Abstract
Aquatic ecosystems are fundamentally altered by nutrient enrichment, and effective monitoring tools are needed to detect biological responses especially in the early stages of eutrophication. We tested the utility of biological trait analysis (BTA) to quantify the temporal responses of nematodes inhabiting salt marsh creeks that were experimentally enriched with nutrients for 6 years. Feeding, body shape, and tail shape traits were characterized on >6000 nematodes from annual samples from enriched and non-enriched sites. Here, we ask if trait combinations are more effective than single traits in detecting the magnitude and rate of change. We also sought to identify combinations of traits that best distinguish natural from nutrient-induced variation. BTA revealed that feeding, body shape, and all traits combined equally detected the response to nutrient enrichment. Compared to single traits however, BTAs were more sensitive to temporal trends and better distinguished natural variation from the response to nutrient enrichment. Tail shape traits (that might respond to altered sediment texture or geochemistry) were not affected by enrichment, and feeding traits yielded the greatest difference between enriched and reference communities indicating that changes in food resources drove responses. Feeding traits provided the highest quality information content in our study, and the use of feeding traits alone may adequately identify anthropogenic effects in many studies. However, we caution that body shape, tail shape, and feeding traits were strongly interrelated at our study site, and a diversity of trait groups may increase the information content of BTAs in more diverse habitats.
Similar content being viewed by others
References
Alves, A. S., Adão, H., Ferrero, T. J., Marques, J. C., Costa, M. J., & Patrício, J. (2013). Benthic meiofauna as indicator of ecological changes in estuarine ecosystems: the use of nematodes in ecological quality assessment. Ecological Indicators, 24, 462–475.
Alves, A. S., Verissimo, H., Costa, M. J., & Marques, J. C. (2014). Taxonomic resolution and biological traits analysis (BTA) approaches in estuarine free-living nematodes. Estuarine, Coastal and Shelf Science, 138, 69–78.
Anderson, M.J. (2005). PERMANOVA. Permutational multivariate analysis of variance. A computer program. Department of Statistics University of Auckland. pp, 1–24.
Ax, P. (1963). Die Ausbildung eines Schwanzfadens in der interstitiellen Sandfauna und die Venvertbarkeit von Lebensformcharakteren fir die Verwandt- schaftsformschung. Zoologischer Anzeiger, 171, 51–76.
Bolam, S. G. (2014). Macrofaunal recovery following the intertidal recharge of dredged material: a comparison of structural and functional approaches. Marine Environment Research, 97, 15–29.
Bongers, T. (1990). The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia, 38, 14–19.
Bongers, T., Alkemade, R., & Yeates, G. W. (1991). Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the maturity index. Marine Ecology Progress Series, 76, 135–142.
Bremner, J., Rogers, S. I., & Frid, C. L. J. (2003). Assessing functional diversity in marine benthic ecosystems: a comparison of approaches. Marine Ecological Progress Series, 254, 11–25.
Bremner, J., Rogers, S. I., & Frid, C. L. J. (2006). Methods for describing ecological functioning of marine benthic assemblages using biological traits analysis (BTA). Ecological Indices, 6, 609–622.
Brustolin, M. C., Thomas, M. C., & Lana, P. C. (2012). A functional and morphological approach to evaluate the vertical migration of estuarine intertidal nematodes during tidal cycle. Helgoland Marine Research. doi:10.1007/s10152-012-0306-3.
Cloern, J. E. (2001). Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series, 210, 223–253.
Cooper, K. M., Barrio Froján, C. R. S., Defew, E., Curtis, M., Fleddum, A., Brooks, L., & Paterson, D. M. (2008). Assessment of ecosystem function following marine aggregate dredging. Journal of Experimental Marine Biology and Ecology, 366, 82–91.
Culhane, F. E., Briers, R. A., Tett, P., & Fernandes, T. F. (2014). Structural and functional indices show similar performance in marine ecosystem quality assessment. Ecological Indicators, 43, 271–280.
Deegan, L. A., Bowen, J. L., Drake, D., Fleeger, J. W., Friedeichs, C. T., Galvan, K. A., Hobbie, J. E., Hopkinson, C., Johnson, D. J., May, L. E., Miller, E., Peterson, B. J., Picard, C., Sheldon, S., Sutherland, M., Vallino, J., & Warren, R. S. (2007). Susceptibility of salt marshes to nutrient enrichment and predator removal. Ecological Applications, 17, S42–S63.
Deegan, L. A., Johnson, D. S., Warren, R. S., Peterson, B. J., Fleeger, J. W., Fagherazzi, S., & Wollheim, W. (2012). Coastal eutrophication as a driver of saltmarsh loss. Nature, 490, 388–394.
Diaz, S., & Cabido, M. (2001). Vive la differénce: plant functional diversity matters to ecosystem functioning (review article). Trends in Ecology & Evolution, 16, 646–655.
Dolédec, S., & Statzner, B. (2008). Invertebrate traits for biomonitoring of large European rivers: an assessment of specific types of human impact. Freshwater Biology, 53, 617–634.
