Fever and Behavioural Temperature Regulation in the Frog Rana esculenta

Abstract

The skin and colonic temperatures were recorded in frogs (Rana esculenta) which had selected a suitable microenvironment in a box filled with 2-3 cm water. The water temperatures ranged from 0 degrees C to + 40 degrees C. Such measurements were performed before and after intraperitoneal injections of killed pathogenic bacteria (M. xenopi and M. range), killed non-pathogenic bacteria (M. aquae II) and 0.9% sterile saline, intraperitoneal injections of blood plasma from frogs pre-injected with killed M. ranae, injections of PGE1 into the brain. The injections of pathogenic bacterial endotoxin caused, after latencies of 5-120 min, higher preferred water temperatures, which produced an average maximum colonic temperature increase of 6.5 degrees C +/- 1.0 degrees C (S.E.) (p less than 0.001). The non-pathogenic bacteria and sterile saline caused no temperature change. Monophasic hyperthermia of shorter latency was caused by injections of blood plasma from frog preinjected with M. ranae. Monophasic hyperthermia of the shortest latency was observed after diencephalic injections of PGE1. Based on their similarity we suggest that ectothermic and endothermic fever have a common phylogenetic origin.

Behavioral fever in ectothermic vertebrates

“…Myhre et al (1977) demonstrated an increase of final thermal preferendum in frog Rana esculenta, injected with blood plasma from frogs pre-injected with pathogenic bacteria M. ranae (Myhre et al, 1977). Also, lizards Dipsosaurus dorsalis developed behavioral fever after injection of supernatant collected from ex vivo incubated leukocytes isolated from peritoneal cavity of lizards pre-injected with dead A. hydrophila or 3% thioglycollatesaline solution, as well as from rabbits in which fever was previously induced (Bernheim and Kluger, 1977).…”

“…Up to date, behavioral fever has been described in all groups of ectothermic vertebrates including reptiles (Bernheim and Kluger, 1976a,b;Burns et al, 1996;do Amaral et al, 2002;Hallman et al, 1990;Kluger et al, 1975;Merchant et al, 2007Merchant et al, , 2008Monagas and Gatten, 1983;Muchlinski et al, 1995;Ortega et al, 1991;Ramos et al, 1993;Vaughn et al, 1974), amphibians (Casterlin and Reynolds, 1977;Kluger, 1977;Murphy et al, 2011;Myhre et al, 1977;Richards-Zawacki, 2010;Sherman et al, 1991), fish (Boltaña et al, 2013;Cabanac and Laberge, 1998;Covert and Reynolds, 1977;Grans et al, 2012;Reynolds, 1977;Reynolds et al, 1976Reynolds et al, , 1978 but also in invertebrates (Campbell et al, 2010;Elliot et al, 2002) and newborn mammals, which in response to bacterial pyrogens are unable to develop fever physiologically but do so behaviorally (Satinoff et al, 1976). However, there have been some contrasting data showing that injection of pyrogens, killed bacteria or parasites in some species of lizards (Don et al, 1994;Hallman et al, 1990;Laburn et al, 1981;Muchlinski et al, 1995;Ortega et al, 1991;Schall, 1990), turtles (Zurovsky et al, 1987b), snakes (Burns et al, 1996;Zurovsky et al, 1987a) and fish …”

“…1b) including LPS (Cabanac and Laberge, 1998;do Amaral et al, 2002;Grans et al, 2012;Merchant et al, 2007Merchant et al, , 2008Reynolds et al, 1978;Sherman et al, 1991), various species of Gram-positive and Gram-negative bacteria, administrated as killed or live forms (Bernheim and Kluger, 1976a,b;Burns et al, 1996;Casterlin and Reynolds, 1977;Covert and Reynolds, 1977;Hallman et al, 1990;Kluger, 1977;Kluger et al, 1975;Monagas and Gatten, 1983;Muchlinski et al, 1995;Myhre et al, 1977;Ortega et al, 1991;Ramos et al, 1993;Reynolds, 1977;Reynolds et al, 1976Reynolds et al, , 1978Vaughn et al, 1974), fungi (Murphy et al, 2011;Richards-Zawacki, 2010), ectoparasite (Gyrodactylus turnbulli) (Mohammed et al, 2016), synthetic dsRNA (poly I:C) (Boltaña et al, 2013) or viruses (Boltaña et al, 2013). Because of the relatively low sensitivity of fish and toads to LPS, the dose used to induce behavioral fever in these animals (toad:…”

“…The injections of heat-killed pathogenic Mycobacterium (M. xenopi and M. ranae) into frog (Rana esculenta) caused behavioral fever while non-pathogenic bacteria (M. aquae II) caused no change in temperature preferendum (Myhre et al, 1977).…”

“…Two experimental strategies have been applied to test the role of PG in the expression of behavioral fever in ectothermic vertebrates: (i) induction of behavioral fever by injection of PG or (ii) inhibition of behavioral fever expression by administration of PG synthesis inhibitors. Microinjection of PGE 1 into the third ventricle of the brain of the salamander Necturus maculosus (Hutchison and Erskine, 1981) or into the diencephalon of the frog Rana esculenta (Myhre et al, 1977) resulted in an increase of the final thermal preferendum. There is, however, one contrasting study showing no behavioral fever in fish Lepomis gibbosus after PGE 1 injection (Marx et al, 1984).…”