Current Zoology 57 (3): 390−405, 2011

Host-parasite interactions under extreme climatic conditions

J. MARTINEZ1*, S. MERINO2

1 Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Alcalá, Alcalá de Henares, Madrid, Spain 2 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 or- ganisms. 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 determin- ing 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 fre- quency of intraspecific contact. What are the consequences for host-parasite interactions? Here we summarize the present knowl- edge 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 decline and even extinction. Extreme environmental the influences that other celestial bodies exert on it have changes (i.e. unusual events that are at the extremes of greatly been shaping the structure and physical- the historical distribution for a given area) are usually chemical characteristics of Earth in a way that allow it faster and of shorter duration than less extreme changes to sustain life. Since the very beginning living beings and thus the possibilities of organisms to adapt to these have acted as another factor in the dynamics of the events are in many cases dependent on the magnitude of Earth, creating new opportunities for some organisms to the change and the duration of its effects (NRC, 2002). evolve, but simultaneously eliminating the stability of Of course the final impact of a change will depend on conditions for others (e.g., Mayhew, 2006 and refe- the physiological tolerance of affected individuals, and rences therein). This lack of stasis has been a feature in this respect, eurytopic organisms, tolerant of highly since the origin of the Earth (Jansen et al., 2007). diverse conditions, are more likely to adapt to new en- Therefore, the generation or destruction of ecological vironmental conditions, although these changes affect in niches or enlargement or reduction of existing niches is different degrees all organisms and, therefore, intra- and a constant in the dynamics of our planet (Millennium interspecific ecological interactions. Ecosystem Assessment, 2005). Biotic and abiotic envi- In the case of parasitic interactions where there exists ronmental changes along with individual genetic vari- a tight dependency of the parasites on their hosts, the ability of living beings are the engine for evolution by effect of an environmental change can affect asymme- natural selection and, therefore, are responsible for ac- trically both members of the association. Thus, the sur- tual biodiversity at each geological time (Darwin, vival of parasites from environmental change will be 1859). determined by several factors such as host dependence These environmental changes are a wonderful possi- and parasitic specificity, the complexity of the life cycle, bility for geographic expansion and diversification of the biodiversity of the environment, the density and some organisms, but for others denote the start of its mobility of their hosts and the physiological tolerance of

Received Feb 01, 2011; accepted Mar. 06, 2010. ∗ Corresponding author. E-mail: [email protected] © 2011 Current Zoology MARTINEZ J, MERINO S: Parasitism and extreme climate 391 individuals (resistance to both internal and external en- including drastic reduction of host populations and even vironments). For example, specific parasitic interactions extinction (see for example Warner, 1968; Van Riper et will be much more susceptible to a drastic reduction in al., 1986; Christe et al., 2006). However, such invasions hosts density caused by an environmental change that can be beneficial for the endemic fauna in some circum- will hinder transmission to a new host as compared to stances producing a dilution effect. In other words, generalist parasitic interactions. This reduction in host parasites are “diluted” among more species of hosts not density could be extremely deleterious if organisms are all of them being competent for the parasite to complete obligate parasites (Poulin, 1998). However, parasites its life cycle (Begon, 2008). could even in this scenario survive under a certain The number of potential scenarios to take into ac- threshold of host density if they have sufficient phe- count after an abrupt environmental change is enormous notypic plasticity to adjust their level of virulence that due to the large number of variables that affect the dif- is, by increasing the time of permanence in the host ferent parasite systems in a given ecosystem. However, (Ewald, 1994). On the other hand, those parasites with the more interesting effects of these changes are on pub- life cycles presenting free-living stages and especially lic and veterinary health due to their social and eco- those without forms of resistance will also be more nomic costs (see also NRC, 2002). Thus, the most susceptible to direct environmental changes (Bush et feared harmful effects of such changes are relapses al., 2001; De La Rocque et al., 2008; Mas-Coma et al., and/or expansion of certain parasitic diseases that could 2008). In addition, we can expect that complex bio- affect large human populations or agriculture logical cycles are more susceptible to irreversibly (Macpherson, 2005; Brooks and Hoberg, 2007; Morgan changes than in the case of direct cycles simply be- and Wall, 2009). However, the deleterious effects of cause the latter have shorter generation time and faster such changes on wildlife and ecosystems may have population growth (Mas-Coma et al., 1987; Taylor et consequences for conservation (Christe et al., 2006; al., 2001), and in complex cycles there are more possi- Ostfeld et al., 2008). bilities that one of its phases or one of the hosts is af- In this paper we synthesize relevant information on fected by extreme environmental changes (Combes, the determinants of parasite-host interactions affected 2001). Moreover, due to the reduced or absent motility by extreme conditions. Due to the scarcity of studies on of many parasites, the possibility of escape from a the effects of extreme climate changes on host-parasite hostile environment shall be determined mainly by interactions, and the fact that the same factors are im- their host mobility. However, the extent or change in plied in responses to environmental