Subindividual variability in sea pens (Octocorallia: Pennatulacea)
DOI:
https://doi.org/10.3989/scimar.05260.063Keywords:
intracolonial variability, Pennatulacea, Pennatula, Ptilella, coefficient of variation, variance, within-plant variationAbstract
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.
Downloads
References
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. https://doi.org/10.1093/aob/mcx140 PMid:29186299 PMCid:PMC5786237
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. https://doi.org/10.1371/journal.pone.0111519 PMid:25369515 PMCid:PMC4219758
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. https://doi.org/10.1007/s00227-013-2311-8
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. https://doi.org/10.1111/azo.12141
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. https://doi.org/10.1163/9789004631915
Birkeland C. 1974. Interactions between a sea pen and seven of its predators. Ecol. Monogr. 44: 211-232. https://doi.org/10.2307/1942312
Borges R.M. 2005. Do plants and animals differ in phenotypic plasticity? J. Biosci. 30: 41-50. https://doi.org/10.1007/BF02705149 PMid:15824440
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. https://doi.org/10.1080/01621459.1974.10482955
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. https://doi.org/10.1111/j.1439-0485.2010.00359.x
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. https://doi.org/10.1016/j.csr.2015.06.007
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. https://doi.org/10.3354/meps117173
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. https://doi.org/10.1080/00401706.1981.10487680
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. https://doi.org/10.1007/s00227-008-1028-6
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. https://doi.org/10.1016/j.ecss.2009.01.006
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. https://doi.org/10.3354/meps07101
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. https://socialsciences.mcmaster.ca/jfox/Books/Companion/
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. https://doi.org/10.1080/17451000.2022.2147949
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 https://doi.org/10.1007/s41208-022-00505-6
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. https://doi.org/10.3989/scimar.04845.26A
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. https://doi.org/10.1007/s12526-010-0063-y
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. https://doi.org/10.1080/17451000.2010.492222
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. https://doi.org/10.2307/1938043
Herrera C.M. 2009. Multiplicity in unity. Plant subindividual variation and interactions with animals, Univ. Chicago Press, Chicago, USA. 437 pp. https://doi.org/10.7208/chicago/9780226327952.001.0001
Herrera C.M. 2017. The ecology of subindividual variability in plants: patterns, processes, and prospects. Web Ecology 17: 51-64. https://doi.org/10.5194/we-17-51-2017
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. https://doi.org/10.3732/ajb.1400437 PMid:25667075
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. https://doi.org/10.1111/nph.17257 PMid:33634863
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. https://doi.org/10.3989/scimar.2005.69s1169
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. https://doi.org/10.1098/rstb.1986.0022
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. https://doi.org/10.1007/978-3-662-04339-4_2
Key M.M. 1990. Intracolony variation in skeletal growth rates in Paleozoic ramose trepostome bryozoans. Paleobiology 16: 483-491. https://doi.org/10.1017/S0094837300010204
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. https://doi.org/10.1007/s10750-004-2646-8
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. https://doi.org/10.3354/meps282161
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. https://doi.org/10.2307/1543295 PMid:14672986
Lenth R. 2019. emmeans 1.4: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4. https://CRAN.R-project.org/package=emmeans.
Leuzinger S., Anthony K.R.N., Willis B.L. 2003. Reproductive energy investment in corals: Scaling with module size. Oecologia 136: 524-31. https://doi.org/10.1007/s00442-003-1305-5 PMid:12802676
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. https://doi.org/10.1590/S1676-06032013000100012
O'Dea A. 2003. Seasonality and zooid size variation in Panamanian encrusting bryozoans. J. Mar. Biol. Ass. U. K. 83: 1107-1108. https://doi.org/10.1017/S0025315403008348h
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. https://doi.org/10.1016/S0031-0182(00)00136-X
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. https://doi.org/10.3354/meps231101
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. https://doi.org/10.1007/s00442-014-2966-y PMid:24844645
Oury N., Gélin P., Magalon H. 2020. Together stronger: Intracolonial genetic variability occurrence in Pocillopora corals suggests potential benefits. Ecol. Evol. 10: 5208-5218. https://doi.org/10.1002/ece3.5807 PMid:32607144 PMCid:PMC7319244
Paradis E., Schliep K. 2018. ape 5.0: an environment for modern phylogenetic and evolutionary analyses in R. Bioinformatics 35: 526-528. https://doi.org/10.1093/bioinformatics/bty633 PMid:30016406
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. https://doi.org/10.1098/rsta.1901.0020
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. https://doi.org/10.1071/BT12225
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. https://doi.org/10.1186/1471-2148-8-47 PMid:18271961 PMCid:PMC2275222
R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Sakai K. 1998. Effect of colony size, polyp size, and budding mode on egg production in a colonial coral. Biol. Bull. 195: 319-25. https://doi.org/10.2307/1543143 PMid:28297616
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. https://doi.org/10.1098/rspb.2003.2471 PMid:14561292 PMCid:PMC1691470
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. https://doi.org/10.1186/1471-2148-7-122 PMid:17650324 PMCid:PMC1959521
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. https://doi.org/10.1093/sysbio/34.4.449
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. https://doi.org/10.1111/maec.12388
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. https://doi.org/10.1016/j.dsr.2008.05.013
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. https://doi.org/10.3732/ajb.1300284 PMid:24343815
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. https://doi.org/10.1111/ele.12508 PMid:26415616
Soong K. 2005. Reproduction and colony integration of the sea pen Virgularia juncea. Mar. Biol. 146: 1103-1109. https://doi.org/10.1007/s00227-004-1509-1
Soong K, Lang J.C .1992. Reproductive integration in reef corals. Biol. Bull. 183: 418-431. https://doi.org/10.2307/1542018 PMid:29300508
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. https://doi.org/10.1007/s00227-006-0286-4
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. https://doi.org/10.1080/00288330809509967
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. https://doi.org/10.1007/978-3-319-24277-4
Wickham H., Bryan J. 2019. readxl: Read Excel Files. R package version 1.3.1. https://CRAN.R-project.org/package=readxl
Wickham H., Romain F., Lionel H., Kirill M. 2019. dplyr: A Grammar of Data Manipulation. R package version 0.8.3. https://CRAN.R-project.org/package=dplyr
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.
Funding data
Ministerio de Economía y Competitividad
Grant numbers CTM2017-83920-P