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• W2895925245 abstract "In order to survive and reproduce, flowering plants must balance the conflicting selective pressures of herbivore avoidance and pollinator attraction. Links between herbivory and reproduction are often attributed to indirect effects of leaf damage on pollination via reductions in floral allocation, or increases in chemical defenses on herbivore-damaged plants. However, the impacts of herbivory on pollinators have the potential to extend beyond initial floral visits when plant defenses impact pollinator health, foraging behavior, and reproductive success. Here, we examine important but underexplored ways in which herbivory may alter floral phenotype and thus impact pollinators. First, we outline genetic and biochemical mechanisms predicted to underlie floral changes following herbivory, as they impact the floral resources (nectar and pollen) sought by pollinators. Next, we discuss how the consumption of secondary compounds might impact pollinator fitness, including carryover effects on subsequent foraging, mating success, and transgenerational effects on offspring. We consider how pollinator health, life history, and coevolutionary history might result in context-dependent impacts of plant defensive chemistry on pollinator fitness. Finally, we call for studies that measure the impact of herbivore-induced plant defenses on the full spectrum of flower visitors, and contrast case studies on conventional pollinators (for example, generalized bees) versus insects whose larvae are herbivores on the same plants that adults pollinate (such as several butterflies and moths). By linking these consequences of herbivory to fitness effects on both herbivores and pollinators, we will better understand how coevolution between plants, herbivores, and pollinators shapes both defensive and reproductive plant traits. In order to survive and reproduce, flowering plants must balance the conflicting selective pressures of herbivore avoidance and pollinator attraction. Links between herbivory and reproduction are often attributed to indirect effects of leaf damage on pollination via reductions in floral allocation, or increases in chemical defenses on herbivore-damaged plants. However, the impacts of herbivory on pollinators have the potential to extend beyond initial floral visits when plant defenses impact pollinator health, foraging behavior, and reproductive success. Here, we examine important but underexplored ways in which herbivory may alter floral phenotype and thus impact pollinators. First, we outline genetic and biochemical mechanisms predicted to underlie floral changes following herbivory, as they impact the floral resources (nectar and pollen) sought by pollinators. Next, we discuss how the consumption of secondary compounds might impact pollinator fitness, including carryover effects on subsequent foraging, mating success, and transgenerational effects on offspring. We consider how pollinator health, life history, and coevolutionary history might result in context-dependent impacts of plant defensive chemistry on pollinator fitness. Finally, we call for studies that measure the impact of herbivore-induced plant defenses on the full spectrum of flower visitors, and contrast case studies on conventional pollinators (for example, generalized bees) versus insects whose larvae are herbivores on the same plants that adults pollinate (such as several butterflies and moths). By linking these consequences of herbivory to fitness effects on both herbivores and pollinators, we will better understand how coevolution between plants, herbivores, and pollinators shapes both defensive and reproductive plant traits. For plants that rely on insect pollinators, herbivory and pollination often result in conflicting selection on plant traits [1Kessler A. Halitschke R. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study.Funct. Ecol. 2009; 23: 901-912Crossref Scopus (187) Google Scholar, 2Knauer A.C. Schiestl F.P. The effect of pollinators and herbivores on selection for floral signals: a case study in Brassica rapa.Evol. Ecol. 2017; 31: 285-304Crossref Scopus (44) Google Scholar]. This link between herbivory and reproduction may reflect direct impacts of herbivory on plant reproductive allocation or may result from indirect effects, such as those mediated by pollinators. Additionally, studies linking herbivore damage to reproduction and/or pollination are hard to synthesize into a general framework because of the different ways that herbivores and pollinators can interact using their shared host plant resources [3Lucas-Barbosa D. Integrating studies on plant-pollinator and plant-herbivore interactions.Trends Plant Sci. 2016; 21: 125-133Abstract Full Text Full Text PDF PubMed Scopus (93) Google Scholar]. The effects of herbivory on reproduction are most obvious when florivores consume flowers or developing seeds [4McCall A.C. Irwin R.E. Florivory: the intersection of pollination and herbivory.Ecol. Lett. 2006; 9: 1351-1365Crossref PubMed Scopus (310) Google Scholar]. However, leaf herbivores can also have direct and indirect effects on reproduction and pollination [5Lucas-Barbosa D. Sun P. Hakman A. van Beek T.A. van Loon J.J.A. Dicke M. Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors.Funct. Ecol. 2016; 30: 431-441Crossref Scopus (49) Google Scholar, 6Mothershead K. Marquis R.J. Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa.Ecology. 2000; 81: 30-40Google Scholar]. Understanding the traits that plants use to attract pollinators while deterring herbivores is crucial to reconciling the factors that facilitate plant–insect coevolution and constrain plant defenses and floral displays (reviewed by [7Johnson M.T.J. Campbell S.A. Barrett S.C.H. Evolutionary interactions between plant reproduction and defense against herbivores.Annu. Rev. Ecol. Evol. Syst. 2015; 46: 191-213Crossref Scopus (66) Google Scholar]). Previous reviews have covered the roles of plant mating systems [8Campbell S.A. Ecological mechanisms for the coevolution of mating systems and defence.New Phyt. 2015; 205: 1047-1053Crossref PubMed Scopus (25) Google Scholar], belowground herbivory [9Barber N.A. Gorden N.L.S. How do belowground organisms influence plant-pollinator interactions?.J. Plant Ecol. 2015; 8: 1-11Crossref Scopus (55) Google Scholar], florivory [4McCall A.C. Irwin R.E. Florivory: the intersection of pollination and herbivory.Ecol. Lett. 2006; 9: 1351-1365Crossref PubMed Scopus (310) Google Scholar] and floral rewards (including nectar and pollen) [7Johnson M.T.J. Campbell S.A. Barrett S.C.H. Evolutionary interactions between plant reproduction and defense against herbivores.Annu. Rev. Ecol. Evol. Syst. 2015; 46: 191-213Crossref Scopus (66) Google Scholar] on pollinator attraction, so we focus on less explored aspects of plant–herbivore–pollinator interactions. First, we discuss how leaf herbivory can alter floral traits important to pollinators, and we outline the predictions and evidence for the mechanisms underlying these changes from the plant perspective. Next, we discuss the consequences of herbivore-induced plant reproductive and floral changes on insect attraction, behavior and fitness. Lastly, we focus on the direct role of leaf defensive cues on pollinator behavior, comparing conventional pollinators with ‘pollinating herbivores’ that sequentially utilize leaf and floral resources during different life stages. We argue that future research should aim to quantify and compare the fitness effects of herbivore-induced secondary compounds (including volatiles) in systems where herbivores and pollinators are tightly linked (that is, different life stages of the same species) versus unlinked (as with different genera or guilds). The proposed links between herbivory and reproduction include energetic trade-offs, genetic factors, and biochemical pathways involving plant hormones (phytohormones) that are important for both defense and flowering. Energetic trade-offs have long been proposed to explain decreases in plant growth and reproduction following costly leaf loss and defensive induction [10Coley P.D. Bryant J.P. Chapin F.S. Resource availability and plant antiherbivore defense.Science. 1985; 230: 895-899Crossref PubMed Scopus (2783) Google Scholar]. Although the overall costs of plant defense or herbivory on plant reproductive allocation are well established in terms of floral number, size and flowering time [11Strauss S.Y. Rudgers J.A. Lau J.A. Irwin R.E. Direct and ecological costs of resistance to herbivory.Trends Ecol. Evol. 2002; 17: 278-285Abstract Full Text Full Text PDF Scopus (674) Google Scholar], these studies are often correlative and have not revealed the mechanism(s) underlying observed reductions in floral traits. Pleiotropy and linkage provide direct genetic mechanisms for changes in floral traits following herbivory when the same genes or transcription factors control both leaf traits and floral defenses. As reviewed by Johnson et al. [7Johnson M.T.J. Campbell S.A. Barrett S.C.H. Evolutionary interactions between plant reproduction and defense against herbivores.Annu. Rev. Ecol. Evol. Syst. 2015; 46: 191-213Crossref Scopus (66) Google Scholar], antagonistic pleiotropy among growth, reproduction and defense can limit a plant’s ability to both defend itself against herbivores and attract pollinators when the same genes mediate attraction for pollinators at the expense of deterring herbivores (and vice versa). Similarly, the biosynthetic pathways that produce and are regulated by phytohormones also link plant defense and reproduction. Two major phytohormones regulating plant defensive responses are jasmonic acid and salicylic acid. Jasmonic acid is thought to play a crucial role in coordinating plant defenses against chewing insects, whereas salicylic acid is presumed to coordinate defense against piercing and sucking herbivores and pathogenic microbes. In addition to their roles in plant defense, jasmonic acid and salicylic acid are both important for floral development and reward traits, including stamen development [12Dobritzsch S. Weyhe M. Schubert R. Dindas J. Hause G. Kopka J. Hause B. Dissection of jasmonate functions in tomato stamen development by transcriptome and metabolome analyses.BMC Biol. 2015; 13: 28Crossref PubMed Scopus (24) Google Scholar], nectar secretion [13Radhika V. Kost C. Boland W. Heil M. The role of jasmonates in floral nectar secretion.PLoS One. 2010; 5: e9265Crossref PubMed Scopus (60) Google Scholar], and flowering time and fruit set [14Rasmann S. Vilas J.S. Glauser G. Cartolano M. Lempe J. Tsiantis M. Pannell J.R. Pleiotropic effect of the Flowering Locus C on plant resistance and defence against insect herbivores.J. Ecol. 2018; 106: 1244-1255Crossref Scopus (8) Google Scholar]. This association between plant defense and flowering provides a mechanistic link between herbivore-induced defensive changes and traits important to pollinator attraction and pollinator fitness. Plant anatomy and physiology may also limit separation of leaf and floral defenses. For example, sugars and secondary compounds travel through the phloem, and correlations between leaf defense and floral defense may indicate metabolite diffusion into floral resources [15Adler L.S. The ecological significance of toxic nectar.Oikos. 