Published April 30, 2024 | Version v1
Journal article Open

Exploring marine mollusc drilling predation: insights into predator-prey dynamics and selective pressures in gastropod shell assemblages of Playa Guardalavaca, Cuba

Authors/Creators

  • 1. Museum of Nature Hamburg –Zoology, Leibniz Institute for the Analysis of Biodiversity Change
  • 2. Universidad de Oriente, Biology and Geography Department
  • 3. IDACOR, CONICET. Universidad Nacional de Córdoba

Description

Predation marks by drilling molluscs serve as evidence for feeding activity. This behaviour has been extensively studied to understand predator-prey relationships. The objective of this study is to characterise the mollusc drilling predation on gastropods from Playa Guardalavaca, Cuba. We examined the species richness and abundance of drilled and non-drilled shells and calculated predation rates and its relationship with prey size. To compare drilled and non-drilled shells, we used the median and interquartile range due to the asymmetric distribution of the measurements. Furthermore, we employed a Kolmogorov-Smirnov test to compare the size distribution frequencies. A total of 114 morphospecies and nine species groups were identified. Five species were identified as new records for the area. A total of 5,795 shells were quantified, out of which 24.4% displayed drillholes. The most abundant species are not the most preyed upon, presenting a distinct pattern compared to bivalve assemblages in this and other locations. The highest predation rate was observed among individuals of medium size, may be attributed to the predators' ability to manipulate their prey. Smaller shells may not offer sufficient food resources, resulting in lower predation rates. Statistical analyses revealed significant differences in predation related to shell size for six out of the 11 tested species. Potential predators were identified, some of which exhibit drillholes themselves. In general, drilling predation in gastropods from the studied area appears to be influenced by a combination of factors, including high species richness of both predators and prey, prey abundance, specialised feeding strategies of predators, and habitat diversity.

Files

RIM 44 (1) art 1-1.pdf

Files (1.3 MB)

Name Size Download all
md5:1ed68c4bcc8e954c5b71e27fa67abc60
1.3 MB Preview Download

