Beyond keystone predation
•
•
•
•
•
Predation is a pairwise interaction
Interference competition is a pairwise interaction
Effects on the two species involved
There can be effects beyond the pair of species
Indirect effect: An effect of one species on
another that occurs via an effect on a third
species
Predator #1
+
Predator #2
+
- Prey
RESOURCE COMPETITION
negative effects caused via a
shared victim
A surprising
Indirect effect
Increase predator

Decrease Herbivore

Increase Plant
Indirect effect
Predator
+
Herbivore
+
TROPHIC CASCADE
effects produced 2 or more trophic
levels down from top predator
Plant
Indirect effect
+
Prey #1
Predator
+
Prey #2
APPARENT COMPETITION
negative effects caused via a
shared enemy
Decrease prey #1

Decrease Predator

Increase Prey #2
Apparent competition
• Can play a role in effects of
invasions
• Novel pathogens can have
devastating effects on natives
– American Chestnut
– Pollen data for eastern forests
• White oak 25-65% of stems
• Hickory
5-15%
• Am. Chestnut 5-15%
• Parallel story for American Elm
Apparent competition
Settle & Wilson 1990
• Invasion effects via native enemies
– Variegated leaf hopper VLF
(Erythroneura elegantula)
– Grape leaf hopper GLF
(Erythroneura variabilis)
• Feed on grape
• in California GLF native; VLF invasive
• 1980s: as VLF spread in San Joaquin Valley,
GLF declined
Parasitoid
•
•
•
•
Anagrus epos
Egg parasitoid
Attacks both, prefers GLH
as proportion of VLH
increases, proportion of
unparasitized eggs that are
VLF increases
• and therefore proportion
parasitism of GLH increases
Reductions of GLF
• Interspecific competition detectable, but
not particularly strong or asymmetrical
• Apparent competition seems to be the
main driver of replacement of GLF by VLF
Intraguild Predator
+
+
Intraguild prey
+
- Resource
INTRAGUILD PREDATION
Preying on your competitor
Indirect effect
Intraguild predation (IGP)
• Intraguild predator and intraguild prey are
competitors
• For IGP to be stable, intraguild prey must be
better competitors for the shared resource
than intraguild predators
– otherwise intraguild prey must have access to
resources unavailable to intraguild predators
• high productivity favors intraguild predators
• low productivity favors intraguild prey
Intraguild predation (IGP)
Resource
Resource +
Intraguild prey
Resource +
Intraguild prey +
Intraguild predator
Resource +
Intraguild predator
Productivity (Carrying capacity for resource)
Intraguild predation (IGP)
• Diehl & Feissel 2001
• Tested this with:
– Bacteria (=resource)
– Tetrahymena (=intraguild prey)
– Blepharisma (intraguild predator)
Predator #1
+
Prey #1
Predator #2
+
-
Prey #2
INDIRECT PREDATOR MUTUALISM
positive effects of one predator
on another via competing prey
Indirect
effect
Decrease predator #1

