Learning predator promotes coexistence of prey species in host–parasitoid systems

Abstract

Ecological theory suggests that frequency-dependent predation, in which more common prey types are disproportionately favored, promotes the coexistence of competing prey species. However, many of the earlier empirical studies that investigated the effect of frequency-dependent predation were short-term and ignored predator-prey dynamics and system persistence. Therefore, we used long-term observation of population dynamics to test how frequency-dependent predation influences the dynamics and coexistence of competing prey species using insect laboratory populations. We established two-host-one-parasitoid populations with two bruchid beetles, Callosobruchus chinensis and C. maculatus, as the hosts and the pteromalid wasp Anisopteromalus calandrae as their common parasitoid. When the parasitoid was absent, C. chinensis was competitively excluded in ∼20 wk. Introducing the parasitoid greatly enhanced the coexistence time to a maximum of 118 wk. In the replicates of long-lasting coexistence, the two host species C. maculatus and C. chinensis exhibited periodic antiphase oscillations. Behavioral experiments showed frequency-dependent predation of A. calandrae that was caused by learning. Females of A. calandrae learned host-related olfactory cues during oviposition and increased their preference for the common host species. Numerical simulations showed that parasitoid learning was the essential mechanism that promoted persistence in this host-parasitoid system. Our study is an empirical demonstration that frequency-dependent predation has an important role in greatly enhancing the coexistence of prey populations, suggesting that predator learning affects predator-prey population dynamics and shapes biological communities in nature.prey switching | flexible foraging | search image O ne of the key challenges of both ecology and evolutionary biology is to understand the mechanisms that maintain biodiversity. In Chesson's terms (1), species coexistence has been explained by two mechanisms: a "stabilizing" mechanism that includes classical niche differentiation, and an "equalizing" mechanism that includes neutral processes (2). Frequency-dependent predation is one of the strong stabilizing mechanisms that are essential for stable species coexistence (1). Since the 1970s, theoretical studies have investigated the effect of frequency-dependent predation on prey coexistence (3-8). Predators that feed on a variety of food items in nature can behaviorally switch to abundant prey types in response to temporal and spatial variations in resource availability. This causes frequency-dependent predation that generally promotes the coexistence of competing prey species because the foraging strategies of predators that switch to more common prey types could prevent rare prey types from being eliminated. However, more recent studies that incorporate prey switching as an optimal diet choice have argued that the effect of switching on the stability of predator-prey systems is quite complex, and sometimes destabilizing, depending on prey c...

Potential impact of the native hyperparasitoidConura albifrons(Hymenoptera: Chalcididae) on the exotic biological control agentDiadromus pulchellus(Hymenoptera: Ichneumonidae)

“…Biased parasitism rates on the common colour morph were consistent with changes in parasitism rates on the two colour morphs in the field (Langley et al, 2006). Similarly, learning resulted in frequency-dependent parasitism rates in Anisopteromalus calandrae (Howard) Hymenoptera: Pteromalidae) attacking two competing beetles Callosobruchus chinensis (L.) and Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae) (Ishii & Shimada, 2012). Simulations and lab experiments demonstrated that learning, acting through frequency-dependent parasitism, increased the stability of the system, allowing for coexistence of the two beetle species (Ishii & Shimada, 2012).…”

“…Similarly, learning resulted in frequency-dependent parasitism rates in Anisopteromalus calandrae (Howard) Hymenoptera: Pteromalidae) attacking two competing beetles Callosobruchus chinensis (L.) and Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae) (Ishii & Shimada, 2012). Simulations and lab experiments demonstrated that learning, acting through frequency-dependent parasitism, increased the stability of the system, allowing for coexistence of the two beetle species (Ishii & Shimada, 2012). To our knowledge, the link between learning and frequency-dependent parasitism has not been demonstrated for facultative hyperparasitoids such as C. albifrons.…”

Does the host's developmental stage affect host preference following an ovipositioning experience in Heterospilus prosopidis?

“…To this end, work with some pteromalid wasps that utilize the same host species and developmental stages and have oviposition learning ability would be useful (e.g., A. calandrae; Shimada & Fujii, 1985;Ishii & Shimada, 2012;Sasakawa et al, 2013). This finding is notable because in parasitoid wasps that parasitize both larval and pupal hosts, the host's developmental stages have attracted little attention as factors affecting oviposition learning.…”

“…In oviposition learning, various non-host-associated cues can, in principle, serve as conditioned stimuli (e.g., artificial chemical odors; Takasu & Lewis, 2003;Collatz et al, 2006;Schurmann et al, 2012). In the real world, however, cues more-or-less associated with hosts, such as hostinduced plant volatiles in host herbivore-parasite systems (as discussed in Bleeker et al, 2006) and some of the odor components of the host per se (figure 1 in Ishii & Shimada, 2010; see also Ishii & Shimada, 2012), are considered to often serve as conditioned stimuli.…”

The role of learning by a predator, Rivulus hartii, in the rare‐morph survival advantage in guppies

“…NFDS can operate either through enhanced survival or reproductive success of rare morphs. Our work, along with the work by Ishii & Shimada (), has elucidated a role of learning in generating NFD predation. In the study of NFD reproductive success, there is an analogous process: the ‘learned mate recognition’ hypothesis.…”