Abstract
Biological invasions have modified habitat structure, forcing changes in ecosystem functions. Structural complexity modulates diversity and trophic pathways, but the roles of invasive species in mediating coral reef habitat attributes and trophic effects are poorly understood. We investigated the influence of invasive corals on reef structural complexity and their implications on reef fish trophic structure. To assess habitat complexity and trophic relationships, we used a digital probe to map reef rugosity and characterized benthic cover and fish abundances by video and visual estimates. We calculated a coral skeleton complexity index (for individual invasive and native colonies) by building high-resolution three-dimensional models with photogrammetry techniques. The study was conducted between February 2018 and March 2019 in Cascos Reef, located on the east coast of Brazil. We reveal that the complex morphology of the invasive coral Tubastraea spp. skeleton had a significant positive effect on reef rugosity, contributing to substrate complexity at a sub-metric scale. However, this likely did not promote reef fish diversity but altered the assemblage structure patterns, demonstrated by a negative relationship between coral colony complexity index and abundance of trophic groups such as roving herbivores and omnivores and a positive relationship with planktivores. Thus, our findings support that habitat attribute modification promoted by invasive corals can influence the benthos-fish dynamic, promoting some fish groups to the detriment of others, with pervasive implications for ecosystem functions. Global changes are increasing invasions worldwide, enhancing the need for effective policies for regulation and management to ensure human well-being and ecosystem services.
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Data availability
The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request. The Video Transect Analyzer software (Version 1.0) is available for download at https://bit.ly/VTA1installer.
References
Agudo-Adriani EA, Cappelletto J, Cavada-Blanco F, Croquer A (2016) Colony geometry and structural complexity of the endangered species Acropora cervicornis partly explains the structure of their associated fish assemblage. PeerJ 4:e1861. https://doi.org/10.7717/peerj.1861
Almany GR (2004) Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141:105–113. https://doi.org/10.1007/s00442-004-1617-0
Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proc R Soc B Biol Sci 276:3019–3025. https://doi.org/10.1098/rspb.2009.0339
Alvarez-Filip L, Dulvy NK, Côté IM, Watkinson AR, Gill JA (2011a) Coral identity underpins architectural complexity on Caribbean reefs. Ecol Appl 21:2223–2231. https://doi.org/10.1890/10-1563.1
Alvarez-Filip L, Gill JA, Dulvy NK, Perry AL, Watkinson AR, Côté IM (2011b) Drivers of region-wide declines in architectural complexity on Caribbean reefs. Coral Reefs 30:1051–1060. https://doi.org/10.1007/s00338-011-0795-6
Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. J Wildl Manag 72:1658–1659. https://doi.org/10.2193/2008-264
Ault TR, Johnson C (1998) Relationships between habitat and recruitment of three species of damselfish (Pomacentridae) at Heron Reef, Great Barrier Reef. J Exp Mar Biol Ecol 223:145–166. https://doi.org/10.1016/S0022-0981(97)00158-5
Bastos N, Calazans SH, Altvater L, Neves EG, Trujillo AL, Sharp WC, Hoffman EA, Coutinho R (2022) Western Atlantic invasion of sun corals: incongruence between morphology and genetic delimitation among morphotypes in the genus Tubastraea. Bull Mar Sci. https://doi.org/10.5343/bms.2021.0031
Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323. https://doi.org/10.1016/S0308-597X(03)00041-1
