Death feigning as an adaptive anti‐predator behaviour: Further evidence for its evolution from artificial selection and natural populations

Death feigning is considered to be an adaptive antipredator behaviour. Previous studies on Tribolium castaneum have shown that prey which death feign have a fitness advantage over those that do not when using a jumping spider as the predator. Whether these effects are repeatable across species or whether they can be seen in nature is, however, unknown. Therefore, the present study involved two experiments: (a) divergent artificial selection for the duration of death feigning using a related species T. freemani as prey and a predatory bug as predator, demonstrating that previous results are repeatable across both prey and predator species, and (b) comparison of the death‐feigning duration of T. castaneum populations collected from field sites with and without predatory bugs. In the first experiment, T. freemani adults from established selection regimes with longer durations of death feigning had higher survival rates and longer latency to being preyed on when they were placed with predatory bugs than the adults from regimes selected for shorter durations of death feigning. As a result, the adaptive significance of death‐feigning behaviour was demonstrated in another prey–predator system. In the second experiment, wild T. castaneum beetles from populations with predators feigned death longer than wild beetles from predator‐free populations. Combining the results from these two experiments with those from previous studies provided strong evidence that predators drive the evolution of longer death feigning.     

Predation selects for low resting metabolic rate and consistent individual differences in anti-predator behavior in a beetle

Significant between-individual variation in resting metabolic rate (RMR) of animals is a widespread phenomenon that may have important implications for our understanding of variation in behavior and animal personality. By using wild caught mealworm beetles, Tenebrio molitor, we examined the relationships among survival rate under predator tests, individual response latency time to become immobile under the risk of predation, duration of immobility time, and RMR. Individuals with higher levels of RMR were bold, and bold individuals were found to be more exposed to the risk of bird predation. We found that RMR was positively correlated with the latency of immobility response and negatively correlated with the total duration of immobility. The correlation between behavioral responses suggests a behavioral syndrome in the anti-predator behavior of T. molitor. The results indicate that energy metabolism may be part of a syndrome that involves behavior and life history traits in animals.     

Benefits of polyandry: Molecular evidence from field‐caught dung beetles

When females mate with multiple males, they set the stage for postcopulatory sexual selection via sperm competition and/or cryptic female choice. Surprisingly little is known about the rates of multiple mating by females in the wild, despite the importance of this information in understanding the potential for postcopulatory sexual selection to drive the evolution of reproductive behaviour, morphology and physiology. Dung beetles in the genus Onthophagus have become a laboratory model for studying pre‐ and postcopulatory sexual selection, yet we still lack information about the reproductive behaviour of female dung beetles in natural populations. Here, we develop microsatellite markers for Onthophagus taurus and use them to genotype the offspring of wild‐caught females and to estimate natural rates of multiple mating and patterns of sperm utilization. We found that O. taurus females are highly polyandrous: 88% of females produced clutches sired by at least two males, and 5% produced clutches with as many as five sires. Several females (23%) produced clutches with significant paternity skew, indicating the potential for strong postcopulatory sexual selection in natural populations. There were also strong positive correlations between the number of offspring produced and both number of fathers and paternity skew, which suggests that females benefit from mating polyandrously by inciting postcopulatory mechanisms that bias paternity towards males that can sire more viable offspring. This study evaluates the fitness consequences of polyandry for an insect in the wild and provides strong evidence that female dung beetles benefit from multiple mating under natural conditions.     

Does dimethyl sulfoxide increase protein immunomarking efficiency for dispersal and predation studies?

Marking biological control agents facilitates studies of dispersal and predation. This study examines the effect of a biological solvent, dimethyl sulfoxide (DMSO), on retention of immunoglobulin G (IgG) protein solutions applied to Diorhabda carinulata (Desbrochers) (Coleoptera: Chrysomelidae), an important biological control agent of saltcedar, either internally by feeding them protein‐labeled foliage or externally by immersing them in a protein solution. In addition, we determined whether internally or externally marked DMSO‐IgG labels could be transferred via feeding from marked D. carinulata to its predator, Perillus bioculatus (Fabricius) (Heteroptera: Pentatomidae). The presence of rabbit and chicken IgG proteins was detected by IgG‐specific enzyme‐linked immunosorbent assays (ELISA). DMSO‐IgG treatments showed greater label retention than IgG treatments alone, and this effect was stronger for rabbit IgG than for chicken IgG. Fourteen days after marking, beetles immersed in rabbit IgG showed 100% internal retention of label, whereas beetles immersed in chicken IgG showed 65% internal retention. Immersion led to greater initial (time 0) label values, and longer label retention, than feeding beetles labeled foliage. The DMSO‐IgG label was readily transferred to P. bioculatus after feeding on a single marked prey insect. This investigation shows that addition of DMSO enhances retention of IgG labels, and demonstrates that protein marking technology has potential for use in dispersal and predator–prey studies with D. carinulata. Moreover, our observation of P. bioculatus feeding on D. carinulata is, to our knowledge, a new predator–prey association for the stink bug.     

