Acarina 16 (2): 79–130 © Acarina 2008

DIAPAUSE AND QUIESCENCE AS TWO MAIN KINDS OF DORMANCY AND THEIR SIGNIFICANCE IN LIFE CYCLES OF MITES AND TICKS (CHELICERATA: ARACHNIDA: ACARI). PART 1. ACARIFORMES V. N. Belozerov Biological Research Institute, St. Petersburg State University, Peterhof 198504, Russia; e-mail: [email protected]

ABSTRACT: A review of available data on diapause and quiescence as two main kinds of dormancy in life histories of the acari- form mites (Arachnida: Acari), particularly of Oribatida, Astigmata and Prostigmata, and on the role of both dormant states in life cycles of these mites due to their adaptations to predictable (seasonal) and unpredictable (irregular) environmental changes. The survival during periods of adverse conditions is enabled in the acariform mites by both kinds of dormancy controlled either endog- enously (diapause), or exogenously (quiescence), and also in both ways. However, the role of dormancy in the control of life-cycle seasonality, well known for diapause, is doubtful for the common form of quiescence, arisen as a direct response to unfavorable environmental changes at any life-cycle stage, and called as “the stage-independent quiescence”. However another form, ascer- tained in insects as “the post-diapause quiescence”, and characteristic of many acariform mites also, is of great significance for seasonal time-adjustment in both these groups of terrestrial arthropods. Similar function is characteristic probably of “the stage- specific quiescence” ascertained theoretically for insects. Representatives of the Acari reveal a high diversity of the life-cycle seasonal control systems (from plesiotypic types with numerous diapause-capable ontogenetic stages up to apotypic types with single or limited number of such stages, also enabling the reliable life-cycle seasonality). An adaptation to environmental unpredict- ability in mites with plesiotypic systems is based on overlapping flexible life cycles (with capability of some stages for quiescence also), while in mites with apotypic systems — on special resting stage (often with phoretic dispersal). A combination of diapause and post-diapause quiescence known in many extant prostigmatid mites is suggested as an initial ancestral state of dormancy in adaptations of acariform mites (particularly of Oribatida) to adverse environmental changes. Such a hypothesis gives reason- able solution of controversial interpretations concerning the nature of dormancy in extant oribatid mites during their hibernation.

KEY WORDS: Acariform mites, life history, life-cycle control, dormant stages, diapause, quiescence, post-diapause quiescence

INTRODUCTION The alternation of active and dormant stages present paper I continue this study, paying atten- is an especially conspicuous trait in life histories tion to the diversity of dormant states in the Acari, of invertebrate animals (in particular of insects, in particular to the presence and properties of two crustaceans, arachnids and other arthropods) that main kinds of dormancy (diapause and quies- determines duration, phenology, flexibility and cence) in their life cycles, and to relationships other peculiarities of their life cycles. Such alter- (ecophysiological and evolutionary) between nation of activity and dormancy in life cycles of these opposite types of dormant state. As before, I arthropods reflects deep adaptations to both regu- try to retain a comparative and partly taxonomic lar and irregular environmental changes in their approach to the problem during the description habitats. For all animal and plant inhabitants of the and analysis of data concerning dormancy in mites Earth with its regular and predictable (seasonal, and ticks. The first part of this review is devoted to daily), and unpredictable (occasional, irregular) representatives of the acariform mites (Oribatida, changes of environment, the ability for dormancy Astigmata and Prostigmata), as they are consid- is of great vital importance. Naturally, this phe- ered in the system used by Evans (1992) and Keth- nomenon (with all its diversity in destinations, ley (1982). Some comments due to the contempo- mechanisms and manifestations) has attracted rary taxonomy of Acariformes (Mironov and much attention from biologists of different profile, Bochkov, in press) are given in footnotes. dealing with different invertebrates, in particular with terrestrial and aquatic arthropods. GENERAL CHARACTERISTICS OF DORMANCY IN ARTHROPODS Concerning the Acari (mites and ticks), some aspects of this question, particularly the number The ability to survive in a dormant state is a and distribution of dormant stages in their life cy- widespread feature among invertebrates, as is cles, and possible evolutionary changes in their shown in the comprehensive review of Cáceres ontogenetic systems connected with adaptation to (1997). It is characteristic (either in inducing and climate seasonality, were considered in two my enforcing the dormancy at regular ontogenetic in- previous papers (Belozerov 2007, 2008b), as well stars, or in producing the specialized resting stag- as in a review on the ontogenetic phenomenon of es, or both) of most groups of invertebrates from calyptostasy, characteristic of the prostigmatid the protists and sponges through the hemichor- parasitengone mites and related in some degree to dates. The highest capability for survival in dor- seasonal adaptations (Belozerov 2008a). In the mant state is found in the rotifers, nematodes and 79 V. N. Belozerov tardigrades, but our best insights into the nature dormancy, while diapause as a prospective dor- and regularities of dormancy relate to the arthro- mancy (Ushatinskaya 1973, 1976; Saulich 1999). pods (particularly insects and crustaceans). Whenever quiescence has a seasonal basis, it is It is essential that dormant stages in arthro- called non-diapause dormancy (Tauber et al. 1986; pods enable not only their survival during unfa- Siepel 1994). It is possible also to call quiescence vorable harsh seasons, but also the conformity of an enforced dormancy, while diapause is an in- their life cycles with environmental changes, in duced dormancy (Gurney et al. 1994). particular the synchronization of active develop- Diapause is the more diverse of the two. Clas- ment and reproduction with favorable seasons sified according to destination it may be either a (Lees 1955; Danilevsky 1961; Saunders 1982, hibernation (winter diapause), or an aestivation 2002; Zaslavsky 1984; Tauber et al. 1986; Danks (summer diapause); according to the approached 1987; Saulich 1999; Saulich and Volkovich 2004 ontogenetic instar it may be an egg (embryonic), — for insects; Elgmork 1980; Alekseev 1990; larval, nymphal or adult (imaginal, reproductive) Dahms 1995; Alekseev and Starobogatov 1996; diapause; while according to the program it is Brendonck 1996; Fryer 1996; Hairston and Cáceres obligatory or facultative. According to ecological 1996; Cáceres 1997; Alekseev et al. 2007 — for and physiological mechanisms of its incidence crustaceans). The same concerns the representa- and termination diapause was classified by Müller tives of chelicerate arthropods, in particular the (1970) into three types of dormancy: parapause acarines (Belozerov 1982, 2007; Veerman 1985, (an obligatory hereditary arrest of development or 1992; Walter and Proctor 1999; Wohltmann 2001) activity arising in every generation at a species- and spiders (Schaefer 1987), as well as other in- specific instar), oligopause (an arrest of develop- vertebrates. From an ecological standpoint, dor- ment or activity with control of its induction, mant stages are much more common among inver- maintenance and termination, similar for all these tebrates from terrestrial and fresh-water habitats periods), and eudiapause (also a facultative arrest than in taxa with exclusively or mainly marine of development or activity with different control- representatives (for the crustaceans see Alekseev ling mechanisms of induction and termination, and Starobogatov 1996; Hairston and Cáceres e.g. through photoperiod and chilling respective- 1996). Among parasitic arthropods, dormant stag- ly). In general, this subdivision of diapausing ar- es are characteristic only of temporary parasites, rests is recognized until now (Saunders 2002), and are almost absent in permanent parasites. though there have been modifications both by Two basic types of dormancy differ in their Müller (1992) himself, and by other entomologists fundamental ecophysiological properties (Shel- (Mansingh 1971; Thiele 1973; Ushatinskaya 1973; ford 1929), as recognized now by all students of 1976; etc.). There is a meaning, however, that this phenomenon in insects (Emme 1953; Lees elaborated systems hardly are viable (Danks 1987; 1955; Danilevsky 1961; Müller 1970, 1992; Ush- Koštal 2006). atinskaya 1973, 1976; Tauber et al. 1986; Danks The majority of insects enter diapause at a 1987; Saunders 2002; Saulich and Volkovich single species-specific stage in their life cycle. 2004; Vinogradova 2007; etc.) and crustaceans However some of them are capable of generating (Alekseev 1990; Alekseev and Starobogatov 1996; dormancy in different (two or more), but also spe- Brendonck 1996; Cáceres 1997; Alekseev et al. cies-specific instars. There are known cases in 2007; etc.). Quiescence is an arrest of develop- which diapause is combined with quiescence in ment or activity arisen under direct impact of ei- different instars and stages of life cycle, or at the ther adverse environmental conditions, or deficit same instar, e.g. in species with summer diapause of vitally essential factors, that is due to some ex- followed by the autumn-winter quiescence after ogenous constraints, and recovered after cessation diapause termination (Katsoyannos et al. 2005). of their action. By contrast, diapause is an antici- Such a combination is more common, undoubted- pated arrest of development or activity arisen ac- ly, in insects with winter diapause followed by cording to internal program, either genetically winter quiescence (Koštal 2006). fixed, or induced through effect of token factors While not as diverse as diapause, the state of signalling in time an approach of unfavorable con- quiescence varies somewhat with regard to its des- ditions, and eliminated by special mechanism of tination and mechanisms. According to destina- reactivation. Due to their main traits, quiescence tion it can be either hibernating, or aestivating, was considered by Müller (1970) as a consecutive while in respect to the generating factors (cold,

80 Dormancy and their significance in life cycles of mites and ticks drought, lack of oxygen etc.) it may be considered sonal control of life cycles in ixodid ticks — see as a case similar to some forms of anabiosis (cryp- Belozerov 1982, 1988), that biennial and perennial tobiosis), e.g. cryobiosis, anhydrobiosis, anoxybi- life cycles, involving some instars with one-year osis etc. (see Schmidt 1955; Keilin 1959; Ushatin- duration, are comparable by their regulation with skaya 1990; Clegg 2001), though with not as deep univoltine development, inasmuch as they are also an inhibition of metabolism (Alekseev et al. 2007). controlled by different mechanisms that can com- It is well known that quiescence is possible, as a bine a number of various dormant stages. rule, at any instar (or stage), and this type of dor- DORMANCY IN THE ACARI mancy has been termed “stage-independent quies- cence” (Gurney et al. 1981). However, special From an analysis of dormant stages distribu- “stage-specific quiescence” is capable of synchro- tion in mites and ticks, given in my previous re- nizing particular cases of seasonal development views (Belozerov 2007, 2008b), the main pecu- (instead of diapause) at some specific stage of the liarities of life cycles in Acari (their duration, life cycle (Gurney et al. 1984). voltinism, phenology, flexibility etc.) depend on Unfortunately, information on peculiarities of the function of a special, species-specific System quiescence is rather limited. Nevertheless there of Seasonal Control (SSC), the organizing role in are some important data giving a possibility for which is enabled by dormant stages of diapausing fresh view and new interpretation of relations be- character. Quiescence was not a focus of these re- tween diapause and quiescence. These data are views, though its possibility in the acariform mites from analytical reviews by Hodek (1996, 2002) was suggested there (Belozerov 2007). Plesiotypic and Koštal (2006) evidencing that quiescence may traits of seasonal life cycles in the Acari are char- have a very close relationship with diapause, be- acterized by complex SSC with numerous dormant ing its terminal phase (the post-diapause quies- stages enabling the control of perennial, semivolt- cence) that ensures the maintenance of a dormant ine and monovoltine development, while apotypic state (with covert potentiality for development af- traits are expressed in the presence of reduced SSC ter the end of diapause) and enables the continua- with limited number of dormant stages for control tion of development after adequate environmental of mono- and polyvoltine development. Thus, the changes. More extensive consideration of this evolution of seasonal adaptations in the Acari was form of quiescence, its properties and significance considered to occur through transformation of an- will be given below. cestral polymeric SSC (with numerous dormant The number, position and character of dor- stages) into oligomeric and monomeric systems mant stages (diapause or/and quiescence), as well (with reduced number of diapausing stages). as their relationships during ontogenesis, are of Though quiescence and diapause seem to be great importance for phenology and duration of quite distinct, they can be difficult to distinguish in life cycles in insects and other arthropods. Their practice for the majority of arthropods due to the development, according to the length of genera- lack of adequate ecological and physiological in- tions, can be multivoltine (= polyvoltine, with vestigations. This concerns not only chelicerate some generations per year), univoltine (= mono- arthropods, such as acarines and other arachnids, voltine, with one generation per year), semivoltine but even their relatives, mandibulate arthropods (= biennial, with one generation per two years) (i.e. insects and crustaceans), which are investi- and many-years-long (= perennial, with one gen- gated much better, though with nonequal attention eration per three and more years). In special analy- in regard to diapause (the main subject of investi- sis of ecological mechanisms controlling diapause, gations in insects) and quiescence (studied in crus- Saulich (1999) has shown that all known cases of taceans somewhat more than in insects). No won- multivoltine development of insects are controlled der, therefore, that the evaluation given by L. only by facultative diapause, while mechanisms of Brendonck (1996) for crustaceans, that “the extent univoltine development are very diverse, being to which dormancy … is controlled endogenously provided not only with obligatory diapause, but (diapause) or exogenously (quiescence) is not al- also with facultative diapause and also with com- ways clear”, fits for chelicerates to a much higher bination of some different types of dormancy. degree. For Acari, one could almost substitute the More prolonged developmental cycles were not phrase “is always unclear”. considered by her (Saulich 1999), however it is Therefore, it is important to continue the com- possible to suggest (taking into attention the sea- parative and evolutionary study of dormancy in

81 V. N. Belozerov the Acari, particularly in regard to distribution of terrestrial life-history strategies in extreme envi- diapause and quiescence among phylogenetically ronments fit the features of adversity (“A-selec- different taxa, and the association of these two tion”) characterized by long life cycles, slow over- dormant states with different ontogenetic instars all growth rates, low reproductive output, low of their life cycles. This first of two reviews deals dispersal ability and high investments in survival with the acariform mites — Oribatida, Astigmata adaptations. and Prostigmata. In regard to all these groups, and The prolonged development is characteristic particularly the latter polyphyletic order (Prostig- especially of more derived oribatid mites (e.g. 4.2 mata), I follow in general the classifications used years as in Ceratozetes kananaskis — Mitchell by Evans (1992) and Kethley (1982). Updated in- 1977a), while evolutionary specialized mites, as a formation on the taxonomy and phylogeny of ac- rule, have generations of much less duration (in ariform mites can be found in Mironov and Boch- some cases one month and shorter as in Oppiella kov (in press) and my footnotes. nova — Woodring and Cook 1962) (see also Leb- run 1971; Weigmann 1975; Mitchell 1977b; Lux- ORIBATIDA ton 1981; Grishina 1991). Oribatid mites (Oribatida = Cryptostigma- Thus, the interspecific diversity of develop- ta) represent a basal taxon of ordinal (Evans 1992) mental rates in oribatid mites reveals some depen- or subordinal level (Norton 1994) that includes dence on their phylogenetic and taxonomic posi- more than 9000 species. Among major groups of tion. However, it is more important ecologically, Acari, this taxon is peculiar in expressing the full that most oribatid mites are characterized by in- set of conservative plesiotypic traits related to life traspecific variability, flexibility and plasticity of history, life cycles, and other biological features, their development due to variable and extended due to its historical connection with the soil envi- duration of their instars according to environmen- ronment (Lange 1984; Norton 1994). They retain tal and seasonal conditions, which results in over- the ancestral acariform life cycle including the egg lapping generations, though they are nevertheless and six postembryonic instars — prelarva (PLa), efficiently synchronized through the presence of larva (La), protonymph (PN), deutonymph (DN), some or many dormancy-capable, hibernating or * tritonymph (TN), and adult (Ad) . An important aestivating instars within their life cycles. Though plesiotypic trait, common to all oribatids, is their this is a typical property of most oribatid mites dispersal during the adult instar. Most oribatid from temperate habitats, it is especially character- mites from temperate forest soils (as an ancient istic of slow-developing oribatids living in hard and relatively plesiotypic, if not original, habitat climatic conditions with extreme seasonality re- — as noted by Norton 1994) possess rather low vealed in short cool summer and long winter, as developmental rates and fecundity. The genera- the terrestrial mite Alaskozetes antarcticus from tion time of these mites usually is one or two years, maritime Antarctic (Convey 1994, 1996; Block though besides such typical cases of monovoltine and Convey 1995; Peck et al. 2006), the littoral and semivoltine development many oribatid mites Arctic mite Ameronothrus lineatus (Søvik and reveal either more rapid (bivoltine and polyvolt- Leinaas 2003; Søvik et al. 2003; Søvik 2004), the ine), or more slow (perennial) life cycles. The life- mountain North Norvegian A. lapponicus (Tilrem history attributes of most oribatids seem typical of 1994) and the alpine Austrian mite Oromurcia su­ organisms considered to be “K-selected”, though detica (Schatz 1985). Each instar in these mites is species with more rapid development demonstrate capable of hibernation and takes the whole year rather “r-selected” properties (according to “r/K” for its development. Their life cycles may be system of life strategies — see MacArthur and completed therefore during 5–6 years only (Table Wilson 1967, Pianka 1970), while especially slow- 1). It is very important that the flexibility and developing mites with perennial life cycles may variability in total cycle length, as well as their be considered as possessing the “A”-attributes overlapping, allows A. antarcticus (similar to oth- (Convey 1994; Peck et al. 2006), according to the er polar arthropods — see Danks 1999a, 2006) to “r-K-A” triangle system of life histories developed survive environmental unpredictability of irregu- by Southwood (1977) and Greenslade (1983). In lar repeated changes of harsh and mild conditions, regard to the last group it is necessary to say that that might be fatal for less flexible species (Con- vey 1994). Unfortunately information concerning ∗ These abbreviations (Ad, Eg, PLa, La, PN, DN and TN) will be used throughout this paper. peculiarities of life cycles in tropical or even sub-

