Naticid drilling predation on gastropod assemblages across the K–T boundary in Rajahmundry, India: New evidence for escalation hypothesis

Palaeogeography, Palaeoclimatology, Palaeoecology 411 (2014) 216–228

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Naticid drilling predation on gastropod assemblages across the K–T boundary in Rajahmundry, India: New evidence for escalation hypothesis Sumanta Mallick a,⁎, Subhendu Bardhan b, Shiladri S. Das c, Shubhabrata Paul d, Pritha Goswami b a

Department of Geology, Triveni Devi Bhalotia College, Raniganj 713347, India Department of Geological Sciences, Jadavpur University, Kolkata 700032, India c Indian Statistical Institute, Geological Studies Unit, 203 Barrackpore Trunk Road, Kolkata 700035, India d Department of Earth Sciences, Indian Institute of Science Education and Research, Kolkata, Mohanpur Campus, W.B. 741252, India b

a r t i c l e

i n f o

Article history: Received 19 February 2014 Received in revised form 26 June 2014 Accepted 2 July 2014 Available online 9 July 2014 Keywords: High drilling predation Naticid gastropods Turritelline gastropods Assemblage- and lower taxon-level drilling frequencies Escalation End-Cretaceous mass extinction

a b s t r a c t One of the important and well documented prey–predator interactions in the fossil record is drilling predation done by naticid gastropods which diversified during the Cretaceous. Although drilling frequencies showed fluctuating patterns, most of the previous studies argued that naticid drilling predation was less intense during the Cretaceous and the modern values were achieved since the Paleocene. We, here, present a new dataset of naticid drilling predations, involving 31,929 gastropod specimens, from the latest Maastrichtian Infratrappean bed in Rajahmundry, southern India. These specimens belonged to 40 species of 20 families, thus representing a spectacular gastropod diversity that was not known until recently from this region. We examined 5884 complete or near complete specimens to quantify naticid drilling predation on this assemblage. It appeared that drilling frequency was significantly higher from all previous Cretaceous values. This was true for both assemblage-level and lower taxon-level results. Along with high successful drilling and low unsuccessful drilling frequencies, site and size stereotypy of drillholes suggest that naticid predators were highly efficient, even in the Cretaceous. Predators were prey selective and there was poor correlation between relative abundance and drilling frequency of prey taxa. The present Maastrichtian assemblage underlies the K–T mass extinction level. Drilling frequency was zero in the straddler prey community in the Intertrappean bed found immediately above the K–T boundary. The absence of any drillhole in surviving prey taxa may be due to sudden reduction in abundance of escalated predators, although some prey taxa e.g., cerithiids continued. This emphasizes the role of mass extinction in disrupting predator–prey interaction. We conclude that naticid drilling-induced escalation was already established during the Cretaceous and the present find extends the paleobiogeography of naticid predation (which was previously reported from the western world) up to India. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Dynamics of prey–predator interaction is best evident from the drilling predation which leaves very faithful and reliable proxies in the fossil record. For example, identity and efficiency of the predators, behaviors like stereotypy for drillhole position and prey size, prey preference can be well understood from the drillhole and its morphology (Kowalewski, 2002). Drilling-induced two evolutionary trends are quite apparent (Vermeij, 1987; Kelley and Hansen, 1993; Dietl and Kelley, 2002). One is escalation which can be defined as changes ⁎ Corresponding author. E-mail addresses: [email protected] (S. Mallick), [email protected] (S. Bardhan), [email protected] (S.S. Das), [email protected] (S. Paul), [email protected] (P. Goswami).

http://dx.doi.org/10.1016/j.palaeo.2014.07.001 0031-0182/© 2014 Elsevier B.V. All rights reserved.

occurring within any species due to the changes taking place within their enemies (i.e., predators); another is coevolution which describes cases where two (or more) species reciprocally affect each other's evolution. Coevolution is likely to happen when different species have close ecological interactions with one another. The naticid drilling predation is ubiquitous in the fossil record since the Cretaceous and well documented in the literature (Taylor, 1970; Adegoke and Tevesz, 1974; Vermeij and Dudley, 1982; Taylor et al., 1983; Arua and Hoque, 1989; Kelley and Hansen, 2006; Harries and Schopf, 2007 and many others). These studies indicated considerable variation in spatial and temporal distribution of drilling frequency (DF) made by naticid predators on bivalves and gastropods. It becomes apparent that in spite of great fluctuations of DFs through ages, the Cretaceous DFs on both bivalves and gastropods were low and increased substantially after the end-Cretaceous mass extinction

S. Mallick et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 411 (2014) 216–228

event. This pattern has been supported by most of the workers (e.g., Vermeij, 1987; Allmon et al., 1990; Kelley and Hansen, 2006). During the Cenozoic, DF pattern was cyclical with peaks during Paleocene–Eocene and Miocene. Kelley and Hansen (2006) showed that both assemblage-level and lower-taxon level DFs were well co-ordinated in the Tertiary fossil record, paralleling each other at least in the US Coastal Plain. All of these previous studies on the Cretaceous DFs were done in areas belonging to higher latitude localities of the U.S.A. and the Western Europe (Taylor et al., 1983; Allmon et al., 1990; Kelley and Hansen, 2006). Although the Cretaceous values for drilling frequency were low for both bivalve and gastropod in comparison to the Paleogene values, DFs showed spatial variation among coeval stratigraphic levels (Harries and Schopf, 2007; Kelley and Hansen, 2007a). For example, in gastropod assemblages DF varied from 3.7% in the Ripley Formation, Georgia to 6.0% in the Providence Formation, Georgia of the Maastrichtian. At the lower taxon level, Turritellidae showed variation of DF from 4.2% to 12.6% in Georgia during the Maastrichtian. Bivalve assemblage level DFs showed greater range of variations (5.5% in the Corsicana Formation, Texas to 19.4% in the Providence Formation, Georgia of the Maastrichtian; Kelley and Hansen, 2006). At lower taxon levels bivalves also showed significant spatial variation of DF (for details see Kelley and Hansen, 2006; their Table 2). We, here, reported naticid drilling predation on a latest Maastrichtian gastropod assemblage from southern India which belonged to the subtropic of southern hemisphere during that time (Smith et al., 1981; Bardhan et al., 2002). The present fauna came from a ‘Turritelline-dominated assemblage’ (TDA of Allmon, 2007). We analyzed 31,929 gastropod specimens which were obtained mostly from bulk samples to document diversity and 5884 complete or near complete shells to calculate drilling frequency. Comparison of the present data with those of the previous studies revealed that DFs of south Indian gastropods were consistently higher in majority of the taxonomic levels than all previous values from the Cretaceous. Mallick et al. (2013) previously documented high DF on turritelline gastropods from the same assemblage. Even DFs of southern India were sometimes higher than some of the Paleogene (except the Paleocene) and Neogene values documented in the U.S.A. (see Kelley and Hansen, 2006). Indian DFs may be at par with recent standards. We, therefore, could not support the prevailing hypothesis that Cretaceous naticid drilling intensity was low. Additionally behavioral data (such as size and site stereotypy) of southern Indian naticid predation suggested that the predators were highly experienced and efficient (i.e. size and site selective). Prey effectiveness and prey preferences were also evaluated (see also Anderson et al., 1991; Kelley and Hansen, 2003) to test our claim that escalation of naticid predation had been already established, at least in one region, during the Cretaceous. Future discoveries from other areas may elucidate our understanding of naticid DFs in a better way. The present macrofaunal assemblage occurs in a thin calcareous sandstone bed buried by the Deccan Trap lava, which spans the K–T boundary (Keller et al., 2008). Some workers believed that the Deccan Trap volcanism triggered the K–T boundary mass extinction event (Wignall, 2001; Benton, 2003; Keller, 2005). The huge emission of volatile material associated with the Deccan Trap eruptions (killer with a smoking gun!, cf. Wignall, 2004, p. 130) had the potentiality for drastic perturbation of the global environment (Self et al., 2006) including a lethal rise in temperature (Keller, 2005) and other stresses (Keller and Pardo, 2004). Keller et al. (2008) documented the biotic effects of the Deccan volcanism on the foraminiferal assemblage in Rajahmundry and argued that the Deccan eruption was causally related to the K–T mass extinction (but see Alvarez et al., 1980 and a subsequent large body of literature which favored the impact model). Rajahmundry is the only place in India where the Deccan basalt (the majority of which erupted over less than 0.8 m.y.; see Keller et al., 2008) lies on top of a marine assemblage of the latest Maastrichtian age. Majority of the macrofauna and foraminifera became extinct at this point (manuscript under

