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1.  Soil moisture effects on the activity of three entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) isolated from Meghalaya, India 
Entomopathogenic nematodes (EPNs) are obligate parasites of insects that are widely distributed in soils throughout the world. They have great potential for use as biological control agents for insect pests. It is known that strains of Steinernema and Heterorhabditis isolated from different geographical regions exhibit differences in their ecological traits, such as infectivity, establishment, survival, reproduction, etc. A precise knowledge of these factors is therefore an essential pre-requisite for devising successful strategies to use these nematodes in biological control programmes. The present study investigated the effect of soil moisture on the activity (as measured by number of nematodes established in hosts) of three entomopathogenic nematode species (Heterorhabditis indica Poinar, Karunakar & David; Steinernema thermophilum Ganguly & Singh; Steinernema glaseri Steiner), isolated from forest soils in Meghalaya, India, under laboratory conditions. The experiments for EPNs were conducted at 25 ± 2°C (30 ± 2°C for S. thermophilum) in a sandy loam soil (85% sand, 12% silt and 3% clay, pH 6.54). Last instar larvae of wax moth, Galleria mellonella served as the experimental insect host. The soil moistures tested were 3, 4, 5, 6, 8, 10, 12, 14, 16, 18, 20, 22 and 25% (w/w). The study revealed that soil moisture has marked influences on establishment of infective juveniles of different nematode species in insect host. While, S. thermophilum showed establishment at 4% and above soil moistures, H. indica and S. glaseri showed establishment at 5% and above soil moistures. The optimum soil moisture for different nematode species were noted as: H. indica 8–18%, S. thermophilum 6–20%, and S. glaseri 8–25%. Further, a minimum of 6% soil moisture was noted to be essential for achieving 100% host mortality for all the three nematode species.
doi:10.1007/s12639-011-0076-x
PMCID: PMC3284615  PMID: 23543771
Entomopathogenic nematodes; Soil moisture; Heterorhabditis indica; Steinernema thermophilum; Steinernema glaseri; Galleria mellonella; Biological control; Meghalaya
2.  Incidence of Endemic Entomopathogenic Nematodes Following Application of Steinernema riobrave for Control of Diaprepes abbreviatus 
Journal of Nematology  2003;35(2):178-186.
Control of Diaprepes abbreviatus by endemic and exotic entomopathogenic nematodes (EPN) was monitored during 2000-2001 in two citrus orchards in central Florida (Bartow and Poinciana). Caged sentinel insect larvae were buried beneath citrus trees for 7 days at 1 to 2-month intervals from April to October each year. At Bartow, the survey occurred in experimental plots that were (i) not treated with commercial EPN, (ii) treated twice annually since 1998 with commercially formulated Steinernema riobrave, or (iii) treated twice annually with S. riobrave and liquid fertilization (15 times/year) occurred in place of dry fertilizer (3 times/year) used in the other treatments. Four endemic EPN species, in addition to S. riobrave, were recovered from the sandy soil at Bartow: S. diaprepesi, Heterorhabditis zealandica, H. indica, and H. bacteriophora. Mean insect mortality in control plots was 39.4% (range = 13% to 74%), with seasonal maxima in May to July each year. Endemic EPN were recovered from 55% (range = 22% to 81%) of the cadavers each month. Total numbers of endemic EPN recovered in all plots during 2 years were directly related to the numbers of adult weevils (D. abbreviatus and Pachnaeus litus) captured in modified Tedder's traps and inversely related to recovery of S. riobrave. Insect mortality was higher and cadavers containing endemic EPN were more numerous in untreated control plots than in S. riobrave-treated plots, except during months in which S. riobrave was applied. In treated plots, endemic EPN were recovered from cadavers at twice the rate of S. riobrave. Suppression of endemic EPN in plots treated with S. riobrave, combined with inferior persistence by the introduced species, may have attenuated the net efficacy of S. riobrave against D. abbreviatus. In contrast, H. indica was the only endemic nematode recovered from the sandy clay loam soil at Poinciana, where the average mortality of D. abbreviatus was 12% (range 3% to 20%) and incidence of H. indica did not exceed 8%. Results of these surveys suggest that the regional patterns in the abundance and damage to citrus caused by D. abbreviatus in Florida are regulated by endemic EPN and other soilborne enemies of the weevil.
PMCID: PMC2620623  PMID: 19265992
Abbott's formula; biological control; competition; entomopathogenic nematodes; Heterorhabditis; natural control; seasonality; Steinernema
3.  Natural Occurrence of Entomopathogenic Nematodes (Rhabditida: Steinernema, Heterorhabditis) in the Azores 
Journal of Nematology  2000;32(2):215-222.
A soil survey for entomopathogenic nematodes was conducted throughout the nine islands of the Azorean archipelago. Forty-six out of 1,180 samples (3.9%) were positive, with Heterorhabditis spp. isolated from 30 sites on six islands and Steinernema spp. isolated from 16 sites on three islands. São Miguel and Terceira Islands were positive for both genera, and Pico Island was positive only for Steinernema. Entomopathogenic nematodes were found from sea level up to 750 m. Seventy percent of the samples positive for Heterorhabditis were collected below 150 m, whereas 62.5% of the samples positive for Steinernema were collected above 300 m. Heterorhabditis was not isolated above 450 m. Steinernema was collected mostly in loamy-sand and sandy-loam soils with a pH below 6, whereas Heterorhabditis was mostly collected in sandy and loamy-sand soils with pH higher than 6. Steinernema and Heterorhabditis were found in cropland, orchards, and pastures, while Heterorhabditis was found also in woodland and native vegetation.
