Invasive insects and pathogens are prominent tree mortality agents in forests around the world, and the magnitude of their impacts is increasing. Comparative studies across multiple populations can be helpful for the development of new insights and innovative management strategies. We used the Sirex woodwasp, Sirex noctilio Fabricius, as a model system to compare invasion impacts across a range of ecological contexts around the globe: native woodwasps colonizing native trees, invasive woodwasps in non-native plantation trees, and invasive woodwasps attacking native trees. Across 133 stands of eight pine species on four continents, tree mortality associated with S. noctilio attack was positively correlated with stand basal area and stand density, and was mostly confined to smaller, suppressed trees. Larger average tree size and greater distances between trees were linked to lower levels of tree mortality. To more deeply assess the impacts of tree loss due to this pest, we examined mortality in vigorous trees, defined as those with a stem diameter greater than or equal to 90% of the mean diameter for trees in the stand. Sirex noctilio- related mortality in vigorous trees was rare, with one exception where Pinus contorta stands in Argentina lost as many as 300 vigorous trees ha−1. Pine species varied dramatically in their susceptibility to S. noctilio: for example, these losses in P. contorta were in stark contrast to very low mortality in P. ponderosa, the other pine species grown in Argentina. Surprisingly, location did not alter patterns in the influence of stand basal area on tree susceptibility for individual species. Most notably, Pinus radiata had the same relationship between basal area and tree mortality when grown in Spain (where S. noctilio is native and not considered a meaningful forest pest) and South Africa (where S. noctilio is a problematic invasive). Our findings suggest that the availability of optimal pine hosts is a key driver of S. noctilio-related tree mortality across continents and management regimes. Important variables that influence host availability include species- specific susceptibility and environmental and management-related factors that promote or limit the number of stressed trees present both within stands and across the regional forest or plantation landscape.
Plant-pathogen interactions are often considered in a pairwise manner with minimal consideration of the impacts of the broader endophytic community on disease progression and/or outcomes for disease agents and hosts. Community interactions may be especially relevant in the context of disease complexes (i.e, interacting or functionally redundant causal agents) and decline diseases (where saprobes and weak pathogens synergize the effects of primary infections and hasten host mortality). Here we describe the bark endophyte communities associated with a widespread decline disease of American beech, beech bark disease (BBD), caused by an invasive scale insect (Cryptococcus fagisuga) and two fungal pathogens, Neonectria faginata and N. ditissima. We show that the two primary fungal disease agents co-occur more broadly than previously understood (35.5% of infected trees), including within the same 1-cm diameter phloem samples. The two species appear to have contrasting associations with climate and stages of tree decline, wherein N. faginata was associated with warmer and N. ditissima with cooler temperatures. Neonectria ditissima showed a positive association with tree crown dieback – no such association was observed for N. faginata. Further, we identify fungal endophytes that may modulate disease progression as entomopathogens, mycoparasites, saprotrophs and/or additional pathogens, including Clonostachys rosea and Fusarium babinda. These fungi may alter the trajectory of disease via feedbacks with the primary disease agents or by altering symptom expression or rates of tree decline across the range of BBD.
Resource quality can have direct or indirect effects on female oviposition choice, offspring growth and survival, and ultimately on body size and sex ratio. We examined these patterns in Sirex noctilio Fabricus, the globally invasive European pine woodwasp, in South African Pinus patula plantations. We studied how tree position as well as natural variation in biotic and abiotic factors influenced sex-specific density, larval size, tunnel length, male proportion, and survival across development. Twenty infested trees divided into top, middle, and bottom sections were sampled at three time points during larval development. We measured moisture content, bluestain fungal colonization, and co-occurring insect density and counted, measured, and sexed all immature wasps. A subset of larval tunnels was measured to assess tunnel length and resource use efficiency (tunnel length as a function of immature wasp size). Wasp density increased from the bottoms to the tops of trees for both males and females. However, the largest individuals and the longest tunnels were found in bottom sections. Male bias was strong (~10:1) and likewise differed among sections, with the highest proportion in the middle and top sections. Sex ratios became more strongly male biased due to high female mortality, especially in top and middle sections. Biotic and abiotic factors such as colonization by Diplodia sapinea, weevil (Pissodes sp.) density, and wood moisture explained modest residual variation in our primary mixed effects models (0%–22%). These findings contribute to a more comprehensive understanding of sex-specific resource quality for S. noctilio and of how variation in key biotic and abiotic factors can influence body size, sex ratio, and survival in this economically important woodwasp.
