Skip to main content
SpringerLink
Log in

How mollusk assemblages respond to different urbanization levels: characterization of the malacofauna in subtropical Brazilian mangroves

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

This study aimed to describe the composition of mollusk assemblages in subtropical Brazilian mangroves with different levels of urbanization in their watersheds. Mangroves are important ecosystems, which are vanishing worldwide due to human impacts. The knowledge about the consequences of human pressure on the fauna of these ecosystems is still incipient. In addition, although Brazil is the country with the second largest mangrove area, there is a lack of studies on the mangrove fauna in this country. Mollusks are the second most abundant group of mangrove invertebrates and can be useful indicators of mangrove health. For this reason, mollusk species were assessed in two mangroves surrounded by a dense human population and in two mangroves away from urban centers. A total of 3820 individuals, representing 15 species, were sampled. The results revealed that the mollusk abundance, diversity estimators, and sediment organic matter content were not good indicators of the effects of urbanization on the mangroves studied. However, the species composition of mollusk assemblages differed according to the urbanization level. This survey of the mangrove malacofauna represents another step toward the effort to investigate and conserve the fauna of these important estuarine environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Afonso CM (2006) A paisagem da Baixada Santista: urbanização, transformação e conservação. EDUSP, São Paulo

    Google Scholar 

  • Aguirre ML, Urrutia MI (2002) Morphological variability of Littoridina australis (d’Orbigny, 1835) (Hydrobiidae) in the Bonaerensian marine Holocene (Argentina). Palaeogeogr Palaeoclimatol Palaeoecol 183:1–23. https://doi.org/10.1016/S0031-0182(01)00445-X

    Article  Google Scholar 

  • Aguirre ML, Zanchetta G, Fallick AE (2002) Stable isotope composition of Littoridina australis from the coast of Buenos Aires province, Argentina, during Holocene climatic fluctuations. Geobios 35:79–88. https://doi.org/10.1016/S0016-6995(02)00011-6

    Article  Google Scholar 

  • Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29:331–349. https://doi.org/10.1017/S0376892902000231

    Article  Google Scholar 

  • Alongi DM (2008) Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuar Coast Shelf Sci 76:1–13. https://doi.org/10.1016/j.ecss.2007.08.024

    Article  Google Scholar 

  • Alongi DM (2014) Carbon cycling and storage in mangrove forests. Annu Rev Mar Sci 6:195–219. https://doi.org/10.1146/annurev-marine-010213-135020

    Article  Google Scholar 

  • Alongi DM (2015) The impact of climate change on mangrove forests. Curr Clim Chang Reports 1:30–39. https://doi.org/10.1007/s40641-015-0002-x

    Article  Google Scholar 

  • Alvarez MF, Esquius KS, Addino M et al (2013) Cascading top-down effects on estuarine intertidal meiofaunal and algal assemblages. J Exp Mar Bio Ecol. https://doi.org/10.1016/j.jembe.2012.12.015

  • Amin B, Ismail A, Arshad A et al (2009) Gastropod assemblages as indicators of sediment metal contamination in mangroves of Dumai, Sumatra, Indonesia. Water Air Soil Pollut. https://doi.org/10.1007/s11270-008-9922-6

  • Ashton EC, Macintosh DJ, Hogarth PJ (2003) A baseline study of the diversity and community ecology of crab and molluscan macrofauna in the Sematan mangrove forest, Sarawak. Malaysia J Trop Ecol doi. https://doi.org/10.1017/S0266467403003158

  • Banci KRS, Mori GM, Oliveira MA et al (2017) Can environmental pollution by metals change genetic diversity? Ucides cordatus (Linnaeus, 1763) as a study case in southeastern Brazilian mangroves. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2017.01.039

  • Bandaranayake WM (1998) Traditional and medicinal uses of mangroves. Mangroves Salt Marshes. https://doi.org/10.1023/A:1009988607044

  • Barroso CX, Matthews-Cascon H (2009) Distribuição espacial e temporal da malacofauna no estuário do rio Ceará, Ceará, Brasil. Panamjas 4:79–86

    Google Scholar 

  • Barroso CX, Rabay SG, Meirelles CAO, Matthews-Cascon H (2013) Mollusks from two estuarine areas in Ceará State, northeastern Brazil, with new state records for four species. Check List. https://doi.org/10.15560/9.3.504

