The Occasional Hymenoptera: Parasitism vs mutualism in a long term context

Parasitism and mutualism play a major role in the lives of most hymenopterans. As a particularly striking example of the complex interrelation between mutualism and parasitism, we’ve looked at the  attine ants which live in a complex relationship among fungi (which they cultivate for food), fungal parasites (which infest the fungal food) and bacteria (which are employed by the ant as a manufactory of antibodies against the fungal parasites).

All studies that I am aware of treat the relation between parasite/host or between symbionts synchronically, that is, at a particular time (usually when the relationship reaches some kind of stasis). A new paper by Todd M. Palmer of the University of Florida reports on long-term studies of a relationship that involves successive mutualists/parasites over a considerable period. “Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism,” Proc. Nat’l Acad. Sciences (Sept. 20, 2010, pdf + html format; also available: abstract and pdf file), discusses the succession of different species of ant colonizers of a particular acacia tree over the course of its very long life.

In an earlier study, when he was beginning the long-term project, Palmer showed that Acacia drepanolobium, a tree which dominates vast stretches of the East Africa savannah is associated with a succession of four different ant species. (Todd M. Palmer,  Truman P. Young, Maureen L. Stanton  & Elizabeth Wenk,  “Short-term dynamics of an acacia ant community in Laikipia, Kenya,” 123 Oecologia 425 (2000) (full pdf available).)  The four ants, which the authors there say make up more than 25% of the animal biomass of the savannahs, are:

1. Crematogaster sjostedti, although it (alone among the four species) does not raise its young inside the swollen thorns, it defends its trees against the other three ant species.

2. Crematogaster mimosae, the most common resident, actively defends the tree, especially at the young shoots.

3. Crematogaster nigriceps,  removes almost all axillary buds except at swollen thorns, effectively sterilizing the tree. This and the next species are most common on smaller trees.

4. Tetraponera penzigi, the only species with a painful sting, eats the extrafloral nectaries on its leaves.

The above is listed in order of decreasing hierarchical dominance among the ants. This was determined by Palmer by experimental methods (staged encounters between ant groups), observation over 6-month periods of 1773 tagged trees, and correlation of tree sizes with occupation by species.

Later studies showed that transitions between species occurred approximately on 10% of the trees per year. In the recent paper (with co-authors Daniel F. Doak, Maureen L. Stanton, Judith L. Bronstein, E. Toby Kiers, Truman P. Young, Jacob R. Goheen and Robert M. Pringle) Palmer characterizes the costs and benefits of the four ant species as follows:

C. mimosae and C. nigriceps aggressively defend host plants from herbivores, whereas T. penzigi and C. sjostedti are moderately and weakly aggressive toward herbivores, respectively. Finally, both C. sjostedti and C. nigriceps appear to be “parasites” within this mutualist network: C. sjostedti actively facilitates attack on host plants by cerambycid beetles and is associated with high host-plant mortality, whereas C. nigriceps sterilizes host plants while in residence by destroying floral meristems throughout the canopy.” (citations omitted.)

The data supporting this conclusion are summarized by the table Palmer provides:

Ant species

Dominance
rank

Colonization
rank

Avg. no. trees
per colony

Host plant
defense

Percent shoots
browsed
§

Sterilization
of host plant?

Extrafloral
nectar use

Beetle
damage

Cs

1

N/A

22.0 (4.8)

Low 1.3 (0.3)

8.0 (1.1)

No

Low 0.1 (0.1)

6.6 (1.3)

Cm

2

3

4.4 (0.3)

High 17.6 (1.7)

3.3 (0.4)

No

High 2.0 (0.4)

1.4 (1.0)

Cn

3

2

2.5 (0.2)

High 15.0 (1.5)

2.5 (0.7)

Yes

High 3.8 (0.4)

0.44 (1.2)

Tp

4

1

1.3 (0.3)

Medium 5.4 (0.7)

