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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: 2.35). 10/2009; 137(2):303-9. DOI: 10.1017/S0031182009991326
Source: PubMed

ABSTRACT 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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    • "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 · 2.37 Impact Factor
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    • "Similarly, Kruitbos et al. (2010) also compared EPN foraging in peat and sand and for H. megidis found that it " dispersed well in both media, but only showed taxis towards hosts in sand " . These observations match well with the results from the diffusion experiments and imply that the effectiveness of the signals may be greatly impaired in soil types that contain high levels of chemical activity. "
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    ABSTRACT: Background Entomopathogenic nematodes (EPNs) are tiny parasitic worms that parasitize insects, in which they reproduce. Their foraging behavior has been subject to numerous studies, most of which have proposed that, at short distances, EPNs use chemicals that are emitted directly from the host as host location cues. Carbon dioxide (CO2) in particular has been implicated as an important cue. Recent evidence shows that at longer distances several EPNs take advantage of volatiles that are specifically emitted by roots in response to insect attack. Studies that have revealed these plant-mediated interactions among three trophic levels have been met with some disbelief. Scope This review aims to take away this skepticism by summarizing the evidence for a role of root volatiles as foraging cues for EPNs. To reinforce our argument, we conducted olfactometer assays in which we directly compared the attraction of an EPN species to CO2 and two typical inducible root volatiles. Conclusions The combination of the ubiquitous gas and a more specific root volatile was found to be considerably more attractive than one of the two alone. Hence, future studies on EPN foraging behavior should take into account that CO2 and plant volatiles may work in synergy as attractants for EPNs. Recent research efforts also reveal prospects of exploiting plant-produced signals to improve the biological control of insect pests in the rhizosphere.
    Plant and Soil 09/2012; 358(1-2):1-10. DOI:10.1007/s11104-012-1295-3 · 3.24 Impact Factor
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    • "While there is no doubt that species such as S. carpocapsae engage in behaviors such as standing and jumping that are suited for attaching to mobile hosts at the soil surface (Campbell and Gaugler, 1993; Campbell and Kaya, 2002), it is also clear that this should not preclude them from use against subterranean pests. Kruitbos et al. (2010) have criticized the description of S. carpocapsae as an ambush forager, and propose instead that this species is a habitat specialist, adapted to organic media such as peat or leaf litter. They showed that IJs moved towards hosts more readily in peat than in sand, and suggested that the reason why S. carpocapsae typically remains near the surface is because it does not move well through the mineral soils or the pure sands frequently used in experiments. "
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    ABSTRACT: 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.
    Journal of nematology 06/2012; 44(2):177-184. · 0.69 Impact Factor
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