Bellwood DR (1996) Production and reworking of sediment by parrotfishes (family Scaridae) on the Great Barrier Reef, Australia. Mar Biol 125:795–800. https://doi.org/10.1007/BF00349262
Bonaldo RM, Bellwood DR (2011) Spatial variation in the effects of grazing on epilithic algal turfs on the Great Barrier Reef, Australia. Coral Reefs 30:381–390. https://doi.org/10.1007/s00338-010-0704-4
Bonaldo RM, Hoey AS, Bellwood DR (2014) The ecosystem roles of parrotfishes on tropical reefs. In: Hughes RN, Hughes DJ, Smith IP (eds) Oceanography and marine biology. CRC Press, pp 81–132
Bozec Y-M, Alvarez-Filip L, Mumby PJ (2015) The dynamics of architectural complexity on coral reefs under climate change. Glob Change Biol 21:223–235. https://doi.org/10.1111/gcb.12698
Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. https://doi.org/10.1177/0049124104268644
Cairns SD (1994) Scleractinia of the temperate North Pacific. Smithson Contrib Zool:i–150. https://doi.org/10.5479/si.00810282.557.i
Capasso L, Aranda M, Cui G, Pousse M, Tambutté S, Zoccola D (2022) Investigating calcification-related candidates in a non-symbiotic scleractinian coral. Tubastraea Spp Sci Rep 12:13515. https://doi.org/10.1038/s41598-022-17022-4
Carlos-Júnior LA, Barbosa NPU, Moulton TP, Creed JC (2015) Ecological Niche Model used to examine the distribution of an invasive, non-indigenous coral. Mar Environ Res 103:115–124. https://doi.org/10.1016/j.marenvres.2014.10.004
Castro C, Pires D (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371
Cignoni P, Corsini M, Ranzuglia G (2008) MeshLab: an open-source 3D mesh processing system. ERCIM News 73:47–48
Creed JC (2006) Two invasive alien azooxanthellate corals, Tubastraea coccinea and Tubastraea tagusensis, dominate the native zooxanthellate Mussismilia hispida in Brazil. Coral Reefs 25:350–350. https://doi.org/10.1007/s00338-006-0105-x
Creed JC, Paula AF (2007) Substratum preference during recruitment of two invasive alien corals onto shallow-subtidal tropical rocky shores. Mar Ecol Prog Ser 330:101–111. https://doi.org/10.3354/meps330101
Creed J, Junqueira A, Fleury B, Mantelatto M, Oigman-Pszczol S (2017a) The Sun-Coral Project: the first social-environmental initiative to manage the biological invasion of Tubastraea spp. in Brazil. Manag Biol Invasions 8:181–195. https://doi.org/10.3391/mbi.2017.8.2.06
Creed JC, Fenner D, Sammarco P, Cairns S, Capel K, Junqueira AOR, Cruz I, Miranda RJ, Carlos-Junior L, Mantelatto MC, Oigman-Pszczol S (2017b) The invasion of the azooxanthellate coral Tubastraea (Scleractinia: Dendrophylliidae) throughout the world: history, pathways and vectors. Biol Invasions 19:283–305. https://doi.org/10.1007/s10530-016-1279-y
Cruz ICS, Kikuchi RKP, Leão ZMAN (2008) Use of the video transect method for characterizing the Itacolomis reefs, eastern Brazil. Braz J Oceanogr 56:271–280. https://doi.org/10.1590/S1679-87592008000400002
Denis V, Ribas-Deulofeu L, Sturaro N, Kuo C-Y, Chen CA (2017) A functional approach to the structural complexity of coral assemblages based on colony morphological features. Sci Rep 7:9849. https://doi.org/10.1038/s41598-017-10334-w
Diaz M, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546
dos Santos LAH, Ribeiro FV, Creed JC (2013) Antagonism between invasive pest corals Tubastraea spp. and the native reef-builder Mussismilia hispida in the southwest Atlantic. J Exp Mar Biol Ecol 449:69–76. https://doi.org/10.1016/j.jembe.2013.08.017
Dustan P, Doherty O, Pardede S (2013) Digital reef rugosity estimates coral reef habitat complexity. PLoS ONE 8:e57386. https://doi.org/10.1371/journal.pone.0057386
Dutra L, Kikuchi R, Leao Z (2006) Todos os Santos Bay coral reefs, Eastern Brazil, revisited after 40 years. In: Proceedings of 10th International Coral Reef Symposium. pp 1090–1095
