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Symbiont-bearing foraminifera as health proxy in coral reefs in the equatorial margin of Brazil

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Abstract

Coral communities worldwide are progressively more stressed by anthropogenic activities that increase fluxes of sediment and other pollutants to nearshore areas. Some nearshore coral reef environments off the Equatorial margin of Brazil, including Pirangi and Maracajaú, Rio Grande do Norte (RN, Brazil), seem to be under human-induced stress. However, the horizontal extent of this stress, its effects, and assessment of the environmental response depend on the hydrodynamic conditions (circulation and deposition patterns), sedimentary facies, and the availability of biological indicators. We investigate two Brazilian live reefal corals’ communities by examining seven photosymbiont-bearing species (PSB) of Foraminifera, Amphisorus hemprichii, Amphistegina gibbosa, Archaias angulatus, Borelis schlumbergeri, Heterostegina antillarum, Peneroplis carinatus, and Laevipeneroplis proteus, using numerical analysis FORAM Index (FI), grain size, and particulate organic and inorganic carbonate. Here, we show that coarse sand fraction followed by fine sand fraction and high hydrodynamics plays an important role in transportation and deposition of sediments and foraminiferal tests in the study area. According to FI results, conditions at Pirangi are not suitable for coral reef growth. Maracajaú has sites that are suitable for coral reef growth and sites where coral could not survive after a stress event. We need long-term assessments to improve our knowledge of the distribution and ecological importance of Brazilian reef-dwelling foraminifers and to extend the application of FI to monitoring management plans of the Pirangi and Maracajaú National Marine Parks by providing a first insight into the biodiversity patterns and a reliable tool of the reconstruction of paleo reef health.

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References

  • Alve E (1995) Benthic foraminiferal responses to estuarine pollution: a review. J Foraminifer Res 25:190–203

    Google Scholar 

  • Azevedo CAA, Carneiro MAA, Oliveira SR, Marinho-Soriano E (2011) Macrolgae as an indicator of the environmental health of the Pirangi reefs, Rio Grande do Norte, Brazil. Rev Bras Farm 21(2):323–328

    Google Scholar 

  • Baer J, Woodley CM, Pennington P (2017) Effect of anthropogenic pollutants on ESA coral health. NOAA National Ocean Service National Centers for Coastal Science, Charleston

    Google Scholar 

  • Barbosa CF, Prazeres MF, Ferreira BP, Seoane JCS (2009) Foraminiferal assemblage and reef check census in coral reef health monitoring of east Brazilian margin. Mar Micropaleontol 73:62–69

    Google Scholar 

  • Barbosa CF, Ferreira BP, Seoane JCS, Oliveira-Silva P, Gaspar ALB, Cordeiro RC, Soares-Gomes A (2012) Foraminifer-based coral reef health assessment for southwestern Atlantic offshore archipelagos, Brazil. J Foraminifer Res 42:169–183

    Google Scholar 

  • Barradas JI, Amaral FD, Hernández MIM, Montes MJF, Steiner AQ (2010) Spatial distribution of benthic macroorganisms on reef flats at Porto de Galinhas Beach (northeastern Brazil), with special focus on corals and calcified hydroids. Biotemas 23(2):61–67

    Google Scholar 

  • Bernhard JM, Ostermann DR, Williams DS, Blanks JK (2006) Comparison of two methods to identify live benthic foraminifera: a test between Rose Bengal and CellTracker Green with implications for stable isotope paleoreconstructions. Paleoceanography 21:PA4210. https://doi.org/10.1029/2006PA001290

    Article  Google Scholar 

  • Bicchi E, Debenay JP, Pagès J (2002) Relationship between benthic foraminiferal assemblages and environmental factors in atoll lagoons of the central Tuamotu archipelago (French Polynesia). Coral Reefs 21:275–290

    Google Scholar 

  • Bryant D, Burke L, McManus J, Spalding M (1998) Reefs at risk: a map-based Indicator of threats to the world’s coral reefs. World Resources Institute, Washington, D.C.

