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
Player 1
Mutualism
Commensalism
Predation/
Parasitism
Competition
Player 2
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 – 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 – 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 – 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
Commensalism
Predation/
Parasitism
Competition
Player 2
+
+
+
+
+
A B
Resource 2
Mutualism
Player 1
A
B
Resource 1
Why should we care?
Important
for the LDG
Important in agriculture and
maintaining biodiversity
Mechanisms of co-existence
Origins of diversity
They’re super cool!
“Only in the
tropics…”
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
Sunlight
High
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
Sunlight
High
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
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
Mayfield and Levine (2010)
Predators & Pathogens
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
Janzen-Connell Hypothesis
Probability of Survival
Janzen-Connell Hypothesis
Probability of seed dispersal decreases with
increasing distance from parent
Seedling
Sweet Spot
Less seed/seedling
Lots of seed/seedling
mortality
mortality
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
Species
Population
Population
Species
Species
A
A
B
A
B
(Selective
Target)
(Selective Agent)
Plant-Insect Interactions and Origins
of Diversity
We can use a phylogenetic approach to view past
evolutionary events
A
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 coevolution
Selective
Target
Selective
Agent
Selective
Agent
Selective
Target
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]
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 humblebees 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
CAUTION!
When is it co-evolution?
Janzen, Daniel H. 1980. When is it coevolution?
Evolution 34: 611-612.
1. Just because a pair of species have traits that
are mutualistically congruent, doesn’t mean
they have co-evolved
2. 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
3. “…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…
1.
2.
3.
4.
5.
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:
a) How did these interactions arise?
b) What do these interactions mean with regard to
species diversity and co-existence?
c) Is there enough evidence to support conclusions?
Plant – Herbivore
Interactions
Plant Defenses
Physical Defenses
• Thorns/prickles
• Trichomes
• Toothed leaves
• Tough leaves
• Exudate/latex
Behavioral Defenses
• Ant defense
• Timing of
leafing/masting
Compositional Defenses
• Chemistry
o Alkaloids, tannins,
phenolics,
cyanogenic
glycosides, etc…
• Fiber
content/nutritional
content
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
Inga Evolution
Richardson et al. 2001. Rapid
diversification of a species-rich genus
of Neotropical rain forest trees.
Science 293: 2242-2245.
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)
Defense (I. goldmanii)
•
•
•
•
•
• Opposite patterns of I.
umbellifera
Lower levels of defense compounds
Lower investment in recruitment of ants
Synchronous leafing
Faster leaf expansion
Lower chlorophyll content
Inga – Genus wide
chemical defenses
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
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.
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
Main Results
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 4
Figure 3
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
Why should we care?
Important
for the LDG
Important in agriculture and
maintaining biodiversity
Mechanisms of co-existence
Origins of diversity
They’re super cool!
“Only in the
tropics…”
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!