Additional details

References

  • Abbott, R. (1974). American Sea Shells. New York, USA: Van Nostrand Reinhold.
  • Allmon, W.D., Nieh, J.C., Norris, R.D. (1990). Drilling and peeling of turritelline gastropods since the Late Cretaceous. Palaeontology, 33, 595–611.
  • Archuby, F., Gordillo, S. (2018). Drilling predation traces on recent limpets from northern Patagonia, Argentina. Palaeontol. Electron., 21, 1–23.
  • Archuby, F.M., Adami, M., Martinelli, J.C., Gordillo, S., Boretto, G.M., Malve, M.E. (2015). Regional-scale compositional and size fidelity of rocky intertidal communities from the Patagonian Atlantic coast. Palaios, 30(8), 627–643.
  • Bardhan, S., Saha, S., Das, S.S., Saha, R. (2021). Paleoecology of naticid–molluscan prey interaction during the Late Jurassic (Oxfordian) in Kutch, India: evolutionary implications. J. Paleontol., 95(5), 974–993.
  • Blustein, D.H., Anderson, R.C. (2016). Localization of octopus drill holes on cowries. Am. Malacol. Bull., 34(1), 61–64.
  • Carriker, M. (1981). Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis. Malacologia, 20(2), 403–422.
  • Chattopadhyay, D., Dutta, S. (2013). Prey selection by drilling predators: a case study from Miocene of Kutch, India. Palaeogeogr., Palaeoclimatol., Palaeoecol., 374, 187–196.
  • Chattopadhyay, D., Kella, V.G.S., Chattopadhyay, D. (2020). Effectiveness of small size against drilling predation: Insights from lower Miocene faunal assemblage of Quilon Limestone, India. Palaeogeogr., Palaeoclimatol., Palaeoecol., 551, 109742.
  • Chiu, J.M., Shin, P.K., Wong, K.P., Cheung, S.G. (2010). Sibling cannibalism in juveniles of the marine gastropod Nassarius festivus (Powys, 1835). Malacologia, 52(1), 157–161.
  • Delance, J.H., Emig, C.C. (2004). Drilling predation on Gryphus vitreus (Brachiopoda) off the French Mediterranean coasts. Palaeogeogr., Palaeoclimatol., Palaeoecol., 208(1–2), 23–30.
  • Denis, D., Ramirez-Arrieta, V.M. (2020). Si una imagen vale más que mil palabras: ¿cuanto puede decir un gráfico de cajas? Rev. Jard. Bot. Nac., 41, 57–69.
  • Diez, Y.L., Jover, A. (2012). Moluscos marinos del sector Bahía de Puerto Padre-Bahía de Nipe, Cuba. Amici Molluscarum, 20(1), 17–28.
  • Diez, Y.L., García-Mora, O., Batista-Zaldívar, C.D. (2022). New records of marine molluscs for the northeastern coast of Cuba. Rev. Invest. Mar., 42(2), 47–53.
  • Diez, Y.L., García-Mora, O., Catalá, A., Gordillo, S. (2023). Drilling predation on bivalve shell assemblages at Playa Guardalavaca, Cuba. Rev. Invest. Mar., 43(1), 55–68.
  • Espinosa, J., Ortea J. (2002). Descripción de cuatro nuevas especies de la familia Rissoinidae (Mollusca: Gastropoda). Avicennia, 15, 141–146.
  • Espinosa, J., Ortea, J., Sánchez, R., Gutiérrez, J. (2012). Moluscos marinos de la Reserva de la Biósfera de la Península de Guanahacabibes. La Habana, Cuba: Instituto de Oceanología.
  • Fox, J. (2005). The R Commander: A Basic Statistics Graphical User Interface to R. J. Stat. Softw., 14(9), 1–42.
  • Fox, J. (2017). Using the R Commander: A Point-and-Click Interface or R. Florida, USA: Chapman and Hall/CRC Press.
  • Fox, J., Bouchet-Valat, M. (2022). Rcmdr: R Commander. R package version 2.8-0.
  • Fürsich, F.T., Jablonski, D. (1984). Late Triassic naticid drillholes: carnivorous gastropods gain a major adaptation but fail to radiate. Science, 224, 78–80.
  • Gordillo, S., Diez, Y.L., Espinosa, J. (2019). Marcas de depredación por perforación en bivalvos y gasterópodos de la costa norte de Cuba. Rev. Invest. Mar., 39(1), 66–75.
  • Gordillo, S., Malvé, M.E. (2021). Drilling predation on Antarctic tusk shells: first records on Recent scaphopods from the Southern Hemisphere. Antarct. Sci., 33(4), 344–348.
  • Gordillo, S., Malvé, M.E., Morán, G.A., Boretto, G.M. (2020). Naticid drilling predation from tidal flats in northern Patagonia, SW Atlantic. J. Mar. Biol. Assoc. UK, 100(6), 909–919.