    Google Scholar 

  • Carilli J, Walsh S (2012) Benthic foraminiferal assemblages from Kiritimati (Christmas) island indicate increased nitrification has occurred on a decadal scale. Mar Ecol Prog Ser 456:87–99

    Google Scholar 

  • Carnahan EA, Hoare MM, Hallock P, Lidz BH, Reich CD (2009) Foraminiferal assemblages in Biscayne Bay, Florida, USA: responses to urban and agricultural influence in a subtropical estuary. Mar Pollut Bull 59:221–233

    CAS  Google Scholar 

  • Carver RE (1971) Procedures in sedimentary petrology. Wiley InterScience, New York 653 p

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143

    Google Scholar 

  • Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219

    Google Scholar 

  • Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  • Cockey EM, Hallock PM, Lidz BH (1996) Decadal-scale changes in benthic foraminiferal assemblages off key largo, Florida. Coral Reefs 15:237–248

    Google Scholar 

  • De Araújo HAB, De Jesus Machado A (2008) Benthic foraminifera associated with the south Bahia coral reefs, Brazil. J Foram Res 38(1):23–38

    Google Scholar 

  • Eichler PPB, Eichler BB, de Miranda LB, Rodrigues AR (2007) Modern foraminiferal facies in a subtropical estuarine channel, Bertioga, São Paulo, Brazil. J Foram Res 37(3):234–247

    Google Scholar 

  • Eichler PPB, Eichler BB, Sen Gupta B, Rodrigues AR (2012a) Foraminifera as indicators of marine pollutant contamination on the inner continental shelf of southern Brazil. Mar Pollut Bull 64:22–30

    CAS  Google Scholar 

  • Eichler PPB, Rodrigues AR, Eichler BB, Braga ES, Campos EJD (2012b) Tracing latitudinal gradient, river discharge and water masses along the subtropical south American coast using benthic foraminifera assemblages. Braz J Biol 72:723–759

    CAS  Google Scholar 

  • Eichler PPB, de Farias CC, Amorin A, de Moura DFS, de Andrade AU, de Oliveira Martins JF, Vital H, Gomes MP (2019) Symbiont-bearing foraminifera from reefal areas: a case study from Rio Grande Do Norte (RN, Brazil). J Foraminifer Res 49(2):131–140. https://doi.org/10.2113/gsjfr.49.2.131

    Article  Google Scholar 

  • Engle VD (2000) Application of the indicator evaluation guidelines to an index of benthic condition for Gulf of Mexico estuaries. In: Jackson LE, Kurtz JC, Fisher WS (eds) Evaluation guidelines for ecological indicators. U.S. Environmental Protection Agency, Research Triangle Park 29 p

    Google Scholar 

  • Ferreira BP, Maida M (2006) Monitoramento dos recifes de coral do Brasil. MMA, Secretaria de Biodiversidade e Florestas

  • Folk RL, Ward WC (1957) Brazos river bar: study of the significance of grain size parameters. J Sediment Petrol 27:3–27

    Google Scholar 

  • Francini-Filho RB, Coni EOC, Meirelles PM, Amado-Filho GM, Thompson FL, Pereira-Filho GH (2013) Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLoS One 8(1):e54260. https://doi.org/10.1371/journal.pone.0054260

    Article  CAS  Google Scholar 

  • Hallock P (1999) Symbiont-bearing foraminifera. In: Sen Gupta BK (ed) Modern foraminifera. Kluwer Academic Publishers, Dordrecht, pp 123–139

    Google Scholar 

  • Hallock P (2000) Larger foraminifera as indicators of coral-reef vitality. In: Martin RE (ed) Environmental micropaleontology. Kluwer Academic/Plenum Publishers, New York, pp 121–150

    Google Scholar 

  • Hallock P (2012) The FORAM index revisited. Uses, challenges, and limitations. Proceedings of the 12th international coral reef symposium

  • Hallock P, Lidz BH, Cockey-Burkhard EM, Donnelly KB (2003) Foraminifera as bioindicators in coral reef assessment and monitoring: the FORAM index. Environ Monit Assess 81:221–238

    Google Scholar 

  • Hallock, Pamela, "The FoRAM Index Revisited: Uses, Challenges, and Limitations" (2012). Marine Science Faculty Publications. 1218. https://scholarcommons.usf.edu/msc_facpub/1210

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

  • Humphreys AF, Halfar J, Ingle JC, Manzello D, Reymond CE, Westphal H, Riegl B (2019) Shallow-water benthic foraminifera of the Galápagos archipelago: ecologically sensitive carbonate producers in an atypical tropical oceanographic setting. J Foraminifer Res 49(1):48–65

    Google Scholar 

  • Kay AM, Liddle MJ (1989) Environmental Management 13: 509. Publisher Name Springer-Verlag Print ISSN 0364-152X

  • Krajewski JP, Floeter SR (2011) Reef fish community structure of the Fernando de Noronha archipelago (equatorial Western Atlantic): the influence of exposure and benthic composition. Environ Biol Fish 92:25–40

    Google Scholar 

  • Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117

    CAS  Google Scholar 

  • Kuroyanagi A, Kawahata H, Suzuki A, Fujita K, Irie T (2009) Impacts of ocean acidification on large benthic foraminifers: results from laboratory experiments. Mar Micropaleontol 73:190–195

