Oecologia (2009) 160:411–420 DOI 10.1007/s00442-009-1318-9
CONCEPTS, REVIEWS AND SYNTHESES
Effects of air pollution on biogenic volatiles and ecological interactions Quinn S. McFrederick Æ Jose D. Fuentes Æ T’ai Roulston Æ James C. Kathilankal Æ Manuel Lerdau
Received: 27 October 2008 / Accepted: 18 February 2009 / Published online: 8 April 2009 Ó Springer-Verlag 2009
Abstract Chemical signals play important roles in ecological interactions but are vulnerable to perturbation by air pollution. In polluted air masses, signals may travel shorter distances before being destroyed by chemical reactions with pollutants, thus losing their specificity. To determine which scent-mediated interactions are likely to be affected, we review existing literature to build a picture of what chemicals are commonly found in such interactions and the spatial scales at which interactions occur. We find that pollination, attraction of natural enemies of plant pests, aggregation pheromones, and mate attraction are likely to be affected. We review the scant literature on this topic and extend the hypothesis to include heretofore unexplored interactions. New research should investigate whether air pollution deleteriously affects populations of organisms that rely on scent plumes. Additionally, we need to investigate whether or not breakdown products created by
Communicated by Carlos Ballere´. Q. S. McFrederick M. Lerdau Department of Biology, University of Virginia, P.O. Box 400328, Gilmer Hall, Charlottesville, VA 22904, USA e-mail:
[email protected] J. D. Fuentes T. Roulston J. C. Kathilankal M. Lerdau (&) Department of Environmental Sciences, University of Virginia, Clark Hall, Charlottesville, VA 22904, USA e-mail:
[email protected] J. D. Fuentes e-mail:
[email protected] T. Roulston e-mail:
[email protected] J. C. Kathilankal e-mail:
[email protected]
the reaction of signaling chemicals with pollutants can provide usable signals, and whether or not there has been adaptation on the part of scent emitters or receivers to use either breakdown products or more robust chemical signals. The proposed research will necessarily draw on tools from atmospheric science, evolutionary biology, and ecology in furthering our understanding of the ecological implications of how air pollution modifies the scentscape. Keywords Scent plumes Pollinators Ecosystem services Biogenic hydrocarbons Global change
Introduction For many organisms, scent plumes provide more reliable and longer range cues than visual signals; these plumes can travel hundreds of meters from sources and be recognizable at concentrations in the low parts per billion (Dobson 1994). Unlike visual cues, scent plumes may circumvent physical barriers. Chemical signals also differ from visual cues in that they can be transformed by chemical reactions, while visual signals are limited only by light, obstruction, and the visual acuity of receivers. Like a physical landscape cluttered with visual stimuli competing for attention, the ‘‘scentscape’’ is muddled with odors of different types and strengths arising from a wide variety of sources. Thus, in order to successfully follow an odor, recipients must distinguish the cue at different concentrations among various background scents and navigate upstream to the source. To scent-challenged humans, such a task is daunting; to scentdependent organisms, however, it is a way of life. The advent of two technologies, in particular, has allowed ecologists to gain a richer understanding of
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chemically-mediated ecological processes. Gas chromatography–mass spectrometry came about in the late 1950s and allowed identification of the chemicals that comprise scent plumes (Gohlke 1959; Williams 1983). Electrophysiological methods such as electroantennograms (Schneider 1957), which were coupled with gas chromatography in the late 1960s (Moorhouse et al. 1969), allow detection of chemicals that elicit responses in insect chemoreceptors. Myriad volatile organic compounds (hereafter VOCs) have been identified, and their effects on behavior, physiology, and ecology are being unraveled (Theis and Lerdau 2003). Insect detection thresholds of these VOCs can be in trace amounts; the lowest levels yet recorded being only about six molecules on one insect antenna (Angioy et al. 2003). Although scent as a communication signal is ubiquitous in ecological communities and essential for a range of interactions, it also displays sensitivity to environmental perturbation that is unique among biological signals. Scent molecules contain reduced carbon, and this carbon is susceptible to atmospheric oxidation by compounds such as ozone (O3), the hydroxyl radical (HO), and the nitrate radical (NO3) (Fuentes et al. 2000). The oxidation of biogenic scent molecules produces secondary compounds, some of which may have similar chemical structures, despite coming from different parent compounds (Fuentes et al. 2000; McFrederick et al. 2008). This perturbation of scent signals hastens the destruction and also changes the identity of the scent plume, both of which can affect the probability of detection by intended or unintended recipients. We briefly review the natural history of the ecological interactions mediated by scents and the atmospheric chemistry of the volatile hydrocarbons involved in these interactions. We then highlight how anthropogenic increases in atmospheric oxidants affect these signals. Though this interaction between signaling molecules and anthropogenic pollutants has been examined in the context of certain tritrophic interactions and plant pollinator communication, we extend this idea to other ecological interactions. We find several interactions that are likely to be affected by this perturbation but have not been studied in this context, and we identify scent-mediated interactions that are less likely to be affected by pollution. Finally, we suggest areas for research in the future.
