Noise affects the shape of female preference functions for acoustic signals

The shape of female mate preference functions influences the speed and direction of sexual signal evolution. However, the expression of female preferences is modulated by interactions between environmental conditions and the female's sensory processing system. Noise is an especially relevant environmental condition because it interferes directly with the neural processing of signals. Although noise is therefore likely a significant force in the evolution of communication systems, little is known about its effects on preference function shape. In the grasshopper Chorthippus biguttulus, female preferences for male calling song characteristics are likely to be affected by noise because its auditory system is sensitive to fine temporal details of songs. We measured female preference functions for variation in male song characteristics in several levels of masking noise and found strong effects of noise on preference function shape. The overall responsiveness to signals in noise generally decreased. Preference strength increased for some signal characteristics and decreased for others, largely corresponding to expectations based on neurophysiological studies of acoustic signal processing. These results suggest that different signal characteristics will be favored under different noise conditions, and thus that signal evolution may proceed differently depending on the extent and temporal patterning of environmental noise.     

Regeneration of axotomized tympanal nerve fibres in the adult grasshopper Chorthippus biguttulus (L.) (Orthoptera: Acrididae) correlates with regaining the localization ability

Adult males of the grasshopper Chorthippus biguttulus exhibit a stereotyped turning behaviour towards the direction of the female song. This behaviour has been used to study the regeneration of synaptic connections used for pattern recognition and sound localization. Unilaterally deafened animals are not able to localize the sound direction and turn exclusively towards the intact side, regardless of the speaker position. This behaviour does not change with postoperative time. After an axotomy of the tympanic nerve fibres the sensory axons regrow and regenerate their synaptic contacts which is deduced from the recovery of the ability to localize sound. The behavioural threshold for stimulation from the operated side is increased by approx. 5 dB SPL. The probability of correct turning towards the operated side increases with postoperative time. The ability for lateralization improves with postoperative time and may reach values of intact animals (discrimination of 1–2 dB SPL difference. Animals with two operations (axotomy of one tympanal nerve and blocking of the other ear) do not react to the female song, which suggests that recognition of the species-specific song pattern is not possible with the regenerated fibres and their synaptic connections alone. Neuroanatomical studies show that the regeneration of localization ability is correlated with an ingrowth of sensory fibres into the frontal auditory neuropil of the metathoracic ganglion.     

Neural mechanisms of auditory species recognition in birds

Auditory communication in humans and other animals frequently takes place in noisy environments with many co‐occurring signallers. Receivers are thus challenged to rapidly recognize salient auditory signals and filter out irrelevant sounds. Most bird species produce a variety of complex vocalizations that function to communicate with other members of their own species and behavioural evidence broadly supports preferences for conspecific over heterospecific sounds (auditory species recognition). However, it remains unclear whether such auditory signals are categorically recognized by the sensory and central nervous system. Here, we review 53 published studies that compare avian neural responses between conspecific versus heterospecific vocalizations. Irrespective of the techniques used to characterize neural activity, distinct nuclei of the auditory forebrain are consistently shown to be repeatedly conspecific selective across taxa, even in response to unfamiliar individuals with distinct acoustic properties. Yet, species‐specific neural discrimination is not a stereotyped auditory response, but is modulated according to its salience depending, for example, on ontogenetic exposure to conspecific versus heterospecific stimuli. Neuromodulators, in particular norepinephrine, may mediate species recognition by regulating the accuracy of neuronal coding for salient conspecific stimuli. Our review lends strong support for neural structures that categorically recognize conspecific signals despite the highly variable physical properties of the stimulus. The available data are in support of a ‘perceptual filter’‐based mechanism to determine the saliency of the signal, in that species identity and social experience combine to influence the neural processing of species‐specific auditory stimuli. Finally, we present hypotheses and their testable predictions, to propose next steps in species‐recognition research into the emerging model of the neural conceptual construct in avian auditory recognition.     