3.8 (0.6)

No

None

4.5 (1.1)

Notes: Numerical data for host plant defense are mean number of workers recruiting in response to simulated disturbance; Percentage shoots browsed is the percentage of total shoots with mammalian browsing damage from randomly selected size-matched trees; Numerical data for Extrafloral nectar use are mean number of workers tending nectaries for 50 scans of different host plants occupied by each species. Note that T. penzigi does not use extrafloral nectar, because this species destroys all host-plant nectaries; Beetle Damage is the number of new cerambycid beetle scars accumulating on host plants over an 18-mo period; n/a = C. sjostedti colonies do not appear to colonize new host plants via aerial dispersal. (References omitted. See paper for additional details.)

Palmer and colleagues studied 1,50 Acacia trees over an eight-year period. The goal was to determine whether either the “parasites” or the “free loaders” harm the trees overall. Although certain of the ants seem to be beneficial and others harmful on first glance, they determined that none of them were “perfect” partners for the tree and none of them were net deleterious. Considered individually all four species improved Acacia survival and (with the exception of C. nigriceps, which sterilizes the tree by browsing on young meristems) the ants increased fruiting compared to trees with no ant relationships. But they benefited the trees differently: T. penzigi and C. nigriceps produced higher survival rates and C. sjostedti greater fruiting frequencies.

The trees generally experienced the ant colonies sequentially with small colonies of strongly colonizing ants (T. penzigi and C. nigriceps) followed by dominant species with larger colonies (C. mimosae and C sjostedti). A tree that reached 54 years had a 90% of having been colonized by three of the species and more than a 50% chance of having been colonized by all four.

Palmer’s group proved that the ants influenced the growth and fruiting of the trees rather than merely responded to preexisting conditions of trees by experiment (by switching ant colonies and measuring the trees’ growth rate against “control” trees of the same condition over an 18 month period) and by statistical analysis of the date they accumulated over an 8 year demographic study.

The conclusion reached was that an accurate accessment of the benefits conferred by the ants depended on a consideration of the entire life-span of the tree as well as the relationship among the “guild of ant symbionts.”  Considering the contribution of any one ant species individually at any particular time lead to the conclusion that they were insufficiently beneficial. The overall benfit arises because, given the sequence of colonizing, different species contributed differently at different stages of the tree’s life. Even the “free-loader” (C. sjostedti, which permitted large beetle damage and consumed nectar while provided little plant defense) and the “sterilizer” (C. nigriceps) which ate budding meristems provided positive benefits to the plant given the life stage the acacias were typcially at when colonized by these two species. Although C. sjostedti, for example, negatively affects survival rate, its association with the tree correlated with substantially increased reproduction. Palmer speculations why this should be so: “Because large trees occupied by C. sjostedti produced fewer, smaller swollen thorns and fewer active nectaries than similar-sized trees occupied by C. mimosae, C. sjostedti trees might have more energy available for reproduction.” Likewise, although C. nigriceps prevented reproduction by eliminating the stems that would grow flowers and fruits, it nevertheless enhances tree survival. And since it tends to occupy the trees when young, it benefits the trees when survival is more important (in terms of long run species success) than immediate reproduction. (A larger tree is able to withstand vicissitudes and contribute seeds for many years; a young plant with energy divided between growth and seeding might die altogether without reproduction.)

Thus, to understand a specific ecology of mutualism it is necessary to consider the long-term welfare of each of the partners and not just the synchronic cost and benefit of any particular time.

Incidentally, this very same Palmer and group, as well as the same acacia and ants, have gotten much more publicity recently for their study, published in Science (free pdf), concerning the relationship of the ants, trees and large African herbivores. You can see that study commented on by Scientific American. Palmer has a similarly themed study in Current Biology (abstract; article  behind pay wall), which Ed Yong comments on in Discovery Magazine.

Update [12/26]: Links to abstract and paper of the main study discussed have been updated.

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