Predator-induced macroevolutionary trends in Mesozoic crinoids

Predator-induced macroevolutionary trends
in Mesozoic crinoids
Przemysław Gorzelak a,1 , Mariusz A. Salamon b , and Tomasz K. Baumiller c
a Department of Biogeology, Institute of Paleobiology, Polish Academy of Sciences, PL-00-818 Warsaw, Poland; b Faculty of Earth Sciences, University of Silesia,
PL-41-200 Sosnowiec, Poland; and c Museum 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
where they exert a key role as grazers and benthic predators.
However, their impact on past marine organisms, such as crinoids,
is hard to infer in the fossil record. Analysis of bite mark frequencies
on crinoid columnals and comprehensive genus-level
diversity data provide unique insights into the importance of sea
urchin predation through geologic time. These data show that
over the Mesozoic, predation intensity on crinoids, as measured
by bite mark frequencies on columnals, changed in step with diversity
of sea urchins. Moreover, Mesozoic diversity changes in the
predatory sea urchins show a positive correlation with diversity of
motile crinoids and a negative correlation with diversity of sessile
crinoids, consistent with a crinoid motility representing an effective
escape strategy. We contend that the Mesozoic diversity history
of crinoids likely represents a macroevolutionary response to
changes in sea urchin predation pressure and that it may have set
the stage for the recent pattern of crinoid diversity in which motile
forms greatly predominate and sessile forms are restricted to
deep-water refugia.
echinoderms | escalation | macroecology
It has long been hypothesized that predator–prey interactions
represent a significant driving force of evolutionary change in
the history of life (1–4). However, not only is predation itself
hard to detect in the fossil record, which makes it difficult to
ascertain its intensity over geologic time, but macroevolutionary
predictions of the hypothesis are far from simple (5–13). Recent
sea urchins (Echinoidea), are known to play a key role in shallow
sea ecosystems as grazers and benthic predators that can modify
the distribution, abundance, and species composition of coral
and algal reef communities (14–16); however, only few data have
hinted at the importance of sea urchins to crinoids (17–19).
Crinoids (Crinoidea), commonly known as sea lilies or feather
stars, were one of the dominant components of many shallow-sea
environments through much of geologic history and a key contributor
to the sedimentary record (20). Although predation by
fish on crinoids and its evolutionary consequences have received
the most attention (21–27), sparse data indicated that crinoids
may be the prey of benthic invertebrates (28), most notably sea
urchins (17–19, 29, 30). Recently it has been shown that during
the Triassic, the radiation of cidaroid sea urchins capable of
handling the crinoid skeleton coincided with high frequency
of bite marks on crinoids likely produced by the jaw apparatus of
these sea urchins (18). Because it was also during the Triassic
that various modes of active and passive motility appeared
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,
was an evolutionary response to echinoid predation (18).
The hypothesized evolutionary response of crinoids to benthic
predators in the Triassic (18), however, tells us little about
subsequent interactions and whether it led to any subsequent
macroevolutionary consequences. Because quantitative data on
the geologic history of predator–prey interactions can sometimes
be gathered from trace fossils left on skeletons of prey (3) and
because it has been shown that the teeth of echinoids can produce
such traces (17, 18), we surveyed Mesozoic skeletons of
crinoids for such bite marks (Fig. 1A and Table S1). Various
traces left by predators on skeletons of their prey, such as drill
holes, have often been used in a similar fashion (31). However,
many complexities can plague the use of trace fossils as a predation
proxy (18, 32) and recognizing the maker of the traces is
perhaps most challenging. The bite traces we report were culled
from among other traces on the basis of their similarity to traces
found on crinoid skeletal elements retrieved from the guts and
feces of extant cidaroids (17, 18). Furthermore, we collected data
for stalk fragments only, as stalks are most likely to be bitten by
benthic organisms, such as sea urchins, rather than fish, which
have been shown to focus on crinoid arms and cups (21–25). The
repeated co-occurrence of sea urchins at the localities from
which crinoids with bite marks were recovered is also consistent
with this interpretation.
Results
Our data indicate that bite mark frequencies on crinoids generally
increased throughout the Mesozoic, although not with a
strictly monotonic trend. Moreover, in every time bin (Fig. 1A)
the frequencies of bite marks on motile crinoids were lower than
those on sessile crinoids, a pattern consistent with the hypothesis
based on observations of modern crinoids (17) that motility
constitutes an escape strategy from benthic predation.
To test whether the documented changes in bite mark frequencies
on crinoids could be a consequence of changes in the
diversity of their benthic predators, we compared data on bite
marks to changes in the diversity of cidaroids, camarodonts, and
diadematoids (Fig. 1B), groups of regular echinoids with a strong
and active jaw apparatus that were observed to feed on extant
crinoids (17–19, 29, 30).
The results show a statistically significant positive correlation
between trends in bite mark frequencies and sea urchin diversity
(P values

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.
Gorzelak et al. PNAS | May 1, 2012 | vol. 109 | no. 18 | 7005
EVOLUTION
EARTH, ATMOSPHERIC,
AND PLANETARY SCIENCES

etween bite mark frequencies and sea urchin abundance also
exists, but we have no way of independently testing that claim.
Having shown that bite mark frequencies on crinoids varied
through the Mesozoic and that they were correlated with the
diversity of their presumed predators, it is now possible to explore
whether such changes had macroevolutionary consequences
for the prey. A plausible scenario is that changes in predation
pressure (inferred from bite mark frequencies) would lead to
corresponding changes in the incidence of effective defenses
among prey. Given that crinoid motility is an effective defense
against sea urchin predation and the already established correlation
between sea urchins and bite mark frequencies, two
macroevolutionary patterns might be expected for sea urchins
and crinoids: changes in the diversity of cidaroids, camarodonts,
and diadematoids, should be correlated with changes in diversities
of motile taxa, crinoids that can avoid predators both
actively and passively, and anticorrelated with changes in diversities
of sessile forms, crinoids permanently attached to the
substrate with no obvious protection from benthic predators.
These predictions were tested statistically using the genus-level
diversity histories of each group obtained from the Paleobiology
Database (PBDB) and other literature sources (36). Our analyses
at epoch and subperiod resolution suggest strong interdependence
between most observed trends (Fig. 1 E–H). Diversity
of motile crinoids is positively correlated with that of sea urchins
(P values

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