  • Gordillo, S., Morán, G.A., Malvé, M.E. (2022). Octopuses and drilling snails as the main suspects of predation traces on shelled molluscs in West Antarctica. Polar Biol., 45(1), 127–141.
  • Greenwell, C.N., Loneragan, N.R., Admiraal, R., Tweedley, J.R., Wall, M. (2019). Octopus as predators of abalone on a sea ranch. Fish. Manag. Ecol., 26(2), 108–118.
  • Grun, T.B., Kroh, A., Nebelsick, J.H., Zamora, S., Rahman, I.A. (2017). Comparative drilling predation on time-averaged phosphatized and nonphosphatized assemblages of the minute clypeasteroid echinoid Echinocyamus stellatus from Miocene offshore sediments (Globigerina Limestone Formation, Malta). J. Paleontol., 91(4), 633–642.
  • Harper, E.M. (2003). Assessing the importance of drilling predation over the Palaeozoic and Mesozoic. Palaeogeogr., Palaeoclimatol., Palaeoecol., 201(3–4), 185–198.
  • Huelsken, T. (2011). First evidence of drilling predation by Conuber sordidus (Swainson, 1821) (Gastropoda: Naticidae) on soldier crabs (Crustacea: Mictyridae). Moll. Res., 31(2), 125–132.
  • Hughes, R.N., Hughes, H.P.I. (1981). Morphological and behavioral aspects of feeding in the cassidae (Tonnacea, Mesogastropoda). Malacology, 20, 385–402.
  • Huntley, J.W., Kowalewski, M. (2007). Strong coupling of predation intensity and diversity in the Phanerozoic fossil record. Proc. Natl. Acad. Sci. USA, 104, 15006–15010.
  • Kabat, A.R. (1990). Predatory ecology of naticid gastropods with a review of shell boring predation. Malacologia, 32(1), 155–193.
  • Kelley, P.H., Hansen, T.A. (1993). Evolution of the naticid gastropod predator-prey system: an evaluation of the hypothesis of escalation. Palaios, 8(4), 358–375.
  • Kelley, P.H., Hansen, T.A. (2006). Comparisons of class and lower taxon level patterns in naticid gastropod predation, Cretaceous to Pleistocene of the US Coastal Plain. Palaeogeogr., Palaeoclimatol., Palaeoecol., 236, 302–320.
  • Kidwell, S.M. (2001). Preservation of species abundance in marine death assemblages. Science, 294(5544), 1091–1094.
  • Kidwell, S.M. (2002). Time-averaged molluscan death assemblages: palimpsests of richness, snapshots of abundance. Geology, 30(9), 803–806.
  • Kidwell, S. M. (2013). Time‐averaging and fidelity of modern death assemblages: building a taphonomic foundation for conservation palaeobiology. Palaeontology, 56(3), 487–522.
  • Klompmaker, A.A., Kowalewski, M., Huntley, J.W., Finnegan, S. (2017). Increase in predator-prey size ratios throughout the Phanerozoic history of marine ecosystems. Science, 356, 1178–1180.
  • Kong, D.-Y., Lee, M.-H., Park, C.H., Lee, S.J. (2017). Boreholes on three bivalve species found on the sand beach at Sagot. J. Asia-Pac. Biodivers., 10, 441–447.
  • Kowalewski, M. (2002). The fossil record of predation: An overview of analytical methods. Paleont. Soc. Pap., 8, 3–42.
  • Kowalewski, M., Dulai, A., Fürsich, F.T. (1998) A fossil record full of holes: the Phaneorozoic history of drilling predation. Geology, 26, 1091–1094.
  • Ludwig, J., Reynolds, J. (1988). Statistical Ecology. New York, USA: John Wiley and Sons. Mondal, S., Chakraborty, H., Paul, S. (2019). Latitudinal patterns of gastropod drilling predation intensity through time. Palaios, 34, 261–270.
  • Mondal, S., Chakraborty, H., Saha, S., Dey, S., Sarkar, D. (2021a). High biogeographic and latitudinal variability in gastropod drilling predation on molluscs along the eastern Indian coast: Implications on the history of fossil record of drillholes. PLoS ONE, 16(8), e0256685.
  • Mondal, S., Maitra, A., Bose, K., Goswami, P., Bardhan, S., Mallick, S. (2021b). Substrate-controlled naticid gastropod drilling predation on recent barnacles from Chandipur, India and its Palaeontological implications. Hist. Biol., 33(7), 1029–1042.
