Skip to main content
Log in

Nematode biomass and morphometric attributes as descriptors during a major Zostera noltii collapse

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Benthic nematodes are recognized as suitable organisms to provide valuable information on the potential ecological effects of natural and anthropogenic disturbances in aquatic ecosystems. The biomass and morphometric attributes of nematodes (body length, width, and length/width) collected in the Mira estuary (SW Portugal) were analysed before the collapse and during the natural recovery process of the Zostera noltii bed. In addition, their relationship with community characteristics and environmental variables was studied. Moreover, biomass and morphometric attributes were investigated for their potential use as a complementary tool to the classical descriptor “density” (from which several other descriptors are derived) when studying nematodes as biological indicators. Nematode biomass and morphometric attributes proved to be valuable as correlate with the environmental changes associated with the Z. noltii collapse. High values of nematode biomass, length, width, and length/width ratio were observed during the early recovery process of Z. noltii, contrasting with nematode densities, which showed consistently higher values before the collapse. These findings suggest that biomass and morphometric attributes indicate a functional adaptation of nematode communities to the new environmental conditions in the early recovery process of Z. noltii. Therefore, these traits may be used to provide complementary information to standing stocks of nematode assemblages so as to assess ecological changes over spatial and temporal scales in marine ecosystems, particularly within seagrass bed habitats.

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

Access this article

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

  • Adão H (2004) Dynamics of meiofauna communities in association with Zostera noltii seagrass beds in the Mira estuary (SW Portugal)

  • Almeida A (1994) Macrofauna acompanhante de zosteráceas. Importância na conservação do meio marinho. Museu Bocage

  • Alongi D (1987) Intertidal zonation and seasonality of meiobenthos in tropical mangrove estuaries. Mar Biol 95:447–458

    Article  Google Scholar 

  • Alves A, Adao H, Ferrero T, Marques J, Costa M, Patricio J (2013) Benthic meiofauna as indicator of ecological changes in estuarine ecosystems: the use of nematodes in ecological quality assessment. Ecol Indic 24:462–475. https://doi.org/10.1016/j.ecolind.2012.07.013

    Article  Google Scholar 

  • Alves A, Veríssimo H, Costa M, Marques J (2014) Taxonomic resolution and Biological Traits Analysis (BTA) approaches in estuarine free-living nematodes. Estuar Coast Shelf Sci 138:69–78

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA A + for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Andrade F (1986) O estuário do Mira: caracterização geral e análise quantitativa da estrutura dos macropovoamentos bentónicos, Lisbon, Portugal

  • Andrassy I (1956) The determination of volume and weight of nematodes. Acta Zool (Hungarian Academy of Science) 2:1–15

    Google Scholar 

  • Boström C, Bonsdorff E (1997) Community structure and spatial variation of benthic invertebrates associated with Zostera marina (L.) beds in the northern Baltic Sea. J Sea Res 37:153–166

    Article  Google Scholar 

  • Boström C, Jackson E, Simenstad C (2006) Seagrass landscapes and their effects on associated fauna: a review. Estuar Coast Shelf Sci 68:383–403

    Article  Google Scholar 

  • Chalcraft D, Resetarits W (2003) Mapping functional similarity of predators on the basis of trait similarities. Am Nat 162:390–402

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Clarke K, Green R (1988) Statistical design and analysis for a biological effects study. Mar Ecol Prog Ser 46:213–226

    Article  Google Scholar 

  • Clarke KR, Warwick RM (2001) Changes in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E Ltd, Plymouth

  • Costa J (2004) A biologia do xarroco, Halobatrachus didactylus (Bloch and Schneider, 1801), e o seu papel na estruturação e funcionamento das comunidades em que se insere; referência especial à população do estuário do Mira

  • Costa MJ, Santos CI, Costa HN (2002) Comparative analysis of a temperate and a tropical seagrass bed fish assemblages in two estuarine systems: the Mira estuary (Portugal) and the Mussulo lagoon (Angola). Cah Biol Mar 43:73–81

    Google Scholar 

  • Coull B (1988) The ecology of marine meiofauna. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institute Press, Washington

    Google Scholar 

  • Coull B (1999) Role of meiofauna in estuarine soft-bottom habitats. Aust J Ecol 24:327–343

    Article  Google Scholar 

  • Coull B, Chandler G (1992) Pollution and meiofauna: field, laboratory and mesocosm studies. Oceanogr Mar Biol 30:191–271

