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Mutualisms and Indirect Effects Positive – Positive interactions Interactions through third parties (trophic cascades, apparent competition, indirect mutualism,

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Presentation on theme: "Mutualisms and Indirect Effects Positive – Positive interactions Interactions through third parties (trophic cascades, apparent competition, indirect mutualism,"— Presentation transcript:

1 Mutualisms and Indirect Effects Positive – Positive interactions Interactions through third parties (trophic cascades, apparent competition, indirect mutualism, etc) _ _ _

2 Topics for today Mutualism – Definitions – Impact on community structure (removal experiments, invasive species) Indirect effects – Definitions – Examples from removal experiments

3 Nutritional and energetic mutualisms: Plants and mycorrhizal fungi -the vast majority of plants Plants and Nitrogen-fixing bacteria -mostly legumes (beans, peas) Coral and algae -all reef-building corals Also: gut bacteria, lichens

4 Protection mutualisms: Fish and cleaner fish, cleaner shrimp Boxing crabs and anemones Seeing-eye fish Aphids and protective ants Ants and many plants

5 Transport mutualisms: Plants and pollinators (gamete movement) 87.5% of plants Plants and seed dispersers Examples

6 Multiple mutualisms Leafcutter ants cultivate fungus (mutualism) A microfungus attacks the fungus (antagonism) Ant fights microfungus: behaviourally (weeding) and with antibiotic mutualist bacterium that lives on ant cuticle Currie et al Science 299:

7 Congruent phylogenies Leafcutter ants, cultivated fungus, and parasitic fungus Currie et al Science 299:

8 Adaptations associated with mutualism can be amazing….


10 Facultative vs. Obligate Most protection mutualisms Some nutritional mutualisms (e.g. lichen = alga + fungus) vs.

11 Diffuse vs. Pairwise vs. Examples

12 Mutualism isn’t about being nice, interactions seldom 100% +/+ “Mutualisms are a kind of reciprocal parasitism; each partner is out to do the best it can by obtaining what it needs from its mutualist at the lowest possible cost to itself” Judie Bronstein

13 Mutualism and Ecological Theory Affect the organization, structure, function of ecosystems (coral reefs, tropical forests as examples) Affect cross-ecosystem energy and nutrient flow But, most community ecology theory is based on antagonisms

14 Predicted frequencies of positive and negative interactions Bertness and Callaway 1994

15 Observed changes in interaction strength may be caused by either variation in negative OR positive interactions Facilitation weak, constant Facilitation strong, variable Bruno et al 2003 Integration of mutualism/facilitation into ecological theory

16 Facilitation may affect relationship between species diversity and invasibility Usual paradigm Inclusion of facilitative effects

17 Facilitation may affect relationship between predation and richness Intermediate disturbance hypothesis; also holds for keystone predation Including facilitation: blue = secondary space holders (that live, e.g., on primary space holders like mussels, in red)

18 May widen realized niche Bruno et al 2003

19 Other points about diversity and mutualisms Some mutualisms may decrease diversity – Removals of competitors by protectors, or enhancement of competitive ability by nutritional symbionts Diversity in pollination mutualisms (specialist to generalist) thought to increase diversity in communities – Insurance against losses of partners Kothomasi et al 2010

20 Random plug…. Community ecologist Laura Burkle giving seminar Nov. 21st Paper in Science 339: examined interaction networks 120 years after they were first characterized

21 Burkle et al. re-sampled an area of Illinois that had been intensively studied in the 1800s. Only 46% of plant-pollinator interactions retained Extirpated bee species were specialists with narrow diet breadth Bees were active earlier (but plants less so); phenological mis-matches could be one reason for extirpations Line = no change

22 Mutualists and invasion Invasion facilitated when organisms not associated with mutualism, are facultative mutualists, or have transportable mutualists Pringle et al. 2009

23 Mutualists and invasion Traveset&Richardson 2006

24 Mutualists and invasion Demography of Myrica affects nutrient cycling, succession, non-native birds, exotic earthworms, vegetation (displaces some natives, increases biomass and carbon storage of others)..... Vitousek et al. 1987; Vitousek &Walker 1989; Aplet 1990; Hall &Asner 2007; Asner et al Myrica faya, N-fixer, introduced to HI

25 Mutualisms.... Diverse, ubiquitous, essential, but role in community structure and organization still under-appreciated

26 Indirect interactions From the godfather of macroecology: facilitation of ants by rodents Small-seeded Plants Large-seeded Plants AntsRodents - direct Indirect + - direct

27 Definitions Direct effects: consumption, competition, etc. Indirect effects: mediated through a third party Non-consumptive effects (NCE): changes in prey traits, growth, behavior, or development in response to the presence of a predator

28 Importance? Menge (1995): 40% of studies of the intertidal document indirect effects – Number of indirect effects increases with species richness (even when spp. # accounted for): that is, more complex communities also have more complex II’s – Can be trait/density based, behavioral, chemical, or environmental

