TESTING THE ROLES OF EXTRATROPICAL ORIGINATION AND PREDATION

ON IRREGULAR ECHINOID EVOLUTION

by

JUSTIN MATTHEW MILLER

(Under the Direction of Sally E. Walker)

ABSTRACT

The number of extratropical vs. tropical originations and the predation

frequency of fossil irregular echinoids were analyzed to gain a better understanding of

their evolution. The latitudinal diversity gradient for irregular echinoids is atypical

compared to other marine bivalves and current evolutionary models are not applicable.

An out-of-the-extratropics (OTE) model is used to describe how marine organisms may

originate in the extratropics and then migrate into tropical regions. Irregular echinoids

from the Late Eocene Ocala Limestone were categorized into burrow tiers based on

morphological characters so predation frequency at different burrow depths could be

assessed. Predation frequency was highest for medium and deep burrow tiers, suggesting

that burrowing does not reduce cassid predation. This may indicate that evolution

towards infaunalism for irregular echinoids was not driven by increasing predation

pressure in the Mesozoic.

INDEX WORDS: Evolution, Echinoid, Diversity, Planktotrophic, Extratropical,

Predation, Drill Hole, Burrow, Tier, Eocene, Ocala Limestone

TESTING THE ROLES OF EXTRATROPICAL ORIGINATION AND PREDATION

ON IRREGULAR ECHINOID EVOLUTION

by

JUSTIN MATTHEW MILLER

B.S., Georgia Southwestern State University, 2006

A Thesis Submitted to the Graduate Faculty of The University of Georgia in Partial

Fulfillment of the Requirements for the Degree

MASTER OF SCIENCE

ATHENS, GEORGIA

2011

© 2011

Justin Matthew Miller

All Rights Reserved

TESTING THE ROLES OF EXTRATROPICAL ORIGINATION AND PREDATION

ON IRREGULAR ECHINOID EVOLUTION

by

JUSTIN MATTHEW MILLER

Major Professor: Sally E. Walker

Committee: Steven M. Holland

Bruce L. Railsback

Electronic Version Approved:

Maureen Grasso

Dean of the Graduate School

The University of Georgia

May 2011

iv

ACKNOWLEDGEMENTS

My deepest and most sincere thanks go to my major advisor Dr. Sally Walker.

Without her seemingly unwavering patience and guidance this project would not have

been possible. I showed up at her office needing a major advisor in geology and she

happily took me in and transformed my understanding of educating and science.

I thank Dr. Railsback for helping to alleviate some of my major early writing

problems. Thanks to Dr. Steven Holland for showing me that statisitics can be enjoyable

through the use of R. Dr. Burt Carter, whether intentinally or not, is responsible for my

interest in working with echinoids. Many thanks go to him for our many discussions

regarding southeastern echinoids as well as educating me more on echinoids with each

conversation. Special thanks go to Roger Portell for giving me access to Ocala

Limestone quarries that were normally inaccessible. Thanks to Eleanor Gradner for

helpful editing and to my good friend and field partner Matt Jarrett I thank you for your

generous “donation” of fossil echinoids that contributed to this project. My friend

Benjamin Caulton I thank for late night discussions regarding echinoids and allowing me

to hone my ideas. Lastly, many thanks must go to my girlfriend Jacquie whose constant

support allowed me to overcome many obstacles during this journey. I simply could not

have done this without her.

Financial support for this work was graciously awarded by the Paleontological

Society Stephen J. Gould Student Grant-in-Aid Program, University of Georgia

Department of Geology Wheeler-Watts Fund, and the Southwest Florida Fossil Club.

v

TABLE OF CONTENTS

Page

ACKNOWLEDGEMENTS ............................................................................................... iv

LIST OF TABLES ............................................................................................................ vii

LIST OF FIGURES ......................................................................................................... viii

CHAPTER

1 INTRODUCTION AND LITERATURE REVIEW .........................................1

Statement of Objectives ...............................................................................2

Thesis Structure ...........................................................................................3

References ....................................................................................................4

2 THE EXTRATROPICS AS A CENTER FOR EVOLUTIONARY

DIVERSIFICATION ...................................................................................6

Abstract ........................................................................................................7

Introduction ..................................................................................................7

Results ........................................................................................................11

Out of the Extratropics Model for Evolutionary Diversification ...............14

Methods......................................................................................................17

Acknowledgments......................................................................................19

References ..................................................................................................20

vi

3 TESTING THE INFAUNAL-EVOLUTION HYPOTHESIS: DO DEEP

BURROWING IRREGULAR ECHINOIDS HAVE REDUCED

INCIDENCE OF DRILLING PREDATION ............................................31

Abstract ......................................................................................................32

Introduction ................................................................................................32

Methods......................................................................................................35

Results ........................................................................................................37

Discussion ..................................................................................................39

Conclusions ................................................................................................44

Acknowledgments......................................................................................45

References ..................................................................................................45

4 CONCLUSIONS..............................................................................................61

APPENDICES

A LATITUDINAL DIVERSITY GRADIENT DATA FOR MODERN

IRREGULAR ECHINOIDS ..................................................................................64

B IRREGULAR ECHINOID GENERA WITH A MODERN REPRESENTATIVE

AND FOSSIL RECORD .......................................................................................66

C COLLECTIONS DATA FROM THE SMITHSONIAN AND PALEOBIOLOGY

DATABASES ........................................................................................................69

D REGISTER OF FIELD SITES ............................................................................137

E FIELD AND MUSEUM SPECIMENS ANALYZED FOR PREDATION ........139

vii

LIST OF TABLES

Page

Table 2.1: Number of irregular echinoid genera (includes subgenera) that originated in

the Cretaceous to Plio-Pleistocene .........................................................................26

Table 3.1: Burrow tiers used and the morphological characters that define those tiers ....52

Table 3.2: Irregular echinoid species, their inferred burrow depth and number of

individuals examined for cassid predation .............................................................53

Table 3.3: Predation frequency of each species within the four burrow tiers....................54

Table 3.4: General size metrics for the fourteen species of irregular echinoids from the

Late Eocene Ocala Limestone ...............................................................................55

Table 3.5: Summary of bore hole analysis performed by Gibson and Watson on five

species of Ocala Limestone irregular echinoids ....................................................56

viii

LIST OF FIGURES

Page

Figure 2.1: Comparative latitudinal diversity gradients (LDG) for modern irregular

echinoids, infaunal and epifaunal bivalves ............................................................27

Figure 2.2: Latitudinal differences in tropical and extratropical originations and present-

day latitudinal limits of irregular echinoid genera that first occur in the tropics ...28

Figure 2.4: Number of irregular echinoid collections per latitudinal bin for Cenozoic time

periods. ...................................................................................................................29

Figure 2.4: Theoretical schematic for the out of the extratropics (OTE) model ................30

Figure 3.1: Location of museum and field samples used in this study ..............................57

Figure 3.2: Generalized stratigraphic column of the Ocala Limestone .............................58

Figure 3.3: Number of species per burrow tier for irregular echinoids from the Late

Eocene Ocala Limestone........................................................................................59

Figure 3.4: Predation frequency vs. size class of irregular echinoids from the Late Eocene

Ocala Limestone ....................................................................................................60

1

CHAPTER 1

INTRODUCTION AND LITERATURE REVIEW

2

Statement of Objectives

Irregular echinoids (heart urchins, sand dollars, sea biscuits) are a group of infaunal

invertebrates that have colonized many marine environments from the tropics and Antarctic

regions (Smith, 1984; David et al., 2005). Irregular echinoids diversified from their regular

echinoid (sea urchin) counterparts in the Early Jurassic and the diversity of both groups increased

rapidly during the remaining Mesozoic (Kier, 1982; Smith, 1984). For other groups of marine

invertebrates, such as bivalves, an apparent trend of decreasing diversity towards higher latitudes

is known as the latitudinal diversity gradient (LDG). Three evolutionary models have been

postulated to explain the latitudinal diversity gradient: 1) cradle 2) museum and 3) out of the

tropics (OTT) (Stebbins, 1974; Jablonski et al., 2006), but it is unknown which of these models,

if any, apply to the diversification history of irregular echinoids.