PMCID: PMC2620449  PMID: 19270969
azores; biological control; entomopathogenic nematodes; Heterorhabditis spp.; insecta; island; natural occurrence; Steinernema spp.; survey
4.  Virulence of Entomopathogenic Nematodes to Plum Curculio, Conotrachelus nenuphar: Effects of Strain, Temperature, and Soil Type 
Journal of Nematology  2011;43(3-4):187-195.
The plum curculio, Conotrachelus nenuphar, is a major pest of stone and pome fruit (e.g., apples, pears, peaches, cherries, etc.). Entomopathogenic nematodes (Steinernema spp. and Heterorhabditis spp.) may be used to control the larval stage of C. nenuphar following fruit drop. Indeed, certain entomopathogenic nematodes species have previously been shown to be highly effective in killing C. nenuphar larvae in laboratory and field trials. In field trials conducted in the Southeastern, USA, Steinernema riobrave has thus far been shown to be the most effective species. However, due to lower soil temperatures, other entomopathogenic nematode strains or species may be more appropriate for use against C. nenuphar in the insect’s northern range. Thus, the objective of this study was to conduct a broad screening of entomopathogenic nematodes. Under laboratory conditions, we determined the virulence of 13 nematode strains (comprising nine species) in two different soils (a loam and clay-loam) and three different temperatures (12°C, 18°C, and 25°C). Superior virulence was observed in S. feltiae (SN strain), S. rarum (17 C&E strain), and S. riobrave (355 strain). Promising levels of virulence were also observed in others including H. indica (HOM1 strain), H. bacteriophora (Oswego strain), S. kraussei, and S. carpocapsae (Sal strain). All nematode treatments were affected by temperature with the highest virulence observed at the highest temperature (25°C). In future research, field tests will be used to further narrow down the most suitable nematode species for C. nenuphar control.
PMCID: PMC3547350  PMID: 23430967
biological control; Conotrachelus nenuphar; entomopathogenic nematode; Heterorhabditis; plum curculio; Steinernema
5.  Competition Between Entomopathogenic and Free-Living Bactivorous Nematodes in Larvae of the Weevil Diaprepes abbreviatus 
Journal of Nematology  2003;35(2):187-193.
Field and laboratory experiments were conducted to determine the degree to which free-living, bactivorous nematodes (FLBN) are able to competitively displace entomopathogenic nematodes (EPN) from insect cadavers. Two hundred larvae of the insect Diaprepes abbreviatus were buried at regular intervals during 2 years in experimental plots that were untreated or treated twice annually with Steinernema riobrave. Larvae were recovered after 7 days, and nematodes emerging from cadavers during the next 30 days were identified. The monthly prevalence of FLBN was directly related to that of S. riobrave (r = 0.38; P = 0.001) but was not related to the prevalence of the endemic EPN, S. diaprepesi, Heterorhabditis zealandica, H. indica, or H. bacteriophora (r = 0.02; P = 0.80). In a second experiment, treatment of small field plots with S. riobrave increased the prevalence of insect cadavers in which only FLBN were detected compared to untreated controls (30% vs. 14%; P = 0.052), and increased numbers of FLBN per buried insect by more than 10-fold. In the laboratory, sand microcosms containing one D. abbreviatus larva were treated with (i) the FLBN, Pellioditis sp.; (ii) S. riobrave; (iii) S. riobrave + Pellioditis; or (iv) neither nematode. Insect mortality was higher in the presence of both nematodes (57%) than when S. riobrave was alone (42%) (P = 0.01). An average of 59.2 Pellioditis sp. g-1 insect body weight emerged in the presence of S. riobrave, whereas 6.2 nematodes g-1 insect were recovered in the absence of the EPN (P = 0.01). Pellioditis sp. reduced the number of S. riobrave per cadaver by 84%; (P = 0.03), and per available insect by 82% (P = 0.001), compared to S. riobrave alone. Population size of S. diaprepesi was not affected by Pellioditis sp. in experiments of the same design. Faster development (P = 0.05) and nutrient appropriation within the insect cadaver by S. diaprepesi compared to S. riobrave may increase the fitness of the former species to compete with Pellioditis sp. The results of these studies demonstrate the potential of FLBN to regulate population densities of EPN and to dampen estimates of EPN-induced mortality of insect pests in the field.
PMCID: PMC2620622  PMID: 19265993
free-living nematodes; microbivorous nematodes; Pellioditis; Steinernema diaprepesi; Steinernema riobrave; Steinernematidae
6.  Perspectives on the Behavior of Entomopathogenic Nematodes from Dispersal to Reproduction: Traits Contributing to Nematode Fitness and Biocontrol Efficacy 
Journal of Nematology  2012;44(2):177-184.
The entomopathogenic nematodes (EPN) Heterorhabditis and Steinernema are widely used for the biological control of insect pests and are gaining importance as model organisms for studying parasitism and symbiosis. In this paper recent advances in the understanding of EPN behavior are reviewed. The “foraging strategy” paradigm (distinction between species with ambush and cruise strategies) as applied to EPN is being challenged and alternative paradigms proposed. Infection decisions are based on condition of the potential host, and it is becoming clear that already-infected and even long-dead hosts may be invaded, as well as healthy live hosts. The state of the infective juvenile (IJ) also influences infection, and evidence for a phased increase in infectivity of EPN species is mounting. The possibility of social behavior - adaptive interactions between IJs outside the host - is discussed. EPNs’ symbiotic bacteria (Photorhabdus and Xenorhabdus) are important for killing the host and rendering it suitable for nematode reproduction, but may reduce survival of IJs, resulting in a trade-off between survival and reproduction. The symbiont also contributes to defence of the cadaver by affecting food-choice decisions of insect and avian scavengers. I review EPN reproductive behavior (including sperm competition, copulation and evidence for attractive and organizational effects of pheromones), and consider the role of endotokia matricida as parental behavior exploited by the symbiont for transmission.