    Google Scholar 

  • Cunha A, Assis J, Serrão E (2013) Seagrass in Portugal: a most endangered marine habitat. Aquat Bot 104:193–203

    Article  Google Scholar 

  • Danovaro R, Gambi C, Dell’Anno A, Corinaidesi C, Fraschetti S, Vanreusel A, Vincx M, Gooday A (2008) Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss. Curr Biol 18:1–8

    Article  CAS  Google Scholar 

  • Duarte C, Borum J, Short F, Walker D (2008) Seagrass ecosystem: their global status and prospects. In: Polunin NVC (ed) Aquatic ecosystems: trend and global prospects. Cambridge University Press, Cambridge, pp 281–294

    Chapter  Google Scholar 

  • Edgar GJ, Shaw C, Watsona GF, Hammond L (1994) Comparisons of species richness, size structure and productions of benthos in vegetated and unvegetated habitats in Western Port, Victoria. J Exp Mar Bio Ecol 176:201–226

    Article  Google Scholar 

  • Fisher R, Sheaves M (2003) Community structure and spatial variability of marine nematodes in tropical Australian pioneer seagrass meadows. Hydrobiologia 495:143–158

    Article  Google Scholar 

  • Fleeger J, Grippo M, Pastorick S (2011) What is the relative importance of sediment granulometry and vertical gradients to nematode morphometrics? Mar Biol Res 7:122–134

    Article  Google Scholar 

  • Fonseca G, Hutchings P, Gallucci F (2011) Meiobenthic communities of seagrass beds (Zostera capricorni) and unvegetated sediments along the coast of New South Wales, Australia. Estuar Coast Shelf Sci 91:69–77

    Article  Google Scholar 

  • Gallucci F, Steyaert M, Moens T (2005) Can field distributions of marine predacious nematodes be explained by sediment constraints on their foraging success? Mar Ecol Prog Ser 304:167–178

    Article  Google Scholar 

  • Gerlach S (1953) Die Biozonotische gliederung der Nematodenfauna an den Deutschen Kusten. Zeitschrift für Morfologie und okologie der Tiere 41:411–512

    Article  Google Scholar 

  • Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments, 2nd edn. Springer, Berlin

    Google Scholar 

  • Green E, Short F (2003) World atlas of seagrasses. California University Press, California

    Google Scholar 

  • Guerrini A, Colangelo M, Ceccherelli V (1998) Recolonization patterns of meiobenthic communities in brackish vegetated and unvegetated habitats after induced hypoxia/anoxia. Hydrobiologia 375(376):73–87

    Article  Google Scholar 

  • Guilini K, Bezerra T, Eisendle-Flöckner U, Deprez T, Fonseca G, Holovachov O, Leduc D, Miljutin D, Moens T, Sharma J, Smol N, Tchesunov A, Mokievsky V, Vanaverbeke J, Vanreusel A, Venekey V, Vincx M (2016) NeMys: world database of free-living marine nematodes

  • Heip C, Vincx M, Vranken G (1985) The ecology of free-living nematodes. Oceanogr Mar Biol 23:399–489

    Google Scholar 

  • Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hendelberg M, Jensen P (1993) Vertical distribution of the nematode fauna in coastal sediment influenced by seasonal hypoxia in the bottom water. Ophelia 37:83–94

    Article  Google Scholar 

  • Hirst J, Attrill M (2008) Small is beautiful: an inverted view of habitat fragmentation in seagrass beds. Estuar Coast Shelf Sci 78:811–818

    Article  Google Scholar 

  • Hughes A, Williams S, Duarte C, Heck K, Waycott M (2009) Associations of concern: declining seagrasses and threatened dependent species. Front Ecol Environ 7:242–246

    Article  Google Scholar 

  • Jensen P (1984) Ecology of benthic and epiphytic nematodes in brackish waters. Hydrobiologia 108:201–217

    Article  Google Scholar 

  • Leduc D, Probert P, Nodder S (2010) Influence of mesh size and core penetration on estimates of deep-sea nematode abundance, biomass, and diversity. Deep Sea Res Part 1 Oceanogr Res Pap 57:1354–1362

    Article  Google Scholar 

  • Losi V, Moreno M, Gaozza L, Vezzulli L, Fabiano M, Alberteli G (2013) Nematode biomass and allometric attributes as indicators of environmental quality in a Mediterranean harbour (Ligurian Sea, Italy). Ecol Indic 30:80–89

