A classical biological control agent is an exotic host-specific natural enemy, which is intentionally introduced to obtain long-term control of an alien invasive species. Among the arthropods considered for this role, eriophyid mites are likely to possess the main attributes required: host specificity, efficacy, and long-lasting effects. However, so far, only a few species have been approved for release. Due to their microscopic size and the general lack of knowledge regarding their biology and behavior, working with eriophyids is particularly challenging. Furthermore, mites disperse in wind, and little is known about biotic and abiotic constraints to their population growth. All these aspects pose challenges that, if not properly dealt with, can make it particularly difficult to evaluate eriophyids as prospective biological control agents and jeopardize the general success of control programs. We identified some of the critical aspects of working with eriophyids in classical biological control of weeds and focused on how they have been or may be addressed. In particular, we analyzed the importance of accurate mite identification, the difficulties faced in the evaluation of their host specificity, risk assessment of nontarget species, their impact on the weed, and the final steps of mite release and post-release monitoring.

Tree of heaven (Ailanthus altissima) is a fast-growing deciduous tree native to China, considered a serious invasive species worldwide, with several socio-economic and ecological impacts attributed to it. Chemical and mechanical methods have limited efficacy in its management, and biological controls may offer a suitable and sustainable option. Aculus mosoniensis (Ripka) is an eriophyid mite that has been recorded to attack tree of heaven in 13 European countries. This study aims to explore the host range of this mite by exposing 13 plant species, selected either for their phylogenetic and ecological similarity to the target weed or their economic importance. Shortly after inoculation with the mite, we recorded a quick decrease in mite number on all nontarget species and no sign of mite reproduction. Whereas, after just one month, the population of mites on tree of heaven numbered in the thousands, irrespective of the starting population, and included both adults and juveniles. Significantly, we observed evidence of damage due to the mite only on target plants. Due to the specificity, strong impact on the target, and the ability to increase its population to high levels in a relatively short amount of time, we find A. mosoniensis to be a very promising candidate for the biological control of tree of heaven.

The taxonomy of Aculus mosoniensis appears to be an unresolved question and its clarification is required, owing to the potential relevance of this mite species as a biological control agent of the tree of heaven. This paper is aimed at giving accurate details on a previously and shortly announced synonymization with Aculops taihangensis, using a morphological and molecular approach. A fusiform morph of A. mosoniensis was distinguished from a vermiform morph and this latter was recognized as deutogyne, which was herein documented. Phylogenetic relationships between Chinese Ac. taihangensis and all A. mosoniensis mites collected in twenty localities in Europe were examined through the analysis of the mitochondrial cytochrome c subunit I (CO1) protein and the nuclear ribosomal internal transcribed spacer 1 region (ITS1). CO1 sequences of Ac. taihangensis from the Shandong province in China and those from mites collected in Austria and Slovenia were 100% identical; the ITS1 sequence of an Ac. taihangensis paratype matched for 99.8% with those obtained from protogynes and deutogynes of A. mosoniensis collected in Italy. All these data supported the announced synonymization of A. mosoniensis with Ac. taihangensis. Aculusmosoniensis was found genetically variable, with five CO1 haplotypes in Europe (becoming eight along with those of Ac. taihangensis) clustering in two highly supported maternal lineages and eight ITS1 haplotypes (becoming nine along with those of Ac. taihangensis) distributed in four supported clades. No overlap between intra- and interspecies distances was observed for both markers and all studied A. mosoniensis populations clustered in one monophyletic mitochondrial clade, suggesting that only one single species might occur in Europe. However, more mite clades may be related to more tree of heaven biotypes with potential ecological differences, which might have potential effects on the biological control and should be investigated.

Summary: In May 2020, populations of Eriophyid mites were detected on tree of heaven,AilanthusaltissimaMill., in a recreative park in the city of Colombes, near Paris, and later in August and September in four locations, in Southern France. Morphological examination supplemented with sequencing data for the cytochrome c oxidase subunit I (COI) assigned all collected mites to a single species,Aculusmosoniensis(Ripka) (Acari; Prostigmata; Eriophyoidea). This is the first record of this species in France and the first insights into its intraspecific variability based on a barcode dataset. In Europe, this species is considered one of the most promising biological control agents of tree of heaven. This new record provides encouraging evidence that the geographic occurrence of this species is expanding in Europe which may be indicative of its dispersal and establishment abilities, two key factors for a future biological control program.