217

preparation) and the first Paleocene bed (known as Intertrappean bed) yielded the Early Danian microfossils (Keller et al., 2008). It may be possible that many predators and prey died due to the stress related to the emission of lava. Mass extinction might influence drilling frequency and predator behavioral stereotypy by eliminating more escalated prey (Kelley and Hansen, 1996a; for opposite views see Hansen et al., 1999; Reinhold and Kelley, 2005). Kelley and Hansen (1993) found a decline in drilling frequency across the K–T boundary. We also examined the gastropod assemblage for naticid predation from the Intertrappean bed immediately overlying the K–T boundary and assessed the impact of mass extinction. 2. Material and methods The samples were collected following the bulk sampling (see Kowalewski, 2002) and random surface sampling protocols from the Infratrappean (latest Maastrichtian bed). Infratrappean bed is a calcareous sandstone having average 40 cm thickness and occurs in two small areas (Mallick et al., 2013). Detailed geological setting and age of the Infratrappean bed had been already dealt with in a previous paper (see Mallick et al., 2013). All total 14 bulk samples from the Infratrappean bed were collected in two consecutive field trips (2011 and 2012) from two sections (see Mallick et al., 2013; Fig. 1). Each bulk sample was put in plastic bags of 32 cm × 23 cm size. In the laboratory, all gastropods were separated from other taxa by hand and pincer. For smaller specimens (b 10 mm), we used sieves (ASTM No. 5, 10, 20) to separate them from larger ones. Intertrappean bed containing fossils crops out in Duddukuru area and has average thickness of 140 cm. It is a heterolithic facies having mainly limestone, chert and mudstone layers (Fig. 1; see also Keller et al., 2008; Mallick et al., 2013). Fossiliferous intertrap is exposed only in quarry sections in Soma mines where basalts have been excavated for building and road materials. Fossils are extremely patchy within the intertrap. We fortunately encountered fossil assemblages only in a recently opened section (about 100 m long). Even within a few meters of this section, fossils disappeared and thus, rendering the rock completely barren. Besides, quarry sections are very steep and beds were often not accessible. Because of this nature of fossil record and outcrop condition, we could not devise any systematic sampling design, like bulk or grid sampling protocol. Instead, we employed random surface sampling and collected all specimens we encountered, including small and large and broken and intact. When fossils were small and loosely found within weathered sediments, we used sieve (ASTM No. 5, 10, 20) to separate them from matrix. Our search was intense and we worked for two consecutive days at this particular locality in two consecutive years (2011 and 2012). The hours we spent per day were 4 to 5. Gastropod specimens were identified at the species level following previously published literature (Stoliczka, 1868; Wade, 1926; Krishnan, 1960; Sohl, 1963; Ladd, 1972; Taylor et al., 1983; Bandel, 2000; Saul and Squires, 2008). Both complete and identifiable broken shells were included to document gastropod diversity of these two assemblages. The Infratrappean assemblage included 31,929 gastropod specimens, representing 40 species and 27 genera, belonging to 20 families (Table 1). The Intertrappean assemblage included 164 specimens, consisting of 16 species belonging to 9 genera and 6 families (Table 2). While, 24 species out of 40, in the Infratrappean assemblage, were represented by a few (b10) or solitary specimens, 29,014 specimens belonged to the turritelline subfamily. This high abundance of turritelline gastropods led us to conclude that the Infratrappean gastropods represented a turritelline-dominated assemblage (TDA, see also Mallick et al., 2013). TDA was first defined by Allmon and Knight (1993) as “dense macrofossil assemblages of low total diversity (b~20 species) in which turritellines are more than two to three times as abundant as the next most common species”. However, in Allmon (2007) TDA was defined as any assemblage constituting at least 20% turritelline species, thus suggesting the possibilities of high diversity in this

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Fig. 1. Regional lithostratigraphy in Rajahmundry based on composite sections. Arrow indicates fossiliferous horizons (Infratrappean and Intertrappean beds). Modified after Mallick et al. (2013).

assemblage. We explained why the present assemblage was a TDA in spite of having high diversity (see Mallick et al., 2013). 99.44% of the turritelline specimens in the present assemblage belonged to Turritella dispassa, two other species, Turritella neptuni and Turritella cf. pondicheriensis, represented only 0.56% of the turritelline assemblage. Since taxonomy of turritelline gastropods is not well established, we followed Dudley and Vermeij (1978) and Allmon et al. (1990), and considered Turritella sensu lato as a catch-all genus. The present species were provisionally assigned to it. Small turritelline shells occurred side by side with the larger ones (shell size varies from 1 mm to 5–6 cm in height). Small specimens had fewer whorls and were indistinguishable from early whorls of the larger specimens. This indicates that small specimens were juveniles of the large, adult species. There was no preferential alignment of the turritelline shells on the bed surface (see Mallick et al., 2013; Fig. 5). Many gastropod species retained their delicate ornamentation and pristine color patterns. Some bivalves were found articulated and very thin shelled bivalve shells were also present. We, therefore, believed that the present TDA represented a biocoenosis i.e. a naturally occurring live assemblage (see also Mallick et al., 2013). Cerithium cf. limbatum (maximum height b2 cm.) was the second most abundant (N = 1585) gastropod species in the assemblage. Other gastropod species had varying individuals and their abundances were shown in Table 1. 2.1. Predator identification The drillholes showed some degree of variation in shape, size, and internal structures. However, the majority of them were circular in outline, with beveled, parabolic walls (see Mallick et al., 2013; Fig. 6). The holes were perpendicular to the shell surface. This type of drillholes, Oichnus paraboloides, is generally attributed to naticid predation (Carriker and Yochelson, 1968; Bromley, 1981; but see Dietl et al., 2004; Daley et al., 2007). None of the drillholes was cylindrical with straight-sided walls, typical of muricid predation. Small shells, when examined under SEM, clearly revealed naticid drillhole morphology (see Mallick et al., 2013; Fig. 6). Our collection included one species of naticid, Mammilla carnatica, which was common (N = 414), and one

