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The Science of Nature

, 106:35 | Cite as

Underwater acoustic communication during the mating behaviour of the semi-terrestrial crab Neohelice granulata

  • Francesco FiliciottoEmail author
  • María P. Sal Moyano
  • Fernando Hidalgo
  • Giovanni de Vincenzi
  • Maria C. Bazterrica
  • Maria Ceraulo
  • Valentina Corrias
  • Enza Maria Quinci
  • Martìn Lorusso
  • Salvatore Mazzola
  • Giuseppa Buscaino
  • María A. Gavio
Original Paper
  • 24 Downloads

Abstract

In semi-terrestrial crabs, the production of sounds has been recognized to be related to courtship communication dynamics. The present study aimed to assess if the crab Neohelice granulata (Varunidae) was able to emit acoustic signals and if they played a role in the crab’s behaviour. We also assessed the locomotor behaviours to examine these parameters in different mating contexts of crabs. The study was divided into two different experimental conditions: ‘solitary experiment’ (consisting of three combination layouts with male, unreceptive and receptive females alone) and ‘group experiment’ (consisting of mixed combinations layouts of males, unreceptive, and receptive females). Synchronized acoustic and video monitoring systems were used to record the acoustic signals and locomotor behaviours of alone and grouped specimens. The greatest values of locomotor behavioural parameters were observed in layouts with receptive females alone and with 2 males plus 1 receptive female, probably related to courtship behaviour. N. granulata produced two distinct signals, a multi-pulse rasp signal (highest numbers were recorded in layouts with male alone and with 2 males plus 1 receptive female) and a single rasp signal. These results may suggest that males use the multi-rasp signal to advertise their presence to other males or to attract receptive females.

Keywords

Communication Semi-terrestrial crab Neohelice granulata Acoustic signals Mating behaviour 

Notes

Acknowledgements

This work has been funded by IRSES-RECOMPRA Project (Staff Exchange Planning–Grant Agreement n. 295213) and supported by CAIMAR Joint Laboratory Italy-Argentina (Laboratori Congiunti Bilaterali Internazionali del CNR, 2017-2019) and by the project BOSS–Study of bioacoustics and applications for the sustainable exploitation of marine resources (Projects of major importance in the Scientific and Technological Collaboration Executive Programmes, funded by the Italian Ministry of Foreign Affairs and International Cooperation).

Supplementary material

114_2019_1633_MOESM1_ESM.pdf (96 kb)
ESM 1 (PDF 96 kb)