  • Morton, B. (2006). Diet and predation behaviour exhibited by Cominella eburnea (Gastropoda: Caenogastropoda: Neogastropoda) in Princess Royal Harbour, Albany, Western Australia, with a review of attack strategies in the Buccinidae. Moll. Res., 26(1), 39–50.
  • Morton, B., Chan, K. (1997). First report of shell boring predation by a member of the Nassariidae (Gastropoda). J. Moll. Stud., 63(3), 476–478.
  • Morton, B., Harper, E.M. (2009). Drilling predation upon Ditrupa arietina (Polychaeta: Serpulidae) from the Mid-Atlantic Açores, Portugal. Açoreana, suppl. 6, 157–165.
  • Morton, B., Peharda, M., Harper, E. M. (2007). Drilling and chipping patterns of bivalve prey predation by Hexaplex trunculus (Mollusca: Gastropoda: Muricidae). J. Mar. Biol. Assoc. UK, 87(4), 933–940.
  • Munoz-Marquez, M. (2022). RcmdrPlugin.UCA: UCA Rcmdr Plug-in_. R package version 5.1-1, https://CRAN.R-project.org/package=RcmdrPlugin.UCA.
  • Pahari, A., Mondal, S., Bardhan, S., Sarkar, D., Saha, S., Buragohain, D. (2016). Subaerial naticid gastropod drilling predation by Natica tigrina on the intertidal molluscan community of Chandipur, Eastern Coast of India. Palaeogeogr., Palaeoclimatol., Palaeoecol., 451, 110–123.
  • Peterson, C.H., Black, R. (1994). Drilling by buccinid gastropods of the genus Cominella in Australia. Veliger, 38, 37–42.
  • Ponder, W.F., Taylor, J.D. (1992). Predatory shell drilling by two species of Austroginella (Gastropoda: Marginellidae). J. Zool., 228(2), 317–328.
  • Pruss, S., Stevenson, M., Duffey, S. (2011). Drilling predation and taphonomy in modern mollusk death assemblages, San Salvador Island, Bahamas. Palaeogeogr., Palaeoclimatol., Palaeoecol., 311, 74–81.
  • Ramirez-Arrieta, V.M. (2020). Extended Boxplot Graphics. https://vmra.shinyapps.io/univariados/. Revised February 14, 2023.
  • Rolán, E., Fernández-Garcés, R. (2010). The shouldered species of the Rissoininae (Mollusca: Rissooidea) in the Caribbean with the description of three new species. Novapex, 11(4), 83–91.
  • Sarkar, D., Bardhan, S., Mondal, S., Das, A., Pahari, A., Buragohain, D., Saha, S. (2016) Predation on Recent terebrid gastropods from the Indian subcontinent and a spatiotemporal reappraisal based on a revised global database. Malacologia, 59, 271–303.
  • Sawyer, J.A., Zuschin, M. (2010). Intensities of drilling predation of molluscan assemblages along a transect through the northern Gulf of Trieste (Adriatic Sea). Palaeogeogr., Palaeoclimatol., Palaeoecol., 285(3–4), 152–173.
  • Taylor, J.D. (1998). Understanding biodiversity: adaptive radiations of predatory marine gastropods. In The marine biology of the South China Sea (pp. 187–206). Hong Kong: Hong Kong University Press.
  • Thomas, M., Day, R. W. (1995). Site selection by a small drilling predator: Why does the gastropod Haustrum baileyanum drill over muscle tissue of the abalone Haliotis rubra? Mar. Freshw. Res., 46(3), 647–655.
  • Tomašových, A., Kidwell, S.M. (2009). Fidelity of variation in species composition and diversity partitioning by death assemblages: time-averaging transfers diversity from beta to alpha levels. Paleobiology, 35(1), 94–118.
  • Villegas-Martín, J., Rojas-Consuegra, R., Klompmaker, A.A. (2016). Drill hole predation on tubes of serpulid polychaetes from the Upper Cretaceous of Cuba. Palaeogeogr., Palaeoclimatol., Palaeoecol., 455, 44–52.
  • Warmke, G., Abbott, R. (1962). Caribbean Seashells. Pennsylvania, USA: Livingston Publishing Company.
  • WoRMS (2023). Mollusca. https://www.marinespecies.org/aphia.php?p=taxdetails&id=51. Revised March 10, 2023.
  • Zuschin, M., Nawrot, R., Dengg, M., Gallmetzer, I., Haselmair, A., Wurzer, S., Tomašových, A. (2022). Scale dependence of drilling predation in the Holocene of the northern Adriatic Sea across benthic habitats and nutrient regimes. Paleobiology, 48(3), 462–479.