Herbivory

1. Herbivory • What is herbivory? • What kinds of impacts do herbivores have in nature? • Why is the Earth green? • Control of herbivores by carnivores • Plants fight back: plant defenses • Importance of herbivores economically

2. What is herbivory? • Herbivory is the eating or consumption of plants (primary producers) or plant material by animals known as primary consumers • Heterotrophs • Autotrophs • Herbivory, like parasitism & predation, is a +,- interaction • Herbivory is important because plants are the ultimate source of energy for food webs in most environments.

3. Are all herbivores equal? Feeding Specialization • Specialists: • Koalas • Monarch caterpillars • Generalists: • Deer • Cows • Leaf-cutter ants • The degree of feeding specialization is more like a continuum

4. What are the various ecological effects of herbivores? • Herbivores can affect plant fitness • Reduce plant growth rate • Reduce plant reproductive output • Directly as seed predators • Indirectly by reducing plant biomass • Herbivores can control plant distribution and abundance • Through alterations of plant distribution patterns and relative abundances, can alter plant community structure and composition • The effects of herbivores on plants often depend on the degree of feeding specialization.

5. Herbivores can control their “prey” (plants) under some circumstances • Example: Prickly pear cactus (Opuntia stricta) and cactus moth • Introduced to Australia in 1839, came to cover large areas by 1925, destroying rangeland. • Several herbivores were introduced to try to control the plant • In 1925, cactus moth (Cactoblastis cactorum--moth larva) was introduced from South America, with great success controlling the prickly pear

6. Klamath weed (St. John’s wort (Hypericum perforatum) became a pest as an invasive species in California; it was finally controlled by an introduced (biological control) leaf beetle (Chrysomelid: Chrysolina).

7. Lessons from prickly pear and Klamath weed examples? • Invasive plant such as prickly pear, introduced to Australia without its co-evolved herbivore control agents, was able to spread rapidly and become a pest • A specialized herbivore was able to bring the plant totally under control • However, this example involved introduced organisms, and thus a potentially artificial situation... how general is this phenomenon of herbivores controlling plant populations? • In a 1991 review of efforts to control plant weeds biologically, using herbivores (N = 701 cases), noticeable control by herbivore occurred in only 26% of cases, so herbivores certainly are not always effective!

8. Third example: Eucalyptus Native Eucalyptus trees of Australia were 100% taller when native herbivorous insects were experimentally removed compared with controls

9. Cattle grazing can radically alter plant communities Effects of cattle grazing on plant communities, Mauna Loa Volcano, HawaiiAgain, this example is artificial, involving a domesticated herbivore.

10. Herbivores can alter plant species dominance patterns by feeding selectively on dominant interspecific competitors: E.g., Bison feeding in Great Plains feed selectively on C4 plants (tall grasses), allowing more light at ground level and a greater proportion of C3 plants to thrive (see text).

11. “Why is the Earth Green?” • Why don’t herbivores eat more of the terrestrial plant biomass? • What controls abundance of herbivores? • Two basic answers involve trophic interactions: • Predators and parasites control herbivore abundance • Plants defend themselves (particularly terrestrial plants) • We’ll look at these answers one at a time…

12. Top-down control of herbivores • Theory put forth in basic form by Hairston, Smith, & Slobodkin (HSS) in 1960 paper • Assumptions & assertions of HSS study: • Most terrestrial ecosystems have just three trophic levels • Plants generally limited by resource availability (not by herbivores) • Herbivores generally limited by their predators and parasites • Carnivores generally food-limited, since their predators are rare or absent • Any system with an odd number of trophic levels follows this scheme

13. Consequences of this HSS theory? Predator • Top-down trophic cascade of effects from carnivore to plant • Carnivores tend to compete with each other for food, and plants also, but herbivores tend to compete less (controlled by predators) • This theory was based on much empirical support, but few if any direct tests at the time of indirect effects such as benefit by carnivores to plants by controlling herbivores. • Better tested in aquatic systems - + Herbivore + + - Plant

14. Empirical support from experiments: Marquis & Whelan (1994) show cascading top-down effects • Three treatments on white oak saplings in Illinois: (1) spray saplings with insecticide to remove insect herbivores (caterpillars), (2) cages to exclude birds & thus protect caterpillars, (3) controls (untreated trees) • Predict that insect herbivore densities on plants would be in following order: cages > control > insecticide • Predict, furthermore, that + indirect effects (plant benefits) would be observed in following order: insecticide > control > cages

15. Results of Marquis & Whelan study • Greatest leaf damage & herbivore density in cages where protected from carnivorous birds • Leaf biomass greatest where herbivores least abundant: spray & control (fewer caterpillars) had more biomass than cages (with most caterpillars) • Different letters over bar indicate statistically significant differences

16. Results of Marquis & Whelan study, continued: Indirect effects of birds on plants Indirect effects of birds shown by larger leaf sizes in controls compared to cages, and in spray treatment (simulates “super carnivores”) compared to controls.

