Herbivore-Plant Interactions 2 : Seed-Slayers

1. Herbivore-Plant Interactions 2 :Seed-Slayers Peter B. McEvoy Oregon State University

2. Outline • The nature of seed slaying • Characteristics of seeds • Taxa engaged in attack seeds • Species packing among fig bugs • Impact of seed slayers • On plant communities • On plant populations

3. Characteristics of Seeds • Nutrient values per unit volume high • Shorter time courses • Once dispersed, hard to find • Chemical defense might be greater – low self repair • Continuous seed production not required for survival of plant except in case of annual without a seed bank Result: Seed timing, quality and quantity can be more freely manipulated by natural selection that those same characteristics of leaves and other vegetative parts

4. Taxa engaged in seed slaying • Coleoptera (Curculionidae, Bruchidae) • Heteroptera (Lygaeidae, Phyrrhocoridae) • Lepidoptera (Pyralidae, Tortricidae, Olethreutidae, Lycaenidae) • Hymenoptera (Formicidae, Chalcidoidea) • Diptera (Tephritidae) • Mammals and Birds

5. Seed-Slaying Coleoptera:Seed weevils (Bruchidae) occasionally become pests of stored beans, cowpeas, and peas Pea Weevil Bruchus pisorum (Linnaeus) Acanthoscelides obtectus (Say) Bean weevil weevil Curculio glandium attacking acorn of English Oak Quercus robur

6. Seed Slaying Heteroptera (Lygaeidae, Phyrrhocoridae) Oncopeltus fasciatus Lygaeidae: Oncopeltus fasciatusfeeds on developing pods of milkweed, requires seeds for reproduction Pyrrhocoridae : Dysdercus saturelluspest of cotton, damages developing bolls causing plant sap to exude from feeding site

7. Ostrininia nubilalis Seed slaying Lepidoptera: Pyralidae Ostrininia nubilalis European Corn Borer Ostrinia nubilalis attacks corn, sorghum, cotton, and many vegetables, causing damages in US > $ 1 billion annually. Introduced to NA in early 1900s.

8. Damage in cone; note frass mass Spruce budwormChoristoneura fumiferanaTortricidae Dispersing larva dangling on a silken thread One of most destructive native pests of spruce and fir forests in eastern NA Sister species, western spruce budworm, Choristoneura occidentalis, defoliator of coniferous forests in W NA Adult and pupa

9. Codling mothCydia pomonellaLep: Tortricidae, Olethreutinae Multivoltine, destructive pest introduced to NA by EU settlers. Larvae tunnel into center of fruit where they feed and develop. Oriental fruit moth Grapholitha molesta

10. Mexican jumping bean mot Lep: Tortricidae Cydia saltitans Mexican jumping bean - seed of Mexican shrubs of the genus Sebastiana (Euphorbiaceae) containing the larva of a moth whose movements cause the bean to jerk or tumble

11. Hymenoptera(Formicidae, Chalcidoidea) Alfalfa Seed Chalcid seed-harvesting ant species in the genera Messor, Pheidole and Pogonomyrmex Pogonomyrmex (naegelii-group) imberbiculus AntWeb California Academy of Sciences

12. Diptera: Tephritidae Above: Urophora stylata: female; and 2 males. Imported to NA for BC thistles Photos by Albert Krebs Right: Rhagoletis completa breeds in the husks of walnuts (Juglans spp.). Photo by Erwin Mani http://www.sel.barc.usda.gov/Diptera/tephriti/PhotTour/Photos.htm

13. Mammals and Birds Orangutans and parakeets feed on dipterocarp seeds. (B) A carpet of dipterocarp seedlings established during the 1987 mast-fruiting event. (D) Dipterocarp trees in Borneo's Gunung Palung National Park. ECOLOGY: Tropical Forest Synergies by Gary Hartshorn and Nora Bynum

14. Effects of seeds on InsectsLygaeid bugs as seed predators of figs Ficus spp (Moraceae) • Arboreal feeders • Obligate terrestrial • Early species • Late species • Facultative terrestrial • Predispersal seeds are a concentrated resource • Mechanisms facilitating exploitation of a patchy resource, macroptery and ovoviparity Slater 1977

15. Fluctuations in abundance of fig foliage unrelated to herbivores Fig leaves added after original fresco was painted, probably at the request of Cosimo III de' Medici in the late 17th century, who saw nudity as disgusting. Leaves were removed when painting restored in 1980s MasaccioThe Expulsion Of Adam and Eve from Eden (1426-28) fresco in Florence

16. Are plant populations seed-limited? Turnbull, L. A., M. J. Crawley, and M. Reese. 2000. Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225-238. • Definition. They define seed limitation to be an increase in population size following seed addition. • Two types of experiments. They review two types of seed addition experiments: seed augmentation studies where seeds are added to existing populations; and seed introductions where seeds are sown in unoccupied sites. • Overall results. Approximately 50% of seed augmentation experiments show evidence of seed limitation. These studies show that seed limitation tends to occur more commonly in early successional habitats and in early successional species.

