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Measuring Recurrence of Marine Biotic Gradients: A Case

Study from the Pennsylvanian-Permian Midcontinent
Department of Geological Sciences, Indiana University, Bloomington, IN 47405

Department of Geosciences, The Pennsylvania State University, University Park, PA 16802

PALAIOS, 2001, V. 16, p. 444–460 represented by the modern world. In contrast, although
there are limitations imposed by taphonomy and strati-
The aim of this study was to determine whether biotic as- graphic resolution (Kidwell and Flessa, 1995; Martin,
sociations of Pennsylvanian-Permian brachiopods and bi- 1999 and references therein), paleoecologists can examine
valves from the northern Midcontinent differ in their degree the fossil record of biological communities through time.
of recurrence through time. The study interval includes 2.5 The aim of this paper is to identify and characterize the
Myr that can be divided into 5 full and 2 partial composite consistency of species associations through time using
depositional sequences separated by subaerial unconformi- Pennsylvanian-Permian bivalves and brachiopods of the
ties. These stratigraphic packages represent replicate natu- North American Midcontinent as a case study.
ral experiments in establishing the benthic marine ecosys- Recent paleoecological studies of marine invertebrates
tem of the basin. Based on cluster and ordination analyses, (e.g., Brett and Baird, 1995; Westrop, 1996; Tang and Bo-
two discrete biofacies can be recognized—one dominated by ttjer, 1996; Patzkowsky and Holland, 1997; Olszewski and
brachiopods and the other by bivalves. Within each of these, Patzkowsky, in press) have focused on compositional
environmental gradients can be recognized. The brachio- change at the scale of entire basins, combining taxonomic
pod gradient is interpreted to reflect the degree of water-col- lists from a variety of environments. In this study, the fo-
umn oxygenation, whereas the bivalve gradient is interpret- cus is on changes within biofacies rather than the entire
ed to reflect the transition from restricted to open-marine basin. Cluster analysis has been used to define paleocom-
conditions. Comparison of measured recurrence with ran- munity types, gradient analysis to examine inter-specific
domized data indicates that the ecological segregation of associations within paleocommunity types, and recur-
the two biofacies is maintained to a significant degree rence analysis to test for changes in associations through
through the succession of depositional sequences in the time. In order to put the results in a broader context, they
study interval. In contrast, the gradients within each bio- are compared with those of other recent studies covering
facies, although recognizable, are not maintained rigidly different groups, environments, and ages (Bennington
from sequence to sequence. There is also no significant dif- and Bambach, 1996; Holterhoff, 1996; Pandolfi, 1996).
ference in gradient recurrence between the two biofacies.
These results imply that there is no need to call upon strong STRATIGRAPHIC FRAMEWORK
interspecific interactions to maintain the structure of these
paleocommunities through time. This study focuses on a 2.5-Myr interval of late Pennsyl-
vanian to early Permian rocks (Fig. 1) of the northern Mid-
continent (Fig. 2). At this time of global ‘‘icehouse’’ climatic
INTRODUCTION conditions (Fischer, 1984), an ice sheet was present at the
south pole (Ziegler et al., 1997), leading to cyclical eustatic
A question of long-standing interest to ecologists and and climatic changes analogous in frequency, amplitude,
paleoecologists concerns the degree of integration in bio- and effect to those of the Quaternary (Veevers and Powell,
logical communities (Jackson, 1994). This issue frequently 1987). These are reflected in the cyclothemic stratigraphy
is cast as a debate between advocates of strong interde- of Pennsylvanian-Permian rocks in the Midcontinent
pendence of species (Clements, 1916) and strong indepen- (Heckel, 1984, 1986, 1995).
dence of species (Gleason, 1926). Ecologists have tested Cyclicity occurs at two scales in the study interval. At
these alternative hypotheses by examining how species the finest resolution, meter-scale cycles occur in both
compositions change along environmental gradients open-marine, platform settings and nearshore, coastal set-
(Whittaker, 1967). In a Clementsian world, species com- tings (Miller and West, 1993; Miller et al., 1996; Olszew-
position and abundance are expected to be very consistent ski, 2000). These cycles are very thin (1 to 5 m), unconfor-
over a range of environmental conditions because the spe- mity-bounded depositional sequences and, therefore, rep-
cies that make up a community form an integrated entity resent temporally significant packets of rock (Posamentier
(Ricklefs, 1990). In a Gleasonian world, species composi- et al., 1988; Van Wagoner et al., 1988) averaging 50,000
tion and abundance should vary from site to site as condi- years or less in duration.
tions change because every species reacts to environmen- At a larger scale (that of the classical cyclothems), com-
tal change independently (Ricklefs, 1990). Ecologists gen- posite depositional sequences, composed of 8 to 13 meter-
erally study species associations in the single time slice scale cycles, can be recognized (Miller and West, 1993,
Copyright Q 2001, SEPM (Society for Sedimentary Geology) 0883-1351/01/0016-0444/$3.00

FIGURE 2—Study area. Shaded area indicates exposure of upper

Pennsylvanian through lower Permian rocks used in this study. North-
south geographic zones are also indicated (see Table 2).

ments on the platform. Each composite sequence, there-

fore, can be treated as a replicate natural experiment in
setting up a benthic marine ecosystem that provides a
means of measuring the recurrence of ecological associa-

Data consist of fossil bivalve and articulate brachiopod
collections (plus the calcareous inarticulate genus Petro-
crania) from two sources: 341 collections from Mudge and
Yochelson’s (1962) monograph on the stratigraphy and pa-
leontology of the Pennsylvanian-Permian Midcontinent
and 132 additional collections made in 1997 through 1999
(‘‘new collections’’). Each collection represents the assem-
blage of fossils found in a bed at a site; they were not com-
bined to create composite lists by geologic unit or location.
The entire data set is included in Olszewski (2000) and
can be accessed at the Pennsylvania State University’s
Electronic Theses and Dissertations website (http://
FIGURE 1—Stratigraphic study interval. Stratigraphic column modified All fossils were identified to as fine a taxonomic level as
from Zeller (1968) and Baars et al. (1994). Roman numerals denote possible. Although many specimens were identifiable to
composite depositional sequences. I through V are complete sequenc- species, a large proportion could only be determined to ge-
es. 0 and VI are partial sequences.
nus. Therefore, to make use of as much data as possible,
all statistical analyses were conducted at the genus level.
This choice did not have a strong influence on patterns of
1998; Olszewski, 2000). Open-marine carbonates, marine ecological association for two reasons. First, most genera
mudrocks, and condensed sections dominate their trans- in the study interval are monospecific. Second, most poly-
gressive and early highstand phases. Late highstand de- specific genera in the data set are dominated by one spe-
posits include peritidal carbonates, deltaic sandstones, cies. For example, in Mudge and Yochelson’s (1962) data,
and pedogenic mudrocks. Correlation of meter-scale cycles Neospirifer is reported 116 times: 38 as N. sp. indet., 7 as
reveals angular unconformities at the boundaries of com- N. cf. N. kansasensis, and 71 as N. dunbari. If the propor-
posite sequences (Olszewski, 2000), indicating that these tion of 7 to 71 is representative of the relative frequency of
too are temporally significant packages of rock. these two species, then only 11 of the 116 Neospirifer oc-
The 51 meter-scale cycles identified in the study inter- currences are expected to be N. cf. N. kansasensis. These
val (Olszewski, 2000) provide a means of examining figures, which are typical of other genera as well, indicate
trends in paleoecological communities at relatively high that the number of associations gained by using genera
temporal resolution (;5·104 year). The five complete and rather than species provides more information (in a statis-
two partial composite sequences (Fig. 1) are separated by tical sense) than including many rare species and reject-
extensive subaerial unconformities. This means that their ing specimens not identified to the species level.
deposition required re-establishment of marine environ- Because the interest of this study was in associations of

