Behavioural responses to video playbacks by zebra finch males

A major problem for communication research is to provide standardized stimuli and to disentangle the relative contribution of different sensory channels to the compound signal and its effectiveness. Video techniques have frequently been used for this purpose. Fifty Hertz cathode ray tube (CRT) screens cannot be used for birds because their flicker frequency is lower than the time resolution of at least songbirds. Thin film transistor (TFT) screens have successfully been used to present video clips of behaving conspecifics. We show here that they are indeed transmitting video images in a way that enables zebra finches to react appropriately to live video images of conspecifics and that the test birds are able to detect small differences in the behaviour of the stimulus animals. Adding acoustic information strongly enhanced the reaction to the video clips.     

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.     

Convergent evolution of eye ultrastructure and divergent evolution of vision-mediated predatory behaviour in jumping spiders

All jumping spiders have unique, complex eyes with exceptional spatial acuity and some of the most elaborate vision-guided predatory strategies ever documented for any animal of their size. However, it is only recently that phylogenetic techniques have been used to reconstruct the relationships and key evolutionary events within the Salticidae. Here, we used data for 35 species and six genes (4.8 kb) for reconstructing the phylogenetic relationships between Spartaeinae, Lyssomaninae and Salticoida. We document a remarkable case of morphological convergence of eye ultrastructure in two clades with divergent predatory behaviour. We, furthermore, find evidence for a stepwise, gradual evolution of a complex predatory strategy. Divergent predatory behaviour ranges from cursorial hunting to building prey-catching webs and araneophagy with web invasion and aggressive mimicry. Web invasion and aggressive mimicry evolved once from an ancestral spartaeine that was already araneophagic and had no difficulty entering webs due to glue immunity. Web invasion and aggressive mimicry was lost once, in Paracyrba, which has replaced one highly specialized predation strategy with another (hunting mosquitoes). In contrast to the evolution of divergent behaviour, eyes with similarly high spatial acuity and ultrastructural design evolved convergently in the Salticoida and in Portia.     

Orchestrating the score: complex multimodal courtship in the Habronattus coecatus group of Habronattus jumping spiders (Araneae: Salticidae)

Jumping spiders in the genus Habronattus use complex multimodal signals during courtship displays. In the present study, we describe multimodal displays from the Habronattus coecatus clade, comprising a diverse group of 23 described species. Habronattus coecatus group displays are made up of sex‐specific ornamentation and temporally coordinated combinations of motion displays and vibratory songs. Vibratory songs are complex, consisting of up to 20 elements organized in functional groupings (motifs) that change as courtship progresses. This temporal structuring of displays is analogous to a musical composition. Vibratory elements are associated with movement displays involving coloured and patterned ornaments on the male body. We describe general patterns of multimodal displays for 11 species including one, Habronattus borealis, which appears to have lost complex display behaviour. Habronattus coecatus group courtship is one of the most complex communication systems yet described in arthropods and this group may reveal important factors driving the evolution of complex signals. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 522–547.     

Extreme ultraviolet sexual dimorphism in jumping spiders (Araneae: Salticidae)

Jumping spiders (Salticidae) have acute vision with some cells in the retina that are sensitive to ultraviolet (UV) spectra (< 400 nm). However, no study has documented the use of UV signals in salticids. To appreciate the function of UV vision, it is necessary to characterize the UV colours of salticids. In the present study, the UV and human-visible wavelengths of a tropical ornate salticid spider, Cosmophasis umbratica , were analysed using reflectance spectrometry to obtain evidence of sex-specific UV colours. An absolute sexual dimorphism in the UV colours of this salticid species was found. All of the body parts of adult males that are displayed to conspecifics during intra-specific interactions reflected UV (300–400 nm) light, whereas the adult females and juveniles did not reflect UV light from any body part. A great deal of variation was also found in the UV wavebands among males. This is the first full UV characterization of a salticid spider and the first study to demonstrate an extreme sexual UV dimorphism in jumping spiders. The findings obtained provide evidence that UV reflectance may comprise important sexual signals in jumping spiders.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 397–406.     

