Influence of upwelling and tropical environments on the breeding development of the intertidal barnacle Tetraclita stalactifera (Lamarck, 1818)

Skinner, Luis Felipe; Macharet, Hariana Kelen Lisboa; Coutinho, Ricardo

Abstracts

Cabo Frio, with its unique oceanographic conditions, is an important biogeographical transitional region between tropical and sub-tropical waters. This is due to the presence of upwelling from the Central Water of the South Atlantic (CWSA), and the presence of tropical waters from the Brazilian Current (BC) and Coastal Water (CW). The intertidal barnacle, Tetraclita stalactifera, and its brooding stages were analyzed to correlate environmental conditions with reproductive development. Two thermal contrasting sites were chosen: Ponta da Cabeça (PC), which is under the influence of seasonal upwelling, and Ponta da Fortaleza (PF) which experiences tropical influences. At each site, T. stalactifera specimens were collected monthly and their egg lamellae conditions classified into stages from 0 (empty) to IV (ready to release). Our results show a seasonal effect on brooding at the PC site and a continuous development at the PF site. Nauplii larval availability also followed this trend. Differences between the sites could be due to ecological differences related to water temperature and the ecological-physiological response of the barnacles to these differences.

Reproductive cycle; Tetraclita stalactifera; Cabo Frio; Upwelling

Cabo Frio, devido suas características oceanográficas, causado pela é uma importante região biogeográfica transicional entre águas tropicais e sub-tropicais. Isto é ressurgência da Água Central do Atlântico Sul (ACAS) e a presença de águas tropicais da Corrente do Brasil (CB) e de Água Costeira (AC). A craca do mediolitoral Tetraclita stalactifera e seus estágios de maturação larval foram analisados a fim de serem correlacionados às condições ambientais. Dois locais com características termais contrastantes foram escolhidos: a Ponta da Cabeça (PC), que está sobre influência sazonal da ressurgência e a Ponta da Fortaleza (PF), sob influência da água tropical. Em cada local, indivíduos de T. stalactifera foram coletados mensalmente e a condição de suas lamellas ovígeras aferida e classificada desde o estágio 0 (vazio) até o IV (prestes a liberar). Nossos resultados amostram um efeito sazonal na PC, enquanto no local PF foi identificado um desenvolvimento contínuo. A disponibilidade de larvas náuplios também segue esta tendência. As diferenças observadas entre os locais podem ser explicadas pelas diferenças na temperatura da água e as respostas eco-fisiológicas exibidas por T. stalactifera na região.

