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Marine Biology

, 165:140 | Cite as

Living under intertidal mussels: distribution, reproduction, and condition indices in a brooding sea star, Anasterias minuta, in Patagonia, Argentina

  • Damián G. Gil
  • María B. Reartes
  • Carolina Mutti
  • Javier A. Tolosano
  • Héctor E. Zaixso
Original paper

Abstract

Anasterias minuta is an abundant brooding sea star inhabiting tidepool habitats and mussel beds of Perumytilus purpuratus in Patagonia, Argentina. This study explores the influence of mussel bed complexity and tidal height on the size distribution of A. minuta living under mussel beds, and compares the abundance, reproduction, and condition indices in contrasting intertidal microhabitats (mussel hummocks and tidepools). Distribution patterns in mussel beds were explored at four sites along the coast of Argentina (45.4°S–47.4°S) during the austral spring, 2012/2017. Microhabitat comparisons were done at Caleta Cordova Norte between May 2004 and June 2005. Abundance inside mussel beds was correlated positively with mussel bed thickness and presence of mussel hummocks, and negatively with tidal height. Within mussel beds, early juveniles (recruits) and juveniles (greatest radius R < 15 mm) were generally restricted to low-tidal heights, while adults (R ≥ 15 mm) extended to mid-tidal levels. Sea stars were more abundant and larger in tidepools than under mussel beds. Numbers of recruits and juveniles increased significantly under mussel hummocks during austral spring and summer, coinciding with the release and subsequent growth of early juveniles. Brooding and gonadal cycles were synchronized between the microhabitats; however, the brooding cycle was nearly 2 months shorter under mussel hummocks (April–August) than in tidepools (April–October). The sea stars under mussels were smaller, had a less developed body wall, and greater gonadal production, indicating that more energy was allocated to reproduction compared to sea stars of similar size from tidepools. Further studies are needed to identify the specific environmental conditions that led to the observed adaptations and to understand the underlying physiological mechanisms.

Notes

Acknowledgements

We thank Alicia Boraso, Martin Varisco, Val Gerard, and two anonymous reviewers for insightful comments.

Funding

This study was partially supported by Universidad Nacional de la Patagonia San Juan Bosco. Project UNPSJB 955 (RN°127/2012).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2018_3397_MOESM1_ESM.pdf (40 kb)
Supplementary material 1 (PDF 40 kb)

