Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111

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Palaeogeography, Palaeoclimatology, Palaeoecology

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The fossil record of drilling on

Adiël A. Klompmaker a,⁎, Roger W. Portell a, Susan E. Lad b,Michał Kowalewski a a Florida Museum of Natural History, University of Florida, 1659 Museum Road, Gainesville, FL 32611, USA b Department of Anthropology, University of Florida, P.O. Box 117305, Gainesville, FL 32611, USA article info abstract

Article history: The fossil record of drilling predation has been studied in detail for a few major invertebrate groups (bivalves, Received 26 November 2014 gastropods, brachiopods, and echinoids), while other prey (e.g., scaphopods, serpulids, decapods, and barnacles) Received in revised form 16 February 2015 have been largely neglected. Herein, we report on drilling predation using an extensive collection of – Accepted 24 February 2015 barnacles (N50,000 specimens). In total, 312 drill holes of predatory origin were found in Eocene– Available online 4 March 2015 Holocene wall and opercular plates of balanomorph and scalpellomorph barnacles. The drilled specimens Keywords: originated from localities in the USA, Jamaica, Panama, The , Belgium, Antarctica, South Africa, Cirripedia Chile, and Venezuela, suggesting that drilling predation on barnacles was a worldwide phenomenon during the Cenozoic. Muricid gastropods are the inferred producers of the majority of the drill holes; two drill holes Octopoda were likely caused by octopods. Drilling frequencies lack major temporal trends and appear low (b10%), consistent Drill hole with observations in modern ecosystems that muricids are facultative drillers and commonly kill barnacles without drilling. Drill holes are placed non-randomly in balanomorph wall plates: they occur preferentially between plates in the interplate region, on and around the rostrum, and in the middle part of shell (height-wise). Drill holes in opercular plates occur preferentially in scuta rather than terga despite a notable taphonomic bias: scuta are preserved more frequently than the less robust terga are (2.22:1 based on a bulk sample). Drill holes in wall plates are commonly incomplete (23.4%), but, as documented for extant prey, successful attacks can be often accomplished via non-penetrative drilling. Also, drill holes are significantly larger in larger barnacles. The results provide limited support for the hypothesis that a reduction in the number of wall plates, tubes within wall plates, and strong external sculpture may have evolved as a result of muricid drilling predation of balanomorphs during the Cenozoic. © 2015 Elsevier B.V. All rights reserved.

1. Introduction drilling predation, although less frequently, include echinoderms (e.g., Kowalewski and Nebelsick, 2003; Złotnik and Ceranka, 2005), The fossil record of predator–prey interactions has been investigated brachiopods (e.g., Leighton, 2003; Kowalewski et al., 2005; Baumiller most extensively using drill holes produced in prey skeletons by drilling et al., 2006; Tyler et al., 2013), and ostracods (e.g., Reyment et al., predators (e.g., Kelley and Hansen, 2003; Huntley and Kowalewski, 1987; Reyment and Elewa, 2003). Prey that have been studied in 2007). These trace fossils, generally referred to as Oichnus ispp. or more detail in recent years are scaphopods (Yochelson et al., 1983; Sedilichnus ispp. (Zonneveld and Gingras, 2014), are easily recognizable, Klompmaker, 2011; Li et al., 2011), annelids (Klompmaker, 2012; fossilize well, have modern counterparts, and are found in shells of a Martinell et al., 2012), (Rojas et al., 2014), and decapod crusta- variety of invertebrates. However, an overwhelming majority of previ- ceans (Pasini and Garassino, 2012; Klompmaker et al., 2013). Most of ous studies centered on drill holes in post- bivalves and gas- these studies are limited in scope being based on specimens from a tropods (e.g., Kowalewski et al., 1998; Kelley and Hansen, 2003; single locality and stratigraphic level (but see Yochelson et al., 1983; Klompmaker, 2009; Chattopadhyay and Dutta, 2013; Mallick et al., Klompmaker et al., 2013). 2014; Paul and Herbert, 2014; Klompmaker and Kelley, 2015,and Drilling predation in molluscs is often attributed to naticid and many more), as these molluscs tend to be common, are relatively muricid gastropods (e.g., Kelley and Hansen, 2003), although other well-preserved compared to other invertebrates, and are easy to predatory drillers are known (e.g., Kowalewski, 2002). Whereas collect. Prey clades that have also received attention with regard to naticids were not reported to drill modern barnacles (Taylor et al., 1980; Barnes, 1999), drilling predation by muricids and octopods on modern barnacles has been documented in numerous studies ⁎ Corresponding author. Tel.: +1 352 273 1939. (e.g., Connell, 1961; Radwin and Wells, 1968; Menge, 1974; Pratt, E-mail addresses: [email protected] (A.A. Klompmaker), portell@flmnh.ufl.edu (R.W. Portell), slad@ufl.edu (S.E. Lad), mkowalewski@flmnh.ufl.edu 1974; Barnett, 1979; Palmer, 1982, 1988, 1990; Perry, 1985; Guerra (M. Kowalewski). and Nixon, 1987; Hart and Palmer, 1987; Nixon and Maconnachie,

http://dx.doi.org/10.1016/j.palaeo.2015.02.035 0031-0182/© 2015 Elsevier B.V. All rights reserved. 96 A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111

1988; Barnes, 1999; Gordillo, 2001; Sanford and Swezey, 2008). In Biodiversity Center were studied. Nearly all drilled balanomorph contrast, few studies have been devoted to drilling predation on barnacles (see Fig. 1 for morphological features of barnacles) had barnacles in the fossil record. To our knowledge, drill holes have only skeletons that included six wall plates, except for UF 245098 (four wall been reported from isolated occurrences of “subfossil” barnacles from plates). The following data were recorded for each specimen that Antarctica (Jonkers, 2000: p. 251); the Pleistocene of Russia (Nielsen contained at least one drill hole of predatory origin: (1) the number of and Funder, 2003: Oichnus paraboloides Bromley, 1981), Jamaica drill holes; (2) the type of drilled plate [i.e., wall (= parietal) plate or (Collins et al., 2009: O. simplex), and Chile (Gordillo, 2013); and from opercular plate (tergum or scutum)]; (3) completeness of the drill the of the USA (Florida) (Klompmaker et al., 2014: O. ovalis hole (complete or incomplete); (4) the specific location of the drill Bromley, 1993)andSpain(Donovan and Novak, 2015: O. simplex hole: a) which of the 12 plate and interplate regions (= overlap zones Bromley, 1981). Lastly, Gale and Sørensen (2015: fig. 4D, 19O; 2014: at plate margins with alae and radii or suture zone) was drilled, fig. 17F) documented the only known gastropod drill holes b) whether the drill hole was located at the base, middle or top part of in Cretaceous barnacles: two drill holes were found in Campanian a plate or interplate region; (5) outer drill hole diameter; (6) the barnacles from Sweden. Our survey of figures in the systematic litera- maximum diameter of an intact barnacle shell measured from the ros- ture on fossil barnacles yields additional examples of specimens that tral to carinal plate; and (7) the height of the drilled plate or interplate contain drill holes of possible predatory origin (De Alessandri, 1906: region (for scuta this was the maximum length). Digital calipers pl. 4.24, Pleistocene of Italy; Zullo and Miller, 1986: fig. 3f, Pleistocene (precision = 0.03 mm) were used for measurements. The relationship of the USA (North Carolina); Davadie, 1963: pl. 34.7, Pliocene of between drill hole size and specimen size was evaluated using reduced Morocco; Carriol and Schneider, 2013: fig. 2, Pliocene of central Chile; major axis regression, a bivariate analysis optimized for assessing two Yamaguchi, 1982: pls. 45.2b, 47.1a, of Japan; Buckeridge, dependent variables with comparable measurement errors. 1983: pl. 4i, Miocene of New Zealand; Zullo, 1992: fig. 15.15, Miocene To assess spatial distribution of drill holes across different regions of of the USA (California); Withers, 1953: pls. 31.4, 42.3, of the barnacle skeleton (i.e., site selectivity or stereotypy), the drilling Hungary). These examples suggest that drilling predation in barnacles frequencies were tallied for each of the 12 wall plate and interplate may have been much more common in the fossil record than reported regions. DF is defined here as the total number of specimens with so far and thus deserve more detailed investigation. The evolutionary at least one drill hole (complete or incomplete) divided by the total history of barnacles as prey is particularly interesting because predation number of specimens (see also discussion). Because those 12 regions pressure by drilling gastropods has been postulated as a cause of vary notably in surface area, we quantified the surface area of each reduction of the number of wall plates in Cenozoic Balanomorpha interplate and plate regions, for three randomly selected, well- (Palmer, 1982). Here we report the results of an extensive study on preserved balanomorph barnacles with six wall plates (UF 250777, this understudied prey of drilling predators based on barnacle collections 250939, and 251028). These specimens were photographed from all from the Cretaceous–Quaternary originating from North and South sides and the area of each plate and interplate region was measured America, Europe, Africa, and Antarctica. We also explore the role of using ImageJ 1.46r. The mean for the areas of the three specimens was drilling predation on morphological evolution of the balanomorph used to estimate average proportional surface area of the six plate and barnacles. six interplate regions. The average surface areas were then used to de- velop an expected frequency of drill holes under the null hypothesis 2. Methods that attack sites were distributed randomly across barnacle plate and interplate regions. A Monte Carlo simulation was used for each of The Cretaceous–Quaternary collections of barnacles in the inverte- the 12 plate and interplate regions to estimate (1) expected drilling brate paleontology collection of the Florida Museum of Natural History frequencies, (2) 95% confidence intervals, and (3) p-values under the (FLMNH-IP) at the University of Florida (UF), consisting mostly of null hypothesis that drill holes were randomly distributed. This simula- barnacles from the southeastern USA and circum-Caribbean, were tion was carried out by assigning 312 drill holes (i.e., the number of drill surveyed for the presence of drill holes of inferred predatory origin. holes observed in the actual data) to 12 regions with probabilities given The cataloged collections contained 47,867 cirriped specimens, domi- by their proportional surface areas. The simulation was repeated 10,000 nated by balanomorphs (N 90%). Additionally, a barnacle specimen times and the resulting frequency distribution was used to compute the with a drill hole from the Pliocene of Langenboom (The Netherlands) estimates listed above. Concurrently, the standard deviation of drill hole deposited in the Oertijdmuseum and a small lot of barnacles from the frequencies across the 12 regions was computed for each iteration and Miocene of Miste (Winterswijk, The Netherlands) stored in the Naturalis the resulting null distribution of standard deviations was compared

