Osmotrophy in modular Ediacara organisms
Open accessAbstract
The Ediacara biota include macroscopic, morphologically complex soft-bodied organisms that appear globally in the late Ediacaran Period (575-542 Ma). The physiology, feeding strategies, and functional morphology of the modular Ediacara organisms (rangeomorphs and erniettomorphs) remain debated but are critical for understanding their ecology and phylogeny. Their modular construction triggered numerous hypotheses concerning their likely feeding strategies, ranging from micro-to-macrophagus feeding to photoautotrophy to osmotrophy. Macrophagus feeding in rangeomorphs and erniettomorphs is inconsistent with their lack of oral openings, and photoautotrophy in rangeomorphs is contradicted by their habitats below the photic zone. Here, we combine theoretical models and empirical data to evaluate the feasibility of osmotrophy, which requires high surface area to volume (SA/V) ratios, as a primary feeding strategy of rangeomorphs and erniettomorphs. Although exclusively osmotrophic feeding in modern ecosystems is restricted to microscopic bacteria, this study suggests that (i) fractal branching of rangeomorph modules resulted in SA/V ratios comparable to those observed in modern osmotrophic bacteria, and (ii) rangeomorphs, and particularly erniettomorphs, could have achieved osmotrophic SA/V ratios similar to bacteria, provided their bodies included metabolically inert material. Thus, specific morphological adaptations observed in rangeomorphs and erniettomorphs may have represented strategies for overcoming physiological constraints that typically make osmotrophy prohibitive for macroscopic life forms. These results support the viability of osmotrophic feeding in rangeomorphs and erniettomorphs, help explain their taphonomic peculiarities, and point to the possible importance of earliest macroorganisms for cycling dissolved organic carbon that may have been present in abundance during Ediacaran times.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The fractal organisation of early fronds such as Rangea and their large surface area may imply that these organisms fed, at least partly, via absorption of dissolved organic carbon (DOC) from seawater.
“An additional point in favour of their interpretation as stem-group metazoans is the fractal organisation of the early fronds such as Rangea ; a large surface area (especially given the lack of any other feeding structures) may imply that these organisms fed, at least partly, via absorption of DOC from the sea water”
From The origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution (2017) · cites this paper as Laflamme, Xiao & Kowalewski, 2009
The advantage of gastric pouches was extension of the internal resorptive surface, which would have intensified body physiology and probably allowed the maintenance and movement of larger body forms.
“The obvious advantage of this innovation was the extension of the internal surface, i.e. the surface of the resorptive epithelium, and would have intensified body physiology and probably allowed the maintenance and movement of larger body forms [163]”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [163]
The open-pipe model would predict preservation of some specimens with sediment infilling the distal open ends of the branches, but such specimens are not currently known.
“Secondly, the alternative possibility that the rangeomorph branches were open to the water column at one end-in the manner of an open pipe (raised by Laflamme et al., 2009)-would predict preservation of some specimens with sediment infilling the distal (open) ends of the branches; such specimens are not currently known.”
From Remarkable insights into the paleoecology of the Avalonian Ediacaran macrobiota (2015) · cites this paper as Laflamme et al., 2009
Fractofusus grew by both addition and inflation of primary branches.
“Similarly, Fractofusus appears to have grown by both addition and inflation of primary branches (Laflamme et al., 2009), with this combination of accretion and inflation mirrored by seemingly unrelated tubular body fossils later in the Ediacaran Period (e.g.Wutubus, Z. Chen et al., 2014).”
From Remarkable insights into the paleoecology of the Avalonian Ediacaran macrobiota (2015) · cites this paper as Laflamme et al., 2009
For the erniettomorph Pteridinium, the required inert material equates to around 98.72% of its volume.
“For the erniettomorph Pteridinium, this equates to around 98.72% of its volume.”
From Remarkable insights into the paleoecology of the Avalonian Ediacaran macrobiota (2015) · cites this paper as Laflamme et al., 2009
The extent of hollowness required for SA/V ratios to be consistent with those modelled for modern osmotrophs seems unlikely on a number of grounds.
“Although there is evidence for some degree of 'hollowness' in certain Ediacaran organisms (Narbonne et al., 1997;Laflamme et al., 2009;Vickers-Rich et al., 2013), the extent required for SA/V ratios to be consistent with those modelled for modern osmotrophs seems unlikely on a number of grounds.”
From Remarkable insights into the paleoecology of the Avalonian Ediacaran macrobiota (2015) · cites this paper as Laflamme et al., 2009
For SA/V ratios of modelled Ediacaran organisms Pteridinium and Fractofusus to be consistent with those of extant osmotrophic bacteria, their metabolically active layer cannot exceed 0.01 mm in thickness and the remainder must be metabolically inert material such as sediment or fluid.
“In order for SA/V ratios of modelled Ediacaran organisms (Pteridinium and Fractofusus) to be consistent with those of extant osmotrophic bacteria, their metabolically active layer cannot exceed 0.01 mm in thickness; the remainder of the organism must be filled with metabolically inert material such as sediment or fluid (Laflamme et al., 2009).”
