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