Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 August 2020 | 12(11): 16510–16520
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
doi: https://doi.org/10.11609/jott.5903.12.11.16510-16520
#5903 | Received 26 March 2020 | Final
received 30 July 2020 | Finally accepted 05 August 2020
First record of a
morphologically abnormal and highly metal-contaminated Spotback
Skate Atlantoraja castelnaui
(Rajiformes: Arhynchobatidae)
from southeastern Rio de Janeiro, Brazil
Rachel Ann Hauser-Davis
1 , Márcio L.V. Barbosa-Filho 2 , Lucia Helena S. de S.
Pereira 3 ,
Catarina A. Lopes 4 ,
Sérgio C. Moreira 5 , Rafael C.C. Rocha 6 , Tatiana D. Saint’Pierre 7 ,
Paula Baldassin
-8 & Salvatore
Siciliano 9
1 Laboratório de Avaliação e
Promoção da Saúde Ambiental, Instituto Oswaldo Cruz/Fiocruz, Av. Brazil, 4.365, Manguinhos, Rio de Janeiro, 21040-360, Brazil.
1.5,9 Grupo de Estudos de Mamíferos
Marinhos da Região dos Lagos (GEMM-Lagos), Rua São José 1.260, Praia Seca,
Araruama,
RJ 28970-000 Brazil.
2 Programa de Pós-graduação em Etnobiologia e Conservação da
Natureza, Universidade Federal Rural de Pernambuco, Campus Dois Irmãos,
52171-900, Recife, PE, Brazil.
3,6,7 Departamento de Química, Pontifícia Universidade Católica
do Rio de Janeiro (PUC-Rio), Rua Marquês de São Vicente, 225, Gávea,
22453-900 Rio de Janeiro, RJ, Brazil.
4 Programa de Pós-graduação em
Ecologia e Evolução, Universidade Estadual do Rio de Janeiro, Rua São Francisco
Xavier, 524, Maracanã, 20550-900, Rio de Janeiro, RJ, Brazil.
5 Programa de Pós-graduação em
Zoologia, Museu Nacional, UFRJ, Quinta da Boa Vista, São Cristóvão, Rio de
Janeiro, RJ 20940-040 Brazil
8 BW Consultoria Veterinária, Praia
Seca, Araruama, RJ 28970-000 Brazil.
9 Laboratório de Biodiversidade,
Instituto Oswaldo Cruz/Fiocruz, Pav. Mourisco sala
217, Manguinhos, Rio de Janeiro, RJ 21040-900 Brazil.
1 rachel.hauser.davis@gmail.com (corresponding author), 2 titobiomar1@gmail.com,
3 luciahelena.rj@hotmail.com,
4 catarina.amorim.lopes@hotmail.com,
5 sergiocmoreira@gmail.com, 6 rafaelccrocha@hotmail.com, 7
tatispierre@puc-rio.br,
8 pauletsbj@gmail.com, 9 gemmlagos@gmail.com
Editor: Mandar Paingankar, Government Science College, Gadchiroli,
India. Date of publication:
26 August 2020 (online & print)
Citation: Hauser-Davis, R.A., M.L.V. Barbosa-Filho, L.H.S. de.
S. Pereira, C.A. Lopes, S.C. Moreira, R.C.C. Rocha, T.D.S. Pierre, P. Baldassin & S. Siciliano (2020). First record of a morphologically abnormal and highly
metal-contaminated Spotback Skate Atlantoraja
castelnaui (Rajiformes:
Arhynchobatidae) from southeastern Rio de Janeiro,
Brazil. Journal of Threatened Taxa 12(11): 16510–16520. https://doi.org/10.11609/jott.5903.12.11.16510-16520
Copyright: © Hauser-Davis et al. 2020. Creative Commons Attribution 4.0 International
License. JoTT
allows unrestricted use, reproduction, and distribution of this article in any
medium by providing adequate credit to the author(s) and the source of
publication.
Funding: TDSP and SS acknowledge CNPq productivity grants. This is a Programa Fiocruz de Fomento à Inovação (INOVA): Elasmobrânquios como ferramentas bioindicadoras de contaminação por metais no Sudeste Brasileiro: Impactos na saúde pública e no contexto socioambiental de populações vulneráveis locais (VPPIS-004-FIO-18) contribution. INOVA supports LHSSP, RAHD and SS. RAHD would also like to acknowledge support from FAPERJ (Carlos Chagas Filho Foundation for Supporting Research in the State of Rio de Janeiro).
Ethics statement: Elasmobranch
sampling is permitted under SISBIO license 70078-1. All samples were bought from local artisanal
fishers and no animals required sacrifice.
Competing interests: The authors declare no competing interests.
Author details: Rachel Ann
Hauser-Davis: Biologist, holds a public health
researcher position at Fiocruz, Rio de Janeiro,
Brazil. Primary research interests include Ecotoxicology, Environmental
Chemistry and Science Education. Expertise focusing on subcellular metal
compartmentalization and detoxification and Ecotoxicology applied to
Biodiversity conservation. She also works alongside artisanal fishers carrying
out baseline fisheries contamination assessments. Márcio L. V.
Barbosa-Filho: Biologist, Master in Zoology and PhD in
Ethnobiology and Nature Conservation. Applies Biological Sciences and Social
Sciences methodologies focusing on the conservation of artisanal fishing
culture and exploited fishing resources. Acts as an environmental consultant in
wild fauna rescue and also carries out socio-environmental education alongside
indigenous and other traditional communities.
Lucia Helena S. de S. Pereira:
Biologist, focusing on Ecotoxicology applied to Biodiversity conservation
efforts. Is currently studying entrepreneurships actions at the Pontifical
Catholic University of Rio de Janeiro, in order to sharpen her skills in
applying multidisciplinary methodologies to scientific research. Catarina Amorim-Lopes: Biologist,
currently a master’s candidate at the UERJ Ecology and Evolution Postgraduate
Program. Is a member of the American Elasmobranch Society. Develops studies on
negative metal contamination effects on shark health off the coast of Rio de
Janeiro. Sergio
C. Moreira: Biologist with a Master’s in Animal Biology. Member of the
Latin American Society of Aquatic Mammals. Associate researcher at the
Laboratory of Bioacoustics and Cetacean Ecology. Has executive and financial
management experience in third sector activities. Expert in bioacoustics, aquatic
mammal conservation, marine sound and impact assessments and environmental
licensing. Rafael C. C. Rocha: Chemist, currently a master’s candidate at the Analytical
Chemistry Postgraduate Program at PUC-Rio. Has experience in Analytical
Chemistry (Sample Preparation, ICP-MS, HPLC) and Bioanalytical Techniques
(HPLC-ICP-MS, LA-ICP-MS). Performs the development and validation of analytical
methods and performs metallomic analyses in
environmental and clinical contexts. Tatiana
D. Saint’Pierre: Holds a master’s and PhD
degree in Analytical Chemistry. Is currently a Professor at PUC-Rio and
develops research in atomic spectrometry, with emphasis on trace element
analyses in petroleum fuels and biofuel and environmental samples. Holds a CNPq Level 2 productivity fellowship and FAPERJ Cientista do Nosso Estado
fellowship. Paula Baldassin: Veterinarian with
a PhD in Chemical Oceanography. Is experienced in environmental conservation
actions and aquatic fauna rescue and rehabilitation. Performs research on
environmental contaminants and sanitary qualities. Is currently the
socio-environmental director at iGUi Ecologia, partner at BW Consultoria
Veterinária, and a veterinary medicine consultant for
several agencies and companies. Salvatore Siciliano:
Head researcher at the Oswaldo Cruz Institute/Fiocruz
Biodiversity Laboratory. Coordinates the Lagos Region Marine Mammals Study
Group (GEMM-Lagos). Experienced in zoology, natural resource conservation and
ethnozoology. Member of the International Whaling Commission Scientific
Committee. Founder and editor of the Latin American Journal of Aquatic Mammals.
