Research Article ISSN 2336-9744 (online) | ISSN 2337-0173 (print) The journal is available on line at www.biotaxa.org/em

Towards an integrative approach to taxonomy of Eriophyoidea (Acari, Prostigmata) - an overview

RADMILA U. PETANOVIĆ1, 2

1Department of Entomology and Agricultural Zoology, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Zemun, Serbia, E-mail: [email protected] 2Serbian Academy of Sciences and Arts, Knez Mihailova 35, 11000 Belgrade, Serbia, E-mail: [email protected]

Received 6 November 2016 │ Accepted 22 December 2016 │ Published online 27 December 2016.

Abstract A contemporary approach to describing species diversity, so called integrative taxonomy, aims to delimit the units of life‘s diversity from multiple and complementary perspectives. An overview of alpha taxonomy of eriophyoid mites, one of the most economically important and speciose groups of the Acari, is presented from its very beginnings at the end of 19th century until today. The analysis follows the development of morphotaxonomy, from the increase of the number of characters visible and distinguishable in slide-mounted specimens, up to the discovery of new characters using LTSEM, CLSM and other modern microscopic techniques. Molecular genetic tools, as one of the complementary segments of the integrative approach and ideally suited for the elucidation of cryptic eriophyoid diversity, have been intensively applied nowadays. All this is considered in the light of improvements of alpha taxonomy of Eriophyoidea moving gradually towards integrative taxonomy.

Key words: phytophagous mites, plant parasites, alpha taxonomy, delimitation of species, morphospecies, cryptic species.

Introduction

Since the late 20th century, when the protection of biodiversity became the center of scientific and public interest in light of the consequences that the erosion of biodiversity could bring to the planet, taxonomy – one of the oldest zoological disciplines — has made a comeback after a long period of unjustified neglect. This was facilitated by the development of new methods and approaches in morphological, ecological and molecular biology studies and as a result, the development of the conceptual paradigm of ―integrative taxonomy‖. ―Integrative taxonomy‖ aims to delimit the units of life‘s diversity from multiple and complementary perspectives (e.g. phylogeography, comparative morphology, population genetics, ecology, development, behaviour). It gives priority to species delineation over the creation of new species names. Traditional morphology-based taxonomy can only discriminate between ‗morphospecies‘, i.e. those based on morphology, according to just one aspect of biological diversity (Dayrat 2005). The same author suggests that traditional taxonomists should describe morphodiversity, analyse the variation of morphological features among individuals and proposed hypothetical morphospecies which should be then analysed using the data from molecular, behavioural, ecological and other approaches (Dayrat, 2005: p. 409). Biological species are

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PETANOVIĆ complex and the delimitation of species using different methods and approaches from collaborative disciplines is useful and should become a standard in taxonomy as a discipline. Eriophyoid mites are obligate plant feeders on all epigean plant parts, although overwintering females of few species have been recorded on root buds (Amrine & Flechtmann, personal communication). They can cause direct damage to their hosts or can transmit agents of serious plant diseases (Oldfield and Proeseler 1996, Malagnini et al. 2016). About 5000 Eriophyoidea species are known worldwide (Navajas and Ochoa 2013). Most of them are highly host specific, with one, or few host species within a single plant genus. Using available data on described species and recorded hosts it was estimated that 80% eriophyoid species feed on only one host species, 95% on hosts within one genus, and 99% within one host family (Skoracka et al. 2010). Eriophyoidea are minute (on average 150-250 μm long), with elongated bodies and annulated opisthosoma, and they are unique in that all motile instars of both sexes have two pairs of legs. Their accurate identification by morphological characters is made difficult by their minute size and simplified body structure and the consequent morphological similarity among species (Lindquist 1996). Eriophyoid morphology for systematic use is almost exclusively studied on cleared and slide-mounted females using phase-contrast light microscopy and those females do not remain suitable for examination permanently. Eriophyoid descriptions still largely follow the standard and the format set by Keifer (1975), the recommendations by Amrine and Manson (1996) and terminology by Lindquist (1996), who reviewed the taxonomic characters and their use in alpha-taxonomy. Recently, recommended procedures and techniques for morphological studies of Eriophyoidea have been contemplated by de Lillo et al. (2010). These authors emphasized that ―today many descriptions and drawings still often do not achieve the required standard and the quality‖ and that ―many relevant taxonomic details may be permanently lost or obscured as a result‖. These shortcomings can lead to incorrect classification or misinterpretation. Moreover, because even the best slide mounted specimens rarely last long, type slides are not obligatory for use as comparable material within the description of the new taxa. Appempts to use dried samples and to recover specimens fixed for years in alcoholic solutions have been reviewed by de Lillo et al. (2010). A protocol for recovering mites from old, collections preserved in liquid by Nalepa was developed and could help in recovery of old species currently listed as nomen nudum or described based on a few details and never described since (Chetverikov et al. 2016). Besides Nalepa‘s collection, Chetverikov et al. (2016) emphasized that there are several additional important old collections of eriophyoids and that accurate revisions and the establishment of digital profiles of these collections is an important goals for the future. Building on the traditional morphological approach to the description of eriophyoid taxa new trends appeared in the last decade, paving the way towards integrative taxonomy. Methods of linear and geometric morphological analysis are applied more frequently, since these can help in distinguishing intraspecific variation, including host-adapted strains or even cryptic species (Amrine et al. 1994, Skoracka et al. 2002, Skoracka and Kuczyński 2006, Navia et al. 2006, Magud et al. 2007, Vidović et al. 2010, 2014, Navia et al. 2015). Moreover, a complex approach using the combined techniques of phase-contrast light microscopy, diffraction interference contrast microscopy, confocal laser scanning microscopy and scanning electron microscopy as well as the sequencing of standard barcoding DNA regions, including the mitochondrial gene COI DNA and the nuclear regions ITS1 and ITS2, enables descriptions of eriophyoid taxa with much more detail than before. These combined techniques have revealed new characters and their cladistic consideration, i.e. polarization of character states into plesiomorphic (or ―primitive‖) and apomorphic (or ―derivative‖) (Chetverikov et al. 2013). For lower taxonomic levels, uncertainties on Eriophyoidea systematics are numerous and molecular techniques can help to answer questions and test hypotheses of different nature, e.g. synonymies and occurrence of cryptic species (Navajas and Navia 2010). Taking into consideration that very little (only 10%) of the eriophyoid mite fauna has currently been described and a huge number of species has been estimated to remain yet undiscovered (Amrine et al. 2003), as well as the small number of eriophyoid taxonomists in the world, we cannot expect that application of the concept of integrative taxonomy of these mites, will be widely accepted any time soon. Instead, more rigorous standards should be proposed and followed in modern morphotaxonomy of eriophyoids suggesting the use of combined techniques and tools when they are available. This contribution presents improvements in morphotaxonomy of this mite taxon from its very beginnings at the end of the 19th century until today. Time intervals were designated according to the periods in which progress in methodology and leading researchers increased the number of described species due to their innovative approaches to taxonomic description. In addition, an effort was made to analyse improvements made in delimitating cryptic species on phenotypic, as well as genotypic levels.

