Host-plant specificity and specialization in eriophyoid mites and their importance for the use of eriophyoid mites as biocontrol agents of weeds

Eriophyoid mites, which are among the smallest plant feeders, are characterized by the intimate relationships they have with their hosts and the restricted range of plants upon which they can reproduce. The knowledge of their true host ranges and mechanisms causing host specificity is fundamental to understanding mite-host interactions, potential mite-host coevolution, and diversity of this group, as well as to apply effective control strategies or to use them as effective biological control agents. The aim of this paper is to review current knowledge on host specificity and specialization in eriophyoid mites, and to point out knowledge gaps and doubts. Using available data on described species and recorded hosts we showed that: (1) 80% of eriophyoids have been reported on only one host species, 95% on one host genus, and 99% on one host family; (2) Diptilomiopidae has the highest proportion of monophagous species and Phytoptidae has the fewest; (3) non-monophagous eriophyoids show the tendency to infest closely related hosts; 4) vagrant eriophyoids have a higher proportion of monophagous species than refuge-seeking and refuge-inducing species; (5) the proportions of monophagous species infesting annual and perennial hosts are similar; however, many species infesting annual hosts have wider host ranges than those infesting perennial hosts; (6) the proportions of species that are monophagous infesting evergreen and deciduous plants are similar; (7) non-monophagous eriophyoid species have wider geographic distribution than monophagous species. Field and laboratory host-specificity tests for several eriophyoid species and their importance for biological control of weeds are described. Testing the actual host range of a given eriophyoid species, searching for ecological data, genetic differentiation analysis, and recognizing factors and mechanisms that contribute to host specificity of eriophyoid mites are suggested as future directions for research.     

The impact of eriophyoids on crops: recent issues on Aculus schlechtendali, Calepitrimerus vitis and Aculops lycopersici

The nature of the damage caused by eriophyoid mites and the assessment of yield losses still require detailed studies if appropriate control and risk mitigation strategies are to be planned. The economic importance of eriophyoid mites is increasing worldwide and a lot of species have reached a permanent pest status in certain crops, while others represent a quarantine threat for several countries. Due to their relevant role in Europe and elsewhere, three eriophyoid mites that have been frequently reported in recent research, are here considered as case studies: two of them (the apple rust mite, Aculus schlechtendali, and the grape rust mite, Calepitrimerus vitis) colonise temperate fruits, while one (the tomato russet mite, Aculops lycopersici) affects vegetables. The damage assessment related to the apple rust mite has been evaluated on different apple varieties with implications for pest control. Some factors affecting the spread and economic importance of the grape rust mite have been identified. The complexity and difficulty in controlling the tomato russet mite by chemicals enhances the interest in biological control agents. Considerations on interactions between eriophyoids and host plants (e.g. resistance, varietal susceptibility), on pest management regimes (e.g. impact of fungicides, resistance to acaricides, perspectives on biological control) are presented.     

Behavioural studies on eriophyoid mites: an overview

Eriophyoid mites are excellent candidates for ethological research using the approaches of behavioural ecology and sociobiology. These tiny haplodiploid mites are highly specialized plant parasites, producing galls, forming nests, inhabiting refuges or living freely on plants. They reproduce via spermatophores deposited on a substrate and without pairing, which is a fascinating, though still poorly understood, mode of reproduction widespread in some groups of arthropods. Eriophyoid males can be involved in external sperm competition. In some species they also guard pre-emergent females and deposit spermatophores beside them. Although slow-walking, the minute eriophyoid mites can disperse for long distances on air currents or specific animal carriers. After landing on a plant they can distinguish between suitable and unsuitable hosts. Biological observations on a deuterogynous species indicate that parasociality could occur among eriophyoid mites. Many eriophyoids are of economic importance. Knowledge of their behaviour may promote understanding their ecology, may resolve problems in their phylogeny and may help developing methods for their control. In this paper, attention is directed to dispersal modes of eriophyoid mites, their feeding and host acceptance, spermatophore deposition and mating, defence against predators, and social behaviour.     

