Interspecific mutualistic relationships
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INTERSPECIFIC MUTUALISTIC RELATIONSHIPS. Reciprocally beneficial interactions. Photo of clownfish & anemone from Wikipedia Photo of fig & fig wasps from http://www.zoology.ubc.ca. Mutualisms. Benefits that accrue to one or both mutualists: Cleaning Defense against enemies

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INTERSPECIFIC MUTUALISTIC RELATIONSHIPS

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Interspecific mutualistic relationships

INTERSPECIFIC MUTUALISTICRELATIONSHIPS

Reciprocally beneficial

interactions

Photo of clownfish & anemone from Wikipedia

Photo of fig & fig wasps from http://www.zoology.ubc.ca


Interspecific mutualistic relationships

Mutualisms

Benefits that accrue to one or both mutualists:

Cleaning

Defense against enemies

Protection from environmental stresses

Transport

Trophic enhancement

(energy, nutrients)

Etc.

Janzen (1985) recognized five types:

(1) Harvest mutualisms

(2) Pollination mutualisms

(3) Seed-dispersal mutualisms

(4) Protective mutualisms

(5) Human agriculture / animal husbandry

Photo of Dan Janzen & mutualist(?) from http://www-tc.pbs.org/wgbh/nova/rats/images/janz-01-l.jpg


Interspecific mutualistic relationships

Mutualisms

Mutualisms may occur along each of the following continua:

Long-term symbiotic Ephemeral

A species of fig & one of its

many seed dispersers

A species of fig & its

specialist pollinating wasp

Photo of fig & fig wasps from http://www.zoology.ubc.ca

Photo of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm


Interspecific mutualistic relationships

Mutualisms

Mutualisms may occur along each of the following continua:

Obligate Facultative

(non-essential)

A species of fig & one of its

many seed dispersers

A species of fig & its

specialist pollinating wasp

Photo of fig & fig wasps from http://www.zoology.ubc.ca

Photo of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm


Interspecific mutualistic relationships

Mutualisms

Mutualisms may occur along each of the following continua:

One-to-oneDiffuse

(Monophilic Oligophilic Polyphilic)

A species of fig & its

many seed dispersers

A species of fig & its

specialist pollinating wasp

Photo of fig & fig wasps from http://www.zoology.ubc.ca

Photo of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm


Interspecific mutualistic relationships

Mutualisms

Connor’s (1995) mechanisms by which each organism benefits:

By-product: An individual benefits as a by-product of the selfish act(s) of the benefactor; benefit is incidental to the benefactor’s activities

Investment: An individual benefits from the costly act(s) of the benefactor

Purloin (“steal”): An individual benefits by partially consuming the benefactor


Interspecific mutualistic relationships

Mutualisms

Both parties receive by-product benefits

Mutualist 2

Investment

Purloin

By-product

Bird sp. 1

E.g., mixed species flocks;

Mullerian mimicry

By-product

Bird sp. 1

Purloin

Mutualist 1

Investment

Adapted from Connor (1995)


Interspecific mutualistic relationships

Mutualisms

A parasite confers by-product benefits on its host

Mutualist 2

Investment

Purloin

By-product

Insect sp.

E.g., mixed species flocks;

Mullerian mimicry

E.g., original insect pollination (w/o extra reward)

By-product

Plant sp.

Purloin

Mutualist 1

Investment

Adapted from Connor (1995)


Interspecific mutualistic relationships

Mutualisms

A party receiving by-product benefits begins to invest in the other party

Mutualist 2

Investment

Purloin

By-product

Ant sp.

E.g., mixed species flocks;

Mullerian mimicry

E.g., original insect pollination (w/o extra reward)

E.g., ants &

extra-floral nectaries

By-product

Plant sp.

Purloin

Mutualist 1

Investment

Adapted from Connor (1995)


Interspecific mutualistic relationships

Mutualisms

A host begins to parasitize the parasite

Mutualist 2

Investment

Purloin

By-product

E.g., mixed species flocks;

Mullerian mimicry

E.g., original insect pollination (w/o extra reward)

E.g., ants &

extra-floral nectaries

By-product

No examples!