TABLE 1—Descriptive statistics of data subsets. S is the richness of collections included in each data subset. ‘‘New collections’’ are those
made for this study and added to those of Mudge and Yochelson (1962). ‘‘All collections’’ denotes Mudge and Yochelson (1962) collections
plus ‘‘new collections.’’ ‘‘All genera’’ indicates inclusion of both brachiopod and bivalve genera (as opposed to just one group or the other). An
occurrence denotes the presence of a taxon in a collection regardless of its abundance. In a presence–absence data matrix, where 1 indicates
presence and 0 indicates absence, the total number of occurrences is simply the sum of the matrix (i.e., the number of 1’s).

Data subset Taxa Collections Occurrences Specimens

All collections All genera, S $ 2 40 474 2,593 18,737

All genera, S $ 4 35 317 2,191 16,122
Brachiopods, S $ 2 23 382 2,080 16,317
Bivalves, S $ 2 16 128 367 1,745
Bivalves, S $ 3 12 60 225 927
New collections All genera, S $ 2 34 132 865 7,687
All genera, by sequence, I 31 157 844 4,902
S$2 II 27 61 314 2,002
III 31 147 925 6,209
IV 23 29 167 1,727
V 26 82 319 1,764
Brachiopods, by sequence, I 20 119 634 3,866
S$2 II 16 41 199 1,452
III 20 140 851 6,043
IV 17 25 143 1,628
V 16 49 187 977
Bivalves, by sequence, I 11 49 149 702
S$2 II 11 27 91 497
III 9 18 42 116
IV 4 5 12 53
V 10 39 109 646

two or more taxa, collections including only one taxon equal to 5 and median number of specimens equal to 21
were not included in statistical analyses. The final data (Fig. 3). Although their small sizes suggest that many tax-
set of 474 collections includes a total of 18,737 specimens onomic lists may not be complete, the large number of col-
and 2,593 occurrences (Table 1). lections reduces statistical uncertainty.
The geographic and stratigraphic distribution of collec- Collections were taken from a wide variety of lithologies
tions is summarized in Table 2 for seven north-south geo- and taphonomic states. Some collections came from hard
graphic zones (Fig. 2) of about 48 km each (five townships limestone, from which specimens had to be removed with
or about 30 miles) and the five complete composite se- chisel and hammer or examined on slab surfaces, whereas
quences. Four hundred and twenty-four collections are in- others came from soft mudrocks, which could be easily
cluded in the table, leaving 50 unassigned. Seven of these bulk sampled or surface collected. Some fossils occurred as
came from Nebraska, thirty-eight came from the two par- original shell material while others were molds (some-
tial composite sequences (marked 0 and VI in Fig. 1), and times in the same collection). In addition, collections most
five came from stratigraphically floating exposures. These certainly represent different amounts of time-averaging
collections were included in ordination and cluster analy- (Kidwell and Bosence, 1991; Brett, 1995); some come from
ses despite uncertain external information because they condensed intervals within meter-scale cycles represent-
still shed light on taxonomic associations. Although con- ing 100’s to 1000’s of years, whereas others come from fa-
tingency table analysis indicates that collections are not cies that represent relatively rapid burial.
distributed randomly (Gadj(df 5 24) 5 54.45, P 5 0.00037; So- Although all these non-uniform factors increase vari-
kal and Rohlf, 1995), no stratigraphic or geographic trends ability, the collections are reliable as records of fossil taxa
are evident in Table 2. that demonstrably co-occur in specific beds at specific lo-
Most of the collections are small with median richness cations. As such, they provide a great deal of information

TABLE 2—Distribution of collections used in this study by geographic zone and composite sequence. Values are ‘‘all collections’’ with S $ 2
(Table 1). Numbers in parentheses are ‘‘new collections’’, S $ 2. The distributions of Mudge and Yochelson’s (1962) collections and ‘‘new
collections’’ are significantly correlated (r 5 0.738 . r950.05 5 0.334; df 5 33).

Geographic zones
Composite sequences 1 2 3 4 5 6 7 Row totals

V 4 (0) 31 (14) 16 (6) 15 (3) 4 (0) 8 (0) 14 (0) 92 (23)

IV 2 (1) 9 (6) 3 (0) 3 (1) 7 (6) 1 (0) 5 (1) 30 (15)
III 10 (0) 73 (33) 25 (12) 3 (0) 8 (1) 16 (9) 12 (1) 147 (56)
II 3 (0) 21 (7) 16 (2) 7 (0) 3 (0) 6 (0) 5 (2) 61 (11)
I 12 (1) 31 (6) 18 (2) 5 (0) 14 (0) 10 (0) 4 (1) 94 (10)
Column totals 31 (2) 165 (66) 78 (22) 33 (4) 36 (7) 41 (9) 40 (5) 424 (115)

the small number of specimens in many collections means

that relative and rank abundances are poorly constrained.
Third, different collecting methods bias samples in differ-
ent ways. For example, large bulk collections yield reliable
abundance data (Bennington and Rutherford, 1999), but
surface collecting often results in samples with elevated
diversity relative to the number of specimens because the
aim in the field was to maximize the number of different
taxa. Finally, presence/absence data are less sensitive to
differences between collections and are, therefore, more
likely to indicate a higher level of similarity between any
two collections than absolute abundances or abundance
rankings (Rahel, 1990). As it turns out, this bias is in op-
position to our findings and strengthens the interpreta-
tion presented below. This is not to say that relative abun-
dance data are inappropriate for paleoecological studies.
In many cases, where sampling procedures are strictly
controlled and taphonomy and lithology are more uniform
than this study, relative abundances can reveal patterns
of ecological or taphonomic significance that are obscured
by presence/absence data (Olszewski and West, 1997).


