Herbivory

1. Herbivory Top-down effects in communities: Assumption that top predators regulate lower trophic levels of consumer organisms assumes that food is not limiting (e.g lemmings and stoats) Is the abundance of food an illusion?? Assess here: - costs of herbivory - plant defense theory - trade-offs of defense with other life-history traits and significance for species coexistence

2. Cost of herbivory Obvious costs when complete defoliation of plants precludes reproduction or results in death (e.g. Gypsy moth defoliation of oak trees) Less conspicuous herbivores may have significant costs that are difficult to assess without experimentation (e.g. grazing of ovules or undispersed seeds affecting reproductive output, or partial defoliation resulting in decreased carbon budget) Marquis (1984) Looked at the effect of simulated leaf herbivory by a weevil Ambetes on an understorey tropical shrub Piperarieianum in Costa Rica

3. Piper (Piperaceae) large genus of tropical and sub-tropical shrubs (~1400 spp) both pioneers and understorey species Includes black pepper Looked at herbivory to Piperarieianum in forest understorey at La Selva in Costa Rica. Herbivory rates were very variable among plants 1-6 % lost over 2-3 months, but leaves live up to 2.5 years therefore total losses over the leaf life time can be substantial - One time measure of missing leaf area on entire plants ranged between 3 and 50 %

4. - Cloning of plant material and transplanting to understory indicated that variation in herbivory rate has a genetic component - Experimentally removed leaf area with a hole-punch to mimic the pattern of natural damage - some leaves lots of damage others remove little tissue… - Treatments of 0, 10, 30 and 50 % of the plant’s total leaf area removed, plus 100 % removal of leaves (mimicking leaf-cutter ant damage - Tracked growth and reproduction over following 2 years Results: Small and medium sized plants showed a 50 % reduction in growth with > 30 % defoliation measured over the two years Seed production dropped in half for both first and second years after defoliation

5. Large effects of damage on growth and reproductive output in Piper coupled with genotypic variation in susceptibility to damage suggests that defensive characters of Piper are under continuous selection • Coley (1986) found similar effects in Cecropia peltata • Measured growth and herbivory rates of seedlings grown from seeds of several parent trees • Measured tannin levels in foliage as major chemical defense • -Wide variation in tannin levels among plants • Found that plants with high tannin levels had low herbivory rates, but also had lower growth rates.

6. Plant defense theory - Under what conditions to plants evolve different kinds of defenses? - What are the predictors for the level of defense exhibited? Biochemical coevolution theory: Ehrlich and Raven (1964) - Plant species evolve secondary compounds in response to attacks by insects, while insects evolve new detoxification systems to over-come them - Adaptation to a set of host plant chemicals results in losing the ability to consume other hosts - Chemical arms races eventually results in plant families acquiring a complex of defenses that exclude all but a fauna of related taxa of specialist herbivores - Can explain patterns of specialist herbivores (e.g. Berenbaum 1983), but does not address wider issues:

7. Why do most vertebrates (and many insects) have wide host preferences? Why do plants differ so much in vulnerability to herbivores? Plant apparency theory (Feeny 1976) Plants that are easily found by herbivores (‘apparent’ plants) should invest heavily in quantitative defenses that are effective against all herbivores. Plants that are difficult to locate (‘unapparent’ plants) should invest smaller amounts in qualitative defenses that are effective against all but specialist herbivores Apparent plants: Trees and shrubs, and grasses from late successional communities with long generation times Unapparent plants: Short-lived herbaceous plants of early successional environments

8. Ecological correlates of plant defenses according to apparency theory (from Howe and Westley 1988) Apparency theory arose out of Feeny’s studies on Oaks (apparent) and mustard plants (unapparent) in central New York Mustard: very low concentrations of a variety of glucosinolates, toxic at extremely low doses to all but specialist feeders

9. Oaks: defensive chemicals are primarily tannins. Stunt larval growth and reduces 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 Limits to apparency theory: Futuyma (1976) reviewed literature on defenses - some correspondence but some apparent plants had qualitative defenses as well as quantitative defenses and some herbs had high phenol concentrations. Apparency is difficult to measure. Need more explicit hypotheses linking plant traits to constituents of defense

10. Resource availability theory: Coley et al (1985) Proposed that plant defensive capabilities are mediated by their capacity to replace lost parts with resources at their disposal. While apparency theory stresses herbivore foraging efficiency Resource availability stresses economics of growth: inherent growth rate, and nutrient availability as determinants of the amounts and kinds of defenses that plants use. Fast-growing plants in well-lit environments with fertile soils can easily replace leaves or other tissues lost to herbivores (‘cost of herbivory’ is low).

