Research Article
Response of Rattus norvegicus (Berkenhout, 1769) (Rodentia: Muridae) to entomopathogenic bacteria infected insect cadavers
Abstract
Xenorhabdus Thomas & Poinar (Enterobacterales: Morganellaceae) and Photorhabdus Thomas & Poinar (Enterobacterales: Morganellaceae) bacteria are mutualistically associated with Steinernema Travassos, 1927 (Rhabditida: Steinernematidae) and Heterorhabditis Poinar, 1976 (Rhabditida: Heterorhabditidae) nematodes, respectively, and are known to produce several secondary metabolites that protect nematode-killed insects from different competitors. One of these compounds called “the scavenger deterrent factor” (SDF) is known to deter different arthropod, bird, and fish species from feeding on insects killed by Xenorhabdus or Photorhabdus bacteria. The effects of SDF from five different Xenorhabdus and one Photorhabdus species against the Norway rat, Rattus norvegicus (Berkenhout, 1769) (Rodentia: Muridae) were investigated using either a one-choice or two-choice experimental design during 2019-2020 in Aydın Adnan Menderes University. Rats were given four-day-old bacteria-killed Galleria mellonella (L., 1758) (Lepidoptera: Pyralidae) larvae and feeding behavior was observed and recorded. The results demonstrate that the Norway rat is deterred from feeding on insects killed by certain Xenorhabdus and Photorhabdus species and it is likely due to the distastefulness of these cadavers. Ecologically, the data suggest that insects killed by the entomopathogenic nematode/bacterium complex in nature may be protected from attack from insectivorous mammals, especially those that feed on soil-dwelling insects.
Supporting Institution
Aydın Adnan Menderes Üniversitesi, The Scientific and Technological Research Council of Türkiye (TÜBİTAK-KBAG)
Project Number
Aydın Adnan Menderes Üniversitesi FEF-20002, TÜBİTAK-KBAG 116Z074
Thanks
This study was supported by Aydın Adnan Menderes University (Project Number: FEF-20002) and The Scientific and Technological Research Council of Türkiye (TÜBİTAK–KBAG Project Number: 116Z074). I thank Dr. Asude Gülçe Oryaşın for her assistance and Dr. Harry K. Kaya for his comments on the manuscript.
References
- Baur, M. E., H. K. Kaya & D. R. Strong, 1998. Foraging ants as scavengers on entomopathogenic nematode killed insects. Biological Control, 12 (3): 231-236.
- Bode, H. B., 2009. Entomopathogenic bacteria as a source of secondary metabolites. Current Opinion in Chemical Biology, 13 (2): 224-230.
- Boemare, N. E., 2002. “Biology, Taxonomy and Systematics of Photorhabdus and Xenorhabdus, 35-56”. In: Entomopathogenic Nematology (Eds. R. Gaugler). CABI Publishing Wallingford, UK, 388 pp.
- Çimen, H., M. Touray, Ş. H. Gülşen, Ö. Erincik, S. L. Wenski, H. B. Bode, D. I. Shapiro-Ilan & S. Hazır, 2021. Antifungal activity of different Xenorhabdus and Photorhabdus species against various fungal phytopathogens and identification of the antifungal compounds from X. szentirmaii. Applied Microbiology and Biotechnology, 105 (13): 5517-5528.
- Fenton, A., L. Magoolagan, Z. Kennedy & K. A. Spencer, 2011. Parasite-induced warning coloration: a novel form of host manipulation. Animal Behaviour, 81 (2): 417-422.
- Ffrench-Constant, R. H. & D. J. Bowen, 2000. Novel insecticidal toxins from nematode-symbiotic bacteria. Cellular and Molecular Life Sciences, 57 (5): 828-833.
- Gaugler, R. & H. K. Kaya, 1990. Entomopathogenic Nematodes in Biological Control. CRC Press Boca Raton, FL, USA, 381 pp.
- Gómez Villafañe, I. E., F. Miñarro, M. Ribicich, C. A. Rossetti, D. Rossotti & M. Busch, 2004. Assessment of the risks of rats (Rattus norvegicus) and opossums (Didelphis albiventris) in different poultry-rearing areas in Argentina. Brazilian Journal of Microbiology, 35 (4): 359-363.
