Two new species of Ta m a r i x i a (Hymenoptera: Eulophidae) from Chile and Australia, established as biological control agents of invasive psyllids (Hemiptera: Calophyidae, Triozidae) in California
Author
Zuparko, Robert L.
Author
Queiroz, Dalva Luiz De
Author
Salle, John La
text
Zootaxa
2011
2921
13
27
journal article
46635
10.5281/zenodo.277920
134e43ac-a588-4e4b-9a64-7468ce0c7f31
1175-5326
277920
Tamarixia
Mercet, 1924
Type
species:
Tamarixia bicolor
Mercet, 1924
(original designation)
Diagnostic characters.
Tamarixia
possesses two apomorphic characters that are unique within the
Tetrastichinae
: males have exceptionally long genitalia, and the anterior margin of the female hypopygium is almost straight (which may be hidden under the preceding sternite and is not easily visible in undissected specimens). Specimens of
Tamarixia
can also generally be distinguished by a combination of characters: fore wing with a single seta on the dorsal surface of the submarginal vein, propodeum without a Y-shaped carina as seen in
Tetrastichus
(although see description of
Tamarixia dahlsteni
), midlobe of mesoscutum with 2 pairs of long, semi-erect setae that are about equal in length (
Figs 14, 15
) (although some specimens of
T. dahlsteni
have three pairs) (
Graham 1991
;
LaSalle 1994
). An additional diagnostic character is that the toruli are closer to eye margin than to each other (
Figs 6
,
13
). Species are generally shiny black, but may have yellow markings on the gaster and/or head.
Identification.
Tamarixia
contains species once treated as belonging to the
pubescens
group of the genus
Tetrastichus
(
Graham 1961
;
Domenichini 1966
,
1967
). The species group was subsequently treated as a subgenus within
Tetrastichus
by
Kostjukov (1977
,
1978
), but has since been treated as a genus by most authors (
Graham 1987
,
1991
;
Bouček 1988a
;
LaSalle 1994
;
Kostjukov, 1995
,
1996
,
2000
;
Schauff
et al
. 1997
;
Narendran 2007
).
Generic keys that distinguish
Tamarixia
from other tetrastichine genera are available for Australasia (
Bouček 1988a
), North
America
(
LaSalle 1994
;
Schauff
et al
. 1997
), Europe (
Graham 1987
,
1991
) and
India
(
Narendran 2007
). Keys to
Tamarixia
species are available for Europe (
Graham 1991
), European part of the
USSR
(
Kostjukov 1978: couplets
68–87 in
key to
Tetrastichus
), Far eastern
Russia
(
Kostjukov 1995
,
2000
),
India
(
Narendran 2007
) and North
America
(
Burks 1943, couplet
24 in
the key to species of the genus
Tetrastichus
, treating only the two species
). A list of the 47 described
Tamarixia
species, with host and distributional information, is given in
Table 1
.
TABLE 1.
Annotated list of species of
Tamarixia
.
See Noyes (2003) for further information on taxonomic history and synonymy. Classification of psyllid hosts follows Burckhardt (2005). Host information mainly taken from Noyes (2003), and in some cases updated following Burckhardt (pers. comm.) and Burckhardt & Lauterer (1997) for
Bactericera
.
actis
(Walker 1839)
Distribution. Europe:
Czech Republic
,
France
,
Germany
,
Hungary
,
Ireland
,
England
. Macaronesia: Azores, Canary Islands.
Hosts.
Psyllidae, Strophingiinae
:
Strophingia cinereae
Hodkinson
,
Strophingia ericae
(Curtis)
.
Host plants.
Ericaceae
:
Calluna vulgaris
(Linnaeus)
,
Erica cinerea
Linnaeus
,
Erica scoparia
Linnaeus.
akkumica
(
Kostjukov 1978
)
Distribution. Asia:
Kazakhstan
.
arboreae
(Graham 1979)
Distribution. Macaronesia: Madeira Islands.
Hosts.
Psyllidae, Strophingiinae
:
Strophingia arborea
Loginova
,
Strophingia fallax
Loginova. Host
plants.
Ericaceae
:
Erica arborea
Linnaeus
,
Erica scoparia
Linnaeus.
asiatica
Kostjukov 1996
Distribution. Asia:
Kazakhstan
.
atamiensis
(
Ashmead 1904
)
. New combination from
Tetrastichus
Tetrastichus atamiensis
Ashmead, 1904
: 162
.