Species Recognition Influences Female Mate Preferences in the Common European Grasshopper (Chorthippus biguttulus Linnaeus, 1758)

Species recognition and intraspecific mating preferences constitute two basic aspects of animal communication. Both can be considered as variations in response to signals and it has been suggested that they represent a continuum. Selection on species recognition could therefore influence intraspecific mating preferences. We show that females of the common European grasshopper Chorthippus biguttulus prefer conspecific male signals that can be distinguished more reliably from sympatrically occurring heterospecific signals. This suggests that in C. biguttulus, sexual selection might be influenced by pleiotropic effects from species recognition. The results show how the heterospecific signal environment could have determined why and in which direction specific traits become sexually selected.     

Behavioural divergence,interfertility and speciation: A review

Behavioural compatibility between mates is fundamental for maintaining species boundaries and is achieved through appropriate communication between males and females. A breakdown in communication will lead to behavioural divergence and reduced interfertility. In this review, we summarise the current knowledge on male signals and female perception of these signals, integrating the literature from several taxa. We advocate that signaller–perceiver coevolution, which is usually under strong stabilising selection to enable mating, forms the basis of species-specific mate recognition systems. The mechanisms (phylogeny, geography, ecology, biology) shaping signaller–perceiver systems are briefly discussed to demonstrate the factors underpinning the evolution of signaller–perceiver couplings. Since divergence and diversification of communication systems is driven by changes in the mechanical properties of sensory pathways and morphology of sensory organs, we highlight signal modalities (auditory, olfactory, visual, tactile) and their importance in communication, particularly in mate selection. Next, using available examples and generating a stylised model, we suggest how disruption (biological, ecological, stochastic) of signaller–perceiver systems drives behavioural divergence and consequently results in reduced interfertility and speciation. Future studies should adopt an integrative approach, combining multiple parameters (phylogeny, adaptive utility of communication systems, genetics and biomechanical/biochemical properties of signals and perception) to explore how disruption of signaller–perceiver systems results in behavioural divergence and reduced interfertility. Finally, we question the impact that rapid environmental change will have on disruption of communication systems, potentially interfering with signaller–perceiver couplings.     

Spatial vision in binocular and monocular common field grasshoppers (Chorthippus brunneus)

Abstract The ability of the common field grasshopper Chorthippus brunneus to discriminate between different distances under binocular and monocular stimulus conditions is investigated based upon the peering‐jump behaviour. The results show that information obtained from only one eye is sufficient for the grasshopper to determine the jump direction and distance. However, information obtained from both eyes is advantageous for relative distance determination. It is hypothesized that the motion parallax signals from the left and right eye may be summed, thus improving performance. There is no behavioural evidence of a more complex correlation of the information from the two eyes.     

Tooth impact rate in the song of a shorthorned grasshopper: A parameter carrying specific behavioral information

Summary Receptive females of the gomphocerine grasshopperOmocestus viridulus L. were offered different artificial grasshopper songs in a one- or two-channel test situation. In the computer generated songs the tooth-impact-rate and the amplitude functions of the chirp were varied.The results of the one-channel experiments showed that the grasshoppers preferred signals with normal tooth-impact-rate to signals with half the rate. The amplitude function seems to play a minor role in the recognition process, unless this parameter is changed very radically.The results of the two-channel tests were ambiguous. A third test series was developed to interpret these results. It was found that female grasshoppers once excited by an acceptable signal afterwards responded to former unacceptable signals. Accordingly, if just one of the two signals is able to excite the female, the female may subsequently choose randomly between the signals. If the signals are of different sound levels, the louder is preferred.The shorthorned grasshopper may interpret the tooth-impact-rate as a frequency. It is proposed that the grasshopper may use the four sense cell groups of the ear as a simple sort of a spectral analyzer. These cells are tuned to different frequencies and/or differently tuned.The running Root Mean Square value of a grasshopper signal, its dependence on the applied integration time and its possible relation to perceived energy are reported in an appendix.     

