Host-parasite interactions under extreme climatic conditions

6 downloads 2361 Views 159KB Size Report
ing the altered dynamics of host-parasite interactions due to an extreme change are ... edge on three principal factors in determining host-parasite associations; ...
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,

391

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.

392

Current Zoology

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

Vol. 57

No. 3

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,

393

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-

394

Current Zoology

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

Vol. 57

No. 3

(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

395

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-

396

Current Zoology

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-

Vol. 57

No. 3

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.

References Achinelly MF, Micieli MV, Garcia JJ, 2003. Pre-parasitic juveniles of Strelkovimermis spiculatus Poinar and Camino, 1986 (Nematoda: Mermithidae) predated upon by freshwater copepods (Crustacea: Copepoda). Nematology 5: 885–888. Adamo SA, 2004. How should behavioural ecologists interpret measurements of immunity? Anim. Behav. 68: 1443–1449. Alessa L, Chapin FS, 2008. Anthropogenic biomes: A key contribution to earth-system science. Trends Ecol. Evol. 23: 529–531.

Vol. 57

No. 3

Alessa L, Kliskey AA, Brown G, 2008. Social-ecological hotspots mapping: A spatial approach for identifying coupled socialecological space. Landsc. Urban Plan. 85: 27–39. Allan BF, Langerhans RB, Ryberg WA, Landesman WJ, Griffin NW et al., 2009. Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 155: 699–708. Allen JE, MacDonald AS, 1998. Profound suppression of cellular proliferation mediated by the secretions of nematodes. Parasite. Immunol. 20: 241–247. Ardia DR, Schat KA, Winkler DW, 2003. Reproductive effort reduces long-term immune function in breeding tree swallows Tachycineta bicolor. Proc. R. Soc. Lond. B–Biol. Sci. 270: 1679–1683. Atkinson CT, 2008. Avian malaria. In: Atkinson CT, Thomas NJ, Hunter B ed. Parasitic Diseases of Wild Birds. Iowa: Wiley-Blackwell, 35–53. Banerjee BD, 1999. The influence of various factors on immune toxicity assessment of pesticides chemicals. Toxicol. Lett. 107: 21–31. Bates AE, Stickle WS, Harley CDG, 2010. Impact of temperature on an emerging parasitic association between a sperm-feeding scuticociliate and Northeast Pacific sea stars. Journal of Experimental Marine Biology and Ecology 384: 44–50. Beauchamp KA, Kelley GO, Nehring RB, Hedrick RP, 2005. The severity of whirling disease among wild trout corresponds to differences in the genetic composition of Tubifex tubifex populations in central Colorado. J. Parasitol. 91: 53–60. Begon M, 2008. Effects of host diversity on disease dynamics. In: Ostfeld RS, Keesing F, Eviner VT ed. Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems. Princeton: Princeton University Press, 12–29. Berger S, Wikelski M, Romero LM, 2007. Behavioral and physiological adjustments to new predators in an endemic island species, the Galapagos marine iguana. Horm. Behav. 52: 653–663. Biek R, Real LA, 2010. The landscape genetics of infectious disease emergence and spread. Mol. Ecol. 19: 3515–3531. Bisdorff B, Wall R, Milnes A, 2006. Prevalence and regional distribution of scab, lice and blowfly strike in Great Britain. Vet. Rec. 158: 749–752. Boëté C, Paul REL, Koella JC, 2004. Direct and indirect immunosuppression by a malaria parasite in its mosquito vector. Proc. R. Soc. Lond. B 271: 1611–1615. Bordes F, Morand S, Krasnov BR, Poulin R, 2010. Parasite diversity and latitudinal gradients in terrestrial mammals. In: Morand S, Krasnov BR eds. The biogeography of Host-Parasite Interactions. Oxford: Oxford University Press, 89–98. Boulinier T, Danchin E, 1996. Effects of potential climatic changes on plant-parasitic nematodes. Asp. Appl. Biol. 45: 331–334. Bowden TJ, Thompson KD, Morgan AL, Gratacap RM, Nikoskelainen S, 2007. Seasonal variation and the immune response: A fish perspective. Fish Shellfish Immunol. 22: 695–706. Bravo de Guenni L, Cardoso M, Goldammer J, Hurtt G, Mata LJ et al., 2005. Regulation of natural hazards: Floods and fires. In: Millennium Ecosystem Assessment. ed. Ecosystem and Human well-being: Current State and Trends. Volume I. Cambridge: Cambridge University Press, 441–454.