Ecology of the scentscape Scents play crucial roles in the ecological processes modulating ecosystems (Table 1). Pollinators use floral scents to navigate at both long and short spatial scales (Dobson 1994). Over short distances (within 1 m), pollinators such
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as bees may use floral fragrances to decide whether flowers are rewarding enough to visit (Dobson 2006; Raguso 2001), while night-flying moths have been shown to orient to flowers by scent alone (Dobson 1994). Scents play additional roles in plant–herbivore interactions: as direct defenses against herbivores by serving as repellants (Kessler and Baldwin 2001), as induced attractants of parasitoids and predators of herbivores (Pare and Tumlinson 1999), and as plumes exploited by herbivores (Theis 2006). In predator–prey interactions, scents serve to indicate presence of both prey (Conover 2007) and predators (Apfelbach et al. 2005), as alarm pheromones (Dicke and Grostal 2001), and as defenses against predators (Millar 2004). Many competitive interactions are mediated by scents; scent markings at territorial boundaries are composed of VOCs (Hurst and Beynon 2004). Many insects, notably many moths, use scents to advertise to mates, and males are known to navigate over long distances ([100 m) to find emitting females (Carde and Haynes 2004). Sex pheromones can be made up of unique compounds or unique blends of components, and receptors can be accordingly specialized (Byers 2006; Kurtovic et al. 2007). Scent is also involved in many social interactions. Aggregation pheromones are used by animals such as bark beetles to attract a critical mass of beetles to a host tree. This quorum is necessary to overcome the host’s defenses (Byers 1995). Social insects use pheromones to modulate the behavior and physiology of colony mates (primer pheromones), to create scent trails between the colony and food sources, and for nestmate recognition (do Nascimento and Morgan 1996; Vander Meer and Morel 1998). Finally, though still controversial, there is growing evidence that volatiles can serve as signals within and among plants (Frost et al. 2008). Within the same plant, VOCs from damaged parts have been shown to induce and prime defenses in uninjured parts (Frost et al. 2007; Heil and Silva Bueno 2007). Several studies have demonstrated that volatiles released from conspecifics serve to prime defenses of nearby, uninjured plants (reviewed in Frost et al. 2008; Karban et al. 2000; Kost and Heil 2006).
