Convergence in carnivorous pitcher plants reveals a mechanism for composite trait evolution.

Composite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses, and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous Nepenthes pitcher plant species independently evolved similar adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently through "spontaneous coincidence" of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty.

Spider dynamics under vertical vibration and its implications for biological vibration sensing.

Often overlooked, vibration transmission through the entire body of an animal is an important factor in understanding vibration sensing in animals. To investigate the role of dynamic properties and vibration transmission through the body, we used a modal test and lumped parameter modelling for a spider. The modal test used laser vibrometry data on a tarantula, and revealed five modes of the spider in the frequency range of 20-200 Hz. Our developed and calibrated model took into account the bounce, pitch and roll of the spider body and bounce of all the eight legs. We then performed a parametric study using this calibrated model, varying factors such as mass, inertia, leg stiffness, damping, angle and span to study what effect they had on vibration transmission. The results support that some biomechanical parameters can act as physical constraints on vibration sensing. But also, that the spider may actively control some biomechanical parameters to change the signal intensity it can sense. Furthermore, our analysis shows that the parameter changes in front and back legs have a greater influence on whole system dynamics, so may be of particular importance for active control mechanisms to facilitate biological sensing functions.

Sexual selection and predation drive the repeated evolution of stridulation in Heteroptera and other arthropods.

Acoustic and substrate-borne vibrations are among the most widely used signalling modalities in animals. Arthropods display a staggering diversity of vibroacoustic organs generating acoustic sound and/or substrate-borne vibrations, and are fundamental to our broader understanding of the evolution of animal signalling. The primary mechanism that arthropods use to generate vibroacoustic signals is stridulation, which involves the rubbing together of opposing body parts. Although stridulation is common, its behavioural context and evolutionary drivers are often hard to pinpoint, owing to limited synthesis of empirical observations on stridulatory species. This is exacerbated by the diversity of mechanisms involved and the sparsity of their description in the literature, which renders their documentation a challenging task. Here, we present the most comprehensive review to date on the systematic distribution and behavioural context of stridulation. We use the megadiverse heteropteran insects as a model, together with multiple arthropod outgroups (arachnids, myriapods, and selected pancrustaceans). We find that stridulatory vibroacoustic signalling has evolved independently at least 84 times and is present in roughly 20% of Heteroptera, representing a remarkable case of convergent evolution. By studying the behavioural context of stridulation across Heteroptera and 189 outgroup lineages, we find that predation pressure and sexual selection are the main behaviours associated with stridulation across arthropods, adding further evidence for their role as drivers of large-scale signalling and morphological innovation in animals. Remarkably, the absence of tympanal ears in most Heteroptera suggests that they typically cannot detect the acoustic component of their stridulatory signals. This demonstrates that the adoption of new signalling modalities is not always correlated with the ability to perceive those signals, especially when these signals are directed towards interspecific receivers in defensive contexts. Furthermore, by mapping their morphology and systematic distribution, we show that stridulatory organs tend to evolve in specific body parts, likely originating from cleaning motions and pre-copulatory displays that are common to most arthropods. By synthesising our understanding of stridulation and stridulatory organs across major arthropod groups, we create the necessary framework for future studies to explore their systematic and behavioural significance, their potential role in sensory evolution and innovation, and the biomechanics of this mode of signalling.

Slit sense organ distribution on the legs of two species of orb-weaving spider (Araneae: Araneidae).

Biotic and abiotic mechanical stimuli are ubiquitous in the environment, and are a widely used source of sensory information in arthropods. Spiders sense mechanical stimuli using hundreds of slit sense organs (small isolated slits, large isolated slits, groups of slits and lyriform organs) distributed across their bodies and appendages. These slit sense organs are embedded in the exoskeleton and detect cuticular strain. Therefore, the spatial pattern of these sensors can give clues into how mechanical stimuli from different sources might be processed and filtered as they are transmitted through the body. Here, we map the distribution of slit sense organs on the legs in two species of orb-weaving spider, A. diadematus and T. edulis, in which slit sense organ distribution has not previously been investigated. We image the spiders' legs using scanning electron microscopy, and trace the position and orientation of slits on these images to describe the distribution and external morphology of the slit sense organs. We show that both species have a similar distribution of slit sense organs, with small isolated slits occurring in consistent lines parallel to the long axis of the legs, whilst large isolated slits, groups of slits and lyriform organs appear in fixed positions near the leg joints. Our findings support what has been described in the literature for several other species of spider, which indicates that slit organ arrangement is conserved across spiders in different evolutionary lineages and with disparate hunting strategies. The dispersed distribution of small isolated slits along the whole length of the leg may be used to detect large-scale strain of the leg segment as a result of muscle activity or internal changes in haemolymph pressure.

