Predator-induced macroevolutionary trends in Mesozoic crinoids Przemysław Gorzelaka,1, Mariusz A. Salamonb, and Tomasz K. Baumillerc aDepartment of Biogeology, Institute of Paleobiology, Polish Academy of Sciences, PL-00-818 Warsaw, Poland; bFaculty of Earth Sciences, University of Silesia, PL-41-200 Sosnowiec, Poland; and cMuseum of Paleontology and Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI 48109 Edited by Steven M. Stanley, University of Hawaii, Honolulu, HI, and approved March 23, 2012 (received for review January 27, 2012) Sea urchins are a major component of recent marine communities be gathered from trace fossils left on skeletons of prey (3) and where they exert a key role as grazers and benthic predators. because it has been shown that the teeth of echinoids can pro- However, their impact on past marine organisms, such as crinoids, duce such traces (17, 18), we surveyed Mesozoic skeletons of is hard to infer in the fossil record. Analysis of bite mark fre- crinoids for such bite marks (Fig. 1A and Table S1). Various quencies on crinoid columnals and comprehensive genus-level traces left by predators on skeletons of their prey, such as drill diversity data provide unique insights into the importance of sea holes, have often been used in a similar fashion (31). However, urchin predation through geologic time. These data show that many complexities can plague the use of trace fossils as a pre- over the Mesozoic, predation intensity on crinoids, as measured dation proxy (18, 32) and recognizing the maker of the traces is by bite mark frequencies on columnals, changed in step with di- perhaps most challenging. The bite traces we report were culled versity of sea urchins. Moreover, Mesozoic diversity changes in the from among other traces on the basis of their similarity to traces predatory sea urchins show a positive correlation with diversity of found on crinoid skeletal elements retrieved from the guts and motile crinoids and a negative correlation with diversity of sessile feces of extant cidaroids (17, 18). Furthermore, we collected data crinoids, consistent with a crinoid motility representing an effec- for stalk fragments only, as stalks are most likely to be bitten by tive escape strategy. We contend that the Mesozoic diversity his- benthic organisms, such as sea urchins, rather than fish, which tory of crinoids likely represents a macroevolutionary response to – have been shown to focus on crinoid arms and cups (21 25). The EVOLUTION changes in sea urchin predation pressure and that it may have set repeated co-occurrence of sea urchins at the localities from the stage for the recent pattern of crinoid diversity in which motile which crinoids with bite marks were recovered is also consistent forms greatly predominate and sessile forms are restricted to with this interpretation. deep-water refugia. Results echinoderms | escalation | macroecology Our data indicate that bite mark frequencies on crinoids gen- erally increased throughout the Mesozoic, although not with a t has long been hypothesized that predator–prey interactions strictly monotonic trend. Moreover, in every time bin (Fig. 1A) fi Irepresent a signi cant driving force of evolutionary change in the frequencies of bite marks on motile crinoids were lower than EARTH, ATOMSPHERIC, the history of life (1–4). However, not only is predation itself those on sessile crinoids, a pattern consistent with the hypothesis AND PLANETARY SCIENCES hard to detect in the fossil record, which makes it difficult to based on observations of modern crinoids (17) that motility ascertain its intensity over geologic time, but macroevolutionary constitutes an escape strategy from benthic predation. predictions of the hypothesis are far from simple (5–13). Recent To test whether the documented changes in bite mark fre- sea urchins (Echinoidea), are known to play a key role in shallow quencies on crinoids could be a consequence of changes in the sea ecosystems as grazers and benthic predators that can modify diversity of their benthic predators, we compared data on bite the distribution, abundance, and species composition of coral marks to changes in the diversity of cidaroids, camarodonts, and and algal reef communities (14–16); however, only few data have diadematoids (Fig. 1B), groups of regular echinoids with a strong hinted at the importance of sea urchins to crinoids (17–19). and active jaw apparatus that were observed to feed on extant Crinoids (Crinoidea), commonly known as sea lilies or feather crinoids (17–19, 29, 30). stars, were one of the dominant components of many shallow-sea The results show a statistically significant positive correlation environments through much of geologic history and a key con- between trends in