Bioerosion of reef-building crustose coralline algae by endolithic invertebrates in an upwelling-influenced reef


Coral reef growth is primarily determined by constructive and bioerosive processes acting on key reef-building organisms. Among them, corals are major contributors to the construction of reef frameworks, while crustose coralline algae (CCA) primarily take part in reef cementation. Despite the significance of CCA for reef ecology and functioning, there is very little information on CCA bioerosion rates, in particular in reefs influenced by coastal upwelling. Therefore, the aim of this study was to examine the percentage and rates of internal bioerosion by macroborer invertebrates in two dominant CCA species and to explore whether the oceanographic variability influences the nature of bioerosion in coral reefs of the Tayrona Natural National Park (Colombian Caribbean). Annual rates of gross calcium carbonate production for Lithoplyllum kaiseri and Porolithon antillarum were 0.556 (± 0.38) and 0.883 (± 1.0) g CaCO3 cm−2 year−1, respectively, and estimates of percent area covered by macroborer boreholes showed values of 29.7% for L. kaiseri and 18.0% for P. antillarum. Rates of calcium carbonate removal by internal macroborers in L. kaiseri (0.19 ± 0.17 g CaCO3 cm−2 year−1) were higher than those in P. antillarum (0.14 ± 0.17 g CaCO3 cm−2 year−1). The percentage of internal bioerosion did not vary significantly across climatic/oceanographic seasons. Boreholes produced by mollusks, polychaetes, sponges and sipunculids were identified, with mollusks having the highest erosion activity. A total of 2,095 individuals of boring and opportunistic organisms were identified and grouped into 29 families (17 polychaetes, 4 mollusks, 2 sipunculids and 6 crustaceans). The composition of the macroborer invertebrate community also varied between CCA species, with higher boreholes attributed to vermetids in L. kaiseri than in P. antillarum. Although there is no clear influence of climatic seasons on internal bioerosion, the high rates of CCA bioerosion may reduce reef consolidation in the region.

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  1. Andrade CA (2000) The circulation and variability of the colombian basin in the Caribbean Sea. Ph.D. Thesis, University of Wales, Cardiff. 223 p

  2. Andrade C, Barton E (2005) The Guajira upwelling system. Cont Shelf Res 25(13):1629

  3. Andrade CA, Barton ED, C Mooers NK (2003) Evidence for an eastward ow along the Central and South American Caribbean Coast. J Geophys Res 108(C6):3185

  4. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences of the United States of America 105: 17442–17446

  5. Arévalo-Martínez D, Franco-Herrera A (2008) Características oceanográficas de la surgencia frente a la ensenada de Gaira, Departamento del Magdalena, época seca menor de 2006. Boletín de Investigaciones Marinas y Costeras 37:1312–162

  6. Bak R (1976) The growth of the coral colonies and the importance of crustose coralline algae and burrowing sponges in relation of carbonate accumulation. Journal of Sea Research 10:285–337

  7. Barkley HC, Cohen AL, Golbuu Y, Starczak VR, Decarlo TM, Shamberger KEF (2015) Changes in coral reef communities across a natural gradient in seawater pH. Science Advances 1, e1500328

  8. Bayraktarov E, Pizarro V, Eidens C, Wilke T, Wild C (2013) Bleaching susceptibility and recovery of Colombian Caribbean corals in response to water current exposure and seasonal upwelling. PLoS ONE 8(11): e80536

  9. Bayraktarov EV, Pizarro V, Wild C (2014) Spatial and temporal variability of water quality in the coral reefs of Tayrona National Natural Park, Colombian Caribbean. Environmental Monitory and Assessment 186(6):3641–3659

  10. Brock RE, Brock JH (1977) A method for quantitatively assessing the infaunal community in coral rock. Limnology and Oceanography 22:948–951

  11. Bromley RG (1978) Bioerosion of Bermuda reefs. Palaeogeography, Palaeoclimatology, Palaeoecology 23:169–197

  12. Bromley RG, D’Alessandro A (1984) The ichnogenus Entobia from the Miocene, Pliocene and Pleistocene of southern Italy. Rivista Italian Paleontology y Straitagrafia 90: 227–296

  13. Bromley RG, D’Alessandro A (1989) Ichnological study of shallowmarine endolithic sponges form the Italian coast. Rivista Italian Paleontology y Straitagrafia 95: 279–314