MARTINEZ J, MERINO S: Parasitism and extreme climate

Brooks DR, Hoberg EP, 2007. How will global climate change affect parasite-host assemblanges? Trends Parasitol. 23: 571–574. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL et al, 2007. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS. Biol. 5: 1220–1227. Bush AO, Fernández JC, Esch GW, Seed RJ, 2001. Parasitism. The diversity and ecology of animal parasites. Cambridge: Cambridge University Press. Chandra RK, 1981. Immunocompetence as a functional index of nutritional status. Brit. Med. Bull. 37: 89–94. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT et al, 2008. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J. Infect. Dis. 197: 435–438. Chen WH, Sun LT, Tsai CL, Song YL, Chang CF, 2002. Coldstress induced the modulation of catecholamines, cortisol, immunoglobulin M, and leukocyte phagocytosis in tilapia. Gen. Comp. Endocrinol. 126: 90–100. Chisholm J, Smith V, 1994.Variation of antibacterial activity in the haemocytes of the shore crab Carcinus maenas with temperature. J. Marine Biol. Assoc. UK 74: 979–982. Christe P, Morand S, Michaux J, 2006. Biological conservation and parasitism. In: Morand S, Krasnov BR, Poulin R ed. Micromammals and Macroparasites: From Evolutionary Ecology to Management. Dusseldorf: Springer, 593–613. Christensen NØ, 1980. A review of the influence of host and parasites-related factors and environmental conditions on the host-finding capacity of the trematode miracidium. Acta Trop. 37: 303–318. Colborn T, Saal FSV, Soto AM, 1993. Developmental effects of endocrine-disrupting chemical in wildlife and humans. Environ. Health Persp. 101: 378–384. Combes C, 2001. Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago: University of Chicago Press. Cook T, Folli M, Klinck J, Ford S, Miller J, 1998. The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuarine, Coastal and Shelf Sci. 46: 587–597. Costanza R, d’Arge R, de Groot R, Farberk S, Grasso M et al., 1997. The value of the world´s ecosystems and natural capital. Nature 387: 253–260. Coteur G, Corriere N, Dubois P, 2004. Environmental factors influencing the immune responses of the common European starfish Asterias rubens. Fish Shellfish Immunol. 16: 51–63. Darwin C, 1859. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. 1st edn. London: Murray J. Dawson RD, Hillen KK, Whitworth TL, 2005. Effects of experimental variation in temperature on larval densities of parasitic Protocalliphora (Diptera: Calliphoridae) in nest of tree swallows (Passeriformes: Hirundinidae). Environ. Entomol. 34: 563–568. De La Rocque S, Rioux JA, Slingenbergh J, 2008. Climate change: Effects on animal disease systems and implications for surveillance and control. Rev. Sci. Tech. 27: 339–354. Demas GE, Nelson RJ, 1998. Photoperiod, ambient temperature, and food availability interact to affect reproductive and im-

401

mune function in adult male deer mice Peromyscus maniculatus. J. Biol. Rhythms 13: 253–262. Denver RJ, 2009. Structural and functional evolution of vertebrate neuroendocrine stress system. Trends Comp. Endocrin. Neurobiol. 1163: 1–16. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK et al., 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl. Acad. Sci. USA 105: 6668–6672. Dominguez M, Takemura A, Tsuchiya M, Nakamura S, 2004. Impact of different environmental factors on the circulating immunoglobulin levels in the Nile tilapia Oreochromis niloticus. Aquaculture 241:491–500. Drew ML, Samuel WM, 1986. Reproduction of the winter tick Dermacentor albipictus, under field conditions in Alberta, Canada. Can. J. Zool. 64: 714–721. Duffy DC, 1983. The ecology of tick parasitism on densely nesting Peruvian seabirds. Ecology 64: 110–119. Dunier M, Siwicki AK, 1993. Effects of pesticides and other organic pollutants in the aquatic environment on immunity of fish: A review. Fish Shellfish Immunol. 3: 423–438. Dunn RR, Davies TJ, Harris NC, Gavin MC, 2010. Global drivers of human pathogen richness and prevalence. Proc. R. Soc. Lond. B 277: 2587–2595. Ellis EC, Ramankutty N, 2008. Putting people on the map: Anthropogenic biomes of the world. Front. Ecol. Environ. 6: 439–447. Epstein JH, Field HE, Luby S, Pulliam JRC, Daszak P, 2006. Hipah virus: Impact, origins, and causes of emergence. Curr. Infect. Dis. Rep. 8: 59–65. Estrada-Peña A, Martínez Avilés M, Muñoz Reoyo MJ, 2011. A population model to describe the distribution and seasonal dynamics of the tick Hyalomma marginatum in the Mediterranean Basin. Transbound Emerg. Dis. doi: 10.1111/j. 1865– 1682.2010.01198.x. Ewald PW, 1994. Evolution of Infectious Diseases. Oxford: Oxford University Press. Forsythe P, Bienenstock J, 2010. Immunomodulation by commensal and probiotic bacteria. Immunol. Invest. 39: 429–48. Frank SA, 1996. Models of Parasite virulence. Quart. Rev. Biol. 71: 37–78. Frebel H, Richter K, Oxenius A, 2010. How chronic viral infections impact on antigen-specific T-cell responses. Eur. J. Immunol. 40: 654–63. Freire MG, Schweigmann N, 2009. Effect of temperature on the flight activity of culicids in Buenos Aires City, Argentina. J. Nat. Hist. 43: 2167–2177. French SS, Moore MC, Demas GE, 2009. Ecological immunology: the organism in context. Integr. Comp. Biol. 49: 246–253. Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G, 2009. Climate and Dirofilaria infection in Europe. Vet. Parasitol. 163: 286–292. Gething PW, Smith DL, Patil AP, Tatem AJ, Snow RW et al., 2010. Climate change and the global malarial recession. Nature 465: 342–346. Gill CA, 1938. The Seasonal Periodicity of Malaria and the Mechanism of the Epidemic Wave. London: J&A Churchill. Glines MV, Samuel WM, 1989. Effect of Dermacentor albipictus