Coding of a sexually dimorphic song feature by auditory interneurons of grasshoppers: the role of leading inhibition

The shape of stimulus onset is a distinct feature of many acoustic communication signals. In some grasshopper species the steepness of amplitude rise of the pulses which comprise the song subunits is sexually dimorphic and a major criterion of sex recognition. Here, we describe potential mechanisms by which auditory interneurons could transmit the information on onset steepness from the metathoracic ganglion to the brain of the grasshopper. Since no single interneuron unequivocally encoded onset steepness, it appears that this information has to reside in the relative spike counts or the relative spike timing of a small group of ascending auditory interneurons. The decisive component of this mechanism seems to be the steepness-dependent leading inhibition displayed by two interneurons (AN3, AN4). The inhibition increased with increasing onset steepness, thus delayed the excitatory response, and in one interneuron even strongly reduced the spike count. Other ascending interneurons, whose responses were little affected by onset steepness, could serve as reference neurons (AN6, AN12). Thus, our results suggest that a comparison of both, spike count and first-spike timing within a small set of ascending interneurons could yield the information on signal onset steepness, that is on the sex of the sender.     

Effect of sound signals on spontaneous activity in grasshopper interneurons (Orthoptera,Tettigonidae)

According to one of hypotheses proposed for explaining mechanisms of sound signal recognition in insects, their CNS contains a group of rhythmically active neurons that function as a reference standard for comparison with perceived acoustic information. To check this hypothesis, the spontaneous neuronal activity and its changes in perception of conspecific and heterospecific signals (CS and HS) were analyzed in the CNS of two sympatric grasshopper species Tettigonia cantans and Metrioptera roeselii. The activity of individual neurons was assayed in fixed and freely moving insects. The results of the experiment have shown that in the thoracic part of the CNS there is a group of rhythmically active neurons that do not directly respond to sound signal but readjust their impulses under effect of its action. On presentation of CS the following reactions were observed: attenuation or enhancement of impulses; stabilization or destabilization of rhythm; regular increase or decrease in interspike intervals; phasic readjustments leading to synchronization of impulses with sound stimuli (pulses). No similar alterations were usually produced by HS; still, if they did appear, they were less pronounced or of opposite direction. These data indicate that the grasshopper auditory system affects markedly the rhythmically active neurons, their reaction depending considerably on temporal organization of sound signals. Selectivity of these reactions allows us to suggest that the rhythmically active neurons are directly related to the neuronal networks providing the sound signal recognition.Translated from Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, Vol. 40, No. 6, 2004, pp. 531–538.Original Russian Text Copyright © 2004 by Zhantiev, Korsunovskaya, Chukanov.To the 100-Anniversary of A. K. VoskresenskayaThis revised version was published online in April 2005 with a corrected cover date.     

Effects of signal duration on the recognition of masked communication signals by the grasshopper Chorthippus biguttulus

The detection and recognition of acoustic communication signals masked by noise was investigated in a grasshopper (Chorthippus biguttulus) whose auditory system exhibits only poor spectral resolution and therefore has to operate in the time domain. The signals of this species consist of numerous identical subunits that enable the receiver, in principle, to make repetitive measurements. We aimed at determining the maximum integration time in this species by using stimuli of different durations under increasing noise levels. As a criterion for recognition the typical phonotactic turning response of the males was evaluated, which is reliably triggered by a female song, and thus is a sensitive indicator for recognition of conspecific signals. When confronted with a long signal (1000 ms) males tolerated a 2.4 dB higher noise level as compared to a short signal (250 ms). Noise tolerance improved with increasing signal duration from 250 ms to 450 ms. Beyond this signal duration, however, no further improvement was observed, indicating an upper limit for temporal integration that corresponds to only five song subunits. The gain in noise tolerance had a slope of 2.7 dB per doubling duration, which corresponds to the expectation derived from an energy detector model (3 dB per doubling duration) rather than to the value expected from signal detection theory (1.5 dB per doubling duration).     

