Typhloseiulus simplex (Chant)

Tixier, Marie-Stéphane, Baldassar, Andrea, Duso, Carlo & Kreiter, Serge, 2013, Phytoseiidae in European grape (Vitis vinifera L.): bio-ecological aspects and keys to species (Acari: Mesostigmata), Zootaxa 3721 (2), pp. 101-142 : 122-134

Typhloseiulus simplex (Chant)

Seiulus simplex Chant, 1956: 32 .

Typhlodromus simplex .—Hirschmann, 1962: 15.

Seiulus (Seiulus) simplex . — Beglyarov, 1981: 18.

Typhloseiulus simplex .—Moraes et al., 2004: 374; Chant & McMurtry, 2007: 145.

Reports on V. vinifera in Europe: Spain.

Reports on V. vinifera in non-European countries: None.

Reports not on V. vinifera: England, France, Greece, Hungary, Israel, Italy, Spain, Ukraine. Remarks. This species has been mainly reported from the Mediterranean region, essentially on oaks.

Species of Phytoseiidae on V. vinifera and the prey species associated

Tables 3 to 5 report species of the families of Eriophyidae , Tetranychidae , Tydeidae , Tenuipalpidae and Tarsonemidae that the 54 Phytoseiidae species have been reported to feed on. Thirty-five species among the 54 reported in European vineyards have been reported to feed on a great number of species, which is in accordance with the fact that most of Phytoseiidae are generalist predators (McMurtry & Croft, 1997).

Of the 54 species of Phytoseiidae considered here, 21 species feed on 21 species of Eriophyidae (Table 3). Calepitrimerus vitis (Nalepa) and Colomerus vitis (Pagenstecher) , the most important Eriophyidae on V. vinifera (Duso & De Lillo, 1996; Ferragut et al., 2008), can be preyed by T. (T.) pyri , A. andersoni and K. aberrans (Lorenzon et al., 2012) , whereas Cal. vitis has been found to be also fed by Neoseiulus alpinus . Furthermore, T. (T.) pyri is the species reported to feed on the highest number of Eriophyidae species (9), while K. aberrans preys upon four Eriophyidae species. Thirty-one Phytoseiidae have been reported to prey on at least one Tetranychidae species of the 47 considered (Table 4). Phytoseiulus persimilis is the species reported to fed on the highest number of Tetranychidae species (23) followed by N. californicus , N. fallacis and T. (T.) pyri . Among these 47 Tetranychidae species, 13 have been recorded on V. vinifera in Europe ( Tetranychus kanzawai (Kishida) , Tetranychus ludeni (Zacher) , Tetranychus mcdanieli (McGregor) , Tetranychus turkestani Ugarov & Nikolski , Tetranychus urticae Koch , Panonychus ulmi (Koch) , Panonychus citri (McGregor) , Oligonychus punicae (Hirst) , Bryobia praetiosa (Koch) , Eutetranychus banksi (McGregor) , Eutetranychus orientalis (Klein) , Eotetranychus carpini (Oudemans) , Eotetranychus pruni (Oudemans) . Typhlodromus (T.) pyri and K. aberrans are reported to prey on five of these 13 species, N. fallacis on six, N. californicus on seven and P. persimilis on eight. It is interesting to note that K. aberrans is reported to consume a low number of prey species and mainly in vineyards. The two main damaging Tetranychidae species in European vineyards are P. ulmi and E. carpini . Seventeen predatory mite species are reported to feed on the former species; among them, the most frequent are: E. finlandicus , K. aberrans , T. (T.) pyri , and T. (T.) exhilaratus . Seven Phytoseiidae species are reported to feed on E. carpini ; among them the most frequent are: K. aberrans , T. (T.) pyri , and T. (T.) exhilaratus .

Table 5 shows the species in the families Tydeidae , Tenuipalpidae , and Tarsonemidae preyed by the Phytoseiidae reported on V. vinifera in Europe. Only five species ( E. finlandicus , E. stipulatus , K. aberrans , T. pyri , T. phialatus ) are recorded to prey on Tydeidae (genera Lorrya and Tydeus ). Also six Phytoseiidae species have been reported to prey on Tenuipalpidae . Euseius scutalis seems to be more polyphagous, and preys on five species of Tenuipalpidae , among them the unique species found in vineyards is Brevipalpus lewisi . Eleven species of the Phytoseiidae have been reported to prey on Tarsomemidae (genera Polyphagotarsonemus and Steneotarsonemus ). Among them, only T. (T.) pyri is important in vineyards. However, none of these phytophagous species are considered vine pests.

