Abstract
In this experimental study we explore a dominance-subordination network within a key group of polyphagous opportunistic organisms. This study also includes the possible reconfiguration of this network after the arrival of exotic species of the same ecological guild. Intertidal sea anemone species have been used as an experimental model for this purpose. There are a few documented fight-specialized external morphological structures in actiniarians, including acrorhagii and catch-tentacles, which are also accompanied by a more-or-less differentiated endowment of cnidocysts. Although it is possible to identify an old immigrant in the native dominance-subordination network under study, we also explore the hypothetical arrival of an exotic population of a pantropical sea anemone species, and its effects on the current set of interactions. In this community we detected the presence of the alien species Diadumene lineata (= Haliplanella lineata, = H. luciae) of Pacific origin, which is considered to be a relatively old immigrant in European waters. Exaiptasia pallida (= Aiptasia pallida, among other synonyms), with a worldwide warm-tropical distribution, is here used experimentally as a second invasive alien. A simple Competitive Efficiency index (CEi) is proposed in order to quantify the competitive capacities of these species. The CEi of a given species is based on the percentage of conflicts won, lost, tied, and mutually avoided. Our results demonstrate how alien species can re-organize the hierarchy and dominance-subordination relationships in an established network of interactions, even considering the possible ecological substitution of natives by alien species which are ecologically equivalent (but not identical in their relationships).
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References
Anderluh G, Macek P (2002) Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 40:111–124
Anderluh G, Krizaj I, Strukelj B, Gubensek F, Macek P, Pungercar J (1999) Equinatoxins, pore-forming proteins from the sea anemone Actinia equina, belong to a multigene family. Toxicon 37:1391–1401
Andrews PLR (2011) Laboratory invertebrates: only spineless, or spineless and painless? ILAR J 52:121–125
Ayre DJ (1982) Inter-genotype aggression in the solitary sea anemone Actinia tenebrosa. Mar Biol 68:199–205
Ayre DJ (1983) The effects of asexual reproduction and inter-genotypic aggression on the genotypic structure of populations of the sea anemone Actinia tenebrosa. Oecologia 57:158–165
Bigger CH (1976) The acrorhagial response in Anthopleura krebsi: intraspecific and interspecific recognition. In: Mackie GO (ed) Coelenterate ecology and behaviour. Plenum Press, New York, pp 127–136
Bigger CH (1980) Interspecific and intraspecific acrorhagial aggressive behaviour among sea anemones: a recognition of self and not-self. Biol Bull Mar Biol Lab Woods Hole 159:117–134
Biro PA, Beckmann C, Stamps JA (2010) Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc R Soc B 277:71–77
Biro PA, O’Connor J, Pedini L, Gribben PE (2013) Personality and plasticity: consistent responses within-, but not across-temperature situations in crabs. Behaviour 150:799–811
Brace RC, Pavey J (1978) Size-dependent dominance hierarchy in the anemone Actinia equina. Nature 273:752–753
Brace RC, Pavey J, Quicke DLJ (1979) Intraspecific aggression in the colour morphs of the anemone Actinia equina: the ‘Convention’ governing dominance ranking. Anim Behav 27:553–561
Briffa M, Bridger D, Biro PA (2013) How does temperature affect behaviour? Multilevel analysis of plasticity, personality and predictability in hermit crabs. Anim Behav 86:47–54
Briffa M, Sneddon LU, Wilson AJ (2015) Animal personality as a cause and consequence of contest behaviour. Biol Lett 11:20141007