Data were analyzed using a variety of techniques, each
with a different purpose. Exploratory approaches included
cluster analysis (R-mode, Q-mode, and two-way) and or-
dination (correspondence analysis). To test for changes in
paleoecological associations through time, randomization
and resampling approaches were applied (Crowley, 1992),
here dubbed ‘‘recurrence analysis.’’
External information for collections included geograph-
ic location, stratigraphic position, and lithology. External
information for genera included membership in higher
taxonomic groups.
In some cases, collections below a specified richness or
taxa below a specified rarity were discarded (subsets listed
FIGURE 3—Relationship between number of specimens and number
of taxa (Richness, S). Plots describe data including all genera (bi- in Table 1). This is because outliers, consisting of a few
valves and brachiopods) and all collections with S $ 2. The majority small collections or rare taxa, often obscure broader pat-
of collections include fewer than 40 specimens. (A) Number of collec- terns when using exploratory statistical techniques. Anal-
tions with a given total abundance (number of specimens). (B) Num- yses were initially performed using all data but were
ber of collections with a given richness. (C) Cross-plot of total abun- pared down to see if interpretable patterns became more
dance versus richness. Each cross represents a collection. clear; the results included here were selected for the pat-
terns they show and presentability. The characteristics of
the data used in each analysis are described in the figure
with regard to paleoecological associations. This is not to captions.
say that fossil co-occurrence proves co-occurrence during
life, which is rarely demonstrable in the rock record. How- Cluster Analysis
ever, a long history of actualistic live-dead comparisons of
shelly, marine macrofauna indicates that death assem- Clustering was conducted using the hierarchical, un-
blages, and ultimately fossil assemblages, faithfully re- weighted pair group method with arithmetic averaging
cord compositional differences between different environ- (UPGMA). The aim was to examine how collections and
ments (Kidwell and Bosence, 1991; Martin, 1999). taxa group together and whether a clear classification
All analyses presented here were performed using pres- emerges from the data. The similarity metric used was the
ence/absence data rather than abundance data for several Dice coefficient:
reasons. First, actualistic studies and numerical models
SD 5 2c/(Ni 1 Nj) (1),
indicate that, although relative abundance data in death
assemblages do reflect living abundances to some degree c 5 number of taxonomic co-occurrences between collec-
(Kidwell and Flessa, 1995), they also experience modifica- tions i and j, Ni, Nj 5 total number of occurrences in i and
tion due to differences in taphonomic susceptibility among j, respectively. This definition is in the context of Q-mode
taxa and environments (Cummins et al., 1986; Staff et al., analysis (clustering of collections), but the coefficient also
1986; Staff and Powell, 1988; Powell et al., 1989; Miller can be used for R-mode analysis (clustering of taxa). Note
and Cummins, 1990; Olszewski and West, 1997). Second, that other names for the same metric are the Sorenson

and Czekanowski coefficients and that equation (1) is the

binary reduction of the ‘‘percentage similarity’’ and ‘‘Bray-
Curtis measure’’ (Sepkoski, 1974). The Dice coefficient
was chosen for several reasons. First, in its fully numerical
form, this metric has been found to reflect ecological differ-
ences very effectively (Faith et al., 1987). Second, it cor-
rects for sparseness in the data matrix, thereby decreasing
the influence of rare taxa and low-diversity collections in
the overall result (Archer and Maples, 1989). Third, like
the related Jaccard coefficient (S D 5 2Sj/(Sj11), Sj 5 Jac-
card coefficient), it does not count mutual absences, which
can severely skew results using sparse paleoecological
data matrices (Maples and Archer, 1988). Unlike the Jac-
card coefficient, however, the Dice has a wider and more
symmetrical spread of expected values in randomized
tests (Archer and Maples, 1987).
R-mode analysis of brachiopods and bivalves together
(Fig. 4), using only collections with a taxonomic richness of
4 or more, reveals three major groupings—a brachiopod
cluster, a bivalve cluster, and a group of rare taxa. Both
major clusters have a ‘‘chain’’ topology, suggesting that
taxa were added one by one to a single, growing cluster
rather than being segregated into subgroups and then ag-
glomerated. The rare taxa are grouped at very low levels of
similarity, indicating that they do not form a cluster based
on strong association. Within the brachiopods, Crurithyr-
is, Hystriculina, and Lissochonetes form a subcluster.
These are all small taxa typically found in dark gray to
black, pyritic mudrocks containing high organic carbon.
Collections are usually numerically dominated by one spe-
cies. These characteristics indicate a physiologically
stressful environment due to low oxygen concentrations in
the water column (Boardman et al., 1984; Kammer et al.,
Q-mode and two-way cluster analyses of the same data
used to generate figure 4 yield very large dendrograms
that could not be shown in a single journal figure; hence,
the subset of the data collected as part of this study (‘‘new
collections’’) is presented instead (Fig. 5). Comparison
with analyses of the entire data set, which can be found in
Olszewski (2000), have a similar geographic and strati-
FIGURE 4—R-mode cluster analysis of all genera using collections
graphic distribution (Table 2), and show the same basic
with S $ 4. Clusters are labeled by their dominant taxa: brachiopods,
patterns as described here. bivalves, and rare taxa. Numbers in parentheses are genus identifi-
The Q-mode analysis of collections (Fig. 5) reveals a cation numbers provided for comparison with other figures (see Fig.
large number of clusters. Some, but not all, show strong 7 for key). ‘B’ and ‘C’ signify brachiopod and bivalve, respectively.
associations with lithology. For example, H has a high pro- Other numbers represent the total number of occurrences of each
portion of carbonate collections, and D is entirely siliciclas- genus in this data set. Note the low number of occurrences in the
group of rare taxa and that degree of association within the other
tic. In addition, there is some correspondence between
clusters correlates to rarity. Apparent ‘‘polytomies’’ are an artifact of
clusters and collections from particular composite se- the software used (SPSS) and do not represent unresolved associa-
quences. For example, all the collections from composite tions.
sequence VI are included in cluster A, many collections
from sequence IV occur in D, and many collections from
sequence V are seen in G, H, and I. ly, this is interpreted to reflect an environmental gradient
The two-way cluster analysis (Fig. 5) relates taxonomic from well-to-poorly oxygenated conditions (Boardman et
content to collection clusters. Q-mode clusters G, H, and I al., 1984), although taxa from both ends of the gradient
clearly segregate from the other clusters because they are also can be found together. Note that although bivalves
dominated by bivalves rather than brachiopods. The clus- and brachiopods are clearly segregated, they are not mu-
ters of rare taxa are easily revealed as such. Within the tually exclusive—there are collections in almost all of the
low-diversity brachiopod clusters, a trend can be seen clusters that include representatives of both major taxa.
starting at the Derbyia-Neochonetes-Composita (taxa 9, 23, The last cluster analysis to be presented here includes
and 7) R-mode subcluster and migrating to the previously only bivalves (Fig. 6). The aim was to see if there were any
described dysoxic subcluster (Crurithyris-Hystriculina- patterns within this group that were being swamped by
Lissochonetes; taxa 8, 14, and19). As mentioned previous- including them with the more numerous brachiopod-dom-

inated collections. In the R-mode, taxa associate in much

the same way as before, and rare taxa are still excluded.
However, the two-way analysis suggests a possible gradi-
ent from Septimyalina (taxon 36) and Schizodus (taxon
35) to Edmondia (taxon 11) and Myalina (Orthomyalina)
(taxon 21).