Do pygidial secretions of dung beetles have the potential to repel urban pest ants?

Various organisms emit malodorous secretions against competitors, and the potential use of these secretions in pest management should be investigated. For example, some ant species feed on similar resources as dung beetles, which might have led to counter chemical defences in dung beetles. We tested whether pygidial secretions of the dung beetle Canthon smaragdulus (Fabricius) (Coleoptera: Scarabaeidae, Scarabaeinae) alter the locomotor behaviour of the exotic urban pest ant Tapinoma melanocephalum (Fabricius) (Hymenoptera: Formicidae), specifically whether these secretions repel those ants. We also tested whether the disturbance in the locomotor behaviour of T. melanocephalum increases with the amount of pygidial secretion. We found that individual T. melanocephalum displayed changes in their locomotor behaviour when exposed to pygidial secretions of coupled dung beetles, single males, and single females. Additionally, the pygidial secretions from male and female dung beetles could repel ants. The change in the locomotor behaviour of T. melanocephalum increased with the amount of pygidial secretion. Our results suggest that the pygidial secretions of dung beetles have potential as a biological repellent of T. melanocephalum. Hence, pygidial secretions from dung beetles may be used in the future for the development of urban pest management strategies.     

Male mealworm beetles increase resting metabolic rate under terminal investment

Harmful parasite infestation can cause energetically costly behavioural and immunological responses, with the potential to reduce host fitness and survival. It has been hypothesized that the energetic costs of infection cause resting metabolic rate (RMR) to increase. Furthermore, under terminal investment theory, individuals exposed to pathogens should allocate resources to current reproduction when life expectancy is reduced, instead of concentrating resources on an immune defence. In this study, we activated the immune system of Tenebrio molitor males via insertion of nylon monofilament, conducted female preference tests to estimate attractiveness of male odours and assessed RMR and mortality. We found that attractiveness of males coincided with significant down‐regulation of their encapsulation response against a parasite‐like intruder. Activation of the immune system increased RMR only in males with heightened odour attractiveness and that later suffered higher mortality rates. The results suggest a link between high RMR and mortality and support terminal investment theory in T. molitor.     

Observations of parasitoid behaviour in both no‐choice and choice tests are consistent with proposed ecological host range

The solitary larval endoparasitoid Eadya daenerys Ridenbaugh (Hymenoptera: Braconidae) is a proposed biocontrol agent of Paropsis charybdis Stål (Coleoptera: Chrysomelidae, Chrysomelinae), a pest of eucalypts in New Zealand. Eadya daenerys oviposition behaviour was examined in two assay types during host range testing, with the aim of improving ecological host range prediction. No‐choice sequential and two‐choice behavioural observations were undertaken against nine closely related species of New Zealand non‐target beetle larvae, including a native beetle, introduced weed biocontrol agents, and invasive paropsine beetles. No behavioural measure was significantly different between no‐choice and two‐choice tests. In sequential no‐choice assays the order of first presentation (target–non‐target) had no significant effect on the median number of attacks or the attack rate while on the plant. Beetle species was the most important factor. Parasitoids expressed significantly lower on‐plant attack rates against non‐targets compared to target P. charybdis larvae. The median number of attacks was always higher towards target larvae than towards non‐target larvae, except for the phylogenetically closest related non‐target Trachymela sloanei (Blackburn) (Coleoptera: Chrysomelidae, Chrysomelinae). Most non‐target larvae were disregarded upon contact, which suggests that the infrequent attack behaviour observed by two individual E. daenerys against Allocharis nr. tarsalis larvae in two‐choice tests and the frass of Chrysolina abchasica (Weise) was probably abnormal host selection behaviour. Results indicate that E. daenerys is unlikely to attack non‐target species apart from Eucalyptus‐feeding invasive paropsines (Chrysomelinae). Non‐lethal negative impacts upon less preferred non‐target larvae are possible if E. daenerys does attack them in the field; however, this is likely to be rare.     

