Skip to main content

Advertisement

Log in

Taking a detour: invasion of an octocoral into the Tropical Eastern Pacific

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The tropical snowflake octocoral Carijoa riisei, which is thought to be native to the Indo-Pacific biogeographical region, has been increasingly reported from the Colombian Tropical Eastern Pacific (TEP) over the past two decades. Massive mortalities of native octocorals, particularly in Pacifigorgia spp. and Muricea spp., were observed due to C. riisei overgrowth. However, the area of origin of TEP C. riisei remains unknown and its potential invasive status has not been addressed yet. We evaluated geographical scenarios for the colonization of the Colombian TEP by conducting phylogeographical analyses based on nuclear and mitochondrial sequences of 306 individual specimens from across the species’ (native/non-native) range and applying hypothesis-specific operational criteria. Additionally, we assessed whether C. riisei has to be considered an invasive species based on the previously proposed ‘unified framework for biological invasions’. Our results showed relatively high genetic differentiation between Colombian TEP populations, on the one side, and Indo-Pacific and Hawaiian populations, on the other side. In contrast, we could not identify genetic differentiation and significant isolation by distance (IBD) between Colombian TEP and Tropical Atlantic populations. C. riisei might have been introduced from the Atlantic into the Colombian TEP, possibly via the Panama Canal. Based on the criteria of the ‘unified framework for biological invasions’, we also conclude that this octocoral constitutes an invasive species. Our study may serve as a basis for establishing strategies to protect native species from one of the very few invasive coral species worldwide.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baez Espinosa AS (2015) Diversidad de macro invertebrados asociados a los octocolares en el islote el Pelado “Bajo la pared”, Ayangue-Ecuador. Dissertation, Universidad Estatal Peninsula de Santa Elena

  • Barbosa TM, Gomes PB, Bergeron AS, Santos AM et al (2014) Comparisons of sexual reproduction in Carijoa riisei (Cnidaria, Alcyonacea) in South Atlantic, Caribbean, and Pacific areas. Hydrobiologia 734:201–212

    Article  CAS  Google Scholar 

  • Barrero-Canosa J, Dueñas LF, Sánchez JA (2013) Isolation of potential fungal pathogens in gorgonian corals at the Tropical Eastern Pacific. Coral Reefs 32:35–41

    Article  Google Scholar 

  • Baums IB, Boulay JN, Polato NR, Hellberg ME (2012) No gene flow across the Eastern Pacific Barrier in the reef-building coral Porites lobata. Mol Ecol 21:5418–5433

    Article  PubMed  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Birkeland C, Meyer DL, Stames JP, Buford CL (1975) Subtidal communities of Malpelo Island. In: Graham JB (ed) The biological investigation of Malpelo Island, Colombia. Smithsonian contributions to zoology, vol 176, pp 55–68

  • Blackburn TM, Pysek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339

    Article  PubMed  Google Scholar 

  • Budd AF, Johnson KG, Stemann TA (1996) Plio- Pleistocene turnover and extinctions in the Caribbean Reef-Coral Fauna. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. University of Chicago, Chicago, pp 168–204

    Google Scholar 

  • Calcinai B, Bavestrello G, Cerrano C (2004) Dispersal and association of two alien species in the Indonesian coral reefs: the octocoral Carijoa riisei and the demosponge Desmapsamma anchorata. J Mar Biol Assoc UK 84:937–941

    Article  Google Scholar 

  • Carlton JT (1987) Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bull Mar Sci 41:452–465

    Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Carlton JT, Newman WA, Pitombo FB (2011) Barnacle invasions: introduced, cryptogenic, and range expanding Cirripedia of North and South America. In: Galil BS, Clark PF, Carlton JT (eds) In the wrong place—alien marine crustaceans: distribution, biology and impacts, vol 6. Springer series in invading ecology. Springer, Dordrecht, pp 159–213

    Chapter  Google Scholar 

  • Chen H, Strand M, Norenburg JL, Sun S, Kajihara H et al (2010) Statistical parsimony networks and species assemblages in cephalotrichid nemerteans (Nemertea). PLoS ONE 5:e12885. doi:10.1371/journal.pone.0012885