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A simple indicator of progress in the taxonomic study of new species could be the lengths of the descriptions. Until the beginning of the new millennium, they were typically two pages or less (figures included) while currently each description requires 10-30 pages or about a 10-fold increase in recent years.

Morphotaxonomy

Eriophyoids possess a number of structural modifications unique among plant-feeding Prostigmata. They lost legs III and IV, along with the true paired claws of pretarsi I and II. In addition, they lack a discrete respiratory system and have retained few setae on the body and appendages. Perhaps the most important basic morphological adaptations contributing to the success of the superfamily as a whole are their minute size, their annulated body arrangement, unusual mouthparts based on paired pedipalps and 7-9 stylets flanked by robust paired pedipalps (de Lillo et al, 2001) and position of legs facilitating the access of the mites into natural or induced refuges on the host plants. The cuticular structures of eriophyoid mites used in systematics are relatively few compared to those on the majority of acariform mites as a consequence of the considerable reduction and simplification in the body plan of eriophyoids (Lindquist and Amrine 1996). Over 100 traits and over 250 character states can be used nowadays for the morphological delimitation of species. Additional characters with more phylogenetic information (homologous or at least less homoplasious characters) will be of tremendous use in finding more clades and more robust and reliable hypothetical phylogenetic relationships between taxa (Craemer 2010). Only recently new characters of eriophyoid gnathosoma using combined microscopic techniques (Chetverikov and Craemer 2015, Chetverikov and Bolton 2016) have been highlighted. Similarly, cuticle- lined elements of male and female internal genitalia have been described and measured using confocal laser scanning microscopy and a relatively simple protocol for the description of these characters has been proposed (Chetverikov et al. 2012, 2013). In order to follow the improvements in eriophyoid alpha taxonomy, it will be useful to illustrate the set of characters used in the different periods, starting from the very beginning until recently.

1. The earliest period (last decade of 19th century till 1929) The founder of eriophyidology, A. Nalepa, in his early stages of research (late 19th and early 20th century), as well as other authors who investigated eriophyoid mites during this period, namely G. Canestrini, A. Corti, and J. Cotte, in the descriptions of new species used around 30 to 40 morphological features. In the earliest phases there were only around 30, of which only a few utilized precise, quantitative measurements (expressed in mm), while the others were relative or qualitatively expressed. Later morphometric characters were more precise and expressed in micrometers.

Morphometric characteristics used in these early descriptions are presented below:

1. shape of the body 2. shape of the prodorsal shield 3. ornamentation of the prodorsal shield (i.e. description of the shield lines, their position and length, but in many cases ornamention was characterized as ―distinct‖ or ―obscure‖) 4. position of the tubercles of the scapular setae (according to new nomenclature, proposed by Lindquist, 1996 - setae sc) in relation to the rear margin of the prodorsal shield 5. length of scapular setae. In the early descriptions this length was not reported in absolute values, but typically in proportion to the prodorsal shield length. For example in Nalepa‘s papers sc setae were short, longer, or as long as the prodorsal shield itself. Corti (1903) compared the length of setae sc with the number of dorsal annuli (for instance ―setae sc cover the length of 6 dorsal annuli‖), but later their length was expressed in micrometers. 6. shape of the rostrum (former term of gnathosoma) and its position in respect to the body axes (orthognathous or hypognathous ) 7. length of the gnathosoma 8. description of the leg aspect (e.g. ―articulated,‖ ―thin,‖ ―robust‖) 9. relative length of the tarsus in relation to the tibia

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10. number of the rays of the tarsal empodium 11. length of solenidion of legs I and II (according to current nomenclature - ω), first in mm, and later in μm; their shape and position relative to the leg axes (more or less curved). 12. shape and length of the coxal epimera 13. relative length of the sternal line in relation to the coxae I and comment if forked or not 14. position of the coxal setae II (according to current nomenclature - 1a) in relation to the sternal line and the inner margins of the coxal apodemes (epimera) 15. position of the coxal setae I (according to current nomenclature - 1b) 16. shape of the opisthosoma and the size of the anal lobe 17. width of the opisthosomal annuli (with comments – similar or different dorso-ventrally, and notes about ridges, furrows, lateral lobes of the dorsal semiannuli) 18. number of annuli (semi annuli) 19. shape of the dorsal and ventral microtubercles 20. length of the lateral setae (according to curernt nomenclature - c2 ) 21. length of the ventral setae I (according to curernt nomenclature - d) 22. length of the ventral setae II (according to curernt nomenclature - e) 23. length of the ventral setae III (according to curernt nomenclature - f). In Nalepa‘s descriptions, length of the opisthosomal setae was presented in relation to the other setae or in relation to the length of the prodorsal shield. Corti presented length of opisthosomal setae in relation to the equal number of annuli (for instance the length of a given seta was as long as 7 annuli) 24. length of the caudal setae (according to curernt nomenclature - h2) .In Nalepa‘s descriptions this character is descriptive, but Canestrini, Corti and Cotte presented this character quantitatively. 25. presence or absence of the accessory setae (according to curernt nomenclature - h1) 26. width of the epigynium 27. ornamentation of the genital coverflap 28. length of the genital setae (according to curernt nomenclature - 3a). In Nalepa‘s descriptions it was usually expressed in relation to the ventral setae III, Corti expressed their length in relation to the a number of annuli 29. width and shape of the male genitalia (epiandrium) 30. length of the female body 31. width of the female body (behind the rear margin of the prodorsal shield) 32. length of the male body 33. length of the prodorsal shield 34. length of the forelegs (legs I) 35. length of the hindlegs (legs II) 36. length of the leg tarsus II 37. length of the leg tibia II 38. length of the coxal setae III (according to curernt nomenclature - 2a) 39. length of the female genital coverflap (epigynium)

