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Stress avoidance: vertical movement of entomopathogenic nematodes in response to soil moisture gradient

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Abstract

Survival of entomopathogenic nematodes (EPNs) in soils is attributed to their entering a dormant state—anhydrobiosis—as soil moisture decreases, but EPNs with poor desiccation tolerance and low anhydrobiotic capabilities may practice desiccation avoidance. We compared the effect of soil moisture gradient on downward movement of the highly desiccation-tolerant Steinernema carpocapsae and the poorly desiccation-tolerant Heterorhabditis bacteriophora. Infective juveniles (IJs) were applied to the surface of moist (11–13% w/w moisture) sandy soil in buckets. Nematode distribution was monitored at different depths 3, 14 and 28 days after application. In uncovered buckets, soil moisture decreased to 1% in the upper 5-cm layer after 28 days. H. bacteriophora IJs abandoned the upper soil layers as dryness intensified with >80% found in the bottom (20–25 cm) layer. In contrast, >70% S. carpocapsae IJs remained in the upper layer. In covered buckets, with 10% moisture throughout the experiment, heterorhabditid IJs were equally distributed between the 10–15 cm and 20–25 cm layers; only 7% remained in the upper layer. Again, >70% S. carpocapsae IJs remained in the upper layer throughout. Soil type influenced H. bacteriophora IJs' downward migration. In sandy and sandy loam soils, with rapid evaporation, >80% IJs were in the bottom layer 14 and 28 days after application. In the loam soil, with higher moisture retention, >75% IJs remained in the 10–15 cm layer and <20% migrated to the bottom. Results provide initial evidence of a possible stress-avoidance strategy in H. bacteriophora under natural conditions.

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References

  • Alekseev, E., Glazer, I., & Samish, M. (2006). Effect of soil texture and moisture on the activity of entomopathogenic nematodes against female Boophilus annulatus ticks. BioControl, 51, 507–518.

    Article  Google Scholar 

  • Ali, J. G., Alborn, T. H., Campos-Herrera, R., Kaplan, F., Duncan, W. L., Rodriguez-Saona, C., Koppenhofer, M. A., & Stelinski, L. L. (2012). Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. PLoS ONE, 7, e38146.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ali, J. G., Campos-Herrera, Alborn, T. H., Duncan, W. L., & Stelinski, L. L. (2013). Sending mixed messages: A trophic cascade produced by a belowground herbivore-induced cue. Journal of Chemical Ecology, 39, 1140–1147.

    Article  CAS  PubMed  Google Scholar 

  • Bal, K. H., Taylor, A. J. R., & Grewal, S. P. (2014). Ambush Foraging Entomopathogenic Nematodes Employ ‘Sprinters' for Long-Distance Dispersal in the Absence of Hosts. Journal of Parasitology, 100, 422–432.

    Article  PubMed  Google Scholar 

  • Cooper, A. F., Jr., & Van Gundy, S. D. (1971). Senescence, quiescence and cryptobiosis. In B. M. Zuckerman, W. F. Mai, & R. A. Rohde (Eds.), Plant parasitic nematodes, Vol. II (pp. 297–318). New York and London: Academic Press.

    Google Scholar 

  • Dillman, A. R., Chaston, J. M., Adams, B. J., Ciche, T. A., Goodrich-Blair, H., Stock, S. P., & Sternberg, P. W. (2012). An entomopathogenic nematode by any other name. PLoS Pathogens, 8, e1002527.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Duncan, L. W., & McCoy, C. W. (1996). Vertical distribution in soil, persistence, and efficacy against citrus root weevil (Coleoptera: Curculionidae) of two species of entomopathogenic nematodes (Rhabditida: Steinernematidae; Heterorhabditidae). Environmental Entomology, 25, 174–178.

    Article  Google Scholar 

  • Efron, D., Nestel, D., & Glazer, I. (2001). Spatial analysis of entomopathogenic nematodes and insect hosts in a citrus grove in a semi-arid region in Israel. Environmental Entomology, 30, 254–261.

    Article  Google Scholar 

  • Ehlers, R.-U. (2001). Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology, 56, 623–633.

    Article  CAS  PubMed  Google Scholar 

  • Ennis, D. E., Dillon, A. B., & Griffin, C. T. (2010). Simulated roots and host feeding enhance infection of subterranean insects by the entomopathogenic nematode Steinernema carpocapsae. Journal of Invertebrate Pathology. doi:10.1016/j.jip.2009.11.004.

