Download Host-parasite interactions under extreme climatic conditions

Current Zoology
57 (3): 390−405, 2011
Host-parasite interactions under extreme climatic conditions
J. MARTINEZ1*, S. MERINO2
1
2
Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Alcalá, Alcalá de Henares, Madrid, Spain
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas,
Madrid, Spain
Abstract The effect that climatic changes can exert on parasitic interactions represents a multifactor problem whose results are
difficult to predict. The actual impact of changes will depend on their magnitude and the physiological tolerance of affected organisms. When the change is considered extreme (i.e. unusual weather events that are at the extremes of the historical distribution
for a given area), the probability of an alteration in an organisms’ homeostasis increases dramatically. However, factors determining the altered dynamics of host-parasite interactions due to an extreme change are the same as those acting in response to
changes of lower magnitude. Only a deep knowledge of these factors will help to produce more accurate predictive models for the
effects of extreme changes on parasitic interactions. Extreme environmental conditions may affect pathogens directly when they
include free-living stages in their life-cycles and indirectly through reduced resource availability for hosts and thus reduced ability
to produce efficient anti-parasite defenses, or by effects on host density affecting transmission dynamics of diseases or the frequency of intraspecific contact. What are the consequences for host-parasite interactions? Here we summarize the present knowledge on three principal factors in determining host-parasite associations; biodiversity, population density and immunocompetence.
In addition, we analyzed examples of the effects of environmental alteration of anthropogenic origin on parasitic systems because
the effects are analogous to that exerted by an extreme climatic change [Current Zoology 57 (3): 390–405, 2011].
Keywords
Biodiversity, Climate change, Immunocompetence, Parasite-host interactions, Pollution, Population density
The autonomous dynamics of our planet along with
the influences that other celestial bodies exert on it have
greatly been shaping the structure and physicalchemical characteristics of Earth in a way that allow it
to sustain life. Since the very beginning living beings
have acted as another factor in the dynamics of the
Earth, creating new opportunities for some organisms to
evolve, but simultaneously eliminating the stability of
conditions for others (e.g., Mayhew, 2006 and references therein). This lack of stasis has been a feature
since the origin of the Earth (Jansen et al., 2007).
Therefore, the generation or destruction of ecological
niches or enlargement or reduction of existing niches is
a constant in the dynamics of our planet (Millennium
Ecosystem Assessment, 2005). Biotic and abiotic environmental changes along with individual genetic variability of living beings are the engine for evolution by
natural selection and, therefore, are responsible for actual biodiversity at each geological time (Darwin,
1859).
These environmental changes are a wonderful possibility for geographic expansion and diversification of
some organisms, but for others denote the start of its
Received Feb 01, 2011; accepted Mar. 06, 2010.
∗ Corresponding author. E-mail: [email protected]
© 2011 Current Zoology
decline and even extinction. Extreme environmental
changes (i.e. unusual events that are at the extremes of
the historical distribution for a given area) are usually
faster and of shorter duration than less extreme changes
and thus the possibilities of organisms to adapt to these
events are in many cases dependent on the magnitude of
the change and the duration of its effects (NRC, 2002).
Of course the final impact of a change will depend on
the physiological tolerance of affected individuals, and
in this respect, eurytopic organisms, tolerant of highly
diverse conditions, are more likely to adapt to new environmental conditions, although these changes affect in
different degrees all organisms and, therefore, intra- and
interspecific ecological interactions.
In the case of parasitic interactions where there exists
a tight dependency of the parasites on their hosts, the
effect of an environmental change can affect asymmetrically both members of the association. Thus, the survival of parasites from environmental change will be
determined by several factors such as host dependence
and parasitic specificity, the complexity of the life cycle,
the biodiversity of the environment, the density and
mobility of their hosts and the physiological tolerance of
MARTINEZ J, MERINO S: Parasitism and extreme climate
individuals (resistance to both internal and external environments). For example, specific parasitic interactions
will be much more susceptible to a drastic reduction in
hosts density caused by an environmental change that
will hinder transmission to a new host as compared to
generalist parasitic interactions. This reduction in host
density could be extremely deleterious if organisms are
obligate parasites (Poulin, 1998). However, parasites
could even in this scenario survive under a certain
threshold of host density if they have sufficient phenotypic plasticity to adjust their level of virulence that
is, by increasing the time of permanence in the host
(Ewald, 1994). On the other hand, those parasites with
life cycles presenting free-living stages and especially
those without forms of resistance will also be more
susceptible to direct environmental changes (Bush et
al., 2001; De La Rocque et al., 2008; Mas-Coma et al.,
2008). In addition, we can expect that complex biological cycles are more susceptible to irreversibly
changes than in the case of direct cycles simply because the latter have shorter generation time and faster
population growth (Mas-Coma et al., 1987; Taylor et
al., 2001), and in complex cycles there are more possibilities that one of its phases or one of the hosts is affected by extreme environmental changes (Combes,
2001). Moreover, due to the reduced or absent motility
of many parasites, the possibility of escape from a
hostile environment shall be determined mainly by
their host mobility. However, the extent or change in
the geographical distribution of the hosts can open new
associations for both parasites that are transported by
hosts to a new area and for parasites that are present in
newly occupied areas (Tompkins and Gleason, 2006;
Hoberg, 2010; Biek and Real, 2010).
