BULLETIN OF MARINE SCIENCE. 89(4):905–919. 2013
http://dx.doi.org/10.5343/bms.2012.1058
905Bulletin of Marine Science
© 2013 Rosenstiel School of Marine & Atmospheric Science of 
the University of Miami
DRILLING INTENSITY VARIES AMONG NEOGENE 
TROPICAL AMERICAN BIVALVIA IN RELATION 
TO SHELL FORM AND LIFE HABIT
Jill S Leonard-Pingel and Jeremy BC Jackson
ABSTRACT
We calculated the incidence of drilling on bivalve genera from the Neogene fossil 
record of Panama and Costa Rica to determine differences in predation intensity 
among groups based on shell architecture, life habit, mobility, and taxonomic 
affinity. Bulk samples from 28 localities yielded >106,000 bivalve specimens, which 
were examined for characteristic drilling traces of muricid and naticid gastropods. 
We calculated the drilling intensity for the 90 most common genera, and 
characterized the size, ornament, life habit, and mobility for each genus. Large size 
confers considerable protection from drilling, but shell ornamentation does not. 
Life habit is strongly linked with drilling intensity. Epifaunal bivalves experience 
higher predation than infaunal bivalves and shallow burrowers experience higher 
drilling than deep burrowers. Mobility is also important for epifaunal bivalves; 
cemented taxa are twice as likely to be drilled as their uncemented counterparts. 
Our results suggest that bivalve behavior and life habits are more important than 
shell architecture for defense against drilling predators.
Interactions between predators and prey have long been recognized as major driv-
ers of community evolution and diversification (Darwin 1859, Dawkins and Krebs 
1979, Vermeij 1977, 1983, Bambach 1983, Steneck 1983, Roy 1996, Thompson 1998). 
In the marine realm, escalation, or enemy-driven evolution (Vermeij 1987, 1994), ap-
pears to occur more often than does coevolution, or reciprocal evolution (Vermeij 
1994, Kelley and Hansen 2001, Dietl and Kelley 2002). The response of molluscan 
prey to shell-damaging (durophagous) predators is particularly well suited to mac-
roevolutionary studies of predation because of the abundant fossil record of mol-
lusks and the potential for preservation of direct evidence of predation, especially 
traces such as drill holes and repair scars (Kowalewski 2002 and references therein, 
Alexander and Dietl 2003, Kelley and Hansen 2003). 
Several traits related to shell architecture and life habit are hypothesized to 
confer protection against predators (Vermeij 1977, 1983, Bambach 1983, Stanley 
1988, Alexander and Dietl 2003, Kelley and Hansen 2003). Among bivalves, thick, 
robust shells and ornamentation such as spines, knobs, and crenulations of valve 
margins are thought to reduce the probability of a fatal attack by crushing or 
drilling predators (Stanley 1970, Logan 1974, Vermeij 1978, 1983, Bertness and 
Cunningham 1981, Kelley 1989, Harper and Skelton 1993, Smith and Jennings 
2000, Kelley and Hansen 2001, Alexander and Dietl 2003). Organic rich laminae 
within bivalve shells (conchiolin) also appear to inhibit drilling and shell break-
age (Harper and Skelton 1993, Kardon 1998). Rapid burrowing and the ability of 
some bivalves to swim by jet propulsion are also interpreted as adaptations to 
reduce predation. Epifaunal bivalves cemented to a hard substrate may be more 
difficult for predators to manipulate (Harper 1991). Still other bivalves may escape 
BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013906
predation by boring into hard substrates, nestling (occupying crevices or holes 
abandoned by other organisms), burrowing deeply into the sediment, or camou-
flaging themselves with sponges or other encrusting organisms (Stanley 1970, 
Vermeij 1983, Harper and Skelton 1993, Alexander and Dietl 2003). 
These interpretations are compromised, however, because they are based large-
ly upon experimental manipulations of bivalve shells and predators (Harper 1991, 
Smith and Jennings 2000) or are anecdotal. To address these problems, we used a 
large quantitative data set of fossil bivalve assemblages to calculate drilling inten-
sities for 90 common genera in the context of data on shell architecture and life 
mode for the same specimens. Specifically, we tested the hypothesis that bivalves 
with smaller, less ornamented shells should experience higher predation than their 
larger, more highly ornamented counterparts. Secondly, we tested the hypothesis 
that bivalves that can move freely by deep/rapid burrowing or swimming should be 
drilled less often than bivalves that are epifaunal, cemented, or have otherwise re-
duced mobility.
Methods
We collected a total of 176 bulk samples from 28 fossil localities termed faunules (O’Dea 
et al. 2007, Smith and Jackson 2009, Leonard-Pingel et al. 2012) from four basins in north-
ern Panama and eastern Costa Rica (11–0.007 My; Fig. 1, Table 1). All collection locali-
ties are interpreted to represent typical nearshore paleoenvironments and samples come 
from similar lithologic composition (a blue-gray sandy siltstone). In addition, all samples 
Figure 1. Map of Panama and eastern Costa Rica, with insets showing the four basins from which 
collections were taken; Limon Basin, Costa Rica; Bocas del Toro Basin, Panama; Panama Canal 
Zone, Panama; and Darien Basin, Panama. Numbers correspond to faunules listed in Table 1.
