Social Plasticity Enhances Signal-Preference Codivergence.

AbstractThe social environment is often the most dynamic and fitness-relevant environment animals experience. Here we tested whether plasticity arising from variation in social environments can promote signal-preference divergence-a key prediction of recent speciation theory but one that has proven difficult to test in natural systems. Interactions in mixed social aggregations could reduce, create, or enhance signal-preference differences. In the latter case, social plasticity could establish or increase assortative mating. We tested this by rearing two recently diverged species of Enchenopa treehoppers-sap-feeding insects that communicate with plant-borne vibrational signals-in treatments consisting of mixed-species versus own-species aggregations. Social experience with heterospecifics (in the mixed-species treatment) resulted in enhanced signal-preference species differences. For one of the two species, we tested but found no differences in the plastic response between sympatric and allopatric sites, suggesting the absence of reinforcement in the signals and preferences and their plastic response. Our results support the hypothesis that social plasticity can create or enhance signal-preference differences and that this might occur in the absence of long-term selection against hybridization on plastic responses themselves. Such social plasticity may facilitate rapid bursts of diversification.

Noise matters: elephants show risk-avoidance behaviour in response to human-generated seismic cues.

African elephants (Loxodonta africana) use many sensory modes to gather information about their environment, including the detection of seismic, or ground-based, vibrations. Seismic information is known to include elephant-generated signals, but also potentially encompasses biotic cues that are commonly referred to as 'noise'. To investigate seismic information transfer in elephants beyond communication, here we tested the hypothesis that wild elephants detect and discriminate between seismic vibrations that differ in their noise types, whether elephant- or human-generated. We played three types of seismic vibrations to elephants: seismic recordings of elephants (elephant-generated), white noise (human-generated) and a combined track (elephant- and human-generated). We found evidence of both detection of seismic noise and discrimination between the two treatments containing human-generated noise. In particular, we found evidence of retreat behaviour, where seismic tracks with human-generated noise caused elephants to move further away from the trial location. We conclude that seismic noise are cues that contain biologically relevant information for elephants that they can associate with risk. This expands our understanding of how elephants use seismic information, with implications for elephant sensory ecology and conservation management.

Vibrational signalling, an underappreciated mode in cricket communication.

Signalling via substrate vibration represents one of the most ubiquitous and ancient modes of insect communication. In crickets (Grylloidea) and other taxa of tympanate Ensifera, production and detection of acoustic and vibrational signals are closely linked functionally and evolutionarily. Male stridulation produces both acoustic and vibrational signal components, the joint perception of which improves song recognition and female orientation towards the signaller. In addition to stridulation, vibrational signalling mainly through body tremulation and/or drumming with body parts on the substrate has long been known to be part of crickets' close-range communication, including courtship, mate guarding and aggression. Such signalling is typically exhibited by males, independently or in conjunction with stridulation, and occurs literally in all cricket lineages and species studied. It is further also part of the aggressive behaviour of females, and in a few cricket groups, females respond vibrationally to acoustic and/or vibrational signals from males. The characteristics and function of these signals have remained largely unexplored despite their prevalence. Moreover, the communication potential and also ubiquity of cricket vibrational signals are underappreciated, limiting our understanding of the function and evolution of the cricket signalling systems. By providing a concise review of the existing knowledge of cricket perception of vibrations and vibrational signalling behaviour, we critically comment on these views, discuss the communication value of the emitted signals and give some methodological advice respecting their registration and control. The review aims to increase awareness, understanding and research interest in this ancient and widespread signalling mode in cricket communication.

The relationship between a combinatorial processing rule and a continuous mate preference function in an insect.

Mate choice involves processing signals that can reach high levels of complexity and feature multiple components, even in small animals with tiny brains. This raises the question of whether and how such organisms deal with this complexity. One solution involves combinatorial processing, whereby different signal elements are processed as single units. Combinatorial processing has been described in several mammals and birds, and recently in a vibrationally signalling insect, Enchenopa treehoppers. Here, we ask about the relationship between combinatorial rules and mate preferences for continuously varying signal features. Enchenopa male advertisement signals are composed of two elements: a 'whine' followed by a set of pulses. The dominant frequency of the whine and element combination both matter to females. We presented synthetic signals varying in element order (natural [whine-pulses], reverse [pulses-whine]) and in frequency to Enchenopa females and recorded their responses. The reverse combination resulted in a decrease in attractiveness of the signals, and also slightly changed the shape of the preference for frequency. We found that females could be classified into three 'types': females with both a strong preference and a strong combinatorial rule, females with both a weak preference and weak rule, and females with a strong preference but a weak rule. Our results suggest that in Enchenopa signal processing, the mate preference for a continuous signal feature 'takes precedence' over, but also interacts with, the combinatorial rule. The relationship between the preference and the rule could evolve to take different forms according to selection on mate choice decisions. We suggest that exploring the relationship between such preferences and rules in species with more complex signals will bring insight into the evolution of the multi-component communication systems.

