Paleobiology, 35(1), 2009, pp. 77-93 
Ecology of extreme faunal turnover of tropical American 
scallops 
J. Travis Smith and Jeremy B.C. Jackson 
Abstract.?The marine faunas of tropical America underwent substantial evolutionary turnover in 
the past 3 to 4 million years in response to changing environmental conditions associated with the 
rise of the Isthmus of Panama, but the ecological signature of changes within major clades is still 
poorly understood. Here we analyze the paleoecology of faunal turnover within the family Pectin- 
idae (scallops) over the past 12 Myr. The fossil record for the southwest Caribbean (SWC) is re- 
markably complete over this interval. Diversity increased from a low of 12 species ca. 10-9 Ma to 
a maximum of 38 species between 4 and3 Ma and then declined to 22 species today. In contrast, 
there are large gaps in the record from the tropical eastern Pacific (TEP) and diversity remained 
low throughout the past 10 Myr. Both origination and extinction rates in the SWC peaked between 
4 and 3 Ma, and remained high until 2-1 Ma, resulting in a 95% species level turnover between 3.5 
and 2 Ma. The TEP record was too incomplete for meaningful estimates of origination and extinc- 
tion rates. All living species within the SWC originated within the last 4 Myr, as evidenced by a 
sudden jump in Lyellian percentages per faunule from nearly zero up to 100% during this same 
interval. However, faunules with Lyellian percentages near zero occurred until 1.8 Ma, so that geo- 
graphic distributions were extraordinarily heterogeneous until final extinction occurred. There 
were also striking differences in comparative diversity and abundance among major ecological 
groups of scallops. Free-swimming scallops constituted the most diverse guild throughout most 
of the last 10 Myr in the SWC, and were always moderately to very abundant. Leptopecten and 
Argopecten were also highly diverse throughout the late Miocene and early Pliocene, but declined 
to very few species thereafter. In contrast, byssally attaching scallops gradually increased in both 
diversity and abundance since their first appearance in our samples from 8-9 Ma and are the most 
diverse group today. Evolutionary turnover of scallops in the SWC was correlated with strong eco- 
logical reorganization of benthic communities that occurred in response to declining productivity 
and increased development of corals reefs. 
/. Travis Smith. Scripps Institution of Oceanography, University of California, San Diego, La Jolla, Cali- 
fornia 92093-0244. E-mail: tsmith@dudek.com 
Jeremy B. C. Jackson. Scripps Institution of Oceanography, University of California, San Diego, La Jolla, 
California 92093-0244, and Center for Tropical Paleoecology and Archeology, Smithsonian Tropical Re- 
search Institute, Box 2072, Balboa, Republic of Panama 
Accepted:    23 July 2008 
The isolation of the Atlantic from the Pacific 
Introduction Anderson and Roopnarine 2003), reef corals 
(Budd   and  Johnson   1999),   and  bryozoans 
(Cheetham  and  Jackson   1996,  2000,   all  of 
Ocean by the Isthmus of Panama ca. 3.5 Ma , . ,      , ., .. .                ,        ,   ,. J which exhibit increased evolutionary turnover (Coates et al. 1992, 2004; Coates and Obando ,,      _ _ , ,     ^  ,        r     ?   ?     . ?            , 
after 3.5 Ma. Kates of origination and extmc- 
1996; Bartoli et al. 2005) was associated with ..                        .,                   ,.rr        ,,                 ,. 
' tion vary greatly among different taxa, result- 
large changes in oceanographic conditions, ing ^ very ^rong faunal turnover in some 
high faunal turnover, and significant reorga- ^axa such as gastropods, reef corals, and erect 
nization of the benthic communities in the bryozoans but not in other groups such as hi- 
Tropical   Western   Atlantic   (TWA)   between valves and encrusting bryozoans (Cheetham 
about 3.5 and 1.5 Ma (Woodring 1966; Jackson and jackson 1996; Budd and Johnson 1999; 
and Johnson 2000; Todd et al. 2002; O'Dea et Jackson and Johnson 2000; Todd et al. 2002; 
al. 2007. Early studies were based largely on Johnson et al. 2007). Greater focus on origi- 
extinction of gastropods (Woodring 1966; Ver- nation also revealed that overall molluscan di- 
meij   1978;  Petuch  1982; Jones  and  Hasson versity    within    the    southwest    Caribbean 
1985; Vermeij and Petuch 1986), but more re- (SWC)    increased   during   faunal   turnover 
cent analyses have included bivalves (Jackson (Jackson et al. 1993), despite high extinction 
et al. 1993; Roopnarine 1996; Anderson 2001; rates of several "paciphillic" taxa that were 
? 2009 The Paleontological Society. All rights reserved. 0094-8373/09/3501-0006/$1.00 
78 J. T. SMITH AND J. B. C. JACKSON 
the primary focus of most earlier analyses 
(Woodring 1966; Jones and Hasson 1985; Ver- 
meij and Petuch 1986). 
Some of the most important ecological 
changes are apparent only through compila- 
tions of relative abundance instead of just lists 
of taxa (Todd et al. 2002). Predatory gastro- 
pods and suspension-feeding bivalves de- 
clined significantly in abundance, but not in 
overall diversity while reef dwelling gastro- 
pods became more abundant (Todd et al. 
2002). In contrast, other ecological groups of 
mollusks remained relatively unchanged in 
abundance. These differences between ecolog- 
ical patterns based on relative abundance data 
versus those derived only from taxonomic 
lists emphasize the importance of using abun- 
dance data in addition to diversity (McKinney 
et al. 1998; Jackson and Erwin 2006). However, 
abundance data can be highly affected by 
sampling biases, so samples must be collected 
in a standardized and systematic fashion 
(Jackson et al. 1999; Jackson and Erwin 2006). 
A major enigmatic feature of the SWC ex- 
tinction is that much of the peak in rates of 
faunal turnover, especially for gastropods and 
reef corals, occurred up to 2 Myr after the final 
closure of the Isthmus and associated major 
changes in TWA environments (Budd and 
Johnson 1999; Jackson and Johnson 2000; 
O'Dea et al. 2007). High levels of extinction 
around the end of the Pliocene and early Pleis- 
tocene have also been noted in faunas as far 
north as Florida (Stanley and Campbell 1981; 
Stanley 1986a; Petuch 1982,1995; Allmon et al. 
1993, 1996) and California (Stanley 1986b; 
Smith and Roy 2006). However, the relation of 
extinction patterns in these more northern 
faunas to the formation of the Isthmus is dif- 
ficult to define, despite the temporal correla- 
tion. Synthesizing the previous work of Petuch 
(1982), Vermeij and Petuch (1986), Jones and 
Allmon (1995), and Roopnarine (1996), All- 
mon (2001) postulated that the major environ- 
mental cause of extinction in the TWA was a 
regional decrease in productivity. This hy- 
pothesis is supported by major changes in 
abundance of different trophic groups in the 
SWC and by evidence for a regional drop in 
productivity ca. 4-3 Ma (Todd et al. 2002; 
O'Dea et al. 2007). However, the relationship 
between events in the SWC and the North 
American faunas analyzed by Stanley and 
Campbell (1981), Stanley (1986a) and Allmon 
et al. (1993, 1996) is still unclear. 