References

  1. Baldwin J, Johnsen S (2012) The male blue crab, Callinectes sapidus, uses both chromatic and achromatic cues during mate choice. J Exp Biol 215:1184–1191CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48.  https://doi.org/10.18637/jss.v067.i01> CrossRefGoogle Scholar
  3. Boon PY, Yeo DCJ, Todd PA (2009) Sound production and reception in mangrove crabs Perisesarma spp.(Brachyura: Sesarmidae). Aquat Biol 5:107–116CrossRefGoogle Scholar
  4. Bortolus A, Iribarne O (1999) Effects of the SW Atlantic burrowing crab Chasmagnathus granulata on a Spartina salt marsh. Mar Ecol Prog Ser 178:79–88CrossRefGoogle Scholar
  5. Bouwma PE, Herrnkind WF (2009) Sound production in Caribbean spiny lobster Panulirus argus and its role in escape during predatory attack by Octopus briareus. N Z J Mar Freshw Res 43:3–13CrossRefGoogle Scholar
  6. Brockerhoff AM, McLay CL (2005) Mating behaviour, female receptivity and male–male competition in the intertidal crab Hemigrapsus sexdentatus (Brachyura: Grapsidae). Mar Ecol Prog Ser 290:179–191CrossRefGoogle Scholar
  7. Buscaino G, Filiciotto F, Gristina M, Bellante A, Buffa G, di Stefano V, Maccarrone V, Tranchida G, Buscaino C, Mazzola S (2011a) Acoustic behaviour of the European spiny lobster Palinurus elephas. Mar Ecol Prog Ser 441:177–184CrossRefGoogle Scholar
  8. Buscaino G, Filiciotto F, Gristina M, Buffa G, Bellante A, Maccarrone V, Patti B, Mazzola S (2011b) Defensive strategies of European spiny lobster Palinurus elephas during predator attack. Mar Ecol Prog Ser 423:143–154CrossRefGoogle Scholar
  9. Buscaino G, Gavio A, Galvan D, Filiciotto F, Maccarrone V, de Vincenzi G, Mazzola S, Orensanz JM (2015) Acoustic signals and behaviour of Ovalipes trimaculatus in the context of reproduction. Aquat Biol 24:61–73CrossRefGoogle Scholar
  10. Bushmann PJ, Atema J (2000) Chemically mediated mate location and evaluation in the lobster, Homarus americanus. J Chem Ecol 26:883–899CrossRefGoogle Scholar
  11. Busnel RG (1963) Acoustic behaviour of animals. Elsevier, London and New York, p 933Google Scholar
  12. Christy JH, Rittschof D (2010) Deception in visual and chemical communication in crustaceans. In: Chemical communication in crustaceans. Springer, pp 313–333Google Scholar
  13. Clayton D (2008) Singing and dancing in the ghost crab Ocypode platytarsus (Crustacea, Decapoda, Ocypodidae). J Nat Hist 42:141–155CrossRefGoogle Scholar
  14. de Vincenzi G, Filiciotto F, Maccarrone V, Mazzola S, Buscaino G (2015) Behavioural responses of the European spiny lobster, Palinurus elephas (Fabricius, 1787), to conspecific and synthetic sounds. Crustaceana 88:523–540CrossRefGoogle Scholar
  15. Escapa M, Isaacch JP, Daleo P et al (2004) The distribution and ecological effects of the introduced Pacific oyster Crassostrea gigas (Thunberg, 1793) in northern Patagonia. J Shellfish Res 23:765–773Google Scholar
  16. Guinot-Dumortier D, Dumortier B (1960) La stridulation chez les crabes. Crustaceana 1:117–155CrossRefGoogle Scholar
  17. Grier JW, Burk T (1992) Biology of animal behavior, 2nd edn. Mosby, St LouisGoogle Scholar
  18. von Hagen H-O (1975) Klassifikation und phylogenetische Einordnung der Lautäußerungen von Ocypodiden und Grapsiden (Crustacea, Brachyura). J Zool Syst Evol Res 13:300–316CrossRefGoogle Scholar
  19. Imafuku M, Ikeda H (1990) Sound production in the land hermit crab Coenobita purpureus Stimpson, 1858 (Decapoda, Coenobitidae). Crustaceana 58:168–174CrossRefGoogle Scholar
  20. Isacch JP, Costa CSB, Rodríguez-Gallego L et al (2006) Distribution of saltmarsh plant communities associated with environmental factors along a latitudinal gradient on the south-West Atlantic coast. J Biogeogr 33:888–900CrossRefGoogle Scholar
  21. Jézéquel Y, Bonnel J, Coston-Guarini J, Guarini JM, Chauvaud L (2018) Sound characterization of the European lobster Homarus gammarus in tanks. Aquat Biol 27:13–23.  https://doi.org/10.3354/ab00692 CrossRefGoogle Scholar
  22. Luppi T, Bas C, Méndez-Casariego A et al (2013) Variations in activitypatterns in the estuarine crab Neohelice (= C hasmagnathus) granulata indifferent habitats, seasons and tidal regimen. Helgol Mar Res 67:1–15CrossRefGoogle Scholar
  23. Meyer-Rochow VB, Penrose JD (1976) Sound production by the western rock lobster Panulirus longipes (Milne Edwards). J Exp Mar Biol Ecol 23:191–209CrossRefGoogle Scholar
