Innate Avoidance Behavior Research Articles

A systematic review and meta-analysis of thigmotactic behaviour in the open field test in rodent models associated with persistent pain.

Thigmotaxis is an innate predator avoidance behaviour of rodents. To gain insight into how injury and disease models, and analgesic drug treatments affect thigmotaxis, we performed a systematic review and meta-analysis of studies that assessed thigmotaxis in the open field test. Systematic searches were conducted of 3 databases in October 2020, March and August 2022. Study design characteristics and experimental data were extracted and analysed using a random-effects meta-analysis. We also assessed the correlation between thigmotaxis and stimulus-evoked limb withdrawal. This review included the meta-analysis of 165 studies We report thigmotaxis was increased in injury and disease models associated with persistent pain and this increase was attenuated by analgesic drug treatments in both rat and mouse experiments. Its usefulness, however, may be limited in certain injury and disease models because our analysis suggested that thigmotaxis may be associated with the locomotor function. We also conducted subgroup analyses and meta-regression, but our findings on sources of heterogeneity are inconclusive because analyses were limited by insufficient available data. It was difficult to assess internal validity because reporting of methodological quality measures was poor, therefore, the studies have an unclear risk of bias. The correlation between time in the centre (type of a thigmotactic metric) and types of stimulus-evoked limb withdrawal was inconsistent. Therefore, stimulus-evoked and ethologically relevant behavioural paradigms should be viewed as two separate entities as they are conceptually and methodologically different from each other.

Bumble Bee Avoidance of Argentine Ants and Associated Chemical Cues

Bees provide pollination services in both agricultural and natural ecosystems. However, invasive ants that exploit floral nectar in these landscapes can compete with bees for resources, with implications for pollinator resource acquisition, plant fitness, and, ultimately, ecosystem function. While interference competition has been described between bees and nectivorous, non-pollinator antagonists, the behaviors and sensory mechanisms involved remain largely unresolved. Here, we studied the mechanisms by which invasive Argentine ants influence bee nectar foraging behavior. In a series of laboratory assays, we assessed the foraging behavior of bumble bees (Bombus impatiens) in response to live Argentine ants (Linepithema humile) or to a subset of ant chemical cues. Bees were clearly deterred by live ants at a nectar source: they consumed less, fed less frequently, and fed for a shorter duration when live ants were present. Bees were also deterred by a combination of olfactory and gustatory ant chemical cues, consistent with both innate and learned avoidance behavior. Naïve and ant-experienced bees were deterred through chemosensation of ants, feeding less from nectar infused with ant chemicals as compared to nectar lacking ants or their associated cues. Some ant-experienced bees showed a unique behavior, displaying aggression toward ants as well as in response to ant chemicals. The marked effects of this invasive ant on bee foraging behavior—through physical interaction and chemical cues—highlights Argentine ants as a serious pest whose control should be considered when developing pollinator conservation and management strategies.

Bidirectional Influence of Limbic GIRK Channel Activation on Innate Avoidance Behavior.