species of muricid (Neptunea rhomboidalis) which was rare (N = 8). We, therefore, argued that drillholes in our bulk samples were made by mainly naticid predators (see Taylor et al., 1983; Allmon et al., 1990 for similar inference). 2.2. Drilling frequency 5884 complete or near complete (i.e. only apertural and/or apical part partially broken) gastropod specimens from the Infratrappean bed were analyzed to measure drilling frequencies (DF) in both assemblage as well as lower-taxon levels (family and species; see Table 1). The younger Intertrappean bed had much less complete specimens (N = 46) and not a single shell contained drillhole (Table 2). Intertrappean gastropods, therefore, were excluded from the analysis. Broken specimens were also studied to see any taphonomic influence on drilled specimens (Roy et al., 1994; and see also Kelley and Hansen, 2006). Study of the broken specimens showed no taphonomic bias against drilled specimens. We found no significant evidence of breakage through holes in drilled specimens. Drilling, in contrast, may also increase the chance of preservation of shells when a naticid predator takes its victim within the sediments before drilling (Edwards, 1974). Transportation of drilled and undrilled specimens may have different entrainment velocities and thus can undergo differential sorting (Yanes et al., 2012; Chattopadhyay et al., 2014). But, Kelley (2008) did not find any taphonomic bias between drilled and undrilled shells in the fossil record. We already mentioned that the present assemblage did not suffer much posthumous transport. We, therefore, considered equal potentialities of drilled and undrilled shells for preservation in this assemblage (see also Dudley and Vermeij, 1978; Allmon et al., 1990; Mallick et al., 2013). DF was defined as percentage of shells with complete drillholes divided by the total number of shells (Allmon et al., 1990). Assemblagelevel DF was measured as the ratio between the number of drilled specimens by the total number of specimens in an assemblage. This method is similar to the assemblage frequency (AF) method in Kowalewski (2002), where DF = Di / Ni, Di is the number of specimens of i-th species with at least one drillhole and Ni is the number of specimens of the i-th species. Similarly, family-level DFs were calculated as the lower

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Table 1 List of families, species, number of individuals (total and intact) and corresponding drilling frequencies (DFs) found in the Infratrappean bed of the latest Maastrichtian age, Rajahmundry, India. Drilling frequencies were determined at both species and family levels based on intact specimens (N). Family

Species

Total specimens (intact + broken)

N (intact)

D (species)

DF (species)

D (family)

DF (family)

Naticidae

Mammilla carnatica Mammilla sp. Ampullina bulbiformis Neptunea rhomboidalis Hemifusus cf. acuticostatus Athleta sp. Volutilithes radula Pugnellus sp. Cancellaria (Euclia) breviplicata Cancellaria sp. 1 Cancellaria sp. 2 Cancellaria sp. 3 Paladmete sp. Pleurotoma subfusiformis Cerithium cf. limbatum Cerithium trimonile Cerithium stoddardi Pseudomelania undosa Pseudomelania sp. 1 Pseudomelania sp. 2 Turritella (Torcula) dispassa Turritella neptuni Turritella (Torcula) cf. pondicheriensis Melanatria sp. Lacrimiforma cf. secunda Pseudoliva subcostata Pseudoliva cf. elegans Calyptraea sp. Rostellaria palliata Euchrysalis gygantea Bellifusus aff. Indicus Paleopsephaea latisepta Pyrifusus (Beisselia) oldhaminus Tubulostium callosum Scala striatocostata Patella sp. B Patella sp. A Pseudamaura sp. Pseudamaura nobilis Littorina acicularis

428 2 13 12 41 36 7 1 94 5 48 7 5 56 1532 9 1 28 39 8 28,851 147 16 2 21 4 5 2 107 6 297 7 4 36 5 28 2 8 5 4 31,929

414 1 11 8 33 29 4 1 81 2 43 … 1 46 1121 5 … 23 32 3 3449 112 2 1 17 2 2 … 94 3 272 38 2 … … 23 … 5 3 1 5884

15 … 2 1 10 2 … … 6 … 1 … … 3 664 … … 4 9 2 906 3 … … 2 … … … 4 1 61 … … … … … … … … … 1696

0.04 … 0.18 0.13 0.30 0.07 … … 0.07 … 0.02 … … 0.07 0.59 … … 0.17 0.28 0.67 0.26 0.03 … … 0.12 … … … 0.04 0.33 0.22 … … … … … … … … … 0.29

15

0.04

2 1 10 2

0.18 0.13 0.30 0.06

7

0.06

3 679

0.07 0.57

909

0.26

… 2

… 0.10

… 4 1 61

… 0.04 0.33 0.20

… … …

… … …

…

…

…

…

Ampullinidae Muricidae Melongenidae Athletidae

Cancellaridae

Pleurotomidae Cerithidae

Turritellidae

Thiaridae Buccinidae

Calyptridae Strombidae Eulimidae Pyrifusidae

Vermetidae Scalidae Patellidae Pseudamauridae Littorinidae Total assemblage

taxon frequency (LTF) method in Kowalewski (2002), LTF = Dk / Nk, where k is the specific family, D is the number of specimens of that family with at least one drillhole, and N is the total number of specimens of that family. Table 2 List of families, species and number of individuals (total and intact) found in the Intertrappean bed of the Early Danian age, Rajahmundry, India. Note that no complete/incomplete drillholes were found in the entire assemblage. Family

Species

Total specimens (intact + broken)

N (intact)

Cerithiidae

Gourmya sp. 1 Gourmya sp. 2 Cerithium (Bellardia) naricum Cerithium stoddardi Cerithium trimonile Cerithium Type 2 Cerithium Type 3 Bittium sp. Bartrumella waitakerensis Physa sp. 1 Physa sp. 2 Protoma retrodilatatum Cantharidus aff. striolatus Semisolarium sp. 1 Semisolarium sp. 2 Euspira sp.

17 1 13 8 1 35 2 54 25 1 1 2 1 1 1 1 164

8 1 9 3 1 3 2 4 8 1 1 1 1 1 1 1 46

Pyramidellidae Physidae Turritellidae Trochidae

Naticidae

Although the present Infratrappean assemblage included a great diversity of gastropod species (see, Table 1), all species were not targeted by naticid predators. To understand the relation between relative abundance of species (Fig. 2) and DF (Fig. 3), we used Spearman rank correlation. Following Vermeij (1987), prey species with 10 or more individuals were incorporated in this analysis. 2.3. Incomplete and multiple drilling frequencies Incomplete drillholes were those that failed to penetrate to the shell interior and multiple drillholes indicated more than one hole in a specimen by successive predation attempt (Vermeij, 1987; Kelley et al., 2001). But, in case of muricids, multiple holes could represent simultaneous attacks (Kelley, pers. com.) A number of studies suggested that incomplete drilling frequency and multiple drilling frequencies indicated the ability of the prey to minimize the predation mortality (Kelley and Hansen, 1993, 1996a; Kelley et al., 2001) and hence increased the prey resistance against predation. However, other studies suggested that incomplete drillholes may not necessarily indicate failed attack (see Ansell and Morton, 1987 and Hutchings and Herbert, 2013 for an alternative hypothesis where prey with incomplete borings were consumed by suffocation). Hutchings and Herbert (2013) suggested that decrease in incomplete drillhole intensity may result from decreased competition among predators, rather than any attributes of prey species. In the present study, we maintained that incomplete drilling

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Fig. 2. Most abundant species (n N 10) and corresponding number of individuals collected from the Infratrappean bed of the latest Maastrichtian age, Rajahmundry, India.

frequency indicated unsuccessful drilling attempt, irrespective of the source (see also Visaggi et al., 2013). Incomplete drilling frequency (PE) was measured as the ratio between the number of incomplete drillholes and the number of total attempted drillholes (including both successful and unsuccessful drillholes). Multiple drilling frequency (MULT) was measured as the proportion of drillholes that occurred in multiply bored specimens (see Kelley and Hansen, 1993). Similar to DF, PE and MULT were also measured at the assemblage-level and species-level, separately (Table 3).

