Abstract
Entomopathogenic nematodes Steinernema and Heterorhabditis are excellent biocontrol agents of crop insect pests. These beneficial nematodes decrease the reliance on synthetic pesticides and assist in maintaining a desirable ecological balance. They adapt to a wide range of behavioural strategies, and their degree of efficacy varies with species and the ecological niche where nematode -insect interactions take place. Occurrence and distribution of entomopathogenic nematodes are related to certain insect groups that are considered their suitable hosts. Soil texture and presence of a host affect the nematode ’s direction of movement. The specific behaviours and cues used by infective juveniles of different nematode species vary while searching and finding the hosts. The process of infection is governed by several factors such as host recognition behaviour, acceptance behaviour and infection behaviour . Cues such as feces or cuticle associated with living insects affect a nematode ’s foraging behaviour which varies with respect to nematode species. Therefore, correct selection of nematode species is of foremost importance in the insect pest management strategies. Apart from nematodes’ habitat preference and infection behaviour , survival strategy and reproductive behaviour are other important parameters that need attention.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Abd-Elgawad MMM, Askary TH, Coupland J (2017) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CAB International, Wallingford, UK, p 648
Alatorre-Rosas R, Kaya HK (1990) Interspecific competition between entomopathogenic nematodes in the genera Heterorhabditis and Steinernema for an insect host in sand. J Invertebr Pathol 55:179–188
Ali SS, Ahmad R, Hussain MA, Parvez R (2005) Pest management in pulses through entomopathogenic nematodes. Indian Institute of Pulse Research, Kanpur, India
Askary TH (2010) Nematodes as biocontrol agents. In: Lichtfouse E (ed) Sociology, organic farming climate change and soil science. Springer, The Netherlands, pp 347–378
Askary TH, Abd-Elgawad MMM (2017) Beneficial nematodes in agroecosystems: a global perspective. In: Abd-Elgawad MMM, Askary TH, Coupland J (eds) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CAB International, Wallingford, UK, pp 3–25
Askary TH, Ahmad MJ (2017) Entomopathogenic nematodes: mass production, formulation and application. In: Abd-Elgawad MMM, Askary TH, Coupland J (eds) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CAB International, Wallingford, UK, pp 261–287
Askary TH, Nermuť J, Ahmad MJ, Ganai MA (2017) Future thrusts in expanding the use of entomopathogenic and slug parasitic nematodes in agriculture. In: Abd-Elgawad MMM, Askary TH, Coupland J (eds) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CAB International, Wallingford, UK, pp 620–627
Barbercheck ME, Kaya HR (1991) Effect of host condition and soil texture on host finding by the entomogenous nematodes Heterorhabditis bacteriophora (Rhabditida, Heterorhabditidae) and Steinernema carpocapsae (Rhabditida, Steinernematidae). Environ Entomol 20:582–589
Barker DM (1994) Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim Behav 48:147–156
Baur ME, Kaya HK, Strong DR (1998) Foraging ants as scavengers on entomopathogenic nematode-killed insects. Biol Control 12:231–236
Byers JA, Poinar GO Jr (1982) Location of insect hosts by the nematode, Neoaplectana carpocapsae, in response to temperature. Behaviour 79:1–10
Campbell JF, Gaugler R (1993) Nictation behaviour and its ecological implications in host search strategies of entomopathogenic nematodes. Behaviour 126:155–169
