Marc Laflamme

The Cambrian conundrum: early divergence and later ecological success in the early history of animals.

Major animal clades evolved tens of millions of years before the widespread appearance of animal fossils. Diverse bilaterian clades emerged apparently within a few million years during the early Cambrian, and various environmental, developmental, and ecological causes have been proposed to explain this abrupt appearance. A compilation of the patterns of fossil and molecular diversification, comparative developmental data, and information on ecological feeding strategies indicate that the major animal clades diverged many tens of millions of years before their first appearance in the fossil record, demonstrating a macroevolutionary lag between the establishment of their developmental toolkits during the Cryogenian [(850 to 635 million years ago (Ma)], and the later ecological success of metazoans during the Ediacaran (635 to 541 Ma) and Cambrian (541 to 488 Ma) periods. We argue that this diversification involved new forms of developmental regulation, as well as innovations in networks of ecological interaction within the context of permissive environmental circumstances.

On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota

Ediacara fossils document an important evolutionary episode just before the Cambrian explosion and hold critical information about the early evolution of macroscopic and complex multicellular life. They also represent an enduring controversy in paleontology. How are the Ediacara fossils related to living animals? How did they live? Do they share any evolutionary patterns with other life forms? Recent developments indicate that Ediacara fossils epitomize a phylogenetically diverse biosphere, probably including animals, protists, algae, fungi and others. Their simple ecology is dominated by epibenthic osmotrophs, deposit feeders and grazers, but few if any predators. Their evolution started with an early morphospace expansion followed by taxonomic diversification within confined morphospace, and concluded by extinction of many taxa at the Ediacaran-Cambrian boundary.

Osmotrophy in modular Ediacara organisms

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.

RECONSTRUCTING A LOST WORLD: EDIACARAN RANGEOMORPHS FROM SPANIARD'S BAY, NEWFOUNDLAND

Abstract Ediacaran fronds at Spaniards Bay on the Avalon Peninsula of Newfoundland exhibit exquisite, three-dimensional preservation with morphological features less than 0.05 mm in width visible on the best preserved specimens. Most of the nearly 100 specimens are juvenile rangeomorphs, an extinct Ediacaran clade that numerically dominated the early evolution of complex multicellular life. Spaniards Bay rangeomorphs are characterized by cm-scale architectural elements exhibiting self-similar branching over several fractal scales that were used as modules in construction of larger structures. Four taxa of rangeomorph fronds are present – Avalofractus abaculus n. gen. et sp., Beothukis mistakensis Brasier and Antcliffe, Trepassia wardae (Narbonne and Gehling), and Charnia cf. C. masoni Ford. All of these taxa exhibit an alternate array of primary rangeomorph branches that pass off a central stalk or furrow that marks the midline of the petalodium. Avalofractus is remarkably self similar over at least four fractal scales, with each scale represented by double-sided rangeomorph elements that were constrained only at their attachment point with the higher-order branch and thus were free to rotate and pivot relative to other branches. Beothukis is similar in organization, but its primary branches show only one side of a typical rangeomorph element, probably due to longitudinal branch folding, and the position of the individual branches was moderately constrained. Trepassia shows only single-sided branches with both primary and secondary branches emanating from a central stalk or furrow; primary branches were capable of minor pivoting as reflected in bundles of secondary branches. Charnia shows only single-sided primary branches that branch from a zigzag central furrow and that were firmly constrained relative to each. This sequence provides a developmental linkage between Rangea-type and Charnia-type rangeomorphs. Avalonian assemblages show a wide array of rangeomorph constructions, but later Ediacaran assemblages contain a lower diversity of rangeomorphs represented mainly by well-constrained forms.