Holds a CNPq Productivity fellowship.
Author contribution: Rachel Ann Hauser-Davis:
Conceptualization, Resources, Investigation, Validation, Data Curation, Formal
analysis; Project administration, Supervision, Writing - Original Draft,
Writing – Draft reviewing; Márcio L. V.
Barbosa-Filho: Data Curation, Visualization, Investigation, Formal analysis,
Writing - Original Draft; Lucia Helena S. de S. Pereira: Validation,
Visualization, Investigation, Formal analysis; Catarina Amorim-Lopes: Data
Curation, Visualization, Investigation, Formal analysis; Sérgio
C. Moreira: Validation, Data Curation, Visualization, Investigation, Formal
analysis; Rafael C. C. Rocha: Validation, Data Curation, Formal analysis;
Tatiana D. Saint’Pierre: Validation, Resources,
Funding acquisition, Supervision, Writing - Original Draft; Paula Baldassin: Validation, Visualization, Investigation, Formal
analysis, Writing - Original Draft; Salvatore Siciliano:
Conceptualization, Resources, Funding acquisition, Project administration,
Supervision, Writing - Original Draft, Writing – Draft reviewing.
Acknowledgements: The authors would like to thank
Dr. Johnny Jensen for his extreme patience and dedication in taking the
radiographic images.
Abstract: This paper reports the first
record of a morphologically abnormal and highly metal-contaminated Spotback Skate Atlantoraja
castelnaui (Ribeiro, 1907) (Elasmobranchii,
Rajidae) in Rio de Janeiro, Brazil.
Incomplete fusion of the right
pectoral fin with the head was
observed, while a radiography indicated muscle sheaf discontinuity
near the rostrum. Extremely high contamination by several elements,
including teratogenic As,
Hg and Cd in the individual was detected. The observed morphological deformity may be
due to high concentrations of teratogenic elements in the environment, possibly playing a role in
abnormal embryonic development
in egg cases exposed to high environmental concentrations of these contaminants. Atlantoraja
castelnaui is the least biologically
understood member of the genus Atlantoraja,
and this paper furthers both morphological observations and ecotoxicological assessments on this species.
Keywords: Altered embryonic development, Arhynchobatidae, food safety, metal contamination,
morphological abnormality,
Introduction
The Spotback
Skate Atlantoraja castelnaui
(Ribeiro,
1907), Arhynchobatidae, is endemic to the
southwestern Atlantic Ocean, between Rio de Janeiro, Brazil, and northern
Argentina (Hozbor et al. 2004; Figueiredo
& Menezes 2015). A. castelnaui can reach 1.5m and occurs between 10 and 500
meters in depth, with benthic habits, oviparous reproduction mode and feeds on
teleost fish, cephalopods, decapods and other elasmobranchs (Moreira et al.
2011; Barbini & Lucifora
2012; Figueiredo & Menezes 2015). It is especially vulnerable to trawl
fisheries due to its benthonic habits (Ebert & Sulikowski
2009). In addition, owing to its large
size, this taxon achieves high commercial values and trawl experiences along
the coast of Uruguay and Argentina have indicated a 75% drop in biomass between
1994 and 1999 (Hozbor et al. 2004). As such, many populations are overexploited
throughout their distribution, A. castelnaui
is listed as “Endangered” by the IUCN and currently undergoing decreasing
population trend (Hozbor et al. 2004). In fact, the
vulnerability of large skates and rays to overexploitation and, consequently,
stock depletion, is well documented (Dulvy &
Reynolds 2002). Given this scenario,
alongside the fact that this species is the least biologically understood
member of the Atlantoraja genus
(Moreira et al. 2011), information on the basic biology of A. castelnaui is required to support fisheries
management and conservation actions (Ribeiro-Prado et al. 2008).
The
most common morphological abnormality in skates (order Rajiformes)
is the non-fusion of the pectoral fins to the head or rostrum (Mejía-Falla et al. 2011) (Figure 1), and some studies have
reported such abnormalities for the Arhynchobatidae
family (Casarini et al. 1996; Ribeiro-Prado et al.
2008).
In order to contribute towards
biological knowledge on A. castelnaui, the aim
of this study was to describe a morphological abnormality in a very young
specimen captured in southeastern Brazil, where no conservation measures are in
place for this species (Hozbor et al. 2004), through
morphometric measurements, radiography and chemical analyses.
Material
and Methods
An abnormal and very young male A.
castelnaui specimen was collected during regular
field studies of elasmobranchs caught by artisanal fishing gillnets at Tamoios, Cabo Frio, southeastern Brazil (Image 1) on 12 October 2019.
The ray specimen is deposited at
the Fish, Chelonian, Seabird, and Marine Mammal Tissue Collection, at
the Instituto Oswaldo Cruz, Fiocruz, under
identification code CTPQAMM #01-2019. At
the laboratory, the following morphometric measurements were taken: total
length (TotL); disk length (DL); disk width (DW);
total weight (TW); tail length (TailL). Bilaterally symmetric structures were also
measured on the right and left sides, as follows: gill length (GL); eye height
(EH); eye diameter (ED), spiracle height (SH); spiracle diameter (SD); pelvic
fin length (PFL); pectoral fin length (PectFL). All
measurements were taken to the nearest mm using a caliper.
The abnormal specimen was
then submitted to a radiography for further abnormality assessments.
A ventral muscle sample was
removed with the aid of a stainless-steel scissors and metals, metalloids and
rare earth elements were determined by inductively coupled plasma mass
spectrometry (ICP-MS). Briefly,
approximately 150mg of the sample were placed in a 15mL screw-capped
polypropylene tube and mixed with concentrated sub-boiled bidistilled
nitric acid (Merck, Rio de Janeiro).
This mixture was then left to stand overnight at room temperature in the
closed tube. After 12 hours, the acid
decomposition was completed by heating the sample at 100°C, for 4h in the
closed vessel, avoiding volatilization of volatile elements, such as Hg and
Se. The sample was then diluted with
ultra-pure water (resistivity > 18.0 MΩ cm) obtained from a Merck Millipore
purifying system (Darmstadt, Germany) to 10mL.
Metals, metalloids and rare earth elements were determined, in
quintuplicate, using multi-elemental external calibration, by appropriate
dilutions of a mixed standard solution (Merck IV) and using 102Rh as
the internal standard at 20 mg L-1.
