1. HERBIVORY

2. 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…” Herbivory Photo of Don Strong from U. C. Davis (Strong 1988; Perhaps a bit of an overstatement, but nevertheless conveys the importance of plant-herbivore interactions)

3. 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 (a broad definition): the consumption of all or parts of living plants Herbivory

4. 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)

5. 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) Costs of Herbivory Complete defoliation that precludes reproduction (owing to death, etc.) obviously results in net costs; e.g., Gypsy moth (Lymantria dispar) defoliation Photos from Wikipedia

6. Water calyces dissuade floral herbivores P < 0.01 Chrysothemis friedrichsthaliana Osa Peninsula, Costa Rica Costs of Herbivory Photos from Greg Dimijian (plant) & Jane Carlson (moth); Figure redrawn from Carlson & Harms (2007)

7. 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%. Costs of Herbivory Photo of a species of Piper (not P. arieianum) from Wikipedia

8. 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 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

9. 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 Confronted with damaging herbivory, why is the (non- desert / non-polar terrestrial & near-shore) world green?

10. Costs of herbivory favor the evolution of defenses Photo of a species of Piper (not P. arieianum) from Wikipedia 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

11. 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 E.g., Acacia trees that are protected from browsing giraffes produce fewer, shorter thorns (Young 1987); thorns are constitutive, but exhibit inducible characteristics  Derek McDonald Plant defense traits

12. 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”

13. Slide courtesy of Alyssa Stocks Hakes; modified from the original Resistant Tolerant Susceptible

14. Benefits of defense are obvious in the presence of herbivores Slide courtesy of Alyssa Stocks Hakes; modified from the original Resistant Tolerant Susceptible

15. Slide courtesy of Alyssa Stocks Hakes; modified from the original Resistant Tolerant Susceptible Costs of defense are obvious in the absence of herbivores

16. Resistance-related Plant Traits Slide courtesy of Amanda Accamando; modified from the original

17. Resistance-related Plant Traits: Direct Defense Secondary Metabolites E.g., Tannins Toxic chemicals Anti-nutritive compounds Slide courtesy of Amanda Accamando; modified from the original Tim Ross

18. Resistance-related Plant Traits: Direct Defense Morphological Characteristics Leaf Toughness Trichomes Thorns Chris Evans, River to River CWMA, Bugwood.org James H. Miller, USDA Forest Service http://remf.dartmouth.edu/imagesindex.html Slide courtesy of Amanda Accamando; modified from the original

19. Secondary Chemistry Milkweeds (Asclepias spp.) Cardenolides Toxic to many herbivores Specialist counter- adaptations Morphological Characteristics Physical Barriers Trichomes Latex Agrawal and Fishbein 2008; EcoEd Digital Library; monarchwatch.org Slide courtesy of Amanda Accamando; modifid from the original

20. Resistance-related Plant Traits: Indirect Defense Natural Enemies recruited by: Plant Volatile Emissions Extrafloral Nectaries www.usda.gov http://aggie-horticulture.tamu.edu/gavelston EcoEd Digital Library Slide courtesy of Amanda Accamando; modified from the original

21. Plant Defense Resources Defense Growth & Reproduction How do plants optimize types & levels of defense? Slide courtesy of Amanda Accamando; modified from the original

22. Trait X Trait Y High Costs + High Benefits Low Costs + Low Benefits High Costs + High Benefits Low Costs + Low Benefits constraint line Trade-offs & constraints & constraints

23. 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

24. From Emlen (2000) Trade-offs & constraints (Allocation) Size of horns Size of eyes

25. From Losos et al. (2004) Trade-offs & constraints (Design) Performance on ground Performance on branches

26.  Lynn Adler The efficacy of defenses against herbivores 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: Hemiparasites grown with “bitter” hosts suffered lower herbivory, and experienced increased seed set Conclusions: “Secondary chemicals” can indeed serve as beneficial plant defenses Observations: Adler (2000) realized that hemiparasitic plants that obtain “secondary chemicals” from their hosts would serve as good experimental subjects

27. 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 counter- evolve 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

28. 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) Co-evolution 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)

29. Host Herbivore Co-cladogenesis (e.g., co-speciation; macroevolutionary focus)… Co-cladogenesis

30. 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

31. Plant-apparency theory (Feeny 1976; Rhoades & Cates 1976): Apparent plants: Trees, shrubs, and grasses from late successional communities with long generation times 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. 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. Unapparent plants: Short-lived herbaceous plants of early successional environments Plant Defense Theory

32. Mustards: Very low concentrations of a variety of glucosinolates, toxic at extremely low doses to all but a few specialist herbivores Plant-apparency theory arose especially out of Feeny’s studies on oaks (apparent) and wild mustards (unapparent) in central New York “Apparent” “Unapparent” 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 Plant Defense Theory

33. Ecological correlates of plant defenses according to plant-apparency theory (from Howe and Westley 1988) Favored in “apparent” plants Favored in “unapparent” plants Plant Defense Theory

34. 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

35. 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 Plant Defense Theory Photo of Coley from U. Utah

36. Species with high intrinsic growth rates are adapted to life in a high resource environment Coley et al. (1985) Plants that grow rapidly in high- resource 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?