References

  1. Agresti A (2015) Foundations of linear and generalized linear models. Wiley, New YorkGoogle Scholar
  2. Alvarado JL, Castilla JC (1996) Tridimensional matrices of mussels Perumytilus purpuratus on intertidal platforms with varying wave forces in central Chile. Mar Ecol Prog Ser 133:135–141.  https://doi.org/10.3354/meps133135 CrossRefGoogle Scholar
  3. Baker P, Mann R (1997) The postlarval phase of bivalve mollusks: a review of functional ecology and new records of postlarval drifting of Chesapeake Bay bivalves. Bull Mar Sci 61:409–430Google Scholar
  4. Barahona M, Navarrete SA (2010) Movement patterns of the seastar Heliaster helianthus in central Chile: relationship with environmental conditions and prey availability. Mar Biol 157:647–661.  https://doi.org/10.1007/s00227-009-1350-7 CrossRefGoogle Scholar
  5. Bernasconi I (1964) Distribución geográfica de los equinoideos y asteroideos de la extremidad austral de Sudamérica. Bol Inst Biol Mar 7:43–50Google Scholar
  6. Bertness MD, Gaines SD, Yeh SM (1998) Making mountains out of barnacles: the dynamics of acorn barnacle hummocking. Ecology 79:1382–1394.  https://doi.org/10.1890/0012-9658(1998)079%5B1382:MMOOBT%5D2.0.CO;2 CrossRefGoogle Scholar
  7. Bertness MD, Crain CM, Silliman BR, Bazterrica MC, Reyna M, Hildago F, Farina J (2006) The community structure of western Atlantic Patagonian rocky shores. Ecol Monogr 76:439–460.  https://doi.org/10.1890/0012-9615(2006)076%5B0439:TCSOWA%5D2.0.CO;2 CrossRefGoogle Scholar
  8. Blankley WO, Grindley JR (1985) The intertidal and shallow subtidal food web at Marion Island. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 630–636CrossRefGoogle Scholar
  9. Briones C, Guiñez R (2005) Asimetría bilateral de la forma de las valvas y posición espacial en matrices del chorito Perumytilus purpuratus (Lamarck, 1819) (Bivalvia: Mytilidae). Rev Chil Hist Nat 78:3–14.  https://doi.org/10.4067/S0716-078X2005000100001 CrossRefGoogle Scholar
  10. Brogger MI, Gil DG, Rubilar T, Martinez MI, Díaz de Vivar ME, Escolar M, Epherra L, Pérez AF, Tablado A (2013) Echinoderms from Argentina: Biodiversity, distribution and current state of knowledge. In: Alvarado JJ, Solís-Marín FA (eds) Echinoderm research and diversity in Latin America. Springer, Berlin, pp 359–402CrossRefGoogle Scholar
  11. Burnaford JL (2004) Habitat modification and refuge from sublethal stress drive a marine plant–herbivore association. Ecology 85:2837–2849.  https://doi.org/10.1890/03-0113 CrossRefGoogle Scholar
  12. Buschbaum C, Dittmann S, Hong JS, Hwang IS, Strasser M, Thiel M, Valdivia N, Yoon S, Reise K (2009) Mytilid mussels: global habitat engineers in coastal sediments. Helgol Mar Res 63:47–58.  https://doi.org/10.1007/s10152-008-0139-2 CrossRefGoogle Scholar
  13. Byrne M (1995) Changes in larval morphology in the evolution of benthic development by Patiriella exigua (Asteroidea: Asterinidae), a comparison with the larvae of Patiriella species with planktonic development. Biol Bull 188:293–305CrossRefPubMedGoogle Scholar
  14. Castilla JC, Luxoro C, Navarrete SA (1989) Galleries of the crabs Acanthocyclus under intertidal mussel beds: their effects on the use of primary substratum. Rev Chil Hist Nat 62:199–204Google Scholar
  15. Chen BY, Chen CP (1992) Reproductive cycle, larval development, juvenile growth and population dynamics of Patiriella pseudoexigua (Echinodermata: Asteroidea) in Taiwan. Mar Biol 113:271–280.  https://doi.org/10.1007/BF00347281 CrossRefGoogle Scholar
