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Marine Biology

, 166:138 | Cite as

Crawling and righting behavior of the subtropical sea star Echinaster (Othilia) graminicola: effects of elevated temperature

  • Lila M. Ardor Bellucci
  • Nancy F. SmithEmail author
Original Paper

Abstract

Sea stars exhibit discrete neuromuscular-mediated behaviors, such as crawling and righting, which are critical to daily functioning and survival. As global seawater temperatures rise, subtidal asteroids such as Echinaster (Othilia) graminicola on the Gulf Coast of Florida are increasingly subjected to elevated temperatures, which may compromise their neuromuscular health. To better understand the neuromuscular biology of E. graminicola and the effects of elevated seawater temperature on behavior, we first describe their righting mechanism and identify the arms used in righting and crawling. Together, this allowed us to determine if they exhibit any bilateral tendencies, related to their anterior–posterior ancestry, by measuring the frequency with which each arm led in righting and crawling. To determine the effect of elevated seawater temperature on their described righting behavior, we tested the effects of acute (1 day) and chronic (7 day) exposure to seawater temperatures ranging from 28 to 36 °C on righting time in a laboratory experiment. We found that E. graminicola rights by somersaulting, but exhibits no lead arm preference during this behavior. In crawling, Arm E, located adjacent to the madreporite, led most frequently, indicating a partial tendency toward bilateralism. Sea stars righted significantly faster with increasing temperature and exposure time as temperatures increased from 28 to 34 °C, suggesting some capacity for acclimatization to elevated temperatures. However, at 36 °C, righting time increased dramatically and sea stars experienced high mortality, suggesting E. graminicola may be living near the upper limits of its thermotolerance. As seawater temperatures rise beyond an organism’s thermal tolerance, their neuromuscular responses may become critically impaired, reducing their capacity to survive in a warming ocean.

Notes

Acknowledgements

We thank William Szelistowski and Cory Krediet for their helpful suggestions toward improving this manuscript, John Ferguson for sharing his expertise on local Echinaster populations, and David Bennett for his assistance with the temperature experiments. We thank the anonymous reviewers for their constructive comments which helped improve this manuscript. This research was supported by the Ford Apprentice Scholars Program at Eckerd College.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The collection and handling of sea stars were followed by the regulations and policies outlined in Special Activity License SAL-14-0780-SR, issued by the Florida Wildlife Conservation Commission, Tallahassee, Florida, USA.