17. Sea otter-sea urchin-giant kelp community shows similar results • When sea otters present, they control sea urchins, allowing huge communities of giant kelp • When sea otters removed (e.g., by over hunting), sea urchins released from control, and themselves devour giant kelp beds. • Many experimental studies in aquatic communities show same top-down effects (phytoplanktonzooplanktonzooplanktivorous fish; fish control zooplankton, allowing phytoplankton to flourish)

18. Why is the Earth green? Plants fight back! • Defenses come in many forms: • Mechanical • Phenological • Hormonal • Biotic • Biochemical

19. Mechanical defenses against browsers, grazers, etc.: • Leaf toughness • Spined leaf margins • Thorns, spines

20. Honey locust tree • Common in Jean Lafitte Park • Presumably the very sharp thorns on trunks & branches evolved to defend against large climbing herbivores that are now extinct in N. America (e.g., giant sloth)

21. Some generalizations about situations where mechanical defenses have evolved (Peter Grubb) • Open sites, such as deserts, where plants are close to ground & thus vulnerable to grazers (also benefit of producing thorns, etc., outweighs costs because of expense of replacing lost tissue in desert) • Plants with only one meristem (such as palms) often spiny, to protect apical meristem • Evergreens such as American holly may be spiny (common in Louisiana upland forests) because they face severe herbivore pressure in winter when other plants have lost their leaves

22. Phenological Defense Mast fruiting to swamp seed predators-e.g., oaks, bamboos

23. Hormonal Defense Reproductive inhibition (e.g., firs, genus Abies, produce insect hormone derivatives that inhibit metamorphosis of insect herbivores)

24. Biotic Defense Mutualisms for defense--e.g., ant acacias use ants to protect foliage

25. Biochemical Defense:Green Desert • Chemical plant compounds—these are often referred to as secondary chemicals (i.e., 2º metabolites) • Plants produce a huge variety of compounds, in widely varying amounts

26. Chemical defensive compounds can be classified into broad classes • Quantitative defenses = substances eaten in large amounts by herbivores that impede digestion. Tend to be carbon-based. • E.g., tannins (phenolics) in oak trees, resins (terpenoids) in long-leaf pine that fight off attacks of southern pine beetle • In some cases these tannins affect herbivores’ feeding preferences: e.g., a variety of browsers (goats, kudus, impalas) rejected a variety of plants with > 5% condensed tannins • In general condensed tannins tend to attach to cellulose and fiber-bound proteins, acting against microbial and fungal attack, thus affecting also some vertebrates; hydrolyzable tannins tend to inactivate digestive enzymes of herbivores • Slow development times, prolonging exposure to predators and parasitoids

27. Chemical defensive compounds can be classified into broad classes • Qualitative defenses – often toxic compounds that can deter feeding or affect herbivores after ingestion of small doses. Often nitrogen-based • Hypericum (Klamath Weed--see example earlier in lecture) contains alkaloid hypericin, evolved to protect it from many insect herbivores…and it’s also toxic to cattle. • What are some other examples of qualitative defenses?

28. Examples of secondary compounds used in defense against herbivores • THC in marijuana is an alkaloid, a nitrogenous secondary compound • Mustards in the family Cruciferae contain glucosinolates, another nitrogenous class of defensive compounds • Queen Anne’s lace in family Umbelliferae contains furanocoumarins, belonging to the flavanoids (phenolic, carbon-based compounds) • Tobacco contains nicotine, another alkaloid

29. Generalizations about these two kinds of chemical defense? • Quantitative defenses tend to be found in plants that are highly apparent to herbivores (long-lived, large), especially K-selected species like oak trees • Qualitative defenses tend to be most important in species that are un-apparent, especially herbaceous and other r-selected (weedy) species • Note that many exceptions exist to the above assertions • Induced defenses (both physical, and chemical) are facultative defenses that are strengthened in proportion to consumption of plant material by herbivore (e.g., oaks increase production of tannins in response to herbivory; browsed Acacia depranolobium trees in Kenya have longer thorns than unbrowsed trees)

30. Evolutionary “Arms Race” Between Plants and Herbivores • Complex plant-herbivore interactions may have resulted from a long evolutionary history • Some herbivores have evolved to benefit from, even depend on chemicals originally evolved as defense • These herbivores, often specialists on a particular plant group, have evolved the ability to use secondary chemicals as protection against the herbivores’ natural enemies (e.g., wasps, birds) • An example of this is Monarch butterflies, which feed on milkweeds and use the cardenolides (terpenoids) from the plants as defensive compound against birds which find the monarchs to be toxic (famous series of experiments done by Browers using blue jays as predators)

31. Plants often produce a combination of several chemical defenses • Why? • Synergism • Many herbivores • But, this strategy may be expensive

32. Piper cenocladum Beetles Ants Herbivores Plants

33. Herbivory is extremely important economically, and huge scientific effort goes into controlling the negative impacts of herbivores in agricultural systems • Pesticides • Biological control • Integrated pest management (use of biological control, coupled with judicious use of pesticides)

34. Conclusions: • Herbivores can in unusual situations completely control the plants on which they feed, consuming essentially all the available leaf tissue biomass • Normally herbivores in terrestrial environments, at least, do not consume much of the green (photosynthetic) biomass…why? • Plants fight back with diverse weapons (part of a co-evolutionary arms race involving plants and their herbivores). • Herbivores are a major factor influencing agricultural productivity, and scientists have developed a variety of strategies, such as integrated pest management, to try to control herbivores.