Host-Seeking Behavior of Aphidius gifuensis (Hymenoptera: Braconidae) Modulated by Chemical Cues Within a Tritrophic Context.

Aphidius gifuensis Ashmaed is a generalist endoparasitoid that parasitizes a variety of aphid species. In China, it is widely used as a biological control agent to protect vegetables and tobaccos in open fields; control efficiency is largely dependent on its host-seeking ability. In this study, a six-choice olfactometer was used to investigate the olfactory responses of A. gifuensis to tobacco plants that had suffered damage (either varying degrees of mechanical damage or from aphid-feeding at different time intervals) and tobacco volatiles with different dosages. Furthermore, the regularity of A. gifuensis females' response toward an aphid/tobacco complex was monitored using a Y-tube olfactometer. Our findings suggest that tobacco plants are significantly attractive to A. gifuensis after they have been punctured with 50 holes, or housed with Myzus persicae (Sulzer) at a density of 400 aphids, except at an infestation time of 12 h. Moreover, aphid density had a more significant effect on the response than the time interval since aphid application. Aphidius gifuensis was found to be active during the daytime and preferred to search for their aphid hosts at 14:00 h. Five EAG-active tobacco volatiles (trans-2-hexenal, methyl salicylate, benzaldehyde, cis-3-hexen-1-ol, and 1-hexanal) were found to significantly attract A. gifuensis females at different concentration ranges. The practical implications of these results are discussed in the framework of the sustainable biological control of pest aphids in agricultural production systems.

Chemical host-seeking cues of entomopathogenic nematodes.

Entomopathogenic nematodes (EPNs) are obligate parasites that infect a broad range of insect species. Host-seeking is a crucial step for EPN infection success and survival. Yet, the identity and ecological functions of chemicals involved in host-seeking by EPNs remain overlooked. In this review, we report known CO2, plant-derived and insect-derived cues shaping EPN host-seeking and recognition. Despite species-specific response to environmental cues, we highlight a hierarchical integration of chemicals by EPNs. We further emphasize the impact of EPN selection pressure, age, and experience on their responsiveness to infochemicals. Finally, we feature that EPN chemical ecology can translate into powerful sustainable strategies to control insect herbivores in agriculture.

Why Lyme disease is common in the northern US, but rare in the south: The roles of host choice, host-seeking behavior, and tick density.

Lyme disease is common in the northeastern United States, but rare in the southeast, even though the tick vector is found in both regions. Infection prevalence of Lyme spirochetes in host-seeking ticks, an important component to the risk of Lyme disease, is also high in the northeast and northern midwest, but declines sharply in the south. As ticks must acquire Lyme spirochetes from infected vertebrate hosts, the role of wildlife species composition on Lyme disease risk has been a topic of lively academic discussion. We compared tick-vertebrate host interactions using standardized sampling methods among 8 sites scattered throughout the eastern US. Geographical trends in diversity of tick hosts are gradual and do not match the sharp decline in prevalence at southern sites, but tick-host associations show a clear shift from mammals in the north to reptiles in the south. Tick infection prevalence declines north to south largely because of high tick infestation of efficient spirochete reservoir hosts (rodents and shrews) in the north but not in the south. Minimal infestation of small mammals in the south results from strong selective attachment to lizards such as skinks (which are inefficient reservoirs for Lyme spirochetes) in the southern states. Selective host choice, along with latitudinal differences in tick host-seeking behavior and variations in tick densities, explains the geographic pattern of Lyme disease in the eastern US.

Host feeding patterns of Nyssorhynchus darlingi (Diptera: Culicidae) in the Brazilian Amazon.

Nyssorhynchus darlingi (Root) is the dominant malaria vector in the Brazilian Amazon River basin, with additional Anophelinae Grassi species involved in local and regional transmission. Mosquito blood-feeding behavior is an essential component to define the mosquito-human contact rate and shape the transmission cycle of vector-borne diseases. However, there is little information on the host preferences and blood-feeding behavior of Anophelinae vectors in rural Amazonian landscapes. The barrier screen sampling (BSS) method was employed to sample females from 34 peridomestic habitats in 27 rural communities from 11 municipalities in the Brazilian Amazon states of Acre, Amazonas, Pará and Rondônia, from August 2015 to November 2017. Nyssorhynchus darlingi comprised 97.94% of the females collected resting on barrier screens, and DNA sequence comparison detected 9 vertebrate hosts species. The HBI index ranged from 0.03-1.00. Results revealed the plasticity of Ny. darlingi in blood-feeding on a wide range of mainly mammalian hosts. In addition, the identification of blood meal sources using silica-dried females is appropriate for studies of human malaria vectors in remote locations.