PMCID: PMC3578460  PMID: 23482343
Behavior; biological control; ecology; endotokia matricida; entomopathogenic nematode; fitness trade-off; foraging strategy; Heterorhabditis; phased infectivity; Photorhabdus; reproduction; scavenging; sexual maturation; symbiosis; Steinernema; Xenorhabdus
7.  Food Web Responses to Augmenting the Entomopathogenic Nematodes in Bare and Animal Manure-Mulched Soil 
Journal of nematology  2007;39(2):176-189.
Factorial treatments of entomopathogenic nematodes (EPN) and composted, manure mulches were evaluated for two years in a central Florida citrus orchard to study the post-application biology of EPN used to manage the root weevil, Diaprepes abbreviatus. Mulch treatments were applied once each year to study the effects of altering the community of EPN competitors (free-living bactivorous nematodes) and antagonists (nematophagous fungi (NF), predaceous nematodes and some microarthro-pods). EPN were augmented once with Steinernema riobrave in 2004 and twice in 2005. Adding EPN to soil affected the prevalence of organisms at several trophic levels, but the effects were often ephemeral and sometimes inconsistent. EPN augmentation always increased the mortality of sentinel weevil larvae, the prevalence of free-living nematodes in sentinel cadavers and the prevalence of trapping NF. Subsequent to the insecticidal effects of EPN augmentation in 2004, but not 2005, EPN became temporarily less prevalent, and fewer sentinel weevil larvae died in EPN-augmented compared to non-augmented plots. Manure mulch had variable effects on endoparasitic NF, but consistently decreased the prevalence of trapping NF and increased the prevalence of EPN and the sentinel mortality. Both temporal and spatial abundance of NF were inversely related to the prevalence of Steinernema diaprepesi, whereas Heterorhabditis zealandica prevalence was positively correlated with NF over time. The number of weevil larvae killed by EPN was likely greatest in 2005, due in part to non-target effects of augmentation on the endemic EPN community in 2004 that occurred during a period of peak weevil recruitment into the soil.
PMCID: PMC2586487  PMID: 19259487
Diaprepes abbreviatus; entomopathogenic nematodes; food webs; IPM; nematophagous fungi; post-application biology; survival; trophic cascades
8.  Survey of Heterorhabditidae and Steinernematidae (Rhabditida, Nematoda) in Western Canada 
Journal of Nematology  1993;25(4):710-717.
A survey was done in the summer months along the Alaska Highway, in other parts of British Columbia, in northern Alberta, and in the Yukon Territory for steinernematid and heterorhabditid nematodes occurring in the top 10 cm of soil. Steinernema feltiae and Steinernema spp. were found at 18 and Heterorhabditis megidis at 7 sites of 125 sampled. Most nematodes were found where visible insect infestation occurred and where human influence on the habitat was substantial (e.g., agricultural, forested and bush-hedgerow habitats); none was found in grassland or virgin forests. Heterorhabditis megidis occurred in only the southern, warmer, drier region of British Columbia. In the laboratory some steinernematid isolates and H. megidis killed Galleria mellonella larvae at 13 and 22 C, whereas some isolates of Steinernema killed the larvae at only 13 C. Steinernema spp. from three high altitude sites with low, average July temperatures (13-14 C) are cold-active in that they produced infective juveniles at 13 C and killed G. mellonella at 6 C.
PMCID: PMC2619435  PMID: 19279830
biological control; entomopathogenic nematode; Heterorhabditidae; low-temperature activity; nematode; Steinernenaatidae; survey; temperature
9.  Augmenting Entomopathogenic Nematodes in Soil from a Florida CitrusOrchard: Non-Target Effects of a Trophic Cascade 
Journal of nematology  2007;39(2):203-210.
Laboratory experiments were conducted to study non-target effects of augmenting entomopathogenic nematode (EPN)communities in soil. When raw soil from a citrus orchard was augmented with either 2,000 Steinernema riobrave or S. diaprepesi, fewer EPN (P ≤ 0.05) survived if the soil had also been treated with 2,000 S. riobrave 7 d earlier (i.e., two augmentation events rather than one). EPN survival was unaffected by treatment (P ≤ 0.05) in soil that was air-dried to disrupt antagonist activity prior to the experiment. When S. diaprepesi, S. riobrave, Heterorhabditis zealandica or no EPN were added to raw soil and S. diaprepesi was added 5 d later, the survival of both S. diaprepesi and of total EPN was greater (P ≤ 0.05) in soil that received no pretreatment than in soilpre treated with S. riobrave. Pretreatment of soil with H. zealandica or S. diaprepesi had less or no affect on survival of S. diaprepesi or total EPN. When nematodes were recovered from soil and placed on water agar, the number of S. diaprepesi that were killed by endoparasitic and trapping nematophagous fungi was greater (P ≤ 0.05) if soil was pretreated with steinernematid species than if the soil was not pretreated or was pretreated with H. zealandica. The adverse effects of pretreating soil on EPN survival were density dependent within a range of pretreatment dosages (20–100 IJ/cm2 soil surface), and the treatment effects required more time to become evident at lower than at higher dosages. These experiments suggest that non-target effects of augmenting the EPN community in soil vary among EPN species and have the potential to temporarily reduce EPN numbers below the natural equilibrium density.
PMCID: PMC2586486  PMID: 19259489
Antagonism; nematophagous fungi; numerical response; post-application biology; predation; survival
10.  Long-Term Persistence of Yersinia pseudotuberculosis in Entomopathogenic Nematodes 
PLoS ONE  2015;10(1):e0116818.
