Mutualisms and Indirect Effects

• Positive – Positive interactions• Interactions through third parties (trophic

cascades, apparent competition, indirect mutualism, etc)

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Topics for today• Mutualism– Definitions– Impact on community structure (removal

experiments, invasive species)• Indirect effects– Definitions– Examples from removal experiments

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

Protection mutualisms:

Fish and cleaner fish, cleaner shrimp

Boxing crabs and anemones

Seeing-eye fish

Aphids and protective ants

Ants and many plants

Transport mutualisms:

Plants and pollinators (gamete movement)

87.5% of plants

Plants and seed dispersers

Examples

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. 2003. Science 299:386-388

Congruent phylogeniesLeafcutter ants, cultivated fungus, and parasitic fungus

Currie et al. 2003. Science 299:386-388

Adaptations associated with mutualism can be amazing….

www.waynesworld.com

Facultative vs. Obligate

Most protection mutualisms Some nutritional mutualisms

(e.g. lichen = alga + fungus)

vs.

Diffuse vs. Pairwise

vs.

http://vimeo.com/7048122

Examples

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

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

Predicted frequencies of positive and negative interactions

Bertness and Callaway 1994

• 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

• Facilitation may affect relationship between species diversity and invasibility

Usual paradigm

Inclusion of facilitative effects

• 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)

• May widen realized niche

Bruno et al 2003

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

Random plug….

• Community ecologist Laura Burkle giving seminar Nov. 21st

• Paper in Science 339: 1611-1615 examined interaction networks 120 years after they were first characterized

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

Mutualists and invasion

• Invasion facilitated when organisms not associated with mutualism, are facultative mutualists, or have transportable mutualists

Pringle et al. 2009

Mutualists and invasion

Traveset&Richardson 2006

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. 2010

Myrica faya, N-fixer, introduced to HI

Mutualisms....

• Diverse, ubiquitous, essential, but role in community structure and organization still under-appreciated

Indirect interactions• From the godfather of macroecology:

facilitation of ants by rodents

Small-seeded Plants

Large-seeded Plants

Ants Rodents

- direct

Indirect

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- direct

- direct

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

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

Menge 1995

A BMII from the Dill lab

Dugong

Seagrass

local habitat avoidance

Tiger shark

BMIIBMII(+)(+)

reduced herbivory

SharkBay.org

Behaviourally Mediated Indirect Interaction

Initiator

Transmitter

Receiver

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

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Wooton 1994

Wooton 1994

Hypothesis 1: r2 = 99.7%

Hypothesis 2: r2 = 55.5%

Example: Fish facilitate plant reproduction

• Fish eat dragonfly larvae; dragonflies eat pollinators like bees and flies

Knight et al. 2005. Nature 437:880-883

• Fewer dragonfly larvae in (and adults near) ponds with fish (for three size categories)

Knight et al. 2005. Nature 437:880-883

• Visit rate higher near ponds with fish; plants near these ponds had lower pollen limitation

Knight et al. 2005. Nature 437:880-883

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 2007. Biological Conservation 138:514-519

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

Schmitz 1998

Plants onlyPlants +

grasshoppers

Plant biomass same with “risk” treatment (spiders with glued jaws) and “predation” treatment (spiders that could actually eat grasshoppers)

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

Indirect effects....

• Especially likely for interactors that are already exerting strong direct effects

• Design experiments on interactions so importance can be estimated

Reading for next week

• INDIRECT EFFECTS: Davidson, D. W., R. S. Inouye, J. H. Brown. 1984. Granivory in a desert ecosystem: experimental evidence for indirect facilitation of ants by rodents. Ecology 65: 1780-1786.

• FYI, in the past we also included this one on MUTUALISM: Janzen, D. H. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution: 20(3) 249-275.

As always: Morin, P. J. 1999. Community Ecology. Blackwell Publishing

• Abrams, P. A. 1995. 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. 1994. Positive interactions in communities. TREE 9: 191-193.• Bruno, J. F., J. J. Stachowitch, and M. D. Bertness. 2003. Inclusion of facilitation into ecological theory. TREE 18: 119-125• Byers, J. E., J. T. Wright, and P. E. Gribben. 2010. 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. 1998. Impact of a parasitic plant on the zonation of two salt marsh perennials. Oecologia 114: 100-105• Dill, L. M., M. R. Heithaus, and C. J. Walters. 2003. Behaviourally mediated indirect interactions in marine communities and their conservation

implications. Ecology 84: 1151-1157. • Hay, M. E., J. D. Parker, D.E. Burkepile, C. C. Caudill, A. E.Wilson, Z. P. Hallinan, and A. D. Chequer. 2004. 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. 2010. Mutualisms and community organization. Chapter 13 in H. A. Verhoef and P. J.Morin

. Community Ecology: Processes, Models, and Applications.• Menge, B. A. 1995. Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecological Monographs 65, 21–74. • Menge, B. A.1997. Detection of direct versus indirect effects: were experiments long enough? American Naturalist 149, 801.• Peckarasky et al. 2008. Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions.

Ecology 89: 2416-2429.• Preisser, E. L. And D. I. Bolnick. 2008. 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. 2009. Mycorrhizal symbioses and plant invasions. Annu. Rev.

Ecol. Evol. Syst. 40: 699-715.• Schmitz O (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. American Naturalist 151: 327–342. • Schoener, T. 1993. "On the relative importance of direct versus indirect effects in ecological communities.“ pp 365-411 In Mutualism and

Community Organization: Behavioral, Theoretical, and Food Web Approaches, eds. H. Kawanabe, J. E. Cohen, & K. Wasaki • Strauss, S. Y. 1991. Indirect effects in community ecology: their definition , study, and importance. TREE 6: 206-210.• Strong, D. R. 1997. Quick indirect interactions in intertidal food webs. Trends in Ecology and Evolution 12, 173–174 . • Traveset, A and D. M. Richardson. 2006. Biological invasions and plant reproductive mutualisms. TREE 21: 208-216.• Vitousek, P. M. & L. R. Walker. 1989. Biological invasion by Myrica faya in Hawai’i: Plant demography, nitrogen fixation, ecosystem effects.

Ecological Monographs 59: 247-265.• Werner, E. A. and S. D. Peakall. 2003. A review of trait-mediated indirect interactions in ecological communities. Ecology 84: 1083-1100.• Wooton, T. 1994. Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75: 151-165.