    Google Scholar 

  • Epsky, N. D., Walter, E. D., & Capinera, L. J. (1988). Potential role of nematophagous microarthropods as biotic mortality factors of entomogenous nematodes (Rhabditida: Steinernematidae, Heterorhabditidae). Journal of Economic Entomology, 81, 821–825.

    Article  Google Scholar 

  • Georgis, R., & Poinar, O. G., Jr. (1983). Effect of soil texture on the distribution and infectivity of Neoaplectana carpocapsae (Nematode: Steinernematidae). Journal of Nematology, 15, 308–311.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Glazer, I. (1992). Survival and efficacy of Steinernema carpocapsae in an exposed environment. Biocontrol Science and Technology, 2, 101–107.

    Article  Google Scholar 

  • Glazer, I. (2002). Survival biology. In R. Gaugler (Ed.), Entomopathogenic nematology (pp. 169–187). Oxon, UK: CABI Publishing.

    Chapter  Google Scholar 

  • Glazer, I., Liran, N., & Steinberger, Y. (1991). A survey of entomopathogenic nematodes (Rhabditida) in the Negev desert. Phytoparasitica, 19, 291–300.

    Article  Google Scholar 

  • Gouge, H. D., Smith, A. K., Lee, L. L., & Henneberry, J. T. (2000). Effect of soil depth and moisture on the vertical distribution of Steinernema riobrave (Nematoda: Steinernematidae). Journal of Nematology, 32, 223–228.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grewal, P. S., Ehlers, R.-U., & Shapiro-Ilan, D. I. (2005). Nematodes as biocontrol agents. Wallingford, UK: CABI Publishing.

    Book  Google Scholar 

  • Grewal, P. S., Selvan, S., Lewis, E. E., & Gaugler, R. (1993). Male insect-parasitic nematodes: A colonizing sex. Experientia, 49, 605–608.

    Article  Google Scholar 

  • Hiltpold, I., Erb, M., Robert, A. M. C., & Turlings, C. J. T. (2011). Systemic root signaling in a belowground, volatile-mediated tritrophic interaction. Plant, Cell and Environment, 34, 1267–1275.

    Article  CAS  PubMed  Google Scholar 

  • Hiltpold, I., Jaffuel, G., & Turlings, C. J. T. (2015). The dual effects of root-cap exudates on nematodes: From quiescence in plant-parasitic nematodes to frenzy in entomopathogenic nematodes. Journal of Experimental Botany, 66, 603–611.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ishibashi, N., Tojo, S., & Hatate, H. (1987). Desiccation survival of Steinernema feltiae str. DD-136 and possible desiccation protectants for foliage application of nematodes. In N. Ishibashi (Ed.), Recent advances in biological control of insect pests by entomogenous nematodes in Japan (pp. 139–144). Japan: Ministry of Education.

    Google Scholar 

  • Jabbour, R., & Barbercheck, M. C. (2008). Soil and habitat complexity effects on movement of the entomopathogenic nematode Steinernema carpocapsae in maize. Biological Control, 47, 235–243.

    Article  Google Scholar 

  • Kaya, H. K. (1990). Soil ecology. In R. Gaugler & H. K. Kaya (Eds.), Entomopathogenic nematodes in biological control (pp. 93–115). Boca Raton, FL: CRC Press.

    Google Scholar 

  • Kaya, H. K., & Gaugler, R. (1993). Entomopathogenic nematodes. Annual Review of Entomology, 38, 181–206.

    Article  Google Scholar 

  • Kaya, H. K., & Stock, S. P. (1997). Techniques in insect nematology. In L. Lacey (Ed.), Manual of techniques in insect pathology (pp. 281–324). San Diego, CA: Academic Press.

    Chapter  Google Scholar 

  • Koppenhöfer, M. A., Kaya, K. H., & Taormino, P. S. (1995). Infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae) at different soil depths and moistures. Journal of Invertebrate Pathology, 65, 193–199.

    Article  Google Scholar 

  • Kruitbos, L. M., Heritage, S. E., Hapca, S., & Wilson, M. J. (2010). The influence of habitat quality on the foraging strategies of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidis. Parasitology, 137, 303–309.

    Article  CAS  PubMed  Google Scholar 

  • Kung, S. P., & Gaugler, R. (1990). Soil type and entomopathogenic nematode persistence. Journal of Invertebrate Pathology, 55, 401–406.

    Article  Google Scholar 

  • Kung, S. P., Gaugler, R., & Kaya, H. K. (1990). Influence of soil pH and oxygen on entomopathogenic nematode persistence. Journal of Nematology, 22, 440–445.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kung, S. P., Gaugler, R., & Kaya, H. K. (1991). Effects of soil temperature, moisture and relative humidity on entomopathogenic nematode persistence. Journal of Invertebrate Pathology, 57, 242–249.