In this paper, we describe basic patterns of 
diversity, origination, and extinction, as well 
as apparent causes of faunal turnover, for spe- 
cies of the highly diverse and abundant bi- 
valve family Pectinidae (scallops) in the SWC 
and TEP over the past 12 Myr. The family Pec- 
tinidae is monophyletic (Waller 1978, 1984, 
1991,1993, 2006) yet exhibits a great variety of 
life habits and ecology that are useful to dis- 
sect how changes in the environment have af- 
fected the evolutionary expansion or decline 
of different functional groups. We also exam- 
ine patterns of origination and extinction at 
different taxonomic levels as well as the cor- 
respondence between diversity and abun- 
dance on a sample-by-sample basis. Use of all 
the available information provides a much 
more complete and subtle understanding of 
evolution and environment than that based on 
taxon counting alone. Analysis of the relation- 
ships between environmental change and 
scallop life-history evolution will be presented 
in a separate paper. 
Materials and Methods 
Quantitative samples of fossil scallops from 
Panama, Costa Rica, and Ecuador were ob- 
tained from 226 bulk samples supplemented 
by the more than 350 collections of specimens 
gleaned from outcrops by members of the 
Panama Paleontology Project (PPP) over the 
past 20 years. Paleontologists have studied all 
of the sedimentary basins included here since 
the 1920s so that we have been able to build 
on their early collections and stratigraphic 
framework. Samples come from three regions: 
(1) the TEP, (2) central and eastern Panama 
(referred to here as "isthmian"), and (3) the 
Bocas del Toro and Limon regions of north- 
western Panama and southeastern Costa Rica 
(Fig. 1). The most important collections from 
the TEP are from the Borbon and Manabi ba- 
sins in Ecuador (Pilsbry and Olsson 1941; Ols- 
son 1964; Hasson and Fischer 1986; Aalto and 
Miller 1999; Landini et al. 2002; Cantalamessa 
et al. 2005), the Nicoya Peninsula in Costa 
Rica,  and the Burica Peninsula in Panama 
ECOLOGY OF FAUNAL TURNOVER 79 
FIGURE 1. Map of sample areas. Boxed areas enclose the 
generalized sedimentary basins described in the text. A, 
Manabi. B, Borbon. C, Burica/Nicoya Peninsulas. D, Ca- 
nal Zone. E, Chucunaque. F, Bocas del Toro. G, Limon. 
Dredge samples were collected in the region of all five 
basins sampled for fossils in Panama and Costa Rica, as 
well as two areas off Nicaragua and Honduras where no 
fossils were sampled. Abbreviations: GP, Gulf of Pana- 
ma; GC, Gulf of Chiriqui; SB, western San Bias archi- 
pelago; BT, Bocas del Toro province from the Laguna 
Chiriqui to the Golfo de los Moskitos; LCH, Los Cochi- 
nos, Honduras; CMN, Cayos Moskitos, Nicaragua. 
(Olsson 1942; Coates et al. 1992). Collections 
from the isthmian region that have both TEP 
and SWC affinities include the classic forma- 
tions from the Canal Zone (Woodring 1957- 
1982; Collins et al. 1996b; Johnson and Kirby 
2006), the north-central Coast of Panama 
(Coates 1999), and the Darien region of Pan- 
ama (Coates et al. 2004). The Bocas del Toro 
and Limon region is the most extensively sam- 
pled and includes the Limon Basin in north- 
eastern Costa Rica (Olsson 1922; Collins et al. 
1995; McNeill et al. 2000), and the Bocas del 
Toro Basin in northwestern Panama (Olsson 
1922; Collins 1993; Collins et al. 1995; Coates 
et al. 2003, 2005; Coates 2006). In the analyses 
that follow, samples from the Isthmian and 
Bocas del Toro/Limon regions were combined 
to constitute the SWC regional fauna. Finally, 
dredge samples of recent scallops were ob- 
tained from the TEP and SWC as a baseline for 
comparison and calculation of Lyellian per- 
centages for samples of fossils (Fig. 1) (Smith 
et al. 2006). 
Bulk samples were first sorted to class (e.g., 
bivalve, gastropod, coral). Scallops were pick- 
ed and sorted from the bivalve fraction and 
identified to species following Waller (1969, 
1984, 1991, 1993, 2006). Previously unde- 
scribed species were identified using open no- 
menclature pending more thorough taxonom- 
ic comparison with samples from outside the 
regions sampled. Appendix 1 includes a com- 
plete list of all of the species found in this 
study. Individual samples were combined 
into faunules (Jackson et al. 1999; O'Dea et al. 
2007) to obtain a more representative sample 
of the composition and diversity of the scallop 
fauna from different places, environments, 
and ages through time. A faunule represents a 
group of samples from a single outcrop or 
closely adjacent exposures that can be as- 
signed with confidence to the same age and 
environment. Appendix 2 lists all of the faun- 
ules along with their age, environmental con- 
ditions, and diversity of scallops used in this 
study. These groupings do not reflect com- 
pletely equivalent sampling in terms of range 
of environment or sampling intensity, but they 
provide larger sample sizes allowing analysis 
of patterns within time bins. 
Diversity was calculated as species richness 
(S) and Shannon-Weiner diversity (H) (Hayek 
and Buzas 1997; Foggo et al. 2003). Species 
richness was calculated from all of the differ- 
ent collections combined. H was calculated 
from only the quantitative data from bulk 
samples. We calculated stratigraphic ranges 
for all species collected on the basis of actual 
occurrence and range-through data and used 
1-Myr time bins to assess general trends in di- 
versity. We also calculated extinction and 
origination rates through time on the basis of 
numbers of occurrences and per-taxon rates. 
We have not calculated confidence intervals 
for first and last occurrences of species be- 
cause all of the established methods are based 
only on occurrences (Strauss and Sadler 1989; 
Marshall   1994,   1997;   Wang   and   Marshall 
80 J. T. SMITH AND J. B. C. JACKSON 
-4 - 
-S 
-6 
1=1 
? 
? 
0 
? 
0 
0        S       ID       IS 
Faunules 
a 
o     so   ice   iso 
Collections 
0     10    JO    30    40 
Richness 
n \ZZL 
o i 00 
i 
n 
i 
0 
.30   -10   0    10   20 
LO      FO 
? 
a 
m 
CD 
D 
I 
m i 
n 
D 
h 
.!?   .15    ti     OS    14 
Ext Rate   Orig. Rate 
-2 
.3 
-4 - 
.S 
, -6 
B 
=1 
0   1    i    3   t    s 
Faunules 
? 
0     40    so   wo 
Collections 
? 
? 
0 
? 
0 
0 
0 
i 
0 
I 
CO 
1 
0 
1 
1 
0     10    SO    30    40 
Richness 
JO  -10   0    10   20 
LO FO 
-IX   -05   Ofl   OS   1.0 
Ext Rate   Orig. Rate 
FIGURE 2. Sampling, species diversity, extinction, and origination. Sampling is plotted as the number of faunules 
and collections. Species values are plotted as numbers of species for richness, first occurrences (FO), and last oc- 
currences (LO), and as per-taxon rates for extinction and origination rates. All data were calculated in 1-Myr time 
bins. A, Southwest Caribbean (SWC). B, Tropical eastern Pacific (TEP). 
2004), even though non-occurrences are of ob- 
vious biostratigraphic and evolutionary sig- 
nificance (Hayek and Bura 2001). Most scallop 
species in our collections are rare, as is typical 
of faunal samples generally (Hayek and Buzas 
1997; Jackson et al. 1999), and more than half 
of the Caribbean species and >80% of eastern 
Pacific species occur in just three or fewer 
faunules. In spite of their rarity however, the 
collector's curves for most of the younger 
stratigraphic intervals suggest that we have 
sampled most of the available species. Thus, it 
is unlikely that the absence of species from ho- 
rizons younger than their last observed occur- 
rence is an artifact. For all of these reasons, 
and the lack of practical alternative statistical 
methods that incorporate non-occurrences 
(Hayek and Bura 2001), we have taken the 
ranges of species occurrences of species at face 
value. 
