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Paleobiology, 31(4), 2005, pp. 578–590

Body size, extinction events, and the early record of veneroid bivalves: a new role for recoveries?

Rowan Lockwood

Abstract.—Mass extinctions can play a role in shaping macroevolutionary trends through time, but the contribution of recoveries to this process has yet to be examined in detail. This study focuses on the effects of three extinction events, the end- (K/T), mid- (mid-E), and end- Eocene (E/O), on long-term patterns of body size in veneroid bivalves. Systematic data were col- lected for 719 species and 140 subgenera of veneroids from the through of and . Centroid size measures were calculated for 101 subgenera and glob- al stratigraphic ranges were used to assess extinction selectivity and preferential recovery. Vene- roids underwent a substantial extinction at the K/T boundary, although diversity recovered to pre- extinction levels by the early Eocene. The mid-E and E/O events were considerably smaller and their recovery intervals much shorter. None of these events were characterized by significant ex- tinction selectivity according to body size at the subgenus level; however, all three recoveries were strongly size biased. The K/T recovery was biased toward smaller veneroids, whereas both the mid-E and E/O recoveries were biased toward larger ones. The decrease in veneroid size across the K/T recovery actually reinforced a Late Cretaceous trend toward smaller sizes, whereas the increase in size resulting from the Eocene recoveries was relatively short-lived. Early Cenozoic changes in , temperature, and/or may explain these shifts.

Rowan Lockwood. Department of , The College of William and Mary, Post Office Box 8795, Wil- liamsburg, Virginia 23187. E-mail: [email protected]

Accepted: 17 January 2005

Introduction intervals or among events? and (3) What ef- fects (if any) do these events have on long- Mass extinctions can influence large-scale term patterns of veneroid size? patterns in the record by reinforcing, Body size is considered one of the most fun- disrupting, or in some cases, even establishing damental attributes of organisms, reflecting trends. Few extinction events have a discern- interactions among developmental, life histo- ible effect on long-term trends, but in situa- ry, physiological, and ecological processes tions in which they do, extinction selectivity is (McKinney 1990; Blackburn and Gaston 1994). presumed to play a major role (Norris 1991; Large-scale patterns associated with body Saunders et al. 1999). Although recovery in- size, including ‘‘Cope’s rule,’’ have been doc- tervals have received little attention until re- umented across a variety of clades and time cently, preferential (or biased) recovery can af- intervals (Stanley 1973; see review in Jablonski fect both the direction and magnitude of evo- 1996, 1997; Alroy 1998; among others). The ef- lutionary and ecomorphological change. Com- fects of extinction events on these trends are paring patterns of selectivity in a single clade rarely investigated, although the broader across multiple events may shed light on the question of whether extinctions are size selec- connections among extinction, recovery, and tive has received considerable attention. long-term trends. The purpose of this study is A clear-cut relationship between body size to examine extinction selectivity and prefer- and extinction probability has proved difficult ential recovery with respect to body size in ve- to document in the fossil record. Studies of neroid bivalves across the end-Cretaceous and background extinction in the fossil record Eocene extinctions. Questions to be addressed seem to show no significant relationship be- include (1) Do these events show any evidence tween body size and survivorship (see dis- of extinction selectivity or preferential recov- cussion of Hallam 1975 in Jablonski 1996; ery according to veneroid size? (2) Does selec- Budd and Johnson 1991), with the exception of tivity differ between extinction and recovery Stanley’s (1986, 1990) data on Late bi-

