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

Parasitology ◽  
1992 ◽  
Vol 105 (2) ◽  
pp. 309-315 ◽  
Author(s):  
E.E. Lewis ◽  
R. Gaugler ◽  
R. Harrison

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.

BMC Genomics ◽  
2019 ◽  
Vol 20 (1) ◽  
Author(s):  
Neil D. Warnock ◽  
Deborah Cox ◽  
Ciaran McCoy ◽  
Robert Morris ◽  
Johnathan J. Dalzell

Abstract Background Steinernema carpocapsae is an entomopathogenic nematode that employs nictation and jumping behaviours to find potential insect hosts. Here we aimed to investigate the transcriptional basis of variant host-finding behaviours in the infective juvenile (IJ) stage of three S. carpocapsae strains (ALL, Breton and UK1), with a focus on neuronal genes known to influence behaviour in other nematode species. Identifying gene expression changes that correlate with variant host-finding behaviours will further our understanding of nematode biology. Results RNA-seq analysis revealed that whilst up to 28% of the S. carpocapsae transcriptome was differentially expressed (P < 0.0001) between strains, remarkably few of the most highly differentially expressed genes (> 2 log2 fold change, P < 0.0001) were from neuronal gene families. S. carpocapsae Breton displays increased chemotaxis toward the laboratory host Galleria mellonella, relative to the other strains. This correlates with the up-regulation of four srsx chemosensory GPCR genes, and a sodium transporter gene, asic-2, relative to both ALL and UK1 strains. The UK1 strain exhibits a decreased nictation phenotype relative to ALL and Breton strains, which correlates with co-ordinate up-regulation of neuropeptide like protein 36 (nlp-36), and down-regulation of an srt family GPCR gene, and a distinct asic-2-like sodium channel paralogue. To further investigate the link between transcriptional regulation and behavioural variation, we sequenced microRNAs across IJs of each strain. We have identified 283 high confidence microRNA genes, yielding 321 predicted mature microRNAs in S. carpocapsae, and find that up to 36% of microRNAs are differentially expressed (P < 0.0001) between strains. Many of the most highly differentially expressed microRNAs (> 2 log2 fold, P < 0.0001) are predicted to regulate a variety of neuronal genes that may contribute to variant host-finding behaviours. We have also found evidence for differential gene isoform usage between strains, which alters predicted microRNA interactions, and could contribute to the diversification of behaviour. Conclusions These data provide insight to the transcriptional basis of behavioural variation in S. carpocapsae, supporting efforts to understand the molecular basis of complex behaviours in nematodes.


Parasitology ◽  
1996 ◽  
Vol 113 (5) ◽  
pp. 473-482 ◽  
Author(s):  
J. F. Campbell ◽  
E. Lewis ◽  
F. Yoder ◽  
R. Gaugler

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.


Nematology ◽  
2012 ◽  
Vol 14 (4) ◽  
pp. 389-394 ◽  
Author(s):  
Michael J. Wilson ◽  
Ralf-Udo Ehlers ◽  
Itamar Glazer

For many years, entomopathogenic nematodes have been classified as either ‘ambush’, ‘cruise’ or ‘intermediate’ foragers. Here, we critically examine the evidence that Steinernema carpocapsae, the most studied ‘ambush’ forager, does actually use an ambush foraging strategy in nature. We propose an alternative hypothesis for the characteristic behaviours of S. carpocapsae (and other supposed ‘ambush’ foragers) based on adaptation to habitats other than mineral soils in which S. carpocapsae can ‘cruise’. Several papers are reviewed in which S. carpocapsae was used successfully to control sedentary or cryptic pests in organic habitats, thus supporting our hypothesis. If this hypothesis is correct, it does not preclude S. carpocapsae (or any entomopathogenic nematode species) using an ambushing strategy under certain circumstances, but we believe on current evidence that the classification of S. carpocapsae as an ambush forager cannot be sustained.