Ordination Analysis
As a complement to cluster analysis, the data were or-
dinated using correspondence analysis. Ordination helps
to reveal gradients that can be broken up artificially by
clustering, and orders taxa and collections less arbitrarily
than they are depicted by a dendrogram. In addition, or-
dination expresses multidimensional relationships more
effectively than cluster analysis.
Correspondence analysis was chosen for two reasons.
First, Kenkel and Orlóci (1986) found it to be very effective
at extracting known patterns in artificial ecological data
compared to other ordination techniques. Second, corre-
spondence analysis ordinates both taxa and collections in
the same multivariate space (i.e., both R- and Q-mode
analyses are conducted simultaneously), which allows the
two to be directly related (Jongmann et al., 1995).
A disadvantage of correspondence analysis is that it can
produce an ‘‘arch’’ effect. This is the result of compression
at the ends of ordination axes and a systematic, often qua-
dratic, relationship between axes. These problems can be
corrected by non-linear rescaling (Hill and Gauch, 1980),
but we chose not to do so for several reasons. First, non-
linear detrending is a ‘‘brute force’’ re-adjustment of the
pattern that often can lead to loss of ecologically meaning-
ful information (Pielou, 1984). If patterns are readily in-
terpretable, as is the case in the present analyses, there is
no need for adjustment. Second, Minchin (1987) and Ken-
kel and Orlóci (1986) found that non-linear detrending of-
ten does not improve simulated patterns and can even ex-
acerbate distortion of the ordination space. Ter Braak
(1995) provides a more comprehensive discussion of these
issues, including their mathematical basis and recom-
mended solutions.
Analyzing both brachiopods and bivalves together (Fig.
7A) reveals that they are segregated strongly in ordina-
tion space. Almost all brachiopod genera have positive val-
ues, while the bivalves are negative without exception.
Demarcating the R-mode clusters of genera from figure 4
on the ordination shows that results of the two analyses
are quite consistent. Note that, although the cluster
marked ‘‘Rare Taxa’’ appears to sit within the brachiopod
cluster, it is separated in higher ordination dimensions
where it is pulled out of the plane defined by the ‘‘Bivalve
Dominated’’ and ‘‘Brachiopod Dominated’’ clusters. The
slight overlap of bivalve and brachiopod genera involves
the bivalves Wilkingia (taxon 40) and Pteronites (taxon 3),
and the brachiopod Juresania (taxon 16) (the other taxa in
the region of overlap are rare and, therefore, their posi-
tions in ordination space are constrained poorly and pro-
vide limited information on their relationships). This is
consistent with direct observations in the field, where
Wilkingia and Pteronites are often the only bivalves in a
collection otherwise dominated by brachiopods and other
FIGURE 5—Two-way cluster analysis of ‘‘new collections’’ with S $
2 (key to genera as in Fig. 7); B 5 brachiopod, C 5 bivalve. External open-marine groups, and where Juresania seems to be
data for collections includes composite sequence (Roman numerals) characteristic of nearshore environments otherwise domi-
and lithology (s 5 siliciclastic, c 5 carbonate).

FIGURE 7—Correspondence analyses of genera. (A) All genera (bi-

valves circled), all collections with S $ 4. Outlined regions are R-mode
clusters from figure 4. Note the gap (indicated) between brachiopod-
and bivalve-dominated biofacies. (B) Brachiopod genera, collections
with S $ 2. (C) Bivalve genera, collections with S $ 3. Percent of
total inertia is shown for each axis. Units are mean standard devia-
tions. 1 5 Anthraconeilopsis, 2 5 Aviculopecten, 3 5 Pteronites, 4 5
Beecheria, 5 5 Cancrinella, 6 5 Clavicosta, 7 5 Composita, 8 5
Crurithyris, 9 5 Derbyia, 10 5 Echinaria, 11 5 Edmondia, 12 5 En-
teletes, 13 5 Hustedia, 14 5 Hystriculina, 15 5 Isogramma, 16 5
Juresania, 17 5 Leptalosia, 18 5 Linoproductus, 19 5 Lissochonetes,
20 5 Meekella, 21 5 Myalina (Orthomyalina), 22 5 Myalina (Myali-
nella), 23 5 Neochonetes, 24 5 Neospirifer, 25 5 Paleyoldia, 26 5
Permophorus, 27 5 Petrocrania, 28 5 Promytilus, 29 5 Pseudomon-
otis, 30 5 Pteria, 31 5 Punctospirifer, 32 5 Retaria, 33 5 Reticulatia,
34 5 Rhipidomella, 35 5 Schizodus, 36 5 Septimyalina, 37 5 Strob-
FIGURE 6—Two-way cluster analysis of bivalve genera and collec- lochondria, 38 5 Volsellina, 39 5 Wellerella, 40 5 Wilkingia.
tions with S $ 2 (key to genera as in Fig. 7). External data for collec-
tions includes composite sequence (Roman numerals) and lithology
(s 5 siliciclastic, c 5 carbonate).

