Barrett A. Klein

Faux frogs: multimodal signalling and the value of robotics in animal behaviour

A long-standing interest in animal behaviour has been to understand chains of stimulus—response. One approach to understanding the links between stimulus and response has been to use models (animal replicas) in which details of a behaviour can be manipulated to determine how such manipulations influence the response of the focal animal. Static models (Tinbergen & Perdeck 1950; Searcy 1998; McLister 2003), manually controlled robots (Brown & Kiely 1974; Taylor et al. 2007) and motorized static models (MacLaren et al. 2004; Gumm et al. 2006) have been effective in eliciting responses from animals in behavioural studies. The current availability, however, of low-cost electric motors, easily designed circuit boards and a wide variety of sculpting materials has created even greater possibilities for developing robots as tools in studies of animal behaviour. In recent years a number of workers have capitalized on these technologies which are now increasingly being employed in controlled experiments (Knight 2005). In some research programmes, robots have been developed as a physical algorithm to test hypotheses about the mechanisms of behaviour (reviewed in: Webb 2000). In these studies, biological systems are modelled with robots and the behaviour of the robots is analysed in response to some stimulus input. Examples of these include studies of navigation (Lambrinos et al.

Multimodal signal variation in space and time: how important is matching a signal with its signaler?

SUMMARY Multimodal signals (acoustic+visual) are known to be used by many anuran amphibians during courtship displays. The relative degree to which each signal component influences female mate choice, however, remains poorly understood. In this study we used a robotic frog with an inflating vocal sac and acoustic playbacks to document responses of female túngara frogs to unimodal signal components (acoustic and visual). We then tested female responses to a synchronous multimodal signal. Finally, we tested the influence of spatial and temporal variation between signal components for female attraction. Females failed to approach the isolated visual cue of the robotic frog and they showed a significant preference for the call over the spatially separate robotic frog. When presented with a call that was temporally synchronous with the vocal sac inflation of the robotic frog, females did not show a significant preference for this over the call alone; when presented with a call that was temporally asynchronous with vocal sac inflation of the robotic frog, females discriminated strongly against the asynchronous multimodal signal in favor of the call alone. Our data suggest that although the visual cue is neither necessary nor sufficient for attraction, it can strongly modulate mate choice if females perceive a temporal disjunction relative to the primary acoustic signal.

Sleep deprivation impairs precision of waggle dance signaling in honey bees

Sleep is essential for basic survival, and insufficient sleep leads to a variety of dysfunctions. In humans, one of the most profound consequences of sleep deprivation is imprecise or irrational communication, demonstrated by degradation in signaling as well as in receiving information. Communication in nonhuman animals may suffer analogous degradation of precision, perhaps with especially damaging consequences for social animals. However, society-specific consequences of sleep loss have rarely been explored, and no function of sleep has been ascribed to a truly social (eusocial) organism in the context of its society. Here we show that sleep-deprived honey bees (Apis mellifera) exhibit reduced precision when signaling direction information to food sources in their waggle dances. The deterioration of the honey bees ability to communicate is expected to reduce the foraging efficiency of nestmates. This study demonstrates the impact of sleep deprivation on signaling in a eusocial animal. If the deterioration of signals made by sleep-deprived honey bees and humans is generalizable, then imprecise communication may be one detrimental effect of sleep loss shared by social organisms.

Quantifying the symbiont contribution to essential amino acids in aphids: the importance of tryptophan for Uroleucon ambrosiae

A complete amino acid budget was constructed using the aphid Uroleucon ambrosiae (Strecker), feeding on a suboptimal host, Tithonia fruticosa. The availability of amino acids was estimated from phloem analyses and phloem intake rates at each stage of development. Requirements for amino acids were estimated from gravimetric studies and from analyses of body amino acids. Because the budget was found to be well balanced, estimates of specific needs and shortfalls of essential amino acids were calculated, thus quantifying the role of symbiotic bacteria in fulfilling needs for these amino acids. The most dramatic shortfall was for tryptophan, consistent with the amplification of relevant genes in the symbiont.