  16. Chia FS, Walker CW (1991) Echinodermata: Asteroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, vol VI. Echinoderms and lophophorates. Boxwood Press, California, pp 301–353Google Scholar
  17. Clark AM, Downey ME (1992) Starfishes of the Atlantic. Chapman & Hall, LondonGoogle Scholar
  18. Cossi PF, Boy CC, Giménez J, Pérez AF (2015) Reproductive biology and energy allocation of the sea star Cosmasterias lurida (Echinodermata: Asteroidea) from the Beagle Channel, Tierra del Fuego, Argentina. Polar Biol 38:1321–1333CrossRefGoogle Scholar
  19. Dahlhoff EP, Buckley BA, Menge BA (2001) Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient. Ecology 82:2816–2829.  https://doi.org/10.1890/0012-9658(2001)082%5B2816:POTRIP%5D2.0.CO;2 CrossRefGoogle Scholar
  20. Davenport J, Moore PG, LeComte E (1996) Observations on defensive interactions between predatory dogwhelks, Nucella lapillus (L.) and mussels, Mytilus edulis L. J Exp Mar Biol Ecol 206:133–147.  https://doi.org/10.1016/S0022-0981(96)02628-7 CrossRefGoogle Scholar
  21. Davenport J, Moore PG, Magill SH, Fraser LA (1998) Enhanced condition in dogwhelks, Nucella lapillus (L.) living under mussel hummocks. J Exp Mar Biol Ecol 230:225–234.  https://doi.org/10.1016/S0022-0981(98)00082-3 CrossRefGoogle Scholar
  22. Dolmer P (1998) The interactions between bed structure of Mytilus edulis L. and the predator Asterias rubens L. J Exp Mar Biol Ecol 228:137–150.  https://doi.org/10.1016/S0022-0981(98)00024-0 CrossRefGoogle Scholar
  23. Duarte C, Jaramillo E, Contreras H, Figueroa L (2006) Community structure of the macroinfauna in the sediments below an intertidal mussel bed (Mytilus chilensis (Hupe)) of southern Chile. Rev Chil Hist Nat 79:353–368CrossRefGoogle Scholar
  24. Feder HM, Christensen AM (1966) Aspects of asteroid biology. In: Boolootian RA (ed) Physiology of echinodermata. Interscience, New York, pp 87–127Google Scholar
  25. Firstater FN, Hidalgo FJ, Lomovasky BJ, Ramos E, Gamero P, Iribarne OO (2011) Habitat structure is more important than nutrient supply in modifying mussel bed assemblage in an upwelling area of the Peruvian coast. Helgol Mar Res 65:187–196.  https://doi.org/10.1007/s10152-010-0214-3 CrossRefGoogle Scholar
  26. Fly EK, Monaco CJ, Pincebourde S, Tullis A (2012) The influence of intertidal location and temperature on the metabolic cost of emersion in Pisaster ochraceus. J Exp Mar Biol Ecol 422:20–28.  https://doi.org/10.1016/j.jembe.2012.04.007 CrossRefGoogle Scholar
  27. Fréchette M, Butman CA, Geyer WR (1989) The importance of boundary-layer flows in supplying phytoplankton to the benthic suspension feeder, Mytilus edulis L. Limnol Oceanogr 34:19–36.  https://doi.org/10.4319/lo.1989.34.1.0019 CrossRefGoogle Scholar
  28. Gaymer CF, Himmelman JH, Johnson LE (2001) Distribution and feeding ecology of the seastars Leptasterias polaris and Asterias vulgaris in the northern Gulf of St. Lawrence, Canada. J Mar Biol Assoc UK 81:827–843.  https://doi.org/10.1017/S0025315401004660 CrossRefGoogle Scholar
  29. Gemmill JF (1912) I. The development of the starfish Solaster endeca Forbes. Trans Zool Soc Lond 20:1–71.  https://doi.org/10.1111/j.1469-7998.1912.tb07829.x CrossRefGoogle Scholar
  30. George SB (1994) Population differences in maternal size and offspring quality for Leptasterias epichlora (Brandt) (Echinodermata: Asteroidea). J Exp Mar Biol Ecol 175:121–131.  https://doi.org/10.1016/0022-0981(94)90179-1 CrossRefGoogle Scholar