nated by mollusks. The wide gap between most of the bi-

valves and the brachiopods (marked in Fig. 7A) suggests a
strong discontinuity between the two main compositional
groups. The first axis not only separates brachiopods from
bivalves, it also strings the bivalves into a compositional
gradient. Axis 2 extracts a gradient in the brachiopods
perpendicular to the bivalve gradient of axis 1. This or-
thogonal relationship suggests that the gradients within
the two groups are largely independent of one another.
Ordinating the two main taxonomic groups further re-
fines the patterns seen in the large ordination. In the bra-
chiopods (Fig. 7B), the first axis, which is very consistent
with the second axis of figure 7A, segregates Rhipidomella
(34), Crurithyris (8), Wellerella (39), Lissochonetes (19),
Hustedia (13), and Hystriculina (14) from the rest. As de-
scribed above in the cluster analyses, these genera are all
relatively small (,1.5 cm across) and often very abundant
in facies interpreted as dysoxic deposits. The opposite end
of the gradient is dominated primarily by Juresania (16)
and some rare taxa (e.g., Echinaria [10], Cancrinella [5],
Meekella [20]). The second axis further pulls out these rar-
ities but is otherwise uninterpretable.
In the bivalve ordination (Fig. 7C), the gradient along
the first axis separates Pteronites (3), Wilkingia (40), and
Schizodus (35) at the negative extreme, and Edmondia
(11), Pseudomonotis (29), and Myalina (Orthomyalina)
(21) at the other. Although not identical, this is consistent
with the faunal gradient from open-marine to relatively
restricted coastal or lagoonal environments interpreted in
the cluster analyses.
Because correspondence analysis performs both R-mode
and Q-mode analyses simultaneously (Figs. 7 and 8), it is
possible to examine patterns of other important variables
in the same ordination space, thereby directly relating
taxa to environment and time. An important difference be-
tween figures 7A and 8A (R and Q-modes of the same or-
dination space) is the lack of two distinct clumps in the
scatter of collections (Fig. 8A). This suggests that the seg-
regation of brachiopods and bivalves is not an artifact re-
sulting from uneven sampling at the ends of a continuous
gradient—i.e., the correspondence analysis shows the po-
sition of the intermediate collections. Also investigated
was the relationship of taxa to lithology. Comparison of
figures 7A and 8A indicates that both bivalves and bra-
chiopods can be found in either siliciclastic or carbonate
rocks. The contrast between these two main lithologies is
one of the most prominent in the study interval, yet these FIGURE 8—Correspondence analysis of collections. Solid circles 5
analyses suggest that it does not restrict the distribution carbonates; empty circles 5 siliciclastics; two-tone circles 5 mix of
of the two main taxonomic groups. Rather, Olszewski carbonates and siliciclastics. Large circles represent means for the
(2000) recognized complete paralic to open marine gradi- two lithologies and brackets indicate one standard deviation on each
ents based on lithology in both siliciclastic and carbonate side. These are the same ordination spaces as shown in figure 7. (A)
facies, suggesting that the benthic organisms analyzed All genera, collections with S $ 4. (B) Brachiopod genera, S $ 2. (C)
Bivalve genera, S $ 3. Percentages of total inertia are shown for each
here were more sensitive to the onshore-offshore gradient axis. Units are mean standard deviations.
(a gradient-complex reflecting water depth, environmen-
tal energy, sediment grain size, storm frequency, salinity,
etc.) than the mineral composition of the substrate. Previ- val. Using all taxa (Fig. 9), the average value of each cycle
ous work by Miller (1988, 1989) has found that by the late shifts from nearshore, bivalve-dominated assemblages at
Paleozoic, North American bivalves do not seem to favor the base of each composite sequence to open marine, bra-
terrigenous over carbonate environments, as they seem to chiopod-dominated assemblages through the middle of
have earlier in the Paleozoic. each composite sequence.
To investigate change in communities through time, the The same approach using only brachiopods (Fig. 10)
first axis correspondence-analysis values of collections shows an overall trend through the entire study interval
were plotted against meter-scale cycles in the study inter- from well-oxygenated to poorly-oxygenated assemblages

except for a brief reversal in the lower part of composite se-

quence V. Composite sequences I and II are dominated by
well-oxygenated faunas, sequence III has equal numbers
of low and high oxygen collections, whereas sequences IV
and V are dominated by low oxygen faunas (despite the
switchback in composite sequence V, it also contains many
of the most dysoxic brachiopod assemblages). Note that
dysoxic collections do not increase at the expense of well-
oxygenated collections; rather, increasingly low-oxygen
points are added to a continuous succession of high oxygen
points. Cycle 51 represents a return to well-oxygenated
conditions, which is consistent with findings based on co-
nodonts (Boardman et al., 1995).
Lastly, with respect to paleocommunity recurrence, it is
of interest to compare the faunal gradients of each com-
posite sequence separately (Fig. 11). As mentioned earlier,
each composite sequence represents, in effect, a naturally
replicated experiment in repopulating the Midcontinent
platform after subaerial exposure. In the brachiopod plots,
dysoxic taxa (Rhipidomella [34], Wellerella [39], Crurithyr-
is [8], Hystriculina [14], Lissochonetes [19]) and nearshore
taxa (Juresania [16], Linoproductus [18]) are indicated. In
all sequences, the dysoxic group and the nearshore group
form distinct patches in the ordination space, but they do
not always fall at the ends of the ordination-defined gra-
The inferred end-members of the bivalve gradient also
are indicated—Wilkingia (40), Pteronites (3), and Schizo-
dus (35) at the open-marine end, and Edmondia (11), Per-
mophorus (26), Pseudomonotis (29), and Promytilus (28) at
the restricted end (Fig. 11). The bivalve collections are far
less numerous than the brachiopod collections; hence,
their plots are less well constrained in terms of faunal re-
lationships. For example, sequence IV, although it shows
the gradient nicely, is based on only five collections (Table
1). Sequences I and III show the two patches segregated,
but sequences II and V show them overlapping. Exploring
higher axes failed to improve the pattern. Also noteworthy
is the distribution of taxa within these groups, which is not
consistent from sequence to sequence. This suggests that
genera in this data set are not tightly restricted to partic-
ular associations. The statistical significance of this sug-
gestion is tested using recurrence analysis.

Recurrence Analysis
In addition to exploratory methods, tests were also con-
ducted for stratigraphic recurrence of paleoecologic asso-
ciations using methods similar to those described by
Clarke and Warwick (1994; see also Ivany and Baumiller,
1998). Taxonomic associations in a set of fossil collections
can be described completely by an R-mode matrix of simi-
larity coefficients between every pair of taxa. Such a ma-

FIGURE 9—First axis correspondence analysis values for all collec-
tions (all genera, S $ 4) plotted against stratigraphic position. Crosses
represent individual collections, dots represent mean values for each
meter-scale cycle. Composite sequence boundaries are shown by dot-
ted lines. Gray stripe shows interpreted general trend of stronger bi-
valve influence at the base of each composite sequence followed by
increased brachiopod dominance upward.

FIGURE 11—Correspondence analyses of brachiopod and bivalve

genera by composite sequence (key to genera as in Fig. 7). Percent
of total inertia is shown for each axis. Units are mean standard devi-
ations. Outlined patches represent inferred gradient end-members
(see text for discussion).

