Science to the Grower: Are plants intelligent enough to earn a scouting merit badge?
by Richard Evans
I know what you're thinking as you read about scouting in this issue of UCNFA News. You’re thinking about all the time and money you’ll have to spend detecting pests and deciding when a problem requires action. Wouldn’t it be nice if plants could get off their butts and take care of business themselves? It’s not so far-fetched. Plants may seem like couch potatoes, but there is abundant evidence that they can take an active role in scouting. They can recognize pests, count their numbers, defend themselves from attackers, warn neighboring plants that pests are present and even send out orders for pest management.
The best-known example of a plant monitoring and responding to insects is the Venus flytrap (Dionaea muscipula). It responds to an insect touching the trigger hairs located on each leaf-like lobe of the trap. The trap snaps shut when two trigger hairs are bent, or when one hair is bent twice, within about 15 to 20 seconds (Escalante-Pe´rez and others 2011). Yes, plants can count and tell time! The flytrap doesn’t waste much energy on false alarms, either. It secretes digestive chemicals only after the trapped insect triggers the hairs three more times (Böhm and others 2016).
Another well-known response is that of the sensitive plant, Mimosa pudica. It folds its leaflets in response to physical disturbance, apparently as a defensive response to herbivores. Since many leaf disturbances are non-threatening, it would be to the plant’s benefit if it could decide whether to respond, rather than wasting energy every time the wind blows. Monica Gagliano, an Australian ecologist, made a remarkable discovery when she conducted experiments on potted Mimosa plants (Gagliano and others 2014). She constructed a device that dropped the plants from a height of about 6 inches every 5 seconds. Leaflets closed after the first drop, but the plants stopped responding after a few more drops, and all leaflets were open by the time the plants had been dropped 60 times. The plants recognized that the disturbance was annoying, but not threatening. Or maybe they got bored. However, if the plants were disturbed in a different way, like shaking them from side to side, the leaflets closed again. If Gagliano commenced dropping them again, the plants didn’t respond. They remembered that dropping 6 inches wasn’t going to damage them. In fact, the plants remembered for as long as 28 days! Even more amazing is that Mimosa plants growing in low light conditions, where leaf exposure to light is essential to maximize photosynthesis, are more likely to ignore leaf disturbances than plants exposed to high light conditions. Apparently they recognize that when light is in short supply it’s worth spreading leaves to photosynthesize, even if it increases the risk of getting chomped.
These are both examples of rapid plant responses that we can easily observe. But plants have a surprisingly large array of senses, and most of their responses to pests seem subtle to us, but perhaps not so subtle to the attackers. In addition to sensing light and moisture, they can detect gravity, pressure, surface texture, air and soil volumes, nutrients like nitrogen and phosphorus, toxic chemicals, chemical signals from plants and other organisms, and microbes. For instance, tobacco and soybean plants can detect the footsteps of caterpillars crawling on leaves. Glandular trichomes — hair-like cells on plant surfaces — get ruptured when caterpillars crawl by. Within seconds, the leaves create toxins that provide protection until the plant can synthesize and release systemic compounds to resist attack (Peiffer and others 2009). Goldenrod plants that detect the pheromone sex attractant of a gall-forming fly initiate chemical changes that make the plants unappealing to egg-laying female flies (Helms and others, 2013).
Plants have other early-warning systems, too. They can detect the presence of insect saliva, pheromones, skin (cuticle) and frass (Ray and others 2015). Plants recognize that these are evidence of insect presence. They even remember these cues of potential insect attack so that they can defend themselves quickly and vigorously the next time insects seek a meal (Conrath, 2011). For example, plants may detect insect egg-laying from physical signals, insertion of the eggs into plant tissue, or chemical signals released by the eggs or the female insect. Detection of egg laying can lead to all sorts of responses. When the Colorado potato beetle lays eggs on potato leaves, the leaf cells within a couple of millimeters of the egg mass undergo a hypersensitive response which kills the cells that have attached eggs. When these cells dry out, the eggs fall off the plant, where emerging insect larvae are likely to be eaten themselves (Balbyshev and Lorenzen 1997). Rice plants respond to leafhopper egg-laying by releasing a chemical that kills the eggs (Suzuki and others 1996). When elm leaf beetles lay eggs on elm trees, the trees release a volatile chemical that attracts a parasitoid wasp species that specializes in attacking elm leaf beetle eggs (Meiners and others 2000).