Identification key to species of Phytoseiidae in European vineyards. The dichotomous key has been constructed to distinguish between the 54 species (3 sub-families and 15 genera) of Phytoseiidae reported on V. vinifera in Europe. It is also available on the website: http://www1.montpellier.inra.fr/CBGP/ phytoseiidae / sitewebvineyards2/index.htm. A polytomous identification key has also been constructed; it includes the 54 Phytoseiidae mite species and 30 continuous or discrete characters. This key has been elaborated in the same way as that described in Akashi et al. (2012). It allows beginning the identification with any of the 30 characters considered. It is an alternative of the dichotomous key, especially when a character is not visible (or with some doubt) in the pathway of identification of this latter tool. Finally, it allows the use of different and more characters than those imposed in the dichotomous key and to check the identification with the avalaible illustrations. This key is available on the same website.

1. Podonotal region of the dorsal shield, anterior to R1, with 4 pairs of lateral setae (j3, z2, z4 and s4); z3 and s6 are absent. Sub- family Amblyseiinae ................................................................................... 3

- Podonotal region of the dorsal shield, anterior to R1 with 5 or 6 pairs of lateral setae (j3, z2, z4 and s4 always present); z3 and/ or s6 are present....................................................................................... 2

2. Posterior lateral dorsal shield setae Z1, S2, S4 and S5 absent. Sub-family Phytoseiinae ............................. 23

- At least one of the setae Z1, S2, S4 or S5 is present. Sub-family Typhlodrominae ................................. 27

3. Sternal shield with median posterior projection, some forward migration of pre-anal setae J V 2 and Z V 2. ................ 4

- Sternal shield without posterior projection, without forward migration of pre-anal setae J V 2 and Z V 2. .................. 7

4. Ventrianal shield divided into separate ventral and anal shields. Dorsal shield strongly sclerotised, dark brown in colour, lateral integument also strongly sclerotised.............................................................................................Genus I phiseius: the unique species found on V. vinifera in Europe is I. degenerans (Berlese, 1889)

- Ventrianal shield entire, dorsal shield not strongly sclerotised, not brown in colour, lateral integument not strongly sclerotised.................................................................................................... 5

5. Peritreme short, extending to setae z4. Spermatheca with a short calyx and a globular atrium................................................................................................ Euseius finlandicus (Oudemans, 1915)

- Peritreme long, extending at least to setae z2. Spermatheca with a long calyx..................................... 6

6. Setae j1 and j3 subequal. Calyx of the spermatheca narrow and very long (40 µm). Setae S2, 41 µm long; setae s4, 62 µm long..................................................................... Euseius scutalis (Athias-Henriot, 1958)

- Setae j1 shorter than j3. Calyx of the spermatheca long (20 µm). Setae S2, 21 µm long; setae s4, 42 µm long................................................................................. Euseius stipulatus (Athias-Henriot, 1960a)

7. Setae S4 absent...................................................................................... 8

- Setae S4 present....................................................................................... 9

8. Setae J2 and S2 absent. Setae j6 very long; 2–3 times longer than distances between their bases. Ventrianal shield reduced, with 0-1 pair of pre-anal setae. The living mites are orange or red in colour............................................

............... Genus Phytoseiulus : the unique species found on V. vinifera in Europe is P. persimilis Athias-Henriot, 1957 - Setae J2 and S2 present. Setae j6 much shorter. Ventrianal shield elongate and narrow with three pairs of pre-anal setae. Short distance between the bases of setae Z1 and S2................................................................ .............. Genus Kampimodromus : the unique species found on V. vinifera in Europe is K. aberrans (Oudemans, 1930) 9. Ratio setae s4: Z1 <3.0:1.0; s4, Z4, and Z5 not greatly longer than other setae, never with wide sternal shield; J2 always pres- ent. Macrosetae absent on genu II and III................................................................ 10

- Ratio setae s4: Z1> 3.0:1.0; wide sternal shield. s4, Z4, and Z5 markedly longer than other dorsal setae. J2 present or absent. Macrosetae present on genu II and III..................................................................... 16

10. Sternal shield sometimes with two pairs of setae (setae ST3 off the sternal shield). Z4 length ranging from 55 to 77 µm; s4 length ranging from 56 to 78 µm............................................. Neoseiulus fallacis ( Garman, 1948)

- Sternal shield with three pairs of setae (setae ST3 on the sternal shield).......................................... 11

11. Calyx of the spermatheca fundibular*................................................................... 12

- Calyx of the spermatheca pocular*...................................................................... 14

12. Calyx of spermatheca not markedly constricted or stalked at junction with atrium. Crescentic pores on the ventrianal shield............................................................................ Neoseiulus barkeri Hughes, 1948

