Research Article: Laser surgery reveals the biomechanical and chemical signaling functions of aphid siphunculi (cornicles)

Date Published: October 8, 2018

Publisher: Public Library of Science

Author(s): Serine Alfaress, Craig R. Brodersen, El-Desouky Ammar, Michael E. Rogers, Nabil Killiny, Antonio Riveiro Rodríguez.


Aphids are an attractive food source to many predators and parasitoids because of their small size, soft bodies and slow movement. To combat predation, aphids evolved both behavioral and chemical defensive mechanisms that are operated via siphunculi (cornicles), differently developed structures that more or less extend from their abdomen. Although both direct and indirect linkages between siphunculi and their defensive mechanisms have been explored, their ultimate effects on aphid fitness are still broadly debated. To explicitly test the influence of siphunculi on brown citrus aphid, Aphis (Toxoptera) citricida (Kirkaldy), fitness, we razor-cut and laser-sealed the siphunculi. Siphunculi removal resulted in two distinct behavior modifications, (false aggregation and increased drop-off rates) that led to decreased survival and the loss of the ability to right themselves from an inverted position. These results together indicate that siphunculi play an important role in survival, and removal of these organs will have negative effect on aphid fitness. Furthermore, results suggested that released alarm pheromone may play an important role in communication among aphid clone-mate, and omitting it results in miscommunication and competition among clonemates. These findings will help in better understanding the aphid biology.

Partial Text

As aphids (Hemiptera, Aphididae) aggregate in high-density colonies on the stems and leaves of host plants, they are highly vulnerable to predation [1, 2]. To defend themselves, aphids have evolved physical, behavioral and chemical defensive mechanisms [2, 3] that appear to be linked to both the preservation of the individual and the colony, which likely stems from their parthenogenetic life history [4, 5]. A unique morphological structure of aphids that appears to play a major role in these defense mechanisms are the siphunculi (or siphunculi), two unique tube-like structures found only in aphids [6], and located dorsally/dorso-laterally on the posterior part of the abdomen [1, 6]. Siphunculi secrete two types of defensive compounds–a sticky droplet that binds the appendages and mouthparts of predators [7, 8] and an alarm pheromone, trans-β-farnesene ((E)-β-farnesene) used for chemical signaling [9]. Siphunculi have received significant attention from researchers, and rightly so: aphids are a significant agricultural pest and have also become model organisms for studying the ecology of predator-prey relationships [10]. While many studies hypothesize the direct or indirect fitness benefits provided by siphunculi, no definitive research shows the direct impact of the presence or absence of siphunculi on aphid survival and fitness. Investigating the effect of siphunculi removal will help in exploring their impact on aphid biology.

The evolution and diversification of siphunculi within the Aphididae suggests a strong link between their function and fitness of aphids. Therefore, given the range of reported functions associated with siphunculi, the loss of cornicle function should incur some degree of disruption in communication dynamics and decreases in direct or indirect fitness. Our results show that cornicle removal had no influence on survival or reproduction in isolated aphids, but cornicle removal led to significant fitness costs when aphids were in close proximity and within the effective range of the signaling pheromone trans-β-farnesene emitted from siphunculi. Interestingly, the loss of communication ability in aphids without siphunculi could be recovered by the addition of aphids with fully functional siphunculi to the colony, strongly implicating the trans-β-farnesene in the structuring of the spatial organization of aphids on the host plant. Furthermore, to our knowledge, our data identify siphunculi an important biomechanical structure that they use to flip over after being inverted. So, siphunculi function at both ends of the functional spectrum: they emit the alarm pheromone that initiates drop-off behavior, which may cause them to fall onto their backs, and the siphunculi then serve as a biomechanical fulcrum point for inversion in A. citricida.




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