Leonard-PingeL and Jackson: differentiaL Predation rates among bivaLves 907
collected came from an inferred paleodepth of ≤100 m. However, the faunules are inter-
preted to represent a range of paleoenvironments from soft-sediment/sandy bottom sub-
strates to reef and seagrass beds based on sediment composition and faunal assemblages 
(O’Dea et al. 2007, Johnson et al. 2007, Leonard-Pingel et al. 2012; see Table 2). We recog-
nize the possibility for habitat patchiness to influence predation, but expect overall trends 
to hold (sensu Sawyer and Zuschin 2010). 
Bulk samples were processed and washed on a 2-mm sieve to remove fossil material 
from the rock matrix and fossils were sorted into gross taxonomic groups. More than 
106,000 identifiable bivalves with a hinge and umbo (see Gilinsky and Bennington 1994) 
were sorted, counted, and identified to genus following Todd (2001). Total valve counts 
were then halved to obtain the number of bivalve individuals. Valves were examined for 
the presence of distinctive drilling traces left by predatory gastropods (see Kitchell et al. 
1981, Vermeij 1987, Kelley et al. 2001, Leighton 2002, Walker 2007). We did not remove 
fragmented individuals from the analysis because most individuals were intact with the 
majority of fragmentation along the edges. With the exception of edge-drilling, which we 
did not observe in our samples, most drilling on bivalve prey occurs near the central or 
Table 1. List of faunules including median age, number of bulk samples analyzed, and the number of identifiable 
bivalve valves sorted and counted. Numbers correspond to localities shown in Figure 1. Ages from O’Dea et al. 
(2007), Leonard-Pingel et al. (2012), and Fredston-Hermann et al. (2013).
Faunule 
Median age 
(Ma)
No. of 
samples
No. of 
bivalve shells Longitude Latitude
Lennond   (1) 0.007 10 1,292 −82.266350 9.354883
Swan Cay  (2) 1.400 11 1,327 −82.299414 9.453347
Empalme  (3) 1.600 6 3,646 −83.061250 9.985583
Upper Lomas (4) 1.600 21 14,793 −83.036720 9.991950
Wild Cane Reef (5) 2.050 7 278 −82.167983 9.349978
Wild Cane Key  (6) 2.050 4 331 −82.168700 9.351047
Ground Creek Porites  (7) 2.050 9 2,119 −82.304567 9.416992
Ground Creek Mud  (8) 2.050 6 24,476 −82.301983 9.407367
Fish Hole  (9) 2.600 4 329 −82.110838 9.318311
Bomba  (10) 3.050 10 2,339 −83.066306 9.913861
Quebrada Chocolate  (11) 3.100 1 8,438 −83.084728 9.973608
Quitaria (12) 3.500 1 478 −83.085750 9.910228
Cayo Agua: Punta Níspero West  (13) 3.550 3 989 −82.031914 9.168555
Cayo Agua: Punta Tiburón–Punta Piedra 
(14)
3.550 4 998 −82.023775 9.151892
Río Vizcaya  (15) 3.550 3 1,651 −83.069381 9.880608
Santa Rita (16) 3.550 6 802 −83.129910 9.970380
Isla Solarte  (17) 3.550 3 2,626 −82.218714 9.333214
Cayo Agua: Punta Níspero South  (18) 3.550 3 1,922 −82.030579 9.167275
Isla Popa (19) 4.250 6 11,067 −82.107000 9.214520
Cayo Agua: Punta Norte West  (20) 4.250 9 3,887 −82.053814 9.178117
Cayo Agua: Punta Piedra Roja West  (21) 4.250 10 10,616 −82.016778 9.139444
Cayo Agua: Punta Norte East  (22) 4.250 7 1,493 −82.042417 9.174883
Río Chico N17  (23) 6.350 4 5,030 −77.531889 8.257639
Río Tupisa (24) 6.350 3 1,103 −77.610417 8.308611
Río Indio  (25) 6.950 11 601 −80.241389 9.179083
Mattress Factory (26) 9.000 2 1,388 −79.830930 9.360060
Isla Payardi  (27) 9.600 9 3,184 −79.821389 9.382722
Sand Dollar Hill  (28) 11.000 3 1,551 −79.810472 9.351500
Total 176 108,754
BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013908
umbonal regions of the shell (Kelley 1988, Kingsley-Smith et al. 2003, Dietl et al. 2004, 
Kowalewski 2004); therefore, we believe that our use of incomplete and fragmented in-
dividuals had minimal impact on our calculations. Initially, we distinguished between 
naticid and muricid drill holes, but because of vagaries in preservation and in the mani-
festation of drill holes among different shell types (Kowalewski 1993, Kelley and Hansen 
2003), we only considered whether a valve had been drilled or not, and not the predator’s 
taxonomic affinity. 
