Figure 4 - uploaded by Ashley N. Schulz
Content may be subject to copyright.
Source publication
Understanding the successes and failures of nonnative species remains challenging. In recent decades, researchers have developed the enemy release hypothesis and other antagonist hypotheses, which posit that nonnative species either fail or succeed in a novel range because of the presence or absence of antagonists. The premise of classical biologic...
Contexts in source publication
Context 1
... our review of the literature, we propose a unifying framework that includes many of the most commonly cited antagonist hypotheses (table 1, figure 4) and could be updated as researchers develop new or discard existing hypotheses regarding the specific roles that antagonists play in the success or failure of biological invasions and biological control agents. Our simplified framework includes subhypotheses that fall under two categories: hypotheses concerning antagonists not inhibiting invasion and hypotheses concerning antagonists inhibiting invasion (figure 4). ...
Context 2
... if our end goal is to aid in the failure of nonnative species and the success of biological control agents, we should take antagonists at various trophic levels into consideration. To this end, we have combined the concepts from figure 3 and figure 4 to map the antagonist hypotheses that are most relevant to each of the four trophic levels discussed in this review (figure 5). Many of these hypotheses, such as biotic resistance, enemy escape, enemy reduction, enemy release, evolution of increased competitive ability, and new associations, can be applied to studies of plant hosts, as well as herbivores, predators, parasitoids, and hyperparasitoids. ...
Citations
... The enemy release hypothesis suggests that the absence of enemies in non-native ranges is important for the invasion success of non-native species (Enders et al., 2020;Schulz et al., 2019). Given that species interactions in nature are complex and it is impossible to construct detailed food webs for each site at the global scale (Brose et al., 2019), we applied a relatively coarse but general approach by assuming that species at higher trophic levels can be regarded as potential predators or natural enemies, following previous studies (Fornoff et al., 2021). ...
... The important effect of reduced natural enemies on CIP events corroborated the enemy release hypothesis (Enders et al., 2020; Schulz et al., 2019). This result was also consistent with some empirical observations. ...
Article impact statement: A global picture of the conservation-invasion paradox would help threatened species' conservation and invasive species management. Abstract The conservation-invasion paradox (CIP) refers to a long-term phenomenon wherein species threatened in their native range can sustain viable populations when introduced to other regions. Understanding the drivers of CIP is helpful for conserving threatened species and managing invasive species, which is unfortunately still lacking. We compiled a global data set of 1071 introduction events, including 960 CIP events (successful establishment of threatened species outside its native range) and 111 non-CIP events (unsuccessful establishment of threatened species outside its native range after introduction), involving 174 terrestrial vertebrates. We then tested the relative importance of various predictors at the location, event, and species levels with generalized linear mixed models and model averaging. Successful CIP events occurred across taxonomic groups and biogeographic realms, especially for the mammal group in the Palearctic and Australia. Locations of successful CIP events had fewer native threat factors, especially less climate warming in invaded regions. The probability of a successful CIP event was highest when species introduction efforts were great and there were more local congeners and fewer natural enemies. These results can inform threatened species ex situ conservation and non-native invasive species mitigation.
... Building confidence in the fact that gene drives will act as intended is vital. There has been too many dreadful examples of biocontrol measures becoming biosecurity issues (Blossey and Notzold 1995;Shine 2010;Schulz et al. 2019). Models provide guidelines and driving principles but can also be leveraged for the in silico stress-testing of new tools. ...
Gene drives have enormous potential for solving biological issues by forcing the spread of desired alleles through populations. However, to safeguard from the potentially irreversible consequences on natural populations, gene drives with intermediate outcomes that neither fixate nor get removed from the population are of outstanding interest.
To elucidate the conditions leading to intermediate gene drive frequency, a stochastic, individual allele-focused gene drive model accessible was developed to simulate the diffusion of a homing gene drive in a population. The frequencies of multiple alleles at a locus targeted by a gene drive were tracked under various scenarios. These explored the effect of gene drive conversion efficiency, strength and frequency of resistance alleles, presence and strength of a fitness cost for the gene drive, its dominance and the level of inbreeding.
Four outcomes were consistently observed: Fixation, Loss, Temporary and Equilibrium. The latter two are defined by the frequency of the gene drive peaking then crashing or plateauing, respectively. No single variable determined the outcome of a drive, instead requiring a combination of variables. The difference between the conversion efficiency and resistance level differentiated the Temporary and Equilibrium outcomes. The frequency dynamics of the gene drive within outcomes varied extensively, with different variables driving this dynamics between outcomes.