402

Current Zoology

(Acari: Ixodidae) on blood composition, weight gain and hair coat of moose Alces alces. Exp. Appl. Acarol. 6:197–213. Goodenough AE, 2010. Are the ecological impacts of alien species misrepresented? A review of the “native good, alien bad” philosophy. Comm. Ecol. 11: 13–21. Gourbeyre P, Denery S, Bodinier M, 2011. Probiotics, prebiotics, and synbiotics: Impact on the gut immune system and allergic reactions. J. Leukoc. Biol. doi: 10.1189/jlb.1109753. Grossman CJ, 1984. Regulation of the immune-system by sex steroids. Endocrine Rev. 5: 435–455. Guérnier V, Hochberg ME, Guégan JFO, 2004. Ecology drives the worldwide distribution of human diseases. PLoS Biol. 2: 740–746. Hanson D, 1997. Fever, temperature, and the immune response. Ann. N. Y. Acad. Sci. 813: 453–464. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR et al., 2009. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 3: 818–824. Harrus S, Baneth G, 2005. Drivers for the emergence and re-emergence of vector-borne protozoal and bacterial diseases. Int. J. Parasitol. 35: 1309–1318. Harvell D, Jordán-Dahlgren E, Merkel S, Rosenberg E, Raymundo L et al., 2007. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20: 172–195. Hayes TB, Case P, Chui S, Chung D, Haeffele C et al., 2006. Pesticide mixtures, endocrine disruption, and amphibian declines: Are we underestimating the impact? Environ. Health Persp. 114: 40–50. Hayes TB, Falso P, Gallipeau S, Stice M, 2010. The cause of global amphibian declines: A development endocrinologist´s perspective. J. Exp. Biol. 213: 921–933. Hillebrand H, 2004. On the generality of the latitudinal diversity gradient. Am. Nat. 163: 192–211. Hoberg EP, 2010. Invasive processes, mosaics and the structure of helminth parasite faunas. Rev. Sci.Tech.-Off. Int. Epiz. 29: 255–272. Holmes JC, 1996. Parasites as threats to biodiversity in shrinking ecosystems. Biod. Cons. 5: 975–983. Holzman C, Leventhal JM, Qiu H, Jones NM, Wang J et al., 2001. Factors linked to bacterial vaginosis in nonpregnant women. Am. J. Public Health 91: 1664–1670. Hopkins WA, Rowe CL, Congdon JD, 1999. Elevated trace element concentrations and standard metabolic rate in banded water snakes Nerodia fasciata exposed to coal combustion wastes. Environ. Toxicol. Chem. 18: 1258–1263. Hudson PJ, 1986. The effect of a parasitic nematode on the breeding production of red grouse. J. Anim. Ecol 55: 85–94. Hudson PJ, Dobson AP, Newborn D, 1998. Prevention of population cycles by parasite removal. Science 282: 2256–2258. Hudson PJ, Newborn D, Dobson AP, 1992. Regulation and stability of a free-living host-parasite system Trichostrongylus tenuis in red grouse. I. Monitirung and parasite reduction experiments. J. Anim. Ecol 61: 477–486. Hunter PR, 2003. Climate change and waterborne and vectorborne disease. J. Appl. Microbiol. 94: 37S–46S. Isolauri E, Sütas Y, Kankaanpää P, Arvilommi H, Salminen S, 2001. Probiotics: Effects on immunity. Am. J. Clin. Nutr. 73:

Vol. 57

No. 3

444S–450S. Jansen E, Overpeck J, Briffa KR, Duplessy J-C, Joos F et al., 2007. Palaeoclimate. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M et al. ed. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, 433–497. Johnson PTJ, Hartson RB, Larson DJ, Sutherland DR, 2008. Diversity and disease: Community structure drives parasite transmission and host fitness. Ecol. Lett. 11: 1017–1026. Johnson PTJ, Lund P, Hartson RB, Yoshino T, 2009. Community diversity reduces Schistosoma mansoni transmission, host pathology, and human infection risk. Proc. R. Soc. Lond. B 276: 1657–1663. Johnson PTJ, Thieltges DW, 2010. Diversity, decoys and the dilution effect: How ecological communities affect disease risk. J. Exp. Biol. 213: 961–970. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D et al., 2008. Global trends in emerging infectious diseases. Nature 451: 990–994. Kagami M, Van Donk E, de Bruin A, Rijkeboer M, ibelings BW, 2004. Daphnia can protect diatoms from fungal parasitism. Limnol. Oceanogr. 49: 680–685. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD et al., 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468: 647–652. Keesing F, Brunner J, Duerr S, Killilea M, LoGiudice K et al., 2009. Hosts as ecological traps for the vector of Lyme disease. Proc. R. Soc. Lond. B 276: 3911–3919. Keesing F, Holt RD, Ostfeld RS, 2006. Effects of species diversity on disease risk. Ecol. Lett. 9: 485–498. Kelly P, 2010. Nutrition, intestinal defence and the microbiome. Proc. Nutr. Soc. 69: 261–268. Kleinschmidt I, Sharp B, Benavente LE, Schwabe C, Torrez M et al., 2006. Reduction in infection with Plasmodium falciparum one year after the introduction of malarial control interventions on Bioko Island, Equatorial Guinea. Am. J. Trop. Med. Hyg. 74: 972–978. Knapp SE, Baldwin NL, Presindente PJ, 1972. Experimental transmission of an isolate of Nosema strigeoideae Hussey 1971 to Fasciola hepática. J. Parasitol. 58: 1206–1207. Kosoy MY, Regnery RL, Tzianabos T, Marston EL, Jones DC et al., 1997. Distribution, diversity, and host specificity of Bartonella in rodents from the Southeastern United States. Am. J. Trop. Med. Hyg. 57: 578–588. Krakau M, Thieltges DW, Reise K, 2006. Native parasites adopt introduced bivalves of the North Sea. Biol. Invasions 8: 919–925. Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA, 2004. Flea species richness and parameters of host body, host geography and host ‘milieu’. J. Anim. Ecol. 73: 1121–1128. Ksiazek A, Konarzewski M, Chadziska M, Cicho M, 2003. Costs of immune response in cold-stressed laboratory mice selected for high and low basal metabolism rates. Proc. Biol. Sci. 270: 2025–2031. Kutz SJ, Hoberg EP, Nishi J, Polley L, 2002. Development of the muskox lungworm Umingmakstrongylus pallikuukensis (Protostrongylidae) in gastropods in the Arctic. Can. J. Zool. 80:

MARTINEZ J, MERINO S: Parasitism and extreme climate

1977–1985. Kutz SJ, Hoberg EP, Polley L, Jenkins EJ, 2005. Global warming is changing the dynamics of arctic host-parasite systems. Proc. R. Soc. Lond. B 272: 2571–2576. Kutz SJ, Jenkins EJ, Veitch AM, Ducrocq J, Polley L et al., 2009. The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host-parasite interactions. Vet. Parasitol. 163: 217–228. Laaksonen S, Solismaa M, Kortet R, Kuusela J, Oksanen A, 2009. Vectors and transmission dynamics for Setaria tundra (Filaroidea; Onchocercidae), a parasite of reindeer in Finland. Parasites & Vectors, doi: 10.1186/1756–3305–2–3. Lam SH, Sin YM, Gong Z, Lam TJ, 2005. Effects of thyroid hormone on the development of immune system in zebrafish. Gen. Comp. Endocrinol. 142: 325–335. Lawley TD, Clare S, Walker AW, Goulding D, Stabler RA et al., 2009. Antibiotic treatment of clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect. Immun. 77: 3661–3669. Lee KA, Wikelski M, Robinson WD, Robinson TR, Klasing KC, 2008. Constitutive immune defenses correlate with life-history variables in tropical birds. J. Anim. Ecol. 77: 356–363. Leiro J, Santamarina MT, Sernfindez L, Sanmartin ML, Ubeira FM, 1988. Immunomodulation by Trichinella spiralis: Primary versus secondary response to phosphorylcholine-containing antigens. Med. Microbiol. Immunol. 177: 161–167. Liang S, Seto E, Remais J, Zhong B, Yang C et al., 2007. Environmental effects on transmission and control of parasitic diseases exemplified by schistosomiasis in Western China. Proc. Natl. Acad. Sci. USA 104: 7110–7115. Lindenfors P, Nunn CL, Jones KE, Cunningham AA, Sechrest W et al., 2007. Parasite species richness in carnivores: Effects of host body mass, latitude, geographical range and population density. Global Ecol. Biogeogr. DOI: 10.1111/j.1466– 8238.2006.00301.x. Loetti V, Burroni N, Prunella P, Schweigmann N, 2008. Effect of temperature on the development time and survival of preimaginal Culex hepperi (Diptera: Culicidae). Rev. Soc. Entomol. Argentina 67: 79–85. LoGiudice K, Duerr ST, Newhouse MJ, Schmidt KA, Killilea ME et al., 2008. Impact of host community composition on Lyme disease risk. Ecology 89: 2841–2849. Lovejoy T, 2008. Climate change and biodiversity. Rev. Sci. Tech. -Off. Int. Épizoot. 27: 331–338. Macpherson CNL, 2005. Human behaviour and the epidemiology of parasitic zoonoses. Int. J. Parasitol. 35: 1319–1331. Maizels RM, 2009. Parasite immunomodulation and polymorphisms of the immune system. J. Biol. 8: 62. Maizels RM, Bundy DA, Selkirk ME, Smith DF, Anderson RM, 1993. Immunological modulation and evasion by helminth parasites in human populations. Nature 365: 797–805. Maizels RM, Pearce EJ, Artis D, Yazdanbakhsh M, Wynn TA, 2009. Regulation of pathogenesis and immunity in helminth infections. J. Exp. Med. 206: 2059–2066. Maniero GD, Carey C, 1997. Changes in selected aspects of immune function in the leopard frog Rana pipiens associatedwith exposure to cold. J. Comp. Physiol. B. Biochem. Syst. Envi-

403

ron. Physiol. 167: 256–263. Marcogliese DJ, 2008. The impact of climate change on the parasites and infectious diseases of aquatic animals. Rev. Sci. Tech. Off. Int. Epiz 27: 467–484. Martin LB, Hasselquist D, Wikelski M, 2006. Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147: 565–575. Martin LB, Hopkins WA, Mydlarz LD, Rohr JR, 2010. The effects of anthropogenic global changes on immune functions and disease resistance. Ann. New York Acad. Sci. 1195: 129–148. Martin LB, Navara KJ, Weil ZM, Nelson RJ, 2007a. Immunological memory is compromised by food restriction in deer mice Peromyscus maniculatus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292: R316–R320. Martin LB, Scheuerlein A, Wikelski M, 2003. Immune activity elevates energy expenditure of house sparrows: A link between direct and indirect costs? Proc. R. Soc. Lond. B. Biol. Sci. 270: 153–158. Martin LB, Weil ZM, Nelson RJ, 2007b. Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88: 2516–2528. Martínez J, Merino S, Rodríguez-Caabeiro F, 2004. Physiological responses to Trichinella spiralis infection in Wistar rats: Is immune response costly? Helminthologia 41: 67–71. Martínez-de la Puente J, Merino S, Lobato E, Rivero-de-Aguilar J, del Cerro S et al., 2009. Does weather affect biting fly abundance in avian nest? J. Avian Biol. 40: 653–657. Martínez-de la Puente J, Merino S, Lobato E, Rivero-de-Aguilar J, del Cerro S et al., 2010. Nest-climatic factors affect the abundance of biting flies and their effects on nestling condition. Acta Oecol. 36: 543–547. Mas-Coma S, Bargues MD, Gracenea M, Montoliu I, 1987. Las estrategias etoecologicas generales y especificas en el ciclo biologico de los Digenidos Brachylaimidae Joyeux et Foley, 1930 (Trematoda:Brachylaimoidea) y el concepto de seleccion r/K. In: Sans-Coma V, Mas-Coma S, Gosálbez J ed. Mamiferos y Helmintos. Volumen Homenaje al Prof. Dr. Herman Kahmann en su 81 Aniversario. Barcelona: Ketres Editora S.A., 253–317. Mas-Coma S, Valero MA, Bargues MD, 2008. Effects of climate change on animal and zoonotic helminthiases. Rev. Sci. Tech. 27: 443–457. Maszle DR, Whitehead PG, Johnson RC, Spear RC, 1998. Hydrological studies of schistosomiasis transport in Sichuan Province, China. Sci. Total Environ. 216: 193–203. Mayhew, P. 2006. Discovering Evolutionary Ecology: Bringing together ecology and evolution. Oxford: Oxford University Press. McClanahan TR, Weil E, Maina J, 2009. Strong relationship between coral bleaching and growth anomalies in massive Porites. Glob. Change Biol. 15: 1804–1816. McKenzie VJ, Townsend AR, 2007. Parasitic and infectious diseases responses to changing global nutrient cycles. EcoHealth 4: 384–396. McMichael AJ, Woodruff RE, Hales S, 2006. Climate change and human health: present and future risks. Lancet 367: 859–869. Meerburg BG, Kijlstra A, 2009. Changing climate-changing pathogens: Toxoplasma gondii in North-Western Europe. Para-