changes of different the geographical distribution of the hosts can open new degree, we explore these factors having in mind that associations for both parasites that are transported by such changes are of great magnitude and short duration. hosts to a new area and for parasites that are present in We specifically explore the following three aspects of newly occupied areas (Tompkins and Gleason, 2006; extreme changes on parasite-host associations (Fig. 1): Hoberg, 2010; Biek and Real, 2010). (i) the possibility that environmental changes impact In addition, environmental changes can have an ad- three main aspects that can affect the equilibrium of verse effect on availability of resources necessary for parasite-host relationships; biodiversity, population den- hosts to maintain an adequate nutritional status. In this sity and immunocompetence, (ii) the difficulty of pre- case individuals that do not have the ability to move dicting effects of particular environmental change on away from the focus of stress or find a way to exploit parasite-host interactions because of dependence on other resources will see their health seriously compro- intrinsic characteristics of each parasitic interaction, but mised (Chandra, 1981; Merino and Møller, 2010), and also on all ecological interactions maintained in the their immunocompetence could be reduced thereby fa- ecosystem by the parasitic relationship; and (iii) the cilitating settlement and reproduction of parasites (San- potential effect of socioeconomic advance of developing tos, 1994; Christe et al., 2006; Merino, 2010). But not countries along with the implementation of control pro- only hosts present in the focus of change can be affected grammes in the reduction of impact of global diseases. negatively. As previously mentioned, displacement of We have included examples of the effects of anthropo- hosts to new areas may lead to the introduction of para- genic changes on parasitic systems because such effects sites without a previous coevolutionary history with are analogous to those exerted by extreme climatic native hosts (Goodenough, 2010). The consequences for change, although in general such effects tend to be per- such new host-parasite associations are unsuspected, manent rather than reversible. 392 Current Zoology 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 bio- diversity by reducing the number of no-competent hosts for the parasite. In contrast, if the decrease in the num- ber of competent hosts occurs transmission of the dis- ease 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 de- pending 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 in- crease in the transmission of the pathogen (for example Lyme disease and hantavirus in rodents or West Nile Fig. 1 Schematic representation of the mechanisms af- virus in birds; Kosoy et al., 1997; Allan et al., 2009; fecting host-parasite interactions following an extreme Suzán et al., 2009). One of the best examples of the re- environmental alteration lationship between disease transmission and biodiver- sity is offered by the spread of Lyme disease in north- 1 Biodiversity east USA (LoGiudice et al., 2008; Keesing et al., 2009). This bacterial disease is caused by a species of the ge- Ecosystems with a high biodiversity favour the exis- nus Borrelia and is transmitted to mammal hosts by tence of many interspecific relationships that could ticks. The main reservoir of the disease in the area is show high buffering capacity to environmental pertur- white-footed mice Peromyscus leucopus. However, the bations (Bravo de Guenni et al., 2005). However, under presence of Virginia possum Didelphis virginiana abrupt environmental change ecological interactions clearly determines the incidence of the diseases in hu- may suffer fast and profound alterations. With respect to man populations. The marsupial species acts as subop- the parasite-host systems, the first sign of imbalance is timal hosts of ticks because they are able to eliminate fluctuation in the incidence of disease further deepening most ticks attached to their bodies. In areas where the the initial imbalance. For example, there is evidence of density of marsupials is high the transmission of Lyme a clear relationship between biodiversity decline and disease is low because the density of ticks is also low. increase in transmission of certain diseases (Keesing et However, in areas with low biodiversity due to envi- al., 2010). The dilution effect hypothesis suggests the ronmental degradation the presence of the marsupial is existence of several biological mechanisms in complex reduced thus increasing the population of mice that are communities acting to reduce the risk of transmission of not efficient at avoiding tick infestations. As a conse- diseases (Keesing et al., 2006). Several of these mecha- quence density of ticks is higher and therefore the nisms have been characterized in parasitic systems, no- transmission of the disease. It is possible that the same tably including the existence of decoy and suboptimal characteristics that allow some hosts to resist environ- hosts, predation, hyper-parasitism, physical interference, mental change that provoke a reduction in biodiversity and toxic-production (Johnson and Thieltges, 2010). We can also increase susceptibility of these hosts to infec- briefly explain these mechanisms. tion (Keesing et al., 2010). In this respect it is important Decoy hosts are species that are not part of the life to note that species with a high reproductive and devel- cycle of the pathogen. The presence of such hosts in- opmental rate are more resistant to environmental creases the possibility that parasites encounter them change, but in addition they also have lower levels of without being able to complete the life cycle and there- adaptive immunity (Martin et al., 2006, 2007a; Lee et fore reducing the number of contacts with specific hosts al., 2008). MARTINEZ J, MERINO S: Parasitism and extreme climate 393