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.

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.

Dynamic environments do not appear to constrain spider web building behaviour.

Many laboratory experiments demonstrate how orb-web spiders change the architecture of their webs in response to prey, surroundings and wind loading. The overall shape of the web and a range of other web parameters are determined by frame and anchor threads. In the wild, unlike the lab, the anchor threads are attached to branches and leaves that are not stationary but move, which affects the thread tension field. Here we experimentally test the effect of a moving support structure on the construction behaviour and web-parameters of the garden cross spider Araneus diadematus. We found no significant differences in building behaviour between rigid and moving anchors in total time spent and total distance covered nor in the percentage of the total time spent and distance covered to build the three major web components: radials, auxiliary and capture spirals. Moreover, measured key parameters of web-geometry were equally unaffected. These results call for re-evaluation of common understanding of spider webs as thread tensions are often considered to be a major factor guiding the spider during construction and web-operation.

Correction: Planthopper bugs use a fast, cyclic elastic recoil mechanism for effective vibrational communication at small body size.

[This corrects the article DOI: 10.1371/journal.pbio.3000155.].

Functional flexibility in a spider's orb web.

Web spiders rely on vibrations propagated via their web to identify, locate and capture entangled prey. Here, we experimentally tested the robustness of the orb weaver's predation strategy when webs are severely distorted and silk tensions are drastically altered throughout the web, a common occurrence in the wild. We assessed prey identification efficiency by comparing the spider's initial reaction times towards a fruit fly trapped in the web, we measured location efficiency by comparing times and number of tugging bouts performed, and we determined capture efficiency by comparing capture times. It emerged that spiders are capable of identifying, locating and capturing prey in distorted webs, albeit taking somewhat longer to do so.

On the morphology and evolution of cicadomorphan tymbal organs.

Cicadas and many of their relatives (Hemiptera: Cicadomorpha) generate vibroacoustic signals using tymbal organs located on their first two abdominal segments. Although tymbals are well-studied in Cicadidae, their systematic distribution in other Cicadomorpha and their possible homologies to the vibroacoustic mechanisms of other Hemiptera have been debated for more than a century. In the present study, we re-examine the morphology of the musculoskeletal system of cicadomorphan vibroacoustic organs, and we document their systematic distribution in 78 species drawn from across the phylogeny of Cicadomorpha. We also compare their morphology to the recently-described snapping organ of planthoppers (Fulgoromorpha). Based on the structure and innervation of the metathoracic and abdominal musculoskeletal system, we find that several key elements of cicadomorphan vibroacoustic organs that have previously been assigned to the first abdominal segment in fact belong to the second. We find that tymbal organs are nearly ubiquitous in Cicadomorpha, and conclude based on their phylogenetic distribution, that they are likely to be synapomorphic. The unusual tymbal-like organs of the Deltocephalinae and Typhlocybinae, represent derived modifications. Finally, we propose a standardised terminology for sternal components of the cicadomorphan vibrational organs, which can be used in future taxonomic descriptions.

On the morphology and possible function of two putative vibroacoustic mechanisms in derbid planthoppers (Hemiptera: Fulgoromorpha: Derbidae).

A mechanism involving interaction of the metathoracic wing and third abdominal segment of derbid planthoppers was first discovered over a century ago, and interpreted as a stridulatory organ for sound production. Although referred to occasionally in later taxonomic works, the detailed morphology, systematic distribution, and behavioural significance of this structure have remained unknown, and its proposed use in sound production has never been corroborated. Here we examine the distribution and morphology of the supposed stridulatory organ of Derbidae and the recently-described vibratory mechanism of planthoppers - the snapping organ, across 168 species covering the entire taxonomic spectrum of the family. We find that many derbids possess snapping organs morphologically similar to those of other planthoppers, and find no evidence for the presence of tymbal organs, which were previously thought to generate vibrational signals in derbids. We find the supposed stridulatory mechanism to be widespread in Derbidae, and conclude that it provides several systematically and taxonomically important characters. Nevertheless, its morphology appears unsuitable for the production of sound, and we instead speculate that the mechanism plays a role in spreading chemical secretions or wax. Finally, we observe wax production by tergal glands in derbid larvae, and illustrate their external morphology in adults.

