Entomopathogenic nematodes can protect citrus fruits from the damage caused by the mediterranean fruit fly

The data presented by Abd-Elgawad et al., at the 49th Annual meeting of the Society of Nematlogists held from July 11-14, 2010 in Boise, Idaho clearly demonstrated that the application of two species of entomopathogenic nematodes (Steinernema riobrave and Heterorhabditis bacteriophora) in the soil significantly reduced the emergence of adults Mediterranean fruit fly, Ceratitis capitata when  compared with the untreated control.

Control of annual bluegrass weevil, Listronotus maculicollis with entomopathogenic nematodes

It has been reported that the entomopathogenic nematodes including Steinernema carpocapsae, S. feltiae and Heterorhabditis bacteriophora when applied at rate of 2.5 billion infective juveniles/ha can cause 69- 94% mortality of first generation late instars of annual bluegrass weevil, Listronotus maculicollis. Of the 3 species of entomopathogenic nematodes, S. feltiae showed higher virulence against annual bluegrass weevil than the other two nematode species (see McGraw et al., 2010).

Read following research papers for more information on interaction between entomopathogenic nematodes and annual bluegrass weevil, L. maculicollis.

McGraw, B.A., Vittumb, P.J. Cowlesc, R.S.and Koppenhoumlfera, A.M. 2010.  Field evaluation of entomopathogenic nematodes for the biological control of the annual bluegrass weevil, Listronotus maculicollis (Coleoptera: Curculionidae), in golf course turfgrass. Journal Biocontrol Science and Technology. 20: 149 - 163.

Entomopathogenic nematodes can be used for controlling pests of stored grains

It has been demonstrated that the efficacy of entomopathogenic nematodes (Heterorhabditis bacteriophora, Steinernema carpocapsae, and Steinernema feltiae against various stored grain pests (Mediterranean flour moth, Ephestia kuehniella, lesser grain borer, Rhyzopertha dominica, rice weevil, Sitophilus oryzae and confused flour beetle, Tribolium confusum) of wheat (Triticum aestivum L.) varied with nematode dosages and temperature in the storage structures. Please read following papers for detailed information on the interaction between entomopathogenic nematodes and stored grain pests.

Athanassiou, C.G., Kavallieratos, N.C., Menti, H. and Karanastasi, E. 2010.  Mortality of four stored product pests in stored wheat when exposed to doses of three entomopathogenic nematodes.  Journal of Economic Entomology. 103: 977-984.

Athanassiou, C.G., Palyvos, N.E. and Kakoull-Duarte, T. 2008.  Insecticidal effect of Steinernema feltiae (Filipjev) (Nematoda : Steinernematidae) against Tribolium confusum du Val (Coleoptera : Tenebrionidae) and Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) in stored wheat  Journal of Stored Products Research. 44: 52-57.

Mbata, G.N., and Shapiro-Ilan, D.I. 2005.  Laboratory evaluation of virulence of heterorhabditid nematodes to Plodia interpunctella Hübner (Lepidoptera: Pyralidae). Environmental Entomology. 34: 676 – 682.

Ramos-Rodríguez, O., Campbell, J. F. and Ramaswamy, S. 2006.  Pathogenicity of three species of entomopathogenic nematodes to some major stored- product insect pest. Journal of Stored Product Research 42: 241 – 252.

Ramos-Rodríguez,O., Campbell, J. F. and Ramaswamy, S. 2007.  Efficacy of the   entomopathogenic nematodes Steinernema riborave against the stored-product pests Tribolium castaneum and Plodia interpunctella. Biological Control 40:15 -21.

Tradan, S., Vidric, M. and Valic, N. 2006.  Activity of four entomopathogenic nematodes against young adult of Sitophilus granarious (Coleptera: Curculionidae ) and Oryzophilus surinamensis ( Coleoptera: Silvanidae ) under laboratory condition. Plant Disease and Protection. 113: 168 – 173.

Kill cereal leaf beetles, Oulema melanopus with entomopathogenic nematodes

Recently, it has been demonstrated that the entomopathogenic nematodes including Steinernema feltiae strain B30, S. carpocapsae strain C101, and Heterorhabditis bacteriophora strain D54 have a potential to use as biological control agents against cereal leaf beetles (Oulema melanopus), which is a most common pest of many cereal crops including barley, corn, oats, wheat, rye, millet and rice.

For more information on interaction between entomopathogenic nematodes and cereal leaf beetles read following research paper.

Laznik, Z., Toth, I., Lakatos, T., Vidrih, M. and Trdan, S. 2010.  Oulema melanopus (L.) (Coleoptera: Chrysomelidae) adults are susceptible to entomopathogenic nematodes (Rhabditida) attack: results from a laboratory study. Journal of Plant Diseases and Protection. 117: 30-32.