The dilution effect provoked by the presence of in- and also of definitive hosts (Pellegrino et al., 1966). competent hosts or hosts with low competence has been Cases of predation decreasing parasite transmission also characterized in diseases with complex life cycles. have been described for other systems (Thieltges et al., For example, transmission of the trematode Schistosoma 2008; Johnson et al., 2010) including some implying mansoni depends on the presence of appropriate fresh- species of protozoa (Beauchamp et al., 2005) and fungi water snails acting as intermediate hosts of miradicida, a (Kagami et al., 2004). In contrast hyperparasitism can free living parasite life stage emerging from eggs. An diminish transmission success of some diseases, as is experiment using competent and incompetent snails the case of trematode species susceptible to infection by showed that transmission of the parasite is clearly re- microsporidia (Knapp et al., 1972). In addition, in com- duced as compared with the transmission when only plex systems the density of organisms in the area can competent snails are present. The result is a lower pro- interfere with transmission of diseases simply by direct duction of cercariae, the parasitic infective stage for physical avoidance of movements of aquatic free-living humans, in the snails, and, therefore, a lower risk of forms of parasites (Prinz et al., 2009) or by the produc- transmission of the disease (Johnson et al., 2009). A tion and liberation of toxic substances in the environ- similar case has been reported for a trematode of the ment that affects parasites (Christensen, 1980). genus Ribeiroia. This parasite uses snails as first inter- Although the dilution effect in complex systems can mediate hosts, several species of amphibians as second be expected due to higher number of species present intermediate hosts and different species of birds as de- that potentially can affect parasitic transmission as finitive hosts. An experimental study showed that the compared with more simple systems, an increase in the introduction of two species of amphibians with different number of species in a system does not always cause a degrees of compatibility with the parasite caused a dilution effect on parasite transmission (Upatham and lower level of production of cercariae compared with Sturrock, 1973) and even in some cases an increase in production when only the more competent species is the risk of infection has been reported (Begon, 2008). present (Johnson et al., 2008). The net effect that a change in biodiversity can generate However, the presence of a less competent host is not on certain host-parasite systems will be related to the always necessary for production of a dilution effect in a kind of interaction maintained by the parasite with the parasitic interaction. The trematode Renicola roscovita species affected by the change (Johnson and Thieltges, uses different species of bivalves as intermediate hosts 2010). In addition, parasite intrinsic factors such as fer- and birds as definitive hosts. In two localities in the tility, resistance of parasitic forms in the environment, northern Wadden Sea two species of introduced bivalves and parasitic specificity can counteract the potential are competent hosts for R. roscovita. However, definite dilution effect (Johnson and Thieltges, 2010). hosts only prey upon endemic bivalves thus reducing The alleged benefits of biodiversity buffering the the possibilities of successful parasite transmission transmission of certain diseases have to be weighed (Krakau et al., 2006). against the greater diversity of infectious pathogens. In Predation and hyperparasitism are other biological fact, a latitudinal gradient in biodiversity, including mechanisms related to the dilution effect. In a complex pathogens, decreasing as we move away from the equa- ecosystem these mechanisms are more likely to occur tor has been described (Rohde, 1992; Guernier et al., due to the higher number of species in the system and 2004; Hillebrand, 2004; Jones et al., 2008; Merino et al., they can play an important role in the transmission of 2008). However, other studies have shown contradictory certain diseases. For example, experimental systems results in this respect. For example, Nunn et al. (2005) have shown that predation on larvae of the nematode found this pattern in primates only for protozoans, but Strelkovimermis spiculatus by copepods reduces both not for viruses or helminths, and Poulin (1995) and prevalence and density of parasites infecting the next Bordes et al. (2010) did not find any correlation be- hosts, the mosquito Aedes aegypti. In some cases the tween helminth species richness at intra- or interspecific predation rate reaches 100% of the larvae (Achinelly et levels and latitude. Moreover, Lindenfors et al. (2007) al., 2003). In the case of the life cycle of Schistosoma and Krasnov et al. (2004) found the opposite pattern for mansoni introduction of the predator Lebistes reticulates, helminths of carnivores and fleas on rodents, respec- a guppy fish, produces an important reduction in both tively, although the asymmetric sampling effort could be miracidia and cercarie, thus reducing the infection rate one explanation for these inconsistent results (Poulin, of intermediate hosts, the snail Biomphalaria glabrata, 1995; Lindenfors et al., 2007). The need for special re- 394 Current Zoology Vol. 57 No. 3 quirements for parasite transmission that do not follow a (Hunter, 2003; Rogers and Randolph, 2006; Genchi et clear latitudinal distribution and/or spread of diseases by al., 2009). The result of this increase in temperature is migratory hosts can also affect the latitudinal gradient in an increase in density of vectors that may cause the ap- parasitic diseases (Merino et al., 2008). Regardless of pearance of diseases in new regions and/or increased whether the correlation between parasitic species rich- transmission in endemic regions. Rainfall regime may ness and latitude is general or specific, some authors also alter the density of vectors. An increase in precipi- have suggested that prevalence of a particular parasite tation can promote reproduction of water-dependent may be low in areas with high biodiversity, which usu- species allowing them to complete their life cycle. This ally occurs at low latitudes, as compared with other re- is the case for different mosquito species whose abun- gions with less biodiversity that usually occurs at higher dance is associated with the prevalence