Fig. 1. Morphological features of balanomorph barnacles. A. Names of the six wall plates; six interplate regions outlined in yellow. “Left” and “right” are arbitrarily based on the orientation of the barnacle. B. Top view of the placement of opercular plates in a barnacle shell, attached to another barnacle. C. (Right) lateral view of articulated opercular plates. Table 1 Drilling frequency of samples of fossil balanomorph wall plates and opercular plates from multiple localities and stratigraphic intervals. * Some scuta contained partial drill holes at the margin of scuta that were counted as 1/2 in the DF calculation because the other part of the drill hole would be present in the other scutum of that barnacle specimen. ..Kopae ta./Plegorpy aaolmtlg,Pleeooy46(05 95 (2015) 426 Palaeoecology Palaeoclimatology, Palaeogeography, / al. et Klompmaker A.A. Locality Age Stratigraphic Barnacle Total # # specimens % complete # specimens % incomplete Total # drilled Drilling frequency Source unit part specimens with complete drill holes of with incomplete drill holes of specimens (% drilled specimens) drill holes total number drill holes total number of specimens of specimens

Crescent beach 02, early Waccamaw Fm 6 connected 468 13 2.8 5 1.1 18 3.8 Herein (museum NC, USA Pleistocene (Unit 2) wall plates collection) De Soto Shell Pit 05, early Caloosahatchee 6 connected 1090 17 1.6 9 0.8 26 2.4 Herein (museum FL, USA Pleistocene Fm (Portell Bed 7) wall plates collection) Pampa Mejillones 01, ?late Upper unit 6 connected 213 3 1.4 3 1.4 Herein (museum Atacama Desert, Pliocene wall plates collection) Chile Pampa Mejillones 01, ?late Upper unit Opercular 177 (161 scuta; 10 (scuta) 8.7* Herein (museum Atacama Desert, Pliocene plates 16 terga) collection) Chile Quality Aggregates late Tamiami Fm 6 connected 449 12 2.7 5 1.1 17 3.8 Herein (museum Phase 09, FL, USA Pliocene (Pinecrest beds) wall plates collection) SMR Aggregates, FL, late Tamiami Fm 6 connected 115 1 0.9 1 0.9 Herein (bulk USA Pliocene (Pinecrest beds) wall plates sample) SMR Aggregates, FL, late Tamiami Fm Opercular 319 (220 scuta; 4 (scuta) 3.6 Herein (bulk USA Pliocene (Pinecrest beds) plates 99 terga) sample) Chipola 08, FL, USA early Chipola Fm 6 connected 639 3 0.5 1 0.2 4 0.6 Herein (museum Miocene wall plates collection) Stella 01, NC, USA late Silverdale Fm, Opercular 55 (52 scuta; 3 terga) 2 (scuta) 3.8* Herein (museum Oligocene Haywood Landing plates collection) Mbr Whately 01, AL, USA late Yazoo Fm, Cocoa Opercular 252 scuta 3 1.2* Herein (museum Eocene Mbr plates collection) Navarino Island, late “Whole 94 4 4.3 4 4.3 Gordillo (2013) –

southern Chile Pleistocene specimens” 111 Pickett Bay 01, FL, early Intracoastal All visible 365 (individual 1 1 1.6 Klompmaker et al. USA Pliocene Formation wall plates wall plates) (2014) 97 98 A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 against the actual standard deviation observed in the data. Additional Virginia, and Alabama), Jamaica, Panama, Venezuela, Chile, Antarctica, site-selectivity analyses were carried out by comparing combined South Africa, The Netherlands, and Belgium (Fig. 3, Appendix 1). In interplate vs. plate areas and vertical location (top, middle, or base, all terms of stratigraphic range, drill holes of inferred predatory origin are of equal height) of drill holes on plate walls. χ 2 tests were used to eval- found in Eocene, Oligocene, Miocene, Pliocene, Pleistocene, and late uate (1) whether the relative proportion of incomplete drill holes dif- Pleistocene–Recent collections (Figs. 4–6). The drill holes can be classi- fered on plates compared to interplate regions, (2) whether the fied as Oichnus ispp. or Sedilichnus isp.: O. paraboloides (e.g., Figs. 4–6), relative proportion of incomplete drill holes differed from the top to O. simplex (e.g., Fig. 4–6), O. ovalis (e.g., Fig. 7), and Sedilichnus the base of the barnacle, and (3) whether the relative proportion of spongiophilus Müller, 1977 (Fig. 4I), although it was suggested recently drill holes in the interplate area differed from the top to the base of that Oichnus Bromley, 1981 is a junior synonym of Sedilichnus Müller, the barnacle. The Kruskal–Wallis and the subsequent Bonferroni- 1977 (Zonneveld and Gingras, 2014). Here, Rojas et al. (2014) is followed corrected Mann–Whitney tests were used to evaluate whether drill by continuing the use of Oichnus. Drill hole size increases with increasing hole diameters differed from the top to the base of the barnacle and prey size as measured from the maximum diameter of the barnacle whether barnacles differed in size for those drilled at the top, middle, and the plate height when drill holes from all stratigraphic levels and and base. Mann–Whitney tests were used to evaluate (1) drill hole localities are combined regardless of drill hole completeness or when diameters in wall plates vs. those in interplate regions, (2) barnacle complete and incomplete drill holes are analyzed separately (Fig. 8A–F). size for those that are drilled in wall plates vs. those drilled in interplate The same usually applies when a more restricted stratigraphic range is regions, (3) drill hole diameters of complete vs. incomplete drill holes, used (Fig. 8G–I). and (4) barnacle size for specimens with complete vs. incomplete drill The majority of the drill holes in the wall plates of balanomorphs are holes. Given the limited and variable preservation of most collections, located between the plates (56.8%, 155/273) (Fig. 9), despite the fact the low number of specimens per locality for many collections, and that the combined outer surface area of these regions is estimated to the multi-component skeleton of barnacles, no meaningful quantitative represent only ~15.8% of the total surface area (Appendix 2). Palmer assessment of drilling frequencies (DF) was feasible for the entire (1982) also estimated the interplate area represents a small fraction of dataset generated in the survey. However, some of the individual collec- the total area (b15%). Drill holes located between plates are significantly tions included in this survey consisted of reasonably well-preserved more frequent than would be expected if they were distributed specimens (i.e., all wall plates well-preserved, connected, and visible randomly (Table 2). The significant preference for the interplate area or well-preserved opercular plates) and were deemed appropriate for is also observed when the data are restricted to barnacles from the De deriving DF estimates because the specimens were collected randomly Soto Shell Pit 05 locality and include only those specimens that have irrespective of the presence of a drill hole and contained a relatively all six wall plates preserved (Table 2). Half (50.5%, 138/273) of all drill large number of specimens (Table 1). Additionally, the DF was deter- holes in balanomorph barnacles are located on the rostrum and between mined for specimens with all wall plates preserved and articulated for the rostrum and lateral plates on either side of the rostrum (Fig. 9), one in situ bulk sample (~10,750 cm3) collected from Bed 7 above the whereas this area occupies only 28.7% of the periphery of the barnacle. Strombus floridanus Mansfield, 1930 Zone (upper Pliocene Tamiami The preferential drill hole placement in the rostrum area is also observed Formation, Pinecrest beds) at FLMNH-IP SMR Aggregates Phase 10 when the data are restricted to specimens with all six wall plates locality, USA (Florida). This bulk sample was also used to determine preserved and then further restricted to such specimens from the De the preserved relative abundance of terga and scuta. A χ 2 test was Soto Shell Pit 05 locality only (Table 2). The Monte Carlo simulation used to evaluate whether the observed abundance differed significantly indicates that the observed frequency of drill holes across 12 plate from the expected relative abundances if terga and scuta had the same regions is significantly different than expected for randomly distributed probability of preservation. Statistical analyses were performed in attack sites with the exception of the rostrum and the two interplate PAST 2.17 (Hammer et al., 2001) and R 3.0.1 (R Development Team). areas adjacent to the carina yielding p-values N0.05 (Fig. 9). The overall Institutional abbreviations for specimen numbers: UF—University of variation in drill hole frequency across 12 plate regions (standard Florida, Florida Museum of Natural History (Invertebrate Paleontology), deviation = 17.3) is notable and significantly higher than is predicted USA; MAB k—Oertijdmuseum De Groene Poort, The Netherlands; by the Monte Carlo simulation (p = 0.0036; Fig. 10). The relative RGM—Naturalis Biodiversity Center, Leiden, The Netherlands. proportion of incomplete drill holes appears higher for attacks located on plates compared with interplate attacks (plate: 27.6%, 32/116; 3. Results