The determinations were conducted on a NexIon
300 Perkin Elmer ICP-MS (Norwalk, CT, USA).
Method accuracy was verified with procedural blanks and by the parallel
analysis of the certified reference material (CRM) ERM®- BB422 (fish
muscle) in triplicate. All CRM recovery
values were within acceptable Eurachem standards (Eurachem 1998).
Results
The A. castelnaui
abnormality consisted of the incomplete fusion of the right pectoral fin with
the head, resulting in cleft between the pectoral fin and the rostrum (Image
2). No anophthalmia was observed.
The morphometric measurements of
the A. castelnaui specimen are
displayed in Table 1.
Bilaterally symmetric structures
were also measured, in order to assess possible variations, displayed in Table
2.
The radiography image of the
specimen is displayed in Image 3. Muscle
sheaf discontinuity is noted near the rostrum, while a very discrete
radio-opacity, possibly indicative of arthrosis, is also observed.
The metal, metalloid and rare
earth element concentrations detected in the muscle tissue sample are displayed
in Table 3.
The metals Bi, Cd, In, Nb and Re were all below their respective LQ of 0.024,
0.035, 0.008, 0.029 and 0.0005 mg kg-1 wet weight, while the rare
Earth elements Nd, Pr and Th were below their LQ of
0.0001, 0.0003 and 0.014 mg kg-1 wet weight, respectively.
Discussion
It appears that pectoral fins
non-adherent to the head are the most frequently recorded abnormality in Rajidae species worldwide (Ribeiro-Prado et al. 2008),
where the pectoral fin fails to fuse together at the front of the head during
early development stages (Ahlstrom & Bigelow 1963). Records of such
abnormalities are available for Atlantoraja cyclophora, A. platina, Raja asterias, R. brachyura,
R. clavate, R. miraletus,
R. radiata, R. radula, R. richardsoni, Rioraja agassizi and Rostroraja alba (see
Ribeiro-Prado et al. 2008 for more details).
For A. castelnaui, a
previous record of incomplete pectoral fin fusion is noted for the state of São
Paulo, also located in southeastern Brazil, in one
sub-adult specimen (total length and disk width of 87.5cm and 61cm,
respectively), albeit for the left pectoral fin (Ribeiro-Prado et al. 2008).
Fluctuating asymmetry, defined as
random deviations from perfect bilateral symmetry due to developmental
disturbances during early life, is a valuable tool to quantify stress during
early developmental stage (Jagoe & Haines
1985). In the present study, most
right-side structures were slightly smaller compared to the left-side
structures, with the exception of the 1st gill arch (same size), eye
diameter (larger), spiraculum height (higher) and
pelvic fin width (larger). Although the
sample size is of only one individual, the observed differences in bilaterally
symmetric structure may be indicative of developmental disturbances, and future
studies in the study area should also carry out this analysis in order to build
a fluctuating asymmetry database for this and other species.
It has been postulated that unfavorable environmental conditions, such as high
pollutant loads, probably play a role in occurrence of abnormalities (Casarini et al. 1996; Ribeiro-Prado et al. 2008),
especially during early developmental fish stages, which are considered
particularly sensitive to water pollution toxicity (Osman et al. 2007; Jezierska et al. 2009; Zhang et al. 2012). In vitro exposure to metals, in
particular, has been proven as responsible for increasing the frequency of
several types of body malformations of fish embryos (Cheng et al. 2000; Flik et al. 2002; González-Doncel
et al. 2003; Hallare et al. 2005; Jezierska
et al. 2009), confirming the teratogenic and genotoxic properties of metals in
fish. In addition, several field studies
have also been carried out and have associated the genotoxic potential of these
compounds to morphological abnormalities in fish (Ferrante et al. 2017; Braga
et al. 2019). This shall be further
discussed ahead.
This hypothesis was assessed by a
screening of metals, metalloids and rare earth elements in the muscle tissue of
this individual prior to fixation in alcohol.
The specimen assessed herein was
a very young individual. A. castelnaui juveniles and females have been reported
as inhabiting more coastal areas in Brazil (Oddone et
al. 2008). This leads to high exposure
to environmental contamination from anthropogenic activities in these
individuals. In addition, A. castelnaui feeds mainly on bony fish, followed by
decapods, elasmobranchs, mollusks, and
cephalochordates, with crustaceans present in this species diet in greater
amounts in smaller individuals, while cephalopods, elasmobranchs, and
echinoderms predominate in higher class sizes (Barbini
& Lucifora 2012).
Therefore, this skate is at high risk for the bioaccumulation of several
contaminants, including metals, through the dietary route.
Morphological deformities in
several fish species have been related to water quality and contamination,
including metal concentrations (Hiraoka & Okuda
1983; Sun et al. 2009; Alavi-Yeganeh et al.
2019). For example, altered spinal
curvatures in Rainbow Trout Oncorhynchus mykiss larvae hatched from
Cd-incubated eggs has been reported (Woodworth & Pascoe 1982), as well as
spinal and cranial malformations and jaw underdevelopment in common carp larvae
exposed to Cu during embryonic development (Stouthart
et al. 1995). Other assessments have
verified various types of vertebral deformities and two-headed morphological
abnormalities in Cu- and Zn-exposed White Sucker Catostomus
commersoni larvae (Munkittrick
& Dixon 1989), skeletal kinking, improperly formed mouth, head and eyes and
reduced brain size, among others, in Zn-exposed Fatthead
Minnow Pimephales promelas
embryos (Dawson et al. 1988), eye and optic capsules malformations and jaw and
branchial arch deformities in Zn-exposed Atlantic Herring Clupea
harengus eggs who hatched into larvae
(Somasundaram et al. 1984), and several spinal cord deformations in Cu-exposed
common carp embryos (Flik et al. 2002). In addition, Zebrafish Danio rerio, widely applied as a model bioindicator species
concerning metal effects, assessments concerning Cd exposure in embryos have
reported several morphological alterations, such as head and eye hypoplasia,
altered axial curvature and tail malformations (Cheng et al. 2000), helical
bodies, hooked tails, tail degeneration and abnormal body posture (Hallare et al. 2005), and severe stunting, ocular
deformities (microphthalmia, anisophthalmia and
anophthalmia) and dystrophic jaws (synarthrosis) (González-Doncel
et al. 2003).
