Parasitism, climate oscillations and the structure of natural communities

Recently, Ottersen et al. (2001) reviewed the ecological impacts of the North Atlantic climate oscillation (NAO). The NAO is responsible for interannual and decadal fluctuations in winter temperatures, precipitation, wind conditions as well as distribution and fluxes of currents on both sides of the North Atlantic Ocean (Hurrell and van Loon 1997). A highly positive NAO index (measured as the deviance from the average sea level pressure difference between the Azores and Iceland) is associated with high temperatures, strong winds and high levels of precipitation in northern Europe, and low temperatures in eastern North America. A low NAO index gives rise to the opposite conditions (Hurrell and van Loon 1997). The NAO can be seen as a North Atlantic parallel to the El Niño-Southern-Oscillation (ENSO) in the Pacific Ocean also resulting in temporal and geographical fluctuations in temperature and precipitation from the Indian Ocean to the Gulf of Mexico (Allan et al. 1996). Such large-scale climatic fluctuations are bound to affect a multitude of ecological processes. Indeed, in addition to the direct influence on the general biological performance of various organisms, Ottersen et al. (2001) also report studies demonstrating more complex and indirect cascading effects in which NAO mediates the outcome of interspecific competitive and predatorprey/herbivore-plant interactions. However, despite the mounting evidence that parasites can influence the composition and structure of natural communities (Minchella and Scott 1991, Hudson and Greenman 1998), and that parasite transmission is often strongly affected by weather conditions, there was no mention of parasitism in the review. In the ecological literature, this is not an unusual omission, as several authors have emphasised recently (Mouritsen and Madsen 1994, Huxham et al. 1995, Marcogliese and Cone 1997, Morand and Gonzales 1997, Poulin 1999, Thomas et al. 1999, Skorping and Högstedt 2001). To the authors’ defence, their review focused on papers that either investigated the influence of NAO directly or presented time-series that would suggest the signature of this climate oscillation. And to our knowledge, no study has hitherto explicitly considered the impact of NAO on host-parasite interactions. Nevertheless, examples of ENSO-mediated parasiteinduced host dynamics do exist, and several papers have directly or indirectly shown that parasite-induced host population dynamics or distribution are governed by short-term changes in weather conditions or general climate change (see e.g. Harvell et al. 1999, Marcogliese 2001, and references in Table 1). To us, this clearly justifies specific attention to the potential influence of climate oscillations on host-parasite interactions, host population dynamics, and consequently also on community structure. Table 1 summarises a range of very different hostparasite systems influenced by temperature in particular, but also by precipitation and ocean currents. Although comprehensive, the list is certainly not exhaustive and only serves to illustrate the potential widespread effect of climate oscillations on parasitism and its consequences. Although the oscillations will affect the climate almost worldwide throughout the year, they are basically ocean phenomena restricted – in the case of the extratropical oscillations – to the winter season (Allan et al. 1996, Hurrell and van Loon 1997). For this reason, we have focused on host-parasite systems from nearcoastal areas where the winter sea surface temperature may carry over through to the summer (Ottersen et al. 2001), and on parasites having life cycles that will render them sensitive also to the winter and/or early spring climate. The first examples emphasise the direct impact on the life-cycle processes of the parasites (especially transmission rates) whereas the remaining ones demonstrate more complex cascade effects, in which the outcome of the specific host-parasite interaction is found or