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Light-trapped caddisflies to decipher the role of species traits and habitats in Hg accumulation and transfer

MARLE, Pierre, et al.

MARLE, Pierre, et al . Light-trapped caddisflies to decipher the role of species traits and habitats in Hg accumulation and transfer. Chemosphere , 2022, vol. 287, p. 131909

PMID : 34461331

DOI : 10.1016/j.chemosphere.2021.131909

Available at:

http://archive-ouverte.unige.ch/unige:155084

Disclaimer: layout of this document may differ from the published version.

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Chemosphere 287 (2022) 131909

Available online 17 August 2021

0045-6535/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Light-trapped caddisflies to decipher the role of species traits and habitats in Hg accumulation and transfer

Pierre Marle

a,b,*

, Pablo Timoner

c

, Wei Liu

b

, Emmanuel Castella

a

, Vera I. Slaveykova

b

aUniversity of Geneva, Faculty of Sciences, Earth and Environment Sciences, Department F.-A. Forel for Environmental and Aquatic Sciences, Laboratory of Aquatic Ecology and Biology, And Institute for Environmental Sciences, Uni Carl Vogt, 66 Bvd Carl-Vogt CH 1211, Geneva, Switzerland

bUniversity of Geneva, Faculty of Sciences, Earth and Environment Sciences, Department F.-A. Forel for Environmental and Aquatic Sciences, Environmental Biogeochemistry and Ecotoxicology, And Institute for Environmental Sciences, Uni Carl Vogt, 66 Bvd Carl-Vogt CH 1211, Geneva, Switzerland

cUniversity of Geneva, Faculty of Sciences, Earth and Environment Sciences, Department F.-A. Forel for Environmental and Aquatic Sciences, EnviroSPACE Laboratory, And Institute for Environmental Sciences, Uni Carl Vogt, 66 Bvd Carl-Vogt CH 1211, Geneva, Switzerland

H I G H L I G H T S G R A P H I C A L A B S T R A C T

•Variation of [THg] between species is best explained by the larval feeding type.

•Species [THg] depends also on their larval macrohabitat (main river channel vs floodplain).

•The most contaminated species are related to predators, filterers and sponge-feeders.

•Bioavailability of mercury could depend on complexation by DOM and MES.

A R T I C L E I N F O Handling Editor: Michael Bank Keywords:

Mercury Caddisflies Floodplain Contaminant Rhˆone river

Dissolved organic matter

A B S T R A C T

We present a novel meta-community approach to explore the influence of species traits, such as adult body size, larval feeding type and microhabitat, as well as larval macrohabitat (main river channel vs. floodplain water bodies) on the concentration of total Hg accumulated ([THg]) in assemblages of adult caddisflies. We analyzed [THg] in 157 light-trapped adult caddisflies in a floodplain sector of the French upper Rhˆone River and used a linear mixed effect model to decipher the role of species traits and habitats in Hg accumulation. Variation of [THg] between species was best explained by the larval feeding type, whereas the contributions of adult size and larval micro and macro-habitat were minor. Results showed that [THg] in species associated with floodplain macrohabitats in the larval stage was lower than in those associated with the main river channel. This difference could depend on complexation of Hg by DOM (in the floodplain) and MES (in the main channel). This research provides a first evidence of the potential of an entire caddisfly assemblage for the assessment of contamination in large alluvial rivers. The implications of the results are discussed in view of the possible role of caddisflies as vectors of Hg to riparian predators.

* Corresponding author. University of Geneva, Faculty of Sciences, Earth and Environment Sciences, Department F.-A. Forel for Environmental and Aquatic Sciences, Laboratory of Aquatic Ecology and Biology, And Institute for Environmental Sciences, Uni Carl Vogt, 66 Bvd Carl-Vogt CH 1211, Geneva, Switzerland.

E-mail address: pierre.marle@unige.ch (P. Marle).

Contents lists available at ScienceDirect

Chemosphere

journal homepage: www.elsevier.com/locate/chemosphere

https://doi.org/10.1016/j.chemosphere.2021.131909

Received 19 May 2021; Received in revised form 19 July 2021; Accepted 14 August 2021

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1. Introduction

Mercury (Hg) is a persistent priority contaminant of global concern.

In most aquatic ecosystems, the main sources of Hg include diffuse at- mospheric deposition and point sources related to industrial activities (UNEP, 2018). Hg accumulates into biota and biomagnifies in food webs of different aquatic environments, including invertebrates, in large river ecosystems (Azevedo et al., 2020; Naimo et al., 2000; Walters et al., 2020). Accumulation of Hg in invertebrates depends on various envi- ronmental and biological factors, including physiology, ecological traits and habitats (Amirbahman et al., 2013; Baird and Van den Brink, 2007).

Among invertebrate traits, body size, used as a proxy for trophic level (Akin and Winemiller, 2008; Cohen et al., 2003; France et al., 1998), larval feeding types and habitats (Collins and Fahrig, 2020; Ippolito et al., 2012; Rubach et al., 2011; Wiberg-Larsen et al., 2016) are considered as relevant factors for metal bioaccumulation. However, the relative contributions of these interrelated species traits operating simultaneously on Hg accumulation are not known.

From marine (Karimi et al., 2013) to floodplain (Hug Peter et al., 2017, 2018) ecosystems, trait studies prompted a change in the lens through which scientist view bioaccumulation of metals. However, these studies rarely considered the role of ecosystem processes (e.g. flood and sediment transport), organismal physiology, community composition, and species interactions in metal transfers and bioaccumulation in food webs. Additionally, metal bioaccumulation by terrestrial predators, driven by both metal concentrations and prey abundance (Becker et al., 2018; Chumchal and Drenner, 2015; Tweedy et al., 2013), suggests a key role of prey traits in mediating contaminant flux. Because interest continues to grow in the transfer of contaminants from aquatic to terrestrial systems (Kraus, 2019), the role of larval feeding type, habitat and body size on mercury concentrations in adult aquatic insects emerging from a large river floodplain may provide an excellent window to improve the understanding of Hg bioaccumulation and transfers in large aquatic ecosystems.

