Density‐mediated indirect interactions alter host foraging behaviour of parasitoids without altering foraging efficiency

1. Foraging decisions of parasitoids are influenced by host density via density‐mediated indirect interactions. However, in the parasitoid's environment, non‐suitable herbivores are also present. These non‐hosts also occur in different densities, which can affect a parasitoid's foraging behaviour. 2. The influence of non‐host densities can be expressed during the first phase of the foraging process, when parasitoids use plant volatiles to locate plants infested by their host. They may also play a role during the second phase, when parasitoids use infochemicals from the host and plant to locate, recognise and accept the host. 3. By using laboratory and field setups, it was studied whether the density of non‐host herbivores influences these two phases of the foraging behaviour of the parasitoid Cotesia glomerata as well as the parasitoid's efficiency to find its host, Pieris brassicae caterpillars. 4. The findings show that a high non‐host density, regardless of the species used, negatively affected parasitoid preference for host‐infested plants, but that the behaviour on the plant and the total host‐finding efficiency of the parasitoids were not influenced by non‐host density. 5. These results are discussed in the context of density‐mediated indirect interactions.     

Chemical information transfer in freshwater plankton

The structure of aquatic ecosystems is determined by complex interactions among individual organisms at different trophic levels. Although our basic understanding of how top-down and bottom-up processes interact to determine food-web dynamics has advanced, we still lack insights into how complex interactions and feedbacks affect the dynamics and structure of food webs. It is now becoming increasingly clear that, in addition to energy transfer from one trophic level to the other, there is exchange of information between these levels facilitated by the release of infochemicals by the organisms. There is evidence from recent studies that the exchange of chemical information in freshwater ecosystems is likely to play a decisive role in shaping structure and functioning of these systems. Chemical communication among freshwater organisms mediates many aspects of both predation and interspecific competition, which play key roles in determining community structure and ecosystem functioning. For example, consumer-induced defences in phytoplankton and zooplankton include modifications in the characteristics relating to life history, behaviour, morphology and biochemistry. These inducible defences affect trophic interactions by altering predator feeding rates through changes in attack rate or handling time, or both. Also host-specific fungal parasitism in phytoplankton is probably controlled by infochemicals. The motile fungi recognise their host by host-secreted compounds. Until now models describing the functioning of ecosystems mainly considered flows of biomass and energy. Integration of new knowledge about the role of chemical communication in these models may be one of the aims of ecological informatics. In this chapter I discuss how infochemicals may affect the dynamics and structure of planktonic food webs.     

Gastropod grazing on a benthic alga leads to liberation of food‐finding infochemicals

Chemical information transfer is a major agent in the regulation of interspecific and intraspecific interactions in natural ecosystems. One important group of such infochemicals both in terrestrial and aquatic ecosystems are so‐called volatile organic compounds (VOCs) that can evoke behavioral or physiological responses like predator avoidance and mate or host location. In previous work, we have demonstrated that freshwater gastropods utilize VOCs released from benthic algae as food finding cues, although the specific nature of the VOC release and perception were not yet clear. Therefore we tested whether gastropod grazing on biofilms leads to algal cell damage and a subsequent liberation of wounding‐associated VOCs. In bioassays we investigated the algal VOC bouquet level which is necessary to elicit a behavioural response of freshwater gastropods. The results of the liberation experiment showed that gastropod grazing leads to VOCs release. We also found that a certain threshold level of volatiles is necessary for snails to recognise the volatile infochemicals and subsequently respond with a directed foraging behaviour towards the odour. Finally, a calculated mass balance model demonstrated that the grazer mediated VOC release produced a signal concentration that is sufficient to be recognized by conspecifics and utilized as foraging infochemicals. The emission of ecologically relevant volatiles through snail grazing with subsequent attraction of other gastropod grazers to algal biofilms indicates an important but so far understudied chemical signaling mechanism of ecological importance.     