82 Dormancy and their significance in life cycles of mites and ticks References Bücking et al. 1998 Convey 1994, 1996; Block, Convey 1995 Søvik, Leinaas 2003; Søvik, Leinaas, Solhoy 2003; Ims, Søvik 2004 Marshall, Convey 1999 Stamou 1989 Luxton 1981 Luxton 1981 Bücking et al. 1998 Pugh, King 1986 Bücking et al. 1998 from (cited 1994 Tilrem Bucking et al. 1998) - - C. o _ _ _ _ Remarks Presence of autumn pre-diapause mi - pre-diapause autumn of Presence hiber - into Ad and TN DN, of gration nating places. Oviposition, hatch and moulting syn - moulting and hatch Oviposition, chronized after hibernation by crease in - of temperature in early sum - mer. There are pre-diapause before hibernation. traits Larviposition and moulting synchro - of increase by hibernation after nized temperature in early summer. Moulting and reproduction synchro - of increase by hibernation after nized temperature in early summer. Presence of autumn pre-diapause mi - pre-diapause autumn of Presence gration of TN and Ad into hibernat ing places. Restoration of development by tem perature increase above 10 Rigid mechanism of diapause in TN with pre-diapause migration to hi - bernating places. ? ? ? ? _ _ _ of TN of TN Diapause of TN and Ad after migration of DN, TN , Ad Winter diapause Winter diapause Winter diapause Winter diapause Type of dormancy ? ? ? _ (?) DN ? winter. winter. DN , Ad ? Quiescence DN, TN, Ad pre-reproduction The pre-moult, pre- low temperatures in quiescence in winter. Inactivity of all stages at Pre-hatch, pre-moult and reproduct. Quiescences in Quiescence of PN and DN The pre-moult and pre-re - production quiescence in winter. TN Table 1. Different types of dormancy (quiescence/diapause) in dormant stages the oribatid mites. 1. Different Table TN and Ad and Ad and Ad and Ad TN, Ad (mainly) Spitsbergen: DN, TN , Ad DN, TN, Ad DN, TN, Ad N. Germany: In N. Germany L, PN, DN, Ad Dormant stages L, PN, DN, TN L, PN, DN, TN L, PN, DN, TN In S. Britain PN, DN, Eg, La, PN, DN, PN, DN, TN, Ad peren - ( 4–6 years ). monovoltine flexible Main traits perennial cycle (5–6 perennial cycle (3 years monovoltine rigid life cy - perennial life cycles (5–6 Continental Antarctic larviparous mite with or more). Maritime Antarctic oviparous mite with years or more). European littoral mite ovoviviparous with life cycle. Holarctic littoral mite ovoviviparous with years or more) (Spitsbergen) monovoltine or flexible life(North Germany) . cycle European forest soil-dwelling mite with semivoltine cycle. European forest soil-dwelling mite with semivoltine cycle. Supralittoral mite from N. Germa - ny with cle. Lichen-dwelling mite from moun - with Norway North of tains nial life cycle Soil-dwelling mite from Greece (with semivoltine cycle). s Mite species 3. Madheimia wilsoni 1. Alaskozetes antarcticus 2. Ameronothrus lineatu 4. Ameronothrus marinus 8. Achipetria coleoptrata 9. Damaeus clavipes 5. Ameronothrus maculatus 6. Ameronothrus lapponicus 7. Achipetria holomonensis

83 V. N. Belozerov Sitnikova 1959 Gourbiere et al. 1985; Lions, Gourbiere 1989; Hågwar 1998 Luxton 1981 Block 1965; Harding 1973; Weigmann 1975; Schenker 1985 Webb 1977; Luxton 1981 Reeves (1969) Reeves 1969 Kaneko 1989 Soma 1990 Grishina 1997 _ The same TN is non-hibernating instar. Egg-laying in June-July by overwin - tered females. The first year is com - need which TN, hibernating by pleted the summer to transform into Ad in autumn. In Norway (Hågwar) the cy - cle is completed in two years. Cold reactivation of females for ovi - position (Woodring, Cook 1962). Suggested role of photoperiod for in - duction of adult diapause ovipo - of (Harding season Synchronized 1973). sition (spring) and larval (summer). hatching Presence of oviposition delay of 3–6 months. Synchronized season of egg-laying hatching larval and hibernation) (after (June-July). The whole life cycle in rather soil cold of alpine zone more). is Duration 4 of years each (or stage gether with (to - winter dormancy) is not less than one year. Synchronized season of oviposition sum - (late hatching larval and (spring) mer). ? ? ? ? adult females adult females? adult females? adult females? adult females? adult females? ter diapause of ter diapause of ter diapause of ter diapause of ter diapause of ter diapause of Reproductive win - Reproductive Reproductive win - Reproductive win - Reproductive Reproductive win - Reproductive Reproductive win - Reproductive Reproductive win - Reproductive ? ? ? ? ? ? ? ? ? ? PN, L, PN, TN, Ad Ad Ad and Ad and Ad TN, Ad PN, DN, Ad PN, DN, Ad DN , TN, Ad DN, TN , Ad In Europe: L, PN, DN, TN PN, DN, In Siberia: Eg, L, PN, DN and Eg, L, PN, DN, TN DN, PN, L, Eg,

long semivolt - semivoltine Picea abies ) mono - and distributed in Holarctic. Abies alba (and European forest soil-dwelling mite soil-dwelling forest European with mono/ semivoltine flexible cycles. Temperate forest mites soil-dwelling from Japan with ine cycles. fallen in the soil (semivolt/ bien - nial development). European forest soil-dwelling mite soil-dwelling forest European with monovoltine cycles. with mite Soil/litter-dwelling life cycle cycles. East US forest soil-dwelling mite with semivoltine cycle. East US forest soil-dwelling mite with semivoltine cycle. Inhabitant of pine needles in soil of alpine pine shrubs of Central Japan. needles of colonizer Soil-dwelling of Litter-dwelling mite from S. Eng - land with Eohypoch ­ 10. Damaeus boreus 11–13. thonius Archoplophora magnus, vil ­ losa, Quadroppia quadriacarinata 16. Chamobates cuspidatus 17. Platynothrus peltifer 19. Tectocepheus velatus 20. Oribella sp. 14. Phthiracarus japonicus 15. Adoristes ovatus 18. Steganacarus magnu s

84 Dormancy and their significance in life cycles of mites and ticks Norton et al. 1996 Smrž 2002 Reeves 1969 Reeves 1969 Reeves 1969 The quiescent state lasts from some days up to two years. The quiescent state lasts at least 10 days and is generally characterized by an empty gut, guanine deposition and, in adults, by the resorption of spermatids or oocytes and eggs. Regular succession of juvenal stages in summer-autumn after nized egg-laying in early summer. synchro - Regular succession of juvenal stages from two summer generations after synchronized egg-laying in summer. early The same _ _ Reproductive Reproductive Reproductive adult females? adult females? adult females? winter diapause of winter diapause of winter diapause of - - ? ? ? quiescent state In periods of drying pools these mites survive state of quiescenct, being in dur - sediment in burrowed ing long period, but rap - idly revive after moister ing. Both adults and tures imma enter immobile co - matose under extreme dry con - ditions . The reverse pro - cess occurs two hours af - ter remoistening. Ad paper) TN, Ad TN, Ad Ad, immatures Ad (not DN and TN as in Reeves This inhabitant of small ephemeral pools in deserts of the Colorado pla - teau (USA) has similar case of dor - mancy enforced by drying of pools and terminated by watering. Life cy - cle is unknown. East US forest soil-dwelling with monovoltine cycle. mite Forest soil-dwelling mite from East - ern US with bivoltine life cycle. Forest soil-dwelling mite from East - ern US with bivoltine life cycle. European mite inhabiting moss-cov - er on roofs of buildings. Very resis - tant to drought. Voltinism and gen - eration time are unknown. ronothrid mite 25. Undescribed ame ­ from Eastern USA, similar ecologically with some African ameronothrids. 21. Pergalumna altera 22. Oppiella nova 23. Oppia subpectinata 24. Scutovertex minutus Note. Column “Dormant stages”: More probable dormant stages — in bold print, less normal print. Column “Type of dormancy”: Stages definite corresponding type dormancy — in bold, while probable normal print. In Tables 2–5 the notes of same content.

85 V. N. Belozerov tropical oribatid mites is absent or extremely Though some corrections may be necessary scarce. after further studies in regard to the sets of instars As seen in Table 1, including data on 25 dif- capable of dormancy and hibernation in the men- ferent oribatid mites with life histories studied tioned species (Table 1), and the addition of oth- more or less thoroughly in field conditions, about ers, I believe that the above conclusion on the re- half (11 species) have semivoltine (sometimes bi- lationship between the number of dormant stages, ennial) life cycles with 2–6 (mean 3.8) dormancy- and the duration and flexibility of life cycles will capable overwintering instars, and a similar num- hold. ber of species (9) have rapid development The exact nature of overwintering dormancy (mono- and bivoltine) with 1–3 (mean 2.0) dor- in oribatid mites (quiescence or diapause) is rarely mant instars, while only 5 polar species have pe- indicated in literature and its identification is ham- rennial cycles with 4–6 (mean 5.0) dormant in- pered by the deficit of adequate ecophysiological stars. Thus, some important traits of life histories information. In most cases oribatologists use for in oribatid mites, such as duration of generations, this purpose, as a rule, the indefinite terms “inac- voltinism of development, and flexibility of their tive”, “dormant” or “resting”, avoiding strict des- life cycles, definitely depend on and are deter- ignations. The real exceptions concern Norton mined by the number of dormancy-capable, over- (1994) who considers winter dormancy in oribatid wintering stages that compose together the orga- mites as a cold-induced quiescence and manifesta- nized System of Seasonal Control (SSC) consisting tion of metabolic constraints at low temperatures, of single, some or many dormant stages (Beloze- as well as. Convey (1996) and Søvik (2004), who rov 2007, 2008b). studied the biology of polar oribatids with peren- These and some other characteristics of orib- nial life cycles (the Antarctic mite A. antarcticus atid life histories (particularly the phenology) de- and the littoral Arctic mite A. lineatus respective- pend also on the localization of dormant stages ly), and concluded that the dormant state of nu- along the chain of ontogenetic instars. It is accept- merous hibernating instars in these mites repre- ed as a common rule that such stages participating sents a quiescence enforced and terminated by the in the seasonal control of life cycles in Insects, Ac- direct effect of temperature. In accordance to their ari and other arthropods are species-specific (Dani- opinion, there is little evidence of true diapause levsky 1961; Luxton 1981; Tauber et al. 1986; mediated by environmental cues in these mites Danks 1987; Alekseev and Starobogatov; 1996; due to disadvantages resulting from possible in- Belozerov 2007, 2008b; etc.), though with some correct cueing of entry into or exit from diapause exceptions related usually to their geographic vari- under these harsh and often unpredictable condi- ability. Such exceptions are known in oribatid tions (Convey 1996; Danks 1999a; Peck et al. mites also (Table 1). One is the holarctic Amerono­ 2006). For the oribatid A. antarcticus the term thrus lineatus, which has five dormant instars and “non-diapause dormancy” was used by Young and perennial life cycle in its polar populations, but Block (1980), and this term has found currency in only a couple of dormant instars (some adults, but cases where quiescence has a seasonal basis (Tau- mainly tritonymphs) and monovoltine life cycle in ber et al. 1986; Danks 1987; Siepel 1994). the temperate European population (see Søvik Nevertheless in studies of polar oribatids, 2004; Bucking et al. 1998). Another is the Euro- some data give evidence of a diapausing nature to pean monovoltine mite Ameronothrus marinus, the overwintering state in nymphs and adults of overwintering in North Germany in three instars these littoral oribatids. First is the presence of a (DN, TN, Ad), but in South Britain only as a single resting pre-ecdysial (pre-moult) phase* in A. ant­ TN-instar (Bucking et al. 1998; Pugh and King arcticus mites that prepare for hibernation at the 1986). A significant example of such geographic end of summer before the onset of cold, and is ac- variability is the holarctic soil-dwelling mite companied by active clearing the gut, as shown by Platynothrus peltifer with all-round common semi- Convey (1996). Second, the autumn migrations of voltine cycles, but with different sets of overwin- tering instars in temperate Europe (PN, DN, TN, ∗ Unfortunately the real ontogenetic and physiological traits Ad) and continental Siberia (L, PN, Ad) (Block of this “pre-moult phase” are not described and not explained in the mentioned papers (Convey 1996, etc.), and I suggest 1965; Grishina 1997). However, the latter case that the onset of this resting state precedes the apolysis, repre- may be complicated by the existence of cryptic senting the first step of moulting events, and mites overwinter species in different areas (Heethoff et al. 2007). therefore with no traits of morphogenetic processes.

86 Dormancy and their significance in life cycles of mites and ticks deutonymphs and tritonymphs of A. lineatus to hi- been preadapted to Arctic and Antarctic conditions bernating places takes place before the onset of (without special polar adaptations). However, no the dormant state (the same is true in other inter- less possible, as was suggested by Søvik (2004), tidal ameronothrids, A. marinus and A. maculatus, that the success of oribatid mites in polar habitats with their “rigid diapause” according to Bucking is attributable to a combination of both derived an- et al. 1998). These peculiarities have allowed me cestral preadaptations and special derivative adap- (Belozerov 2007, 2008b) to use the term “dia- tations. The solution of this “polar” problem is pause” for the mentioned cases of dormancy in quite impossible without establishing the real na- polar oribatids with perennial life cycles, and con- ture of dormancy (quiescence, diapause or their sider this “resting pre-moult phase” as an expres- combination) in typical versions of oribatid life sion of real diapause preceding the onset of apoly- histories, which is still unknown. Naturally, there sis (but not of ecdysis itself). Short remarks on the is a great need in further ecophysiological investi- presence of diapause in life cycles of soil-dwelling gations of dormant stages in life cycles of oribatid oribatid mites, though with no special explanation mites from climatically different habitats, which is and support, were given also by Grishina (1991) a difficult, but interesting and necessary task. and some other authors. ASTIGMATA Unfortunately, the available data (Table 1) and the above considerations of species from ex- The situation, quite different from the above treme habitats give no definite answer to the ques- considered Oribatida, is observed in the related, tion of the real nature of dormant states in over- but derivative taxon Astigmata, a large, mono- wintering instars. Its solution needs, of course, phyletic order with some 75 families and 850 gen- ecophysiological data permitting the identification era of mites, whose ancestral ecology and ontog- of quiescence (as direct response to adverse condi- eny involve exploitation of ephemeral temporary tions) and diapause (as a programmed response to habitat patches and the use of phoresy on insect or token factors signalling the approach of adverse vertebrate carriers to ensure dispersal for coloniz- conditions). However, such data for overwintering ing new adequate habitats (OConnor 1982). Due instars in oribatid mites are absent, or very frag- to some important apomorphies (mainly of mor- mentary, sometimes conjectural or contradictory, phologic and biochemical character), Astigmata as illustrated in Table 1, particularly by the oppo- are accepted as a subgroup of Oribatida (Norton site opinions of Søvik (2004) and Bucking et al. 1994, 1998; Sakata and Norton 2001; Maraun et (1996) concerning the nature of dormancy in Am­ al. 2004) evolved within the oribatid mites as a eronothrus lineatus. paedomorphic lineage (Zachvatkin 1953; OCon- A more definite and clear situation probably nor 1984). According to Norton (1998), the deri- exists in dormancies arising in oribatid mites as a vation of Astigmata has occurred within Des- response not to low temperature, but to low humid- monomata, one of the middle-derivative groups of ity. The real quiescent state of such dormancy is Oribatida (Fig. 1), particularly within the super- known in nymphs and adults of the European mite Scutovertex minutus (inhabitants of moss on roofs of buildings) which reveal the onset of a comatose dormant state as a rapid response to drought with an immediate exit from it after moistering (Smrž 2002). The similar case of dormancy enforced by drying of small ephemeral pools in desert habitats of the Colorado plateau (USA) and swiftly termi- nated by pool watering is presented by an amer- onothrid oribatid mite (Norton et al. 1997). As a conclusion to this part of the paper, I should like to remind two opinions on the charac- ter of life histories of oribatid mites in extreme po- lar conditions. Their life histories are considered by many oribatologists (Norton 1994; Convey 1996; Behan-Pelletier 1999) as an extreme version Fig. 1. Schematic relationships of major oribatid mites groups of the typical ancestral oribatid life history that has and the Astigmata (after Norton 1994).

87 V. N. Belozerov family Malaconothroidea, confirmed later by Really, 21 of 25 species of these mites pre- Sakata and Norton (2001). The possibility of close sented in Table 2 possess deutonymphal hypopo- relations of Astigmata and Oribatida is supported des (either phoretic, or sedentary) with diapausing by Mironov and Bochkov (in press) in their com- properties and in some cases with real traits of prehensive analysis of macrophylogeny in acari- post-diapause quiescence (Fig. 2). Such species form mites. However, some other authors see no are different taxonomically, being representatives connections between Astigmata and Oribatida of the whole set of families. Only in four species (Grandjean 1937; Woas 2002). For instance, the the function of dormancy seems belong to the TN results of recent molecular investigations (Domes (instead of DN, which may be lost or retain pho- et al. 2007) placed Astigmata outside Oribatida, as retic function only). Probably in these cases, par- a sister-group of the endeostigmatid mites (par- ticularly in marine hemisarcoptid Hyadesia fusca ticularly Alicorhagiidae). (Bucking 1999; Bucking et al. 1998) the resting The Astigmata represent an outstanding ex- TN is characterized by the state of quiescence (Ta- ample evidencing that life-history evolution in ble 2), and only in the acarid Naiadacarus arbori­ Acari may play a principal role in their radiation, cola (from tree-holes in North America) does the particularly through changes of their dispersal TN have the traits of winter diapause, while the style and instar involved. An important life-histo- DN enables a summer dispersal by phoresy syn- ry difference that oribatid mites disperse as adults, chronized with eclosion of dipterous carriers while astigmatid mites disperse only as immatures (Fashing 1977, 1994). (usually phoretic deutonymphs) is considered a Thus, terrestrial temperate species of Acaridia key to the radiation of the Astigmata (Norton are characterized by the presence of a single im- 1994). mature dormant instar adapted for survival and The Astigmata includes two big groups of dispersal (mainly as heteromorphic non-feeding mites (namely the free-living Acaridia and the DN with vestigial mouthparts and some morpho- parasitic/symbiotic Psoroptidia) differing in many logic adaptations for phoresy). The rapid polyvol- biological and ecological properties, but similar in tine development of these mites may be broken some essential traits in their life-history strategies. through formation of a resting hypopus and re- They all are mostly characterized by small size, stored after its transformation into an active TN rapid development and rather high reproduction followed by Ad. The regularities and mechanisms potential. In contrast to Oribatida, where K-attri- controlling the onset and maintenance of dormant butes are typical, the Astigmata in general belongs state in hypopodes were studied by many authors, to “r”-selected lineage of life-history strategies, ir- but especially deep insight into these mechanisms respective of “r/K” (MacArthur and Wilson 1967; has been taken by W. Knülle and coworkers from Pianka 1970), or ”r-K-A” their models (South- the FU, Berlin (Knülle 1987, 1991a,b, 1995, 2003; wood 1977; Greenslade 1983). Corente and Knülle 2003; etc.) in a series of inves- The systems controlling life cycles in Astig- tigations on the glycyphagid Lepydoglyphus de­ mata (in contrast to Oribatida) have apotypic traits structor, and perfectly presented by Danks (1994, of reduction (oligomerization), usually with single 1999b) in his scheme of different developmental (Acaridia) or no dormant instars (Psoroptidia). In pathways of this mite (Fig. 2) in diapausing (with Acaridia the function of dormancy, often com- long or short diapause at DN instar) and non-dia- bined with the function of dispersal through phore- pausing direction (with direct transformation of sy, belongs usually only to the heteromorphic PN into TN without DN), as well as with the obvi- deutonymph (hypopus) that can be facultative or ous presence of post-diapause quiescence in this obligatory. The presence of facultative DN be- acaridian mite. Nevertheless, the mechanisms of tween PN and TN, or its failure, is determined at termination of hypopus stage and its transforma- previous instars (La and PN) by an interaction of tion into the TN instar require further thorough environmental and genetic factors (Knülle 1999, investigations. 2003) that evidences the diapausing traits of its Dormant hypopodes of Acaridia serve usually dormant state. These resistant heteromorphic DNs, as tools for survival in conditions of unpredictabil- capable for survival and dispersal, are typical for ity in their ephemeral habitats, though in species the major part of Acaridia exploiting ephemeral associated with insects, the hypopodes reveal sea- habitats (Athias-Binche 1991; Houck and OCon- sonal adaptations synchronizing the hibernation nor 1991; Houck 1994). and dispersal of both associates (Table 2). An es-