- Gülcü, B., H. Çimen, R. K. Raja & S. Hazır, 2017. Entomopathogenic nematodes and their mutualistic bacteria: Their ecology and application as microbial control agents. Biopesticides International, 13 (2): 79-112.
- Gülcü, B., S. Hazır & H. K. Kaya, 2012. Scavenger deterrent factor (SDF) from symbiotic bacteria of entomopathogenic nematodes. Journal of Invertebrate Pathology, 110 (3): 326-333.
- Gülcü, B., S. Hazır, E. E. Lewis & H. K. Kaya, 2018. Evaluation of responses of different ant species (Formicidae) to the scavenger deterrent factor associated with the entomopathogenic nematode-bacterium complex. European Journal of Entomology, 115 (1): 312-317.
- Gulzar, S., M. Usman, W. Wakil, B. Gülcü, C. Hazır, M. Karagöz, S. Hazır & D. I. Shapiro-Ilan, 2020. Environmental tolerance of entomopathogenic nematodes differs among nematodes arising from host cadavers versus aqueous suspension. Journal of Invertebrate Pathology, 175: 107452 (1-7).
- Han, R. & R.U. Ehlers, 2000. Pathogenicity, development and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. Journal of Invertebrate Pathology, 75 (1): 55-58.
- Hazır, S., D. I. Shapiro-Ilan, C. H. Bock, C. Hazır, L. G. Leite & M. W. Hotchkiss, 2016. Relative potency of culture supernatants of Xenorhabdus and Photorhabdus spp. on growth of some fungal phytopathogens. European Journal of Plant Pathology, 146 (2016): 369-381.
- Hazır, S., H. K. Kaya, M. Touray, H. Çimen & D. I. Shapiro-Ilan, 2022. Basic laboratory and field manual for conducting research with the entomopathogenic nematodes, Steinernema and Heterorhabditis, and their bacterial symbionts. Turkish Journal of Zoology, 46 (4): 305-350.
- Hazır, S., N. Keskin, N., S. P. Stock, H. K. Kaya & S. Özcan, 2003. Diversity and distribution of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Turkey. Biodiversity and Conservation, 12 (2): 375-386.
- Jaffuel, G., S. Krishnamani, R. A. R. Machado, R. Campos-Herrera & T. C. J. Turlings, 2021. Potent Ant Deterrents Emitted from Nematode-Infected Insect Cadavers. Journal of Chemical Ecology, 48 (2021): 71-78.
- Jones, R. S., A. Fenton, & M. P. Speed, 2016. "Parasite-induced aposematism" protects entomopathogenic nematode parasites against invertebrate enemies. Behavioral Ecology, 27 (2): 645-651.
- Jones, R. S., A. Fenton, A., M. P. Speed, & J. Mappes, 2017. Investment in multiple defences protects a nematode-bacterium symbiosis from predation. Animal Behaviour, 129 (12): 1-8.
- Kaya, H. K. & P. Stock, 1997. “Techniques in Insect Nematology, 282-324”. In: Manual of Techniques in Insect Pathology (Eds. L. A. Lacey). Academic Press, San Diego, 409 pp.
- Kaya, H. K., A. M. Koppenhöfer, & M. W. Johnson, 1998. Natural enemies of entomopathogenic nematodes. Japanese Journal of Nematology, 28 (supplement): 13-21.
- Marples, N. M. & D. J. Kelly, 1999. Neophobia and dietary conservatism: Two distinct processes? Evolutionary Ecology, 3 (7-8): 641-653.
- Marples, N. M., T. J. Roper & D. G. C. Harper, 1998. Responses of wild birds to novel prey: Evidence of dietary conservatism. Oikos, 83 (1): 161-165.
- Mertz, N. R., E. J. G. Agudelo, F. S. Sales & A. Moino Junior, 2015. Effects of entomopathogenic nematodes on the predator Calosoma granulatum in the laboratory. Journal of Insect Behavior, 28 (3): 312-327.
- Perez, E. E., E. E. Lewis & D. I. Shapiro-Ilan, 2003. Impact of the host cadaver on survival and infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) under desiccating conditions. Journal of Invertebrate Pathology, 82 (2): 111-118.
