Plant Resistance against Herbivory

By: Brent Mortensen (Dept. of Ecology, Evolution, and Organismal Biology, Iowa State
Uni.) 2013 Nature Education
Citation: Mortensen, B. (2013) Plant Resistance against Herbivory. Nature Education
Knowledge 4(4):5
2012 Nature Education All rights reserved.

http://www.nature.com/scitable/knowledge/library/plant-resistance-against-herbivory-96675700
Every bite an herbivore takes comes at the expense of a plant. Are plants passive
victims or do they actively resist these attacks?

Plants must invest energy and nutrients to grow stems, leaves, roots, and reproductive tissues.
When herbivores eat these tissues, plants must cope with decreased abilities to convert nutrients
and energy into offspring. Therefore, natural selection favors plant traits that limit the negative
effects of herbivores. Some plants have evolved tolerance to herbivory, growing compensatory
tissues so rapidly that reproduction can sometimes increase with light damage (Strauss &
Agrawal 1999, Stowe et al. 2000). By comparison, other plants have evolved traits that reduce
consumption by herbivores, or resistance. Because herbivores rely on plants for food, natural
selection favors herbivores that overcome plant resistance, thus prompting plants to evolve new
forms of resistance. This evolutionary race between plants and herbivores (i.e., coevolution')
has resulted in a wide array of resistance traits in terrestrial plants (Erlich & Raven 1964,
Agrawal et al. 2009) including reduced apparency to herbivores and structural, chemical, and
indirect defenses. These resistance traits are described in greater detail below.
Apparency

Some plants avoid herbivory by decreasing their apparency or hiding' from herbivores in
spatial or temporal refuges. Spatial refuges are areas physically inaccessible to or hidden from
herbivores as when plants grow on cliff ledges and plateaus in the case of geologic refuges
(Figure 1). Other spatial refuges can include areas above or below the reach of herbivores as
when grazing stimulates plant growth near the ground for non-woody plants or above the browse
line for trees and shrubs (Hayes & Holl 2003; Figure 1). Alternatively, some plants take
advantage of temporal refuges by growing or flowering when herbivores are rare or inactive.

Figure 1: Spacial refuges.

Plants may reduce herbivory by growing in areas inaccessible to herbivores as
represented in the figure above. The dashed red lines represent the area where a
particular herbivore can reach a plant and feed. Refuge types shown here include
(a) a geological refuge on top of a cliff or plateau, (b) a biotic refuge beneath plants
capable of excluding or repelling the herbivore, and (c) spatial refuges occurring
below or above the browse line for the herbivore.

Biotic refuges, sometimes referred to as associational resistance, occur whenever a plant

reduces the chances that herbivores find and consume neighboring plants of a different species.
Associational resistance can occur as the result of several processes. First, some plants can
release volatile organic chemicals (VOCs) that mask or overpower VOCs released by another
plant that would normally attract herbivores (Jactel et al. 2011). Alternatively, plants may release
VOCs that repel herbivores, though evidence of this effect is limited (Hambck et al. 2000,
Agrawal et al. 2006). Second, plants may provide an alternate food source that draws herbivores
away from another plant (Russell & Louda 2005), an effect referred to as the alternate host
hypothesis (Atsatt & O'Dowd 1976) in which associational resistance for one plant species is
paired with associational susceptibility in another plant species. From the perspective of plants
that serve as the alternate food source, association with the less preferred plant results in
associational susceptibility rather than resistance. Finally, plants may alter the physical
environment by changing the microclimate (Shepherd 1985) or increasing the structural
complexity of an environment so that herbivores are unable to find or access their preferred host.
Such complexity may occur when a poorly defended plant is growing under heavy brush
(Milchunas & Noy-Meir 2002) or intermixed with similarly colored species (Finch & Collier
2000).
While refuges allow plants to escape some herbivores, small, mobile, or temporally flexible
herbivores are not so easily deterred. As an alternative to refuges, some plants use crypsis (i.e.,
camouflage) to avoid herbivores. For example, the sensitive plant (Mimosa pudica) mimics the

appearance of a dead or wilting plant by folding and drooping its leaves when touched (Figure 2a
and b). Alternatively, stone plants (Lithops spp.) decrease apparency by, as their name implies,
resembling stones (Figure 2c and d).