  24. Meyer-Rochow VB, Penrose JD, Oldfield BP, Bailey WJ (1982) Phonoresponses in the rock lobster Panulirus longipes (Milne Edwards). Behav Neural Biol 34:331–336CrossRefGoogle Scholar
  25. Moulton JM (1957) Sound production in the spiny lobster Panulirus argus (Latreille). Biol Bull 113:286–295CrossRefGoogle Scholar
  26. Ng PK, Guinot D, Davie PJ (2008) Systema Brachyurorum: part I. an annotated checklist of extant brachyuran crabs of the world. Raffles Bull Zool 17:1–286Google Scholar
  27. Parker AR, Mckenzie DR, Ahyong ST (1998) A unique form of light reflector and the evolution of signalling in Ovalipes (Crustacea: Decapoda: Portunidae). Proc R Soc Lond B Biol Sci 265:861–867.  https://doi.org/10.1098/rspb.1998.0371 CrossRefGoogle Scholar
  28. Patek SN (2001) Spiny lobsters stick and slip to make sound. Nature 411:153–154CrossRefGoogle Scholar
  29. Patek SN, Caldwell RL (2006) The stomatopod rumble: low frequency sound production in Hemisquilla californiensis. Mar Freshw Behav Physiol 39:99–111CrossRefGoogle Scholar
  30. Patek SN, Oakley TH (2003) Comparative tests of evolutionary trade-offs in a palinurid lobster acoustic system. Evolution 57:2082–2100CrossRefGoogle Scholar
  31. Patek SN, Shipp LE, Staaterman ER (2009) The acoustics and acoustic behavior of the California spiny lobster (Panulirus interruptus). J Acoust Soc Am 125:3434–3443CrossRefGoogle Scholar
  32. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag, New YorkCrossRefGoogle Scholar
  33. Popper AN, Salmon M, Horch KW (2001) Acoustic detection and communication by decapod crustaceans. J Comp Physiol A 187:83–89CrossRefGoogle Scholar
  34. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 26 Nov 2018Google Scholar
  35. Reta R, Martos P, Perillo GME, et al (2001) Características hidrográficas del estuario de la laguna Mar Chiquita. Reserva Biósfera Mar Chiquita Características Físicas Biológicas Ecológicas Ed Martín Mar Plata 31–41Google Scholar
  36. Sal Moyano MP, Gavio MA, Luppi TA (2012a) Mating system of the burrowing crab Neohelice granulata (Brachyura: Varunidae) in two contrasting environments: effect of burrow architecture. Mar Biol 159:1403–1416CrossRefGoogle Scholar
  37. Sal Moyano MP, Gavio MA, McLay CL, Luppi T (2014a) Habitat-related differences in the pre-copulatory guarding and copulation behavior of Neohelice granulata (Brachyura, Grapsoidea, Varunidae). J Sea Res 87:8–16CrossRefGoogle Scholar
  38. Sal Moyano MP, Luppi T, Gavio MA, Vallina M, McLay C (2012b) Receptivity of female Neohelice granulata (Brachyura, Varunidae): different strategies to maximize their reproductive success in contrasting habitats. Helgol Mar Res 66:661–674CrossRefGoogle Scholar
  39. Sal Moyano MP, Silva P, Luppi T, Gavio MA (2014b) Female mate choice by chemical signals in a semi-terrestrial crab. J Sea Res 85:300–307CrossRefGoogle Scholar
  40. Salmon M (1967) Coastal distribution, display and sound production by Florida fiddler crabs (genus Uca). Anim Behav 15:449–459.  https://doi.org/10.1016/0003-3472(67)90043-7 CrossRefPubMedGoogle Scholar
  41. Salmon M, Horch KW (1972) Acoustic Signalling and detection by Semiterrestrial crabs of the family Ocypodidae. In: Winn HE, Olla BL (eds) Behavior of marine animals. Springer US, pp 60–96Google Scholar
  42. Spivak ED (2010) The crab Neohelice (= Chasmagnathus) granulata: an emergent animal model from emergent countries. Helgol Mar Res 64:149–154CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Francesco Filiciotto
    • 1
    Email author
  • María P. Sal Moyano
    • 2
  • Fernando Hidalgo
    • 2
  • Giovanni de Vincenzi
    • 3
  • Maria C. Bazterrica
    • 2
  • Maria Ceraulo
    • 4
  • Valentina Corrias
    • 3
  • Enza Maria Quinci
    • 4
  • Martìn Lorusso
    • 2
  • Salvatore Mazzola
    • 4
  • Giuseppa Buscaino
    • 4
  • María A. Gavio
    • 2
  1. 1.Consiglio Nazionale delle RicercheIstituto di Scienze Polari (ISP-CNR)MessinaItaly
  2. 2.Instituto de Investigaciones Marinas y Costeras (IIMyC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Estación Costera J. J. Nágera, Facultad de Ciencias Exactas y NaturalesUniversidad Nacional de Mar del PlataMar del PlataArgentina
  3. 3.Consiglio Nazionale delle Ricerche–Istituto per le Risorse Biologiche e le Biotecnologie MarineMessina (IRBIM-CNR)MessinaItaly
  4. 4.Consiglio Nazionale delle Ricerche - Istituto per lo studio degli impatti Antropici e Sostenibilità in ambientemarinoCapo Granitola (IAS-CNR)SicilyItaly

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