Parasitology ◽  
1995 ◽  
Vol 110 (2) ◽  
pp. 207-213 ◽  
Author(s):  
E. E. Lewis ◽  
P. S. Grewal ◽  
R. Gaugler

SUMMARYThe importance of host cues to three species of steinernematid nematodes (Rhabdita: Steinernematidae) with different foraging strategies was compared. We presented host materials to nematodes in series to test responses to combinations of host cues. If a fixed hierarchy of cues is followed during foraging, parasites should respond most strongly to cues offered in natural order. Steinernema carpocapsae, an ambush forager, aggregated at the source of volatile host cues only after attachment to host cuticle. They also parasitized hosts more efficiently after contact with cuticle. Steinernema glaseri, a cruise forager, was unaffected by exposure to combinations of host cues. Steinernema feltiae, a nematode with characteristics of both ambushing and cruising, was affected by cue hierarchies when either contact or volatile cues were presented first. Host-associated materials encountered out of the context may not qualify as host cues for the ambush forager, S. carpocapsae. Perhaps the order in which cues are encountered is more predictable for ambushers than for cruisers. Therefore an ambusher's response to host materials has a more fixed contextual framework.


1996 ◽  
Vol 74 (1) ◽  
pp. 164-170 ◽  
Author(s):  
Robin J. Stuart ◽  
Randy Gaugler

Laboratory culture can have detrimental effects on populations through adverse environmental conditions such as poor nutrition or disease, or through genetic effects such as inbreeding depression, founder effect, genetic drift, or laboratory adaptation. We tested for laboratory effects on the entomopathogenic nematode Steinernema glaseri (Steiner) by forming a genetically diverse base population from a series of field isolates and rearing several independent lines through 12 cycles of laboratory culture, using larvae of the greater wax moth, Galleria mellonella (L.), or the Japanese beetle, Popillia japonica Newman, as hosts. Laboratory bioassays based on G. mellonella indicated that lines maintained with large breeding populations did not deteriorate but often showed significant increases in infectivity (15.3–48.0%), proportion of males (12.2–36.1%), and reproductive potential (39.0–160.4%). Lines reared on P. japonica larvae responded similarly to lines reared on G. mellonella but showed higher levels of reproductive potential. Two of three lines subjected to initial genetic bottlenecks to test for founder effects differed from other lines by showing very high infectivity but little change in sex ratio or reproductive potential. These results demonstrate that laboratory adaptation can produce dramatic changes in important biological attributes of these nematodes, but that a lack of genetic variation associated with founder effects can impede this process. Laboratory adaptation should be considered a potent factor when designing, interpreting, and comparing studies of this important group of biological control organisms.


2005 ◽  
Vol 95 (5) ◽  
pp. 473-482 ◽  
Author(s):  
S. Toepfer ◽  
C. Gueldenzoph ◽  
R.-U. Ehlers ◽  
U. Kuhlmann

AbstractEntomopathogenic nematode species available in Europe were screened for their efficacy against both the root-feeding larvae and silk-feeding adults of the western corn rootworm, Diabrotica virgifera virgifera LeConte. Laboratory screening tests were aimed at the selection of candidate biological control agents for the management of this invasive alien pest in Europe. Steinernema glaseri, S. arenarium, S. abassi, S. bicornutum, S. feltiae, S. kraussei, S. carpocapsae and Heterorhabditis bacteriophora were studied to determine their virulence against third instar larvae and adults of D. v. virgifera in small-volume arenas (using nematode concentrations of 0.5, 0.8, 7.9 and 15.9 infective juveniles cm–2). All nematode species were able to invade and propagate in D. v. virgifera larvae, but adults were rarely infected. At concentrations of 7.9 and 15.9 cm–2, S. glaseri, S. arenarium, S. abassi and H. bacteriophora caused the highest larval mortality of up to 77%. Steinernema bicornutum, S. abassi, S. carpocapsae and H. bacteriophora appeared to have a high propagation level, producing 5970±779, 5595±811, 5341±1177 and 4039±1025 infective juveniles per larva, respectively. Steinernema glaseri, S. arenarium, S. feltiae, S. kraussei and H. bacteriophora were further screened at a concentration of 16.7 nematodes cm–2 against third instar larvae in medium-volume arenas (sand-filled trays with maize plants). Heterorhabditis bacteriophora, S. arenarium and S. feltiae caused the highest larval mortality with 77±16.6%, 67±3.5%, and 57±17.1%, respectively. In a next step, criteria for rating the entomopathogenic nematode species were applied based on results obtained for virulence and propagation, and for current production costs and availability in Europe. These criteria were then rated to determine the potential of the nematodes for further field testing. Results showed the highest potential in H. bacteriophora, followed by S. arenarium and S. feltiae, for further testing as candidate biological control agents.