of the diseases latitudes (Johnson and Thieltges, 2010). However, (i) that they transmit (Gill, 1938; Wegbreit and Reisen, studies showing the existence of a latitudinal gradient 2000; Tong and Hu, 2001; Zhou et al., 2004; Shaman for virulence of diseases, being higher at low latitudes and Day, 2007). (Møller et al., 2009; Robar et al., 2010), and (ii) the Obviously, decreases in temperature below a certain possible relationship between biodiversity and emergent threshold or prolonged drought will have the opposite diseases constitute two serious difficulties for the dilu- effect, decreasing the density of vectors and the preva- tion effect hypothesis (Woolhouse and Gowtage- lence of diseases they are transmitting. There are some Sequeria, 2005; Jones et al., 2008). examples of such relationships between climate and 2 Host Density and Prevalence density or incidence of parasites and diseases transmit- ted by them. For example, some studies have linked an Density of hosts, vectors and parasites in a geo- increase in temperature associated with NAO and graphic area are key factors for disease transmission. ENSO with the advance in development of species of Any extreme environmental change can alter the density ticks and increased transmission by seabirds (Duffy, of every component of the host-parasite system, and, 1983; Boulinier and Danchin, 1996). Other studies re- therefore, the prevalence of the disease. Some causes of port the adverse effect of minimum temperature and extreme environmental change are related to human wind on the abundance of Simulium blackflies attacking activity like agriculture, livestock farming, hunting, nests of birds (Martínez-de la Puente et al., 2009), or the urbanisation, pollution and transports (Macpherson, potential importance of nest temperature as a cue used 2005; Hayes et al., 2010). However, we cannot disre- by insects for locating nests of their hosts (Martínez-de gard the impact of climatic change on parasitic interac- la Puente et al., 2010). The advancement of spring in tions (Marcogliese, 2008; Pech et al., 2010). Regardless parts of Northern Europe due to an increase in tempera- of the origin of environmental changes, these may have ture has affected the phenology of parasites and their an impact on different aspects that ultimately affect the abundance. In particular, advancement in phenology of density of hosts and parasites: survival, phenology, be- the hippoboscid fly Ornithomyia avicularia was associ- haviour and/or distribution range. ated with a higher prevalence of this parasite in barn In parasite-host systems dependent on vectors or swallows Hirundo rustica (Møller, 2010). Other studies possessing free-living stages, weather conditions to a have found that a rainy and cold spring negatively af- large extent determine the transmission of diseases. fects the abundance of certain ectoparasites of birds Variation in temperature and rainfall regime can cause (Merino and Potti, 1996). The effect of temperature on fluctuations in density and distribution of hosts and the abundance of ectoparasites has also been experi- parasites. Species that act as vectors of many infectious mentally demonstrated in nests of the tree swallow and parasitic diseases are usually arthropods showing a Tachycineta bicolor parasitized by Protocalliphora high dependence on environmental temperature for their blowfly larvae, with an increase in the number of larvae survival and development. In fact, there are studies that with an increase in temperature up to 25°C (Dawson et demonstrate a positive correlation between the degree of al., 2005). In the case of the nematode Setaria tundra feeding activity, reproduction and mortality of mosqui- transmitted to reindeer Rangifer tarandus by mosquitoes toes and ticks with temperature (Drew and Samuel, of the genera Aedes and Anopheles, there is a positive 1986; Loetti et al., 2008; Freire and Schweigmann, 2009; relationship between average summer temperature, Estrada-Peña et al., 2011). Vector distribution range also vector density and prevalence of helminths in their de- seems to be related to an increase in temperature finitive hosts (Laaksonen et al., 2009). Tempera- MARTINEZ J, MERINO S: Parasitism and extreme climate 395 ture/abundance relationships seem clear for ectopara- North-western Europe if the trends of increasing tem- sites showing autonomy outside their hosts, while para- perature and precipitation continue because survival of site species more dependent on their hosts are less sus- oocysts of the parasite is favoured under these condi- ceptible to fluctuations in temperature (Møller, 2010). tions (Meerburg and Kijlstra, 2009). Other models pre- Parasites with free-living stages in their life cycles are dict an increase in the prevalence of Dirofilariosis in especially sensitive to changes in temperature and hu- Europe due to the alleged temperature increase an- midity (Bush et al., 2001). In particular, an increase in nounced by IPCC. In this case both development of the temperature and rainfall increases survival and devel- parasite in the vector (mosquito) and its expansion to opment of free-living larvae of the nematode Trichos- more northern areas would be favoured (Genchi et al., tronylus tenuis, a fact that affects the population dy- 2009). The parasite-host system formed by the pulmo- namics of its definitive host, the red grouse Lagopus nary nematode Umingmakstrongylus pallikuukensis and lagopus (Hudson, 1986; Hudson et al., 1992, 1998). the musk ox Ovibos moschatus is yet another example Another study shows the beneficial effect of an increase of how to integrate empirical and experimental knowl- in temperature on development of fluke cercariae, in- edge acquired in a predictive model. The nematode de- creasing levels of infection in their intermediate hosts pends on a snail as intermediary host to complete its life (Poulin, 2006). Other studies on flukes demonstrate the cycle, but its development is slow due to low tempera- close relationship between rainfall regime and the pro- tures in the Arctic (Kutz et al., 2002). Generally, the portion of hosts infected by different species of Digenea parasite takes two years to be infective, which implies (Pech et al., 2010). Moreover, this relationship