Diversity in Space and Time 
The fossil record of the past 12 Myr is much 
more complete for the SWC than for the TEP 
(Coates et al. 1992) (Fig. 2A,B). Detailed sam- 
pling in the Bocas del Toro and Limon Basins 
has produced a reasonably complete record of 
scallop macroevolution in this region, espe- 
cially for the last 5 Myr. We sampled 14 faun- 
ules from the late Pliocene and Pleistocene, 16 
faunules from the early Pliocene, and seven 
faunules from the late Miocene. The most im- 
ECOLOGY OF FAUNAL TURNOVER 81 
portant gap in the record is for the Pleistocene 
younger than 1.4 Ma and the relatively poorly 
sampled interval from about 4.3 to 7 Ma. The 
isthmian region includes 15 late Miocene 
faunules and nothing from younger deposits 
including the Pleistocene deposits reported by 
Woodring (1957-1982). In contrast, the record 
from the TEP includes a huge gap in sampling 
between 7.3 and 3.6 Ma. Seven faunules were 
sampled from the late Miocene and seven 
faunules from the late Pliocene to early Pleis- 
tocene. 
Scallops were present in more than 95% of 
all the samples both fossil and recent, indicat- 
ing that the species within this family utilize 
a very broad range of environments compa- 
rable to bivalves as a whole. There were 82 
species of Pectinidae in our collections, 61 
from the SWC, 18 from the TEP, and three that 
occur as fossils in both regions (Appendix 1). 
Species richness over the past 12 Myr was 
much more variable in the SWC than the TEP 
(Fig. 2B). Diversity in the SWC increased from 
a low of eight species in the late Miocene to a 
high of 41 species in the middle Pliocene (4-3 
Ma) and then declined to 22 species today 
(Fig. 2A). In contrast, diversity in the TEP was 
essentially unchanged over the same period, 
with the apparent decrease between 7 and 4 
Ma due to a lack of samples for this interval, 
so the data are for range-through taxa only. 
Ten species occurred in the late Miocene and 
early Pliocene collections and nine to ten spe- 
cies in the Pleistocene to Recent (Fig. 2B). 
Collector's curves were constructed for each 
time bin sampled to test for sampling bias, 
and compared numbers of species collected to 
the total known diversity represented by col- 
lected and range-through taxa combined. In 
the SWC (Fig. 3A), the most heavily sampled 
fossil time bin, as measured by total number 
of specimens, is the middle Pliocene (4-3 Ma). 
A remarkable 40 of 41 total known taxa (98%) 
were recovered from this interval. Excluding 
the early Pleistocene (2-1 Ma), the next four 
most heavily sampled time bins (10-9, 5-4, 
3-2, and 7-6 Ma) contained 82-92% recovery 
of species known to have been present. In con- 
trast, the five most poorly sampled bins (6-5, 
9-8, 8-7,12-11, and 11-10 Ma) contained few- 
4) 
to 
e 3 
?~ 
*' *'        4to3Ma 
s- 
^T                  3 to 2 Ma 
5I04M3 
/ ^^Ir"tf^*-'10 s ** p. 
Recent, N = 9148 
Aj%/^__.      10 to SMJ       .- 2 to 1 Ma 
K^X^3to8Ma 
#f        Bto7Ma 
*?*         1310 12 Ms 
f-            11 to 10 Ma 
f_*          6 to 5 Ma 
*"*^         121011 Ms 
500 1000 1500 
Number of Specimens 
E 
? 3 
Z 
s
" 
s- 
R- 
10to9Ma 
^f '?               2to1MS 
Off'   '  810 7Ma 
wf     4 to 3 Ma 
Recent. N = 9806 
o- ' 
B 
500 1000 1500 
Number of Specimens 
FIGURE 3. Collector's curves. Sampling effort for the 
time bins sampled in the SWC (A) and TEP (B). The 
x-axis was truncated at 2000 specimens, far fewer than 
the sampled level of the Recent time bins, to allow visual 
appraisal of the fossil time bins. 
er than 50% of the species known to have oc- 
curred in the SWC during those age intervals. 
The records for two additional bins require 
separate comment. The high recovery (80%) of 
the oldest bin (13-12 Ma) is an artifact of the 
first occurrence of all but a single early Mio- 
cene species. In contrast, the early Pleistocene 
(2-1 Ma) bin is relatively well sampled (the 
third most specimens), but contained only 
67% of the species known to have occurred in 
the TWA during this time. We attribute this 
low recovery to the small number of faunules 
sampled (all from Swan Cay and several faun- 
ules in the Limon Basin) coupled with the in- 
creasing heterogeneity of Caribbean environ- 
82 J. T. SMITH AND J. B. C. JACKSON 
ments at this time (O'Dea et al. 2007). Testing 
these ideas, however, will require comparably 
detailed sampling from other regions of the 
TWA. 
Sampling in the TEP was generally good 
(Fig. 4B) despite the relatively small number 
of specimens because of the greater homoge- 
neity of TEP environments and relatively low 
numbers of species throughout the last 12 Myr. 
The stratigraphic ranges of all species in this 
study are depicted in Figure 4. 
Origination, Extinction, and the Ecology of 
Faunal Turnover 
The peaks in both origination and extinc- 
tion in the SWC at 4-3 Ma coincide with the 
maximum diversity of scallop species (Fig. 
2A). This is true for both the raw numbers of 
first and last occurrences and for per-taxon 
rates. In contrast, there is no obvious peak in 
origination or extinction in the TEP, although 
the 3-Myr gap in sampling may obscure a gen- 
uine peak in faunal turnover between 4 and 3 
Ma (Fig. 2B). 
The overall patterns of diversity and evo- 
lution of scallops in the SWC correlate closely 
with those observed for bivalve genera and 
subgenera from the same region (Todd et al. 
2002). There is a significant correlation be- 
tween numbers of scallop species and of bi- 
valve genera and subgenera (Fig. 5A; r2 = 
0.739, p = 0.0003) and between rates of ex- 
tinction for bivalves and for scallops (Fig. 5B, 
r
2
 = 0.736, p = 0.0004). However, the correla- 
tion between rates of origination for the two 
groups is only marginally significant (Fig. 5C; 
r2 = 0.324, p = 0.0536). 
Scallops exhibit a very wide range of life 
habits, including byssal attachment, free 
swimming, and cementing and nestling on 
both level bottoms and hard substrata (Stan- 
ley 1970), although the two latter life habits 
were not observed in our samples from the 
SWC. Several genera exhibit a mixture of life 
habits. Most species of scallops begin their ju- 
venile benthic existence attached by byssal 
threads to small hard substrata, but subse- 
quently detach to become merely sedentary or 
strongly free-swimming as adults (Stanley 
1970; Waller 1984, 1991, 2006). However, spe- 
cies in several genera, particularly those as- 
sociated with coral reef and seagrass environ- 
ments, retain byssal attachment as adults. Life 
habit of most species is readily apparent for 
fossil as well as living species from their shell 
morphology (Stanley 1970), although the ge- 
nus Leptopecten does not fit the overall mor- 
phological pattern as well as other genera in- 
cluded in Stanley's (1970) study. 
