Ecotoxicology and Environmental Safety 290 (2025) 117561

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Ecotoxicology and Environmental Safety

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

Exposure pathways (diet, dissolved or particulate substrate) of rare earth

elements to aquatic organisms
Ashlyn Kernaghan a,b,* , Duc Huy Dang a,b,c
a
School of the Environment, Trent University, Peterborough, Canada
b
Environmental and Life Science graduate program, Trent University, Peterborough, Canada
c
Department of Chemistry, Trent University, Peterborough, Canada

A R T I C L E I N F O A B S T R A C T

Edited by Bing Yan The global extraction and use of rare earth elements (REEs) continue to rise as they are implemented in tech­
nologies that improve human and environmental livelihoods. However, the general understanding of transfer
Keywords: processes and fates of REEs in aquatic systems remains limited. Here, we aim to determine the REEs’ main
Natural uptake mechanisms exposure pathways, e.g., particulate fraction, diet, or dissolved (ionic) fractions, to three benthic and three
REE Fractionations
pelagic organisms. They were maintained under laboratory conditions and exposed to natural river water, with
Background conditions
or without a sand substrate and an adapted diet. The organisms include northern clearwater crayfish (Faxonius
Bioaccumulation potential
Freshwater organisms propinquus), chinese mystery snail (Cipangopaludina chinensis), black sandshell mussel (Ligumia recta), striped
shiner minnows (Luxilus chrysocephalus), Daphnia magna, and Euglena gracilis. The combined results of REE
concentrations, fractionations, and anomalies highlighted that pelagic organisms are characterized by heavy
REEs enrichment indicating they mainly uptake REEs in the dissolved form with high bioaccumulation potential,
i.e., bioconcentration (BCF) > 1 and diet accumulation factors (DAF) < 1. Pelagic organisms exhibited relatively
low REE concentrations in their tissues ([La] ranging from 4.6 to 57.7 µg kg− 1 in minnows, 18.4 µg kg− 1 in whole
body D. magna, and 32.2 µg kg− 1 in E. gracilis). On the other hand, snails and mussels were enriched in light REEs
showing they mainly uptake REEs through their respective diets and particulate sand substrate. Relative to
pelagic organisms, mussels and snails have higher DAFs (161.2 and 18.6, respectively) and REE levels in their
soft tissues ([La] of 5700 µg kg − 1 and 650 µg kg − 1, respectively), but DAF for crayfish remains < 1. In summary,
under environmental-relevant conditions, the six aquatic organisms has the potential to accumulate REEs
through various uptake pathways. Nevertheless, our results confirming preferential uptake pathways of the six
organisms can help select appropriate species in future studies to monitor REE exposure from vaious fractions:
dissolved, particulate forms or in the food webs (i.e., diet).

1. Introduction Dy to Lu) (Wang et al., 2022) due to their slightly progressive differing
reactivities in aquatic environments (Dang et al., 2021; Garcia-Solsona
Rare earth elements (REEs) form a homogenous group of elements, and Jeandel, 2020; Mehmood, 2018). For instance, LREEs form strong
composed of 15 lanthanides (57La to 71Lu) and two non-lanthanides: inner sphere complexations (Lawrence and Kamber, 2006; Sholkovitz,
scandium (21Sc) and yttrium (39Y). Various jurisdictions have identi­ 1995), whereas HREEs form weak outer sphere complexations via
fied REEs as priority critical elements, e.g., Canada, USA, EU (Ellis, electrostatic forces (Byrne and Li, 1995). Consequently, LREEs have a
2018; European Commission, 2020; Government of Canada, 2022), as higher susceptibility to scavenge (Labassa et al., 2023) and adsorb onto
their geochemical and physical properties allow for advancements in reactive surfaces of mineral and colloidal particles (Merschel et al.,
vital high-end technologies (Balaram, 1996; Dang et al., 2021; Labassa 2017), causing enrichment of LREEs in the particulate form (Dang et al.,
et al., 2023). 2023; Luo et al., 2016). Heavy REEs are found more available in the
Rare earth elements can be subcategorized into light (LREEs: La to dissolved form (Merschel et al., 2017), where they have a higher affinity
Nd), medium (MREEs: Sm to Tb), and heavy rare earth elements (HREEs: to form complexations with inorganic dissolved carbonate (Luo and

* Corresponding author at: School of the Environment, Trent University, Peterborough, Canada.
E-mail address: [email protected] (A. Kernaghan).

https://doi.org/10.1016/j.ecoenv.2024.117561
Received 15 September 2024; Received in revised form 28 November 2024; Accepted 15 December 2024
Available online 19 December 2024
0147-6513/© 2024 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/by-
nc/4.0/).
A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