Besides in vitro assessments,
real environmental scenarios have also indicated that metals are most likely
causative of morphological abnormalities in fish. For example, spinal deformities in natural
Grass Goby Zosterisessor ophiocephalus populations from the Gulf of Gabès in Tunisia have been associated to metal (Cd, Cu and
Zn) accumulation, as higher frequencies of deformities were observed in
metal-contaminated areas compared to non-contaminated areas (Messaoudi et al. 2009); a high frequency of vertebral
deformities in Fourhorn Sculpin Myoxocephalus
quadricornis exposed to heavy metal pollution in
the Gulf of Bothnia (Baltic Sea) has been verified (Bengtsson & Lithner 1988), and higher frequencies of skeletal anomalies
(deformed fins, the lack of one or more fins and pelvic girdle, pugheadedness, asymmetric cranium, shortened operculae, fused and deformed vertebrae and spinal
curvatures) were observed in Bream Abramis brama sampled from a polluted area (River Rhine)
compared to a control area (Lake Braassem) (Slooff 1982). In
addition, one assessment carried out on Mediterranean Killifish, Alphanius fasciatus,
from different unpolluted and polluted areas off the coast of Tunisia reported
deformed specimens only from the polluted sampling areas, presenting higher Cd
concentrations in their livers and spinal columns when compared to normal
specimens, also indicating significantly higher Cd bioaccumulation factors in
the former (Kessabi et al. 2009). In another study carried out by the same
group also associated skeletal deformities in the vertebral column of
Mediterranean Killifish from the Tunisian coast to high concentration of heavy
metals (Cd, Cu and Zn) (Kessabi et al. 2013). In another study, many different skeletal
deformities in the vertebral column, cranium, operculum, fins and jaws of
tilapia (Oreochromis spp.) sampled from different rivers in Taiwan were
correlated to Hg, Zn, Pb, Cu and Cr concentrations
(Sun et al. 2009).
In addition, some assessments
have evaluated genotoxicity effects of several metals comparing polluted and
non-polluted sites and associated this with morphological abnormalities in
fish. For example, an assessment carried
out concerning the ichthyofauna from polluted and non-polluted/protected
estuaries located on the São Paulo coast, Brazil,
reported several genotoxic alterations (nuclear abnormalities in erythrocytes)
in two teleosts, Centropomus
paralelus and Diapterus
rhomneus due to high Zn, Co, Cr, and As
concentrations (Braga et al. 2019), while another assessment observed a clear
and significant correlation between two genotoxic biomarkers of effect
(micronuclei and nuclear abnormalities) and Cd, Cr, Hg and Pb,
as well as to an overall degree of metal pollution index, in a benthic teleost
species, the Rusty Blenny Parablennius sanguinolentus (Ferrante et al. 2017).
These assessments, however, have
all been carried out in teleosts, and studies in this
regard for elasmobranchs are severely lacking.
To the best of our knowledge, no assessments in this regard are
available in the literature concerning this group, indicating a significant
knowledge gap that must be bridged.
Furthermore, morphological
abnormalities are more frequently observed in oviparous species compared to
viviparous species (Ribeiro-Prado et al. 2008), as embryos developed in egg
cases maintain direct contact with environmental conditions, including
contaminants, while embryos that develop inside the womb are protected from
external influence up to a certain extent.
Feeding solely only on yolk, as A. castelnaui
embryos do (Dulvy & Reynolds 1997), produced
through lipid mobilization from the mother’s liver during vitellogenesis
(Rossouw 1987), also allows for high maternal transfer of several contaminants,
including metals.
Regarding the contaminant
concentrations observed herein, almost no studies regarding rare Earth elements
(REE) in elasmobranchs are
available. This group of elements,
comprising scandium, yttrium, lanthanum and the 14 chemical elements following
lanthanum, termed lanthanoids (Redling 2006),
consists of non-essential elements for living systems and have been reported as
presenting low to moderate toxicity, including substitution of bone calcium by
certain REE, due to their same oxidation state, carcinogenic properties (Rim et
al. 2013) and the ability to result in cytotoxicity and genetic damage through
oxidative stress (Huang et al. 2011; Jha & Singh 1995). In addition, long-term REE intake has been
postulated as resulting in chronic poisoning (Hirano & Suzuki 1996). The sum of the Rare Earth Elements (ΣREE)
detected herein did not reach the only maximum permissible concentration
available worldwide, of 0.7 mg kg-1 (China 2005), although this has
been established only for animal feeds and no other limits are available for
other matrices. REE are found in the geological composition of sediments (Hu et
al. 2006; Laveuf & Cornu
2009) and, as A. castelnaui is a benthic
species, it may ingest sediment during feeding, accounting for the levels
detected in muscle tissue. Higher REE
concentrations have, in fact, been previously reported as being higher in
benthic species (Guo et al. 2003; Mayfield & Fairbrother 2015), suggesting
that they experience higher REE exposure due to their feeding habits, as REEs
in aquatic environments are preferentially adsorbed to sediments and to fine
suspended sediment particulates compared to the dissolved water column phase
(Yang et al. 1999; Moermond et al. 2001; Taylor et
al. 2012).
Although certain essential
elements, such as Cu, Fe, Mn, Se and Zn, when present in high amounts can also
lead to negative biota and consumer effects, three of the most noteworthy
environmental contaminants, As, Hg and Pb were
observed at extremely high concentrations in the evaluated specimen. Thus, we
shall focus on these elements, as they are known carcinogenic and teratogenic
compounds.
Arsenic, a dangerous teratogen
(Eisler 1988a) at almost 62mg kg-1 w.w.,
was astonishingly high. This element, however, is usually present in its
non-toxic form arsenobetaine, which comprises over
90% of total As, in fish (Gao et al. 2018; Ruelas-Inzunza
et al. 2018). This demonstrates the need
to carry out arsenic speciation analyses, in order to quantify both the toxic
inorganic fractions and nontoxic organic fractions in fish. Nevertheless, even when taking this
percentage into account, about 6mg kg-1 w.w.
would still be present in the toxic inorganic form, over the threshold for
adverse aquatic organism effects reported as ranging from 1.3 to 5 mg kg-1
w.w. (Eisler 1988a).
Arsenic exposure has been directly associated to skeletal abnormalities
in fish. In one study, adult Mummichog Fundulus heteroclitus
were exposed to 230mg kg-1 of arsenic, an environmentally
relevant in drinking water and aquatic environments in several areas worldwide,
resulting in an average arsenic body burden of 74.6μg kg-1 (one
order of magnitude lower than the observed value of 6mg kg-1 in
toxic form calculated herein, albeit for muscle only) for 10 days immediately
prior to spawning, and the hatchlings of exposed fish presented significantly
increased incidence of curved or stunted tails (Gonzalez et al. 2006). In addition, this is also six-fold higher the
maximum amount stipulated by the Brazilian ANVISA and the Codex Alimentarius
(1.0 and 0.5 mg kg-1 w.w., respectively),
indicating significant consumer health risks for humans who consume this
species (Codex Alimentarius Commission 2009; ANVISA 2013).
Concerning Hg, a potent
neurotoxin, concentrations as low as 0.008mg kg-1 w.w. in muscle have been reported as enough to alter
biochemistry and gene expression, while the threshold for negative
reproductive, histological and growth effects is of about 0.135mg kg-1
w.w. in muscle (Sandheinrich
& Wiener 2011). Morphological
abnormalities have been previously reported in Hg-exposed fish. For example, one study assessed Hg-exposed
Mummichog Fundulus heteroclitus
and reported various eye vesicle malformations, ranging from partially fused
eyes with two separate lenses to cyclopia and severe gross malformation of the
craniofacial, cardiovascular and skeletal systems (Weis & Weis 1977),
indicating the direct effect of this element on embryo development. Therefore, the concentration observed herein
indicates significant biota health effects, as well as potential consumer
risks, since the maximum amount stipulated by the Brazilian ANVISA and the
Codex Alimentarius for total mercury amounts in fish is of 0.5mg kg-1
(Codex Alimentarius Commission 2009; ANVISA 2013), almost the same as the
0.487mg kg-1 detected in the present study.