Systemic administration of ML297, a selective activator of G-protein-gated inwardly rectifying K+ (GIRK) channels, decreases innate avoidance behavior in male C57BL/6J mice. The cellular mechanisms mediating the ML297-induced suppression of avoidance behavior are unknown. Here, we show that systemic ML297 administration suppresses elevated plus maze (EPM)-induced neuronal activation in the ventral hippocampus (vHPC) and basolateral amygdala (BLA) and that ML297 activates GIRK1-containing GIRK channels in these limbic structures. While intracranial infusion of ML297 into the vHPC suppressed avoidance behavior in the EPM test, mirroring the effect of systemic ML297, intra-BLA administration of ML297 provoked the opposite effect. Using neuron-specific viral genetic and chemogenetic approaches, we found that the combined inhibition of excitatory neurons in CA3 and dentate gyrus (DG) subregions of the vHPC was sufficient to decrease innate avoidance behavior in the EPM, open-field, and light-dark tests in male C57BL/6J mice, while performance in the marble-burying test was not impacted. Furthermore, genetic ablation of GIRK channels in CA3/DG excitatory neurons precluded the suppression of avoidance behavior evoked by systemic ML297 in the EPM test. Thus, acute inhibition of excitatory neurons in the ventral CA3 and DG subregions of the vHPC is necessary for the apparent anxiolytic efficacy of systemic ML297 and is sufficient to decrease innate avoidance behavior in male C57BL/6J mice.SIGNIFICANCE STATEMENT We interrogated the cellular mechanisms underlying the apparent anxiolytic efficacy of ML297, a selective activator of G-protein-gated inwardly rectifying K+ (GIRK) channels and promising lead compound. Intracranial infusion of ML297 into the ventral hippocampus (vHPC) and basolateral amygdala (BLA) complex exerted opposing influence on innate avoidance behavior in male C57BL/6J mice, the former recapitulating the suppression of avoidance behavior evoked by systemic ML297. Using viral genetic and chemogenetic approaches, we showed that combined inhibition of excitatory neurons in CA3 and dentate gyrus (DG) subregions of the vHPC is sufficient to decrease innate avoidance behavior in male mice and mediates the decrease in avoidance behavior evoked by systemic ML297. These findings establish a foundation for future investigations into the therapeutic potential of GIRK channel modulation in anxiety disorders.

Frontostriatal Projections Regulate Innate Avoidance Behavior.

The dorsomedial prefrontal cortex (dmPFC) has been linked to avoidance and decision-making under conflict, key neural computations altered in anxiety disorders. However, the heterogeneity of prefrontal projections has obscured identification of specific top-down projections involved. While the dmPFC-amygdala circuit has long been implicated in controlling reflexive fear responses, recent work suggests that dmPFC-dorsomedial striatum (DMS) projections may be more important for regulating avoidance. Using fiber photometry recordings in both male and female mice during the elevated zero maze task, we show heightened neural activity in frontostriatal but not frontoamygdalar projection neurons during exploration of the anxiogenic open arms. Additionally, using optogenetics, we demonstrate that this frontostriatal projection preferentially excites postsynaptic D1 receptor-expressing neurons in the DMS and causally controls innate avoidance behavior. These results support a model for prefrontal control of defensive behavior in which the dmPFC-amygdala projection controls reflexive fear behavior and the dmPFC-striatum projection controls anxious avoidance behavior.SIGNIFICANCE STATEMENT The medial prefrontal cortex has been extensively linked to several behavioral symptom domains related to anxiety disorders, with much of the work centered around reflexive fear responses. Comparatively little is known at the mechanistic level about anxious avoidance behavior, a core feature across anxiety disorders. Recent work has suggested that the striatum may be an important hub for regulating avoidance behaviors. Our work uses optical circuit dissection techniques to identify a specific corticostriatal circuit involved in encoding and controlling avoidance behavior. Identifying neural circuits for avoidance will enable the development of more targeted symptom-specific treatments for anxiety disorders.

Sex differences and effects of the estrous stage on hippocampal-prefrontal theta communications.