2000; 91: 409-420Crossref Scopus (435) Google Scholar]. Lastly, although herbivory and pollination often result in conflicting selection, herbivory combined with flower feeding, risk of nectar robbing or flower microbial attack may lead to correlated selection for defenses in leaves and flowers [15Adler L.S. The ecological significance of toxic nectar.Oikos. 2000; 91: 409-420Crossref Scopus (435) Google Scholar, 16Irwin R.E. Adler L.S. Correlations among traits associated with herbivore resistance and pollination: Implications for pollination and nectar robbing in a distylous plant.Am. J. Bot. 2006; 93: 64-72Crossref Google Scholar]. Regardless of mechanism, plant defensive responses to herbivory alter both herbivore and pollinator attraction. Whereas the effects of plant defenses on herbivore growth and development are well described [17Thaler J.S. Stout M.J. Karban R. Duffey S.S. Jasmonate-mediated induced plant resistance affects a community of herbivores.Ecol. Ent. 2001; 26: 312-324Crossref Scopus (232) Google Scholar], pollinator fitness is often overlooked or only inferred from studies testing the effects of herbivory on plant reproductive traits. Previous research has shown that pollinators generally prefer undamaged plants over damaged plants for foraging [18Kessler A. Halitschke R. Poveda K. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions.Ecology. 2011; 92: 1769-1780Crossref PubMed Scopus (141) Google Scholar] and/or oviposition [5Lucas-Barbosa D. Sun P. Hakman A. van Beek T.A. van Loon J.J.A. Dicke M. Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors.Funct. Ecol. 2016; 30: 431-441Crossref Scopus (49) Google Scholar, 19Reisenman C.E. Riffell J.A. Duffy K. Pesque A. Mikles D. Goodwin B. Species-specific effects of herbivory on the oviposition behavior of the moth Manduca sexta.J. Chem. Ecol. 2013; 39: 76-89Crossref PubMed Scopus (46) Google Scholar]. This decrease in pollinator attraction is likely due to damage-induced changes in floral sensory cues [18Kessler A. Halitschke R. Poveda K. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions.Ecology. 2011; 92: 1769-1780Crossref PubMed Scopus (141) Google Scholar] and energetic rewards. However, these factors are often considered from the plant perspective, by measuring visitation rates and time spent at focal flowers of defended plants. From the pollinator perspective, the fitness consequences of consuming nectar containing secondary compounds or visiting flowers on defended plants are rarely quantified, despite much being known about floral changes in plants following herbivore damage. The established post-herbivory changes, and their mechanisms and implications for pollinators, are summarized in Table 1.Table 1Effects of herbivory on plant reproductive allocation, floral defense, and pollinator behavior.Plant reproductive changes following herbivoryPlant mechanism for the changeImplications for pollinator visitation and pollinator fitnessReduced floral allocation•Smaller flowers•Fewer flowers•Less nectarResources reallocated to defense over reproduction 10Coley P.D. Bryant J.P. Chapin F.S. Resource availability and plant antiherbivore defense.Science. 1985; 230: 895-899Crossref PubMed Scopus (2783) Google Scholar, 11Strauss S.Y. Rudgers J.A. Lau J.A. Irwin R.E. Direct and ecological costs of resistance to herbivory.Trends Ecol. Evol. 2002; 17: 278-285Abstract Full Text Full Text PDF Scopus (674) Google ScholarReduced pollinator visitation 6Mothershead K. Marquis R.J. Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa.Ecology. 2000; 81: 30-40Google ScholarIncreased floral secondary compounds in pollen and nectar•Correlations between leaf and floral defense 15Adler L.S. The ecological significance of toxic nectar.Oikos. 2000; 91: 409-420Crossref Scopus (435) Google Scholar, 20Adler L.S. Wink M. Distl M. Lentz A.J. Leaf herbivory and nutrients increase nectar alkaloids.Ecol. Lett. 2006; 9: 960-967Crossref PubMed Scopus (144) Google Scholar•Selection to avoid floral antagonists•Antimicrobial properties 22Stevenson P.C. Nicolson S.W. Wright G.A. Plant secondary metabolites in nectar: impacts on pollinators and ecological functions.Funct. Ecol. 2017; 31: 65-75Crossref Scopus (155) Google Scholar•Reduced pollinator visitation 18Kessler A. Halitschke R. Poveda K. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions.Ecology. 2011; 92: 1769-1780Crossref PubMed Scopus (141) Google Scholar or time spent per flower•Reduced florivory 4McCall A.C. Irwin R.E. Florivory: the intersection of pollination and herbivory.Ecol. Lett. 2006; 9: 1351-1365Crossref PubMed Scopus (310) Google Scholar or nectar robbing 15Adler L.S. The ecological significance of toxic nectar.Oikos. 