17. Protocol recommended for seed addition experimentsmodified from Turnbull et al. 2000 • Estimate seed output of natural population. Facilitate comparison by making seed addition some specified multiple of natural seed rain. • Manipulate seed outputs over a sufficient range. • Monitor response throughout the life cycle, at least to adult stage. • Manipulate seed-feeding herbivores as part of the design. Combine enhanced, control, and diminished seed predators with enhanced, control, and diminished seed rain. • Conduct additions on appropriate spatial and temporal scale. Mimic the spatial and temporal scale "sampled" by the life history of the organism.

18. Seed limitation more common in early successional habitats Varies from strong seed-limtation to strong micro-site limitation

19. Seed limitation more common in early successional species (confounded with habitat)

20. Impacts of seed predators on thistles studied by Svata Louda Introduced weevil invaded Nebraska sand dunes where Louda was studying native thistles Rhinocyllus conicus Svata Louda Thistle in Sand Dune Habitat

21. Effects of Insects on Reproductive Success of Cirsium canescens • Removal experiment: insecticide Herbivore effect = protected – exposed • Spatial, temporal, organizational scales of observation • Temporal scales (within and between years) • Spatial scales (region, habitat, between plant, within plant) • Organizational scales (plant/arthropod association, guild, and species within guild • Platte thistle inflorescence feeders • Tephritid flies Orelliaoccidentalis and Paracantha culta • Pyralid moth Hoemosoma stypetallum

22. Life Cycle Graph for Thistle

23. Seedling Shadows with and without insecticide Seed predator effect conditional on distance Recruitment declines with distance from parent Higher recruitment rate when insects are removed using an insecticide at shorter distances

24. Seed Predator Effects Conditional on Year and Habitat

25. Lifetime Seed Production higher in Protected vs Exposed Plants (Louda and Potvin 1984)

26. Plants responses to heavy exploitation by seed slayers • Evolving deterrents (may increase confer resistance or increase ‘handling time’ for consumer) • Hard Seed coat • Toxic chemistry • Mast cropping – escape in time -synchronous, mass production of fruits at interval of n years with very light crops or no crop in intervening years • May lead to Predator Satiation – producing so many seeds that slayer can’t use them all (saturates consumers functional response) • Intervals of little or no seed mitigiate risk of predator increase (counters consumer’s numerical response) • Rapid dispersal – escape in space

27. Problem for Community Ecologists • Seeds slayers have been invoked in explanations of the extraordinary species richness of tropical forests • For example, how are we account for the more than 700 species of trees, shrubs and linas (vines) found on 17 km2 of Barro Colorado Island, Panama? • Two aspects of the problem • Evolutionary question – origins of so much diversity, so many species • Ecological question – maintenance of diversity, what prevents competitive exclusion

28. Janzen-Connell Model • Seed Shadow (I curve) – seed density falls off with distance from the parent. Shape varies with size of seed crop and model of dispersal. • Probability of Survival (P curve) – increases with distance from the parent. Seed slaying varies with distance and/or density. • Population Recruitment Curve (PRC curve) – Taking the product of the I and P curves yields the recruitment curve

29. Distance from parent tree Number of seeds per unit area Prob. of survival Janzen-Connell Model Dispersal (I), Survivorship (P), Recruitment (PRC) Distance from parent tree

30. Question • To what extent can seed predation alone lead to variable recruitment patterns? • Which components of predator activity are responsible for this variation? • How are they responsible? Model varies the • Number of dispersed seeds • Mean distances of dispersed seeds • Predator’s activity

31. Basic Model(Nathan and Casagrandi 2004 J Ecol) Dynamics of seeds S at distance ρ from the source over time t reflects balance in seed gains(the dispersal kernel Φ) and seed losses due to predation ( η ) and other causes ( ω) Mass balance equation with one input (the dispersal kernel Φ) and two outputs (seed losses ω and η)

32. 7 Model Parameters

33. Seed Gains modeled by Dispersal Curve with2 Parameters • Seed rain α and mean dispersal distance D • Effect of increasing dispersal D • Effect of increasing fecundity α

34. Seed lossespartitioned into two components • Losses due to Predation depend on number of predators, their spatial distribution, searching efficiency, and handling times • Numerical response of predator • Functional response of predator • Losses due to all causes other than predation (e.g. micro-site limitation) depends on number of seeds, spatial distribution, and per capita morality rate

35. Full Model of Dynamics of dispersed seeds S at specific location ρ and time t

36. Alternative Recruitment Patterns explained by the model

37. Recruitment patterns obtained by the model The plots are based on the following parameter setting fecundity α = 100, seed handling time Th = 0.1 mortality not by predation µ = 0.1 searching rate a = 5 predation intensity β = 30 mean distance of predators q = 10 mean seed dispersal distance (a) D = 20; (b) D = 10; (c) D = 3.

38. A Field Guide to Estimating Model Parameters

39. Summary • Seeds have distinctive features as a plant resource • Characteristics of seeds have shaped the life styles of consumers as in the fig-bug example • Characteristics of seed slayers have shaped seed production in plants including seed size and number, resistance, timing, and dispersal • Unclear to what degree recruitment in plants depends on available seeds, microsites for establishment, or escape from seed predators