In addition, environmental changes can have an adverse effect on availability of resources necessary for
hosts to maintain an adequate nutritional status. In this
case individuals that do not have the ability to move
away from the focus of stress or find a way to exploit
other resources will see their health seriously compromised (Chandra, 1981; Merino and Møller, 2010), and
their immunocompetence could be reduced thereby facilitating settlement and reproduction of parasites (Santos, 1994; Christe et al., 2006; Merino, 2010). But not
only hosts present in the focus of change can be affected
negatively. As previously mentioned, displacement of
hosts to new areas may lead to the introduction of parasites without a previous coevolutionary history with
native hosts (Goodenough, 2010). The consequences for
such new host-parasite associations are unsuspected,
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including drastic reduction of host populations and even
extinction (see for example Warner, 1968; Van Riper et
al., 1986; Christe et al., 2006). However, such invasions
can be beneficial for the endemic fauna in some circumstances producing a dilution effect. In other words,
parasites are “diluted” among more species of hosts not
all of them being competent for the parasite to complete
its life cycle (Begon, 2008).
The number of potential scenarios to take into account after an abrupt environmental change is enormous
due to the large number of variables that affect the different parasite systems in a given ecosystem. However,
the more interesting effects of these changes are on public and veterinary health due to their social and economic costs (see also NRC, 2002). Thus, the most
feared harmful effects of such changes are relapses
and/or expansion of certain parasitic diseases that could
affect large human populations or agriculture
(Macpherson, 2005; Brooks and Hoberg, 2007; Morgan
and Wall, 2009). However, the deleterious effects of
such changes on wildlife and ecosystems may have
consequences for conservation (Christe et al., 2006;
Ostfeld et al., 2008).
In this paper we synthesize relevant information on
the determinants of parasite-host interactions affected
by extreme conditions. Due to the scarcity of studies on
the effects of extreme climate changes on host-parasite
interactions, and the fact that the same factors are implied in responses to environmental changes of different
degree, we explore these factors having in mind that
such changes are of great magnitude and short duration.
We specifically explore the following three aspects of
extreme changes on parasite-host associations (Fig. 1):
(i) the possibility that environmental changes impact
three main aspects that can affect the equilibrium of
parasite-host relationships; biodiversity, population density and immunocompetence, (ii) the difficulty of predicting effects of particular environmental change on
parasite-host interactions because of dependence on
intrinsic characteristics of each parasitic interaction, but
also on all ecological interactions maintained in the
ecosystem by the parasitic relationship; and (iii) the
potential effect of socioeconomic advance of developing
countries along with the implementation of control programmes in the reduction of impact of global diseases.
We have included examples of the effects of anthropogenic changes on parasitic systems because such effects
are analogous to those exerted by extreme climatic
change, although in general such effects tend to be permanent rather than reversible.
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Fig. 1 Schematic representation of the mechanisms affecting host-parasite interactions following an extreme
environmental alteration
1 Biodiversity
Ecosystems with a high biodiversity favour the existence of many interspecific relationships that could
show high buffering capacity to environmental perturbations (Bravo de Guenni et al., 2005). However, under
abrupt environmental change ecological interactions
may suffer fast and profound alterations. With respect to
the parasite-host systems, the first sign of imbalance is
fluctuation in the incidence of disease further deepening
the initial imbalance. For example, there is evidence of
a clear relationship between biodiversity decline and
increase in transmission of certain diseases (Keesing et
al., 2010). The dilution effect hypothesis suggests the
existence of several biological mechanisms in complex
communities acting to reduce the risk of transmission of
diseases (Keesing et al., 2006). Several of these mechanisms have been characterized in parasitic systems, notably including the existence of decoy and suboptimal
hosts, predation, hyper-parasitism, physical interference,
and toxic-production (Johnson and Thieltges, 2010). We
briefly explain these mechanisms.
Decoy hosts are species that are not part of the life
cycle of the pathogen. The presence of such hosts increases the possibility that parasites encounter them
without being able to complete the life cycle and therefore reducing the number of contacts with specific hosts
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and hence transmission of the disease. In the case of
suboptimal hosts the parasite can complete the life cycle
and the disease can be transmitted, but not as efficiently
as in the case of the specific host. In both cases the force
of transmission is clearly reduced. An increase in the
probability of parasites to contact a specific host can
emerge if an extreme environmental change affects biodiversity by reducing the number of no-competent hosts
for the parasite. In contrast, if the decrease in the number of competent hosts occurs transmission of the disease will also be reduced. In other words, a reduction in
biodiversity due to an extreme change can affect the
dynamics of disease transmission in different ways depending on the characteristics of the host species mostly
affected. However, several studies have shown that a
reduction in biodiversity negatively affects the species
unable to transmit the disease, thus producing an increase in the transmission of the pathogen (for example
Lyme disease and hantavirus in rodents or West Nile
virus in birds; Kosoy et al., 1997; Allan et al., 2009;
Suzán et al., 2009). One of the best examples of the relationship between disease transmission and biodiversity is offered by the spread of Lyme disease in northeast USA (LoGiudice et al., 2008; Keesing et al., 2009).
This bacterial disease is caused by a species of the genus Borrelia and is transmitted to mammal hosts by
ticks. The main reservoir of the disease in the area is
white-footed mice Peromyscus leucopus. However, the
presence of Virginia possum Didelphis virginiana
clearly determines the incidence of the diseases in human populations. The marsupial species acts as suboptimal hosts of ticks because they are able to eliminate
most ticks attached to their bodies. In areas where the
density of marsupials is high the transmission of Lyme
disease is low because the density of ticks is also low.