On the suborder level, drilled specimens are dominated by balanomorphs (97.9%, 286/292 drilled specimens), but six scalpellomorph specimens (=2.1%) also contained a drill hole. On the family level, balanid specimens are drilled most frequently (89.4%, 261/292), followed by (6.8%, 20/292), Scalpellidae (2.1%, 6/292), Pachylasmatidae (1.0%, 3/292), and Pyrgomatidae (0.7%, 2/292). The order-level dominance of balanomorphs and family-level dominance of balanids is expected given that these groups dominate the studied collections. Large barnacle collections typi- cally contained evidence of drilling. Drilling frequencies have been com- puted for subsets of the dataset (Table 1, Fig. 2). Drilling frequencies tend to be lower than 10% for all samples in the museum collections and in the bulk sample. These low drilling frequencies are observed for both wall plate and opercular plate samples. Using the bulk sample, anal- ysis of the relative abundance of terga and scuta yields a ratio of 1:2.22 (n = 329), which is statistically different from the expected 1:1 ratio (χ 2 = 44.8, p b 0.001). Fig. 2. Drilling frequencies in balanomorph barnacles throughout time based on results Drilled barnacles from the surveyed collections represent specimens herein (see Table 1 for details), and single values extracted from Jernakoff and Fairweather with a broad geographic distribution, including the southeastern USA (1985), Gordillo (2013), Archuby and Leighton (2014), and Klompmaker et al. (2014). (Florida, Georgia, South and North Carolina, Maryland, Mississippi, Inset shows the variation of DFs within 0–10%. A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 99

Fig. 3. The location and age of known drill holes of inferred predatory origin in fossil barnacles. Abbreviations: USA: MD = Maryland; VA = Virginia; NC = North Carolina; SC = South Carolina; GA = Georgia; FL = Florida; AL = Alabama; MS = Mississippi; JA = Jamaica. Other countries: PA = Panama; VEN = Venezuela; CHI = Chile; ANT = Antarctica; SW = Sweden; NL = The Netherlands; BE = Belgium; SP = Spain; RUS = Russia; SAF = South Africa.

interplate: 21.9%, 34/155), although this difference is not statistically p = 0.410). The maximum diameter of barnacles also does not differ significant (χ 2 = 1.15, p = 0.56). significantly when comparing specimens with complete drill holes to Most drill holes are located in the middle part of a plate or interplate specimens with incomplete drill holes (Mann–Whitney: p = 0.209). area height-wise (67.4%, 182/270) (Fig. 11A). The percentage of incom- One balanid wall plate from the Miocene Choptank Formation in plete drill holes slightly decreases from the top to the base of the barnacle Maryland (USA) (UF 250786) shows a pronounced thickening on the (Fig. 11B), although these changes are not statistically significant based inside of the shell (Fig. 12). This thickening encapsulates a drill hole on the underlying values (χ 2 = 2.49; p = 0.29). The percentage of (diameter on outer side = 1.2 mm) so that it does not penetrate into drill holes in the interplate area also decreases from the top of the barna- the interior of the barnacle. cle to the base (Fig. 11C), which is statistically significant using the un- derlying values (χ 2 = 9.77; p = 0.008). Drill holes vary significantly in 4. Discussion diameter across top, middle, and base regions of the wall plates (H = 7.46; p = 0.024; Kruskal–Wallis test) (Fig. 11D). Specifically, the 4.1. Likely predators Bonferroni-corrected Mann–Whitney pairwise comparisons tests sug- gest that the diameter of the drill holes differ significantly between the Given the size (0.2–4.6 mm outer diameter) and circular shape of the top and the base regions of the barnacle wall plates (p = 0.023, i.e. drill holes (Figs. 4–6), the overwhelming majority of drill holes can be, drill hole diameters on the top are greater), whereas the other two com- most likely, attributed to muricid gastropods, well-known modern parisons yield non-significant results (middle vs. top: p = 0.174; middle drillers of barnacles (e.g., Connell, 1961; Menge, 1974; Barnett, 1979; vs. base: p = 0.334). Barnacles containing drill holes in the top part of Palmer, 1982, 1988, 1990; Hart and Palmer, 1987; Barnes, 1999; the wall plates appear larger than those with drill holes placed near Sanford and Swezey, 2008). Taylor et al. (1980: table 1) also listed the base (Fig. 11E). Although the Kruskal–Wallis test was non- Buccinidae, Nassariidae, and Fasciolariidae as predators of cirripedes. significant (H = 5.24; p = 0.073), the Bonferroni-corrected Mann– These non-muricid gastropods are unlikely to have produced drill Whitney pairwise comparisons test shows that the median maximum holes in barnacles and barnacles are not considered to be a common diameter of drilled barnacles is larger for specimens with drill holes in prey for these predators. For example, Paine (1963: table 1) listed that the top part compared to those specimens with drill holes near the the non-drilling gastropod Fasciolaria hunteria (Perry, 1811) preyed on base (p = 0.040). The other two comparisons yield non-significant re- a specimen of Chthamalus sp. in the marine waters of Florida. Taylor sults (middle vs. top: p = 0.837; middle vs. base: p = 0.332). (1978) found that 10% of gut contents of the Median drill hole size in wall plates does not differ significantly from Linnaeus, 1758 consisted of (Linnaeus, 1758), whereas those between the plates (Mann–Whitney: p = 0.345). The same barnacles were not eaten by the buccinid Neptunea antiqua (Linnaeus, applies for the maximum diameter of barnacles that are drilled in 1758). Nielsen (1975) found that B. undatum waits until the valves of wall plates vs. those drilled between wall plates (Mann–Whitney: bivalves open after which the lip and proboscis are inserted. No drilling p = 0.523). Drill hole diameter is not significantly different for complete was involved, which may suggest that barnacles are not frequently drill holes and incomplete drill holes in wall plates (Mann–Whitney: drilled either, but are preyed upon by a different method. Furthermore, 100 A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111

Barnes (1999), when reviewing causes of cirriped mortality, did not cemented bivalves (Harper, 1991). Interestingly, many drill holes in mention buccinids, nassariids, and fasciolariids as potential predators barnacles studied herein are classified as Oichnus paraboloides (see of intertidal barnacles. Naticids, very common drillers of molluscs and Figs. 4–6), drill holes that are usually attributed to naticid predation other invertebrates, have not been reported to drill modern barnacles, (e.g., Hingston, 1985; Kelley and Hansen, 2003; Reyment and Elewa, probably because naticids live mainly infaunally (e.g., Kelley and 2003). Drill holes that have steep walls resulting in a cylindrical mor- Hansen, 2003,butseeCarriker and Yochelson, 1968), whereas barnacles phology are usually attributed to muricids (e.g., Hingston, 1985; Kelley are epifaunal encrusters. Moreover, naticids typically cover their prey in and Hansen, 2003; Reyment and Elewa, 2003). However, steep walls mucus, envelope it, and orient prey preferentially (e.g., Kelley and do not seem evident from drill holes produced by muricids in modern Hansen, 2003), which is not possible with cemented barnacles. An inhi- (Kowalewski, 2004: fig. 3) and Carriker and Yochelson (1968) bition of prey manipulability by predators was also suggested for showed further evidence that this generalization may not always