The impact of water pH on association preferences in fish

Acidification of lakes and rivers, as a consequence of anthropogenic interference, can cause fundamental changes to biological and ecological processes. One of the main consequences of a reduction in water pH for aquatic organisms is the disruption of their chemosensory abilities, as the detection of chemical cues underpins a wide range of decision‐making processes; for example, a reduction to low pH has been shown to interfere with predator avoidance and the detection of foraging cues. Moreover, aquatic organisms are known to make widespread use of chemical information to inform their social behaviour, although we have a comparably poor understanding of how this is impacted by water acidification, especially their shoaling behaviour. Using a standard behavioural assay, we therefore investigated the impact of low water pH on the social interactions mediated by diet‐derived chemical cues in three‐spined sticklebacks (Gasterosteus aculeatus), by quantifying social behaviour in water that varied either experimentally or naturally in pH. In both cases, we predicted that association patterns would be disrupted by low pH conditions, as reduced pH has shown to interfere with the perception of chemical cues in other non‐social contexts. Consistent with this prediction, our results demonstrate that an acute, short‐term reduction in water pH caused a breakdown in the diet‐mediated social interaction patterns seen in more alkaline water, although, interestingly, the pattern of associations for fish tested in naturally acidic water was both more complex and in a direction that was precisely contrary to our predictions. Overall, the findings provide insights into the potential effects of an acute reduction in water pH on fish communication and social interaction patterns, which may have implication for various individual, group, population and community‐level processes.     

Plant‐mediated effects of host plant density on a specialist herbivore of Solanum carolinense

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Associational susceptibility in broccoli: mediated by plant volatiles,impeded by ozone

Plant‐emitted volatile organic compounds (VOCs) mediate interactions within a plant community. Typically, receiving a signal from a damaged neighbour enhances the defensive attributes of a receiver plant. The mechanisms underlying plant–plant interactions may be divided into active and passive processes, both of which involve transit of VOCs between plants and are vulnerable to environmental perturbation. Numerous studies have documented between‐plant interactions, but the specific effects on a receiver plant's interactions with herbivores have received little attention. Moreover, the relative contributions of active and passive processes to plant defence and the effects of environmental pollutants on the processes have been largely unexplored. We used a system comprising Brassica oleracea var. italica (broccoli) and the specialist herbivore Plutella xylostella to test whether plants previously exposed to herbivore‐damaged neighbours differed from nonexposed plants in their susceptibility to oviposition. We then investigated the roles of active and passive mechanisms in our observations and whether differences in susceptibility remained under elevated ozone concentrations. Plants exposed to herbivore‐damaged neighbours were more susceptible to oviposition than plants exposed to undamaged neighbours, which indicates associational susceptibility. Mechanistically, active and passive volatile‐mediated processes occurred in tandem with the passive process – involving adsorption of sesquiterpenes to receiver plants – appearing to structure the oviposition response. Exposure to ozone rapidly degraded the sesquiterpenes and eliminated the associational susceptibility. Plant volatiles have typically been thought to play roles in between‐plant interactions and to promote receiver plant defence. Here, we show that receiver plants may also become more susceptible to oviposition and thus more likely to be damaged. Extensive disruption of volatile‐mediated interactions by an atmospheric pollutant highlights the need to consider the pervading environment and changes therein when assessing their ecological significance.     

Volatile affairs in microbial interactions

Microorganisms are important factors in shaping our environment. One key characteristic that has been neglected for a long time is the ability of microorganisms to release chemically diverse volatile compounds. At present, it is clear that the blend of volatiles released by microorganisms can be very complex and often includes many unknown compounds for which the chemical structures remain to be elucidated. The biggest challenge now is to unravel the biological and ecological functions of these microbial volatiles. There is increasing evidence that microbial volatiles can act as infochemicals in interactions among microbes and between microbes and their eukaryotic hosts. Here, we review and discuss recent advances in understanding the natural roles of volatiles in microbe–microbe interactions. Specific emphasis will be given to the antimicrobial activities of microbial volatiles and their effects on bacterial quorum sensing, motility, gene expression and antibiotic resistance.     