bite mark frequencies and sea urchin diversity tributor to the sedimentary record (20). Although predation by (P values <0.001, Pearson r = 0.982). However, it is well known fish on crinoids and its evolutionary consequences have received that correlations in temporal trends may be spurious (“ships that the most attention (21–27), sparse data indicated that crinoids pass in the night”) and that in time series, each value is partly may be the prey of benthic invertebrates (28), most notably sea dependent on the previous value (value in bin t is dependent on urchins (17–19, 29, 30). Recently it has been shown that during value in bin t − 1) (33). To reduce the effect of such autocor- the Triassic, the radiation of cidaroid sea urchins capable of relation in each time series, first differencing, or comparison of handling the crinoid skeleton coincided with high frequency changes between bins, is recommended (34). After such differ- of bite marks on crinoids likely produced by the jaw apparatus of encing, the correlations remain significant (P values <0.001, these sea urchins (18). Because it was also during the Triassic Pearson r = 0.989) (Fig. 1 C and D). As diversity and abundance that various modes of active and passive motility appeared often covary (10, 35), it is plausible that a secondary correlation among crinoids, a group that throughout its rich pre-Triassic history was almost exclusively sessile, it was argued that crinoid motility, an effective escape strategy against benthic predation, Author contributions: P.G., M.A.S., and T.K.B. designed research, performed research, was an evolutionary response to echinoid predation (18). analyzed data, and wrote the paper. The hypothesized evolutionary response of crinoids to benthic The authors declare no conflict of interest. predators in the Triassic (18), however, tells us little about This article is a PNAS Direct Submission. subsequent interactions and whether it led to any subsequent 1To whom correspondence should be addressed. E-mail: [email protected]. macroevolutionary consequences. Because quantitative data on This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the geologic history of predator–prey interactions can sometimes 1073/pnas.1201573109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1201573109 PNAS Early Edition | 1of4 Downloaded by guest on October 2, 2021 Fig. 1. Temporal trends in bite mark frequencies on Mesozoic motile and sessile crinoids (A). Solid line represents the mean bite mark frequencies for the six time intervals; statistical significance of changes in frequencies from one time interval to the next were evaluated using a bootstrapping procedure and are shown by asterisks (*P < 0.1 NS; **P < 0.05; ***P < 0.01), for example, the difference between LK and UK is significant at the 0.05 level (**); bite mark frequencies for motile (blue dots) and sessile (green diamonds) crinoids at localities where both taxa were found—fine dotted lines connecting motile and sessile frequencies at each locality are for visual enhancement only and the numbers correspond to localities as in Table S1; note that for all localities, bite mark frequencies are lower for motile taxa. Global Mesozoic sea urchin and crinoid (motile and sessile) diversity curves (B). Cross-correlations between changes in the average bite mark frequencies on Mesozoic crinoids and number of Mesozoic genera of sea urchins (C). Cross-correlations in C after first differencing (D). Cross-correlations between changes in the proportions of Mesozoic genera of motile crinoids and sea urchins (E). Cross-correlations in E after first differencing (F). Cross-correlations between changes in the proportions of genera of Mesozoic sessile crinoids and sea urchins (G). Cross-correlations in G after first differencing (H). Dashed lines represent least-square lines of best fit. Ma, million years ago; L, Lower; M–U, Middle–Upper; U, Upper. 2of4 | www.pnas.org/cgi/doi/10.1073/pnas.1201573109 Gorzelak et al. Downloaded by guest on October 2, 2021 between bite mark frequencies and sea urchin abundance also of both groups, with rare crinoids and echinoids; (ii) the Middle– exists, but we have no way of independently testing that claim. Late Triassic phase, when both sea urchins and motile crinoids Having shown that bite mark frequencies on crinoids varied underwent significant evolutionary radiation, whereas sessile crin- through the Mesozoic and that they were correlated with the oids constituted a minority; (iii) the Early Jurassic phase, when the diversity of their presumed predators, it is now possible to ex- number of sea urchins dropped, leading to a release from predation plore whether such changes had macroevolutionary consequences pressure on sessile crinoids,