- Calyx of spermatheca stalked or narrowly constricted at juncture with atrium. More puctiform pores on the ventrianal shield.................................................................................................... 13

13. Neck between atrium and calyx short but well differentiated. Z4 length ranging from 26 to 38 µm; Z5 length ranging from 38 to 54 µm............................................................... Neoseiulus alpinus (Schweizer, 1922)

- Neck between atrium and calyx long and well differentiated. Z4 length ranging from 41 to 59 µm; Z5 length ranging from 26 to 38 µm............................................................. eoseiulus marginatus (Wainstein, 1961)

14. Dorsal shield with three pairs of prominent solenostomes (gd1 - gd6 - gd9). Ventrianal pores with crescentic form.............................................................................. Neoseiulus californicus (McGregor, 1954)

- Dorsal shield with five pairs of prominent solenostomes (gd1 - gd2 - gd6 - gd8 - gd9). Ventrianal pores punctiform.......... 15

15. Calyx of spermatheca bell-shaped. Z5 length ranging from 59 to 81 µm. Macrosetae present on leg IV....................................................................................... Neoseiulus cucumeris (Oudemans, 1930)

- Calyx of spermatheca cup-shaped. Z5 length ranging from 72 to 98 µm. Macrosetae absent on leg IV......................................................................................... Neoseiulus bicaudus (Wainstein, 1962)

16. Setae J2 absent, leg I without macrosetae on tarsus............................................................................. Genus Proprioseiopsis : the unique species found on V. vinifera in Europe is P. messor (Wainstein, 1960)

- Setae J2 present, leg I with macrosetae on tarsus........................................................... 17

17. Setae S5 present, ratio setae s4: S2>3.0:1.0; ventrianal shield not reduced, usually pentagonal....................... 18

- Setae S5 absent, ratio setae s4: S2 <2.7:1.0; ventrianal shield reduced, with a single pair of pre-anal setae......................................... Genus Amblyseiella : the unique species found on V. vinifera in Europe is A. setosa Muma, 1955

18. Spermatheca with atrium bifurcate/vacuolated at juncture with major duct. Male spermatophoral process T-shaped, with both heel and toe elongate, approximately subequal................................ Graminaseius graminis (Chant, 1956)

- Spermatheca with atrium not bifurcate/vacuolated at the juncture with major duct................................ 19

19. Setae Z V 2 off the ventrianal shield............................................. Amblyseius italicus (Chant, 1959)

- Setae Z V 2 on the ventrianal shield...................................................................... 20

20. Ventrianal pores punctiform. Spermatheca with very long neck; setae z2 5 µm long; setae Z5, 290 µm long; setae r3, 11 µm long...................................................................... Amblyseius obtusus (Koch, 1839)

- Ventrianal pores crescentic. Spermatheca with short neck; setae z2 at least 14 µm long; setae Z5, maximum 145 µm long; setae r3, at least 20 µm long............................................................................... 21

21. Setae Z5 77 µm long; macrosetae on genu IV 45 µm long. Calyx of spermatheca conical-shaped. Fixed digit of chelicera with six teeth............................................................ Amblyseius swirskii Athias-Henriot, 1962

- Setae Z5 at least 100 µm long; macrosetae on genu IV at least 78 µm long. Fixed digit of chelicerae with eight teeth..... 22

22. Ratio of setae S2 (25 µm): J2 (8 µm) is about 3:1. Calyx of spermatheca bell-shaped with nodular atrium. Three macrosetae on leg IV, genu, tibia and tarsus, the longest (78 µm) on the genu...................... Amblyseius andersoni (Chant, 1957)

- Setae S2 (13 µm) subequal in length to setae J2 (10 µm); Calyx of spermatheca U-shaped. Three macrosetae on leg IV, genu, tibia and tarsus, the longest (81 µm) on the tarsus.............................. Amblyseius rademacheri Dosse, 1958

23. Setae J2 and R1 present...................................................... Phytoseius finitimus Ribaga, 1904

- Setae J2 and R1 absent............................................................................... 24

24. Setae Z4 much longer than 100 µm (108 µm); setae s4 much longer than 100 µm (148 µm)...................................................................................................... Phytoseius horridus Ribaga, 1904

- Setae Z4, with maximum length of 70 µm; setae s4 w ith a maximum length of 100 µm............................. 25

25. Ventrianal shield without pores. Length of setae j4, j5, j6 much longer than 10 µm................................................................................................ Phytoseius plumifer (Canestrini & Fanzago, 1876)

- Ventrianal shield with a pair of pores. Length of setae j4, j5, j6 smaller than 10 µm................................ 26

