Species interactionsSpecies interactions

- / - Competition - / 0 Amensalism - / + Exploitation 0 / + Commensalism + / + Mutualism

Effects on Interactionsp. 1 / sp. 2

Mutualism• Mutualism is not synonymous with

symbiosis• Mutualism: mutually beneficial interaction• Symbiosis: living in intimate association• symbioses may be:

– exploitative (e.g., Schistosomiasis, Heart worm)

– mutualistic (e.g., bacteria in gut, zooxanthellae)– neutral (e.g., many bacteria on skin)

Mutualism vs. other interactions• Not as well-studied as predation &

competition• Not modeled as frequently• Not studied experimentally as frequently

Facultative vs. Obligate

• Obligate: Interaction is required for life of one or both members

• Facultative: Interaction, though beneficial, is not absolutely required

• For a pair of mutualists, the relationship may be facultative for one and obligate for the other

Examples of mutualisms• Flowering Plants &

Pollinators• Bees, butterflies,

flies, beetles, wasps, birds, bats, others

• some obligate, some facultative

• variable specificity

Examples of mutualisms• Cleaner mutualism• Fish, shrimp, some

birds• Small organism

removes ectoparasites from larger organisms

• facultative, nonspecific

Examples of mutualisms• Ants & Aphids• Aphids feed on phloem• High sugar, low Nitrogen• Excess sugar excreted• Ants feed on sugar excretions• Ants defend aphids against

predators• facultative for both

Examples of mutualisms

• Mycorrhizal mutualism• Roots of most plants colonized by fungi• fungi provide H2O and nutrients,

especially Phosphorus• plant provides carbohydrates

Ectomycorrhizal mutualisms

• fungal mycelium covers root surface and penetrates between cells

• most trees, forest mushrooms• for the fungus - facultative• for the plants - sometimes obligate

Endomycorrhizal (AM) mutualisms

• Arbuscular Mycorrhizal fungi

• most non-woody plants• fungi penetrate plant cells• arbuscules: site of

exchange• for the fungus - obligate• for the plant - facultative

Mutual altruism or mutual exploitation?

• Mutualism has costs and benefits to both parties

• Costs and benefits depend on the environment– cost > benefit … parasitism– cost < benefit … mutualism

• Example: AM fungi and plants

AM fungi and plant root

• Benefit: Plant gets P• Roots deplete P in soil• Fungal hyphae extend

plant’s ability to get P• Cost: Plant must give

photosynthates to fungus – 7 to 20% of daily total

RO

OT

root hairs

fungal hyphae

Zone of depletion (root hair)

Zone of depletion (fungal hyphae)

Soil conditions alter relationship• Low P soil• Plants without

mycorrhizal fungi cannot get enough P

• Mycorrhizal plants grow more rapidly than non-mycorrhizal plants

• Benefit > Cost• Mutualism

• High P soil• Plants obtain ample

P even without mycorrhizal fungi

• Mycorrhizal plants grow less rapidly than non-mycorrhizal plants

• Benefit < Cost • Parasitism

References: West 1997; Peng et al. 1993; Fitter 1985, 1991; Koide & Elliott 1989

Other potential effects on this relationship

• High light• High photosynthesis• High carbohydrate availability• Plant can easily afford to pay the cost of

having AM fungi• Mutualism

• Low light (shade)• Low photosynthesis• Low carbohydrate availability• Plant less able to pay the cost of having

AM fungi• Parasitism

General point• Mutualism depends on the balance of

costs and benefits• For plants, that balance may vary in

space and in time• Mutualism Parasitism• For fungus, plant always provides net

benefits (benefit > cost)

Direct vs. Indirect mutualism• Direct mutualism: Benefits occur

between individuals, and without intermediaries– an individual phenomenon– may have population or community effects

• Indirect mutualism: Benefits depend on effects on a 3rd species– often propagated through trophic network– a population phenomenon, usually with

community effects

Dynamic effects of mutualism• How does mutualism affect population

growth ( dN / dt )?– Increase equilibrium density – Increase maximum population growth– Increase both equilibrium density and

maximum population growth– Increase neither equilibrium density and

maximum population growth

Lotka-Volterra models of mutualism

• Mutualism modeled as negative competition• Competition

dN1 / dt = r1 N1 [ K1 - N1 - a2 N2] / K1

– a2 is the per capita effect of N2 reducing effective dN1 / dt

• MutualismdN1 / dt = r1 N1 [ K1 - N1 + b2 N2] / K1

– b2 is the per capita effect of N2 increasing effective dN1 / dt

Lotka-Volterra mutualism isoclines

N2

N1

K2

K1

2-species equilibrium

dN1/dt = dN2/dt = 0

Lotka-Volterra models of mutualism

• Isoclines have positive slopes• Equilibrium exists and is stable if b1b2 <

1.0 – Both species attain greater equilibrium

densities when together vs. when alone.• Equilibrium is undefined if b1b2 > 1.0

– Isoclines don’t cross– Both species increase to

Lotka-Volterra models of mutualism

• Suppose mutualism coefficients are not constants

• Suppose b’s decrease as N1 and N2 increase

• At sufficiently high N ‘s, mutualist has no effect on dN / dt

• Stabilty• Increase equilibrium density

Modified Lotka-Volterra mutualism isoclines

N2

N1

2-species equilibrium

dN1/dt = dN2/dt = 0

K1

K2

Increased maximum dN / dt

• Suppose r1 is an increasing function of N2

dN1 / dt = r1 N1 [ K1 - N1 ] / K1

– where: r1 = rmax N2 / [ k1/2 + N 2 ]– as N2 increases, r1 rmax

r1

N2

rmax

k1/2

Example: Pollinators

• Suppose K for the plant is set by available space (or by soil nutrients or by light)