These simulation results highlight the possibility of fine-tuning gene drive outcomes and compensating through biotechnological design constraint imposed by population features. To that end, we provide a web application implementing our model which will guide the safer design of gene drives able to achieve a range of controllable outcome tailored to population management needs.
... It is true that a freshly distributed pathogen epidemic that intensifies can alter the afflicted ecology significantly. Here, polyphagous species coexisting in the same ecosystem might eventually switch to a different carbon source and modify their biology to take advantage of the newcomer [99]. However, attempts have been made to biologically control several of the most devastating nonnative pathogens using a bottom-up strategy; many potential biological control agents (BCAs), although promising in vitro, have almost completely failed in the field (e. g., Fusarium circinatum; failure in situ, and this may be climatic constraints, lack of an alternative host, development of resistance to BCA, and biotic disturbance by native organisms). ...
Fusarium spp. cause severe harm to forest plants. These fungi can induce latent infections that lead to planted seedlings rooting, as well as pre- and post-emergence damping. However, a phylogenetic study suggests that the most virulent strains of Fusarium oxysporum Schlechtend, which has been identified as the primary cause of root and root rot in nurseries, are more closely aligned with the recently identified Fusarium genus, Skovgaard, O’Donnell, and Nirenberg. Before planting, soil fumigation was the primary method of treating Fusarium illnesses in nurseries with bare roots. Alternative therapies are being investigated as rules impede the supply of the most effective fumigants. This entails improving sanitation, preserving a healthy microbial population that inhibits pathogens infecting trees through their roots, and refraining against actions that increase the risk of disease in trees, such as overfertilization and inadequate soil drainage. Although Fusarium circinatum, Nirenberg, and O’Donnell can be problematic in nurseries, they can harm ancient trees in native forests, plantations, seed farms, and landscape plantings. It is not advisable to transfer seeds or seedlings from contaminated to uninfected areas because they can spread the virus. To stop F. circinatum from spreading to nations where it has not yet been discovered, quarantine measures must be upheld. F. circinatum infections are linked to harm from weather-related events, insect activity, pruning, and seed harvesting, among other forest management practices. Pruning during the cold, dry season, when conditions are less conducive to infection, can help minimize the risk of illness in managed plantations and control insects that have the potential to be vectors and pests. Ecologically friendly biological strategies, such as using endophytic fungi and bacteria that are antagonistic to F. circinatum, plant essential oils, chitosan, or phosphite, have also been researched as ways to lessen the impact. Additionally, to reduce the number of contaminated seeds introduced into nurseries in disease-free areas, heat treatment is an easy and affordable way to eradicate the pathogen from contaminated seeds. Therefore, to address the problems of Fusarium spp,effects on nurseries, natural forests, and plantations using integrated approaches is required for sustainable managements of the forests.
... Other frameworks have been suggested that propose splitting the ERH into sub-hypotheses (e.g. Schulz et al., 2019) or splitting the ERH according to how it is tested (e.g. Heger & Jeschke, 2014). ...
The enemy release hypothesis (ERH) is the best-known hypothesis explaining high performance (e.g. rapid population growth) of exotic species. However, the current framing of the ERH does not explicitly link evidence of enemy release with exotic performance. This leads to uncertainty regarding the role of enemy release in biological invasions. Here, we demonstrate that the effect of enemy release on exotic performance is the product of three factors: enemy impact, enemy diversity, and host adaptation. These factors are modulated by seven contexts: time since introduction, resource availability, phylogenetic relatedness of exotic and native species, host–enemy asynchronicity, number of introduction events, type of enemy, and strength of growth–defence trade-offs. ERH-focused studies frequently test different factors under different contexts. This can lead to inconsistent findings, which typifies current evidence for the ERH. For example, over 80% of meta-analyses fail to consider ecological contexts which can alter study findings; we demonstrate this by re-analysing a recent ERH synthesis. Structuring the ERH around factors and contexts promotes generalisable predictions about when and where exotic species may benefit from enemy release, empowering effective management. Our mechanistic factor–context framework clearly lays out the evidence required to support the ERH, unifies many enemy-related invasion hypotheses, and enhances predictive capacity.
... The establishment of microbial agents depends on several aspects (i.e. climatic constraints, interactions with native organisms, lack of hosts, common cultivation practices), and the intensive irrigation during warmer weather conditions probably had a negative impact on the establishment of microbial additives (Schulz et al. 2019). Biological management of fungal pathogens in forest nurseries still lags behind agricultural production systems, and better targeted BCAs for forest seedlings are needed. ...
