HERBIVORY

1. HERBIVORY

2. 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

3. 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

4. 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)

5. 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

6. 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)

7. Costs of Herbivory Piper (Piperaceae) – tropical and sub-tropical shrubs (~1400 species); includes black pepper Observations: Marquis (1984) examined herbivory on Piperarieianum 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

8. 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

9. Confronted with damaging herbivory, why is the (non-desert / 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

10. 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 hada 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

11. 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 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

12. 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”

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

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

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

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

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

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

19. Secondary Chemistry Morphological Characteristics Milkweeds(Asclepias spp.) Cardenolides • Toxic to many herbivores • Specialist counter-adaptations 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: www.usda.gov • Plant Volatile Emissions • ExtrafloralNectaries EcoEd Digital Library Slide courtesy of Amanda Accamando; modified from the original http://aggie-horticulture.tamu.edu/gavelston

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

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

23. 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

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

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

26. 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: Hemiparasites grown with “bitter” hosts suffered lower herbivory, and experienced increased seed set  Lynn Adler Conclusions: “Secondary chemicals” can indeed serve as beneficial plant defenses

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 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)

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

30. 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…

31. 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.

32. 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 “Apparent” Mustards: Very low concentrations of a variety of glucosinolates, toxic at extremely low doses to all but a few specialist herbivores “Unapparent”

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

34. 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?

35. 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

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

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

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

40. 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 Mobile defenses Immobile defenses Cumulative defense cost Leaf lifetime Coley et al. (1985)

41. 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 Mobile defenses Immobile defenses Cumulative defense cost Leaf lifetime Some live to 14 yr Coley et al. (1985)

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

43. Plant Defense Theory 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

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

45. Plant Defense Theory 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

46. Plant Defense Theory 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.

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

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