  • Beasley CR, Fernandes CM, Gomes CP et al (2005) Molluscan diversity and abundance among coastal habitats of northern Brazil. Ecotropica 11:9–20

    Google Scholar 

  • Bernardino AF, Pagliosa PR, Christofoletti RA et al (2016) ReBentos studies to assess climate change impacts. Brazilian J Oceanogr 64:83–97

    Article  Google Scholar 

  • Blanco JF, Castaño MC (2012) Effects mangrove conversion to pasture on density and shell size of two gastropods in the turbo river delta (Urabá gulf, Caribbean coast of Colombia) [Efecto de la conversión del manglar a potrero sobre la densidad y tallas de dos gasterópodos en el delta]. Rev Biol Trop 60:1707–1719

    Article  PubMed  Google Scholar 

  • Bodin N, N’Gom Ka R, Le Loc’h F et al (2011) Are exploited mangrove molluscs exposed to persistent organic pollutant contamination in Senegal, West Africa? Chemosphere. https://doi.org/10.1016/j.chemosphere.2011.04.012

  • Boehs G, Absher TM, Cruz-Kaled A da (2004) Composition and distribution of benthic molluscs on intertidal flats of Paranagua Bay (Parana, Brazil). Sci Mar doi: https://doi.org/10.3989/scimar.2004.68n4537

  • Cavalcante RM, Sousa FW, Nascimento RF, Silveira ER, Freirec GSS (2009) The impact of urbanization on tropical mangroves (Fortaleza, Brazil): evidence from PAH distribution in sediments. J Envir Manag 91:328–335

    Article  CAS  Google Scholar 

  • Canepuccia AD, Escapa M, Daleo P et al (2007) Positive interactions of the smooth cordgrass Spartina alterniflora on the mud snail Heleobia australis, in south western Atlantic salt marshes. J Exp Mar Bio Ecol. https://doi.org/10.1016/j.jembe.2007.09.009

  • Cannicci S, Bartolini F, Dahdouh-Guebas F et al (2009) Effects of urban wastewater on crab and mollusc assemblages in equatorial and subtropical mangroves of East Africa. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2009.04.021

  • Cantagallo C, Garcia GJ, Milanelli JCC (2008) Mapeamento de sensibilidade ambiental a derramamentos de óleo do Sistema Estuarino de Santos, Estado de São Paulo. Brazilian J Aquat Sci Technol 12:33–47

    Article  Google Scholar 

  • Cazzaniga NJ (2011) El género Heleobia (Caenogastropoda : Cochliopidae) en América del Sur. Amici Molluscarum 48:11–48

    Google Scholar 

  • Chao A, Hwang WH, Chen YC, Kuo CY (2000) Estimating the number of shared species in two communities. Stat Sin ​10:227–246

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. Primer-E, Plymouth

    Google Scholar 

  • Colpo KD, Chacur MM, Guimarães FJ, Negreiros-Fransozo ML (2011) Subtropical Brazilian mangroves as a refuge of crab (Decapoda: Brachyura) diversity. Biodivers Conserv. https://doi.org/10.1007/s10531-011-0125-x

  • Cordeiro CAMM, Costa TM (2010) Evaluation of solid residues removed from a mangrove swamp in the São Vicente Estuary, SP, Brazil. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2010.06.010

  • Daru BH, Yessoufou K, Mankga LT, Davies TJ (2013) A global trend towards the loss of evolutionarily unique species in mangrove ecosystems. PLoS One. https://doi.org/10.1371/journal.pone.0066686

  • Dauvin JC (2007) Paradox of estuarine quality: benthic indicators and indices, consensus or debate for the future. Mar Pollut Bull 55:271–281. https://doi.org/10.1016/j.marpolbul.2006.08.017

    Article  CAS  PubMed  Google Scholar 

  • de Francesco CG, Isla FI (2004) The life cycle and growth of Heleobia australis (d’Orbigny, 1835) and H. conexa (Gaillard, 1974) (Gastropoda: Rissooidea) in Mar Chiquita coastal lagoon (Argentina). J Molluscan Stud. https://doi.org/10.1093/mollus/70.2.173

  • Duke NC, Meynecke JO, Dittmann S et al (2007) A world without mangroves? Science. https://doi.org/10.1126/science.317.5834.41b

