Clonal behavior has been hypothesized to provide an escape from allometric metabolic scaling that limits the maximum mass achieved by a single individual. Here, we demonstrate the capacity of a wide-spread, non-native sea anemone to buffer its colony biomass accumulation rate across environments by modulating ramet body size through environmentally dependent growth, fission, and catabolism. In 2015, thermal reaction norms for growth and fission behavior were constructed using clonal lines of the sea anemone Diadumene lineata. In 2018, variation in growth patterns under a factorial cross of temperature level and oxygen availability was examined to test the hypothesis that individual ramet size is regulated by oxygen limitation in accordance with optimal size theory. Across a wide range of temperatures, colonies accumulated a similar amount of biomass despite a radical shift from unitary to clonal growth, supporting fission as a mechanism to buffer growth rates over a range of conditions. Individual body size appears to be regulated by the environment with increased temperature and reduced oxygen modifying fission and mass-specific growth patterns, leading to the production of smaller-bodied ramets in warm conditions. However, whether anemones in common garden conditions reduce individual body size through catabolism or fission depends on the region of origin and may relate to differences in seasonal temperature patterns among coastlines, which influence the energetic benefits of fission rate plasticity.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Data generated during the current study are available from the corresponding author on reasonable request.
Amarasekare P, Johnson C (2017) Evolution of thermal reaction norms in seasonally varying environments. Am Nat 189:E31–E45
Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58
Atoda K (1973) Pedal laceration of the sea anemone, Haliplanella Luciae. Publ Seto Mar Biol Lab 20:299–313
Audzijonyte A, Barneche DR, Baudron AR, Belmaker J, Clark TD, Marshall CT, Morrongiello JR, van Rijn I (2018) Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms? Global Ecol Biogeogr 28:64–77
Ayre DJ (1985) Localized adaptation of clones of the sea anemone Actinia tenebrosa. Evolution 39:1250–1260
Barton K (2018) MuMIn: multi-modal inference. R Package version 1(15):6
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Baumann H, Conover DO (2011) Adaptation to climate change: contrasting patterns of thermal-reaction-norm evolution in Pacific versus Atlantic silversides. Proc R Soc B 278:2265–2273
Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155
Burgess SC, Ryan WH, Blackstone NW, Edmunds PJ, Hoogenboom MO, Levitan DR, Wulff JL (2017) Metabolic scaling in modular animals. Invertebr Biol 136:456–472
Buss LW, Blackstone NW (1991) An Experimental Exploration of Waddington’s Epigenetic Landscape. Philos Trans R Soc B Biol Sci 332:49–58
Cancino JM, Rodger NH (1985) An ecological overview of cloning in Metazoa. In: Jeremy BC, Jackson BLW, Robert EC (eds) Population biology and evolution of clonal organisms. Yale University Press, New Haven, pp 153–186
Chia F (1976) Sea anemone reproduction: patterns and adaptive radiations. Coelenterate Ecol Behav 261–270
Chomsky O, Kamenir Y, Hyams M, Dubinsky Z, Chadwick-Furman NE (2004) Effects of temperature on growth rate and body size in the Mediterranean Sea anemone Actinia equina. J Exp Mar Bio Ecol 313:63–73
Cohen AN, Carlton JT (1995) Nonindigenous aquatic species in a United States Estuary: a case study of the biological invasions of the San Francisco Bay and Delta. Washington D.C.: US Fish and Wildlife Service
Edmunds PJ (2007) Physiological ecology of the clonal corallimorpharian Corynactis californica. Mar Biol 150:783–796
Fautin DG (2002) Reproduction of Cnidaria. Can J Zool 80:1735–1754
Ferretti P, Géraudie J (1998) Cellular and molecular basis of regeneration: from invertebrates to humans. Wiley, Hoboken