11. Resource availability theory predicts that these plants should invest relatively little in defense, and should use mobile resources that can be moved out of quickly senescing tissue - Why invest costly immobile defenses in tissues that will be discarded after a few months anyway? Slow growing plants, characteristic of low resource environments (eg deserts, forest understory) should invest more in defense because tissue is costly to replace. Costly replacement means tissues should be ‘built to last’ and can use more immobile defenses (lignin and tannins) that are permanently employed in leaves and stems and less expensive in the long run - Plant structures in low resource environments can be extremely long-lived (e.g 14 year old leaves in tropical forest understory)

12. Plants varying in intrinsic growth rate and habitat preference should differ in the optimal level of defense investment to maximise realized growth rates Vertical arrows indicate optimal defense investment to maximize growth rate

13. Can argue the opposite: 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 Can therefore think of allocation to defense as imposing a trade-off on plants that limits the range of microsites in which recruitment can occur: Growth-defense (or growth-mortality trade-off) High investment in defense = low growth rate and low mortality rate. Plants grow in shade Low investment in defense = high growth rate and high mortality rate (in shade). Plants constrained to sunny sites

14. Kitajima (1994) highlighted this trade-off and shifted a paradigm which stressed physiological traits as determining shade-tolerance to one in which allocation patterns are emphasized Plants that grow fastest in high light (24 % full sun) also grow fastest in shade (2 % full sun) Individual points on graph represent species (n=13) varying in ‘shade tolerance’

15. Growth rate in sun or shade is positively correlated with mortality rate in the shade In Kitajima’s growing house experiment mortality was attributable to fungal pathogens

16. 1.0 0.8 0.6 0.4 0.2 0.0 0 10 20 30 40 1.0 0.8 0.6 0.4 0.2 0.0 0 10 20 30 40 a) Growth - mortality for pioneer species in small gaps (10 % Full sun) Proportional seedling mortality Dalling & Hubbell 2002 b) Mortality is attributable to browsing damage and insect herbivores Proportion of seedlings with apical damage Maximum daily relative height growth mm/mm/day x 1000

18. Growth-mortality trade-off driven by herbivores/pathogens has important implications for understanding species distribution patterns: • Among site variation in the ‘cost of herbivory’ • Among site variation in intensity of herbivory • Understanding species invasions

19. Resource availability theory arose out of community wide studies of herbivory. Coley (1983) measured herbivory rates and characterized plant defenses of 46 tree species in lowland forest, Panama - Multivariate analyses to determine what traits correlated with damage: leaf toughness>fiber content>nutritive value - Pioneer species have least tough leaves, lowest phenolics and 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 than mature leaves - young leaves have not toughened but have 2-3 times [phenolics] of mature leaves - Several common adaptations to minimize damage to young leaves (rapid expansion, synchronous leaf flush, delayed greening)

20. Delayed greening Young leaves are white or pink and do no net photosynthesis Only observe delayed greening in tropical forest understories, but is a common trait across evolutionary lineages

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

22. Rapid leaf expansion Develop whole leaves (or branches in a few days) Brownea claviceps

23. Herbivory and the third trophic level “Inviting friends to feast on foe” - Many ways that plant harness the third trophic level to defend themselves: - fast growing trees are commonly ant plants because abundant light allows them to make sugar and lipid awards relatively cheaply - mites are also common, but little studied (Walter and O’Dowd 1992). Mites live in domatia and feed on fungal spores and so might be important in protecting plants against pathogens?? In N. Queensland 15 % of trees have domatia (O’Dowd and Wilson 1989)

24. Quantitative defenses slow down insect feeding and/or digestion rates ‘Quantitative’ defenses (tannins, fiber and toughness) are clearly effective anti-herbivore defenses. Yet they do not present an absolute barrier against herbivores. Their effectiveness may be due to mediation by the third trophic level -Slowing grazing rates is important because most damage occurs in the last instars of insect development -Slowing rates also lengthens the time that larvae are exposed to predators and parasitoids (‘slow-growth-high-mortality’ SG-HM hypothesis)

25. Evidence for SG-HM: Benrey and Denno (1997) - Several studies using ‘free-living’ larvae show higher incidence of mortality from parasitoids for slow vs fast developing larvae. - Not supported in cases where larvae are protected (building shelters out of plant material or inside galls) Fast developing larvae are better able to defend themselves against parasitoids instar

26. Some plants may also send out a distress signal… (see lots of neat work by Karban et al at UC Davis on jasmonate signalling) Thaler (1999) looked at the effect of Jasmonate a volatile chemical that induces chemical defence in plants. Compared parasitism of caterpillars in induced vs non-induced plants