信息化合物对昆虫行为的影响

本文综述了来自寄主植物的挥发性物质和同种昆虫或异种昆虫释放的各种信息素及两者的协同作用的信息化合物对昆虫行为的影响。特别强调了寄主植物的气味物质和昆虫信息素协同作用在昆虫寻找寄主、求偶、交配及天敌在寄主识别过程中的重要地位。昆虫对寄主植物的识别是由于识别了植物气味的由一定组分、按照严格比例组成的化学指纹图。昆虫信息素与植物挥发性物质相结合为昆虫寻找求偶、交配场所提供更复杂或更全面的信息。许多昆虫只有在寄主植物或寄主植物气味存在时 ,才能释放性或聚集信息素。天敌在寄主识别、搜索及定位等一系列过程中 ,来自寄主的食料、寄主本身及两者的互作的信息化合物起重要的作用。研究信息化合物对昆虫行为的影响可以探索昆虫各种行为的内在机理 ,更好的了解寄主—昆虫—天敌三层营养关系的相互作用 ,对利用天然活性化合物防治害虫及生物防治提供理论依据     

Ecological impacts of human‐induced animal behaviour change

A growing body of literature has documented myriad effects of human activities on animal behaviour, yet the ultimate ecological consequences of these behavioural shifts remain largely uninvestigated. While it is understood that, in the absence of humans, variation in animal behaviour can have cascading effects on species interactions, community structure and ecosystem function, we know little about whether the type or magnitude of human‐induced behavioural shifts translate into detectable ecological change. Here we synthesise empirical literature and theory to create a novel framework for examining the range of behaviourally mediated pathways through which human activities may affect different ecosystem functions. We highlight the few empirical studies that show the potential realisation of some of these pathways, but also identify numerous factors that can dampen or prevent ultimate ecosystem consequences. Without a deeper understanding of these pathways, we risk wasting valuable resources on mitigating behavioural effects with little ecological relevance, or conversely mismanaging situations in which behavioural effects do drive ecosystem change. The framework presented here can be used to anticipate the nature and likelihood of ecological outcomes and prioritise management among widespread human‐induced behavioural shifts, while also suggesting key priorities for future research linking humans, animal behaviour and ecology.     

Non‐pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid‐induced plant volatiles via jasmonic acid signalling

Beneficial soil‐borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col‐0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant‐mediated interaction between the non‐pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore‐induced plant volatiles. The volatile blend from rhizobacteria‐treated aphid‐infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid‐infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore‐induced volatiles and parasitoid response to aphid‐infested plants is lost in an Arabidopsis mutant (aos/dde2‐2) that is impaired in jasmonic acid production. By modifying the blend of herbivore‐induced plant volatiles that depend on the jasmonic acid‐signalling pathway, root‐colonizing microbes interfere with the attraction of parasitoids of leaf herbivores.     

The effects of asymmetric competition on the life history of Trinidadian guppies

The effects of asymmetric interactions on population dynamics has been widely investigated, but there has been little work aimed at understanding how life history parameters like generation time, life expectancy and the variance in lifetime reproductive success are impacted by different types of competition. We develop a new framework for incorporating trait‐mediated density‐dependence into size‐structured models and use Trinidadian guppies to show how different types of competitive interactions impact life history parameters. Our results show the degree of symmetry in competitive interactions can have dramatic effects on the speed of the life history. For some vital rates, shifting the competitive superiority from small to large individuals resulted in a doubling of the generation time. Such large influences of competitive symmetry on the timescale of demographic processes, and hence evolution, highlights the interwoven nature of ecological and evolutionary processes and the importance of density‐dependence in understanding eco‐evolutionary dynamics.     