The evolutionary force that led to an infaunal mode of life for echinoids is also not well

understood. For other groups of marine organisms, predation has been a major influence on the

evolution of morphology (Kelley and Hansen, 1993; Dietl et al, 2000; Vermeij, 2008), behavior

(Chattopadhyay and Baumiller, 2007; Casey and Chattopadhyay, 2008), and diversity (Huntley

and Kowalewski, 2007). In fact, one of the main trends resulting from the purported Marine

Mesozoic Revolution was an increase in infaunal organisms due to increasing predation

pressures (Stanley, 1977; Aberhan et al., 2006). This has led some workers to hypothesize that

the infaunalization of echinoids in the Early Jurassic may have also been a product of predation

pressure (Kier, 1982; Cross and Rose, 1994; McNamara, 1994). If the predation hypothesis for

echinoids is valid, then deeper burrowing echinoids should have fewer traces of predation. To

adequately assess whether predation decreases with increasing sediment depth, the relative

burrow depth for irregular echinoids must be known.

3

To provide a more complete understanding of irregular echinoid evolution, the objectives

of this research are twofold. The first objective is to test the evolutionary diversification history

of irregular echinoids using the three evolutionary models. If irregular echinoids do not fit any

of these existing models, a fourth model will be proposed. The second objective is to test

whether deep burrowing reduces predation on Late Eocene irregular echinoids by categorizing

them into relative burrow depths based on test morphology.

Thesis Structure

The evolution of irregular echinoids is presented by examining their evolutionary

diversification history first (Chapter 2). The modern latitudinal diversity gradient (LDG) of

irregular echinoids is shown so that the evolutionary patterns that may have produced their LDG

can be tested. Assessment of the three current evolutionary models is tested by calculating the

number of fossil irregular echinoids that originate in both the tropical and extratropical regions.

Collections from two fossil databases are utilized to determine if sampling is biased towards a

particular region. The predation frequency of irregular echinoids from the Late Eocene Ocala

Limestone is analyzed in relation to paleoecological burrow tiers (Chapter 3). The importance of

burrowing and the ramifications it can have on the Ocala Limestone paleoecology is also

examined. Finally, the results from all analyses are summarized in the concluding chapter

(Chapter 4).

4

References

Chattopadhyay, D., and T. K. Baumiller. 2007. Drilling under threat: an experimental

assessment of the drilling behavior of Nucella lamellosa in the presence of a predator.

Journal of Experimental Marine Biology and Ecology, v. 352, p. 257-266.

Casey, M. M., and D. Chattopadhyay. 2008. Clumping behavior as a strategy against drilling

predation: implications for the fossil record. Journal of Experimental Marine Biology and

Ecology 376:174-179.

Cross, N. E. and E. P. F. Rose. 1994. Predation of the Upper Cretaceous spatangoid echinoid

Micraster. Pp. 607-61 in B. David, A. Guille, J.P. Féral and M. Roux, eds. Echinoderms

through Time, Rotterdam, Netherlands.

David, B., T. Chone, and A. Festeau. 2005. Biodiversity of Antarctic echinoids: a comprehensive

and interactive database. Scientia Marina 69:201-203.

Dietl, G., R. Alexander, andW. Bien. 2000. Escalation in late Cretaceous-early Paleocene

oysters (Gryphaeidae) from the Atlantic Coastal Plain. Paleobiology 26:215-237.

Huntley, J. W., and M. Kowalewski. 2007. Strong coupling of predation intensity and diversity

in the Phanerozoic fossil record. Proceedings of the National Academy of Sciences

104:15006-15010.

Jablonksi D, K. Roy, and J. W. Valentine. 2006. Out of the tropics: evolutionary dynamics of the

latitudinal diversity gradient. Science 314:102-106.

Kelley, P., and T. Hansen. 1993. Evolution of the naticid gastropod predator-prey system: an

evaluation of the hypothesis of escalation. Palaios 8:358-375.

Kier, P. M. 1982. Rapid evolution in echinoids. Palaeontology 25:1-9.

5

McNamara, K. 1994. The significance of gastropod predation to patterns of evolution and

extinction. Pp. 785-793 in B. David, A. Guille, J.P. Féral and M. Roux, eds. Echinoderms

through Time, Rotterdam, Netherlands.

Smith, A. B. 1984. Echinoid Palaeobiology, Allen & Unwin Press, Australia.

Stanley, S. M. 1977. Trends, rates, and patterns of evolution in the Bivalvia. Pp 209-253 in A.

Hallam, ed. Pattens of evolution as illustrated by the fossil record, New York, New York.

Stebbins, G. L. 1974. Flowering plants: Evolution Above the Species Level, Belknap Press,

Cambridge.

Vermeij, G. 2008. Escalation and its role in Jurassic biotic history. Palaeogeography,

Palaeoclimatology, Palaeoecology 262:5-8.

6

CHAPTER 2

THE EXTRATROPICS AS A CENTER FOR EVOLUTIONARY DIVERSIFICATION1

1 Miller, J.M. and Walker, S.E. Submitted to Proceedings of the National Academy of Sciences,

3/16/2011.

7

Abstract

Many terrestrial and marine organisms exhibit a latitudinal diversity gradient (LDG), but

the evolutionary dynamics behind the LDG are not well understood. We found that an important

group of marine invertebrates, irregular echinoids, had an unusual LDG and that their

evolutionary originations were higher in the extratropics than in the tropics. Additionally, nearly

76% of genera that originated in the extratropics now have some presence in the tropics.

Because current evolutionary models are not applicable to this ecologically-important clade, we

propose an out of the extratropics (OTE) model to describe how marine organisms may originate

in the extratropics and then migrate into tropical regions. This model is applicable to other taxa,

such as sediment-dwelling foraminifera and terrestrial mammals. Despite the fact that fossil

echinoid collections date to the early 1800s and are arguably well sampled, much of their

evolutionary history (Paleogene to Neogene) is based on collections representing extratropical

paleoregions. If there is an extratropical bias, we can not address the full extent of this bias until

the intensity of tropical sampling is known. Irregular echinoids have colonized shallow shelf to

deep water from the tropics to the polar regions of Antarctica, and are among the most diverse

groups of echinoderms. Altered ecological conditions tied to global climate change have the

potential to disrupt contemporary LDGs, and thus it is important to examine the fossil record of

ecologically-important clades that originated in extratropical and polar regions to understand

their susceptibility to climate-induced perturbations.

Introduction

Few trends in evolutionary biogeography are more studied than the pattern of decreasing

diversity with increasing latitude known as the latitudinal diversity gradient (LDG) (Hillebrand,

8

2004). Many organisms such as birds, bacteria, terrestrial mammals, marine fish and marine

invertebrates exhibit a LDG (Hawkins et al., 2003; Fisher et al., 2008; Fuhrman et al., 2008;

Buckley et al., 2010). While a number of studies have focused on the ecological causes behind

the LDG, little attention is given to the evolutionary dynamics that may have produced it

(Mittelbach et al., 2007). Altered conditions tied to global climate change may disrupt LDGs

(Fisher et al., 2008). Therefore, it is important to examine the fossil record of ecologically-

important clades to understand their susceptibility to climate-induced perturbations in the past.

