Predation on Recent Terebrid Gastropods from the Indian Subcontinent and a Spatiotemporal Reappraisal Based on a Revised Global Database

ABSTRACT Predator-prey interaction, especially drilling and shell-breaking predation pressure, caused significant evolutionary changes within these predator-prey communities. Although temporal trends are well understood in prey assemblages, studies to trace such changes within taxonspecific clades up to Recent times have been rare. Here, we studied both the drilling and shell-breaking predation on Recent terebrid gastropods from the Indian subcontinent and compared the results with a newly updated, global database. The major part of our data came from a large collection reposited in the archive of the Zoological Survey of India in Kolkata for more than 100 years. Detailed analyses of this study based on a newly raised, global database revealed the following findings: (1) Drilling frequency (DF) of Indian terebrids was low, but consistent with the DF of only available but limited data provided by Vermeij et al. (1980). In comparison, peeling frequency (PF) in Indian terebrids appeared to be highest in the world; (2) DF showed latitudinal variation, that is, higher incidence of drilling occurred in higher latitudes; no such pattern emerged from the PF data; (3) drillholes were site-stereotyped, which suggested that Recent naticid drillers were escalated; (4) shell ornaments failed to protect against durophagy; (5) shell shape and thickness had different impact against different modes of predation. While slender and thicker shells were almost immune to drilling predation, no such relation existed for peeling predation; (6) on the other hand, body size appears to have evolved as anti-predatory traits in Recent terebrids. Larger species had low DF and high PF values; (7) temporally, DF showed fluctuating pattern, with modern values showing declining trend. This was perhaps due to increase in body size and behavioural change of the terebrid gastropods. Unfortunately, no peeling frequency data for this clade was available from the fossil record.

[1]  P. Harries,et al.  Temporal patterns in successful and unsuccessful shell-breaking predatory attack strategies on Varicorbula in the Plio-Pleistocene of Florida , 2015 .

[2]  Arindam Roy,et al.  Repair scars on Mactra violacea from the eastern coast of India: A new classification and a model for describing shell breakage on bivalves , 2014 .

[3]  Christy C. Visaggi,et al.  Validation of taxon-specific sampling by novice collectors for studying drilling predation in fossil bivalves , 2014 .

[4]  S. Mallick,et al.  Naticid drilling predation on gastropod assemblages across the K–T boundary in Rajahmundry, India: New evidence for escalation hypothesis , 2014 .

[5]  Anirban Das,et al.  A note on exceptionally high confamilial naticid drilling frequency on Natica gualteriana from the Indian subcontinent , 2014 .

[6]  S. Dutta,et al.  What controls cannibalism in drilling gastropods? A case study on Natica tigrina , 2014 .

[7]  M. V. Modica,et al.  A Good Compromise: Rapid and Robust Species Proxies for Inventorying Biodiversity Hotspots Using the Terebridae (Gastropoda: Conoidea) , 2014, PloS one.

[8]  J. Hutchings,et al.  A note on edge drilling predation by naticid gastropods , 2014 .

[9]  P. Harries,et al.  Paleoecological significance of coupling metrics of successful and unsuccessful shell-breaking predation: Examples using Neogene bivalve prey , 2014 .

[10]  Y. Kantor,et al.  Trophic diversification in the evolution of predatory marine gastropods of the family Terebridae as inferred from stable isotope data , 2014 .

[11]  Anirban Das,et al.  Predation on Recent Turritelline Gastropods from the Indian Subcontinent and Comparison with a Revised Global Database , 2013 .

[12]  C. Cruaud,et al.  Macroevolution of venom apparatus innovations in auger snails (Gastropoda; Conoidea; Terebridae). , 2012, Molecular phylogenetics and evolution.

[13]  G. Dietl,et al.  A comparison of analyses of drilling predation on fossil bivalves: Bulk- vs. taxon-specific sampling and the role of collector experience , 2012 .

[14]  E. Harper,et al.  Treatise Online no. 44: Part N, Revised, Volume 1, Chapter 22: Predation of bivalves , 2012 .

[15]  A. Strasser,et al.  A comparison of recent and fossil large, high-spired gastropods and their environments: the Nopparat Thara tidal flat in Krabi, South Thailand, versus the Swiss Kimmeridgian carbonate platform , 2011 .

[16]  N. Puillandre,et al.  The Terebridae and teretoxins: Combining phylogeny and anatomy for concerted discovery of bioactive compounds , 2010, BMC chemical biology.

[17]  D. Mukherjee,et al.  Sympatric Character Convergence between Two Species of Closely Related Genera of Pholadinae (Bivalvia: Pholadidae) from the Eastern Coast of India , 2009 .

[18]  M. Kowalewski,et al.  Strong coupling of predation intensity and diversity in the Phanerozoic fossil record , 2007, Proceedings of the National Academy of Sciences.

[19]  H. Fortunato.  Naticid gastropod predation in the Gatun Formation (late Middle Miocene), Panama: preliminary assessment , 2007 .

[20]  T. Hansen,et al.  Comparisons of class- and lower taxon-level patterns in naticid gastropod predation, Cretaceous to Pleistocene of the U.S. Coastal Plain , 2006 .

