon-
strated (Shorb, 1944b; Veglia, 1915), but is unlikely to be a significant lim-
itation in the external environment. Different light intensities have been
postulated as a significant factor affecting the viability of larval stages, with
a deleterious effect of ultraviolet (UV) light demonstrated for preinfective
larvae (Conder, 1978; Gupta et al., 1982) and on the infective larval stage
(Krecek et al., 1992; Van Dijk et al., 2009). This is consistent with observa-
tions by Rees (1950), who related the greatest larval recoveries to periods of
low light intensity (although this was also the period of greatest pasture
moisture), and although the effect of UV irradiation would vary diurnally
and depend on the degree of shade within a pasture sward, this may have
an under-recognized effect on the availability of infective larvae to grazing
animals.
4.2 Ecological investigations in the field

In contrast to laboratory-based studies which examine the effects of various
variables under controlled conditions, field plot data integrate the effects of
ambient weather and other environmental variables on the developmental
process. For the usual experimental format, faeces containing undeveloped
nematode eggs are deposited onto small pasture plots sequentially over a
particular period, and then recovered at intervals and assayed to estimate
the numbers of various developmental stages present. The results can indi-
cate the proportion of eggs that yield larvae in relation to the number of
eggs deposited, and the period of survival of infective larvae in relation to
weather conditions and (if measured) the microclimatic conditions at ground
level. Inferences from these studies must be qualified according to the rigour
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of the study design, relating mainly to the frequency and duration of depo-
sitions, the efficacy of recovery techniques, and the use of replicates to mini-
mize statistical variation among plots. Nevertheless, a large number of studies
over a wide range of environments provides a basis for explanations
regarding the observed epidemiology of infections and allows predictions
from computer simulation modelling.
Differences in ecological results related to the nature of the measure-
ments taken add some complexity to the interpretation of the data (Levine
et al., 1974). Studies in the laboratory suggest values for environment
parameters directly associated with egg and larval development; in field
plot studies, the majority of recordings are from standard meteorological
monitoring stations situated above ground level. During mid-2010s, data
loggers have been utilized to measure a wider range of variables, with
simultaneous recordings at different points, including within the pasture
microclimate and soil. An additional challenge relates to the measurement
of moisture-related variables; although, in practice, the amount and timing
of rainfall are key parameters, they do not always correlate directly with the
moisture available to the free-living stages at ground level. Factors such as
cloud cover, wind effects and evaporation rate influence the availability of
moisture, as does the nature of soil and composition of herbage. In part,
differences in the results among studies are likely to reflect the effects of fac-
tors not measured in a particular study, and comparisons require careful
consideration.
It is of interest that most studies conducted in tropical regions involved
goats, whereas those in subtropical and temperate regions were largely
with sheep.
4.2.1 Tropical and subtropical climates

Where temperatures are either continually or seasonally high, plot studies
confirm rainfall as the principal limitation on H. contortus development,
and in the true tropics, year-round rainfall permits continual H. contortus
development. For instance, in the wet zone of Fiji, larvae developed in every
month, although they survived for only 5e9 weeks under environmental
temperatures of 25e30 C (Banks et al., 1990). Similarly, in the Caribbean,
a study in Guadeloupe (Berbigier et al., 1990) found high desiccation rates to
limit larval viability under hot conditions (mean temperatures of 29 C),
but with a major difference in larval recoveries and survival periods in rela-
tion to the microclimate (short or tall grass plots) and to the time of the day
when the herbage was collected.
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In more seasonal tropical locations, with distinct wet and dry seasons,
larval development is more highly seasonal. For example, in a study in the
Kenyan Highlands (Dinnik and Dinnik, 1958), development occurred
only during warm and wet periods and after rainfall of 8 mm over a 10-
day period. Larval survival was short, despite rainfall (14e65 days at maxima
of 25e29 C), but increased as temperatures decreased, with the annual
onset of dry conditions (Dinnik and Dinnik, 1961). At Hissar, northern In-
dia, infective larvae were found to survive on plots for 2 months during
rainy seasons when daily maximum temperatures were 25e44 C (Misra
and Ruprah, 1972), but even at extreme temperatures (45 C), infective
larvae developed, provided that rainfall occurred at the time of deposition
(Misra and Ruprah, 1973b). A small proportion of eggs yielded larvae during
the dry and cool season (mean minima of 3e8 C).
At different sites in Nigeria, a marked difference was similarly related
to season, with rapid larval development during the rainy season at tem-
peratures of 25e30 C and survival for 2 months in studies in Ibadan
(Okon and Enyenihi, 1977) and Vom (Onyali et al., 1990). During the
dry season, no larvae developed at either of these sites, and larvae from pre-
vious depositions died rapidly as mean temperatures rose to >25 C. This
seasonal pattern was also evident in the recovery of H. contortus larvae
from pasture plots studies in a subtropical region of Pakistan (Islamabad)
(Chaudry et al., 2008). Temperatures were conducive to substantial
development for most of the year (maxima: 22.9e37.0 C, minima:
15.0e24.0 C), but recoveries declined during short periods of cool or
dry conditions. Almost all infective larvae had died within 3 months of
faecal deposition, and in half of this time if deposited prior to or during
the dry season. The effects of dry conditions also seen in studies near Addis
Ababa, Ethiopia, where despite lower mean temperatures associated with
altitude, development was confined to the warm and wet summer season,
with little development during the dry seasons over several months
(Tembely, 1998).
The close relationship between rainfall and the migration of infective
larvae from faecal pellets was shown in plot experiments in San Paulo State,
Brazil (Santos et al., 2012), with the recovery of infective larvae at all depo-
sition times, but the greatest recoveries in the hot and wet summer months
(maxima: >40 C). Migration rates also varied with rainfall; infective larvae
were found on herbage within 24 h of experimental deposition of H. contor-
tus eggs on days when rainfall occurred, but during dry periods, larvae
remained in the faecal masses. The very small proportion of H. contortus
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eggs recovered as infective larvae (typically 1e2%) raises a query as to

whether mortality is accelerated under repeated cycles of desiccation and
rehydration, in comparison to the potential for extended survival in relation
to desiccation under colder conditions (anhydrobiosis) (Lettini and
Sukhdeo, 2006).
4.2.2 Warm, temperate and Mediterranean climates