    Article  CAS  Google Scholar 

  • Materatski P, Vafeiadou A, Ribeiro R, Moens T, Adão H (2015) A comparative analysis of benthic nematode assemblages from Zostera noltii beds before and after a major vegetation colapse. Estuar Coast Shelf Sci 167:256–268

    Article  Google Scholar 

  • Materatski P, Vafeiadou A-M, Moens T, Adão H (2016) Structural and functional composition of benthic nematode assemblages during a natural recovery process of Zostera noltii seagrass beds. Estuar Coast 39:1–13. https://doi.org/10.1007/s12237-016-0086-0

    Article  Google Scholar 

  • Metodik Limnologisk (1992) Københavns University, Ferksvandsbiologisk Laboratorium, Akademisk Forlag, Copenhagen

    Google Scholar 

  • Moens T, Vincx M (1997) Observations on the feeding ecology of estuarine nematodes. J Mar Biol Assoc UK 77:211–227

    Article  Google Scholar 

  • Moreno M, Ferrero T, Gallizia I, Vezzulli L, Albertelli G, Fabiano M (2008) An assessment of the spatial heterogeneity of environmental disturbance within an enclosed harbour through the analysis of meiofauna and nematode assemblages. Estuar Coast Shelf Sci 77:565–576

    Article  Google Scholar 

  • Ndaro S, Olafsson E (1999) Soft-bottom fauna with emphasis on nematode assemblage structure in a tropical intertidal lagoon in Zanzibar, eastern Africa: I. Spatial variability. Hydrobiologia 405:133–148

    Article  CAS  Google Scholar 

  • Norling K, Rosenberg R, Hulth S, Grémare A, Bonsdorff E (2007) Importance of functional biodiversity and species-specific traits of benthic fauna for ecosystem functions in marine sediment. Mar Ecol Prog Ser 332:11–23

    Article  CAS  Google Scholar 

  • Orth R, Carruthers T, Dennison W, Duarte C, Fourqurean J, Heck K, Hughes A, Kendrick G, Kenworthy W, Olyarnik S, Short F, Waycott M, Williams S (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

    Article  Google Scholar 

  • Parsons T, Maita Y, Lally C (1985) Pigments a manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, pp 101–104

    Google Scholar 

  • Platt H, Warwick R (1983) Free-living marine nematodes. Part I. British Enoplids. Cambridge University Press, Cambridge

    Google Scholar 

  • Platt H, Warwick R (1988) Free living marine nematodes. Part II: British chromadorids. Pictorial key to world genera and notes for the identification of British species, Leiden

  • Ratsimbazafy R, Boucher G, Dauvin J (1994) Mesures indirectes de la biomasse des nématodes du meiobenthos subtidal de la Manche. Cah Biol Mar 35: 511–523

  • Rede Natura (2000). http://www.icnf.pt/portal/pn/biodiversidade/rn2000/rn-pt. Accessed 23 Jan 2016

  • Romeyn K, Bouwman L (1983) Food selection and consumption by estuarine nematodes. Aquat Ecol 17:103–109

    Google Scholar 

  • Schratzberger M, Warr K, Rogers S (2007) Functional diversity of nematode communities in the southwestern North Sea. Mar Environ Res 63:368–389

    Article  CAS  Google Scholar 

  • Schratzberger M, Maxwell T, Warr K, Ellis J, Rogers S (2008) Spatial variability of infaunal nematode and polychaete assemblages in two muddy subtidal habitats. Mar Biol 153:621–642

    Article  Google Scholar 

  • Schwinghamer P (1983) Generating ecological hypothesis from biomass spectra using causal analysis: a benthic example. Mar Ecol Prog Ser 13:151–166

    Article  Google Scholar 

  • Sheppard C (2006) The muddle of “Biodiversity”. Mar Pollut Bull 52:123–124

  • Short F, Polidoro B, Livingstone S, Carpenter K, Bandeira S, Bujang J, Calumpong H, Carruthers T, Coles R, Dennison W, Erftemeijer P, Fortes M, Freeman A, Jagtap T, Kamal A, Kendrick G, Kenworthy W, La Nafie Y, Nasution I, Orth R, Prathep A, Sanciangco J, Van Tussenbroek B, Vergara S, Waycott M, Zieman J (2011) Extinction risk assessment of the world’s seagrass species. Biol Conserv 144:1961–1971