Entomopathogenic nematodes (EPNs) are small worms whose ecological behaviour consists to invade, kill insects and feed on their cadavers thanks to a species-specific symbiotic bacterium belonging to any of the genera Xenorhabdus or Photorhabdus hosted in the gastro-intestinal tract of EPNs. The symbiont provides a number of biological functions that are essential for its EPN host including the production of entomotoxins, of enzymes able to degrade the insect constitutive macromolecules and of antimicrobial compounds able to prevent the growth of competitors in the insect cadaver. The question addressed in this study was to investigate whether a mammalian pathogen taxonomically related to Xenorhabdus was able to substitute for or “hijack” the symbiotic relationship associating Xenorhabdus and Steinernema EPNs. To deal with this question, a laboratory experimental model was developed consisting in Galleria mellonella insect larvae, Steinernema EPNs with or without their natural Xenorhabdus symbiont and Yersinia pseudotuberculosis brought artificially either in the gut of EPNs or in the haemocoel of the insect larva prior to infection. The developed model demonstrated the capacity of EPNs to act as an efficient reservoir ensuring exponential multiplication, maintenance and dissemination of Y. pseudotuberculosis.
doi:10.1371/journal.pone.0116818
PMCID: PMC4312075  PMID: 25635766
11.  Characterization of Biocontrol Traits in Heterorhabditis floridensis: A Species with Broad Temperature Tolerance 
Journal of Nematology  2014;46(4):336-345.
Biological characteristics of two strains of the entomopathogenic nematode, Heterorhabditis floridensis (332 isolated in Florida and K22 isolated in Georgia) were described. The identity of the nematode’s symbiotic bacteria was elucidated and found to be Photorhabdus luminescens subsp. luminescens. Beneficial traits pertinent to biocontrol (environmental tolerance and virulence) were characterized. The range of temperature tolerance in the H. floridensis strains was broad and showed a high level of heat tolerance. The H. floridensis strains caused higher mortality or infection in G. mellonella at 30°C and 35°C compared with S. riobrave (355), a strain widely known to be heat tolerant, and the H. floridensis strains were also capable of infecting at 17°C whereas S. riobrave (355) was not. However, at higher temperatures (37°C and 39°C), though H. floridensis readily infected G. mellonella, S. riobrave strains caused higher levels of mortality. Desiccation tolerance in H. floridensis was similar to Heterorhabditis indica (Hom1) and S. riobrave (355) and superior to S. feltiae (SN). H. bacteriophora (Oswego) and S. carpocapsae (All) exhibited higher desiccation tolerance than the H. floridensis strains. The virulence of H. floridensis to four insect pests (Aethina tumida, Conotrachelus nenuphar, Diaprepes abbreviatus, and Tenebrio molitor) was determined relative to seven other nematodes: H. bacteriophora (Oswego), H. indica (Hom1), S. carpocapsae (All), S. feltiae (SN), S. glaseri (4-8 and Vs strains), and S. riobrave (355). Virulence to A. tumida was similar among the H. floridensis strains and other nematodes except S. glaseri (Vs), S. feltiae, and S. riobrave failed to cause higher mortality than the control. Only H. bacteriophora, H. indica, S. feltiae, S. riobrave, and S. glaseri (4-8) caused higher mortality than the control in C. nenuphar. All nematodes were pathogenic to D. abbreviatus though S. glaseri (4-8) and S. riobrave (355) were the most virulent. S. carpocapsae was the most virulent to T. molitor. In summary, the H. floridensis strains possess a wide niche breadth in temperature tolerance and have virulence and desiccation levels that are similar to a number of other entomopathogenic nematodes. The strains may be useful for biocontrol purposes in environments where temperature extremes occur within short durations.
PMCID: PMC4284085  PMID: 25580026
beneficial trait; biological control; entomopathogenic nematode; Heterorhabditis floridensis
12.  Entomopathogenic Nematodes as a Model System for Advancing the Frontiers of Ecology 
Journal of Nematology  2012;44(2):162-176.
Entomopathogenic nematodes (EPNs) in the families Heterorhabditidae and Steinernematidae have a mutualistic–symbiotic association with enteric γ-Proteobacteria (Steinernema–Xenorhabdus and Heterorhabditis–Photorhabdus), which confer high virulence against insects. EPNs have been studied intensively because of their role as a natural mortality factor for soil-dwelling arthropods and their potential as biological control agents for belowground insect pests. For many decades, research on EPNs focused on the taxonomy, phylogeny, biogeography, genetics, physiology, biochemistry and ecology, as well as commercial production and application technologies. More recently, EPNs and their bacterial symbionts are being viewed as a model system for advancing research in other disciplines such as soil ecology, symbiosis and evolutionary biology. Integration of existing information, particularly the accumulating information on their biology, into increasingly detailed population models is critical to improving our ability to exploit and manage EPNs as a biological control agent and to understand ecological processes in a changing world. Here, we summarize some recent advances in phylogeny, systematics, biogeography, community ecology and population dynamics models of EPNs, and describe how this research is advancing frontiers in ecology.
PMCID: PMC3578465  PMID: 23482825
biodiversity; entomopathogenic nematodes; Heterorhabditis; multivariate analysis; Photorhabdus; soil ecology; soil food web; Steinernema; Xenorhabdus
13.  Diversity of Xenorhabdus and Photorhabdus spp. and Their Symbiotic Entomopathogenic Nematodes from Thailand 
PLoS ONE  2012;7(9):e43835.