However, in areas with low biodiversity due to environmental degradation the presence of the marsupial is
reduced thus increasing the population of mice that are
not efficient at avoiding tick infestations. As a consequence density of ticks is higher and therefore the
transmission of the disease. It is possible that the same
characteristics that allow some hosts to resist environmental change that provoke a reduction in biodiversity
can also increase susceptibility of these hosts to infection (Keesing et al., 2010). In this respect it is important
to note that species with a high reproductive and developmental rate are more resistant to environmental
change, but in addition they also have lower levels of
adaptive immunity (Martin et al., 2006, 2007a; Lee et
al., 2008).
MARTINEZ J, MERINO S: Parasitism and extreme climate
The dilution effect provoked by the presence of incompetent hosts or hosts with low competence has been
also characterized in diseases with complex life cycles.
For example, transmission of the trematode Schistosoma
mansoni depends on the presence of appropriate freshwater snails acting as intermediate hosts of miradicida, a
free living parasite life stage emerging from eggs. An
experiment using competent and incompetent snails
showed that transmission of the parasite is clearly reduced as compared with the transmission when only
competent snails are present. The result is a lower production of cercariae, the parasitic infective stage for
humans, in the snails, and, therefore, a lower risk of
transmission of the disease (Johnson et al., 2009). A
similar case has been reported for a trematode of the
genus Ribeiroia. This parasite uses snails as first intermediate hosts, several species of amphibians as second
intermediate hosts and different species of birds as definitive hosts. An experimental study showed that the
introduction of two species of amphibians with different
degrees of compatibility with the parasite caused a
lower level of production of cercariae compared with
production when only the more competent species is
present (Johnson et al., 2008).
However, the presence of a less competent host is not
always necessary for production of a dilution effect in a
parasitic interaction. The trematode Renicola roscovita
uses different species of bivalves as intermediate hosts
and birds as definitive hosts. In two localities in the
northern Wadden Sea two species of introduced bivalves
are competent hosts for R. roscovita. However, definite
hosts only prey upon endemic bivalves thus reducing
the possibilities of successful parasite transmission
(Krakau et al., 2006).
Predation and hyperparasitism are other biological
mechanisms related to the dilution effect. In a complex
ecosystem these mechanisms are more likely to occur
due to the higher number of species in the system and
they can play an important role in the transmission of
certain diseases. For example, experimental systems
have shown that predation on larvae of the nematode
Strelkovimermis spiculatus by copepods reduces both
prevalence and density of parasites infecting the next
hosts, the mosquito Aedes aegypti. In some cases the
predation rate reaches 100% of the larvae (Achinelly et
al., 2003). In the case of the life cycle of Schistosoma
mansoni introduction of the predator Lebistes reticulates,
a guppy fish, produces an important reduction in both
miracidia and cercarie, thus reducing the infection rate
of intermediate hosts, the snail Biomphalaria glabrata,
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and also of definitive hosts (Pellegrino et al., 1966).
Cases of predation decreasing parasite transmission
have been described for other systems (Thieltges et al.,
2008; Johnson et al., 2010) including some implying
species of protozoa (Beauchamp et al., 2005) and fungi
(Kagami et al., 2004). In contrast hyperparasitism can
diminish transmission success of some diseases, as is
the case of trematode species susceptible to infection by
microsporidia (Knapp et al., 1972). In addition, in complex systems the density of organisms in the area can
interfere with transmission of diseases simply by direct
physical avoidance of movements of aquatic free-living
forms of parasites (Prinz et al., 2009) or by the production and liberation of toxic substances in the environment that affects parasites (Christensen, 1980).
Although the dilution effect in complex systems can
be expected due to higher number of species present
that potentially can affect parasitic transmission as
compared with more simple systems, an increase in the
number of species in a system does not always cause a
dilution effect on parasite transmission (Upatham and
Sturrock, 1973) and even in some cases an increase in
the risk of infection has been reported (Begon, 2008).
The net effect that a change in biodiversity can generate
on certain host-parasite systems will be related to the
kind of interaction maintained by the parasite with the
species affected by the change (Johnson and Thieltges,
2010). In addition, parasite intrinsic factors such as fertility, resistance of parasitic forms in the environment,
and parasitic specificity can counteract the potential
dilution effect (Johnson and Thieltges, 2010).
The alleged benefits of biodiversity buffering the
transmission of certain diseases have to be weighed
against the greater diversity of infectious pathogens. In
fact, a latitudinal gradient in biodiversity, including
pathogens, decreasing as we move away from the equator has been described (Rohde, 1992; Guernier et al.,
2004; Hillebrand, 2004; Jones et al., 2008; Merino et al.,
2008). However, other studies have shown contradictory
results in this respect. For example, Nunn et al. (2005)
found this pattern in primates only for protozoans, but
not for viruses or helminths, and Poulin (1995) and
Bordes et al. (2010) did not find any correlation between helminth species richness at intra- or interspecific
levels and latitude. Moreover, Lindenfors et al. (2007)
and Krasnov et al. (2004) found the opposite pattern for
helminths of carnivores and fleas on rodents, respectively, although the asymmetric sampling effort could be
one explanation for these inconsistent results (Poulin,
1995; Lindenfors et al., 2007). The need for special re-
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quirements for parasite transmission that do not follow a
clear latitudinal distribution and/or spread of diseases by
migratory hosts can also affect the latitudinal gradient in
parasitic diseases (Merino et al., 2008). Regardless of
whether the correlation between parasitic species richness and latitude is general or specific, some authors
have suggested that prevalence of a particular parasite
may be low in areas with high biodiversity, which usually occurs at low latitudes, as compared with other regions with less biodiversity that usually occurs at higher
latitudes (Johnson and Thieltges, 2010). However, (i)
studies showing the existence of a latitudinal gradient
for virulence of diseases, being higher at low latitudes
(Møller et al., 2009; Robar et al., 2010), and (ii) the
possible relationship between biodiversity and emergent
diseases constitute two serious difficulties for the dilution effect hypothesis (Woolhouse and GowtageSequeria, 2005; Jones et al., 2008).
