Courtship behaviour in the sandfly Lutzomyia longipalpis, the New World vector of visceral leishmaniasis

Courtship behaviour in Lutzomyia longipalpis Lutz and Neiva (Diptera: Psychodidae) was examined to determine the sequence of behaviours that occur prior to copulation. Courtship consisted of a series of male and female touching and wing-flapping behaviours, with males performing a greater variety of wing-flapping behaviours than previously described. Occurrence of male approach-flapping, semi-circling and female stationary-flapping were all predictors of eventual copulation, and may coincide with the dispersal of pheromones or the production of auditory signals important to courtship. Touching occurred in the majority of observations, with contact most often made with the tips of the legs and antennae. This behaviour, not previously described in sandflies, was initiated by males and females, and may indicate the use of contact pheromones, a form of communication previously overlooked in L. longipalpis. Future studies are required to separate the auditory and chemical signals associated with wing-flapping, and to confirm whether L. longipalpis possesses cuticular hydrocarbons capable of inducing behavioural responses. The identification of signals that inhibit sexual behaviour during courtship may be particularly relevant to developing mating disruption techniques against L. longipalpis.     

Ethology of Hygienic Behaviour in the Honey Bee Apis mellifera L. (Hymenoptera: Apidae): Behavioural repertoire of Hygienic bees

Hygienic behaviour performed by middle‐aged worker bees is an important intranidal task in colonies of the honey bee Apis mellifera (L.). It comprises detecting diseased brood in the larval and pupal stages and removing all such infected brood, thereby decreasing the incidence of infection. Hygienic behaviour consists of two task‐components: uncapping cells and removing the cell contents. The aim of this study was to observe bees performing hygienic behaviour to determine their age at performance of the behaviour and to describe their behavioural repertoire. The bees performing hygienic behaviour were middle‐aged bees, younger than foragers. In the colonies where the behaviours of individual bees were observed, all bees performing the hygienic behaviour were seen to exhibit both the components, though at different frequencies. One behavioural class performed the task of uncapping cells at higher frequencies than the task of removing cell contents, while another class performed both tasks to the same extent. While these two classes had higher frequencies of the tasks comprising the hygienic behaviour but lower frequencies of other common behaviours in their repertoire, a third class of bees included those that performed all behaviours in their repertoire at similar frequencies. There was no difference in the ages of the bees in these three behavioural classes. These results suggest that there is no evidence of task partitioning among bees performing the hygienic behaviour. The segregation observed could, however, be based on their response thresholds to the stimulus and/or on their ability to discriminate the various cues emanating from the dead brood.     

Addressing the pain associated with disbudding and dehorning in cattle

The pain caused by disbudding or dehorning of cattle and its alleviation may be assessed by behavioural, physiological and production responses. Disbudding can be carried out by cautery or the application of a chemical paste. Cautery disbudding and amputation dehorning stimulate definite pain related behaviours during and after the procedure but caustic disbudding causes little response during the procedure though it is followed by behaviours indicative of pain. All three procedures cause definite plasma cortisol responses but the response to amputation dehorning is significantly greater than the response to cautery or chemical disbudding. It has a characteristic format; a rapid increase following dehorning to a maximum concentration within 30 min, then a decline to plateau levels, followed by a return to pretreatment values at 7-8 h. Local anaesthesia administered before disbudding or dehorning eliminates pain-related behaviour and reduces the plasma cortisol response for about 1.5 h. Following amputation dehorning the plasma cortisol concentration then increases for about 6 h before returning to pretreatment levels. When local anaesthesia and a non-steroidal anti-inflammatory drug (NSAID) are given before disbudding or dehorning the cortisol responses to these procedures are virtually eliminated. Chronic pain in the days following disbudding and dehorning is poorly understood. As a general rule, if pain relief is not available, cautery disbudding is preferable to chemical disbudding or amputation dehorning. If possible, local anaesthesia and better still local anaesthesia plus a NSAID should be used to minimise the pain caused by all three procedures.     

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.     