- Raja, R. K., D. Aiswarya, B. Gülcü, M. Raja, P. Perumal, S. Sivaramakrishnan, H. K. Kaya & S. Hazır, 2017. Response of three cyprinid fish species to the scavenger deterrent factor produced by the mutualistic bacteria associated with entomopathogenic nematodes. Journal of Invertebrate Pathology,143: 40-49.
- Richards, E. L., L. G. Alexander, D. Snellgrove, R. J. Thomas, N. M. Marples & J. Cable, 2014. Variation in the expression of dietary conservatism within and between fish species. Animal Behaviour, 88: 49-56.
- Shapiro-Ilan, D. I. & E. E. Lewis, 1999. Comparison of entomopathogenic nematode infectivity from infected hosts versus aqueous suspension. Environmental Entomology, 28 (5): 907-911.
- Shapiro-Ilan, D. I., E. E. Lewis & W. L. Tedders, 2003. Superior efficacy observed in entomopathogenic nematodes applied in infected-host cadavers compared with application in aqueous suspension. Journal of Invertebrate Pathology, 83 (3): 270-272.
- Thomas, R. J., T. A. King, H. E. Forshaw, N. M. Marples, M. P. Speed & J. Cable, 2010. The response of fish to novel prey: evidence that dietary conservatism is not restricted to birds. Behavioral Ecology, 21 (4): 669-675.
- Uluğ, D., S. Hazır, H. K. Kaya & E. E. Lewis, 2014. Natural enemies of natural enemies: the potential top-down impact of predators on entomopathogenic nematode populations: Top-down impact of predators on EPNs. Ecological Entomology, 39 (4): 462-469.
- Zhou, X., H. K. Kaya, K. Heungens & H. Goodrich-Blair, 2002. Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Applied and Environmental Microbiology, 68 (12): 6202-6209.
Rattus norvegicus (Berkenhout, 1769) (Rodentia: Muridae)’un entomopatojen bakteriler ile enfekte böcek kadavralarına tepkisinin belirlenmesi
Abstract
Xenorhabdus Thomas & Poinar (Enterobacteriales: Morganellaceae) ve Photorhabdus Thomas & Poinar (Enterobacteriales: Morganellaceae) cinslerine ait bakteriler sırasıyla Steinernema Travassos, 1927 (Rhabditida: Steinernematidae) ve Heterorhabditis Poinar, 1976 (Rhabditida: Heterorhabditidae) cinslerine ait enotomopatojen nematodlarla mutualistik ilişki içerisindedirler. Bu bakterilerin nematodla enfekte kadavraları rekabetçi organizmalardan korumak amacıyla pek çok sekonder metabolit ürettiği bilinmektedir. Bu sekonder metabolitlerden bir tanesi olan yağmacı uzaklaştırıcı faktörün farklı eklembacaklı, kuş ve balık türlerine karşı uzaklaştırıcı etki gösterdiği bilinmektedir. 2019-2020 yılları arasında Aydın Adnan Menderes Üniversitesi’nde yürütülen bu çalışmada farklı Xenorhabdus ve Photorhabdus türleri ile enfekte kadavraların Rattus norvegicus (Berkenhout, 1769) (Rodentia: Muridae)’a karşı uzaklaştırıcı etkisi tek ya da ikili besin tercihi deneyleri ile test edilmiştir. Ratlara bakteriler ile enfekte edilmiş 4 günlük enfekte Galleria mellonella (L., 1758) (Lepidoptera: Pyralidae) kadavraları verilmiş ve ratların beslenme davranışları gözlemlenerek kaydedilmiştir. Yapılan çalışma sonucunda bazı Xenorhabdus ve Photorhabdus türleri ile enfekte kadavraların ratlara karşı uzaklaştırıcı etki gösterdiği belirlenmiştir. Bu etkinin büyük olasılıkla larvalarda oluşan kötü tattan kaynaklandığı düşünülmektedir. Ekolojik olarak, veriler entomopatojen nematod/bakteri kompleksinin doğada böceklerle beslenen memelilerin saldırılarına karşı korunabileceğini göstermiştir.