We pooled bivalve genera across all samples and time, and calculated the drilling in-
tensity for every bivalve genus with >25 valves by tallying the number of valves display-
ing at least one drilling trace, and dividing that by the number of individuals of that 
genus (Kowalewski 2002). The size (small or large based on average adult length found 
in the literature), ornamentation (low, moderate, high), depth of burial (epifaunal, semi-
infaunal, surface infaunal, shallow infaunal, deep infaunal), and mobility (cemented, bys-
sally attached, free living, or variable) were determined for each bivalve genus using the 
Neogene Marine Biota of Tropical America molluscan life habits database (Todd 2001; 
see Appendix 1).
Each variable related to shell architecture or life habit was examined in relation to drill-
ing intensity. Pearson’s chi-squared tests were used to test for significant differences in 
relative abundance of drilled and undrilled valves for different shell sizes, among different 
levels of shell ornamentation, and among different life habits and mobility. To test how 
habitat influenced drilling trends, we subdivided the faunules into either biogenic (reef 
or seagrass, see Table 2) or soft-sediment habitats, and analyzed the bivalves from those 
two habitats for each of the variables listed above. Because multiple chi-squared tests were 
performed, a stringent Bonferroni correction was applied; all values reported as significant 
are significant at an alpha of P < 0.0017. 
For the analyses of shell size and predation frequency, genera were grouped as small (<10 
mm) or large (>10 mm) based on average adult lengths (see Appendix 1). The median drill-
ing percentage for each abundant bivalve family (Pectinidae, Cardidae, Arcidae, Veneridae, 
Crassinellidae, Osteridae, Glycymeridae, Lucinidae, Corbulidae) was calculated for each 
faunule. These percentages were compared using a Kruskal-Wallis ANOVA. 
Results
Results indicate that size has a significant impact on drilling incidence among 
all bivalve genera. Small bivalves (those with an adult length <10 mm) were drilled 
nearly twice as often as larger bivalves (Fig. 2A, Table 3; χ2 = 875.39, P < 0.0001, df 
= 1). This pattern generally holds within families as well; the percentage of drilled 
small venerids is slightly higher than that of larger venerids, without Bonferroni 
correction this would be a significant difference, but with the stringent Bonferroni 
it is not significant (Fig. 2B, Table 3; χ2 = 8.80, P = 0.0030, df = 1). However, the 
incidence of drilling upon small lucinids is more than double their larger counter-
parts (Fig. 2C, Table 3; χ2 = 135.19, P < 0.0001, df = 1). 
Drilling percentage differs significantly among all bivalves with low, moder-
ate, or high ornamentation in unexpected ways (Fig. 3A, Table 3). Bivalves with 
moderate ornamentation experience significantly higher drilling than do bivalves 
with low (χ2 = 656.87, P < 0.0001, df = 1) or high (χ2 = 461.08, P < 0.0001, df = 1) 
ornamentation. When only epifaunal bivalves are considered, bivalves with low 
ornament have drilling percentages significantly lower than both moderate (χ2 
= 38.00, P < 0.0001, df = 1) and high (χ2 = 36.20, P < 0.0001, df = 1) ornament 
groups; moderate and high ornament groups do not show a significant difference 
Leonard-PingeL and Jackson: differentiaL Predation rates among bivaLves 909
in drilling percentages within the epifaunal group (χ2 = 2.19, P = 0.1392, df = 1) 
(Fig. 3B, Table 3). 
Relationship to the substrate strongly influences susceptibility of bivalves to 
predation. Predation intensity is twice as high for epifaunal bivalves as for in-
faunal bivalves (Fig. 4A, Table 3, χ2 = 362.70, P < 0.0001, df = 1). Corbulids and 
scallops were removed for this analysis because of their distinctive life habits that 
obscure the general pattern. Corbulids were excluded because of their anomalous, 
quasi semi-infaunal life habit (byssal attachment to sediment grains at or just 
below the sediment surface) and their overwhelmingly high abundance in most 
samples. Scallops were excluded because of their unique ability to move freely or 
swim. 
Table 2. Age, inferred paleoenvironment, and environmental data for each faunule. Paleodepths were inferred 
from either benthic foraminifera or coral assemblages, mean annual range in temperature (MART) was inferred 
from bryozoan zooid size (O’Dea and Okamura 2000, O’Dea and Jackson 2009). Percent carbonate and mud 
come from analysis of the sediment, and percent coral shows what percent of the skeletal fossil assemblage was 
coral. For more information see O’Dea et al. (2007) and Leonard-Pingel et al. (2012).
