Parasitism in a changing world: The intertidal trematode Maritrema novaezealandensis and its hosts

Abstract

There is growing concern about increases in diseases and parasitism with on-going and predicted global climate changes in many ecosystems, including marine ecosystems. Understanding and predicting the possible consequences of these changes on a particular host-parasite system, however, requires a sound knowledge of various aspects of the life cycle components, including their interactions with the environment.

This thesis investigated the ecology of the intertidal microphallid trematode Maritrema novaezealandensis and the hosts associated with its complex life cycle: first intermediate snail hosts Zeacumantus subcarinatus, second intermediate amphipod hosts Paracalliope novizealandiae and definitive bird hosts. An integrative approach was adopted to examine current temporal patterns on a high prevalence mudflat (field study), study the sensitivity of individual steps of the parasite’s transmission process from first to second intermediate host (both ectotherms) to abiotic (temperature, salinity and ultraviolet radiation) and biotic environmental factors (laboratory studies), and subsequently use that information to model the life cycle of the parasite and assess the consequences of predicted global warming on the study system, in particular on amphipod hosts.

The seasonal field monitoring showed not only that most of the parasite transmission from first to second intermediate invertebrate hosts takes place during warm summer months, but also that probably the entire life cycle of this parasite is accelerated during that time. This is due to temperature directly, but also due to the availability of hosts.

All environmental factors investigated in the laboratory studies emerged as potentially strong modulators of the transmission of M. novaezealandensis, with temperature having the most pronounced effects overall. The two steps of the transmission process identified as the most sensitive were the survival of the free-living parasitic transmission stage (affected by all factors, also interactively) and the survival of amphipods. Results indicated that conditions considered optimal for transmission (low tide, warming water in tide pools) benefited the successful transmission of the parasite to amphipod hosts up to an optimum temperature. Furthermore, the presence of a non-host community member that preys upon the parasitic transmission stages was not strong enough to counteract an increased transmission success of the parasite under conditions of warmer temperatures.

In contrast, ultraviolet radiation may account for substantial mortality of the free-living parasite stages in nature, due to the absence of protective mechanisms. This effect may, however, be compensated by an increased susceptibility of amphipods to infection.

The mathematical model simulating the dynamics of the life cycle of M. novaezealandensis under different temperature increases was based on information from the field, laboratory experiments or the literature. The simulations indicated that the predicted temperature increases capable of driving the modelled amphipod host population to collapse mostly fell within the range of temperatures predicted to prevail in the study area over the next 80 years.

Overall, M. novaezealandensis and its impacts on hosts were not only shown to be influenced by environmental conditions intrinsic to intertidal ecosystems, but are also predicted to be affected by the changing conditions due to global change.