Ranavirus infection does not reduce heat tolerance in a larval amphibian

Journal of Thermal Biology - Tập 114 - Trang 103584 - 2023
Jason W. Dallas1, Robin W. Warne1
1School of Biological Sciences, Southern Illinois University Carbondale, 1125 Lincoln Street, Carbondale, IL, 62901, USA

Tài liệu tham khảo

Agudelo-Cantero, 2019, Interactive effects of experimental heating rates, ontogeny and body mass on the upper thermal limits of anuran larvae, J. Therm. Biol., 82, 43, 10.1016/j.jtherbio.2019.03.010 Arietta, 2021 Baker, 2018, Characterization of serum complement immune activity in the prairie rattlesnake (Crotalus viridis), J. Basic Appl. Zool., 79, 36, 10.1186/s41936-018-0050-6 Blehert, 2009, Bat white-nose syndrome: an emerging fungal pathogen?, Science, 323, 227, 10.1126/science.1163874 Bowler, 2018, Heat death in poikilotherms: is there a common cause?, J. Therm. Biol., 76, 77, 10.1016/j.jtherbio.2018.06.007 Brand, 2016, Water temperature affects susceptibility to ranavirus, EcoHealth, 13, 350, 10.1007/s10393-016-1120-1 Brattstrom, 1968, Thermal acclimation in anuran amphibians as a function of latitude and altitude, Comp. Biochem. Physiol., 24, 93, 10.1016/0010-406X(68)90961-4 Brattstrom, 1962, The rate of thermal acclimation in anuran amphibians, Physiol. Zool., 35, 148, 10.1086/physzool.35.2.30152723 Brunner, 2019, Ranavirus infection dynamics and shedding in American bullfrogs: consequences for spread and detection in trade, Dis. Aquat. Org., 135, 135, 10.3354/dao03387 Burraco, 2016, Physiological stress responses in Amphibian larvae to multiple stressors reveal marked anthropogenic effects even below lethal levels, Physiol. Biochem. Zool., 89, 462, 10.1086/688737 Camini, 2017, Implications of oxidative stress on viral pathogenesis, Arch. Virol., 162, 907, 10.1007/s00705-016-3187-y Chatterjee, 2016, 35 Christen, 2018, Thermal tolerance and thermal sensitivity of heart mitochondria: mitochondrial integrity and ROS production, Free Radic. Biol. Med., 116, 11, 10.1016/j.freeradbiomed.2017.12.037 Chung, 2020, Mitochondria and the thermal limits of ectotherms, J. Exp. Biol., 223, 10.1242/jeb.227801 Cupp, 1980, Thermal tolerance of five salientian amphibians during development and metamorphosis, Herpetologica, 234 Dahlke, 2020, Thermal bottlenecks in the life cycle define climate vulnerability of fish, Science, 369, 65, 10.1126/science.aaz3658 Dallas, 2023, Heat hardening of a larval amphibian is dependent on acclimation period and temperature, J. Exp. Zool. Part A: Ecological and Integrative Physiology, 339, 339, 10.1002/jez.2689 Dallas, 2021, Eurythermic sprint and immune thermal performance and ecology of an exotic lizard at its northern invasion front, Physiol. Biochem. Zool., 94, 12, 10.1086/712059 de Groot, 2015, Is membrane homeostasis the missing link between inflammation and neurodegenerative diseases?, Cell. Mol. Life Sci., 72, 4795, 10.1007/s00018-015-2038-4 De Jesus Andino, 2012, Susceptibility of Xenopus laevis tadpoles to infection by the ranavirus Frog-Virus 3 correlates with a reduced and delayed innate immune response in comparison with adult frogs, Virology, 432, 435, 10.1016/j.virol.2012.07.001 Deutsch, 2008, Impacts of climate warming on terrestrial ectotherms across latitude, Proc. Natl. Acad. Sci. USA, 105, 6668, 10.1073/pnas.0709472105 Dittmar, 2014, Heat and immunity: an experimental heat wave alters immune functions in three-spined sticklebacks (Gasterosteus aculeatus), J. Anim. Ecol., 83, 744, 10.1111/1365-2656.12175 Duarte, 2012, Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities, Global Change Biol., 18, 412, 10.1111/j.1365-2486.2011.02518.x Fernandez-Loras, 2019, Infection with Batrachochytrium dendrobatidis lowers heat tolerance of tadpole hosts and cannot be cleared by brief exposure to CTmax, PLoS One, 14, 10.1371/journal.pone.0216090 Fisher, 2020, Chytrid fungi and global amphibian declines, Nat. Rev. Microbiol., 18, 332, 10.1038/s41579-020-0335-x Floyd, 1983, Ontogenetic change in the temperature tolerance of larval Bufo marinus (Anura: bufonidae), Comp. Biochem. Physiol. Physiol., 75, 267, 10.1016/0300-9629(83)90081-6 Fontaine, 2022, Experimental depletion of gut microbiota diversity reduces host thermal tolerance and fitness under heat stress in a vertebrate ectotherm, Nat. Ecol. Evol., 6, 405, 10.1038/s41559-022-01686-2 Forzan, 2017, Pathogenesis of frog virus 3 (ranavirus, iridoviridae) infection in wood frogs (Rana sylvatica), Vet. Pathol., 54, 531, 10.1177/0300985816684929 Gantress, 2003, Development and characterization of a model system to study amphibian immune responses to iridoviruses, Virology, 311, 254, 10.1016/S0042-6822(03)00151-X Gosner, 1960, A simplified table for staging Anuran embryos and larvae with notes on identification, Herpetologica, 16, 183 Graham, 2017, Thermal performance and acclimatization of a component of snake (Agkistrodon piscivorus) innate immunity, J. Exp. Zool. A Ecol. Integr. Physiol., 327, 351, 10.1002/jez.2083 Greenspan, 2017, Infection increases vulnerability to climate change via effects on host thermal tolerance, Sci. Rep., 7, 9349, 10.1038/s41598-017-09950-3 Gunderson, 2015, Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming, Proc. Biol. Sci., 282 Hall, 2020, Salinity stress increases the severity of ranavirus epidemics in amphibian populations, Proc. Biol. Sci., 287 Hector, 2023, Infection burdens and virulence under heat stress: ecological and evolutionary considerations, Philos. Trans. R. Soc. Lond. B Biol. Sci., 378, 10.1098/rstb.2022.0018 Hector, 2019, Pathogen exposure disrupts an organism's ability to cope with thermal stress, Global Change Biol., 25, 3893, 10.1111/gcb.14713 Hector, 2020, The influence of immune activation on thermal tolerance along a latitudinal cline, J. Evol. Biol., 33, 1224, 10.1111/jeb.13663 Hector, 2021, Thermal limits in the face of infectious disease: how important are pathogens?, Global Change Biol., 27, 4469, 10.1111/gcb.15761 Hoverman, 2011, Phylogeny, life history, and ecology contribute to differences in Amphibian susceptibility to ranaviruses, EcoHealth, 8, 301, 10.1007/s10393-011-0717-7 Hoyt, 2021, Ecology and impacts of white-nose syndrome on bats, Nat. Rev. Microbiol., 19, 196, 10.1038/s41579-020-00493-5 Huey, 2009, Why tropical forest lizards are vulnerable to climate warming, Proc. Biol. Sci., 276, 1939 Huey, 2012, Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation, Philos. Trans. R. Soc. Lond. B Biol. Sci., 367, 1665, 10.1098/rstb.2012.0005 2021 Jørgensen, 2022, Extreme escalation of heat failure rates in ectotherms with global warming, Nature, 611, 93, 10.1038/s41586-022-05334-4 Kassahn, 2009, Animal performance and stress: responses and tolerance limits at different levels of biological organisation, Biol. Rev. Camb. Phil. Soc., 84, 277, 10.1111/j.1469-185X.2008.00073.x Katzenberger, 2021, Variation in upper thermal tolerance among 19 species from temperate wetlands, J. Therm. Biol., 96, 10.1016/j.jtherbio.2021.102856 Katzenberger, 2018, Source of environmental data and warming tolerance estimation in six species of North American larval anurans, J. Therm. Biol., 76, 171, 10.1016/j.jtherbio.2018.07.005 Kirschman, 2017, Exogenous stress hormones alter energetic and nutrient costs of development and metamorphosis, J. Exp. Biol., 220, 3391 Kregel, 2002, Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance, J. Appl. Physiol., 92, 2177, 10.1152/japplphysiol.01267.2001 Kuznetsova, 2017, lmerTest package: tests in linear mixed effects models, J. Stat. Software, 82, 1, 10.18637/jss.v082.i13 Laidlaw, 2020, Pathogen exposure reduces sexual dimorphism in a host's upper thermal limits, Ecol. Evol., 10, 12851, 10.1002/ece3.6828 Liu, 2018, Effects of both cold and heat stress on the liver of the giant spiny frog (Quasipaa spinosa): stress response and histological changes, J. Exp. Biol., 221 Lorch, 2016, Snake fungal disease: an emerging threat to wild snakes, Philos. Trans. R. Soc. Lond. B Biol. Sci., 371, 10.1098/rstb.2015.0457 Madeira, 2013, Influence of temperature in thermal and oxidative stress responses in estuarine fish, Comp. Biochem. Physiol. Mol. Integr. Physiol., 166, 237, 10.1016/j.cbpa.2013.06.008 Miller, 2018, Quantifying climate sensitivity and climate-driven change in North American amphibian communities, Nat. Commun., 9, 3926, 10.1038/s41467-018-06157-6 Miller, 2015, Comparative pathology of ranaviruses and diagnostic techniques, 171 Morales, 2010, Innate immune responses and permissiveness to ranavirus infection of peritoneal leukocytes in the frog Xenopus laevis, J. Virol., 84, 4912, 10.1128/JVI.02486-09 Moretti, 2019, Thermal sensitivity of innate immune response in three species of Rhinella toads, Comp. Biochem. Physiol. Mol. Integr. Physiol., 237, 10.1016/j.cbpa.2019.110542 Munoz, 