Fig. 4. Balanids with drill holes in their wall plates. A. Incomplete drill hole in a balanid from the Puerto Armuelles 01 locality (Pleistocene, Armuelles Formation), Panama (UF 250804). A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 101 apply based on experiments with modern muricids because several fig. 2; Ambrose et al., 1988: pls. 1c, 1d; Nixon and Maconnachie, 1988: prey drilled by of different muricid genera exhibited a “parabol- pls. 1 g, 3e; Saunders et al., 1991: fig. 2). Such a concavity is also seen ic” drill hole (their pls. 1.3, 1.4, 1.13, 1.18, 1.20, 1.21, 1.22, 2.10, 2.14, in one of the drill holes attributed to octopods herein (Fig. 7B). These 2.15, and 2.17–2.22). Although most of these examples are based on examples add to the evidence that octopods, as they do today (Guerra molluscan prey, their plate 1.4 shows a barnacle with a parabolic drill and Nixon, 1987; Nixon and Maconnachie, 1988), occasionally preyed hole produced by a modern muricid, reminiscent of many drill holes upon barnacles in the past (see also Klompmaker et al., 2014). shown herein. Radwin and Wells (1968) further showed that parabolic drill holes are commonly produced by muricids (their figs. 12–18), in- 4.2. Paleogeography and stratigraphic age cluding a parabolic drill hole in a barnacle scutum (fig. 15). Thus, para- bolic drill holes get produced frequently by muricids besides cylindrical Given the new data summarized here, the few previous reports drill holes. Incomplete drill holes figured herein do not exhibit a central regarding occurrences of drill holes of inferred predatory origin in fossil boss, thought to be typical for naticid drill holes (Kowalewski, 2004;see barnacles, and occasional images of barnacles with potential drill holes Fig. 4A, J). Although it is possible that some drill holes are caused by of predatory origin found in literature (see 1.), it appears that drilling naticids, most of the parabolic and cylindrical drill holes herein are likely predation on barnacles occurred in many parts of the world and was to have been caused by muricids. ubiquitous at least since the Miocene. The earliest reported drill hole Consistent with this hypothesis, fossil specimens of these gastropods of predatory origin in a barnacle until very recently was from the Pliocene are frequent at many localities from which the studied material was (Klompmaker et al., 2014; Donovan and Novak, 2015). It is conceivable derived. The barnacles from the ?upper Pliocene Pampa Mejillones 01 lo- that pre-Eocene occurrences of drill holes in barnacles will be found cality in Chile are found in association with numerous muricid species in- because (a) drilling predation became more common in the Cretaceous cluding Herminespina mirabilis (Möricke, 1896), blainvillei and Cenozoic (e.g., Kowalewski et al., 1998; Kelley and Hansen, 2006; (d'Orbigny, 1842), Chorus doliaris (Philippi, 1887), unicornis Huntley and Kowalewski, 2007) and (b) barnacles have been common (Bruguière, 1789), and cassidiformis (Blainville, 1832). since the Mesozoic, based on fossil and molecular evidence (Foster and Muricids are also found in deposits in Florida that yielded several drilled Buckeridge, 1987; Sepkoski, 2000; Pérez-Losada et al., 2008, 2014). barnacles including the Chipola, Penney Farms, Tamiami (Pinecrest Balanomorph barnacles were present in the late Mesozoic, but became beds), Jackson Bluff, Nashua, Caloosahatchee, Bermont, and Fort Thomp- much more diverse since the Eocene (Palmer, 1982). Recently, drill son formations as well as the Waccamaw Formation in South Carolina holes of predatory origin were reported from the Cretaceous (Campanian, and the Bowden shell bed of the Bowden Formation in Jamaica Sweden) by Gale and Sørensen (2014, 2015): two out of ~3500 barnacle (e.g., Vermeij and Vokes, 1997; Kittle and Portell, 2010; Portell and plates contained a drill hole. Kittle, 2010; Kittle et al., 2013; FLMNH IP database, 2014; Portell et al., 2015). Four muricid species were reported from the upper Oligocene Haywood Landing Member (Silverdale Formation) in North Carolina 4.3. Drilling frequencies and potential biases (Vermeij and Vokes, 1997), a member yielding drilled specimens of Balanus halosydne Zullo and Katuna in Zullo et al., 1992. Muricids are The low DFs reported here (Table 1) are consistent with some quan- also known from the North American Eocene Moodys Branch and Gosport titative data from modern barnacles (Connell, 1961; Jernakoff and formations (Palmer and Brann, 1966); the Dutch Pliocene Oosterhout For- Fairweather, 1985: 7.4% of 438 dead barnacles; Archuby and Leighton, mation (Klompmaker, 2012); and the Miocene Dutch Breda Formation 2014: 9% of 720 dead barnacles). The fact that results based on museum (Janssen, 1984). Despite the presence of drilled barnacles, no muricids collections are comparable to those from the bulk sample and results are known from the Eocene Yazoo Formation (Pachuta Marl and Cocoa from extant barnacles suggests that a potential bias in collecting Sand Members, Alabama) or the Dry Branch Formation (Griffins Landing more pristine barnacles was minimal. Similar to results for decapod Member, South Carolina) (pers. comm. to RWP from G. Polites, August (Klompmaker et al., 2013), DFs as reported herein may 2014), either because muricids were absent, have not been found yet, be underestimated despite studying relatively well-preserved speci- were not preserved, or the drill holes were produced by another predator. mens with all six wall plates articulated. The reasons for this are twofold. Another culprit for two drill holes, one each from the Pleistocene and First, a drill hole could hypothetically lead to the preferential breakage of Pliocene of Florida, may be octopods (Fig. 7, Oichnus ovalis). These drill a barnacle shell, leading to a lower DF (see discussion for bivalves: holes are comparable in size and shape to octopod drill holes found in Wainwright et al., 1982; Roy et al., 1994; Hagstrom, 1996; Zuschin and modern molluscs and crustaceans (e.g., Arnold and Arnold, 1969; Stanton, 2001; Kelley, 2008). Second, drilling also occurs in the opercu- Boyle and Knobloch, 1981; Nixon and Maconnachie, 1988; Harper, lar plates, which are often not preserved within the barnacle wall plates. 2002: fig. 1). One key feature often seen in octopod holes is an irregular Loose fossil opercular plates contain evidence of drill holes (Table 1, Fig. outline of the outer diameter, consisting of concavities and/or rounded 6), and drill holes in opercular plates are also known from modern extensions superimposed on the general oval outline of many octopod barnacles (e.g., Barnett, 1979; Dunkin and Hughes, 1984; Hart and holes (e.g., Pilson and Taylor, 1961: fig. 1; Arnold and Arnold, 1969: Palmer, 1987).