Epstein HE, Kingsford MJ (2019) Are soft coral habitats unfavourable? A closer look at the association between reef fishes and their habitat. Environ Biol Fishes 102:479–497. https://doi.org/10.1007/s10641-019-0845-4
Ferrari R, Figueira WF, Pratchett MS, Boube T, Adam A, Kobelkowsky-Vidrio T, Doo SS, Atwood TB, Byrne M (2017) 3D photogrammetry quantifies growth and external erosion of individual coral colonies and skeletons. Sci Rep 7:16737. https://doi.org/10.1038/s41598-017-16408-z
Ferreira CEL, Floeter SR, Gasparini JL, Ferreira BP, Joyeux JC (2004) Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J Biogeogr 31:1093–1106. https://doi.org/10.1111/j.1365-2699.2004.01044.x
Floeter SR, Ferreira CEL, Dominici-Arosemena A, Zalmon IR (2004) Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns. J Fish Biol 64:1680–1699. https://doi.org/10.1111/j.0022-1112.2004.00428.x
Francini-Filho RB, Ferreira CM, Coni EOC, De Moura RL, Kaufman L (2010) Foraging activity of roving herbivorous reef fish (Acanthuridae and Scaridae) in eastern Brazil: influence of resource availability and interference competition. J Mar Biol Assoc U K 90:481–492. https://doi.org/10.1017/S0025315409991147
Glynn PW, Colley SB, Maté JL, Cortés J, Guzman HM, Bailey RL, Feingold JS, Enochs IC (2008) Reproductive ecology of the azooxanthellate coral Tubastraea coccinea in the Equatorial Eastern Pacific: Part V. Dendrophylliidae Mar Biol 153:529–544. https://doi.org/10.1007/s00227-007-0827-5
Goatley CHR, Bellwood DR (2012) Sediment suppresses herbivory across a coral reef depth gradient. Biol Lett:1016–1018. doi: https://doi.org/10.1098/rsbl.2012.0770
Graham NAJ (2014) Habitat complexity: coral structural loss leads to fisheries declines. Curr Biol 24:R359–R361. https://doi.org/10.1016/j.cub.2014.03.069
Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326. https://doi.org/10.1007/s00338-012-0984-y
Graham N, Wilson S, Pratchett M, Polunin N, Spalding M (2009) Coral mortality versus structural collapse as drivers of corallivorous butterflyfish decline. Biodivers Conserv 18:3325–3336. https://doi.org/10.1007/s10531-009-9633-3
Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7:e33353. https://doi.org/10.1371/journal.pone.0033353
Halpern B, Floeter S (2008) Functional diversity responses to changing species richness in reef fish communities. Mar Ecol Prog Ser 364:147–156. https://doi.org/10.3354/meps07553
Hamylton SM, Duce S, Vila-Concejo A, Roelfsema CM, Phinn SR, Carvalho RC, Shaw EC, Joyce KE (2017) Estimating regional coral reef calcium carbonate production from remotely sensed seafloor maps. Remote Sens Environ 201:88–98. https://doi.org/10.1016/j.rse.2017.08.034
Hixon MA, Beets JP (1993) Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101. https://doi.org/10.2307/2937124
Kleypas JA, Buddemeier RW, Gattuso J-P (2001) The future of coral reefs in an age of global change. Int J Earth Sci 90:426–437. https://doi.org/10.1007/s005310000125
Knudby A, LeDrew E (2007) Measuring structural complexity on coral reefs. Diving Sci 2007 Proc Am Acad Underw Sci 26th Symp 8
Koeda K, Fukagawa T, Ishihara T, Tachihara K (2013) Reproductive biology of nocturnal reef fish Pempheris sp. (Pempherididae) in Okinawa Island. Japan Galaxea J Coral Reef Stud 15:221–228. https://doi.org/10.3755/galaxea.15.221
Kolar CS (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298:1233–1236. https://doi.org/10.1126/science.1075753
Lages BG, Fleury BG, Pinto AC, Creed JC (2010) Chemical defenses against generalist fish predators and fouling organisms in two invasive ahermatypic corals in the genus Tubastraea. Mar Ecol 31:473–482. https://doi.org/10.1111/j.1439-0485.2010.00376.x
Lages BG, Fleury BG, Hovell AMC, Rezende CM, Pinto AC, Creed JC (2012) Proximity to competitors changes secondary metabolites of non-indigenous cup corals, Tubastraea spp., in the southwest Atlantic. Mar Biol 159:1551–1559. https://doi.org/10.1007/s00227-012-1941-6
