Abstract
For the antitropical gooseneck barnacle Pollicipes elegans, population-specific physiological temperature tolerance of larvae may serve as a barrier to larval dispersal across the warmest regions of the tropical Pacific Ocean. Thermal tolerance ranges of larvae of three different populations of P. elegans sampled in 2011 and 2012 (Mexico [MX], El Salvador [ES], and Peru [PE]) were investigated by measuring three indicators of physiological performance: swimming activity, oxygen consumption, and lethality or LT50. The thermal tolerance profiles, which include measurable optimum (maximum aerobic performance), pejus (“getting worse”) and pessimum (worst aerobic performance) ranges, of larvae from the three populations were consistent with their characteristic environmental temperatures. In MX, larvae live close to the upper border of their optimum during warm months and so have a limited capacity to tolerate higher-than-normal temperatures. Larvae from the ES population likewise appear to live within their optimum temperature range, but these larvae lack a detectable pessimum range, suggesting they would be unable to cope with temperatures above their pejus range. Larvae from PE have a broad optimum but no pejus range. Different thermal tolerance ranges provide strong evidence for population-dependent physiological adaptations in P. elegans. For the southern (PE) and northern (MX) P. elegans populations, high tropical temperatures are likely to be a strong direct physiological barrier to larval survival and dispersal, which is in contrast to the more thermally tolerant ES population.
Similar content being viewed by others
References
Acker JG, Leptoukh G (2007) Online analysis enhances use of NASA earth science data. Eos Trans AGU 88(2):14–17
Anker A, Ahyong S (2007) A rediagnosis of Athanopsis australis BANNER & BANNER, 1982, a rare alpheid shrimps from Southern Australia, with a phylogeny of Athanopsis COUTIERE, 1897 and remarks on antitropical distributions in the Alpheidae (Decapoda, Caridae). Crustaceana 80:685–697
Burridge C (2002) Antitropicality of Pacific fishes: molecular insights. Environ Biol Fish 65:151–164
Burridge CP, White RWG (2000) Molecular phylogeny of the antitropical subgenus Goniistius (Perciformes: Cehilodactylidae: Cehilodactylus): evidence for multiple transequatorial divergences and non-monophyly. Biol J Linn Soc 70:435–458
Carriquiry JD, Cupul-Magana AL, Rodriguez-Zaragoza F, Medina-Rosas P (2001) Coral bleaching and mortality in the Mexican Pacific during the 1997–98 El Niño and prediction from a remote sensing approach. Bull Mar Sci 69:237–249
Carstensen D, Laudien J, Siefeld W, Oliva ME, Arntz WE (2010) Early larval development of Donax obesulus: response to El Niño temperature and salinity conditions. J Shellfish Res 29:361–368
Coles SL, Jokiel PL, Lewis CR (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac Sci 30:159–166
Dawson MN, Grosberg RK, Stuart YE, Sanford E (2010) Population genetic analysis of a recent range expansion: mechanisms regulating the poleward range limit in the volcano barnacle Tetraclita rubescens. Mol Ecol 19:1585–1605
Emlet RB, Sadro SS (2006) Linking stages of life history: how larval quality translates into juvenile performance for an intertidal barnacle (Balanus glandula). Integr Comp Biol 46:334–346
Fowler AE, Gerner NV, Sewell MA (2011) Temperature and salinity tolerance of Stage 1 zoeae predict possible range expansion of an introduced portunid crab, Charybdis japonica, in New Zealand. Biol Invasions 13:691–699
Frederich M, Pörtner H (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol Regul Integr Comp Physiol 279:R1531–R1538
Garrison T (2009) Oceanography: an invitation to marine science, 7th edn. Brooks/Cole, Belmont, USA
Hamasaki K (2003) Effects of temperature on the egg incubation period, survival and developmental period of larvae of the mud crab Scylla serrata (Forskal) (Brachyura: Portunidae) reared in the laboratory. Aquaculture 219:561–572
Hilbish TJ, Mullinax A, Dolven SI, Meyer A, Koehn RK, Rawson PD (2000) Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration. Mar Biol 136:69–77
Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, Princeton, NJ
Hubbs CL (1952) Antitropical distribution of fishes and other organisms. In: Proceedings of the 7th Pacific Science Congress 3:324–330
Jost JA, Podolski SM, Frederich M (2012) Enhancing thermal tolerance by eliminating the pejus range: a comparative study with three decapod crustaceans. Mar Ecol Prog Ser 444:263–274
Kameya A, Zeballos J (1988) Distribuxion y desidad de percebes P. elegans (Crustacea: Cirripedia) en el Mediolitoral peruano (Yasila, Paita, Chilca, Lima). Bol Inst mar Peru 12:6–13
Kauffman EG, Johnson CC (1988) The morphological and ecological evolution of middle and upper cretaceous reef-building rudists. Palaois 3:194–216
Koufopanou V, Reid DG, Ridgway SA, Thomas RH (1999) A molecular phylogeny of the patellid limpets (Gastropoda: Patellidae) and its implications of the origins of their antitropical distribution. Mol Phylogenet Evol 11:138–156
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
Laguna JE (1990) Shore barnacles (Cirripedia, Thoracica) and a revision of their provincialism and transition zones in the tropical eastern Pacific. Bull Mar Sci 46:406–424
Lindberg DL (1991) Marine biotic interchange between the northern and southern hemispheres. Paleobiology 17:308–324
