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Predatory drilling on molluscan assemblages along the Patagonian shelf (southern Argentina)

Published online by Cambridge University Press:  22 March 2024

Sandra Gordillo*
Affiliation:
Facultad de Filosofía y Humanidades, Universidad Nacional de Córdoba, Museo de Antropologías, Córdoba, Argentina Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Instituto de Antropología de Córdoba (IDACOR), Avda. Hipólito Yrigoyen 174, X5000JHO, Córdoba, Argentina
M. Sol Bayer
Affiliation:
Facultad de Ciencias Exactas y Naturales, Instituto de Geología de Costas y del Cuaternario (CIC-UNMdP), Universidad Nacional de Mar del Plata, Deán Funes 3350, 1° Nivel, B7602AYL, Mar del Plata, Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Godoy Cruz 2290, C1425FQB, Caba, Argentina
*
Corresponding author: Sandra Gordillo; Email: gordillosan@yahoo.es

Abstract

Both present-day and fossil molluscan assemblages offer an opportunity for a better understanding of the structure and organization of both modern and past benthic communities. In this framework, drill holes are used widely to explore predator–prey interactions. This research focuses on predation marks, especially drill holes, recorded on modern molluscan assemblages in a Patagonian sector of the Argentinean continental shelf. Shelled molluscs (n = 2179) were recovered from 27 to 135 m depths covering a long latitudinal extent (between 39° and 54°S). For each station, taxonomic position, ecological composition and relative abundance of taxa were determined, and then drilling frequency (DF) was calculated to infer drilling intensity. The collected molluscs belong to 37 families, with Veneridae being the most abundant in terms of the number of specimens (n = 419). Specimens with drill holes (n = 226) belong to 21 families (with at least 33 different species). Most of them are suspension feeders (85.8%) and the remaining percentage comprised other trophic types. Naticids and muricids, as main potential predators, together account for 19.6% of the gastropods present in the molluscan assemblages. DF across all the stations was moderate (9.9%) but varied between low (0–2.4%) and high (28.9%). These results do not show a trend linked to latitude or depth, and the great variability of DF between stations suggests that other local ecological or environmental conditions would influence drilling predation at a small spatio-scale.

Type
Research Article
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Acha, EM, Mianzan, HW, Guerrero, RA, Favero, M and Bava, J (2004) Marine fronts at the continental shelves of austral South America. Journal of Marine Systems 44, 83105.CrossRefGoogle Scholar
Alexander, RR and Dietl, GP (2001) Shell repair frequencies in New Jersey bivalves: a recent baseline for tests of escalation with Tertiary, Mid-Atlantic congeners. Palaios 16, 354371.2.0.CO;2>CrossRefGoogle Scholar
Archuby, F and Gordillo, S (2018) Drilling predation traces on recent limpets from northern Patagonia, Argentina. Palaeontologia Electronica 21, 123.CrossRefGoogle Scholar
Arnold, JM and Arnold, KO (1969) Some aspects of hole- boring predation by Octopus vulgaris. American Zoologist 9, 991996.CrossRefGoogle Scholar
Ashton, GV, Freestone, AL, Duffy, JE, Torchin, ME, Sewall, BJ, Tracy, B, Albano, M, Altieri, AH, Altvater, L, Bastida-Zavala, R, Bortolus, A, Brante, A, Bravo, V, Brown, N, Buschmann, AH, Buskey, E, Barrera, RC, Cheng, B, Collin, R, Coutinho, R, De Gracia, L, Dias, GM, DiBacco, C, Flores, AAV, Haddad, MA, Hoffman, Z, Erquiaga, BI, Janiak, D, Campeán, AJ, Keith, I, Leclerc, J-C, Lecompte-Pérez, OP, Longo, GO, Matthews-Cascon, H, McKenzie, CH, Miller, J, Munizaga, M, Naval-Xavier, LPD, Navarrete, SA, Otálora, C, Palomino-Alvarez, LA, Palomo, MG, Patrick, C, Pegau, C, Pereda, SV, Rocha, RM, Rumbold, C, Sánchez, C, Sanjuan-Muñoz, A, Schlöder, C, Schwindt, E, Seemann, J, Shanks, A, Simoes, N, Skinner, L, Suárez-Mozo, NY, Thiel, M, Valdivia, N, Velez-Zuazo, X, Vieira, EA, Vildoso, B, Wehrtmann, IS, Whalen, M, Wilbur, L and Ruiz, GM (2022) Predator control of marine communities increases with temperature across 115 degrees of latitude. Science 376, 12151219.CrossRefGoogle ScholarPubMed