Biotremology in arthropods.

Effective communication is essential in animal life to allow fundamental behavioral processes and survival. Communicating by surface-borne vibrations is likely the most ancient mode of getting and exchanging information in both invertebrates and vertebrates. In this review, we concentrate on the use of vibrational communication in arthropods as a form of intraspecific and interspecific signaling, with a focus on the newest discoveries from our research group in terrestrial isopods (Crustacea: Isopoda: Oniscidea), a taxon never investigated before in this context. After getting little attention in the past, biotremology is now an emerging field of study in animal communication, and it is receiving increased interest from the scientific community dealing with these behavioral processes. In what follows, we illustrate the general principles and mechanisms on which biotremology is based, using definitions, examples, and insights from the literature in arthropods. Vibrational communication in arthropods has mainly been studied in insects and arachnids. For these taxa, much evidence of its use as a source of information from the surrounding environment exists, as well as its involvement in many behavioral roles, such as courtship and mating, conspecific recognition, competition, foraging, parental care, and danger perception. Recently, and for the first time, communication through surface-borne waves has been studied in terrestrial isopods, using a common Mediterranean species of the Armadillidae family as a pilot species, Armadillo officinalis Duméril, 1816. Mainly, for this species, we describe typical behavioral processes, such as turn alternation, aggregation, and stridulation, where vibrational communication appears to be involved.

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae).

Variation in temperature can affect the expression of a variety of important fitness-related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences-as well as the relationship between how male signals and female mate preferences change across temperatures (signal-preference temperature coupling)-in Enchenopa binotata treehoppers. These small plant-feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal-preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals-the trait for which females show strongest preference-and female peak preference-the signal frequency most preferred by females-across a range of biologically relevant temperatures (18°C-36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal-preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal-preference matches, and directional selection in those with signal-preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal-preference mismatches at thermal extremes.

Transmission of the frequency components of the vibrational signal of the glassy-winged sharpshooter, Homalodisca vitripennis, within and between grapevines.

The agricultural pest, Homalodisca vitripennis, relies on vibrational communication through plants for species identification, location, and courtship. Their vibrational signal exhibits a dominant frequency between 80 and 120 Hz, with higher frequency, lower intensity harmonics occurring approximately every 100 Hz. However, previous research revealed that not all harmonics are recorded in every signal. Therefore, how the female H. vitripennis vibrational signal changes as it travels through the plant was investigated. Results confirmed that transmission was a bending wave, with decreased signal intensity for increasing distance from the source; moreover, at distances of 50 cm, higher frequencies traveled faster than lower frequencies, suggesting that dispersion of H. vitripennis signal components may enable signaling partners to encode distance. Finally, H. vitripennis generates no detectable airborne signal (pressure wave), yet their low vibrational frequency components are detectable in neighboring plants as a result of leaf-to-air-to-leaf propagation. For instance, with isolated key female signal frequencies, 100 Hz was detected at a 10 cm gap between leaves, whereas 600 Hz was detectable only with a 0.1 cm gap. Together, these results highlight the complexity of vibration propagation in plants and suggest the possibility of the animals using the harmonic content to determine distance to the signaling H. vitripennis source.

Are terrestrial isopods able to use stridulation and vibrational communication as forms of intra and interspecific signaling and defense strategies as insects do? A preliminary study in Armadillo officinalis.

The capability of producing sounds and vibrations is well known in insects and is thought to be a form of intra- and interspecific communication. Sounds and vibrations are used and modulated for several aims such as interacting with conspecifics, getting information from the environment, and defending against predators. This phenomenon is less known but also present in other arthropods, including a few roller-type terrestrial isopods. In this study, we used a Y-shape test apparatus to investigate the behavior of adult individuals of Armadillo officinalis Duméril, 1816 (Crustacea: Isopoda: Oniscidea) when exposed to two particular vibrational stimuli, namely species-specific stridulations and non-specific substrate-borne vibrations. Our results showed that adults of A. officinalis significantly react to the presence of both types of vibrational stimuli, by moving away from the vibrational source as if they experienced these vibrations as a sign of danger or disturbance. A. officinalis can produce stridulations only when it rolls into a ball during the so-called conglobation, a possible defense mechanism against predators. Stridulation might thus be a secondary form of defense used during conglobation to deter a predator following contact with it and might be experienced as an alert by conspecifics nearby. The high sensitivity to non-specific substrate-borne vibrations might provide A. officinalis with the possibility to anticipate dangers and adverse conditions, giving it a better chance of survival.

