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)
Also: gut bacteria, lichens
Coral and algae
-all reef-building
corals
Protection mutualisms:
Fish and cleaner fish,
cleaner shrimp
Seeing-eye fish
Aphids and
protective ants
Boxing crabs and anemones
Ants and many
plants
Examples
Transport mutualisms:
Plants and seed
dispersers
Plants and
pollinators
(gamete
movement)
87.5% of
plants
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 phylogenies
Leafcutter 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
vs.
Most protection
mutualisms
Some nutritional mutualisms
(e.g. lichen = alga + fungus)
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
Integration of mutualism/facilitation
into ecological theory
• 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
• 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
Line = no
change
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
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
Myrica faya, N-fixer, introduced to HI
• 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
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
Indirect
Ants
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- direct
- direct
Small-seeded
Plants
Rodents
- direct
Large-seeded
Plants
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
Initiator
Tiger shark
local habitat avoidance
Transmitter
Dugong
BMII
(+)
reduced herbivory
Receiver
Seagrass
SharkBay.org
Behaviourally
Mediated
Indirect
Interaction
Distinguishing Indirect &Direct interactions
• In most cases, inferred from interpretation of
results (& natural history knowledge) of
removal experiments
– Ideally, intermediate links
also manipulated
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• Sometimes untangled via path analysis
Wooton 1994
Hypothesis 1: r2 = 99.7%
Hypothesis 2: r2 = 55.5%
Wooton 1994
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
Plant biomass same with
“risk” treatment (spiders
with glued jaws) and
“predation” treatment
(spiders that could actually
eat grasshoppers)
Plants only
Plants +
grasshoppers
Schmitz 1998
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
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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
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Callaway, R. and S. C. Pennings. 1998. Impact of a parasitic plant on the zonation of two salt marsh perennials. Oecologia 114: 100-105
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