Behavioural fever in infected honeybees: parasitic manipulation or coincidental benefit?

Abstract

Infection by a parasite often induces behavioural changes in the host and these changes may benefit either the host or the parasite. However, whether these changes are active host defence mechanisms or parasitic manipulations or simply incidental byproducts of the infection is not always clear. It has been suggested that understanding the proximate mechanisms of these changes as well as comparative studies could help distinguish these alternatives better. Behavioural fever is a common response to an infection in many animals and we investigated the phenomenon in the novel host-parasite relationship between the honeybee and the temperature-sensitive microsporidian Nosema ceranae. Our results show that infected bees prefer higher temperatures and even though this seems to benefit the pathogen, the proximate mechanism underlying this change is the pathological stress underlying the infection. Especially because it is a new host-parasite relationship, it is best to label the observed behavioural change as a case of incidental benefit although this does not rule out selection acting on it. We discuss the importance of looking at the behavioural outcomes of host-parasite relationships and the importance of studying them at multiple levels for understanding their origin and maintenance.

Behavioral fever in ectothermic vertebrates

“…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 …”

Parasitized snails take the heat: a case of host manipulation?

“…Although less well documented, selection of cool temperatures upon infection can also retard parasite development (e.g., Moore and Freehling 2002). However, alterations in host behavior may simply be a side-eVect of the infection and beneWt neither the host nor parasite (Campbell et al 2010;Kavaliers and Colwell 1992;Lefcort and Bayne 1991;Holmes and Zohar 1990;Minchella 1985;Ewald 1980).…”

“…Identifying how temperature inXuences a parasite's development and subsequent outcome of the infection is critical to the appropriate interpretation of thermal biology data (Campbell et al 2010). The challenge is to link changes in the thermal behavior of infected hosts to Wtness beneWts for the host or parasite, a daunting task in Weld conditions.…”

Detection of Nosema spp. in worker bees, pollen and bee bread during the honey flow season

“…its demand for food, or suggested contamination of worker bees with pesticides (Nozal et al 2008;Alaux et al 2010). Energetic stress may depopulate a honey bee colony, and impaired immunity can lead to fully-symptomatic nosemosis or promote the onset of other diseases (Campbell et al 2010;Hedtke et al 2011;Botias et al 2013). It seems that pollen and probably water are more important epizootic sources of infection with Nosema spores, and the spread of the disease in a honey bee colony is promoted by trophallaxis and the hygiene-related behaviour of bees.…”