Parasitology ◽  
1994 ◽  
Vol 108 (2) ◽  
pp. 207-215 ◽  
Author(s):  
P. S. Grewal ◽  
E. E. Lewis ◽  
R. Gaugler ◽  
J. F. Campbell

SUMMARYForaging strategies of eight species of entomopathogenic nematodes were predicted from their response to host volatile cues and dispersal behaviour on 2-dimensional substrates. Positive directional response to chemical cues and similar distances travelled on smooth (agar) or nictation substrates (agar overlaid with sand grains) by Heterorhabditis bacterio-phora, Heterorhabditis megidis, Steinernema anomali, and Steinernema glaseri suggest their cruising approach to finding hosts. The absence of directional response and less distance travelled on nictation substrate, than on smooth agar by Steinernema carpocapsae and Steinernema scapterisci suggest their ambushing mode of foraging. Steinernema feltiae and Steinernema sp. responded directionally to host volatiles, but travelled less distance on the nictation substrate than on smooth agar; the two species also did not nictate. The cruiser species located hosts more effectively in the sand columns, whereas the ambushers were more effective at finding hosts on filter paper. Steinernema feltiae and Steinernema sp. performed equally on filter paper and in the sand column. We conclude that H. bacteriophora, H. megidis, S. anomali and S. glaseri cruise to find hosts, whereas S. carpocapsae and S. scapterisci ambush hosts. Steinernema feltiae and Steinernema sp. are intermediary in the search continuum sharing some characteristics of both ambush and cruise foragers.


Parasitology ◽  
2009 ◽  
Vol 137 (2) ◽  
pp. 303-309 ◽  
Author(s):  
L. M. KRUITBOS ◽  
S. HERITAGE ◽  
S. HAPCA ◽  
M. J. WILSON

SUMMARYEntomopathogenic nematodes (EPN) are soil-transmitted parasites and their foraging strategies are believed to range from ‘ambush’ to ‘cruise’ foragers. However, research on their behaviour has not considered the natural habitat of these nematodes. We hypothesized that EPN behaviour would be influenced by soil habitat quality and tested this hypothesis using 2 EPN species Steinernema carpocapsae (an ‘ambusher’) and Heterorhabditis megidis (a ‘cruiser’) in 2 contrasting habitats, sand and peat. As predicted from previous studies, in sand most S. carpocapsae remained at the point of application and showed no taxis towards hosts, but in peat S. carpocapsae dispersed much more and showed a highly significant taxis towards hosts. H. megidis dispersed well in both media, but only showed taxis towards hosts in sand. In outdoor mesocosms in which both species were applied, S. carpocapsae outcompeted H. megidis in terms of host finding in peat, whereas the opposite was true in sand. Our data suggest that these 2 EPN may be habitat specialists and highlight the difficulties of studying soil-transmitted parasites in non-soil media.


2016 ◽  
Vol 30 (2) ◽  
pp. 78
Author(s):  
Masaaod Zolfagharian ◽  
Ayatollah Saeedizadeh ◽  
Habib Abbasipour

The diamondback moth, <em>Plutella xylostella</em> (L.) (Lepidoptera: Plutellidae) is an important pest of cruciferous crops in Iran. The susceptibility of <em>P. xylostella</em> larvae to two species of entomopathogenic nematodes (EPNs) (<em>Steinernema carpocapsae</em> and <em>Heterorhabditis bacteriophora</em>) was examined under laboratory conditions. Leaf bioassays were conducted to evaluate the nematode's capability to reach the larvae and kill them. High larval mortality (72.6-96%) was observed in laboratory experiments. The ET<sub>50</sub> of <em>H. bacteriophora</em> was higher than that of <em>S. carpocapsae</em>. The ET<sub>50</sub> of entomopatpgenic nematodes, <em>H. bacteriophora</em> and <em>S. carpocapsae</em> tested ranged from 21 to 139.7 and 11.3 to 71.4 hours, respectively. The effect of both factors infective juveniles (IJs) and exposure time of 50% (ET50) on the larval mortality was significant (df = 6; P &lt; 0.001) and (df = 2; P &lt; 0.001), respectively. This study revealed that entomopatogenic nematodes (EPNs) have great potential that should be exploited in diamondback moth, <em>P. xylostella</em> management.


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