1. Parasitism, Mutualism & commensalism: lecture content
Continuum of predation
Parasitism - +
Parasitoids

2. Mutualisms in nature
Mutualism is an interaction between two species in which both participants benefit
Mutualism thus a +,+ interaction, to contrast with competition (-,-), predation, parasitism (both +,-)
Mutualism is one kind of symbiosis
Latter defined as close (ecologically interdependent) relationship of two or more species
Other kinds symbiosis involve parasites, predators
Distinguish obligate from facultative mutualism, & give examples (class discussion)

3. Mutualisms can be classified ecologically:
Trophic--specialized partnerships for obtaining energy and nutrients
Corals (algae & zoozanthellae)
Nitrogen-fixing bacteria (e.g., rhizobium & plant)
Ectotrophic mycorrhizae & plants
Lichens (fungus & alga)
Defensive--partnerships providing protection against herbivores, predators, or parasites
Cleaner fish
Ant-Acacia (ants protect against herbivores)
Dispersive--partnerships in which animals disperse pollen or seeds of plants, generally for food reward
Flower-pollinator
Fruit-seed disperser

4. Trophic mutualism formed by coral reef symbionts: Coelenterates & zoozanthellae (coralline algae; from Ricklefs, 2001 )

5. Trophic mutualism comprised of Rhizobium (bacteria are red, false-color image in right figure) in soybean root nodules (left figure; from Ricklefs, 2001)

6. Defensve mutualism between “cleaner organism” in this case a prawn (Lysmata amboiensis, a shrimp relative) and moray eel: prawn gets food, eel gets parasites removed (from Ricklefs, 2001)

7. Defensive mutualism: ants and acacias--e. g
Defensive mutualism: ants and acacias--e.g., bull’s horn acacia (Acacia cornigera trees & Pseudomyrmex ants)
Newly developing bull’s horns (evolutionarily enlarged thorns)
Filled with a pith that ants easily remove, creating hollow interiors
Ants chew small hole into each thorn for use as home
Plants also provide ants with “extra-floral nectar”, secreted from glands at base of leaves (arrows)

8. Older, hollowed-out bull’s horns of Acacia cornigera, next to main trunk (Photo by T.W. Sherry)

9. Plants also supply ants with protein and fat-rich food in the form of “Beltian bodies”, shown here being harvested by ants (arrows) from the tips of newly expanding leaflets of Acacia cornigera (Photo by T.W. Sherry)

10. Pseudomyrmex ants provide two services to Acacia trees:
24-hour patrolling of leaves for protection against herbivorous animals (insects and mammals) by stinging & biting
Clearing of plants from ground and from Acacia trees themselves as protection from competitors (for water, nutrients)
Small grove of Acacia cornigera trees in Costa Rica, showing ground cleared around base of trees by a single colony of Pseudomyrmex ants (Photo by T.W. Sherry)

11. Ant-acacia system, Costa Rica

12. Ground cleared by ants around Acacia tree in Costa Rica

13. Dan Janzen’s (1966*) experiment, tested ecological impact of ants on plants *Co-evolution of mutualism between ants and acacias in Central America. Evolution 20:
Methods:
Fumigated randomly selected sample of Acacia cornigera trees to remove Pseudomyrmex ants
Kept ants from re-colonizing experimental trees using “tanglefoot” (sticky goo) at base of trees
Monitored plant growth of cut, re-growing suckers (stems), and ant activity at experimental (defaunated) versus control trees (containing normal densities of ants)
Results? Next slide...

15. Janzen’s conclusions?
Ants definitely play active role in protecting plants from herbivory by insects (and other animals)
Both ants and acacias involved in co-evolved, obligate relationship (each depends on other species, in specialized, one-to-one relationship)
Value of ants to plants is particularly great in tropical dry forests, where rains don’t fall and water is limiting to plant growth for up to half a year
Mutualism has evolved here in a stressful environment for plants

16. Protective mutualisms
Nutritive mutualisms

17. Other facultative mutualisms with extrafloral nectary plants
Ipomoea (Morning glory), various legumes (Mung Beans etc),
Cotton and other mallows, lots of tropical trees like Balsa.

18. Pollination is an extraordinarily important mutualism
Dispersive mutualism: Flowers of Penstemon sp. in the Sonoran Desert pollinated by the rufous hummingbird(Photo from ) Below is another Penstemon sp. being pollinated by a bee (from helios.bto.ed.ac.uk/ bto/desertecology/bees.htm)
Pollination is an extraordinarily important mutualism

19. Melastome fruits (see arrow) eaten by, and seeds dispersed by, Cocos Finch, Pinaroloxias inornata (Photo by T.W. Sherry & T.K. Werner)

20. Coevolution important in mutualisms
Define Coevolution as reciprocal evolutionary adaptations involving both partners of ecologically interacting species (often difficult to document in nature)
Coevolution well documented in a few cases
In Ant-Acacia system, both participants have traits that are unique to the interaction, and that facilitate the mutualism
Unique Acacia traits include Beltian bodies, hollow thorns
Ant traits include high running speed, stinging ferocity, 24-hour activity patrolling plant, attacks on plants
Dodo bird’s extinction on Island of Mauritius jeopardized survival of its coevolved tree, Calvaria major, indicating obligate relationship of tree to bird (bird evolved to abrade seed in gut, helping germination)

