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.
Similar content being viewed by others
References
Alve E (1995) Benthic foraminiferal responses to estuarine pollution: a review. J Foraminifer Res 25:190–203
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
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
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
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
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
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
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
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.
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
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
Carver RE (1971) Procedures in sedimentary petrology. Wiley InterScience, New York 653 p
Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143
Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219
Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth
Cockey EM, Hallock PM, Lidz BH (1996) Decadal-scale changes in benthic foraminiferal assemblages off key largo, Florida. Coral Reefs 15:237–248
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
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
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
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
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
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
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
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
Hallock P (1999) Symbiont-bearing foraminifera. In: Sen Gupta BK (ed) Modern foraminifera. Kluwer Academic Publishers, Dordrecht, pp 123–139
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
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
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
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
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
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
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
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
Machado AJ, Souza FBC (1994) Principais espécies de foraminíferos e Briozoários do Atol das Rocas. Rev Bras Geociênc 24(4):247–261
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
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
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
Müller G (1967) Methods in sedimentary petrography (part I). Hafner Publishing Co., New York 283 p
Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101
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
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
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
Pelejero C, Calvo E, Hoegh-Guldberg O (2010) Paleo-perspectives on ocean acidification. Trends Ecol Evol 25:332–344
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
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
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
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
Scott DB, Medioli FS, Schafer CT (2001) Monitoring of coastal environments using foraminifera and Thecamoebian indicators. Cambridge University Press, Cambridge 176 p
Sen Gupta BK (1999) Foraminifera in marginal marine environments. In: Sen Gupta BK (ed) Modern foraminifera. Kluwer Academic Publishers, Dordrecht, pp 141–159
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
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
Shepard FP (1954) Nomenclature based on sand-silt-clay ratios. J Sediment Petrol 24:151–158
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
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
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
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
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
Wilson B, Ramsook A (2007) Population densities and diversities of epiphytal foraminifera on nearshore substrates, Nevis, West Indies. J Foraminifer Res 37:213–222
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
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
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
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
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, Englewood Cliffs 718 p
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-07483-y