Responses of the ecological characteristics and antioxidant enzyme activities in Rotaria rotatoria to UV-B radiation

UV-B radiation is an increasing threat to aquatic organisms and also a potential driving force for zooplankton population dynamics. To explore the ecological effects of UVR on rotifers and the responses of antioxidant system against UVR, the acute lethal effects, the life history strategies, population growth, and antioxidant enzyme activities were assessed in the Bdelloid Rotaria rotatoria after exposure to UV-B radiation. The results indicated that the persistence of tolerance in rotifer to stress was playing a more vital role than the radiation dose in survival. The larger the culture volume, the weaker the lethal effect. Rotifers prolonged their first reproductive time and shortened their reproductive period and longevity with the increasing of radiation dose, and the fecundity was significant inhibited by UV-B radiation. These responses can be taken as energy trade-off to retard their mortality. The population density of the rotifers increased at the lowest dose of radiation and then descended with the increasing of UVR dose, and this pattern was also corroborated by detecting the content of SOD and CAT, which suggested that hormesis also applies to R. rotatoria under UV-B radiation stress. The enzyme SOD has higher level of content and more sensitive to low UVR than CAT.


Introduction
Ultraviolet radiation is an important case of exogenous factor that is ecologically relevant for small-bodied invertebrates (Heine et al., 2019). Over the past few decades, it has been well demonstrated that nature ultraviolet-B (UV-B) radiation increased significantly with the continuing depletion of stratospheric ozone, which has becoming one of the grave concerns and most striking global changes (Robinson & Erickson, 2015;Peng et al., 2017). There is growing evidence that adverse biological effects of ambient ultraviolet radiation exposure occur in not only marine but also freshwater ecosystem at different trophic levels (Häder et al., 2007;Peng et al., 2017), involving algae (Sun et al., 2020), rotifers (Luijckx et al., 2018;Colangeli et al., 2019), copepods (Puthumana et al., 2017;Laspoumaderes et al., 2019), cladocerans (Fernández & Rejas, 2017), shrimps (Harbi et al., 2018;Marcoval et al., 2018), and fishes (Lawrence et al., 2020). In all cases, UVR was found to harm the organisms in question by damaging DNA directly at the molecular level and affect fitness at the individual and population levels (Grad et al., 2001). In terms of the former case, excessive UVR may cause oxidative stress by generating reactive oxygen species (ROS) that are highly reactive molecules and can directly damage DNA, lipids, and proteins, resulting in the elevated antioxidant enzymatic activity and linking to modulation of the expression of DNA repair-related genes as an efficient defense mechanism (Kim et al., 2015). For the latter, UV radiation acts as a stressor for several physiological processes that lead to reduced survival and limited reproduction capacity, associating with detrimental effects on life-cycle parameters and population growth of small-sized organisms (Malloy et al., 1997;Wong et al., 2015;Han et al., 2016).
Taking into account the sensitivity of zooplankton to ambient ultraviolet radiation, an increasing number of works have been focusing on the negative effects of increased UV-B radiation on zooplankton (Grad et al., 2001;Rautio & Tartarotti, 2010;Peng et al., 2017). The bdelloid rotifer, a kind of ancient asexually invertebrate, is the largest metazoan group that reproduces only through parthenogenesis, simultaneously notorious for the features of anhydrobiotic capability and horizontal gene transfer (Mark Welch & Meselson, 2000;Barraclough et al., 2007;Hespeels et al., 2020). These features are considered to be responsible for their success in adapting to most types of habitats (moss, lichens, temporary pools, soil, and water), stress tolerance, and having persisted asexually for millions of years (Ricci, 1983;Flot et al., 2013). The radio resistance in bdelloid rotifers has been reported with a 137 Cs source, which indicated that reproduction of the bdelloids Adineta vaga (Davis, 1873) and Philodina roseola (Ehrenberg, 1830) is much more resistant to ionizing radiation (IR) than that of monogononta rotifer (Gladyshev & Meselson, 2008), and Krisko et al. (2012) found that A. vaga is far more resistant to IR-induced protein carbonylation than the much more radiosensitive nematode Caenorhabditis elegans (Maupas, 1900). In another study, the survival of A. vaga was reduced under IR stress, what could be mediated by endogenously generated oxidative stress induced by reproduction (Latta et al., 2019). When exposing P. roseola to UV-B radiation, it appeared to shield itself from DNA damage through uncharacterized UV-absorbing compounds, but it was largely impossible to repair UV-Binduced damage. Fischer et al. (2013) reported that UV-irradiation had a significant negative impact on the reproductive output of P. roseola but was shown to have no significant effects on monogononta rotifer Brachionus rubens (Ehrenberg, 1838). The above incongruous founding could be attributed to the type of radiation and the intensity and dose they were exposed to. Therefore, further investigations are needed with the respects of the effects of exposure to incident UV-B on the reproduction, survival, and defense system in bdelloid rotifers.
