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, which consequently diversified; and (iv) for the prey. A plausible scenario is that changes in predation theMiddleJurassic–Late Cretaceous phase, when diversification of pressure (inferred from bite mark frequencies) would lead to sea urchins increased gradually, leading to the coevolutionary corresponding changes in the incidence of effective defenses increases of diversity of motile crinoids and simultaneous decreases among prey. Given that crinoid motility is an effective defense of sessile crinoids (starting from the Early Cretaceous). The timing against sea urchin predation and the already established cor- of these changes is roughly coincident with the Mesozoic marine relation between sea urchins and bite mark frequencies, two revolution (MMR) (2), although it suggests two major phases of macroevolutionary patterns might be expected for sea urchins intensification in predation-driven evolution in benthic marine and crinoids: changes in the diversity of cidaroids, camarodonts, communities: one in the Middle–Late Triassic and the another in and diadematoids, should be correlated with changes in di- Late Cretaceous times. These data are intriguingly consistent with versities of motile taxa, crinoids that can avoid predators both recent suggestions that the major antipredatory innovations among actively and passively, and anticorrelated with changes in di- benthic fauna might have occurred during two periods, the Late versities of sessile forms, crinoids permanently attached to the Triassic and the Late Cretaceous (39, 40). substrate with no obvious protection from benthic predators. To date, most evolutionary trends among crinoids connected These predictions were tested statistically using the genus-level with the MMR (2) have been ascribed to predation by fish (21–24, diversity histories of each group obtained from the Paleobiology 26, 27). Our data suggest that benthic predation by sea urchins has Database (PBDB) and other literature sources (36). Our analy- also been an important (if not the main) causal driver of biological ses at epoch and subperiod resolution suggest strong interde- change throughout the Mesozoic, and that it may have set the pendence between most observed trends (Fig. 1 E–H). Diversity stage for the recent pattern in which motile crinoids greatly pre- of motile crinoids is positively correlated with that of sea urchins dominate over sessile forms that live only at great depths (20). (P values <0.017, Pearson r = 0.89), whereas diversity of sessile crinoids is negatively correlated with that of sea urchins (P Materials and Methods EVOLUTION values = ∼0.146, Pearson r = −0.747). After differencing, Three echinoid groups with a strong and active jaw apparatus are known to changes in motile crinoid and sea urchin diversities show an even interact with modern crinoids, i.e., cidaroids, camarodonts, and diadematoids stronger positive correlation (P values <0.005, Pearson r = (17–19, 29, 30), and genus-level data for these were extracted from the 0.975). Although after first differencing the relationship between PBDB. The data were extracted using the following parameters: group G H names “Cidaroida” (on October 25, 2011), “Camarodonta” (on November sessile crinoids and sea urchins (Fig. 1 and ) lacks statistical 13, 2011), and “Diadematoida” (on November 13, 2011), and time intervals = significance (P values = ∼0.339, Pearson r = −0.661), it should r 251 to 0 Ma. The data were then recounted per six time bins (Early Triassic, be noted that values remain strongly negative as predicted. Middle–Late Triassic, Early Jurassic, Middle–Late Jurassic, Early Cretaceous, Discussion and Late Cretaceous). The genus-level data for crinoids were taken from the new Treatise on Invertebrate Paleontology, Part T, Echinodermata 2 Revised, EARTH, ATOMSPHERIC,

The results presented here suggest that for Mesozoic crinoids Crinoidea, Vol 3 (36), which, at least for crinoids, is a much more compre- AND PLANETARY SCIENCES changes in the diversity of motile and sessile taxa shown in Fig. 1 hensive source of genus-level data than the PBDB. Motile crinoids include: (i) most probably reflect an evolutionary response of the prey to sea taxa capable with benthic locomotion, including isocrinids, holocrinids, and urchin predation. Of course, other scenarios could be offered to comatulids (except bourgueticrinids) and (ii) nektonic, planktonic, or pseu- doplanktonic taxa, including pentacrinids, traumatocrinids, roveacrinids, explain the observed patterns. For example, one might argue for and other microcrinoids (such as Lanternocrinus, Nasutocrinus, and Leocri- the opposite directional causation, that it was the evolutionary fi nus). Sessile crinoids include taxa with a cementing or root-like mode of changes in crinoids that triggered a diversi cation of sea urchins attachment: encrinids (except traumatocrinids), bourgueticrinids, miller- leading to more intense predation and a consequent increase in icrinids, cyrtocrinids, and other stalked crinoids (such as Cyclocrinus, Qin- the frequency of bite marks. However, given that sea urchins are gyanocrinus, Tulipacrinus, Bihaticrinus, Cratecrinus, and Taurocrinus). omnivorous, it is more likely that their own predators, rather than Diversity data for crinoids and echinoids were subjected to a runs test prey, drove their evolution. Thus, in this case, the documented (“linear models”)onPAST2.02tofind P and Pearson r values (41). patterns are best explained as reflecting an evolutionary response Bite marks were counted on every affected skeletal element, such that of prey to their predators. for articulated columnal ossicles (= pluricolumnals), each columnal within fl a pluricolumnal was counted separately. It has been argued that global diversity trends need not re ect The frequencies of bite marks are higher on sessile taxa in all five time bins local responses of lineages to biotic interactions and that it is at in which both sessile and motile taxa coexisted (Table S1). This pattern is the latter, smaller scales that the evolutionary impact of such consistent with the hypothesis that motile taxa should be less prone to interactions is most appropriately tested (7, 8). However, our data, benthic predation because the null model, that the probability of either one as well as those for several other groups (13, 37, 38), indicate that being higher in any time bin is equal (P = q = 0.5), can be rejected at P ∼0.05. such interactions can have consequences, directly or indirectly, at A test of statistical significance of differences in bite mark frequencies higher taxonomic levels. Most compelling are cases of increasing between adjacent time bins was done using a bootstrapping procedure incidence of taxa with well-developed antipredatory defenses, and that involved calculating 1,000 average bite mark frequencies for each bin it has been suggested that taxa possessing such traits may be more by sampling each bin with replacement and comparing the distribution of bootstrapped averages in adjacent bins. All differences in bite mark frequencies prone to speciation (38). Although our study does not allow us to between adjacent bins were significant at P < 0.05, with the exception of make any claims about whether differences in speciation and/or Middle–Upper Jurassic to Lower Cretaceous, which was marginally significant extinction rates are the cause of changes in diversities of motile (P < 0.1). The correlations for Fig. 1 C and D are statistically significant (P < and sessile crinoids, it does show that over geologic time diversities 0.05) regardless of whether mean, median, or logit transform is used. of well-defended taxa need not change in a monotonic fashion and may be correlated with diversities of predators. ACKNOWLEDGMENTS. Comments by two reviewers greatly helped improve On the basis of the diversity data and the analysis of bite mark this paper. This work was funded by State Committee for Scientific Research Grant (Komitet Badan Naukowych, KBN) N307 138835, National Geographic frequencies on crinoid columnals, four major phases in the Meso- Society Grant NGS 8505-08, and Division of Environmental Biology of the zoic evolutionary history of sea urchins and crinoids can be iden- National Science Foundation Grant DEB 1036393. This is Paleobiology tified: (i) the Early Triassic phase that followed the near extinction Database publication no. 155.

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