Abstract
The invasive sun corals Tubastraea spp. were introduced to Brazil in the late 1980s. The invasion prompted rapid changes in seascapes and local biological communities by excluding native species, particularly sessile ones. However, little is known about the impact on the mobile invertebrates. Using an experimental approach this study investigated the effects of living and dead sun corals and coral cover (50 vs. 100% covered areas) on the taxonomic composition, diversity (H’) and abundance of reptant and natant macro-crustaceans and tanaids at the species level. Experimental units consisted of 60 tiles measuring 400 cm2, half and fully covered with living or dead corals which were deployed between 3 and 5 m for 12 months on concrete blocks. A total of 1346 specimens of decapods were obtained (27 native and 1 invasive species). 1059 specimens of the tanaid Chondrochelia dubia were sampled. The overall taxonomic composition was neither affected by coral condition (live or dead) nor by coral cover area. The diversity of reptant and natant species responded differently to coral condition and coral cover. The combination of dead corals and full cover accounted for the highest abundance of reptants. Natant abundance was influenced by coral cover area, irrespective of coral condition. The positive relationship between body size and abundance was statistically significant. Abundance of the obligate tube builder C. dubia was favoured by the greater availability of space on blocks half covered by corals. No signs were found of invasion meltdown in the mobile crustacean fauna.
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References
Almeida AO, Boehs G, Araújo-Silva CL, Bezerra LEA (2012a) Shallow-water caridean shrimps from southern Bahia, Brazil, including the first record of Synalpheus ul (Ríos & Duffy, 2007) (Alpheidae) in the southwestern Atlantic Ocean. Zootaxa 35:1–35
Almeida AO, Simões SM, Costa RC, Mantelatto FL (2012b) Alien shrimps in evidence: new records of the genus Athanas Leach, 1814 on the coast of São Paulo, southern Brazil (Caridea: Alpheidae). Helgol Mar Res 66:557–565. https://doi.org/10.1007/s10152-012-0291-6
Almeida AO, Santos PS, Soledade GO et al (2015) New invertebrate host records (Porifera and Cnidaria) for some caridean shrimps in estuaries of north-eastern Brazil. Mar Biodivers Rec 8:1–6. https://doi.org/10.1017/S1755267215000111
Almeida AO, Terossi M, Buranelli RC et al (2018) Checklist of decapods (Crustacea) from the coast of São Paulo State (Brazil) supported by integrative molecular and morphological data: II. Infraorder Caridea: Family Alpheidae. Zootaxa 4450:331–358. https://doi.org/10.11646/zootaxa.4450.3.2
Alves DFR, de Barros-Alves SP, Cobo VJ et al (2012) Checklist of the brachyuran crabs (Crustacea: Decapoda) in the rocky subtidal of Vitória Archipelago, southeast coast of Brazil. Check List 8:940–950
Anker A, Ahyong ST, Noel PY, Palmer AR (2006) Morphological phylogeny of alpheid shrimps: parallel preadaptation and the origin of a key morphological innovation, the snapping claw. Evolution 60:2507–2528. https://doi.org/10.1111/j.0014-3820.2006.tb01886.x
Badaró MFS, Neves EG, Castro P, Johnsson R (2012) Description of a new genus of Cryptochiridae (Decapoda: Brachyura) associated with Siderastrea (Anthozoa: Scleractinia), with notes on feeding habits. Sci Mar 76:517–526. DOI: https://doi.org/10.3989/scimar.03538.02E
Beck MW (1995) Size-specific shelter limitation in stone crabs: a test of the demographic bottleneck hypothesis. Ecology 76:968–980
Beck MW (1997) A test of the generality of the effects of shelter bottlenecks in four stone crab populations. Ecology 78:2487–2503. https://doi.org/10.1890/0012-9658(1997)078[2487:ATOTGO]2.0.CO;2
Behringer DC, Hart JE (2017) Competition with stone crabs drives juvenile spiny lobster abundance and distribution. Oecologia 184:205–218. https://doi.org/10.1007/s00442-017-3844-1