FIGURE 10—First-axis correspondence-analysis values for all collec-
tions (brachiopod genera, S $ 2) plotted against stratigraphic position.
Crosses represent individual collections, dots represent mean values
for each meter-scale cycle. Composite sequence boundaries are
shown by dotted lines. Gray stripe shows interpreted general trend of
increasingly dysoxic faunal signatures through study interval.

trix was built using the Dice coefficient and all the collec-
tions (S$2) from each composite sequence. These are the
same data that were ordinated for each sequence (Fig. 11),
so they can be generally compared with the results of the
exploratory techniques. Such comparisons should not be
taken too literally because correspondence analysis, al-
though it is an effective means of visualizing complex pa-
leoecological patterns, does not make use of the Dice coef-
ficient. Recurrence of faunal associations was measured
by comparing the Dice coefficient matrices for each pair of
composite sequences using Spearman’s rank correlation
coefficient (r). Note that only taxa occurring in both se-
quences can be included using this approach.
The recurrence coefficients obtained in this manner can
be tested for significance, which measures whether the r
based on real data is significantly greater than if taxa
were distributed randomly among collections. Standard
significance tables for Spearman’s rank correlation coeffi-
cient are not valid in this case for two reasons. First, they
assume a null hypothesis of r 5 0, but non-random struc-
ture (i.e., r.0) can occur in similarity matrices (i.e., the R-
mode Dice matrices used here) due to differences in the
number of occurrences of different taxa, regardless of
whether there are any ecological associations. Second, un-
derlying distributions are not normal (Clarke and War-
wick, 1994). To deal with these issues, a randomization
approach was adopted (Crowley, 1992). The occurrences of
each taxon were randomized among all the collections for
each of two composite sequences. By doing so, the number
of occurrences of each genus did not change, just the dis-
tribution of co-occurrences between genera. Occurrences
were shuffled randomly within taxa until all collections
had at least one occurrence. Note that this loosens the re-
striction of at least two occurrences per collection in the
original data matrices and makes the test conservative in
recognizing recurrence by widening the calculated signifi-
cance values. After both data matrices intended for com-
parison were randomized, their similarity matrices and
correlation coefficient were calculated in the same manner
as the original data. This was performed 1000 times to
build a distribution of correlation coefficients, the top and
bottom 2.5% of which were used to determine the 95% sig-
nificance values. If the correlation coefficient from the real
data lies outside this range, the statistical null hypothesis
(i.e., that the degree of similarity between taxonomic as-
sociations in the two sequences being tested would be pos-
sible with just random associations of taxa) can be reject-
ed. In other words, if the recurrence coefficient lies outside
the 95% range, it is reasonably certain that there is a non-
random degree of recurrence of taxonomic associations be-
FIGURE 12—Randomized recurrence significance. Triangles,
tween sequences. squares, and circles indicate measured Spearman Rank Correlation
According to the randomization results (Fig. 12), the de- Coefficient using all genera (A), brachiopods (B), and bivalves (C),
gree of faunal association using all taxa (brachiopods and respectively. I-bars indicate 95% two-sided confidence intervals based
bivalves) is significantly recurrent (except for sequence I on randomized data. Roman numerals indicate composite sequences
versus IV). In contrast, the gradients within each group (Fig. 1). If the measured value falls outside the confidence interval,
then it is outside the expected degree of recurrence if genus associ-
are generally not recurrent. This suggests that the segre-
ations were random.
gation of bivalves and brachiopods is a real aspect of the
data set, while the faunal associations within each group
are weak. ing bivalve and brachiopod associations, the aim is to de-
Whether or not the correlation coefficients differ signif- termine whether one is more recurrent than the other. To
icantly from random associations, they still describe the test this, a bootstrap procedure was used (Efron and Tib-
amount of recurrence in the structure of the data, which shirani, 1991): rather than randomize the data matrices,
may differ between the two taxonomic groups. In compar- they were sampled with replacement by randomly picking

Summary of Results

In the Pennsylvanian-Permian Midcontinent, two dis-

tinct biofacies can be distinguished—one dominated by bi-
valves and the other by brachiopods. This is the over-
whelming pattern in both the cluster analyses and ordi-
nations of these data, and is consistent with the findings of
previous workers in the region (Elias, 1937; Mudge and
Yochelson, 1962). Within each of these two biofacies, pre-
viously unrecognized compositional gradients can be re-
solved. In the brachiopods, one end of the gradient is inter-
preted as representing dysoxic environments (dominated
by relatively small taxa like Crurithyris, Rhipidomella,
Wellerella, Lissochonetes, and Hystriculina). The other end
of the gradient is represented by Juresania and Linoprod-
uctus, which are interpreted to have lived in more near-
shore environments. In the bivalve biofacies, Wilkingia
FIGURE 13—Bootstrapped confidence intervals (CI’s) for recurrence. and Pteronites are associated frequently with brachiopods,
Squares and circles indicate measured Spearman Rank Correlation suggesting they preferred open marine conditions, while
Coefficients using brachiopod and bivalve genera, respectively. I-bars other bivalves like Edmondia occupied more restricted
indicate 95% two-sided confidence intervals based on bootstrapped
resampling. Roman numerals indicate composite sequences (Fig. 1).
nearshore settings.
If any of these cases showed the measured values of each group Ordination of collections from each composite sequence
falling outside the confidence interval of the other, then that would suggests that these broad gradients recurred each time
indicate that the degree of recurrence was significantly different. This marine conditions were re-established on the platform,
is not the case in any of these comparisons. but the particular order of specific taxa along the gradi-
ents does not strictly recur. Recurrence analysis using a
randomization approach confirms that bivalves and bra-
chiopods remain segregated in each cycle, but the gradi-
entire collections from the original data set. The difference ents within each biofacies do not recur to a degree signifi-
between this procedure and the randomization approach cantly distinguishable from random associations. Boot-
is that the bootstrapped matrix is composed of collections strapping recurrence coefficients indicates that the rigidi-
known to be samples reflecting real species associations in ty (or lack thereof) of the order of species is not
each composite sequence. (The randomized matrices shuf- significantly different between the brachiopod gradient
fled occurrences; hence, any non-random species associa- and bivalve gradient.
tions originally present were destroyed.) The bootstrap At first glance, the lack of gradient recurrence may
procedure addresses the question: if the two sequences seem contradictory with the results of correspondence
were resampled many times over, retaining any structure analysis, which show interpretable environmental trends
of taxonomic associations present in the collections, what within the two groups. However, this simply indicates that
would be the range of correlation coefficients? Repeating taxa within the two communities are not strictly limited in
the bootstrap 1000 times and using the top and bottom their associations—they may co-occur with certain taxa
2.5% of the distribution of the correlation coefficients pro- more often than others, as depicted by the ordinations, but
vides 95% confidence intervals to bracket the true values. their range of tolerances relative to the amount of environ-
When comparing bivalves and brachiopods for differences mental change along the gradients allows them to occur
in degree of recurrence, if either of the two true correlation with most other taxa in the paleocommunity. This lack of
coefficients falls within the 95% bracket of the other strictly limited associations means that recurrence is dif-
group, the two are not considered significantly different. ficult to detect because the order of taxa observed every
This is a very stringent criterion, but this choice helps time the gradient is resampled will be quite variable.
compensate for the tendency of bootstrapping to inherent-
ly underestimate the true range of variation. In addition,
note that bootstrapped occurrence matrices were created DISCUSSION
so that every taxon occurred at least once, slightly loosen- Nature of Pennsylvanian-Permian Paleocommunities
ing the original restrictions of two or more occurrences per of the Midcontinent
taxon and making the test conservative.
The results of the bootstrapped tests of whether the re- The approach taken in this investigation is related
currence coefficients differ between the two groups are closely to gradient analysis as described by Whittaker
presented in figure 13. Although there are numerous oc- (1967). Rather than classifying assemblages into commu-
currences of r for one biofacies falling outside the range of nity types, he was interested in how species assemblages
the other, because the exclusion was not mutual, they change across a landscape in response to a changing envi-
were not counted as significant. These findings indicate ronmental complex. Springer and Miller (1990) advocated
that given the number and nature of the collections, there adopting such an approach in paleoecological studies.
is no consistently documentable difference in the strength Whittaker’s concept is summarized in figure 14. The
with which bivalve and brachiopod genera adhere to their ‘‘environmental gradient’’ is the sum of interrelated envi-
respective environmental gradients. ronmental factors that affect the organisms of the com-

