Phytoseiidae in European grape (Vitis vinifera L.): bio-ecological aspects and keys to species (Acari: Mesostigmata)
Author
Tixier, Marie-Stéphane
Author
Baldassar, Andrea
Author
Duso, Carlo
Author
Kreiter, Serge
text
Zootaxa
2013
3721
2
101
142
journal article
10.11646/zootaxa.3721.2.1
04f0570e-ea0e-4409-b137-eb88e83225ae
1175-5326
217326
73B3C2CF-BAEE-4ED0-9F87-1DD85B7802C3
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)