88 Dormancy and their significance in life cycles of mites and ticks

Fig. 2. Life-cycle pathways in Lepidoglyphus desrtuctor (Astigmata: Glyciphagidae) (after Danks 1999, according data by Knülle 1991). pecially original example is represented by the within hay patches (Sorokin 1946). Similar diver- mentioned acarid Naiadacarus that inhabits wa- gence in stages adapted for predictable and unpre- ter-filled tree-holes and hibernates there as TN (in dictable environmental changes is quite probable the state of seasonal diapause) with other stages in other families of Acaridia, though the key role (in the state of quiescence), while its DN serves as in them (Norton 1994) belongs to the phoretic DN a phoretic tool for summer dispersal on dipterous (hypopus). Dormancy of seasonal character is insects (Fashing 1977, 1994). Some traits of adap- characteristic here for species which associate tation for hibernation are known in the TN of sap- with insects possessing obvious seasonal life cy- rophagous Tyrophagus, aggregating in autumn cles. First place belongs, of course, to the family

89 V. N. Belozerov - References Kielczewski, Seniczak 1972 Cowan 1984 Klompen, Luko schus, OConnor 1987; Houck, OConnor 1991 Houston 1987 Perron 1954; Hill, Deahl 1978 Fashing 1994 1937; Boulanova Barker 1967, 1968; 1988; Fain Hart, Knülle 1991, 2003; Kasuga, Amano 2003 - L.destructor have post- Remarks Diapause of phoretic DN (hypopodes) from August to May. Phoresy of hypopodes on wasps and further development (until formation of next DN phoretic) on larval/pupal wasp stages. Appearance of summer phoretic DN is synchronized with discharge of tree sap attracting adult wasps used by mites for phoresy. The transformation of PN to DN is initi ated by defecations of metamorphized bee larvae. Hibernated phoretic hypopo - des are dispersed in spring by eclosed adult bees. Dispersal is realized, as in most Acaridia, most in as realized, is Dispersal by resistant hypopodes (heteromorphic DN). Phoretic hypopodes are formed during dispersal for (May-June) season summer on insects and partly for hibernation. Sedentary hypopodes are more resistant than phoretic hypopodes, but both are adapted for unpredictable environmental changes. TN of diapause quiescence (Danks 1999). DN DN DN DN Diapause generation generation Hibernating Hibernating Hibernating Hibernating bee prepupa from autumn second, autumn diapause of diapause of DN with diapausing bee cells together diapause of DN in diapause of DN Type of dormancy _ _ – _ _ _ _ Quiescence of autumn generation Dormant stages DN (=Hypopus) DN (=Hypopus) DN (=Hyppous) DN (=Hypopus) DN (=Hypopus) DN (=Hypopus) DN (=Hypopus) Table 2. Different types of dormancy (quiescence/diapause) in dormant stages astigmatid mites. 2. Different Table - - Lep ­ . Drosophila cultures , with bivoltine devel Main traits in Australia. in nests of nests in rossi Allodynerus opment (summer generation without hibernat with generation. autumn DN, ing hypopodes). Bivoltine mite associated with larval pupal and this solitary vespid. Both generations phoretic, are DN summer but DN, have while autumn DN overwinter on host prepupa or pupa. Inhabitant of galleries of scolytid erisinus fraxini Monovoltine mite associated with soli - with associated mite Monovoltine tary wasp Ancistrocerus antilope Polyvoltine mites from decaying veg - etation (1), from (2) etc. with generation = 4–8 day. Filtering (monovoltine?) mite water-filled tree-holes in N. America from Polyvoltine mites (from soil, generation with products) stored nests, litter, morph one have Usually days. 10–15 = of facultative hypopus. Species noted by * have dimorphic hypopodes (pho - retic and sedentary). Monovoltine mite with symbiotic and phoretic contacts to Stenotritid bees Ctenocolletes

sp. Mite species Tyrophagus putrescentiae 13. Ensliniella kostylevi (Winterschmidtiidae) and other Ensliniellinae mites associated with solitary vespids 14. Calvolia fraxini (Winterschmidtiidae) 12. Kennethiella trisetosa (Winterschmidtiidae) A ca ri d i a 1. Histiostoma heinemanni 2. H. laboratorium (Histiostomatidae) 3. Hormosianoetus mallotae (Histiostomatidae) 4. 5. Tyrophagus similis (both Acaridae) 6. Glycyphagus domesticus 7. Glycyphagus privatus * 8. Glycyphagus ornatus* 9. Lepydoglyphus destructor 10. Gohieria fusca (all five Glycyphagidae) 11. Ctenocolletacarus (Acaridae)

90 Dormancy and their significance in life cycles of mites and ticks Okabe, Makino 2003 Timms et al. 1981 Krombein 1967 Houck, OConnor 1991; Ji et al. 1996 Sorokin 1946; Zyromska-Rudzka 1964; Wharton 1976 Fashing 1977, 1994 Dosse, Schneider 1957 Bucking et al. 1998; Bucking 1999 - _ _ _ TN is a dominant stage during stage dominant a is TN C. lactis C. DN molted to TN in host cell, where TN prey wasp of hemolymph on feed Ad and scav - PN and La whereas larvae, host and on hatch eggs Mite feces. and debris enge prepupal host and reach PN on host pu - and eclosion, host before appear DN pae. attach to overwintering adult hosts. Termination of DN instar occurs after its phoresy on beetles. In depression period of mite culture (simul - taneously with single hypopodes). TN in T. longior dominates in autumn hays. The accumulation of TN as main hiber - nating instar begins from middle sum - mer, while synchronized spring into moult adults occurs after winter reactiva tion. Phoretic DN appear in summer for dispersal. Development of tritonymphs stops August until in next spring (even conditions). at lab. TN DN DN ? _ _ DN ? Diapause of phoretic Overwintering ia a facultative facultative diapause of Obligate winter in May-June for Winter diapause of TN , while DN seasonal phoretic dispersal on flies. hypopus occuring hypopus _ _ _ _ _ Ad TN ? Winter and Ad The cold of L, PN of TN and quiescence quiescence TN TN (L, PN), TN, Ad DN (=Hypopus) DN (= Hypopus ) DN (=Hypopus) DN (=Hypopus) (L) PN, TN , (Ad) Carpoglyphus is _ into the wasp cell when cell wasp the into Mite from Japan, phoretic as DN on Anterhynchium the wasp is laying eggs. Saprophagous polyvoltine mite with generation = 6–8 days and facultative resistant hypopus. Polyvoltine mites in cells of solitary bees. 29–66 days). They have TN or PN as dormant stages (instead of DN). the lost Mites feeding on diaspidid scale in - sects and phoretic as facultative hy - popodes on Chilocorus beetles. Polyvoltine nidicoles and mites from domestic stored food reserves etc. (generation time in Saprophagous larviparous mite from water-filled tree-holes in N. America ex - (with instars all of hibernation with ception of phoretic DN). Dominant hi - bernating stage is diapausing TN syn - chronizing overlapping life cycles. European littoral mite with two over - lapping summer generations (in Germany). Generations = 46–73 days. N. Hypopus is absent. ­ )

(Acaridae) Sancassania (= Calogly Chaetodactylus krombeini 15. Kurosaia jiju (Winterschmidtiidae) phus ) berlesei 16. 17. (Chaetodactylidae) 18. Horstia virginica (Acaridae) 19. Hemisarcoptes cooremani 20. H. coccophagus (Hemisarcoptidae) 21. Carpoglyphus lactis (Carpoglyphidae) 22. Tyrophagus longior (Acaridae) 23. Naiadacarus arboricola (Acaridae) 24. Hyadesia fusca (Hemisarcoptidae) 25. Czenspinskia lordi (= Calvolia transversostriata (Winterschmidtiidae)

91 V. N. Belozerov Mercado et al. 2001 Mironov 2000 Wharton 1976; Dubinina, Pletnev 1977; Mumcuoglu, Lutsky 1990 Dubinin 1951 Sweatman 1958; Otranto et al. 2004 Zekhnov 1946 Dubinin 1951 Dubinin 1951 Dubinin 1954; Meleney 1985 Dubinin 1954; Meleney 1985; Arlian et al. 1989 F. The same The same Non-migrating birds Non-migrating birds Non-migrating birds Hosts without migration . During migrations the diapause There is no DN (Hypopus) in life cycle of cycle life in (Hypopus) DN no is There this mite (as well as in Pyroglyphidae). In spring and autumn migration the mite population is represented mainly by fe - pre - reveal instars immature while males, domination during summer nesting of coelebs in mites was not observed. of cycle life in (Hypopus) DN no is There this pyroglyphid mites. Due to infestation through direct contact, there host are no dormant stages in mites. ? ? _ _ _ _ _ Eg (?) TN, Eg (?) TN, Eg (?) ? ______Ad ? other Better instars TN than (PN), TN survival of _ _ _ Eg Ad ? TN ? TN, Eg TN, Eg PN, TN PN, TN - - reveals coelebs Fringilla Polyvoltine nidicoles and mites from domestic food reserves, house dust etc. With generation of 18–26 days. Important allergenic mites. with mite allergenic domestic Tropical generation = 13 days and adult life 50 days. DN is absent. The chaffinch The summer increase of this feather mite population (with domination of imma ture instars) and accumulation of fe - males for spring and autumn migra tion. Feather mites of jackdaws with repro - duction during nesting period of hosts (VII–IX). Monovoltine mites with hi - bernating nymphs. Feather mites of hens. Feather mite of ducks. Feather mite of skylarks. Permanent ear parasites of cats with polyvoltine development and (about Ad and TN for off-host survival short 6–7 days). Polyvoltine parasites in mammalian skin (Ss), and on skin with generation of 10–12 days. surface (Ps), Polyvoltine parasite on mammalian skin (generation of 21–28 surface of days).

(= pontifi ­ and

(Sarcoptidae) Dermatophagoides ptero ­ Suidasia medanensis Suidasia 12–15. nyssinus, D. evansi, D. farinae, D. microceras (Pyroglyphidae) 16. ca ) (Suidasiidae) 11. Monojoubertia microphylla 5. Proctophyllodes corvorum 6. Analgopsis corvinum 7–8. Pterolichus obfusus P. solutocurtus 9. Bdellorhynchus polymorphus 10. Pterodectes bilobata 4. Otodectes cynotis and other species of (Psoroptidae) this genus 3. Chorioptes bovis (Psoroptidae) P so r opt i d a 1. Sarcoptes scabiei 2. Psoroptes sp. (Psoroptidae)

92 Dormancy and their significance in life cycles of mites and ticks

Winterschmidtiidae, where the main function of two dormant stages — TN and eggs (Dubinin phoretic hypopodes with diapausing dormancy in- 1951). Such dormant stages, considered by Dubi- cludes synchronizing seasonal development of nin (1951) as diapausing, are typical, for instance, these mites and their carriers (Table 2). Good ex- for Trouessartia corvina (a parasite of corvine and amples of this synchronization by means of pho- passerine birds) and Bdellorhynchus polymorphus retic hypopodes are represented by polyvoltine (duck’s parasite), as well as for Pterolichus ob­ Kurosaia jiju associated with the wasp Anter­ tusus and P. solutocurtus (hen’s parasites) (Dubi- hynchium in Japan, by two bivoltine mites, Calvo­ nin 1951; Dubinin and Vasilev 1958); while Proc­ lia fraxini (associated with scolytid beetles) and tophyllodes corvorum and Analgopsis corvinum Ensliniella kostylevi (associsated with solitary (parasites of jackdaws) have PN and TN as dor- vespids), both of which produce phoretic hypopo- mant instars (Zekhnov 1946). All these mentioned des only in their autumn generation, and monovol- hosts belong to the group of non-migratory birds tine Kennethiella trisetosa, also associated by de- living in temperate areas with summer and winter velopment and dispersal with solitary vespids seasons. But some feather mites of migratory pas- (Table 2). serine birds (for instance Pterodectes bilobata The Psoroptidia, as permanent parasites and from skylarks) overwinter only as eggs (Dubinin symbionts (paraphages) of vertebrate animals 1951). Comparison of migratory and non-migrato- (birds and mammals), differ from their free-living ry birds in their “summer” and “winter” areas is relatives (Acaridia) by the obligate absence of doubtless necessary for solving the questions of deutonymphal instar in their nymphal phase (they seasonal dynamics and changes of instar structure retain only PN and TN). This enables more rapid in populations of feather mites, as well as of their and non-interrupted development, especially due dormant instars. to favorable microclimate within their habitats (on The study of Monojoubertia microphylla con- or inside the skin or plumage of hosts). From para- ducted by Mironov (2000) has shown the regular- sitological data on mammalian psoroptids (Dubi- ity of seasonal dynamics in micropopulations of nin1954; Meleney1985; etc) it is known that these this feather mite on its migratory passerine host, mites, as a rule, do not need special resistant stages the chaffinch Fringilla coelebs. During the sum- for long off-host survival (because the infestation mer nesting season in the European part of Russia, of hosts occurs through their direct contact) and micropopulations of this mite, represented mainly demonstrate therefore no programmed seasonality by immature instars, increase both on old birds in their life histories. The same infestation modus and on nestlings which are initially infested by the concerns the avian psoroptids, though they reveal TN and Ad through the contact with parents; but some traits of seasonality in their micropopula- after some decrease during the moulting of birds, tions, due to regular and manifold seasonal events the mite population increases again to be domi- of their hosts (migrations, nesting, moulting etc.), nated by females of mites for the autumn migra- and the ability of some instars in feather mites (te- tion, and this prevalence retained in birds recover- leonymphs, adults, and eggs) for seasonal hiber- ing their nesting places during spring migration. nating arrest (Dubinin 1951). Quite possibly, such Though all adult and immature mites on birds dur- a difference between avian and mammalian pso- ing both their migrations were active, as noted by roptids is connected with the origin of Psoroptidia Mironov (2000), and “diapause in them was not as parasites of birds, with a secondary radiation observed”, such a conclusion is only suggestive onto mammals with a dominance of host-parasite (as well as the above mentioned notes of Dubinin relations (OConnor 1994). about diapausing state of hibernating TN and eggs For feather mites representing the huge com- in other feather mites), and needs special reinves- plex Analgesoidea (Dubinin 1951) with its three tigation. main superfamilies — Analgoidea, Pterolichoid- In spite of real seasonal changes in population ea, and Freyanoidea (Proctor 2003), it has been structure of feather mites (Zekhnov 1946; Dubinin shown that in those species of mites associated 1951; Dubinin and Vasilev 1958; Mironov 2000; with migratory and non-migratory birds that nest etc), it is impossible to give a clear answer about in temperate zones of the Northern hemisphere, the modus of overwintering in these mites. Quite reproduction of mites and their active develop- possibly, in psoroptid mites with their life style as ment occur during spring-summer season, while permanent mammalian and avian parasites, the the hibernating “reserve” is formed in autumn by main role in their life histories belongs to symbi-

93 V. N. Belozerov otic adaptations determining their permanent con- in regard to life histories) are presented in Tables tacts and relationships with host organisms (as a 3–5 in accordance to the taxonomic systems used milieu of the first order), but not to ecophysiologi- by Evans (1992) and Kethley (1982). The Table cal adaptations determining their relations with with respective data on the parasitengone mites is external environment (as a milieu of the second available in my paper on calyptostasy (Belozerov order). This makes seasonal adaptations to be of 2008a). low necessity. The abundance and location of The most derived traits are peculiar for the vane-dwelling feather mites depend mainly on the suborder Endeostigmata represented usually by host behavioural and physiological state, particu- small hygrobiotic mites from humid habitats (for- larly on activity of uropygial glands (Blanco and est soil/litter, moss etc), though others in this group Frias 2001; Proctor 2003). Similar opinions were are xerophiles from deserts habitats. Some of them impressed already by OConnor (1984): “As mites retained the ancestral acariform type of develop- adapt to a completely parasitic existence in a rela- ment with two free-living active larvae and three tively stable “host” environment, the selective free-living active nymphs (as Speleorchestes), pressures which originally favored life-history though majority retain the single active larva, that traits such as fast generation time and good disper- follows the embryonalized prelarva, while some sal ability become somewhat reversed and coevo- others (Neonanorchestes) demonstrate a modified lutionary processes begin to dominate”. metamorphosis with alternating calyptostasy, that As we have seen, immature instars (DN or is more characteristic of another suborder of pros- TN) possessing in Acaridia the functions of sur- tigmatid mites, namely Parasitengona (Wohlmann vival (through dormancy expressed in the form of 2001; Belozerov 2008a). According to the latest diapause and apparently of post-diapause quies- molecular studies (Domes et al. 2007) the astig- cence) and dispersal (through phoresy) enable, as matid mites may be considered as a sister-group of a rule, adaptations to environmental non-predict- the endeostigmatid mites (fam. Alicorhagiidae), ability of their ephemeral habitats (though in mites and get its origin therefore not from apotypic orib- associated with insects the mentioned functions atids, but from plesiotypic endeostigmatid mites. enable the adaptation to seasonal peculiarities of We have more data on the life history for the their insect associates). By contrast, , Psoroptidia suborder Eupodina including different terrestrial due to domination of parasitic or mutualistic adap- predaceous and phyto/myceto/saprophagous mites tations, are characterized by the loss of ability for from superfamilies Eupodoidea (with families dormancy and dispersal in some instars of their Eupodidae, Penthaleidae, Rhagidiidae), Tydeoidea life cycles (as well as by the obligate absence of (Tydeidae, Ereynetidae**), Bdelloidea (Bdellidae, the DN), though in feather mites the ability for Cunaxidae), and the bdelloid-like marine mites dormancy in some instars (not as diapause, but (predatory and phytophagous) from the superfam- sooner as quiescence determined by host-parasite ily Halacaroidea (Table 3). relationships) may be retained. Especially full information among Eupodina PROSTIGMATA (= Trombidiformes)* concerns the herbivorous penthaleid mites, Halo­ Representatives of the order Prostigmata by tydeus destructor (“redlegged earth mite”) and their morphological, biological and ecological di- some cryptic species of “blue oat mites” of the ge- versity, as well known, overcome all others acari- nus Penthaleus, important pests of plant cultures form mites. This huge and diverse taxon (with and grasses in Australia and S. Africa***, where many unsolved systematic problems) includes they have polyvoltine development in winter from more than 14000 species related to some 6–8 sub- April up to November (with 2–3 active genera- ordinal groups of different size and importance. tions lasting 6–8 weeks each) and resistant egg The available data on life cycles and dormant diapause for survival during dry summer season stages in prostigmatid mites (due to their diversity (December-April). Depending on the mite species,

*Prostigmata and Trombidiformes in contemporary under- **Some representatives of the family Ereynetidae adapt to en- standing [see Mironov and Bochkov (in press)] are not syn- doparasitic habits (on vertebrates) with transformation of nor- onyms, but subdominant (in taxonomic meaning) groups in mal development to complex calyptostasy (André and Fain ranks of the infraorder and suborder, respectively. In regard 1991). to Endeostigmata, it is necessary to know, that this group had ***Penthaleus mites with the same life history of winter plant complex structure and its subgroups are transferred now into pests are known also from the southern parts of the U.S.A. the suborders Trombidiformes and Sacoptiformes. (Bauernfeind 2005).