  14. Bula-Meyer G (1990) Altas temperaturas estacionales del agua como condición disturbadora de las macroalgas del Parque Nacional Natural Tayrona, Caribe colombiano: una hipótesis. Anales del Instituto de Investigaciones Marinas de Punta de Betín 19-20, 9-21

  15. Carreiro-Silva M, McClanahan TR (2012) Macrobioerosion of dead branching Porites, 4 and 6 years after coral mass mortality. Marine Ecology Progress series 458:103–122

  16. Chave KE, Smith S, Roy K (1972) Carbonate production by coral reefs. Marine Geology 12:123–140

  17. Chazottes V, Le Campion-Alsumard T, Peyrot-Clausade M, Cuet P (2002) The effects of eutrophication-related alterations to coral reef communities on agents and rates of bioerosion (Reunion Island, Indian Ocean). Coral Reefs 21(4):375–390

  18. Chollett I, Mumby PJ, Cortés J (2010) Upwelling areas do not guarantee refuge for coral reefs in a warming ocean. Marine Ecology Progress Series 416: 47–56

  19. Davies PS (1989) Short-term growth measurements of coral using an accurate buoyant weighing technique. Marine Ecology 101(3):389-395

  20. Davies PJ, Hutchings PA (1983) Initial colonization, erosion and accretion on coral substrate: experimental results. Lizard Island Great Barrier Reef. Coral Reefs 2:27–35

  21. Díaz J, Barrios M, Cendales J, Garzón-Ferreira J, Geister M, López G, Ospina F, Parra J, Pinzón B, Vargas F, Zapata S, Sea S (2000) Áreas coralinas de Colombia. Instituto de Investigaciones Marinas, Santa Marta 5:130–136

  22. Diaz-Pulido G, Garzón-Ferreira J (2002) Seasonality in algal assemblages on upwelling-influenced coral reefs in the Colombian Caribbean. Botanica Marina 45:284–292

  23. Diaz-Pulido G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O (2012) Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. Journal of Phycology 48:32-39

  24. Diaz-Pulido G, Nash MC, Anthony KRN, Bender D, Opdyke BN, Reyes-Nivia M, Troitzsch U (2014) Greenhouse conditions induce mineralogical changes and dolomite accumulation in coralline algae on tropical reefs. Nature Communications 5:3310

  25. Dineen JF (1990) Burrowing rates of Lithotrya dorsalis (Cirripedia: Thoracica) in Jamaica. Bulletin of Marine Science 4:656–662

  26. Edinger E, Limmon G, Jompa J, Widjatmoko W, Heikoop J, Risk M (2000) Normal coral growth rates on dying reefs: are coral growth rates good indicators of reef health? Mar Pollut Bull 40:606–617

  27. Eidens C, Bayraktarov E, Hauffe T, Pizarro V, Wilke T, Wild C (2014) Benthic primary production in an upwelling-influenced coral reef, Colombian Caribbean. PeerJ 2, e554

  28. Fajardo G (1979) Surgencia costera en las proximidades de la península colombiana de La Guajira. Boletín Científico CIOH 2:7–19

  29. Fonseca AC, Dean HK, Cortés J (2006) Non-colonial coral macro-borers as indicators of coral reef status in the south Pacific of Costa Rica. Reviste de Biología Tropical 54(1):101–115

    CAS  Article  Google Scholar 

  30. Freiwald A, Henrich R (1994) Reefal coralline algal build-ups within the Arctic Circle: morphology and sedimentary dynamics under extreme environmental seasonality. Sedimentology 41(5):963–984

  31. Gabrielson PW, Hughey JR, Diaz-Pulido G (2018) Genomics reveals abundant speciation in the coral reef building alga Porolithon onkodes (Corallinales, Rhodophyta). Journal of Phycology 54: 429–434

  32. García CB, Salzwedel H (1993) Recruitment patterns of sessile invertebrates onto fouling plates in the bay of Santa Marta, Colombian Caribbean. Anales del Instituto de Investigaciones Marinas de Punta de Betín 22: 30–44

  33. Garzón-Ferreira J (1998) Bahía de Chengue, Parque Natural Tayrona, Colombia. 115-125. In: Kjerfve, B. (Ed.). Caricomp Caribbean coral reef, seagrass and mangrove sites. Coastal Region and Small Islands Papers 3, Unesco, Paris. 82 p

  34. George JD, Hartmann-Schroder G (1985) Polychaetes: British Amphinomida, Spintherida and Eunicida. Synopses of the British Fauna, New Series 32: 1–221.

