Subindividual variability in sea pens (Octocorallia: Pennatulacea)




intracolonial variability, Pennatulacea, Pennatula, Ptilella, coefficient of variation, variance, within-plant variation


Comparisons between plants and sessile modular colonial invertebrates offer interesting parallelisms between plant and animal body plans after millions of years of divergent evolution. Among these parallelisms might be the existence and distribution of intraindividual heterogeneity in organ traits, also named subindividual variability. Subindividual variability is quantitatively important and has many consequences for plant individuals, populations and communities, and for animal consumers as well. However, could a similar process of subindividual variability occur in sea pens, which have a modular architecture similar to that of plants? In the literature of marine invertebrates very little is known about the presence and magnitude of subindividual variability in modular organisms. This study provides for the first time a quantitative assessment of subindividual variability in sea pens, analysing certain biometric features of reiterated structures that presumably have some ecological function, and offers an initial comparison of quantitative levels of subindividual variation between plants and sea pens.


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Alonso C., Pérez R., Bazaga P., et al. 2018. Within-plant variation in seed size and inflorescence fecundity is associated with epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae). Ann. Bot. 121: 153-160.

Baillon S., Hamel J.-F., Mercier A. 2014a. Diversity, distribution and nature of faunal associations with deep-sea pennatulacean corals in the Northwest Atlantic. PLoS ONE 9: e111519.

Baillon S., Hamel J.-F., Wareham V.E., Mercier A. 2014b. Seasonality in reproduction of the deep-water pennatulacean coral Anthoptilum grandiflorum. Mar. Biol. 161: 29-43.

Baillon S., English M., Hamel J.F., Mercier A. 2016. Comparative biometry and isotopy of three dominant pennatulacean corals in the Northwest Atlantic. Acta Zool. 97: 475-493.

Bayer F.M. 1956. Octocorallia. In: Moore, R.C. (ed). Treatise on invertebrate paleontology. Part F. Coelenterata. Geol. Soc. America Univ. Kansas Press. New York and Lawrence Kansas, pp. 166-231.

Bayer F.M., Grasshoff M., Verseveldt J. 1983. Illustrated trilingual glossary of morphological and anatomical terms applied to Octocorallia. E. J. Brill/ Dr. Backhuys, Leiden. 75 pp.

Birkeland C. 1974. Interactions between a sea pen and seven of its predators. Ecol. Monogr. 44: 211-232.

Borges R.M. 2005. Do plants and animals differ in phenotypic plasticity? J. Biosci. 30: 41-50.

Brito T.A.S., Tyler P.A., Clarke A. 1997. Reproductive biology of the Antarctic octocoral Thouarella variabilis Wright and Studer 1889. Proc 6th Int Conf Coelenterate Biology, Natural History Museum of Leiden, The Netherlands. 63-69 pp.

Brown M.B., Forsythe A.B. 1974. Robust tests for the equality of variances. J. Am. Stat. Assoc. 69: 364-367.

Buhl-Mortensen L., Vanreusel A., Gooday A.J., et al. 2010. Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar. Ecol. 31: 21-50.

Clippele L.H., Buhl-Mortensen P., Buhl-Mortensen L. 2015. Fauna associated with cold water gorgonians and sea pens. Cont. Shelf Res. 105: 67-78.

Coma R., Ribes M., Zabala M., Gili J.M. 1995. Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuricea clavata. Mar. Ecol. Prog. Ser. 117: 173-183.

Conover W.J., Johnson M.E., Johnson M.M. 1981. A comparative study of tests for homogeneity of variances, with applications to the outer continental shelf bidding data. Technomet. 23: 351-361.

Darwin C. 1859. On the origin of species. Murray, London.

Duncan J.C. 1998. Biology of the sea pen Pteroeides sp. in Fiordland, New Zealand. PhD dissertation, Univ. Otago (New Zealand), 88 pp.