Outside of the subtropical zones, H. contortus development on pasture is
restricted when dry and hot seasons coincide, and sometimes by cooler
winter conditions. This pattern is clearly evident in a classic account of
the life history of H. contortus at the Onderstepoort Laboratory in Pretoria,
South Africa, in a summer rainfall environment. Veglia (1915) noted a
marked difference in development rates in relation to the coincidence of
temperature and moisture on field plots, with little or no development un-
der dry conditions, regardless of temperature, and significant development
only under warm and wet conditions. In the same location, M€ onnig
(1930) showed that larvae survived for 9 months through winter, but for
only a few weeks in summer. Similarly, in the uniform rainfall climate of
Sydney, Australia, Donald (1968) found little or no H. contortus egg devel-
opment on field plots during dry winter periods, although infective larvae
that had developed prior to winter could also survive for some months.
A strongly seasonal pattern was also evident in later studies involving
microclimatic effects on the development of infective larvae of H. contortus
on irrigated kikuyu grass pastures at Pretoria, with strong correlations be-
tween larval recovery and the temperature and relative humidity at ground
level (and also the wind speed and light intensity) (Krecek et al., 1992).
Infective larvae of H. contortus and H. placei were found to survive under a
grass sward for up to 10 and 16 months, respectively (Krecek et al., 1991).
This strongly seasonal pattern is also evident in Mediterranean (winter
rainfall) climatic regions, where the major restrictions on H. contortus are ex-
tremes of heat and dryness during summer, and cool winter conditions are
only a transient limitation. In plot studies in south-west Western Australia,
no development occurred during summer on dry plots with mean
maximum temperatures of 27e30 C (Besier and Dunsmore, 1993a), and
larvae that developed during spring died after a few weeks as temperatures
rose (Besier and Dunsmore, 1993b). The development of eggs ceased for
a few weeks during winter (mean minima of 6e8 C), but infective larvae
survived for some months, including through the winter period. A key
finding was the association of H. contortus larval development with the
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presence of actively growing pasture, presumably as an index of the availabil-

ity of moisture at the microclimatic level; almost all depositions on to a dense
green pasture sward yielded infective larvae, compared with only 50% of
those on dry pasture plots, and not in large numbers (Besier and Dunsmore,
1993a). In Mexico, under similar temperature conditions, but in a summer
rainfall climate, Fermindez-Ruvalcaba et al. (1994) found greatest larval
development in autumn, when both rainfall and temperature were begin-
ning to decline, indicating the lethal effect of high temperatures, even
when moisture was available, as occurs in true tropical zones.
A number of investigations in northern New South Wales, Australia,
confirm the critical importance of moisture at the time H. contortus eggs
are deposited onto pasture during periods of high temperatures (O’Connor
et al., 2007a,b; 2008). During the summer period, with a range in daily air
temperatures from w10 to 36 C, simulated rainfall on to pasture plots led to
the development of infective larvae when this occurred over the first few
days following deposition, but not with a single rainfall event, regardless
of amount (O’Connor et al., 2007a). In controlled incubator studies at
similar temperatures, but under conditions of low evaporation (2 mm/
day), larval development increased with rainfall amount, and correlated
with the cumulative precipitation/evaporation (P/E) ratio (O’Connor
et al., 2007b). A further study (O’Connor et al., 2008) confirmed the lower
percentage of infective larvae developing under high evaporation rates,
regardless of the amount or distribution of simulated rainfall. From these
results, it is suggested that moisture indices other than rainfall might correlate
most closely with developmental success of H. contortus, with a P/E ratio of
1.0 required for the first 4 days following egg deposition on to pasture.
Similarly, in Texas, USA, Amaradasa et al. (2010) found a close correlation
between rainfall and larval recoveries from herbage, particularly when it
rained on the day of sampling, or on days immediately before.
4.2.3 Cool, temperate climates

A different pattern is seen in higher latitudes, where H. contortus is closer to
the edge of its geographical range, and the temperature becomes relatively
more important. Development is largely confined to the warmer summer
months, provided that the rainfall is adequate, although infective larvae of
H. contortus that develop during the colder months may remain viable for
considerable periods. In the temperate climate of New Zealand (North
Island), the results of plot studies appear to be consistent with the relatively
minor significance here of haemonchosis, with poor or zero recoveries of
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infective larvae after faecal egg depositions for periods of 5e6 months, when
the mean air temperature is close to or 10 C (Waghorn et al., 2011). The
mean daily temperature was recognized as the most significant variable for
the development of H. contortus, although rainfall during the first 14 days af-
ter faecal deposition was also required (Reynecke et al., 2011).
In the more extreme climate of Beltsville, Maryland, USA, plot studies
(Dinaburg, 1944a) found eggs of H. contortus to produce infective larvae
only when the mean maximum temperature was >18.3 C (65 F), later
referred to as the ‘Dinaburg Line’ (Kates, 1950) to indicate the lower limit
of temperature for development. Larvae survived for 3 months during spring
(maximum temperatures: 17e23 C), but for only 2 weeks in summer
(maximum temperature: >30 C; Dinaburg, 1944b). Very few infective
larvae survived over winter in this environment (mean maximum tempera-
tures occasionally <0 C). In the cold winter climate of Illinois, USA (mean
monthly temperatures: <5 C), eggs developed to infective larvae only for
6 months of the year, but development proceeded when mean temperatures
ranged between 10 C and 25 C, provided that the monthly rainfall was
>50 mm (Levine, 1980). Similarly, development of H. contortus eggs failed
in winter in southern England (Weybridge), with greatest larval recoveries in
summer when mean temperatures varied from 8 C to 13 C (minima) to
14e25 C (maxima) (Rose, 1963). However, some infective larvae that
developed in summer were recorded as surviving for 40 weeks (Rose,
1963; Gibson and Everett, 1976). The critical importance of moisture was
later confirmed; H. contortus larvae developed only on plots that were either
consistently watered during summer, or where rainfall occurred for some
time after deposition (Rose, 1964). An effect of microclimate was apparent
in the greater larval development on tall (20 cm) herbage compared with on
shorter (5 cm) pasture.
4.2.4 Arid regions

