{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T05:31:30Z","timestamp":1792647090584,"version":"4.5.0"},"reference-count":72,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,10,18]],"date-time":"2023-10-18T00:00:00Z","timestamp":1697587200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Neurosci."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>At the cellular level, acute temperature changes alter ionic conductances, ion channel kinetics, and the activity of entire neuronal circuits. This can result in severe consequences for neural function, animal behavior and survival. In poikilothermic animals, and particularly in aquatic species whose core temperature equals the surrounding water temperature, neurons experience rather rapid and wide-ranging temperature fluctuations. Recent work on pattern generating neural circuits in the crustacean stomatogastric nervous system have demonstrated that neuronal circuits can exhibit an intrinsic robustness to temperature fluctuations. However, considering the increased warming of the oceans and recurring heatwaves due to climate change, the question arises whether this intrinsic robustness can acclimate to changing environmental conditions, and whether it differs between species and ocean habitats.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We address these questions using the pyloric pattern generating circuits in the stomatogastric nervous system of two crab species, <jats:italic>Hemigrapsus sanguineus<\/jats:italic> and <jats:italic>Carcinus maenas<\/jats:italic> that have seen a worldwide expansion in recent decades.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results and discussion<\/jats:title><jats:p>Consistent with their history as invasive species, we find that pyloric activity showed a broad temperature robustness (&amp;gt;30\u00b0C). Moreover, the temperature-robust range was dependent on habitat temperature in both species. Warm-acclimating animals shifted the critical temperature at which circuit activity breaks down to higher temperatures. This came at the cost of robustness against cold stimuli in <jats:italic>H. sanguineus<\/jats:italic>, but not in <jats:italic>C. maenas<\/jats:italic>. Comparing the temperature responses of <jats:italic>C. maenas<\/jats:italic> from a cold latitude (the North Sea) to those from a warm latitude (Spain) demonstrated that similar shifts in robustness occurred in natural environments. Our results thus demonstrate that neuronal temperature robustness correlates with, and responds to, environmental temperature conditions, potentially preparing animals for changing ecological conditions and shifting habitats.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fncel.2023.1263591","type":"journal-article","created":{"date-parts":[[2023,10,18]],"date-time":"2023-10-18T09:19:45Z","timestamp":1697620785000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":13,"title":["Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit"],"prefix":"10.3389","volume":"17","author":[{"given":"Wolfgang","family":"Stein","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriela","family":"Torres","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luis","family":"Gim\u00e9nez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"No\u00e9","family":"Espinosa-Novo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan Phillipp","family":"Gei\u00dfel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andr\u00e9s","family":"Vidal-Gadea","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steffen","family":"Harzsch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,10,18]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"e55470","DOI":"10.7554\/eLife.55470","article-title":"Temperature compensation in a small rhythmic circuit","volume":"9","author":"Alonso","year":"2020","journal-title":"Elife"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.5324\/fn.v39i0.2738","article-title":"Thermal behaviour of edible crab Cancer pagurus Linnaeus, 1758 in coastal Norway","volume":"39","author":"Bakke","year":"2019","journal-title":"Fauna Norv."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1154769","DOI":"10.3389\/fnins.2023.1154769","article-title":"Neural circuit regulation by identified modulatory projection neurons","volume":"17","author":"Blitz","year":"2023","journal-title":"Front. 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The life of the adult crab","volume":"2","author":"Crothers","year":"1968","journal-title":"Field Stud."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/S0306-4565(98)00008-4","article-title":"Thermal tolerance of two species of marine crab, Cancer pagurus and Carcinus maenas","volume":"23","author":"Cuculescu","year":"1998","journal-title":"J. Therm. Biol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"329","DOI":"10.3391\/ai.2011.6.3.09","article-title":"Hemigrapsus sanguineus (De Haan, 1835) (Crustacea: Brachyura: Grapsoidea) a new invasive species in European waters: the case of the French English Channel coast (2008-2010)","volume":"6","author":"Dauvin","year":"2011","journal-title":"Aquat. Invasions"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"103080","DOI":"10.1016\/j.pocean.2023.103080","article-title":"Investigation of marine temperature changes across temporal and spatial gradients: providing a fundament for studies on the effects of warming on marine ecosystem function and biodiversity","volume":"216","author":"De Amorim","year":"2023","journal-title":"Prog. Oceanogr."