Using marine bivalves from the late Miocene through Pleistocene, Jablonski et al. (2006)

tested two LDG diversification models and proposed a third model: 1) the museum model posits

that origination occurs in both the tropics and extratropics but lower extinction rates in the

tropics leads to increased diversity in that region (Stebbins, 1974; Arita and Vazquez-

Dominquez, 2008); 2) the cradle model where taxa in the tropics a higher more origination rate

than those in the extratropics (Stebbins, 1974); and 3) the out of the tropics model (OTT) where

more taxa originate in the tropics and then migrate to higher latitudes while maintaining a strong

tropical presence (Jablonski et al., 2006). The museum model appears to hold for birds

(Blackburn and Gaston, 1996), whereas the cradle model may explain coral LDGs (Kiessling et

al., 2010). Jablonski et al. (2006) and Roy et al. (2009) tested the OTT model and found that it

explains the LDG pattern for most marine bivalves. Terrestrial groups such as liverworts, leaf

beetles, and butterflies also appear to fit the OTT model (McKenna and Farell, 2006).

Recently, Buzas and Culver (2009) reported a pattern different from the OTT model: that

sediment-dwelling protists (foraminifera) have more originations outside of the tropics. For

these protists, none of the three existing evolutionary models are applicable. Are there any

metazoan groups that may exhibit a non-tropical origination and diversification pattern that

9

Buzas and Culver (2009) document for protists? The evolutionary diversification pattern for

infaunal metazoans, those that burrow and exploit food-nutrients within the sediment, are not

well studied (Roy et al., 2000). Previously, Thorson (1957) argued that infaunal metazoans lack

a LDG because subsurface benthic habitats were more homogeneous between the tropics and

poles and thus a gradient would not occur. Roy et al. (2000) tested Thorson's hypothesis by

using infaunal and epifaunal marine bivalves from different trophic groups (suspension and

deposit feeders). For nearly all bivalve groups examined, a strong LDG does exist which does

not support Thorson‟s hypothesis. However, Roy et al. (2000) also found that for one important

and highly diverse group of infaunal deposit-feeding bivalves, the protobranchs, a steep

latitudinal gradient was not evident. They discussed numerous ecological and evolutionary

reasons, from a deposit-feeding trophic mode to non-planktotrophic larval development, that

may account for the atypical LDG. Although food within the sediments could be sourced from

surface productivity (Roy et al., 2007), it is possible that a deposit-feeding mode of life coupled

with an infaunal ecological strategy and non-planktotrophic larvae may disrupt the typical LDG.

It is implied that if a clade has planktotrophic larvae, then that group is more likely to have a

typical LDG with a steeply dipping slope toward the poles.

We assessed whether an ecologically-important group of marine animals, the infaunal

irregular echinoids, have a similar LDG as infaunal bivalves and if the OTT model is applicable

to their clade. We also tested the larval hypothesis put forward by Roy et al. (2007) to determine

if larval feeding mode provides a mechanism for explaining LDGs for marine invertebrate

clades. Irregular echinoids are deposit-feeders and are represented by semi-infaunal

clypeasteroids and cassiduloids (sand-dollars, sea biscuits), and the infaunal spatangoids (heart

urchins) (Nebelsick, 1996; Kroh and Smith, 2010). Irregular echinoids have colonized shallow-

10

to-deep water (up to 5000 meters) from the tropics to the polar region of Antarctica, and are

among the most diverse group of echinoderms (Smith, 1984; David et al., 2005). Their

burrowing behavior releases nutrients back into the water column, enhancing benthic marine

diversity in modern seas (Schinner, 1993; Hollertz and Duchene, 2001).

The fossil record of irregular echinoids began in the Jurassic when they diverged from

the epifaunal regular echinoids, such as sea urchins (Smith, 1984). Echinoid diversity increased

rapidly following the origin of irregular echinoids (Kier, 1982). Today, most irregular echinoids

have planktonic larvae (Smith, 1984) but non-planktotrophic (e.g., brooding and lecithotropic)

larvae are more common in polar regions, especially in Antarctica: of the 28 brooding echinoid

species, 25 of them are from Antarctica (Philip and Foster, 1971; Jeffrey, 1997). In a review of

modern echinoderm development McEdward and Miner (2001) found that 38 of 70 (54%)

irregular echinoid species had a planktotrophic larva, and 22 were brooding species from

Antarctica. Non-planktotrophy and planktotrophy can be determined from echinoid skeletons,

and non-planktotrophic echinoids are not known from Paleozoic through the Late Cretaceous (to

Santonian) (Jeffrey, 1997; Cunningham and Abt, 2009). Larval feeding mode can be inferred

from fossil adult specimens by either the presence of brood pouches (no free swimming larvae),

relative enlargement of the gonopores (non-planktotrophic eggs are larger), and crystallographic

orientation of the apical plates (Cunningham and Abt, 2009). After the Santonian Stage, non-

planktotrophic development evolved in numerous echinoid clades, but is rare overall (Jeffrey,

1997). If planktotrophy is the dominant larval feeding mode for irregular echinoids, then we also

would expect that irregular echinoids would have a steep LDG, and not one that follows the

atypical LDG of infaunal protobranchs which have non-planktotrophic larvae (Roy et al., 2000).

However, if planktotrophic irregular echinoids exhibit an LDG like non-planktotrophic

11

protobranch bivalves, then larval feeding adaptations may not be the overall driver of

evolutionary LDGs.

If irregular echinoids do not fit the typical LDG or OTT model, it is possible that an

additional model is warranted, especially in light of the protobranch bivalve clade (Roy et al.,

2000) and infaunal foraminifera (Buzas and Culver, 2009) findings. Here we propose an out of

the extratropics model (OTE) where origination is highest in the extratropics with subsequent

migration of taxa into the tropics. Additionally, we tested whether the paleobiogeographic

patterns were biased by collections (Allison and Briggs, 1993; Jackson and Johnson, 2001; Krug

et al., 2009) or were biased by not taking into account wider tropical regions in the past.

Results

The modern LDG for irregular echinoids declines with increasing latitude but not as

steeply as other organisms (Fig. 2.1A). For example, diversity of marine bivalves drops

precipitously after outside of the tropical boundary (Fig. 2.1B), but irregular echinoid diversity

does not start to decline until 40° latitude. A similar pattern was reported for infaunal

depositing-feeding protobranchs (Roy et al., 2000) (Fig. 2.1C). In contrast to other marine and

terrestrial organisms, irregular echinoid diversity does not plummet at the poles because of the

high modern diversity of irregular echinoids recorded from Antarctic waters at 70° S (Fig. 2.1A).

In fact, suspension- and deposit-feeding bivalves that have known LDGs do not have an increase

in diversity at the poles (Fig. 2.1B, C).

The diversification of irregular echinoid genera from the Cretaceous through the modern

record is higher in extratropical regions than in tropical regions if the tropics are defined as 25o N

and S latitude (Table 2.1; tropics defined after Jablonski et al., 2006). Of the five irregular

12

echinoid genera that originated during the Cretaceous only two (40%) were from tropical areas

(Fig. 2.2). In the Eocene, 26% of irregular echinoid originations were from tropical latitudes,

31% in the Miocene and 78% in the Plio-Pleistocene. The total number of modern echinoid

genera that originated in extratropical habitats (n = 38) was significantly higher (p = 0.02) than

those that originated in tropical habitats (n = 23). When grouped into Neogene and Paleogene

time bins, echinoid extratropical originations were significantly higher for the Paleogene (p =

0.01). Unlike marine bivalves (Jablonski et al., 2006), the extratropics are very important for

irregular echinoid origination and diversification. Additionally, tropical origination of irregular

echinoid taxa increases through the Cenozoic culminating in the Plio-Pleistocene where tropical

originations overshadow extratropical originations.