Ciclo reprodutivo; Tetraclita stalactifera; Cabo Frio; Ressurgência

ALVES, S. L. S.; PEREIRA, A. D.; VENTURA, C.R.R. Sexual and asexual reproduction of Coscinasterias tenuispina (Echinodermata: Asteroidea) from Rio de Janeiro, Brazil. Mar. Biol., v. 140, p. 95-101, 2002.
BARNES, H. Processes of restoration and synchronization in marine ecology. The spring diatom increase and the spawning of the common barnacle Balanus balanoides (L.). Année biol., Paris, v. 33, p. 68-85, 1957.
BARNES, M. Mortality of intertidal cirripedes. Oceanogr. mar. Biol. A. Rev., v. 37, p. 153-244, 1999.
BEGON, M.; HARPER, J. L.; TOWSEND, C. R. Ecology: individuals, populations and communities Oxford: Blackwell Science, 1996.
BROCKINGTON, S.; CLARKE, A. The relative influence of temperature and food on the metabolism of a marine invertebrate. J. Exp. Mar. Biol. Ecol., v 258, p 87-99, 2001
CARBONEL, C. A. A. H.; VALENTIN, J. L. Numerical modelling of phytoplankton bloom in the upwelling ecosystem of Cabo Frio (Brazil). Ecol. Model., v.116, p. 135-148, 1999.
CARVALHO, A. L. P. S.; VENTURA, C. R. R. The reproductive cycle of Asterina stellifera (Möbius) (Echinodermata: Asteroidea) in the Cabo Frio region, southeastern Brazil. Mar. Biol., v. 141,p. 947-954, 2002.
CLARE, A. S. Chemical signals in barnacles: old problems, new approaches. In: SCHRAM, F.R.; HOEG, J.T. (Ed.). New frontiers in barnacle evolution. Rotterdam: A. A. Balkema, 1995. p. 49-67.
CRISP, D. J. A substance promoting hatching and liberation of young in cirripedes. Nature, v.178 ,p. 263, 1956.
CRISP, D. J.; RICHARDSON, C. A. Tidally-Produced Internal Bands in the Shell of Elminius modestus Mar. Biol., v. 33, p. 155-160, 1975.
DESAI, D. V.; · ANIL, A. C.; VENKAT, K. Reproduction in Balanus amphitrite Darwin (Cirripedia: Thoracica): influence of temperature and food concentration. Mar. Biol., v. 149, p. 1431-1441, 2006:
GUIMARAENS, M. A.; COUTINHO, R. Temporal and spatial variation of Ulva spp. and water properties in the Cabo Frio upwelling region of Brazil. Aquat. Bot., v.66, 101-114, 2000.
GONZALEZ-RODRIGUEZ, E.; VALENTIN, J. L.; ANDRÉ, D. L.; JACOB, S. A. Upwelling and downwelling at Cabo Frio (Brazil): Comparison of biomass and primary production responses. J. Plank. Res., v 14, p 289-306, 1992
HERBERT, R. J. H.; HAWKINS, S. ; SHEADER, M.; SOUTHWARD, A.J. Range extension and reproduction of the barnacle Balanus perforatus in the eastern English Channel. J. mar. biol. Ass. U. K., v. 83, p. 73-82, 2003.
HOEGH, G. O.; PEARSE, J. S. Temperature, food availability, and the development of marine invertebrate larvae. Am. Zool., v. 35, n.4, p. 415-425, 1995.
JUNQUEIRA, A. O. R.; VENTURA, C. R. R.; CARVALHO, A. L. P. S.; SCHIMDT, A. J. Population recovery of the sea urchin Lytechinus variegatus in a seagrass flat (Araruama Lagoon, Brazil): the role of recruitment in a disturbed environment. Invert. Reprod. Dev. , v. 31, n.1-3, p. 143-150, 1997.
LAWRENCE, A. J; SOAME, J. M. The effects of climate change on the reproduction of coastal invertebrates. Íbis, v.146, Suppl.1, p. 29-39, 2004.
LESLIE, H. M.; BRECK, E. N.; CHAN, F.; LUBCHENCO, J.; MENGE, B.A. Barnacle reproductive hotspots linked to nearshore ocean conditions. Proc. Natn. Acad. Sci. USA, v. 102, n.30, p.10534-10539, 2005.
MALUSA, J. R. Life history and environment in two species of intertidal barnacles. Biol. Bull., v.170, p 409-428, 1986
ROZAIMI, M. B. J.; O'RIORDAN, R. Reproduction of intertidal barnacles. Available from: http://www.ntu.edu.sg/eee/urop/congress2003/Proceedings/proceeds.html Accessed: 07/10/2010, 2003.
