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Seasonal variation of peracarid assemblages in natural and artificial marine environments of the Southwestern Atlantic Ocean

  • Carlos Rumbold
  • Sandra Obenat
  • Samira Nuñez Velazquez
  • Brian Gancedo
  • Eduardo Spivak
Original Paper

Abstract

The diversity and seasonal variations of two assemblages of marine benthic peracarids were studied between a natural rocky shore and an artificial harbour area over a 12-month period. Samples were obtained monthly in La Estafeta, a rocky intertidal zone with low human impact, and Mar del Plata Harbour, a polluted environment, between March 2011 and March 2012. The two sites differed markedly in the composition and abundance of species across all seasons: the tanaid Tanais dulongii was most abundant in La Estafeta rocky shore, followed by the amphipods Monocorophium acherusicum, Hyale grandicornis, Ampithoe valida, the isopod Idotea balthica, the tanaid Leptochelia sp. and the isopod Sphaeroma serratum. In contrast, M. acherusicum was most abundant in the harbour area, followed by T. dulongii, S. serratum, Ericthonius punctatus, I. balthica, Caprella equilibra and C. dilatata. Total density of peracarids varied between months in La Estafeta rocky shore and Mar del Plata Harbour. In La Estafeta rocky shore mean density increased from March to May 2011 (autumn in the southern hemisphere; ca. 45,000 ind/m2), decreased sharply until August and then increased in January 2012. In Mar del Plata Harbour the mean density was lower from March to October (ca. 500,000 ind/m3), then increased and reached a maximum in January 2012 (more than 1,500,000 ind/m3), and decreased until the following March. This study suggests that the differences in peracarid assemblages, diversity and seasonality could be related to an effect of temperature, but we should not rule out a synergistic effect of other factors, such as pollution, food availability and hydrodynamic factors.

Keywords

Diversity Harbour Intertidal Peracarida Seasonal variation 

Notes

Acknowledgements

This paper was funded by Grants from the Universidad Nacional de Mar del Plata (EXA 610/12, EXA705/14) and from the Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET) (PIP 112-201101-00830). Finally, we appreciate the important comments and suggestions made by Dr. Stefanie Kaiser and three anonymous referees that largely improved the manuscript.