Susceptibility of longicorn beetle (Dorcadion pseudopreissi) to entomopathogenic nematodes

Recently, it has been reported that a new insect pest of turf called longicorn beetle (Dorcadion pseudopreissi) was susceptible to three species entomopathogenic nematodes including Steinernema carpocapsae, S. feltiae and Heterorhabditis bacteriophora under laboratory condition. The results of this study suggests that the entomopathogenic nematodes have a potential to use as biological control agents against longicorn beetles (Susurluk et al., 2009). Susurluk, I.A., Kumral, N.A., Peters, A., Bilgili, U. and Acikgoz, E. 2009. Pathogenicity, reproduction, and foraging behaviours of some entomopathogenic nematodes on a new turf pest,

How entomopathogenic nematodes find their insect hosts (Foraging Strategies)

Infective juveniles of entomopathogenic nematodes use three different strategies to find their insect hosts.1. Ambush foraging: Ambushers such as Steinernema carpocapsae and S. scapterisci have adapted "sit and wait" strategy to attack highly mobile insects (billbugs, sod webworms, cutworms, mole-crickets and armyworms) when they come in contact at the surface of the soil.  These nematodes do not respond to host released cues but infective juveniles of some Steinernema spp can stand on their tails (nictate) and easily infect passing insect hosts by jumping on them.  Since highly mobile insects live in the upper soil or thatch layer, ambushers are generally effective in infecting more insects on the surface than deep in the soil. 2. Cruise foraging: Cruiser nematodes such as Heterorhabditis bacteriophora, H. megidis, Steinernema glaseri and S. kraussei generally move actively in search of hosts and therefore, they are distributed throughout the soil profile and more effective against less mobile hosts such as white grubs and black vine weevils.  Cruisers never nictate but respond to carbon dioxide released by insects as cues. 3. Intermediate foraging: Some nematode species such as Steinernema feltiae and S.riobrave have adapted a strategy in between ambush and cruise strategies called an intermediate strategy to attack both the mobile and sedentary/less mobile insects at the surface or deep in the soil.  Steinernema feltiae is highly effective against fungus gnats and mushroom flies whereas S.riobrave is effective against corn earworms, citrus root weevils and mole crickets.

Kill Western Flower Thrips with Entomopathogenic Nematodes

• The Western flower thrips, Frankliniella occidentalis is a most economically important pest of many field- and glasshouse-grown vegetables and ornamentals.

• Adults lay eggs in the parenchyma tissue and there are two larval stages (first and second instars), prepupal and pupal stages are present in the life cycle of thrips.

• Adult thrips generally feed by piercing and scraping of the stem, leaf, flower and fruit tissues.

• Both instars also feed on all the aerial plant parts including leaves, flowers and fruits.

• Piercing and scraping of the plant tissues leads to discoloration and drying of the damaged area, in some cases, abortion of flower/leaf buds or distortion of emerging leaves, thus reducing field crop yield and aesthetic value of ornamental plants.

• Thrips are also capable of transmitting tospoviruses such as tomato spotted wilt virus (TSWV) and impatiens necrotic spot virus (INSV) during feeding, thus causing a tremendous loss to agricultural and horticultural greenhouse industries.

• Controlling western flower thrips is difficult because of their small size and cryptic behavior.

• Western flower thrips are commonly eradicated using endosulfan, chlorpyrifos, bendiocarb, and synthetic pyrethrinoids but use of these insecticides is restricted due to their environmental pollution and human health concerns, development of resistance to pesticides and removal of some of the most effective products from the market.

• Biological control agents including predacious mites (Neoseilus cucumeris and Neoseilus degenerans), predacious bugs (Orius insidiosus), entomopathogenic fungi (Beauveria bassiana, Metarhizium anisopliae) and entomopathogenic nematodes (see below) have been used as alternatives to chemical pesticides.

• The entomopathogenic nematodes species including Heterorhabditis bacteriophora, H. indica, H. marelata and Steinernema abassi, S. carpocapase, and S. feltiae have been found to be effective alternatives to chemical insecticides in controlling western flower thrips.

• The entomopathogenic nematodes specifically attack soil-dwelling second instar larval, prepupal and pupal stages.

• Generally, Heterorhabditis species are more effective than Steinernema species nematodes in controlling western flower thrips.

• The insect- parasitic nematodes such as Thripinema nicklewoodii also have a potential to use as a biological control agent against western flower thrips.

• Application of entomopathgenic nematodes at the rate of 400 infective juveniles/ cm2 of soil surface can cause over 50% mortality of thrip population.

