Daphnias SPP As Bioindicator Organisms of Toxicity

REVISTA OBSERVATORIO DE LA ECONOMIA LATINOAMERICANA
Curitiba, v.21, n.10, p. 17419-17431. 2023.
ISSN: 1696-8352
Daphnias spp. as bioindicator organisms of toxicity and environmental

characterization of eutrophized aquatic systems
Daphnias spp. como organismos bioindicadores de toxicidade e

caracterização ambiental de sistemas aquáticos eutrofizados
DOI: 10.55905/oelv21n10-156
Recebimento dos originais: 15/09/2023

Aceitação para publicação: 16/10/2023
Maria Virgínia da Conceição Albuquerque

PhD in Environmental Engineering in the line of Research Water and Waste Treatment
Technologies by Universidade Estadual da Paraíba (UEPB)
Institution: Instituto Nacional do Semiárido (INSA)
Address: Avenida Francisco Lopes de Almeida, 4000, Serrotão, Campina Grande - PB,
Brasil, CEP: 58434700
E-mail: maria.albuquerque@insa.gov.br
Joelma Dias
PhD in Chemical Engineering in the line of Research in Regional Resources and
Environment by Universidade Federal de Campina Grande (UFCG)
E-mail: joelmadias@insa.gov.br
Fabiane Rabelo da Costa Batista

PhD in Genetics and Plant Improvement in the Area of Agronomy, with emphasis on
Genetics by Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF)
E-mail: fabiane.costa@insa.gov.br.
Emmanuelle Marie Albuquerque Oliveira

Specialist in Pediatrics and Neonatal ICU by Faculdade Novo
Horizonte de Ipojuca (FHN)
Institution: Universidade Estadual da Paraíba (UEPB)
Address: Rua Baraúnas, 351, Universitário, Campina Grande – PB, CEP: 58429-500
E-mail: emmanuellemarie.uepb@gmail.com
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REVISTA OBSERVATORIO DE LA ECONOMIA LATINOAMERICANA, Curitiba, v.21, n.10, p. 17419-17431. 2023..

Curitiba, v.21, n.10, p. 17419-17431. 2023.
ISSN: 1696-8352
Maria Célia Cavalcante de Paula e Silva

PhD in Environmental Engineering, Research Line Water and Waste
Treatment Technologies
E-mail: celiadoutorado@gmail.com
Roberta Milena Moura Rodrigues

Master in Environmental Science and Technology Research Line Water and Waste
Treatment Technologies
E-mail: robertamilena_rm@hotmail.com
Valderi Duarte Leite

PhD in Hydraulics and Sanitation, Actuation Area Water and Waste Treatment
Technologies by Escola de Engenharia de São Carlos da Universidade de
São Paulo (EESC – USP)
E-mail: mangabeiraleite@gmail.com
Wilton Silva Lopes