has a survival of the harsh winter to reach the definitive host. marked seasonality clearly explained by the amount of This fact reduces the success of the parasite because rainfall, and such seasonality have also been observed in many individuals fail to overcome the winter. However, diseases caused by intestinal nematodes in domestic if the increase in average temperature in this area during animals (van Dijk et al., 2008). The positive effect of an recent years is included in the model, nematode infec- increase in temperature has also been noted in some tivity could be achieved in only one year, before the species of protozoa. In particular the ciliated Orchito- arrival of winter. Therefore, mortality of larval stages phrya stellarum, parasite of starfish, shows a faster de- decreased considerably, leaving more larvae available velopment between 10 and 15°C, and in addition an for infection of the definitive host causing an increase in increase in infectivity is also noted (Bates et al., 2010). the pressure of the parasite on muskoxen (Kutz et al., Seasonality in the prevalence of certain parasitic dis- 2005). eases is a feature of regions where there is marked fluc- Therefore, factors that should be taken into account tuation in weather conditions, indicating that the para- to assess the impact of extreme climatic changes on sites dependent on external environmental conditions parasitic relationships would be (i) autonomy and resis- can only develop within certain thresholds of tempera- tance exhibited by parasites outside their host. For ex- ture and rainfall. Therefore, these conditions limit the ample, some ectoparasites such as flies that are also transmission of diseases caused by parasites. The in- vectors of diseases have sufficient autonomy away from crease in temperature and humidity in certain geo- their hosts, but are very susceptible to fluctuations in graphic areas can not only increase the abundance and temperature and humidity from a phenologic point of the prevalence of parasites, but also their range and that view. However, some ectoparasites are totally dependent of their hosts. The expansion of the range of certain on their hosts (lice and some mites), and although they vectors such as mosquitoes has occurred for altitude on are affected to a lesser extent by changes in weather, the Hawaii Islands (Atkinson, 2008; Lovejoy, 2008) and they are more susceptible to fluctuations in density of latitude in New Zealand (Tompkins and Gleeson, 2006). their hosts; (ii) parasite specificity because highly spe- In both cases the change of distribution of the vectors cific parasites will have greater difficulty finding a host would be associated with an increase in the prevalence if their density drops due to environmental change; and of diseases transmitted, in these two cases listed above (iii) type and complexity of epidemiological cycle be- avian malaria. cause parasites with complex life cycles that depend on Several models predict change in abundance and/or invertebrate intermediate hosts (for example, flukes) or distribution of diseases under scenarios of climate with free-living stages (for example nematodes) also change. Some models predict an increase in prevalence experience more difficulties completing their life cycle, of toxoplasmosis in human populations in parts of because in both cases they lack homeostatic mecha- 396 Current Zoology Vol. 57 No. 3 nisms to resist wide fluctuations in temperature and hu- cies can be direct if they imply a change in density of midity. Parasites with resistant forms such as eggs or hosts and parasites, and therefore in transmission of cysts will be affected to a lesser extent because these diseases, or they can be indirect if they increase in sus- adaptations allow them to expand their range of tole- ceptibility to infection due to immunosuppression rance to environmental changes. caused by a reduction in appropriate nutrients (see next A good example of the possible effect caused by the section). In the case where movement implies a change introduction of a new species in an established ecosys- in their range, they can be considered invasive species tem occurred in Canada. In order to reduce the pressure and their effects for native species may be very different. exerted by hunting on certain species of ungulates such For example, if an invasive species introduces new as caribou Rangifer tarandus and moose Alces alces, parasites into an area, they could have (i) a deleterious white-tailed deer Odocoileus virginianus were intro- effect on the host endemic species if their immune sys- duced from another region where the tick Dermacentor tem has not the appropriate response to control new albipictus was common (Kutz et al., 2009). However, parasites, or (ii) a beneficial effect if the novel parasites the introduced deer are a perfect reservoir of ticks for compete with endemic parasites. However, competition the other species of ungulates to be protected. Although between parasites may also produce an increase in viru- it is unclear whether ticks come from infected intro- lence if competition selects for parasites being able to duced individuals, it seems obvious that the introduction obtain resources at a fast rate to outcompete other para- of deer has considerably increased the abundance of this site lineages (Frank, 1996). species of tick, with serious consequences for the en- 3 Immunosuppression demic fauna as for example chronic weight loss, anemia, hypoalbuminemia, hypophosphatemia, transient de- When biodiversity and density of parasites and hosts creases in serum aspartate transaminase and calcium allow contact between the two members of the hypo- and hair loss in moose (Glines and Samuel, 1989; Sam- thetical parasitic interaction, the immune system deter- uel, 1989). Another example that illustrates the impor- mines the future of the association (Combes, 2001; Me- tance of population density for transmission of diseases rino, 2010). The system of protection against intrusion comes from Malaysia. In this region, frugivorous bats includes multiple mechanisms, from simple physical are host of Nipah virus and they transmit this disease to barriers like the skin and mucous membranes to very domestic pigs. The disease spreads at high speed among specific adaptive mechanisms at the cellular level like pigs due to their high density in local farms and finally the production of antibodies. Investment in immunity is jumps to humans without much difficulty (Epstein et al., a balance between the energetic cost involved in 2006). mounting a particular response (Råberg et al., 2000; Population density can also be affected indirectly by Martínez et al., 2004), the collateral damage that this pollution. In particular, the use of fertilizers containing response can generate in the host, and the protection that

