ArticlePublisher preview available
To read the full-text of this research, you can request a copy directly from the authors.

Abstract and Figures

Acoustic signalling is widespread in arthropods and appears to be common in spiders, but the function is still unknown in many species. Acoustic signals have several functions and can be used both in interspecific (e.g., to threaten potential predators) and intraspecific (during courtship) communication. In our study, we investigated the intraspecific role of stridulation in the araneophagous Palpimanus spider (Araneae: Palpimanidae). These spiders are specialised in hunting other spiders at all ontogenetic stages. We hypothesised that stridulation is used to avoid cannibalism. We investigated the morphology of the stridulatory apparatus, analysed the acoustic signals that various stages produce, and found two types of stridulation, low- and high-intensity stridulation. Then, we investigated the presence of cannibalism between individuals of variable body size and the use of stridulation during interactions. We found that cannibalism occurred only when the prosoma size difference between the two opponents was more than 200%. Then, we paired conspecific large control Palpimanus with smaller control individual or with individual whose stridulatory organs were impaired and found that impaired spiders suffered significantly higher cannibalism than the control spiders. Our study reveals a novel role of acoustic communication in the conspecific recognition of araneophagous spiders. Significance statement Cannibalism is widespread among predatory animals. However, cannibalism might not be an optimal strategy for several reasons and should be a less preferred option for predators. Palpimanus spiders are prey specialised predators preying primarily on other spiders thus the risk of cannibalism is even higher than in generalist predators. These spiders possess stridulatory apparatus and they often stridulate following a contact with conspecifics. We found that cannibalism occasionally occurred during contact with conspecifics and that the probability of cannibalism increased with the size difference between the interacting individuals. When the spiders were not able to stridulate during contact, the probability of cannibalism increased significantly. Our results thus show that Palpimanus spiders use stridulation to reduce cannibalism among unequally sized individuals.
This content is subject to copyright. Terms and conditions apply.
ORIGINAL ARTICLE
Stridulation can suppress cannibalism in a specialised
araneophagous predator
Eva Líznarová
1
&Lenka Sentenská
1
&František Šťáhlavský
2
&Stano Pekár
1
Received: 31 January 2018 /Revised: 20 June 2018 /Accepted: 29 June 2018 /Published online: 10 July 2018
#Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Acoustic signalling is widespread in arthropods and appears to be common in spiders, but the function is still unknown in many
species. Acoustic signals have several functions and can be used both in interspecific (e.g., to threaten potential predators) and
intraspecific (during courtship) communication. In our study, we investigated the intraspecific role of stridulation in the
araneophagous Palpimanus spider (Araneae: Palpimanidae). These spiders are specialised in hunting other spiders at all onto-
genetic stages. We hypothesised that stridulation is used to avoid cannibalism. We investigatedthe morphology of the stridulatory
apparatus, analysed the acoustic signals that various stages produce, and found two types of stridulation, low- and high-intensity
stridulation. Then, we investigated the presence of cannibalism between individuals of variable body size and the use of
stridulation during interactions. We found that cannibalism occurred only when the prosoma size difference between the two
opponents was more than 200%. Then, we paired conspecific large control Palpimanus with smaller control individual or with
individual whose stridulatory organs were impaired and found that impaired spiders suffered significantly higher cannibalism
than the control spiders. Our study reveals a novel role of acoustic communication in the conspecific recognition of
araneophagous spiders.
Significance statement
Cannibalism is widespread among predatory animals. However, cannibalism might not be an optimal strategy for several reasons
and should be a less preferred option for predators. Palpimanus spiders are prey specialised predators preying primarily on other
spiders thus the risk of cannibalism is even higher than in generalist predators. These spiders possess stridulatory apparatus and
they often stridulate following a contact with conspecifics. We found that cannibalism occasionally occurred during contact with
conspecifics and that the probability of cannibalism increased with the size difference between the interacting individuals. When
the spiders were not able to stridulate during contact, the probability of cannibalism increased significantly. Our results thus show
that Palpimanus spiders use stridulation to reduce cannibalism among unequally sized individuals.
Keywords Acoustic signal .Araneophagy .Defence .Intraspecific interaction .Predation .Spider
Introduction
Animals communicate via visual, chemical, tactile, vibratory,
and acoustic signals. Acoustic communication is widespread
and diverse not only among vertebrates but in arthropods too
(Alexander 1967); yet, the biological significance of sounds in
arthropods is often elusive (Lazzari et al. 2006; Wessel 2006).
