The public world of insect vibrational communication

Food webs involving plants, herbivorous insects and their predators account for 75% of terrestrial biodiversity (Price 2002). Within the abundant arthropod community on plants, myriad ecological and social interactions depend on the perception and production of plant-borne mechanical vibrations (Hill 2008). Study of ecological relationships has shown, for example, that termites monitor the vibrations produced by competing colonies in the same tree trunk (Evans et al. 2009), that stink bugs and spiders attend to the incidental vibrations produced by insects feeding or walking on plants (Pfannenstiel et al. 1995, Barth 1998) and that caterpillars can distinguish among the foraging-related vibrations produced by their invertebrate predators (Castellanos & Barbosa 2006). Study of social interactions has revealed that many insects and spiders have evolved the ability to generate intricate patterns of substrate vibration, allowing them to communicate with potential mates or members of their social group (Cokl & Virant-Doberlet 2003; Hill 2008). Surprisingly, research on the role of substrate vibrations in social and ecological interactions has for the most part proceeded independently, in spite of evidence from other communication modalities – acoustic, visual, chemical and electrical – that predators attend to the signals of their prey (Zuk & Kolluru 1998; Stoddard 1999). The study by Virant-Doberlet et al. (2011) in this issue of Molecular Ecology now helps bring these two areas of vibration research together, showing that the foraging behaviour of a spider is influenced by the vibrational mating signals of its leafhopper prey.     

白蚁采食行为中的信息交流

白蚁作为社会性昆虫, 其采食个体间依赖各种信息交流机制进行联系与协作, 其中包括踪迹、 警戒、 食物信息、 同伴识别和助食等。通常的联系信号为挥发性或半挥发性化学物质或者一定频谱和功率的机械振动波。其中踪迹信息素、 蚁源烃类、 警戒信息素、 助食素和机械振动信号等都在白蚁采食过程中起着重要作用。白蚁采食过程中食物定向和食物品质信息的传达主要依靠腹板腺分泌的踪迹信息素, 已发现有十二碳烯醇类、 降碳倍半萜类和大环二萜类。蚁源的机械振动也在食物品质表达方面起到一定作用, 但食物品质的表达机制还不明确。白蚁采食协作的基础是同伴识别, 蚁源烃类（C21~C35）是同伴识别的主要信息物质, 采食个体分泌的助食素则可促成共同取食。警戒信息素传递白蚁采食的安全信息, 通常为一些兵蚁源的萜类物质, 但得到功能鉴定的结构还不多。近来研究还发现特殊的蚁源机械振动也可起到示警作用。已初步证实各种信息交流机制间存在交互作用, 但交互作用的机理有待进一步解析。生物物理因素在白蚁采食行为中的作用值得更多重视。本文以白蚁的采食行为为线索, 评述白蚁采食个体间信息交流机制的研究进展及利用问题, 并对今后的研究提出展望。     

Cryptic termites avoid predatory ants by eavesdropping on vibrational cues from their footsteps

Eavesdropping has evolved in many predator–prey relationships. Communication signals of social species may be particularly vulnerable to eavesdropping, such as pheromones produced by ants, which are predators of termites. Termites communicate mostly by way of substrate‐borne vibrations, which suggest they may be able to eavesdrop, using two possible mechanisms: ant chemicals or ant vibrations. We observed termites foraging within millimetres of ants in the field, suggesting the evolution of specialised detection behaviours. We found the termite Coptotermes acinaciformis detected their major predator, the ant Iridomyrmex purpureus, through thin wood using only vibrational cues from walking, and not chemical signals. Comparison of 16 termite and ant species found the ants‐walking signals were up to 100 times higher than those of termites. Eavesdropping on passive walking signals explains the predator detection and foraging behaviours in this ancient relationship, which may be applicable to many other predator–prey relationships.     