Chemistry of the scentscape in the presence of pollution Chemical signals are composed of hydrocarbons, and the bonds between carbon atoms in the molecules influence their reactivity (Seinfeld and Pandis 1996). These hydrocarbons are reactive with HO, O3, and NO3 (Atkinson 1994). Though HO, O3, and NO3 have long resided in the lower atmosphere, their concentrations have been increasing or changing due to anthropogenic precursor emissions (Fiore et al. 2002; Prinn et al. 2001). One time series of data shows a fivefold increase of O3
Sex pheromones
Reproduction
Alkanes, alkenes
Defensive secretions
Alcohols, aldehydes and acetates
Terpenes, benezonoids, ketone
Ketones, terpenes, aldehydes
Alarm pheromone
Territorial marking
Aldehydes, monoterpene alcohols
Alcohols, benzenoids (aromatics), aldehydes
Herbivore attractants
Scents as signals of prey availability/ predator presence
Terpenes, alcohols, aldehydes and phenolics
Indirect defenses
Competition
Predator-prey interactions
Terpenes
Direct defenses
Monoterpenes, benzenoids (aromatics) and sesquiterpenes
Nocturnal
Herbivory
Monoterpenes, benzenoids (aromatics) and sesquiterpenes
Diurnal
Pollination
Common volatile chemicals
Sub-category
Interaction
Table 1 Summary of interactions mediated by chemicals
Best studied in moths, which use pheromone plumes to navigate long distances to find females
Mammal territorial signals act at both long and short distances
Defensive secretions act at short scale, in response to perturbation by a predator
Alarm pheromones act at short distances, as warnings to social partners
Predators-prey use olfaction to detect prey/predators at long distances
Herbivore use volatile signals on both long and short scales
Herbivore induced volatile signals work at long ranges
Y tube and cage experiments have shown that direct defenses act at a small scale, as far as we know there is no evidence for long distance effects of direct defenses
Long distance: evidence for attraction of moths
Short scale: influences decisions to visit flower; long distance: evidence for attraction in orchid bees and sexually deceptive pollination
Spatial scale of attraction
(Theis 2006)
Low for short distance interactions; long distance interactions, if they occur, are more vulnerable
High: long distance activity of signal and high reactivity Low for short distance signal; high for long distance signal
Terpenes: HO, O3 NO3
Terpenes: HO, O3, NO3; phenolics: HO, O3, NO3; alcohols: HO; aldehydes: HO, NO3
Aldehydes: HO, NO3; alcohols: HO; acetates: HO
Terpenes: HO, O3, NO3; benzenoids: HO, NO3; ketones: HO
Alkanes: HO, NO3; alkenes: HO, O3, NO3
Ketones: HO; terpenes: HO, O3, NO3; aldehydes: HO, NO3
Aldehydes: HO, NO3; alcohols: HO
Alcohols: HO; aldehydes: HO, NO3; benzenoids: HO, NO3
(Kessler and Baldwin 2001; Kessler and Baldwin 2002; Turlings et al. 1995)
Moderate: scents are important at night but oxidant levels are lower
Terpenes: NO3; benzenoids: NO3
(Ando et al. 2004; Carde and Haynes 2004)
(Brennan and Kendrick 2006; Hurst and Beynon 2004; Novotny et al. 1999)
Low for short distance interactions; high for long distance interactions High: scent is extremely important long distance mate attractant
(Conner et al. 2007; Millar 2004)
(Blum 1996)
Low due to short distance nature of interactions Low due to short distance nature of interactions
(Conover 2007; Kats and Dill 1998)
Moderate: these scents act at long distances, but reaction rates are slightly lower than those of terpenes
(De Moraes et al. 2001; Heil 2004; Vourc’h et al. 2002)
(Dobson 1994; Knudsen et al. 2006)
(Dobson 1994; Knudsen et al. 2006)
Low for short distance interactions; high for long distance interactions
Terpenes: HO, O3; benzenoids: HO
References for volatiles and scale
Potential vulnerability, assessed in this paper
Relative oxidant [rate constant range (cm3 s-1 molecule-1): Atkinson 1994]
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123 Acids
Primer pheromone
Aldehydes, alcohols, acetates
Terpenes, oxygenated hydrocarbons
Scent trails
Within and between plant communication
Alkanes, alkenes
Nestmate recognition
Plant to plant signaling
Terpenes, alcohols
Aggregation pheromone
Social interactions
Common volatile chemicals
Sub-category
Interaction
Table 1 continued
Herbivore induced plant volatiles have been indicated in priming plant defenses, though this is most likely to occur at short scales
Retinue or primer pheromones control colony member’s behavior, and act at short scales
Trails laid on ground (for example ant trails) are short scale signals, while aerial trails may act on larger distances
Nestmate recognition occurs at short distances
Insects such as bark beetles (Ips spp.) use pheromones to create a quorum
Spatial scale of attraction
Low, these interaction occur at the colony scale
Absent for within plant signaling, low for between plant signaling due to short spatial scale
Aldehydes, alcohols, acetates
Low for terrestrial trails, greater for aerial trails
Acids: HO
Terpenes: HO, O3 NO3; oxygenated hydrocarbons: HO
Low: the interactions take place on short scales
High: pheromones act at distances of 100 meters or more
