Skip to main content
SpringerLink
Log in

Variable thermal stress tolerance of the reef-associated symbiont-bearing foraminifera Amphistegina linked to differences in symbiont type

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Adaptation, acclimatization and symbiont diversity are known to regulate thermal tolerance in corals, but the role of these mechanisms remains poorly constrained in other photosymbioses, such as large benthic foraminifera (LBFs), which are known to bleach at temperatures that are likely to be exceeded in the near future. LBFs inhabit a broad range of shallow-water settings. Within species, differences in thermal tolerance have been found among populations from different habitats, but it is not clear whether such differences occur among LBFs inhabiting similar habitats, but differing in other aspects, such as symbiont type. To this end, we compared responses to thermal stress in specimens from a population of Amphistegina lessonii, an abundant Indo-Pacific species, to specimens of Amphistegina gibbosa, its Atlantic counterpart, from a similar environment but two different water depths (5 and 18 m). Test groups of each species were exposed in a common experiment to three thermal stress scenarios over a four-week period. Growth, respiration, mortality and motility were measured to characterize the holobiont response. Coloration, photosynthesis and chlorophyll a content were measured to determine the response of the endosymbiotic diatoms. The photosymbionts were characterized by genetic fingerprinting. Our results show that, although groups of A. gibbosa were collected from different habitats, their responses were similar, indicating only marginally higher tolerance to thermal peaks in specimens from the shallower site. In contrast, species-specific differences were stronger, with A. lessonii showing higher tolerance to episodic stress and less pronounced impacts of chronic stress on motility, growth and photosymbiont performance. These interspecies variations are consistent with the presence of different and more diverse symbiont assemblages in A. lessonii compared with A. gibbosa. This study demonstrates the importance of considering symbiont diversity in the assessment of intra- and interspecific variations in stress responses in LBFs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson J, US DOC, NOAA, NOS, NOMS, Florida Keys National Marine Sanctuary (2011) Continuous bottom temperature measurements in strategic areas of the Florida reef tract at Tennessee Reef, 2004-2006; NODC Accession 0014272, National Oceanographic Data Center, NOAA. Dataset accessed 23/01/2017

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • Baker RD, Hallock P, Moses EF, Williams DE, Ramirez A (2009) Larger foraminifers on the Florida Reef Tract, USA: Distribution patterns on reef-rubble habitats. J Foraminifer Res 39:267–277

    Article  Google Scholar 

  • Barnes KH (2016) Diversity and distribution of diatom endosymbionts in Amphistegina spp. (Foraminifera) based on molecular and morphological techniques. Ph.D. thesis, University of South Florida

  • Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: Does host genotype limit phenotypic plasticity? Mol Ecol 19:1705–1720

    Article  PubMed  CAS  Google Scholar 

  • Bergman KC, Öhman MC (2001) Coral reef structure at Zanzibar Island, Tanzania. Mar Sci Dev Tanzania East Africa Proc 20th Anniv Conf Adv Mar Sci Tanzania 28:263–275

  • Bernhard JM (2000) Distinguishing live from dead foraminifera: Methods review and proper applications. Micropaleontology 46:38–46

    Google Scholar 

  • Boyd PW, Cornwall CE, Davison A, Doney SC, Fourquez M, Hurd CL, Lima ID, McMinn A (2016) Biological responses to environmental heterogeneity under future ocean conditions. Glob Chang Biol 22:2633–2650

    Article  PubMed  Google Scholar 

  • Cooper TF, Gilmour JP, Fabricius KE (2009) Bioindicators of changes in water quality on coral reefs: Review and recommendations for monitoring programmes. Coral Reefs 28:589–606

    Article  Google Scholar 

  • Doo SS, Hamylton S, Byrne M (2012) Reef-scale assessment of intertidal large benthic foraminifera populations on One Tree Island, Great Barrier Reef and their future carbonate production in a warming ocean. Zool Stud 51:1298–1307

    CAS  Google Scholar 

  • Engel BE, Hallock P, Price RE, Pichler T (2015) Shell dissolution in larger benthic foraminifers exposed to pH and temperature extremes: Results from an in situ experiment. J Foraminifer Res 45:190–203