29 Menge 1995

30 A BMII from the Dill lab Behaviourally Mediated Indirect Interaction Initiator Transmitter Receiver

31 Distinguishing Indirect &Direct interactions In most cases, inferred from interpretation of results (& natural history knowledge) of removal experiments – Ideally, intermediate links also manipulated Sometimes untangled via path analysis _ _ +

32 Wooton 1994

33 Hypothesis 1: r 2 = 99.7% Hypothesis 2: r 2 = 55.5%

34 Example: Fish facilitate plant reproduction Fish eat dragonfly larvae; dragonflies eat pollinators like bees and flies Knight et al Nature 437:

35 Fewer dragonfly larvae in (and adults near) ponds with fish (for three size categories) Knight et al Nature 437:

36 Visit rate higher near ponds with fish; plants near these ponds had lower pollen limitation Knight et al Nature 437:

37 Trophic cascades can include BMII Reintroduction of wolves to Yellowstone example from last time Leads to aspen recovery— through both predation and fear Recovery primarily in riparian areas with downed logs (predation risk higher) Ripple and Beschta Biological Conservation 138:

38 The ecology of fear NCEs can include changes in foraging effort or efficiency; mate seeking behavior; stress physiology; defense physiology; etc. “prey” can die even when not consumed due to poor diet or starvation

39 Schmitz 1998 Plants only Plants + grasshoppers Plant biomass same with “risk” treatment (spiders with glued jaws) and “predation” treatment (spiders that could actually eat grasshoppers)

40 How NCE’s are re-writing the classics Hare/lynx cycles: presence of lynx stresses hare, changes behavior and reduces reproductive output Killer whales, otters, urchins, and kelp forests: movement of otters away from whales and changing urchin behavior now considered important Peckarasky et al 2008

41 Indirect effects.... Especially likely for interactors that are already exerting strong direct effects Design experiments on interactions so importance can be estimated

42 Reading for next week INDIRECT EFFECTS: Davidson, D. W., R. S. Inouye, J. H. Brown Granivory in a desert ecosystem: experimental evidence for indirect facilitation of ants by rodents. Ecology 65: FYI, in the past we also included this one on MUTUALISM: Janzen, D. H Coevolution of mutualism between ants and acacias in Central America. Evolution: 20(3)

43 As always: Morin, P. J Community Ecology. Blackwell Publishing Abrams, P. A Implications of dynamically variable traits for identifying, classifying and measuring direct and indirect effects in ecological communities. American Naturalist 146:112–134. Bertness, M. D. and R. Callaway Positive interactions in communities. TREE 9: Bruno, J. F., J. J. Stachowitch, and M. D. Bertness Inclusion of facilitation into ecological theory. TREE 18: Byers, J. E., J. T. Wright, and P. E. Gribben Variable direct and indirect effects of a habitat modifying invasive species on mortality of native fauna. Ecology 91, 1787–1798. Callaway, R. and S. C. Pennings Impact of a parasitic plant on the zonation of two salt marsh perennials. Oecologia 114: Dill, L. M., M. R. Heithaus, and C. J. Walters Behaviourally mediated indirect interactions in marine communities and their conservation implications. Ecology 84: Hay, M. E., J. D. Parker, D.E. Burkepile, C. C. Caudill, A. E.Wilson, Z. P. Hallinan, and A. D. Chequer Mutualisms and aquatic community structure: The enemy of my enemy is my friend. Annu. Rev. Ecol. Evol. Syst. 35:175–97. Kothamasi, D., E. T. Keirs, M. G. A. van der Heijden Mutualisms and community organization. Chapter 13 in H. A. Verhoef and P. J.Morin. Community Ecology: Processes, Models, and Applications. Menge, B. A Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecological Monographs 65, 21–74. Menge, B. A Detection of direct versus indirect effects: were experiments long enough? American Naturalist 149, 801. Peckarasky et al Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions. Ecology 89: Preisser, E. L. And D. I. Bolnick The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. Plos ONE 3(6)e2465 Pringle, A., J.D. Bever, M. Gardes, J. L. Parrent, M. C. Rillig, and J. N. Klironomos Mycorrhizal symbioses and plant invasions. Annu. Rev. Ecol. Evol. Syst. 40: Schmitz O (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. American Naturalist 151: 327–342. Schoener, T "On the relative importance of direct versus indirect effects in ecological communities.“ pp In Mutualism and Community Organization: Behavioral, Theoretical, and Food Web Approaches, eds. H. Kawanabe, J. E. Cohen, & K. Wasaki Strauss, S. Y Indirect effects in community ecology: their definition, study, and importance. TREE 6: Strong, D. R Quick indirect interactions in intertidal food webs. Trends in Ecology and Evolution 12, 173–174. Traveset, A and D. M. Richardson Biological invasions and plant reproductive mutualisms. TREE 21: Vitousek, P. M. & L. R. Walker Biological invasion by Myrica faya in Hawai’i: Plant demography, nitrogen fixation, ecosystem effects. Ecological Monographs 59: Werner, E. A. and S. D. Peakall A review of trait-mediated indirect interactions in ecological communities. Ecology 84: Wooton, T Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:

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