Leão ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. In: Latin American coral reefs. Elsevier, pp 9–52
Levin P, Hay M (1996) Responses of temperate reef fishes to alterations in algal structure and species composition. Mar Ecol Prog Ser 134:37–47. https://doi.org/10.3354/meps134037
Longo GO, Ferreira CEL, Floeter SR (2014) Herbivory drives large-scale spatial variation in reef fish trophic interactions. Ecol Evol 4:4553–4566. https://doi.org/10.1002/ece3.1310
McCormick M (1994) Comparison of field methods for measuring surface topography and their associations with a tropical reef fish assemblage. Mar Ecol Prog Ser 112:87–96. https://doi.org/10.3354/meps112087
Miranda RJ, Cruz ICS, Barros F (2016) Effects of the alien coral Tubastraea tagusensis on native coral assemblages in a southwestern Atlantic coral reef. Mar Biol 163:45. https://doi.org/10.1007/s00227-016-2819-9
Miranda RJ, Nunes JACC, Mariano-Neto E, Sippo JZ, Barros F (2018a) Do invasive corals alter coral reef processes? An empirical approach evaluating reef fish trophic interactions. Mar Environ Res 138:19–27. https://doi.org/10.1016/j.marenvres.2018.03.013
Miranda RJ, Tagliafico A, Kelaher B, Mariano-Neto E, Barros F (2018b) Impact of invasive corals Tubastrea spp. on native coral recruitment. Mar Ecol Prog Ser 605:125–133. https://doi.org/10.3354/meps12731
Mizrahi D, Navarrete SA, Flores AAV (2014) Uneven abundance of the invasive sun coral over habitat patches of different orientation: an outcome of larval or later benthic processes? J Exp Mar Biol Ecol 452:22–30. https://doi.org/10.1016/j.jembe.2013.11.013
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492. https://doi.org/10.1890/070064
Moreira TSG, Creed JC (2012) Invasive, non-indigenous corals in a tropical rocky shore environment: No evidence for generalist predation. J Exp Mar Biol Ecol 438:7–13. https://doi.org/10.1016/j.jembe.2012.09.015
Nunes JACC, Loiola M, Miranda RJ, Sampaio CLS, Barros F (2016) Are Abrolhos no-take area sites of naïve fish? An evaluation using flight initiation distance of labrids. Neotropical Ichthyol. https://doi.org/10.1590/1982-0224-20160133
Paula AF, Creed JC (2004) Two species of the coral Tubastraea (Cnidaria, Scleractinia) in Brazil: a case of accidental introduction. Bull Mar Sci 74:175–183
Paula AF, Pires DO, Creed JC (2014) Reproductive strategies of two invasive sun corals (Tubastraea spp.) in the southwestern Atlantic. J Mar Biol Assoc U K 94:481–492. https://doi.org/10.1017/S0025315413001446
Rogers A, Blanchard JL, Mumby PJ (2014) Vulnerability of coral reef fisheries to a loss of structural complexity. Curr Biol 24:1000–1005. https://doi.org/10.1016/j.cub.2014.03.026
Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632. https://doi.org/10.1093/icb/37.6.621
Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in north america: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531. https://doi.org/10.1146/annurev.ecolsys.31.1.481
Sampaio CLS, Miranda RJ, Maia-Nogueira R, Nunes JACC (2012) New occurrences of the nonindigenous orange cup corals Tubastraea coccinea and T. tagusensis (Scleractinia: Dendrophylliidae) in Southwestern Atlantic. Check List 8:528–530
Schuhmacher H (1984) Reef-building properties of Tubastraea micranthus (Scleractinia, Dendrophylliidae), a coral without zooxanthellae. Mar Ecol Prog Ser 20:93–99
Schuhmacher H, Zibrowius H (1985) What is hermatypic?: a redefinition of ecological groups in corals and other organisms. Coral Reefs 4:1–9. https://doi.org/10.1007/BF00302198
Seebens H, Gastner MT, Blasius B (2013) The risk of marine bioinvasion caused by global shipping. Ecol Lett 16:782–790. https://doi.org/10.1111/ele.12111