Sometimes the plant summons a parasite that attacks the insect larvae instead of eggs. After cabbage butterflies lay eggs on a black mustard plant, the plant produces a volatile compound that attracts a parasitic wasp to feeding caterpillars (Pashalidou and others 2015). This plant can even detect what sort of insect eggs have been laid. If a black mustard plant detects egg laying by a butterfly whose larvae adore the taste of black mustard leaves, the plant goes into defense mode. If the eggs are deposited by a species whose larvae are likely to move on without doing much damage, the mustard plant doesn’t waste energy building up its defenses (Pashalidou and others 2013).
The Scots pine has a particularly remarkable response to egg laying by sawflies. Exactly three days after eggs are laid, the pine needles produce a chemical that summons an insect that parasitizes sawfly eggs (Hilker and others 2002). Why wait three days? Because that is when the insect predator is most successful at parasitizing the eggs.
However, early warning systems don’t always prevent attacks. You may know that when insects do start gnawing, plants react by producing defensive chemicals to limit the damage. This might surprise you, though: plants can also hear insects having a meal. Heidi Appel and Rex Cocroft, researchers at the University of Missouri, recorded the acoustic vibrations that caterpillars make while eating leaves, then played back those recordings later to other plants that hadn’t been touched by the caterpillars. Those plants responded by producing defensive chemicals that made them unappealing to the caterpillars (Appel and Cocroft 2014). Remarkably, the plants could distinguish these caterpillar feeding sounds from acoustically similar insect sounds, which did not stimulate production of chemical defenses by the plant.
Sometimes plants ask for assistance from others. Aphid-free fava bean plants that are connected via a mycorrhizal network to plants that have suffered aphid attacks will produce chemicals that repel aphids and attract aphid parasitoids (Babikova and others 2013). Common bean plants attacked by twospotted spider mites react by producing methyl salicylate, a volatile chemical signal that can attract insect predators. However, if the bean plants have formed mycorrhizal associations prior to attack and the spider mites have been present for more than three days, the mycorrhizae modify the chemical signal to make it strongly attractive to the predatory mite Phytoseiulus persimilis, which can control the spider mite infestation (Schausberger and others 2012).
Plants even warn their neighbors and family of insect threats. Rick Karban’s group at UC Davis found that sagebrush plants can communicate with each other through emission of volatile chemicals. When they clipped leaves of a plant to simulate an insect attack, both the clipped plant and its neighbors were subsequently less likely to suffer insect damage (Karban and others 2006). Sagebrush plants even recognize their close relatives through these volatile emissions. Closely related plants experienced less insect damage than neighboring plants that were more distantly related (Karban and others 2013).
These studies demonstrate that plants can take care of pest scouting and implement their own integrated pest management program. So why don’t they get off their lazy roots and do it? Part of the answer has to do with the fact that all of these ways to combat pests evolved over many millions of years of natural selection. The fittest survive and pass on their genes to the next generation, but they rarely survive undamaged because pests are not usually eliminated completely in natural systems. And the pests can evolve, too, so that they can trick, avoid, or overcome plant defenses. The problem may be compounded by us, because these pest scouting traits in plants have been neglected in most breeding and selection of commercial cultivars.
There may be ways we can take advantage of the pest management skills in plants, or even enhance them. Some researchers already are trying to genetically modify plants — mostly food crops, so far — to increase their production of volatile compounds that repel pests and attract insect parasites. A British group genetically engineered wheat to produce a pheromone that repels aphids, and demonstrated that the transformed wheat plants were aphid-free. However, aphids reared in the presence of those wheat plants lost most of their sensitivity to the pheromone within five generations (Bruce and others 2015), so it isn’t a promising long-term solution. Many of the plant-pest interactions I’ve described are complex, and some scientists think that current methods of genetic engineering are unlikely to work on such complex interactions (Stenberg and others 2015).
