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Environmental Science and Pollution Research

, Volume 26, Issue 3, pp 2908–2917 | Cite as

Effects of long-term 4-nonylphenol dietary exposure on reproductive ability of Japanese quails (Coturnix japonica)

  • Yan Cheng
  • Zhengjun Shan
  • Junying Zhou
  • Yuanqing Bu
  • Pengfu LiEmail author
  • Shan LuEmail author
Research Article
  • 67 Downloads

Abstract

As an endocrine disruptor, 4-nonylphenol (4-NP) is widespread in the environment. Here, we investigated the effect of long-term 4-NP dietary exposure on Japanese quails (Coturnix japonica). A total of 72 quails were evenly divided into 24 cages (12 cages for the reproductive toxicity study and 12 cages for the histopathology study, with one male quail and two female quails in each cage) and fed with various doses of 4-NP in diet. The body weight in quails administered with 4-NP was significantly decreased (P < 0.05) in a time- and dose-dependent manner. The egg fertilization rate significantly decreased (P < 0.05) in all treated groups, which was 91.4%, 86.5%, 85.4%, and 86.2% in the control group, 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups, respectively. Moreover, the hatching rate was also significantly decreased (P < 0.05) in the 50 mg·kg−1 treatment group compared with the control group. Furthermore, the 14-day survival rate of young quails was significantly decreased (P < 0.05) in all treated groups, which was 98.0%, 91.1%, 89.8%, and 86.8% in the control group, 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups, respectively. Damaged spermatogenesis in male quails was found in all treated groups. In conclusion, oral administration of 4-NP impaired the gonads of male quails, leading to reproduction performance damage of Japanese quails.

Keywords

4-Nonylphenol Coturnix japonica Reproductive ability Toxicity 

Introduction

Nonylphenol (NP), which is a mixture of isomers, primarily 4-NP, arises mainly from biodegradation of NPEOs. As non-ionic surfactants with emulsifying, moisturizing, decontamination, and emulsion-disrupting actions, NPEOs are widely used in pesticides and other industrial applications. According to the survey conducted by Bu et al. (2014), the contents of adjuvants like NPEOs in the formulation of pesticides always range between 1 and 99%, with the average content of about 70%. The widely use of pesticides thus results in the relatively high concentrations of NP in the environment (Lu and Gan 2014; Roig et al. 2014).

Currently, lots of studies reported the influence of pesticide active ingredients on environmental organisms, while less attention has been paid to the effects of the adjuvants and their metabolites. As an important degradation product of NPEOs, studies have shown that NP has toxicity to fish, crab, shrimp, daphnia, rats, silkworms, and birds (Jager et al. 1999; Kinnberg et al. 2000; Lahnsteiner et al. 2005; Lye et al. 2008; Preuss et al. 2008; Yuan et al. 2013; Nishijima et al. 2003; Oshima et al. 2012; Roig et al. 2014; Razia et al. 2005, 2006; Yoshimura et al. 2002). And from the literature review, we can see that most of the current studies on birds employ direct injection of NP into the egg yolk or egg white with the aims to investigate the effect of NP on the development of the birds’ reproductive organs before their sex differentiation (Nishijima et al. 2003; Oshima et al. 2012; Razia et al. 2006; Roig et al. 2014) except the study conducted by Fujita et al. (2004) fed 1 or 2 mg of NP in corn oil to 7-day-old female Japanese quails once a day to examine the appearance of ingested nonylphenol in the blood, liver, and egg yolk. But in Fujita’s study, the exposure lasts only for 5 days and the research emphasis was put on the distribution of NP in vivo after ingestion but not the effects.

Birds are important in the environment, and they are exposed to hazardous and toxic substances such as pesticides through feeding, drinking, and breathing. While the exposure routes adopted in current studies of NP on birds are destructive and unrealistic. In order to mimic the actual exposure of pesticides to birds, in the present study, we fed the test birds with food treated by NP and aimed to explore the effects of long-term NP exposure by ingestion on the reproductive ability (i.e., egg production and sex determination) of Japanese quails (Coturnix japonica), providing a scientific reference for the environmental safety management of this widespread endocrine disruptor.

Materials and methods

Materials

4-NP (CAS, 104405, 98%) was purchased from Sigma (USA). C. japonica was supplied from Baojun Quail Breeding Center (Nanjing, Jiangsu, China). Quail diet, including diet for young quail, diet for adult quail, and diet for egg production, was also provided by Baojun Quail Breeding Center (Nanjing, Jiangsu, China).

Methods

The test was conducted according to the OECD test guideline 206: avian reproduction test, in order to determine the effects of a substance administered with food on the reproductive ability of birds (1984). In this test, a total of 100 eggs from the same batch were selected and incubated at 37.5 °C in a constant humidified (RH 70%) incubator (Ruipu Incubation Equipment Co. Ltd., Nanjing, Jiangsu, China). In order to exclude any deformed, abnormal, sick, or injured quails, the nestling quails hatched on the same day were fed and examined before starting the experiments. Healthy quails were randomly assigned to each treatment group. All quails were 14-day-old at the start of the experiments. Quails were housed indoors to avoid any potential interference from the external environment.

