Marine Biology

, Volume 148, Issue 3, pp 467–478 | Cite as

Phenotypic plasticity in a mutualistic association between the sponge Haliclona caerulea and the calcareous macroalga Jania adherens induced by transplanting experiments. I: morphological responses of the sponge

  • José Luis CarballoEmail author
  • Enrique Ávila
  • Susana Enríquez
  • Leonardo Camacho
Research Article


The mutualistic association between the sponge Haliclona caerulea and the calcareous red macroalga Jania adherens is conspicuous on shallow rocky regions of Mazatlán Bay (eastern tropical Pacific, Mexico). Transplanting experiments were carried out to examine the morphological responses of the association to an environmental depth gradient. Simultaneously, we conducted caging experiments to examine the effects of predation (mainly by angelfishes) on association morphology. For this, we transplanted specimens of the association from a control area at 3 m depth to depths of 1 and 5 m, and measured the morphological responses in the association (macro- and microstructure) from the three sites before and after 103 days. The association had the capacity to adjust both macro and micromorphologically, and both external morphology and body structure changed significantly with depth. The specimens grown at 1 m developed a larger surface area of attachment, higher organic density and higher inorganic content than the control specimens at 3 m, and the organisms grown at 5 m depth. We also detected significant differences in the aquiferous system of the sponge, which developed smaller and more numerous oscula at 1 m than at 5 m depth. These differences seem to be consistent with the wave movement as one of the main regulatory factors of the morphology of the association. However, the spicules from H. caerulea were most slender in shallow water, which is not consistent with increasing robustness in the face of greater wave force. The algal skeleton supplied up to 27% of the total inorganic structure of the association; thus, algal contribution significantly reduces the energy costs of spicule production, specifically under high wave exposure, when H. caerulea requires structural reinforcement relative to organic content. The contribution of the sponge to the association (as ratio Si to CaCO3) increased significantly from 3 to 5 m (12% in the uncaged specimens and 22% in the caged specimens), showing that the mutualistic relationship decreases with depth. The production of sponge branches in caged individuals was the most notable difference from uncaged morphs, which could suggest the effect of predators like angelfishes. However, branches could also be a response to the reduction in water movement and irradiance inside the cages. Sponges are known to show morphological acclimation in response to habitat variation, but this is the first study to show it in a sponge living in association with a macroalga.


Sponge Uncaged Specimen Inorganic Content Uncaged Individual Plaster Sphere 
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The study has been funded in part by the project "Ecología de la asociación entre la esponja Haliclona Caerulea y el alga roja Jania adherens”, (IX232004), funded by the PAPIIT (Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, DGAPA). We thank the support of Postgrado de Ciencias del Mar y Limnología (UNAM), the support in funding the exchange of EA and SE. We also thank JM Geraldía (Servicio Central de Ciencia y Tecnología) of Universidad de Cádiz (Spain) for his help with the SEM photographs, C Ramírez Jáuregui, P. Allende and V. Montes (ICML–UNAM) for generous help with the literature and aerial images, G. Ramirez Reséndiz and C. Suarez (ICML-UNAM) for their computer assistance, and staff members at the ICML-UNAM (Mazatlán), C Vega Juarez, P Pérez and J Toto Fiscal, for their help in the sampling.