Terpenes: HO, O3, NO3; alcohols: HO Alkanes: HO, NO3; alkenes: HO, O3, NO3
Potential vulnerability, assessed in this paper
Relative oxidant [rate constant range (cm3 s-1 molecule-1): Atkinson 1994]
(Frost et al. 2008)
(Keeling et al. 2004)
(Keeling et al. 2004)
(Dani et al. 2001; Gordon et al. 1993)
(Byers 1995; Wermelinger 2004)
References for volatiles and scale
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Table 2 Classes of volatiles and their relevant oxidants with range of rate constants for each class Rate constant HO
Rate constant NO3
10-15-18
10-10-12
10-10-16
-11-12
10-15-16
-10-13
-11-12
Benezenoids Phenolics
10 -19
10
10
10
Alcohols
10-11-13
Aldehydes
10-11
10-15
Alkanes
10-11-15
10-16-17
10-10-12
10-10-16
Alkenes Acetates
10-15-18
10
1
0.1
0
25
50 75 [O3] in ppb
100
10
-11-13
10
Oxygenated hydrocarbons
10-10-12 -12-13
10
Rate constants represent the speed at which volatiles react with each oxidant and are reported in cm3 s-1 molecule-1. Rate constant values are from Atkinson (1994)
b 100
10
1 0
5x106 10x106 15x106 20x106 -3 [HO] in molec cm
1000
c Lifetime in minutes
from the pre-industrial era through the early 1990s (Marenco et al. 1994). In the presence of sunlight, O3 is produced by reactions involving nitrogen oxides, carbon monoxide, and hydrocarbons. HO concentrations are sustained by photolysis of O3 along with other compounds such as nitric and nitrous acid. During the daytime in the rural atmosphere, O3 and HO thus share a pronounced pattern. HO concentrations exist in the atmosphere at trace levels, reaching only fractions of parts per trillion (Prinn et al. 2001). The high reactivity of HO means that it is the major driver of atmospheric chemistry despite its lower concentration when compared to O3 and NO3. NO3 is formed from the reaction of O3 with nitrogen dioxide, but is rapidly destroyed by photolysis and is therefore nearly absent during the day, except within plant canopies (Fuentes et al. 2007). Nighttime concentrations of NO3 can reach 20 parts per trillion (Fuentes et al. 2000). Pollutants react with hydrocarbons in one of two ways: through hydrogen atom abstraction and through addition of HO, O3, or NO3 (Fuentes et al. 2000). These reactions result in loss of signal quantity and quality. Each VOC species has a unique reaction rate constant with each of the three pollutants (Atkinson 1994; summarized in Table 2), and will therefore decrease in quantity depending on this constant. Rate constants reflect how quickly reactions between two compounds take place; they are a function of the activation energy required for the reaction to proceed and the geometry of the reacting molecules (Seinfeld and Pandis 1996). The destruction rate of VOCs depends not only on the rate constant of the VOC with air pollutants, but also on the concentration of the air pollutants in the atmosphere (Fig. 1). This concentration dependence occurs
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1000
-12
Ketones Acids
Lifetime in minutes
Terpenes
Rate constant O3
Lifetime in minutes
Volatile chemical
a
100
100
10
1
0
4x106 8x106 -3 [NO3] in molec cm β-ocimene Benzaldehyde
12x106
β-caryophyllene β-pinene
Fig. 1 The destruction rates of volatile organic compounds (VOCs) in relation to concentrations of HO, O3, and NO3
because pollutants need to collide with VOCs in order for the two gases to react (Seinfeld and Pandis 1996). Signal quality may be degraded in two inter-connected ways: loss of signal specificity and changes in the ratios of the VOCs that compose the signal. The reaction of different VOCs with air pollutants can yield similar breakdown products, and such new compounds may themselves be volatile (Fuentes et al. 2000). For example, the reactions involving b-myrcene and b-ocimene with HO and O3 produce three common compounds: acetone, 4-vinyl4-pentanal, and 4-methyl-3,5-hexadienal (McFrederick et al. 2008; Reissell et al. 2002). Such common reaction products
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(i.e., 4-vinyl-4-pentanal and 4-methyl-3,5-hexadienal) are also volatile and may therefore serve as signals. However, the reaction products may be less abundant and exhibit different fragrances and volatilities compared to the parent compounds. It is important to note that the reactions between specific floral volatiles (e.g., b-myrcene, b-ocimene) and pollutants occur at different rates, with the result that oxidation reactions yield changes in the ratios of the compounds that comprise a scent plume, as well as the production of common products. Therefore, in a floral scent blend, the relative concentration of different parent volatiles and their breakdown products changes as reactions with pollutants occur. This consideration is important as receptors ordinarily respond to mixture-specific scents (Bruce et al. 2005). For scent recipients, this loss of signal quality and quantity may mean that the signal becomes unrecognizable. This loss may be particularly significant if recipients are signal specialists and have evolved specific receptors to the biogenic signal, as is the case with receptors of many insect sex pheromones (Hildebrand and Shepherd 1997; Kurtovic et al. 2007).
