Parasite Manipulation of Its Host’s Physiological Reaction to Acute Stress: Experimental Results from a Natural Beetle-Nematode System

Abstract

All animals, whether vertebrate or invertebrate, must be capable of reacting to acute stressors, such as escaping from predators, and most do so with a suite of transient physiological changes that temporarily enhance survival. Some of these changes include mobilization of immune cells and increased cardiac output. A small but growing number of studies have begun to show that certain parasites appear capable of modifying such responses. We addressed this topic using a natural host and parasite system, that is, a nematode (Chondronema passali) that parasitizes horned passalus beetles, Odontotaenius disjunctus (family Passalidae), of the eastern United States. With a series of experiments, we sought to determine whether this parasite affects (1) the immune reaction to stress, (2) the output of stress-induced alarm calls, or (3) the increase in heart rate that occurs in response to acute stressors, with the stressors being mechanical or thermal. Results showed that hemocyte density increased after both stressors in nonparasitized beetles but did not increase in parasitized beetles. While mobilization of immune cells would enhance host immunity during stress, this would also be damaging to the nematode, so this scenario appears to benefit the parasite. We found no evidence that the nematode suppresses the overall reaction to stress (or prevents stress from occurring), since parasitized beetles did not differ from nonparasitized ones in alarm call rates or in heart beat frequency after exposure to mechanical stressors. Suppression of the host's normal immune reaction to stressful stimuli could translate to delayed or even reduced wound healing or pathogen resistance during these events. This project is a rare demonstration of parasite manipulation of host immune response to acute stress and should stimulate further investigations into the interactive nature of stress and parasites.

The Heartrate Reaction to Acute Stress in Horned Passalus Beetles (Odontotaenius disjunctus) is Negatively Affected by a Naturally-Occurring Nematode Parasite

“…Prior work in our lab using this host–parasite system also indicated how this nematode can negatively affect the immune activation that takes place during an acute stress reaction [ 22 ]. In that study, acute stress (mechanical tumbling) led to an increase in circulating hemocyte abundance in healthy beetles, but in parasitized beetles the hemocyte proliferation following stress was significantly reduced.…”

“…Lower cardiac output would lead to less hemolymph distribution during stress, and by extension, fewer hemocytes being distributed during the stress event. Also of note from this prior work was that there was an attempt made to examine the effects of the nematode on ‘stressed’ beetle heartrates, and surprisingly, no effect was found [ 22 ]. However, in retrospect this probably had to do with the timing of the measurements; heartrates were measured before and after 10 min of mechanical stress.…”

“…Each experiment involved measuring heartrate in individual beetles, which has been described previously [ 22 ]. Briefly, we removed a section of the elytra near the posterior end of the beetle ( Figure 1 ) exactly one week prior to the experiment.…”

“…Despite this, the nematode seems to convey little outward negative effect to the host. Recent projects in our lab have begun to examine how this parasite affects its host [ 21 , 22 , 23 ], with particular attention given to behaviors and events in the lives of beetles where its impact might be felt most strongly, that is, during times of stress, when energy demand is high.…”

Limulus and heart rhythm

“…Like humans, beetles were also sensitive to heat as a source of physical stress, and at 45°C the corresponding values of HR in two groups increased to ~71 versus 69 beats min −1 (Davis et al, ). It was revealed that the “parasitism” did not influence the HR of host beetles Odontotaenius disjunctus and the mean values were 61 versus 64 beats min −1 when nematodes were absent.…”