Figure 2: Crypsis.
(a) Sensitive plants (Mimosa pudica) limit herbivory by folding up their leaves after
being touched (b), thus mimicking a dead, leafless plant. (c, d) Stone plants avoid
herbivores by blending in with their environment.
Photos courtesy of Sten Porse (a, b), Dun Holm (c, d), Wikimedia Commons
Structural defenses

Once herbivores find and access a plant, structural defenses can discourage consumption. These
structures include spinescence, trichomes, thick leaves, and microscopic sand- and needle-like
particles inside plant tissues (Figures 3 and 4).

Figure 3: Structural defenses.

Examples of structural defenses: (a-c) spinescence including (a) evolutionarily
modified stems, or thorns, as in honey locust (Gleditsia triacanthos), (b) leaves
modified into spines as in the California barrel cactus (Ferocactus cylindraceus), a
member of the otherwise leafless cactus family (Cactaceae), and (c) prickles, or
extensions of the epidermis, as in rose (Rosa floribunda); (d) trichomes on a
strawberry (Fragaria virginiana) bud; and (e) sclerophyllous leaves on American
holly (Ilex opaca).
2012 Nature Education Photo credit: (e) Robert H. Mohlenbrock of USDA-NRCS
PLANTS Database/USDA NRCS All rights reserved.

Figure 4: Calcium oxalate crystals.

Plants can reduce herbivory by producing calcium oxalate crystals in the form of (a)
long, needle-like raphides (from a Psychotria sp. leaf), (b) shorter and stouter
styloids (from a water hyacinth, Eichhornia sp., petiole), or (c) spherical druses
(from a Peperomia sp. leaf).
2012 Nature Education Photos used by permission of Harry T. (Jack) Horner,
Ph.D., Director of Microscopy and NanoImaging Facility, Iowa State University, Ames.
Some rights reserved.

Spinescence includes evolutionarily modified stems or leaves known as thorns or spines,

respectively, or sharp extensions of the epidermis (i.e., the 'skin) known as prickles (Figure 3a, b
and c). These sharp, pointed extensions can deter large herbivores but are generally less effective
against smaller, more maneuverable herbivores like insects. To guard against herbivorous insects,
some plants use a layer of plant hairs, or trichomes (Figure 3d). Trichomes are extensions of the
epidermis that can prevent insect eggs from sticking to a plant, hinder movement by insects, and
limit consumption by large herbivores due to their unpleasant texture. When combined with
chemical defenses, trichomes can act as glands that secrete sticky resins or irritating chemicals to
reduce grazing by large herbivores. For example, stinging nettle (Urtica dioica) produces
trichomes that break easily when handled and inject painful chemicals, much like a syringe, to
discourage grazing by large mammals (Lambers et al. 1998).
Plants may further limit herbivory by producing hard, rigid leaves (i.e., sclerophylly) and stems
that are difficult to chew (Figure 3e). Leaf toughness and stem strength are bolstered by woody
compounds such as cellulose and lignin. These compounds can only be digested with the aid of
symbiotic bacteria, which occur, for example, in the guts of cows and termites, and have little to
no dietary value. Structural compounds are therefore associated with poor nutritional values,

sometimes expressed as large carbon-to-nutrient ratios, that diminish the benefits of eating a
plant.
Some plants store non-toxic minerals from the soil, such as silica or calcium, as a form of
physical defense. Silica released into the spaces between cells (extracellular spaces) forms stonelike phytoliths (from Greek phuton for plant, and lithos for stone) that increase wear on insect
mouthparts or vertebrate teeth (Hanley et al. 2007). Calcium ions may be bound to an organic
anion, oxalate, to form crystals in cell walls, vacuoles, and trichomes (Figure 4) that can pierce
mouth tissues and cause swelling and irritation as in dumb cane (Dieffenbachia spp.; Mrvos et al.
1991). Both calcium oxalate crystals and silica phytoliths can also form painful, and potentially
lethal, kidney stones, increasing the risks of feeding on plants with these structural defenses.
Chemical defenses