2000; 91: 409-420Crossref Scopus (435) Google Scholar•Improved pollinator memory (for example, caffeine) 48Wright G.A. Baker D.D. Palmer M.J. Stabler D. Mustard J.A. Power E.F. Borland A.M. Stevenson P.C. Caffeine in floral nectar enhances a pollinator's memory of reward.Science. 2013; 339: 1202-1204Crossref PubMed Scopus (200) Google Scholar and constancy•Reduced pollinator survival•Protective against natural enemies (such as pathogens 36Palmer-Young E.C. Tozkar C.O. Schwarz R.S. Chen Y.P. Irwin R.E. Adler L.S. Evans J.D. Nectar and pollen phytochemicals stimulate honey bee (Hymenoptera: Apidae) immunity to viral infection.J. Econ. Entomol. 2017; 110: 1959-1972Crossref PubMed Scopus (49) Google Scholar and parasites 37Richardson L.L. Bowers M.D. Irwin R.E. Nectar chemistry mediates the behavior of parasitized bees: consequences for plant fitness.Ecology. 2016; 97: 325-337Crossref PubMed Scopus (50) Google Scholar)Altered volatilesIncreased leaf volatilesTargeted production of compounds that deter herbivores or attract their enemies 39Karpati Z. Knaden M. Reinecke A. Hansson B.S. Intraspecific combinations of flower and leaf volatiles act together in attracting hawkmoth pollinators.PLoS One. 2013; 8: e72805Crossref PubMed Scopus (16) Google ScholarReduced pollinator visitation if compounds are deterrent or unfamiliar to pollinators 18Kessler A. Halitschke R. Poveda K. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions.Ecology. 2011; 92: 1769-1780Crossref PubMed Scopus (141) Google ScholarDecreased floral volatilesReduced allocation available for floral scent productionAltered flowering timeEarly season floweringMay escape later season herbivory with early flowering 49Hoffmeister M. Wittkopper N. Junker R.R. Herbivore-induced changes in flower scent and morphology affect the structure of flower-visitor networks but not plant reproduction.Oikos. 2016; 125: 1241-1249Crossref Scopus (32) Google ScholarPlants may be out of sync with pollinators and have decreased pollinator visitation 11Strauss S.Y. Rudgers J.A. Lau J.A. Irwin R.E. Direct and ecological costs of resistance to herbivory.Trends Ecol. Evol. 2002; 17: 278-285Abstract Full Text Full Text PDF Scopus (674) Google ScholarLate season floweringDelayed flowering 50Thompson K.A. Johnson M.T.J. Antiherbivore defenses alter natural selection on plant reproductive traits.Evolution. 2016; 70: 796-810Crossref PubMed Scopus (16) Google Scholar as a result of decreased plant growth following damage Open table in a new tab Although reductions in floral display or changes in the timing of flowering have clear implications for pollinator attraction, other herbivore-induced changes can convey important information that affects pollinator behavior. Insect pollinators may use visual, olfactory, and chemosensory cues to avoid flowers on damaged plants, but it is not known precisely why they do so. Kessler and Halitschke [1Kessler A. Halitschke R. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study.Funct. Ecol. 2009; 23: 901-912Crossref Scopus (187) Google Scholar] suggested several factors that could affect pollinator attraction or decision making, including reduced nectar and/or pollen quality or quantity, increased predation pressure, and unfamiliar floral volatiles (Table 1). Reductions in the quantity of floral rewards points to decreased reproductive allocation in damaged plants [6Mothershead K. Marquis R.J. Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa.Ecology. 2000; 81: 30-40Google Scholar], underscoring a traditional ‘plant resource limitation’ view (Figure 1A). In contrast, more recent studies of herbivore-induced plant responses suggest that reduced resource quality (for example, increased secondary compounds in nectar or pollen) may result from pleiotropy between leaf and floral defense [1Kessler A. Halitschke R. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study.Funct. Ecol. 2009; 23: 901-912Crossref Scopus (187) Google Scholar, 7Johnson M.T.J. Campbell S.A. Barrett S.C.H. Evolutionary interactions between plant reproduction and defense against herbivores.Annu. Rev. Ecol. Evol. Syst. 2015; 46: 191-213Crossref Scopus (66) Google Scholar, 15Adler L.S. The ecological significance of toxic nectar.Oikos. 2000; 91: 409-420Crossref Scopus (435) Google Scholar, 20Adler L.S. Wink M. Distl M. Lentz A.J. Leaf herbivory and nutrients increase nectar alkaloids.Ecol. Lett. 2006; 9: 960-967Crossref PubMed Scopus (144) Google Scholar] rather than differences in allocation (Figure 1B). We suspect that both quantitative and qualitative responses of plants to herbivory will impact their pollinators. Changes in reward quality are not necessarily less costly to a plant, and may be molded by selection to avoid floral larceny [15Adler L.S. The ecological significance of toxic nectar.Oikos. 2000; 91: 409-420Crossref Scopus (435) Google Scholar] or alter pollinator movement [21Kessler D. Baldwin I.T. Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata.Plant J. 2007; 49: 840-854Crossref PubMed Scopus (231) Google Scholar], with consequences for gene flow [7Johnson M.T.J. Campbell S.A. Barrett S.C.H. Evolutionary interactions between plant reproduction and defense against herbivores.Annu. Rev. Ecol. Evol. Syst. 2015; 46: 191-213Crossref Scopus (66) Google Scholar]. At the same time, these plant changes affect pollinator behavior and performance. The direct negative effects of plant defenses on pollinators can result in altered feeding or flight behaviors and decreased mating success. Prior studies have shown the impact of nectar containing secondary compounds on pollinator behaviors [22Stevenson P.C. Nicolson S.W. Wright G.A. Plant secondary metabolites in nectar: impacts on pollinators and ecological functions.Funct. Ecol. 2017; 31: 65-75Crossref Scopus (155) Google Scholar], including decreased activity in adult bees [23Hurst V. Stevenson P.C. Wright G.A. Toxins induce 'malaise' behaviour in the honeybee (Apis mellifera).J. Comp. Physiol. A. 2014; 200: 881-890Crossref PubMed Scopus (43) Google Scholar] and reduced visitation or time spent at each flower [21Kessler D. Baldwin I.T. Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata.Plant J. 2007; 49: 840-854Crossref PubMed Scopus (231) Google Scholar, 24Bruinsma M. Lucas-Barbosa D. ten Broeke C.J.M. van Dam N.M. van Beek T.A. Dicke M. van Loon J.J.A. Folivory affects composition of nectar, floral odor and modifies pollinator behavior.J. Chem. Ecol. 2014; 40: 39-49Crossref PubMed Scopus (47) Google Scholar]. Flight is energetically costly and nectar containing secondary compounds could decrease energy available for flight or increase the time spent flying between foraging bouts [25Adler L.S. Irwin R.E. Ecological costs and benefits of defenses in nectar.Ecology. 2005; 86: 2968-2978Crossref Scopus (139) Google Scholar], with consequences for predator avoidance, mating success and offspring fitness. Decreased flight time or performance after consumption could reflect direct negative effects on muscle performance or indirect effects of reduced nectar sugar intake and therefore reduced caloric reserves to fuel flight activity. Plant secondary compounds may affect insect mating success if their presence in the larval or adult diets impacts pheromone production and/or perception. Physiological studies on non-pollinating insects demonstrate a link between diet and mating success, and similar mechanisms are likely to operate in pollinating insects. In Drosophila melanogaster, fat content of the larval diet affects female morphological and pheromone traits used by males to select mates [26Schultzhaus J.N. Bennett C.J. Iftikhar H. Yew J.Y. Mallett J. Carney G.E. High fat diet alters Drosophila melanogaster sexual behavior and traits: decreased attractiveness and changes in pheromone profiles.Sci. Rep. 2018; 8: 5387Crossref PubMed Scopus (21) Google Scholar]. In tephritid flies, exposure to plant volatiles increases male sexual signaling and longevity [27Kouloussis N.A. Gerofotis C.D. Ioannou C.S. Iliadis I.V. Papadopoulos N.T. Koveos D.S. Towards improving sterile insect technique: Exposure to orange oil compounds increases sexual signalling and longevity in Ceratitis capitata males of the Vienna 8 GSS.PLoS One. 2017; 12: e0188092Crossref PubMed Scopus (14) Google Scholar]. Thus, plant compounds can impact life history and mating traits in the insects that interact with them. Alternatively, plant compounds can be essential components of mating for insects that consume specific metabolites at the larval stage and modify those compounds into adult mating pheromones. In this case, specialization on host plant species with different chemistry can result in sexual isolation in part due to differences in pheromone production [28Orono L. Paulin L. Alberti A.C. Hilal M. Ovruski S. Vilardi J.C. Rull J. Aluja M. Effect of host plant chemistry on genetic differentiation and reduction of gene flow among Anastrepha fraterculus (Diptera: Tephritidae) populations exploiting sympatric, synchronic hosts.Environ. Entomol. 2013; 42: 790-798Crossref PubMed Scopus (21) Google Scholar]. Quantifying the direct impacts of plant defense on pollinator behavior and fitness will allow us to distinguish between larval, adult, and offspring fitness effects. In addition to the direct mechanisms described above, there are indirect and context-dependent effects of plant secondary compounds on pollinators and their offspring. Larval exposure to leaf secondary compounds may alter adult behavioral or physiological responses to the same compounds (in either leaves or flowers) as the result of carry-over effects or post-pupation memory [29Sharp D.N. Lentz-Ronning A.J. Barron J. Adler L.S. The effect of larval diet and sex on nectar nicotine feeding preferences in Manduca sexta (Lepidoptera: Sphingidae).Fla. Entomol. 2009; 92: 374-376Crossref Scopus (7) Google Scholar, 30Petit C. Le Ru B. Dupas S. Frerot B. Ahuya P. Kaiser-Arnauld L. Harry M. Calatayud P.A. Influence of dietary experience on the induction of preference of adult moths and larvae for a new olfactory cue.PLoS One. 2015; 10: e0136169Crossref PubMed Scopus (18) Google Scholar]. This could result in increased adult sensitivity to — or tolerance of — the same compounds. This difference in ‘preference induction’ may also be context-dependent, whereby memory of larval experiences is contingent on the quality of the food source they encounter earlier in life [31Lhomme P. Carrasco D. Larsson M. Hansson B. Anderson P. A context-dependent induction of natal habitat preference in a generalist herbivorous insect.Behav. Ecol. 2018; 29: 360-367Crossref Scopus (18) Google Scholar]. The effects of secondary compounds in the diet may also persist trans-generationally. Mothers consuming secondary compounds may give rise to smaller or lower quality offspring that are less able to cope with the stresses of secondary compound exposure in their own diet. Similarly, bee pollinators provision offspring with pollen and oils that contain secondary compounds. Larval bee consumption of nicotine (an inducible secondary compound) decreases survival, indicating a cost of provisioning offspring with resources high in certain secondary compounds [32Human H. Archer C.R. du Rand E.E. Pirk C.W.W. Nicolson S.W. Resistance of developing honeybee larvae during chronic exposure to dietary nicotine.J. Insect Physiol. 