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Steinernema khuongi n. sp. (Panagrolaimomorpha, Steinernematidae), a new entomopathogenic nematode species from Florida, USA

Published online by Cambridge University Press:  10 May 2018

S.P. Stock ,
R. Campos-Herrera ,
F.E. El-Borai  and
L.W. Duncan
S.P. Stock*
Affiliation:
Department of Entomology, University of Arizona, 1140 E. South Campus Dr. Tucson, AZ 85721-0036, Arizona, USA
R. Campos-Herrera
Affiliation:
Citrus Research and Education Center (CREC), University of Florida (UF), 700 Experiment Station Road, FL, 33850, USA Centro para os Recursos Biológicos e Alimentos Mediterrânicos, Universidade do Algarve Campus Gambelas, 8005-139 Faro, Portugal
F.E. El-Borai
Affiliation:
Centro para os Recursos Biológicos e Alimentos Mediterrânicos, Universidade do Algarve Campus Gambelas, 8005-139 Faro, Portugal Plant Protection Department, Faculty of Agriculture, Zagazig University, Egypt
L.W. Duncan
Affiliation:
Citrus Research and Education Center (CREC), University of Florida (UF), 700 Experiment Station Road, FL, 33850, USA
*
Author for correspondence: S.P. Stock, Fax: +1-520-621-1150, E-mail: [email protected]
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Abstract

In this study, molecular (ribosomal sequence data), morphological and cross-hybridization properties were used to identify a new Steinernema sp. from Florida, USA. Molecular and morphological data provided evidence for placing the novel species into Clade V, or the ‘glaseri-group’ of Steinernema spp. Within this clade, analysis of sequence data of the rDNA genes, 28S and internal transcribed spacer (ITS), depicted the novel species as a distinctive entity and closely related to S. glaseri and S. cubanum. Additionally, cross-hybridization assays showed that the new species is unable to interbreed with either of the latter two species, reinforcing its uniqueness from a biological species concept standpoint. Key morphological diagnostic characters for S. khuongi n. sp. include the mean morphometric features of the third-stage infective juveniles: total body length (average: 1066 μm), tail length (average: 65 μm), location of the excretory pore (average: 80.5 μm) and the values of c (average: 16.4), D% (average: 60.5), E% (average: 126) and H% (average: 46.6). Additionally, males can be differentiated from S. glaseri and S. cubanum by the values of several ratios: D% (average: 68), E% (average: 323) and SW% (average: 120). The natural distribution of this species in Florida encompasses both natural areas and citrus groves, primarily in shallow groundwater ecoregions designated as ‘flatwoods’. The morphological, molecular, phylogenetic and ecological data associated with this nematode support its identity as a new species in the S. glaseri-group.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 2 , March 2019 , pp. 226 - 241
Copyright
Copyright © Cambridge University Press 2018 

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References

Artyukhovsky, AK, Kozodoi, EM, Reid, AP and Spiridonov, SE (1997) Redescription of Steinernema arenarium (Artyukhovsky, 1967) topotype from Central Russia and a proposal for S. anomalae (Kozodoi, 1984) as a junior synonym. Russian Journal of Nematology 5, 31–37.Google Scholar
Beavers, JB and Selhime, AG (1975) Development of Diaprepes abbreviatus on potted citrus seedlings. Florida Entomologist 1, 271–273.Google Scholar
Bedding, RA and Akhurst, RJ (1975) A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica 21, 109–110.Google Scholar