B. Complete drill hole in Balanus cf. B. venustus Darwin, 1854, from the Leisey Shell Pit 01 locality (middle Pleistocene, Bermont Formation), Florida, USA (UF 250370). C. Complete drill hole in Balanus venustus Darwin, 1854, from the De Soto Shell Pit 05 locality (lower Pleistocene, Caloosahatchee Formation), Florida, USA (UF 250403). D. Complete drill hole in Balanus sp., from the Crescent Beach 02 locality (lower Pleistocene, Waccamaw Formation), South Carolina, USA (UF 250373). E. Close-up of the drill hole shown in Fig. 4D. F. Complete drill hole in Balanus sp., from the Lee Creek Mine locality (Plio-Pleistocene), North Carolina, USA (UF 250361). G. Complete drill hole in balanoides (Linnaeus, 1767), from the Langenboom locality (Pliocene, Oosterhout Formation), The Netherlands (MAB k3387). H. Complete drill hole in Balanus sp. from the Pampa Mejillones 01 locality (?upper Pliocene, upper unit), Atacama Desert, Chile (UF 245144). I. Incomplete drill hole in Tamiasoma sp., from the Pickett Bay 01 locality (Pliocene, Intracoastal Formation), Florida, USA (UF 239684/239685). J. Close-up of the drill hole shown in Fig. 4I. K. Complete drill hole in a balanid from the Jackson Bluff locality (upper Pliocene, Jackson Bluff Formation), Florida, USA (UF 250372). L. Complete drill hole in a balanid from the SMR Aggregates Phase 10 locality (Pliocene, Tamiami Formation, Pinecrest beds), Florida, USA (UF 251491). M. Close-up of the drill hole shown in Fig. 4L. N. Complete drill hole in a balanid from the Macasphalt Shell Pit locality (Plio-Pleistocene), Florida, USA (UF 250407). O. Close-up of the drill hole shown in Fig. 4N. P. Complete drill hole in a balanid from the Macasphalt Shell Pit locality (Plio-Pleistocene), Florida, USA (UF 250406). Q. Complete drill hole in a balanid from the SMR Aggregates Phase 10 locality (Pliocene, Tamiami Formation, Pinecrest beds), Florida, USA (UF 250791). R. Complete drill hole in a balanid from the Jackson Bluff 01 locality (upper Pliocene, Jackson Bluff Formation), Florida, USA (UF 250381). S. Complete drill hole in a balanid from the Richardson Road Shell Pit 01B locality (Pliocene, Tamiami Formation, Pinecrest beds), Florida, USA (UF 53931). T. Close-up of the drill hole shown in Fig. 4S. U. Complete drill hole in a balanid from the Miocene (Uloa Formation), Zululand, South Africa (UF 250856). V. Complete drill hole in a balanid from the Calvert Beach locality (Miocene, Choptank Formation), Maryland, USA (UF 250405). W. Close-up of the drill hole shown in Fig. 4V. X. Complete drill hole in a balanid from the Winsterswijk-Miste locality (Miocene, Breda Formation, Aalten Member), The Netherlands (RGM.1007738 (A)). Ichnotaxa drill holes: Oichnus simplex:A,P,R,U;Sedilichnus spongiophilus:I;O. paraboloides: rest. Scale bars: 5.0 mm except E, G, J, L, M, O, Q, T, U, W (1.0 mm). 102 A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111

Fig. 5. Non-balanid barnacles with drill holes. A. Complete drill hole in an opercular plate of the scalpellid Aporolepas howei Cheetham, 1963,fromtheIsney01locality(upperEocene,Yazoo Formation, Cocoa Sand Member), Alabama, USA (UF 250376). B. Complete drill hole in an opercular plate (tergum) of the scalpellid Anguloscalpellum jacksonense (Withers, 1953), from the Town Creek 01 locality (upper Eocene, Moodys Branch Formation), Mississippi, USA (UF 250377). C. Complete drill hole in a wall plate of the pyrgomatid Ceratoconcha sp. from the Farley Creek 07 locality (lower Miocene, Chipola Formation), Florida, USA (UF 49262). D. Complete drill hole in a wall plate of the pachylasmatid Hexelasma antarcticum Borradaile, 1916,fromthe Sars Bank locality (upper Pleistocene–Recent), Antarctica (UF 250419). E. Complete drill hole in a wall plate of the archaeobalanid Conopea sp. from the Bowden locality (Pliocene, Bowden For- mation), Jamaica (UF 77319). F. Complete drill hole in a wall plate of the archaeobalanid Conopea sp. from the Chipola 08 locality (lower Miocene, Chipola Formation), Florida, USA (UF 250387). G. Complete drill hole in a wall plate of the archaeobalanid Actinobalanus sp., from the Borgerhout locality (lower Miocene, Berchem Formation, Edegem Sand Member), Belgium (UF 250416). H. Complete drill hole in a wall plate of the archaeobalanid Hesperibalanus huddlestoni Zullo and Kite, 1985,fromtheGriffins Landing 01 locality (upper Eocene, Dry Branch Formation, Griffins Landing Member), Georgia, USA (UF 250409). Ichnotaxa drill holes: Oichnus simplex:C,E,H;O. paraboloides: rest. Scale bars: 1.0 mm for A, B, G, H; 5.0 mm for C–F.

It should be stressed that drilling is not a necessity for modern (1985) reported that when the shell spine, normally used for smashing gastropods to kill barnacle prey, as gastropods may feed through the and/or forcing open of the opercular plates, is broken in the muricid opercular opening without leaving obvious traces, make use of a labral spirata (Blainville, 1832), this species will alter its strategy spine to enter through the opercular plates, or pry apart the opercular to drilling through the opercular plates (Perry 1985). Experimental work plates (e.g., Luckens, 1975; Barnett, 1979; Dunkin and Hughes, 1984; is required to evaluate this issue rigorously. Perry, 1985; Barnes, 1999; Sanford and Swezey, 2008; Gordillo, 2013). For example, Barnett (1979) reported that drilling was involved in only 4.4. Drill hole location and size 23 and 54% of the two barnacle species consumed by a muricid ( Röding, 1798), whereas Archuby and Leighton (2014) reported that 53 The present study and other studies on barnacles suggest that out of 54 barnacles killed by muricids (Nucella) during experiments muricids do not select a drill hole site randomly. This may be related were not drilled or exhibited incomplete drill holes. Such alternative to the fact that muricids put considerable effort in selecting a drill hole modes of feeding do not necessarily leave a trace behind: Sanford and site. For example, Carriker and Van Zandt (1972) observed a muricid Swezey (2008) found that only 2/17 cases of feeding through the opercu- preying on and found that the would take minutes to lar opening resulted in a trace. Thus, the DF does not necessarily reflect about half an hour to select the drill hole site. the frequency with which gastropods successfully preyed upon barnacles. The high preference for drilling between the plates (56.8% here) is The diverse strategies employed by muricids when preying upon bar- roughly comparable with results of Palmer (1988) for modern barnacles nacles help to explain the low drilling frequencies found herein and in the (46% drill holes between plates). Drilling between the plates is an literature. The fact that barnacles consist of many more skeletal compo- effective strategy to increase predation efficiency since the shell is nents compared to brachiopods, molluscs, and echinoids, resulting in a substantially thinner in the interplate areas (pers. obs.) and complete higher number of shell margins, might explain why alternative strategies penetration is not necessary to inject the toxin between the plates. appear more frequently used by predatory gastropods feeding on barna- Some muricid taxa are known to possess toxin (e.g., Huang and Mir, cles. Dunkin and Hughes (1984) noted that prying apart the opercular 1972; Shiomi et al., 1998), although more muricids have been suggested plates took less time than drilling in their experiments. Assuming that to use venom during predatory attacks (e.g., Urrutia and Navarro, 2001; this observation is true for other gastropod–barnacle interactions as Paul et al., 2014). well, it can be asked why drilling takes place at all. This may at least par- Our finding that the rostral plate was a preferred site for drilling is in tially be explained by experience—more experienced muricids tend to agreement with Tan (2003), who focused on a single prey taxon from drill less frequently (Dunkin and Hughes, 1984)—and adulthood—small Australia [Tetraclita squamosa (Bruguière, 1789) drilled by the muricid muricids tend to drill barnacles more frequently (Connell, 1961). Perry Tenguella granulata (Duclos, 1832)]. We concur with this author that A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 103

Fig. 6. Opercular plates of balanid, archaeobalanid, and pyrgomatid barnacles with drill holes. A. Drill hole on edge of scutum of the balanid Balanus sp. from the Pampa Mejillones 01 locality (?upper Pliocene, upper unit), Atacama Desert, Chile (UF 250396). B. Complete drill hole in scutum of Balanus sp. from the same locality and stratigraphic unit (UF 250392). C. Complete drill hole in scutum of the pyrgomatid Ceratoconcha sp. from the Farley Creek 07 locality (lower Miocene, Chipola Formation), Florida, USA (UF 49694). D. Drill hole on edge of scutum of the balanid Balanus halosydne Zullo and Katuna in Zullo et al., 1992, from the Stella 01 locality (upper Oligocene, Silverdale Formation, Haywood Landing Member), North Carolina, USA (UF 250399). E. Drill hole in scutum of the archaeobalanid Newmanrossia antiquua antiquua (Meyer, 1886), from the Puss Cuss Creek 01 locality (upper Eocene, Moodys Branch Formation), Alabama, USA (UF 250363). F. Drill hole in scutum of the archaeobalanid Newmanrossia sp., from the Whately 01 locality (upper Eocene, Yazoo Formation, Cocoa Sand Member), Alabama, USA (UF 250384). G. Drill hole in scutum of the archaeobalanid Hesperibalanus huddlestoni Zullo and Kite, 1985, from the Savannah River Plant 01 locality (upper Eocene, Dry Branch Formation), South Carolina, USA (UF 250410). Ichnotaxon drill holes: Oichnus paraboloides:B,C;restdifficult to determine. Scale bars: 1.0 mm. the relatively gentle slope of the rostral region may provide a more to drill the more convex surface (heightwise) of the rostrum given the stable position for drilling than the carinal region, lowering the chance convex morphology of their other main prey, molluscs; and (b) the of dislodgment by wave action. Tan (2003) also suggested that the opercular plates on the rostral side (scuta) seem oriented more toward rostral plate is significantly thinner than the lateral plates, which may the top of the wall plates than the opercular plates on the carinal side also apply to some barnacle taxa herein. Two other factors may be (terga) for balanomorph barnacles, implying that drilling on the rostral important as well: (a) it may be considered more natural for muricids side increases the chance of avoiding drilling into the opercular plates.