Plot studies in regions with prolonged or continual hot and dry conditions
confirm the presence of H. contortus only during brief periods of seasonal
rainfall, or on irrigated pastures. A study in Utah, USA (Bullick and
Anderson, 1978) showed considerably greater recoveries of infective larvae
of H. contortus from irrigated than dry plots, with few larvae on the latter able
to migrate from faecal pellets on to dry herbage. In central Iraq, a pattern
similar to that of Western Australia (Besier and Dunsmore, 1993a) was
shown, with no larvae produced during summer, with maximum tempera-
tures of >40 C, but some development after autumn rains, although the
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survival periods of infective larvae decreased as temperatures increased (Altaif

and Yacoob, 1987).
4.2.5 Effect of microclimatic factors on larval development

Although difficult to measure objectively, the microenvironment within the
herbage sward has a direct effect on strongylid nematode eggs and larvae;
data on this aspect, if quantifiable, would provide useful predictions of
developmental success in a particular circumstance. Thus, laboratory
investigations are likely to better define relationships between H. contortus
development and environmental factors than standard weather station mea-
surements. Factors, such as pasture height and density, will affect the local
microclimate. In addition to the presence of shade from trees and shrubs,
such environment-modifying factors are likely to explain differences in
the development of infective larval on a particular pasture or field.
Differences in temperature between the biome occupied by the free-
living stages and the air can be marked. Two studies (Bailey et al., 2009;
O’Connor et al., 2007a) reported consistently lower maximum air temper-
atures of 15 C in a weather station compared with those at ground level
during spring and summer, although, interestingly, there was virtually no
difference in minimum temperature values between the points of measure-
ment. Temperatures on irrigated pastures are also likely to be lower. For
instance, in Utah, USA, Bullick and Anderson (1978) recorded air temper-
atures under vegetation of 26 C on irrigated plots compared with 35 C on
dry pasture. Similarly, daily maximum temperatures under long high
(15 cm) pastures can be up to 5e10 C lower than under short (3 cm) pas-
tures (Sakwa et al., 2003). Within faecal pellets, temperatures during hot sea-
sons are typically considerably higher than in the air (up to 60 C when
weather station air temperatures are 35 C; RB Besier, unpublished data).
The most consistent relationships between microclimate and nematode
development are likely to involve the faecal pellet and the adjacent soil.
An early report (Veglia, 1915) in South Africa indicated that moisture within
4 days after faecal deposition was important for successful development to
infective larvae, a finding that was confirmed in a detailed investigation in
northern New South Wales (O’Connor et al., 2008). FMC during the
4 days after faecal deposition on to pasture was closely correlated with larval
development, which was negligible when FMC declined to <10%. From an
earlier study in Nouzilly, France, Rossanigo and Gruner (1995) suggested a
minimum FMC requirement of 39% for the development of infective larvae
of H. contortus, although a subsequent Australian study (Khadijah et al.,
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2013b) found development at a considerably lower FMC, possibly due to

diurnal temperature fluctuations. A threshold effect of FMC, mediated by
(simulated) rainfall and relative humidity, was also demonstrated for larval
migration from faecal matter in laboratory studies in the UK (Wang et al.,
2014), where migration occurred at an FMC of 70%, but was negligible
at 10%. These authors concluded that rates of faecal desiccation and rehydra-
tion on pasture could explain temporal patterns of larval availability, and that
sheep faeces may act as a larval reservoir in dry conditions, with peaks of
infection following rainfall.
Investigations have also highlighted the role of soil moisture, presumably
through transfer to faecal pellets. H. contortus larval development has been
shown to be as great on plots contaminated on the day prior to simulated
rainfall as it was on plots watered on the 2 days immediately beforehand
(Khadijah et al., 2013a), and correlated closely with FMC. The interaction
between rainfall and soil moisture was also evident, as increasing the daily
simulated rainfall on dry soil from 12 to 24 mm led to a significant increase
in both soil moisture and FMC, but had little effect when the soil was
already moist (Khadijah et al., 2103b). This explains earlier field observations
from the East Cape region of South Africa, which indicated that the avail-
ability of H. contortus infective larvae varied over a property according to the
wetness of the ground (McCulloch et al., 1984); it is perhaps surprising that
this correlation had not been empirically established earlier.
4.2.6 Lateral and vertical migration of infective larvae

