Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-13T04:18:47.129Z Has data issue: false hasContentIssue false
  • English
  • Français

Macrobenthic fauna associated with Diopatra cuprea (Onuphidae: Polychaeta) tubes on a macrotidal sandy beach of the Brazilian Amazon Coast

Published online by Cambridge University Press:  25 September 2018

T.M.T. Santos Open the ORCID record for T.M.T. Santos [Opens in a new window]  and
D. Aviz Open the ORCID record for D. Aviz [Opens in a new window]
T.M.T. Santos*
Affiliation:
Grupo de Estudos de Nematoda Aquáticos, Laboratório de Pesquisa em Monitoramento Ambiental Marinho, Universidade Federal do Pará. Av. Augusto Corrêa s/n, Guamá, Belém, PA. CEP: 66075-110, Brazil
D. Aviz
Affiliation:
Laboratório de Oceanografia Biológica, Instituto de Geociência, Universidade Federal do Pará, Av. Augusto Corrêa s/n, Guamá, Belém, PA. CEP: 66075-110, Brazil
*
Author for correspondence: T.M.T. Santos, E-mail: thuareag@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Tube-building polychaetes are an important group of marine bioengineers in soft-bottom habitats, where they provide structures that potentially influence the composition of the benthic community. The present study investigated the effects of Diopatra cuprea tubes on the structure of the macrobenthic fauna found on a sandy beach of the Amazon coast. Samples were collected in June (rainy season) and September (dry season) 2012 in two different areas: (1) an area in which D. cuprea tubes were present, and (2) a control area, in which worm tubes were absent. A total of 53 taxa were found, of which 30 were associated exclusively with D. cuprea tubes. While large aggregations of D. cuprea were not found in the study area, the presence of even a single tube may have a significant influence on the environmental conditions available for other organisms, especially those adapted to consolidated or muddy substrates. The two areas presented different seasonal patterns. A significant increase in the abundance and richness of the macrofauna was observed in area 1 in the rainy season, when the density of worm tubes increased and the hydrodynamic conditions were less intense. The results of the study highlight the importance of this organism as an ecosystem engineer on the sandy beaches of the Amazon coast.