Behavioral response of insecticide-resistant mosquitoes against spatial repellent: A modified self-propelled particle model simulation.

Rapidly increasing pyrethroid insecticide resistance and changes in vector biting and resting behavior pose serious challenges in malaria control. Mosquito repellents, especially spatial repellents, have received much attention from industry. We attempted to simulate interactions between mosquitoes and repellents using a machine learning method, the Self-Propelled Particle (SPP) model, which we modified to include attractiveness/repellency effects. We simulated a random walk scenario and scenarios with insecticide susceptible/resistant mosquitoes against repellent alone and against repellent plus attractant (to mimic a human host). Simulation results indicated that without attractant/repellent, mosquitoes would fly anywhere in the cage at random. With attractant, all mosquitoes were attracted to the source of the odor by the end. With repellent, all insecticide-susceptible mosquitoes eventually moved to the corner of the cage farthest from the repellent release point, whereas, a high proportion of highly resistant mosquitoes might reach the attractant release point (the human) earlier in the simulation. At fixed concentration, a high proportion of mosquitoes could be able to reach the host when the relative repellency efficacy (compare to attractant efficacy) was <1, whereas, no mosquitoes reached the host when the relative repellency efficacy was > 1. This result implies that repellent may not be sufficient against highly physiologically insecticide resistant mosquitoes, since very high concentrations of repellent are neither practically feasible nor cost-effective.

Mosquito heat seeking is driven by an ancestral cooling receptor.

Mosquitoes transmit pathogens that kill >700,000 people annually. These insects use body heat to locate and feed on warm-blooded hosts, but the molecular basis of such behavior is unknown. Here, we identify ionotropic receptor IR21a, a receptor conserved throughout insects, as a key mediator of heat seeking in the malaria vector Anopheles gambiae Although Ir21a mediates heat avoidance in Drosophila, we find it drives heat seeking and heat-stimulated blood feeding in Anopheles At a cellular level, Ir21a is essential for the detection of cooling, suggesting that during evolution mosquito heat seeking relied on cooling-mediated repulsion. Our data indicate that the evolution of blood feeding in Anopheles involves repurposing an ancestral thermoreceptor from non-blood-feeding Diptera.

The Road Not Taken: Host Infection Status Influences Parasite Host-Choice.

The manipulation of host organisms by their parasites has captured the attention of ecologists, parasitologists, and the public. However, our knowledge of parasite behavior independent of a host is limited despite the far-reaching implications of parasite behavior. Parasite behaviors can help explain trematode community structure, the aggregation of parasites within host populations, and can potentially be harnessed in biocontrol measures. In this study, we used a simple choice chamber design to examine whether trematode parasites can detect the infection status of a potential host and avoid hosts infected with a competitively dominant species. Our results show that Schistosoma mansoni, a competitively subordinate species, can detect and avoid hosts infected with a competitively dominant parasite, Echinostoma caproni. However, E. caproni, despite showing a significant preference for snails infected with S. mansoni over uninfected snails, showed little ability to detect the infection status of the host or even the host's presence. We propose subordinate species may be under stronger selection to avoid dominant competitors whereas dominant competitors may be more strongly selected to find any suitable host, regardless of infection status. Previous research has focused on parasites distinguishing between 'host' and 'non-host', which does not fully capture the complexity of these interactions. However, the ability of subordinate parasites to determine the infection status of a host results in a consistent evolutionary advantage.

Does membrane feeding compromise the quality of Aedes aegypti mosquitoes?

