Hunger is the best spice: Effects of starvation in the antennal responses of the blood-sucking bug Rhodnius prolixus

Abstract

Blood-sucking insects strongly rely on olfactory cues to find their vertebrate hosts. As in other insects with different lifestyles, it has been shown that endogenous and exogenous factors modulate olfactory responses. The triatomine bug Rhodnius prolixus is an important vector of Chagas Disease and a classical model for studies of physiology and behavior. In this species, the behavioral response to host-derived odorants is modulated by both the time of the day and the starvation. Here I investigated the peripheral neural mechanisms underlying these modulatory effects. For this, I measured the electroantennogram (EAG) responses of insects towards different concentrations (from 0.5% to 75% vol/vol) of an attractive host- odorant, ammonia. I tested the responses of starved and fed animals during the middle of the day (when insects are inactive and aggregated in refuges) and at the beginning of the night (when insects become active and search for hosts). Regardless of the time of the day and the starvation status, EAG responses systematically increased with odorant concentration, thus accurately reflecting the response of olfactory receptor cells. Interestingly, the EAG responses of starved insects were larger than those of fed insects only during the night, with larger differences (6–7 times) observed at low-middle concentrations. This is study is, to my knowledge, the first reporting modulation of sensory responses at the neural level in triatomines. This modulation, considering that triatomine hosts are mostly diurnal and are also potential predators, has an important adaptive value, ensuring that insects search for hosts only when they are hungry and at appropriate times.

Molecular basis of peripheral olfactory plasticity in Rhodnius prolixus, a Chagas disease vector

“…Larval R. prolixus display reduced electrophysiological responses to ammonia after ingesting a blood meal (Reisenman, 2014). Moreover, engorged triatomine larvae are refractory to host odor stimulation for a prolonged time after feeding (Bodin et al, 2009a) and remain hidden in shelters for several days while their molting is completed.…”

Neuroethology of Olfactory-Guided Behavior and Its Potential Application in the Control of Harmful Insects

“…It should be noted that any odor-based control strategy should consider that different types of natural odor stimuli (including background odors) often interact (e.g., Chaffiol et al, 2012 , 2014 , see also Section Effects of Background Odor). In addition, it should be considered that the physiological state of the insects (e.g., mating, feeding) as well as learning affects their responses to odors (e.g., Barrozo et al, 2010 ; Saveer et al, 2012 ; Reisenman, 2014 ; Matthews et al, 2016 ; Section Plasticity in the Responses to Semiochemicals).…”

“…In both blood-sucking and herbivorous insects the activity of ORCs can be affected by experience (e.g., long-term odor exposure and sensory adaptation to deterrents; see Section Mating Disruption). Experience can also cause downregulation of olfactory responses according to the feeding/mating status, and the time of the day (e.g., Almaas et al, 1991 ; Fox et al, 2001 ; Takken et al, 2001 ; Glendinning et al, 2009 ; Saveer et al, 2012 ; Stanczyk et al, 2013 ; Anderson and Anton, 2014 ; Claudianos et al, 2014 ; Reisenman, 2014 ). In general, associative learning is not usually represented at this level, although recent work in honeybees revealed that olfactory memories downregulate the expression of specific ORs.…”

The Post-mating Switch in the Pheromone Response of Nasonia Females Is Mediated by Dopamine and Can Be Reversed by Appetitive Learning

“…Other important factors influencing the strength of odor guided behavior in insects are related to their physiological state (Gadenne et al, 2016 ). Starving individuals, for example, respond more strongly to food-related odors than satiated ones (Edgecomb et al, 1994 ; Reisenman et al, 2013 ; Reisenman, 2014 ) and the response to sex pheromones depends on the age insects reach sexual maturity (Shorey et al, 1968 ; Landolt and Heath, 1988 ). Similar to some mammals (Serguera et al, 2008 ), the mating status of insects is another intrinsic parameter modulating their olfactory response to sex pheromones (Gadenne et al, 2016 ).…”