Chemical defenses include compounds with chemical properties that directly deter herbivores
from feeding on a plant. Organic chemical defenses are produced by plants as secondary
metabolites, compounds not directly related to basic metabolic pathways (e.g., photosynthesis or
respiration), or by mutualistic fungi known as endophytes. By comparison, elemental defenses
are inorganic chemical defenses that must be concentrated from the environment.
Organic chemical defenses include qualitative and quantitative defenses. Qualitative defenses
are typically effective and, therefore, produced at low concentrations. Most qualitative defenses
are used in tissues that are vulnerable over short time spans, such as young, tender leaves or
seeds, and are often recycled when no longer needed. For example, some plants produce
cyanide-containing compounds in their seeds that can kill herbivores when consumed in low
doses. As the threat of herbivory declines, nitrogen stored in these compounds is recycled for
plant growth (Poulton 1990). Although qualitative defenses are typically effective against
generalist herbivores, specialists have adapted methods through coevolution to circumvent or
even highjack these defenses. For instance, monarch butterfly (Danaus plexippus) caterpillars
store qualitative chemical defenses from milkweed (Asclepias spp.) in their bodies to deter
predators (Nishida 2002). As an important resource for some specialists, qualitative defenses can
attract herbivores, turning the benefits of plant defense into a liability.
In comparison to qualitative defenses, quantitative defenses are generally effective against all
herbivores but require larger doses. As a result, these compounds are typically mass produced
and are rarely recycled. Condensed tannins are common quantitative defenses that bind to
proteins, interfering with digestion and potentially leading to malnutrition (Ayres et al. 1997).
Other quantitative defenses include chemicals that cause pain, inflammation, or swelling in the
skin or mouth when touched as in the case of stinging nettle (see Structural defenses' above) or
poison ivy (Toxicodendron radicans).
Whether a plant relies more heavily on qualitative or quantitative defenses may be influenced by
factors such as growth rate (Coley et al. 1985), nutrient availability (Stamp 2003), or how easily
it can be found by herbivores (Feeny 1976). Regardless of their mode of operation, organic
chemical defenses reduce the incentive for herbivores to feed on a plant and, consequently, the
amount of damage sustained.

Humans use organic chemical defenses as common ingredients in food and medicine. For
example, caffeine belongs to a class of qualitative defenses that block brain signals relaying
drowsiness (Fisone et al. 2004). Uses for defensive and other secondary compounds are studied
in the fields of ethnobotany and pharmacology (Fowler 2006, Soetan 2008).
Inorganic, elemental defenses likely evolved as a way for plants to cope with toxic elements
inadvertently absorbed from the soil such as nickel, zinc, cadmium, and lead. Many plants avoid
poisoning by storing these elements away from cell machinery in cell walls, vacuoles, or
trichomes until they are released when a plant dies or is consumed. As these elements are also
poisonous to most herbivores, plants that absorb and store toxic elements, referred to as metal
hyperaccumulators', benefit from reduced herbivory (Poschenrieder et al. 2006, Boyd 2007,
Boyd 2009).
Chemical defenses are not always meant to deter all herbivores. Many plants benefit from
interactions with mutualistic herbivores such as pollinators or seed dispersers and have evolved
defenses that only target harmful herbivores. For example, chili seeds pass safely through the
digestive systems of birds and are dispersed in the droppings but are destroyed when eaten by
mammals. Not surprisingly, capsaicin, the compound that gives chilies their hot flavor, affects
mammals but not birds (Tewksbury & Nabhan 2001).
Indirect defenses

Instead of directly defending against herbivores, indirect defenses reduce herbivory by

increasing the likelihood that herbivores (usually insects) are attacked, removed, or harassed by
predators like ants, wasps, and mites (Figure 5). Because indirect defenses rely on a third trophic,
or feeding, level in the food web, they are sometimes referred to as tritrophic or biotic defenses.
Plants increase predation of herbivores by luring and keeping predators on a plant with food
rewards, shelters from harsh conditions, or chemicals signaling prey availability.

Figure 5: Indirect defenses.