Brooks WR (1988) The influence of the location and abundance of the sea anemone Calliactis tricolor (Le Sueur) in protecting hermit crabs from octopus predator. J Exp Mar Biol Ecol 116:15–21
Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81(5):1225–1239
Carlgren O (1949) A survey of the Ptychodactiaria, Corallimorpharia and Actiniaria. K Sven Vetensk Handl 1(1):1–121
Chadwick NE (1987) Interspecific aggressive behaviour of the corallimorpharian Corynactis californica (Cnidaria: Anthozoa): effects on sympatric corals and sea anemones. Biol Bull 173:110–125
Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Salai OE, Hobbie SE, Mack MC, Díaz S (2000) Consequences of changing biodiversity. Nature 405:234–242
Connell JH (1980) Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35:131–138
Daly M (2003) The anatomy, terminology, and homology of acrorhagi and pseudoacrorhagi in sea anemones. Zool Verh Leiden 345:89–101
Daly M, Brugler MR, Cartwright P, Collins AG, Dawson MN, Fautin DG, France SC, Mcfadden CS, Opresko DM, Rodríguez E, Romano SL, Stake JL (2007) The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668:127–182
Den Hartog JC, Ates RML (2011) Actiniaria from Ria de Arosa, Galicia, northwestern Spain, in the Netherlands Centre for Biodiversity Naturalis, Leiden. Zool Med Leiden 85(2):11–53
Dorsett DA, Turner R (1986) Colour-morph dominance and avoidance responses of Anemonia sulcata. Mar Behav Physiol 12:115–123
Edmunds M, Potts GW, Swinfen RC, Waters VL (1976) Defensive behaviour of sea anemones in response to predation by the opisthobranch mollusc Aeollidia papilosa (L.). J Mar Biol Ass UK 56:65–83
Elias-Piera F, Rossi S, Gili JM, Orejas C (2013) Trophic ecology of seven Antarctic gorgonian species through stable isotope and biochemical analysis. Mar Ecol Prog Ser 477:93–106
Elton CS (2000) The ecology of invasions by animal and plants. Methuen, London
Elwood RW (2011) Pain and suffering in invertebrates? ILAR J 52:175–184
Escribano-Álvarez P, López-González PJ (2015) Second record of the Indo-Pacific nudibranch Polycera hedgpethi from Atlantic European waters (Gastropoda, Nudibranchia, Polyceridae). Mar Biodivers Rec 8:e127
Fautin DG (1988) Anthozoan dominated benthic environments. In: Proc 6th Int. Coral Reefs Symp, vol. 3
Fautin DG (2009) Structural diversity, systematic, and evolution of cnidae. Toxicon 54:1054–1064
Ferriz-Domínguez N, Horta-Puga G (2001) Short-term aggressive behaviour in scleractinian corals from La Blanquilla reef, Veracruz Reef System. Rev Biol Trop 49(1):67–75
Francis L (1973a) Clone specific segregation in the sea anemone Anthopleura elegantissima. Biol Bull Mar Biol Lab Woods Hole 144:64–72
Francis L (1973b) Intraspecific aggression and its effect on the distribution of Anthopleura elegantissima and some related sea anemones. Biol Bull Mar Biol Lab Woods Hole 144:73–92
Francis L (1988) Cloning and aggression among sea anemones (Coelenterata: Actiniaria) of the rocky shore. Biol Bull 174:241–253
Galil BS (2000) A sea under siege—alien species in the Mediterranean. Biol Invasions 2:177–186
Galil BS (2012) Truth and consequences: the bioinvasion of the Mediterranean Sea. Int Zool 7:299–311
Galil BS, Zenetos A (2002) A sea change—exotics in the eastern Mediterranean. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer Academic Publishers, Dordrecht, pp 325–336
Galil BS, Boero F, Campbell ML et al (2015) ‘Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea. Biol Invasions 17:973–976
Gili JM, Ballesteros E (1991) Structure of mediterranean cnidarian populations in sublittoral benthic communities as a result of adaptation to different environmental conditions. Oecol Aquat 10(243):254
Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13:316–321