    Article  PubMed  PubMed Central  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a compute program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Coffroth MA, Lasker HR, Diamond ME, Bruenn JA, Bermingham E (1992) DNA fingerprints of a gorgonian coral: a method for detecting clonal structure in a vegetative species. Mar Biol 114:317–325

    Article  CAS  Google Scholar 

  • Cohen A (2006) Species introductions and the Panama Canal. In: Gollasch S, Galil BS, Cohen A (eds) Bridging divides: maritime canals as invasion corridors monographie biologicae, vol 83. Springer, Dordrecht, pp 127–206

    Chapter  Google Scholar 

  • Coles SL, Eldredge LG (2002) Nonindigenous species introductions on coral reefs: a need for information. Pac Sci 56:191–209

    Article  Google Scholar 

  • Combosch DJ, Guzman HM, Schuhmacher H, Vollmer SV (2008) Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Mol Ecol 17:1304–1312

    Article  CAS  PubMed  Google Scholar 

  • Concepcion GT, Crepeau MW, Wagner D et al (2008) An alternative to ITS, a hypervariable, single-copy nuclear intron in corals, and its use in detecting cryptic species within the octocoral genus Carijoa. Coral Reefs 27:323–336

    Article  Google Scholar 

  • Concepcion GT, Kahng S, Crepeau M et al (2010) Resolving natural ranges and marine invasions in a globally distributed octocoral (genus Carijoa). Mar Ecol Prog Ser 401:113–127

    Article  Google Scholar 

  • Cortes J (1997) Biology and geology of eastern Pacific coral reefs. Coral Reefs 16:S39–S46

    Article  Google Scholar 

  • Dana TF (1975) Development of contemporary eastern Pacific coral reefs. Mar Biol 33:355–374

    Article  Google Scholar 

  • De Barro P, Ahmed M (2011) Genetic networking of the Bemisia tabaci cryptic species complex reveals pattern of biological invasions. PLoS ONE 6:e25579. doi:10.1371/journal.pone.0025579

    Article  PubMed  PubMed Central  Google Scholar 

  • Duchassaing P, Michelotti J (1860) Mémoire sur les coralliaires des Antilles. Imprimerie Royale, Turin, p 89

    Google Scholar 

  • Edgar RC, Drive RM, Valley M (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ekman S (1953) Zoogeography of the sea. Sidgwick and Jackson, London, p 417

    Google Scholar 

  • Evans ECI, Buske NL, Grovhoub JG, Guinther EB et al (1974) Pearl Harbor biological survey—final report. Naval Undersea Center Rep. No. NUC TN 1128. San Diego

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Google Scholar 

  • Ferreira CE, Goncçalves JE, Coutinho R (2001) Community structure of fishes and habitat complexity on a tropical rocky shore. Environ Biol Fishes 61:353–369

    Article  Google Scholar 

  • Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782

    Article  CAS  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glynn PW, Ault JS (2000) A biogeographic analysis and review of the far eastern Pacifc coral reef region. Coral Reefs 19:1–23

    Article  Google Scholar 

  • Glynn PW, Colgan MW (1992) Sporadic disturbances in fluctuating coral reef environments: El Niño and coral reef development in the eastern Pacific. Am Zool 32:707–718

    Article  Google Scholar 

  • Goldberg J, Wilkinson C (2004) Global threats to coral reefs: coral bleaching, global climate change, disease, predator plagues, and invasive species. In: Wilkinson C (ed) Status of coral reefs of the world, vol 1. Australian Institute of Marine Science, Townsville, pp 67–92

    Google Scholar 

  • Gomes PB, Lira AK, Naud JP, Santos AM, Pérez CD (2012) Prey selectivity of the octocoral Carijoa riisei at Pernambuco, Brazil. An Acad Bras Ciênc 84:157–164

    Article  PubMed  Google Scholar 

  • Gomez C, Guzman HM, Gonzalez A, Breedy O (2014) Survival, growth, and recruitment of octocoral species (Coelenterata: Octocorallia) in Coiba National Park, Pacific Panama. Bull Mar Sci 90:623–650

    Article  Google Scholar 

  • Grapputo A, Boman S, Lindström L et al (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14:4207–4219

    Article  CAS  PubMed  Google Scholar 

  • Grigg RW (2003) Invasion of a deep black coral bed by an alien species, Carijoa riisei, off Maui, Hawaii. Coral Reefs 22:121–122