Keywords

Benthosecosystem engineeringestuaryworm tubes
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 4 , June 2019 , pp. 751 - 759
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Attolini, FS, Flynn, MN and Tararam, AS (1997) Influence of Spartina alterniflora and tide level on the structure of polychaete associations in a euryhaline salt marsh in Cananéia lagoon estuarine region (SE Brazil). Revista Brasileira de Oceanografia 45, 25–34.Google Scholar
Bailey-Brock, J (1984) Ecology of the tube-building polychaete Diopatra leuckarti Kinberg, 1865 (Onuphidae) in Hawaii: community structure, and sediment stabilizing properties. Zoological Journal of the Linnean Society 80, 191–199.Google Scholar
Beasley, CR, Fernandes, CM, Gomes, CP, Brito, BA, Santos, SML and Tagliaro, CH (2005) Molluscan diversity and abundance among coastal habitats of northern Brazil. Ecotropica 11, 9–20.Google Scholar
Beasley, CR, Fernandes, MEB, Figueira, EAG, Sampaio, DS, Melo, KR and Barros, RS (2010) Mangrove infauna and sessile epifauna. In Saint-Paul, U and Schineider, H (eds), Mangrove Dynamics and Management in North Brazil. Berlin: Springer, pp. 109–123.Google Scholar
Bell, SS (1985) Habitat complexity of polychaete tube-caps: influence of architecture dynamics of meioepibenthic assemblage. Journal of Marine Research 43, 647–671.Google Scholar
Bell, SS and Coen, LD (1982 a) Investigations on epibenthic meiofauna. II. Influence of microhabitat and macroalgae on abundance of small invertebrates of Diopatra cuprea tube-caps in Virginia. Journal of Experimental Marine Ecology 61, 175–188.Google Scholar
Bell, SS and Coen, LD (1982 b) Investigations on epibenthic meiofauna. I. Abundances on and repopulation of the tube caps of Diopatra cuprea (Polychaeta: Onuphidae). Marine Biology 67, 303–309.Google Scholar
Bell, SS and Devlin, DJ (1983) Short-term macrofaunal recolonization of sediment and epibenthic habitats in Tampa Bay Florida. Bulletin of Marine Science 33, 102–108.Google Scholar
Bell, SS and Woodin, SA (1984) Community unity: experimental evidence for meiofauna and macrofauna. Journal of Marine Research 42, 605–632.Google Scholar
Berke, SK and Woodin, SA (2008) Tube decoration may not be cryptic for Diopatra cuprea (Polychaeta: Onuphidae). Biological Bulletin 214, 50–56.Google Scholar
Berke, SK, Mahon, ARF, Lima, P, Halanych, KM, Wethey, DS and Woodin, SA (2010) Range shifts and species diversity in marine ecosystem engineers: patterns and predictions for European sedimentary habitats. Global Ecology and Biogeography 19, 223–232.Google Scholar
Bolam, SG and Fernandes, TF (2003) Dense aggregations of tubebuilding polychaetes: response to small-scale disturbances. Journal of Experimental Marine Biology and Ecology 269, 197–222.Google Scholar
Braga, CF, Monteiro, VF, Rosa-Filho, JS and Beasley, CR (2011) Benthic macroinfaunal assemblages associated with Amazonian saltmarshes. Wetlands Ecology and Management 19, 257–272.Google Scholar
Braga, CF, Silva, RF, Rosa-Filho, JS and Beasley, CR (2013) Spatio-temporal changes in macroinfaunal assemblages of tropical saltmarshes, northern Brazil. Pan-American Journal of Aquatic Sciences 8, 282–298.Google Scholar
Breitburg, DL, Crump, BC, Dabiri, JO and Gallegos, CL (2010) Ecosystem engineers in the pelagic realm: alteration of habitat by species ranging from microbes to jellyfish. Integrative and Comparative Biology 50, 188–200.10.1093/icb/icq051Google Scholar
Buchanan, JB (1984) Sediment analysis. In Holme, NA and McIntyre, AD (eds), Methods for the Study of Marine Benthos. Oxford: Blackwell Scientific Publications, pp. 41–65.Google Scholar
Budaeva, N and Fauchald, K (2008) Diopatra tuberculantennata: a new species of Onuphidae (Polychaeta) from Belize with a key to onuphids from the Caribbean Sea. Zootaxa 1795, 29–45.Google Scholar
Callaway, R (2003) Long-term effects of imitation polychaete tubes on benthic fauna: they anchor Mytilus edulis (L.) banks. Journal of Experimental Marine Biology and Ecology 283, 115–132.Google Scholar
Callaway, R (2006) Tube worms promote community change. Marine Ecology Progressive Series 30, 849–860.Google Scholar
Callaway, R, Desroy, N, Dubois, SF, Fournier, J, Frost, M, Godet, L, Hendrick, VJ and Rabaut, M (2010) Ephemeral bio-engineers or reef-building polychaetes: how stable are aggregations of the tube worm Lanice conchilega (Pallas 1766). Integrative and Comparative Biology 50, 237–250.10.1093/icb/icq060Google Scholar
Carey, DA (1983) Particle resuspension in the benthic boundary layer induced by flow around polychaete tubes. Canadian Journal of Fisheries and Aquatic Sciences 40, 301–330.Google Scholar
Çinar, ME, Fauchald, K and Dagli, E (2014) Occurrence of Diopatra marocensis (Annelida, Onuphidae) in the eastern Mediterranean. ZooKeys 445, 1–11.Google Scholar