Bayer, S, Gordillo, S and Morsan, E (2016) Late Quaternary faunal changes in northeastern Patagonia (Argentina) according to a dynamic mosaic of benthic habitats: taphonomic and paleoecological analyses of mollusk assemblages. Ameghiniana 53, 655674.CrossRefGoogle Scholar
Borel, M and Franco Arias, DA (2012) Variaciones climáticas y eustáticas holocenas. Relación potencial con el cambio climático global, In: Informe Campaña ‘Patagonia Austral’ marzo-abril 2012, 24–27. Unpublished report.Google Scholar
Bromley, RG (1993) Predation habits of octopus past and present and a new ichnospecies, Oichnus ovalis. Bulletin of the Geological Society of Denmark 40, 167173.CrossRefGoogle Scholar
Carriker, MR (1981) Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis. Malacologia 20, 403422.Google Scholar
Carriker, MR and Gruber, GL (1999) Uniqueness of the gastropod accessory boring organ (ABO): comparative biology, an update. Journal of Shellfish Research 18, 579595.Google Scholar
Chattopadhyay, D and Baumiller, TK (2007) Drilling under threat: an experimental assessment of the drilling behavior of Nucella lamellosa in the presence of a predator. Journal of Experimental Marine Biology and Ecology 352, 257266.CrossRefGoogle Scholar
Cooke, R, Whitelaw, B, Norman, M, Caruana, N and Strugnell, JM (2017) Toxicity in cephalopods. In Gopalakrishnakone, P and Malhotra, A (eds), Evolution of Venomous Animals and Their Toxins. Dordrecht: Springer, pp. 125143.CrossRefGoogle Scholar
Dogliotti, AI, Lutz, VA and Segura, V (2014) Estimation of primary production in the southern Argentine continental shelf and shelf-break regions using field and remote sensing data. Remote Sensing of Environment 140, 497508.CrossRefGoogle Scholar
Duquette, A, McClintock, JB, Amsler, CD, Pérez-Huerta, A, Milazzo, M and Hall-Spencer, JM (2017) Effects of ocean acidification on the shells of four Mediterranean gastropod species near a CO2 seep. Marine Pollution Bulletin 124, 917928.CrossRefGoogle Scholar
Fainburg, L, Trassens, M, Bastida, J, Farenga, M, Isla, F and Bastida, R (2012) Nearshore benthic communities and bioengineers from the macrotidal San Jorge Gulf: Patagonia, Argentina. Thalassas 28, 4556.Google Scholar
Fee, GN, Mather, J, Landschoff, J and Griffiths, CL (2023) Finding the sweet spot: drilling precision on shelled molluscs by Octopus vulgaris type III in False Bay, South Africa. Marine Biology 170, 22.CrossRefGoogle Scholar
Fortunato, H (2015) Mollusks: tools in environmental and climate research. American Malacological Bulletin 33, 115.Google Scholar
Franco, BC, Ruiz-Etcheverry, LA Marrari, M, Piola, AR and Matano, RP (2022) Climate change impacts on the Patagonian shelf break front. Geophysical Research Letters 49, e2021GL096513.CrossRefGoogle Scholar
Frey, RW, Howard, JD and Hong, JS (1986) Naticid gastropods may kill solenoid bivalves without boring: ichnologic and taphonomic consequences. Palaios 1, 610612.CrossRefGoogle Scholar
Fujita, S (1916) On the boring of the pearl oyster by Octopus (Polypus) vulgaris Lamarck. Dobutsugaku Zasshi 28, 250257.Google Scholar
Gordillo, S (1998) Trophonid gastropod predation on recent bivalves from the Magellanic region. In Johnston, PA and Haggart, JW (eds), Bivalves: An Eon of Evolution. Calgary: University of Calgary Press, pp. 251254.Google Scholar
Gordillo, S (2001) Marcas de la depredación de Acanthina Fischer von Waldheim, 1807 (Gasteropoda: Muricidae) sobre Bivalvia. Ameghiniana 38, 5560.Google Scholar
Gordillo, S (2013) Cannibalism in Holocene muricid snails in the Beagle Channel, at the extreme southern tip of South America: an opportunistic response? Palaeontologia Electronica 16, 113.Google Scholar