    Article  Google Scholar 

  • Fay SA, Weber MX, Lipps JH (2009) The distribution of Symbiodinium diversity within individual host foraminifera. Coral Reefs 28:717–726

    Article  Google Scholar 

  • Fujita K, Okai T, Hosono T (2014) Oxygen metabolic responses of three species of large benthic foraminifers with algal symbionts to temperature stress. PLoS One 9:e90304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garcia-Cuetos L, Pochon X, Pawlowski J (2005) Molecular evidence for host-symbiont specificity in soritid foraminifera. Protist 156:399–412

    Article  PubMed  CAS  Google Scholar 

  • Glez-Peña D, Gómez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D (2010) ALTER: Program-oriented conversion of DNA and protein alignments. Nucleic Acids Res 38:14–18

    Article  CAS  Google Scholar 

  • Green MR, Sambrook J (2012) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Hallock P (1999) Symbiont-bearing foraminifera. In: Louisiana SU (ed) Sen Gupta BK. Kluwer Academic Publishers, Modern foraminifera, pp 123–368

    Google Scholar 

  • Hallock P (2000) Symbiont-bearing foraminifera: Harbingers of global change? Micropaleontology 46:95–104

    Google Scholar 

  • Hallock P, Forward LB, Hansen HJ (1986) Influence of environment on the test shape of Amphistegina. J Foraminifer Res 16:224–231

    Article  Google Scholar 

  • Hallock P, Lidz BH, Cockey-Burkhard EM, Donnelly KB (2003) Foraminifera as bioindicators in coral reef assessment and monitoring: The FORAM Index. Environ Monit Assess 81:221–238

    Article  PubMed  Google Scholar 

  • Hallock P, Pomar L (2009) Cenozoic evolution of larger benthic foraminifers: Paleoceanographic evidence for changing habitats. Proc 11th Int Coral Reef Symp 1:16–20

  • Hallock P, Talge HK, Cockey EM, Muller RG (1995) A new disease in reef-dwelling foraminifera: Implications for coastal sedimentation. J Foraminifer Res 25:280–286

    Article  Google Scholar 

  • Hallock P, Williams DE, Toler SK, Fisher EM, Talge HK (2006) Bleaching in reef-dwelling foraminifers: Implications for reef decline. 10th Int Coral Reef Symp 1:729–737

  • Hammer Ø, Harper D, Ryan P (2001) PAST: Paleontological statistics software package.

  • Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S (2017) Coral reef ecosystems under climate change and ocean acidification. Front Mar Sci 4:158

    Article  Google Scholar 

  • Hohenegger J, Yordanova E, Nakano Y, Tatzreiter F (1999) Habitats of larger foraminifera on the upper reef slope of Sesoko Island, Okinawa, Japan. Mar Micropaleontol 36:109–168

    Article  Google Scholar 

  • Holzmann M, Berney C, Hohenegger J (2006) Molecular identification of diatom endosymbionts in nummulitid foraminifera. Symbiosis 42:93–101

    CAS  Google Scholar 

  • Hosono T, Fujita K, Kayanne H (2012) Estimating photophysiological condition of endosymbiont-bearing Baculogypsina sphaerulata based on the holobiont color represented in CIE L*a*b* color space. Mar Biol 159:2663–2673

    Article  CAS  Google Scholar 

  • Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2011) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120

    Article  Google Scholar 

  • IPCC (2013) Climate Change 2013: The physical science basis. Cambridge University Press, Cambridge, United Kingdom and New York

    Google Scholar 

  • Langer MR (2008) Assessing the contribution of foraminiferan protists to global ocean carbonate production. J Eukaryot Microbiol 55:163–169

    Article  PubMed  Google Scholar 

  • Langer MR, Hottinger L (2000) Biogeography of selected “larger” foraminifera. Micropaleontology 46:105–126

    Google Scholar 

  • Lee JJ (2006) Algal symbiosis in larger foraminifera. Symbiosis 42:63–75

    Google Scholar 

  • Leichter JJ, Helmuth B, Fischer AM (2006) Variation beneath the surface: Quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida. J Mar Res 64:563–588

    Article  Google Scholar 

  • Loeblich ARJ, Tappan H (1988) Foraminiferal genera and their classification. Van Nostrand Reinhold, New York