37. 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 Coley et al. (1985) For slow growing plants in low resource environments it is costly to replace lost tissue

38. 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)

39. Leaf lifetime Cumulative defense cost Immobile defenses (lignins, tannins) have a saturating cumulative cost curve owing to low turnover Immobile defenses Coley et al. (1985)

40. Leaf lifetime Cumulative defense cost Immobile defenses (lignins, tannins) have a saturating cumulative cost curve owing to low turnover Mobile defenses (toxic, small molecules) have a monotonically increasing cumulative cost curve because they continuously turn over Immobile defenses Mobile defenses Coley et al. (1985)

41. Leaf lifetime Cumulative defense cost Immobile defenses (lignins, tannins) have a saturating cumulative cost curve owing to low turnover Mobile defenses (toxic, small molecules) have a monotonically increasing cumulative cost curve because they continuously turn over 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 Mobile defenses advantageous Immobile defenses advantageous Immobile defenses Mobile defenses Some live to 14 yr Coley et al. (1985)

42. Leaf lifetime Cumulative defense cost Mobile defenses advantageous Immobile defenses advantageous Immobile defenses Mobile defenses What subtle assumption is being made? Benefits are equivalent for mobile vs. immobile defenses Coley et al. (1985)

43. Resource availability theory arose out of community-wide studies of herbivory by Coley (1983, etc.) & colleagues (e.g., Bryant & Chapin) Coley (1983) measured herbivory rates and characterized plant defenses of 46 tree species in lowland forest, Panama Multivariate analyses to determine which traits correlated with damage: leaf toughness > fiber content > nutritive value Pioneer species have least tough leaves, lowest phenolics and lowest fiber concentration Mature leaves of pioneer trees were grazed six times more rapidly than leaves of shade-tolerant trees In 70% of species, young leaves suffered higher damage levels than mature leaves – young leaves have not toughened but have 2-3 times [phenolics] of mature leaves Plant Defense Theory

44. Growth and defense characters of tropical trees, from Coley (1983) and subsequent work

45. Grubb’s (1992) “positive distrust of simplicity” concerning plant defenses… Grubb suggested that a univariate approach to understanding the distribution of plant defenses among species (e.g., apparency or resource availability) was probably too simplistic Grubb suggested that a combination of variables determines the level & type of defense found in a given species, population, or individual plant, including: habitat productivity (resource availability), accessibility of the plant to herbivores, relative abundance of the plant (as in “apparency”), plant architecture, phenological pattern (especially relative to other plants in the vicinity), nutritious value of the plant (especially relative to other plants in the vicinity), and the type of herbivores present Plant Defense Theory

46. At any rate, allocation to defense is part of the resource budget of the plant; plants that allocate a large proportion of resources to defense have little left to invest in leaf production and therefore have low intrinsic growth rates Growth-defense (or growth-mortality) trade-off: High investment in defense = low growth rate and low mortality rate. Plants can grow in shade. Low investment in defense = high growth rate and high mortality rate (in shade). Plants constrained to sunny sites. Plant Defense Theory

47. Kitajima (1994) highlighted this trade-off and challenged the paradigm that favored physiological rates as the principle determinants of shade- tolerance; allocation patterns must also be considered Plants that grow fastest in high light (24% full sun) also grow fastest in shade (2% full sun) N = 13 species that vary in “shade tolerance” Kitajima (1994)

48. Growth rate in sun or shade is positively correlated with mortality rate in the shade Mortality was caused by fungal pathogens Allocation to defense may impose an allocation-based trade-off between growth and survivorship Kitajima (1994)

49. Slide courtesy of Alyssa Stocks Hakes; modified from the original Plant Defense Theory

50. Herbivory on a plant may be influenced by the diversity & composition of its neighborhood Plant Resistance: Neighbor Effects Slide courtesy of Amanda Accamando; modified from the original

51. Resource Concentration Hypothesis Hypotheses are interrelated and not necessarily mutually exclusive Associational Resistance Framework Enemies Hypothesis Repellant Plant Hypothesis Attractant -Decoy Hypothesis Slide courtesy of Amanda Accamando; modified from the original