PhD in Chemistry area of operation Water and Waste Treatment Technologies
E-mail: wiltonuepb@gmail.com
ABSTRACT
The ecotoxicological study is a tool for determining the harmful effects of chemical
agents on the environment, enabling the verification of the ecotoxicological
characteristics of chemical substances, mechanisms of action on living organisms,
definition of guidelines for controlling the quality of effluents and evaluation of efficiency
of water treatment processes. Therefore, this article presents a review on the assessment
of ecotoxicity as an environmental characterization tool in eutrophicated aquatic systems
using Daphnias spp. as bioindicator organisms. The studies evaluated showed that
cyanotoxins cause inhibition of feeding activity, decreased growth, low reproduction rate,
poor offspring formation, decreased lifespan and increased tolerance to toxins throughout
generations of this microcrustacean. Acute toxicity analyzes showed different toxic
effects, as the results depended on the strain tested. Some factors are attributed to the
toxicity of cyanobacteria extracts in zooplanktonic organisms, mainly nutritional
inadequacy, decreased filtration activity, inhibition of digestive enzymes,
bioaccumulation and oxidative stress.
Keywords: Daphnias ssp., ecotoxicity, cyanobacteria.
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RESUMO
O estudo ecotoxicológico é uma ferramenta para a determinação de efeitos deletérios de
agentes químicos sobre o meio ambiente, possibilitando a verificação das características
ecotoxicológicas de substâncias químicas, mecanismos de ação sobre organismos vivos,
definição de diretrizes para controle da qualidade de efluentes e avaliação da eficiência
de processos de tratamento de águas. Diante disso, este artigo apresenta uma revisão sobre
a avaliação da ecotoxicidade como ferramenta de caracterização ambiental em sistemas
aquáticos eutrofizados utilizando como organismos bioindicadores a Daphnias spp. Os
estudos avaliados apontaram que as cianotoxinas causam inibição da atividade alimentar,
diminuição no crescimento, baixo índice de reprodução, má formação de filhotes,
diminuição do tempo de vida e aumento da tolerância às toxinas ao longo de gerações
deste microcrústaceo. As análises de toxicidade aguda apresentaram diferentes efeitos
tóxicos, pois os resultados dependeram da cepa testada. Alguns dos fatores atribuídos à
toxicidade de extratos de cianobactérias em organismos zooplanctônicos, foram
principalmente, a inadequação nutricional, diminuição da atividade de filtração, inibição
de enzimas digestivas, bioacumulação e estresse oxidativo.
Palavras-chave: Daphnia ssp., ecotoxicidade, cianobactérias.
1 INTRODUCTION
Cyanobacteria are distributed throughout the world and their blooms are a concern
in aquatic ecosystems, as they cause adverse effects on all aquatic biodiversity (KIM et
al., 2019). Generally, these microorganisms reduce the quality of aquatic ecosystems and
the efficiency of the energy flow from producers to herbivores, as they have low
nutritional value and generate toxins (LYU et al., 2019).
The toxins produced by these microorganisms can exert harmful effects on
zooplankton, with consequences for the survival, reproduction and population growth rate
of these organisms. However, the patterns of cyanobacteria and cyanotoxin actions on
herbivorous zooplankton are controversial. Some authors report, in addition to negative
effects, neutral and positive effects on zooplankton (FERRÃO-FILHO et al., 2009;
ZAGATTO et al., 2012).
Possible adaptive advantages of toxin production have been pointed out by
Holland and Kinnear (2013) and Omidi , Esterhuizen-Londt and Pflugmacher (2018) who
discuss the importance of these metabolites for competitive success, through allelopathic
effects , toxicity and persistence; and/or “physiological facilitators”, in improving
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metabolic activities, such as photosynthetic efficiency. In addition to the production of

bioactive metabolites, the high versatility in morphological attributes such as the
formation of large filaments and colonies, favors resistance to predation (GER et al.,
2016; RANGEL et al., 2020). In general, together with abiotic factors, these attributes are
considered to favor the dominance of cyanobacteria. In turn, such phenomena can cause
changes not only in water quality, but above all in the structure and functioning of these
ecosystems, generating loss of biodiversity, directly affecting the consumer community
(AMORIM et al., 2019) and limiting the flow of energy in aquatic trophic webs.
Despite being great filter feeders, daphinids tend to have a reduced ability to select
the particles they ingest, being directly affected by fluctuations in phytoplankton that lead
to qualitative and quantitative variations in the diet of these animals (KOUSSOROPLIS
et al., 2017; FERRÃO-FILHO et al., 2019). The rapid evolution of these consumers in
response to eutrophication and the consequent occurrence of harmful blooms may have
implications at the ecosystem level (CHISLOCK et al., 2019) such as the suppression of
trophic decoupling due to the dominance of cyanobacteria in phytoplankton.
The toxic effects of cyanobacteria and their metabolites produced in aquatic fauna,
including microinvertebrates, zooplankton and fish, have been the subject of several
studies (FERRÃO-FILHO and KOZLOWSKY-SUZUKI, 2011; ZANCHETT and
OLIVEIRA-FILHO, 2013). Special attention has been paid to cyclic peptides -
hepatotoxic microcystins, neurotoxic alkaloids - analogues of anatoxin-a (ATX-A) and
saxitoxin (STX), and cylindrospermopsin (CYN) - cytotoxic tricyclic guanidine alkaloid
(KOUSSOROPLIS et al., 2017; FERRÃO -FILHO et al., 2019).
For some decades now, the evaluation of fresh effluents or already treated water
has been described and recommended by standard methods from various international
entities such as the International Organization for Standardization (ISO), the Organization
for Economic Cooperation and Development (OECD), the US Environmental Protection
Agency (USEPA), among other environmental protection organizations. Among the
methods used are ecotoxicological tests, which are well analyzed and in many countries
they are a standard tool for characterizing effluent quality (POWER and BOUMPHREY,
2004).
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The ecotoxicological study is a tool for determining the harmful effects of