Acoustic signals are employed in interspecific interactions,
e.g. to deter potential enemies (Alexander 1960;Masters
1979;UetzandStratton1982;Marshalletal.1995;Lazzari
et al. 2006), to locate prey (e.g. Jones 2005; Surlykke and
Kalko 2008), or in intraspecific communication, particularly
during courtship and copulation (Gwynne and Dadour 1985;
Maddison and Stratton 1988;UhlandSchmitt1996).
Communicated by J. Pruitt
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00265-018-2541-3) contains supplementary
material, which is available to authorized users.
*Eva Líznaro
liznarovaeva@centrum.cz
1
Department of Botany and Zoology, Faculty of Science, Masaryk
University, Kotlářská 2, 611 37 Brno, Czech Republic
2
Department of Zoology, Faculty of Sciences, Charles University,
Vin ičná 7, Praha 128 43, Czech Republic
Behavioral Ecology and Sociobiology (2018) 72: 127
https://doi.org/10.1007/s00265-018-2541-3
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Palpimanus also possesses very potent venom, which is especially effective on spiders (Michálek et al., 2019a;Pekár et al., 2018a). In addition, stridulation produced by the chelicera-palp apparatus is used to reduce intraspecific predation on small individuals (Líznarová et al., 2018). Unfortunately, for other palpimanids, no such data are available. ...
... Detection of cannibalism by gut content DNA analysis is impossible if it occurs among specimens of the same haplotype but here we found different haplotypes. The very high frequency in Palpimanus spp., however, was very much surprising, because palpimanids were found to avoid cannibalism by means of stridulation (Líznarová et al., 2018). In laboratory trials, the cannibalism frequency amounted to only about 20%, and was only observed when the body size ratio was more than two, i.e. adult specimens preyed on small juveniles. ...
Article
Spiders are among the most diversified and abundant predators in terrestrial ecosystems across the world, but information on their prey is limited. Particularly, there is paucity of data for prey-specialised species, such as palpimanid spiders. Here we investigated the trophic strategy of four palpimanid species (Diaphorocellus biplagiatus, Otiothops birabeni, Palpimanus gibbulus, and P. potteri) representing all three subfamilies (Chediminae, Otiothopinae, Palpimaninae) and three geographic areas (Mediterranean, South America, South Africa) in order to infer a trophic strategy for the entire family Palpimanidae. We predicted that all palpimanids are specialised araneophagous predators. We used molecular gut-content analysis, combined with comparative analysis of morphological trophic traits. We found all four species to catch spiders more than insects. All species captured spiders belonging to several families, but predominantly those of the cursorial guild. The diet composition did not differ between sexes and juveniles. The breadth of trophic niche was narrow for all species, suggesting stenophagy. Using comparative analysis of morphological traits (thick cuticle, stout forelegs, scopulae on forelegs, and stridulatory apparatus) and araneophagy, we estimated that preying on spiders combined with the morphological traits is ancestral state for the entire family. We suggest that the whole family Palpimanidae includes araneophagous species.
... Nevertheless, 6 th stadium adults of both sexes seem to be typical among Palpimanus. Citing unpublished data, Líznarová et al. (2018) reported that Palpimanus have a lifespan of up to three years which agrees with observations made on female P. uncatus during this study. For male P. uncatus, evidence suggested a potential two-year lifespan. ...
... Spiders use different mechanisms to defend themselves against predators and intruders, or to lower the probability of encountering them. Some examples include: fleeing at speeds as high as approximately two metres per second (Jäger 2014), diving (Swierk et al. 2022), gliding (Crews et al. 2020a), aposematism, displaying defence postures and biting (Foelix 2011), autotomy (Formanowicz 1990), stridulation (Líznarová et al. 2018), death-feigning, camouflaging (Théry & Casas 2002), mimicry (Shamble et al. 2017), constructing cryptic burrows sometimes bearing antipredatory decorations or additional escape routes (Williams et al. 2006), and rubbing off urticating setae (Kaderka et al. 2019) ( Figures 6A-F). Almost all spiders have a solitary and territorial lifestyle; a few groups, however, display different forms of sociality, ranging from a temporary aggregation of webs to dozens of individuals living in family-group territories within a communal nest, and cooperating in prey capture, feeding, brood care and web maintenance (Avilés & Guevara 2017) (Figure 7). ...