Marsh AG, Manahan DT (1999) A method for accurate measurements of the respiration rates of marine invertebrate embryos and larvae. Mar Ecol Prog Ser 184:1–10
Mora C, Ospina AF (2001) Tolerance to high temperatures and potential impact of sea warming on reef fishes of Gorgona Island (tropical eastern Pacific). Mar Biol 139:765–769
Newman WA, Foster BA (1987) Southern hemisphere endemism among the barnacles: explained in part by extinction of northern members of amphitropical taxa. Bull Mar Sci 4:361–377
O’Dea A, Hoyos N, Rodriguez F, De Gracia B, Degracia C (2012) History of upwelling in the Tropical Eastern Pacific and the paleogeography of the Isthmus of Panama. Palaeogeogr Palaeoecol 349:59–66
Pennington JT, Mahoney KL, Kuwahara VS, Kolber DD, Calienes R, Chavez FP (2006) Primary production in the eastern tropical Pacific: a review. Prog Oceanogr 69:285–317
Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146
Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692
Pörtner HO, Lucassen M, Storch D (2005) Metabolic biochemistry: its role in thermal tolerance and in the capacities of physiological and ecological function. In: Farrell A, Steffensen JF (eds) The physiology of polar fishes. Elsevier, Amsterdam, pp 79–154
Shi GR, Grunt TA (2000) Permian Gondwana-Boreal antitropicality with special reference to brachiopod faunas. Palaeogeogr Palaeoecol 155:239–263
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15
Somero GN (2005) Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front Zool 2:1. doi:10.1186/1742-9994-2-1
Sommer AM, Pörtner HO (2004) Mitochondrial function in seasonal acclimatization versus latitudinal adaptation to cold in the lugworm Arenicola marina (L.). Physiol Biochem Zool 77:174–186
Stepien CA, Rosenblatt RH (1996) Genetic divergence in antitropical pelagic marine fishes (Trachurus, Merluccius and Scomber) between North and South America. Copeia 3:586–598
Stillman JH, Somero GN (1996) Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus Petrolisthes): correlation of physiology, biochemistry and morphology with vertical distribution. J Exp Biol 199:1845–1855
Stinson TF, Fang K, Lubov A (1979) User’s guide to SegReg. Staff papers 13330. University of Minnesota. Department of Applied Economics, Minnesota
Storch D, Santelices P, Barria J, Cabeza K, Pörtner HO, Fernandez M (2009) Thermal tolerance of crustacean larvae (zoea I) in two different populations of the kelp crab Taliepus dentatus (Milne-Edwards). J Exp Biol 212:1371–1376
Storch D, Fernandez M, Navarrete SA, Pörtner HO (2011) Thermal tolerance of larval stages of the Chilean kelp crab Taliepus dentatus. Mar Ecol Prog Ser 429:157–167
Strathmann M (1987) Reproduction and development of marine invertebrates of the northern Pacific coast. University of Washington Press, Seattle
Stroup WW (2012) Generalized linear mixed models: modern concepts, methods and applications. CRC Press, Boca Raton, FL
Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B 278:1823–1830
Tschischka K, Abele D, Pörtner HO (2000) Mitochondrial oxyconformity and cold adaption in the polychaete Nereis pelagica and the bivalve Arctica islandica from the Baltic and the White Seas. J Exp Biol 203:3355–3368
Urban H-J (1994) Upper temperature tolerance of ten bivalve species off Peru and Chile related to El Niño. Mar Ecol Prog Ser 107:139–145
Van Syoc RJ (1994) Genetic divergence between subpopulations of the eastern Pacific goose barnacle Pollicipes elegans: mitochondrial cytochrome c subunit 1 sequences. Mol Mar Biol Biotech 3:338–346
Walther K, Anger K, Pörtner HO (2010) Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79°N). Mar Ecol Prog Ser 417:159–170
Weiss M, Heilmayer O, Brey T, Thatje S (2009) Influence of temperature on the zoeal development and elemental composition of the cancrid crab, Cancer setosus Molina, 1782 from Pacific South America. J Exp Mar Biol Ecol 376:48–54
Weiss M, Heilmayer O, Brey T, Lucassen M, Pörtner HO (2012) Physiological capacity of Cancer setosus larvae—adaptation to El Niño southern oscillation conditions. J Exp Mar Biol Ecol 413:100–105
White BN (1986) The Isthmian link, antitropicality, and American biogeography: distributional history of the Atherinopsinae (Pisces: Atherinidae). Syst Zool 35:176–196
Zippay ML, Hofmann GE (2010) Physiological tolerances across latitudes: thermal sensitivity of larval marine snails (Nucella spp.). Mar Biol 157:707–714
Acknowledgements
This work was supported by Clemson University’s Department of Biological Sciences and by the National Science Foundation (OCE-0961996 to PBM and ALM). We thank Carmen Yamashiro from the Marine Invertebrates Research unit of IMARPE in Peru and Enrique Barraza from the Natural Resources and Environmental Department in El Salvador for providing collection permits and logistical support. We also thank L. Plough and C. Genovese for help with collection and technical support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. P. Grassle.
Rights and permissions
About this article
Cite this article
Walther, K., Crickenberger, S.E., Marchant, S. et al. Thermal tolerance of larvae of Pollicipes elegans, a marine species with an antitropical distribution. Mar Biol 160, 2723–2732 (2013). https://doi.org/10.1007/s00227-013-2265-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-013-2265-x