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"e1008057","DOI":"10.1371\/journal.pcbi.1008057","article-title":"Temperature-robust activity patterns arise from coordinated axonal sodium channel properties","volume":"16","author":"Demaegd","year":"2020","journal-title":"PLoS Comput. Biol."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"7607","DOI":"10.1523\/JNEUROSCI.0101-21.2021","article-title":"Neuropeptide modulation increases dendritic electrical spread to restore neuronal activity disrupted by temperature","volume":"41","author":"Demaegd","year":"2021","journal-title":"J. Neurosci."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.jembe.2013.01.010","article-title":"Invasion biology of the Asian shore crab Hemigrapsus sanguineus: a review","volume":"441","author":"Epifanio","year":"2013","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"3119","DOI":"10.1007\/s10530-023-03095-3","article-title":"On their way to the north: larval performance of Hemigrapsus sanguineus invasive to the European coast\u2014a comparison with the native European population of Carcinus maenas","volume":"25","author":"Espinosa-Novo","year":"2023","journal-title":"Biol. Invasions"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"121","DOI":"10.5134\/176156","article-title":"Comparative studies on the life history of the grapsid crabs (Crustacea, Brachyura) inhabiting intertidal cobble and boulder shores","volume":"33","author":"Fukui","year":"1988","journal-title":"Publ. Seto Mar. Biol. Lab."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1016\/j.ecss.2017.11.032","article-title":"Recruitment patterns, low cannibalism and reduced interspecific predation contribute to high invasion success of two Pacific crabs in northwestern Europe","volume":"200","author":"Geburzi","year":"2018","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"1142","DOI":"10.1038\/s42003-021-02585-1","article-title":"A state-space approach to understand responses of organisms, populations and communities to multiple environmental drivers","volume":"4","author":"Gim\u00e9nez","year":"2021","journal-title":"Commun. Biol."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"1423","DOI":"10.1111\/ecog.04725","article-title":"Exploring larval phenology as predictor for range expansion in an invasive species","volume":"43","author":"Gim\u00e9nez","year":"2020","journal-title":"Ecography"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1146\/annurev-neuro-092920-121538","article-title":"Ion Channel degeneracy, variability, and covariation in neuron and circuit resilience","volume":"44","author":"Goaillard","year":"2021","journal-title":"Annu. Rev. Neurosci."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"1424","DOI":"10.1038\/nn.2404","article-title":"Functional consequences of animal-to-animal variation in circuit parameters","volume":"12","author":"Goaillard","year":"2009","journal-title":"Nat. Neurosci."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1093\/biosci\/biu070","article-title":"Ionic current variability and functional stability in the nervous system","volume":"64","author":"Golowasch","year":"2014","journal-title":"Bioscience"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"R641","DOI":"10.1016\/j.cub.2019.05.029","article-title":"Neuronal homeostasis: voltage brings it all together","volume":"29","author":"Golowasch","year":"2019","journal-title":"Curr. Biol."},{"key":"ref9001","doi-asserted-by":"publisher","first-page":"e1207","DOI":"10.3791\/1207","article-title":"Cancer borealis stomatogastric nervous system dissection","volume":"25","author":"Gutierrez","year":"2009","journal-title":"J. Vis. Exp."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1080\/00222937700770221","article-title":"Aspects of the biology of the Jonah crab, Cancer borealis Stimpson, 1859 in the mid-Atlantic bight","volume":"11","author":"Haefner","year":"1977","journal-title":"J. Nat. Hist."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"336","DOI":"10.3389\/fnins.2019.00336","article-title":"The temperature dependence of sleep","volume":"13","author":"Harding","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1146\/annurev-physiol-021909-135900","article-title":"Living in the now: physiological mechanisms to tolerate a rapidly changing environment","volume":"72","author":"Hofmann","year":"2010","journal-title":"Annu. Rev. Physiol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1023\/A:1008822218061","article-title":"Phase maintenance in the pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion","volume":"4","author":"Hooper","year":"1997","journal-title":"J. Comput. Neurosci."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"20784","DOI":"10.1073\/pnas.1116795108","article-title":"Alternatively spliced domains interact to regulate BK potassium channel gating","volume":"108","author":"Johnson","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00227-018-3313-3","article-title":"Invasive versus native brachyuran crabs in a European rocky intertidal: respiratory performance and energy expenditures","volume":"165","author":"Jungblut","year":"2018","journal-title":"Mar. Biol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"8709","DOI":"10.1523\/JNEUROSCI.1274-07.2007","article-title":"Neuromodulators, not activity, control coordinated expression of ionic currents","volume":"27","author":"Khorkova","year":"2007","journal-title":"J. Neurosci."