OLIVE, P. J. W. Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J. therm. Biol., v. 20, p. 79-90, 1995.
OLIVE, P. J. W.; LEWIS, C.; BEARDALL, V. Fitness components of seasonal reproduction: an analysis using Nereis virens as a life history model. Oceanologica Acta, v.23, n.4, p. 377-389, 2000.
O'RIORDAN, R. M.; MYERS, A. A.; CROSS, T. F. The reproductive cycles of Chthamalus stellatus (Poli) and C. montagui Southward in south-western Ireland. J. Exp. Mar. Biol. Ecol., v. 190, p. 17-38, 1995.
ORNELLAS, A. B.; COUTINHO, R. Spatial and temporal patterns of distribution and abundance of a tropical fish assemblage in a seasonal Sargassum bed, Cabo Frio Island, Brazil. J. Fish Biol., v. 53, Suppl. A , p.198-208, 1998.
PODOLSKY, R. D. Integrating development and environment to model reproductive performance in natural populations of an intertidal gastropod. Integr. Comp. Biol., v 43, n. 3, p 450-458, 2003
ROCHA, R. M.; COSTA, L. V. G. Ascidians (Urochordata: Ascidiacea) from Arraial do Cabo, Rio de Janeiro, Brazil. Iheringia, Sér. Zool., v. 95, n.1, 57-64, 2005.
ROCHA-BARREIRA, C. A. Gonad characterization and reproductive cycle of Collisella subrugosa (Orbigny, 1846) (Gastropoda: Acmaeidae) in the northeastern Braz. J. Biol., v. 62, p. 885-895, 2002.
SATHEESH, S; WESLEY, S. G. Breeding biology of the barnacle Amphibalanus amphitrite (Crustacea: Cirripedia): influence of environmental factors in a tropical coast. J. mar. biol. Ass. U. K, v.89, n.6, p.12031208, 2009.
SCHMIDT-NIELSEN, K. Fisiologia animal: adaptações e meio ambiente São Paulo: Ed. Santos, 2002.
SKINNER, L. F.; COUTINHO, R. Preliminary results on settlement of the barnacles Tetraclita stalactifera and Chthamalus bisinuatus on a Brazilian tropical rocky shore under upwelling conditions. Invert. Reprod. Dev., v.41, n. 1-3, p. 151-156, 2002.
SKINNER, L. F.; SIVIERO, F. N.; COUTINHO, R. Comparative growth of the intertidal barnacle Tetraclita stalactifera (Thoracica: Tetraclitidae) in sites influenced by upwelling and tropical conditions at the Cabo Frio region, Brazil. Rev. biol. trop. (International Journal of Tropical Biology and Conservation), v. 55, Suppl. 1, p.71-78, 2007.
VALENTIN, J. L.; ANDRÉ, D. L.; JACOB, S. A. Hydrobiology in the Cabo Frio (Brazil) upwelling: twodimensional structure and variability during a wind cycle. Continent. Shelf Res., v. 7, p. 77-88, 1987.
VALENTIN, J. L.; MONTEIRO-RIBAS W. M. Zooplankton community structure on the east-southeast Brazilian continental shelf (18-23ºS latitude). Continent. Shelf Res., v. 13, p. 407-424, 1993.
VENTURA, C. R. R.; FALCÃO, A. P. C.; SANTOS, J. S.; FIORI, C. S. Reproductive cycle and feeding periodicity in the starfish Astropecten brasiliensis in the Cabo Frio upwelling ecosystem (Brazil). Invert. Reprod. Dev., v. 31, n.1-3, p. 135-141, 1997.
WETHEY, D. S. Microclimate, competition, and biogeography: the barnacle Chthamalus fragilis in New England. Integr. Comp. Biol., v. 42, p.872-880, 2002.
WHITE, N. Semibalanus balanoides An acorn barnacle. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on-line]. Plymouth: Marine Biological Association of the United Kingdom. Available from: http://www.marlin.ac.uk/reproduction.php?speciesID=4328 Accessed: 07/10/2010, 2008
YAN, Y.; MIAO, S. The effect of temperature on the reproductive cycle of the tropical barnacle, Chthamalus malayensis Pilsbry (Cirripedia). Crustaceana, v. 77, n. 2, p. 205-212, 2004
YOUNG, P. S. Maxillopoda. Thecostraca In: YOUNG, P.S. (Ed.). Catalogue of Crustacea of Brazil. Rio de Janeiro: Museu Nacional, 1998. p. 263-285. (Série Livros, n. 6)

