Projects

Three-dimensional network representation of the Otago Harbour
intertidal mudflat food web. Free-living taxa are shown in blue, and parasitic ones
in red. The vertical position of a taxon corresponds to its trophic level.

Parasites and food webs: Although traditionally excluded from food web studies, parasites are integral parts of trophic networks. They contribute to the flow of energy through a food web both as consumers of their hosts, but also as resources themselves (they are eaten by a range of predators). We investigate how incorporating parasites into food webs changes their topological structure as well as their stability, resilience and other dynamical properties. Also, we use network analysis tools to determine how food web structure affects parasite transmission, by favouring certain trophic transmission routes over others. Our work focuses on New Zealand lake ecosystems as model food webs varying with respect to species richness, presence of introduced species, etc. The project is currently funded by the Marsden Fund. [Poulin, Lagrue]

Molecular ecology and diversity of trematodes: Despite the ubiquity and importance of trematodes within natural ecosystems, few studies have used genetic data to examine their ecology. Identifying trematode genetic clones within the same species provides empirical data for addressing questions concerning the number of parasite infections within individual hosts, the influence of environmental conditions on parasite clonal diversity within hosts, the spatial distribution of clones within hosts, trematode transmission strategies, how genetic relatedness affects life history strategies adopted by trematodes, etc. We are investigating several of these questions with New Zealand freshwater and marine trematodes using microsatellite loci to identify genetic clones. In addition, we are also using molecular markers identify cryptic species and to address large-scale questions of phylogeography and gene flow among trematode populations, and making contributions to the taxonomic description of New Zealand's parasite biodiversity. [Poulin, Blasco-Costa, Presswell]

The trematode Acanthoparyphium sp. (Echinostomatidae): rediae and some free cercariae inside the snail first intermediate host (left), free-swimming cercariae (middle), and encysted metacercariae inside a cockle second intermediate host (right).

Evolution of host specificity: There are constraints on the ability of parasites to expand their host range by exploiting novel host species. We are investigating the role of morphological and genetic variation in determining how parasites perform when exposed to hosts that are progressively more phylogenetically distant from their normal host. The research uses trematodes as model organisms, and also explores what affects the ability of parasites to overcome local adaptation and succeed at exploiting geographically distant host populations. [Poulin]

Transmission and life history strategies of trematodes: Most parasites show some intraspecific variability in their developmental schedules and transmission pathways. In some trematode species within their first intermediate hosts (snails), we now have evidence that members of the same clone show a division of labour, with some rediae specializing for defence, others for reproduction. In other trematodes within their second intermediate hosts, precocious maturation involving an abbreviated life cycle is commonly observed. Some of this plasticity is under genetic control, but much of it is also influenced by external factors. For instance, the presence of other parasites within the same host can affect the strategies chosen by a parasite: these other parasites can be close genetic kin, unrelated conspecifics, or individuals of other species. Can a parasite adjust its developmental strategy based on the identity of the other parasites with whom it shares the host? Also, parasites in their intermediate host can benefit from information on the current abundance of definitive hosts. For example, trematodes capable of progenesis (early sexual maturation) would benefit by initiating reproduction inside their intermediate host when definitive hosts are rare, thus bypassing the need for transmission to the definitive host to complete the life cycle. Are parasites capable of adjusting their life history strategies based on the likelihood of transmission under current external conditions? We are using field and laboratory experiments, using single and mixed-clone infections of model trematode species in their intermediate hosts, to explore plasticity in development, life history strategies, and transmission routes in parasites. [Poulin, Lloyd, Kamiya]

Alternative transmission modes in the trematode Coitocaecum parvum (Opecoelidae): the normal 3-host life cycle (left), and the truncated 2-host cycle in which the parasite reproduces precociously in its second intermediate host (right).

Coitocaecum parvum: progenetic metacercaria (left)
with its eggs, and two 'normal' metacercariae (right),
including a recently-encysted one. By
self-insemination, hermaphroditic worms adopting
progenesis can produce several hundred eggs while
inside their amphipod intermediate host.

Parasitism, environmental change and community structure in natural ecosystems: Parasites are ubiquitous, though often invisible, components of ecosystems. They influence the survival and reproduction of individual hosts, the dynamics of host populations, and the structure of entire communities. In marine systems, our research focuses mostly on parasitism in molluscs, crustaceans and polychaetes. Using field and lab experiments, we study the transmission ecology of parasites in these systems, as well as the direct and indirect impact of parasitism on the density of key host species, the biomass of key functional groups, and the overall biodiversity of intertidal ecosystems. We explore the likely effect of species invasion, global warming, ocean acidification and other environmental changes on the interaction between parasitism and the structure and diversity of coastal systems. In freshwater systems, we are investigating the impact of parasites on the structure and dynamics of planktonic communities, as well as on entire lake communities. We are also interested (i) in the interaction between parasitism and biological invasions, i.e. when exotic species become hosts to native parasites and then act as a reservoirs of infection to native hosts, and (ii) in the influence of agricultural pollution on host-parasite interactions, and the impact of trematode parasites on juvenile fish, following up evidence that infection within the first few weeks of life can cause malformations in fish and affect survival and recruitment to the adult population. [Poulin, MacLeod, Studer, Thomas, Hock, Valois, O'Dwyer]

When heavily infected by echinostome trematodes, cockles lose their ability to burrow and simply lie at the sediment surface (left). Echinostome metacercariae accumulate in a cockle's foot until its function is impaired. This has major implications for the benthic community, because surfaced cockles alter habitat properties such as sedimentation rates and availability of hard substrate, with consequences for other organisms. There may also be effects on other parasites living in cockles, such as the copepod Pseudomyicola spinosus (right).