Neural mechanisms underlying the evolvability of behaviour

The complexity of nervous systems alters the evolvability of behaviour. Complex nervous systems are phylogenetically constrained; nevertheless particular species-specific behaviours have repeatedly evolved, suggesting a predisposition towards those behaviours. Independently evolved behaviours in animals that share a common neural architecture are generally produced by homologous neural structures, homologous neural pathways and even in the case of some invertebrates, homologous identified neurons. Such parallel evolution has been documented in the chromatic sensitivity of visual systems, motor behaviours and complex social behaviours such as pair-bonding. The appearance of homoplasious behaviours produced by homologous neural substrates suggests that there might be features of these nervous systems that favoured the repeated evolution of particular behaviours. Neuromodulation may be one such feature because it allows anatomically defined neural circuitry to be re-purposed. The developmental, genetic and physiological mechanisms that contribute to nervous system complexity may also bias the evolution of behaviour, thereby affecting the evolvability of species-specific behaviour.     

Size-mediated response to public cues of predation risk in a tropical stream fish

In order to investigate any size-dependent differences between behavioural patterns, wild-caught Hart's rivulus Rivulus hartii of varying sizes were exposed to chemical alarm cues extracted from the skin of conspecifics or heterospecific Poecilia reticulata, or a tank water control, in a series of laboratory trials. In response to conspecific alarm cues, R. hartii subjects of the range of body sizes tested exhibited consistent, size-independent antipredator behaviours that were characterized by decreased locomotory activity and foraging levels and increased refuging behaviour. Conversely, focal R. hartii demonstrated significant size-dependent trends in response to heterospecific alarm cues, with smaller individuals exhibiting antipredator responses and larger individuals shifting their behaviour to increased levels of activity consistent with a foraging, or predatory, response. These results show that the behavioural responses of individual R. hartii to publicly available chemical alarm cues from heterospecifics are mediated by the size of the receiver.     

Colour‐based foraging diverges after multiple generations under different light environments

When the environment changes, sensory systems can adapt plastically or evolve genetically to the new surroundings, and traits and behaviours reliant on these sensory systems may also change, leading to altered evolutionary trajectories. We tested for differences in colour‐based foraging preferences of guppies (Poecilia reticulata) that lived for 6–10 generations under each of three light environments (green, lilac or control) to determine whether evolution under different light environments alters visually based behaviour. When tested in a common light environment, we found differences in pecking behaviour between treatments that were likely due to changes in the visual system. Pecking behaviour towards green stimuli was consistent across light treatments, possibly reflecting the importance of detecting green algae in the wild. The blue stimulus was only pecked at by fish from the control environments. Behaviour towards long wavelength stimuli varied, possibly due to the polymorphic nature of the long wavelength opsins. These results are consistent with one component of sensory drive but do not allow us to conclude whether these differences are due to plastic or evolved responses.     

The genomic basis of vomeronasal-mediated behaviour

The vomeronasal organ (VNO) is a chemosensory subsystem found in the nose of most mammals. It is principally tasked with detecting pheromones and other chemical signals that initiate innate behavioural responses. The VNO expresses subfamilies of vomeronasal receptors (VRs) in a cell-specific manner: each sensory neuron expresses just one or two receptors and silences all the other receptor genes. VR genes vary greatly in number within mammalian genomes, from no functional genes in some primates to many hundreds in rodents. They bind semiochemicals, some of which are also encoded in gene families that are coexpanded in species with correspondingly large VR repertoires. Protein and peptide cues that activate the VNO tend to be expressed in exocrine tissues in sexually dimorphic, and sometimes individually variable, patterns. Few chemical ligand–VR–behaviour relationships have been fully elucidated to date, largely due to technical difficulties in working with large, homologous gene families with high sequence identity. However, analysis of mouse lines with mutations in genes involved in ligand–VR signal transduction has revealed that the VNO mediates a range of social behaviours, including male–male and maternal aggression, sexual attraction, lordosis, and selective pregnancy termination, as well as interspecific responses such as avoidance and defensive behaviours. The unusual logic of VR expression now offers an opportunity to map the specific neural circuits that drive these behaviours.     

