Getting into hot water sick guppies frequent warm

Authors: Ryan S Mohammed Michael Reynolds Joanna James Chris Williams Azad Mohammed Adesh Ramsubhag Cock van Oosterhout Jo Cable

Publish Date: 2016/03/10

Volume: 181, Issue: 3, Pages: 911-917

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Abstract

Ectotherms depend on the environmental temperature for thermoregulation and exploit thermal regimes that optimise physiological functioning They may also frequent warmer conditions to upregulate their immune response against parasite infection and/or impede parasite development This adaptive response known as ‘behavioural fever’ has been documented in various taxa including insects reptiles and fish but only in response to endoparasite infections Here a choice chamber experiment was used to investigate the thermal preferences of a tropical freshwater fish the Trinidadian guppy Poecilia reticulata when infected with a common helminth ectoparasite Gyrodactylus turnbulli in femaleonly and mixedsex shoals The temperature tolerance of G turnbulli was also investigated by monitoring parasite population trajectories on guppies maintained at a continuous 18 24 or 32 °C Regardless of shoal composition infected fish frequented the 32 °C choice chamber more often than when uninfected significantly increasing their mean temperature preference Parasites maintained continuously at 32 °C decreased to extinction within 3 days whereas mean parasite abundance increased on hosts incubated at 18 and 24 °C We show for the first time that gyrodactylidinfected fish have a preference for warmer waters and speculate that sick fish exploit the upper thermal tolerances of their parasites to self medicateTemperature is perhaps the most important environmental determinant of the activity and performance of ectothermic vertebrates and is particularly critical for fishes that unlike amphibians and reptiles are inefficient thermoregulators Atkinson 1994 Fish behaviourally regulate their body temperature by selecting habitats with thermal regimes that optimise physiological performance Reynolds et al 1976 Ward et al 2010 The metabolism feeding rate and activity levels of ectotherms generally increase with temperature until conditions become stressful Thermal stress can have longlasting effects on fish behaviour with respect to migration Jonsson and Jonsson 2009 reproductive success Pankhurst and Munday 2011 predatory avoidance Marine and Cech 2004 and shoaling Weetman et al 1998 1999 For temperate fish this results in marked seasonal and diel behaviours but even tropical species are subjected to distinct temperature heterogeneities Webb et al 2008In addition to optimizing physiological performance ectotherms exploit thermal regimes to hinder parasite transmission and development A change in a host’s thermal preference driven by pathogenic infection otherwise known as ‘behavioural fever’ has been documented in several taxa including bumblebees Müller and SchmidHempel 1993 locusts Elliot et al 2002 lizards Vaughn et al 1974 and fish The first evidence of behavioural fever in fish was observed in largemouth bass Micropterus salmoides and bluegill sunfish Lepomis macrochirus both species displayed a significant increase +27 °C in mean temperature preference when inoculated with bacteria Reynolds et al 1976 This response was associated with bacterial pyrogens feverinducing chemicals acting directly on the host’s hypothalamic thermoregulatory centre Reynolds et al 1976 A subsequent study speculated that an increase in thermal preference by the fish host upregulates the immune response against parasite infection Covert and Reynolds 1977 Using zebrafish Danio rerio infected with viraemia of carp virus it was confirmed that host behavioural fever induces a major upregulation of the innate immune response in this case expression of antiviral genes which subsequently cleared viral infections within infected fish Boltaña et al 2013Acute thermal changes can be detrimental to the immune functions of fish reviewed in Martin et al 2010 However some immune responses including elevations in lysozyme and immunoglobulin M levels are positively correlated with temperature until thermal limits are exceeded Bowden et al 2007 MarcosLopez et al 2010 Thermal stress can reduce host immunocompetence thereby increasing disease susceptibility in ectotherms Rohr and Raffel 2010 Interactions between these factors ultimately determine whether infections lead to severe pathology and even mortality or host recovery Parasites also respond directly to thermal variation as elevated temperatures typically reduce development time For example Schistocephalus solidus pleroceroid larvae infecting threespined sticklebacks have faster growth rates and become infectious to their definitive host sooner at 20 °C compared to 15 °C Macnab and Barber 2011For directly transmitted ectoparasites including monogenean gyrodactylids the rate of reproduction is positively correlated within a temperature range from 17 to 28 °C in tropical gyrodactylids and 25–195 °C in temperate species Scott and Nokes 1984 Jansen and Bakke 1991 Gyrodactylids are ubiquitous on teleosts feeding on the skin and fin tissues of a host Kearn 1996 Harris et al 2004 Their life history traits transmission and population dynamics have been extensively studied using the Trinidadian guppyGyrodactylus system reviewed by Cable 2011 Gyrodactylus turnbulli a common guppy ectoparasite exhibits a viviparous reproductive strategy Cable and Harris 2002 often resulting in explosive population growth which can significantly impede host survival eg Cable and van Oosterhout 2007a As gyrodactylid embryonic development is temperature dependent reviewed by Bakke et al 2007 natural variations in water temperature can determine parasite population growthWhilst guppies exhibit broad temperature tolerance Reeve et al 2014 small changes in water temperature can dramatically modify gyrodactylid life history traits Bakke et al 2007 and temperatures exceeding 30 °C impede G turnbulli survival Scott and Nokes 1984 The present study investigates the thermal preferences of guppies in femaleonly and mixedsex shoals when uninfected and infected with the ectoparasite G turnbulli We also examine the temperature tolerance of these parasites by monitoring population trajectories on fish maintained at constant temperatures of 18 24 or 32 °C We hypothesize that guppies infected with G turnbulli will frequent warmer water in comparison to when they are uninfected and exposure to extreme thermal conditions has benefits in terms of selfmedication against parasites

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