    Article  Google Scholar 

  • Smol N, Willems K, Govaere JCR, Sandee A (1994) Composition, distribution, biomass of meiobenthos in the Oosterschelde estuary (SW Netherlands). Hydrobiologia 282:197–217

    Article  Google Scholar 

  • Soetaert K, Vincx M, Wittoeck J, Tulkens M (1995) Meiobenthic distribution and nematode community structure in five European estuaries. Hydrobiologia 311:185–206

    Article  Google Scholar 

  • Soetaert K, Muthumbi A, Heip C (2002) Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns. Mar Ecol Prog Ser 242:179–193

    Article  Google Scholar 

  • Soetaert K, Franco M, Lampadariou N, Muthumbi A, Steyaert M, Vandepitte L, Vanden Berghe E, Vanaverbeke J (2009) Factors affecting nematode biomass, length and width from the shelf to the deep sea. Mar Ecol Prog Ser 392:123–132

    Article  Google Scholar 

  • Somerfield P, Gee J, Warwick R (1994) Soft sediment meiofaunal community structure in relation to a long-term heavy metal gradient in the Fal estuary system. Mar Ecol Prog Ser 105:79–88

    Article  CAS  Google Scholar 

  • Steyaert M, Garner N, Van Gansbeke D, Vincx M (1999) Nematode communities from the North Sea: environmental controls on species diversity and vertical distribution within the sediment. J Mar Biol Assoc UK 79:253–264

    Article  Google Scholar 

  • Steyaert M, Moodley L, Nadong T, Moens T, Soetaert K, Vincx M (2007) Responses of intertidal nematodes to short-term anoxic events. J Exp Mar Biol Ecol 345:175–184

    Article  CAS  Google Scholar 

  • Strickland J, Parsons T (1972) A practical handbook of seawater analysis. Fisheries Research Board of Canada, Ottawa

    Google Scholar 

  • Ter Braak C, Smilauer P (2002) CANOCO reference manual and CanoDraw for windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power, CANOCO, Ithaca, NY

    Google Scholar 

  • Thistle D, Sherman K (1985) The nematode fauna of a deep-sea site exposed to strong near-bottom currents. Deep Sea Res Part 1 Oceanogr Res Pap 32:1077–1088

    Article  Google Scholar 

  • Tietjen J (1976) Distribution and species diversity of deep-sea nematodes of North Carolina. Deep Sea Res Part 1 Oceanogr Res Pap 23:755–768

    Google Scholar 

  • Tietjen J (1980) Population structure and species composition of the free-living nematodes inhabiting sands on the New York Bight Apex. Estuar Coast Mar Sci 10:61–73

    Article  CAS  Google Scholar 

  • Tita G, Vincx M, Desrosier G (1999) Size spectra, body width and morphotypes of intertidal nematodes: an ecological interpretation. J Mar Biol Assoc UK 79:1007–1015

    Article  Google Scholar 

  • Tita G, Desrosiers G, Vincx M, Clément M (2002) Intertidal meiofauna of the St Lawrence estuary Quebec, Canada: diversity, biomass and feeding structure of nematode assemblages. J Mar Biol Assoc UK 82:779–791

    Article  Google Scholar 

  • Vafeiadou A, Materatski P, Adão H, De Troch M, Moens T (2013) Food sources of macrobenthos in an estuarine seagrass habitat (Zostera noltii) as revealed by dual stable isotope signatures. Mar Biol 160:2517–2523

    Article  Google Scholar 

  • Valle M, Chust G, del Campo A, Wisz M, Olsen S, Garmendia J, Borja A (2014) Projecting future distribution of the seagrass Zostera noltii under global warming and sea level rise. Biol Conserv 170:74–85

    Article  Google Scholar 

  • Van den Brink P, Ter Braak C (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18:138–148

    Article  Google Scholar 

  • Van den Brink P, van Wijngaarden R, Lucassen W, Brock T, Leeuwangh P (1996) Effects of the insecticide Dursban 14E (a.i. chlorpyrifos) in outdoor experimental ditches. II. Invertebrate community responses. Environ Toxicol Chem 15:1143–1153

    Article  Google Scholar 

  • Vanaverbeke J, Steyaert M, Vanreusel A, Vincx M (2003) Nematode biomass spectra as descriptors of functional changes due to human and natural impact. Mar Ecol Prog Ser 249:157–170