2014; 69: 74-79Crossref PubMed Scopus (20) Google Scholar]. Understanding whether larval exposure to secondary compounds increases or decreases adult or offspring sensitivity to the same compounds is necessary for determining whether such factors facilitate or constrain plant–insect co-evolution. We expect such outcomes to vary considerably, depending on the degree of host specialization or generalization shown by a given insect species. Prior experience can also influence oviposition preferences for host plant species encountered as larvae [31Lhomme P. Carrasco D. Larsson M. Hansson B. Anderson P. A context-dependent induction of natal habitat preference in a generalist herbivorous insect.Behav. Ecol. 2018; 29: 360-367Crossref Scopus (18) Google Scholar, 33Cahenzli F. Wenk B.A. Erhardt A. Female butterflies adapt and allocate their progeny to the host-plant quality of their own larval experience.Ecology. 2015; 96: 1966-1973Crossref PubMed Scopus (21) Google Scholar], thus impacting offspring environment and fitness. Many flower-visiting Lepidoptera lay their eggs on the host plant that will serve as the initial food source for their herbivorous offspring. Although these effects are generally studied in preferred versus non-preferred hosts or in high versus low nutritional quality plants, the same principles may apply for insects exposed to different levels of secondary compounds in their larval diets. Pollinators may be more likely to lay eggs on defended plants if they encountered highly defended plants as larvae, even if the general trend suggests that pollinators avoid oviposition on damaged plants, either to escape competition or avoid the induced defenses that could decrease offspring success [34De Moraes C.M. Mescher M.C. Tumlinson J.H. Caterpillar-induced nocturnal plant volatiles repel conspecific females.Nature. 2001; 410: 577-580Crossref PubMed Scopus (749) Google Scholar]. Although secondary compounds are generally considered harmful to herbivores, the direct and indirect consequences of secondary compounds on pollinators and their offspring also are context-dependent and can have a net benefit under certain circumstances. Compared with generalist pollinators, specialists are widely predicted to be more tolerant of host plant defenses and are more likely to sequester plant defensive compounds as protection against enemies [35Irwin R.E. Cook D. Richardson L.L. Manson J.S. Gardner D.R. Secondary compounds in floral rewards of toxic rangeland plants: Impacts on pollinators.J. Agric. Food Chem. 2014; 62: 7335-7344Crossref PubMed Scopus (57) Google Scholar]. Even in the absence of sequestration, consumption of defensive compounds can be protective against a variety of natural enemies, including pathogens [36Palmer-Young E.C. Tozkar C.O. Schwarz R.S. Chen Y.P. Irwin R.E. Adler L.S. Evans J.D. Nectar and pollen phytochemicals stimulate honey bee (Hymenoptera: Apidae) immunity to viral infection.J. Econ. Entomol. 2017; 110: 1959-1972Crossref PubMed Scopus (49) Google Scholar]. As a result, some pollinators have shown evidence of consuming plant secondary compounds as a type of ‘self-medication’. For example, bumble bees infected with intestinal parasites preferred foraging from plants with nectar high in iridoid glycosides [37Richardson L.L. Bowers M.D. Irwin R.E. Nectar chemistry mediates the behavior of parasitized bees: consequences for plant fitness.Ecology. 2016; 97: 325-337Crossref PubMed Scopus (50) Google Scholar]. Many studies of transgenerational effects in insects focus on immune system priming and disease, but there is also evidence that maternal and/or paternal consumption of secondary compounds protects offspring from parasites or egg parasitoids [38Woestmann L. Saastamoinen M. The importance of trans-generational effects in Lepidoptera.Curr. Zool. 2016; 62: 489-499Crossref PubMed Scopus (24) Google Scholar]. Therefore, the costs and benefits of consuming plant secondary compounds depend not only on how harmful the compounds are to the insect and whether the insect had prior exposure to the compound, but also on whether consuming secondary compounds or placing offspring on defended plants provides additional defense against enemies. The complexity of interacting factors influencing the effects of plant defense on insect fitness at the community scale makes it difficult to concurrently examine these factors in a lab setting. Oviposition behavior is particularly challenging to measure in an experimental context because insects exhibit different oviposition patterns under lab settings (where oviposition space is limited) than in the field. Flowers host a broad spectrum of associated organisms, ranging from