Transcript Slide 1
HERBIVORY Herbivory Herbivory (a broad definition): the consumption of all or parts of living plants Seed “predators” = granivores “Parasites” – live in close association with their host plants, e.g., parasitic plants, aphids, nematodes, etc. “The overwhelming majority of all species interactions occur between herbivorous insects and plants, simply because these two groups comprise half of the macroscopic species on Earth…” (Strong 1988; Perhaps a bit of an overstatement, but nevertheless conveys the importance of plant-herbivore interactions) Photo of Don Strong from U. C. Davis Herbivory Herbivory (a broad definition): the consumption of all or parts of living plants Grazers – consume plant parts (mostly green) near the substrate, e.g., snails graze algae, antelope graze grass; including roots (a relatively unexplored frontier) Browsers – consume plant parts (mostly green) well above the substrate, e.g., deer browse the leaves of shrubs and saplings Frugivores – consume fruits, often without damaging the seeds within, in which case the relationship is likely to be mutualistic Herbivory Can herbivory of “green parts” ever be advantageous to the plant? Compensation & overcompensation – increases in growth or reproduction beyond what would occur in the absence of herbivory; no net difference in fitness for consumed vs. unconsumed plants (compensation), or an advantage to consumed plants (overcompensation) See: McNaughton (1983); Belsky et al. (1993) Results supposedly supporting compensation or overcompensation usually depended on faulty logic or false assumptions (e.g., aboveground plant production is proportional to total plant production) Overall assessment: herbivory entails net costs (ardent defenders of compensation & overcompensation notwithstanding) Costs of Herbivory Complete defoliation that precludes reproduction (owing to death, etc.) obviously results in net costs; e.g., Gypsy moth (Lymantria dispar) defoliation Less conspicuous damage may have significant costs that are difficult to assess without experimentation (e.g., grazing of ovules; partial defoliation resulting in decreased carbon budget) Photos from Wikipedia Costs of Herbivory Water calyces dissuade floral herbivores P < 0.01 Chrysothemis friedrichsthaliana Osa Peninsula, Costa Rica Photos from Greg Dimijian (plant) & Jane Carlson (moth); Figure redrawn from Carlson & Harms (2007) Costs of Herbivory Piper (Piperaceae) – tropical and sub-tropical shrubs (~1400 species); includes black pepper Observations: Marquis (1984) examined herbivory on Piper arieianum in forest understory, La Selva, Costa Rica. Highly variable among plants: mean damage 1 - 6% leaf-tissue loss over 2 - 3 mo. Leaves often live ~2.5 yr; total lifetime losses can be substantial. Missing leaf area on entire plants ranged 4 - 50%. Photo of a species of Piper (not P. arieianum) from Wikipedia Costs of Herbivory Methods: Marquis (1984) experimentally removed leaf area with a hole-punch Treatments: 0, 10, 30 & 50% of the plant’s total leaf area removed, plus 100% removal of leaf area (mimicking leaf-cutter ant damage); he then assessed growth and reproduction over 2 yr Results: Small- and medium-sized plants suffered ~50% reduction in growth with 30% defoliation; seed production dropped ~50% for both years after defoliation Conclusion: Herbivory is costly Confronted with damaging herbivory, why is the (nondesert / non-polar terrestrial & near-shore) world green? Hairston, Smith & Slobodkin (1960; “HSS”) speculated that since “the world is green” herbivores must fail to limit the plants they feed on, so herbivores must be limited by their own predators In addition, since herbivory is costly to plants – even when it isn’t fatal – plants are expected to evolve defenses against herbivores; in this case, the abundance of food for herbivores would be illusory Costs of herbivory favor the evolution of defenses Methods: Marquis (1984) grew clones of several genotypes in understory experimental arrays Results: Variation in resistance to herbivory had a genetic component Conclusions: Large effects of damage on growth & reproductive output coupled with genotypic variation in susceptibility to damage suggests that defensive characters are under continuous selection Photo of a species of Piper (not P. arieianum) from Wikipedia Plant defense traits Plants use a variety of mechanical (toughness, spines, etc.), chemical (alkaloids, phenolics, terpenoids, latex, etc. – the realm of chemical ecology), developmental, and phenological defenses Defenses may also be classified with reference to their production: Constitutive – produced by & present in the plant irrespective of attack Induced – produced by & present in the plant in response to attack Derek McDonald E.g., Acacia trees that are protected from browsing giraffes produce fewer, shorter thorns (Young 1987); thorns are constitutive, but exhibit inducible characteristics Plant defense traits Tiffin (2000) Resistance traits – those that “reduce herbivory” Avoidance (antixenosis) traits – those that “affect herbivore behavior;” i.e., deter or repel herbivores Antibiosis traits – those that “reduce herbivore performance” Tolerance traits – those that “reduce the impact of herbivory on fitness” Resistant Tolerant Slide courtesy of Alyssa Stocks Hakes; modified from the original Susceptible Benefits of defense are obvious in the presence of herbivores Resistant Tolerant Slide courtesy of Alyssa Stocks Hakes; modified from the original Susceptible Costs of defense are obvious in the absence of herbivores Resistant Tolerant Slide courtesy of Alyssa Stocks Hakes; modified from the original Susceptible Resistance-related Plant Traits Slide courtesy of Amanda Accamando; modified from the original Resistance-related Plant Traits: Direct Defense Secondary Metabolites Toxic chemicals E.g., Tannins Slide courtesy of Amanda Accamando; modified from the original Tim Ross Anti-nutritive compounds James H. Miller, USDA Forest Service Resistance-related Plant Traits: Direct Defense Morphological Characteristics Leaf Toughness http://remf.dartmouth.edu/imagesindex.html Trichomes Slide courtesy of Amanda Accamando; modified from the original Thorns Chris Evans, River to River CWMA, Bugwood.org Secondary Chemistry Milkweeds (Asclepias spp.) Cardenolides Morphological Characteristics Physical Barriers • Toxic to many herbivores • Specialist counteradaptations • Trichomes • Latex Agrawal and Fishbein 2008; EcoEd Digital Library; monarchwatch.org Slide courtesy of Amanda Accamando; modifid from the original Resistance-related Plant Traits: Indirect Defense Natural Enemies recruited by: EcoEd Digital Library Plant Volatile Emissions www.usda.gov Extrafloral Nectaries Slide courtesy of Amanda Accamando; modified from the original http://aggie-horticulture.tamu.edu/gavelston Plant Defense How do plants optimize types & levels of defense? Resources Slide courtesy of Amanda Accamando; modified from the original Trade-offs & constraints High Costs + High Benefits constraint line Trait Y Low Costs + Low Benefits Low Costs + Low Benefits Trait X High Costs + High Benefits Trade-offs & constraints A jack-of-all-trades is master of none… Adam Smith (1776) – applied the concept to economics Robert MacArthur (1961) – applied the concept to evolutionary ecology So most organisms become the master of one (or a few), i.e., they specialize Trade-offs & constraints (Allocation) Size of eyes Size of horns From Emlen (2000) Trade-offs & constraints (Design) Performance on branches Performance on ground From Losos et al. (2004) The efficacy of defenses against herbivores Observations: Adler (2000) realized that hemiparasitic plants that obtain “secondary chemicals” from their hosts would serve as good experimental subjects Methods: Adler (2000) grew Indian paintbrush (Castilleja indivisa) with either “sweet” or “bitter” lines of lupines (Lupinus albus) – that differ in alkaloid production – and she followed their fates Results: Lynn Adler Hemiparasites grown with “bitter” hosts suffered lower herbivory, and experienced increased seed set Conclusions: “Secondary chemicals” can indeed serve as beneficial plant defenses Plant Defense Theory Ehrlich & Raven (1964) – Proposed a biochemical co-evolutionary hypothesis to explain why plants differ in their chemical defenses & why herbivores differ in their ability to detoxify, tolerate, or otherwise handle specific chemical defenses Plants evolve defense chemicals in response to attacks by insects, while insects counterevolve detoxification systems Adaptation to the host-plant chemicals of one host trades-off against the ability to consume other hosts Chemical arms races result in related plants having complexes of defenses that exclude all but their own specialist herbivores (that are generally themselves closely