404

Current Zoology

sitol. Res. 105: 17–24. Merino S, 2010. Immunocompetence and parasitism in nestlings from wild populations. Open Ornithol. J. 3: 27–32. Merino S, Møller AP, 2010. Host-parasite interactions and climate change. In: Møller AP, Fiedler W, Berthold P ed. Effects of Climate Change on Birds. Oxford University Press, 213–226. Merino S, Moreno J, Vásquez RA, Martínez J, SánchezMonsálvez I et al., 2008. Haematozoa in forest birds from southern Chile: Latitudinal gradients in prevalence and parasite lineage richness. Austral Ecol. 33: 329–340. Merino S, Potti J, 1996. Weather dependent effects of ectoparasites on their bird host. Ecography 19: 107–113. Millennium Ecosystem Assessment, 2005. Ecosystems and Human Well-Being: Current Status and Trends. Cambridge: Cambridge University Press. Møller AP, 2010. Host-parasites interactions and vectors in the barn swallow in relation to climate change. Glob. Change Biol. 16: 1158–1170. Møller AP, Arriero E, Lobato E, Merino S, 2009. A meta-analysis of parasite virulence in nestling birds. Biol. Rev. 84: 567–588. Møller AP, Martín-Vivaldi M, Merino S, Soler JJ, 2006. Densitydependent and geographical variation in bird immune response. Oikos 115: 463–474. Morgan ER, Wall R, 2009. Climate change and parasitic disease: Farmer mitigation? Trends Parasitol. 25: 308–313. Nayak SK, 2010. Probiotics and immunity: A fish perspective. Fish Shellfish Immunol. 29: 2–14. Ndong D, Chen YY, Lin YH, Vaseeharan B, Chen JC, 2007. The immune response of tilapia Oreochromis mossambicus and its susceptibility to Streptococcus iniae under stress in low and high temperatures. Fish Shellfish Immunol. 22: 686–694. NRC, 2002. National Research Council-Committee on Abrupt Climate Change. Abrupt Climate Change: Inevitable Surprises. Washington, D.C., USA: National Academies Press. Nunn CL, Altizer SM, Sechrest W, Cunningham AA, 2005. Latitudinal gradients of parasite species richness in primates. Div. Dist. 11: 249–256. Nussenzweig RS, 1982. Parasitic disease as a cause of immunosuppression. N. Engl. J. Med. 306: 423–424. O'Connor LJ, Walkden-Brown SW, Kahn LP, 2006. Ecology of the free-living stages of major trichostrongylid parasites of sheep. Vet. Parasitol. 142: 1–15. Omenn GS, 2010. Evolution and public health. Proc. Natl. Acad. Sci. USA 107: 1702–1709. Ostfeld RS, Keesing F, Eviner VT, 2008. Infectious Disease Ecology: Effects of Ecosystems on Disease and of Diseases on Ecosystems. Princeton, NJ: Princeton University Press. Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Hõrak P, 2001. Immune challenge affects basal metabolic activity in wintering great tits. Proc. R. Soc. Lond. B. Biol. Sci. 268: 1175–1181. Paillard C, Allam B, Oubella R, 2004. Effect of temperature on defense parameters in Manila clam Ruditapes philippinarum challenged with Vibrio tapetis. Dis. Aquat. Org. 59: 249–262. Pech D, Aguirre-Macedo ML, Lewis JW, Vidal-Martinez VM, 2010. Rainfall induces time-lagged changes in the proportion of tropical aquatic hosts infected with metazoan parasites. Int. J. Parasitol. 40: 937–944.

