Trends in Eukaryote Body Size in an Ecological and ...€¦ · This volume examines body size of eukaryotes and its correlates in various temporal and spatial contexts in three distinct

Trends in Eukaryote Body Size in an Ecological and Evolutionary Context

John Warren Huntley

Dissertation submitted to the faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the degree of

Doctor of Philosophy

In Geosciences

Michał Kowalewski, Committee Chair Shuhai Xiao J. Fred Read

Kenneth A. Eriksson Patricia H. Kelley

March 22, 2007 Blacksburg, VA

Keywords: body size, macroevolution, microevolution, morphological disparity,

organismal interactions, climate change

Trends in Eukaryote Body Size in an Ecological and Evolutionary Context

John Warren Huntley

ABSTRACT

Body size is one of the most fundamental quantifiable traits of living or fossil organisms, and understanding it in various temporal and spatial contexts can offer key insights into the process of evolution. This volume examines body size of eukaryotes and its correlates in various temporal and spatial contexts in three distinct studies. The first study investigates the relationship between parasitism and body size of modern bivalve hosts. Individuals of Protothaca staminea were extensively parasitized (86%) by two types of trace-producing parasites. The only significant relationship between parasitism and body size was that spionid mudblister infested clams from one environment were slightly, yet significantly, smaller than their non-infested counterparts. The most obvious pattern regarding body size was that clams from a lagoon were significantly larger than clams from a tidal creek. This size discrepancy could be related to environmental stress, durophagous predators, differing hydrodynamic conditions, or the comparison of differing cohorts. Even though there was no discernible impact of trematode parasitism on bivalve body size, their traces were abundant and easy to identify. Investigators of body size in the fossil record should be aware of these organisms and their possible ramifications for body size studies. The second study, using Quaternary terrestrial gastropods from the Canary Islands, tests the hypothesis of limiting similarity, the idea that two closely related species will alter their size/morphology in order to minimize competition. By integrating amino acid geochronology, stable isotope estimates, and morphometric techniques I was able to more adequately test whether limiting similarity is an evolutionary process or a transient ecological phenomenon. The first prediction of limiting similarity, character displacement, was confirmed. The second prediction of limiting similarity, character release, was not confirmed. It appears that changing climate at the end of the Pleistocene may be responsible for the body size trends, but intraspecific competition likely played a secondary role in the evolution of body size of Theba. The third study addressed the history of body size and morphological disparity of the first 1.3 billion years of acritarch history. The results reject the idea that acritarch body size increased monotonically through the Proterozoic; in fact they displayed non-directional fluctuation. Acritarch body size decreased significantly following the first appearance of Ediacara organisms and gradually rose during the Cambrian. Morphological disparity increased a half billion years before the first taxonomic radiation. Morphological disparity decreased significantly during the snowball earth events and upon the first appearance of Ediacaran organisms suggesting multiple events of selective extinction in the Proterozoic biosphere. Disparity then increased in step with the diversification of acritarch and metazoans through the Cambrian suggesting ecological links between the two groups. Ecological processes, whether extrinsic abiotic processes or biotic interactions, influence the body size and evolution of organisms at wide range of spatial and temporal scales.

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Dedication I dedicate this dissertation to my family, Tom, Frieda and Adam, whose loving support has sustained me these many years. Also to my dear Laura, our new found love has brought me an enjoyment and appreciation of life that I never knew existed. Thank you all for everything you have done for me.

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Acknowledgments This research was funded by a Stephen Jay Gould Grant-in-Aid from the Paleontological Society, a Geological Society of America Graduate Student Research Grant, a Byron Cooper Geosciences Graduate Research Award from the Department of Geosciences (VPI&SU), the Consejería de Educación, Cultura y Deporte of Gobierno de Canarias, the Ministerio de Ciencia y Tecnologia of Spain, the National Science Foundation, and the Petroleum Research Fund (American Chemical Society). I owe an enormous debt of gratitude to my advisor, Mike Kowalewski. You taught me much more than just how to be a scientist. I am grateful that you gave me a chance and for all that you have done for me. To my committee, Shuhai, Fred, Ken and Tricia; thank you for all your support. You have been great teachers, collaborators, reviewers, friends, and mentors. I am grateful to my fellow students in the geobiology and sed/strat groups for their open ears, sharp minds, and meaningful friendships.

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Attributions Chapter Two is currently in press as “Huntley, J.W. (2007) A Modern Baseline for Paleopathology: Neoichnology of Spionid and Trematode Parasites in a Bivalve Host. The Journal of Shellfish Research.” J.W. Huntley conceived the project, collected and analyzed the data, and prepared the manuscript.

Chapter Three is in the final stages of preparation for submission to Evolutionary Ecology Research as “Huntley, J.W., Y. Yanes, M. Kowalewski, C. Castillo, A. Delgado-Huertas, M. Ibanez, M.R. Alonso, J.E. Ortiz, T. de Torres. A Tale of Two Snails: Testing Limiting Similarity in Quaternary Theba.” Previous versions of this manuscript have been through review at Science and Geology. J.W. Huntley conceived the project, performed the statistical analyses, and wrote the paper. Y. Yanes collected, measured and performed chemical analyses on the gastropod specimens with the aid of C. Castillo, A. Delgado-Huertas, M. Ibanez, M.R. Alonso, J.E. Ortiz, and T. de Torres. M. Kowalewski wrote the bootstrap module for SAS and aided in manuscript preparation.

Chapter Four was published as “Huntley, J.W., S. Xiao, and M. Kowalewski. 2006. 1.3 Billion Years of Acritarch History: An Empirical Morphospace Approach. Precambrian Research 144:52-68”. It is reprinted here with permission from J. Huntley. An updated version was published as an invited chapter as: “Huntley, J.W., S. Xiao, and M. Kowalewski. 2006. On the Morphological History of Proterozoic and Cambrian Acritarchs, p. 23-56. S. Xiao and A.J. Kaufman (eds.). Neoproterozoic Geobiology and Paleobiology, Topics in Geobiology: v. 27, Springer.” J.W. Huntley collected data, analyzed the data, and wrote the manuscript. S. Xiao and M. Kowalewski conceived the project. S. Xiao provided data sources and aided in manuscript preparation. M. Kowalewski wrote SAS codes for data analysis and aided in manuscript preparation.

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Table of Contents

Abstract…………………………………………………………………………………....ii

Dedication………………………………………………………………………………...iii

Acknowledgments………………………………………………………………………..iv

Attributions………………………………………………………………………………..v

Table of Contents…………………………………………………………………………vi

List of Figures…………………………………………………………………………….ix

List of Tables……………………………………………………………………………..xi

Chapter 1: Overview……………………………………………………………………..1

References…………………………………………………………………………………5

Chapter 2: Parasitic Worms and Seafood: Implications for Body Size Studies in the

Fossil Record……………………………………………………………………………...6

Abstract……………………………………………………………………………………6

Introduction………………………………………………………………………………..7

Trace-Producing Parasites of Modern Bivalve Mollusks…………………………………8

Materials and Methods…………………………………………………………………...11

Results……………………………………………………………………………………13

Discussion………………………………………………………………………………..15

Conclusions………………………………………………………………………………19

References………………………………………………………………………………..20

Chapter 3: A Tale of Two Snails: Testing Limiting Similarity in Quaternary Theba…..23

Abstract…………………………………………………………………………………..23

Introduction………………………………………………………………………………24

vii

Materials and Methods…………………………………………………………………...25

Results……………………………………………………………………………………28

Discussion………………………………………………………………………………..30

References………………………………………………………………………………..32

Chapter 4: 1.3 Billion Years of Acritarch History: An Empirical Morphospace

Approach…………………………………………………………………………………35

Abstract…………………………………………………………………………………..35

Introduction………………………………………………………………………………35

Methodology……………………………………………………………………………..37

Body Size Analysis………………………………………………………………40

Morphological Disparity Analyses………………………………………………42

Results……………………………………………………………………………………45

Body Size Analysis……………………………………………………………....45

Morphological Disparity Analyses………………………………………………46

Discussion………………………………………………………………………………..55

Body Size History………………………………………………………………..55

Comparative Histories of Taxonomic Diversity and Morphological Disparity….55

Morphological Constraints, Convergence, and Nutrient Stress in the

Mesoproterozoic…………………………………………………………………57

Neoproterozoic Global Glaciations……………………………………………....59

The Coming of Ediacara Organisms and New Ecological Interactions…………61

The Cambrian Explosion of Eukaryotes…………………………………………64

Conclusions………………………………………………………………………………65

viii

References……………………………………………………………………………….66

Chapter 5: Conclusions and Summary Statement………………………………………73

Appendix 1: Size and infestation data for Protothaca staminea………………………..76

Appendix 2: Size data for land snail species Theba arinagae and Theba geminata……79

Appendix 3: Maximum diameter of acritarchs………………………………………….92

Appendix 4: Mean diameter of acritarchs……………………………………………..104

Appendix 5: Diameter of figured acritarchs…………………………………………...108

Appendix 6: Acritarch morphology data………………………………………………124

ix

List of Figures

Chapter 2 Figure 2.1. Microphotographs of parasite traces. A. Trematode-induced pits indicated by arrows. The sinuous vertical line at right is the pallial line. B. Spionid-induced mudblister on antero-dorsal margin of bivalve. C. Two spionid-induced u-shaped borings along the pallial sinus…………………………………………………………………….10 Figure 2.2. Location map of study. A. Map of Washington state. B. Map of San Juan Island, Washington. C. Map of collection sites at Argyle Lagoon and Argyle Creek outlined by circles. Map modified after Stempien (In Press)…………………………...12 Figure 2.3. Infestation frequencies of Protothaca staminea classified by type of parasite (any parasite trace, trematode pits and blisters, spionid mudblisters, and spionid u-shaped borings) and environment………………………………………………………………..14 Figure 2.4. Histograms of bivalve length (mm) classified by environment and type of parasite trace and results of Mann-Whitney U tests. Note that the scales of each axis are equal for all histograms…………………………………………………………………..16

Chapter 3

Figure 3.1. Theba geminata and T. arinagae with morphometric dimensions labeled. 1.) 42.5 kyr (left) and 5.4 kyr (right) T. geminata. 2.) 42.5 kyr (left) and 14.9 kyr (right) T. arinagae. Note how both species became smaller with time……………………………26 Figure 3.2. Map of the Canary Islands and the Chinijo Archipelago. Bulk samples were collected from La Graciosa and Montaña Clara Islets. 1.) Caleta de Guzman-Llano del Aljibe section, Montana Clara Islet. 2.) Morros Negros section, La Graciosa Islet . 3.) Caleta del Sebo-Bahia del Salado section, La Graciosa Islet……………………………27 Figure 3.3. Comparison of δ13C values of T. geminata and T. arinagae. The distributions are statistically indistinguishable. Mann-Whitney U-test for medians and Kolmogorov-Smirnov tests were completed in PAST 1.39 (Hammer et al., 2001)……………………28 Figure 3.4. Morphometrics and size history of T. geminata and T. arinagae. 1.) Scatterplot of PC1 and PC2 scores. 2.) Mean PC1 score ± 95% bootstrap confidence intervals. 3.) Mean geometric mean of natural log transformed shell height (A) and width (B) ± 95% bootstrap confidence intervals……………………………………………….29

Chapter 4

Figure 4.1. Estimates of acritarch taxonomic diversity during the Phanerozoic and early Paleozoic. Bars are adapted from Knoll (1994). Black circles adapted from Vidal and

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Moczydlowska-Vidal (1997). Vertical black lines represent Era boundaries. The dashed vertical line to the left of the Neoproterozoic/Paleozoic boundary represents the first appearance of Ediacara organisms. The gray box represents the Cryogenian Period when multiple global glaciations occurred……………………………………………………..37 Figure 4.2. Size history of acritarchs. Solid circles represent log-transformed mean maximum vesicle diameter of acritarchs (from species descriptions) through time with 95% CI calculated from 1000 iteration naïve bootstrapped sampling distribution. Solid triangles represent log-transformed mean vesicle diameter of acritarchs as measured from figured specimens. Empty circles represent log-transformed average mean vesicle diameter reported in species description (note there were no mean diameters reported for the M2 bin). Insets show correlations between maximum reported sizes and sizes of figured specimens and maximum reported sizes and mean reported sizes. R-sq (R-squared) and p-value from Pearson correlation analysis performed in SAS 9.1………………………………………………………………………………………...46 Figure 4.3. History of acritarch disparity. (A) Mean dissimilarity coefficient ± 1 standard error. (B) MDS Variance. Inset graph displays results of MDS randomization. Center line represents mean variance from 1000 iteration randomization. Lower and upper lines represent 95% confidence intervals. (C) Number of species per formation from this study’s database, color-coded according to sampling intensity (number of processed rock samples) of each formation. The empty circle represents our estimate of species diversity in Paleoproterozoic formations. Vertical black lines represent era boundaries. The gray box represents the Cryogenian. The vertical red line represents the first appearance of the Ediacara organisms……………………………………………...48 Figure 4.4. MDS scatterplots for each geochronological bin and PCA scatter plot for the pooled data. The first panel shows MDS loading chart relating variables to Dim 1 (x-axis) and Dim 2 (y-axis), and the last PCA loading chart relating PCA variables to PCA1 and PCA2. Solid outlines are convex hulls for bin data. Dashed outlines are convex hulls for pooled data representing maximum realized morphospace. Note how MDS and PCA scatter plots and loadings are mirror images of one another……………………………………………………………………………………51 Figure 4.5. Stratigraphic occurrences of morphological characters utilized in this study: 1) spherical vesicle; 2) ellipsoidal vesicle; 3) barrel-shaped vesicle; 4) bulb-shaped vesicle; 5) polyhedral vesicle; 6) medusoid vesicle; 7) cylindrical process; 8) dome-shaped process; 9) tapered process; 10) hair-like process; 11) triangular process; 12) rounded-tip process; 13) capitate-tip process; 14) blunt-tip process; 15) pointed-tip process; 16) funnel-tip process; 17) hollow process; 18) interior of process communicates with interior of vesicle; 19) branching process; 20) processes fuse at tip; 21) enveloping membrane; 22) excystment-like structure; 23) internal bodies in vesicle; 24) concentric ornamentation on vesicle surface; 25) plates on vesicle; 26) multi-celled appearance (vesicles contained in a larger envelope); 27) colonial appearance (aggregation of vesicles); 28) pores in vesicle wall; 29) flange ornamentation; 30) crest ornamentation; 31) costae meshwork surrounding vesicle…………………………………….................53

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List of Tables

Chapter 2 Table 2.1. Results of bionomial test comparing distribution of parasitic traces on left and right valves of Protothaca staminea. Ratio represents the number of right valves having more parasitic traces than left valves to the total number of comparisons………………15

Chapter 4

Table 4.1. Stratigraphic intervals and data sources used in this study…………………..39 Table 4.2. Description of geochronological bins used in this study…………………….40 Table 4.3. Description of morphological characters and coding used in disparity Analyses………………………………………………………………………………….41 Table 4.4. Binning structure for morphometric analyses………………………………...45 Table 4.5. Correlation analyses between measures of disparity and body size…………46 Table 4.6. Correlation analyses between measures of disparity and unequal binning characters………………………………………………………………………………...54

1

Chapter 1

Overview

Body size is one of the most fundamental quantifiable traits of living or fossil

organisms. Size has been correlated with many biological traits including metabolism,

feeding ecology, reproductive rates, abundance, and species geographic range (Brown,

1995). Understanding the context of changing body size in multiple spatial and temporal

contexts can offer key insights into the process of evolution. Investigating body size and

its correlates in various ecological and environmental contexts is the theme of this

dissertation. The chapters are arranged such that there is an initial focus on ecological

time scales (modern live-collected bivalves), to intermediate ecological/evolutionary time

scales (fossil terrestrial gastropods from the last 45,000 years), to decidedly long-term

evolutionary time scales (1.3 billion years of fossil phytoplankton history).

Chapter Two, entitled “Parasitic Worms and Seafood: Implications for Body Size

Studies in the Fossil Record”, investigates the relationship between parasitism and body

size of modern bivalve hosts. Some trematode parasites have been shown to drastically

alter the growth rates of their molluscan host (Ballabeni, 1995; Sorensen and Minchella,

1998, 2001; Taskinen, 1998) resulting in either dwarfism or gigantism. Trematodes have

no body fossil record, but their traces are found as early as the Eocene (Ruiz and

Lindberg, 1989). Trematode parasites have infested molluscan hosts through geologic

time, and their physiological effects on their hosts, if left unnoticed, could produce

spurious results in body size studies. This study was completed at Friday Harbor Labs of

the University of Washington in the summer of 2004. One-hundred one (101) live

specimens of the venerid bivalve Protothaca staminea were collected from adjacent

2

environments: Argyle Lagoon and Argyle Creek. Argyle Lagoon is an intertidal lagoon

with a sandy/muddy substrate; the majority of which remains submerged at low tide. P.

staminea individuals are able to burrow (the typical venerid habit) in Argyle Lagoon.

Argyle Creek is the conduit through which sea water circulates between Argyle Lagoon

and the open waters of North Bay. The substrate of Argyle Creek is primarily composed

of gravel and sand. Individuals of P. staminea cannot burrow in such a coarse-grained

substrate. The live-collected clams were sacrificed, measured and investigated for

parasite-induced traces. A large majority of the individuals possessed parasite-induced

traces. In this chapter these traces are characterized and clam body sizes are compared by

infestation type and environment.

Chapter Three, entitled “A Tale of Two Snails: Testing Limiting Similarity in

Quaternary Theba”, tests the hypothesis of limiting similarity. Limiting similarity is an

outgrowth of the competitive exclusion principle which states that species cannot make a

living in the same way (occupy the same niche) and coexist. One species will have a

competitive advantage over the other, and given enough time will drive it to extinction.

The hypothesis of limiting similarity suggests that closely related species, which overlap

in time and space, will alter their size or shape to minimize competition (Brown Jr. and

Wilson, 1956; Hutchinson, 1959). Limiting similarity has been demonstrated in living

populations and in time-averaged fossil deposits, but it has not been demonstrated in

high-resolution geologic time series establishing it as an evolutionary process and not

merely a transient ecological phenomenon. To that end, this study tests the hypothesis of

limiting similarity in Quaternary terrestrial gastropods from the Canary Islands. Previous

studies, using amino acid geochronology, have established a high-resolution stratigraphy

3

of the fossil deposits covering the last 45,000 years (Ortiz et al., 2006). The subjects of

this study are two congeneric gastropod species Theba geminata and T. arinagae. These

species range through the majority of the sampled section and are always the most

abundant species. Previous work has shown that stable isotope estimates (δ13C) of the

two species are statistically indistinguishable, suggesting that the two species consumed

the same plants in their respective diets. Given that T. geminata and T. arinagae co-

occur throughout their geologic ranges, are always the most abundant species, and had

similar diets they seem to present an ideal system for testing the hypothesis of limiting

similarity. Six linear measurements were made on 642 snails. Multiple proxies of body

size were calculated from these measurements to test the two predictions of limiting

similarity: 1) character displacement (distinct morphologies) will occur when the species

overlap in space and time and 2) character release (convergence of morphologies) will

occur when the species do not overlap. The possible effects of climate change on body

size are also explored.

Chapter Four, entitled “1.3 Billion Years of Acritarch History: An Empirical

Morphospace Approach”, is an exploratory study investigating the history of size and

morphological disparity of some of the earliest eukaryotes in the fossil record. Acritarchs

are organic-walled microfossils of uncertain biologic affinity (though many have been

interpreted as eukaryotic phytoplankton). It has generally been thought that acritarch size

increased monotonically from their first appearance 1.8-1.9 billion years ago through the

Neoproterozoic and decreased dramatically across the Ediacaran-Cambrian boundary

though no data have been presented to support this view. Estimates of taxonomic

diversity suggest that acritarch diversity was low from their first appearance through the

4

Mesoproterozoic. In the early Neoproterozoic diversity began to rise, but decreased

during the mid-Neoproterozoic global glaciations (Hoffman et al., 1998; Kirschvink,

1992). Acritarch diversity rose quickly in the early Ediacaran Period with the advent of

the large Doushantuo-Pertatataka acritarchs, declined drastically in association with the

first appearance of Ediacara organisms, and increased in step with the Cambrian

explosion of metazoan diversity. Given their uncertain taxonomic status and relatively

simple morphology, macroevolutionary studies of acritarchs (Knoll, 1994; Vidal and

Moczydlowska-Vidal, 1997) have been hampered by taxonomic inconsistencies

(Butterfield, 2004). The purpose of this study is two fold: 1) to document the history of

acritarch body size and 2) to provide a taxon-free proxy of acritarch biodiversity from the

Paleoproterozoic through the Cambrian. I surveyed the published literature for body size

data and morphological data from species descriptions. Maximum size and mean size

were recorded from species descriptions. Figured specimens were also measured as a

proxy of body size. Morphological data of species descriptions were recorded as the

presence or absence of 31 characters. The resulting database consists of 778 species

occurrences representing 47 stratigraphic intervals, 247 locations and 1,766 processed

rock samples. Sophisticated computer-intensive techniques (e.g., multivariate

ordinations, similarity indices, randomizations and bootstrapping) were used to

characterize the history of acritarch morphological disparity. These results were

compared and contrasted to estimates of taxonomic diversity and considered in their

ecological and evolutionary contexts.

Chapter Five provides a summary for the results of the chapters of this

dissertation as well as concluding remarks.

5

References

Ballabeni, P., 1995, Parasite-Induced Gigantism in a Snail: A Host Adaptation?: Functional Ecology, v. 9, p. 887-893.

Brown, J.H., 1995, Macroecology: Chicago, University of Chicago Press, 284 p. Brown Jr., W.L., and Wilson, E.O., 1956, Character displacement: Syst. Zool., v. 5. Butterfield, N.J., 2004, A vaucheriacean alga from the middle Neoproterozoic of

Spitsbergen: Implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion: Paleobiology, v. 30, p. 231-252.

Hoffman, P.F., Kaufman, A.J., Halverson, G.P., and Schrag, D.P., 1998, A Neoproterozoic snowball Earth: Science, v. 281, p. 1342-1346.

Hutchinson, G.E., 1959, Homage to Santa Rosalia or why are there so many kinds of animals?: The American Naturalist, v. 93, p. 145-159.

Kirschvink, J.L., 1992, Late Proterozoic low-latitude global glaciation: the snowball Earth, in Schopf, J.W., and Klein, C., eds., The Proterozoic Biosphere: A Multidisciplinary Study: Cambridge, Cambridge University Press, p. 51-52.

Knoll, A.H., 1994, Proterozoic and Early Cambrian protists: Evidence for accelerating evolutionary tempo: Proc. Nat. Acad. Sci. USA, v. 91, p. 6743-6750.

Ortiz, J.E., Torres, T., Yanes, Y., Castillo, C., de la Nuez, J., Ibanez, M., and Alonso, M.R., 2006, Climatic cycles inferred from the aminostratigraphy and aminochronology of Quaternary dunes and paleosols from the eastern islands of the Canary Archipelago: Journal of Quaternary Science, v. 21, p. 287-306.

Ruiz, G.M., and Lindberg, D.R., 1989, A fossil record for trematodes: extent and potential uses.: Lethaia, v. 22, p. 431-438.

Sorensen, R.E., and Minchella, D.J., 1998, Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails: Oecologia, v. 115, p. 188-195.

—, 2001, Snail-trematode life history interactions: past trends and future directions: Parasitology, v. 123, p. S3-S18.

Taskinen, J., 1998, Influence of trematode parasitism on the growth of a bivalve host in the field.: International Journal for Parasitology, v. 28, p. 599-602.

Vidal, G., and Moczydlowska-Vidal, M., 1997, Biodiversity, speciation, and extinction trends of Proterozoic and Cambrian phytoplankton: Paleobiology, v. 23, p. 230-246.

6

Chapter 2

Parasitic Worms and Seafood: Implications for Body Size Studies in the Fossil Record

Abstract

Some parasites have been shown to significantly alter the growth rates of their molluscan

hosts. Parasite-induced dwarfism or gigantism, if undetected, could significantly distort

studies of body size in the fossil record. One-hundred one (101) individuals of

Protothaca staminea were live-collected from Argyle Lagoon (sand/mud substrate; low

energy) and Argyle Creek (gravel/sand substrate; high energy), and examined for trace-

producing parasite infestation. Seventy-four percent (74%) of individuals from Argyle

Lagoon and 98% of individuals from Argyle Creek contained at least one parasite-

induced trace. Epifaunal clams from Argyle Creek were significantly smaller than their

infaunal counterparts from Argyle Lagoon. This size discrepancy between environments

may be related to the reduction of growth rates triggered by environmental stress or

parasitism, increased susceptibility to durophagous predators, differences in

hydrodynamics, or the comparison of different cohorts. Only one predation trace-type

was related to body size: spionid mudblister-infested clams from Argyle Creek are

significantly smaller than non-infested clams from the same environment. This suggests

that substrate-induced epifaunality and parasite-induced shell-weakening reduced the

bivalves’ defenses against durophagous predators. The frequent occurrence of trematode

and spionid trace-producing parasites in modern bivalve populations suggests that these

traces are common in the fossil record, making the systems amenable to study in deep

time.

7

Introduction

Parasitism and predation are important agents of natural selection, and have likely

had an important impact on the history of life. Studies of parasite-host and predator-prey

interactions have been instrumental in leading to hypotheses such as Red Queen (Van

Valen, 1973) and Escalation (Vermeij, 1987), which have sought to explain various

ecological and evolutionary trends (e.g., increasing armament of gastropods and

infaunalization of some echinoids) and trends in biodiversity through deep time.

Predator-prey interactions and their evolutionary consequences have been documented

extensively in the fossil record (Dietl and Kelley, 2001; Kelley et al., 2003; Kowalewski

and Kelley, 2002; Leighton, 1999).

Parasites greatly outnumber predators in terms of number of individuals and

diversity. Moreover, some parasites may dramatically increase or decrease the growth

rates of their hosts (Ballabeni, 1995; Sorensen and Minchella, 1998 & 2001; Taskinen,

1998). Such a phenomenon, if undetected, could produce spurious results in body size

studies of fossil lineages. The reporting of parasitism in the fossil record is much less

common than the reporting of predation, and studies of long-term trends of parasite-host

interactions in the fossil record are rare indeed (Boucot, 1990; Brett, 1978; Cameron,

1967; Clarke, 1921; Conway Morris, 1981 & 1990; Feldman and Brett, 1998; Feldmann,

1998; Fry and Moore, 1969; Gahn and Baumiller, 2003; Moodie, 1923; Ruiz and

Lindberg, 1989; Savazzi, 1995).

Is the reporting of parasites in the fossil record rare because they are infrequently

preserved, or because they are seldom looked for? Perhaps parasite traces are quite

common in the fossil record. The purpose of this study is to investigate the occurrence of

8

trace-producing parasites in two populations of modern bivalves. What proportions of

the populations are infested with parasites? Are the parasites valve-selective? Is there a

relationship between body size and infestation? The answers to these questions will be

an important first step toward developing a modern baseline against which to compare

the infestation of metazoans, and elucidate their implications, for the fossil record.

Trace-Producing Parasites of Modern Bivalve Mollusks

Various parasites infest modern bivalve mollusks, but at least two types of

parasites leave traces in their bivalve hosts thus making them ideal for study in the fossil

record: trematodes (Phylum Platyhelminthes, Class Trematoda, Order Digenea) and

spionid polychaetes (Family Spionidae, Genera Polydora, Boccardia, and

Pseudopolydora)(Blake and Evans, 1973; Ruiz and Lindberg, 1989). Given the ubiquity

of these parasites today, traces of their activity should also be common in the fossil

record.