Fig. 7. Two specimens with oval drill holes (ichnotaxon: Oichnus ovalis), inferred to be made by octopods. A, B. A drill hole located between the left lateral compartments in a balanid bar- nacle from the upper Pliocene Jackson Bluff Formation, Florida, USA (UF 251043). C. A drill hole located in the interplate region between the rostrum and the left lateral compartment in a balanid barnacle from the lower Pleistocene Caloosahatchee Formation, Florida, USA (UF 250936). Scale bars: A = 10.0 mm; B, C = 1.0 mm. 104 A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111

Fig. 8. Drill hole size vs. barnacle size (loge measurements). A. Drill hole size vs. maximum barnacle diameter for all drill holes combined. B, C. Same as in A, but with complete and incomplete drill holes shown separately, respectively. D. Drill hole size vs. length of drilled barnacle wall plate for all drill holes combined. E, F. Same as in D, but with complete and in- complete drill holes shown separately, respectively. G. Drill hole size vs. maximum barnacle diameter for barnacles from the upper Pliocene–lower Pleistocene Tamiami Formation. H. Drill hole size vs. maximum barnacle diameter for barnacles from the upper Pliocene Jackson Bluff Formation. I. Drill hole size vs. maximum barnacle diameter for barnacles from the De Soto Shell Pit 05 locality (lower Pleistocene, Caloosahatchee Formation—Portell Bed 7). All lines depict reduced major axis regression estimates.

The latter suggestion is consistent with the observation of Hart and position to drill, which is consistent with the relatively low percentage Palmer (1987) that the tergal plates were held against the inner surface, of drill holes placed here. being less exposed. The percentage of drill holes in the interplate area decreases going Drill holes were made typically midway the height of the drilled from the top of the barnacle to the base, which is expected given the de- barnacle wall plate (Fig. 11A), as was observed by Tan (2003).This creasing area occupied by interplate area toward the base (Fig. 11C). positioning of the drill holes seems logical because drill holes produced This observation is consistent with the results reported by Palmer (1982). in the top part of the shell may be above the opercular plates instead of Drill holes in the opercular plates are predominantly found in the below, where the soft tissue is located. Moreover, drilling below the top scuta (Appendix 1). This result does not necessarily mean that scuta part of the shell also avoids having to drill through the apertural sheath, are more commonly bored than terga because terga tend to be under- an extra layer of shell only present on the inner side of the top part in represented in the samples of well-preserved opercular plates (see balanomorph barnacles (e.g., Raman and Kumar, 2011). The top part Table 1). The bulk sample analysis of terga vs. scuta yielded a ratio of of the plates may also not be the most stable place to drill because 1:2.22 (see Section 3), confirming the higher preservation potential of waves may dislodge the muricid more easily. In addition to a potentially scuta compared to terga due to the more robust nature of scuta. This thicker shell near the base, attaching to the base may be difficult in some bias is not as prominent as observed in museum collections (Table 1). instances because the substrate or other barnacles may prevent easy We argue that the taphonomic bias toward enhanced preservation access (see also Tan, 2003). The fact that the percentage of incomplete of scuta cannot fully explain why scuta are drilled more frequently drill holes is greatest at the top may suggest the top is not the best because (a) not a single tergum is drilled in the bulk sample, whereas A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 105

Fig. 10. The sampling distribution of standard deviations for drill hole frequencies expected under the null hypothesis that the drill holes are randomly distributed across 12 plate regions (based on a 10,000-iteration Monte Carlo simulation). The arrow indicates the actual standard deviation observed for the data. P-value estimated as the proportion of extreme replicate samples for which the simulated standard deviation exceeded the observed standard deviation.

Fig. 9. Locations of drill holes per plate and interplate regions plotted on a balanomorph gastropods (e.g., Kitchell et al., 1981; Kelley, 1991). Moreover, from barnacle in dorsal view (UF 251028). Yellow bars represent drill holes in interplate areas, whereas green bars are drill holes in wall plates. The numbers within brackets are the modern is it known that larger barnacles are preyed upon by larger derived from the Monte Carlo model for drill holes placed randomly on the wall plates; muricid and that drill hole size in barnacles and predator size are first and last number: 95% confidence interval around the mean (second number). Note positively correlated (Hart and Palmer, 1987; Palmer, 1990; Tan, 2003). that the interplate areas appear larger than in reality due to the angle of the photo. (For Drill hole diameter correlates with muricid body size also for bivalve interpretation of the references to color in this figure legend, the reader is referred to prey (Kowalewski, 2004, and references therein). the web version of this article.)

4.5. Meaning of incomplete drill holes some scuta are drilled and (b) scuta tend to be more exposed in balanomorph barnacles (Fig. 1). Hart and Palmer (1987) also suggested Complete drill holes in gastropods and bivalves have been considered that scuta are drilled more frequently than terga. Table 1 provides data successful, whereas incomplete drill holes are often seen as unsuccessful on the Chilean Pampa Mejillones 01 locality showing a higher DF for (e.g., Kitchell et al., 1986: p. 291; Kelley and Hansen, 2003: p. 119), opercular plates than the wall plates. Hart and Palmer (1987) indicated although Kelley and Hansen (2003) noted that exceptions occur due to that the muricid Thais Röding, 1798 attacked the opercular plates more suffocation citing Ansell and Morton (1987). For example, Edwards frequently with increased age irrespective of barnacle size, specifically (1969) also showed experimentally that 14/21 (67%) of consumed the suture between scutal plates, whereas younger muricids placed specimens of the gastropod Olivella biplicata (Sowerby, 1825)showed the drill holes more randomly. The muricids from the Pampa Mejillones incomplete drill holes, with death probably due to suffocation during 01 samples exhibit a maximum width range from 16.25–66.29 mm and the drilling process by a naticid, explaining the presence of incomplete median of 30.60 mm (n = 106, Appendix 3). Thus, it may be speculated drill holes. More recently, Hutchings and Herbert (2013) documented that these muricids were focusing too on the opercular plates during the that as many as 8/20 (= 40%) naticid prey with incomplete drill holes Pliocene at Pampa Mejillones 01. were successfully preyed upon due to suffocation by naticids, also in an Our results show that drill hole size and barnacle size are positively experimental setting. However, Visaggi et al. (2013) documented that correlated (Fig. 8). A similar relationship is known for bivalves and suffocation of a bivalve due to naticids was rare during their experiments

Table 2 Observed (OF) and expected frequencies (EF) of drill holes in balanomorph wall plates and the associated χ2 tests.

# Drill holes # Drill holes # Drill holes in rostral area # Drill holes outside χ2-value p-value between wall in wall plates (rostrum + adjacent rostral area plates interplate regions)

OF (All) 155 118 126.4 b0.001 EF (All) 43 230 OF (De Soto Shell Pit 05) 22 8 74.6 b0.001 EF (De Soto Shell Pit 05) 5 25 OF (All) 138 135 29.0 b0.001 EF (All) 78 195 OF (Six plates preserved) 114 123 43.6 b0.001 EF (Six plates preserved) 68 169 OF (Six plates preserved, De Soto Shell Pit 05) 16 14 7.8 0.005 EF (Six plates preserved, De Soto Shell Pit 05) 9 21 106 A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111

Fig. 11. Drill hole variables as a function of the height of barnacle (UF 53931). A. The number of drill holes, n = 270; B. The percentage of complete and incomplete drill holes, n = 266; C. The percentage of drill holes in plate and interplate regions, n = 267; D. Boxplots of drill hole diameter, n = 271; E. Boxplots of the maximum diameter of drilled bar- nacles, n = 226.