Neonectria ditissima and N. faginata are canker pathogens involved in an insect-fungus disease complex of American beech (Fagus grandifolia) commonly known as beech bark disease (BBD). In Europe, both N. ditissima and N. coccinea are involved in BBD on European beech (Fagus sylvatica). Field observations across the range of BBD indicate that new infections occur primarily via ascospores. Both heterothallic (self-sterile) and homothallic (self-fertile) mating strategies have been reported for Neonectria fungi. As such, investigations into mating strategy are important for understanding both the disease cycle and population genetics of Neonectria. This is particularly important in the U.S. given that over time N. faginata dominates the BBD pathosystem despite high densities of non-beech hosts for N. ditissima. This study utilized whole-genome sequences of BBD-associated Neonectria spp. along with other publicly available Neonectria and Corinectria genomes and in vitro mating assays to characterize mating type (MAT) loci and confirm thallism for select members of Neonectria and Corinectria. MAT gene-specific primer pairs were developed to efficiently characterize the mating types of additional single ascospore strains of N. ditissima, N. faginata, and N. coccinea and several other related species lacking genomic data. In vitro mating assays were used in combination with molecular results to confirm thallism. These assays also comfirmed the sexual compatibility among N. ditissima strains from different plant hosts. Maximum likelihood phylogenetic analysis of both MAT1-1-1 and MAT1-2-1 sequences recovered trees with similar topology to previously published phylogenies of Neonectria and Corinectria. The results of this study indicate that all Neonectria and Corinectria tested are heterothallic based on our limited sampling and, as such, thallism cannot help explain the inevitable dominance of N. faginata in the BBD pathosystem.
Insect pest invasions pose a major threat to agriculture, forestry and many natural ecosystems. Thaumastocoris peregrinus is an invasive sap-sucking pest of significant economic importance to Eucalyptus forestry that has recently invaded several countries worldwide. In this study we identify the origin and retrace the invasion history of T. peregrinus. We analysed samples from six locations in Africa, South America and Australia using microsatellites markers and a combination of clustering methods and scenario testing using Approximate Bayesian Clustering. We detected clear genetic substructure differentiating African and South American samples, with representatives of both present in Australia. The Australian population from New South Wales showed substantially higher genetic diversity than the Queensland source, which could indicate that this region could be part of the core range and evolutionary origin of the species. Africa and South America were colonised by independent introductions that occurred more or less concurrently. The study illustrates the impact of the bridgehead effect on global invasions following an outbreak or ‘invasion’ within a city in the native range of the insect.
Comprehensive understanding of the patterns and drivers of microbial diversity at a landscape scale is in its infancy, despite the recent ease by which soil communities can be characterized using massively parallel amplicon sequencing. Here we report on a comprehensive analysis of the drivers of diversity distribution and composition of the ecologically and economically important Phytophthora genus from 414 soil samples collected across Australia. We assessed 22 environmental and seven categorical variables as potential predictors of Phytophthora species richness, αandβ diversity, including both phylogenetically and non-phylogenically explicit methods. In addition, we classified each species as putatively native or introduced and examined the distribution with respect to putative origin. The two most widespread species, P. multivora and P. cinamomi, are introduced, though five of the ten most widely distributed species are putatively native. Introduced taxa comprised over 54% of Australia's Phytophthora diversity and these species are known pathogens of annual and perennial crop habitats as well as urban landscapes and forestry. Patterns of composition were most strongly predicted by bioregion (R2=0.29) and ecoregion (R2=0.26) identity; mean precipitation of warmest quarter, mean temperature of the wettest quarter and latitude were also highly significant and described approximately 21%, 14% and 13% of variation in NMDS composition, respectively. We also found statistically significant evidence for phylogenetic over-dispersion with respect to key climate variables.This study provides a strong baseline for understanding biogeographical patterns in this important genus as well the impact of key plant pathogens and invasive Phytophthora species in natural ecosystems.
The Botryosphaeriales, and in particular the Botryosphaeriaceae, are a well-studied group of fungi best known for the canker diseases they cause on woody hosts especially in stressed or damaged trees. Australian Plant Pathology herbaria contain many records for this group, but due to considerable taxonomic changes over the past decade, many of the species names have since been reclassified. In this article we used all published records with available sequence data of the Botryosphaeriaceae in Australia to examine the distribution and host range of these taxa. There are 24 genera encompassing 222 species in the Botryosphaeriaceae; 9 genera and 62 species have been recorded in Australia. Some genera such as Neoscytalidium are only found in warm, humid climates while Dothiorella species are more common in temperate climates. There were species, such as Lasiodiplodia theobromae, Neofusicoccum parvum and Botryosphaeria dothidea, which had a wide host range with many records. However, there were also several species found only in one location on a single host. While systematic data collection is still required, the information presented here provides a baseline of species present in Australia and will underpin future studies into this group of important pathogens.
