Contributions of Trimorphic Life Cycles to Dispersal and Evolutionary Trends in Large Benthic Foraminifers

Pamela Hallock , Claire E. Reymond

Journal of Earth Science ›› 2022, Vol. 33 ›› Issue (6) : 1425 -1433.

PDF
Journal of Earth Science ›› 2022, Vol. 33 ›› Issue (6) : 1425 -1433. DOI: 10.1007/s12583-022-1707-0
Regular Article

Contributions of Trimorphic Life Cycles to Dispersal and Evolutionary Trends in Large Benthic Foraminifers

Author information +
History +
PDF

Abstract

The basic life cycle of Foraminifera has long been recognized as alternation between sexual and asexual generations; a common modification is several successive asexual generations. Production and release of flagellated gametes also has been documented as the basic sexual-reproductive mode in extant lineages. Research on population dynamics, local spatial distributions, and biogeography of Amphistegina spp. and Heterostegina depressa have been augmented by culture studies over the past 50 years, providing insights that have been widely used in paleoecological and paleoenvironmental interpretations. Hypotheses are proposed suggesting how stages in the life cycle might contribute to understanding biogeographic and evolutionary trends commonly observed in large benthic foraminifers. Recruitment of sexually-produced cryptobiotic propagules, followed by successive asexual generations (schizogeny), can potentially establish viable, locally-adapted populations within literally years, consistent with the concepts of both allopatric speciation and reticulate evolution associated with isolation and reconnection of local basins. The review concludes with the recommendation that future studies utilizing genomics, proteonomics, geochemistries, scanning technologies, and other approaches can promote greater understanding of both modern and fossil larger benthic foraminiferal lineages.

Keywords

Amphistegina / coiling ratio / diatom symbionts / Heterostegina depressa / propagule / schizogeny / life cycle

Cite this article

Download citation ▾
Pamela Hallock, Claire E. Reymond. Contributions of Trimorphic Life Cycles to Dispersal and Evolutionary Trends in Large Benthic Foraminifers. Journal of Earth Science, 2022, 33(6): 1425-1433 DOI:10.1007/s12583-022-1707-0

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Alve E, Goldstein S T. Resting Stage in Benthic Foraminiferal Propagules: A Key Feature for Dispersal? Evidence from Two Shallow-Water Species. Journal of Micropalaeontology, 2002, 21(1): 95-96.

[2]

Alve E, Goldstein S T. Propagule Transport as a Key Method of Dispersal in Benthic Foraminifera (Protista). Limnology and Oceanography, 2003, 48(6): 2163-2170.

[3]

Alve E, Goldstein S. Dispersal, Survival and Delayed Growth of Benthic Foraminiferal Propagules. Journal of Sea Research, 2010, 63(1): 36-51.

[4]

Amergian K, Beckwith S, Gfatter C, . Can Areas of High Alkalinity Freshwater Discharge Provide Potential Refugia for Marine Calcifying Organisms?. Journal of Foraminiferal Research, 2022, 52(1): 60-73.

[5]

Barnes K H. Diversity and Distribution of Diatom Endosymbionts in Amphistegina spp. (Foraminifera) Based on Molecular and Morphological Techniques: [Dissertation], 2016, Tampa: University of South Florida, 177

[6]

Briguglio A, Woger J, Wolfgring E, . Kitazato H, Bernhard J M, . Changing Investigation Perspectives: Methods and Applications of Computed Tomography on Larger Benthic Foraminifera. Approaches to Study Living Foraminifera: Collection, Maintenance and Experimentation. Environmental Science and Engineering, 2014, Tokyo: Springer, 55-70.

[7]

Dämmer L K, van Dijk I, de Nooijer L D, . Temperature Impact on Magnesium Isotope Fractionation in Cultured Foraminifera. Frontiers in Earth Science, 2021, 9: 642256

[8]

Dettmering C, Röttger R, Hohenegger J, . The Trimorphic Life Cycle in Foraminifera: Observations from Cultures Allow New Evaluation. European Journal of Protistology, 1998, 34(4): 363-368.

[9]

Dubey R, Saraswat R, Nigam R. Dwarf Foraminifera off Kerala, India: A Response to Mudbank Formation. Journal of the Palaeontological Society of India, 2018, 63(1): 81-90

[10]

Fujita K, Kanda Y, Hosono T. Light is an Important Limiting Factor for the Vertical Distribution of the Largest Extant Benthic Foraminifer Cycloclypeus carpenteri. Journal of Earth Science, 2022, 33(6): xxx-xxx

[11]

Fryxell G R. Survival Strategies of the Algae, 1983, Cambridge: Cambridge University Press, 144

[12]

Goldstein S T. Gametogenesis and the Antiquity of Reproductive Patterns in the Foraminiferida. Journal of Foraminiferal Research, 1997, 27 319-328.

