Plants are not sitting ducks waiting for herbivores to eat them

ABSTRACT

There is a common attitude toward plants, accordingly, plants are waiting around to be found and eaten by herbivores. This common approach toward plants is a great underestimation of the huge and variable arsenal of defensive plant strategies. Plants do everything evolution has allowed them to do in order not to be eaten. Therefore, plants are not sitting ducks and many plants outsmart and even exploit many invertebrate and vertebrate herbivores and carnivores for pollination and for seed dispersal, and even carnivores and parasitoids for defense.

KEYWORDS:

• Defense
• herbivory
• plants
• sitting ducks

Human patients with severe brain damage due to trauma or ischemia may never regain recognizable mental functions, and they never speak because of absence of function in the cerebral cortex. Such patients were described in a classic medical paper as in a “persistent vegetative state,”¹ and are referred to either as “plants” or “vegetables” by laymen depending on language and culture. This attitude toward plants was recently manifested by Laundré² in an essay about the hunting hardships of large carnivores. Laundré² posited that “meeting daily energetic needs by large carnivores is not as easy as just going out and gathering plants that are waiting around to be found and eaten.”

This common approach toward plants is a great underestimation of the huge and variable arsenal of defensive plant strategies. Plants do everything evolution has allowed them to do in order not to be eaten, and all land plants employ several simultaneous constitutive and induced defensive strategies. I clearly and sharply posit that except for rewarding flowers toward legitimate pollinators,³ ripe animal-dispersed fruits toward seed dispersers,⁴ or various food rewards to mutualistic ants,⁵ plants as a whole, or even specific plant organs, do not wait around to be found and eaten.

Defenses are aimed at enemies, and the herbivore enemies of land plants include vertebrates (mammals, reptiles and birds), invertebrates (Mollusca, arthropods, worms),^6-10 and parasitic plants that should be considered as herbivores.¹¹ Evidence from fossils indicates that herbivory on land plants began not later than the Early Devonian, some 400 million years ago,¹² and since earlier land plant fossils are uncommon and not well preserved, it probably started at least dozens of millions years earlier, even before the appearance of vascular land plants. In spite of the large arsenal of anti-herbivory defenses that plants possess, herbivory in terrestrial ecosystems may consume in extreme cases up to about 75% of the net primary production. However, the range of plant consumption is enormous, and can be as low as less than 0.1%,¹³ with a median of 18%.¹⁴

Even most animal-pollinated, and food-rewarding flowers and animal-dispersed fleshy fruits that are intended to be at least partly eaten in order to facilitate plant gene dispersal, have multitudes of defensive mechanisms. For instance, flower and fruit colors and odors, and their chemical and physical defenses have commonly been discussed as mechanisms for filtering pollinators and seed dispersers.^3,15-18 Pollen odors in certain wind-pollinated plants that certainly are not aimed at attracting pollinators are rich in defensive molecules, such as α-methyl alcohols and ketones.¹⁹ Colored nectar (yellow, red, brown, black, green, blue) is known in at least 68 taxa belonging to 20 genera in 15 families.²⁰ These authors showed data indicating that the colors and their associated nectar chemistry serve as honest signals and as floral filters against nectar thieves and inefficient pollinators. Thus, certain floral scents may have a defensive role^17,21 in addition to their well-known attracting function. The de-aromatized isoprenylated phloroglucinols may visually attract pollinators of Hypericum calycinum by their UV pigmentation properties, but at the same time the plant may use this pigmentation as a toxic substance against caterpillars, defending the flowers from herbivory.²² A similar double strategy of using signals to attract certain animals and repel others occurs in fruits.^23,24 Ripe fleshy fruits that are intended to be eaten by seed dispersers defend themselves, especially when they are unripe, by means of chemistry, timing, camouflage, aposematism, and mechanical defenses.^25-28

Plant defenses can be classified as static (constitutive) or dynamic (induced), and many types of anti-herbivory plant defenses serve both as constitutive and induced ones. The main constitutive ones are: the cuticle, cork, thorns, spines, prickles, cutting leaf edges, trichomes, resins, gums, latex, toxins, raphids and other calcium oxalate structures, silica bodies (phytoliths), protease inhibitors, lignification, stone cells (sclereids), aposematism (visual, olfactory, movement), camouflage, masquerade, mimicry, statistical (rarity, flowering once in many years, mast fruiting), and collaboration with other organisms (ants, fungi, bacteria, birds, parasitoids and predaceous arthropods, nurse plants). The main induced ones are: wound cork, thorns, spines, prickles, trichomes, traumatic resin and gum ducts and their products, toxins, PR proteins, protease inhibitors, lignification, silica bodies, jasmonate (inducing both direct internal plant defenses and attraction of predators and parasitoids) and hypersensitivity.^29-34 The expression of induced plant defenses is regulated in many cases by their ability to sense who attacked them and thus employ specific induced defenses through cues such as chitin (fungal and insect attacks), volatiles, and probably by other cues and signals.^{7,10,29,31,33}

I give some specific examples of the complicated and sophisticated ways by which plants defend themselves from herbivory as a demonstration of plants not being sitting ducks. Plants were proposed to cause false satiation by various molecules,³⁵ and to intimidate herbivores visually and chemically by aposematism³⁶ and possibly even by movement.³⁷ For instance, when thorny branches and spiny leaves move in the wind, they are actually “patrolling,” and will hit anything positioned in their way and inflict wounds on large herbivores that enter their territory. Similarly, when such branches and leaves are bent by a large moving animal, they often return quickly and forcefully to their original position, stabbing the herbivores. I was painfully wounded by such spring actions numerous times during field work and fully appreciate their nasty reaction. Plants also use camouflage,^38-45 and pathogenic bacteria that they insert into the tissues of herbivores,⁴⁶ they undermine the camouflage of herbivorous insects,⁴⁷ and also use strong wind-induced leaf movements to get rid of herbivores,^48,49 all of these in order to defend themselves from herbivory. Plants have many other types of mechanical defenses^30,50,51 including even anisotropic arrangement of structural defenses that can lead invertebrate herbivores away from the plants.⁵² From time to time, flowers and fruits may overwhelm and satiate herbivores by their sudden appearance in huge numbers in cases of mast fruiting or synchronous flowering.^53,54 Plants can even remember herbivore attacks for a long time^10,55 and receive volatile cues about risks from kin individuals that result in upregulating various defenses that then result in reduced herbivory damage compared to plants that receive such cues from non kin.⁵⁶ Plants employ bodyguards such as ants,⁵ and call predators and parasitoids of their attacking invertebrate herbivores by using volatiles.^10,57 This list is only a short partial summary of the many ways plants defend themselves from herbivores or manipulate them, and manipulate various herbivores' predaceous or parasitic enemies to the benefit of the plants.

I conclude that considering plants as defenseless and motionless victims (sitting ducks) of herbivores, because they are not as fast and agile as are large mammalian herbivores or carnivores, is a huge underestimation of plant defensive abilities, as many plants outsmart and even exploit many invertebrate and vertebrate herbivores and carnivores for pollination and for seed dispersal, and even carnivores and parasitoids, as was mentioned above, for defense.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.