25.3.

2023

Why is the world green?

ayco.tack@su.se
Stockholm University
www.plantmicrobeinsect.com

Outline

• Plant-feeding insects
• How green is the world?
• What factors keep the world green?
• A historical debate
• A synthetic modern view

• Comparison with agriculture

• Conclusions

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Plants and insects dominate the world

Price, 1984

Majoriteten av den levande

biomassan (=vikten) består av
växter

99. 8% 0.2% <0.01

Bar-On et al, 2018, PNAS

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Biomass

Bar-On et al, 2018, PNAS

How green is the world?

https://www.nature.com/articles/s41586-020-3010-5

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How green is the world?

• Herbivory on land started 455 MYA

• What do you think is the percentage of total
leaf biomass being eaten in nature?

Labandeira, 2007, Insect Science

How green is the world?

Turcotte et al, 2014, PRSB

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Why is the world green?

What keeps herbivore densities low?

• Plant-feeding insects are highly diverse
• But why don’t they multiply till they have eaten all the
plants?

Let’s brainstorm in pairs!

https://padlet.com/aycotack1/1ojf4hgbbclv8695

Outbreaks can be spectacular though!

Gypsy moth

“And the locust went up over all the land of Egypt,

and rested in all the coasts of Egypt […] For they
covered the face of the whole earth, so that the land
was darkened; and they did eat every herb of the
land, and all the fruit of the trees which the hail had
left: and there remained not any green thing in the
trees, or in the herbs of the field, through all the land
of Egypt.”

Exodus 10:14–15 Hunter & Dwyer, 1998, Integrative Biology

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The oak system

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Herbivore communities on oak

Leaf miner

Evans, 1984

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Galler

Redfern & Askew, 1984

Oaks on Wattkast

500 m

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Temporal patterns in plant attack

• Plant attack varies varies through time

• But what keeps species density generally low?

Factors that may keep the world green

• Weather

• Plant defense

• Natural enemies

• Competition

• Dispersal limitation

• Spatial heterogeneity

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Weather Growth rate in a normal

year (1997)

Growth rate in a dry

year (2010)

Drought in July

• Weather may not regulate populations

• However, it frequently explains population dynamics
Tack, Mononen & Hanski, 2015, Proc Roy Soc B

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Factors that may keep the world green

• Weather

• Plant defense

• Natural enemies

• Competition

• Dispersal limitation

• Spatial heterogeneity

``Plants are prickly and taste bad´´

Antiherbivore substances

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Resistance versus tolerance

More on this in a future lecture!

Factors that may keep the world green

• Weather

• Plant defense

• Natural enemies

• Competition

• Dispersal limitation

• Spatial heterogeneity

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https://www.youtube.com/watch?v=kObnRVjX0hM
http://www.wired.com/2014/10/absurd-creature-week-glyptapanteles-wasp-caterpillar-bodyguard/

Natural enemies

Cage with parasitoid

Cage without parasitoid

(Howard, 1911)

No cage

Biological control of the invasive red scale in The impact of the removal of the parasitoid of
Californian citrus stands the gall midge on the coyote bush

From Murdoch et al, 2003, Consumer-resource dynamics

(DeBach et al, 1971; Briggs, 1993)

Factors that may keep the world green

• Weather

• Plant defense

• Natural enemies

• Competition

• Dispersal limitation

• Spatial heterogeneity

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Competition can take many forms

• Direct competition

• Plant-mediated competition

• Natural enemy-mediated
competition (apparent competition)

Indirect competition mediated by

plant responses
“Theoretically, induced defences open up the possibility of two species competing even though
they occur on the host at different times, and ⁄ or exploit different parts of that host. There is no
hard evidence that this does happen, but it is an interesting possibility” (Strong et al, 1984)

Donald Strong

Bob Denno

Kaplan & Denno, 2007

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Plant-mediated competition

Sugimoto et al, 2014, PNAS Appel & Cocroft, 2014, Oecologia

Figure from Mescher & De Moraes, 2014, Nature https://www.youtube.com/watch?v=TKQ-CIX9afA

Apparent competition
Apparent competition is defined as a negative effect between two species mediated by a shared
natural enemy.