Dolédec, S., Statzner, B., & Bournard, M. (1999). Species traits for future biomonitoring across ecoregions: patterns along a human-impacted river. Freshwater Biology, 42, 737–758.
Elliott, M., & Quintino, V. (2007). The Estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stresses areas. Marine Pollution Bulletin, 54, 640–645.
Fleeger, J. W., Carman, K. R., Weisenhorn, P. B., Sofranko, H., Marshall, T., Thistle, D., & Barry, J. P. (2006). Simulated sequestration of anthropogenic carbon dioxide at a deep-sea site: effects on nematode abundance and biovolume. Deep-Sea Research Part I: Oceanography Research, 53, 1135–1147.
Fleeger, J. W., Johnson, D. S., Galván, K. A., & Deegan, L. A. (2008). Top-down and bottom-up control of infauna varies across the saltmarsh landscape. Journal of Experimental Marine Biology and Ecology, 357, 20–34.
Fleeger, J. W., Johnson, D. S., Carman, K. R., Weisenhorn, P. B., Gabriele, A., & Thistle, D. (2010). The response of nematodes to deep-sea Co2 sequestration: a quantile regression approach. Deep Sea Research Part I: Oceanographic Research Papers, 57(5), 696–707.
Gambi, C., Vanreusel, A., & Danovaro, R. (2003). Biodiversity of nematode assemblages from deep-sea sediments of the Atacama slope and trench (South Pacific Ocean). Deep Sea Research, Part I, 50, 103–117.
Giere, O. (2009). Meiofauna from selected biotopes and regions. In Meiobenthology (2nd ed.). Berlin Heidelberg: Springer. doi:10.1007/b106489.
Grime, J. P. (1997). Biodiversity and ecosystem function: the debate continues. Science, 277, 1260–1261.
Jensen, P. (1987). Feeding ecology of free-living aquatic nematodes. Marine Ecology Progress Series, 35(1953), 187–196.
Kalogeropoulou, V., Keklikoglou, K., & Lampadariou, N. (2014). Functional diversity patterns of abyssal nematodes in the eastern Mediterranean: a comparison between cold seeps and typical deep sea sediments. Journal of Sea Research. doi:10.1016/j.seares.2014.11.003.
Kazemi-Dinan, A., Schroeder, F., Peters, L., Majdi, N., & Traunspurger, W. (2014). The effect of trophic state and depth on periphytic nematodecommunities in lakes. Liminologica, 44, 49–57.
Losi, V., Moreno, M., Gaozza, L., Vezzulli, L., Fabiano, M., & Albertelli, G. (2013). Nematode biomass and allometric attributes as indicators of environmental quality in a Mediterranean harbour (Ligurian Sea, Italy). Ecological Indicators, 30, 80–89. doi:10.1016/j.ecolind.2013.01.034.
Marchini, A., Munari, C., & Mistri, M. (2008). Functions and ecological status of eight Italian lagoons examined using biological traits analysis (BTA). Marine Pollution Bulletin, 56, 1076–1085.
Maurer, D. (2000). The dark side of the taxonomic sufficiency TS. Marine Pollution Bulletin, 40, 98–101.
McLusky, D. S., & Elliott, M. (2004). The estuarine ecosystem: ecology, threats and management (3rd ed., p. 216). Oxford: Oxford University Press.
McLusky, D. S., & Elliott, M. (2007). Transitional waters: a new approach, semantics or just muddying the waters? Estuarine, Coastal & Shelf Science, 71, 359–363.
Mitwally, H. M., & Fleeger, J. W. (2013). Long-term nutrient enrichment elicits a weak density response by saltmarsh meiofauna. Hydrobiologia, 713(1), 97–114.
Mitwally, H. M., & Fleeger, J. W. (2015). Long-term nutrient enrichment alters nematode trophic structure and body size in a Saprtina alterniflora saltmarsh. Marine Ecology, 36, 910–925.
Moens, T., Herman, P., Verbeeck, I., Steyaert, M., & Vincx, M. (2000). Predation rates and prey selectivity in two predacious estuarine nematode species. Marine Ecology Progress Series, 205, 185–193.
Moens, T., Bouillon, S., & Gallucci, F. (2005). Dual stable isotope abundances unravel trophic position of estuarine nematodes. Journal of the Marine Biological Association of the United Kingdom, 85, 1401–1407.
Munari, C. (2013). Benthic community and biological trait composition in respect to artificial coastal defense structures: a study case in the northern Adriatic sea. Marine Environmental Research, 90, 47–54.
Nilsson, P., Jönsson, B., Lindström Swanberg, I., & Sundbäck, K. (1991). Response of a marine shallow-water sediment system to an increased load of inorganic nutrients. Marine Ecology Progress Series, 71, 275–290.
Pascal, P.-Y., Fleeger, J. W., Boschker, H. T. S., Mitwally, H. M., & Johnson, D. S. (2013). Response of the benthic food web to short- and long-term nutrient enrichment in saltmarsh mudflats. Marine Ecology Progress Series, 474, 27–41.
Pereira, T. J., Arce, M. A. G. R., & Olivare, A. C. (2009). Direct nematode predation in the marine nematode Synonchiell Spiculora (Selachinematidae: Nematoda). Marine Biodiversity Records, 2, 1–4.
