Trichogramma natural enemies of stored-product insects

Egg parasitoids have the advantage of killing pest eggs before they hatch into larvae which can cause larval feeding damage to the stored commodity and have the disadvantage that egg mortality of pest is often quite high so many of the eggs parasitized would have died anyway before hatching. Host feeding has been observed and reported for ten species of Trichogramma, i. e., Trichogramma australicum (Nurindah and Gordh 1999), Trichogramma brassicae (Blanche et al. 1996, Lessard and Boivin 2013, Vasquez et al. 1997),  Trichogramma chilonis (Suzuki et al. 1984, Miura and Kobayashi 1998), Trichogramma embryophagum (Ryvkin 1959), Trichogramma evanescens (Jacob and Boivin 2005), Trichogramma ostriniae (Vasquez et al. 1997), Trichogramma minutum (Vasquez et al. 1997), Trichogramma platneri (Hohmann et al. 1988, Mills and Kuhlmann 2004, Vasquez et al. 1997), Trichogramma pretiosum (Mills and Kuhlmann 2004, Rukmowati and Walter 2006, Vasquez et al. 1997) and Trichogramma turkestanica (Ferracini et al. 2006, Hansen and Jensen 2002, Schöller et al. 1996 as T. evanescens?). Hansen and Jensen 2002 reported that research on T. turkestanica had been reported under the name “Lager” strain T. evanescens in Germany (e.g., Schöller 1996, 2001). Ferracini et al. 2006 studied the benefits of host feeding for T. turkestanica. Destructive host feeding by T. brassicae, T. ostriniae and T. pretiosum averaged 19-29% and by T. minutum, T. platneri and T. turkestanica averaged between 50-63%.

Quite a few species of Trichogramma (55) can be added to the ten Trichogramma species given in the Stored-Product Insect Resources book as shown below. Brower 1984, Hayat and Viggiani 1984, Polaszek 2010 and Smith 1996 have provided extensive lists of Trichogramma hosts. A large number of Trichogramma species are known to attack Corcyra cephalonica, Ephestia kuehniella and Sitotroga cerealella because these stored-product insect species often are used as factitious hosts for rearing Trichogramma in the laboratory. Smith 1996 reviewed the literature on rearing Trichogramma and concluded that S. cerealella is used by producers in slightly more than half the countries. Several countries, including France and Canada, have switched to E. kuehniella. C. cephalonica, is used in Asian countries. Trichogramma emerging from E. kuehniella eggs are equivalent in quality in the field to those from or S. cerealella eggs, but better performance has been observed in the laboratory with E. kuehniella eggs, possibly because of their slightly larger size. In Stored-Product Insect Resoruce the host range, for the five species with the broadest range of stored-product insect pest species, varied from 8 (Trichogramma chilonis) to 22 (Trichogramma evanescens). In list below, Trichogramma brassicae and Trichogramma cacoeciae also attacked 8 species of stored-product insect pests.

Field scale studies of Trichogramma deion against Plodia interpunctella eggs in simulated retail store by Grieshop et al. 2006, Trichogramma pretiosum against Cadra cautella and P. interpunctella eggs in bulk stored peanuts by Brower 1988, T. turkestanica against E. kuehniella eggs in flour mill by Hansen and Jensen 2002b are cited in SPI Res, but not identified as field scale studies. Three additional field scale studies have been published (T. evanescens against E. kuehniella eggs in flour mill by Tuncbilik et al. 2008 and in bakery by Prozell and Scholler 1998; Trichogramma nubilale against Phthorimaea operculella eggs in potato storage by Chouvalitwongporn 1993). Scholler et al 1994, 1996 investigated the depth of penetration of wheat by T. evanescens and T. embryophagum. In above studies, egg parasitization ranged from 11 to 97%. Also, E. kuehniella and/or S. cerealella egg cards have been used in vineyard (Barnay et al. 2001) and olive grove (Hegazi et al. 2012, Herz et al. 2007) to monitor several species of Trichogramma. Kuske et al. 2003 used E. kuehniella egg cards to monitor the dispersal of Trichogramma brassicae in the field.

Several studies have shown the not all Trichogramma recognized Apomyelois ceratoniae, E. kuehniella or S. cerealella eggs as hosts. Ksentini et al. 2013 showed that Trichogramma oleae and Trichogramma bourarachae did not recognize A. ceratoniae or E. kuehniella eggs as hosts. Monje et al. 1999 showed that Trichogramma galloi did not recognize S. cerealella eggs as hosts. Reznik et al 2001 showed that half of Trichogramma principium parasitized S. cerealella eggs on the first day of adult life, 10% refused to parasitize and the rest delayed parasitization 2-19 days, and Reznik et al 2009 showed that Trichogramma buesi did not recognized S. cerealella eggs as hosts. Rundle et al. 2004 found that Trichogramma funiculatum did not recognize S cerealella eggs as hosts.