Caddisflies (Trichoptera) are an abundant and diverse group of freshwater insects characterized by multiple morphologies, life strate- gies, feeding modes and habitat requirements (Graf et al., 2008; Mackay and Wiggins, 1979). Given their relatively sedentary lifestyle during the aquatic larval stage, caddisflies gained importance in ecological field studies and environmental assessment (Ruiz-García et al., 2012; Tachet et al., 1994; Waringer et al., 2005). Indeed, they provide information on the structure and hydrological function of waterbodies (Sagnes et al., 2008; Schmera et al., 2007; Statzner and Dol´edec, 2011a), as well as environmental changes (Statzner and Dol´edec, 2011b; Timoner et al., 2020; Usseglio-Polatera and Bournaud, 1989). In the larval stage, cad- disfly species cover the complete array of freshwater conditions, from alpine glacier-fed streams to lowland stagnant and temporary water- bodies. Some are adapted to warm temperature and low dissolved ox- ygen (Wiggins, 1973), which are conditions that lead to high mercury toxicity and bioaccumulation are expected to increase (Jonsson et al., 2012; Skyllberg, 2008). In addition, some species of hydropsychid caddisflies (mainly filterers) are reported to be highly tolerant to toxic metals (Luoma and Rainbow, 2011; Rainbow et al., 2012). Caddisflies are therefore considered as efficient biomonitors to assess ecological impacts of metal stressors in freshwater systems (Awrahman et al., 2015;

Rainbow et al., 2012; Sol`a and Prat, 2006; Ueno et al., 2018). However, we would expect significant variation in metal bioaccumulation in adult caddisflies and in metal transfer from emerging insects to terrestrial food chains. To date, comprehensive studies on bioaccumulation and transfer of metals by aquatic insects in large ecosystems such as river floodplains are still lacking.

The current study examines Hg accumulation in emerging adult caddisflies and employs a trait-based approach to assess landscape-scale control on mercury bioaccumulation processes in a large river flood- plain. We tested the hypotheses that (i) the total Hg concentrations in caddisflies were largely related to species traits, specifically larval

feeding type; and (2) species whose larval feeding habits and aquatic habitats depend on sediments (whether suspended or deposited) were the most contaminated. To this end, we measured the concentration of total mercury ([THg]) accumulated in light-trapped adult caddisflies representative for a variety of floodplain aquatic habitats. Given the impossibility to assign females to species, THg was only measured in males. Then, we used mixed models to examine the contribution of factors in explaining species [THg], such as species maximum forewing length as a measure of adult body size, larval feeding type as well as multi-scale larval habitat (i.e. micro and macrohabitat). Through the identification of their ecological preferences, we could relate the trap- ped individuals to their likely larval macro-habitat, i.e. the lotic main river channel or the more stagnant and isolated water bodies of the floodplain. The outcomes of the study have broad implications regarding the transfer of freshwater Hg towards terrestrial food webs.

2. Material and methods

2.1. Study sites and collection of adult caddisflies

Caddisflies were caught by two light-traps placed in the Grand Brotteaux and the Molottes islands located in the Br´egnier-Cordon sector, respectively 102.9 and 91.6 km upstream from Lyon on the French upper Rhˆone River (eastern France; Fig. 1A). The River Rhone ˆ has nearby chemical and metal working factories among several cities, which may be responsible for some of the Hg contamination, including in the study area (Cossa and Martin, 1991). Metal pollution exists in the Gier River (0.28 mg/kg in SPM in base conditions; Poulier et al., 2019), the main tributary whose confluence is located 5 km upstream from the study area. In addition, the flushing of accumulated sediments in up- stream reservoirs occur every 4–5 years and entail the resuspension of large amounts of sediment for short periods of time that have an ecological impact on downstream communities in terms of bio- accumulation of trace metals (Hug Peter et al., 2014). During the 2012 reservoir flushing, Launay (2014) reported elevated mercury concen- trations, from 0.42 to 0.47 mg/kg, in SPM collected directly downstream (Creys-M´epieu city, France) of the studied area.

Light-trapping was chosen because the trapped specimens provide a picture, not only of the most adjacent waterbody, but of an array of aquatic sites occurring in the landscape (Collier et al., 1997; Usseglio-- Polatera and Bournaud, 1989). As some caddisfly species are shoreline emergers, other devices such as emergence traps were deemed ineffec- tive in this case. Because the two sampling sites were surrounded pre- dominantly by alluvial forest, the average range of attraction of light-traps was estimated close to 200 m (Collier et al., 1997; Collier and Smith, 1997). Hence, each light-trap had an estimated 0.125 km2 area of attraction, thus the adults captured likely emerged from sur- rounding habitats, including the main river, active side-channels and floodplain waterbodies at various stages of disconnection (Fig. 1A). If one extends the catchment area of individual light-traps to 1500 m, a figure used in open landscapes (Collier and Smith, 1997), it also included a paleo-meander (Grand-Brotteaux site) and a tail-race canal (Molottes site) (Fig. 1A).