Xenorhabdus and Photorhabdus spp. are bacterial symbionts of entomopathogenic nematodes (EPNs). In this study, we isolated and characterized Xenorhabdus and Photorhabdus spp. from across Thailand together with their associated nematode symbionts, and characterized their phylogenetic diversity. EPNs were isolated from soil samples using a Galleria-baiting technique. Bacteria from EPNs were cultured and genotyped based on recA sequence. The nematodes were identified based on sequences of 28S rDNA and internal transcribed spacer regions. A total of 795 soil samples were collected from 159 sites in 13 provinces across Thailand. A total of 126 EPNs isolated from samples taken from 10 provinces were positive for Xenorhabdus (n = 69) or Photorhabdus spp. (n = 57). Phylogenetic analysis separated the 69 Xenorhabdus isolates into 4 groups. Groups 1, 2 and 3 consisting of 52, 13 and 1 isolates related to X. stockiae, and group 4 consisting of 3 isolates related to X. miraniensis. The EPN host for isolates related to X. stockiae was S. websteri, and for X. miraniensis was S. khoisanae. The Photorhabdus species were identified as P. luminescens (n = 56) and P. asymbiotica (n = 1). Phylogenenic analysis divided P. luminescens into five groups. Groups 1 and 2 consisted of 45 and 8 isolates defined as subspecies hainanensis and akhurstii, respectively. One isolate was related to hainanensis and akhurstii, two isolates were related to laumondii, and one isolate was the pathogenic species P. asymbiotica subsp. australis. H. indica was the major EPN host for Photorhabdus. This study reveals the genetic diversity of Xenorhabdus and Photorhabdus spp. and describes new associations between EPNs and their bacterial symbionts in Thailand.
doi:10.1371/journal.pone.0043835
PMCID: PMC3440396  PMID: 22984446
14.  Impact of a Nematode-parasitic Fungus on the Effectiveness of Entomopathogenic Nematodes 
Journal of Nematology  1992;24(1):1-8.
The impact of the nematode-parasitic fungus Hirsutella rhossiliensis on the effectiveness of Steinernema carpocapsae, S. glaseri, and Heterorhabditis bacteriophora against Galleria mellonella larvae was assessed in the laboratory. The presence of Hirsutella conidia on the third-stage (J3) cuticle of S. carpocapsae and H. bacteriophora interfered with infection of insect larvae. Conidia on the J3 cuticle of S. glaseri and on the ensheathing second-stage cuticle of H. bacteriophora did not reduce the nematodes' ability to infect larvae. The LD₅₀ values for S. carpocapsae, S. glaseri, and H. bacteriophora in sand containing H. rhossiliensis were not different from those in sterilized sand when Galleria larvae were added at the same time as the nematodes. However, when Galleria larvae were added 3 days after the nematodes, the LD₅₀ of S. glaseri was higher in Hirsutella-infested sand than in sterilized sand, whereas the LD₅₀ of H. bacteriophora was the same in infested and sterilized sand. Although the LD₅₀ of S. carpocapsae was much higher in Hirsutella-infested sand than in sterilized sand, the data were too variable to detect a significant difference. These data suggest that H. bacteriophora may be more effective than Steinernema species at reducing insect pests in habitats with abundant nematode-parasitic fungi.
PMCID: PMC2619251  PMID: 19283194
biological control; entomopathogenic nematode; fungus; Heterorhabditis; Hirsutella rhossiliensis; nematode; nematophagous fungus; Steinernema
15.  Interspecific Nematode Signals Regulate Dispersal Behavior 
PLoS ONE  2012;7(6):e38735.
Background
Dispersal is an important nematode behavior. Upon crowding or food depletion, the free living bacteriovorus nematode Caenorhabditis elegans produces stress resistant dispersal larvae, called dauer, which are analogous to second stage juveniles (J2) of plant parasitic Meloidogyne spp. and infective juveniles (IJ)s of entomopathogenic nematodes (EPN), e.g., Steinernema feltiae. Regulation of dispersal behavior has not been thoroughly investigated for C. elegans or any other nematode species. Based on the fact that ascarosides regulate entry in dauer stage as well as multiple behaviors in C. elegans adults including mating, avoidance and aggregation, we hypothesized that ascarosides might also be involved in regulation of dispersal behavior in C. elegans and for other nematodes such as IJ of phylogenetically related EPNs.
Methodology/Principal Findings
Liquid chromatography-mass spectrometry analysis of C. elegans dauer conditioned media, which shows strong dispersing activity, revealed four known ascarosides (ascr#2, ascr#3, ascr#8, icas#9). A synthetic blend of these ascarosides at physiologically relevant concentrations dispersed C. elegans dauer in the presence of food and also caused dispersion of IJs of S. feltiae and J2s of plant parasitic Meloidogyne spp. Assay guided fractionation revealed structural analogs as major active components of the S. feltiae (ascr#9) and C. elegans (ascr#2) dispersal blends. Further analysis revealed ascr#9 in all Steinernema spp. and Heterorhabditis spp. infected insect host cadavers.