those in Fig. 14) regardless of their geographic or strati-

graphic position. The Pennsylvanian-Permian Midconti-
nent Platform was a complex mosaic of depositional envi-
ronments disrupted by numerous stratigraphic disconti-
nuities—the outcrop belt rarely shows a simple facies gra-
dient vertically or laterally (Olszewski 2000). However, by
using as many collections as possible, compositional gra-
dients can be well constrained by reducing the gaps be-
tween samples. Correspondence analysis is one approach
to indirect gradient analysis and it provides a maximum
likelihood approximation of Gaussian curves for species
distributions (ter Braak, 1985).
The results presented above—i.e., two biofacies each
with an interpretable but weak gradient (Fig. 7A)—can be
depicted as in figure 14E. Although bivalves and brachio-
pods segregate, there is no pattern indicating competitive
exclusion or coadaptation within either biofacies. This is
more consistent with a Gleasonian model of species inde-
pendence within communities than with a strong Cle-
mentsian interconnection.
However, with regard to species interactions within a
biotic community, Whittaker et al. (1973) very clearly
warned against using the distribution of taxa along a gra-
dient as an indicator of how they divide the habitat at a lo-
FIGURE 14—Graphical representation of ecological composition gra- cation into niches (see Schoener, 1989 for elaboration).
dients. (A) Taxa showing exclusion and coadaptation. (B) Taxa show-
These patterns each represent a different scale, and the
ing exclusion but no coadaptation. (C) Taxa showing coadaptation but
no exclusion. (D) Taxa showing neither coadaptation nor exclusion. question of niches (sensu Whittaker et al., 1973) cannot be
(E) Exclusion between biofacies, but neither coadaptation nor exclu- addressed using data of the sort used in this study. The
sion within biofacies (after Springer and Miller, 1990; modified from point is that understanding the range of conditions that a
Whittaker, 1975). species can occupy along an environmental gradient pro-
vides only limited insight into the nature of interactions
with neighboring species at a single location during life.
munity. ‘‘Species importance values’’ are typically thought
of as abundances but can be any ecological variable, such Paleocommunity Stasis in the
as biomass or frequency of occurrence. When using pres- Pennsylvanian-Permian Midcontinent
ence/absence data, as in this study, the curves can be
thought of as the chance that a species will occur in a col- Another question of interest to paleoecologists is wheth-
lection from a certain point on the gradient. Note that al- er these paleocommunities are static or not. The present
though abundance and commonness (i.e., number of col- results indicate that the biofacies-level division into bra-
lections in which a taxon occurs) are often related (e.g., chiopod-dominated and bivalve-dominated assemblages
Fig. 3C), they need not be: some taxa occur in many collec- in these data is static—that is, it recurs consistently every
tions but rarely in great abundance, and some occur in time the basinal ecosystem is re-established. On the other
profusion but only at a few sites. hand, the way taxa fall along faunal gradients (i.e., how
There are two related means of understanding how spe- they divide up habitats) within the two biofacies is not
cies are distributed across an ecological gradient: direct static.
gradient analysis and indirect gradient analysis. Direct In a comparison of taxonomic turnover in the basin over
gradient analysis involves plotting species distributions 12.5 Myr, analysis presented by Olszewski and Patzkows-
against some factor like elevation, moisture, temperature, ky (in press) found that background turnover in bivalves
water depth, or oxygenation. Such distributions can be fit and brachiopods was not significantly different, although
with Gaussian curves showing overlapping species distri- their histories of first and last appearance episodes were.
butions in an environment (Fig. 14). Note that the mea- With regard to the relationship between ecological struc-
sured factor need not be the actual control on species dis- ture (measured using recurrence) and background turn-
tribution—it can be a proxy for a complex of environmen- over, the present results are equivocal—neither group dif-
tal factors. In marine paleoecology, biotic gradients often fers from the other in either aspect. If ecological structure
are associated with water depth when the main control had differed but turnover had not, or vice-versa, then it
may actually be a composite of turbidity, substrate tex- could be concluded that one had little influence on the oth-
ture, temperature, and oxygenation (Robbins and Bell, er. If both aspects were different in both groups then it
1994). could be determined whether stronger ecological structure
Indirect gradient analysis arranges samples based on fostered or suppressed turnover (depending on whether
taxonomic composition. Compositional differences typical- the two were positively or negatively correlated).
ly can be related to environmental factors without strict In contrast to background turnover, the consistent seg-
adherence to a geographic or stratigraphic gradient. That regation of biofacies suggests that the independence of
is to say, collections can be arranged along a gradient (like turnover episodes (brief periods of elevated first or last ap-

pearance) in the two groups (Olszewski and Patzkowsky,

in press) may be related to the introduction or elimination
of the habitat conditions required by the taxa composing
each biofacies. For example, the dramatic decrease in bra-
chiopod diversity above the Beattie Limestone Formation
(Olszewski and Patzkowsky, in press) may occur because
some environments favored by the brachiopods were elim-
inated (see the dramatic shift from dysoxic to well-oxygen-
ated brachiopod collections near the top of the study inter-
val in Fig. 10; the base of cycle 51 is the base of the Beattie
Limestone Formation). Habitat destruction (i.e., elimina-
tion of habitable environments) is one of the most efficient
extinction mechanisms in the modern world (Tilman et al.,
1994), and this is consistent with the paleontological re-
sult found in this study.

