Agonistic signals received by an arthropod filiform hair allude to the prevalence of near-field sound communication

Arthropod filiform hairs respond to air particle movements and are among the most sensitive animal sensory organs. In many species, they are tuned to detect predators or prey and trigger escape or prey capture behaviours. Here we show for the first time that these hairs also receive intraspecific near-field sound signals in an arachnid. During agonistic encounters, whip spiders (Arachnida, Amblypygi) perform antenniform leg vibration (ALV) displays that have significantly longer duration in contest winners than losers. During an ALV display: (i) the vibrating antenniform leg of the displaying whip spider is positioned close to the trichobothria (filiform hairs) on its opponent's walking legs, (ii) the vibrating antenniform leg can excite these trichobothria via air movements and without direct contact, (iii) the antenniform leg of the displaying whip spider vibrates at a frequency that causes particularly strong, sustained excitation and little adaptation in the trichobothria, and (iv) the duration of an ALV display can be extracted from the response of a trichobothrium. Since filiform hairs are widespread among arthropods, communication via such hairs could be extremely prevalent.     

The sensory equipment of a spider – A morphological survey of different types of sensillum in both sexes of Argiope bruennichi (Araneae,Araneidae)

Spiders show a wide range of sensory capabilities as evidenced by behavioural observations. Accordingly, spiders possess diverse sensory structures like mechano-, hygro-, thermo- or chemoreceptive sensilla. As to chemoreceptive structures, only trichoid tip-pore sensilla were found so far that were tested for gustation. That spiders are also able to receive airborne signals is corroborated by numerous behavioural experiments but the responsible structures have not been determined yet. Here, we provide sensilla distribution maps of pedipalps and walking legs of both sexes of the wasp spider Argiope bruennichi whose biology and mating system is well explored. By means of scanning electron microscopy, we scrutinized whether there is in fact only one type of trichoid pore sensillum and if so, if there are deviations in the outer structure of the tip-pore sensilla depending on their position on the body. We also describe the external structure and distribution of slit sense organs, trichobothria and tarsal organs. Our study shows that all four sensillum types occur on pedipalps and walking legs of both sexes. As to chemosensory organs, only tip-pore sensilla were found, suggesting that this sensillum type is used for both gustation and olfaction. The highest numbers of tip-pore sensilla were observed on metatarsi and tarsi of the first two walking legs. Mechanosensitive slit sense organs occur as single slit sensilla in rows along all podomers or as lyriform organs next to the joints. The mechanosensitive trichobothria occur on the basal part of tibiae and metatarsi. Tarsal organs occur on the dorsal side of all tarsi and the male cymbium. The distribution maps of the sensilla are the starting point for further exploration of internal, morphological differences of the sensilla from different regions on the body. Cryptic anatomical differences might be linked to functional differences that can be explored in combination with electrophysiological analyses. Consequently, the maps will help to elucidate the sensory world of spiders.     

The formation of the antenna sensory apparatus in some bug (Heteroptera) species in the course of their postembryonic development

In the antenna sensory apparatus of bugs Coreus marginatus, Cimex lectularius, and Rhodnius prolixus sensilla of the four main types are identified: chaetica, trichodea, basiconica, and coeloconica. Chaetoid sensilla are differentiated into two subtypes: sensilla with cogged cuticles and those with smooth ones; trichoid sensilla were divided into long pointed and short ones with blunt tips. In larvae and adults of R. prolixus trichobothria (long filiform hairs) were found on the medial side of pedicellum. The postembryonic changes in the quantitative and qualitative composition of the antenna sensory apparatus were assessed using biometric analysis. The greatest increase of sensory organs was observed upon the nymphal ecdysis from the 5th instar to adult.     

Sounds Modulate Males’ Aggressiveness in a Cichlid Fish

Acoustic signals are produced in many fish species during agonistic or courtship interactions. A way to test the biological role of these sounds is the use of acoustic playback experiments. However, sounds are usually associated with visual displays and playback experiments performed in fish so far, often failed to match acoustic and visual stimuli. To avoid this mismatch issue, we experimentally separated or coupled visual and acoustic channels to test the role of sounds produced during male–male aggressive interactions in a cichlid fish, Metriaclima zebra. Results show that aggressive behaviour is based on visual stimuli and that acoustic signals alone never trigger aggression. Furthermore, the association between visual and acoustic channels lowers the level of aggressiveness found when fish can only interact visually. This suggests that acoustic signals used during a dispute may complement visual displays to modulate males’ behaviour by reducing their aggressiveness and the risk of escalated fights.     

