Oxygen, animals and oceanic ventilation: an alternative view

Butterfield, Nicholas J.

doi:10.1111/j.1472-4669.2009.00188.x

Cited by 248 publications

(169 citation statements)

References 88 publications

(139 reference statements)

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“…In addition, suspension feeders can filter large volumes of water, particularly in more protected systems having longer hydrodynamic resident times, and therefore preventing eutrophication and reducing water turbidity, which makes light available for microphytobenthos [47,49,50]. In fact, the appearance of a suspension-feeder infauna may have been the driving force for a dramatic increase in ocean ventilation [51].…”

Section: Discussionmentioning

confidence: 99%

Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks

2014

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The rapid appearance of bilaterian clades at the beginning of the Phanerozoic is one of the most intriguing topics in macroevolution. However, the complex feedbacks between diversification and ecological interactions are still poorly understood. Here, we show that a systematic and comprehensive analysis of the trace-fossil record of the Ediacaran-Cambrian transition indicates that body-plan diversification and ecological structuring were decoupled. The appearance of a wide repertoire of behavioural strategies and body plans occurred by the Fortunian. However, a major shift in benthic ecological structure, recording the establishment of a suspension-feeder infauna, increased complexity of the trophic web, and coupling of benthos and plankton took place during Cambrian Stage 2. Both phases were accompanied by different styles of ecosystem engineering, but only the second one resulted in the establishment of the Phanerozoic-style ecology. In turn, the suspension-feeding infauna may have been the ecological drivers of a further diversification of deposit-feeding strategies by Cambrian Stage 3, favouring an ecological spillover scenario. Trace-fossil information strongly supports the Cambrian explosion, but allows for a short time of phylogenetic fuse during the terminal Ediacaran-Fortunian.

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Section: Discussionmentioning

confidence: 99%

Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks

2014

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“…For decades, the consensus view was that oxygen levels of 1-10% of present atmospheric levels (PALs) were required for metazoan life and particularly for collagen biosynthesis. However, recent studies have radically revised this view, indicating that at least at small size, animals could have lived and reproduced at much lower oxygen levels [35][36][37][38]. Discussions about the drivers of this late Neoproterozoic oxygenation event have led many authors to conclude that the biological activity of organisms may have played an important role [18,36,37,39].…”

Section: Environmental Frameworkmentioning

confidence: 99%

Early metazoan life: divergence, environment and ecology

Erwin

2015

Phil. Trans. R. Soc. B

119

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One contribution of 16 to a discussion meeting issue 'Origin and evolution of the nervous system'. Recent molecular clock studies date the origin of Metazoa to 750-800 million years ago (Ma), roughly coinciding with evidence from geochemical proxies that oxygen levels rose from less than 0.1% present atmospheric level (PAL) to perhaps 1-3% PAL O 2 . A younger origin of Metazoa would require greatly increased substitution rates across many clades and many genes; while not impossible, this is less parsimonious. Yet the first fossil evidence for metazoans (the Doushantuo embryos) about 600 Ma is followed by the Ediacaran fossils after 580 Ma, the earliest undisputed bilaterians at 555 Ma, and an increase in the size and morphologic complexity of bilaterians around 542 Ma. This temporal framework suggests a missing 150-200 Myr of early metazoan history that encompasses many apparent novelties in the early evolution of the nervous system. This span includes two major glaciations, and complex marine geochemical changes including major changes in redox and other environmental changes. One possible resolution is that animals of these still unknown Cryogenian and early Ediacaran ecosystems were relatively simple, with highly conserved developmental genes involved in cell-type specification and simple patterning. In this model, complex nervous systems are a convergent phenomenon in bilaterian clades which occurred close to the time that larger metazoans appeared in the fossil record.