},{"key":"ref29","volume-title":"Biological synopsis of the Asian shore crab, Hemigrapsus sanguineus","author":"Klassen","year":"2012"},{"key":"ref30","volume-title":"A biological synopsis of the European green crab, Carcinus maenas","author":"Klassen","year":"2007"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.jembe.2014.02.013","article-title":"Temperature preference and acclimation in the Jonah crab, Cancer borealis","volume":"455","author":"Lewis","year":"2014","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1007\/s12035-014-8674-0","article-title":"Regulation of membrane excitability: a convergence on voltage-gated sodium conductance","volume":"51","author":"Lin","year":"2015","journal-title":"Mol. Neurobiol."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"eaat3272","DOI":"10.1126\/sciadv.aat3272","article-title":"Projected changes in persistent extreme summer weather events: the role of quasi-resonant amplification","volume":"4","author":"Mann","year":"2018","journal-title":"Sci. Adv."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1146\/annurev.physiol.69.031905.161516","article-title":"Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs","volume":"69","author":"Marder","year":"2007","journal-title":"Annu. Rev. Physiol."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"10213","DOI":"10.1523\/JNEUROSCI.1261-21.2021","article-title":"From the neuroscience of individual variability to climate change","volume":"41","author":"Marder","year":"2021","journal-title":"J. Neurosci."},{"key":"ref36","first-page":"161","article-title":"The structure of the stomatogastric neuromuscular system in Callinectes sapidus, Homarus americanus and Panulirus argus (Decapoda Crustacea)","volume":"268","author":"Maynard","year":"1974","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1007\/s00360-012-0730-3","article-title":"A review of gastric processing in decapod crustaceans","volume":"183","author":"Mcgaw","year":"2013","journal-title":"J. Comp. Physiol. B"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1016\/j.jtherbio.2012.07.003","article-title":"Effects of acclimation and acute temperature change on specific dynamic action and gastric processing in the green shore crab, Carcinus maenas","volume":"37","author":"Mcgaw","year":"2012","journal-title":"J. Therm. Biol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1007\/s00285-007-0150-2","article-title":"Maintaining phase of the crustacean tri-phasic pyloric rhythm","volume":"57","author":"Mouser","year":"2008","journal-title":"J. Math. Biol."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"26980","DOI":"10.1073\/pnas.1911413116","article-title":"Molecular profiling of single neurons of known identity in two ganglia from the crab Cancer borealis","volume":"116","author":"Northcutt","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1038\/417343a","article-title":"A small-systems approach to motor pattern generation","volume":"417","author":"Nusbaum","year":"2002","journal-title":"Nature"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"2935","DOI":"10.1016\/j.cub.2016.08.061","article-title":"Temperature-robust neural function from activity-dependent Ion Channel regulation","volume":"26","author":"O\u2019leary","year":"2016","journal-title":"Curr. Biol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"E2645","DOI":"10.1073\/pnas.1309966110","article-title":"Correlations in ion channel expression emerge from homeostatic tuning rules","volume":"110","author":"O\u2019leary","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"1324","DOI":"10.1038\/s41467-018-03732-9","article-title":"Longer and more frequent marine heatwaves over the past century","volume":"9","author":"Oliver","year":"2018","journal-title":"Nat. Commun."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"e60454","DOI":"10.7554\/eLife.60454","article-title":"Coupling between fast and slow oscillator circuits in Cancer borealis is temperature-compensated","volume":"10","author":"Powell","year":"2021","journal-title":"Elife"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"9950","DOI":"10.1523\/JNEUROSCI.1095-13.2013","article-title":"Neurons within the same network independently achieve conserved output by differentially balancing variable conductance magnitudes","volume":"33","author":"Ransdell","year":"2013","journal-title":"J. Neurosci."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"1454","DOI":"10.1016\/j.bpj.2021.01.038","article-title":"Neuronal oscillator robustness to multiple global perturbations","volume":"120","author":"Ratliff","year":"2021","journal-title":"Biophys. J."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0065-2881(09)56001-4","article-title":"Chapter 1. Impacts of the oceans on climate change","volume":"56","author":"Reid","year":"2009","journal-title":"Adv. Mar. Biol."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"101055","DOI":"10.1016\/j.cois.2023.101055","article-title":"A cold and quiet brain: mechanisms of insect CNS arrest at low temperatures","volume":"58","author":"Robertson","year":"2023","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"724","DOI":"10.1016\/j.conb.2012.01.008","article-title":"Temperature and neuronal circuit function: compensation, tuning and tolerance","volume":"22","author":"Robertson","year":"2012","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1038\/nn1639","article-title":"Variable channel expression in identified single and electrically coupled neurons in different animals","volume":"9","author":"Schulz","year":"2006","journal-title":"Nat. Neurosci."