Effective communication between the mammalian hippocampus and neocortex is essential to certain cognitive‐behavioral tasks critical to survival in a changing environment. Notably, functional synchrony between local field potentials (LFPs) of the ventral hippocampus (vHPC) and the medial prefrontal cortex (mPFC) within the theta band (4–12 Hz) underlies innate avoidance behavior during approach‐avoidance conflict tasks in male rodents. However, the physiology of vHPC‐mPFC communications in females remains unestablished. Furthermore, little is known about how mPFC subdivisions functionally interact in the theta band with hippocampal subdivisions in both sexes in the absence of task demand. Given the established roles of biological sex and gonadal hormone status on innate avoidance behaviors and neuronal excitability, here, we characterize the effects of biological sex and female estrous stage on hippocampal‐prefrontal (HPC‐mPFC) theta signaling in freely moving female and male rats. LFPs from vHPC, dorsal hippocampus (dHPC), mPFC‐prelimbic (PrL), and mPFC‐infralimbic (IL) were simultaneously recorded during spontaneous exploration of a familiar arena. Data suggest that theta phase and power in vHPC preferentially synchronize with PrL; conversely, dHPC and IL preferentially synchronize. Males displayed greater vHPC‐PrL theta synchrony than females, despite similar regional frequency band power and inter‐regional coherence. Additionally, several significant estrous‐linked changes in HPC‐mPFC theta dynamics were observed. These findings support the hypothesis that HPC‐mPFC theta signaling is sensitive to both biological sex and female estrous stage. These findings establish novel research avenues concerning sex as a biological variable and effects of gonadal hormone status on HPC‐mPFC network activity as it pertains to threat evaluation biomarkers.

Orexin neurons and inhibitory Agrp→orexin circuits guide spatial exploration in mice.

Photoinhibition of endogenous activity of lateral hypothalamic orexin neurons causes place preference and reduces innate avoidance Endogenous activity of orexin neurons correlates with place preference Mediobasal hypothalamic Agrp neurons inhibit orexin neurons via GABA, and chemogenetic suppression of Agrp neurons increases avoidance in an orexin receptor-dependent manner. Hypothalamic orexin/hypocretin neurons integrate multiple sensory cues and project brain-wide to orchestrate diverse innate behaviours. Their loss impairs many context-appropriate actions, but the motivational characteristics of orexin cell activity remain unclear. We and others previously approached this question by artificial orexin stimulation, which could induce either rewarding (positive valence) or aversive (negative valence) brain activity. It is unknown to what extent such approaches replicate natural/endogenous orexin signals, which rapidly fluctuate during wakefulness. Here we took an alternative approach, focusing on observing and silencing natural orexin cell signals associated with a fundamental innate behaviour, self-paced spatial exploration. We found that mice are more likely to stay in places paired with orexin cell optosilencing. The orexin cell optosilencing also reduced avoidance of places that mice find innately aversive. Correspondingly, calcium recordings revealed that orexin cell activity rapidly reduced upon exiting the innately aversive places. Furthermore, we provide optogenetic evidence for an inhibitory GABAergic Agrp→orexin hypothalamic neurocircuit, and find that Agrp cell suppression increases innate avoidance behaviour, consistent with orexin disinhibition. These results imply that exploration may be motivated and oriented by a need to reduce aversive orexin cell activity, and suggest a hypothalamic circuit for fine-tuning orexin signals to changing ethological priorities.

<i>Drosophila</i> Larval Light Avoidance is Negatively Regulated by Temperature Through Two Pairs of Central Brain Neurons

Animal’s innate avoidance behavior is crucial for its survival. It subjects to modulation by environmental conditions in addition to the commanding sensorimotor transformation pathway. Although much has been known about the commanding neural basis, relatively less is known about how innate avoidance behavior is shaped by external conditions. Here in this paper, we report that Drosophila larvae showed stronger light avoidance at lower temperatures than at higher temperatures. Such negative regulation of light avoidance by temperature was abolished by blocking two pairs of central brain neurons, ACLPR60F09 neurons, that were responsive to both light and temperature change, including cooling and warming. ACLPR60F09 neurons could be excited by pdf-LaN neurons in the visual pathway. On the downstream side, they could inhibit the CLPNR82B09 neurons that command light induced reorientation behavior. Compared with at warm temperature, ACLPR60F09 neurons’ response to light was decreased at cool temperature so that the inhibition on CLPNR82B09 neurons was relieved and the light induced avoidance was enhanced. Our result proposed a neural mechanism underlying cross-modal modulation of animal innate avoidance behavior.

Functional divergence of the bitter receptor TAS2R38 in Sulawesi macaques.