References

  1. Bennett AF (1990) Thermal dependence of locomotor capacity. Am J Physiol 259:R253–R258PubMedGoogle Scholar
  2. Brothers CJ, McClintock JB (2015) The effects of climate-induced elevated seawater temperature on the covering behavior, righting response, and Aristotle’s lantern reflex of the sea urchin Lytechinus variegatus. J Exp Mar Biol Ecol 467:33–38.  https://doi.org/10.1016/j.jembe.2015.02.019 CrossRefGoogle Scholar
  3. Buccheri E, Foellmer MW, Christensen BA, Langis P, Ritter S, Wolf E, Freeman AS (2019) Variation in righting times of Holothuria atra, Stichopus chloronotus, and Holothuria edulis in response to increased seawater temperatures on Heron Reef in the southern GBR. J Mar Biol 2019:1–6.  https://doi.org/10.1155/2019/6179705 CrossRefGoogle Scholar
  4. Campbell DB, Turner RL (1984) Echinaster graminicola, a new species of spinulosid sea star (Echinodermata: Asteroidea) from the west coast of Florida, USA. Proc Biol Soc Wash 97:167–178.  https://doi.org/10.1242/jeb.136101 CrossRefGoogle Scholar
  5. Carey N, Harianto J, Byrne M (2016) Sea urchins in a high-CO2 world: partitioned effects of body size, ocean warming and acidification on metabolic rate. J Exp Biol 219:1178–1186.  https://doi.org/10.1242/jeb.136101 CrossRefPubMedGoogle Scholar
  6. Clark AM, Downey ME (1992) Starfishes of the Atlantic. Chapman & Hall, LondonGoogle Scholar
  7. Cobb JLS (1995) The nervous systems of Echinodermata: recent results and new approaches. In: Breidbach O, Kutsch W (eds) The nervous systems of invertebrates: an evolutionary and comparative approach. Birkhäuser Basel, Basel, pp 407–424CrossRefGoogle Scholar
  8. Cole LJ (1913) Direction of locomotion of the starfish (Asterias forbesi). J Exp Zool 14:1–32CrossRefGoogle Scholar
  9. Domenici P, Gonzales-Calderon D, Ferrari RS (2003) Locomotor performance in the sea urchin Paracentrotus lividus. J Mar Biol Assoc UK 83:285–292.  https://doi.org/10.1017/S0025315403007094h CrossRefGoogle Scholar
  10. Hamilton WF (1922) Coordination in the starfish. J Comp Psychol 2:61–94CrossRefGoogle Scholar
  11. Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241.  https://doi.org/10.1111/j.1461-0248.2005.00871.x CrossRefGoogle Scholar
  12. Hotchkiss FHC (2011) Table of ray identification schemes for nonluidiid Asteroidea. Marine and Paleobiological Research Institute. http://mprinstitute.org/PDF/Notulae_MPRI_1001_rev01.pdf. Accessed 15 April 2019
  13. Hurlbert AH, Ballantyne F, Powell S (2008) Shaking a leg and hot to trot: the effects of body size and temperature on running speed in ants. Ecol Entomol 33:144–154.  https://doi.org/10.1111/j.1365-2311.2007.00962.x CrossRefGoogle Scholar
  14. Jennings HS (1907) Behavior of the starfish, Asterias forreri de Loroil. U Calif Publicat Zool 4:102–152Google Scholar
  15. Ji C, Wu L, Zhao W, Wang S, Lv J (2012) Echinoderms have bilateral tendencies. PLoS One 7:1–6.  https://doi.org/10.1371/journal.pone.0028978 CrossRefGoogle Scholar
  16. Kidawa A, Potocka M, Janecki T (2010) The effects of temperature on the behaviour of the Antarctic sea star Odontaster validus. Pol Polar Res 31:273–284.  https://doi.org/10.2478/v10183-010-0003-3 CrossRefGoogle Scholar
  17. Kleitman N (1941) The effect of temperature on the righting of echinoderms. Biol Bull 80:292–298CrossRefGoogle Scholar
  18. Lawrence JM, Cowell BC (1995) The righting response as an indication of stress in Stichaster striatus (Echinodermata, Asteroidea). Mar Freshw Behav Phy 27:239–248.  https://doi.org/10.1080/10236249609378969 CrossRefGoogle Scholar
  19. Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3:704.  https://doi.org/10.1038/ncomms1713 CrossRefPubMedGoogle Scholar
  20. Loeb J (1900) Experiments on Asteroids. In: McKeen Catell J, Beddard FE (eds) Comparative physiology of the brain and comparative psychology. G. P. Putnam’s Sons, New YorkGoogle Scholar
  21. Lopes EM, Ventura CRR (2016) Development of the sea star Echinaster (Othilia) brasiliensis, with inference on the evolution of development and skeletal plates in Asteroidea. Biol Bull 230:25–35.  https://doi.org/10.1086/BBLv230n1p25 CrossRefPubMedGoogle Scholar
  22. Lopes EM, Perez-Portela R, Paiva PC, Ventura CRR (2016) The molecular phylogeny of the sea star Echinaster (Asteroidea: Echinasteridae) provides insights for genus taxonomy. Invertebr Biol 135:235–244.  https://doi.org/10.1111/ivb.12135 CrossRefGoogle Scholar
  23. Marsh RL (1990) Deactivation rate and shortening velocity as determinants of contractile frequency. Am J Physiol Regul Integr Comp Physiol 259:R223–R230.  https://doi.org/10.1152/ajpregu.1990.259.2.R223 CrossRefGoogle Scholar
  24. Montgomery EM, Palmer AR (2012) Effects of body size and shape on locomotion in the Bat Star (Patiria miniata). Biol Bull 222:222–232.  https://doi.org/10.1086/BBLv222n3p222 CrossRefPubMedGoogle Scholar
  25. Morris VB (2007) Origins of radial symmetry identified in an echinoderm during adult development and the inferred axes of ancestral bilateral symmetry. Proc R Soc Lond B Biol Sci 274:1511–1516.  https://doi.org/10.1098/rspb.2007.0312 CrossRefGoogle Scholar