Trematodes are a class of parasitic worms some of which spend part of their

complex life cycle in bivalve mollusks. Trematode infestation results in damage to or

total destruction of the bivalve’s gonads, thus resulting in either impeded ability or

inability to reproduce. Infestation can influence growth rates of the host in various ways,

though the effects are far from straight forward. Parasite-induced castration can lead to

increased growth rates and gigantism by either: 1) diverting energy that would have been

used in reproduction into growth or by 2) triggering rapid growth as a host adaptation so

as to outlive or sequester the parasite. Trematode infestation can also stunt the growth of

its host by diverting energy and resources that would have gone into growth (Ballabeni,

1995; Sorensen and Minchella, 1998 & 2001; Taskinen, 1998). Trematode infestation

9

represents a significant agent of natural selection to their bivalve hosts. There is no body

fossil record for trematodes; however their presence is indicated as oval pits and blisters

within the pallial line on the interior of bivalves (Fig. 2.1). Thin-section examination

reveals that growth bands are deformed around these pits (Ruiz and Lindberg, 1989).

This deformation indicates that the pit formed while the clam was living, thus reducing

the possibility of misidentification of such parasitic traces with post-mortem borings (i.e.

Cliona).

Spionid polychaetes bore dwellings into bivalves, gastropods, brachiopods, corals,

and other hard substrates through chemical dissolution (Blake and Evans, 1973; Thayer,

1974; Zottoli and Carriker, 1974). The spionids gain a cryptic habitat by boring, and

weaken the shell of their host; thereby making it more susceptible to its own predators.

By narrower definitions of parasitism spionids might not classify as parasites. Spionids

do not gain nutrition from their hosts. In fact they are suspension feeders and facultative

deposit feeders (Lindsay and Woodin, 1992). However, for the purposes of this study I

will adopt a broader definition of parasitism as spionid infestation can undermine the

structural integrity of the host’s shell.

Spionids produce three types of burrows/borings: surface fouling, mud-blisters,

and u-shaped borings (Fig. 2.1). In surface fouling, spionids produce their burrows in

accumulated mud on the surface of the shell, and do not penetrate the shell. Mud-blisters

are formed when spionids settle on the growing margin of the host. The host attempts to

grow around the spionid, and a blister is formed that is filled with mud by the boring

worm. U-shaped borings are produced by chemical dissolution of the host’s shell. The

10

Figure 2.1. Microphotographs of parasite traces. A. Trematode-induced pits indicated by arrows. The sinuous vertical line at right is the pallial line. B. Spionid-induced mudblister on antero-dorsal margin of bivalve. C. Two spionid-induced u-shaped borings along the pallial sinus.

11

simplest morphology is produced by a single bore hole that penetrates the shell, turns 180

degrees, and emerges adjacent to the initial boring, producing paired holes at the surface

of the shell. U-shaped borings can be more complex with many undulations of the single

borehole (Blake and Evans, 1973; Zottoli and Carriker, 1974).

Surface fouling has little chance of being preserved in the fossil record as it is

merely an accumulation of mud on the surface of the shell, and will not be addressed

further in this study. U-shaped borings are readily preserved in the fossil record (Blake

and Evans, 1973); however the fossil record of u-shaped borings could produce

ambiguous information about the biotic interaction between parasite and host, as they can

be formed pre- or postmortem. Mud-blisters have the most potential for elucidating the

history of spionid-bivalve interactions in the fossil record as they can only be produced

when the host is alive.

Materials and Methods

The molluscan biota from San Juan Island (Washington, US) is an ideal system

for examining the relationships between molluscan hosts and parasites and their possible

connection to body size. A total of 101 live specimens of the venerid bivalve Protothaca

staminea were collected between August 10-17, 2004 from the intertidal sand/mud

substrate of Argyle Lagoon (50 infaunal specimens) and the intertidal gravel/sand

substrate of Argyle Creek (51 epifaunal specimens: the bivalves can not burrow in the

gravel) (Fig. 2.2).

Argyle Lagoon is a shallow body of marine water connected to the open waters of

Argyle Bay and North Bay via Argyle Creek. Even though Argyle Lagoon is in the

intertidal environment, it is sufficiently deep that the bottom is only exposed at the

12

Figure 2.2. Location map of study. A. Map of Washington state. B. Map of San Juan Island, Washington. C. Map of collection sites at Argyle Lagoon and Argyle Creek outlined by circles.

margins during low tide. Argyle Creek is a shallow high-energy tidal creek through

which circulation is conducted between Argyle Lagoon and Argyle Bay.

Protothaca staminea is a very common bivalve in shallow sandy environments in

the Pacific Northwest region (Kozloff, 1993), and is one of the dominant bivalves in the

study area (Lazo, 2004; Stempien, In Press). It is a typical member of the Family

Veneridae, one of the most evolutionary and ecologically successful bivalve clades (Cox

et al., 1969).

The bivalves were sacrificed and measured for anterior-posterior length and

dorsal-ventral width. The numbers of parasite traces (trematode-induced pits and blisters,

spionid u-shaped borings and mud-blisters) were counted for the left and right valves.

Pits are considered to be diagnostic of trematode infestation, while trematodes and other

irritants can produce blisters (Ruiz and Lindberg, 1989). The pit and blister count may

overestimate trematode infestation, but may be a more accurate estimate of total parasite

infestation of a host.

In order to determine if parasites were valve selective within the individuals they

infest, the number of valves with pits/blisters, u-shaped borings and mud-blisters were

13

tallied for left and right valves, respectively, from both locations. Each individual was

coded with a value of zero (0) if the left valve had more parasitic traces than the right or

coded with a value of one (1) if the right valve had more parasitic traces than the left.

The data were analyzed using a binomial test with an assumed probability of 0.5.

Each individual was classified for the presence or absence of any parasite trace,

trematode pit/blister, spionid mud-blister, spionid u-shaped boring, and by its

environment (lagoon or creek). Mann-Whitney U tests were performed using PAST 1.37

(Hammer et al., 2001) to investigate differences in median size between bivalves from

the two environments and between parasitized and non-parasitized bivalves within each

environment. An α=0.05 was assumed for all statistical analyses. The results of statistical

tests for length and width were identical, therefore only length is reported here.

Results

Live-collected specimens of P. staminea from Friday Harbor exhibited very high

parasite infestation frequencies. Eighty-six percent (86%) of individuals examined in this

survey contained at least one parasite-induced trace on its shell (Fig. 2.3). Seventy-four

percent (74%) of bivalves from Argyle Lagoon and 98% of bivalves from Argyle Creek

contained at least one parasite-induced trace. Sixty-eight percent (68%) of Argyle

Lagoon bivalves and 57% of Argyle Creek bivalves possess traces attributable to

trematode parasites. Spionid mudblisters were located in 24% of Argyle Lagoon bivalves

and 75% of Argyle Creek bivalves. Spionid u-shaped borings were found only in Argyle

Creek bivalves (57%).

14

Figure 2.3. Infestation frequencies of Protothaca staminea classified by type of parasite (any parasite trace, trematode pits and blisters, spionid mudblisters, and spionid u-shaped borings) and environment.

Trematode and spionid parasites were not valve selective when infesting P.

staminea (Table 2.1). The binomial tests examining valve selectivity of all three trace

types (trematode pits and blisters, spionid mudblisters, and spionid u-shaped borings)

were insignificant when comparing bivalves from each environment (Argyle Creek and

Argyle Lagoon) separately.

Protothaca staminea from Argyle Lagoon (M=45.7 mm) were significantly larger

(p<0.001) than those from Argyle Creek (M=36.5 mm; Fig. 2.4). Therefore median sizes

of infested versus non-infested bivalves need to be evaluated separately for each

environment. There were no significant differences in anterior-posterior length between

infested and non-infested bivalves with regards to any parasite trace from either

15

Table 2.1. Results of bionomial test comparing distribution of parasitic traces on left and right valves of Protothaca staminea. Ratio represents the number of right valves having more parasitic traces than left valves to the total number of comparisons. Argyle Creek Argyle Lagoon

15:28 15:29 Trematode Pits/Blisters p=0.71 p=0.65 19:32 4:11 Spionid Mud-blisters

p=0.89 p=0.27 10:26 Spionid U-Shaped Borings

p=0.16 No U-shaped borings

from lagoon.

environment with one exception. Protothaca staminea infested with spionid mudblisters

(M=36.0 mm) from Argyle Creek were significantly smaller (p=0.02) than non-infested

individuals (M=39.3 mm; Fig. 2.4).

Discussion

Parasite infestation frequencies of P. staminea reported in this study are very

high, and are by and large much larger than values of drilling predation intensity of

bivalves, gastropods, brachiopods, and echinoderms reported in the paleontological

literature (Kelley and Hansen, 2003; Kowalewski et al., 1998; Kowalewski et al., 2005).

The traces of these parasites do not indicate the death of the bivalve (as most drill holes

on bivalves likely do); however they likely indicate a significant agent of selection.

Trematode parasites consume the gonads of their bivalve host, resulting in the loss or

limitation of the host’s fecundity. The boring and blister-forming behavior of spionid

parasites reduces the strength of the bivalve’s shell. Weakened shells make bivalves

more vulnerable to their durophagous predators (Vermeij 1983, 1987 & 2004).

Given the high infestation frequencies of bivalves it is likely that parasite traces

on molluscan hosts are common in the fossil record, and suffer a lack of attention by

invertebrate workers. Such a fossil record of parasite-host interactions would be as useful

16

Figure 2.4. Histograms of bivalve length (mm) classified by environment and type of parasite trace and results of Mann-Whitney U tests. Note that the scales of each axis are equal for all histograms.

as the well-studied drilling predator-molluscan/brachiopod/echinoderm prey systems in

elucidating organismal interactions in deep time. It is time that workers begin to devote

17

more attention to not only identifying, but quantifying, the relationship between

invertebrate hosts and their trace-producing parasites. One caveat, however, is that the

shell-weakening activity of void-producing parasites (spionids) could make the valves of

their hosts more susceptible to taphonomic processes, thereby making their occurrence

less obvious. The taphonomic effect of parasite-induced voids upon valves can be

quantified by examining whole shells and shell fragments for tell-tale spionid-induced u-

shaped borings and mudblisters. A higher frequency of parasite traces in valve fragments

than in whole shells would suggest a taphonomic bias. This bias should not be as

important when considering trematode traces as they typically leave much smaller voids.

Spionid infestation frequencies were typically higher in the epifaunal clams from

Argyle Creek than in the infaunal clams of Argyle Lagoon. There appears to be little

difference in trematode infestation frequencies between infaunal and epifaunal clams.

These results are to be expected as spionids are suspension-feeding polychaetes. Feeding

is much easier for a suspension-feeder that makes its home on an epifaunal clam rather

than on a clam buried in the mud. Trematodes, however, are endoparasites that feed on

bivalve gonads; therefore it is not surprising that there is little difference in infestation

frequencies between infaunal and epifaunal hosts.

Trace-producing parasites were shown not to be valve-selective in our samples.

This result suggests that there is no advantage for a parasite to live on one valve or the

other. This is to be expected since the bivalve hosts are equivalved. The non-selectivity

of parasites between host valves maximizes the likelihood of detecting this phenomenon

in the fossil record.

18

Infaunal P. staminea from Argyle Lagoon were significantly larger than epifaunal

individuals from Argyle Creek. A number of scenarios (perhaps working in combination

with one another) might explain this phenomenon and are discussed below. 1) The

epifaunal clams from Argyle Creek may be experiencing greater stress (e.g., occasional

subaerial exposure and the inability to burrow) than their lagoonal counterparts thus

reducing their growth rates. In order to calculate growth rates, one must know the age as

well as the size of the clam. The ages of the bivalves are not known, and the estimation

of age through the number of major growth bands in P. staminea is problematic (major

growth bands are difficult to identify) and inaccurate (Berta, 1976). 2) Higher incidence

of parasitism in Argyle Creek may reduce growth rates. Trematode infestation is known

to effect host growth rates in multiple ways (Sorensen and Minchella, 2001; Taskinen,

1998), however regression analyses (the results of which are not shown here) do not

suggest a relationship between the extent of infestation of a bivalve and its length. 3)

Higher incidence of parasitism combined with forced epifaunality may make clams from

Argyle Creek more susceptible to durophagous predators such as crabs, birds, and

raccoons. Spionid-infestation is much more common in Argyle Creek than in Argyle

Lagoon, and the characteristic mudblisters and u-shaped borings likely weaken the shell.

4) Differences in hydrodynamics between the two environments may also affect shell size

and morphology (Vermeij, 1973). 5) The two populations may simply represent different

cohorts. Future investigations of bivalve age (through stable isotope sclerochronology)

and predator-prey interactions in these environments can elucidate the cause of the

disparity in size between these two populations.

19

Clams infested with spionid mudblisters were significantly smaller than those that

were not infested from Argyle Creek. There was no discernable difference in size

between mudblister-infested and non-infested clams from Argyle Lagoon. Again, it is

problematic to determine the cause of this size discrepancy. Given that both groups lived

in the creek differing environmental stress and hydrodynamic conditions can be ruled out

as likely causes. The small difference in size (3.3 mm), though significant, seems to rule

out the possibility that the infested and non-infested clams are from different cohorts.

Spionid infestation is not known to affect growth rates. Perhaps spionid-induced

mudblisters weakened the shells of the Creek bivalves and made them more vulnerable to

their predators thus reducing their likelihood of surviving to a larger size. Once again

further work needs to be done to determine not only the source of this size discrepancy

but the stability of this discrepancy over longer time scales (seasons to years).

Conclusions

• Both populations of live-collected bivalves were extensively infested by trace-

producing parasites.

• There was no relationship between trematode infestation and bivalve body size,

contrary to the mixed results of other studies.

• There was a significant difference in body size between bivalves from different

environments. This discrepancy could be related to one or a combination of the

following: parasitism, environmental stress, durophagous predation,

hydrodynamics, or differing cohorts.

• Bivalves infested by spionid mudblisters in Argyle Creek were slightly, though

significantly, smaller that their non-infested counterparts. Spionid mudblisters

20

likely weaken the host’s valves and make them more susceptible to shell-breaking

predators.

• Even though there was no relationship between trematode infestation and body

size in this case, trematode traces were extremely common and easy to identify.

Investigators of fossil bivalves should be aware of these parasites and their

possible impact on host body size.

References Ballabeni, P. 1995. Parasite-Induced Gigantism in a Snail: A Host Adaptation?

Functional Ecology 9(6):887-893. Berta, A. 1976. An investigation of individual growth and possible age relationships in a

population of Protothaca staminea (Mollusca: Pelecypoda). Paleobios 21. Blake, J. A., and J. W. Evans. 1973. Polydora and related genera as borers in mollusk

shells and other calcareous substrates. The Veliger 15(3):235-249. Boucot, A. J. 1990. Evolutionary Paleobiology of Behavior and Coevolution. Elsevier,

New York. Brett, C. E. 1978. Host-specific pit-forming epizoans on Silurian crinoids. Lethaia

11:217-232. Cameron, B. 1967. Fossilization of an ancient (Devonian) soft-bodied worm. Science

155:1246-1248. Clarke, J. M. 1921. Organic Dependence and Disease. Yale University Press, New

Haven. Conway Morris, S. 1981. Parasites and the fossil record. Parasitology 82:489-509. Conway Morris, S. 1990. Parasitism. Pp. 376-381. In D. E. G. Briggs, and P. R.

Crowther, eds. Palaeobiology: A Synthesis. Blackwell Scientific Publications, Oxford.

Cox, L. R., N. D. Newell, D. W. Boyd, C. C. Branson, R. Casey, A. Chavan, A. H. Coogan, C. Dechaseaux, C. A. Fleming, F. Haas, L. G. Hertlein, E. G. Kauffman, A. M. Keen, A. LaRocque, A. L. McAlester, R. C. Moore, C. P. Nuttall, B. F. Perkins, H. S. Puri, L. A. Smith, T. Soot-Ryen, H. B. Stenzel, E. R. Trueman, R. D. Turner, and J. Weir. 1969. Part N, Mollusca 6, Bivalvia. The Geological Society of America and The University of Kansas, Lawrence, Kansas.

Dietl, G. P., and P. H. Kelley. 2001. Mid-Paleozoic latitudinal predation gradient: Distribution of brachiopod ornamentation reflects shifting Carboniferous climate. Geology 29(2):111-114.

Feldman, H. R., and C. E. Brett. 1998. Epi- and endobiontic organisms on Late Jurassic crinoid columns from the Negev Desert, Israel: Implications for co-evolution. Lethaia 31(1):57-71.

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Feldmann, R. M. 1998. Parasitic castration of the crab, Tumidocarcinus giganteus Glaessner, from the Miocene of New Zealand: Coevolution within the Crustacea. Journal of Paleontology 72(3):493-498.

Fry, G. F., and J. G. Moore. 1969. Enterobius vermicularis: 10,000-Year-Old Human Infection. Science 166:1620.

Gahn, F. J., and T. K. Baumiller. 2003. Infestation of Middle Devonian (Givetian) camerate crinoids by platyceratid gastropods and its implications for the nature of their biotic interaction. Lethaia 36:71-82.

Hammer, O., D. A. T. Harper, and P. D. Ryan. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4(1).

Kelley, P. H., and T. A. Hansen. 2003. The Fossil Record of Drilling Predation on Bivalves and Gastropods. In P. H. Kelley, M. Kowalewski, and T. A. Hansen, eds. Predator-Prey Interactions in the Fossil Record. Kluwer Academic/Plenum Publishers, New York.

Kelley, P. H., M. Kowalewski, and T. A. Hansen, eds. 2003. Predator-Prey Interactions in the Fossil Record. Kluwer Academic/Plenum Publishers, New York.

Kowalewski, M., A. Dulai, and F. Fürsich. 1998. A Fossil Record Full of Holes: The Phanerozoic History of Drilling Predation. Geology 26(12):1091-1094.

Kowalewski, M., A. P. Hoffmeister, T. K. Baumiller, and R. K. Bambach. 2005. Secondary evolutionary escalation between brachiopods and enemies of other prey. Science 308:1774-1777.

Kowalewski, M., and P. H. Kelley, eds. 2002. The Fossil Record of Predation. The Paleontological Society, New Haven, CT.

Kozloff, E. N. 1993. Seashore life of the Northern Pacific Coast: an illustrated guide to Northern California, Oregon, Washington, and British Columbia. University of Washington Press, Seattle.

Lazo, D. G. 2004. Bivalve taphonomy: testing the effect of life habits on the shell condition of the littleneck clam Protothaca (Protothaca) staminea (Mollusca: Bivalvia). Palaios 19(5):451-459.

Leighton, L. R. 1999. Possible latitudinal predation gradient in middle Paleozoic oceans. Geology 27(1):47-50.

Lindsay, S. M., and S. A. Woodin. 1992. The effect of palp loss on feeding behavior of two spionid polychaetes: changes in exposure. Biol. Bull. 183:440-447.

Moodie, R. L. 1923. Paleopathology: an introduction to the study of ancient evidences of disease. University of Illinois Press, Urbana, Illinois.

Ruiz, G. M., and D. R. Lindberg. 1989. A fossil record for trematodes: extent and potential uses. Lethaia 22:431-438.

Savazzi, E. 1995. Parasite-induced teratologies in the Pliocene bivalve Isognomon maxillatus. Palaeogeography, Palaeoclimatology, Palaeoecology 116:131-139.

Sorensen, R. E., and D. J. Minchella. 1998. Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia 115:188-195.

Sorensen, R. E., and D. J. Minchella. 2001. Snail-trematode life history interactions: past trends and future directions. Parasitology 123:S3-S18.

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Stempien, J. In Press. Detecting avian predation on bivalve assemblages using indirect methods. Journal of Shellfish Research.

Taskinen, J. 1998. Influence of trematode parasitism on the growth of a bivalve host in the field. International Journal for Parasitology 28:599-602.

Thayer, C. W. 1974. Substrate specificity of Devonian epizoa. Journal of Paleontology 48(5):881-894.

Van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1:1-30. Vermeij, G. J. 1973. Morphological patterns in high-intertidal gastropods: adaptive

strategies and their limitations. Marine Biology 20(4):319-346. Vermeij, G. J. 1983. Traces and trends of predation, with special reference to bivalved

animals. Palaeontology 26(3):455-465. Vermeij, G. J. 1987. Evolution and Escalation: An Ecological History of Life. Princeton

University Press, Princeton. Vermeij, G. J. 2004. Nature: An Economic History. Princeton University Press,

Princeton. Zottoli, R. A., and M. A. Carriker. 1974. Burrow morphology, tube formation, and

microarchitecture of shell dissolution by the spionid polychaete Polydora websteri. Marine Biology 27:307-316.

23

Chapter 3

A Tale of Two Snails: Testing Limiting Similarity in Quaternary Theba

Abstract

The hypothesis of limiting similarity, which postulates that morphologically similar

sympatric species will differ enough in shape/size to minimize competition, has been

controversial among ecologists and paleoecologists. However, empirical high-resolution

time series demonstrating limiting similarities over longer time scales are lacking. We

have integrated radiocarbon-calibrated amino acid dating techniques, stable isotope

estimates, and morphometric data to test the hypothesis of limiting similarity in late

Quaternary land snails from the Canary Islands over a period of 27,600 yrs. Multiple

proxies of body size consistently show that two endemic congeneric pulmonate gastropod

species (Theba geminata and T. arinagae) maintained a difference in size from ~42,500

BP through the last occurrence of T. arinagae 14,900 BP, with a concomitant trend of a

decreasing body size, possibly related to climate change. Theba geminata did not

converge on the morphology of T. arinagae following its extinction; therefore character

release did not occur. However, T. geminata displayed volatile fluctuation in body size

following the demise of T. arinagae suggesting that interspecific competition may still

have had an effect on the morphological history of these species. The hypothesis of

limiting similarity is partially supported by our findings. This study not only

demonstrates the problems inherent in biological “snapshot” studies and geological

studies of time-averaged deposits to adequately test limiting similarity, but presents a

more adequate research protocol to address the importance of interspecific competition

and limiting similarity in the history of life.

24

Introduction

The theory of limiting similarity is an outgrowth of the competitive exclusion

principle: species can not make a living in identical ways and coexist (Abrams, 1983;

Brown Jr. and Wilson, 1956; Dayan and Simberloff, 2005; Hutchinson, 1959; Macarthur

and Levins, 1967). One way that species can partition their niche is through altering their

body size and/or the size of their feeding structures. Ecologists have uncovered the

occurrence of limiting similarity in a wide array of organisms including butterfly larvae,

ermine and weasels, diverse groups of birds, desert rodent communities, and sand dune

floras (Bowers and Brown, 1982; Dyar, 1890; Hutchinson, 1959; Schoener, 1965; Stubbs

and Bastow Wilson, 2004). However, these examples lack a temporal dimension that

might validate limiting similarity as an evolutionary process rather than a transient

ecological phenomenon. And while paleoecologists did document possible cases of

limiting similarity in deep time – in such diverse groups as Ordovician brachiopods,

Pleistocene land snails, and Devonian trilobites (Eldredge, 1974; Hermoyian et al., 2002;

Schindel and Gould, 1977) – these fossil snapshots focused on individual sites rather than

long-term time-series that would allow us to examine limiting similarity in a temporal

context. Limiting similarity seems ubiquitous in diverse biological systems today (as

well as non-biological systems including musical instruments, bicycles, and skillets

(Horn and May, 1977)), but can it be traced persistently over longer time scales?

Fossil land snails represent a tested system for addressing ecological hypotheses

in deep time while minimizing the confounding factor of limited temporal resolution so

common in many paleontological studies (Chiba, 1998; Goodfriend and Gould, 1996).

Here, we test for the occurrence of limiting similarity in Quaternary terrestrial gastropods

25

over a period of 27,600 years. Two predictions can be made if limiting similarity driven

by interspecific competition is a dominant driver of the evolutionary history of the two

species. 1) Morphologies will remain clearly distinct through time. 2) Character release,

or the morphological convergence of one species towards the other following the removal

of the other species, will occur if the species’ ranges become allopatric either in time or

space.

Materials and Methods

We examined the morphological history of the endemic sympatric species Theba

geminata (Mousson, 1857) and Theba arinagae (Gittenberger and Ripken, 1987) from

the Quaternary deposits of the Chinijo Archipelago of the Eastern Canary Islands (Figs.

3.1 and 3.2). These species were chosen because they are the most abundant species in

the Eastern Canary Islands (Gittenberger and Ripken, 1987; Gittenberger et al., 1992) and

because they both occur through the majority of the sampled fossil record (Castillo et al.,

2002; Yanes et al., 2004). Standardized bulk sampling of dune and paleosol deposits and

live collecting of modern snails resulted in 413 specimens of T. geminata and 229

specimens of T. arinagae suitable for morphometric analysis. T. geminata and T.

arinagae were the most abundant gastropod species identified from the bulk samples.

Age dates for these deposits were estimated using radiocarbon-calibrated amino acid

racemization rates (Ortiz et al., 2006; Yanes, 2005).

26

Figure 3.1. Theba geminata and T. arinagae with morphometric dimensions labeled. 1.) 42.5 kyr (left) and 5.4 kyr (right) T. geminata. 2.) 42.5 kyr (left) and 14.9 kyr (right) T. arinagae. Note how both species became smaller with time.

Thirty-two individuals of T. geminata and 22 individuals of T. arinagae were

measured for δ13C values. δ13C values of land snails have been interpreted as a reflection

of the proportion of C3 to C4 plants consumed in their diet (Balakrishnan et al., 2005) as

well as inorganic carbonate. Due to statistically significant differences between the

variances of δ13C values between T. geminata and T. arinagae, a Mann-Whitney U-test

(U=282, p=0.22) and a Kolmogorov-Smirnov test (D=0.276, p=0.23) were performed

using PAST 1.39 (Hammer et al., 2001). The δ13C values of T. geminata and T. arinagae

are statistically indistinguishable (Fig. 3.3). In view of the evidence that the two

considered species were congeneric endemics, represented the two most abundant species

sampled, and likely fed on common food sources, it is reasonable to infer that they were

long-term competitors. They offer a model system to test if limiting similarity can persist

over longer-time scales.

27

Figure 3.2. Map of the Canary Islands and the Chinijo Archipelago. Bulk samples were collected from La Graciosa and Montaña Clara Islets. 1.) Caleta de Guzman-Llano del Aljibe section, Montana Clara Islet. 2.) Morros Negros section, La Graciosa Islet . 3.) Caleta del Sebo-Bahia del Salado section, La Graciosa Islet.

Specimens that possessed between four and five whorls were selected for

morphometric analysis to minimize ontogenetic-related variation in size and shape.

Traditional measurements were taken, rather than landmark data, due to the difficulty of

defining homologous landmarks on globose snails. The resulting matrix of 6 linear

measurements (mm) from 642 individuals was log-transformed and subjected to a

Principal Components Analysis (PCA) on a variance-covariance matrix using PAST

1.38b (Hammer et al., 2001). PC1 scores for each species were grouped a posteriori into

age categories. Geometric means of log-transformed shell height and shell width were

calculated for each individual as a second proxy of body size (Kosnik et al., 2006).

28

Figure 3.3. Comparison of δ13C values of T. geminata and T. arinagae. The distributions are statistically indistinguishable. Mann-Whitney U-test for medians and Kolmogorov-Smirnov tests were completed in PAST 1.39 (Hammer et al., 2001).

For each age category, PC1 scores and geometric means were resampled with

replacement 1000 times and mean scores were recomputed using a balanced bootstrap

module written in SAS/IML (Kowalewski et al., 1998). The percentile approach, or

naïve bootstrap (Efron, 1981), was used to calculate 95% confidence intervals (CI) from

the bootstrapped sampling distributions.

Results

The first principal component (PC1) accounts for 95.5% of the variation in the

data matrix while PC2 and PC3 account for 1.9% and 1.3% of the variation, respectively

(Fig. 3.4). The two species show the most separation along PC1. Variation along the

first principal component has often been attributed to differences in size.

29

Figure 3.4. Morphometrics and size history of T. geminata and T. arinagae. 1.) Scatterplot of PC1 and PC2 scores. 2.) Mean PC1 score ± 95% bootstrap confidence intervals. 3.) Mean geometric mean of natural log transformed shell height (A) and width (B) ± 95% bootstrap confidence intervals.

