Variation in entomopathogenic nematode (Steinernematidae and Heterorhabditidae) infective-stage jumping behaviour

AbstractSpecies and strains of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) were assessed for the expression of standing and jumping behaviour. Jumping occurred in 11 species of Steinernema, but the rate of jumping varied considerably among the species. Variation in the duration of crawling bouts, the tendency to body wave, the rate of standing, the duration of standing bouts, and the tendency to jump after standing contributed to the differences in frequency of jumping among species. Within a species, nematodes that jumped were similar in size, infectivity and sex ratio to those that did not jump, but jumpers tended to be more infective and to have lost their sheath (i.e., the second stage cuticle). This comparison of species is an important first step in assessing the adaptive value of jumping behaviour as part of the foraging strategies of entomopathogenic nematodes.

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Sex and the dynamics of infection in the entomopathogenic nematode Steinernema feltiae

Journal of Helminthology ◽

10.1017/s0022149x00015911 ◽

1997 ◽

Vol 71 (3) ◽

pp. 197-202 ◽

Cited By ~ 12

Author(s):

D.A. Bohan ◽

W.M. Hominick

Keyword(s):

Sex Ratio ◽

Entomopathogenic Nematodes ◽

Galleria Mellonella ◽

Entomopathogenic Nematode ◽

Steinernema Feltiae ◽

Infective Juvenile ◽

Infective Stage ◽

Male And Female ◽

Per Capita ◽

Infection Interaction

AbstractAn infection experiment was conducted to assess the change in the proportions of Steinernema feltiae Filipjev (Site 76 strain) infective juveniles becoming male or female on exposure to the test host Galleria mellonella L. Using a mathematical model for the infection interaction, the per capita probability of penetration per unit time (transmission coefficient), for those juveniles becoming male or female, and the magnitude of the male and female classes in the infective juvenile pool were estimated. The results show that S. feltiae infective juveniles which subsequently become female have a greater probability of invasion into test hosts than their male counterparts, which leads to markedly female biased sex ratios during the initial stages of the infection interaction. As the infection progresses, however, it was found that the sex ratio became balanced. This was because the underlying sex ratio in the infective stage pool was balanced. The implications of this dynamism in the sex ratio of the entomopathogenic nematodes are discussed with respect to the infection interaction, transmission and the likely environment in which the infective juveniles reside.

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Changes in foraging behaviour during the infective stage of entomopathogenic nematodes

Parasitology ◽

10.1017/s0031182000065306 ◽

1995 ◽

Vol 110 (5) ◽

pp. 583-590 ◽

Cited By ~ 25

Author(s):

E. E. Lewis ◽

S. Selvan ◽

J. F. Campbell ◽

R. Gaugler

Keyword(s):

Metabolic Rate ◽

Entomopathogenic Nematodes ◽

Storage Period ◽

Foraging Strategy ◽

Heterorhabditis Bacteriophora ◽

Steinernema Carpocapsae ◽

Foraging Strategies ◽

Infective Juvenile ◽

Infective Stage ◽

Energy Reserves

SUMMARYStudies of foraging strategies are often complicated by competing goals of the forager. In contrast, non-feeding infective juvenile entomopathogenic nematodes forage exclusively for a single host. Two questions were posed: (1) what is the relationship between metabolic rate, energy reserves and foraging strategy and (2) when a foraging strategy fails, will an infective-stage parasite switch strategies? Three species of entomopathogenic nematodes were stored in water and changes in their behaviour, metabolic rate, energy reserves, and infectivity were measured throughout the storage period. Steinernema carpocapsae ambushes insect hosts, whereas S. glaseri and Heterorhabditis bacteriophora cruise forage. Steinernema carpocapsae was least active and had the lowest metabolic rate. Heterorhabditis bacteriophora was more active and had the highest metabolic rate. Steinernema glaseri was most active and had an intermediate metabolic rate. Neither cruising species changed foraging strategy. Steinernema carpocapsae decreased nictation (a behaviour associated with ambushing only) and increased their locomotory rate. Any change in searching strategy occurred without assessment of the profitability or distribution of potential hosts, but the advantage this confers is unknown.