The acanthocephalan Acanthocephalus galaxii is a common
intestinal parasite of New Zealand freshwater fishes, but is very
rare among amphipod intermediate hosts. Can it alter amphipod
behaviour in ways that increase its transmission success to fish?

Manipulation of host phenotype by parasites: Numerous taxa of parasites are capable of modifying the appearance or behaviour of their host in ways that increase the probability that the parasites will achieve transmission and complete their life cycle. Larval helminths that must pass from an intermediate host (prey) to a definitive host (predator) via the food chain are notorious for their abilities to enhance their host's susceptibility to predation, though parasites with other transmission modes are also capable of host manipulation. Our current interests focus on two aspects of this phenomenon. First, we are trying to identify the physiological and/or neurological mechanisms underlying behavioural alterations in parasitized hosts, and are also looking at altered gene expression within an epigenetic framework. Second, we are testing the possibility that interactions may exist among manipulative parasites that share an intermediate host. For example, one parasite can benefit from the investment in manipulation made by a second parasite if they both have the same definitive host, possibly favouring the evolution of a hitch-hiking strategy. These possibilities are explored using experimental infections in which the intensity and genetic identity of parasite clones used can be manipulated. [Poulin, Joe]

Encapsulated (melanized) metacercariae of Maritrema
novaezealandensis in a resistant amphipod. The
metacercariae are visible as three reddish dots through
the amphipod's exoskeleton; they were killed by the host
immune system following penetration.

Geographical variation and local adaptation in parasites: Different populations of the same host species experience different levels of infection, and are also exploited by different parasite species. We investigate the factors responsible for these spatial patterns in parasitism. Also, immunity to infection comes at a cost: any energy allocated to fighting parasites is unavailable for other functions, such as reproduction. We thus expect natural selection to optimize investments in immunity such that they reflect actual exposure to parasites: if infection is likely, greater immunity should be favoured, and vice versa. We are comparing the ability of crustaceans from different populations to resist infection by parasites, to determine whether individuals from areas where parasites are absent are more susceptible to infection and less capable of an immune response than those from populations facing high levels of parasitism. [Poulin, O'Dwyer]

Macroecology and biogeography of parasitism: Large-scale ecological patterns are the outcome of both evolutionary processes and historical biogeographical events. The way in which parasite species within any given taxon are distributed among host species or among geographical areas reflect the action of these forces, and these distribution patterns can shed light on which force has played the most important role in shaping parasitism in natural systems. Using large databases on host-parasite associations, and a range of phylogenetic, biogeographical and macroecological approaches, we search for emergent patterns in parasite ecology. In particular, we have recently investigated global patterns in parasite biodiversity, as well as patterns of parasite specialization in host-parasite networks. The taxa we investigate range from helminths in fish to fleas on mammals. Our findings are casting a new light on the general importance of parasitism as a component of complex ecological systems. [Poulin, O'Dwyer]

Molecular systematics and coevolution of cestodes and elasmobranchs: Host and parasite phylogenetic hypotheses provide ecological and historical insights into the evolution of host and parasite associations. Conversely, host and parasite ecological data can provide insights into phylogenetic relationships. Lack of facts, at either end, hampers our knowledge of the evolutionary ecology of parasites. For instance, tetraphyllidean plerocercoids and merocercoids (larval stages) have been reported from arthropods, cetaceans, chaetognaths, ctenophores, echinoderms, echiurans, molluscs, nemerteans, and teleost fishes. However, no complete tetraphyllidean life cycle has been elucidated to date. Our inability to accurately identify these larval stages to species in intermediate or paratenic (non-obligate) hosts, due to the absence of descriptive characters, has made it difficult to link these to their adult forms. However, the advent of molecular tools has rendered the identification of larvae possible using a phylogenetic approach. This approach is of little use in the absence of knowledge about the tetraphyllidean fauna of the final hosts. Rajid skates are known to harbour a diverse assemblage of tetraphyllideans, often comprising echeneibothriine cestodes. Fewer than 50 of 236 rajid skate species have been sampled for parasites, including <10% in many genera; therefore, leaving important gaps in our knowledge of the ecology and phylogenetics of echeneibothriine cestodes. The objectives of this study are to: (1) identify the tetraphyllidean fauna from rajid skates in the southern hemisphere; (2) reconstruct a molecular phylogeny for tetraphyllideans, with particular emphasis on echeneibothriines; (3) identify potential intermediate hosts from stomach contents of rajid skates; (4) assign accurately to species the various larval stages collected during our sampling; (5) assess the degree of cospeciation of echeneibothriines with their intermediate and final hosts; and (6) study the evolution of the complex life cycle of echeneibothriine cestodes. The proposed work will not only provide insights into the life cycles of tetraphyllideans, but it will also shed light on the processes shaping their evolution. [Randhawa]

Scanning electron micrograph of the scolex of Pseudanthobothrium purtoni (Cestoda: Tetraphyllidea: Phyllobothriidae: Echeneibothriinae) (left).  Light micrograph of terminal proglottis of P. purtoni, depicting some of the reproductive characters used for species identification in echeneibothriine cestodes (middle). V, Vitelline follicle; T, Testis; U, Uterus; ga, Genital atrium; cp, Cirrus pouch; O, Ovary.  Photo of rajid skate (right): typical host for echeneibothriine cestodes.