While this is an interpretation that should not be made without careful consideration, it

especially seems to be true in this case as all six morphological variables are highly

positively correlated with PC1 values (r>0.96). In addition PC1 is considered an

30

appropriate proxy of body size in this case as it is a reflection of six linear measurements

instead of one (e.g., length or width).

The PCA ordination, based on linear dimensions, suggests that there are

significant size-driven differences in morphology between T. geminata and T. arinagae

(Fig. 3.4). The morphological history of the two congeneric species is remarkably

concordant through time: whether estimated by the mean PC1 score or the mean

geometric mean value (Fig. 3.4), the temporal trends in body size of two snails parallel

each other perfectly. The two proxies of body size are stable between 42.5 and 29.4 kya.

Beginning at 29.4 kya, both species undergo a reduction in body size at similar rates.

This trend ends at 14.9 kya with the last occurrence of T. arinagae.

Following the last occurrence of T. arinagae at 14.9 kya, T. geminata body size

initially increased and exhibited non-directional, though significant, fluctuation until the

modern. The average shift in body size (approximated by mean geometric mean)

between sequential populations of T. geminata were twice as large following the last

occurrence of T. arinagae (0.166) than sequential populations that co-occurred with T.

arinagae (0.078).

Discussion

The first prediction of limiting similarity was confirmed; the morphology of the

two species remained clearly distinct through time. The parallel temporal tracking in

shell size between the congeneric species and a synchronous reduction in their body size

at a comparable rate is striking, and might seem to suggest that interspecific competition

played an important role in controlling body size of Theba in the Canary Islands

throughout the late Quaternary. However the second prediction of the hypothesis of

31

limiting similarity was not confirmed. Indeed one might mistakenly make a strong case

for limiting similarity were it not for the exceptional stratigraphic resolution afforded by

the radiocarbon-calibrated amino acid racemization age dates. The morphology of Theba

geminata did not converge on that of Theba arinagae following its extinction; therefore

character release did not occur suggesting that interspecific competition was not the

primary force controlling the evolution of these two snails.

The timing of the consistent multi-millennial decline in body size suggests that

snail body size may have been influenced by long-term changes in temperature and

humidity brought about at the end of the most recent glacial period (Beyerle et al., 2003;

Kutzbach et al., 1996; Petit et al., 1999). Indeed, the significant increase in T. geminata

body size between 14.9-11 kyr coincides with the Younger Dryas, a geologically-brief

period characterized by cooler climate in Europe and North America (Cronin, 1999).

The hypothesis of limiting similarity was not fully supported by our data;

however there are clues that interspecific competition may have played a minor role in

controlling the morphologic evolution of the two gastropod species. The body size

histories of T. geminata and T. arinagae were remarkably coherent. Moreover,

morphological shifts of T. geminata were of a higher magnitude and non-directional in

nature following the extinction of T. arinagae perhaps suggesting some type of

constraining force imposed during the temporal overlap of the two congeners.

This study highlights the difficulties of testing whether limiting similarity driven

by interspecific competition is a transient ecological phenomenon or an evolutionary

process. Studies focused on modern biological systems, though they have exhibited

many interesting patterns, are found wanting due to their lack of a temporal element.

32

Many geological studies, with the advantage of deep time, are often limited by the effects

of time averaging. This study has shown that the hypothesis of limiting similarity can be

tested more adequately by integrating multiple geochemical and morphometric

techniques. Interpreting the results may not always be as simple as supporting or

rejecting a null hypothesis. In this case we interpret that climate change was an important

control of snail morphology followed closely by interspecific competition.

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34

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35

Chapter 4

1.3 Billion Years of Acritarch History: An Empirical Morphospace Approach

Abstract

Acritarchs are a group of organic-walled vesicular microfossils interpreted as protists,

and are among the first eukaryotes preserved in the fossil record. Taxonomic

inconsistencies amongst acritarch workers have made it difficult to address the

evolutionary history of this group through more traditional methods (i.e. biodiversity

through species counts). We have constructed an empirical morphospace to examine the

first 1.3 billion years of acritarch evolution. We show that protist morphologic evolution

is broadly correlated with major environmental and biologic revolutions in Earth history

such as late Neoproterozoic global glaciations, the first appearance of the Ediacaran

metazoans and the Cambrian explosion. Our results also show that protist morphologic

expansion precedes their taxonomic diversification; this pattern, similar to that seen in

Phanerozoic animal clades, suggests that early morphospace saturation and convergence

are common occurrences in eukaryote macroevolution. Our data do not support a

monotonic increase in maximum diameter of acritarch vesicles through the Proterozoic;

instead, maximum vesicle diameter appears to fluctuate in the Proterozoic before

decreasing significantly in the early Cambrian.

Introduction

Acritarchs, a group of decay-resistant organic-walled vesicular microfossils,

dominate the fossil record of Proterozoic (2500-542 Ma) and Cambrian (542-488 Ma)

protists. Most acritarchs from the Proterozoic and Paleozoic are interpreted as unicelled

photosynthetic protists, though some may represent multicellular algae (Mendelson,

36

1987; Butterfield, 2004), and a few have been tentatively interpreted as fungi

(Butterfield, 2005). Acritarchs are among the oldest eukaryotes in the fossil record

(Zhang, 1986; Yan, 1991) and offer the earliest adequate data to assess the history of

protistan biodiversity (Knoll, 1994; Vidal and Moczydlowska-Vidal, 1997).

Previous estimates of acritarch diversity suggest that the number of acritarch

species was low from the first occurrence in the Paleoproterozoic to as late as the early

Neoproterozoic (Fig.4.1). Acritarch taxonomic diversity began to increase through the

Neoproterozoic, but suffered a decline during mid-Neoproterozoic glaciation events. An

unprecedented, though short-lived, diversification occurred after these glaciation events,

and was then followed by a taxonomic decline, concurrent with the rise of macroscopic

Ediacara organisms, some of which clearly were metazoans (Fedonkin and Waggoner,

1997). Acritarch taxonomic diversity subsequently increased in step with animal

radiation in the early Cambrian (Knoll, 1994; Vidal and Moczydlowska-Vidal, 1997).

Taxonomic inconsistencies have caused some to question the validity of taxic

measures of protistan biodiversity (Butterfield, 2004). The problem is common in

paleontology, and can be acute in the study of acritarchs. Evolutionary convergence

among simple protists can lead to taxonomic deflation, or an underestimation of

diversity; whereas the heteromorphic alternation of generations can lead to taxonomic

inflation, or an overestimation of diversity (Butterfield, 2004).

The usefulness of morphometric tools in the analysis of Phanerozoic organisms

(Foote and Gould, 1992; Boyce, 2005) encouraged us to use such strategies to

independently clarify the morphological history of acritarchs. If acritarch diversity is

merely a reflection of form taxa in a uniformly populated morphospace, patterns of

37

Figure 4.1. Estimates of acritarch taxonomic diversity during the Phanerozoic and early Paleozoic. Bars are adapted from Knoll (1994). Black circles adapted from Vidal and Moczydlowska-Vidal (1997). Vertical black lines represent Era boundaries. The dashed vertical line to the left of the Neoproterozoic/Paleozoic boundary represents the first appearance of Ediacara organisms. The gray box represents the Cryogenian Period when multiple global glaciations occurred.

morphological disparity and taxonomic diversity should match one another. In contrast, a

mismatch would indicate either inconsistent form taxonomy or unevenly populated

morphospace. By contrasting diversity and disparity patterns, we can also quantitatively

address the issue of morphological constraint and convergence.

Taxonomy aside, quantitative morphological analysis would also allow us to

quantitatively address a number of questions related to acritarch evolution, including,

among others, the relation between acritarch disparity and major environmental and

biotic events. To address these questions, we conducted a literature-based investigation

of the first 1.3 billion years of morphological evolution in the Group Acritarcha.

Methodology

We used a literature-based morphometric approach to examine the evolutionary

history of acritarchs from their first appearance in the Paleoproterozoic through the

Cambrian. An extensive (although by no means exhaustive) literature review, utilizing

38

50 publications (Table 4.1), produced a database of species descriptions from 47

stratigraphic intervals representing 778 species occurrences (the occurrence of a species

in a lithostratigraphic unit), 247 locations and 1,766 processed rock samples. The species

occurrences were assigned to nine geochronological bins based on our best age estimate

of the lithostratigraphic units (Table 4.2).

Size and morphological data were collected from species descriptions and

illustrations published in the literature (Table 4.1). Vesicle diameter was recorded, when

reported, from species descriptions and measured from microphotographs of figured

specimens. Thirty-one morphological characters were identified to quantify acritarch

morphology (Table 4.3). Every species occurrence in the database was coded for the

presence or absence of all 31 morphological characters based on species descriptions of

type specimens found in the literature survey. The resulting database of morphological

characters was comprised of binary variables, where a present character was scored as

one(1) and an absent character was scored as zero(0) (Table 4.3).

The characters applied here (Table 4.3) may at first appear a somewhat redundant

representation (alternative states) of only three characters: vesicle morphology, process

morphology, and process tip morphology. However, these 31 characters, as classified,

are not mutually exclusive. The choice of 31 presence-absence characters, rather than

three multi-state characters, makes it possible to accommodate species descriptions that

reported multiple morphologies (for example, a single species occurrence might have

multiple process tip morphologies). Also, altering our data matrix to combine these

morphologic characters would pose analytical problems, because the calculation of

dissimilarity coefficients requires binary presence/absence data. Finally, and most

39

Table 4.1. Stratigraphic intervals and data sources used in this study.

Bin (Age in Ma) Stratigraphic Interval Reference C3 (488-500) Booley Bay (Moczydlowska and Crimes, 1995) Tempe (Zang and Walter, 1992) C2 (500-520) Kaplanosy/Radzyn (Moczydlowska, 1991) Ella Island (Vidal, 1979) Buen (Vidal and Peel, 1993) Læså (Moczydlowska and Vidal, 1992) C1 (520-540) Mazowsze (Moczydlowska, 1991) Dracoisen/Tokammane (Knoll and Swett, 1987) Taozichong (Yin, 1992) Yurtus/Xishanblaq (Yao et al., 2005) N3 (540-630) Lublin (Moczydlowska, 1991) Doushantuo (Yuan and Hofmann, 1998; Zhang et

al., 1998; Yin, 1999; Zhou et al., 2001; Xiao, 2004b)

Pertatataka (Zang and Walter, 1992) Khamaka (Moczydlowska et al., 1993) Dongjia (Yin and Guan, 1999) Scotia Group (Knoll, 1992) Yudoma Complex (Pyatiletov and Rudavskaya, 1985) N2 (630-720) Tanafjord Group (Vidal, 1981) Tillite Group (Vidal, 1979) N1 (720-1000) Barents Sea Group (Vidal and Siedlecka, 1983) Chuar (Vidal and Ford, 1985) Uinta (Vidal and Ford, 1985) Svanbergfjellet (Butterfield et al., 1994) Visingö (Vidal, 1976b) Eleonore Bay Group (Vidal, 1976a; Vidal, 1979) Vadso Group (Vidal, 1981) Tindir Group (Allison and Awramik, 1989) Wanlong (Gao et al., 1995) Qinggouzi (Gao et al., 1995) Qiaotou (Gao et al., 1995) Draken Conglomerate (Knoll et al., 1991) Hunnberg (Knoll, 1984) Liulaobei (Yin and Sun, 1994) Lone Land (Samuelsson and Butterfield, 2001) Mirojedikha (Hermann, 1990) Bitter Springs (Zang and Walter, 1992) Veteranen (Knoll and Swett, 1985) Wynniatt (Butterfield and Rainbird, 1998) M2 (1000-1270) Ruyang Group (Yin, 1997) Lakhanda (Hermann, 1990)

40

Thule Group (Hofmann and Jackson, 1996) Baichaoping (Yan and Zhu, 1992) Bylot (Hofmann and Jackson, 1994) M1 (1400-1500) Bangemall Group (Buick and Knoll, 1999) Roper Group (Javaux et al., 2001) P1 (1625-1800) Chuanlinggou (Yan, 1982; Luo et al., 1985; Zhang,

1986; Yan, 1995; Sun and Zhu, 2000) Changzhougou (Luo et al., 1985; Yan, 1991; Yan,

1995; Zhang, 1997; Sun and Zhu, 2000)

Table 4.2. Description of geochronological bins used in this study.

Bin Bin Description P1 Paleoproterozoic: 1625-1800 Ma M1 Mesoproterozoic: 1400-1500 Ma M2 Mesoproterozoic: 1000-1270 Ma N1 Pre-Glacial Neoproterozoic: 720-1000 Ma N2 Cryogenian: 630-720 Ma N3 Ediacaran: 540-630 Ma C1 Early Cambrian pre-trilobite: 520-540 Ma C2 Early Cambrian with trilobites: 500-520 Ma C3 Middle and Late Cambrian: 488-500 Ma

importantly, analyses carried out on a non-redundant subset of character states (not

shown here) do not differ notably from the results presented below.

Body Size Analysis

Maximum vesicle diameters were recorded from species descriptions, when available, for

all species occurrences. Figure vesicle diameters were measured from microphotographs

of acritarchs. In addition, mean vesicle diameters, if reported, were also recorded in our

database, but such data are far less complete than the maximum and figure vesicle

diameters. Thus, maximum vesicle diameters were used as a proxy for acritarch body size

history, whereas the mean and figure vesicle diameters were used as a cross-check. The

averages of maximum, mean, and figure vesicle diameters for each geochronological bin

41

Table 4.3. Description of morphological characters and coding used in disparity analyses.

Character Scoring Spherical vesicle? 0=no 1=yes Ellipsoidal vesicle? 0=no 1=yes Polyhedral vesicle? 0=no 1=yes Bulb-shaped vesicle? 0=no 1=yes Medusoid vesicle? 0=no 1=yes Barrel-shaped vesicle? 0=no 1=yes Enveloping membrane surrounding vesicle?

0=no 1=yes

Costae meshwork surrounding vesicle? 0=no 1=yes Triangular processes? 0=no 1=yes Cylindrical processes? 0=no 1=yes Tapered processes? 0=no 1=yes Hair-like processes? 0=no 1=yes Dome-shaped processes? 0=no 1=yes Blunt process tips? 0=no 1=yes Pointed process tips? 0=no 1=yes Capitate process tips? 0=no 1=yes Rounded process tips? 0=no 1=yes Funnel-shaped process tips? 0=no 1=yes Do process tips fuse? 0=no 1=yes Do processes branch? 0=no 1=yes Are processes hollow? 0=no 1=yes Does interior of process communicate with interior of vesicle?

0=no 1=yes

Does vesicle have external plates? 0=no 1=yes Does vesicle have multicelled appearance (vesicles contained in a larger envelope)?

0=no 1=yes

Do vesicles occur in colonial-like clusters (aggregation of vesicles)?

0=no 1=yes

Does vesicle have internal body? 0=no 1=yes Does vesicle have excystment? 0=no 1=yes Does vesicle have pores? 0=no 1=yes Does vesicle have crests? 0=no 1=yes Does vesicle have flange? 0=no 1=yes Does vesicle surface have concentric ornamentation?

0=no 1=yes

were presented in a log-transformed plot. For each bin, maximum diameter values were

resampled with replacement 1000 times and mean size values were recomputed using a

balanced bootstrap module written in SAS/IML (1998). The percentile approach, or

42

naïve bootstrap (Efron, 1981), was used to calculate 95% confidence intervals (CI) from

the bootstrapped sampling distributions.

Morphological Disparity Analyses

The nature of our morphological data matrix lent itself to multiple analytical

approaches to investigate the history of disparity in acritarchs. In fact, it is desirable to

use multiple methods, when possible, to better understand the morphological history of a

clade (Foote, 1997). Therefore, we utilized two methods in this study: 1) an estimation of

within-geochronological-bin-dissimilarity and 2) an exploratory non-metric multivariate

ordination that simultaneously considered all species occurrences from all

geochronological bins.

Pairwise comparison of character differences between species occurrences was

used to calculate mean dissimilarity coefficients for each bin (Sneath and Sokal, 1973;

Foote, 1995). Species occurrences were separated a priori into their geochronological

bins. Pairwise comparison was made between each and every other species occurrence in

the same geochronological bin, and for each comparison a dissimilarity coefficient was

calculated from the number of character differences divided by the total number of

characters (a total of 31 characters). The mean dissimilarity coefficient was then

calculated for each geochronological bin. Pairwise comparisons of character differences

were performed using codes written in SAS/IML interactive matrix language.

Balanced-resampling bootstrap was used to assess the analytical error of the mean

dissimilarity coefficients. For each bin, dissimilarity coefficients were resampled with

replacement 1000 times (Efron, 1981) and mean dissimilarity coefficients were

recalculated. Standard errors were calculated from the resulting bootstrapped sampling

43

distribution. Standard errors are considered the appropriate method for assessing

analytical error, because phylogenetically related organisms are our units of study, and

are therefore not independent observations (Foote, 1994). Bootstrapping and calculation

of standard errors were performed using codes written in SAS/IML interactive matrix

language.

Non-metric multidimensional scaling (MDS) is an exploratory multivariate

ordination technique used to simplify multidimensional data matrices (Kruskal and Wish,

1978; Schiffman et al., 1981; Marcus, 1990; Roy, 1994). MDS is a particularly attractive

method in the case of our data set in that it does not require continuous variables (our

variables are binary presence/absence values) and allows for missing values, unlike

commonly used parametric techniques such as Principal Components Analysis. MDS

was used to create a two dimensional ordination from the original 31 characters of all 778

species occurrences (SAS reported convergence criterion satisfied: 17 iterations were

performed, final badness-of-fit: 0.21). Three and four dimensional ordinations were also

calculated and resulted in the same patterns of variance, but are not reported here. The

MDS procedure calculated two scores (dimension one and dimension two) for each

species occurrence, which was then assigned to a geochronological bin. For each bin,

variances of dimension one and dimension two scores were calculated. The sum of the

two variance scores for each time bin is referred to as MDS variance. Correlation

coefficients (r) were calculated among MDS loadings and original morphological

variables. The MDS procedure was performed using SAS 9.1.

MDS is different from other ordination techniques in that the primary dimension

does not always align with maximum variance of the data. This can make it problematic

44

to relate the dimensions provided by the ordination with the original variables. To

alleviate this concern we subjected the MDS scores (dimensions one and two, which are

continuous) to a principal components analysis (PCA). The PCA produced two scores

(PCA1 and PCA2) for each species occurrence, which was then assigned to a

geochronological bin. For each bin, variances of PCA1 and PCA2 scores were

calculated. The sum of the two variance scores for each time bin is referred to as PCA

variance. Correlation coefficients (r) were calculated among PCA loadings and original

morphological variables. The principal components analysis was performed using PAST

1.33 (Hammer et al., 2001). Interestingly enough, in this case, the primary dimension of

the MDS ordination did coincide with maximum variance of the data. Therefore the

results of the PCA are similar to those of the MDS (they are a mirror image of one

another), and the interpretation of the MDS morphospace in relation to the original

variables should thus be possible.

A randomization with 1000 iterations was performed on the MDS variances to

evaluate the possible range of disparity trends allowed under the null model that disparity

varied randomly through time. The paired MDS scores (dimension one and two scores)

of all 778 species occurrences were randomly shuffled into the geochronological bins to

replicate the original sampling structure, so that 104 paired MDS scores were placed

randomly in the P1 bin, 11 in the M1 bin, and so on (Table 4.4). MDS variance was then

calculated for the values re-assigned to each bin. This randomization procedure was

repeated 1000 times, resulting in a distribution of 1000 variance estimates per bin. We

calculated the mean, 2.5 percentile, and 97.5 percentile values from the randomly

produced distribution of variance estimates for each bin. The MDS randomization was

45

Table 4.4. Binning structure for morphometric analyses.

Bin Species Occurrences P1 104 M1 11 M2 41 N1 248 N2 13 N3 156 C1 54 C2 115 C3 36

performed using codes written in SAS/IML interactive matrix language and the

SAS/STAT Proc MDS module.

Results

Body Size Analysis

The average maximum vesicle diameter of acritarchs displayed non-directional

fluctuation through the Proterozoic (Fig.4. 2). Acritarch body size decreased

significantly across the Neoproterozoic-Paleozoic transition, but increased significantly

by the middle/late Cambrian (though not to the size seen in the late Neoproterozoic). The

mean and figure vesicle diameter displayed a similar pattern, though typically at smaller

sizes (Fig. 4.2). Average maximum diameter and average figure diameter are

significantly positively correlated, and figure data generally underestimate maximum

vesicle diameter (Fig. 4.2 inset). Neither of the disparity metrics analyzed show any

significant correlation with body size for all possible comparisons, including both raw

data and data corrected for autocorrelations by first differencing (Table 4.5).

46

Figure 4.2. Size history of acritarchs. Solid circles represent log-transformed mean maximum vesicle diameter of acritarchs (from species descriptions) through time with 95% CI calculated from 1000 iteration naïve bootstrapped sampling distribution. Solid triangles represent log-transformed mean vesicle diameter of acritarchs as measured from figured specimens. Empty circles represent log-transformed average mean vesicle diameter reported in species description (note there were no mean diameters reported for the M2 bin). Insets show correlations between maximum reported sizes and sizes of figured specimens and maximum reported sizes and mean reported sizes. R-sq (R-squared) and p-value from Pearson correlation analysis performed in SAS 9.1. Table 4.5. Correlation analyses between measures of disparity and body size.

Raw Data First Differences Pearson Pearson r2 p r2 p MDS 0.113 0.38 0.180 0.29 Dissimilarity 0.038 0.62 0.247 0.21

Morphological Disparity Analyses

Mean dissimilarity was very low in the Paleoproterozoic (<0.02; Fig. 4.3A). This

low value starkly contrasts with the high species per formation values calculated from our

database (Fig. 4.3C). We interpret this discordance as an artifact of severe taxonomic

over-splitting in the original literature. Our re-evaluation of the original literature (Yan,

47

1982, 1991, 1995; Luo et al., 1985; Zhang, 1986, 1997; Sun and Zhu, 2000) suggests that

there are only 5-10 distinct acritarch species in our Paleoproterozoic bin. One of the

criteria used to differentiate Paleoproterozoic acritarchs in the original literature is

thickness of vesicle walls. However, vesicle wall thickness is likely susceptible to

taphonomic processes such as degradation and may not be a reliable taxonomic criterion.

Moreover, reports of vesicle wall thickness in species descriptions are overwhelmingly

qualitative (e.g., thick or thin), and are likely not consistently applied between workers.

Thus, vesicle wall thickness is not included as a variable in our data matrix, and our

interpretation of the difference between Paleoproterozoic diversity and disparity should

be viewed with some caution.

A significant increase in mean dissimilarity occurred between the P1 and M1 bin,

with an M1 value of 0.08. Mean dissimilarity coefficients reached a plateau during the

M1 bin that would remain through the early Neoproterozoic (M2=0.10 and N1=0.09). A

slight, yet significant, decrease in dissimilarity occurred during the Cryogenian (N2=0.08

and upper standard error <0.09).

A rapid morphological diversification occurred in the early Ediacaran Period,

resulting in a mean dissimilarity coefficient significantly higher than any seen in previous

bins (N3= 0.15). This increase in morphological disparity, though dramatic, was short-

lived. The first appearance of the Ediacara organisms (~575 Ma) corresponds in time

with a dramatic decrease in acritarch disparity. We did not create a separate

geochronological bin (i.e., 575-542 Ma) due to low data density. All known acritarchs

48

Figure 4.3. History of acritarch disparity. (A) Mean dissimilarity coefficient ± 1 standard error. (B) MDS Variance. Inset graph displays results of MDS randomization. Center line represents mean variance from 1000 iteration randomization. Lower and upper lines represent 95% confidence intervals. (C) Number of species per formation from this study’s database, color-coded according to sampling intensity (number of processed rock samples) of each formation. The empty circle represents our estimate of species diversity in Paleoproterozoic formations. Vertical black lines represent era boundaries. The gray box represents the Cryogenian. The vertical red line represents the first appearance of the Ediacara organisms.

49

from the late Ediacaran are dominated by simple sphaeromorphic leiosphaerid-like

vesicles (Volkova et al., 1983; Germs et al., 1986; Ragozina and Sivertseva, 1990;

Volkova, 1990). Moreover, it would be impossible to calculate a dissimilarity coefficient

(much less mean dissimilarity) in such a bin as our data base contains only one known

named species in this time interval (Fig. 4.3C). Therefore the dramatic decrease in

disparity associated with the first appearance and subsequent diversification of Ediacara

organisms is much more dramatic than Fig. 4.3A suggests.

Mean dissimilarity coefficients increased monotonically through the Cambrian.

Pre-trilobite Early Cambrian mean dissimilarity (C1=0.11) reflects the morphological

diversification following the late Ediacaran drop in disparity addressed above. Mean

dissimilarity coefficients continued to increase significantly through the trilobite-bearing

Early Cambrian (C2=0.12) and Middle and Late Cambrian (C3=0.15), achieving a

disparity level comparable to that of the early Ediacaran (N3). Our database of Cambrian

acritarchs (particularly for the Middle and Late Cambrian bin C3) is admittedly less

comprehensive than Proterozoic acritarchs (for example, Moczydlowska, 1998 is not

included in our database of C3 bin), but the addition of more data in the C3 bin would

only strengthen the pattern of increasing morphological disparity through the Cambrian

(Moczydlowska, 1998).

Non-metric multidimensional scaling analysis shows significant secular variation

in acritarch morphologies (Fig. 4.3B). The trend in variation is unlikely a sampling

artifact as its overall trajectory falls outside of the 95% confidence intervals obtained in

the randomization simulating random (non-trending) disparity trajectories (Fig. 4.3B

inset).

50

MDS variance was very low in the Paleoproterozoic (P1=0.35; Fig. 4.3B, 4.4).

This indicator of low disparity is also in stark contrast with high species richness per

formation reported in the original literature (Fig. 4.3C); again, this discrepancy is

indicative of taxonomic over-splitting and would be reduced with a more realistic

reevaluation of Paleoproterozoic species richness (see above). A significant increase in

MDS variance occurred in the early Mesoproterozoic (M1=1.24), signaling the beginning

of a disparity plateau that would continue through the early Neoproterozoic (M2=1.49

and N1=1.70).

MDS variance decreased during the Cryogenian (N2=1.48) (Figs. 4.3B, 4.4).

This morphological contraction, together with taxonomic decrease (Knoll, 1994; Vidal

and Moczydlowska-Vidal, 1997; Xiao, 2004a), indicates possible acritarch extinction

during the Cryogenian. Further analysis of MDS plots and loading reveals the restriction

of acritarchs from the right-hand side of the morphospace (Fig. 4.4), suggesting that the

Cryogenian acritarch extinction strongly affected acanthomorphic forms. The post-

Cryogenian recovery of acritarchs resulted in the highest MDS variance seen until that

time (N3=2.23).

MDS variance decreased between the early Ediacaran and the pre-trilobite Early

Cambrian (C1=2.04), concurrent with the diversification of Ediacara organisms. MDS

variance increased monotonically through the remainder of the Cambrian in step with the

taxonomic diversification of acritarchs and animals (C2=2.16, C3=2.90).

51

Figure 4.4. MDS scatterplots for each geochronological bin and PCA scatter plot for the pooled data. The first panel shows MDS loading chart relating variables to Dim 1 (x-axis) and Dim 2 (y-axis), and the last PCA loading chart relating PCA variables to PCA1 and PCA2. Solid outlines are convex hulls for bin data. Dashed outlines are convex hulls for pooled data representing maximum realized morphospace. Note how MDS and PCA scatter plots and loadings are mirror images of one another.

52

The dissimilarity coefficient and MDS results, described above, are broadly

supported by the geochronological distribution of morphological characters (Fig. 4.5).