Gastral drumming: a nest-based food-recruitment signal in a social wasp.

Many social insect species produce signals that either recruit foragers to a specific food source or simply activate more nestmates to become foragers. Both are means of enhancing resource exploitation by increasing the number of individuals devoted to gathering profitable resources. Gastral drumming (GD) has been documented in several species of yellowjackets and hornets (Vespidae: Vespinae). It has been hypothesized that it is a hunger signal, but there is little empirical evidence to support this claim. An alternative hypothesis is that GD recruits workers to forage for food. Here, we report the results of a test between the hunger-signal and food-recruitment hypotheses in the German yellowjacket wasp, Vespula germanica. We show that the rate of performance of GD decreased when colonies were deprived of food and increased when supplemental food was provided. Playback of GD caused increased rates of (1) movement in the nest, (2) trophallaxis, and (3) worker departures from the nest. Together, these results support the conclusion that GD is not a hunger signal as previously asserted but instead is a nest-based food-recruitment signal, the first to be reported for a social wasp.

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.

Local population density and group composition influence the signal-preference relationship in Enchenopa treehoppers (Hemiptera: Membracidae).

Many animals exhibit social plasticity - changes in phenotype or behaviour in response to experience with conspecifics that change how evolutionary processes like sexual selection play out. Here, we asked whether social plasticity arising from variation in local population density in male advertisement signals and female mate preferences influences the form of sexual selection. We manipulated local density and determined whether this changed how the distribution of male signals overlapped with female preferences - the signal preference relationship. We specifically look at the shape of female mate preference functions, which, when compared to signal distributions, provide hypotheses about the form of sexual selection. We used Enchenopa binotata treehoppers, a group of plant-feeding insects that exhibit natural variation in local densities across individual host plants, populations, species and years. We measured male signal frequency and female preference functions across the density treatments. We found that male signals varied across local social groups, but not according to local density. By contrast, female preferences varied with local density - favouring higher signal frequencies in denser environments. Thus, local density changes the signal-preference relationship and, consequently, the expected form of sexual selection. We found no influence of sex ratio on the signal-preference relationship. Our findings suggest that plasticity arising from variation in local group density and composition can alter the form of sexual selection with potentially important consequences both for the maintenance of variation and for speciation.

Chordotonal organs in hemipteran insects: unique peripheral structures but conserved central organization revealed by comparative neuroanatomy.

Hemipteran insects use sophisticated vibrational communications by striking body appendages on the substrate or by oscillating the abdominal tymbal. There has been, however, little investigation of sensory channels for processing vibrational signals. Using sensory nerve stainings and low invasive confocal analyses, we demonstrate the comprehensive neuronal mapping of putative vibration-responsive chordotonal organs (COs) in stink bugs (Pentatomidae and Cydinidae) and cicadas (Cicadidae). The femoral CO (FCO) in stink bugs consists of ventral and dorsal scoloparia, homologous to distal and proximal scoloparia in locusts, which are implicated in joint movement detection and vibration detection, respectively. The ligament of the dorsal scoloparium is distally attached to the accessory extensor muscle, whereas that of the ventral scoloparium is attached to a specialized tendon. Their afferents project to the dorso-lateral neuropil and the central region of the medial ventral association center (mVAC) in the ipsilateral neuromere, where presumed dorsal scoloparium afferents and subgenual organ afferents are largely intermingled. In contrast, FCOs in cicadas have decreased dorsal scoloparium neurons and lack projections to the mVAC. The tymbal CO of stink bugs contains four sensory neurons that are distally attached to fat body cells via a ligament. Their axons project intersegmentally to the dorsal region of mVACs in all neuromeres. Together with comparisons of COs in different insect groups, the results suggest that hemipteran COs have undergone structural modification for achieving faster signaling of resonating peripheral tissues. The conserved projection patterns of COs suggest functional importance of the FCO and subgenual organ for vibrational communications.

Males adjust their signalling behaviour according to experience of male signals and male-female signal duets.