Publication Dates

Publication in this collection
03 Feb 2012
Date of issue
Dec 2011

History

Accepted
01 Sept 2011
Reviewed
05 June 2011
Received
15 Oct 2010

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] ALVES, S. L. S.; PEREIRA, A. D.; VENTURA, C.R.R. Sexual and asexual reproduction of Coscinasterias tenuispina (Echinodermata: Asteroidea) from Rio de Janeiro, Brazil. Mar. Biol., v. 140, p. 95-101, 2002.

[2] BARNES, H. Processes of restoration and synchronization in marine ecology. The spring diatom increase and the spawning of the common barnacle Balanus balanoides (L.). Année biol., Paris, v. 33, p. 68-85, 1957.

[3] BARNES, M. Mortality of intertidal cirripedes. Oceanogr. mar. Biol. A. Rev., v. 37, p. 153-244, 1999.

[4] BEGON, M.; HARPER, J. L.; TOWSEND, C. R. Ecology: individuals, populations and communities Oxford: Blackwell Science, 1996.

[5] BROCKINGTON, S.; CLARKE, A. The relative influence of temperature and food on the metabolism of a marine invertebrate. J. Exp. Mar. Biol. Ecol., v 258, p 87-99, 2001

[6] CARBONEL, C. A. A. H.; VALENTIN, J. L. Numerical modelling of phytoplankton bloom in the upwelling ecosystem of Cabo Frio (Brazil). Ecol. Model., v.116, p. 135-148, 1999.

[7] CARVALHO, A. L. P. S.; VENTURA, C. R. R. The reproductive cycle of Asterina stellifera (Möbius) (Echinodermata: Asteroidea) in the Cabo Frio region, southeastern Brazil. Mar. Biol., v. 141,p. 947-954, 2002.

[8] CLARE, A. S. Chemical signals in barnacles: old problems, new approaches. In: SCHRAM, F.R.; HOEG, J.T. (Ed.). New frontiers in barnacle evolution. Rotterdam: A. A. Balkema, 1995. p. 49-67.

[9] CRISP, D. J. A substance promoting hatching and liberation of young in cirripedes. Nature, v.178 ,p. 263, 1956.

[10] CRISP, D. J.; RICHARDSON, C. A. Tidally-Produced Internal Bands in the Shell of Elminius modestus Mar. Biol., v. 33, p. 155-160, 1975.

[11] DESAI, D. V.; · ANIL, A. C.; VENKAT, K. Reproduction in Balanus amphitrite Darwin (Cirripedia: Thoracica): influence of temperature and food concentration. Mar. Biol., v. 149, p. 1431-1441, 2006:

[12] GUIMARAENS, M. A.; COUTINHO, R. Temporal and spatial variation of Ulva spp. and water properties in the Cabo Frio upwelling region of Brazil. Aquat. Bot., v.66, 101-114, 2000.

[13] GONZALEZ-RODRIGUEZ, E.; VALENTIN, J. L.; ANDRÉ, D. L.; JACOB, S. A. Upwelling and downwelling at Cabo Frio (Brazil): Comparison of biomass and primary production responses. J. Plank. Res., v 14, p 289-306, 1992

[14] HERBERT, R. J. H.; HAWKINS, S. ; SHEADER, M.; SOUTHWARD, A.J. Range extension and reproduction of the barnacle Balanus perforatus in the eastern English Channel. J. mar. biol. Ass. U. K., v. 83, p. 73-82, 2003.

[15] HOEGH, G. O.; PEARSE, J. S. Temperature, food availability, and the development of marine invertebrate larvae. Am. Zool., v. 35, n.4, p. 415-425, 1995.

[16] JUNQUEIRA, A. O. R.; VENTURA, C. R. R.; CARVALHO, A. L. P. S.; SCHIMDT, A. J. Population recovery of the sea urchin Lytechinus variegatus in a seagrass flat (Araruama Lagoon, Brazil): the role of recruitment in a disturbed environment. Invert. Reprod. Dev. , v. 31, n.1-3, p. 143-150, 1997.

[17] LAWRENCE, A. J; SOAME, J. M. The effects of climate change on the reproduction of coastal invertebrates. Íbis, v.146, Suppl.1, p. 29-39, 2004.

[18] LESLIE, H. M.; BRECK, E. N.; CHAN, F.; LUBCHENCO, J.; MENGE, B.A. Barnacle reproductive hotspots linked to nearshore ocean conditions. Proc. Natn. Acad. Sci. USA, v. 102, n.30, p.10534-10539, 2005.

[19] MALUSA, J. R. Life history and environment in two species of intertidal barnacles. Biol. Bull., v.170, p 409-428, 1986

[20] ROZAIMI, M. B. J.; O'RIORDAN, R. Reproduction of intertidal barnacles. Available from: http://www.ntu.edu.sg/eee/urop/congress2003/Proceedings/proceeds.html Accessed: 07/10/2010, 2003.

[21] OLIVE, P. J. W. Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J. therm. Biol., v. 20, p. 79-90, 1995.

[22] OLIVE, P. J. W.; LEWIS, C.; BEARDALL, V. Fitness components of seasonal reproduction: an analysis using Nereis virens as a life history model. Oceanologica Acta, v.23, n.4, p. 377-389, 2000.