Paleoproterozoic acritarchs typically had spherical vesicles with the occasional medial

split (e.g., Schizofusa sinica; Yan, 1982), enveloping membrane (e.g.,

Pterospermopsimorpha pileiformis), internal bodies (e.g., Nucellosphaeridium magnum),

or concentric surface ornamentation (e.g., Thecatovalvia annulata and Valvimorpha

annulata; Yan, 1995). The Mesoproterozoic saw the first appearance of elliptical

vesicles (e.g., Navifusa; Hofmann and Jackson, 1994), ten process-related characters

(e.g., Shuiyousphaeridium macroreticulatum and Tappania plana), vesicle plates (e.g., S.

macroreticulatum and Dictyosphaera delicata), pores in vesicle walls (e.g., Tasmanites),

and multi-celled and colonial appearance (e.g., Satka squamifera). Of the thirty-one

characters identified in this study, fifteen first appeared in the Mesoproterozoic (nine in

the M1 bin and six in the M2 bin). Many new acritarch morphological features evolved

in the Neoproterozoic. Polyhedral vesicles (e.g., Octoedryxium truncatum), bulb-shaped

vesicles (e.g., Sinianella uniplicata), barrel-shaped vesicles (e.g., Arctacellularia kellerii,

although other species of Arctacellularia may extend to the Mesoproterozoic; Hofmann

and Jackson, 1994), triangular and hair-like processes (e.g., Cymatiosphaera

wanlongensis and Dasysphaeridium trichotum), funnel-tipped processes (e.g., Briareus

borealis), processes that fuse at the tips (e.g., Tappania sp. in Butterfield, 2005), and

flange ornamentation about the vesicle equator (e.g., Simia simica) all appear for the first

time in the Neoproterozoic. Two new morphological characters appeared in the

Cambrian: a costae meshwork that surrounds the vesicle (e.g., Retisphaeridium brayense)

53

Figure 4.5. Stratigraphic occurrences of morphological characters utilized in this study: 1) spherical vesicle; 2) ellipsoidal vesicle; 3) barrel-shaped vesicle; 4) bulb-shaped vesicle; 5) polyhedral vesicle; 6) medusoid vesicle; 7) cylindrical process; 8) dome-shaped process; 9) tapered process; 10) hair-like process; 11) triangular process; 12) rounded-tip process; 13) capitate-tip process; 14) blunt-tip process; 15) pointed-tip process; 16) funnel-tip process; 17) hollow process; 18) interior of process communicates with interior of vesicle; 19) branching process; 20) processes fuse at tip; 21) enveloping membrane; 22) excystment-like structure; 23) internal bodies in vesicle; 24) concentric ornamentation on vesicle surface; 25) plates on vesicle; 26) multi-celled appearance (vesicles contained in a larger envelope); 27) colonial appearance (aggregation of vesicles); 28) pores in vesicle wall; 29) flange ornamentation; 30) crest ornamentation; 31) costae meshwork surrounding vesicle.

and crest-ornamentation—equatorial ornamentation that is similar to flange but does not

circumvent the vesicle resulting in wing-like structures (e.g., Pterospermella solida). It

should be noted that our data for Cambrian acritarchs was not as exhaustive as our

Proterozoic data, and that further investigation would likely reveal more first appearances

of characters in the Cambrian than what we report. Another caveat to note is that

morphological characters in different taxa or in different geochronological bins may not

be phylogenetically homologous or evolutionarily continuous; instead, the presence of a

54

character simply means morphological resemblance, which may be due to convergence or

homology.

The two proxies of morphological disparity used in this study, mean dissimilarity

coefficient and MDS variance, resulted in coherent histories of acritarch morphological

disparity (Fig. 4.3). The agreement of the two methods, the independent verification of

the significance of the trends found by each method (i.e. randomization for MDS and

calculation of standard error for mean dissimilarity), the elimination of allometry as a

confounding factor (i.e., the lack of correlation between non-directional fluctuation in

body size and disparity trends), and the invariance of disparity estimates relative to

unequal binning characters (e.g., temporal duration of bin, number of formations per bin,

number of sampling localities per bin, number of processed rock samples per bin, and

number of species occurrences per bin) (Table 4.6) all attest to the robustness of our

interpreted history of acritarch morphological evolution.

Table 4.6. Correlation analyses between measures of disparity and unequal binning characters.

MDS Variance Mean Dissimilarity Coefficient Spearman Spearman r2 p r2 p Duration of Bin -0.639 0.06 -0.571 0.11 Number of Formations 0.367 0.33 0.428 0.25 Number of Locations 0.092 0.81 0.185 0.63 Number of Samples 0.067 0.86 0.100 0.80 Species Occurrences 0.333 0.38 0.317 0.41

55

Discussion

Body Size History

The non-directional fluctuation of acritarch body size during the Proterozoic does

not confirm the previously held perception that acritarchs increased in size monotonically

during the Precambrian. The significant decrease in body size between the N3 and C1

bins is likely due to the extinction of the large Doushantuo/Pertatataka acritarchs

coincident with the first appearance of the Ediacaran organisms.

The absence of any notable long-term trend in acritarch body size minimizes the

likelihood of mistaking spurious disparity trends due to secular changes in body size

(e.g., morphological disparity may increase due to diffusive increase in body size) with

shifts in size-invariant shape disparity. Moreover, the discordance between body size and

morphospace occupation suggests that the disparity trends discussed below are not a mere

secondary reflection of some trends in body size.

The significant positive correlation between maximum reported body size and

figured specimen size suggests that retrieving body size information from figured

specimens is a legitimate approach for Proterozoic and Cambrian acritarchs when one is

interested in investigating long-term patterns. This technique should prove useful for

future research interests that include documenting body size and morphologic disparity

for acritarchs through the Phanerozoic.

Comparative Histories of Taxonomic Diversity and Morphological Disparity

The overall pattern of morphological disparity (as approximated by mean

dissimilarity coefficients, MDS variance, and stratigraphic ranges of individual

morphological characters) appears to be broadly similar to the taxonomic pattern

56

assembled by other investigators (Knoll, 1994; Vidal and Moczydlowska-Vidal, 1997)

and indicated by our own data (Fig. 4.3C). The dramatic mismatch between

Paleoproterozoic disparity (Fig. 4.3A-B) and diversity (Fig. 4.3C) is clearly due to

taxonomic oversplitting in the original literature. This mismatch disappears if we

consider a more reasonable estimate of Paleoproterozoic taxonomic diversity.

Closer examination of the diversity and disparity patterns, however, reveal some

important differences in the Meso- and Neoproterozoic. Morphological disparity initially

increased significantly by the early Mesoproterozoic (Fig. 4.3, 4.5). In contrast, the first

taxonomic radiation did not occur until the early Neoproterozoic (Fig. 4.1). This increase

in disparity preceded the first major taxonomic radiation by approximately 500 million

years. This statement remains true even if the diversity curve (Knoll, 1994; Vidal and

Moczydlowska-Vidal, 1997) is updated with more recent data (Xiao et al., 1997; Yin,

1997; Javaux et al., 2001).

The pattern of high morphological disparity early in the history of acritarchs is

similar to patterns seen in the evolution of multi-celled organisms in the Phanerozoic.

Many groups of organisms in the Phanerozoic display high morphological disparity early

in their history: Cambrian metazoa (Thomas et al., 2000), marine arthropods (Briggs et

al., 1992), Paleozoic gastropods (Wagner, 1995), seed plant leaves (Boyce, 2005), and

Cenozoic ungulate teeth (Jernvall et al., 1996). Thus, high morphological disparity in the

early evolutionary history appears to be a prevailing, although not universal, pattern

among many groups (Foote, 1997). As far as we know, this study documents the first

example of a similar pattern in protists and in the Precambrian. Morphological

57

diversification preceding taxonomic diversification may be a prevailing pattern in

eukaryote evolution.

Our comparative analysis of disparity and diversity does differ from the results of

other studies. Morphological disparity typically approaches its maximum realized value

early in the history of other clades [e.g., Paleozoic crinoids (Foote, 1995)], but our

analysis reveals periodic expansions of realized morphospace (Fig. 4.3). Because the

Group Acritarcha is undoubtedly polyphyletic and includes organisms from many phyla

or divisions (Butterfield, 2004; Butterfield, 2005), the periodic expansion of acritarch

morphospace is best interpreted as a result of the evolutionary appearance of new clades.

In particular, fluctuation of acritarch morphospace in the Neoproterozoic and Cambrian

may represent the coming and going of different eukaryote groups.

Morphological Constraints, Convergence, and Nutrient Stress in the Mesoproterozoic

The ~1500 Ma (M1) saturation of acritarch morphospace was ensued by a

prolonged plateau until ~800 Ma (N1). Apparently, constraints on protist morphology

played a dominant role in a significant part of protist history from 1500 Ma to 800 Ma.

The increasingly populated morphospace during this period indicates that the

morphological history of acritarchs was characterized by convergent evolution. Given

that acritarchs are polyphyletic and thus include multiple clades, it is remarkable that the

morphological constraints were not overcome for such a long time.

Buick and others (Buick et al., 1995) described the Mesoproterozoic as “the

dullest time in Earth’s history (p.153)” and remarked that “never in the course of Earth’s

history did so little happen to so much for so long (p.169)”. These statements were based

upon δ13C values that hovered around 0‰ with little change for nearly 600 million years

58

(1600-1000 Ma) (Buick et al., 1995; Xiao et al., 1997; Brasier and Lindsay, 1998). The

global rate of organic carbon burial (as a proportion of total carbon burial), as inferred

from the Bangemall Group of northwestern Australia and equivalent carbonates

elsewhere, remained unchanged through the Mesoproterozoic, resulting in the static δ13C

pattern. This was ascribed to relatively little environmental and tectonic changes during

this most lackluster era (Buick et al., 1995). Tectonic and environmental tranquility

would lead to low bioproductivity through nutrient stress such as phosphorus limitation

(Brasier and Lindsay, 1998) and/or the dearth of metabolically important trace metals in

the Mesoproterozoic oceans (Anbar and Knoll, 2002).

Our results suggest that Buick and others were only partially correct in their

depiction of the Mesoproterozoic as being irksome and tedious. Our quantitative

measures of acritarch morphological disparity do suggest a long plateau lasting ~600

million years. However, the first appearance of nearly half the morphological characters

considered in this study (15 of 31) occurred during the early Mesoproterozoic, well

within the time of subdued δ13C fluctuations, and the plateau continued into the early

Neoproterozoic when the carbon cycle fluctuated moderately. Is this plateau indeed

related to Mesoproterozoic nutrient stress, as it has been shown in modern ecosystems

that diversity is often related, although may not be linearly, with energetic flow through

bottom-up ecological interactions (Vermeij, 2004)? The great temporal overlap between

acritarch disparity plateau and Mesoproterozoic geochemical stasis is suggestive of a

possible cause relationship, but the apparent mismatch in their initiation and termination

raises some concerns. At the present, the mismatch cannot be fully addressed because of

59

poor temporal resolution in both acritarch and δ13C data, as well as poor understanding of

the response time (lag time) between the different components of the Earth system.

Neoproterozoic Global Glaciations

The late Neoproterozoic saw perhaps the most dramatic of global climatic events

in the history of Earth. It has been hypothesized that multiple global glaciations occurred

during this time (~720-630 Ma), even to the extent of glaciers at the equator with tropical

sea ice 1 km thick (Kirschvink, 1992; Hoffman et al., 1998; Hoffman and Schrag, 2002).

It is reckoned that the “snowball Earth” glaciations would have lasted for approximately

10 million years (Hoffman et al., 1998; Bodiselitch et al., 2005). With the carbon cycle

cut short, due to completely iced-over oceans, the CO2 concentration in the atmosphere

(sourced by volcanic out-gassing) would have built up, eventually resulting in greenhouse

conditions and deglaciation. The deglaciation events would have also been likely very

dramatic, with wind and waves unlike those seen on Earth before or since (Allen and

Hoffman, 2005).

The controversial snowball Earth hypothesis has been criticized on biological

grounds (Runnegar, 2000). The fossil record clearly indicates that several major

photosynthetic clades, including green, red, and chromophyte algae (Butterfield et al.,

1994; Butterfield, 2000; Butterfield, 2004), evolved prior to the Cryogenian glaciations.

If the snowball model is correct then these three algal clades must have survived the

global glaciations, either in sea ice cracks, hydrothermal vents, fresh water melt ponds

(Hoffman et al., 1998; Hoffman and Schrag, 2002), or perhaps in an ice-free tropical

ocean that may have persisted during the snowball Earth events (Hyde et al., 2000;

Runnegar, 2000).

60

Acritarchs did experience significant change in the Cryogenian. Morphological

disparity (Fig. 4.3) as well as global taxonomic diversity (Fig. 4.1) decreased

significantly in the Cryogenian (N2). It is possible that the Cryogenian suffers from

fewer acritarch assemblages reported in the literature; however, Cryogenian acritarch

assemblages (Knoll et al., 1981; Vidal, 1981; Vidal and Nystuen, 1990; Yin, 1990) do

show lower taxonomic diversity and morphological disparity than older and younger

assemblages. Large acritarchs and complex acanthomorphic acritarchs are few in the

Cryogenian (Fig. 4.2, 4.4). This pattern suggests that, whether or not the tropical ocean

remained ice-free during the snowball Earth events, acanthomorphic acritarchs suffered

significant loss in the Cryogenian.

Runnegar hypothesized about the biological consequences of the various models

for Cryogenian glaciations (Runnegar, 2000). A strict snowball scenario would result in

an evolutionary bottleneck with the extinction of all but a few eukaryotic lineages. A

slushball scenario with ice-free tropical seas would result in a “blue-water refugium” with

the selective filtering of eukaryotic lineages favoring planktonic forms over benthic

forms. He also hypothesized a scenario in which global refrigeration would have had

mild impact on the biosphere. Paleoenvironmental analysis appears to suggest that

acanthomorphic acritarchs tend to occur in near-shore facies as compared to leiosphaerids

(Butterfield and Chandler, 1992). If this paleoecological pattern holds true for all

Proterozoic acritarchs, then the selective extinction of acanthomorphic acritarchs during

the Cryogenian may be taken as evidence in support of Runnegar’s blue-water refugium

hypothesis (Runnegar, 2000). It remains to be seen whether benthic algae survived

61

Cryogenian glaciations, and, if not, whether post-Cryogenian benthic ecosystem recruited

from planktonic algae that did survive the glaciations.

The Coming of Ediacara Organisms and New Ecological Interactions

The first macroscopic complex organisms in the fossil record are members of the

Ediacara biota and first appeared approximately 575 Ma, within 5 million years after the

580 Ma Gaskiers glaciation that lasted no more than one million years (Narbonne, 1998;

Bowring et al., 2003; Narbonne and Gehling, 2003; Narbonne, 2005). The phylogenetic

affinity of many of these organisms is controversial, but whether they represent the

ancestors of modern organisms (Runnegar and Fedonkin, 1992) or a failed evolutionary

experiment (Seilacher, 1992; Buss and Seilacher, 1994) they certainly indicate a

fundamental ecological restructuring of the world previously dominated by prokaryotes

and single-celled eukaryotes (Lipps and Valentine, 2004). The diverse body plans of

Ediacara organisms suggest equally diverse trophic strategies, probably including

heterotrophy. Evidence for the presence of heterotrophic consumers includes molluscan-

grade bilaterians (Fedonkin and Waggoner, 1997), cnidarian-grade metazoans (Runnegar

and Fedonkin, 1992), scratch marks interpreted as radular grazing traces (Seilacher, 1999;

Seilacher et al., 2003), epifaunal tiering (Clapham and Narbonne, 2002), and boring of

mineralized exoskeletons (Bengston and Zhao, 1992; Hua et al., 2003).

In light of the 580 Ma Gaskiers glaciation and probable consumers in the late

Ediacaran (575-542 Ma), it is instructional to explore their possible effects on the primary

producers (as represented by most acritarchs). Our data show that acritarch

morphological disparity and taxonomic diversity in the late Ediacaran decreased to levels

not seen since the Paleoproterozoic. During this time, acritarchs were dominated by

62

simple leiosphaerid forms, whereas all acritarchs that typified early Ediacaran (so called

Doushantuo-Pertatataka acritarchs) disappeared.

To test whether the Gaskiers glaciation, the diversification of Ediacara organisms,

or perhaps something else caused the disappearance of Doushantuo-Pertatataka

acritarchs, we need to sort out the exact temporal relationship between several

geobiological events. In South Australia, the appearance of Doushantuo-Pertatataka

acritarchs occurred long after the Marinoan glaciation and shortly after the Acraman

Impact, which has been estimated to be 580 Ma on the basis of chemostratigraphic

correlation (Grey et al., 2003). However, the late appearance of Doushantuo-Pertatataka

acritarchs in South Australia was probably due to regional, environmental, or

preservational biases. In South China, Doushantuo-Pertatataka acritarchs first appear in

chert nodules in association with an ash bed dated from 632 Ma (Condon et al., 2005),

range into the upper Doushantuo Formation (Zhang et al., 1998), and disappear below an

ash bed dated from 550 Ma (Condon et al., 2005). Condon et al. (2005) also considered a

putative sequence boundary associated with a mild negative δ13C excursion in the middle

Doushantuo Formation of the Yangtze Gorges area as related to the 580 Ma Gaskiers

glaciation. According to Condon et al.’s (2005) age estimation, Doushantuo-Pertatataka

acritarchs persisted 52–81 million years and disappeared somewhere between 580 Ma

and 551 Ma. If true, both the Acraman Impact and the Gaskiers glaciation predate,

perhaps significantly, the disappearance of Doushantuo-Pertatataka acritarchs, and

neither may have directly contributed to the disappearance of Doushantuo-Pertatataka

acritarchs.

63

Alternatively, a major negative δ13C excursion (-8‰) just below the 550 Ma ash

bed may be correlated to the Gaskiers glaciation. If this alternative correlation is true,

then the Gaskiers glaciation may postdate the disappearance of Doushantuo-Pertatataka

acritarchs, although the Acraman Impact would still predate the last occurrence of

Doushantuo-Pertatataka acritarchs as demonstrated in South Australia (Grey et al., 2003).

A third alternative is that herbivory by, or other ecological interactions with,

Ediacara organisms may have led to the decline of Doushantuo-Pertatataka acritarchs in

the late Ediacaran Period. Currently available radiometric constraints do not exclude

partial temporal overlap between the last Doushantuo-Pertatataka acritarchs and the first

Ediacara organisms, thus allowing ecological interactions between them. If this

hypothesis survives more rigorous tests in the future, the disappearance of Doushantuo-

Pertatataka acritarchs would be the first top-down driven mass extinction recorded in the

fossil record (Vermeij, 2004).

Recently, it has been hypothesized that the origin, not the extinction, of

Doushantuo-Pertatataka acritarchs was linked to the origin of eumetazoans through top-

down ecological interactions (Peterson and Butterfield, 2005). This hypothesis proposes

that the benthic, motile, macrophagous eumetazoans, which first evolved 634-604 Ma

according to molecular clock estimates, triggered an ecological response that led to the

evolution of benthic acanthomorphic acritarchs (i.e., Doushantuo-Pertatataka acritarchs).

In order to test these alternative hypotheses, we desperately need more precise age

constraints on several key Ediacaran events. We note that the estimates of when

Doushantuo-Pertatataka acritarchs went extinct, when eumetazoans evolved, and when

the Acraman Impact occurred are based on chemostratigraphic correlations or molecular

64

clock estimates, all associated with large uncertainties. Whether and how Ediacaran

acritarch history was affected by environmental and ecological events can be tested in

greater detail with tighter age constraints, but it is clear from both taxonomic compilation

and morphometric analysis that a short-lived burst of complex acritarchs occurred in the

early Ediacaran Period.

The Cambrian Explosion of Eukaryotes

Perhaps the most dramatic event in the history of life began approximately 540

Ma at the beginning of the Cambrian Period. Many metazoan phyla diverged in the

Early-Middle Cambrian (Conway Morris, 1998; Levinton, 2001; Zhuravlev and Riding,

2001; Valentine, 2004). The Cambrian explosion resulted in major ecological

restructuring of the biosphere (Zhuravlev and Riding, 2001) and alteration of

sedimentation patterns (Bottjer et al., 2000; Droser and Li, 2001).

It has been noted by several observers that acritarch diversity increased in step

with animal evolution during the Cambrian explosion (Knoll, 1994; Vidal and

Moczydlowska-Vidal, 1997; Butterfield, 2001). So did acritarch morphological disparity

(Figs. 4.1, 4.3). This implies a close link between these two ecological groups during the

radiation. The nature of these links, however, is less clear. It has been argued that

morphological diversification of phytoplankton, as shown in acritarch morphology, was

an ecological response to the evolution of filter-feeding mesozooplankton in the

Cambrian (Butterfield, 1997; Butterfield, 2001). Conversely, it is also possible that the

Cambrian metazoan diversification was driven by morphological and ecological radiation

of primary producers including most acritarchs (Moczydlowska, 2001; Moczydlowska,

2002). Further investigation of this matter, including detailed biostratigraphic studies

65

across the Proterozoic-Phanerozoic transition, will help determine which of these

scenarios most likely occurred.

Conclusions

We utilized the acritarch literature to produce an empirical morphospace that

describes the evolution of Proterozoic and Cambrian acritarchs. Acritarch body size

fluctuated non-directionally through the Proterozoic, but decreased significantly across

the Ediacaran-Cambrian boundary. Although the general pattern of disparity broadly

matches that of taxonomic diversity, the initial increase of morphological disparity

preceded the first taxonomic radiation by 500 million years. Morphological expansion

preceding taxonomic diversification, a pattern that is seen in many Phanerozoic multi-

celled organisms, may be a ubiquitous feature of eukaryote evolution. The

Mesoproterozoic disparity plateau may be linked to prolonged morphological constraints

and convergence related to long-term nutrient stress. The selective removal of

acanthomorphic acritarchs in the Cryogenian suggests significant impact of extensive

Cryogenian glaciations on the evolution of acritarchs, particularly those that lived in

near-shore environments. The appearance of Ediacara organisms may have altered the

Proterozoic trophic structure resulting in a major change in acritarch disparity and

diversity in the late Ediacaran Period. The late Ediacaran disappearance of Doushantuo-

Pertatataka acritarchs that thrived in the early Ediacaran Period may represent a rare case

of top-down driven extinction in the fossil record, testifying to the unique nature of the

Proterozoic biosphere. Acritarch disparity and diversity increased in step with animal

evolution during the Cambrian explosion, suggesting close ecological ties between these

two trophic groups.

66

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Chapter 5

Conclusions and Summary Statement

In this volume I have explored trends in eukaryote body size in various ecological

and evolutionary contexts. Despite the diverse temporal and spatial scales observed in

the three studies, there appear to be common controls of body size: external abiotic

environmental factors and biotic interactions.

In Chapter Two I investigated the relationships between parasites and their

bivalve hosts. Individuals of Protothaca staminea were extensively parasitized (86%) by

two types of trace-producing parasites. By and large there was no relationship between

parasitism and body size, even though some of these parasites (trematodes) have been

shown to alter growth rates. The only significant relationship between parasitism and

body size was that spionid mudblister infested clams from Argyle Creek were slightly,

yet significantly, smaller than their non-infested counterparts. Perhaps the void spaces

produced by the spionid parasites weakened the hosts’ shells and made them more

susceptible to durophagous predators. The most obvious pattern regarding body size was

that clams from Argyle Lagoon were significantly larger than clams from Argyle Creek.

This size discrepancy could be related to environmental stress, durophagous predators,

differing hydrodynamic conditions, or the comparison of differing cohorts. Even though

there was no discernible impact of trematode parasitism on bivalve body size, their traces

were abundant and easy to identify. Investigators of body size in the fossil record should

be aware of these organisms and their possible ramifications for body size studies.

In Chapter 3 I tested the hypothesis of limiting similarity, the idea that two closely

related species will alter their size/morphology in order to minimize competition, using

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Quaternary terrestrial gastropods from the Canary Islands. By integrating amino acid

geochronology for a high resolution geologic time series and stable isotope estimates to

support the claim that our two species were likely in competition with one another we

were able to more adequately test whether limiting similarity is an evolutionary process

or a transient ecological phenomenon. The first prediction of limiting similarity,

character displacement, was confirmed; Theba geminata and T. arinagae maintained

distinct morphologies throughout their spatial and temporal overlap. Their parallel trends

in body size were striking; maintaining sharp distinction even as both species became

smaller with time. However, the second prediction of limiting similarity, character

release, was not confirmed. The morphology of T. geminata did not converge on that of

T. arinagae following its extinction. The hypothesis of limiting similarity sensu stricto

was not confirmed in this case. It appears that changing climate at the end of the

Pleistocene may be responsible for the trend of decreasing body size, however there is

some evidence that interspecific competition did play a role in the evolution of Theba.

Theba geminata displayed non-directional fluctuation in body size at much higher rates

following the extinction of T. arinagae. Perhaps intraspecific competition played a

secondary role to climate change in the evolution of body size of Theba.

In Chapter 4 I examined the history of body size and morphological disparity of

the first 1.3 billion years of acritarch history. The results reject the idea that acritarch

body size increased monotonically through the Proterozoic; in fact they displayed non-

directional fluctuation. Acritarch body size decreased significantly following the first

appearance of Ediacara organisms and gradually rose during the Cambrian.

Morphological disparity increased a half billion years before the first taxonomic

75

radiation. This pattern is common among multicellular eukaryotes and is the first

demonstration of such a pattern in either protists or in the Precambrian. It appears that

morphospace saturation preceding taxonomic diversification is ubiquitous among

eukaryotes. Morphological disparity decreased significantly during the snowball earth

events and upon the first appearance of Ediacaran organisms suggesting multiple events

of selective extinction in the Proterozoic biosphere. Disparity then increased in step with

the diversification of acritarch and metazoans through the Cambrian suggesting

ecological links between the two groups.

There is a common theme to the results of these three case studies: ecology

influences body size and evolution at a wide range of scales of observation. Changing

environment seems to have a large influence on organisms at all spatial and temporal

scales whether it be differing substrates and hydrodynamic conditions for adjacent

populations of clams, the end of an ice age for sub-tropical land snails, or the complete

freezing of the earth for fossil phytoplankton. Interactions with other organisms seems to

be an important influence as well for parasites, clams, and their shell-breaking predators;

two congeneric snails trying to eek out a living on a desert island, and acritarchs facing

the onslaught of a new ecological dynamic never before seen on the earth. Despite the

claims of some, ecological processes do matter in evolution at multiple spatial and

temporal scales.

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Appendix 1. Size and infestation data for Protothaca staminea. 0=absent. 1=present.

Specimen No.

Length (mm) Parasite?

Trematode Pit/Blister?

Spionid Mudblister?