Byrne, 2004) and hydroxide complexes (Byrne and Li, 1995; de Baar or capable of uptaking and bioaccumulating dissolved, diet, or partic­
et al., 2018; Goldstein and Jacobsen, 1988). The “hat-shaped” or ulate forms of REEs.
MREE-enriched patterns are found to be associated with authigenic, Few studies have determined the uptake mechanisms of REEs in
diagenetic, and biogenic phosphate minerals (Hannigan et al., 2001; pelagic organisms. The bioaccumulation of REEs in zooplankton and in
Pourret et al., 2007; Pourret and Tuduri, 2017). Middle REE enrichment Arctic Char (Salvelinus alpinus) was strongly linked to uptaking free ionic
is also associated with the organic carbon fraction of sediments within dissolved forms (Macmillan et al., 2019; Nørregaard et al., 2019).
lakes, rivers, estuaries, and ocean river systems (Freslon et al., 2014; Similarly, Rétif et al. (2023) reported that both vertebrates and crusta­
Manoj et al., 2016; Morgan et al., 2012; Osborne et al., 2014; Zhang ceans held REE patterns similar to the dissolved phase. In marine di­
et al., 1998) due to the binding of REEs to the weak sites of solid-phase atoms, dissolved REEs quickly bind to cell surfaces and are assimilated
humic substances (Pourret et al., 2007; Tang and Johannesson, 2010). (Bingler et al., 1989). The bioaccumulation and uptake mechanisms of
Moreover, the Oddo-Harkins effect causes elemental abundances to REEs through the dissolved form have mainly been investigated on
be presented in a zigzag pattern (Ramos et al., 2016); REEs with even pelagic organisms of primary and secondary consumer trophic levels.
atomic numbers are more abundant than adjacent Here, we investigate the uptake mechanisms and exposure pathways
odd-atomic-numbered elements (Nikanorov, 2016; Piper and Bau, (diet, dissolved fraction, or particulate substrate) of REEs to both pelagic
2013). Normalization of REE patterns against a geological standard (e. and benthic organisms under environmental-relevant conditions using a
g., Upper Continental Crust (UCC, Rudnick and Gao, 2013; Taylor and lab-based approach. The objective is to determine whether aquatic or­
McLennan, 1995), Post-Archean Australian Shale (PAAS, McLennan, ganisms are susceptible to taking up and accumulating bioavailable
2001, 1989), North American Shale Composite (NASC), or European REEs from the different exposure fractions. These results would provide
Shales (EUS, Bau et al., 2018)) helps eliminate the zig-zag REE patterns insights on what organisms are highly sensitive to REE exposures under
and create smooth trends for interpretation (Bau et al., 2018), e.g., real-world ecosystems. Thus, organisms most susceptible to uptake REEs
geochemical processes, tracer of water masses, and anthropic releases could be used to biomonitor REEs within aquatic ecosystems vulnerable
(Arienzo et al., 2022). Normalized REE patterns are also used to to higher levels of REEs.
recognize anomalous concentrations of an individual REE as either
positive or negative anomalies (Pourret et al., 2022). Furthermore, all 2. Methods
REEs have a stable oxidation state of +III (de Baar et al., 1988), except
Eu and Ce. Europium holds the additional valance of +II under a 2.1. Experimental design and organism collection
strongly reducing environment, while Ce can be further oxidized to +IV
(Dang et al., 2023; Tyler, 2004; Zheng et al., 2016). This distinct Test subjects were housed in a temperature-controlled (21◦ C) room
behaviour of Eu and Ce has made them important tracers of geochemical with a 12 h/12 h light/dark cycle at the Trent University Animal Care
redox processes in the aquatic environment (Dang et al., 2022b; Floback Facilities for the duration of the study. Test subjects were placed in
and Moffett, 2021). separate polypropylene plastic tanks filled with Otonabee River water
The emissions of REEs from various activities (e.g., ore extraction that had been sand-filtered and ozonated. Bubblers and submersible
and refining processes, medical and residential wastewater effluent, active powerhead pumps (40 gallons per hour) were used for water
agriculture, and REE-based coagulants for ecological restoration) have circulation and aeration. Temperature was verified to be within a range
led to progressive enrichments of REEs in the sediment and water col­ of 19–21◦ C using a submersed thermometer. Other chemical parame­
umn of aquatic systems (Amyot et al., 2017; Hatje et al., 2016). Aquatic ters, i.e., pH, ammonia, nitrate, and nitrite concentrations, were
organisms are susceptible to assimilating REEs into their bodies from measured every four days using a freshwater test kit (API) to determine
surrounding abiotic environmental compartments (water column and whether water changes were needed. For the entire study, water changes
sediments) and their diets, i.e., bioconcentration and bioaccumulation. were not required since water quality levels for each parameter did not
There are a few reference points to consider; the global total mean exceed the danger thresholds for any organisms: constant pH at
∑
concentrations of the lanthanides ( [REEmean]) in the UCC is 7.6 ± 0.3, nitrite < 1 mg L-1, nitrate < 1 mg L− 1, and ammonia
146 mg kg (Taylor et al., 1981), relative to 199 mg kg− 1 in river
− 1
< 1.5 mg L− 1.
sediment and 175 mg kg− 1 in suspended particulate matters from rivers Tank water samples were collected at the beginning of the experi­
(Pereto et al., 2024). In freshwater systems, the global total median of all ment and on the last day to determine changes in elemental composition
∑
REEs ( [REEmed]) is 0.14 ± 0.17 μg L− 1 based on a recent compilation over time; a volume of 50 mL of raw Otonabee River water was filtered
(Pereto et al., 2024). Before REE levels continue to rise, investigations on at 0.45 µm using hydrophilic syringe filters (nylon, ChemScience
the bioaccumulation potential of REEs will allow insights into whether TLG™). Unfiltered and filtered water was acidified with double-distilled
organisms can depurate REEs through metabolizing or dilution pro­ trace metal grade HNO3 (BDH Aristar Plus) to 0.2 % v/v.
cesses (Amyot et al., 2017; Arnot and Gobas, 2006). Organisms were collected from local natural habitats or purchased
Currently, lab-based exposure experiments have investigated the from local commercial stores and allowed a 21-day equilibration period
impacts of solely dissolved REEs on freshwater organisms, including to adapt to the diet and acclimate to housing conditions (Behets et al.,
toxicity to mussels (Freitas et al., 2020; Pinto et al., 2019), Daphnia and 2020; Cardon et al., 2020). Benthic organisms, including crayfish
fungi (Bergsten-Torralba et al., 2020; Lachaux et al., 2022), microalgae (n = 4), snails (n = 6), and mussels (n = 5), were collected from Jack
(Lachaux et al., 2022; Siciliano et al., 2021), and inhibition to plankti­ Lake (Ontario). For benthic organisms, thoroughly rinsed and accli­
vory bacteria growth (Wang et al., 2000). However, the impacts of mated sand substrate (2–4 kg) was added to the tanks to provide refuge,
particulate REE forms, e.g., REE-based coagulants, or the trophic protection, and habitat during the study period. Diet feed samples were
transfers of contaminated food sources throughout the aquatic food web purchased thoroughly dried from both local health and commercial
are less documented. Lanthanum from a REE-based coagulant has the stores. Crayfish were fed bottom-feeder shrimp pellets (API) at 2 % of
potential to bioaccumulate into crayfish (Procambarus sp.) (Goitom, their body weight daily (Cardon et al., 2020) and housed in one 50 L
2011). Nevertheless, the bioavailable forms of REEs to crayfish were not polypropylene plastic tank. Freshwater snails and mussels were housed
fully resolved, i.e., the particulate form, such as the coagulant that has separately in two 30 L polypropylene plastic tanks and fed a daily 50 mL
been ingested, or the dissolved La3+ released from the particles. There is spirulina and chickpea powder (1:1 ratio) solution. Minnows (n = 10)
also evidence of REE trophic transfers in rainbow trout, which slightly were purchased from Bridgenorth Sports & Marine (Bridgenorth,
assimilated REEs from their prey, but no bioaccumulation occurred Ontario) and housed in one 200 L polypropylene plastic tank. They were
(Cardon et al., 2020). Despite these findings, there is no evidence on fed spirulina flakes at 2 % of their body weight daily (Cardon et al.,
whether benthic and pelagic organisms are impacted by REE exposures 2020). Daphnia magna (n ~ 100) were cultured and housed in a 16 L

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A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