Rotaria rotatoria (Pallas, 1766) is a conventional bdelloid rotifer species, which offers an advantageous model for investigating the ecological consequences of enhanced UV-B. Given the strong tolerance of bdelloid rotifer to environmental stressors, such as IR radiation (Gladyshev & Meselson, 2008;Krisko et al., 2012), we hypothesized that R. rotatoria could also hold the ability to tolerate significant UV radiation, and this capacity may be associated with the trade-off strategies among life historic components. In aquatic ecosystems, the tolerance and resistance of rotifer to ultraviolet radiation could be varied depending on the culture volume, radiation intensity, and duration. With this study, we examined the radiation lethality of UV-B (280 to 400 nm) under different culture systems, the responses of population growth, and fecundity of the R. rotatoria to the incident UVR, and measure the levels of superoxide dismutase (SOD) and catalase (CAT) of R. rotatoria under adverse conditions. We aimed to (1) detect the acute lethal effects of UVR to bdelloid rotifer; (2) estimate the ecological effects of harmful UVR on bdelloid rotifers; and (3) explore the responses of antioxidant system in bdelloid rotifers against UV radiation toxicity.

Rotifer collection and culture
The R. rotatoria was sampled at a pond near Jing village (31°73 0 67 00 N, 118°33 0 72 00 E) in Hexian County, Anhui Province, China. Then the rotifers were isolated individually under microscope and cultured in the 28°C constant temperature incubator. The EPA medium, used to maintain rotifers, was freshly prepared by dissolving 96 mg NaHCO 3 , 60 mg CaSO 4 , 60 mg MgSO 4 , and 4 mg KCl in 1 L of distilled water (pH 7.4-7.8) (Peltier & Weber, 1985). The algae Scenedesmus obliquus (Turpin) Kützing 1833, purchased from Freshwater Algae Culture Collection at the Institute of Hydrobiology (FACHBcollection), were semi-continuously cultured in HB-4 medium (Li et al., 1959) with the 16:8 light:dark photoperiod of 3000lx fluorescent light and 28°C in illumination incubator. The algae were stored at 4°C for using as rotifer foodstuff after centrifuging in exponential growth. We estimated the density of the algal concentrate by a hemocytometer, and the eventually density of the algal fed by rotifers is 1.0 9 10 6 cells/mL.

UV-B radiation settings
The ultraviolet radiation was supplied with UV-B lamps as the sole light source, which simulates the ultraviolet rays of the sun with the wavelength range of 280 to 312 nm and the main peak of 308 nm (UVB-308NM 8W, Shengzheng Guanya Optoelectronic Technology Co., Ltd.). The intensity of UVR was measured by a UV-B radiometer manufactured by Beijing Normal University. In order to ensure that rotifers were under the same UVR intensity, they were placed on the low-speed rotating platform directly below UV-B lamps. Furthermore, to obtain the stable intensity of UV light source, the lamp was turned on 30 min before the experiment began. For the following specific assay (mortality test, life history, population growth, and determination of antioxidant), the animals will be treated with different doses of UVR by exposing them under UV-B radiation for different times.

