Acquisition of fungi from the environment modifies ambrosia beetle mycobiome during invasion

Microbial symbionts can play critical roles when their host attempts to colonize a new habitat. The lack of symbiont adaptation can in fact hinder the invasion process of their host. This scenario could change if the exotic species are able to acquire microorganisms from the invaded environment. Understanding the ecological factors that influence the take-up of new microorganisms is thus essential to clarify the mechanisms behind biological invasions. In this study, we tested whether different forest habitats influence the structure of the fungal communities associated with ambrosia beetles. We collected individuals of the most widespread exotic (Xylosandrus germanus) and native (Xyleborinus saxesenii) ambrosia beetle species in Europe in several old-growth and restored forests. We characterized the fungal communities associated with both species via metabarcoding. We showed that forest habitat shaped the community of fungi associated with both species, but the effect was stronger for the exotic X. germanus. Our results support the hypothesis that the direct contact with the mycobiome of the invaded environment might lead an exotic species to acquire native fungi. This process is likely favored by the occurrence of a bottleneck effect at the mycobiome level and/or the disruption of the mechanisms sustaining co-evolved insect-fungi symbiosis. Our study contributes to the understanding of the factors affecting insect-microbes interactions, helping to clarify the mechanisms behind biological invasions

From arrival to spread: improving the early-detection of alien wood-boring beetles

The introduction of alien species in new habitats is a global and growing problem worldwide. Since the discovery of the Americas about 10,000 species have been introduced in Europe, mainly plants and insects. Among the latter, wood-boring beetles (mainly Scolytinae, Cerambycidae and Buprestidae) are recognized as one of the most successful group of invaders. These insects can be transported in almost all types of woody materials and, once introduced and established, they can cause enormous damage to ecosystems and economies of the invaded countries. In addition to traditional control methods, in the last years several countries have implemented other kinds of tools, such as traps baited with attractive lures, in order to enhance the chances of alien wood-boring beetles interception. Resources available for these activities are however limited while the number of sites that should be monitored is extremely high. For this reason, it is of utmost importance to have reliable and efficient trapping protocols as well as to understand where surveillance efforts should be focused. However, the general solution of this problem is strictly related to a better comprehension of the three steps characterizing the invasion process: arrival, establishment and spread. This thesis has two main aims: first, to enhance the early-detection of alien wood-boring beetles at high-risk sites located both in coastal and continental areas, and second, to gain insight into the mechanisms driving the alien wood-boring beetle invasion process. The first study concerns the development of efficient early-detection protocols that can be adopted for the interception of alien wood-boring beetles arriving at European ports of entry. This is focused on how different use of attractive lures, different trap models and trap positions (inside ports vs surrounding areas) may influence the chances of interception of alien species. The results suggest the use of multi-funnel traps baited with different lures for monitoring alien wood-boring beetles. The deployment of traps outside the port is also recommended to validate the surveillance program. The second study concerns how port size, in terms of amount of imported commodities, and characteristics of the landscape surrounding the ports, in terms of forest cover and forest composition, may affect the early-detection of alien wood-boring beetles. The results suggest that surveillance should be focused mainly in large ports and in the surrounding broadleaf forests, deploying traps simultaneously in both habitats. The third study is focused on the comparison between ports of entry and wood waste landfills, considered as the final destination of a large part of wood packaging materials imported together with goods. The results show that wood waste landfills are a crucial site where detecting alien species associated with woody materials, even in continental areas far away from the coasts. The forth and fifth studies investigate how the main climatic and environmental variables affect the establishment and spread of alien bark and ambrosia beetles at both regional and continental scale. The main results demonstrate that the invasion process of exotic scolytids is not random and that both climate and forest composition play a key role in shaping their communities and their spatial distribution in the invaded environment. However, these mechanisms occur differently according to the feeding guild of the two main groups of scolytids, the bark beetles and the ambrosia beetles. In general, the five studies carried out in this thesis provide suggestions to increase the probability of an early-detection of alien species both in coastal and continental areas, describing a protocol applicable both at local and international scale. At the same time, they contribute to improve the knowledge about the mechanisms characterizing the invasion process of alien wood-boring beetles, information that can be of utmost importance for the development of future strategies focused to reduce economic and environmental damage due to alien species

Improving the early detection of alien wood-boring beetles in ports and surrounding forests