Robots in the service of animal behavior.

As reading fiction can challenge us to better understand fact, using fake animals can sometimes serve as our best solution to understanding the behavior of real animals. The use of dummies, doppelgangers, fakes, and physical models have served to elicit behaviors in animal experiments since the early history of behavior studies, and, more recently, robotic animals have been employed by researchers to further coax behaviors from their study subjects. Here, we review the use of robots in the service of animal behavior, and describe in detail the production and use of one type of robot – “faux” frogs – to test female responses to multisensory courtship signals. The túngara frog (Physalaemus pustulosus) has been a study subject for investigating multimodal signaling, and we discuss the benefits and drawbacks of using the faux frogs we have designed, with the larger aim of inspiring other scientists to consider the appropriate application of physical models and robots in their research.

MALE RESIDENCY AND MATING PATTERNS IN A SUBSOCIAL SPIDER

Abstract Male mating strategies are often deployed with regard to female maturity and receptivity, possibly in response to sperm utilization patterns on the part of the female. We examined the pattern of male residency with females during the mating period of the subsocial spider Anelosimus cf. jucundus (Araneae, Theridiidae). We first examined patterns of male cohabitation with naturally occurring penultimate instar and adult females in the field. Males were significantly more likely to be found in association with adult females, rather than with penultimate instar females. Penultimate instar and virgin adult females of known age were then placed into the field and monitored for residency by subsequently marked males. Males were, again, significantly more likely to be found in association with adult females, rather than with penultimate-instar females, although we were unable to determine if this pattern was due to differential arrival or to differential retention of males at adult female web sites. Aspects of A. cf. jucundus natural history, including duration of male residency and frequency of mating in the field, are provided for the first time. We discuss the patterns of male residency in relation to predictions based on sperm utilization patterns by female A. cf. jucundus spiders.

Mapping sleeping bees within their nest: spatial and temporal analysis of worker honey bee sleep.

Patterns of behavior within societies have long been visualized and interpreted using maps. Mapping the occurrence of sleep across individuals within a society could offer clues as to functional aspects of sleep. In spite of this, a detailed spatial analysis of sleep has never been conducted on an invertebrate society. We introduce the concept of mapping sleep across an insect society, and provide an empirical example, mapping sleep patterns within colonies of European honey bees (Apis mellifera L.). Honey bees face variables such as temperature and position of resources within their colonys nest that may impact their sleep. We mapped sleep behavior and temperature of worker bees and produced maps of their nests comb contents as the colony grew and contents changed. By following marked bees, we discovered that individuals slept in many locations, but bees of different worker castes slept in different areas of the nest relative to position of the brood and surrounding temperature. Older worker bees generally slept outside cells, closer to the perimeter of the nest, in colder regions, and away from uncapped brood. Younger worker bees generally slept inside cells and closer to the center of the nest, and spent more time asleep than awake when surrounded by uncapped brood. The average surface temperature of sleeping foragers was lower than the surface temperature of their surroundings, offering a possible indicator of sleep for this caste. We propose mechanisms that could generate caste-dependent sleep patterns and discuss functional significance of these patterns.

The Curious Connection Between Insects and Dreams

A majority of humans spend their waking hours surrounded by insects, so it should be no surprise that insects also appear in humans’ dreams as we sleep. Dreaming about insects has a peculiar history, marked by our desire to explain a dream’s significance and by the tactic of evoking emotions by injecting insects in dream-related works of art, film, music, and literature. I surveyed a scattered literature for examples of insects in dreams, first from the practices of dream interpretation, psychiatry, and scientific study, then from fictional writings and popular culture, and finally in the etymology of entomology by highlighting insects with dream-inspired Latinate names. A wealth of insects in dreams, as documented clinically and culturally, attests to the perceived relevance of dreams and to the ubiquity of insects in our lives.