Light-traps were operated for approximately 8 h following sunset during three nights: June 26, 2017, May 14, 2018 and July 13, 2018 corresponding to the known period of highest caddisfly abundance and richness for the region (Marle, 2015; Marle et al., 2016; Rabarivelo, 2016). In case of adverse weather conditions (rain, strong wind, flood risks …) trapping was postponed, but carried out as close as possible to the new moon optimum. Light-traps (“Leuchtfallen 12 V/220 V classic”, Bioform, Nürnberg, Germany) were suspended over the water from a riverbank tree (Fig. 1B) (i) to be seen from at least 150–200 m in a downstream direction and (ii) to trap insects that mostly fly upstream and follow the water network especially just after emergence (May, 2019; Graham et al., 2017). Black-light (Sylvania light tubes BLACK- LIGHT F15 W/BL350; 438 mm; Ø26mm) was used as detailed in the

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study of Price and Baker (2016). Collecting jars contained milliQ water with a drop of liquid soap to reduce surface tension and increase the efficiency of the trap (Price and Baker, 2016). A light detector caused automatic switching on and off of the light traps.

2.2. Caddisfly identification, preservation and ecological traits

From the total number of individuals trapped that could reach several hundreds, between 1 and 11 male specimens per species were selected for Hg analysis. Adult males were identified to species level using Malicky (1983). Adult females were not considered due to the difficulty of species determination. Species traits for larval feeding types and microhabitats, as well as adult forewing maximum length were extracted from the freshwater ecology database (Schmidt-Kloiber and Hering, 2015) available online at http://www.freshwaterecology.info/, in which information derived from publications, unpublished literature and expert opinion is coded and updated by specialists. Trichoptera, together with Ephemeroptera and Plecoptera, are the insect orders for which trait information is best documented. The feeding type with the highest affinity score was retained for each species. The affinity scores ranged from “0′′to “5′′, indicating “no” and “high” affinity respectively.

When the same score was given for two feeding types in one species, we retained the feeding type generally assigned to the genus. This method was used to avoid mixed feeding types in the species traits, thus providing simplicity and consistency in the analysis. Seven categories of feeding types were represented: (1) sponge-feeder; (2) filterer: filtering drifting food particles; (3) predator: preying on others invertebrates; (4) shredder: dilacerating coarse plant material; (5) gatherer: sediment or deposit feeders, mainly detritivores; (6) grazer: grazing algae and associated material growing on the substrates (periphyton) and (7) piercer: sucking contents from the cells of filamentous algae. Filterer, sponge-feeder and piercer feeding types were represented in only one of the two macrohabitats. Predators, gatherers, grazers and shredders were present in both (Table S3).

Concerning micro-habitats, the caddisfly species were classified into six categories describing their substrate association: gravel, stones and cobbles (lithal), sand (psammal), organic matter, macrophyte (phytal) and algae (algal). These larval micro-habitats included species from both macro-habitats, excepting gravel habitat that was only assigned to the main channel species (Table S3).

The larval macrohabitat, i.e. main river channel or more stagnant and isolated water bodies of the floodplain was coded according to the preferences for current velocity. In addition, occurrence data from the monitoring of the Rhone River restoration (Lamouroux et al., 2015) was ˆ used for validation.

Species body size refers to the maximum length of the forewing (from the tip to the point of insertion on the thorax). Because females were excluded from the study, only male forewing length was considered.

2.3. Quantification of mercury accumulated in caddisflies

After being captured, specimens were kept in soapy waters on ice, during transport by car, and in the fridge upon arrival at the laboratory.

Then, specimens were individually pinned and frozen at − 80 C prior to freeze-drying, which occurred within 48 h after light-trapping. Whole body of each specimen was weighted and total Hg concentration ([THg]

=Inorganic Hg +Methylated Hg) was measured by a Direct Mercury Analyzer® (DMA, DMA-80, Milestone, Sorisole, Italy). For Hydro- ptilidae, the smallest caddisflies in the study (2–3 mm), three specimens were pooled for mercury analysis each of the three species: Hydroptila angulata, Hydroptila sparsa and Agraylea sexmaculata. Because adult caddisflies typically do not feed (Crichton, 1957; Holzenthal et al., 2007), adults were not depurated. Adults are also short-lived (typically one month) and, with the exception of a small proportion of contami- nants excreted with the insect larval and pupal skin (Larsson, 1984), body burdens remain unchanged after emergence. Thus, contaminants accumulated during the larval period (several months to nearly a year) can be measured directly by analysing the adults.

The reference material BCR-414, certified by the European Com- mission, with Hg concentration of 0.276 ±0.018 μg/g was used to evaluate the accuracy of the method. The recovery was 76.88% (range 76–78%, n =8) and 75.83 (range 73–82%, n =6), respectively for the two runs. The limit of detection (LOD) was 0.0015 mg/kg. Data values below the LOD were replaced with the fixed value of LOD prior to analyses.

2.4. Linking Hg accumulation with caddisfly traits 2.4.1. Modelling technique and calibration

To explore the possible links between Hg accumulation and caddisfly Fig. 1. The study area showing the floodplain water bodies (red) and the main river channel (blue) of the Upper Rhone River, France. Circles ˆ refer to the catchment area of each light-trap, Grand Brotteaux (northern site) and Molottes (southern site) [orange circle, 200 m radius and black circle, 1500 m radius (Collier and Smith, 1997)]. Data from Corine Land Cover was used to obtain forest cover (in green) (A). Light-trap installation (B). Floodplain waterbodies (left):

isolated and stagnant pools covered by Lemna sp. (1), isolated stagnant channel (2), side-channel connected downstream to the main river (3); and the Rhˆone river main channel (4).

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traits, [THg] measured in caddisflies from the two light-traps were gathered in a single dataset. The set contained multiple individuals and consequently multiple [THg] replicates per species. We therefore quantified the relationships between [THg] and caddisfly traits using a linear mixed effect model (LMM; Bolker et al., 2009), using the lme4 R package (Bates et al., 2015).