Predatory bug <Emphasis Type="Italic">Picromerus bidens</Emphasis> communicates at different frequency levels

The Asopinae (Heteroptera: Pentatomidae) are a subfamily of stinkbugs with predaceous feeding habits and poorly understood communication systems. In this study we recorded vibratory signals emitted by Picromerus bidens L. on a non-resonant substrate and investigated their frequency characteristics. Males and females produced signals by vibration of the abdomen and tremulation. The female and male songs produced by abdominal vibrations showed gender-specific time structure. There were no differences in the temporal patterns of male or female tremulatory signals. The signals produced by abdominal vibrations were emitted below 600 Hz whereas tremulatory signals had frequency ranges extending up to 4 kHz. Spectra of male vibratory signals produced by abdominal vibrations contained different peaks, each of which may be dominant within the same song sequence. Males alternated with each other during production of rivalry signals, using different dominant frequency levels. We show that the vibratory song repertoire of P. bidens is broader than those of other predatory stinkbugs that have been investigated. The emission of vibrational signals with different dominant frequencies but the same production mechanism has not yet been described in heteropteran insects, and may facilitate location of individual sources of vibration within a group.     

Does body size predict the buzz‐pollination frequencies used by bees?

Body size is an important trait linking pollinators and plants. Morphological matching between pollinators and plants is thought to reinforce pollinator fidelity, as the correct fit ensures that both parties benefit from the interaction. We investigated the influence of body size in a specialized pollination system (buzz‐pollination) where bees vibrate flowers to release pollen concealed within poricidal stamens. Specifically, we explored how body size influences the frequency of buzz‐pollination vibrations. Body size is expected to affect frequency as a result of the physical constraints it places on the indirect flight muscles that control the production of floral vibrations. Larger insects beat their wings less rapidly than smaller‐bodied insects when flying, but whether similar scaling relationships exist with floral vibrations has not been widely explored. This is important because the amount of pollen ejected is determined by the frequency of the vibration and the displacement of a bee's thorax. We conducted a field study in three ecogeographic regions (alpine, desert, grassland) and recorded flight and floral vibrations from freely foraging bees from 27 species across four families. We found that floral vibration frequencies were significantly higher than flight frequencies, but never exceeded 400 Hz. Also, only flight frequencies were negatively correlated with body size. As a bee's size increased, its buzz ratio (floral frequency/flight frequency) increased such that only the largest bees were capable of generating floral vibration frequencies that exceeded double that of their flight vibrations. These results indicate size affects the capacity of bees to raise floral vibration frequencies substantially above flight frequencies. This may put smaller bees at a competitive disadvantage because even at the maximum floral vibration frequency of 400 Hz, their inability to achieve comparable thoracic displacements as larger bees would result in generating vibrations with lower amplitudes, and thus less total pollen ejected for the same foraging effort.     

Vibratory stimuli in host location by parasitic wasps

Parasitic wasps use a broad spectrum of different stimuli for host location and host acceptance. Here we review the published evidence for the use of mechanical stimuli, i.e. substrate born vibrations which are invariably regarded as vibrotaxis. We propose a set of criteria to class behavioural reactions as vibrotaxis or vibrokinesis and characterize 14 studies reporting the use of host-associated vibrations by parasitoids. The studies are compared concerning (i) experimental design; (ii) characterisation of vibrational signals; and (iii) progress of the parasitoid towards the host.The recent experimental development based on new measurement techniques shows the growing body of evidence that host-associated vibrations are exploited by parasitic wasps. Nevertheless a definite proof for vibrotaxis is still lacking. To assess the exact mechanisms by which parasitoids use vibrations bioassays comparing reactions to natural and artificially generated signals are needed. Vibrotaxis as well as vibrokinesis are both helpful host location strategies for parasitoids foraging in a multimodal environment. At the community level they may lead to niche differentiation.     