N2 causes eutrophication of ecosystems, increasing pri- it provides (Råberg et al., 1998), this balance differing mary productivity. This fact positively affects reproduc- among pathogens. The more complex defensive mecha- tion and development of certain intermediary hosts nisms are accurately adjusted at the neuroendocrine (snails) and vectors (mosquitoes), as well as certain level although numerous circumstances may alter this bacteria and fungi, increasing the efficiency of trans- adjustment. Factors that may be involved in the altera- mission of certain diseases (McKenzie and Townsend, tion of the adjustment of the immune system and there- 2007). However, an increase in nutrients can also pro- fore the balance of the parasitic associations tend to be mote development of competitors or predators of hosts associated with the presence of (i) chemical contamina- infected by parasites, and in this case a reduction in tion of human origin, and (ii) different types of stress transmission of the disease can occur. In addition, under especially heat and nutritional stress and/or infection by conditions of increased parasite transmission, as is usual certain pathogens. Although many of these factors can when host density increases, an increase in virulence is modulate immune mechanisms, the increased suscepti- expected simply because ease of transmission can select bility to a disease will depend upon the altered mecha- for more virulent parasite lineages (Ewald, 1994) and nism and on the magnitude of the change, because the consequently an increase in immune response (Møller et immune system is able to act properly exercising its al., 2006). protective role within ranges that are characteristic for The effects of phenologic changes in migratory spe- every immunological parameter and pathogen (Adamo, MARTINEZ J, MERINO S: Parasitism and extreme climate 397

2004). The effects that chemical pollutants exert on the ture can cause heat stress in individuals depending on immune system can directly impact on the cells of the their thermoregulation system and the magnitude and immune system and on the production of soluble me- duration of the change (Bowden et al., 2007; Deutsch et diators like antibodies and cytokines (Dunier and Si- al., 2008). Both increases and decreases in temperature wicki, 1993; Banerjee, 1999; Voccia et al., 1999), and can alter immune system functions involved in resis- on the neuroendocrine system (Colborn et al., 1993), tance to infections. It is know that heat stress in ecto- which regulates development, maturation and activity of therm animals adversely affects certain immune mecha- the immune system (by secretion of hormones like oes- nisms as phagocytosis (Wang et al., 2008), oxidative trogen, thyroid hormones and glucocorticoids) capacity (Coteur et al., 2004), the prophenoloxidase (Grossman, 1984; Lam et al., 2005; Sternberg, 2006). system (Vargas-Albores et al., 1998) and the synthesis Although numerous studies have shown the toxic/ of antibodies (Maniero and Carey, 1997). Something modulator effect of numerous chemical pollutants on the similar occurs in endotherm animals, where a decrease immune system, very few directly relate changes of in innate and adaptive immune response is associated susceptibility to a disease with immunological altera- with increases in temperature (Sinclair and Lochmiller, tions caused by pollutants. However, two studies carried 2000; Zahraa, 2008). Sometimes an increase in tem- out on amphibians suggest that the pesticides atrazine perature can enhance the performance of the immune and malation have an effect on the increase of certain system by inducing greater production of lysozyme and infections (Hayes et al., 2006, 2010; Denver, 2009). IgM (Chen et al., 2002; Dominguez et al., 2004; Ndong The immune mechanisms protecting individuals from et al., 2007). Moreover, elevated body temperature (fe- pathogens are energetically expensive to maintain ver) produced by infection in endotherm animals is a (Råberg et al., 2000; Ots et al., 2001; Martin et al., 2003, very useful adaptive mechanism for generating a hostile 2007b; Martínez et al., 2004), and, therefore, any energy environment for the intruder and for promoting activa- deficit caused by a reduction in resources or an increase tion of the immune system (Hanson, 1997). This appar- in basal metabolic rate may indirectly affect immune ent contradiction can be explained by taking into ac- response. Individuals subject to this type of nutritional count the magnitude and duration of heat stress, because stress redistribute energy to vital physiological systems prior acclimation of individuals to thermal conditions while neglecting others such as the immune system. removes the immunosuppressive effect of the stress This relationship has been established in different spe- (Demas and Nelson, 1998; Shephard and Shek, 1998; cies naturally undergoing high energetic demands (re- Ksiazek et al., 2003). Thus, fluctuation in temperature is production) or under experimental restriction of food as important as the time interval during which it occurs. intake (Sheldon and Verhulst, 1996; Ardia et al., 2003; Although the relationship between thermal stress and French et al., 2009). Therefore, any environmental immunosuppression seems evident, this direct associa- change that causes nutritional stress may adversely af- tion with disease episodes or increases in susceptibility fect the immune system and consequently susceptibility to certain infections has been confirmed in only few to disease. Chemical contaminants may also have this cases. However, numerous studies have linked the onset indirect effect