polypropylene plastic container and fed a 50 mL spirulina and chickpea at − 20◦ C and further freeze-dried (Labconco).
powder solution (1:2 ratio) daily. Euglena gracilis (six 50-mL culture Around 300–700 mg of dried biota and feed samples were weighed
flasks) was cultured in Otonabee River and amended with nutrients and and digested using double-distilled trace-metal grade HNO3 (15.6 M)
trace elements following the formulations of the Modified Acid Medium and H2O2 (9.8 M) in a 1/0.2 (v/v) ratio. Samples were left to digest
(MAM) (Olaueson and Stokes, 1989); the composition is listed in overnight in the fume hood at 100◦ C until a clear solution was obtained.
Table S1. After the 21-day equilibration period, test subjects were To test digestion recovery, the Standard Reference Materials (SRMs)
housed in laboratory conditions for 64 days and were exposed to par­ NIST-1566a Oyster Tissue and NIST-1515 Apple Leaves (with informa­
ticulate REEs from the sand substrate (benthic organisms only), dis­ tion values of REE concentrations), underwent the same digestion pro­
solved REEs from the ozonated and sand-filtered Otonabee River water, cedure and analysis (Dang et al., 2023). The recovery of REEs in the two
and REEs from specified diets. The survival rate of organisms was 100 % SRMs ranged from 81 % to 100.6 % (Table S3).
during the experiment.
2.4. Chemical analysis
2.2. REE removal by the sand substrate
Elemental analysis was completed using Triple Quadrupole Induc­
To assess the potential capacity of the sand substrate to scavenge tively Coupled Plasma Mass Spectrometry (Agilent 8800) at the Trent
dissolved REEs, 240 mL of the sand substrate and 760 mL of Otonabee University Water Quality Centre. Elements were analyzed under three
River water were mixed into three 1-L HDPE bottles. The sand substrate gas modes following analytical procedures described by (Dang et al.,
was given an hour to settle, and the initial water samples were taken on 2022a). Major, minor, and trace elements (Cd, Co, Cs, Cu, Fe, Pb, Rb, Th,
day 1. On days 1, 5, 9, 12, 16, and 20, three water aliquots of 10 mL were U, V, Zn) were analyzed in helium collision mode to eliminate poly­
collected and filtered through 0.45 µm using syringe filters and acidi­ atomic interferences. REEs were analyzed in an MS/MS mode with O2 as
fied. The sand substrates (before and after the experiments) were dried the reaction cell gas (Dang et al., 2018). The quantification of Eu iso­
and analyzed using a scanning electron microscope (SEM, Hitachi topes (151Eu and 153Eu) can be affected by isobaric overlap from various
FlexSEM1000 II) with energy-dispersive X-ray spectroscopy (EDX, barium oxides and barium hydroxide interferences (Thompson et al.,
Bruker Quantax Compact 30). The dried sand was sprinkled onto 12 mm 2016), causing artificial positive Eu anomalies within samples. Because
carbon conductive tabs (Pleco, Ted Pella Inc.) and placed in the SEM- of their low abundance and potential polyatomic interferences, Eu iso­
EDX stage to collect images and elemental composition (C, O, Mg, Al, topes were not assessed and Eu concentrations were not reported. The
Si, K, Ca, Fe, and Na) using secondary electron, backscattered electron analytical procedure was verified using SRM NIST 1640a (Trace Ele­
and X-ray detectors. ments in Natural Water) and the river water CRM SLRS-6 (National
Research Council of Canada). A blank and water CRM were used to
2.3. Treatment of biological and feed samples bracket every ten samples. The measured concentrations are compared
against certified concentrations within solid and liquid CRMs (Tables S3
After exposure, organisms underwent a 72-h depuration in ozonated & S4).
and sand-filtered Otonabee River water without feed. A 72-h depuration
period was selected based on previous rare earth element exposure 2.5. Data analysis
studies (Cardon et al., 2020; Fasola, 2010; Lachaux et al., 2023; Lam and
Wang, 2006; Nørregaard et al., 2019). Minnows were housed in a 2.5.1. REE patterns, normalization, and calculation of anomalies
separate clean 16 L propylene container, and snails, mussels, and cray­ Firstly, the organotropism of REEs in each organism was assessed,
fish were housed in a second 16 L propylene container to allow the including organs such as soft tissues, internal organs, gills, and shells.
depuration of feed and feces from bodies. Daphnia magna underwent Then, REE concentrations were normalized against Post-Archean
depuration in separate 50 mL clean Falcon tubes to prevent sample loss Australian shale (PAAS, Bau and Dulski, 1996; McLennan, 2001; Tay­
due to predator consumption. After depuration, vertebrates were hu­ lor and McLennan, 1995); the PAAS-normalized concentrations are
manely euthanized according to the Animal Use Protocol #26697, hereafter referred to as REEPAAS. This normalization also allowed for the
approved by the Trent University Animal Care Committee. Minnows calculation of Ce anomalies (Ce/Ce*) to characterize the behaviour of Ce
were euthanized following the protocol “Use of MS-222”. The test sub­ relative to the abundance of their neighbouring REEs and trace
jects were rinsed twice with high-purity water (18.2 MΩ cm) and 0.5 % biochemical redox transformations (Dang et al., 2023; Piper and Bau,
ethylenediaminetetraacetic acid (EDTA) solution to remove REE 2013). Ce anomalies were calculated following Eq. 1 (Dang et al., 2023;
adsorbed on the organisms’ body surfaces (Cardon et al., 2020). The fork Och et al., 2014).
length and whole-body wet weight of test subjects were recorded before
CePAAS
dissection. The fish were dissected using a surgical razor blade, and Ce/Ce∗ = (1)
0.5 × (LaPAAS + PrPAAS )
individual tissues (soft tissue (n = 10), gills (n = 10), intestines (n = 10),
and liver (n = 10)) were placed in Falcon tubes. Due to the low weight, The PAAS-normalized REE patterns were used to quantify REE
we pooled tissue samples of five organisms in one composite sample, fractionation, i.e., the enrichment or depletion of three subgroups,
creating two replicates. Similarly, two replicate composite samples of ca. including LREEs, MREEs, and HREEs. Lanthanum, Tb, and Er were used
50 D. magna individuals were collected by centrifugation at 4500 rpm as representatives of the three LREE, MREE, and HREE subgroups,
for ten minutes. The pellets were separated from supernatant water and respectively. The particulate fraction is usually characterized by the
washed with high-purity water and EDTA. Crayfish were dissected into enrichment in LREE, i.e., a linear decrease from LREEs to HREEs, and
soft tissue (n = 4), hard tissue (n = 4), internal organs (n = 4), and therefore reflects TbPAAS/LaPAAS and ErPAAS/LaPAAS < 1 (Dang et al.,
antennal glands (n = 4), while mussels and snails were separated into 2023). The MREE enrichment is characterized by ErPAAS/LaPAAS < 1 and
soft (n = 5 & n = 6, respectively) and hard tissues (n = 5 & n = 6, TbPAAS/LaPAAS > 1, while the dissolved fraction (HREE enrichment) is
respectively). Each crayfish, snail, and mussel subsample was treated characterized by TbPAAS/LaPAAS and ErPAAS/LaPAAS > 1 (Dang et al.,
individually as discrete samples, creating four replicates for four cray­ 2023).
fish tissues (n = 16), six replicates for both snail soft and hard tissues
(n = 12), and five replicates for both mussel soft and hard tissues 2.5.2. Diet bioaccumulation factor and bioconcentration factor
(n = 10). Additional information about the number of organisms, tissue The bioaccumulation potential of REEs in organisms can be empiri­
dissection sub-samples, length, and feed sources are summarized in cally determined using the bioconcentration factor (BCF), which rep­
Table S2. After the dissection of all organisms, the samples were frozen resents the ratio of REE concentration in an organism (typically the

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A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