Widespread reliance on olfactory sex and species identification by lyssomanine and spartaeine jumping spiders

Jumping spiders (Salticidae) are renowned for their exceptional vision, but this does not preclude use of other senses. Here we provide evidence that olfactory pheromones are widespread in the Spartaeinae and Lyssomaninae, two subfamilies regarded as basal clades within the Salticidae. Pheromone use by salticids was tested in a series of experiments: males were tested with the odour of conspecific females, heterospecific females, and conspecific males, and females were tested with the odour of conspecific males. With seven of the 29 species tested, we also tested males using the draglines of conspecific females (spider absent) as the odour source. Males of all species tested were attracted to the odour of conspecific females and to the odour of the draglines of conspecific females. There was no evidence of males responding to the odour of heterospecific females or conspecific males, or of females responding to the odour of conspecific males. These findings suggest that it is primarily males that respond to olfactory sex pheromones, consistent with the apparent trend within spiders of males more actively searching for females and females placing greater emphasis on mate‐choice decisions. Compared with most salticid groups, lyssomanines and spartaeines are unusually sedentary and this lifestyle may favour olfactory mate searching. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 664–677.     

Eavesdropping and signal matching in visual courtship displays of spiders

Eavesdropping on communication is widespread among animals, e.g. bystanders observing male-male contests, female mate choice copying and predator detection of prey cues. Some animals also exhibit signal matching, e.g. overlapping of competitors' acoustic signals in aggressive interactions. Fewer studies have examined male eavesdropping on conspecific courtship, although males could increase mating success by attending to others' behaviour and displaying whenever courtship is detected. In this study, we show that field-experienced male Schizocosa ocreata wolf spiders exhibit eavesdropping and signal matching when exposed to video playback of courting male conspecifics. Male spiders had longer bouts of interaction with a courting male stimulus, and more bouts of courtship signalling during and after the presence of a male on the video screen. Rates of courtship (leg tapping) displayed by individual focal males were correlated with the rates of the video exemplar to which they were exposed. These findings suggest male wolf spiders might gain information by eavesdropping on conspecific courtship and adjust performance to match that of rivals. This represents a novel finding, as these behaviours have previously been seen primarily among vertebrates.     

Molecular diagnostics reveal spiders that exploit prey vibrational signals used in sexual communication

Vibrational signalling is a widespread form of animal communication and, in the form of sexual communication, has been generally regarded as inherently short‐range and a private communication channel, free from eavesdropping by generalist predators. A combination of fieldwork and laboratory experiments was used to test the hypothesis that predators can intercept and exploit such signals. First, we developed and characterized PCR primers specific for leafhoppers of the genus Aphrodes and specifically for the species Aphrodes makarovi. Spiders were collected from sites where leafhoppers were present and screened with these primers to establish which spider species were significant predators of this species during the mating period of these leafhoppers. Analysis using PCR of the gut contents of tangle‐web spiders, Enoplognatha ovata (Theridiidae), showed that they consume leafhoppers in the field at a greater rate when signalling adults were present than when nymphs were dominant, suggesting that the spiders were using these vibrations signals to find their prey. Playback and microcosm experiments then showed that E. ovata can use the vibrational signals of male leafhoppers as a cue during foraging and, as a result, killed significantly more male than female A. makarovi. Our results show, for the first time, that arthropod predators can exploit prey vibrational communication to obtain information about prey availability and use this information to locate and capture prey. This may be a widespread mechanism for prey location, one that is likely to be a major unrecognized driver of evolution in both predators and prey.     

Multisensory signals trigger approach behaviour in the fire-bellied toad Bombina orientalis: sex differences and call specificity

Animal communication often involves multimodal signals, and interactions between sensory modalities can trigger unique responses in receivers. Response to social signals was investigated in fire-bellied toads by exposing them to playback of male calls (advertisement and release calls) and a video clip of a male conspecific in the laboratory. The cues were presented in isolation and as a combined bimodal stimulus, and approach frequency, latency to approach and time spent around the stimulus source were measured. No positive phonotaxis was observed toward the advertisement call, both during the day and during a phonotaxis trial performed at night. However, females, but not males, approached with greater frequency, lower latency, and spent more time near the source of the bimodal stimulus in an experiment involving the advertisement call. Female response was specific to the advertisement call, as approach was not increased when the release call was used. Males, on the other hand, did not show increased approach in the advertisement call experiment, but approached with greater frequency the bimodal stimulus involving the release call within the first minute of stimulus presentation. The findings suggest that females orient toward calling males and that males eavesdrop on release calls, but in both cases a visual stimulus is also needed to trigger a response. Social approach in Bombina orientalis is thus dependent on multisensory cues, and the nature of the interaction between sensory modalities depends on receiver sex and call type.     