2 Host Density and Prevalence
Density of hosts, vectors and parasites in a geographic area are key factors for disease transmission.
Any extreme environmental change can alter the density
of every component of the host-parasite system, and,
therefore, the prevalence of the disease. Some causes of
extreme environmental change are related to human
activity like agriculture, livestock farming, hunting,
urbanisation, pollution and transports (Macpherson,
2005; Hayes et al., 2010). However, we cannot disregard the impact of climatic change on parasitic interactions (Marcogliese, 2008; Pech et al., 2010). Regardless
of the origin of environmental changes, these may have
an impact on different aspects that ultimately affect the
density of hosts and parasites: survival, phenology, behaviour and/or distribution range.
In parasite-host systems dependent on vectors or
possessing free-living stages, weather conditions to a
large extent determine the transmission of diseases.
Variation in temperature and rainfall regime can cause
fluctuations in density and distribution of hosts and
parasites. Species that act as vectors of many infectious
and parasitic diseases are usually arthropods showing a
high dependence on environmental temperature for their
survival and development. In fact, there are studies that
demonstrate a positive correlation between the degree of
feeding activity, reproduction and mortality of mosquitoes and ticks with temperature (Drew and Samuel,
1986; Loetti et al., 2008; Freire and Schweigmann, 2009;
Estrada-Peña et al., 2011). Vector distribution range also
seems to be related to an increase in temperature
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(Hunter, 2003; Rogers and Randolph, 2006; Genchi et
al., 2009). The result of this increase in temperature is
an increase in density of vectors that may cause the appearance of diseases in new regions and/or increased
transmission in endemic regions. Rainfall regime may
also alter the density of vectors. An increase in precipitation can promote reproduction of water-dependent
species allowing them to complete their life cycle. This
is the case for different mosquito species whose abundance is associated with the prevalence of the diseases
that they transmit (Gill, 1938; Wegbreit and Reisen,
2000; Tong and Hu, 2001; Zhou et al., 2004; Shaman
and Day, 2007).
Obviously, decreases in temperature below a certain
threshold or prolonged drought will have the opposite
effect, decreasing the density of vectors and the prevalence of diseases they are transmitting. There are some
examples of such relationships between climate and
density or incidence of parasites and diseases transmitted by them. For example, some studies have linked an
increase in temperature associated with NAO and
ENSO with the advance in development of species of
ticks and increased transmission by seabirds (Duffy,
1983; Boulinier and Danchin, 1996). Other studies report the adverse effect of minimum temperature and
wind on the abundance of Simulium blackflies attacking
nests of birds (Martínez-de la Puente et al., 2009), or the
potential importance of nest temperature as a cue used
by insects for locating nests of their hosts (Martínez-de
la Puente et al., 2010). The advancement of spring in
parts of Northern Europe due to an increase in temperature has affected the phenology of parasites and their
abundance. In particular, advancement in phenology of
the hippoboscid fly Ornithomyia avicularia was associated with a higher prevalence of this parasite in barn
swallows Hirundo rustica (Møller, 2010). Other studies
have found that a rainy and cold spring negatively affects the abundance of certain ectoparasites of birds
(Merino and Potti, 1996). The effect of temperature on
the abundance of ectoparasites has also been experimentally demonstrated in nests of the tree swallow
Tachycineta bicolor parasitized by Protocalliphora
blowfly larvae, with an increase in the number of larvae
with an increase in temperature up to 25°C (Dawson et
al., 2005). In the case of the nematode Setaria tundra
transmitted to reindeer Rangifer tarandus by mosquitoes
of the genera Aedes and Anopheles, there is a positive
relationship between average summer temperature,
vector density and prevalence of helminths in their definitive hosts (Laaksonen et al., 2009). Tempera-
MARTINEZ J, MERINO S: Parasitism and extreme climate
ture/abundance relationships seem clear for ectoparasites showing autonomy outside their hosts, while parasite species more dependent on their hosts are less susceptible to fluctuations in temperature (Møller, 2010).
Parasites with free-living stages in their life cycles are
especially sensitive to changes in temperature and humidity (Bush et al., 2001). In particular, an increase in
temperature and rainfall increases survival and development of free-living larvae of the nematode Trichostronylus tenuis, a fact that affects the population dynamics of its definitive host, the red grouse Lagopus
lagopus (Hudson, 1986; Hudson et al., 1992, 1998).
Another study shows the beneficial effect of an increase
in temperature on development of fluke cercariae, increasing levels of infection in their intermediate hosts
(Poulin, 2006). Other studies on flukes demonstrate the
close relationship between rainfall regime and the proportion of hosts infected by different species of Digenea
(Pech et al., 2010). Moreover, this relationship has a
marked seasonality clearly explained by the amount of
rainfall, and such seasonality have also been observed in
diseases caused by intestinal nematodes in domestic
animals (van Dijk et al., 2008). The positive effect of an
increase in temperature has also been noted in some
species of protozoa. In particular the ciliated Orchitophrya stellarum, parasite of starfish, shows a faster development between 10 and 15°C, and in addition an
increase in infectivity is also noted (Bates et al., 2010).