[23] O'RIORDAN, R. M.; MYERS, A. A.; CROSS, T. F. The reproductive cycles of Chthamalus stellatus (Poli) and C. montagui Southward in south-western Ireland. J. Exp. Mar. Biol. Ecol., v. 190, p. 17-38, 1995.

[24] ORNELLAS, A. B.; COUTINHO, R. Spatial and temporal patterns of distribution and abundance of a tropical fish assemblage in a seasonal Sargassum bed, Cabo Frio Island, Brazil. J. Fish Biol., v. 53, Suppl. A , p.198-208, 1998.

[25] PODOLSKY, R. D. Integrating development and environment to model reproductive performance in natural populations of an intertidal gastropod. Integr. Comp. Biol., v 43, n. 3, p 450-458, 2003

[26] ROCHA, R. M.; COSTA, L. V. G. Ascidians (Urochordata: Ascidiacea) from Arraial do Cabo, Rio de Janeiro, Brazil. Iheringia, Sér. Zool., v. 95, n.1, 57-64, 2005.

[27] ROCHA-BARREIRA, C. A. Gonad characterization and reproductive cycle of Collisella subrugosa (Orbigny, 1846) (Gastropoda: Acmaeidae) in the northeastern Braz. J. Biol., v. 62, p. 885-895, 2002.

[28] SATHEESH, S; WESLEY, S. G. Breeding biology of the barnacle Amphibalanus amphitrite (Crustacea: Cirripedia): influence of environmental factors in a tropical coast. J. mar. biol. Ass. U. K, v.89, n.6, p.12031208, 2009.

[29] SCHMIDT-NIELSEN, K. Fisiologia animal: adaptações e meio ambiente São Paulo: Ed. Santos, 2002.

[30] SKINNER, L. F.; COUTINHO, R. Preliminary results on settlement of the barnacles Tetraclita stalactifera and Chthamalus bisinuatus on a Brazilian tropical rocky shore under upwelling conditions. Invert. Reprod. Dev., v.41, n. 1-3, p. 151-156, 2002.

[31] SKINNER, L. F.; SIVIERO, F. N.; COUTINHO, R. Comparative growth of the intertidal barnacle Tetraclita stalactifera (Thoracica: Tetraclitidae) in sites influenced by upwelling and tropical conditions at the Cabo Frio region, Brazil. Rev. biol. trop. (International Journal of Tropical Biology and Conservation), v. 55, Suppl. 1, p.71-78, 2007.

[32] VALENTIN, J. L.; ANDRÉ, D. L.; JACOB, S. A. Hydrobiology in the Cabo Frio (Brazil) upwelling: twodimensional structure and variability during a wind cycle. Continent. Shelf Res., v. 7, p. 77-88, 1987.

[33] VALENTIN, J. L.; MONTEIRO-RIBAS W. M. Zooplankton community structure on the east-southeast Brazilian continental shelf (18-23ºS latitude). Continent. Shelf Res., v. 13, p. 407-424, 1993.

[34] VENTURA, C. R. R.; FALCÃO, A. P. C.; SANTOS, J. S.; FIORI, C. S. Reproductive cycle and feeding periodicity in the starfish Astropecten brasiliensis in the Cabo Frio upwelling ecosystem (Brazil). Invert. Reprod. Dev., v. 31, n.1-3, p. 135-141, 1997.

[35] WETHEY, D. S. Microclimate, competition, and biogeography: the barnacle Chthamalus fragilis in New England. Integr. Comp. Biol., v. 42, p.872-880, 2002.

[36] WHITE, N. Semibalanus balanoides An acorn barnacle. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on-line]. Plymouth: Marine Biological Association of the United Kingdom. Available from: http://www.marlin.ac.uk/reproduction.php?speciesID=4328 Accessed: 07/10/2010, 2008

[37] YAN, Y.; MIAO, S. The effect of temperature on the reproductive cycle of the tropical barnacle, Chthamalus malayensis Pilsbry (Cirripedia). Crustaceana, v. 77, n. 2, p. 205-212, 2004

[38] YOUNG, P. S. Maxillopoda. Thecostraca In: YOUNG, P.S. (Ed.). Catalogue of Crustacea of Brazil. Rio de Janeiro: Museu Nacional, 1998. p. 263-285. (Série Livros, n. 6)