Spionid U-Shaped Boring? Environment

ALPS1 40.45 0 0 0 0 LagoonALPS2 50.80 1 1 0 0 LagoonALPS3 50.90 1 1 0 0 LagoonALPS4 42.55 0 0 0 0 LagoonALPS5 44.00 1 1 0 0 LagoonALPS6 51.80 1 1 1 0 LagoonALPS7 39.25 0 0 0 0 LagoonALPS8 42.40 0 0 0 0 LagoonALPS9 44.15 1 1 1 0 LagoonALPS10 50.10 1 1 0 0 LagoonALPS11 44.10 1 1 1 0 LagoonALPS12 52.10 1 1 0 0 LagoonALPS13 49.05 1 0 1 0 LagoonALPS14 41.90 1 1 0 0 LagoonALPS15 44.00 1 1 0 0 LagoonALPS16 45.25 0 0 0 0 LagoonALPS17 45.95 1 1 0 0 LagoonALPS18 47.10 0 0 0 0 LagoonALPS19 53.20 1 1 1 0 LagoonALPS20 45.35 1 1 0 0 LagoonALPS21 48.00 0 0 0 0 LagoonALPS22 43.50 0 0 0 0 LagoonALPS23 49.40 1 1 0 0 LagoonALPS24 50.80 0 0 0 0 LagoonALPS25 46.75 1 1 0 0 LagoonALPS26 42.30 1 1 1 0 LagoonALPS27 40.40 1 1 0 0 LagoonALPS28 45.60 1 1 0 0 LagoonALPS29 49.60 1 1 1 0 LagoonALPS30 45.25 1 1 0 0 LagoonALPS31 47.60 1 1 0 0 LagoonALPS32 48.40 1 1 1 0 LagoonALPS33 44.00 1 1 0 0 LagoonALPS34 48.60 1 1 0 0 LagoonALPS35 43.30 1 1 1 0 LagoonALPS36 55.30 1 1 0 0 LagoonALPS37 49.45 1 1 0 0 LagoonALPS38 45.75 1 1 0 0 LagoonALPS39 43.30 0 0 0 0 LagoonALPS40 48.05 1 1 0 0 LagoonALPS41 44.45 0 0 0 0 LagoonALPS42 46.50 0 0 0 0 LagoonALPS43 44.95 1 0 1 0 LagoonALPS44 48.85 1 1 0 0 LagoonALPS45 44.65 1 1 0 0 Lagoon

77

ALPS46 47.55 0 0 0 0 LagoonALPS47 40.55 1 1 0 0 LagoonALPS48 38.65 1 1 0 0 LagoonALPS49 47.70 1 1 1 0 LagoonALPS50 44.30 1 0 1 0 LagoonACPS1 38.30 1 1 1 0 CreekACPS2 37.70 1 1 0 0 CreekACPS3 37.55 1 1 1 0 CreekACPS4 36.65 1 1 1 0 CreekACPS5 34.30 1 1 1 1 CreekACPS6 41.85 1 1 1 1 CreekACPS7 34.50 1 0 1 1 CreekACPS8 32.30 1 0 1 0 CreekACPS9 35.90 1 1 1 0 CreekACPS10 39.50 1 1 1 0 CreekACPS11 42.30 1 1 0 1 CreekACPS12 46.10 1 0 1 1 CreekACPS13 36.60 1 1 0 1 CreekACPS14 36.40 1 0 1 0 CreekACPS15 40.70 0 0 0 0 CreekACPS16 40.20 1 1 0 0 CreekACPS17 35.00 1 1 1 1 CreekACPS18 38.60 1 1 0 0 CreekACPS19 44.70 1 0 1 1 CreekACPS20 42.95 1 0 1 0 CreekACPS21 36.50 1 0 0 1 CreekACPS22 37.85 1 0 1 1 CreekACPS23 43.20 1 0 0 1 CreekACPS24 31.45 1 1 1 1 CreekACPS25 29.55 1 1 1 1 CreekACPS26 49.25 1 1 1 1 CreekACPS27 47.70 1 1 0 0 CreekACPS28 43.20 1 0 1 1 CreekACPS29 35.95 1 1 1 0 CreekACPS30 33.80 1 1 1 1 CreekACPS31 39.25 0 0 0 0 CreekACPS32 39.15 1 0 1 0 CreekACPS33 29.25 1 1 1 0 CreekACPS34 35.00 1 0 1 1 CreekACPS35 31.15 1 1 1 0 CreekACPS36 39.60 1 1 1 0 CreekACPS37 34.40 1 0 0 1 CreekACPS38 36.00 1 0 1 0 CreekACPS39 36.40 1 0 1 1 CreekACPS40 33.80 1 0 1 1 CreekACPS41 33.75 1 0 1 1 CreekACPS42 34.20 1 1 1 1 CreekACPS43 34.30 1 0 0 1 CreekACPS44 33.50 1 1 1 1 CreekACPS45 34.90 1 1 1 1 Creek

78

ACPS46 35.30 1 0 1 1 CreekACPS47 49.30 1 1 0 0 CreekACPS48 32.95 1 0 1 1 CreekACPS49 40.00 1 1 1 1 CreekACPS50 36.35 1 1 1 0 CreekACPS51 39.75 1 1 1 1 Creek

79

Appendix 2. Size data for land snail species Theba arinagae and Theba geminata (mm). Character dimensions are described in text.

Species Age (ky) A B C D E F T. arinagae 14.9 8.62 10.06 8.13 5.63 4.3 4.71 T. arinagae 14.9 6.67 8.68 5.66 4.57 3.56 3.8 T. arinagae 14.9 6.99 9.13 6.23 4.74 3.76 3.84 T. arinagae 14.9 7.22 9.96 6.5 5.44 4.06 4.63 T. arinagae 14.9 7.72 10.38 6.68 5.43 4.38 5.06 T. arinagae 14.9 7.8 10.37 6.92 5.66 4.46 4.8 T. arinagae 14.9 7.02 9.16 6.09 4.68 3.36 3.94 T. arinagae 14.9 6.63 8.08 5.99 5.06 3.6 3.71 T. arinagae 14.9 6.71 9.03 5.9 4.61 3.99 4.02 T. arinagae 22.4 8.61 11.52 7.64 6.25 5.22 5.32 T. arinagae 22.4 9.57 12.27 8.59 7.04 5.88 6.15 T. arinagae 22.4 9.15 12.04 7.88 6.5 5.13 6.01 T. arinagae 22.4 9.32 12.01 8.26 6.84 5.67 5.97 T. arinagae 22.4 9.51 11.95 8.42 6.51 4.99 5.4 T. arinagae 22.4 8.59 10.74 7.5 5.91 4.19 4.73 T. arinagae 22.4 8.06 10.37 7.16 6.1 4.69 4.74 T. arinagae 22.4 9.08 11.25 8.15 6.69 5.13 5.3 T. arinagae 22.4 10.27 12.55 8.99 6.53 5.4 6.25 T. arinagae 22.4 8.38 11.2 7.43 6.19 4.39 5.09 T. arinagae 22.4 7.65 10.45 6.74 5.39 4.14 4.94 T. arinagae 22.4 8.22 10.85 6.96 5.95 4.32 5.27 T. arinagae 22.4 7.32 9.56 6.55 5.4 3.89 4.4 T. arinagae 22.4 7.03 9.35 6.4 5.33 3.89 4.28 T. arinagae 22.4 9.24 11.63 7.81 6.06 4.91 5.6 T. arinagae 22.4 8.97 11.58 8.16 6.7 5.38 5.53 T. arinagae 22.4 9.08 11.36 7.7 6.08 4.82 5.28 T. arinagae 22.4 8.02 11.13 7.06 5.83 4.46 4.85 T. arinagae 22.4 7.1 10.42 6.62 5.86 4.38 4.99 T. arinagae 22.4 7.63 10.49 6.8 5.72 4.18 4.27 T. arinagae 22.4 7.64 9.89 6.67 5.51 4.45 4.59 T. arinagae 22.4 8.28 10.47 6.95 5.9 3.78 4.51 T. arinagae 22.4 6.95 9.45 6.24 5.07 3.23 4.29 T. arinagae 22.4 7.67 10.33 6.55 5.48 3.99 4.42 T. arinagae 22.4 9.07 11.51 7.89 6.42 5.25 5.39 T. arinagae 22.4 7.93 11.15 7.26 6.12 4.37 4.97 T. arinagae 22.4 7.92 9.68 6.57 5.41 4.25 4.37 T. arinagae 22.4 7.22 9.89 6.77 5.59 4.11 4.74 T. arinagae 22.4 8.05 10.99 6.91 5.69 4.69 5.52 T. arinagae 22.4 7.24 9.01 6.37 5.22 3.7 3.83 T. arinagae 22.4 7.62 10.08 6.55 5.45 3.76 4.72 T. arinagae 22.4 8.21 10.32 7.19 5.82 4.5 4.53 T. arinagae 22.4 7.59 10.18 6.72 5.37 4.16 4.96 T. arinagae 22.4 7.98 10.9 6.94 5.3 3.77 4.53 T. arinagae 22.4 7.84 9.88 6.8 5.66 4.05 4.5 T. arinagae 22.4 7.93 10.81 7.17 5.93 4.18 4.86 T. arinagae 22.4 7.77 10.5 7.05 5.78 4.15 4.99

80

T. arinagae 22.4 7.35 9.4 6.4 4.92 4.26 4.6 T. arinagae 22.4 7.27 9.45 6.37 5 4 4.34 T. arinagae 22.4 8.65 11.27 7.49 6.07 4.64 5.19 T. arinagae 22.4 9.45 11.93 8.39 6.81 4.72 6.05 T. arinagae 22.4 8.4 11.44 7.59 6.13 4.87 5.62 T. arinagae 22.4 9.61 12.28 8.64 6.57 5.56 6.31 T. arinagae 22.4 7.71 10.01 6.12 4.72 3.57 4.29 T. arinagae 22.4 7.21 9.22 6.12 4.72 3.57 4.29 T. arinagae 22.4 9.04 11.15 7.95 5.91 4.62 5.58 T. arinagae 22.4 10 12.65 8.69 6.63 5.52 5.7 T. arinagae 22.4 9.99 12.99 8.43 6.68 5.29 6.28 T. arinagae 22.4 9.37 12.17 8.32 6.93 5.59 6.02 T. arinagae 22.4 8.01 11.17 7.3 6.25 5.01 5.68 T. arinagae 22.4 7.82 10.75 7.25 5.87 4.45 4.79 T. arinagae 22.4 7.6 10.61 6.78 5.72 4.36 4.8 T. arinagae 22.4 7.1 10.71 6.38 5.53 4.52 5.01 T. arinagae 22.4 7.5 9.87 6.78 5.74 4.73 5.32 T. arinagae 22.4 9.78 12.16 8.67 7.07 5.29 5.81 T. arinagae 29.4 9.4 12.22 7.95 6.48 5.33 5.25 T. arinagae 29.4 8.01 9.75 7.21 5.98 4.79 4.52 T. arinagae 29.4 8.55 11.79 7.62 6.39 5 4.99 T. arinagae 29.4 8.75 11.55 6.88 6.32 4.46 4.99 T. arinagae 29.4 8.73 11.91 7.78 5.88 5.07 5.71 T. arinagae 29.4 7.79 11.02 6.79 5.92 4.6 4.76 T. arinagae 29.4 8.15 11.75 7.55 6.14 4.79 5.28 T. arinagae 29.4 8.44 9.92 7.07 5.79 4.3 4.71 T. arinagae 29.4 9.14 12.69 8.26 7.39 5.93 5.77 T. arinagae 29.4 9.47 12.41 8.25 6.65 5.23 5.84 T. arinagae 29.4 9.41 12.66 8.02 6.48 5.27 6.22 T. arinagae 29.4 9.89 13.45 9.14 7.32 5.72 6.6 T. arinagae 29.4 11.49 14.19 9.98 8.14 6.77 7.48 T. arinagae 29.4 9.14 12.49 8.11 6.43 5.34 5.73 T. arinagae 29.4 9.04 12 7.79 6.69 5.11 6.05 T. arinagae 29.4 9.78 12.39 8.46 7.11 5.09 5.71 T. arinagae 29.4 9.3 13.19 8.78 7.14 5.81 6.71 T. arinagae 29.4 8.77 12.5 8.02 6.63 5.51 6.43 T. arinagae 29.4 7.91 10.6 6.97 5.82 4.23 5.1 T. arinagae 29.4 8 10.51 7.06 5.83 4.68 4.99 T. arinagae 29.4 8.95 11.11 7.71 6.12 4.78 4.95 T. arinagae 29.4 8.78 11.82 7.86 6.34 5.44 5.78 T. arinagae 29.4 9.01 11.72 8.04 6.52 5.86 5.55 T. arinagae 29.4 10.02 13.03 8.9 6.97 5.45 6.07 T. arinagae 29.4 10.27 13.51 9.05 7.44 5.66 6.13 T. arinagae 29.4 10.48 14 9.15 7.29 6.02 6.53 T. arinagae 29.4 9.06 11.41 8.01 6.36 5.09 5.6 T. arinagae 29.4 8.33 11.9 7.13 5.62 4.62 5.33 T. arinagae 29.4 9.08 11.61 7.65 6.81 4.55 5.27 T. arinagae 29.4 9.4 12.4 8.45 6.99 5.45 5.59 T. arinagae 29.4 9 11.59 7.73 6.44 5.05 5.57 T. arinagae 29.4 8.66 11.68 7.64 6.32 5.17 5.43

81

T. arinagae 29.4 8.83 12.1 7.72 6.58 5.6 5.7 T. arinagae 29.4 8.12 11.55 7.69 6.09 4.62 5.39 T. arinagae 29.4 9.02 11.62 7.65 6.02 4.71 5.55 T. arinagae 29.4 8.63 11.8 7.92 6.5 4.61 5.43 T. arinagae 29.4 8.6 11.54 7.52 5.91 4.91 5.27 T. arinagae 29.4 8.37 11.66 7.58 6.3 4.57 5.59 T. arinagae 29.4 8.81 10.6 7.79 6.9 5.21 5.03 T. arinagae 29.4 8.05 11.96 7.55 6.31 4.3 5.45 T. arinagae 29.4 8.63 11.32 7.66 6.11 4.9 5.08 T. arinagae 29.4 8.57 11.15 7.23 5.9 4.24 5.4 T. arinagae 29.4 8.79 11.8 7.65 6.28 5.1 5.81 T. arinagae 29.4 7.94 11.26 7.16 6.19 5 5.6 T. arinagae 29.4 8.26 10.51 7.11 5.8 4.6 4.93 T. arinagae 29.4 8.86 11.69 7.87 6.46 5.25 5.68 T. arinagae 29.4 10.07 12.51 8.58 6.85 5.6 6.58 T. arinagae 29.4 8.79 11.39 7.66 6.08 4.61 5.57 T. arinagae 29.4 7.81 10.72 6.85 5.82 4.71 5.63 T. arinagae 29.4 7.75 9.44 6.66 5.28 3.99 4.62 T. arinagae 29.4 7.5 9.65 6.49 5.3 4.2 4.53 T. arinagae 29.4 8.38 10.58 7.16 5.26 4.66 5.2 T. arinagae 29.4 8.2 11.26 7.41 5.95 4.74 5.21 T. arinagae 29.4 7.35 9.74 6.46 5.44 3.95 4.62 T. arinagae 29.4 7.37 9.9 6.51 5.49 4.09 4.78 T. arinagae 42.5 8.64 13.41 7.78 6.67 5.15 6.8 T. arinagae 42.5 7.41 12.52 7.29 6.44 5.58 6.49 T. arinagae 42.5 9.69 12.82 9.18 8.11 5.8 4.85 T. arinagae 42.5 8.46 12.85 7.73 6.46 4.89 6.1 T. arinagae 42.5 8.61 12.85 7.99 6.92 5.48 5.94 T. arinagae 42.5 8.37 12.26 7.44 6.56 4.61 5.71 T. arinagae 42.5 9.72 12.52 8.66 7.35 5.68 5.61 T. arinagae 42.5 8.4 12.25 7.56 6.66 5 6.09 T. arinagae 42.5 7.98 11.39 7.51 6.34 4.83 5.53 T. arinagae 42.5 9.07 11.94 7.73 6.5 5.17 6.9 T. arinagae 42.5 9.19 12.12 8.04 6.58 4.78 6.13 T. arinagae 42.5 9.98 12.51 7.99 6.78 5.35 5.88 T. arinagae 42.5 8.49 10.96 7.34 6 4.92 5.08 T. arinagae 42.5 8.22 11.02 7.2 5.94 4.43 4.81 T. arinagae 42.5 8.08 11.01 7.03 6.04 4.51 5.09 T. arinagae 42.5 8.55 10.63 7.33 5.47 4.91 5.01 T. arinagae 42.5 8.56 11.3 7.5 6.5 5.03 5.63 T. arinagae 42.5 8.33 11.03 7.15 5.78 3.89 5.13 T. arinagae 42.5 8.73 11.04 7.42 5.97 4.93 5.09 T. arinagae 42.5 7.95 11.55 7.38 6.3 5.19 5.3 T. arinagae 42.5 8.1 11.61 7.28 5.8 5.57 5.34 T. arinagae 42.5 7.67 10.51 6.99 5.16 4.28 4.82 T. arinagae 42.5 7.25 9.11 6.11 4.99 4.22 4.27 T. arinagae 42.5 8.04 10.23 7.01 5.82 4.46 4.76 T. arinagae 42.5 7.22 9.87 6.32 5.19 4.15 4.39 T. arinagae 42.5 7.39 10.08 6.61 5.28 4.92 4.77 T. arinagae 42.5 9.21 13.16 8.27 7.02 5.72 6.24

82

T. arinagae 42.5 8.22 10.93 7.37 6.06 4.57 5.38 T. arinagae 42.5 8.68 12.76 7.74 6.27 4.71 6.3 T. arinagae 42.5 9.38 11.43 8.05 6.21 4.46 5.01 T. arinagae 42.5 7.75 11.27 6.78 5.64 4.56 5.2 T. arinagae 42.5 9.57 12.24 8.53 6.67 5.01 5.34 T. arinagae 42.5 8.6 11.05 7.67 6.12 6.64 5.51 T. arinagae 42.5 7.67 10.88 6.95 5.87 3.91 4.89 T. arinagae 42.5 7.64 10.11 6.78 5.8 4.65 4.85 T. arinagae 42.5 7.55 11.22 7.02 5.76 4.31 5.44 T. arinagae 42.5 8.94 12.76 8.26 6.25 4.56 5.84 T. arinagae 42.5 7.94 11.02 7.28 5.88 4.71 5.14 T. arinagae 42.5 9.54 12.67 8.71 7.19 5.36 5.63 T. arinagae 42.5 9.15 12.33 8.16 6.14 4.73 5.68 T. arinagae 42.5 8.4 11.75 7.2 6.04 4.35 5.18 T. arinagae 42.5 8.16 11.54 7.51 6.2 4.54 5.3 T. arinagae 42.5 8.32 11.56 7.25 5.98 4.81 5.48 T. arinagae 42.5 8.2 10.97 7.33 5.91 5.64 4.96 T. arinagae 42.5 8.87 12.43 7.94 6.75 4.89 5.4 T. arinagae 42.5 8.57 11.67 7.7 6.5 4.07 3.59 T. arinagae 42.5 8.81 12.68 8.15 6.72 5.18 5.58 T. arinagae 42.5 9.28 12.66 8.44 6.66 5.12 5.81 T. arinagae 42.5 9.23 12.74 8.55 6.94 5.77 5.8 T. arinagae 42.5 8.58 11.62 7.83 6.17 4.67 5.01 T. arinagae 42.5 9.22 12.66 7.98 6.56 5.4 5.8 T. arinagae 42.5 9.47 11.95 7.69 5.81 4.57 5.02 T. arinagae 42.5 9.29 13.16 8.17 6.47 5.34 5.58 T. arinagae 42.5 8.27 11.75 7.27 5.56 4.49 5.39 T. arinagae 42.5 8.01 11.59 7.07 5.75 4.77 5.67 T. arinagae 42.5 8.01 11.45 6.97 5.61 4.51 5.02 T. arinagae 42.5 8.39 12.07 7.49 6.06 4.97 5.2 T. arinagae 42.5 8.26 12.04 7.69 6.16 5 5.46 T. arinagae 42.5 7.75 10.79 6.91 5.74 4.4 5.27 T. arinagae 42.5 8.09 11.9 7.11 5.67 4.97 5.55 T. arinagae 42.5 8.24 11.88 7.24 5.52 4.99 5.51 T. arinagae 42.5 7.23 11.02 6.57 5.07 4.29 4.93 T. arinagae 42.5 8.26 11.79 6.89 5.35 4.16 5.12 T. arinagae 42.5 8.19 11.78 7.39 6.11 5.03 6.03 T. arinagae 42.5 7.63 11.12 6.82 5.45 4.45 5.05 T. arinagae 42.5 8.02 11.39 7.49 6.12 5 5.02 T. arinagae 42.5 8.64 12.45 7.53 6.19 4.6 5.7 T. arinagae 42.5 8.19 11.81 7.6 5.55 4.21 5.28 T. arinagae 42.5 7.85 12.36 6.98 5.77 4.94 5.28 T. arinagae 42.5 7.71 11.11 6.95 5.61 4.81 5.32 T. arinagae 42.5 8.34 11.87 7.37 6.1 4.28 5.26 T. arinagae 42.5 8.49 11.4 7.58 5.81 4.8 6.13 T. arinagae 42.5 8.27 11.94 7.23 5.91 4.02 5.43 T. arinagae 42.5 8.4 11.4 7.41 5.86 4.72 5.21 T. arinagae 42.5 9.71 12.83 8.68 7.23 6.01 5.58 T. arinagae 42.5 9.35 12.98 8.32 6.66 5.12 6.06 T. arinagae 42.5 9.3 13.81 8.45 6.73 5.18 6.5

83

T. arinagae 42.5 7.83 11.6 7.01 5.63 4.66 5.45 T. arinagae 42.5 9.3 12.54 8.3 6.49 5.2 6.07 T. arinagae 42.5 8.17 10.6 6.89 5.43 4.9 4.86 T. arinagae 42.5 8.75 12 7.66 6.04 4.98 5.64 T. arinagae 42.5 8.35 11.87 7.81 5.98 4.94 5.61 T. arinagae 42.5 9.17 17.91 8.15 6.89 6 6.07 T. arinagae 42.5 7.94 11.54 7.01 5.6 4.65 5.2 T. arinagae 42.5 8.66 12.3 7.36 6.16 5.19 5.79 T. arinagae 42.5 9.24 12.82 8.05 6.39 4.97 5.57 T. arinagae 42.5 7.76 10.72 6.7 5.8 4.54 5 T. arinagae 42.5 8.72 12.02 7.69 5.74 5.1 5.39 T. arinagae 42.5 8.14 10.68 7.17 5.83 5.26 5.5 T. arinagae 42.5 8.26 11.46 7.25 5.86 4.41 5.31 T. arinagae 42.5 8.62 11.83 7.44 6.28 4.79 5.3 T. arinagae 42.5 8.41 11.8 7.18 5.86 4.74 5.58 T. arinagae 42.5 7.78 10.14 6.7 5.37 4.29 4.81 T. arinagae 42.5 8.83 11.83 7.95 5.94 4.92 5.82 T. arinagae 42.5 8.01 11.39 6.76 5.88 4.77 5.27 T. arinagae 42.5 8.34 11.22 7.4 5.79 4.7 4.98 T. arinagae 42.5 9 12.37 7.97 5.95 4.79 5.55 T. arinagae 42.5 9.73 12.47 8.35 6.47 5.13 5.29 T. arinagae 42.5 7.85 11.09 6.95 5.7 4.99 5.54 T. arinagae 42.5 8.09 10.85 7.24 5.88 4.68 5.11 T. arinagae 42.5 8.06 10.67 6.82 5.74 4.67 4.81 T. arinagae 42.5 9.32 12.66 8.44 6.46 5.79 7.14 T. arinagae 42.5 8.82 12.18 7.93 6.08 4.73 5.87 T. arinagae 42.5 9.06 11.65 8.05 6.84 5.52 6 T. arinagae 42.5 8.38 10.79 7.4 6.26 5.3 5.6 T. arinagae 42.5 8.91 10.98 7.67 6.37 4.21 5.33 T. arinagae 42.5 9 12.29 7.77 6.31 5.43 6.95 T. arinagae 42.5 8.75 11.35 7.72 6.14 5.18 5.35 T. arinagae 42.5 9.43 11.54 7.7 6.36 5.03 5.89 T. arinagae 42.5 8.68 11.44 7.67 6.58 4.85 5.99 T. geminata 0 14.66 18.38 12.75 10.47 9.27 9.14 T. geminata 0 12.97 15.56 11.53 9.23 8.68 8.47 T. geminata 0 12.53 17.31 11.13 8.53 7.9 9.22 T. geminata 0 10.9 15.4 9.66 7.89 6.98 7.97 T. geminata 0 11.03 15.44 9.68 7.9 6.65 7.94 T. geminata 0 11.93 16.37 10.12 7.77 6.96 8.72 T. geminata 0 12.05 16.45 10.96 8.17 7.23 8.28 T. geminata 0 11.01 16.46 9.86 7.97 6.81 8.28 T. geminata 0 10.5 14.68 9.18 7.54 6.56 7.61 T. geminata 0 12.14 15.2 10.21 7.68 6.96 7.68 T. geminata 0 12.09 15.18 10.34 7.61 6.67 7.79 T. geminata 0 11.44 15.32 10.21 7.65 6.94 7.86 T. geminata 0 11.06 15.48 10.05 8.36 7.91 7.73 T. geminata 0 11.8 14.52 10.42 8.43 7.8 7.12 T. geminata 0 12.55 15.95 10.76 8.37 7.14 7.99 T. geminata 0 11.56 15.65 10.13 7.82 6.89 7.96 T. geminata 0 13.06 16.8 11.61 8.16 7.03 8.12

84

T. geminata 0 11.94 16.09 10.62 8.58 7.45 8.47 T. geminata 0 14.23 18.96 12.76 10.23 8.63 8.86 T. geminata 0 11.93 16.51 10.95 8.09 7.37 8.42 T. geminata 0 10.68 15.08 9.88 7.8 7.44 7.74 T. geminata 0 11.25 15.53 9.71 7.87 6.75 5.56 T. geminata 0 11.34 15.32 9.93 7.95 7.14 7.75 T. geminata 0 11.51 15.01 10.06 8.11 7.22 7.64 T. geminata 0 10.92 15.06 9.81 8.21 7.05 7.97 T. geminata 0 12.08 14.44 10.11 7.65 6.38 7.42 T. geminata 0 11.16 15.15 9.81 7.85 6.93 7.61 T. geminata 0 10.13 14.82 9.08 7.5 6.29 7.65 T. geminata 0 10.31 14.69 9.42 7.85 6.64 7.7 T. geminata 0 10.39 14.16 9.23 7.83 6.64 7.33 T. geminata 0 10.36 14.25 9.35 7.44 6.52 7.41 T. geminata 0 11.87 14.76 10.31 8.1 6.76 7.64 T. geminata 0 10.26 14.03 9.28 7.48 6.06 7.79 T. geminata 0 11.02 13.88 9.55 7.85 6.92 7.08 T. geminata 0 10.47 14.53 9.33 7.37 6.67 7.85 T. geminata 0 10.34 14.07 9.23 7.37 6.55 7.16 T. geminata 0 11.57 14.68 10.03 7.73 7.01 7.77 T. geminata 0 10.88 14.34 9.79 8.15 7.13 7.6 T. geminata 0 11.2 15.27 9.96 7.6 6.29 7.79 T. geminata 0 11.37 15.46 10.27 7.9 6.61 8.16 T. geminata 0 14.78 17.92 13.14 10.18 8.49 9.42 T. geminata 0 10.17 14.67 9.03 7.27 6.17 7.38 T. geminata 0 10.1 14.87 9.1 7.52 6.19 7.49 T. geminata 0 10.75 14.71 9.03 7.25 5.86 7.64 T. geminata 0 10.21 14.05 9.14 7.21 6.38 6.82 T. geminata 0 13.36 17.09 11.54 8.86 7.84 8.67 T. geminata 0 12.74 16.74 11.27 8.75 7.69 8.26 T. geminata 0 14.87 18.1 13.79 10.79 9.5 9.11 T. geminata 0 13.88 18.07 12.45 9.56 7.83 9.1 T. geminata 0 13.15 17.26 11.93 8.86 7.2 8.67 T. geminata 0 13.83 15.85 11.37 8.79 7.51 8.18 T. geminata 0 13.5 17.02 11.89 9.19 7.2 8.48 T. geminata 0 12.34 15.63 10.91 8.73 6.68 7.65 T. geminata 0 13.16 16.61 11.95 9.06 7.37 8.38 T. geminata 0 13.09 17.53 11.84 9.25 7.79 9 T. geminata 0 13.26 16.27 11.38 8.43 6.65 8.02 T. geminata 0 13.62 17.09 12.09 8.96 7.53 8.69 T. geminata 0 12.5 16.19 10.65 8.77 7.65 8.06 T. geminata 0 13.91 17.76 12.72 9.6 8.25 8.93 T. geminata 0 13.44 16.93 12.06 9.24 7.75 8.59 T. geminata 0 11.72 15.43 10.4 8.3 7.12 7.44 T. geminata 0 12.37 16.79 11.26 9.35 7.86 9.1 T. geminata 0 13.59 17.07 11.67 9.09 8.15 9.06 T. geminata 0 12.12 15 10.6 8.38 6.91 7.81 T. geminata 0 12.88 17.38 11.16 9.12 7.4 8.47 T. geminata 0 13.7 17.03 12.24 8.98 6.64 8.31 T. geminata 0 15.4 17.55 13.54 9.73 8.54 8.93

