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The targeting of large-sized benthic macrofauna by an invasive portunid predator: evidence from a caging study

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Abstract

The Portunid crab Charybdis japonica was first found in Waitemata Harbour, New Zealand, in 2000. It has established breeding populations and has been spreading, yet information on its dietary preferences in New Zealand are unknown. We conducted field caging experiments to elucidate prey choices and potential impacts of Charybdis on benthic communities. We tested the hypothesis that Charybdis would reduce the previously demonstrated positive influence of native pinnid bivalves, Atrina zelandica, on the abundance and richness of surrounding soft-sediment macrofauna. Adult male Charybdis were introduced to cages with and without Atrina that included soft-sediment macrofaunal communities of ambient composition and abundance. After leaving the crabs to feed overnight, changes in community structure (relative to sediments without crabs) were determined by coring the sediment and analysing the resident macrofauna. Prey choices were verified by extracting taxa from the stomachs of crabs collected from the cages in which they had been feeding. The abundance of large taxa including burrowing urchins, bivalves and native crabs was lower in the presence of Charybdis compared to areas without this invader. The stomach contents of Charybdis were dominated by these same three taxa, constituting 85 % of the prey abundance when using stomach fullness as a weighting factor. Our hypothesis was supported with the greatest net losses occurring in cages with Charybdis and Atrina. Reduction in the abundance of Echinocardium cordatum by Charybdis could have cascading ecological effects, as these urchins play a critical role in benthic soft-sediment ecosystems in New Zealand via bioturbation and biogenic disturbance.

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References

  • Ahyong ST, Wilkens SL (2011) Aliens in the antipodes: non-indigenous marine crustaceans of New Zealand and Australia. In: Galil BS, Clark PF, Carlton JT (eds) In the wrong place—alien marine crustaceans: distribution, biology and impacts. Invading nature—Springer series in invasion ecology 6:451–485

  • Brazao SAE, Silva ACF, Boaventura DM (2009) Predation: a regulating force of intertidal assemblages on the central Portuguese coast? J Mar Biol Assoc UK 89:1541–1548

    Article  Google Scholar 

  • Buchanan JB (1966) The biology of Echinocardium cordatum [Echinodermata: Spatangoidea] from different habitats. J Mar Biol Assoc UK 46:97–114

    Article  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:2075

    Article  Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Choy SC (1986) Natural diet and feeding habits of the crabs Liocarcinus puber and L. holsatus (Decapoda, Brachyura, Portunidae). Mar Ecol Prog Ser 31:87–99

    Article  Google Scholar 

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558

    Article  CAS  PubMed  Google Scholar 

  • Cohen AN, Carlton JT, Fountain MC (1995) Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San-Francisco Bay, California. Mar Biol 122:225–237

    Google Scholar 

  • Cranfield HJ, Gordon DP, Willan RC et al (1998) Adventive marine species in New Zealand. NIWA Technical Report 34, p 48. http://docs.niwa.co.nz/library/public/NIWAtr34.pdf

  • Davidson, RJ (1986) Natural food and predatory activity of the paddle crab Ovalipes. MSc Thesis, University of Canterbury Christchurch. http://ir.canterbury.ac.nz/bitstream/10092/6681/1/davidson_thesis.pdf

  • Dineen JF, Clark PF, Hines AH et al (2001) Life history, larval description, and natural history of Charybdis hellerii (Decapoda, Brachyura, Portunidae), an invasive crab in the western Atlantic. J Crustacean Biol 21:774–805

    Article  Google Scholar 

  • Elner RW, Hughes RN (1978) Energy maximization in the diet of the shore crab, Carcinus maenas. J Anim Ecol 47:103–116

    Article  Google Scholar 

  • Essink K, Dekker R (2002) General patterns in invasion ecology tested in the Dutch Wadden Sea: the case of a brackish-marine polychaetous worm. Biol Invasions 4:359–368

    Article  Google Scholar 

  • Fernandes TF, Huxham M, Piper SR (1999) Predator caging experiments: a test of the importance of scale. J Exp Mar Biol Ecol 241:137–154