González-Duarte MM, Megina C, López-González PJ, Galil B (2016) Cnidarian Alien species in expansion. In: Goffredo S, Dubinsky Z (eds) The cnidaria, past, present and future. Springer International Publishing, Switzerland, pp 139–160
Grajales A, Rodríguez E (2014) Morphological revision of the genus Aiptasia and the family Aiptasiidae (Cnidaria, Actiniaria, Metridioidea). Zootaxa 3826(1):55–100
Häussermann V, Spano C, Thiel M, Lohrmann KB (2015) First record of the sea anemone Diadumene lineata (Verrill, 1869) from the Chilean coast. Spixiana 38(1):39–42
Hazlett BA (1981) The behavioral ecology of hermit crabs. Ann Rev Ecol Syst 12:1–22
Helmuth B, Broitman BR, Blanchette CA, Gilman S, Halpin P, Harley CDG, O’Donell MJ, Hofmann GE, Menge B, Strickland D (2006) Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change. Ecol Monogr 76(4):461–479
Herbold B, Moyle PB (1986) Introduced species and vacant niches. Am Nat 128:751–760
Honma T, Minagawa S, Nagai H, Ishida M, Nagashima Y, Shiomi K (2005) Novel peptide toxins from acrorhagi, aggressive organs of the sea anemone Actinia equina. Toxicon 46:768–774
Howe PL, Reichelt-Brushett AJ, Clark MW (2012) Aiptasia pulchella: a tropical cnidarian representative for laboratory ecotoxicological research. Environ Toxicol Chem 31:2653–2662
Jackson JBC (1977) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am Nat 111:743–767
Johnson LK, Hubbell SP (1974) Aggression and competition among stingless bees: field studies. Ecology 55:120–127
Jousson O, Pawlowski J, Zaninetti L, Meinesz A, Boudouresque CF (1998) Molecular evidence for the aquarium origin of the green alga Caulerpa taxifolia introduced to the Mediterranean Sea. Mar Ecol Prog Ser 172:275–280
Kass-Simon G, Scappaticci AA AA Jr (2002) The behavioural and developmental physiology of nematocyst. Can J Zool 80:1772–1794
Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Bioddiversity as a barrier to ecological invasion. Nature 417:636–638
Lange RG, Dick MH, Müller WA (1992) Specificity and early ontogeny of historecognition in the hydroid Hydractinia. J Exp Zool 262:307–316
Lathlean JA, Ayre DJ, Minchinton TE (2011) Rocky intertidal temperature variability along the southeast coast of Australia: comparing data from in situ loggers, satellite-derived SST and terrestrial weather stations. Mar Ecol Prog Ser 469:83–95
Logan A (1984) Interspecific aggression in hermatypic corals from Bermuda. Coral Reefs 3:131–138
Manuel RL (1981) British Anthozoa (Coelenterata: Octocorallia & Hexacorallia). EJ Brill/Dr. Backhuys, Leiden
McLean RB, Mariscal RN (1973) Protection of hermit crab by its symbiotic sea anemone Calliactis tricolor. Experientia 29:128–130
Meinesz A, Belsher T, Thibaut T, Antolic B, Mustapha KB, Boudouresque C-F, Chiaverini D, Cinelli F, Cottalorda JM, Djellouli A, El Abel A, Orestano C, Grau AM, Ivesa L, Jaklin A, Langar H, Massuti-Pascual E, Peirano A, Tunesi L, de Vaugelas Jean, Zavodnik N, Zuljevic A (2001) The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol Invasions 3:201–210
Menge BA, Sutherland JP (1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am Nat 110:351–369
Mercier JL, Lenoir A, Dejean A (1997) Ritualised versus aggressive behaviours displayed by Polyrhachis laboriosa (F. Smith) during intraspecific competition. Behav Proc 41:39–50
Molina LM, Valiñas MS, Pratolongo PD, Elias R, Perillo GME (2009) First record of the sea anemone Diadumene lineata (Verrill 1871) associated to Spartina alterniflora roots and stems, in marshes at the Bahia Blanca estuary, Argentina. Biol Invasions 11:409–416
Müller WE, Maidhof A, Zahn RK, Müller I (1983) Histoincompatibility reactions in the hydrocoral Millepora dichotoma. Coral Reefs 1:237–241