Biagi R, Melo GA (2004) Majoid crabs community (Crustacea: Decapoda) from infralittoral rocky/sandy bottom of Anchieta Island, Ubatuba. Braz Arch Biol Technol 47:273–279. https://doi.org/10.1590/S1516-89132004000200015
Bosc C, Hui C, Roets F, Pauw A (2019) Importance of biotic niches versus drift in a plant-inhabiting arthropod community depends on rarity and trophic group. Ecography (cop) 42:1926–1935. https://doi.org/10.1111/ecog.04396
Capel KCC, Toonen RJ, Rachid CTCC et al (2017) Clone wars: asexual reproduction dominates in the invasive range of Tubastraea spp. (Anthozoa: Scleractinia) in the South-Atlantic Ocean. PeerJ 2017:1–21. https://doi.org/10.7717/peerj.3873
Capel KCC, Creed JC, Kitahara MV (2020) Invasive corals trigger seascape changes in the southwestern Atlantic. Bull Mar Sci 96:217–218. https://doi.org/10.5343/bms.2019.0075
Carlquist S (1974) Island biology. Columbia University Press, New York, p 660
Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371
Coles S (1980) Species diversity of decapods associated with living and dead reef coral Pocillopora meandrina. Mar Ecol Prog Ser 2:281–291. https://doi.org/10.3354/meps002281
Cotgreave P (1993) The relationship between body size and population abundance in animals. Trends Ecol Evol 8:244–248. https://doi.org/10.1016/0169-5347(93)90199-Y
Creed JC, De 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 JC, Fenner D, Sammarco P et al (2017a) 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
Creed JC, Junqueira AOR, Fleury BG, Mantelatto MC, Oigman-Pszczol SS (2017b) The sun-coral project: the first social-environmental initiative to manage the biological invasion of Tubastraea spp. in Brazil. Manag Biol Inv 8:181–195
Creed JC, Pires DO, Figueiredo MAO (2007) Biodiversidade marinha da Baía da Ilha Grande, RJ. Ministério do Meio Ambiente, Brasília
da Silva AG, Carlos-Júnior LA, Sasada Sato CY et al (2022) Living with an enemy: invasive sun-coral (Tubastraea spp.) competing against sponges Desmapsamma anchorata in southeastern Brazil. Mar Environ Res 174:105559. https://doi.org/10.1016/j.marenvres.2022.105559
De 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
Ferreira LADA, de Melo GAS (2016) Porcelain crabs from Brazil (Crustacea: Decapoda: Anomura: Porcellanidae). Zootaxa 4092:175–194
Ferreira LADA, Mendes CB, Pachelle PPG (2021) Range extensions of three marine shrimps (Caridea: Alpheidae, palaemonidae) on the Brazilian coast. An Acad Bras Cienc 93:1–6. https://doi.org/10.1590/0001-3765202120190634
Fitzgerald PC, Carlson SJ (2006) Examining the latitudinal diversity gradient in Paleozoic terebratulide brachiopods: should singleton data be removed? Paleobiology 32:367–386. https://doi.org/10.1666/05029.1
Gilchrist SL (2003) Hermit crab population ecology on a shallow coral reef (Bailey’s Cay, Roatan, Honduras): octopus predation and hermit crab shell use. Mem Mus Vic 60:35–44. https://doi.org/10.1017/S0025315407054604
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
Grajal A, Laughlin R (1984) Decapodcrustaceans inhabiting live and dead colonies of three species of Acropora in the Roques Archipelago, Venezuela. Bijdr Tot Dierkd 54:220–230
Hsieh TC, Ma KH, Chao A (2022) iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 3.0.0. http://chao.stat.nthu.edu.tw/wordpress/software-download/
Instituto Estadual do Ambiente (2011) Rio de Janeiro. Governo do Estado. Proposta de criação da Área de Proteção Ambiental Estadual Marinha da Baía da Ilha Grande. Rio de Janeiro, Secretaria do Meio Ambiente; INEA Instituto Estadual do Ambiente
Johnsson R, Neves E, Franco GMO, Da Silveira FL (2006) The association of two gall crabs (Brachyura: Cryptochiridae) with the reef-building coral Siderastrea stellata Verrill, 1868. Hydrobiologia 559:379–384. https://doi.org/10.1007/s10750-005-9307-4
Krasnow LD, Taghon GL (1997) Rate of tube building and sediment particle size selection during tube construction by the tanaid crustacean, Leptochelia dubia. Estuaries 20:534–546. https://doi.org/10.2307/1352612