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“…Flying insects should be particularly susceptible to variations in atmospheric pO 2 because their flight musculature has high energy demands (10), particularly during periods of active flight (11, 12). The volume occupied by tracheae, tubes that transport oxygen throughout the body, scales hypermetrically with body volume, imposing further surface area-to-volume constraints on maximum size (13,14).Although these responses underscore the physiological importance of oxygen, developmental plasticity exhibited by different insect groups may not be indicative of evolutionary changes (15), especially in natural settings where other abiotic influences, biotic interactions, and selective pressure from allometric scaling of life-history traits are also important (16)(17)(18)(19)(20). For example, temperature can also be an important influence on insect body size via physiological effects on metabolic oxygen demand and ecological effects on food supply, growing season, and foraging time (20).…”

mentioning

confidence: 99%

“…Although these responses underscore the physiological importance of oxygen, developmental plasticity exhibited by different insect groups may not be indicative of evolutionary changes (15), especially in natural settings where other abiotic influences, biotic interactions, and selective pressure from allometric scaling of life-history traits are also important (16)(17)(18)(19)(20). For example, temperature can also be an important influence on insect body size via physiological effects on metabolic oxygen demand and ecological effects on food supply, growing season, and foraging time (20).…”

mentioning

confidence: 99%

Environmental and biotic controls on the evolutionary history of insect body size

Clapham

Karr

2012

Proc. Natl. Acad. Sci. U.S.A.

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Giant insects, with wingspans as large as 70 cm, ruled the Carboniferous and Permian skies. Gigantism has been linked to hyperoxic conditions because oxygen concentration is a key physiological control on body size, particularly in groups like flying insects that have high metabolic oxygen demands. Here we show, using a dataset of more than 10,500 fossil insect wing lengths, that size tracked atmospheric oxygen concentrations only for the first 150 Myr of insect evolution. The data are best explained by a model relating maximum size to atmospheric environmental oxygen concentration (pO 2 ) until the end of the Jurassic, and then at constant sizes, independent of oxygen fluctuations, during the Cretaceous and, at a smaller size, the Cenozoic. Maximum insect size decreased even as atmospheric pO 2 rose in the Early Cretaceous following the evolution and radiation of early birds, particularly as birds acquired adaptations that allowed more agile flight. A further decrease in maximum size during the Cenozoic may relate to the evolution of bats, the Cretaceous mass extinction, or further specialization of flying birds. The decoupling of insect size and atmospheric pO 2 coincident with the radiation of birds suggests that biotic interactions, such as predation and competition, superseded oxygen as the most important constraint on maximum body size of the largest insects.paleoecology | temperature | maximum likelihood estimation B ecause metabolic oxygen demand increases with increasing body size, environmental oxygen concentration (pO 2 ) is frequently invoked as an important constraint on the size of animals (1-6). Giant late Paleozoic insects, with wingspans as large as 70 cm, are the iconic example of the oxygen-body size link; hyperoxic conditions during the Carboniferous and Permian are thought to have permitted the spectacular sizes of the largest insects ever (2, 4). The physiological basis linking insect body size and pO 2 has been elucidated in numerous experimental tests (5,7,8). Body size and metabolic rate respond to pO 2 when insects are reared in hypoxic or hyperoxic atmospheres (7,8), although the effects are not uniform in all taxa (9). Flying insects should be particularly susceptible to variations in atmospheric pO 2 because their flight musculature has high energy demands (10), particularly during periods of active flight (11, 12). The volume occupied by tracheae, tubes that transport oxygen throughout the body, scales hypermetrically with body volume, imposing further surface area-to-volume constraints on maximum size (13,14).Although these responses underscore the physiological importance of oxygen, developmental plasticity exhibited by different insect groups may not be indicative of evolutionary changes (15), especially in natural settings where other abiotic influences, biotic interactions, and selective pressure from allometric scaling of life-history traits are also important (16)(17)(18)(19)(20). For example, temperature can also be an important influence on insect body size via physiologica...

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Oxygen, animals and oceanic ventilation: an alternative view

Cited by 248 publications

References 88 publications

Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks

Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks

Early metazoan life: divergence, environment and ecology

Environmental and biotic controls on the evolutionary history of insect body size

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