Campbell JF, Gaugler R (1997) Inter-specific variation in entomopathogenic nematode foraging strategy: dichotomy or variation along a continuum? Fundam Appl Nematol 20:393–398
Campbell JF, Kaya HK (1999a) How and why a parasitic nematode jumps. Nature 397:485–486
Campbell JF, Kaya HK (1999b) Mechanism, kinematic performance, and fitness consequences of jumping behaviour in entomopathogenic nematodes (Steinernema spp.). Can J Zool 77:1947–1955
Campbell JF, Kaya HK (2000) Influence of insect associated cues on the jumping behavior of entomopathogenic nematodes (Steinernema spp.). Behaviour 137:591–609
Campbell JF, Kaya HK (2002) Variation in entomopathogenic nematode (Steinernematidae and Heterorhabditidae) infective-stage jumping behaviour. Nematology 4:471–482
Campbell JF, Lewis EE (2002) Entomopathogenic nematode host-search strategies. In: Lewis EE, Campbell JF, Sukhdeo MVK (eds) The behavioural ecology of parasites. CABI Publishing, Wallingford, UK, pp 13–38
Campbell JF, Orza G, Yoder F, Lewis EE, Gaugler R (1998) Spatial and temporal distribution of endemic and released entomopathogenic nematode populations in turfgrass. Entomol Exp Appl 86:1–11
Campbell JF, Koppenhofer AM, Kaya HK, Chinnasri B (1999) Are there temporarily non-infectious dauer stages in entomopathogenic nematode populations? A test of the phased infectivity hypothesis. Parasitology 118:499–508
Christen JM, Campbell JF, Lewis EE, Shapiro-Ilan DI, Ramaswamy SB (2007) Responses of the entomopathogenic nematode, Steinernema riobrave to its insect hosts, Galleria mellonella and Tenebrio molitor. Parasitology 134:889–898
Ciche TA, Darby C, Ehlers R-U, Forst S, Goodrich-Blair H (2006) Dangerous liaisons: the symbiosis of entomopathogenic nematodes and bacteria. Biol Control 38:22–46
Ciche TA, Kim KS, Kaufmann-Daszczuk B, Nguyen KCQ, Hall DH (2008) Cell invasion and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes. Appl Environ Microbiol 74:2275–2287
Coupland J, Abd-Elgawad MMM, Askary TH (2017) Beneficial nematodes and the changing scope of crop protection. In: Abd-Elgawad MMM, Askary TH, Coupland J (eds) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CAB International, Wallingford, UK, pp 26–42
Csontos AS (2002) Lateral movement of the entomopathogenic nematodes Steinernema glaseri and Heterorhabditis bacteriophora in sand at different temperatures in response to host seeking. Biocontrol Sci Tech 12:137–139
Dillon AB, Ward D, Downes MJ, Griffin CT (2006) Suppression of the large pine weevil Hylobius abietis (L.) (Coleoptera: Curculionidae) in pine stumps by entomopathogenic nematodes with different foraging strategies. Biol Control 38:217–226
Dix I, Koltai H, Glazer I, Burnell AM (1994) Sperm competition in mated 1st generation hermaphrodite females of the HP-88 strain of Heterorhabditis (Nematoda, Heterorhabditidae) and progeny sex-ratios in mated and unmated females. Fundam Appl Nematol 17:17–27
Doutt RL (1964) Biological characteristics of entomophagous adults. In: DeBach P (ed) Biological control of insect pests and weeds. Reinhold, New York, USA, pp 145–167
Downes MJ, Griffin CT (1996) Dispersal behaviour and transmission strategies of the entomopathogenic nematodes Heterorhabditis and Steinernema. Biocontrol Sci Tech 6:347–356
Ebssa L, Dix I, Griffin CT (2008) Female presence is required for male sexual maturity in the nematode Steinernema longicaudum. Curr Biol 18:R997–R998
Ehlers R-U (2001) Mass production of entomopathogenic nematodes for plant protection. Appl Microbiol Biotechnol 56:623–633
