Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution

Baumiller, Tomasz K.; Salamon, Mariusz A.; Gorzelak, Przemysław; Mooi, Richard; Messing, Charles G.; Gahn, Forest J.

doi:10.1073/pnas.0914199107

Cited by 140 publications

(127 citation statements)

References 29 publications

(38 reference statements)

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“…Predator identity inferred from diagnostic marks (e.g., gastropod boring scars), stomach contents, or recent observations gives little indication of pervasiveness (3,5). Large-scale predation pressure inferred from escalation of, or persistent damage to, prey defenses reveals little about specific relationships and might not reflect real trends (3,4,6).…”

mentioning

confidence: 99%

“…The first was a diversification climax starting in the Tournaisian stage (359-345 Mya), establishing an "Age of Crinoids" evidenced by widespread encrinital limestones (12). The second was faunal turnover in the later Mississippian (345-318 Mya), as increased extinction rates for camerate crinoids resulted in the advanced cladid-dominated late Paleozoic evolutionary fauna (5,12,19).…”

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confidence: 99%

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Persistent predator–prey dynamics revealed by mass extinction

Sallan

Kammer²,

Ausich³

et al. 2011

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

108

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Predator-prey interactions are thought by many researchers to define both modern ecosystems and past macroevolutionary events. In modern ecosystems, experimental removal or addition of taxa is often used to determine trophic relationships and predator identity. Both characteristics are notoriously difficult to infer in the fossil record, where evidence of predation is usually limited to damage from failed attacks, individual stomach contents, onesided escalation, or modern analogs. As a result, the role of predation in macroevolution is often dismissed in favor of competition and abiotic factors. Here we show that the end-Devonian Hangenberg event (359 Mya) was a natural experiment in which vertebrate predators were both removed and added to an otherwise stable prey fauna, revealing specific and persistent trophic interactions. Despite apparently favorable environmental conditions, crinoids diversified only after removal of their vertebrate consumers, exhibiting predatory release on a geological time scale. In contrast, later Mississippian (359-318 Mya) camerate crinoids declined precipitously in the face of increasing predation pressure from new durophagous fishes. Camerate failure is linked to the retention of obsolete defenses or "legacy adaptations" that prevented coevolutionary escalation. Our results suggest that major crinoid evolutionary phenomena, including rapid diversification, faunal turnover, and species selection, might be linked to vertebrate predation. Thus, interactions observed in small ecosystems, such as Lotka-Volterra cycles and trophic cascades, could operate at geologic time scales and higher taxonomic ranks. Both trophic knock-on effects and retention of obsolete traits might be common in the aftermath of predator extinction.Carboniferous | durophagy | biodiversity | paleontology | macroecology

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mentioning

confidence: 99%

mentioning

confidence: 99%

Persistent predator–prey dynamics revealed by mass extinction

Sallan

Kammer²,

Ausich³

et al. 2011

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

108

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“…Therefore, currently there is no evidence for fundamental differences in the chemical defense of comatulids and stalked crinoids that might explain the offshore displacement of stalked crinoids. In contrast to a possible deterrent function of the pigments against fishes, such a function against benthic predation by echinoids is not supported, because indications of predation by echinoids have been observed for (likely hypericinoid-containing) crinoids of the order Encrinida (31). A further defensive function of the pigments might be antifouling, because most echinoderms are free from fouling organisms, and antifouling properties have been reported for ethanolic extracts of echinoderms (32).…”

Section: Resultsmentioning

confidence: 93%

Persistent and widespread occurrence of bioactive quinone pigments during post-Paleozoic crinoid diversification

Wolkenstein

2015

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

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Secondary metabolites often play an important role in the adaptation of organisms to their environment. However, little is known about the secondary metabolites of ancient organisms and their evolutionary history. Chemical analysis of exceptionally well-preserved colored fossil crinoids and modern crinoids from the deep sea suggests that bioactive polycyclic quinones related to hypericin were, and still are, globally widespread in post-Paleozoic crinoids. The discovery of hypericinoid pigments both in fossil and in presentday representatives of the order Isocrinida indicates that the pigments remained almost unchanged since the Mesozoic, also suggesting that the original color of hypericinoid-containing ancient crinoids may have been analogous to that of their modern relatives. The persistent and widespread occurrence, spatially as well as taxonomically, of hypericinoid pigments in various orders during the adaptive radiation of post-Paleozoic crinoids suggests a general functional importance of the pigments, contributing to the evolutionary success of the Crinoidea.crinoids | molecular preservation | marine natural products | polyketides | liquid chromatography-mass spectrometry

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“…Among these traits, autotomy planes and crawling abilities, which probably originated in the Triassic holocrinids and isocrinids (but see also Donovan 2012), are two of the best known textbook examples of dramatic functional changes in the evolutionary history of crinoids (e.g., Hagdorn 2011). Baumiller et al (2010) argued that this novelty evolved as an effective escape strategy from echinoid predators during the so-called Mesozoic marine revolution. The ability to shed the stalk, which allowed active relocation, in the oldest post-Paleozoic stem-group isocrinids has been supported by taphonomic data (preferential disarticulation at the distal facets of nodals; see Baumiller and Hagdorn 1995), functional morphology (occurrence of highly flexible muscular arms, lack of holdfast; see, e.g., Hagdorn 2011) and micromorphology (occurrence of synostosial stereom in the distal facets of nodals, Gorzelak 2018).…”

Section: Discussionmentioning

confidence: 99%

“…d-f Gypsum casts (hypichnia) of the above illustrated traces (a-c; correspondingly). Scale bars 1 cm 2005), but also through major functional changes (Baumiller et al 2008(Baumiller et al , 2010. More specifically, Paleozoic crinoids, dominated by sessile forms, were replaced by predominantly motile taxa displaying many morphological and behavioral novelties (e.g., Gorzelak et al 2012Gorzelak et al , 2016.…”

Section: Discussionmentioning

confidence: 99%

Experimental neoichnology of crawling stalked crinoids

et al. 2018

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Stalked crinoids have long been considered sessile. In the 1980s, however, observations both in the field and of laboratory experiments proved that some of them (isocrinids) can actively relocate by crawling with their arms on the substrate, and dragging the stalk behind them. Although it has been argued that this activity may leave traces on the sediment surface, no photographs or images of the traces produced by crawling crinoids have been available. Herein, we present results of neoichnological experiments using the shallowest species of living stalked crinoid, Metacrinus rotundus, dredged from Suruga Bay (near the town of Numazu, Shizuoka Prefecture, * 140 m depth). Our results demonstrate that isocrinids produce characteristic locomotion traces, which have some preservation potential. They are composed of rather deep and wide, sometimes weakly sinuous, central drag marks left by the stalk and cirri, and short, shallow scratch marks made by the arms. Based on the functional morphology and taphonomy, it has been argued that the ability to autotomize the stalk and relocate had already evolved in the oldest stem-group isocrinids (holocrinids), likely in response to increased benthic predation pressure during the so-called Mesozoic marine revolution. Our data show that this hypothesis may be corroborated in the future by ichnological findings, which may provide more direct proof of active locomotion in Triassic holocrinids.

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Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution

Cited by 140 publications

References 29 publications

Persistent predator–prey dynamics revealed by mass extinction

Persistent predator–prey dynamics revealed by mass extinction

Persistent and widespread occurrence of bioactive quinone pigments during post-Paleozoic crinoid diversification

Experimental neoichnology of crawling stalked crinoids

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