Effect of Willow Tit Poecile montanus alarm calls on attack rates by Pygmy Owls Glaucidium passerinum

One suggested anti‐predator function of alarm calls is to deliver a message to a predator that it has been detected. Moreover, giving the alarm call could provide a signal to the predator that capturing the individual giving the alarm is more difficult than capturing its silent group members, as the caller is probably the most aware of the predator's location. In an aviary experiment using stuffed dummy Willow Tits Poecile montanus, we assessed whether an authentic alarm call given by Willow Tit affected Pygmy Owl Glaucidium passerinum prey preference. In the experiment, the Owls attacked only the ‘silent’ dummy individuals, suggesting that alarm calling could offer direct fitness benefits to the caller by decreasing the attack risk of the caller relative to its group members.     

Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

The within‐host dynamics of infection in trans‐generationally primed flour beetles

Many taxa exhibit plastic immune responses initiated after primary microbial exposure that provide increased protection against disease‐induced mortality and the fitness costs of infection. In several arthropod species, this protection can even be passed from parents to offspring through a phenomenon called trans‐generational immune priming. Here, we first demonstrate that trans‐generational priming is a repeatable phenomenon in flour beetles (Tribolium castaneum) primed and infected with Bacillus thuringiensis (Bt). We then quantify the within‐host dynamics of microbes and host physiological responses in infected offspring from primed and unprimed mothers by monitoring bacterial density and using mRNA‐seq to profile host gene expression, respectively, over the acute infection period. We find that priming increases inducible resistance against Bt around a critical temporal juncture where host septicaemic trajectories, and consequently survival, may be determined in unprimed individuals. Our results identify a highly differentially expressed biomarker of priming, containing an EIF4‐e domain, in uninfected individuals, as well as several other candidate genes. Moreover, the induction and decay dynamics of gene expression over time suggest a metabolic shift in primed individuals. The identified bacterial and gene expression dynamics are likely to influence patterns of bacterial fitness and disease transmission in natural populations.     

Major histocompatibility complex variation is similar in little brown bats before and after white‐nose syndrome outbreak

White‐nose syndrome (WNS), caused by the fungal pathogen Pseudogymnoascus destructans (Pd), has driven alarming declines in North American hibernating bats, such as little brown bat (Myotis lucifugus). During hibernation, infected little brown bats are able to initiate anti‐Pd immune responses, indicating pathogen‐mediated selection on the major histocompatibility complex (MHC) genes. However, such immune responses may not be protective as they interrupt torpor, elevate energy costs, and potentially lead to higher mortality rates. To assess whether WNS drives selection on MHC genes, we compared the MHC DRB gene in little brown bats pre‐ (Wisconsin) and post‐ (Michigan, New York, Vermont, and Pennsylvania) WNS (detection spanning 2014–2015). We genotyped 131 individuals and found 45 nucleotide alleles (27 amino acid alleles) indicating a maximum of 3 loci (1–5 alleles per individual). We observed high allelic admixture and a lack of genetic differentiation both among sampling sites and between pre‐ and post‐WNS populations, indicating no signal of selection on MHC genes. However, post‐WNS populations exhibited decreased allelic richness, reflecting effects from bottleneck and drift following rapid population declines. We propose that mechanisms other than adaptive immunity are more likely driving current persistence of little brown bats in affected regions.     