Trichogramma acacioi Brun, Moraes & Soares

     Hosts: Ephestia kuehniella, Sitotroga cerealella

     Sources: Pratissoli et al. 2008, 2009

Trichogramma achaeae Nagaraja and Nagarkatti

     Hosts: Corcyra cephalonica, Pectinophora gossypiella, Sitotroga cerealella

     Sources: Hayat and Viggiani 1984, Jalali 2013, Polaszek 2010, Rao and Suhas 1987

Trichogramma agriae Nagaraja

     Hosts: Corcyra cephalonica

     Sources: Hayat and Viggiani 1984, Polaszek 2010

Trichogramma agrotidis Voegelé and Pintureau

     Hosts: Ephestia kuehniella

     Sources: Polaszek 2010

Trichogramma aurosum Sugonjaev and Sorokina

     Hosts: Cydia pomonella

     Sources: Polaszek 2010

Trichogramma australicum Girault

     Hosts: Corcyra cephalonica

     Sources: Kareem et al. 1977, Medina and Cadapan 1981

Trichogramma bournieri Pintureau and Babault

     Hosts: Sitotroga cerealella

     Sources: Haile et al. 2002

Trichogramma bourarachae Pintureau and Babault

     Hosts: Apomyelois ceratoniae, Ephestia kuehniella

     Sources: Polaszek 2010

Trichogramma brasiliensis Ashmead

     Hosts: Corcyra cephalonica, Phthorimaea operculella

     Sources: Bharti et al. 1994, Harwalkar et 1987

Trichogramma brassicae Bezdenko

     Hosts: Apomyelois ceratoniae, Cadra cautella, Cydia pomonella, Ephestia kuehniella,      Galleria mellonella, Pectinophora gossypiella. Plodia interpunctella, Sitotroga cerealella, Tineola bisselliella

     Sources: Bigler et al. 1987, Iranipour et al. 2009, Polaszek 2010, Steidle et al. 2001, Wajnberg et al. 2000, Zimmermann et al. 2003

Trichogramma buesi Voegelé

     Hosts: Ephestia kuehniella

     Sources: Polaszek 2010

Trichogramma cacoeciae Marchal

     Hosts: Apomyelois ceratoniae, Cadra cautella, Cydia pomonella, Ephestia elutella, Ephestia kuehniella, Galleria mellonella, Phthorimaea operculella, Plodia interpunctella, Sitotroga cerealella

     Sources: Barnay et al. 1999, Bennett et al. 2002, Ksentini et al. 2013, Makee 2005, Mansour 2010, Ozder and Kara 2010, Polaszek 2010, Saour 2004, Scholler 2001, Vourlioti and Milonas 2005-2006

Trichogramma californicum Nagaraja and Nagarkatti

     Hosts: Ephestia kuehniella

     Sources: Rajendram 1978

Trichogramma carverae Oatman and Pinto

      Hosts: Cadra cautella, Ephestia kuehniella

      Sources: Steidle et al. 2001

Trichogramma cephalciae Hochmut and Martinek

     Hosts: Ephestia kuehniella

     Sources: Polaszek 2010

Trichogramma chilonis Ishii

     Hosts: Cadra cautella, Corcyra cephalonica, Cydia pomonella, Ephestia kuehniella, Galleria mellonella, Leguminivora glycinivorella, Pectinophora gossypiella, Phthorimaea operculella, Sitotroga cerealella

     Sources: Hayat and Viggiani 1984, Hugar et al. 1990, Paul et al. 1981, Polaszek 2010, Reay-Jones et al. 2006, Saljoqi et al. 2012

Trichogramma chilotraeae Nagaraja and Nagarkatti

     Hosts: Corcyra cephalonica, Ephestia kuehniella

     Sources: Hayat and Viggiani 1984, Medina and Cadapan 1981, Polaszek 2010

Trichogramma closterae Pang and Chen

     Hosts: Corcyra cephalonica

     Sources: Polaszek 2010

Trichogramma cordubense Vargas and Cabello

     Hosts: Apomyelois ceratoniae, Ephestia kuehniella

     Sources: Polaszek 2010, Roriz et al. 2006

Trichogramma cultellus Jose, Hirose and Honda

     Hosts: Ephestia kuehniella

     Sources: Polaszek 2010

Trichogramma danubiense Birova and Kazimirova

     Hosts: Ephestia kuehniella

     Sources: Polaszek 2010

Trichogramma daumalae Dugast and Voegelé

     Hosts: Cydia pomonella, Ephestia kuehniella, Galleria mellonella, Sitotroga cerealella