Fine Structure of the Trichobothria and their Regeneration during Moulting in the Whip Scorpion Typopeltis crucifer Pocock, 1894

Abstract The highly complicated structure of the trichobothrium in the whip scorpion Typopeltis crucifer (Uropygi, Arachnida) has been reconstructed from ultra-thin serial sections. The spatial positions of two trichobothria on the first pair of legs, as well as their innervation by several dendrites point to an effective spatial localization of stimulus sources. Numerous cells are involved in the regeneration of the trichobothrium during moulting. They can be classified according to their position and function in forming the sensillum: there are 11 sensory cells, four inner envelope cells, about 21 trichogen cells and numerous outer envelope cells, including tormogen cells. The complicated cell pattern is compared to conditions in similar sensilla of other arthropods in terms of function and phylogeny.     

Behavioural evidence of UV sensitivity in jumping spiders (Araneae: Salticidae)

Jumping spiders are known to possess ultraviolet (UV) receptors in the retinas of their large-principal eyes. The existence of UV visual cells, however, does not prove that jumping spiders can see into the UV part of spectrum (300–400 nm) or whether such an ability plays any role in salticid intra-specific interactions. In the study reported herein, we performed behavioural experiments to test whether a UV−reflecting jumping spider, Cosmophasis umbratica, is sensitive to UV wavelengths and whether UV cues are important in intra-specific communication. The absence of UV cues not only affected intra-specific behaviour by significantly reducing the frequency of agonistic displays, but also elicited unprecedented courtship displays in males towards their own mirror images and conspecific opponents. Furthermore, C. umbratica males were able to respond rapidly to changes in UV cues of conspecific mirror images by switching between agonistic and courtship displays. These findings clearly demonstrate that C. umbratica males are capable of seeing UV wavelengths and that UV cues are necessary and sufficient for this species to enable the agonistic displays. Hence, UV light may have an important role to play in intra-specific communication in jumping spiders.     

Non‐sex‐biased Dominance in a Sexually Monomorphic Electric Fish: Fight Structure and Submissive Electric Signalling

Males and females commonly compete for limited resources. When interaction costs are similar for both sexes and there are no sexual differences in resource value estimation, a non‐sex‐biased dominance is expected. Moreover, only non‐sex‐biased assessment of contenders fighting ability (Resource Holding Potential, RHP) should influence contest decisions. To test these predictions, we evaluated non‐breeding agonistic intra‐ and intersexual dyadic interactions in the weakly electric fish, Gymnotus omarorum. During the non‐breeding season, resource value is not expected to depend on individuals’ reproductive status and should thus be equal for males and females. In addition, as G. omarorum presents no sexual differences in body size, interaction costs can be considered symmetric between sexes. We confirmed that body size differences, but not individuals’ gender, is the best predictor of dominance. We correlated RHP asymmetries with contest duration and evidenced that body size but not sex influences assessment in intrasexual and intersexual encounters. All dyads tested engaged in agonistic interactions (N = 33) in which a clear dominant emerged. The analysis of conflict phases evidenced the submissive role of electric displays. Electric organ discharge (EOD) interruptions appear early in the contest as an electric hiding attempt, whereas chirps are post‐resolution signals of subordinate status. Interestingly, the decision of interrupting the EOD was also influenced by RHP asymmetries, whereas chirping activity was influenced by the intensity of the attacks received. Our results confirm that body size is the best RHP proxy in non‐breeding intra‐ and intersexual contests of this monomorphic species and demonstrated a sequential pattern of submissive signalling by means of two different electric displays.     

Fine structure of tarsal sensory organs in the whip spider Admetus pumilio (Amblypygi, Arachnida).

