Behavioral and electrophysiological response of sugarcane aphids and imported fire ants to 2, 4, 6-trimethylpyridine, an alkaloid from the pink-spotted lady beetles

Authors: ZHOU, AIMING - Huazhong Agricultural University; Du, Yuzhe - Cathy; Riddick, Eric; LI, LEI - Chinese Academy Of Tropical Agricultural Sciences; Chen, Jian

Submitted to: Journal of Pest Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2021
Publication Date: 3/29/2021
Citation: Zhou, A., Du, Y., Riddick, E.W., Li, L., Chen, J. 2021. Behavioral and electrophysiological response of sugarcane aphids and imported fire ants to 2, 4, 6-trimethylpyridine, an alkaloid from the pink-spotted lady beetles. Journal of Pest Science. https://doi.org/10.1007/s10340-021-01363-6.
DOI: https://doi.org/10.1007/s10340-021-01363-6

Interpretive Summary: The mutualistic relation between some ants and aphids has been well documented. For example, sugarcane aphids produce honeydew for the red imported fire ants, in exchange, fire ants protect the aphids from predators, such as pink-spotted lady beetles. So, lady beetles have to compete with ants for their resources. Chemical communication plays an important role in the lives of insects. It is known that volatiles released by lady beetles are important for their chemical communication within the species. However, whether these compounds influence insects of other species, such as aphids and ants, is still not clear. In this study, we investigated the behavioral and electrophysiological responses of sugarcane aphids, red imported fire ants, and pink-spotted lady beetles to an alkaloid, 2, 4, 6-trimethylpyridine (TMP), which was identified from the pink-spotted lady beetles. The results showed that TMP elicited significant electroantennogram responses in all three tested insects. In addition, TMP triggered significant preference and aggregation in both males and females of pink-spotted lady beetles, while induced a strong avoidance in sugarcane aphids. TMP repelled red imported fire ants at high concentration, but showed certain attractiveness to fire ants at low concentration. TMP significantly reduced aphid-tending efficiency of the red imported fire ants. The findings provide important evidence that TMP is a pheromone in pink-spotted lady beetles and a semiochemical to both red imported fire ants and sugarcane aphids. This compound may affect the mutualistic interactions between red imported fire ants and sugarcane aphids by mediating the behaviors of both species. These findings may help us better understand the ant-aphid-lady beetle interactions.

Technical Abstract: Semiochemicals play key roles in mediating interactions between ecological niche-related species. Many predatory coccinellids conflict with hemipteran tending ants, because they both use hemipterans as resources. Lady beetles may thus be important in the ecology of ants and their reciprocal relationship with hemipterans. Volatiles released by lady beetles have diverse biological significance in intraspecific communication, attraction, and aggregation. However, whether the semiochemicals from lady beetles influence the sympatric members, such as aphids and ants, are still obscure. Sugarcane aphids Melanaphis sacchari (Zehntner) (Hemiptera: Aphididae) was closely associated with honeydew collecting ants and coccinellid predators. Herein, we investigated the behavioral and electrophysiological responses of M. sacchari and their attending red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae) to an alkaloid, 2, 4, 6-trimethylpyridine (TMP), which was recently identified from the pink-spotted lady beetle Coleomegilla maculata De Geer (Coleoptera: Coccinellidae). The response of C. maculata to this alkaloid was also evaluated. The results showed that TMP elicited significant electroantennogram (EAG) responses in M. sacchari, S. invicta, and C. maculata. In addition, it triggered significant preference and aggregation in both C. maculata males and females at 100 µg/µL, while induced a strong avoidance in M. sacchari. It significantly decreased the digging and residing preference of S. invicta workers at high concentration, but showed certain attractiveness to workers at a lower concentration. Further investigations showed that TMP inhibited aphid-tending efficiency of S. invicta thereby curbing the benefits to M. sacchari. The findings provide important evidence that TMP is a pheromone in C. maculata and a semiochemical to both S. invicta and M. sacchari. It may affect the mutualistic interactions between S. invicta and M. sacchari by mediating the behaviors of both species.