MORPHOMETRIC ANALYSIS OF THE EDIACARAN FROND CHARNIODISCUS FROM THE MISTAKEN POINT FORMATION, NEWFOUNDLAND

Abstract Charniodiscus is a leaf-shaped Ediacaran (terminal Neoproterozoic) fossil with a worldwide distribution, but the scarcity of complete specimens has previously hindered evaluation of its taxonomy and ecology. The presence of hundreds of complete (fronds with stem and disc attached) Charniodiscus specimens from the Avalon Zone of Newfoundland has allowed for detailed morphometric analysis of Charniodiscus specimens and permits determination of characteristics which vary with growth (e.g., stem length, frond width, and disc diameter) versus those that reflect taxonomic differences (e.g., number of primary segments, presence of a distal spine, shape ratios). This has led to the recognition of three species of Charniodiscus in the Mistaken Point biota, including numerous specimens of two new taxa, C. procerus n. sp. and C. spinosus n. sp., and rare specimens of the Australian species C. arboreus. C. procerus n. sp. and C. spinosus n. sp. represent similar, yet ecologically distinct forms of upper-level filter feeders with diverging feeding strategies in order to reduce the competition for resources. Ratio plots and principal components analyses (PCAs) confirm the existence of five (possibly six) morphologically distinct species of Charniodiscus worldwide.

Biotic replacement and mass extinction of the Ediacara biota

The latest Neoproterozoic extinction of the Ediacara biota has been variously attributed to catastrophic removal by perturbations to global geochemical cycles, ‘biotic replacement’ by Cambrian-type ecosystem engineers, and a taphonomic artefact. We perform the first critical test of the ‘biotic replacement’ hypothesis using combined palaeoecological and geochemical data collected from the youngest Ediacaran strata in southern Namibia. We find that, even after accounting for a variety of potential sampling and taphonomic biases, the Ediacaran assemblage preserved at Farm Swartpunt has significantly lower genus richness than older assemblages. Geochemical and sedimentological analyses confirm an oxygenated and non-restricted palaeoenvironment for fossil-bearing sediments, thus suggesting that oxygen stress and/or hypersalinity are unlikely to be responsible for the low diversity of communities preserved at Swartpunt. These combined analyses suggest depauperate communities characterized the latest Ediacaran and provide the first quantitative support for the biotic replacement model for the end of the Ediacara biota. Although more sites (especially those recording different palaeoenvironments) are undoubtedly needed, this study provides the first quantitative palaeoecological evidence to suggest that evolutionary innovation, ecosystem engineering and biological interactions may have ultimately caused the first mass extinction of complex life.

Experimental Formation of a Microbial Death Mask

Abstract This study represents a first attempt to observe soft-tissue decay in association with microbial mats, in order to recreate the death-mask model proposed for terminal Neoproterozoic Lagerstätten. This model explains the precipitation of authigenic iron sulfide minerals on, and around, decaying carcasses in association with microbial mats, cementing the sediment as a sole veneer and retaining the external morphology of the organism in relief on the upper and lower surface of coarse-grained sandy event beds. Although this model has been substantiated by the discovery of abundant microbially induced sedimentary structures (MISS) and pyrite veneers in close association with Ediacaran fossils, it has not been tested previously by experimental taphonomic studies under controlled laboratory conditions. Arthropod larvae that decayed on top of a cyanobacterial mat demonstrated higher quality preservation of fine-scale anatomy than larvae that decayed in the absence of a mat. Decay experiments involving bacterial mats and organic-rich sands generated a black ring extending radially from the decaying carcasses. When this precipitate was analyzed using XPS and ESEM-EDS it revealed the presence of likely iron sulfides, or at least spatially associated Fe and S, and localized concentrations of common aluminosilicate elements (Al, K, Fe, and Mg), which is a composition that has been documented in association with Ediacaran fossil preservation.

