Advertisement

Oecologia

, Volume 191, Issue 3, pp 621–632 | Cite as

Spatial distribution of damage affects the healing, growth, and morphology of coral

  • Elizabeth A. HammanEmail author
Community ecology – original research

Abstract

Many predators and herbivores do not kill their prey, but rather remove or damage tissue. Prey are often able to heal or regenerate this lost tissue. If the prey are modular organisms (e.g., some plants and cnidarians), regeneration is frequently influenced by other modules interconnected to damaged ones. For example, many coral predators remove tissue from colonies consisting of many polyps, and these polyps often share resources with their neighbors. Thus, the distribution of tissue loss on a coral colony could affect the coral’s response. I hypothesized that spatially aggregated damage might be slow to heal due to competing demands on nearby polyps. To explore the spatial patterns of corallivory and their implications, I conducted: (1) field surveys documenting the spatial distribution of lesions on corals; (2) field experiments testing the effect of the distance between lesions on coral tissue healing, skeletal growth, and morphology; and (3) field surveys relating corallivore presence to coral growth and morphology. In the field surveys, lesions were aggregated at multiple spatial scales, and most lesions had other lesions within 2 cm. When lesions were near one another, coral tissue regeneration was depressed, although there was no effect on whole colony growth. After a year, however, linear extension was lower in the neighborhood of the lesions. Additionally, gastropod corallivores (Coralliophila violacea) with low movement decreased coral growth and increased coral topographical complexity. These results suggest that corallivores that create clusters of coral damage have a greater effect on coral growth and recovery from damage than corallivores that spread damage throughout the colony.

Keywords

Coral damage Coralliophila violacea Massive Porites Spatial distributions 

Notes

Acknowledgements

I thank Alissa Rubin, Luc Overholt, and Carly Roeser for assistance with image analysis, the Osenberg lab and Caitlin Cameron for helpful discussions, and Angela Mulligan, Julie Zill, and Morgan Farrell for field assistance. This work was supported by NSF grant OCE-1130359 and is a contribution from UC Berkeley’s Richard B. Gump South Pacific Research Station.

Author contribution statement

EAH conceived, designed, and executed this study and wrote the manuscript. No other person is entitled to authorship.

Funding

This study was funded by the National Science Foundation (NSF Grant OCE-1130359)

Compliance with ethical standards

Conflict of interest

The author declares that there is no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2019_4509_MOESM1_ESM.docx (2.2 mb)
Supplementary material 1 (DOCX 2286 kb)