We exploited these ecological differences 
among scallops to examine the ecological pat- 
terns associated with faunal turnover. Species 
were assigned to one of four groups based on 
differences in life habits and taxonomy: (1) 
byssally attaching; (2) free swimming; (3) Ar- 
gopecten sensu stricto, excluding the unde- 
scribed Pectinid Genus A (Smith et al. 2006), 
that exhibit a combination of byssally attach- 
ing and free-swimming habits; and (4) Lepto- 
pecten (plus Pacipecten) that defy clear-cut eco- 
logical separation. These four groups include 
63 of the 82 scallop species (77%) of the entire 
tropical American fauna sampled from the 
two oceans; the rest were excluded from the 
ecological analyses. 
Byssally attaching scallops include species 
in the genera Spathochlamys, Demarzipecten, 
Caribachlamys, Bractechlamys, and Laevichla- 
mys. Spathochlamys occurs in both the TWA 
and TEP, whereas the other byssally attaching 
genera are restricted to the Caribbean, where 
they are overwhelmingly associated with cor- 
al reef environments (Waller 1993). Free- 
swimming species include all those tradition- 
ally assigned to the genus Euvola (Waller 
1991). However, Waller (2006) has emended 
this group and species are now assigned to 
two genera, Leopecten and Euvola. This group 
also includes species traditionally considered 
Amusium, which Waller (1991) included in the 
genus Euvola. The two taxonomically defined 
groups are distinct ecologically and are di- 
verse and abundant enough to justify separate 
analysis. Argopecten occurred in all environ- 
ments sampled whereas Leptopecten was more 
narrowly distributed ecologically in the SWC. 
Recent Leptopecten in the eastern Pacific have 
been described as r-selected (Morton 1994), a 
life-history pattern that appears to be unique 
among tropical American scallops. 
The proportional diversity and abundance 
of the four groups in the SWC varied greatly 
ECOLOGY OF FAUNAL TURNOVER 83 
o 
?2 
-4 
a    -6 
-e 
-10 
-12 
A 
o 
-2 
-4 
IE     -6 
-8 
-10 
-12 
B 
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c c tfl c: c c=    yirf c c c cCDcccc=c c^q c *? c:cccccc{n^<r?cW*inccccc lOcccWc     *,   .. ... ...      ,.. _ ,. 
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QQJ Q. Q. *-\jP CL       CL       CLCL 6. ,? _l        CLU ?      V 
tfl    tO   tf)W 
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i i i i i i i i i i 
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Ml  Q_ & O. & O. & Q_ Q__? 
o*? o> a> o> E E? BU 
CJQ.?'?'?' Q> <<- 
I I I I I 1 I I I I 
? E 
02 <CL- 
1 1^ 
FIGURE 4.    Stratigraphic ranges of tropical American scallops in the SWC (A) and TEP (B). Tick marks indicate 
actual stratigraphic occurrences. Generic names are indicated for each species for comparison with Appendix 1. 
<u   ? 
= . ? 13 
V) ac -. 
01 c o o B *. *T "3  3 to V^ c 
a. 
mmy/9 ?? 
?g 
LU   S 
To *^* o. 
a ^ o 
? / n  5 
*< % o 
60 60       100      120      HO      160      ISO 
Bivalve Genera 
0.01 0 05 0.10 0.15 
Bivalve Extinction Rate 
0D      0.1       0.2       0 3       0.4       05       0.6 
Bivalve Origination Rate 
FIGURE 5. Comparison of taxonomic extinction rates in the SWC. Plot compares the extinction rates for all bivalves 
(data from Todd et al. 2002) with the rates obtained in this study for scallop species. Individual points represent a 
1-Myr time bin. There is a significant correlation between the calculated rates (see text). 
84 J. T. SMITH AND J. B. C. JACKSON 
CO     01      02      OS     04 
/\        Proportion Richness   Q 
00   0:2   04   OS   0 8    10 
Proportion Abundance 
FIGURE 6. Proportions of species richness and abun- 
dance in the SWC for byssally attaching (B), free-swim- 
ming (F), Argopecten (A), and Leptopecten (L) in 1-Myr 
time bins. These data do not include all species in the 
data set, so proportions do not sum to 1 (see text for ex- 
planation of these four ecological/taxonomic groups). 
over the last 13 Myr (Fig. 6A,B). We used pro- 
portions instead of absolute numbers of spe- 
cies and specimens to reduce the effects of 
sampling bias. The proportion of species rich- 
ness through time was based on actual occur- 
rences plus range through data (Fig. 6A). The 
most notable difference is in the byssally at- 
taching group, which was absent prior to 8 Ma 
except for one species from the Emperador 
Limestone (16 to 18 Ma) that was not included 
in the analysis. The proportion of byssally at- 
taching species increased gradually to about 
15% from 8 to 4 Ma, after which diversity in- 
creased more rapidly until 2-3 Ma when bys- 
sally attaching species became the most di- 
verse group. Argopecten diversity increased to 
about 30% of early Pliocene pectinid faunas, 
when it was the most diverse scallop genus, 
and then gradually declined to only a single 
species. Leptopecten was the most diverse 
group ca. 11-10 Ma but declined thereafter. 
Patterns of proportional abundance for the 
four groups contrast markedly with patterns 
of proportional diversity (Fig. 6B). Sampling 
is poorest before 8 Ma (Fig. 3A), so the highly 
erratic nature of the older portion of this plot 
is most likely due to sampling bias. Between 
8?9 Ma and 1-2 Ma Argopecten was over- 
whelmingly the most abundant group of seal- 
I     I I 
A/ 
f A   \ 
W   L A 
ft F 
l\\ IV/L / 
0 0      0 1       0 2      0 3      04 0.0    0 2    0.4    0 6    03    10 
A        Proportion Richness   g        Proportion Abundance 
FIGURE 7.    Proportions of richness and abundance in the 
TEP. Data are for the same groups as in Figure 6. 
lops in the SWC before plummeting in the late 
Pleistocene to Recent. Byssally attaching spe- 
cies steadily increased in relative abundance 
after 4 Ma but did not become numerically 
dominant. Relative abundance of Leptopecten 
and free-swimming scallops varied much less 
after 8 Ma. 
As for origination and extinction, patterns 
of proportional diversity and abundance in 
the TEP (Fig. 7A,B) are obscured by the 3 Ma 
gap in samples. There are no samples prior to 
9 Ma, between 7 and 4 Ma, and between 3 and 
2 Ma (Fig. 2). Nevertheless, it is obvious that 
the patterns are strikingly different from 
those in the SWC because Leptopecten or Ar- 
gopecten are overwhelmingly dominant for the 
two well-sampled fossil horizons in the TEP as 
well as the Recent (Smith et al. 2006) (Fig. 7B). 
In contrast, byssally attaching and free-swim- 
ming species are both low in diversity and nu- 
merically rare. The decline in diversity but not 
abundance of Argopecten in the SWC and TEP 
is similar to the pattern observed for this ge- 
nus in California (Stump 1979; Smith and Roy 
2006), the Gulf of Mexico, and the Atlantic 
coast of Florida (Waller 1969). 
Origination rates in the SWC declined 
greatly over time for all groups except Lepto- 
pecten, which remained low throughout the 
entire 12 Myr (Fig. 8). Focusing just on the last 
5 Myr for which sampling is generally excel- 
lent, all four groups exhibit elevated evolu- 
ECOLOGY OF FAUNAL TURNOVER 85 
Argopicten FrBeSwl mining Lepra pec-ten 
?2 
)- 
?* - 
.5 
6 
ij 
-o 
.9 - 
-10 - 
-ii ? 
