Ecological functions of volatile organic compounds in aquatic systems

In terrestrial ecosystems, volatile organic compounds (VOCs) are widely acknowledged as an important group of infochemicals. They play a major role in pollinator attraction by terrestrial plants and as insect pheromones. Furthermore, they are the mediating agent of so-called 'tritrophic interactions'. When plants are attacked by herbivorous insects, volatile signal substances are emitted, which act as attractants for parasitoids that kill the herbivores, thereby protecting the plant from herbivory. Despite the generally acknowledged importance of VOCs in terrestrial chemical ecology, their functions in aquatic food webs are largely unknown. VOCs produced by algae and cyanobacteria are a major concern in water processing, since aquatic primary producers are the reason for regularly encountered taste and odour problems in drinking water. Only very recently, research in aquatic chemical ecology has started to investigate possible ecological functions for the production of VOCs by algae and cyanobacteria. Volatile aldehydes released by wounded cells of marine planktonic diatoms seem to act as defensive compounds against herbivorous copepods on the population level. Just recently, it was found that VOCs released from benthic algae and cyanobacteria can be utilised as food and/or habitat finding cues by aquatic invertebrates such as freshwater gastropods and nematodes. Here, I review concepts and recent experimental studies on the ecological functions of such VOCs in aquatic ecosystems. Understanding the factors that lead to the liberation of volatile compounds is an essential prerequisite to properly assessing their ecological functions. It appears that (similar to terrestrial plant-herbivore interactions) VOCs can also play a steering role for both attraction and defence in aquatic ecosystems.     

Petrol exhaust pollution impairs honey bee learning and memory

Volatile organic compounds (VOCs) serve as important infochemicals, mediating several ecological interactions including herbivory and pollination. Atmospheric pollutants including traffic‐related air pollution may impair the detection of VOCs used by insects in insect–plant interactions. We investigated the indirect effect of petrol exhaust pollution on olfactory learning and memory (short and long term) in honey bees. Using appetitive olfactory conditioning, we trained bees to learn one of four floral VOC profiles; linalool, dipentene, myrcene and geranium. VOCs were unpolluted or polluted with exhaust collected from a petrol generator. Exhaust emissions included concentrations of CO (246.07 + 17 ppm), NO (20.50 + 6.90 ppb) and NO2 (20.93 + 0.05 ppb) consistent with those typically encountered in urban areas and near roads. Once bees had learnt the training VOC, we tested whether they could recognise that VOC 1 h, 24 h and 48 h post‐training. Bees took significantly longer to learn polluted VOCs and forgot them faster than unpolluted ones. We also tested the ‘masking’ potential of pollution on floral VOCs. Using gas chromatography mass spectroscopy we noted differences in the chemical profile of polluted versus unpolluted VOCs and tested whether bees could recognise polluted VOCs if trained using unpolluted ones. For several VOCs tested, bees could distinguish between polluted and unpolluted VOCs. Ultimately, our results show that air pollution changes the recognition and retention of floral VOCs by bees which may consequently impact foraging efficiency.     

Eutrophication and Dreissena Invasion as Drivers of Biodiversity: A Century of Change in the Mollusc Community of Oneida Lake

Changes in nutrient loading and invasive species are among the strongest human-driven disturbances in freshwater ecosystems, but our knowledge on how they affect the biodiversity of lakes is still limited. We conducted a detailed historical analysis of the mollusc community of Oneida Lake based on our comprehensive lakewide study in 2012 and previous surveys dating back to 1915. In the early 20th century, the lake had a high water clarity, with abundant macrophytes and benthic algae, and hosted the most diverse molluscan community in New York State, including 32 gastropod and 9 unionid species. By the 1960s, lake turbidity increased during a period of anthropogenic eutrophication, resulting in a 38% decline in species richness and a 95% reduction in abundance of native gastropods grazing on benthic algae. Following the invasion of Dreissena spp. in 1991 and subsequent increases in water clarity, native gastropod species richness expanded by 37% and abundance increased 20-fold by 2012. In contrast, filter-feeding unionids were unaffected by increased turbidity during the period of eutrophication but were extirpated by dreissenids. Through contrasting effects on turbidity, eutrophication and Dreissena spp. have likely driven the observed changes in native grazing gastropods by affecting the abundance of light-limited benthic algae. Given the high species richness and ecological importance of benthic grazers, monitoring and managing turbidity is important in preserving molluscan diversity.     