94 Dormancy and their significance in life cycles of mites and ticks References Alberti 1973, 1974 Kethley 1991 Wallace 1970 a,b; James, O'Malley 1993; Ridsdill-Smith 1997; Ridsdill-Smith, Annelis 1997; Umina, Hoffmann 2003; Umina, Weeks 2004; Ridsdill-Smith et al. 2005 Zacharda 2004 James, O'Malley 1993; Umina, Hoffmann 2003; Umina, Weeks 2004; Umina, Hoffmann, Weeks 2004; Bauernfeind 2005 Bucking et al. 1998

- - Eg, and Ad . All ? Remarks The same Eg-La-(PN)-DN-(TN)- Eg-La-PN-DN-TN-Ad Cycle as in Penthaleidae: La , N I II III postembr. instars are preda ceous. Cycle: Ad . In brackets — calyptostases. Cycle: (phytophagous). Summer dor - mancy of aestivating eggs is en - sured by diapause, followed by post-diapause quiescence. Hibernating eggs, spring-sum mer immature stages and summer-autumn adult mites. - - ? ? ? Eg Eg Eg ed by hot Diapause quiescence. quiescence. changed into changed into treatment and treatment and post-diapause post-diapause (aestivating resist. (aestivating resist. ed by 2-month hot diapause terminat diapause diapause terminat diapause Type of dormancy ? ? _ _ _ Ad (?) Eg L, DN, Quiescence ? Eg Eg Eg TN also) (probably The same? calyptostasic Eg L, DN, Ad Dormant stages instars – PN and - Table 3. Different types of dormancy (quiescence/diapause) in dormant stages prostigmatid mites. 3. Different Table Main traits Isobactrus unicutatus ). Redlegged earth mite is an plant-pest from S. Australia important with winter development (2–3 generations of weeks 6–8 each) and (aestivating summer eggs produced by dormancy females of the pre-summer generation) terminat Winter oat mites from S. Australia and USA giving 2–3 winter generations and that eggs (aestivating dormancy summer are laid by females of all winter genera - tions). ed by impact of high temperature fol - lowed by watering. Supralittoral mite from North Germany overlap - and development bivoltine with ping generations, as well as with hiber - nation of all instars (similar to halacarid mite Mites with plesiotypic traits (slow mon - ovoltine development, low tion). reproduc - Relict periglacial predatory mite with monovoltine development and hibernat - ing eggs. Sandsoil-dwelling (phyto- and fungivo - rous) mites.

spp. ( P. major , etc.) (Penthaleidae) Mite species Nanorchestes amphibiosus Sub o r de Eu pod i na Eu podo i dea 3. Halotydeus destructor (Penthaleidae) 4. Penthaleus P. falcatus Or de r Pr ost igm ata : Sub o E ndeost 1. (Nanorchestidae) Bdello i dea Bdellidae Cunaxidae 5. Rhagidia gelida (Rhagidiidae) 2. Neonanorchestes sp. (Nanorchestidae)

95 V. N. Belozerov Lange et al. 1974; Golovach 1989; Cuthbertson, Murchie 2004 Wallace 1971 Bartsch 1972; Pugh, Bucking 1986; King et al. 1998 McCoy et al. 1969 Knop, Hoy 1983 Sokolow 1952; Makkaveeva 1956 (for H. basteri ); Straarup 1968; Bartsch 1972; Pugh, King 1986; Siemer 1996, 1999; Bucking et al. 1998 (for M. armatrus ) ­ Halotyde Isobactrus ) to A. baccarum Eg-La-PN-DN-TN-Ad : L-9, PN-14, DN-96±32, o Study with Anystis mites fed on Rhopalosiphum insertum (apple-grass aphid) used as a food. In contrast to (with only egg diapause) some other anystid mites have more rich set of dormant stages in most instars (see Olomski 1955 in Wohltmann 2001). Synchronization of life cycles in M. armatus occurs by means of diapause in DN, characterized by increased resistance to re - for cooling in necessity by and dryness activation (and into Ad). transformation Duration of instars 20 at Similarity of phenology and control its with penthaleid us (see Wallace 1970). Halacaridae comprise some groups with 1, 2 and 3 nymphal instars, from three ( one ( Copidognathus ). The same (but diapause known). is un - Cycle: (fungi- and phytophagous). Photoperiodic adult diapause. Ad -407±148 days. Eg ? _ Ad DN autumn autumn) diapause diapause facultative quiescence cold in late diapause in diapause of generations mites of the followed by Summer Egg Reproductive terminated by mated females Facultative summer-autumn ? _ _ Ad temperature DN, TN, Ad quiescence is terminated by oviposition in Post-diapause (quiescent winter watering and cool arrest followed by December-January) ? Eg Eg A d L, PN, Ad , E g DN, Ad DN, TN, aestivation - - C. o C. Reproductive winter diapause in mated, o Polyvoltine mite (about 10 at days generations 21 = time generation with April-October); during 24 Common predatory mite in apple orchards, vine - yards etc. with 2–3 generations. Females of all generations migrate down to the soil for oviposi - tion. Eggs laid by females of spring generation are non-diapause, while eggs laid by females of summer-autumn generations have photoperiod-determined winter diapause. facultative, Holarctic mite (with two nymphal instars) from Monovol - (Germany). estuaria Weser in eulittoral DN of diapause aestivation with development tine (in V–XII), cold reactivation, and long hibernat ing quiescence of Ad ovipositing in winter. Australian mite with winter development and egg and development winter with mite Australian diapause during the summer. Needs watering of eggs and low temperature to hatch after the com - pletion of diapause development. Mono/bivoltine littoral mite (with three nymphal overlap with Germany and England from instars) ping generations and year-round presence of all instars. nongravid females induced by short-day photope - short-day by induced females nongravid riod. Food — fungi, pollen etc. Acacia-inhabiting fungiforous mite from Florida (USA), having polyvolt. development with gen - eration time of 15–18 days at 25 I.

Rhombog ­ (Tydeidae) Ty deo i dea 7 . Homeopronematus anconai (Tydeidae) Sub o r de A n y st i na 11. Anystis baccarum (Anystidae) H alaca r o i dea 9. Metarhombognathus armatrus Similar monovolt. cycles with rigid diapausing con - trol in DN, typcal also for Halacarellus basteri, balticus, H. Rhombognathus pascens, R. notons, R. sea ­ hami 8. Parapronematus acaciae 6. Bdellodes lapidaria (Bdellidae) 10. Isobactrus uniscutatus Similar development in ungulatus and nathides spinipes

96 Dormancy and their significance in life cycles of mites and ticks the production of diapausing eggs occurs either cence (Wallace 1971). However the tydeoid mites during the whole winter (by females of all winter are rather different in this regard. One of them, generations in Penthaleus spp., that lay diapaus- namely Homeopronematus anconai (fam. Tydei- ing eggs on the ground and plants), or at the end of dae), is a myceto/pollen feeder and partly predator winter only (by females of the last, pre-summer in vineyards (USA), where it has approximately generation of H. destructor, whose diapausing ten generations during summer, and the reproduc- eggs are retained in dead female bodies, while fe- tive facultative diapause induced in mated, non- males from its previous generations lay non-dia- gravid females by decreased autumn photoperiod pause eggs on the ground and plants, similar to (Knop and Hoy 1983). It is possible to conclude, diapausing eggs of Penthaleus spp.). The egg dia- therefore, that in most terrestrial Eupodina with pause in H. destructor is facultative and photope- polyvoltine development, the system of life-cycle riod-dependent, while in Penthaleus spp. it is control and seasonal synchronization is based on obligatory, but in both cases termination of dia- the single regulatory dormancy-capable instar, ei- pause is enabled by reactivating impact of high ther with diapause (as in females of tydeid mites), summer temperatures during 1–2 months, though or with combination of diapause and quiescence the realization of development in potentially reac- (as in eggs of penthaleid and bdellid mites). tivated eggs becomes possible only after they are Quite different peculiarities of life history are affected by moistering and temperature decrease. characteristic of specialized group of prostigmatic Such peculiarities of life cycles in penthaleid mites eupodine mites adapted as predators and algo- and of their control by means of aestivating dia- phags for life in variable marine habitats. Accord- pause of eggs are thoroughly enlighten in publica- ing to Bartsch (2004) the superfamily Halacaroi- tions of Australian acarologists (Wallace 1970 a,b; dea comprises more than 1000 species. They are James and O’Malley 1993; Ridsdill-Smith 1997; oviparous mites with one larval and one to three Ridsdill-Smith and Annellis 1997; Umina and nymphal instars before the final moult to the adult. Hoffmann 2003; Umina et al. 2004; Ridsdill- There are known two types of seasonal life cycles Smith et al. 2005; etc). The egg diapause in pen- in halacarids, noted by the early students of halac- thaleid mites considered usually as the single dor- arid biology (Lohman 1893) and supported by re- mant stage controlling their life cycles, is combined cent acarologists. The majority of species from really with a separate stage of quiescence (as the temperate North Atlantic waters (Metarhombog­ post-diapause phase — see Hodek 1996 and Koštal nathus armatus, Rhombognathus pascens, R. sea­ 2006) retained under hot and dry summer condi- hami, Halacarellus balticus) have monovoltine tions, but terminated by the opposite factors (rain- development (Straarup 1968; Bartsch 1972; Pugh ing and cooling). That is, as it follows from pri- and King 1986; Bucking et al. 1998) with rapid mary studies of Wallace (1970a,b), the seasonal seasonal succession of La and PN, and aestiva- synchronization of life cycle in penthaleid mites is tional arrest of DN during 2–4 month, followed by ensured by combination of both kinds of dorman- transformation into hibernating Ad. Such mono- cy at the egg stage — by real diapause and by voltine development is determined mainly by the post-diapause quiescence. presence of rigid seasonal arrest in DN instar, con- The available data of other terrestrial Eupo- sidered as aestival diapause by Bucking et al. dina (though very limited) concern dormant stages (1998); but as parapause by Siemer (1999). The in rhagidiid mites (the monovoltine Rhagidia geli­ same phenology is known for monovoltine preda- da), life history traits of which are common with tory mite H. basteri both in the northern Barents the considered penthaleids, as far as the dormant See (Sokolow 1952) and in the southern Black See stage in them is represented by diapausing eggs (Makkaveeva 1956), that is undoubtedly may be also (Zacharda 2004). The tydeoid and bdelloid explained by mechanisms of life-cycle control, mites retain the common (basic) acariform onto- similar with the above mentioned halacarids, genesis and predatory habits of their soil-dwelling though special attention to ascertain aestivational ancestors (André and Fain 2000), but usually re- diapause in DN was not paid here. Another type of veal polyvoltine development. Some representa- development is known in some species of Isobac­ tives of bdelloid mites (Bdellodes lapidaria from trus (I. ungulatus, I. uniscutatus, I. setosus) and in Australia) by their life-history traits are very close Rhombognathides spinipes with mono- and bivol- to penthaleid mites due to winter development and tine development, overlapping generations and summer egg diapause with post-diapause quies- slowly expressed seasonality due to the year-round

97 V. N. Belozerov occurrence practically of all instars (Bartsch 1972; Parasitengone mites display usually the uni- Pugh and King 1986; Bucking et al. 1998), which and semivoltine life cycles completed in one or probably are capable for quiescence. two years respectively. Some many species are The regularities and peculiarities of mono- characterized also by uni-semivoltine develop- voltine halacarid development are especially well ment, when some individuals complete their de- studied in European populations of the holarctic velopment within one year, while others need two eulittoral algophagous Metarhombognathus ar­ years. Such life cycles of plesiotypic character matus (Bucking et al. 1998, Siemer 1999) with may be considered as characteristic of the stem rapid development of larvae in February-May and species of Parasitengona along with two other cor- protonymphs in March-June (with duration of 9 related traits expressed in the nymphal calyptosta- and 14 days respectively), followed by aestiva- sy and larval parasitism (Wohltmann 2001; Wohlt- tional arrest of DN in May-December and their mann et al. 2001). Multivoltine development with transformation (after cold reactivation) into some generations per year is apotypic and not adults, which represent a real hibernating stage common in Parasitengona from temperate climate, with capability for oviposition in winter. Un- especially in terrestrial Trombidia, though tropical doubtedly, the last two instars — DN in the state and subtropical trombiculid mites may give up to of summer-autumn diapause (with post-diapause 3–5 generations per year (Sasa 1961). quiescence) and adult females in the state of win- The high degree of life cycle synchronization ter quiescence — are both responsible for main- found in most species of parasitengone mites is taining the phenological regularity of monovolt- explained usually by their need in simultaneous ine life cycle. It is quite probable, however, that appearance of parasitic larvae and their hosts very long survival of adult females in this mite (Wohltmann 2001). Such an explanation fits quite (1–2 years according to Siemer 1999) may result well the situation with these mites, the larvae of the possibility of two overlapping generations which use insects and other mobile arthropods not (monovoltine as basic, and semivoltine as addi- only for many-days parasitism, but also for effi- tional), the synchronization of which is enabled cient dispersal. But, unfortunately, this approach by both dormant instars (diapausing DN with does not consider the more general aspect of post-diapause quiescence, and quiescent Ad) in evolving the synchronized life cycles in parasiten- autumn and winter. gone mites as an adaptation to climate seasonality The suborder Parasitengona represents an itself, that determines also the seasonal events in especially interesting group in Prostigmata. It con- their hosts (see also Siepel 1994). Though the role sists also (similarly to the above considered Eupo- of synchronization of life cycles in parasitengone dina with its marine Halacaroidea and other ter- mites with hosts is more evident, the available data restrial superfamilies) of two ecologically different give manifold confirmation for important role of complexes — terrestrial Trombidia and aquatic adaptations to climate seasonality and their regu- (fresh-water) Hydrachnidia, including about latory functions for this synchronization, that is 2000–3000 and 4000–5000 nominated species re- ensured, according to Wohltmann (2001), mainly spectively (Kethley 1982; Welbourn 1991). They by diapause of obligatory character at particular have common origin from terrestrial predatory developmental stage, such as the egg (Echino­ mites, the typical acariform ontogenesis of which thrombium rhodinum, Johnstoniana rapax), the has been modified into special metamorphosis adult female (Trombidium brevimanum, Eutrom­ with alternating calyptostasy, characterized by an bidium trigonum) or the calyptostasic protonymph alternation of active feeding stages (parasitic La (Leptus ignotus; L. fernandezi). These data are and predaceous DN and Ad) and non-feeding ca- presented with more details in numerous papers of lyptostases (PLa, PN and TN), and retained in al- A. Wohltmann (1995, 1996, 1997, 1998, 1999) most all extant parasitengone mites. Special char- with colleagues (Wendt et al. 1992, 1994; Wohlt- acteristic of them concerns the differences in mann et al. 1994, 1996, 2001; etc.), in his review feeding habits of larvae (parasites of vertebrate on the evolution of life histories in parasitengone animals in case of trombiculid chiggers from a mites (Wohltmann 2001), and in my review on part of Trombidia, and of different invertebrates in their calyptostasic stages (Belozerov 2008a). case of Hydrachnidia and most Trombidia), while As it follows from these reviews, the obliga- deutonymphs and adult mites always are predators tory diapause in mites with uni-semivoltine devel- of small arthropods and their eggs. opment is usually supplemented by other dormant

98 Dormancy and their significance in life cycles of mites and ticks stages (with properties of quiescence or diapause) man diseases) are investigated quite insufficiently in variable ontogenetic position. It is of no doubts in regard to their seasonal adaptations. It is of no that such combinations are peculiar not only for wonder, therefore, to read in the last comprehen- mites with complex uni-semivoltine life cycles sive review on trombiculid mites (Shatrov and (majority of Microtrombidiidae, Trombidiidae, Kudryashova 2006) that “the seasonal pattern of Johnstonianidae, and Trombiculidae), but may oc- trombiculid mite development and stages at which cur in mites with typically univoltine development they overwinter (hibernate) are still unclear”. I can (most Erythraeidae and some Johnstonianidae), add that especially unclear in them are relations of that is illustrated by the univoltine erythraeids hibernating dormant instars to diapause and quies- Leptus fernandezi with diapausing protonymphal cence. Nevertheless, it is known that some chig- calyptostase and facultative hibernation of eggs gers with uni-semivoltine development (e.g. (Wohltmann 1995, 2001), by L. trimaculatus with Neotrombicula autumnalis and Hirsutiella zach­ diapausing adults and hibernating protonymphal vatkini in Europe) have the plesiotypic capability calyptostases also (Wendt et al. 1992), and by for overwintering of most instars (Ad, Eg, La, johnstonianid Johnstoniana eximia (= J. tubercu­ nymphs) (Daniel 1961; Shatrov 2000; etc.), while lata) with diapausing eggs and hibernating adult univoltine chiggers Leptotrombidium akamushi females (Wohltmann et al. 1994). and L. pallidum from Japan have more limited Naturally, that in Trombidia with semivoltine number of instars capable for hibernation (Ad+DN life cycles, every postlarval instars (sometimes and Ad+La+TN, respectively) (Takahashi et al. even larvae) in the state of quiescence have the 1993, 1995). capacity to survive winter, while active (non-dor- Similar situation with the sets of dormant mant) instars in strictly univoltine species are not stages is characteristic of the life cycles in Hy- able to overwinter (Wohltmann, pers. comm.). drachnidia, as shown by specialists in this group According to another information from Wohlt- (Böttger 1977; Proctor and Harvey 1998; De Sa- mann, the capacity to survive winter in quiescence batino et al. 2001; Smith et al. 2001; etc) and is present sometimes even in eggs. Such affirma- shortly summarized in my reviews (Belozerov tions evidence the obligatory need of parasiten- 2007, 2008a) on life cycles of parasitengone mites. gone, as of all other mites, in possessing dormant The diversity of dormant stages in Hydrachnidia is state of any kind for efficient hibernation at defi- about the same as in their terrestrial relatives, inas- nite instars. much as in both groups for seasonal dormancy are The simple treatment of data from my paper able not only mobile Ad and DN, but also immo- on calyptostasy (Belozerov 2008a) have shown bile eggs and calyptostases (PN and TN), and even that Microtrombidiidae with uni-semivoltine cy- larvae (not only unfed and engorged, but also at- cles have 2–4 dormant instars (majority have two, tached to their hosts for feeding). The presence of one of which is adult female), Trombidiidae have numerous dormant stages ensures not only the bet- 2–3 (usually two, one of which is female also), ter seasonal synchronization of life cycles, but and Johnstonianidae have three (one of which is also increases their flexibility and therefore the egg stage). In contrast, mites with strongly mono- more efficient adaptation of parasitengone mite voltine cycles (practically all Erythraeidae*) have populations to unpredictable environmental as a rule the single diapausing instar (of variable changes. ontogenetic location, but usually eggs or calyp- The suborder Anystina is represented by tostasic PN). Namely these two dormant stages of eight families of soil/litter-dwelling, middle-sized erythraeids can be found during the most part of predaceous mites, plant-inhabiting representatives the year, in contrast to active La, DN and Ad with of which reveal their connections with soil through their limited occurrence along the year (Southcott oviposition. It is considered as a sister taxon of 1961). Parasitengona (Wohltmann 2001), but ontogeneti- Unfortunately chiggers (the family Tromb- cally the Anystina are characterized by two active iculidae), being the most important group among nymphal instars. One of its species, the so called terrestrial Trombidia (as vectors and agents of hu- ‘whirli-gig’ mite, Anystis baccarum, is very com- mon and efficient predator of small arthropod *The family Erythraeidae is considered now as a separate pests in apple orchards, vineyards etc. According taxon (Erythraeina) that is equivalent for Trombidiina and to data from Russia (Lange et al. 1974; Golovach Hydracarina inside the Parasitengona (Mironov and Bochk- ov, in press). 1989) and Ireland (Cuthbertson and Murchie