In modern seas, irregular echinoid genera that originated in extratropical environments

have more species than genera that evolved in the tropics. Modern genera with extratropical

originations have 138 species; for genera that originate in the tropics, there are 55 species. For

genera that originated in the extratropics there are 3.8 species per genus; for the tropics, 2.4

species. Geographic patterns in organisms can be related to their phylogenetic antiquity in

particular regions (Wilson, 1987; Fjeldsaå and Lovett, 1997), could these differences in species

per genera be related to the irregular echinoid phylogenetic legacy in the extratropics? For

irregular echinoid genera that originated in the extratropics, 76% (29/38) have at least one

species found in the tropics, strongly indicating that the extratropics may be the evolutionary

crucible for this clade.

Alternatively, are we undersampling the tropics because, in the past, the tropics existed in

a wider geographical belt? During warmer global periods, for instance, the tropics may have

extended to 30° N and S latitude (Scotese, 2002; Boucot et al., in press). When we re-examined

13

the data using tropical limits of 30° for warmer periods of time, there was no change in species

originations for irregular echinoids for the Late Cretaceous and Paleocene (Table 2.1). But

during the Eocene, 16 genera originated in the tropics compared to 5 when the tropics were

delineated by 25°. During the Oligocene through the Plio-Pleistocene the paleotropical limits

were similar to modern ones (Scotese, 2002; Boucot et al., in press), thus tropical limits were not

increased for those epochs. In total, tropical origination for modern irregular echinoids increased

from 23 to 38 genera when latitudinal limits were expanded to reflect presumed wider tropical

belts in the Eocene. Thus, if tropical belts were wider in the past, this could account for

differences in origination centers.

We also examined whether there was an extratropical collection bias for our data. A total

of 2563 Paleogene-to-Neogene collections that had irregular echinoids were found in the

Smithsonian database and 1349 collections from the Paleobiology Database (PaleoDB). For the

Smithsonian data, collection numbers were highest for each time period at latitudes greater than

25° (Fig. 2.3A). The PaleoDB collections have a similar pattern except that the Oligocene and

Plio-Pleistocene collection peaks occurred at approximately 25° latitude (Fig. 2.3B). Of the total

collections from the Smithsonian 78% were found in either Western Europe or the United States

(57% for the PaleoDB). Only 54 (2.1%) collections from the Smithsonian and 144 (10.6%) of

the PaleoDB collections were found in the Southern Hemisphere. Is this bias because of lack of

sampling in these regions, or a lack of having them in northern hemisphere museum collections?

We do not know.

As an additional test for possible extratropical sample bias we determined how many

modern genera from the tropics and extratropics have had some presence in the fossil tropics and

extratropics. Of the 48 genera that have at least one representative in modern tropical

14

environments 39 (81.3%) have at least one fossil tropical presence. Additionally, of the 40

genera that have at least one extratropical representative in modern oceans, 35 (87.5%) also have

at least one fossil representative. This suggests that the extratropics are only marginally better

represented in the fossil record. Given what we have, there is a remarkable distribution of

irregular echinoids in extratropical regions throughout most of their evolutionary and collection

history. If this is a true trend, then a new model to account for their evolutionary origins is

warranted; whether it stands the test of time will only be known with more focused sampling

effort in the southern hemisphere and paleotropical regions.

Out of the Extratropics Model for Evolutionary Diversification

The LDG for irregular echinoids is distinctly different than bivalves of the OTT model

which posits that origination is highest in tropical regions for all time periods. If the tropics are

defined as 25o N and S latitude, then throughout most of the irregular echinoid history,

extratropical originations and tropical immigrations have dominated. It is only in the Plio-

Pleistocene that irregular echinoids diversified higher in tropical regions than extratropical.

Irregular echinoids do not appear to conform to the OTT model. Thus we propose an out of the

extratropics model (OTE) where extratropical origination dominates and immigration of taxa

into tropical environments explains high modern tropical diversity. Consequently, our out of the

extratropics model may explain why irregular echinoid diversity is highest in the tropics today,

but had higher originations in extratropical regions for most of their evolutionary history (Fig.

2.4). We posit that our OTE model complements prior diversification models and shows that the

extratropics can be major foci for evolutionary innovation. Indeed, an extratropical origin for

terrestrial mammals, reptiles and amphibians is well known (Mueller et al., 2004; Feranac, 2007;

15

Pyron and Burbrink, 2009), and also is reported for infaunal foraminifera (Buzas and Culver,

2009). The extratropics also may be just as important as an ecological evolutionary crucible as

the tropics.

Following (Jablonski et al., 2006), the tempo and mode of species distribution are based

on three variables: origination rates (O), extinction rates (E) and immigration (I); the tropics and

extratropics are denoted by subscripts (T, E). For example, if the tropics and the extratropics had

equal origination rates, then this would be represented by OT = OE. For the OTT model,

origination is highest in the tropical regions (OT>OE) and immigration to the extratropics from

the tropics is high (IT

16

If the tropics are expanded to 30° for time periods when warmer waters possibly

infiltrated high latitudes a transition between the OTT and OTE models may occur. During the

Eocene, echinoid diversity was at its highest, with most of the diversity restricted to the

southeastern United States (Carter, 1987). By increasing latitudinal limits to 30° southeastern

United States irregular echinoid genera would be included in the tropics and may be driving the

apparent increase in tropical originations. The Eocene example shows that how the tropics are

latitudinally defined is critical to paleobiogeographic evolutionary outcomes (Crame, 2002; Roy

and Pandolfi, 2005).

However, if the tropics were 25° for all time periods, extratropical origination is higher

for each time period except for the Plio-Pleistocene, a time of general global cooling. During the

Neogene we find that tropical and extratropical originations were roughly equal for irregular

echinoids. This could be related to Neogene seasonality which was more pronounced at higher

latitudes, favoring a diversity in larval forms that were adapted to a wide-range of nutrient input.

Higher latitudinal echinoids are characterized by non-planktotrophic larvae and this may be one

adaptation to seasonal food fluxes (Jeffrey, 1997; Cunningham and Abt, 2009). Additionally,

non-planktotrophic larval development in irregular echinoids evolves during cooling global

climate (Cunningham and Abt, 2009).

The non-typical LDG observed for both irregular echinoids (with mostly planktotrophic

larvae) and protobranch bivalves (with non-planktotrophic larvae) seems to rule out larval

feeding strategies as an evolutionary driver of invertebrate LDGs. If both of these infaunal

deposit-feeding groups do not conform to the OTT model then it may be that mode of

development is not solely responsible for the LDG. Perhaps the combination of infaunalism and

deposit feeding plays a role in shaping the modern LDG for these groups. It is also possible that

17

extratropical origination for irregular echinoids may be related to their ability to successfully

colonize non-carbonate environments, but this remains to be tested (Barras, 2008).

Is the pattern of high extratropical origination for irregular echinoids merely a product of

sample bias? Extensive collection data from the Smithsonian and PBDB represent extratropical

latitudes, with much of the data from the northern hemisphere, specifically Western Europe and

the United States (see also Smith, 2001). This finding is similar to the Indo-Pacific as a

repository of high biodiversity today but is one of the least sampled paleoenvironments for fossil

molluscs (Jackson and Johnson, 2001; Krug et al., 2009). Alternatively, the irregular echinoid

extratropical collection pattern may be a true approximation of their evolutionary history. For

example, collections do not document whether the paleotropics have been sampled intensely for

irregular echinoids, rather that little has been found. Furthermore, echinoids have been studied

since the 1830s (Kroh and Smith, 2010) and the results of collections from over 180 years yield

few fossil tropical irregular echinoids. Therefore we must ask: are the paleotropics truly

undersampled for irregular echinoids or is the high number of originations in the extratropics a

true pattern? Our work provides a working hypothesis in which to test the validity of the OTE

model, until more work has been completed in the paleotropics. While the tropics are immensely

important, the extratropical and polar regions also maintain large repositories of biodiversity

(Brandt et al., 2007; Cheung et al., 2009), the history of which is just starting to be revealed.