Thesis
Full-text available
Spiders (Araneae) are the largest order of Arachnida and the sixth most speciose order of Animalia, comprising more than 50,000 extant species as well as over 1,400 species known from fossils. Despite this immense diversity that has been estimated to comprise 120,000–200,000 species, our knowledge of their systematics and distribution remains rather incipient. While attempts to evaluate the diversity and distribution patterns of spiders have been made for the Neotropical and a few other faunas, most other regions remain historically neglected. The aim of this dissertation is to explore the systematics, diversity and distribution of spiders of Iran, a highly interesting region from a zoological and biogeographical point of view that unfortunately has been poorly investigated regarding its invertebrate fauna. For this purpose, I examined more than 9,000 specimens that were either collected during expeditions to numerous regions and ecosystems across the country or deposited in several natural history collections from around the world. As a result of these efforts, which were initiated in 2013 and mostly carried out in collaboration with researchers from various countries, a total of 11 genera and 147 species of Iranian spiders were described as new to science, and 419 taxa (i.e., 13 families, 87 genera and 319 species) were recorded in Iran for the first time. The total number of newly described and recorded species (i.e., 466 species) constitutes almost half (i.e., 49.83%) of the currently known Iranian species diversity of this group (i.e., 935 species). Amongst 147 species described, 137 are known only from Iran, representing 63.72% of all species currently considered endemic to this country (i.e., 215 species). These results were published in a total of 87 publications, 38 of which were published after the beginning of my doctoral studies at UTU in 2019. This dissertation, however, is primarily based on only nine taxonomic articles (i.e., I–IX), all published after 2019 and highlighting some of the more important findings. Because of the newly obtained taxonomic information and an extensive database of all published records, it was possible to conduct a comprehensive review of spatial variation in the diversity patterns of spiders in Iran. This was the main objective of publication X, which also included an evaluation of the effect of sampling bias on the current understanding of the distribution of Iranian spiders. The analyses showed that the diversity of Iranian spiders remains inadequately studied and is heavily affected by the Linnean shortfall (i.e., gaps in taxonomic knowledge), despite a remarkable improvement in taxonomic research on this fauna since the beginning of the 21st century. There are 935 spider species in the 1,648,195 km2 of Iran. Comparing the number of species per area of 171 countries and other political regions indicated that Iran was in position 132, whereas many considerably smaller and less ecologically diverse countries were in lower positions. It was also found that this fauna clearly suffers from a severe Wallacean shortfall (i.e., lack of knowledge of species distributions), as approximately 85% of Iran lacks a single record of spiders. There is a highly uneven distribution of records throughout the country and its provinces and ecoregions, with most of the records situated near large cities. A high correlation was found between the number of records of spiders and the number of records of plants and other animals in Iran, indicating that the noted shortfalls are indeed corroborated by other taxa. Finally, it is suggested that to gain a more complete picture of the diversity of Iranian spiders, future collecting efforts should be primarily in the form of extensive systematic surveys instead of opportunistic sampling, and ideally targeting lesser sampled areas and ecoregions. Once a satisfactory amount of information regarding the taxonomy and distribution of species becomes available, it will be possible to properly assess the conservation status and risk factors that affect these species and to identify areas of higher conservation and management priority.
... Additionally, these components can be detected individually or in concert (Keuper & Kühne, 1983) and by different sensory structures (Hill & Shadley, 1997). The function of stridulation can also be quite varied, as it is known to play a role in courtship (crickets: Alexander, 1962;homopterans: Roces & Manrique, 1995;jumping spiders: Elias, Hebets, Hoy, & Mason, 2005; Schizocosa wolf spiders: Hebets et al., 2013;Rundus, Santer, & Hebets, 2010), agonistic contests (crickets: Alexander, 1961;Brown, Smith, Moskalisk, & Gabriel, 2006;crabs: Chen et al., 2014), coordination of social behavior (leaf-cutter ants: Masters et al., 1983, Roces et al., 1993treehoppers: Cocroft, 1999), foraging (leaf-cutter ants: Tautz et al., 1995), and even cannibalism suppression (spiders: Líznarova, Sentenska, Štáhlavsky, & Pekár, 2018). ...