(b1%), and that suffocation in previous studies may have been higher 66/282). Another reason for the presence of incomplete drill holes is in- due to weak prey health and other laboratory effects. With regard to terruption during the drilling process as noted by Palmer (1982: p. 32) barnacles, Palmer (1982) noted that incomplete drill holes are not neces- for intertidal barnacles. Furthermore, as much as 99.6% (n = 762) of sarily unsuccessful because toxin released by the muricid Stramonita barnacle prey drilled elsewhere were consumed from between the haemastoma (Linnaeus, 1767)(seeHuang and Mir, 1972) between the opened opercular plates (Palmer, 1982), in agreement with the sugges- radii and alae in the interplate region, or through an incomplete hole tion of Archuby and Leighton (2014) that Nucella rarely consume in a plate, may relax the barnacles after which feeding may occur S. cariosus through the drill holes. Thus, the goal of drilling in barna- through the gaping opercular plates. Sanford and Swezey (2008) cles by at least some muricids may not be to penetrate the shell to found that most drill holes (14/17) in the interplate area did not pene- feed, but to inject toxin to relax the muscles that are responsible trate the shell for Semibalanus cariosus (Pallas, 1788) consumed by for keeping the opercular plates closed. This strategy may have Nucella analiculata (Duclos, 1832), and Archuby and Leighton (2014) been employed by at least some muricid predators over millions also mentioned that drill holes in S. cariosus are rarely complete. In of years as, for example, Stramonita spp. occur as far back as the this study, drill holes in wall plates are commonly incomplete (23.4%, Miocene (Fossilworks.org, accessed 5 August 2014). To what extent

Fig. 12. A plate of a balanid barnacle from the Miocene Choptank Formation in Maryland (USA) exhibiting a thickening on the inside of the drilled wall plate (UF 250786). A. Plate as pre- served. B. Close-up of the drill hole on the outer side (ichnotaxon drill hole: Oichnus simplex). C. Side view of the thickening. Scale bars: A = 10.0 mm; B, C = 1.0 mm. A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 107 incomplete drill holes in barnacles were unsuccessful is difficult to Whether muricids would drill the interplate area when fewer such estimate. areas are available depends partly on the time spent by the predator selecting a drill hole site. From this perspective, a reduction of the number 4.6. Morphological evolution of barnacles vs. drilling frequencies of interplate areas may not be effective per se as muricids take minutes to about half an hour to select the drill hole site (Carriker and Van Plate reduction in balanomorphs from eight to one or four plates was Zandt, 1972), which should be sufficient to encounter and recognize suggested by Buckeridge (1983: fig. 89) and already recognized by an interplate area. Using Palmer's model (his fig. 3) and assuming that Darwin (1854), although a phylogenetic analysis on modern barnacles the probability of recognizing an interplate area could correspond to suggested a more complex pattern (Pérez-Losada et al., 2014). Palmer the percentage of drill holes between the plates observed herein (1982: p. 31, fig. 5), however, showed a clear trend based on fossil (56.8%), it follows that the probability to encounter an interplate area is balanomorphs and hypothesized that “predation by drilling gastropods N90%. Instead of reducing the number of wall plates, narrowing of the has been an important selective force behind the widespread, parallel interplate regions may make it much harder for predators to detect it evolutionary tendency toward plate reduction in the Balanomorpha.” (Fig. 13), consistent with the suggestion in Murdock and Currey (1978: This depends on the relative vulnerability of interplate regions and p. 186). Also, because opercular plates appear to have a higher DF than wall plates and the ability and effectiveness of muricids to detect wall plates (Table 1), reducing the opening may decrease successful interplate regions (Palmer, 1982). As mentioned in 4.4, the total shell predation there (Fig. 13). thickness appears lower in the interplate areas, suggesting that drilling External sculpture was suggested to have evolved in response to there would reduce the total drilling time and energy expenditure. drilling predation (Palmer, 1982). He noted that muricids had a harder If muricid predation is responsible for the evolution toward fewer time recognizing the interplate regions for barnacles with height-wise wall plates, then it may be hypothesized that DF should be high. ribs as opposed to barnacles with smooth ribs, and that strong sculpture However, drilling frequencies herein are rather low (b10%, despite is often more common on barnacles found on the lower intertidal zone several biases) as they appear today (Connell, 1961; Jernakoff and as predation pressure tends to be higher there compared to the upper Fairweather, 1985; Archuby and Leighton, 2014) compared to DFs in part of the intertidal zone. Supporting evidence would be the observa- many bivalves and gastropods (e.g., Kelley and Hansen, 2006: tables 3, tion of an increase in sculpted barnacles throughout the Cenozoic, 4; Klompmaker, 2009: table 1; Das et al., 2014). A key question is concurrent with the increase in muricid diversity and abundance. whether these consistently low DFs were sufficient to promote evolu- Although most barnacles studied herein likely represent shallow tion toward fewer wall plates. subtidal settings (an extrapolation based on the present-day distribu- This research shows that drilling is not random in that a dispro- tion of balanids and archaeobalanids; see Foster, 1987: fig. 1), it may portionally high percentage of drill holes are concentrated in between be hypothesized that external sculpture such as ribs should be uncom- the plates (56.8%), consistent with results reported by Palmer (1982: mon in balanomorphs prior to the increase in muricid diversity since tables 1, 2). If muricid drilling led to fewer wall plates, then specimens the Eocene to Oligocene (Sohl, 1969). Moreover, it may be expected with fewer wall plates are expected to have a lower proportion of drill that Paleogene balanoids would exhibit less sculpture than Neogene holes located in the interplate regions. Additionally, more incomplete species. However, the proportion of strongly ribbed balanomorph drill holes would be expected in specimens with fewer interplate re- species (excluding whale-encrusting coronulids) did not increase gions. Unfortunately, nearly all of our drilled specimens consist of six throughout the Cenozoic in Australia and New Zealand (using wall plates, which preclude investigating this hypothesis in more detail. Buckeridge, 1983): Paleocene, 33% (n = 3); Eocene, 33% (n = 9); Oligocene, 33% (n = 9); Miocene, 22% (n = 23); Pliocene, 33% (n = 15); Pleistocene, 33% (n = 9), despite an apparent increase in muricid diversity in this region of the world throughout the Cenozoic (Fossilworks.org; accessed 20 September 2014), in agreement with the global pattern (Sohl, 1969). Furthermore, strongly ribbed barnacles are not uncommon in the Eocene: Archaeobalanus semicanaliculatus Menesini, 1971; Kathpalmeria georgiana Ross, 1965; K. hantkeni (Kolosváry, 1947); Solidobalanus (Hesperibalanus) parahesperius (Menesini, 1971), and Hesperibalanus phineus (Kolosváry, 1956), and the oldest recognized balanomorph, Pachydiadema cretaceum Withers, 1935, already shows ridges on the wall plates (his pl. 50). We also have not observed an increase in external sculpture based on prelimi- nary observations in the FLMNH-IP collections. Whale-encrusting barnacles such as aotea Fleming, 1959, (Linnaeus, 1767), and Neogene and modern Coronula spp., taxa which do not interact with muricids, also possess moderate to strong ribs (Buckeridge, 1983; pers. obs. FLMNH-IP collection), as do some turtle- and manatee-encrusting barnacles (e.g., Cintrón-De Jesús, 2000; Lazo-Wasem et al., 2011; Zardus et al., 2014). These observations may suggest that strong ribs did not evolve in response to muricid drilling predation even though they may function in lowering the success rate of drilling predation (i.e., an exaptation). Recently, bivalve ribs were suggested to represent a likely example of exaptation with respect to drilling predation (Klompmaker and Kelley, 2015). Conversely, Tyler et al. (2014) documented that ribbed experienced a higher mortality due to crabs than did smooth limpets. A third argument used by Palmer (1982) in support of evolution of Fig. 13. A cluster of barnacles from the ?late Pliocene of Chile showing narrow interplate barnacles in response to muricid predation is the emergence of tubes regions and small opercular openings (UF 245098). Note a complete drill hole in the right-most shell (arrow, ichnotaxon Oichnus paraboloides), which is the only drilled in wall plates, although Stanley and Newman (1980) favored the inter- specimen with four wall plates. Scale bar: 10.0 mm. pretation that tubes helped to grow the barnacle faster for competitive 108 A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 purposes by creating a thicker overall shell wall without an increase in plates are expected to be much more efficient than cirri in protecting shell mass. These tubes seem to appear in balanoids starting in the the internal soft tissue against predation. Oligocene (Stanley and Newman, 1980), which postdates the initial radiation of muricids (Paleocene, Eocene). Such tubes are usually not 4.8. Regeneration of the shell infilled, and, hence, Gordillo (2013) noted that empty tubes reduce the shell material to be drilled through for Balanus laevis Bruguière, The drill hole in the Miocene specimen showing a pronounced 1789 compared to a massive shell. This space can, however, be infilled thickening on the inside of a hole (UF 250786, Fig. 12)maybe throughout ontogeny in some species ( non-predatory (parasitic or domichnial) in origin as the barnacle (Linnaeus, 1767), Darwin, 1854 and many species of wouldnothavehadsufficient time to thicken the interior of the Tetraclita Schumacher, 1817,seePalmer, 1982), but secondary infilling shell as protection after successful penetration by a gastropod. Al- is rare in the Balanoidea (Newman and Ross, 1976). Some balanomorph ternatively, the predator may have abandoned the live prey due to tubes are infilled with chitinous material (Newman and Ross, 1971, disturbance after completing the drill hole and thus allowing the 1976), which may be functional in deterring drilling predation surviving barnacle to partly regenerate its shell. Either way, the (Newman and Ross, 1971); an organic substance (conchiolin layers) hole was not lethal. Similar regeneration (“marked calcification around in some bivalves was also suggested to be functional against drilling the drill holes”) of a barnacle wall plate was observed experimentally for predation (e.g., Harper, 1994; Kardon, 1998; Ishikawa and Kase, modern barnacles using mechanical drills (Tighe-Ford and Vaile, 1972, 2007). Palmer (1982) suggested that the presence of tubes, widening 1974: p. 303). the distance between the outer and interior shell wall, may impede the muricid's accessory boring organ (ABO—a mushroom-shaped 4.9. Possibilities for future studies papillae in the muricid's foot that secretes chemicals to dissolve the shell locally) from reaching the interior. The key question is then the The FLMNH-IP collection contained a limited number of specimens maximum reaching range of the ABO relative to the size of the muricid from the Paleocene and Cretaceous, whereas barnacles from these (if ABO length is a limiting factor). Carriker and Van Zandt (1972) inves- older time intervals may have also been affected by drilling predators, tigated this question for adult specimens of the muricid as shown recently for the Cretaceous barnacles (Gale and Sørensen, cinerea (Say, 1822) (maximum shell height reported in their table 6 is 2014, 2015). We also need to evaluate if the placement of drill holes is 42 mm) drilling large oysters in an experimental setting. They found more random on strongly sculpted barnacles as suggested by Palmer that the deepest incomplete drill holes ranged from 4.3–5.3 mm (1982) for modern taxa and whether this would lead to more (diameter 1.16–1.65 mm) and suggested that “in extremely large prey incomplete drill holes in wall plates. Similarly, it may be expected that with thick shells they are not able to complete perforations” (p. 229). more ornamented taxa experience lower DFs if such morphology is Given that barnacles typically do not exhibit an overly thick shell functional against drilling predation and if DF is indicative of elevated (usually b3 mm; e.g., Hart and Palmer, 1987), especially given the predation pressure on barnacles. Also, because opercular plates are a limited size for the vast majority of the species herein, it seems unlikely target for muricid and decapod predators, it would be useful to study that the extra space created by tubes in balanoids would exclude quantitatively any morphological changes through time (e.g., shell complete penetration by muricids. Furthermore, barnacles that are typ- thickening). We also do not have rigorous data to evaluate if the ically excluded from interaction with muricids (e.g., whale-encrusting percentage of drill holes between plates decreases as the number of Coronula spp. and turtle- and manatee encrusting Chelonibia spp.) also plates decreases as predicted by the Palmer's hypothesis. Unfortunately, contain wall tubes (e.g., Newman and Ross, 1976). Although it cannot the barnacle collections studied herein do not lend themselves to an- be ruled out that the presence of tubes may confuse some muricids in swer this question as balanomorphs that possess fewer or more than perceiving that they completed a drill hole, the evolution of tubes six wall plates are rare. Experimental work would be useful to further does not conclusively support the hypothesis that tube walls evolved assess circumstances in which drilling is employed and whether there in response to muricid predation. are advantages at all to drilling given the cost and time involved. Our Whether strong external sculpture, tubes in wall plates, and a reduc- current knowledge is also biogeographically uneven, with few or no tion in the number of wall plates have evolved in response to muricid studies of predation on fossil barnacles outside North America and drilling predation should be investigated further. Barnacles are vulnerable Europe. No studies are known to us from Asia and Australia. to many types of predators, although muricid predation has been studied relatively more extensively (e.g., Foster, 1987; Barnes, 1999). Barnes et al. 5. Conclusions (1970) suggestedthatstronglyribbedbarnacleswouldbemoreresistant to breakage by other predators. As the strength of the barnacle shell is 1. Drill holes of predatory origin in wall plates and opercular plates of closely related to the articulation of wall plates at the interplate regions fossil barnacles were found at all 12 examined localities ranging (Barnes et al., 1970), a reduction of the number of wall plates may be ef- from the Eocene to the Pleistocene, although drilling frequencies fective to some extent against crushing predators such as fish and deca- are generally low (range b1% to ~9%). pod crustaceans (Barnes, 1999). Other factors such as predation by non- 2. Drill holes are found mostly in the , but also occur in mem- drilling predators, competition among barnacles, and protection against bers of the Archaeobalanidae, Scalpellidae, Pachylasmatidae, and physical disturbance cannot be ruled out to have influenced the morpho- Pyrgomatidae. These families belong to the suborders Balanomorpha logical evolution of barnacles. and . 3. Drilling predation of barnacles was likely a worldwide phenomenon during the Cenozoic given their distribution in marine strata from 4.7. Cirri various continents. 4. Most drill holes are interpreted to be caused by predatory gastropods Donovan and Novak (2015: p. 3) suggested a role for the cirri in such as muricids; two holes in our sample were likely produced by defending a part of the shell (“antipredatory interference by the cirri”) octopods. based on drill holes in fossil barnacles. This hypothesis is unlikely 5. Drill holes tend to be larger in larger barnacles. because Palmer et al. (1982) and Barnes (1999: p. 155) already noted 6. Placement of drill holes is non-random in balanomorph wall plates for extant barnacles that, in the presence of predators, prey typically because they are found preferentially (a) between plates in the withdraw the cirri into the shell by closing the opercular plates to interplate region, (b) on and around the rostrum, and (c) in the mid- protect these feeding structures. The opercular plates and the wall dle part of shell (height-wise). For the opercular plates, scuta are A.A. Klompmaker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 426 (2015) 95–111 109