Mortality test
Before starting the experiments, the rotifer population was precultured at 28°C for at least one month to minimize maternal effects. To obtain the value for 50% of the lethal dose (semi-lethal dose, LD 50 ) upon UV-B radiation in three culture volumes of 0.5 ml, 6 ml, and 30 ml, we introduced 10 neonates (less than 6 h old) into different culture vessels (1-ml 24-well culture plate, 8-ml glass jars, and 50-ml beakers, respectively, resulting in the maximum water depth of 0.5, 1.6, and 2.3 cm, respectively.) which contained EPA medium with 1.0 9 10 6 cells/ml of S. obliquus and exposed them to constantly UV-B radiation at the intensity of 0.01, 0.02, 0.03, 0.04, and 0.05 mW/cm 2 . Under five radiation intensities (from 0.01 to 0.05 mW/cm 2 ), the UV-B source was maintained at a fixed distance of 45, 32, 24, 19, and 16 cm, respectively. In total, 540 neonates were tested (10 neonates/treatment 9 3 replicates 9 3 volumes 9 5 UVR intensities, and one control group). The culture vessels were shaded with a quartz cover to allow UV-B transparency and to prevent evaporation during UV-B exposure. Thereafter, the survival of rotifers was checked every half hour under a stereomicroscope until each individual of every cohort died. The standard for evaluating the death of rotifers in the experiment is the stop of cilia movement and visceral peristalsis. Then the LD 50 values were, respectively, derived following the probit method (Finney, 1971).

Life history experiment
According to the lethal effect assay, to ensure that the rotifer can complete the whole life history, the radiation intensity was set as 0.01 mW/cm 2 , so the radiation dose in this experiment was 0, 0.012, 0.024, 0.036, 0.048, 0.060, 0.072, and 0.084 kJ/m 2 (0, 2, 4, 6, 8, 10, 12, and 14 min radiation duration, respectively, each day). After preculture of one month at 28°C, the neonates (less than 6 h old) were separated indiscriminately and transferred into each well of 1-ml 24-well culture plate (working volume, 0.5 ml EPA with 1.0 9 10 6 cells/ml of S. obliquus). The 24 individuals were inspected for each radiation dose, so 384 neonates in total were prepared and then exposed to UV-B radiation. After UVR treatment, we checked the rotifers every 12 h during the first two days, followed by observation every 6 h until each infant grow into an adult and produced the first offspring. Then they were examined every 12 h until the end of experiment. Meanwhile, the time and number of the offspring produced and the death time of female adult were recorded. During the life table experiment, the surviving mature females were exposed to UV-B radiation at the same time every day, observed and transferred to clean culture plates with fresh food and medium, and the counted neonates were removed.

Population growth
In order to enable the rotifer population to grow smoothly, the radiation intensity was set to 0.02 mW/ cm 2 , and the UVR dose was 0 (control), 0.012, 0.024, 0.048, 0.096, 0.192, and 0.384 kJ/m 2 (0, 1, 2, 4, 8, 16, and 32 min radiation duration, respectively, each day). Before the formal experiment, the rotifer population was precultured at 28°C for one month. After that, 252 alive neonates (less than 6 h old) were collected and placed equally into 21 8-ml glass jars (7 treatments 9 3 replicates) containing 6 ml of EPA medium with 1.0 9 10 6 cells/ml of algae food. These organisms were exposed to UV-B radiation at the same time every day until the end of experiment. To avoid the disadvantageous effects of UVR on algae cells, S. obliquus at the density of 1.0 9 10 6 cells/ml was fed to rotifers after the radiation treatment once a day. The rotifers were maintained in a 28°C incubator without light and counted once every day before the radiation treatment in the first few days, while sampling counted when the population is large.
Determination of catalase and superoxide dismutase activity The radiation dose was designed to be 0 (control), 0.36, 0.72, 1.44, and 2.16 kJ/m 2 at the intensity of 0.02 mW/cm 2 . To meet the demand for detecting the enzyme activity, adequate numbers of rotifer were necessary, and 90 50-ml beakers (& 3000 individuals in 30-ml culture volume) were dealt with in total (6 beakers/treatment 9 5 treatments 9 3 replicates). After preculture as stated above and starvation for one day, rotifers were exposed to the UVR (0, 0.5, 1, 2, and 3 h radiation duration, respectively). Then the rotifers were sampling counted and filtered rapidly using a plankton net (mesh size, 20 lm), washed several times with double distilled water, centrifuged, and immediately froze at -80°C for use within 10 days. The rotifers on ice thawed gradually in a temperature gradient were homogenized by ultrasonication and centrifuged at 10,0009g for 10 min at 4°C. The supernatant containing the enzyme was collected for the enzymatic assay according to the protocols (SOD by WST-1 method: Cat. No. A001-3; CAT by visible spectrometry method: Cat. No. A007-1; both manufactured by Nanjing Jiancheng Bioengineering Institute, China). The SOD and CAT activities were then measured at the absorbance of 450 nm and 405 nm using an enzyme-labeled meter at 25°C. The soluble protein content in R. rotatoria was measured using Pierce TM BCA Protein Assay Kit (Cat. No. 23227, Thermo Fisher Scientific) according to the protocol direction.