Indirect defenses function by (a) attracting predators (third trophic level) such as
ants, wasps, and mites with incentives including food rewards, domatia, or chemical
signals advertising the presence of prey. (b) Once present, predators attack and/or
remove herbivores (second trophic level) that can damage a plant (first trophic
level). (c) By comparison, direct defenses do not require a mediator to negatively
affect herbivores. (d) Decreased feeding by herbivores results in less damage to the
plant.
2012 Nature Education All rights reserved.

Many plants produce energy-rich food rewards to attract predators, decreasing production when
predators or herbivores are absent or inactive (Heil et al. 1997, Wckers & Bonifay 2004). Food
rewards used in plant defense include nectar, produced by extrafloral nectaries (EFNs), and
solid food bodies (Figure 6a). Unlike floral nectaries, the primary function of EFNs is to attract
predators rather than pollinators. EFNs promote defensive mutualisms ranging from absolute
requirements for survival in myrmecophytes (i.e., ant plants') to beneficial but nonessential
relationships in a number of other plants (Bentley 1977). Solid food bodies range in form from
fruit-like appendages to soft layers of nutritious tissue. These structures contain lipids,
carbohydrates, and proteins that represent a substantial investment by the plant. Consequently,
food bodies have only been observed on myrmecophytes and are associated with other forms of
indirect defense such as domatia (Heil 2008).
Domatia are structures that shelter predators from harsh environmental conditions or other
predators. Domatia may range in complexity from shallow crevasses covered with trichomes as
in some varieties of avocado (Persea americana; Agrawal 1997) to hollow tissues with multiple
chambers and elaborate entrances as in many acacia (Acacia spp.; Figure 6b and c). Although
domatia and food rewards may not directly attract predators, they can increase the likelihood that
visiting predators will remain on a plant and reduce herbivory.

Figure 6: Food rewards and domatia.

The bullhorn acacia (Acacia cornigera) uses indirect defenses to encourage
predators to remain on the plant and attack visiting herbivores. These indirect
defenses include (a) food rewards for foraging ants including EFNs (red arrow)
located at the base of the leaves and food bodies (blue arrow) located on the tips of
individual leaflets; and (b, c) domatia formed from hollow spines that provide
shelter for ants (b: exterior view; c: interior view).
2012 Nature Education All rights reserved.

The only indirect defenses that actively attract predators are volatile organic chemicals (VOCs).
These gaseous signals are often released from damaged plant tissues, advertising the presence of
potential prey. VOCs can vary with time of attack (e.g., night vs. day) or herbivore identity to
attract predators best adapted for a particular herbivore. For example, broad bean plants (Vicia
faba) attacked by different species of aphid (Acyrthosiphon pisum and A. fabae) release different
VOCs that attract different predators (Powell et al. 1998). Many VOCs also repel herbivores,
including adult hawkmoths (Manduca quinquemaculata) that avoid laying eggs on tobacco
plants (Nicotiana attenuata) emitting predator-attracting VOCs (Kessler & Baldwin 2001).
VOCs, therefore, serve dual defensive purposes by indirectly reducing herbivory via predator
attraction and directly deterring herbivores.
Resistance costs

The resistance traits discussed above can be costly in terms of energy, resource, and opportunity
costs (Strauss et al. 2002). As plants have limited resources, an increase in either resistance or
growth must be balanced by a decrease in the other (Coley et al. 1985), a relationship referred to
as a tradeoff. Consequently, fast-growing plant species are typically less resistant to herbivory
than slower growing species (Endara & Coley 2011). Tradeoffs may also exist among resistance
traits so that a plant cannot maximize all forms of resistance against all possible herbivores. As a
result, plants may express different resistance traits that minimize consumption by different
herbivores in different places (e.g., Berenbaum & Zangerl 2006) or at different times (e.g.,
Wckers et al. 2004).
To avoid negative effects of tradeoffs, many plants maintain low baseline, or constitutive,
defensive levels until stimulated, or induced, by herbivore damage, VOCs, light availability, or
day length (Zangerl 2003, Wckers & Bonifay 2004, Conrath et al. 2006, Radhika et al. 2008).
In fact, many direct (Chen 2008) and indirect (Heil 2008) resistance traits are only expressed
following induction by some stimulus. In this way plants are able to avoid investing resource in
unneeded resistance traits, thus allowing more resources for growth and reproduction.

