Will Climate Change Affect Insect Pheromonal Communication?
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Available online at www.sciencedirect.com ScienceDirect Will climate change affect insect pheromonal communication? 1 2 1 Antoine Boullis , Claire Detrain , Fre´ de´ ric Francis and 1 Franc¸ois J Verheggen Understanding how climate change will affect species interactions mediated by plant secondary metabolites interactions is a challenge for all branches of ecology. We have [3,4 ]. only limited understanding of how increasing temperature and atmospheric CO2 and O3 levels will affect pheromone- Communication between insects relies mainly on semi- mediated communication among insects. Based on the ochemicals, which are organic molecules involved in the existing literature, we suggest that the entire process of chemical interactions between organisms [5]. They in- pheromonal communication, from production to behavioural clude pheromones (intraspecific communication) and alle- response, is likely to be impacted by increases in temperature lochemicals (interspecific communication). Pheromones and modifications to atmospheric CO2 and O3 levels. We argue have a variety of important roles, especially related to that insect species relying on long-range chemical signals will foraging, aggregation or sexual behaviour [6]. Using be- be most impacted, because these signals will likely suffer from haviour-changing pheromones (named releaser phero- longer exposure to oxidative gases during dispersal. We mones) is central to integrated pest management (IPM) provide future directions for research programmes [7], so predicting the impact of climate change on IPM investigating the consequences of climate change on insect programmes depends on understanding the impact of pheromonal communication. changes in related abiotic parameters on insect pheromon- Addresses al communication. However, few studies have focused on 1 Entomologie Fonctionnelle et Evolutive, Gembloux Agro-Bio Tech, how changes in climate will disturb each stage in the Universite´ de Lie` ge, 2 Passage des De´ porte´ s, 5030 Gembloux, Belgium pheromone pathway from emitters to receivers (Figure 1). 2 Service d’Ecologie Sociale, Universite´ libre de Bruxelles, Campus de la Plaine, Boulevard du Triomphe, 1050 Brussels, Belgium A pheromone’s long journey Biosynthesis Corresponding author: Verheggen, Franc¸ois J. ([email protected]) Most insect pheromones are synthesised de novo and secreted in specialised glandular tissues, regulated by Current Opinion in Insect Science 2016, 17:87–91 various enzymatic activities [8,9]. Others are sequestered This review comes from a themed issue on Global change biology and/or derived from dietary precursors and depend on the nutritive quality of the diet. Elevated temperatures will Edited by Vladimir Kosˇ ta´ l and Brent J Sinclair likely have pronounced effects on pheromone biosynthe- sis. Because insects are ectothermic and poikilothermic, changing their body temperature will influence enzymatic http://dx.doi.org/10.1016/j.cois.2016.08.006 activities [10], and impact pheromone biosynthesis both 2214-5745/# 2016 Elsevier Inc. All rights reserved. quantitatively and qualitatively. For example, tempera- ture modifies the ratio of compounds in the sex phero- mone of the potato tuber worm moth Phthorimaea operculella [11]. Moths (Lepidoptera: Heterocera) differ- entially use the same precursors to synthesise different pheromone components, thanks to a wide variety of Introduction enzymes (i.e. oxidase, desaturases, reductase), allowing th Since the 19 century, the atmospheric concentration of specific recognition [12]. Although these insects can per- greenhouse gases, particularly carbon dioxide (CO2), have ceive a wide range of pheromone components, the activa- drastically increased causing changes to environmental tion of neurons in their macroglomerular complexes, and parameters at a global scale, including temperature [1]. the elicitation of relevant behavioural responses, is com- Recent studies now highlight the impact of such modifica- binatorial: it will happen only when the right combination tions on the whole dynamics of life [2]. Through cascade and ratio of components is perceived at the same time [6]. effects, entire ecosystems are being disturbed, impacting the population dynamics of inhabiting species and altering Developmental temperature has a strong influence on adult the ways that they interact with one another. This phe- life history, morphology, and physiology. Furthermore, in nomenon has been well documented for insect–plant some species, pheromone production and availability is www.sciencedirect.com Current Opinion in Insect Science 2016, 17:87–91 88 Global change biology Figure 1 3 Dispersion 2 Emission 4 Perception 1 Biosynthesis 5 Behavioural response Current