Project Number
Aydın Adnan Menderes Üniversitesi FEF-20002, TÜBİTAK-KBAG 116Z074
References
- Baur, M. E., H. K. Kaya & D. R. Strong, 1998. Foraging ants as scavengers on entomopathogenic nematode killed insects. Biological Control, 12 (3): 231-236.
- Bode, H. B., 2009. Entomopathogenic bacteria as a source of secondary metabolites. Current Opinion in Chemical Biology, 13 (2): 224-230.
- Boemare, N. E., 2002. “Biology, Taxonomy and Systematics of Photorhabdus and Xenorhabdus, 35-56”. In: Entomopathogenic Nematology (Eds. R. Gaugler). CABI Publishing Wallingford, UK, 388 pp.
- Çimen, H., M. Touray, Ş. H. Gülşen, Ö. Erincik, S. L. Wenski, H. B. Bode, D. I. Shapiro-Ilan & S. Hazır, 2021. Antifungal activity of different Xenorhabdus and Photorhabdus species against various fungal phytopathogens and identification of the antifungal compounds from X. szentirmaii. Applied Microbiology and Biotechnology, 105 (13): 5517-5528.
- Fenton, A., L. Magoolagan, Z. Kennedy & K. A. Spencer, 2011. Parasite-induced warning coloration: a novel form of host manipulation. Animal Behaviour, 81 (2): 417-422.
- Ffrench-Constant, R. H. & D. J. Bowen, 2000. Novel insecticidal toxins from nematode-symbiotic bacteria. Cellular and Molecular Life Sciences, 57 (5): 828-833.
- Gaugler, R. & H. K. Kaya, 1990. Entomopathogenic Nematodes in Biological Control. CRC Press Boca Raton, FL, USA, 381 pp.
- Gómez Villafañe, I. E., F. Miñarro, M. Ribicich, C. A. Rossetti, D. Rossotti & M. Busch, 2004. Assessment of the risks of rats (Rattus norvegicus) and opossums (Didelphis albiventris) in different poultry-rearing areas in Argentina. Brazilian Journal of Microbiology, 35 (4): 359-363.
- Gülcü, B., H. Çimen, R. K. Raja & S. Hazır, 2017. Entomopathogenic nematodes and their mutualistic bacteria: Their ecology and application as microbial control agents. Biopesticides International, 13 (2): 79-112.
- Gülcü, B., S. Hazır & H. K. Kaya, 2012. Scavenger deterrent factor (SDF) from symbiotic bacteria of entomopathogenic nematodes. Journal of Invertebrate Pathology, 110 (3): 326-333.
- Gülcü, B., S. Hazır, E. E. Lewis & H. K. Kaya, 2018. Evaluation of responses of different ant species (Formicidae) to the scavenger deterrent factor associated with the entomopathogenic nematode-bacterium complex. European Journal of Entomology, 115 (1): 312-317.
- Gulzar, S., M. Usman, W. Wakil, B. Gülcü, C. Hazır, M. Karagöz, S. Hazır & D. I. Shapiro-Ilan, 2020. Environmental tolerance of entomopathogenic nematodes differs among nematodes arising from host cadavers versus aqueous suspension. Journal of Invertebrate Pathology, 175: 107452 (1-7).
- Han, R. & R.U. Ehlers, 2000. Pathogenicity, development and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. Journal of Invertebrate Pathology, 75 (1): 55-58.
- Hazır, S., D. I. Shapiro-Ilan, C. H. Bock, C. Hazır, L. G. Leite & M. W. Hotchkiss, 2016. Relative potency of culture supernatants of Xenorhabdus and Photorhabdus spp. on growth of some fungal phytopathogens. European Journal of Plant Pathology, 146 (2016): 369-381.
- Hazır, S., H. K. Kaya, M. Touray, H. Çimen & D. I. Shapiro-Ilan, 2022. Basic laboratory and field manual for conducting research with the entomopathogenic nematodes, Steinernema and Heterorhabditis, and their bacterial symbionts. Turkish Journal of Zoology, 46 (4): 305-350.
- Hazır, S., N. Keskin, N., S. P. Stock, H. K. Kaya & S. Özcan, 2003. Diversity and distribution of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Turkey. Biodiversity and Conservation, 12 (2): 375-386.