LMM was optimal for our purpose since it allows to measure the effect of traits on [THg] independently of species that we considered as random effect in the model. A LMM was developed with feeding type, maximum forewing length, larval micro-habitat and larval macro- habitats as fixed effects respectively. We used measured [THg] (log- transformed to reduce heteroscedasticity) as the response variable in the LMM. Visual checks of residual plots (Figure S1) were used to confirm model residuals met assumptions of normality and heteroscedasticity (Pardoe, 2012).

2.4.2. Estimate importance of each trait on species [THg]

We ran variance partitioning based on the LMM to estimate the importance of each of the four traits in the [THg] measured in caddis- flies. The marginal r-squared (r2) of the LMM was partitioned into the variance explained by each trait using the partR2 function from the partR2 R package (Stoffel et al., 2020). This same function also imple- mented parametric bootstrapping to quantify confidence intervals for each variance estimate.

2.4.3. Testing [THg] differences

Estimated model coefficients and their covariance were computed via the summary function available for most statistical models including LMM. Based on the results of the LMM, Tukey’s post hoc multiple comparisons tests were used to assess [THg] differences between cate- gories of species traits (glht function, set at α =0.05, within the mult- comp R package; Hothorn et al., 2008). This analysis also included the mcp (for multiple comparison procedure) function, from the same multcomp R package (Hothorn et al., 2008), that set up the matrix for Tukey’s all-pairwise comparisons among categories of each species traits.

The effect of maximum forewing length (the sole quantitative pre- dictor in the LMM) on predicted species [THg] was analyzed using linear regression model with the macro-habitats as interaction term.

2.4.4. Extrapolation of [THg] to a total assemblage

Using the trait-based LMM (see section 2.4.1), we extrapolated the observed [THg] in the light-trapped species to those of an existing in- ventory of the caddisflies known in the French upper Rhone River (Marle et al., 2016). We preferred to use an existing inventory for predictions rather than simulated data in which mis-combinations between trait categories (e.g. filterers do not live on macrophytes) and inconsistency of some traits with size (e.g. piercers are all small in size) can lead to misinterpretation or reduce the accuracy of predictions. The 115 species in the inventory varied in size (based on adult forewing length) but also in larval feeding types and microhabitat and are representative of both floodplain (nb of species =61) and main channel (nb of species =54) macrohabitats (Table S4). Feeding types, maximum forewing length and preferences in larval habitats (from Schmidt-Kloiber and Hering, 2015) of these species are listed in Table S4. Model predictions were made using the predictInterval function in the merTools R package (Knowles and Frederick, 2016) with 1000 simulations. This analysis resamples from the normal distribution of the fixed coefficient, including the un- certainty of the model, to generate predictions. We set the [THg] esti- mate to be the median of the generated values. A 95% confidence interval around the median was chosen. The ggplot2 R package (Wick- ham, 2009) was used for all graphics. Analyses were processed in the R statistical environment (version 1.1.423, R Development Core Team, 2016).

2.5. Complementary analysis

2.5.1. Mercury concentrations in sediments and dissolved oxygen measurements

Sediments were collected June 29, 2018 at two floodplain channels (downstream-connected channels) with Ekman Grab Samplers. Both channels are located in the restricted area (i.e. inside the orange circle;

Fig. 1) around each of the two light-traps. A plastic spatula was used to transfer the sediment subsamples into acid-rinsed glass bottles. The samples were placed in cold conditions until they arrived at the labo- ratory for chemical analyses. Total Hg concentrations in sediments were determined by atomic absorption spectrometry using direct mercury analyzer (DMA-80, Milestone, Sorisole, Italy). The detection limit of the machine was 10 pg. The accuracy of the analyses was verified by repeated measurements of certified reference material – Inorganic Ma- rine Sediment (SRM-2702, National Institute of Standards and Tech- nology, USA) for which the recovery was 103% ±4 (n =3).

Monomethylemercury (MeHg, CH3Hg+) was extracted from sedi- ments using HNO3 leaching/CH2Cl2 and measured with a Cold Vapor Atomic Fluorescence Spectrophotometer (MERX, Brooks Rand, Seattle, WA; Liang et al., 2004). The detection limit was 5 pg. The recovery of repeated extraction and analyses of the estuarine sediment ERM certi- fied Reference Material (ERM-CC580) was always above 55%.

Dissolved oxygen in the downstream-connected channels were the light-traps were installed was monitored with data logger (onset HOBO, Pocasset, MA, USA).

2.5.2. Organic carbon and fluorescence measurements in water

Dissolved organic carbon (DOC) concentrations and excitation emission matrices (EEMs) of dissolved organic matter (DOM) were determined. Water samples were collected the June 29, 2018 during low water periods to integrate more DOM signals as proposed in Peduzzi et al. (2008). The concentration of DOC was measured by Shimadzu TOC-L series analyzer (TOC-5000 A, Shimadzu, Japan). Water was filtered through 0.8 μm pore size sterile filters, acidified with 200 μL of 2 M HCl (pro-analysis, Merck, Darmstadt, Germany). Calibration was performed using standard solutions containing hydrogenophtalate (Merck, Germany) for DOC analysis.

Fluorescence spectra of DOM in water samples filtered through sterilized filter with pore size of 0.8 μm were recorded on an LS 55 Luminescence Spectrometer (PerkinElmer Ltd, Beaconsfield, England) using a 3 mL, 1 cm path length quartz cuvette, as detailed in Worms et al.

(2019). The EEMs were generated by recording emission spectra from 300 to 550 nm at 0.5 nm steps for excitation wavelengths between 200 and 450 nm with 5 nm steps. All EEMs were processed in the R statistical environment (version 1.1.423, R Development Core Team, 2016).

