1. Plant-Insect Interactions in the Tropics
ZOL/ENT/PLB 485
September 24, 2013

2. Examples of Plant-Animal Interactions
Pollination
Herbivory
Seed Dispersal
Seed Predation
Pathogens
Microbial
Fungal
Insect Mimicry
And on, and on…

3. Types of Biotic Interactions
Mutualism – both spp. benefit (but think of it as mutual exploitation)
Commensalism – 1 spp. benefits, and other gets no benefit/harm
Predation/Parasitism – 1 spp. benefits, and other is harmed/killed
Competition – both spp. (or individuals) negatively impact the other
Mutualism
Commensalism
Predation/
Parasitism
Competition
Player 1
Player 2

4. + Types of Biotic Interactions Mutualism Commensalism Competition
Mutualism – both spp. benefit (but think of it as mutual exploitation)
Commensalism – 1 spp. benefits, and other gets no benefit/harm
Predation/Parasitism – 1 spp. benefits, and other is harmed/killed
Competition – both spp. (or individuals) negatively impact the other
Player 1
Player 2
Mutualism
Commensalism
Predation/
Parasitism
Competition +

5. + Types of Biotic Interactions Mutualism Commensalism Competition
Mutualism – both spp. benefit (but think of it as mutual exploitation)
Commensalism – 1 spp. benefits, and other gets no benefit/harm
Predation/Parasitism – 1 spp. benefits, and other is harmed/killed
Competition – both spp. (or individuals) negatively impact the other
Mutualism
Commensalism
Predation/
Parasitism
Competition +
Player 1
Player 2

6. + Types of Biotic Interactions Mutualism Commensalism Competition
Mutualism – both spp. benefit (but think of it as mutual exploitation)
Commensalism – 1 spp. benefits, and other gets no benefit/harm
Predation/Parasitism – 1 spp. benefits, and other is harmed/killed
Competition – both spp. (or individuals) negatively impact the other
Mutualism
Commensalism
Predation/
Parasitism
Competition +
Player 1
Player 2

7. + Types of Biotic Interactions Mutualism Commensalism Competition
Mutualism – both spp. benefit (but think of it as mutual exploitation)
Commensalism – 1 spp. benefits, and other gets no benefit/harm
Predation/Parasitism – 1 spp. benefits, and other is harmed/killed
Competition – both spp. (or individuals) negatively impact the other
Mutualism
Commensalism
Predation/
Parasitism
Competition +
Player 1
Player 2 B A A B
Resource 1
Resource 2

8. Why should we care?
Important in agriculture and maintaining biodiversity
Mechanisms of co-existence
Origins of diversity
They’re super cool!
Important for the LDG
“Only in the tropics…”
How do these interactions affect the distribution of diversity, both locally and globally, and across temporal scales?
Super cool organisms!
Cool from a basic science point of view, but also…
Easy to get people excited about these charismatic creatures.

9. Plant-Insect Interactions and Mechanisms of Co-existence
Species “niche”: the sum of all the environmental factors acting on an organism (Hutchinson 1944)
An “n-dimensional hypervolume” (Hutchinson 1957)
We can consider environmental axes that act as limiting factors as “niche axes”

10. Plant-Insect Interactions and Mechanisms of Co-existence
High
Sunlight
Soil Phosphorous
Note that species diversity not only represents species richness, but can also allude to the diversity in form and function that aid co-existence
Low
Dry
Wet
Soil Moisture

11. Plant-Insect Interactions and Mechanisms of Co-existence
High
Sunlight
Soil Phosphorous
Biotic Interactions creating niche axes
Low
Low
High
Herbivore Pressure

12. Plant-Insect Interactions and Mechanisms of Co-existence
Biotic interactions can act as additional niche axes
Niche partitioning enables species co-existence among species
Biotic Interactions creating niche axes
Figure 2 from Mayfield and Levine (2010) – Ecol Letters