  1. Ávila E (2002) Dinámica poblacional de la asociación Haliclona caerulea (Hechtel, 1965) (Demospongiae, Haplosclerida) y algas rojas en la bahía de Mazatlán (México, Pacífico Oriental). MS dissertation, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, p 76Google Scholar
  2. Ávila E, Carballo JL (2004) Growth and standing stock biomass of a mutualistic association between the sponge Haliclona caerulea and the red alga Jania adherens. Symbiosis 36(3):225–244Google Scholar
  3. Barthel D (1989) Growth of the sponge Halichondria panicea in the North Sea habitat. Polish Academy of Sciences, Institute of Oceanology, pp 23–30Google Scholar
  4. Bell JJ (2002) Regeneration rates of a temperate demosponge: the importance of water flow rate. J Mar Biol Assoc UK 82:169–170CrossRefGoogle Scholar
  5. Bell JJ, Barnes DKA (2000) The influences of bathymetry and flow regime upon the morphology of sublittoral sponge communities. J Mar Biol Assoc UK 80:707–718CrossRefGoogle Scholar
  6. Bell JJ, Barnes DKA, Turner JR (2002) The importance of micro and macro morphological variation in the adaptation of a sublittoral demosponge to current extremes. Mar Biol 140:75–81CrossRefGoogle Scholar
  7. Camacho-Cruz ML (2004) Estudio preliminar de la composición faunística de depredadores de esponjas en la bahía de Mazatlán (Sinaloa). Bs dissertation, Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa, p 53Google Scholar
  8. Carballo JL (1994) Taxonomía, zoogeografía y autoecología de los Poríferos del Estrecho de Gibraltar. PhD dissertation, Facultad de Biología, Universidad de Sevilla, p 334Google Scholar
  9. Carballo JL, Ávila E (2004) Population dynamics of a mutualistic interaction between the sponge Haliclona caerulea, and the red alga Jania adherens. Mar Ecol Prog Ser 279:93–104CrossRefGoogle Scholar
  10. Carballo JL, Naranjo SA, García Gómez JC (1996) The use of marine sponges as stress indicators in marine ecosystems at Algeciras Bay (Southern Iberian Peninsula). Mar Ecol Prog Ser 135:109–122CrossRefGoogle Scholar
  11. Davy SK, Trautman DA, Borowitzka MA, Hinde R (2002) Ammonium excretion by a symbiotic sponge supplies the nitrogen requirements of its rhodophyte partner. J Exp Biol 205:3505–3511PubMedGoogle Scholar
  12. Ellison AM, Farnsworth EJ, Twilley RR (1996) Facultative mutualism between red mangroves and root-fouling sponges in belizean mangle. Ecology 77(8):2431–2444CrossRefGoogle Scholar
  13. Enríquez S, Ávila E, Carballo JL (2005) Phenotypic plasticity induced in transplanting experiments with a mutualistic association between the sponge Haliclona caerulea and the red macroalgae Jania adherens II Morphological responses of the algae. Oecologia (submitted)Google Scholar
  14. Gambi MC, Buia MC, Casola E, Scardi M (1989) Estimates of water movement in Posidonia oceanica beds: a first approach. In: Boudouresque CF, Meinesz A, Fresi E, Gravez V (eds) International Workshop of Posidonia Beds, France 2:101–112Google Scholar
  15. Hill MS (1999) Morphological and genetic examination of phenotypic variability in the tropical sponge Anthosigmella varians. Mem Qld Mus 44:239–247Google Scholar
  16. Hill MS, Hill AL (2002) Morphological plasticity in the tropical sponge Anthosigmella varians: responses to predators and wave energy. Biol Bull 202:86–95CrossRefGoogle Scholar
  17. Kaandorp JA (1999) Morphological analysis of growth forms of branching marine sessile organisms along environmental gradients. Mar Biol 134:295–306CrossRefGoogle Scholar
  18. Kaandorp JA, Sloot PMA, Merks RMH, Bak RPM, Vermeij MJA (2005) Morphogenesis of the branching reef coral Madracis mirabilis. Proc R Soc B 272:127–133CrossRefGoogle Scholar
  19. Koehl MAR (1982) Mechanical design of spicule-reinforced connective tissue: stiffness. J Exp Biol 98:239–267Google Scholar
  20. Lewis JR (1968) Water movement and their role in rocky shore ecology. Sarsia 34:13–36CrossRefGoogle Scholar
  21. Maldonado M, Young CM (1996) Effects of physical factors on larval behavior, settlement and recruitment of four tropical demosponges. Mar Ecol Prog Ser 138:169–180CrossRefGoogle Scholar
  22. McDonald JI, Hooper JNA, McGuinness KA (2002) Environmentally influenced variability in the morphology of Cinachyrella australiensis (Carter 1886) (Porifera: Spirophorida: Tetillidae). Mar Fresh Res 53:79–84CrossRefGoogle Scholar
