Marine Biology

, 163:228 | Cite as

Retention of high thermal tolerance in the invasive foraminifera Amphistegina lobifera from the Eastern Mediterranean and the Gulf of Aqaba

  • C. Schmidt
  • R. Morard
  • M. Prazeres
  • H. Barak
  • M. Kucera
Invasive Species - Original paper
Part of the following topical collections:
  1. Invasive Species

Abstract

Invasive species allow an investigation of trait retention and adaptations after exposure to new habitats. Recent work on corals from the Gulf of Aqaba (GoA) shows that tolerance to high temperature persists thousands of years after invasion, without any apparent adaptive advantage. Here, we test whether thermal tolerance retention also occurs in another symbiont-bearing calcifying organism. To this end, we investigate the thermal tolerance of the benthic foraminifera Amphistegina lobifera from the GoA (29°30.14167 N, 34°55.085E) and compare it to a recent “Lessepsian invader population” from the Eastern Mediterranean (EaM) (32°37.386 N, 34°55.169E). We first established that the studied populations are genetically homogenous but distinct from a population in Australia and that they contain a similar consortium of diatom symbionts, confirming their recent common descent. Thereafter, we exposed specimens from GoA and EaM to elevated temperatures for three weeks and monitored survivorship, growth rates and photophysiology. Both populations exhibited a similar pattern of temperature tolerance. A consistent reduction of photosynthetic dark yields was observed at 34 °C and reduced growth was observed at 32 °C. The apparent tolerance to sustained exposure to high temperature cannot have a direct adaptive importance, as peak summer temperatures in both locations remain <32 °C. Instead, it seems that in the studied foraminifera, tolerance to high temperature is a conservative trait and the EaM population retained this trait since its recent invasion. Such pre-adaptation to higher temperatures confers A. lobifera a clear adaptive advantage in shallow and episodically high temperature environments in the Mediterranean under further warming.

Supplementary material

227_2016_2998_MOESM1_ESM.xlsx (20 kb)
Sequence data on the symbionts extracted from Amphistegina lobifera (XLSX 20 kb)