Forster J, Hirst AG, Atkinson D (2011) How do organisms change size with changing temperature? The importance of reproductive method and ontogenetic timing. Funct Ecol 25:1024–1031
Forster J, Hirst AG, Atkinson D (2012) Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc Natl Acad Sci 109:19310–19314
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks
Francis L (1979) Contrast between solitary and clonal lifestyles in the sea anemone. Am Zool 19:669–681
Francis L (1988) Cloning and aggression among sea anemones (Coelenterata: Actiniaria) of the rocky shore. Biol Bull 174:241–253
Geller JB, Walton ED (2001) Breaking up and getting together: evolution of symbiosis and cloning by fission in sea anemones (Genus Anthopleura). Evolution 55:1781–1794
Geller JB, Fitzgerald LJ, King CE (2005) Fission in sea anemones: integrative studies of life cycle evolution. Integr Comp Biol 45:615–622
Glazier DS (2014) Metabolic scaling in complex living systems. Systems 2:451–540
Glon H, Haruka Y, Daly M, Nakaoka M (2019) Temperature and salinity survival limits of the fluffy sea anemone, Metridium senile (L.), in Japan. Hydrobiologia 830:303–315
Gotthard K, Nylin S (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74:3
Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017
Horne CR, Hirst AG, Atkinson D (2015) Temperature-size responses match latitudinal-size clines in arthropods, revealing critical differences between aquatic and terrestrial species. Ecol Lett 18:327–335
Hughes RN (1987) The functional ecology of clonal animals. Funct Ecol 1:63–69
Hughes RN (1989) Functional biology of clonal animals, 1st edn. Springer Science and Business Media, Suffolk
Jackson JBC (1977) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am Nat 111:743–767
Jackson JBC (1985) Distribution and ecology of clonal and aclonal benthic invertebrates. In: Jackson JBC, Buss LW, Cook RE (eds) Population biology and evolution of clonal organisms. Yale University Press, New Haven, pp 297–355
Jackson JBC, Coates AG (1986) Life Cycles and Evolution of Clonal (Modular) Animals. Philos Trans R Soc B Biol Sci 313:7–22
Johnson LL, Shick JM (1977) Effects of fluctuating temperature and immersion on asexual reproduction in the intertidal sea anemone Hauplanella luciae (Verrill) in laboratory culture. J Exp Mar Bio Ecol 28:141–149
Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268
Kooijman SALM (2010) Dynamic energy budget theory for metabolic organization. Cambridge University Press, Cambridge
Lefcheck J (2018) Piecewise structural equation modeling. R Package version 2:2
Levitan DR (1988) Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76:627–629
McManus MG, Place AR, Zamer WE (1997) Physiological variation among clonal genotypes in the sea anemone Haliplanella lineata: growth and biochemical content. Biol Bull 192:426–443
Minasian LL (1979) The effect of exogenous factors on morphology and asexual reproduction in laboratory cultures of the intertidal sea anemone, Haliplanella luciae (Verrill) (Anthozoa: Actiniaria) from Delaware. J Exp Mar Bio Ecol 40:235–246
Mire P, Venable S (1999) Programmed cell death during longitudinal fission in a sea anemone. Invertebrate Biol 118:319–331
Miyawaki M (1952) Temperature as a factor influencing upon the fission of the orange-striped sea-anemone, Diadumene luciae (with 2 text-figures). J Fac Sci Hokkaido Univ, Ser 6 Zool 11:77–80
Murren CJ, Maclean HJ, Diamond SE, Steiner UK, Heskel MA, Handlesman CA, Ghalambor CK, Auld JR, Callahan HS, Pfenning DW, Relyea RA, Schlicting CD, Kingsolver J (2014) Evolutionary change in continuous reaction norms. Am Nat 183:453–467
Pörtner H (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146
Rasband WS (1997) Image J. National Institutes of Health, Bethesda
Reitzel AM, Burton P, Krone C, Finnerty J (2007) Comparison of developmental trajectories in the Starlet Sea Anemone Nematostella vectensis: embryogenesis, regeneration, and two forms of asexual fission. Invertebr Biol 126:99–112
