The nine newly identified Cenozoic Southern Hemisphere isocrinid species (Fig. 2), and previously identified occurrences32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48 which have been compiled together for the first time to our knowledge (Fig. 4), confirm that the response of stalked crinoids to increased predation pressure as part of the MMR was asynchronous34,38. Our data refute the hypothesis that the Antarctic and South American benthic communities experienced periodic reversions to a Palaeozoic type community structure as a response to environmental perturbations35,47. The new data provided herein, in addition to previously published occurrences32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48, demonstrate that a shallow water Southern Hemisphere fauna of isocrinid crinoids persisted over the Cretaceous-Paleogene boundary, continued into the early Paleocene and to at least the Eocene/Oligocene boundary (Figs. 3 and 5). The shift in distribution of isocrinids out of shallow water may have occurred at the end of the Eocene around Antarctica and Australia, and later in the Miocene in New Zealand. The modern deep water Isocrinida Metacrinus and Saracrinus may have evolved from shallow water Antarctic habitats in the Paleocene, spreading to the southern margin of Australia in the Eocene, and to their present distribution in deeper waters around Australia, New Zealand, New Caledonia, Indonesia, the Philippines and Japan14,51,52,53.

The late persistence of isocrinid crinoids in Antarctica, Australia, New Zealand and South America could be explained either as a result of an absence of, or reduced durophagous predation during the MMR in the Southern Hemisphere. Alternatively, it could be as a result of a delayed distribution and/or radiation of motile and more competitive comatulid crinoids which had greater success in shallow waters than the less mobile isocrinids13. These two options are considered below.

The role of durophagous predation in relation to the distribution of isocrinid crinoids is difficult to assess because, until recently, there was little information about predation on crinoids1,10,54,55,56. Diving investigations have shown predation on recent comatulid crinoids by fishes of several families, consisting of sublethal damage to the crinoid visceral mass and arms56. Crinoid ossicles from the Order Millericrinida were found in bromalites from the Triassic; durophagous sharks, colobodontid fish, placodonts, and some pachypleurosaurs or sauropterygian reptiles were suggested as possible predators57. Predation on comatulid crinoids by cidaroid echinoids has been indicated by studying bite marks on crinoid columnals as well as through direct observation1,10. However, thus far, the only confirmed evidence of predation on isocrinid crinoids has come from laboratory observations and in situ observations using submersibles of predation by cidaroid echinoids10. Therefore, echinoid predation was suggested as a major driver of crinoid radiation and diversity in the Mesozoic1,10. Predation has also been inferred by looking at arm loss and regeneration, suggested to be a response to predation, in fossil isocrinids like Metacrinus from the La Meseta Formation33.

Latitudinal differences in predation may explain the patterns of Cenozoic isocrinid depth distribution seen in the Southern Hemisphere, if predation pressure decreased with increasing latitude3. In modern brachiopods, lower frequencies of repaired predator attacks were observed at high latitudes, possibly due to a lower diversity of crushing predators58. However, it is only today that durophagous predators are rare or absent from Antarctica59. The presence of isocrinids in the La Meseta Formation was attributed to the population being subjected to lower predation pressure than generally prevailed in post-Mesozoic shallow water environments33 as the isocrinids had a lower rate of regenerated arms than in modern settings33. However, taxa thought to predate upon crinoids are found along with isocrinids in Antarctic deposits so a lack of predators cannot be invoked to explain the presence of the isocrinids in the region at the time. Teleost fish, crustaceans and sharks are found in Cretaceous, Paleocene and Eocene deposits of Antarctica60,61,62,63,64 in the same formations as isocrinids. The same is true for Western Australian Eocene deposits (K. McNamara pers. obser.). Isocrinids also co-occur with spines of cidaroid echinoids (known to predate on isocrinids10) in the Sobral Formation, and cidaroid echinoids have also been described from the La Meseta Formation65. Similarly cidaroids and isocrinids are both common in the middle Eocene Nanarup Formation in south-western Australia (McNamara pers. obser.).