Methods

Data for the latitudinal diversity curve (LDG) were compiled from literature sources that

documented global species diversity of modern irregular echinoids (Ghiold and Hoffman, 1986;

18

1989). Modern irregular echinoid species numbers were obtained for 38 geographic regions and

placed into 10° latitudinal bins both north and south of the equator (Appendix A).

To test the cradle, museum, and OTT model, Sepkoski‟s compendium (2002) was used to

generate the data for living genera of irregular echinoids with a fossil record dating back to the

Early Cretaceous (145 million years ago). Smith's Echinoid Directory (2009) was used to

determine the first appearance of an irregular echinoid genus and the locality the genus

originated in. The first appearance of a species was assigned as extratropical or tropical based on

tropical limits defined as 25° N or S of the equator after Jablonski et al. (2006). For any genus

with a tropical origination, a modern maximum pole-ward limit either north or south of the

equator was determined using Smith‟s Echinoid Directory (2009). For any genus that originated

in the extratropics (greater than 25° N and S of the equator) we determined whether the taxon

had any modern tropical presence (Appendix B). t-test statistics were used to test for

significance in the amount of extratropical versus tropical origination numbers using the latitude

a genera originated in. Data were analyzed using the software package R (2009).

We also examined whether the tropical belt was broader in the past: Warmer waters may

have extended to 30o

during the Late Cretaceous through the Late Eocene and we determined if

broader tropical regions increased the number of tropical originations of irregular echinoids

during those time periods. We used climate data from the PALEOMAP project (Scotese, 2002;

Boucot et al., in press), and found that for all time bins, a strict definition of the tropical limit of

25° N and S latitude is viable based on the presence of bauxite and laterite deposits. To be

conservative, however, the Late Cretaceous and Late Eocene time bins were a time when warm

waters may have infiltrated higher latitudes and thus we applied a 30° N and S latitude tropical

19

limit to those time bins. Once tropical limits were defined for each time period, the numbers of

irregular echinoid originations were recalculated using the same genera listed in Appendix B.

To test whether our data was not biased by monotypic genera the total number of species

per genera were calculated. Smith's Echinoid Directory (2009) was used to calculate the number

of modern echinoid species for each genera used in this study. The number of species per genera

was derived by dividing the number of species in a region (i.e. tropical or extratropical) by the

number of genera.

To determine if the tropical regions were undersampled compared to extratropical regions

global collections data were analyzed for both geographic and collection biases. Collections data

was obtained from the Paleobiology Database (PBDB; http://paleodb.org) and Smithsonian

(http://collections.nmnh.si.edu) online databases (Appendix C). These two databases include

genera from Andrew Smith‟s Echinoid Directory (2009). The number of collections per 10°

latitudinal bin for each time period of the Cenozoic was calculated for each database separately

to test whether the tropics are sampled less than the extratropics. The number of collections in

each hemisphere, Western Europe, and the United States was calculated to determine if a

collections bias is evident for irregular echinoids. If a bias was present then we would expect to

see a higher number of collections for regions outside of the tropics (> 25° latitude).

Acknowledgments

We thank A. J. Boucot for generously allowing access to in press paleoclimate data; A.

J. Boucot, K. K. Davis, and A. Bush reviewed earlier drafts of this manuscript; A. B Smith's

Echinoid Directory provided the baseline data for this study; and B. Carter provided expertise on

southeastern USA echinoids. Supported by grants from the Paleontological Society, Watts-

20

Wheeler Fund (University of Georgia), Southwest Florida Fossil Club, and NSF grant ANT-

0739512.

21

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27

Table 2.1. Number of irregular echinoid genera (includes subgenera) that originated in the

Cretaceous to Plio-Pleistocene. The number of irregular echinoid genera that originated in the

tropics (within 25° N and S latitude) and extratropics are listed; those that originated during a

wider tropical range (within 30o N and S latitude) are listed within parentheses. For the data

within parentheses, the tropical limits are as follows: Cretaceous 30°, Paleocene 30°, Eocene 30°,

Oligocene 25°, Miocene 25°, Plio-Pleistocene 25° (distilled from Scotese, 2002; Boucot et al., in

press). The number of genera originating in the extratropics is higher than in the tropics when

the tropics are assumed to be less than 25° for all time periods. When the tropical zone is

increased to reflect warmer global temperatures the number of tropical originations is higher than

extratropical for only the Eocene time period.

Geologic

Time

Number of irregular genera per

time period that have a modern

distribution

Number

Originated in

Tropics

Number Originated

in Extratropics

Cretaceous

5

2 (2)

3 (3)

Paleocene

3

1 (1)

2 (2)

Eocene

23

5 (16)

18 (7)

Oligocene

6

2 (2)

4 (4)

Miocene

13

4 (4)

9 (9)

Plio-

Pleistocene

11

9 (9)

2 (2)

Total

61 23 (34) 38 (27)

28

Figure 2.1. Comparative latitudinal diversity gradients (LDG) for modern irregular echinoids,

infaunal and epifaunal bivalves. (A) LDG for irregular echinoid species that occur worldwide in

both hemispheres (compiled from Ghiold and Hoffman, 1986; 1989). (B) LDG of marine

bivalves from the Northern hemipshere (adapted from Jablonski et al., 2006) (C) LDG of

infaunal bivalves from the north-eastern Pacific (adapted from Roy et al., 2000). B and C are

presented as contrasts to the irregular echinoid LDG. Grey dashed lines represent 25° tropical

latitude limit. Data for all parts was compiled into 10° latitudinal bins

29

Figure 2.2. Latitudinal differences in tropical (T) and extratropical (E) originations (on the left)

and present-day latitudinal limits of irregular echinoid genera that first occur in the tropics on the

right (the vertical line indicates 25o, the tropical proxy latitude). (A) Cumulative data

represented for all time bins: Late Cretaceous through Plio-Pleistocene. (B) The number of

genera that first appeared in the Paleogene. (C) The number of genera that first appeared in the

Neogene. For the cumulative (A) and Paleogene (B) data sets the difference in origination is

significant [(A) T-test, p = 0.02; (B) p = 0.01], but not significant for (C) . (D) Greatest

latitudinal extent for genera that originate in the tropics.

30

Figure 2.3. Number of collections bearing irregular echinoids per latitudinal bin for Cenozoic

time periods. (A) Collection data from the Smithsonian. (B) Collection data from the

Paleobiology Database. Black dashed line represents the 25° tropical latitude limit.

31

Figure 2.4. Theoretical schematic out of the extratropics (OTE) model (compare to Jablonski et

al., 2006). Red dashed lines denote irregular echinoid lineages that originated in the tropics; blue

solid lines represent lineages that originated in the extratropics. Lineages connected by a

horizontal line are sister taxa. Horizontal lines that cross from extratropical into tropical regions

and vice versa indicate taxa that immigrated into different zones. The dashed horizontal line

indicates the present day. The dotted vertical lines denotes tropical boundaries.

