Water, wing or wind? Spatial patterns of genetic variation reveal different dispersal and persistence mechanisms in large woody perennial plants of Australian dryland river systems

Abstract

<p>The preservation of plant biodiversity is a critical factor determining the resilience of dryland ecosystems. In Australia, large woody perennial plants of dryland river systems act as ecosystem engineers supporting a wide range of vital ecosystem functions and services at both local and landscape scales. Consisting of a small number of tree and long-lived shrubs, large woody perennial species in these environments are typically widespread and welladapted to the unpredictable occurrence of expansive floods and prolonged drought that are characteristic of Australian dryland rivers. Riparian and floodplain tree and shrub species currently sit high on the management agenda in these environments, particularly with respect to the allocation of environmental water. Understanding the mechanisms governing the persistence of these species in these highly variable and unpredictable environments is crucial for informing the development and prioritisation of effective management investments and interventions. </p> <p>Dispersal and gene flow are key processes influencing the persistence of species across numerous scales. For plants inhabiting environments that are highly variable over both temporal and spatial scales, dispersal through time, via dormancy, or through space, via the passive dispersal of propagules, provides a means of both avoiding habitat patches that are not conducive to survival and of reaching habitat patches that are favourable to growth and reproduction. Very little is currently known, however, regarding these critical processes amongst key woody perennial plant species of Australian dryland river floodplains.</p> <p>This thesis explores the dispersal, gene flow and genetic structure of two common large woody perennial species of Australian dryland rivers: <i>Duma florulenta</i> (Meisn.) T.M. Schust. (tangled lignum) and <i>Acacia stenophylla</i> cunn. Ex. Benth. (river cooba). Knowledge generated regarding these species is also integrated with that from previous studies to make inferences regarding variation in the ability of these species to persist in an environment subject to increasing environmental change.<i> Eucalyptus camaldulensis</i> Dehnh. was included in this last analysis so as to provide a broader spectrum of the different types of woody perennial plants in these systems (i.e. shrub, small tree, large tree).</p> <p>The research presented in this thesis utilised 454 next-generation sequencing to identify and validate a suite of 13 and 12 polymorphic microsatellite markers for <i>A. stenophylla</i> and <i>D. florulenta</i> respectively. Designed primers were found to amplify the microsatellite target regions sufficiently when tested on samples collected from three different rivers in the Murray-Darling Basin (The Darling, The Warrego and The Balonne). The polymorphic information content of the developed markers ranged from low to high (0.025 – 0.789) with both marker sets possessing moderate overall levels of polymorphic information content. Furthermore, the cumulative probability of falsely identifying multilocus genotypes was sufficiently low for both marker sets that they could confidently be used to separate individuals and identify clones (< 0.003 for both species). Thus, marker sets for <i>A. stenophylla</i> and <i>D. florulenta</i> were considered to provide sufficient levels of information for population genetic analysis providing a useful resource to study these ecologically important species for which genetic information is currently limited.</p> <p>Samples collected from 13 populations located on seven different rivers of the northern Murray-Darling Basin were subject to population genetic analyses using the newly developed sets of microsatellite markers. Although levels of genetic differentiation between subpopulations were small, contrasting patterns of spatial genetic variation were identified for each species. A large amount of the variation in pairwise genetic distances between subpopulations could be explained by a combination of river distance and the proportion of days without flow for <i>A. stenophylla</i>. On the other hand, a significant, but small, proportion of pairwise genetic differentiation in <i>D. florulenta</i> could be explained by distance along the river and straight-line geographic distance, although the percentage contribution of the latter was almost double that of the former in this case. In addition, patterns of genetic variation conformed to a stream hierarchy model for <i>A. stenophylla</i> with differences among river systems greater than differences between subpopulations within river systems. The opposite was true for <i>D. florulenta</i>, indicating that while dispersal and gene flow were largely restricted to the river corridor for <i>A. stenophylla</i>, overland dispersal was common in D. florulenta. Similarity between subpopulations on different rivers was largest for subpopulations that shared floodplains in <i>D. florulenta</i>. As a result, it was hypothesised that while hydrochory provides efficient dispersal along the river corridor for <i>A. stenophylla</i>, dispersal via hydrochory is most efficient across the floodplain for <i>D. florulenta</i>.</p> <p>As a result of a long history of human alteration, as well as their inherent biophysical characteristics, dryland and riparian systems are potentially vulnerable to the impacts of increasing pressure from water resource development and global climate change. Understanding how different plant attributes, such as dispersal capability, influence vulnerability and/or resilience to environmental change is important if we are to effectively manage and conserve these ecosystems into the future. The attributes of the two study species, as well as <i>E. camaldulensis</i>, were examined and the implications under projected climate change assessed. Despite commonly being treated as a single broad functional group, the large woody perennial plants in this study possess distinct survival strategies that help them persist in an environment subject to high levels of environmental change. <i>Acacia stenophylla</i> was designated as a ‘stationary persistent’ as a result of its tendency to persist through unfavourable conditions with little to no change to above ground biomass; <i>E. camaldulensis</i> was classified as a ‘fluctuating persistent’ given a limited ability to alter morphology and biomass in response to changing conditions; and <i>D. florulenta</i> a ‘perennial ephemoroid’ due to an ability to avoid unfavourable conditions by reverting to a dormant state before rapidly responding to favourable conditions on their return. </p> <p>Climate projections for Australian dryland rivers suggest overall drying is highly likely with an increase in the intensity of rainfall events as well as the duration of intervening droughts. Given the relatively high levels of gene flow and dispersal apparent in large woody perennial species of these systems, which is often facilitated by hydrochory, persistence of these species may be more heavily reliant on surviving the increasing periods of drought that separate large rainfall and flooding events than on efficient dispersal capabilities. This being the case, species with stationary persistent strategies such as <i>A. stenophylla</i> may be the most vulnerable to future climate change given their lack of flexibility in response to both unfavourable and favourable conditions. To protect these species, water management in these systems should focus on maintaining a minimum level of vigour in adult individuals through extended periods of drought in order to provide the best chance for successful reproduction and recruitment during large flow events.</p>