Reduction of oviposition time and enhanced larval feeding: two potential benefits of aggregative oviposition for the viburnum leaf beetle

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Intraspecific difference among herbivore lineages and their host‐plant specialization drive the strength of trophic cascades

Trophic cascades – the indirect effect of predators on non‐adjacent lower trophic levels – are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of trophic cascade remains largely unexplored, which limits our understanding of the mechanisms underlying ecological networks. Here we experimentally investigated how intraspecific difference among herbivore lineages specialized on different host plants influences trophic cascade strength in a terrestrial tri‐trophic system. We found that the occurrence and strength of the trophic cascade are strongly influenced by herbivores’ lineage and host‐plant specialization but are not associated with density‐dependent effects mediated by the growth rate of herbivore populations. Our findings stress the importance of intraspecific heterogeneities and evolutionary specialization as drivers of trophic cascade strength and underline that intraspecific variation should not be overlooked to decipher the joint influence of evolutionary and ecological factors on the functioning of multi‐trophic interactions.     

Direct and plant trait‐mediated effects of the local environmental context on butterfly oviposition patterns

Variation in the intensity of plant–animal interactions over different spatial scales is widespread and might strongly influence fitness and trait selection in plants. Differences in traits among plant individuals have been shown to influence variation in interaction intensities within populations, while differences in environmental factors and community composition are shown to be important for variation over larger scales. However, little is still known about the relative importance of the local environmental context vs. plant traits for the outcome of interactions within plant populations. We investigated how oviposition by the seed‐predator butterfly Phengaris alcon on its host plant Gentiana pneumonanthe was related to host plant traits and to local environmental variation, as well as how oviposition patterns translated into effects on host plant fruit set. We considered the local environmental context in terms of height of the surrounding vegetation and abundance of the butterfly's second host, Myrmica ants. The probability of oviposition was higher in plants that were surrounded by lower vegetation, and both the probability of oviposition and the number of eggs increased in early‐flowering and tall plants with many flowers in the three study populations. Flowering phenology, shoot height and flower production were, in turn, related to higher surrounding vegetation. Myrmica abundance was correlated with vegetation height, but had no effect on oviposition patterns. Oviposition and subsequent seed predation by the caterpillars strongly reduced host plant fruit set. Our results show that plant–animal interactions are context‐dependent not only because the context influences the abundance or the behavior of the animal interactor, but also because it influences the expression of plant traits that affect the outcome of the interaction. The results also demonstrate that heterogeneity in environmental conditions at a very local scale can be important for the outcomes of interactions.     

Role of infochemical mediated zooplankton grazing in a phytoplankton competition model

Infochemicals released by marine phytoplankton play important roles in food web interactions by influencing the feeding behavior and selectivity of zooplanktonic predators. Recent modeling efforts have focused on the role of such chemicals as toxic grazing deterrents in phytoplankton competition. However, infochemicals may also be utilized as grazing cues, leading predators to profitable foraging patches. Here we investigate the role of infochemical mediated zooplankton grazing in a standard 3-species phytoplankton competition model, with the aim of further elucidating the ecological role of phytoplankton derived infochemicals. We then extend this to consider a more realistic 4-species model. The models produce a range of solutions depending on the strength of competition and microzooplankton grazing selectivity. Our key result is that infochemical chemoattractants, which increase the susceptibility of the producer to grazing, can provide a refuge for both competing phytoplankton species by attracting carnivorous copepods to consume microzooplankton grazers in a multi-trophic interaction. Our results indicate that infochemicals potentially have important consequences for the dynamics of marine food webs.     

Ant cues affect the oviposition behaviour of fruit flies (Diptera: Tephritidae) in Africa

Abstract. Although most studies on fruit fly oviposition behaviour focus on horizontal interactions with competitors and cues from host plants, vertical interactions with predators are poorly documented. The present study provides direct evidence indicating that the oviposition behaviour of the two main mango fruit fly species, Ceratitis cosyra (Walker) and Bactrocera invadens Drew‐Tsurata & White, is affected by secretions of the dominant arboreal ant Oecophylla longinoda (Latreille). When offered ant‐exposed and unexposed mangoes in the absence of the ants, both fly species are reluctant to land on ant‐exposed fruits and, when having landed, often take off quickly and fail to oviposit. The number of puparia collected from unexposed mangoes is approximately eight‐fold higher than from ant‐exposed ones. The results obtained from laboratory experiments and field observations confirm that adult fruit flies are more affected through repellence by ant cues than by direct predation. The use of cues by fruit flies in predator avoidance has implications for evolutionary ecology, behavioural ecology and chemical ecology.     