Purloin

Mutualist 1

Investment

Adapted from Connor (1995)


Interspecific mutualistic relationships

Mutualisms

A dependent parasite begins to invest in its host

Mutualist 2

Investment

Purloin

By-product

Yucca sp.

E.g., mixed species flocks;

Mullerian mimicry

E.g., original insect pollination (w/o extra reward)

E.g., ants &

extra-floral nectaries

By-product

E.g., yucca & yucca moth

No examples!

Purloin

Mutualist 1

Moth sp.

Investment

Adapted from Connor (1995)


Interspecific mutualistic relationships

Mutualisms

Each party invests in the other, providing safeguards

against “cheating” are possible

Mutualist 2

Investment

Purloin

By-product

Fungus sp.

E.g., mixed species flocks;

Mullerian mimicry

E.g., original insect pollination (w/o extra reward)

E.g., ants &

extra-floral nectaries

By-product

E.g., yucca & yucca moth

No examples!

Purloin

Mutualist 1

E.g., lichens

Investment

Alga sp.

Adapted from Connor (1995)


Interspecific mutualistic relationships

Mutualisms

Does Batesian mimicry fit into one of these categories?

Mutualist 2

Investment

Purloin

By-product

E.g., mixed species flocks;

Mullerian mimicry

E.g., original insect pollination (w/o extra reward)

E.g., ants &

extra-floral nectaries

By-product

E.g., yucca & yucca moth

No examples!

Purloin

Mutualist 1

E.g., lichens

Investment

Adapted from Connor (1995)


Interspecific mutualistic relationships

Mutualisms

Game-theoretical approach

towards understanding the

Evolutionary Stable Strategy

(ESS) conditions of mutualisms

(Axelrod & Hamilton 1981)


Interspecific mutualistic relationships

Mutualisms

Game-theoretical approach

towards understanding the

Evolutionary Stable Strategy

(ESS) conditions of mutualisms

(Axelrod & Hamilton 1981)

Potential Mutualist 2

Defect

Cooperate

S = 0

Sucker’s payoff

R = 2

Reward for mutual cooperation

Cooperate

Potential

Mutualist 1

P = 1

Punishment for mutual defection

T = 3

Temptation to defect

Payoffs to 1 are

shown with illustrative

values

Defect

E.g., the Prisoner’s Dilemma – two players, each of whom can

cooperate or defect (act selfishly)


Interspecific mutualistic relationships

Mutualisms

Game-theoretical approach

towards understanding the

Evolutionary Stable Strategy

(ESS) conditions of mutualisms

(Axelrod & Hamilton 1981)

Potential Mutualist 2

Defect

Cooperate

S = 0

Sucker’s payoff

R = 2

Reward for mutual cooperation

Cooperate

Potential

Mutualist 1

P = 1

Punishment for mutual defection

T = 3

Temptation to defect

Payoffs to 1 are

shown with illustrative

values

Defect

The conditions for this particular “game”, i.e., the Prisoner’s Dilemma, are:

T > R > P > S, and R > (S + T) / 2


Interspecific mutualistic relationships

Mutualisms

Game-theoretical approach

towards understanding the

Evolutionary Stable Strategy

(ESS) conditions of mutualisms

(Axelrod & Hamilton 1981)

Potential Mutualist 2

Defect

Cooperate

S = 0

Sucker’s payoff

R = 2

Reward for mutual cooperation

Cooperate

Potential

Mutualist 1

P = 1

Punishment for mutual defection

T = 3

Temptation to defect

Payoffs to 1 are

shown with illustrative

values

Defect

The dilemma is whether to cooperate or defect given the paradox that either player is always better off defecting, even though if both cooperated, they would both be better off than if they both defected


Interspecific mutualistic relationships

Mutualisms

Game-theoretical approach

towards understanding the

Evolutionary Stable Strategy

(ESS) conditions of mutualisms

(Axelrod & Hamilton 1981)