Comparison with Other Studies

Most recent studies concerning evolution of benthic ma-
rine faunas have focused on the taxonomic composition of
an entire basin over 106 to 107 years (e.g., Brett and Baird,
1995; Tang and Bottjer, 1996; Patzkowsky and Holland,
1997; Olszewski and Patzkowsky, in press), although
some have examined patterns at the finer scale of biofacies
(e.g., Delcourt and Delcourt, 1991; DiMichele and Phillips,
1995, 1996; Westrop, 1996). Some of these studies (Brett
and Baird, 1995) have recognized ecological-evolutionary
(EE) subunits (lasting 3 to 11 Myr) showing a static pat-
tern of taxonomic composition and bounded by brief epi-
sodes of elevated turnover. Morris et al. (1995) suggested
FIGURE 15—Graphic explanation of difference between analysis of
that processes governing ecological interactions might be Bennington and Bambach (1996) and this study. Resampling of sites
responsible for the static patterns within EE subunits. permitted Bennington and Bambach (1996) to constrain the range of
Such processes would be expected to result in strong re- compositional variation at points along an environmental gradient
currence of biotic gradients between composite sequences (sensu Whittaker, as in Fig. 14). The approach taken here, based on
due to strict limitation of the roles and interactions of in- numerous collections from many points along the environmental gra-
dividual taxa (however, see comments of Whittaker et al. dient, does not allow testing of individual collections for compositional
similarity, but does constrain the expected range of compositional var-
[1973] discussed above). In this study, no influence of any iation along an environmental gradient.
such processes acting within biofacies has been detected.
In addition, no patterns of EE subunit stasis in the faunas
of the Pennsylvanian-Permian Midcontinent platform many (but not all) collections from individual cycles, and
have been found (Olszewski and Patzkowsky, in press). in all comparisons between cycles. They found recurrence
In contrast to long-term, basinal analyses, several stud- only at the level of ‘‘paleocommunity type’’—equivalent to
ies of macroinvertebrates are comparable to this one in the biofacies identified in this study.
terms of duration, resolution, and geographic scale (Ben- These results are consistent with the present study, al-
nington and Bambach, 1996; Holterhoff, 1996; Pandolfi, though the scale of analysis is somewhat different. Large-
1996). All of these, like the present one, were based on in- scale associations between cycles were compared in this
dividual site collections rather than basinal compilations work, whereas Bennington and Bambach (1996) focused
and take advantage of stratigraphic cycles to test for con- on reproducibility of individual collections (Fig. 15). In
sistency of faunas through time. The findings of each are both studies, biofacies or ‘‘paleocommunity types’’ recur
briefly reviewed here to search for broader similarities but show a wide range of internal variation that is not
and differences. structured in a recurrent manner.
Bennington and Bambach (1996) examined fossil as- Holterhoff (1996) examined crinoid associations from
semblages from four major marine incursions in Pennsyl- three Upper Pennsylvanian cycles of the northern Mid-
vanian strata of the Appalachians. These recurred every continent (just a few million years older than rocks of the
0.4 to 2.5 Myr (about the same as the composite sequences present study). His cycles are similar in structure and du-
of the Midcontinent) and contain many of the same taxa as ration to the present composite sequences. He found five
the data presented here. The aim of their study was to de- paleocommunity types arrayed along an onshore-offshore
termine how similar individual collections had to be before gradient. Three of these paleocommunity types recur in
they could be considered the same. They did this by com- each cycle (the two others are absent in all but one due to
paring collections from different locations in the same cy- absence of sufficiently offshore depositional environ-
cle, comparing collections between cycles, and resampling ments). One of these biofacies was unique to the trans-
individual collections to constrain the range of variation. gressive phase of the cycles and absent from the regressive
They found that there were significant differences in portions.

These results are also consistent with the present study, factors (temperature, salinity, oxygenation, etc.) are un-
although a ‘‘no-analog’’ assemblage (Overpeck et al., 1992) clear.
unique to only one portion of a composite sequence has not (3) Testing for the recurrence of taxonomic associations
been recognized. Like the present results and those of each time marine conditions were re-established indicates
Bennington and Bambach (1996), none of Holterhoff’s that segregation of the biofacies is strongly recurrent, but
(1996) individual collections appear identical, although the order of species along gradients within the biofacies is
they do fall into distinct associations that recur from cycle not. The groups of genera defining the compositional gra-
to cycle. dients described above do roughly recur, but the specific
Lastly, Pandolfi (1996) examined Pleistocene coral-reef relationships among individual taxa do not.
assemblages from Papua New Guinea. He examined nine (4) With regard to stasis, a pattern of recurrent associa-
cycles over a 95-kyr period, comparable in resolution to tions within biofacies that is statistically distinguishable
the meter-scale cycles of the Midcontinent, but much finer from random taxonomic associations cannot be identified.
than Midcontinent composite sequences. At three differ- On the other hand, the segregation of the bivalve and bra-
ent locations, he measured transects from reef crest to reef chiopod biofacies is significantly recurrent, but probably
slope and compared assemblages from those two environ- reflects different environmental preferences between
ments from place to place and through time. He found these two groups rather than coevolutionary integration of
greater differences between locations than through time paleocommunities.
at any single location; this contrasts to other studies of
Quaternary terrestrial and level-bottom marine commu- ACKNOWLEDGMENTS
nities. As a result, Pandolfi (1996) suggested that coral-
reef dynamics distinctly differ from these other systems. This work was completed in partial fulfillment of T.D.
An important difference that Pandolfi (1996) points out Olszewski’s doctoral dissertation in the Department of
between his work and some other studies is the difference Geosciences, The Pennsylvania State University (avail-
in temporal scale—many other studies either focused on able through the Penn State Electronic Theses and Disser-
much shorter ecological time scales or much longer pale- tations website at: http://etda.libraries.psu.edu/). Discus-
ontological time scales. This led him to suggest that differ- sions with R.R. West and D.R. Boardman II in the field
ent patterns may be emerging at different scales of study. provided insights to the stratigraphy and paleoecology of
Although the temporal resolution used herein is signifi- the Midcontinent. Thanks to A.I. Miller and an anony-
cantly coarser than his, similarities are seen between Pan- mous reviewer for thoughtful and encouraging comments
dolfi’s (1996) results and the present investigation. Be- that helped to improve this article. Grants from the Na-
cause it was not possible to resample the same point on an tional Geographic Society, the Geological Society of Amer-
environmental gradient through time, results of the pre- ica, Sigma Xi, and the Krynine Fund of the Penn State De-
sent study only can be compared to his individual tran- partment of Geosciences made this work possible.
sects through time. However, if his three sites are consid-
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