Bitter perception is mediated by G protein‐coupled receptors TAS2Rs and plays an important role in avoiding the ingestion of toxins by inducing innate avoidance behavior in mammals. One of the best‐studied TAS2Rs is TAS2R38, which mediates the perception of the bitterness of synthetic phenylthiocarbamide (PTC). Previous studies of TAS2R38 have suggested that geographical separation enabled the independent divergence of bitter taste perception. The functional divergence of TAS2R38 in allopatric species has not been evaluated. We characterized the function of TAS2R38 in four allopatric species of Sulawesi macaques on Sulawesi Island. We found variation in PTC taste perception both within and across species. In most cases, TAS2R38 was sensitive to PTC, with functional divergence among species. We observed different truncated TAS2R38s that were not responsive to PTC in each species of Macaca nigra and M. nigrescens due to premature stop codons. Some variants of intact TAS2R38 with an amino acid substitution showed low sensitivity to PTC in M. tonkeana. Similarly, this intact TAS2R38 with PTC‐low sensitivity has also been found in humans. We detected a shared haplotype in all four Sulawesi macaques, which may be the ancestral haplotype of Sulawesi macaques. In addition to shared haplotypes among Sulawesi macaques, other TAS2R38 haplotypes were species‐specific. These results implied that the variation in TAS2R38 might be shaped by geographical patterns and local adaptation.OPEN RESEARCH BADGES This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.908jf3r.

Identification of environmental stressors and validation of light preference as a measure of anxiety in larval zebrafish.

BackgroundLarval zebrafish, with a simple and transparent vertebrate brain composed of ~100 K neurons, is well suited for deciphering entire neural circuit activity underlying behavior. Moreover, their small body size (~4–5 mm in length) is compatible with 96-well plates, making larval zebrafish amenable to high content screening. Despite these attractive features, there is a scarcity of behavioral characterizations in larval zebrafish compared to other model organisms as well as adult zebrafish.ResultsIn this study, we have characterized the physiological and behavioral responses of larval zebrafish to several easily amenable stimuli, including heat, cold, UV, mechanical disturbance (MD), and social isolation (SI). These stimuli are selected based on their perceived aversive nature to larval zebrafish. Using a light/dark choice paradigm, in which larval zebrafish display an innate dark avoidance behavior (i.e. scotophobia), we find that heat, cold and UV stimuli significantly enhance their dark avoidance with heat having the most striking effect, whereas MD and SI have little influence on the behavior. Surprisingly, using the cortisol assay, a physiological measure of stress, we uncover that all stimuli but heat and SI significantly increase the whole body cortisol levels.ConclusionThese results identify a series of stressors that can be easily administered to larval zebrafish. Those stimuli that elicit differential responses at behavioral and physiological levels warrant further studies at circuit levels to understand the underlying mechanisms. The findings that various stressors enhance while anxiolytics attenuate dark avoidance further reinforce that the light/dark preference behavior in larval zebrafish is fear/anxiety-associated.

Caenorhabditis elegans employs innate and learned aversion in response to bacterial toxic metabolites tambjamine and violacein.

Bacteriovorus eukaryotes such as nematodes are one of the major natural predators of bacteria. In their defense bacteria have evolved a number of strategies to avoid predation, including the production of deterrent or toxic metabolites, however little is known regarding the response of predators towards such bacterial defenses. Here we use the nematode C. elegans as a model to study a predators’ behavioral response towards two toxic bacterial metabolites, tambjamine YP1 and violacein. We found that C. elegans displays an innate avoidance behavior towards tambjamine YP1, however requires previous exposure to violacein before learning to avoid this metabolite. The learned avoidance of violacein is specific, reversible, is mediated via the nematode olfactory apparatus (aversive olfactory learning) and is reduced in the absence of the neurotransmitter serotonin. These multiple strategies to evade bacterial toxic metabolites represent a valuable behavioral adaptation allowing bacteriovorus predators to distinguish between good and bad food sources, thus contributing to the understanding of microbial predator-prey interactions.