Conclusion

The goal of this article is to briefly introduce various forms of plant resistance against
herbivores; however, resistance traits against pathogens such as fungi, viruses, and nematodes
also exist. Despite some overlap between herbivore and pathogen resistance, a number of
uniquely anti-pathogenic defenses exist (Lambers et al. 1998, Anderson et al. 2010).
Natural selection from herbivory has prompted plants to evolve a wide array of resistance traits
to reduce losses from herbivory. Plants avoid herbivory by hiding, building structural barriers,
producing and acquiring chemical toxins, and recruiting predatory bodyguards'. Thus, plants are
not the helpless victims of herbivory but defend themselves against the loss of resources and
energy, allowing for greater investment in reproduction and survival.

Glossary
apparency: Ease by which an object, in this case a plant, is found
associational resistance: Defensive benefits acquired by a plant due to close spatial association
with a different plant species
associational susceptibility: Increased herbivory on a plant as a result of close spatial
association with a different plant species
chemical defense: Compounds and elements with chemical properties that directly deter or limit
herbivory
coevolution: Paired, reciprocal evolution between two closely interacting species in response to
evolutionary change of either species
crypsis: Morphological adaptations used to specifically avoid herbivores/predators; a form of
camouflage
domatia: Plant structures that shelter predators from environmental conditions or predation
(from the Latin domus-house')
elemental defense: Toxic elements absorbed from the soil and stored in plant vacuoles, cell
walls, and trichomes that reduce herbivory
endophytes: Fungi that live in the intracellular space of plant tissues, some of which produce
chemical toxins used to deter herbivores
extrafloral nectaries (EFNS): Nectar-secreting structures that are not directly related to
reproduction; typically used in indirect defense
food bodies: Dense multicellular structures, composed of carbohydrate, lipid, and protein,
offered as food rewards to predatory mutualists
generalist: An organism with a wide resource base; as herbivores, generalists are not well

adapted to defenses on any one plant

indirect defense: Traits that reduce herbivory without directly affecting herbivores, usually by
attracting predators
inorganic chemical defense: Chemical defense not produced by a living organism that must be
acquired from the environment (see elemental defense)
metal hyperaccumulators: Plants that actively acquire and store toxic elements in their tissues
in lethal concentrations
microclimate: Climatic conditions that may vary at small geographical scales (typically <1 m),
such as temperature, humidity, etc.
mutualism: Interaction between two organisms in which both organisms benefit
myrmecophytes: Plants that are nearly or completely reliant on predatory, mutualistic ants for
survival (from the Greek murmx-ant', phuton-plant')
organic chemical defense: Chemical defense produced by a living organism, in this case a plant
or its mutualist
qualitative defense: Chemical defenses produced in low concentrations that have similar effects
regardless of concentration
quantitative defense: Chemical defenses typically produced in high concentrations that increase
in effect with concentration
refuge: A point in space (i.e., spatial refuge) or time (i.e., temporal refuge) where plants are
inaccessible to herbivores
resistance: Plant strategy in which the negative effects of herbivores on plant fitness are reduced
by preventing or limiting herbivory
sclerophylly: Hard or tough leaves; used as a form of structural defense (from the Greek
sklros-hard', phullon-leaf')
secondary metabolites: Chemical compounds produced by a plant that are not involved in basic
metabolic processes
specialist: An organism with a narrow resource base. For herbivores, specialists are well adapted
to defenses on one or a few plants.
spinescence: Collective term for pointed, prong-like extensions, including thorns, spines, and
prickles

structural defense: Physical structures that reduce the amount of damage a plant receives from
herbivores
tolerance: Plant strategy in which the negative effects of herbivores are reduced by increasing
growth rates after herbivory
tradeoff: A negative relationship between two traits owing to limited resources so that one trait
must decrease as the other increases
trichomes: Thin, hair-like extensions of the epidermis
volatile organica chemicals (VOCS): Chemical signals released from damaged plant tissues as
a gas; VOCs can be used to attract predators or repel herbivores