References

  1. Alve E (1999) Colonization of new habitats by benthic foraminifera: a review. Earth Sci Rev 46:167–185. doi:10.1016/S0012-8252(99)00016-1 CrossRefGoogle Scholar
  2. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE. doi:10.1371/journal.pone.0006372 Google Scholar
  3. André A, Quillévéré F, Morard R, Ujiié Y, Escarguel G, de Vargas C, de Garidel-Thoron T, Douady CJ, Ketmaier V (2014) SSU rDNA Divergence in Planktonic Foraminifera: molecular taxonomy and biogeographic implications. PLoS ONE 9:e104641. doi:10.1371/journal.pone.0104641 CrossRefGoogle Scholar
  4. Berkelmans R, Willis BL (1999) Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18:219–228. doi:10.1007/s003380050186 CrossRefGoogle Scholar
  5. Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23:74–83. doi:10.1007/s00338-003-0353-y CrossRefGoogle Scholar
  6. Bernhard JM (2000) Distinguishing live from dead foraminifera: methods review and proper applications. Micropaleontology 46:38–46Google Scholar
  7. Braithwaite CJR (1987) Geology and Paleogeography of the Red Sea region. In: Edwards AJ, Head SM (eds) Red Sea. Pergamon Press, Oxford, pp 22–44CrossRefGoogle Scholar
  8. Caruso A, Cosentino C (2014) The first colonization of the genus Amphistegina and other exotic benthic foraminifera of the Pelagian Islands and south-eastern Sicily (central Mediterranean Sea). Mar Micropaleontol 111:38–52. doi:10.1016/j.marmicro.2014.05.002 CrossRefGoogle Scholar
  9. Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026. doi:10.1126/science.1206432 CrossRefGoogle Scholar
  10. Coles SL, Riegl BM (2013) Thermal tolerances of reef corals in the Gulf: a review of the potential for increasing coral survival and adaptation to climate change through assisted translocation. Mar Pollut Bull 72:323–332. doi:10.1016/j.marpolbul.2012.09.006 CrossRefGoogle Scholar
  11. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  12. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109:17995–17999. doi:10.1073/pnas.1208909109 CrossRefGoogle Scholar
  13. deVargas C, Zaninetti L, Hilbrecht H, Pawlowski J (1997) Phylogeny and rates of molecular evolution of planktonic foraminifera: SSU rDNA sequences compared to the fossil record. J Mol Evol 45:285–294. doi:10.1007/pl00006232 CrossRefGoogle Scholar
  14. Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Glob Change Biol 19:3640–3647. doi:10.1111/gcb.12356 CrossRefGoogle Scholar
  15. Grimm GW, Stögerer K, Topaç Ertan K, Kitazato H, Kučera M, Hemleben V, Hemleben C (2007) Diversity of rDNA in Chilostomella: molecular differentiation patterns and putative hermit types. Mar Micropaleontol 62:75–90. doi:10.1016/j.marmicro.2006.07.005 CrossRefGoogle Scholar
  16. Gruber L, Almogi-Labin A, Sivan D, Herut B (2007) The life cycle of the symbiont-bearing larger foraminifera Amphistegina lobifera, a new arrival on the Israeli shelf. Rapports et procès-verbaux des réunions Commission Internationale pour l’exploration scientifique de la Mer Méditerranée 38:491Google Scholar
  17. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321CrossRefGoogle Scholar
  18. Hallock P (1979) Trends in test shape with depth in large, symbiont-bearing foraminifera. J Foraminifer Res 9:61–69CrossRefGoogle Scholar
  19. Hallock P (1981) Light dependence in Amphistegina. J Foraminifer Res 11:40–46. doi:10.2113/gsjfr.11.1.40 CrossRefGoogle Scholar
  20. Hallock P (1981b) Production of carbonate sediments by selected large benthic foraminifera on two Pacific coral reefs. J Sediment Res 51:467–474Google Scholar
  21. Hallock P (2000) Symbiont-bearing foraminifera: harbingers of global change? Micropalaeontology 46:95–104Google Scholar
  22. Hallock P, Talge HK (1993) Symbiont loss (“bleaching”) in the reef-dwelling benthic foraminifer Amphistegina gibbosa in the Florida Keys in 1991–92. In: Ginsburg RN (ed) Proceedings of the colloquium on global aspects of coral reefs: health, hazards and history. University of Miami, Florida, pp 94–100Google Scholar
  23. Hallock P, Talge HK, Smith KM, Cockey EM (1992) Bleaching in the reef-dwelling foraminifera Amphistegina gibbosa. In: Richmond RH (ed) Proceedings of the 7th international coral reef symposium. University of Guam Press, Mangilao, pp 44–49Google Scholar