From Remarkable insights into the paleoecology of the Avalonian Ediacaran macrobiota (2015) · cites this paper as Laflamme et al., 2009
Cites
A General Model for the Origin of Allometric Scaling Laws in Biology
West, G. B., Brown, J. H., & Enquist, B. J. (1997) · Science · doi:10.1126/science.276.5309.122 · Cited by 5,016 · see citing works
Oxidation of the Ediacaran Ocean
Fike, D. A., Grotzinger, J. P., Pratt, L. M., & Summons, R. E. (2006) · Nature · doi:10.1038/nature05345 · Cited by 989 · see citing works
The Ediacara biota: Neoproterozoic origin of animals and their ecosystems
Narbonne, G. M. (2005) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.33.092203.122519 · Cited by 714 · see citing works
On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota
Xiao, S., & Laflamme, M. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.07.015 · Cited by 543 · see citing works
Self-citationEdiacaran biota: the dawn of animal life in the shadow of giant protists
SEILACHER, A., GRAZHDANKIN, D., & LEGOUTA, A. (2003) · Paleontological Research · doi:10.2517/prpsj.7.43 · Cited by 290 · see citing works
Yahel, G., Sharp, J. H., Marie, D., Häse2, C., & Genin, A. (2003) · Limnology and Oceanography · doi:10.4319/lo.2003.48.1.0141 · Cited by 270 · see citing works
Modular Construction of Early Ediacaran Complex Life Forms
Narbonne, G. M. (2004) · Science · doi:10.1126/science.1099727 · Cited by 269 · see citing works
Wood, D. A., Dalrymple, R. W., Narbonne, G. M., Gehling, J. G., & Clapham, M. E. (2003) · Canadian Journal of Earth Sciences · doi:10.1139/e03-048 · Cited by 159 · see citing works
Assemblage palaeoecology of the Ediacara biota: The unabridged edition?
Droser, M. L., Gehling, J. G., & Jensen, S. R. (2006) · Palaeogeography, Palaeoclimatology, Palaeoecology · doi:10.1016/j.palaeo.2005.12.015 · Cited by 124 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Multiple Origins of Complex Multicellularity
Knoll, A. H. (2011) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.031208.100209 · Cited by 562 · see citing works
The end of the Ediacara biota: Extinction, biotic replacement, or Cheshire Cat?
Laflamme, M., Darroch, S. A. F., Tweedt, S. M., Peterson, K. J., & Erwin, D. H. (2013) · Gondwana Research · doi:10.1016/j.gr.2012.11.004 · Cited by 300 · see citing works
Self-citationThe origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution
Budd, G. E., & Jensen, S. (2017) · Biological Reviews · doi:10.1111/brv.12239 · Cited by 240 · see citing works
“Bond, C. & Harris, A. K. (1988).”
BackgroundInfluentialSperling, E. A., & Vinther, J. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00404.x · Cited by 194 · see citing works
Patterns of evolution of the Ediacaran soft-bodied biota
Grazhdankin, D. (2014) · Journal of Paleontology · doi:10.1666/13-072 · Cited by 175 · see citing works
The Rise of Animals in a Changing Environment: Global Ecological Innovation in the Late Ediacaran
Droser, M. L., Tarhan, L. G., & Gehling, J. G. (2017) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-063016-015645 · Cited by 172 · see citing works
Remarkable insights into the paleoecology of the Avalonian Ediacaran macrobiota
Liu, A. G., Kenchington, C. G., & Mitchell, E. G. (2015) · Gondwana Research · doi:10.1016/j.gr.2014.11.002 · Cited by 157 · see citing works
Ecological drivers of the Ediacaran-Cambrian diversification of Metazoa
Erwin, D. H., & Tweedt, S. (2012) · Evolutionary Ecology · doi:10.1007/s10682-011-9505-7 · Cited by 152 · see citing works
The Latest Ediacaran Wormworld Fauna: Setting the Ecological Stage for the Cambrian Explosion
Schiffbauer, J. D., Huntley, J. W., O’Neil, G. R., Darroch, S. A. F., Laflamme, M., & Cai, Y. (2016) · GSA Today · doi:10.1130/gsatg265a.1 · Cited by 137 · see citing works
Self-citationGastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112 · see citing works
Affirming life aquatic for the Ediacara biota in China and Australia
Xiao, S., Droser, M., Gehling, J. G., Hughes, I. V., Wan, B., Chen, Z., & Yuan, X. (2013) · Geology · doi:10.1130/g34691.1 · Cited by 115 · see citing works
Self-citationControls on the evolution of Ediacaran metazoan ecosystems: A redox perspective
Bowyer, F., Wood, R. A., & Poulton, S. W. (2017) · Geobiology · doi:10.1111/gbi.12232 · Cited by 112 · see citing works
SPERLING, E. A., PETERSON, K. J., & LAFLAMME, M. (2011) · Geobiology · doi:10.1111/j.1472-4669.2010.00259.x · Cited by 112 · see citing works
Self-citationDeep-water Ediacaran fossils from northwestern Canada: taphonomy, ecology, and evolution
Narbonne, G. M., Laflamme, M., Trusler, P. W., Dalrymple, R. W., & Greentree, C. (2014) · Journal of Paleontology · doi:10.1666/13-053 · Cited by 103 · see citing works
Darroch, S. A. F., Cribb, A. T., Buatois, L. A., Germs, G. J. B., Kenchington, C. G., Smith, E. F., Mocke, H., O’Neil, G. R., Schiffbauer, J. D., Maloney, K. M., et al. (2021) · Earth-Science Reviews · doi:10.1016/j.earscirev.2020.103435 · Cited by 102 · see citing works
Self-citationThe rise and early evolution of animals: where do we stand from a trace-fossil perspective?