    Article  Google Scholar 

  • Lacey, L., & Georgis, R. (2012). Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44, 218–225.

    PubMed Central  PubMed  Google Scholar 

  • Lewis, E. E. (2002). Behavioral ecology. In R. Gaugler (Ed.), Entomopathogenic nematology (pp. 205–224). Wallingford, UK: CABI Publishing.

    Chapter  Google Scholar 

  • Lewis, E. E., Gaugler, R., & Harrison, R. (1992). Entomopathogenic nematode host finding: Response to host contact cues by cruise and ambusher foragers. Parasitology, 105, 109–115.

    Article  Google Scholar 

  • Liu, Q.-Z., & Glazer, I. (2000). Factors affecting desiccation survival of the entomopathogenic nematodes, Heterorhabditis bacteriophora HP88. Phytoparasitica, 28, 331–340.

    Article  Google Scholar 

  • Liu, Q.-Z., Piggott, S. J., Solomon, A., & Glazer, I. (2002). Physiological and biochemical changes in nematodes from the genus Heterorhabditis following desiccation. Phytoparasitica, 30, 253–261.

    CAS  Google Scholar 

  • Molyneux, A. S., & Bedding, A. R. (1984). Influence of soil texture and moisture on the infectivity of Heterorhabditis sp. D1 and Steinernema glaseri for larvae of the sheep blowfly, Lucilia cuprina. Nematologica, 30, 358–365.

    Article  Google Scholar 

  • Portillo-Aguilar, C., Villani, G. M., Tauber, J. M., Tauber, A. C., & Nyrop, P. J. (1999). Entomopathogenic nematode (Rhabditida: Heterorhabditidae and Steinernematidae) response to soil texture and bulk density. Environmental Entomology, 28, 1021–1035.

    Article  Google Scholar 

  • Rasmann, S., Kollner, G. T., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., & Turlings, C. J. T. (2005). Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434, 732–737.

    Article  CAS  PubMed  Google Scholar 

  • Russell, J., Vidal-Gadea, G. A., Makay, A., Lanam, C., & Pierce-Shimomura, T. J. (2014). Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans. Proceedings of National Academy of Sciences, 111, 8269–8274.

    Article  CAS  Google Scholar 

  • Shapiro-Ilan, D., Han, R., & Qiu, X. (2014). Production of entomopathogenic nematodes. In J. Morales-Ramos, G. Rojas, & D. I. Shapiro-Ilan (Eds.), Mass Production of Beneficial Organisms: Invertebrates and Entomopathogens (pp. 321–356). Amsterdam: Academic Press.

    Chapter  Google Scholar 

  • Simons, W. R., & Poinar, G. O., Jr. (1973). The ability of Neoaplectana carpocapsae (Steinernematidae: Nematodea) to survive extended periods of desiccation. Journal of Invertebrate Pathology, 22, 228–230.

    Article  Google Scholar 

  • Solomon, A., Paperna, I., & Glazer, I. (1999). Induction of anhydrobiosis on the entomopathogenic nematodes Steinernema feltiae. Nematology, 1, 61–68.

    Article  CAS  Google Scholar 

  • Surrey, M. R., & Wharton, D. A. (1995). Desiccation survival of the infective larvae of the insect parasitic nematode, Heterorhabditis zealandica Poinar. International Journal of Parasitology, 25, 749–752.

    Article  CAS  PubMed  Google Scholar 

  • Westerman, P. R. (1992). The influence of time of storage on performance of the insect parasitic nematode, Heterorhabditis sp. Fundamental and Applied Nematology, 15, 407–412.

    Google Scholar 

  • Wilson, J. M., Ehlers, R.-U., & Glazer, I. (2012). Entomopathogenic nematode foraging strategies—Is Steinernema carpocapsae really an ambush forager? Nematology, 14, 389–394.

    Article  Google Scholar 

  • Womersley, C. Z. (1990). Dehydration survival and anhydrobiotic potential. In R. Gaugler & H. K. Kaya (Eds.), Entomopathogenic nematodes in biological control (pp. 117–137). Boca Raton, FL: CRC Press.

    Google Scholar 

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Salame, L., Glazer, I. Stress avoidance: vertical movement of entomopathogenic nematodes in response to soil moisture gradient. Phytoparasitica 43, 647–655 (2015). https://doi.org/10.1007/s12600-015-0488-8

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