Canestrini (1892a,b) and Cotte (1924) provided average measurements of the length and width of females and the length of all opisthosomal setae. In the later period of his work Nalepa (1921) described new species with the size in μm of the length of the setae sc, legs I and II, tibia and tarsi of legs II, tarsal solenidia of legs I and II, coxal III setae (according to the current nomenclature -2a), lateral and all three pairs of ventral setae, the length and width of the epigynium, and the female and male bodies. In addition, the descriptions were usually complete with data about the origin of the material, type locality, the date and the collector, as well as the name of the host plant species (and the plant family). Detailed descriptions of the symptoms on the host plant provoked by the mite species were supplemented. Drawings of whole mites viewed dorsally and ventrally, and sometimes with the details of the prodorsal shield, as well as drawings of alterations on the host plants (galls, leaf rolling, erinea, etc.), in the Nalepa‘s manner were also included.

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2. Second period (1930–1982) The most active authors in this period were H. Keifer who published between 1930 and 1982, as well as C. Hall Jr., M. Briones and B. McDaniel in the USA; H. Farkas, J. Liro, H. Roivainen, J. Boczek, V. Shevtchenko, M. Carmona, G. Nuzzaci, M. Castagnoli, P. Natcheff, and S. Sukhareva in Europe; G. ChannaBasavanna, M. Mohanasundaram, and S. Mondal in India; K. Lamb and D. Manson in New Zealand; B. Abou-Awad and M. Smith Meyer in Africa; and others. In his descriptions of eriophyoids, besides the above mentioned characteristics, Keifer involved some new items:

40. thickness of the body [according to Shevtchenko et al. (1973)- ―height‖] 41. colour of the mite (based on observations of living mites) 42. width of the dorsal shield 43. length of the antapical setae of the pedipalps (according to current nomenclature - palpal seta d) 44. distance between the tubercles bearing setae sc 45. length of the leg tibia I 46. length of tibial setae (according to current nomenclature - l’) 47. length of the leg tarsus I 48. ornamentation of the coxae 49. position of all coxal tubercles 50. position of the lateral setae on the ventral annulus from the rear coxal apodeme 51. position of the setae d on the annulus 52. position of the setae e on the annulus 53. position of the setae f on the annulus from the last one

ChannaBasavanna (1966), Carmona (1972), Castagnoli (1977), Mohanasundaram (1982) followed Keifer‘s standard in their descriptions, while Liro (1943), Roivainen (1951), and Natcheff (1966) introduced one more feature, length of the cheliceral stylets. Boczek (1961) introduced measurements of the coxal setae 1a and 1b. Farkas (1962) also introduced the length of the caudal setae (in most descriptions from that time, this feature was omitted). Hall (1967) introduced measurements of length of all leg segments (starting from femur) and all leg setae (except unguinal setae) and these measurements were followed by Mondal et al. (1982) and Schliesske (1985) in their descriptions. Briones and McDaniel (1976) measured the length of the femora, femoral setae and the length of patella (genu). Soliman and Abou-Awad (1977) measured the length of all leg segments (starting from femur) and all leg setae (except dorsal tarsal and unguinal setae). Shevtchenko et al. (1973) introduced distance between coxal setae, I, II and III distance from I to II and from coxal setae II to III. Nuzzaci (1975) and Nuzzaci and Vovlas (1977) introduced length of tarsal empodium, while Shevtchenko and Pogosova (1983) introduced measurements of distance between genital setae. Some authors did not strictly follow Keifer in their descriptions, reducing the number of characteristics. For instance, Smith Meyer (1981) did not include the size of the gnathosoma but only its position in relation to opisthosoma. In her study, length of cheliceral stylets and mesasurements of legs were not included, only the relative position of the coxal tubercles and the number of rays in the tarsal empodium. The following characters were added owing to the works of authors who published papers in the field of alpha taxonomy in this period:

54. length of the cheliceral stylets 55. length of the tarsal empodium (according to current nomenclature - em) 56. length of the coxal setae 1b 57. length of the coxal setae 1a 58. distance between the coxal setae1b 59. distance between the coxal setae1a 60. distance between the coxal setae 2a 61. distance from the coxal setae 1b to 1a

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62. distance from the coxal setae 1a to 2a 63. length of the leg femora I 64. length of the femoral seta (according to current nomenclature - bv) of leg I 65. length of the leg femora II 66. length of the femoral setae of the leg II 67. length of the leg genua I 68. length of genual seta (according to current nomenclature - l”) of leg I 69. length of the leg genua II 70. length of the genual setae of leg II 71. length of the anterolateral (paraxial) tarsal setae (according to current nomenclature – ft’) of leg I 72. length of the dorsal tarsal setae (according to current nomenclature – ft”) of leg I 73. length of anterolateral (paraxial) tarsal setae of leg II 74. length of the dorsal tarsal setae of leg II 75. distance between genital setae 3a