Seebens H, Bacher S, Blackburn TM, Capinha C, Dawson W, Dullinger S, Genovesi P, Hulme PE, Kleunen M, Kühn I, Jeschke JM, Lenzner B, Liebhold AM, Pattison Z, Pergl J, Pyšek P, Winter M, Essl F (2021) Projecting the continental accumulation of alien species through to 2050. Glob Change Biol 27:970–982. https://doi.org/10.1111/gcb.15333
Thresher R (1983) Environmental correlates of the distribution of planktivorous fishes in the one tree reef lagoon. Mar Ecol Prog Ser 10:137–145. https://doi.org/10.3354/meps010137
Urbina-Barreto I, Chiroleu F, Pinel R, Fréchon L, Mahamadaly V, Elise S, Kulbicki M, Quod J-P, Dutrieux E, Garnier R, Henrich Bruggemann J, Penin L, Adjeroud M (2021) Quantifying the shelter capacity of coral reefs using photogrammetric 3D modeling: from colonies to reefscapes. Ecol Indic 121:107151. https://doi.org/10.1016/j.ecolind.2020.107151
Veal CJ, Holmes G, Nunez M, Hoegh-Guldberg O, Osborn J (2010) A comparative study of methods for surface area and three-dimensional shape measurement of coral skeletons: surface area measurements of corals. Limnol Oceanogr Methods 8:241–253. https://doi.org/10.4319/lom.2010.8.241
Wellington GM, Trench RK (1985) Persistence and coexistence of a nonsymbiotic coral in open reef environments. Proc Natl Acad Sci 82:2432–2436. https://doi.org/10.1073/pnas.82.8.2432
Wells JW (1993) Corals of the cretaceous of the atlantic and gulf coastal plains and western interior of the United States. Harris co., Ithaca, NY
Wetz JJ, Ajemian MJ, Shipley B, Stunz GW (2020) An assessment of two visual survey methods for documenting fish community structure on artificial platform reefs in the Gulf of Mexico. Fish Res 225:105492. https://doi.org/10.1016/j.fishres.2020.105492
Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Polunin NVC (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob Change Biol 12:2220–2234. https://doi.org/10.1111/j.1365-2486.2006.01252.x
Wilson SK, Graham NAJ, Polunin NVC (2007) Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Mar Biol 151:1069–1076. https://doi.org/10.1007/s00227-006-0538-3
Acknowledgements
We thank T. Albuquerque, R. Lapa, D. Lisboa, M. Caetano, Y. Costa, I. “Buda” Andrade, and L. Tourinho for assistance in field activities. We also thank I. Cruz for his help with the three-dimensional reconstruction methods of objects and G. Lessa for enriching technical-scientific discussions. C. “Catruco” provided assertive and safe navigation in all field activities. F. Moraes prepared the map of the study area. I. Menezes and L. Carvalho provided support with the GLMs. Finally, we thank the reviewers for their valuable considerations and improvement suggestions provided.
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This work is a product of the National Institute of Science and Technology of Tropical Marine Environments (inct AmbTropic), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Process 465634/2014-1. Ruy Kenji Papa de Kikuchi is a CNPq Research Productivity Fellow (PQ1C—CNPq Process 311449/2019-0). LSNR was supported by CNPq (Ph.D. scholarship 158799/2015-1). RJM was supported by CNPq (post-doc scholarship 150883/2020-0).
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LSNR, JACCN, RJM, and RKPK designed the study; LSNR performed fieldwork; RKPK and LSNR provided infrastructure/material/technical support; LSNR, JACCN, and RJM analyzed the data; and LSNR, JACCN, RJM, and RKPK contributed to the manuscript.
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Neves da Rocha, L.S., Nunes, J.A.C.C., Miranda, R.J. et al. Effects of invasive sun corals on habitat structural complexity mediate reef trophic pathways. Mar Biol 171, 76 (2024). https://doi.org/10.1007/s00227-024-04394-6
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DOI: https://doi.org/10.1007/s00227-024-04394-6