References

  1. Adonsou KE, Drobyshev I, DesRochers A, Tremblay F (2016) Root connections affect radial growth of balsam poplar trees. Trees 30:1775–1783.  https://doi.org/10.1007/s00468-016-1409-2 CrossRefGoogle Scholar
  2. Alpert P, Holzapfel C, Slominski C (2003) Differences in performance between genotypes of Fragaria chiloensis with different degrees of resource sharing. J Ecol 91:27–35CrossRefGoogle Scholar
  3. Ando Y, Ohgushi T (2008) Ant- and plant-mediated indirect effects induced by aphid colonization on herbivorous insects on tall goldenrod. Popul Ecol 50:181–189.  https://doi.org/10.1007/s10144-007-0072-2 CrossRefGoogle Scholar
  4. Bak RPM (1983) Neoplasia, regeneration and growth in the reef-building coral Acropora palmata. Mar Biol 77:221–227.  https://doi.org/10.1007/BF00395810 CrossRefGoogle Scholar
  5. Bak RPM, Steward-Van Es Y (1980) Regeneration of superficial damage in the Scleractinian Corals Agaricia Agaricites F. Purpurea and Porites Astreoides. https://www.ingentaconnect.com/content/umrsmas/bullmar/1980/00000030/00000004/art00010
  6. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 1(1):2015Google Scholar
  7. Baums IB, Miller MW, Szmant AM (2003) Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two Scleractinian hosts. II. Feeding, respiration and growth. Mar Biol 142:1093–1101.  https://doi.org/10.1007/s00227-003-1053-4 CrossRefGoogle Scholar
  8. Burmester E, Finnerty J, Kaufman L, Rotjan R (2017) Temperature and symbiosis affect lesion recovery in experimentally wounded, facultatively symbiotic temperate corals. Mar Ecol Prog Ser 570:87–99.  https://doi.org/10.3354/meps12114 CrossRefGoogle Scholar
  9. Burmester EM, Breef-Pilz A, Lawrence NF et al (2018) The impact of autotrophic versus heterotrophic nutritional pathways on colony health and wound recovery in corals. Ecol Evol.  https://doi.org/10.1002/ece3.4531 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cameron C, Edmunds P (2014) Effects of simulated fish predation on small colonies of massive Porites spp. and Pocillopora meandrina. Mar Ecol Prog Ser 508:139–148.  https://doi.org/10.3354/meps10862 CrossRefGoogle Scholar
  11. Cameron AC, Trivedi PK (1990) Regression-based tests for overdispersion in the poisson model. J Econom 46:347–364CrossRefGoogle Scholar
  12. Chen J-S, Lei N-F, Liu Q (2011) Defense signaling among interconnected ramets of a rhizomatous clonal plant, induced by jasmonic-acid application. Acta Oecologica 37:355–360.  https://doi.org/10.1016/j.actao.2011.04.002 CrossRefGoogle Scholar
  13. Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35:445–453.  https://doi.org/10.2307/1931034 CrossRefGoogle Scholar
  14. Clements CS, Hay ME (2018) Overlooked coral predators suppress foundation species as reefs degrade. Ecol Appl 28:1673–1682.  https://doi.org/10.1002/eap.1765 CrossRefPubMedPubMedCentralGoogle Scholar
  15. D’Angelo C, Smith EG, Oswald F et al (2012) Locally accelerated growth is part of the innate immune response and repair mechanisms in reef-building corals as detected by green fluorescent protein (GFP)-like pigments. Coral Reefs 31:1045–1056.  https://doi.org/10.1007/s00338-012-0926-8 CrossRefGoogle Scholar
  16. Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395.  https://doi.org/10.1007/BF00428135 CrossRefGoogle Scholar
  17. DeFilippo L, Burmester EM, Kaufman L, Rotjan RD (2016) Patterns of surface lesion recovery in the Northern Star Coral, Astrangia poculata. J Exp Mar Biol Ecol 481:15–24.  https://doi.org/10.1016/j.jembe.2016.03.016 CrossRefGoogle Scholar
  18. Denis V, Debreuil J, De Palmas S et al (2011) Lesion regeneration capacities in populations of the massive coral Porites lutea at Réunion Island: environmental correlates. Mar Ecol Prog Ser 428:105–117.  https://doi.org/10.3354/meps09060 CrossRefGoogle Scholar
  19. Denis V, Guillaume MMM, Goutx M et al (2013) Fast growth may impair regeneration capacity in the branching coral Acropora muricata. PLoS One.  https://doi.org/10.1371/journal.pone.0072618 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Edmunds PJ, Lenihan HS (2010) Effect of sub-lethal damage to juvenile colonies of massive Porites spp. under contrasting regimes of temperature and water flow. Mar Biol 157:887–897.  https://doi.org/10.1007/s00227-009-1372-1 CrossRefPubMedGoogle Scholar