Edwards D.C.B., Moore C.G. 2008. Reproduction in the sea pen Pennatula phosphorea (Anthozoa: Pennatulacea) from the west coast of Scotland. Mar. Biol. 155: 303-314.

Edwards D.C.B., Moore C.G. 2009. Reproduction in the sea pen Funiculina quadrangularis (Anthozoa: Pennatulacea) from the west coast of Scotland. Estuar. Coast. Shelf Sci. 82: 161-168.

Finelli C.M., Helmuth B.S., Pentcheff N.D., Wethey D.S. 2007. Intracolony variability in photosynthesis by corals is affected by water flow: role of oxygen flux. Mar. Ecol. Prog. Ser. Ser. 349: 103-110.

Foster A.B. 1980. Environmental variation in skeletal morphology within the Caribbean reef corals Montastraea annularis and Siderastrea siderea. Bull. Mar. Sci. 30: 678-709.

Foster A.B. 1985. Variation within coral colonies and its importance for interpreting fossil species. J. Paleontol. 59: 1359-1381.

Fox J., Weisberg S. 2019. An {R} Companion to Applied Regression, Third Edition. Thousand Oaks CA: Sage.

García-Cárdenas F.J, López-González P.J. 2022a. Growth and reproductive traits of deep-sea pen Anthoptilum murrayi Kölliker, 1880, from Iceland (North Atlantic). Mar. Biol. Res. 18: 7-8, 448-465.

García-Cárdenas F.J, López-González P.J. 2022b. Some observations on the reproductive biology of the Mediterranean pennatulacean Pteroeides spinosum (Ellis and Solander, 1786) (Cnidaria: Octocorallia: Pennatulacea). Thalassas

García-Cárdenas F.J, Drewery J., López-González P.J. 2019. Resurrection of the sea pen genus Ptilella Gray, 1870 and description of Ptilella grayi n. sp. from the NE Atlantic (Octocorallia: Pennatulacea). Sci. Mar. 83: 261-276.

García-Matucheski S., Muniain C. 2011. Predation by the nudibranch Tritonia odhneri (Opisthobranchia: Tritoniidae) on octocorals from the South Atlantic Ocean. Mar. Biodivers. 41: 287-297.

Goffredo S., Caroselli E., Gasparini G., et al. 2011. Colony and polyp biometry and size structure in the orange coral Astroides calycularis (Scleractinia: Dendrophylliidae). Mar. Biol. Res. 7: 272-280.

Haeckel E.H.P.A. 1869. Ueber Den Organismus Der Schwamme und Ihre Verwandtschaft Mit Den Coralen.

Hallé F. 1999. Éloge de la plante. Pour une nouvelle biologie. Éditions du Seuil, Paris, France. 356 pp.

Harrison P.L., Wallace C.C. 1990. Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed). Ecosystems of the World. Vol. 25. Coral Reefs. Amsterdam: Elsevier. 133-207 pp.

Harvell D. 1984. Why nudibranchs are partial predators: intracolonial variation in bryozoan palatability. Ecology 65: 716-724.

Herrera C.M. 2009. Multiplicity in unity. Plant subindividual variation and interactions with animals, Univ. Chicago Press, Chicago, USA. 437 pp.

Herrera C.M. 2017. The ecology of subindividual variability in plants: patterns, processes, and prospects. Web Ecology 17: 51-64.

Herrera C.M., Medrano M., Bazaga P. 2015. Continuous within plant variation as a source of intraspecific functional diversity: patterns, magnitude, and genetic correlates of leaf variability in Helleborus foetidus (Ranunculaceae). Am. J. Bot. 102: 225-232.

Herrera C.M., Bazaga P., Pérez R., Alonso C. 2021. Lifetime genealogical divergence within plants leads to epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae). New Phytol. 231: 2065-2076.

Hickson S.J. 1916. The Pennatulacea of the Siboga Expedition, with a general survey of the order. Siboga Expeditie Monographs 14, Livr. 77: 1-265.