related) Photo from Greg Dimijian Co-evolution Co-evolution (microevolutionary focus)… “An evolutionary change in a trait of the individuals of one population in response to a trait of the individuals of a second population followed by an evolutionary response by the second population to the change in the first” Janzen (1980) Diffuse co-evolution… “…occurs when either or both populations in the above definition are represented by an array of populations that generate a selective pressure as a group” Janzen (1980) Co-cladogenesis Co-cladogenesis (e.g., co-speciation; macroevolutionary focus)… Host Herbivore Plant Defense Theory Ehrlich & Raven (1964) is incomplete; it does not anwer: Do contrasting ecological circumstances favor different types of defenses? Do contrasting ecological circumstances favor different levels of defenses? Why do plants differ in overall vulnerability to herbivores? Etc… Plant Defense Theory Plant-apparency theory (Feeny 1976; Rhoades & Cates 1976): Apparent plants: Trees, shrubs, and grasses from late successional communities with long generation times Unapparent plants: Short-lived herbaceous plants of early successional environments Plants that are easily found by herbivores (apparent plants) should invest heavily in quantitative defenses that make them less digestible to all herbivores. “Quantitative” because their effect is proportional to their concentration. These defenses are costly. Plants that are difficult to locate (unapparent plants) should invest smaller amounts in qualitative defenses that are effective against all but specialist herbivores. These defenses are less costly. Plant Defense Theory Plant-apparency theory arose especially out of Feeny’s studies on oaks (apparent) and wild mustards (unapparent) in central New York Oaks: Defensive chemicals are primarily tannins, that stunt larval growth and reduce fecundity of insects when they reach maturity; oaks only suffer major outbreaks during early spring bud-breaks before tannin concentrations in expanding leaves reach toxic concentrations Mustards: Very low concentrations of a variety of glucosinolates, toxic at extremely low doses to all but a few specialist herbivores “Apparent” “Unapparent” Plant Defense Theory Ecological correlates of plant defenses according to plant-apparency theory (from Howe and Westley 1988) Examples Properties Qualitative defenses Alkaloids, cyanogens, terpenes Small toxic molecules Distribution in plant New leaves, buds Distribution among plants Rare, short-lived herbs; Early successional plants Advanced angiosperms Phylogeny Favored in “unapparent” plants Quantitative defenses Cellulose & lignins (fiber), silica, phenolics, tannins Complex polymers Permanent woody tissue Common long-lived; Late successional plants Also in ancient ferns, gymnosperms Favored in “apparent” plants Plant Defense Theory Limits to plant-apparency theory: Futuyma’s (1976) review found some support, but also many exceptions Apparency is difficult to measure objectively Can plant traits be more directly linked to mechanisms of defense? Plant Defense Theory Resource-availability theory (Coley et al. 1985) Optimum strategy of defense is mediated by a plant’s capacity to replace lost parts with resources at its disposal Whereas plant-apparency theory stresses the economics of herbivore foraging efficiency, resource-availability theory stresses the economics of plant growth & differentiation (especially allocation) According to resource-availability theory, inherent growth rate and resource availability are determinants of the amounts and kinds of defenses that plants employ Photo of Coley from U. Utah Species with high intrinsic growth rates are adapted to life in a high resource environment Plants that grow rapidly in highresource environments can inexpensively & quickly replace tissues lost to herbivores (i.e., the costs of herbivory are low) Why invest in costly immobile defenses that will be discarded after a few months anyway? Coley et al. (1985) Species with high intrinsic growth rates are adapted to life in a high resource environment Species with low intrinsic growth rates are adapted to life in a low resource environment For slow growing plants in low resource environments it is costly to replace lost tissue Coley et al. (1985) Species with high intrinsic growth rates are adapted to life in a high resource environment Species with low intrinsic growth