chemical agents on the environment, enabling the verification of the ecotoxicological
characteristics of chemical substances, mechanisms of action on living organisms,
definition of guidelines for controlling the quality of effluents and evaluation of efficiency
of treatment processes (RIZZO, 2011). Therefore, this article presents a review on the
assessment of ecotoxicity as an environmental characterization tool in eutrophicated
aquatic systems using Daphnias spp. as bioindicator organisms.
2 METHODOLOGY
A bibliographic, descriptive, integrative literature review type survey was carried
out. The analysis was carried out by searching for publications indexed in databases:
LILACS, MEDLINE, SCOPUS and Web of Science and SciELO Virtual Library. The
method of reading and evaluation at a systemic level was used to carry out the systemic
and descriptive analysis of the information. To this end, articles covering most of the
years of research were randomly selected. The key words used for this search were:
“Daphnia spp.”, “ecotoxicity” and “cyanobacteria”, published between 2000 and 2022.
Furthermore, this study is qualitative in nature, as it establishes connections between the
aspects theoretical and conceptual used to discuss the topic with the researchers'
perception.
3 RESULTS AND DISCUSSION

According to Ferrão-Filho, Herrera and Echeverri (2014), the bioaccumulation of
microcystins in aquatic animals occurs through two main routes: the consumption of
bacterial cells during blooms and the ingestion of water contaminated by dissolved toxins.
In their research, the authors used three species of cladocerans: Moina micrura , Daphnia
laevis and Daphnia similis , which were exposed for 96 hours to aqueous extracts of
freeze-dried flower matter at different concentrations. The results showed that the uptake
of microcystins by zooplankton was directly proportional to the concentrations of
aqueous extracts, therefore showing that the ingestion of contaminated water from the
dissolution of the toxin is also a determining factor for bioaccumulation. This study
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showed, that the uptake of microcystin from the dissolved fraction by zooplankton is
possible, not only from the ingestion of these cyanotoxins or bound to cells.
Kosiba et al. (2018) in their study sought to answer the hypothesis of whether the
effect of dissolved microcystins would be more evident in artificial reservoirs and lakes
than in natural waters. In the study, the concentrations of microcystins dissolved in the
waters studied ranged from 0.07 to 0.81 μg . L -1
. The authors showed that artificial
lagoons were more prone to cyanobacteria blooms. Zooplankton present in artificial lakes
were exposed to significantly higher concentrations of dissolved microcystins than those
in natural lakes. Using a general linear model (GLM) regression, the study further
identified a significant relationship between dissolved microcystins on the density,
biomass and richness of certain zooplankton groups (ciliates, rotifers, cladocerans,
copepods), which were significantly lower in the artificial lagoons than in natural lakes.
The impact of microcystins and the time they remained in the water caused structural
changes in the phytoplankton.
Ortiz-Rodriguez et al. (2018) evaluated the acute effects related to the exposure
time of MC-LR in Daphnia magna on the biotransformation of its antioxidant enzymes
(glutathione S-transferase, GST and catalase, CAT), subsequent lipid peroxidation, into
lactate and the enzyme lactate dehydrogenase (LDH). Daphnia magna neonates (<3 days)
and young adults (7 days) were exposed to increasing concentrations of MC-LR (up to
100 µg. L -1 ) for 24 and 48 h. It was found that the metabolic activities of Daphnia magna
were decreased in exposure to higher concentrations of MC-LR, suggesting a lower
capacity to biotransform cyanotoxin. Oxidative protection was more efficient in neonates,
where TAC was strongly elevated and contributed to buffering oxidative stress. Lactate
dehydrogenase LDH was negatively affected in neonates and adults by exposure to all
used concentrations of MC-LR, leading to constant low concentrations. As this enzyme
is involved in the production of rapidly needed energy, the results suggested an energetic
compromise due to the presence of MC-LR.
Brachionus Survival calyciflorus Pallas (Rotifera) and Daphnia pulex Leyding (
Cladocera ) exposed to pure microcystin (MC-LR), anatoxin-a (ATX-A) and five extracts
obtained from cyanobacteria Microcystis , Planktothrix and Dolichospermus spp.,
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Pawlik-Skowrońska and collaborators 2019 obtained results relevant to different