The migration of nematode infective larvae both laterally from faecal masses
and vertically onto the herbage is the essential final step in the ecology of the
free-living stages (reviewed by Van Dijk and Morgan, 2011). Larval move-
ment is subject to specific behavioural characteristics, and with directional
movement at random provided energy reserves are adequate, and moisture
and temperature determinants permit (Crofton, 1954).
Provided microclimatic factors are in the optimal range for larval survival,
the availability of moisture largely determines the rate and distance of migra-
tion. Moisture requirements were indicated in investigations in Bristol, UK,
using faecal masses isolated on sieves (Wang et al., 2014). At temperatures of
25e27 C, a single simulated heavy rainfall event (20 mm) within the first
few days of faecal deposition was not sufficient to permit migration, but
significant larval emergence occurred when light ‘rain’ (2 mm) over several
days coincided with high relative humidity (98%), although this was reduced
at lower levels of humidity (30e50%). It appears that, within moisture
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constraints, infective larvae migrate from the faeces shortly after their devel-
opment, with maximum recovery rates reported to be within w24 h
(Crofton, 1948; Silangwa and Todd, 1964; Van Dijk and Morgan, 2011).
From various accounts and their own laboratory work, Van Dijk and
Morgan (2011) estimated that, at a constant air temperature of 20 C and
adequate moisture conditions, the numbers of larvae would remain negli-
gible after 3e4 weeks, although diurnal temperature fluctuations would
alter this time period in different seasons. A similar rapid depletion of the
faecal reservoir (2e4 weeks) during warm months was reported earlier
from pasture plot investigations in southern England (Rose, 1963), but small
numbers continued to migrate for >4 months from depositions under colder
winter conditions. A desiccated faecal mass can function as a reservoir for
infective larvae of trichostrongyles (Amaradasa et al., 2010; Stromberg,
1997), with a mass release of larvae after rainfall. It is also apparent that infec-
tive trichostrongyle larvae can remain within the soil or in the vegetation
mat at the soil surface, also providing a potential larval reservoir (Amaradasa
et al., 2010; Krecek et al., 1991; Rose and Small, 1985; Stromberg, 1997;
Van Dijk and Morgan, 2011). The rapid release of significant numbers of
infective larvae onto pasture from a desiccated faecal mass following periods
of rainfall after dry conditions would explain the sudden outbreaks of hae-
monchosis a few weeks later. However, where dung masses disintegrate after
heavy rainfall, there is little opportunity for a reservoir function.
In a study of the lateral migration of H. contortus on grass plots (unspec-
ified species) in Illinois, USA, Skinner and Todd (1980) found >90% of
infective larvae within 10 cm of the faecal mass and few beyond 20 cm,
and that migration essentially ceased during ‘hot, dry weather’. The require-
ment for moisture is at least as pertinent for the vertical migration of infective
larvae, as the microclimate becomes less favourable (drier, and a more vari-
able temperature) with the increasing height of pasture herbage. Most
studies of vertical migration of trichostrongyle larvae (not necessarily H. con-
tortus) found w90% of larvae within 5 cm of the ground in grass swards, and
very few above 20 cm (Crofton, 1948; Rees, 1950; Silangwa and Todd,
1964), although this varied with factors affecting the microclimate, such as
the herbage height (Amaradasa et al., 2010; Berbigier et al., 1990; Rose,
1964); the latter authors also considered the physical capacity of the foliage
to retain moisture to affect migration. Although Krecek et al. (1991) found
no difference in larval recovery in relation to the height (above or below 5e
7 cm) of kikuyu grass pasture, their study was conducted on irrigated plots,
where moisture was not limiting. There has long been a contention over
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whether free water (rainfall, mist or dew) is essential for larval migration, but
from their own experimentation and a review of other findings, Van Dijk
and Morgan (2011) concluded that a high relative humidity is sufficient.
The diurnal pattern of larval recovery observed by Rees (1950) and Aumont
and Gruner (1989) was greatest in the early morning, presumably reflecting
considerable moisture availability, as dews, or high relative humidity at this
time, before the temperature increase during the day.
5. EPIDEMIOLOGY
Sequential observations of worm burdens in grazing animals indicate
relationships between nematode development and environmental factors,
and provide an epidemiological context. These investigations include: (1)
structured studies using ‘tracer’ animals grazing small pasture areas contam-
inated with worm eggs at specific times; (2) worm counts from flocks or
herds grazing continually contaminated pastures and (3) abattoir surveys.
Total worm counts from grazing animals also indicate the presence of hypo-
biotic larvae and their relative importance as a survival mechanism during
adverse environmental conditions. Studies based only on FWECs are not
included here, as the results are not necessarily indicative of the actual
worm burden. In the majority of studies of grazing animals or from abattoir
surveys a number of nematode species were recorded, and while interspecies
competitive effects may affect the worm numbers recovered, the comments
here relate only to H. contortus. Not all studies aimed to define the epidemi-
ology of H. contortus over the course of an entire year, and the frequency and
rigour of observations varies greatly. However, overall, they provide a good
understanding of seasonal effects on the annual pattern of worm burdens for
a range of environments, as the basis for locally applicable control pro-
grammes (Barger, 1999). A summary of the major ecological influences
and epidemiological features of H. contortus infections for each climatic
zone is provided in Table 2.
5.1 Tropical and subtropical regions

When temperatures are continually adequate for H. contortus development,
studies of worm counts in sheep have confirmed their close relationship with
rainfall patterns. In the wet tropics where rainfall occurs throughout the
year, studies in Malaysia using ‘tracer’ goats found no seasonal cessation of
H. contortus development, or a relationship with rainfall (Ikeme et al.,
Table 2 Ecological features and epidemiology of Haemonchus contortus infections in small ruminants in different climatic zones
Ecological features (References:

Climatic zonea Section 4.2) Epidemiology (References: Section 5)
Tropical, subtropical zones (tropical Temperatures are sufficiently high to Haemonchosis is a continual threat in the
Africa and the Americas, southern and permit the development of infective wet tropics, as larval populations
South-East Asia, tropical Pacific islands, larvae year-round, but these typically develop rapidly, and animals can remain
Central America, southern states of the survive on the herbage for only a continually infected. Where annual dry
USA, the Caribbean, the north of relatively short period (weeks). The seasons occur, larval availability is
Australia) availability of moisture is the key seasonal and confined to the wetter
determinant of larval occurrence, with months, with the highest burdens
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little development and short survival associated with higher rainfall. Survival
periods during dry seasons. In high- as hypobiotic fourth-stage larvae occurs
altitude regions in these zones, larval routinely in seasonally dry
development and the period of survival environments, but is of minor
increases during cooler winter periods, importance or has not been reported
provided sufficient moisture is present. where infective larvae are present for
prolonged periods of the year.
Warm temperate and summer rainfall The coincidence of warm and wet Haemonchosis is a major health threat
zones (from the tropics to w35 N and conditions during summer favours the during the warmer months, although
S, including regions in southern Africa, development of infective larvae in the risk is either constant or sporadic,
higher-rainfall eastern Australia, parts of summer and adjacent months, although dependant on rainfall. Where winter
southern USA, mid-regions of South development may cease during temperatures are mild, the availability
America, southern and eastern Asia) prolonged dry periods. Development of infective larvae to livestock is less
during other seasons is dependent on sharply seasonal than in subtropical
both rainfall and temperature, and is zones. In regions with a relatively cold
limited or may cease under cold winter winter, the pattern of infection is more
conditions, such as occurs in high- seasonal. The occurrence of hypobiosis
altitude regions. appears to be variable and is mainly
associated with the avoidance of cold
29
winter periods.
(Continued)
30
Table 2 Ecological features and epidemiology of Haemonchus contortus infections in small ruminants in different climatic zonesdcont'd
Ecological features (References:
Climatic zonea Section 4.2) Epidemiology (References: Section 5)
Mediterranean climatic zones (the The hot, dry summer conditions prevent Annual infection patterns in livestock are
Mediterranean region, south-west the development or survival of infective typically bi-phasic, with the largest H.
Cape of South Africa, south-west of larvae during, and in much of this zone, contortus burdens developing from late
Western Australia, some regions in winter conditions are too cold for eggs autumn to early winter, and then from
south-east Australia) to hatch. Larval populations are late spring to early summer. The risk of
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therefore largest in autumn and spring, haemonchosis varies considerably
although where winters are relatively between years and between locations
mild there is some survival of infective within this zone, depending mostly on
larvae over winter. the rainfall. Hypobiosis is reported as
either absent or variably important, and
appears to be related to the length and
severity of summer conditions.
Cool and cold temperate zones (above Low temperatures are usually a greater Haemonchosis is typically an occasional or
latitudes 40e45 N and S, including restriction on the development of rare occurrence, and restricted to the
northern Europe, Britain, Scandinavia, infective larvae than the availability of warmer months, due to the short
northern USA and Canada, south-east moisture. Development usually ceases periods of larval development and
Australia, New Zealand) completely during winter in this zone, hence availability for ingestion.
and in higher latitudes there is little or Hypobiosis is usually the major factor in
no survival of larvae through winter. overwinter survival, with the arrested
Larvae that develop when temperatures development of the majority of
R.B. Besier et al.

are adequate typically survive for some infective larvae ingested in autumn in
months until the onset of very cold frigid zones. However, under
conditions, although development may favourable weather conditions, rapid
be sporadic during dry periods in development during short periods of
summer. high summer temperatures can lead to
haemonchosis.
Arid zones (desert and very low rainfall Lack of moisture is a critical limitation, Haemonchus contortus is typically absent or
regions of southern and sub-Saharan restricting larval development to short present in livestock in very low
Africa, the Middle East, inland periods of sufficient rainfall, often numbers, and haemonchosis is rare.
Australia) varying considerably between years. However, unusually heavy and
When infective larvae develop, these prolonged rainfall may lead to short
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usually survive on pasture for short periods of larval availability that
periods only. Larvae can develop on occasionally result in significant
irrigated pastures, but in many regions burdens of H. contortus. Hypobiosis
within this zone, constantly high occurs routinely in some locations but is
temperatures limit their survival. usually of limited consequence given
the hostile external environment.
Haemonchosis is a potentially greater
risk on irrigated pastures, but high
temperatures often limit the persistence
of large larval populations.
a
Regions listed are indicative of type environments based on published reports, and are not inclusive of all locations in a particular zone where H. contortus may exist.
31
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1987; Dorney et al., 1995; Cheah and Rajamanickam, 1997; Chandrawa-

thani, 2004).
In tropical and subtropical zones with both wet and dry seasons, and
nonlimiting temperatures (mean monthly maxima typically >30 C), the
annual pattern and, to an extent, the amount of rainfall is closely related
to H. contortus abundance. Studies in a range of environments in tropical
Africa have indicated the sharply seasonal pattern of heavy burdens during
rainy seasons, in some cases with two peaks each year, and abrupt declines
after the sudden onset of the dry season. These investigations include
some from Cameroon (Ndamukong and Ngone, 1996), Ethiopia (Sissay
et al., 2007), Ghana (Agyei, 1997; Blackie, 2014), Kenya (Nginyi et al.,
2001), Nigeria (Anene et al., 1994; Bolajoko and Morgan, 2012; Chiejina
et al., 1988; Fakae, 1990; Nwosu et al., 2007; Shillhorn van Veen and
Ogunsusi, 1978), Senegal (Vercruysse, 1983), Tanzania (McCulloch and
Kasimbala, 1968) and the Gambia (Fritsche et al., 1993). The numbers of
adult H. contortus recovered at slaughter were considerably higher where
annual rainfall was high (>1000 mm; Ogunsusi, 1979; Fakae, 1990)
compared with low rainfall regions (300 mm; Fabiyi, 1973; Vercruysse,
1983). In Pernambuco state, Brazil, Charles (1989) found grazing goats to
be continually infected with H. contortus throughout a dry season of several
months, but new infections from pastures were largely confined to the rainy
season. Where altitude moderates conditions in this zone, however, the
seasonal pattern of H. contortus infection also appears to reflect lower winter
temperatures (mean monthly minima typically <10 C), with higher worm
recoveries than in summer, for example, in Kenya (Allonby and Urqhart,
1975) and Zimbabwe (Grant, 1981; Pandey et al., 1994).
Most published reports (Eysker and Ogunsusi, 1980; Fakae, 1990;
Fritsche et al., 1993; Gatongi et al., 1998; Sissay et al., 2007; Vercruysse,
1985) indicate that H. contortus survives throughout the dry season as
hypobiotic fourth-stage larvae, although hypobiosis appears to be absent
or less important if the dry season is short (Agyei et al., 1991; Chiejina
et al., 1988; Okon and Enyenihi, 1977; Pandey, 1990). As would be
expected, there is the potential for a continual H. contortus transmission
risk under constantly high-temperature conditions in monsoonal climates,
but with seasonal fluctuations in burdens according to rainfall. In Haryana,
northern India (mean maxima of 20e40 C), a slaughter study (Gupta et al.,
1987) found that H. contortus burdens related to local rainfall at different
locations, although the practice of irrigation maintained H. contortus
throughout seasonally dry periods, without evidence of hypobiosis.
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5.2 Warm, temperate climates

