Indirect interactions

By Matthew C. Perry - US Geological Survey. "Chapter 14: Changes in Food and Habitats of Waterbirds." Public
Domain, https://commons.wikimedia.org/w/index.php?curid=10491372
Discuss in groups exemples
of indirect effects
 Dramatic and large scale effects

Carpenter et al. 2001

Estes and Duggins 1995

https://thefisheriesblog.com/2012/09/03/trophic-downgrading/
 Another example

With fox Fox free

Croll et al. 2005, Maron et al. 2006
A similar effect of sea eagles

NH4+
What types of indirect interactions can we
expect in food webs?

Why do neighboring species matter?

How does complexity affect trophic

interactions between species?
Density versus trait mediated indirect
interactions

A chain of direct interactions Modification of a direct interaction

Also, numerical Also, functional

indirect interaction indirect interaction
 Four types of density mediated indirect
interactions
Trophic Resource Apparent Intraguild
cascade competition competition predation

Resource mediated Predator mediated

indirect interaction indirect interaction
 Three types of trait mediated indirect
interactions or behavioural modifications
Predator Attracting your Associational
avoidance enemies enemy effects
 Separating trait and density mediated effects

Andrew P. Beckerman et al. PNAS 1997;94:10735-10738

 Separating trait and density mediated effects

Test: glued
mouth parts

Andrew P. Beckerman et al. PNAS 1997;94:10735-10738

 Trait mediated indirect interactions more
important

+
-

Andrew P. Beckerman et al. PNAS 1997;94:10735-10738

Interactions occur at different scales

Example predator mediated effects

Population level (population growth)– Species A

increases population growth of a shared predator, that
also supress species B

Habitat level (behaviour) – Species A attracts a shared

predator, that also feed on species B

Resource level (behaviour) – Species A affects the

ability of the predator to locate or feed on species B

Why is this important? – affects predictability of

interaction
 Population level effect

Population growth = birth – death

For the predator, the balance is determined by the amount of food

For the prey, the balance is determined by the number of predators

In resource competition, the predator

that is able to sustain population
growth on the lowest resource
density wins
Competition for phosphorus leading to
exclusion
 Population level effect

Population growth = birth – death

For the predator, the balance is determined by the amount of food

For the prey, the balance is determined by the number of predators

In apparent competition, the prey

that is able to sustain population
growth at the highest predator
density wins
An example: Population level effects of
apparent competition
 Habitat level effect

Population abundance = immigration - emigration

For the predator, the balance is determined by the size of source and
sink populations and by the species doing the migration
En example: indirect effects between aquatic
and terrestrial systems
Different diets: circle =
rainbow trout, square =
native trout

RBT reduce aquatic

herbivores

And increase
phytoplankton

And reduce insect

emergence

And reduce shoreline

spider abundance

Control With rainbow trout

Short-term behaviour and long-term
population level effects

Effect of competition direct

Effect of apparent competition

delayed due to shift from
behavioural to population
level effect

+ -
Associational effects from the right neighbor

How does complexity affect trophic

interactions between species?

Why is herbivory higher in

monocultures – or is it?
Associational effects in a shopping mall?
A matter of scale
An important tool for pest control in
agriculture and forestry

15 m 15m
700
700
600
600

Eggs/plant
500
500
400
400
300
300
200
200 Intercropping
100
100 Monoculture
00
11 Centre
22 33 44of
Centre of55 66 77 88 99 10
10 11
11 12
12 13
13Centre
14 15
14 15 16
Centre of 17
of
Border area
Border area
intercropping
intercropping monoculture
monoculture
 What is the general pattern?

Negative associations Positive associations

A simple explanation
 Responses to different aspects

Patch size Patch complexity

Resource density
 An example:
Nanophyes marmoratus purple loosestrife
(Lythrum salicaria)

Galerucella pusilla/calmariensis
 Strong insect
damage

Control

Sprayed
 Attack in- and outside sweet gale (Myrica
gale)
Galerucella spp Nanophyes marmoratus
1.4 4
1.2

# adults per plant

# adults per plant

1 3
0.8
2
0.6
0.4 1
0.2
0 0
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. 2002. Funct Ecol 17: 87
Three types of mechanisms

Myrica attracts
predators

Myrica reduce
searching
efficiency

Myrica change
chemistry, size or
abundance of
Lythrum
The enemies hypothesis – more predation in
diverse habitats

Essentially
apparent
competition
Resource concentration hypothesis
Associational effects
Hypothesis 1: Myrica change some feature
of Lythrum, chemistry or abundance, such
that the beetles avoid the plants