rates are adapted to life in a low resource environment Species that differ in intrinsic growth rate and habitat preference should differ in the optimal levels (arrows) of defense investment to maximize realized growth rates Coley et al. (1985) Cumulative defense cost Immobile defenses (lignins, tannins) have a saturating cumulative cost curve owing to low turnover Leaf lifetime Coley et al. (1985) Mobile defenses (toxic, small molecules) have a monotonically increasing cumulative cost curve because they continuously turn over Cumulative defense cost Immobile defenses (lignins, tannins) have a saturating cumulative cost curve owing to low turnover Leaf lifetime Coley et al. (1985) Immobile defenses (lignins, tannins) have a saturating cumulative cost curve owing to low turnover Where growth is slow, costly replacement means tissues should be “built to last”, and plants should use immobile defenses (lignin and tannins) that are permanently employed and less expensive over the long term Immobile defenses advantageous Cumulative defense cost Mobile defenses (toxic, small molecules) have a monotonically increasing cumulative cost curve because they continuously turn over Mobile defenses advantageous Leaf lifetime Some live to 14 yr Coley et al. (1985) What subtle assumption is being made? Benefits are equivalent for mobile vs. immobile defenses Immobile defenses advantageous Cumulative defense cost Mobile defenses advantageous Leaf lifetime Coley et al. (1985) Plant Defense Theory Hypotheses Defense & Environment Resource Availability Ho: Defense increases in low resource environment Coley et al. (1985) Growth Differentiation Balance: Herms & Mattson (1992) Compensatory Continuum Ho: Defense decreases in low and high resource environment Maschinski & Whitham (1989) Tolerance decreases in low resource environment Defense-Stress Cost Ho: Defense decreases under competition Siemens et al. (2003) Defense-Stress Benefit Ho: Defense increases under competition Siemens et al. (2003) Associational Resistance: Tahvanainen & Root (1972) Associational Susceptibility: Brown & Ewel (1987) Location by resistant neighbors lowers susceptibility of focal plant Location by susceptible neighbors lowers resistance of focal plant Slide courtesy of Alyssa Stocks Hakes; modified from the original Herbivory does not occur in isolation from other species-interactions Costs of herbivory differ depending on food-web architecture… Observations by Steinberg et al. (1995): Kelp from NW coast of the U.S. experience low herbivory rates (because otters limit urchin populations); U.S. kelp are consequently poorly defended No otters, but plenty of urchins in Australia; herbivory rates are much higher; Australian kelp have 6 times higher concentrations of phenolics Australian urchins relish U.S. kelp; U.S. urchins can’t eat Australian kelp Herbivory does not occur in isolation from other species-interactions Herbivory may increase the costs of other species interactions… Herbivores often damage plants such that plant pathogens may enter (Marquis and Alexander 1992) Leaf-chewing insects… Bark-browsing mammals… Phloem- and xylem-tapping insects… Stem-boring insects… Root-boring insects… All may provide entry points for fungi, bacteria, nematodes, & other pests, parasites, & pathogens to bypass the plant’s external physical defenses Herbivory does not occur in isolation from other species-interactions Herbivory, plant defense, and the third trophic level… Plants often exploit the third trophic level to defend themselves Pioneers are commonly myrmecophytes (“ant plants”) because abundant light allows them to make sugar and lipid awards relatively cheaply Herbivory does not occur in isolation from other species-interactions Herbivory, plant defense, and the third trophic level… van Bael et al. (2003) assessed the impact of the third trophic level on herbivory in the canopy of tropical forests Methods: Bird exclosures vs. controls on paired branches, both in canopy and understory Results: Bird exclusion increased herbivory in the canopy, but not in the understory Conclusions: The impact of the third trophic level, and the nature of trophic cascades, differs with productivity Ghosts of Herbivory Past Is the “divaricate” architecture of several species of shrub in New Zealand an adaptation to browsing by extinct moas? (Greenwood & Atkinson 1980) Photo from http://haasep.homepage.t-online.de/research.htm