A larval aggregation pheromone as foraging cue for insectivorous birds

Although birds have traditionally been considered anosmic, increasing evidence indicates that olfaction plays an important role in the foraging behaviours of insectivorous birds. Recent studies have shown that birds can exploit herbivore-induced plant volatiles and sexual pheromones of adult insects to locate their prey. Many insectivorous birds prey on immature insects, providing relevant ecosystem services as pest regulators in natural and agricultural ecosystems. We asked whether birds could rely on chemical cues emitted by the immature stages of insects to prey on them. To address this question, we performed field experiments to evaluate if insectivorous birds can detect the aggregation pheromone produced by the larvae of the carpenter worm, Chilecomadia valdiviana . Groups of five artificial larvae were placed in branches of 72 adult trees in a remnant fragment of a sclerophyllous forest in central Chile. Each grouping of larvae contained a rubber septum loaded with either larval pheromone as treatment or solvent alone as control. We found that the number of larvae damaged by bird pecks was significantly higher in groups with dispensers containing the larval extract than in control groups. Our results show that birds can rely on immature insect-derived chemical cues used for larvae aggregation to prey on them.

Evolved differences in larval social behavior mediated by novel pheromones

Pheromones, chemical signals that convey social information, mediate many insect social behaviors, including navigation and aggregation. Several studies have suggested that behavior during the immature larval stages of Drosophila development is influenced by pheromones, but none of these compounds or the pheromone-receptor neurons that sense them have been identified. Here we report a larval pheromone-signaling pathway. We found that larvae produce two novel long-chain fatty acids that are attractive to other larvae. We identified a single larval chemosensory neuron that detects these molecules. Two members of the pickpocket family of DEG/ENaC channel subunits (ppk23 and ppk29) are required to respond to these pheromones. This pheromone system is evolving quickly, since the larval exudates of D. simulans, the sister species of D. melanogaster, are not attractive to other larvae. Our results define a new pheromone signaling system in Drosophila that shares characteristics with pheromone systems in a wide diversity of insects.

Laboratory assessment of the role of a larval pheromone and natural stream odor in spawning stream localization by migratory sea lamprey (Petromyzon marinus)

This study used large laboratory mazes and natural stream waters to test the role of olfactory cues, including a pheromone released by larvae, in spawning stream localization by migratory sea lamprey (Petromyzon marinus). We found that migratory lamprey strongly prefer stream water over lake water and that this response is dependent upon a functional olfactory system. Responses persisted among migratory lamprey even after stream water was diluted a thousand times but were not seen among non-migratory lamprey. Experiments using waters from five streams demonstrated that a larval pheromone is a key determinant of stream attractiveness: water from streams with larval populations were consistently more attractive than those without, and adding larval odor to the latter reversed this relationship. Larval odor was attractive at low, realistic concentrations, especially when presented together with natural stream water, suggesting that streams contain other odors that synergize the actions of the pheromone. Some, but not all, of the activity of the larval pheromone could be explained by two bile acids released by larvae (petromyzonol sulfate and allocholic acid). Together, these results strongly suggest that migratory lamprey locate streams using a larval pheromone. This cue could be useful in lamprey control.

Direct behavioral evidence that unique bile acids released by larval sea lamprey (Petromyzon marinus) function as a migratory pheromone

Four behavioral experiments conducted in both the laboratory and the field provide evidence that adult sea lamprey (Petromyzon marinus) select spawning rivers based on the odor of larvae that they contain and that bile acids released by the larvae are part of this pheromonal odor. First, when tested in a recirculating maze, migratory adult lamprey spent more time in water scented with larvae. However, when fully mature, adults lost their responsiveness to larvae and preferred instead the odor of mature individuals. Second, when tested in a flowing stream, migratory adults swam upstream more actively when the water was scented with larvae. Third, when migratory adults were tested in a laboratory maze containing still water, they exhibited enhanced swimming activity in the presence of a 0.1 nM concentration of the two unique bile acids released by larvae and detected by adult lamprey. Fourth, when adults were exposed to this bile acid mixture within flowing waters, they actively swam into it. Taken together, these data suggest that adult lamprey use a bile acid based larval pheromone to help them locate spawning rivers and that responsiveness to this cue is influenced by current flow, maturity, and time of day. Although the precise identity and function of the larval pheromone remain to be fully elucidated, we believe that this cue will ultimately prove useful as an attractant in sea lamprey control.

Factors influencing the selection of larviposition sites in the laboratory by Glossina morsitans morsitans Westwood (Diptera: Glossinidae)

Pregnant females of Glossina morsitans morsitans Westw. were offered choices of larviposition sites in the vicinity of various models and patterns. Ground-level surfaces of black, green, white or red were not attractive. Vertical surfaces did not attract a majority of flies, but 50% of those that settled on them gave birth in that region of the chamber. Shade cast by horizontal surfaces was attractive, but shade cast by vertical objects was not. Models with an enclosed space were attractive, but larviposition rarely occurred within the model, probably because flies do not readily enter cavities unless the temperature is very high. Among patterns presented at a distance, a simple unbroken area of black was more attractive than equivalent areas in the form of stripes, etc. No distinction was made between stripes presented vertically, horizontally and at an angle. Models representing logs or trees with rot holes were not attractive. Models with subterranean cavities, even a simple trench, were attractive. Loose sand was not more attractive than sand glued to a substrate, but there was an indication of a preference for larger particles. No evidence was obtained for the hypothesis of Nash et al. (1976) that a larval pheromone attracts gravid females to larviposition sites.

Observations on the free larval stage of Glossina morsitans morsitans Westw. (Diptera, Glossinidae): the possibility of a larval pheromone

Under simulated natural conditions the anal orifice of the larva of Glossina morsitans morsitans Westw. appears to open either at or soon after parturition. The larva burrows on average within two minutes of deposition; pupariation is completed 10–15 min later. Using methods that prevent burrowing and prolong the crawling period, certain larval movements were related to the pre-pupariation anal discharges and to the rapid spread of the fluid. Although the anus is not generally thought to be connected with the hind gut during the whole of larval life, the presence of uric acid in the discharges indicates that the fluid is a product of Malpighian tubule excretion. In a two-choice chamber in an incubator, flies larviposited significantly more often in the experimental pot if it contained a water- or ether-soluble extract of larval excretion in addition to any pupariating larvae. This points to the presence of a larval phero-mone which may attract gravid females to a breeding site.