... Other frameworks have been suggested that propose splitting the ERH into sub-hypotheses (e.g. Schulz et al., 2019) or splitting the ERH according to how it is tested (e.g. Heger & Jeschke, 2014). ...
The enemy release hypothesis (ERH) is the best-known hypothesis explaining high performance (e.g., rapid population growth) of exotic species. However, the current framing of the ERH does not explicitly link evidence of enemy release with exotic performance. This leads to uncertainty regarding the role of enemy release in biological invasions. Here we demonstrate that the effect of enemy release on exotic performance is the product of three factors: enemy impact, enemy diversity, and host adaptation. These factors are modulated by seven contexts: time since introduction, resource availability, phylogenetic relatedness of exotic and native species, host-enemy asynchronicity, number of introduction events, type of enemy, and strength of growth-defence trade-offs. ERH-focused studies frequently test different factors under different contexts, leading to inconsistent findings, which characterise current evidence for the ERH. For example, over 80% of meta-analyses fail to consider ecological contexts that can modulate study findings; we demonstrate this by re-analysing a recent ERH synthesis. Structuring the ERH around factors and contexts promotes generalisable predictions about when and where exotic species may benefit from enemy release, empowering effective management. Our mechanistic factor-context framework clearly lays out the evidence required to support the ERH, unifies many enemy-related invasion hypotheses and enhances predictive capacity.
... The dotted lines indicate the two points we analysed data from; border interceptions after transport, and lists of established insects. Adapted from Schulz et al. (2019). by the extent to which its individuals or propagules can overcome these barriers (Blackburn et al., 2011). ...
Aim
Non‐native species are part of almost every biological community worldwide, yet numbers of species establishments have an uneven global distribution. Asymmetrical exchanges of species between regions are likely influenced by a range of mechanisms, including propagule pressure, native species pools, environmental conditions and biosecurity. While the importance of different mechanisms is likely to vary among invasion stages, those occurring prior to establishment (transport and introduction) are difficult to account for. We used records of unintentional insect introductions to test (1) whether insects from some biogeographic regions are more likely to be successful invaders, (2) whether the intensity of trade flows between regions determines how many species are intercepted and how many successfully establish, and (3) whether the variables driving successful transport and successful establishment differ.
Location
Canada, mainland USA, Hawaii, Japan, Australia, New Zealand, Great Britain, South Korea, South Africa.
Methods
To disentangle processes occurring during the transport and establishment stages, we analysed border interceptions of 8199 insect species as a proxy for transported species flows, and lists of 2076 established non‐native insect species in eight areas. We investigated the influence of biogeographic variables, socio‐economic variables and biosecurity regulations on the size of species flows between regions.
Results
During transport, the largest species flows generally originated from the Nearctic, Panamanian and Neotropical regions. Insects native to 8 of 12 biogeographic regions were able to establish, with the largest flows of established species on average coming from the Western Palearctic, Neotropical and Australasian/Oceanian regions. Both the biogeographic region of origin and trade intensity significantly influenced the size of species flows between regions during transport and establishment. The transported species richness increased with Gross National Income in the source country, and decreased with geographic distance. More species were able to establish when introduced within their native biogeographic region.
Main Conclusions
Our results suggest that accounting for processes occurring prior to establishment is crucial for understanding invasion asymmetry in insects, and for quantifying regional biosecurity risks.
... To suppress D. suzukii populations, control measures, including insecticides, attract-to-kill traps, altered cultivation environment, sterilized male release, and engineered gene drive systems have been explored without practical success (Buchman et al. 2018;Hamby et al. 2012;Mori et al. 2017;Schetelig et al. 2018;Tait et al. 2021). Introducing natural enemies (predators, parasites, parasitoids, and pathogens) is an additional, clean strategy to combat invasive species, which can cause pandemics as they may be free from the natural enemies present in their original habitat (Roy et al. 2011;Schulz et al. 2019). Natural enemies applicable to D. suzukii have been sought in their original distribution range as well as among commercial products of biopesticides (Becher et al. 2018;Bing et al. 2021;Cuthbertson and Audsley 2016;Daane et al. 2016;Foye and Steffan 2020;Garriga et al. 2018;Girod et al. 2018;Kasuya et al. 2013;Renkema et al. 2015;Sario et al. 2021), and the studies are ongoing. ...
