Research Article: Functional Synchronization of Biological Rhythms in a Tritrophic System

Date Published: June 10, 2010

Publisher: Public Library of Science

Author(s): Sufang Zhang, Jianing Wei, Xiaojiao Guo, Tong-Xian Liu, Le Kang, Shin Yamazaki.

Abstract: In a tritrophic system formed by a plant, an herbivore and a natural enemy, each component has its own biological rhythm. However, the rhythm correlations among the three levels and the underlying mechanisms in any tritrophic system are largely unknown. Here, we report that the rhythms exhibited bidirectional correlations in a model tritrophic system involving a lima bean, a pea leafminer and a parasitoid. From the bottom-up perspective, the rhythm was initiated from herbivore feeding, which triggered the rhythms of volatile emissions; then the rhythmic pattern of parasitoid activities was affected, and these rhythms were synchronized by a light switch signal. Increased volatile concentration can enhance the intensity of parasitoid locomotion and oviposition only under light. From the top-down perspective, naive and oviposition-experienced parasitoids were able to utilize the different volatile rhythm information from the damaged plant to locate host leafminers respectively. Our results indicated that the three interacting organisms in this system can achieve rhythmic functional synchronization under a natural light-dark photoperiod, but not under constant light or darkness. These findings provide new insight into the rhythm synchronization of three key players that contribute to the utilization of light and chemical signals, and our results may be used as potential approaches for manipulating natural enemies.

Partial Text: The biological rhythm of most organisms is formed under an oscillatory environment of daily rotation of the planet earth, expressed as a roughly 24-hour cycle in their biochemical, physiological or behavioral processes [1]. These rhythms could be regulated by either endogenous circadian molecular machinery [2], [3] or external abiotic cues such as the presence or absence of light or food [4], [5]. Interestingly, it has also been suggested that biological factors, such as volatiles plants, can alter the behavior of an herbivore at different times of day [6], but this study did not provide clear evidence of rhythm interactions. Therefore, we sought to determine whether rhythms of different organisms could interact with each other, especially how abiotic and biotic factors could cooperatively regulate the rhythm interactions among different organisms. Here, we used a tritrophic system containing three closely related species to resolve this question.

In this study, we investigated the rhythms in a tritrophic system under LD, LL and DD, and presented a clear illustration of the rhythm correlations among three different organisms. It seems that they exhibited bidirectional correlations. From the bottom-up perspective, the results indicate that the biological rhythms of the lima bean, leafminer and parasitoid system are synchronized under the natural light-dark cycle, and the correlation was initiated from herbivore feeding, followed by the rhythms of volatile emissions, and then the rhythms of parasitoid activities. Our data showed that healthy lima beans produce few volatiles, but when damaged by leafminers, lima beans emitted a large amount of volatiles, and the larval feeding rhythm paralleled that of terpene emission from the leafminer-damaged lima bean plants but with one interval (3 hours) ahead. These observations suggest that volatiles were induced by the feeding of leafminers, and it took several hours for plants to respond to the damages from herbivores, as has been described before [9]. Parasitoid locomotion corresponded well with the emission of terpenes, and manipulating the plant volatiles by providing a high concentration in the chamber increased both parasitoid locomotion and oviposition rates (Figure 3A, 3B). Thus, the volatile emission rhythms drove the periodic activities of the parasitoids. However, the synchronized rhythms across the tritrophic levels were disrupted under LL and almost disappeared in the DD condition, indicating that light was a necessary synchronizer in this system. From the top-down perspective, the naive and oviposition-experienced parasitoids can differently interpret the volatile rhythm information, which may help the parasitoid locate its host efficiently.