Screening of natural products in the laboratory and the field for control of pollen beetles

Pollen beetles, Meligethes spp. (Coleoptera: Nitidulidae), are among the most damaging pests of oilseed rape (Brassica napus L.). Increasing populations of pyrethroid‐resistant pollen beetles coupled with the prohibition of synthetic pest control products in organic farming means that other direct control methods are needed. A laboratory study was therefore conducted to evaluate the effect of natural products, combinations of natural products and additives as well as natural and synthetic insecticides on mortality of pollen beetles. In addition, field trials under both integrated and organic production were conducted to evaluate the efficacy of six natural products, nine combinations of natural products, two synthetic insecticides (integrated‐production trials only), two natural insecticides and two additives to reduce pollen beetles. The laboratory trial, using both a curative and preventive approach, showed that two of the eight natural products (lavender oil and stone meal) caused a mortality of over 98% within the first day of application. The other natural products were only partially effective compared with the untreated control. In the field trials, the natural products reduced the number of pollen beetles 1 day after application compared with the untreated control in both trial years and production systems. Promising substances were stone meal, Silico‐Sec and liquid manure. Nevertheless, the efficacy was not consistent, and no effect on oilseed rape yield was observed. In spite of this, these products have the potential to control pollen beetles under field conditions with comparable effects to synthetic insecticides. Further research should therefore focus on timing and frequency of applications as well as on the formulation of the natural products to increase the persistency of the products under field conditions.     

Anti‐predatory behaviour of wild‐caught vs captive‐bred freshwater angelfish,Pterophyllum scalare

Environments and experiences encountered in early life stages of animals shape their adult behaviour. When environments are maintained for several generations, differential selection forces act upon individuals to select those most fit to the particular conditions. As such, differences in the behaviour of captive bred and wild caught individuals have been observed recurrently. In fish, hatchery raised individuals tend to seek refuge less, making them more vulnerable to predators. We tested the hypothesis that captive breeding induces non‐adaptive changes in behaviour of freshwater angelfish, Pterophyllum scalare. Wild‐caught and captive‐bred fish were exposed to a natural predator and measured for their anti‐predator behaviours; no differences were found in behaviour under control conditions. When exposed to a natural predator, wild‐caught fish exhibited significantly shorter freezing durations than captive‐bred fish, and took significantly shorter time to resume normal behaviour. No differences in the time taken to initiate investigations of the predator were detected. The results demonstrate that captive‐bred fish respond differently than their wild counterparts when exposed to a natural predator, and that this domestication has implications for captive rearing programmes.     

Combining lacewings and parasitoids for biological control of foxglove aphids in sweet pepper

The role of natural enemy diversity in biological pest control has been debated in many studies, and understanding how interactions amongst predators and parasitoids affect herbivore populations is crucial for pest management. In this study, we assessed the individual and combined use of two species of natural enemies, the parasitoid Aphidius ervi Haliday, and the predatory brown lacewing Micromus variegatus (Fabricius), on their shared prey, the foxglove aphid, Aulacorthum solani (Kaltenbach), on sweet pepper. We hypothesized that the presence of intraguild predation (IGP) and predator facilitation (through induced aphid dropping behaviour) might have both negative and positive effects on aphid control, respectively. Our greenhouse trial showed that overall, the greatest suppression of aphids occurred in the treatment with both the parasitoid and the lacewing. While the combination of lacewings and parasitoids significantly increased aphid control compared to the use of parasitoids alone, the effect was not significantly different to the treatment with only predators, although there was a clear trend of enhanced suppression. Thus, the combined effects of both species of natural enemies were between additive and non‐additive, suggesting that the combination is neither positive nor negative for aphid control. High levels of IGP, as proven in the laboratory, were probably compensated for by the strong aphid suppression provided by the lacewings, whether or not supplemented with some level of predator facilitation. For aphid management over a longer time scale, it might still be useful to combine lacewings and parasitoids to ensure stable and resilient aphid control.     

Maladaptive behavioural phenotypes in captive‐reared darters (Etheostoma caeruleum,Storer 1845)

The foraging and anti‐predator behaviour of captive‐reared rainbow darters (Etheostoma caeruleum) was compared to their wild‐caught counterparts. Wild‐caught darters responded with appropriate anti‐predator behaviour (reduced foraging activity) when exposed to alarm cues (e.g. stimuli from damaged skin) from both wild‐caught and captive‐reared darters, indicating that the diet in captivity did not inhibit the production of alarm cues. Captive‐reared individuals did not change their level of activity when exposed to alarm cues; however, their significantly lower baseline activity (movement and prey consumption) makes it unclear as to whether they actually failed to recognize risk. Regardless, captive‐reared darters showed little motivation to feed when food became available (i.e. they made few movements to obtain food) and appeared impervious to chemical cues indicating risk. Exposing captive‐reared individuals to both semi‐natural foraging opportunities and predator‐recognition training before their release is recommended.     