[13]

Goldstein S T. Sen Gupta B K. Foraminifera: A Biological Overview. Modern Foraminifera, 1999, Dordrecht: Kluwer, 37-55.

[14]

Grell K G. Protozoology, 1973, Berlin: Springer-Verlag, 556

[15]

Guastella R, Marchini A, Caruso A, . “Hidden Invaders” Conquer the Sicily Channel and Knock on the Door of the Western Mediterranean Sea. Estuarine, Coastal and Shelf Science, 2019, 225: 106234

[16]

Guastella R, Mancin N, Marchini A, . Reconstructing Bioinvasion Dynamics through Micropaleontologic Analysis Highlights the Role of Temperature Change as a Driver of Alien Foraminifera Invasion. Frontiers in Marine Science, 2021, 8 675807

[17]

Hallock P. Trends in Test Shape in Large, Symbiont-Bearing Foraminifera. Journal of Foraminiferal Research, 1979, 9(1): 61-69.

[18]

Hallock P. Production of Carbonate Sediments by Selected Large Benthic Foraminifera on Two Pacific Coral Reefs. Journal of Sedimentary Petrology, 1981, 51(2): 467-474

[19]

Hallock P. Evolution and Extinction in Larger Foraminifera. Third North American Paleontological Convention Proceedings, 1982, 1 221-225.

[20]

Hallock P. Distribution of Selected Species of Living Algal Symbiont-Bearing Foraminifera on Two Pacific Coral Reefs. Journal of Foraminiferal Research, 1984, 14(4): 250-261.

[21]

Hallock P. Why are Larger Foraminifera Large?. Paleobiology, 1985, 11(2): 195-208.

[22]

Hallock P. Fluctuations in the Trophic Resource Continuum: A Factor in Global Diversity Cycles?. Paleoceanography, 1987, 2(5): 457-471.

[23]

Hallock P. Notes on Coiling Direction in Trochospiral Benthic Foraminifera. Revue de Paléobiologie, 1988, 2(Spec.): 799-802

[24]

Hallock P, Larsen A R. Coiling Direction in Amphistegina. Marine Micropaleontology, 1979, 4: 33-44.

[25]

Hallock P, Seddighi M. Why did some Larger Benthic Foraminifera Become so Large and Flat?. Sedimentology, 2022, 69(1): 74-87.

[26]

Hallock P, Forward L B, Hansen H J. Influence of Environment on the Test Shape of Amphistegina. Journal of Foraminiferal Research, 1986, 16(3): 224-231.

[27]

Hallock, P., Talge, H. K., Smith, K., et al., 1993. Bleaching in a Reef-Dwelling Foraminifer, Amphistegina gibbosa. Proceedings, 7th International Coral Reef Symposium, Guam. 42–47

[28]

Hallock P, Talge H K, Cockey E M, . A New Disease in Reef-Dwelling Foraminifera; Implications for Coastal Sedimentation. Journal of Foraminiferal Research, 1995, 25(3): 280-286.

[29]

Harney J N, Hallock P, Talge H K. Observations on a Trimorphic Life Cycle in Amphistegina gibbosa Populations from the Florida Keys. Journal of Foraminiferal Research, 1998, 28(2): 141-147.

[30]

Hjulstrom F. Studies of the Morphological Activity of Rivers as Illustrated by the River Fyris. Bull. Geol. Inst. Uppsala, 1935, 25: 221-527.

[31]

Hottinger L. Illustrated Glossary of Terms Used in Foraminiferal Research. Notebooks on Geology, Brest, Memoir, 2006, 2: 1-126.

[32]

Humphreys A, Riegl B, Reymond C, . Shallow-Water Benthic Foraminifera of the Galápagos Archipelago: Ecologically Sensitive Carbonate Producers in an Atypical Tropical Oceanographic Setting. Journal of Foraminiferal Research, 2019, 49(1): 48-65

[33]

Humphreys A F, Halfar J, Rivera F, . Variable El Niño-Southern Oscillation Influence on Biofacies Dynamics of Eastern Pacific Shallow-Water Carbonate Systems. Geology, 2016, 44(7): 571-574.