References and Recommended Reading

Introduction/General
Agrawal, A. A et al. Evidence for adaptive radiation from a phylogenetic study of plant defenses.
Proceedings of the National Academy of Sciences (USA) 106, 18067-18072 (2009).
Ehrlich, P. R. & Raven, P. H. Butterflies and plants: A study in coevolution. Evolution 18, 586608 (1964).
Stowe, K. A. et al. 2000. The evolutionary ecology of tolerance to consumer damage. Annual
Review of Ecology and Systematics 31, 565-595 (2000).
Strauss, S. Y. & Agrawal, A. A. 1999. The ecology and evolution of plant tolerance to herbivory.
Trends in Ecology & Evolution 14, 179-185 (1999).
Apparency
Agrawal, A. A. et al. Community heterogeneity and the evolution of interactions between plants
and insect herbivores. Quarterly Review of Biology 81, 349-376 (2006).
Atsatt, P. R. & O'Dowd, D. J. Plant defense guilds. Science 193, 24-29 (1976).
Finch, S. & Collier, R. H. Host-plant selection by insects - a theory based on
'appropriate/inappropriate landings' by pest insects of cruciferous plants. Entomologia
Experimentalis et Applicata 96, 91-102 (2000).
Hmback, P. A. & Beckerman, A. P. Herbivory and plant resource competition: a review of two
interacting interactions. Oikos 101, 26-37 (2003).
Hmback, P. A. et al. Associational resistance: Insect damage to purple loosestrife reduced in
thickets of sweet gale. Ecology 81, 1784-1794 (2000).

Hayes, G. F. & Holl, K. D. Cattle grazing impacts on annual forbs and vegetation composition of
mesic grasslands in California. Conservation Biology 17, 1694-1702 (2003).
Jactel, H. et al. Non-host volatiles mediate associational resistance to the pine processionary
moth. Oecologia 166, 703-711 (2011).
Milchunas, D. G. & Noy-Meir, I. Grazing refuges, external avoidance of herbivory and plant
diversity. Oikos 99, 113-130 (2002).
Russell, F. L. & Louda, S. M. Indirect interaction between two native thistles mediated by an
invasive exotic floral herbivore. Oecologia 146, 373-384 (2005).
Shepherd, R. C.H. The present status of St. John's wort (Hypericum perforatum L.) and its
biological control agents in Victoria, Australia. Agriculture, Ecosystems & Environment 12, 141149 (1985).
Structural defenses
Hanley, M. E. et al. Plant structural traits and their role in anti-herbivore defence. Perspectives in
Plant Ecology Evolution and Systematics 8, 157-178 (2007).
Kahn, S. R [ed.]. Calcium oxalate in biological systems., Boca Raton, FL: CRC Press 1995.
Lambers, H. et al. Plant physiological ecology. New York, NY: Springer Science, 1998.
Massey, F. P. & Hartley, S. E. Physical defences wear you down: progressive and irreversible
impacts of silica on insect herbivores. Journal of Animal Ecology 78, 281-291 (2009).
Mrvos, R. et al. Philodendron/Dieffenbachia ingestions: Are they a problem? Clinical Toxicology
29, 485-491 (1991).
Turner, I. M. Sclerophylly: Primarily protective? Functional Ecology 8, 669-675 (1994).
Chemical defenses
Ayres, M. P. et al. Diversity of structure and antiherbivore activity in condensed tannins. Ecology
78, 1696-1712 (1997).
Boyd, R. S. The defense hypothesis of elemental hyperaccumulation: status, challenges and new
directions. Plant and Soil 293, 153-176 (2007).
Boyd, R. S. High-nickel insects and nickel hyperaccumulator plants: A review. Insect Science 16,
19-31 (2009).
Coley, P. D. et al. Resource availability and plant antiherbivore defense. Science 230, 895-899
(1985).