Importance of spatial scale VOC-mediated interactions that occur between organisms in close proximity are less likely to be vulnerable to perturbation by air pollution. If the time between signal emission and reception is brief, there will be few opportunities for VOCs to contact and react with pollutants. Therefore, short-range (0–10 m) interactions are less likely to be affected by pollution, unless the volatiles involved are extremely reactive. One example of this is aphid alarm pheromone, which acts on a short scale and was not negatively affected by experimentally elevated O3 levels (Mondor et al. 2004). On the other hand, VOCs involved in long-range (which we define as from ten to hundreds of meters) interactions can be exposed to pollutants for longer periods of time. This indicates that when pollutants are in elevated concentrations, pollutants and volatiles are more likely to collide and react. The vulnerability of long distance scentmediated interactions therefore hinges on the reactivity of the VOCs involved. Highly reactive scent plumes involved in long distance interactions are at risk of degradation by air pollution.
Reaction rate controls Atmospheric warming and associated anthropogenic emissions of pollutant precursors are likely to affect the destruction of VOCs. The same anthropogenic processes responsible for carbon dioxide emissions (e.g., fossil fuel
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burning) often lead to increases in nitrogen oxide emissions, which, in turn, can augment ambient HO, O3, and NO3 concentrations (IPCC 2007). Numerical model simulations (Wu et al. 2008) show that climate change and anthropogenic emissions of ozone precursors for the 2000– 2050 period (IPCC 2007) will likely increase O3 and HO levels by 17 and 10%, respectively. We therefore anticipate that increased air pollution levels will cause increasing destruction of VOC signals. It important to recognize that numerical models predict that, in the twenty-first century, HO levels can change from –18 to ?5% depending on the precursor emission scenarios (IPCC 2007, p.147).
Vulnerability of interactions To determine the vulnerability of the different scent mediated interactions, we used existing literature to obtain a broad estimate of the scale of interaction and the classes of the chemicals involved (Table 1), along with their reaction rates (Table 2). It should be noted that there is considerable variation in the exact chemical make-up of scent plumes within each category and that the effective distances of these plumes have rarely been carefully quantified. We therefore base our classification of long or short distance on what is available in the literature: carefully quantified data where possible or more qualitative statements when quantitative data are lacking. The vulnerability of a specific interaction will depend on the exact chemistry of that interaction (for an illustration of the reactivity of several common VOC signaling species see Fig. 1), along with the scale at which the interaction takes place and the detection threshold of the recipient for the signal. Therefore, this broad view serves as a general guide as to which interactions provide the best opportunities for further study. We identified five scent-mediated interactions that are highly vulnerable to perturbation by air pollution and merit further study: long distance diurnal pollinator attraction, long distance herbivore attraction, natural enemy of plant pest attraction, mate attraction, and aggregation pheromone (Table 1). These interactions all have the key characteristics of acting at long scales and including reactive VOCs in their signaling plumes (Fig. 1). Insect mate attraction is particularly vulnerable, as the reactive signaling molecules are received by the insect with neurons that can be exceptionally narrowly tuned, and small modifications to the structure of the signaling molecule can greatly affect detection (Hildebrand and Shepherd 1997; Liljefors et al. 1984). Nocturnal pollinator attraction and predator and prey detection may both be moderately vulnerable to perturbation, due to lower levels of pollutants at night (Fuentes et al. 2000) and slightly lower reactivity of the signaling molecules, respectively. The vulnerability of