An insight into some relevant aspects concerning eriophyoid mites inhabiting forests, ornamental trees and shrubs

Worldwide a great variety of eriophyoid mites inhabit forest canopy trees and ornamental plants that are used in city parks, squares and boulevards. An analysis of the relevant bibliography portrays only a fragmentary knowledge and the majority of our information concerns the temperate zone. Three case studies are presented as examples of different approaches to solve problems connected with eriophyoid mites of forest and ornamental trees. The first example deals with eriophyoids of a temperate zone forest in a natural environment, focusing on conifers which represent the largest component. The second case study documents a possible approach to obtain greater knowledge and control of the bud mite species, Trisetacus juniperinus (Nalepa) on Cupressaceae. This is a harmless species in the natural environment which becomes a serious pest in nurseries and young stands of Cupressus sempervirens in the Mediterranean region. The final case study reports on long-term studies carried out in Poland on injurious eriophyoid species that are found in nurseries, city greenery and parks. This paper also discusses future perspectives for research on eriophyoid mites living on forest and ornamental plants.     

Two species of eriophyoid mites (Acari, Prostigmata) in wheat cultivation (Triticum aestivum L.) and associated grass community in Wielkopolska, Poland

Abstract: Quantitative characteristics of the occurrence of eriophyoid mites on wheat and associated grasses were studied. Three groups of hosts: cultivated wheat ( Triticum aestivum ), quackgrass ( Agropyron repens ) in cultivation, and quackgrass in balks were analysed. Two species of eriophyoid mites were recorded: Aceria tosichella Keifer and Abacarus hystrix (Nalepa). A. hystrix appeared more frequent [present in 65.0% of all collected samples; (95% confidence interval: 50–80)] and abundant [mean number of individuals per sample: 207.3 (94.4–351.5)] than A. tosichella (17.5%; (7.5–3.0), 13.8 (0.9–32.8), respectively). Significant differences in numbers among studied mite species populations on different host plants have been found. It is concluded that wheat is the marginal host for these two eriophyoids when compared to quackgrass.     

Plant–eriophyoid mite interactions: cellular biochemistry and metabolic responses induced in mite-injured plants. Part I

This review is a comprehensive study of recent advances related to cytological, biochemical and physiological changes induced in plants in response to eriophyoid mite attack. It has been shown that responses of host plants to eriophyoids are variable. Most of the variability is due to individual eriophyoid mite–plant interactions. Usually, the direction and intensity of changes in eriophyoid-infested plant organs depend on mite genotype, density, or the feeding period, and are strongly differentiated relative to host plant species, cultivar, age and location. Although the mechanisms of changes elicited by eriophyoid mites within plants are not fully understood, in many cases the qualitative and quantitative biochemical status of mite-infested plants are known to affect the performance of consecutive herbivorous arthropods. In future, elucidation of the pathways from eriophyoid mite damage to plant gene activation will be necessary to clarify plant responses and to explain variation in plant tissue damage at the feeding and adjacent sites.     

Plant–eriophyoid mite interactions: specific and unspecific morphological alterations. Part II

The paper presents recent advances related to both specific and unspecific morphological alterations of plant organs caused by eriophyoid mites. Based on old and new case studies, the diversity of plant malformations, such as galls, non-distortive feeding effects and complex symptoms induced by eriophyoids and/or pathogens vectored by them, is analysed and summarised.     

Eriophyoid Mites (Acariformes,Eriophyoidea) from Rosaceae: Taxonomic Diversity,Host-Parasite Relationships,and Ability to Cause Galls