Increase Prey #1

Decrease Prey #2

Decrease Predator #2
Indirect effects
• Possibilities are complex
• Become more complex with more species
• Two problems:
– 1. How do you detect indirect effects?
– 2. How important are indirect effects in
determining community composition?
Kinds of indirect effects
• Up to this point – density mediated
effects
• direct interactions produce effects that in
turn have effects on other species
• other possibilities exist
Kinds of indirect effects
• Chains of interactions
– effects of one species’ population propagate
through chains (or networks) of other direct
interactions like competition and predation
– also called “density mediated interactions”
• Interaction modification
– the presence of one species alters in some
way the direct interaction of two other species
– also called “trait mediated interactions”
Density vs. Trait mediated
interactions
B
B
A
A
C
A
C
C
increase C, increases B,
which indirectly decreases
A
the presence of B changes something about
how A and C affect one another
Examples of trait mediated
interactions
• Apocephalus sp.
– phorid fly
– parasite of ants
• Pheidole diversipilosa
– host
• Other ant species competing for
food
– presence of competitors improves
Apocephalus ability to find and to
parasitize P. diversipilosa
• Presence of Apocephalus at food
– reduces competitive ability of P.
diversipilosa
Detecting indirect effects
• You must know something about the pairwise
direct interactions within the community
• You often must do experiments, typically
species removals and additions
• If you don’t know which pairwise interactions are
present, indirect effects may be interpreted
incorrectly even in an experiment
Predator #2
+
Misinterpreting an
indirect effect in an
experiment
Predator #1
+
-
Prey
-
Competitor
-
•
•
•
•
•
Remove predator #2
Predator #1 increases
Prey decreases
Competitor increases
If you don’t know the
interactions, it looks like
Predator #2 might prey
on Competitor
The importance of indirect effects
• Commonly assumed that
– direct effects are strong
– indirect effects are weak
• Relative to any single direct effect,
indirect effects may be stronger, more
important determinants of species
composition and diversity
• Data? (Wootton 1994)
Intertidal invertebrates (again)
Sea star
Leptasterias + + Predatory snail
Nucella
+
-
Acorn Barnacle
Semibalanus
+
-
Birds
+ (crows, gulls)
+
+
+
- Goose N. Barn.
Pollicipes
-
-
-
-
Mussel
Mytilus
Interactions in intertidal
• Observation: Exclude bird predation (cages)
–
–
–
–
Nucella: decreases relative to control (2 - 4 X)
Pollicipes: increases relative to control (~5 X)
Semibalanus: decreases relative to control (3 - 7 X)
Mytilus: decreases relative to control (to 70%)
• Excluding predator:
– 2 prey species decrease
– 1 non-prey species decreases
– 1 prey species increases
Understanding this effect
• A hypothesis to explain this result
• Which direct interactions are strong?
– affect numbers of individuals
• Which direct interactions are weak?
– do not affect numbers of individuals
Hypothesis #1:
strong & weak interactions
+
Sea star
Leptasterias + + Predatory snail
Nucella
+
-
Acorn Barnacle
Semibalanus
-
Birds
+ (crows, gulls)
+
+
+
- Goose N. Barn.
Pollicipes
-
-
-
-
Mussel
Mytilus
Hypothesis #2:
strong & weak interactions
+
Sea star
Leptasterias + +
Predatory snail
Nucella
+
-
Acorn Barnacle
Semibalanus
-
Birds
+ (crows, gulls)
+
+
+
- Goose N. Barn.
Pollicipes
-
-
-
-
Mussel
Mytilus
Hypothesis #3:
strong & weak interactions
Sea star
Leptasterias + + Predatory snail
Nucella
+
-
Acorn Barnacle
Semibalanus
+
-
Birds
+ (crows, gulls)
+
+
+
- Goose N. Barn.
Pollicipes
-
-
-
-
Mussel
Mytilus
Hypotheses  new predictions
• Remove Pollicipes with birds excluded
– H #1: Mytilus, Semibalanus, Nucella all
increase
– H #2: Mytilus, Semibalanus increase
– H #3: Mytilus only increases
• vs. birds excluded only
Hypotheses  new predictions
• Exclude birds after removing Pollicipes
– H #1: no effects
– H #2: Nucella decreases, Leptasterias
increases
– H #3: Semibalanus, Nucella decrease,
Leptasterias increase
• vs. removing Pollicipes only
Experiment 1
Manipulate Pollicipes without birds
Seastar
Leptasterias
+
Birds
EXCLUDED
+
-
Predatory snail
Nucella
+
-
+
-
-
-
Acorn Barnacle
Semibalanus
-
Goose N. Barn.
Pollicipes
-
-
Mussel
Mytilus
Experiment 2.
Manipulate birds without Pollicipes
Seastar
Leptasterias
+
+
-
-
+
-
Predatory snail
Nucella
Birds
(crows, gulls)
+
+
REMOVE
Pollicipes
-
-
-
Acorn Barnacle
Semibalanus
-
-
Mussel
Mytilus
Results of experiment 1
• Remove Pollicipes in cages that exclude
birds
– Mytilus increases (2 X)
– Semibalanus increases (7 X)
– Nucella increases (3.6 x)
• compared to cages with Pollicipes
