Urban pollution of sediments: Impact on the physiology and burrowing activity of tubificid worms and consequences on biogeochemical processes

Abstract. One of the goals of urban ecology is to link community structure to ecosystem function in urban habitats. Pollution-tolerant wetland invertebrates have been shown to enhance greenhouse gas (GHG) flux in controlled laboratory experiments, suggesting that they may influence urban wetland roles as sources or sinks of GHG. However, it is unclear if their effects can be detected in highly variable conditions in a field setting. Here we use an extensive data set on carbon dioxide (CO 2 ), methane (CH 4 ), and nitrous oxide (N 2 O) flux in sediment cores (n = 103) collected from 10 urban wetlands in Melbourne, Australia during summer and winter in order to test for invertebrate enhancement of GHG flux. We detected significant multiplicative enhancement effects of temperature, sediment carbon content, and invertebrate density on CH 4 and CO 2 flux. Each doubling in density of oligochaete worms or large benthic invertebrates (oligochaete worms and midge larvae) corresponded to~42% and~15% increases in average CH 4 and CO 2 flux, respectively. However, despite exceptionally high densities, invertebrates did not appear to enhance N 2 O flux. This was likely due to fairly high organic carbon content in sediments (range 2.1-12.6%), and relatively low nitrate availability (median 1.96 lmol/L NO 3 À -N), which highlights the context-dependent nature of community structural effects on ecosystem function. The invertebrates enhancing GHG flux in this study are ubiquitous, and frequently dominate faunal communities in impaired aquatic ecosystems. Therefore, invertebrate effects on CO 2 and CH 4 flux may be common in wetlands impacted by urbanization, and urban wetlands may make greater contributions to the total GHG budgets of cities if the negative impacts of urbanization on wetlands are left unchecked.

show abstract

“…, Pigneret et al. ). They have also been shown to enhance nutrient, metal, and GHG flux in controlled laboratory experiments (Lagauzère et al.…”

Section: Introductionmentioning

confidence: 99%

Pollution‐tolerant invertebrates enhance greenhouse gas flux in urban wetlands

Mehring

Cook

Evrard

et al. 2017

Ecological Applications

View full text Add to dashboard Cite

show abstract

“…Estragnat et al., ; Gette‐Bouvarot et al., ). Therefore, we used enclosure experiments in this kind of artificial ecosystem to evaluate the impact of tubificid worms on (a) sediment characteristics (grain size distribution, water‐filled porosity using X‐ray computed microtomography, Li et al., ; Pigneret et al., ), (b) bacterial and algal components of the biofilm (biomass/abundances and activities) and (c) the community structure of benthic fauna. According to literature (Ciutat et al., ; McCall & Tevesz, ), we first expected that tubificid worms would increase the percentage of clay and silt particles in top sediment layer through their selective feeding within sediment and pellet egestion at the sediment surface (first hypothesis).…”

Section: Introductionmentioning

confidence: 99%

“…This reconstruction was performed with Datos x2 software from Phoenix X-ray (GE Sensing & Inspection Technology, USA). Image analyses were made using the ImageJ freeware (version 1.48) according toPigneret et al (2016). Quantitative analyses were performed on subvolumes (stacks of 741 slices of 870 × 870 pixels) cropped in the centre of the sediment cores to discard edge effects and to keep the central zone that was not affected by sampling.…”

mentioning

confidence: 99%

Influence of tubificid worms on sediment structure, benthic biofilm and fauna in wetlands: A field enclosure experiment

et al. 2018

View full text Add to dashboard Cite

Bioturbation activities of tubificid worms play a major role in nutrient cycling and microbial processes occurring at water–sediment interfaces of freshwater environments. Nevertheless, evidence of significant contributions of worms to ecosystem functioning largely arises from experiments performed at laboratory scales, because studies exploring the role of tubificid worms in the field are scarce. Therefore, this study aimed to test the influence of tubificid worms on benthic habitat structure and functioning in field experiments. According to literature, we predicted that feeding activities of tubificid worms would increase the percentage of clay and silt particles, the bacterial growth and microbial activities in the top sediment layer. The experiment was performed at the water–sediment interface of a shallow wetland. Enclosures with and without addition of the tubificid worm Limnodrilus hoffmeisteri were used to quantify the influences of tubificid worms on the sedimentary habitat (sediment grain size distribution, water‐filled porosity using microtomography), the biofilm (algal biomass, bacterial abundance, total organic carbon and total nitrogen, microbial enzymatic activity, photosynthetic activity and efficiency of the photosystem II) and the benthic fauna. Measures were performed before worm addition and at the end of the experiment. After 6 weeks, the proportion of fine sediment particles (<63 μm) and the water‐filled porosity were significantly modified by the bioturbation activities of tubificid worms. The bacterial abundance was stimulated by twofold, the microbial hydrolytic activity by +35% and the algal biomass by +40%. The field enclosures with and without L. hoffmeisteri showed differences in benthic invertebrate assemblages, especially for nematodes that were excluded from enclosures with worms. Our results indicate that bioturbation mechanisms and impacts reported from laboratory experiments with tubificid worms are not only significant at a field scale, but also highlight unpredicted interactions with other benthic organisms (autotrophic compartment of the biofilm and invertebrates).