Modified Aedes aegypti mosquitoes are being mass-reared for release in disease control programs around the world. Releases involving female mosquitoes rely on them being able to seek and feed on human hosts. To facilitate the mass-production of mosquitoes for releases, females are often provided blood through artificial membrane feeders. When reared across generations there is a risk that mosquitoes will adapt to feeding on membranes and lose their ability to feed on human hosts. To test adaptation to membrane feeding, we selected replicate populations of Ae. aegypti for feeding on either human arms or membrane feeders for at least 8 generations. Membrane-selected populations suffered fitness costs, likely due to inbreeding depression arising from bottlenecks. Membrane-selected females had higher feeding rates on membranes than human-selected ones, suggesting adaptation to membrane feeding, but they maintained their attraction to host cues and feeding ability on humans despite a lack of selection for these traits. Host-seeking ability in small laboratory cages did not differ between populations selected on the two blood sources, but membrane-selected females were compromised in a semi-field enclosure where host-seeking was tested over a longer distance. Our findings suggest that Ae. aegypti may adapt to feeding on blood provided artificially, but this will not substantially compromise field performance or affect experimental assessments of mosquito fitness. However, large population sizes (thousands of individuals) during mass rearing with membrane feeders should be maintained to avoid bottlenecks which lead to inbreeding depression.

A field-based modeling study on ecological characterization of hourly host-seeking behavior and its associated climatic variables in Aedes albopictus.

BACKGROUND: The global spread of mosquito-borne diseases (MBD) has presented increasing challenges to public health. The transmission of MBD is mainly attributable to the biting behaviors of female mosquitoes. However, the ecological pattern of hourly host-seeking behavior in Aedes albopictus and its association with climatic variables are still not well understood, especially for a precise requirement for establishing an effective risk prediction system of MBD transmission. METHODS: Mosquito samples and data on mosquito hourly density and site-specific climatic variables, including temperature, relative humidity, illuminance and wind speed, were collected simultaneously in urban outdoor environments in Guangzhou during 2016-2018. Kernel regression models were used to assess the temporal patterns of hourly host-seeking behavior in mosquito populations, and negative binomial regression models in the Bayesian framework were used to investigate the associations of host-seeking behavior with climatic variables. RESULTS: Aedes albopictus was abundant, constituting 82% (5569/6790) of the total collected mosquitoes. Host-seeking behavior in Ae. albopictus varied across time and was significantly influenced by climatic variables. The predicted hourly mosquito densities showed non-linear relationships with temperature and illuminance, whereas density increased with relative humidity but generally decreased with wind speed. The range of temperature estimates for female biting was 16.4-37.1 °C, peaking at 26.5 °C (95% credible interval: 25.3-28.1). During the favorable periods, biting behavior of female Ae. albopictus was estimated to occur frequently all day long, presenting a bimodal distribution with peaks within 2-3 h around both dawn and dusk (05:00-08:00 h and 16:00-19:00 h). Moreover, a short-term association in hourly density between the females and males was found. CONCLUSIONS: Our field-based modeling study reveals that hourly host-seeking behavior of Ae. albopictus exhibits a complex pattern, with hourly variation constrained significantly by climatic variables. These findings lay a foundation for improving MBD risk assessments as well as practical strategies for vector control. For instances of all-day-long frequent female biting during the favorable periods in Guangzhou, effective integrated mosquito control measures must be taken throughout the day and night.

The nature of the arena surface affects the outcome of host-finding behavior bioassays in Varroa destructor (Anderson & Trueman).

Varroa destructor, an acarian parasite of the Western honey bee Apis mellifera L., is a serious threat to colonies and beekeeping worldwide. The parasite lifecycle occurs in close synchrony with its host development. The females have to discriminate between different developmental stages of the host and trigger an appropriate behavioral response. Many studies have focused on these behavioral aspects, whether it is the choice of a precise host stage or the reproduction of female mites. Behavioral tests often require laboratory settings that are very different from the mite's environment. Our first experiment was designed to study the impact of the surface of test arena on the mite behavior. We found that plastic from Petri dishes commonly used as test arenas disturbs the female mites and can cause death. We searched for a substrate that does not harm mites and found that gelatin-coated plastic Petri dishes responded to these expectations. We then investigated the host choice behavior of phoretic mites confronted with larval stages of the bee on gelatin-coated arenas to watch if the well-documented orientation towards 5th instar larva was observable in our conditions. Pupal stages were included in the host choice experiments, initially to act as neutral stimuli. As white-eyed pupae were revealed attractive to the mite, several pupal stages were then included in a series of host choice bioassays. These additional experiments tend to show that the positive response to the white-eyed pupa stage depends on cues only delivered by living pupae. Further investigation on the nature and impact of these cues are needed as they could shed light on key signals involved in the parasite lifecycle.

Study on host-seeking behavior and chemotaxis of entomopathogenic nematodes using Pluronic F-127 gel.