Holt, 1977, TPB

Holt & Lawton, 1994, Annu Rev Ecol Evol Syst
https://www.youtube.com/watch?v=kObnRVjX0hM

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Apparent competition

Morris et al, 2004, Nature

Photos from Becky Morris

Apparent competition

Morris et al, 2004, Nature

Photos from Becky Morris

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Apparent competition

Parasitism
rate was
lower after
removal
alternative
host

And
abundance
was higher

Morris et al, 2004, Nature

Photos from Becky Morris

Factors that may keep the world green

• Weather

• Plant defense

• Natural enemies

• Competition

• Dispersal limitation

• Spatial heterogeneity

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Differences in dispersal ability

CC-BY-SA-3.0, Captain-tucker,
Creative Commons CC0 1.0
Universal Public Domain

not edited
Dedication
SCALE INSECTS MONARCH BUTTERFLY

Many scale insects only disperse One generation flies South to

a few millimetres or centimetres Mexico to overwinter, the next
from their mother generation disperses back to the
North

An example for a leaf miner on oak

The female moth has an

average life-time dispersal of
about 100 meter

Zheng, Ovaskainen, Roslin & Tack, 2015, Ecology

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Metacommunity framework

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Dispersal limitation

Tack et al, 2010, Ecology

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Dispersal ability of insects

• Lifetime dispersal varies between 75 – 300 meter

Zheng, Ovaskainen, Roslin & Tack, to be submitted

Factors that may keep the world green

• Weather

• Plant defense

• Natural enemies

• Competition

• Dispersal limitation

• Spatial heterogeneity

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Spatial heterogeneity

We frequently observe spatial (and temporal) variation in:

• The abiotic environment
• The biotic environment
• Intraspecific genetic structure and intraspecific variation

Variation in the abiotic and biotic environment affects the ecology and
evolution of many species!

Chamberlain, 2014, PRSB

Spatial variation in the biotic environment affects the ecology of

beetles on purple loosestrife

Photo: B. Richard

Galerucella pusilla/calmariensis

Nanophyes marmoratus

Purple loosestrife
Photo: E. Coombs
(Lythrum salicaria)

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Spatial variation in the biotic environment affects the ecology

of beetles on purple loosestrife

40 8

# larvae per plant

# egg per plant

30 6

20 4

10 2

0 0

outside inside outside inside

shrubs shrubs

Hambäck et al, 2003, Functional Ecology

Spatial variation in the abiotic environment affects

species interactions: wild flax and flax rust

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The wild flax (Linum marginale) – flax rust

(Melampsora lini) host-pathogen system

• Native Australian plant-pathogen

association
• Gene-for-gene interaction
• Resistance types easily identified
• A model system in wild plant-pathogen
interactions

Bog habitat

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Hill habitat

Plant resistance

Susceptible Resistant

Strong divergence in resistance structure between plants from the bog

and hill habitat types

Tack et al, 2015, NPH

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Local adaptation

**
*
*

• Reciprocal inoculation experiment shows that pathogens are adapted to

plants from their local habitat type:
• Bog pathogens have higher infectivity on bog plants, whereas hill pathogens have higher
infectivity on hill plants
• Pathogens cannot adapt perfectly to plants from all habitat types

Laine et al, 2014, PRSB

Summary for wild plants

• There are many forces that keep

pests of plants to low levels:
– Plant defense
– Natural enemies
– Competition
– Dispersal limitation
– Evolution
– Spatial heterogeneity
• (A)biotic environment
• Intraspecific diversity

• Their importance varies in space

and time

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A food web model

Hunter & Price, 1992, Ecology

Comparison with agriculture

• High variation in plant resistance • Low variation in plant resistance

• High spatial heterogeneity in abiotic • Low spatial heterogeneity in abiotic
and biotic conditions and biotic conditions
• High dispersal limitation • Low dispersal limitation
• Many resources for natural enemies • Few resources for natural enemies

Stuckenbrock & McDonald, 2008, Annu Rev of Phyt

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Conclusions

• Many factors contribute to controlling herbivore populations in

natural systems
– Most important factors may vary through space and time
– Most important factors may differ among plants

• Insights from the natural world may inform us on agricultural

practices

Questions?

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