Grazing studies confirm the potential for rapid population increases in
warmer temperate zones during periods when moisture is not limiting.
Under these conditions, haemonchosis is a major seasonal risk. In a study
conducted in Louisiana, USA, where rainfall occurs throughout the year
and temperatures are high for most of the year, H. contortus was recovered
from tracer sheep in all months of the year (Miller et al., 1998). A decrease
in recovery during winter was associated with cooler conditions (mean
minima of <10 C for 4 months); the highly variable pattern of recovery
of hypobiotic larvae suggested that under these climatic conditions arrested
development in the host animal was not necessary to ensure the survival of
H. contortus. However, a marked seasonal effect of cold winter conditions
was reported from other locations where the severity of haemonchosis is a
significant limitation on sheep production. In the summer rainfall region of
northern New South Wales, Australia, H. contortus development occurred
when mean temperature maxima exceeded 18 C (Southcott et al., 1976),
and heavy burdens were recovered from grazing lambs during summer
when rainfall coincided with warm temperatures (mean maxima of
25 C). However, few or no H. contortus larvae were acquired from plots
contaminated during winter, and most of the worms recovered from the
sheep during this period were as hypobiotic larvae. The poor development
in winter at this location was confirmed in later tracer sheep studies, with
negligible H. contortus worm recoveries in months when the mean minima
were consistently <5 C (Bailey et al., 2009). In a similar environment in
inland southern Queensland, Swan (1970) considered H. contortus to
require monthly minimum temperatures of >10 C, but hot summer
conditions allowed a rapid population ‘recovery’ from poor winter
development.
An even more seasonal pattern was evident in the Mediterranean climate
of southern Western Australia, with negligible larval infection from winter
egg deposition and a total cessation of intake over the hot dry summer
period (De Chaneet and Mayberry, 1978). However, the development of
lethal H. contortus burdens in tracer lambs in the warm spring months, and
a limited peak in autumn, attest to the ability of H. contortus to capitalize
on short periods when conditions are favourable for rapid development.
In this region, there is presently no evidence of hypobiosis in H. contortus
(RB Besier, unpublished findings), consistent with its absence in sheep
and goats in an abattoir study in the Nile Delta, also a Mediterranean climate
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(E1-Azazy, 1990). However, in the Ebro Valley in Spain, under broadly

similar climatic conditions, Uriarte and Valderrabano (1989) recovered a
high proportion of hypobiotic larvae of H. contortus in both spring and
autumn from tracer lambs.
In South Africa, H. contortus has been shown to survive virtually
throughout the year in sheep in temperate and higher rainfall regions,
including the South-West Cape (Muller, 1968) and the Eastern Province
(Rossitter, 1964), with highest counts in summer. In the winter rainfall
region of Stellenbosch, development was poor during the winter months,
but H. contortus remained present throughout the year in sheep grazing
perennially green pastures (Reinecke et al., 1987). In drier climates, cold
winters further limit the period for effective H. contortus development,
with haemonchosis essentially confined to summer in the South-East
Cape (Barrow, 1964), particularly on kikuyu grass and irrigated pastures.
Expansions of H. contortus populations were recorded following periods
of summer rainfall in the dry Eastern Cape region (McCulloch and
Kasimbala, 1968).
5.3 Cool temperate climates

In cooler zones, where summer temperatures are warm rather than hot,
variably cold winter conditions are a critical limitation on H. contortus
development. Hypobiosis is usually a routine survival mechanism,
although apart from regions where extremely cold winter conditions
prevail, its importance in comparison to survival as the free-living stages
on pasture is not clear. In the North Island of New Zealand, development
appears to be restricted by cold winter periods (mean air temperatures of
<10 C), despite abundant moisture. In studies by Brunsdon (1970) and
Vlassoff (1973), H. contortus was recovered throughout summer, but its
availability was limited by sporadic dry conditions, and recoveries of adult
worms in lambs peaked in autumn. Hypobiosis has been demonstrated to
occur variably, but is not the sole mechanism for survival during winter
(Brunsdon, 1973; McKenna, 1974).
In colder climates, however, where mean minimum winter tempera-
tures are <0 C for some months, development is usually confined to
summer and autumn. Hypobiosis is an essential requirement for overwin-
tering in these regions, with 100% of ingested infective larvae entering an
arrested state in extreme climates (Waller et al., 2004). In the Northern
Hemisphere, numerous studies have confirmed the negligible develop-
ment of eggs and limited survival of infective larvae of H. contortus over
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winter, in Canada (Alayew and Gibbs, 1973; Falzon et al., 2014; Mederos
et al., 2010), England (Connan, 1971; Gibson and Everett, 1976; Thomas
and Waller, 1979), France (Kerboeuf, 1985), Norway (Domke et al., 2013;
Helle, 1971), Sweden (Troell et al., 2005; Waller and Chandrawathani,
2005), and northern zones of the USA (Grosz et al., 2013; cf. Levine,
1980). Haemonchosis outbreaks, with considerable animal mortalities,
can occur occasionally following the development of hypobiotic larvae
to adult worms in spring (Sargison et al., 2007), but in the more extreme
climatic regions, the almost total dependence of H. contortus on hypobiosis
for survival over the winter period has raised speculation regarding the
feasibility of eradication of H. contortus (Domke et al., 2013; Waller
et al., 2006).
5.4 Arid climates