  35. Gherardi DF, Bosence DW (2001) Composition and community structure of the coralline algal reefs from atoll das Rocas, Brazil. Coral Reefs 19:205–219

  36. Glynn P (1997) Bioerosion and coral reef growth: a dynamic balance. En: Birkeland, C. (ed.) Life and death coral reefs. Chapman and Hall, New York, pp 68–95

  37. Gómez E, Ardila N, Sanjuan-Muñoz A (2013) Sipunculans associated with dead coral skeletons in the Santa Marta region of Colombia, South-Western Caribbean. Journal of the Marine Biological Association of the United Kingdom 93(7):1785–1793

  38. Hepburn LJ, Perry CT, Blanchon P (2005) Distribution of macroborers in reef rubble, Puerto Morelos, Mexican Caribbean. Proc 10th Int Coral Reef Symp 327–334

  39. Hernandez-Kantun JJ, Gabrielson PW, Hughey JR, Pezzolesi L, Rindi F, Robinson NM, Peña V, Riosmena-Rodríguez R, Le Gall, Adey WH (2016) Reassessment of branched Lithophyllum spp. (Corallinales, Rhodophyta) in the Caribbean Sea with global implications. Phycology 55: 619–639

  40. Hutchings PA (1974) A preliminary report on the density and distribution of invertebrates living in coral reefs. Proc 2nd Int Coral Reef Symp 2:285–296

  41. Hutchings PA (1986) Biological destruction of coral reefs - A review. Coral Reefs 4:239–252

  42. Hutchings PA (2008) Role of polychaetes in bioerosion of coral substrates. En: Wisshak and Tapanila Current developments in Bioerosion, pp. 249–64

  43. Hutchings PA, Kiene WE, Cunningham RB, Donelly C (1992) Spatial and temporal patterns of non-colonial boring organisms (polychaetes, sipunculans, and bivalve molluscs) in Parites at Lizard Island, Great Barrier Reef. Coral Reefs 11: 23–32

  44. Kiene WE, Hutchings PA (1994) Bioerosion experiments at Lizard Island, Great Barrier Reef. Coral Reefs 13:19–98

  45. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geoscience 1:114–117.

  46. Le Grand HM, Fabricius KE (2011) Relationship of internal macrobioeroder densities in living massive Porites to turbidity and chlorophyll on the Australian Great Barrier Reef. Coral Reefs 30:97–107

  47. Lewis B, Kennedy E, Diaz-Pulido G (2017) Seasonal growth and calcification of a reef-building crustose coralline alga on the Great Barrier Reef. Marine Ecology Progress Series 568:73–86

  48. Londoño-Cruz E, Cantera JR, Toro-Farmer G, Orozco C (2003) Internal bioerosion by macroborers in Pocillopora spp. in the tropical eastern Pacific. Marine Ecology Progress Series 265: 289–295

  49. Macintyre IG (1997) Reevaluating the role of crustose coralline algae in the construction of coral reefs. Proc 8th Int Coral Reef Symp 1: 725–730

  50. Manzello DP, Kleypas JA, Budd DA, Eakin CM, Glynn PW, Langdon C (2008) Poorly cemented coral reefs of the eastern tropical Pacific: Possible insights into reef development in a high-CO2 world. Proc Natl Acad Sci 105: 10450–10455.

  51. Martínez S, Acosta A (2005). Cambio temporal en la estructura de la comunidad coralina del área de Santa Marta – Parque Nacional Natural Tayrona (Caribe colombiano). Boletín de Investigaciones Marinas y Costeras 34:161–191

  52. Milazzo M, Rodolfo-Metalpa R, Chan VB, Fine M, Alessi C, Thiyagarajan V, HallSpencer J, Chemello R (2014) Ocean acidification impairs vermetid reef recruitment. Science Report 4(4189):1–7

  53. Moreno-Forero S, Navas G, Solano O (1998) Crytobiota associated to dead Acropora palmata (Scleractinia: Acroporidae) coral, Isla Grande, Colombian Caribbean. Revista de Biología Tropical 46(2):229–236