In search of higher energy: metabolism-dependent behaviour in bacteria

Bacteria use different strategies to navigate to niches where environmental factors are favourable for growth. Chemotaxis is a behavioural response mediated by specific receptors that sense the concentration of chemicals in the environment. Recently, a new type of sensor has been described in Escherichia coli that responds to changes in cellular energy (redox) levels. This sensor, Aer, guides the bacteria to environments that support maximal energy levels in the cells. A variety of stimuli, such as oxygen, alternative electron acceptors, light, redox carriers that interact with the electron transport system and metabolized carbon sources, effect changes in the cellular energy (redox) levels. These changes are detected by Aer and by the serine chemotaxis receptor Tsr and are transduced into signals that elicit appropriate behavioural responses. Diverse environmental signals from Aer and chemotaxis receptors converge and integrate at the level of the CheA histidine kinase. Energy sensing is widespread in bacteria, and it is now evident that a variety of signal transduction strategies are used for the metabolism-dependent behaviours. The occurrence of putative energy-sensing domains in proteins from cells ranging from Archaea to humans indicates the importance of this function for all living systems.     

Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole antipredator defences

Temporal variation in predation risk may be an important determinant of prey antipredator behaviours. According to the risk allocation hypothesis, the strongest antipredator behaviours are expected when periods of high risk are short and infrequent. We tested this prediction in a laboratory experiment where common frog Rana temporaria tadpoles were raised form early larval stages until metamorphosis. We manipulated the time a predatory Aeshna dragonfly larva was present and recorded behavioural responses (activity) of the tadpoles at three different time points during the tadpoles' development. We also investigated how tadpole shape, size and age at metamorphosis were affected by temporal variation in predation risk. We found that during the two first time points activity was always lowest in the constant high-risk situation. However, antipredator response in the two treatments with brief high-risk situation increased as tadpoles developed, and by the third time point, when the tadpoles were close to metamorphosis, activity was as low as in the constant high-risk situation. Exposure to chemical cues of a predation event tended to reduce activity during the first time period, but caused no response later on. Induced morphological changes (deeper tail and shorter relative body length) were graded the response being stronger as the time spent in the proximity of predator increased. Tadpoles in the brief risk and chemical cue treatments showed intermediate responses. Modification of life history was only found in the constant high-risk treatment in which tadpoles had longer larval period and larger metamorphic size. Our results indicate that both behavioural and morphological defences were sensitive to temporal variation in predation risk, but behaviour did not respond in the manner predicted by the risk allocation model. We discuss the roles of concentration of predator chemical cues and prey stage-dependency in determining these responses.     

Plant behaviour and communication

Plant behaviours are defined as rapid morphological or physiological responses to events, relative to the lifetime of an individual. Since Darwin, biologists have been aware that plants behave but it has been an underappreciated phenomenon. The best studied plant behaviours involve foraging for light, nutrients, and water by placing organs where they can most efficiently harvest these resources. Plants also adjust many reproductive and defensive traits in response to environmental heterogeneity in space and time. Many plant behaviours rely on iterative active meristems that allow plants to rapidly transform into many different forms. Because of this modular construction, many plant responses are localized although the degree of integration within whole plants is not well understood. Plant behaviours have been characterized as simpler than those of animals. Recent findings challenge this notion by revealing high levels of sophistication previously thought to be within the sole domain of animal behaviour. Plants anticipate future conditions by accurately perceiving and responding to reliable environmental cues. Plants exhibit memory, altering their behaviours depending upon their previous experiences or the experiences of their parents. Plants communicate with other plants, herbivores and mutualists. They emit cues that cause predictable reactions in other organisms and respond to such cues themselves. Plants exhibit many of the same behaviours as animals even though they lack central nervous systems. Both plants and animals have faced spatially and temporally heterogeneous environments and both have evolved plastic response systems.     