whole body, [REEs]organisms in mg kg− 1) to its dissolved concentration conducted using the Excel data analysis packages under ANOVA single
([REEs]water in mg L− 1). factor. The pairwise comparison was performed to demonstrate signifi­
cant differences between La, Tb, and Er group mean concentrations
[REEs]organisms
BCF = (2) within Otonabee River water on days 1, 5, 9, 12, 16, and 20. If the one-
[REEs]water way ANOVA reported a P value < 0.05, the null (Ho) hypothesis that
Comparably, the bioaccumulation factor (BAF) is typically calcu­ there is no difference between La, Tb, or Er on days 1, 5, 9, 12, 16, and
lated under field conditions as the ratio of the REE concentrations in an 20, was rejected. A Tukey’s HSD test determined if there was a signifi­
organism ([REEs]organisms) to the total chemical composition of REEs in cant difference between group means. If the difference between the two
the unfiltered water phase using the equation (Arnot and Gobas, 2006): means is greater than the HSD calculated (diff > HSD), then the two
means are considered significantly different.
[REE]organisms
BAF = (3)
[REE]dissolved + [REE]colloidal +[REE]particulate +[REE]diet 3. Results and discussion
The BCF was calculated and BAFs were adapted into diet bio­
3.1. Scavenging potential of dissolved REEs on the sand substrate
accumulation factors (DAF) to assess the enrichment of two REE frac­
tions (dissolved vs diet) within organisms. Diet bioaccumulation factors
The PAAS-normalized dissolved REE patterns were linear and
were calculated to determine the extent of REE accumulation in aquatic
showed an increasing trend from LREEs to HREEs (Fig. 1A), which re­
organisms’ tissue from the diet. The DAF is a ratio between the average
flected the REE pattern commonly referred to as “seawater-like” (Alibo
concentration of the studied biota tissue and that in their feed, following
and Nozaki, 1999; Johannesson et al., 2006; Pourret and Tuduri, 2017).
Eq. 4.
This behaviour is well documented in natural systems as LREEs have a
[REE]Organismsʹtissue higher affinity to create strong inner-sphere complexes with the car­
DAF = (4)
[REE]Feed bonates and oxides in the sand substrate (Figure S1), while HREEs tend
to remain in solution as dissolved REE-carbonate complexes (Byrne and
A DAF or BCF ratio > 1 indicates enrichment, whereas a ratio < 1 Li, 1995).
shows depletion. Furthermore, bio-accumulative chemical substances With increasing time after contact with the sand substrate, there is a
are identified using Canada’s Persistence and Bio-accumulative Regu­ depletion of dissolved light, medium, and heavy REEs and the equilib­
lations; a DAF or BCF value over 5000 indicates very bio-accumulative rium was reached after two weeks (Fig. 1B). For instance, La concen­
substances, whereas values between 2000 and 5000 indicate sub­ trations depleted in Otonabee River water from 29 ± 2 ng L− 1 on day 1
stances with high bioaccumulation potential (Arnot and Gobas, 2006; to 5.6 ± 0.1 ng L− 1 by day 20. The Tb and Er concentrations decreased
Government of Canada, 2023). For toxicity recommendations, BCF from 1.0 ± 0.1 ng L− 1 to 0.31 ± 0.02 ng L− 1 and 4.5 ± 0.1 ng L− 1 to
values should be mass-weighted based on the percentage a tissue con­ 1.9 ± 0.2 ng L − 1, respectively. We observed a preferential removal of
stitutes of the total body weight (Mackay et al., 2018). For instance, the LREEs (80.2 ± 2.9 %, n = 3) compared to MREE (67.4 ± 5.0 %, n = 3)
intestines constitute 5 %, and muscle constitutes 50–80 % of body and HREE (56.4 ± 5.5 %, n = 3) from the Otonabee River water
weight, thus the highest metal burdens may be in muscles (Wood et al., (Fig. 1A). The percent difference means from day 1 to day 20 for LREEs,
2012). Here, we chose to consider individual tissues rather than the MREEs, and HREEs were significantly different (ρ = 0.006 ANOVA).
mass-weighted approach to identify the specific enrichment of REEs. Lanthanum held the highest average percent difference (ρ < 0.05 Tukey)
Furthermore, BCF and DAF were calculated for composite samples of compared to Tb and Er. A description of the various minerals in the sand
minnow tissues and Daphnia magna, in addition to DAF values for substrate and mechanisms responsible for scavenging dissolved REEs
discrete individual tissues of snails, mussels, and crayfish. Given the can be found in supplementary text 1 and Figure S1. Similar obser­
limited information on the uptake mechanism of REEs into aquatic or­ vations were made studying the REE cycling and transportation from the
ganisms, we also related REE organotropisms and bioaccumulation Congo River into the sea by analyzing quartz samples (Garzanti et al.,
patterns to other trace elements (such as Cd, Co, Cs, Cu, Fe, Pb, Rb, Th, 2021). The silt and coarse sand had REE patterns with significant LREE
U, V, Y, and Zn) with better documented biological roles. enrichment. This experiment highlighted active scavenging of REEs onto
the sand substrate, confirming that benthic organisms may be exposed to
2.5.3. Statistics REEs through this additional particulate phase, which has a unique
Analysis of Variance (ANOVA) followed by Tukey’s HSD test was LREE enrichment pattern.

Fig. 1. A) PAAS-normalized REE patterns of Otonabee River water over time after the contact with the sand substrate. The black-and-white gradient reflects the
temporal sampling from day 1 (D1, black) to day 20 (D20, white). B) Variations of the average (n = 3) concentrations of La (LREE), Tb (MREE), and Er (HREE) in
Otonabee River water over time after the introduction of the sand substrate. The compact letters in B) display Tukey post hoc test results for pairwise comparison
among REE concentrations.

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3.2. REE organotropism and REE fractionation in the organs relative to pores at the base of the antenna (Riegel, 1966). The similar concentra­
exposure pathways tions of REEs in the antennal glands and the diet suggest the regular
transit of feed through this organ. The uptaken metals from the diet can
3.2.1. Northern clearwater crayfish (Faxonius propinquus) be further transferred into other internal organs. However, the
Using Ce as a representative REE, the REE organotropism in crayfish decreasing concentrations in internal organs and soft tissues (Fig. 2)
is as follows: antennal gland (1821 ± 549 µg kg − 1) > hard tissue (818 indicate a low transfer potential because of efficient excretion through
± 196 µg kg − 1) > internal organs (212 ± 143 µg kg − 1) > soft tissue the antennal glands or detoxification through the hepatopancreas
(59 ± 30 µg kg − 1) (Fig. 2 and S2F, Table S5). The organotropism pat­ (Guner, 2010).
terns for our crayfish were similarly found in marbled crayfish exposed On the other hand, the concentrations of REEs, Fe, V, Th, and U, were
to La-based coagulant (Goitom, 2011). Besides, the enrichment of Cd, found to be second highest in the hard tissues, which are a composite of
Zn, and Cu in our crayfish samples followed the decreasing order of cheliped, carapace, and pereiopods structured by a framework of
internal organs > antennal glands > soft tissue > hard tissue (Table S6), α-chitin/protein microfibres and Ca carbonates (Sugawara et al., 2006).
previously reported in multiple crayfish species (Guner, 2010). The The lattice of these materials can retain dissolved metals by weak
significant correlation between La and Fe in crayfish tissues (Fig. 3) is complexes (Chassard-Bouchard and Hallegot, 1984), explaning the
also noteworthy. Iron is an essential element used in crayfish for accumulation of these trace elements in hard tissues from dissolved
metabolism and in constituents of cytochrome proteins (Vuori, 1995). fractions.
This strong relationship between Fe and La indicates similar uptake,
storage, repartition, and elimination pathways or similar biochemical 3.2.2. Black sandshell mussel (Ligumia recta)
functions in crayfish. Further studies are required to investigate such Mussels have the potential to accumulate pollutants in their tissues at
relationships. elevated levels related to pollutant availability in the diet or dissolved
The PAAS-normalized REE patterns for crayfish tissues show MREE forms (Beyer et al., 2017). Within this study, the soft tissue samples of
enrichment, which reflects their diet (Figure S3F). Nevertheless, the mussels are a composite of their gills, digestive gland, hemolymph, and
normalized REE concentrations in internal organs, hard and soft tissues rest of the soft tissues, which have higher REE concentrations ([Ce] of
were 1–2 orders of magnitude lower than the diet, whereas levels in 3962 ± 2032 µg kg − 1) than hard tissue (1381 ± 357 µg kg − 1) (Fig. 2
antennal glands are in the same order of magnitude as their diet and S2B, Table S5). The soft tissue concentrations are also two to three
(Figure S3F). The fractionation signatures (TbPAAS/LaPAAS and ErPAAS/ orders of magnitude higher than that of their diet (Figure S3B, Table S7).
LaPAAS) of crayfish hard tissue, internal organs, and soft tissues (brown The higher REE concentrations in our mussel soft tissues compared to
symbols in Fig. 4) overlap with the signatures of both the river water and hard tissue are similar to literature data for various mollusc species
their diet (blue circle and brown cross symbol in Fig. 4). These over­ (Weltje et al., 2002). The REE organotropisms in the soft tissues of
lapping signatures create difficulty in differentiating whether diet or Corbicula fluminea clams after exposure to dissolved Nd, Gd, and Yb
dissolved exposure is the dominant pathway by which crayfish uptake followed the decreasing order of gills > digestive glands > rest of soft
REEs. tissues > hemolymph > mantle (Lachaux et al., 2023). Further, within
The REE organotropism order can be explained by crayfish physi­ the freshwater mussel Hyriopsis cumingii, the mantle attached to the shell
ology; crayfish passively absorb dissolved trace metals from their diet held the highest REE concentrations compared to the muscle, foot, and
(Guner, 2010) or through the permeable ectodermal hard tissues siphon (Xu et al., 2022). It has been suggested by Merschel and Bau,
(Rainbow and White, 1989). For instance, the antennal glands accu­ (2015) that REEs are incorporated in the carbonate shells of mussels
mulated the highest concentrations of REEs, Fe, Pb, Sc, V, Th, and U after uptake from ambient waters and food. Rare earth elements could
(Table S5 & S6) because the glands act as the excretory organ through pass through the mantle via extrapallial fluid and into the inorganic Ca

