How to perceive the insecticide? The Neotropical termite Nasutitermes corniger (Termitidae: Nasutitermitinae) triggers alert behavior after exposure to imidacloprid.

In eusocial insects, alarm signaling is used to inform nestmates about threats such as predators, competitors, and pathogens. Such behavior is important for the survival of colonies. However, studies evaluating the effect of insecticides on the alarm in termites have not yet been reported. Here, we inspected the effects of insecticide on alarm communication in Nasutitermes corniger. Specifically, we test the following hypotheses: (1) termite groups exposed to insecticide imidacloprid increase the body shaking movements, displaying an alert behavior; and (2) the alert behavior displayed after exposition to insecticide is dose dependent. Bioassays were conducted evaluating the body shaking movements and walking activity of termite groups exposed and non-exposed to insecticide. Thereafter, body shaking movements were evaluated in groups submitted to different doses of insecticide. In general, exposing termite groups to insecticide resulted in significantly higher body shaking movements compared to non-exposed groups. There was a positive effect of imidacloprid doses on the shaking movements. Walking activity, however, decreases in those groups exposed to the insecticide. Our results demonstrate the existence of 'insecticide alert behavior' in N. corniger and it appears to be a previously unrecognized communication mechanism in termites that allows for reducing the intoxication risks in the colony.

Social context modulates scale-free movements in a social insect.

Most animals move intermittently, pausing or slowing down for short moments and short moves, and darting away towards a new location where to hover again. This pattern occurs at a range of spatial and temporal scales (thence, resembling 'scale-free'), from the quick inspection of local areas to the sum of all movements performed from birth to death. While this pattern has been extensively described, its proximate drivers remain open to debate. A current hypothesis states that underlying proximate generative mechanisms of intermittent movement of animals are linked to external stimuli, e.g., interactions with the abiotic environment, resources, and other individuals. Here we investigated a prediction from this hypothesis, using termites as a biological model. We verified whether the social background in which a termite is inserted will modify the parameters of its intermittent scale-free spatial displacement. This relates to the hypothesis because it inspects how do external stimuli coming from intraspecifics can affect this type of movement. We tracked the trajectories of a focal termite confined along its nestmates in experimental clueless arenas, every 0.5 s along about six hours. Arenas varied in group size and comprised 22 distinct caste compositions, yielding 75 trackings (> 400 h) and more than two million Cartesian coordinates. Most of these trajectories (96% or 72/75) were classified as intermittent scale free (Lévy-like), indicating prevalence of this type of movement over non-Lévy-like ones (P=1.62×10-15). Moreover, intermittent scale-free movements performed by the focal termite (i) did arise outside the foraging-searching framework, and (ii) were modified by the social context while remaining within the limits of Lévy-walk realms. That is, some limits seem to exist along with the necessary plasticity to provide room for natural selection. Moreover, by arising outside the foraging framework, Lévy-like movements are shown to have broader relevance. Studies on processes that depend on social context and movement (e.g., collective behaviour, the spread of diseases) may, hence, profit from such concepts.

Scale-free movement patterns in termites emerge from social interactions and preferential attachments.

As the number or density of interacting individuals in a social group increases, a transition can develop from uncorrelated and disordered behavior of the individuals to a collective coherent pattern. We expand this observation by exploring the fine details of termite movement patterns to demonstrate that the value of the scaling exponent µ of a power law describing the Lévy walk of an individual is modified collectively as the density of animals in the group changes. This effect is absent when termites interact with inert obstacles. We also show that the network of encounters and interactions among specific individuals is selective, resembling a preferential attachment mechanism that is important for social networking. Our data strongly suggest that preferential attachments, a phenomenon not reported previously, and favorite interactions with a limited number of acquaintances are responsible for the generation of Lévy movement patterns in these social insects.

Nonaggressive behavior: A strategy employed by an obligate nest invader to avoid conflict with its host species.