3. Results

3.1. Mercury concentrations in sediments and dissolved oxygen measurements in the floodplain

Regarding sediments, our results showed no important differences between PONT and MOLO sampling sites. The concentration of THg in the sediments of the two waterbodies was below 0.1 mg/kg and could be

Table 1

Dissolved oxygen and mercury concentrations (average±s.d.) in sediments measured in two semi-lotic systems on the French upper Rhˆone River.

Molottes channel

(MOLO) Ponton channel

(PONT) Dissolved oxygen (mg/L) 4.51 ±2.30 7.96 ±1.69 [THg] in sediment (mg/kg) 0.065 ±0.005 0.026 ±0.001 [MeHg] in sediment (μg/kg) 0.30 ±0.07 0.67 ±0.06

Ratio [MeHg]/[THg] in sed. 0.005 0.025

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considered as very low. Similarly, the concentrations of MeHg were very low in both channels, corresponding to <2.5% of the THg (Table 1).

However, the dissolved oxygen concentration in PONT was 1.75 higher than in MOLO (Table 1).

3.2. Dissolved organic carbon and fluorescence measurements in floodplain and main channels

DOC concentrations were higher in the water sampled in the flood- plain (range 1.5–17) than in the main channel (range 1.218–1.268;

Table 2). The general fluorescence properties of the water collected in two isolated floodplain water bodies indicated that DOM was repre- sentative of humic substances (peaks A; Fig. 2). The fluorescence in- tensity of the humic-like peak C also varied between the two samples (Fig. 2).

3.3. Observed Hg accumulation in adult caddisflies

Based on the analysis of 157 adult males (Table S2), [THg] was two to three times lower in the individuals from the 12 species associated with floodplain macro-habitat (median 0.0245 mg/kg dry weight, n = 41) compared with those found in the 17 species associated with the main river channel (median 0.0718 mg/kg dry weight, n =93). Average [THg] for the whole assemblage was 0.048 mg/kg. Approximately 30%

(40) of the specimens, belonging mainly to species associated with the floodplain habitats, contained [THg] below LOD (0.0015 mg/kg).

Specimens with the highest [THg] (>0.09 mg/kg) all belonged to main channel species: Hydropsyche saxonica, Hydropsyche pellucidula, Ceraclea dissimilis, Ceraclea riparia and Ceraclea albimacula, listed in decreasing [THg] order. The floodplain species Phryganea grandis, came in ninth position with an average [THg] of 0.071 ±0.013 mg/kg (Table S2).

3.4. Exploring the link between Hg accumulation in caddisflies and species traits

3.4.1. Overview of the model

The variance component of the model associated with the random effect appeared as relatively low (difference between conditional and marginal r2 =0.07). As assessed with the marginal r2 (0.61), the LMM appeared to make reliable predictions. Among species traits, feeding type was found to be the best predictor of the model (r2 =0.18; Fig. 3).

While the relationships of [THg] with macro-habitats, micro-habitats and forewing length were highly similar with a lower r2 (close to 0.05;

Fig. 3).

3.4.2. Relation with larval feeding types

The paired comparisons between feeding types showed that grazers significantly accumulated the lowest [THg] (P < 0.05; Fig. 4C) compared with other groups (except for piercers and predators, not significant). Among the feeding types studied, predators, shredders, filterers and sponge-feeders associated with the main channel contained the highest predicted [THg] (median > 0.065 mg/kg), whereas the lowest values mostly concerned gatherers, grazers, piercers and flood- plain predators (median <0.025 mg/kg, Fig. 4C). The highest predicted [THg] values concerned, for each of the two macrohabitats, sponge-

feeders (in the main channel) and predators (in the floodplain;

Fig. 4C). [THg] in predators from the floodplain and the main channel were not significantly different (Wilcoxon test, P =0.051).

3.4.3. Relation with larval (micro and macro) habitats

[THg] in species associated with floodplain macrohabitat was three times lower than in those associated with the main river channel (Fig. 4A). Caddisflies related to main channel lithal and floodplain organic matter had the highest [THg] (average >0.06 mg/kg; Table S3 and Fig. 4B) compared with those associated with other micro-habitats.

The average [THg] measured in other groups were in the range 0.01 – 0.05 mg/kg with a minimum in algae and sand for floodplain species (average [THg] =0.001 mg/kg for both habitats) and phytal for main channel species (average [THg] =0.04 mg/kg; Table S3). In the main channel, adult caddisfly [THg] increased with the sediment grain size associated with their respective larval stage, i.e. [THg] psammal <[THg]

gravel <[THg] lithal (Fig. 4B).

3.4.4. Relation with body size

Hg bioaccumulation increased linearly with the forewing length of adult caddisflies used as a surrogate for body size (Fig. 4D). For the species of the main channel the increase in accumulated [THg] was at least two times stronger (slope =0.009; p <2e-16) than for floodplain species (slope =0.004; p <2e-16).

4. Discussion

The present study depicted significant relationships between envi- ronmental characteristics (sediment, water and organic matter) and the species [THg] and traits of a caddisfly assemblage in a large alluvial river. The average [THg] (0.048 mg/kg) was 5x higher than that found in invertebrates from Canadian Rocky mountain streams (<0.01 mg/kg;

Painter et al., 2016) but 10-fold lower than the average value in chi- ronomids of a French contaminated wetland (0.518 mg/kg; Yung et al., 2019). However, owing to a number of differing factors, such as feeding modes, habitats, Hg background concentrations and physicochemical parameters, comparisons between field studies remain questionable.

