Abstract
Combinations of entomopathogenic nematode (EPN) species are sometimes more or less effective than individual species for the management of insect pests. We hypothesized that these outcomes are due in part to dispersal rates that differ when EPN species are conspecific or heterospecific. Dispersal rates of three heterorhabditid species, six steinernematid species, and mixtures of some were assessed using image analysis of nematodes on water agar. The dispersal rates between the genera differed significantly and were unrelated to the estimated body mass or the putative foraging strategy, including that of the recently named Steinernema khuongi, characterized here as a cruise forager (actively search for hosts). Heterorhabditis indica dispersed more rapidly on agar when combined with S. diaprepesi, but not with S. glaseri. The presence of S. diaprepesi in soil microcosms also increased the proximity of H. indica to Galleria mellonella host insects, while H. indica presence reduced the number of G. mellonella killed by S. diaprepesi. Nevertheless, increasing the H. indica dispersal rate did not increase its insecticidal effectiveness, likely due to competition with the more virulent S. diaprepesi. Rather, the effect of combining the species on the mortality of G. mellonella was additive. Our results suggest that interspecific EPN communication affects not only orientation but also dispersal rate, with potential impacts on biological control and the subsequent fitness of each species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andrássy L (1956) Die rauminhalst and gewichtsbestimmung der fadenwurmer (Nematoden). Acta Zool Acad Sci Hungary 2:1–15
Bashey F, Hawlena H, Lively CM (2013) Alternative paths to success in a parasite community: Within-host competition can favor higher virulence or direct interference. Evolution 67:900–907. https://doi.org/10.1111/j.1558-5646.2012.01825.x
Campbell JF, Gaugler YR (1997) Inter-specifie variation in entomopathogenic nematode foraging strategy: Dichotomy or variation along a continuum? Fundam Appl Nematol 20:393–398. https://doi.org/10.1056/NEJMra1602113
Campbell JF, Lewis EE, Stock SP et al (2003) Evolution of host search strategies in entomopathogenic nematodes. J Nematol 35:142–145
Campos-Herrera R, Jaffuel G, Chiriboga X et al (2015) Traditional and molecular detection methods reveal intense interguild competition and other multitrophic interactions associated with native entomopathogenic nematodes in Swiss tillage soils. Plant Soil 389:237–255. https://doi.org/10.1007/s11104-014-2358-4
Campos-Herrera R, Johnson EG, EL-Borai FE, et al (2011) Long-term stability of entomopathogenic nematode spatial patterns in soil as measured by sentinel insects and real-time PCR assays. Ann Appl Biol 158:55–68. https://doi.org/10.1111/j.1744-7348.2010.00433.x
Campos-Herrera R, Stuart RJ, Pathak E et al (2019) Temporal patterns of entomopathogenic nematodes in Florida citrus orchards: evidence of natural regulation by microorganisms and nematode competitors. Soil Biol Biochem 128:193–204. https://doi.org/10.1016/J.SOILBIO.2018.10.012
Chang DZ, Serra L, Lu D et al (2019) A core set of venom proteins is released by entomopathogenic nematodes in the genus Steinernema. PLOS Pathog 15:e1007626. https://doi.org/10.1371/JOURNAL.PPAT.1007626
Choe A, Von Reuss SH, Kogan D et al (2012) Ascaroside signaling is widely conserved among nematodes. Curr Biol 22:772–780. https://doi.org/10.1016/j.cub.2012.03.024
Demir S, Karagoz M, Hazir S, Kaya HK (2015) Evaluation of entomopathogenic nematodes and their combined application against Curculio elephas and Polyphylla fullo larvae. J Pest Sci 88:163–170. https://doi.org/10.1007/s10340-014-0571-9
Duncan LW, Graham JH, Zellers J et al (2007) Food web responses to augmenting the entomopathogenic nematodes in bare and animal manure-mulched soil. J Nematol 39:176–189