- Jaffuel, G., S. Krishnamani, R. A. R. Machado, R. Campos-Herrera & T. C. J. Turlings, 2021. Potent Ant Deterrents Emitted from Nematode-Infected Insect Cadavers. Journal of Chemical Ecology, 48 (2021): 71-78.
- Jones, R. S., A. Fenton, & M. P. Speed, 2016. "Parasite-induced aposematism" protects entomopathogenic nematode parasites against invertebrate enemies. Behavioral Ecology, 27 (2): 645-651.
- Jones, R. S., A. Fenton, A., M. P. Speed, & J. Mappes, 2017. Investment in multiple defences protects a nematode-bacterium symbiosis from predation. Animal Behaviour, 129 (12): 1-8.
- Kaya, H. K. & P. Stock, 1997. “Techniques in Insect Nematology, 282-324”. In: Manual of Techniques in Insect Pathology (Eds. L. A. Lacey). Academic Press, San Diego, 409 pp.
- Kaya, H. K., A. M. Koppenhöfer, & M. W. Johnson, 1998. Natural enemies of entomopathogenic nematodes. Japanese Journal of Nematology, 28 (supplement): 13-21.
- Marples, N. M. & D. J. Kelly, 1999. Neophobia and dietary conservatism: Two distinct processes? Evolutionary Ecology, 3 (7-8): 641-653.
- Marples, N. M., T. J. Roper & D. G. C. Harper, 1998. Responses of wild birds to novel prey: Evidence of dietary conservatism. Oikos, 83 (1): 161-165.
- Mertz, N. R., E. J. G. Agudelo, F. S. Sales & A. Moino Junior, 2015. Effects of entomopathogenic nematodes on the predator Calosoma granulatum in the laboratory. Journal of Insect Behavior, 28 (3): 312-327.
- Perez, E. E., E. E. Lewis & D. I. Shapiro-Ilan, 2003. Impact of the host cadaver on survival and infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) under desiccating conditions. Journal of Invertebrate Pathology, 82 (2): 111-118.
- Raja, R. K., D. Aiswarya, B. Gülcü, M. Raja, P. Perumal, S. Sivaramakrishnan, H. K. Kaya & S. Hazır, 2017. Response of three cyprinid fish species to the scavenger deterrent factor produced by the mutualistic bacteria associated with entomopathogenic nematodes. Journal of Invertebrate Pathology,143: 40-49.
- Richards, E. L., L. G. Alexander, D. Snellgrove, R. J. Thomas, N. M. Marples & J. Cable, 2014. Variation in the expression of dietary conservatism within and between fish species. Animal Behaviour, 88: 49-56.
- Shapiro-Ilan, D. I. & E. E. Lewis, 1999. Comparison of entomopathogenic nematode infectivity from infected hosts versus aqueous suspension. Environmental Entomology, 28 (5): 907-911.
- Shapiro-Ilan, D. I., E. E. Lewis & W. L. Tedders, 2003. Superior efficacy observed in entomopathogenic nematodes applied in infected-host cadavers compared with application in aqueous suspension. Journal of Invertebrate Pathology, 83 (3): 270-272.
- Thomas, R. J., T. A. King, H. E. Forshaw, N. M. Marples, M. P. Speed & J. Cable, 2010. The response of fish to novel prey: evidence that dietary conservatism is not restricted to birds. Behavioral Ecology, 21 (4): 669-675.
- Uluğ, D., S. Hazır, H. K. Kaya & E. E. Lewis, 2014. Natural enemies of natural enemies: the potential top-down impact of predators on entomopathogenic nematode populations: Top-down impact of predators on EPNs. Ecological Entomology, 39 (4): 462-469.
- Zhou, X., H. K. Kaya, K. Heungens & H. Goodrich-Blair, 2002. Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Applied and Environmental Microbiology, 68 (12): 6202-6209.
There are 32 citations in total.
Details
| Primary Language | English |
|---|---|
| Journal Section | Articles |
| Authors | |
| Project Number | Aydın Adnan Menderes Üniversitesi FEF-20002, TÜBİTAK-KBAG 116Z074 |
| Publication Date | April 25, 2023 |
| Submission Date | November 4, 2022 |
| Acceptance Date | March 21, 2023 |
| Published in Issue | Year 2023 Volume: 47 Issue: 1 |