2.4. Temporal trend in DF, PE and MULT In order to understand the temporal trend in naticid predation, comparisons were made between successful and unsuccessful drilling frequencies of the present study and those of other Cretaceous and Paleogene examples which were available in the literature (sources are, Taylor, 1970; Adegoke and Tevesz, 1974; Taylor et al., 1983; Arua and Hoque, 1989; Allmon et al., 1990; Kelley and Hansen, 2006). We compared with the Paleogene data because high modern values of DF and PE were already achieved during this interval (Dudley and Vermeij, 1978; Vermeij et al., 1980; Kelley and Hansen, 1993). From previously published literature, we compiled a list of all naticid drilling results on gastropod prey taxa during the Cretaceous through the Oligocene (Table 4). Both assemblage-level and family-level comparisons were used to understand the variation of drilling intensity at various taxonomic levels. In the Cretaceous all the previously documented drilling data came from different stratigraphic levels, ranging from the Albian to the Maastrichtian of North America and Western Europe. Therefore, the inclusion of our Indian subcontinent results would also facilitate our present understanding of geographically mosaic pattern of drilling intensity. Similar procedure was followed to evaluate temporal trend in PE and MULT (Table 5). 2.5. Behavioral stereotypy

Fig. 3. Most abundant (N N 10) and frequently drilled (DF N 10%) species from the Infratrappean gastropod assemblage.

One of the measures of predator efficiency is the stereotypic nature of successful predation (Kelley and Hansen, 1993). As we recorded high intensity drilling in the present gastropod assemblage it was expected that predatory naticids were quite efficient. In order to test this hypothesis, we investigated the site selectivity of naticid drillholes, in terms of both radial and vertical positions. To understand the behavioral stereotypy of the Cretaceous naticid predators, we selected four species of four different families to determine the site and size stereotypy — Turritella dispassa from the Turritellidae, Cerithium cf. limbatum of the Cerithiidae, Bellifusus aff. indicus of the Pyrifusidae and Mammilla carnatica of the Naticidae family

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Table 3 Number of incomplete drillholes, PE, multiple drillholes and MULT in the Infratrappean assemblage have been shown. Species

No. of incomplete drillholes

PE (species)

PE (family)

No. of multiple drillholes

MULT (species)

MULT (family)

Mammilla carnatica Mammilla sp. Ampullina bulbiformis Neptunea rhomboidalis Hemifusus cf. acuticostatus Athleta sp. Volutilithes radula Pugnellus sp. Cancellaria (Euclia) breviplicata Cancellaria sp. 1 Cancellaria sp. 2 Cancellaria sp. 3 Paladmete sp. Pleurotoma subfusiformis Cerithium cf. limbatum Cerithium trimonile Cerithium stoddardi Pseudomelania undosa Pseudomelania sp. 1 Pseudomelania sp. 2 Turritella dispassa Turritella cf. pondicheriensis Turritella neptuni Melanatria sp. Lacrimiforma cf. secunda Pseudoliva subcostata Pseudoliva cf. elegans Calyptraea sp. Rostellaria palliata Euchrysalis gygantea Bellifusus aff. Indicus Paleopsephaea latisepta Pyrifusus (Beisselia) oldhaminus Tubulostium callosum Scala striatocostata Patella sp. A Patella sp. B Pseudamaura sp. Pseudamaura nobilis Littorina acicularis Total assemblage

5 … … … … … … … 3 … … … … … 15 … … … 1 … 24 … … … … … … … … … 1 … … … … … … … … … 49

0.25 … … … … … … … 0.33 … … … … … 0.02 … … … 0.17 … 0.03 … … … … … … … … … 0.02 … … … … … … … … … 0.03

0.25

… … … … … … … … … … … … … … 48 … … 2 … … 49 … … … … … … … … … 2 … … … … … … … … … 101

… … … … … … … … … … … … … … 0.07 … … 0.50 … … 0.05 … … … … … … … … … 0.03 … … … … … … … … … 0.06

…

(Figs. 4 and 5). The common basis for selecting this four species was that they were most abundant (N N 250) (see, Fig. 2). We measured the position of drillholes in the vertical profile and radial quadrant systems (following Allmon et al., 1990; Hagadorn and Boyajian, 1997). To understand whether the Cretaceous predatory naticids were size selective, we plotted outer borehole diameter (OBD), which served as proxy for the predator size (see for example, Anderson et al., 1991), against maximum whorl diameter (MWD) of prey shell. Drilled and undrilled shells were classified into different size categories (with 0.5 mm size interval). Initially, the distribution of drillholes within various prey size classes was compared to determine whether predators were selective with respect to prey body size (Fig. 6). Afterwards the distribution of drilled and undrilled shells was compared to determine prey size preference (Fig. 7).

2.6. Statistical analysis Two tailed Chi-square test of independence was used to compare between successful and unsuccessful drilling intensities of the present study and previous studies. Chi-square test was also used to determine statistical significance of drillhole site preference. Prey size selectivity was measured with linear regression (least-square) and the correlation coefficient, Pearson's r, between maximum whorl diameter (prey length) and outer borehole diameter (proxy for predator size). For all these analyses, statistical significance was measured against an α-value of 0.05. All statistical

… … … …

0.33

… 0.02

0.03

… …

… … … 0.02

… … … … …

… … … …

…

… 0.07

0.05

… …

… … … 0.03

… … … … …

analyses were performed in the R programming environment (R development core team, 2007). 3. Results 3.1. Drilling frequency In the Infratrappean assemblage, 1696, out of a total of 5884 shells (28.82%) were drilled. Table 1 provides the complete list of 40 species found in the Infratrappean assemblage. Out of these 40 species, 34 species contained at least one complete or near complete specimen. Among 34 species, only 18 species were drilled. Present gastropod assemblagelevel DF for the Infratrappean bed was 28.82% (N = 5884). The high value of assemblage-level DF was also reflected in the lineage-level data (mainly for the Turritellidae and the Cerithiidae). However, DF for the Naticidae showed low value for our Cretaceous assemblage (see Table 1). When only drilled species were considered, there was no statistically significant correlation between the number of specimen and species-level drilling intensity (Spearman's rank correlation, r = −0.28, p = 0.27). 3.2. Incomplete and multiple drilling frequency In the assemblage-level, Rajahmundry gastropods showed about 3% and 6% incomplete and multiple drillhole frequencies respectively (Table 3).

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Table 4 Temporal distribution (Cretaceous to Oligocene) of gastropod drilling frequencies at assemblage-level and three lineage (Turritellidae, Cerithiidae, Naticidae) levels. Temporal data were tabulated from the present study and previously published literature. Geographic location/Formation

Age

Gastropod assemblage

Rajahmundry Infratrap Pierre Shale (Manitoba) Fox Hill (WIS) Ripley (Georgia) Providence (Georgia) Blackdown Greensand (England) Ripley (South-eastern U.S.A.) Mississippia Alabamaa Rajahmundry Intertrap Brightseat (Maryland) Matthews Landing (Alabama) Bells Landing (Alabama) Alabamaa Virginiaa Virginiaa Paris Basina Paris Basina Ameki Formation (Nigeria) Mississippia Alabamaa Alabamaa Mississipia Louisianaa Texasa Bashi (Virginia) Cook Mountain (Texas, Louisiana) Gosport (Alabama) Moodys Branch (Louisiana, Mississippi) Mississippia Red Bluff (Mississippi) Mint Spring (Mississippi) Byram (Mississippi) Belgrade (North Carolina)

Latest Maastrichtian Campanian Maastrichtian Maastrichtian Maastrichtian Albian Maastrichtian Campanian Campanian Early Danian Early Paleocene Middle Paleocene Late Paleocene Paleocene Paleocene Paleocene Eocene Eocene Middle Eocene Eocene Eocene Eocene Eocene Eocene Eocene Early Eocene Late Middle Eocene Late Middle Eocene Late Eocene Oligocene Early Oligocene Early Oligocene Early Oligocene Late Oligocene