Perceived Synchrony of Frog Multimodal Signal Components Is Influenced by Content and Order

Multimodal signaling is common in communication systems. Depending on the species, individual signal components may be produced synchronously as a result of physiological constraint (fixed) or each component may be produced independently (fluid) in time. For animals that rely on fixed signals, a basic prediction is that asynchrony between the components should degrade the perception of signal salience, reducing receiver response. Male túngara frogs, Physalaemus pustulosus, produce a fixed multisensory courtship signal by vocalizing with two call components (whines and chucks) and inflating a vocal sac (visual component). Using a robotic frog, we tested female responses to variation in the temporal arrangement between acoustic and visual components. When the visual component lagged a complex call (whine + chuck), females largely rejected this asynchronous multisensory signal in favor of the complex call absent the visual cue. When the chuck component was removed from one call, but the robofrog inflation lagged the complex call, females responded strongly to the asynchronous multimodal signal. When the chuck component was removed from both calls, females reversed preference and responded positively to the asynchronous multisensory signal. When the visual component preceded the call, females responded as often to the multimodal signal as to the call alone. These data show that asynchrony of a normally fixed signal does reduce receiver responsiveness. The magnitude and overall response, however, depend on specific temporal interactions between the acoustic and visual components. The sensitivity of túngara frogs to lagging visual cues, but not leading ones, and the influence of acoustic signal content on the perception of visual asynchrony is similar to those reported in human psychophysics literature. Virtually all acoustically communicating animals must conduct auditory scene analyses and identify the source of signals. Our data suggest that some basic audiovisual neural integration processes may be at work in the vertebrate brain.

Sleep and the gut microbiome: antibiotic-induced depletion of the gut microbiota reduces nocturnal sleep in mice

Several bacterial cell wall components such as peptidoglycan and muramyl peptide are potent inducers of mammalian slow-wave sleep when exogenously administered to freely behaving animals. It has been proposed that the native gut microflora may serve as a quasi-endogenous pool of somnogenic bacterial cell wall products given their quantity and close proximity to the intestinal portal. This proposal suggests that deliberate manipulation of the hosts intestinal flora may elicit changes in host sleep behavior. To test this possibility, we evaluated 24 h of sleep-wake behavior after depleting the gut microbiota with a 14 d broad-spectrum antibiotic regimen containing high doses of ampicillin, metronidazole, neomycin, and vancomycin. High-throughput sequencing of the bacterial 16S rDNA gene was used to confirm depletion of fecal bacteria and sleep-wake vigilance states were determined using videosomnography techniques based on previously established behavioral criteria shown to highly correlate with standard polysomnography-based methods. Additionally, considering that germ-free and antibiotic-treated mice have been earlier shown to display increased locomotor activity, and since locomotor activity has been used as a reliable proxy of sleep, we suspected that the elevated locomotor activity previously reported in these animals may reflect an unreported reduction in sleep behavior. To examine this potential relationship, we also quantified locomotor activity on a representative subsample of the same 24 h of video recordings using the automated video-tracking software ANY-maze. We found that antibiotic-induced depletion of the gut microbiota reduced nocturnal sleep, but not diurnal sleep. Likewise, antibiotic-treated mice showed increased nocturnal locomotor activity, but not diurnal locomotor activity. Taken together, these results support a link between the gut microbiome and nocturnal sleep and locomotor physiology in adult mice. Additionally, our findings indicate that antibiotics may be insomnogenic via their ability to diminish gut-derived bacterial somnogens. Given that antibiotics are among the most commonly prescribed drugs in human medicine, these findings have important implications for clinical practice with respect to prolonged antibiotic therapy, insomnia, and other idiopathic sleep-wake and circadian-rhythm disorders affecting an estimated 50-70 million people in the United States alone. Highlights - 14 d broad-spectrum antibiotic treatment effectively depletes the gut microbiota. - Gut microbiota depletion reduces nocturnal sleep, but not diurnal sleep. - Gut microbiota depletion increases nocturnal locomotion, but not diurnal locomotion. - Antibiotics may be insomnogenic: implications for idiopathic sleep disorders.