Faunule
Age
(Ma)
Inferred 
paleoenvironment
Depth
(m)
MART
(°C)
Carbonate 
(%)
Mud 
(%)
Coral 
(%)
Lennond 0.007 Mixed reef and seagrass 15.0 3.80 85.18 39.03 94.98
Swan Cay 1.400 Reef 100.0 3.22 63.49 20.90 15.74
Empalme 1.600 Reef 20.0 2.82 43.43 32.55 3.45
Upper Lomas 1.600 Reef 75.0 2.82 43.28 21.33 35.70
Wild Cane Reef 2.050 Reef 25.0 4.19 56.40 28.29 67.05
Wild Cane Key 2.050 Mixed reef and seagrass 30.0 4.19 45.76 33.11 52.62
Ground Creek (Porites) 2.050 Reef 10.0 4.19 51.41 53.01 93.79
Ground Creek (seagrass) 2.050 Seagrass 10.0 4.19 29.60 30.78 9.45
Fish Hole 2.600 Mixed reef and seagrass 88.0 2.36 19.55 59.34 34.64
Bomba 3.050 Soft sediment 30.0 3.13 68.96 29.78 1.65
Quebrada Chocolate 3.100 Reef 25.0 3.13 31.98 17.22 0.17
Quitaria 3.500 Soft sediment 30.0 3.13 20.83 20.19 2.67
Cayo Agua: Punta 
Níspero West
3.550 Soft sediment 60.0 7.23 26.10 33.85 1.56
Cayo Agua: Punta 
Tiburón
3.550 Seagrass 60.0 5.68 32.01 30.14 25.02
Rio Vizcaya 3.550 Soft sediment 12.0 3.13 31.66 15.47 0.19
Santa Rita 3.550 Soft sediment 30.0 5.73 44.40 28.88 5.86
Isla Solarte 3.550 Soft sediment 75.0 6.68 54.10 14.79 3.28
Cayo Agua: Punta 
Níspero South
3.550 Seagrass 60.0 7.23 26.10 15.34 3.00
Isla Popa 4.250 Soft sediment 50.0 6.65 19.77 56.69 0.02
Cayo Agua: Punta 
Norte West
4.250 Seagrass 30.0 6.25 15.93 42.59 8.08
Cayo Agua: Punta 
Piedra Roja West
4.250 Seagrass 42.0 3.52 27.73 18.72 17.32
Cayo Agua: Punta 
Norte East
4.250 Soft sediment 60.0 4.11 18.87 49.57 1.60
Rio Chico N17 6.350 Soft sediment 30.0 8.67 20.11 36.02 0.00
Rio Tupisa 6.350 Soft sediment 100.0 6.65 15.28 41.20 0.00
Rio Indio 6.950 Soft sediment 25.0 6.77 9.76 12.13 0.09
Mattress Factory 9.000 Soft sediment 28.0 6.18 24.55 35.30 0.25
Isla Payardi 9.600 Soft sediment 27.5 6.18 25.73 47.90 0.00
Sand Dollar Hill 11.000 Soft sediment 27.5 6.18 20.24 8.60 0.43
BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013910
Analysis of drilling and life habit showed that infaunal bivalves with the ability 
to burrow deeply into the sediment experience significantly less drilling than do 
bivalves that are shallow burrowers (Fig. 4B, Table 3, χ2 = 2017.77, P < 0.0001, df = 
1). Similarly, uncemented epifaunal bivalves are drilled half as often as cemented 
epifaunal bivalves (Fig. 4C, Table 3; including scallops: χ2 = 330.43, P < 0.0001, df 
= 1; excluding scallops: χ2 = 48.37, P < 0.0001, df = 1).
These patterns hold when controlling for environment, with two notable excep-
tions (Table 4). Drilling percentages for infaunal and epifaunal bivalves are not 
significantly different in biogenic habitats (18.58% and 17.87%, respectively; χ2 = 
1.13, P = 0.2869, df = 1). Additionally, uncemented epifaunal bivalves excluding 
scallops are less frequently drilled than cemented taxa, but the differences are not 
significant under the selected Bonferroni correction (χ2 = 7.35, P = 0.0067, df = 1).
Taxonomic affinity also influences susceptibility to predation. Drilling percent-
ages differ significantly among abundant bivalve families (Fig. 5; Kruskal-Wallis 
test: χ2 = 74.01, P < 0.0001, df = 8). Pectinidae (scallops) experience the lowest inci-
dence of drilling with a median drilling percentage of only 0.87%. Several families 
with different life habits and shell architecture experience similar intermediate 
levels of drilling (Fig. 5). Families experiencing highest overall drilling intensity 
are Lucinidae (17.4%) and Corbulidae (21.7%). Corbulids are small and live just 
beneath the sediment surface. Lucinids are more variable in size and have well de-
veloped siphons that allow larger individuals to live well below the sediment sur-
face. The high drilling percentage of lucinids reflects the predominance of small 
specimens and taxa in our data set.