Social electric signals in freely moving dyads of <Emphasis Type="Italic">Brachyhypopomus pinnicaudatus</Emphasis>

Brachyhypopomus pinnicaudatus (pulse-type weakly electric fish) is a gregarious species that displays reproductive behavior and agonistic encounters between males only during the breeding season. During social interactions, in addition to its basal electric organ discharge (EOD), fish emit social electric signals (SESs) in the contexts of reproduction and intrasexual aggression. We reproduced natural behavior in laboratory settings: SESs recorded in the field are indistinguishable from those observed in our experimental setup. SESs are nocturnal, change seasonally and exhibit sexual dimorphism. This study provides an exhaustive characterization and classification of SESs produced by males and females during the breeding season. In male–female dyads, males produce accelerations and chirps while females interrupt their EODs. The same SESs are observed in male–male dyads. We present a novel, thorough classification of male chirps into four independent types (A, B, C, and M) based on their duration and internal structure. The type M chirp is only observed in male–male dyads. Chirps and interruptions, both in male–female and male–male dyads, are emitted in bouts, which are also grouped throughout the night. Our data suggest the existence of a sophisticated electric dialog during reproductive and aggressive interaction whose precise timing and behavioral significance are being investigated.     

Comparative biology of Portia africana,P. albimana,P. fimbriata,P. labiata,and P. shultzi,araneophagic, web-building jumping spiders (Araneae: Salticidae): Utilisation of webs,predatory versatility,and intraspecific interactions

Abstract

Portia is a behaviourally complex and aberrant salticid genus. The genus is of unusual importance because it is morphologically primitive. Five species were studied in nature (Australia, Kenya, Malaysia, Sri Lanka) and in the laboratory in an effort to clarify the origins of the salticids and of their unique, complex eyes. All the species of Portia studied were both web builders and cursorial. Portia was also an araneophagic web invader, and it was a highly effective predator on diverse types of alien webs. Portia was an aggressive mimic, using a complex repertoire of vibratory behaviour to deceive the host spiders on which it fed. The venom of Portia was unusually potent to other spiders; its easily autotomised legs may have helped Portia escape if attacked by its frequently dangerous prey. Portia was also kleptoparasitic and oophagic when occupying alien webs. P. fimbriata from Queensland, where cursorial salticids were superabundant, used a unique manner of stalking and capturing other salticids. The display repertoires used during intraspecific interactions were complex and varied between species. Both visual (typical of other salticids) and vibratory (typical of other web spiders) displays were used. Portia copulated both on and away from webs and frequently with the female hanging from a dragline. Males cohabited with subadult females on webs, mating after the female matured. Adult and subadult females sometimes used specialised predatory attacks against courting or mating males. Sperm induction in Portia was similar to that in other cursorial spiders. Portia mimicked detritus in shape and colour, and its slow, mechanical locomotion preserved concealment. Portia occasionally used a special defensive behaviour (wild leaping) if disturbed by a potential predator. Two types of webs were spun by all species (Type 1, small resting platforms; Type 2, large prey-capture webs). Two types of egg sacs were made, both of which were highly aberrant for a salticid. Responses of different species and both sexes of Portia were quantitatively compared for different types of prey. Many of the trends in behaviour within the genus, including quantitative differences in predatory behaviour, seemed to be related to differences in the effectiveness of the cryptic morphology of Portia in concealing the spider in its natural habitat (‘effective crypsis’). The results of the study supported, in general, Jackson & Blest’s (1982a) hypothesis of salticid evolution which, in part, proposes that salticid ancestors were web builders with poorly developed vision and that acute vision evolved in conjunction with the ancestral spiders becoming proficient as araneophagic invaders of diverse types of webs.     

Conditional strategies and interpopulation variation in the behaviour of jumping spiders