Data analysis
Statistical analysis was performed using SPSS19.0 software. All data were tested for normality using the one-sample Kolmogorov-Smirnov procedure. The homogeneity of variances was checked using Levene's test. One-way analysis of variance (ANOVA) and residual analysis were conducted to identify the significant effects of UVR on the lethal effects, life history parameters in rotifer, and multiple comparisons were conducted using Student-Newman-Keulsa (SNK) to identify which groups were significantly different among different radiation doses, and the significance level was corrected by the formula a 0 = a/m, of which a = 0.05 and m is the number of simultaneously tested hypotheses according to the Bonferroni adjustments (Morgan, 2007;Chen et al., 2017). Consequently, regression analysis was performed on the relationships of the dose-response.
The durations of juvenile period (JP, the time between a neonate and that producing the first offspring), reproductive period (RP, the time between an adult producing the first offspring and the last offspring), longevity, and offspring of rotifers grown at different doses of UV-B radiation were calculated depended on the recorded data. In the population growth experiment, the population growth rate was calculated using the formula, r = ln N t -ln N 0 /t, where N 0 is the initial population density (2 ind./ml), and N t is the population density at time t in days (Krebs, 1985).

Results
Under different intensities of UV-B radiation, all treatments caused lethal effects on R. rotatoria, and the time for the rotifers to die as well as all the rotifers have died moved in advance with the increasing of radiation intensity. The multiple comparisons showed that the radiation duration at the half death of rotifers (semi-lethal exposure time, LT 50 ) decreased significantly with the enhancing of radiation intensity at the same culture volumes, which indicated that the rotifers are more sensitive to the high intensity of UVR. While comparing the LD 50 in terms of dose, the regularity in lethal effects was not obvious. The highest and lowest LD 50 of rotifers were 2.5603 and 1.8021 kJ/m 2 in the culture volume 0.5 ml, respectively, while they were 3.2774 and 2.2321 kJ/m 2 for 6 ml. For these two culture volume, both of the highest LD 50 occurred under the weakest radiation intensity (0.01 mW/cm 2 ). When the culture volume was 30 ml, the highest and lowest LD 50 of rotifers both were higher (4.5305 and 3.3115 kJ/m 2 , respectively). As the culture volume increases, the lethal effect of UVR on rotifers was weakened, and the LT 50 and LD 50 of rotifers increased at the same radiation intensity (Fig. 1).
The one-way ANOVA showed that all life table parameters in R. rotatoria (JP, RP, longevity, and offspring) were affected significantly by the UV-B radiation treatments (P \ 0.001) ( Table 1). By multiple comparisons, the rotifers delayed their first reproductive time (JP) and shortened their reproductive period (RP) and longevity with the increasing of radiation dose. The fecundity (offspring) was significant inhibited by UV-B radiation (Supplementary  Table S1). Among them, the no observed effect dose (NOED) and lowest observed effect dose (LOED) were 0.024 and 0.036 kJ/m 2 in terms of the JP and RP, respectively, while the LOED of the longevity and offspring was 0.012 kJ/m 2 without NOED. By regression analysis, the significant dose-response relationships between the UV-B radiation and life table parameters were established with linear regression (Fig. 2). To determine whether or not a linear regression model is appropriate for the data and the reliability of data, the residual analyses were performed for each life history parameters (Supplementary Table S2-S6, Fig. S1-S8).
Throughout the experimental period, the agespecific survivorships (l x ) declined earlier after different doses irradiation treatment compared with the control group that means the time for the rotifers to die was advanced. At the radiation-free condition, the rotifers began to die on the 14th day and died entirely on the 36th day. As comparison, the rotifers started to decline on the 11th, 5th, 6th, 5th, 5th, 4th, 4th day at 0.012, 0.024, 0.036, 0.048, 0.060, 0.072, and 0.084 kJ/ m 2 , then these groups survived for another 35 days, 41 days, 35 days, 31 days, 21 days, 23 days, and 13 days, respectively.