Pluronic F-127 gel (PF127) has proven to be a powerful medium in which to study host-finding behavior and chemotaxis for plant-parasitic nematodes. Pluronic gel can also be used to study host-habitat seeking behavior of entomopathogenic nematodes (EPN), which are natural enemies of root-feeding insect pests. In this study, PF127 was used to study tritrophic interactions among EPNs, host-habitat roots and insects. We also tested whether EPN aggregated to acetic acid (pH gradient) which mimicked the conditions near the roots. The chive root gnat Bradysia odoriphaga alone significantly attracted more nematodes than chive roots alone or the combination of roots plus insects. The attractiveness of B. odoriphaga differed (3.7-15.4%) among all tested species/strains of EPNs. In addition, we found that Heterorhabditis spp. and Steinernema spp. infective juveniles responded to pH gradients formed by acetic acid in Pluronic gel. The preferred pH ranges for strains of H. bacteriophora and H. megidis were from 4.32-5.04, and from 5.37-6.92 for Steinernema species, indicating that Heterorhabditis spp. prefer low pH conditions than Steinernema species. A narrow pH gradient between 6.84 and 7.05 was detected around chive root tips in which EPN was attracted. These results suggest that Pluronic gel can be broadly used for the study of host or host-habitat seeking behaviors and chemotaxis of nematodes.

A Critical Role for Thermosensation in Host Seeking by Skin-Penetrating Nematodes.

Skin-penetrating parasitic nematodes infect approximately one billion people worldwide and are a major source of neglected tropical disease [1-6]. Their life cycle includes an infective third-larval (iL3) stage that searches for hosts to infect in a poorly understood process that involves both thermal and olfactory cues. Here, we investigate the temperature-driven behaviors of skin-penetrating iL3s, including the human-parasitic threadworm Strongyloides stercoralis and the human-parasitic hookworm Ancylostoma ceylanicum. We show that human-parasitic iL3s respond robustly to thermal gradients. Like the free-living nematode Caenorhabditis elegans, human-parasitic iL3s show both positive and negative thermotaxis, and the switch between them is regulated by recent cultivation temperature [7]. When engaging in positive thermotaxis, iL3s migrate toward temperatures approximating mammalian body temperature. Exposing iL3s to a new cultivation temperature alters the thermal switch point between positive and negative thermotaxis within hours, similar to the timescale of thermal plasticity in C. elegans [7]. Thermal plasticity in iL3s may enable them to optimize host finding on a diurnal temperature cycle. We show that temperature-driven responses can be dominant in multisensory contexts such that, when thermal drive is strong, iL3s preferentially engage in temperature-driven behaviors despite the presence of an attractive host odorant. Finally, targeted mutagenesis of the S. stercoralis tax-4 homolog abolishes heat seeking, providing the first evidence that parasitic host-seeking behaviors are generated through an adaptation of sensory cascades that drive environmental navigation in C. elegans [7-10]. Together, our results provide insight into the behavioral strategies and molecular mechanisms that allow skin-penetrating nematodes to target humans.

Modeling host-seeking behavior of African malaria vector mosquitoes in the presence of long-lasting insecticidal nets.

The efficiency of spatial repellents and long-lasting insecticide-treated nets (LLINs) is a key research topic in malaria control. Insecticidal nets reduce the mosquito-human contact rate and simultaneously decrease mosquito populations. However, LLINs demonstrate dissimilar efficiency against different species of malaria mosquitoes. Various factors have been proposed as an explanation, including differences in insecticide-induced mortality, flight characteristics, or persistence of attack. Here we present a discrete agent-based approach that enables the efficiency of LLINs, baited traps and Insecticide Residual Sprays (IRS) to be examined. The model is calibrated with hut-level experimental data to compare the efficiency of protection against two mosquito species: Anopheles gambiae and Anopheles arabiensis. We show that while such data does not allow an unambiguous identification of the details of how LLINs alter the vector behavior, the model calibrations quantify the overall impact of LLINs for the two different mosquito species. The simulations are generalized to community-scale scenarios that systematically demonstrate the lower efficiency of the LLINs in control of An. arabiensis compared to An. gambiae.

Effects of malaria infection on mosquito olfaction and behavior: extrapolating data to the field.