  54. Nash MC, Diaz-Pulido G, Harvey AS, Adey WH (2019) Coralline algal calcificatios: a morphological and process-based understanding. PLoS One 14, e0221396

  55. Neumann AC (1966) Observations on coastal erosion in Bermuda and measurements of the boring rate of the sponge, Cliona lampa. Limnol Oceanogr 11:92–108

  56. Osorno A, Peyrot-Clausade M, Hutchings PA (2005) Patterns and rates of erosion in dead Porites across the Great Barrier Reef, Australia after 2 and 4 years of exposure. Coral Reefs 24:292–303

  57. Pari N, Peyrot-Clausade M, Le Campion-Alsumard T, Hutchings PA, Chazottes V, Golubic S, Le Campion J, Fontaine MF (1998) Bioerosion of experimental substrates on high islands and atoll lagoons (French Polynesia) after two years of exposure. Marine Ecology Progress Series 166:119–130

  58. Perry CT (1996) Distribution and Abundance of Macroborers in an Upper Miocene Reef System, Mallorca, Spain: Implications for Reef Development and Framework Destruction. PALAIOS 11(1): 40

  59. Perry CT, Edinger EN, Kench PS, Murphy GN, Smithers SG, Steneck RS, Mumby P (2012) Estimating rates of biologically driven coral reef framework production and erosion: a new census-based carbonate budget methodology and applications to the reefs of Bonaire. Coral Reefs 31:853–868

  60. Peyrot-Clausade M, Hutchings PA, Richard G (1992) The distribution and successional patterns of macroborers in marine Porites at different stages of degradation on the barrier, Tiahura, Moorea, French Polynesia. Coral Reefs 11: 161–166

  61. Prahl H, Erhardt H (1985). Colombia: Corales y Arrecifes coralinos. FEN, Bogotá. 295 p.

  62. Reyes-Nivia C, Diaz-Pulido G, Kline D, Guldberg OH, Dove S (2013) Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. Global Change Biology 19: 1919–1929.

  63. Reyes-Nivia M, Diaz-Pulido G, Dove SG (2014) Relative roles of endolithic algae and carbonate chemistry variability in the skeletal dissolution of crustose coralline algae. Biogeosciences 11:4615–4626

  64. Risk M, Heikoop J, Edinger E, Erdmann M (2001) The assessment ‘toolbox’: community-based reef evaluation methods coupled with geochemical techniques to identify sources of stress. Bulletin of Marine Science 69:443–458

  65. Ritson-Williams R, Arnold SN, Paul VJ, and Steneck RS (2014) Larval settlement preferences of Acropora palmata and Montastraea faveolata in response to diverse red algae. Coral Reefs 33:59–66

  66. Rose C, Risk M (1985) Increase in Cliona delitrix infestation of Montastrea cavernosa heads on an organically polluted portion of the Grand Cayman fringing reef: PSZNI. Marine Ecology 6:345–363

  67. Salzwedel H. Müller K (1983) A summary of meteorological and hydrological data from the bay of Santa Marta, Colombian Caribbean. Anales del Instituto de Investigaciones Marinas de Punta de Betín 13:67–83

  68. Sammarco PW (1987) A comparison of some ecological processes on coral reefs of the Caribbean and Great Barrie Reef. En: Birkeland, C. (ed.) Unesco Reports in Marine Science 46:127–166

  69. Savazzi E (1999) Cemented and Embedded Gastropods. En: Savazzi, E. (ed.) Functional Morphology of the Invertebrate Skeleton. John Wiley and Sons Ltd., Chichester pp. 183–195

  70. Savazzi E (2001) Morphodynamics of an endolithic vermetid gastropod. Paleontological Research, 5:3–11

  71. Spotorno-Oliveira P, Figueiredo MAO, Tâmega FTS (2015) Coralline algae enhance the settlement of the vermetid gastropod Dendropoma irregulare (d’Orbigny, 1842) in the southwestern Atlantic. Journal Experimental Marine Biology and Ecology 471:137–45

  72. Stearn C, Scoffin T (1977) Carbonate budget of a fringing reef, Barbados. Proc 3rd Int Coral Reef Symp 2:471–476

  73. Steneck RS (1985) Adaptations of crustose coralline algae to herbivory: Patterns in space and time. En: Toomy D, Nitecki M (eds) Paleoalgology, Berlin: Springer Verlagium pp. 352–66