Potential Mutualist 2

Defect

Cooperate

S = 0

Sucker’s payoff

R = 2

Reward for mutual cooperation

Cooperate

Potential

Mutualist 1

P = 1

Punishment for mutual defection

T = 3

Temptation to defect

Payoffs to 1 are

shown with illustrative

values

Defect

Under these circumstances, an individual can benefit from mutual cooperation, but it can do even better by exploiting the cooperative efforts of others, i.e., mutualism is not an ESS


Interspecific mutualistic relationships

Mutualisms

Game-theoretical approach

towards understanding the

Evolutionary Stable Strategy

(ESS) conditions of mutualisms

(Axelrod & Hamilton 1981)

Potential Mutualist 2

Defect

Cooperate

S = 0

Sucker’s payoff

R = 2

Reward for mutual cooperation

Cooperate

Potential

Mutualist 1

P = 1

Punishment for mutual defection

T = 3

Temptation to defect

Payoffs to 1 are

shown with illustrative

values

Defect

However, mutualism (cooperation) is a possible ESS in the Iterated Prisoner’s Dilemma, e.g., Tit-for-Tat, in which an individual cooperates on the first move and then adopts its opponent’s previous action for each future move


Interspecific mutualistic relationships

Mutualisms

Ever-present conflict within mutualisms: each party constantly tests opportunities to cheat (cf. “biological barter” – Ollerton 2006)

Therefore, mutualisms can evolve into parasitic

relationships (and vice versa)

Sliding scale of impact of one species

(that always acts to benefit itself) on another:

Very positive

Very negative

Neutral

More virulent

Less virulent

Weak mutualism

Strong mutualism

Pairwise species interactions are often condition dependent, i.e., they could shift between mutualistic and parasitic depending on environmental conditions

The location on the above scale can therefore change

in either evolutionary or ecological time


Interspecific mutualistic relationships

Transport Mutualisms(“mobile links”)

Pollinator mutualisms (bird-, bat-, bee-, etc. syndromes):

Benefits to pollinators include pollen, nectar, oil, resin, fragrances

(e.g., Euglossine bees), ovipositionsites, foodsupplyforlarvae, etc.

Can significantly impact plant-community structure when pollen limitation

occurs (which is often; see Knight et al. 2005)

Image of “Darwin’s hawk moth” pollinating its Malagasy orchid

from http://botany.si.edu/events/sbsarchives/sbs2008


Interspecific mutualistic relationships

Transport Mutualisms(“mobile links”)

Pollinator mutualisms (bird-, bat-, bee-, etc. syndromes):

Benefits to pollinators include pollen, nectar, oil, resin, fragrances

(e.g., Euglossine bees), ovipositionsites, foodsupplyforlarvae, etc.

Can significantly impact plant-community structure when pollen limitation

occurs (which is often; see Knight et al. 2005)

Artist’s reconstruction of Mesozoic (~250 mya to ~65 mya; ended with K-T extinction event) scorpionfly pollination

of a member of the extinct order Czekanowskiales; from Ollerton & Coulthard (2009) Science.


Interspecific mutualistic relationships

Transport Mutualisms(“gone bad”, i.e., no longer mutualistic!)

Pollination by deception likely often arises from a reward-based mutualism

Photo of a Bee Orchid (Ophrys apifera) from Wikipedia


Interspecific mutualistic relationships

Transport Mutualisms(“mobile links”)

Seed-dispersal mutualisms (bird-, bat-, megafauna-, etc. syndromes;

primary & secondary):

Endozoochory– inside animals

Exozoochory– outside animals

Mymecochory– by ants

Can significantly impact plant-community structure when seed-dispersal

limitation occurs (which is often; see Hubbell et al. 1999)

Photos of dung beetles, Proboscidea parviflora, & Trillium recurvatum with elaisomes from Wikipedia


Interspecific mutualistic relationships

Transport Mutualisms

Fig = syconium

Flowers are on the inside

Female wasp enters fig through ostiole carrying pollen

Female lays eggs on some flowers

& pollinates others

“Scales” grow over ostiole

Wasp larvae feed on fig seeds as they grow and develop

Newly hatched male wasps fertilize newly hatched female wasps & cut escape holes; females collect pollen in specialized structures prior to dispersing