Opinion in Insect Science Intraspecific chemical communication in insects may be subdivided into five steps that are probably impacted by modifications to atmospheric gas composition and associated raise in ambient temperature. Graphic art by Carolina Levicek. dependent on larval, pupation, and/or adult developmental Emission conditions [8,13,14], hence the effect of abiotic parameters Few studies have specifically investigated how changes in on all the insect life stages is important. In the male temperature and atmospheric gas composition act on beewolf, Philanthus triangulum, an increase of 5 8C in pheromone release. In the moth Striacosta ablicosta, in- the larval rearing temperature led adult males to produce crease in average temperature does not affect the calling more pheromonal secretions [13]. Moreover, warmer rear- behaviour of females, while an increasing variation be- ing conditions led to higher relative amounts of compounds tween photophase and scotophase temperatures alter with high molecular weight. As a consequence, a shift in significantly this behaviour, as also observed in Phyllonor- temperature could weaken intraspecific relationships of ycter junoniella [19]. Ladybird larvae deposit more long- these insect species by reducing the efficiency (i.e. speci- chained hydrocarbons — used as oviposition deterring ficity, activity, timing of production, etc.) of their chemical pheromone — when exposed to rising temperature [20 ]. communication. An increase in atmospheric CO2 concentration reduces the emission rate of the alarm pheromone in pea aphids Increasing atmospheric CO2 concentrations [1] could also (Acyrthosiphon pisum) (Boullis et al., unpublished). affect the biosynthesis of insect pheromones. Changes in CO2 concentrations affect plant biochemistry, including Signal dispersal the synthesis of secondary metabolites [4 ]. Since some After pheromone release by the emitter, volatile pher- phytophagous insect species produce their pheromone omones may be altered by oxidative gases such as ozone components based on precursors taken from their host on their way to the receiver. Most pheromones are simple, plant, we hypothesise that phytophagous insects could be lipophilic and of low molecular weight, which facilitate among the most vulnerable to changes in atmospheric their long-distance dispersal in the air. Other pheromones CO2 concentrations, through cascade effects of CO2 on are heavier molecules, including semi-volatile phero- plant chemistry [15,16 ]. In Holomelina spp. moths, leu- mones and cuticular hydrocarbons (CHC), which are used cine is the starting material for sex pheromone production in short-range or contact communication [6]. Like phyto- [17]. In bark beetles, while pheromones are produced genic volatile organic compounds (VOCs), insect pher- primarily de novo mainly through the mevalonate path- omones made of unsaturated terpenes may be way, some aggregation pheromone components arise from decomposed by ozone [21–23]. Similar terpenes are con- the hydroxylation of host tree-derived secondary metab- stitutive of sexual, aggregation or alarm pheromones in olites [18]. several insect taxa, such as ladybirds [24,25], aphids Current Opinion in Insect Science 2016, 17:87–91 www.sciencedirect.com Climate change and insect pheromones Boullis et al. 89 [26,27], bark beetles [28] and fruit flies [29]. As highlight- with photoperiod that determines the intensity and tim- ed for Drosophila melanogaster, terpenes could lose their ing of various insects’ activities [42,43]. Field studies biological activity after short-term ozone fumigation at related to IPM approaches on several lepidopterans have environmentally-realistic concentrations (ranging from shown that the diel periodicity of their sexual attraction is 40 to 120 ppb) [30]. The lifespan of trail-pheromones modified by both photoperiod and ambient temperature and alarm-pheromones, which act in a short time window [44–46]. Moreover, the seasonal rate of capture by trap and small spatial scale [31,32], may thus be further catching is generally related to the associated tempera- reduced in an ozone-rich atmosphere. In addition to ture, depending on specific seasonal degree-days that the effect of ozone on pheromones, temperature acts insects are subjected to [47,48]. By this logic, an increase on the volatility of semiochemicals. In the case of pher- in global surface temperature may shift the seasonal omones dispersed over long distances such as sex or periodicity of sex-related flights in insects, requiring an aggregation pheromones, temperature changes may mod- adaptation of monitoring and treatment periods against ify the shape of scent plumes and disturb the efficiency of these pest insects. Another example is the impact of insects to reach their target [33]. changing temperatures on ant foraging