References

  1. Adami ML, Tablado A, López-Gappa JL (2004) Spatial and temporal variability in intertidal assemblages dominated by the mussel Brachidontes rodriguezii (d’Orbigny, 1846). Hydrobiologia 520:49–59CrossRefGoogle Scholar
  2. Albano MJ (2012) Patrones de distribución y abundancia de invertebrados bentónicos exóticos en áreas naturales y portuarias de la provincia de Buenos Aires. Dissertation, Universidad Nacional de Mar del PlataGoogle Scholar
  3. Albano MJ, Obenat SM (2009) Assemblage of benthic macrofauna in the aggregates of the tubiculous worm Phyllochaetopterus socialis in the Mar del Plata harbour, Argentina. J Mar Biol Assoc UK 89:1099–1108CrossRefGoogle Scholar
  4. Albano MJ, Seco Pon J, Obenat S (2006) Macrozoobentos asociado a los agregados de Phyllochaetopterus socialis Claparède, 1870 en el puerto de Mar del Plata, Argentina. Rev Invest Mar 34:197–203Google Scholar
  5. Albano MJ, Lana P, Bremec C, Elías R, Martins C, Venturini N, Muniz P, Rivero S, Vallarino EA, Obenat S (2013) Macrobenthos and multi–molecular markers as indicators of environmental contamination in a South American port (Mar del Plata, Southwest Atlantic). Mar Pollut Bull 73:102–114CrossRefPubMedGoogle Scholar
  6. Alonso GM (1984) Anfipodos Gammarideos litorales del Mar Austral Argentino (Crustacea Amphipoda Gammaridea). Dissertation, Universidad de Buenos AiresGoogle Scholar
  7. Alonso GM (2004) Crustáceos anfípodos. In: Boschi EE, Cousseau MB (eds) La vida entre mareas: vegetales y animales de las costas de Mar del Plata, Argentina. Publicaciones Especiales INIDEP, Mar del Plata, pp 169–178Google Scholar
  8. Baeza JA, Farías NE, Luppi TA, Spivak ED (2010) Refuge size, group living and symbiosis: testing the “resource economic monopolization” hypothesis with the shrimp Betaeus lilianae and description of its partnership with the crab Platyxanthus crenulatus. J Exp Mar Biol Ecol 389:85–92CrossRefGoogle Scholar
  9. Bastida RO (2004) Crustáceos isópodos. In: Boschi EE, Cousseau MB (eds) La vida entre mareas: vegetales y animales de las costas de Mar del Plata, Argentina. Publicaciones Especiales INIDEP, Mar del Plata, pp 187–204Google Scholar
  10. Bastida RO, Capezzani DAA, Torti MR (1971) Los organismos incrustantes del Puerto de Mar del Plata. I. Siphonaria lessoni (Blainville, 1824). Aspectos ecológicos y biométricos. LEMIT Serie II 149:200–233Google Scholar
  11. Bertness MD (1999) The ecology of Atlantic shorelines. Sinauer Associates, SunderlandGoogle Scholar
  12. Brankevich G, Bastida R, Lemmi C (1988) A comparative study of biofouling settlements in different sections of Necochea power plant (Quequén Port, Argentina). Biofouling 1:113–135CrossRefGoogle Scholar
  13. Bueno M, Dena-Silva SA, Flores AAV, Leite FPP (2016) Effects of wave exposure on the abundance and composition of amphipod and tanaidacean assemblages inhabiting intertidal coralline algae. Mar Biol Assoc UK 96:761–767Google Scholar
  14. Carcedo C, Fiori S, Bremec C (2015) Macrobenthic surf zone communities of temperate sandy beaches: Spatial and temporal patterns. Mar Ecol 36:326–336CrossRefGoogle Scholar
  15. Chapman JW (2007) Amphipoda. In: Carlton JT (ed) The Light and Smith Manual: Intertidal Invertebrates from Central California to Oregon. The University of California Press, Richmond, pp 545–630Google Scholar
  16. Chen K, Tian S, Jiao JJ (2010) Macrobenthic community in Tolo Harbour, Hong Kong and its relations with heavy metals. Estuar Coast 33:600–608CrossRefGoogle Scholar
  17. Chiesa IL, Alonso GM (2014) Amphipoda. In: Calcagno JA (ed) Los Invertebrados Marinos. Fundación de Historia Natural Félix de Azara. Editorial Vazquez Mazzini, Buenos Aires, pp 265–276Google Scholar
