Learning predator

promotes prey coexistence

Yumiko Ishii*, Masakazu Shimada (2012) PNAS Department of System Sciences (Biology) , University of Tokyo

*Present address: Center of Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies

Importance of Frequency-dependent predation in maintaining species diversity in nature ?

- Since the 1970s, theoretical studies have predicted that frequency-dependent predation is one of the strong mechanisms in maintaining prey coexistence.

- There is a lack of empirical evidence directly testing the effect of

learning and frequency-dependent predation in a multigenerational prey–predator system.

Time

Prey switching for abundant prey species

Pop

ula

tio

n

Predator

Prey1 Prey2

Pedators that switch to more common prey types promotes the coexistence of prey species because it prevent rare prey types from being eliminated.

Two- host one-parasitoid host-parasitoid system

Predation

Host2：CC Callosobruchus chinensis

Host1: CM

Callosobruchus

maculatus

Parasitoid Anisopteromalus calandrae

Predation

Competition For resource beans

Does the presence / absence of a predator contribute to coexistence of two prey species?

How does learning of a predator affect the dynamics?

Experimental insect population as a mimic of species interaction occurring in natural ecosystems.

Life cycle of seed beetles and parasitoids.

4 weeks

2weeks

Anisopteromalus

calandrae

Challosobruchus

chinensis

Challosobruchus

maculatus

Seed beetles - Insect Pests of stored beans.

Parasitoids - A parasite that oviposits on and eventually kills the host organism.

The adult female lay their eggs on the surface of beans.

Adult emergence from the bean, and mating.

Larvae feed and develop inside the beans.

Female wasp attacks the host of about 2 week of age.

♪ Black-eye beans:

High parasitization rate.

Azuki beans

Low parasitization rate.

Refuge for host.

The predation pressure was altered by changing the ratio of the black-eye bean, BR.

Methods: Multi-generation experimental system

-Introduction of CC, CM, and Parasitoids. -Renew the resource once a week. -Count the number of adults once a week.

BR = 0

BR = 1

BR = 0.5

Pred

ation

pressu

re

low

high

Host-parasitoid population dynamics at varying predation pressure.

low

Pred

ation

pressu

re high

Ratio of Black-eye beans: BR

Time (weeks)‏ Time (weeks)‏ Time (weeks)‏

Num

ber

of

Adults

Num

ber

of

Adults

Num

ber

of

Adults

Num

ber

of

Adults

Num

ber

of

Adults

BR = 0

BR = 0.2

BR = 0.5

BR = 0.8

BR = 0.8 BR = 1 BR = 1

BR = 0

BR = 0.2

BR = 0.5

BR = 0

BR = 1

CM outcompeted CC.

Long coexistence of CM and CC.

Outbreak of parasitoids. Extinction of CM and CC.

Parasitoid present

Parasitoid absent

Time (week)

Nu

mb

er

of

Ad

ult

s N

um

be

r o

f A

du

lts

Parasitoid promoted the coexistence of host species !

BR = 0.8

The coexistence time of CC and CM.

Parasitoid absent

Parasitoid present

Parasitoid introduction prolonged the coexistence time of CC and CM at intermediate predation pressure (BR=0.2, BR=0.5, BR=0.8).

low Predation pressure high

Host search behavior of A. calandrae

- Search the concealed host larvae in a bean with antennal tapping.

- Oviposit on the host larva & pupa.

Can A. calandrae distinguish between CC and CM ?

Larva of CC Larva of CM

Hatched egg of the seed beetle.

!

Inside the bean

Learning in parasitoids

- Many parasitoid species have been well-studied for their learning ability. (Godfray & Waage 1988, Turlings et

al. 1993 ).

- They prefer the experienced host by learning the host-related odors during successful oviposition.

Nu

mb

er o

f o

vip

osi

tio

n

Conditioning time (h) Conditioning time (h) Conditioning time (h)

A. calandrae learned to preferred the host they experienced.

CC

CM

Number of oviposition on

Experienced female on CM

Control female without experience

Experienced female on CC

The effect of the oviposision experience on the preference were examined. -Conditioning: A. calandrae experienced oviposition on the larvae of CM or CC for 6, 24, 48hrs.

-Choice test: The conditionded female was provided the equal numbers of CM and CC larve, and allowed to oviposit for 3 hrs.

mean±SE

Choice test A. calandrae increased preference for the conditioned host after 24 h.

Ishii and Shimada (2010) Popul Ecol

A. calandrae distinguished between two hosts by olfactory cues.

Experienced female on CM

Control female without experience

B

A

CC

CM CC

CM

B

A

CC

CM

B

A

A. calandrae walked extensively over the surface of the bean treated with the acetone extract from the experienced host and tried to oviposit on the bean.

Experienced female on CC

Host searching behavior of A. calandrae for olfactory cues. - Female experienced oviposition on the each hosts for 3 days. - The extracts (acetone) were made from black eye beans containing the larvae of each host species.

CM： C. maculatus

CC：C. chinensis

B: Clean black-eye beans A: Control (acetone)

Clean black-eye beans were treated with aceton extract from:

White line: the trajectories of walking A. calandrae.

CC

F

Time shift, L (week)

CC

F A. calandrae showed frequency-dependent preference.

Cross correlation：preference for CC, P (t) and the adult density of CC and CM, ( t + L ).

CCF for adult density of CC

Time

Host adult density ( periodic oscillation of 4 weeks )

Host larval density

Parasitoid Preference for CC

CC

CC

CM

CM

CCF for adult density of CM

-Negative correlation between

preference for CC - adult CC density

-2 weeks lag between adult CC density - vulnerable CC larvae density

-Positive correlation between preference for CC - vulnerable CC larvae density

Female parasitoid preference in fluctuating host-parasitoid multi-generation dynamics was examined.

Preference test every week.

Parasitoid absent

Non-learning parasitoids

g : degree of frequency-dependence.

Parasitoid present

Numerical simulation: learning / non-learning parasitoids

- Non-learning parasitoids does not prolong the coexistence time. - Frequency-dependence of host preference is the major mechanism that prolonged

the coexistence time.

The effect of frequency-dependent predation on the coexistence time of CC and CM was tested by numerical simulations using the stage-structured host-parasitoid model.

Conclusion : Frequency-dependent predation of A. calandrae the promoted the prey coexistence in this host-parasitoid system.

- Olfactory search image is thought to cause frequency-dependent predation.

- “Search image”: Perceptual change in the ability of predators to detect cryptic prey (Tinbergen 1960).

Birds selectively search for particular cryptic insects after discovering this type of prey because they ‘‘learn to see.’’

Search-image examples in insect visual predators

-Butterflies: Frequency-dependent oviposition

for two different shapes of leaves (Rausher 1978).

- Honeybees: Flower constancy.

Individuals often specialize on a few flower species while ignoring equally rewarding flowers (Chittka et al. 1999).

- Parasitoids：Frequency-dependent oviposition for aphid color polymorphism (Langley et al. 2006).

- Jumping spiders： Preference for the experienced prey type (Jackson & Li 2004).

Cognitive ecology

Our result showed the possible importance of cognition and leaning of organisms on species interaction, population dynamics, and species diversity in ecological communities.