Host plant defense signaling in response to a coevolved herbivore combats introduced herbivore attack

Abstract

Defense-free space resulting from coevolutionarily naïve host plants recently has been implicated as a factor facilitating invasion success of some insect species. Host plants, however, may not be entirely defenseless against novel herbivore threats. Volatile chemical-mediated defense signaling, which allows plants to mount specific, rapid, and intense responses, may play a role in systems experiencing novel threats. Here we investigate defense responses of host plants to a native and exotic herbivore and show that (1) host plants defend more effectively against the coevolved herbivore, (2) plants can be induced to defend against a newly-associated herbivore when in proximity to plants actively defending against the coevolved species, and (3) these defenses affect larval performance. These findings highlight the importance of coevolved herbivore-specific defenses and suggest that naïveté or defense limitations can be overcome via defense signaling. Determining how these findings apply across various host-herbivore systems is critical to understand mechanisms of successful herbivore invasion.

Keywords: Coevolution; HIPVs; defense priming; herbivore-induced plant volatiles; insect herbivore; invasive species; naïve host; plant defense; plant–plant signaling.

Figure 1

Fifth instar cactus-boring moth larvae. (A) Cactoblastis cactorum (Berg) and (B) Melitara prodenialis Walker.

Figure 2

Observable inducible defenses of Opuntia. (A) Programmed cell death defense in Opuntia humifusa, (B) mucilage defense in O. humifusa, and (C) programmed cell death defense and mucilage in Opuntia stricta.

Figure 3

Experimental design of the two rearing experiments. (A) For Experiment 1 at Mississippi State University (2009–2010), two rearing rooms were used. The treatment of Cactoblastis cactorum reared only in the presence of plants infested with C. cactorum was separated in time from the treatment of C. cactorum reared in the presence of plants fed on by Melitara prodenialis (as well as M. prodenialis reared in the presence of plants fed on by C. cactorum). Half of the cages contained Opuntia stricta as the host plant, and the other half contained Opuntia humifusa. (B) In Experiment 2 at Arkansas State University (2010–2011), four treatments (C. cactorum reared only in the presence of plants fed on by C. cactorum, C. cactorum reared in the presence of plants fed on by with M. prodenialis, M. prodenialis reared in the presence of plants fed on by C. cactorum, and M. prodenialis reared only in the presence of plants fed on by M. prodenialis) were separated in space, in three rearing rooms. Half of the cages contained O. stricta as the host plant, and half contained O. humifusa.

Figure 4

Host plant defense responses resulting from the four treatments applied. Percentage of plants defending at each of the described observable defense levels is shown. Data were analyzed with a Kruskal–Wallis test followed by a least significant difference in ranks test to determine pair-wise differences. Different letters above bars indicate significant differences between treatments.

Figure 5

Larval performance responses to the four treatments applied. (A) Average larval development time, (B) percent survivorship to pupation, and (C) mean female pupal mass for each of the experimental treatments. Orange squares denote Cactoblastis cactorum and blue squares denote Melitara prodenialis larval performance responses. Error bars are 95% confidence intervals; different letters above mean points indicate significant differences at P < 0.05. Data were analyzed with a general linear mixed model with herbivore treatment as a fixed effect and experiment as a random effect. Pair-wise differences were determined with a Tukey LSD. Size differences exist between pupae of opposite sexes; only mass of female pupae is presented to eliminate bias associated with uneven sex ratios.