Discussion
Large size confers a significant refuge from predation. Smaller bivalves experience 
higher drilling intensities than larger bivalves (Fig. 2). In particular, larger infauna 
are able to burrow more deeply than smaller infauna (Stanley 1970), and are more 
difficult for naticid gastropods to manipulate for drilling (Kelley and Hansen 2003 
and references therein). 
Figure 2. Difference in drilling intensity between large and small bivalves. n indicates the number 
of individual valves. (A) Average drilling intensity of all small bivalves is significantly higher 
than that of large bivalves (χ2 = 875.39, P < 0.0001, df = 1). (B) Small venerids experience higher 
drilling than do large venerids (χ2 = 8.80, P = 0.0030, df = 1). (C) Small lucinids experience sig-
nificantly higher drilling than do large lucinids (χ2 = 135.19, P < 0.0001, df = 1). 
Leonard-PingeL and Jackson: differentiaL Predation rates among bivaLves 911
Extensive ornamentation was a surprisingly ineffective deterrent to drilling pre-
dation, although it may be effective against other predators (Logan 1974, Bertness 
and Cunningham 1981, Vermeij 1987). Among all bivalve life habits, moderate to 
high ornamentation appears to confer little or no protection against drilling. This 
is consistent with the hypothesis that surface ornament in infaunal bivalves is more 
closely related to burrowing (Stanley 1970). High ornamentation also does not ap-
pear to deter drilling predation in epifaunal bivalves. Low incidence of predation 
on epifaunal bivalves with little ornamentation is almost certainly due to their mo-
bility. Highly ornamented epifaunal bivalves do not appear to enjoy any additional 
protection from drilling predators than their moderately ornamented counterparts. 
Thus, our results are consistent with experimental studies that suggest the role of 
Table 3. Table of percent drilling and P-values for comparisons between different shell architecture 
characteristics, life habits, and mobility of all bivalves. All statistical comparisons were made 
using Pearson’s chi-square test.
Comparison Percent drilled P-values
Large bivalves 16.08 P < 0.0001Small bivalves 27.27
Large venerids 18.99 P = 0.0030Small venerids 23.15
Large lucinids 19.35 P < 0.0001Small lucinids 48.04
All bivalves
Low ornament 10.23 P < 0.0001Moderate ornament 26.50
Low ornament 10.23 P < 0.0001High ornament 17.74
Moderate ornament 26.50 P < 0.0001High ornament 17.74
Epifaunal bivalves
Low ornament 5.01 P < 0.0001Moderate ornamnet 15.37
Low ornament 5.01 P < 0.0001High ornament 13.26
Moderate ornament 15.37 P = 0.1392High ornament 13.26
Infaunal bivalves 8.19 P < 0.0001Epifaunal bivalves 26.70
Deep infauna 8.19 P < 0.0001Shallow infauna 26.77
Uncemented epifauna (with scallops) 6.88 P < 0.0001Cemented epifauna 19.76
Uncemented epifauna (no scallops) 12.75 P < 0.0001Cemented epifauna 19.76
BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013912
ornament in reducing predation is ambiguous (Carter 1968, Logan 1974, Vance 1978, 
Feifarek 1987, Harper and Skelton 1993).
Life habit is a very important determinant of bivalve susceptibility to drilling 
predation. Deep burrowers are drilled less often than shallow burrowers and sur-
face-dwelling infauna. This protection appears to extend even to burrowing naticid 
predators. Scallops that can swim away from predators experience much lower in-
cidence of predation than any other epifaunal or infaunal bivalves in our sample. 
In contrast, cemented epifaunal bivalves suffer much higher predation. This may 
reflect two factors. First, cementation, which acts as a deterrent to some predators 
(Harper and Skelton 1993, Alexander and Dietl 2003), may not deter drilling gastro-
pods, especially muricid gastropods, which do not manipulate their prey  (Harper 
Figure 3. Drilling intensities for bivalve genera with low, moderate, and high shell ornamentation. 
n indicates the number of individual valves. (A) For all life habits, bivalves with moderate orna-
ment experience significantly higher drilling intensities than do bivalves with low (χ2 = 656.87, P 
< 0.0001, df = 1) or high (χ2 = 461.08, P < 0.0001, df = 1) ornamentation and bivalves with high 
ornamentation experience a higher average drilling intensity than bivalves with low ornament (χ2 
= 186.43, P < 0.0001, df = 1). (B) Within the epifaunal life habit, bivalves with low ornamentation 
experience significantly lower drilling intensities than bivalves with either moderate (χ2 = 38.00, 
P < 0.0001, df = 1) or high (χ2 = 36.20, P < 0.0001, df = 1) ornamentation. 