Influence of amplitude modulated noise on the recognition of communication signals in the grasshopper Chorthippus biguttulus

The detection of acoustic communication signals in the presence of sinusoidally amplitude modulated noise was investigated in males of the grasshopper Chorthippus biguttulus. The auditory system of grasshoppers exhibits only poor spectral resolution. Hence, these animals are ideally suited to investigate noise tolerance in a system operating in the temporal domain. As a sensitive indicator for signal recognition the conspicuous phonotactic turning responses of males were recorded. The main result was that noise modulated at low frequencies (1.5-5 Hz) did not impair recognition compared to a unmodulated noise. With long stimuli even a moderate improvement of noise tolerance was observed, an effect that can probably be attributed to the existence of long troughs at low modulation frequencies during which the masking of the signal was reduced. Higher modulation frequencies (15-150 Hz), however, rendered detection and recognition increasingly difficult, due to a strong interference of the sound pulses of the masking noise with the syllable-pause structure of the species-specific signals. There are no indications for the operation of mechanisms analogous to comodulation masking release as found in vertebrates, nor for a spatial release from masking.     

Influence of different envelope maskers on signal recognition and neuronal representation in the auditory system of a grasshopper

Background

Animals that communicate by sound face the problem that the signals arriving at the receiver often are degraded and masked by noise. Frequency filters in the receiver''s auditory system may improve the signal-to-noise ratio (SNR) by excluding parts of the spectrum which are not occupied by the species-specific signals. This solution, however, is hardly amenable to species that produce broad band signals or have ears with broad frequency tuning. In mammals auditory filters exist that work in the temporal domain of amplitude modulations (AM). Do insects also use this type of filtering?

Principal Findings

Combining behavioural and neurophysiological experiments we investigated whether AM filters may improve the recognition of masked communication signals in grasshoppers. The AM pattern of the sound, its envelope, is crucial for signal recognition in these animals. We degraded the species-specific song by adding random fluctuations to its envelope. Six noise bands were used that differed in their overlap with the spectral content of the song envelope. If AM filters contribute to reduced masking, signal recognition should depend on the degree of overlap between the song envelope spectrum and the noise spectra. Contrary to this prediction, the resistance against signal degradation was the same for five of six masker bands. Most remarkably, the band with the strongest frequency overlap to the natural song envelope (0–100 Hz) impaired acceptance of degraded signals the least. To assess the noise filter capacities of single auditory neurons, the changes of spike trains as a function of the masking level were assessed. Increasing levels of signal degradation in different frequency bands led to similar changes in the spike trains in most neurones.

Conclusions

There is no indication that auditory neurones of grasshoppers are specialized to improve the SNR with respect to the pattern of amplitude modulations.     

Candidate neural locus for sex differences in reproductive decisions

Sexual selection and signal detection theories predict that females should be selective in their responses to mating signals in mate choice, while the response of males to signals in male competition should be less selective. The neural processes underlying this behavioural sex difference remain obscure. Differences in behavioural selectivity could result from differences in how sensitive sensory systems are to mating signals, distinct thresholds in motor areas regulating behaviour, or sex differences in selectivity at a gateway relaying sensory information to motor systems. We tested these hypotheses in frogs using the expression of egr-1 to quantify the neural responses of each sex to mating signals. We found that egr-1 expression in a midbrain auditory region was elevated in males in response to both conspecific and heterospecific calls, whereas in females, egr-1 induction occurred only in response to conspecific signals. This differential neural selectivity mirrored the sex differences in behavioural responsiveness to these stimuli. By contrast, egr-1 expression in lower brainstem auditory centres was not different in males and females. Our results support a model in which sex differences in behavioural selectivity arise from sex differences in the neural selectivity in midbrain areas relaying sensory information to the forebrain.     

Exploring the hidden landscape of female preferences for complex signals

A major challenge in evolutionary biology is explaining the origins of complex phenotypic diversity. In animal communication, complex signals may evolve from simpler signals because novel signal elements exploit preexisting biases in receivers’ sensory systems. Investigating the shape of female preference functions for novel signal characteristics is a powerful, but underutilized, method to describe the adaptive landscape potentially guiding complex signal evolution. We measured female preference functions for characteristics of acoustic appendages added to male calling songs in the grasshopper Chorthippus biguttulus, which naturally produces only simple songs. We discovered both hidden preferences for and biases against novel complex songs, and identified rules governing song attractiveness based on multiple characteristics of both the base song and appendage. The appendage's temporal position and duration were especially important: long appendages preceding the song often made songs less attractive, while following appendages were neutral or weakly attractive. Appendages had stronger effects on songs of shorter duration, but did not restore the attractiveness of very unattractive songs. We conclude that sensory biases favor, within predictable limits, the evolution of complex songs in grasshoppers. The function‐valued approach is an important tool in determining the generality of these limits in other taxa and signaling modalities.     