Müller WE, Müller I, Zahn RK, Maidhof A (1984) Intraspecific recognition system in scleractinian corals: morphological and cytochemical description of the autolysis mechanism. J Histochem Cytochem 32:285–288
Ottaway JR (1978) Population ecology of the intertidal anemone Actinia tenebrosa I. Pedal locomotion and instraspecific aggression. Aust J Mar Freshw Res 29(6):787–802
Palaoro AV, Velasque M, Santos S, Briffa M (2017) How does environment influence fighting? The effects of tidal flow on resource value and fighting costs in sea anemones. Biol Lett 13:20170011
Palaoro AV, Briffa M (2017) Weaponry and defenses in fighting animals: how allometry can alter predictions from contest theory. Behav Ecol 28(1):328–336
Podbielski I, Bock C, Lenz M, Melzner F (2016) Using the critical salinity (Scrit) concept to predict invasion potential of the anemone Diadumene lineata in the Baltic Sea. Mar Biol 163:227
Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330
Purcell JE (1977) Aggressive function and induced development of catch tentacles in the sea anemone Metridium senile (Coelenterata, Actiniaria). Biol Bull 153:355–368
Purcell JE, Kitting CL (1982) Intraspecific aggression and population distributions of the sea anemone Metridium senile. Biol Bull 162:345–359
Rinkevich B, Loya Y (1985) Intraspecific competition in a reef coral: effects on growth and reproduction. Oecologia 66:100–105
Rodríguez E, Barbeitos MS, Brugler MR, Crowley LM, Grajales A, Gusmao L, Häussermann V, Reft A, Daly M (2013) Hidden among sea anemones: the first comprehensive phylogenetic reconstruction of the order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) reveals a novel group of hexacorals. PLoS ONE 9:1–17
Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when and why these impacts occur. Biol Invasions 8:927–939
Ross DM (1967) Behavioural and ecological relationships between sea anemones and other invertebrates. Oceanogr Mar Biol Ann Rev 5:291–316
Ross DM (1971) Protection of hermit crabs (Dardanus spp.) from octopus by commensal sea anemones (Calliactis spp.). Nature 230:401–402
Ross DM (1979) A third species of swimming actinostolid (Anthozoa: Actiniaria) on the Pacific Coast of North America? Can J Zool 57:943–945
Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417
Rudin FS, Briffa M (2011) The logical polyp: assessments and decisions during contests in the beadlet anemone Actinia equina. Behav Ecol 22:1278–1285
Rudin FS, Briffa M (2012) Is boldness a resource-holding potential trait? Fighting prowess and changes in startle response in the sea anemone, Actinia equina. Proc R Soc B 279:1904–1910
Sammarco PW, Coll JC (1992) Chemical adaptations in the Octocorallia: evolutionary considerations. Mar Ecol Prog Ser 88:93–104
Sammarco PW, Coll JC, La Barre S (1985) Competitive strategies of soft corals (Coelenterata: Octocoralia) II. Variable defensive responses and susceptibility to scleractinian corals. J Exp Mar Biol Ecol 91:199–215
Sánchez JA, Díaz JM, Zea S (1997) Gorgonian communities in two contrasting environments on oceanic atolls of the southwestern Caribbean. Bull Mar Sci 61:453–465
Schmidt H (1972) Podromus zu einer monographie der mediterranen aktinien. Zoologica 42:1–146
Sebens KP (1984) Agonistic behaviour in the intertidal sea anemone Anthopleura xanthogrammica. Biol Bull 166:457–472
Sheppard CRC (1979) Interspecific aggression between reef corals with reference to their distribution. Mar Ecol Prog Ser 1:237–247
Shick JM (1991) A functional biology of sea anemones. Functional Biology Series. Springer, Dordrech
Simberloff D, Dayan T (1991) The guild concept and the structure of ecological communities. Annu Rev Ecol Syst 22:115–143
Smith JA (1991) A question of pain in invertebrates. ILAR News 33(1–2):25–31
Smith JM, Parker G (1976) The logic of asymmetric contests. Anim Behav 24:159–175
