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Cadmium and Morphological Alterations in the Rotifer Philodina Cf

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Cadmium and Morphological Alterations in the Rotifer Philodina Cf Cadmium and morphological alterations in the rotifer Philodina cf. roseola (Bdelloidea: Philodinidae) and the worm Aeolosoma hemprichi (Annelida: Aeolosomatidae) Daniela Pérez-Yañez, Danika Ruth Soriano-Martínez, Mendy Eded Damian-Ku, Eduardo Cejudo-Espinosa & Jesús Alvarado-Flores* Unidad de Ciencias del Agua, Centro de Investigación Científica de Yucatán A. C. Cancún, Quintana Roo, México. Calle 8, No. 39, Mz. 29, S.M. 64, C.P. 77500; [email protected], [email protected], [email protected], [email protected], [email protected] * Correspondence Received 23-I-2019. Corrected 29-V-2019. Accepted 27-IX-2019. Abstract: Cadmium is a toxic metal for zooplankton that produces deformations. It is also considered an environmental hazard to aquatic life. Since it has a significant effect in some marine organisms, we used two native zooplankton species from Quintana Roo, Mexico to obtain data regarding cadmium toxicity including the threshold concentration for observable morphological alterations and the percentage of organisms with morpho- logical alterations at the exposure concentrations. We used the rotifer Philodina cf roseola and the oligochaeta Aeolosoma hemprichi, since both feed from the algae Nannochloropsis oculata. Both animals were exposed to a cadmium concentration range from 0.05 mg/l (0.047 mg/l, real concentration) to 10.0 mg/l (9.39 mg/l, real con- centration) for 24 h. The LC50 for cadmium in P. cf roseola was 0.7 mg/l (0.65 mg/l, real concentration), whereas in A. hemprichi was 3.38 mg/l (3.17 mg/l, real concentration). The exposure of cadmium at 0.5 mg/l (0.47 mg/l, real concentration) for less than 24 h induced morphological alterations in the lorica of rotifers, foot deforma- tions, and constriction in the middle part of the body. In oligochaetes, damage to the epidermis was noted. The threshold concentration where deformations appeared in rotifer was 0.3 mg/l at 24 h, while in oligochaeta was 0.5 mg/l (0.47 mg/l, real concentration) at 30 min. We concluded that cadmium promotes alterations in aquatic organisms due to direct exposure added to the culture medium. Key words: teratology, ecotoxicology, zooplankton, Yucatan Peninsula, metal toxicity. Pérez-Yañez, D., Soriano-Martínez, D. R., Damian-Ku, M. E., Cejudo-Espinosa, E., & Alvarado-Flores, J. (2019). Cadmium and morphological alterations in the rotifer Philodina cf. roseola (Bdelloidea: Philodinidae) and the worm Aeolosoma hemprichi (Annelida: Aeolosomatidae). Revista de Biología Tropical, 67(6), 1406-1417. Cadmium is present in aquatic ecosystems for Toxic Substances and Disease Registry through both anthropogenic and natural means, (ATSDR, 2016). In general terms, cadmium but is hazardous to aquatic organisms and belongs to the IIB group of the periodic table human health (ATSDR, 2016). It is one of the and has an atomic mass of 112.41. Its ionic form most toxic elements to which man is exposed of cadmium (Cd2+) is usually combined with (Bernard, 2008), causing severe adverse effects oxygen (CdO2), chloride (CdCl2), or sulfate from chronic exposure. It also ranks seventh (CdSO4) (Kabata-Pendias, 2001). According on the substance priority list from the Agency to several reports, an estimated 300 000 tons 1406 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(6): 1406-1417, December 2019 of cadmium a year are released to the environ- exposure in rotifers and oligochaetes exist. ment (Kabata-Pendias, 2001; Nava-Ruiz & Therefore, a study of this kind is necessary Mendez-Armenta, 2011). to have a better understanding of this metal’s The first report of cadmium in the Yucatan hazardous effects on invertebrate communities. Peninsula was published back in 1987 (Rojas- For that reason, the present study is the Minguer & Morales-Vela, 2002). The report first to show that cadmium induces morpholog- found that this substance has high persistence ical alterations in species of rotifers (Philodina and wide distribution in underground water in cf roseola) and necrosis in oligochaetes (Aeo- the Yucatan Peninsula, to the point that con- losoma hemprichi) at concentrations below the centrations ranging from 0.02 to 0.062 mg/l LC50, within an exposure time of less than 24 h. have been reported. These values exceed the This investigation opens the door to potentially maximal permissible limit of cadmium concen- using these two native species as bio-indicators trations at sea (0.005 mg/l), set by the current of cadmium pollution. Our interest is to help Mexican legislation (NOM-127-SSA1-1994, generate information for the protection of water 1994). It also violates the Ley Federal de and biological resources and to help determine Derechos en Materia de Agua (Federal Law on its vulnerability. Water Rights) (2016) which suggests concen- Currently, there are 58 