  21. Edmunds PJ, Yarid A (2017) The effects of ocean acidification on wound repair in the coral Porites spp. J Exp Mar Biol Ecol 486:98–104.  https://doi.org/10.1016/j.jembe.2016.10.001 CrossRefGoogle Scholar
  22. Fine M, Oren U, Loya Y (2002) Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica. Mar Ecol Prog Ser 234:119–125.  https://doi.org/10.3354/meps234119 CrossRefGoogle Scholar
  23. Fisher E, Fauth J, Hallock P, Woodley C (2007) Lesion regeneration rates in reef-building corals Montastraea spp. as indicators of colony condition. Mar Ecol Prog Ser 339:61–71.  https://doi.org/10.3354/meps339061 CrossRefGoogle Scholar
  24. Fletcher RJ Jr, Revell A, Reichert BE et al (2013) Network modularity reveals critical scales for connectivity in ecology and evolution. Nat Commun 4:2572.  https://doi.org/10.1038/ncomms3572 CrossRefPubMedGoogle Scholar
  25. Goodsman DW, Lusebrink I, Landhäusser SM et al (2013) Variation in carbon availability, defense chemistry and susceptibility to fungal invasion along the stems of mature trees. New Phytol 197:586–594.  https://doi.org/10.1111/nph.12019 CrossRefPubMedGoogle Scholar
  26. Hall VR (1997) Interspecific differences in the regeneration of artificial injuries on Scleractinian corals. J Exp Mar Biol Ecol 212:9–23.  https://doi.org/10.1016/S0022-0981(96)02760-8 CrossRefGoogle Scholar
  27. Hamman EA (2018) Aggregation patterns of two corallivorous snails and consequences for coral dynamics. Coral Reefs 37:851–860.  https://doi.org/10.1007/s00338-018-1712-z CrossRefGoogle Scholar
  28. Hayes JA (1990) Distribution, movement and impact of the corallivorous gastropod Coralliophila abbreviata (Lamarck) on a Panamánian patch reef. J Exp Mar Biol Ecol 142:25–42.  https://doi.org/10.1016/0022-0981(90)90135-Y CrossRefGoogle Scholar
  29. Hellström K, Kytöviita M-M, Tuomi J, Rautio P (2006) Plasticity of clonal integration in the perennial herb Linaria vulgaris after damage. Funct Ecol 20:413–420.  https://doi.org/10.1111/j.1365-2435.2006.01115.x CrossRefGoogle Scholar
  30. Hench JL, Leichter JJ, Monismith SG (2008) Episodic circulation and exchange in a wave-driven coral reef and lagoon system. Limnol Oceanogr 53:2681–2694.  https://doi.org/10.4319/lo.2008.53.6.2681 CrossRefGoogle Scholar
  31. Henry L-A, Hart M (2005) Regeneration from injury and resource allocation in sponges and corals—a review. Int Rev Hydrobiol 90:125–158.  https://doi.org/10.1002/iroh.200410759 CrossRefGoogle Scholar
  32. Honkanen T, Haukioja E, Kitunen V (1999) Responses of Pinus sylvestris branches to simulated herbivory are modified by tree sink/source dynamics and by external resources. Funct Ecol 13:126–140.  https://doi.org/10.1046/j.1365-2435.1999.00296.x CrossRefGoogle Scholar
  33. Jayewardene D (2010) Experimental determination of the cost of lesion healing on Porites compressa growth. Coral Reefs 29:131–135.  https://doi.org/10.1007/s00338-009-0560-2 CrossRefGoogle Scholar
  34. Jayewardene D, Donahue MJ, Birkeland C (2009) Effects of frequent fish predation on corals in Hawaii. Coral Reefs 28:499–506.  https://doi.org/10.1007/s00338-009-0475-y CrossRefGoogle Scholar
  35. Johst K, Drechsler M (2003) Are spatially correlated or uncorrelated disturbance regimes better for the survival of species? Oikos 103:449–456.  https://doi.org/10.1034/j.1600-0706.2003.12770.x CrossRefGoogle Scholar
  36. Jompa J, McCook L (2003) Coral-algal competition: macroalgae with different properties have different effects on corals. Mar Ecol Prog Ser 258:87–95.  https://doi.org/10.3354/meps258087 CrossRefGoogle Scholar
  37. Kallimanis AS, Kunin WE, Halley JM, Sgardelis SP (2005) Metapopulation extinction risk under spatially autocorrelated disturbance. In: conservation biology. https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1523-1739.2005.00418.x. Accessed 3 Jul 2019