99 V. N. Belozerov

2004), A. baccarum has two-three generations de- Special place among Cheyletoidea take repre- veloped on plants and the same number of corre- sentatives of seven separate families, comprising sponding egg-layings into soil with non-diapause big number of mites adapted to diverse form of eggs in first generation, and diapausing hibernat- parasitism on vertebrate animals. As was noted by ing eggs in next generation(s). Naturally, the egg Kethley (1982), each of these families is charac- diapause in this bi/polyvoltine mite is facultative, terized by rather morphologic uniformity through and probably is determined by photoperiod. Some great reduction, and by close restriction of these ontogenetic peculiarities (two-nymphal postlarval permanent parasites to a definite class of hosts. development) and the reduced character of life- The families of Demodicidae, Myobiidae and cycle control (with the only diapausing egg stage) Psorergatidae are parasites of mammals, while the evidence for rather apotypic evolutionary trait of families of Syringophilidae and Harpyrhinchidae this species, though other representatives of this are parasites of birds. The last two families (Ophi- group are known to be more plesiotypic, as far as optidae and Cloacaridae) represent ectoparasites the control of their life cycles is quite diverse, be- of snakes and turtles respectively. Being the spe- ing supported not only by diapause (obligatory or cialized permanent parasites of mentioned verte- facultative), but also by dormancy of consecutive brate animals, these parasitic cheyletoids are quite type, i.e. quiescence (Olomski 1995 — cited from comparable with psoroptid representatives of Wohltmann 2001). astigmatid mites (especially with parasites of The next subordinal taxon, Eleutherengona mammals) in regard to the reduction of seasonal (= Raphignathina), consists of four superfamilies, adaptations (in general) and to the failure of spe- two of which (Raphignathoidea and Cheyletoidea) cial dormant stages (in particular) due to domi- are represented mainly by predaceous mites with nance of parasitic adaptations. rather derived traits, and also by deeply special- Much more we know about the life history ized parasites of vertebrate animals*, while two traits in the specialized and agriculturally impor- others (Tetranychoidea and Eriophyoidea) com- tant, phytophagous eleutherengone mites from prise highly specialized phytophagous mites (Ta- two superfamilies — Tetranychoidea (with ple- ble 4), some of which are important agricultural siotypic features in morphology and ontogenesis, pests making serious injury for diverse plants but with apotypic traits in systems of their season- (Jeppson et al. 1975). al control), and Eriophyoidea (with great apotyp- One of the raphignathoid mites from the fam- ic reductions in their morphology and ontogenesis, ily Stygmaeidae, arboreal acarophagous Zetzellia but, in contrast, with more derived, plesiotypic mali (studied in apple orchards of southern Cana- and variable systems controlling the seasonal life da) has polyvoltine development broken by hiber- cycles). nal diapause of adult females and restored next The superfamily Tetranychoidea contains 5 spring after cold reactivation of overwintered fe- families, three of which are monogeneric and bio- males (White and Laing 1977). Quite possible that logically not investigated, while two other fami- tropical stygmaeid mite Agistemus floridanus, an lies — Tetranychidae (spider mites) and Tenuipal- important predator of Tenuipalpus heveae in Bra- pidae (false spider mites) are obligate plant feeders zil, may have the seasonal dormancy in adult fe- and agricultural pests of great economic impor- males also, as far as its prey T. heveae possess the tance. The first family (Tetranychidae) contains capability for reproductive diapause (Poutier et al. approximately 40 genera and over 600 species, in- 2000). habiting higher flowering plants and trees (sub- Very few we know about dormant events in fam. Tetranychinae) or grasses and low-growing cheyletoid mites, especially in common preda- plants (subfam. Bryobiinae). They are medium- ceous representatives of the family Cheyletidae sized oviparous mites with rapid polyvoltine de- (possibly due to their low efficiency as controlling velopment (5–7 and more generations in the sea- agents), though some cases of phoresy of chey- son with the average generation time of two weeks letid females on beetles are known, that allows to — Sabelis, 1991), that is stopped either by egg compare this trait of them with dormancy and oth- (embryonic) diapause (in eight genera — Bryobia, er properties of phoretic DN in astigmatid mites. Petrobia, Schizonobia, Aplonobia, Eurytetrany­ chus, Schizotetranychus, Panonychus and Oligo­ * More information on predaceous and parasitic representa- nychus), or by reproductive diapause of adult fe- tives of cheyletid mites is given in a book by Akimov and Gorgol’ (1990). males

100 Dormancy and their significance in life cycles of mites and ticks References Kethley 1982 Zacher et al. 1981 Saleh et al. 1986 Kapil, B hanot 1972 B oczek 1959 Kanavel, Selhime 1967 White, Laing 1977 Ferla, M oraes 2003; G oldarazena et al. 2004 - C. o . . Z. mali F. o Agistemus fed Remarks C 20–23 days, to male C. Longevity of female o o Eg, La, PN, DN, Ad Eg, L, PN, DN, Ad 70–95 days. Development time of Eg and (6–6.5 L days each), PN (5–6 days each) at 75 and DN (without DN) 15–17 days. (with female of time Development two nymphs) is 37–43 days, male of (with one days at 25 nymph) 30–36 Survival of Ad is 10–13 days. Pre - days. 10–13 is Ad of Survival daceous. Generation lasts 14.4 days at 35 at days 14.4 lasts Generation The acarophagous mite from Canada was studied under laboratory conditions. Mean gen - eration time is 21 days. Diapause in overwintered females is termi nated after cold reactivation. Cycle: All three species of spider mite eggs and plant pollen. 30–38 is them of times Generation days. Cycle: Development from Eg to female lasts at 25 ? ? ? ? Ad Ad ? (winter Diapause diapause) reproductive Type of dormancy ? ? ? ? _ _ Quiescence ? ? ? ? ? Ad Dormant stages Table 4. Different types of dormancy (quiescence/diapause) in dormant stages Eleutherengona. 4. Different Table Medio ­ Trogoder ­ Tenuipalpus Aleuroglyphus Aleuroglyphus Agistemus , Main traits , Zetzellia in Brazil. Low efficient agent for control of spider mites with life cycle of 2 month. This predaceous cheyletid mite Egypt cultured on tetranychid from eggs and immatures. No data on its seasonality. ma . Culturing in India on eggs of Species of lata are arboreal predators of phytopha - gous mites and insects in orchards many countries. of heveae Longevity of females = 25–35 days. A. floridanus is predator of This predaceous cheyletid is taken from the culture of grain mite ovatus .

(Stigmaeidae) Mite species Agistemus floridanus, A. 7. Paracheyletia bakeri (Cheyletidae) 6. Cheletogenes ornatus (Cheyletidae) 9. Cheyletus eruditus (Cheyletidae) 8. Acaropsis docta (Cheyletidae) 1. Zetzellia mali Pr ost igm ata : E le u the r en g ona Raph ig nathae Raph ig natho i dea (contains 9 families of primarily predaceous mites; some species Stigmaeidae are phytophagous) (Stigmaeidae) 2–4. cypriu, A. industani C he y leto i dea (contains 8 families of predaceous and parasitic mites) 5. Cheyletus malaccensis (Cheyletidae)

101 V. N. Belozerov G abele 1959; Veerman 1985; Hallas, G udleifsson 2004 Veerman 1985 Veerman 1985 Veerman 1985 Koveos, Tzanakakis 1991 Kethley 1982 B ondarenko 1950; G eispitz, Orlovskaja 1971; G linyanaya 1972; Veerman 1985; Kroon, Veeendaal 1998; G rbic et al. 2007 U shida 1980; Veerman 1985 Veerman 1985 - . . Panonychus ulmi Tetranychus urticae In Central Europe this mite laid aestivating and hibernating eggs hatching spring. Active development simultaneously in summer. The hi - in in possible is adults and larvae eggs, of bernation Iceland, but in Switzerland it has year-round de - velopment with a few of diapausing eggs laid in summer. early in begins Canada in eggs winter of Hatching Septem in hatch to begin eggs Aestivated spring. ber with hatching peak before the cool period. Hatching of winter eggs occurs in Canada 2–3 weeks earlier than of Egg diapause completes in January. Diapausing eggs are laid by females under long- day photo-periods. Arrest after of terminated and humidity, low by maintained late embryos is eggs were hydrated. Diapause is finishedmonth (with no chilling). in 2 Photoperiod is connected both with induction and induction with both connected is Photoperiod maintenance of diapause. During serves to retain the state of diapause until the ar - diapause it development Diapause temperatures. low of rival is ended at the beginning of winter, but mites re - tain dormant state till spring (by means of post- diapause quiescence). Great similarity in mechanisms controlling win - ter diapause with Mass migration of females in autumn down to the to down autumn in females of migration Mass trunk for their places of hibernation (before pig - speci - diapausing for specific changes, mentation men). - - - female female eggs. female dia - Aestivating and hibernating diapausing eggs. Hibernating diapaus ing eggs. Hibernating diapaus ing eggs. facul - of diapause Egg tative summer charac ter. Summer and winter diapausing Hibernating or aesti - vating pause determined by photoperiods. Hibernating diapause. Hibernating diapause. _ _ _ _ _ Ad Ad Ad Egg Egg Egg Egg Egg (aestivation) - Oxalis and On grass and herbaceous plants. In Switzerland this clover mite has two gener - ations, separated by aesti val and hibernal diapauses of eggs. The brown mite infesting fruit trees. In Switzerland it is polyvoltine species. This monovoltine species Swit - in bushes berry infest zerland. Cosmopolitan mite living on leaves of other plants. Active poly - voltine development cool season, with egg in dia - pause in summer. Cosmopolitan plant pest with polyvoltine develop - dia - reproductive and ment pause of adult females. spi - polyphagous Common S. and Japan from mite der Asia. Lime tree inhabitant with polyvoltine development and winter diapause of fe - males. grass - on develops Usually es with diapause in eggs laid in May-June.

14. Bryobia praetiosa (Tetranychidae) 15. Bryobia rubrioculus (Tetranychidae) 16. Bryobia ribis (Tetranychidae) 17. Petrobia harti (Tetranychidae) 10. Tetranychus urticae 11. Tetranychus kanzawai (Tetranychidae) (Tetranychidae) T et r an y cho i dea 12. Eotetranychus tilarium 13. Bryobia cristata (Tetranychidae) (Tetranychidae)

102 Dormancy and their significance in life cycles of mites and ticks Lakshman 1978 Childers et al. 2003 NPA G data 2000 Düzgünes 1969 Poutier et al. 2000 R ashki et al. 2004 G otoh 1986 Loyttyniemi 1970; Shinkaji 1975 Lees 1950; M iller 1950; Veerman 1985 Attiah et al. 1973 - C =26 (fe - o _ _ _ _ _ male) and 19 (male) days. Egg diapause is induced by short-day photope - riod in females, and terminated by 40-day cold exposure (as well as by 50-day “winter-habit” females from Sapporo). exposure of Diapause of winter eggs completes from Janu - ary and reaches max in February/March with 50% hatch in April/May. Diapause is photoperiodically determined and reqieres very long chilling (150–200 days and more) to be completed. The diapause termina tion is followed by post-diapause cold quies - cence. 11 generations (in Egypt) with duration of 17 days each in summer up to 47 days in late au - tumn. Overwintering females begin activity at the end the at activity begin females Overwintering of April and give three generations per year. Development from egg to egg at 32 dia - Egg Egg dia - Hibernating Hibernating pause. Ad (?) pause Hibernating diapaus - ing eggs Hibernating repro - ductive diapause Hibernating repro - ductive diapause Hibernating repro - ductive diapause Hibernating repro - ductive diapause Hibernating repro - ductive diapause Hibernating repro - ductive diapause Hibernating repro - ductive diapause ______Egg Egg Adult Adult Adult Adult Adult Adult Adult females females females females females females females Egg, Ad - C respec - o C and 27 o Cosmopolitan arboreal mite with polyvoltine development (4 gener - ations in Sweden, 6–8 in Red USA). diapause eggs are laid from September to November. tively). Longevity of each species is two to two is species each of Longevity three times more than in various tetranychid mites. Duration of generation 44.5 days. Apple tree pests in Turkey of hibernation and generations two with females. polyvol - with pest citrus Important tine development and hibernating adult females. ple. In Europe has one generation, in Iran, Iraq and Egypt three gen - erations per year. Flat scarlet mite is pest of pear/ap The conifer mite distributed from Finland to Japan. polyvol - with Iran in pest apple An tine development and overwinter - ing females. Hibernation of this mite in Hok - kaido normally takes place at egg stage, though winter from Sapporo consists population of eggs and “winter-habit” females. Life cycle is completed in 20 and 30 days (at 21

Brevipalpus Brevipalpus ­ califor Brevipalpus californicus (Tetranychidae) 18. Panonychus ulmi 27–30. nicus, B. obovatus, B. phoe ­ nicis, B. lewisi (Tenuipalpidae) (Tenuipalpidae) 23. Cenopalpus bakeri (Tenuipalpidae) 24. Tenuipalpus heveae 25. (Tenuipalpidae) 22. Cenopalpus pulcher (Tenuipalpidae) 20. Oligonychus ununguis (Tetranychidae) 21. Cenopalpus irani (Tenuipalpidae) 19. Panonychus akitanus (Tetranychidae) 26. Brevipalpus phoenicis (Tenuipalpidae)

103 V. N. Belozerov Caresche, Wapshere 1974 I nternet Ozman, Toros 1997; Ozman 2000 Ozman, Toros 1997 Ozman 2001 Westphal et al. 1990 Ozman, G oolsby 2005 Jeppson et al. 1975; Kozlowski, B oczek 1989; Oldfield, Manson 1996 Jeppson et al. 1975; Oldfield, M anson 1996 - ­ Phytop vagrans from elms from maples from Vasates _ _ _ _ Rhincaphytoptus ulmi Gall form with a single nymphal type.and simle type.and nymphal single a with form Gall life cycle. In spring its nymphs migrate from old buds to healthy buds, where occurs devel opment. tus . avellanae Reproduction continues during winter. of species two and Ulmus Acer spp. (Jeppson et al. 1975). Without alternating females specialised for hi - bernation; Inhabits the same buds, as gall form of form gall as buds, same the Inhabits Similar complex cycles with deuteroginy have also A potential biological control agent of climbing of agent control biological potential A fern by means of premature fern defoliation of this aggressive weed in Australia. Tegono - N2 , in va - No No Ad? N? N3. Ad + Ad + N2 N2 and Ad Deutogynes Deutogynes Deutogynes In gall form grants tus-like – – ______No No and Ad Ad? N? Nq2, N3 Ad + N2 N2 and Ad Deutogynes Deutogynes Deutogynes - - - Chon ­ Solanum dulca ­ Convolvulus arven ­ Convolvulus Acer negunde in Turkey Lygodium microphyllum , S. European polyvoltine gall mite Hi - females. of form one only with bernation in leaf rosettes of drilla juncea without reproduction and gall formation. Gall mite from mite Gall sis . Overwinters as an nymph below adult ground on rhizome or buds. with polyvoltine summer develop ment (3–4 generations) and over - wintering deutogynes crevices). (in bark Common pest of filbert (hazelnut) with 2 types of life cycles (simple complex modified and mites gall in in vagrants). Also pest of filbert (hazelnut) with modified complex cycle. Inhabits buds, where develops and hiber - nates. The leaf vagrant on box elder ornamental Gall mite from mara wiuth simple polyvoltine de - velopment. ment with producing galls. leaf roll The important pest of fern, climbing having non-interrapted develop Vagrant mite, very common poly - voltine pest of apples with terogeny. deu - eny. Vagrant mite, very common poly - deuterog with pears of pest voltine

Eri oph y o i dea 31. Aceria chondrillae (Eriophyidae) 32. Aceria malherbae (Eriophyidae) 33. Phytoptus avellanae (Phytoptidae) 34. Cecidophyopsis vermiformis (Eriophyidae) 35. Rhincaphytoptus negundivagrans (Diptilomiopidae) 36. Aceria cladophthirus (Eriophyidae) 37. Floracarus perrepae (?) 38. Aculus schlechtenali (Phytoptidae) 39. Epitrimerus pyri (Phytoptidae)

104 Dormancy and their significance in life cycles of mites and ticks Sukhareva, Sapozhnikova 1975; Sukhareva 1992 Sukhareva, Sapozhnikova 1975; Sukhareva 1992 Shevchenko, De- M illo 1968 B agnjuk 1976 B agnjuk 1984 Löyttyniemi 1971 Hassan, Keifer 1978 Sokolov 1986 Shevchenko 1957 Shevchenko Picea abies ______N.haarlovi , infests needles of and givies 4–8 generations, overwinter only as diapausing eggs laid by females from two last generations. The cold reactivation of di - apause eggs occurs by January and followed afterwards possibly with cold quiescence. _ _ Nymphs 2 Deutogynes Deutogynes Deutogynes Deutogynes for dispersal Non-dormant Diapausing eggs deutogynes serving _ _ _ _ _ hibernate nymphs ? plus eggs ? protogynes Hibernating Protogynes Protogynes All stages of plus eggs and life cycle may _ eggs cycle nymphs Nymphs 2 simple life protogynes Protogynes Deutogynes Deutogynes Deutogynes and protog - All stages of Deutogynes, Hibernating plus eggs and ynes plus eggs - - - Pi ­ Ju ­ character Abies sibirica Picea Common grass-inhabiting mite. ment in buds of ized by every-year alternation of protogyne and deutogyne genera - hibernate to capable are which tion together with eggs and immature instars also. Common grass-inhabiting known as vector of virus diseases. mite, Gall mite with biennial develop Gall mite with biennial develop ment in “berries” of mountain niperus is peculiar by every-year change of summer and winter gen - erations. Gall fir mite from with biennial development and hi - bernating nymphs of second gen - eration. Vagrant coniferous mite from cea needles with polyvoltine de - velopment and diapausing eggs. Vagrant mite leaves in many tropical countries. infesting mango Leaf-eryneum birch mite with aes - tivo-hibernating deutogynes. Bivoltine alder leaf gall mite with hibernating deutogynes from sec - ond generation. (?)