Campos–Herrera, R, Johnson, EG, El–Borai, FE, Stuart, RJ, Graham, JH and Duncan, LW (2011) Long-term stability of entomopathogenic nematode spatial patterns measured by sentinel insects and real-time PCR assays. Annals of Applied Biology 158, 55–68.Google Scholar
Campos–Herrera, R, Pathak, E, El–Borai, FE, Stuart, RJ, Gutiérrez, C, Rodríguez–Martín, JA, Graham, JH and Duncan, LW (2013) Geospatial patterns of soil properties and the biological control potential of entomopathogenic nematodes in Florida citrus groves. Soil Biology and Biochemistry 66, 163–174.Google Scholar
Campos-Herrera, R, El-Borai, FE, Rodriguez Martin, JA and Duncan, LW (2016) Entomopathogenic nematode food web assemblages in Florida natural areas. Soil Biology and Biochemistry 93, 105–114.Google Scholar
Çimen, H, Lee, MM, Hatting, J, Hazir, S and Stock, SP (2015) Steinernema innovationi n. sp. (Panagrolaimomorpha: Steinernematidae), a new entomopathogenic nematode species from South Africa. Journal of Helminthology 89, 415–427.Google Scholar
Duncan, LW, Stuart, RJ, El-Borai, FE, Campos-Herrera, R, Pathak, E, Giurcanu, M and Graham, JH (2013) Modifying orchard planting sites conserves entomopathogenic nematodes, reduces weevil herbivory and increases citrus tree growth, survival and fruit yield. Biological Control 64, 26–36.Google Scholar
El-Borai, FE, Zellers, JD and Duncan, LW (2007a) Suppression of Diaprepes abbreviatus in potted citrus by combinations of entomopathogenic nematodes with different lifespans. Nematropica 37, 33–42.Google Scholar
EL-Borai, FE, Brentu, CF and Duncan, LW (2007b) Augmenting entomopathogenic nematodes in soil from a Florida citrus orchard: non-target effects of a trophic cascade. Journal of Nematology 39, 203–210.Google Scholar
EL-Borai, FE, Bright, DB, Graham, JH, Stuart, RJ, Cubero, J and Duncan, LW (2009) Differential susceptibility of entomopathogenic nematodes to nematophagous fungi from Florida citrus orchards. Nematology 11, 231–241.Google Scholar
El-Borai, FE, Killiny, N and Duncan, LW (2016) Concilience in entomopathogenic nematode responses to water potential and their geospatial patterns in Florida. Frontiers in Microbiology. http://journalfrontiersin.org/article/10.3389/fmicb.2016.00356.Google Scholar
Franklin, M and Goodey, JB (1949) A cotton blue–lactophenol method for mounting plant parasitic nematodes. Journal of Helmintholology 23, 175–178.Google Scholar
Hominick, WM, Briscoe, BR, del Pino, FG, et al. (1997) Biosystematics of entomopathogenic nematodes, current status, protocols and definitions. Journal of Helminthology 71, 271–298.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.Google Scholar
Kaya, HK and Stock, SP (1997) Techniques in insect nematology. pp. 281–324 in Lacey, L (Ed.) Manual of techniques in insect pathology. San Diego, California, Academic Press.Google Scholar
Kearse, M, Moir, R, Wilson, A, et al. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.Google Scholar
Khatri-Chhetri, HB, Waeyenberge, L, Spiridonov, S, Manandhar, HK and Moens, M (2011) Steinernema lamjungense n. sp. (Rhabditida: Steinernematidae), a new species of entomopathogenic nematode from Lamjung district, Nepal. Nematology 13, 589–605.Google Scholar
Kim, SK, Flores-Lara, Y and Stock, SP (2012). Morphology and ultrastructure of the bacterial receptacle in Steinernema nematodes (Nematoda: Steinernematidae). Journal of Invertebrate Pathology 110, 366–374.Google Scholar
Lee, MM, Sicard, M, Skeie, M and Stock, SP (2009) Steinernema boemarei n. sp. (Nematoda: Steinernematidae), a new entomopathogenic nematode from southern France. Systematic Parasitology 72, 127–141.Google Scholar