The sensory organs on the tarsi of the antenniform first legs of the whip spider Admetus pumilio C. L. Koch (Amblypygi, Arachnida) were examined with the scanning and transmission electron microscope. At least four different types of hair sensilla were found: (1) thick-walled bristles, which have the characteristics of contact chemoreceptors (several chemoreceptive dendrites in the lumen plus two mechanoreceptors at the base); (2) short club sensilla, innervated by 4-6 neurons which terminate in a pore on the tip; they are possibly humidity receptors; (3) porous sensilla, which are either innervated by 20-25 neurons and have typical pore tubules, or they have 40-45 neurons but no pore tubules; both types are considered to be olfactory; (4) rod sensilla occur in clusters near segmental borders; they are innervated by only one large dendrite which branches inside the lumen. Other tarsal receptors are the claws, which correspond to contact chemoreceptors, and the pit organ which resembles the tarsal organ of spiders. Compared to other arthropod sensilla, the contact chemoreceptors are very similar to those of spiders, while the porous sensilla correspond structurally to olfactory receptors in insects; the club and rod sensilla seem to be typical for amblypygids.     

Digger wasp against crickets. II. An airborne signal produced by a running predator

Summary Females of the digger wasp Liris niger Fabr. hunt crickets to provide food for their offspring by running with high velocity on the ground (>20–50 cm/s). Crickets are able to detect the running wasps by the air particle movement generated by the predator. We measured signals produced by running wasps using a microphone sensitive to air particle velocity. The wasps generated single air puffs with peak air particle velocities of 1–2 cm/s measured close to the running wasp. We measured frequency spectra of the signals containing only components below 50 Hz, with increasing intensities towards lower frequencies, especially below 10 Hz.We measured the air particle movement generated by artificially moved wasps, crickets or a styrofoam dummy of similar size to investigate the effect of velocity and shape of the moving object upon the composition of the signal. The velocity of movement appeared to be important for the intensity and frequency composition of the air particle movement. The shape of the moved body had an influence on the intensity but only little effect on the frequency spectrum. Measurements with a thermistor anemometer showed that a moving object caused air currents lasting longer than 100 ms after passing or approaching the probe. The air particle movements generated by hunting wasps are entirely sufficient with respect to intensity and frequency range to be registered by the filiform hair sensilla upon the cerci of crickets.     

Multi-Modal Use of a Socially Directed Call in Bonobos

‘Contest hoots’ are acoustically complex vocalisations produced by adult and subadult male bonobos (Pan paniscus). These calls are often directed at specific individuals and regularly combined with gestures and other body signals. The aim of our study was to describe the multi-modal use of this call type and to clarify its communicative and social function. To this end, we observed two large groups of bonobos, which generated a sample of 585 communicative interactions initiated by 10 different males. We found that contest hooting, with or without other associated signals, was produced to challenge and provoke a social reaction in the targeted individual, usually agonistic chase. Interestingly, ‘contest hoots’ were sometimes also used during friendly play. In both contexts, males were highly selective in whom they targeted by preferentially choosing individuals of equal or higher social rank, suggesting that the calls functioned to assert social status. Multi-modal sequences were not more successful in eliciting reactions than contest hoots given alone, but we found a significant difference in the choice of associated gestures between playful and agonistic contexts. During friendly play, contest hoots were significantly more often combined with soft than rough gestures compared to agonistic challenges, while the calls'' acoustic structure remained the same. We conclude that contest hoots indicate the signaller''s intention to interact socially with important group members, while the gestures provide additional cues concerning the nature of the desired interaction.     

Information content of male agonistic displays in the territorial tawny dragon (Ctenophorus decresii)

Two potential signals used during male–male agonistic encounters were examined for signal content in the territorial agamid lizard Ctenophorus decresii, or tawny dragon. Males have black chest patches, which are apparent when they posture during agonistic encounters. Patches are not condition or size dependent. The area of the patches is positively associated with levels of aggression and likelihood of winning a fight. The patch thus functions as a badge of status indicating male aggression. The complex dynamic displays given by males contain information on male endurance and size. The number of push-ups given during a display reflects the aggressiveness of an animal. There was no relationship between patch size and endurance. There is some overlap in the content of the two signals, both contain information on aggressiveness, suggesting that they may function as back-up signals. The multiple-message hypothesis is not ruled out as endurance and size are only related to the dynamic displays. However, it is not clear that endurance is an important determinant of contest outcomes in this species, and so it is not certain that the receiver uses this information.     