Gordillo, S and Amuchástegui, S (1998) Estrategias de depredación del gastrópodo perforador Trophon geversianus (Pallas) (Muricoidea: Trophonidae). Malacologia 39, 8391.Google Scholar
Gordillo, S and Archuby, FM (2012) Predation by drilling gastropods and asteroids upon mussels in rocky shallow shores of southernmost South America: paleontological implications. Acta Palaeontologica Polonica 57, 633643.CrossRefGoogle Scholar
Gordillo, S and Archuby, FM (2014) Live-live and live-dead interactions in marine death assemblages: the case of the Patagonian clam Venus antiqua. Acta Palaeontologica Polonica 59, 429442.Google Scholar
Gordillo, S, Bayer, MS and Martinelli, J (2010) Moluscos recientes del Canal Beagle, Tierra del Fuego: un análisis cualitativo y cuantitativo de los ensambles de valvas fósiles y actuales. Anales del Instituto de la Patagonia 38, 95106.CrossRefGoogle Scholar
Gordillo, S, Bernasconi, E, Cusminsky, G, Coronato, AJ and Rabassa, JO (2013) Late Quaternary environmental changes in southernmost South America reflected in marine calcareous macro- and microfossils. Quaternary International 305, 149162.CrossRefGoogle Scholar
Gordillo, S, Malvé, M, Morán, G and Boretto, G (2020) Naticid drilling predation from tidal flats in northern Patagonia, SW Atlantic. Journal of the Marine Biological Association of the UK 100, 909919.CrossRefGoogle Scholar
Gordillo, S, Martinelli, J, Cárdenas, J and Bayer, S (2011) Testing ecological and environmental changes during the last 6000 years: a multiproxy approach based on the bivalve Tawera gayi from southern South America. Journal of the Marine Biological Association of the United Kingdom 91, 14131427.CrossRefGoogle Scholar
Gordillo, S, Morán, G and Malvé, M (2021) Octopuses and drilling snails as the main suspects of predation traces on shelled molluscs in West Antarctica. Polar Biology 45, 127141.CrossRefGoogle Scholar
Gordillo, S, Muñoz, D, Bayer, S and Malvé, M (2018) How physical and biotic factors affect brachiopods from the Patagonian Continental Shelf. Journal of Marine Systems 187, 223234.CrossRefGoogle Scholar
Hansen, TA and Kelley, PH (1995) Spatial variation of naticid gastropod predation in the Eocene of North America. Palaios 10, 268278.CrossRefGoogle Scholar
Harper, EM (2016) Uncovering the holes and cracks: from anecdote to testable hypotheses in predation studies. Palaeontology 59, 597609.CrossRefGoogle Scholar
Harper, EM, Peck, LS and Hendry, KR (2009) Patterns of shell repair in articulate brachiopods indicate size constitutes a refuge from predation. Marine Biology 156, 19932000.CrossRefGoogle Scholar
Hartwick, EB, Thorarinsson, G and Tulloch, L (1978) Methods of attack by Octopus dofleini (Wulker) on captured bivalve and gastropod prey. Marine Behavior and Physiology 5, 193200.CrossRefGoogle Scholar
Hoffmeister, AP and Kowalewski, M (2001) Spatial and environmental variation in the fossil record of drilling predation: a case study from the Miocene of central Europe. Palaios 16, 566579.2.0.CO;2>CrossRefGoogle Scholar
Iribarne, OO, Fernandez, M, Diaz, M and Clemente, M (1993) Prey attack by the Patagonian octopus Octopus tehuelchus d'Orbigny: an odd pattern. The Veliger 32, 199202.Google Scholar
Kabat, AR (1990) Predatory ecology of naticid gastropods with a review of shell boring predation. Malacologia 32, 155193.Google Scholar
Kelley, PH (1988) Predation by Miocene gastropods of the Chesapeake group: stereotyped and predictable. Palaios 3, 436448.CrossRefGoogle Scholar
Kelley, PH (1991) The effect of predation intensity on rate of evolution of five Miocene bivalves. Historical Biology 5, 6588.CrossRefGoogle Scholar
Kelley, PH and Hansen, TA (2003) The fossil record of drilling predation on bivalves and gastropods. In Kelley, PH, Kowalewski, M and Hansen, TA (eds), Predator–Prey Interactions in the Fossil Record, Topics in Geobiology Series 20. New York: Kluwer Academic/Plenum Publishers, pp. 113139.Google Scholar