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Entomopathogenic nematode (Heterorhabditidae and Steinernematidae) spatial distribution in turfgrass

Parasitology ◽

10.1017/s0031182000081543 ◽

1996 ◽

Vol 113 (5) ◽

pp. 473-482 ◽

Cited By ~ 50

Author(s):

J. F. Campbell ◽

E. Lewis ◽

F. Yoder ◽

R. Gaugler

Keyword(s):

Spatial Distribution ◽

Vertical Distribution ◽

Entomopathogenic Nematodes ◽

Entomopathogenic Nematode ◽

Soil Surface ◽

Nematode Species ◽

Horizontal Distribution ◽

Steinernema Carpocapsae ◽

Foraging Strategies ◽

Temporal And Spatial Distribution

SUMMARYUnderstanding the temporal and spatial distribution of entomopathogenic nematodes is essential for determining the role of these insect parasites in soil communities and ultimately for their use in suppression of pest insect populations. We measured the vertical and horizontal distribution of endemic populations of entomopathogenic nematodes (Steinernema carpocapsae and Heterorhabditis bacteriophord) in turfgrass. Vertical distribution was determined by taking soil cores every 3 h from 05.00 to 23.00 h, over 4 days, and dividing the cores into 8, 1 cm deep sections. Steinernema carpocapsae was recovered primarily near the soil surface: 50% of positive sections were recovered in the thatch or first 1 cm of soil. S. carpocapsae recovery was lower during the middle of the day and none were recovered in the upper section. H. bacteriophora was recovered uniformly throughout the top 8 cm of soil and its vertical distribution did not change over the course of the day. Horizontal distribution was measured as the number of nematodes recovered from cores taken from 12 randomly selected 0·3 × 0·8 m sections from within four 15·3 × 15·3 m plots. Samples were collected biweekly over a 9-month period. H. bacteriophora had a patchier distribution than S. carpocapsae and both nematode species had more patchy distributions then their potential hosts. Our results support the hypothesis that these two species of nematode utilize different foraging strategies; S. carpocapsae primarily a surface adapted ambusher and H. bacteriophora as a cruise forager.

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Virulence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) for the control of Diabrotica speciosa germar (coleoptera: chrysomelidae)

Ciência e Agrotecnologia ◽

10.1590/s1413-70542011000600015 ◽

2011 ◽

Vol 35 (6) ◽

pp. 1149-1156 ◽

Cited By ~ 6

Author(s):

Viviane Santos ◽

Alcides Moino Junior ◽

Vanessa Andaló ◽

Camila Costa Moreira ◽

Ricardo Alves de Olinda

Keyword(s):

Biological Control ◽

Entomopathogenic Nematodes ◽

Entomopathogenic Nematode ◽

Larval Mortality ◽

Steinernema Glaseri ◽

Soil Insects ◽

Diabrotica Speciosa ◽

Pupal Mortality

Entomopathogenic nematodes (EPNs) are used in biological control of soil insects and show promise in the control of D. speciosa. The objective of this work was to evaluate the potential of native and exotic entomopathogenic nematode isolates in the control of D. speciosa under laboratory and greenhouse conditions. Results showed that all of EPNs caused larval mortality. The most virulent were Heterorhabditis sp. RSC01 (94%), Steinernema glaseri (84%), Heterorhabditis sp. JPM04 (82%) and Heterorhabditis amazonensis RSC05 (78%). There was no effect of the Heterorhabditis sp. RSC01 and S. glaseri isolates on eggs. The maximum mortality of D. speciosa larvae by Heterorhabditis sp. RSC01 was observed at a concentration of 300 IJ/ insect, while by S. glaseri observed the highest mortality at the concentration of 200 IJ/ insect. The Heterorhabditis sp. RSC01 isolate caused over 80% pupal mortality at a concentration of 250 IJ/insect. The virulence of Heterorhabditis sp. RSC01 and S. glaseri was affected by temperature. The Heterorhabditis sp. RSC01 isolate caused reduction in larva survival under greenhouse conditions at all of the tested concentrations and there was no difference in mortality among different concentrations of infectid juveniles.

