What controls the productivity and abundance of plants in this ecosystem?

1. Nutrients What controls the productivity and abundance of plants in this ecosystem? Bottom-up Controls – refer to control of abundance or productivity of a species or functional group by supply of resources.

2. and Benthic Faunal Biomass mg/m3 Global Ocean distribution of Chlorophyll

3. Top-Down Controls – refer to control of abundance or productivity of prey species or functional group by the actions of its consumers Nutrients Bottom-up Controls – refer to control of abundance or productivity of a species or functional group by supply of resources.

4. But, plants may become depleted whenever herbivores become numerous enough (insect outbreaks, e.g. adelgid) The remaining general method of herbivore control is predation” Top-Down Control & Inferences about Trophic Cascades Hairston, Slobodikin and Smith 1960 Basic Premise: “Any population which is not resource limited must, of course, be limited to a level below that set by its resources.” Therefore the “usual condition is for populations of herbivores not to be limited by food supply….” and producers are limited by resources, not herbivores • World is Green “Predators and parasites in controlling herbivores … must be food limited.”

5. Green World Hypothesis Nutrients Limited by prey availability Limited by predation Limited by nutrient availability, not herbivory

6. False color aerial infra-red photo of fertilized plots at Great Sippewissett Salt Marsh Controlled manipulation of resources by ecosystem fertilization at Great Sippewissett Salt Marsh (Valiela, Teal, et al. 1970-1990) • HF receives sewage sludge based fertilizer • UP receives equivalent does of urea/phosphate • C are control plots

7. Above ground biomass of salt marsh grasses in fertilized vs. control plots Despite naturally high porewater N levels, further N-additions increase productivity of marsh grasses

8. Annual Cycle of Benthic Chlorophyll in fertilized and control creeks at Great Sippewissett Salt Marsh • Lowest biomass of benthic microphytes in summer • Fertilization effect only occurs in winter-spring period – why? Foreman 1989

9. Macrofaunal Density (1000’s per m-2) Seasonality of fish and macroinfaunal abundance Werme et al.

10. Caging Experiments in a Salt Marsh Exclude fish and crabs with cage

11. Caging Experiment Open one Cage Begin Caging -In cages, algae biomass remains high in cages as grazing pressure by fish and crabs is reduced and fertilization effect persists -Biomass converges on ambient (low) levels when cages are opened and grazers can gain access; diminishes fertilization effect -Suggests consumer control overwhelms resource control of benthic algae in the summer Foreman 1989

12. Effect of excluding fish and crabs using cages and fertilization on benthic productivity and respiration From Giblin, Foreman & Banta, 1995

13. - Bass Control + Bass A “Trophic Cascade” • If piscivores added to lake, they will eat and deplete zooplanktivorous fish. • Populations of larger herbivorous zooplankton will grow. • Phytoplankton populations will be reduced. Food web manipulations in Peter, Paul and Tuesday Lakes

14. Food web manipulation experiments of in 3 lakes (from Carpenter et al., 1987. Ecology 68:1863-1876). ZOOPLANKTON PHYTOPLANKTON Control +Bass -Bass Lakes with bass (piscivore added), zooplanktivorous fish depleted, large zooplankton increase, chl a is lower Lakes with piscivore removed have higher chl a

15. Sea Otters TROPHIC CASCADE IN KELP ECOSYSTEMS and urchin grazers And Killer Whales

16. Amchitka I. N. Adak I. Kagalaska I. L. Kiska I. 400 300 200 100 0 gms 0.25 m -2 60 50 40 30 20 10 0 Grazing Intensity % Loss 24 hr -1 10 8 6 4 2 0 Total Kelp Density No. per 0.25 m2 1972 1985 1989 1993 1997 Year Effect of Killer whale predation on Sea Otters Sea Otter Abundance 100 80 60 40 20 0 # Otters (% max count) Sea Urchin Biomass From Estes et al. 1998 Science 282:473

17. Are Trophic Cascades All Wet?

18. 20.0 7.4 2.7 1.0 Ratio B+predators/B-predatorsfor Plants 0.7% 1.8% 5.0% 13.5% 36.8% 100% RatioN+predators/N-predators for Herbivores as % Comparative Strength of Trophic Cascades Across Ecosystems based on Manipulations of Predators in Six Types of Ecosystems (102 studies)Plot loge (Abundance+predators/Abundance-predators) • Plant response greatest in marine benthos (biomass 4.7X > in systems with predators) vs. terrestrial (1.1X > with predators) • Across systems, as Herbivores ⇩ plant biomass response ⇧ (modified from Shurin et al. 2002, Ecology Letters 5:785)

19. Reasons Why Trophic Cascades Might be Stronger in Aquatic Ecosystems than in Terrestrial Ecosystems • Herbivores are bigger relative to plants in aquatic ecosystems (e.g. zooplankton vs. phytoplankton compared with insects vs. trees) • Aquatic primary producers are more nutritious and have element composition more like their herbivores • Terrestrial plants have lower P:B ratios than aquatic plants • Aquatic herbivores consume about 3X more autotrophic production than terrestrial herbivores (but why??)