Acoustic pattern recognition in a grasshopper: processing in the time or frequency domain?

Males of the grasshopper Chorthippus biguttulus produce songs which consist of the stereotyped and rhythmic iteration of a sound unit (termed syllable) separated by distinct syllable pauses. Virgin females respond to this signal, and to similar artificial signals, with song phrases of their own. In behavioural experiments the response probability of virgin females can be measured with artificial acoustic stimuli. The stimuli consisted of an amplitude modulated noise the envelope of which was altered. We investigated several hypotheses on the mechanisms of conspecific song recognition with special emphasis on the question whether recognition occurs in the frequency domain or in the time domain. (1) Females of Ch. biguttulus required only the first five Fourier components of the envelope function (corresponding to 50 Hz for a fundamental frequency of 10 Hz) to detect the syllable/pause structure. In addition, they detected small gaps within syllables if the signal contained at least ca. 15 Fourier components (corresponding to a frequency of 150 Hz). Further experiments showed that the correct phase information of the Fourier components is necessary for recognition, indicating that pattern recognition is not achieved merely on the basis of band pass filtering. (2) A cross correlation between the signal and an assumed internal template yields only inconsistent predictions of the response probabilities. (3) The recognizer system probably works in the time domain, possibly by direct comparison of adjacent syllable and pause durations. It is not yet clear whether the duration of a syllable is evaluated with respect to the preceding or succeeding pause. We emphasize that the neural recognizer of the grasshopper does not only examine a signal for its similarity to an internal template, but that it also takes into account features that indicate an incorrect signal. This may be a general feature of neuronal pattern recognition systems which have been shaped by natural selection. Received: 4 October 1997 / Accepted in revised form: 26 August 1998     

Phylogenetic distribution of a male pheromone that may exploit a nonsexual preference in lampreys

Pheromones are among the most important sexual signals used by organisms throughout the animal kingdom. However, few are identified in vertebrates, leaving the evolutionary mechanisms underlying vertebrate pheromones poorly understood. Pre‐existing biases in receivers' perceptual systems shape visual and auditory signalling systems, but studies on how receiver biases influence the evolution of pheromone communication remain sparse. The lamprey Petromyzon marinus uses a relatively well‐understood suite of pheromones and offers a unique opportunity to study the evolution of vertebrate pheromone communication. Previous studies indicate that male signalling with the mating pheromone 3‐keto petromyzonol sulphate (3kPZS) may exploit a nonsexual attraction to juvenile‐released 3kPZS that guides migration into productive rearing habitat. Here, we infer the distribution of male signalling with 3kPZS using a phylogenetic comparison comprising six of 10 genera and two of three families. Our results indicate that only P. marinus and Ichthyomyzon castaneus release 3kPZS at high rates. Olfactory and behavioural assays with P. marinus, I. castaneus and a subset of three other species that do not use 3kPZS as a sexual signal indicate that male signalling might have driven the evolution of female adaptations to detect 3kPZS with specific olfactory mechanisms and respond to 3kPZS with targeted attraction relevant during mate search. We postulate that 3kPZS communication evolved independently in I. castaneus and P. marinus, but cannot eliminate the alternative that other species lost 3kPZS communication. Regardless, our results represent a rare macroevolutionary investigation of a vertebrate pheromone and provide insight into the evolutionary mechanisms underlying pheromone communication.     

