Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit
IntroductionAt 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...
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| Format: | Article |
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Frontiers Media S.A.
2023-10-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncel.2023.1263591/full |
| _version_ | 1797657252368220160 |
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| author | Wolfgang Stein Wolfgang Stein Gabriela Torres Luis Giménez Luis Giménez Noé Espinosa-Novo Jan Phillipp Geißel Jan Phillipp Geißel Andrés Vidal-Gadea Steffen Harzsch |
| author_facet | Wolfgang Stein Wolfgang Stein Gabriela Torres Luis Giménez Luis Giménez Noé Espinosa-Novo Jan Phillipp Geißel Jan Phillipp Geißel Andrés Vidal-Gadea Steffen Harzsch |
| author_sort | Wolfgang Stein |
| collection | DOAJ |
| description | IntroductionAt 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.MethodsWe address these questions using the pyloric pattern generating circuits in the stomatogastric nervous system of two crab species, Hemigrapsus sanguineus and Carcinus maenas that have seen a worldwide expansion in recent decades.Results and discussionConsistent with their history as invasive species, we find that pyloric activity showed a broad temperature robustness (>30°C). 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 H. sanguineus, but not in C. maenas. Comparing the temperature responses of C. maenas 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. |
| first_indexed | 2024-03-11T17:41:49Z |
| format | Article |
| id | doaj.art-55fcc60759774f69ad14f4f02830e20b |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-03-11T17:41:49Z |
| publishDate | 2023-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-55fcc60759774f69ad14f4f02830e20b2023-10-18T09:18:23ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022023-10-011710.3389/fncel.2023.12635911263591Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuitWolfgang Stein0Wolfgang Stein1Gabriela Torres2Luis Giménez3Luis Giménez4Noé Espinosa-Novo5Jan Phillipp Geißel6Jan Phillipp Geißel7Andrés Vidal-Gadea8Steffen Harzsch9School of Biological Sciences, Illinois State University, Normal, IL, United StatesStiftung Alfried Krupp Kolleg Greifswald, Greifswald, GermanyAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung, Biologische Anstalt Helgoland, Helgoland, GermanyAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung, Biologische Anstalt Helgoland, Helgoland, GermanySchool of Ocean Sciences, Bangor University, Bangor, United KingdomAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung, Biologische Anstalt Helgoland, Helgoland, GermanyAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung, Biologische Anstalt Helgoland, Helgoland, GermanyDepartment of Cytology and Evolutionary Biology, Zoological Institute and Museum, University of Greifswald, Greifswald, GermanySchool of Biological Sciences, Illinois State University, Normal, IL, United StatesDepartment of Cytology and Evolutionary Biology, Zoological Institute and Museum, University of Greifswald, Greifswald, GermanyIntroductionAt 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.MethodsWe address these questions using the pyloric pattern generating circuits in the stomatogastric nervous system of two crab species, Hemigrapsus sanguineus and Carcinus maenas that have seen a worldwide expansion in recent decades.Results and discussionConsistent with their history as invasive species, we find that pyloric activity showed a broad temperature robustness (>30°C). 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 H. sanguineus, but not in C. maenas. Comparing the temperature responses of C. maenas 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.https://www.frontiersin.org/articles/10.3389/fncel.2023.1263591/fullstomatogastric ganglioncentral pattern generationclimate changedegeneracyacclimatizationphase constancy |
| spellingShingle | Wolfgang Stein Wolfgang Stein Gabriela Torres Luis Giménez Luis Giménez Noé Espinosa-Novo Jan Phillipp Geißel Jan Phillipp Geißel Andrés Vidal-Gadea Steffen Harzsch Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit Frontiers in Cellular Neuroscience stomatogastric ganglion central pattern generation climate change degeneracy acclimatization phase constancy |
| title | Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit |
| title_full | Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit |
| title_fullStr | Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit |
| title_full_unstemmed | Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit |
| title_short | Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit |
| title_sort | thermal acclimation and habitat dependent differences in temperature robustness of a crustacean motor circuit |
| topic | stomatogastric ganglion central pattern generation climate change degeneracy acclimatization phase constancy |
| url | https://www.frontiersin.org/articles/10.3389/fncel.2023.1263591/full |
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