Despite the adverse conditions for larval development, grazing studies
confirm that despite temperatures as high as 40e45 C, H. contortus is
commonly present in very low rainfall zones in tropical and warm
temperate climates, although rarely in large numbers. In trials at three
different localities in the Karoo of South Africa, with maximum tempera-
tures of up to 40 C, the numbers of H. contortus recovered by Viljoen
(1969) from tracer lambs decreased as rainfall declined, with negligible bur-
dens in the severely arid Klerefontein region. Similarly, recoveries of H.
contortus were generally minimal in the Kalahari (Biggs and Anthonissen,
1982); although relatively heavy burdens were found in sheep following
only 25 mm of rainfall within a month, it was considered that the distribu-
tion of rainfall was more important than the total. Haemonchus contortus was
not found in sheep on dry pastures in Libya (Pullan and Megadmi, 1983) or
Iraq (Altaif and Issa, 1983), but small numbers were recovered on irrigated
pastures, despite maximum temperatures of 40 C (Altaif and Yakoob,
1987). Very small H. contortus burdens were found in extensively grazed
sheep and goats in the extreme climate of Saudi Arabia (summer maxima
of 45 C), and a degree of hypobiosis was evident in the autumn and sum-
mer months (El Azazy, 1995).
Presumably H. contortus populations are maintained through brief periods
of larval development when the rainfall is adequate. Local eradication of
H. contortus may be feasible in environments marginal for H. contortus
(Le Jambre, 2006), provided that treated flocks could be kept separate and
alternate hosts are not present, although in many cases the effort may not
be warranted.
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6. PREDICTION OF THE OCCURRENCE OF

H. CONTORTUS
6.1 Predictive models
Attempts to define regions where H. contortus is likely to present a
threat to the livestock industries led Gordon (1948) to develop the concept
of ‘bioclimatographs’, which indicate the monthly suitability for the devel-
opment of infective larvae of H. contortus in a particular location, on the basis
of long-term climatic averages in relation to limiting temperature and rainfall
requirements. The initial models used the mean monthly maximum temper-
ature of 18 C, as proposed by Dinaburg (1944a,b), and a monthly rainfall of
51 mm, and were later modified by Swan (1970) to include a lower mean
monthly minimum of 10 C in environments with major diurnal tempera-
ture fluctuations. These criteria have proved generally suitable for indicating
the haemonchosis risk in different localities in Australia (Donald et al., 1978;
Southcott et al., 1976), although outbreaks not consistent with predictions
have occurred in some regions (De Chaneet and Mayberry, 1978). Levine
(1963) also considered bioclimatographs to provide a general indication of
the seasonal and geographical distribution of H. contortus, but indicated
that they are not sufficiently sensitive for predictions regarding specific loca-
tions, years or pasture conditions.
Since 1980s computer simulation models to indicate nematode popula-
tion changes for various locations have been developed based, initially based
mostly on the response of the free-living stages to weather inputs (eg, Barger
et al., 1972), and later including more complex factors such as host immuno-
logical effects (Barnes et al., 1995; Smith and Grenfell, 1994; Thomas, 1982;
Leathwick et al., 1992). Simulation models have evolved further to explore
strategies to avoid the development of anthelmintic resistance, including in
H. contortus (Dobson et al., 2011; Learmount et al., 2006; Van Wyk and
Reynecke, 2011). These models mostly utilize standard weather station ob-
servations, because their prime purpose is not to indicate the relative suitability
for egg and larval development within specific localities. However, the poten-
tial for using microclimatic factors to increase between-site sensitivity has been
recognized (Leathwick, 2013), including a combination of ecological, cli-
matic and topographical inputs (Van Wyk and Reynecke, 2011). Greater
sensitivity would be of significant value for predictions of the epidemiology
of H. contortus in regions where few studies have been conducted to date,
and of changes over time to its importance in different climatic zones.
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6.2 Potential effects of climate change