85

T. geminata 0 11.9 16.08 10.49 8.57 6.75 8.25 T. geminata 0 13.32 16.1 11.32 8.64 6.92 8.1 T. geminata 0 11.61 16.2 10.56 8.48 7.01 8.16 T. geminata 0 12.09 17.09 11.22 9.15 7.9 8.69 T. geminata 0 12.55 15.81 11.15 8.05 6.6 7.64 T. geminata 5.4 11.06 14.43 9.81 8.11 6.3 7.43 T. geminata 5.4 9.95 13.17 8.57 6.96 5.63 6.8 T. geminata 5.4 10.23 12.62 9.03 7.54 6.33 6.28 T. geminata 5.4 11.68 15.07 10.13 7.84 6.34 7.64 T. geminata 5.4 11.29 14.73 9.99 7.38 5.99 7.71 T. geminata 5.4 10.38 13.7 8.99 7.51 5.85 6.49 T. geminata 5.4 10.16 13.27 8.72 6.96 5.98 6.51 T. geminata 5.4 10.5 13.76 9.29 7.52 6.59 7.31 T. geminata 5.4 11.62 14.66 10.3 8.21 6.42 7.36 T. geminata 5.4 10.39 13.32 9.17 7.64 6.06 6.34 T. geminata 5.4 10.95 14.58 9.56 7.36 5.93 7.35 T. geminata 11 12.47 15.7 10.78 8.69 7.67 7.94 T. geminata 11 12.63 14.58 10.44 8.45 6.99 8.1 T. geminata 11 13.07 16.61 11.54 9.02 7.63 8.21 T. geminata 11 11.38 16.57 10.47 8.75 7.42 8.64 T. geminata 11 12.62 16.18 11.04 8.77 7.3 8.4 T. geminata 11 13.29 15.63 11.87 10.22 8.32 8.17 T. geminata 11 12.51 16.71 10.89 8.92 7.47 8.13 T. geminata 11 11.48 15.46 10.27 8.48 7.65 7.71 T. geminata 11 11.87 14.36 10.25 8.11 6.18 7.33 T. geminata 11 11.94 15.12 10.24 8.39 6.27 7.29 T. geminata 11 11.59 14.67 10.43 8.83 6.62 6.87 T. geminata 11 12.47 15.79 11.36 9.05 7.06 8.21 T. geminata 11 13.94 16.82 11.71 9.06 7.52 8.48 T. geminata 11 14.03 17.68 12.54 9.49 7.83 8.14 T. geminata 11 11.84 15.08 10.42 8.45 6.61 7.46 T. geminata 11 13.48 16.46 11.72 8.81 6.54 8.43 T. geminata 11 14.33 16.93 12.12 9.77 8.37 8.63 T. geminata 11 12.47 14.86 10.95 9.51 7.68 7.77 T. geminata 14.9 10.27 13.02 8.73 7.49 5.53 6.47 T. geminata 14.9 9.34 13.43 8.38 6.96 5.42 6.53 T. geminata 14.9 9.99 13.08 8.97 7.81 6.09 6.27 T. geminata 14.9 9.05 12.36 7.92 7.11 5.26 6.12 T. geminata 14.9 9.44 13.59 8.81 7.7 5.84 6.71 T. geminata 22.4 12.31 15.19 10.79 8.8 6.87 6.7 T. geminata 22.4 11.24 14.13 10.06 8.25 6.15 6.77 T. geminata 22.4 12.08 16.17 10.99 8.85 6.83 7.62 T. geminata 22.4 10.88 15.07 10.01 8.53 6.52 5.76 T. geminata 22.4 10.36 13.75 9.29 7.99 5.53 6.38 T. geminata 22.4 11.69 15.42 10.53 8.29 6.83 7.5 T. geminata 22.4 10.98 14.55 9.83 8.25 7.4 7.61 T. geminata 22.4 11.23 14.26 10 7.95 6.18 6.64 T. geminata 22.4 11.72 14.66 10.33 7.96 6.73 7.89 T. geminata 22.4 10.12 13.5 9.04 7.32 6.25 6.86 T. geminata 22.4 11.02 13.99 9.54 7.62 5.8 6.33

86

T. geminata 22.4 11.78 15.21 10.76 8.77 7.04 8.28 T. geminata 22.4 11.91 14.85 10.92 9.34 8.11 7.62 T. geminata 22.4 11.42 14.52 9.89 8.13 6.14 7.4 T. geminata 22.4 11.64 14.63 10.29 8.09 5.94 7.35 T. geminata 22.4 12.71 17.55 11.84 9.92 7.64 9.47 T. geminata 22.4 11.02 15.05 10.15 8.26 6.82 7.9 T. geminata 22.4 10.94 14.82 9.82 7.87 7 7.65 T. geminata 22.4 10.32 13.83 9.23 7.96 6 6.73 T. geminata 22.4 11.96 15.69 10.57 8.32 6.31 7.84 T. geminata 22.4 9.91 15.25 9.46 7.42 6.28 7.56 T. geminata 22.4 10.57 14.83 9.71 8.09 6.22 7.75 T. geminata 22.4 11.05 14.96 9.91 7.92 6.3 7.95 T. geminata 22.4 9.81 14.39 9.01 7.55 5.84 7.2 T. geminata 22.4 11.02 14.4 9.54 7.8 6.53 7.56 T. geminata 22.4 10.45 14.12 9.45 7.49 5.67 6.65 T. geminata 22.4 10.78 14.69 9.96 8.13 6.58 7.6 T. geminata 22.4 10.81 14.03 9.47 7.69 6.35 7.44 T. geminata 22.4 11.05 14.64 9.94 7.79 5.98 7.51 T. geminata 22.4 12.05 14.97 10.4 8.51 6.55 6.94 T. geminata 22.4 11.55 15.58 10.64 8.79 6.99 7.88 T. geminata 22.4 10.33 13.9 9.3 7.49 6.91 7.95 T. geminata 22.4 11.49 16.27 11.26 8.92 7.13 7.87 T. geminata 22.4 11.94 15.67 10.73 8.56 6.95 7.57 T. geminata 22.4 10.75 15.08 9.68 7.68 5.51 7.39 T. geminata 22.4 9.95 13.91 8.6 7.2 5.41 7.06 T. geminata 22.4 10.19 13.97 9.6 7.44 6.54 7.22 T. geminata 22.4 10.57 13.94 9.58 8.11 5.5 6.46 T. geminata 22.4 10.87 15.01 9.93 8.06 6.69 7.53 T. geminata 22.4 10.65 15.18 9.84 8.06 7.13 7.85 T. geminata 22.4 9.99 13.3 9.23 7.86 5.3 6.63 T. geminata 22.4 10.21 13.57 9.03 7.42 6.21 6.88 T. geminata 22.4 11.43 16.33 10.63 8.42 7.07 8.01 T. geminata 22.4 11.16 15.22 10.16 8.5 6.86 7.41 T. geminata 22.4 11.28 15.44 10.37 8.03 6.8 7.66 T. geminata 22.4 11.72 15.64 10.42 8.47 6.6 7.72 T. geminata 22.4 9.99 13.6 9.22 7.52 5.96 6.84 T. geminata 22.4 9.88 13.34 8.73 7.17 6.03 6.81 T. geminata 22.4 11.22 14.36 10.24 8.3 7.11 7.48 T. geminata 22.4 11.41 15.11 10.45 7.66 6.54 7.68 T. geminata 22.4 11.38 15.24 10.26 7.93 6.99 7.81 T. geminata 22.4 10.62 14.28 10 7.85 5.77 6.66 T. geminata 22.4 10.78 14.13 9.77 7.36 6.29 6.78 T. geminata 22.4 11.14 14.87 9.81 7.82 6.53 7.28 T. geminata 22.4 10.48 13.56 9.3 7.53 5.7 6.29 T. geminata 22.4 10.39 14.34 9.47 7.61 6.25 7.22 T. geminata 22.4 11.36 14.49 10.01 8.09 7.07 7.63 T. geminata 22.4 10.75 14.35 9.57 7.46 6.08 6.93 T. geminata 22.4 12.29 16.65 11.24 9.1 6.53 7.62 T. geminata 22.4 10.26 14.22 9.3 7.27 5.7 7.07 T. geminata 22.4 13.75 17.19 12.24 9.28 7.48 8.72

87

T. geminata 29.4 13.39 17.21 11.52 9.23 7.72 8.4 T. geminata 29.4 14.7 19.54 13.32 10.19 7.94 9.27 T. geminata 29.4 13.37 17.95 11.82 9.49 7.5 9.8 T. geminata 29.4 14.97 18.92 13.47 9.88 6.99 8.55 T. geminata 29.4 14.75 18.77 13.6 10.9 8.28 8.69 T. geminata 29.4 15.17 17.93 13.47 10.55 8.31 8.76 T. geminata 29.4 12.78 17.09 11.65 9.56 8.27 8.6 T. geminata 29.4 13.35 17.27 12.2 9.42 7.07 8.12 T. geminata 29.4 13.34 18.17 12.12 10.72 7.56 8.29 T. geminata 29.4 12.92 15.9 11.53 8.89 6.8 7.86 T. geminata 29.4 13.23 16.25 11.87 9.65 8.09 8.15 T. geminata 29.4 12.98 16.29 11.71 9.08 7.63 8.01 T. geminata 29.4 14.1 17.22 12 9.34 6.8 7.85 T. geminata 29.4 12.83 15.82 11.5 9.37 7.49 7.53 T. geminata 29.4 12.64 17.49 11.55 9.46 7.62 8.44 T. geminata 29.4 12.16 15.68 10.57 8.49 6.34 7.33 T. geminata 29.4 12.97 16.8 12.04 9.94 7.18 8.71 T. geminata 29.4 13.28 16.75 11.68 9.41 7.42 8.17 T. geminata 29.4 13.07 16.5 11.53 8.99 7.36 8.58 T. geminata 29.4 15.61 17.3 13.77 9.92 8 8.5 T. geminata 29.4 13.22 17.23 12.23 8.83 7.06 8.38 T. geminata 29.4 12.92 16.18 11.36 8.71 6.7 8.34 T. geminata 29.4 13.64 17.46 12.01 8.99 7.48 9.02 T. geminata 29.4 14.72 17.15 12.28 9.47 6.95 8.35 T. geminata 29.4 13.71 15.92 11.77 8.57 6.36 8.65 T. geminata 29.4 12.22 15.38 11.29 8.75 6.71 7.6 T. geminata 29.4 13.91 16.85 12.34 9.34 7.53 8.51 T. geminata 29.4 12.38 16.23 11.26 8.76 7.33 7.81 T. geminata 29.4 13.98 17.08 12.31 10.21 7.53 8.93 T. geminata 29.4 14.3 18.83 13.04 10.32 7.19 9.43 T. geminata 29.4 11.9 16.31 10.57 8.41 6.2 7.58 T. geminata 29.4 13.22 15.44 11.72 9.13 7.2 7.57 T. geminata 29.4 11.79 15.54 10.84 8.81 6.98 7.46 T. geminata 29.4 13.65 16.76 11.89 8.74 6.55 8.22 T. geminata 29.4 12.88 16.73 11.17 8.86 6.89 8.1 T. geminata 29.4 13.36 16.91 11.95 9.38 7.04 8.49 T. geminata 29.4 12.8 16.62 11.46 9.04 7.02 8.67 T. geminata 29.4 12.94 17.4 11.59 8.72 7.86 8.69 T. geminata 29.4 12.55 16.31 11.44 9.17 7.61 8.1 T. geminata 29.4 12.16 15.35 10.92 8.79 7.32 7.54 T. geminata 29.4 13.06 15.84 11.27 8.49 6.64 7.68 T. geminata 29.4 12.28 16.04 10.76 8.66 6.64 8.08 T. geminata 29.4 12.91 15.61 11.19 8.55 7.57 8.02 T. geminata 29.4 13.07 15.83 11.4 8.64 7.61 7.91 T. geminata 29.4 12.26 16.67 10.77 8.57 6.96 8.16 T. geminata 29.4 13.88 16.86 12.48 16.19 8.19 8.66 T. geminata 29.4 12.28 16.37 11.14 8.67 7.1 7.9 T. geminata 29.4 11.51 14.22 10.02 7.63 6.1 7.03 T. geminata 29.4 12.2 15.99 11.07 8.51 6.91 7.93 T. geminata 29.4 13.4 17.01 12.06 10.33 7.58 8.12

88

T. geminata 29.4 13.08 16.58 11.43 9.1 6.76 8.38 T. geminata 29.4 12.81 16.35 11.44 9.4 7.88 8.92 T. geminata 29.4 12.53 16.01 11 9.07 6.74 7.52 T. geminata 29.4 13.31 16.72 11.67 8.92 7.2 8.22 T. geminata 29.4 14.65 16.82 13.02 9.04 7.6 8.3 T. geminata 29.4 13.07 16.21 11.42 8.28 6.57 7.08 T. geminata 29.4 12.49 15.34 11.16 8.72 7.08 7.82 T. geminata 29.4 12.47 16.34 11.08 8.32 6.76 8.32 T. geminata 29.4 12.78 15.93 10.84 8.7 7.14 8.02 T. geminata 29.4 11.82 14.69 10.09 8.52 6.31 6.84 T. geminata 29.4 12.52 16.15 11.24 9.14 7.25 7.97 T. geminata 29.4 13.96 16.99 12.52 9.75 8.12 8.48 T. geminata 29.4 13.18 18.02 11.9 9.32 7.67 8.83 T. geminata 29.4 11.79 14.82 10.17 8.1 6.43 7.19 T. geminata 29.4 11.35 15.17 10.07 8.07 6.7 8.32 T. geminata 29.4 11.9 14.37 9.66 7.95 5.63 6.99 T. geminata 29.4 10.05 14.83 9.13 7.63 6.03 6.45 T. geminata 29.4 10.43 13.78 8.91 7.32 5.5 5.66 T. geminata 29.4 10.55 14.04 9.52 8.29 6.23 7.51 T. geminata 29.4 10.18 13.34 9.2 7.61 6.16 6.51 T. geminata 29.4 8.3 12.06 7.51 6.08 5.79 5.02 T. geminata 29.4 10.57 13.54 9.26 7.64 5.35 6.07 T. geminata 29.4 10.64 14.85 9.92 7.8 5.7 7.2 T. geminata 29.4 12.41 15.64 10.87 8.16 6.85 7.3 T. geminata 29.4 12.25 14.29 10.51 7.95 6.6 7.35 T. geminata 29.4 10.79 15.14 9.79 7.71 6.75 7.8 T. geminata 29.4 10.75 14.74 9.48 8.5 6.61 6.73 T. geminata 29.4 8.49 12.59 8.34 6.96 5.44 5.65 T. geminata 29.4 11.31 14.57 9.67 7.72 6.6 7.54 T. geminata 29.4 10.09 15.62 9.66 7.62 6.99 7.12 T. geminata 29.4 9.75 13.48 8.73 7.42 6.01 6.27 T. geminata 29.4 11.39 15.15 10 7.57 6.43 7.63 T. geminata 29.4 10.74 13.56 9.48 8.06 6.88 7.11 T. geminata 29.4 11.06 14.52 10.12 8.38 6.99 7.18 T. geminata 29.4 10.7 13.91 9.38 7.59 6.39 7.22 T. geminata 29.4 10.91 14.64 9.7 7.79 6 7.34 T. geminata 29.4 10.45 14.71 9.54 7.71 5.8 7.03 T. geminata 29.4 10.01 13.08 8.93 7.24 6.1 6.46 T. geminata 29.4 12.09 16.06 10.72 8.63 6.57 7.62 T. geminata 29.4 11.18 14.98 10.05 8.15 6.35 6.95 T. geminata 29.4 10.11 12.82 8.82 6.91 5.55 6.2 T. geminata 42.5 12.32 16.4 11.15 9.01 7.62 8.03 T. geminata 42.5 9.28 12.94 8.56 7.02 5.24 6.07 T. geminata 42.5 10.79 14.09 9.67 7.63 6.21 6.33 T. geminata 42.5 11.02 14.24 10.09 8.45 6.67 6.79 T. geminata 42.5 12.6 15.85 10.82 8.41 6.74 7.54 T. geminata 42.5 12.29 15.55 10.6 8.89 7.52 7.66 T. geminata 42.5 10.58 14.13 9.64 7.99 6.68 6.94 T. geminata 42.5 10.76 15.19 9.79 8.2 6.74 7.52 T. geminata 42.5 13.28 16.86 11.45 8.71 7.28 7.7

89

T. geminata 42.5 13.17 17.71 11.71 9.38 7.44 7.98 T. geminata 42.5 9.24 13.23 8.69 7.67 6.79 7.01 T. geminata 42.5 11.64 15.72 10.33 8.96 6.84 7.41 T. geminata 42.5 13.29 16.9 12.51 10.4 7.65 8.05 T. geminata 42.5 13.44 18.32 12.11 10.76 7.38 8.94 T. geminata 42.5 12.83 16.23 11.15 9.57 6.89 6.8 T. geminata 42.5 12.96 16.26 11.38 9.7 6.44 7.18 T. geminata 42.5 13.34 17.65 11.62 10.14 7.79 7.41 T. geminata 42.5 12.68 16.04 11.67 9.15 7.44 8.48 T. geminata 42.5 12.6 17.21 11.6 9.45 7.34 8.28 T. geminata 42.5 13.31 17.2 12.34 10.02 7.42 7.62 T. geminata 42.5 13.88 17.77 11.99 9.55 6.78 7.92 T. geminata 42.5 12.04 16.14 11.52 9.3 7.48 8.35 T. geminata 42.5 10.78 15.15 9.7 8.79 6.86 7.38 T. geminata 42.5 11.43 15.34 10.23 8.57 6.74 7.48 T. geminata 42.5 10.95 14.9 9.92 8.29 6.61 7.58 T. geminata 42.5 12.93 16.36 11.47 9.13 6.64 7.93 T. geminata 42.5 11.08 16.41 10.3 8.65 7.58 8.73 T. geminata 42.5 11.94 15.23 10.27 8.23 6.3 7.66 T. geminata 42.5 11.28 15.71 9.95 8.49 7.18 7.53 T. geminata 42.5 12.62 17.4 11.64 9.43 8.09 8.92 T. geminata 42.5 12.44 16.12 11.28 9.04 7.41 8.01 T. geminata 42.5 11.91 15.87 10.61 8.49 7.1 7.7 T. geminata 42.5 12.7 17.31 11.78 9.45 6.81 8.04 T. geminata 42.5 11.75 15.96 10.54 8.9 7.48 7.58 T. geminata 42.5 13.06 16.67 11.73 8.82 6.94 8.08 T. geminata 42.5 13.73 17.28 12.17 9.38 8.18 8.35 T. geminata 42.5 11.11 14.33 10.14 8.82 6.51 7.07 T. geminata 42.5 12.61 15.66 11.44 9.96 7.3 7.87 T. geminata 42.5 13.43 16.93 11.96 9.7 8.14 8 T. geminata 42.5 12.62 16.62 11.13 8.55 7.2 8.22 T. geminata 42.5 12 16.07 10.65 9.01 7.09 7.77 T. geminata 42.5 13.12 16.69 11.43 9.36 7.38 8.14 T. geminata 42.5 12.88 17.06 11.84 8.88 7.3 7.91 T. geminata 42.5 12.19 16.5 11.09 9.23 7.28 7.92 T. geminata 42.5 11.46 15 10.31 8.52 6.83 7.15 T. geminata 42.5 11.45 16.63 10.41 9.23 7.32 8.75 T. geminata 42.5 10.83 15.13 10.21 8.88 6.2 7 T. geminata 42.5 12.02 15.91 10.78 8.57 7.1 7.86 T. geminata 42.5 11.18 15.02 10.31 8.18 6.63 7.38 T. geminata 42.5 12.52 16.11 11.07 8.48 7.03 7.98 T. geminata 42.5 11.45 14.93 10.36 8.72 6.48 7 T. geminata 42.5 11.84 15.19 10.26 8.63 6.28 6.77 T. geminata 42.5 11.9 16.54 11.02 8.75 6.72 7.84 T. geminata 42.5 13.22 17.03 12.07 10.09 7.75 7.13 T. geminata 42.5 11.96 16.28 11 8.61 6.88 7.78 T. geminata 42.5 13.01 16.81 11.8 9.11 7.03 8.18 T. geminata 42.5 11.72 15.76 10.42 9.03 6.47 6.71 T. geminata 42.5 12.09 16.76 10.98 8.66 7.35 8.53 T. geminata 42.5 11.86 15.55 10.43 8.26 6.48 7.19

90

T. geminata 42.5 12.75 16.65 11.07 8.75 6.62 7.58 T. geminata 42.5 12.19 15.47 10.81 8.48 6.9 7.36 T. geminata 42.5 14.1 16.93 12.38 9.36 7.7 8.3 T. geminata 42.5 13.07 16.69 11.41 8.42 6.85 7.97 T. geminata 42.5 12.66 16.88 11.01 8.53 7.3 8.21 T. geminata 42.5 12.25 16.07 10.78 8.73 6.92 7.66 T. geminata 42.5 13.13 17.02 11.76 8.83 7.26 8.29 T. geminata 42.5 14.62 18.18 13.09 9.7 7.44 8.81 T. geminata 42.5 12.92 16.31 11.19 8.78 7.36 8.54 T. geminata 42.5 11.93 15.91 10.42 8.03 6.22 7.64 T. geminata 42.5 14.29 17.71 12.64 9.88 7.86 8.63 T. geminata 42.5 11.36 16.81 10.46 8.73 6.83 8.18 T. geminata 42.5 12.61 15.68 10.98 8.78 6.86 7.27 T. geminata 42.5 13.77 17.43 12 8.92 7.38 8.28 T. geminata 42.5 13.62 17.02 11.64 8.55 6.94 8.2 T. geminata 42.5 13.04 16.22 11.2 8.64 7.31 7.69 T. geminata 42.5 12.85 16.34 11.58 9.3 7.36 8.1 T. geminata 42.5 12.13 15.78 10.99 8.47 6.64 7.42 T. geminata 42.5 13.16 18.2 11.93 9.23 7.91 9.3 T. geminata 42.5 12.56 16.05 10.88 8.25 7.18 7.87 T. geminata 42.5 12.81 16.63 11.56 9.63 7.61 8.37 T. geminata 42.5 13.25 18.14 11.8 9.65 7.27 8.37 T. geminata 42.5 12.8 16.57 11.03 8.73 7.19 8.31 T. geminata 42.5 11.9 15.69 10.58 8.06 6.57 7.62 T. geminata 42.5 13.25 16.65 11.32 8.47 6.84 7.92 T. geminata 42.5 11.39 15.24 10.3 7.9 6.13 7.3 T. geminata 42.5 12.56 16.92 11.52 9.87 7.82 8.11 T. geminata 42.5 11.8 14.99 10.36 8.29 6.45 7.13 T. geminata 42.5 12.36 15.85 10.83 8.41 6.37 7.2 T. geminata 42.5 11.52 15.68 10.05 8.46 6.34 7.91 T. geminata 42.5 12.83 17.19 11.4 8.8 7.25 8.02 T. geminata 42.5 12.81 16.48 11.01 8.7 7.14 7.48 T. geminata 42.5 11.16 15.34 10.06 8.41 6.15 7.55 T. geminata 42.5 13.67 17.85 12.29 9.33 7.42 8.45 T. geminata 42.5 12.79 16.17 10.95 8.26 6.11 7.62 T. geminata 42.5 12.36 16.09 10.9 8.37 6.32 6.81 T. geminata 42.5 11.5 15.96 10.2 8.49 6.39 7.57 T. geminata 42.5 11.5 14.91 10.17 7.66 6.31 6.5 T. geminata 42.5 13.7 17.3 12.09 9.88 8.05 7.93 T. geminata 42.5 12.36 16.2 10.92 8.83 6.8 7.79 T. geminata 42.5 12.49 17.07 11.42 9.87 8.01 8.56 T. geminata 42.5 11.57 16.12 10.3 9.07 7.04 8.89 T. geminata 42.5 11.47 14.66 9.94 8.15 6.59 7.17 T. geminata 42.5 13.69 17.54 11.87 8.71 7.02 8.78 T. geminata 42.5 12.78 16.03 11.3 8.35 7.15 8.16 T. geminata 42.5 11.18 15.53 9.96 8.19 6.3 7.41 T. geminata 42.5 14.04 17.19 12.14 9.06 7.67 8.53 T. geminata 42.5 12.61 16.78 11.24 8.98 7.17 8.52 T. geminata 42.5 11.27 15.19 10.02 8.36 6.81 7.06 T. geminata 42.5 12.37 15.19 10.49 7.4 5.91 6.72

91

T. geminata 42.5 14.6 17.98 13.26 9.65 7.49 8.73 T. geminata 42.5 13.08 17.51 11.01 8.83 7.08 8.93 T. geminata 42.5 13.27 16.82 12.11 9.61 7.91 7.94 T. geminata 42.5 12.79 16.58 11.59 9.65 7.53 7.96 T. geminata 42.5 14.23 17.16 12.16 9.11 7.66 8 T. geminata 42.5 12.22 15.91 10.64 8.5 6.92 7.38 T. geminata 42.5 12.5 17.01 11.32 8.91 7.02 8.39 T. geminata 42.5 11.23 15.19 9.84 8.21 6.12 7.01 T. geminata 42.5 14.24 16.9 12.31 9.1 7.71 8.15 T. geminata 42.5 15.34 14.33 13.49 10.03 7.92 9.27 T. geminata 42.5 14.09 16.89 11.8 9.19 7.44 6.94 T. geminata 42.5 13.22 16.97 11.44 8.88 7.16 7.97 T. geminata 42.5 11.56 15.29 10.1 8.2 6.83 7.34 T. geminata 42.5 12.68 16.24 11 8.05 6.49 7.98 T. geminata 42.5 12.4 16.78 11.03 8.52 6.76 7.74 T. geminata 42.5 11.68 15.18 10.34 8.51 6.84 7.05 T. geminata 42.5 11.67 14.82 10.17 8.24 6.71 7.43 T. geminata 42.5 13.56 17.12 11.78 9.25 7.5 8.03 T. geminata 42.5 13 16.18 11.33 8.61 7.43 7.64 T. geminata 42.5 11.54 15.49 10.15 8.38 6.72 7.4 T. geminata 42.5 13 16.91 11.47 8.64 6.31 7.56 T. geminata 42.5 12.49 16.31 10.72 7.95 6.69 7.53 T. geminata 42.5 12.42 17.45 11.01 9.08 7.33 8.26 T. geminata 42.5 12.4 16.64 11.08 8.74 6.99 7.71 T. geminata 42.5 11.18 14.83 9.96 8.21 6.4 6.49 T. geminata 42.5 12.41 15.5 10.28 7.9 6.43 7.38 T. geminata 42.5 10.68 13.83 9.35 7.7 6.41 6.81 T. geminata 42.5 10.83 14.5 9.72 8.62 7.02 7.15 T. geminata 42.5 11 15.22 9.45 7.54 6.03 6.64 T. geminata 42.5 10.93 14.73 9.95 8.18 6.55 6.79 T. geminata 42.5 11.44 15.66 10.32 8.36 6.07 7.3 T. geminata 42.5 12.75 16.82 11.75 9.16 6.18 6.2 T. geminata 42.5 12.06 16.23 10.48 7.98 6.8 7.89 T. geminata 42.5 13.13 17.04 11.35 8.54 7.21 8.19 T. geminata 42.5 12.16 16.28 10.29 8.53 7.33 7.67 T. geminata 42.5 13.22 17.08 11.5 9.25 7.46 8.06 T. geminata 42.5 11.44 14.64 10.02 8.04 6.32 6.44 T. geminata 42.5 14.63 17.3 12.3 9.35 7.33 8.03 T. geminata 42.5 14.42 17.87 12.63 9.98 7.9 10.17 T. geminata 42.5 14.92 18.2 13 9.68 8.37 8.91 T. geminata 42.5 10.75 14.48 9.49 7.83 6.38 7.39 T. geminata 42.5 8.99 13.08 7.79 5.89 5.41 6.42 T. geminata 42.5 14.98 17.71 13.08 10.26 8.09 8.67 T. geminata 42.5 14.5 17.89 12.95 9.75 8.05 9.52 T. geminata 42.5 15.05 18.41 13.47 11.02 9.1 9.95 T. geminata 42.5 13.68 17.7 12.73 9.84 7.97 9.62

92

Appendix 3. Published maximum diameter of acritarchs from species descriptions (µm).