    Article  Google Scholar 

  • Fowler AE, Gerner NV, Sewell MA (2011) Temperature and salinity tolerances of Stage 1 zoeae predict possible range expansion of an introduced portunid crab, Charybdis japonica, in New Zealand. Biol Invasions 13:691–699

    Article  Google Scholar 

  • Froglia D (2012) First record of Charybdis japonica (Crustacea: Decapoda: Portunidae) in the Mediterranean Sea. Mar Biodivers Rec 5:0-3

    Google Scholar 

  • Galil BS (2000) A sea under siege—alien species in the Mediterranean. Biol Invasions 2:177–186

    Article  Google Scholar 

  • Godfriaux BL (1969) Food of predatory demersal fish in Hauraki Gulf. N Z J Mar Freshw Res 3:518–544

    Article  Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    Article  PubMed  Google Scholar 

  • Gust N, Inglis GJ (2006) Adaptive multi-scale sampling to determine an invasive crab’s habitat usage and range in New Zealand. Biol Invasions 8:339–353

    Article  Google Scholar 

  • Hall SJ, Raffaelli D, Robertson MR et al (1990) The role of the predatory crab, Liocarcinus depurator, in a marine food web. J Anim Ecol 59:421–438

    Article  Google Scholar 

  • Hayward BW (1997) Introduced marine organisms in New Zealand and their impact in the Waitemata Harbour, Auckland. Tane 36:197–223

    Google Scholar 

  • Hayward BW, Stephenson AB, Morley M et al (1997) Faunal changes in Waitemata Harbour sediments, 1930s–1990s. J R Soc N Z 27:1–20

    Article  Google Scholar 

  • Hewitt JE, Thrush SF, Legendre P et al (2002) Integrating heterogeneity across spatial scales: interactions between Atrina zelandica and benthic macrofauna. Mar Ecol Prog Ser 239:115–128

    Article  Google Scholar 

  • Hidalgo FJ, Baron PJ, Orensanz JM (2005) A prediction come true: the green crab invades the Patagonian coast. Biol Invasions 7:547–552

    Article  Google Scholar 

  • Hines AH (1982) Coexistence in a kelp forest: size population dynamics and resource partitioning in a guild of spider crabs (Brachyura, Majidae). Ecol Monogr 52:17–198

    Article  Google Scholar 

  • Hollebone AL, Hay ME (2008) An invasive crab alters interaction webs in a marine community. Biol Invasions 10:347–358

    Article  Google Scholar 

  • Inglis G, Gust N, Fitridge I, Floerl O, Hayden BJ, Fenwick G (2005a) Port of Auckland: baseline survey for non-indigenous marine species. Biosecurity New Zealand Technical Paper No: 2005/08: 58. http://www.biosecurity.govt.nz/files/pests/salt-freshwater/2005-08-port-of-auckland.pdf

  • Inglis GJ, Gust N, Fitridge I et al (2005b) Gulf Harbour Marina: baseline survey for non-indigenous marine species. Biosecurity New Zealand Technical Paper 2005/12. http://maxa.maf.govt.nz/mafnet/publications/biosecurity-technical-papers/2005-12-gulf-harbour-marina.pdf

  • Jiang W, Meng T, Chen R et al (1998) Diet of Charybdis japonica (A. Miline-Dewards Milne-Edwards) and Portunus trituberculatus (Miers) in the Bohai Sea. Mar Fish Res 19:53–59

    Google Scholar 

  • Kennish MJ (1997) Pollution impacts on marine biotic communities. CRC Press, Boca Raton

    Google Scholar 

  • Kim KB (2001) Growth and Reproduction of Charybdis japonica (A. Milne-Edwards) (De-capoda: Portunidae) in Korean Waters, Ph.D. Thesis, Department of Marine Biology, Graduate School, Pukyong National University, Pusan (in Korean)

  • King RB, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84:108–115

    Article  Google Scholar 

  • Kolpakov NV, Kolpakov EV (2011) On the biology of the Japanese Swimming Crab Charybdis japonica (Portunidae) in waters of primorye at the northern boundary of their range. Russ J Mar Biol 37(7):570–578