Conclusions/Significance
Ascaroside blends represent evolutionarily conserved, fundamentally important communication systems for nematodes from diverse habitats, and thus may provide sustainable means for control of parasitic nematodes.
doi:10.1371/journal.pone.0038735
PMCID: PMC3368880  PMID: 22701701
16.  Hemocyte Responses of the Colorado Potato Beetle, Leptinotarsa decemlineata, and the Greater Wax Moth, Galleria mellonella, to the Entomopathogenic Nematodes, Steinernema feltiae and Heterorhabditis bacteriophora  
Hemocyte encapsulation reactions of infective juveniles of two Iranian isolates of the entomopathogenic nematodes, Heterorhabditis bacteriophora Poinar (Rhabditina: Heterorhabditidae) and Steinernema feltiae Filipjev (Tylenchina: Steinernematidae), were compared in the economic pest Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), and the greater wax moth, Galleria mellonella L. (Lepidoptera: Pyralidae). The former was a more responsive host than the latter and the hemocyte responses occurred sooner and more extensively. Complete encapsulation of some of the nematodes occurred by 4 h post injection for H. bacteriophora in both L. decemlineata and G. mellonella, and by 2 h pi for S. feltiae in L. decemlineata. The percentage of encapsulation from 24 h to 72 h pi in L. decemlineata was 86.2% for S. feltiae and 39% for H. bacteriophora. In G. mellonella there were no encapsulation or melanization responses against S. feltiae, whereas when H. bacteriophora was encapsulated and melanized (16.7%) the encapsulation level was lower than in L. decemlineata. This study may contribute to effectively selecting entomopathogenic nematode species active against significant economic pests based on the latter's cellular immune response.
doi:10.1673/031.011.7501
PMCID: PMC3281463  PMID: 21867441
cellular encapsulation; insect; melanization; resistant host
17.  Steinernema feltiae Intraspecific Variability: Infection Dynamics and Sex-Ratio 
Journal of Nematology  2014;46(1):35-43.
Entomopathogenic nematodes (EPNs) from the Heterorhabditidae and Steinernematidae families are well-known biocontrol agents against numerous insect pests. The infective juveniles (IJs) are naturally occurring in the soil and their success in locating and penetrating the host will be affected by extrinsic/intrinsic factors that modulate their foraging behavior. Characterizing key traits in the infection dynamics of EPNs is critical for establishing differentiating species abilities to complete their life cycles and hence, their long-term persistence, in different habitats. We hypothesized that phenotypic variation in traits related to infection dynamics might occur in populations belonging to the same species. To assess these intraspecific differences, we evaluated the infection dynamics of 14 populations of Steinernema feltiae in two experiments measuring penetration and migration in sand column. Intraspecific variability was observed in the percentage larval mortality, time to kill the insect, penetration rate, and sex-ratio in both experiments (P < 0.01). Larval mortality and nematode penetration percentage were lower in migration experiments than in penetration ones in most of the cases. The sex-ratio was significantly biased toward female-development dominance (P < 0.05). When the populations were grouped by habitat of recovery (natural areas, crop edge, and agricultural groves), nematodes isolated in natural areas exhibited less larval mortality and penetration rates than those from some types of agricultural associated soils, suggesting a possible effect of the habitat on the phenotypic plasticity. This study reinforces the importance of considering intraspecific variability when general biological and ecological questions are addressed using EPNs.
PMCID: PMC3957570  PMID: 24644369
entomopathogenic nematode; female-biased; migration assay; penetration assay; sex ratio; Steinernema feltiae
18.  Natural Occurrence of Entomogenous Nematodes in Tennessee Nursery Soils 
Journal of Nematology  1993;25(2):181-188.
To isolate potential insect biocontrol agents, entomogenous nematodes were surveyed in Tennessee plant nurseries in 1991. Soil samples from 113 nursery sites were baited with greater wax moth (Galleria mellonella) larvae, house cricket (Acheta domesticus) adults, lesser mealworm (Alphitobius diaperings) adults, and house fly (Musca domestica) larvae. Heterorhabditis bacteriophora and Steinernema carpocapsae were each recovered from 17 soil samples. Heterorhabditis bacteriophora was more common in habitats with crape myrtle (Lagerstroemia indica) and Chinese juniper (Juniperus chinensis) than other nursery plants, and S. carpocapsae was more frequently recovered from habitats with juniper and Southern magnolia (Magnolia grandiflora). Bulk density, electrical conductivity, organic matter, pH, temperature, and moisture content of the entomogenous-nematode positive soil samples were compared. Other nematode genera recovered with insect baits included Rhabditis sp., Pelodera sp., Cryptaphelenchoides sp., and Mesodiplogaster sp., which was recovered from a greater percentage of soil samples than the other five genera.
PMCID: PMC2619373  PMID: 19279756
Acheta; Alphitobius; biological control; Cryptaphelenchoides; distribution; entomogenous nematode; Heterorhabditis; Mesodiplogaster; Musca; nursery plant; Pelodera; Rhabditis; Steinernema; survey
19.  Evaluation of the efficacy of three indigenous strains of entomopathogenic nematodes from Meghalaya, India against mustard sawfly, Athalia lugens proxima Klug (Hymenoptera: Tenthredinidae) 
The objective of this study was to evaluate the efficacy of three indigenous strains of entomopathogenic nematodes (EPN) from Meghalaya, India, namely Heterorhabditis indica Poinar, Karunakar and David, Steinernema thermophilum Ganguly and Singh, and Steinernema glaseri (Steiner) against the last instar larva of mustard sawfly, Athalia lugens proxima Klug, a serious pest of mustard and radish in India. The larvae of A. lugens proxima were exposed to 10, 25, 50, 75 and 100 infective juveniles (IJs) concentration of each nematode species in Petri dishes. Percentage larval mortality and nematode reproduction in insect larvae was studied. The sawfly larvae were found to be susceptible to all the three EPNs tested, but the degree of susceptibility to infection varied from among nematode species. Based on LC50 value, H. indica was the most pathogenic species. Nevertheless, S. thermophilum and S. glaseri also showed a high insect mortality. This study also revealed that all the three test nematodes are also able to propagate in the host cadaver and produce first generation infective juveniles. However, H. indica produced significantly more number of IJs per insect larva than the other two nematode species. The progeny production was recorded to be the least in case of S. glaseri. In conclusion, our findings suggest that of the three indigenous EPNs studied, H. indica and S. thermophilum have good potential as biological control agents against mustard sawfly, A. lugens proxima.
