Edwin E. Lewis

Host finding behaviour as a predictor of foraging strategy in entomopathogenic nematodes

Foraging 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.

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

Search 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.

Activation of Akt Signaling Reduces the Prevalence and Intensity of Malaria Parasite Infection and Lifespan in Anopheles stephensi Mosquitoes

Malaria (Plasmodium spp.) kills nearly one million people annually and this number will likely increase as drug and insecticide resistance reduces the effectiveness of current control strategies. The most important human malaria parasite, Plasmodium falciparum, undergoes a complex developmental cycle in the mosquito that takes approximately two weeks and begins with the invasion of the mosquito midgut. Here, we demonstrate that increased Akt signaling in the mosquito midgut disrupts parasite development and concurrently reduces the duration that mosquitoes are infective to humans. Specifically, we found that increased Akt signaling in the midgut of heterozygous Anopheles stephensi reduced the number of infected mosquitoes by 60–99%. Of those mosquitoes that were infected, we observed a 75–99% reduction in parasite load. In homozygous mosquitoes with increased Akt signaling parasite infection was completely blocked. The increase in midgut-specific Akt signaling also led to an 18–20% reduction in the average mosquito lifespan. Thus, activation of Akt signaling reduced the number of infected mosquitoes, the number of malaria parasites per infected mosquito, and the duration of mosquito infectivity.

Ecology in the service of biological control: the case of entomopathogenic nematodes

Abstract Biological control manipulations of natural enemies to reduce pest populations represent large-scale ecological experiments that have both benefited from and contributed to various areas of modern ecology. Unfortunately, economic expediency and the need for rapid implementation often require that biological control programs be based more on trial and error than on sound ecological theory and testing. This approach has led to some remarkable successes but it has also produced dismal failures. This point is particularly well illustrated in the historical development and use of entomopathogenic nematodes for the biological control of insect pests. Intense effort has focused on developing these natural enemies as alternatives to chemical insecticides, in part because laboratory assays indicated that these nematodes possess a broad host range. This illusory attribute launched hundreds of field releases, many of which failed due to ecological barriers to infection that are not apparent from laboratory exposures, where conditions are optimal and host-parasite contact assured. For example, the entomopathogenic nematode Steinernema carpocapsae is a poor choice to control scarab larvae because this nematode uses an ambusher foraging strategy near the soil surface whereas the equally sedentary scarab remains within the soil profile, shows a weak host recognition response to scarabs, has difficulty overcoming the scarab immune response, and has low reproduction in this host. Conversely, two other nematodes, Heterorhabditis bacteriophora and S. glaseri, are highly adapted to parasitize scarabs: they use a cruising foraging strategy, respond strongly to scarabs, easily overcome the immune response, and reproduce well in these hosts. Increased understanding of the ecology of entomopathogenic nematodes has enabled better matches between parasites and hosts, and more accurate predictions of field performance. These results underline the importance of a strong partnership between basic and applied ecology in the area of biological control.

Biology and Behaviour

Entomopathogenic nematodes (EPNs) of the families Steinernematidae and Heterorhabditidae are lethal pathogens of insects. These pathogens contribute to the regulation of natural populations of insects, but the main interest in them is as an inundatively applied biocontrol agent. Their success in this role can be attributed to the unique partnership between a host-seeking nematode and a lethal insect-pathogenic bacterium. Because of their biocontrol potential, considerable attention has been directed over the past few decades to Heterorhabditis and Steinernema and their respective bacterial partners, Photorhabdus and Xenorhabdus.

Superior efficacy observed in entomopathogenic nematodes applied in infected-host cadavers compared with application in aqueous suspension.

Two greenhouse experiments were conducted to compare the efficacy of entomopathogenic nematodes applied in aqueous suspensions with application in infected cadavers. One experiment targeted the diaprepes root weevil Diaprepes abbreviatus with Heterorhabditis indica and the other targeted the black vine weevil Otiorhynchus sulcatus with H. bacteriophora. Entomopathogenic nematode application in infected cadavers were more effective than nematode application in aqueous suspensions in all cases. The increased efficacy observed in the cadaver applications may have been due to the additional physiological stress in the aqueous application (during temporary storage in water or upon application). Superior efficacy in the cadaver application might also have been due to compounds in the infected host cadaver that can enhance nematode infectivity.

The behavioural ecology of parasites.

Parasites have evolved numerous complex and fascinating ways of interacting with their hosts. The subject attracts the interest of numerous biologists from the perspective of ecology and behavioral biology, as well as from those concerned with more applied aspects of parasitology. However, until now there has been no recent book to synthesize this field. This book, written by leading authorities from the USA, Europe, Australia and New Zealand, provides the most comprehensive coverage of this important topic on the market.

Biochemical energy reserves of entomopathogenic nematodes

Quantitative and qualitative analyses of the biochemical energy reserves of 6 species of entomopathogenic nematodes (Rhabditida: Heterorhabditidae and Steinemematidae) were conducted. Lipid, glycogen, and protein contents of 2 species of Heterorhabditis (H. bacteriophora and H. megidis) and 4 species of Steinernema (S. carpocapsae, S.feltiae, S. glaseri, and S. scapterisci) were determined. The quantitative measurement of energy reserves (32-38% lipids and 42-46% proteins) suggested that entomopathogenic nematodes are more similar to free-living nematodes than to parasitic ones in this respect. These results also elucidate relationships between activity levels and life span from an energetic perspective

Entomopathogenic nematode (Heterorhabditidae and Steinernematidae) spatial distribution in turfgrass

Understanding 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 bacteriophora) 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 x 0.8 m sections from within four 15.3 x 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.

Response of infective stage parasites (Nematoda : Steinernematidae) to volatile cues from infected hosts

Volatile infochemicals play a significant role in the interactions between trophic levels. Volatile infochemicals may allow species within the third trophic level to avoid patches where conspecifics or heterospecifics are present. We show odor-mediated resource assessment by entomopathogenic nematodes in the family Steinernematidae. We hypothesized that the infective juvenile nematodes may reduce inter- and intraspecific competition by responding differently to unparasitized hosts vs. hosts parasitized by conspecific or heterospecific nematodes. All Steinernema spp. except S. carpocapsae were attracted to hosts that were not parasitized. Steinernema carpocapsae infective juveniles were repelled from hosts infected for 4 hr with all heterospecific infections except S. anomaliwhereas S. glaseri were repelled only from S. riobravis-infected hosts. Steinernema feltiae did not differentiate any heterospecific or heterogeneric infections. Steinernema glaseri were attracted to four of five heterospecific infections and S. anomali and S. riobravis were attracted to two of five heterospecific infections. Both S. anomali and S. glaseri were more attracted to hosts infected with the out-group Heterorhabditis bacteriophora than those infected by conspecific nematodes. Infective juvenile S. carpocapsaeS. anomaliand S. glaseri were more attracted to insects colonized by conspecific nematodes than to uninfested insects. Infective juvenile S. carpocapsae were repelled from the 24-hr-old conspecific infections, whereas S. glaseri were less attracted to 24- than to 4-hr-old conspecific infections. Experiments with insects injected with bacteria from the nematodes suggested the latter as the source of active volatiles. We suggest that odor-mediated host recognition by infective juveniles may reduce inter- and intraspecific competition among Steinernematidae.