    Article  Google Scholar 

  • Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Let 3:509–512

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Kahng SE (2005) Localization of fluorescent pigments in a nonbioluminescent, azooxanthellate octocoral suggests a photoprotective function. Coral Reefs 24:435

    Article  Google Scholar 

  • Kahng SE, Grigg RW (2005) Impact of an alien octocoral, Carijoa riisei, on black corals in Hawaii. Coral Reefs 24:556–562

    Article  Google Scholar 

  • Larsson A (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30:3276–3278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leydet KP, Hellberg ME (2015) The invasive coral Oculina patagonica has not been recently introduced to the Mediterranean from the western Atlantic. BMC Evol Biol 15:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lira AKF, Naud JP, Gomes PB et al (2009) Trophic ecology of the octocoral Carijoa riisei from littoral of Pernambuco, Brazil. I. Composition and spatio-temporal variation of the diet. J Mar Biol Assoc UK 89:89–99

    Article  Google Scholar 

  • Madariaga DJ, Rivadeneira MM, Tala F, Thiel M (2014) Environmental tolerance of the two invasive species Ciona intestinalis and Codium fragile: their invasive potential along a temperate coast. Biol Invasions 16:2507–2527

    Article  Google Scholar 

  • Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846

    Article  PubMed  Google Scholar 

  • Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233

    Article  Google Scholar 

  • Neusser TP, Jörger KM, Schrödl M (2011) Cryptic species in tropic sands-interactive 3D anatomy, molecular phylogeny and evolution of meiofaunal Pseudunelidae (Gastropoda, Acochlidia). PLoS ONE 6:e23313. doi:10.1371/journal.pone.0023313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noguerales V, Cordero PJ, Ortego J (2016) Hierarchical genetic structure shaped by topography in a narrow-endemic montane grasshopper BCM. Evol Biol 16:96

    Google Scholar 

  • Okada M, Grewell BJ, Jasieniuk M (2009) Clonal spread of invasive Ludwigia hexapetala and L. grandiflora in freshwater wetlands of California. Aquat Bot 91:123–129

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R et al (2017) vegan: community ecology package, version. R package version 2.4. http://CRAN.R-project.org/package=vegan

  • Padmakumar K, Chandran R, Kumar JSY, Sornaraj R (2011) Carijoa riisei (Cnidaria: Octocorallia: Clavulariidae), a newly observed threat to Gulf of Mannar coral biodiversity? Curr Sci 100:35–37

    Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E et al (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Prabhukumar KM, Sreejith PE, Prasad MG et al (2015) Snowflake coral, Carijoa riisei from Grand Island, Goa: a case of invasion of an alien species or re-establishment of a native species? Curr Sci 109:1028–1030

    Google Scholar 

  • R Development Core Team (2016): R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org (accessed March 2017)

  • Raghunathan C, Venkataraman K, Satyanarayana C et al (2013) An invasion of snowflake coral Carijoa riisei (Duchassaing and Michelotti 1860) in Indian seas: threats to coral reef ecosystem. In: Venkataraman K et al (eds) Ecology and conservation of tropical marine faunal communities. Springer, Berlin, pp 381–393

    Chapter  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  PubMed  Google Scholar 

  • Robertson DR, Grove JS, Mccosker JE (2004) Tropical transpacific shore fishes. Pac Sci 58:507–565

    Article  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sánchez JA (1994) Presencia de los octocorales Stylatula diadema Bayer (Pennatulacea) y Carijoa riisei (Duchassaing y Michelotti) (Telestacea) en la costa Caribe suroccidental, Colombia. Anales del Instituto de Investigaciones Marinas de Punta de Betín 23:137–147

    Google Scholar 

  • Sánchez JA, Ballesteros D (2014) The invasive snowflake coral (Carijoa riisei) in the Tropical Eastern Pacific, Colombia. Rev Biol Trop 62:197–207

    Google Scholar 

  • Sánchez JA, McFadden CS, France SC, Lasker HR (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987

    Article  Google Scholar 

  • Sánchez JA, Gómez CE, Escobar D, Dueñas LF (2011) Diversidad, abundancia y amenazas de los octocorales de la isla Malpelo, Pacifico Oriental Tropical, Colombia. Revista de Investigaciones Marinas Costeras 40:139–154