Holotype
Ƥ,
Japan
, Atami. USNM
Type
7206 [examined, digital image]. Distribution: Asia:
Japan
.
bermius
(Walker 1848)
=
upis
bicolor
Mercet 1924
Distribution. Europe:
Bulgaria
,
Spain
. Asia:
Pakistan
. Hosts.
Triozidae
:
Trioza chenopodii
Reuter. Host
plants.
Chenopodiaceae
:
Chenopodium album
Linnaeus.
brovni
Kostjukov 2000
Distribution. Asia:
Russia
(Primor'ye Kray).
caillardiae
(
Kostjukov 1978
)
Distribution. Asia:
Kazakhstan
.
Hosts.
Psyllidae
,
Aphalarinae
:
Caillardia notata
Loginova. Host
plants.
Amaranthaceae
:
Haloxylon
sp.
callunae
(Erdös 1969)
=
actis
cometes
(
Girault 1915
)
Distribution.
Australia
(Northern Territory).
dahlsteni
Zuparko
,
sp. nov.
Distribution.
Australia
(New South
Wales
, Queensland, Western
Australia
, Victoria). Hosts.
Triozidae
:
Trioza eugeniae
.
Host plants.
Myrtaceae
:
Syzygium paniculatum
.
Biological control. Imported into
USA
: California for the biological control of
Trioza eugeniae
.
dhetysaicus
Kostjukov 1996
Distribution. Asia:
Kazakhstan
.
dryi
(Waterston 1922)
Distribution. Africa:
Kenya
,
South Africa
,
Swaziland
,
Zimbabwe
. Hosts.
Triozidae
:
Trioza erytreae
(Del Guercio)
.
Host plants.
Rutaceae
:
Citrus
spp.
Biological control. Imported into
Réunion
,
Mauritius
for the biological control of
Trioza erytreae
.
dwivarnus
Narendran 2007
Distribution. Asia:
Sri Lanka
.
dyra
(
Burks 1943
)
Distribution. North
America
:
USA
(Colorado, Montana, Wyoming). Hosts.
Psyllidae
,
Aphalarinae
:
Aphalara curta
(Caldwell)
;
Triozidae
:
Trioza
sp. Host plants.
Rutaceae
:
Citrus
spp.;
Apiaceae
:
Angelica
sp.;
Salicaceae
:
Salix
sp.;
Ranunculaceae
:
Thalictrum
sp.
flavicoxae
Kostjukov 2000
Distribution. Asia:
Russia
(Primor'ye Kray).
flavigaster
(Brothers & Moran 1969)
Distribution. Africa:
South Africa
.
Hosts.
Psyllidae
,
Rhinocolinae
:
Moraniella calodendri
(Moran)
. Host plants.
Rutaceae
:
Calodendrum capense
(Linnaeus filius).
flaviventris
(
Kostjukov 1978
)
Distribution. Asia:
Kazakhstan
,
Tajikistan
.
girishi
Narendran 2007
Distribution. Asia:
India
(Kerala).
hanca
Kostjukov 2000
Distribution. Asia:
Russia
(Primor'ye Kray).
klarisae
Kostjukov 1996
Distribution. Asia:
Kazakhstan
.
leptothrix
Graham 1991
Distribution. Europe:
Czechoslovakia
,
Hungary
,
Ireland
,
Italy
,
England
,
Yugoslavia
. Host plants.
Salicaceae
:
Salix alba
Linnaeus
,
Salix cinerea
Linnaeus
,
Salix fragilis
Linnaeus.
leucaenae
Bou
ĕ
ek 1988
Distribution. North
America
:
USA
(Florida). Central
America
and Caribbean:
Mexico
,
Trinidad & Tobago
. Hosts.
Psyllidae, Ciriacreminae
:
Heteropsylla cubana
.
Host plants.
Rutaceae
:
Citrus
spp.;
Fabaceae
:
Leucaena
sp.,
Leucaena leucocephala
(Lamarck)
. Biological control. Imported into Africa and Asia for the biological control of
Heteropsylla cubana
.
meteroa
(
Girault 1915
)
Distribution.
Australia
(Queensland).
monesus
(Walker 1839)
Distribution. Europe:
Czech Republic
,
England
,
France
,
Germany
,
Hungary
,
Ireland
,
Italy
,
Slovakia
,
Slovenia
,
Sweden
,
Yugoslavia
. Asia:
Kazakhstan
,
Moldova
,
Russia
(Astrakhanskaya Oblast).
newelskoyi
(Kostjukov 1990)
Distribution. Asia:
Russia
(Yevreyskaya Oblast).
nocturna
Kostjukov 2000
Distribution. Asia:
Russia
(Primor'ye Kray).
obscuratus
(André 1878)
=
pronomus
orientalis
Khan, Agnihotri & Sushil 2005
Distribution. Asia:
India
(Uttaranchal).
