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.
Biological control is a valuable and effective strategy for controlling arthropod pests and has been used extensively against invasive arthropods. As one approach for control of invasives, exotic natural enemies from the native range of a pest are introduced to areas where control is needed. Classical biological control began to be used in the late 1800s and its use increased until, beginning in 1983, scientists began raising significant concerns and questions about nontarget and indirect effects that can be caused by these introductions. In recent years, similar issues have been raised about augmentative use of exotic natural enemies. Subsequently, international guidelines, national regulations and scientific methods being used for exotic natural enemies in biological control have changed to require appropriate specificity testing, risk assessment and regulatory oversight before exotic natural enemies can be released. National and international standards aimed at minimizing risk have increased awareness and promoted more careful consideration of the costs and benefits associated with biological control. The barriers to the implementation of classical and augmentative biological control with exotic natural enemies now are sometimes difficult and, as a consequence, the numbers of classical biological control programs and releases have decreased significantly. Based in part on this new, more careful approach, classical biological control programs more recently undertaken are increasingly aimed at controlling especially damaging invasive arthropod pests that otherwise cannot be controlled. We examine evidence for these revised procedures and regulations aimed at increasing success and minimizing risk. We also discuss limitations linked to the apparent paucity of post-introduction monitoring and inherent unpredictability of indirect effects.
The mutualism between siricid woodwasps and Amylostereum fungal symbionts has long been considered to be species-specific. Recent studies from North America have challenged this assumption, where native siricids and the introduced Sirex noctilio are clearly swapping symbionts. Whether this pattern is a consequence of invasion or an underappreciated property of siricid biology is unknown. Here we show that the native Japanese siricid, Sirex nitobei, carries both Amylostereum areolatum and Amylostereum chailletii, rather than only A. areolatum as long assumed. Furthermore, all samples from a Urocerus sp. unexpectedly carried, A. chailletii and not Amylostereum laevigatum. Vegetative compatibility group tests revealed extensive clonality, with one VCG present amongst three A. areolatum isolates and six VCGs present amongst 61 A. chailletii isolates. These results contribute to the understanding of insect-fungal fidelity in the siricid-Amylostereum association and, together with other studies, suggest that host tree influences Amylostereum species occurrence, perhaps more strongly than wasps.
During the first half of the twentieth century, two accidental cases of introduction of Pissodes weevils were recorded from the southern hemisphere. The weevils in South Africa were identified as the deodar weevil (Pissodes nemorensis) and those in South America as the small banded pine weevil (Pissodes castaneus). Wide distribution of the two species in their invasive range, general difficulty in identifying some Pissodes spp., and the varying feeding and breeding behaviours of the species in South Africa has necessitated better evidence of species identity and genetic diversity of both species and population structure of the species in South Africa. Barcoding and the Jerry-to-Pat region of the COI gene were investigated. Morphometric data of the South African species was analysed. Our results confirmed the introduction of only one Pissodes species of North American origin to South Africa. However, this species is not P. nemorensis, but an unrecognized species of the P. strobi complex or a hybrid between P. strobi and P. nemorensis. Only P. castaneus, of European origin, was identified from South America. We identified ten mitochondrial DNA haplotypes from South Africa with evidence of moderate genetic structure among geographic populations. Terminal leader and bole-feeding weevils did not differ at the COI locus. A single haplotype was identified from populations of P. castaneus in South America. Results of the present study will have implications on quarantine, research and management of these insect species.
Some of the most devastating diseases of trees involve associations between forest insects and microorganisms. Although a small number of native insect-microorganism symbioses can cause tree mortality, the majority of associations with tree health implications involve one or more exotic organisms. Here, we divide damaging symbioses between forest insects and microorganisms into four categories based on the native/exotic status of the species involved: (1) insect and microorganism are native; (2) insect is native, microorganism is exotic; (3) insect is exotic, microorganism is native; and (4) insect and microorganism are both exotic. For each category, we describe several well-researched examples of forest insect symbioses and discuss some of the consequences of the types of interactions within each category. We then discuss priorities for research on forest insect symbioses that could help to further elucidate patterns in the complexity of such interactions in the context of invasion biology. We argue that a nuanced understanding of insect-pathogen relationships is lacking, even for the few well-studied examples. Because novel associations between insects, microorganisms, and trees are increasing with globalization, such symbioses and their potential to negatively impact forest ecosystems demand focused research in the future.