Genetics of Intraspecies Variation in Avoidance Behavior Induced by a Thermal Stimulus in Caenorhabditis elegans.

Individuals within a species vary in their responses to a wide range of stimuli, partly as a result of differences in their genetic makeup. Relatively little is known about the genetic and neuronal mechanisms contributing to diversity of behavior in natural populations. By studying intraspecies variation in innate avoidance behavior to thermal stimuli in the nematode Caenorhabditis elegans, we uncovered genetic principles of how different components of a behavioral response can be altered in nature to generate behavioral diversity. Using a thermal pulse assay, we uncovered heritable variation in responses to a transient temperature increase. Quantitative trait locus mapping revealed that separate components of this response were controlled by distinct genomic loci. The loci we identified contributed to variation in components of thermal pulse avoidance behavior in an additive fashion. Our results show that the escape behavior induced by thermal stimuli is composed of simpler behavioral components that are influenced by at least six distinct genetic loci. The loci that decouple components of the escape behavior reveal a genetic system that allows independent modification of behavioral parameters. Our work sets the foundation for future studies of evolution of innate behaviors at the molecular and neuronal level.

Aquatic adaptation and the evolution of smell and taste in whales.

IntroductionWhile olfaction is one of the most important senses in most terrestrial mammals, it is absent in modern toothed whales (Odontoceti, Cetacea). Furthermore, behavioral evidence suggests that gustation is very limited. In contrast, their aquatic sistergroup, baleen whales (Mysticeti) retain small but functional olfactory organs, and nothing is known about their gustation. It is difficult to investigate mysticete chemosensory abilities because experiments in a controlled setting are impossible.ResultsHere, we use the functional regionalization of the olfactory bulb (OB) to identify the loss of specific olfactory functions in mysticetes. We provide the whole-genome sequence of a mysticete and show that mysticetes lack the dorsal domain of the OB, an area known to induce innate avoidance behavior against odors of predators and spoiled foods. Genomic and fossil data suggest that mysticetes lost the dorsal domain of the OB before the Odontoceti-Mysticeti split. Furthermore, we found that all modern cetaceans are revealed to have lost the functional taste receptors.ConclusionThese results strongly indicate that profound changes in the chemosensory capabilities had occurred in the cetacean lineage during the period when ancestral whales migrated from land to water.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-014-0002-z) contains supplementary material, which is available to authorized users.

High-affinity olfactory receptor for the death-associated odor cadaverine

Carrion smell is strongly repugnant to humans and triggers distinct innate behaviors in many other species. This smell is mainly carried by two small aliphatic diamines, putrescine and cadaverine, which are generated by bacterial decarboxylation of the basic amino acids ornithine and lysine. Depending on the species, these diamines may also serve as feeding attractants, oviposition attractants, or social cues. Behavioral responses to diamines have not been investigated in zebrafish, a powerful model system for studying vertebrate olfaction. Furthermore, olfactory receptors that detect cadaverine and putrescine have not been identified in any species so far. Here, we show robust olfactory-mediated avoidance behavior of zebrafish to cadaverine and related diamines, and concomitant activation of sparse olfactory sensory neurons by these diamines. The large majority of neurons activated by low concentrations of cadaverine expresses a particular olfactory receptor, trace amine-associated receptor 13c (TAAR13c). Structure-activity analysis indicates TAAR13c to be a general diamine sensor, with pronounced selectivity for odd chains of medium length. This receptor can also be activated by decaying fish extracts, a physiologically relevant source of diamines. The identification of a sensitive zebrafish olfactory receptor for these diamines provides a molecular basis for studying neural circuits connecting sensation, perception, and innate behavior.