Article
The observable diversity of antipredator defences across organisms demonstrates predation's impact on trait evolution. The functions of many traits that are presumed to have an antipredator function have never been directly tested. The spiny orb-weaving spider, Micrathena gracilis, for example, stridulates when grasped. While stridulation was first hypothesized to be an antipredator defence nearly 50 years ago, no data exist to support this hypothesis. To explore the form and function of M. gracilis stridulation, we first quantified the behavioural and acoustical properties of sound production. Next, using laboratory assays, we directly tested the effect of stridulation on survival with an avian predator – blue jays, Cyanocitta cristata. Finally, we conducted a large mark–recapture field study in which we compared the natural survival of experimentally manipulated adult female M. gracilis that could not stridulate (silenced) versus could stridulate (control). Stridulatory pulses produced broadband frequency spectra, consistent with acoustic antipredator defences in other taxa. We also observed stridulation by male M. gracilis for the first time. In staged laboratory interactions with captive blue jays, we found no differences in survival between silenced and control M. gracilis. Similarly, in our mark–recapture field study, we found no differences in survival estimates between silenced and control groups, nor an effect of stridulation rate. While M. gracilis stridulation closely resembles antipredator stridulation in other arthropods, our behavioural data do not yet provide solid support for an antipredator function in M. gracilis.
... Aggressiveness decreased in both cave and stream larvae, and in both newborn and older larvae. Such a reduction of aggressiveness led by predator occurrence may result in a waning or even a complete suppression of cannibalism in risky habitats (Kishida et al. 2011;Líznarová et al. 2018). As cannibalism plays a key role in many aquatic ecosystems (Rudolf 2008;Wissinger et al. 2010;Takatsu and Kishida 2015;Takatsu et al. 2017), its suppression may impact the survival and life-history of individuals (Kishida et al. 2011), with potential broad consequences on population dynamics (Claessen et al. 2004;Rudolf 2008). ...
Article
Full-text available
Intraspecific aggressiveness can be affected by multiple environmental pressures. In several cases, aggressiveness can grade into full-scale cannibalism, particularly when resources are scarce. However, limited information exists on how intraspecific aggressiveness varies among populations experiencing different environmental pressures, and on the role intraspecific predation plays for the exploitation of harsh habitats. The fire salamander, Salamandra salamandra, is an excellent model species to study factors affecting intraspecific aggressiveness, because of its ability to breed in habitats with contrasting food resources and predation pressure. Here, we evaluated the influence of predation risk and habitat of origin on aggressive interactions. To this extent, we reared larvae from cave (scarce resources; nearly-absent predators) and surface (abundant resources and predators) populations under different risk conditions and measured aggressive behavior towards conspecifics. During behavioral trials, larvae were exposed to different combinations of predator and wounded conspecific chemical cues. Intraspecific aggressiveness increased in large and late-development larvae. Larvae from all the populations significantly reduced aggressiveness under both typologies of risk experienced during rearing (constant presence of predator; pulses of high predation risk), and also when stimulated by predator cues. However, larvae from cave populations exhibited a more pronounced aggressiveness, especially when exposed to wounded conspecific cues. Intraspecific aggressiveness can be modulated by the complex interaction between multiple variables, and both behavioral plasticity and local adaptations can determine its variation across populations. Our findings reveal that aggressive interactions are favored in cave environment, suggesting intraspecific predation can play a key role in the exploitation of resource-depleted habitats. Significance statement In this study, we investigated how intraspecific aggressiveness of salamander larvae is shaped under predation risk in populations originating from contrasting environments, such as cave and surface habitats. Larvae experiencing predator presence during their development or exposed to predator cues significantly reduced their aggressive interactions, both in cave and surface populations. Interestingly, cave-originating individuals reacted to wounded conspecific cues by increasing the frequency of their aggressive displays, suggesting cannibalistic behavior is locally enhanced in populations from resource-depleted habitats. The present study offers new insights on the importance of intraspecific aggressiveness for the adaptation to harsh environments.
Article
Full-text available
Acoustic and substrate-borne vibrations are among themost 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 andmorphological 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.