Abstract

Conditional strategies and interpopulation variation in the mating and predatory behaviour of salticid spiders are reviewed. A functional approach is adopted, and defended, in which specified behavioural phenotypes are accounted for, in large part, by specified selection factors. Courtship versatility, in which a male's behaviour depends on the female's maturity and location, is common in the Salticidae. If a male encounters an adult female in the open, where there is ample ambient light, he performs vision-dependent displays (Type 1 courtship) in front of her. If he encounters an adult female inside her nest, he uses different displays (Type 2 courtship) which are not vision–dependent and consist of various tugging, probing and jerking movements on the silk of the nest. These displays apparently send vibratory stimuli to the female. When a male encounters a subadult female inside her nest, he initially performs Type 2 courtship, then spins a second chamber on the nest and cohabits until the female moults and matures. A modification of optimal foraging theory has been used to examine factors that influence interpopulation variation in male courtship persistence. A study of five populations corroborated predictions from the model. Persistence appears to be related to female availability. Female availability is related to local phenology, which is, in turn, related to local climate. Complex examples of predatory versatility also have evolved in the Salticidae, especially in the genus Portia. All species of Portia studied are araneophagic spiders that invade other spiders' webs and practise aggressive mimicry. Portia fimbriata, uniquely among Portia species studied, uses specialised behaviour to prey on other salticids. Portia fimbriata and one of the salticids on which it preys, Euryattus sp., appear to be co-adapted to each other.     

Horse signals: The sounds and scents of fury

Summary During contests animals typically exchange information about fighting ability. Among feral horses these signals involve olfactory or acoustical elements and each type can effectively terminate contests before physical contact becomes necessary. Dung transplant experiments show that for stallions, irrespective of rank, olfactory signals such as dung sniffing encode information about familiarity suggesting that such signals can be used as signatures. As such they can provide indirect information about fighting ability as long as opponents associate identity with past performance. Play-back experiments, however, show that vocalizations, such as squeals, directly provide information about status regardless of stallion familiarity. Sonographs reveal that squeals of dominants are longer than those of subordinates and that only those of dominants have at their onset high-frequency components.     

Nestling colouration is adjusted to parent visual performance in altricial birds

Hitherto, most of the investigation on the perceptual efficacy of begging signals has dwelled on how patterns of nestling colouration adjust to predominant nest luminosity. However, visual sensitivity of birds varies across species, which raises the question of whether colouration of traits involved in begging displays is adjusted to parent visual capacities. Here, by comparing nestling colouration and visual sensitivity across 22 altricial bird species, we provide a first test of this hypothesis. Firstly, we assessed differences in performance of typical UV‐tuned and violet‐tuned bird eyes when looking at the nestling traits under the light regimes prevailing at their nests. Secondly, while controlling for common ancestry in a comparative approach, we explored variation in colouration of nestlings in relation to parent visual system. The colour discrimination model indicated a general higher performance of the ultraviolet over the violet eye at detecting gape and body skin traits in either open‐ or hole‐nest light conditions. Gape colouration was associated with parental visual system as the nestlings of UVS species displayed more yellow and less pure ultraviolet mouths than the nestlings of VS species. Thus, our results agree with an adaptive parent–offspring communication scenario where the nestlings’ colours tuned the perception capacities of their parents.     

Courtship behaviour in Japanese macaques during heterosexual and homosexual consortships

Female Japanese macaques (Macaca fuscata) in the Arashiyama population near Kyoto, Japan, are unusual, in that they exhibit what many would consider to be male-typical sexual characteristics. Specifically, they mount other females within the context of temporary, but exclusive, sexual relationships (i.e., homosexual consortships) and they sometimes exhibit a preference for female sexual partners, even when given the choice of a sexually motivated male alternative. In this study, we examined whether female Japanese macaques also exhibited male-typical patterns of courtship behaviour during homosexual consortships. Data were collected on courtship behaviour during heterosexual and homosexual consortships in free-ranging Japanese macaques from the Arashiyama (Japan) population. We analyzed the occurrence of 12 different courtship behaviours during 3374 heterosexual inter-mount intervals and 1412 homosexual inter-mount intervals. Sex differences between heterosexually consorting males and females existed for only two of the 12 courtship behaviours we investigated: inclined-back presentations and sexual vocalizations. Dominant and subordinate homosexually consorting females were sex-typical in their expression of inclined-back presentations and sexual vocalizations. Consequently, facultative same-sex sexual partner preference, mounting and consortships do not co-occur with male-typical patterns of courtship behaviour in female Japanese macaques.     

Lizards speed up visual displays in noisy motion habitats

Extensive research over the last few decades has revealed that many acoustically communicating animals compensate for the masking effect of background noise by changing the structure of their signals. Familiar examples include birds using acoustic properties that enhance the transmission of vocalizations in noisy habitats. Here, we show that the effects of background noise on communication signals are not limited to the acoustic modality, and that visual noise from windblown vegetation has an equally important influence on the production of dynamic visual displays. We found that two species of Puerto Rican lizard, Anolis cristatellus and A. gundlachi, increase the speed of body movements used in territorial signalling to apparently improve communication in visually 'noisy' environments of rapidly moving vegetation. This is the first evidence that animals change how they produce dynamic visual signals when communicating in noisy motion habitats. Taken together with previous work on acoustic communication, our results show that animals with very different sensory ecologies can face similar environmental constraints and adopt remarkably similar strategies to overcome these constraints.     