facultative to obligate in their interaction strength, from antagonism to mutualism in their ecological function, and from microbes to vertebrates in their size and phylogenetic affiliation. We seek a broader, more predictive understanding of how herbivore-induced plant responses impact all members of the floral micro-community, and how those impacts propagate across the larger communities to which they belong (see [17Thaler J.S. Stout M.J. Karban R. Duffey S.S. Jasmonate-mediated induced plant resistance affects a community of herbivores.Ecol. Ent. 2001; 26: 312-324Crossref Scopus (232) Google Scholar]). For example, herbivore-induced plant volatiles (Figure 1B) are known to deter further oviposition by herbivores [34De Moraes C.M. Mescher M.C. Tumlinson J.H. Caterpillar-induced nocturnal plant volatiles repel conspecific females.Nature. 2001; 410: 577-580Crossref PubMed Scopus (749) Google Scholar] and to attract their parasitoids and predators [39Karpati Z. Knaden M. Reinecke A. Hansson B.S. Intraspecific combinations of flower and leaf volatiles act together in attracting hawkmoth pollinators.PLoS One. 2013; 8: e72805Crossref PubMed Scopus (16) Google Scholar], but their independent impacts on pollinator behavior have only recently been examined [3Lucas-Barbosa D. Integrating studies on plant-pollinator and plant-herbivore interactions.Trends Plant Sci. 2016; 21: 125-133Abstract Full Text Full Text PDF PubMed Scopus (93) Google Scholar, 5Lucas-Barbosa D. Sun P. Hakman A. van Beek T.A. van Loon J.J.A. Dicke M. Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors.Funct. Ecol. 2016; 30: 431-441Crossref Scopus (49) Google Scholar, 18Kessler A. Halitschke R. Poveda K. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions.Ecology. 2011; 92: 1769-1780Crossref PubMed Scopus (141) Google Scholar, 40Aartsma Y. Bianchi F. van der Werf W. Poelman E.H. Dicke M. Herbivore-induced plant volatiles and tritrophic interactions across spatial scales.New Phyt. 2017; 216: 1054-1063Crossref PubMed Scopus (112) Google Scholar, 41Dong F. Fu X.M. Watanabe N. Su X.G. Yang Z.Y. Recent advances in the emission and functions of plant vegetative volatiles.Molecules. 2016; 21: 124Crossref PubMed Scopus (72) Google Scholar]. Floral and leaf volatiles can have interacting effects on both pollinators and herbivores [15Adler L.S. The ecological significance of toxic nectar.Oikos. 2000; 91: 409-420Crossref Scopus (435) Google Scholar, 20Adler L.S. Wink M. Distl M. Lentz A.J. Leaf herbivory and nutrients increase nectar alkaloids.Ecol. Lett. 2006; 9: 960-967Crossref PubMed Scopus (144) Google Scholar, 40Aartsma Y. Bianchi F. van der Werf W. Poelman E.H. Dicke M. Herbivore-induced plant volatiles and tritrophic interactions across spatial scales.New Phyt. 2017; 216: 1054-1063Crossref PubMed Scopus (112) Google Scholar]. However, the scale at which floral and leaf herbivore-induced plant volatiles act and how easily distinguishable they are by different types of pollinators remain understudied in field settings [39Karpati Z. Knaden M. Reinecke A. Hansson B.S. Intraspecific combinations of flower and leaf volatiles act together in attracting hawkmoth pollinators.PLoS One. 2013; 8: e72805Crossref PubMed Scopus (16) Google Scholar, 42Holopainen J.K. Blande J.D. Where do herbivore-induced plant volatiles go?.Front Plant Sci. 2013; 4: 185Crossref PubMed Scopus (108) Google Scholar]. Whereas conventional pollinators interact mainly with the flowers of a plant, insect species that serve as both larval herbivores and adult foragers and/or pollinators interact with different plant tissues at different life stages. Along the spectrum of flower-visiting insects, ‘pollinating herbivores’ fall somewhere between obligate pollinators (such as fig wasps) in so-called ‘nursery pollination’ systems and facultative pollinators (for example, Pieris butterflies) of plants with generalized pollination systems [3Lucas-Barbosa D. Integrating studies on plant-pollinator and plant-herbivore interactions.Trends Plant Sci. 2016; 21: 125-133Abstract Full Text Full Text PDF PubMed Scopus (93) Google Scholar, 5Lucas-Barbosa D. Sun P. Hakman A. van Beek T.A. van Loon J.J.A. Dicke M. Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors.Funct. Ecol. 2016; 30: 431-441Crossref Scopus (49) Google Scholar, 24Bruinsma M. Lucas-Barbosa D. ten Broeke C.J.M. van Dam N.M. van Beek T.A. Dicke M. van Loon J.J.A. Folivory affects composition of nectar, floral odor and modifies pollinator behavior.J. Chem. Ecol. 2014; 40: 39-49Crossref PubMed Scopus (47) Google Scholar]. In a meta-analysis of European Lepidoptera, 54% of the 845 species examined in the study showed an association between larval and adult host feeding [43Altermatt F. Pearse I.S. Similarity and specialization of the larval versus adult diet of European butterflies and moths.Am. Nat. 2011; 178: 372-382Crossref PubMed Scopus (50) Google Scholar]. Although pollinating herbivore species are often butterflies or moths, some non-lepidopteran pollinators also consume both leaf and floral resources at the larval and/or adult stages (such as sawflies and thrips) [44Wackers F.L. Romeis J. van Rijn P. Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions.Annu. Rev. Entomol. 