The consequences of volatile organic compound mediated bacterial and fungal interactions

Microbial interactions via infochemicals are fundamental to the development of spatial distribution and activity variations in ecosystems. Microorganisms produce a wide range of infochemicals, frequently secondary metabolites, most of which are soluble and many volatile. Volatile organic compounds (VOCs) have been identified in soil atmospheres and related to community structure and function. VOC profiles produced by microorganisms are consistent, relating to cultural conditions, environment and inputs, and so to population and function dynamics. VOC-mediated interactions can result in functional responses by the organisms involved that result in selective advantage to some community members. Positive, negative or neutral interactions can occur between a very wide range of soil bacteria and fungi. These effects include both stimulation and inhibition of growth, by 40 and 60%, respectively, and enzyme production. These effects are usually transient, e.g. removal of an antagonist is followed by complete recovery. Up- and down-regulation of gene expression, by mRNA and protein profiling has been demonstrated. VOCs have played an important role during the evolution of microorganisms in the context of their communities. This revised version was published online in August 2006 with corrections to the Cover Date.     

Bacterial volatiles induce systemic resistance in Arabidopsis

Plant growth-promoting rhizobacteria, in association with plant roots, can trigger induced systemic resistance (ISR). Considering that low-molecular weight volatile hormone analogues such as methyl jasmonate and methyl salicylate can trigger defense responses in plants, we examined whether volatile organic compounds (VOCs) associated with rhizobacteria can initiate ISR. In Arabidopsis seedlings exposed to bacterial volatile blends from Bacillus subtilis GB03 and Bacillus amyloliquefaciens IN937a, disease severity by the bacterial pathogen Erwinia carotovora subsp. carotovora was significantly reduced compared with seedlings not exposed to bacterial volatiles before pathogen inoculation. Exposure to VOCs from rhizobacteria for as little as 4 d was sufficient to activate ISR in Arabidopsis seedlings. Chemical analysis of the bacterial volatile emissions revealed the release of a series of low-molecular weight hydrocarbons including the growth promoting VOC (2R,3R)-(-)-butanediol. Exogenous application of racemic mixture of (RR) and (SS) isomers of 2,3-butanediol was found to trigger ISR and transgenic lines of B. subtilis that emitted reduced levels of 2,3-butanediol and acetoin conferred reduced Arabidopsis protection to pathogen infection compared with seedlings exposed to VOCs from wild-type bacterial lines. Using transgenic and mutant lines of Arabidopsis, we provide evidence that the signaling pathway activated by volatiles from GB03 is dependent on ethylene, albeit independent of the salicylic acid or jasmonic acid signaling pathways. This study provides new insight into the role of bacteria VOCs as initiators of defense responses in plants.     

TROPHIC INTERACTIONS IN THE SEA: AN ECOLOGICAL ROLE FOR CLIMATE RELEVANT VOLATILES?1

When attacked by herbivores, land plants can produce a variety of volatile compounds that attract carnivorous mutualists. Plants and carnivores can benefit from this symbiotic relationship, because the induced defensive interaction increases foraging success of the carnivores, while reducing the grazing pressure exerted by the herbivores on the plants. Here, we examine whether aquatic phytoplankton use volatile chemical cues in analogous tritrophic interactions. Marine algae produce several classes of biogenic gases such as non‐methane hydrocarbons, organohalogens, ammonia and methylamines, and dimethylsulfide. The grazing‐induced release of marine biogenic volatiles is poorly understood, however, and its effect on the chemical ecology of plankton and the foraging behavior of predators is essentially unknown. We outline grazing‐induced defenses in algae and highlight the biogenic production of volatiles when phytoplankton are attacked by herbivores. The role of chemical signaling in marine ecology presents several possible avenues for future research, and we believe that progress in this area will result in better understanding of species competition, bloom development, and the structuring of food webs in the sea. This has further implications for biogeochemical cycles, because several key compounds are emitted that influence the chemistry of the atmosphere and global climate.     

Belowground volatiles facilitate interactions between plant roots and soil organisms

Many interactions between organisms are based on the emission and perception of volatiles. The principle of using volatile metabolites as communication signals for chemo-attractant or repellent for species-specific interactions or mediators for cell-to-cell recognition does not stop at an apparently unsuitable or inappropriate environment. These infochemicals do not only diffuse through the atmosphere to process their actions aboveground, but belowground volatile interactions are similarly complex. This review summarizes various eucaryotes (e.g., plant (roots), invertebrates, fungi) and procaryotes (e.g., rhizobacteria) which are involved in these volatile-mediated interactions. The soil volatiles cannot be neglected anymore, but have to be considered in the future as valuable infochemicals to understand the entire integrity of the ecosystems.     