  18. Chintiroglou CC, Antoniadou C, Baxevanis A, Damianidis P, Karalis P, Vafidis D (2004) Peracarida populations of hard substrate assemblages in ports of the NW Aegean Sea (eastern Mediterranean). Helgoland Mar Res 58:54–61CrossRefGoogle Scholar
  19. Clarke K, Gorley R (2006) PRIMER v6. User Manual/Tutorial. PRIMER-E, PlymouthGoogle Scholar
  20. Clarke K, Warwick R (1994) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. PRIMER–E, PlymouthGoogle Scholar
  21. Cuevas JM, Martin JP, Bastida R (2006) Benthic community changes in a patagonian intertidal: a forty years later comparison. Thalassas 22:29–37Google Scholar
  22. Darbra RM, Pittam N, Royston KA, Darbra JP, Journee H (2009) Survey on environmental monitoring requirements of European ports. J Environ Manage 90:1396–1403CrossRefPubMedGoogle Scholar
  23. R Development Core Team (2011) R: A Language and environment for statistical computing. R foundation for statistical computing. Version R 2.13.0. Vienna: R Development Core Team. Computer programGoogle Scholar
  24. Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263CrossRefGoogle Scholar
  25. El-Din MIS, Sakiko Y, Mohamed SZ, Bedir MA, Bahgat IM, Nishimura O (2014) Investigating the use of Sphaeroma serratum (Crustacea, Isopoda) as bio–indicator for heavy metals pollution in Lake Timsah, Suez Canal using alkaline comet assay technique. Egypt Acad J Biol Sci 6:7–26Google Scholar
  26. Esquete P, Moreira J, Troncoso JS (2011) Peracarid assemblages of Zostera meadows in an estuarine ecosystem (O Grove inlet, NW Iberian Peninsula): spatial distribution and seasonal variation. Helgoland Mar Res 65:445–455CrossRefGoogle Scholar
  27. Excoffon AC, Genzano GN, Zamponi MO (1999) Macrobentos asociado con una población de Antothoe chilensis (Lesson. 1830) (Cnidaria, Actiniaria) en el puerto de Mar del Plata, Argentina. Cienc Mar 25:177–191Google Scholar
  28. Fockedey N, Meesa J, Vangheluwe M, Verslycked T, Janssen CR, Vincxa M (2005) Temperature and salinity effects on postmarsupial growth of Neomysis integer (Crustacea: Mysidacea). J Exp Mar Biol Ecol 326:27–47CrossRefGoogle Scholar
  29. Galil BS, Clark PF, Carlton JT (2011) In the wrong place - alien marine crustaceans: distribution, biology and impacts. Invading Nature-Springer Series in Invasion Ecology 6. Springer, DordrechtGoogle Scholar
  30. Genzano G, Giberto D, Bremec C (2011) Benthic survey of natural and artificial reefs off Mar del Plata, Argentina. Lat Am J Aquat Res 39:553–566CrossRefGoogle Scholar
  31. Goldberg RN, Averbuj A, Cledón M, Luzzatto D, Sbarbati–Nudelman N (2004) Search for triorganotins along the Mar del Plata (Argentina) marine coast: finding of tributyltin in egg capsules of a snail Adelomelon brasiliana (Lamarck, 1822) population showing imposex effects. Appl Organomet Chem 18:117–123CrossRefGoogle Scholar
  32. Guerra-García JM, García–Gómez JC (2004) Crustacean assemblages and sediment pollution in an exceptional case study: a harbour with two opposing entrances. Crustaceana 77:353–370CrossRefGoogle Scholar
  33. Guerra-García JM, Tierno de Figueroa JM (2009) What do caprellids (Crustacea: Amphipoda) feed on? Mar Biol 156:1881–1890CrossRefGoogle Scholar
  34. Guerra-García JM, Ros M, Sánchez JA (2009) Isopods, tanaids and cumaceans (Crustacea, Peracarida) associated to the seaweed Stypocaulon scoparium in the Iberian Peninsula. Zool Baetica 20:35–48Google Scholar
  35. Guerra-García JM, Cabezas MP, Baeza–Rojano E, García–Gómez JC (2010) Na, K, Ca and Mg of intertidal caprellids (Crustacea: Amphipoda). Mar Biol Res 6:321–326CrossRefGoogle Scholar
  36. Henninger TO, Froneman PW, Booth AJ, Hodgson AN (2010) Growth and longevity of Exosphaeroma hylocoetes (Isopoda) under varying conditions of salinity and temperature. J Afr Zool 45:41–51CrossRefGoogle Scholar