• As predicted by hypothesis #1
• Inconsistent with hypotheses #2 & #3
Results of experiment 2
• Exclude birds (cages) after removing
Pollicipes
– Mytilus unaffected
– Semibalanus unaffected
– Nucella unaffected
• compared to no exclusion of birds after
removing Pollicipes
• As predicted by hypothesis #1
• Inconsistent with hypotheses #2 & #3
More...
• Experiment 3. Removal of Nucella
– no effects on Pollicipes, Semibalanus,
Mytilus
– As predicted by hypothesis #1
– Inconsistent with hypotheses #2 & #3
• Experiment 4. Removal of Semibalanus
– Nucella decreases
– As predicted by hypothesis #1
– Inconsistent with hypotheses #2 & #3
Path analysis
• Statistical technique for estimating
direct and indirect effects among
observational variables
• Analysis predicts important direct paths
are:
– birds  Pollicipes
– Pollicipes  Mytilus, Semibalanus, Nucella
– Semibalanus  Nucella
– Mytilus  Semibalanus
• Most similar to Hypothesis #1
Overall...
• Experiment, alterntive hypotheses, new
predictions, new experiments
• Sophisticated experiments to test
indirect effects
• Statistical technique combined with
experiments
• Hypothesis #1 clearly supported
• Indirect effects of primary importance in
this system
Trophic cascades
Predator
+
-
Herbivore
+
-
Plant
• Hairston, Smith, Slobodkin, 1960. Am. Nat.
– Green earth argument
– predators limit herbivorous prey and so enhance
production & populations of plants
• Examples: Morin pp. 214-221
Trophic cascades
• May involve more than trophic interactions
• May cross ecosystem bondaries
• Ecosystem engineers: species affect
others, but the interaction has no effect on
their own fitness or population growth
– Large herbivores
– Burrowing species
– Fire-prone species
• Trophic cascades can work through
ecosystem engineers
Foxes on Aelutian Islands
Croll et al. 2005
• Beginning
1900
– Foxes
introduced
– Absent on
some
• Effects
– Reduced bird
density
– Vegetation
change
– Change in
nutrient
import
Resource subsidy from
marine system
defecating
hunting
N, P
Effects of foxes as predators
• Without Foxes
• Large nesting bird
populations
• Lots of guano input
– N, P
– high soil P
• More grass, less shrub
• Greater grass biomass
• With Foxes
• Bird populations reduced
(100x)
• Reduced guano input
– low soil P (60x)
• Less grass (3x), more shrub
(10x)
• Less grass biomass (3x)
significance
• Importance of subsidies from one
ecosystem to another
• Importance of predation, even predation
several trophic levels removed
– trophic cascade
• Trophic cascades can include
nontrophic interaction.
– Birds impact via ecosystem engineering,
not feeding
– This type of effect rarely demonstrated
Trophic cascades across system boundaries
(Knight et al. 2005)
• Species with complex life cycles
– Aquatic larvae – terrestrial adults
– Amphibians, Odonates, Mosquitoes, many
insects
– How do predators in one environment
(aquatic) affect trophic systems in the other
(terrestrial)?
Fish predation
• Dominant factor in freshwater systems
• Influences abundances of many invertebrates
Knight et al.
• Eight ponds
– 4 with fish (Sunfish)
– 4 without fish
– Not experimental
• Dragonflies
– Abundances
significantly lower in
and around fish ponds
vs. no fish ponds.
– Particularly for
medium and large
dragonflies
Plants and pollinators
• St. John’s Wort
• More pollinators near fish
ponds
– More Diptera, Lepidoptera,
& especially Hymenoptera
Knight et al.
• Fish
– Reduce dragonflies
– Increases pollinators
• Does this matter to the plants?
• Does reduced pollinator density near
fishless ponds reduce plant reproductive
success?
Knight et al.
• Pollen supplementation
– St. John’s wort
• Supplemental pollen increases seed set near
both fish and fishless ponds
– Magnitude of increase ~3X greater near fishless
ponds (where pollinators are reduced)
– Similar for Sagittaria as well
Effects on pollinators
• Data suggest that effects of dragonflies on
pollinators is both density mediated and
trait mediated
• Pollinators avoid behaviorally areas with
lots of dragonflies
Effects of fish
• Solid –
direct
• Dashed
- indirect
Significance
• Interactions cross community boundaries
• Complex life cycles
– Dragonflies
– Other insects
– Link terrestrial and aquatic communities
Disturbance and stress
• Disturbance and stress can be
accommodated with isoclines
• Assessment of the conditions necessary
for coexistence of e.g., competitors
• Chase & Leibold Fig. 2.11
Stress-Resource isoclines
sp. 2
S
sp. 1
species 2 only
species 1 only
R
Nonequilibrium coexistence
• Chase & Leibold
– Ch. 6
– especially pp. 99-101
• Tradeoffs create equilibrium conditions
• Analysis has primarily concerned
conditions where dN / dt = 0
• conditions with dN / dt ≠ 0 …