  31. Gil DG, Zaixso HE (2007) The relation between feeding and reproduction in Anasterias minuta (Asteroidea: Forcipulata). Mar Biol Res 3:256–264.  https://doi.org/10.1080/17451000701472035 CrossRefGoogle Scholar
  32. Gil DG, Zaixso HE (2008) Feeding ecology of the subantarctic sea star Anasterias minuta within tide pools in Patagonia, Argentina. Rev Biol Trop 56:311–328Google Scholar
  33. Gil DG, Escudero G, Zaixso HE (2011) Brooding and development of Anasterias minuta (Asteroidea: Forcipulata) in Patagonia, Argentina. Mar Biol 158:2589–2602.  https://doi.org/10.1007/s00227-011-1760-1 CrossRefGoogle Scholar
  34. Guiñez R, Castilla JC (1999) A tridimensional self-thinning model for multilayered intertidal mussels. Am Nat 154:341–357PubMedGoogle Scholar
  35. Gutiérrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90.  https://doi.org/10.1034/j.1600-0706.2003.12322.x CrossRefGoogle Scholar
  36. Gutiérrez JL, Palomo MG, Bagur M, Arribas LP, Soria SA (2015) Wave action limits crowding in an intertidal mussel. Mar Ecol Prog Ser 518:153–163.  https://doi.org/10.3354/meps11086 CrossRefGoogle Scholar
  37. Harger JRE, Landenberger DE (1971) The effect of storms as a density dependent mortality factor on populations of sea mussels. Veliger 14:195–201Google Scholar
  38. Harrold C, Pearse JS (1980) Allocation of pyloric caecum reserves in fed and starved sea stars, Pisaster giganteus (Stimpson): somatic maintenance comes before reproduction. J Exp Mar Biol Ecol 48:169–183.  https://doi.org/10.1016/0022-0981(80)90015-5 CrossRefGoogle Scholar
  39. Hendler G, Franz DR (1982) The biology of a brooding seastar, Leptasterias tenera, in Block Island Sound. Biol Bull 162:273–289CrossRefGoogle Scholar
  40. Hernández DA, Tablado A (1985) Asteroidea de Puerto Deseado (Santa Cruz, Argentina). Contribución CENPAT N°104, ArgentinaGoogle Scholar
  41. Hidalgo FJ, Silliman BR, Bazterrica MC, Bertness MD (2007) Predation on the rocky shores of Patagonia, Argentina. Estuar Coast 30:886–894.  https://doi.org/10.1007/BF02841342 CrossRefGoogle Scholar
  42. Hosmer DW, Lemeshow S (2000) Interpretation of the fitted logistic regression model. In: Hosmer DW, Lemeshow S (eds) Applied logistic regression. Wiley, New York, pp 47–90CrossRefGoogle Scholar
  43. Joly-Turquin G, Dubois P, Leyzour S, Pernet P, De Ridder F, Pintelon R, Guillou M (2013) Contrasting relationships between pyloric caecum and gonad growth in the starfish Asterias rubens: combined field and experimental approaches. J Mar Biol Assoc UK 93:1073–1086CrossRefGoogle Scholar
  44. Labraga JC (1994) Extreme winds in the Pampa del Castillo Plateau, Patagonia, Argentina, with reference to wind farm settlement. J Appl Meteorol 33:85–95CrossRefGoogle Scholar
  45. Lane DJW, Beaumont AR, Hunter JR (1985) Byssus drifting and the drifting threads of the young post-larval mussel Mytilus edulis. Mar Biol 84:301–308.  https://doi.org/10.1007/BF00392500 CrossRefGoogle Scholar
  46. Lawrence JM, Herrera J (2000) Stress and deviant reproduction in echinoderms. Zool Stud 39:151–171Google Scholar
  47. Lawrie SM, McQuaid CD (2001) Scales of mussel bed complexity: structure, associated biota and recruitment. J Exp Mar Biol Ecol 257:135–161.  https://doi.org/10.1016/S0022-0981(00)00290-2 CrossRefPubMedGoogle Scholar
  48. Le Corre N, Martel AL, Guichard F, Johnson LE (2013) Variation in recruitment: differentiating the roles of primary and secondary settlement of blue mussels Mytilus spp. Mar Ecol Prog Ser 481:133–146.  https://doi.org/10.3354/meps10216 CrossRefGoogle Scholar