Seasonality in the prevalence of certain parasitic diseases is a feature of regions where there is marked fluctuation in weather conditions, indicating that the parasites dependent on external environmental conditions
can only develop within certain thresholds of temperature and rainfall. Therefore, these conditions limit the
transmission of diseases caused by parasites. The increase in temperature and humidity in certain geographic areas can not only increase the abundance and
the prevalence of parasites, but also their range and that
of their hosts. The expansion of the range of certain
vectors such as mosquitoes has occurred for altitude on
the Hawaii Islands (Atkinson, 2008; Lovejoy, 2008) and
latitude in New Zealand (Tompkins and Gleeson, 2006).
In both cases the change of distribution of the vectors
would be associated with an increase in the prevalence
of diseases transmitted, in these two cases listed above
avian malaria.
Several models predict change in abundance and/or
distribution of diseases under scenarios of climate
change. Some models predict an increase in prevalence
of toxoplasmosis in human populations in parts of
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North-western Europe if the trends of increasing temperature and precipitation continue because survival of
oocysts of the parasite is favoured under these conditions (Meerburg and Kijlstra, 2009). Other models predict an increase in the prevalence of Dirofilariosis in
Europe due to the alleged temperature increase announced by IPCC. In this case both development of the
parasite in the vector (mosquito) and its expansion to
more northern areas would be favoured (Genchi et al.,
2009). The parasite-host system formed by the pulmonary nematode Umingmakstrongylus pallikuukensis and
the musk ox Ovibos moschatus is yet another example
of how to integrate empirical and experimental knowledge acquired in a predictive model. The nematode depends on a snail as intermediary host to complete its life
cycle, but its development is slow due to low temperatures in the Arctic (Kutz et al., 2002). Generally, the
parasite takes two years to be infective, which implies
survival of the harsh winter to reach the definitive host.
This fact reduces the success of the parasite because
many individuals fail to overcome the winter. However,
if the increase in average temperature in this area during
recent years is included in the model, nematode infectivity could be achieved in only one year, before the
arrival of winter. Therefore, mortality of larval stages
decreased considerably, leaving more larvae available
for infection of the definitive host causing an increase in
the pressure of the parasite on muskoxen (Kutz et al.,
2005).
Therefore, factors that should be taken into account
to assess the impact of extreme climatic changes on
parasitic relationships would be (i) autonomy and resistance exhibited by parasites outside their host. For example, some ectoparasites such as flies that are also
vectors of diseases have sufficient autonomy away from
their hosts, but are very susceptible to fluctuations in
temperature and humidity from a phenologic point of
view. However, some ectoparasites are totally dependent
on their hosts (lice and some mites), and although they
are affected to a lesser extent by changes in weather,
they are more susceptible to fluctuations in density of
their hosts; (ii) parasite specificity because highly specific parasites will have greater difficulty finding a host
if their density drops due to environmental change; and
(iii) type and complexity of epidemiological cycle because parasites with complex life cycles that depend on
invertebrate intermediate hosts (for example, flukes) or
with free-living stages (for example nematodes) also
experience more difficulties completing their life cycle,
because in both cases they lack homeostatic mecha-
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nisms to resist wide fluctuations in temperature and humidity. Parasites with resistant forms such as eggs or
cysts will be affected to a lesser extent because these
adaptations allow them to expand their range of tolerance to environmental changes.
A good example of the possible effect caused by the
introduction of a new species in an established ecosystem occurred in Canada. In order to reduce the pressure
exerted by hunting on certain species of ungulates such
as caribou Rangifer tarandus and moose Alces alces,
white-tailed deer Odocoileus virginianus were introduced from another region where the tick Dermacentor
albipictus was common (Kutz et al., 2009). However,
the introduced deer are a perfect reservoir of ticks for
the other species of ungulates to be protected. Although
it is unclear whether ticks come from infected introduced individuals, it seems obvious that the introduction
of deer has considerably increased the abundance of this
species of tick, with serious consequences for the endemic fauna as for example chronic weight loss, anemia,
hypoalbuminemia, hypophosphatemia, transient decreases in serum aspartate transaminase and calcium
and hair loss in moose (Glines and Samuel, 1989; Samuel, 1989). Another example that illustrates the importance of population density for transmission of diseases
comes from Malaysia. In this region, frugivorous bats
are host of Nipah virus and they transmit this disease to
domestic pigs. The disease spreads at high speed among
pigs due to their high density in local farms and finally
jumps to humans without much difficulty (Epstein et al.,
2006).
Population density can also be affected indirectly by
pollution. In particular, the use of fertilizers containing
N2 causes eutrophication of ecosystems, increasing primary productivity. This fact positively affects reproduction and development of certain intermediary hosts
(snails) and vectors (mosquitoes), as well as certain
bacteria and fungi, increasing the efficiency of transmission of certain diseases (McKenzie and Townsend,
2007). However, an increase in nutrients can also promote development of competitors or predators of hosts
infected by parasites, and in this case a reduction in
transmission of the disease can occur. In addition, under
conditions of increased parasite transmission, as is usual
when host density increases, an increase in virulence is
expected simply because ease of transmission can select
for more virulent parasite lineages (Ewald, 1994) and
consequently an increase in immune response (Møller et
al., 2006).
The effects of phenologic changes in migratory spe-
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cies can be direct if they imply a change in density of
hosts and parasites, and therefore in transmission of
diseases, or they can be indirect if they increase in susceptibility to infection due to immunosuppression
caused by a reduction in appropriate nutrients (see next
section). In the case where movement implies a change
in their range, they can be considered invasive species
and their effects for native species may be very different.