Environmentally‐mediated consumer control of algal proliferation in Florida springs

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Origin of volatile organic compound emissions from subarctic tundra under global warming

Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature‐dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using ¹³CO₂‐labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil–plant–atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The ¹³C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%–44% (Salix) and 60%–68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%–58% (Salix) and 87%–95% (Betula). Analyses of above‐ and belowground ^12/13C showed shifts of C allocation in the plant–soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO₂ and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.     

Practical approaches to plant volatile analysis

Plants emit volatile organic compounds (VOCs) that play important roles in their interaction with the environment and have a major impact on atmospheric chemistry. The development of static and dynamic techniques for headspace collection of volatiles in combination with gas chromatography-mass spectrometry analysis has significantly improved our understanding of the biosynthesis and ecology of plant VOCs. Advances in automated analysis of VOCs have allowed the monitoring of fast changes in VOC emissions and facilitated in vivo studies of VOC biosynthesis. This review presents an overview of methods for the analysis of plant VOCs, including their advantages and disadvantages, with a focus on the latest technical developments. It provides guidance on how to select appropriate instrumentation and protocols for biochemical, physiological and ecologically relevant applications. These include headspace analyses of plant VOCs emitted by the whole organism, organs or enzymes as well as advanced on-line analysis methods for simultaneous measurements of VOC emissions with other physiological parameters.     

Induced defenses of Veronica spicata: Variability in herbivore-induced volatile organic compounds

Plants release volatile organic compounds (VOCs) that have many eco-physiological functions. Induction of plant VOCs is known to occur upon herbivory. Herbivore-induced VOCs are involved in the attraction of predators and parasitoids, a phenomenon known as an indirect defense of plants. We measured the VOC profiles of the wild species Veronica spicata with and without larval feeding and oviposition by the specialist butterfly Melitaea cinxia. V. spicata showed great plasticity when deploying indirect defences. The induction of several ubiquitous terpenoids and green leaf volatiles (GLVs) was associated with larval feeding, whereas the increase of two ketones, 6-methyl-5-hepten-2-one and t-geranylacetone and the suppression of GLVs were associated with oviposition by the butterfly.     

Drought effects on volatile organic compound emissions from Scots pine stems

Tree stems have been identified as sources of volatile organic compounds (VOCs) that play important roles in tree defence and atmospheric chemistry. Yet, we lack understanding on the magnitude and environmental drivers of stem VOC emissions in various forest ecosystems. Due to the increasing importance of extreme drought, we studied drought effects on the VOC emissions from mature Scots pine (Pinus sylvestris L.) stems. We measured monoterpenes, acetone, acetaldehyde and methanol emissions with custom-made stem chambers, online PTR-MS and adsorbent sampling in a drought-prone forest over the hot-dry summer of 2018 and compared the emission rates and dynamics between trees in naturally dry conditions and under long-term irrigation (drought release). The pine stems were significant monoterpene sources. The stem monoterpene emissions potentially originated from resin, based on their similar monoterpene spectra. The emission dynamics of all VOCs followed temperature at a daily scale, but monoterpene and acetaldehyde emission rates decreased nonlinearly with drought over the summer. Despite the dry conditions, large peaks of monoterpene, acetaldehyde and acetone emissions occurred in late summer potentially due to abiotic or biotic stressors. Our results highlight the potential importance of stem emissions in the ecosystem VOC budget, encouraging further studies in diverse environments.     

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.     

Do mussel patches provide a refuge for algae from grazing gastropods?

On rocky shores, cover of macroalgae is often greater growingepibiotically on mussels compared to algae growing directlyattached to rock. A survey of two shores on the east coast ofIreland confirmed that mussel beds contained greater percentagealgal cover and more diverse algal assemblages compared to thoseon rock. The reasons for this difference are not clear. It hasbeen suggested that mussel beds provide a refuge for algae fromgrazing gastropods. Surprisingly, we found no evidence to supportthis. Using wax discs, gastropod grazing patterns were foundto be similar within the mussel beds as on rock. The musselbeds do not appear to provide a refuge for algae from grazingactivity at this scale and we suggest other possible mechanismsfor the prevalence of epibiotic algal cover on mussels. Intertidalgrazers may in fact affect the epibiotic algae on mussels andthereby affect indirectly the persistence of mussel beds. (Received 14 May 2007; accepted 20 October 2007)     

Reduced levels of volatile emissions in jasmonate-deficient spr2 tomato mutants favour oviposition by insect herbivores