Evaluation of predation risk in the collectively foraging termite Macrotermes bellicosus

Summary. Few studies have investigated foraging decisions in collectively foraging social insects with no studies in termites. In termites predation is assumed to be a key mortality factor. Therefore, we experimentally investigated the role of predation pressure in foraging decisions of the fungus cultivating, mound building termite Macrotermes bellicosus in two habitats of the Comoé National Park (Ivory Coast). We used the indirect approach of measuring the Giving up Density (GUD), which is the amount of food left when individuals stop foraging in a food patch, whilst experimentally varying predation pressure. Three different conditions were examined: (a) natural predation, (b) no predation, and (c) experimental predation through artificial removal of termites. In the shrub savanna, foraging termites responded to increasing predation with increasing GUDs. By contrast, in the gallery forest, there was no gradual response. Instead termites abandoned a food patch immediately after an attack by predators. Without predation GUDs were lower in the savanna than in the gallery forest indicating that food had a higher value in the former habitat. This, together with the differential behavioral responses to predation, was in accordance with high availability of food in the gallery forest and a limited supply of food in the savanna. Thus, according to our results termites traded off predation pressure differently, according to the availability of food in both habitats.     

Structure and sensory physiology of the leg scolopidial organs in Mantophasmatodea and their role in vibrational communication

Individuals of the insect order Mantophasmatodea use species-specific substrate vibration signals for mate recognition and location. In insects, substrate vibration is detected by mechanoreceptors in the legs, the scolopidial organs. In this study we give a first detailed overview of the structure, sensory sensitivity, and function of the leg scolopidial organs in two species of Mantophasmatodea and discuss their significance for vibrational communication. The structure and number of the organs are documented using light microscopy, SEM, and x-ray microtomography. Five scolopidial organs were found in each leg of male and female Mantophasmatodea: a femoral chordotonal organ, subgenual organ, tibial distal organ, tibio-tarsal scolopidial organ, and tarso-pretarsal scolopidial organ. The femoral chordotonal organ, consisting of two separate scoloparia, corresponds anatomically to the organ of a stonefly (Nemoura variegata) while the subgenual organ complex resembles the very sensitive organs of the cockroach Periplatena americana (Blattodea). Extracellular recordings from the leg nerve revealed that the leg scolopidial organs of Mantophasmatodea are very sensitive vibration receptors, especially for low-frequency vibrations. The dominant frequencies of the vibratory communication signals of Mantophasmatodea, acquired from an individual drumming on eight different substrates, fall in the frequency range where the scolopidial organs are most sensitive.     

Vibrational alarm communication in the damp-wood termite Zootermopsis nevadensis

Abstract. Vibrational alarm communication was studied in the New World, damp-wood termite Zootermopsis nevadensis (Isoptera: Termopsidae). Workers and soldiers react to disturbance such as sudden bright light or air currents by drumming their heads against the substratum. This drumming has been described as alarm signalling; its functional significance and perception by the nest mates, however, remained unclear. In the present study we analysed spectral and temporal properties and absolute amplitudes of the vibrational signals and used behavioural responses of the termites to determine the thresholds of the sense of vibration and to find out if and how the termites discriminate the conspecific alarm signals from the background noise.
The drumming signals are trains of pulses of vibrations of the substratum with a pulse repetition rate of about 20 Hz. The carrier frequency depends on the substratum; in the nests studied it was in the range 1–3 kHz. The highest vibrational amplitudes measured close to the signal emitters are usually about 10m/s² (acceleration, RMS). The threshold of the behavioural response is about 1m/s² over a wide range of frequencies (10 Hz to 5 kHz), indicating that the termites can detect these signals as vibrations of the substratum. The animals respond preferentially to temporal patterns similar those of the natural signals; temporal rather than spectral cues seem to be used for signal discrimination.     

Shaking Youngsters and Shaken Adults: Female Beetles Eavesdrop on Larval Seed Vibrations to Make Egg-Laying Decisions