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
Lages BG, Fleury BG, Menegola C, Creed JC (2011) Change in tropical rocky shore communities due to an alien coral invasion. Mar Ecol Prog Ser 438:85–96. https://doi.org/10.3354/meps09290
Lages BG, Fleury BG, Hovell AMC et al (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
Lima D, Tavares M, Mendonça JB (2019) Paguroids (Decapoda: Anomura: Diogenidae and Paguridae) of the remote oceanic Archipelago Trindade and Martin Vaz, off southeast Brazil, with new records, description of three new species and zoogeographical notes. Zootaxa 4694:1–63. https://doi.org/10.11646/zootaxa.4694.1.1
Lindahl U, Öhman MC, Schelten CK (2001) The 1997/1998 mass mortality of corals: effects on fish communities on a Tanzanian coral reef. Mar Pollut Bull 42:127–131. https://doi.org/10.1016/S0025-326X(00)00167-3
Magalhães T, Pantaleão JAF, Mantelatto FL (2021) Resurrection of Pilumnus vinaceus A. Milne-Edwards, 1880 (Brachyura: Pilumnidae) using integrative evidence from molecular and morphology. Zootaxa 5047:547–556. https://doi.org/10.11646/zootaxa.5047.5.4
Magurran AE (2013) Medindo a diversidade biológica, 1st edn. UFPR, Curitiba
Magurran AE, Henderson PA (2003) Explaining the excess of rare species in natural species abundance distributions. Nature 422:714–716. https://doi.org/10.1038/nature01547
Mantelatto FL, Tamburus AF, Magalhães T et al (2020) Checklist of decapod crustaceans from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: III. Infraorder Brachyura Latreille, 1802
Melo GAS (1996) Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro. Editora Plêiade
Melo GAS de (1999) Manual de identificação dos Crustacea Decapoda do litoral brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. Plêiade/FAPESP, São Paulo
Mendoza JA (1982) Some aspects of the autoecology of Leptochelia dubia (Krøyer, 1842) (Tanaidacea). Crustaceana 43:225–240
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 163:1–12. https://doi.org/10.1007/s00227-016-2819-9
Miranda RJ, de Anchieta CCJ, Mariano-Neto E, Sippo JZ, Barros F (2018) 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
Moraes IRR, Almeida AO, Cobo VJ et al (2021) Biodiversity of caridean shrimps on rocky bottoms of two preserved islands on the southeastern Brazilian coast. Mar Biol Res 16:616–631. https://doi.org/10.1080/17451000.2020.1864830
Moraes IRR, Davanso TM, da Silva AR et al (2022) A first report of decapod crustaceans (Anomura and Brachyura) from Laje de Santos: a no-take marine reserve in the southeast coast of Brazil. Rev Mex Biodivers. https://doi.org/10.22201/ib.20078706e.2022.93.3658
Moreira TSG, Creed JC (2012) Invasive, non-indigenous corals in a tropical rocky shore environment: no evidence for generalist predation. J Exp Mar Bio Ecol 438:7–13. https://doi.org/10.1016/j.jembe.2012.09.015
Moreira PL, Ribeiro FV, Creed JC (2014) Control of invasive marine invertebrates: an experimental evaluation of the use of low salinity for managing pest corals (Tubastraea spp.). Biofouling 30:639–650
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) vegan: Community Ecology Package_. R package version 2.6-4
Paula AF, Creed JC (2005) Spatial distribution and abundance of nonindigenous coral genus Tubastraea (Cnidaria, Scleractinia) around Ilha Grande, Brazil. Braz J Biol 65:661–673
Paula AF, Fleury BG, Lages BG, Creed JC (2017) Experimental evaluation of the effects of management of invasive corals on native communities. Mar Ecol Prog Ser 572:141–154
Pescinelli RA, Mantelatto FL, Almeida AO, Costa RC (2021) First detailed insights into the life-history traits of the alien shrimp Athanas nitescens (Decapoda: Alpheidae) in the western Atlantic. Mar Ecol 42:1–10. https://doi.org/10.1111/maec.12655
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
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