[34]

Kenigsberg C, Titelboim D, Ashckenazi-Polivoda S, . The Combined Effects of Rising Temperature and Salinity may Halt the Future Proliferation of Symbiont-Bearing Foraminifera as Ecosystem Engineers. Science of the Total Environment, 2022, 806(P2): 150581

[35]

Langer M R, Weinmann A E, Lotters S, . “Strangers” in Paradise: Modeling the Biogeographic Range Expansion of the Foraminifera Amphistegina in the Mediterranean Sea. Journal of Foraminiferal Research, 2012, 42 3 234-244.

[36]

Lee J J. Fine Structure of the Rhodophycean Porphyridium purpureum in situ in Peneroplis pertusus (Forskal) and P. acicularis (Batsch) and in Axenic Culture. Journal of Foraminiferal Research, 1990, 20(2): 162-169.

[37]

Lee J J. Seckbach J, Kociolek J P. Diatoms as Endosymbionts. The Diatom World, 2011, Netherlands: Springer, 437-464.

[38]

Lee J J, McEnery M E, Shilo M, . Isolation and Cultivation of Diatom Symbionts from Larger Foraminifera (Protozoa). Nature, 1979, 280(5717): 57-58.

[39]

Lee J J, Morales J, Symons A, . Diatom Symbionts in Larger Foraminifera from Caribbean Hosts. Marine Micropaleontology, 1995, 26(1/2/3/4): 99-105.

[40]

Leutenegger S. Reproduction Cycles of Larger Foraminifera and Depth Distribution of Generations. Utrecht Micropaleontol. Bull., 1977, 15: 27-34.

[41]

Lister J J. Contributions to the Life-History of the Foraminifera. Philosoph. Transact. Royal Soc. London, Ser. B, 1896, 186: 401-453.

[42]

MacArthur R H, Wilson E O. The Theory of Island Biogeography, 1967, Princeton: Princeton University Press, 203

[43]

Mayr E. Animal Species and Evolution, 1963, Cambridge: Harvard University Press, 515

[44]

Meng M, Yu K F, Hallock P, . Distribution of Recent Foraminifera as Depositional Indicators in Yongle Atoll, Xisha Islands, South China Sea. Marine Micropaleontology, 2020, 158: 101880

[45]

Morard R, Vollmar N M, Greco M, . Unassigned Diversity of Planktonic Foraminifera from Environmental Sequencing Revealed as Known but Neglected Species. PLoS One, 2019, 14(3): e0213936

[46]

Muller P H. Sediment Production and Population Biology of the Benthic Foraminifer Amphistegina madagascariensis. Limnology and Oceanography, 1974, 19 5 802-809.

[47]

Narayan G R, Reymond C E, Stuhr M, . Response of Large Benthic Foraminifera to Climate and Local Changes: Implications for Future Carbonate Production. Sedimentology, 2022, 69(1): 121-161.

[48]

Omana L, Alencaster G, Torres Hernandez J R, . Morphological Abnormalities and Dwarfism in Maastrichtian Foraminifera from the Cárdenas Formation, Valles-San Luis Potosí, Mexico. Boletin de la Sociedad Geologica Mexicana, 2012, 64(3): 305-318.

[49]

Parker A H, Wilkinson S W, Ton J. Epigenetics: A Catalyst of Plant Immunity against Pathogens. The New Phytologist, 2022, 233(1): 66-83.

[50]

Parker J H, Gischler E. Modern Foraminiferal Distribution and Diversity in Two Atolls from the Maldives, Indian Ocean. Marine Micropaleontology, 2011, 78(1): 30-49.

[51]

Prazeres M, Ainsworth T, Roberts T E, . Symbiosis and Microbiome Flexibility in Calcifying Benthic Foraminifera of the Great Barrier Reef. Microbiome, 2017, 5(1): 38

[52]

Prazeres M, Morard R, Roberts T E, . High Dispersal Capacity and Biogeographic Breaks Shape the Genetic Diversity of a Globally Distributed Reef-Dwelling Calcifier. Ecology and Evolution, 2020, 10 12 5976-5989.