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Entomopathogenic nematode host finding: response to host contact cues by cruise and ambush foragers

Parasitology ◽

10.1017/s0031182000074230 ◽

1992 ◽

Vol 105 (2) ◽

pp. 309-315 ◽

Cited By ~ 127

Author(s):

E.E. Lewis ◽

R. Gaugler ◽

R. Harrison

Keyword(s):

Entomopathogenic Nematode ◽

Nematode Species ◽

Host Finding ◽

Steinernema Carpocapsae ◽

Foraging Strategies ◽

Popillia Japonica ◽

Search Behaviour ◽

Search Area ◽

Steinernema Glaseri ◽

Host Cues

SUMMARYSearch behaviour of two entomopathogenic nematode species with different foraging strategies was compared by measuring parameters of unrewarded search after contact with host cues. Steinernema glaseri cruises in search of hosts. Steinernema carpocapsae ambushes hosts. Nematodes should respond to contact with relevant host cues by shifting their search from ranging to localized after contact with them. We predicted that cruising foragers rely on chemical cues more heavily than ambushers. These species were also tested for host affinities. Nematodes were tracked by image analysis after exposure to faeces, cuticle or food of either Popillia japonica or Spodoptera exiqua. Steinernema glaseri responded to selected host cues by shifting from ranging to localized search, characterized by decreased locomotory rate, distance travelled, search area and the proportion of the test period spent moving. Steinernema carpocapsae did not respond to host cues. Steinernema glaseri responds to selected chemical host cues for host location, whereas S. carpocapsae does not.

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Dissemination of Isaria fumosorosea Spores by Steinernema feltiae and Heterorhabditis bacteriophora

Journal of Fungi ◽

10.3390/jof6040359 ◽

2020 ◽

Vol 6 (4) ◽

pp. 359

Author(s):

Jiří Nermuť ◽

Jana Konopická ◽

Rostislav Zemek ◽

Michal Kopačka ◽

Andrea Bohatá ◽

...

Keyword(s):

Entomopathogenic Nematodes ◽

Heterorhabditis Bacteriophora ◽

Potato Dextrose Agar ◽

Steinernema Feltiae ◽

Soil Organisms ◽

Isaria Fumosorosea ◽

Second Stage ◽

Glass Tubes ◽

First Time ◽

Globally Distributed

Entomopathogenic nematodes and fungi are globally distributed soil organisms that are frequently used as bioagents in biological control and integrated pest management. Many studies have demonstrated that the combination of biocontrol agents can increase their efficacy against target hosts. In our study, we focused on another potential benefit of the synergy of two species of nematodes, Steinernema feltiae and Heterorhabditis bacteriophora, and the fungus Isaria fumosorosea. According to our hypothesis, these nematodes may be able to disseminate this fungus into the environment. To test this hypothesis, we studied fungal dispersal by the nematodes in different arenas, including potato dextrose agar (PDA) plates, sand heaps, sand barriers, and glass tubes filled with soil. The results of our study showed, for the first time, that the spreading of both conidia and blastospores of I. fumosorosea is significantly enhanced by the presence of entomopathogenic nematodes, but the efficacy of dissemination is negatively influenced by the heterogeneity of the testing arena. We also found that H. bacteriophora spread fungi more effectively than S. feltiae. This phenomenon could be explained by the differences in the presence and persistence of second-stage cuticles or by different foraging behavior. Finally, we observed that blastospores are disseminated more effectively than conidia, which might be due to the different adherence of these spores (conidia are hydrophobic, while blastospores are hydrophilic). The obtained results showed that entomopathogenic nematodes (EPNs) can enhance the efficiency of fungal dispersal.