The joy of sex pheromones

Sex pheromones provide an important means of communication to unite individuals for successful reproduction. Although sex pheromones are highly diverse across animals, these signals fulfil common fundamental roles in enabling identification of a mating partner of the opposite sex, the appropriate species and of optimal fecundity. In this review, we synthesize both classic and recent investigations on sex pheromones in a range of species, spanning nematode worms, insects and mammals. These studies reveal comparable strategies in how these chemical signals are produced, detected and processed in the brain to regulate sexual behaviours. Elucidation of sex pheromone communication mechanisms both defines outstanding models to understand the molecular and neuronal basis of chemosensory behaviours, and reveals how similar evolutionary selection pressures yield convergent solutions in distinct animal nervous systems.EMBO reports advance online publication 13 September 2013; doi:10.1038/embor.2013.140     

Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles

Antipredator behaviour is an important factor influencing survival probability of prey animals, and it may evolve rapidly as a response to changes in predator regime. I studied antipredator behaviour of common frog ( Rana temporaria ) tadpoles from three populations that differ in predator regimes. In the first experiment, tadpoles obtained from four natural matings in each population were subjected to chemical cues from either European perch ( Perca fluviatilis ) or from larvae of the dragonfly Aeshna juncea . Tadpoles decreased their activity in response to both predators, but the spatial behaviour of tadpoles differed between the two predator treatments. In general, there were no differences in behaviours among the populations, but in three out of four studied behaviours there were differences between parentages within the populations suggesting that these behaviours may be genetically determined. The lack of a significant Predator×Population interaction suggests no differences in plastic antipredator behaviour among the populations, while the lack of significant Predator×Parentage interaction suggests no genetic variance within the populations for plastic antipredator behaviour. In the second experiment, tadpoles from the three populations were exposed to predation by a free-ranging A. juncea . In line with the first experiment, there were no differences in survival rate between the populations. R. temporaria tadpoles seem to rely heavily on plastic antipredator behaviour as their main response to predator chemical cues. There was very little indication of local behavioural differentiation and the possible reasons for the lack of divergence among populations are discussed.     

Orchid pollination by sexual deception: pollinator perspectives

The extraordinary taxonomic and morphological diversity of orchids is accompanied by a remarkable range of pollinators and pollination systems. Sexually deceptive orchids are adapted to attract specific male insects that are fooled into attempting to mate with orchid flowers and inadvertently acting as pollinators. This review summarises current knowledge, explores new hypotheses in the literature, and introduces some new approaches to understanding sexual deception from the perspective of the duped pollinator. Four main topics are addressed: (1) global patterns in sexual deception, (2) pollinator identities, mating systems and behaviours, (3) pollinator perception of orchid deceptive signals, and (4) the evolutionary implications of pollinator responses to orchid deception, including potential costs imposed on pollinators by orchids. A global list of known and putative sexually deceptive orchids and their pollinators is provided and methods for incorporating pollinator perspectives into sexual deception research are provided and reviewed. At present, almost all known sexually deceptive orchid taxa are from Australia or Europe. A few sexually deceptive species and genera are reported for New Zealand and South Africa. In Central and Southern America, Asia, and the Pacific many more species are likely to be identified in the future. Despite the great diversity of sexually deceptive orchid genera in Australia, pollination rates reported in the literature are similar between Australian and European species. The typical pollinator of a sexually deceptive orchid is a male insect of a species that is polygynous, monandrous, haplodiploid, and solitary rather than social. Insect behaviours involved in the pollination of sexually deceptive orchids include pre‐copulatory gripping of flowers, brief entrapment, mating, and very rarely, ejaculation. Pollinator behaviour varies within and among pollinator species. Deception involving orchid mimicry of insect scent signals is becoming well understood for some species, but visual and tactile signals such as colour, shape, and texture remain neglected. Experimental manipulations that test for function, multi‐signal interactions, and pollinator perception of these signals are required. Furthermore, other forms of deception such as exploitation of pollinator sensory biases or mating preferences merit more comprehensive investigation. Application of molecular techniques adapted from model plants and animals is likely to deliver new insights into orchid signalling, and pollinator perception and behaviour. There is little current evidence that sexual deception drives any species‐level selection on pollinators. Pollinators do learn to avoid deceptive orchids and their locations, but this is not necessarily a response specific to orchids. Even in systems where evidence suggests that orchids do interfere with pollinator mating opportunities, considerable further research is required to determine whether this is sufficient to impose selection on pollinators or generate antagonistic coevolution or an arms race between orchids and their pollinators. Botanists, taxonomists and chemical ecologists have made remarkable progress in the study of deceptive orchid pollination. Further complementary investigations from entomology and behavioural ecology perspectives should prove fascinating and engender a more complete understanding of the evolution and maintenance of such enigmatic plant‐animal interactions.     

Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans

The pintado (Pseudoplatystoma coruscans) is a ferocious carnivorous catfish with evident cannibalistic behaviour; its nocturnal habits are related to its ability to use predominately chemical sensorial modalities. This study investigated whether the pintado distinguishes conspecifics of different body sizes using chemical cues, which may reflect different physiological conditions such as hunger or stress. Pintados were observed when receiving water conditioned by either larger or similar-size conspecifics. A control group consisted of pintados receiving unconditioned water. Twelve repetitions were used for each condition. Feeding-like behaviours were investigated in the receiver fish and showed that they responded only to the conditioned water. Furthermore, a higher frequency of responses occurred when the water was conditioned by a similar-size conspecific. Thus, it is concluded that pintados are able to recognize conspecific size by chemical cues related to size and that this ability contributes to the individual's decision making on whether to approach or to avoid the conspecific.     

Response kinetics of tethered bacteria to stepwise changes in nutrient concentration

We examined the changes in swimming behaviour of the bacterium Rhodobacter sphaeroides in response to stepwise changes in a nutrient (propionate), following the pre-stimulus motion, the initial response and the adaptation to the sustained concentration of the chemical. This was carried out by tethering motile cells by their flagella to glass slides and following the rotational behaviour of their cell bodies in response to the nutrient change. Computerised motion analysis was used to analyse the behaviour. Distributions of run and stop times were obtained from rotation data for tethered cells. Exponential and Weibull fits for these distributions, and variability in individual responses are discussed. In terms of parameters derived from the run and stop time distributions, we compare the responses to stepwise changes in the nutrient concentration and the long-term behaviour of 84 cells under 12 propionate concentration levels from 1 nM to 25 mM. We discuss traditional assumptions for the random walk approximation to bacterial swimming and compare them with the observed R. sphaeroides motile behaviour.     

Generalization of predator recognition: Velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes

Many prey species detect chemical cues from predators and modify their behaviours in ways that reduce their risk of predation. Theory predicts that prey should modify their anti-predator responses according to the degree of threat posed by the predator. That is, prey should show the strongest responses to chemicals of highly dangerous prey, but should ignore or respond weakly to chemicals from non-dangerous predators. However, if anti-predator behaviours are not costly, and predators are rarely encountered, prey may exhibit generalised antipredator behaviours to dangerous and non-dangerous predators. In Australia, most elapid snakes eat lizards, and are therefore potentially dangerous to lizard prey. Recently, we found that the nocturnal velvet gecko Oedura lesueurii responds to chemicals from dangerous and non-dangerous elapid snakes, suggesting that it displays gen-eralised anti-predator behaviours to chemicals from elapid snakes. To explore the generality of this result, we videotaped the be-haviour of velvet geckos in the presence of chemical cues from two small elapid snakes that rarely consume geckos: the nocturnal golden-crowned snake Cacophis squamulosus and the diurnal marsh snake Hemiaspis signata. We also videotaped geckos in tri-als involving unsceted cards (controls) and cologne-scented cards (pungency controls). In trials involving Cacophis and Hemi-aspis chemicals, 50% and 63% of geckos spent long time periods (> 3 min) freezing whilst pressed flat against the substrate, re-spectively. Over half the geckos tested exhibited anti-predator behaviours (tail waving, tail vibration, running) in response to Ca-cophis (67%) or Hemiaspis (63%) chemicals. These behaviours were not observed in control or pungency control trials. Our re-sults support the idea that the velvet gecko displays generalised anti-predator responses to chemical cues from elapid snakes. Generalised responses to predator chemicals may be common in prey species that co-occur with multiple, ecologically similar, dangerous predators.     