  49. Legendre P, Legendre LF (2012) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  50. Lohrer AM, Fukui Y, Wada K, Whitlatch RB (2000) Structural complexity and vertical zonation of intertidal crabs, with focus on habitat requirements of the invasive Asian shore crab, Hemigrapsus sanguineus (de Haan). J Exp Mar Biol Ecol 244:203–217CrossRefGoogle Scholar
  51. López DA, López BA, Burgos IC, Arriagada SE, González ML (2007) Consequences of base modification in hummocks of the barnacle Austromegabalanus psittacus. N Z J Mar Freshw Res 41:291–298.  https://doi.org/10.1080/00288330709509916 CrossRefGoogle Scholar
  52. Mauzey KP (1966) Feeding behavior and reproductive cycles in Pisaster ochraceus. Biol Bul 131:127–144CrossRefGoogle Scholar
  53. McArdle BH, Anderson MJ (2004) Variance heterogeneity, transformations, and models of species abundance: a cautionary tale. Can J Fish Aquat Sci 61:1294–1302.  https://doi.org/10.1139/f04-051 CrossRefGoogle Scholar
  54. Menge BA (1970) The population ecology and community role of the predaceous asteroid, Leptasterias hexactis (Stimpson). Ph.D. dissertation, University of WashingtonGoogle Scholar
  55. Menge BA (1972) Foraging strategy of a starfish in relation to actual prey availability and environmental predictability. Ecol Monogr 42:25–50CrossRefGoogle Scholar
  56. Menge BA, Olson AM, Dahlhoff EP (2002) Environmental stress, bottom-up effects, and community dynamics: integrating molecular-physiological and ecological approaches. Integr Comp Biol 42:892–908.  https://doi.org/10.1093/icb/42.4.892 CrossRefPubMedGoogle Scholar
  57. Nakamura Y (2015) Mucous-cord secretion for drifting by the clam Meretrix lusoria (Veneridae) under varying light/dark and submergence/exposure conditions. Plankton Benthos Res 10:18–25.  https://doi.org/10.3800/pbr.10.18 CrossRefGoogle Scholar
  58. Navarrete SA, Castilla JC (1990) Resource partitioning between intertidal predatory crabs: interference and refuge utilization. J Exp Mar Biol Ecol 143:101–129.  https://doi.org/10.1016/0022-0981(90)90114-R CrossRefGoogle Scholar
  59. Nicastro KR, Zardi GI, McQuaid CD (2007) Behavioural response of invasive (Mytilus galloprovincialis) and indigenous (Perna perna) mussels exposed to risk of predation. Mar Ecol Prog Ser 336:69–175CrossRefGoogle Scholar
  60. Nicastro KR, Zardi GI, McQuaid CD, Pearson GA, Serrão EA (2012) Love thy neighbour: group properties of gaping behaviour in mussel aggregations. PLoS ONE 7(10):e47382CrossRefPubMedPubMedCentralGoogle Scholar
  61. Nielsen TM (1973) Population and reproductive biology of the six-rayed sea star Leptasterias hexactis on the protected outer coast. Ph.D. dissertation, University of OregonGoogle Scholar
  62. O’Donnell MF (2008) Reduction of wave forces within bare patches in mussel beds. Mar Ecol Prog Ser 362:157–167.  https://doi.org/10.3354/meps07435 CrossRefGoogle Scholar
  63. Olsson AA (1961) Mollusks of the tropical eastern Pacific, Panamic Pacific Pelecypoda. Paleontological Research Institute, IthacaGoogle Scholar
  64. Paine RT (1976) Size-limited predation: an observational and experimental approach with the MytilusPisaster interaction. Ecology 57:858–873CrossRefGoogle Scholar
  65. Paine RT, Levin SA (1981) Intertidal landscapes: disturbance and the dynamics of pattern. Ecol Monogr 51:145–178.  https://doi.org/10.2307/2937261 CrossRefGoogle Scholar
  66. Perales SG, Boraso AL (2006) Relación de Blidingia minima (Ulvales, Chlorophyta) con factores ambientales en Punta Maqueda (golfo San Jorge, Argentina). Rev Biol Mar Oceanogr 41:21–33CrossRefGoogle Scholar