Relationship between male-male and male-female sexual behavior in 5-6-month-old male lambs

To characterize male–male sexual behavior during lamb development, to relate it with lamb body and testicular growth, and with sexual behavior toward estrual ewes, 40 Milchschaf male lambs, weaned at 45 days of age, were kept with ewes that were nursing younger lambs. Experimental lambs were weighed and scrotal circumference was measured every 2 weeks. Male–male sexual behavior was observed during 1–2 h every 2 weeks after birth until 7 months of age. Observations were recorded more intensively (3–4 h on five different days) for 2 weeks (5–6 months of age) as male–male sexual behavior increased during that period. Both mounting and mounted lambs were identified. An individual mounting index (MI) was calculated. To study male–female sexual behavior, lambs were individually located with two estrual ewes, and during 5 min the number of ano-genital sniffing, lateral approaches, mounts, and mounts with ejaculation were recorded. From those data, a libido index was also calculated. Male–male mounts (n = 308) were observed. Courtship behavior was displayed in 25% of interactions; mounts were accepted in 72.1% of attempted mounts. Mounts without previous courtship were accepted more frequently than mounts with previous courtship (P = 0.002). Lamb weight and scrotal circumference were not different according to MI groups. Lambs that mounted more times estrual ewes (first tertile) had greater (P = 0.04) MI (0.61 ± 0.10) than lambs with medium (0.27 ± 0.09) and less (0.30 ± 0.10) MI. The regression between MI and heterosexual libido index was r = 0.33 (P < 0.05). In summary, intensive male–male sexual activity during a short period of male lamb development was observed. There was a positive relationship between sexual behavior of male lambs towards other male lambs and towards estrual ewes.     

Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders

A long-standing goal for biologists has been to understand how female preferences operate in systems where males have evolved numerous sexually selected traits. Jumping spiders of the Maratus genus are exceptionally sexually dimorphic in appearance and signalling behaviour. Presumably, strong sexual selection by females has played an important role in the evolution of complex signals displayed by males of this group; however, this has not yet been demonstrated. In fact, despite apparent widespread examples of sexual selection in nature, empirical evidence is relatively sparse, especially for species employing multiple modalities for intersexual communication. In order to elucidate whether female preference can explain the evolution of multi-modal signalling traits, we ran a series of mating trials using Maratus volans. We used video recordings and laser vibrometry to characterize, quantify and examine which male courtship traits predict various metrics of mating success. We found evidence for strong sexual selection on males in this system, with success contingent upon a combination of visual and vibratory displays. Additionally, independently produced, yet correlated suites of multi-modal male signals are linked to other aspects of female peacock spider behaviour. Lastly, our data provide some support for both the redundant signal and multiple messages hypotheses for the evolution of multi-modal signalling.     

Male singing behaviour and female presence in the territory in whitethroats Sylvia communis

Unmated male songbirds usually change their vocal behaviour when females enter their territories. Either the males court the females by changing the rate or pattern with which their normal long-ranging full songs are emitted, or they shift to special displays and long- or short-ranging vocalisations. In this study we quantified how female presence and behaviour affect the singing behaviour of male whitethroats. In the presence of a female the male frequently performed song flights, maybe to locate the female before it was courted, with sequences of diving-song displays. The courtship was interrupted by periods of perch songs. Female dscharp calls and short movements made the males initiate or resume courtship, whereas short horizontal jumps made the males intensify their courtship. Overall, the males changed their dual-function song activity in females' presence by emitting fewer perch songs and more flight songs. The quiet diving songs were only emitted during direct courtship of a female. The song types emitted immediately before, during, and after courtship are all highly variable, thus allowing for a quick assessment of the male's song repertoire. The courtship was also interrupted by periods of male woid calling, a call that is known to have a deterring effect on rival males. Bouts of woid calls were usually followed by song flights, again probably to locate the female that might have moved out of sight, or maybe to locate potential rival intruders. The latter was supported by an increased intrusion rate during female presence. Communicated by P. McGregor