Jeffrey T. Wright

Chemical defense in a marine alga: heritability and the potential for selection by herbivores

Herbivores have major impacts on many marine algae and are assumed to have been important forces driving the evolution of algal chemical defenses. However, an evolutionary change in chemical defenses in response to herbivory requires that there is both heritable variation for that trait and a response by herbivores to such variation. The subtidal red alga Delisea pulchra produces four main secondary metabolites (furanones) that vary in concentration at a variety of spatial and temporal scales. Here we determined the heritability of furanone concentrations and then, with a series of feeding experiments, determined how feeding by herbivores associated with D. pulchra varied as a function of nonpolar extract and furanone concentration. Total furanone concentration showed signif- icant broad-sense heritability (h 0.234), but broad-sense heritability of the four individual 2 C furanones varied in magnitude, ranging from 0.058 to 0.321. Compound 3, which is often the most abundant furanone, was the only one of the four furanones to show significant genetic variation. However, all four furanones were strongly genetically correlated, indi- cating that selection acting on any one of them will cause a corresponding change in the others. With the exception of the mesograzer gastropodPhasianotrochus eximius,herbivores generally consumed D. pulchra at lower rates compared to other common macroalgae. Macrograzers (sea urchins and large gastropods) were mostly deterred by nonpolar extract that contained levels of furanones that spanned the range of furanone variation in the field. The amphipod Ampithoe ngana was not deterred at the lowest extract concentration, and P. eximius was not deterred by any naturally occurring extract concentration. Compound 3 was deterrent to macrograzers at 3 and 5 mg/g dry mass, but was not deterrent at 1 mg/ g dry mass. Compound 3 was also not deterrent to A. ngana at any of those concentrations. For the most part D. pulchra in the field contains concentrations of furanones that are strongly deterrent to most herbivores. However, at some places and times, furanones do occur at lower concentrations that are not deterrent to herbivores. Given the heritable variation for furanones, when this overlap occurs there is the potential for selection by herbivores for higher concentrations of furanones in D. pulchra.

Behavioural interactions between ecosystem engineers control community species richness

Behavioural interactions between ecosystem engineers may strongly influence community structure. We tested whether an invasive ecosystem engineer, the alga Caulerpa taxifolia, indirectly facilitated community diversity by modifying the behaviour of a native ecosystem engineer, the clam Anadara trapezia, in southeastern Australia. In this study, clams in Caulerpa-invaded sediments partially unburied themselves, extending >30% of their shell surface above the sediment, providing rare, hard substrata for colonization. Consequently, clams in Caulerpa had significantly higher diversity and abundance of epibiota compared with clams in unvegetated sediments. To isolate the role of clam burial depth from direct habitat influences or differential predation by habitat, we manipulated clam burial depth, predator exposure and habitat (Caulerpa or unvegetated) in an orthogonal experiment. Burial depth overwhelmingly influenced epibiont species richness and abundance, resulting in a behaviourally mediated facilitation cascade. That Caulerpa controls epibiont communities by altering Anadara burial depths illustrates that even subtle behavioural responses of one ecosystem engineer to another can drive extensive community-wide facilitation.

Limited grazing pressure by native herbivores on the invasive seaweed Caulerpa taxifolia in a temperate Australian estuary

Caulerpa taxifolia is an invasive alga threatening biodiversity in invaded regions. Its proliferation in recipient communities will be due to several factors including limited grazing effects by native herbivores. However, little is known about grazing pressure exerted by native herbivores on C. taxifolia relative to native macrophytes or its attractiveness to them as habitat. The present study determined which herbivores co-occurred with invasive C. taxifolia in a temperate Australian estuary and documented their abundance, relative grazing effects, habitat preference and survivorship on C. taxifolia compared with native macrophytes. Four herbivores co-occurred with C. taxifolia and their densities were often low or zero at the sites studied. Feeding experiments showed that compared with C. taxifolia: the fish, Girella tricuspidata, preferred Ulva sp.; the sea-hare, Aplysia dactylomela, preferred Laurencia sp.; whereas the mesograzers, Cymadusa setosa and Platynereis dumerilii antipoda, both consumed Cystoseira trinodus and Sargassum sp. at higher rates. The two mesograzers also showed strong habitat preference for C. trinodus and Sargassum sp. Cymadusa setosa had poor survivorship on Caulerpa taxifolia whereas P. dumerilii antipoda had 100% survivorship on C. taxifolia after 41 days. We consider that the low diversity and abundance of native herbivores, their weak grazing pressure on C. taxifolia and its low attractiveness as habitat may facilitate further local spread in this estuary, and potentially in other invaded locations.