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Virulence of two entomopathogenic nematode species, Steinernema sp. (strain PQ16) and Heterorhabditis indica (strain KT3987), to nymphs of the coffee cicada Dundubia nagarasingna

Nematology ◽

10.1163/15685411-00003193 ◽

2019 ◽

Vol 21 (1) ◽

pp. 35-44 ◽

Cited By ~ 1

Author(s):

Chau N. Nguyen ◽

Anh T. Do ◽

Phap Q. Trinh ◽

Phuc K. Hoang

Keyword(s):

Biological Control ◽

Entomopathogenic Nematodes ◽

Entomopathogenic Nematode ◽

Nematode Species ◽

Mortality Rates ◽

Coffee Plantations ◽

Heterorhabditis Indica ◽

Inoculation Dose ◽

Pot Trial

Summary The virulence and efficacy of two species of entomopathogenic nematodes, Steinernema sp. (strain PQ16) and Heterorhabditis indica (strain KT3987), against nymphs of the coffee cicada, Dundubia nagarasingna, was evaluated under laboratory and glasshouse conditions. The highest mortality rates of coffee cicada nymphs caused by these two nematode strains were 93.5 and 100%, respectively, at an inoculation dose of 600 infective juveniles (IJ) nymph−1. The virulence (LC50) was established as 137.5 IJ and 149.1 IJ for strains S-PQ16 and H-KT3987, respectively. The highest IJ yields of these nematode strains were 66 × 103 IJ (for S-PQ16) and 134.4 × 103 IJ (for H-KT3987) at a dose of 500 IJ nymph−1. The efficacies of the two nematode strains to coffee cicadas at treated dose of 60 × 103 IJ pot−1 were 84.4 and 88.9% after 30 days, higher than the efficacies at treated dose of 40 × 103 IJ pot−1. The number of IJ in 250 ml of soil at 10, 20 and 30 days after treatment, increased from 0.38 × 103 to 4.80 × 103 IJ in soil treated with a dose of 40 × 103 IJ and from 0.66 × 103 to 5.02 × 103 IJ in soil treated with a dose of 60 × 103 IJ (for S-PQ16). Similarly, for H-KT3987 the number of IJ increased from 0.43 × 103 to 8.99 × 103 IJ and from 0.62 × 103 to 9.64 × 103 IJ, at the respective doses. Based on results of a pot trial from glasshouse modelling, an IJ application dosage for biological control of coffee cicada nymphs in coffee plantations was proposed.

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Bacteria from the Midgut of Common Cockchafer (Melolontha melolontha L.) Larvae Exhibiting Antagonistic Activity Against Bacterial Symbionts of Entomopathogenic Nematodes: Isolation and Molecular Identification

International Journal of Molecular Sciences ◽

10.3390/ijms21020580 ◽

2020 ◽

Vol 21 (2) ◽

pp. 580 ◽

Cited By ~ 2

Author(s):

Marcin Skowronek ◽

Ewa Sajnaga ◽

Małgorzata Pleszczyńska ◽

Waldemar Kazimierczak ◽

Magdalena Lis ◽

...

Keyword(s):

Gut Microbiota ◽

Entomopathogenic Nematodes ◽

Insect Pests ◽

Entomopathogenic Nematode ◽

Acinetobacter Calcoaceticus ◽

Inhibitory Effect ◽

Antagonistic Activity ◽

Reca Gene ◽

Melolontha Melolontha ◽

Insect Gut

The mechanisms of action of the complex including entomopathogenic nematodes of the genera Steinernema and Heterorhabditis and their mutualistic partners, i.e., bacteria Xenorhabdus and Photorhabdus, have been well explained, and the nematodes have been commercialized as biological control agents against many soil insect pests. However, little is known regarding the nature of the relationships between these bacteria and the gut microbiota of infected insects. In the present study, 900 bacterial isolates that were obtained from the midgut samples of Melolontha melolontha larvae were screened for their antagonistic activity against the selected species of the genera Xenorhabdus and Photorhabdus. Twelve strains exhibited significant antibacterial activity in the applied tests. They were identified based on 16S rRNA and rpoB, rpoD, or recA gene sequences as Pseudomonas chlororaphis, Citrobacter murliniae, Acinetobacter calcoaceticus, Chryseobacterium lathyri, Chryseobacterium sp., Serratia liquefaciens, and Serratia sp. The culture filtrate of the isolate P. chlororaphis MMC3 L3 04 exerted the strongest inhibitory effect on the tested bacteria. The results of the preliminary study that are presented here, which focused on interactions between the insect gut microbiota and mutualistic bacteria of entomopathogenic nematodes, show that bacteria inhabiting the gut of insects might play a key role in insect resistance to entomopathogenic nematode pressure.