2022, The Bogert effect, a factor in evolution, Evolution, 76, 49, 10.1111/evo.14388 Neely, 2020, Synergistic effects of warming and disease linked to high mortality in cool-adapted terrestrial frogs, Biol. Conserv., 245, 10.1016/j.biocon.2020.108521 Ørsted, 2022, Finding the right thermal limit: a framework to reconcile ecological, physiological and methodological aspects of CTmax in ectotherms, J. Exp. Biol., 225, 10.1242/jeb.244514 Pockley, 2018, Extracellular cell stress (heat shock) proteins-immune responses and disease: an overview, Philos. Trans. R. Soc. Lond. B Biol. Sci., 373, 10.1098/rstb.2016.0522 Porras, 2021, Fungal infections lead to shifts in thermal tolerance and voluntary exposure to extreme temperatures in both prey and predator insects, Sci. Rep., 11, 10.1038/s41598-021-00248-z Pörtner, 2017, Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology, J. Exp. Biol., 220, 2685, 10.1242/jeb.134585 Rollins-Smith, 2020, Global Amphibian declines, disease, and the ongoing battle between Batrachochytrium fungi and the immune system, Herpetologica, 76, 10.1655/0018-0831-76.2.178 Ruthsatz, 2022, Thermal tolerance and acclimation capacity in the European common frog (Rana temporaria) change throughout ontogeny, J. Exp. Zool. A Ecol. Integr., 337, 477, 10.1002/jez.2582 Sauer, 2019, Behavioural fever reduces ranaviral infection in toads, Funct. Ecol., 33, 2172, 10.1111/1365-2435.13427 Schmidt-Nielsen, 1997 Sears, 2011, The economy of inflammation: when is less more?, Trends Parasitol., 27, 382, 10.1016/j.pt.2011.05.004 Seneviratne, 2021, Weather and climate extreme events in a changing climate Seppala, 2011, Immune defence under extreme ambient temperature, Biol. Lett., 7, 119, 10.1098/rsbl.2010.0459 Sherman, 2008, Thermal biology of newts (Notophthalmus viridescens) chronically infected with a naturally occurring pathogen, J. Therm. Biol., 33, 27, 10.1016/j.jtherbio.2007.09.005 Sherman, 1991, Fever and thermal tolerance in the toad Bufo marinus, J. Therm. Biol., 16, 297, 10.1016/0306-4565(91)90021-S Sherman, 2003, Heat hardening as a function of developmental stage in larval and juvenile Bufo americanus and Xenopus laevis, J. Therm. Biol., 28, 373, 10.1016/S0306-4565(03)00014-7 Siddons, 2021, Exposure to a fungal pathogen increases the critical thermal minimum of two frog species, Ecol. Evol., 11, 9589, 10.1002/ece3.7779 Sokolova, 2023, Ectotherm mitochondrial economy and responses to global warming, Acta Physiol., 237, 10.1111/apha.13950 Somero, 2010, The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine 'winners' and 'losers', J. Exp. Biol., 213, 912, 10.1242/jeb.037473 Sørensen, 2009, Complex patterns of geographic variation in heat tolerance and Hsp70 expression levels in the common frog Rana temporaria, J. Therm. Biol., 34, 49, 10.1016/j.jtherbio.2008.10.004 Stahlschmidt, 2017, A simulated heat wave has diverse effects on immune function and oxidative physiology in the corn snake (Pantherophis guttatus), Physiol. Biochem. Zool., 90, 434, 10.1086/691315 Stilwell, 2018, Partial validation of a TaqMan real-time quantitative PCR for the detection of ranaviruses, Dis. Aquat. Org., 128, 105, 10.3354/dao03214 Sunday, 2014, Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation, Proc. Natl. Acad. Sci. U. S. A., 111, 5610, 10.1073/pnas.1316145111 Team, 2021 Turriago, 2015, Upper thermal tolerance in anuran embryos and tadpoles at constant and variable peak temperatures, Can. J. Zool., 93, 267, 10.1139/cjz-2014-0254 Turriago, 2022, The effect of thermal microenvironment in upper thermal tolerance plasticity in tropical tadpoles. Implications for vulnerability to climate warming, J. Exp. Zool. A Ecol. Integr. Physiol., 337, 746, 10.1002/jez.2632 Voyles, 2009, Pathogenesis of chytridiomycosis, a cause of catastrophic Amphibian declines, Science, 326, 582, 10.1126/science.1176765 Wallin, 2002, Heat-shock proteins as activators of the innate immune system, Trends Immunol., 23, 130, 10.1016/S1471-4906(01)02168-8 Warne, 2011, Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles, Funct. Ecol., 25, 139, 10.1111/j.1365-2435.2010.01793.x Woodburn, 2021, Shell lesions associated with emydomyces testavorans infection in freshwater aquatic turtles, Vet. Pathol., 58, 578, 10.1177/0300985820985217 Zhou, 2020, A pneumonia outbreak associated with a new coronavirus of probable bat origin, Nature, 579, 270, 10.1038/s41586-020-2012-7