Generally, the descriptions of new species included the morphometry of only the holotype female with a few characters of the male allotype. A few specimens on slides and some additional material fixed in ethanol or on dry plant parts were also supplied. Some of the authors, besides the holotype female, started to measure about 10 female individuals (holotype plus paratypes) in order to present individual variability within the species. This was the case of Shevtchenko et al. (1970) in the description of Aceria tritici, providing the morphometry of the holotype and within brackets, the minimum and maximum size of all quantitative traits of 10 individuals. This approach was also used by Sukhareva (1985) and some other authors. At the end of 1960‘s De-Millo (1968) counted the coefficient of variability of 42 traits and realized that some of them were less variable, e.g. number of annuli, length and width of the prodorsal shield, length and width of the genital coverflap, length of the gnathosoma, length of legs I and II, distance between sc, 3a, and coxal setae, and length of setae sc (all together 15 features). Counting the coefficient of correlation among 20 pairs of characteristics she realized that the most correlative were the number of the ventral and dorsal opisthosomal annuli, the length of legs I and II, the length and width of the genital coverflap, the lengths of the gnathosoma and the prodorsal shield, and the distance between the coxal setae. Such correlations were proposed to minimize the number of required quantitative traits to measure within the complex of basic characteristics. Among two correlativelly linked characteristics the one with the lower variation should be chosen. According to De-Millo (1968) the following 12 characteristics form the basic complex: number of dorsal opisthosomal annuli, number of ventral annuli, length of prodorsal shield, length of gnathosoma, length of leg I, length of genital coverflap, distance between scapular setae, distance between genital setae, distance between I coxal setae, distance between II coxal setae, distance between III coxal setae and the length of accessory setae. Apart from this complex of basic characteristics she suggested a complex of alternative characteristics: the ornamentation of the prodorsal shield, the shape of the genital coverflap, the shape of the opisthosomal semiannuli. Additional characteristics are all other measurements. Results of this analysis are interesting and could be used in differential diagnoses in comparing distinctive characteristics. The majority of the authors in this period followed Keifer‘s model in the description of new species, as well as in the details of illustrations. Besides presenting the whole mite (in some cases and for some genera) mostly in the lateral view, Keifer presented illustrations of the following details for the females: prodorsal shield, coxigenital region, antero-lateral mite with the details of legs I (almost always) and II (sometimes), magnified lateral view of the opisthosoma (in order to show differences in the distribution and shape of dorsal and ventral microtubercles), magnified tarsal empodium in frontal position (in order to present secondary branches within the main one) and the internal sclerotized parts of female genitalia, where the transverse apodemes, longitudinal bridge, spermathecal tubes and spermatheca are shown. Moreover, external male genitalia were sometimes drawn, but not always. Because Keifer (1942) coined the term and explained deuterogyny within eriophyoid mites, in the cases of structural polymorphism, deutogyne females were also described and illustrated. Compared with the early period (Nalepa‘s period) the number of characteristics important for the descriptions of new species in this second period (Keifer‘s period) was doubled.

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It should be emphasized that variability of phenotypic traits between populations of mites living on different closely related host plants or interspecific similarities or differences of congeneric species living on closely related hosts with the aim of their delimitations, began in this period in papers published by Roivainen (1947, 1951), Lamb (1953), Proeseler (1972), Boczek et al. (1976,), Sukhareva (1981) and others.

3. The third period (1983-2000) The most of the alpha taxonomic papers published in this period were authored by: J. Boczek, G. Nuzzaci, E.de Lillo, R. Petanovic, S. Sukhareva, A. Skoracka, G. Soika and G. Labanowski in Europe; A. Chandrapatya (in collaboration with J. Boczek), M. Mohanasundaram,S. Mondal, S. Chakrabarti, H. Kuang, and F. Kadono in Asia; C. Flechtmann and J. Amrine in the Americas; M. Smith Meyer and E. Ueckermann in Africa; and others. In this period the number of morphological characteristics used for species descriptions was more or less stabilized. Some authors like Smith Meyer and Ueckermann (1989, 1990) in descriptions of new African Eriophyoidea, presented only measurements of the whole legs, although with neither the separate leg segments, nor the lengths of leg setae. Some new characteristics were considered by Kadono (1992):

76. distance between the setae c2 77. distance between the setae d 78. distance between the setae e 79. distance between the setae f

A holistic approach to describing the morphology of species has been accepted by the majority of authors. So, besides the detailed description of the protogyne female, descriptions of deutogyne females, males and juveniles were added (Shevtchenko and Pogosova 1983, Bagnjuck 1984, Petanović and Boczek 1990, 1991). In this period many authors, for example de Lillo (1988, 1994, 1997), Petanović and de Lillo (1992), in addition to measuring the holotype female, included the span of measurements of at least 10 individuals (paratypes + holotype). Along with semischematic line drawings in Keifer‘s manner, SEM photographs were added by some authors. These photographs presented whole mites in different views, e.g. the prodorsal shield, the coxigenital region of females and males, legs, tarsal empodium, solenidion, lateral view of opisthosoma, posterior opisthosoma. These photographs served mainly to confirm the image seen under the phase contrast light microscope. Such, more complex descriptions were published by Schliesske (1985), de Lillo (1988), Boczek and Nuzzaci (1988), Amrine et al. (1994), Kuang (1995), Craemer et al. (1999), Soika and Labanowski (1999), Chandrapatya et al. (2000), Flechtmann (2000), Skoracka and Boczek (2000) and others. Along with the inclusion of more than one individual in the description of a new species, studies of phenotypic intraspecific variability continued to be the subject of interest in eriophyidology in this period and results were published by Boczek et al.(1984), Boczek and Kozlowski (1985), Petanović (1990), Sukhareva (1992), Amrine et al. (1994), Petanović and Dimitrijević (1995), and others. The work of Amrine et al. (1994), providing redescriptions of three species and detailed description of two new species of the genus Cecidophyopsis, is illustrative and represents a new approach to the description in eriophydology. Besides the detailed comparative analysis of 18 selected distinctive characteristics, detailed semischematic drawings of the prodorsal shield, coxigenital region, lateral opisthosoma, both pairs of legs, tarsal empodium and internal sclerotized female genitalia were enclosed, followed by excellent LT SEM photographs. In this paper new characters, never used before were measured:

80. length of the basal or palpcoxal setae (in later papers assigned as - ep) 81. apicoventral palpal setae - v 82. relation of the position of the femoral setae bv of leg I 83. relation of the position of the tibial seta l’ 84. relation of the position of the femoral setae bv of the leg II 85. number of the annuli in the coxigenital field between coxae and coverflap 86. number of the microtubercles in the row I 87. number of the microtubercles in the row II

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88. number of the microtubercles in the row III 89. number of the microtubercles in the row IV

All paired setae were measured separately (left as well as right). Aside from that, the number of microtubercles from left to the right of each tubercles of the corresponding opisthosomal setae was enclosed as well as the number of microtubercles in each of 6 terminal ventral annuli. In the previous descriptions only a few characteristics of males were measured. In the study by Amrine et al. (1994), the description of male did not differ in comparison with the description of females. In the monograph about fundamental knowledge on morphology, biology, ecology and economic importance of Eriophyoidea, Lindquist (1996) established a new nomenclature of all body setae in Eriophyoidea and from that time successively in almost all papers this nomenclature has been accepted, and the measurements of all body setae became obligatory. Thus, Flechtmann (1998) besides already measured characters included:

90. unguinal seta - u’ Huang et al. (1996) included one trait more which was only descriptively stated before (sc ahead of the rear shield margin or sc tubercles on the rear shield margin): 91. distance from sc tubercle and the rear shield margin (Dt-Sr).

As a part of this new approach which started in this period, aside from the distinctive diagnosis in relation to the most similar species, authors very often enclose comparison between a few similar congeneric species from closely related host plants. Besides all the mentioned characters, some specific plesiomorphic characters of the representatives of the family Phytoptidae like the following were also included: unpaired inner seta vi, paired outer anterior setae ve, subdorsal setae c1, as well as tibial solenidion φ. Within the representatives of the subfamily Phyllocoptinae besides the length of whole prodorsal shield, the length of lobe over gnathosoma was separately measured which enlarges the number of characteristics to approximately 100.

4. Recent studies (2001-2016) The beginning of the new Millennium is characterized by the essential progress in alpha taxonomy of Eriophyoidea and the tendency of authors to apply integrative approach in describing new species. It could be mainly due to the editorial lines of representative journals with higher impact factors, the improvements of techniques, the reductions of the costs of the tools, instruments and chemicals; rapid communication via internet and the possibility to combine results of more authors, etc. This tendency of authors of the new age to use complex data and to join efforts with co-authors of different interests coincide with the crisis in taxonomic research at the end of the 20th century. Although new integrative approaches have been theoretically widely accepted, it presupposes the use of new methods together with traditional approaches used before. In this period most papers in the field of alpha taxonomy of Eriophyoidea were published by: K-W. Huang, C. Flechtmann, A. Skoracka, E. de Lillo, D. Navia, J. Amrine, P. Chetverikov, R. Petanović, G. Ripka, B. Vidović, C. Craemer, D. Knihinicki, M. Lewandovski, X-Y. Hong, X-F. Xue, D. Pye and others. In this subchapter the complexity of morpho-taxonomy in the newest studies concerning the descriptions, and /or supplementary descriptions of eriophyoid species will be presented. In order to avoid wide variations among authors in describing new species Amrine and Manson (1996) and later Amrine et al. (2003) gave very detailed instructions regarding the content of scientific papers in which new species would be presented: characters to be measured, how they should be measured, their contemporary nomenclature, how to shape the text, how to illustrate, what are the standardized abbreviations in marking certain parts, etc. Most authors who published in the field of alpha taxonomy from the end of the last and the beginning of the new Millennium followed cited instructions. It is typical to measure protogyne female designated as the holotype, and 9 paratype females. Numeric value of the holotype characteristics are followed (in brackets) by the span of minimum and maximum according to the 10 measured individuals. Males (one is assigned as the allotype), deutogyne females, nymphs and larvae (all instars and forms), are often measured too. Number of males, deutogyne females and juveniles could be less than the number of protogyne females. Besides morphometric characters, descriptions now contain meristic characters, as well