Originally endemic to Asia, Drosophila suzukii (Matsumura, 1931) is a serious agricultural pest that is spreading rapidly throughout the world. To suppress the growing D. suzukii populations, several pest management programs have been implemented. Researchers have searched for natural enemies, such as predators, parasites, parasitoids, and pathogens. We discovered an obligate ectobiont fungus, Stigmatomyces majewskii H. L. Dainat, Manier & Balazuc, 1974, which is associated with D. suzukii. Our laboratory experiments revealed that S. majewskii infection was successfully transmitted through self-grooming and sexual contact during the courtship behavior of D. suzukii, although non-sexual contact through other behaviors may also be involved. Infected flies lived long enough for S. majewskii to mature on the host. Other fitness traits, such as fecundity, are necessary to evaluate the effect of S. majewskii on D. suzukii.
... In most cases, classic biological control is employed to target problematic invasive species with the aim to slow or decrease their population growth with minimal impact on surrounding native species [49]. These reductions in invasive populations can be achieved by releasing known above-or below-ground herbivores, predators or pathogens, that are native to the same areas as the invasive species, as controlling agents [50]. There are many successful examples of biocontrol around the world [51][52][53] and meta-analyses by Stiling & Cornelissen [55] found that biocontrols can reduce the biomass and reproductive output of weeds by over 80%. ...
... But not all instances of biocontrol succeed. Failed attempts at biologically controlling invasive plants have been recorded globally [50,56]. Plant species that have been identified as being released from their enemies should theoretically have royalsocietypublishing.org/journal/rspb ...
When a plant is introduced to a new ecosystem it may escape from some of its coevolved herbivores. Reduced herbivore damage, and the ability of introduced plants to allocate resources from defence to growth and reproduction can increase the success of introduced species. This mechanism is known as enemy release and is known to occur in some species and situations, but not in others. Understanding the conditions under which enemy release is most likely to occur is important, as this will help us to identify which species and habitats may be most at risk of invasion. We compared in situ measurements of herbivory on 16 plant species at 12 locations within their native European and introduced Australian ranges to quantify their level of enemy release and understand the relationship between enemy release and time, space and climate. Overall, plants experienced approximately seven times more herbivore damage in their native range than in their introduced range. We found no evidence that enemy release was related to time since introduction, introduced range size, temperature, precipitation, humidity or elevation. From here, we can explore whether traits, such as leaf defences or phylogenetic relatedness to neighbouring plants, are stronger indicators of enemy release across species.
... In pest-parasitoid systems, identifying and comparing relative habitat suitability of pest and parasitoid can help to guide effective biological control programs (Pérez-de la O et al., 2020;Tepa-Yotto et al., 2021a;Tepa-Yotto et al., 2021b). The utility of ENM in applications to biological control of pests can be attributed to two factors: alien parasitoid species must survive and reproduce in the geographic regions where they are released (Mills, 2018;Schulz, Lucardi & Marsico, 2019), and unfavorable abiotic factors can reduce the long-term efficacy of biological control measures (Olfert et al., 2016). Modeling climatic preferences of deliberately introduced parasitoid species can also provide insights into possible range expansions, an important aspect to be tested in improving effectiveness of classical biological control programs (Pérez-de la O et al., 2020). ...
Insect pest invasions cause significant damage to crop yields, and the resultant economic losses are truly alarming. Climate change and trade liberalization have opened new ways of pest invasions. Given the consumer preference towards organic agricultural products and environment-friendly nature of natural pest control strategies, biological control is considered to be one of the potential options for managing invasive insect pests. Drosophila suzukii (Drosophilidae) is an extremely damaging fruit pest, demanding development of effective and sustainable biological control strategies. In this study, we assessed the potential of the parasitoid Leptopilina japonica (Figitidae) as a biocontrol agent for D. suzukii using ecological niche modeling approaches. We developed global-scale models for both pest and parasitoid to identify four components necessary to derive a niche based, target oriented prioritization approach to plan biological control programs for D. suzukii : (i) potential distribution of pest D. suzukii , (ii) potential distribution of parasitoid L. japonica , (iii) the degree of overlap in potential distributions of pest and parasitoid, and (iv) biocontrol potential of this system for each country. Overlapping suitable areas of pest and parasitoid were identified at two different thresholds and at the most desirable threshold ( E = 5%), potential for L. japonica mediated biocontrol management existed in 125 countries covering 1.87 × 10 ⁷ km ² , and at the maximum permitted threshold ( E = 10%), land coverage was reduced to 1.44 × 10 ⁷ km ² in 121 countries. Fly pest distributional information as a predictor variable was not found to be improving parasitoid model performance, and globally, only in half of the countries, >50% biocontrol coverage was estimated. We therefore suggest that niche specificities of both pest and parasitoid must be included in site-specific release planning of L. japonica for effective biocontrol management aimed at D. suzukii . This study can be extended to design cost-effective pre-assessment strategies for implementing any biological control management program.