In addition to its builders, termite nests are known to house a variety of secondary opportunistic termite species so-called inquilines, but little is known about the mechanisms governing the maintenance of these symbioses. In a single nest, host and inquiline colonies are likely to engage in conflict due to nestmate discrimination, and an intriguing question is how both species cope with each other in the long term. Evasive behaviour has been suggested as one of the mechanisms reducing the frequency of host-inquiline encounters, yet, the confinement imposed by the nests' physical boundaries suggests that cohabiting species would eventually come across each other. Under these circumstances, it is plausible that inquilines would be required to behave accordingly to secure their housing. Here, we show that once inevitably exposed to hosts individuals, inquilines exhibit nonthreatening behaviours, displaying hence a less threatening profile and preventing conflict escalation with their hosts. By exploring the behavioural dynamics of the encounter between both cohabitants, we find empirical evidence for a lack of aggressiveness by inquilines towards their hosts. Such a nonaggressive behaviour, somewhat uncommon among termites, is characterised by evasive manoeuvres that include reversing direction, bypassing and a defensive mechanism using defecation to repel the host. The behavioural adaptations we describe may play an important role in the stability of cohabitations between host and inquiline termite species: by preventing conflict escalation, inquilines may improve considerably their chances of establishing a stable cohabitation with their hosts.

Insecticidal activity of indole derivatives against Plutella xylostella and selectivity to four non-target organisms.

The diamondback moth Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae) is a destructive pest of brassica crops of economic importance that have resistance to a range of insecticides. Indole derivates can exert diverse biological activities, and different effects may be obtained from small differences in their molecular structures. Indole is the parent substance of a large number of synthetic and natural compounds, such as plant and animal hormones. In the present study, we evaluate the insecticidal activity of 20 new synthesized indole derivatives against P. xylostella, and the selectivity of these derivatives against non-target hymenopteran beneficial arthropods: the pollinator Apis mellifera (Linnaeus, 1758) (Hymenoptera: Apidae), and the predators Polybia scutellaris (White, 1841), Polybia sericea (Olivier, 1791) and Polybia rejecta (Fabricius, 1798) (Hymenoptera: Vespidae). Bioassays were performed in the laboratory to determine the lethal and sublethal effects of the compounds on P. xylostella and to examine their selectivity to non-target organisms by topical application and foliar contact. The treatments consisted of two synthesized derivatives (most and least toxic), the positive control (deltamethrin) and the negative control (solvent). The synthesized compound 4e [1-(1H-indol-3-yl)hexan-1-one] showed high toxicity (via topical application and ingestion) and decreased the leaf consumption by P. xylostella, displaying a higher efficiency than the pyrethroid deltamethrin, widely used to control this pest. In addition, the synthesized indole derivatives were selective to the pollinator A. mellifera and the predators P. scutellaris, P. sericea and P. rejecta, none of which were affected by deltamethrin. Our results highlight the promising potential of the synthesized indole derivatives for the generation of new chemical compounds for P. xylostella management.

Effect of temperature and substrate moisture on group survival of Constrictotermes sp. (Isoptera: Termitidae) under laboratory conditions

ABSTRACT Laboratory bioassays should be performed under appropriate conditions that minimize stress and promote greater longevity to tested animals. For social insects, for instance, the stress triggered by removal individuals from nests may result in changes in their survival and behavior. Here we analyzed the effects of variations of different combinations of temperature and substrate moisture (mL of water/g of nest substrate) on group survival of Constrictotermes sp. (Termitidae: Nasutitermitinae). In general, lower substrate moisture resulted in faster mortality. On the other hand, groups survival longer at a temperature of 26 ºC and under higher substrate moisture (2-3 mL/7 g of nest substrate). The result of this study may contribute to the establishment of bioassay protocols performed with Constrictotermes sp. in the laboratory.

Essential oils from Varronia curassavica (Cordiaceae) accessions and their compounds (E)-caryophyllene and α-humulene as an alternative to control Dorymyrmex thoracius (Formicidae: Dolichoderinae).