Maddison, WP and Maddison, DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. Available at http://mesquiteproject.org (accessed 31 January 2018).Google Scholar
Malan, AP, Knoetze, R and Tiedt, LR (2016) Steinernema jeffreyense n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from South Africa. Journal of Helminthology 90, 262–278.Google Scholar
McClure, MJ and Stowell, LJ (1978) A simple method of processing nematodes for electron microscopy. Journal of Nematology 18, 376–377.Google Scholar
McCoy, CW, Shapiro, DI, Duncan, LW and Nguyen, K (2000) Entomopathogenic nematodes and other natural enemies as mortality factors for larvae of Diaprepes abbreviatus (Coleoptera: Curculionidae). Biological Control 19, 182–190.Google Scholar
McCoy, CW, Rogers, ME, Futch, SH, Graham, JH, Duncan, LW and Nigg, HN (2008) Florida citrus pest management guide: citrus root weevils. Entomology and Nematology Department document ENY-611. Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida.Google Scholar
Mráček, Z, Hernandez, EA and Boemare, NE (1994) Steinernema cubana sp. n. (Nematoda: Rhabditida: Steinernematidae) and the preliminary characterization of its associated bacterium. Journal of Invertebrate Pathology 64, 123–129.Google Scholar
Nadler, SA, Bolotin, E and Stock, SP (2006) Phylogenetic relationships of Steinernema (Cephalobina, Steinernematidae) based on nuclear, mitochondrial, and morphological data. Systematic Parasitology 63, 159–179.Google Scholar
Nguyen, KB and Buss, EA (2011) Steinernema phyllophagae n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from Florida, USA. Nematology 13, 425–442.Google Scholar
Nguyen, KB and Duncan, LW (2002) Steinernema diaprepesi n. sp. (Rhabditida: Steinernematidae), a parasite of the citrus root weevil Diaprepes abbreviatus (L) (Coleoptera: Curculionidae). Journal of Nematology 34, 159–170.Google Scholar
Nguyen, KB, Maruniak, J and Adams, BJ (2001) The diagnostic and phylogenetic utility of the rDNA internal transcribed spacer sequences in Steinernema. Journal of Nematology 33, 73–82.Google Scholar
Nguyen, KB, Malan, AP and Gozel, U (2006) Steinernema khoisanae n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from South Africa. Nematology 8, 157–175.Google Scholar
Nguyen, KB, Ginarte, CMA, Leite, LG, dos Santos, JM and Harakava, R (2010) Steinernema brazilense n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from Mato Grosso, Brazil. Journal of Invertebrate Pathology 103, 8–20.Google Scholar
Nigg, HN, Simpson, SE, Ramos, LE, Tomerlin, T, Harrison, JM and Cuyler, N (2001) Distribution and movement of adult Diaprepes abbreviatus (Coleoptera: Curculionidae) in a Florida citrus grove. Florida Entomologist, 84, 641–651.Google Scholar
Poinar, GO Jr (1990) Biology and taxonomy of Steinernematidae and Heterorhabditidae. pp. 23–62 in Poinar, GO Jr (Ed.) Entomopathogenic nematodes in biological control. Boca Raton, Florida, CRC Press.Google Scholar
Qiu, L, Fang, Y, Zhou, Y, Pang, Y and Nguyen, KB (2004) Steinernema guangdongense sp. n. (Nematoda: Steinernematidae), a new entomopathogenic nematode from southern China with a note on S. serratum (nomen nudum). Zootaxa 704, 1–20.Google Scholar
Qiu, L, Yan, X, Zhou, Y, Nguyen, KB and Pang, Y (2005) Steinernema aciari sp. n. (Nematoda: Steinernematidae), a new entomopathogenic nematode from Guangdong, China. Journal of Invertebrate Pathology 88, 58–69.Google Scholar
Román, J and Figueroa, W (1994) Steinernema puertoricensis n. sp. (Rhabditida: Steinernematidae) a new entomopathogenic nematode from Puerto Rico. Journal of Agriculture, University of Puerto Rico 78, 167–175.Google Scholar