  • Egres AG, Martins CC, de OVM, Lana P da C (2012) Effects of an experimental in situ diesel oil spill on the benthic community of unvegetated tidal flats in a subtropical estuary (Paranaguai Bay, Brazil). Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2012.10.007

  • Etchegoin JA, Merlo MJ (2011) Heleobia conexa y H. australis como bioindicadores de fauna y de fluctuaciones ambientales en la laguna Mar Chiquita (Buenos Aires, Argentina). Amici Molluscarum 33–35

  • FAO - Food and Agriculture Organization of the United Nations (2007) The world’s mangroves 1980-2005. Food and Agriculture Organization of the United Nations, Roma

  • Ferreira AC, Lacerda LD (2016) Degradation and conservation of Brazilian mangroves, status and perspectives. Ocean Coast Manag. https://doi.org/10.1016/j.ocecoaman.2016.03.011

  • Figueiredo-Barros MP, Leal JJF, de Esteves AF et al (2006) Life cycle, secondary production and nutrient stock in Heleobia australis (d’Orbigny 1835) (Gastropoda: Hydrobiidae) in a tropical coastal lagoon. Estuar Coast Shelf Sci 69:87–95. https://doi.org/10.1016/j.ecss.2006.03.023

    Article  Google Scholar 

  • Fiori SM, Carcedo MC (2011) Estado actual del conocimiento sobre Heleobia australis y perspectivas futuras. Amici Molluscarum:28–28

  • Fonseca G, Netto SA (2006) Shallow sublittoral benthic communities of the Laguna Estuarine System, South Brazil. Brazilian J Oceanogr. https://doi.org/10.1590/S1679-87592006000100004

  • Friess DA, Phelps J, Leong RC et al (2012) Mandai mangrove, Singapore: lessons for the conservation of Southeast Asia’s mangroves. Raffles Bull Zool 25:55–65

    Google Scholar 

  • Gao X, Chen S, Long A (2008) Composition and sources of organic matter and its solvent extractable components in surface sediments of a bay under serious anthropogenic influences: Daya Bay. China Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2008.03.036

  • Gaston KJ (2003) The structure and dynamics of geographic ranges. Oxford University Press, New York

    Google Scholar 

  • Gilman EL, Ellison J, Duke NC, Field C (2008) Threats to mangroves from climate change and adaptation options: a review. Aquat Bot. https://doi.org/10.1016/j.aquabot.2007.12.009

  • Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Grilo CF, Neto RR, Vicente MA et al (2013) Evaluation of the influence of urbanization processes using mangrove and fecal markers in recent organic matter in a tropical tidal flat estuary. Appl Geochem. https://doi.org/10.1016/j.apgeochem.2013.08.009

  • Hamilton SE, Casey D (2016) Creation of a high spatio-temporal resolution global database of continuous mangrove forest cover for the 21st century (CGMFC-21). Glob Ecol Biogeogr 25:729–738

    Article  Google Scholar 

  • Hargreaves AL, Samis KE, Eckert CG (2014) Are species’ range limits simply niche limits writ large? A review of transplant experiments beyond the range. Am Nat. doi: https://doi.org/10.1086/674525

  • IBGE - Instituto Brasileiro de Geografia e Estatística. (2010) Relatório 2010. Available at http://www.ibge.gov.br. accessed 5 March 2012

  • Kabir M, Abolfathi M, Hajimoradloo A et al (2014) Effect of mangroves on distribution, diversity and abundance of molluscs in mangrove ecosystem: a review. AACL Bioflux 7:286–300

    Google Scholar 

  • Koch V, Wolff M (2002) Energy budget and ecological role of mangrove epibenthos in the Caeté estuary, North Brazil. Mar Ecol Prog Ser. https://doi.org/10.3354/meps228119

  • Lee SY, Primavera JH, Dahdouh-Guebas F et al (2014) Ecological role and services of tropical mangrove ecosystems: a reassessment. Glob Ecol Biogeogr. https://doi.org/10.1111/geb.12155

  • Macintosh DJ, Ashton EC, Havanon S (2002) Mangrove rehabilitation and intertidal biodiversity: a study in the Ranong mangrove ecosystem, Thailand. Estuar Coast Shelf Sci. https://doi.org/10.1006/ecss.2001.0896

  • McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst. https://doi.org/10.1007/s11252-007-0045-4