Fig. 2. Average concentrations of La, Tb and Er in partitioned tissues within benthic (snail, mussel, crayfish) and pelagic (minnows, D. magna, and E. gracilis) or­
ganisms, compared to their feed sources (coloured cross symbols) and Otonabee River (dark blue circle). Tissue types are represented by various shapes: circle (soft
tissue), square (hard tissue), half-filled circle (intestines/internal organs), half-filled square (gills), and diamond (antennal gland). Feed sources are represented by
coloured cross symbols: shrimp pellet for crayfish (brown), spirulina flake for minnows (purple), and a combination of spirulina and chickpea powder for snail,
mussel, and D. magna (pink).

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A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

Fig. 4. Biplot of TbPAAS/LaPAAS as the function of ErPAAS/LaPAAS in benthic and

pelagic organisms, Otonabee River, and feed sources. Refer to the caption of
Fig. 3 for symbol and colour legend. Note that TbPAAS/LaPAAS represents the
ratios of MREE/LREE while ErPAAS/LaPAAS represents the ratio of HREE/LREE.
The gray texts, i.e. “Hat-shaped, LREEEnrichment, HREEEnrichment, identify the
main REE pattern quadrants such as the dominance of MREEs, and the linear
decrease with enrichment of LREEs in particles.

fractionations in bivalve mussels have been previously studied to

determine whether the accumulation of trace elements is associated
with dissolved or particulate sources. For instance, the REE patterns in
hard and soft tissue of bivalves from Tokyo Bay resembled patterns of
resuspended particles, indicating REE accumulation was due to expo­
sure to sediment (Akagi and Edanami, 2017). A similar confirmation was
obtained for oysters from the Pearl River Estuary of China based on
different REE anomalies in dissolved, particulate, and biological samples
(Ma et al., 2019).

3.2.3. Chinese mystery snail (Cipangopaludina chinensis)

Snail soft tissue (combination of the viscera and foot, [Ce] ~ 1287
± 493 µg kg− 1) contained higher concentrations of REEs and other trace
elements (Zn, V, Co, Cu, Cd, Cs, Y, Rb, U, and Pb) than in their hard
Fig. 3. A) Correlation between the average concentrations of La and Fe in
tissues ([Ce] ~ 404 ± 54 µg kg− 1) (Table S5 & S6, Figure S2A). The soft
partitioned tissues of crayfish, mussels, E. Gracilis, and minnow. B) Correlation tissue of snails acts as a more effective sink for metal accumulation than
between La and Fe in all tissue samples of crayfish. Tissue types are represented the hard tissue because of metal storage in subcellular fractions
by various shapes: circle (soft tissue), square (hard tissue), half-filled circle (Dallinger and Wieser, 1984; Gimbert et al., 2008). It should be noted
(intestines/internal organs), half-filled square (gills), and diamond (antennal that both soft and hard tissues of our snail samples have higher REE
gland). The colors represent different organisms: brown (crayfish), purple levels than their diet (Figure S3A). The fractionation patterns of snails
(minnows), yellow (mussel), green (E. gracilis), and light blue (D. magna). (red symbols in Fig. 4) also point toward the LREE-enrichment quadrant,
suggesting a potential contribution from the sand substrate, which has
concretions of carbonate shells (Marigómez et al., 2002; Merschel and been the case for mussels.
Bau, 2015). Rare earth elements could be incorporated in the position of Among the trace elements we measured, there was a correlation
the Ca ion in the crystal lattice (Zhong and Mucci, 1995) during calci­ between REEs, V (R2 = 0.76), and Cs (R2 = 0.61) (Figure S4). These
fication and shell formation (Lachaux et al., 2023) due to the similarity elements have different ionic radii and charge numbers (Shannon,
of ionic radii (1.03 Å to 0.86 Å for La to Lu vs. 1.00 Å for Ca) (Merschel 1976), indicating non-selective uptake mechanisms (Aharchaou et al.,
and Bau, 2015; Shannon, 1976). 2020; Crémazy et al., 2019). Though limited studies have investigated
The PAAS-normalized REE patterns for the soft and hard tissue of the uptake mechanisms of REEs into aquatic snails, we can compare our
mussels show a distinctive enrichment of LREEs compared to MREEs and results to the uptake mechanisms of other trace elements. Littorinid
HREEs; both TbPAAS/LaPAAS and ErPAAS/LaPAAS are < 1 (yellow symbols snails exposed to dissolved Tl and Tl-amended green macroalgae (Ulva
in Fig. 4). This signature is different from that of the water (blue symbol) lactuca) in a 20:1 ratio, accumulated 2 % of dissolved Tl versus 15 %
and the diet (pink cross symbol), suggesting a third end member that can from the diet (Turner and Pilsbury, 2013). Even though the relative
be uniquely represented by the sand substrate that has been significantly contribution of metals through the aqueous form is higher, metals from
enriched in LREEs (see Section 3.1). Rare earth element patterns and the diet seem to accumulate in the soft tissues (Turner and Pilsbury,