reports of cad- trations of 0.01 mg/l in water and 0.1 mg/l for mium in water and 16 reports in tissues of protection of aquatic life as a limit (Pacheco- aquatic organisms in the Yucatan Peninsula Ávila, Cabrera-Sansores, Barcelo-Quintal, & (Pacheco-Ávila et al., 2011; Rojas-Minguer & Pacheco-Perera, 2011). Morales-Vela, 2010; Avelar et al., 2013; Solís Regrettably, there is no continuous moni- et al., 2008; & Tah-Euan, 2009). However, toring for the variations of cadmium concentra- there is still a lack of information regarding tion in water, sediment, and biota. Therefore, the sensitivity of aquatic species to cadmium. the risks of cadmium pollution for aquatic In this research, we experimentally observed biota are unknown, which has become a seri- the deformations associated to acute exposure ous problem because cadmium and other met- to cadmium. For the purpose of this study, we als are persistent, toxic, and bio-accumulate assumed that deformations were physiologi- (Mackay, Celsie, Powell, & Parnis, 2018). For cal responses of molecular, cellular tissue and instance, cadmium’s acute toxicity, expressed biochemical damage before lethality is induced by high doses in short times (Alvarado-Flores, as lethal concentration 50 (LC50) in zooplank- ton, ranges between 0.01 and 39 mg/l. The Rico-Martínez, Adabache-Ortiz, & Silva-Bria- no, 2015; Lavoie et al., 2017). lowest LC50 value reported for cadmium in rotifers from freshwater strains of Mexico City, such as Brachionus calyciflorus, is 0.01 mg/l MATERIALS AND METHODS (Sarm, Martínez-Jerónimo, Ramírez-Pérez, & Nandini, 2006), while the highest value is for Collection and cultivation in labora- Brachionus plicatilis (Snell, Moffat, Janssen, tory: Organisms were collected from June & Persoone, 1991). to October 2017 in two dolines (cenotes) in Regarding the toxicity of cadmium for northeastern Quintana Roo. Temperature (°C), oligochaetes, Neto, Moreira, Dos Santos Lima, pH, and electrical conductivity (mS/cm) were Daam and Rocha (2019) reported that, for 96 h measured in situ by means of a previously of exposure, the LC50 of cadmium chloride is calibrated multi-parametric probe Condutronic 627 and 364 μg/L for Allonais inaequalis and PC18. Organisms were collected using a Wis- Dero furcatus respectively. This shows that the consin net with a 55-µm mesh aperture. Three latter species is almost twice as sensitive to this drags were performed to collect a final volume metal as A. inaequalis. However, no reports of of 250 ml per sample. Two samples per doline morphological alterations induced by cadmium were collected. Specialized dichotomic and Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(6): 1406-1417, December 2019 1407 pictorial keys were used for species identifica- mL for 15 days with three replicates. Both spe- tion (Fontaneto & Ricci, 2004; Fontaneto, De cies were incubated in a bio-climatic cabinet Smet, & Melone, 2008; Brinkhurst, 1971). (Thermo Scientific) at a temperature of 25 ± The species identified as Philodina cf 2 °C, with a photoperiod of 12 hours of light roseola was isolated from the locality named and 12 hours of darkness. After 15 days, the “La Victoria” (20°59’18.8” N & 87°12’08.2” organisms with the best growth per well were W), a doline with a maximum depth of 20 transferred to petri dishes in a volume of 10 meters. More details related to identifications mL and reproduced in a monoclonal way over and photographs of the specimen are added 2 months in preparation for the cadmium expo- as an appendix (Digital Appendix 1, Digital sure experiments. Appendix 2, Digital Appendix 3) to this manu- We used these two native species from script. This location has a rocky bottom with Quintana Roo, Mexico to estimate the hazard unsolidified sediment and mostly arboreal and to aquatic biota because they have the potential herbaceous vegetation. The temperature at the to become model organisms for ecotoxicol- time of collection was 27.2 ºC with an electri- ogy and genotoxicology in assays and for cal conductivity of 0.8 mS/cm and a pH of 7.3. their importance in aquatic ecosystems (Song This site is also used for tourism and produc- & Chen, 2009; Snell, Johnston, & Matthews, tion of tilapia for human consumption. On the 2017). Additionally, rotifers and oligochaetes other hand, A. hemprichi was isolated from clonal reproduction permits individual geno- a cave-type urban doline named “Chac Mool types to be cultured for many generations (21°09’29.0” N & 86°52’14.6”W). This zone in the lab. has unsolidified sediments: the water had a temperature of 24.5 ºC, electrical conductivity Acute toxicity: Deionized water was used of 1.2 mS/cm and pH of 8.53. for all analytical work; for acute toxicity test- The isolation of organisms was carried ing, we utilized a standard solution of cad- out in 24-well polystyrene plates (Costar) in mium for atomic absorption (1000 Cd+2 mg/l in which one individual was placed per well in HNO3, Sigma-Aldrich).
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