Trisetacus kirghizorum 48. Phytocoptes deschampsiae (Phytoptidae) 46. Trisetacus piceae 47. Abacarus hystrix (Phytoptidae) (Phytoptidae) 45. (Phytoptidae) 44. Trisetacus bagdasariani (Phytoptidae) 43. Nalepella haarlovi (Phytoptidae) 42. Cisaberoptus kenyae 41. Eriophyes leionotus (Eriophyidae) 40. Eriophyes laevis (Eriophyidae)

105 V. N. Belozerov

(in mites from four other genera — Tetranychus, ment of hatch in overwintered eggs of spider mites Eotetranychus, Platytetranychus and Neotetrany­ (Veerman 1985). The same conclusion concerns, chus, plus one species of the genus Oligonychus, of course, the synchronization of reproduction in namely O. pratensis). The egg diapause is consid- overwintered adult females of spider mites, and of ered as a derived ancestral trait, while the adult moult in overwintered immatures of some other diapause as a secondary apotypic feature (Gutier- mites. rez and Helle 1988). Quite possible that this trait There are known some cases when tetrany- concerns some other acariform mites. Both types chid mites reveal unusual peculiarities in their hi- of diapause in spider mites are facultative, and bernating stages. For instance, the monovoltine have a lot of common with insects in their photo- Bryobia cristata in subarctic conditions of Iceland periodic control (Veerman 1985, 2001). The role can overwinter not only by diapausing eggs, but of photoperiod in diapause induction was discov- also at larval and immature instars in unknown ered simultaneously in Panonychus ulmi with egg dormant state (Hallas and Gudleifsson 2004). The diapause (Lees 1950; Miller 1950), and in Tet­ possibility of hibernation in spider mites at some ranychus urticae with adult diapause (Bondarenko instars, though with low survival (as in Tetrany­ 1950). The latter species, owing to easy cultiva- chus takafujii infesting Solanum nigrum in Central tion, rapid development and accuracy of photope- Japan), can be explained suggestively by their in- riodic responses, is one of the main models (to- troduction from tropical or subtropical areas gether with some insects) in the study of (Ohashi et al. 2003). Another, more interesting ex- mechanisms of seasonal photoperiodism in arthro- ample is represented by Panonychus akitanus that pods (Veerman 1985, 2001). Due to the noted and hibernate in Hockaido (Japan) both by diapausing other advantages, T. urticae is suggested also as eggs and adult “winter-habit” females, and such a the perspective genetic model for studies in devel- population with two different dormant stages may opmental biology (Grbic et al. 2007). represent a transient evolutionary state from egg The diapause in spider mites has been consid- to adult diapause, or vice versa (Gotoh 1986). In ered (mainly on the basis of studies of its induc- spite of those supplementary notes, the typical tion) as the main, if not the single instrument that trait for spider mites (Tetranychidae) is represent- determines peculiarities of their seasonal develop- ed by diapause in eggs (as of primary kind) or ment. However, some available data on termina- adult females (as of secondary kind). tion of diapause make to suggest, that restoration The second family (Tenuipalpidae) contains of active development after diapausing state in- 15 genera and 290 nominated species distributed volve also processes of quiescence in the same mainly in tropical and subtropical regions. These manner, as in penthaleid prostigmatid mites (see small-sized mites with many traits of morphologi- p. 97). I mean the data concerning the aestivating cal and ontogenetic reduction are important pests egg diapause in Petrobia apicalis (Zein-Eldin of commercial orchards, vineyards, tea plantations 1956) and P. harti (Koveos and Tzanakakis 1991) and grass pastures. They are oviparous and have requiring high temperature and relatively dry at- rapid polyvoltine development that is stopped only mosphere for maintenance of resting state, but at the stage of adult females with reproductive dia- rather low temperature and high humidity to break pause. The mentioned apotypic specialized traits it and to evoke embryonic development. Being in morphology and ontogeny coincide here with very expressive in cases with aestivating diapause, the same apotypic features of their dormant instar. the role of quiescence as synchronizing agent is False spider mites develop slower than tetrany- less obvious in cases with hibernating diapause, as chids (see Table 5), their generation time is about far as the resting state is maintained here (simulta- 20–40 days at 20–30oC. Species of the genus neously with events resulting the developmental Cenopalpus give annually from one (in Europe) to potentiality) by low temperatures and is broken two (in Turkey) and three generations (in Iran, during post-diapause quiescence by an increase of Iraq and Egypt). Hibernating females are in the temperature. The interface of these events en- state of diapause, which is unfortunately not stud- abling firstly to reach the covert potentiality for ied in details. development (at the end of diapause), and to real- The last eleutherengone superfamily Erio- ize it afterwards during post-diapause quiescence phyoidea (the so called four-legged mites) con- (Hodek 1996; Koštal 2006) is of great adaptive tains three families (Eriophyidae, Phytoptidae and significance for “coarse” and “fine” time-adjust- Diptilomiopidae, comprising more than 50 genera

106 Dormancy and their significance in life cycles of mites and ticks References White, Sinha 1982 Doberski 1986 Baker, Wharton 1952; Internet 2007 Gerson 1992 Volkonsky 1940 (cited from Baker, Wharton 1952) Baker, Wharton 1952 Lombardero et al. 2000 - — in win - population is Remarks The same D. vandefriei Tarsonemus adult peaces in autumn females to infest other bees. Eg-La-Ad . Pharate females Eg-La-Ad . In 40 days (devel There are no seasonal changes in mite in changes seasonal no are There abundance, in spite of strong changes of temperature in granaries. Fungivo - rous. D. hewitti (Aug-Oct) and in May), but of spring (March- ter (max January). Algophagous. Mites live in tracheal tubes of adult the outside move only and bees honey host as Parasitic. The family Podapolipidae comprises parasites of different arthropods and characterized by the highest level of ontogenetic and morphological duction.. re - Cycle: (often termed “pupae” or “quiescent nymphs”). Short-lived males and fe - males (about 1 week). Phytophagous. Cycle: opmental time of beetle generation) increase of mites all in time Generation 170–380. is 18–19 days. Female lives 28 days. Fungivorous. ? ? ? ? _ ? _ Diapause ? ? ? ? _ ? _ Type of dormancy Quiescence as ? ? ? Ad bees infestation copulation Ad female an agent of Dormant stages Mite female as a La as an agent of Larval female infestation of new infestation of adult locusts during host short-lived agent of Table 5. Different types of dormancy (quiescence/diapause) in dormant stages heterostigmatid mites. 5. Different Table Ophiostoma Dendroctonus fron ­ Main traits C. Annually may give 20–30 o The honey bee tracheal mite, is an internal parasite of adult bees. It has one generation mul - but bees, summer short-lived in host per win - in bee each in mites of generations tiple ter. Mycophagous mite. Generation is 10 days, life of females 17 days. Ectoparasite of locusts in North Africa with Infes - females. adult and larval of alternation tation of hosts (by means of larval mite fe - males) during host’s copulation. Two species of mites (algo-lichenophagous) from Elm bark with strong adult seasonality and of larval abundance correlated with bark epiphytic algae dynamics. Mite parasitic within tracheal tubes and air sacks of locusts and grasshoppers. Eggs are laid by physogastric females also there. Tropical and subtropical plant pest with poly - with pest plant subtropical and Tropical voltine development. The generation lasts 1 week under 25 generations. talis , which larvae need fungus Phoretic females of mites these on the pine beetle micetophagous minus , the best food for all three mites. r Mite species 8. Acarapis woodi (Tarsonemidae) 7. Tarsonemus granaries (Tarsonemidae) 9. Podapolipus diande (Podapolipidae) 5–6. Daidalotarsonemus hewitti, D. vandefriei (Tarsonemidae) 10. Locustacarus trachealis (Podapolipidae) 4. Polyphagotarsonemus latus (Tarsonemidae) Or de r Pr ost igm ata , Sub o H ete T a r sone m o i dea 1–3. Tarsonemus ips, T. krantzi, fusarii (Tarsonemidae)

107 V. N. Belozerov Keith, Kalisch, Broce 2005 Baker, Wharton 1952; Bruce, LeCato 1979 Schousboe 1986 Zou et al. 1993 Rack, Eickwort 1979 Gao, Zou 2001 Cross, Kaliszewski 1988 Clift, Larsson 1987; Gao Zou 2001 Eg-Ad . No data Eg-Ad . Eggs de - females. Histoplasma capsulatum . Eg-La-Ad . Two types of fe - Agaricus in the soil. Fungivo - Eg-La-Ad (phoretic and phy - Reproduction by physogastric lium of Cycle: direct development of adult mites (female and male) inside physogastric female. Parasitoids. the myce - on cultured Easy Fungivorous. Direct development of adult (female and mites male) inside the physo - gastric female. Saprophagous/fungivorous mite feed - mite Saprophagous/fungivorous ing in bee nests on faeces of bee lar - vae. Cycle shortened to velop directly into adults within phy - sogastric female, where mating oc - curs. Fungivorous. Cycle shortened to on phoretic dispersal. Fungivorous. Cycle: males — phoretic (dispersal on Dip - tera) and non-phoretic. Fungivorous. sogastric females). Detachment phoretic mites and their of reproduction is determined by the presence of my - celium rous. Cycle: ? ? ? ? ? Ad Ad Ad phoretic females) (diapausing ? ? ? ? ? ? _ ? - ? ? ? Ad tions females females) Dispersing Ad female Ad female Ad (phoretic phoretomorph phoretomorph different genera unfed females of in fallen galls and non-phoretic unfed Ad (gravid females - Sitotroga moth Agaricus . . Agapostemon nasutus . Bombus and Psithyrus . myce - bisporus Agaricus C); phoretic as adult females on females adult as phoretic C); o C. o Phoretic females occur on hibernating males of bumblebees fe - P. herfsi , parasite of larval midges that in - duce leaf galls of pin oaks. Polyvoltine mite with physogastric females April-November and dispersed as developed unfed fe - in males in August-December. and other grain pests. Mite females are agents are females Mite pests. grain other and of human hay (grain) itch. Polyvoltine mite (Costa-Rica), associuated with polyvoltine bees Polyvoltine ectoparasitoid of Olygophagous pest of farming Auricularia polytricha mushroom New pest in mushroom farms. Its food is my - is food Its farms. mushroom in pest New celium of wild moulds and Monophagous pest in mushroom farms, with polyvoltine development (generation time is 27 at days 10 ment with generation 21–25 time = 5 days at Polyphagous fungiforous mites using differ - ent wild moulds as a food. Rapid develop lium. some flies. Food — Food flies. some

Pediculaster mesembri ­ Pediculaster Pyemotes tritici, P. ven ­ Parapygmephorus costari ­ Parapygmephorus 9. Scutacarus acarorum (Scutacaridae) 8. Pyemotes herfsi (Pyemotidae) 5. canus (Pygmephoridae) 6–7. tricosus (Pyemotidae) 4. Luciaphorus auriculariae (Pygmephoridae) 3. Dolichocybe perniciosa (Pygmephoridae) Pygm epho r o i dea 1. Brennandania lambi (Pygmephoridae) 2. Pediculaster flechtmann (Pygmephoridae) Also nae (Pygmephoridae)

108 Dormancy and their significance in life cycles of mites and ticks and 2000 species of obligatory phytophagous galls and premature defoliation of this Australian mites with high host-specifity*. Morphological aggressive weed (Ozman and Goolsby 2005). and ontogenetic peculiarities of eriophyoid mites The presence of two types of females (deu- (extremely small-sized vermiform body, retaining terogeny) is typical for the majority of these mites only two pairs of legs, the reduced postembryonic from deciduous plants in temperate areas with ob- development with only two immature instars con- vious seasonality, but occurs in species from ever- sidered as larva and nymph, or nymphs I and II) green and tropical plants also (Table 4). In general, are uniform in all these mites, having monophyl- the heteromorphic deutogyne females serve for hi- etic origin and possessing very tight co-evolution- bernation and aestivation in the state of diapause, ary connections with their host-plants. But in con- but are capable for dispersal also. Deutogynes of trast, they have a large diversity in their life cycles tropical vagrant Cisaberoptus kenyae from mango (poly-, bi-, mono- and semivoltine development), leaves have no dormancy, and serve for dispersal and in their systems of seasonal control (with only. many, some and single dormant stages) enabling It is of interest that no true deutogyne females diverse versions of life cycles (Table 5). Thus, were discovered in grass-inhabiting eriophyoid Eriophyoidea reveal quite contrasting situation, as mites that overwinter either at the stage of protog- was told above, concerning the relationships be- yne females (Abacarus hystrix), or at every stages tween apotypic morphological and ontogenetic of their life cycle (Phytocoptes deschampsiae) traits (from one side), and rather plesiotypic traits (Sukhareva and Sapozhnikova 1975; Sukhareva in diversity of their life histories, especially of sea- 1992). It is possible that in the last case (but may sonal peculiarities of life cycles (from another be in both cases) the hibernation is realized through side). the state of quiescence, as far as populations of Such diversity is revealed firstly in the pres- grass-inhabiting eriophyoid mites are affected by ence of two categories of these mites (according to temporary and unpredictable environmental fac- places of their feeding, reproduction and develop- tors quite more, than arboreal eriophyids (Sko- ment). They live either in buds, galls, erineums racka and Kuczyński 2003). and other plant deformations giving them a shelter Eriophyoid mites reveal a large diversity in and food source (namely “the gall mites”), or in- regard to their systems of seasonal control that habit rather open surface of leaves and other veg- may involve many overwintering stages, as in the etative and generative plant organs (the so called gall/bud-living coniferous mites Trisetacus kir­ “vagrants”). Diptilomiopid mites are principally ghizorum (Shevchenko and De-Millo 1968) and T. surface vagrants, while eriophyids and phytoptids piceae (Bagnjuk 1976), or the only overwintering relate to gall mites usually (Kethley 1982). Repre- eggs in the vagrant coniferous mite Nalepella sentatives of both these categories may have life haarlovi (Löyttyniemi 1971), as well as the only cycles of different complexity — either simple deutogyne females in vagrants Aculus schlechten­ cycles (with one type of adult females that repro- dali and Epitrimerus vitis (Kozlowski and Boczek duce throughout the year under favorable condi- 1989; Manson and Oldfield 1996) from apple- tions), or more common complex cycles (usually trees and grapes, and in the alder gall mite Erio­ with two types of adult females — summer repro- phyes laevis (Shevchenko 1957). It is known now, ductive protogynes and dormant deutogynes with that in some eriophyoid mites the arrest of devel- diapausing arrest of reproduction). Simple cycles opment at the stage of adult females (mainly deu- are characteristic, for instance, of the gall mite togynes, but protogynes in some cases also) is in- Aceria cladophthirus from Solanum dulcamara duced by photoperiod (Sapozhnikova 1982), while (Westphal et al. 1990) and subtropical Floracarus its termination is enabled usually by long chilling perrepae with non-interrupted polyvoltine devel- in winter, as in many other species with diapaus- opment on its native host, the climbing fern Lygo­ ing dormancy (Jeppson et al. 1975). For instance, dium microphyllum; with formation of leaf roll the cold reactivation of diapause in overwintering eggs of N. haarlovi is completed by January (Löyt- *The used taxonomic approach corresponds to Kethley (1982). More recent taxonomy of Eriophyoidea is presented in the tyniemi 1971), being followed afterwards un- Catalog of Amrine and Stasny (1994). The full information doubtedly with the cold-maintained post-diapause about these mites is given in the comprehensive manual quiescence. “Eriophyoid Mites — Their Biology, Natural Enemies and Deutogyne females are the main dormant Control” (1996) under the editorship of Lindquist, Sabelis and. Bruin, published by Elsevier Science. stages in eriophyoid mites. Nevertheless, in some

109 V. N. Belozerov species the same role is characteristic of nymphal have apparently secondary, derivative characters instar specialized for hibernation and resumption (Belozerov 2007). of spring development after overwintering, either The special case of life cycles is presented by together with adult females as in Aceria mal­ the mentioned P. avellanae (Krantz 1979; Ozman herbae, inducing gall formation in the field bind- and Toros 1997; Ozman 2000). Differing from weed Convolvulus arvensis, and in the vagrant other phytoptids, this filbert (hazelnut) mite has form of the filbert pest Phytoptus avellanae (Oz- two different types of life cycles (simple cycle in man and Toros 1997; Ozman 2000), or among the gall form and specific complex cycle in the va- other hibernating stages as in the coniferous bud grant form). In both vagrant and bud forms of this mite Trisetacus piceae (Bagnjuk 1976), or even species the overwintering instars are represented alone as in the gall fir mite Trisetacus bagdasari­ by nymphs, which hibernate in buds. In gall form ani (Bagnjuk 1984) and in the gall form of the fil- the hibernated nymphs migrate in spring from old bert mite P. avellanae (Ozman and Toros 1997; buds to new healthy buds, where they reveal the Ozman 2000). temporary, month-long dormancy before moult- Some more data on seasonality of develop- ing to adults, and further development of station- ment and on dormant stages in eriophyoid mites ary polyvoltine population begins only afterwards are given in the book of Jeppson, Keifer and Baker inside the infested bud. The same temporary dor- (1975), and in recent review by Manson and Old- mancy after spring migration of hibernated nymphs field (1996). Nevertheless, it is worth to illustrate is characteristic of vagrant form also. Its complex the eriophyoid life-cycle diversity by some addi- life cycle is characterized by two versions (with tional examples. two and three nymphal stages, the third of which The typical complex life cycles (with repro- is heteromorphic Tegonotus-like nymph), that is ductive summer protogynes and hibernating dor- unknown in any eriophyid mites. Hibernating in- mant deutogynes) are characteristic of some dip- stars are presented here by Tegonotus-like nymphs tilomiopid vagrant mites Rhincaphytoptus and and adult mites with their spring migration from Vasates from different deciduous Acer trees (Oz- old big buds onto open places for summer poly- man 2001) and Calepitrimerus vitis from vine- voltine development (vegetative and generative yards (Pérez-Moreno and Moraza-Zorrillab parts of the plant, and new small buds also). Poly- 1998.). More complicated cycles with 2-year du- voltine development ends in September with ac- ration and hibernation of some (or all) ontoge- cumulation of Tegonotus-like nymphs, migrating netic instars are peculiar for mites of the genus together with adults to winter places (as in sum- Trisetacus, inhabitants of galls and buds in conif- mer to new places for feeding). erous trees. The biennial development of T. kir­ Unfortunately, the presented data on life his- ghisorum in “berries” of Juniperus semiglobosus tories of Eriophyoidea give few materials for de- is characterized by the every-year change of sum- termination of definite kinds of dormancy in them. mer and winter generations with hibernation of Nevertheless, it is quite probable, that the control both deutogyne and protogyne females, as well of seasonal life cycles in most four-legged mites is as of eggs (Shevchenko and De-Millo 1968), enabled by hibernating and aestivating diapauses while the development of T. piceae in host buds in adult females (as a rule by deutogynes, although occurs with annual change of generations with sometimes by protogynes), in nymphs and in eggs. protogyne adults and deutogyne adults, which The hibernation and aestivation in the state of qui- are capable to hibernate together with eggs and escence may be quite possible (particularly in immature instars also (Bagnjuk 1976). From my grass-inhabiting mites), but needs special ecophys- meaning, plesiotypic life-history traits of gall- iological investigations. Such investigations are of producing coniferous eriophyoid mites (Triseta­ great importance also for clearing the presence of cus) revealed in the presence of numerous dor- post-diapause quiescence in processes of develop- mant stages, that enable hibernation and seasonal mental arrest termination, known in many acari- control of biennial life cycles, coincide quite well form mites. There is a great field yet for thorough with their archaic plesiomorphic traits. In con- study of seasonal cycles and their control mecha- trast, arboreal vagrant mites (Aculus, Epitrimer­ nisms in eriophyoid mites. us, Nalepella etc.) with rapid polyvoltine devel- The more specialized traits concerning the opment and limited number of dormant stages morphology, ontogeny and life history are charac- (adult deutogyne females or overwintering eggs) teristic of the suborder Heterostigmata with its