show abstract

“…In terms of applied studies, monitoring of pest and invasive species (Fuchs et al., 2004; Halley et al., 2005; Harrison et al., 1993; Monaenkova et al., 2015; Soné, Mori, Ide, Setoguchi, & Yamanouchi, 1995; Tarver et al., 2006), interaction between hosts and parasites (Greco et al., 2010; Schwabe et al., 2014), forensic entomology (Johnson et al., 2012), and ecotoxicological research (Brinkmann et al., 2016; Holliday & Holliday, 2012; Lind et al., 2004; Pigneret et al., 2016; Yunusa, Braun, & Lawrie, 2009) have been also benefited greatly from this technique so far.…”

Section: Perspectives and Final Considerationsmentioning

confidence: 99%

“…To date, X-ray CT has proven to be a suitable technique to reveal the biology and ecology of elusive organisms (Jennings & Austin, 2011;Mouginot et al, 2015), diet analysis of extinct species (Collareta et al, 2015;Gill et al, 2014), and to examine nest/ colony life, development, and structure (Fuchs et al, 2004;Greco et al, 2005Greco et al, , 2006. In terms of applied studies, monitoring of pest and invasive species (Fuchs et al, 2004;Halley et al, 2005;Harrison et al, 1993;Monaenkova et al, 2015;Soné, Mori, Ide, Setoguchi, & Yamanouchi, 1995;Tarver et al, 2006), interaction between hosts and parasites (Greco et al, 2010;Schwabe et al, 2014), forensic entomology (Johnson et al, 2012), and ecotoxicological research (Brinkmann et al, 2016;Holliday & Holliday, 2012;Lind et al, 2004;Pigneret et al, 2016;Yunusa, Braun, & Lawrie, 2009) have been also benefited greatly from this technique so far.…”

Section: Per S Pec Tive S and Final Cons Ider Ationsmentioning

confidence: 99%

X‐ray computed tomography and its potential in ecological research: A review of studies and optimization of specimen preparation

Gutiérrez

Ott

Töpperwien

et al. 2018

Ecology and Evolution

View full text Add to dashboard Cite

Imaging techniques are a cornerstone of contemporary biology. Over the last decades, advances in microscale imaging techniques have allowed fascinating new insights into cell and tissue morphology and internal anatomy of organisms across kingdoms. However, most studies so far provided snapshots of given reference taxa, describing organs and tissues under “idealized” conditions. Surprisingly, there is an almost complete lack of studies investigating how an organism′s internal morphology changes in response to environmental drivers. Consequently, ecology as a scientific discipline has so far almost neglected the possibilities arising from modern microscale imaging techniques. Here, we provide an overview of recent developments of X‐ray computed tomography as an affordable, simple method of high spatial resolution, allowing insights into three‐dimensional anatomy both in vivo and ex vivo. We review ecological studies using this technique to investigate the three‐dimensional internal structure of organisms. In addition, we provide practical comparisons between different preparation techniques for maximum contrast and tissue differentiation. In particular, we consider the novel modality of phase contrast by self‐interference of the X‐ray wave behind an object (i.e., phase contrast by free space propagation). Using the cricket Acheta domesticus (L.) as model organism, we found that the combination of FAE fixative and iodine staining provided the best results across different tissues. The drying technique also affected contrast and prevented artifacts in specific cases. Overall, we found that for the interests of ecological studies, X‐ray computed tomography is useful when the tissue or structure of interest has sufficient contrast that allows for an automatic or semiautomatic segmentation. In particular, we show that reconstruction schemes which exploit phase contrast can yield enhanced image quality. Combined with suitable specimen preparation and automated analysis, X‐ray CT can therefore become a promising quantitative 3D imaging technique to study organisms′ responses to environmental drivers, in both ecology and evolution.

show abstract

Urban pollution of sediments: Impact on the physiology and burrowing activity of tubificid worms and consequences on biogeochemical processes

Cited by 33 publications

References 69 publications

Pollution‐tolerant invertebrates enhance greenhouse gas flux in urban wetlands

Pollution‐tolerant invertebrates enhance greenhouse gas flux in urban wetlands

Influence of tubificid worms on sediment structure, benthic biofilm and fauna in wetlands: A field enclosure experiment

X‐ray computed tomography and its potential in ecological research: A review of studies and optimization of specimen preparation

Contact Info

Product

Resources

About