Vol. 57

No. 3

Pellegrino J, de Maria M, de Moura MF, 1966. Observations on the predatory activity of Lebistes reticulatus (Peters, 1959) on cercariae of Schistosoma mansoni. Am. J. Trop. Med. Hyg 15: 337–342. Poulin R, 1995. Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecol. Monogr. 65: 283–302. Poulin R, 1998. Evolutionary Ecology of Parasites. London: Chapman and Hall. Poulin R, 2006. Global warming and temperature-mediated increased in cercarial emergence in trematode parasites. Parasitology 132: 143–151. Prinz K, Kelly TC, O´Riordan RM, Culloty SC, 2009. Non-host organisms affect transmission processes in two common trematode parasites of rocky shores. Mar. Biol. 156: 2303–2311. Råberg L, Grahn M, Hasselquist D, Svensson E, 1998. On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. B 265: 1637–1641. Råberg L, Nilsson J-A, Ilmonen P, Stjernman M, Hasselquist D, 2000. The cost of an immune response: Vaccination reduces parental effort. Ecol. Lett. 3: 382–386. Remais J, Liang S, Spear R, 2007. Coupling hydrologic and infectious disease models to explain regional differences in schistosomiasis transmission in southwestern China. Environ. Sci. & Tech. 42: 2643–2649. Robar N, Burness G, Murray DL, 2010. Tropics, trophics and taxonomy: The determinants of parasite-associated host mortality. Oikos 119: 1273–1280. Rogers DJ, Randolph SE, 2006. Climate change and vector-borne diseases. Adv. Parasitol. 62: 345–81. Rohde K, 1992. Latitudinal gradients in species diversity: The search for the primary cause. Oikos 65: 514–527. Roos K, Håkansson EG, Holm S, 2001. Effect of recolonisation with ‘‘interfering’’ a streptococci on recurrences of acute and secretory otitis media in children: Randomised placebo controlled trial. Br. Med. J. 322: 1–4. Rowe CL, Hopkins WA, Zehnder C, Congdon JD, 2001. Metabolic costs incurred by crayfish Procambarus acutus in a trace element-polluted habitat: Further evidence of similar responses among diverse taxonomic groups. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 129: 275–283. Samuel WM, 1989. Locations of moose in northwestern Canada with hair loss probably caused by the winter tick Dermacentor albipictus (Acari: Ixodidae). J. Wildl. Dis. 25: 436–439. Santos JL, 1994. Nutrition, infection, and immunocompetence. Infect. Dis. Clin. North. Am. 8: 243–267. Semenza JC, Menne B, 2009. Climate change and infectious diseases in Europe. Lancet Infect. Dis. 9: 365–375. Senior K, 2008. Climate change and infectious disease: A dangerous liaison? Lancet Infect. Dis. 8: 92–93. Shaman J, Day JF, 2007. Reproductive phase locking of mosquito populations in response to rainfall frequency. PLoS ONE 2: e331. doi:10.1371/journal.pone.0000331 Sharp BL, Kleinschmidt I, Streat E, Maharaj R, Barnes KI et al., 2007. Seven years of regional malarial control collaboration: Mozambique, South Africa and Swaziland. Am. J. Trop. Med. Hyg. 76: 42–47. Sheldon BC, Verhulst S, 1996. Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology.