Commito, JA, Como, C, Grupe, BM and Dowa, WE (2008) Species diversity in the soft-bottom intertidal zone: biogenic structure sediment and macrofauna across mussel bed spatial scales. Journal of Experimental Marine Biology and Ecology 366, 70–81.Google Scholar
Crooks, JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97, 153–166.Google Scholar
Dagli, E, Ergen, Z and Çinar, ME (2005) One-year observation on the population structure of Diopatra neapolitana Delle Chiaje (Polychaeta Onuphidae) in Izmir Bay (Aegean Sea, eastern Mediterranean). Marine Ecology 26, 265–272.Google Scholar
Dauer, DM, Tourtelotte, GH and Ewing, RM (1982) Oyster shells and artificial worm tubes: the role of refuge in structuring benthic communities of the lower Chesapeake Bay. Hydrobiology 67, 661–677.Google Scholar
Dittmar, T and Lara, RJ (2001) Driving forces behind nutrient and organic matter dynamics in a mangrove tidal creek in North Brazil. Estuarine Coastal and Shelf Science 52, 249–259.Google Scholar
Dubois, S, Retière, C and Olivier, F (2002) Biodiversity associated with Sabellaria alveolata (Polychaeta: Sabellariidae) reefs: effects of human disturbances. Journal of the Marine Biological Association of the United Kingdom 82, 817–826.Google Scholar
Eckman, JE (1983) Hydrodynamic processes affecting benthic recruitment. Limnology and Oceanography 28, 241–257.10.4319/lo.1983.28.2.0241Google Scholar
Eckman, JE, Nowell, ARM and Jumars, PA (1981) Sediment destabilization by animal tubes. Journal of Marine Research 39, 361–374.Google Scholar
Flynn, MN, Wakabara, Y and Tararam, AS (1998) Macrobenthic associations of the lower and upper marshes of a tidal flat colonized by Spartina alterniflora in Cananéia lagoon estuarine region (southeastern Brazil). Bulletin of Marine Science 63, 427–442.Google Scholar
Folk, RL and Ward, WC (1957) Brazos River Bar: a study in the significance of grain size parameters. Journal of Sedimentary Petrology 27, 3–26.Google Scholar
Friederichs, M, Graf, G and Springer, B (2000) Skimming flow induced over a simulated polychaete tube lawn at low population densities. Marine Ecology Progress Series 192, 219–228.Google Scholar
Guilherme, BC, Silva, GB, El-Deir, ACA and Santos, PJP (2011) Meiofauna associada ao tubo de Diopatra cuprea Bosc 1902 (Polychaeta: Onuphidae). Revista Brasileira de Zoologia 5, 37–52.Google Scholar
Hartman, O (1969) Atlas of the Sedentariate Polychaetous Annelids from California. Los Angeles: Allan Hancock Foundation, University of Southern California.Google Scholar
Jaeger, JM and Nittrouer, CA (1995) Tidal controls on the formation of fine-scale sedimentary strata near the Amazon River mouth. Marine Geology 125, 259–281.Google Scholar
Jones, CG, Lawton, JH and Shachak, M (1994) Organisms as ecosystem engineers. Oikos 69, 373–386.Google Scholar
Jones, CG, Lawton, JH and Shachak, M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78, 1946–1957.Google Scholar
Jumars, PA and Nowell, ARM (1984) Fluid and sediment dynamic effect on marine benthic community structure. American Zoologist 24, 44–55.Google Scholar
Khaitov, VM, Fokin, MV and Nicolaeva, AM (1999) Structure of communities associated with dense assemblages of the tube-dwelling polychaete Polydora quadrilobata Jacobi (Spionidae) in the White Sea. Hydrobiologia 393, 221–226.Google Scholar
Lana, PC, Guiss, C and Disaró, ST (1991) Seasonal variation of biomass and production dynamics for above and below-ground components of a Spartina alterniflora marsh in the euhaline sector of Paranaguá Bay (SE Brazil). Estuarine, Coastal and Shelf Science 32, 231–241.10.1016/0272-7714(91)90017-6Google Scholar
Luckenbach, MW (1986) Sediment stability around animal tubes: the roles of hydrodynamic processes and biotic activity. Limnology and Oceanography 31, 779–787.Google Scholar
Mangum, CP, Santos, LS and Rhodes, WR (1968) Distribution and feeding in the Onuphid polychaete, Diopatra cuprea (Bosc). Marine Biology 2, 33–40.Google Scholar
Martorano, LG, Pereira, LC, César, EGM and Pereira, ICB (1993) Estudos Climáticos do Estado do Pará: Classificação Climática (Köppen) e Deficiência Hídrica (Thornthwaite, Mather). Belém: Sudam/Embrapa/SNLCS.Google Scholar
Matsui, GY, Ringelberg, DB and Lovell, CR (2004) Sulfate-reducing bacteria in tubes constructed by the marine infaunal polychaete Diopatra cuprea. Applied and Environmental Microbiology 70, 7053–7065.Google Scholar
Mendes, AC (2005) Geomorfologia e sedimentologia. In Fernandes, MEB (ed.), Os Manguezais da Costa Norte Brasileira. Vol. 2. Belém: Fundação Rio Bacanga, pp. 13–31.Google Scholar
Moraes, BC, Costa, JMN, Costa, ACL and Costa, MH (2005) Variação espacial e temporal da precipitacão no Estado do Pará. Acta Amazonica 35, 207–214.10.1590/S0044-59672005000200010Google Scholar