[21]  W. Allmon.  The importance of museum collections in paleobiology , 2005, Paleobiology.

[22]  G. Vermeij,et al.  Reduced Competition and Altered Feeding Behavior Among Marine Snails After a Mass Extinction , 2004, Science.

[23]  A. Collins,et al.  Anthropogenic impacts and historical decline in body size of rocky intertidal gastropods in southern California , 2003 .

[24]  M. Kowalewski,et al.  The fossil record of predation: an overview of analytical methods , 2002 .

[25]  M. Zuschin,et al.  Experimental Measurement of Shell Strength and its Taphonomic Interpretation , 2001 .

[26]  T. Baumiller,et al.  Taphonomic Inferences on Boring Habit in the Richmondian Onniella meeki Epibole , 2000 .

[27]  George E. Boyajian,et al.  Subtle changes in mature predator-prey systems; an example from Neogene Turritella (Gastropoda) , 1997 .

[28]  M. Labarbera,et al.  Taphonomic bias in analyses of drilling predation: effects of gastropod drill holes on bivalve shell strength , 1994 .

[29]  K. Böhning‐Gaese,et al.  Patterns of drilling predation on gastropods of the family Turritellidae in the Gulf of California , 1993, Paleobiology.

[30]  T. Hansen,et al.  Evolution of the naticid gastropod predator-prey system: an evaluation of the hypothesis of escalation , 1993 .

[31]  R. Nehm,et al.  A comparative study of naticid gastropod predation on Varicorbula caloosae and Chione cancellata, Plio-Pleistocene of Florida, U.S.A. , 1991 .

[32]  B. Morton,et al.  Alternative predation tactics of a tropical naticid gastropod , 1987 .

[33]  A. Kohn,et al.  Predation on early Pleistocene naticid gastropods in Fiji , 1986 .

[34]  G. Vermeij,et al.  Shell repair and drilling in some gastropods from the Ripley Formation (Upper Cretaceous) of the south-eastern U.S.A. , 1982 .

[35]  James F. Kitchell,et al.  Prey Selection by naticid gastropods: experimental tests and application to the fossil record , 1981, Paleobiology.

[36]  R. G. Bromley.  Conceptos en ichnotaxonomía ilustrados por perforaciones pequeñas y redondas sobre conchas = Concepts in ichnotaxonomy illustrated by small round holes in shells , 1981 .

[37]  G. Vermeij,et al.  Predation in time and space: peeling and drilling in terebrid gastropods , 1980, Paleobiology.

[38]  G. Vermeij,et al.  Predation in time and space: drilling in the gastropod Turritella , 1978, Paleobiology.

[39]  G. Vermeij,et al.  Crushing behavior of tropical and temperate crabs , 1978 .

[40]  B. A. Miller.  The Biology of Terebra gouldi Deshayes, 1859, and a Discussion of Life History Similarities among Other Terebrids of Similar Proboscis Type , 1975 .

[41]  H. B. Preston.  Descriptions of New Species of Land, Marine and Freshwater Shells from the Andaman Islands , 1908, Records of the Zoological Survey of India.

[42]  E. A. Smith.  XXIV.—Natural history notes from H.M. Indian Marine Survey Steamer ‘Investigator,’ Commander T. H. Heming, R.N.—Series III., No. 1. On Mollusca from the Bay of Bengal and the Arabian Sea , 1904 .

[43]  E. R. Sykes,et al.  NOTES ON A COLLECTION OF MARINE SHELLS FROM THE ANDAMAN ISLANDS, WITH DESCRIPTIONS OF NEW SPECIES , 1897 .

[44]  J. Martinell,et al.  CONFAMILIAL PREDATION IN PLIOCENE NATICID GASTROPODS FROM SOUTHERN FRANCE: UTILITY OF PREEXISTING COLLECTIONS IN QUANTITATIVE PALEOECOLOGY , 2010 .

[45]  T. Hansen,et al.  Latitudinal Patterns in Naticid Gastropod Predation Along the East Coast of the United States A Modern Baseline for Interpreting Temporal Patterns in the Fossil Record , 2007 .

[46]  T. Hansen,et al.  The Fossil Record of Drilling Predation on Bivalves and Gastropods , 2003 .

[47]  J. Nieh,et al.  Drilling and peeling of turritelline gastropods since the Late Cretaceous , 1990 .

[48]  P. W. Signor.  The role of shell geometry as a deterrent to predation in terebrid gastropods , 1985 .

[49]  John D. Taylor,et al.  Food specialization and the evolution of predatory prosobranch gastropods , 1980 .

[50]  P. Nelson.  PALEONTOLOGY: COMMUNITY STRUCTURE IN THE STONE CITY FORMATION (MIDDLE EOCENE, TEXAS) , 1980 .

[51]  A. Hoffman,et al.  Predation by muricid and naticid gastropods on the Lower Tortonian moIlusks from the Korytnica clays , 1974 .

[52]  W. T. Pecora,et al.  Recent gastropod boreholes and Ordovician cylindrical borings , 1968 .