Figure 4. Differences in drilling between different life habits and mobilities of bivalves. n indi-
cates the number of individual valves. (A) The percentage of epifaunal bivalves drilled is twice 
that of infaunal bivalves (χ2 = 362.70, P < 0.0001, df = 1). (B) The percentage of surface and 
shallow burrowers drilled is more than three times higher than that of deeply burrowing infaunal 
bivalves (χ2 = 2017.77, P < 0.0001, df = 1). (C) The percentage of drilling in cemented epifaunal 
bivalves is more than twice that of uncemented epifaunal bivalves (χ2 = 330.43, P < 0.0001, df = 1).
Leonard-PingeL and Jackson: differentiaL Predation rates among bivaLves 913
and Skelton 1993, Kelley and Hansen 2003). Second, cemented epifaunal bivalves are 
often found in reef habitats where drilling intensities are significantly higher than 
other habitats (Stanley 1970). Our results are similar to those of Sawyer and Zuschin 
(2010), who also reported that epifaunal bivalves had consistently higher drilling 
frequencies than infaunal bivalves across a variety of nearshore habitats and that 
attached epifaunal bivalves experienced higher drilling frequencies than their reclin-
ing counterparts. The similarity of these results from different times and geographic 
localities lends credence to our assertion that bivalve life habits are of fundamental 
importance in determining their susceptibility to drilling predators.
Bivalve families differ greatly in their overall susceptibility to drilling predators 
in ways that transcend differences in size, ornamentation, and life habit. Differences 
in the incidence of drilling among higher taxa are strikingly clear and make intui-
tive sense because taxonomy reflects many factors at once, including ornamenta-
tion, ecology, and shell microstructure. Scallops (Pectinidae), which have crenulated 
shells and an ability to actively escape predators, are rarely preyed upon by drilling 
gastropods. In contrast, small bivalves that live right beneath the sediment surface, 
such as Corbulidae and most lucinids, exhibit the highest incidence of drilling in our 
study (17.4% and 21.7%, respectively), a pattern that is consistent with other research 
(Kelley and Hansen 1993, 2006). This is likely due to their life habit and typically 
small size. 
Table 4. Table of percent drilling and P-values for comparisons between different shell architecture 
characteristics, life habits, and mobility of bivalves within either biogenic or soft-sediment habitats. 
All statistical comparisons were made using Pearson’s chi-square test.
Biogenic habitats Soft-sediment habitats
Comparison
Percent 
drilled P-values Comparison
Percent 
drilled P-values
Large bivalves 18.63 P < 0.0001 Large bivalves 11.09 P < 0.0001Small bivalves 31.83 Small bivalves 19.62
All bivalves All bivalves
Low ornament 11.56 P < 0.0001 Low ornament 6.88 P < 0.0001Moderate ornament 30.38 Moderate ornament 19.72
Low ornament 11.56 P < 0.0001 Low ornament 6.88 P < 0.0001High ornament 20.23 High ornament 11.74
Moderate ornament 30.38 P < 0.0001 Moderate ornament 19.72 P < 0.0001High ornament 20.23 High ornament 11.74
Infaunal bivalves 18.58 P = 0.2869 Infaunal bivalves 9.75 P < 0.0001Epifaunal bivalves 17.87 Epifaunal bivalves 14.43
Deep infauna 20.25 P < 0.0001 Deep infauna 9.29 P < 0.0001Shallow infauna 31.48 Shallow infauna 19.15
Uncemented epifauna 
(with scallops)
7.54
P < 0.0001
Uncemented epifauna 
(with scallops)
3.76
P < 0.0001
Cemented epifauna 17.20 Cemented epifauna 18.65
Uncemented epifauna 
(no scallops)
14.01
P = 0.0067
Uncemented epifauna 
(no scallops)
6.89
P < 0.0001
Cemented epifauna 17.20 Cemented epifauna 18.65
BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013914
Differences among habitats may also be important in determining predation 
frequency. For example, both Lucinidae and Veneridae are infaunal and similar in 
range of size and ornament, but exhibit strikingly different incidences of predation. 
Lucinids predominate in seagrass habitats where drilling percentages are more than 
double those in unvegetated sandy sediments where venerids are most abundant and 
drilling frequencies are lower (Sawyer and Zuschin 2010). We see some evidence of 
this in the analysis of infaunal vs epifaunal drilling proportions within biogenic habi-
tats, where infaunal bivalves have a statistically indistinguishable drilling percentage 
from epifaunal bivalves. Especially in seagrass beds, small or surface dwelling infau-
nal bivalves experience unusually high predation (Sawyer and Zuschin 2010). 
Higher drilling intensity within seagrass beds also accounts for the higher drill-
ing percentage of uncemented epifauna (not counting scallops) within biogenic en-
vironments. Susceptibility to predation based on habitat may therefore be difficult 
to tease apart from inherent susceptibility based on shell architecture, behavior, and 
taxonomy. However, we believe that the trends described here are generally true for 
bivalves from all habitats.