Kelley, PH and Hansen, TA (2007) Latitudinal patterns in naticids gastropod predation along the east coast of the United States: a modern baseline for interpreting temporal patterns in the fossil record. In Bromley, RG, Buatois, LA, Mángano, MG, Genise, JF and Melchor, RN (eds), Sediment-Organism Interactions: A Multifaceted Ichnology, vol. 88. Tulsa, OK: SEPM Special Publications, pp. 284299.Google Scholar
Kidwell, SM (2001) Preservation of species abundance in marine death assemblages. Science 294, 10911094.CrossRefGoogle ScholarPubMed
Kidwell, SM (2002) Time-averaged molluscan death assemblages: palimpsests of richness, snapshots of abundance. Geology 30, 803806.2.0.CO;2>CrossRefGoogle Scholar
Kidwell, SM (2013) Time-averaging and fidelity of modern death assemblages: building a taphonomic foundation for conservation palaeobiology. Palaeontology 56, 487522.CrossRefGoogle Scholar
Kondo, Y (1987) Burrowing depth of infaunal bivalve – observation of living species and its relation to shell morphology. Transactions and Proceedings of the Palaeontological Society of Japan, N.S. 148, 306323.Google Scholar
Kowalewski, M (2002) The fossil record of predation: an overview of analytical methods. Paleontological Society Special Paper 8, 342.CrossRefGoogle Scholar
Kowalewski, M (2004) Drill holes produced by the predatory gastropod Nucella lamellosa (Muricidae): paleobiological and ecological implications. Journal of Molluscan Studies 70, 359370.CrossRefGoogle Scholar
Kowalewski, M, Dulai, A and Fursich, FT (1998) A fossil record full of holes: the Phanerozoic history of drilling predation. Geology 26, 10911094.2.3.CO;2>CrossRefGoogle Scholar
Kroeker, KJ, Sanford, E, Jellison, BM and Gaylord, B (2014) Predicting the effects of ocean acidification on predator-prey interactions: a conceptual framework based on coastal molluscs. Biological Bulletin 226, 211222.CrossRefGoogle ScholarPubMed
Lord, JP, Harper, EM and Barry, JP (2019) Ocean acidification may alter predator–prey relationships and weaken nonlethal interactions between gastropods and crabs. Marine Ecology Progress Series 616, 8394.CrossRefGoogle Scholar
Martinelli, JC, Gordillo, S and Archuby, F (2013) Muricid drilling predation at high latitudes: insights from the southernmost Atlantic. Palaios 28, 3341.CrossRefGoogle Scholar
Martos, P and Piccolo, MC (1988) Hydrography of the Argentine continental shelf between 38° and 42°S. Continental Shelf Research 8, 10431056.CrossRefGoogle Scholar
Matano, RP, Palma, ED and Piola, AR (2010) The influence of the Brazil and Malvinas currents on the Southwestern Atlantic Shelf circulation. Ocean Science 6, 983995.CrossRefGoogle Scholar
Melatunan, S, Calosi, P, Rundle, SD, Widdicombe, S and Moody, AJ (2013) Effects of ocean acidification and elevated temperature on shell plasticity and its energetic basis in an intertidal gastropod. Marine Ecology Progress Series 472, 155168.CrossRefGoogle Scholar
Miller, LP (2013) The effect of water temperature on drilling and ingestion rates of the dogwhelk Nucella lapillus feeding on Mytilus edulis mussels in the laboratory. Marine Biology 160, 14891496.CrossRefGoogle Scholar
Mondal, S, Chakraborty, H, Saha, S, Dey, S and Sarkar, D (2021) 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, e0256685.CrossRefGoogle ScholarPubMed
Nixon, M (1979) Hole-boring in shells by Octopus vulgaris Cuvier in the Mediterranean. Malacologia 18, 431443.Google Scholar
Nixon, M and Boyle, P (1982) Hole-drilling in crustaceans by Eledone cirrhosa (Mollusca: cephalopods). Journal of Zoology, London 196, 439444.CrossRefGoogle Scholar
Nixon, M and Maconnachie, E (1988) Drilling by Octopus vulgaris (Mollusca: Cephalopoda) in the Mediterranean. Journal of Zoology 216, 687716.CrossRefGoogle Scholar
O'Neill, M, Mala, R, Cafiso, D, Bignardi, C and Taylor, D (2018) Repair and remodelling in the shells of the limpet Patella vulgata. Journal of the Royal Society Interface 15, 20180299.CrossRefGoogle ScholarPubMed