Vector-borne pathogens have been shown to influence behavioral and other traits of their hosts and vectors across multiple systems, frequently in ways that enhance transmission. In malaria pathosystems, Plasmodium parasites have been reported to alter mosquito physiology, fitness and host-seeking behavior. Such effects on vector behavior have obvious medical relevance given their potential to influence disease transmission. However, most studies detailing these effects have faced methodological limitations, including experiments limited to laboratory settings with model vector/pathogen systems. Some recent studies indicate that similar effects may not be observed with natural field populations; furthermore, it has been suggested that previously reported effects on vectors might be explained by immune responses elicited due to the use of pathogen-vector systems that are not co-evolved. In light of these developments, further work is needed to determine the validity of extrapolation from laboratory studies to field conditions and to understand how parasite effects on vectors affect transmission dynamics in real-world settings.

Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes.

BACKGROUND: Entomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors. Although EPNs have been successfully commercialized for pest control, their efficacy in the field is often inconsistent for reasons that remain elusive. EPN infective juveniles (IJs) actively search for hosts to infect using a diverse array of host-emitted odorants. Here we investigate whether their host-seeking behavior is subject to context-dependent modulation. RESULTS: We find that EPN IJs exhibit extreme plasticity of olfactory behavior as a function of cultivation temperature. Many odorants that are attractive for IJs grown at lower temperatures are repulsive for IJs grown at higher temperatures and vice versa. Temperature-induced changes in olfactory preferences occur gradually over the course of days to weeks and are reversible. Similar changes in olfactory behavior occur in some EPNs as a function of IJ age. EPNs also show temperature-dependent changes in their host-seeking strategy: IJs cultured at lower temperatures appear to more actively cruise for hosts than IJs cultured at higher temperatures. Furthermore, we find that the skin-penetrating rat parasite Strongyloides ratti also shows temperature-dependent changes in olfactory behavior, demonstrating that such changes occur in mammalian-parasitic nematodes. CONCLUSIONS: IJs are developmentally arrested and long-lived, often surviving in the environment through multiple seasonal temperature changes. Temperature-dependent modulation of behavior may enable IJs to optimize host seeking in response to changing environmental conditions, and may play a previously unrecognized role in shaping the interactions of both beneficial and harmful parasitic nematodes with their hosts.

Exogenous RNA interference exposes contrasting roles for sugar exudation in host-finding by plant pathogens.

Plant parasitic nematodes (PPN) locate host plants by following concentration gradients of root exudate chemicals in the soil. We present a simple method for RNA interference (RNAi)-induced knockdown of genes in tomato seedling roots, facilitating the study of root exudate composition, and PPN responses. Knockdown of sugar transporter genes, STP1 and STP2, in tomato seedlings triggered corresponding reductions of glucose and fructose, but not xylose, in collected root exudate. This corresponded directly with reduced infectivity and stylet thrusting of the promiscuous PPN Meloidogyne incognita, however we observed no impact on the infectivity or stylet thrusting of the selective Solanaceae PPN Globodera pallida. This approach can underpin future efforts to understand the early stages of plant-pathogen interactions in tomato and potentially other crop plants.

Cues Triggering Mating and Host-Seeking Behavior in the Aphid Parasitoid Aphidius colemani (Hymenoptera: Braconidae: Aphidiinae): Implications for Biological Control.

Aphidius colemani Viereck (Hymenoptera: Braconidae: Aphidiinae) is a pan-tropical, broadly oligophagous, solitary endoparasitoid of many aphids of economic importance. Here, we review current knowledge about this important biological control agent, with a special focus on the physical and chemical cues triggering mating and host-seeking behavior. First, we focus on female-borne olfactory cues evoking courtship in A. colemani males, as well as on the relationship between male mating performance and quality of the host species. Second, we examine how A. colemani females forage for hosts and assess their suitability, using both aphid-borne kairomones and host-related physical cues. Third, we review A. colemani-based biological control approaches, outlining how knowledge of its reproductive behavioral ecology may enhance biological control of aphid pests. Concepts for future biocontrol programs are outlined, including 1) use of sex attractant dispensers for monitoring, 2) mass-rearing optimization based on knowledge of mate-finding strategies and sexually selected traits, 3) deployment of aphid-borne foraging kairomones as field lures to attract parasitoids into infested agro-ecosystems, 4) use of sensitization or associative learning practices to optimize efficacy of mass-reared wasps.