13. Plant-Insect Interactions and Mechanisms of Co-existence
Negative density dependence
Species population growth rates are limited by effects associated with high density(frequency) of individuals
Competition/Crowding
Predators & Pathogens
Mayfield and Levine (2010)

14. Plant-Insect Interactions and Mechanisms of Co-existence
Janzen-Connell Hypothesis: tree species richness is kept high due to the increased probability of mortality of seeds and seedlings growing nearer to their parent tree
Negative density dependence scenario
Often, predators and pathogens are specialized
Janzen 1970 and Connell 1971

15. Probability of Survival
Janzen-Connell Hypothesis
Probability of Survival

16. Janzen-Connell Hypothesis
Lots of seed/seedling mortality
Less seed/seedling mortality
Probability of seed dispersal decreases with increasing distance from parent
Seedling Sweet Spot
Figure 1 from Janzen (1970) – AmNat
(w/ my colorful adaptations!)

17. Plant-Insect Interactions and Origins of Diversity
Selective pressures that are the result of biotic interactions drive evolution, and ultimately speciation A
Species A
Population B
Population A
Species
Species B
(Selective Target)
(Selective Agent)

18. Ancestral state = Square flower shape
Plant-Insect Interactions and Origins of Diversity
We can use a phylogenetic approach to view past evolutionary events A B
Ancestral state = Square flower shape
Circle flower shape

19. Plant-Insect Interactions and Co-evolution
If there are reciprocal selective pressures exerted by both interactors in the relationship, you can get co-evolution
Selective Target
Selective Agent

20. Plant-Insect Interactions and Co-evolution
Again, let’s take a look at this past evolution using a phylogenetic approach
Ancestral state
Ancestral state

21. Plant-Insect Interactions and Co-evolution
We can see how co-evolution can drive species diversification (ie: lineage splitting), but note that it can also drive continued evolution within a lineage without leaving many descendants
Note, these two scenarios are really not mechanistically different, but we may observe different patterns of species diversity today
“Evolutionary Arms Race”
Red Queen Hypothesis]
Draw this on the board!

22. Just so you know…Darwin has almost always said it first…
“The tubes of the corollas of the common red and incarnate clovers (Trifolium pratense and incarnatum) do not on a hasty glance appear to differ in length; yet the hive-bee can easily suck the nectar out of the incarnate clover, but not out of the common red clover, which is visited by humble-bees alone” (Darwin, On The Origin of Species).
Top:
Bottom:
Humle.jpg

23. When is it co-evolution?
CAUTION!
When is it co-evolution?
Janzen, Daniel H When is it coevolution? Evolution 34:
Just because a pair of species have traits that are mutualistically congruent, doesn’t mean they have co-evolved
Parasites/predators could have evolved along with the plant they parasitize, or elsewhere, and then dispersed to their new host plant that is not “evolutionary informed” of this newly arrived predator’s tactics
First, note that not all the plant-insect interactions are the result of evolutionary mechanisms, or at least these really intricate evolutionary relationships we observe in some of these interactions.
We’ll be talking about these really neat plant-insect interactions, many of which are so specialized that it’s hard to believe that they aren’t the product of co-evolution, but this is a process that is hard to actually provide substantial evidence for. Evolution, is awesome, and we know that the diversity of life we see today is the result of evolution, but in most cases, the outcomes we observe are the result of past selection…and thus hard to identify.
So, we’ll be looking at these natural history studies, as well as some studies that have investigated these relationships more in depth, but be wary. Which studies do you think provide substantial evidence for their conclusiosn?
“…it is likely that many defense traits of plants were produced through co-evolution with animals no longer present…” (Janzen 1980)

24. Just a few (very few) examples…
Inga diversification in response to herbivores
Bursera
Complex relationships of figs and their fig wasps
Ant-Acacia relationships: The Ant Defenders!!!
Lepidoptera evolution
With these examples, keep in mind:
How did these interactions arise?
What do these interactions mean with regard to species diversity and co-existence?
Is there enough evidence to support conclusions?