2007; 52: 301-323Crossref PubMed Scopus (239) Google Scholar]. Therefore, selection to synthesize information from both leaf and floral tissues is likely important for a number of flower-visiting insects. Thus, it stands to reason that there should be selection for pollinating herbivores to independently distinguish leaf from floral defensive traits to determine foraging and oviposition locations [45Smith G.P. Johnson C.A. Davidowitz G. Bronstein J.L. Linkages between nectaring and oviposition preferences of Manduca sexta on two co-blooming Datura species in the Sonoran Desert.Ecol. Entomol. 2018; 43: 85-92Crossref Scopus (11) Google Scholar]. In contrast, insects that function solely as pollinators should attend to the most relevant floral traits. In a study of conventional bee pollinators, Kessler et al. [18Kessler A. Halitschke R. Poveda K. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions.Ecology. 2011; 92: 1769-1780Crossref PubMed Scopus (141) Google Scholar] paired damaged and undamaged leaves with flowers from either damaged or undamaged wild tomato plants and measured visitation by wild bees. Because the bees are interested in floral resources (pollen) rather than leaf tissues, it was not surprising that floral scent mattered for pollinator attraction but vegetative herbivore-induced plant volatiles did not [18Kessler A. Halitschke R. Poveda K. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions.Ecology. 2011; 92: 1769-1780Crossref PubMed Scopus (141) Google Scholar]. However, in this case, leaf volatiles should not provide additional information about host quality other than the cues already provided by the flowers, which contain the nectar and pollen required by adult bee pollinators and their offspring, respectively. In contrast, vegetative background volatiles appear to provide oviposition context for pollinating herbivores, such as the tobacco hornworm moth, Manduca sexta. The vegetative odors of Datura wrightii are more attractive for oviposition by M. sexta females than are those of Nicotiana attenuata, potentially because the volatile headspace of the latter species is five-fold stronger and includes compounds that are generally indicative of herbivore attack [46Spathe A. Reinecke A. Haverkamp A. Hansson B.S. Knaden M. Host plant odors represent immiscible information entities — Blend composition and concentration matter in hawkmoths.PLoS One. 2013; 8: e77135Crossref PubMed Scopus (19) Google Scholar]. In a different study of the same focal species, moths showed nectar foraging preferences for floral scent combined with the conspecific leaf volatile background, but not when floral and vegetative backgrounds did not match [40Aartsma Y. Bianchi F. van der Werf W. Poelman E.H. Dicke M. Herbivore-induced plant volatiles and tritrophic interactions across spatial scales.New Phyt. 2017; 216: 1054-1063Crossref PubMed Scopus (112) Google Scholar]. Combined, these studies suggest that vegetative volatiles impact both oviposition and nectar foraging behavior, but more work is needed to determine whether different pollinator classes can use volatiles to differentiate between damaged and undamaged host plants at individual versus patch scales, particularly in field settings. Here, we have focused on just two of the many kinds of floral visitors (herbivores and pollinators). Future studies should measure the impact of pleiotropic defense chemistry on the full spectrum of flower visitors and residents, including nectar yeasts, seed predators, avian pollinators that defend floral patches as territories and even ambush predators (such as crab spiders) that hunt on flowers. Such progress would expand our ability to model the selective forces that mold induced plant responses to herbivory. In recent years there has been a surge of studies breaking down the artificial barriers between the fields of herbivory and pollination, and here we have outlined the plant mechanisms linking herbivore damage with pollinator preference and behavior. Deterring herbivory while attracting pollinators is a challenge common to insect-pollinated plants and may be particularly strong when insects act as both larval herbivores (antagonists) and adult pollinators (mutualists). Understanding the relative importance of plant floral and leaf defenses and volatiles for herbivore and pollinator choice is necessary to understand the evolution of plant defenses and insect host choice. Plants may solve this conundrum through differential resource partitioning in vegetative and floral tissues or by altering the timing of volatile emission during night and day [34De Moraes C.M. Mescher M.C. Tumlinson J.H. Caterpillar-induced nocturnal plant volatiles repel conspecific females.Nature. 2001; 410: 577-580Crossref PubMed Scopus (749) Google Scholar, 47Zhou W.W. Kuegler A. McGale E. Haverkamp A. Knaden M. Guo H. Beran F. Yon F. Li R. Lackus N. et al.Tissue-specific emission of (E)-alpha-bergamotene helps resolve the dilemma when pollinators are also herbivores.Curr. Biol. 2017; 27: 1336-1341Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar]. Experiments determining the extent to which plants are able to alter the diel rhythm of plant defenses or target accumulation of defenses in different plant tissues in response to different herbivore and pollinator environments would provide critical evidence as to how plants balance herbivory and pollination." @default.
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