on the immune system, because different of epidemic outbreaks with extreme fluctuations in both species of fish, amphibians and reptiles when exposed cold and heat for different parasite-host systems (Chis- to industrial effluents show abnormally high metabolic holm and Smith, 1994; Cook et al., 1998; Paillard et al., rates and reduced growth (Hopkins et al., 1999; Rowe et 2004; Bruno et al., 2007; Harvell et al., 2007; Travers et al., 2001). Nutritional stress can also be produced by a al., 2008; Wegner et al., 2008; McClanahan et al., 2009). redistribution of ecological associations present in the In the future these systems could be the basis for estab- ecosystem. For example, a change that promotes in- lishing the immunological mechanisms that are imbal- creases in competitors and/or predators may provoke anced by heat stress. nutritional stress by a reduction in resources caused by In some parasitic associations, proper functioning of competition or an increase in the metabolic rate caused the immune system of the hosts can be compromised as by predators (Martin et al., 2010). In fact a study shows a result of the action of the parasite. A good example of that the introduction of a predator species affects the this fact is the human immunodeficiency virus (HIV). level of stress of the native prey species (Berger et al., This virus causes immunosuppression in affected indi- 2007). viduals, making them much more susceptible to diseases The environmental changes that affect air tempera- of all kinds (Frebel et al., 2010). This immunosuppres- 398 Current Zoology Vol. 57 No. 3 sive effect caused by HIV is not an exception as it is onstrated that the diversity of human pathogens present well documented for other parasitic infections (Nus- in a given region is explained by an astonishing 72% by senzweig, 1982; Leiro et al., 1988; Maizels et al., 1993; the diversity of mammals and birds present in the area Szteina and Kierszenbaumb, 1993; Allen and Mac- (Dunn et al., 2010). In contrast, the prevalence of hu- Donald, 1998; Boëte et al., 2004; Maizels, 2009; man diseases is positively related to the diversity of Maizels et al., 2009; Stempin et al., 2010). pathogens, the size of the population, climate and in- Finally, it is important to mention the role of the mi- vestment in campaigns of control (Dunn et al., 2010). crobiomas, microbial endosymbiotic communities living Given these data, and considering that less diverse eco- in a particular organism, on the immune system. About systems support fewer human pathogens, there could be 90% of the cells in humans are bacteria (Turnbaugh et a conflict between conservation and health. However, al., 2007). These microorganisms live in all kinds of the net benefits provided by complex ecosystems to epithelial tissues where they established so tight rela- humans (Costanza et al., 1997) discard completely the tions with the host that proper functioning of the tissue possibility of reduction of biodiversity to solve health would be impossible without the presence of these or- problems. In the same study, the economic investment ganisms. In addition, they are able to exert a protective in control campaigns appeared as a very important role against certain diseases because the alteration of variable in predicting the prevalence of human diseases. these microbial communities has been linked on several The economic investment does not reduce the diversity occasions to increased susceptibility to a disease of pathogens, but shows a very significant impact on (Holzman et al., 2001; Roos et al., 2001; Chang et al., reducing the prevalence of diseases, especially in re- 2008). This benefit has not only been found in humans, gions with many inhabitants, high prevalences and low but also in other mammals, amphibians and even corals or no investment in prevention campaigns. As a conclu- (Harris et al., 2009; Lawley et al., 2009; Sunagawa et al., sion, the authors propose to invest money in such re- 2009). In some cases the protective effect is exercised gions, because a small investment will produce a sig- by competition between species, either preventing the nificant reduction in prevalence. By reducing the preva- development of the pathogens installed in the host or by lence in these areas the probability of occurrence of a blocking their invasion. This protective role is suffi- disease outbreak and, thus, of a pandemic is considera- ciently important to consider microbiomas as part of the bly reduced. Therefore, this recommendation would innate immune system acting as a first barrier of de- have a benefit on a global scale. Such measures should fence. However, their role seems to go further as studies be carried out especially in areas with high incidence of show an active role of these organisms in the modula- extreme environmental changes so that the potential for tion of immune responses (Isolauri et al., 2001; Forsythe spread of diseases following the event is reduced. and Bienenstock, 2010; Kelly, 2010; Nayak, 2010; Tre- Attempts to completely eradicate a disease with a bichavsky et al., 2010; Gourbeyre et al., 2011). It is low prevalence are not very realistic as this requires clear that if extreme environmental changes affect these thorough monitoring of the disease with the costs that symbiotic relationships, an indirect effect of the envi- this entails. A real example of the implementation of ronmental change on immunity of hosts may favour the these recommendations is based on malaria. Using pre- spread of diseases. dictive models some researchers have predicted an in- 4 Consequences and Future Directions crease in endemicity, morbidity and mortality of human parasitosis in general (McMichael et al., 2006; Senior, Alterations of host-parasite relations caused by envi- 2008; Semenza and Menne, 2009) and of malaria in ronmental change often produce undesired effects on particular (Tanser et al., 2003; van Lieshout et al., 2004) public and veterinary health (Mas-Coma et al., 2008; due to the hypothetical increase in global average tem- http://who.int/globalchange/climate/summary/en/index5. perature during the present century. However, the extent html). From the health point of view, the occurrence of of endemic malaria areas in the world between 