Sammarco PW, Porter SA, Sinclair J, Genazzio M (2014) Population expansion of a new invasive coral species, Tubastraea micranthus, in the northern gulf of Mexico. Mar Ecol Prog Ser 495:161–173. https://doi.org/10.3354/meps10576
Santos PS, Soledade GO, Almeida AO (2012) Decapod crustaceans on dead coral from reef areas on the coast of Bahia, Brazil. Nauplius 20:145–169. https://doi.org/10.1590/s0104-64972012000200007
Schopfe S, Werding B (1996) The breholes of the sea urchin genus Echinometra (Echinodermata: Echinoidea: Echinometridae) as a microhabitat in tropical south America. Mar Ecol 17:181–186. https://doi.org/10.1111/j.1439-0485.1996.tb00499.x
Sgarbi LF, Melo AS (2018) You don’t belong here: explaining the excess of rare species in terms of habitat, space and time. Oikos 127:497–506. https://doi.org/10.1111/oik.04855
Silva AG, Paula AF, Fleury BG, Creed JC (2014) Eleven years of range expansion of two invasive corals (Tubastraea coccinea and Tubastraea tagusensis) through the southwest Atlantic (Brazil). Estuar Coast Shelf Sci 141:9–16
Silva AG, Fortunato HFM, Lôbo-Hajdu G, Fleury BG (2017) Response of native marine sponges to invasive Tubastraea corals: a case study. Marine Biol 164:1–11
Silva R, Vinagre C, Kitahara MV et al (2019) Sun coral invasion of shallow rocky reefs: effects on mobile invertebrate assemblages in Southeastern Brazil. Biol Invasions. https://doi.org/10.1007/s10530-018-1903-0
Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species. Biol Invasions 1:21–32
Snell Taylor SJ, Evans BS, White EP, Hurlbert AH (2018) The prevalence and impact of transient species in ecological communities. Ecology 99:1825–1835. https://doi.org/10.1002/ecy.2398
Soledade GO, Santos GG, Pinheiro U, Almeida AO (2017) New records of association between caridean shrimps (Decapoda) and sponges (Porifera) in Abrolhos Archipelago, northeastern Brazil. Nauplius. https://doi.org/10.1590/2358-2936e2017027
Straatsma G, Egli S (2012) Rarity in large data sets: singletons, modal values and the location of the species abundance distribution. Basic Appl Ecol 13:380–389. https://doi.org/10.1016/j.baae.2012.03.011
Tanasovici RM, Kitahara MV, Dias GM (2020) Invasive coral Tubastraea spp. population growth in artificial habitats and its consequences to the diversity of benthic organisms. Mar Biol 167:1–12. https://doi.org/10.1007/s00227-020-03734-6
Tavares M, Mendonça JB (2022) Brachyuran crabs (Crustacea, Decapoda) from the remote oceanic Archipelago Trindade and Martin Vaz, South Atlantic Ocean. Zootaxa 5146(1):1–129. https://doi.org/10.11646/zootaxa.5146.1.1
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Yiu SKF, Qiu J-W (2022) Three new species of the sun coral genus Tubastraea (Scleractinia: Dendrophylliidae) from Hong Kong, China. Zool Stud 61:1–12. https://doi.org/10.6620/ZS.2022.61-45
Acknowledgements
The authors thank Pró-Reitoria de Pesquisa da USP for financial support in the form of a Post-Doctoral Fellowship to ARS (Processo USP: 2021.1.10424.1.9). We acknowledge funding for this study from Petrobras through the Petrobras Environmental Program and the Brazilian Institute for Marine Biodiversity as well as all those who helped in the field, especially Joel Braga and Marcelo Mantelatto. JCC also thanks funding from Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ E-26/010.003031/2014 and E26/203.002/2017) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 305924/2018-4 and 313698/2021-0). MT also thanks CNPq (309488/2020-6) for supporting studies on the systematics and ecology of marine invertebrates. This article is no. 53 from the Projeto Coral-Sol.
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da Silva, A.R., Creed, J.C. & Tavares, M. Species diversity and abundance of mobile crustaceans associated with living and dead colonies of the invasive sun coral Tubastraea. Aquat Ecol 57, 529–541 (2023). https://doi.org/10.1007/s10452-023-10027-9
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DOI: https://doi.org/10.1007/s10452-023-10027-9