[53]

Prazeres M, Roberts T E, Ramadhani S F, . Diversity and Flexibility of Algal Symbiont Community in Globally Distributed Larger Benthic Foraminifera of the Genus Amphistegina. BMC Microbiology, 2021, 21(1): 243

[54]

Remin Z, Cyglicki M, Barski M, . The K-Pg Boundary Section at Nasilow, Poland: Stratigraphic Reassessment Based on Foraminifers, Dinoflagellate Cysts and Palaeomagnetism. Geological Quarterly, 2021, 65 3 45

[55]

Renema W. Terrestrial Influence as a Key Driver of Spatial Variability in Large Benthic Foraminiferal Assemblage Composition in the Central Indo-Pacific. Earth-Science Reviews, 2018, 177 514-544.

[56]

Reymond C E, Patel F, Uthicke S. Stable Adult Growth but Reduced Asexual Fecundity in Marginopora vertebralis, under Global Climate Change Scenarios. Journal of Earth Science, 2022, 33(6): xxx-xxx

[57]

Reymond C E, Zihrul K, Halfar J, . Heterozoan Carbonates from the Equatorial Rocky Reefs of the Galápagos Archipelago. Sedimentology, 2016, 63 940-958.

[58]

Ross B, Hallock P. Dormancy in the Foraminifera: A Review. Journal of Foraminiferal Research, 2016, 46(4): 358

[59]

Röttger R. Die Kultur von Heterostegina depressa (Foraminifera: Nummulitidae). Marine Biology, 1972, 15 2 150-159.

[60]

Röttger R. Analyse von Wachstumskurven von Heterostegina depressa (Foraminifera: Nummulitidae). Marine Biology, 1972, 17(3): 228-242.

[61]

Röttger R, Berger W H. Benthic Foraminifera: Morphology and Growth in Clone Cultures of Heterostegina depressa. Marine Biology, 1972, 15(1): 89-94.

[62]

Röttger R. Larger Foraminifera: Reproduction and Early Stages of Development in Heterostegina depressa. Marine Biology, 1974, 26(1): 5-12.

[63]

Röttger R. Heterostegina apogama, a New Holocene Nummulitid (Protozoa, Foraminiferida) from Hawaii. Journal of Foraminiferal Research, 1987, 17(3): 187-189.

[64]

Röttger R, Fladung M, Schmaljohann R, . A New Hypothesis; The So-Called Megalospheric Schizont of the Large Foraminifer, Heterostegina depressa d’Orbigny, 1826, is a Separate Species. Journal of Foraminiferal Research, 1986, 16: 141-149.

[65]

Röttger R, Krüger R, de Rijk S. Trimorphism in Foraminifera (Protozoa) -Verification of an Old Hypothesis. European Journal of Protistology, 1990, 25(3): 226-228.

[66]

Stuhr M, Blank-Landeshammer B, Reymond C E, . Disentangling Thermal Stress Responses in a Reef-Calcifier and Its Photosymbionts by Shotgun Proteomics. Scientific Reports, 2018, 8 3524

[67]

Stuhr M, Cameron L P, Blank-Landeshammer B, . Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios. Oceans, 2021, 2(2): 281-314.

[68]

Talge H K, Hallock P. Ultrastructural Responses in Field-Bleached and Experimentally Stressed Amphistegina gibbosa (Class Foraminifera). Journal of Eukaryotic Microbiology, 2003, 50(5): 324-333.

[69]

Veron J E N. Corals in Space and Time: The Biogeography and Evolution of the Scleractinia, 1995, Ithaca, NY: Cornell University Press, 321

[70]

Weiner A K M, Cerón-Romero M A, Yan Y, . Phylogenomics of the Epigenetic Toolkit Reveals Punctate Retention of Genes across Eukaryotes. Genome Biology and Evolution, 2020, 12(12): 2196-2210.

[71]

Weinmann A E, Goldstein S T, Triantaphyllou M V, . Effects of Sampling Site, Season, and Substrate on Foraminiferal Assemblages Grown from Propagule Banks from Lagoon Sediments of Corfu Island (Greece, Ionian Sea). PLoS One, 2019, 14(6): e0219015

[72]

Weinmann A E, Rödder D, Lötters S, . Heading for New Shores: Projecting Marine Distribution Ranges of Selected Larger Foraminifera. PLoS One, 2013, 8 4 e62182

[73]

Weinmann A E, Goldstein S T, Triantaphyllou M V, . Community Responses of Intertidal Foraminifera to pH Variations: A Culture Experiment with Propagules. Aquatic Ecology, 2021, 55 1 309-325.

[74]

Wilson E O. The Diversity of Life, 1992, Cambridge: Harvard University Press, 424

AI Summary AI Mindmap
PDF

150

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/