    Google Scholar 

  • Leao ZM, Kikuchi RK (2005) A relic coral fauna threatened by global changes and human activities, eastern Brazil. Mar Pollut Bull 51(5–7):599–611

    CAS  Google Scholar 

  • Leão ZMAN, Kikuchi RKP, Oliveira MD, Vasconcellos V (2010) Status of eastern Brazilian coral reefs in time of climate changes. Pan-Am J Aquat Sci 5(2):224–235

    Google Scholar 

  • Machado AJ, Souza FBC (1994) Principais espécies de foraminíferos e Briozoários do Atol das Rocas. Rev Bras Geociênc 24(4):247–261

    Google Scholar 

  • Martinez AS, Mendes LF, Leite TS (2012) Spatial distribution of epibenthic mollusks on a sandstone reef in the northeast of Brazil. Braz J Biol 72:1–12

    Google Scholar 

  • Mayal EM, Neumann-Leitão S, Feitosa FAN, Schwamborn R, Almeida e Silva T, Silva-Cunha MGG (2009) Hydrology, plankton, and corals of the Maracajaú reefs (northeastern Brazil), an ecosystem under severe thermal stress. Braz Arch Biol Technol 52:665–678

    CAS  Google Scholar 

  • Moraes SS, Machado AJ (2003) Avaliação das condições hidrodinâmicas de dois recifes costeiros do litoral norte do Estado da Bahia. Braz J Geol 33:201–210

    Google Scholar 

  • Müller G (1967) Methods in sedimentary petrography (part I). Hafner Publishing Co., New York 283 p

    Google Scholar 

  • Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101

    CAS  Google Scholar 

  • Narayan YR, Pandolfi JM (2010) Benthic foraminiferal assemblages from Moreton Bay, south-East Queensland, Australia: applications in monitoring water and substrate quality in subtropical estuarine environments. Mar Pollut Bull 60:2062–2078

    CAS  Google Scholar 

  • Oliveira-Silva P, Barbosa CF, Machado de Almeida C, Seoane JCS, Cordeiro RC, Turcq BJ, Soares-Gomes A (2012) Sedimentary geochemistry and foraminiferal assemblages in coral reef assessment of Abrolhos, Southwest Atlantic. Mar Micropaleontol 94:14–24

    Google Scholar 

  • Oliver LM, Fisher WS, Dittmar J, Hallock P, Campbell J, Quarles RL, Lo HP, Bue C (2014) Contrasting responses of coral reef fauna and foraminiferal assemblages to human influence in La Parguera, Puerto Rico. Mar Environ Res 99:95–105

    CAS  Google Scholar 

  • Pelejero C, Calvo E, Hoegh-Guldberg O (2010) Paleo-perspectives on ocean acidification. Trends Ecol Evol 25:332–344

    Google Scholar 

  • Pereira-Filho GH, Menezes G, Guimarães SMPB, Moura RL, Sumida PYG, Abrantes DP, Bahia RG, Güth AZ, Jorge RR, Francini Filho RB (2011) Reef fish and benthic assemblages of the Trindade and Martin Vaz Island group, southwestern Atlantic. Braz J Oceanogr 59(3):201–212. https://doi.org/10.1590/S1679-87592011000300001

    Article  Google Scholar 

  • Reymond CE, Lloyd A, Kline DI, Dove SG, Pandolfi JM (2013) Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios. Glob Chang Biol 19(1):291–302

    Google Scholar 

  • Reymond CE, Mateu-Vicens G, Westphal H (2014) Foraminiferal assemblages from a transitional tropical upwelling zone in the Golfe d'Arguin, Mauritania. Estuar Coast Shelf Sci 148:70–84

    Google Scholar 

  • Schueth JD, Frank TD (2008) Reef foraminifera as bioindicators of coral reef health: low isles reef, northern great barrier reef, Australia. J Foram Res 38(1):11–22

    Google Scholar 

  • Scott DB, Medioli FS, Schafer CT (2001) Monitoring of coastal environments using foraminifera and Thecamoebian indicators. Cambridge University Press, Cambridge 176 p

    Google Scholar 

  • Sen Gupta BK (1999) Foraminifera in marginal marine environments. In: Sen Gupta BK (ed) Modern foraminifera. Kluwer Academic Publishers, Dordrecht, pp 141–159

    Google Scholar 

  • Sen Gupta BK, Platon E (2006) Tracking past sedimentary records of oxygen depletion in coastal waters: use of the Ammonia-Elphidium foraminiferal index. J Coast Res Spec Issue 39:1351–1355