     Sources: Polaszek 2010

Trichogramma deion Pinto & Oatman

     Hosts: Ephestia kuehniella, Plodia interpunctella

     Sources: Grieshop et al. 2006, 2008, Schöller and Fields 2002

Trichogramma dendrolimi Matsumura

     Hosts: Cadra cautella, Corcyra cephalonica, Cydia pomonella, Ephestia kuehniella, Galleria mellonella, Leguminivora glycinivorella, Sitotroga cerealella

     Sources: Hegazi et al. 2000, Polaszek 2010

Trichogramma elegantum Sorokina

     Hosts: Sitotroga cerealella

     Sources: Polaszek 2010

Trichogramma embryophagum (Hartig)

     Hosts: Apomyelois ceratoniae, Corcyra cephalonica, Cydia pomonella, Ephestia elutella, Ephestia kuehniella, Pectinophora gossypiella, Sitotroga cerealella

     Sources: Hayat and Viggiani 1984, Klomp and Teerink. 1978, Polaszek 2010, Poorjavad et al. 2011

Trichogramma erosicornis Westwood

     Hosts: Corcyra cephalonica, Ephestia cautella, Ephestia kuehniella, Sitotroga cerealella

     Sources: Hayat and Viggiani 1984, Polaszek 2010

Trichogramma euproctidis (Girault)

     Hosts: Corcyra cephalonica, Cydia pomonella, Ephestia kuehniella, Sitotroga cerealella

     Sources: Polaszek 2010, Tuncbilek et al. 2012

Trichogramma evanescens Westwood

     Hosts: Acanthoscelides obtectus, Achroia grisella, Apomyelois ceratoniae, Cadra calidella, Cadra cautella, Cydia pomonella, Corcyra cephalonica, Dermestes maculates, Endrosis lactella, Ephestia elutella, Ephestia kuehniella, Etiella zinckenella, Galleria mellonella, Maruca vitrata, Pectinophora gossypiella, Phthorimaea operculella, Plodia interpunctella, Sitotroga cerealella, Tribolium castaneum

     Sources: Boldt and Marston 1974, Boldt et al. 1973, Boldt 1974, Ksentini et al. 2013, Lewis and Redlinger 1969, Polaszek 2010, Prozell and Scholler 1998, Saour 2004, Scholler 2000, 2001, Tuncbilek et al. 2008

Trichogramma exiguum (Pinto and Platner)

     Hosts: Cadra cautella, Corcyra cephalonica, Sitotroga cerealella

     Sources: Dass et al. 1983, Hayat and Viggiani 1984, Paul et al. 1981

Trichogramma fasciatum (Perkins)

     Hosts: Corcyra cephalonica

     Sources: Hayat and Viggiani 1984, Ram and Sharma 1977

Trichogramma hesperidis Nagaraja

     Hosts: Corcyra cephalonica

     Sources: Hayat and Viggiani 1984, Jalali 2013, Polaszek 2010

Trichogramma ingricum Sorokina

     Hosts: Sitotroga cerealella

     Sources: Polaszek 2010

Trichogramma ivelae Pang and Chen

     Hosts: Carpocapsa pomonella, Sitotroga cerealella

     Sources: McLaren and Rye 1983, Polaszek 2010

Trichogramma japonicum Ashmead

     Hosts: Achroia grisella, Corcyra cephalonica, Ephestia cautella, Galleria mellonella, Pyralis farinalis, Sitotroga cerealella

     Sources: Bentur et al. 1994, Hayat and Viggiani 1984, Polaszek 2010

Trichogramma jezoense Ishii

     Hosts: Leguminivora glycinivorella

     Sources: Polaszek 2010

Trichogramma kilinceri Bulut and Kilinçer

     Hosts: Cydia pomonella

     Sources: Polaszek 2010

Trichogramma lopezandinensis Sarmiento

     Hosts: Tecia solanivora

     Sources: Rubio et al. 2004

Trichogramma minutum Riley

      Hosts: Corcyra cephalonica, Cydia pomonella, Ephestia kuehniella, Galleria mellonella, Plodia interpunctella, Sitotroga cerealella

      Sources: Alden and Farlinger 1931, Boldt 1974, Boldt and Marston 1974, Hayat and Viggiani 1984, Losey 1995, Schöller and Fields 2002

Trichogramma nubilale Ertle and Davis

      Hosts: Corcyra cephalonica, Phthorimaea operculella, Sitotroga cerealella

      Sources: Chouvalitwongporn 1993, Polaszek 2010

Trichogramma oleae Voegelé and Pointel

      Hosts: Cadra calidella, Cadra cautella, Ephestia kuehniella

      Sources: Polaszek 2010

Trichogramma ostriniae Pang and Chen

      Hosts: Corcyra cephalonica, Ephestia cautella, Ephestia kuehniella, Galleria mellonella, Plodia interpunctella, Sitotroga cerealella