  • Magnone L, Bessonart M, Gadea J, Salhi M (2015) Trophic relationships in an estuarine environment: a quantitative fatty acid analysis signature approach. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2014.12.033

  • Maia RC, Coutinho R (2013) The influence of mangrove structure on the spatial distribution of Melampus coffeus (Gastropoda: Ellobiidae) in Brazilian estuaries. Panam J Aquat Sci 8:21–29

    Google Scholar 

  • Melo KR, Tagliaro CH, Beasley CR (2013) Seasonal changes in the subtidal benthic macrofauna of a mangrove coast in northern Brazil. J Coast Res. https://doi.org/10.2112/SI65-016.1

  • Morrisey DJ, Turner SJ, Mills GM et al (2003) Factors affecting the distribution of benthic macrofauna in estuaries contaminated by urban runoff. Mar Environ Res. https://doi.org/10.1016/s0141-1136(02)00211-8

  • Muniz P, Venturini N (2005) Macrobenthic communities in a temperate urban estuary of high dominance and low diversity: Montevideo Bay (Uruguay). Ocean Bol Inf del Mar 13:9–20

    Google Scholar 

  • Muniz P, Venturini N, Borja A (2015) Marine pollution and assessment of marine status in Latin America. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2014.12.057

  • Muniz P, Venturini N, Hutton M et al (2011) Ecosystem health of Montevideo coastal zone: a multi approach using some different benthic indicators to improve a ten-year-ago assessment. J Sea Res 65. https://doi.org/10.1016/j.seares.2010.07.001

  • Nagelkerken I, Blaber SJM, Bouillon S et al (2008) The habitat function of mangroves for terrestrial and marine fauna: a review. Aquat Bot. https://doi.org/10.1016/j.aquabot.2007.12.007

  • Negrete L, Colpo KD, Brusa F (2014) Land planarian assemblages in protected areas of the interior Atlantic forest: implications for conservation. PLoS One. https://doi.org/10.1371/journal.pone.0090513

  • Netto SA, Gallucci F (2003) Meiofauna and macrofauna communities in a mangrove from the Island of Santa Catarina, South Brazil. Hydrobiologia. https://doi.org/10.1023/B:HYDR.0000007304.22992.b2

  • Netto SA, Lana PC (1997) Intertidal zonation of benthic macrofauna in a subtropical salt marsh and nearby unvegetated flat (SE Brazil). Hydrobiologia. https://doi.org/10.1023/A:1003090701675

  • Pagliosa PR, Barbosa FAR (2006) Assessing the environment-benthic fauna coupling in protected and urban areas of southern Brazil. Biol Conserv 129:408–417. https://doi.org/10.1016/j.biocon.2005.11.008

    Article  Google Scholar 

  • Pérez-Reyes O, Crowl TA, Covich AP (2016) Comparison of decapod communities across an urban-forest land use gradient in Puerto Rican streams. Urban Ecosyst. https://doi.org/10.1007/s11252-015-0490-4

  • Pinheiro MAA, Duarte LFA, Toledo TR et al (2013) Habitat monitoring and genotoxicity in Ucides cordatus (Crustacea: Ucididae), as tools to manage a mangrove reserve in southeastern Brazil. Environ Monit Assess. https://doi.org/10.1007/s10661-013-3172-9

  • Pinheiro MAA, PPG e S, Duarte LF de A et al (2012) Accumulation of six metals in the mangrove crab Ucides cordatus (Crustacea: Ucididae) and its food source, the red mangrove Rhizophora mangle (Angiosperma: Rhizophoraceae). Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2012.05.004

  • Polidoro BA, Carpenter KE, Collins L et al (2010) The loss of species: mangrove extinction risk and geographic areas of global concern. PLoS One. https://doi.org/10.1371/journal.pone.0010095

  • Pons L, Fiselier JL (1991) Sustainable development of mangroves. Landsc UrbanPlanning 20:103–109

    Article  Google Scholar 

  • Printrakoon C, Wells FE, Chitramvong Y (2008) Distribution of molluscs in mangroves at six sites in the upper Gulf of Thailand. Raffles Bull Zool 18:247–257

    Google Scholar 

  • Reiss H, Kröncke I (2005) Seasonal variability of infaunal community structures in three areas of the North Sea under different environmental conditions. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2005.06.008