In conclusion, several functional morphological traits of bivalves are related to 
drilling intensity in ways previously hypothesized, whereas others are not. Shell size, 
life habit, and mobility strongly influence susceptibility of bivalves to drilling preda-
tors, whereas ornamentation does not. Taxonomic affinity integrates the influence 
of different characters and provides a useful signature of susceptibility to predation 
that is intuitive and informative. Nevertheless, variability within families is high (Fig. 
5) due to variations in predation intensity based on environmental influences such 
as habitat type. 
Figure 5. Bivalve genera grouped by taxonomic affinity (families) are significantly different (χ2 = 
74.01, P < 0.0001, df = 8).
Leonard-PingeL and Jackson: differentiaL Predation rates among bivaLves 915
Acknowledgments
We thank F Rodríguez, B de Gracia, and M Ho for their assistance in the laboratory, A 
O’Dea and J Todd for discussion on the subject, and P Kelley, M Kowalewski, L Levin, R 
Norris, and an anonymous reviewer for insightful feedback that greatly improved the quality 
of the manuscript.
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Date Submitted: 1 August, 2012.
Date Accepted: 24 June, 2013.
Available Online: 12 August, 2013.
Addresses: (JSLP) 1: Geoscience Research Division, Scripps Institution of Oceanography, 
La Jolla, California 92093. 2: Department of the Geophysical Sciences, University of 
Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637. (JBCJ) 1: Geoscience Research 
Division, Scripps Institution of Oceanography, La Jolla, California 92093. 2: Department of 
Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, 
DC 20013. 3: Smithsonian Tropical Research Institute, PO Box 0843-03093, Balboa, Panama. 
Corresponding Author: (JSLB) Email: <jleonardpingel@uchicago.edu>. 
BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013918
Appendix 1. The 90 bivalve genera with a least 25 valves in all samples. The table lists the total number of 
valves counted in all samples, the percent of the valves with at least one drill hole, and size, ornament, depth, 
and mobility classifications for each genus.
Genus Family
No. of 
valves
Percent 
drilled Size Ornament Depth Mobility
Anomia Anomiidae 299 5.35 Large High Epifaunal Cemented
Acar Arcidae 162 9.88 Large High Epifaunal Bysally attached
Anadara Arcidae 3,961 12.62 Large High Semi infaunal Bysally attached
Arca Arcidae 296 10.81 Large High Epifaunal Bysally attached
Barbatia Arcidae 827 7.01 Large Moderate Epifaunal Bysally attached
Lunarca Arcidae 36 11.11 Large High Surface infaunal Variable
Americardia Cardiidae 32 12.50 Large High Shallow infaunal Free living
Laevicardium Cardiidae 210 3.81 Large Low Shallow infaunal Free living
Trachycardium Cardiidae 321 1.25 Large High Shallow infaunal Free living
Trigoniocardia Cardiidae 1,548 6.85 Large High Shallow infaunal Free living
Cardites Carditidae 908 19.16 Large High Shallow infaunal Free living
Arcinella Chamidae 254 14.17 Large High Epifaunal Cemented
Chama Chamidae 1,085 26.91 Large High Epifaunal Cemented
Caryocorbula Corbulidae 18,526 35.05 Small Moderate Surface infaunal Bysally attached
Varicorbula Corbulidae 16,997 25.43 Small Moderate Surface infaunal Bysally attached
Crassinella Crassatellidae 878 19.59 Small Moderate Semi infaunal Free living
Eucrassatella Crassatellidae 72 13.89 Large Moderate Semi infaunal Free living
Cardiomya Cuspidariidae 119 3.36 Small Moderate Surface infaunal Free living
Dimya Dimyidae 359 57.94 Large High Epifaunal Cemented
Donax Donacidae 72 0.00 Large Low Deep infaunal Free living
Axinactis Glycymerididae 65 9.23 Large High Semi infaunal Free living
Tucetona Glycymerididae 4,471 25.41 Large High Semi infaunal Free living
Hyotissa Gryphaeidae 253 32.41 Large High Epifaunal Cemented
Isognommon Isognomonidae 77 10.39 Large Low Epifaunal Bysally attached
Temblornia Leptonidae 28 0.00 Small Low Shallow infaunal Variable
Ctenoides Limidae 51 7.84 Large Moderate Epifaunal Bysally attached
Limea Limidae 29 20.69 Small High Epifaunal Free living
Limopsis Limopsodae 486 30.45 Small Moderate Epifaunal Bysally attached
Cavilinga Lucinidae 39 46.15 Large Moderate Deep infaunal Free living
Codakia Lucinidae 45 26.67 Large Moderate Deep infaunal Free living
Lucina Lucinidae 2,134 12.84 Large Moderate Deep infaunal Free living
Myrtea Lucinidae 1,243 28.16 Large Moderate Deep infaunal Free living
Parvilucina Lucinidae 787 50.06 Small Moderate Surface infaunal Free living
Phacoides Lucinidae 208 22.12 Large Moderate Deep infaunal Free living
Radiolucina Lucinidae 106 33.96 Small Moderate Surface infaunal Free living
Mulinia Mactridae 26 7.69 Large Low Deep infaunal Free living
Crenella Mytilidae 119 10.08 Small Moderate Epifaunal Bysally attached
Arcopsis Noetiidae 820 18.54 Large High Epifaunal Bysally attached
Noetia Noetiidae 225 4.44 Large High Semi infaunal Bysally attached
Sheldonella Noetiidae 61 19.67 Large High Shallow infaunal Bysally attached
Adrana Nuculanidae 60 3.33 Large Moderate Surface infaunal Free living
Costelloleda Nuculanidae 102 3.92 Large Moderate Surface infaunal Free living
Propeleda Nuculanidae 27 7.41 Large Moderate Surface infaunal Free living
Saccella Nuculanidae 3,064 10.77 Small Moderate Surface infaunal Free living
Acila Nuculidae 166 2.41 Large Moderate Shallow infaunal Free living
Leonard-PingeL and Jackson: differentiaL Predation rates among bivaLves 919
Appendix 1. Continued.