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Evaluation of an Entomopathogenic Nematode and Chemical Insecticides for Control of Metamasius hemipterus sericeus (Coleoptera: Curculionidae)2

Journal of Entomological Science ◽

10.18474/0749-8004-31.3.240 ◽

1996 ◽

Vol 31 (3) ◽

pp. 240-251 ◽

Cited By ~ 9

Author(s):

R. M. Giblin-Davis ◽

J. E. Peña ◽

R. E. Duncan

Keyword(s):

Canary Island ◽

Entomopathogenic Nematodes ◽

Entomopathogenic Nematode ◽

Field Tests ◽

Effective Management ◽

The West ◽

Phoenix Canariensis ◽

Long Period ◽

Cryptic Habitat ◽

Metamasius Hemipterus

Several chemical insecticides and the entomopathogenic nematode, Steinernema carpocapsae (Weiser) (All strain), were evaluated for efficacy against the West Indian sugarcane weevil, Metamasius hemipterus sericeus (Olivier), in laboratory and field tests. Three different bioassays and a field study with sugarcane demonstrated that S. carpocapsae were efficacious against larvae but not adults of the weevil. These bioassays also demonstrated that adults of M. h. sericeus were killed by labelled rates of commercial formulations of acephate 75WP, carbofuran 2F, chlorpyrifos 4 EC, cyfluthrin 2 EC, disulfoton 15G, imidacloprid 2F, isofenphos 2I, lindane 25WP, and Vydate L. In a field test with weevil-infested Canary Island date palms, Phoenix canariensis Hortorum ex Chabaud, lindane (25 WP, 1.5 g AI/palm), and imidacloprid (75 WP, 1.2 g AI/palm) had the greatest effect on the percentage mortality of total weevils present per palm (> 60%) followed by S. carpocapsae (8 × 106 infective juveniles [IJs]/palm) (51%) and acephate (2.9 g AI/palm) (39%) which were statistically equal to the controls (14%). Control palms harbored over 200 M. h. sericeus per tree in the petioles and stem periphery. Because of the potential for high weevil production per palm and the cryptic habitat of the boring stages of this weevil, chemical insecticides and/or entomopathogenic nematodes will need to be applied frequently and over a long period of time for effective management.

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Host-Specific Activation of Entomopathogenic Nematode Infective Juveniles

Insects ◽

10.3390/insects9020059 ◽

2018 ◽

Vol 9 (2) ◽

pp. 59 ◽

Cited By ~ 7

Author(s):

Valentina Alonso ◽

Shyon Nasrolahi ◽

Adler Dillman

Keyword(s):

Entomopathogenic Nematodes ◽

Morphological Changes ◽

Entomopathogenic Nematode ◽

Infection Process ◽

Bacterial Symbiont ◽

Infective Juvenile ◽

Free Living ◽

Initial Infection ◽

Host Tissues ◽

Insect Parasites

Entomopathogenic nematodes (EPNs) are potent insect parasites and have been used for pest control in agriculture. Despite the complexity of the EPN infection process, hosts are typically killed within 5 days of initial infection. When free-living infective juveniles (IJs) infect a host, they release their bacterial symbiont, secrete toxic products, and undergo notable morphological changes. Collectively, this process is referred to as “activation” and represents the point in a nematode’s life cycle when it becomes actively parasitic. The effect of different host tissues and IJ age on activation, and how activation itself is related to virulence, are not well understood. Here, we employed a recently developed bioassay, which quantifies IJ activation, as a tool to address these matters. Appreciating that activation is a key part of the EPN infection process, we hypothesized that activation would positively correlate to virulence. Using the EPNs Steinernema carpocapsae and S. feltiae we found that EPN activation is host-specific and influenced by infective juvenile age. Additionally, our data suggest that activation has a context-dependent influence on virulence and could be predictive of virulence in some cases such as when IJ activation is especially low.

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