A review on the complex of species of eriophyoid mites associated with Rosaceae is given, focused on the phylogeny, biology, and distribution of their host plants and galls induced by these mites. About 200 species of 39 genera from 3 families ofEriophyoidea are known from Rosaceae. Among them, 6 species from 2 genera belong to Phytoptidae, 178 species from 27 genera, to Eriophyidae, and 28 species from 10 genera, to Diptilomiopidae; 7 genera of the latter family are represented on Rosaceae by a single species each. The ability to induce galls is discussed using the example of the most widespread and numerous genera of the family Eriophyidae from Rosaceae. Mites of two large subfamilies, Eriophyinae and Phyllocoptinae, include both vagrant and concealed forms. The types of galls caused by mites are related to the systematic position of mites and the distribution of mites and their host plants. The hypothesis of host shifts of eriophyoid mites from other plant families to Rosaceae is considered. Most of the species which presumably switched to Rosaceae have been described from Southeast Asia. Morphological similarity between vagrant and concealed forms from the paraphyletic tribes Eriophyini and Phyllocoptini, and also Aceriini and Anthocoptini is discussed. Their pairwise similarity might be the result of evolution (Eriophyini → Phyllocoptini and Aceriini → Anthocoptini) connected with change oflife style.     

DNA-based methods for eriophyoid mite studies: review, critical aspects, prospects and challenges

Besides their potential for species identification, DNA-based methods are also routinely used for addressing ecological, evolutionary, phylogenetic and genetic questions to study several groups of Acari. However, in contrast to other plant-feeding mites and despite the economical relevance of many species of Eriophyoidea, very few scientists have dared so far to use DNA methods for the study of this group of mites; their very small size certainly has influenced this. In this review we examine the main techniques that have been used to study eriophyoid mites and discuss the results from the literature where DNA methods have provided significant advances to address several essential questions of the eriophyoid biology, e.g., to clarify suspect synonymies, to test hypothesis of cryptic species, to examine the occurrence of biotypes, especially in relation to virus ability or host-plant associations, to understand colonization patterns of invasive species, and for uses as biological control agents against invasive plants. We discuss these questions which might be related to agricultural issues, together with more fundamental aspects as the revision of the phylogeny of the Eriophyoidea. We discuss on the advantages as well as limitations of the most commonly used genetic markers and emphasize prospects and challenges of new molecular approaches. Much is now expected from molecular techniques in many fields of biology and for virtually all taxa. Eriophyoids should not be the exception.     

Diseases of Mites

An overview is given of studies on diseases of mites. Knowledge of diseases of mites is still fragmentary but in recent years more attention has been paid to acaropathogens, often because of the economic importance of many mite species. Most research on mite pathogens concerns studies on fungal pathogens of eriophyoids and spider mites especially. These fungi often play an important role in the regulation of natural mite populations and are sometimes able to decimate populations of phytophagous mites. Studies are being conducted to develop some of these fungi as commercial acaricides.Virus diseases are known in only a few mites, namely, the citrus red mite and the European red mite. In both cases, non-occluded viruses play an important role in the regulation of mite populations in citrus and peach orchards, respectively, but application of these viruses as biological control agents does not seem feasible. A putative iridovirus has been observed in association with Varroa mites in moribund honeybee colonies. The virus is probably also pathogenic for honeybees and may be transmitted to them through this parasitic mite.Few bacteria have been reported as pathogens of the Acari but in recent years research has been concentrated on intracellular organisms such as Wolbachia that may cause distorted sex ratios in offspring and incompatibility between populations. The role of these organisms in natural populations of spider mites is in particular discussed. The effect of Bacillus thuringiensis on mites is also treated in this review, although its mode of action in arthropods is mainly due to the presence of toxins and it is, therefore, not considered to be a pathogen in the true sense of the word.Microsporidia have been observed in several mite species especially in oribatid mites, although other groups of mites may also be affected. In recent years, Microsporidia infections in Phytoseiidae have received considerable attention, as they are often found in mass rearings of beneficial arthropods. They affect the efficacy of these predators as biological control agent of insect and mite pests. Microsporidia do not seem to have potential for biological control of mites.     

What’s “cool” on eriophyoid mites?