Turritellidae

Cerithiidae

Naticidae

References

N

DF

N

DF

N

DF

N

DF

5884 458 … 2426 516 3894 … … … 46 414 297 742 … … … … 2767 1157 … … … … … … 271 2761 200 1291 … 329 737 178 348

0.29 0.03 … 0.04 0.06 0.05 … … … 0.00 0.38 0.47 0.35 … … … 0.26 0.12 0.28 … … … … … … 0.20 0.16 0.08 0.08 … 0.12 0.15 0.17 0.12

3563 15 … 589 175 706 46 140 13 1 237 132 562 246 179 14 … 519 265 70 39 68 45 30 30 70 546 134 289 45 84 26 8 14

0.26 0.20 … 0.04 0.13 0.04 0.09 0.04 0.00 … 0.54 0.58 0.43 0.17 0.19 0.07 0.63 0.00 0.27 0.21 0.00 0.13 0.09 0.60 0.03 0.39 0.24 0.09 0.12 0.02 0.26 0.39 0.38 0.14

1184 … … … … 174 24 … … 31 … … … … … … … … … … … … … … … … … … … … … … … …

0.57 … … … … 0.01 0.13 … … 0.00 … … … … … … …. … … … … … … … … … … … … … … … … …

415 403 … 167 137 302 110 … … 1 18 15 46 … … … … 152 243 … … … … … … 74 228 10 54 … 72 229 41 40

0.04 0.02 0.04 0.01 0.03 0.03 0.00 … … 0.00 0.17 0.20 0.07 … … … … 0.10 0.14 … … … … … … 0.07 0.14 0.20 0.15 … 0.01 0.11 0.17 0.15

A B C D D E F G G A D D D H H G I J K G G H H H H D D D D H D D D D

N = number of specimens, D = number of drilled specimens. Data sources are, A = Present study; B = Li et al. (2011); C = Jones et al. (1998); D = Kelley and Hansen (2006); E = Taylor et al. (1983); F = Vermeij and Dudley (1982); G = Dudley and Vermeij (1978); H = Allmon et al. (1990); I = Fischer (1966); J = Taylor (1970); K = Adegoke and Tevesz (1974). a Formations not specified.

Table 5 Temporal distribution (Cretaceous to Oligocene) of incomplete and multiple drilling frequencies at assemblage-level and three lineage (Turritellidae, Cerithiidae, Naticidae) levels. Geographic location/formation

Age

Rajahmundry Infratrap Blackdown Greensand (England) Ripley (Georgia) Providence (Georgia) Rajahmundry Intertrap Brightseat (Maryland) Matthews Landing (Alabama) Bells Landing (Alabama) Alabama & Virginiaa Bashi (Virginia) Cook Mountain (Texas, Louisiana) Gosport (Alabama) Moodys Branch (Louisiana, Mississippi) Paris Basin Ameki Formation (Nigeria) Mississippia Red Bluff (Mississippi) Mint Spring (Mississippi) Byram (Mississippi) Belgrade (North Carolina)

Latest Maastrichtian Albian Maastrichtian Maastrichtian Early Danian Early Paleocene Middle Paleocene Late Paleocene Paleocene Early Eocene Late Middle Eocene Late Middle Eocene Late Eocene Eocene Middle Eocene Oligocene Early Oligocene Early Oligocene Early Oligocene Late Oligocene

Gastropod

Turritellidae

Cerithiidae

Naticidae

References

No

PE

MULT

No

PE

MULT

No

PE

MULT

No

PE

MULT

1799 201 91 31 0 156 138 264 … 56 470 17 140 527 392 … 40 113 37 45

0.03 … 0.01 0.00 … 0.00 0.00 0.01 … 0.02 0.05 0.12 0.26 0.04 0.12 … 0.03 0.05 0.14 0.09

0.06 0.03 0.04 0.00 … 0.00 0.34 0.02 … 0.04 0.10 0.12 0.18 … … … 0.23 0.16 0.19 0.15

957 … 25 22 0 128 93 225 84 28 32 11 26 … 75 1 25 10 3 2

0.03 … 0.00 0.00 … 0.00 0.00 0.01 0.06 0.00 0.13 0.18 0.00 … 0.04 0.00 0.04 0.00 0.00 0.00

0.05 … … … … … 0.33 0.02 … 0.07 0.22i+ 0.18 0.08 … … 0.00 0.20 … … …

721 … … … 0 … … … … … … … … … .. … … … … …

0.02 … … … … … … … … … … … … … … … … … … …

0.07 … … … … … … … … … … … … … … … … … … …

20 … 1 4 0 3 3 3 … .5 71 2 9 25 46 … 1 26 3 6

0.25 … 0.00 0.00 … 0.00 0.00 0.00 … 0.00 0.13 0.00 0.11 0.40 0.28 … 0.00 0.00 0.00 0.00

… … … … … … … … … … … … … … … … … … … …

A E L, M L, M A L, M L, M L, M H L, M L, M L, M L, M J K H L D D D

No = number of attacks. Data sources are, A = Present study; D = Kelley and Hansen (2006); E = Taylor et al. (1983); H = Allmon et al. (1990); J = Taylor (1970); K = Adegoke and Tevesz (1974); L = Kelley and Hansen (1993); M = Kelley et al. (2001). (+No = 135). a Formations not specified. + sign indicates the sample number from Kelley and Hansen (1993) (see Table no. 16 in p.372).

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demonstrated by us and briefly stated here. Drillhole sites were situated mainly at the middle part of the total shell height (present Fig. 4A), i.e., drillholes were restricted to the 2–3 whorls prior to the aperture. Here, we also analyzed behavioral stereotypy in three other abundant species. In Cerithium cf. limbatum (Cerithiidae), which were also turreted in form, drillholes were stereotyped and clustered at 2–3 whorls before the aperture (p b 0.01), i.e., at the middle part of the shell height (Fig. 4B). Most of the drillholes (86.54%) were located on the body whorl of Bellifusus aff. indicus (Pyrifusidae) (Fig. 4C). In Mammilla carnatica (Naticidae) the drillholes were scattered and there was no vertical stereotypy as such (Fig. 4D). We did not find any statistically significant preference for the radial location of drillholes on turritelline gastropods with respect to any particular quadrant (Fig. 5A; see also Mallick et al., 2013, Fig. 10). Analysis of the radial location of drillholes in Cerithium cf. limbatum suggested that quadrants I and II contained (Fig. 5B) more number of drillholes (68.22%) which were statistically significant (p b 0.01). 76.92% of drillholes were situated abaperturally (p b 0.01) in Bellifusus aff. indicus (Fig. 5C). Like vertical distribution, radial stereotypy was not present in Mammilla carnatica (p = 0.58) (Fig. 5D), although most of the drillholes (73.33%) were situated in the apertural side aligning along the axis of coiling. Mallick et al. (2013) also documented in detail the size selectivity of naticid predation on Turritella dispassa. We updated the dataset with recent addition of more samples. When outer borehole diameter (OBD) was regressed on the maximum whorl diameter (MWD) of the prey shell (Fig. 6A), prey and predator sizes displayed a significant positive correlation (r = 0.68, p b 0.01). In the case of Cerithium cf. limbatum (Fig. 6B) prey size and predator size were weakly correlated, but still significant (r = 0.42, p b 0.01). Fig. 6C and D showed that size selectivity was better expressed in case of Bellifusus aff. indicus and Mammilla carnatica (r = 0.64, p bb 0.01 and r = 0.78, p bb 0.01 respectively). Fig. 7 showed the size–frequency distributions of the drilled and the undrilled individuals of the abovementioned four species. Size distribution of the drilled and the undrilled specimens of these four species did not differ significantly (Kolmogorov–Smirnov test, p b 0.05); all of these four distributions showed that smaller individuals were preferentially targeted by naticid predators. 4. Discussion

Fig. 4. Schematic diagrams showing vertical distribution of drillholes on different gastropod prey taxa. A) T. dispassa (modified after Mallick et al., 2013); B) Cerithium cf. limbatum (n = 664); C) Bellifusus aff. indicus (n = 61) and D) Mammilla carnatica (n = 15).