Photo of fig & fig wasps from http://www.zoology.ubc.ca


Interspecific mutualistic relationships

Transport Mutualisms

Benefits to plant:

Highly effective pollination

Benefits to wasp:

Larval provisioning

Costs to plant:

Larval provisioning &

maintaining appropriate fig

temperature for wasp development

Costs to wasp:

Pollen transport, competition

for oviposition sites when

multiple foundresses enter a fig

Mutualism conflict: Production of fig seeds is negatively correlated

with production of fig wasps

(“biological barter” along an inter-specific trade-off axis)

Photo of fig & fig wasps from http://www.zoology.ubc.ca


Interspecific mutualistic relationships

Trophic Mutualisms

Mycorrhizae = fungus-plant interactions that influence

nutrient (& water?) uptake by the plant

Present in 92% of plant families (80% of species);

see Wang & Qiu (2006)

Mycorrhizal associations occur throughout the sliding scale, depending on ontogeny, environment, identity of fungus and plant

(see Johnson et al. 1997)

These considerations suggest that mycorrhizae could have substantial effects on plant communities, as they may influence the colonization and competitive abilities of plant species in complex ways (see Bever 2003)


Interspecific mutualistic relationships

Trophic Mutualisms

Photosynthate can pass from “source” plants to “sink” plants via the mycorrhizal hyphal net

This could have a major impact on competitive interactions among plants

Grime et al. (1987) were the first to show the influence of mycorrhizae on competition (in a microcosm): isotopically labeled photosynthate passed from a dominant species (Festuca) to less abundant species

Photo of Phil Grime from http://archive.sciencewatch.com/interviews/philip_grime.htm


Interspecific mutualistic relationships

Trophic Mutualisms

Mycorrhizae: An explanation

for yield decline under continuous

cropping? (Johnson et al. 1992)

Distinctly different VAM communities

in plots with continuous corn vs.

continuous soybeans;

since VAM influence nutrient uptake,

differences can influence yield

Under some circumstances declining yield of continuous monocultures reflects proliferation of mycorrhizae that provide inferior benefits to their host plants (sliding towards parasitism)

Crop rotation reduces the relative abundance of detrimental VAM

An example of Darwinian Agriculture (see Denison et al. 2003)


Interspecific mutualistic relationships

Defense Mutualisms

Endophytic fungi = fungi that inhabit plant parts without causing disease

Hyperdiverse and common: Arnold et al. (2000) isolated 347 distinct genetic taxa of endophytes from 83 leaves from 2 tropical tree species; > 50% of taxa were only collected once

What are they doing in there?

At least some are apparently mutualist symbionts & might have dramatic effects on coexistence, especially by indirectly affecting competitive ability through resistance to disease & herbivory


Interspecific mutualistic relationships

Defense Mutualisms

Clay and Holah (1999) examined an endophytic fungus in a successional old-field community;

the host-specific fungus grows intercellularly in introduced Tall Fescue (Festucaarundinacea), and is transmitted through seeds

Infected plants have greater “vigor,” toxicity to herbivores & drought tolerance

Methods:

8 plots (20 x 20 m) were mown & cleared, sown

with infected (+E) or uninfected (-E) Tall Fescue;

a mixture of other species germinated from the soil-seed bank

Results:

Species diversity declined in +E plots over time relative to -E plots

Photomicrograph of endophyte in Festuca from

http://www.goatworld.com/articles/nutrition/tallfescuetoxicosis.shtml


Interspecific mutualistic relationships

Defense Mutualisms

Freeman and Rodriguez (1993):

The heart-warming tale of a reformed parasite...

Notorious filamentous fungal pathogen, Colletotrichummagna, causes anthracnose disease in cucurbits

Member of a large clade of pathogens capable of infecting the majority of agricultural crops worldwide

Infection occurs when spores adhere to host tissue, enter a cell and subsequently grow through the host leaving a trail of necrotic tissue

Photo of anthracnose on cucumber leaf from

http://urbanext.illinois.edu/hortanswers/detailproblem.cfm?PathogenID=128


Interspecific mutualistic relationships

Defense Mutualisms

Freeman and Rodriguez (1993):

The heart-warming tale of a reformed parasite...

