Effects of ZnO nanoparticles on the Giant freshwater prawn (Macrobrachium rosenbergii, de Man, 1879): Reproductive performance, larvae development, CHH concentrations and anti-oxidative enzymes activity

Highlights

• ZnO cause strong effects on reproductive performance in M. rosenbergii.

• In 100 mg/L ZnO, M. rosenbergii broodstock didn’t spawn at all.

• In 50 mg/L ZnO, M. rosenbergii spawned but larvae died as soon as they hatched.

• Fertilization rate and eggs weight parameters were influenced by ZnO.

• Antioxidant enzymes activities have direct relations to ZnO levels.

Abstract

The Giant freshwater prawn (Macrobrachium rosenbergii) breeds when in captive conditions. The eggs of a clutch are attached to the abdomen of berried females. Zinc oxide (ZnO) is one of the most important metal oxide-nanoparticles (NPs) that is widely used in various industries and is released into aquatic environments from wastewater management facilities. The present study was conducted to evaluate effects of ZnO on values for the reproductive variables: larvae development, crustacean hyperglycemic hormone (CHH) release from the X-organ into the hemolymph and anti-oxidative enzymes activity of M. rosenbergii. There were five groups including a group not treated (control), and groups treated with10, 20, 50, 100 mg/L ZnO in triplicate during a 90-day period. Results indicated that ZnO-NPs have marked effects on reproductive performance, offspring development, CHH release from the X-organ into the hemolymph and anti-oxidant enzymes activities with there being no spawning of brood-stock in the 100 mg/L ZnO group and in the prawns treated with 50 mg/L there was spawning but there was larvae mortality immediately subsequent to hatching. Also, values for viability rate of eggs, dry weight of eggs, brood-stock inter-spawn period and egg clutch somatic index (ESI) reproductive variables were affected by the NP. This NP was found to have a dose-dependent effect on CHH release from the X-organ into the hemolymph and also superoxide dismutase (SOD) and catalase activities in M. rosenbergii. The results indicate that M. rosenbergii, a freshwater decapod crustacean, is an appropriate species to study nano-material effects on reproduction in freshwater ecosystems.

Introduction

Nanoparticles (NPs) are materials that at least, one of the dimensions is in range of 1–100 nm and are widely used for various purposes in different industries (Qu et al., 2013). Zinc oxide (ZnO) NPs are one of these materials which have a white to yellowish-white color and is a crystalline powder that is soluble in water (Dimapilis et al., 2018). This NP is one of the most important metal oxide NPs and due to the large surface ratio to size and marked catalytic activities is widely used in various industries such as for rubber, paint, coating, cosmetic (Jiang et al., 2018), biomedical ointment, and anti-microbial (Siddiqi et al., 2018; Raghunath and Perumal, 2017) production as well as for water disinfection (Dimapilis et al., 2018; Ashori et al., 2019) and wastewater treatment (Qu et al., 2013; Nezhadheydari et al., 2019). Because of the nano-scale size of ZnO, this compound can penetrate cell walls which results in production of reactive oxygen species (ROS) and eventually leads to cell necrosis and, therefore, tissue damage (Stoimenov et al., 2002). Physicochemical properties, oxidizing agent production, duration in time cells are in contact and concentration are the main factors that pose a threat to the health of aquatic species when there is use of the metal oxide nanoparticles (MeO-NPs) for different applications (Raghunath and Perumal, 2017; Vali et al., 2020). The NPs can affect different organs of aquatic species, and signals may be transmitted between these organ systems, affecting body functions (Brohi et al., 2017). There can be effects of these agents directly on primary ovarian follicles and/or subsequent disruption of vitellogenesis of aquatic organisms (Wang et al., 2011).