• Pollinators may increase seed set and therefore increase maximum dN / dt

• Pollinators don’t alter available space so don’t alter K

Inreased equilibrium density and maximum dN / dt

• Suppose r1 is an increasing function of N2

dN1 / dt = f (N2) N1 [ K1 - N1 + b2 N2] / K1

– where: f (N2) is an increasing function of N2

• Example: Ants & Aphids– ants increase survivorship & reproduction of

aphids (increase dN / dt )– ants alter equilibrium density (by local

elimination of enemies)

No effect on equilibrium density and maximum dN / dt

• Benefits of mutualism may be to individuals

• Those that have mutualists have advantage in intraspecific competition

• But, no necessary advantage at population level.

Resource based mutualisms• Lotka-Volterra models phenomenological• Resource based models mechanistic• Resource processing

– Resources may pass through a series of transformations caused by their use by organisms

RESOURCE

MODIFIED RESOURCE

Resource processing• When resource is changed by processing, it

may become valuable to another species• Different consumers may specialize on the

same resource in different states• Processing chain• Models:

– Heard, S. B. 1994. J. Anim. Ecol. 63:451-466– Heard, S. B. 1995. Ecol. Modelling 80:57-68

• Experiments– Daugherty & Juliano 2002. Ecological

Entomology

Processing chain examples

• Vinegar– yeast consume sugar, excrete alcohol– Acetobacter consume alcohol, excrete acetic acid

• Stream invertebrates– leaves, eaten by shredders (e.g., pteronarcid

stoneflies, tipulid flies)– defecate fine particles, fed upon by filterers,

gatherers (e.g., simuliids - blackflies, mayflies, chironomids)

Processing chain examples

• Predation & scavenging– large predators (e.g., lions)– carrion eaters (e.g., vultures)

• Fish carrion– Bald eagle– Crows, gulls

• Many other examples (see Heard 1994, Journal of Animal Ecology 63:451-464)

A two species processing

chainResource condition 1

(upstream) R1

Resource condition 2

(downstream) R2

Consumer 1(upstream)

Consumer 2(downstream)

lossw1(R1)

lossw2(R2)

consumerindependent

processing h (R1)

consumerdependentprocessing

s [f1 (R1,S1)]

consumption f1 (R1,S1)

consumptionf2 (R2,S2)

supply p

Processing has multiple effects• Upstream consumer exploits the resource

– reduces its value (e.g., energy content)

• Downstream consumer cannot use the resource until it is processed– by upstream consumer– by other means

• Upstream consumer, by processing, makes resources available to downstream consumer

A simple processing chain model

• R1 … upstream resource

• R2 … downstream resource

• S1 … upstream consumer

• S2 … downstream consumer

• p … supply rate of upstream resource• h(R1) … consumer independent processing

• w1(R1) … loss rate for upstream resource

• w2(R2) … loss rate for upstream resource

A simple model of a processing chain

• f1 (R1 , S1) … resource consumed by upstream consumer

• f2 (R2 , S2) … resource consumed by downstream consumer– note: feeding functions could be in the form of

saturation kinetics models.• s … fraction of upstream resource that is used

by the upstream consumer and made available to the downstream consumer

A simple model of a processing chain

• m1 … upstream consumer per capita mortality

• m2 … downstream consumer per capita mortality

• g1 … growth per unit resource consumed for upstream consumer

• g2 … growth per unit resource consumed for downstream consumer

A simple model of a processing chain

• dR1 / dt = p - h(R1) - w1(R1) - f1(R1,S1)

• dR2 / dt = h(R1) - w2(R2) + s [f1(R1,S1)] - f2(R2,S2)

• dS1 / dt = g1{(1 - s)[f1(R1,S1)]} - m1(S1)

• dS2 / dt = g2{[f2(R2,S2)]} - m2(S2)

• equilibrium – growth rates = 0– S1

* , S2* , R1

* , R2*

Commensal vs. Amensal

• Effects are one way– S1 can affect S2, but S2 cannot affect S1

• Consider equilibrium S2 when:– S1 > 0 … upstream consumer present

– S1 = 0 … upstream consumer absent

• S2* | S1 > 0 > S2

* | S1 = 0 … commensal

• S2* | S1 > 0 < S2

* | S1 = 0 … amensal

What determines commensal vs. Amensal

• Equilibrium commensalism occurs whens > h / (h + w1)