4.1. Species [THg] was different among traits 4.1.1. Feeding types

Our study reinforces recently published work in which feeding type was shown to be a more sensitive indicator of Hg contents in aquatic invertebrates than other traits (Pouil et al., 2020; Rodriguez et al., 2018). The fact that feeding type is a key factor explaining among-species variation in [THg] is also based on the principle that the forewing length (body size) of a caddisfly is causally linked to its feeding capacities (Burrell and Ledger, 2003; Davidowitz et al., 2003; Wagner, 2002). Moreover, feeding capacity (i.e. capacity to encounter a feeding resource more frequently) with food availability are also habitat specific (Smith-Cuffney and Wallace, 1987; Wetmore et al., 1990). This suggests that the notion of feeding type overlaps both with the habitats and the size (among other morphological characteristics) of species, increasing therefore the predictive power of feeding traits.

The use of caddisflies for Hg monitoring in riverine environments has several advantages. Firstly, they provide rapid results that allow direct comparison of different contaminant levels between different areas/

environments. And secondly, filterers, predators and sponge-feeders could provide information about the maximal accumulation potential of Hg. Should these feeding categories be missing, this could be indic- ative of a high pollution exposure (Santoro et al., 2009). It remains that Hg uptake of the studied feeding groups is currently not well known.

The highest [THg] values measured in sponge-feeders (in the main channel) and predators (in the floodplain; Fig. 4C) indicated that trophic transfer of Hg in invertebrate food web did occur. However, [THg] in those groups were not significantly different from feeding groups Table 2

DOC in the surface waters of the main channel and the floodplain1 in the MOLO and PONT stations.

Sampling locations Stations DOC (mg/L)

Rhˆone River main channel MOLO 1.218

Rhˆone River main channel PONT 1.268

Downstream connected channel1 MOLO 3.950/3.588

Downstream connected channel1 PONT 2.136/1.620

Isolated channel1 MOLO 16.620

Isolated channel1 PONT 7.596

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occupying lower trophic levels (e.g. shredders and filterers). Certainly, the low percentage of THg that was MeHg (observed in floodplain sed- iments; Table 1) did not allow predators and sponge-feeders to accu- mulate significantly higher [THg] than filterers and shredders.

Sponges filter large volume of water and represent the principal filter-feeding macroinvertebrates in some freshwater environments (Pile et al., 1997). Exposed to current (Resh et al., 1976), filterers are directly exposed to suspended particulate matter (SPM). Although the relation- ship between filterers and Hg bound to SPM is not yet documented in large rivers, SPM was shown to be a major source of metals in bivalve molluscs of coastal and estuarine environments (Edge et al., 2014;

Griscom and Fisher, 2004). In the latter, Hg concentrations in SPM also predicted mercury concentration in fish (Chen et al., 2014). We hy- pothesized that suspended sediments may play a similar role in the mercury bioaccumulation among filterer and sponge-feeder caddisflies of the main channel, however further research is needed to tackle this issue.

Excepting shredders, [THg] did not differ among feeding groups of floodplain caddisflies (Fig. 4C). Floodplain shredders accumulated higher [THg] than other feeding groups because they may feed on bio- film (growing on living or dead plants) that potentially concentrate metal load (Ancion et al., 2013). These results are consistent with high concentrations of metals in shredders and scrapers from the Coeur d’Alene River, Idaho (Farag et al., 1998) and the Arkansas River, Col- orado (Kiffney and Clements, 1993). However, low observed [THg] in grazers (median =0.0015 mg/kg; Table S3) suggested another source of mercury contamination than biofilm for shredders. We believe that the diet of shredders could be composed at least in part of animal preys, implying a higher trophic level in older larval instars. Moreover, the predation capacity of shredders is often comparable or higher than that of some filterers [see feeding traits from the freshwater ecology database from Schmidt-Kloiber and Hering (2015), but also Basaguren et al.

(2002) and Hellmann et al. (2013)]. In contrast, piercers (associated with floodplain sites) and grazers and gatherers contained lower [THg]

(average < 0.025 mg/kg; Fig. 4C). This finding suggests that these groups are feeding in a micro-habitat (i.e. macrophytes) or upon food (i.

e. algae) with low Hg concentrations.

4.1.2. Relation with body size

We showed for the first time that Hg bioaccumulation increased linearly with the forewing length of adult caddisflies used as a surrogate for body size (Fig. 4D). In general, Hg concentrations in organisms appear strongly linked with body size: in fish, molluscs (Karimi et al., 2013; Le et al., 2018) and some insects (Buckland-Nicks et al., 2014;

Gimbert et al., 2016; Lesch and Bouwman, 2018). Our results also showed, for the species of the main channel, that the increase in accu- mulated [THg] was at least two times stronger than for floodplain spe- cies (Fig. 4D). Because the difference in forewing length between both groups is not significant (Wilcoxon test, P = 0.77), lower [THg] in floodplain species cannot be due to an effect of differential growth in the two habitats. In contrast, higher Cd concentrations were found in smaller chironomid larvae (Hare et al., 1991). With increasing body size, the surface:volume ratio decreases, and the relative contribution of surface adsorbed metal to the total body content becomes less impor- tant. Our results are therefore in agreement with the findings that the contribution of surface adsorption to the overall uptake remains very low for biomagnifying metals such as Hg (Hare et al., 1991; Krantzberg, 1989; Lavilla et al., 2010; Vijver et al., 2005).

Therefore, forewing length may encompass other related traits such as trophic level and life span, which makes interpretation of the influ- ence of this factor more complex. Indeed, low [THg] in small caddisflies can be associated with the fact that most of them are hydroptilids (Hydroptila sparsa, Hydroptila angulata) and psychomyids (Psychomyia pusilla) (Table S3). These species are also at the base of the food chain (i.

e. gatherers for the Hydroptila species and grazers for Psychomyia pusilla), as well as associated with short life cycles (Townsend and Hil- drew, 1994) and thus, potentially shorter exposure to contaminants.