For example, if an invasive species introduces new
parasites into an area, they could have (i) a deleterious
effect on the host endemic species if their immune system has not the appropriate response to control new
parasites, or (ii) a beneficial effect if the novel parasites
compete with endemic parasites. However, competition
between parasites may also produce an increase in virulence if competition selects for parasites being able to
obtain resources at a fast rate to outcompete other parasite lineages (Frank, 1996).
3 Immunosuppression
When biodiversity and density of parasites and hosts
allow contact between the two members of the hypothetical parasitic interaction, the immune system determines the future of the association (Combes, 2001; Merino, 2010). The system of protection against intrusion
includes multiple mechanisms, from simple physical
barriers like the skin and mucous membranes to very
specific adaptive mechanisms at the cellular level like
the production of antibodies. Investment in immunity is
a balance between the energetic cost involved in
mounting a particular response (Råberg et al., 2000;
Martínez et al., 2004), the collateral damage that this
response can generate in the host, and the protection that
it provides (Råberg et al., 1998), this balance differing
among pathogens. The more complex defensive mechanisms are accurately adjusted at the neuroendocrine
level although numerous circumstances may alter this
adjustment. Factors that may be involved in the alteration of the adjustment of the immune system and therefore the balance of the parasitic associations tend to be
associated with the presence of (i) chemical contamination of human origin, and (ii) different types of stress
especially heat and nutritional stress and/or infection by
certain pathogens. Although many of these factors can
modulate immune mechanisms, the increased susceptibility to a disease will depend upon the altered mechanism and on the magnitude of the change, because the
immune system is able to act properly exercising its
protective role within ranges that are characteristic for
every immunological parameter and pathogen (Adamo,
MARTINEZ J, MERINO S: Parasitism and extreme climate
2004). The effects that chemical pollutants exert on the
immune system can directly impact on the cells of the
immune system and on the production of soluble mediators like antibodies and cytokines (Dunier and Siwicki, 1993; Banerjee, 1999; Voccia et al., 1999), and
on the neuroendocrine system (Colborn et al., 1993),
which regulates development, maturation and activity of
the immune system (by secretion of hormones like oestrogen, thyroid hormones and glucocorticoids)
(Grossman, 1984; Lam et al., 2005; Sternberg, 2006).
Although numerous studies have shown the toxic/
modulator effect of numerous chemical pollutants on the
immune system, very few directly relate changes of
susceptibility to a disease with immunological alterations caused by pollutants. However, two studies carried
out on amphibians suggest that the pesticides atrazine
and malation have an effect on the increase of certain
infections (Hayes et al., 2006, 2010; Denver, 2009).
The immune mechanisms protecting individuals from
pathogens are energetically expensive to maintain
(Råberg et al., 2000; Ots et al., 2001; Martin et al., 2003,
2007b; Martínez et al., 2004), and, therefore, any energy
deficit caused by a reduction in resources or an increase
in basal metabolic rate may indirectly affect immune
response. Individuals subject to this type of nutritional
stress redistribute energy to vital physiological systems
while neglecting others such as the immune system.
This relationship has been established in different species naturally undergoing high energetic demands (reproduction) or under experimental restriction of food
intake (Sheldon and Verhulst, 1996; Ardia et al., 2003;
French et al., 2009). Therefore, any environmental
change that causes nutritional stress may adversely affect the immune system and consequently susceptibility
to disease. Chemical contaminants may also have this
indirect effect on the immune system, because different
species of fish, amphibians and reptiles when exposed
to industrial effluents show abnormally high metabolic
rates and reduced growth (Hopkins et al., 1999; Rowe et
al., 2001). Nutritional stress can also be produced by a
redistribution of ecological associations present in the
ecosystem. For example, a change that promotes increases in competitors and/or predators may provoke
nutritional stress by a reduction in resources caused by
competition or an increase in the metabolic rate caused
by predators (Martin et al., 2010). In fact a study shows
that the introduction of a predator species affects the
level of stress of the native prey species (Berger et al.,
2007).
The environmental changes that affect air tempera-
397
ture can cause heat stress in individuals depending on
their thermoregulation system and the magnitude and
duration of the change (Bowden et al., 2007; Deutsch et
al., 2008). Both increases and decreases in temperature
can alter immune system functions involved in resistance to infections. It is know that heat stress in ectotherm animals adversely affects certain immune mechanisms as phagocytosis (Wang et al., 2008), oxidative
capacity (Coteur et al., 2004), the prophenoloxidase
system (Vargas-Albores et al., 1998) and the synthesis
of antibodies (Maniero and Carey, 1997). Something
similar occurs in endotherm animals, where a decrease
in innate and adaptive immune response is associated
with increases in temperature (Sinclair and Lochmiller,
2000; Zahraa, 2008). Sometimes an increase in temperature can enhance the performance of the immune
system by inducing greater production of lysozyme and
IgM (Chen et al., 2002; Dominguez et al., 2004; Ndong
et al., 2007). Moreover, elevated body temperature (fever) produced by infection in endotherm animals is a
very useful adaptive mechanism for generating a hostile
environment for the intruder and for promoting activation of the immune system (Hanson, 1997). This apparent contradiction can be explained by taking into account the magnitude and duration of heat stress, because
prior acclimation of individuals to thermal conditions
removes the immunosuppressive effect of the stress
(Demas and Nelson, 1998; Shephard and Shek, 1998;
Ksiazek et al., 2003). Thus, fluctuation in temperature is
as important as the time interval during which it occurs.