᭧ 2005 The Paleontological Society. All rights reserved. 0094-8373/05/3104-0003/$1.00 BODY SIZE, EXTINCTIONS, AND VENEROIDS 579 valves from California and Japan. The concept Possible causes of both of these extinctions in- that mass extinctions selectively eliminate clude change (Hansen 1987; Ivany et large taxa is intuitively appealing, but rarely al. 2003a) and sea level fluctuation (Dockery substantiated (LaBarbera 1986; Raup 1995). 1986; Dockery and Lozouet 2003). Global data for bivalve genera show no evi- dence of size selectivity across the K/T mass Methods extinction (Jablonski and Raup 1995; Jablonski This study involved the collection of sys- 1996). Similar patterns have been documented tematic data for 719 veneroid species (repre- in European bivalves across the end- senting 140 subgenera) recorded from Late extinction (McRoberts and Newton 1995; Cretaceous to Oligocene deposits in North McRoberts et al. 1995) and North American America and Europe. Data collection was lim- across the late Eocene extinction ited to extratropical regions to avoid the poor (Van Valkenburgh 1994). Although size selec- preservation and minimal sampling associat- tivity is often cited for K/T and ed with tropical environments during this (Russell 1977; Clemens 1986), it is un- time. Taxonomic identifications were based on clear to what extent these patterns represent personal observation and alpha-taxonomic in- clade-specific extinction (Jablonski 1996). Per- formation available in the literature. For a haps the best-documented case of size selec- more detailed description of systematics and tivity in the fossil record is the preferential ex- sampling, see Lockwood (2004). tinction of large planktonic Size data were obtained for 1236 specimens across the K/T extinction (Norris 1991; Ar- (representing 101 subgenera) sampled from nold et al. 1995). both field and museum collections. Specimens The present study focuses on the late Me- were photographed in two orientations (lat- sozoic and early Cenozoic record of body size eral and cross-sectional [Fig. 1]) and 100 in three closely related superfamilies of het- equally spaced points were digitized around erodont bivalves: the Veneroidea, Arcticoidea, each outline using Optimas 5.2 for Windows. and Glossoidea (collectively referred to here, Centroid size was calculated in both lateral for simplicity’s sake, as veneroids). The vene- (Cl) and cross-sectional (Cc) orientations as the roids are infaunal, suspension-feeding bi- square root of the sum of squared distances of valves that experienced a remarkable radia- the set of landmarks from their centroid tion during the last 65 Myr and are abundant (Bookstein 1991). Centroid size is the only in modern shallow marine environments measure of size to be uncorrelated with shape (Palmer 1927; Cox 1969; Canapa et al. 1996, in the absence of allometry and is increasingly 1999; Harte 1998a,b; Passamonti et al. 1998, used in morphometric studies of fossil taxa 1999; Coan et al. 2000). (e.g., Roopnarine and Beussink 1999; Ander- The extinction events examined in this son 2001; Roopnarine and Tang 2001). Cen- study differ considerably according to dura- troid size measures were significantly posi- tion, magnitude, and causal mechanism. The tively correlated with traditional linear mea- K/T extinction, which occurred at 65 Ma, is sures (including shell length and height) (all ϭ Ͻ one of the ‘‘Big Five’’ mass extinctions and has Spearman R100 0.81; p 0.0000001). Given received considerable attention, primarily be- the tight correlations among these size mea- cause of evidence that it was caused by a bo- sures and the advantages associated with cen- lide impact (see papers in Ryder et al. 1996). troid size, I opted to use the latter for the re- The Eocene–Oligocene transition was one of mainder of this study. I combined the two the most severe events faced by marine inver- measures of centroid size into a single mea- tebrates during the Cenozoic (Prothero et al. sure by calculating their geometric mean

2003). When this event is examined in detail, (Cgeo) (Stanley 1986, 1990). I used the largest at least two minor pulses of extinction can be specimen available for each species to ensure recognized: one at the end of the middle Eo- that I was measuring adult, rather than juve- cene (37 Ma, mid-E) and one at the end of the , specimens (Stanley 1973; Jablonski 1997). Eocene (33.7 Ma, E/O) (Ivany et al. 2003a). I compiled stratigraphic occurrences from 580 ROWAN LOCKWOOD

calculated by using the number of taxa that range completely through an interval relative to the total number that range out of the in- terval, as in Foote (2000). Global stratigraphic ranges were used to categorize subgenera as victims, survivors, or new taxa for the K/T, mid-E, and E/O events. Victims are subgen- that went extinct, survivors are subgenera that survived, and new taxa are subgenera that originated during the recovery interval. I defined recovery as the interval required for veneroid diversity to reach pre-extinction lev- els. I compared the means of victims and sur- vivors to assess extinction selectivity and the means of survivors and new taxa to assess preferential recovery. All of the species representing a subgenus throughout its geographic (in North America and Europe) and stratigraphic range were pooled to calculate the mean of each size mea- sure for each subgenus. Kolmogorov-Smirnov one-sample tests of normality revealed no sig- nificant deviation in the distribution of any of the size measures from a normal distribution after adjustment for multiple comparisons (all Ͼ Ͼ D100 0.14; p 0.05). Subsequent analyses of these measures used parametric statistics, ex- cept when otherwise stated. Sequential Bon-

FIGURE 1. Lateral and cross-sectional size measures. ferroni adjustment was applied to each inde- One hundred equally spaced points were digitized pendent pool of statistical analyses, to adjust around the shell outline in two orientations: lateral and for multiple comparisons (Rice 1989). cross-sectional.