Feeny, P. P. 1976. "Plant apparency and chemical defense," in Recent Advances in

Phytochemistry, eds. by Wallace, J. W. & Mansell, R. L. (New York: Plenum Press, 1976) 1-40.
Fisone, G. et al. Caffeine as a psychomotor stimulant: mechanism of action. Cellular and
Molecular Life Sciences 61, 857-872 (2004).
Hartley, S. E. & Gange, A. C. Impacts of plant symbiotic fungi on insect herbivores: mutualism
in a multitrophic context. Annual Review of Entomology 54, 323-342 (2009).
Fowler, M. W. Plants, medicines and man. Journal of the Science of Food and Agriculture 86,
1797-1804 (2006).
Kramer, U. Metal Hyperaccumulation. Annual Review of Plant Biology 61, 517-534 (2010).
Nishida, R. Sequestration of defensive substances from plants by Lepidoptera. Annual Review of
Entomology 47, 57-92 (2002).
Poschenrieder, C. et al. Can metals defend plants against biotic stress? Trends in Plant Science
11, 288-295 (2006).
Poulton, J. E. Cyanogenesis in plants. Plant Physiology 94, 401-405 (1990).
Tewksbury, J. J. & Nabhan, G. P. Directed deterrence by capsaicin in chillies. Nature 412, 403404 (2001).
Soetan, K. O. Pharmacological and other beneficial effects of anti-nutritional factors in plants: A
review. African Journal of Biotechnology 7, 4713-4721 (2008).
Stamp, N. Out of the quagmire of plant defense hypotheses. Quarterly Review of Biology 78, 2355 (2003).
Indirect defenses
Agrawal, A. A. Do leaf domatia mediate a plant-mite mutualism? An experimental test of the
effects on predators and herbivores. Ecological Entomology 22, 371-376 (1997).
Bentley, B. L. Extrafloral nectaries and protection by pugnacious bodyguards. Annual Review of
Ecology & Systematics 8, 407-427 (1977).
Bronstein, J. L. et al. The evolution of plant-insect mutualisms. New Phytologist 172, 412-428
(2006).
Heil, M. Indirect defence via tritrophic interactions. New Phytologist 178, 41-61 (2008).
Heil, M. et al. Food body production in Macaranga triloba (Euphorbiaceae): a plant investment
in anti-herbivore defence via symbiotic ant partners. Journal of Ecology 85, 847-861 (1997).

Kessler, A. & Baldwin, I. T. Defensive function of herbivore-induced plant volatile emissions in

nature. Science 291, 2141-2144 (2001).
Powell, W. et al. Strategies involved in the location of hosts by the parasitoid Aphidius ervi
Haliday (Hymenoptera : Braconidae : Aphidiinae). Biological Control 11, 104-112 (1998).
Romero, G. Q. & Benson, W. W. Biotic interactions of mites, plants and leaf domatia. Current
Opinion in Plant Biology 8, 436-440 (2005).
Wckers, F. L. & Bonifay, C. How to be sweet? Extrafloral nectar allocation by Gossypium
hirsutum fits optimal defense theory predictions. Ecology 85, 1512-1518 (2004).
Resistance costs
Berenbaum, M. R. & Zangerl, A. R. . Parsnip webworms and host plants at home and abroad:
Trophic complexity in a geographic mosaic. Ecology 87, 3070-3081 (2006).
Chen, M. S. Inducible direct plant defense against insect herbivores: A review. Insect Science 15,
101-114 (2008).
Coley, P. D. et al. Resource availability and plant antiherbivore defense. Science 230, 895-899
(1985).
Conrath, U. et al. 2006. Priming: Getting ready for battle. Molecular plant-microbe interactions
19, 1062-1071.
Endara, M. J. & Coley, P. D. The resource availability hypothesis revisited: a meta-analysis.
Functional Ecology 25, 389-398 (2011).
Radhika, V. et al. Testing the optimal defence hypothesis for two indirect defences: extrafloral
nectar and volatile organic compounds. Planta 228, 449-457 (2008).
Strauss, S. Y. et al. Direct and ecological costs of resistance to herbivory. Trends in Ecology &
Evolution 17, 278-285 (2002).
Wckers, F. L. & Bonifay, C. How to be sweet? Extrafloral nectar allocation by Gossypium
hirsutum fits optimal defense theory predictions. Ecology 85, 1512-1518 (2004).
Zangerl, A. R. Evolution of induced plant responses to herbivores. Basic and Applied Ecology 4,
91-103 (2003).
Conclusion
Anderson, J. P. et al. Plants versus pathogens: An evolutionary arms race. Functional Plant
Biology 37, 499-512 (2010).

Lambers, H. et al. Plant physiological ecology. New York, NY: Springer Science, 1998.