    Article  Google Scholar 

  • Vanaverbeke J, Soetaert K, Vincx M (2004) Changes in morphometric characteristics of nematode communities during a spring phytoplankton bloom deposition. Mar Ecol Prog Ser 273:139–146

    Article  Google Scholar 

  • Vanhove S, Vermeeren H, Vanreusel A (2004) Meiofauna towards the South Sandwich Trench (750–6300 m) focus on nematodes. Deep Sea Res Part 2 Top Stud Oceanogr 51:1665–1687

    Article  Google Scholar 

  • Vidakovic J, Bogut I (2004) Aquatic nematodes of Sakadaš lake (Kopački rit Nature Park, Croatia). Biologia 59:567–575

    Google Scholar 

  • Vincx M (1996) Meiofauna in marine and freshwater sediments. In: Hall GS (ed) Methods for the examination of organismal diversity in soils and sediments. Cabi Publishing, Wallingford, pp 187–195

    Google Scholar 

  • Ward S, Thomson N, White J, Brenner S (1975) Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160:313–337

    Article  CAS  Google Scholar 

  • Warwick RM (1971) Nematode associations in the Exe Estuary. J Mar Biol Assoc UK 51:439–454

    Article  Google Scholar 

  • Warwick R, Price R (1979) Ecological and metabolic studies on free-living nematodes from an estuarine mudflat. Estuar Coast Mar Sci 9:257–271

    Article  Google Scholar 

  • Warwick R, Clarke K, Suharsono (1990) A statistical analysis of coral community responses to the 1982–1983 El Nino in the Thousand Islands, Indonesia. Coral Reefs 8:171–179

    Article  Google Scholar 

  • Waycott M, Duarte C, Carruthers T, Orth R, Dennison W, Olyarnik S, Calladine A, Fourqurean J, Heck K, Hughes A, Kendrick G, Kenworthy W, Short F, Williams S (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381

    Article  CAS  Google Scholar 

  • Webster P, Rowden A, Attrill M (1998) Effect of shoot density on the infaunal macroinvertebrate community within a Zostera marina seagrass bed. Estuar Coast Shelf Sci 47:351–357

    Article  Google Scholar 

  • Wieser W (1959) The effect of grain size on the distribution of small invertebrates inhabiting the beaches of Puget Sound. Limnol Oceanogr 4:181–194

    Article  Google Scholar 

  • Wright J, Jones C (2006) The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. Bioscience 56:203–209

    Article  Google Scholar 

  • Zeppilli D, Sarrazin J, Leduc D, Arbizu PM, Fontaneto D, Fontanier C, Gooday AJ, Kristensen RM, Ivanenko VN, Sorensen MV, Vanreusel A, Thebault J, Mea M, Allio N, Andro T, Arvigo A, Castrec J, Danielo M, Foulon V, Fumeron R, Hermabessiere L, Hulot V, James T, Langonne-Augen R, Le Bot T, Long M, Mahabror D, Morel Q, Pantalos M, Pouplard E, Raimondeau L, Rio-Cabello A, Seite S, Traisnel G, Urvoy K, Van der Stegen T, Weyand M, Fernandes D (2015) Is the meiofauna a good indicator for climate change and anthropogenic impacts? Mar Biodivers 45(3):505–535

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Fundação para a Ciência e Tecnologia (FCT), through the research projects CoolNematode (FCT; EXPL/MAR-EST0553/2013) and ProMira (PROMAR; 31-03-02-FEP-006) and by the strategic project UID/MAR/04292/2013. P. Materatski and M. Moreira-Santos are grateful to the Portuguese Foundation for Science and Technology (FCT) for a doctoral (ref. SFRH/BD/65915/2009) and postdoctoral fellowship (ref. SFRH/BPD/99800/2014), both funded by Programa Operacional Potencial Humano of QREN Portugal (2007–2013 and 2014–2020, respectively) and by the Portuguese budget through the Ministry of Education and Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick Materatski.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: M. G. CHapman.

Reviewed by D. Zeppilli and undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Materatski, P., Ribeiro, R., Moreira-Santos, M. et al. Nematode biomass and morphometric attributes as descriptors during a major Zostera noltii collapse. Mar Biol 165, 24 (2018). https://doi.org/10.1007/s00227-018-3283-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3283-5

Navigation