Egg-laying decisions are critical for insects, and particularly those competing for limited resources. Sensory information used by females to mediate egg-laying decisions has been reported to be primarily chemical, but the role of vibration has received little attention. We tested the hypothesis that vibrational cues produced by feeding larvae occupying a seed influences egg-laying decisions amongst female cowpea beetles. This hypothesis is supported by three lines of evidence using two strains of the cowpea beetle (Callosobruchus maculatus), an Indian strain with choosy females and aggressively competing larvae and a Brazilian strain with less choosy females and larvae exhibiting an “accommodating” type of competition. First, in free-choice bioassays of seed selection, choosy Indian females selected control seeds (free of eggs, larvae, or egg-laying marker) over seeds with live larvae (free of eggs and egg-laying marker), but did not discriminate between control seeds and those with dead larvae. In contrast, less choosy Brazilian females showed no preference for seeds containing live or dead larvae over controls. Second, laser-doppler vibrometer recordings confirmed that larvae feeding inside seeds generate vibrations that are available to the female during egg-laying decisions. Third, during dichotomous choice experiments where artificial vibrations approximating those produced by feeding larvae were played back during seed selection, Indian females preferred immobile control seeds over vibrating seeds, but Brazilian females showed no preference. These results support the hypothesis that females use larval vibrations in their egg-laying decisions; whether these vibrations are passive cues exploited by the female, or active signals that ‘steer’ the behaviour of the female is unknown. We propose that vibration cues and signals could be important for host selection in insects, particularly those laying on substrates where visual or chemical cues may be unreliable. This seems to be the case with females of the cowpea beetle since visual cues are not important and chemical egg-marking does not last more than two weeks, allowing vibration cues to improve discrimination of egg-laying substrate particularly by choosy females.     

Thorax vibrations of a stingless bee (<Emphasis Type="Italic">Melipona seminigra</Emphasis>). I. No influence of visual flow

An important question in stingless bee communication is whether the thorax vibrations produced by foragers of the genus Melipona upon their return to the nest contain spatial information about food sources or not. As previously shown M. seminigra is able to use visual flow to estimate flight distances. The present study investigated whether foraging bees encode the visually measured distance in their thorax vibrations. Bees were trained to collect food in flight tunnels lined with a black-and-white pattern on their side walls and floor, which substantially influenced the image motion they experienced. When the bees had collected inside the tunnels the temporal pattern of their vibrations differed significantly from the pattern after collecting in a natural environment. These changes, however, were not associated with the visual flow experienced inside the tunnel. Bees collecting in tunnels offering little visual flow (stripes parallel to flight direction) modified their vibrations similarly to bees collecting in tunnels with high image motion (cross stripes). A higher energy expenditure due to drastically reduced flight velocities inside the tunnel is suggested to be responsible for changes in the thorax vibrations. The bees' vibrations would thus reflect the overall energetic budget of a foraging trip.     

Chimpanzee insectivory in the northern half of Uganda’s Rift Valley: do Bulindi chimpanzees conform to a regional pattern?

Insects are a nutritious food source for many primates. In chimpanzees, insectivory is most prevalent among communities that manufacture tools to harvest social insects, particularly ants and termites. In contrast to other long-term study sites, chimpanzees (Pan troglodytes schweinfurthii) in Budongo Forest and Kibale National Park, Uganda, rarely eat insects and have small foraging tool kits, supporting speculation that infrequent insectivory—technically aided or otherwise—characterises chimpanzees in this part of Uganda’s Rift Valley. To expand the dataset for this region, insect foraging was investigated at Bulindi (25 km from Budongo) over 19 months during two studies in 2007–2008 and 2012–2013. Systematic faecal analysis demonstrated that insectivory is a habitual foraging activity at this site. Overall levels of insect consumption varied considerably across months but were not predicted by monthly changes in rainfall or fruit intake. Unlike their Budongo and Kibale counterparts, Bulindi chimpanzees often consume ants (principally weaver ants, Oecophylla longinoda) and use sticks to dig out stingless bee (Meliponini) ground nests. In other respects, however, insectivory at Bulindi conforms to the pattern observed elsewhere in this region: they do not manufacture ‘fishing’ or ‘dipping’ tools to harvest termites and aggressive or hard-to-access ants (e.g., army ants, Dorylus spp.), despite availability of suitable prey. The Bulindi data lend support to the supposition that chimpanzees in this part of the Rift Valley rarely exploit termites and Dorylus ants, apparently lacking the ‘cultural knowledge’ that would enable them to do so most efficiently (i.e., tool use). The study’s findings contribute to current debates about the relative influence of genetics, environment and culture in shaping regional and local variability in Pan foraging ecology.     