32

CHAPTER 3

TESTING THE INFAUNAL-EVOLUTION HYPOTHESIS: DO DEEP BURROWING

IRREGULAR ECHINODS HAVE REDUCED INCIDENCE OF DRILLING PREDATION?2

2 Miller, J. M. and Walker, S. E. To be submitted to Palaios.

33

Abstract

Predation has been implicated as a main driver of ecological-evolutionary change in

several marine invertebrate groups including mollusks, brachiopods, and echinoderms. In the

echinoderm clade, predation may have provided the evolutionary selective force for the irregular

echinoids to colonize and diversify within sediment starting in the Early Jurassic. However, it is

unknown whether burrowing within sediments (infaunalism) reduces the incidence of predation

for irregular echinoids. To test whether burrowing reduces the frequency of predation, fourteen

species of irregular echinoids from the Late Eocene Ocala Limestone were apportioned to four

burrowing tiers based on test morphology, and the frequency of cassid gastropod predation

(counted by presence of drill holes on the skeletons) was determined for each species. Predation

frequency was greatest in the medium infaunal tier, the next greatest was the deep infaunal tier,

followed by the shallow burrowers and finally, the semi-infaunal tier had the least predation

frequency. These results indicate that burrow depth does not correlate to a reduction in cassid

gastropod predation. Modern irregular echinoids that modify their burrow depth in response to

nutrient quantity may not be restricted to particular depths within the sediment. Therefore, the

infaunal paradigm that predation may have driven these irregular echinoids deeper does not

appear to hold. Rather, the evolution of echinoids into the sediments may be more a function of

food resources rather than escaping predators.

Introduction

Traces of predation (drill holes, repair scars) offer a unique glimpse at ancient

predator/prey relationships (Kowalewski et al., 1998; Huntley and Kowalewski 2007). Predation

has significantly affected the evolution of morphology (Vermeij, 1977; Kelley and Hansen,

1993; Dietl et al, 2000; Vermeij, 2008), behavior (Chattopadhyay and Baumiller, 2007; Casey

34

and Chattopadhyay, 2008), community structure (Aberhan et al., 2006), and diversity (Huntley

and Kowalewski, 2007; Vermeij, 2008). It was proposed, though never tested, that a change to

infaunalism for irregular echinoids (i.e. oligopygoids, clypeasteroids, cassiduloids, spatangoids)

during the early Jurassic was influenced by predation (Kier, 1982; Rose and Cross, 1993; Cross

and Rose, 1994; McNamara, 1994). Implicit in this theory is that the deeper an echinoid can

burrow the less likely a predator may consume it (McNamara, 1994).

Evolution toward a burrowing lifestyle required substantial morphological changes from

an epifaunal mode of life (Kier, 1977). In comparison to their epifaunal counterparts, the first

burrowing echinoids in the Jurassic had a flatter, more elongate test that facilitated unidirectional

movement (Kier, 1982; Smith, 1984). The evolution of specialized burrow-building tube feet,

depressed petals (ambulacra), and fascioles were necessary adaptations for deeper burrowing

(Kier, 1982; Smith, 1984). For example, the tube feet became more shovel-like and longer to

produce and maintain the walls of the burrow (Smith, 1984). Depressed ambulacral petals allow

for a spine canopy that could protect the respiratory pores from becoming clogged with sediment

(Smith, 1984). The appearance of skeletal fascioles that facilitated the movement of oxygenated

water into a burrow allowed colonization to deeper depths for some infaunal echinoids (Smith,

1984; Smith and Stockley, 2005). These skeletal attributes can be used to infer the burrow depth

of fossil echinoids (Nichols, 1959; Carter et al., 1989).

By the Early Cretaceous, all the morphologies related to burrowing had appeared,

resulting in the first adaptive radiation for irregular echinoids throughout the Cretaceous (Kier,

1974; Kier, 1982; Smith, 1984). The end Cretaceous extinctions resulted in diminished irregular

echinoid diversity; declining diversity continued through the Paleocene (Smith and Jeffrey,

35

1998). By the end of the Paleocene about 36% of irregular echinoid genera had gone extinct and

the extinctions may be due to a reduced nutrient supply (Smith and Jeffrey, 1998).

The Eocene was a time when irregular echinoids underwent a second major adaptive

radiation, and by the Late Eocene, global generic and species diversity was higher than at any

other time period (Raup, 1975; Kier, 1974; Smith, 1984). For example, the Late Eocene Ocala

Limestone of the southeastern United States has approximately 36 irregular echinoid species

distributed among 11 families (Oyen and Portell, 2001). The Ocala Limestone is an excellent

unit to test McNamara‟s (1994) hypothesis that deeper burrowing echinoids are preyed upon less

frequently then shallow burrowers because of the high irregular echinoid diversity. However,

only a few Ocala Limestone irregular echinoid species have been analyzed for predation. Gibson

and Watson (1989) examined five species of irregular echinoid from the Ocala Limestone and

found that cassid gastropod drilling predation varied among the species (14-66%). They did not

consider the role burrow depth had on the observed predation patterns.

Full testing of Kier‟s (1974) hypothesis, that predation pressure contributed to

infaunalism in echinoids, is not attempted here. Rather, McNamara‟s hypothesis (i.e., decreasing

predation with increasing burrow depth) will be tested, and its implications for the evolution of

infaunalism in irregular echinoids. If McNamara‟s hypothesis is valid then the shallowest

burrowing echinoids should have the greatest extent of predation traces because they are more

likely to encounter predators. In contrast, the deepest burrowing echinoids would be less likely

to have predatory drill holes on their tests. Alternatively, if predation does not decrease with

increasing burrow depth then other evolutionary hypotheses may account for irregular echinoids

radiation below the sediment-water interface. Smith (1984) has suggested that the irregular

echinoid evolutionary expansion below the sediment-water interface was driven by a change in

36

food acquisition and the ability to exploit open niches (Smith, 1984; Barras, 2007). Additionally,

if predation frequency does not decrease with burrow depth the predator may have selected a

certain size of prey to consume regardless of the prey‟s burrow depth. A predator‟s ability to be

selective for prey that will yield the most food for it‟s effort has been noted previously for

modern and fossil predatory gastropods (Kitchell et al., 1981; Palmer, 1984).

Methods

Irregular echinoid specimens were obtained from museum and field samples collected

from the Late Eocene Ocala Limestone of the southeastern United States (Fig. 3.1). Museum

samples used in this study were from the Florida Museum of Natural History (FMNH) and the

Alabama Geological Survey (AGS). The Ocala Limestone echinoids have been used in

paleoenvironmental (McKinney and Zachos, 1986), biostratigraphic (McKinney, 1984),

paleoecological (Carter, et al., 1989; Carter, 1997) and taphonomic studies (Gibson and Watson,

1989). The Ocala Limestone was deposited as a carbonate ramp during a 3 million year period

during the Late Eocene (Gaswirth et al., 2006). The Ocala Limestone is divided into three parts

based on the presence or absence of three irregular echinoid species (Fig. 3.2). All of the

samples used in this study came from the middle (Williston Formation, middle Late Eocene) and

upper unit (Crystal River Formation, late Late Eocene) of the Ocala Limestone. A total of 774

irregular echinoids representing fourteen species were used in this study.

Burrowing tiers (semi-infaunal, shallow infaunal , medium infaunal, and deep infaunal

tiers) were determined based on irregular echinoid skeletal morphology (Table 3.1).

Morphological characters used to demark burrowing depth were assessed using Nichols (1959),

Smith (1984), and Kanazawa (1992). Relative burrow depths were used instead of absolute

37

depths because we cannot with certainty ascertain the true burrow depth of a fossil species.

Species richness was tabulated as the number of species within each tier and was calculated so

that results could be compared to other studies.

We then examined the irregular echinoid specimens within each burrowing tier for cassid

gastropod drilling predation. Drill holes from cassids were used because of their unambiguous

identification and high preservation potential on the skeleton of the echinoid (Hoffmeister and

Kowalewski, 2001; Kowalewski and Nebelsick, 2003). Cassids drill a circular hole with straight

walls that often have rough, etched edges from acidic secretions (Sohl, 1969; Hughes and

Hughes, 1981; Nebelsick and Kowalewski, 1999). Naticid or muricid predation has not been

documented for either regular or irregular echinoids (Kowalewski and Nebelsick, 2003).