Tactile learning by a whip spider, <Emphasis Type="Italic">Phrynus marginemaculatus</Emphasis> C.L. Koch (Arachnida,Amblypygi)

The ability of animals to learn and remember underpins many behavioural actions and can be crucial for survival in certain contexts, for example in finding and recognising a habitual refuge. The sensory cues that an animal learns in such situations are to an extent determined by its own sensory specialisations. Whip spiders (Arachnida, Amblypygi) are nocturnal and possess uniquely specialised sensory systems that include elongated ‘antenniform’ forelegs specialised for use as chemo- and mechanosensory feelers. We tested the tactile learning abilities of the whip spider Phrynus marginemaculatus in a maze learning task with two tactile cues of different texture—one associated with an accessible refuge, and the other with an inaccessible refuge. Over ten training trials, whip spiders got faster and more accurate at finding the accessible refuge. During a subsequent test trial where both refuges were inaccessible, whip spiders searched for significantly longer at the tactile cue previously associated with the accessible refuge. Using high-speed cinematography, we describe three distinct antenniform leg movements used by whip spiders during tactile examination. We discuss the potential importance of tactile learning in whip spider behaviour and a possible role for their unique giant sensory neurons in accessing tactile information.     

Development of cricket sensory hairs: changes of dynamic mechanical properties

Summary Mechanical oscillation properties of cricket (Acheta domesticus) filiform hair sensilla were measured at different larval stages, as an indication of larval sensory capacities and for comparison with data in the literature on central nervous changes during development. The hairs were stimulated by airborne vibration over a frequency range of 10 to 220 Hz. Best frequency, angular displacement at best frequency, slope of angular-displacement tuning curve and phase of hair deflection relative to air particle velocity were tested for correlation with hair length, which is proportional to the age of a sensillum. The ranges found for the various oscillation parameters in early larval stages were similar to or larger than those in adults. Oscillation properties changed with both the developmental stage of the hair sensilla and that of the whole animal. Four individually identifiable hair sensilla were analysed separately; the sensory neurons of two of them are known to change synaptic properties during maturation. Angular displacement at a given stimulus intensity was maximal for all hairs after differentiation, and decreased during further development. The hairs did not show clear common changes for any of the other oscillation parameters. Yet particular changes were found for individual hairs.     

The morphology of spider sensilla. I. Mechanoreceptors

The common tactile hair sensilla of spider tarsi were studied in web spiders (Araneus) and ground spiders (Lycosa, Dugesiella) using scanning and transmission electron microscopy. All of these sensilla are innervated by three bipolar neurons whose dendrites end proximally at the sensillum base. Each dendritic terminal exhibits a tubular body, a dense array of microtubules typical for mechanoreceptive sensilla. A dendritic sheath encloses the outer dendritic segments and connects the dendritic terminals to cuticular components of the hair sensillum in three different ways: (1) A distal extension of the dendritic sheath connects to the midline of the hair base; (2) A forked arrangement of cuticular (?) strands attaches on both lateral sides of the hair base, and (3) The socket cuticle directly contacts a part of the dendritic sheath. The latter connection provides a fixed position for the three dendritic terminals and any movement of the hair shaft could be transmitted via connections (I) and (2). The triple innervation strongly suggests a directional sensitivity of these sensilla.Structural comparison between arachnid and insect mechanoreceptive sensilla indicates that tactile hair sensilla in Arachnida are multi-innervated whereas the corresponding reccptors in Insecta are singly innervated.     