Hosts.
Agromyzidae
: Unspecified species. NOTE: This is the only record of a species of
Tamarixia
from an agromyzid, and indeed from a non-Hemipteran. It should be treated as doubtful without subsequent confirmation.
Host plants.
Asteraceae
:
Helianthus
sp.
orsillus
(Walker 1839)
=
upis
pallicornis
(Walker 1872)
Distribution. Macaronesia: Madeira Islands.
pallicornis
(Thomson 1878)
=
monesus
pallidicornis
(Dalla Torre 1898)
=
monesus
pamyles
(Walker 1839)
=
pronomus
poddubnyi
(
Kostjukov 1978
)
Distribution. Asia:
Moldova
,
Uzbekistan
,
China
(
new record
- NingXia, Yinchuan, Gaojiazha,
22 June 2010
, coll. C.D. Zhu, on
Eleagnus angustifolia
Linnaeus
).
Hosts.
Triozidae
:
Trioza magnisetosa
Loginova
;
Aphididae
:
Capitophorus hippophaes
(Walker)
.
Host plants.
Elaeagnaceae
:
Elaeagnus
sp.,
Elaeagnus orientalis
Linnaeus
,
Eleagnus angustifolia
(
new record
).
pojarkovi
(Kostjukov 1990)
Distribution. Asia:
Russia
(Primor'ye Kray).
pookodica
Narendran 2007
Distribution. Asia:
India
(Kerala).
pronomus
(Walker 1839)
Distribution. Europe:
Czech Republic
,
England
,
France
,
Germany
,
Greece
,
Hungary
,
Ireland
,
Italy
,
Norway
,
Portugal
,
Sweden
. Macaronesia: Canary Islands, Madeira Islands.
Hosts.
Triozidae
:
Bactericera kratochvili
Vondracek
,
Trioza apicalis
Förster
,
Trioza centranthi
(Vallot)
,
Trioza urticae
(Linnaeus)
.
Host plants.
Valerianaceae
:
Centranthus angustifolius
(Miller)
.
przewalskii
(Kostjukov 1990)
Distribution. Asia:
Russia
(Yevreyskaya Oblast).
pubescens
(Nees 1834)
Distribution. Europe:
Czech Republic
,
England
,
Germany
,
Hungary
,
Italy
,
Slovakia
,
Yugoslavia
. Hosts:
Triozidae
.
Trioza remota
Förster.
pygmaea
(Erdös 1954)
=
pygmaeola
pygmaeola
(Erdös 1958)
Distribution. Europe:
France
,
Hungary
,
Yugoslavia
. Hosts.
Triozidae
:
Trioza rumicis
Löw.
Host plants.
Polygonaceae
:
Rumex scutatus
Linnaeus.
radiata
(Waterston 1922)
Distribution. Asia:
India
,
Pakistan
.
Hosts.
Psyllidae, Diaphorininae
:
Diaphorina citri
;
Psyllidae, Aphalaroidinae
:
Pallipsylla hyalina
(Mathur)
;
Triozidae
:
Trioza erytreae
,
Trioza
sp.
Host plants.
Fabaceae
:
Albizia lebbeck
(Linnaeus)
;
Rutaceae
:
Citrus
spp.,
Murraya paniculata
(Linnaeus)
.
Biological control. Imported into
Réunion
,
India
,
Saudi Arabia
,
Mauritius
,
Nepal
,
Taiwan
,
China
,
Indonesia
,
Malaysia
,
Thailand
,
Vietnam
,
USA
(Florida, Texas),
Mexico
,
Brazil
,
Argentina
,
Guadeloupe
,
Puerto Rico
for the biological control of
Diaphorina citri
.
rudolfae
(
Kostjukov 1978
)
Distribution. Asia:
Kazakhstan
.
schina
Zuparko
,
sp. nov.
Distribution. South
America
:
Chile
.
Hosts.
Calophyidae
:
Calophya schini
.
Host plants.
Anacardiaceae
:
Schinus molle
.
Biological control. Imported into
USA
(California) for the biological control of
Calophya schini
. Also present in
Mexico
, presumably as spread of the California introduction.
sheebae
Narendran 2005
Distribution. Asia:
India
(Kerala).