PRIMER-E 7. Computer soft ware version 7.0. 8. © Copyright (2015). PRIMER-E ltd, all rights reserved.
Revill, A. T., Jock, J. W., & Young, J. E. (2009). Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia. Marine Biology, 156, 1241–1253.
Riemann, F. (1974). On hemisessile nematodes with flagella-form tail living in marine soft bottoms and on micro-tubes found in deep sea sediments. Mikrofauna Meeresbodens, 40, 1–15.
Ristau, K., Spann, N., & Traunspurger, W. (2015). Species and trait compositions of fresh water nematodes as indicative descriptors of lake eutrophication. Ecological Indicators, 53, 196–205.
Ritter, A.N. (2012). Effect of eutrophication on benthic microalgae. Master thesis, Department of Biology, Middlebury College, Vermont, p, 51.
Schratzberger, M., Warr, K., & Rogers, S. I. (2007). Functional diversity of nematode communities in the southwestern North Sea. Marine Environmental Research, 63, 368–389.
Soetaert, K., Muthumbi, A., & Heip, C. (2002). Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns. Marine Ecology Progress Series, 242, 179–193.
Soetaert, K., Franco, M., Lamapadariou, N., Muthumbi, A., Steyaert, M., Vandepitte, L., Berghe, E. V., & Vanaverbeke, J. (2009). Factors affecting nematode biomass, length and width from the shelf to the deep sea. Marine Ecology Progress Series, 392, 123–132.
Somerfield, P. J., & Warwick, R. M. (1996). Meiofauna in marine pollution monitoring programmes. A laboratory manual (p. 71). Lowestoft: Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research.
Sundbäck, K., Alsterberg, C., & Larson, F. (2010). Effects of multiple stressors on marine shallow–water sediment microalgae and meiofauna to nutrient-toxicant exposure. Journal of Experimental Marine Biology and Ecology, 388, 39–50.
Thistle, D., & Sherman, K. M. (1985). The nematode fauna of a deep-sea site exposed to strong near-bottom currents. Deep Sea Research, 32(9), 1077–1088.
Thistle, D., Lambshead, P. J. D., & Sherman, K. M. (1995). Nematode tail- shape groups respond to environmental differences in the deep sea. Vie Milieu, 45, 107–115.
Tita, G., Vincx, M., & Desrosiers, G. (1999). Size spectra, body width and morphotypes of intertidal nematodes: an ecological interpretation. Journal of the Marine Biological Association of the United Kingdom, 79, 1007–1015.
Vanaverbeke, J., Steyaert, M., Vanreusel, A., & Vincx, M. (2003). Nematode biomass spectra as descriptors of functional changes to human and natural impact. Marine Ecology Progress Series, 249, 17–157.
Vanaverbeke, J., Steyaert, M., Soetaert, K., Rousseau, V., Van Gansbeke, D., Parent, J.-Y., & Vincx, M. (2004). Changes in structural and functional diversity of nematode communities during a spring phytoplankton bloom in the southern North Sea. Journal of Sea Research, 52, 281–292.
Vanaverbeke, J., Deprez, T., & Vincx, M. (2007). Changes in nematode communities at the long-term sand extraction of the Kwinte-bank (Southern Bight of the North Sea). Marine Pollution Bulletin, 54, 1351–1360.
Vanaverbeke, J., Merckx, B., Degraer, S., & Vincx, M. (2011). Sediment-related distribution patterns of nematodes and macrofauna: two sides of the benthic coin? Marine Environmental Research, 71, 31–40.
Wan Hussin, W. M. R., Cooper, K. M., Christorpher, R. S., Frojan, B., Defew, E. C., & Paterson, D. M. (2012). Impacts of physical disturbance on the recovery of a macrofaunal community: a comparative analysis using traditional and novel approaches. Ecological Indicators, 12(1), 37–45.
Wieser, W. (1953). Die Beziehung zwischenMundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebendenmarinenNematoden. Arkiv for Zoology, 2, 439–484.
Wilson, J. G., Fleeger, J. W. (2013). Estuarine benthos. In J. W Day, Jr., B. C. Crump, W. M Kemp, A. Yanez- Arncibia (Eds.). Estaurine ecology (pp. 303–325). Wiley.
Acknowledgments
The authors express their deep gratitude to the TIDE project leaders and its many participants for collecting samples and providing support necessary to maintain a demanding program of nutrient enrichment. We also thank Dr. Kevin Carman for graciously allowing us to use his laboratory with its facilities for nematode body size/shape measurements, trophic/tail identification, and photographs. We also thank Dr. J. Geagan for his help with statistical consultations at the early stages of the manuscript. The first author expresses her deep gratitude to the Fulbright commissions for support that allowed her to do this research in the USA. This material is based upon work supported by the National Science Foundation under Grant Nos. 0213767 and 9726921. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mitwally, H.M., Fleeger, J.W. A test of biological trait analysis with nematodes and an anthropogenic stressor. Environ Monit Assess 188, 140 (2016). https://doi.org/10.1007/s10661-016-5128-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-016-5128-3