  37. Hosono T (2011) Effect of temperature on growth and maturation pattern of Caprella mutica (Crustacea, Amphipoda): does the temperatura size rule function in caprellids? Mar Biol 158:363–370CrossRefGoogle Scholar
  38. Isla FI (2004) Geología del sudeste de Buenos Aires. In: Boschi EE, Cousseau MB (eds) La vida entre mareas: vegetales y animales de las costas de Mar del Plata, Argentina. Publicaciones Especiales INIDEP, Mar del Plata, pp 19–28Google Scholar
  39. Isla IF, Lasta CA (2006) Manual de manejo costero para la Provincia de Buenos Aires. Eudem, Mar del PlataGoogle Scholar
  40. Izquierdo D, Guerra-García JM (2011) Distribution patterns of the peracarid crustaceans associated with the alga Corallina elongata along the intertidal rocky shores of the Iberian Peninsula. Helgoland Mar Res 65:233–243CrossRefGoogle Scholar
  41. Johnson WS, Stevens M, Watling L (2001) Reproduction and development of Marine Peracaridans. Adv Mar Biol 39:105–260CrossRefGoogle Scholar
  42. Kalkan E, Karhan SÜ, Mutlu E, Simboura N, Bekbölet M (2007) Application of the bentix index in assessing ecological quality of hard substrata: a case study from the Bosphorus Strait, Turkey. Mediterr Mar Sci 8–1:15–29Google Scholar
  43. Kneib RT (1984) Patterns of invertebrate distribution and abundance in the intertidal salt marsh: causes and questions. Estuaries 7:392–412CrossRefGoogle Scholar
  44. Laitano MV, Castro IB, Costa PG, Fillmann G, Cledón M (2015) Butyltin and PAH contamination of Mar del Plata port (Argentina) sediments and their influence on adjacent coastal regions. Bull Environ Contam Toxicol 95:513–520CrossRefPubMedGoogle Scholar
  45. LeCroy S (2007) An illustrated identification guide to the nearshore marine and estuarine gammaridean Amphipoda of Florida. Families Anamixidae, Eusiridae, Hyalellidae, Hyalidae, Iphimedidae, Ischyroceridae, Lysianassidae, Megaluropidae and Melphidippidae. United States Environmental Protection Agency. http://publicfiles.dep.state.fl.us/dear/labs/biology/biokeys/amphipoda_fl_v4.pdf. Accessed 29 November 2015
  46. Lee JS, Lee KT (2005) Delayed mortality of benthic amphipods Monocorophium acherusicum exposed to various pollutants in seawater (Cd, Cu, Hg, TBT, ammonia and phenanthrene). J Environ Toxicol 20:133–141Google Scholar
  47. Lee WY, Macko SA, Nicol JAC (1981) Changes in nesting behavior and lipid content of a marine amphipod (Amphithoe valida) to the toxicity of no. 2 fuel oil. Water Air Soil Poll 15:185–195CrossRefGoogle Scholar
  48. López-Gappa J, Sueiro MC (2007) The subtidal macrobenthic assemblages of Bahía San Sebastián (Tierra Del Fuego, Argentina). Polar Biol 30:679–687CrossRefGoogle Scholar
  49. López-Gappa J, Alonso GM, Landoni NA (2006) Biodiversity of benthic Amphipoda (Crustacea: Peracarida) in the Southwest Atlantic between 35°S and 56°S. Zootaxa 1342:1–66Google Scholar
  50. Lourido A, Moreira J, Troncoso JS (2008) Assemblages of peracarid crustaceans in subtidal sediments from the Ría de Aldán (Galicia, NW Spain). Helgoland Mar Res 62:289–301CrossRefGoogle Scholar
  51. Maranhão P, Marques JC (2003) The influence of temperature and salinity on the duration of embryonic development, fecundity and growth of the amphipod Echinogammarus marinus Leach (Gammaridae). Acta Oecol 24:5–13CrossRefGoogle Scholar
  52. Martin JW, Davis GE (2006) Historical trends in crustacean systematics. Crustaceana 79:1347–1368CrossRefGoogle Scholar
  53. Martínez–Lladó X, Gibert O, Martí V, Díez S, Romo J, Bayona JM, De Pablo J (2007) Distribution of polycyclic aromatic hydrocarbons (PAHs) and tributyltin (TBT) in Barcelona harbour sediments and their impact on benthic communities. Environ Pollut 149:104–113CrossRefPubMedGoogle Scholar