Sucking pump activity in feeding behaviour regulation in carpenter ants

Modulation of liquid feeding-rate would allow insects to ingest more food in the same time when this was required. Ants can vary nectar intake rate by increasing sucking pump frequency according to colony requirements. We analysed electrical signals generated by sucking pump activity of ants during drinking solutions of different sucrose concentrations and under different carbohydrate-deprivation levels. Our aim was to define parameters that characterize the recordings and analyse their relationship with feeding behaviour.Signals showed that the initial and final frequencies of sucking pump activity, as well as the difference between them were higher in sugar-deprived ants. However, these parameters were not influenced by sucrose solution concentration, which affected the number of pump contractions and the volume per contraction. Unexpectedly, we found two different responses in feeding behaviour of starved and non-starved ants depending on concentration. Starved ants drank dilute solutions for the same length of time as non-starved ants but ingested higher volumes. While drinking the concentrated solutions, starved ants drank the same volume, but did so in a shorter time than the non-starved ones. Despite these differences, for each analysed concentration the total number of pump contractions remained constant independently of sugar-deprivation level. These results are discussed in the frame of feeding regulation and decision making in ant foraging behaviour.     

Subterranean termites (Isoptera: Rhinotermitidae): Exploitation of equivalent food resources with different forms of placement

Abstract Coptotermes gestroi and Heterotermes tenuis have been described as important urban pests in Brazil. The establishment of control technologies using baits that consider the social behavior of termites requires a better knowledge of their foraging behavior. Thus, this study analyzed the feeding behavior of these species with three different forms of food placement: food on the surface of a substrate and food either partially or completely buried in the substrate. Experimental arenas were composed of a central chamber connected to three food chambers. Each central chamber contained 550 foragers of C. gestroi or 517 foragers of H. tenuis. Blocks of Pinus elliottii were placed in the different food chambers. After 28 days, the consumption of each wood block and the percentage of foraging individuals recruited for food chambers were verified in relation to the total survival rate obtained for each one of the 20 replicates. Results showed that completely buried food was most consumed for H. tenuis and presented a higher recruitment rate of workers and soldiers for both species. Although the consumption had non‐significant differences for C. gestroi, these termites exhibited a tendency to prefer completely buried food. In these conditions, it can be concluded that the forms of food placement used in the present research influenced the recruitment of individuals for both species. Data also suggests that when the foraging subterranean termites find food resources in the tunneling substrate, they tend to concentrate their efforts on it, a behavior regime that reduces exposure to external environment.     

Tremulatory and Abdomen Vibration Signals Enable Communication through Air in the Stink Bug Euschistus heros

Communication by substrate-borne mechanical signals is widespread among animals but remains one of their least understood communication channels. Past studies of vibrational communication in insects have been oriented predominantly to communication during mating, showing that species- and sex-specific vibrational signals enable recognition and localization of potential mates on continuous solid substrates. No special attention has been paid to vibrational signals with less obvious specificity as well as to the possibility of vibrational communication across substrates that are not in physical contact. We aimed to reinvestigate emission of the aforementioned vibrational signals transmitted through a plant in the stink bug Euschistus heros (Pentatomidae: Pentatominae) and to check whether individuals are able to communicate across adjecent, physically separated substrates. We used laser vibrometry for registration of substrate-borne vibrational signals on a bean plant. Using two bean plants separated for 3 to 7 cm between two most adjacent leaves, we investigated the possibility of transmission of these signals through air. Our study showed that males and females of E. heros communicate using tremulatory, percussion and buzzing signals in addition to the previously described signals produced by vibrations of the abdomen. Contrary to the latter, the first three signal types did not differ between sexes or between pentatomid species. Experiments with two physically separated plants showed significant searching behaviour and localization of vibrational signals of an E. heros male or a female, in response to abdominal vibration produced signals of a pair duetting on the neighbouring plant, in comparison to control where no animals were on the neighbouring plant. We also confirmed that transmission through air causes amplitude and frequency decay of vibrational signals, which suggests high-amplitude, low-frequency tremulatory signals of these stink bugs their most plausible way of communication across discontinuous substrates.     