DEMOGRAPHIC FEEDBACK BETWEEN CLONAL GROWTH AND FRAGMENTATION IN AN INVASIVE SEAWEED

Many abundant plants, invertebrates, and seaweed are clonal, and this allows the formation of high-density aggregations, foraging, and the placement of modules into new space, and rapid rates of expansion. For these species, population density and rates of expansion are functions of recruitment of asexual modules and post-recruitment vegetative growth and survivorship. In this study, we provide the first experimental test of the relative importance of these two processes in determining the abundance of a clonal seaweed using Caulerpa taxifolia, an invasive green alga that spreads rapidly and reaches very high abundance. We asked two main questions: What is the relative importance to abundance (biomass) of vegetative stolon growth and fragment recruitment during expansion of established patches? Does greater fragment recruitment result in greater abundance in established patches? Vegetative growth of stolons underpinned patch expansion. Plots with stolons growing into them always had a greater abundance than plots where stolons were removed, even when fragment recruitment was increased. Greater recruitment only resulted in greater abundance when stolons were absent, a situation analogous to the establishment of new populations. Although post-recruitment processes were more important in determining abundance during patch expansion, there was greater ambient fragment recruitment when stolons were present compared to when they were absent, and as the abundance of C. taxifolia increased, demonstrating an important feedback between stolon growth, abundance, and fragment recruitment. In established patches, greater fragment recruitment over six months (six levels ranging from 0 to 480 recruits x m(-2) x mo(-1)) had no effect on biomass. Our experiments demonstrate that the rapid expansion and high abundance of invasive C. taxifolia are underpinned by post-recruitment vegetative growth and, during expansion, by a feedback between vegetative growth and asexual fragmentation.

POPULATION STRUCTURE AND PHYSIOLOGICAL DIFFERENTIATION OF HAPLOTYPES OF CALOGLOSSA LEPRIEURII (RHODOPHYTA) IN A MANGROVE INTERTIDAL ZONE

Zonation of macroalgae in the intertidal zone has been well documented. However, studies of zonation of macroalgae have predominantly examined the distribution of different species rather than the distribution of variants within a species. This study investigated the spatial variation of plastid haplotypes of the mangrove red alga Caloglossa leprieurii (Montagne) J. Agardh at a site in eastern Australia and tests for physiological differences (growth, photosynthesis) between those haplotypes. RUBISCO spacer plastid haplotypes were scored using single‐stranded comformational polymorphism, and the population structure at two sites was examined using a nested sampling design comparing between sites, among transects within sites, and among quadrats within transects. Growth rates at various salinities and light intensities and the photosynthesis–irradiance curves of the three main haplotypes were compared. The two sites showed a high degree of genetic differentiation across a short distance, suggesting limited gene flow. The distribution of haplotypes was patchy and did not reflect a zonation pattern along the intertidal gradient. The three haplotypes were physiologically differentiated with haplotype A, with a lower growth rate and a lower photosynthetic efficiency at higher light intensities. There is some evidence of physiological differentiation between life history phases in C. leprieurii with sporophytes having a higher growth rate than females under most conditions. Our results suggest a correlation between our culture results and our population data. Haplotypes (haplotype A) and life history phases (gametophytes) with lower performance (growth and photosynthetic efficiency) under our culture conditions were correlated with a minor representation in the field. This is the first study to integrate population‐level data with physiological parameters toward an understanding of the distribution and relative abundance of red algal genetic variants.

EFFECT OF VARIABLE RECRUITMENT AND POST-RECRUITMENT HERBIVORY ON LOCAL ABUNDANCE OF A MARINE ALGA

For marine algae, the relative importance of recruitment and post-recruitment processes in determining population abundance is not well understood. We documented patterns of recruitment and post-recruitment mortality for a common, clonally reproducing subtidal red alga from southeastern Australia, Delisea pulchra, and used a combination of empirical analyses and population simulations to assess the relative importance of the two processes to local population abundance. Using a hierarchical sampling design consisting of two depths and two spatial scales (quadrats and sites) within each depth, we followed monthly cohorts from recruitment to adulthood (6 mo of age). Recruitment of D. pulchra varied significantly in space and time and was generally decoupled from local adult abun- dance. Mortality was consistently high, particularly in the deep sites where only 1 of 291 plants survived >5 mo, and in the shallow sites when high densities of grazing sea urchins were present. Both early (1 mo) and late (6 mo) post-recruitment mortality of monthly cohorts were density independent at both spatial scales examined. Despite this pattern of mortality, variation in recruitment explained a significant amount of the subsequent variation in adult abundance in only 3 out of 10 cohorts at both spatial scales. This result indicates that high density-independent mortality was often important in determining adult abundance for individual cohorts. However, cumulative (across cohorts) recruitment into sites and quadrats over the entire study period explained a significant amount of the variation in the total number of plants that survived to reproduce there. Simulation models based on the measured demography of D. pulchra examined how the relative importance of recruitment and survivorship to population growth changed under two categories of sea urchin density: low ( 80 urchins/M2). These two categories represented the densities of sea urchins above and below a transition point where the mortality of D. pulchra went from being relatively low (17-33%/mo) to very high (63%/mo). When the effects of high densities of sea urchins were simulated, they caused a 95% decline in the population abundance of D. pulchra, compared to only a 31% decline when there were low densities of urchins. Significantly, the relative importance of recruitment and survivorship varied with sea urchin density: when there were high densities of sea urchins, population growth was more sensitive to increases in recruitment, whereas when there were low densities of urchins, survivorship was more important. Our findings demonstrate that the local popu- lation abundance of D. pulchra is determined by a combination of recruitment and density- independent mortality following recruitment, but it appears that the relative importance of the two processes varies in time and space.