  54. McKenney CL, Celestial DM (1995) Interactions among salinity, temperature, and growth of the estuarine mysid Mysidopsis bahia reared in the laboratory in the complete life cycle. 1. Body mass and age specific growth rate. J Crustacean Biol 15:169–178CrossRefGoogle Scholar
  55. McQuaid CD, Branch GM (1984) Influence of sea temperature, substratum and wave exposure on rocky intertidal communities – an analysis of faunal and floral biomass. Mar Ecol Prog Ser 19:145–151CrossRefGoogle Scholar
  56. Mendez MM, Schwindt E, Bortolus A, Roche A, Maggioni M, Narvarte M (2015) Ecological impacts of the austral–most population of Crassostrea gigas in South America: a matter of time? Ecol Res 30:979–987CrossRefGoogle Scholar
  57. Pearson TH, Rosenberg R (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr Mar Biol 16:229–311Google Scholar
  58. Penchaszadeh PE, Averbuj A, Cledón M (2001) Imposex in Gastropods from Argentina (south–western Atlantic). Mar Pollut Bull 42:790–791CrossRefPubMedGoogle Scholar
  59. Perez–Schultheiss J (2009) Composición y diversidad de la fauna de Amphipoda (Crustacea, Peracarida) asociada a instalaciones acuícolas de Bahía Metri, Región de Los Lagos, Chile. Informe final. Centro de Estudios en Biodiversidad, Chile (CEBCh). https://centroestudiosbiodiversidad.files.wordpress.com/2009/08/informe_amphipoda_metri1.pdf. Accessed 27 November 2015
  60. Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144CrossRefGoogle Scholar
  61. Pöckl M (1992) Effects of temperature, age and body size on moulting and growth in the freshwater amphipods Gammarus fossarum and G. roeseli. Freshwater Biol 27:211–225CrossRefGoogle Scholar
  62. Prato E, Danieli A, Maffia M, Biandolino F (2012) Lipid Contents and Fatty Acid Compositions of Idotea baltica and Sphaeroma serratum (Crustacea: Isopoda) as Indicators of Food Sources. Zool Stud 51:38–50Google Scholar
  63. Rechimont ME, Galván DE, Sueiro MC, Casas G, Piriz ML, Diez ME, Primost M, Zabala MS, Márquez F, Brogger M, Alfaya JEF, Bigatti G (2013) Benthic diversity and assemblage structure of a north Patagonian rocky shore: a monitoring legacy of the NaGISA project. J Mar Biol Assoc UK 93:2049–2058CrossRefGoogle Scholar
  64. Reizopouloua S, Nicolaidou A (2004) Benthic diversity of coastal brackish–water lagoons in western Greece. Aquat Conserv 14:S93–S102CrossRefGoogle Scholar
  65. Rivero MS, Elías R, Vallarino EA (2005) First survey of macroinfauna in the Mar del Plata Harbour (Argentina), and the use of polychaetes as pollution indicators. Rev Biol Mar Oceanogr 40:101–108CrossRefGoogle Scholar
  66. Rumbold CE, Obenat SM, Spivak ED (2012) Life history of Tanais dulongii (Tanaidacea: Tanaidae) in an intertidal flat in the Southwestern Atlantic. J Crustacean Biol 32:891–898CrossRefGoogle Scholar
  67. Rumbold CE, Obenat SM, Spivak ED (2015) Comparison of life history traits of Tanais dulongii (Tanaidacea: Tanaididae) in natural and artificial marine environments of the south-western Atlantic. Helgoland Mar Res 69:231–242CrossRefGoogle Scholar
  68. Rumbold CE, Ruíz-Barlett T, Gavio MA, Obenat SM (2016) Population dynamics of two invasive amphipods in the Southwestern Atlantic: Monocorophium acherusicum and Ericthonius punctatus (Crustacea). Mar Biol Res 12:268–277CrossRefGoogle Scholar
  69. Sánchez-Moyano JE, García-Asencio I (2010) Crustacean assemblages in a polluted estuary from South–Western Spain. Mar Pollut Bull 60:1890–1897CrossRefPubMedGoogle Scholar
  70. Sánchez-Moyano JE, García-Adiego EM, Estacio FJ, García–Gómez JC (2000) Effect of environmental factors on the spatial distribution of the epifauna of the alga Halopteris scoparia in Algeciras Bay, Southern Spain. Aquatic Ecol 34:355–367CrossRefGoogle Scholar