Climate change affects the rate of insect invasions as well as the abundance, distribution and impacts of such invasions on a global scale. Among the principal analytical approaches to predicting and understanding future impacts of biological invasions are Species Distribution Models (SDMs), typically in the form of correlative Ecological Niche Models (ENMs). An underlying assumption of ENMs is that species–environment relationships remain preserved during extrapolations in space and time, although this is widely criticised. The semi-mechanistic modelling platform, CLIMEX, employs a top-down approach using species ecophysiological traits and is able to avoid some of the issues of extrapolation, making it highly applicable to investigating biological invasions in the context of climate change. The tephritid fruit flies (Diptera: Tephritidae) comprise some of the most successful invasive species and serious economic pests around the world. Here we project 12 tephritid species CLIMEX models into future climate scenarios to examine overall patterns of climate suitability and forecast potential distributional changes for this group. We further compare the aggregate response of the group against species-specific responses. We then consider additional drivers of biological invasions to examine how invasion potential is influenced by climate, fruit production and trade indices. Considering the group of tephritid species examined here, climate change is predicted to decrease global climate suitability and to shift the cumulative distribution poleward. However, when examining species-level patterns, the predominant directionality of range shifts for 11 of the 12 species is eastward. Most notably, management will need to consider regional changes in fruit fly species invasion potential where high fruit production, trade indices and predicted distributions of these flies overlap.
Globalization is triggering an increase in the establishment of alien insects in Europe, with several species having substantial ecological and economic impacts. We investigated long-term changes in rates of species spread following establishment. We used the total area of countries invaded by 1171 insect species for which the date of first record in Europe is known, to estimate their current range radius (calculated as [invaded area]0.5/π). We estimated initial rates of radial spread and compared them among different groups of insects for all years (1800–2014) and for a subset of more recent decades (1950–2014). Accidentally introduced species spread faster than intentionally introduced species. Considering the whole period 1800–2014, spread patterns also differ between feeding guilds, with decreasing spread rates over residence time in herbivores but not in detritivores or parasitic species. These decreases for herbivorous species appeared mainly in those associated with herbaceous plants and crops rather than woody plants. Initial spread rate was significantly greater for species detected after 1990, roughly 3–4 times higher than for species that arrived earlier. We hypothesize that the political changes in Europe following the collapse of the Iron Curtain in 1989, and the further dismantling of customs checkpoints within an enlarged European Union (EU) have facilitated the faster spread of alien insect species. Also, the number of species first recorded in the Eastern Bloc of the politically-divided Europe before 1989 was lower than for the rest of Europe. A detailed analysis of six recent invaders indicated a dominant role of long-distance translocations related to human activities, especially with the plant trade, in determining rates of spread.
Thaumastocoris peregrinus is a sap-sucking insect that infests non-native Eucalyptus plantations in Africa, New Zealand, South America and parts of Southern Europe, in addition to street trees in parts of its native range of Australia. In South Africa, pronounced fluctuations in the population densities have been observed. To characterise spatiotemporal variability in T. peregrinus abundance and the factors that might influence it, we monitored adult population densities at six sites in the main eucalypt growing regions of South Africa. At each site, twenty yellow sticky traps were monitored weekly for 30 months, together with climatic data. We also characterised the influence of temperature on growth and survival experimentally and used this to model how temperature may influence population dynamics. T. peregrinus was present throughout the year at all sites, with annual site-specific peaks in abundance. Peaks occurred during autumn (February-April) for the Pretoria site, summer (November-January) for the Zululand site and spring (August-October) for the Tzaneen, Sabie and Piet Retief monitoring sites. Temperature (both experimental and field-collected), humidity and rainfall were mostly weakly, or not at all, associated with population fluctuations. It is clear that a complex interaction of these and other factors (e.g. host quality) influence population fluctuations in an annual, site specific cycle. The results obtained not only provide insights into the biology of T. peregrinus, but will also be important for future planning of monitoring and control programs using semiochemicals, chemical insecticides or biological control agents.
Exotic ants have become invasive in many regions around the world, with variable ecological impacts. Postinvasion, native ant communities are often found to be depauperate, though the causes of this apparent lack of coexistence are rarely well known. Myrmica rubra (L.), a Palearctic Myrmecine ant, is currently expanding its range as an invasive in North America. This aggressive ant forms dense, patchy local infestations and appears to aggressively displace native ant fauna. We measured behavioral interactions and rates of recruitment in experimental field assays pitting native foragers against captive colonies of M. rubra at tuna-jelly or aphid baits in uninfested areas of Mt. Desert Island, ME. Behavioral interactions were idiosyncratic with respect to the native opponent, but M. rubra generally showed significantly higher levels of recruitment, aggression, and displacement of native foragers. As with other invasive ant species shown to have broken the "dominance-discovery trade-off," M. rubra was consistently faster to discover baits and disproportionately displaced native foragers, providing a plausible proximate mechanism for native ant exclusion. Finally, we surveyed ant recruitment at baits for 24 h in August 2004 at four sites with varying M. rubra abundance but found little evidence of temporal niche partitioning. Taken together, these results indicate competitive superiority by M. rubra with respect to native ant communities of the northeastern North America and suggest direct aggression and competitive exclusion at food resources can lead to local native displacement.