Persistence of Alarm-Call Behaviour in the Absence of Predators: A Comparison Between Wild and Captive-Born Meerkats (Suricata Suricatta)

Performing correct anti‐predator behaviour is crucial for prey to survive. But, are such abilities lost in species or populations living in predator‐free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti‐predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which relaxed selection has taken place. Here we investigated whether captive‐born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to distinguish between faeces of potential predators (carnivores) and non‐predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti‐predator behaviour in terms of alarm‐call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.     

Susceptibility of Dendroctonus simplex to Hypocreales fungi: towards the development of a biological control strategy

The use of Hypocreales fungi against bark beetles is an attractive alternative strategy for biological control in forestry. However, fungal inoculation methods remain a major challenge due to the cryptic behaviour of these beetles. Experiments were conducted to evaluate the susceptibility of adult eastern larch beetles, Dendroctonus simplex, to different isolates of Hypocreales fungi and to assess the efficiency of direct inoculation of fungal conidia using an assisted autodissemination device. Among the nine fungal isolates tested, Beauveria bassiana INRS‐242 was selected as the utmost isolate causing a mortality rate of 64.4% of D. simplex adults within 10 days and having a high conidial viability of 81.7%. Using an assisted autodissemination device, a fungal‐coated pouch was a promising contamination chamber. Once it had fallen onto the fungal‐coated pouch, each D. simplex adult loaded an average lethal dose of 2.1 × 10⁹ conidia, which induced a mortality rate of 98.0%. Our results demonstrated the fungal pathogenicity of B. bassiana INRS‐242 against the eastern larch beetles and pointed out the potential of the assisted autodissemination device as an effective method of conidia inoculation. These findings represent the first step to develop a biological control strategy against D. simplex populations.     

Oddity,predation risk and social decisions in aquatic invertebrates

Group living is widespread across animal taxa, incurring benefits such as increased foraging efficiency or an enhanced chance of surviving a predator's attack. The chances of escaping a predator are often lower for odd‐looking individuals, as these are detected at a higher rate than uniform looking group members. While this “oddity effect” shall operate in animals differing in any given phenotype, including colour, size or species identity, it has been experimentally tested mainly for odd‐coloured individuals. We examined the oddity effect and swarming preferences in two differently sized species of freshwater planktonic crustaceans (large Daphnia magna and small Daphnia pulex). We experimentally investigated whether odd individuals in a swarm of heterospecific Daphnia were more vulnerable to predation by a common predator, the three‐spined stickleback (Gasterosteus aculeatus). Furthermore, Daphnia's swarming preference was tested by giving individuals the opportunity to choose between conspecific/heterospecific odour and a neutral control. In contrast to the predictions of the oddity effect, odd individuals were not always preyed on earlier; instead three‐spined stickleback preferentially predated large, more nutritious individuals. Daphnia of both species reacted towards the perception of con‐ and heterospecifics odours. While D. pulex generally avoided the smell of other daphnids, D. magna avoided conspecifics but tended to prefer heterospecifics over the neutral control. These findings provide new insights into swarming strategies and social preference of an invertebrate and how this behaviour can influence predation risk.     

Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

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Orientation behavior of Propylaea japonica toward visual and olfactory cues from its prey–host plant combination

The lady beetle Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) is an important predator of aphids in agroecosystems. The inundative release of coccinellid beetles can be an effective biological control strategy. An understanding of how biological control agents perceive and use stimuli from host plants is the key to successfully implement commercially produced predators. Here, we studied the relative role of visual and volatile cues. Dual‐choice assays using foraging‐naïve and foraging‐experienced P. japonica adults were conducted using cotton plants [Gossypium hirsutum L. (Malvaceae)] with or without infestation by the cotton aphid, Aphis gossypii (Glover) (Hemiptera: Aphididae). Overall, experienced beetles were more attracted than naïve beetles toward cues associated with aphid‐infested plants. Experienced beetles were also more responsive to olfactory cues compared with naïve beetles. Both foraging‐naïve and ‐experienced lady beetles integrate olfactory and visual cues from plants infested with aphids, with an apparently greater reliance on olfactory cues. The results suggest that foraging experience may increase prey location in P. japonica.