  71. Scelzo MA, Elias R, Vallarino EA, Lucero N (1996) Variación estacional de la fauna acompañante del mejillin (Brachydontes rodriguezi) en Mar del Plata, provincia de Buenos Aires, Argentina. Frente Marítimo 16:149–156Google Scholar
  72. Schram FR (1986) Crustacea. Oxford University Press, New YorkGoogle Scholar
  73. Schwindt E, Darrigan G, Repizo H (2010) Evaluación nacional de situación en materia del agua de lastre en el litoral marino y fluvial, Argentina - Informe Final. Proyecto Globallast. http://www.ambiente.gov.ar/archivos/web/GTRA/file/Aves%20marinas/Informe%20Final%20ENSMAL%20marino%20y%20fluvial.pdf. Accessed 27 November 2015Google Scholar
  74. Schwindt E, López-Gappa J, Raffo MP, Tatián M, Bortolus A, Orensanz JM, Alonso G, Diez ME, Doti B, Genzano G, Lagger C, Lovrich G, Piriz ML, Mendez MM, Savoya V, Sueiro MC (2014) Marine fouling invasions in ports of Patagonia (Argentina) with implications for legislation and monitoring programs. Mar Environ Res 99:60–68CrossRefPubMedGoogle Scholar
  75. Sepúlveda R, Cancino JM, Thiel M (2003) The peracarid epifauna associated with the ascidian Pyura chilensis (Molina, 1782) (Ascidiacea: Pyuridae). J Nat Hist 37:1555–1569CrossRefGoogle Scholar
  76. Shannon CE, Wiener W (1963) The mathematical theory of communications. University of Illinois, UrbanaGoogle Scholar
  77. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  78. Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486CrossRefPubMedGoogle Scholar
  79. Sueiro MC, Bortolus A, Schwindt E (2011) Habitat complexity and community composition: relationships between different ecosystem engineers and the associated macroinvertebrate assemblages. Helgoland Mar Res 65:467–477CrossRefGoogle Scholar
  80. Thiel M, Hinojosa I (2009) Peracarida - anfípodos, isópodos, tanaidáceos y cumáceos. In: Försterra G (ed) Häussermann V. Fauna marina bentónica de la patagonia chilena, Santiago de Chile, pp 671–738Google Scholar
  81. Thiel M, Watling L (2015) Lifestyles and Feeding Biology. Oxford University Press, New YorkGoogle Scholar
  82. Tsoi KH, Chiu KM, Chu KH (2005) Effects of temperature and salinity on survival and growth of the amphipod Hyale crassicornis (Gammaridea, Hyalidae). J Nat Hist 39:325–336CrossRefGoogle Scholar
  83. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  84. Valdivia N, Thiel M (2006) Effects of point-source nutrient addition and mussel removal on epibiotic assemblages in Perumytilus purpuratus beds. J Sea Res 56:271–283CrossRefGoogle Scholar
  85. Vallarino EA, Rivero MS, Gravina MC, Elías R (2002) The community–level response to sewage impact in intertidal mytilid beds of the Southwestern Atlantic and the use of the Shannon index to assess pollution. Rev Biol Mar Oceanogr 37:25–33CrossRefGoogle Scholar
  86. Wahl M (2009) Marine hard bottom communities, ecological studies Vol 206. Springer–Verlag, Berlin–HeidelbergGoogle Scholar
  87. Ward TJ, Hutchings PA (1996) Effects of trace metals on infaunal species composition in polluted intertidal and subtidal marine sediments near a lead smelter, Spencer Gulf, South Australia. Mar Ecol Prog Ser 135:123–135CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Carlos Rumbold
    • 1
  • Sandra Obenat
    • 1
  • Samira Nuñez Velazquez
    • 1
  • Brian Gancedo
    • 1
  • Eduardo Spivak
    • 1
  1. 1.Departamento de Biología e Instituto de Investigaciones Marinas y Costeras (IIMyC)Universidad Nacional de Mar del Plata y Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Mar del PlataArgentina

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