International ports are generally considered the most likely points of entry for alien wood-boring beetles. A better understanding of the factors affecting their arrival and establishment at ports and their surrounding areas is of utmost importance to improve the efficacy and the cost-effectiveness of early detection programmes. Our work aimed at understanding how port size and the characteristics of the landscape surrounding the port, in terms of forest cover and forest composition, influence the occurrence of alien wood-boring beetles. From May to September 2012, 15 Italian international ports and the surrounding forests were monitored with multi-funnel traps baited with a multi-lure blend (\u3b1-pinene, ethanol, ipsdienol, ipsenol, methyl-butenol), three in each port and three in forests located 3\u20135 km away from the port. We identified both alien and native Scolytinae, Cerambycidae and Buprestidae beetles. Fourteen alien species, among which four are new to Italy, were trapped. Alien species richness was positively related to the amount of imported commodities at the port scale. Broadleaf forests surrounding ports received larger number of alien species than conifer forests. By contrast, total forest cover in the landscape surrounding ports was positively related to the occurrence of native but not alien species. The alien and native species richness was higher in the surrounding forests than in the ports. Synthesis and applications. The simultaneous use of traps in ports with large volume of imported commodities and in their surrounding broadleaf forests can strongly increase the probability of alien wood-boring beetle interceptions. The identification of sites where the arrival and establishment of alien species is more probable, combined with an efficient trapping protocol, can substantially improve the efficacy of early detection. Similar approaches may be used in other countries as early warning systems to implement timely measures to eradicate or contain alien invasions at the European scale

Acquisition of fungi from the environment modifies ambrosia beetle mycobiome during invasion

Microbial symbionts can play critical roles when their host attempts to colonize a new habitat. The lack of symbiont adaptation can in fact hinder the invasion process of their host. This scenario could change if the exotic species are able to acquire microorganisms from the invaded environment. Understanding the ecological factors that influence the take-up of new microorganisms is thus essential to clarify the mechanisms behind biological invasions. In this study, we tested whether different forest habitats influence the structure of the fungal communities associated with ambrosia beetles. We collected individuals of the most widespread exotic (Xylosandrus germanus) and native (Xyleborinus saxesenii) ambrosia beetle species in Europe in several old-growth and restored forests. We characterized the fungal communities associated with both species via metabarcoding. We showed that forest habitat shaped the community of fungi associated with both species, but the effect was stronger for the exotic X. germanus. Our results support the hypothesis that the direct contact with the mycobiome of the invaded environment might lead an exotic species to acquire native fungi. This process is likely favored by the occurrence of a bottleneck effect at the mycobiome level and/or the disruption of the mechanisms sustaining co-evolved insect-fungi symbiosis. Our study contributes to the understanding of the factors affecting insect-microbes interactions, helping to clarify the mechanisms behind biological invasions

Investigating beetle communities in and around entry points can improve surveillance at national and international scale

Beetles are commonly moved among continents with international trade. Baited traps set up in and around entry points are commonly used to increase chances of early-detection of incoming species and complement visual inspections. A still underestimated benefit of this surveillance approach is the high number and diversity of collected bycatch species. In this study, we exploited a multiyear surveillance program carried out with baited traps at five Spanish ports and their surrounding natural areas to investigate i) the importance of identifying bycatch to more promptly detect nonnative species belonging to non-target groups; ii) patterns of native and nonnative species richness and abundance inside the port areas vs. surrounding natural areas; iii) the occurrence of spillover events between natural areas surrounding ports and the port areas, and iv) whether the native species most commonly introduced into other countries are more abundant in port areas than in surrounding natural areas. A total of 23,538 individuals from 206 species representing 33 families were collected. The number and taxonomic diversity of the 26 bycatch nonnative beetle species testified that the identification of these unintentionally trapped species can provide additional information on ongoing invasions. Patterns of spillover and native species richness and abundance in port areas vs. surrounding natural areas highlighted a differential ability of different beetle families to colonize port areas. Finally, native species most commonly introduced into other countries were more abundant in port areas than in their surroundings, while the opposite trend occurred for native species that have not been introduced elsewhere. Our study highlighted that the use of traps baited with generic attractants can aid in early-detection of nonnative beetle species, and that the identification of native species can provide useful information on the risk of introduction in other countries.The study was funded by the Servei d’Ordenació i Gestió Forestal (Conselleria d’Agricultura, Desenvolupament Rural, Emergència Climàtica i Transició Ecològica) of Generalitat Valenciana. Davide Rassati was partially supported by the CRUI-CARE Agreement. 2019 STARS Grants programme (project: MOPI–Microorganisms as hidden players in insect invasions)

Investigating beetle communities in and around entry points can improve surveillance at national and international scale

Beetles are commonly moved among continents with international trade. Baited traps set up in and around entry points are commonly used to increase chances of early-detection of incoming species and complement visual inspections. A still underestimated benefit of this surveillance approach is the high number and diversity of collected bycatch species. In this study, we exploited a multiyear surveillance pro-gram carried out with baited traps at five Spanish ports and their surrounding natural areas to investigate i) the importance of identifying bycatch to more promptly detect nonnative species belonging to non-target groups; ii) patterns of native and nonnative species richness and abundance inside the port areas vs. surrounding natural areas; iii) the occurrence of spillover events between natural areas surrounding ports and the port areas, and iv) whether the native species most commonly introduced into other countries are more abundant in port areas than in surrounding natural areas. A total of 23,538 individuals from 206 species representing 33 families were collected. The number and taxonomic diversity of the 26 bycatch nonnative beetle species testified that the identification of these unintentionally trapped species can pro-vide additional information on ongoing invasions. Patterns of spillover and native species richness and abundance in port areas vs. surrounding natural areas highlighted a differential ability of different beetle families to colonize port areas. Finally, native species most commonly introduced into other countries were more abundant in port areas than in their surroundings, while the opposite trend occurred for native species that have not been introduced elsewhere. Our study highlighted that the use of traps baited with generic attractants can aid in early-detection of nonnative beetle species, and that the identification of native species can provide useful information on the risk of introduction in other countrie