Understanding how insects will respond both ecologically and evolutionarily to complex and interacting factors linked to global change is an important challenge that underpins our ability to produce better predictive models and to anticipate and manage ecosystem-scale disruption in the Anthropocene. Insects have the capacity to rapidly adapt to changing conditions via a variety of mechanisms which include both phenotypically plastic and evolutionary responses that interact in important ways. This short review comments on the current state of knowledge surrounding rapid evolution in insects and highlights conceptual and empirical gaps. Emphasis is placed on the need to consider direct and indirect community-level feedbacks via both ecological and evolutionary mechanisms when examining the consequences of global change, with particular focus on insects and their facultative and obligate symbionts.
1 The weevil Pissodessp. was first reported as an introduced pest on exotic Pinusspp. inSouthAfricain1942.ItisonlyrecentlythatthenativewaspPycnetronpixPrinsloo was described fromSouth Africaas a parasitoidof thisweevil. 2 We estimated the frequency and distribution of the association between P. pix and Pissodessp., as well as the occurrence of possible other natural enemies. Parasitoids were reared from Pissodes-infested Pinus radiata D. Don and Pinus patula Schiede ex Schltdl. & Cham logs collected frommajor Pinus-growing regions. 3 The identity of parasitoids was confirmed using morphological and molecular tech- niques. Parasitismwas confirmed by analyzing gut content sequences of parasitoids. 4 Pycnetron pix was found parasitizing Pissodes sp. throughout major Pinus-growing provinces of the country. Another native parasitoid, Cratocnema sp., is reported for the first time as a parasitoid of Pissodes sp. Rhopalicus tutela (Walker), a known parasitoid of Pissodes spp. in their native range, was also detected and confirmed to be ofEuropean origin. 5 Althoughcharacterizedbyanerraticdistributionandalowparasitismrate,anaccruing suite of natural enemies was documented, suggesting that there is potential for augmentative biological control of Pissodessp. inSouth Africa.
The introduction and subsequent impact of Phytophthora cinnamomi within native vegetation is one of the major conservation issues for biodiversity in Australia. Recently, many new Phytophthora species have been described from Australia’s native ecosystems; however, their distribution, origin, and potential impact remain unknown. Historical bias in Phytophthora detection has been towards sites showing symptoms of disease, and traditional isolation methods show variable effectiveness of detecting different Phytophthora species. However, we now have at our disposal new techniques based on the sampling of environmental DNA and metabarcoding through the use of high-throughput sequencing. Here, we report on the diversity and distribution of Phytophthora in Australia using metabarcoding of 640 soil samples and we compare the diversity detected using this technique with that available in curated databases. Phytophthora was detected in 65% of sites, and phylogenetic analysis revealed 68 distinct Phytophthora phylotypes. Of these, 21 were identified as potentially unique taxa and 25 were new detections in natural areas and/or new introductions to Australia. There are 66 Phytophthora taxa listed in Australian databases, 43 of which were also detected in this metabarcoding study. This study revealed high Phytophthora richness within native vegetation and the additional records provide a valuable baseline resource for future studies. Many of the Phytophthora species now uncovered in Australia’s native ecosystems are newly described and until more is known we need to be cautious with regard to the spread and conservation management of these new species in Australia’s unique ecosystems.
Traps designed to capture insects during normal movement/dispersal, or via attraction to non-specific (plant) volatile lures, yield by-catch that carries valuable information about patterns of community diversity and composition. In order to identify potential native/introduced pests and detect predictors of colonization of non-native pines, we examined beetle assemblages captured in intercept panel traps baited with kairomone lures used during a national monitoring of the woodwasp, Sirex noctilio, in Southern Africa. We identified 50 families and 436 morphospecies of beetles from nine sites sampled in both 2008 and 2009 and six areas in 2007 (trap catch pooled by region) across a latitudinal and elevational gradient. The most diverse groups were mainly those strongly associated with trees, known to include damaging pests. While native species dominated the samples in terms of richness, the dominant species was the introduced bark beetle Orthotomicus erosus (Curculionidae: Scolytinae) (22 +/- 34 individuals/site). Four Scolytinae species without previous records in South Africa, namely Coccotrypes niger, Hypocryphalus robustus (formerly Hypocryphalus mangiferae), Hypothenemus birmanus and Xyleborus perforans, were captured in low abundances. Communities showed temporal stability within sites and strong biogeographic patterns across the landscape. The strongest single predictors of community composition were potential evaporation, latitude and maximum relative humidity, while the strongest multifactor model contained elevation, potential evaporation and maximum relative humidity. Temperature, land use variables and distance to natural areas did not significantly correlate with community composition. Non-phytophagous beetles were also captured and were highly diverse (32 families) perhaps representing important beneficial insects.