Fundamental knowledge on the morphology, biology, ecology, and economic importance of Eriophyoidea has been exhaustively compiled by Lindquist et al. (Eriophyoid mites—their biology, natural enemies and control; Elsevier, 1996). Since that time, the number of recognized species and the economic importance of the taxon have increased substantially. The aim of this paper is to analyze and briefly review new findings from eriophyoid mites’ literature after Lindquist et al. book, stressing persistent gaps and needs. Much recent attention has been given to sampling and detection, taxonomy and systematics, faunistic surveys, internal morphology, rearing techniques, biological and ecological aspects, biomolecular studies, and virus vectoring. Recommendations are made for integrating research and promoting broader dissemination of data among specialists and non-specialists.     

Is the Cereal Rust Mite, Abacarus Hystrix Really a Generalist? – Testing Colonization Performance on Novel Hosts

The majority of eriophyoid mites are highly host specific and restricted to a narrow range of acceptable host plant species. The cereal rust mite, Abacarus hystrix was considered to be one of a few exceptions among them and has been found to be using a relatively wide host range. Since this species is a vagrant, inhabiting short-lived plants and aerially dispersing, it has commonly been considered to be a host generalist. Here the opposite hypothesis is tested, that host populations of A. hystrix are specialized on their local host plants and may represent host races. For this purpose, females from two host populations (quack grass, Agropyron repens and ryegrass, Lolium perenne) were transferred, and subsequently reared, on their normal (grass species from which females came from) and novel (other grass species) hosts. The female's fitness was assessed by survival and fecundity on the normal and novel host. Females of both populations had no success in the colonization of the novel host. They survived significantly better and had significantly higher fecundity on their normal host than on the novel one. These findings correspond with observations on host-dependent phenotype variability and host acceptance. The presence of locally specialized host populations in A. hystrix may be evidence for high host specificity among eriophyoids and the viruses they transmit. The main conclusion is that A. hystrix, which so far has been considered as a host generalist, in fact may be a complex species consisting of highly specialized host races.     

Fungal Biocontrol of Acari

Mites and ticks are susceptible to pathogenic fungi, and there are opportunities to exploit these micro-organisms for biological control. We have collated records of 58 species of fungi infecting at least 73 species of Acari, either naturally or in experiments. Fungal pathogens have been reported to kill representatives of all three orders of the Actinotrichida (the Astigmata, Oribatida and Prostigmata) and the Ixodida and Mesostigmata in the Anactinotrichida. Most reports concern infections in the Prostigmata, particularly in the families Tetranychidae and Eriophyidae. Two species of Acari-specific pathogens - Hirsutella thompsonii and Neozygites floridana - are important natural regulators of pestiferous eriophyoid and tetranychid mites respectively. Research has been done to understand the factors leading to epizootics of these fungi and to conserve and enhance natural pest control. Hirsutella thompsonii was also developed as the commercial product Mycar for the control of eriophyoid mites on citrus, but was withdrawn from sale in the 1980s, despite some promising effects in the field. Beauveria bassiana , Metarhizium anisopliae, Paecilomyces farinosus, Paecilomyces fumosoroseus and Verticillium lecanii infect ixodid ticks in nature, and B. bassiana and M. anisopliae are being studied as biological control agents of cattle ticks in Africa and South America. Beauveria bassiana also has potential as a mycopesticide of the two-spotted spider mite, Tetranychus urticae . There is scope to develop fungal biocontrol agents against a range of acarine pests, both as stand-alone treatments and for use in integrated pest management. Further research is required to clarify the taxonomic status of fungal pathogens of Acari, to study their ecosystem function, and to develop efficient mass production systems for species of Hirsutella and Neozygites .     

Review: Milking robot utilization,a successful precision livestock farming evolution

Automatic milking systems (AMS), one of the earliest precision livestock farming developments, have revolutionized dairy farming around the world. While robots control the milking process, there have also been numerous changes to how the whole farm system is managed. Milking is no longer performed in defined sessions; rather, the cow can now choose when to be milked in AMS, allowing milking to be distributed throughout a 24 h period. Despite this ability, there has been little attention given to milking robot utilization across 24 h. In order to formulate relevant research questions and improve farm AMS management there is a need to determine the current knowledge gaps regarding the distribution of robot utilization. Feed, animal and management factors and their interplay on levels of milking robot utilization across 24 h for both indoor and pasture-based systems are here reviewed. The impact of the timing, type and quantity of feed offered and their interaction with the distance of feed from the parlour; herd social dynamics, climate and various other management factors on robot utilization through 24 h are provided. This novel review draws together both the opportunities and challenges that exist for farm management to use these factors to improved system efficiency and those that exist for further research.     