20. Comparison of Herbivory in Aquatic and Terrestrial Ecosystems (Cyr and Pace, 1993 Nature 361:148) Frequency distributions showing the proportion of NPP removed by herbivores in ecosystems with different primary producers Median, 79% Median, 30% Median, 18%

21. Regardless of amount of NPP, rates of Herbivory are on average about 3X higher in Aquatic than Terrestrial Ecosystems (note: log scale) Aquatic Terrestrial

22. Reasons why we might not ‘see’ top down cascades in land ecosystems • Many terrestrial plants have complex structural tissue that is harder to digest and have evolved ‘anti-herbivore’ compounds

23. Are Top Down Controls and Trophic Cascades All Wet?Perhaps grazing in terrestrial ecosystems is inhibited by Antiherbivore Compounds/Lignin Derivitives

24. Feeding Experiments with Marsh Invertebrates on Agar Plates Mix Spartina detritus or grass with agar, spike with different concentrations of ferulic acid and allow invertebrates to feed. Count bite marks.

25. Relative Amount Eaten Effect of Tannins on palatability of grass to Geese Demonstrates that chemical composition of plants can affect feeding by herbivores From Buchsbaum et al

26. Reasons why we might not ‘see’ top down cascades in terrestrial ecosystems • Plants have complex tissues and anti-herbivore compounds • Terrestrial may have more complex and more detritus based food webs, less direct grazing. • Many terrestrial apex predators have been hunted to near or local extinction • Longevity of the plant community (decades to centuries for mature plants) makes it hard to measure the results • Terrestrial ecosystems are less experimentally tractable than their aquatic counterparts, in part because of extreme longevity of the plant community • Many of the more charismatic species now enjoy stringent legal protection, which hampers manipulation;

27. But organisms feeding at multiple trophic levels can complicate picture Nutrients H P P CX C1 C2 C3 Links - 1 (odd) 2 (even) 3 (odd) 4 (even) - + - - + - - + + For simple food chains: An oddnumber of trophic links results in control of primary producers by grazing (top-down) An even number of trophic links results in control of primary producers by resources (bottom-up) And nutrients or other factors limiting producers can still increase producer biomass and have effects that propagate up the food web Trophic Cascades and Feedbacks Both Top-down and bottom-up controls influence the abundance and productivity of popluations

28. The Study of ECOLOGY Wolves present absent 30 15 0 ASPEN Number of trees 150 75 0 COTTON- WOOD 1750 1850 1950 2000 WOLVES IN NORTH AMERICA 250 200 150 100 50 Number of wolves in lower 48 (1,000’s) 1750 1850 1950 2000 Ripple et al. 2005 BioScience

29. WOLVES AND WILLOWS 100 50 0 <2 m Percent Browsing 2-3 m 3-4 m 400 200 0 Willow Height (cm) 98 99 00 01 02 03 04 05 Wolves Re-introduced Ripple et al. 2006. For. Ecol & Mgt. 230:96

30. Nutrients H P P C1 - Behavior alters species roles in ecosystem Algae Mummichog Inverts

31. Mummichog Reduction No Trophic Cascade : Creek Infauna Abundance was lower Algae Inverts Mummichog Expected 60 Total Annelids (# / m 2 x 10 3) 40 Observed 20 0 -Fish -Fish Fish Fish Reference Nutrient

32. Behavior alters species roles in ecosystem 12 10 Shrimp d15N 8 6 Fish -Fish Fish -Fish Reference Nutrient enrichment Removal of mummichogs allows shrimp to forage in more open areas and become more carnivorous. David JohnsonKari Galvan Linda Deegan

33. THE IMPORTANCE OF INDIRECT EFFECTS IN ECOSYSTEMS 63% 25 15 5 0 Non-Lethal Effects Aka Trait-mediated Number of studies 40 20 0 Lethal Effects Aka:Density mediated 51% 0 0.5 1.0 1.5 2.0 Ratio of effect size to total predator effect Preisser et al. 2005. Scared to death? The effects of intimidation and consumption in predator prey interactions. Ecology 86:501

34. SUMMARY • Top down controls can be important in ecosystem dynamics • Can affect more than just the level below (cascade), including effects on adjoining ecosystems • Interact with nutrient level • Trait mediated effects may be as important as consumption effects • Stronger in Aquatic or Terrestrial? No consensus just yet.

35. Top Down or Bottom-up?? The End