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TOWARDS AN INTEGRATIVE APPROACH TO TAXONOMY OF ERIOPHYOIDEA as qualitative characters. Host plant species, the family of the host plant, type material (with locus typicus with the details like GPS coordinates and the name of the collector), relation of the eriophyoid species to the host, etymology, differential diagnosis and short remarks or discussion regarding the diagnostic characters are always a very useful supplement of the description. It is obligatory to include semischematic line drawings of the structural elements of the body. Very frequently they are followed by scanning electron (SEM), light phase contrast (LPCM), differential interference contrast (DIC) or confocal laser scanning (CLSM) microphotographs which additionally illustrate the distinctive characters of the new species. In contemporary descriptions, tables with comparative data of characteristics of the new species and the species stated in differential diagnosis are often included. Examples of such descriptions could be found in the following papers: Boczek et al. (2002), Domes (2005), Malandraki et al. (2004), Navia and Flechtmann (2005), Hong and Xue (2005), Chetverikov (2005), Skoracka and Czarna (2007), Petanović and Rector (2007), Denizhan et al. (2007), Petanović and Vidović (2009), Pye and de Lillo (2010), Vidović (2014), Ripka and Ếrsek (2014). However, there were and still are, many deviances from these instructions that are addressed in manuscript peer reviews; such manuscripts are typically rejected or evaluated for major revisions (E. de Lillo, personal communication). It should be mentioned that nowadays along with the descriptions of new species, additional descriptions and redescriptions of species named long ago are undertaken. In previous times many characteristics could not be seen because of the limitations of older microscopes or mites were very simply described or just proposed as nomen nudum. In many species juvenile instars, dimorph adult forms or males were not described, so they are described afterwards. Additional descriptions and/or redescriptions can be found in following papers: Skoracka et al. (2004), Petanović et al. (2007), Vidović et al. (2008), Chetverikov (2011), Vidović (2011), Beaulieu et al. (2015), Chetverikov et al. (2014a), Flechtmann et al. (2015), and Xue et al. (2015). The impact of slide mounting practice (with or without fibers) on the appearance of the shield pattern was emphasized as an example of possible erroneous conclusions on mite identification (Denizhan et al. 2008). Similarly, in addition to the description of a new species from all motile stages, Flechtmann (2009) used in his description non-flattened and flattened specimens. His analysis of more than 100 specimens clearly indicated differences in the shape of prodorsal shield, its length, insertion and the position of setae sc. It was concluded that study of differently mounted specimens (flattened and not flattened) and of the immatures, is necessary and will lead to a reappraisal of some morphological characters commonly used in keys and the description of the Eriophyoidea. Huang (2001a, 2001b, 2005) and Huang and Wang (2003, 2004) described many new species from Taiwan (10-20 per paper). Although they do not follow entirely these standards, they also use some specific marks for the distance between tubercles, for instance: Dt-Dt - distance between tubercles sc, Ct1-Ct1- distance between tubercles 1b, Vt2-Vt2- distance between tubercles e, etc. They use diagonal distances between coxal and opisthosomal setae, characters proposed by Shevtchenko et al. (1973), but not measured by the most contemporary taxonomists.Besides, they measured only holotype, the allotype is very frequently omitted, as well as juveniles, and variability of measurable characters is not possible to anticipate. This deviation from standard makes it more difficult to compare newly described species from Taiwan with similar species described by other authors. In the period after 2010 morphotaxonomy became more complex, owing to the new microscopic techniques (above all SEM and CLSM). These techniques greatly helped to discover new characteristics which were invisible before and could not be objects of analyses. Until recently SEM photographs were only sporadically, but not routinely incorporated in taxonomic articles. Although SEM started to be used in eriophydology since the early 1980‘s, these microphotographs were moreover largely used to enhance and confirm illustration of characteristics already seen under light phase contrast microscope. No one additional morphological information was defined or discussed from these SEM supplements. Such examples could be found not only in the pepers published in previous period, but also in the papers of Huang and Wang (2004), Petanović and Rector (2007), etc. More complex descriptions of the new taxa since 2010, appeared in the papers of Craemer (2010), Chetverikov et al. (2012, 2013, 2014b), Chetverikov and Petanović (2016a),, Guo et al. (2015), Navia et al. (2015), Petanović et al. (2015), Duarte et al. (2016), etc. Craemer (2010) describing three new species from the genus Diptilomiopus, used the so called low- temperature SEM (cryo-SEM) which seems to be the most successful in obtaining highly magnified, largely artefact-free images, and particularly minimizing shrinkage. The descriptions were more detailed than the norm for Eriophyoidea species descriptions (on over 60 pages) including characters described from SEM

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92. length of idiosoma ( body without gnathosoma) 93. body width at the level of setae f 94. base width of the prodorsal shield 95. number of the dorsal microtubercles/ 20μm 96. number of the ventral microtubercles/ 20μm 97. number of the microtubercles between setae d 99. number of the microtubercles between setae e 99. number of the microtubercles between setae f 100. number of the dorsal annuli laterally to the prodorsal shield 101. number of the annuli clearly forming central ridge 102. length (including coxa) including extremities 103. length (including coxa) excluding extremities 104. trochanter length (in dorsal view)

Chetverikov (2012) introduced the use of confocal laser scanning microscopy (CLSM) as a powerful modern technique that can be used for studying the external and internal anatomy of Eriophyoidea. It allows the capture of precise digital images of the fine details of external and internal chitinous structures, which can be further analyzed using computer software. This is possible because the exoskeletons of mites and ticks, as well as other arthropods exhibit a very strong autofluorescence signal which makes them highly suitable for CLSM without additional staining with fluorochromes. CLSM seems to be an effective tool for comparing closely related and/or cryptic species, correcting diagnoses of poorly described taxa, studying immature instars, and particularly, for studying the structures and the functioning of the internal genitalia of adult females and males. Using this microscopic technique Chetverikov et al. (2012, 2013) suggested measurements of characteristics of the spermathecal apparatus and apodemes of the internal female genitalia as new characters in describing species. In his latest synthetic studies, Chetverikov (2014, 2016) unified and specified measurable characteristics of internal sclerotized parts of female genitalia, proposing and using them in descriptions of the new species.

105. spermatheca length (Ls) 106. spermatheca width (Ws) 107. Assymetry A (ratio of the half of the length and the whole length of the spermatheca) 108. Elongation Es (ratio of the width and length of the spermatheca) 109. length of the distal segment of spermathecal tube (Lt) 110. width of the distal segment of spermathecal tube (Wt) 111. elongation of the distal segment of spermathecal tube Et (ratio of the length and width of the distal segment) 112. length of the proximal part of the spermathecal duct 113. length of the anterior (prespermathecal part) of the longitudinal bridge La 114. length of the posterior (postspermathecal part) of the longitudinal bridge Lp 115. length of the ventral X-projection of transverse genital apodeme, Lx 116. basal width of the transverse genital apodeme, Wg1 117. apical width of the transverse genital apodeme, Wg2 118. half-length of the transverse genital apodeme, Lh 119. triangularity T of the transverse genital apodeme (ratio of the apical and basal width) 120. hight/width ratio of the transverse genital apodeme, R