    Google Scholar 

  • Sánchez JA, Ardila NE, Andrade J et al (2014) Octocoral densities and mortalities in Gorgona Island, Colombia, Tropical Eastern Pacific. Rev Biol Trop 62:209–219

    Article  Google Scholar 

  • Spalding MD, Fox HE, Allen GR, Davidson N et al (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583

    Article  Google Scholar 

  • Stefaniak L, Zhang H, Gittenberger A et al (2012) Determining the native region of the putatively invasive ascidian Didemnum vexillum Kott, 2002. J Exp Mar Biol Ecol 422–423:64–71

    Article  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens M et al (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas WJ (1979) Aspects of the microcommunity associated with Telesto riisei, an introduced alcyonarian species. Dissertation, University of Hawaii at Manoa

  • Vargas-Angel B (1996) Distribution and community structure of the reef corals of Ensenada de Utría, Pacific coast of Colombia. Rev Biol Trop 44:627–635

    Google Scholar 

  • Wagner D, Kahng SE, Toonen RJ (2009) Observations on the life history and feeding ecology of a specialized nudibranch predator (Phyllodesmium poindimiei), with implications for biocontrol of an invasive octocoral (Carijoa riisei) in Hawaii. J Exp Mar Biol Ecol 372:64–74

    Article  Google Scholar 

  • Wood S, Baums IB, Paris CB et al (2016) El Niño and coral larval dispersal across the Eastern Pacific marine barrier. Nat Commun 7:12571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xavier R, Santos AM, Lima FP, Branco M (2009) Invasion or invisibility: using genetic and distributional data to investigate the alien or indigenous status of the Atlantic populations of the peracarid isopod, Stenosoma nadejda (Rezig 1989). Mol Ecol 18:3283–3290

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Fonseca DM, Hamilton GC et al (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions 16:153–166

    Article  CAS  Google Scholar 

  • Zapata FA, Vargas-Angel B (2003) Corals and coral reefs of the Pacific coast of Colombia. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 419–447

    Chapter  Google Scholar 

  • Zapata FA, Rodríguez-Ramírez A, Caro-Zambrano C, Garzón-Ferreira J (2010) Mid-term coral-algal dynamics and conservation status of a Gorgona Island (Tropical Eastern Pacific) coral reef. Rev Biol Trop 58:81–94

    Article  PubMed  Google Scholar 

  • Zeas Valarezo S (2015) Diversidad y abundancia de octocorales en el bajo “La pared”, de la reserva marino costera el Pelado, Ayangue-Ecuador. Dissertation, Universidad Estatal Peninsula de Santa Elena

  • Zhang YY, Zhang DY, Barrett SC (2010) Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Mol Ecol 19:1774–1786

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Fundación Malpelo and Parques Nacionales Naturales (PNN) in Colombia for organizing the expeditions to Malpelo Island, especially Sandra Bessudo and Nancy Murillo for their valuable support. We also thank PNN Gorgona, particularly Ximena Zorrilla and Luis Payán for their cooperation during the field surveys. We are grateful to Javier Torres for its help in sample collection. The help from colleagues and students from Laboratorio de Biología Molecular Marina (BIOMMAR, Universidad de los Andes) during the field and laboratory stages was invaluable, particularly from Lina Gutierrez, Iván Calixto and Natalia Jiménez. We also acknowledge Björn Stelbrink for his constructive comments on the manuscript, the contributions of Arthur Sands, Pauline Gauffre and Alejandro Reyes in the earlier stages of this paper as well as the support from local communities in Cabo Corrientes, Chocó. Finally, we thank two anonymous reviewers that helped us improving the manuscript. This study was funded by COLCIENCIAS (Grant No. 1204-521-29002 to JAS), the Facultad de Ciencias (Universidad de los Andes) and the Center of Excellence in Marine Sciences (CEMarin) in Bogotá.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elena Quintanilla.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Quintanilla, E., Wilke, T., Ramírez-Portilla, C. et al. Taking a detour: invasion of an octocoral into the Tropical Eastern Pacific. Biol Invasions 19, 2583–2597 (2017). https://doi.org/10.1007/s10530-017-1469-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1469-2

Keywords

Navigation