Genus Maximum Diameter Bin

Heliosphaeridium 15 C3 Stellechinatum 20 C3 Comasphaeridium 25 C3 Timofeevia 27 C3 Polygonium 35 C3 Retisphaeridium 35 C3 Timofeevia 40 C3 Trichosphaeridium 40 C3 Cristallinium 45 C3 Cristallinium 45 C3 Eliasum 67 C3 Leiosphaeridia 140 C3 Micrhystridium 7 C3 Myxococcoides 12 C3 Micrhystridium 19 C3 Lophosphaeridium 20 C3 Micrhystridium 21 C3 Paleasphaeridium 23 C3 Baltisphaeridium 24 C3 Skiagia 25 C3 Lophosphaeridium 30 C3 Leiosphaeridia 45 C3 Dictyotidium 60 C3 Simia 60 C3 Leiosphaeridia 80 C3 Satka 83 C3 Leiosphaeridia 85 C3 Pirea 87 C3 Chomotriletes 87 C3 Leiosphaeridia 100 C3 Unnamed 130 C3 Sinianella 175 C3 Leiosphaeridia 240 C3 Leiosphaeridia 350 C3 Leiosphaeridia 1000 C3 Elektoriskos 5 C2 Heliosphaeridium 6 C2 Celtiberium 6 C2 Heliosphaeridium 6 C2 Asteridium 8 C2 Comasphaeridium 8 C2 Fimbriaglomerella 8 C2 Goniosphaeridium 8 C2 Heliosphaeridium 9 C2 Asteridium 9 C2 Estiastra 10 C2

93

Heliosphaeridium 10 C2 Heliosphaeridium 10 C2 Fimbriaglomerella 11 C2 Asteridium 12 C2 Heliosphaeridium 12 C2 Asteridium 15 C2 Heliosphaeridium 15 C2 Heliosphaeridium 16 C2 Cymatiosphaera 16 C2 Multiplicisphaeridium 16 C2 Asteridium 17 C2 Asteridium 17 C2 Asteridium 17 C2 Heliosphaeridium 18 C2 Heliosphaeridium 18 C2 Heliosphaeridium 20 C2 Multiplicisphaeridium 20 C2 Volkovia 20 C2 Granomarginata 20 C2 Asteridium 21 C2 Comasphaeridium 22 C2 Baltisphaeridium 24 C2 Heliosphaeridium 24 C2 Fimbriaglomerella 25 C2 Pterospermella 25 C2 Alliumella 26 C2 Globosphaeridium 30 C2 Pterospermella 30 C2 Pterospermella 30 C2 Comasphaeridium 30 C2 Skiagia 30 C2 Skiagia 32 C2 Skiagia 33 C2 Leipaina 34 C2 Skiagia 34 C2 Globosphaeridium 35 C2 Skiagia 35 C2 Skiagia 35 C2 Baltisphaeridium 35 C2 Globosphaeridium 35 C2 Archaeodiscina 36 C2 Lophosphaeridium 36 C2 Lophosphaeridium 36 C2 Globosphaeridium 36 C2 Skiagia 36 C2 Baltisphaeridium 37 C2 Dictyotidium 37 C2 Goniosphaeridium 38 C2 Lophosphaeridium 38 C2 Skiagia 38 C2

94

Skiagia 38 C2 Archaeodiscina 38 C2 Comasphaeridium 39 C2 Goniosphaeridium 39 C2 Skiagia 40 C2 Retisphaeridium 40 C2 Fimbriaglomerella 41 C2 Granomarginata 43 C2 Goniosphaeridium 44 C2 Cymatiosphaera 45 C2 Skiagia 45 C2 Skiagia 45 C2 Lophosphaeridium 46 C2 Comasphaeridium 47 C2 Goniosphaeridium 48 C2 Comasphaeridium 48 C2 Cymatiosphaera 50 C2 Skiagia 50 C2 Lophosphaeridium 50 C2 Comasphaeridium 60 C2 Trachysphaeridium 62 C2 Comasphaeridium 70 C2 Tasmanites 70 C2 Lophosphaeridium 80 C2 Dictyotidium 80 C2 Leiosphaeridia 80 C2 Leiovalia 80 C2 Tasmanites 90 C2 Tasmanites 100 C2 Lophosphaeridium 110 C2 Tasmanites 120 C2 Tasmanites 124 C2 Tasmanites 150 C2 Comasphaeridium 180 C2 Tasmanites 184 C2 Micrhystridium 5 C1 Micrhystridium 10 C1 Asteridium 11 C1 Heliosphaeridium 11 C1 Comasphaeridium 12 C1 Micrhystridium 12 C1 Heliosphaeridium 13 C1 Micrhystridium 14 C1 Comasphaeridium 14 C1 Micrhystridium 15 C1 Bavlinella 16 C1 Small 18 C1 Symphysosphaera 18 C1 Estiastra 19 C1 Asteridium 20 C1

95

Fimbriaglomerella 20 C1 Asteridium 21 C1 Asteridium 21 C1 Protosphaeridium 25 C1 Comasphaeridium 26 C1 Pterospermella 26 C1 Celtiberium 26 C1 Celtiberium 26 C1 Granomarginata 27 C1 Comasphaeridium 28 C1 Comasphaeridium 30 C1 Granomarginata 30 C1 Granomarginata 30 C1 Pterospermella 32 C1 Archaeodiscina 32 C1 Lophosphaeridium 32 C1 Skiagia 32 C1 Baltisphaeridium 33 C1 Comasphaeridium 33 C1 Skiagia 33 C1 Pterospermella 35 C1 Skiagia 35 C1 Cymatiosphaera 36 C1 Goniosphaeridium 36 C1 Granomarginata 37 C1 Skiagia 40 C1 Skiagia 42 C1 Skiagia 43 C1 Goniosphaeridium 47 C1 Leiosphaeridia 65 C1 Trachysphaeridium 78 C1 Tasmanites 82 C1 Tasmanites 123 C1 Tasmanites 160 C1 Leiosphaeridia 400 C1 Leiosphaeridia 400 C1 Leiosphaeridia 330 N3 Satka 9 N3 Micrhystridium 12 N3 Baltisphaeridium 30 N3 Synsphaeridium 30 N3 Simia 35 N3 Octoedryxium 40 N3 Goniosphaeridium 42 N3 Eotylotopalla 42 N3 Eotylotopalla 45 N3 Leiosphaeridia 45 N3 Meghystrichosphaeridium 45 N3 Eotylotopalla 50 N3 Myxococcoides 50 N3

96

Trachyhystrichosphaera 52 N3 Dictyotidium 54 N3 Comasphaeridium 55 N3 Germinosphaera 55 N3 Pterospermopsimorpha 55 N3 Lophosphaeridium 60 N3 Goniosphaeridium 60 N3 Simia 60 N3 Trachysphaeridium 60 N3 Leiosphaeridia 60 N3 Leiosphaeridia 60 N3 Leiosphaeridia 60 N3 Leiosphaeridia 65 N3 Cavaspina 68 N3 Filisphaeridium 70 N3 Meghystrichosphaeridium 70 N3 Trachysphaeridium 70 N3 Leiosphaeridia 70 N3 Dicrospinasphaera 75 N3 Polyhedrosphaeridium 80 N3 Briareus 80 N3 Echinosphaeridium 85 N3 Solisphaeridium 86 N3 Vandalosphaeridium 87 N3 Meghystrichosphaeridium 95 N3 Goniosphaeridium 97 N3 Goniosphaeridium 100 N3 Kirbia 100 N3 Leiosphaeridia 100 N3 Astercapsoides 104 N3 Dictyotidium 108 N3 Appendisphaera 115 N3 Tanarium 115 N3 Comasphaeridium 120 N3 Ericiasphaera 120 N3 Appendisphaera 121 N3 Trachyhystrichosphaera 122 N3 Distosphaera 125 N3 Meghystrichosphaeridium 125 N3 Solisphaeridium 127 N3 Ericiasphaera 130 N3 Cavaspina 133 N3 Solisphaeridium 135 N3 Hocosphaeridium 138 N3 Ericiasphaera 139 N3 Vulcanisphaera 140 N3 Appendisphaera 147 N3 Sphaerocongregus 170 N3 Comasphaeridium 173 N3 Sinianella 175 N3

97

Goniosphaeridium 176 N3 Tanarium 176 N3 Apodastoides 180 N3 Mastosphaera 182 N3 Melanocyrillium 189 N3 Tasmanites 195 N3 Goniosphaeridium 200 N3 Meghystrichosphaeridium 200 N3 Leiosphaeridia 200 N3 Leiosphaeridia 200 N3 Briareus 200 N3 Cymatiosphaeroides 205 N3 Tanarium 207 N3 Sphaerocongregus 210 N3 Baltisphaeridium 220 N3 Sticcasphaeridium 220 N3 Monosozosphaeridium 225 N3 Trachyhystrichosphaera 230 N3 Ericiasphaera 233 N3 Cymatiosphaeroides 236 N3 Rhopaliophora 236 N3 Goniosphaeridium 240 N3 Leiosphaeridia 240 N3 Palaeovolvox 240 N3 Papillomembrana 240 N3 Amadeusphaeridium 245 N3 Indigestosphaeridium 248 N3 Ericiasphaera 275 N3 Trachyhystrichosphaera 275 N3 Gyalosphaeridium 276 N3 Variomargosphaeridium 288 N3 Gyalosphaeridium 297 N3 Trachyhystrichosphaera 297 N3 Amadeusphaeridium 300 N3 Schizofusa 300 N3 Filisphaeridium 302 N3 Somphosphaeridium 306 N3 Trachyhystrichosphaera 316 N3 Gyalosphaeridium 320 N3 Meghystrichosphaeridium 350 N3 Papillomembrana 350 N3 Alicesphaeridium 350 N3 Leiosphaeridia 350 N3 Favososphaeridium 350 N3 Baltisphaeridium 352 N3 Multifronsphaeridium 384 N3 Meghystrichosphaeridium 400 N3 Castaneasphaera 420 N3 Unnamed 420 N3 Spheromorphs 424 N3

98

Polyhedrosphaeridium 433 N3 Cucumiforma 440 N3 Bacatisphaera 450 N3 Sinosphaera 525 N3 Asterocapsoides 600 N3 Unnamed 600 N3 Echinosphaeridium 650 N3 Echinosphaeridium 650 N3 Meghystrichosphaeridium 700 N3 Meghystrichosphaeridium 700 N3 Cerionopora 730 N3 Tianzhushania 750 N3 Trachyhystrichosphaera 765 N3 Tianzhushania 850 N3 Unnamed 1000 N3 Leiosphaeridia 1000 N3 Leiosphaeridia 1300 N3 Micrhystridium 20 N3 Bavlinella 25 N3 Leiomarginata 25 N3 Granomarginata 27 N3 Baltisphaeridium 28 N3 Polyedryxium 30 N3 Paracrassasphaera 32 N3 Polyedryxium 35 N3 Baltisphaeridium 37 N3 Octoedryxium 45 N3 Baltisphaeridium 125 N3 Leiovalvia 130 N3 Baltisphaeridium 150 N3 Leiosphaeridia 500 N3 Pterospermopsimorpha 20 N2 Trachysphaeridium 40 N2 Vandalosphaeridium 40 N2 Protosphaeridium 50 N2 Kildinella 70 N2 Octoedryxium 16 N2 Bavlinella 20 N2 Chuaria 410 N2 Bavlinella 12 N1 Sphaeromorph 15 N1 Stictosphaeridium 30 N1 Octoedryxium 40 N1 Enigmatic 40 N1 Kildinosphaera 60 N1 Leiosphaeridia 60 N1 Kildinosphaera 70 N1 Podolina 80 N1 Kildinosphaera 135 N1 Trachysphaeridium 225 N1

99

Kildinosphaera 230 N1 Chuaria 333 N1 Leiosphaeridia 41 N1 Vandalosphaeridium 45 N1 Trachysphaeridium 50 N1 Trachysphaeridium 50 N1 Cymatiosphaeroides 50 N1 Trachysphaeridium 80 N1 Trachysphaeridium 80 N1 Vase-Shaped 99 N1 Leiosphaeridia 100 N1 Leiosphaeridia 100 N1 Kildinosphaera 177 N1 Kildinosphaera 177 N1 Kildinosphaera 216 N1 Kildinosphaera 216 N1 Kildinosphaera 250 N1 Kildinosphaera 255 N1 Tasmanites 296 N1 Tasmanites 296 N1 Satka 300 N1 Chuaria 712 N1 Bavlinella 15 N1 Pterospermopsis 25 N1 Protosphaeridium 30 N1 Synsphaeridium 30 N1 Leiosphaeridia 30 N1 Pterospermopsis 30 N1 Trachysphaeridium 30 N1 Striasphaera 30 N1 Stictosphaeridium 34 N1 Germinosphaera 35 N1 Cymatiosphaera 35 N1 Striasphaera 35 N1 Enigmatic 40 N1 Trachysphaeridium 40 N1 Nucellosphaeridium 40 N1 Trachysphaeridium 42 N1 Triangular 42 N1 Pterospermopsimorpha 43 N1 Pterospermopsimorpha 45 N1 Palaeosphaeridium 45 N1 Pterospermopsimorpha 48 N1 Trachysphaeridium 50 N1 Kildinella 50 N1 Trachysphaeridium 57 N1 Cymatiosphaeroides 58 N1 Dictyotidium 60 N1 Kildinella 62 N1 Kildinella 64 N1

100

Trematosphaeridium 64 N1 Protosphaeridium 68 N1 Leiosphaeridia 70 N1 Kildinella 70 N1 Kildinella 70 N1 Leiosphaeridia 70 N1 Kildinella 72 N1 Comasphaeridium 75 N1 Kildinella 77 N1 Octoedryxium 80 N1 Stictosphaeridium 80 N1 Pteinosphaeridium 83 N1 Germinosphaera 86 N1 Trachysphaeridium 100 N1 Nucellosphaeridium 100 N1 Trachysphaeridium 115 N1 Germinosphaera 120 N1 Oculosphaera 131 N1 Kildinella 132 N1 Favososphaeridium 144 N1 Stictosphaeridium 150 N1 Nucellosphaeridium 200 N1 Palaeodiacrodium 200 N1 Leiosphaeridia 210 N1 Trachyhystrichosphaera 235 N1 Gorgonisphaeridium 250 N1 Trachyhystrichosphaera 250 N1 Leiosphaeridia 265 N1 Cymatiosphaeroides 345 N1 Chuaria 410 N1 Leiosphaeridia 488 N1 Leiosphaeridia 624 N1 Trachyhystrichosphaera 702 N1 Leiosphaeridia 796 N1 Trachyhystrichosphaera 865 N1 Cerebrosphaera 960 N1 Chuaria 1000 N1 Leiosphaeridia 1325 N1 Protosphaeridium 2000 N1 Leiosphaeridia 2480 N1 Chuaria 3500 N1 Pterospermopsimorphid 35 N1 Kildinella 70 N1 Stictosphaeridium 80 N1 Cymatiosphaeroides 87 N1 Trachysphaeridium 91 N1 Trachysphaeridium 100 N1 Kildinella 150 N1 Pterospermopsimorphid 200 N1 Unnamed 200 N1

101

Trachysphaeridium 350 N1 Aimia 500 N1 Trachyhystrichosphaera 535 N1 Chuaria 600 N1 Satka 11 N1 Synsphaeridium 18 N1 Protoleiosphaeridium 45 N1 Spumosina 55 N1 Undetermined 70 N1 Leiosphaeridia 90 N1 Pololeptus 115 N1 Kildinosphaera 120 N1 Pololeptus 127 N1 Myxococcoides 6 N1 Sphaerophycus 11 N1 Gloeodiniopsis 14 N1 Myxococcoides 14 N1 Dasysphaeridium 15 N1 Comasphaeridium 18 N1 Micrhystridium 18 N1 Micrhystridium 18 N1 Skiagia 18 N1 Lophosphaeridium 20 N1 Glenobotrydion 22 N1 Melanocyrillium 37 N1 Octoedryxium 39 N1 Paracrassosphaera 40 N1 Unnamed 41 N1 Caudosphaera 45 N1 Leiosphaeridia 45 N1 Leiosphaeridia 45 N1 Dasysphaeridium 48 N1 Simia 60 N1 Simia 70 N1 Leiosphaeridia 80 N1 Leiosphaeridia 85 N1 Simia 96 N1 Leiosphaeridia 100 N1 Satka 145 N1 Sinianella 175 N1 Leiosphaeridia 200 N1 Trachyhystrichosphaera 250 N1 Leiosphaeridia 350 N1 Leiosphaeridia 1000 N1 Satka 14 N1 Synsphaeridium 17 N1 Leiosphaeridia 52 N1 Stictosphaeridium 63 N1 Kildinosphaera 78 N1 Kildinosphaera 85 N1

102

Favososphaeridium 95 N1 Chuaria 300 N1 Gemmuloides 482 N1 Tappania 100 M2 Tappania 110 M2 Shuiyousphaeridium 357 M2 Spumosina 40 M2 Pterospermopsimorpha 42 M2 Symplassosphaeridium 44 M2 Satka 64 M2 Leiosphaeridia 69 M2 Leiosphaeridia 69 M2 Synsphaeridium 105 M2 Eomicrocystis 108 M2 Fabiformis 120 M2 Shuiyousphaeridium 133 M2 Shuiyousphaeridium 145 M2 Valeria 153 M2 Dictyosphaera 160 M2 Dictyosphaera 160 M2 Leiosphaeridia 196 M2 Leiosphaeridia 228 M2 Dictyosphaera 274 M2 Leiosphaeridia 345 M2 Lophosphaeridium 48 M2 Leiosphaeridia 70 M2 Leiosphaeridia 70 M2 Leiosphaeridia 107 M2 Pterospermopsimorpha 155 M2 Leiosphaeridia 228 M2 Valeria 340 M2 Leiosphaeridia 395 M2 Pterospermopsimorpha 23 M1 Leiosphaeridia 60 M1 Leiosphaeridia 60 M1 Satka 61 M1 Tappania 160 M1 Goniocystis 68 P1 Kildinella 85 P1 Goniocystis 102 P1 Thecatovalvia 129 P1 Schizospora 135 P1 Schizospora 172 P1 Pterospermopsimorpha 185 P1 Valvimorpha 200 P1 Chuaria 200 P1 Heteropetalia 213 P1 Valvimorpha 216 P1 Leiosphaeridia 238 P1 Schizofusa 243 P1

103

Pseudofavososphaera 250 P1 Nucellosphaeridium 252 P1 Schizofusa 260 P1 Schizofusa 263 P1 Leiosphaeridia 354 P1 Schizospora 361 P1 Schizospora 361 P1

104

Appendix 4. Published mean diameter of acritarchs from species descriptions (µm).

Genus Mean

Diameter Bin Trichosphaeridium 40.00 C3 Elektoriskos 4.50 C2 Goniosphaeridium 7.20 C2 Estiastra 7.23 C2 Heliosphaeridium 7.44 C2 Fimbriaglomerella 8.00 C2 Comasphaeridium 8.08 C2 Comasphaeridium 8.60 C2 Asteridium 9.68 C2 Heliosphaeridium 10.00 C2 Fimbriaglomerella 10.50 C2 Heliosphaeridium 10.70 C2 Asteridium 10.80 C2 Asteridium 12.15 C2 Heliosphaeridium 13.33 C2 Heliosphaeridium 14.30 C2 Heliosphaeridium 15.27 C2 Pterospermella 19.55 C2 Multiplicisphaeridium 20.00 C2 Volkovia 20.00 C2 Granomarginata 20.00 C2 Comasphaeridium 20.30 C2 Alliumella 22.36 C2 Globosphaeridium 25.77 C2 Globosphaeridium 27.35 C2 Skiagia 27.50 C2 Goniosphaeridium 27.88 C2 Leipaina 27.92 C2 Skiagia 30.30 C2 Skiagia 30.60 C2 Skiagia 31.70 C2 Cymatiosphaera 31.82 C2 Skiagia 31.86 C2 Skiagia 32.27 C2 Skiagia 32.60 C2 Skiagia 32.90 C2 Cymatiosphaera 33.00 C2 Skiagia 33.70 C2 Skiagia 34.68 C2 Comasphaeridium 35.64 C2 Archaeodiscina 36.00 C2 Skiagia 36.00 C2 Goniosphaeridium 38.00 C2 Skiagia 38.00 C2 Lophosphaeridium 40.00 C2 Goniosphaeridium 44.00 C2

105

Lophosphaeridium 45.75 C2 Lophosphaeridium 50.00 C2 Tasmanites 80.22 C2 Tasmanites 90.00 C2 Tasmanites 90.40 C2 Comasphaeridium 94.10 C2 Tasmanites 95.00 C2 Tasmanites 150.00 C2 Comasphaeridium 180.00 C2 Micrhystridium 4.00 C1 Asteridium 8.00 C1 Heliosphaeridium 8.10 C1 Micrhystridium 9.00 C1 Heliosphaeridium 9.20 C1 Bavlinella 9.30 C1 Small 9.80 C1 Micrhystridium 10.00 C1 Micrhystridium 10.00 C1 Micrhystridium 11.50 C1 Comasphaeridium 12.70 C1 Comasphaeridium 13.34 C1 Asteridium 13.36 C1 Asteridium 14.65 C1 Asteridium 14.82 C1 Estiastra 19.00 C1 Pterospermella 21.00 C1 Granomarginata 22.00 C1 Granomarginata 22.50 C1 Comasphaeridium 22.94 C1 Granomarginata 23.18 C1 Comasphaeridium 23.50 C1 Comasphaeridium 23.76 C1 Granomarginata 23.82 C1 Pterospermella 25.06 C1 Skiagia 25.50 C1 Celtiberium 26.00 C1 Celtiberium 26.00 C1 Archaeodiscina 26.50 C1 Skiagia 26.50 C1 Baltisphaeridium 27.50 C1 Cymatiosphaera 28.60 C1 Skiagia 29.00 C1 Skiagia 30.50 C1 Skiagia 31.00 C1 Skiagia 31.50 C1 Leiosphaeridia 33.00 C1 Goniosphaeridium 36.00 C1 Trachysphaeridium 78.00 C1 Tasmanites 80.00 C1 Tasmanites 81.00 C1

106

Tasmanites 91.00 C1 Leiosphaeridia 289.00 C1 Leiosphaeridia 289.00 C1 Leiosphaeridia 55.38 N3 Goniosphaeridium 42.00 N3 Cavaspina 57.00 N3 Filisphaeridium 70.00 N3 Polyhedrosphaeridium 80.00 N3 Solisphaeridium 86.00 N3 Cavaspina 96.90 N3 Astercapsoides 104.00 N3 Appendisphaera 115.00 N3 Ericiasphaera 120.00 N3 Trachyhystrichosphaera 122.00 N3 Tanarium 124.30 N3 Meghystrichosphaeridium 125.00 N3 Tanarium 130.20 N3 Vulcanisphaera 140.00 N3 Leiosphaeridia 175.00 N3 Mastosphaera 182.00 N3 Meghystrichosphaeridium 350.00 N3 Castaneasphaera 420.00 N3 Octoedryxium 14.00 N2 Trachysphaeridium 53.50 N1 Trachysphaeridium 53.50 N1 Leiosphaeridia 58.00 N1 Leiosphaeridia 58.00 N1 Kildinosphaera 143.00 N1 Satka 164.00 N1 Chuaria 275.00 N1 Leiosphaeridia 19.10 N1 Goniosphaeridium 24.00 N1 Protosphaeridium 24.60 N1 Germinosphaera 25.00 N1 Dictyotidium 33.00 N1 Pterospermopsimorpha 40.00 N1 Triangular 42.00 N1 Pterospermopsimorpha 43.00 N1 Kildinella 50.00 N1 Kildinella 56.00 N1 Cymatiosphaeroides 57.60 N1 Favososphaeridium 60.00 N1 Germinosphaera 71.00 N1 Oculosphaera 78.00 N1 Germinosphaera 87.00 N1 Cymatiosphaeroides 129.00 N1 Trachyhystrichosphaera 160.00 N1 Leiosphaeridia 232.00 N1 Leiosphaeridia 237.00 N1 Gorgonisphaeridium 250.00 N1

107

Trachyhystrichosphaera 250.00 N1 Trachyhystrichosphaera 264.00 N1 Leiosphaeridia 319.00 N1 Cerebrosphaera 365.00 N1 Leiosphaeridia 798.00 N1 Trachyhystrichosphaera 865.00 N1 Leiosphaeridia 1270.00 N1 Chuaria 1760.00 N1 Trachysphaeridium 59.00 N1 Stictosphaeridium 80.00 N1 Cymatiosphaeroides 81.00 N1 Unnamed 156.00 N1 Chuaria 310.00 N1 Trachyhystrichosphaera 317.00 N1 Leiosphaeridia 32.90 N1 Kildinosphaera 40.00 N1 Kildinosphaera 52.20 N1 Favososphaeridium 95.00 N1 Shuiyousphaeridium 357.00 M2 Spumosina 27.60 M2 Leiosphaeridia 33.60 M2 Symplassosphaeridium 33.70 M2 Synsphaeridium 50.10 M2 Eomicrocystis 59.60 M2 Leiosphaeridia 76.60 M2 Fabiformis 92.00 M2 Leiosphaeridia 103.90 M2 Leiosphaeridia 124.80 M2 Dictyosphaera 274.00 M2 Leiosphaeridia 36.40 M2 Lophosphaeridium 48.00 M2 Leiosphaeridia 49.20 M2 Leiosphaeridia 57.10 M2 Pterospermopsimorpha 58.50 M2 Leiosphaeridia 112.10 M2 Leiosphaeridia 129.00 M2 Valeria 158.40 M2 Leiosphaeridia 60.00 P1 Pterospermopsimorpha 185.00 P1 Heteropetalia 213.00 P1

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Appendix 5. Diameter (µm) of figured acritarch specimens.