Common pathways by which non-native forest insects move internationally and domestically

International trade and movement of people are largely responsible for increasing numbers of non-native insect introductions to new environments. For forest insects, trade in live plants and transport of wood packaging material (WPM) are considered the most important pathways facilitating long-distance invasions. These two pathways as well as trade in firewood, logs, and processed wood are commonly associated with insect infestations, while “hitchhiking” insects can be moved on cargo, in the conveyances used for transport (e.g., containers, ships), or associated with international movement of passengers and mail. Once established in a new country, insects can spread domestically through all of the above pathways. Considerable national and international efforts have been made in recent years to reduce the risk of international movement of plant pests. International Standards for Phytosanitary Measures (ISPMs) No. 15 (WPM), 36 (plants for planting), and 39 (wood) are examples of phytosanitary standards that have been adopted by the International Plant Protection Convention to reduce risks of invasions of forest pests. The implementation of ISPMs by exporting countries is expected to reduce the arrival rate and establishments of new forest pests. However, many challenges remain to reduce pest transportation through international trade, given the ever-increasing volume of traded goods, variations in quarantine procedures between countries, and rapid changes in distribution networks. It is therefore likely that many more human-assisted invasions of forest insects will take place. New geographic expansions by natural modes are also made possible due to changes in host distribution and/or climate.http://link.springer.com/journal/103402020-01-01hj2018Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Special issue on invasive pests of forests and urban trees : pathways, early detection, and management

This special issue on pathways, early detection, and management of invasive pests of forests and urban trees was spawned in a symposium entitled “Invasive species surveillance: new methods and tools for survey and early detection,” held at the International Union of Forestry Research Organizations (IUFRO) 125th Anniversary Congress in Freiburg, Germany, September 19–22, 2017.http://link.springer.com/journal/103402020-01-04hj2019Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Reproductive biology of Sclerodermus brevicornis, a European parasitoid developing on three species of invasive longhorn beetles

The reproductive performance of Sclerodermus brevicornis (Kieffer), a bethylid wasp native to Europe, was evaluated on three species of facticious hosts. These are longhorn beetles which have recently invaded Europe from Asia: Anoplophora glabripennis (Motschulsky), Anoplophora chinensis (Forster) and Psacothea hilaris hilaris (Pascoe) (Coleoptera: Cerambycidae). Sclerodermus brevicornis attacked all three species, but offspring only developed to maturity on medium and large sized host larvae. Host species influenced the duration of parasitoid development and the number of offspring maturing, both were greatest on A. glabripennis, with up to 373 adult parasitoids emerging from a single host. The sex ratios of S. brevicornis broods were strongly female biased (ca. 9% males). We conclude that S. brevicornis has the potential to be efficiently mass-reared and actively deployed in the biological control of invasive longhorn beetles. Further progress should be encouraged by the successful use of other species of Sclerodermus against beetle pests in China

Recent advances toward the sustainable management of invasive Xylosandrus ambrosia beetles

We provide an overview of both traditional and innovative control tools for management of three Xylosandrus ambrosia beetles (Coleoptera: Curculionidae: Scolytinae), invasive species with a history of damage in forests, nurseries, orchards and urban areas. Xylosandrus compactus, X. crassiusculus and X. germanus are native to Asia, and currently established in several countries around the globe. Adult females bore galleries into the plant xylem inoculating mutualistic ambrosia fungi that serve as food source for the developing progeny. Tunneling activity results in chewed wood extrusion from entry holes, sap outflow, foliage wilting followed by canopy dieback, and branch and trunk necrosis. Maintaining plant health by reducing physiological stress is the first recommendation for long-term control. Baited traps, ethanol-treated bolts, trap logs and trap trees of selected species can be used to monitor Xylosandrus species. Conventional pest control methods are mostly ineffective against Xylosandrus beetles because of the pests’ broad host range and rapid spread. Due to challenges with conventional control, more innovative control approaches are being tested, such as the optimization of the push–pull strategy based on specific attractant and repellent combinations, or the use of insecticide-treated netting. Biological control based on the release of entomopathogenic and mycoparasitic fungi, as well as the use of antagonistic bacteria, has yielded promising results. However, these technologies still require validation in real field conditions. Overall, we suggest that management efforts should primarily focus on reducing plant stress and potentially be combined with a multi-faceted approach for controlling Xylosandrus damage