Emelianoff V, Sicard M, N-le Brun, Moulia C, Ferdy JB (2007) Effect of bacterial symbionts Xenorhabdus on mortality of infective juveniles of two Steinernema species. Parasitol Res 100:657–659
Emelianoff V, Chapuis E, Le Brun N, Chiral M, Moulia C, Ferdy JB (2008) A survival-reproduction trade-off in entomopathogenic nematodes mediated by their bacterial symbionts. Evolution 62:932–942
Ennis DE, Dillon AB, Griffin CT (2010) Simulated roots and host feeding enhance infection of subterranean insects by the entomopathogenic nematode Steinernema carpocapsae. J Invertebr Pathol 103:140–143
Fenton A, Magoolagan L, Kennedy Z, Spencer KA (2011) Parasite-induced warning coloration: a novel form of host manipulation. Anim Behav 81:417–422
Gaugler R, Bilgrami AL (2004) Introduction and overview. In: Gaugler R, Bilgrami AL (eds) Nematode behaviour. CAB International, Wallingford, UK, pp XI–XXIV
Gaugler R, Kaya HK (1990) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, Florida, USA, p 349
Gaugler R, Kaya HK (1993) Entomopathogenic Nematodes. Annu Rev Entomol 38:181–206
Gaugler R, LeBeck L, Nakagaki B, Boush GM (1980) Orientation of the entomogenous nematode, Neoaplectana carpocapsae to carbon dioxide. Environ Entomol 9:649–652
Gaugler R, Lewis EE, Stuart RJ (1997) Ecology in the service of biological control: the case of entomopathogenic nematodes. Oecology 109:483–489
Gaugler R, Brown I, Shapiro-Ilan DI, Atwa A (2002) Automated technology for in vivo mass production of entomopathogenic nematodes. Biol Control 24:199–206
Ghally SE (1995) Some factors affecting the activity and pathogenicity of Heterorhabditis heliothids and Steinernema carpocapsae nematodes. J Egypt Soc Parasitol 25:125–135
Glazer I (1997) Effects of infected insects on secondary invasion of steinernematid entomopathogenic nematodes. Parasitology 114:597–604
Glazer I, Kozodoi E, Salame L, Nestel D (1996) Spatial and temporal occurrence of natural populations of Heterorhabditis spp. (Nematoda: Rhabditida) in a semiarid region. Biol Control 6:130–136
Grewal PS, Gaugler R, Selvan S (1993) Host recognition by entomopathogenic nematodes: Behavioral response to contact with host feces. J Chem Ecol 19:1219–1231
Grewal PS, Lewis EE, Gaugler R, Campbell JF (1994) Host finding behaviour as a predictor of foraging strategy in entomopathogenic nematodes. Parasitology 108:207–215
Grewal PS, Lewis EE, Gaugler R (1997) Response of infective stage parasites (Nematoda: Steinernematidae) to volatile cues from infected hosts. J Chem Ecol 23:503–515
Griffin CT (2012) Perspectives on the behavior of entomopathogenic nematodes from dispersal to reproduction: traits contributing to nematode fitness and biocontrol efficacy. J Nematol 44:177–184
Griffin CT, Boemare NE, Lewis EE (2005) Biology and behaviour. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CAB International, Wallingford, UK, pp 47–64
Han RC, Ehlers R-U (2000) Pathogenicity, development, and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. J Invertebr Pathol 75:55–58
Hara AH, Kaya HK (1983) Development of the entomogenous nematode, Neoaplectana carpocapsae (Rhabditida: Steinernematidae), in insecticide killed beet armyworm (Lepidoptera: Noctuidae). J Econ Entomol 76:423–426
Huettel RN (2004) Reproductive behaviour. In: Gaugler R, Bilgrami AL (eds) Nematode behaviour. CAB International, Wallingford, UK, pp 127–149
Jaworska M (1993) Investigations on the possibility of using entomopathogenic nematodes in reduction of Cephalcia abietis (L.) (Hym., Pamphilidae) population. Polskie Pismo Entomologiczne 62:201–213