  67. Pérez AF, Boy CC, Calcagno J, Malanga G (2015) Reproduction and oxidative metabolism in the brooding sea star Anasterias antarctica (Lütken, 1957). J Exp Mar Biol Ecol 463:150–157CrossRefGoogle Scholar
  68. Petes LE, Menge BA, Murphy GD (2007) Environmental stress decreases survival, growth, and reproduction in New Zealand mussels. J Exp Mar Biol Ecol 351:83–91.  https://doi.org/10.1016/j.jembe.2007.06.025 CrossRefGoogle Scholar
  69. Petes LE, Mouchka ME, Milston-Clements RH, Momoda TS, Menge BA (2008) Effects of environmental stress on intertidal mussels and their sea star predators. Oecologia 156:671–680.  https://doi.org/10.1007/s00442-008-1018-x CrossRefPubMedGoogle Scholar
  70. Pincebourde S, Sanford E, Helmuth B (2008) Body temperature during low tide alters the feeding performance of a top intertidal predator. Limnol Oceanogr 53:1562–1573.  https://doi.org/10.4319/lo.2008.53.4.1562 CrossRefGoogle Scholar
  71. Porri F, Zardi GI, McQuaid CD, Radloff S (2007) Tidal height, rather than habitat selection for conspecifics, controls settlement in mussels. Mar Biol 152:631–637.  https://doi.org/10.1007/s00227-007-0716-y CrossRefGoogle Scholar
  72. Prado L, Castilla JC (2006) The bioengineer Perumytilus purpuratus (Mollusca: Bivalvia) in central Chile: biodiversity, habitat structural complexity and environmental heterogeneity. J Mar Biol Assoc UK 86:417–421.  https://doi.org/10.1017/S0025315406013282 CrossRefGoogle Scholar
  73. Raymond JF, Himmelman JH, Guderley HE (2004) Sex differences in biochemical composition, energy content and allocation to reproductive effort in the brooding sea star Leptasterias polaris. Mar Ecol Prog Ser 283:179–190.  https://doi.org/10.3354/meps283179 CrossRefGoogle Scholar
  74. Roediger LM, Bolton TF (2008) Abundance and distribution of South Australia’s endemic sea star, Parvulastra parvivipara (Asteroidea: Asterinidae). Mar Freshw Res 59:205–213.  https://doi.org/10.1071/MF07084 CrossRefGoogle Scholar
  75. Saier B (2001) Direct and indirect effects of seastars Asterias rubens on mussel beds (Mytilus edulis) in the Wadden Sea. J Sea Res 46:29–42.  https://doi.org/10.1016/S1385-1101(01)00067-3 CrossRefGoogle Scholar
  76. Salvat MB (1985) Biología de la reproducción de Anasterias minuta Perrier (Echinodermata, Asteroidea), especie incubadora de las costas patagónicas. Ph.D. dissertation, Universidad de Buenos AiresGoogle Scholar
  77. Seed R (1996) Patterns of biodiversity in the macro-invertebrate fauna associated with mussel patches on rocky shores. J Mar Biol Assoc UK 76:203–210.  https://doi.org/10.1017/S0025315400029131 CrossRefGoogle Scholar
  78. Silliman BR, Bertness MD, Altieri AH, Griffin JN, Bazterrica MC, Hidalgo FJ, Crain CM, Reyna MV (2011) Whole-community facilitation regulates biodiversity on Patagonian rocky shores. PLoS ONE 6:e24502CrossRefPubMedPubMedCentralGoogle Scholar
  79. Sloan NA (1980) Aspects of the feeding biology of asteroids. Oceanogr Mar Biol Annu Rev 18:57–124Google Scholar
  80. Šmilauer P, Lepš J (2014) Multivariate analysis of ecological data using CANOCO 5. Cambridge University Press, LondonCrossRefGoogle Scholar
  81. Smith JR, Fong P, Ambrose RF (2006) Dramatic declines in mussel bed community diversity: response to climate change? Ecology 87:1153–1161.  https://doi.org/10.1890/0012-9658(2006)87[1153:DDIMBC]2.0.CO;2 CrossRefPubMedGoogle Scholar
  82. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman and Co, New YorkGoogle Scholar
  83. Soliman ES, Nojima S (1984) Some observations on dispersal behavior of the early juvenile of the sea-star, Asterina minor. Publ Amakusa Mar Biol Lab 7:81–93Google Scholar