1900 and outbreaks of new or established diseases in a given re- 2007 has been considerably reduced in spite of this pe- gion is a concern for health authorities. This has riod being characterized by global warming (Gething et prompted recent studies of factors contributing to such al., 2010). This apparent paradox is resolved if we con- epidemics/pandemics as well as preventive measures sider effects of urbanization and economic development (Harrus and Baneth, 2005; Macpherson, 2005; Brooks during the 20th century, namely, development of thera- and Hoberg, 2007; Omenn, 2010). A recent study dem- pies and health infrastructure and investment in control MARTINEZ J, MERINO S: Parasitism and extreme climate 399 campaigns on a large scale (Kleinschmidt et al., 2006; human-dominated ecosystems, future predictive models Sharp et al., 2007; Teklehaimanot et al., 2009). There- should take the socio-ecological system (Alessa et al., fore, the predictive models on the dynamics of a given 2008) and the concept of anthropogenic biome (Alessa disease should take the effects of these variables into and Chapin, 2008; Ellis and Ramankutty, 2008) into account. However, the potential increase of extreme account to achieve a more realistic approach to the con- climatic events can destroy or pose important difficul- sequences of the social and environmental changes. ties for development and implement of any measure to From a veterinary perspective implications are usua- control the extent of diseases. In this respect, interna- lly economic since the appearance of disease outbreaks, tional action to control emerging epidemics following or simply an increase in the abundance of certain para- extreme environmental change, with special emphasis sites, often lead to a detriment of animal health and a on areas with higher incidence of these events, is proba- reduction in productivity (Morgan and Wall, 2009). The bly the only possible prevention measure. overcrowding of animals is a determining factor in the A case apparently opposite to that of malaria is transmission of certain pathogens (Bisdorff et al., 2006), schistosomiasis with the etiological agent being the while those feeding on the vegetation are most suscepti- fluke Schistosoma japonicum. The prevalence of this ble to parasites with free living stages like nematodes disease has shown an increase in certain areas of China (O’Connor et al., 2006). However, it is almost impossi- despite investments by the government in control cam- ble to avoid overcrowding of surviving livestock after paigns during the last decades (Liang et al., 2007). The an extreme event due to the disappearance of appropri- epidemiological cycle of this parasite is totally depen- ate space for livestock and other domestic animals. dent on water availability for survival of their Health and veterinary problems are not independent. free-living forms and development of their intermediate In the last 10 years about 75% of new diseases detected host (freshwater snails). Although some studies attribute in humans have been caused by pathogens of animals or a role to the overall increase in temperature in this case animal products. Some of these zoonotic diseases can (Zhou et al., 2005), the main cause seems to be greater follow an extreme climatic event and have the potential impact caused by building of the Three George dam that to extend globally and therefore to cause serious health generates the right environmental conditions to facilitate problems (http://www.who.int/zoonoses/en/). However, transmission of this disease (Maszle et al., 1998; Remais other diseases are easily prevented, but remain prevalent et al., 2007). In fact, numerous dams such as the Aswan in developing countries, especially in poorer popula- Dam in Egypt, the Tigay dam in Ethiopia, the Kossou tions. One of the first consequences of extreme climatic and Taabo dams in Cote d'Ivoire, the Diama dam in conditions as well as human activity is habitat destruc- Senegal and Manantali dam in Mali have resulted in tion and thus shrinking ecosystems. Under these condi- major outbreaks of schistosomiasis (http://ehs.sph. tions an increase in pathogenicity is expected, mainly berkeley.edu/china/current_projects/Environmental_ due to the increase in host density and influx of new Change.htm). Although the economic implications of diseases in fragmented areas (Holmes, 1996). Therefore, the dam for China may justify its construction, control special attention to the potential emergence of diseases campaigns should have emphasised the increased risk of should be directed to such newly fragmented habitats, transmission that it entails. Therefore, uncoordinated where contact between different areas increases abruptly, policies can lead to a high economic cost without allowing for the contact between different organisms achieving the proposed objectives, that is, the reduction with new parasitic interactions. or eradication of a disease. Such cases can be consi- 5 Conclusion dered similar to the production of important and recur- rent floods in some areas and the same logistic measures The consequences of environmental changes on should be carried out to avoid the spread of diseases. parasite-host interactions are difficult to forecast. To do The lack of foresight exhibited by some predictive that we should know all abiotic and biotic factors that models is the result of the classical view of ecological determine the stability of the specific interaction, and sciences on humans and nature (Millennium Ecosystem this implies a deep knowledge not only of the epidemi- Assessment, 2005). That view has traditionally sepa- ological cycle of the parasite, but also of the entire eco- rated humans from nature, ignoring the human feedback system in which the interaction takes place. Although on ecosystems and biomes (Ellis and Ramankutty, 2008). the stability of ecological associations is a chimera, However, as most of the world is constituted of parasitic associations with certain stability probably 400 Current Zoology Vol. 57 No. 3 occurred long ago in conditions of little fluctuation in Alessa L, Kliskey AA, Brown G, 2008. Social-ecological hotspots abiotic and biotic factors. 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