The ecology and evolution of invasive Potamopyrgus antipodarum in Australia

The spread of invasive organisms is one of the greatest threats to ecosystems and biodiversity worldwide. Understanding the evolutionary and ecological factors responsible for the transport, introduction, establishment and spread of invasive species will assist the development of control strategies. The New Zealand mudsnail, Potamopyrgus antipodarum (Gray 1843) (Gastropoda: Hydrobiidae), is a global freshwater invader, with populations established in Europe, Asia, the Americas and Australia. While sexual and asexual P. antipodarum coexist in the native range, invasive populations reproduce by parthenogenesis, producing dense populations that compete for resources with native species. Potamopyrgus antipodarum is a natural model system for the study of evolutionary and ecological processes underlying invasion. This thesis assesses the invasion history, genetic diversity and ecology of P. antipodarum in Australia, with particular focus on: a) potential source populations, b) distribution and structure of populations, and c) species traits related to the establishment, persistence and spread of invasive P. antipodarum. Genetic analyses were carried out on specimens collected for this study from New Zealand and Australia, along with existing museum samples. In combination with published data, the analyses revealed low genetic diversity among and within invasive populations in south-eastern Australia, relative to New Zealand populations. Phylogenetic relationships inferred from mitochondrial sequences indicated that the Australian populations belong to clades dominated by parthenogenetic haplotypes that are known to be present in Europe and the US. These ‘invasive clades’ are likely to originate from the North Island of New Zealand, and suggest a role for selection in determining genetic composition of invasive populations. The genotypic diversity of Australian P. antipodarum was low, with few, closely related clones distributed across south-eastern Australia. The pattern of clone distribution was not consistent with any assessed geographical or abiotic factors; instead a few, widely-distributed clones were present in high frequencies at most sites. Differences in clone frequencies were found, which may indicate differential success of clonal lineages. A range of traits have been proposed as facilitators of invasion success, and within-species variation in these traits can promote differential success of genotypes. Using laboratory-based experiments, the performance of the three most common Australian clones was tested across a suite of invasion-relevant traits. Ecologically-relevant variation in traits was found among the clones. These differences may have determined the spatial distribution of clones, and may continue to do so into the future. This thesis found that the P. antipodarum invasion of Australia is the result of few introductions of a small number of globally-invasive genotypes that vary in ecologically-relevant traits. From a source of considerable genetic diversity in the native range, very few genotypes have become invasive. Those that are invasive appear to be very successful at continental scales. These findings highlight a capacity in asexual invaders to successfully invade, and potentially adapt to, a broad range of ecosystems. The P. antipodarum invasion system is amenable to research using combinations of field-based studies, molecular and laboratory approaches, and is likely to yield significant, broadly-applicable insights into invasion.

Distribution of an alien aquatic snail in relation to flow variability, human activities and water quality

1. Disturbance and anthropogenic land use changes are usually considered to be key factors facilitating biological invasions. However, specific comparisons of invasion success between sites affected to different degrees by these factors are rare.

2. In this study we related the large-scale distribution of the invading New Zealand mud snail (Potamopyrgus antipodarum) in southern Victorian streams, Australia, to anthropogenic land use, flow variability, water quality and distance from the site to the sea along the stream channel.

3. The presence of P. antipodarum was positively related to an index of flow-driven disturbance, the coefficient of variability of mean daily flows for the year prior to the study.

4. Furthermore, we found that the invader was more likely to occur at sites with multiple land uses in the catchment, in the forms of grazing, forestry and anthropogenic developments (e.g. towns and dams), compared with sites with low-impact activities in the catchment. However, this relationship was confounded by a higher likelihood of finding this snail in lowland sites close to the sea.

5. We conclude that P. antipodarum could potentially be found worldwide at sites with similar ecological characteristics. We hypothesise that its success as an invader may be related to an ability to quickly re-colonise denuded areas and that population abundances may respond to increased food resources. Disturbances could facilitate this invader by creating spaces for colonisation (e.g. a possible consequence of floods) or changing resource levels (e.g. increased nutrient levels in streams with intense human land use in their catchments).

Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds

Many plant seeds and invertebrates can survive passage through the digestive system of birds, which may lead to long distance dispersal (endozoochory) in case of prolonged retention by moving vectors. Endozoochorous dispersal by waterbirds has nowadays been documented for many aquatic plant seeds, algae and dormant life stages of aquatic invertebrates. Anecdotal information indicates that endozoochory is also possible for fully functional, active aquatic organisms, a phenomenon that we here address experimentally using aquatic snails. We fed four species of aquatic snails to mallards (Anas platyrhynchos), and monitored snail retrieval and survival over time. One of the snail species tested was found to survive passage through the digestive tract of mallards as fully functional adults. Hydrobia (Peringia) ulvae survived up to five hours in the digestive tract. This suggests a maximum potential transport distance of up to 300 km may be possible if these snails are taken by flying birds, although the actual dispersal distance greatly depends on additional factors such as the behavior of the vectors. We put forward that more organisms that acquired traits for survival in stochastic environments such as wetlands, but not specifically adapted for endozoochory, may be sufficiently equipped to successfully pass a bird's digestive system. This may be explained by a digestive trade-off in birds, which maximize their net energy intake rate rather than digestive efficiency, since higher efficiency comes with the cost of prolonged retention times and hence reduces food intake. The resulting lower digestive efficiency allows species like aquatic snails, and potentially other fully functional organisms without obvious dispersal adaptations, to be transported internally. Adopting this view, endozoochorous dispersal may be more common than up to now thought.

Macroinvertebrate abundance and proportion of trait categories in river biotopes across England and Wales

There is a long tradition of river monitoring using macroinvertebrate communities to assess environmental quality in Europe. A promising alternative is the use of species life-history traits. Both methods, however, have relied on the time-consuming identification of taxa. River biotopes, 1-100 m**2 'habitats' with associated species assemblages, have long been seen as a useful and meaningful way of linking the ecology of macroinvertebrates and river hydro-morphology and can be used to assess hydro-morphological degradation in rivers. Taxonomic differences, however, between different rivers had prevented a general test of this concept until now. The species trait approach may overcome this obstacle across broad geographical areas, using biotopes as the hydro-morphological units which have characteristic species trait assemblages. We collected macroinvertebrate data from 512 discrete patches, comprising 13 river biotopes, from seven rivers in England and Wales. The aim was to test whether river biotopes were better predictors of macroinvertebrate trait profiles than taxonomic composition (genera, families, orders) in rivers, independently of the phylogenetic effects and catchment scale characteristics (i.e. hydrology, geography and land cover). We also tested whether species richness and diversity were better related to biotopes than to rivers. River biotopes explained 40% of the variance in macroinvertebrate trait profiles across the rivers, largely independently of catchment characteristics. There was a strong phylogenetic signature, however. River biotopes were about 50% better at predicting macroinvertebrate trait profiles than taxonomic composition across rivers, no matter which taxonomic resolution was used. River biotopes were better than river identity at explaining the variability in taxonomic richness and diversity (40% and <=10%, respectively). Detailed trait-biotope associations agreed with independent a priori predictions relating trait categories to near river bed flows. Hence, species traits provided a much needed mechanistic understanding and predictive ability across a broad geographical area. We show that integration of the multiple biological trait approach with river biotopes at the interface between ecology and hydro-morphology provides a wealth of new information and potential applications for river science and management.