Seinhorst, JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4, 67–69.Google Scholar
Shapiro, DI and McCoy, CW (2000) Virulence of entomopathogenic nematodes to Diaprepes abbreviatus (Coleoptera: Curculionidae) in the laboratory. Journal of Economic Entomology 93, 1090–1095.Google Scholar
Spiridonov, SE, Reid, AP, Podrucka, K, Subbotin, SA and Moens, M (2004) Phylogenetic relationships within the genus Steinernema (Nematoda: Rhabditida) as inferred from analyses of sequences of the ITS1–5.8S–ITS2 region of rDNA and morphological features. Nematology 6, 547–566.Google Scholar
Stiernagle, T (2006) Maintenance of C. elegans (11 February 2006). In The C. elegans Research Community (Ed.) WormBook. doi/10.1895/wormbook.1.101.1. Available at http://www.wormbook.org/ (accessed 31 January 2018).Google Scholar
Stock, SP and Goodrich-Blair, H (2012) Nematode parasites, pathogens and associates of insects and invertebrates of economic importance. pp. 373–426 in Lacey, L (Ed.) Manual of techniques in invertebrate pathology. 2nd edn. San Diego, California, USA, Academic Press.Google Scholar
Stock, SP and Koppenhöfer, AM (2003) Steinernema scarabaei n. sp. (Rhabditida: Steinernematidae), a natural pathogen of scarab beetle larvae (Coleoptera: Scarabaeidae) from New Jersey, USA. Nematology 5, 191–204.Google Scholar
Stock, SP, Campbell, JF and Nadler, SA (2001a) Phylogeny of Steinernema Travassos, 1927 (Cephalobina, Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. Journal of Parasitology 87, 877–889.Google Scholar
Stock, SP, Heng, J, Hunt, DJ, Reid, AP, Shen, X and Choo, HY (2001b) Redescription of Steinernema longicaudum Shen & Wang (Nematoda: Steinernematidae); geographic distribution and phenotypic variation between allopatric populations. Journal of Helminthology 75, 81–92.Google Scholar
Stock, SP, Griffin, CT and Chaenari, R (2004) Morphological and molecular characterisation of Steinernema hermaphroditum n. sp. (Nematoda: Steinernematidae), an entomopathogenic nematode from Indonesia, and its phylogenetic relationships with other members of the genus. Nematology 6, 401–412.Google Scholar
Stuart, RJ, El-Borai, FE and Duncan, LW (2008) From augmentation to conservation of entomopathogenic nematodes: trophic cascades, habitat manipulation and enhanced biological control of Diaprepes abbreviatus root weevils in Florida citrus groves. Journal of Nematology 40, 73–84.Google Scholar
Swofford, DL (2002) PAUP*. Phylogenetic analysis using parsimony (and other methods), version 4. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Tamiru, T, Waeyenberge, L, Hailu, T, Ehlers, RU, Půža, V and Mráček, Z (2012) Steinernema ethiopiense sp. n. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from Ethiopia. Nematology 14, 741–757.Google Scholar
Uribe-Lorío, L, Mora, M and Stock, SP (2007) Steinernema costaricense n. sp. and Steinernema puntauvense n. sp. (Rhabditida, Steinernematidae), two new entomopathogenic nematodes from Costa Rica. Systematic Parasitology 68, 167–172.Google Scholar
Waturu, CN, Hunt, DJ and Reid, AP (1997) Steinernema karii sp. n. (Nematoda: Steinernematidae), a new entomopathogenic nematode from Kenya. International Journal of Nematology 7, 68–75.Google Scholar
Weissling, TJ, Peña, JE, Giblin-Davis, RM and Knapp, JL (2002) Sugarcane rootstock borer weevil, Diaprepes abbreviatus (L.). Featured creatures. University of Florida, Gainesville, Florida, USA. Available at http://creatures.ifas.ufl.edu/citrus/sugarcane_rootstock_borer_weevil.htmGoogle Scholar