6
A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

2013). The REE organotropism for partitioned minnow tissues followed the
decreasing order of intestines > liver > swim bladder ~ gills (Fig. 2).
3.2.4. Euglena gracilis The REE concentrations in soft tissues were below analytical detection
Rare earth element binding and uptake into phytoplankton cells due limits. The REE organotropism for our minnows can be compared to
to their analogy with essential elements could be one of the most wild-caught fish. Common sole (Solea solea) (Labassa et al., 2023), yel­
important processes explaining REE accumulation in E. gracilis low eels (Lortholarie et al., 2021), arctic char (Salvelinus alpinus)
(Valcheva-Traykova et al., 2014). The uptake of Nd3+ and Ce3+ in (Nørregaard et al., 2019), rainbow trout (Oncorhynchus mykiss) (Cardon
E. gracilis led to decreases in Zn, Ca, and Fe content, suggesting a et al., 2020), and lumpfish (Cyclopterus lumpus) (Østerås, 2023) held the
competitive uptake through similar pathways (Shen et al., 2002). highest levels of REEs in gills (i.e., gills > kidneys > liver > soft tissue).
Furthermore, it has been suggested that Nd3+ can be transported into Despite the common organotropism in various fish species, differ­
cellular compartments through Ca ion channels, with the largest quan­ ences in depuration and elimination response times exist. The ability to
tity of Nd3+ residing in chloroplasts and replacing Mg in chlorophyll excrete metals during depuration is related to the response time of
(Kang et al., 2000). The substitution of Mg2+ by REEs in chlorophyll enzymatic activities surrounding the detoxification of non-essential el­
suggests REEs accumulate in E. gracilis by replacing essential elements ements (Regoli et al., 2011), such as the production of metallothionein
from the ion binding sites on proteins (Prokop et al., 2015). (Si and Lang, 2018) which binds and sequesters metals from the in­
The REE patterns for E. gracilis were similar to the Otonabee River testines, liver, and gills (Deb and Fukushima, 1999). After three days of
water (Figure S3C). However, the absorption process of REEs by depuration, our minnows held the highest REE levels in the intestine and
phytoplankton and algae is complex and depends on REE availability liver, the main sites for sequestration and detoxification of non-essential
and chemical speciation. It has been demonstrated that MREEs have elements (Deb and Fukushima, 1999). Therefore, temporarily enhanced
slightly higher stability constants for biological uptake sites to REE bioaccumulation in the liver and intestines of minnows could be
outcompete cellular binding spots on phytoplankton (Costa et al., 2020; due to a higher presence of metallothionein-bound metals and unregu­
Dang et al., 2023; Tan et al., 2017). Furthermore, when dissolved REEs lated enzymatic response times (Deb and Fukushima, 1999). Further­
were equally available, HREEs with the largest ionic radii were least more, the assimilation efficiency of diet REEs was 0.8–3 % in rainbow
preferentially uptaken by Euglena gracilis (Ishii et al., 2006), Gracilaria trout, highlighting the low transfer of diet REEs into fish (Cardon et al.,
gracilis (Costa et al., 2020; Jacinto et al., 2018), and microalgae (Costa 2020). Overall, minimum REE levels within gills and swim bladder and
et al., 2020). Such fractionation processes might influence the change in maximum REE levels in excretory organs suggest minnows effectively
REE patterns we observed for Euglena gracilis (Fig. 4); the TbPAAS/LaPAAS eliminate diet and dissolved REEs post-exposure.
decreased from the value of the river water (~ 1.7) to that of the algal Most minnow tissues are characterized by an enrichment of HREEs, i.
cells (1.2 ± 0.1), highlighting a flatter pattern in biological tissues. e., TbPAAS/LaPAAS and ErPAAS/LaPAAS > 1, which further accentuated the
Despite this slight fractionation between REEs, the overall signature of river water signature (blue circle in Fig. 4) and their diet (purple cross in
REEs in algae (green symbol) remains close to river water (blue symbol) Fig. 4). The opposite direction between the diet and fish tissue would
in the HREE-enrichment quadrant (Fig. 4). indicate minimal contributions from the diet and additional REE frac­
tionation from the dissolved fractions. Minnows could uptake REEs
3.2.5. Daphnia magna similarly to Ca2+ past the cells of the branchial epithelium of gills via
D. magna accumulated low REE levels within the whole body passive influx through divalent protein transporters located in the gills
(Figure S3D), ranging from Ce (30.7 ± 1.9 µg kg− 1) to Yb (1.9 (Flik et al., 1995; Martin and Frederick, 1979). It is, however, uncertain
± 0.1 µg kg− 1) (Table S5). Rare earth element patterns for the whole whether such processes induce REE fractionations, i.e., the differential
body of D. magna were linear, following their Otonabee River water uptake of HREEs relative to LREEs.
patterns and overlapping their diet (spirulina & chickpea powder) pat­ In summary, the fractionation signatures highlight the dissolved
terns (Figure S3D). Our D. magna samples were characterized by an fractions as the main exposure pathway to pelagic organisms. The
enrichment of HREEs, holding a HREE fractionation (ErPAAS/LaPAAS of effective digestive elimination decreases the possibility of REEs being
2.1 ± 0.1) that was higher than the signature of the river water (blue assimilated from the diet signatures. On the other hand, benthic or­
circle in Fig. 4) and had a MREE fractionation (TbPAAS/LaPAAS of 1.1 ganisms might have more complex exposure pathways. The REE signa­
± 0.1) similar to their diet (1.3 ± 0.3, pink cross in Fig. 4). tures in crayfish overlap for the three sources of REEs, while the sand
D. magna was used as a model organism to determine the fraction­ substrate seems to be the dominant source of REEs to snails and mussels,
ation/distribution of particulate La vs. ionic Gd (Revel et al., 2023). as identified by the LREE-enrichment signatures. Overall, it is important
Ingested La precipitates accumulated in the intestines of D. magna, to consider factors such as the physiochemical behaviour of REEs in
whereas ionic Gd3+ accumulated in tissues via metal-transporting pro­ organisms, REE availability, and binding capacities, which impact
teins. The accumulation of REEs in intestines did not induce lethal ef­ whether REEs accumulate into the organisms via the diet, dissolved, or
fects since D. magna detoxified diet REEs, whereas ionic Gd taken up particulate form.
through the exoskeleton or gills, lowered mobility and induced oxidative
stress (Di Toro et al., 2001; Revel et al., 2023). 3.3. Ce/Ce* anomalies
This organism has various mechanisms for eliminating REEs; 75 % of
REEs absorbed through the gills and exoskeleton in D. magna are Cerium anomalies are used to reveal the enrichment (Ce/Ce* > 1) or
detoxified through sequestration in specific subcellular compartments, depletion (Ce/Ce* < 1) behaviours of Ce caused by environmental
e.g., the NaOH-resistant fractions (Cardon et al., 2019). Further, processes decoupling Ce relative to neighbouring REEs (Barrat et al.,
16–70 % of diet trace metals are lost to offspring production, moulting, 2023). The Otonabee River is characterized by a negative Ce anomaly
metal excretion, and fecal excretion (Barata et al., 2002; Tsui and Wang, (Ce/Ce* = 0.8). However, spirulina flakes - the diet for minnows -
2007; Yu and Wang, 2002). These detoxification and elimination contained positive anomalies (1.7 ± 0.05), while the diet for D. magna,
mechanisms might help D. magna minimize the uptake of REEs into their mussels, and snails had no Ce anomalies (1.0 ± 0.03) (Table S8). In the
bodies, explaining the low REE levels compared to other organisms tissues, D. magna (0.6 ± 0.1), E. gracilis (0.5 ± 0.02), mussels (0.05
(Fig. 2). ± 0.01), snails (0.9 ± 0.04), and the soft tissues (0.5), gills (0.8), liver
(0.8), swim bladder (0.5), and intestines (0.7) of minnows contain
3.2.6. Striped shiner minnow (Luxilus chrysocephalus) negative Ce anomalies that were lower than their respected diet and
The lowest REE concentrations within minnows were found in the water exposures (Fig. 5, Table S8).
gills and swim bladder, and the highest in the intestines (Fig. 2 and S2E). The negative cerium anomaly in the Otonabee River water suggests

7
A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

involving siderophores secreted by microbes (Kraemer and Bau, 2022).