Genus Figure

Diameter BinHeliosphaeridium 13.10 C3 Polygonium 13.79 C3 Polygonium 14.48 C3 Polygonium 14.83 C3 Polygonium 16.55 C3 Comasphaeridium 22.50 C3 Timofeevia 26.52 C3 Timofeevia 26.96 C3 Timofeevia 27.39 C3 Aryballomorpha 29.25 C3 Timofeevia 31.30 C3 Cristallinium 33.08 C3 Cristallinium 33.08 C3 Cristallinium 38.08 C3 Cristallinium 40.38 C3 Cristallinium 42.31 C3 Cristallinium 46.92 C3 Micrhystridium 8.21 C3 Lophosphaeridium 18.97 C3 Micrhystridium 19.00 C3 Skiagia 20.51 C3 Baltisphaeridium 21.00 C3 Micrhystridium 21.00 C3 Baltisphaeridium 22.00 C3 Micrhystridium 22.00 C3 Skiagia 22.56 C3 Baltisphaeridium 23.00 C3 Simia 23.40 C3 Skiagia 23.59 C3 Lophosphaeridium 24.62 C3 Skiagia 26.15 C3 Leiosphaeridia 27.46 C3 Lophosphaeridium 30.26 C3 Leiosphaeridia 32.59 C3 Dictyotidium 34.87 C3 Dictyotidium 36.92 C3 Leiosphaeridia 40.00 C3 Dictyotidium 41.03 C3 Chomotriletes 57.89 C3 Leiosphaeridia 58.27 C3 Leiosphaeridia 59.40 C3 Leiosphaeridia 59.77 C3 Leiosphaeridia 60.50 C3 Leiosphaeridia 68.36 C3 Satka 75.92 C3 Satka 79.15 C3

109

Satka 80.77 C3 Chomotriletes 88.11 C3 Chomotriletes 94.63 C3 Leiosphaeridia 98.54 C3 Leiosphaeridia 111.46 C3 Leiosphaeridia 121.50 C3 Leiosphaeridia 158.33 C3 Leiosphaeridia 158.97 C3 Leiosphaeridia 315.38 C3 Celtiberium 6.00 C2 Pterospermella 6.34 C2 Comasphaeridium 6.50 C2 Goniosphaeridium 7.00 C2 Leiosphaeridia 7.32 C2 Comasphaeridium 7.50 C2 Fimbriaglomerella 8.00 C2 Asteridium 9.25 C2 Heliosphaeridium 10.00 C2 Comasphaeridium 10.24 C2 Heliosphaeridium 10.25 C2 Fimbriaglomerella 10.50 C2 Comasphaeridium 10.73 C2 Goniosphaeridium 11.50 C2 Heliosphaeridium 11.50 C2 Comasphaeridium 11.71 C2 Asteridium 13.50 C2 Multiplicisphaeridium 15.37 C2 Heliosphaeridium 18.85 C2 Lophosphaeridium 20.00 C2 Elektoriskos 21.00 C2 Heliosphaeridium 22.00 C2 Skiagia 22.44 C2 Skiagia 22.50 C2 Comasphaeridium 23.41 C2 Cymatiosphaera 24.39 C2 Comasphaeridium 24.88 C2 Retisphaeridium 25.50 C2 Skiagia 25.75 C2 Dictyotidium 25.85 C2 Retisphaeridium 26.50 C2 Skiagia 26.83 C2 Skiagia 27.78 C2 Skiagia 27.80 C2 Skiagia 28.00 C2 Comasphaeridium 28.50 C2 Heliosphaeridium 28.50 C2 Lophosphaeridium 28.50 C2 Skiagia 28.50 C2 Globosphaeridium 29.00 C2 Comasphaeridium 30.24 C2

110

Cymatiosphaera 30.49 C2 Skiagia 31.22 C2 Skiagia 31.71 C2 Goniosphaeridium 31.76 C2 Archaeodiscina 36.00 C2 Retisphaeridium 37.50 C2 Skiagia 39.57 C2 Lophosphaeridium 41.75 C2 Skiagia 41.95 C2 Tasmanites 52.96 C2 Tasmanites 68.89 C2 Tasmanites 73.70 C2 Tasmanites 121.33 C2 Baltisphaeridium 12.96 C2 Baltisphaeridium 14.40 C2 Baltisphaeridium 15.84 C2 Baltisphaeridium 23.04 C2 Tasmanites 171.05 C2 Estiastra 5.00 C2 Heliosphaeridium 6.75 C2 Heliosphaeridium 7.20 C2 Heliosphaeridium 7.20 C2 Estiastra 8.50 C2 Heliosphaeridium 9.00 C2 Heliosphaeridium 9.00 C2 Heliosphaeridium 9.75 C2 Estiastra 10.00 C2 Heliosphaeridium 10.20 C2 Estiastra 10.50 C2 Heliosphaeridium 12.00 C2 Heliosphaeridium 13.00 C2 Heliosphaeridium 13.20 C2 Asteridium 13.50 C2 Heliosphaeridium 13.80 C2 Heliosphaeridium 13.80 C2 Heliosphaeridium 15.00 C2 Heliosphaeridium 15.60 C2 Asteridium 15.75 C2 Heliosphaeridium 16.20 C2 Heliosphaeridium 16.20 C2 Asteridium 16.50 C2 Asteridium 16.50 C2 Heliosphaeridium 16.80 C2 Heliosphaeridium 17.40 C2 Leipaina 17.50 C2 Heliosphaeridium 18.60 C2 Pterospermella 21.05 C2 Leiosphaeridia 21.54 C2 Skiagia 21.75 C2 Fimbriaglomerella 22.50 C2

111

Pterospermella 23.16 C2 Leipaina 23.75 C2 Multiplicisphaeridium 24.00 C2 Lophosphaeridium 24.75 C2 Goniosphaeridium 26.15 C2 Skiagia 26.46 C2 Skiagia 27.00 C2 Skiagia 27.08 C2 Globosphaeridium 28.42 C2 Skiagia 28.50 C2 Skiagia 29.25 C2 Skiagia 29.25 C2 Skiagia 29.54 C2 Granomarginata 29.74 C2 Leiosphaeridia 31.50 C2 Skiagia 32.00 C2 Skiagia 32.31 C2 Globosphaeridium 32.37 C2 Skiagia 32.62 C2 Skiagia 33.08 C2 Skiagia 33.46 C2 Skiagia 33.85 C2 Skiagia 34.62 C2 Goniosphaeridium 34.87 C2 Globosphaeridium 35.53 C2 Skiagia 36.92 C2 Skiagia 36.92 C2 Skiagia 37.33 C2 Skiagia 37.50 C2 Cymatiosphaera 39.00 C2 Leiosphaeridia 39.00 C2 Cymatiosphaera 40.00 C2 Lophosphaeridium 44.62 C2 Leiosphaeridia 50.00 C2 Tasmanites 62.82 C2 Tasmanites 73.85 C2 Tasmanites 74.39 C2 Leiosphaeridia 75.38 C2 Leiosphaeridia 79.23 C2 Leiosphaeridia 89.74 C2 Granomarginata 20.00 C2 Granomarginata 22.07 C2 Dictyotidium 28.69 C2 Globosphaeridium 31.03 C2 Comasphaeridium 34.18 C2 Globosphaeridium 34.76 C2 Archaeodiscina 38.48 C2 Comasphaeridium 40.46 C2 Comasphaeridium 40.46 C2 Lophosphaeridium 47.03 C2

112

Comasphaeridium 49.50 C2 Tasmanites 61.55 C2 Tasmanites 67.03 C2 Micrhystridium 5.75 C1 Small 8.78 C1 Small 9.02 C1 Micrhystridium 9.25 C1 Micrhystridium 10.00 C1 Micrhystridium 10.25 C1 Bavlinella 10.49 C1 Micrhystridium 11.00 C1 Micrhystridium 11.25 C1 Micrhystridium 11.50 C1 Small 11.71 C1 Bavlinella 12.20 C1 Small 12.44 C1 Micrhystridium 14.50 C1 Comasphaeridium 17.14 C1 Protosphaeridium 18.54 C1 Pterospermella 20.00 C1 Granomarginata 21.00 C1 Skiagia 21.46 C1 Skiagia 21.46 C1 Lophosphaeridium 21.90 C1 Skiagia 22.44 C1 Baltisphaeridium 23.81 C1 Skiagia 23.90 C1 Lophosphaeridium 24.29 C1 Skiagia 24.39 C1 Evittia 24.50 C1 Granomarginata 25.00 C1 Skiagia 25.37 C1 Cymatiosphaera 25.71 C1 Baltisphaeridium 26.19 C1 Skiagia 26.34 C1 Skiagia 26.34 C1 Granomarginata 27.00 C1 Protosphaeridium 27.32 C1 Skiagia 27.32 C1 Granomarginata 27.50 C1 Archaeodiscina 28.10 C1 Skiagia 28.29 C1 Skiagia 29.27 C1 Skiagia 30.24 C1 Skiagia 30.24 C1 Leiosphaeridia 30.95 C1 Skiagia 31.22 C1 Baltisphaeridium 33.81 C1 Skiagia 34.15 C1 Skiagia 35.61 C1

113

Leiosphaeridia 36.19 C1 Skiagia 39.02 C1 Leiosphaeridia 47.50 C1 Tasmanites 71.95 C1 Tasmanites 75.61 C1 Tasmanites 84.15 C1 Tasmanites 92.68 C1 Tasmanites 104.88 C1 Leiosphaeridia 7.00 C1 Leiosphaeridia 11.50 C1 Comasphaeridium 12.00 C1 Asteridium 12.75 C1 Comasphaeridium 12.75 C1 Asteridium 15.75 C1 Fimbriaglomerella 17.00 C1 Comasphaeridium 21.75 C1 Comasphaeridium 22.50 C1 Comasphaeridium 23.25 C1 Pterospermella 24.21 C1 Granomarginata 26.46 C1 Pterospermella 26.84 C1 Comasphaeridium 27.00 C1 Pterospermella 32.37 C1 Pterospermella 37.89 C1 Pterospermella 40.00 C1 Granomarginata 41.03 C1 Leiosphaeridia 41.25 C1 Granomarginata 48.21 C1 Leiosphaeridia 51.75 C1 Leiosphaeridia 54.75 C1 Asteridium 7.12 C1 Asteridium 7.80 C1 Heliosphaeridium 7.80 C1 Heliosphaeridium 8.14 C1 Heliosphaeridium 8.14 C1 Heliosphaeridium 8.14 C1 Asteridium 9.15 C1 Heliosphaeridium 10.17 C1 Heliosphaeridium 12.88 C1 Comasphaeridium 13.90 C1 Comasphaeridium 13.90 C1 Leiosphaeridia 324.14 C1 Leiosphaeridia 400.00 C1 Leiosphaeridia 36.75 N3 Leiosphaeridia 64.80 N3 Leiosphaeridia 88.20 N3 Leiosphaeridia 103.25 N3 Eotylotopalla 30.00 N3 Baltisphaeridium 32.67 N3 Eotylotopalla 32.86 N3

114

Eotylotopalla 34.29 N3 Eotylotopalla 40.00 N3 Eotylotopalla 45.45 N3 Distosphaera 51.43 N3 Distosphaera 54.29 N3 Dicrospinasphaera 70.34 N3 Leiosphaeridia 75.86 N3 Leiosphaeridia 111.11 N3 Meghystrichosphaeridium 111.63 N3 Ericiasphaera 133.33 N3 Ericiasphaera 142.86 N3 Meghystrichosphaeridium 146.43 N3 Apodastoides 171.43 N3 Apodastoides 178.57 N3 Leiosphaeridia 190.48 N3 Meghystrichosphaeridium 217.65 N3 Echinosphaeridium 257.14 N3 Meghystrichosphaeridium 270.00 N3 Meghystrichosphaeridium 282.35 N3 Meghystrichosphaeridium 351.72 N3 Echinosphaeridium 400.00 N3 Bacatisphaera 400.00 N3 Meghystrichosphaeridium 402.35 N3 Castaneasphaera 425.45 N3 Bacatisphaera 427.27 N3 Bacatisphaera 454.55 N3 Cymatiosphaeroides 486.67 N3 Pustulisphaera 557.14 N3 Unnamed 1040.00 N3 Cavaspina 48.42 N3 Cavaspina 50.00 N3 Spheromorphs 66.25 N3 Cavaspina 72.00 N3 Appendisphaera 78.00 N3 Tanarium 84.38 N3 Appendisphaera 85.00 N3 Tanarium 85.45 N3 Tanarium 89.29 N3 Appendisphaera 96.00 N3 Cavaspina 97.92 N3 Tanarium 113.33 N3 Appendisphaera 116.00 N3 Tanarium 128.57 N3 Tanarium 178.57 N3 Spheromorphs 281.25 N3 Leiosphaeridia 12.84 N3 Simia 19.00 N3 Octoedryxium 21.60 N3 Octoedryxium 23.71 N3 Octoedryxium 24.30 N3

115

Octoedryxium 32.93 N3 Sphaerocongregus 44.00 N3 Comasphaeridium 44.59 N3 Solisphaeridium 46.15 N3 Comasphaeridium 51.90 N3 Dictyotidium 53.90 N3 Dictyotidium 59.05 N3 Sphaerocongregus 61.60 N3 Leiosphaeridia 65.71 N3 Comasphaeridium 71.15 N3 Comasphaeridium 76.92 N3 Goniosphaeridium 77.89 N3 Sphaerocongregus 83.70 N3 Dictyotidium 83.74 N3 Gyalosphaeridium 85.38 N3 Leiosphaeridia 89.74 N3 Goniosphaeridium 94.74 N3 Dictyotidium 95.42 N3 Solisphaeridium 98.89 N3 Dictyotidium 100.94 N3 Goniosphaeridium 101.84 N3 Solisphaeridium 104.44 N3 Sphaerocongregus 117.00 N3 Hocosphaeridium 120.00 N3 Cymatiosphaeroides 123.08 N3 Hocosphaeridium 123.75 N3 Leiosphaeridia 128.42 N3 Hocosphaeridium 135.00 N3 Palaeovolvox 138.89 N3 Monosozosphaeridium 141.75 N3 Cymatiosphaeroides 146.15 N3 Sphaerocongregus 148.00 N3 Palaeovolvox 148.15 N3 Cymatiosphaeroides 156.92 N3 Leiosphaeridia 161.54 N3 Leiosphaeridia 165.00 N3 Palaeovolvox 170.37 N3 Amadeusphaeridium 176.25 N3 Indigestosphaeridium 187.50 N3 Cymatiosphaeroides 189.00 N3 Amadeusphaeridium 191.25 N3 Cymatiosphaeroides 191.25 N3 Alicesphaeridium 193.50 N3 Goniosphaeridium 194.21 N3 Baltisphaeridium 195.00 N3 Cymatiosphaeroides 196.15 N3 Cymatiosphaeroides 196.15 N3 Gyalosphaeridium 196.15 N3 Indigestosphaeridium 196.88 N3 Monosozosphaeridium 198.75 N3

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Alicesphaeridium 207.00 N3 Baltisphaeridium 211.50 N3 Amadeusphaeridium 225.00 N3 Somphosphaeridium 226.67 N3 Baltisphaeridium 228.00 N3 Monosozosphaeridium 228.75 N3 Baltisphaeridium 229.50 N3 Gyalosphaeridium 229.50 N3 Polyhedrosphaeridium 232.50 N3 Indigestosphaeridium 242.31 N3 Alicesphaeridium 247.50 N3 Alicesphaeridium 247.50 N3 Monosozosphaeridium 247.50 N3 Somphosphaeridium 251.11 N3 Multifronsphaeridium 256.50 N3 Multifronsphaeridium 270.00 N3 Baltisphaeridium 280.25 N3 Filisphaeridium 286.15 N3 Gyalosphaeridium 290.77 N3 Polyhedrosphaeridium 292.50 N3 Multifronsphaeridium 294.75 N3 Polyhedrosphaeridium 299.25 N3 Polyhedrosphaeridium 324.00 N3 Multifronsphaeridium 339.75 N3 Baltisphaeridium 346.75 N3 Multifronsphaeridium 408.00 N3 Pterospermopsimorpha 28.44 N2 Vandalosphaeridium 43.00 N2 Stictosphaeridium 46.00 N2 Kildinella 55.00 N2 Stictosphaeridium 65.50 N2 Chuaria 233.33 N2 Bavlinella 28.57 N2 Octoedryxium 50.00 N2 Chuaria 328.95 N2 Bavlinella 8.96 N1 Protosphaeridium 13.76 N1 Enigmatic 21.12 N1 Enigmatic 21.44 N1 Octoedryxium 32.64 N1 Podolina 34.56 N1 Leiosphaeridia 42.88 N1 Podolina 51.84 N1 Kildinosphaera 56.16 N1 Kildinosphaera 56.16 N1 Kildinosphaera 65.52 N1 Kildinosphaera 78.52 N1 Satka 22.41 N1 Satka 22.41 N1 Trachysphaeridium 28.36 N1

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Leiosphaeridia 36.40 N1 Leiosphaeridia 38.13 N1 Vandalosphaeridium 38.57 N1 Trachysphaeridium 41.76 N1 Trachysphaeridium 45.07 N1 Satka 45.52 N1 Cymatiosphaeroides 53.23 N1 Leiosphaeridia 61.36 N1 Tasmanites 84.85 N1 Kildinosphaera 144.52 N1 Kildinosphaera 166.67 N1 Kildinosphaera 190.00 N1 Trachysphaeridium 33.88 N1 Leiosphaeridia 43.94 N1 Trachysphaeridium 47.67 N1 Kildinosphaera 164.52 N1 Leiosphaeridia 35.24 N1 Leiosphaeridia 46.67 N1 Leiosphaeridia 198.33 N1 Leiosphaeridia 218.57 N1 Trachyhystrichosphaera 300.00 N1 Stictosphaeridium 32.50 N1 Kildinella 46.72 N1 Kildinella 55.00 N1 Goniosphaeridium 22.11 N1 Leiosphaeridia 22.50 N1 Goniosphaeridium 25.26 N1 Germinosphaera 27.50 N1 Dictyotidium 31.58 N1 Germinosphaera 33.75 N1 Dictyotidium 38.95 N1 Germinosphaera 42.35 N1 Oculosphaera 52.50 N1 Comasphaeridium 57.82 N1 Germinosphaera 60.00 N1 Oculosphaera 60.00 N1 Germinosphaera 66.67 N1 Germinosphaera 69.44 N1 Germinosphaera 77.65 N1 Oculosphaera 82.50 N1 Trachyhystrichosphaera 91.67 N1 Oculosphaera 92.50 N1 Oculosphaera 95.00 N1 Germinosphaera 105.56 N1 Germinosphaera 119.44 N1 Leiosphaeridia 130.00 N1 Germinosphaera 130.56 N1 Germinosphaera 133.33 N1 Trachyhystrichosphaera 136.11 N1 Trachyhystrichosphaera 155.56 N1

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Leiosphaeridia 160.00 N1 Trachyhystrichosphaera 166.67 N1 Trachyhystrichosphaera 166.67 N1 Trachyhystrichosphaera 187.50 N1 Trachyhystrichosphaera 195.56 N1 Trachyhystrichosphaera 204.17 N1 Trachyhystrichosphaera 216.67 N1 Trachyhystrichosphaera 220.83 N1 Trachyhystrichosphaera 231.11 N1 Trachyhystrichosphaera 266.67 N1 Trachyhystrichosphaera 324.44 N1 Leiosphaeridia 480.00 N1 Cerebrosphaera 507.69 N1 Leiosphaeridia 550.00 N1 Chuaria 753.81 N1 Leiosphaeridia 840.00 N1 Leiosphaeridia 28.33 N1 Cymatiosphaeroides 56.00 N1 Kildinella 35.00 N1 Kildinella 42.00 N1 Kildinella 46.00 N1 Stictosphaeridium 50.00 N1 Kildinella 55.00 N1 Kildinella 57.00 N1 Kildinella 121.67 N1 Chuaria 233.33 N1 Bavlinella 20.41 N1 Synsphaeridium 24.62 N1 Trematosphaeridium 24.90 N1 Protosphaeridium 25.39 N1 Trematosphaeridium 29.30 N1 Pterospermopsimorpha 30.60 N1 Enigmatic 30.61 N1 Protosphaeridium 31.25 N1 Trachysphaeridium 31.25 N1 Pterospermopsimorpha 32.40 N1 Octoedryxium 32.46 N1 Stictosphaeridium 41.71 N1 Pterospermopsimorpha 42.30 N1 Pteinosphaeridium 43.05 N1 Pterospermopsimorpha 44.44 N1 Protosphaeridium 45.14 N1 Trachysphaeridium 45.88 N1 Trachysphaeridium 46.77 N1 Stictosphaeridium 47.26 N1 Trachysphaeridium 47.37 N1 Trachysphaeridium 48.12 N1 Trachysphaeridium 49.62 N1 Kildinella 49.68 N1 Protosphaeridium 51.09 N1

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Octoedryxium 51.19 N1 Pteinosphaeridium 51.22 N1 Pteinosphaeridium 55.56 N1 Trachysphaeridium 55.65 N1 Kildinella 60.72 N1 Favososphaeridium 60.87 N1 Octoedryxium 64.29 N1 Trachysphaeridium 72.62 N1 Protosphaeridium 77.27 N1 Trachysphaeridium 80.60 N1 Favososphaeridium 83.64 N1 Stictosphaeridium 102.50 N1 Chuaria 189.47 N1 Chuaria 870.59 N1 Chuaria 1063.49 N1 Chuaria 1380.00 N1 Protosphaeridium 36.36 N1 Trematosphaeridium 40.00 N1 Trachysphaeridium 40.50 N1 Pterospermopsimorphid 43.50 N1 Kildinella 55.68 N1 Cymatiosphaeroides 68.29 N1 Unnamed 87.80 N1 Kildinella 92.73 N1 Trachysphaeridium 108.00 N1 Chuaria 216.36 N1 Pterospermopsimorphid 225.64 N1 Leiosphaeridia 45.00 N1 Pololeptus 45.00 N1 Leiosphaeridia 45.71 N1 Kildinosphaera 45.92 N1 Pololeptus 50.00 N1 Pololeptus 52.50 N1 Spumosina 55.00 N1 Leiosphaeridia 61.25 N1 Leiosphaeridia 87.27 N1 Leiosphaeridia 88.00 N1 Kildinosphaera 90.00 N1 Pololeptus 93.33 N1 Chuaria 1900.00 N1 Micrhystridium 9.00 N1 Paracrassosphaera 9.47 N1 Skiagia 9.47 N1 Micrhystridium 9.50 N1 Myxococcoides 10.26 N1 Skiagia 10.53 N1 Gloeodiniopsis 10.77 N1 Gloeodiniopsis 11.28 N1 Comasphaeridium 11.58 N1 Skiagia 11.58 N1

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Skiagia 11.58 N1 Paracrassosphaera 12.11 N1 Paracrassosphaera 12.63 N1 Paracrassosphaera 12.63 N1 Paracrassosphaera 13.16 N1 Myxococcoides 13.33 N1 Paracrassosphaera 13.68 N1 Paracrassosphaera 14.74 N1 Dasysphaeridium 15.79 N1 Dasysphaeridium 15.79 N1 Paracrassosphaera 15.79 N1 Skiagia 15.79 N1 Micrhystridium 16.00 N1 Micrhystridium 16.00 N1 Glenobotrydion 16.28 N1 Micrhystridium 16.50 N1 Dasysphaeridium 16.84 N1 Paracrassosphaera 16.84 N1 Micrhystridium 17.00 N1 Paracrassosphaera 17.37 N1 Micrhystridium 18.00 N1 Comasphaeridium 18.95 N1 Micrhystridium 20.00 N1 Leiosphaeridia 20.53 N1 Paracrassosphaera 21.05 N1 Dasysphaeridium 21.54 N1 Octoedryxium 22.00 N1 Dasysphaeridium 22.56 N1 Simia 23.00 N1 Octoedryxium 23.50 N1 Glenobotrydion 24.00 N1 Dasysphaeridium 24.21 N1 Leiosphaeridia 26.32 N1 Leiosphaeridia 26.32 N1 Dasysphaeridium 27.69 N1 Caudosphaera 28.18 N1 Dasysphaeridium 29.47 N1 Octoedryxium 30.00 N1 Octoedryxium 32.00 N1 Dasysphaeridium 32.63 N1 Dasysphaeridium 33.85 N1 Octoedryxium 36.00 N1 Leiosphaeridia 38.52 N1 Dasysphaeridium 40.00 N1 Leiosphaeridia 42.05 N1 Leiosphaeridia 44.21 N1 Caudosphaera 46.40 N1 Leiosphaeridia 53.33 N1 Leiosphaeridia 62.11 N1 Leiosphaeridia 85.85 N1

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Satka 99.24 N1 Satka 100.48 N1 Leiosphaeridia 118.52 N1 Leiosphaeridia 127.18 N1 Satka 146.84 N1 Pterospermopsimorpha 84.21 N1 Leiosphaeridia 113.16 N1 Leiosphaeridia 115.79 N1 Trachyhystrichosphaera 126.32 N1 Gemmuloides 142.86 N1 Gemmuloides 257.14 N1 Chuaria 1221.43 N1 Artacellularia 14.14 N1 Leiosphaeridia 23.00 N1 Pterospermopsimorpha 24.00 N1 Dividing 24.21 N1 Leiosphaeridia 27.93 N1 Octoedryxium 28.89 N1 Stictosphaeridium 30.00 N1 Leiosphaeridia 34.29 N1 Leiosphaeridia 36.19 N1 Cell_under 46.15 N1 Simia 140.91 N1 Aimia 250.00 N1 Trachyhystrichosphaera 265.38 N1 Leiosphaeridia 23.00 N1 Kildinosphaera 24.00 N1 Kildinosphaera 32.00 N1 Kildinosphaera 38.00 N1 Kildinosphaera 41.00 N1 Kildinosphaera 44.00 N1 Kildinosphaera 53.00 N1 Favososphaeridium 105.00 N1 Acanthomorph 68.42 N1 Thin-walled 78.95 N1 Dark-walled 89.47 N1 Acanthomorph 89.47 N1 Germinosphaera 115.79 N1 Trachyhystrichosphaera 147.37 N1 Osculosphaera 147.86 N1 Cymatiosphaeroides 173.57 N1 Polygonal 180.00 N1 Cavate 285.71 N1 Spinose 314.29 N1 Tappania 50.58 M2 Tappania 52.33 M2 Tappania 56.00 M2 Tappania 58.67 M2 Tappania 63.27 M2 Shuiyousphaeridium 141.67 M2

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Shuiyousphaeridium 162.50 M2 Shuiyousphaeridium 163.33 M2 Shuiyousphaeridium 165.00 M2 Shuiyousphaeridium 166.67 M2 Shuiyousphaeridium 171.67 M2 Majasphaeridium 200.00 M2 Membrane 266.67 M2 Pterospermopsimorpha 425.00 M2 Spumosina 15.00 M2 Leiosphaeridia 19.17 M2 Spumosina 23.33 M2 Symplassosphaeridium 26.67 M2 Pterospermopsimorpha 35.00 M2 Synsphaeridium 35.83 M2 Leiosphaeridia 39.17 M2 Synsphaeridium 39.17 M2 Synsphaeridium 40.00 M2 Leiosphaeridia 41.67 M2 Leiosphaeridia 41.67 M2 Eomicrocystis 41.67 M2 Leiosphaeridia 43.33 M2 Leiosphaeridia 45.00 M2 Leiosphaeridia 45.00 M2 Leiosphaeridia 46.67 M2 Leiosphaeridia 53.33 M2 Ostiana 61.67 M2 Synsphaeridium 64.17 M2 Synsphaeridium 76.67 M2 Leiosphaeridia 78.33 M2 Ostiana 83.33 M2 Eomicrocystis 94.17 M2 Leiosphaeridia 98.33 M2 Leiosphaeridia 193.33 M2 Leiosphaeridia 8.00 M2 Leiosphaeridia 8.00 M2 Leiosphaeridia 28.00 M2 Leiosphaeridia 42.00 M2 Leiosphaeridia 46.00 M2 Leiosphaeridia 46.00 M2 Leiosphaeridia 50.00 M2 Leiosphaeridia 50.00 M2 Leiosphaeridia 50.00 M2 Leiosphaeridia 54.00 M2 Leiosphaeridia 54.00 M2 Leiosphaeridia 58.00 M2 Valeria 59.20 M2 Leiosphaeridia 60.00 M2 Leiosphaeridia 64.00 M2 Leiosphaeridia 66.00 M2 Valeria 78.40 M2

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Leiosphaeridia 82.00 M2 Leiosphaeridia 92.00 M2 Leiosphaeridia 106.00 M2 Leiosphaeridia 376.92 M2 Leiosphaeridia 24.24 M1 Leiosphaeridia 31.52 M1 Pterospermopsimorpha 31.52 M1 Satka 68.18 M1 Leiosphaeridia 53.85 P1 Leiosphaeridia 56.92 P1 Leiosphaeridia 42.22 P1 Kildinella 86.67 P1 Chuaria 110.00 P1

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Appendix 6. Acritarch morphology data. Characters defined in Fig. 4.5.

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Trends in Eukaryote Body Size in an Ecological and ...€¦ · This volume examines body size of eukaryotes and its correlates in various temporal and spatial contexts in three distinct