The MeO-NPs are relatively new materials and there are concerns about the possible hazards on the reproduction of organisms because animal cells can easily uptake these NPs through the cytoplasmic membrane. One of these synthetic MeO-NPs is ZnO can have surface defects such as edges and corners that results in abrasive actions in disrupting cell walls (Stoimenov et al., 2002). Even though there are reports of zinc oxide NPs in the M. rosenbergii diet when feeding occurs as a supplement in aquaculture enterprises (Thirunavukkarasu et al., 2014, 2019), there continues to be incorporation of ZnO in diets in the micro-sized, but not nano-sized forms. The MeO-NPs in micro-size forms aren’t toxic and can be safely used in various animal feed and food industries. Even though this is the situation, there are many reports that ZnO-NPs due to the small size, structure and water solubility properties are toxic to aquatic organisms (Franklin et al., 2007; Aruoja et al., 2009; Bai et al., 2010; Hao and Chen, 2012; Tomilina et al., 2014; Chupani et al., 2018). The ZnO-NPs are released into the aquatic ecosystems through domestic and industrial wastewaters and can cause adverse effects on aquatic organisms and result in toxicity as a result of effects on reproductive organs (Rajput et al., 2018; Wu et al., 2019). Reproductive toxicity occurs when there are adverse effects on reproductive performance in adults, as well as toxicity during developmental stages, therefore, affecting production of offspring (Kumar et al., 2018; Rezaei Tavabe et al., 2020). There is greater toxicity of NPs in females because of effects on the reproduction system, and germ cells as well as during embryogenesis (Brohi et al., 2017). There are some reports that ZnO in nano-size forms has acute and chronic effects on the reproductive capacity of Daphnia magna (Wiench et al., 2009), earthworms Eisenia fetida (Cañas et al., 2011) and Zebrafish Danio rerio (Choi et al., 2016). Nevertheless, the reproductive toxicity of NPs and ZnO NPs on aquatic organisms and especially reproductive capacity of decapod crustaceans has not been studied in depth.

Different aquatic organisms have different tolerances to stress; therefore, there may be differences in the physiological response in different species and reproductive consequences to stressors. Furthermore, in aquatic organisms the physiology associated with maturation and spawning appears to be tightly coupled with stress physiology responses (Schreck et al., 2001; Rezaei Tavabe et al., 2020). Depending on the stage of animal development, stress factors have different reproductive consequences and the stress response is a process that requires energy. Aquatic organisms also mobilize considerable energy resources for reproduction (Contreras-Sánchez et al., 1998). Like most invertebrates, crustaceans when in stressful conditions switch to an alternative anaerobic energy metabolism via glycolysis and hyperglycemia with the process being regulated by crustacean hyperglycemic hormone (CHH) which has been evaluated as a biochemical stress biomarker (Chung et al., 2010). In decapod crustaceans, CHH is primarily involved as a metabolizing factor and has important functions in reproduction and molting regulation (Tavabe et al., 2013). Also, these stress conditions can result in induction of production of reactive oxygen species (ROS) and oxidative stress in aquatic animals (Chang et al., 2012). Decapod crustaceans because of the ecological and physiological characteristics including wide habitat distribution, minimum mobility capacity, well-known ecological characteristics, numerical abundance, suitability for laboratory experiments and sensitivity to different stressors are excellent bio-indicators and bio-monitors for different contaminants in freshwater ecosystems (Rezaei Tavabe et al., 2010, 2019; Chen et al., 2020; Zhang et al., 2020). The giant freshwater prawn, Macrobrachium rosenbergii, is an important decapod crustacean aquaculture species; originally from the southeastern region of Asia, however, during the past decades these animals have been transplanted throughout many other countries globally, for aquaculture purposes (Tidwell et al., 2005; New and Nair, 2012). Because this species breeds readily in captivity and has marked reproductive capacities and the eggs are produced in clutches with egg attachment being to the abdomen section of the ovigerous females (Tavabe et al., 2013; Rafiee et al., 2015; Rezaei Tavabe et al., 2015a, b; Rezaei Tavabe et al., 2017), it is an appropriate benthic species for toxicological studies in laboratory conditions. The objective of the present study, therefore, was assessment of the possible effects of ZnO-NPs on reproductive performance, larvae development, CHH release from the X-organ into the hemolymph and anti-oxidative enzyme activity of M. rosenbergii.