Results fieldwork, museum collections, and the liter- Veneroid Diversity ature for 140 subgenera. First (FAD) and last (LAD) appearance data were established for Patterns of veneroid diversity from the Late each subgenus on the basis of global occur- Cretaceous through early Cenozoic (Fig. 2A) rence data. Stratigraphic range data for sub- are similar to those documented for bivalves genera are available in Lockwood (2004). The as a whole (Miller and Sepkoski 1988; Raup Late Cretaceous through Oligocene was divid- and Jablonski 1993). Veneroid diversity in- ed into 28 intervals, which range in duration creased throughout the Late Cretaceous and from 2 to 4 Myr, and make it possible to com- early Cenozoic, with the exception of a minor pare diversity across time intervals of roughly plateau in the Eocene. A major extinction oc- similar durations. These intervals were de- curred at the K/T boundary, along with very signed to coincide with major chronostrati- minor extinctions in the early , at the graphic and biostratigraphic boundaries, end of the middle Eocene, and at the end of the whenever possible. Eocene (Fig. 2B). The K/T extinction was Subgeneric diversity was calculated by slightly more severe for veneroids (79% de- counting boundary-crossing taxa (Foote 2000; crease in subgeneric diversity, 81% extinction) see also Harper 1975; Bambach 1999). Esti- than for bivalves in general (Raup and Jablon- mated per-taxon rates of extinction (q) were ski 1993). This may relate to the fact that ma- BODY SIZE, EXTINCTIONS, AND VENEROIDS 581

8.5% decrease in subgeneric diversity, 8.5% extinction) and a second, slightly more severe extinction at the end of the Eocene (33.7 Ma; 16.3% decrease in subgeneric diversity, 18.6% extinction). Background extinction levels (ex- cluding the K/T, mid-E, or E/O events) aver- age 4.1% for veneroid subgenera throughout this interval. Bootstrap resampling (1000 ran- dom resamplings with replacement) yielded 95% confidence intervals ranging from 1.98% to 6.76%, indicating that the extinction levels documented for the K/T, mid-E, and E/O events exceed background levels. The recov- ery intervals following the mid-E and E/O events were considerably shorter than the K/ FIGURE 2. A, Diversity patterns in veneroids. Global subgeneric diversity measured as the number of taxa T recovery and were complete by 35.4 Ma and crossing boundary intervals. Error bars represent the 31 Ma, respectively. Comparing the timing square root of the number of taxa crossing each bound- and magnitude of veneroid extinctions with ary (Foote 1993), derived from the standard error of a Poisson variable. The three gray lines represent the K/ Eocene extinctions in other mollusks is com- T, mid-E, and E/O extinctions. B, Estimated per-taxon plicated by a scarcity of published data with extinction rate (q) measured by using the number of taxa comparable taxonomic and spatial scaling. that range completely through an interval relative to the total number that cross into the interval (Foote 2000). Er- Dockery’s and Hansen’s studies of Gulf Coast ror bars are approximate and represent Ϯ 1 SD calcu- molluscan faunas remain the most often cited lated from the 95% confidence intervals of a proportion studies (Dockery 1984, 1986; Hansen 1987, (M. Foote, personal communication, 2000). The three gray lines represent the K/T, mid-E, and E/O extinc- 1988, 1992; Haasl and Hansen 1996; Dockery tions. and Lozouet 2003). Both of these data sets doc- ument a major extinction of mollusk species at the mid-E boundary and a larger, more abrupt rine suspension feeders such as veneroids extinction at or near the E/O boundary. Haasl tended to suffer greater extinction at the K/T and Hansen (1996) argued that the immediate than deposit feeders (Sheehan and Hansen appearance of a high diversity fauna after the 1986; Jablonski and Raup 1995). The K/T re- E/O boundary demonstrates that the recovery covery was relatively rapid and veneroid di- was complete by the earliest Oligocene. Their versity reached pre-extinction levels by 53 Ma. estimate of recovery duration agrees well with This contrasts with Hansen’s (1988) data for the patterns documented in this study. Gulf Coast bivalve species, which indicate that diversity did not rebound fully before the E/ Extinction Selectivity and Preferential O event (Hansen 1988; see also Stanley 1990). Recovery Hansen’s results may conflict with mine sim- K/T. Veneroid size frequency distributions ply because of the different taxonomic levels before the K/T extinction differ considerably and spatial scales used in the two analyses. It from those after the K/T recovery (Fig. 3A,B), is worth noting, however, that the effects of suggesting that this event may be size selec- the K/T were not protracted for the majority tive at the subgenus level. To determine of marine organisms and paleocommunities whether this selectivity is associated with the (Arnold et al. 1995; Sheehan et al. 1996; Ja- extinction itself or the subsequent recovery, I blonski 1998; Heinberg 1999). compared victims with survivors and survi- Similar to Gulf Coastal mollusks vors with new taxa across the K/T boundary. (Dockery 1998), veneroids show little genus- I found no evidence of size-selective extinction level extinction across the /Eocene across the K/T event (Table 1, Fig. 4A). The boundary (Fig. 2). A very minor extinction oc- recovery was, however, biased toward smaller curred at the end of the middle Eocene (37 Ma; veneroids. New taxa are significantly smaller 582 ROWAN LOCKWOOD

