Abstract
Some sedentary marine invertebrates have the potential to modify the environments they experience by moving, even as adults. Of particular interest are sea anemones, which, despite appearing immobile, can move throughout their lives. Individual locomotion may mitigate changes in environment conditions and, therefore, play an important role in the natural history of sea anemones, especially in naturally variable and/or stochastic environments. Sea anemones that associate with algal endosymbionts may respond to changes in nutrition, both autotrophic (from algae) and heterotrophic (from prey). Here, we describe the adult movement behaviors and asexual reproduction of the sea anemone Exaiptasia diaphana in response to changes in food availability and photosymbiont density. Anemones were collected from mangrove roots in the Florida Keys USA (24° 49′ 21.91″ N, 80° 48′ 37.95″ W) during January 2016 and exposed to a factorial experiment in which food availability and exposure to temperature shock were manipulated. Sea anemones exhibited a variety of responses, including (1) increased crawling along the substrate in response to starvation, (2) increased detachment from the substrate and reattachment in a new location in response to starvation, and (3) increased production of motile asexual clones in response to both starvation and temperature-induced changes in symbiont density. These responses are shaped not only by the direct consequences to the sea anemone, but also by the effects on the symbiotic algae, which exchange sugars, lipids, and oxygen for nutrients within the host. Observed patterns of movement and reproduction are likely advantageous for life in the dynamic mangrove root fouling communities where this anemone species occurs. The ability to disperse as an adult may give this otherwise sedentary invertebrate an advantage in naturally stochastic conditions or in rapidly changing environments.
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Data availability
The datasets generated during and analysed during the current study are available in the Dryad Digital Repository, https://doi.org/10.15146/R3509H.
References
Bellis ES, Edlund RB, Berrios HK, Lessios HA, Denver DR (2018) Molecular signatures of host specificity linked to habitat specialization in Exaiptasia sea anemones. Ecol Evol 8:5413–5426. https://doi.org/10.1002/ece3.4058
Bergschneider H, Muller-Parker G (2008) Nutritional role of two algal symbionts in the temperate sea anemone Anthopleura elegantissima Brandt. Biol Bull 215:73–88. https://doi.org/10.2307/25470685
Brooker RW, Travis JMJ, Clark EJ, Dytham C (2007) Modelling species’ range shifts in a changing climate: the impacts of biotic interactions, dispersal distance and the rate of climate change. J Theor Biol 245:59–65. https://doi.org/10.1016/j.jtbi.2006.09.033
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138. https://doi.org/10.1007/s003380050249
Cary LR (1911) A study of pedal laceration in actinians. Biol Bull 20:81–107. https://doi.org/10.2307/1536038
Chadwick NE (1987) Interspecific aggressive behavior of the corallimorpharian corynactis californica (cnidaria: anthozoa): effects on sympatric corals and sea anemones. Biol Bull 173:110–125. https://doi.org/10.2307/1541866
Chadwick-Furman N, Loya Y (1992) Migration, habitat use, and competition among mobile corals (Scleractinia: Fungiidae) in the Gulf of Eilat, Red Sea. Mar Biol 114:617–623. https://doi.org/10.1007/BF00357258
Chadwick-Furman NE, Spiegel M (2000) Abundance and clonal replication in the tropical corallimorpharian Rhodactis rhodostoma. Invertebr Biol 119:351–360. https://doi.org/10.1111/j.1744-7410.2000.tb00103.x
Chintiroglou Ch, Koukouras A (1992) The feeding habits of three Mediterranean sea anemone species, Anemonia viridis (Forskål), Actinia equina (Linnaeus) and Cereus pedunculatus (Pennant). Helgoländer Meeresunters 46:53–68. https://doi.org/10.1007/BF02366212
