Learning predator promotes coexistence of prey species in host–parasitoid systems
Learning predatorpromotes 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 maintainingspecies diversity in nature ? - Since the 1970s, theoretical studies have predicted that frequency- dependent predation is one of the strong mechanisms in maintaining prey coexistence. Predator Prey switching for abundant prey species Prey1 Prey2 Pedators that switch to more Population common prey types promotes the coexistence of prey species because it prevent rare prey types from being eliminated. Time - There is a lack of empirical evidence directly testing the effect of learning and frequency-dependent predation in a multigenerational prey–predator system.
Two- host one-parasitoid host-parasitoid systemExperimental insect population as a mimic of species interaction occurring innatural ecosystems. Parasitoid Anisopteromalus calandrae Predation Predation Host1: CM Competition Host2：CC Callosobruchus For resource beans Callosobruchus maculatus chinensis Does the presence / absence of a predator contribute to coexistence of two prey species? How does learning of a predator affect the dynamics?
Life cycle of seed beetles and parasitoids. The adult female lay their eggs on the surface of beans. Seed beetles - Insect Pests of stored beans. Challosobruchus chinensis Parasitoids - A parasite that oviposits Larvae feed and developChallosobruchus inside the beans. on and eventually kills themaculatus 4 weeks host organism. Anisopteromalus Adult emergence from calandrae the bean, and mating. Female wasp attacks 2weeks the host of about 2 week of age.
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.The predation pressure was altered by changing the ratio of the black-eyebean, BR. low Azuki beans BR = 0 Predation pressure Low parasitization rate. Refuge for host. BR = 0.5 Black-eye beans: ♪ BR = 1 High parasitization rate. high
Host-parasitoid population dynamics at varying predation pressure.Ratio of Black-eye beans: BR Number of Adults BR = 0 BR = 0 BR = 0 CM outcompeted CC. low Number of Adults BR = 0.2 BR = 0.2 Predation pressure Number of Adults BR = 0.5 BR = 0.5 Long coexistence of CM and CC. Number of Adults BR = 0.8 Outbreak of parasitoids. Number of Adults high BR = 0.8 BR = 1 BR = 1 Extinction of CM and CC.BR = 1 Time (weeks) Time (weeks) Time (weeks)
Parasitoid promoted the coexistence of host species ! Number of Adults Parasitoid absent Number of Adults Parasitoid present BR = 0.8 Time (week)
The coexistence time of CC and CM. Parasitoid absent Parasitoid present low Predation pressure highParasitoid introduction prolonged the coexistence time of CC and CMat intermediate predation pressure (BR=0.2, BR=0.5, BR=0.8).
Can A. calandrae distinguish between CC and CM ? Host search behavior of A. calandrae ! - Search the concealed host larvae in a bean with antennal tapping. - Oviposit on the host larva & pupa. Hatched egg of the seed beetle. Inside the bean Larva of CM Larva of CC 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.
A. calandrae learned to preferred the host they experienced. 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. Experienced Experienced Control female female on CM female on CC without experience Number of oviposition onNumber of oviposition mean±SE CC CM Conditioning time (h) Conditioning time (h) Conditioning time (h) A. calandrae increased preference for the Choice test conditioned host after 24 h.
A. calandrae distinguished between two hosts by olfactory cues. 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. Experienced Experienced Control female female on CM female on CC without experience Clean black-eye beans were treated with aceton extract from: CM： C. maculatus CC：C. chinensis CC B CC B: Clean black-eye beans A: Control (acetone) A CM CC A A CM White line: the trajectories of B CM walking A. calandrae. B 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. Ishii and Shimada (2010) Popul Ecol
A. calandrae showed frequency-dependent preference. Female parasitoid preference in fluctuating host-parasitoid multi- generation dynamics was examined. Cross correlation：preference for CC, P (t) and the adult density of CC and CM, ( t + L ). CCF for adult density of CC Preference test every week. CCF for adult density of CMCCF CCF Host adult density ( periodic oscillation of 4 weeks ) CM Time shift, L (week) CC Host larval density CC -Negative correlation between preference for CC - adult CC density CM -2 weeks lag between adult CC density - vulnerable CC larvae density Parasitoid Preference for CC -Positive correlation between preference for CC - vulnerable CC larvae density Time
Numerical simulation: learning / non-learning parasitoidsThe effect of frequency-dependent predation on the coexistence time of CC and CMwas tested by numerical simulations using the stage-structured host-parasitoid model. Parasitoid present g : degree of frequency-dependence. Non-learning parasitoids Parasitoid absent- Non-learning parasitoids does not prolong the coexistence time.- Frequency-dependence of host preference is the major mechanism that prolonged the coexistence time.
Conclusion : Frequency-dependent predation of A. calandrae thepromoted 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 specieswhile 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.