Protein marking reveals predation on termites by the woodland ant, <Emphasis Type="Italic">Aphaenogaster rudis</Emphasis>

Subterranean termites provide a major potential food source for forest-dwelling ants, yet the interactions between ants and termites are seldom investigated largely due to the cryptic nature of both the predator and the prey. We used protein marking (rabbit immunoglobin protein, IgG) and double antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) to examine the trophic interactions between the woodland ant, Aphaenogaster rudis (Emery) and the eastern subterranean termite, Reticulitermes flavipes (Kollar). We marked the prey by feeding the termites paper treated with a solution of rabbit immunoglobin protein (IgG). Subsequently, we offered live, IgG-fed termites to ant colonies and monitored the intracolony distribution of IgG-marked prey. Laboratory experiments on the distribution of protein-marked termite prey in colonies of A. rudis revealed that all castes and developmental stages receive termite prey within 24 h. In field experiments, live, protein-marked termites were offered to foraging ants. Following predation, the marker was recovered from the ants, demonstrating that A. rudis preys on R. flavipes under field conditions. Our results provide a unique picture of the trophic-level interactions between predatory ants and subterranean termites. Furthermore, we show that protein markers are highly suitable to track trophic interactions between predators and prey, especially when observing elusive animals with cryptic food-web ecology. Received 19 January 2007; revised 23 March 2007; accepted 26 March 2007.     

Distinguishing signals and cues: bumblebees use general footprints to generate adaptive behaviour at flowers and nest

Chemicals used in communication are divided into signals and cues. Signals are moulded by natural selection to carry specific meanings in specific contexts. Cues, on the other hand, have not been moulded by natural selection to carry specific information for intended receivers. Distinguishing between these two modes of information transfer is difficult when animals do not perform obvious secretion behaviours. Although a number of insects have been suspected of leaving cues at food sites and nest entrances, studies have not attempted to experimentally distinguish between cues and signals. Here, we examine the chemical composition of the scent marks left by the bumblebee Bombus terrestris at food sites and compare it to those found at a neutral location. If bees are depositing a cue, we expect the same chemicals to be found at both sites, but if they deposit a signal we only expect to find the scent marks at the food site. We were also interested in identifying the chemicals left at the nest entrance to determine if they differed from those used to mark food sites. We find that bees deposit the same chemicals at food, nest and neutral sites. Therefore, bumblebees leave behind general chemical footprints everywhere they walk and we propose that they learn to use these footprints in a manner that ultimately enhances their fitness, for example, to improve their foraging efficiency and locate their nest. Experimentally, distinguishing these two modes of information transfer is crucial for understanding how they interact to shape animal behaviour and what chemical bouquets are under natural selection. Handling Editor: Heikki Hokkanen     

Female Mate Choice Can Drive the Evolution of High Frequency Echolocation in Bats: A Case Study with Rhinolophus mehelyi

Animals employ an array of signals (i.e. visual, acoustic, olfactory) for communication. Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise. When the signal is used for more than one function, antagonisms amongst the different signalling functions may constrain the optimisation of the signal for any one function. Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve. Echolocating bats represent a fascinating group in which to study the evolution of signalling systems as unlike bird songs or frog calls, echolocation has a dual role in foraging and communication. The function of bat echolocation is to generate echoes that the calling bat uses for orientation and food detection with call characteristics being directly related to the exploitation of particular ecological niches. Therefore, it is commonly assumed that echolocation has been shaped by ecology via natural selection. Here we demonstrate for the first time using a novel combined behavioural, ecological and genetic approach that in a bat species, Rhinolophus mehelyi: (1) echolocation peak frequency is an honest signal of body size; (2) females preferentially select males with high frequency calls during the mating season; (3) high frequency males sire more off-spring, providing evidence that echolocation calls may play a role in female mate choice. Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.