At the family-level we found that only five gastropod families (Turritellidae, Naticidae, Cerithiidae, Pyrifusidae and Cancellaridae) contained incomplete holes from our entire collection. Incomplete drilling frequency (PE) for the Turritellidae and the Cerithiidae was 2.51% and 2.22% respectively. But, for the Naticidae, the present PE value was very high (PE = 25%). For two other families (Pyrifusidae and Cancellaridae) the PE values were 2% and 33% respectively. At the family-level we found that only three gastropod families (Turritellidae, Cerithiidae and Pyrifusidae) contained multiple holes from our entire collection. MULT for the Turritellidae was 5.12%. For the Cerithiidae and Pyrifusidae, the present values were 6.93% and 3% respectively.

3.3. Behavioral stereotypy In a previous contribution (Mallick et al., 2013) stereotypy of drillhole site in one turritelline species, Turritella dispassa was

Among 40 gastropod species of the present study 18 were drilled (45%). Of these 18 species 15 (83.33%) were abundant (≥ 10 specimens). Among abundant species, 8 species (53.33%) were significantly drilled (N 10%) (Fig. 3). All these above measures indicated high and efficient predation in the present gastropod assemblage. Proportion of the drilled species in the present Cretaceous assemblage was very similar to other previously published Cretaceous records (see Kelley and Hansen, 2006). Two abundant species, Paleopsephaea latisepta (N = 38) and Patella sp. B (N = 23) were not drilled. Patella sp. B was a limpet; being an epifaunal encruster, it was not targeted by the naticids which are mainly infaunal predators. The other species, P. latisepta had many escalated features like large size (2.7–6.5 cm), thick shell (0.51– 1.75 mm) and strong ornamentation and thus was well adapted against naticid predation. 4.1. Temporal trend of drilling frequency In order to facilitate our present understanding of naticid drilling frequency over temporal scale, we compared our present drilling dataset with previously published records (Tables 4 and 6). All previous Cretaceous DFs on gastropods at both assemblage and lower-taxon levels showed lower values. At the assemblage level previous DFs varied from 3 to 6% (Table 4), while the present DF of Rajahmundry gastropod assemblage was significantly higher (29%) (for pair-wise comparisons, see Table 6). Drilling frequency reached a new high in the Paleocene

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Fig. 5. Radial distribution of drillholes on the gastropod prey taxa. A) T. dispassa (modified after Mallick et al., 2013); B) Cerithium cf. limbatum (n = 664); C) Bellifusus aff. indicus (n = 61) and D) Mammilla carnatica (n = 15).

(Table 4). This is evident from the fact that drilling frequencies of previous reports ranged from 35 to 47%, which is even significantly higher than our present assemblage (Table 6). On the other hand, all drilling

frequencies of the Eocene and Oligocene, except the middle Eocene Ameki Formation of Nigeria, were significantly lower than our Infratrappean assemblage (Tables 4 and 6).

Fig. 6. Prey size selectivity of naticid predators on gastropod prey. The lines represent linear regression (least-square) between prey size (estimated by maximum whorl diameter) and predator size (estimated by outer borehole diameter). A) T. dispassa (modified after Mallick et al., 2013; MWD = 0.15 OBD + 0.66, p b 0.01); B) Cerithium cf. limbatum (N = 664; MWD = 0.19 OBD + 0.19, p b 0.01); C) Bellifusus aff. indicus (N = 61; MWD = 0.15 OBD + 0.63, p bb 0.01) and D) Mammilla carnatica (N = 15; MWD = 0.10 OBD + 0.42, p bb 0.01).

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Fig. 7. Histogram showing distribution of drilled (gray shade) and undrilled (black) shells of the gastropod prey taxa. A) T. dispassa (modified after Mallick et al., 2013); B) Cerithium cf. limbatum (n = 664); C) Bellifusus aff. indicus (n = 61) and D) Mammilla carnatica (n = 15).

Table 6 Results of chi-square test for comparisons of drilling frequency (DF), incomplete drilling frequency (PE) and multiple drilling frequency (MULT) of the Rajahmundry gastropods (assemblage and family levels) with other previously published reports. Numbers indicate the Chi-square values and *** indicates p b 0.001, ** indicates p b 0.01, * indicates p b 0.05, others p N 0.05. Location/ formation

DF

PE

MULT

Pierre Shale Fox Hill Ripley Providence Blackdown Greensand Ripley Mississippi Alabama Brightseat Matthews Landing Bells Landing Alabama Virginia Virginia Paris Basin Paris Basin Ameki Formation Mississippi Alabama Alabama Mississippi Louisiana Texas Bashi Cook Mountain Gosport Moodys Branch Mississippi Red Bluff Mint Spring Byram Belgrade

140.79*** … 642.10*** 125.34*** 852.04***

0.24 … 131.03*** 14.94*** 164.16***

… … … … 195.59***

0.89 … 4.05* 0.15 0.52

… … … … …

… … … … …

… … … … …

… … … … …

… … … … 2.26

… … … … …

… … … … …

… … … … …

… … … 14.62*** 42.16***

6.8** 32.62*** 4.45* 90.94*** 66.93***

19.25*** … … … …

4.09* … … 7.38** 9.69**

0.85 … … … …

… … … … …

… … … … …

… … … … …

0.22 … … … 103.18***

… … … … 73.98***

… … … … …

… … … … …

12.77*** … … … … 277.95*** 0.07

75.78*** 7.92* 3.84 2.48 … 170.34*** 0.36

… … … … … … …

0.93 … … … … 8.68** 23.95***

2.27 … … … … 2.08 59.69***

1.48 2.76 … … … … 0.41

… … … … … … …

… … … … … 0.57 0.043

7.45** … … … … … …

5.55* … … … … … …

… … … … … … …

… … … … … … …

… … … … … … 160.89*** 160.89*** 43.51*** 241.08*** … 44.58*** 62.52*** 12.16*** 45.87***

0.6 13.31*** 5.32* 6.50* 18.48*** 7.74** 6.12* 0.58 18.93*** 25.95*** 12.78*** 0.02 2.27 0.6 0.93

… … … … … … … … … … … … … … …

… … … … … … 1.58 23.59*** 6.83** 12.85*** … 0.96 13.51*** 14.72*** 10.74**

… … … … … … … … 4.40* 126.60*** … 44.58*** 2.35 13.16*** 6.28*

… … … … … … … 9.24** 7.85** … … 0.14 … … …

… … … … … … … … … … … … … … …

… … … … … … … 1.26 … 0.12 … … … … …

… … … … … … … … 1 25.63*** … … 15.77*** 9.63** 4.9*

… … … … … … … 42.30*** 2.57 0.18 … 7.33** … … …

… … … … … … … … … … … … … … …

… … … … … … … … … … … … … … …

Assemblage Turritellidae Cerithiidae Naticidae Assemblage Turritellidae Cerithiidae Naticidae Assemblage Turritellidae Cerithiidae Naticidae