Regarding Pb,
there is no safe threshold for exposure to this carcinogen and neurotoxin for
any organism (ATSDR 2017). Dietary
levels as low as 0.1 to 0.5 mg kg-1 have been linked to learning
deficits in vertebrates (Eisler 1988b), and Pb
effects range from neurotoxic and immunological to physiological and behavioral (ATSDR 2017).
Pb exposure in fish has also been directly
linked to diverse embryonic organogenesis malformations. For example, one study carried out in Pb-treated Common Carp Cyprinus
carpio reported craniofacial anomalies, yolk sac
malformation, vertebral shortening and curvatures and cardiac malformations (Jezierska et al. 2009), while another verified scoliosis in
Pb-exposed brook trout (Salvelinus
fontinalis) eggs who hatched into larvae
(Holcombe et al. 1976). Regarding human
consumption, the FAO/WHO permissible level for Pb of
0.3 mg kg-1 (Codex Alimentarius Commission 2009) was exceeded almost
100 times in the present study, indicate severe human consumption risks for
this toxic element.
On a side note, Ti, although not considered a classic environmental
contaminant, has emerged in recent decades as a contaminant of increasing
concern in the form of t itanium dioxide nanoparticles applied to many personal care
products. These compounds have been
reported as eliciting deleterious effects in marine trophic webs, although
scarce data is available for either Ti or its nanoparticle
forms in the marine environment (Frenzilli et al.
2014). In the present study, it is
noteworthy that Ti concentrations were an order of
magnitude higher than observed in marine mammal muscle, liver, and kidneys (Holsbeek et al. 1998, 1999), which are long-lived animals
highly exposed to metals through the dietary route and expected to
bioaccumulate more contaminants than a very young skate. Thus, Ti
contamination is probable, and should be further assessed in future studies.
Other assessments concerning
pollutant concentrations for elasmobranchs carried out in only one specimen are
available in the literature. For
example, one study assessed metals, persistent organic pollutants and polonium
in the muscle and liver of a rare filter-feeding shark specimen, the Megamouth Megachasma pelagios,
found stranded on the central-north coast of the Rio de Janeiro, Southeastern Brazil (de Moura et al. 2015), while another
assessment was carried out in one shortfin Mako Shark Isurus
oxyrinchus specimen and one Big-eye Thresher Alopias superciliosus
specimen, also from Brazilian waters, concerning persistent organic pollutant
concentrations in muscle (Azevedo-Silva et al. 2009), although the studies did
not aim to verify the causes of morphological abnormalities. Another report verified metal concentrations
in the liver of one specimen from three marine mammal species (one Orca, one
Pygmy Killer Whale and one Franciscana Dolphin) (Lemos et al. 2013).
Thus, even though discussion with the literature is hampered, reports
concerning only one specimen of threatened species are also important to create
baseline data for threatened species.
Conclusions
Atlantoraja castelnaui
is an
endangered species displaying a current decreasing population trend and
especially vulnerable to trawl fisheries due to its benthonic habits. In
addition, no conservation measures are in place for this species in
Brazil. This study is the first record
of a specimen displaying incomplete pectoral fin fusion with the head in Rio de
Janeiro, southeastern Brazil. A radiography indicated disordered muscle sheafs near the rostrum, while a metal, metalloid and
rare-earth screening indicated extremely high contamination by teratogenic
elements such as As, Hg, and Cd. The observed morphological deformity may in
fact be due to the high concentrations of these elements in the Cabo Frio environment, also indicating high environmental
contamination and significant human health risk concerns for populations who
consume this species regularly in southeastern
Brazil. It should be noted that this
coastal environment undergoes under a strong influence of the so-called Cabo Frio upwelling system, an oceanographic anomaly that
significantly enriches these waters, yielding locally higher fish catches. This paper furthers both morphological
observations and ecotoxicological assessments on this relatively biologically
unknown species in Brazil, paramount for future conservation measures. Although only one specimen was assessed
herein, environmental contamination cannot be discarded as a possible cause for
the observed deformity, and the extremely high contaminant levels observed
indicate the need for further assessments for the species, both with regard to
deleterious effects on the species itself and in a public health context.
Table 1. Morphometric body
measurements of a very young A. castelnaui specimen
from Cabo Frio, Rio de Janeiro, southeastern
Brazil.
Morphometric body measurements |
|
Total length (cm) |
34.50 |
Total weight (g) |
115.00 |
Disk length (cm) |
15.00 |
Disk width (cm) |
20.90 |
Tail length (cm) |
16.50 |
Table 2. Bilaterally symmetric
structure measurements of the assessed A. castelnaui
specimen from Cabo Frio, Rio de Janeiro, southeastern Brazil.
Measurement |
Right |
Left |
Length of the 1st
gill arch |
3.80 |
3.80 |
Length of the 2nd
gill arch |
2.90 |
3.30 |
Length of the 3rd
gill arch |
3.20 |
3.36 |
Length of the 4th
gill arch |
3.00 |
3.30 |
Gill arch length means |
2.20 |
2.40 |
Eye diameter |
6.37 |
6.00 |
Eye height |
10.03 |
10.53 |
Spiraculum diameter |
4.66 |
6.13 |
Spiraculum height |
4.43 |
4.06 |
Pectoral fin width |
105.6 |
106.83 |
Pelvic fin width |
40.80 |
38.66 |
Table 3. Metal, metalloid and rare earth element
concentrations (mg kg-1 wet weight) in the muscle of the assessed A.
castelnaui specimen from Cabo Frio,
Rio de Janeiro, Southeastern Brazil. LQ – Limit of
Quantification (mg kg-1 wet weight), defined as the lower limit that
elements can be accurately quantified.
Metals and metalloids |
|||||
Element |
LQ |
Sample |
Element |
LQ |
Sample |
Ag |
0.003 |
0.178 |
Pb |
0.010 |
2.288 |
Al |
0.101 |
82.74 |
Pd |
0.003 |
0.113 |
As |
0.015 |
61.64 |
Rb |
0.002 |
4.626 |
Au |
0.001 |
0.006 |
Sb |
0.002 |
0.052 |
Ba |
0.014 |
2.442 |
Sc |
0.087 |
0.82 |
Br |
1.022 |
265.55 |
Se |
0.428 |
7.951 |
Co |
0.002 |
0.17 |
Sn |
0.007 |
0.149 |
Cr |
0.034 |
13.59 |
Sr |
0.018 |
635.162 |
Cs |
0.001 |
0.098 |
Ta |
0.003 |
0.007 |
Cu |
0.018 |
5.45 |
Ti |
0.163 |
39.40 |
Fe |
2.642 |
378.24 |
Tl |
0.001 |
0.002 |
Ga |
0.002 |
0.12 |
U |
0.006 |
0.022 |
Ge |
0.020 |
0.12 |
V |
0.006 |
3.39 |
Hg |
0.009 |
0.487 |
W |
0.019 |
0.046 |
Mn |
0.022 |
8.17 |
Y |
0.001 |
0.352 |
Mo |
0.009 |
0.197 |
Zn |
0.206 |
256.37 |
Ni |
0.010 |
4.19 |
Zr |
0.014 |
0.076 |
Rare earth elements |
|||||
Element |
LQ |
Sample |
Element |
LQ |
Sample |
Ce |
0.004 |
0.176 |
La |
0.001 |
0.085 |
Dy |
0.001 |
0.012 |
Lu |
0.001 |
0.001 |
Er |
0.000 |
0.007 |
Sm |
0.001 |
0.015 |
Eu |
0.001 |
0.032 |
Tb |
0.000 |
0.001 |
Gd |
0.001 |
0.028 |
Tm |
0.000 |
0.001 |
Ho |
0.000 |
0.001 |
Yb |
0.001 |
0.005 |
For
figure & images – click here
References
Ahlstrom,
E.H. & Bigelow, H.B. (1963). Fishes of the Western North
Atlantic. Part Four. Soft-Rayed Bony Fishes: Orders Isospondyli
and Giganturoidei: Argentinoids,
Stomiatoids, Pickerels, Bathylaconids,
Giganturids. Yale, 599pp.