The process of urbanization of natural environments has dramatically increased the incidence of pest insects. To control these organisms in urban environments, the last decades have been marked by an increase in the use of synthetic insecticides. However, the intensive and indiscriminate use of synthetic insecticides has provoked a series of environmental problems and human health. In this way, the concern and the searching for environmentally safer alternatives for the control of urban pests is increasing. In the present study we evaluated the lethal and sublethal effects of essential oils (EOs) of six accessions of Varronia curassavica (Jacq.) (Cordiaceae) and their constituents (E)-caryophyllene and α-humulene on the ant Dorymyrmex thoracicus Gallardo, 1916 (Formicidae: Dolichoderinae), a species commonly found in urban environments and which can cause damage to human health. Bioassays of fumigation toxicity and locomotor activity in partially treated arenas were performed. The lethal concentrations to kill 50% of the D. thoracicus population ranged from 0.69 to 2.48 µL/L for EOs and from 3.75 to 1.49 µL/L for the (E)-caryophyllene and α-humulene compounds. The survival of the ants exposed to LC95 of the treatments was reduced over time, ranging from 4.2 to 35.6 h to kill 50% of the D. thoracicus population. In general, EOs of V. curassavica caused repellency and affected the locomotor activity of the ants. Our results indicate that EOs of V. curassavica are a promising source for the control of the urban ant D. thoracicus.

Apis mellifera (Insecta: Hymenoptera) in the target of neonicotinoids: A one-way ticket? Bioinsecticides can be an alternative.

The recent decline of Apis mellifera populations around the world has been subject of intense research due to ecological and economic damages resulting from the loss of pollination services. The intensive use of insecticides from the neonicotinoids group is among the possible causal factors of this decline, including also sub-lethal effects. However, the use of synthetic insecticides has been increased on a global scale in the recent decades. In order to evaluate an alternative to the use of neonicotinoids, this work investigated the effects of a bioinsecticide and its major compound on A. mellifera (Apidae: Hymenoptera), one of the main pollinators of crop plants. For this, bees were exposed, by contact and ingestion, to the essential oil of Cymbopogon martinii (Poaceae: Poales), to geraniol (major compound) and the insecticide imidacloprid to evaluate the toxicity and behavioral effects as well as the locomotion changes and immune responses of bees treated with these compounds. In general, toxicity was greater through ingestion and the insecticide imidacloprid was more toxic to A. mellifera compared to the essential oil and its major compound. The individual and collective behaviors (i.e. trophallaxis, grooming, avoidance) as well as the immune responses of bees were not significantly affected by bioinsecticides. However, the locomotion response and flight orientation of the bees were significantly altered by insecticide when administered by ingestion. Our results highlight the potential of C. martinii essential oil and its major compound as a possible alternative to mitigate the harmful effects of neonicotinoids on bees.

Alternative control of Aedes aegypti resistant to pyrethroids: lethal and sublethal effects of monoterpene bioinsecticides.

BACKGROUND: The mosquito Aedes aegypti is intensively controlled because it is a vector of viruses that cause numerous diseases, especially in tropical regions. As a consequence of the indiscriminate use of insecticides, populations from different regions have become resistant to pyrethroids. Here, we analyzed the lethal and sublethal effects of essential oil of Aristolochia trilobata and its major compounds on A. aegypti from susceptible and pyrethroid-resistant populations. RESULTS: Our results showed that the toxicity of the different compounds and behavioral changes in response to them are dependent on the stage of the insect life cycle. The monoterpene ρ-cymene caused high mortality in both larvae and adult females of A. aegypti, including those from the pyrethroid-resistant population. The monoterpenes limonene and linalool caused a sublethal effect in the larvae, triggering changes in the swimming pattern. CONCLUSION: This study highlights the potential of the essential oil of A. trilobata and its major compounds ρ-cymene and limonene for the control of A. aegypti and reveals the importance of analyzing sublethal effects on the population dynamics of the A. aegypti mosquito. © 2017 Society of Chemical Industry.

Nematode Root Herbivory in Tomato Increases Leaf Defenses and Reduces Leaf Miner Oviposition and Performance.