  26. Mueller B, Bos AR, Graf G, Gumanao GS (2011) Size-specific locomotion rate and movement pattern of four common Indo-Pacific sea stars (Echinodermata; Asteroidea). Aquat Biol 12:157–164.  https://doi.org/10.3354/ab00326 CrossRefGoogle Scholar
  27. Newell RC (1969) Effects of fluctuations in temperature on the metabolism of intertidal invertebrates. Am Zool 9:293–307CrossRefGoogle Scholar
  28. Nixon SW, Granger S, Buckley BA, Lamont M, Rowell B (2004) A one hundred and seventeen year coastal water temperature record from Woods Hole, Massachusetts. Estuaries 27:397–404.  https://doi.org/10.1007/BF02803532 CrossRefGoogle Scholar
  29. NOAA/NDBC (2017) Station CLBF1—Clam Bayou, FL. National Data Buoy Center. http://ndbc.noaa.gov/station_page.php?station=clbf1. Accessed 15 April 2019
  30. Oczkowski A, McKinney R, Ayvazian S, Hanson A, Wigand C, Markham E (2015) Preliminary evidence for the amplification of global warming in shallow, intertidal estuarine waters. PLoS One.  https://doi.org/10.1371/journal.pone.0141529 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Oviatt CA (2004) The changing ecology of temperate coastal waters during a warming trend. Estuaries 27:895–904.  https://doi.org/10.1007/bf02803416 CrossRefGoogle Scholar
  32. Peck LS, Webb KE, Miller A, Clark MS, Hill T (2008) Temperature limits to activity, feeding and metabolism in the Antarctic starfish Odontaster validus. Mar Ecol Prog Ser 358:181–189.  https://doi.org/10.3354/meps07336 CrossRefGoogle Scholar
  33. Peck L, Morley S, Clark M (2010) Poor acclimation capacities in Antarctic marine ectotherms. Mar Biol 157:2051–2059.  https://doi.org/10.1007/s00227-010-1473-x CrossRefGoogle Scholar
  34. Pinsky ML, Eikeset AM, McCauley DJ, Payne JL, Sunday JM (2019) Greater vulnerabilty to warming of marine versus terrestrial ecotherms. Nature 569:108–111.  https://doi.org/10.1038/s41586-019-1132-4 CrossRefPubMedGoogle Scholar
  35. Polls I, Gonor J (1975) Behavioral aspects of righting in two asteroids from the Pacific coast of North America. Biol Bull 148:68–84.  https://doi.org/10.2307/1540651 CrossRefPubMedGoogle Scholar
  36. Pörtner H-O, Karl D, Boyd PW, Cheung W, Lluch-Cota SE, Nojiri Y, Schmidt DN, Zavialov PO (2014) Ocean systems. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea S (eds) Climate change 2014: impacts, adaptation, and vulnerability. Part A: Global and sectoral aspects. Contribution of working group II to the fifth assessment report of the Intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 411–484Google Scholar
  37. Rhein M, Rintoul SR, Aoki S, Campos E, Chambers D, Feely RA, Gulev S, Johnson GC, Josey SA, Kostianoy A, Mauritzen C, Roemmich D, Talley LC, Wang F (2013) Observations: ocean. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 255–316Google Scholar
  38. Richard J, Morley SA, Deloffre J, Peck LS (2012) Thermal acclimation capacity for four Arctic marine benthic species. J Exp Mar Biol Ecol 424–425:38–43.  https://doi.org/10.1016/j.jembe.2012.01.010 CrossRefGoogle Scholar
  39. Schmidt-Nielsen K (1975) Scaling in biology: the consequences of size. J Exp Zool 194(1):287–307.  https://doi.org/10.1002/jez.1401940120 CrossRefPubMedGoogle Scholar
  40. Sherman E (2015) Can sea urchins beat the heat? Sea urchins, thermal tolerance and climate change. PeerJ 3:e1006.  https://doi.org/10.7717/peerj.1006 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936PubMedGoogle Scholar
  42. Turner RE (2003) Coastal ecosystems of the Gulf of Mexico and climate change. In: Ning H, Turner RE, Doyle T, Abdollahi KK (eds) Integrated assessment of the climate change impacts on the Gulf Coast region. Gulf Coast Climate Change Assessment Council, WashingtonGoogle Scholar
  43. Turner RL (2013) Echinaster. In: Lawrence JM (ed) Starfish: biology and ecology of the asteroidea. The John Hopkins University Press, Baltimore, pp 200–215Google Scholar
  44. Ubaldo JP, Uly FA, Dy DT (2007) Temperature tolerance of some species of Philippine intertidal echinoderms. Philipp Sci 47:105–119.  https://doi.org/10.3860/psci.v44i0.381 CrossRefGoogle Scholar
  45. Ulbricht R (1973) Effect of temperature acclimation on the metabolic rate of sea urchins. Mar Biol 19:273–277.  https://doi.org/10.1007/BF00348893 CrossRefGoogle Scholar
  46. Verrill AE (1869) On new and imperfectly known echinoderms and corals. Proc Boston Soc Nat Hist 12:381–391Google Scholar
  47. Young JS, Peck LS, Matheson T (2006a) The effects of temperature on peripheral neuronal function eurythermal and stenothermal crustaceans. J Exp Biol 209:1976–1987CrossRefGoogle Scholar
  48. Young JS, Peck LS, Matheson T (2006b) The effects of temperature on walking and righting in temperature and Antarctic crustaceans. Polar Biol 29:978–987CrossRefGoogle Scholar
  49. Zhang LS, Zhang LL, Shi DT, Wei J, Chang YQ, Zhao C (2017) Effects of long-term elevated temperature on covering, sheltering and righting behaviors of the sea urchin Strongylocentrotus intermedius. PeerJ 5:e3122.  https://doi.org/10.7717/peerj.3122 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Galbraith Marine Science LaboratoryEckerd CollegeSt. PetersburgUSA

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