Concentration‐dependent chemosensory responses towards pheromones are influenced by receiver attributes in Asian elephants

The physical structure of a signal is not sufficient to determine its meaning. For chemical signals between conspecifics, this concept is termed “pheromonal parsimony.” The function of a compound depends not only on its molecular structure but also on its context, which can include signal concentration and various receiver attributes. We sought to investigate the contextual flexibility of chemosensory responses through bioassays with Asian elephant (Elephas maximus) sex pheromones of various concentrations (frontalin, from males, and (Z)‐7‐dodecenyl acetate [Z7‐12:Ac], from females). We hypothesized that elephants would respond stronger to higher concentrations, especially towards the opposite‐sex pheromone, and that receiver age and sexual experience would modify responses. We examined responses of 73 captive elephants to both compounds. Pheromone concentration impacted the rate of chemosensory response, which was further modified by the sex, age and/or sexual experience of the receiver. Response rates increased with concentration for each compound across both sexes. Experience shaped male responses with older, physiologically primed males responding more often. The interaction between experience and age affected female response to frontalin, but not to Z7‐12:Ac. Furthermore, response thresholds were modified by sexual experience in most cases: experienced animals generally had lower thresholds than inexperienced animals. Elephants responded to each solution according to its perceived relevance, including concentration. These results also indicate that receiver attributes (e.g., sex, age and sexual experience) may modify seemingly fixed chemosensory responses and further emphasize the flexibility of vertebrate communication systems.     

An Analysis of Field Potentials During Different Tailflip Behaviours in Crayfish

Crayfish tailflips have been intensively studied to reveal the decision-making processes and neural organisation underlying a stereotyped escape behaviour. Three behaviours mediated by different neural pathways have been well described: medial giant, lateral giant and non-giant tailflips. It has proved difficult to distinguish between the three without invasive or restrictive experimental manipulation. We report unambiguous differences between the signals generated by the crayfish Cherax destructor during the three types of tailflip when recorded by bath electrodes placed in the holding aquarium. Using our ability to distinguish between the different behaviours in freely moving animals we examined the relationship between the type of tailflip evoked by stimulation to different parts of the body. The transition zone between medial and lateral giant tailflips is the thoracic-abdominal border but it is not absolute and some stimuli produce responses that cannot be unambiguously assigned to either behavioural category. We examined the latency between stimulation at different points down the length of the body and the appearance of the electrical signal accompanying escape for both medial and lateral tailflips. We used two methods to estimate the proportion of the latency accounted for by giant fibre conduction velocity. The results support current views of the differences between the activation sites of the two giant fibre systems and suggest why stimulation in the transition zone results in ambiguous outcomes.     

Auditory change detection by a single neuron in an insect

The detection of novel signals in the auditory scene is an elementary task of any hearing system. In Neoconocephalus katydids, a primary auditory interneuron (TN-1) with broad spectral sensitivity, responded preferentially to rare deviant pulses (7 pulses/s repetition rate) embedded among common standard pulses (140 pulses/s repetition rate). Eliminating inhibitory input did not affect the detection of the deviant pulses. Detection thresholds for deviant pulses increased significantly with increasing amplitude of standard pulses. Responses to deviant pulses occurred when the carrier frequencies of deviant and standard were sufficiently different, both when the deviant had a higher or lower carrier frequency than the standard. Recordings from receptor neurons revealed that TN-1 responses to the deviant pulses did not depend on the population response strength of the receptors, but on the distribution of the receptor cell activity. TN-1 responses to the deviant pulse occurred only when the standard and deviant pulses were transmitted by different groups of receptor cells. TN-1 responses parallel stimulus specific adaptation (SSA) described in mammalian auditory system. The results support the hypothesis that the mechanisms underlying SSA and change-detection are located in the TN-1 dendrite, rather than the receptor cells.