With regard to the age-specific fecundities (m x ), the reproduction peak of the rotifers was 1.63 at 4th day for the control group, while the other peaks were 1.42, 1.21, 0.92, 0.78, 0.45, 0.44 and 0.29 at 4th, 4th, 5th, 6th, 6th, 7th, and 8th day, respectively, which indicated the occurrence of these peaks delayed gradually and the peaks decreased with the strengthening of UV-B radiation (Fig. 3).
During the first 4 days of the experiment, there was no significant difference in population density between the treatment and control groups. However, with the extension of the irradiation duration, the population densities exposed to the radiation dose of 0.048 kJ/m 2 and 0.096 kJ/m 2 were much lower than that of the control group, and from the 16th day, the population density of the rotifers in the 0.012 kJ/m 2 UVR treatment was higher than that of the control group. When the experiment was carried out on the 40th day, the entire population of the 0.096 kJ/m 2 treatment group was extinct. Since the treatment groups at the highest radiation dose (0.192 kJ/m 2 and 0.384 kJ/m 2 ) did not increase and all died on the 11th day, the processing of the experimental data did not include the two groups (Fig. 4).
In addition, the UV-B radiation had a significant effect on the maximum population density of the rotifers (P \ 0.001). The maximum population density of rotifers in the 0.012 kJ/m 2 treatment group was the highest, reaching 1176 ind./ml. Compared with the control group, there was no significant difference in the maximum population density of the rotifers in the 0.024 kJ/m 2 treatment group, and the maximum population densities of the two groups with the higher radiation dose (0.048 kJ/m 2 and 0.096 kJ/m 2 ) were much lower than the control group (Fig. 5a). As the radiation dose increased, the population growth rates of the treatment groups gradually decreased and were smaller than the control group (Fig. 5b).
After treatment with different doses of UV-B radiation, the superoxide dismutase activity in rotifers was significantly higher than that of the control group (P \ 0.05). With the increase of radiation dose, the activity of SOD enzyme increased first and then decreased. When the radiation dose was 0.72 kJ/m 2 , 0.5ml-LT50 6ml-LT50 30ml-LT50 0.5ml-LD50 6ml-LD50 30ml-LD50 Fig. 1 The semi-lethal time (LT 50 ) and dose (LD 50 ) of R. rotatoria in different UV-B radiation intensities and culture systems (Mean ± Standard Error, SE) JP the durations of juvenile period, RP the durations of reproductive period, SS sum of square, df degrees of freedom, MS mean square, F ratio of mean squares, p p values the SOD activity was the highest, and the peak was 66.35 U/mgprot, and it was significantly different from other experimental groups (P \ 0.05) (Fig. 6a). After treatments with low doses of UV-B radiation (0.36 kJ/m 2 and 0.72 kJ/m 2 ), there was no significant difference in catalase activity between the treatments and the control group (P [ 0.05). However, with the further increase in radiation dose, higher doses of UV-B radiation (1.44 kJ/m 2 and 2.16 kJ/m 2 ) significantly weakened the activity of the CAT enzyme. When the radiation dose was 0.72 kJ/m 2 , the CAT activity was the highest with a peak of 10.44 U/mgprot (Fig. 6b).