21. Simplistic, but useful model of mutualism based on expansion of logistic model
dN1/dt = r1N1[(X1-N1+a12N2)/X1]
dN2/dt = r2N2[(X2-N2+a21N1)/X2]
All variables same as in logistic model, except a21 is mutualistic per capita effect of species 1 on species 2, and a12 is effect of species 2 on species 1; these alphas increase N’s
Also, K’s replaced by X’s, because mutualists can attain population size > carrying capacity for each species alone
How does this model behave? Again, look for isoclines
Species 1 isocline: (X1-N1+a12N2) = 0 implies N2 = N1/a12 - X1/a12
Species 2 isocline: (X2-N2+a21N1) = 0 implies N2 = X2 + a21N1
Both these isoclines are lines of positive slope

22. Isoclines --> variety of responses, depending on parameter values (see Stiling, Fig. 9.10)
Facultative mutualisms (X1, X2 exist, both >0; i.e., each mutualist can live alone, without other mutualist)
Isoclines cross ==> stable equilibrium
Isoclines parallel,not crossing ==> runaway populations (instability)
More realistic (curvilinear) crossing isoclines, in which alphas change with density ==> stable equilibrium
Obligate mutualisms (X1, X2 do not exist)
Isoclines cross ==> unstable “equilibrium”, unpredictable outcomes
Isoclines parallel ==> unstability, extinction both spp.
Curvilinear isoclines ==> region of stability in state space

23. Possible explanations for curved isoclines in Fig. 9.10 c, f?
Optimal allocation of energy by species interacting mutualistically: Excessive resources allocated to symbiont will be penalized by natural selection
E.g., plants must produce nectar just sweet enough to attract pollinator, but no sweeter
Similarly, plants must produce fruits just attractive enough to be eaten by seed-dispersal agent
This would explain diminishing benefits (and reduced population growth) of each species as the other increases
Alternatively, cost of mutualism is substantial
If cost of mutualism increased with density of mutualist, then benefit would be reduced, leading to curvilinear isoclines
E.g.: 50% of fig seeds destroyed by larvae of fig wasp pollinator (Bronstein)
Conclusion: Mutualism is more complicated than just linear positive feedback of each species on the other!

24. What does model tell us?
A variety of outcomes of mutualism are possible, all consistent with positive slopes of isoclines
Outcome depends on parameter values, which determine slopes and y-intercepts of isoclines
Mutualistic organisms may either coexist stably at fixed densities, populations spiral upwards, or populations collapse to extinction
Obligate mutualisms should be less stable than facultative
Indeed, some obligate mutualisms fall apart in changing environments (e.g., coral bleaching, Ingas at higher altitudes, Cecropia on islands)
Facultative mutualism can be stabilized by changing alphas, such that benefit to each partner decreases with density

25. Aspects of mutualism not included in model?
Benefit of mutualism increases with decreased resource availability
Examples:
Nitrogen-fixing Alders in nutrient-stressed bogs
Many legumes in tropics dominate in nitrogen-poor soils
Plants with mycorrhizal fungi prevalent in phosphorus- poor soils
Corals prevalent in nutrient-poor (carbon-limited) tropical water
Termites & cattle use microbial mutualists to digest cellulose (plant cell walls & wood, difficult-to-digest)
Lesson: theory of mutualism needs to incorporate resource-use dynamics

26. Another aspect of mutualism not in model
Mutualism often found in stressed habitats (In favorable environments, by contrast, species can make it on their own, without expending energy on behalf of mutualist)
Examples:
Ant-acacia mutualism in tropical deciduous forests (seasonally water-stressed soils)
Other nectary and domatia mediated mutualisms common on white sand (low nutrient) tropical soils.
Lichens (association of fungus with alga) live in physically, and nutrient-stressed environments (e.g., arctic tundra, dry soils, water-stressed tree canopies, rocks)
Lesson: theory of mutualism needs to incorporate life-history characteristics, and negative feedback mitigating against mutualism at higher population densities

27. Applied ecology: humans have developed extensive mutualisms with plants & animals that provide us with food and other resources. In turn, we provide nutrients, water, and protection from herbivores. (Photo by T.W. Sherry)
Blue Mountain Coffee, sun-grown, in Jamaica (coffee bushes in foreground, and across hills in distance)

28. Commensalism
Defined as an ecological relationship in which one species benefits from other species, which is itself not affected one way or the other by the relationship
This is thus a “+, 0” relationship
Examples include spanish moss (epiphyte) on trees in Louisiana, cattle egrets, and cactus wren nesting in ant acacia trees
Next few slides illustrate some examples

29. Commensalism between cattle (as food beaters) and cattle egrets (three white birds, one sitting on cow) in Jamaica (photo T.W. Sherry)

30. Cactus wren

31. Conclusions: Mutualism extremely common, widespread in nature
Human agriculture is mutualistic in nature
Many mutualisms have co-evolved
Mutualism ranges from facultative to obligate
Model of mutualism, based on Logistic model, helps explain some aspects of mutualism, but does not really explain when they are stable; obligate mutualism should be less stable than facultative, according to theory
Natural history of mutualism indicates a variety of factors that will make models more realistic: consumer-resource dynamics, tradeoffs, habitat stress
Commensalism also widespread, not well understood

32. Acknowledgements: Some illustrations for this lecture from R. E
Acknowledgements: Some illustrations for this lecture from R.E. Ricklefs The Economy of Nature, 5th Edition. W.H. Freeman and Company, New York.