Population structure of the oldest known macroscopic communities from Mistaken Point, Newfoundland

Abstract The presumed affinities of the Terminal Neoproterozoic Ediacara biota have been much debated. However, even in the absence of concrete evidence for phylogenetic affinity, numerical paleoecological approaches can be effectively used to make inferences about organismal biology, the nature of biotic interactions, and life history. Here, we examine the population structure of three Ediacaran rangeomorph taxa (Fractofusus, Beothukis, and Pectinifrons), and one non-rangeomorph taxon (Thectardis) across five fossil surfaces around the Avalon Peninsula, Newfoundland, through analysis of size-frequency distributions using Bayesian Information Criterion (BIC). Best-supported models resolve communities of all studied Ediacaran taxa at Mistaken Point as single cohorts with wide variance. This result is best explained in terms of a “continuous reproduction” model, whereby Ediacaran organisms reproduce aseasonally, so that multiple size modes are absent from preserved communities. Modern benthic invertebrates (both as a whole and within specific taxonomic groups) in deeper-water settings reproduce both seasonally and aseasonally; distinguishing between biological (i.e., continuous reproductive strategies) and environmental (lack of a seasonal trigger) causes for this pattern is therefore difficult. However, we hypothesize that the observed population structure could reflect the lack of a trigger for reproduction in deepwater settings (i.e., seasonal flux of organic matter), until the explosive appearance of mesozooplankton near the base of the Cambrian.

DEEP-WATER EDIACARAN FOSSILS FROM NORTHWESTERN CANADA: TAPHONOMY, ECOLOGY, AND EVOLUTION

Abstract Impressions of soft-bodied Ediacaran megafossils are common in deep-water slope deposits of the June beds at Sekwi Brook in the Mackenzie Mountains of NW Canada. Two taphonomic assemblages can be recognized. Soles of turbidite beds contain numerous impressions of simple (Aspidella) and tentaculate (Hiemalora, Eoporpita) discs. A specimen of the frond Primocandelabrum is attached to an Aspidella-like holdfast, but most holdfast discs lack any impressions of the leafy fronds to which they were attached, reflecting Fermeuse-style preservation of the basal level of the community. Epifaunal fronds (Beothukis, Charnia, Charniodiscus) and benthic recliners (Fractofusus) were most commonly preserved intrastratally on horizontal parting surfaces within turbidite and contourite beds, reflecting a deep-water example of Nama-style preservation of higher levels in the community. A well-preserved specimen of Namalia significantly extends the known age and environmental range of erniettomorphs into deep-water aphotic settings. Infaunal bilaterian burrows are absent from the June beds despite favorable beds for their preservation. The June beds assemblage is broadly similar in age and environment to deep-water Avalonian assemblages in Newfoundland and England, and like them contains mainly rangeomorph and arboreomorph fossils and apparently lacks dickinsoniomorphs and other clades typical of younger and shallower Ediacaran assemblages. Fossil data presently available imply that the classically deep- and shallow-water taxa of the Ediacara biota had different evolutionary origins and histories, with sessile rangeomorphs and arboreomorphs appearing in deep-water settings approximately 580 million years ago and spreading into shallow-water settings by 555 Ma but dickinsoniomorphs and other iconic clades restricted to shallow-water settings from their first known appearance at 555 Ma until their disappearance prior to the end of the Ediacaran.

Ecological Tiering and the Evolution of a Stem: The Oldest Stemmed Frond from the Ediacaran of Newfoundland, Canada

Abstract The ecological segregation of large, multicellular eukaryotes in the Ediacaran in response to competitive feeding results in the evolution of novel morphological adaptations such as sturdy stems to elevate above lower-tier feeding guilds. Culmofrons plumosa n. gen. n. sp. lived attached to the ocean floor and probably fed osmotrophically from dissolved organic nutrients in the water column. Competition for nutrients with specialized lower-tiered organisms resulted in the evolution of a specialized non-feeding structure, drastically expanding the functional morphospace available to Ediacaran rangeomorphs. The first appearance of a cylindrical macroscopic stem in C. plumosa in the Briscal Formation of the Mistaken Point Ecological Reserve marks a significant departure from the modular repetitive branching typical of the Rangeomorpha, and exemplifies the importance of nutrient acquisition in early ecosystem engineering.