Discussion
UV-B radiation is an environmental stressor for almost all aquatic trophic levels, from primary producers, zooplankton, crustaceans, amphibians, corals, to fishes (Day & Neale, 2002;Hansson & Hylander, 2009;Kim et al., 2011;Vitt et al., 2020).The effects of UV-B may not only act at the micro-level like inducing DNA mutation and altering enzyme activity, but also at the phenotypic attributes including affecting organismal survival, growth, motility, photosynthesis, and reproduction (Häder, 2000;Dahms & Lee, 2010). Therefore, UV radiation is a potential driving force for zooplankton community structure and population  (Häder et al., 2007). In the present study, a coincident conclusion showed that the survivorship of R. rotatoria was adversely affected by the UV-B radiation. The highest value of 24 h-LD 50 measured by the acute toxicity test was 4.5305 kJ/m 2 with the radiation intensity of 0.03mW/cm 2 in the 30-ml test volume. The 24 h-LD 50 value of UV-B has been reported for a variety of studies. For example, similar to our findings, Feng et al. (2006) found that the 24 h-LD 50 value of B. plicatilis (Muller, 1786) and B. urceus (Linnaeus, 1758) was 4.393 kJ/m 2 and 5.856 kJ/m 2 , respectively, in the radiation intensity of 0.05 mW/cm 2 . Li et al. (2006) also evaluated the 24-LD 50 value of adult males of Schmacheria inopinus (Burckhardt, 1913) was 5.77 kJ/m 2 , as well as the 48 h-LD 50 value of adult females was 5.04 kJ/m 2 . However, a much higher 24 h-LD 50 was reported for B. koreanus (Hwang, Dahms, Park & Lee, 2013), with a value as high as 24.6 kJ/m 2 in 4-ml working volume (no radiation intensity displayed) (Kim et al., 2011). Such differences may further attribute to the species specificity, individual ages and physiological status, and other processes which could regulate the responses of antioxidant system and repair mechanisms to UVR injuries (Hecox-Lea & Mark Welch, 2018). The effects of UV-B on organisms may be affected by the difference in experimental conditions, such as UV-B wavelengths, ultraviolet intensities, and culture system volume. The semi-lethal time (LT 50 ) of the copepod Calanus sinicus (Brodsky, 1965) was 30.47 h, 2.86 h, and 1.96 h at the radiation intensity of 0.2mW/cm 2 , 0.3mW/cm 2 , and 0.5mW/cm 2 , separately (Tao, 2005). Consistent with these results, the radiation duration within which approaching to the half death of R. rotatoria decreased significantly with the increasing of radiation intensity at the same culture volumes in this study, which indicated that the rotifers are more sensitive to the high intensity of UVR. In addition, the persistence of tolerance (evaluating by LT 50 ) in rotifer to stress was playing a more vital role than the radiation dose (LD 50 ) in survival. As the culture volume increases, the lethal effect of UVR on rotifers was weakened, which could due to the variety of UV radiation transmission for different working volumes.
During the last few decades, a growing cognition considering the organism as an adapted complex has increased awareness of adaptive evolution not only at the biochemical, physiological, and morphological level but also at the life history level (Wilbur et al., 1974). Life history trait, like all other phenotypic attributes, represents a suite of plastic components in a specific environment and can be seen as compromises to various investments in growth, reproduction, and survivorship. With the tactics of trade-off between growth and reproduction, and quantity and quality of offspring, organisms may maximize the benefits by allocating limited resources and energy towards growth, maintenance, reproduction, raising offspring to independence and avoiding death, even under good conditions (Norgan et al., 2012). So these trade-offs are keys to understanding the diversity of life histories, the pattern of population dynamics, the ecological strategies, and evolutionary adaptation of living beings to changing environments in the field (Bednekoff, 2010;Martin & Bize, 2018).
The present study was carried out to explore the effects of UV-B radiation on the life history of the rotifer and further inspect whether there are trade-off strategies among life historic components. From the results, the fecundity and survivorship of rotifers were negative affected remarkably by UVR treatment. Compared with the control group, the fecundity of rotifers exposed to UV-B radiation was significantly decreased, which was validated by the cumulated number of offspring and the age-specific fecundities (m x ). The greater the radiation dose, the more obvious the inhibitory effects. Our results are consistent with some previous studies which indicated exposure to UV radiation had a significant effect on the abundance and/or reproduction of four rotifers, two cladocerans, Fig. 6 The enzyme activities of SOD (a) and CAT (b) after the UV-B radiation treatment (Mean ± SE). Note SNK-q multiple comparison; Letters (a, b, c, and d) represent the significance of differences among treatment levels, respectively; Treatments with the same letter are not significantly different, whereas treatments with different letters are significantly different and one copepod (Persaud & Williamson, 2005), and UV-B effectively inhibited B. calyciflorus (Pallas, 1766) reproduction and reduced ingestion by up to 90% (Preston et al., 1999). Possibly, the reproductive system of rotifers could be destroyed by the high dose of UV-B radiation. Alternatively, animals may have to invest more energy to maintain basal living processes to ensure survivorship, which in turn comes at the cost of reductions in reproduction. In addition, the rotifers in this study prolonged their first reproductive time (JP) and shortened the longevity with the increasing of radiation dose, which also could be the key factor causing the decrease of reproduction. In the experiments about the effects of the thiophanate-methyl on the reproduction and survival in B. calyciflorus, as well as the studies for impacts of the deltamethrin on experimental population dynamics of B. calyciflorus (Xi & Hu, 2003;Xu et al., 2005), the extension of juvenile period was regarded as the major cause resulted in lower m x . This is in line with Pourriot (1986), who considered that the m x more depended on the duration of juvenile period and embryonic development during the period of parthenogenetic reproduction in rotifers, rather than R 0 . As the strategy of trade-off, the rotifers have to prolong their reproductive duration at the low dose of radiation (0.012 kJ/m 2 ) as a response to reduced reproduction, while shorten their reproductive period (RP) with increasing of radiation dose, which resulted in the phenomenon that the end time of reproduction increased firstly and then decreased.