responses of the organisms zooplankton at high concentrations of pure MC-LR, ATX and
complex cyanobacteria extracts. The toxicity of the extracts to invertebrates was greater
than that exerted by pure cyanotoxins and depended on the composition of the
cyanobacteria metabolites: Microcystis spp. The extract containing anabaenopeptins A
and B, aeruginosamide , four cyanopeptolin variants and five MCs were not found to be
toxic to any of the organisms, while the Planktothrix extract agardhii (I), containing
anabaenopeptins A, B, F, 915, oscililide Y, five different aeruginosins and four MC
variants were more toxic to Daphnia than to rotifers. This indicated that non-ribosomal
oligopeptides and MCs had an essential contribution to toxicity and their effects on
specific species or populations may vary depending on the secondary metabolic profile
of cyanobacteria.
Investigating the physiological reactions of microcystin – LR produced by
Microcystis aeruginosa (PCC7806) in Daphnia magna , Savic et al. (2020) tested the
following hypotheses: I) the presence of D. magna will negatively affect growth, increase
the stress response and metabolite production in Microcystis aeruginosa. II) The presence
of Microcystis aeruginosa will negatively affect the physiological responses and life
characteristics in Daphnia magna . To test these hypotheses, experiments were conducted
in a specially designed co-culture chamber that allowed exchange of metabolites without
direct contact. A clear impact was evidenced, as cyanobacterial metabolites reduced
Daphnia magna survival and decreased oxidative stress enzyme activity. Simultaneously,
the presence of D. magna did not affect the photosynthetic activity of the cyanobacteria.
However, there was a decrease in cell density, suggesting possible allocation of energy to
anti-oxidative stress enzymes or other protective mechanisms against Daphnia chemicals.
The elevated concentration of intracellular and extracellular microcystin-LR, as well as
intracellular concentrations of aerucyclamide A and D in the presence of Daphnia ,
indicated a potential protective function.
In a study carried out by Shahmohamadloo et al. (2019) changes in the
reproduction, growth and survival of Ceriodaphnia were investigated dubia , Daphnia
magna and Hexagenia grown in laboratories exposed to microcystins through a series of
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life cycle bioassays. Organisms were exposed to a concentration gradient ranging from
-1 -1
0.5 µg. L to 300 µg. L of microcystins, which corresponds to the values normally
found in fresh waters during the flowering process. The lethal concentrations in C. dubia
(LC 50 = 5.53 µg. L -1) and D. magna (LC 50 = 85.72 µg. L -1) exposed to microcystins
were among the lowest recorded to date, and reproductive effects have been observed at
concentrations as low as 2.5 µg. L -1. The length of D. magna was significantly affected
-1
in treatments with microcystin concentrations greater than 2.5 µg. L . However, no
lethality or growth impairment was observed in Hexagenia.
Savic and colleagues (2021) exposed cell-free cyanobacterial concentrations of
Microcystis aeruginosa to represent higher and lower ecologically relevant concentrations
of cyanobacteria and their metabolites to assess whether the concentration and time-
dependent negative impact, survival, digestion of expression tag Genetics and
metabolism, response to oxidative stress, cell cycle and molting, in Daphnia magna . As
a consequence of all these responses and presumably molecular and physiological
changes, the survival of D. magna was impaired over time in a concentration-dependent
manner. The authors confirmed that in addition to microcystin-LR, other metabolites
contribute to the negative impact on the survival of D. magna .
Ferrão – Filho and collaborators (2020), evaluated the effects of the
cyanobacterium Raphidiopsis raciborskii (CYRF-01) on the swimming activity and
physiological parameters of Daphnia similis , as well as the movements of antennae,
limbs, post-abdominal claw and heart rate. The results showed a rapid effect of the CYRF
strain on all parameters. Animals began to be immobilized within the first 30 minutes of
exposure and showed complete paralysis after 2 h at 500 μg . L −1 of saxitoxin and after
24 h in other concentrations. The antennas stopped moving after 2-3 h at 250-500 μg . L
−1
, reinforcing the paralysis of swimming activity in Daphnia . Thoracic movements,
post-abdominal movements and heart rate were significantly inhibited after 30 min at all
concentrations.
The study by Albuquerque (2022) evaluated the acute toxicity of the species
Daphnia magna to exposure to different cyanobacteria and different concentrations of
cyanotoxins. The results demonstrated that Daphnia neonates showed a high rate of
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herbivory . The immobility/mortality effects were specific to each cyanobacteria strain.