    Book  Google Scholar 

  • Marcus R, Peritz E, Gabriel K (1976) On closed testing procedures with special reference to ordered analysis of variance. Biometrika 63:655–660

    Article  Google Scholar 

  • Mendez-Ferrer N, Hallock P, Jones D (2018) Photochemical efficiencies of diatom symbionts in hospite in Amphistegina gibbosa (Foraminifera) across seasons in the Florida Keys, USA. J Foraminifer Res 48:4–16

    Google Scholar 

  • Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056

    Article  PubMed  Google Scholar 

  • Moberly RJ, Chamberlain T (1964) Hawaiian beach systems. Hawaii Inst Geophys Rep 64

  • Momigliano P, Uthicke S (2013) Symbiosis in a giant protist (Marginopora vertebralis, Soritinae): Flexibility in symbiotic partner ships along a natural temperature gradient. Mar Ecol Prog Ser 491:33–46

    Article  Google Scholar 

  • Moses EF, Hallock P, Fauth J (2017) Dynamics of larger benthic foraminiferal populations in the upper Florida Keys Reef Tract, USA: Comparisons with other coral reef bioindicators. In: Kathal PK, Nigam R, Talib A (eds) Micropaleontology and its applications. Scientific Publisher, New Delhi, pp 15–39

    Google Scholar 

  • Muhando CA (2002) Seawater temperature on shallow reefs off Zanzibar Town, Tanzania. In: Lindén O, Souter D, Wilhelsson D, Obura D (eds) Coral reef degradation in the Indian Ocean - status report 2002. CORDIO, pp 40–46

  • Muller PH (1976) Sediment production by shallow-water, benthic foraminifera at selected sites around Oahu, Hawaii. Marit Sediments Spec Publ 1:263–265

    Google Scholar 

  • Narayan GR, Westphal H (2016) Are Zanzibar’s reefs undergoing ecological change? Foraminifera bio-indicators for monitoring and assessment of reef ecosystems in the west Indian Ocean. Proc 13th Int Coral Reef Symp 1:197–205

  • Notredame C, Higgins DG, Heringa J (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217

    Article  PubMed  CAS  Google Scholar 

  • Oliver TA, Palumbi SR (2011a) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440

    Article  Google Scholar 

  • Oliver TA, Palumbi SR (2011b) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241–250

    Article  Google Scholar 

  • Pochon X, Garcia-Cuetos L, Baker AC, Castella E, Pawlowski J (2007) One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26:867–882

    Article  Google Scholar 

  • Prazeres M, Ainsworth T, Roberts TE, Pandolfi JM, Leggat W (2017a) Symbiosis and microbiome flexibility in calcifying benthic foraminifera of the Great Barrier Reef. Microbiome 5:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Prazeres M, Roberts TE, Pandolfi JM, Schmaljohann R, Hoegh-Guldberg O (2017b) Variation in sensitivity of large benthic Foraminifera to the combined effects of ocean warming and local impacts. Sci Rep 92:45227

    Article  CAS  Google Scholar 

  • Prazeres M, Uthicke S, Pandolfi JM (2015) Ocean acidification induces biochemical and morphological changes in the calcification process of large benthic foraminifera. Proc R Soc B 282:8–11

    Article  CAS  Google Scholar 

  • Prazeres M, Uthicke S, Pandolfi JM (2016) Influence of local habitat on the physiological responses of large benthic foraminifera to temperature and nutrient stress. Sci Rep 6:21936

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing.

  • Safaie A, Silbiger NJ, McClanahan TR, Pawlak G, Barshis DJ, Hench JL, Rogers JS, Williams GJ, Davis KA (2018) High frequency temperature variability reduces the risk of coral bleaching. Nat Commun 9:1671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt C, Morard R, Prazeres M, Barak H, Kucera M (2016a) Retention of high thermal tolerance in the invasive foraminifera Amphistegina lobifera from the Eastern Mediterranean and the Gulf of Aqaba. Mar Biol 163:228

    Article  Google Scholar 

  • Schmidt C, Titelboim D, Brandt J, Herut B, Abramovich S, Almogi-Labin A, Kucera M (2016b) Extremely heat tolerant photo-symbiosis in a shallow marine benthic foraminifera. Sci Rep 6:30930