    Article  Google Scholar 

  • le Roux PJ, Branch GM, Joska MAP (1990) On the distribution, diet and possible impact of the invasive European shore crab Carcinus maenas (L.) along the South African coast. S Afr J Mar Sci 9(1):85–93

    Article  Google Scholar 

  • Lemaitre R (1995) Charybdis hellerii (Milne Edwards, 1867), a nonindigenous portunid crab (Crustacea: Decapoda: Brachyura) discovered in the Indian River lagoon system of Florida. Proc Biol Soc Wash 108:643–648

    Google Scholar 

  • Lohrer AM, Whitlatch RB (2002) Interactions among aliens: apparent replacement of one exotic species by another. Ecology 83:719–732

    Article  Google Scholar 

  • Lohrer AM, Thrush SF, Gibbs MM (2004) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–1095

    Article  CAS  PubMed  Google Scholar 

  • Lohrer AM, Chiaroni LD, Hewitt JE et al (2008a) Biogenic disturbance determines invasion success in a subtidal soft-sediment system. Ecology 89:1299–1307

    Article  PubMed  Google Scholar 

  • Lohrer AM, Chiaroni LD, Hewitt JE et al (2008b) Isolated and interactive effects of two key species on ecosystem function and trophic linkages in New Zealand soft-sediment habitats. NZ Aquatic Environment and Biodiversity Report for the Ministry of Fisheries (Project ZBD200419). NIWA Report number HAM2008-106. http://docs.niwa.co.nz/library/public/NZAEBR44.pdf

  • Lohrer AM, Rodil IF, Townsend M et al (2013) Biogenic habitat transitions influence facilitation in a marine soft-sediment ecosystem. Ecology 94:136–145

    Article  PubMed  Google Scholar 

  • Loreau M, Naeem S, Inchausti P (2002) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford

    Google Scholar 

  • MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609

    Article  Google Scholar 

  • Mantelatto FLM, Garcia RB (2001) Biological aspects of the nonindigenous portunid crab Charybdis hellerii in the western tropical south Atlantic. Bull Mar Sci 68:469–477

    Google Scholar 

  • McMillen-Jackson AL (2008) First record of the Indo-Pacific swimming crab, Charybdis hellerii (A. Milne-Edwards, 1867) in the Gulf of Mexico. Crustac Int J Crustac Res 81:889–894

    Article  Google Scholar 

  • Miron G, Audet D, Landry T et al (2005) Predation potential of the invasive green crab (Carcinus maenas) and other common predators on commercial bivalve species found on Prince Edward Island. J Shellfish Res 24:579–586

    Article  Google Scholar 

  • Morton B (1979) A comparison of lip structure and function correlated with other aspects of the functional morphology of Lima lima, Limaria (Platilimaria) fragilis, and Limaria (Platilimaria) hongkongensis sp.nov. (Bivalvia: Limacea). Can J Zool 57:728–742

    Article  Google Scholar 

  • Nakamura Y (2001) Autoecology of the heart urchin, Echinocardium cordatum, in the muddy sediment of the Seto Inland Sea, Japan. J Mar Biol Assc UK 81:289–297

    Google Scholar 

  • Needham HR, Pilditch CA, Lohrer AM et al (2011) Context-specific bioturbation mediates changes to ecosystem functioning. Ecosystems 14:1096–1109

    Article  CAS  Google Scholar 

  • Norkko A, Hewitt JE, Thrush SF et al (2001) Benthic-pelagic coupling and suspension-feeding bivalves: linking site-specific sediment flux and biodeposition to benthic community structure. Limnol Oceanogr 46:2067–2072

    Article  Google Scholar 

  • Norkko A, Hewitt JE, Thrush SF et al (2006) Conditional outcomes of facilitation by a habitat-modifying subtidal bivalve. Ecology 87:226–234

    Article  PubMed  Google Scholar 

  • Rhoads DC, Young DK (1970) The influence of deposit-feeding organisms on sediment stability and community trophic structure. J Mar Res 28:150–178

    Google Scholar 

  • Ricciardi A, Rasmussen JB (1998) Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Can J Fish Aquat Sci 55:1759–1765

    Article  Google Scholar 

  • Ruiz GM, Carlton JT, Grosholz ED et al (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632