    Google Scholar 

  • Sen Gupta BK, Turner RE, Rabalais NN (1996) Seasonal oxygen depletion in continental-shelf waters of Louisiana: historical record of benthic foraminifers. Geology 24:227–230

    Google Scholar 

  • Shepard FP (1954) Nomenclature based on sand-silt-clay ratios. J Sediment Petrol 24:151–158

    Google Scholar 

  • Stuhr et al (2017) Reef calcifiers are adapted to episodic heat stress but vulnerable to sustained warming. PLoS One 12(7):e0179753. https://doi.org/10.1371/journal.pone.0179753

    Article  CAS  Google Scholar 

  • Stuhr et al (2019) Proteomics reveals early stress responses in photosymbiont foraminifera (2018). Sci Rep 8:3524. https://doi.org/10.1038/s41598-018-21875-z

    Article  CAS  Google Scholar 

  • Uthicke S, Nobes K (2008) Benthic foraminifera as ecological indicators for water quality on the great barrier reef. Estuar Coast Shelf Sci 78:763–773

    Google Scholar 

  • Uthicke S, Thompson A, Schaffelke B (2010) Effectiveness of benthic foraminiferal and coral assemblages as water quality indicators on inshore reefs of the great barrier reef, Australia. Coral Reefs 29:209–225

    Google Scholar 

  • Velásquez J, López-Angarita J, Sánchez JA (2011) Benthic foraminifera as indicators of ecosystem resilience in protected and non-protected coral reefs of the Southern Caribbean. Biodivers Conserv 20:3591–3603. https://doi.org/10.1007/s10531-011-0152-7

    Article  Google Scholar 

  • Wilson B, Ramsook A (2007) Population densities and diversities of epiphytal foraminifera on nearshore substrates, Nevis, West Indies. J Foraminifer Res 37:213–222

    Google Scholar 

  • Yanko V, Kronfeld J, Flexer A (1994) Response of benthic foraminifera to various pollution sources: implications for pollution monitoring. J Foraminifer Res 24:1–17

    Google Scholar 

  • Yanko V, Ahmad M, Kaminski M (1998) Morphological deformities of benthic foraminiferal test in response to pollution by heavy metals: implications for pollution monitoring. J Foraminifer Res 28:177–200

    Google Scholar 

  • Yanko V, Arnold AJ, Parker WC (1999) The effect of marine pollution on benthic foraminifera. In: Sen Gupta BK (ed) Modern Foraminifera. Kluwer Academic Publishes, Dordrecht, pp 217–235

    Google Scholar 

  • Yanko-Hombach V, Kondariuk T, Motnenko I (2017) Benthic foraminifera indicate environmental stress from river discharge to marine ecosystems: example from the Black Sea. J Foraminifer Res 47(1):70–92

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, Englewood Cliffs 718 p

    Google Scholar 

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Acknowledgments

The first author thanks CAPES through the Edital Ciências do Mar 2 no. 43/2013, Proj. no. 23038.004320/2014-11 for the postdoctoral fellowship at UFRN-Brazil. We also acknowledge CAPES and CNPq for the Professor Visitante Especial Fellowship (Proj. 151/2012 and AUX PE 242/2013) in the Science Without Borders Program. We thank PROBRAL 337/10 (CAPES/DAAD) for the short postdoctoral fellowship for P.P.B. Eichler (grant n. 8116-12-1) at Kiel University, CNPq (Researcher Grant PQ number 311413/2016-1) and MCTI/CNPq N° 23/2011. Apoio Técnico para Fortalecimento da Paleontologia Nacional (grant number 552976/2011-3). We also acknowledge the University of California Museum of Paleontology and the Smithsonian Institution for the loan of reference specimens.

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Correspondence to Patrícia P. B. Eichler.

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Foraminiferal data (Appendix)

Foraminiferal data (Appendix)

The abundance and distribution of “live” (Rose Bengal-stained) foraminifera are given in Tables 5, 6, 7, and 8

Table 5 Pirangi 2013 foraminifera: number of Rose Bengal-stained individuals picked per station sample fraction
Table 6 Pirangi 2014 foraminifera: number of Rose Bengal-stained individuals picked per station sample fraction
Table 7 Maracajaú 2013 foraminifera: number of Rose Bengal-stained individuals picked per station sample fraction
Table 8 Maracajaú 2014 foraminifera: number of Rose Bengal-stained individuals picked per station sample fraction

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Eichler, P.P.B., de Moura, D.S. Symbiont-bearing foraminifera as health proxy in coral reefs in the equatorial margin of Brazil. Environ Sci Pollut Res 27, 13637–13661 (2020). https://doi.org/10.1007/s11356-019-07483-y

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