Maintenance of body‐size variation and host range in the orange‐tip butterfly: evidence for a trade‐off between adult life‐history traits

1. The evolution of host range and preference in phytophagous insects is driven by a female's oviposition choice impacting her offspring's fitness. Analysis of the fitness of progeny on different host plants has commonly been restricted to the performance of immature stages. However, since host use can affect adult size, it is important to measure the ongoing effects of host choice on the resulting imagines. 2. The orange‐tip butterfly, Anthocharis cardamines, shows a strong preference for two host plants in Britain, Alliaria petiolata and Cardamine pratensis, which affect body size. Whilst females exhibit a strong positive size–fecundity relation, the impact of body‐size alteration is unknown in males. In this study, fitness effects of host plant choice for male A. cardamines were examined. 3. Males reared on C. pratensis were smaller and emerged earlier than those reared on A. petiolata, and early‐season males were smaller than late‐season ones in the field. Interestingly, regression analysis indicated that the earlier emergence of small males was a host‐mediated rather than a size‐mediated effect. Small size was associated with reduced male dispersal in a semi‐isolated wild population over a 3‐year period. 4. It is proposed that the earlier emergence associated with C. pratensis has evolved in response to depressed dispersal in isolated/semi‐isolated populations associated with this patchily distributed host. We suggest that adult life‐history traits are important for the maintenance of host range in this species, and offer a critique of Courtney's earlier hypothesis that host range is maintained by time‐limited oviposition behaviour.     

Size‐based ecological interactions drive food web responses to climate warming

Predicting climate change impacts on animal communities requires knowledge of how physiological effects are mediated by ecological interactions. Food‐dependent growth and within‐species size variation depend on temperature and affect community dynamics through feedbacks between individual performance and population size structure. Still, we know little about how warming affects these feedbacks. Using a dynamic stage‐structured biomass model with food‐, size‐ and temperature‐dependent life history processes, we analyse how temperature affects coexistence, stability and size structure in a tri‐trophic food chain, and find that warming effects on community stability depend on ecological interactions. Predator biomass densities generally decline with warming – gradually or through collapses – depending on which consumer life stage predators feed on. Collapses occur when warming induces alternative stable states via Allee effects. This suggests that predator persistence in warmer climates may be lower than previously acknowledged and that effects of warming on food web stability largely depend on species interactions.     

Volatile and non-volatile fungal oxylipins in fungus-invertebrate interactions

Eight-carbon volatiles are characteristic of the odour profile of many filamentous fungi. They derive from enzymatic or non-enzymatic lipid oxidation and are thus termed volatile oxylipins. Collectively, non-volatile and volatile fungal oxylipins are important hormone-like factors that regulate the phenotypic status of a fungus, i.e. growth, morphological differentiation and secondary metabolite production. Given this intimate link between oxylipin formation and phenotypic change, we propose that the release of volatile oxylipins is an important means by which fungi may influence the course and outcome of interactions with animals. Such invertebrate – fungus interactions are intricate inter–kingdom relationships where either one depends on the other, or both on each other, where one is to the others benefit or detriment – eventually having even consequences on third parties and thus influencing whole foodwebs. In this review, we first highlight the connections between oxylipin formation and fungal phenotypic changes, how they affect invertebrate interactions and vice versa. We then expand this by implementing eight-carbon volatiles as infochemicals. Infochemicals are cues or signals perceived by the invertebrates' chemical senses, that are to the invertebrates' or the fungus’ benefit or detriment, through the behavioural responses they elicit. We point out, with various examples, that there is a strong analogy between fungus-invertebrate interactions mediated by fungal eight-carbon volatiles and plant-herbivore interactions mediated by six-carbon green-leaf volatiles released from wounded or stressed plants.