Genus Family
No. of 
valves
Percent 
drilled Size Ornament Depth Mobility
Nucula Nuculidae 2,688 10.71 Small Low Surface infaunal Free living
Varinucula Nuculidae 128 6.25 Large Moderate Shallow infaunal Free living
Crassostrea Ostreidae 172 4.65 Large High Epifaunal Cemented
Dendostrea Ostreidae 5,151 12.89 Large High Epifaunal Cemented
Ostreola Ostreidae 549 25.87 Large High Epifaunal Cemented
Aequipecten Pectinidae 40 0.00 Large High Epifaunal Bysally attached
Amusium Pectinidae 56 3.57 Large Low Epifaunal Free living
Argopecten Pectinidae 3,765 1.75 Large High Epifaunal Free living
Caribachlamys Pectinidae 49 4.08 Large High Epifaunal Bysally attached
Cyclopecten Pectinidae 612 7.52 Small Low Epifaunal Free living
Flabellipecten Pectinidae 36 0.00 Large High Epifaunal Free living
Leopecten Pectinidae 482 0.83 Large Low Epifaunal Free living
Leptopecten Pectinidae 538 0.37 Large High Epifaunal Bysally attached
Pacipecten Pectinidae 70 22.86 Large High Epifaunal Bysally attached
Spathochlamys Pectinidae 582 1.37 Large High Epifaunal Bysally attached
Plicatula Plicatulidae 753 34.53 Large High Epifaunal Cemented
Spondylus Propeamussiidae 60 13.33 Large High Epifaunal Cemented
Pteria Pteriidae 169 7.10 Large Low Epifaunal Bysally attached
Yoldia Sareptidae 108 11.11 Small Low Semi infaunal Free living
Abra Semelidae 50 4.00 Small Low Surface infaunal Free living
Cumingia Semelidae 61 13.11 Large Low Deep infaunal Free living
Ervilia Semelidae 598 16.72 Small Low Surface infaunal Free living
Semele Semelidae 49 0.00 Large Low Deep infaunal Free living
Tagelus Solecurtidae 1,240 2.26 Large Low Deep infaunal Free living
Angulus Tellinidae 853 6.57 Large Low Deep infaunal Free living
Elpidollina Tellinidae 88 11.36 Large Low Deep infaunal Free living
Eurytellina Tellinidae 536 8.21 Large Moderate Deep infaunal Free living
Merisca Tellinidae 563 2.13 Large Moderate Deep infaunal Free living
Moerella Tellinidae 285 30.88 Small Low Surface infaunal Free living
Strigilla Tellinidae 85 7.06 Large Moderate Deep infaunal Free living
Tellina Tellinidae 332 7.23 Large Low Deep infaunal Free living
Felaniella Ungulinidae 100 18.00 Large Low Deep infaunal Free living
Anomalocardia Veneridae 55 0.00 Large Moderate Deep infaunal Free living
Chione Veneridae 15,317 23.24 Large High Semi infaunal Free living
Chionista Veneridae 36 5.56 Large High Shallow infaunal Free living
Cyclinella Veneridae 92 4.35 Large Low Shallow infaunal Free living
Dosinia Veneridae 117 8.55 Large Moderate Shallow infaunal Free living
Gouldia Veneridae 1,982 23.21 Small Moderate Surface infaunal Free living
Lamelliconcha Veneridae 302 12.58 Large Moderate Shallow infaunal Free living
Lirophora Veneridae 839 10.49 Large High Shallow infaunal Free living
Macrocallista Veneridae 4,405 12.12 Large Low Deep infaunal Free living
Panchione Veneridae 150 20.00 Large High Shallow infaunal Free living
Pitar Veneridae 990 13.13 Large Moderate Shallow infaunal Free living
Ventricolaria Veneridae 73 16.44 Large Moderate Shallow infaunal Free living
Trigonulina Verticordiidae 70 11.43 Small Moderate Surface infaunal Free living