Abstract
The responses of ectothermic organisms to changes in temperature can be modified by acclimatization or adaptation to local thermal conditions. Thus, the effect of global warming and the deleterious effects of extreme heating events (e.g., heatwaves) on the metabolism and fitness of ectotherms can be population specific and reduced at warmer sites. We tested the hypothesis that when environmental temperature is greater, grazer populations in the Galápagos are less thermally sensitive (potentially due to acclimatization or adaptation). We quantified the acute thermal sensitivity of four populations of the pencil sea urchin, Eucidaris galapagensis, by measuring individual oxygen consumption across a range of temperatures. Thermal performance curves were estimated for each population and compared to local thermal conditions 2 months prior to collection. Results indicate that E. galapagensis populations were adapted and/or acclimatized to short-term local temperature as populations at warmer sites had substantially higher thermal tolerances. The acute thermal optimum (Topt) for the warmest and coolest site populations differed by 3 °C and the Topt was positively correlated with maximum temperature recorded at each site. Additionally, temperature-normalized respiration rate and activation energy (E) were negatively related to the maximum temperature. Understanding the temperature-dependent performance of the pencil urchin (the most significant mesograzer in this system), including its population specificity, provides insight into how herbivores and the functions they perform might be affected by further ocean heating.
Similar content being viewed by others
Data availability
All R data and code will be made publicly available at https://github.com/njsilbiger/GalapagosUrchins.
References
Alvarado JJ, Solís-Marín FA (2013) Echinoderms of Ecuador. Echinoderm research and diversity in Latin America. Springer, Berlin, pp 191–202
Andrew N (1993) Spatial heterogeneity, sea urchin grazing, and habitat structure on reefs in temperate Australia. Ecology 74:292–302
Angilletta MJ Jr, Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford
Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471
Banks S, Edgar G, Glynn P, Kuhn A, Moreno J, Ruiz D, Schuhbauer A, Tiernan JP, Tirado N, Vera M (2011) A review of Galápagos marine habitats and ecological processes under climate change scenarios. Clim Change Vulnerability Assess Galápagos Isl 47
Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci 110:1387–1392
Brandt M, Guarderas P (2002) Erizos de mar. In: Reserva Marina de Galápagos. Línea Base de la Biodiversidad. Fundación Charles Darwin/Servicio Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador. Fundación Charles Darwin/Servicio Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador, pp 396–418
Brandt M, Witman JD, Chiriboga AI (2012) Influence of a dominant consumer species reverses at increased diversity. Ecology 93:868–878
Bruno JF, Carr LA, O’Connor MI (2015) Exploring the role of temperature in the ocean through metabolic scaling. Ecology 96:3126–3140. https://doi.org/10.1890/14-1954.1
Burge CA, Mark Eakin C, Friedman CS, Froelich B, Hershberger PK, Hofmann EE, Petes LE, Prager KC, Weil E, Willis BL (2014) Climate change influences on marine infectious diseases: implications for management and society. Annu Rev Mar Sci 6:249–277
Carr LA, Bruno JF (2013) Warming increases the top-down effects and metabolism of a subtidal herbivore. PeerJ 1:e109
Castillo K, Helmuth B (2005) Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Mar Biol 148:261–270
Chapman A, Johnson C (1990) Disturbance and organization of macroalgal assemblages in the Northwest Atlantic. Hydrobiologia 192:77–121
Chevin L-M, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLOS Biol 8:e1000357. https://doi.org/10.1371/journal.pbio.1000357
Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905