FIGURE 3. Size frequency distributions for veneroid subgenera that occur before the K/T extinction (A), after the

K/T recovery (B), before the mid-E extinction (C), and after the E/O recovery (D). Mean centroid size (Cgeo) for each interval is indicated by the dashed line on each plot. than survivors. These patterns remain robust basis of species and to test for when size is partitioned into lateral and cross- preferential recovery, I calculated the means sectional measures. There is no indication of of survivors and new taxa solely on the basis extinction selectivity in either measure, and of Paleocene species. The resulting trends preferential recovery toward smaller taxa is were in the same direction, although not al- evident in both lateral and cross-sectional ways statistically significant, as those outlined measures, although the signal is stronger in above. the former. Mid-E. Turning to the Eocene events, size These selectivity analyses are based on frequency distributions record a very slight means calculated by pooling all of the species increase in veneroid size across these intervals representing a subgenus throughout its strati- (Fig. 3 C,D). The mid-E extinction showed no graphic and geographic range (in North selectivity according to subgeneric size, re- America and Europe). To determine whether gardless of how size was measured (Table 1, this pooling affected the results, I also com- Fig. 4B). The recovery was, however, size bi- piled subgeneric means at the level. To ased. New taxa are significantly larger than assess extinction selectivity, I calculated the survivors when size is measured as geometric means of victims and survivors solely on the mean, centroid size in lateral orientation, or

TABLE 1. Extinction selectivity (Ext) and preferential recovery (Rec) according to veneroid size across the K/T, mid-E, and E/O events. Statistically significant results are in boldface.

KT mid-E E/O Ext Rec Ext Rec Ext Rec Ϫ ؍ Ϫ ϭϪ ؍ ϭϪ ؍ ϭ Cgeo t19,9 0.35, t9,29 1.99, t6,49 0.66, t49,2 2.90, t5,46 1.08, t46,11 2.6, 0.01 ؍ p ϭ 0.29 p 0.005 ؍ p ϭ 0.51 p 0.05 ؍ p ϭ 0.73 p Ϫ ؍ Ϫ ϭϪ ؍ ϭϪ ؍ ϭϪ Cl t19,9 0.24, t9,29 2.90, t6,49 0.99, t49,2 3.64, t5,46 0.81, t46,11 2.85, 0.006 ؍ p ϭ 0.42 p 0.0007 ؍ p ϭ 0.32 p 0.006 ؍ p ϭ 0.81 p Ϫ ϭϪ ϭϪ ؍ ϭϪ ؍ ϭ Cc t19,9 0.18, t9,29 2.18, t6,49 0.48, t49,2 1.97, t5,46 1.18, t46,11 1.77, p ϭ 0.24 p ϭ 0.08 0.05 ؍ p ϭ 0.63 p 0.04 ؍ p ϭ 0.86 p BODY SIZE, EXTINCTIONS, AND VENEROIDS 583