Comparing the survival of cladocerans exposed to crude cultures and lysates containing
microcystin-LR (MC-LR), saxitoxin (STX), anatoxin-a (ATX-A) and
cylindrospermopsin (CYN), results were obtained relevant to different responses of
organisms to high concentrations (5 μg . L -1
) for pure MC-LR, and low concentrations
(0.61 μg . L -1
) of ATX-A. The hypotheses that the sensitivity of the species Daphnia
magna exposed to strains of toxic cyanobacteria is greater in colonial species, and that
the rate of population immobility of cladocerans increases when exposed to higher
concentrations of cyanotoxins, were refuted. At an initial concentration 2.05 μg . L -1
of
SXT, the movements of Daphnia magna were temporarily paralyzed when exposed to the
neurotoxic cyanobacteria Raphidiopsis raciborskii . However, when they were exposed
to medium free of the smallest dilutions, there was a high rate of recovery of motor
activity, since only around 20 to 25% of the individuals showed immobility. Relating the
results obtained to what occurs in the natural aquatic environment, during flowering, the
Daphnia species are exposed to intracellular and extracellular toxins, therefore, there may
be a variation in the sensitivity of these animals at the beginning and end of flowering,
which may affect the structure of the zooplankton community and interfere throughout
the trophic chain.
4 CONCLUSION
Considering the negative interference of cyanobacteria on zooplankton, and the
exposure of cladocerans to intracellular and extracellular toxins in aquatic environments,
we verified the urgent need to evaluate the adverse effects of cyanobacteria producing
cyanotoxins on Daphnia under these two exposure routes, contributing to the knowledge
of the sensitivity of these animals, as well as understanding the role of these toxins in
aquatic ecosystems.
The studies evaluated showed that cyanotoxins cause inhibition of feeding
activity, decreased growth, low reproduction rate, poor offspring formation, decreased
lifespan and increased tolerance to toxins throughout generations of Daphnia spp. Acute
toxicity analyzes showed different toxic effects, as the results depended on the strain
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tested. Some factors are attributed to the toxicity of cyanobacteria extracts in

zooplanktonic organisms, mainly nutritional inadequacy, decreased filtration activity,
inhibition of digestive enzymes, bioaccumulation and oxidative stress.
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REVISTA OBSERVATORIO DE LA ECONOMIA LATINOAMERICANA

Curitiba, v.21, n.10, p. 17419-17431. 2023.

Daphnias spp. as bioindicator organisms of toxicity and environmental

Daphnias spp. como organismos bioindicadores de toxicidade e

Recebimento dos originais: 15/09/2023

Maria Virgínia da Conceição Albuquerque

Fabiane Rabelo da Costa Batista

Emmanuelle Marie Albuquerque Oliveira

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Maria Célia Cavalcante de Paula e Silva

Roberta Milena Moura Rodrigues

Valderi Duarte Leite

Wilton Silva Lopes

Keywords: Daphnias ssp., ecotoxicity, cyanobacteria.

REVISTA OBSERVATORIO DE LA ECONOMIA LATINOAMERICANA, Curitiba, v.21, n.10, p. 17419-17431. 2023..

Palavras-chave: Daphnia ssp., ecotoxicidade, cianobactérias.

REVISTA OBSERVATORIO DE LA ECONOMIA LATINOAMERICANA, Curitiba, v.21, n.10, p. 17419-17431. 2023..

metabolic activities, such as photosynthetic efficiency. In addition to the production of

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The ecotoxicological study is a tool for determining the harmful effects of

3 RESULTS AND DISCUSSION

REVISTA OBSERVATORIO DE LA ECONOMIA LATINOAMERICANA, Curitiba, v.21, n.10, p. 17419-17431. 2023..

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Pawlik-Skowrońska and collaborators 2019 obtained results relevant to different

REVISTA OBSERVATORIO DE LA ECONOMIA LATINOAMERICANA, Curitiba, v.21, n.10, p. 17419-17431. 2023..

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herbivory . The immobility/mortality effects were specific to each cyanobacteria strain.

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tested. Some factors are attributed to the toxicity of cyanobacteria extracts in

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ALBUQUERQUE, Maria Virgínia da Conceição. Assessment of the potential toxic effect

AMORIM, C.A; VALENÇA, C.R; MOURA-FALCÃO, R.H; MOURA, A.N. (2019)

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FERRÃO-FILHO, A. DA S., & DA SILVA, D. A. C. (2020). Saxitoxin-producing

FERRÃO-FILHO, A.S; DIAS, T.M; PEREIRA, U.J; SANTOS, J.A; KOZLOWSKY-

GER, K.A; URRUTIA-CORDERO P; FROST, P.C; HANSSON, L.A; SARNELLE O,

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KOUSSOROPLIS, A. M., SCHWARZENBERGER, A., WACKER, A. (2017). Diet

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SAVIC, G.B; COLINET, H; BORMANS, M; EDWARDS, C; LINDA, A; LAWTON,

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SHAHMOHAMADLOO, R. S., POIRIER, D. G., ORTIZ ALMIRALL, X., BHAVSAR,

WIECZERZAK, M.; NAMIESNIK, J.; KUDLAK, B. Bioassays as one of the Green

ZAGATTO, P.A.; BURATINI S.A.; ARAGÃO M., FERRÃOFILHO; A.S. 2012.

ZANCHETT G, OLIVEIRA-FILHO EC, 2013. Cyanobacteria and cyanotoxins: from

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