110 Dormancy and their significance in life cycles of mites and ticks numerous representatives demonstrating the trends tiple generations may develop in each bee in win- to parasitism and reduction (Kethley 1982). Ac- ter. The function of dormancy is unknown, and cording to Wainstein (1978), this taxon (consid- distant dispersal is absent in these mites. As adult ered by him as the cohort Tarsonemina) displays females they move outside the host only for a short the strongly limited group, differing from other time to infest other bees, usually young workers. trombidiform mites, and comprising subgroups of Some other examples of Heterostigmata are big similarity. Heterostigs, as they were called by given in Table 5. The dormant stages are known Kethley (1982), comprise 5 superfamilies, two of mainly in pygmephoroid mites associated with in- which (Tarsocheyloidea and Heterocheyloidea) sects through phoresy and parasitism. For instance, include the derived and slow studied mites with the fungivorous oligophagous mite Brennandania three immature stages (La, PN and DN), while lambi, an important polyvoltine pest in mushroom three others (Pygmephoroidea, Pyemotoidea and farms, has its dispersal by phoretic adult females Tarsonemoidea) represent more specialized taxa on sciarid and phorid flies. The related fungivo- that demonstrate apotypic traits of increasing mor- rous mites, Pediculaster flechtmanni and P. me­ phological and ontogenetic reduction (their life sem­brinae, feeding on wild moulds, have two cycles may be condensed to a larval stage or even forms of adult females for dispersal (phoretic and to its loss, when adults give birth directly to adults), non-phoretic). Adult females serve as non-phoret- combined with close phoretic or parasitic associa- ic dispersing agents in different pyemotid mites, tions with insects. The developmental rate is very parasitic on stored-product insect pests (Pyemotes high and may overcome even that of astigmatid tritici, P. ventricosus) and on midges producing mites. leaf galls (Pyemotes herfsi). Phoretic females of Pygmephoroidea comprise 3 families, two if fungiphorous scutacarid mite, Scutacarus acaro­ which — Pygmephoridae (300 nominated species) rum, serve as dormant overwintering phoretics on and Scutacaridae (400 nominated species) — have hibernating bumblbee females. There is a real diverse associations with insects, mammals, their similarity in life-history traits of some heterostig- nests and litter. The females, often physogastric, matid and astigmatid mites, especially associated are either oviparous or larviparous. Life cycles are with insects as phoretics and parasites/paraphags. with no nymphal stage. Pyemotoidea consists of 4 Diapausing state of phoretic stages in heterostig- families, three of which are associated with bee- matid mites is quite similar, probably, to such tles, while the representatives of Pyemotidae are states in hypopodes of astigmatid mites. predators or parasitoids of immature instars in very different insects. The life cycles of pyemotids DISCUSSION AND CONCLUSION are highly modified. For instance, all development General distribution of diapause and of Pyemotes tritici takes place within a gravid quiescence in acariform mites physogastric female with approximately 200 prog- The main seasonal peculiarities of life cycles eny, and males (sons) just after birth mate with in the Acari, as already noted, depend on the func- their sisters. Life cycle lasts 4–7 days at 25oC. tion of special, species-specific System of Season- Representatives of Pygmephoroidea and Pyemo- al Control (SSC), which affects the duration, volt- toidea due to their morphological similarity and inism, phenology, flexibility and other life-cycle low level of taxonomic study sometimes refer to traits. The organizing role in these systems is en- the combined group (e.g. to Pygmephoroidea in abled by dormant stages of diapausing character Table 5). The last superfamily Tarsonemoidea (Belozerov 2006, 2007, 2008b). The number and (with two families) has no nymphal stages in life distribution of such stages are determined by evo- cycles also. The family Podapolipidae is repre- lutionary transformation of the named systems — sented by parasites of insects and other arthropods, from ancestral polymeric SSC (with numerous while Tarsonemidae are extremely diverse in their diapausing stages) into oligomeric and monomeric food relations (fungi-, herbi- and entomophagous SSC (with reduced number of these stages). The mites, symbionts and parasites of insects). One of presence of another kind of dormancy in acariform the most important pests among tarsonemoid mites mites (quiescence) is apparent, but its participa- is the honey bee tracheal mite, Acarapis woodi, a tion in these control systems would seem improb- cosmopolitan endoparasite of Apis mellifera. able according to the common belief of insect There is possible only one generation of this para- ecologists, but the presented data suggest an op- site per host in short-lived summer bees, but mul- posite opinion.

111 V. N. Belozerov

From materials presented above, survival dur- in the state of diapause under conditions of tem- ing unfavorable conditions is doubtless enabled in perate seasonality (Table 1). In contrast to the acariform mites by both kinds of dormancy, con- cold-dependent hibernating dormancy, the nature trolled either endogenously, (diapause), exoge- of which in oribatid mites is still unclear, the pres- nously (quiescence), or in both ways. However, ence of typical drought-dependent quiescence in such opposite kinds of dormancy in these mites these mites is quite definite, being discovered in are hardly similar functionally as adaptations for case of summer rest (with temporary comatose time-adjustment of their life cycles to predictable state) in the European species Scutovertex minutus environmental changes. While the real necessity (Smrž 2002), and in one ameronothrid mite in the for quiescence occurs under conditions of non- western USA from ephemeral pools after their predictability, it is rather ambiguous for diapause drying (Norton et al. 1996). A similar form of qui- in the same situation. Diapause in mites is of deci- escence as a response to humidity deficit is known sive importance for life-cycle synchronization also in some erythraeid mites (Prostigmata: Para- with environmental seasonality (as in most other sitengona:) with eggs and calyptostasic instars arthropods), but the same role of quiescence needs (PLa and PN), capable to survive the drought dur- special comparative analytical consideration. All ing a month-long period in the state of dryness- available data concerning quiescence and diapause dependent quiescence (Wohltmann 1998). The in acariform mites, considered in this review, are quiescent state in response to humidity deficit presented for this purpose in Tables 1–5 and sum- presents a case of special interest for solving the marized in Table 6. origin and evolutionary trends in dormancy and Among Oribatida, according to general opin- life-history strategies of terrestrial arthropods ion (Norton 1994), all soil-dwelling oribatid mites (Emme 1953; Ushatinskaya 1973, 1990; Jönsson from temperate climate conditions (with uni-semi- 2005; etc.). This can be ascertained through study voltine life cycles and other “K”-attributes of life- of their dormant states, and through comparison history strategies) are quiescent during hibernation. with similar forms of latent life, particularly anhy- The same idea about the ability of temperate orib- drobiosis. Of great necessity in the same regard is atid mites to overwinter in the state of quiescence to learn and understand the real (but still unclear) (similarly with Collembola and other soil-dwelling nature of winter dormancy in temperate- and po- microarthropods) was expressed by Siepel (1994). lar-climate oribatid mites due to their general ple- Quiescence is assigned also as the only dormant siotypic traits. It is necessary to add to the Nor- state for hibernation (with no traits of diapause) in ton’s (1994) note about “full set of conservative those oribatid species that live under conditions of plesiotypic traits concerning their life history”, extreme polar seasonality and possess perennial that the Oribatida are characterized by positive life cycles and “A”-attributes of life-history (Con- conformance of plesiotypic characters in both bio- vey 1996; Søvik 2004), as well as many polar in- logical (life history) and ontogenetic aspects. sects (Danks 1999a, 2004; Peck et al. 2006). But Among free-living Astigmata (Acaridia) dia- this is not the only conclusion for polar oribatid pause, combined usually with phoresy, is a domi- mites, since before hibernation they exhibit some nant form of dormancy for survival during tempo- diapausing traits (see above: p. 86–87). Their life rary periods between colonizations of their histories look and are considered as extreme ver- ephemeral habitats, as well as during adverse sea- sions of the typical ancestral oribatid life history sons. It relates usually to the deutonymphal heter- that has been preadapted to Arctic and Antarctic omorphic instar (hypopus) with adaptations for conditions without special polar adaptations (Nor- phoretic or non-phoretic dispersal (but in some ton 1994; Convey 1996; Behan-Pelletier 1999). cases to the non-phoretic tritonymphal instar). In Unfortunately, the problem of identifying real na- contrast, Psoroptidia, as permanent parasites of ture of dormancy (quiescence, diapause or their vertebrate animals, are deprived usually of dor- combination) in typical versions of oribatid life mant stages due to dominance of close host-para- histories has no definite solution (due to the lack site relationships, especially in mammalian para- of sufficient information for temperate soil-dwell- sites, while feather mites, as more plesiotypic ing mites, as well as to some doubts and contradic- parasites of birds, may retain sometimes the capa- tions). However, according to Reeves (1969) and bility for dormancy (rather as quiescence, though some other acarologists, almost all oribatid spe- in literature suggested as diapause). The number cies with “K”- and “r”-attributes seem to hibernate of dormant stages that participate as regulators of

112 Dormancy and their significance in life cycles of mites and ticks

Table 6. Summary of data on dormant stages and their types in different groups of the acariform mites. Number of Types of dormancy Voltinism or hostal Number of Taxons dormant specifity species Quiescence Diapause Unknown stages 1 2 3 4 5 6 7 Oribatida perennial 4–6 4 3 (all stages) 0 1 Oribatida semivoltine 3–5 12 1 (all stages) 6 (alm. all stages) 5 uni/bivoltine 1–3 6 1 (TN, Ad) 5 (DN, TN+AD) 0 Astigmata multivoltine 1 or 2 16 1 TN 12 DN + 1 TN 2 Acaridia uni-bivoltine 1 or 2 8 1 (TN+Ad) 6 DN + 1 TN 0 on mammals no 4 – – – Psoroptidia on birds 1–3 7 1 (?) 4 (?) 2 dust mites ? 5 5 0 0 Prostigmata Eupodina Eupodoidea multi/univoltine 1 4 mv, 1 uv 0 5 aestiv. Eggs 0 Bdelloidea univoltine 1 1 0 1 aestiv. Eggs 0 Tydeoidea multivoltine 1 1 0 1 hibern. Ad female 0 univoltine 2 6 6 Ad 6 DN 0 Halacaroidea bivoltine 6 3 3 all stages 0 ? 0 Parasitengona Erythraeina univoltine 1–2 (usual 1) 16 Ad, Eg, PN 3Ad, 7Eg, 4PN, 0 2DN Trombidiina uni/semivoltine 1–5 (usual 2) 39 Ad, Eg, La, N. 19Ad, 13Eg, 6La, 0 1N Hydracarina uni/semivoltine 1–3 (usual 1) 15 La, DN, TN 4Ad, 6Eg, 3La, 2Nm 0 Anystina Anystidae multivoltine 1 1 0 hibern. Eggs 0 Eleutherengona Raphignathoidea multivoltine 1 1 0 1 hibern. Ad female 0 Tetranychoidea 10 Ad female and 7 multivoltine 1 17 0 * Eggs 0–4 (usual N2, N2+Ad, gall/bud mites 11 0 0 l–2) Eg+NN+Ad+Deut arboreal vagrants 1–4 (usual 1) 8 0 Eggs, N3, Deutog. 0 Eriophyoidea Protogynes or grass inhabitants 1 or 4 2 Eg+N1+ N2+ ? 0 Protog. Heterostigmata Mycetophags etc. ? 3 ? ? 3

Tarsonemoidea Ad, Ad Insect associates female, La 6 ? ? 6 female Mycetophags etc. Ad female 5 – 3 Ad female 2 Pygmephoroidea Insect associates Ad female 4 – 1 Ad female 3 Note: Data were compiled from Tables 1–5 of this paper and Tables 1–2 of the paper on the calyptostasy in Parasitengona (Belozerov 2008a). An asterisk in the last column opposite to Tetranychoidea means the presence of some exclusions in regard to their dormant stages (see text). Numerals in columns 5, 6 and 7 mean the number of mite species with corresponding traits. Numerals in the column 3 mean the number of dormant stages in life cycles of investigated mite species. The compilation presents very approximate results on relationships, but more definite results on distribution of dormancy types in different taxa of the acariform mites.

113 V. N. Belozerov life cycles in the acaridian mites is limited usually more apotypic traits of their life histories, than in to the single diapausing instar (deutonymphal hy- other Parasitengona (see Wohltmann 2001). At popus) characterized by special morphological ad- last, Eleutherengona comprise taxa with very dif- aptations due to phoresy and aphagy. Quite possi- ferent relationships between their traits, concern- ble, that post-diapause quiescence ascertained in ing the life-cycle seasonality and morphology/on- hypopodes of Lepdoglyphus destructor (Knülle togeny. If the four-legged mites (Eriophyoidea) 1991b; Danks 1994, 1999) may be the common reveal plesiotypic and variable systems of season- dormant adaptation in the acaridian mites for syn- al control (including both diapause and quiescent chronous moult of their DN to TN. The acarid stages) in contrary to apotypic morphological and mite Naiadacarus arboricola presents a unique ontogenetic reduction, the relationships between case of life cycles with the TN for winter diapause these trends in true spider mites (Tetranychoidea: (followed by post-diapause quiescence), phoretic Tetranychidae) is perfectly opposite (the apotypic DN for summer dispersal and other instars, prob- uniformity of regulatory systems presented by ei- ably, for winter quiescence. The number of resting ther embryonic, or reproductive diapause, and stages (of indefinite nature) in feather mites may quite plesiotypic traits in morphology and ontog- be one to three. The Astigmata, as well as Orib- eny), while in false spider mites (Tetranychoidea: atida, are characterized by the conformance of bi- Tenuipalpidae) both trends coincide as apotypic ological and ontogenetic traits, though in contrast (the single dormant stage of diapausing adult fe- to Oribatida (due to derivative position and spe- males and obvious traits of deep morphological cialization of astigmatid mites) they reveal apo- reduction). In this regard they are quite compara- typic trends in both aspects (biological and onto- ble with astigmatic Acaridia (especially in regard genetic). Some peculiarities and properties of to the single dormant stage, presented by diapaus- diapause in acaridian hypopodes are rather inge- ing adult female in tenuipalpid mites and by dia- nious and want special separate investigations in pausing deutonymphal hypopus in almost all free- spite of great insight into the general life history of living acaridian mites). The mentioned differences these mites (Athias-Binche 1991; Houck and between biological and morpho-ontogenetic trends OConnor 1991; Houck 1994). in taxa of Eleutherengona support the meaning of Quite a different picture is characteristic of entomologists (Danilevsky 1961; Ushatynskaya the complex taxon Prostigmata with its biologi- 1976; Tyshchenko 1983; etc.), that evolution of cal, ontogenetic and morphological diversity. The seasonal adaptations in insects does not corre- main life-history peculiarity, deserved special spond their phylogenetic evolution, though phy- consideration in this taxon, concerns the combina- logeny may influence on biological features tion of diapause and quiescence in life cycles of its through the life style, which is peculiar for taxo- representatives either at different instars, or at the nomic groups. This corresponds also to a state- same ontogenetic instar (this is unknown in ple- ment that location of diapause at definite ontoge- siotypic Oribatida and practically absent in apo- netic instar depends mainly on the ecology of typic Astigmata). For instance, in terrestrial Eupo- species and has slow connections with its taxo- dina the combination of diapause and post-diapause nomic position (Danilevsky 1961), that is well il- quiescence occurs at the same instar (eggs in pen- lustrated by various species-specific position of thaleid and bdellid mites, or adult females in ty- diapause in Erythraeina mites (see above). These deid mites), but in marine halacarid mites this con- data quite agree with my opinion that evolutionary trol includes deutonymphal diapause with events of seasonal adaptations have occurred in post-diapause quiescence, followed by common different animal taxa according to and depending cold-enforced quiescence in adult females. The on their organization, manner of life, geographic combination of diapause and quiescence at differ- distribution and historic changes in conditions of ent stages of life cycle is characteristic of most their existence (Belozerov 2006, 2007, 2008b). Parasitengona (terrestrial Trombidiina and fresh- At last, among Heterostigmata with their ex- water Hydracarina with uni-semivoltine develop- treme ontogenetic and morphological reduction ment), though representatives of Erythraeina dif- (as well as with r-selected attributes), some many fer from them usually by a single dormant stage of representatives of tarsonemoid and pygmophoroid diapausing character (at different species-specific mites reveal associations with insects as their pho- instars), that give evidences (together with rigid retics, parasites and parasitoids, sometimes with univoltinity of these rather xerophylic mites) for synchronized appearance and hibernation of both

114 Dormancy and their significance in life cycles of mites and ticks associates. The last trait favours for diapausing developmental thresholds. The main significance nature of their dormant and phoretic stages. Some and peculiarity of this special quiescence is pre- heterostigmatids (e.g. Scutacarus acarorum, hi- sented by its capability not only to provide higher bernating on bumblebee females), reveal the obvi- tolerance, but also to synchronize life cycles and, ous probability of combination of diapause and thus, to replace diapause as a means of seasonal post-diapause quiescence. All known cases of dis- synchrony. This is a very interesting result based persal through phoresy relate to adult females in also on mathematical modeling that is consistent heterostigmatid mites (usually due to extreme re- with empirical data of some entomologists. Nev- duction and condensation of their life cycles). ertheless the stage-specific quiescence still re- Many parasitic representatives of this taxon are quires thorough evaluations through special bio- deprived of dormant stages (e.g. the endoparasitic logical (hopefully also acarological) investigations, tracheal bee mite Acarapis woodi, enabling infes- because the authors themselves consider their re- tation of hosts by its adult females, which are not sults as abstractions, hoping that “their analysis capable for long off-host survival). In spite of low encourages further empirical documentation of knowledge of life histories in heterostigmatid these patterns”. mites, it is possible, nevertheless, to see their es- The most important perspective on the prob- sential convergent similarity in some regards with lem of quiescence and its relations to diapause is free-living astigmatid mites, especially associated represented, undoubtedly, by the third type of qui- also with insects through phoresy and parasitism. escent dormancy, ascertained by Czech entomolo- gists (Hodek 1996, 2002; Koštal 2006)* as “the The diversity of quiescence types and their functions in life cycles of acariform mites post-diapause quiescence” after their comprehen- sive analysis of successive physiological stages of According to the common meaning, the main diapause in insects. This form of quiescence, rep- (if not the unique) function of quiescence in ar- resenting the terminal phase of diapause develop- thropods concerns their survival during adverse ment (Fig. 3), ensures both vital functions attribut- environmental conditions, due to high general and able for diapause (survival and synchronization), specific tolerance obtained in this state, while qui- though not through replacing diapause (as in pre- escent stages are hardly capable to be of use for vious case of the stage-specific quiescence), but the seasonal control of life cycles. However, such by means of diapause supplementation for an in- an opinion concerns only the most common type crease of accuracy in seasonal synchronization of of quiescence, that arises as a direct response to life cycles. This is enabled firstly through the en- adverse environmental conditions at any life-cycle forced maintenance of post-diapause dormant stage and ceases just after elimination of unfavor- state under adverse conditions (together with the able factors. covert developmental potentiality received at the This opinion, accepted by almost all ecolo- end of diapause), and then by realization of this gists, has obtained theoretical support from a potentiality through resumption of overt develop- group of entomologists and mathematicians from ment after adequate environmental changes. Ac- USA (Gurney et al. 1991). They showed by means cording to Koštal (2006), the potentiality for de- of mathematical modeling that this form of en- velopment may be realized either immediately forced dormancy, received from these authors the after the end of diapause, if the conditions are per- term “the stage-independent quiescence”, acting missive, or after some delay in the state of quies- alone (with no diapause) and independent of any cence until favorable environmental changes. developmental stage, can never synchronize insect Some cases with traits of the post-diapause life cycles to the seasons. Undoubtedly, this is quiescence were demonstrated before and after the characteristic of the acariform mites also. Thus, mentioned publications of Hodek and Koštal by the theoretical analysis has confirmed the common meaning about the enforced quiescent dormancy *The first entomological data on diapause followed by quies- ascertained by biologists in field and laboratory. cence in accordance to traits of post-diapause quiescence The same authors revealed later (Gurney et al. were obtained by Hodek (1971, 1973) in Pyrrhocoris apterus 1994) another modified type of quiescent dorman- and in coccinellid beetles, as well as by Krysan (1978) in Diabrotica virgifera. The first case of the same type in Ac- cy, called by them as “the stage-specific quies- arology with aestivatng egg diapause followed by quiescence cence” due to its functional connection with some was described for the spider mite Petrobia apicalis by Zein- ontogenetic stage, differing from other stages by Eldin (1956).