Carr LA, Gittman RK, Bruno JF (2018) Temperature influences herbivory and algal biomass in the Galápagos Islands. Front Mar Sci. https://doi.org/10.3389/fmars.2018.00279
Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105:6668–6672. https://doi.org/10.1073/pnas.0709472105
Dong Y, Somero GN (2009) Temperature adaptation of cytosolic malate dehydrogenases of limpets (genus Lottia): differences in stability and function due to minor changes in sequence correlate with biogeographic and vertical distributions. J Exp Biol 212:169–177. https://doi.org/10.1242/jeb.024505
Edgar G, Banks S, Fariña J, Calvopiña M, Martínez C (2004) Regional biogeography of shallow reef fish and macro-invertebrate communities in the Galapagos archipelago. J Biogeogr 31:1107–1124
Edgar GJ, Banks SA, Brandt M, Bustamante RH, Chiriboga A, Earle SA, Garske LE, Glynn PW, Grove JS, Henderson S (2010) El Niño, grazers and fisheries interact to greatly elevate extinction risk for Galapagos marine species. Glob Change Biol 16:2876–2890
Elzhov TV, Mullen KM, Spiess A-N, Bolker B (2013) minpack. lm: R interface to the Levenberg-Marquardt nonlinear least-squares algorithm found in MINPACK, plus support for bounds. R package version 1.1–8
Eppley RW (1972) Temperature and phytoplankton growth in the sea. In: Fishery Bulletin. U.S. Department of Commerce/National Oceanic and Atmospheric Administration/National Marine Fisheries Services, Seattle, pp 1063–1085
Feingold JS, Glynn PW (2014) Coral research in the Galápagos Islands, Ecuador. The Galapagos marine reserve: a dynamic social–ecological system. Springer, New York, pp 3–22
Glynn PW (1984) Widespread coral mortality and the 1982–83 El Niño warming event. Environ Conserv 11:133–146
Glynn PW (1988) El Niño warming, coral mortality and reef framework destruction by echinoid bioerosion in the eastern Pacific. Galaxea 7:129–160
Glynn PW (1990) Coral mortality and disturbances to coral reefs in the tropical eastern Pacific. In: Global Ecological Consequences of the 1982–1983 El Nino—Southern Oscillation. Elsevier Oceanography Series, pp 55–126
Glynn PJ, Glynn PW, Riegl B (2017) El Niño, echinoid bioerosion and recovery potential of an isolated Galápagos coral reef: a modeling perspective. Mar Biol 164:146
Graham MH (2004) Effects of local deforestation on the diversity and structure of southern California giant kelp forest food webs. Ecosystems 7:341–357
Gunderson AR, Stillman JH (2015) Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc R Soc B Biol Sci 282:20150401
Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251. https://doi.org/10.1126/science.1061967
Harris M (1969) Breeding seasons of sea-birds in the Galapagos Islands. J Zool 159:145–165
Houde ED (1989) Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish Bull 87:471–495
Harvell C, Montecino-Latorre D, Caldwell J, Burt J, Bosley K, Keller A, Heron S, Salomon A, Lee L, Pontier O (2019) Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Sci Adv 5:eaau7042
Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485. https://doi.org/10.1038/nature09670
Houvenaghel G (1978) Oceanographic conditions in the Galapagos Archipelago and their relationships with life on the Islands. Upwelling ecosystems. Springer Berlin, Heidelberg, New York, pp 181–200
Houvenaghel G (1984) Oceanographic setting of the Galapagos Islands. Key environments: Galapagos. Pergamon Press, Oxford, pp 43–54
Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135
Huey RB, Stevenson R (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Integr Comp Biol 19:357–366. https://doi.org/10.1093/icb/19.1.357
Irving AD, Witman JD (2009) Positive effects of damselfish override negative effects of urchins to prevent an algal habitat switch. J Ecol 97:337–347
Jennings S, Brierley A, Walker J (1994) The inshore fish assemblages of the Galápagos Archipelago. Biol Conserv 70:49–57
Kern P, Cramp RL, Franklin CE (2015) Physiological responses of ectotherms to daily temperature variation. J Exp Biol 218:3068–3076. https://doi.org/10.1242/jeb.123166