Test: Transplantation experiment

Layout Hypothesis refuted if

the pattern is the same
as for natural plants
+ Myrica - Myrica

N = 36 N = 36
 0.2

Leaf damage
0.1

Plant damage
And, similar effect 0

0.8

Meristem damage
0.6

0.4
Galerucella densities 0.2

100 800

# flowers per plant

Number per plant

600
egg
10 400

200

Plant reproductive output

larvae
1 0

80

# fruits per plant

adults 60
0.1
40

20
0.01
0
7-Jul

14-Jul

21-Jul

28-Jul
30-Jun

4000

# seeds per plant

3000

2000

1000
Filled bar = in Myrica gale; Unfilled bar = outside M. gale 0
outside in
Myrica Myrica

Hambäck et al. 2002. Ecology 81: 1784

 Coccinella 5-punctata

Hypothesis 2 refuted:
predators more abundant
outside Myrica
1.6 Coccinella 7-punctata
Control Photo: B. Hamers
Myrica
1.4

1.2
Number per plant

1
Cantharis livida
0.8

0.6

0.4
Chrysoperla carnea
Photo: Ed Nieuwenhuys
0.2

0
Lady-bird Cantharidae Neuroptera Spider

Linyphia triangularis
Hypothesis 3: Myrica affects host-finding by
the beetle

Mechanisms of host finding in insects

Pros Cons
Vision Depth perception Species are all green
Directional information
Smell High degree of information Unclear direction
about identity
Taste Very precise information on Has to be on the plant
identity
Insect vision – visual masking
Using odors to find resources –
olfactory masking
How could that explain herbivory on Lythrum?

Galerucella spp Nanophyes marmoratus

1.4 4
1.2

# adults per plant

# adults per plant

1 3
0.8
2
0.6
0.4 1
0.2
0 0
40 8

# larvae per plant

# egg per plant

30 6

20 4

10 2

0 0

outside inside outside inside

shrubs shrubs
 Could herbivore species differences explain
responses to Myrica?

Host location Food

Leaves
L. salicaria Control

G. pusilla
G. calmariensis
N. marmoratus Flowers
*
-0.8 -0.4 0 0.4 0.8
proportion time in each direction

Hambäck et al. 2002. Funct Ecol 17: 87

 First, an
explanation for
Galerucella?
 Visual masking 10
(A)

and nothing Northern Southern

No. adults per plant

unique about
1
Myrica

0.1
Myrica Artificial 1 Hippophae Artificial 2

(B)
Northern Southern
100
No. eggs per plant

10

Filled bar = in Myrica gale

Unfilled bar = outside M. gale 0.1
Myrica Artificial 1 Salix Hippophae Artificial 2 Alnus
 Solution:
Initial effect magnified by positive feedback

undamaged plant control

Gp NS

Gc NS

plant damaged by beetle

Gp **

Gc **

plant cut by scissor

Gp **

Gc **

-20 -15 -10 -5 0 5 10 15

attraction to cue <> attraction to control
 Different pattern for
Nanophyes marmoratus
Photo: E. Coombs

Northern (A)
Southern
10

L. salicaria Control
No. adults per plant

G. pusilla
G. calmariensis
N. marmoratus
0.1
Myrica Artificial 1 Hippophae Artificial 2
*
-0.8 -0.4 0 0.4 0.8
proportion tid i vardera riktning

Hambäck et al. 2002. Funct Ecol 17:87

 A different explanation

Lower Galerucella-
densities on plants
outside shrubs
1.4
1.2
# adults per plant

1
0.8
0.6
0.4
0.2
0
40
# egg per plant

30

20

10

outside inside
shrubs
 Less flowering

Lower Galerucella- Stronger flowering on

densities on plants plants inside shrubs
outside shrubs
1.4
1.2
# adults per plant

1
0.8
0.6 140
120
# flowers per plant

0.4
0.2 100
0 80
60
40
40
20
# egg per plant

30
0
20
outside inside
10 shrubs
0

outside inside
shrubs
 Compensatory response

Lower Galerucella- Stronger flowering on Nanophyes responds to

densities on plants plants inside shrubs changes in their resource
outside shrubs - higher in shrubs
1.4 8
1.2
# adults per plant

# larvae per plant

1 6
0.8
140 4
0.6
120
# flowers per plant

0.4 2
0.2 100
0 80 0
60
40 0.07
40

# larvae per flower

0.06
20
# egg per plant

30 0.05
0
0.04
20
outside inside 0.03
10 shrubs 0.02
0.01
0 0

outside inside outside inside

shrubs shrubs
 A search for mechanism: intercropping in
cabbage against root flies

100

50

0
Monoculture Intercropping

Björkman, Rämert, Hellqvist & Hambäck. Opubl

 Host finding in root flies

Finch and Collier 2000. Ent Exp Appl 96: 91

 Root flies: continued

Finch and Collier 2000. Ent Exp Appl 96: 91

 A neural theory

Finch and Collier 2000. Ent Exp Appl 96: 91

 Variability among attacking
insects
Plants in bare soil
Plutella xylostella
Pieris rapae
Evergestis forficalis
Delia radicum
Phaedon cochleariae
Brevicoryne brassicae
Pieris brassicae
Mamestra brassicae