115 V. N. Belozerov

Fig. 3. Schematic depiction of phases in diapause development during ontogenesis of one hypothetical insect individual. The points on the line delineate major ontogenetic stages. Three major phases, namely pre-diapause, diapause and post-diapause, are distinguished during the diapause including ontogeny. Further division to sub-phases, namely induction, preparation, ini- tiation, maintenance, termination and quiescence, is indicated by vertical lines Changes in diapause intensity are schematically presented: dotted branches (a and b) apply to the constant conditions, while solid branch (c) applies to the change of environ- mental conditions (specific terminating conditions/stimuli coming at different physiological times-movable carriage) (after Koštal 2006). entomologists and zoologists of other specialties. embryonic development) in autumn by decreasing For instance, this type of quiescence was shown temperature and increasing humidity. Similar rela- also in Crustaceans, particularly in some branchio- tionships with temperature and moisture in mainte- pods, where the larval hatch from reactivated cysts nance and termination of developmental arrest dur- may occur either just after diapause termination, ing and after aestivating diapause were recorded or after temporary delay in the state of post-dia- also in eggs of the predaceous eupodine mite Bdel­ pause quiescence affected by external conditions lodes lapidaria from Australia (Wallace 1971), and (Brendonck 1996), as well as the larval hatch in in especially well investigated Australian plant insects and mites from reactivated eggs. pests, phytophagous eupodine mites, Halotydeus Essential data on this peculiar form of dor- destructor and some cryptic species of Penthaleus mancy were obtained at the same time and even (Prostigmata: Eupodina) with aestivating diapause earlier by acarologists working on phenology and of egg also (Wallace 1970a,b; Ridsdill-Smith 1997; seasonal adaptations (particularly on diapause) of Umina et al. 2003, 2004; etc.). Something similar is different acariform mites. A. Veerman (1985) from revealed in marine halacarid mites with summer- the Amsterdam University was perhaps the first autumn deutonymphal diapause followed by post- who emphasized the great adaptive significance of diapause quiescence (Metarhombognathus armatus the post-diapause quiescence for “fine” time-ad- etc.), as well as in TN of the water acarid mite Na­ justment (as a supplement for “coarse” diapausing iadacarus arboricola, and in adult females of pred- adjustment) of hatch in overwintered eggs of spi- atory stigmaeid mite Zetzellia mali (Eleutherengo- der mite Panonychus ulmi, though initially the na: Raphignathoidea) with winter diapause and traits of this quiescence in spider mites were dis- cold-dependent quiescence in both latter cases. The covered in aestivating eggs of Petrobia apicalis by described mechanisms with participation of post- Zein-Eldin (1956), and confirmed later forP. harti diapause quiescence enable the accurate synchro- by Koveos and Tzanakakis (1991). The mainte- nizing effect in seasonal adjustment of life cycles in nance of developmental arrest in aestivating eggs mentioned mites with aestivating diapause. (together with retaining the developmental potenti- The role of post-diapause quiescence as a syn- ality after the end of diapause) is enabled by sum- chronizing agent, being quite appreciable in spe- mer conditions (high temperature and relatively cies with aestivating diapause, is less obvious and dry atmosphere), but is broken (with restoring the received less attention (as self-evident event) in

116 Dormancy and their significance in life cycles of mites and ticks cases of hibernating diapause, as far as the resting The origin and evolution of dormancy in state is maintained and terminated here mainly by arthropods temperatures (with its reactivating chilling effect There are many hypotheses about both the and recovering effect of increase of temperature). origin and evolution of dormancy in living beings It is quite usual for insects and mites that de- on our planet, but the problem remains unresolved. velopmental potentiality in overwintering speci- It is frequently proposed that quiescence, as the mens (i.e. their cold-reactivation according to Da- simplest form of dormancy, represents the starting nilevsky 1961) is achieved long before the end of point for the evolution of diapause. One of the first cold weather (see Hodek 2002), and the dormant proponents of this view, as noted by Tauber et al. state retains rather long time until the start of warm (1986), was Emme (1953), who suggested that weather, enforcing the synchronized renewal of diapause has arisen from quiescence (firstly tem- development. In acariform mites this is character- porary, but then evolved to long-termed and cold- istic of many spider mites, overwintering both as resistant arrest) due to moisture deficit. The close adult females (Tetranychus urticae, T. kanzawai suggestion was given by Ushatinskaya (1976) that etc.) and eggs (Panonychus ulmi, Bryobia rubrio­ diapause evolved not from torpidity, but from culus, Oligonychus ununguis etc.), of some erio- “sleep” with its basic inherent preconditions. It is phyid mites with winter egg diapause (Nalepella necessary, of course, to remember H.J. Müller haarlovi etc.), and of many parasitengone mites (1992), who considered quiescence as an initial with hibernal diapause at egg stage (Johnstoniana pra-form of all forms of dormancy. Numerous op- rapax, J. tuberculata, Campylothrombium bore­ ponents of these views suggest that the origin of ale, Georgia pulcherima and Balaustium put­ diapause resides in responses other than those in- mani), at adult stage (Camerotrombidium rasum), as deutonymphs (Leptus beroni) and even as ca- volved in quiescence. For instance, Tyshchenko lyptostasic protonymphs (Leptus fernandezi) (see (1973, 1983) and Tauber et al. (1987) proposed Eggers 1995; Wohtmann 2001; Belozerov 2008a). comprehensive hypotheses of diapause evolution The same mechanism is quite probable in the in connection with the evolution of photopeiodism astigmatid mite Naiadacarus arboricola, diapaus- and the perception of seasonal token stimuli. ing in winter at resistant tritonymphal stage (Fash- In regards to the origin of diapause per se, its ing 1977). Mechanisms of adequate character as- capability is considered by some authors as a pri- sociated with post-diapause quiescence are quite mary feature, inherited by arthropods from their possible in most terrestrial acaridian mites. ancestors. According to Alekseev and Staroboga- Thus, the post-diapause quiescence, ascer- tov (1996), diapause has originated only once in tained in insects, is an important device for “fine” the animal kingdom and in any new case has “de- seasonal synchronization of life cycles in repre- pendent, evolutionary transferred origin” based on sentatives of acariform mites, irrespective of dia- original reactions of ancestors (i.e. monophyleti- pause type (aestival or hibernal) and its ontoge- cally). Similar opinions about diapause origin are netic location (egg, immatures or adult stage). characteristic of entomologists C. and M. Tauber Unfortunately, it is impossible yet to clarify the and S. Masaki, who consider each new diapause definite relationships of diapause with post-dia- acquired in the course of insect evolution as a pause quiescence. It is not unlikely, however, that modification of an ancestral diapausing response, the post-diapause quiescence, being displayed at inherent for their ancestors (Tauber et al. 1986, p. the end of diapause only (i.e. after reactivation), 219). In contrast, other authors favor the hypothe- may arise much earlier, at the beginning of dia- sis of polyphyletic origin of diapause (Danilevsky pause (on phases of its initiation or maintenance 1961; Cáceres 1997; etc.), in correspondence with — see Fig. 3), joining their common tolerant capa- the idea of great lability of evolutionary processes bilities. There are many important and interesting concerning diapause and “phenological strate- questions for further investigations of properties, gies”. This idea is very resistant in entomological ecophysiological and evolutionary relationships literature (Kozhanchikov 1959; Alexander 1968; of quiescence, diapause and active state, proposed Masaki 1978; etc.) and admits de novo formation by the remarkable Russian ecologist and evolu- of diapause even in specialized taxa. According to tionist, A.M. Emme (1953) more than half a cen- Cáceres (1997, p. 371), “dormancy has most likely tury ago, which still need comparative study. A arisen multiple times in invertebrate life histories, discussion of one of these follows. both within and between phyla”.

117 V. N. Belozerov

The opinion, that capability for dormancy in population survival in the state of quiescence dur- arthropods was received from their ancient remote ing such a season. ancestors, and its further evolution occurred on This phenomenon, with the association of two the basis of their ancestral responses and proper- different adaptive responses, gives a reasonable ties (with possibility to display their retention basis for the solution of both general and particu- someway later also) seems more correct. My anal- lar problems concerning the origin and evolution ysis of the distribution of dormant stages in life of dormancy in arthropods (e.g. for Oribatida as cycles of Insects, Crustaceans and Acari (Beloze- an important taxon among acariform mites with rov 2006, 2007) suggests that adaptations enabling uncertain nature of their seasonal dormancy and the seasonal alternation of active and dormant pe- its contradictory interpretation). The combination riods in life cycles of arthropods arisen at the earli- of post-diapause quiescence and diapause may be est occurrence of life and developed afterwards in considered as an initial ancestral state of dorman- different animal taxa according to their organiza- cy enabling universal adaptation in the acariform tion, manner of life, geographic distribution and mites to any environmental changes. This opinion historic changes in ecological conditions of their allows a reasonable suggestion for the presence of existence. This is well supported by the above re- the double nature of dormancy in ancestral Orib- corded examples with differences either in corre- atida and the same explanation for retention of this spondence, or in inconsistency of ecophysiologi- feature in extant oribatid mites (in contrast to con- cal and morpho-ontogenetic evolutionary trends tradictory interpretations of their winter dormancy among different lineages of Eleutherengona and as a result of either quiescence, or diapause only). other prostigmatid mites (pp. 100, 109, 112, 114), The hibernal dormancy in extant oribatid mites, in which evidences the non-conformity of phyloge- my view, begins from the state of induced diapause netic and ecophysiological evolution in insects and ends with the state of enforced post-diapause (Danilevsky 1961; Ushatynskaya 1976; Tysh- quiescence followed by events of direct develop- chenko 1983), in spite of some influence of phy- ment. The ascertainment of such double mecha- logeny on biological features through the life man- nisms in hibernating oribatid mites from different ner, that is peculiar for taxonomic groups. habitats and taxonomic groups will give the real Now, on the basis of materials presented confirmation of the idea of ancestral nature of their above (especially in the previous part of the Dis- initial double dormancy. This helps also to under- cussion, emphasizing the role of post-diapausing stand the evolutionary pathways of life-cycle con- quiescence), it is possible to give more reasonable trol in acariform mites from the initial combination suggestions, itemizing the initial state of dorman- of diapause and post-diapause quiescence, with cy in ancestors of acarines and other arthropods as further changes of their control into three main a complex adaptation to both predictable and un- functional directions: (1) either being retained in predictable environmental changes. their descendants as a double controlling mecha- The tight-connected association of diapause nism of plesiotypic character with both types of and quiescence (namely of the post-diapause type) dormancy; (2) or being modified into one of the is characteristic, as we have seen, of many extant specialized mechanisms of apotypic character with species of insects, mites and some other inverte- diapausing or quiescent response; (3) or being brates. The diapause in penthaleid and tetranychid transformed into active stage with no capability for mites considered earlier as the single dormant dormancy (this is well corresponds to general evo- stage controlling their seasonal life cycles, repre- lutionary transformations of life cycles and their sents really a complex involving a diapause and controlling systems in all Acari — Belozerov 2007, post-diapause quiescence (as was ascertained in 2008b). All these hypothetical versions seem prob- investigations of diapause termination). Thus, the able, but need, of course, serious theoretical evalu- seasonal synchronization of life cycle in these ation through the study of ecologically and taxo- prostigmatid mites is ensured by a combination of nomically different acariform mites. both kinds of dormancy — by real diapause and by post-diapause quiescence. An advantage of this Conclusion: some results and tasks for further study of dormancy in acariform mites. association has two essential aspects. It ensures not only accurate time-adjustment of both arrest The analysis of data on dormant stages in and resumption of development (before and after three main taxa of acariform mites (Oribatida, an inappropriate season respectively), but also Astigmata and Prostigmata) has confirmed the

118 Dormancy and their significance in life cycles of mites and ticks main conclusions made in my previous papers cerning the peculiarities of dormancy in free-liv- (Belozerov 2006, 2007, 2008b) concerning regu- ing Astigmata, some properties of diapause in larities in evolution of systems controlling the sea- which are not clear enough. There is a serious in- sonality of acarine life cycles from a plesiotypic consistency of diapausing traits of deutonymphal state (with numerous diapausing stages) to apo- hypopodes in these mites with the common unpre- typic states (with single or limited number of such dictability of their ephemeral habitats. The best stages). These conclusions are supplemented now way to address both these issues may be further by the statement that seasonality control of life experimental study of dormancy termination in cycles is enabled not only by diapause, but also by resting stages of acaridian hypopodes and over- some forms of quiescence, particularly by the wintering dormancy in oribatid mites, i.e. by post-diapause quiescence ascertained by entomol- means of the same efficient procedures which ogists (Hodek 1996; Koštal 2006), and empha- helped to ascertain the post-diapause quiescence sized by an acarologist Veerman (1985). The most in prostigmatid mites. important conclusion is that the combination of ACKNOWLEDGEMENT diapause and post-diapause quiescence, character- istic of many extant acariform mites, corresponds The study was performed under financial sup- the ancestral initial state of dormancy in adapta- port of RFBR (project 07-04-00361), of Federal tions (particularly of Oribatida) to any environ- program for supporting the Leading Scientific mental changes. Schools (project НШ-7130.2006.4) and of the The ascertainment of the cooperating combi- Charity foundation “Inessa”. The author is frankly nation of diapause and post-diapause quiescence grateful to everybody for the attention to my work reveals a facility of great ecophysiological signifi- and especially to Prof. R.A. Norton (USA) for his cance in insects, acarines and other arthropods, comments, remarks and advises for improving the which obtained with its help the efficient capability paper. for adaptations to predictable and unpredictable REFERENCES environmental changes, for adaptations to long- Akimov, I.A. and Gorgol, V.T. 1990. Khishchnye i termed climatic changes, and for preadaptations to parasiticheskie kleshchi-cheyletidy [Predaceous more adverse and extreme conditions. Investiga- and parasitic cheyletid mites]. Naukova Dumka tions of this quiescence, tightly connected with di- Publ., Kiev, 120 pp. [In Russian] apause, give real basis for better understanding the Alberti, G. 1975. Praelarven und Phylogenie der Schna- evolutionary pathways of dormancy in arthropods belmilben (Bdellidae,Trombidiformes). Zeitschrift (in general), as well as for understanding the initial für Zoologie, Systematik und Evolutionsforschung, and real nature of dormancy in the Acari, and espe- 13: 44–62. cially the Oribatida in particular. Alekseev, V.R. 1990. Diapauza rakoobraznykh. Ekofi- Dormancy in ancestral Oribatida was proba- siologicheskie aspekty. [Diapause in Crustaceans. Ecophysiological aspects]. Nauka Publ., Moscow. bly represented, as it is now in many extant pros- 144 pp. [in Russian] tigmatid mites (Eupodina, Eleutherengona etc.), Alekseev, V.R. and Starobogatov, Ya.I. 1996. Types of neither by the single quiescence, nor by the single diapause in the Crustacea: definitions, distribu- diapause, but was based on cooperating combina- tion, evolution. Hydrobiologia, 320: 15–26. tion of both kinds of dormancy, giving real advan- Alekseev, V.R., Ravera, O., and De Stasio, B.T. 2007. tages for coordinated survival of populations and Introduction to diapause. In: V.R. Alekseev et al. their seasonal developmental synchrony under (Eds.). Diapause in aquatic Invertebrates: Theory different climatic conditions. The solution of prob- and Human Use. Springer Verlag, pp.3–10. lems, arisen from conclusions of the presented Alexander, R.D. 1968. Life cycle origins, speciation analytical review on acariform mites, needs fur- and related phenomena in crickets. Quarterly Re­ view of Biology, 43: 1–41. ther investigations of different forms of quies- Amrine, J. and Stasny, T.A. 1994. Catalog of the Erio- cence, their properties and relationships with dia- phyoidea (Acarina, Prostigmata) of the World. In- pause, i.e. of the same problems that were proposed dira Publishing House, West Bloomfield, Michi- by A.M. Emme (1953). gan, 798 pp. Besides the question on the nature of dorman- André, H.M. and Fain, A. 1991. Ontogeny in the cy in Oribatida, which is extremely important for Tydeoidea (Ereynetidae, Tydeidae and Iolinidae. the problem of dormancy evolution in acariform In: F. Dusbabek and V. Bukva (Eds). Modern Ac- mites, there is another controversial question con- arology. Academia, Prague. Vol.2, pp. 297–230.

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