Morais, GC and Lee, JT (2013) Intertidal benthic macrofauna of rare rocky fragments in the Amazon region. Revista de Biología Tropical 62, 69–86.Google Scholar
Myers, AC (1972) Tube-worm-sediment relationships of Diopatra cuprea (Polychaeta: Onuphidae). Marine Biology 17, 350–356.Google Scholar
Peckol, P and Baxter, D (1986) Population dynamics of the onuphid polychaete Diopatra cuprea (Bose) along a tidal exposure gradient. Estuarine, Coastal and Shelf Science 22, 371–377.Google Scholar
Pereira, LCC, Mendes, CM, Monteiro, MDC and Asp, NE (2009) Morphological and sedimentological changes in a macrotidal sand beach in the Amazon Littoral (Vila dos Pescadores, Pará, Brazil). Journal of Coastal Research 56, 113–117.Google Scholar
Pereira, LCC, Sozinho da Silva, NI, da Costa, RM, Asp, NE, da Costa, KG and Vila-Concejo, A (2012) Seasonal changes in oceanographic processes at an equatorial macrotidal beach in northern Brazil. Continental Shelf Research 43, 95–106.Google Scholar
Phillips, TM and Lovell, CR (1999) Distribution of total and active bacteria in biofilms lining tubes of the onuphid polychaete Diopatra cuprea. Marine Ecology Progress Series 183, 169–178.10.3354/meps183169Google Scholar
Rabaut, M, Guilini, K, Van Hoey, G, Magda, V and Degraer, S (2007) A bio-engineered soft-bottom environment: the impact of Lanice conchilega on the benthic species-specific densities and community structure. Estuarine Coastal and Shelf Science 75, 525–536.Google Scholar
Rosa Filho, JS, Almeida, MF and Aviz, DE (2009) Spatial and temporal changes in the benthic fauna of a macrotidal Amazon sandy beach, Ajuruteua, Brazil. Journal of Coastal Research 56, 1796–1780.Google Scholar
Rosa Filho, JS, Busman, DV, Viana, AP, Gregório, AM and Oliveira, DM (2006) Macrofauna bentônica de zonas entre-marés não vegetadas do estuário do rio Caeté (Bragança-PA). Boletim do Museu Paraense Emilio Goeldi. Zoologia 2, 109–121.Google Scholar
Rosa Filho, JS, Gomes, TP, Almeida, MF and Silva, RF (2011) Benthic fauna of macrotidal sandy beaches along a small-scale morphodynamic gradient on the Amazon coast (Algodoal Island, Brazil). Journal of Coastal Research 64, 435–439.Google Scholar
Silva, NIS, Pereira, LCC, Gorayeb, A, Vila-Concejo, A, Sousa, RC, Asp, NE and Costa, RM (2011) Natural and social conditions of Princesa, a macrotidal sandy beach on the Amazon Coast of Brazil. Journal of Coastal Research 64, 1979–1983.Google Scholar
Souza-Filho, PWM, Lessa, GC, Cohen, MCL, Costa, FR and Lara, RF (2009) The subsiding macrotidal barrier estuarine system of the Eastern Amazon coast, northern Brazil. Lectures Notes in Earth Sciences 107, 347–375.10.1007/978-3-540-44771-9_11Google Scholar
Suguio, K (1973) Introdução à sedimentologia. São Paulo: Edgard Blucher.Google Scholar
Thomsen, MS (2004) Species, thallus size and substrate determine macroalgal break force and break location in a low-energy soft-bottom lagoon. Aquatic Botany 80, 153–161.Google Scholar
Thomsen, MS and McGlathery, KJ (2005) Facilitation of macroalgae by the sedimentary tube forming polychaete Diopatra cuprea. Estuarine Coastal and Shelf Science 62, 63–73.Google Scholar
Thomsen, MS, McGlathery, KJ, Schwarzschild, A and Silliman, BR (2009) Distribution and ecological role of the non-native macroalga Gracilaria vermiculophylla in Virginia salt marshes. Biological Invasions 11, 2303–2316.Google Scholar
Thomsen, MS, Wernberg, T, Altieri, A, Tuya, F, Gulbransen, D, McGlathery, K, Holmer, M and Silliman, BR (2010) Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integrative and Comparative Biology 50, 158–175.Google Scholar
Thomsen, MS, Muth, MF and McGlathery, KJ (2011) Tube-forming polychaetes enhance invertebrate diversity and abundance in sandy sediments of Mozambique Africa. African Journal of Marine Science 33, 327–332.Google Scholar
Toupoint, N, Godet, L, Fournier, J, Retiere, C and Olivier, F (2008) Does Manila clam cultivation affect habitats of the engineer species Lanice conchilega (Pallas, 1766)? Marine Pollution Bulletin 56, 1429–1438.Google Scholar
Van Hoey, G, Guilini, K, Rabaut, M, Vincx, M and Degraer, S (2008) Ecological implications of the presence of the tube-building polychaete Lanice conchilega on soft-bottom benthic ecosystems. Marine Biology 154, 1009–1019.Google Scholar
Woodin, SA (1978) Refuges disturbance and community structure: a marine soft-bottom example. Ecology 59, 274–284.Google Scholar
Woodin, SA, Wethey, DS and Volkenborn, N (2010) Infaunal hydraulic ecosystem engineers: cast of characters and impacts. Society for Integrative and Comparative Biology 50, 176–187.Google Scholar
Supplementary material: File

Santos and Aviz supplementary material

Santos and Aviz supplementary material 1

Download Santos and Aviz supplementary material(File)
File 22.3 KB