  24. Hammer, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9. http://palaeo-electronica.org/2001_2001/past/issue2001_2001.htm
  25. Hariri MS (2008) Effect of hydrographic conditions on the ecology of benthic foraminifera in two different hypersaline lagoons, eastern Red Sea coast, Kingdom of Saudi Arabia. Mar Sci 19:3–13Google Scholar
  26. Herut B, Almogi-Labin A, Jannink N, Gertman I (2000) The seasonal dynamics of nutrient and chlorophyll a concentrations on the SE Mediterranean shelf-slope. Oceanol Acta 23:771–782. doi:10.1016/s0399-1784(00)01118-x CrossRefGoogle Scholar
  27. Hohenegger J (2006) The importance of symbiont-bearing benthic foraminifera for West Pacific carbonate beach environments. Mar Micropaleontol 61:4–39. doi:10.1016/j.marmicro.2006.05.007 CrossRefGoogle Scholar
  28. Hyams O, Almogi-Labin A, Benjaminia C (2002) Larger foraminifera of the southeastern Mediterranean shallow continental shelf off Israel. Isr J Earth Sci 51:169–179. doi:10.1560/QAE1-KTEE-2K2L-QPCH CrossRefGoogle Scholar
  29. Hyams-Kaphzan O, Almogi-Labin A, Sivan D, Benjamini C (2008) Benthic foraminifera assemblage change along the southeastern Mediterranean inner shelf due to fall-off of Nile-derived siliciclastics. Neues Jahrbuch Fur Geologie Und Palaontologie-Abhandlungen 248:315–344. doi:10.1127/0077-7749/2008/0248-0315 CrossRefGoogle Scholar
  30. Langer MR (2008) Foraminifera from the Mediterranean and the Red Sea. In: Por FD (ed) Aqaba-Eilat, the Improbable Gulf: Environment, Biodiversity and Preservation. Magnes Press, Jersusalem, pp 399–417Google Scholar
  31. Langer MR, Hottinger L (2000) Biogeography of selected “larger” foraminifera. Micropaleontology 46:105–126. doi:10.2307/1486184 Google Scholar
  32. Langer MR, Silk MT, Lipps JH (1997) Global ocean carbonate and carbon dioxide production; the role of reef foraminifera. J Foraminifer Res 27:271–277. doi:10.2113/gsjfr.27.4.271 CrossRefGoogle Scholar
  33. Langer MR, Weinmann AE, Lötters S, Rödder D (2012) “Strangers” in paradise: modeling the biogeographic range expansion of the foraminifera Amphistegina in the Mediterranean Sea. J Foraminifer Res 42:234–244. doi:10.2113/gsjfr.42.3.234 CrossRefGoogle Scholar
  34. Lee J, Reimer C, McEnergy M (1980) The Identification of diatoms isolated as endosymbionts from larger foraminifera from the Gulf of Eilat (Red Sea) and the description of two new species, Fragilaria shiloi sp. nov. and Navicula reissii sp. nov. Bot Mar 23:41–48CrossRefGoogle Scholar
  35. Lee J, Erez J, McEnery M, Lagziel A, Xenophontos X (1986) Experiments on persistence of endosymbiotic diatoms in the larger foraminifer: Amphistegina lessonii. Symbiosis 1:211–226Google Scholar
  36. Locarnini RA, Mishonov AV, Antonov JI, Boyer TP, Garcia HE, Baranova OK, Zweng MM, Paver CR, Reagan JR, Johnson DR, Hamilton M, Seidov D (2013) World Ocean Atlas 2013 temperature. In: AMTENAN (ed) National Centers for environmental information NOAA Atlas NESDIS 73. NOAA, USA, p 40Google Scholar
  37. McKee ED, Chronic J, Leopold EB (1959) Sedimentary belts in lagoon of Kapingamarangi Atoll. AAPG Bull 43:501–562Google Scholar
  38. Meric E, Avsar N, Yokes MB (2008) Some alien foraminifers along the Aegean and southwestern coasts of Turkey. Micropaleontology 54:307–349Google Scholar
  39. Meriç E, Yokeş MB, Avşar N, Kıyak NG, Öner E, Nazik A, Demirtaşlı E, Dinçer F, Öztürk MZ (2015) Did Amphistegina lobifera Larsen reach the Mediterranean via the Suez Canal? Quatern Int. doi:10.1016/j.quaint.2015.08.088 Google Scholar
  40. Merkado G, Holzmann M, Apotheloz-Perret-Gentil L, Pawlowski J, Abdu U, Almogi-Labin A, Hyams-Kaphzan O, Bakhrat A, Abramovich S (2013) Molecular evidence for Lessepsian invasion of Soritids (larger symbiont bearing benthic foraminifera). PLoS ONE. doi:10.1371/journal.pone.0077725 Google Scholar
  41. Morard R, Quillevere F, Escarguel G, Ujiie Y, de Garidel-Thoron T, Norris RD, de Vargas C (2009) Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa. Mar Micropaleontol 71:148–165. doi:10.1016/j.marmicro.2009.03.001 CrossRefGoogle Scholar
  42. Mouanga GH, Langer MR (2014) At the front of expanding ranges: shifting community structures at amphisteginid species range margins in the Mediterranean Sea. Neues Jb Geol Paläontol Abh 271:141–150. doi:10.1127/0077-7749/2014/0381 CrossRefGoogle Scholar