Koppenhöfer AM, Kaya HK (1995) Density-dependent effects on Steinernema glaseri (Nematoda: Steinernematidae) within an insect host. J Parasitol 81:797–799
Koppenhöfer AM, Baur ME, Kaya HK (1996) Competition between two steinernematid nematode species for an insect host at different soil depths. J Parasitol 82:34–40
Koppenhöfer AM, Baur ME, Stock SP, Choo HY, Chinnasri B, Kaya HK (1997) Survival of entomopathogenic nematodes within host cadavers in dry soil. Appl Soil Ecol 6:231–240
Koppenhöfer AM, Cowles RS, Cowles EA, Fuzy EM, Kaya HK (2003) Effect of neonicotinoid synergists on entomopathogenic nematode fitness. Entomol Exp Appl 106:7–18
Kruitbos LM, Heritage S, Hapca S, Wilson MJ (2010) The influence of habitat quality on the foraging strategies of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidis. Parasitology 137:303–309
Kunkel BA, Shapiro-Ilan DI, Campbell JF, Lewis EE (2006) Effect of Steinernema glaseri infected host exudates on movement of conspecific infective juveniles. J Invertebr Pathol 93:42–49
Lee DL (2002) Behaviour. In: Lee DL (ed) The biology of nematodes. Taylor and Francis, London, UK, pp 369–387
Lewis EE, Gaugler R (1994) Entomopathogenic nematode (Rhabdita: Steinernematidae) sex ratio relates to foraging strategy. J Invertebr Pathol 64:238–242
Lewis EE, Gaugler R, Harrison R (1992) Entomopathogenic nematode host finding: response to host contact cues by cruise and ambush foragers. Parasitology 105:309–315
Lewis EE, Gaugler R, Harrison R (1993) Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) in host volatile cues. Can J Zool 71:765–769
Lewis EE, Grewal PS, Gaugler R (1995) Hierarchical order of host cues in parasite foraging: a question of context. Parasitology 110:207–213
Lewis EE, Ricci M, Gaugler R (1996) Host recognition behaviour predicts host suitability in the entomopathogenic nematode Steinernema carpocapsae. (Rhabditida: Steinernematidae). Parasitology 113:573–579
Lewis EE, Campbell JF, Gaugler R (1997) The effects of ageing on the foraging behaviour of Steinernema carpocapsae (Rhabditida: Steinernematidae). Nematologica 43:355–362
Lewis EE, Barbarosa B, Gaugler R (2002) Mating and sexual communication by Steinernema carpocapsae (Nemata: Steinernematidae). J Nematol 34:328–331
Lewis EE, Campbell JF, Griffin C, Kaya HK, Peters A (2006) Behavioral ecology of entomopathogenic nematodes. Biol Control 38:66–79
Mitani DK, Kaya HK, Goodrich-Blair H (2004) Comparative study of the entomopathogenic nematode, Steinernema carpocapsae, reared on mutant and wild-type Xenorhabdus nematophila. Biol Control 29:382–391
Molyneux AS (1983) The biology and ecology of the entomopathogenic nematodes, Heterorhabditis spp. (Heterorhabditidae) and Steinernema spp. (Steinernematidae). Unspecified thesis, University of Tasmania
Morton A, García-Del-Pino F (2009) Ecological characterization of entomopathogenic nematodes isolated in stone fruit orchard soils of Mediterranean areas. J Invertebr Pathol 102:203–213
Mracek Z, Becvar S, Kindlmann P (1999) Survey of entomopathogenic nematodes from the families Steinernematidae and Heterorhabditidae (Nematoda: Rhabditida) in the Czech Republic. Folia Parasitol 46:145–148
Neves JM, Simoes N, Mota M (1998) Evidence for a sex pheromone in Steinernema carpocapsae. Nematologica 44:95–98
Perez EE, Lewis EE, Shapiro-Ilan DI (2003) Impact of the host cadaver on survival and infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) under desiccating conditions. J Invertebr Pathol 82:111–118
Puza V, Mracek Z (2010) Does scavenging extend the host range of entomopathogenic nematodes (Nematoda: Steinernematidae)? J Invertebr Pathol 104:1–3