Predation frequency was calculated for each tier and species using the following formula:

PF=(d/n)

where PF is predation frequency, d is the number of specimens with at least one drill hole and n

is the total number of specimens. For example, if all species are pooled and there are 20

specimens in one burrow tier and 15 were found to have a drill hole then the predation frequency

would be 0.75 (15/20) for that tier. Similarly, if 10 specimens of a given species were drilled out

of 20 then the predation frequency would be 0.50 (10/20) for that species. A Spearman

correlation test as used to determine if a statistically-significant positive correlation existed

between burrow depth and frequency of drilling predation.

To determine if cassid predators may select a particular size of irregular echinoid, the

length of all specimens was measured using digital calipers. The irregular echinoids were then

grouped into 10 mm size classes. The predation frequency for each size class was calculated and

analyzed using a non-parametric Kruskal-Wallis ANOVA to determine if a particular size class

38

was more likely to be preyed upon. Correlation and statistical analyses were preformed in R and

significance was determined at an = 0.05 (R Development Core Team, 2009).

Results

Based on test morphology the fourteen species of Ocala irregular echinoid were placed

within four burrow tiers (Table 3.2). The semi-infaunal tier had both the highest number of

species (S = 8) and individuals (n = 581). The semi-infaunal clypeasteroid Weisbordella cubae

had the highest abundance among all species used in this study (n = 221). The next most

speciose tier was the shallow burrowers (S = 3) represented by fewer individuals (n = 70) than

the semi-infaunal group, and comprised 9% of the total individuals. Eupatagus antillarum was

the most abundant species within this group (n = 50). The medium burrowers were the next

speciose tier (S = 2) but had the fewest individuals (n = 27). Agassizia clevei dominated the

medium burrowing tier in terms of abundance (n = 25). Schizaster armiger was the only species

in the deep burrow tier but had the second highest number of total individuals (n=96) which

accounted for 12.4% of the total individuals (Fig. 3.3).

A total of 27 drill holes were found on 774 specimens of irregular echinoid (Table 3.3).

Of these, 14 drill holes (PF = 0.02) were found on irregular echinoids from the semi-infaunal tier

and was the smallest predation frequency among all tiers (Fig. 3.3). Three drill holes (PF = 0.04)

were found on specimens from the shallow burrow tier. The medium burrow tier had the highest

predation frequency (PF = 0.11) represented by a total of three drill holes. Seven drill holes (PF

= 0.07) were found on deep burrowing specimens corresponding to the second highest predation

frequency. Pearson-Product Moment correlation analysis revealed no significant correlation

39

between predation frequency and burrow depth and was not statistically significant (ρ = 0.30; p

= 0.27).

The medium burrower Agassizia clevei had the highest predation frequency (PF = 0.12)

of any other species in the study and was the only species drilled in the medium burrow tier.

Rhyncholampas georgiensis had the second highest predation frequency (PF = 0.10) among all

species and had the highest predation frequency among species in the semi-infaunal tier. The

other two species of Rhyncholampas (semi-infaunal tier) had only one drill hole among 55

specimens. Among the other species of Rhyncholampas, R. conradi had one drill hole while R.

ericsoni had none. Schizaster armiger, the only deep burrowing species in this study, had the

third highest predation frequency (PF = 0.07). The clypeasteroid, Mortonella quinquefaria

(semi-infaunal tier) had the fourth highest predation frequency among all species analyzed.

Eupatagus antillarum (shallow tier) had the next highest predation frequency (PF = 0.06) and

was the only species drilled in the shallow burrow tier. All other drilled species had a predation

frequency below 0.04 and were found in the semi-infaunal tier (i.e., Oligopygus wetherbyi,

Oligopygus haldemani). No predatory drill holes were found on the most abundant species

analyzed, the semi-infaunal clypeaster, Weisbordella cubae.

The test length of Late Eocene irregular echinoids from the Ocala Limestone ranged from

7.1 mm for the smallest specimen to 74.2 mm for the largest (Table 3.4). The largest size class

(71- 80 mm) had the highest frequency predation frequency and no irregular echinoid less than

11 mm in length had a predatory drill hole (Fig. 3.4). The second smallest size class (21-30 mm)

also had the third highest predation frequency (PF = 0.08). Overall, the predation frequency

appears to increase with increasing test length but is not statistically significant (H = 6.7; p =

0.46).

40

Discussion

Irregular echinoid burrow tiers and their importance--Irregular echinoids are one of the

most abundant marine invertebrates from the Ocala Limestone and, because of their burrowing

activities, they could impact the paleoecology of the Ocala significantly. Just by burrowing,

modern infaunal organisms can rework massive amounts of sediment and increase nutrient

richness at the sediment water interface (Davis, 1993; Schinner, 1993; Bird et al., 1999; Hollertz

and Duchene, 2001). Burrowing by the infaunal spatangoid Echinocardium cordatum can

increase the porosity of buried sediments and allow for a nutrient flux to the sediment water

interface (Lohrer et al., 2004). Large populations of Echinocardium can completely rework the

sediment surface in about three days (Lohrer et al., 20005) and bioturbation can significantly

increase oxygen levels at the sediment surface while simultaneously decreasing dentrification

(Widdicombe and Austen, 1998). Increased nutrient supply and oxygen at the sediment-water

interface due to echinoid burrowing may also lead to enhanced benthic diversity (Widdicombe

and Austen, 1998). The burrowing behavior of deeper burrowing organisms can aerate the

sediment at burrow depths where oxygen levels are depleted (Welsh, 2003). It is puzzling that

the ecological structure of fossil infaunal echinoids is not well studied because of how important

modern burrowers can be to the structure and success of a community (Mermillod-Blondin and

Rosenberg, 2006). If modern populations of burrowing echinoids can have major positive

impacts on marine ecosystems then it is likely that the abundant irregular echinoids from the

Ocala Limestone also had similar effects. The four burrow tiers ascertained from the Ocala

Limestone irregular echinoids is an important step in understanding the paleoecological effects

that burrowing echinoids can have on a fossil ecosystem.

41

For irregular echinoids from the Late Eocene Ocala Limestone four burrow tiers may

have been evident. The number of species in each tier decreases with increasing depth into the

substrate. Because 11 of the total fourteen irregular echinoid species are semi-infaunal or

shallow burrowers sediment agitation was probably highest within the first few layers. Most of

the semi-infaunal and shallow species could not live within the sediment but probably ploughed

through the first few layers of substrate. The medium and deep tier continue the decline in

diversity with two and one species respectively. Even though the medium and deep tiers are

represented by the fewest number of species their burrowing behavior may have at least

oxygenated the deeper sediment allowing other less mobile organisms the ability to colonize

those levels.

Does deep burrowing deter predation?-- Currently, several evolutionary hypotheses have

been proposed to explain the evolution of infaunalism for echinoids. Predation is the most

pervasive and may be due in part to cassid predation traces found on fossil echinoids (Ceranka

and Zlotnik, 2003; Kowalewski and Nebelsick, 2003). Furthermore cassids may be the only

gastropod predator on echinoids (Hughes and Hughes, 1981) leading other workers to

hypothesize that the two groups are evolutionarily linked (Rose and Cross, 1993). McNamara

(1994) attributed the offshore migration in a lineage of Miocene Lovenia was a direct response to

increasing cassid gastropod predation. Although not tested, this led him to conclude that

burrowing may have also been a response to escape predation for irregular echinoids. We found

that the incidence of cassid drill holes did not decrease with increasing burrow depth for irregular

echinoids from the Late Eocene Ocala Limestone. Instead, the two deepest burrow tiers show

the highest predation frequency. If cassid gastropods can only burrow into the first few

42

centimeters of the sediment (Kowalewski and Nebelsick, 2003) to feed on echinoids then we

must consider why drill holes are found on deep burrowing echinoids.