Dedicated olfactory neurons mediating attraction behavior to ammonia and amines in Drosophila

Animals across various phyla exhibit odor-evoked innate attraction behavior that is developmentally programmed. The mechanism underlying such behavior remains unclear because the odorants that elicit robust attraction responses and the neuronal circuits that mediate this behavior have not been identified. Here, we describe a functionally segregated population of olfactory sensory neurons (OSNs) and projection neurons (PNs) in Drosophila melanogaster that are highly specific to ammonia and amines, which act as potent attractants. The OSNs express IR92a, a member of the chemosensory ionotropic receptor (IR) family and project to a pair of glomeruli in the antennal lobe, termed VM1. In vivo calcium-imaging experiments showed that the OSNs and PNs innervating VM1 were activated by ammonia and amines but not by nonamine odorants. Flies in which the IR92a(+) neurons or IR92a gene was inactivated had impaired amine-evoked physiological and behavioral responses. Tracing neuronal pathways to higher brain centers showed that VM1-PN axonal projections within the lateral horn are topographically segregated from those of V-PN and DC4-PN, which mediate innate avoidance behavior to carbon dioxide and acidity, respectively, suggesting that these sensory stimuli of opposing valence are represented in spatially distinct neuroanatomic loci within the lateral horn. These experiments identified the neurons and their cognate receptor for amine detection, and mapped amine attractive olfactory inputs to higher brain centers. This labeled-line mode of amine coding appears to be hardwired to attraction behavior.

A Conserved Dedicated Olfactory Circuit for Detecting Harmful Microbes in Drosophila

Flies, like all animals, need to find suitable and safe food. Because the principal food source for Drosophila melanogaster is yeast growing on fermenting fruit, flies need to distinguish fruit with safe yeast from yeast covered with toxic microbes. We identify a functionally segregated olfactory circuit in flies that is activated exclusively by geosmin. This microbial odorant constitutes an ecologically relevant stimulus that alerts flies to the presence of harmful microbes. Geosmin activates only a single class of sensory neurons expressing the olfactory receptor Or56a. These neurons target the DA2 glomerulus and connect to projection neurons that respond exclusively to geosmin. Activation of DA2 is sufficient and necessary for aversion, overrides input from other olfactory pathways, and inhibits positive chemotaxis, oviposition, and feeding. The geosmin detection system is a conserved feature in the genus Drosophila that provides flies with a sensitive, specific means of identifying unsuitable feeding and breeding sites.

Shovelnose sturgeon exhibit predator avoidance behaviour in the presence of a hungry predator

An experiment was designed to test whether age-0 shovelnose sturgeon (Scaphirhynchus platorynchus) exhibited predator avoidance behaviour in response to a channel catfish (Ictalurus punctatus) predator. It was hypothesized that shovelnose sturgeon would not exhibit any innate predator avoidance behaviour because previous reports have shown a congener of the shovelnose sturgeon, the pallid sturgeon (S. albus), to be an unfavourable prey item for channel catfish. The results, however, indicated that shovelnose sturgeon generally avoided space occupied by the catfish predator and spent a greater proportion of time in the predator avoidance zone within the experimental tank. Bitten fish, in particular, spent a greater period of time in the predator avoidance zone. Of all sturgeon used in this experiment (N = 30), 73% swam within the fork length (350 mm) of the catfish predator. The results seem to indicate that shovelnose sturgeon were initially oblivious to the risk of predation by the catfish predator, but after interaction (e.g. being chased or bitten) appeared to display predator avoidance behaviour. Predator avoidance behaviour in shovelnose sturgeon may thus be suggested as a learned rather than an innate behaviour.

Loss of the V-ATPase B1 subunit isoform expressed in non-neuronal cells of the mouse olfactory epithelium impairs olfactory function.