-12 
?J 
] 
CD 
I 
I 
! 
a 
-0 5        OH OS 10 
Ext. Rale     Orirp. Rale 
? 
i     r 
.1.0       -OS       00        OS IJ0 
Ext. Rale     Orig. Rate 
0 
0 
1   1   1 
0 
1 
1   II 
1 
? 
i         i 
1 
? 
? 
? 
.1.0       -05       00        OS 110 
Ext. Rale     Orig. Rale 
.1.0       -OS       0 0        OS        10 
Ext. Rale    Orig. Rale 
FIGURE 8.    Extinction and origination rates for the four ecological groups plotted in 1-Myr time bins. 
tionary rates between 4 and 3 Ma, just as for 
the family as a whole (Fig. 2A). However, the 
timing of peaks in extinction varies among the 
groups. Argopecten extinction rates peaked be- 
tween 2 and 1 Ma, whereas rates for byssally 
attaching species peaked between 3 and 2 Ma, 
and rates for Leptopecten and free-swimming 
species peaked at 4-3 Ma. Because all of these 
rates were calculated from the same samples, 
the differences among groups almost certain- 
ly reflect differences in their ecology. The ear- 
liest peaks in extinction for all four groups are 
artifacts of their first occurrence in our collec- 
tions. 
Local versus Regional Diversity and 
Geographic Heterochrony 
Analyses of trends through time using 
1-Myr bins ignore the very considerable spa- 
tial variability among local communities that 
we know are important in Recent benthic 
communities (Jackson 1972, 1973; Jackson et 
al. 1999; Smith et al. 2006; O'Dea et al. 2007). 
Therefore we compared patterns over time for 
faunules versus those based on 1-Myr bins to 
determine the magnitude of spatial variability 
in the SWC over time. Diversity of every faun- 
ule is invariably less than for the 1-Myr bin 
that contains the faunule (Appendix 2). This is 
unsurprising because faunules constitute a 
much smaller sample than all of the faunules 
from an entire 1-Myr time bin, so the differ- 
ences in diversity may entirely reflect the dif- 
ferences in sample size. Thus, as expected, 
there is a clear relationship between species 
richness and sampling intensity among faun- 
ules with different numbers of specimens (Fig. 
9A). However, plots of proportional species 
richness (proportion of the richness in the time 
bin) versus numbers of specimens per faunule 
demonstrate that the relationship breaks 
down above approximately 100 specimens per 
faunule (Fig. 9B). This is because each faunule 
includes a much narrower range of environ- 
mental conditions and more closely approxi- 
mates a local benthic community as recog- 
nized in the Recent than do all the samples 
from all the faunules in an entire 1-Myr time 
bin. 
We used two measures of species diversity 
in plotting diversity of faunules against time 
in the SWC: (1) species richness incorporating 
all the data, and (2) the Shannon Diversity In- 
dex H, which was based only on quantitative 
samples. The much higher species richness of 
Recent faunules (Fig. 10A) is due to some 
combination of the greater sampling intensity, 
wider range of bottom conditions encoun- 
tered in a dredge haul that inevitably encom- 
passes multiple habitats in heterogeneous 
tropical environments, and differential taph- 
onomic effects of dredge versus bulk samples. 
However, the differences are much less for 
Shannon's H, for which some of the fossil faun- 
ules approach the diversity of the Recent (Fig. 
10B). Excluding the Recent, diversity within 
86 J. T. SMITH AND J. B. C. JACKSON 
(ft 
CO 
0) 
c 
sz y 
C 
c 
c c 
cc    c 
ccc 
C   CKCC   C 
p 
case   ccc 
C  PCCC 
c   ce 
C E CC FFPC 
OP C   PC 
c       or   IPC 
EC   CC  P 
?I  ?I 1 1? 
1 2 3 
Log (Abundance) 
p 
p 
B Log (Abundance) 
FIGURE 9. Effect of sampling intensity. Sampling effort, plotted as the log of the total abundance in a faunule 
against the species richness (A) and against the proportion of total diversity recovered (B). C signifies faunules from 
the SWC, and p from the TEP. 
faunules increased through time (ANOVA, F 
= 10.76, p = 0.0022), but peaked between 4 
and 3 Ma, and subsequently declined. These 
patterns for faunules mirror those for total re- 
gional diversity (Fig. 2A). 
Petuch (1982) proposed the idea of "geo- 
graphic heterochrony" whereby relict and 
modern faunas could coexist temporally 
through the occupation of different habitats. If 
o - ?                  ?M?? 
t - 
5 
? 
* 
?tog* ? 
** 
g_ ? ? 
? 
?- # 
? 
i      i      i 
5      10     15 
Richness (S) 
~i 1 1 r 
0?   0.5   1.0   1.5   2,0 
Shannon's H 
FIGURE 10. Diversity through time in the SWC. Species 
richness and Shannon's H are plotted through time. Val- 
ues were calculated by faunule. Richness includes all 
samples and H includes only the bulk samples we have 
obtained (see text). 
this is true, we should see faunules composed 
primarily or entirely of extant species co-oc- 
curring within the same 1-Myr age intervals 
with faunules dominated by extinct species. 
To assess this possibility, we calculated Lyel- 
lian percentage for all the faunules using spe- 
cies occurrences and occurrences weighted by 
abundance. There was a striking shift in Lyel- 
lian percentages in the SWC between 4 and 2 
Ma regardless of whether abundance data 
were used (Fig. 11A,B, solid circles). However, 
o- 
* 
? 
? 
?     * 
? ? o    a 
? #?# 
5    4 - 
? 
? 
j0 o 
? O        0 
g_ ? ? 0 
? ? 
?- ? 
: 
=- 
? 
? 
,r 0 
g_ 
? 
? 
O   0 
? i 
0    20   40   60   80  100 
Lyellian by Species 
0    20   40   60   90  100 
Lyellian by Abundance 
FIGURE 11. Lyellian percentages through time. Data are 
plotted by faunule, using both species diversity and 
abundance. Filled circles are SWC, open circles TEP. 
ECOLOGY OF FAUNAL TURNOVER 87 
faunules with Lyellian percentages close to 
zero persisted until 1.6 Ma whereas faunules 
with Lyellian percentages close to 100% oc- 
curred as early as 3.5 Ma. Faunules with in- 
termediate Lyellian percentages were also 
common throughout this time. Thus "geo- 
graphic heterochrony" was widespread 
throughout the SWC for 2 Ma. In contrast, the 
shift from low to high Lyellian percentages oc- 
curred between 7 and 10 Ma in the TEP (Fig. 
11A,B, open circles), and these differences are 
especially apparent for calculations weighted 
by abundance data. 
Petuch postulated that relict faunas would 
occupy marginal environments. To test this 
idea, we compared the Lyellian percentages 
for faunules in the SWC during faunal turn- 
over (4.5-1 Ma) to the percent carbonate in the 
sediment, mean annual range of temperature 
(MART), and water depth (Appendix 2; data 
from O'Dea et al. 2007). None of these vari- 
ables were significantly correlated with Lyel- 
lian percentages despite their importance for 
explaining changes in overall community 
composition during this time. 
Discussion and Conclusions 
Patterns of scallop diversity have changed 
dramatically in the SWC over the past 12 Myr 
but not in the TEP. Total numbers of scallop 
species and their origination and extinction 
rates per million years in the SWC closely 
track their respective values for the entire bi- 
valve fauna at the generic and subgeneric level 
(Fig. 6) (Todd et al. 2002). All values peaked 
between 4 and 3 Ma as the barrier between the 
TEP and SWC was finally sealed and ocean- 
ographic conditions changed from modern 
TEP conditions to those observed in the SWC 
today (Haug and Tiedemann 1998; Coates et 
al. 2004; Bartoli et al. 2005; O'Dea et al. 2007). 