Another interesting idea is for growers to use detection of the volatile compounds released by plants in their scouting programs. A group of biologists and engineers in Missouri and Michigan built an instrument they called an “adaptive two-dimensional microgas chromatograph” —basically a mechanical sniffer — with the idea that it could be used to detect plants under attack (Liu and others 2012). The device would be pulled between rows of crop plants, where it could alarm the grower when it detected production of pest-induced plant volatiles. Unfortunately, last I heard they did not have sufficient funding to construct and test an instrument that could be used in the field. Maybe someone needs to get to work on a money detector.
Richard Evans is UC Cooperative Extension Environmental Horticulturist, Department of Plant Sciences, UC Davis.
Appel HM, Cocroft RB. 2014. Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 175:1257–1266.
Babikova Z, Gilbert L, Bruce TJA, Birkett M, Caul?eld JC, Woodcock C, Pickett JA, Johnson D. 2013. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters 16: 835–843.
Balbyshev NF, Lorenzen JH. 1997. Hypersensitivity and egg drop: a novel mechanism of host plant resistance to Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 90:652−657.
Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller TD, Shabala L, Monte I, Solano R, Al-Rasheid KAS, Rennenberg H, Shabala S, Neher E, Hedrich R. 2016. The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Current Biology 26:286–295.
Bruce TJA, Aradottir GI, Smart LE, Martin JL, Caulfield JC, Doherty A, Sparks CA, Woodcock CM, Birkett MA, Napier JA, Jones HD, Pickett JA. 2015. The first crop plant genetically engineered to release an insect pheromone for defence. Scientific Reports 5: doi:10.1038/srep11183.
Conrath U. 2011. Molecular aspects of defence priming. Trends in Plant Science 16:524−531.
Escalante-Pe´rez M, Krol E, Stange A, Geiger D, Al-Rasheid KAS, Hause B, Neher E, Hedrich R. 2011. A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus ?ytrap. Proceedings of the National Academy of Sciences 108:15492−15497.
Gagliano M, Renton M, Depczynski M, Mancuso S. 2014. Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175:63–72.
Helms AM, De Moraes CM, Tooker JF, Mescher MC. 2013. Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory. Proceedings of the National Academy of Sciences 110:199–204.
Hilker M, Kobs C, Varama M, Schrank K. 2002. Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. Journal of Experimental Biology 205:455–461.
Karban R, Shiojiri K, Huntzinger M, McCall AC. 2006. Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930.
Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evans RY. 2013. Kin recognition affects plant communication and defence. Proceedings of the Royal Society Series B 280:20123062. http://dx.doi.org/10.1098/rspb.2012.3062.
Liu J, Oo MKK, Reddy K, Gianchandani YB, Schultz JC, Appel HM, Fan X. 2012. Adaptive two-dimensional microgas chromatography. Analytical Chemistry 84:4214−4220.
Meiners T, Westerhaus C, Hilker M. 2000. Speci?city of chemical cues used by a specialist egg parasitoid during host location. Entomologia Experimentalis et Applicata 95:151–159.
Pashalidou FG, Lucas-Barbosa D, van Loon JJA, Dicke M, Fatouros NE. 2013. Phenotypic plasticity of plant response to herbivore eggs: effects on resistance to caterpillars and plant development. Ecology 94:702–713.
Pashalidou FG, Gols R, Berkhout BW, Weldegergis BT, van Loon JJA, Dicke M, Fatouros NE. 2015. To be in time: egg deposition enhances plant-mediated detection of young caterpillars by parasitoids. Oecologia 177:477–486.
Peiffer M, Tooker JF, Luthe DS, Felton GW. 2009. Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytologist 184:644–656.
Ray S, Gaffor I, Acevedo FE, Helms A, Chuang W-P, Tooker J, Felton GW, Luthe DS. 2015. Maize plants recognize herbivore-associated cues from caterpillar frass. Journal of Chemical Ecology 41:781–792.
Schausberger P, Peneder S, Jürschik S, Hoffmann D. 2012. Mycorrhiza changes plant volatiles to attract spider mite enemies. Functional Ecology 26:441–449.
Stenberg JA, Heil M, Åhman I, Björkman C. 2015. Optimizing crops for biocontrol of pests and disease. Trends in Plant Science 20:698−712.