Stachowicz JJ, Whitlatch BB, Osman RW (1994) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579
Tanner JE (1997) Interspecific competition reduces fitness in scleractinian corals. J Exp Mar Biol Ecol 214:19–34
Turner VLG, Lynch SM, Paterson L, León-Cortés JL, Thorpe JP (2003) Aggression as a function of genetic relatedness in the sea anemone Actinia equina (Anthozoa: Actiniaria). Mar Ecol Prog Ser 247:85–92
Walther G, Roques A, Hulme PE, Sykes MT, Pysek P, Kühn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H, Czúcz B, Dauber J, Hickler T, Jarosík V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilà M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24:686–693
Williams RB (1975) Catch-tentacles in sea anemones: occurrence in Haliplanella luciae (Verrill) and a review of current knowledge. J Nat His 9:241–248
Williams RB (1978) Some recent observations on the acrorhagi of sea anemones. J Mar Biol Ass UK 58:787–788
Williams RB (1991) Acrorhagi, catch tentacles and sweeper tentacles: a synopsis of ‘aggression’ of actiniarian and scleractinian cnidaria. Hydrobiologia 216(217):539–545
Woodin SA, Jackson JBC (1979) Interphyletic competition among marine benthos. Am Zool 19:1029–1043
Acknowledgements
We thank Dr. César Megina for logistical assistance during the elaboration of this study. Special thanks to Lucía Paniagua for illustrating sea anemone behaviors for this paper, as well as to the colleagues of the research team Biodiversidad y Ecología de Invertebrados Marinos of the Universidad de Sevilla for their assistance during the laboratory work and for the encouragement received during this study. We also thank the specialized stores in tropical marine fauna “Planeta Reef” and “Hobby Zoo” that kindly provided the specimens of Exaiptasia pallida for the experimental designs carried out in this study. This research benefited from discussions among the research team, infrastructures and sampling trips carried out during the Project RNM-744 “Conexiones entre poblaciones de corales en el entorno del Estrecho de Gibraltar y mar de Alborán. Evaluación de riesgos para un endemismo mediterráneo (Astroides calycularis) por la presencia y expansión de especies de corales exóticos. (CORAL)” funded by the Regional Governmental Agency “Consejería de Economía, Innovación, Ciencia y Empleo (Junta de Andalucía)”. The authors would like to thank the Editors and two anonymous reviewers for useful comments and criticisms on the first draft of this paper. Finally, we thank Mr. Tony Krupa for reviewing the English version.
Funding
Partial support (aquaria systems and sampling trips) was provided by the Spanish Regional Governmental Agency “Consejería de Economía, Innovación, Ciencia y Empleo (Junta de Andalucía)” to the Project RNM-744 “CORAL”.
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10530_2018_1748_MOESM1_ESM.docx
Table of variations of the Competitive Efficiency index (CEi) according to the different global results in the interactions (in %) (DOCX 14 kb)
10530_2018_1748_MOESM2_ESM.wmv
Interaction between Actinothoe sphyrodeta (smaller individual on the left) and Bunodactis rubripunctata (larger individual on the right). Although the maximum experimental time was 60 min, this contest was resolved in ca. 12 min. The original video footage has not been edited, just accelerated 64x for observation(WMV 14204 kb)
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Escribano-Álvarez, P., López-González, P.J. Facing the arrival of newcomers: an intertidal sea anemone approach (Hexacorallia, Actiniaria). Biol Invasions 20, 2945–2962 (2018). https://doi.org/10.1007/s10530-018-1748-6
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DOI: https://doi.org/10.1007/s10530-018-1748-6