Hughes R.N. 2005. Lessons in modularity: the evolutionary ecology of colonial invertebrates. Sci. Mar. 69S1: 169-179.

Jackson J.B.C., Coates A.G. 1986. Life cycles and evolution of clonal (modular) animals. Philos. Trans. R. Soc. Lond. B. 313: 7-22.

Jones L.A., Hiscock K., Connor D.W. 2000. Marine habitat reviews, a summary of ecological requirements and sensitivity characteristics for the conservation and management of Marine SACs. UK Marine SACs Project Report. Peterborough: Joint Nature Conservation Committee. 178 pp.

Kaandorp J.A., Kübler J.E. 2001. Environmentally driven plasticity. In: The Algorithmic Beauty of Seaweeds, Sponges and Corals. Springer, Berlin, Heidelberg. 15-66 pp.

Key M.M. 1990. Intracolony variation in skeletal growth rates in Paleozoic ramose trepostome bryozoans. Paleobiology 16: 483-491.

Kim E., Lasker H.R., Coffroth M.A., Kim K. 2004. Morphological and genetic variation across reef habitats in a broadcast-spawning octocoral. Hydrobiologia 530: 423-432.

Lapid E.D., Wielgus J., Chadwick-Furman N.E. 2004. Sweeper tentacles of the brain coral Platygyra daedalea: Induced development and effects on competitors. Mar. Ecol. Prog. Ser. 282: 161-71.

Lasker H.R., Boller M.L., Castanaro J., Sánchez J.A. 2003. Modularity and determinate growth in a gorgonian coral. Biol. Bull. 205: 319-330.

Lenth R. 2019. emmeans 1.4: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.

Leuzinger S., Anthony K.R.N., Willis B.L. 2003. Reproductive energy investment in corals: Scaling with module size. Oecologia 136: 524-31.

Levene H. 1960. Robust tests for equality of variances. In: Olkin I. et al. (eds), Contributions to probability and statistics: Essays in honor of Harold Hotelling. Stanford, CA: Stanford University Press. 278-292 pp.

Menezes N.M.D., Neves E.G., Barros F., et al. 2013. Intracolonial variation in Siderastrea de Blainville, 1830 (Anthozoa, Scleractinia): taxonomy under challenging morphological constraints. Biota Neotropica 13: 108-116.

O’Dea A. 2003. Seasonality and zooid size variation in Panamanian encrusting bryozoans. J. Mar. Biol. Ass. U. K. 83: 1107-1108.

O’Dea A., Okamura B. 2000. Intracolony variation in zooid size in cheilostome bryozoans as a new technique for investigating palaeoseasonality. Palaeogeogr. Palaeoclimatol. Palaeoecol. 162: 319-332.

Orejas C., López-González P.J., Gili J.M., et al. 2002. Distribution and reproductive ecology of the Antarctic octocoral Ainigmaptilon antarcticum in the Weddell Sea. Mar. Ecol. Prog. Ser. 231: 101-114.

Osada N., Yasumura Y., Ishida A. 2014. Leaf nitrogen distribution in relation to crown architecture in the tall canopy species, Fagus crenata. Oecologia 175: 1093-1106.

Oury N., Gélin P., Magalon H. 2020. Together stronger: Intracolonial genetic variability occurrence in Pocillopora corals suggests potential benefits. Ecol. Evol. 10: 5208-5218.

Paradis E., Schliep K. 2018. ape 5.0: an environment for modern phylogenetic and evolutionary analyses in R. Bioinformatics 35: 526-528.

Pearson K. 1901. Mathematical contributions to the theory of evolution: 9, On the principle of homotyposis and its relation to heredity, to the variability of the individual, and to that of the race; part 1, homotyposis in the vegetable kingdom. Philos. Trans. R. Soc. Lond. A. 197: 285-379.