“Path-1” = single-locus mutant of C. magna that spreads throughout the host (albeit more slowly) without necrosis & is a non-sporulating endophyte

Plants infected with Path-1 were protected from the wild-type & were immune to an unrelated pathogenic fungus, Fusariumoxysporum

Path-1 may induce host defenses against pathogens or may outcompete other fungi

Considerable potential exists to tailor endophytes as biocontrol agents; another example of Darwinian Agriculture

Photo of cucurbits grown without (left) and with (right) Path-1 C. magna, both in the presence of Fusarium, from

http://wfrc.usgs.gov/research/contaminants/STRodriguez4.htm


Interspecific mutualistic relationships

Trophic-Protection-Defense Mutualisms

Leaf-cutter (attine) ants and fungi

Ants produce proteolytic compounds

while masticating leaves; fungus further breaks down the leaves and produces food bodies from hyphal tips on which ants feed

Ants carry a species of bacterium (Streptomyces) on their cuticles that controls growth of a parasitic fungus (Escovopsis)

(the “tripartite mutualism” of Currie et al. 2003)

Photo from Wikipedia


Interspecific mutualistic relationships

Trophic-Protection-Defense Mutualisms

Ecosystem-level effects: A single Atta colony can harvest ~ 5% of annual net primary production over 1.4 ha

(summarized in Leigh 1999)

Photo from Wikipedia


Interspecific mutualistic relationships

Mutualism does not occur in isolation

from other species interactions…

E.g., “Aprovechados” (parasites of mutualisms)

sensu Mainero & Martinez del Rio 1985

Parasitic fig wasp

Photo from http://www.pbs.org/wnet/nature/episodes/the-queen-of-trees/photo-essay-an-extraordinary-

ecosystem/1356/attachment/gal23/


Interspecific mutualistic relationships

Mutualism does not occur in isolation

from other species interactions…

E.g., “Aprovechados” (parasites of mutualisms)

sensu Mainero & Martinez del Rio 1985

An herbivorous jumping spider

(Bagheerakiplingi) that exploits an ant-plant mutualism (Vachellia [formerly Acacia] & Pseudomyrmex)

Proxy for Trophic Level

Figure from Meehan et al. (2009)


Interspecific mutualistic relationships

Mutualism does not occur in isolation

from other species interactions…

E.g., Interactions among mutualists of semi-independent function

E.g., Ants that act as defense mutualists against

herbivores may influence pollinators’

activities & pollination success

(see: Wagner 2000; Willmer & Stone 1997)

Photo from http://coronadetucson.blogspot.com/2009_03_01_archive.html


Interspecific mutualistic relationships

Mutualism does not occur in isolation

from other species interactions…

Indirect mutualisms

“The enemy of my enemy is my friend”

(e.g., plants whose defenses enlist the services of the “third trophic level”)

3

-

+

+

2

+

-

+

Me


Interspecific mutualistic relationships

Mutualism does not occur in isolation

from other species interactions…

Indirect mutualisms

“The friend of my friend may be my friend too”

(e.g., a seed-disperser may be an indirect mutualist of a

pollinator of the same plant)

+

2

Me

+

+

+

+

3


Interspecific mutualistic relationships

Phylogenies can help us understand the historical context of mutualisms…

Do mutualisms generally arise from close associations?

Do mutualisms generally arise from initially parasitic interactions?

Do mutualisms spawn adaptive radiations?


Interspecific mutualistic relationships

Hostswitch

Duplication

Host

Mutualist

Failure to speciate

Missing the boat

Extinction

Coexistence

Mutualisms through time

Cospeciation


Interspecific mutualistic relationships

Ghosts of Mutualism Past

E.g., Janzen & Martin (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science 215:19-27.

Image from: http://www.karencarr.com


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