The frequency of introductions of non-indigenous forest insects into new habitats is increasing worldwide, often with profoundly adverse consequences on natural and plantation forest ecosystems. Understanding rates and patterns of spread of invasive forest insects is important for predicting when and where these species will expand their geographical range, with the potential to improve mitigation strategies. The woodwasp Sirex noctilio is a damaging invasive forest insect that kills numerous species of Pinus. Despite encountering highly variable eco-climatic conditions, S. noctilio has arrived and established in exotic pine forest production areas throughout the Southern Hemisphere. In this study, we compiled historical records of S. noctilio invasion to compare spread rates among eight contrasting eco-climatic regions in the Southern Hemisphere and to explore how spread rate is predicted by landscape variation in climate, habitat characteristics and anthropogenic effects. Spread rates for S. noctilio varied considerably among the invaded regions, ranging from 12 to 82 km per year. Among regions, spread rates of S. noctilio increased with increasing mean annual temperature and isothermality. We hypothesize that temperature may directly or indirectly influence S. noctilio population growth and dispersal, thereby influencing spread rates.
Cleruchoides noackae Lin and Huber (Hymenoptera: Mymaridae) is a solitary egg parasitoid of Thaumastocoris peregrinus Carpintero and Dellapé (Hemiptera: Thaumastocoridae). The parasitoid was first described in 2009 and its biology and rearing are poorly understood. A key obstacle to the use of C. noackae as a biological control agent has been the ability to consistently rear it under quarantine conditions. This study reports on a series of experiments conducted in quarantine to rear C. noackae and to examine the effects of diet on longevity, per capita reproduction, and progeny sex ratio, as well as to determine development time, and preference and suitability of host eggs of different ages. When supplemented with honey solution, the longevity of C. noackae females increased significantly by 2.4 d and that of males by 1.7 d, relative to the unfed adults. Mean per capita reproduction for the honey-fed wasps was 7.7 offspring per female, with progeny sex ratio slightly skewed toward males. Mean percentage parasitism was 32.2%. C. noackae was capable of parasitizing and completing development from oviposition to adult eclosion within 15.7 d in host eggs between 0 and 5 d old. The ability of C. noackae to parasitize a wide range of host egg ages increases the period of vulnerability of T. peregrinus to attack, increasing its potential efficacy as a biological control agent. The methods and results reported here represent a crucial step in the ongoing efforts to develop this potential biological control system.
1. Spatial pattern in the distribution and abundance of organisms is an emergent property of collective rates of reproduction, survival and movement of individuals in a heterogeneous environment. 2. The form, intensity and scale of spatial patterning can be used to test hypotheses regarding the relative importance of candidate processes to population dynamics. 3. Using 84 plots across eastern North America, we studied populations of twoassociated plant parasites, the invasive felted beech scale Cryptococcus fagisuga Lind. and the native Neonectria fungi, which together cause beech bark disease (BBD). 4. We evaluated spatial patterns at the scales of trees within stands, stands within the forest and forests within the landscape to examine four hypothetically important factors in the ecology of the disease: (i) local contagion within stands; (ii) regional contagion, or among patch infection–reinfection dynamics; (iii) variation in host susceptibility linked to genetic and/or environmental heterogeneity; and (iv) climate effects on population growth of BBD organisms.5 Analyses revealed an unexpected lack of spatial aggregation in BBD populations among trees, stands and forests. This implies that propagule pressure is generally sufficiently high throughout the infested region of North America such that neither trees nor stands are spared from the disease by dispersal limitations of the disease agents. Furthermore, variation in tree and stand level susceptibility has minimal impact on BBD dynamics and climate is not a conspicuous driver of abundance within the core range of BBD.