Fleshy fruits of indigenous and adventive plants in the diet of birds in forest remnants, Nelson, New Zealand

The relationship between fleshy-fruited indigenous species and adventive weeds in the diet of 500 mist-netted birds was studied in forest remnants of differing size and degree of modification. Fruit abundance Peaked in March and April, and most fruit was either red/orange or purple/black. The physical parameters of adventive and indigenous fruits were not significantly different. Six of the 15 passerine species netted are frugivores, and of those netted 77% had eaten fruit. They were divisible into three groups: endemic (bellbirds, Anthornis melanura; tuis, Prosthemadera novaeseelandiae), non-endemic but indigenous (silvereyes, Zosterops lateralis), and adventive (blackbirds, Turdus merula; song thrushes, T. philomelos; starlings, Sturnus vulgaris). Bird diets varied between the groups and according to fruit availability as determined by sires and seasons. Endemic birds ate the least adventive fruit; bellbirds ate mainly Podocarpus hallii and Coprosma robusta fruits at all sites. Tuis had a varied diet, including some adventive fruits. Silvereyes ate the widest range of indigenous and adventive fruits. Blackbirds and, to a smaller extent, song thrushes ate many of the same indigenous fruits as the other bird groups, but their diet included more adventive fruits, e.g., Berberis glaucocarpa. Starlings were caught only when they fed on Sambucus nigra, but they also ate a few indigenous fruits. There was little seasonal variation in bird numbers caught. Adventive species extended the seasonal availability of fruits into winter, particularly in the forest remnant closest to a town, which had the highest proportion of adventive fruits. Several weed species distributed mainly by non-endemic and adventive birds are forming new secondary vegetation. Some have large fruit crops which generally offer little food for endemic birds. Where fruiting weeds pre-empt sites that may have been occupied by native species, they create an inferior habitat for endemic birds. However, the non-endemic and adventive birds also disperse indigenous fruits into early successional vegetation, and the importance of their seed rain for conservation of biodiversity will therefore depend on the site.     

Quackgrass- and ryegrass-adapted populations of the cereal rust mite, Abacarus hystrix (Acari: Eriophyidae), differ in their potential for wheat, Triticum aestivum, colonization

The cereal rust mite, Abacarus hystrix, is one of the most notable among mites causing losses in cultivated grasslands. It is one of a few eriophyoid species for which a broad host range has been reported. Recent studies, however, have shown that host specialization is very likely in this species. For two populations of A. hystrix (one inhabiting perennial ryegrass, the second inhabiting quackgrass), host-associated differences correlated with strong host fidelity, distinct phenotypes and reproductive barriers have been found. In the present study, the ability of wheat colonization by quackgrass- and ryegrass-adapted cereal rust mite was studied. The hypothesis that the potential for wheat colonization by the quackgrass strain is more likely was tested by comparing the colonization performance (assessed by female survival and fecundity) of quackgrass- and ryegrass-associated A. hystrix on their familiar hosts and on wheat. The ryegrass population had no success in wheat colonization (expressed by extremely low fecundity and female survival). Fecundity and survival of quackgrass strain were similar on wheat and the familiar host, or even higher on wheat. Phylogenetic similarity of quackgrass and wheat is discussed as a possible factor that might influence such patterns of host colonization. Since A. hystrix is the only vector of the ryegrass mosaic virus (RgMV), the presented results may be helpful in explaining the inability of RgMV to successfully infest wheat. The conclusions are that (i) quackgrass- and ryegrass-adapted strains of the cereal rust mite have different physiological host ranges and (ii) phylogenetic relationships between host plant species appear to be drivers for host specialization in this mite species.