Ϯ FIGURE 5. Mean ( SE) centroid size (Cgeo) through time. Gray lines represent the maximum and minimum

values for Cgeo through time. The three dashed lines rep- resent the K/T, mid-E, and E/O extinctions.

centroid size in cross-sectional orientation. The recovery results should be treated with caution, owing to the extremely small sample of new taxa in this analysis (n ϭ two subgen- era classified in different superfamilies). E/O. Finally, I found no evidence of extinc- tion selectivity at the E/O according to sub- generic size, regardless of the size measure ex- amined (Table 1, Fig. 4C). Similar to the mid- E, the E/O recovery was biased toward larger taxa. New taxa are significantly larger than survivors when size is measured as geometric mean and as centroid size in lateral orienta- tion. There is a tendency for new taxa to be larger than survivors when centroid size is measured in the cross-sectional orientation; however, the difference is not statistically sig- nificant. Ϯ FIGURE 4. Mean ( SE) centroid size (Cgeo) of victims, survivors, and new taxa across the K/T, mid-E, and E/ Body Size in Veneroids through Time O events. A, K/T event. No significant difference be- tween victims and survivors. New taxa are significantly General Patterns. To examine the effects of ϭ ϭ smaller than survivors (t9,29 1.99; p 0.05). B, Mid-E event. No significant difference between victims and the K/T, mid-E, and E/O events on long-term survivors. New taxa are significantly larger than survi- patterns of veneroid size, I plotted the mean vors (t ϭϪ2.90; p ϭ 0.005). C, E/O event. No signif- Ϯ 49,2 ( SE) of centroid size (Cgeo) through time icant difference between victims and survivors. New ϭϪ (Fig. 5). All of the species representing a sub- taxa are significantly larger than survivors (t46,11 2.6; p ϭ 0.01). genus throughout its geographic (in North America and Europe) and stratigraphic range were pooled to calculate the mean of each size measure for each subgenus, and all subgenera crossing a boundary contributed to the cal- culation of the mean for that boundary. This 584 ROWAN LOCKWOOD range-through approach assumes that the size fossil record are more likely to be sampled of a subgenus is unlikely to vary appreciably (Valentine 1989; Kidwell and Bosence 1991) relative to the size among subgenera, an as- and identified than small taxa. Indeed, the in- sumption that is supported by the fact that cidence of small taxa increases dramatically centroid size variation is statistically smaller when sediments are bulk-sampled or when within veneroid subgenera than among sub- intervals are particularly well sampled. Al- ϭ Ͻ genera (F62,326 4.34; p 0.001) throughout though sampling could account for the shifts this interval. This technique is not without its in mean size documented here, two pieces of limitations (explored in Foote 1991, 1994); evidence indicate that it is not exerting sub- however, in this particular case it is likely to stantial influence. First, sampling, quantified underestimate rather than overestimate shifts as the number of localities compiled for each in size across these boundary events. Veneroid time interval, is not correlated with size in this size decreased gradually throughout the Late study. Correlation between the first-order dif- Cretaceous. The K/T recovery, which was sig- ferences of size and sampling revealed no sig- ϭ ϭ nificantly biased toward smaller taxa, pro- nificant relationship (r26 0.01; p 0.97). Sec- duced a marked decrease in size that contin- ond, Sohl and Koch (1983, 1984, 1987) bulk- ued until 51.8 Ma. In fact, veneroid size before sampled several localities in the latest Maas- the K/T (averaged across the ten million trichtian and these occurrences are included leading up to the boundary) is significantly in this study. If sampling were affecting these larger than after the K/T (averaged across the results, I would expect size to decrease sharp- ten million years following the boundary) ly within the interval including the Sohl and ϭ ϭ (Mann-Whitney U3,4 2.12; p 0.03). These Koch data. Instead, it remains constant. results are remarkably robust, regardless of Preservation is also unlikely to yield these the time intervals included in the comparison. patterns. Larger taxa are more likely to be pre- The K/T recovery appears to have reinforced served than small taxa (Kidwell and Bosence and even accelerated an established trend to- 1991), and small taxa are more likely to be re- ward decreasing size. corded from well-preserved intervals. Preser- Veneroid size remained relatively constant vation may help to explain the small size of until the E/O event, when it began to increase Eocene veneroids, but it cannot explain the slightly. This increase leveled off by the mid- size decrease immediately after the K/T dle Oligocene. A comparison of veneroid size (which occurs