Chemosensory stimuli in feeding behavior of the leech Hirudo medicinalis

Abstract

The involvement of chemotherapy stimuli in the feeding behavior of the blood-sucking leech Hirudo medicinalis was investigated using a behavioral feeding test in which test solutions were encased in a highly permeable membrane and presented to the leech. Whole human blood or plasma at ambient temperature elicited the complete sequence of feeding behavior: probing, attachment, biting and ingestion. Spring water, 300 mM sucrose, or dialyzed plasma did not elicit any of these responses. Spring water warmed to 38 degrees C elicited probing and transient attachment but not ingestion. Thus, appropriate chemical stimuli were necessary for complete feeding behavior. A chemically defined artificial blood mix, containing the major components of low molecular weight found in blood, elicited all aspects of leech feeding behavior. Eliminating either NaCl or arginine from the mix resulted in complete loss of effectiveness. Moreover, a solution containing only NaCl (150 mM) and arginine (90 microM) was also an effective feeding stimulus. Thus, appropriate chemical stimuli are sufficient for complete feeding behavior. Neither NaCl nor arginine alone induced feeding although NaCl alone elicited probing. Sensory detection of blood was localized to a region of the dorsal lip that contains structures composed of ciliated, bipolar neurons, which are likely candidates as chemoreceptors. Surgical ablation of this region of the skin resulted in complete loss of ability to alert to, orient toward and ingest blood, while sham-operated controls fed normally. Substitution with other ions revealed specificity, with respect to both the cation and the anion, in the response to NaCl. Of the inorganic and organic cations tested, only Li+ substituted effectively for Na+. Of the inorganic and organic anions tested, only Br- was as effective as Cl-. Thus, the requirement for NaCl in leech feeding represents more than simply an ionic strength requirement or a requirement for Na+ ions and bears similarities to the chemosensory detection of NaCl in other species. Substitution with other amino acids and analogues for arginine revealed marked specificity in the feeding response to this compound as well. D-arginine at concentrations of up to 1000-fold greater than the effective threshold for L-arginine did not elicit ingestion, nor did other common L-amino acids, including the other basic amino acids histidine and lysine. Of the arginine analogues tested, only homoarginine and canavanine (in which all three functional groups of arginine are unchanged) were effective feeding stimulants.