  38. Katz SM, Pollock FJ, Bourne DG, Willis BL (2014) Crown-of-thorns starfish predation and physical injuries promote brown band disease on corals. Coral Reefs 33:705–716.  https://doi.org/10.1007/s00338-014-1153-2 CrossRefGoogle Scholar
  39. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw.  https://doi.org/10.18637/jss.v082.i13 CrossRefGoogle Scholar
  40. Lester RT, Bak RPM (1985) Effects of environment on regeneration rate of tissue lesions in the reef coral Montastraea annularis (Scleractinia). Mar Ecol Prog Ser 24:183–185CrossRefGoogle Scholar
  41. Littler MM, Taylor PR, Littler DS (1989) Complex interactions in the control of coral zonation on a Caribbean reef flat. Oecologia 80:331–340.  https://doi.org/10.1007/BF00379034 CrossRefPubMedGoogle Scholar
  42. Marbà N, Hemminga M, Mateo M et al (2002) Carbon and nitrogen translocation between seagrass ramets. Mar Ecol Prog Ser 226:287–300.  https://doi.org/10.3354/meps226287 CrossRefGoogle Scholar
  43. Mascarelli PE, Bunkley-Williams L (1999) An experimental field evaluation of healing in damaged, unbleached and artificially bleached star coral, Montastraea annularis. https://www.ingentaconnect.com/content/umrsmas/bullmar/1999/00000065/00000002/art00019. Accessed 7 Jul 2019
  44. Meesters EH, Bak RPM (1993) Effects of coral bleaching on tissue regeneration potential and colony survival. Mar Ecol Prog Ser 96:189–198CrossRefGoogle Scholar
  45. Meesters EH, Bos A, Gast GJ (1992) Effects of sedimentation and lesion position on coral tissue regeneration. In: Proceedings of the 7th International Coral Reef Symposium pp 681–688Google Scholar
  46. Meesters E, Noordeloos M, Bak R (1994) Damage and regeneration: links to growth in the reef-building coral Montastr annularis. Mar Ecol Prog Ser 112:119–128.  https://doi.org/10.3354/meps112119 CrossRefGoogle Scholar
  47. Meesters E, Pauchli W, Bak R (1997) Predicting regeneration of physical damage on a reef-building coral by regeneration capacity and lesion shape. Mar Ecol Prog Ser 146:91–99.  https://doi.org/10.3354/meps146091 CrossRefGoogle Scholar
  48. Miller MW (2001) Corallivorous snail removal: evaluation of impact on Acropora palmata. Coral Reefs 19:293–295.  https://doi.org/10.1007/PL00006963 CrossRefGoogle Scholar
  49. Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268.  https://doi.org/10.1111/j.0030-1299.2004.12768.x CrossRefGoogle Scholar
  50. Oborny B (2019) The plant body as a network of semi-autonomous agents: a review. Philos Trans R Soc Lond B Biol Sci.  https://doi.org/10.1098/rstb.2018.0371 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Oren U, Benayahu Y, Loya Y (1997a) Effect of lesion size and shape on regeneration of the Red Sea coral Favia favus. Mar Ecol Prog Ser 146:101–107.  https://doi.org/10.3354/meps146101 CrossRefGoogle Scholar
  52. Oren U, Rinkevich B, Loya Y (1997b) Oriented intra-colonial transport of 14C labeled materials during coral regeneration. Mar Ecol Prog Ser 161:117–122.  https://doi.org/10.3354/meps161117 CrossRefGoogle Scholar
  53. Oren U, Brickner I, Loya Y (1998) Prudent sessile feeding by the corallivore snail, Coralliophila violacea on coral energy sinks. Proc Biol Sci 265:2043–2050.  https://doi.org/10.1098/rspb.1998.0538 CrossRefPubMedCentralGoogle Scholar
  54. Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC (2011) Corals use similar immune cells and wound-healing processes as those of higher organisms. PLoS One 6:e23992.  https://doi.org/10.1371/journal.pone.0023992 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rotjan RD, Dimond JL (2010) Discriminating causes from consequences of persistent parrotfish corallivory. J Exp Mar Biol Ecol 390:188–195.  https://doi.org/10.1016/j.jembe.2010.04.036 CrossRefGoogle Scholar
  56. Rotjan R, Lewis S (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91.  https://doi.org/10.3354/meps07531 CrossRefGoogle Scholar
  57. Ruiz-Diaz CP, Toledo-Hernandez C, Mercado-Molina AE et al (2016) The role of coral colony health state in the recovery of lesions. Peer J 4:e1531.  https://doi.org/10.7717/peerj.1531 CrossRefPubMedGoogle Scholar