Article
The importance of vision-reliant defensive traits (e.g. warning colours) in mimicry studies is well established, but their effectiveness is limited by visibility. In low light conditions, for instance, acoustic or tactile channels may be more effective. The juvenile and adult stages of the nocturnal hunting Palpimanus spiders audibly stridulate when harassed. Given this we hypothesized that the sound produced by Palpimanus has a defensive role against interspecific predators. Palpimanus though are poorly defended especially against something as large as a gecko. Hence we hypothesized that the stridulation is effective because the spider mimics co-occurring mutillid wasps. We staged predator feeding experiments in which mutillid wasps, sham-operated Palpimanus, silenced Palpimanus and a nonstridulating spider were offered to Eusparassus spiders and geckoes. Stridulating spiders had significantly greater survival against both predators than the nonstridulating treatments and comparable survival to the mutillid wasps. This result represents the first confirmed case of a spider using stridulation against an interspecific predator. Stridulation deterred Eusparasus spiders, while in geckoes stridulation acted postcapture as they dropped the prey instead of attempting to swallow them. For mutillid wasps this dropping response was typically more rapid than with Palpimanus but attempts to swallow silenced individuals were more frequent than sham-operated individuals, which were more likely to be dropped before any attempt to swallow. Analyses of stridulation characteristics of Palpimanus showed they were similar to acoustic signals of four of the co-occurring mutillid wasps and far more so than distress signals of control insects. Our study overall supports the notion that Palpimanus spiders are Batesian mimics of sympatrically occurring mutillids through the use of an aposematic acoustic signal and not just an example of a startle response.
Article
Full-text available
Within behavioural research, non-normally distributed data with a complicated structure are common. For instance, data can represent repeated observations of quantities on the same individual. The regression analysis of such data is complicated both by the interdependency of the observations (response variables) and by their non-normal distribution. Over the last decade, such data have been more and more frequently analysed using generalized mixed-effect models. Some researchers invoke the heavy machinery of mixed-effect modelling to obtain the desired population-level (marginal) inference, which can be achieved by using simpler tools—namely by marginal models. This paper highlights marginal modelling (using generalized estimating equations [GEE]) as an alternative method. In various situations, GEE can be based on fewer assumptions and directly generate estimates (population-level parameters) which are of immediate interest to the behavioural researcher (such as population means). Using four examples from behavioural research, we demonstrate the use, advantages, and limits of the GEE approach as implemented within the functions of the ‘geepack’ package in R.
Article
Full-text available
Behavioural research often produces data that have a complicated structure. For instance, data can represent repeated observations of the same individual and suffer from heteroscedasticity as well as other technical snags. The regression analysis of such data is often complicated by the fact that the observations (response variables) are mutually correlated. The correlation structure can be quite complex and might or might not be of direct interest to the user. In any case, one needs to take correlations into account (e.g. by means of random-effect specification) in order to arrive at correct statistical inference (e.g. for construction of the appropriate test or confidence intervals). Over the last decade, such data have been more and more frequently analysed using repeated-measures ANOVA and mixed-effects models. Some researchers invoke the heavy machinery of mixed-effects modelling to obtain the desired population-level (marginal) inference, which can be achieved by using simpler tools – namely marginal models. This paper highlights marginal modelling (using generalized least squares [GLS] regression) as an alternative method. In various concrete situations, such marginal models can be based on fewer assumptions and directly generate estimates (population-level parameters) which are of immediate interest to the behavioural researcher (such as population mean). Sometimes, they might be not only easier to interpret but also easier to specify than their competitors (e.g. mixed-effects models). Using five examples from behavioural research, we demonstrate the use, advantages, limits and pitfalls of marginal and mixed-effects models implemented within the functions of the ‘nlme’ package in R.
Article
Any elementary textbook of physics will give the basic facts of sound as a longitudinal wave motion transmitted through a medium and emanating from a source of mechanical vibration. The problem is that, when it comes to describing and analysing insect sounds and their use in communication, it is almost impossible to avoid problems of anthropomorphism. This is, of course, a difficulty in all studies on animal behaviour. Sound is defined in dictionaries as a “sensation caused in the ear by vibrations of the surrounding air” (The Concise Oxford Dictionary of Current English, 6th edition, 1976). Following this definition, the term sound can only be used of vibrations which are heard by the human ear and transmitted through the surrounding air. If this were followed, sound would be a useless concept for describing animal behaviour. The human ear is sensitive to a range of vibrations with frequencies from about 30 Hz to 15 kHz. The terms “ultrasound” and “ultrasonic”, though useful, are anthropomorphic and refer to vibrations having frequencies above those detectable by the unaided human ear. A wide variety of animals, including many insects (e.g. many bushcrickets, cicadas, etc.), have ranges of acoustic sensitivity which extend well above that of the human ear and ultrasound is critical in the lives of many animals (Sales and Pye, 1974). Clearly such a limited definition of sound is not useful in the scientific study of animal behaviour.