Orselli, IBM, Kerr, R, Ito, RG, Tavano, VM, Mendes, CRB and Garcia, CAE (2018) How fast is the Patagonian shelf-break acidifying? Journal of Marine Systems 178, 114.CrossRefGoogle Scholar
Paine, RT (1966) Food web complexity and species diversity. American Naturalist 100, 6575.CrossRefGoogle Scholar
Parker, G, Paterlini, MC and Violante, RA (1997) El fondo marino. In Boschi, EE (ed.), El Mar Argentino y sus recursos pesqueros. Tomo 1. Antecedentes históricos de las exploraciones en el mar y las características ambientales. Mar del Plata: INIDEP, pp. 6587.Google Scholar
Pilson, ME and Taylor, PB (1961) Hole drilling by octopus. Science 134, 13661368.CrossRefGoogle ScholarPubMed
Podestá, GP (1997) Utilización de datos satelitarios en investigaciones oceanográficas y pesqueras en el Océano Atlántico Sudoccidental. In Boschi, EE (ed.), El Mar Argentino y sus recursos pesqueros. Tomo 1. Antecedentes históricos de las exploraciones en el mar y las características ambientales. Mar del Plata: INIDEP, pp. 195222.Google Scholar
R Core Team (2015) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. http://www.r-ptoject.orgGoogle Scholar
Sabatini, ME and Álvarez Colombo, GL (2001) Seasonal pattern of zooplankton biomass in the Argentinian shelf off Southern Patagonia (45°–55° S). Scientia Marina 65, 2131.CrossRefGoogle Scholar
Sabatini, ME, Reta, R, Lutz, VA, Segura, V and Daponte, C (2016) Influence of oceanographic features on the spatial and seasonal patterns of mesozooplankton in the southern Patagonian shelf (Argentina, SW Atlantic). Journal of Marine Systems 157, 2038.CrossRefGoogle Scholar
Sanford, E, Gaylord, B, Hettinger, A, Lenz, EA, Meyer, K and Hill, TM (2014) Ocean acidification increases the vulnerability of native oysters to predation by invasive snails. Proceedings of the Royal Society B 281, 20132681.CrossRefGoogle ScholarPubMed
Segura, V, Lutz, V, Dogliotti, A, Silva, R, Negri, R, Akselman, R and Benavides, H (2013) Phytoplankton types and primary production in the Argentine Sea. Marine Ecology Progress Series 491, 1531.CrossRefGoogle Scholar
Silvy, Y, Guilyardi, E, Sallée, JB et al. (2020) Human-induced changes to the global ocean water masses and their time of emergence. Nature Climate Change 10, 10301036.CrossRefGoogle Scholar
Tomašových, A and Kidwell, SM (2009) Fidelity of variation in species composition and diversity partitioning by death assemblages: time-averaging transfers diversity from beta to alpha levels. Paleobiology 35, 94118.CrossRefGoogle Scholar
Tull, DS and Bohning-Gaese, K (1993) Patterns of drilling predation on gastropods of the family Turritellidae in the Gulf of California. Paleobiology 19, 476486.CrossRefGoogle Scholar
Vermeij, GJ (1980) Drilling predation of bivalves in Guam: some paleoecological implications. Malacologia 19, 329334.Google Scholar
Vermeij, GJ and Carlson, SJ (2000) The muricid gastropod subfamily Rapaninae: phylogeny and ecological history. Paleobiology 26, 1946.2.0.CO;2>CrossRefGoogle Scholar
Vermeij, GJ, Dudley, EC and Zipser, E (1989) Successful and unsuccessful drilling predation in recent pelecypods. Veliger 32, 266273.Google Scholar
Violante, RA, Costa, IP, Cavallotto, JL, Paterlini, CM, Marcolini, S and Bozzano, G (2014) Rasgos morfosedimentarios, procesos y evolución de la plataforma continental argentina desde el último máximo glacial. Revista de la Asociación Geológica Argentina 71, 292310.Google Scholar
Visaggi, CC and Kelley, PH (2015) Equatorward increase in naticid gastropod drilling predation on infaunal bivalves from Brazil with paleontological implications. Palaeogeography, Palaeoclimatology, Palaeoecology 438, 285299.CrossRefGoogle Scholar
Watson, SA, Fields, JB and Munday, PL (2017) Ocean acidification alters predator behaviour and reduces predation rate. Biology Letters 13, 20160797.CrossRefGoogle ScholarPubMed
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