Given the key role of climatic factors in determining the present distribution
of helminths with a free-living phase, permanent changes to climate will
affect the global occurrence and significance of parasitic helminths. For H.
contortus, the length of periods favourable for development and transmission
are likely to increase with trends towards either warmer conditions in cool
temperate zones, or for greater or less seasonal rainfall in presently drier re-
gions. An increased risk of haemonchosis is particularly great due to the high
biotic potential, which allows H. contortus to take advantage of even rela-
tively small changes to external conditions (Van Dijk et al., 2010).
Indications of climate-mediated changes are becoming apparent. Unusu-
ally high H. contortus burdens in lambs in 2003 were reported from the
Netherlands in association with relatively warm and dry conditions, and
an apparent change to the usual pattern of hypobiosis (Eysker et al.,
2005). An increase in outbreaks of haemonchosis has been reported from
Scotland, where H. contortus exists but has rarely led to clinical disease
(Kenyon et al., 2009; Sargison et al., 2007). In the UK, a survey of case re-
ports of haemonchosis indicates an increasing prevalence of H. contortus
infection over the past 30 years, and the fact that the increase has been
chiefly in northern regions, and during autumn, suggests that the parasite
has especially benefited in regions where thermal energy was most limiting
(Van Dijk et al., 2008). It was postulated that a greater proportion than usual
of the ingested larvae that enter hypobiosis were likely to develop to adult
worms, and, significantly, that there is no evidence that summer conditions
were becoming more hostile for transmission.
Mitigating the potential effects of climate changes will firstly require an
estimation of likely changes to the geographical range where significant
burdens of pathogenic helminths may develop, and the extent and season-
ality of an increased risk of disease. Where a significantly altered risk exists,
changes to present animal management practices may be necessary to avert
increased losses caused by parasites (Morgan and Van, Dijk, 2012).
Computer simulation models, suitably adapted to the local ecology of H.
contortus, will be important tools for understanding the epidemiology of
infection under changing climatic conditions, and for developing recom-
mendations for sustainable control in different environments. As with
some other parasites critically dependent on conditions in the external envi-
ronment (Polley et al., 2010), changes to the geographical distribution of H.
contortus may prove to be a useful indicator of long-term climatic changes.
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7. CONCLUSIONS
Of all common nematodes of small ruminants, H. contortus has the
greatest capacity for serious pathogenic effects on a large scale and over a
wide climatic range. The expression of haemonchosis varies with the envi-
ronment and nature of the animal enterprise, from the rapid development of
heavy H. contortus burdens and potentially extensive mortalities within a
short time period, to more chronic forms, where smaller burdens are toler-
ated for long periods but become fatal when the nutritional status declines.
Whether the costs due to haemonchosis are due chiefly to heavy mortalities
and treatment costs, or to reduced animal production and occasional mor-
talities, H. contortus is generally considered the most economically significant
parasite of sheep and goats on a global scale.
The extraordinary ability of H. contortus to survive over a wide range of
climatic zones reflects unique biological characteristics that counter the sus-
ceptibility of the free-living stages to adverse environmental conditions.
Although essentially adapted to tropical or warm-temperature climates,
with a particular requirement for moisture for development from the egg
to the infective larval stage, the high biotic potential of H. contortus allows
the parasite to take advantage of transient periods when adequate moisture
coincides with sufficiently warm temperatures, in order to maximize the
probability of infection in grazing animals. Although the infective larvae
are relatively resilient, in general, their period of survival varies inversely
with the potential for population expansion. The larvae typically survive
for a relatively short period (weeks) in tropical and subtropical zones;
however, due to the continually high temperatures, a large proportion of
H. contortus eggs shed into the environment can develop rapidly. In contrast,
in cooler environments, the scale of egg development is limited or ceases
completely for prolonged periods, but the infective larvae survive for
considerable periods (months). In more hostile environments (extremes of
cold or aridity), H. contortus depends chiefly on hypobiosis (arrested develop-
ment) of the fourth-stage larvae, with the egg-laying adult worms present
mostly during the relatively brief periods when larval development is
possible. There is also evidence of intraspecific variation, with ecological
adaptations permitting H. contortus egg development outside the generally
recognized ideal climatic range; further investigations are necessary to
confirm that such variation occurs, including the existence of a genomic
basis to differences among isolates.
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Observations during mid-2010s suggest an extension to the geographical

range where significant H. contortus populations develop routinely, particu-
larly in colder, temperate climates in the Northern Hemisphere, where out-
breaks of haemonchosis have been attributed to temperature increases that
may reflect long-term climate changes. In this respect, the prevalence and
extent of significant H. contortus burdens might provide a useful general indi-
cator of environmental changes, as the numerous epidemiological investiga-
tions and surveys provide an extensive record of its historical climatic range.
The availability of detailed ecological data also provides a basis for predictions
of the immediate geographical and seasonal risk of haemonchosis, as well as of
longer-term changes to the endemic range.
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The Pathophysiology, Ecology and Epidemiology of

Chapter in Advances in Parasitology · May 2016

Brown Besier Jan Aucamp Van Wyk

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The Pathophysiology, Ecology

Advances in Parasitology, Volume 93

ruminants, and is the most important parasite of livestock in warm climatic

2. OCCURRENCE AND IMPORTANCE

epidemiological studies constitute a vast literature that deﬁnes its ecological

2.1.1 Tropical and subtropical climates

2.1.2 Warm temperate regions

seasonally dry conditions or droughts, although winter temperatures typi-

2.1.3 Cool temperate regions

2.1.4 Arid regions

protracted periods of rainfall, such as in the dry inland of northern Australia

2.2 Economic signiﬁcance

exacerbating the costs and complexity of control (chapter: Diagnosis,

3. PATHOGENESIS AND DISEASE

In acute haemonchosis, signiﬁcant anaemia develops over a relatively

compared with those in groups receiving feed supplements (Abbott et al.,

3.2 Clinical signs of disease

and does (presumably under the inﬂuence of the peri-parturient relaxation of

that unsuspected chronic haemonchosis occurs relatively common in situa-

environmental variables, as well as for estimations of egg and larval numbers.

4.1 Controlled environment studies

4.1.1 Moisture requirements for egg development and survival

R.B. Besier et al.

4.1.2 Moisture requirements for the survival of infective larvae

4.1.3 Temperature requirements for the development of eggs to

4.1.4 Temperature requirements for the survival of infective larvae

4.1.5 Intraspeciﬁc differences in critical requirements

adaptation strategy that allows H. contortus to extend its geographical range,

4.1.6 Other environmental factors

4.2 Ecological investigations in the ﬁeld

4.2.1 Tropical and subtropical climates

eggs recovered as infective larvae (typically 1e2%) raises a query as to

4.2.2 Warm, temperate and Mediterranean climates

presence of actively growing pasture, presumably as an index of the availabil-

4.2.3 Cool, temperate climates

4.2.4 Arid regions

survival periods of infective larvae decreased as temperatures increased (Altaif

4.2.5 Effect of microclimatic factors on larval development

2013b) found development at a considerably lower FMC, possibly due to

4.2.6 Lateral and vertical migration of infective larvae

5.1 Tropical and subtropical regions

Haemonchus contortus Infection in Small Ruminants

R.B. Besier et al.

1987; Dorney et al., 1995; Cheah and Rajamanickam, 1997; Chandrawa-

5.2 Warm, temperate climates

(E1-Azazy, 1990). However, in the Ebro Valley in Spain, under broadly

5.3 Cool temperate climates

5.4 Arid climates

6. PREDICTION OF THE OCCURRENCE OF

6.2 Potential effects of climate change

Observations during mid-2010s suggest an extension to the geographical

Fernandez-Ruvalcaba, M., Vazquez-Prats, V., Liebano-Hernandez, E., 1994. Development

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