High [THg] was found in larger specimens (forewing length >9 mm) with longer lifespan as e.g. Phryganea grandis and various hydropsychids (Table S2).

The slope of the linear relationship between accumulation and forewing length (Fig. 2D) could also be influenced by excretion (Khan et al., 2012). The most efficient mechanisms of metal excretion include metamorphosis (Kraus et al., 2014), molting (Buckland-Nicks et al., 2014; Jop, 1991; Keteles and Fleeger, 2001; Simon et al., 2019), and feces production (Brown, 1986; Croteau et al., 2007). These mecha- nisms, together with the exposure level of the larvae, affect the amount of metal excreted (Kraus et al., 2021). Even if the excretion of mercury by these mechanisms is not well understood for caddisflies, it can be hypothesized that caddisflies may utilize the same metabolic machinery for excretion, regardless of their larval habitat.

Fig. 2.Two examples of EEM fluorescence spectra in water sample collected from two isolated stagnant channels in the floodplain (see pictures 1 and 2 on Fig. 1 for sampling location). Contour plots present spectral shapes of the excitation-emission of humic-acid (Peak C and A) fluorescence.

Fig. 3. Comparison of partitioned r2 for individual predictors included in the LMM.

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4.1.3. Relation with larval (macro and micro) habitat

Results showed that [THg] in species associated with floodplain macrohabitats was 3x lower than in those associated with the main river channel (Fig. 4A). This variation reflects that adult caddisflies are suit- able indicators of Hg level exposure from surrounding aquatic envi- ronments. In addition to the level of exposure, organic matter content is often used to quantify the risk of accumulating contaminant. High DOC values are likely to be encountered in productive environments as floodplains and may substantially modify Hg bioavailability. Here, water samples indicated that the concentrations of DOC were higher in

water sampled in the floodplain than in the main channel (Table 2). This observation matches with the results from Hug Peter et al. (2017), who found that DOC were higher in isolated than in connected floodplain channels.

The explanation for why floodplain species (excepting organic mat- ter dependent ones) appeared less contaminated is the likely adsorption of mercury by DOM in the water column. Typically, the bioaccumulation of Hg by biota is reduced by DOC (Bravo et al., 2017; Wang and Wang, 2010), so we expected lower [THg] in habitat richer in DOM. The lower [THg] found in floodplain species corresponded to 2–15x higher DOC Fig. 4.Predicted [THg] (median) of 54 main channel (blue) and 61 floodplain (red) caddisfly species (A) for different categories of micro-habitats (B), feeding types (C) and adult forewing lengths (a proxy for body size) (D). Stars indicate significant differences (“***" ≤0.001, "**"≤0.01, "*" ≤0.05) tested by a Wilcoxon test (A) and Tukey’s post hoc multiple comparisons tests (B and C). Regression slopes (D) are highly significant (linear model, P <0.001 for both floodplain and main channel species groups). Predictions are based on a linear mixed model developed with the four species traits as fixed effects and the species as random effects. See co- efficients and p-values for traits in Table S1. Through their ecological preferences, species were related to their likely larval habitat, i.e. main river channel or the more stagnant and isolated floodplain waterbodies. For further information see Table S4.

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concentrations in floodplain waters than in the main channel (Table 2).

We therefore contend the complexation of Hg by organic matter in the water column may control Hg bioavailability to caddisfly larvae. Hence, for the larvae related to a floodplain habitat, we observed a decrease of [THg] (Fig. 4A) that may correspond to an increase of humic-like DOM in the water column (Fig. 2). In addition, lower [THg] in floodplain species could also be explained with the co-precipitation of Ca2+, Mn2+ and Fe2+from relatively anoxic groundwater as they meet oxic surface water and scavenge metals (Allard, 1995), also limiting Hg availability for aquatic organisms.

In the floodplain, larvae living on a more organic substrate, are likely ingesting relatively higher amounts of fine organic sediments than in the other larval micro-habitats. Because [THg] in sediment is positively correlated with total organic carbon (Chakraborty et al., 2015), species with psammal and lithal (i.e. mineral) habitats accumulated less Hg than those with organic matter (Fig. 4C). Thanks to their micro-habitats, caddisflies with phytal and algal habitat could feed in submerged mac- rophytes, further away from the bottom sediment. As the amount of accumulated Hg in organic sediments is significantly higher than in submerged macrophytes (Regier et al., 2013; Thompson-Roberts et al., 1999) and mineral sediments (Chakraborty et al., 2015), species crawling on the organic sediments (i.e. gatherers, shredders and even- tually predators) could be exposed to higher concentrations of Hg. Using invertebrate traits as predictors in floodplain channels, Hug Peter et al.

(2018) also showed that living on sediment increased trace metal up- take. On the one hand, fine-grained and organic sediments, anoxic and redox conditions, favor Hg methylation. However, in the present case, as MeHg in sediments represented less than 3% of THg (Table 1), we believe this form does not contribute significantly to the Hg bio- accumulation in caddisflies. On the other hand, the resuspension of sediment and release of accumulated Hg, enhance mercury bioavail- ability for aquatic organisms. Existing literature confirmed these as- sumptions, indicating that high Hg concentrations mostly occur in surface sediments (Farag et al., 1998; Sizmur et al., 2013). This cor- roborates the findings of Naimo et al. (2000) in which mercury bio- accumulated by biota in floodplains was mainly derived from sediments.

On the contrary, because high river flows and significant loads of sediment transport and suspended matter characterized the main channel (Olivier et al., 2009), the likelihood of resuspension of Hg from sediments is relatively higher than in the more stagnant floodplain zone.