Tomato plants release volatile organic compounds (VOCs) following insect or mechanical damage. In this study, the constitutive and wound-induced emission levels of VOCs in suppressor of prosystemin-mediated responses2 (spr2) mutant plants, compromised in linolenic acid (LA) and jasmonic acid (JA) synthesis, and in 35S::prosystemin (35S::prosys) plants, having upregulated direct defence responses, were compared. The spr2 mutants produced constitutively lower levels of VOCs, which were nonetheless increased in response to (a)biotic damage, although at lower levels than wild-type (Wt) and 35S::prosys plants. No significant differences in VOC emissions were detected between the latter two genotypes, thereby suggesting that systemin does not regulate indirect defence responses, whereas differences in fatty acid composition in spr2 plants led to the predominant emission of saturated C6 volatiles in response to wounding. The expression of 1-deoxy-D-xylulose 5-phosphate synthase (DXS2), a key gene involved in VOC synthesis in the chloroplast, was only upregulated in Manduca sexta L.-damaged Wt and 35S::prosys plants. However, its expression was restored in spr2 plants by exogenous LA or JA, suggesting that abated VOC emissions in spr2 plants are correlated with lowered DXS2 expression. Bioassays with two different insects showed that adult females significantly preferred spr2 plants, indicating that lowered levels of VOCs in tomato influence plant selection by insects during oviposition.     

High nutrient availability leads to weaker top‐down control of stream periphyton: Compensatory feeding in Ancylus fluviatilis

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Induced plant defense via volatile production is dependent on rhizobial symbiosis

Nitrogen-fixing rhizobia can substantially influence plant–herbivore interactions by altering plant chemical composition and food quality. However, the effects of rhizobia on plant volatiles, which serve as indirect and direct defenses against arthropod herbivores and as signals in defense-associated plant–plant and within-plant signaling, are still unstudied. We measured the release of jasmonic acid (JA)-induced volatiles of rhizobia-colonized and rhizobia-free lima bean plants (Fabaceae: Phaseolus lunatus L.) and tested effects of their respective bouquets of volatile organic compounds (VOCs) on a specialist insect herbivore (Mexican bean beetle; Coccinellidae: Epilachna varivestis Mulsant) in olfactometer choice trials. In a further experiment, we showed that VOC induction by JA reflects the plant responses to mechanical wounding and insect herbivory. Following induction with JA, rhizobia-colonized plants released significantly higher amounts of the shikimic acid-derived compounds, whereas the emission of compounds produced via the octadecanoid, mevalonate and non-mevalonate pathways was reduced. These changes affected the choice behavior of beetles as the preference of non-induced plants was much more pronounced for plants that were colonized by rhizobia. We showed that indole likely represents the causing agent for the observed repellent effects of jasmonic acid-induced VOCs of rhizobia-colonized lima bean plants. Our study demonstrates a rhizobia-triggered efficacy of induced plant defense via volatiles. Due to these findings, we interpret rhizobia as an integral part of legume defenses against herbivores.     

Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35

Fusarium oxysporum MSA 35 [wild-type (WT) strain] is an antagonistic Fusarium that lives in association with a consortium of bacteria belonging to the genera Serratia, Achromobacter , Bacillus and Stenotrophomonas in an Italian soil suppressive to Fusarium wilt. Typing experiments and virulence tests provided evidence that the F. oxysporum isolate when cured of the bacterial symbionts [the cured (CU) form], is pathogenic, causing wilt symptoms identical to those caused by F. oxysporum f. sp. lactucae . Here, we demonstrate that small volatile organic compounds (VOCs) emitted from the WT strain negatively influence the mycelial growth of different formae speciales of F. oxysporum. Furthermore, these VOCs repress gene expression of two putative virulence genes in F. oxysporum lactucae strain Fuslat10, a fungus against which the WT strain MSA 35 has antagonistic activity. The VOC profile of the WT and CU fungus shows different compositions. Sesquiterpenes, mainly caryophyllene, were present in the headspace only of WT MSA 35. No sesquiterpenes were found in the volatiles of ectosymbiotic Serratia sp. strain DM1 and Achromobacte r sp. strain MM1. Bacterial volatiles had no effects on the growth of the different ff. spp. of F. oxysporum examined. Hyphae grown with VOC from WT F. oxysporum f. sp. lactucae strain MSA 35 were hydrophobic whereas those grown without VOCs were not, suggesting a correlation between the presence of volatiles in the atmosphere and the phenotype of the mycelium. This is the first report of VOC production by antagonistic F. oxysporum MSA 35 and their effects on pathogenic F. oxysporum. The results obtained in this work led us to propose a new potential direct long-distance mechanism for antagonism by F. oxysporum MSA 35 mediated by VOCs . Antagonism could be the consequence of both reduction of pathogen mycelial growth and inhibition of pathogen virulence gene expression.