  84. Stephens EG, Bertness MD (1991) Mussel facilitation of barnacle survival in a sheltered bay habitat. J Exp Mar Biol Ecol 145:33–48.  https://doi.org/10.1016/0022-0981(91)90004-G CrossRefGoogle Scholar
  85. Suchanek TH (1985) Mussels and their role in structuring rocky shore communities. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Hodder and Stoughton, London, pp 70–96Google Scholar
  86. ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 45). Microcomputer Power, New YorkGoogle Scholar
  87. Thiel M, Ullrich N (2002) Hard rock versus soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile, and considerations on the functional role of mussel beds. Helgol Mar Res 56:21–30.  https://doi.org/10.1007/s10152-001-0098-3 CrossRefGoogle Scholar
  88. Tokeshi M (1995) Polychaete abundance and dispersion patterns in mussel beds: a non-trivial infaunal assemblage on a Pacific South American rocky shore. Mar Ecol Prog Ser 125:137–147.  https://doi.org/10.3354/meps125137 CrossRefGoogle Scholar
  89. Tokeshi M, Romero L (1995) Quantitative analysis of foraging behaviour in a field population of the South American sun-star Heliaster helianthus. Mar Biol 122:297–303.  https://doi.org/10.1007/BF00348943 CrossRefGoogle Scholar
  90. Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936PubMedGoogle Scholar
  91. Town JC (1980) Diet and food preference of intertidal Astrostole scabra (Asteroidea: Forcipulata). N Zl J Mar Fresh 14:427–435.  https://doi.org/10.1080/00288330.1980.9515887 CrossRefGoogle Scholar
  92. Tsuchiya M, Nishihira M (1985) Islands of Mytilus as a habitat for small intertidal animals: effect of island size on community structure. Mar Ecol Prog Ser 25:71–81.  https://doi.org/10.3354/meps025071 CrossRefGoogle Scholar
  93. White GC, Bennetts RE (1996) Analysis of frequency count data using the negative binomial distribution. Ecology 77:2549–2557.  https://doi.org/10.2307/2265753 CrossRefGoogle Scholar
  94. Wieters EA, Salles E, Januario SM, Navarrete SA (2009) Refuge utilization and preferences between competing intertidal crab species. J Exp Mar Biol Ecol 374:37–44.  https://doi.org/10.1016/j.jembe.2009.04.006 CrossRefGoogle Scholar
  95. Zaixso HE, Boraso de Zaixso AL, López Gappa JJ (1978) Observaciones sobre el mesolitoral rocoso de la zona de Ushuaia (Tierra del Fuego, Argentina). Ecosur 5:119–130Google Scholar
  96. Zaixso HE, Stoyanoff P, Gil DG (2009) Detrimental effects of the isopod, Edotia doellojuradoi, on gill morphology and host condition of the mussel, Mytilus edulis platensis. Mar Biol 156:2369–2378.  https://doi.org/10.1007/s00227-009-1265-3 CrossRefGoogle Scholar
  97. Zaixso HE, Boraso de Zaixso AL, Pastor de Ward CT, Lizarralde ZI, Dadón J, Galvan D (2015) El bentos costero patagónico. La zona costera patagónica Argentina. EDUPA, Comodoro RivadaviaGoogle Scholar
  98. Zardi GI, Nicastro K, McQuaid CD, Rius M, Porri F (2006) Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy. Mar Biol 150:79–88.  https://doi.org/10.1007/s00227-006-0328-y CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Desarrollo Costero (IDC)Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB)Comodoro RivadaviaArgentina
  2. 2.Facultad de Ciencias Naturales y Ciencias de la Salud, Departamento de Biología y AmbienteUNPSJBComodoro RivadaviaArgentina
  3. 3.Institut des sciences de la mer de RimouskiUniversité du Québec à RimouskiRimouskiCanada

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