drilled more frequently than terga. Bromley, R.G., 1993. Predation habits of past and present and a new ichnospecies, Oichnus ovalis. Bull. Geol. Soc. Den. 40, 167–173. 7. Drill holes in wall plates are often incomplete most likely because Bruguière, M., 1789. Encyclopèdie Methodique: Histoire Naturelle des Vers 1. they need not be complete for successful predation of barnacles. Panckoucke, Paris, pp. 1–344. 8. We find limited support for the hypothesis that balanomorph mor- Buckeridge, J.S., 1983. Fossil barnacles (Cirripedia: ) of New Zealand and Australia. N. Z. Geol. Surv. Paleontol. Bull. 50, 1–151. phology has evolved in response to predation by muricid gastropods. Carriker, M.R., Van Zandt, D., 1972. Predatory behavior of shell boring muricid gastropod. Physical processes and other predators should not be ruled out as In: Win, H.E., Olla, B.L. (Eds.), Behavior of Marine : Current Perspectives in potential selective pressures. Research. Plenum Press, New York, pp. 157–244. 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University of Puerto Rico, Mayagüez. provided to the FLMNH-IP by several prominent barnacle researchers Collins, J.S.H., Donovan, S.K., Stemann, T.A., 2009. Fossil Crustacea of the late Pleistocene Port Morant Formation, west Port Morant Harbour, southeastern Jamaica. Scr. Geol. (e.g., the late Victor Zullo, the late Arnold Ross, and Ray T. Perreault), 138, 23–53. by materials transferred from the Florida Geological Survey, Tulane Connell, J.H., 1961. Effects of competition, predation by Thais lapillus, and other fac- University (Harold and Emily Vokes Collection), and the University of tors on natural populations of the barnacle Balanus balanoides. Ecol. Monogr. – North Carolina Wilmington, along with National Science Foundation 31, 61 104. d'Orbigny, A., 1842. Voyage dans l'Amérique méridionale (le Brésil, la République Oriéntale support to curate those collections (DEB 9509178 and DBI 0645865). de l'Uruguay, la République Argentine, la Patagonie, la République du Chili, la Additional funding for Panama collections was provided through République de Bolivia, la République du Pérou) exécuté pendant les aneées 1826, Partnerships for International Research and Education (PIRE) grant 1927, 1828, 1829, 1830, 1831, 1832 et 1833. Paleontologie 3 (4). Pitois-Levrault, Paris. Darwin, C., 1854. A Monograph on the Subclass Cirripedia with Figures of all the Species. 0966884 and research funding to RWP for fieldwork in the SE USA The Balanidae, the Verrucidae. etc. Ray Society, London. and Caribbean was provided by James Toomey, Barbara Toomey, and Das, A., Mondal, S., Bardhan, S., 2014. A note on exceptionally high confamilial naticid the McGinty Endowment. 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