  43. Muller PH (1974) Sediment production and population biology of the benthic foraminifer Amphistegina madagascariensis. Limnol Oceanogr 19:802–809CrossRefGoogle Scholar
  44. Occhipinti-Ambrogi A (2007) Global change and marine communities: alien species and climate change. Mar Pollut Bull 55:342–352. doi:10.1016/j.marpolbul.2006.11.014 CrossRefGoogle Scholar
  45. Paldor N, Anati DA (1979) Seasonal variations of temperature and salinity in the Gulf of Elat (Aqaba). Deep Sea Res Part A Oceanogr Res Papers 26:661–672. doi:10.1016/0198-0149(79)90039-6 CrossRefGoogle Scholar
  46. Parker JH, Gischler E, Eisenhauer A (2012) Biodiversity of foraminifera from Late Pleistocene to Holocene coral reefs, South Sinai, Egypt. Mar Micropaleontol 86–87:59–75. doi:10.1016/j.marmicro.2012.02.002 CrossRefGoogle Scholar
  47. Pawlowski J, Holzmann M, Berney C, Fahrni J, Cedhagen T, Bowser SS (2002) Phylogeny of allogromiid foraminifera inferred from SSU rRNA gene sequences. J Foraminifer Res 32:334–343. doi:10.2113/0320334 CrossRefGoogle Scholar
  48. Pawlowski J, Fahrni J, Lecroq B, Longet D, Cornelius N, Excoffier L, Cedhagen T, Gooday AJ (2007) Bipolar gene flow in deep-sea benthic foraminifera. Mol Ecol 16:4089–4096. doi:10.1111/j.1365-294X.2007.03465.x CrossRefGoogle Scholar
  49. Prazeres M, Uthicke S, Pandolfi J (2016a) Changing light levels induce photo-oxidative stress and alterations in shell density of Amphistegina lobifera (Foraminifera). Mar Ecol Prog Ser 549:69–78CrossRefGoogle Scholar
  50. Prazeres M, Uthicke S, Pandolfi JM (2016b) Influence of local habitat on the physiological responses of large benthic foraminifera to temperature and nutrient stress. Sci Rep UK 6:21936Google Scholar
  51. Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829CrossRefGoogle Scholar
  52. R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  53. Reiss Z, Hottinger L (1984) The Gulf of Aqaba: ecological micropaleontology. Springer, BerlinCrossRefGoogle Scholar
  54. SAS (2014) JMP statistics software, Version 11. SAS, HeidelbergGoogle Scholar
  55. Schmidt C, Heinz P, Kucera M, Uthicke S (2011) Temperature-induced stress leads to bleaching in larger benthic foraminifera hosting endosymbiotic diatoms. Limnol Oceanogr 56:1587–1602. doi:10.4319/lo.2011.56.5.1587 CrossRefGoogle Scholar
  56. Schmidt C, Kucera M, Uthicke S (2014) Combined effects of warming and ocean acidification on coral reef foraminifera Marginopora vertebralis and Heterostegina depressa. Coral Reefs 33:805–818. doi:10.1007/s00338-014-1151-4 CrossRefGoogle Scholar
  57. Schmidt C, Morard R, Almogi-Labin A, Weinmann AE, Titelboim D, Abramovich S, Kucera M (2015) Recent invasion of the symbiont-bearing foraminifera Pararotalia into the Eastern Mediterranean facilitated by the ongoing warming trend. PLoS ONE 10:e0132917. doi:10.1371/journal.pone.0132917 CrossRefGoogle Scholar
  58. Schmidt C, Titelboim D, Brandt J, Herut B, Abramovich S, Almogi-Labin A, Kucera M (2016) Extremely heat tolerant photosymbiosis in a shallow marine benthic foraminifera. Sci Rep UK. doi:10.1038/srep30930 Google Scholar
  59. Shaltout M, Omstedt A (2014) Recent sea surface temperature trends and future scenarios for the Mediterranean Sea. Oceanologia 56:411–443. doi:10.5697/oc.56-3.411 CrossRefGoogle Scholar
  60. Talge HK, Hallock P (1995) Cytological examination of symbiont loss in a benthic foraminifera, Amphistegina gibbosa. Mar Micropaleontol 26:107–113. doi:10.1016/0377-8398(95)00015-1 CrossRefGoogle Scholar
  61. Talge HK, Hallock P (2003) Ultrastructural responses in field-bleached and experimentally stressed Amphistegina gibbosa (Class Foraminifera). J Eukaryot Microbiol 50:324–333. doi:10.1111/j.1550-7408.2003.tb00143.x CrossRefGoogle Scholar
  62. ter Kuile B, Erez J (1984) In situ growth rate experiments on the symbiont-bearing foraminifera Amphistegina lobifera and Amphisorus hemprichii. J Foraminifer Res 14:262–276. doi:10.2113/gsjfr.14.4.262 CrossRefGoogle Scholar
  63. Titelboim D, Almogi-Labin A, Herut B, Kucera M, Schmidt C, Hyams-Kaphzan O, Ovadia O, Abramovich S (2016) Selective responses of benthic foraminifera to thermal pollution. Mar Pollut Bull. doi:10.1016/j.marpolbul.2016.02.002 Google Scholar