The crayfish feeding habit relies on vegetation, prey, decaying materials,
and detrital biofilm (Ercoli et al., 2021) with their appendages. It is
speculative at this stage, but our crayfish might uptake particles or the
biofilm enriched in Ce+IV, leading to pellicular positive Ce anomalies
(Figure S5A & B). However, further studies will be required to investi­
gate this hypothesis.

3.4. Bioconcentration factor (BCF) and diet bioaccumulation factor

(DAF)

3.4.1. BCF & DAF for pelagic organisms

Relative to their diet, the REE concentrations in D. magna ([Ce] ~
31 ug kg− 1 ± 2) and minnows ([Ce] ~ 93 ug kg− 1) are significantly
lower than their respected spirulina/chickpea powder ([Ce] ~
75 ug kg− 1 ± 26) and spirulina flakes ([Ce] ~ 840 ug kg− 1) (Fig. 2,
Table S5). Therefore, the DAF values for REEs in pelagic organisms are
< 1 (Fig. 6C and D), reflecting the biodilution of diet REEs. The BCF
values for REEs in pelagic organisms are >1 (Fig. 6C, Table S9),
reflecting enrichment near the bioaccumulation potential threshold of
2000. Nevertheless, BCF values for REEs are one to three orders of
magnitudes lower than those of other bioaccumulative trace elements, e.
g., Zn, Cu, V, and Pb (Figure S6). This finding confirms that REEs behave
distinctly from other divalent trace elements and might have limited
bioaccumulation risks for these organisms, as previously suggested by
lab and field studies (Amyot et al., 2017; Cardon et al., 2020; Macmillan
Fig. 5. Ce anomalies of partitioned tissue parts within benthic and pelagic et al., 2017).
organisms, and their respected food and water exposures. The dashed blue line The BCF values of REEs and other trace elements (Co, Cs, Pb, Rb, U,
indicates Ce anomaly of Otonabee River (Ce/Ce* = 0.8), while the horizontal V, and Zn) for minnow tissues are 3–4 magnitudes higher than DAF
black line indicates the absence of Ce anomaly (Ce/Ce* = 1). See the caption of (Fig. 6C and S6). These results relate to the fractionation signatures
Fig. 3 for symbol and colour legend.
found in pelagic organisms and their exposure. The REE signatures in
minnows were similar to water, indicating that minnows’ primary up­
in situ oxidative transformation of Ce+III into Ce+IV (El-Akl et al., 2015; take mechanisms would be dissolved REEs through the gills. These re­
Jiang et al., 2022; Sholkovitz, 1995). Ce+IV is less soluble, less mobile, sults align with those reported by Cardon et al. (2020) as the authors
and highly surface-reactive compared to Ce+III (Byrne and Kim, 1990; observed a strong correlation between dissolved Y and Y concentrations
Tostevin, 2021) and is, therefore, depleted from the aqueous environ­ in the gills but minimal transfer of Y into internal organs (Section 3.2.6).
ment. The negative Ce anomalies found in test subjects were consistent Our BCF values are similar to BCF values for various fish species
in arctic char, cod, whitefish, sculpin (Macmillan et al., 2017; Marginson collected in the field, e.g., reservoirs in Washington State (Mayfield and
et al., 2023), molluscs, crabs (Wang et al., 2019), and snails (Weltje Fairbrother, 2015), the Po River (Pastorino et al., 2024), and 14 lakes in
et al., 2002). It has been suggested that Ce anomalies in aquatic or­ southern Quebec (Amyot et al., 2017). It is a common fact that BCF
ganisms reflect Ce bio-availability (Macmillan et al., 2017); when there values reported in environmental studies are higher than BCF values
is less dissolved Ce available (more negative Ce/Ce*) in the aquatic reported in exposure laboratory studies, such as in carp (Cyprinus carpio)
environment, less Ce is uptaken. exposed to dissolved LREEs (Hao et al., 1996). However, our minnow
In this study, various organisms, e.g., minnows, D. magna, and BCF values were also higher than carp (Cyprinus carpio) BCF values. The
E. gracilis had lower Ce anomaly values than Otonabee River water and accumulation of chemicals in aquatic organisms might differ based on
respective diet exposures (Fig. 5, Table S8). Ce anomalies in minnow the exposure levels. For example, interpreting BCF values in laboratory
tissue are significantly lower than the diet but align with river water exposure experiments requires considering the inverse relationship for
(Fig. 5), confirming dissolved REEs as the primary exposure pathway to BCF vs exposure concentrations; BCF values were highest during low or
minnow (Section 3.2.6). The negative Ce anomalies in minnows, natural exposure concentrations but lower when exposure concentra­
D. magna, and E. gracilis could be due to the further transformation of Ce tions increased because of differential accumulation rates (Mcgeer et al.,
+III
into Ce +IV through biochemical oxidative pathways within the cells, 2003).
as suggested in marine phytoplankton (Dang et al., 2023). Marginson Additionally, DAF values gradually increased from LREEs to HREEs
et al., (2023) also related Ce anomalies in the liver and bone of fish to in minnow organs (Fig. 7A). This fractionation indicates that LREEs
their size, indicating metabolic, ecological, and environmental might be less bioavailable than HREEs. This finding corroborates with
influence. the dissolved REE patterns highlighted by HREE enrichments because of
In contrast, crayfish tissues exhibit positive Ce anomalies (between 1 reactivity with dissolved carbonates and ligands, ultimately pointing
and 1.5), which is higher than their shrimp pellet diet (1.0 ± 0.01) and toward a more significant contribution of the dissolved REE.
Otonabee River water (0.8) (Fig. 5). Higher Ce/Ce anomalies were
observed in hard tissues and the antennal gland with higher Ce con­ 3.4.2. BCF & DAF for benthic organisms
centrations (Figure S5A) but lower zinc (R2 = 0.97, n = 4, Figure S5B). The BCF values for benthic organisms were not reported because a
These two tissues are directly in contact with environmental media: the large proportion of dissolved REEs scavenged onto the sand substrate
hard tissue contacts with river water and sand substrate, while the (Fig. 1). Instead, the primary exposure of REEs to benthic organisms was
antennal gland excretes ingested particles and feed. In the environment, through the diet and particulate forms. The respective contribution of
the accumulation of Ce and high Ce anomalies might be related to the the sand substrate vs. the diet on the assimilated REE concentrations in
bioavailability to crayfish of the oxidized Ce+IV on reactive surfaces (e. the organisms cannot be determined. Therefore, DAF values based on
g., ferric deposit, Ratié et al., 2020) or by bio-mediated processes the diet are reported only for comparison between organisms and

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A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

Fig. 6. Diet bioaccumulation factors (DAF, square) and bioaccumulation concentration factors (BCF, triangle) for benthic (A-B) and pelagic (C-D) organisms. DAF
and BCF ratios were calculated for representative light (La, left panels) and heavy (Er, right panels) REEs. Organisms are represented by various colours: red (snail),
yellow (mussel), brown (crayfish), purple (minnow), green (E. gracilis), blue (D. magna). A BCF or DAF > 1 indicates enrichment of REEs into the tissues. Specifically,
2000 < BCF/BAF < 5000 and BCF/BAF > 5000 indicate bio-accumulative and very bio-accumulative potential, respectively. See text for more details.