Dutka A, McNulty A, Williamson SM (2015) A new threat to bees? Entomopathogenic nematodes used in biological pest control cause rapid mortality in Bombus terrestris. PeerJ 3:e1413. https://doi.org/10.7717/PEERJ.1413
Edison AS (2009) Caenorhabditis elegans pheromones regulate multiple complex behaviors. Curr Opin Neurobiol 19:378–388. https://doi.org/10.1016/J.CONB.2009.07.007
El-Borai FE, Campos-Herrera R, Stuart RJ, Duncan LW (2011) Substrate modulation, group effects and the behavioral responses of entomopathogenic nematodes to nematophagous fungi. J Invertebr Pathol 106:347–356. https://doi.org/10.1016/J.JIP.2010.12.001
El-Borai FE, Stuart RJ, Campos-Herrera R et al (2012) Entomopathogenic nematodes, root weevil larvae, and dynamic interactions among soil texture, plant growth, herbivory, and predation. J Invertebr Pathol 109:134–142. https://doi.org/10.1016/J.JIP.2011.10.012
Galef BG, Laland KN (2005) Social learning in animals: empirical studies and theoretical models. Bioscience 55:489–499. https://doi.org/10.1641/0006-3568
Gaugler R, Lewis E (1997) Stuart RJ (1997) Ecology in the service of biological control: the case of entomopathogenic nematodes. Oecologia 1094(109):483–489. https://doi.org/10.1007/S004420050108
Griffin CT (2015) Behaviour and population dynamics of entomopathogenic nematodes following application. In: Nematode Pathogenesis of Insects and Other Pests: ecology and applied technologies for sustainable plant and crop protection. Springer: Berlin, Germany, pp 57–95. ISBN: 9783319182667
Hartley CJ, Lillis PE, Owens RA, Griffin CT (2019) Infective juveniles of entomopathogenic nematodes (Steinernema and Heterorhabditis) secrete ascarosides and respond to interspecific dispersal signals. J Invertebr Pathol 168:107257. https://doi.org/10.1016/j.jip.2019.107257
Hawlena H, Bashey F, Mendes-Soares H, Lively CM (2010) Natural history note: spiteful interactions in a natural population of the bacterium Xenorhabdus bovienii. Am Nat 175:374–381. https://doi.org/10.1086/650375
Heve WK, El-Borai FE, Carrillo D, Duncan LW (2018) Increasing entomopathogenic nematode biodiversity reduces efficacy against the Caribbean fruit fly Anastrepha suspensa: interaction with the parasitoid Diachasmimorpha longicaudata. J Pest Sci 91:799–813. https://doi.org/10.1007/s10340-017-0942-0
Holladay BH, Willett DS, Stelinski LL (2016) High throughput nematode counting with automated image processing. Biocontrol 61:177–183. https://doi.org/10.1007/s10526-015-9703-2
Jabbour R, Crowder DW, Aultman EA, Snyder WE (2011) Entomopathogen biodiversity increases host mortality. Biol Control 59:277–283. https://doi.org/10.1016/j.biocontrol.2011.07.016
Jenkins WR (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis Rep 48:492
Kaplan F, Alborn HT, von Reuss SH et al (2012) Interspecific nematode signals regulate dispersal behavior. PLoS ONE 7:e38735. https://doi.org/10.1371/journal.pone.0038735
Kaplan F, Perret-Gentil A, Giurintano J et al (2020) Conspecific and heterospecific pheromones stimulate dispersal of entomopathogenic nematodes during quiescence. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-62817-y
Kaya HK, Koppenhöfer AM (1996) Effects of microbial and other antagonistic organism and competition on entomopathogenic nematodes. Biocontrol Sci Technol 6:357–372. https://doi.org/10.1080/09583159631334
Koppenhöfer AM, Kaya HK (1996) Coexistence of two steinernematid nematode species (Rhabditida: Steinernematidae) in the presence of two host species. Appl Soil Ecol 4:221–230. https://doi.org/10.1016/S0929-1393(96)00121-7
Koppenhöfer AM, Kaya HK, Shanmugam S, Wood GL (1995) Interspecific competition between steinernematid nematodes within an insect host. J Invertebr Pathol 66:99–103. https://doi.org/10.1006/JIPA.1995.1070