Ramos-Rodriguez O, Campbell JF, Christen JM, Shapiro-Ilan DI, Lewis EE, Ramaswamy SB (2007a) Attraction behaviour of three entomopathogenic nematode species towards infected and uninfected hosts. Parasitology 134:729–738
Ramos-Rodriguez O, Campbell JF, Lewis EE, Shapiro-Ilan DI, Ramaswamy SB (2007b) Dynamics of carbon dioxide release from insects infected with entomopathogenic nematodes. J Invertebr Pathol 94:64–69
Reed EM, Wallace HR (1965) Leaping locomotion in an insect parasitic nematode. Nature 206:210–211
Ryder JJ, Griffin CT (2002) Density dependent fecundity and infective juvenile production in the entomopathogenic nematode, Heterorhabditis megidis. Parasitology 125:83–92
San-Blas E, Gowen SR (2008) Facultative scavenging as a survival strategy of entomopathogenic nematodes. Int J Parasitol 38:85–91
Sankaranarayanan C, Askary TH (2017) Status of entomopathogenic nematodes in integrated pest management strategies in India. In: Abd-Elgawad MMM, Askary TH, Coupland J (eds) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CAB International, Wallingford, UK, pp 362–382
Selvan S, Campbell JF, Gaugler R (1993) Density-dependent effects on entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) within an insect host. J Invertebr Pathol 62:278–284
Shishiniova M, Budurova I, Gradinarov D (1997) Contribution to fauna of entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae) from Bulgaria. Biotechnol Biotechnol Equip 11:45–52
Steiner WA (1996) Distribution of entomopathogenic nematodes in the Swiss Alps. Rev Suisse Zool 103:439–452
Strauch O, Stoessel S, Ehlers R-U (1994) Culture conditions define automictic or amphimictic reproduction in entomopathogenic rhabditid nematodes of the genus Heterorhabditis. Fundam Appl Nematol 17:573–582
Stuart RJ, Gaugler R (1994) Patchiness in populations of entomopathogenic nematodes. J Invertebr Pathol 64:39–45
Susurluk J (2008) Potential of the entomopathogenic nematodes Steinernema feltiae, S. weiseri and Heterorhabditis bacteriophora for the biological control of the sugar beet weevil Bothynoderes punctiventris (Coleoptera: Curculionidae). J Pest Sci 81:221–225
Timmermeyer N, Gerlach T, Guempel C, Knoche J, Pfann JF, Schliessmann D, Michaels NK (2010) The function of copulatory plugs in Caenorhabditis remanei: hints for female benefits. Front Zool 7:28
Woodring JL, Kaya HK (1988) Steinernematid and Heterorhabditid nematodes: a hand book of biology and techniques. Southern Cooperative Series Bulletin 331, Arkansas Agricultural Experimental Station, Fayetteville, Arkansas, pp 1–30
Zhou XS, Kaya HK, Heungens K, Goodrich-Blair H (2002) Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Appl Environ Microbiol 68:6202–6209
Acknowledgements
This work was supported in part by All India Coordinated Research Project (AICRP), ICAR on Biological Control of Crop Pests and Weeds running in the Biological Control Laboratory, Division of Entomology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir (SKUAST-K), Srinagar, Jammu and Kashmir, India.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Askary, T.H., Jamal Ahmad, M., Wani, A.R., Mohiddin, S., Sofi, M.A. (2018). Behavioural Ecology of Entomopathogenic Nematodes, Steinernema and Heterorhabditis for Insect Biocontrol. In: Lichtfouse, E. (eds) Sustainable Agriculture Reviews 31. Sustainable Agriculture Reviews, vol 31. Springer, Cham. https://doi.org/10.1007/978-3-319-94232-2_8
Download citation
DOI: https://doi.org/10.1007/978-3-319-94232-2_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-94231-5
Online ISBN: 978-3-319-94232-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)