The outcome of plant-mediated interactions among herbivores from several feeding guilds has been studied intensively. However, our understanding on the effects of nematode root herbivory on leaf miner oviposition behavior and performance remain limited. In this study, we evaluated whether Meloidogyne incognita root herbivory affects Tuta absoluta oviposition preference on Solanum lycopersicum plants and the development of the resulting offspring. To investigate the M. incognita-herbivory induced plant systemic responses that might explain the observed biological effects, we measured photosynthetic rates, leaf trypsin protease inhibitor activities, and analyzed the profile of volatiles emitted by the leaves of root-infested and non-infested plants. We found that T. absoluta females avoided laying eggs on the leaves of root-infested plants, and that root infestation negatively affected the pupation process of T. absoluta. These effects were accompanied by a strong suppression of leaf volatile emissions, a decrease in photosynthetic rates, and an increase in the activity of leaf trypsin protease inhibitors. Our study reveals that root attack by nematodes can shape leaf physiology, and thereby increases plant resistance.

Combined foraging strategies and soldier behaviour in Nasutitermes aff. coxipoensis (Blattodea: Termitoidea: Termitidae).

A range of behavioural strategies and sensory abilities allows animals to minimize costs involved in food search. By building a network of tunnels and presenting a large number of soldiers (i.e., trophically dependent individuals), Nasutitermes spp. termites feature behaviours that imply additional costs during this process. Here we evaluated N. aff. coxipoensis foraging strategies focusing on the role of soldiers during foraging. Field experiments were carried out via nests transplantation to dune areas, and laboratory experiments evaluated termite responses to sternal gland chemical signals from workers and soldiers. N. aff. coxipoensis presented primarily nocturnal foraging. Soldiers typically initiated foraging; however, in established trails, the number of workers was always higher than that of soldiers. The number of trails remained constant over time, while the number of tunnels increased linearly over time. A higher proportion of tunnels originated in surrounding areas than directly from the nests. At observation points with tunnels, there were more stationary than walking soldiers; the opposite was true at observation points without tunnels. In mixed groups, the workers chose to follow soldier chemical signals, and in these groups, soldiers were the first to follow trails. Our results allowed us to identify a not common foraging strategy in termite species; which included the establishment of trails followed by construction of tunnels. Such foraging strategies occur predominantly at night and soldiers play a key role in the foraging process. This foraging strategy reported here seems to be employed to optimize energetic gain.

The nature of alarm communication in Constrictotermes cyphergaster (Blattodea: Termitoidea: Termitidae): the integration of chemical and vibroacoustic signals.

Alarm signalling is of paramount importance to communication in all social insects. In termites, vibroacoustic and chemical alarm signalling are bound to operate synergistically but have never been studied simultaneously in a single species. Here, we inspected the functional significance of both communication channels in Constrictotermes cyphergaster (Termitidae: Nasutitermitinae), confirming the hypothesis that these are not exclusive, but rather complementary processes. In natural situations, the alarm predominantly attracts soldiers, which actively search for the source of a disturbance. Laboratory testing revealed that the frontal gland of soldiers produces a rich mixture of terpenoid compounds including an alarm pheromone. Extensive testing led to identification of the alarm pheromone being composed of abundant monoterpene hydrocarbons (1S)-α-pinene and myrcene, along with a minor component, (E)-ß-ocimene. The vibratory alarm signalling consists of vibratory movements evidenced as bursts; a series of beats produced predominantly by soldiers. Exposing termite groups to various mixtures containing the alarm pheromone (crushed soldier heads, frontal gland extracts, mixture of all monoterpenes, and the alarm pheromone mixture made of standards) resulted in significantly higher activity in the tested groups and also increased intensity of the vibratory alarm communication, with the responses clearly dose-dependent. Lower doses of the pheromone provoked higher numbers of vibratory signals compared to higher doses. Higher doses induced long-term running of all termites without stops necessary to perform vibratory behaviour. Surprisingly, even crushed worker heads led to low (but significant) increases in the alarm responses, suggesting that other unknown compound in the worker's head is perceived and answered by termites. Our results demonstrate the existence of different alarm levels in termites, with lower levels being communicated through vibratory signals, and higher levels causing general alarm or retreat being communicated through the alarm pheromone.