• sloppiness (s) is large• loss of upstream resource (w1) is large

• consumer independent processing (h) is small• However, all equilibrium amensal relationships can

behave as commensal relationships prior to equilibrium– short term increases in S2 due to S1

Resource based mutualisms

• Holland & DeAngelis 2010. Ecology 91:1286–1295• Multiple resource-consumer mutualisms

– facultative, obligate, one-way, two-way

• e.g., mycorrhizae– plant provides fungus with carbohydrate– Fungus provides plant with P

Resource based mutualisms

dM1/dt =

M1[r1 + c1(Fmax12M2/(K2+M2)) – q1(Smax1M2/(e1+M1)) – d1M1]

dM2/dt =

M2[r2 + c2(Fmax21M1/(K1+M1)) – q2(Smax2M1/(e2+M2)) – d2M2]

Mi = number or biomass

Fmax, K = Feeding paramters

Smax, e = supply paramters

di = death rate

ci , qi = conversion efficencies

Key results• Mutualisms can yield multiple equilibrium

abundances– Some stable, some not.

• Depends on – unidirectional/bidirectional– obligate/facultative

• Overexploitation and extinction of a mutualist are possible

• Transient dynamics may be inconsistent with the mutualism effect on equilibrium abundance

Consumer-Resource mutualisms

• Takes a cost – benefit approach• But puts a mechanism on costs and

benefits (consumption)• Places costs and benefits into a common

currency

Indirect mutualism

• Beneficial interactions depend on a 3rd species or a network– predation on

predators, competitors– competitor of

predators, competitors– positive effects

necessarily at the population level

competitor #1

competitor #2

competitor #3

food

space

Indirect mutualism(Fritz 1983)

• Insects on Black Locust• Herbivores

– Vanduzea -- membracid treehopper, honeydew– Odontota -- chrysomelid beetle, leaf miner– other herbivores

• Ant– Formica -- tends Vanduzea, feeds on honeydew,

attacks other herbivores and predators

• Predator– Nabicula -- nabid bug, preys on Odontota

Chris Evans, The University of Georgia

Ant mutualist effects on plant?• Branches with ants have fewer other herbivores• Branches with ants have 51% fewer Odontota adults• Ants benefit plant?• Exclude ants from small trees & compare to control

– With ants: fewer Odontota, Nabicula– With ants: Odontota larvae survive at greater rate– With ants: Greater defoliation

• Net effect of ants on plant is detrimental– depends on strengths of direct & indirect effects

Black Locust system

Black Locust

Odontota Other herbivoresVanduzea

Formica Nabicula

Community level effects of mutualism

• How might direct mutualisms affect community properties?– species number & relative abundance

• Can mutualists reduce the impact of competition? Or predation/herbivory?– keystone mutualists

• read: Morris et al. 2007 Ecology

Microcosm experiment(Grime et al. 1987)

• Festuca ovina - canopy dominant• 20 other species• Treatments

– Grazing (scissors)– Soil heterogeneity– AM fungi

Microcosm experiment(Grime et al. 1987)

• Grazing – appeared to increase number of species

slightly– appeared to increase diversity index

• AM – appeared to increase number of species

slightly– appeared to increase diversity index

• NOTE - no real data analysis here

Microcosm experiment(Grime et al. 1987)

• AM – significantly lowered abundance of F. ovina– significantly raised abundances of low-stature,

sub-dominant species

Microcosm experiment(Grime et al. 1987)

• Radio C tracer study– 14CO2 provided to F. ovina

– 72 h later 14C appears in neighboring plants• in VAM replicates 14C is 3 - 150 X greater than in

non-VAM replicates• in VAM replicates 14C is 10 - 100 X lower in a non-

mycorrhizal species ( Rumex acetosa )

– suggests C transfer from dominant to sub-dominant species via mycorrhizae

Community effects of AM fungi

• Fungal mycelium often connects multiple species

• Do fungi equalize competitors by serving as a conduit for C among plants?

• Other investigations also show 14C transferred between plants

However…

• Bergelson & Crawley note:– This and other radiotracer studies show that

14C moves between plants, but NOT that there is net movement

– Festuca ovina clearly harmed by AM– Releases sub-dominant species from

competition– Increases evenness – Little effect on species number

Alternative hypotheses

• AM increase diversity by redistributing C away from dominant and to sub-dominant spp.

• AM increase diversity by parasitizing dominants (C), and secondarily by benefiting sub-dominants (P)

Net movement of C

• Waters & Borowicz 1994 Oikos 71:246-252• Is there net flow of C through AM toward a

stressed plant?– Stress = C drain– Herbivory, shade

Design & Results(Waters & Borowicz 1994)

Clipping 14CO2

Clipping & 14CO2

14CO2

14CO2

14CO2

14CO2

Results

• Net flow of 14C away from the stressed plant – away 100x > toward

• In the absence of fungi, this effect is absent

• Stressed plants do not seem likely to benefit from AM fungi … perhaps the opposite

Do mycorrhizal fungi have community level effects?

• Experiments show that they may• Not necessarily mutualists• Direct effects may involve qualitatively

different interactions with different plants– benefit some (mutualists)– harm others (parasites)

• May enhance diversity or reduce it• Context dependence