MARTINEZ J, MERINO S: Parasitism and extreme climate

Trends Ecol. Evol. 11: 317–321. Shephard R, Shek P, 1998. Cold exposure and immune function. Can. J. Physiol. Pharmacol. 76: 828–836. Sinclair J, Lochmiller R, 2000. The winter immunoenhancement hypothesis: Associations among immunity, density, and survival in prairie vole Microtus ochrogaster populations. Can. J. Zool. 78: 254–264. Stempin CC, Dulgerian LR, Garrido VV, Cerban FM, 2010. Arginase in Parasitic Infections: Macrophage Activation, Immunosuppression, and Intracellular Signals. J. Biomed. Biotech., doi:10.1155/2010/683485 Sternberg EM, 2006. Neural regulation of innate immunity: A coordinated nonspecific host response to pathogens. Nat. Rev. Immunol. 6: 318–328. Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK et al., 2009. Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3: 512–521. Suzán G, Marcé E, Giermakowski JT, Mills JN, Ceballos G et al., 2009. Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS ONE 4, e5461. Szteina MB, Kierszenbaumb F, 1993. Mechanisms of development of immunosuppression during Trypanosoma infections. Trends Parasitol. 9: 424–428. Tanser FC, Sharp B, Le Sueur D, 2003. Potential effect of climate change on malaria transmission in Africa. Lancet 362: 1792–1798. Taylor LH, Latham SM, Woolhouse MEJ, 2001. Risk factors for human disease emergence. Proc. R. Soc. Ser. B 356, 983–989. Teklehaimanot HD, Teklehaimanot A, Kiszewski A, Rampao HS, Sachs JD, 2009. Malaria in Sao Tome and Principe: On the brink of elimination after three years of effective antimalarial measures. Am. J. Trop. Med. Hyg. 80: 133–140. Thieltges DW, Bordalo MD, Hernandez AC, Prinz K, Jensen KT, 2008. Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135: 1111–1116. Tompkins DM, Gleeson DM, 2006. Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand. J. R. Soc. New Zealand 36: 51–62. Tong SL, Hu WB, 2001. Climate variation and incidence of Ross River virus in Cairns, Australia: A time-series analysis. Env Health Perspec. 109: 1271–1273. Travers MA, Le Goïc N, Huchette S, Koken M, Paillard C, 2008. Summer immune depression associated with increased susceptibility of the European abalone Haliotis tuberculata to Vibrio harveyi infection. Fish Shellfish Immunol. 25: 800–808. Trebichavsky I, Splichal I, Rada V, Splichalova A, 2010. Modulation of natural immunity in the gut by Escherichia coli strain Nissle 1917. Nutr. Rev. 68: 459–64.

405

Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R et al., 2007. The human microbiome project. Nature 449: 804–810. Upatham ES, Sturrock RF, 1973. Field investigations on the effect of other aquatic animals on the infection of Biomphalaria glabrata by Schistosoma mansoni miracidia. J. Parasitol. 59: 448–453. van Dijk J, David GP, Baird G, Morgan ER, 2008. Back to the future: Developing hypotheses on the effects of climate change on ovine parasitic gastroenteritis from historical data. Vet. Parasitol. 158: 73–84. Van Lieshout M, Kovats RS, Livermore MT, Martens P, 2004. Climate change and malaria: analysis of the SRES climate and socio-economic scenarios. Glob. Environ. Change 14: 87–99. Van Riper C III, van Riper SG, Goff ML, Laird M, 1986. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol. Mon. 56: 327–344. Vargas-Albores F, Hinojosa-Baltazar P, Portillo-Clark G, Magallon-Baraja F, 1998. Influence of temperature and salinity on the yellowleg shrimp Penaeus californiensis Holmes prophenoloxidase system. Aquacult. Res. 29: 549–553. Voccia I, Blakley B, Brousseau P, Fournier M, 1999. Immunotoxicity of pesticides: A review. Toxicol. Ind. Health 15: 119–132. Wang FY, Yang HS, Gao F, Liu GB, 2008. Effects of acute temperature or salinity stress on the immune response in sea cucumber Apostichopus japonicas. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 151: 491–498. Warner RE, 1968. The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70: 101–120. Wegbreit J, Reisen WK, 2000. Relationships among weather, mosquito abundance and encephalitis virus activity in California: Kern County 1990–98. J. Am. Mosq. Control Assoc. 16: 22–27. Wegner KM, Kalbe M, Milinski M, Reusch TBH, 2008. Mortality selection during the 2003 European heat wave in three-spined sticklebacks: Effects of parasites and MHC genotype. BMC Evol. Biol. 8: 1–12. Woolhouse MEJ, Gowtage-Sequeria S, 2005. Host range and emerging and reemerging pathogens. Emerg. Infect. Dis. 11: 1842–1847. Zahraa H, 2008. Effects of commutative heat stress on immunoresponses in broiler chickens reared in closed system. Int. J. Poultry Sci. 7: 964–968. Zhou G, Minakawa N, Githeko AK, Yan GY, 2004. Association between climate variability and malaria epidemics in the East African highlands. Proc. Natl. Acad. USA 101: 2375–238. Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW et al., 2005. The public health significance and control of schistosomiasis in China: Then and now. Acta Trop. 96: 97–105.