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 Biol Ecol 313:63–73. https://doi.org/10.1016/j.jembe.2004.07.017
Clayton W (1985) Pedal laceration by the anemone Aiptasia pallida. Mar Ecol Prog Ser 21:75–80. https://doi.org/10.3354/meps021075
Clayton WS, Lasker HR (1985) Individual and population growth in the asexually reproducing anemone Aiptasia pallida Verrill. J Exp Mar Biol Ecol 90:249–258. https://doi.org/10.1016/0022-0981(85)90170-4
Colella MA, Ruzicka RR, Kidney JA, Morrison JM, Brinkhuis VB (2012) Cold-water event of January 2010 results in catastrophic benthic mortality on patch reefs in the Florida Keys. Coral Reefs 31:621–632. https://doi.org/10.1007/s00338-012-0880-5
Cook CB, D’Elia CF, Muller-Parker G (1988) Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida. Mar Biol 98:253–262. https://doi.org/10.1007/BF00391203
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466. https://doi.org/10.1146/annurev.marine.010908.163757
Davy S, Cook C (2001) The relationship between nutritional status and carbon flux in the zooxanthellate sea anemone Aiptasia pallida. Mar Biol 139:999–1005. https://doi.org/10.1007/s002270100640
Edmunds M, Potts GW, Swinfen RC, Waters VL (1976) Defensive behaviour of sea anemones in response to predation by the opisthobranch mollusc Aeolidia papillosa (L.). J Mar Biol Assoc UK 56:65–83. https://doi.org/10.1017/S0025315400020440
Ellison AM, Farnsworth EJ (1992) The ecology of Belizean mangrove-root fouling communities: patterns of epibiont distribution and abundance, and effects on root growth. In: Jaccarini V, Martens E (eds) The ecology of mangrove and related ecosystems. Springer, Dordrecht, pp 87–98
Fitt WK, Pardy RL (1981) Effects of starvation, and light and dark on the energy metabolism of symbiotic and aposymbiotic sea anemones, Anthopleura elegantissima. Mar Biol 61:199–205. https://doi.org/10.1007/BF00386660
Fordyce AJ, Camp EF, Ainsworth TD (2017) Polyp bailout in Pocillopora damicornis following thermal stress. F1000Research. https://doi.org/10.12688/f1000research.11522.2
Fox RJ, Donelson JM, Schunter C, Ravasi T, Gaitán-Espitia JD (2019) Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos Trans R Soc B Biol Sci 374:20180174. https://doi.org/10.1098/rstb.2018.0174
Fredericks CA (1976) Oxygen as a limiting factor in phototaxis and in intraclonal spacing of the sea anemone Anthopleura elegantissima. Mar Biol 38:25–28. https://doi.org/10.1007/BF00391482
Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182:324–332. https://doi.org/10.2307/1542252
Hamel J-F, Sun J, Gianasi BL, Montgomery EM, Kenchington EL, Burel B, Rowe S, Winger PD, Mercier A (2019) Active buoyancy adjustment increases dispersal potential in benthic marine animals. J Anim Ecol. https://doi.org/10.1111/1365-2656.12943
Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241. https://doi.org/10.1111/j.1461-0248.2005.00871.x
Hiebert TC, Bingham BL (2012) The effects of symbiotic state on heterotrophic feeding in the temperate sea anemone Anthopleura elegantissima. Mar Biol 159:939–950. https://doi.org/10.1007/s00227-011-1871-8
Hunter T (1984) The energetics of asexual reproduction: Pedal laceration in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943). J Exp Mar Biol Ecol 83:127–147. https://doi.org/10.1016/0022-0981(84)90041-8
ICZN (2017) Opinion 2404 (Case 3633)—Dysactis pallida Agassiz in Verrill, 1864 (currently Aiptasia pallida; Cnidaria, Anthozoa, Hexacorallia, Actiniaria): precedence over Aiptasia diaphana (Rapp, 1829), Aiptasia tagetes (Duchassaing de Fombressin & Michelotti, 1864), Aiptasia mimosa (Duchassaing de Fombressin & Michelotti, 1864) and Aiptasia inula (Duchassaing de Fombressin & Michelotti, 1864) not approved. Bull Zool Nomencl 74:130–132
LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, Pérez AL, Reyes-Bonilla H, Warner ME (2010) Host–symbiont recombination versus natural selection in the response of coral–dinoflagellate symbioses to environmental disturbance. Proc R Soc B Biol Sci 277:2925–2934. https://doi.org/10.1098/rspb.2010.0385
Leal MC, Nunes C, Engrola S, Dinis MT, Calado R (2012) Optimization of monoclonal production of the glass anemone Aiptasia pallida (Agassiz in Verrill, 1864). Aquaculture 354–355:91–96. https://doi.org/10.1016/j.aquaculture.2012.03.035
Lesser MP, Witman JD, Sebnens KP (1994) Effects of flow and seston availability on scope for growth of benthic suspension-feeding invertebrates from the Gulf of Maine. Biol Bull 187:319–335. https://doi.org/10.2307/1542289
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Lowry: protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
McClendon JF (1906) On the locomotion of a sea anemone (Medtridium marginatum). Biol Bull 10:66–67. https://doi.org/10.2307/1535667
McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007. https://doi.org/10.1007/s00248-012-0085-z
Muller-Parker G (1984) Photosynthesis-irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae. Mar Biol 82:225–232. https://doi.org/10.1007/BF00392403
Muller-Parker G, Davy SK (2001) Temperate and tropical algal-sea anemone symbioses. Invertebr Biol 120:104–123
Muscatine L, Grossman D, Doino J (1991) Release of symbiotic algae by tropical sea anemones and corals after cold shock. Mar Ecol Prog Ser 77:233–243
Ottaway JR, Thomas IM (1971) Movement and zonation of the intertidal anemone Actinia tenebrosa Farqu. (Cnidaria: Anthozoa) under experimental conditions. Mar Freshw Res 22:63–78. https://doi.org/10.1071/mf9710063
Parker GH (1916) Locomotion of sea-anemones. Proc Natl Acad Sci USA 2:449–450
Pearse VB (1974) Modification of sea anemone behavior by symbiotic zooxanthellae: phototaxis. Biol Bull 147:630–640. https://doi.org/10.2307/1540746
Piniak GA, Lipschultz F, McClelland J (2003) Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar Ecol Prog Ser 262:125–136. https://doi.org/10.3354/meps262125
Quesada AJ, Acuña FH, Cortés J (2014) Diet of the sea anemone Anthopleura nigrescens: composition and variation between daytime and nighttime high tides. Zool Stud 53:26. https://doi.org/10.1186/s40555-014-0026-2
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 31 July 2019
Rädecker N, Raina J-B, Pernice M, Perna G, Guagliardo P, Kilburn MR, Aranda M, Voolstra CR (2018) Using Aiptasia as a model to study metabolic interactions in cnidarian-Symbiodinium symbioses. Front Physiol 9:214. https://doi.org/10.3389/fphys.2018.00214
Rands ML, Douglas AE, Loughman BC, Ratcliffe RG (1992) Avoidance of hypoxia in a cnidarian symbiosis by algal photosynthetic oxygen. Biol Bull 182:159–162. https://doi.org/10.2307/1542191
Rapp W (1829) Über die Polypen im Allgemeinen und die Actinien. Grolsherzogl. Sdch, Weimar, p 62
Raven JA, Beardall J, Flynn KJ, Maberly SC (2009) Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin’s insectivorous plants. J Exp Bot 60:3975–3987. https://doi.org/10.1093/jxb/erp282
Riemann-Zürneck K (1998) How sessile are sea anemones? A review of free-living forms in the Actiniaria (Cnidaria: Anthozoa). Mar Ecol 19:247–261. https://doi.org/10.1111/j.1439-0485.1998.tb00466.x
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 191:210–219. https://doi.org/10.1086/695496
Ryan WH, Miller TE (2019) Reproductive strategy changes across latitude in a clonal sea anemone. Mar Eco Prog Ser 611:129–141. https://doi.org/10.3354/meps12862
Ryan WH, Adams L, Bonthond G, Mieszkowska PKE, Krueger-Hadfield SA (2019) Environmental regulation of individual body size contributes to geographic variation in clonal life cycle expression. Mar Biol 166:157. https://doi.org/10.1007/s00227-019-3608-z
Sammarco P (1982) Polyp bail-out: an escape response to environmental stress and a new means of reproduction in corals. Mar Ecol Prog Ser 10:57–65. https://doi.org/10.3354/meps010057