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The hypothesis of air pollutants degrading scent plumes and therefore disrupting scent-mediated interactions has been previously posited (Cape 2007; Vuorinen et al. 2004), but we are aware of only a handful of studies that directly address all or part of this hypothesis (Arndt 1995; Gate et al. 1995; McFrederick et al. 2008; Pinto et al. 2007a, b, c, 2008). Gate et al. (1995) studied the effects of O3, sulfur dioxide, and nitrogen dioxide on host location by a parasitoid. Only fumigation with O3 had any effect on proportion of hosts parasitized or searching efficiency of the parasitoid, with significantly reduced parasitism and searching efficiency found in the O3 treatment when compared to a filtered air treatment. The experiment was not designed in a way that could untangle direct from indirect effects of pollution, but did show that pollution can negatively affect the searching efficiency of parasitoids. Arndt (1995) studied the effect of O3 fumigation on the aggregation pheromone of Drosophila melanogaster. O3 significantly reduced the amount of pheromone and showed a trend towards negatively affecting the attractiveness of the pheromone. McFrederick et al. (2008) used a Lagrangian model to follow floral scent plumes as they move across the landscape. To determine the impact of air pollution on floral scents, the model was executed under four levels of pollution: from unpolluted conditions to circumstances found during high pollution events commonly occurring during summertime conditions in the eastern United States of America. The results indicate that the impact of pollutants can be severe; for relatively clean air only 10% of the original scent was lost to reaction with pollutants at a distance of 250 m from the source, while in polluted air 65–75% of the scent was lost to reaction with pollutants at the same distance [for similar results for a relatively unreactive (benzaldehyde) and reactive (b-caryophyllene) species, see Fig. 2]. The steep decline in signal quantity could affect both the pollinators and the plants that rely on them. A recent series of papers by Pinto and colleagues investigates the impacts of O3 on tritrophic interactions under both laboratory (Pinto et al. 2007a, b) and field settings (Pinto et al. 2008). These studies, on the scales of centimeters to meters and seconds to tens of seconds, suggest that O3 may reduce the abilities of insects to use volatile compounds as infochemicals. Y-tube assays
Percentage change
Existing studies
100
Benzaldehyde
75 50 Scenario-1 Scenario-2 Scenario-3 Scenario-4
25 0
β-Caryophyllene
100 Percentage change
territorial scent marking and direct herbivore defense hinges on the importance of the long distance versus short distance components of the signal, as the long distance signal is more likely to be affected by pollution.
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75 50 25 0
0
400 800 Distance in meters
1200
Fig. 2 Loss of scent with distance of benzaldehyde and b-caryophyllene for four pollution scenarios
showed that parasitoids could still use herbivore-induced plant volatiles to locate hosts in the presence of O3, but, given a choice between intact signals and O3-degraded signals, preferred the intact signal. Pinto and colleagues did not include HO and NO3 in their studies, and did not use scales that would mimic longer-range interactions, so it is difficult to extrapolate their results to make predictions about polluted atmospheres. Their results highlight two (not mutually exclusive) possible mechanisms underlying the O3 effects. The first is that products of the oxidation of emitted chemicals are not as effective signals as the original scents but can still provide some signal. The second possibility is that VOCs that exhibit low reactivity can act as signals when more highly reactive VOCs have been oxidized. This second possibility highlights the importance of including HO in these experiments. Pinto and colleagues proposed that methyl salicylate may provide a robust long distance signal, as it is relatively unreactive with O3. However, methyl salicylate is highly reactive with HO (Atkinson 1994) and is quickly destroyed in an atmosphere containing HO at the concentrations typically observed during O3 episodes. Further studies designed to distinguish among these mechanisms are essential and should also be
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conducted with both O3 and HO to simulate realistic pollution events.