The vacuolar proton-pumping ATPase (V-ATPase) is the main mediator of intracellular organelle acidification and also regulates transmembrane proton (H+) secretion, which is necessary for an array of physiological functions fulfilled by organs such as the kidney, male reproductive tract, lung, bone, and ear. In this study we characterize expression of the V-ATPase in the main olfactory epithelium of the mouse, as well as a functional role for the V-ATPase in odor detection. We report that the V-ATPase localizes to the apical membrane microvilli of olfactory sustentacular cells and to the basolateral membrane of microvillar cells. Plasma membrane V-ATPases containing the B1 subunit isoform are not detected in olfactory sensory neurons or in the olfactory bulb. This precise localization of expression affords the opportunity to ascertain the functional relevance of V-ATPase expression upon innate, odor-evoked behaviors in B1-deficient mice. This animal model exhibits diminished innate avoidance behavior (revealed as a decrease in freezing time and an increase in the number of sniffs in the presence of trimethyl-thiazoline) and diminished innate appetitive behavior (a decrease in time spent investigating the urine of the opposite sex). We conclude that V-ATPase-mediated H+ secretion in the olfactory epithelium is required for optimal olfactory function.

Conditioning the crab Carcinus maenas against instinctive light avoidance

Carcinus maenas is an invasive species found in Northern American waters overtaking the less adaptable species and responding to various forms of conditioning. In this study, we conditioned C. maenas to reverse its innate light avoidance behavior. Within 6 days of testing, 21 out of 30 crabs were successfully trained to enter a beam of light to receive food, although their instincts are to seek shelter from predators in dark areas. Some took as little as 2 days to reverse their light aversion. They also responded faster once trained. Larger crabs had faster response times than smaller ones, while there was no difference between sexes. The conditioned response lasted for at least 4 days without reinforcement. The rapid learning abilities observed during this experiment may help to explain the pervasive success of C. maenas as an invasive species.

Hear no evil: The effect of auditory warning signals on avian innate avoidance, learned avoidance and memory

Abstract Many aposematic insect species advertise their toxicity to potential predators using olfactory and auditory signals, in addition to visual signals, to produce a multimodal warning display. The olfactory signals in these displays may have interesting effects, such as eliciting innate avoidance against novel colored prey, or improving learning and memory of defended prey. However, little is known about the effects of such ancillary signals when they are auditory rather than olfactory. The few studies that have investigated this question have provided conflicting results. The current study sought to clarify and extend understanding of the effects of prey auditory signals on avian predator responses. The domestic chick Gallus gallus domesticus was used as a model avian predator to examine how the defensive buzzing sound of a bumblebee Bombus terrestris affected the chick’s innate avoidance behavior, and the learning and memory of prey avoidance. The results demonstrate that the buzzing sound had no effect on the predator’s responses to unpalatable aposematically colored crumbs, suggesting that the agitated buzzing of B. terrestris may provide no additional protection from avian predators.

The snail Potamopyrgus antipodarum grows faster and is more active in the shade, independent of food quality

Ecological stoichiometry has advanced food web ecology by emphasising the importance of food quality over food quantity for herbivores. Here, we focus on the effects of abiotic factors such as nutrients and light (known to influence food quality) on grazer growth rates. As model organism we used the mudsnail Potamopyrgus antipodarum that is native to New Zealand but invasive elsewhere. In a stream channel experiment in New Zealand, we manipulated light (two levels) and nutrients (four levels) to achieve a range of primary producer carbon: nutrient ratios and added mudsnails (3 densities + ungrazed control) to 128 periphyton covered stream channels in a 2 × 4 × 4 full factorial design. We measured snail growth rate and activity, food quality and nutritional imbalance, to test the predictions that (1) less light and more nutrients increase periphyton food quality and thus snail growth rates, and (2) less crowding leads to higher food availability and thus higher snail growth rates. We found that snail growth rates were higher under low light than under high light intensities and this difference increased with increasing nutrient addition. These changes in growth rate were not mediated by food quality in terms of periphyton nutrient ratios. Furthermore, experimental treatments strongly affected snail behaviour. Snails grazed more actively in the low light treatments, and thus it is more likely that snail growth rates were directly affected by light levels, maybe as a result of innate predator avoidance behaviour or as a reaction to high UV intensities. We conclude that in our stream channels snail growth rate was limited by factors other than food quality and quantity such as UV exposure, algal defences or the relatively low ambient water temperature.