Pérez-Harguindeguy N., Díaz S., Garnier E., et al. 2013. New handbook for standardised measurement of plant functional traits worldwide. Aust. J. Bot. 61: 167-234.

Pinheiro J., Bates D., DebRoy S., Sarkar D., R Core Team. 2018. nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1-137.

Prada C., Schizas N.V., Yoshioka P.M. 2008. Phenotypic plasticity or speciation? A case from a clonal marine organism. BMC Evol. Biol. 8: 47.

R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Sakai K. 1998. Effect of colony size, polyp size, and budding mode on egg production in a colonial coral. Biol. Bull. 195: 319-25.

Sánchez J.A., Lasker H.R. 2003. Patterns of morphologic integration in branching colonies of marine modular organisms: supramodule organization in gorgonian corals. Proc. R. Soc. Lond. B. 270: 2039-2044.

Sánchez J.A., Aguilar C., Dorado D., Manrique N. 2007. Phenotypic plasticity and morphological integration in a marine modular invertebrate. BMC Evol. Biol. 7: 122.

Schultz B.B. 1983. On Levene’s test and other statistics of variation. Evol. Theory 6:197-203.

Schultz B.B. 1985. Levene’s test for relative variation. Syst. Zool. 34: 449-456.

Schweinsberg M., Tollrian R., Lampert K.P. 2017. Inter‐and intra‐colonial genotypic diversity in hermatypic hydrozoans of the family Milleporidae. Mar. Ecol. 38: e12388.

Sherwood O.A., Jamieson R.E., Edinger E.N., Wareham V.E. 2008. Stable C and N isotopic composition of cold-water corals from the Newfoundland and Labrador continental slope: Examination of trophic, depth and spatial effects. Deep-Sea Res. I. 55: 1392-1402.

Sides C.B., Enquist B.J., Ebersole J.J., et al. 2014: Revisiting Darwin’s hypothesis: Does greater intraspecific variability increase species’ ecological breadth? Am. J. Bot. 101: 56-62.

Siefert A., Violle C., Chalmandrier L., Albert C.H., et al. 2015: A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol. Lett. 18: 1406-1419.

Soong K. 2005. Reproduction and colony integration of the sea pen Virgularia juncea. Mar. Biol. 146: 1103-1109.

Soong K, Lang J.C .1992. Reproductive integration in reef corals. Biol. Bull. 183: 418-431.

Tixier-Durivault A. 1965. Quelques octocoralliaires australiens. Bull. Mus. Natl. Hist. Nat. 37: 705-716.

Ulstrup K.E., Ralph P.J., Larkum A.W.D., Kühl M. 2006. Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis. Mar. Biol. 149: 1325-1335.

Van Valen L. 1978. The statistics of variation. Evol. Theory 4: 33-43.

Wejnert K.E., Smith A.M. 2008. Within‐colony variation in skeletal mineralogy of Adeonellopsis sp. (Cheilostomata: Bryozoa) from New Zealand. N. Z. J. Mar. Freshw. Res. 42: 389-395.

Williams G.C., Hoeksema B.W., van Ofwegen L.P. 2012. A fifth morphological polyp in pennatulacean octocorals, with a review of polyp polymorphism in the genera Pennatula and Pteroeides (Anthozoa: Pennatulidae). Zool. Stud. 51: 1006-1017.

Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York.

Wickham H., Bryan J. 2019. readxl: Read Excel Files. R package version 1.3.1.

Wickham H., Romain F., Lionel H., Kirill M. 2019. dplyr: A Grammar of Data Manipulation. R package version 0.8.3.



How to Cite

García-Cárdenas FJ. Subindividual variability in sea pens (Octocorallia: Pennatulacea). scimar [Internet]. 2023Jul.4 [cited 2023Oct.4];87(2):e063. Available from:




Funding data

Ministerio de Economía y Competitividad
Grant numbers CTM2017-83920-P