Host plants.
Combretaceae
:
Terminalia arjuna
Roxburgh.
stelleri
(Kostjukov 1990)
Distribution. Asia:
Russia
(Primor'ye Kray).
tamaricis
(
Domenichini 1967
)
=
bicolor
tremblayi
(Domenichini 1965)
Distribution. Europe:
Czechoslovakia
,
Italy
,
United Kingdom
. Hosts.
Triozidae
:
Bactericera tremblayi
(Wagner)
. Host plants.
Alliaceae
:
Allium cepa
Linnaeus.
triozae
(
Burks 1943
)
Distribution.
USA
(Arizona, California, Colorado, Idaho, Kansas, Montana, Nebraska, New
Mexico
, Texas, Washington). NOTE:
Herting (1972)
recorded this species from
Italy
, and
Chazeau (1987)
reported it from
New Caledonia
on
Heteropsylla cubana
on
Leucaena leucocephala
. Because
T
.
triozae
is otherwise known only from the Nearctic region, we suspect these records are misidentifications.
Hosts.
Calophyidae
:
Calophya californica
Schwarz
,
Calophya nigrella
Jensen
,
Calophya nigripennis
Riley
,
Calophya triozomima
Schwarz
;
Psyllidae
:
Ceanothia ceanothi
(Crawford)
,
Euglyptoneura minuta
(Crawford)
,
Euphalerus vermiculosus
Crawford
,
Pexopsylla cercocarpi
Jensen
;
Triozidae
:
Bactericera cockerelli
(Sulc)
,
Bactericera minuta
(Crawford)
,
Bactericera nigricornis
(Förster)
,
Trioza albifrons
Crawford
,
Trioza beameri
Tuthill.
Host plants.
Rosaceae
:
Amelanchier
sp.;
Solanaceae
:
Solanum tuberosum
Linnaeus.
tschirikovi
(Kostjukov 1990)
Distribution. Asia:
Russia
(Yevreyskaya Oblast).
turundaevskayae
(
Kostjukov 1978
)
Distribution. Asia:
Kazakhstan
.
upis
(Walker 1839)
Distribution. Europe:
Czech Republic
,
England
,
France
,
Italy
,
Slovakia
,
Sweden
,
Moldova
,
Russia
(Moscow Oblast, St. Petersberg). Macaronesia: Madeira Islands.
Hosts.
Triozidae
:
Bactericera femoralis
(Förster)
,
Trioza urticae
.
Host plants.
Rosaceae
:
Alchemilla vulgaris
Linnaeus
;
Urticaceae
:
Urtica
sp.
vinokurovi
Kostjukov 1995
Distribution. Asia:
Russia
(Primor'ye Kray).
yoorica
Narendran 2007
Distribution. Asia:
India
(Kerala).
Distribution.
Tamarixia
is a cosmopolitan genus, with most of its 47 described species from the Palearctic and Oriental regions (
Table 1
). Because the greatest diversity of Psylloidea occurs in the southern tropics (
Hodkinson 1984
), the number of known
Tamarixia
species will undoubtedly increase as the fauna from Africa,
Australia
and South
America
becomes better characterized. During the course of this study, specimens have been examined that represent quite a few new species from North
America
(California, Florida), South
America
(
Brazil
,
Chile
), and
Australia
. It is clear that further collecting and rearing of psyllids will greatly expand the known fauna of this genus.
Biology.
Species of
Tamarixia
are primary parasitoids of psyllids (
Graham 1987
,
1991
;
Bouček 1988a
,
1988b
;
LaSalle 1994
;
Noyes 2003
). However, aphids can also serve as hosts for
Tamarixia
species. In his description of
T. poddubnyi
,
Kostjukov (1978)
recorded it from the aphid
Capitophorus hippophaes
(Walker)
, and an undescribed
Tamarixia
species in EMEC has the label data: California: Los Angeles County, Highway 138, 6 miles east of Gorman,
1 June 1961
, J.C. Hall, reared from
Aphis gossypii
[Glover] on
Solanum elaeagnifolium
[Cavanilles]. Further collecting will be required to understand just how frequent the use is of non-psyllid hosts. A record of
T. orientalis
Khan, Agnihotri & Sushil
from an agromyzid (
Table 1
) should be treated as doubtful without subsequent confirmation.
Most records list
Tamarixia
species as ectoparasitoids, however
T. upis
(Walker)
has been recorded as an endoparasitoid (
Noyes 2003
).