  64. Triantaphyllou MV, Koukousioura O, Dimiza MD (2009) The presence of the Indo-Pacific symbiont-bearing foraminifer Amphistegina lobifera in Greek coastal ecosystems (Aegean Sea, Eastern Mediterranean). Mediterr Mar Sci 10:73–85Google Scholar
  65. Triantaphyllou MV, Dimiza MD, Koukousioura O, Hallock P (2012) Observations of the life cycle of the symbiont-bearing foraminifer Amphistegina lobifera Larsen, an invasive species in coastal ecosystems of the Aegean Sea (Greece, E., Mediterranean). J Foraminifer Res 42:143–150CrossRefGoogle Scholar
  66. Tsuchiya M, Grimm GW, Heinz P, Stogerer K, Ertan KT, Collen J, Bruchert V, Hemleben C, Hemleben V, Kitazato H (2009) Ribosomal DNA shows extremely low genetic divergence in a world-wide distributed, but disjunct and highly adapted marine protozoan (Virgulinella fragilis, Foraminiferida). Mar Micropaleontol 70:8–19. doi:10.1016/j.marmicro.2008.10.001 CrossRefGoogle Scholar
  67. Tsui CKM, Marshall W, Yokoyama R, Honda D, Lippmeier JC, Craven KD, Peterson PD, Berbee ML (2009) Labyrinthulomycetes phylogeny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding. Mol Phylogenet Evol 50:129–140CrossRefGoogle Scholar
  68. Uthicke S, Vogel N, Doyle J, Schmidt C, Humphrey C (2012) Interactive effects of climate change and eutrophication on the dinoflagellate-bearing benthic foraminifer Marginopora vertebralis. Coral Reefs 31:401–414. doi:10.1007/s00338-011-0851-2 CrossRefGoogle Scholar
  69. van Dam JW, Negri AP, Mueller JF, Altenburger R, Uthicke S (2012) Additive pressures of elevated sea surface temperatures and herbicides on symbiont-bearing foraminifera. PLoS ONE 7:e33900. doi:10.1371/journal.pone.0033900 CrossRefGoogle Scholar
  70. Webster NS, Negri AP, Botté ES, Laffy PW, Flores F, Noonan S, Schmidt C, Uthicke S (2016) Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci Rep UK 6:19324. http://www.nature.com/articles/srep19324#supplementary-information. doi:10.1038/srep19324
  71. Weinmann AE, Rödder D, Lötters S, Langer MR (2013) Traveling through time: the past, present and future biogeographic range of the invasive foraminifera Amphistegina spp. in the Mediterranean Sea. Mar Micropaleontol 105:30–39. doi:10.1016/j.marmicro.2013.10.002 CrossRefGoogle Scholar
  72. Weis VM (2010) The susceptibility and resilience of corals to thermal stress: adaptation, acclimatization or both? Mol Ecol 19:1515–1517. doi:10.1111/j.1365-294X.2010.04575.x CrossRefGoogle Scholar
  73. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  74. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glockner FO (2014) The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Res 42:D643–D648. doi:10.1093/nar/gkt1209 CrossRefGoogle Scholar
  75. Yokes MB, Meric E, Avsa N (2007) On the presence of alien foraminifera Amphistegina lobifera Larsen on the coasts of the Maltese Islands. Aquat Invasions 2:439–441CrossRefGoogle Scholar
  76. Zenetos A, Gofas S, Morri C, Rosso A, Violanti D, Raso JEG, Cinar ME, Almogi-Labin A, Ates AS, Azzurro E, Ballesteros E, Bianchi CN, Bilecenoglu M, Gambi MC, Giangrande A, Gravili C, Hyams-Kaphzan O, Karachle PK, Katsanevakis S, Lipej L, Mastrototaro F, Mineur F, Pancucci-Papadopoulou MA, Espla AR, Salas C, San Martin G, Sfriso A, Streftaris N, Verlaque M (2012) Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways. Mediterr Mar Sci 13:328–352Google Scholar
  77. Ziegler M, Uthicke S (2011) Photosynthetic plasticity of endosymbionts in larger benthic coral reef foraminifera. J Exp Mar Biol Ecol 407:70–80. doi:10.1016/j.jembe.2011.07.009 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • C. Schmidt
    • 1
  • R. Morard
    • 1
  • M. Prazeres
    • 2
    • 4
  • H. Barak
    • 3
  • M. Kucera
    • 1
  1. 1.MARUM, Center for Marine Environmental SciencesUniversity of BremenBremenGermany
  2. 2.ARC Centre of Excellence for Coral Reef Studies and School of Biological SciencesThe University of QueenslandSt. LuciaAustralia
  3. 3.Israel Oceanographic and Limnological Research (IOLR)National Institute of OceanographyHaifaIsrael
  4. 4.Comparative Genomics CentreJames Cook UniversityTownsvilleAustralia

Personalised recommendations