The Kingdom Fungi adds substantially to the diversity of life, but due to their cryptic morphology and lifestyle, tremendous diversity, paucity of formally described specimens, and the difficulty in isolating environmental strains into culture, fungal communities are difficult to characterize. This is especially true for endophytic communities of fungi living in healthy plant tissue. The developments in next generation sequencing technologies are, however, starting to reveal the true extent of fungal diversity. One of the promising new technologies, namely semiconductor sequencing, has thus far not been used in fungal diversity assessments. In this study we sequenced the internal transcribed spacer 1 (ITS1) nuclear encoded ribosomal RNA of the endophytic community of the economically important tree, Eucalyptus grandis, from South Africa using the Ion Torrent Personal Genome Machine (PGM). We determined the impact of various analysis parameters on the interpretation of the results, namely different sequence quality parameter settings, different sequence similarity cutoffs for clustering and filtering of databases for removal of sequences with incomplete taxonomy. Sequence similarity cutoff values only had a marginal effect on the identified family numbers, whereas different sequence quality filters had a large effect (89 vs. 48 families between least and most stringent filters). Database filtering had a small, but statistically significant, effect on the assignment of sequences to reference sequences. The community was dominated by Ascomycota, and particularly by families in the Dothidiomycetes that harbor well-known plant pathogens. The study demonstrates that semiconductor sequencing is an ideal strategy for environmental sequencing of fungal communities. It also highlights some potential pitfalls in subsequent data analyses when using a technology with relatively short read lengths.
Symbiont fidelity is an important mechanism in the evolution and stability of mutualisms. Strict fidelity has been assumed for the obligate mutualism between Sirex woodwasps and their mutualistic Amylostereum fungi. This assumption has been challenged in North America where the European woodwasp, Sirex noctilio, and its fungal mutualist, Amylostereum areolatum, have recently been introduced. We investigate the specificity of the mutualism between Sirex and Amylostereum species in Canada, where S. noctilio co-infests Pinus with native Sirex nigricornis and its mutualist, Amylostereum chailletii. Using phylogenetic and culture methods, we show that extensive, reciprocal exchange of fungal species and strains is occurring, with 75.3 per cent of S. nigricornis carrying A. areolatum and 3.5 per cent of S. noctilio carrying A. chailletii. These findings show that the apparent specificity of the mutualism between Sirex spp. and their associated Amylostereum spp. is not the result of specific biological mechanisms that maintain symbiont fidelity. Rather, partner switching may be common when shifting geographical distributions driven by ecological or anthropogenic forces bring host and mutualist pairs into sympatry. Such novel associations have potentially profound consequences for fitness and virulence. Symbiont sharing, if it occurs commonly, may represent an important but overlooked mechanism of community change linked to biological invasions.
1. Two cossid moths, Coryphodema tristis Drury and Chilecomadia valdiviana Philippi, have recently become pests on Eucalyptus nitens H. Deane & Maiden in South Africa and Chile, respectively. Both C. tristis and C. valdiviana have large host ranges and high levels of similarity in their host distributions. Their infestations of E. nitens are the first records of these moths on Myrtaceae. 2. The contemporaneous adoption of E. nitens as a novel host, despite widespread availability of native and introduced Myrtaceae, suggests a non-random pattern of invasion. Phylogenetic relatedness among the two species linked to cryptic invasion of one or both moths at some time in the recent past provides a possible explanation for this pattern. 3. To test this hypothesis, variation in mtDNA sequences for the COI gene of C. tristis and C. valdiviana were analyzed. The COI mtDNA sequence data showed that C. tristis and C. valdiviana are highly divergent genetically, indicating that both are native on their respective continents with independent evolutionary trajectories. 4. The parallel host range expansions to E. nitens on different continents appear to be unrelated events, likely driven by characteristics of the biology and/or ecology of the host.
The worldwide homogenization of genetic resources used in plantation forestry (primarily Pinus, Eucalypus, Populus and Acacia spp.) together with accelerating rates of human-aided dispersal of exotic pests, is resulting in plantation pests becoming broadly distributed extremely quickly, sometimes reaching a global distribution within a decade. This unprecedented rate of establishment and spread means that the risk associated with new and emerging pests is shared globally. Biological control represents a major component of the strategy to mitigate such risk, but the current efforts and scope for developing such controls are woefully inadequate for dealing with the increasing rates of pest spread. Given the global nature of the problem, biological control would benefit enormously from an international, collaborative focus. Though inherent difficulties and potential pitfalls exist, opportunities for cost-sharing, growth and maintenance of resources and capacity, and more comprehensive research programmes are critical to the long-term success of biological control. Governments and industries will need to increase their strategic investment in structures specifically designed to promote such focus if they are to successfully protect their forest resources.