1 0.8 0.6 0.4 0.2 0

Proportional reduction in pest damage

Photos: E. Viranen (Pieris), D. Element (Evergestis), R. Coutin (Delia & Mamestra), F. Köhler (Phaedon), S. Carré (aphid)
So, sensory capacity is
important for insects

But different than for the

rabbit-cow example
 But, what about hares feeding on birch –
discuss in groups

7
Amount consumed (g)

6
5
4
3
2
1
0
Alder Birch Rowan
Plant neighbor

Hjältén et al. 1993. Oikos 68:125

 Polyphagous herbivores – pointing to a
general pattern

Sea urchin
Photo: R. Sirna (mare.gol.grosseto.it/acquario)

Sargassum filipendula
 Preference for
fouled algae

100

80

60

Mixed 40

responses 20

-20

-40

-60
6
-80
5
-100 4
3
A Macro
B 2
C algae
D 1
Epibiont Preference for
E
F

clean algae
Wahl & Hay 1995. Oecologia 102:329
 A scaling effect

Unpalatable food Palatable food

Worst Intermediate Best

Compare with monophagous herbivores

 Preference for
fouled algae

100

80

Mixed 60

40

responses 20

due to 0

-20

preference -40

-60

-80
Unpalatable
6
5
-100 4
Palatable 3
A
B 2 Macro
C
D 1
E
algae
F
 So, hare feeding explained by preference
Increasing preference

7
Amount consumed (g)

6
5
4
3
2
1
0
Alder Birch Rowan
Association

Hjältén et al. 1993. Oikos 68:125

 However an opposite effect – trap cropping

Trap crop 2

Acrolepiopsis
Trap crop 1
Plutella

Monoculture

0 5 10 15 20 25
Number of eggs

Åsman 2002. Ent Exp Appl 105: 153

 Selection at a different scale

Less preferred food Preferred food

 Coccinella 5-punctata

Return to the predators:

more abundant
outside Myrica
1.6 Coccinella 7-punctata
Control Photo: B. Hamers
Myrica
1.4

1.2
Number per plant

1
Cantharis livida
0.8

0.6

0.4
Chrysoperla carnea
Photo: Ed Nieuwenhuys
0.2

0
Lady-bird Cantharidae Neuroptera Spider

Linyphia triangularis
Hambäck et al. 2002. Ecology 81: 1784
 0.3

Leaf damage
0.2

0.1

Coccinellids affect 0.8

Meristem damage
Galerucella
0.6

0.4

densities, and plant 0.2

reproduction 600

# flowers per plant

400

200

40

# fruits per plant

30

20

10

1200

# seeds per plant

Coccinella 7-punctata 800

400

0
without with
coccinellids
 Myrica gale Filled arrow = positive effect
Unfilled arrow = negative effect

Galerucella
egg density

Density of
Coccinellid
beetles

A summary of Larval
density

the Galerucella
system Feeding damage

Lythrum flower
production

Density of
Fruit
Nanophyes
production
marmoratus

Seed
production
 A larger spatial scale:
Andean landscapes with potato and maize
 Andean potato weevils in relation to local and
landscape features

Parsa et al. (2012) : PLoS ONE 7(5): e36533

 Andean potato weevils in relation to local and
landscape features

Parsa et al. (2012) : PLoS ONE 7(5): e36533

 Different source size

Parsa et al. (2012) : PLoS ONE 7(5): e36533

 Different source size

Last Last Last

year year year

This
year
This
Last year
Last year
year

Parsa et al. (2012) : PLoS ONE 7(5): e36533

 Dilution effects

Parsa et al. (2012) : PLoS ONE 7(5): e36533

 Dilution effects

This Last
year year
Last
year

This
year This
year

This
year

Parsa et al. (2012) : PLoS ONE 7(5): e36533

Same effect in small patches

Constant number of herbivores

X X X X
X X X X X
X X X X

Density dilution
 Target size effect

Parsa et al. (2012) : PLoS ONE 7(5): e36533

 Target size effect

Number of immigrants
This
year
Last
year

patch size
This
year

Ln(density)
1:1
This
year

ln(patch size)
Parsa et al. (2012) : PLoS ONE 7(5): e36533
 Conclusions
Different types of Potential for Spatial
indirect interactions feedbacks dynamics

Myrica gale Filled arrow = positive effect Source size effect

Unfilled arrow = negative effect

Galerucella
egg density

Density of
Coccinellid
beetles

Larval Dilution effect

density

Feeding damage

Lythrum flower
production

Fruit
Density of
Nanophyes
Target size effect
production
marmoratus

Seed
production
However, increased predator abundance
may be proportional