Although the relationship between thermal stress and
immunosuppression seems evident, this direct association with disease episodes or increases in susceptibility
to certain infections has been confirmed in only few
cases. However, numerous studies have linked the onset
of epidemic outbreaks with extreme fluctuations in both
cold and heat for different parasite-host systems (Chisholm and Smith, 1994; Cook et al., 1998; Paillard et al.,
2004; Bruno et al., 2007; Harvell et al., 2007; Travers et
al., 2008; Wegner et al., 2008; McClanahan et al., 2009).
In the future these systems could be the basis for establishing the immunological mechanisms that are imbalanced by heat stress.
In some parasitic associations, proper functioning of
the immune system of the hosts can be compromised as
a result of the action of the parasite. A good example of
this fact is the human immunodeficiency virus (HIV).
This virus causes immunosuppression in affected individuals, making them much more susceptible to diseases
of all kinds (Frebel et al., 2010). This immunosuppres-
398
Current Zoology
sive effect caused by HIV is not an exception as it is
well documented for other parasitic infections (Nussenzweig, 1982; Leiro et al., 1988; Maizels et al., 1993;
Szteina and Kierszenbaumb, 1993; Allen and MacDonald, 1998; Boëte et al., 2004; Maizels, 2009;
Maizels et al., 2009; Stempin et al., 2010).
Finally, it is important to mention the role of the microbiomas, microbial endosymbiotic communities living
in a particular organism, on the immune system. About
90% of the cells in humans are bacteria (Turnbaugh et
al., 2007). These microorganisms live in all kinds of
epithelial tissues where they established so tight relations with the host that proper functioning of the tissue
would be impossible without the presence of these organisms. In addition, they are able to exert a protective
role against certain diseases because the alteration of
these microbial communities has been linked on several
occasions to increased susceptibility to a disease
(Holzman et al., 2001; Roos et al., 2001; Chang et al.,
2008). This benefit has not only been found in humans,
but also in other mammals, amphibians and even corals
(Harris et al., 2009; Lawley et al., 2009; Sunagawa et al.,
2009). In some cases the protective effect is exercised
by competition between species, either preventing the
development of the pathogens installed in the host or by
blocking their invasion. This protective role is sufficiently important to consider microbiomas as part of the
innate immune system acting as a first barrier of defence. However, their role seems to go further as studies
show an active role of these organisms in the modulation of immune responses (Isolauri et al., 2001; Forsythe
and Bienenstock, 2010; Kelly, 2010; Nayak, 2010; Trebichavsky et al., 2010; Gourbeyre et al., 2011). It is
clear that if extreme environmental changes affect these
symbiotic relationships, an indirect effect of the environmental change on immunity of hosts may favour the
spread of diseases.
4 Consequences and Future Directions
Alterations of host-parasite relations caused by environmental change often produce undesired effects on
public and veterinary health (Mas-Coma et al., 2008;
http://who.int/globalchange/climate/summary/en/index5.
html). From the health point of view, the occurrence of
outbreaks of new or established diseases in a given region is a concern for health authorities. This has
prompted recent studies of factors contributing to such
epidemics/pandemics as well as preventive measures
(Harrus and Baneth, 2005; Macpherson, 2005; Brooks
and Hoberg, 2007; Omenn, 2010). A recent study dem-
Vol. 57
No. 3
onstrated that the diversity of human pathogens present
in a given region is explained by an astonishing 72% by
the diversity of mammals and birds present in the area
(Dunn et al., 2010). In contrast, the prevalence of human diseases is positively related to the diversity of
pathogens, the size of the population, climate and investment in campaigns of control (Dunn et al., 2010).
Given these data, and considering that less diverse ecosystems support fewer human pathogens, there could be
a conflict between conservation and health. However,
the net benefits provided by complex ecosystems to
humans (Costanza et al., 1997) discard completely the
possibility of reduction of biodiversity to solve health
problems. In the same study, the economic investment
in control campaigns appeared as a very important
variable in predicting the prevalence of human diseases.
The economic investment does not reduce the diversity
of pathogens, but shows a very significant impact on
reducing the prevalence of diseases, especially in regions with many inhabitants, high prevalences and low
or no investment in prevention campaigns. As a conclusion, the authors propose to invest money in such regions, because a small investment will produce a significant reduction in prevalence. By reducing the prevalence in these areas the probability of occurrence of a
disease outbreak and, thus, of a pandemic is considerably reduced. Therefore, this recommendation would
have a benefit on a global scale. Such measures should
be carried out especially in areas with high incidence of
extreme environmental changes so that the potential for
spread of diseases following the event is reduced.
Attempts to completely eradicate a disease with a
low prevalence are not very realistic as this requires
thorough monitoring of the disease with the costs that
this entails. A real example of the implementation of
these recommendations is based on malaria. Using predictive models some researchers have predicted an increase in endemicity, morbidity and mortality of human
parasitosis in general (McMichael et al., 2006; Senior,
2008; Semenza and Menne, 2009) and of malaria in
particular (Tanser et al., 2003; van Lieshout et al., 2004)
due to the hypothetical increase in global average temperature during the present century. However, the extent
of endemic malaria areas in the world between 1900 and
2007 has been considerably reduced in spite of this period being characterized by global warming (Gething et
al., 2010). This apparent paradox is resolved if we consider effects of urbanization and economic development
during the 20th century, namely, development of therapies and health infrastructure and investment in control
MARTINEZ J, MERINO S: Parasitism and extreme climate
campaigns on a large scale (Kleinschmidt et al., 2006;
Sharp et al., 2007; Teklehaimanot et al., 2009). Therefore, the predictive models on the dynamics of a given
disease should take the effects of these variables into
account. However, the potential increase of extreme
climatic events can destroy or pose important difficulties for development and implement of any measure to
control the extent of diseases. In this respect, international action to control emerging epidemics following
extreme environmental change, with special emphasis
on areas with higher incidence of these events, is probably the only possible prevention measure.