Additionally, regular sediment flushing from hydropower reservoirs upstream from the study site induce significant increases of SPM and associated metals and consequently increase the metal accumulation in filtering and gathering organisms of the main channel (Hug Peter et al., 2014). Our results also showed that the sediment grain size of the larval habitats is reflective of the degree of exposure to Hg (Fig. 4B). Sand and gravel substrates are most of the time associated with low current ve- locities (Beisel et al., 1998; Hauer et al., 2018), expected to entail a low exposure to drifting sediment-bound Hg. Whereas the opposite can be observed in cobbles, leading to a higher Hg exposure of caddisflies associated with the lithal habitat (Fig. 4B).

4.2. Caddisflies as a possible vector of mercury to terrestrial riparian predators

Caddisflies are probably the group of aquatic insects represented in large rivers that contribute the most to the diet of riverine insectivores as e.g. birds and bats (Alberts et al., 2013; Becker et al., 2018; Graf et al., 2017; Menzie, 1980; Raikow et al., 2011; Tweedy et al., 2013; Walters et al., 2010). The results of the present study revealed for the first time the potential of an entire caddisfly assemblage to provide an in situ assessment of the contamination at the scale of a large river floodplain, with a fine taxonomic resolution. It also confirmed the importance of species traits, and especially larval feeding mode, that have a significant effect on mercury concentration in caddisflies. Relationship between mercury in adults and larval macrohabitat opens an avenue towards the

development of concepts unifying aquatic and terrestrial food webs (Baxter et al., 2005; Kraus, 2019; Laws et al., 2016). While analysis of Hg in sediments is often a good indicator of the exposure level in polluted environments, patterns of bioaccumulation in species, variable in their relationships with aquatic habitats (Fig. 4A), can contribute to changing views of floodplains mainly perceived as contaminant reservoirs.

Indeed, caddisflies that contain the highest concentrations of mercury are main channel dwellers in the larval stage (Fig. 4A). They also pre- dominate quantitatively in adult caddisfly swarms (Marle, 2015; Marle et al., 2016; Rabarivelo, 2016; Usseglio-Polatera and Bournaud, 1989).

Results of the present study clearly illustrated the possibility of Hg exposure in terrestrial predators, such as insectivores that forage over water and consume emergent aquatic insects, via direct dietary ties to the river main channel, both at and above the water surface. The model presented here can be used to predict whether water-dependent in- sectivores are likely to be exposed to high levels of contaminants. Pre- dicting for which habitat (main channel vs. floodplain) the contaminant exposure may be the highest could inform about the range of Hg transfer by emerging insects and subsequently make important contributions to the knowledge of cross-boundary Hg cycle in large alluvial rivers.

However, obvious biases in the selected trait database, e.g. the failure to account for omnivory in species diets (mixed regimes were not consid- ered by the present study), the association of species to a single habitat category or even the study of larval traits to explain Hg concentrations in adults, suggest that caution should be taken in extrapolating from small subsets of biologically well-known species to ecosystem level studies.

Our study also suggested that more than one compartment should be considered in fluvial ecosystems. Along the lateral dimension of alluvial rivers, hydrological and physico-chemical changes can be abrupt (Hug Peter et al., 2017). The most frequent pattern observed was a decrease in dissolved and an increase in sediment associated trace metal concen- trations in the floodplain (Glinska-Lewczuk et al., 2009; Hug Peter et al., ´ 2017), the latter representing therefore a biogeochemical storage in the riverine landscape (Maia et al., 2009). In a worldwide context of continued reduction and narrowing of river floodplains (Tockner et al., 2008), research efforts, especially related to the mediating role of DOM in reducing contaminant bioavailability will be critical to assess the metal retention capacity and improve the long-term conservation of these ecosystems. We contend that this aspect should be prioritized in process-based large river ecosystem restoration.

Credit author statement

P.M. and E.C. conceived the project, designed the study and analyzed data. W.L., P.T. and V.S. assisted with data interpretation and manu- script writing.

Funding sources

This study was funded by the Agence de l’Eau Rhˆone-M´editerran´ee- Corse, the Compagnie Nationale du Rhˆone, the R´egion Auvergne-Rhˆone- Alpes, the R´egion Provence-Alpes-Cote d’Azur and Electricitˆ ´e de France.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors are grateful for the technical support for the sampling campaigns provided by H´el`ene Mayor. We thank Benoit Ferrari and Marc-Olivier Boldi for their fruitful discussions and inputs through their expert opinions. We also thank the research teams involved in the sci- entific monitoring of the Rhone River restauration (RhonEco project) for ˆ

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the availability of data and the Syndicat du Haut-Rhone for fruitful ˆ collaboration. Part of the data acquisition was financed by the Agence de l’Eau Rhˆone-M´editerran´ee-Corse, the Compagnie Nationale du Rhone, ˆ the R´egion Auvergne-Rhˆone-Alpes, the R´egion Provence-Alpes-Cˆote d’Azur and Electricit´e de France.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.

org/10.1016/j.chemosphere.2021.131909.

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Abbreviations: 18F-FDG, 18F-fluorodeoxyglucose; ALK, anaplastic lymphoma kinase; ANN, artificial neural network; AUC, area under the curve; BRAF, v-raf murine sarcoma viral

Spécialiste en biologie clinique, avec orientation en bio- chimie médicale, Marianne Philippe fait toute sa carrière aux Cliniques universitaires Saint-Luc, principalement dans

We mobilize the SSI approach in order to explore conditions of adapta- tion to climate change in the coffee and dairy sectors, which are similar in terms of farmers’ objectives

2 Les dessins suivants sont tracés à main levéeb. Construis chaque triangle en