The influence of habitat quality on the foraging strategies of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidis

Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, Aberdeen, AB24 3UU, UK.
Parasitology (Impact Factor: 2.56). 10/2009; 137(2):303-9. DOI: 10.1017/S0031182009991326
Source: PubMed


Entomopathogenic 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.

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    • "Their presence and abundance is associated with a number of biotic and abiotic soil characteristics, including soil texture, temperature and moisture (Lawrence et al., 2006), as well as a combination of additional physical, chemical and biotic conditions (Hoy et al., 2008). Applied EPNs have been found to disperse more actively in soils high in organic matter than they do in mineral soils (Kruitbos et al., 2010; MacMillan et al., 2009; Wilson et al., 2012) and their persistence is strongly correlated with high soil moisture (Grant and Villani, 2003; Jabbour and Barbercheck, 2008). The persistence of EPN populations after they have been applied as a biological insecticide also depends on the availability of invertebrate hosts within the soil environment (Susurluk and Ehlers, 2008). "
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    ABSTRACT: Soil habitat conditions that promote abundance and persistence of entomopathogenic nematodes (EPNs) might be encouraged by reduced tillage and compost amendments. We hypothesized that altered soil management with reduced tillage, cover crops (clover and barley), and compost (100 kg of N/ha), would increase survival and biocontrol services of EPNs, compared with conventional management. Field trials were conducted at the Ohio Agricultural Research and Development Center Muck Crops Research Station, Huron County, OH in 2010 and 2011. Plots were planted with carrots. EPNs, Heterorhabditis bacteriophora GPS11, were released and their survival was compared between the two soil management regimes by sampling over a period of 8 weeks using in situ bait traps containing Galleria mellonella. Repeated measures analysis of variance did not show significant differences between the two soil management regimes in the pattern of H. bacteriophora survival over time or during any evaluation in either year, except 2 weeks after cadaver application in 2010 when the EPN population was significantly greater in the conventional than in the alternative soil management regime. Although treatment effects were generally not significant, statistically significant increase in nematode population densities between the 2 years of the study, despite generally poor weather conditions following EPN release in the second year, provide encouraging evidence that populations of these biological control agents could increase in vegetable production fields. However, longer periods may be required for clearly distinguishable increase in EPN population density, persistence, and biological control services in the alternative soil management treatments.
    Biological Control 12/2014; 79. DOI:10.1016/j.biocontrol.2014.08.008 · 1.64 Impact Factor
    • "Torr et al. (2004) showed that S. carpocapsae had strong response to a wide range of vibrational cues. Recently Kruitbos et al. (2010) stated that S. carpocapsae is adapted to being active in habitats other than mineral soils (e.g., peat, leaf litter, bark or wood). Our results support this finding and also fit with the habitat preferences of this species; S. carpocapsae prefer woodlands where their soil habitats have much higher organic matter contents (Hominick, 2002). "
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    ABSTRACT: Rosaceae longhorned beetle, Osphranteria coerulescens, is an important pest of fruit trees that attacks all fruit trees belonging to the family Rosaceae in cold regions of Iran. The potential efficacy of two species of entomopathogenic nematodes (EPN), Heterorhabditis bacteriophora and Steinernema carpocapsae, against last instar larvae of this pest was tested under laboratory conditions. In plate assays, the larvae were susceptible to both EPN species but were more susceptible to S. carpocapsae (65.0-97.5% mortality) than H. bacteriophora (42.5-87.8%). Both nematode species were able to penetrate and reproduce within O. coerulescens larvae, but reproduction rate for H. bacteriophora was higher than those of S. carpocapsae; however, the penetration rate for S. carpocapsae was greater than H. bacteriophora. In a migration test on agar plate, S. carpocapsae showed negligible attraction to the pest or to Galleria mellonella cues. However, H. bacteriophora was strongly attracted to the sector of Petri dishes containing larvae. In a test using apricot tree branches, both species of EPN passed from mass frass of O. coerulescens larvae in the tip of the branches, penetrated into the larval galleries, and located and killed the larvae of O. coerulescens in their natural habitat deep inside the branches. Our findings provide the first insight into the biocontrol efficacy of EPN against O. coerulescens larvae, and highlight their potential for the control of this pest. Field experiments are needed to evaluate their potential under the environmental conditions in which rosaceae longhorned beetle larvae are found.
    Nematology 07/2014; DOI:10.1163/15685411-00002802 · 1.24 Impact Factor
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    • "In contrast, ambush foraging nematode species, such as Steinernema carpocapsae are characterized by low motility (Lewis et al. 1992; Campbell and Gaugler 1993) and lack of response to long-range host cues (Gaugler et al. 1989b; Lewis et al. 1993; Grewal et al. 1994b, 1997). Ambushers only respond to host volatile cues either after contact with the host cuticle (Lewis et al. 1995) or during bouts of standing on their tails (Campbell and Kaya 2002; Hallem et al. 2011), 924 Evol Ecol (2014) 28:923–939 123 Author's personal copy which has been referred to as nictation behavior (Campbell and Gaugler 1993) or tail standing (Kruitbos and Wilson 2010). Besides cruisers and ambushers, some EPN species are referred to as ''intermediate foragers'' (Grewal et al. 1994b), such as S. feltiae, that neither nictate like ambushers (Campbell and Gaugler 1993) nor respond to long-range host volatile cues like cruisers (Grewal et al. 1994b; Lewis et al. 1995). "
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    ABSTRACT: Dispersal of organisms is influenced by environmental and innate population variability. It results in redistribution of populations with potential consequences for gene flow population resilience and stability, and evolutionary diversification of traits in response to specific selection pressures. However, dispersal behavior in soil-dwelling organisms is understudied. Species of entomopathogenic nematodes, a group of soil inhabiting lethal insect parasites used in biological pest control show a dichotomy in foraging behavior. Some species have been classified as ambushers while others as cruisers. We previously discovered that the ambush foraging Steinernema carpocapsae possesses a small group of sprinters that disperse faster than the fastest moving cruisers. In this study, we genetically selected S. carpocapsae for enhanced dispersal in the absence of hosts by capturing the fastest and farthest reaching infective juveniles (IJs) emanating from a nematode-infected Galleria mellonella cadaver, in soil. S. carpocapsae showed positive response to selection for dispersal with 13–23 and 21–37 fold increase in the percent IJs dispersing to the farthest distance from the source cadaver, after five and ten rounds of selection, respectively. There was also a significant increase in the average displacement of the selected lines (6.85–7.54 cm/day) than the foundation population (5.54 cm/day) maintained by passing through G. mellonella larvae in Petri dishes. The overall mean realized heritability for dispersal was 0.60. The farthest reaching IJs of the selected lines comprised more males (72 %) than the foundation population (44 %) at most time points. Trade-offs associated with enhanced dispersal included reduced reproduction capacity and nictation ability, a trait associated with ambush foraging. In conclusion, this study revealed the costs and benefits associated with selection for enhanced dispersal in a soil-dwelling insect parasite, enhancing our understanding of the evolution of new behavioral patterns, which could have important implications in biological control.
    Evolutionary Ecology 04/2014; 28(5):923-939. DOI:10.1007/s10682-014-9706-y · 2.52 Impact Factor
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