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shaghude YW, Wannäs KO, Mahongo SB (2002) Biogenic assemblage and hydrodynamic settings of the tidally dominated reef platform sediments of the Zanzibar Channel. West Indian Ocean J Mar Sci 1:107–116

    Google Scholar 

  • Stuhr M, Reymond CE, Rieder V, Hallock P, Westphal H, Kucera M (2017) Reef calcifiers are adapted to episodic heat stress but vulnerable to sustained warming. PLoS One 12:e0179753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Talge HK, Hallock P (2003) Ultrastructural responses in field-bleached and experimentally stressed Amphistegina gibbosa (Class Foraminifera). J Eukaryot Microbiol 50:324–333

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis. Mol Biol Evol 30:2725–2729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • ter Kuile B, Erez J (1984) In situ growth rate experiments on the symbiont-bearing foraminifera Amphistegina lobifera and Amphisorus hemprechii. J Foraminifer Res 14:262–276

    Article  Google Scholar 

  • Uthicke S, Altenrath C (2010) Water column nutrients control growth and C: N ratios of symbiont-bearing benthic foraminifera on the Great Barrier Reef, Australia. Limnol Oceanogr 55:1681–1696

    Article  CAS  Google Scholar 

  • van Dam JW, Negri AP, Mueller JF, Uthicke S (2012) Symbiont-specific responses in foraminifera to the herbicide diuron. Mar Pollut Bull 65:373–383

    Article  PubMed  CAS  Google Scholar 

  • Walker RA, Hallock P, Torres JJ, Vargo GA (2011) Photosynthesis and respiration in five species of benthic foraminifera that host algal endosymbionts. J Foraminifer Res 41:314–325

    Article  Google Scholar 

  • Weinmann AE, Langer MR (2017) Diverse thermotolerant assemblages of benthic foraminiferal biotas from tropical tide and rock pools of eastern Africa. Rev Micropaléontologie 60:511–523

    Article  Google Scholar 

  • Yamano H, Miyajima T, Koike I (2000) Importance of foraminifera for the formation and maintenance of a coral sand cay: Green Island, Australia. Coral Reefs 19:51–58

    Article  Google Scholar 

Download references

Acknowledgements

This project was funded by the Leibniz Association (SAW-2014-ISAS-2) awarded to HW and JR. Sampling in the Florida Keys was conducted under the Research Permit No. FKNMS-2015-026. Samples from Zanzibar were collected under the Revolutionary Government of Zanzibar 434 (S.M.Z.) Research Permit No. 0671.

Author information

Authors and Affiliations

  1. Biogeochemistry and Geology, Leibniz Centre for Tropical Marine Research (ZMT), 28359, Bremen, Germany

    Marleen Stuhr, Achim Meyer, Claire E. Reymond, Gita R. Narayan & Hildegard Westphal

  2. Department of Statistics, TU Dortmund University, 44221, Dortmund, Germany

    Vera Rieder & Jörg Rahnenführer

  3. MARUM, Center for Marine Environmental Sciences, University of Bremen, 28359, Bremen, Germany

    Michal Kucera

  4. Department of Geosciences, University of Bremen, 28359, Bremen, Germany

    Hildegard Westphal

  5. Institute of Marine Sciences, University of Dar es Salaam, P.O. Box 668, Zanzibar, Tanzania

    Christopher A. Muhando

  6. College of Marine Science, University of South Florida, St. Petersburg, FL, 33705, USA

    Pamela Hallock

Authors
  1. Marleen Stuhr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Achim Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claire E. Reymond
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gita R. Narayan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vera Rieder
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jörg Rahnenführer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michal Kucera
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hildegard Westphal
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Christopher A. Muhando
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Pamela Hallock
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marleen Stuhr.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Topic Editor Dr. Mark R. Patterson

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2664 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stuhr, M., Meyer, A., Reymond, C.E. et al. Variable thermal stress tolerance of the reef-associated symbiont-bearing foraminifera Amphistegina linked to differences in symbiont type. Coral Reefs 37, 811–824 (2018). https://doi.org/10.1007/s00338-018-1707-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-018-1707-9

Keywords

Search

Navigation