Sexual signals are conspicuous sources of information about neighbouring competitors, and species in which males and females signal during pair formation provide various sources of public information to which individuals can adjust their behaviour. We performed two experiments with a duetting vibrational insect, Enchenopa binotata treehoppers (Hemiptera: Membracidae), to ask whether males adjust their signalling behaviour according to (1a) their own experience of competitors' signals, (1b) how females adjust their mate preferences on the basis of their experience of male signals (described in prior work), and/or (2) their own experience of female response signals to competitors' signals. We presented males with synthetic male signals of different frequencies and combinations thereof for 2 weeks. We recorded males a day after their last signal exposure, finding that (1a) male signal rate increased in response to experience of attractive competitors, but that (1b) male signal frequency did not shift in a manner consistent with how females adjust their mate preferences in those experience treatments. Second, we presented males with different male-female duets for 2 weeks, finding that (2) male signal length increased from experience of female duets with attractive competitors. Males thus make two types of adjustment according to two sources of public information: one provided by experience of male signals and another by experience of female responses to male signals. Signalling plasticity can generate feedback loops between the adjustments that males and females make, and we discuss the potential consequences of such feedback loops for the evolution of communication systems.

Founder effects initiated rapid species radiation in Hawaiian cave planthoppers.

The Hawaiian Islands provide the venue of one of nature's grand experiments in evolution. Here, we present morphological, behavioral, genetic, and geologic data from a young subterranean insect lineage in lava tube caves on Hawai'i Island. The Oliarus polyphemus species complex has the potential to become a model for studying rapid speciation by stochastic events. All species in this lineage live in extremely similar environments but show strong differentiation in behavioral and morphometric characters, which are random with respect to cave age and geographic distribution. Our observation that phenotypic variability within populations decreases with increasing cave age challenges traditional views on founder effects. Furthermore, these cave populations are natural replicates that can be used to test the contradictory hypotheses. Moreover, Hawaiian cave planthoppers exhibit one of the highest speciation rates among animals and, thus, radically shift our perception on the evolutionary potential of obligate cavernicoles.

Bridging biotremology and chemical ecology: a new terminology.

Living organisms use both chemical and mechanical stimuli to survive in their environment. Substrate-borne vibrations play a significant role in mediating behaviors in animals and inducing physiological responses in plants, leading to the emergence of the discipline of biotremology. Biotremology is experiencing rapid growth both in fundamental research and in applications like pest control, drawing attention from diverse audiences. As parallels with concepts and approaches in chemical ecology emerge, there is a pressing need for a shared standardized vocabulary in the area of overlap for mutual understanding. In this article, we propose an updated set of terms in biotremology rooted in chemical ecology, using the suffix '-done' derived from the classic Greek word 'δονέω' (pronounced 'doneo'), meaning 'to shake'.

Wing buzzing as a mechanism for generating vibrational signals in psyllids (Hemiptera: Psylloidea).

Psyllids, or jumping plant lice (Hemiptera: Sternorrhyncha: Psylloidea), are a group of small phytophagous insects that include some important pests of crops worldwide. Sexual communication of psyllids occurs via vibrations transmitted through host plants, which play an important role in mate recognition and localization. The signals are species-specific and can be used to aid in psyllid taxonomy and pest control. Several hypotheses have been proposed for the mechanism that generates these vibrations, of which stridulation, that is, friction between parts of the forewing and thorax, has received the most attention. We have investigated vibrational communication in the European pear psyllid species Cacopsylla pyrisuga (Foerster, 1848) using laser vibrometry and high-speed video recording, to directly observe the movements associated with signal production. We describe for the first time the basic characteristics of the signals and signal emission of this species. Based on observations and analysis of the video recordings using a point-tracking algorithm, and their comparison with laser vibrometer recordings, we argue that males of C. pyrisuga produce the vibrations primarily by wing buzzing, that is, tremulation that does not involve friction between the wings and thorax. Comparing observed signal properties with previously published data, we predict that wing buzzing is the main mechanism of signal production in all vibrating psyllids.

Vibrational long-distance communication in the termites Macrotermes natalensis and Odontotermes sp.