    Google Scholar 

  • Sanders NJ, Gotelli NJ, Heller NE et al (2003) Community disassembly by an invasive species. Proc Nat Acad Sci USA 100:2474–2477

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sant’Anna BS, Watanabe TT, Turra A et al (2012a) Relative abundance and population biology of the non-indigenous crab Charybdis hellerii (Crustacea: Brachyura: Portunidae) in a southwestern Atlantic estuary-bay complex. Aquat Invasions 7:347–356

    Article  Google Scholar 

  • Sant’Anna BS, Watanabe TT, Turra A et al (2012b) First record of the non-indigenous portunid crab Charybdis variegata from the western Atlantic coast. BioInvasions Rec 1:11–16

    Article  Google Scholar 

  • Seed R, Hughes RN (1995) Criteria for prey size-selection in molluscivorous crabs with contrasting claw morphologies. J Exp Mar Biol Ecol 193:177–195

    Article  Google Scholar 

  • Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9(8):912–919

    Article  PubMed  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1(1):21–32

    Article  Google Scholar 

  • Simberloff D, Martin JL, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28(1):58–66

    Article  PubMed  Google Scholar 

  • Smith PJ, Webber WR, McVeagh SM et al (2003) DNA and morphological identification of an invasive swimming crab, Charybdis japonica, in New Zealand waters. N Z J Mar Freshw Res 37:753–762

    Article  Google Scholar 

  • Sudo H, Kajihara N, Fujii T (2008) Predation by the swimming crab Charybdis japonica and piscivorous fishes: a major mortality factor in hatchery-reared juvenile Japanese flounder Paralichthys olivaceus released in Mano Bay, Sado Island, Japan. Fish Res 89:49–56

    Article  Google Scholar 

  • Tavares M, Amouroux JM (2003) First record of the non-indigenous crab, Charybdis hellerii (A. Milne-Edwards, 1867) from French Guyana (Decapoda, Brachyura, Portunidae). Crustac Int J Crustac Res 76:625–630

    Article  Google Scholar 

  • Thorson G (1957) Bottom communities. In: Hedgpeth JW (ed) Treatise on marine ecology and paleoecology, Ch. 17 (vol 1). Ecology. Mem Geol Soc Am 67:461–534

  • Townsend M, Marshall BA, Greenfield BL (2010) First records of the Australian dog whelk, Nassarius (Plicarcularia) burchardi (Dunker in Philippi, 1849) (Mollusca: Gastropoda) from New Zealand. N Z J Mar Freshw Res 44:343–348

    Article  Google Scholar 

  • Virnstein RW (1978) Predator caging experiments in soft sediment: caution advised. In: Wiley ML (ed) Estuarine interactions. Academic Press, New York, pp 261–273

  • Vitousek PM, Dantonio CM, Loope LL et al (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Wear RG, Haddon M (1987) Natural diet of the crab Ovalipes catharus (Crustacea, Portunidae) around central and northern New Zealand. Mar Ecol Prog Ser 35:39–49

    Article  Google Scholar 

  • Webber R (2001) Space invaders, crabs that turn up in New Zealand unannounced. Seaf N Z 9:80–84

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Acknowledgments

We dedicate this paper to Jim Carlton, who continues to inspire and advance a deeper understanding of the ecology, impact, and management of invasions. This research was funded by NIWA under Coasts and Oceans Research Programmes 3 and 4 (2012/13 SCI). I.F.R. acknowledges the financial support by the postdoctoral program Ángeles Alvariño (XUGA). We would like to thank Graeme Inglis for valuable guidance with the manuscript and Naomi Parker and Andrew Bell from the Ministry of Primary Industries for their input. Barry Greenfield and Jamie Armstrong contributed to macrofaunal processing and identification and Scott Edhouse, Dave Bremner and Andy Miller assisted with fieldwork. We thank the NIWA port surveillance team for their support with trapping Charybdis.

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Townsend, M., Lohrer, A.M., Rodil, I.F. et al. The targeting of large-sized benthic macrofauna by an invasive portunid predator: evidence from a caging study. Biol Invasions 17, 231–244 (2015). https://doi.org/10.1007/s10530-014-0722-1

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