  58. Sabine AM, Smith TB, Williams DE, Brandt ME (2015) Environmental conditions influence tissue regeneration rates in Scleractinian corals. Mar Pollut Bull 95:253–264.  https://doi.org/10.1016/j.marpolbul.2015.04.006 CrossRefPubMedGoogle Scholar
  59. Schmid B, Puttick GM, Burgess KH, Bazzaz FA (1988) Clonal integration and effects of simulated herbivory in old-field perennials. Oecologia 75:465–471.  https://doi.org/10.1007/BF00376953 CrossRefPubMedGoogle Scholar
  60. Schoepf V, Herler J, Zuschin M (2010) Microhabitat use and prey selection of the coral-feeding snail Drupella cornus in the northern Red Sea. Hydrobiologia 641:45–57.  https://doi.org/10.1007/s10750-009-0053-x CrossRefGoogle Scholar
  61. Shaver EC, Burkepile DE, Silliman BR (2018) Local management actions can increase coral resilience to thermally-induced bleaching. Nat Ecol Evol 2:1075–1079.  https://doi.org/10.1038/s41559-018-0589-0 CrossRefPubMedGoogle Scholar
  62. Sheridan C, Grosjean P, Leblud J et al (2014) Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral. Coral Reefs 33:1067–1076.  https://doi.org/10.1007/s00338-014-1202-x CrossRefGoogle Scholar
  63. Shima JS, Osenberg CW, Stier AC (2010) The vermetid gastropod Dendropoma maximum reduces coral growth and survival. Biol Lett 6:815–818.  https://doi.org/10.1098/rsbl.2010.0291 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Shima JS, McNaughtan D, Strong AT (2015) Vermetid gastropods mediate within-colony variation in coral growth to reduce rugosity. Mar Biol 162:1523–1530.  https://doi.org/10.1007/s00227-015-2688-7 CrossRefGoogle Scholar
  65. Stuefer JF, Gómez S, van Mölken T (2004) Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks. Evol Ecol 18:647–667.  https://doi.org/10.1007/s10682-004-5148-2 CrossRefGoogle Scholar
  66. Tack AJM, Dicke M (2013) Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Funct Ecol 27:633–645.  https://doi.org/10.1111/1365-2435.12087 CrossRefGoogle Scholar
  67. Titlyanov EA, Titlyanova TV, Yakovleva IM et al (2005) Regeneration of artificial injuries on Scleractinian corals and coral/algal competition for newly formed substrate. J Exp Mar Biol Ecol 323:27–42.  https://doi.org/10.1016/j.jembe.2005.02.015 CrossRefGoogle Scholar
  68. Van Veghel M, Bak RPM (1994) Reproductive characteristics of the polymorphic Caribbean reef building coral Montastrae annularis. 111. Reproduction in damaged and regenerating colonies. Mar Ecol Prog Ser 109:229–233CrossRefGoogle Scholar
  69. van Woesik R (1998) Lesion healing on massive Porites spp. corals. Mar Ecol Prog Ser 164:213–220CrossRefGoogle Scholar
  70. Wahle CM (1983) Regeneration of injuries among Jamaican gorgonians: the roles of colony physiology and environment. Biol Bull 165:778–790.  https://doi.org/10.2307/1541478 CrossRefPubMedGoogle Scholar
  71. Wei Q, Li Q, Jin Y et al (2019) Transportation or sharing of stress signals among interconnected ramets improves systemic resistance of clonal networks to water stress. Funct Plant Biol 46:613.  https://doi.org/10.1071/FP18232 CrossRefGoogle Scholar
  72. Welsh JQ, Bonaldo RM, Bellwood DR (2015) Clustered parrotfish feeding scars trigger partial coral mortality of massive Porites colonies on the inshore Great Barrier Reef. Coral Reefs 34:81–86.  https://doi.org/10.1007/s00338-014-1224-4 CrossRefGoogle Scholar
  73. White J (1979) The plant as a metapopulation. Annu Rev Ecol Syst 10:109–145.  https://doi.org/10.1146/annurev.es.10.110179.000545 CrossRefGoogle Scholar
  74. You W-H, Han C-M, Liu C-H, Yu D (2016) Effects of clonal integration on the invasive clonal plant Alternanthera philoxeroides under heterogeneous and homogeneous water availability. Sci Rep 6:29767.  https://doi.org/10.1038/srep29767 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Yu F, Dong M, Krüsi B (2004) Clonal integration helps Psammochloa villosa survive sand burial in an inland dune. New Phytol 162:697–704.  https://doi.org/10.1111/j.1469-8137.2004.01073.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Odum School of EcologyUniversity of GeorgiaAthensUSA
  2. 2.Department of BiologyRadford UniversityRadfordUSA

Personalised recommendations