25. Plant – Herbivore Interactions

26. Plant Defenses Physical Defenses Thorns/prickles Trichomes
Toothed leaves
Tough leaves
Exudate/latex
Compositional Defenses
Chemistry
Alkaloids, tannins, phenolics, cyanogenic glycosides, etc…
Fiber content/nutritional content
Behavioral Defenses
Ant defense
Timing of leafing/masting

27. Inga (Fabaceae) (ie: the “pea family”) Over 300 species
Neotropical in range
Recent and rapid diversification (Richardson et al. 2001)
Lineage only 10 million years old
Many species arising only 2 mya
Variety of herbivore defense strategies

28. Richardson et al Rapid diversification of a species-rich genus of Neotropical rain forest trees. Science 293:
Inga Evolution

29. Inga – A pairwise study in defense strategies
Coley et al Divergent defensive strategies of young leaves in two species of Inga. Ecology 86: 2633 – 2643.
Question: Is there a difference in defense strategies between two closely related species of Inga?
Data Collected:
Herbivore-host associations
Ants at EFNs
Leaf size and growth rate
Leaf secondary metabolites

30. Inga – A pairwise study in defense strategies
Main Results:
The two species compared had similar levels of herbivory
There was a difference in defense strategy: Escape vs. Defense
Escape (I. umbellifera)
Lower levels of defense compounds
Lower investment in recruitment of ants
Synchronous leafing
Faster leaf expansion
Lower chlorophyll content
“A fork in the evolutionary road” (Kricher)
Defense (I. goldmanii)
Opposite patterns of I. umbellifera

31. Inga – Genus wide chemical defenses
Kursar et al The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. PNAS 106: –
Study Objectives: evaluate the evolution of antiherbivore defenses and their possible contribution to Inga coexistence
Approach:
37 spp. in Panama & Peru
Characterized defense mechanisms
Evaluated evolution of these mechanisms in a phylo context

32. Inga – Genus wide chemical defenses Main Results
Variation in antiherbivore defense
In all, 13 distinct “chemotypes”
Variation in leaf expansion and chlorophyll content of new leaves (Fig 2)
Much variation in ant abundance and EFN visitation (20-fold difference!)
Figure 2

33. Inga – Genus wide chemical defenses Inga Main Results
Phylo signal in developmental traits, but no signal in ant traits or in chemical traits
Species in bold are “defense”
Developmental, chemical, and ant traits are orthogonal
Figure 3

34. Inga – Genus wide chemical defenses Main Results
Evaluation of Coexistence:
NOTE: Negative values mean members in the community are similar, positive values mean they are dissimilar
At both sites, the species were more different in defensive traits than expected by chance
Figure 4

35. Inga – Genus wide chemical defenses Main Conclusions
Inga species display much variation in all three “trait syndromes” (ie: developmental, chemical, and ant defense strategies)
There is evidence of much trait convergence for chemical and ant defenses, but not for developmental defenses
All three defenses are orthogonal, meaning they potentially represent 3 independent niche axes important for evolution
Species co-occurring at a site are more dissimilar in defense traits than expected, suggesting niche partitioning

36. Plant – Pollinator Interactions

37. Figs and Fig Wasps (and their “friends”…)
Figs (Ficus – Moraceae) and their fig wasps are global in distribution
There are over 750 species worldwide!
Photo by Diana Durance

39. “…were a human to inhabit such a place it would be an utterly dark and crowded room filled with jostling people, some of whom would be homicidal maniacs wielding sharp knives” (Kricher, paraphrasing Hamilton, 1979)

40. Figs and non-pollinating wasps
Study Objectives: To evaluate the role that Idarnes, a non-pollinating fig wasp, has on the overall fitness of its host figs.