Fig. 7. Comparison of diet accumulation factors (DAF) of REEs within the A) soft tissues of D. magna and internal organs of minnows and B) soft tissues of
benthic organisms.

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A. Kernaghan and D.H. Dang Ecotoxicology and Environmental Safety 290 (2025) 117561

individual REEs. dissolved form and benthic organisms (snails and mussels) uptake REEs
The REE concentrations within the soft and hard tissues of snails and mainly from the diet and particulate forms.
mussels are 1–3 orders of magnitude higher than REE concentrations in The bioaccumulative uptake of dissolved REEs into pelagic organ­
their diets, i.e., spirulina and chickpea powder ([Ce] ~ 75 ug kg− 1 isms remained high, based on BCF calculations, suggesting high transfer
± 26) (Fig. 2, Table S5). These results suggest that snails and mussels risks throughout the food web. The BCF values (72–1495, Table S9) for
have the potential to bioaccumulate REEs from their feed or sand sub­ REEs in minnow organisms were in a similar range with BAF values
strate. The DAF values for REEs (Fig. 6, Table S9 and S10) and trace (15− 57,698) from various freshwater fish collected from a Washington
elements Cd, Co, Cs, and U (Figure S7) in mussel soft tissue are one order reservoir (Mayfield and Fairbrother, 2015), from southern Quebec lakes
of magnitude higher than that of snail soft tissue. However, the DAF (19.95) (Amyot et al., 2017), and BCF values of Cyprinus carpio
values for trace elements Pb, Rb, U, V, and Zn are within the same range (0.48–978) (Hao et al., 1996). It is important to note that we calculated
for both snails and mussels (Figure S7). Further, DAF values of LREEs for BCF values using metal concentrations from water samples filtered at
snails and mussels are one order of magnitude higher than that of MREEs 0.45 µm, which might include some colloid fractions, which does not
and HREEs (Fig. 7B). Similarly to our mussel samples, oysters and represent total dissolved metal concentrations. While there is no evi­
mussels exposed to sediment on the eastern coast of China (Zhao et al., dence that colloidal REEs are bio-accumulative to organisms, further
2022) and unfiltered suspended particles in coastal systems of the Vigo studies using different filtration cut-offs might be required to shed light
Ria in Spain (Rodríguez-Velarte et al., 2022) showed preferential on this environmental-relevant component. On the other hand, benthic
enrichment (> 1) of LREEs versus MREEs and HREEs. These patterns are organisms can bioaccumulate diet REEs more significantly in their soft
similar to that of the particulate fraction (Section 3.2.2 and 3.2.3), tissue. The DAF values for snails (from 3.1 ± 1.5 to 21.8 ± 16.8) and
confirming the prevalence of particulate fractions in governing REE mussels (from 8.3 ± 4.7 to 161.2 ± 143.7, Table S9 & S10) were in
accumulation in benthic organisms (Section 3.2). similar range to oysters (1.49) and mussels (1.10) collected from the
On the other hand, REE concentrations in the antennal glands of Chinese coastline (Zhao et al., 2022) but 1–5 magnitudes lower then
crayfish are the same magnitude as their pellet feed (Fig. 2), while the BAF values (3000–20000) for mussels from Vigo Ria (Rodríguez-Velarte
soft tissue, hard tissue, and internal organs of crayfish have REE con­ et al., 2022). Within this study, mussels and snails are the most sensitive
centrations lower than their shrimp pellet feed (Fig. 2). These results to bioaccumulate particulate REEs and minnows to bioaccumulate dis­
suggest that crayfish organisms do not have the potential to bio­ solved REEs. These organisms could be used to bio-monitor ecosystems
accumulate REEs from their feed, explaining the difficulty in assigning a vulnerable to rising REE levels.
primary exposure pathway for this organism (Section 3.2.1). Among the
REE subgroups, crayfish did not have preferential bioaccumulation as CRediT authorship contribution statement
their DAF patterns were flat and remained at ca. 0.31 ± 0.05 (Fig. 7,
Table S9 and S10). Relative to snails and mussels, the DAF values for Ashlyn Kernaghan: Writing – review & editing, Writing – original
REEs (Fig. 6) and other trace elements for crayfish are < 1 (Figure S7), draft, Visualization, Validation, Project administration, Methodology,
indicating limited capacity to bioaccumulate trace elements. In envi­ Investigation, Formal analysis, Data curation, Conceptualization. Huy
ronmental studies, crayfish hold a higher bioaccumulation potential of Duc Dang: Writing – review & editing, Validation, Supervision, Meth­
REEs when subjected to REE levels between 100 and 10,000 mg/L but odology, Investigation, Funding acquisition, Formal analysis,
excreted REEs during depuration (Fasola, 2010). Conceptualization.
The use of bioaccumulation factors needs to be carefully considered
when looking at the bioaccumulation potential of metals in organisms Declaration of Competing Interest
through various exposure routes. The highest susceptibility of organisms
to bioaccumulate metals depends on metals’ uptake mechanisms The authors declare that they have no known competing financial
through various exposure routes (dissolved, diet, and particulate). Bio­ interests or personal relationships that could have appeared to influence
accumulation factors often consider the unfiltered fraction as bioavail­ the work reported in this paper.
able (Revel et al., 2023), and they represent accumulation from all
exposure routes (dietary absorption, transport across respiratory sur­ Acknowledgements
face) (Gobas and Morrison, 2000). However, the concentrations
measured in whole organisms do not necessarily mean that con­ The authors acknowledge the financial support from NSERC to D.H.
taminant–receptor interactions are occurring with the dissolved solution D. (Discovery Grant) and A.K. (Undergraduate Student Research
(Revel et al., 2023). For example, aquatic snails bioaccumulate metals in Awards). We thank the Trent University Animal Care Facility staff,
the intracellular granules or vesicles in the digestive glands from expo­ including the manager (Jason Allen) and technicians (Cynthia Grant &
sure to the diet or sediment (Krupnova et al., 2018). Therefore, BAF Andrea Rogers). The authors also thank Spencer Grieve for his assistance
values for snails should be based on diet and particulate exposures; the during field sampling campaigns and Dr. Wei Wang for his support
conventional approach, considering only the unfiltered dissolved solu­ relative to chemical analysis. The authors thank Dr. Karla Newman and
tion, would neglect an important exposure pathway. Nevertheless, Dr. Hayla Evans of the Trent Water Quality Centre, for their technical
further studies are required to highlight the subcellular distributions of and analytical support.
REE accumulation and whether the signatures of exposure (dissolved,
diet, vs particulate) are undergoing active metabolism and affecting the Appendix A. Supporting information
physiology of the organisms (Revel et al., 2023).
Supplementary data associated with this article can be found in the
4. Conclusion online version at doi:10.1016/j.ecoenv.2024.117561.

An in-depth understanding of REE bioavailability and exposure Data Availability

mechanisms to aquatic organisms is timely given the increasing demand
and use for REE globally. This question can be addressed based on rare Data will be made available on request.
earth element fractionations, Ce anomalies, and bioaccumulation cal­
culations (BCF and DAF). Our results highlighted that, under environ­
mental conditions, the uptake mechanisms of REEs into pelagic
organisms (minnows, D. magna, and E. gracilis) were mainly the

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