Reitzel AM, Stefanik D, Finnerty JR (2011) Asexual reproduction in Cnidaria: Comparative developmental processes and candidate mechanisms. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution: the genetics and physiology of life. Oxford University Press, Oxford, pp 101–113
Reitzel AM, Chu T, Edquist S, Genovese C, Church C, Tarrant AM, Finnerty JR (2013) Physiological and developmental responses to temperature by the sea anemone Nematostella vectensis. Mar Ecol Prog Ser 484:115–130
Ryan WH (2018) Temperature-dependent growth and fission rate plasticity drive seasonal and geographic changes in body size in a clonal sea anemone. Am Nat 191:211–219
Ryan WH, Miller TE (2019) Reproductive strategy changes across latitude in a clonal sea anemone. Mar Ecol Prog Ser 611:129–141
Sassaman C, Mangum CP (1970) Patterns of temperature adaptation in North American Atlantic coastal actinians. Mar Biol 7:123–130
Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integ Comp Biol 51:691–702
Scranton K, Amarasekare P (2017) Predicting phenological shifts in a changing climate. Proc Natl Acad Sci 114:201711221
Sebens KP (1979) The energetics of asexual reproduction and colony formation in benthic marine invertebrates. Am Zool 19:683–697
Sebens K (1980) The regulation of asexual reproduction and indeterminate body size in the sea anemone Anthopleura elegantissima (Brandt). Biol Bull 158:370–382
Sebens K (1981) The allometry of feeding, energetics, and body size in three sea anemone species. Biol Bull 161:152–171
Sebens KP (1982) Asexual reproduction in Anthopleura elegantissima (Anthozoa: Actinaria): seasonality and spatial extent of clones. Ecology 63:434–444
Sebens KP (1987) The ecology of indeterminate growth in animals. Annu Rev Ecol Syst 18:371–407
Sebens KP (2002) Energetic constraints, size gradients, and size limits in benthic marine invertebrates. Integr Comp Biol 42:853–861
Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Clim Chang 1:401–406
Shick JM, Hoffmann RJ, Lamb AN (1979) Asexual Reproduction, Population Structure, and Genotype-Environment Interactions in Sea Anemones. Am Zool 19:699–713
R core team (2014) R: a language and environment for statistical computing
Ting J, Geller JB (2000) Clonal diversity in introduced populations of an Asian sea anemone in North America. Biol Invasions 2:23–32
Uchida T (1932) Occurrence in Japan of Diadumene luciae, a remarkable actinian of rapid dispersal (with plate IV, 1 chart and 4 text-figures). J Fac Sci Hokkaido Univ, Ser 6 Zool 2:69–82
Zamer WE, Mangum CP (1979) Irreversible nongenetic temperature adaptation of oxygen uptake in clones of the sea anemone Haliplanella luciae (Verrill). Biol Bull 157:536–547
We thank C.R. Hadfield and K. Atkins for logistics and help in the mesocosm at the Marine Biological Association; M. Yant for help maintaining anemones at the University of Alabama at Birmingham; J. Mutz and J. Imhoff for field assistance; J. Mutz and two anonymous reviewers for comments on the manuscript; and B. Hughes and K. Wasson for access to Elkhorn Slough. Funding was provided by the PADI Foundation (#21902) to WHR; the Ray Lankester Investigatorship of the Marine Biological Association of the UK (2017–2019) to SAKH; Start-up funds from the University of Alabama at Birmingham to SAKH; the Marine Biological Association of the UK Fellowship to NM. WHR was supported as a UAB MERIT postdoctoral fellow during the preparation of the manuscript.
Conflicts of interest
The authors declare that they have no conflicts of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by Undisclosed experts.
Responsible Editor: F. Bulleri.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Ryan, W.H., Adams, L., Bonthond, G. et al. Environmental regulation of individual body size contributes to geographic variation in clonal life cycle expression. Mar Biol 166, 157 (2019). https://doi.org/10.1007/s00227-019-3608-z