In the population growth experiment, the rotifers all died at the highest radiation dose (0.192 kJ/m 2 and 0.384 kJ/m 2 ), which suggested high UV radiation has significant lethal effect, by probably causing the DNA damage and cell degradation Kim et al., 2011). On the 16th day, the population density under the low UVR dose of 0.012 kJ/m 2 began to be higher than that of control group, and similarly, the maximum population density in R. rotatoria was highest at 0.012 kJ/m 2 and then decreased significantly with increasing UV-B radiation dose, which suggested that low doses of UV-B radiation can stimulate the reproduction of rotifers to some degree. However, high doses of radiation have different levels of inhibition on rotifers. The stimulation effects that were explained as hormesis are also occurred in zooplankton under the other stress (Fang, 2013;Sha, 2015). Low dose of toxic chemicals below the damage threshold can stimulate the growth of organisms and triggers physiological regulation to enter metabolic stasis in response to severe environmental stress. Further studies are needed about the specific biological mechanisms (Stebbing, 1982;Ricci & Perletti, 2006).
Recently, it has been proposed that oxidative stress is the mediator of trade-offs between survival and reproduction. Under normal environmental conditions, oxidative stress can be induced endogenously by reproduction, resulting in reduced survival as a cost. Alternatively, exogenous oxidative stress generated under adverse conditions will decreased the reproduction for having to invest more resources into somatic maintenance, such as the protection and repair of biomolecules damaged by overproduced ROS derived from oxidative attack, which should enhance survival and longevity, but at the expense of reduced fecundity and population growth (Latta et al., 2019). With the long-term evolving, organisms have developed a set of integrated protection system, that is, the enzymatic antioxidant defense system, SOD and CAT are the key members involved in this mechanism, which can be used to detoxify and remove excessively intracorporeal ROS against oxidative stress (Vega & Pizarro, 2000;Barata et al., 2005;Rautio & Tartarotti, 2010;Snell et al., 2012;Köhler et al., 2017). Theoretically, for counteracting the oxidative nature of peroxides and other radicals in response to diverse environmental stressors, organisms most certainly upregulate various antioxidases to decrease the possible damage caused by adversity (Borgeraas & Hessen, 2000;Rautio & Tartarotti, 2010).
In the present study, the two enzymes in the R. rotatoria have the coincident response to UVR stress with a pattern of rising first and then falling. The enzyme SOD has higher level of content and more sensitive to low UVR than CAT. The similar results also present in the phytoplankton under the UVR stresses (Abo-Shady et al., 2008). So, it follows that the antioxidant system plays a very important role when exposed to adverse stress, and the repairing effects occur as the positive response to low dose of UVR, while the enzyme activities decline with the increasing of radiation dose, which could be attributed to the damage of enzymes to varying levels. Rautio & Tartarotti (2010) also found a negative relationship between CAT and solar radiation which indicated this enzyme was inhibited or inactivated by UVR. The fluctuating patterns of antioxidant enzyme activity can reveal the ability of various organisms to cope with environmental stress to a certain extent.
In summary, there were significant responses of the survival, fecundity, duration of development, and the antioxidant enzyme system in R. rotatoria to UV-B radiation in different intensities and doses. The lethal effects of UV-B radiation to organisms depend not only on the conditions they exposed to, like as intensity and time of exposure, but also combination of factors namely, the type and effectiveness of the strategy they employ to cope with the changed environment. The species specificity, individual ages, and physiological responses also could be the regulating factors under the UV-B stresses, and also in this case, we proposed that the strategy of energy trade-off between reproduction and survival in rotifers might play a vital role. At low dose of UVR, rotifers defend against the radiation stress by increasing the antioxidant enzyme activities, while high doses of radiation have significant inhibition effects on rotifers.