doi:10.1007/s12639-012-0099-y
PMCID: PMC3427662  PMID: 24082523
Entomopathogenic nematodes; Biological control; Mustard sawfly; Athalia lugens proxima Klug; Heterorhabditis indica; Steinernema thermophilum; Steinernema glaseri; Meghalaya; India
20.  Efficacy of indigenous entomopathogenic nematodes from Meghalaya, India against the larvae of taro leaf beetle, Aplosonyx chalybaeus (Hope) 
The efficacy of three entomopathogenic nematode (EPN) species, Heterorhabditis indica, Steinernema thermophilum, and S. glaseri, from Meghalaya, India was studied against the larvae of taro leaf beetle, Aplosonyx chalybaeus (Hope) (Coleoptera: Chrysomelidae), under the laboratory conditions. The beetle larvae (grubs) were exposed to 25, 50, 75, 100 and 200 infective juveniles (IJs) of each nematode species for different time periods and they were found to be susceptible to all the EPNs tested. However, the susceptibility of grubs to nematode infection varied according to the dosages of IJs and their exposure periods. Appreciably good performance was achieved by S. glaseri, which showed 100 % mortality of insect larvae in 48 h exposure time. At 48 h of incubation, its LC50 value was 90.3 IJs/larva, which was lower than that of S. thermophilum (115.0 IJs/larva) and H. indica (186.0 IJs/larva), at the same exposure time. All the tested nematode species were also found to reproduce within the host and produced infective juveniles. H. indica, however, showed comparatively more production of IJs per cadaver of infected host (168.9 × 103 IJs/larva), as compared to the other two tested nematode species. The production of IJs per cadaver of infected host by S. thermophilum was recorded to be 82.0 × 103 IJs/larva. In case of S. glaseri, while production of IJs increased initially to 18.9 × 103 IJs/larva at concentration of 100 IJs/larva, it declined thereafter to 14.7 × 103 IJs/larva at the dose of 200 IJs/larva. In conclusion, the evidence obtained in this study suggests that all the three indigenous EPN species are virulent enough to produce 100 % mortality in the last instar larvae of A. chalybaeus. These EPN species thus have potential scope for the management of A. chalybaeus in taro crops.
doi:10.1007/s12639-012-0139-7
PMCID: PMC3427670  PMID: 24082518
Aplosonyx chalybaeus; Biological control; Entomopathogenic nematodes; Heterorhabditis indica; Steinernema glaseri; Steinernema thermophilum; Taro
21.  Influence of Salinity on Survival and Infectivity of Entomopathogenic: Nematodes 
Journal of Nematology  1994;26(3):345-351.
Exposure to NaC1, KCI, and CaCl₂ affected the entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema glaseri differently. Survival, virulence, and penetration efficiency of S. glaseri were not affected by these salts. At high concentrations, however, all three salts inhibited its ability to move through a soil column and locate and infect a susceptible host. Calcium chloride and KCl had no effect on H. bacteriophora survival, penetration efficiency, or movement through a soil column, but moderate concentrations of these salts enhanced H. bacteriophora virulence. NaCl, however, adversely affected each of these parameters at high salinities (>16 dS/m). Salt effects on S. glaseri are attributed solely to interference with nematode host-finding ability, whereas the NaCl effects on H. bacteriophora are attributed to its toxicity and possibly to interference with host-finding behavior.
PMCID: PMC2619511  PMID: 19279902
Entomopathogenic nematode; Heterorhabditis bacteriophora; infectivity; nematode; salinity; survival; Steinernema glaseri
22.  Control of the Oriental Fruit Moth, Grapholita molesta, Using Entomopathogenic Nematodes in Laboratory and Fruit Bin Assays 
Journal of nematology  2006;38(1):168-171.
The oriental fruit moth (OFM), Grapholita molesta (Busck), which is among the most important insect pests of peaches and nectarines, has developed resistance to a wide range of insecticides. We investigated the ability of the entomopathogenic nematodes (EPN) Steinernema carpocapsae (Weiser), S. feltiae (Filipjev), S. riobrave (Cabanillas et al.), and Heterorhabditis marelatus (Liu and Berry) to control OFM under laboratory and fruit bin conditions. At a dosage of 10 infective juveniles (IJ)/cm2 in the laboratory, S. carpocapsae caused 63%, S. feltiae 87.8%, S. riobrave 75.6%, and H. marelatus 67.1% OFM mortality. All four nematode species caused significant OFM larval mortality in comparison to the nontreated controls. Steinernema feltiae was used for the bin assays due to the higher OFM mortality it caused than the other tested EPN species and to its ability to find OFM under cryptic environments. Diapausing cocooned OFM larvae in miniature fruit bins were susceptible to IJ of S. feltiae in infested corner supports and cardboard strips. Treatment of bins with suspensions of 10 or 25 S. feltiae IJ/ml water with wetting agent (Silwet L77) resulted in 33.3 to 59% and 77.7 to 81.6% OFM mortality in corner supports and cardboard strips, respectively. This paper presents new information on the use of EPN, specifically S. feltiae, as nonchemical means of OFM control.
PMCID: PMC2586428  PMID: 19259443
Biological control; cardboard strips; fruit bins; Grapholita molesta; entomopathogenic nematodes; Heterorhabditis marelatus; oriental fruit moth; Steinernema carpocapsae; S. feltiae; S. riobrave; wetting agent
23.  A Comparison of Entomopathogenic Nematode Longevity in Soil under Laboratory Conditions 
Journal of nematology  2006;38(1):119-129.