Variation
• intrinsic
– variation in e.g., species abundance
produced by deterministic dynamics of
population(s)
– cycles, chaos
– e.g., Lotka-Volterra predation, logistic
population growth with discrete
generations
Variation
• extrinsic
– variation imposed on populations or communities
by changing environmental conditions
– typically postulated as temporal variation
– historical argument: Temporal variation disrupts
equilibrium determined by species interactions
– Thus facilitates nonequilibrium coexistence of
competitors
Environmental harshness
• ideas parallel those on extrinsic
variation
• harsh environment (stress)
– causes mortality
– reduces impact of competition
– facilitates coexistence
Harsh or fluctuating conditions
• coexistence of competitors is actually not favored by
harsh conditions
• harsh conditions may actually reduce the likelihood of
coexistence
• fluctuating conditions sometimes can increase the
likelihood of coexistence
– do so when extrinsic variation provides "niche opportunities"
– species benefit differentially from fluctuations
– different species favored at different points along
environmental variable that fluctuates
Some relevant references
• Chesson, P 2000. Mechanisms of maintenance of
species. Annual Review of Ecology & Systematics
31:343-366
___________________________________________
• Chesson, P & N Huntly 1997. American Naturalist
150:519-553
• Pake, CE & DL Venable 1995. Ecology 76:246–61
• Pake, CE & DL Venable 1996. Ecology 77:1427–35
• Cáceres, CE 1997. Proceedings of the National
Academy of Sciences USA 94:9171-9175
Harsh conditions
• increase mortality (m)
• in resource competition that raises R*
– R* = K1/2m / [ pFmax - m ]
• affects all species the same way
– does not alter outcome of competition
– may slow down approach to equilibrium
• affects species differently
– may reverse competitive outcome
– isocline model for effect of stress
Stress-Resource isoclines
sp. 2
S
sp. 1
species 2 only
species 1 only
R
Mechanisms of coexistence
• Fluctuation independent
– resource differences, trade offs, etc.
– the previous lectures on competitive coexistence
– can operate in either fluctuating or constant
environments
• Fluctuation dependent
– mechanisms that require environmental fluctuation
– deterministic (e.g., seasonal)
– stochastic (random)
Fluctuation dependent mechanisms
• Storage effect
– differential responses to environment
– buffered population growth
– covariance between effects of environment
and competition (+)
• Relative nonlinearity of competition
• Both involve "temporal niches"
– concentrates intraspecific effects in time
– greatest intraspecific effect at those times
that most limit its population
Storage effect
• differential responses to the environment
– different species have greatest population
growth at different values of environmental
variable(s) that fluctuate
Storage effect
• covariance between environment and
competition
– intraspecific competition greatest when a
species is favored by the environment
– interspecific competition greatest when the
species’ competitors are favored
• sounds as though species would be
greatly harmed by competition when rare
Storage effect
• buffered population growth
–
–
–
–
resting, inert, or otherwise invulnerable stages
resting eggs
dormant stages
invulnerable, long-lived adults
• limits impact of competition when a species is
not favored
– species escapes those times when it does not
have an advantage
Storage effect
• differential responses, covariance of
environment and competition, &
buffered population growth
• combined they render the impact of
intraspecific competition on population
growth greater than that of interspecific
competition
Examples of storage effect
• Cáceres 1997
– Daphnia
– dormant eggs
• Pake & Venable 1995
– desert rodents
• Pake & Venable 1996
– desert plants
– seed banks
Nonlinearity of competition (fluctuating environment)
Nonlinearity
• species a has advantage (greater resource dependent
growth) on average in the fluctuating environment or in
a constant environment (arrow)
• greater fluctuation of environment favors growth of
species b
• nonlinearity of species a causes fluctuation of
competitive factor F when a is abundant and b is rare
(benefits b)
• species b causes less fluctuation of competitive factor F
when b is abundant and a is rare (benefits a)
Implications
• "Niche differences" essential for
coexistence of competitors
– differences in limiting factors
• Fluctuations are important as alternative
aspects of the environment that limit a
species
• In a sense variation becomes another
resource axis
– Chase & Leibold Fig. 6.3
variation as a resource
Variability of Resource


1
2
Mean Resource
3