Manohar M, Tenjo-Castano F, Chen S et al (2020) Plant metabolism of nematode pheromones mediates plant-nematode interactions. Nat Commun 11:208. https://doi.org/10.1038/s41467-019-14104-2
Millar LC, Barbercheck ME (2001) Interaction between endemic and introduced entomopathogenic nematodes in conventional-till and no-till corn. Biol Control 22:235–245. https://doi.org/10.1006/BCON.2001.0978
Morrill A, Forbes MR (2016) Aggregation of infective stages of parasites as an adaptation and its implications for the study of parasite-host interactions. Am Nat 187:225–235. https://doi.org/10.1086/684508
Neumann G, Shields EJ (2008) Multiple-species natural enemy approach for biological control of alfalfa snout beetle (Coleoptera: Curculionidae) using entomopathogenic nematodes. J Econ Entomol 101:1533–1539. https://doi.org/10.1093/jee/101.5.1533
Nishimatsu T, Jackson JJ (1998) Interaction of insecticides, entomopathogenic nematodes, and larvae of the western corn rootworm (Coleoptera: Chrysomelidae). J Econ Entomol 91:410–418. https://doi.org/10.1093/jee/91.2.410
O’Callaghan KM, Zenner ANRL, Hartley CJ, Griffin CT (2014) Interference competition in entomopathogenic nematodes: Male Steinernema kill members of their own and other species. Int J Parasitol 44:1009–1017. https://doi.org/10.1016/j.ijpara.2014.07.004
Oliveira-Hofman C, Kaplan F, Stevens G et al (2019) Pheromone extracts act as boosters for entomopathogenic nematodes efficacy. J Invertebr Pathol 164:38–42. https://doi.org/10.1016/j.jip.2019.04.008
Shapiro-Ilan DI, Kaplan F, Oliveira-Hofman C et al (2019) Conspecific pheromone extracts enhance entomopathogenic infectivity. J Nematol 51:1–5. https://doi.org/10.21307/jofnem-2019-082
Shapiro-Ilan DI, Lewis EE, Schliekelman P (2014) Aggregative group behavior in insect parasitic nematode dispersal. Int J Parasitol 44:49–54. https://doi.org/10.1016/J.IJPARA.2013.10.002
Stock SP, Campos-Herrera R, El-Borai FE, Duncan LW (2018) Steinernema khuongi n. sp. (Panagrolaimomorpha, Steinernematidae), a new entomopathogenic nematode species from Florida, USA. J Helminthol. https://doi.org/10.1017/S0022149X18000081
White GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66:302–303. https://doi.org/10.1126/science.66.1709.302-a
Willett DS, Alborn HT, Duncan LW, Stelinski LL (2015) Social networks of educated nematodes. Sci Rep 5:14388. https://doi.org/10.1038/srep14388
Willett DS, Alborn HT, Stelinski LL, Shapiro-Ilan DI (2018) Risk taking of educated nematodes. PLoS ONE 13:e0205804. https://doi.org/10.1371/journal.pone.0205804
Acknowledgements
Sheng-Yen Wu expresses his appreciation to the authorities of CREC-UF/IFAS (in Lake Alfred FL, USA) for providing research facilities during his post-doctoral studies and thank Professor Youming Hou for his support in the Fujian Agriculture and Forestry University. We thank Dr. Denis Willett and Dr. Camila Filgueiras for their valuable technical assistance.
Funding
This work was supported by the International Cooperation Project of Fujian Province (2021I0006), the Strait Postdoctoral Foundation of Fujian Province (2021A001), and the US-Egypt Project cycle 17 (no. 172). This article is derived from the Subject Data funded in part by NAS and USAID, and that any opinions, findings, conclusions, or recommendations expressed in it are those of the author alone, and do not necessarily reflect the views of USAID or NAS.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Additional information
Communicated by Aurelio Ciancio.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wu, SY., Duncan, L.W. Entomopathogenic nematode species combinations alter rates of dispersal, host encounter and insecticidal efficiency. J Pest Sci 95, 1111–1119 (2022). https://doi.org/10.1007/s10340-021-01475-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01475-z