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

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

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

+ 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 +

+ 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

+ 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

+ 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

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.

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”

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 http://proceedings.esri.com/library/userconf/proc99/proceed/papers/pap308/p30805.gif

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

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

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)

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

Probability of Survival Janzen-Connell Hypothesis Probability of Survival

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!)

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)

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

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

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

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!

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: https://news.brown.edu/files/article_images/Darwin1.jpg Bottom: https://upload.wikimedia.org/wikipedia/commons/4/41/ Humle.jpg

When is it co-evolution? 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 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)

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?

Plant – Herbivore Interactions

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

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

Richardson et al. 2001. Rapid diversification of a species-rich genus of Neotropical rain forest trees. Science 293: 2242-2245. Inga Evolution

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

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

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

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

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

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

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

Plant – Pollinator Interactions

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

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

“…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)

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.

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

Plant – Ant Defense Interactions

Ant-Acacia Interactions http://www.youtube.com/watch?v=Xm2qdxVVRm4

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

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%.

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

Figure 2 Figure 3 Figure 4

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.

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

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

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

Plant – Insect Interactions on a Global Scale

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

Distributions across the globe

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.

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.

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. 2007. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Letters 10: 315-331.

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!