• Nematodes can be easily applied in water suspension as spray applications to the surface of plant growing medium or on the plant foliage infested with western flower thrips.

• Although larval stages, prepupae and pupae are susceptible to entomopathogenic nematodes, H. bacteriophora HK3 strain can cause higher mortality of larval and prepupal stages than pupal stages

How Entomopathogenic Nematodes kill Western Flower Thrips

• When the infective juveniles are applied to the surface of plant growing medium or injected in the potting medium, they start searching for their hosts, in this case Western Flower Thrip larvae, prepupae and pupae.

• Once a larvae, prepupae and pupae has been located, the nematode infective juveniles penetrate into the larvae, prepupae and pupae body cavity via natural openings (mouth, anus and spiracles).

• Infective juveniles of Heterorhabditis also enter through the intersegmental members of the grub/pupa cuticle.

• Once in the body cavity, infective juveniles release symbiotic bacteria (Xenorhabdus spp. for Steinernematidae and Photorhabdus spp. for Heterorhabditidae) from their gut in the larvae, prepupal and pupal blood.

• Multiplying nematode-bacterium complex in the blood causes septicemia and kills the grub usually within 48 h after infection.

• Nematodes feed on multiplying bacteria, mature into adults, reproduce and then emerge as infective juveniles from the cadaver to seek new larvae, prepupae and pupae in the potting medium/soil.

Biological Control of Black Vine Weevil using Insect Parasitic Nematodes

• Black vine weevil, Otiorhynchus sulcatus is a common insect pest of over 150 plant species that grown in the greenhouses and nurseries.

• Some of the plant species damaged by black vine weevils include Azalea, Cyclamen, Euonymus, Fuxia, Rosa, Rhododendron and Taxus.

• Grubs (Larvae) of these weevils generally girdle the main stem, and feed and damage roots leading to nutrient deficiencies.

• Adults feed on leaves and flowers by notching their edges thus reducing aesthetic value of plants.

• The entomopathogenic nematodes species including Heterorhabditis bacteriophora, H. megidis and Steinernema carpocapase, S. feltiae and S. glaseri have been found to be effective alternatives to chemical insecticides such as chlorpyrifos (Dursban) in controlling black vine weevils.

• Susceptibility of black vine weevil to nematodes is species and strain specific.

• The rate of application of the nematode species/strains that tested against black vine weevil varies (5,000- 60,000 infective juveniles/pot) among different studies but nematodes applied at the rate of 5000- 20,000 infective juveniles/pot can cause up to 100% grub mortality.

• Nematodes can be easily applied in water suspension as spray applications to the surface of plant growing medium but if nematodes are injected at depths deeper than 5 cm i.e. near to grubs they can cause highest mortality of grubs (70-93%) than those nematodes applied to the surface.

• All the four larval stages (instars) and pupae of black vine weevil are susceptible to all entomopathogenic nematode species.

• However, Heterorhabdtis bacteriophora can cause higher mortality of first and second instars than S. carpocapase and S. glaseri.

• Also, all the three nematodes species are equally effective against third and fourth instars of black vine weevil.

How Entomopathogenic Nematodes Kill Black Vine Weevil

• When the infective juveniles are applied to the surface of plant growing medium or injected in the potting medium, they start searching for their hosts, in this case black vine weevil grubs and pupae.

• Once a grub/pupa has been located, the nematode infective juveniles penetrate into the grub or pupa body cavity via natural openings (mouth, anus and spiracles).

• Infective juveniles of Heterorhabditis also enter through the intersegmental members of the grub/pupa cuticle.

• Once in the body cavity, infective juveniles release symbiotic bacteria (Xenorhabdus spp. for Steinernematidae and Photorhabdus spp. for Heterorhabditidae) from their gut in the grub blood.

• Multiplying nematode-bacterium complex in the blood causes septicemia and kills the grub usually within 48 h after infection.

• Nematodes feed on multiplying bacteria, mature into adults, reproduce and then emerge as infective juveniles from the cadaver to seek new grubs or pupae in the potting medium/soil.