Alavi-Yeganeh, M.S, S. Razavi
& J.P. Egan (2019). Taillessness and skeletal deformity in
striped piggy Pomadasys stridens
(Osteichthyes: Haemulidae) from the Persian Gulf. Diseases
of Aquatic Organisms 132: 209–213. https://doi.org/10.3354/dao03322
ANVISA
(2013). RESOLUÇÃO
- RDC N- 42, DE 29 DE AGOSTO DE 2013. Available at:
http://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2013/rdc0042_29_08_2013.html
ATSDR (2017). Lead Toxicity: What Are Possible
Health Effects from Lead Exposure? Available at: https://www.atsdr.cdc.gov/csem/csem.asp?csem=34&po=10
Azevedo-Silva,
C.E., A. Azeredo, A.C.L. Dias, P. Costa, J. Lailson-Brito, O. Malm, J.R.D. Guimarães & J.P.M Torres (2009). Organochlorine compounds in
sharks from the Brazilian coast. Marine Pollution Bulletin 58:
294–298. https://doi.org/0.1016/j.marpolbul.2008.11.003
Barbini, S.A. & L.O. Lucifora (2012). Feeding habits of a large
endangered skate from the south-west Atlantic: The spotback
skate, Atlantoraja castelnaui.
Marine and Freshwater Research 63: 180–188. https://doi.org/10.1071/MF11170
Bengtsson,
B.E. & G. Lithner (1988). Vertebral defects in fourhorn sculpin, Myoxocephalus
quadricornis L., exposed to heavy metal pollution
in the Gulf of Bothnia. Journal of Fish Biology 33: 517–529. https://doi.org/10.1111/j.1095-8649.1988.tb05496.x
Braga, E.S.,
J.S. Azevedo, L. Kuniyoshi & D.I.T. Fávaro (2019). Zn, Co, Cr, As, and genotoxic effects in the
ichthyofauna species from polluted and non-polluted/protected estuaries of the
São Paulo Coast, Brazil. Anais da Academia Brasileira
de Ciências 91: e20190066. https://doi.org/10.1590/0001-3765201920190066
Casarini, L.M., U.L. Gomes & O.B.G.
Tomas (1996). Would be
Santos harbour dredged material dumping a reason of teratogeny on Raja agassizi?.
In: Abstracts of the VII Congresso Latino-Americano sobre Ciências do Mar Caderno de Resumos 7: 152–153.
(SBEEL: Santos, Brazil.)
Cheng, S.H.,
A.W.K. Wai, C.H. So & R.S.S. Wu (2000). Cellular and molecular basis of
cadmium-induced deformities in zebrafish embryos. Environmental Toxicology
and Chemistry 19: 3024–3031. https://doi.org/10.1002/etc.5620191223
China (2005). GB2762-2005 - National Food
Safety Standard Maximum Levels of Contaminants in Food. Available at:
https://apps.fas.usda.gov/newgainapi/api/report/downloadreportbyfilename?filename=Maximum%20Levels%20of%20Contaminants%20in%20Foods%20_Beijing_China%20-%20Peoples%20Republic%20of_12-11-2014.pdf
Codex
Alimentarius Commission (2009). Report of the 32nd session of the Codex
Committee on Nutrition and Foods for Special Dietary Uses (ALINORM 09/32/REP).
Available at: https://www.usda.gov/codex
Dawson, D.A.,
E.F. Stebler, S.L. Burks & J.A. Bantle (1988). Evaluation of the developmental toxicity of
metal-contaminated sediments using short-term fathead minnow and frog
embryo-larval assays. Environmental Toxicology and Chemistry 7: 27–34.
de Moura,
J.F., A. Merico, R.C. Montone, J. Silva, T.G. Seixas, J.M. Godoy, T.D. Saint’Pierre,
R.A. Hauser-Davis, A.P.M. Di Beneditto, E.C. Reis,
D.V. Tavares, L.S. Lemos & S. Siciliano
(2015). Assessment of
trace elements, POPs, 210Po and stable isotopes (15N and 13C)
in a rare filter-feeding shark: The megamouth. Marine Pollution Bulletin
95: 402–406. https://doi.org/10.1016/j.marpolbul.2015.03.038
Dulvy, N.K. & J.D. Reynolds
(1997). Evolutionary
transitions among egg-laying, live-bearing and maternal inputs in sharks and
rays. Proceedings of the Royal Society B: Biological Sciences 264:
1309–1315. https://doi.org/10.1098/rspb.1997.0181
Dulvy, N.K. & J.D. Reynolds
(2002). Predicting
extinction vulnerability in skates. Conservation Biology 16: 440–450. https://doi.org/10.1046/j.1523-1739.2002.00416.x
Ebert, D.A.
& J. Sulikowski (2009). Biology of Skates. In: Noakes, D.L.G. (series ed.) Developments
in Environmental Biology of Fishes. Springer-Verlag, Heidelberg, 244pp.
Eisler, R.
(1988a). Contaminant
Hazard Reviews Arsenic Hazards to Fish, Wildlife, and Invertabrates:
A Synoptic Review. Contaminant Hazard Reviews, U.S. Department of the Interior,
Fish and Wildlife Service 85(1.12) 92pp.
Eisler, R.
(1988b). Lead hazards
to fish, wildlife, and invertebrates: A synoptic review. Contaminant Hazard
Reviews, U.S. Department of the Interior, Fish and Wildlife Service 85(1.14)
134pp.