26. Setae J5 and z5 subequal. Macroseta on tibia of leg IV 80 µm long. Peritreme extending anteriorly to level of j1; fixed digit of chelicerae with three teeth................................................. Phytoseius macropilis (Banks, 1909)

- Setae J5 twice the length of setae z5. Macroseta on tibia of leg IV 49 µm long. Peritreme extending between the level of j1 - j3. Fixed digit of chelicerae with two teeth............................. Phytoseius echinus Wainstein & Arutunjan, 1970

27. Setae z6 present, setae J V 2 absent, ventrianal shield larger than wide, with two pairs of pre-anal setae................. 28

- Setae z6 absent, setae J V 2 present....................................................................... 30

28. Setae Z3 present.................................................... Paraseiulus talbii (Athias-Henriot, 1960b)

- Setae Z3 absent..................................................................................... 29

29. Dorsal shield without solenostomes. Dorsal shield strongly sclerotised. Setae s6 25 µm, S4 23 µm, Z4 28 µm, Z5 28 µm............................................................................ Paraseiulus soleiger (Ribaga, 1904)

- Dorsal shield with three solenostomes (gd2, gd6, gd9). Dorsal shield moderately sclerotised. Setae s6 37 µm, S4 32 µm, Z4 34 µm, Z5 40 µm............................................. Paraseiulus triporus (Chant & Yoshida-Shaul, 1982)

30. Setae S4 and R1 present.............................................................................. 31

- Setae S4 and R1 absent.................................................................................................... Genus Galendromus : the unique species found on V. vinifera in Europe is G. longipilus (Nesbitt, 1951)

31. Setae Z1 absent..................................................................................... 32

- Setae Z1 present.................................................................................... 52

32. Setae S5 absent..................................................................................... 33

- Setae S5 present..................................................................................... 39

33. Ventrianal shield with pre-anal pores. Dorsal shield with five solenostomes (gd2, gd5, gd6, gd8, g d9)........................................................................................ Typhlodromus (T.) corticis Herbert, 1958

- Ventrianal shield without pre-anal pores. Dorsal shield with fewer than five solenostomes (gd5 absent)............... 34

34. Dorsal shield with four pairs of solenostomes (gd2, gd6, gd8, g d9). Seven setae on genu II......................... 35

- Dorsal shield with three pairs of solenostomes (gd2, gd6, gd9). Eight setae on genu II..................................................................................................... Typhlodromus (T.) pyri Scheuten, 1857

35. Cervix of spermatheca with neck....................................................................... 36

- Cervix of spermatheca without neck...................................................................... 37

36. Cervix of spermatheca C-shaped, 20 µm long, with thick, long neck. Peritreme extending to level of j3. Fixed digit of chelicera with four teeth. Setae z3, z4 27 µm long.............................. Typhlodromus (T.) cotoneastri Wanstein, 1961

- Cervix of spermatheca U-shaped, 17 µm long, with short neck. Peritreme extending between the level of j1 - j3. Fixed digit of chelicera with three teeth. Setae z3, z4 19 µm long........................ Typhlodromus (T.) exhilaratus Ragusa, 1977

37. Spermatheca with a short saccular cervix, less than 15 µm long. Peritreme extending between the level of z2 - z3. Movable digit of chelicera with two teeth. Macroseta on basitarsus IV less than half length of setae Z5................................................................................................. Typhlodromus (T.) tiliae Oudemans, 1929

- Spermatheca with a long saccular cervix, at least 15 µm long. Peritreme extending between the level of j1 - j3. Movable digit of chelicera with four teeth. Macroseta on basitarsus IV longer, about 3/4 length of setae Z5 ............................ 38

38. Setae JV5 and Z5 subequal. Setae Z5 54 µm long. Only one macroseta is present on leg IV on basitarsus. STIV 56 µm long. Fixed digit of chelicera with two teeth.............................. yphlodromus (T.) phialatus Athias-Henriot, 1960 b

- Setae JV5 shorter than Z5. Setae Z5 73 µm long. Three macrosetae present on leg I V. STIV 38 µm long. Fixed digit of chelicera with three teeth.............................................. Typhlodromus (T.) athiasae Porath & Swirski, 1965

39. Setae JV1 on the ventrianal shield, ventrianal shield with four pairs of setae..................................... 40

- Setae JV1 off the ventrianal shield, ventrianal shield with three pairs of setae............................................................................................ Typhlodromus (A.) intercalaris Livshitz & Kuznetsov, 1972

40. Dorsal shield with five pairs of solenostomes.............................................................. 41

- Dorsal shield with fewer than five pairs of solenostomes..................................................... 50