during a time of poor preser- before the Eocene events (averaged across the vation, characterized by dissolution of shell ten million years leading up to the boundary) material and moldic preservation) or the in- versus size after the Eocene events (averaged crease after the E/O (which occurs during a across the ten million years following the E/ time of good preservation, characterized by O recovery) documents a significant increase preservation of original aragonitic shell ma- ϭϪ ϭ (Mann-Whitney U4,4 2.31, p 0.029), re- terial). Moreover, preservational bias tends to gardless of the time intervals used in the com- affect the smallest tail of the bivalve size dis- parison. The Eocene recovery intervals re- tribution (Ͻ2 mm in length [see for example versed the earlier trend toward decreasing Staff et al. 1986 in bays]), as opposed to body size and initiated a short-lived interval the mean sizes of veneroids documented of increasing body size. When size is parti- throughout this interval (majority Ͼ 10 mm in tioned into lateral and cross-sectional com- length). ponents, these patterns remain unchanged. It is important to emphasize that the pre- Unfortunately, given the limited sample sizes sent study was carried out at the subgeneric of veneroid subclades (average of four subcla- taxonomic level. Because many of the predic- des, five subgenera per subclade per interval), tions surrounding body size and extinction it was not possible to characterize these trends vulnerability are based on life-history traits as driven versus passive. that are relevant at the population or species Effects of Sampling, Preservation, Taxonomic level, it is worth considering whether the Level, and Phylogenetic Bias. Large taxa in the choice of taxonomic level is affecting these re- BODY SIZE, EXTINCTIONS, AND VENEROIDS 585 sults. Although preferential recovery at the dicates that recovery-driven changes in size subgenus level may well indicate selectivity at are not simply the result of sorting, at least at the species level, a lack of extinction selectivity the superfamily level. at the subgenus level does not necessarily in- Discussion dicate a lack of selectivity at the species level within individual lineages (see, for example, Body Size and Extinction Vulnerability Smith and Roy 1999). The fossil record of ve- The lack of size-selective extinction docu- neroids at the species level is so limited during mented in this study corroborates past conclu- this interval that species-level analyses are sions about mass extinctions in fossil mollusks simply not feasible. One potential way to ex- (Jablonski and Raup 1995; McRoberts and plore the question of species level patterns Newton 1995; McRoberts et al. 1995; Jablonski would be to reanalyze selectivity within spe- 1996). In fossil marine invertebrates, dispersal cies-poor subgenera, presuming that the latter ability and geographic range appear to be would be more likely to mimic species-level much better predictors of extinction vulnera- patterns. Species richness of veneroid subgen- bility than body size. era across this interval varies from one to 30 (mean ϭ 4.23 Ϯ 4.95) and shows no correla- Preferential Recovery According to Size ϭ ϭ tion with size (r25 0.09; p 0.68). When the The K/T, mid-E, and E/O recoveries are all selectivity analyses were redone for species- significantly biased with respect to veneroid poor taxa (defined as subgenera containing size. Early recovery intervals after mass ex- fewer than the mean number of species), the tinctions are sometimes characterized by ‘‘di- only result that changed was the K/T recov- saster’’ taxa, abundant species with unusually ery. The recovery was still biased toward small body sizes. This pattern, termed the small subgenera, but the bias was no longer ‘‘Lilliput’’ phenomenon (Erwin 1998), has ϭ ϭ statistically significant (Cgeo t7,25 1.24, p been documented for paleocommunities im- 0.22), in large part because of a decrease in mediately following the (Kaljo sample size. 1996), (Kaljo 1996), end- Phylogenetic bias could produce these (Gobbett 1973), end- (Harries shifts in size, if the K/T and Eocene recoveries 1993), and K/T (Ha˚kansson and Thomsen represented radiations of single clades of 1999) events. The reduction in size is generally small and large veneroids, respectively. Direct short-lived and restricted to a handful of op- examination of phylogenetic bias requires a portunistic taxa. The protracted nature of the well-resolved phylogeny (Harvey and Pagel veneroid size decrease and the fact that the 1991), which is currently unavailable for ve- subgenera responsible do not appear to be op- neroids. As an alternative, I tested for the ef- portunists or ecological generalists makes it fects of taxonomic sorting by comparing pat- unlikely that the patterns documented in this terns within the three superfamilies