Effects of feeding on medicinal leech swimming performance

Abstract

The locomotor system of sanguivorous leeches is presented with a unique challenge: how to maintain mobility while coping with a 4500% increase in body mass during feeding. A meal of this size is likely to disrupt the function of the muscular hydrostat during swimming, reducing speed and increasing predation risks. We quantified the effects of feeding to satiety on swimming kinematics, and the time course of recovery of swimming performance post-feeding in the medicinal leech Hirudo verbana. There was a 5.07 AE 0.04-fold increase in mass during feeding (mean AE SEM, n= 7). Despite this, leeches were able to swim immediately after feeding, reaching 27% of their pre-feeding speed. Reduced speed was a consequence of a reduction in both swimming cycle frequency and stride length to 69 and 42% of the pre-feeding values, respectively. Recovery of swimming ability was rapid, despite a prolonged increase in body mass. Fifty per cent restoration of swimming speed was achieved in c. 1 h while body mass was still 4.2-fold greater than before feeding. Rapid mass and volume reduction immediately post-feeding, and the properties of the obliquely striated swimming muscles appear to aid recovery of swimming performance. Such features that aid postfeeding recovery of mobility may have been important in the evolution of leech sanguivory.

Multiplexed modulation of behavioral choice

“…When they did crawl, they took short steps with a longer cycle period. These blood-engorged leeches did not often attempt to swim, but when they did, their undulatory movements were slow and labored and the swimming episodes were short, consistent with previous observations (Claflin et al, 2009).…”

“…Chris R. Palmer, Megan N. Barnett, Saul Copado, Fred Gardezy and William B. Kristan, Jr* fed leeches do swim, they make slower progress because of both reduced cycle frequency and reduced distance covered per locomotor cycle ('stride length' in biomechanical terminology) (Claflin et al, 2009). The feeding-mediated distention of the leech body appears to inhibit swimming by activating stretch receptors in the body wall, which inhibit swim gating neurons or swim central pattern generator neurons (Gaudry and Kristan, 2010).…”

Leeches run cold, then hot

“…The increase in metabolism immediately after feeding is probably associated with increased urine production to expel plasma from the ingested blood, a process reliant on the active transport of ions [19]. This rapidly reduces body volume and restores mobility [17]. Increased body temperature during this period would accelerate this process and ensure earlier cessation of the associated SDA.…”

“…Leeches were then fed to satiation on a container of warmed, defibrinated sheep blood (Hemostat Laboratories, Dixon, CA, USA), obtained by biting through a Parafilmcovered aperture [17]. Position monitoring was repeated placing leeches in the gradient at 0, 24, 48, 120 and 240 h after feeding (n ¼ 6-7).…”

“…Medicinal leeches can increase their body mass 1000 per cent during feeding [15], and the resulting SDA involves a 600 per cent increase in aerobic metabolism that can persist for several days [16]. The selection pressures for rapid meal processing should be particularly strong in this group, as in addition to the energy allocation problems posed by SDA, distension of the body reduces flexibility and limits the ability of the body wall musculature to power swimming or crawling [17]. This increases vulnerability to predation [18], and much of the increased energy expenditure is probably associated with increased urine production to expel excess fluid to reduce body volume and restore mobility [19].…”