41. Ventrianal shield with one pair of pores................................................................... 42

- Ventrianal shield without pores........................................................................ 47

42. Dorsal shield reticulated or moderately reticulated......................................................... 43

- Dorsal shield heavily reticulated......................................................................... 46

43. Calyx of spermatheca short. Setae Z 4 30–33 µm long; setae Z5 42–50 µm long................................... 44

- Calyx of spermatheca elongate, 25 µm long. Setae Z4 49 µm long; setae Z5, 63 µm long....................................................................................... Typhlodromus (A.) rhenanoides Athias-Henriot, 1960 b

44. Three pairs of setae on the sternal shield. Peritreme extending between the level of z2 - j3................................................................................................... Typhlodromus (A.) atoosae Faraji, 2011

- Two pairs of setae on the sternal shield. Peritreme extending between the level of j1 - j3............................ 45

45. Macroseta on basitarsus on leg IV 59 µm long. Fixed digit of chelicera with three teeth, movable digit with two teeth.......................................................................... Typhlodromus (A.) yasminae Faraji, 2008

- Macroseta on basitarsus on leg IV 29 µm long. Fixed digit of chelicea with two teeth, movable digit with one tooth........................................................................ Typhlodromus (A.) rhenanus (Oudemans, 1905)

46. Calyx of spermatheca elongate, narrow and funnel-shaped; macroseta on basitarsus on leg IV knobbed and 41 µm long. Fixed digit of chelicera with two teeth......................................... Typhlodromus (A.) bakeri ( Garman, 1948)

- Calyx of spermatheca not elongate, atrium incorporated into the cervix. Macrosetae on basitarsus on leg IV pointed and 30 µm long. Fixed digit of chelicera with three teeth...................... Typhlodromus (A.) kerkirae Swirski & Ragusa, 1976

47. Peritreme extending at least to level of j3. Macroseta on basitarsus of leg IV more than 40 µm long. Fixed digit of chelicera with three teeth..................................................................................... 48

- Peritreme extending to level between setae z2 and j3. Macroseta on basitarsus of leg IV 30 µm long. Fixed digit of chelicera with four teeth....................................... Typhlodromus (A.) bagdasarjani Wainstein & Aratunjan, 1967

48. Movable digit of the chelicera with one tooth. Macroseta on basitarsus of leg IV 45 µm long...................................................................................... Typhlodromus (A.) athenas Swirski & Ragusa, 1976

- Movable digit of the chelicera with two teeth. Macroseta on basitarsus on leg IV 55 µm long........................ 49

49. We can not distinguish Typhlodromus (A.) involutus Livshitz & Kuznetsov, 1972 from Typhlodromus (A.) foenilis Oudemans, 1930 . The diagnostic value of the difference in chelicerae dentition (point 48) is also questionable. To determine if these three species are valid, further studies including molecular sequencing of specimens collected in the original localities of these three species would be required.

50. Dorsal shield with three pairs of solenostomes. Peritreme extending to level of j3. Fixed digit of chelicera with three teeth. 51 - Dorsal shield with four pairs of solenostomes. Peritreme extending to level of j1. Fixed digit of chelicera with two teeth............................................................... Typhlodromus (A.) psyllakisi Swirski & Ragusa, 1976 51. Ventrianal shield with one pair of pores. Peritreme extending forward to level of z2..................................................................................... Typhlodromus (A.) commenticus Livshitz & Kuznetsov, 1972 - Ventrianal shield without pores. Peritreme extending to level between setae z2 and j3 ..................................................................................................... Typhlodromus (A.) recki Wainstein, 1958 52. Ventrianal shield reduced, with one pair of pre-anal setae, peritreme long and striated, setae on dorsal shield mostly thick, thorn-like; cervix of spermatheca elongate and tubular............................................................................... Genus Typhloseiulus : the unique species found on V. vinifera in Europe is T. simplex (Chant, 1956) - Ventrianal shield not reduced, with 3-4 pairs of setae. Setae on dorsal shield mostly slender; peritreme long or short, punctate. Cervix of spermatheca cup-shaped or funnel-shaped....................................................... 53 53. Calyx of spermatheca pocular (5 µm); ventrianal shield with a pair of small round pores. Peritreme extending to setae j3. No teeth on movable digit. Seven setae on genu II.................................... Neoseiulella aceri (Collyer, 1957) - Calyx of spermatheca saccular (16 µm); ventrianal shield without pores. Peritreme extending anteriorly to z4. One tooth on movable digit. Eight setae on genu II....................................... Neoseiulella tiliarum (Oudemans, 1930)

*For the definition of the terms fundibular and pocular see Denmark & Edland (2002) and Denmark & Evans (2011)