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This was also true even at lower taxon family-level (Tables 4 and 6). For example, for Turritellidae, Kelley and Hansen (2006) calculated DF ranging from 4 to 13% during the Cretaceous, while DF was 25% in the present assemblage. Previously, Mallick et al. (2013) reported DF for the Rajahmundry Turritellidae as 23% based on 1869 complete specimens. DF value for the Cretaceous Cerithiidae, although found in a single formation (Blackdown Greensand Formation of England), was 0.57%, whereas in the present Maastrichtian assemblage it was as high as 57.26%. This value was one of the highest DFs ever achieved during the Cenozoic fossil record (in other example, DF = 57.6% for the Turritellidae on the Mathews Landing Formation of the Paleocene; see Kelley and Hansen, 2006). DF values of the present assemblage-level as well as family-level for the Turritellidae matched well with many DFs of the Cenozoic especially Eocene (see Table 4). Unlike the Turritellidae or the Cerithiidae, drilling frequency for the Naticidae was low in our Cretaceous assemblage (3.6%), which was not statistically significantly different from most of the previous Cretaceous reports (Tables 4 and 6). However, when compared with the Cenozoic values, present drilling frequency for the Naticidae was significantly lower than most of the previous records (see Tables 4 and 6). Confamilial naticid DF during the Cretaceous was low in all areas. Naticid indulged in cannibalism or conspecific predation since the Cretaceous (Kelley and Hansen, 2007b). In the present study the naticids were almost monotypic and dominated by Mammilla carnatica (see Table 1). It was apparent that confamilial predation in Rajahmundry was actually cannibalism. The present conspecific DF was also low and did not mimic the assemblage level data which was quite high. Low naticid DF was not even correlated with the abundance of naticids. This was also true for the present assemblage as well as for the all Cretaceous assemblages from elsewhere (Table 4). It was believed by some early workers that this low confamilial or cannibalistic predation behavior was due to the absence of other prey especially bivalves (Paine, 1963; Taylor, 1970) or due to the inaptitude of naticid predators (see Kelley, 1991 for other references). In Rajahmundry not only the gastropod prey were available, but bivalves were also present (Pascoe, 1964; Malarkodi et al., 2009, 2010). Naticid drillholes were also found in some of them (MS in preparation). Low Cretaceous DF on naticid may indicate that naticid predation on naticid was not popular or predators were inexperienced. If the theory of escalation of Vermeij (1987) is true, then it was expected that skill of confamilial or conspecific drilling also evolved with time (see also Kelley and Hansen, 2007b). Low DF and poor site stereotypy (but stereotypy already developed on other prey groups e.g. turritellines) of the present study of Cretaceous naticids were consistent with this expectation. However, size stereotypy in Rajahmundry intraspecific naticid predation was already well developed (Fig. 6D). 4.2. Temporal trend of PE and MULT When we compared the present incomplete drilling frequency data with the previously published studies, it was evident that incomplete drillholes were very rare in the Cretaceous and the Paleocene samples (see Table 5). When compared with the Eocene assemblages, our Cretaceous PE was also not statistically significantly different from the Bashi Formation and the Paris Basin samples, but significantly lower than the Cook Mountain, Gosport, Moodys Branch and Ameki formations (see Tables 5 and 6). Three, out of four previous records of the Oligocene assemblages, showed significantly higher PEs than the present Cretaceous assemblage. PE for the present Turritellidae was 2.51%. From the global data it can be seen that PE varied in a fluctuating manner throughout the Paleogene. Some values (e.g., Alabama and Virginia areas of the Paleocene; Ameki Formation of the Middle Eocene and Red Bluff Formation of the Early Oligocene) were not significantly different than the present value (see Table 6), but other values (Bells Landing Formation of the Late Paleocene, Cook Mountain and Gosport formations of the Late

Middle Eocene) were significantly different from the present value (see Tables 5 and 6). For the Naticidae our present PE was 25%. Incomplete drillholes were reported only from the Eocene. When we compared the present PE value of the Naticidae with the Eocene values we found that some values (Cook Mountain Formation and Paris Basin) were significantly different than the present value (see Table 6), but other values (Moodys Branch and Ameki formations) were not significantly different from the present value (see Table 6). Kelley and Hansen (1993) provided a detailed list (see their Table 15) for MULT from the Cretaceous to Oligocene. In the Cretaceous Ripley Formation, assemblage level MULT was 4.4% and was comparable with the present result (5.61%) (see Table 6), whereas for the Providence Formation MULT was zero. MULT, like the temporal trend showed by PE, also varied in a fluctuating manner throughout the Paleocene to Oligocene. Some values (Bashi and Blackdown Greensand formations) were not significantly different from the present value (see Table 6), but other values (e.g., Matthews Landing, Cook Mountain formations) were significantly different from the present value (see Table 6). Kelley and Hansen (1993) gave MULT for the Turritellidae and showed that it fluctuated throughout the Paleogene. Some values (e.g., Matthews Landing, Cook Mountain, Red Bluff and Bells Landing formations) were significantly different from the present value (for statistical comparisons see Table 6), but other values (e.g., Gosport, Bashi, and Moodys Branch formations) were not statistically significantly different from the present value (see Table 6). 4.3. Behavioral stereotypy Frequency distributions of drilled and undrilled specimens (Fig. 7) demonstrated that most of the drilled specimens were smaller in size. At the same time, it was also true that undrilled specimens were also smaller and abundant in most of the cases (Fig. 7A, B). It may suggest that the availability or abundance of the prey species was the causal factor of this stereotyped predatory behavior. However, this pattern was not applicable for the Bellifusus aff. indicus (Fig. 7C), where intermediate-sized prey was most common, but smaller sized individuals were most frequently drilled. It is interesting to note that the naticids were also strongly skewed (skewness = 0.97) towards smaller individuals (Fig. 7D). This may alternatively suggest that prey size preference of predators, rather than prey abundance, played the dominant role in establishing size stereotypy. Dietl and Alexander (2000) stated that, site selectivity of confamilial predation was necessary to reduce chances of becoming a victim of their own prey during the encounter. Apertural site selection implied that foot of the dangerous prey could be blocked and thus reduce the risk. Alternatively, however one could argue that naticids could have attacked without any behavioral stereotypy but only those lucky ones that happened to attack the apertural area produced successful drillholes. Thus, the observed site selectivity may reflect differential success and may not be behavioral stereotypy. Besides, naticid prey was highly mobile and infaunal. Kelley and Hansen (2007b) stated that cannibalism required greater predatory skill and it appeared that Rajahmundry naticids were yet to attain the required efficiency. This was also reflected in the present low DF and high PE values. In Rajahmundry, PEs on non-naticid prey were low suggesting that predators were highly efficient. This was also evident from high predation mortality (Table 1) and site stereotypy (Fig. 4) (for other instances of low PE, MULT and high site stereotypy in the Cretaceous, see Kelley and Hansen, 1993, 1996b, 2006), but they were yet to be formidable to intraspecific members. 80% of unsuccessful drillholes were located on the dorsal side (abapertural) which indicated that naticids were inexperienced. 4.4. Drilling frequency across the K–T mass extinction event Kelley and Hansen (1996a, 2006) observed the fall of DF immediately below and above the K–T boundary. They, however, observed low DF