Kuo ESL, Sanford E (2009) Geographic variation in the upper thermal limits of an intertidal snail: implications for climate envelope models. Mar Ecol Prog Ser 388:137–146. https://doi.org/10.3354/meps08102
Lawrence J, Sonnenholzner J (2004) Distribution and abundance of asteroids, echinoids, and holothuroids in Galápagos. Echinoderms: München. A.A. Balkema Publishers, New York, pp 239–244
Lessios HA, Kessing BD, Robertson DR, Paulay G (1999) Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53:806–817
López-Urrutia Á, San Martin E, Harris RP, Irigoien X (2006) Scaling the metabolic balance of the oceans. Proc Natl Acad Sci 103:8739–8744. https://doi.org/10.1073/pnas.0601137103
Manzello DP, Enochs IC, Bruckner A, Renaud PG, Kolodziej G, Budd DA, Carlton R, Glynn PW (2014) Galápagos coral reef persistence after ENSO warming across an acidification gradient. Geophys Res Lett 41:9001–9008
Oliver T, Palumbi S (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440
O’Connor MI, Piehler MF, Leech DM, Anton A, Bruno JF (2009) Warming and resource availability shift food web structure and metabolism. PLoS Biol 7:e1000178. https://doi.org/10.1371/journal.pbio.1000178
Padfield D, Matheson G (2018) nls. multstart: robust non-linear regression using AIC scores.
Padfield D, Yvon-Durocher G, Buckling A, Jennings S, Yvon-Durocher G (2016) Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecol Lett 19:133–142
Padfield D, Lowe C, Buckling A, Ffrench-Constant R, Student Research Team, Jennings S, Shelley F, Ólafsson JS, Yvon-Durocher G (2017) Metabolic compensation constrains the temperature dependence of gross primary production. Ecol Lett 20:1250–1260
Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898
Pinsky ML, Eikeset AM, McCauley DJ, Payne JL, Sunday JM (2019) Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569:108
Putnam HM, Gates RD (2015) Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol 218:2365–2372
Ruttenberg BI (2001) Effects of artisanal fishing on marine communities in the Galapagos Islands. Conserv Biol 15:1691–1699
Sanford E (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097
Sanford E (2002) The feeding, growth, and energetics of two rocky intertidal predators (Pisaster ochraceus and Nucella canaliculata) under water temperatures simulating episodic upwelling. J Exp Mar Biol Ecol 273:199–218
Schaeffer BA, Morrison JM, Kamykowski D, Feldman GC, Xie L, Liu Y, Sweet W, McCulloch A, Banks S (2008) Phytoplankton biomass distribution and identification of productive habitats within the Galapagos Marine Reserve by MODIS, a surface acquisition system, and in-situ measurements. Remote Sens Environ 112:3044–3054
Schoolfield R, Sharpe PJ, Magnuson C (1981) Non-linear regression of biological temperature-dependent rate models based on absolute reaction-rate theory. J Theor Biol 88:719–731
Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691–702
Seebacher F, White CR, Franklin CE (2015) Physiological plasticity increases resilience of ectothermic animals to climate change. Nat Clim Change 5:61
Sewell MA, Young CM (1999) Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter. J Exp Mar Biol Ecol 236:291–305
Siddon CE, Witman JD (2003) Influence of chronic, low-level hydrodynamic forces on subtidal community structure. Mar Ecol Prog Ser 261:99–110
Silbiger NJ, Goodbody-Gringley G, Bruno JF, Putnam HM (2019) Comparative thermal performance of the reef-building coral Orbicella franksi at its latitudinal range limits. Mar Biol 166:126
Sinclair B, Williams C, Terblanche J (2012) Variation in thermal performance among insect populations. Physiol Biochem Zool 85:594–606. https://doi.org/10.1086/665388
Sinclair BJ, Marshall KE, Sewell MA, Levesque DL, Willett CS, Slotsbo S, Dong Y, Harley CD, Marshall DJ, Helmuth BS (2016) Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecol Lett 19:1372–1385
Somero G (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers.’ J Exp Biol 213:912–920