However, the evolutionary rates for scallops 
have been shown to be universally higher than 
for bivalves as a whole (Stanley 1986b), and in 
this fauna the intensity of faunal turnover was 
nearly three times greater for scallop species 
than for bivalve genera as a whole, and none 
of the extant species in the SWC originated 
earlier than 4.5 Ma. 
The large stratigraphic gaps in the record 
from the TEP preclude detailed analysis, but 
it is highly unlikely that richness of species in 
the TEP ever exceeded their richness today be- 
cause species richness remained stable and 
low before and after the sampling gap. Inter- 
estingly, several of the species with first oc- 
currences in the late Pliocene of Ecuador have 
earlier fossil records in the Gulf of California 
or farther north along the outer coast of Baja 
California or in California (Stump 1979; 
Moore 1984; Smith and Roy 2006). This pat- 
tern of northern species occurring in Ecuador 
during this time has been noted for fish and 
foraminifera (Landini et al. 2002). Moreover, 
unlike the SWC, three of the species alive to- 
day originated before 9 Ma. Such long species 
durations are always suspect, because de- 
tailed morphological analysis commonly re- 
veals cryptic species (Knowlton 1986; Roop- 
narine and Vermeij 2000). But this is not al- 
ways the case, as is well documented for bryo- 
zoans (Jackson and Cheetham 1994; Cheetham 
et al. 2007), and the exceptional persistence is 
not unsuspected in the TEP where conditions 
do not appear to have changed nearly as much 
as the SWC over the last 10 Myr. 
Three of the four main groups of scallops 
exhibited opposite patterns of success in the 
SWC and TEP as reflected in their proportion- 
al diversity and abundance (Figs. 6, 7). Lepto- 
pecten was the most diverse and abundant ge- 
nus in most samples from the TEP over the 
past 12 Myr but steadily declined in both di- 
versity and abundance in the SWC. Argopecten 
diversity declined sharply in both oceans over 
the past 2 Myr as has been observed elsewhere 
in North America (Waller 1969; Smith and Roy 
2006). Argopecten abundance remained high in 
the TEP but plummeted in the SWC in the last 
2-3 Myr. The decline of Argopecten abundance 
is all the more striking because the genus rep- 
resents the most abundant group of scallops 
in the SWC for the preceding 6 Myr. 
Although byssally attaching species were 
never diverse or abundant in the TEP (Fig. 7), 
they have enjoyed spectacular success in the 
SWC, where they are the group with the great- 
est increase in diversity (Fig. 6). Their increase 
is correlated (r2 = 0.418, p = 0.059) with the 
widespread expansion of high-carbonate en- 
vironments (Appendix 2; O'Dea et al. 2007) 
and increase in the development of coral reefs 
88 J. T. SMITH AND J. B. C. JACKSON 
since 4 Ma (Collins et al. 1996a; Johnson et al. 
1995; Budd and Johnson 1999; Jain and Collins 
2006; Johnson et al. 2007). Indeed, many bys- 
sally attaching species live attached to corals 
(Waller 1993). Although they also increased 
markedly in abundance, byssally attaching 
species never achieved the abundance char- 
acteristic of free-living species (Fig. 6). 
The coexistence for 2 Myr of faunules with 
widely divergent Lyellian percentages (Fig. 
11) strongly supports Petuch's (1982) hypoth- 
esis of "geographic heterochrony." However, 
we found no evidence that local communities 
with low Lyellian percentages were restricted 
to marginal environments, according to mea- 
surements of MART, percent carbonate in sed- 
iments, and water depth. One possible expla- 
nation for a lack of environmental effect is that 
faunules were sampled on the wrong spatial 
and temporal scales relative to environmental 
variability, but this seems highly unlikely for 
two reasons. First, pervasive time-averaging 
of sediments and fossils by bioturbation and 
other forms of disturbance should eliminate 
any fine-scale differences in distributions in 
level-bottom environments (Kidwell and Fles- 
sa 1996; Best and Kidwell 2000a,b; Kidwell 
2002). Second, the scale and density of sam- 
pling were sufficient to identify strong rela- 
tionships between benthic community com- 
position and these same environmental pa- 
rameters (O'Dea et al. 2007). 
An entirely different possible explanation 
stems from metapopulation theory and the 
concept of extinction debt under conditions of 
pervasive environmental change (Jackson et 
al. 1996a; Hanski and Gilpin 1997). By this ar- 
gument, species naturally exist in patches of 
high abundance in a landscape of low abun- 
dance or absence, and the persistence of the 
species depends on the number of patches oc- 
cupied, the rate of colonization of new patch- 
es, and the rate of extinction in patches al- 
ready occupied. Changes in these three pa- 
rameters depend in turn upon the specific life- 
history characteristics of the species in relation 
to their environment (Nee and May 1992; Til- 
man et al. 1994). Thus, species soon fated to 
go extinct may nevertheless persist in a de- 
clining frequency of patches until the last 
patch becomes extinct. 
Our data are in agreement with such a sce- 
nario (Fig. 11A,B). First, faunules within any 
1-Myr interval typically include only a small 
fraction of the scallop species that existed dur- 
ing that interval. This was particularly true 
during the 4-3 Ma interval when no single 
faunule contained more than 13 of the 41 spe- 
cies that inhabited the SWC at that time. Over- 
all differences in molluscan community com- 
position were also extremely high among dif- 
ferent faunules of the same age during this 
time (Jackson et al. 1999: Fig. 16). Thus, dif- 
ferences in species composition among faun- 
ules were extremely high during this period of 
maximum faunal and environmental change, 
and these differences persisted, albeit at de- 
creasing frequency, for 2 Myr. Moreover, some 
of the ill fated species were abundant within 
some faunules until very near the end as seen 
by the greater number of faunules with Lyel- 
lian percentages less than 30-40% when rela- 
tive abundance of species is included in the 
calculation (cf. Fig. 11B and HA). Most im- 
portantly, species that survived had larger 
eggs and shorter larval durations than those 
that became extinct (Smith et al. 2003; Smith 
and Jackson 2004). Such differences in life his- 
tory are the very essence of the model of ex- 
tinction debt (Nee and May 1992; Tilman et al. 
1994). 
In summary, the extreme faunal turnover of 
scallops in the SWC has a strong ecological 
signature that is apparent only when the life 
habits of the different species and their abun- 
dance are fully taken into account. Moreover, 
and despite these considerable differences, the 
patterns of diversity, origination, and extinc- 
tion for scallops as a whole are qualitatively 
very different from patterns for gastropods, 
reef corals, and erect bryozoans from the same 
region (Cheetham and Jackson 1996; Budd 
and Johnson 1999; Todd et al. 2002). Greater 
understanding of such major episodes of fau- 
nal turnover and extinction fundamentally de- 
pends upon exploiting such ecological differ- 
ences to factor out the processes responsible. 
Acknowledgments 
This work would not have been possible 
without the help of A. Coates, A. O'Dea, K. 
Johnson, F Rodriguez, the crew of the R/V 
ECOLOGY OF FAUNAL TURNOVER 89 
Xlrraca, and the many other people who 
helped collect and process samples. This work 
was financially supported by National Science 
Foundation Grants EAR99-09485 and EAR03- 
45471, the Smithsonian Tropical Research In- 
stitute, and the Scripps Institute of Oceanog- 
raphy's William E. and Mary B. Ritter Chair. 