examined study are an example of the ‘‘Lilliput’’ phe- in this study. When I reexamined extinction nomenon. In contrast to the K/T, the Eocene selectivity and preferential recovery within recovery intervals are biased toward larger ve- each of the three superfamilies, I found iden- neroids. Few authors have explored body size tical patterns of preferential recovery in each, patterns across the E/O transition, although although differences between survivors and Hickman (2003) did document an increase in new taxa were not always statistically signif- the size of chemoautotrophic thyasirid bi- icant owing to a reduction in sample size. valves from the Pacific Northwest. When I plotted mean size through time for each superfamily, I also found very similar Why Do Changes in Veneroid Size Occur patterns. The gradual decrease in size in the Throughout This Interval? Late Cretaceous (i.e., before the K/T extinc- Body size in veneroids shows a very clear tion) is driven by arcticoid subgenera, but the pattern of decrease associated with the K/T K/T through Oligocene patterns are almost recovery and minor increase associated with identical in the three superfamilies. This in- the Eocene recoveries. The K/T recovery ap- 586 ROWAN LOCKWOOD pears to reinforce and even accelerate a trend nozoic has improved dramatically during the toward smaller size already established by the past decade and the reader is referred to re- Late Cretaceous. Several factors may be con- cent compilations for additional information tributing to the patterns documented in this (Aubry et al. 1998; Prothero et al. 2003; Wing study and are considered below. et al. 2003). The Late Cretaceous and early Ce- Predation. Large size in bivalves is some- nozoic were, very generally speaking, domi- times considered a refuge against predation nated by warm , which culminated in (Boulding 1984; Vermeij 1987). If predation the Paleocene-Eocene Thermal Maximum pressure is influencing these patterns, then the (PETM), widely recognized as one of the most decrease in veneroid size throughout the Late rapid intervals (Ͻ200,000 years) of extreme Cretaceous should coincide with a decrease in warming in the (Bains et al. 1999; predation and the increase in veneroid size Zachos et al. 2001). The middle Eocene marks across the Eocene events should coincide with the transition from ‘‘greenhouse’’ to ‘‘ice- an increase in predation. Kelley and Hansen’s house’’ conditions, with gradual cooling be- (1996) data on gastropod drilling from the late ginning at approximately 50 Ma (Zachos et al. to early Cenozoic of the coastal 1994). Temperature shifts do tend to track plain allow me to test this hypothesis, albeit changes in veneroid size (Fig. 5) across this in- only for gastropod predators. Their data doc- terval, but the timing is somewhat problem- ument an increase in gastropod predation im- atic. Maximum warming during this interval mediately after the K/T extinction and a (PETM) occurs at approximately 55 Ma, ten slightly smaller increase across the E/O event. million years after the decrease in veneroid Whereas the Eocene data fit the prediction, the size associated with the K/T recovery begins. Late Cretaceous patterns are completely con- Similarly (but perhaps not as troubling), a mi- trary, suggesting that gastropod predation is nor lag exists between the onset of ‘‘icehouse’’ unlikely to be driving this pattern. cooling at approximately 37 Ma and the in- Climate Change. Size is commonly thought crease in veneroid size associated with the Eo- to vary with temperature in modern bivalves cene recoveries (33.7 Ma). It is interesting to and latitude is often used as a proxy for tem- note that the increase in veneroid size does ap- perature when this variation is examined in- pear to coincide with an increase in season- terspecifically. Perhaps the most extensive ality (Ivany et al. 2003b). data set available for modern bivalves has Changes in Productivity. Nutrient availabil- been compiled by Roy and others for Eastern ity and primary productivity are thought to Pacific taxa (Roy et al. 1998, 2000, 2002; Roy scale positively with body size in modern ma- and Martien 2001). Extensive analyses reveal rine invertebrates (Jones et al. 1989; Allmon et no straightforward, linear relationship be- al. 1992; Palmer 1992). If trends in veneroid tween mean size and latitude, although a pos- size are linked to productivity, I would expect itive (nonsignificant) correlation between to see a steady decline in productivity during body size and latitude does exist in several the Late Cretaceous, a drop in productivity temperate marine bivalve lineages. If that is across the K/T boundary, little change in the the case, then given the extratropical distri- early , then an increase across the bution of the data compiled in this study, tem- E/O boundary. perature increases in