Planthopper bugs use a fast, cyclic elastic recoil mechanism for effective vibrational communication at small body size.

Vibrations through substrates are an important source of information for diverse organisms, from nematodes to elephants. The fundamental challenge for small animals using vibrational communication is to move their limited mass fast enough to provide sufficient kinetic energy for effective information transfer through the substrate whilst optimising energy efficiency over repeated cycles. Here, we describe a vibratory organ found across a commercially important group of plant-feeding insects, the planthoppers (Hemiptera: Fulgoromorpha). This elastic recoil snapping organ generates substrate-borne broadband vibrations using fast, cyclical abdominal motion that transfers kinetic energy to the substrate through the legs. Elastic potential energy is stored and released twice using two different latched energy-storage mechanisms, each utilising a different form of elastic recoil to increase the speed of motion. Comparison to the acoustic tymbal organ of cicadas (Hemiptera: Cicadomorpha) reveals functional convergence in their use of elastic mechanisms to increase the efficacy of mechanical communication.

Vibration sensitivity found in Caenorhabditis elegans.

Mechanical sensing is important for all organisms, but is the least understood of the senses. As mechanical stimuli come in diverse forms, organisms often have sensors or sensory systems that specialise in a form of mechanical stimuli, such as touch or vibration. Here, we tested the hypothesis that the nematode worm Caenorhabditis elegans exhibits a behavioural response to vibration that is distinct from its responses to touch. We show that wild-type strain worms respond to sustained low-frequency vibration in a manner distinct from the known responses to non-localised mechanical stimuli. Furthermore, the behavioural responses of mutant strains suggest different roles for ciliated versus non-ciliated neurons in mediating the response. Although further study is required to identify the vibration-sensing pathway, our data support that C. elegans can sense substrate-borne vibrations using cells distinct from those used in gentle touch.

Classifying elephant behaviour through seismic vibrations.

Seismic waves - vibrations within and along the Earth's surface - are ubiquitous sources of information. During propagation, physical factors can obscure information transfer via vibrations and influence propagation range [1]. Here, we explore how terrain type and background seismic noise influence the propagation of seismic vibrations generated by African elephants. In Kenya, we recorded the ground-based vibrations of different wild elephant behaviours, such as locomotion and infrasonic vocalisations [2], as well as natural and anthropogenic seismic noise. We employed techniques from seismology to transform the geophone recordings into source functions - the time-varying seismic signature generated at the source. We used computer modelling to constrain the propagation ranges of elephant seismic vibrations for different terrains and noise levels. Behaviours that generate a high force on a sandy terrain with low noise propagate the furthest, over the kilometre scale. Our modelling also predicts that specific elephant behaviours can be distinguished and monitored over a range of propagation distances and noise levels. We conclude that seismic cues have considerable potential for both behavioural classification and remote monitoring of wildlife. In particular, classifying the seismic signatures of specific behaviours of large mammals remotely in real time, such as elephant running, could inform on poaching threats.

The pregenital abdomen of Enicocephalomorpha and morphological evidence for different modes of communication at the dawn of heteropteran evolution.

The internal and external anatomy of the posterior metathoracic region, pregenital abdomen, and associated nervous system of the heteropteran infraorder Enicocephalomorpha are thoroughly described, using an array of state-of-the art techniques. Based on morphology, it is hypothesised which modes of communication these insects use. This study is based primarily on an undescribed species of Cocles Bergroth, 1905 (Enicocephalidae) and another undescribed species of Lomagostus Villiers, 1958 (Aenictopecheidae), but additional representatives of the infraorder are also examined. Our results are compared with the literature on other Heteroptera. The metathoracic scent gland system of Enicocephalomorpha uses the same muscles as that of more derived Heteroptera, although the efferent system is different. The presence of a tergal plate and well-developed longitudinal musculature in the families Enicocephalidae and Aenictopecheidae, as well as a sexually dimorphic set of sclerites and membranes that allow an as yet undetermined type of motion, may indicate the presence of vibrational signaling in the infraorder, although experimental confirmation is required. Our findings raise new research questions regarding heteropteran functional morphology and communication.