Isocrinids are capable, as are comatulids, of autotomy to avoid predatory attacks15. Autotomy planes in stalks and arms and muscular articulations allowing rapid crawling originated in the Middle Triassic57. This, along with recent evidence that isocrinids are motile15, indicates that isocrinids evolved adaptations that enabled them to evade predators during the Mesozoic. Recent specimens of the isocrinids Metacrinus, Saracrinus and Endoxocrinus have been shown to exhibit arm regeneration12,19. Endoxocrinus shows a greater frequency of arm regeneration in shallower (~150 m deep) water than in deeper water (~750 m), leading to the suggestion that predation in shallow water caused isocrinids to move to deeper water12. However, this also shows that today isocrinids are able to inhabit areas which are subject to predation. Isocrinids have been subject to predation throughout their evolutionary history, and have evolved strategies to deal with predatory attacks. Salamon and Gorzelak22 suggested that predation intensity during the Mesozoic was not the only factor controlling the presence or absence of stalked forms in shallow and deep water environments and our data seem to be consistent with this.

Comatulids (feather stars) are thought to have had a higher survival capacity in shallow water than stalked isocrinids13 due to their greater adaptability13. This resulted in comatulids becoming dominant in shallow waters at the present day66. The timing of the onset of comatulid radiation may have not been globally consistent, accounting for longer survival for isocrinids in shallow waters in the Southern Hemisphere. The first true comatulids date from the Early Jurassic66, but overall their fossil record is poor due to a lack of articulated fossils. Using disarticulated elements relies heavily on finding a single centrodorsal ossicle, as arm ossicles are largely taxonomically indeterminate. The oldest known Antarctic comatulid (Notocrinus) was described from the early Eocene and co-occurred with isocrinids34. In South Australia, specimens of comatulids (Glenotremites, Notocrinus, and Loriolometra–Notocrinidae) have been collected in abundance50 from the shallow water early Miocene Mannum Formation, with no co-occurring Isocrinida. This may indicate comatulid dominance in the marine community.

Here we show that Australia has a shallow water fossil record of Isocrinida from the Paleocene to the end of the Eocene (Fig. 3). The oldest (Paleocene) Australian Isocrinida are from Western Australia (Fig. 3). At this time the southern margin of Australia was still connected to Antarctica67 (Fig. 5), but a transgression in the north led to the formation of a shallow water basin68, which the Isocrinida inhabited until the early Eocene. Australia finally separated from Antarctica later in the Eocene, forming an embayment with a complex of shallow water basins from west to east across the southern margin of the Australian continent (Fig. 5). Like echinoids69, foraminifera70, and brachiopods71, the Isocrinida show a pattern of dispersal in a southerly direction along the western Australia coast during the early Paleogene, then an easterly spread across the southern margin of the Australian continent (Fig. 5). Isocrinids do not occur in post- Eocene strata in Australia (Figs. 3 and 5), having seemingly been replaced by comatulids in shallow water habitats. New Zealand was left as an apparent shallow water refugium for isocrinids until the early Miocene (Fig. 3), isocrinids having persisted here from the Paleocene (Figs. 3 and 5)37,38,39,40,41,42,43,44,45,46. Following this, isocrinids were displaced to deeper water environments, which they still inhabit today14.

Isocrinids inhabited Antarctic shallow water communities until the end of the Eocene33 (Fig. 3). There is no evidence for fossil isocrinids in Antarctica, Australia or South America after the Eocene (Figs. 2 and 4). This was a time of speciation and radiation in the Southern Hemisphere for many taxa, including comatulids72,73 when changes in continental configuration and ocean circulation brought in different water masses and isolated Antarctic marine faunas74. The Antarctic Circumpolar Current (ACC) started around the Eocene⁄Oligocene boundary to early Oligocene75 physically isolating Antarctica and preventing warmer water masses from reaching the continent. Full development of the ACC resulted in faunal turnover in the Southern Hemisphere, and an increase in cool water cosmopolitan and true Antarctic endemic forms76,77. This is supported by molecular clock data, which shows that modern species of the comatulid Promachocrinus evolved in the Antarctic region after the onset of the ACC73. Similar radiation events after the onset of the ACC are seen in other taxa such as amphipods, isopods and octopods72. The radiation of apparently more successful modern comatulid taxa in the Southern Hemisphere is co-incident with the demise of isocrinids in the region. The onset of the ACC may have caused a local extinction of isocrinids in the Southern Ocean. The repeated extension of ice sheets across the Antarctic continental shelf may also have discouraged the less mobile isocrinids from living at the depths at which they are found elsewhere today.

Overall, based on the evidence presented herein, it is clear that isocrinids inhabited shallow waters in the Southern Hemisphere region in the early Cenozoic, with the oldest metacrinid specimens found in Antarctica. Opening seaways resulted in isocrinids dispersing along newly formed shallow Australian basins around the southern margin of Australia to New Zealand.