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

2. Global Ocean distribution of Chlorophyll and Benthic Faunal Biomass mg/m 3

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

4. 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 Top-Down Control & Inferences about Trophic Cascades Hairston, Slobodikin and Smith 1960 “Predators and parasites in controlling herbivores … must be food limited.” But, plants may become depleted whenever herbivores become numerous enough (insect outbreaks, e.g. adelgid) The remaining general method of herbivore control is predation” World is Green

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

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

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

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

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

14. Food web manipulation experiments of in 3 lakes (from Carpenter et al., 1987. Ecology 68:1863-1876). 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 ZOOPLANKTONPHYTOPLANKTON

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

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

17. Are Trophic Cascades All Wet?

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

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, 18% Median, 30% Median, 79%

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

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. H P - C1C1 - + C2C2 - + - Trophic Cascades and Feedbacks C3C3 - + - + Links 1 (odd) 2 (even) 3 (odd) 4 (even) For simple food chains: An odd number 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 CXCX But organisms feeding at multiple trophic levels can complicate picture Nutrients P Both Top-down and bottom-up controls influence the abundance and productivity of popluations

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

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

30. Behavior alters species roles in ecosystem C1C1 H P - Nutrients P Mummichog Inverts Algae

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

32. 6 8 10 12 Shrimp  15 N Fish -Fish ReferenceNutrient enrichment Removal of mummichogs allows shrimp to forage in more open areas and become more carnivorous. Behavior alters species roles in ecosystem David Johnson Kari Galvan Linda Deegan

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

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. The End Top Down or Bottom-up??