52. Resource Concentration Hypothesis (Root 1973) Resource abundance and species richness in a patch influence herbivory Specialist herbivore abundance Specialist herbivore abundance Generalist herbivore abundance Generalist herbivore abundance Increased plant species richness Resource Concentration Hypothesis Enemies Hypothesis Repellant Plant Hypothesis Attractant-Decoy Hypothesis Slide courtesy of Amanda Accamando; modified from the original

53. Enemies Hypothesis (Root 1973) Tritrophic interactions influence herbivory Specialist herbivore abundance Specialist herbivore abundance Generalist herbivore abundance Generalist herbivore abundance Increased plant species richness Herbivore natural enemies Resource Concentration Hypothesis Enemies Hypothesis Repellant Plant Hypothesis Attractant-Decoy Hypothesis Slide courtesy of Amanda Accamando; modified from the original

54. Plant neighborhood composition influences herbivory Generalist herbivore abundance Generalist herbivore abundance Highly-defended neighborhood Resource Concentration Hypothesis Enemies Hypothesis Repellant Plant Hypothesis Attractant-Decoy Hypothesis Slide courtesy of Amanda Accamando; modified from the original Repellent Plant Hypothesis ( Atsatt & O’Dowd 1976 )

55. ‘Attractant Patch’ High herbivore pressure Susceptible → Resistant ‘Repellant Patch’ Low herbivore pressure Slide courtesy of Amanda Accamando; modified from the original Repellent Plant Hypothesis ( Atsatt & O’Dowd 1976 )

56. Attractant-Decoy Hypothesis ( Atsatt & O’Dowd 1976 ) Nearest neighbor influences herbivory Highly-defended nearest neighbor Resource Concentration Hypothesis Enemies Hypothesis Repellant Plant Hypothesis Attractant-Decoy Hypothesis Slide courtesy of Amanda Accamando; modified from the original

57. Specialist herbivore abundance Generalist Herbivore abundance Herbivore natural enemies Highly-defended neighbor Increased plant species richness Highly-defended neighborhood Resource Concentration Hypothesis Enemies Hypothesis Repellant Plant Hypothesis Attractant-Decoy Hypothesis Plants are interdependent with respect to the herbivore pressure they face Slide courtesy of Amanda Accamando; modified from the original

58. 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

59. 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

60. 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

61. Herbivory, plant defense, and the third trophic level… Plants often exploit the third trophic level to defend themselves Mites are also commonly found on plants, but relatively little studied (Walter and O’Dowd 1992). Mites may live in plant domatia & feed on fungal spores. In N. Queensland 15% of trees have domatia (O’Dowd and Wilson 1989). Herbivory does not occur in isolation from other species-interactions

62. “Quantitative” defenses (tannins, fiber and toughness) are apparently effective anti-herbivore defenses, yet they do not present an absolute barrier against herbivores. Their effectiveness may result in part from their influence on the third trophic level… Herbivory, plant defense, and the third trophic level… Plants often exploit the third trophic level to defend themselves. Herbivory does not occur in isolation from other species-interactions

63. Quantitative defenses slow down insect feeding or digestion rates Slowing rates is important because most damage occurs in the last instars of insect development Slowing rates lengthens the time that larvae are exposed to predators and parasitoids (“slow-growth-high-mortality” hypothesis) Herbivory, plant defense, and the third trophic level… Herbivory does not occur in isolation from other species-interactions

64. Quantitative defenses slow down insect feeding or digestion rates Slowing rates is important because most damage occurs in the last instars of insect development Slowing rates lengthens the time that larvae are exposed to predators and parasitoids (“slow-growth-high-mortality” hypothesis) Review of evidence for SG-HM: Benrey and Denno (1997): SG-HM was not supported in cases where larvae are protected (building shelters out of plant material or inside galls) Support for SG-HM in “free-living” larvae – higher mortality from parasitoids in slowly developing larvae Herbivory, plant defense, and the third trophic level… Herbivory does not occur in isolation from other species-interactions

65. van Bael et al. (2003) assessed the impact of the third trophic level on herbivory in the canopy of tropical forests Herbivory, plant defense, and the third trophic level… Conclusions: The impact of the third trophic level, and the nature of trophic cascades, differs with productivity 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 Herbivory does not occur in isolation from other species-interactions

66. Ghosts of Herbivory Past Photo from http://haasep.homepage.t-online.de/research.htm Is the “divaricate” architecture of several species of shrub in New Zealand an adaptation to browsing by extinct moas? (Greenwood & Atkinson 1980)