Fungus-growing higher termites build long subterranean galleries that lead outwards from the nest to foraging sites. When soldiers are disturbed, they tend to drum with their heads against the substrate and thereby create vibrational alarm signals. The present study aimed at describing these acoustic signals, how they are elicited, produced and perceived, and how these signals propagate within the galleries and nests over long distances in two termite species of the Southern African savannah, Macrotermes natalensis and an Odontotermes sp. The signals consist of trains of pulses with a pulse repetition rate of 10-20 Hz. The galleries have physical features that promote vibrational communication and are used as channels for long-distance communication. In M. natalensis, the signal propagation velocity is ~130 m s(-1) and the signals are attenuated by ~0.4 dB per centimetre distance. Nestmates are extremely sensitive to these vibrations with a behavioural threshold amplitude of 0.012 m s(-2). Workers respond by a fast retreat into the nest and soldiers are recruited to the source of vibration. Soldiers also start to drum with a reaction time of about 0.3 s, thereby amplifying the intensity of the signal. This social long-distance communication through chains of signal-reamplifying termites results in a relatively slow propagation (1.3 m s(-1)) of the signal without decrement over distances of several metres.

Web Vibrations in Intraspecific Contests of Female Black Widow Spiders, Latrodectus hesperus.

Female black widow spiders, Latrodectus hesperus Chamberlin and Ivie (Araneae: Theridiidae), are solitary predators of arthropods with no tolerance for intruders on the webs. In California, L. hesperus are found in urban and agricultural settings and can be a phytosanitary pest in fresh produce. Spatial separation of L. hesperus webs could be determined by seasonal population densities, with territorial competition expected under high densities in the environment. However, little is known about female-female communication behaviors in this species. In 1-hr laboratory observations, displays of female-female rivalry included production of vibrational signals in a majority (20 of 30) of trials. The number of signals produced by both females was highest during the initial 10 min of trials, with signaling rate (time interval between signals) peaking during the 40-50 min observation period. The overall ratio of signals produced by the resident female and the introduced female was about 5:1, with the number of signals produced by the resident female higher than the number of signals produced by the introduced female. Analysis of rivalry signals showed a peak in magnitude (about 0.4 m/s) ranging from 6 to 23 Hz and smaller peaks at about 29, 38, and 47 Hz. Collectively, these results demonstrate that female L. hesperus exhibit territorial rivalry and that female-female rivalry is mediated by emission of vibrational signals through the web. Understanding the mechanisms of intraspecific competition in L. hesperus is required for elucidating interspecific interactions in the environment and may lead to development of novel methods to prevent spiders from colonizing crops.

Mating and post-copulation behavior in the tea leafhopper, Empoasca onukii (Hemiptera: Cicadellidae).

The tea leafhopper, Empoasca onukii, relies on substrate-borne vibrations for sexual communication and is mainly controlled with chemical pesticides, which poses risks to the environment and food safety. Based on previous studies, we conducted a series of behavioral assays by simultaneous observation of vibration signals and movement to investigate the mating and post-copulation behavior of tea leafhoppers. During mating, the activity of E. onukii was restricted to dawn and dusk and concentrated on the sixth or seventh mature leaf below the tea bud. By comparing the time spent in locating females among different males, the timely reply of females was the key factor affecting mating success. Empoasca onukii females mated only once in their lives, while males could mate multiple times. Male rivalry behavior involved two distinct strategies. The rivals could send disruptive pulses to overlap the male calling signals, locate the courting males, and drive them away after contact. Some rivals could emit mating disruption signals (MDSs) to interrupt the ongoing identification duet and establish their own mating communication. Both identification and location duets could be interrupted by playback of MDSs, which is essential to create effective synthetic signals to disrupt mating communication of E. onukii. Our study clarified the spatial and temporal distribution of E. onukii in mating and the function of MDSs, which will be essential to develop future vibrational mating disruption techniques for E. onukii and its energy-efficient application in the field.

Seismic localization of elephant rumbles as a monitoring approach.

African elephants (Loxodonta africana) are sentient and intelligent animals that use a variety of vocalizations to greet, warn or communicate with each other. Their low-frequency rumbles propagate through the air as well as through the ground and the physical properties of both media cause differences in frequency filtering and propagation distances of the respective wave. However, it is not well understood how each mode contributes to the animals' abilities to detect these rumbles and extract behavioural or spatial information. In this study, we recorded seismic and co-generated acoustic rumbles in Kenya and compared their potential use to localize the vocalizing animal using the same multi-lateration algorithms. For our experimental set-up, seismic localization has higher accuracy than acoustic, and bimodal localization does not improve results. We conclude that seismic rumbles can be used to remotely monitor and even decipher elephant social interactions, presenting us with a tool for far-reaching, non-intrusive and surprisingly informative wildlife monitoring.