Ferrante, M.,
A.M. Pappalardo, V. Ferrito,
V. Pulvirenti, C. Fruciano,
A. Grasso, S. Sciacca, C. Tigano & C. Copat (2017). Bioaccumulation of metals and biomarkers of
environmental stress in Parablennius sanguinolentus (Pallas 1814) sampled along the Italian
coast. Marine Pollution Bulletin 122: 288–296. https://doi.org/10.1016/j.marpolbul.2017.06.060
Figueiredo, J.L., N.A. Menezes (2015). Manual de peixes
marinhos do sudeste do Brasil. São Paulo: Museu de Zoologia, USP, 105pp. https://doi.org/10.5962/bhl.title.109986
Flik, G., X.J.H.X. Stouthart, F.A.T. Spanings,
R.A.C. Lock, J.C. Fenwick & S.E.W. Bonga (2002). Stress response to waterborne Cu
during early life stages of carp Cyprinus carpio. Aquatic Toxicology 56: 167–176. https://doi.org/10.1016/S0166-445X(01)00202-8
Frenzilli, G., M. Bernardeschi,
P. Guidi, V. Scarcelli, P. Lucchesi, L. Marsili, M.C. Fossi, A. Brunelli, G. Pojana, A. Marcomini & M.
Nigro (2014). Effects of in
vitro exposure to titanium dioxide on DNA integrity of Bottlenose Dolphin (Tursiops truncatus)
fibroblasts and leukocytes. Marine Environmental Research 100: 67–73. https://doi.org/10.1016/j.marenvres.2014.01.002
Gao, Y., P. Baisch, N. Mirlean, F.M.R. da
Silva Júnior, N. Van Larebeke, W. Baeyens
& M. Leermakers (2018). Arsenic speciation in fish and
shellfish from the North Sea (Southern bight) and Açu Port area (Brazil) and
health risks related to seafood consumption. Chemosphere 191: 89–96. https://doi.org/10.1016/j.chemosphere.2017.10.031
Hallare, A.V., M. Schirling,
T. Luckenbach, H.R. Köhler & R. Triebskorn (2005). Combined effects of temperature
and cadmium on developmental parameters and biomarker responses in zebrafish (Danio
rerio) embryos. Journal of Thermal Biology
30: 7–1. https://doi.org/10.1016/j.jtherbio.2004.06.002
González-Doncel, M., M. Larrea, S.
Sánchez-Fortún & D.E. Hinton (2003). Influence of water hardening of
the chorion on cadmium accumulation in Medaka (Oryzias
latipes) eggs. Chemosphere 52: 75–83. https://doi.org/10.1016/S0045-6535(03)00227-3
Gonzalez,
H.O., J.A. Roling, W.S. Baldwin & L.J. Bain
(2006). Physiological
changes and differential gene expression in Mummichogs (Fundulus
heteroclitus) exposed to arsenic. Aquatic
Toxicology 77: 43–52. https://doi.org/10.1016/j.aquatox.2005.10.014
Guo, W.D.,
M.H. Hu, Y.P. Yang, Z.B. Gong & Y.Wu (2003). Characteristics of ecological
chemistry of rare earth elements in fish from Xiamen Bay. Oceanologia
Et Limnologia Sinica 34:
241–248.
Hirano, S.
& K.T. Suzuki (1996). Exposure metabolism and toxicity of rare earths and related compounds. Environmental
Health Perspectives 104: 85–95. https://doi.org/10.1289/ehp.96104s185
Hiraoka, Y. & H. Okuda (1983). Characteristics of vertebral
abnormalities of Medaka as a water pollution indicator. Hiroshima Journal of
Medical Sciences 32: 261–266
Holcombe,
G.W., D.A. Benoit, E.N. Leonard & J.M. McKim (1976). Long-term effects of lead
exposure on three generations of brook trout (Salvelinus
fontinalis). Journal of the Fisheries Research
Board of Canada 33: 1731–1741. https://doi.org/10.1139/f76-220
Holsbeek, L., C.R. Joiris,
V. Debacker, I.B. Ali, P. Roose,
J.P. Nellissen, S. Gobert,
J.M. Bouquegneau & M. Bossicart
(1999). Heavy
metals, organochlorines and polycyclic aromatic hydrocarbons in sperm whales
stranded in the southern North Sea during the 1994/1995 winter. Marine
Pollution Bulletin 38: 304–313. https://doi.org/10.1016/S0025-326X(98)00150-7
Holsbeek, L., U. Siebert & C.R. Joiris (1998). Heavy metals in dolphins stranded on the French
Atlantic coast. Science of the Total Environment 217: 241–249. https://doi.org/10.1016/S0048-9697(98)00177-6
Hozbor, N., A. Massa & C.M. Vooren, (2004). Atlantoraja castelnaui. The IUCN Red List of Threatened
Species 2004: e.T44575A10921544.
Hu. Z., S. Haneklaus, G. Sparovek & E. Schnug (2006). Rare earth elements in soils. Communications in
Soil Science and Plant Analysis 37: 1381–1420. https://doi.org/10.1080/00103620600628680
Huang, P., J.
Li, S. Zhang, C. Chen, Y. Han, N. Liu, Y. Xiao, H. Wang, M. Zhang, Q. Yu, Y.
Liu & W. Wang (2011). Effects of lanthanum cerium and neodymium on the nuclei and
mitochondria of hepatocytes: Accumulation and oxidative damage. Environmental
Toxicology and Pharmacology 31: 25–32. https://doi.org/10.1016/j.etap.2010.09.001
Jagoe, C.H. & T.A. Haines (1985). Fluctuating asymmetry in fishes
inhabiting acidified and unacidified lakes. Canadian Journal of Zoology
63: 130–138. https://doi.org/10.1139/z85-022
Jezierska, B., K. Ługowska
& M. Witeska (2009). The effects of heavy metals on
embryonic development of fish (a review). Fish Physiology and Biochemistry
36: 625–640. https://doi.org/10.1007/s10695-008-9284-4
Jha, A.M.
& A.C. Singh (1995). Clastogenicity of lanthanides: induction of
chromosomal aberration in bone marrow cells of mice in vivo. Mutation
Research - Genetic Toxicology and Environmental Mutagenesis 341 193–197. https://doi.org/10.1016/0165-1218(95)90009-8
Kessabi, K., A. Annabi,
A.I.H. Hassine, I. Bazin,
W. Mnif, K. Said & I. Messaoudi
(2013). Possible
chemical causes of skeletal deformities in natural populations of Aphanius fasciatus
collected from the Tunisian coast. Chemosphere 90: 2683–2689. https://doi.org/10.1016/j.chemosphere.2012.11.047
Kessabi, K., A. Kerkeni,
K. Saïd & I. Messaoudi (2009). Involvement of Cd bioaccumulation
in spinal deformities occurrence in natural populations of mediterranean
killifish. Biological Trace Element Research 128: 72–81. https://doi.org/10.1007/s12011-008-8255-z
Laveuf, C. & S. Cornu
(2009). A review on
the potentiality of Rare Earth Elements to trace pedogenetic processes. Geoderma 154: 1–12. https://doi.org/10.1016/j.geoderma.2009.10.002
Lemos, S.L., J.F. de Moura, R.A.
Hauser-Davis, R.C. de Campos & S. Siciliano
(2013). Small
cetaceans found stranded or accidentally captured in southeastern Brazil:
Bioindicators of essential and non-essential trace elements in the environment.