Kill fungus gnats using biological control agents: Insect-parasitic nematodes

• Several fungus gnat species including Bradysia coprophila, B. impatiens and B. difformis are considered economically important indoor and greenhouse pests in Europe and the US.
• Fungus gnat flies are black or gray in color with clear wings, relatively small (3-4 mm) in size and commonly associated with compost and natural soils with high organic contents.
• You can see these hopping flies when you water your plants.
• Fungus gnat maggots (larvae) are white-bodied with black heads and can be found just under the surface of the potting medium/soil.
• These maggots primarily feed on fungi and organic matter but they can also cause a serious damage to many ornamental plants.
• Maggots often chew or strip plant roots and tunnel stems affecting water and nutrient absorption in severely injured plants resulting in lost vigor, turn off-color and eventually death.
• Maggots are also capable of transmitting fungal pathogens (Fusarium, Phoma, Pythium and Verticillium) during feeding.
• Adult flies are nuisance to people and disseminate fungal spores from plant to plant as they disperse through the greenhouse.
• Females often laying over 1000 eggs in a lifetime on the media surface and completing egg-to-egg life cycle within 20-25 days at 20-25oC.
• Continuous and overlapping generations of fungus gnats in the greenhouse have made most control strategies difficult.
• Currently, most growers rely on insecticides to manage fungus gnats in floriculture.
• However, use of these insecticides is restricted due to their environmental pollution and human health concerns, development of resistance to pesticides and removal of some of the most effective products from the market.
• Biological control agents including Bacillus thuringiensis (Bt), the predatory mite, Hypoaspis miles and entomopathogenic nematodes have been used as alternatives to chemical pesticides.
• The entomopathogenic nematodes species including Heterorhabditis bacteriophora GPS11 strain, H. indica LN2 strain and Steinernema feltiae UK strain have a potential to use as biocontrol agents against fungus gnats.
• These nematodes kill both maggots (larvae) and pupae, but the second and fourth stages are most susceptible than pupae.
• Nematodes are generally applied in water suspension as spray applications to the surface of plant growing medium to target larval and pupal stages.
• The potting medium (Ball-mix, Nursery-mix or Pro-mix) can influence the survival, persistence and efficacy of entomopathogenic nematodes in greenhouse production.
• In the Nursery-mix, H. bacteriophora can survive longer and perform better than H. indica, H. marelatus Oregon, H. zealandica X1 and Steinernema feltiae against fungus gnats.
• In the Pro-mix, only H. indica have performed better than all other nematode species that tested against fungus gnats.
• Application of S. feltiae can cause 40% reduction in fungus gnat population in Ball-mix, 50% in Metro-mix and 56% in Pro-mix, but only 27% in the Nursery-mix.
• In the greenhouse, temperature can influence efficacy of nematodes. For example, H. bacteriophora and H. indica can survive and cause very high mortality of fungus gnats at warmer (above 25oC) temperatures whereas S. feltiae is generally effective against fungus gnats at cooler (below 25oC) temperatures.
• Application of an appropriate concentration of nematodes is a crucial step in the cost effective control of fungus gnats in greenhouse production.
• Generally, application of one billion infective juveniles of H. bacteriophora, H. indica or S. feltiae per acre can kill over 50% fungus gnats in greenhouse productions.

How entomopathogenic nematodes kill fungus gnats

• When the infective juveniles are applied to the surface of plant growing medium, they start searching for hosts, in this case fungus gnat maggots (larvae) and pupae.
• Once a maggot/pupa has been located, the nematode infective juveniles penetrate into the maggot body cavity via natural openings such as mouth, anus and breathing pores called spiracles.
• Infective juveniles of Heterorhabditis spp also enter through the intersegmental members of the maggot/pupal cuticle.
• Once in the body cavity, infective juveniles release symbiotic bacteria (Xenorhabdus spp. for Steinernematidae and Photorhabdus spp. for Heterorhabditidae) from their gut in the fungus gnat blood.
• Multiplying nematode-bacterium complex causes septicemia and kills the host usually within 48 h after infection.
• Nematodes feed on multiplying bacteria, mature into adults, reproduce and then emerge as infective juveniles from the cadaver to seek new maggots in the potting medium/soil.

Nematodes are now commercially available from many suppliers distributed throughout in the USA.

For more information on biological control of fungus gnats, please read following research papers/book chapters:

• Binns, E.S., 1973.  Fungus gnats (Diptera: Mycetophilidae, Sciaridae) and the role of mycophagy in soil: a review. Rev. Ecol. Biol. Sol. 18, 77-90.
• Chambers, R.J., Wright, E.M., Lind, R.J., 1993.  Biological control of glasshouse sciarid larvae (Bradysia spp.) with the predatory mite, Hypoaspis miles on Cyclamen and Poinsettia. Biocontrol Sci. Technol. 3, 285-293.
• Ecke, P.Jr., Faust, J.E., Williams, J., Higgins, A., 2004.  The Poinsettia Manual. Ball Publishing, The Paul Ecke Ranch, Encinitas, California, USA.
• Freeman, P., 1983.  Sciarid flies, Diptera; Sciaridae. Handbooks for the identification of British insects 9, Part 6. London, Royal Entomol. Soc. pp 68.
• Gillespie, D.R., Menzies, J.G., 1993.  Fungus gnat vector Fusarium oxysporum f. sp. radicislycopersici.  Ann. Appl. Biol. 123, 539-544.
• Gouge, D.H., Hague, N.G.M., 1994.  Control of sciarids in glass and propagation houses with Steinernema feltiae. Brighton Crop Protection Conference: Pest Dis. 3, 1073-1078.
• Gouge, D.H., Hague, N.G.M., 1995.  Glasshouse control of fungus gnats, Bradysia paupera, on fuchsias by Steinernema feltiae. Fundam. Appl. Nematol. 18, 77-80.
• Grewal, P.S., Richardson, P.N., 1993.  Effects of application rates of Steinernema feltiae (Nematoda: Steinernematidae) on control of the mushroom sciarid fly, Lycoriella auripila (Diptera: Sciaridae).  Biocontrol Sci. Technol. 3, 29-40.
• Grewal, P.S., Tomalak, M., Keil, C.B.O., Gaugler, R., 1993. Evaluation of a genetically selected strain of Steinernema feltiae against the mushroom sciarid fly, Lycoriella mali. Ann. Appl. Biol. 123, 695-702.
• Harris, M.A., Oetting, R.D., Gardner, W.A., 1995.  Use of entomopathogenic nematodes and new monitoring technique for control of fungus gnats, Bradysia coprophila (Diptera: Sciaridae), in floriculture. Biol. Control 5, 412-418.
• Jagdale, G. B., Casey, M. L., Grewal, P. S. and Lindquist, R. K. 2004.  Application rate and timing, potting medium and host plant on the efficacy of Steinernema feltiae against the fungus gnat, Bradysia coprophila, in floriculture. Biol. Contrl. 29: 296-305.
• Jagdale, G. B., Casey, M. L., Grewal, P. S. and Luis Cañas. 2007.  Effect of entomopathogenic nematode species, split application and potting medium on the control of the fungus gnat, Bradysia difformis (Diptera: Sciaridae), in the greenhouse at alternating cold and warm temperatures. Biol. Control. 43: 23-30.
• Kim, H.H., Choo, H.Y., Kaya, H.K., Lee, D.W., Lee, S.M., Jeon, H.Y., 2004.  Steinernema carpocapsae (Rhabditida: Steinernematidae) as a biological control agent against the fungus gnat Bradysia agrestis (Diptera: Sciaridae) in propogation houses. Biocontrol Sci. Technol. 14, 171-183.
• Lindquist R., Piatkowski J. 1993. Evaluation of entomopathogenic nematodes for control of fungus gnat larvae. Bull. Int. Organiz. Biol. Integr. Control Noxious Animals and Plants. 16, 97-100.
• Lindquist, R.K., Faber, W.R., Casey, M.L., 1985.  Effect of various soilless root media and insecticides on fungus gnats.  HortScience. 20, 358-360.
• Menzel, F., Smith, J.E., Colauto, N.B., 2003.  Bradysia difformis Frey and Bradysia ocellaris (Comstock): two additional neotropical species of black fungus gnats (Diptera : Sciaridae) of economic importance: a redescription and review. Ann. Entomol. Soc. Am. 96, 448-457.
• Nielsen, G. R., 2003. Fungus gnats. http://www.uvm.edu/extension/publications/el/el50.htm
• Oetting, R.D., Latimer, J.G., 1991.  An entomogenous nematode Steinernema carpocapsae is compatible with potting media environments created by horticultural practices. J. Entomol. Sci. 26, 390-394.
• Olson, D.L., Oetting, R.D., van Iersel, M.W., 2002.  Effect of soilless media and water management on development of fungus gnats (Diptera: Sciaridae) and plant growth. HortScience. 37: 919-923.
• Richardson, P.N., Grewal, P.S., 1991.  Comparative assessment of biological (Nematoda: Steinernema feltiae) and chemical methods of control of mushroom fly, Lycoriella auripila (Diptera: Sciaridae).  Biocontrol Sci. Technol. 1, 217-228.
• Tomalak, M., Piggott, S. and Jagdale, G. B. 2005.  Glasshouse applications. In: Nematodes As Biocontrol Agents. Grewal, P.S. Ehlers, R.-U., Shapiro-Ilan, D. (eds.). CAB publishing, CAB International, Oxon. Pp 147-166.
• Wilkinson, J.D., Daugherty, D.M., 1970.  Comparative development of Bradysia impatiens (Diptera: Sciaridae) under constant and variable temperatures. Ann. Entomol. Soc. Am. 63, 1079-1083.