A test of the matched filter hypothesis in two sympatric frogs,Chiromantis doriae and Feihyla vittata

The matched filter hypothesis proposes that the auditory sensitivity of receivers should match the spectral energy distribution of the senders’ signals. If so, receivers should be able to distinguish between species-specific and hetero-specific signals. We tested the matched filter hypothesis in two sympatric species, Chiromantis doriae and Feihyla vittata, whose calls exhibit similar frequency characters and that overlap in the breeding season and microenvironment. For both species, we recorded male calls and measured the auditory sensitivity of both sexes using the auditory brainstem response (ABR). We compared the auditory sensitivity with the spectral energy distribution of the calls of each species and found that (1) auditory sensitivity matched the signal spectrogram in C. doriae and F. vittata; (2) the concordance conformed better to the conspecific signal versus the hetero-specific signal. In addition, our results show that species differences are larger than sex differences for ABR audiograms.     

Prey change behaviour with predation threat, but demographic effects vary with prey density: experiments with grasshoppers and birds

Increasingly, ecologists emphasize that prey frequently change behaviour in the presence of predators and these behavioural changes can reduce prey survival and reproduction as much or more than predation itself. However, the effects of behavioural changes on survival and reproduction may vary with prey density due to intraspecific competition. In field experiments, we varied grasshopper density and threat of avian predation and measured grasshopper behaviour, survival and reproduction. Grasshopper behaviour changed with the threat of predation and these behavioural changes were invariant with grasshopper density. Behavioural changes with the threat of predation decreased per capita reproduction over all grasshopper densities; whereas the behavioural changes increased survival at low grasshopper densities and then decreased survival at high densities. At low grasshopper densities, the total reproductive output of the grasshopper population remained unchanged with predation threat, but declined at higher densities. The effects of behavioural changes with predation threat varied with grasshopper density because of a trade-off between survival and reproduction as intraspecific competition increased with density. Therefore, resource availability may need to be considered when assessing how prey behavioural changes with predation threat affect population and food web dynamics.     

Effects of large herbivore grazing on grasshopper behaviour and abundance in a meadow steppe

1. Adaptive phenotypic plasticity has been a major subject in evolutionary ecology, but how a species' behaviour may respond to certain environmental change is still not clear. In grasslands worldwide, large herbivores are increasingly used as a tool for grazing management, and occur to interact with grasshoppers that dominate grassland insect communities. Previous studies have been well-documented about grazing effects on diversity and abundance of grasshoppers. Yet, how grazing may alter grasshopper behaviour, and potential effects on their abundance remains elusive. 2. We conducted a field experiment by manipulating grazing using sheep, cattle, and their mix to examine the behavioural responses and abundance of the grasshoppers (Euchorthippus unicolor) to grazing in a Leymus chinensis-dominated grassland. 3. Results showed that the grasshoppers spent less time on feeding and resting on grasses, but more time on switching and resting on forbs under cattle grazing and mixed grazing with cattle and sheep. In contrast, the grasshoppers spent more time on feeding but less time on switching and resting on forbs under sheep grazing. The behavioural changes were also potentially linked to grasshopper abundance in the context of grazing management. 4. The responses of grasshopper behaviour and abundance to grazing may be largely triggered by altered vegetation and microclimates. Such behavioural flexibility of grasshoppers must be considered when large herbivores are recognised as a management tool for influencing grasshopper abundance, and grazer species should be paid more attention both individually and jointly for better grassland conservation.     

Singing Activity Reveals Personality Traits in Great Tits

In animal communication, sexually selected signals have been shown to often signal individual attributes such as motivation or quality. Birdsong is among the best studied signalling systems, and song traits vary substantially among individuals. The question remains if variation in signalling also reflects more general and consistent individual characteristics. Such consistent individual differences in behaviour that are relatively stable over time and contexts are referred to as personality or behavioural syndromes. Here, we studied the relation between singing and explorative behaviour, a well‐studied personality trait, using great tits (Parus major) under standardized aviary conditions. The results show that singing activity measured as the number of songs sung in spring prior to breeding correlated with male but not with female explorative behaviour. In contrast, song repertoire was not related to explorative behaviour but varied over the day. The link between explorative and singing behaviour suggests that sexually selected signals are more than signals of quality but can also reflect other intrinsic behavioural characteristics such as personality traits.