Besides these already mentioned characters, Chetverikov et al. (2014b) introduced angle morphometrics of the spermathecal structures:

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121. Angle betwen the left spermatheca and the longitudinal bridge, SB1

122. Angle betwen the right spermatheca and the longitudinal bridge, SB2

123. Average angle between the spermatheca and the longitudinal bridge (SB1+ SB2/2)

124. Angle between the left spermathecal tube and the spermatheca, ST1

125. Angle between the right spermathecal tube and the spermatheca, ST2

126. Average angle between the spermathecal tube and the spermatheca, ST (ST1+ ST2/2)

127. Angle between the left spermathecal tube and the longitudinal bridge, TB1

128. Angle between the right spermathecal tube and the longitudinal bridge, TB2

129. Average angle between spermathecal tube and the longitudinal bridge, TB (TB1+ TB2/2)

Apart from the view into the internal sclerotized parts of the female and male genitalia, quantitative or qualitative, CLSM images of the gnathosoma enabled detection of new structures that were described by Chetverikov and Petanović (2016a). In addition, a previously neglected genital structure of eriophyoids, the thorn-like spermathecal process (corniculus), was discovered with the aid of confocal laser scanning microscopy (Duarte et al. 2016). Besides the above mentioned characters this paper introduced new measurements such as:

130. length of the corniculus 131. length of the oblique apodeme 132. length of the additional perpendicular apodeme

Although CLSM has seldom been used in acarology and very rarely for studying eriophyoid mites until recently, as an innovation at Saint Petersburg State University (Russia), it seems that for the study of undoubtedly very important characters of internal genitalia and gnathosoma, this method should be applied as a routine procedure in the new taxonomic descriptions in the future. The limitating factor for application of CLSM is the small number of laboratories that currently possess such equipment. Along with the new characteristics involved, studies of phenotypic variability have become much more represented in many papers. A quantitative approach, with appropriate sample sizes and restrictive statistical testing, was initiated by Skoracka et al. (2002), and followed by similar studies using linear morphometric or geometric approaches, e.g. Navia et al. (2006), Skoracka and Kuczyński (2006), Magud et al. (2007), Vidović et al. (2008, 2014).

Relation to the host, biology and ecology

Earlier descriptions of eriophyoid species have frequently contained only the names of the host plant species, eventually alternative host plants and a very short description of the symptoms. Some authors, like Canestrini (1892a, b), Corti (1917), Cotte (1924), Liro (1940, 1941) included drawings of symptoms mite infestation of host plants, in addition to the drawings of mites themselves. Later, Wilson (1959), ChannaBasavanna (1966), Briones and McDaniel (1976), Schliesske (1985), Kuang (1995), de Lillo and Sobhian (1996), Craemer et al. (1999), and Vidović and Petanović (2008) included the photographs of the symptoms. Apart from showing photographs of the symptoms, Castagnoli (1973, 1978, 1991) described in detail the biology of the mite species and the development of the provoked symptoms. Bagdasarian (1970), along with the description of a new species Eriophyes armeniacus, also described its life cycle in detail. Chandrapatya (2004), along with the description of the morphology of the new species Phyllocoptes azadirachtae, studied in detail its life history parameters. Together with the more detailed descriptions of the morphological characters of eriophyoid species, relation to the host plant, microhabitat and elements of biology and behavior have recently added more details that contribute to a more complex overview of newly described taxa (Chetverikov et al. 2013, Vidović et al. 2016, Chetverikov and Petanović, 2016b,c). One interesting example is the discovery of an obligate phoresy of Aceria pallida Keifer using the psyllid Bactericera gobica Loginova for transportation as well as for hibernation (Liu et al. 2016).

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Cryptic species (molecular approach)