Modeling arthropod filiform hair motion using the penalty immersed boundary method

Crickets are able to sense their surrounding environment through about 2000 filiform hairs located on a pair of abdominal cerci. The mechanism by which the cricket is able to sense a wide range of input signals using these filiform hairs of different length and orientation is of great interest. Most of the previous filiform hair models have focused on a single, rigid hair in an idealized air field. Here, we present a model of the cercus and filiform hairs that are mechanically coupled to the surrounding air, and the model equations are based on the penalty immersed boundary method. The key difference between the penalty immersed boundary method and the traditional immersed boundary method is the addition of forces to account for density differences between the immersed solid (the filiform hairs) and the surrounding fluid (air). The model is validated by comparing the model predictions to experimental results, and then the model is used to examine the interactions between multiple hairs. With multiple hairs, there is little interaction when the hairs are separated by more than 1mm, and, as they move closer, they interact through viscous coupling, which reduces the deflection of the hairs due to the air movement. We also examine the computational scalability of the algorithm and show that the computational costs grow linearly with the number of hairs being modeled.     

Testing compatibility between molecular and morphological techniques for arthropod systematics: a minimally destructive DNA extraction method that preserves morphological integrity, and the effect of lactic acid on DNA quality

Three practical aspects related to the preservation and destruction of DNA and/or morphological characters of spiders were examined: potential morphological damage during non-destructive DNA extraction was assessed by counting trichobothria, a fragile sensorial feature found on spider legs; the effect on yield of non-destructive DNA extraction; and whether possible DNA degradation is caused by residues of lactic acid, which is used as a temporary mounting medium for the study of morphological structures in spiders and insects. Destructive extractions yielded higher amounts of DNA than non-destructive methods. However, non-destructive methods yielded usable amounts of DNA while leaving delicate trichobothria intact. Of the non-destructive extractions, a longer digestion period (36 h vs. 12) yielded higher amounts of DNA and did not damage trichobothria. Lactic acid did not induce short-term DNA degradation or inhibit PCR reactions, even at high concentrations. These results show compatibility between molecular and morphological requirements without compromising DNA quality or specimen integrity.     

Signal response is context-dependent in Polistes dominula

Journal of Ethology - Theory suggests honest status signals mediate agonistic interactions between unfamiliar individuals, but may be less important during interactions between familiar...     

The aerodynamic signature of running spiders

Many predators display two foraging modes, an ambush strategy and a cruising mode. These foraging strategies have been classically studied in energetic, biomechanical and ecological terms, without considering the role of signals produced by predators and perceived by prey. Wolf spiders are a typical example; they hunt in leaf litter either using an ambush strategy or by moving at high speed, taking over unwary prey. Air flow upstream of running spiders is a source of information for escaping prey, such as crickets and cockroaches. However, air displacement by running arthropods has not been previously examined. Here we show, using digital particle image velocimetry, that running spiders are highly conspicuous aerodynamically, due to substantial air displacement detectable up to several centimetres in front of them. This study explains the bimodal distribution of spider's foraging modes in terms of sensory ecology and is consistent with the escape distances and speeds of cricket prey. These findings may be relevant to the large and diverse array of arthropod prey-predator interactions in leaf litter.     

A sequential analysis of female aggression in a group of lesser galagos (Galago senegalensis)

A sequential analysis of behaviors preceding agonistic interactions between female lesser galagos demonstrated that aggression usually follows locomotor or interactive, as opposed to solitary, behavior. Leaping or leaving a nest box followed by mutual staring is a frequent component preceding both chases and displacements. The probability of predicting an agonistic interaction is improved when more behaviors are examined in sequence, although one cannot predict aggression with certainty due to the variability of preceding sequences. Mutual staring is suggested to be an evolutionary precursor to elaborate visual threat signals.     

Role of the olfactory pathway in agonistic behavior of crayfish, <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

Crayfish establish social dominance hierarchies through agonistic interactions, and these hierarchies are maintained through assessment of social status. Chemical signals influence several aspects of fighting behavior, but the specific chemosensory sensilla involved in detecting these signals in crayfish are unknown. The goal of our study was to examine the importance of aesthetasc sensilla—olfactory sensors on the antennules of decapod crustaceans—in regulating changes in fighting behavior in crayfish, Procambarus clarkii, over the course of repeated pairings. We selectively ablated aesthetascs from pairs of crayfish after the first day of trials and compared the behavior of these ablated animals to that of pairs of intact controls. Results show that unablated crayfish significantly decreased the number and duration of fights over repeated pairings, whereas crayfish lacking aesthetascs continued to engage in similar amounts of fighting across all three trial days. This difference shows that aesthetascs regulate fighting behavior in P. clarkii.