Learning Spatial Aversion Is Sensory-Specific in the Hematophagous Insect Rhodnius prolixus

Abstract

Even though innate behaviors are essential for assuring quick responses to expected stimuli, experience-dependent behavioral plasticity confers an advantage when unexpected conditions arise. As being rigidly responsive to too many stimuli can be biologically expensive, adapting preferences to time-dependent relevant environmental conditions provide a cheaper and wider behavioral reactivity. According to their specific life habits, animals prioritize different sensory modalities to maximize environment exploitation. Besides, when mediating learning processes, the salience of a stimulus usually plays a relevant role in determining the intensity of an association. Then, sensory prioritization might reflect an heterogeneity in the cognitive abilities of an individual. Here, we analyze in the kissing bug Rhodnius prolixus if stimuli from different sensory modalities generate different cognitive capacities under an operant aversive paradigm. In a 2-choice walking arena, by registering the spatial distribution of insects over an experimental arena, we evaluated firstly the innate responses of bugs confronted to mechanical (rough substrate), visual (green light), thermal (32°C heated plate), hygric (humidified substrate), gustatory (sodium chloride), and olfactory (isobutyric acid) stimuli. In further experimental series bugs were submitted to an aversive operant conditioning by pairing each stimulus with a negative reinforcement. Subsequent tests allowed us to analyze if the innate behaviors were modulated by such previous aversive experience. In our experimental setup mechanical and visual stimuli were neutral, the thermal cue was attractive, and the hygric, gustatory and olfactory ones were innately aversive. After the aversive conditioning, responses to the mechanical, the visual, the hygric and the gustatory stimuli were modulated while responses to the thermal and the olfactory stimuli remained rigid. We present evidences that the spatial learning capacities of R. prolixus are dependent on the sensory modality of the conditioned stimulus, regardless their innate valence (i.e., neutral, attractive, or aversive). These differences might be given by the biological relevance of the stimuli and/or by evolutionary aspects of the life traits of this hematophagous insect.

Molecular and functional basis of high-salt avoidance in a blood-sucking insect

“…Salt concentration modulates the behavior of the hematophagous bug Rhodnius prolixus, triggering avoidance or preference responses. For example, they avoid walking over surfaces coated with high-NaCl or -KCl (1 M) while preferred those added with low-NaCl or KCl (0.1 M) (Masague ´et al, 2020;Minoli et al, 2018). Furthermore, R. prolixus accepts feeding on an artificial solution containing a NaCl concentration similar to that of the vertebrate plasma (0.15 M), while refusing if it is above this level (R0.2 M) (Cano et al, 2017;Pontes et al, 2017).…”

Perception of aversive stimuli of different gustatory modalities in an haematophagous insect,Rhodnius prolixus

“…In a completely different behavioural context, Mengoni and collaborators (2017) showed that the innate attractive response to faeces of the kissing bug Triatoma infestans can be switched to avoidance if an aversive conditioning protocol is applied. Finally, Minoli and collaborators (2018) were able to demonstrate that the learning efficiency of R. prolixus under an aversive operant conditioning tested over a spatial preference walking arena, is highly dependent on the sensory modality of the conditioned stimulus.…”

Salty surfaces deter feeding in a blood-sucking disease vector

“…R. prolixus does a gustatory evaluation of the feeding and walking substrate (25, 26, 31). Here, we showed that high doses (1M) of both NaCl and KCl negatively interfered with feeding.…”

“…Salt concentration modulates the behavior of the hematophagous bug Rhodnius prolixus , triggering preference or avoidance responses. For example, they avoid surfaces coated with high-NaCl or -KCl (1 M) (25, 26), preferring instead surfaces impregnated with salt concentrations similar to those of the human sweat (0.1 M) (24, 25). Furthermore, R. prolixus accepts or rejects a feeding solution depending on its NaCl or KCl concentration (3, 8).…”