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below the K–T in the Corsicana Formation where preservational quality was poor (Kelley, pers. com.). If DF was affected by the K–T mass extinction, the effect should be global. We recorded the highest DF below the K–T boundary and the aftermath of the mass extinction at Rajahmundry was devastating as there was a great diversity loss (95% extinct) and abundance was greatly reduced (N = 164 gastropod specimens in the Intertrappean bed). DF was zero in the Intertrappean assemblage. One possible scenario that could explain this complete absence of drilling traces in the Intertrappean bed was the difference in number of specimens (see Tables 1 and 2) and sampling protocols. In the preextinction latest Maastrichtian Infratrappean bed, bulk sampling (Kowalewski, 2002) protocol was used, whereas random surface sampling protocol was employed to recover specimens in the postextinction Intertrappean bed, due to nature of outcrops (see the Material and method section). Although bulk sampling method was more preferable, our surface sampling protocol was also equally exhaustive and adequate to our primary goal. In some aspects it was actually superior, since it incorporated the spatial variations and also included large specimens, which were often missed in bulk samples (see Kowalewski, 2002). Alternatively, it can be argued that the reduction in specimen number and diversity in the post-extinction Intertrappean assemblage were a biological reality, rather than any sampling artifact. Many workers demonstrated that extinction was a nemesis affair, bringing whole scale wipeout of pre-extinction taxa in the other K–T boundary sections (e.g., see Erwin, 2001).Vermeij (1987) and Kelley and Hansen (2006) suggested that high DF during the aftermath of mass extinction may be due to the absence of escalated prey. It was true that the habitat of the Cretaceous prey i.e., turritelline dominated assemblage (TDA) was completely destroyed by the mass extinction in Rajahmundry. The host sedimentary facies i.e. calcareous sandstone did not reappear in the Intertrappean beds. In the Cretaceous, TDAs occurred in many siliciclastic rocks where nutrient supply and productivity were very high (Allmon and Knight, 1993; Malarkodi et al., 2009). Turritelline gastropods were very susceptible to extinction because of the variation of temperature and nutrients (Allmon, 1992). We found only 2 specimens of a large turritelline species in the Intertrappean bed. But, it was not the escalated prey that always suffered extinction. The surviving group in Rajahmundry (i.e., Cerithiidae) diversified in the recovery phase (new 6 species and 3 genera) and was the dominant fauna. Naticids on the other hand, although crossed the K–T boundary, became drastically reduced in number (415 in Infratrappean to only 1 specimen of a new genus, Euspira found in the Intertrappean bed and one specimen of Natica stoddardi was cited in the literature; see Pascoe, 1964). The near extinction of the escalated predator may explain the total absence of DF in younger assemblage. Another alternative explanation was that infra- and intertrappean beds may not represent the same “adaptive syndrome” (Vermeij, 2002; Kelley and Hansen, 2006) and were not compatible for comparison. The Infratrap evidently represented shallow shelf environment (Pascoe, 1964; Malarkodi et al., 2009, 2010) whereas the Intertrap dominated by the cerithiids and Physa may indicate estuarine and/or swampy environments. But, presence of naticids and turritellines indicated a mixed environment near the coast. Coeval foraminiferal assemblage in the Intertrap, however, indicated normal shallow marine environment (Pascoe, 1964; Keller et al., 2008). Cerithiids were common in both assemblages which allowed comparison of DF of the same adaptive syndrome. DF of cerithiids, which was highest in the Infratrap among families, was zero in the Intertrap. Thus it may appear that the absence of DF may be due to near extinction of the escalated predator after the K–T mass extinction event. Why was naticid DF very high and achieved almost the modern standards in the Indian Cretaceous assemblage? This may be due to the fact that all other previous DF values came from higher latitude localities in the U.S.A. and Western Europe of northern hemisphere than the Rajahmundry area which belonged to the southern subtropic during the Maastrichtian (Smith et al., 1981; Bardhan et al., 2002). Naticid

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predation on modern taxa often showed the latitudinal gradients i.e. increasing DF with decreasing latitude (Vermeij et al., 1980; Paul et al., 2013; but, there were inconsistencies of the relation between DF and latitude, see Kelley and Hansen, 2007a). However, higher value of naticid drilling frequency (34.3%) was reported for another molluscan group (scaphopods) from the Cretaceous assemblage of higher latitude Manitoba in Canada (Li et al., 2011). The present high DF may be simply due to the difference in spatial variation of naticid predation in the contemporary stratigraphic horizons. For example, the assemblage-level DF of bivalves during the Maastrichtian varied from 3 to 19% (Kelley and Hansen, 2006; Harries and Schopf, 2007). When we compared our data for gastropod assemblage-level predation with other results during the Late Cretaceous, DF ranged between 3 and 29% which came within the range of variability during most of the Paleogene (Table 4). The Infratrappean bed was localized and had very limited outcrops. Kelley and Hansen (1993) once stated that “the wide range of drilling frequencies found within one stratigraphic level suggests that predation rates from small or geographically restricted samples must be regarded as minimum values”. Future discovery of Cretaceous assemblages from other countries may clear the anomaly regarding the high DF in the Indian Maastrichtian assemblage. Many workers believed that escalation of naticid drilling predation began since the Paleocene, after the K–T mass extinction event (Allmon et al., 1990). But our present find pushed back the escalation time since the Late Cretaceous. That the predators were escalated was supported by their developments of size and site stereotypy, high DFs and low values of PE and MULT (see also Kelley and Hansen, 1993, 1996a, 2006). Acknowledgments Thanks are due to the local people of Devarapalle and Duddukuru, Andhra Pradesh. We are deeply indebted to Late Dr. Amitava Kayal for his help in logistics and transport. We are also thankful to the staff of ONGC in Rajahmundry. Authors benefited greatly from numerous discussions with Dr. T. K. Gangopadhyay of Bengal Engineering and Science University, Shibpur, India, during and after the field visits. We are also thankful to the Management of the Soma quarry for granting access to the quarry sections. We thank reviewers, Patricia Kelley and another anonymous reviewer for their thorough and insightful comments, which substantially improved the manuscript. The first author (S.M.) acknowledges the grant for field work funded by University Grants Commission. S.B. also acknowledges the partial funds provided by Department of Science and Technology and Centre of Advanced Study, Department of Geological Sciences; University with Potential for Excellence-II and Department of Science and Technology — Promotion of University Research and Scientific Excellence, Jadavpur University. P.G. acknowledges the fund provided by Department of Science and Technology, India. S.S.D. also acknowledges Indian Statistical Institute, Kolkata for providing grant to pursue the research work. References Adegoke, O.S., Tevesz, M.J.S., 1974. Gastropod predation patterns in the Eocene of Nigeria. Lethaia 7, 17–24. Allmon, W.D., 1992. Role of temperature and nutrients in extinction of turritelline gastropods: Cenozoic of the northwestern Atlantic and northeastern Pacific. Palaeogeogr. Palaeoclimatol. Palaeoecol. 92, 41–54. Allmon, W.D., 2007. Cretaceous marine nutrients, greenhouse carbonates, and the abundance of turritelline gastropods. J. Geol. 115 (5), 509–524. Allmon, W.D., Knight, J., 1993. Paleoecological significance of a turritelline gastropoddominated layer in the Cretaceous of South Carolina. J. Paleontol. 67, 355–360. Allmon, W.D., Nieh, J.C., Norris, R.D., 1990. Drilling and peeling of turritelline gastropods since the Late Cretaceous. Palaeontology 33, 595–611. Alvarez, L.W., Alvarez, W., Asaro, F., Michel, H.V., 1980. Extraterrestrial cause for the Cretaceous–Tertiary extinction. Science 208, 1095–1108. Anderson, L.C., Geary, D.H., Nehm, R.H., Allmon, W.D., 1991. A comparative study of naticid gastropod predation on Varicorbula caloosae and Chione cancellata, PlioPliestocene of Florida, U.S.A. Palaeogeogr. Palaeoclimatol. Palaeoecol. 85, 29–46.

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