41. Figs and non-pollinating wasps
Main Conclusions: Fig fitness (as measured by fruit crop production) was much lower for figs with Idarnes

42. Plant – Ant Defense Interactions

43. Ant-Acacia Interactions

44. Ant-Acacia Interactions
Palmer et al. (2008) - Science

45. Ant-Acacia Interactions
Study Objectives: To evaluate how the removal of large herbivores in an African savanna impacted the dynamics of an ant-Acacia mutualism
Crematogaster mimosae : very aggressive; needs domatia
C. sjostedti: less aggressive; does not use domatia, but plant stems for housing
Crematogaster nigriceps: a defender; prunes axillary buds and kills apical meristems, which reduces likelihood of contact with trees
occupied by hostile colonies
Tetraponera penzigi, an intermediate protector; destroys its
host-plants’ nectaries: a “scorched-earth” strategy to reduce competition
Under natural conditions, C. mimosae is the most abundant ant symbiont, occupying ~52% of all trees at our sites, whereas C. sjostedti occupies ~16% of host plants. C. nigriceps occupies ~15% and T. penzigi occupies ~17%.

46. Ant-Acacia Interactions
Figure 1
Grey bars represent presence of herbivores, white represent absence

47. Figure 2
Figure 3
Figure 4

48. Ant-Acacia Interactions
Main Conclusions:
Removal of large herbivores in this community can greatly affect the mutualism between ants and their plants, and results in decreased fitness of the Acacia trees.

49. Plant – Insect Interactions (herbivory, pollination, ant defense, oh my!)

50. Lepidopterans – Heliconius & Passiflora
“Lepidopterans are (to plant species) evolutionary examples of Dr. Jekyll and Mr. Hyde” (Kricher, pg. 308)

51. Heliconius & Passiflora
A Suite of Biological Interactions:
Heliconia butterflies pollinate Passiflora
Heliconia caterpillars are Passiflora herbivores, and can greatly reduce fitness due to folivary
Passiflora has many defenses to reduce impact of herbivory by Heliconia
Chemical compounds in leaves
Production of extrafloral nectaries
Egg mimics on leaves
But…not only are the caterpillars undeterred by the chemical compounds, it is thought that these compounds are sequestered and used as a defense in adult butterflies

52. Plant – Insect Interactions on a Global Scale

54. Swallowtail Biodiversity
Study Objectives: Use a phylogenetic approach to investigate the evolutionary process responsible for the LDG in swallowtail butterflies (Papilionidae)

55. Distributions across the globe

56. Correlated Evolution
Figure 2 Phylogenetic relationships of 203 swallowtail species, with evolution of their host plant associations. The tree is a 50% majority rule consensus based on Bayesian analysis, with branch lengths proportional to absolute ages. Outside the phylogeny, two coloured circles represent the different taxonomic groups as shown by the left-corner boxes. Coloured branches on the tree, as indicated in the lower right corner, map the evolution of host plant association (outgroups not shown). At host shifts, a pie chart displays the probability of each plant family. Small black squares on the phylogeny indicate node support with both BV and PP equal to or greater than 70% and 0.95 respectively. Asterisks indicate the illustrated species.

57. Why should we care?
Important in agriculture and maintaining biodiversity
Mechanisms of co-existence
Origins of diversity
They’re super cool!
Important for the LDG
“Only in the tropics…”
How do these interactions affect the distribution of diversity, both locally and globally, and across temporal scales?
Super cool organisms!
Cool from a basic science point of view, but also…
Easy to get people excited about these charismatic creatures.

58. Biotic Interactions and the LDG
Tropics have more “niche space” to occupy than do the temperate zones
Tropics have higher diversification rates
There has been a longer time for diversification to occur
Mittelbach et al Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Letters 10:

60. Biotic Interactions and the LDG
Study Objective: Review the literature and determine if studies showed importance of interactions (a) greater at lower lats, (b) greater at higher lats, (c) no evidence of a difference
Main Results: From 39 studies, found only one instance where the biotic interaction was deemed “more important” in temperate regions
But, obviously this is a limited dataset, and only a review of the literature. Much more work needs to be done!