Glass transitions in native silk fibres studied by dynamic mechanical thermal analysis.

Silks are a family of semi-crystalline structural materials, spun naturally by insects, spiders and even crustaceans. Compared to the characteristic ß-sheet crystalline structure in silks, the non-crystalline structure and its composition deserves more attention as it is equally critical to the filaments' high toughness and strength. Here we further unravel the structure-property relationship in silks using Dynamic Mechanical Thermal Analysis (DMTA). This technique allows us to examine the most important structural relaxation event of the disordered structure the disordered structure, the glass transition (GT), in native silk fibres of the lepidopteran Bombyx mori and Antheraea pernyi and the spider Nephila edulis. The measured glass transition temperature Tg, loss tangent tan δ and dynamic storage modulus are quantitatively modelled based on Group Interaction Modelling (GIM). The "variability" issue in native silks can be conveniently explained by the different degrees of structural disorder as revealed by DMTA. The new insights will facilitate a more comprehensive understanding of the structure-property relations for a wide range of biopolymers.

Unpicking the signal thread of the sector web spider Zygiella x-notata.

Remote sensing allows an animal to extend its morphology with appropriate conductive materials and sensors providing environmental feedback from spatially removed locations. For example, the sector web spider Zygiella x-notata uses a specialized thread as both a structural bridge and signal transmitter to monitor web vibrations from its retreat at the web perimeter. To unravel this model multifunctional system, we investigated Zygiella's signal thread structure with a range of techniques, including tensile testing, laser vibrometry, electron microscopy and behavioural analysis. We found that signal threads varied significantly in the number of filaments; a result of the spider adding a lifeline each time it runs along the bridge. Our mechanical property analysis suggests that while the structure varies, its normalized load does not. We propose that the signal thread represents a complex and fully integrated multifunctional structure where filaments can be added, thus increasing absolute load-bearing capacity while maintaining signal fidelity. We conclude that such structures may serve as inspiration for remote sensing design strategies.

Linking naturally and unnaturally spun silks through the forced reeling of Bombyx mori.

The forced reeling of silkworms offers the potential to produce a spectrum of silk filaments, spun from natural silk dope and subjected to carefully controlled applied processing conditions. Here we demonstrate that the envelope of stress-strain properties for forced reeled silks can encompass both naturally spun cocoon silk and unnaturally processed artificial silk filaments. We use dynamic mechanical thermal analysis (DMTA) to quantify the structural properties of these silks. Using this well-established mechanical spectroscopic technique, we show high variation in the mechanical properties and the associated degree of disordered hydrogen-bonded structures in forced reeled silks. Furthermore, we show that this disorder can be manipulated by a range of processing conditions and even ameliorated under certain parameters, such as annealing under heat and mechanical load. We conclude that the powerful combination of forced reeling silk and DMTA has tied together native/natural and synthetic/unnatural extrusion spinning. The presented techniques therefore have the ability to define the potential of Bombyx-derived proteins for use in fibre-based applications and serve as a roadmap to improve fibre quality via post-processing.

The speed of sound in silk: linking material performance to biological function.

Sonic properties of spider silks are measured independent of the web using laser vibrometry and ballistic impact providing insights into Nature's design of functionalized high-performance materials. Through comparison to cocoon silk and other industrial fibers, we find that major ampullate silk has the largest wavespeed range of any known material.

Forced reeling of Bombyx mori silk: separating behavior and processing conditions.

Controlled reeling is a powerful tool to investigate the details of silk processing. However, consistent forced reeling of silkworms is hindered by the significant degree of behaviorally induced variation caused by the animal. This paper proposes silkworm paralysis as a novel method to control the animal and thus in vivo spinning conditions. Using these methods, we achieve low and consistent reeling forces during the collection of over 500 m of individual silk fiber while monitoring filament variability, morphology, and properties. Novel techniques to measure the irregular silk cross-sectional areas lead to the more accurate calculation of the true engineering values and mechanical property variation of individual silk fibers. Combining controlled reeling and accurate thread measurement techniques allows us to present the relative contributions of processing and behavior in the performance envelope of Bombyx mori silk.