Plant-Insect Interactions in the Tropics

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 Player 1 Player 2 Mutualism Commensalism Predation/ Parasitism Competition

4. 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 Player 1 Player 2 Mutualism + + Commensalism Predation/ Parasitism Competition

5. 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 Player 1 Player 2 Mutualism + + Commensalism + + Predation/ Parasitism Competition

6. 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 Player 1 Player 2 Mutualism + + Commensalism + + Predation/ Parasitism + Competition

7. 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 Player 1 Player 2 Mutualism + + A B A B Commensalism + + Predation/ Parasitism Resource 2 + Competition Resource 1

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…”

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 Low Dry Wet Soil Moisture http://proceedings.esri.com/library/userconf/proc99/proceed/papers/pap308/p30805.gif

11. Plant-Insect Interactions and Mechanisms of Co-existence High Sunlight Soil Phosphorous Low Low High Herbivore Pressure http://proceedings.esri.com/library/userconf/proc99/proceed/papers/pap308/p30805.gif

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 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. Janzen-Connell Hypothesis Probability of Survival

16. Janzen-Connell Hypothesis Probability of seed dispersal decreases with increasing distance from parent Seedling Sweet Spot Less seed/seedling mortality Lots of seed/seedling mortality 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 Species Population Species Population Species B A A A B (Selective Target) (Selective Agent)

18. Plant-Insect Interactions and Origins of Diversity We can use a phylogenetic approach to view past evolutionary events B A A 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 Selective Agent Selective Target

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]

22. Just so you know…Darwin has almost always said it first… “The tubes of the corollas of the common red and incarnate clovers (Trifoliumpratenseand 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: https://news.brown.edu/files/article_images/Darwin1.jpg Bottom: https://upload.wikimedia.org/wikipedia/commons/4/41/ Humle.jpg

23. CAUTION! When is it co-evolution? Janzen, Daniel H. 1980. When is it coevolution? Evolution 34: 611-612. 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 “…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. 2001. Rapid diversification of a species-rich genus of Neotropical rain forest trees. Science 293: 2242-2245. Inga Evolution

29. Inga – A pairwise study in defense strategies Coley et al. 2005. 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 • Defense (I. goldmanii) • Opposite patterns of I. umbellifera

31. Inga – Genus wide chemical defenses Kursar et al. 2009. The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. PNAS 106: 18073 – 18078. 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 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

38. http://www.youtube.com/watch?v=JfkiYfrStrU

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 http://www.youtube.com/watch?v=Xm2qdxVVRm4

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 Crematogastermimosae: very aggressive; needs domatia C. sjostedti: less aggressive; does not use domatia, but plant stems for housing Crematogasternigriceps: a defender; prunes axillary buds and kills apical meristems, which reduces likelihood of contact with trees occupied by hostile colonies Tetraponerapenzigi, an intermediate protector; destroys its host-plants’ nectaries: a “scorched-earth” strategy to reduce competition Under natural conditions, C. mimosaeis the most abundant ant symbiont, occupying ~52% of all trees at our sites, whereas C. sjostedtioccupies ~16% of host plants. C. nigricepsoccupies ~15% and T. penzigioccupies ~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)