We compared the longevity of 29 strains representing 11 entomopathogenic nematode species in soil over 42 to 56 d. A series of five laboratory experiments were conducted with six to eight nematode strains in each and one or more nematode strains in common, so that qualitative comparisons could be made across experiments. Nematodes included Heterorhabditis bacteriophora (four strains), H. indica (Homl), H. marelatus (Point Reyes), H megidis (UK211), H. mexicana (MX4), Steinernema carpocapsae (eight strains), S. diaprepesi, S. feltiae (SN), S. glaseri (NJ43), S. rarum (17C&E), and S. riobrave (nine strains). Substantial within-species variation in longevity was observed in S. carpocapsae, with the Sal strain exhibiting the greatest survival. The Sal strain was used as a standard in all inter-species comparisons. In contrast, little intra-species variation was observed in S. riobrave. Overall, we estimated S. carpocapsae (Sal) and S. diaprepesi to have the highest survival capability. A second level of longevity was observed in H. bacteriophora (Lewiston), H. megidis, S. feltiae, and S. riobrave (3–3 and 355). Lower levels of survivability were observed in other H. bacteriophora strains (Hb, HP88, and Oswego), as well as S. glaseri and S. rarum. Relative to S. glaseri and S. rarum, a lower tier of longevity was observed in H. indica and H. marelatus, and in H. mexicana, respectively. Although nematode persistence can vary under differing soil biotic and abiotic conditions, baseline data on longevity such as those reported herein may be helpful when choosing the best match for a particular target pest.
PMCID: PMC2586445  PMID: 19259437
entomopathogenic; Heterorhabditis; longevity; nematode; persistence; soil; Steinernema
24.  Interspecific competition between entomopathogenic nematodes (Steinernema) is modified by their bacterial symbionts (Xenorhabdus) 
Background
Symbioses between invertebrates and prokaryotes are biological systems of particular interest in order to study the evolution of mutualism. The symbioses between the entomopathogenic nematodes Steinernema and their bacterial symbiont Xenorhabdus are very tractable model systems. Previous studies demonstrated (i) a highly specialized relationship between each strain of nematodes and its naturally associated bacterial strain and (ii) that mutualism plays a role in several important life history traits of each partner such as access to insect host resources, dispersal and protection against various biotic and abiotic factors. The goal of the present study was to address the question of the impact of Xenorhabdus symbionts on the progression and outcome of interspecific competition between individuals belonging to different Steinernema species. For this, we monitored experimental interspecific competition between (i) two nematode species: S. carpocapsae and S. scapterisci and (ii) their respective symbionts: X. nematophila and X. innexi within an experimental insect-host (Galleria mellonella). Three conditions of competition between nematodes were tested: (i) infection of insects with aposymbiotic IJs (i.e. without symbiont) of both species (ii) infection of insects with aposymbiotic IJs of both species in presence of variable proportion of their two Xenorhabdus symbionts and (iii) infection of insects with symbiotic IJs (i.e. naturally associated with their symbionts) of both species.
Results
We found that both the progression and the outcome of interspecific competition between entomopathogenic nematodes were influenced by their bacterial symbionts. Thus, the results obtained with aposymbiotic nematodes were totally opposite to those obtained with symbiotic nematodes. Moreover, the experimental introduction of different ratios of Xenorhabdus symbionts in the insect-host during competition between Steinernema modified the proportion of each species in the adults and in the global offspring.
Conclusion
We showed that Xenorhabdus symbionts modified the competition between their Steinernema associates. This suggests that Xenorhabdus not only provides Steinernema with access to food sources but also furnishes new abilities to deal with biotic parameters such as competitors.
doi:10.1186/1471-2148-6-68
PMCID: PMC1569874  PMID: 16953880
25.  Effect of Entomopathogenic Nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) on Meloidogyne mayaguensis Rammah and Hirschmann (Tylenchida: Meloidoginidae) Infection in Tomato Plants 
Journal of Nematology  2007;39(4):338-342.
Some studies suggest that entomopathogenic nematodes (EPN) affect plant-parasitic nematode populations. Here, the effects of live and dead IJ of Heterorhabditis bacteriophora JPM4, H. baujardi LPP7, Steinernema feltiae SN and S. carpocapsae All were evaluated against eggs and J2 of the plant-parasitic nematode Meloidogyne mayaguensis. According to treatment, 100 IJ were applied with 350 eggs, 350 J2 or 175 eggs + 175 J2 to tomato plants. Bioassays were conducted in March to May and repeated in September to November 2005. Both experiments lasted 9 weeks, and the variable evaluated was number of galls per plant. When eggs were used for infections in the first trial, plants exhibited lower gall number compared to control when live and dead H. baujardi IJ and live S. feltiae IJ were added (9.7, 4.5, 7.3 and 85.7 galls, respectively). In the second trial, live S. feltiae and S. carpocapasae IJ influenced gall formation compared to control (14.33, 14.57 and 168.02 galls, respectively). When J2 were used for infections, plants with live H. baujardi IJ presented less galls when compared to control in both trials (38.3 and 355.7 galls in the first trial and 145.2 and 326.2 in the second one, respectively). Infection with a mixture of J2 and eggs resulted in fewer galls than when live S. feltiae IJ were present in both trials, compared to control (38.3 and 44.2 galls vs. 275.3 and 192.2 galls, respectively). We conclude that H. baujardi and S. feltiae apparently may be inhibiting egg hatching and J2 infection.
PMCID: PMC2586509  PMID: 19259509
Entomopathogenic nematodes; nematode-nematode interaction; biological control; plant-parasitic nematode; Meloidogyne mayaguensis

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