Some species of modern irregular echinoids that burrow have also been observed on the

sediment surface. For example, the modern spatangoid Meoma ventricosa burrows as deep as

100 mm into the sediment, but at night, individuals emerge from their burrows because oxygen

levels are depleted (Chesher, 1969). Additionally, both Moira atropos and M. ventricosa must

emerge from their burrows to reproduce (Chesher, 1969), and although the reproduction

behaviors for many modern irregular echinoids is currently unknown, it seems likely that most

must surface to breed.

Some spatangoids seem to occupy the surface of the sediment (i.e. unburrowed) if food

content is higher than within the burrow (Hollertz et al., 1998). For example, modern medium

burrowing spatangoids like Brissopis lyrifera were documented burrowing up to 20 mm within

the sediment (Hollertz and Duchene, 2001). Hollertz (2002) demonstrated that B. lyrifera also

would feed at the surface if organic content was higher than within the burrow. Brisaster

latifrons, a deep-burrowing species (20-50 mm burrow depth; Kanazawa, 1992) were observed

emerging from their burrows and occupying the surface of the sediment for up to several days

before reburrowing (Nichols et al., 1989). The resurfacing behavior was attributed to calming of

upwelling currents and subsequently more food being available on the sediment surface. Thus

for medium and deep burrowing echinoids of the Ocala Limestone increased nutrient levels may

have driven them to the sediment surface and there, they became exposed to predators. Major

adaptive radiations for irregular echinoids also seem to occur following the arrival of novel food

gathering morphologies, strongly indicating that food, rather than predation, may be the selective

agent for irregular echinoid evolution. For example, the evolution of penicillate tube-feet in the

43

Middle Jurassic allowed irregular echinoids to consume fine-grained sediments for the first time

and resulted in the radiation of spatangoid echinoids (Smith, 1984). Barras (2008) found that

penicillate tube-feet evolution coincides with irregular echinoids colonization of fine-grained

sediments. The sand dollars (clypeasteroids) also seem to have diversified following the

evolution of specialized tube feet used in food acquisition (Smith, 1984). Therefore, the

acquisition of food may be more important to irregular echinoid evolution than becoming food

for predatory cassids.

Alternatively, perhaps medium and deeper burrowing echinoids are preyed upon because

they conform to a specific size class that is preferred by the cassid predator. Qualitatively, it

does appear that larger irregular echinoids are preyed upon more often than smaller ones (refer to

Fig.3. 4). However, equally-sized echinoids (based on average test length) were found in a

variety of burrow tiers. It does not appear that the high predation frequency for the medium and

deep burrowing echinoids resulted from size-specific prey selection.

Comparisons to other echinoid predation studies. -- One advantage of using test

morphology to determine burrow tiers is that we can apply those tiers to prior studies on irregular

echinoid predation to determine if predation frequency is controlled by burrow depth. For

example, if we apply the same criteria for assigning burrow tiers to the five species Gibson and

Watson (1989) examined, four of them would have belonged to the semi-infaunal burrow tier.

The other species (Schizaster ocalanus) would belonged to the deep burrowing tier. From their

work, irregular echinoids that would belong to the semi-infaunal tier had a predation frequency

of 0.38. Although they reported S. ocalanus had a drill hole they only examined one specimen.

They found much higher predation frequency for what we could call the semi-infaunal tier, but

they considered bore holes that may not have been produced by cassid gastropods. For example,

44

two holes were found on the test of Schizaster ocalanus but the morphology of the holes may not

be consistent with drill holes produced by a cassid. Rather, they may be the product of

taphonomy.

McNamara (1994) examined cassid predation for eight species of irregular echinoids

from the Early Miocene Mannum Formation. Of his eight species, five can be placed into the

shallow burrowing tier and three to the semi-infaunal tier. Medium and deep burrowing irregular

echinoids were not represented in his data. Predation frequency was lower for the semi-infaunal

tier (0.17) than the shallow burrow tier (0.37). Although predation frequency was considerably

higher for Early Miocene irregular echinoids the pattern of lower predation frequency for the

shallowest burrowing tier is evident. Additionally, much like the two clypeasteroids analyzed in

our study (i.e., Mortonella quinquefaria and Weisbordella cubae) McNamara (1994) found that

Early Miocene clypeasteroids had very few instances of predation. Clypeasteroids have a

relatively small body cavity and may not contain as much soft tissue compared to other irregular

echinoids (Seilacher, 1979). Thus, cassid gastropods may not drill sand dollars because the

amount of food gained from clypeasteroids may not be enough to warrant an attack.

Hoffmeister and Kowalewski (2001) have shown that for fossil bivalves from the

Miocene predation frequency can vary spatially due to either differences in faunal assemblage or

environmental settings. For example, bivalves from their Parathethys clay sample had a drilling

intenstity of 23.9% while those from Parathethys sand had 12.9% . This may explain why the

predation frequency we find is considerably lower than those from other studies. Several other

studies have documented fossil echinoid predation but only examined species that would occupy

one burrow tier. For example, Ceranka and Zlotnik (2005) found a predation frequency of 0.04

45

for three species of the semi-infaunal Echinocyamus. Their predation frequency is similar to

what we found for semi-infaunal echinoids from the Ocala Limestone.

Conclusions

Because the external morphology of irregular echinoids can readily be used to construct a

burrow profile they are useful for delineating habitat complexity in fossil assemblages. Burrow

tiers can yield important insights regarding the habitat complexity of fossil ecosystems and

burrowing can release vital nutrients other benthic organisms require. One of the noticeable

features of the Ocala Limestone is the high abundance and diversity of irregular echinoids.

Thus, irregular echinoids in the Late Eocene Ocala Limestone may have provided a useful source

for the nitrification and oxygenation of the marine benthos. We find that predation frequency is

highest for the deeper burrowing echinoids. This seems to indicate that deep burrowing is not an

effective means of escaping predation for irregular echinoids. McNamara‟s hypothesis that

burrowing may reduce predation is not supported in this work. Because we only examined cassid

predation in relation to burrow depth it may be possible that other predators in part a greater

evolutionary pressure on irregular echinoids. Other predators such as fish and durophagous

arthropods have been observed preying upon modern irregular echinoids (Kowalewski and

Nebelsick, 2003). Thus, we cannot rule out the possibility that predation by non-gastropods may

have caused echinoids to become infaunal in the Early Jurassic For example, the appearance of

durophagous brachyuran crabs in the Early Jurassic (Walker and Brett, 2002) may coincide with

the appearance of infaunalism for echinoids. However, because irregular echinoids continually

return to the sediment surface or alter their burrow depth to obtain food, and they have evolved

specialized food gathering structures, food gathering may be more important in the evolution of

46

infaunalism than predation. Indeed, Smith (1984) has hypothesized that a change in food

acquisition may have resulted in the infaunalization of echinoids. Predation as an evolutionary

driver towards infaunalism is suggested for Mesozoic marine organisms (e.g., Aberhan et al.,

2006 ) but for Late Eocene irregular echinoids it appears that predation may not be the major

driver for infaunalism in this group.

Acknowledgments

We thank S. Ebersole for access to the Alabama Geological Survey fossil collections; R. Portell

of the University of Florida Natural History Museum for generously gaining us access into

Florida limestone quarries; B. Carter provided access to additional limestone quarries and his

expertise on southeastern irregular echinoids. This work was supported by grants from the

Paleontological Society, Watts-Wheeler Fund (University of Georgia) and Southwest Florida

Fossil Club.

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