Olfactory detection of trace amounts of plant volatiles is correlated with testosterone in a passerine bird

Abstract

In response to damage by insects, plants release herbivore-induced plant volatiles (HIPVs) into 17 the air. Insectivorous birds exploit these cues and, consequently, reduce the damages inflicted to the plants. However, little is known about whether they solely use HIPVs as foraging cues, or if 19 they also use them to modulate traits linked to reproduction. As caterpillars are the primary food 20 source required for insectivorous birds to raise offspring, their ability to locate and predict future 21 peaks in caterpillar biomass using olfaction is likely to be advantageous. Therefore, we tested 22 whether an insectivorous songbird that naturally inhabits oak dominated forests can be trained to 23 detect early spring infestation by hatchling caterpillars, at a time when oaks begin bursting, and 24 birds prepare to breed. Tree buds were either infested with caterpillars or left as a control and 25 visually obscured in a Y-Maze choice test. Additionally, we measured testosterone and 17β-26 estradiol as they influence olfactory perception in mammals and are linked to reproduction in 27 vertebrates. After being trained to associate the presence of HIPVs with that of food, blue tits 28 spent more time with, were more active around, and more frequently chose to first visit the infested 29 trees, showing that blue tits can smell caterpillar activity. Males with higher testosterone spent 30 more time around infested trees, suggesting that foraging behavior during the pre-breeding 31 season is linked with a major reproductive signal. There was no relationship between foraging 32 and estradiol in females. These results are an important foundation for further investigation of the 33 role of hormones in avian olfaction and how smell may be useful for making breeding decisions 34 that could improve reproductive success.

Exogenous Application of Methyl Jasmonate Increases Emissions of Volatile Organic Compounds in Pyrenean Oak Trees, Quercus pyrenaica

“…However, we have to admit that we do not know how exactly this dose mimics the situation when oak trees are infected by caterpillars. Furthermore, based on previous results with Quercus pubescens, where authors found that the emission of VOCs significantly increased from 42 hours after infestation (Graham et al unpublished data,in [29]), we decided to measure the volatiles of our trees after 62 hours from infestation or MeJA application. Therefore, it is possible that differences in the dosage as well as in the timing of the measurement may have provided different results in the analysis of volatiles.…”

“…after placing caterpillars on the sachets or applying MeJA treatment. We collected volatiles 62 hours after adding the treatments because previous results in another Quercus species, the downy oak tree (Quercus pubescens Willd) suggest that HIPVs significantly increase from 48 h after infestation by winter moth (Operophtera brumata) and green oak tortrix (Tortrix viridana) when compared to uninfested control trees (Graham et al unpublished data, in [29]). For each volatile measurement, we removed the organza bag from each branch and removed the caterpillars from the Herbivore-treated trees.…”

“…Therefore, it seems that olfaction is used by birds to search for food [25,27], although the importance of vision and olfaction in foraging behaviour of birds is not completely understood (yet [27,28]). Recent evidence shows that insectivorous birds can detect even small concentration of HIPVs of Herbivore-infested trees that are just developing the new leaves [29], or small amounts of volatiles emitted during insect egg deposition [30]. Attraction to caterpillar-infested trees has been studied in different plantinsect-bird systems using ununified methodology [21,23,24,[29][30][31][32] and showing often contradictory results.…”

Exogenous Application of Methyl Jasmonate Increases Emissions of Volatile Organic Compounds in Pyrenean Oak Trees, Quercus pyrenaica

“…We collected plant volatiles of all experimental trees ( n = 45), and four additional blank samples, 62 h (mean ± SE = 62 ± 1.05 h) after the beginning of the experiment, i.e., after placing caterpillars on the sachets or applying MeJA treatment. We collected volatiles 62 h after adding the treatments because previous results in another Quercus species, the downy oak tree ( Quercus pubescens Willd), suggest that HIPVs significantly increase from 48 h after infestation by winter moth ( Operophtera brumata ) and green oak tortrix ( Tortrix viridana ) when compared to uninfected control trees (Graham et al unpublished data, [ 29 ]). For each volatile measurement, we removed the organza bag from each branch and removed the caterpillars from the Herbivore-treated trees.…”

“…Therefore, it seems that olfaction is used by birds to search for food [ 25 , 27 ], although the importance of vision and olfaction in the foraging behavior of birds is not completely understood yet [ 27 , 28 ]. Recent evidence shows that insectivorous birds can detect even small concentrations of HIPVs of herbivore-induced trees that are just developing new leaves [ 29 ], or small amounts of volatiles emitted during insect egg deposition [ 30 ]. Attraction to caterpillar-infested trees has been studied in different plant-insect-bird systems using ununified methodology [ 21 , 23 , 24 , 29 , 30 , 31 , 32 ] and often showing contradictory results.…”