  • Rodrigues CAL, Ribeiro RP, Santos NB, Almeida ZS (2016) Patterns of mollusc distribution in mangroves from the Sao Marcos Bay, coast of Maranhao State, Brazil. Acta Amaz. https://doi.org/10.1590/1809-4392201600493

  • Salmo SG, Tibbetts I, Duke NC (2017) Colonization and shift of mollusc assemblages as a restoration indicator in planted mangroves in the Philippines. Biodivers Conserv. https://doi.org/10.1007/s10531-016-1276-6

  • Skilleter GA, Warren S (2000) Effects of habitat modification in mangroves on the structure of mollusc and crab assemblages. J Exp Mar Bio Ecol. https://doi.org/10.1016/S0022-0981(99)00133-1

  • Souza F, Brauko K, Lana P et al (2013) The effect of urban sewage on benthic macrofauna: a multiple spatial scale approach. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2012.10.021

  • Spalding MD, Blasco F, Field CD (1997) World mangrove atlas. International Society for Mangrove Ecosystems, Okinawa

    Google Scholar 

  • Surguio K (1973) Introdução à sedimentologia. Edgard Blucher, Editora da USP, São Paulo

  • Valiela I, Bowen JL, York JK (2001) Mangrove forests: one of the world’s threatened major tropical environments. Bioscience. https://doi.org/10.1641/0006-3568(2001)051[0807:MFOOTW]2.0.CO;2

  • Venturini N, Pita AL, Brugnoli E et al (2012) Benthic trophic status of sediments in a metropolitan area (Rio de la Plata estuary): linkages with natural and human pressures. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2011.08.016

  • Vilardy S, Polanía J (2002) Mollusc fauna of the mangrove root-fouling community at the Colombian Archipelago of San Andres and Old Providence. Wetl Ecol Manag. https://doi.org/10.1023/A:1020167428154

  • Villar S, Kandratavicius N, Martinez S, Muniz P (2011) Single cell gel electrophoresis as a tool to assess genetic damage in Heleobia cf. australis (Mollusca: Gastropoda) as sentinel for industrial and domestic pollution in Montevideo bay (Uruguay). Brazilian J Oceanogr. https://doi.org/10.5935/0101-2800.20140068

  • Walters BB, Rönnbäck P, Kovacs JM et al (2008) Ethnobiology, socio-economics and management of mangrove forests: a review. Aquat Bot. https://doi.org/10.1016/j.aquabot.2008.02.009

  • Wells FE (1984) Comparative distribution of macromolluscs and macrocrustaceans in a north-western Australian mangrove system. Mar Freshw Res. https://doi.org/10.1071/MF9840591

  • Wentworth CK (1922) A scale of grade and class terms for clastic sediments. J Geol 30:377–392

    Article  Google Scholar 

Download references

Acknowledgements

We thank Leonardo Mesquita and Dra. Barbara Valentas for their invaluable help with fieldwork and species identification. We also thank the organization COTEC - Comissão Técnico Científica for the field license grant and the university UNESP - Universidade Estadual Paulista, Campus Experimental do Litoral Paulista, for the infrastructure, which has made possible to develop the study.

Funding

This study was supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo), proc. no. 2011/01493-5, and in part by FAPESP, proc. no. 2010/11253-9.

Author information

Authors and Affiliations

  1. Instituto de Biociências, Departamento de Zoologia, Universidade de São Paulo, Rua do Matão, trav. 14, no. 321, São Paulo, 05508-090, Brazil

    Luiza de Oliveira Saad

  2. Universidade Metropolitana de Santos, Ave. Conselheiro Nébias 536, Santos, SP, 11045-002, Brazil

    Carlo Magenta Cunha

  3. Instituto de Limnología Dr. Raúl A. Ringuelet. CONICET, Universidad Nacional de La Plata, 1900, La Plata, Argentina

    Karine Delevati Colpo

Authors
  1. Luiza de Oliveira Saad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlo Magenta Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karine Delevati Colpo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luiza de Oliveira Saad.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements.

Additional information

Communicated by S. E. Lluch-Cota

Electronic supplementary material

ESM 1

(DOCX 941 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saad, L.O., Cunha, C.M. & Colpo, K.D. How mollusk assemblages respond to different urbanization levels: characterization of the malacofauna in subtropical Brazilian mangroves. Mar Biodiv 49, 989–999 (2019). https://doi.org/10.1007/s12526-018-0883-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-018-0883-8

Keywords

Search

Navigation