  23. Meroz E, Ilan M (1995) Cohabitation of a coral reef sponge and a colonial scyphozoan. Mar Biol 124:453–459CrossRefGoogle Scholar
  24. Meroz E, Brickner I, Loya Y, Peretzman-Shemer A, Micha I (2001) The effect of gravity on coral morphology. Proc R Soc Lond B 269:717–720CrossRefGoogle Scholar
  25. Muricy G (1991) Structure des peuplements de spongiaires autour de l’égout de Cortiou (Marseille, France). Vie Milieu 41(4):205–221Google Scholar
  26. Naranjo SA, Carballo JL, Garcìa Gómez JC (1996) The effects of environmental stress on ascidian populations in Algeciras Bay (Southern Spain). Possible Marine Bioindicators. Mar Ecol Prog Ser 144:119–131CrossRefGoogle Scholar
  27. Padilla C (2005) Composición faunística, y alimenticia de moluscos comedores de esponjas (Mollusca, Opistobranquia) en la bahía de Mazatlán (Sinaloa). Bs dissertation, Facultad de Ciencias del Mar, Universidad Autónoma de SinaloaGoogle Scholar
  28. Palumbi SR (1984) Tactics of acclimation: morphological changes of sponges in an unpredictable environ. Science 225:1478–1480CrossRefGoogle Scholar
  29. Palumbi SR (1985) Spatial variation in an alga-sponge commensalism and the evolution of ecological interactions. Am Nat 126:267–274CrossRefGoogle Scholar
  30. Palumbi SR (1986) How body plans limit acclimation: responses of a demosponge to wave force. Ecology 67(1):208–214CrossRefGoogle Scholar
  31. Raven ME (1986) Evolution of plant life forms. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 421–492Google Scholar
  32. Rützler K (1978) Sponges in coral reefs. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. UNESCO Monogr Oceanogr Methodol, Paris 5:299–313Google Scholar
  33. Rützler K (1990) Associations between Caribbean sponges and photosynthetic organisms. In Rützler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington DC, pp 455–466Google Scholar
  34. Sará M, Vacelet J (1973) Ecologie des Démosponges. In: Masson et Cie (eds) Traité de Zoologie, Anatomie, Sistématique, Biologie, vol III. Spongiaires, Paris, pp 472–576Google Scholar
  35. Schönberg CHL, Barthel D (1997) Inorganic skeleton of the demosponge Halichondria panicea. Seasonality in spicule production in the Baltic Sea. Mar Biol 130:133–140CrossRefGoogle Scholar
  36. Sokal RR, Rohlf JJ (1981) Biometry. WH Freeman and Co, San FranciscoGoogle Scholar
  37. Stone AR (1970) Growth and reproduction of Hymeniacidon perleve (Montagu) (Porifera) in Langsone Harbour, Hampshire. J Zool 161:443–459CrossRefGoogle Scholar
  38. Trautman DA, Hinde R (2002) Sponge/algal symbioses: a diversity of associations. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer, Dordrecht, pp 523–537Google Scholar
  39. Trautman DA, Hinde R, Borowitzka MA (2000) Population dynamics of an association between a coral reef sponge and a red macroalga. J Exp Mar Biol Ecol 244:87–105CrossRefGoogle Scholar
  40. Trautman DA, Hinde R, Borowitzka MA. (2003) The role of habitat in determining the distribution of a sponge-red alga symbiosis on a coral reef. J Exp Mar Biol Ecol 283:1–20CrossRefGoogle Scholar
  41. Vicente VP (1978) An ecological evaluation of the West Indian demosponge Anthosigmella varians (Hadromerida: Spirastrellidae). Bull Mar Sci 28:771–777Google Scholar
  42. Vogel S (1981) Life in moving fluids-the physical biology of flow. Princeton University Press, Princeton, pp 1–467Google Scholar
  43. Wilkinson CR, Vacelet J (1979) Transplantation of marine sponges to different conditions of light and current. J Exp Mar Biol Ecol 37:91–104CrossRefGoogle Scholar
  44. Woodin SA (1991) Recruitment of infauna: positive or negative cues? Am Zool 31:797–807CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • José Luis Carballo
    • 1
    Email author
  • Enrique Ávila
    • 1
    • 3
  • Susana Enríquez
    • 2
  • Leonardo Camacho
    • 1
    • 3
  1. 1.Laboratorio de Ecología del Bentos. Instituto de Ciencias del Mar y LimnologíaUniversidad Nacional Autónoma de MéxicoMazatlánMexico
  2. 2.Laboratorio de Fotobiología. Unidad Académica Puerto Morelos. Instituto de Ciencias del Mar y LimnologíaUniversidad Nacional Autónoma de MéxicoCancunMexico
  3. 3.Postgrado en Ciencias del Mar y LimnologíaUNAMMazatlánMexico

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