Metacommunity theory offers a powerful framework to investigating the structure and dynamics of ecological communities. We use Ceratocystidaceae fungi as an empirical system to explore the potential of metacommunity principles to explain the incidence of putative fungal tree pathogens in natural ecosystems. The diversity of Ceratocystidaceae fungi was evaluated on elephant-damaged trees across the Kruger National Park of South Africa. Multivariate statistics were then used to assess the influence of landscapes, tree hosts and nitidulid beetle associates as well as isolation by distance on fungal community structure. Eight fungal and six beetle species were recovered on trees representing several plant genera. The distribution of Ceratocystidaceae fungi was highly heterogeneous across landscapes. Both tree host and nitidulid vector emerged as key factors contributing to this heterogeneity, while isolation by distance showed little influence. Our results are consistent with a model of metacommunity dynamics combining species sorting and patch dynamics processes.
The advent of simple and affordable tools for molecular identification of novel insect invaders and assessment of population diversity has changed the face of invasion biology in recent years. The widespread application of these tools has brought with it an emerging understanding that patterns in biogeography, introduction history and subsequent movement and spread of many invasive alien insects are far more complex than previously thought. We reviewed the literature and found that for a number of invasive insects, there is strong and growing evidence that multiple introductions, complex global movement, and population admixture in the invaded range are commonplace. Additionally, historical paradigms related to species and strain identities and origins of common invaders are in many cases being challenged. This has major consequences for our understanding of basic biology and ecology of invasive insects and impacts quarantine, management and biocontrol programs. In addition, we found that founder effects rarely limit fitness in invasive insects and may benefit populations (by purging harmful alleles or increasing additive genetic variance). Also, while phenotypic plasticity appears important post-establishment, genetic diversity in invasive insects is often higher than expected and increases over time via multiple introductions. Further, connectivity among disjunct regions of global invasive ranges is generally far higher than expected and is often asymmetric, with some populations contributing disproportionately to global spread. We argue that the role of connectivity in driving the ecology and evolution of introduced species with multiple invasive ranges has been historically underestimated and that such species are often best understood in a global context.
The success of a biological invasion is context dependent, and yet two key concepts—the invasiveness of species and the invasibility of recipient ecosystems—are often defined and considered separately. We propose a framework that can elucidate the complex relationship between invasibility and invasiveness. It is based on trait-mediated interactions between species and depicts the response of an ecological network to the intrusion of an alien species, drawing on the concept of community saturation. Here, invasiveness of an introduced species with a particular trait is measured by its per capita population growth rate when the initial propagule pressure of the introduced species is very low. The invasibility of the recipient habitat or ecosystem is dependent on the structure of the resident ecological network and is defined as the total width of an opportunity niche in the trait space susceptible to invasion. Invasibility is thus a measure of network instability. We also correlate invasibility with the asymptotic stability of resident ecological network, measured by the leading eigenvalue of the interaction matrix that depicts trait-based interaction intensity multiplied by encounter rate (a pairwise product of propagule pressure of all members in a community). We further examine the relationship between invasibility and network architecture, including network connectance, nestedness and modularity. We exemplify this framework with a trait-based assembly model under perturbations in ways to emulate fluctuating resources and random trait composition in ecological networks. The maximum invasiveness of a potential invader (greatest intrinsic population growth rate) was found to be positively correlated with invasibility of the recipient ecological network. Additionally, ecosystems with high network modularity and high ecological stability tend to exhibit high invasibility. Where quantitative data are lacking we propose using a qualitative interaction matrix of the ecological network perceived by a potential invader so that the structural network stability and invasibility can be estimated from the literature or from expert opinion. This approach links network structure, invasiveness and invasibility in the context of trait-mediated interactions, such as the invasion of insects into mutualistic and antagonistic networks.