A case apparently opposite to that of malaria is
schistosomiasis with the etiological agent being the
fluke Schistosoma japonicum. The prevalence of this
disease has shown an increase in certain areas of China
despite investments by the government in control campaigns during the last decades (Liang et al., 2007). The
epidemiological cycle of this parasite is totally dependent on water availability for survival of their
free-living forms and development of their intermediate
host (freshwater snails). Although some studies attribute
a role to the overall increase in temperature in this case
(Zhou et al., 2005), the main cause seems to be greater
impact caused by building of the Three George dam that
generates the right environmental conditions to facilitate
transmission of this disease (Maszle et al., 1998; Remais
et al., 2007). In fact, numerous dams such as the Aswan
Dam in Egypt, the Tigay dam in Ethiopia, the Kossou
and Taabo dams in Cote d'Ivoire, the Diama dam in
Senegal and Manantali dam in Mali have resulted in
major outbreaks of schistosomiasis (http://ehs.sph.
berkeley.edu/china/current_projects/Environmental_
Change.htm). Although the economic implications of
the dam for China may justify its construction, control
campaigns should have emphasised the increased risk of
transmission that it entails. Therefore, uncoordinated
policies can lead to a high economic cost without
achieving the proposed objectives, that is, the reduction
or eradication of a disease. Such cases can be considered similar to the production of important and recurrent floods in some areas and the same logistic measures
should be carried out to avoid the spread of diseases.
The lack of foresight exhibited by some predictive
models is the result of the classical view of ecological
sciences on humans and nature (Millennium Ecosystem
Assessment, 2005). That view has traditionally separated humans from nature, ignoring the human feedback
on ecosystems and biomes (Ellis and Ramankutty, 2008).
However, as most of the world is constituted of
399
human-dominated ecosystems, future predictive models
should take the socio-ecological system (Alessa et al.,
2008) and the concept of anthropogenic biome (Alessa
and Chapin, 2008; Ellis and Ramankutty, 2008) into
account to achieve a more realistic approach to the consequences of the social and environmental changes.
From a veterinary perspective implications are usually economic since the appearance of disease outbreaks,
or simply an increase in the abundance of certain parasites, often lead to a detriment of animal health and a
reduction in productivity (Morgan and Wall, 2009). The
overcrowding of animals is a determining factor in the
transmission of certain pathogens (Bisdorff et al., 2006),
while those feeding on the vegetation are most susceptible to parasites with free living stages like nematodes
(O’Connor et al., 2006). However, it is almost impossible to avoid overcrowding of surviving livestock after
an extreme event due to the disappearance of appropriate space for livestock and other domestic animals.
Health and veterinary problems are not independent.
In the last 10 years about 75% of new diseases detected
in humans have been caused by pathogens of animals or
animal products. Some of these zoonotic diseases can
follow an extreme climatic event and have the potential
to extend globally and therefore to cause serious health
problems (http://www.who.int/zoonoses/en/). However,
other diseases are easily prevented, but remain prevalent
in developing countries, especially in poorer populations. One of the first consequences of extreme climatic
conditions as well as human activity is habitat destruction and thus shrinking ecosystems. Under these conditions an increase in pathogenicity is expected, mainly
due to the increase in host density and influx of new
diseases in fragmented areas (Holmes, 1996). Therefore,
special attention to the potential emergence of diseases
should be directed to such newly fragmented habitats,
where contact between different areas increases abruptly,
allowing for the contact between different organisms
with new parasitic interactions.
5
Conclusion
The consequences of environmental changes on
parasite-host interactions are difficult to forecast. To do
that we should know all abiotic and biotic factors that
determine the stability of the specific interaction, and
this implies a deep knowledge not only of the epidemiological cycle of the parasite, but also of the entire ecosystem in which the interaction takes place. Although
the stability of ecological associations is a chimera,
parasitic associations with certain stability probably
400
Current Zoology
occurred long ago in conditions of little fluctuation in
abiotic and biotic factors. Small environmental disturbances may especially be buffered in complex ecological systems. Sudden environmental changes often generate the rupture of the dynamic equilibrium of an interaction, and they may have a negative impact at a
medical, veterinary and environmental level. The origin
of such changes can be natural or anthropogenic, the
latter being more important for sudden environmental
changes observed in recent years. In addition, natural
changes can contribute to the extent and duration of
changes of anthropogenic origin (for example extreme
weather episodes like hurricanes or floods can spread
pollutants or toxic substances or generate accidents that
acute spills of toxic products in the environment).
From the information above it is clear that regardless
of the origin of environmental changes, they always
generate an alteration of ecosystems through three fundamental factors that are important for parasites; biodiversity, the density of organisms and/or immunocompetence. Individual tolerance to these environmental
changes is what determines the degree of impact on
these three factors, and this finally determines the effect
on transmission of a disease. The change produced on
the dynamic of the disease will be totally dependent on
the kind of parasitic interaction and all its relations
within the ecosystem, including human interventions. In
the future, predictive models should include the
socio-ecological system and the anthropogenic biomes
concept to improve their accuracy. Prevention measures
to control and/or eradicate potential epidemic diseases
should be carried out in areas where the highest impact
of extreme condition events is expected.
Acknowledgements We thank A. P. Møller for his kindly
invitation to write this article and help in editing previous
versions. Two anonymous referees made interesting suggestions to improve the manuscript. Our work is currently funded
by Spanish Ministry of Science and Innovation through the
project CGL2009-09439.
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