Engineering or food? Mechanisms of facilitation by a habitat-forming invasive seaweed.

Nonnative species that form novel habitats strongly affect ecosystem processes. The effects of these ecosystem engineers can be both positive and negative but the mechanisms behind their effects are not well described. In this study we determined the relative importance of three main mechanisms by which invasive ecosystem engineers can facilitate native fauna. The engineer may provide new physical structure that reduces harsh abiotic conditions or gives refuge from predation (both engineering mechanisms), or provide a new profitable food resource (a trophic mechanism). The invasive seaweed Gracilaria vermiculophylla is a novel addition to estuarine intertidal mudflats of the southeastern United States. The epifaunal amphipod Gammarus mucronatus is up to 100 times more abundant on Gracilaria-invaded mudflats compared to uninvaded mudflats. Feeding assays, a survivorship experiment and stable isotope analysis demonstrated that Gammarus consumes little Gracilaria and cannot survive on Gracilaria alone. However, the structural engineering effects of Gracilaria greatly enhanced the survivorship of Gammarus in the presence of predators during high tide and when exposed to harsh abiotic conditions during low tide. Our results demonstrate that invasive ecosystem engineers can dramatically affect the distribution and abundance of native species by providing a novel protective structure.

A decline in the abundance and condition of a native bivalve associated with Caulerpa taxifolia invasion.

Caulerpa taxifolia is a fast-spreading invasive seaweed that threatens biodiversity in temperate Australian estuaries. To date, little is known about its effects on infauna. In the present study, we describe variation in demographic and life-history traits of the abundant infaunal bivalve, Anadara trapezia, in C. taxifolia and uninvaded habitats (seagrass and unvegetated sediments) at multiple sites across three estuaries in south-eastern New South Wales. Densities of A. trapezia were always lower in C. taxifolia than on unvegetated sediment, and lower in C. taxifolia than in seagrass at three out of four sites where they were compared. Dry tissue weight of A. trapezia was also lower in C. taxifolia than on unvegetated sediment at most sites, but was only lower in C. taxifolia than in seagrass at one of four sites. Populations were dominated by larger individuals (>45 mm length), but smaller individuals (35–45 mm length) were more common in C. taxifolia and seagrass. A. trapezia shell weight and morphology was variable and appeared weakly affected by invasion. Generally, our findings are consistent with the hypothesis that A. trapezia is negatively affected by C. taxifolia. However, C. taxifolia invasion appears complex and, at some places, its effects may not differ from those of native seagrass. There is a need for manipulative studies to understand the mechanisms underlying the effects of C. taxifolia on infauna.

Sublethal effects on reproduction in native fauna: are females more vulnerable to biological invasion?

Although invasive species are a major threat to survivorship of native species, we know little about their sublethal effects. In soft-sediment marine systems, mat-forming invasive species often have positive effects, facilitating recruitment and enhancing the diversity and abundance of native invertebrates. However, because mat-forming invasive species change the habitat in which they invade, and benthic invertebrates are sensitive to environmental disturbance, important sublethal effects on native species may exist. Using a model marine system we show that the widespread mat-forming invasive alga Caulerpa taxifolia (Vahl) C. Agardh has strong negative effects on the reproductive traits of a native bivalve Anadara trapezia (Deshayes, 1840) (e.g. timing of reproductive development and spawning, and follicle and gamete production) even though the invader has positive effects on recruitment. Moreover, gender specific responses occurred and indicated that females were more susceptible to invasion than males. Our results indicate that sublethal effects of an invasive species on reproductive traits will have severe consequences for fitness of the native species.

Vulnerabilities and adaptation of ports to climate change

Climate change is anticipated to have a significant impact on coastal infrastructure, including navigational aids and ports. This paper presents the results of a vulnerability assessment of ports in Australia to climate change. Results reveal variable vulnerability in ports in the short and long term in relation to their exposure to climate change. However, this is offset by inherent adaptive capacity both in current climate change initiatives driven by ports, and in the self-confidence of the industry to be able to adapt. We conclude with a reflection on the implications of these results for future ports analyses.