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675 (PMID 22930834)
Sebens KP (1981a) Recruitment in a sea anemone population: juvenile substrate becomes adult prey. Science 213:785–787. https://doi.org/10.1126/science.213.4509.785
Sebens KP (1981b) The allometry of feeding, energetics, and body size in three sea anemone species. Biol Bull 161:152–171. https://doi.org/10.2307/1541115
Sebens KP (1984) Agonistic behavior in the intertidal sea anemone Anthopleura xanthogrammica. Biol Bull 166:457–472. https://doi.org/10.2307/1541154
Shick JM, Hoffmann RJ, Lamb AN (1979) Asexual reproduction, population structure, and genotype-environment interactions in sea anemones. Integr Comp Biol 19:699–713. https://doi.org/10.1093/icb/19.3.699
Smith D, Muscatine L, Lewis D (1969) Carbohydrate movement from autotrophs to heterotrophs in parasitic and mutualistic symbioisis. Biol Rev 44:17–85. https://doi.org/10.1111/j.1469-185X.1969.tb00821.x
Sund PN (1958) A study of the muscular anatomy and swimming behaviour of the sea anemone, Stomphia coccinea. J Cell Sci s3-99:401–420
Svensson JR, Marshall DJ (2015) Limiting resources in sessile systems: food enhances diversity and growth of suspension feeders despite available space. Ecology 96:819–827. https://doi.org/10.1890/14-0665.1
Szczebak JT, Henry RP, Al-Horani FA, Chadwick NE (2013) Anemonefish oxygenate their anemone hosts at night. J Exp Biol 216:970–976. https://doi.org/10.1242/jeb.075648
Thornhill DJ, Xiang Y, Pettay DT, Zhong M, Santos SR (2013) Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 22:4499–4515. https://doi.org/10.1111/mec.12416
Wang J, Douglas AE (1998) Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis? J Exp Biol 201:2445–2453
Weis VM (1991) The induction of carbonic anhydrase in the symbiotic sea anemone Aiptasia pulchella. Biol Bull 180:496–504. https://doi.org/10.2307/1542351
Wulff JL (2004) Sponges on mangrove roots, Twin Cays, Belize: early stages of community assembly. Atoll Res Bull. https://doi.org/10.5479/si.00775630.519.1
Wulff J (2017) Bottom-up and top-down controls on coral reef sponges: disentangling within-habitat and between-habitat processes. Ecology 98:1130–1139. https://doi.org/10.1002/ecy.1754
Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694. https://doi.org/10.1111/j.1365-3040.2008.01802.x
Acknowledgements
We thank Will Ballentine, Kate Hill, Katie Kaiser, Jessica Sandelli, Andrea Schmidt, and Kelly Vasbinder for assistance with fieldwork. They made this work wonderbar. We thank the Keys Marine Laboratory for housing and laboratory space while working at our field site. We thank Dr. Joseph Travis for allowing us to use his aquaria and his laboratory, Dr. Thomas Miller for use of his laboratory, and Dr. Scott Burgess for his advice on our experimental design. We thank Genevieve Bernatchez, Laura Elsberry, and Amy Henry for their comments and suggestions on the manuscript as well as five anonymous reviewers that greatly improved the final manuscript. This research was supported by the John Mark Caffrey Endowed Scholarship (to S. Bedgood) and the Florida State University Mentored Research and Creative Endeavors Award (to S. Bedgood).
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The authors declare that they have no conflicts of interest. This research was made possible through funding provided by the John Mark Caffrey Endowed Scholarship (to S. Bedgood) and the Florida State University Mentored Research and Creative Endeavors Award (to S. Bedgood). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Bedgood, S.A., Bracken, M.E.S., Ryan, W.H. et al. Nutritional drivers of adult locomotion and asexual reproduction in a symbiont-hosting sea anemone Exaiptasia diaphana. Mar Biol 167, 39 (2020). https://doi.org/10.1007/s00227-020-3649-3
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DOI: https://doi.org/10.1007/s00227-020-3649-3