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"13187","DOI":"10.1073\/pnas.0705827104","article-title":"Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression","volume":"104","author":"Schulz","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.conb.2016.09.015","article-title":"Homeostatic plasticity of excitability in crustacean central pattern generator networks","volume":"43","author":"Schulz","year":"2017","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1007\/BF00366739","article-title":"Kinetics of osmoregulation in the crab Carcinus maenas","volume":"17","author":"Siebers","year":"1972","journal-title":"Mar. Biol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"912","DOI":"10.1242\/jeb.037473","article-title":"The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine 'winners' and 'losers'","volume":"213","author":"Somero","year":"2010","journal-title":"J. Exp. Biol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1146\/annurev-marine-120710-100935","article-title":"The physiology of global change: linking patterns to mechanisms","volume":"4","author":"Somero","year":"2012","journal-title":"Annu. Rev. Mar. Sci."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"2603","DOI":"10.1152\/jn.00906.2013","article-title":"Phase maintenance in a rhythmic motor pattern during temperature changes in vivo","volume":"111","author":"Soofi","year":"2014","journal-title":"J. Neurophysiol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"e1002265","DOI":"10.1371\/journal.pbio.1002265","article-title":"Neuromodulation to the rescue: compensation of temperature-induced breakdown of rhythmic motor patterns via extrinsic neuromodulatory input","volume":"13","author":"St\u00e4dele","year":"2015","journal-title":"PLoS Biol."},{"key":"ref9002","doi-asserted-by":"publisher","first-page":"e2151","DOI":"10.21769\/BioProtoc.2151","article-title":"Extracellular axon stimulation","volume":"7","author":"St\u00e4dele","year":"2017","journal-title":"Bio-protocol"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"849160","DOI":"10.3389\/fncel.2022.849160","article-title":"Neuromodulation enables temperature robustness and coupling between fast and slow oscillator circuits","volume":"16","author":"Stadele","year":"2022","journal-title":"Front. Cell. Neurosci."},{"key":"ref60","first-page":"473","article-title":"Distribution and abundance of four brachyuran crabs on the Northwest Atlantic shelf","volume":"89","author":"Stehlik","year":"1991","journal-title":"Fish. Bull."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"989","DOI":"10.1007\/s00359-009-0483-y","article-title":"Modulation of stomatogastric rhythms","volume":"195","author":"Stein","year":"2009","journal-title":"J. Comp. Physiol. A"},{"key":"ref62","doi-asserted-by":"crossref","DOI":"10.1093\/acrefore\/9780190264086.013.153","article-title":"Stomatogastric nervous system","volume-title":"Oxford Research Encyclopedia of Neuroscience","author":"Stein","year":"2017"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"125887","DOI":"10.1016\/j.zool.2020.125887","article-title":"The neurobiology of ocean change - insights from decapod crustaceans","volume":"144","author":"Stein","year":"2021","journal-title":"Zoology"},{"key":"ref64","article-title":"Evolutionary aspects of motor control and coordination: the central pattern generators in the crustacean stomatogastric and swimmeret systems","volume-title":"Structure and evolution of invertebrate nervous systems","author":"Stein","year":"2016"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.jembe.2009.04.020","article-title":"Possible temperature limits to range expansion of non-native Asian shore crabs in Maine","volume":"375","author":"Stephenson","year":"2009","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"e1000469","DOI":"10.1371\/journal.pbio.1000469","article-title":"Precise temperature compensation of phase in a rhythmic motor pattern","volume":"8","author":"Tang","year":"2010","journal-title":"PLoS Biol."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"10075","DOI":"10.1523\/JNEUROSCI.1443-12.2012","article-title":"Robustness of a rhythmic circuit to short- and long-term temperature changes","volume":"32","author":"Tang","year":"2012","journal-title":"J. Neurosci."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"718","DOI":"10.1152\/jn.00622.2011","article-title":"Neuromodulation independently determines correlated channel expression and conductance levels in motor neurons of the stomatogastric ganglion","volume":"107","author":"Temporal","year":"2012","journal-title":"J. Neurophysiol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"1129","DOI":"10.1242\/jeb.093849","article-title":"Master of all trades: thermal acclimation and adaptation of cardiac function in a broadly distributed marine invasive species, the European green crab, Carcinus maenas","volume":"217","author":"Tepolt","year":"2014","journal-title":"J. Exp. Biol."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"e67930","DOI":"10.1371\/journal.pone.0067930","article-title":"Temperature sensitivity of the pyloric neuromuscular system and its modulation by dopamine","volume":"8","author":"Thuma","year":"2013","journal-title":"PLoS One"}],"container-title":["Frontiers in Cellular Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncel.2023.1263591\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,18]],"date-time":"2023-10-18T09:19:54Z","timestamp":1697620794000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncel.2023.1263591\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,18]]},"references-count":72,"alternative-id":["10.3389\/fncel.2023.1263591"],"URL":"https:\/\/doi.org\/10.3389\/fncel.2023.1263591","relation":{},"ISSN":["1662-5102"],"issn-type":[{"value":"1662-5102","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,18]]},"article-number":"1263591"}}