the early Cenozoic and The Late Cretaceous is characterized by nor- decreases across the E/O transition could ac- mal levels of productivity until the K/T count for the pattern documented in this boundary event (D’Hondt et al. 1998). Several study. This possibility is further supported by authors have documented a breakdown in the the preferential extinction of warm-water taxa C13 gradient immediately after the K/T bolide at the E/O transition (Hickman 1980; Hansen impact, which has been interpreted as a sud- 1987; see papers in Prothero and Berggren den decrease in productivity (Hsu¨ 1986; Za- 1992 and in Prothero et al. 2003). chos and Arthur 1986). A shift in C13 ratios is Our understanding of temperature changes also recorded across the PETM (Katz et al. throughout the late Mesozoic and early Ce- 1999, among others), which may reflect ele- BODY SIZE, EXTINCTIONS, AND VENEROIDS 587 vated global primary productivity (Bains et al. selective extinction across any of these events; 2000); however, neither the microfossil record however, all three showed biased recovery nor modeling of barite accumulation supports patterns. Subgenera that originated during this hypothesis for the open ocean (Kelly et al. the K/T recovery were significantly smaller 1996; Thomas 1998; Bralower 2002; Dickens et than subgenera that survived the extinction. al. 2003). The late Eocene climate changes de- In contrast, new taxa were actually larger than scribed in the previous section are tied to an survivors across the mid-E and E/O events. increase in upwelling and oceanic productiv- Trends in veneroid size through time indicate ity (Thomas and Gooday 1996; Diester-Haass that the K/T recovery accelerated an estab- and Zahn 2001). Global productivity was low lished trend toward decreasing size, whereas until the earliest Oligocene, when an abrupt the mid-E and E/O initiated a short-lived ␦13C excursion, signaling a two- to threefold trend toward larger size. These patterns are increase in productivity, occurred (Diester- unlikely to be the result of sampling, preser- Haass and Zachos 2003). Changes in produc- vation, or phylogenetic bias. Three alternative tivity seem to parallel some, but not all, of the explanations, predation, temperature change, shifts in veneroid size (Fig. 5) across this in- and changes in productivity, were considered. terval. The decrease in size associated with the It is important to note that the effects of these K/T recovery coincides with the decline in three events are tied not to the extinctions productivity, although the former actually be- themselves, but to the recoveries that follow. gins before and continues long after the latter. If productivity actually increases in shallow Acknowledgments marine environments across the PETM, this This manuscript and the research described presents a problem for this hypothesis, as ve- herein have greatly benefited from the feed- neroid size continues to decrease at this time. back of G. Hunt, M. Foote, P. Wagner, J. Swad- The increase, then stabilization, of veneroid dle, D. Jablonski, M. LaBarbera, B. Chernoff, size across the E/O boundary matches well M. Aberhan, S. Kolbe, and K. Roy. Access to with changes in productivity. I am unaware of museum collections and field sites was gen- ecomorphological and evolutionary trends in erously provided by L. Wingard, T. Waller, W. other macrofossil clades that have been di- Allmon, L. Saul, J. Todd, A. Rage, P. Lozouet, rectly tied to primary productivity during this F. Wesselingh, A. Dhondt, A. Rindsberg, and interval, although Smith and Jeffery (1998) the Geological Survey of Alabama. This work suggest that a decrease in echinoid was supported in part by the American As- size may be due to unpredictable nutrient sociation of University Women, Sigma Xi, the supply across the K/T boundary. In addition, Paleontological Society, Paleontological Re- Allmon (2003) noted that filter-feeding turri- search Institution, the Lerner-Gray Fund for tellid species tend to radiate across the E/O Marine Research, and the Dinamation Inter- boundary coincident with productivity in- national Society and was carried out primarily crease. at the University of Chicago. Given the data currently available, none of the three hypotheses considered provide a Literature Cited consistent explanation for these trends in ve- Allmon, W. D. 2003. Boundaries, turnover, and the causes of evo- neroid size. It is entirely likely that multiple lutionary change: a perspective from the Cenozoic. Pp. 511– factors are acting in concert to produce these 521 in Prothero et al. 2003. Allmon, W. D., D. S. Jones, and N. Vaughn. 1992. Observations trends and that different clades of veneroids on the biology of Turritella Valenciennes from the are responding to different pressures. Gulf of California. 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