Role of Rhipicephalus microplus cheliceral receptors in gustation and host differentiation

Authors: LOPES FERREIRA, LORENA - Federal University Of Goias; FERNANDES SOARES, SARA - Federal University Of Goias; GOMES DE OLIVEIRA, JAIRES - Federal University Of Goias; TATIELLY OLIVEIRA, THAYNARA - Federal University Of Goias; Perez De Leon, Adalberto - Beto; BORGES, LIGIA - Federal University Of Goias

Submitted to: Ticks and Tick Borne Diseases
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/31/2014
Publication Date: 4/1/2015
Publication URL: http://handle.nal.usda.gov/10113/62306
Citation: Lopes Ferreira, L., Fernandes Soares, S., Gomes De Oliveira, J., Tatielly Oliveira, T., Perez De Leon, A.A., Borges, L. 2015. Role of Rhipicephalus microplus cheliceral receptors in gustation and host differentiation. Ticks and Tick Borne Diseases. 6:228-233.

Interpretive Summary: The southern cattle fever tick is considered the most economically important external parasite of cattle worldwide. Breeds of cattle originally from Asia are less susceptible to tick infestation than breeds that originated in Europe. Sensory organs in the mouthparts of ticks are known to respond differently to substances that stimulate blood feeding. However, the role of those sensory organs in blood feeding relative to the susceptibility of cattle to infestation with ticks remains to be fully understood. We addressed this topic by studying the electrical properties of taste in preparations of mouthparts containing sensory organs from female southern cattle fever ticks. Solutions of substances (sodium and potassium chloride, glucose, adenosine triphosphate, and reduced l-glutathione) known to stimulate feeding in hard ticks were tested at different concentrations. Serum samples from six susceptible cattle of the Girolando breed, a mix of Asian and European cattle breeds, and six resistant Nelore bovines (pure Asian breed) were also tested. A dose-dependent response of taste neurons associated with the mouthpart sensory organ to all the feeding stimulants, except potassium chloride, was observed. Notably, electrical responses to potasium chloride and glucose by a mouthpart sensory structure of the southern cattle fever tick termed the cheliceral inner digit pit sensilla were also observed and they are reported here for the first time. Chemical receptors in the southern cattle fever tick mouthparts responded differently to serum from cattle susceptible and resistant to infestation. Sensory neurons in the mouthparts were more responsive to serum of tick resistant bovines than to serum samples from susceptible cattle. The implications of sensation to chemicals during tick blood feeding are discussed.

Technical Abstract: Rhipicephalus microplus is considered the most economically important ectoparasite of cattle worldwide. It is known that zebuine breeds of cattle are less susceptible to tick infestation than taurine breeds. Contact chemoreceptors in the cheliceral pit sensilla of ticks respond selectively to phagostimulant compounds, however their role in blood feeding relative to host susceptibility to infestation remains to be fully understood. We addressed this topic by conducting taste electrophysiology experiments with cheliceral pit sensilla preparations of R. microplus females. Solutions of five known ixodid tick phagostimulants were tested at different concentrations: sodium (NaCl), and potassium chloride (KCl) (10-3–10-1 M); glucose (10-4–10-1 M); adenosine triphosphate (ATP) (10-6–10-2 M); and reduced l-glutathione (GSH) (10-6 –10-2 M). Serum samples from six susceptible animals of the Girolando breed (5/8 Bos indicus × 3/8 B. taurus) and six resistant Nelore bovines (pure B. indicus) were also tested. A dose-dependent response of gustatory neurons associated with the chelicerae sensillum to NaCl, glucose, GSH, and ATP were observed. Responses by the cheliceral inner digit pit sensilla of R. microplus to KCl and glucose were also observed and they are reported here for the first time. In addition to an electrophysiological response to known phagostimulants, chemoreceptors in the chelicera of R. microplus responded differently to serum from cattle susceptible and resistant to infestation. The cheliceral pit neurons were more responsive to serum of R. microplus resistant bovines with a higher mean spike frequency (53.5 ± 2 spikes s-1 ) than to serum samples from susceptible cattle (40.3±2 spikess-1). The implications of chemosensation during tick blood feeding are discussed.