For many years, ecologists have been puzzling over the question of why the world is so green.  Given the abundance of herbivores in the world, it seems, on the surface, that plants don’t stand a chance. The famous naturalist/ecologist Aldo Leopold was one of the first scientists to emphasize the role of predators, which provide service for plants by eating herbivores (his example was wolves eating deer, ultimately preserving the plant community growing on a hillside).  As it turns out there are many different predator species providing these services. Colleen Nell began her PhD program with Kailen Mooney with a keen interest on how insectivorous birds locate their prey, and how this could affect the plants that are being attacked by herbivorous insects.

 A Common Yellowthroat perches on Encelia californica. Credit: Sandrine Biziaux.

Plants are not as poorly defended as you might expect (having sat on a prickly pear cactus I can  painfully attest to that).  In addition to thorns and other discouraging structures, many plants are armed with a variety of toxins that protect them against herbivores.  Thorns and toxins are examples of direct defenses.  But many plants use indirect defenses that involve attracting a predator to the site of attack.  Some plants emit volatile compounds that predators are attuned to; these compounds tell the predator that there is a yummy herbivore nearby.  Nell and Mooney recognized that plant morphology (shape and form) could also act as an indirect defense, making herbivorous insects more accessible to bird predators. They also recognized that we might expect a tradeoff between how much a plant invests in different types of defense.  For example, a plant that produces nasty thorns might not invest so much in a morphology attractive to predaceous birds.

California Coastal Cactus Wren eating an orthopteran insect on a prickly pear cactus. Credit: Sandrine Biziaux.

What is a plant morphology that attracts birds?  The researchers hypothesized that birds might be attracted to a plant with simple branching patterns, so they could easily land on any branch that might be hosting a herbivorous insect (Encelia californica (first photo) has a simple or open branching pattern).  In contrast, birds might have a more difficult time foraging on insects that feed on structurally complex plants that host herbivorous insects which might be difficult to reach.

Isocoma menziesii, a structurally complex plant. Credit: Colleen Nell.

The researchers chose nine common plant species from the coastal sage scrub ecosystem – a shrub-dominated ecosystem along the southern California coast. For each plant species they measured both its direct resistance and indirect resistance to herbivores.  Plants of each species were raised until they were four years old.  Then, for three months during bird breeding season, bird-protective mesh was placed over eight plants of each species, leaving five or six plants as unprotected controls.

Kailen Mooney and Daniel Sheng lower bird-protective mesh over a plant. Credit: Colleen Nell.

After three months, the researchers vacuumed all of the arthropods from the plants, measured each arthropod, and classified it to Order or Family to evaluate whether the arthropod was herbaceous.

Colleen Nell vacuums the arthropods from Artemisia californica. Credit: Colleen Nell.

Nell and Mooney evaluated the herbivore resistance of each plant species by measuring herbivore density in the bird-exclusion plants.  Relatively few herbivorous arthropods in plants that were protected from birds would indicate that these plants had strong direct defenses against herbivores.  The researchers also evaluated indirect defenses as the ratio of herbivore density on bird exclusion plants in comparison to controls (technically the ln[exclusion density/control density]).  A density of herbivores on plants protected from birds that is much greater than the density of herbivores on plants that allowed birds would indicate that birds are eating many herbivores. Finally, Nell and Mooney estimated plant complexity by counting the number of times a branch intersected an axis placed through the center of the plant at three different angles.  More intersecting branches indicated a more complex plant.

The researchers expected a tradeoff between direct and indirect defenses.  As predicted, as herbivore resistance (direct defense) increased, indirect defenses from birds decreased among the nine plant species.

Tradeoff between direct herbivore resistance and indirect defense by predaceous birds, for nine common plant species in the coastal sage scrub ecosystem.

The researchers also expected that more structurally complex plants would be less accessible to birds because complex branching would interfere with bird perching and foraging.  Thus Nell and Mooney predicted that structurally more complex plants would have weaker indirect defenses from birds, which is precisely what they discovered.

Indirect defenses (from birds) in relation to plant structural complexity .

Given that structurally complex plants received little benefit from birds, you might expect that they had greater direct defenses in the form of herbivore resistance.  Once again the data support this prediction.

Direct defenses (herbivore resistance) in relation to plant  structural complexity.

Initially, Nell was uncertain about whether increased plant complexity would deter insectivorous birds.  She points out that the top predators in this ecosystem are birds of prey that circle overhead in search of vulnerable birds to eat.  Structurally complex plants might provide refuge for insectivorous birds, which could result in them spending more time foraging in complex plants.  But the research showed the opposite trend. Plant complexity reduced the foraging efficiency of these small insectivorous birds, who prefer foraging on plants with relatively simple structure, which are easier to access and tend to host more prey.

note: the paper that describes this research is from the journal Ecology. The reference is Nell, C. S., and  Mooney, K. A..  2019.  Plant structural complexity mediates trade‐off in direct and indirect plant defense by birds. Ecology  100( 10):e02853. 10.1002/ecy.2853.  Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.