Mángano, M. G., & Buatois, L. A. (2020) · Interface Focus · doi:10.1098/rsfs.2019.0103 · Cited by 99 · see citing works
Early Cambrian oxygen minimum zone-like conditions at Chengjiang
Hammarlund, E. U., Gaines, R. R., Prokopenko, M. G., Qi, C., Hou, X.-G., & Canfield, D. E. (2017) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2017.06.054 · Cited by 92 · see citing works
Population structure of the oldest known macroscopic communities from Mistaken Point, Newfoundland
Darroch, S. A. F., Laflamme, M., & Clapham, M. E. (2013) · Paleobiology · doi:10.1666/12051 · Cited by 91 · see citing works
Reconstructing <i>Rangea</i>: new discoveries from the Ediacaran of southern Namibia
Vickers-Rich, P., Ivantsov, A. Y., Trusler, P. W., Narbonne, G. M., Hall, M., Wilson, S. A., Greentree, C., Fedonkin, M. A., Elliott, D. A., Hoffmann, K. H., et al. (2013) · Journal of Paleontology · doi:10.1666/12-074r.1 · Cited by 79 · see citing works
Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic body plan
Hoyal Cuthill, J. F., & Conway Morris, S. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408542111 · Cited by 73 · see citing works
Environmental disturbance, resource availability, and biologic turnover at the dawn of animal life
Muscente, A. D., Boag, T. H., Bykova, N., & Schiffbauer, J. D. (2018) · Earth-Science Reviews · doi:10.1016/j.earscirev.2017.11.019 · Cited by 72 · see citing works
Ghisalberti, M., Gold, D. A., Laflamme, M., Clapham, M. E., Narbonne, G. M., Summons, R. E., Johnston, D. T., & Jacobs, D. K. (2014) · Current Biology · doi:10.1016/j.cub.2013.12.017 · Cited by 70 · see citing works
Self-citationThe utility of height for the Ediacaran organisms of Mistaken Point
Mitchell, E. G., & Kenchington, C. G. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0591-6 · Cited by 60 · see citing works
Lenton, T. M., & Daines, S. J. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170156 · Cited by 55 · see citing works
Laflamme, M., Flude, L. I., & Narbonne, G. M. (2012) · Journal of Paleontology · doi:10.1666/11-044.1 · Cited by 51 · see citing works
Evans, S. D., Diamond, C. W., Droser, M. L., & Lyons, T. W. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170148 · Cited by 51 · see citing works
Was the Ediacaran–Cambrian radiation a unique evolutionary event?
Erwin, D. H. (2015) · Paleobiology · doi:10.1017/pab.2014.2 · Cited by 40 · see citing works
Dececchi, T. A., Narbonne, G. M., Greentree, C., & Laflamme, M. (2017) · Paleobiology · doi:10.1017/pab.2016.54 · Cited by 40 · see citing works
Self-citationOxygen and Early Animal Evolution
Xiao, S. (2014) · Treatise on Geochemistry · doi:10.1016/b978-0-08-095975-7.01310-3 · Cited by 31 · see citing works
Self-citationMason, S. J., Narbonne, G. M., Dalrymple, R. W., & O'Brien, S. J. (2013) · Canadian Journal of Earth Sciences · doi:10.1139/cjes-2012-0099 · Cited by 27 · see citing works
- Authors
- Laflamme, M., Xiao, S., & Kowalewski, M.
- Affiliations
- Virginia Tech (US)
- Corresponding author
- Laflamme, Marc
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-08-25
- Volume
- 106
- Issue
- 34
- Pages
- 14438-14443
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2732876
- OpenAlex
- W2072241937
- Cited by
- 180
- References
- 9
- Citations by year
- 2026: 3 · 2025: 25 · 2024: 8 · 2023: 7 · 2022: 8 · 2021: 16 · 2020: 14 · 2019: 3 · 2018: 12 · 2017: 14 · 2016: 10 · 2015: 14 · 2014: 12 · 2013: 12 · 2012: 10
- FWCI
- 5.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Evolutionary Biology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- Ediacara biota, osmotrophy, modular organisms, surface-to-volume ratio, fractal branching, feeding strategies, taphonomy
- MeSH terms
- Animals, Bacteria, Computer Simulation, Dinoflagellida, Biological Evolution, Fossils, Invertebrates, Models, Theoretical, Ecosystem
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