Undetected genetic diversity and cryptic species complexes obstruct our knowledge of biodiversity and our understanding of the processes of speciation. Cryptic complexes are groups of individuals whose morphological similarity masks a measurable level of genetic, as well as physiological, behavioral, or ecological diversity, and reproductive isolation. The potential for high host specialization, host-race formation, and cryptic speciation are particularly great in eriophyoid mites because they are often intimately associated with their hosts, lack long- range host seeking ability and have high reproductive rates (Sabelis and Bruin 1996; Magalhães et al. 2007). The existence of undetected cryptic lineages is a result of host-associated genetic differentiation (Magalhães et al. 2007, Skoracka et al. 2010). Molecular genetic tools, which have begun to be employed in studies of eriophyoid mites (Navajas and Navia 2010), are ideally suited to the elucidation of cryptic eriophyoid diversity and should advance mite taxonomy. Indeed, recent evidence from molecular studies suggests that species complexes in eriophyoid mites may be far more common than previously understood (Carew et al. 2009, Skoracka and Dabert 2010). Six years ago the number of nucleotide sequences deposited in GenBank for Eriophyoidea was 207. Nucleotide sequences belonged to a reduced number of species, viz. 21 species from six genera: Aceria, Calepitrimerus, Cecidophyopsis, Colomerus, Eriophyes and Floracarus included in the family Eriophyidae (Navajas and Navia 2010). At that time there was no information available on Phytoptidae and Diptilomiopidae. At present, 1737 nucleotide sequences of Eriophyoidea (from all three families) are deposited in GenBank (www.ncbi.nlm.nih.gov accessed on October 20, 2016). The majority of the data originate from phylogenetic studies (e.g. Li et al. 2014, 2016, Chetverikov et al. 2015). Species sequences belong to 13 phytoptid genera, 51 eriophyid genera and 10 diptilomiopid genera are available. Here, several examples of studies that were undertaken recently combining data on nucleotide variation and more traditional morphological features are presented. This integrative approach can help in establishing reliable criteria to determine species in Eriophyoidea. Most papers published today concerning alpha–taxonomy are prepared following traditional methods but there are increasing numbers of new eriophyoid species descriptions employing methods of traditional taxonomy combined with the support of DNA sequences of one (typically mitochondrial DNA cytochrome oxidase subunit I - COI) or a few gene fragments. Skoracka (2009) described a new species of grass-feeding eriophyoid mite Abacarus lolii as a cryptic species of Abacarus hystrix (Nalepa) suggesting that it can be effectively separated using mitochondrial DNA cytochrome oxidase subunit I sequences. Skoracka et al. (2012) investigated wheat curl mite (WCM), Aceria tosichella (K.) populations from different host plants in Australia, South America and Europe and tested the hypothesis that WCM is, in fact, a complex of cryptic species, using morphological data in combination with nucleotide sequences of the mitochondrial cytochrome c oxidase subunit I (COI) and nuclear D2 region of 28S rDNA and internal transcribed spacer region (ITS1, ITS2) sequences. The results of their investigations suggested that what has been recognized historically as a single species is, in fact, a complex of several genetically isolated evolutionary lineages that demonstrate potential as cryptic species. Miller et al. (2013) analyzed genetic variation and phylogenetic relationships among WCM from four continents and a wide range of host plants using DNA sequence data from one mitochondrial gene, one nuclear gene and a single nuclear intergenic spacer region. Phylogenetic analyses revealed 11 unique mite lineages associated with specific plant hosts including wheat and barley. Chetverikov et al. (2012, 2013) described the new species Oziella sibirica and Loboquintus subsquamatus using complex morphological studies supported by a partial mitochondrial COI sequence. Lewandowski et al. (2014) assessed morphological and genetic variation of seven Trisetacus species originating from six coniferous hosts in Poland by morphometric analysis and molecular sequencing of the mitochondrial cytochrome oxidase subunit I gene and the nuclear D2 region of 28S rDNA. The results confirmed the monophyly of the genus Trisetacus as well as the monophyly of five out of the seven species studied. Vidović et al. (2015) described a new species of eriophyoid mite, Metaculus diplotaxi n. sp. inhabiting Diplotaxis tenuifolia along with their investigation of interspecific variability between Metaculus spp. on three different Brassicaceae host plants.Analysis of MT-CO1sequences supported the results obtained from the analysis of morphometric features. Petanović et al. (2015) described a new genus Eriocaenus and a new species Eriocaenus ramosissimi. The differential diagnosis between Eriocaenus equiseti and the new species was supplemented by molecular differentiation of 28S rDNA sequences including D2 fragments for both mites. Guo et al.

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(2015) used DNA barcoding in order to separate protogyne and deutogyne forms of the newly described species Tegolophus celtis. The putative protogyne and deutogyne forms of T. celtis were identified by using fragments of three genes, a COI and two nuclear genes (18S rRNA and 28S rRNA). Cvrković et al. (2106) showed that hazelnut big bud mite, Phytoptus avellanae, one of the most harmful pests of Corylus spp. represents a complex of two cryptic species: one that lives and reproduces in buds causing their enlargement (‗big buds‘) and the other, a vagrant living on leaves; based on phylogenetic analyzes of (COI) DNA and the nuclear D2 region of 28S rDNA sequences. Molecular analysis also revealed that atypical flattened nymphs (Tegonotus-like nymphs) with differently annulated opisthosoma, which appear in the life cycle of P. avellanae s.l., belong to a ‗vagrant‘ lineage, i.e. a vagrant cryptic species. Recently, the new species Aceria artemisiifoliae was described following both morphological and bio-molecular approaches, and has been considered as potential important biological control candidate of common ragweed, Ambrosia artemisiifolia (Vidović et al. 2016). In addition to advantages of the molecular approaches listed by Navajas and Navia (2010) in reconstruction of Eriophyoidea phylogeny, management strategies for eriophyoid pests, establishment of efficient biological control strategies, and interception of potential invaders, for lower taxonomic levels molecular techniques could help to answer questions and test hypotheses of synonymies and occurrence of cryptic species.

Final considerations

Eriophyoidea represents the second most economically important superfamily of crop pests among the Acari. It is also the group with the highest number of species, includes the most mite species that transmit plant viruses, and includes numerous released and potential biological control agents of invasive weed species. The number of alien and/or invasive species of these mites is increasing. For these reasons, together with the importance of the knowledge of their diversity and other aspects of taxonomy, systematics and phylogeny, there is a need to introduce new methods (more subtle microscopic as well as molecular tools) and an integrative approach to taxonomy of eriophyoids. An overview of alpha taxonomy of Eriophyoidea from the very beginnings to the recent studies indicates not only the involvement of numerous characteristics, but also improvements in the use of a variety of methods, involvement of all developmental stages of both sexes and seasonal forms, and larger numbers of individuals in order to get information about population variability, biology and life histories. Using advanced microscopic methods, new, previously invisible or indistinguishable characters are now described. Moreover, studies of the impact of these mites to their host plants, their life cycles, and behavior, more often become part of new descriptions or additional description of existing eriophyoid taxa. Molecular genetic tools, which are ideally suited for the elucidation of cryptic eriophyoid diversity and have recently begun to be employed in studies of eriophyoid mites, are more intensively applied. From the analysis presented it could be concluded that a more complex approach to the taxonomy of this group is accepted by many contemporary researchers. This should advance investigations into eriophyoid mite taxonomy and pave the way towards an integrative taxonomy in the future.

Acknowledgements I am grateful to Dr. Carlos H. W. Flechtmann (Senior Professor, Departamento de Entomologia e Acarologia, Escola Superior de Agricultura ―Luiz de Queiroz‖, Universidade São Paulo, Piracicaba, São Paulo, Brasil, CNPq-Brazil Researcher) and to anonymous reviewers for their critical comments of the manuscript. I also thank Dr. Brian G. Rector (USDA-ARS, Great Basin Rangelands Research Unit, Reno, USA) for his comments and linguistic corrections. This work was partly supported by research grant of Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant # III 43001) and by research grant of Serbian Academy of Sciences and Arts (Grant #F- 195).

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