We thank the government of the Republic of 
Panama for the permits allowing such a large- 
scale sampling program. S. Stanley K. Roy R. 
Norris, L. Levin, P. Hastings, and an anony- 
mous reviewer all provided valuable feedback 
on earlier versions of the manuscript. 
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Appendix 1 
List of species with fauna, first (FO) and last (LO) occurrence, and ecological group. 
Species Fauna FO (Ma) LO (Ma) Ecological group 
"Amusium" bocasense (Olsson, 1922) 
"A." laurenti (Gmelin, 1791) 
"A." sp. 2 
"A." toulae (Brown and Pilsbry, 1913) 
"Chlamys" onzola (Olsson, 1964) 
Aequipecten canalis (Brown and Pilsbry, 1913) 
A. plurinomis (Pilsbry and Johnson, 1917) 
A. sp. 3 
A. sp. 4 
A. sua (Olsson, 1964) 
Argopecten costaricaensis (Olsson, 1922) 
A. gibbus (Linnaeus, 1758) 
A. levicostatus (Toula, 1909) 
A. nerterus (Woodring, 1982) 
A. sp. A 
A. sp. 1 
A. sp. 4 
A. sp. 5 
A. sp. 8 
A. uselmae (Pilsbry and Johnson, 1917) 
A. ventricosus (Sowerby II, 1842) 
Bractechlamys antiUarum (Recluz, 1853) 
Caribachlamys imbricata (Gmelin, 1791) 
C. sentis (Reeve, 1853) 
Cryptopecten cactaceus (Dall, 1898) 
C. phrygium (Dall, 1886) 
C. woodringi (Olsson, 1964) 
Demarzipecten sp. 1 
D. sp. 2 
Euvola gordus (Olsson, 1964) 
E. perulus (Olsson, 1961) 
E. sp. (cf. E. perulus) 
E. reliquus (Brown and Pilsbry, 1913) 
E. ziczac (Linnaeus, 1758) 
Laevichlamys multisquamata (Dunker, 1864) 
Leopecten antiguensis (Brown, 1913) 
L. catianus (Weisbord, 1964) 
L. chazaliei (Dautzenberg, 1900) 
L. coralliphila (Olsson, 1922) 
L. gatunensis (Toula, 1909) 
L. macdonaldi (Olsson, 1922) 
swc 4.5 2.05 
swc 3.55 Recent 
swc 8.6 6.9 
swc 6.95 3.55 
TEP 9.65 3.35 
SWC 18 3.55 
SWC 12.6 3.55 
SWC 9.6 3.55 
swc 8.6 8.6 
TEP 9.65 9.65 
SWC 4.5 1.6 
SWC 3.55 Recent 
SWC 9.6 2.75 
swc 9.6 3.55 
TEP 7.3 7.3 
Both 9.65 3.55 
SWC 2.05 2.05 
SWC 3.55 1.4 
SWC 4 4 
SWC 12.6 1.6 
TEP 9 Recent 
SWC 3.55 Recent 
SWC 2.05 Recent 
SWC 3.55 Recent 
SWC 6.95 3.45 
SWC 1.6 Recent 
TEP 3.6 3.35 
SWC 6.9 3.45 
SWC 6.95 6.95 
TEP 9.65 9.65 
TEP 3.35 Recent 
SWC ? Recent 
SWC 9.6 3.55 
SWC 3.55 Recent 
SWC 3.55 Recent 
SWC 9.6 9.6 
SWC 9.6 3.55 
SWC 3.55 Recent 
swc 3.55 1.4 
Both 12.6 2.75 
Both 9.6 6.9 
Free-swimming 
Free-swimming 
Free-swimming 
Free-swimming 
Byssal 
Mixed 
Mixed 
Mixed 
Mixed 
Mixed 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Argopecten 
Byssal 
Byssal 
Byssal 
Mixed 
Mixed 
Mixed 
Byssal 
Byssal 
Free-swimming 
Free-swimming 
Free-swimming 
Free-swimming 
Free-swimming 
Byssal 
Free-swimming 
Free-swimming 
Free-swimming 
Free-swimming 
Free-swimming 
Free-swimming 
92 J. T. SMITH AND J. B. C. JACKSON 
Appendix 1. Continued. 
Species Fauna FO (Ma) LO (Ma) Ecological group 
L. marquerensis (Durham, 1950) 
L. sericeus (Hinds, 1845) 
L. sp. (cf. L. sericeus) 
L. sp. 4 
L. sp. 5 
Lepidopecten scissuratus (Dall, 1898) 
Leptopecten bavayi (Dautzenberg, 1900) 
L. biolleyi (Hertlein and Strong, 1946) 
L. sp. (cf. L. biolleyi) 
L. cracens (Olsson, 1964) 
L. ecnomius (Woodring, 1982) 
L. euterpes (Berry, 1957) 
L. sp. 2 
L. sp. 4 
L. velero (Hertlein, 1935) 
Lindapecten acanthodes (Dall, 1925) 
L. sp. 1 
Nodipecten arthriticus (Reeve, 1853) 
N. sp. (cf. N. arthriticus) 
N. nodosus (Linnaeus, 1758) 
Pacipecten linki (Dall, 1926) 
P. maturensis (Maury, 1925) 
P. sp. A 
P. sp. 1 
P. sp. 3 
P. tumbezensis (d'Orbigny, 1846) 
Pectinid A lineolaris (Lamarck, 1819) 
P. A. mimyum (Woodring, 1982) 
P. A. sol (Brown and Pilsbry, 1913) 
Pseudamusium (Peplum) fasciculatum (Hinds, 1845) 
P. (P.) sp. (cf. P. (P.) fasciculatum) 
Spathochlamys benedicti (Verrill and Bush, 1897) 
S. lowei (Hertlein, 1935) 
vestalis (Reeve, 1853) 
TEP 9 9 Free-swimming 
TEP 9 Recent Free-swimming 
SWC 2.05 Recent Free-swimming 
SWC 3.55 3.55 Free-swimming 
SWC 3.55 3.55 Free-swimming 
SWC 12.6 6.9 Mixed 
SWC 4.25 Recent Leptopecten 
TEP 1.85 Recent Leptopecten 
SWC 3.55 Recent Leptopecten 
TEP 9.65 7.35 Leptopecten 
SWC 11.6 3.45 Leptopecten 
TEP 1.6 Recent Leptopecten 
SWC 9.6 3.05 Leptopecten 
SWC 11.6 3.55 Leptopecten 
TEP 1.85 Recent Leptopecten 
SWC 4 Recent Byssal 
SWC 4.5 3.05 Byssal 
TEP 1.6 Recent Mixed 
SWC ? Recent Mixed 
SWC 2.6 Recent Mixed 
SWC 3.55 Recent Leptopecten 
SWC 4.5 2.6 Leptopecten 
TEP 9.65 9.65 Leptopecten 
SWC 4.5 3.5 Leptopecten 
SWC 2.05 2.05 Leptopecten 
TEP 9 Recent Leptopecten 
SWC ? Recent Mixed 
SWC 8.6 3.45 Mixed 
SWC 4.25 4.25 Mixed 
TEP 1.6 Recent Mixed 
SWC ? Recent Mixed 
SWC 3.55 Recent Byssal 
TEP 3.35 Recent Byssal 
SWC 6.3 6.3 Byssal 
SWC 2.6 2.6 Byssal 
SWC 4 2.05 Byssal 
SWC 7.3 7.3 Byssal 
SWC 3.55 3.55 Byssal 
SWC 2.05 2.05 Byssal 
SWC 2.05 2.05 Byssal 
SWC 4.5 Recent Byssal 
Appendix 2 
List of faunules used in this study with age estimate, mean percent carbonate, estimates of MART, species rich- 
ness, and Shannon's H. 