Staehli A, Schaerer R, Hoelzle K, Ribi G (2009) Temperature induced disease in the starfish Astropecten jonstoni. Mar Biodivers Rec 2:e78. https://doi.org/10.1017/S1755267209000633
Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459
Stillman JH (2002) Causes and consequences of thermal tolerance limits in rocky intertidal porcelain crabs, genus Petrolisthes. Integr Comp Biol 42:790–796. https://doi.org/10.1093/icb/42.4.790
Stickle W, Moore M, Bayne B (1985) Effects of temperature, salinity and aerial exposure on predation and lysosomal stability of the dogwhelk Thais (Nucella) lapillus (L.). J Exp Mar Biol Ecol 93:235–258. https://doi.org/10.1016/0022-0981(85)90242-4
Sweet M, Bulling M, Williamson JE (2016) New disease outbreak affects two dominant sea urchin species associated with Australian temperate reefs. Mar Ecol Prog Ser 551:171–183
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 202:2925–2936
Vasseur DA, DeLong JP, Gilbert B, Greig HS, Harley CD, McCann KS, Savage V, Tunney TD, O’Connor MI (2014) Increased temperature variation poses a greater risk to species than climate warming. Proc R Soc B Biol Sci 281:20132612
Wellington GM (1984) Marine environment and protection. Key environments: Galapagos. Pergamon Press, Oxford, pp 247–264
Wellington GM, Strong AE, Merlen G (2001) Sea surface temperature variation in the Galapagos Archipelago: a comparison between AVHRR nighttime satellite data and in situ instrumentation (1982–1998). Bulletin of marine science. University of Miami—Rosenstiel School of Marine and Atmospheric Science, Miami, pp 27–42
Witman JD, Brandt M, Smith F (2010) Coupling between subtidal prey and consumers along a mesoscale upwelling gradient in the Galapagos Islands. Ecol Monogr 80:153–177
Wolcott TG (1973) Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look at" limiting factors". Biol Bull 145:389–422
Acknowledgements
We thank the Galápagos National Park Directorate for granting the permit PC-25-18 to perform the research, the Galápagos Science Center for logistics and facilities support (special thanks to S. Sotamba, J. Sotamba, D. Alarcón, C. Vintimilla, A. Carrión, and S. Sarzosa), the Universidad San Francisco de Quito and The University of North Carolina at Chapel Hill, the divers and field assistants O. Gorman, B. Morse, D. Fernández, M.J. Guarderas, J.M. Álava and E. Spencer, who either participated in the research cruise or provided guidance with data management preceding its analysis. We thank Captain E. Rosero and the crew of the research vessel Queen Mabel for providing reliable access to study sites and for fieldwork support. We thank the reviewers for their valuable remarks and suggestions that contributed to improving this manuscript.
Funding
The project was funded by the National Science Foundation (Grant OCE #1737071 to JFB).
Author information
Authors and Affiliations
Contributions
JFB and MB designed the experiment. JFB provided the materials and funding. MB, JFB, and ISR collected the data. ISR processed the data. NJS statistically analyzed the data. ISR, JFB, NJS, and MB wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interests.
Ethical approval
All applicable national and institutional guidelines for sampling, care and experimental use of organisms for the study have been followed. We obtained all necessary approvals and performed all the fieldwork and data collection under the permit PC 25–18 granted by the Galápagos National Park Directorate.
Additional information
Responsible Editor: A.E. Todgham.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewers: undisclosed experts.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Silva Romero, I., Bruno, J.F., Silbiger, N.J. et al. Local conditions influence thermal sensitivity of pencil urchin populations (Eucidaris galapagensis) in the Galápagos Archipelago. Mar Biol 168, 34 (2021). https://doi.org/10.1007/s00227-021-03836-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03836-9