  74. Steneck RS (1986) The ecology of coralline algal crusts: Convergent Patterns and Adaptative strategies. Annual Review of Ecology, Evolution, and Systematics 17:273–303

  75. Steneck RS, Adey W (1976) Role of environment in control of morphology in Lithophyllum congestum, a Caribbean algal ridge builder. Botanica Marina 19:197−215

  76. Tomlinson JT (1969) The burrowing barnacles (Cirripedia, Order Aero thoracica). Atoll Research Bulletin 296:1–162

  77. Tribble G, Sansone F, Smith S (1990) Stoichiometric modeling of carbon diagenesis within a coral reef framework. Geochimica et Cosmochimica Acta 54:2439–2449

  78. Tribollet A, Golubic S (2005) Cross-shelf differences in the pattern and pace of bioerosion of experimental carbonate substrates exposed for 3 years on the northern Great Barrier Reef, Australia. Coral Reefs 24:422–434

  79. Tribollet A, Golubic S (2011) Reef bioerosion: agents and processes. En: Dubinsky Z, Stambler N. (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht pp 435–449

  80. Tribollet A, Payri C (2001) Bioerosion of the crustose coralline alga Hydrolithon onkodes by microborers in the coral reefs of Moorea. French Polynesia. Oceanologica Acta 24:329-342.

  81. Uchman A, Kleemann K, Rattazzi B (2017) Macroborings, their tracemakers and nestlers in clasts of a fan delta: the Savignone Conglomerate (Lower Oligocene), Northern Apennines, Italy. Neues Jahrbuch für Geologie und Paläontologie 283(1):35-51

  82. Vecsei A (2004) A new estimate of global reefal carbonate production including the fore-reefs. Global Planet Change 43:1–18

  83. Wilson M (2007) Macroborings and the evolution of marine bioerosion. En: Miller W III (ed.) Trace fossils: concepts, problems, prospects. Elsevier, Amsterdam-Oxford-New York pp 356–367

  84. Wizemann A, Nandini SD, Stuhldreier I, Sánchez-Noguera C, Wisshak M, Westphal H, Rixen T, Wild C, Reymond CE (2018) Rapid bioerosion in a tropical upwelling coral reef. PLoS ONE 13(9): e0202887.

  85. Zar J (2010) Biostatistical analysis. Prentice Hall/Pearson, New Jersey. 944

  86. Zea S (1993) Recruitment of demosponges (Porifera, Demospongiae) in rocky and coral reef habitats of Santa Marta, Colombian Caribbean. P.S.Z.N.I. Marine Ecology 14:1–21

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To the team associated with the Ecology and Diversity of Marine Algae and Coral Reefs Research Group. This study was funded by a grant from the University of Magdalena—FONCIENCIAS. Thanks to the Laboratory of Marine Mollusks at the Pilot Plant of the University of Magdalena for access to the facilities and to the Office of Administration and Management of Protected Areas for granting the scientific research and biological diversity permit (No. 001 March 2017). GDP was supported by an Australian Research Council Discovery grant (DP160103071).

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Correspondence to Rocío García-Urueña.

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Supplementary Information

S1. Photograph showing fragments of the crustose coralline algae Porolithon antillarum and Lithophyllum kaiseri embedded in resin within PVC disks and attached to racks fixed to the reef in Gayraca bay (TNNP) at 5 m depth (DOCX 42 kb)

S2. Table with values of gross calcification in g CaCo3 cm-2 yr-1 and percentages of bioerosion of the crustose coralline algae Porolithon antillarum and Lithophyllum kaiseri (DOCX 17 kb)

S3. Table with relative abundance of macroboring and percentage of bioerosion in Porolithon antillarum and Lithophyllum kaiseri (DOCX 21 kb)

S4. A non-metrical multidimensional scaling (MDS) results showing clustering among climatic seasons (S1 and S4: Upwelling seasons, S2: minor non-upwelling season, S3: major non-upwelling season) and the main groups of macrobioeroders for the two species of coralline algae (L: Lithophyllum and P: Porolithon) (DOCX 39 kb)

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Ramírez-Viaña, A., Diaz-Pulido, G. & García-Urueña, R. Bioerosion of reef-building crustose coralline algae by endolithic invertebrates in an upwelling-influenced reef. Coral Reefs (2021).

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  • Bioerosion
  • Macroborers
  • Colombian Caribbean
  • Coralline algae