      Sources: Grieshop et al. 2008, Hoffmann et al. 2001, Polaszek 2010

Trichogramma pallidiventris Nagaraja

      Hosts: Corcyra cephalonica

      Sources: Hayat and Viggiani 1984, Hussein et al. 1996, Polaszek 2010

Trichogramma papilionis Nagarkatti

      Hosts: Corcyra cephalonica

      Sources: Polaszek 2010

Trichogramma parkeri Nagarakatti

      Hosts: Cadra cautella

      Sources: Brower 1984

Trichogramma pelovi Kostadinov

      Hosts: Cydia pomonella

      Sources: Polaszek 2010

Trichogramma perkinsi Girault

      Hosts: Corcyra cephalonica, Sitotroga cerealella

      Sources: Callejas 1980, Polaszek 2010

Trichogramma piceum Dyurich

      Hosts: Sitotroga cerealella, Tineola bisselliella

      Sources: Zimmermann et al. 2003

Trichogramma pintoi Voegelé

      Hosts: Corcyra cephalonica, Ephestia kuehniella, Sitotroga cerealella

      Sources: Hayat and Viggiani 1984, Polaszek 2010

 

Trichogramma plasseyense Nagaraja

      Hosts: Corcyra cephalonica

      Sources: Hayat and Viggiani 1984, Polaszek 2010

Trichogramma platneri Nagarkatti

     Hosts: Amyelois transitella, Cadra cautella, Cryptoblabes gnidiella, Cydia pomonella, Ephestia kuehniella, Plodia interpunctella, Sitotroga cerealella

      Sources: Hohmann et al. 1988, Losey 1995, Polaszek 2010

Trichogramma poliae Nagaraja

     Hosts: Corcyra cephalonica

     Sources: Hayat and Viggiani 1984, Polaszek 2010

Trichogramma pretiosum Riley

     Hosts: Cadra cautella, Cadra figulilella, Ephestia elutella, Ephestia kuehniella, Galleria mellonella, Phthorimaea operculella, Plodia interpunctella, Sitotroga cerealella

     Sources: Boldt and Marston 1974, Boldt et al. 1973, Brower 1983, 1984, 1988, Grieshop et al. 2008, Losey 1995, Morrison et al.1976, Orphanides and Gonzalez. 1971, Pratissoli and Parra 2000, Pratissoli et al. 2008, Schöller and Fields 2002, Steidle et al. 2001

Trichogramma principium Sugonjaev and Sorokina

      Hosts: Apomyelois ceratoniae, Cydia pomonella, Ephestia kuehniella, Phthorimaea operculella, Sitotroga cerealella

      Sources: Makee 2005, Polaszek 2010, Poorjavad et al. 2011, Reznik et al. 2001, Saour 2004

Trichogramma raoi Nagaraja

     Hosts: Corcyra cephalonica

     Sources: Hayat and Viggiani 1984, Polaszek 2010

Trichogramma retorridum Girault

     Hosts: Ephestia kuehniella, Sitotroga cerealella

     Sources: Orphanides and Gonzalez. 1971

Trichogramma savalense Sorokina

     Hosts: Sitotroga cerealella

     Sources: Polaszek 2010

Trichogramma semblidis (Aurivillius)

     Hosts: Corcyra cephalonica, Cydia nigricana, Cydia pomonella, Ephestia kuehniella, Phthorimaea operculella, Sitotroga cerealella

     Sources: Hayat and Viggiani 1984, Polaszek 2010

Trichogramma semifumatum (Perkins)

     Hosts: Ephestia kuehniella, Sitotroga cerealella

     Sources: Rounbehler and Ellington 1973, Taylor and Stern 1971

Trichogramma sibericum Sorokina

     Hosts: Ephestia kuehniella, Plodia interpunctella

     Sources: Polaszek 2010, Schöller and Fields 2002

Trichogramma silvestre Sorokina

     Hosts: Sitotroga cerealella

     Sources: Polaszek 2010

Trichogramma sorokinae Kostadinov

     Hosts: Ephestia kuehniella

     Sources: Polaszek 2010

Trichogramma turkeiensis Bulut and Kilinçer

     Hosts: Cydia pomonella, Ephestia kuehniella, Sitotroga cerealella

     Sources: Polaszek 2010

Trichogramma turkestanica Meyer

     Hosts: Ephestia kuehniella

     Sources: Hansen 2000a,b; Hansen and Jensen 2002a

Trichogramma yawarae Hirai and Fursov

     Hosts: Ephestia kuehniella

     Sources: Polaszek 2010

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