Ecotoxicology and Environmental Safety
97:166-175. https://doi.org/10.1016/j.ecoenv.2013.07.025
Mayfield,
D.B. & A. Fairbrother (2015). Examination of rare earth element concentration
patterns in freshwater fish tissues. Chemosphere 120: 68–74. https://doi.org/10.1016/j.chemosphere.2014.06.010
Mejía-Falla, P.A., A.F. Navia
& L.A. Muñoz (2011). First record of morphological abnormality in embryos of Urotrygon rogersi
(Jordan & Starks, 1895) (Myliobatiformes: Urotrygonidae) in the Tropical Eastern Pacific. Latin
American Journal of Aquatic Research 39: 184–188. https://doi.org/10.3856/vol39-issue1-fulltext-19
Messaoudi, I., T. Deli, K. Kessabi, S. Barhoumi, A. Kerkeni & K. Saïd (2009). Association of spinal deformities
with heavy metal bioaccumulation in natural populations of grass goby Zosterisessor ophiocephalus
Pallas 1811 from the Gulf of Gabès (Tunisia). Environmental
Monitoring and Assessment 156: 551–560. https://doi.org/10.1007/s10661-008-0504-2
Moermond, C.T.A., J. Tijink,
A.P. Van Wezel & A.A. Koelmans
(2001). Distribution
speciation and bioavailability of lanthanides in the Rhine-Meuse estuary the
Netherlands. Environmental Toxicology and Chemistry 20: 1916–1926. https://doi.org/10.1002/etc.5620200909
Moreira,
R.A., U.L. Gomes & M.R. de Carvalho (2011). Morphological description of Dipturus mennii
(Chondrichthyes: Elasmobranchii: Rajidae)
and its differentiation from Dipturus trachyderma. Zoologia
28: 97–111. https://doi.org/10.1590/S1984-46702011000100014
Munkittrick, K.R. & D.G. Dixon (1989). Effects of natural exposure to
copper and zinc on egg size and larval copper tolerance in white sucker (Catostomus commersoni).
Ecotoxicology and Environmental Safety
18: 15–26. https://doi.org/10.1016/0147-6513(89)90088-2
Oddone, M.C., A.F. Amorim & P.L.
Mancini (2008). Reproductive
biology of the spotback skate, Atlantoraja
castelnaui (Ribeiro, 1907) (Chondrichthyes, Rajidae), in southeastern Brazilian waters. Revista de Biología
Marina y Oceanografía 43: 327–334.
Osman,
A.G.M., S. Wuertz, I.A. Mekkawy,
H.J. Exner & F. Kirschbaum (2007). Lead induced malformations in
embryos of the African catfish Clarias gariepinus (Burchell 1822). Environmental Toxicology
22: 375–389. https://doi.org/10.1002/tox.20272
Redling, K. (2006). Rare Earth Elements in Agriculture
with Emphasis on Animal Husbandry. DVG-Service, Munich, 326pp.
Ribeiro, A.M.
(1907). Fauna
Brasiliense. Peixes. II. Desmobranchios.
Archivos do Museu
Nacional do Rio Janeiro 14:129–212
Ribeiro-Prado,
C.C., M.C. Oddone, M.M.B. Gonzalez, A.F. Amorim &
C. Capapé (2008). Morphological abnormalities in
skates and rays (Chondrichthyes) from off southeastern Brazil. Arquivos de Ciências do
Mar 41: 21–28
Rim, K.T.,
K.H. Koo & J.S. Park (2013). Toxicological evaluations of rare earths and their
health impacts to workers: A literature review. Safety and Health at Work
4: 12–26. https://doi.org/10.5491/SHAW.2013.4.1.12
Rossouw, G.J.
(1987). Function of
the liver and hepatic lipids of the lesser sand shark, Rhinobatos
annulatus (Müller & Henle). Comparative
Biochemistry and Physiology - Part B: Biochemistry & Molecular Biology 86:
785–790. https://doi.org/10.1016/0305-0491(87)90225-2
Ruelas-Inzunza, J., Z. Šlejkovec,
D. Mazej, V. Fajon, M.
Horvat & M. Ramos-Osuna (2018). Bioaccumulation of As, Hg, and Se
in tunas Thunnus albacares
and Katsuwonus pelamis
from the Eastern Pacific: tissue distribution and As speciation. Environmental
Science and Pollution Research 25: 19499–19509. https://doi.org/10.1007/s11356-018-2166-0
Sandheinrich, M.B. & J.G. Wiener (2011). Methylmercury Freshwater Fish:
Recent Advances in Assessing Toxicity and Environmentally Relevant Exposures,
pp. 169–190. In: Beyer, W.N. & J.P. Meador (eds.). Environmental
Contaminants in Biota CRC Press/Taylor and Francis, Boca Raton, FL, 768pp.
Slooff, W. (1982). Skeletal anomalies in fish from
polluted surface waters. Aquatic Toxicology 2: 157–173. https://doi.org/10.1016/0166-445X(82)90013-3
Somasundaram,
B., P.E. King & S. Shackley (1984). The effects of zinc on postfertilization development in eggs of Clupea harengus L. Aquatic
Toxicology 5: 167–178. https://doi.org/10.1016/0166-445X(84)90007-9
Stouthart, A.J.H.X., F.A.T. Spanings, R.A.C. Lock & S.E.W. Bonga (1995). Effects of water pH on chromium
toxicity to early life stages of the common carp (Cyprinus
carpio). Aquatic Toxicology 32: 31–42. https://doi.org/10.1016/0166-445X(94)00079-6
Sun, P.L.,
W.E. Hawkins, R.M. Overstreet & N.J. Brown-Peterson (2009). Morphological deformities as
biomarkers in fish from contaminated rivers in Taiwan. International Journal
of Environmental Research and Public Health 6: 2307–2331. https://doi.org/10.3390/ijerph6082307
Taylor, H.E.,
R.C. Antweiler, D.A. Roth, C.N. Alpers & P. Dileanis (2012). Selected trace elements in the
Sacramento River, California: Occurrence and distribution. Archives of
Environmental Contamination and Toxicology 62: 557–569. https://doi.org/10.1007/s00244-011-9738-z
Weis, J.S.
& P. Weis (1977). Effects of heavy metals on development of the killifish, Fundulus heteroclitus.
Journal of Fish Biology 11: 49–54. https://doi.org/10.1111/j.1095-8649.1977.tb04097.x
Woodworth, J.
& D. Pascoe (1982). Cadmium toxicity to rainbow trout, Salmo gairdneri
Richardson: a study of eggs and alevins. Journal
of Fish Biology 21: 47–57. https://doi.org/10.1111/j.1095-8649.1982.tb02822.x
Yang, X., D.
Yin, H. Sun, X. Wang, L. Dai, Y. Chen, M. Cao (1999). Distribution and bioavailability
of rare earth elements in aquatic microcosm. Chemosphere 39: 2443–2450. https://doi.org/10.1016/S0045-6535(99)00172-1
Zhang, H., H. Cao, Y. Meng, G. Jin & M. Zhu (2012). The toxicity of cadmium (Cd2+)
towards embryos and pro-larva of soldatov’s catfish (Silurus soldatovi).
Ecotoxicology and Environmental Safety
80: 258–265. https://doi.org/10.1016/j.ecoenv.2012.03.013