Basin Median age (Ma) (?) sobs H %CQ3 MART 
SWC, Nicaragua and Honduras 
Bahia Almirante Panama Recent 15 1.95 28.06 3.80 
Bocas del Toro Panama Recent 20 1.63 3338 3.39 
Cayos Moskitos Nicaragua Recent 14 1.44 84.15 1.80 
Golfo de los Moskitos Panama Recent 16 1.4 44.29 2.20 
Laguna Chiriqui Panama Recent 17 1.33 35.24 3.80 
Los Cochinos Honduras Recent 16 2.06 62.83 2.60 
San Bias Panama Recent 14 2.11 67.37 3.13 
Swan Cay Bocas del Toro 1.4   (0.6) 6 1.19 63.49 3.22 
Cangrejos Creek Limon 1.55 (0.05) 2 ? 36.1 ? 
Empalme Limon 1.6   (0.1) 6 1.08 41.07 ? 
Cerro Mocho Limon 1.6   (0.1) 1 ? ? ? 
Upper Lomas del Mar Limon 1.6   (0.1) 9 1.45 43.28 2.82 
Lower Lomas del Mar Limon 1.7   (0.2) 4 0.91 38.83 3.08 
Pueblo Nuevo Limon 1.95 (0.15) 4 
? ? ? 
ECOLOGY OF FAUNAL TURNOVER 93 
Appendix 2. Continued. 
Basin Median age (Ma) (?) sobs H %CQ3 MART 
NW Escudo de Veraguas Bocas del Toro 2.0   (0.1) 9 1.12 37.66 3.88 
Wild Cane Key Bocas del Toro 2.05 (0.15) 7 1.42 45.76 4.19 
Ground Creek Bocas del Toro 2.05 (0.15) 10 1.07 39.40 ? 
Fish Hole Bocas del Toro 2.6   (0.4) 13 1.96 19.55 2.36 
NC Escudo de Veraguas Bocas del Toro 2.75 (0.85) 6 0.77 35.44 2.68 
Bomba Limon 3.05 (0.15) 7 1.26 68.96 3.13 
Old Bank Bocas del Toro 3.3   (0.3) 7 1.49 50.68 ? 
Bruno Bluff Bocas del Toro 3.45 (0.15) 9 1.51 13.52 6.95 
Quitaria Limon 3.5   (0.1) 3 ? 24.53 ? 
Isla Solarte Bocas del Toro 3.55 (0.05) 7 0.88 54.10 6.68 
Santa Rita Limon 3.55 (0.05) 9 1.84 44.40 5.73 
Cayo Agua: Punta Nispero South Bocas del Toro 3.55 (0.05) 9 0.91 31.18 7.23 
Cayo Agua: Punta Nispero West Bocas del Toro 3.55 (0.05) 7 1.43 14.04 ? 
Cayo Agua: Punta Tiburon Bocas del Toro 3.55 (0.05) 10 1.13 30.73 4.23 
SE Escudo de Veraguas Bocas del Toro 3.55 (0.05) 5 0.64 28.10 ? 
NE Escudo de Veraguas Bocas del Toro 3.55 (0.05) 11 0.86 41.40 2.68 
Rio Bananito Limon 3.55 (0.05) 1 ? ? ? 
Rio Vizcaya Limon 3.55 (0.05) 1 ? 17.34 ? 
Cayo Agua: Punta Norte East Bocas del Toro 4.25 (0.75) 11 1.51 18.87 4.11 
Cayo Agua: Piedra Roja Bocas del Toro 4.25 (0.75) 11 1.31 27.73 3.52 
Cayo Agua: Punta Norte West Bocas del Toro 4.25 (0.75) 10 0.91 15.93 6.25 
Isla Popa Bocas del Toro 4.25 (0.75) 10 1.53 19.77 6.65 
Cayo Zapatilla Bocas del Toro 4.25 (0.75) 6 0.90 14.61 5.62 
Shark Hole Point Bocas del Toro 5.65 (0.05) 3 0.8 14.25 5.22 
South Valiente West Bocas del Toro 6.29 (0.97) 5 1.21 18.22 6.16 
Finger Island Bocas del Toro 6.9   (1.3) 2 0.41 16.55 6.17 
Plantain Cay Bocas del Toro 6.9   (1.3) 2 ? ? ? 
Patterson Cay Bocas del Toro 6.9   (1.3) 2 ? ? ? 
Playa Lorenzo Bocas del Toro 6.9   (1.3) 4 ? ? ? 
Toro Cay Bocas del Toro 7.3   (1.3) 4 0.64 54.17 ? 
Rio Tuba Limon 7.7   (0.5) ? ? 
Isthmian 
Gatun Canal 6.0   (2.5) 9 1.2 28.27 ? 
Rio Tupisa Chucunaque 6.35 (0.75) 5 1.19 15.28 6.65 
Rio Chico N17 Chucunaque 6.35 (0.75) 7 0.94 20.11 8.67 
Rio Icuanati Chucunaque 6.95 (1.35) 4 1.18 24.88 ? 
Rio Tuquesa Chucunaque 6.95 (1.35) 6 1.29 17.48 ? 
Yaviza Chucunaque 6.95 (1.35) 2 ? ? ? 
Rio Indio North Coast 6.95 (1.35) 3 0.1 18.47 ? 
Rio Chucunaque Chucunaque 7.05 (1.25) 1 ? 9.46 ? 
Rio Calzones North Coast 8.25 (2.95) 4 0.8 15.02 4.57 
Miguel de la Borda North Coast 8.6   (1.8) 3 0.52 23.57 ? 
Mattress Factory Canal 9.0   (0.4) 10 1.37 24.55 6.18 
Isla Payardi Canal 9.6   (1.3) 7 0.35 25.15 ? 
Rio Tuira Chucunaque 10.15 (0.75) 4 0.64 14.22 ? 
Martin Luther King Canal 11.6   (0.2) 2 ? ? ? 
Rio Chico Nil Chucunaque 12.6   (0.1) 4 0.68 18.36 ? 
Eastern Pacific 
Gulf of Chiriqui Panama Recent 11 1.72 25.92 5.92 
Gulf of Panama Panama Recent 8 1.3 30.26 5.92 
Tablazo Manabi 1.4   (0.4) 5 1.08 15.36 ? 
Armuelles Burica 1.6   (0.1) 9 ? ? ? 
Nicoya Nicoya 1.6   (0.1) 8 ? ? ? 
Punta Canoa Manabi 1.6   (0.6) 4 0.54 23.00 ? 
Golfo Dulce Burica 1.85 (0.35) 6 ? ? ? 
Calle Esmeralda Borbon 3.35 (0.25) 7 1.24 15.39 ? 
Rio Camarones: Onzole Borbon 3.6   (0.4) 1 ? 20.62 ? 
Jama Manabi 7.3   (1.3) 2 ? 13.36 ? 
Favio Alfaro Manabi 7.35 (1.35) 4 0.5 11.13 ? 
Palma Royal Borbon 9       (0.4) 3 0.53 34.01 ? 
Punta Verde: Onzole Borbon 9      (0.4) 3 ? ? ? 
Cueva de Angostura Borbon 9.65 (1.25) 4 0.66 15.54 ? 
Punta Verde: Angostura Borbon 9.65 (1.25) 4 0.67 17.11 ? 
Rio Cayapas Borbon 9.65 (1.25) 2 0.12 16.10 
?