Future research directions The results and ideas discussed above raise several important issues that require empirical efforts at the interface of ecology, evolution, and atmospheric chemistry. First, the basic natural history of insect reactions to gaseous organic and inorganic compounds must continue to be investigated. Second, the impacts of these compounds on organism– organism interactions, e.g., pollination, parasitism, and dispersal, rather than just physiology and behavior, must be understood. Third, we must bear in mind that signal compounds, as they react, form new compounds that may, in turn, serve as novel signals. The signal-activity of these pollutionderived compounds should be investigated from the perspectives of both current effects and evolutionary potentials. More broadly, we must examine the potential for organisms to adapt to pollution-induced changes in the scentscape. While we have focused this paper on the effects of pollutants such as O3 on the concentrations of volatile biogenic signals, there may also be direct effects of pollutants on both signal production and perception. That is, before we can attribute any loss of functioning of scent plumes to signal destruction by pollutants, we need to control for direct effects of pollutants on the reception of chemical signals. Pollutants such as O3 may block olfactory receptor neurons on insect antennae or, in some other way, directly preclude the VOC signal from being detected. For example, O3 may act as an oxidant on antennal surfaces and reduce their sensitivity to biogenic signals, thus raising the detection limit for such signals. It will also be important to understand the ecological implications of changes in signal perception. That is, we need to understand the sensitivity of ecological processes (e.g., pollination or parasitoidism) that depend on the detection of volatile signals to changes in these signals. It may be that processes dominated by generalists that have signal detection thresholds near current ambient concentrations are very sensitive to pollution-induced changes, while processes dominated by specialists with very low detection thresholds are much less sensitive to disruption. Conversely, specialists may have a narrower range of olfactory receptor neurons than generalists and therefore be less able to detect breakdown products. It may be that pollution-induced changes in volatile signals lead to shifts in community composition, but these effects must be studied first in relatively simple pair-wise or tritrophic situations. Finally, it will be important to account for evolutionary change in signal production and detection in response to pollution-mediated changes in atmospheric composition.
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For example, the products of terpene oxidation may themselves become signals if the animal’s detection systems can evolve to recognize them (Theis and Lerdau 2003). Similarly, there may be selection for the biosynthetic rates of signals to increase in response to increased oxidation rates by pollutants. A final possibility is that emitters and receivers may evolve use of more stable VOCs in polluted versus unpolluted atmospheres. As with other aspects of global environmental change, research must proceed along physiological, ecological, and evolutionary fronts simultaneously. Studies in only one of these areas that do not account for the others will be of limited utility from both pure and applied perspectives.
Conclusions Air pollution may be affecting ecosystem functions by interfering with volatile hydrocarbon signals that mediate ecological and receptor behavioral interactions. In polluted air masses, signals may travel shorter distances before being destroyed by chemical reactions with gases such as HO, O3, and NO3. The reactions between different VOCs and air pollutants may lead to some similar breakdown products; even if the breakdown products can be detected by receivers, the specificity of the original signals is likely to be modified. These reactions may affect interactions where long distance cues are important: pollination, attraction of natural enemies of plant pests, aggregation pheromones, and mate attraction. As pest management programs often rely on pheromone baits, such as those used to monitor fruit fly and codling moth populations, pollution could be interfering with human endeavors as well. The scentscape will likely prove to be a rich field of study, incorporating the tools of atmospheric science, evolutionary biology, and ecology in order to understand the implications of anthropogenic change for modern ecosystems. Acknowledgments J.D.F. acknowledges support from the National Science Foundation (grant number ATM-0445012). J.C.K. received support from the Virginia Coastal Reserve (VCR) Long-Term Ecological Research (LTER) to participate in this research (grant number DEB-0621014). The US National Science Foundation supports the VCR-LTER research activities. Thanks to Rob Raguso for help with the historical aspects of this paper and to several anonymous reviewers, as well as Peter Fields, Esther Julier, Stephen Keller, Vijay Panjeti, Dan Sloan. and Dexter Sowell, for comments on an earlier draft. The experiments in this paper comply with the current laws of the country in which they were performed.
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