In order to mimic the realistic exposure of birds to pesticides or pesticide adjuvants, the dose of 4-NP was determined according to the results of Fletcher et al. of which the pesticide residues in different food of birds were in the range of 15~240 mg·kg−1 (Fletcher et al. 1994). The control group was fed with the basic diet only (cage numbers 1–3). Three treatment groups were set up as follows: 10 mg·kg−1 4-NP group (cage numbers 4–6), 20 mg·kg−1 4-NP group (cage numbers 7–9), and 50 mg·kg−1 4-NP group (cage numbers 10–12). Each cage (50 cm × 40 cm × 35 cm) consisted of three quails (including one male quail and two female quails), making a total of 36 quails (12 male quails and 24 female quails) in the 12 cages. In addition to the three cages for the reproductive toxicity study, another three cages of quails were needed for each group (one male and two females per cage) for the histopathology study on gonads. The test quails were randomly assigned to each cage. Table 1 illustrates the test procedure.
Table 1

Design of the avian reproduction test of 4-NP

Test phase

Time (week)

Requirement

Activities

Acclimation

2

Basal diet

Health check, randomly assign the test quails to each cage

Initial phase

8

Treated diet

Exposure of treatment groups to diets containing the test substance begins under 7~8-h illumination per day

Second phase

2

Treated diet

Photoperiod is manipulated to 16 to 17 h to bring the hens into laying condition

Final phase

8

Treated diet

Onset of laying, number, check, measure, and hatch the eggs

Withdraw period

3

Basal diet

Egg production decreases, withdraw of the test

Food intake was measured at weeks 1, 3, 5, 9, 11, 13, 15, 17, 19, and 21 (4-NP exposure was carried out during weeks 1–18) and recorded as g·(cage·day)−1. The body weights of the quails before entering the cage, at the beginning of egg production, and at the end of the feeding experiment were respectively recorded. The eggs were collected after 4-NP exposure for 10 weeks, and the collection lasted for 8 weeks. During this period, the following parameters were recorded: the number of eggs laid, the number of broken eggs, the number of fertilized eggs, the number of egg sets, the number of young quails hatched out, the number of surviving young quails, and the number of males and females amongst the newborn quails. From these data, the percentage of broken eggs, the fertilization rate, the hatching rate, the 14-day survival rate, and the sex ratio of the newborn quails were calculated.

Measurement of eggshell thickness

From the start of the final phase, once every 2 weeks, all eggs newly laid that day were removed and measured for eggshell thickness. Every time, three eggs (for example, No. 1, No. 3, and No. 5) per cage were taken for measurement. Eggs were opened at the widest point, the egg white and egg yolk were cleared, and the eggshell was left to dry at room temperature for more than 48 h. The thickness of the eggshell was determined at its widest point in three different spots using a caliper (resolution of 0.01 mm), and the thickness of the egg inner membrane was included in the measurement. The average value of the three measurements was regarded as the eggshell thickness.

Observation of fertilization

Eggs were observed on day 11 after incubation. Opaque eggs of a red or black color were recorded as fertilized eggs.

Determination of sexual genotype of young quails

All young quails were determined for their sexual ZZ (male) or ZW (female) genotype using a previously described method (Fridolfsson and Ellegren 1999). Genomic DNA was extracted from blood samples of the quails according to the method of Khosravinia and Murthy (Khosravinia et al. 2010).

PCR reactions were performed on a DNA Engine® Peltier Thermo Cycler (BioRad, USA) using the primers 2550F “5′-GTT ACT GAT TCG TCT ACG AGA-3′” and 2718R “5′-ATT GAA ATG ATC CAG TGC TTG-3′.” Briefly, following a DNA polymerase activation at 94 °C for 2 min, amplifications were carried out with nine cycles at a melting temperature of 94 °C for 30 s, an annealing temperature of 50 °C for 30 s, and an extension temperature of 72 °C for 1 min. Subsequently, additional amplifications were performed with 30 cycles at a melting temperature of 94 °C for 30 s, an annealing temperature of 42 °C for 30 s, and an extension temperature of 72 °C for 1 min, followed by an extra extension step at 72 °C for 5 min. PCR amplicons were separated on 2% agarose gels, and the visualized bands were photographed. All the females had a 450-bp CHD1-W female-specific fragment. The young quails of both sexes had a 600-bp CHD1-Z specific fragment.

Histological analysis of test quail’s gonads

The gonads of quails were histopathologically examined after exposure to 4-NP. The gonads of the quails in the three cages used for gonadal sample collection throughout the experiment were dissected at three different time points as follows: before exposure, after exposure, and at the end of the feeding experiment. Moreover, histopathological damage in the testis and ovary was also assessed. Part of the gonad was dissected and fixed in 4% paraformaldehyde at 4 °C overnight. Samples were dehydrated with ethanol and xylene, and embedded in paraffin, and sections of 4-μm thickness were prepared with a microtome. The sections were stained with hematoxylin and eosin, mounted and observed under the microscope.

Data analysis

Data were initially encoded in Excel software and then analyzed using analysis of variance with SPSS 19.0 (SPSS Inc, Chicago IL, USA) and LSD multiple comparison. P < 0.05 was considered statistically significant. Data were expressed as mean ± SD deviation.

Results

Effect of 4-NP on food intake and body weight of C. japonica

Figure 1 reveals that there was no significant difference in food intake between the 4-NP treated groups and the control group (P > 0.05), or between the 4-NP treated groups (P > 0.05).
Fig. 1

Effect of 4-NP on food intake of Japanese quails. Unit, g·(cage·day)−1

As described in the “Materials and methods” section, the body weight of the quails was measured at three time points: before entering the cage, at the beginning of egg production, and at the end of the experiment. For female quails, we did not observe significant differences in body weight between all groups either before the quails were placed in the cage (P > 0.05), or at the beginning of egg production (P > 0.05). However, at the end of the test, the body weight of female quails in 20 mg·kg−1 and 50 mg·kg−1 treatment groups was significantly lower than that of the control group (P < 0.05). Body weight of female quails in the 50 mg·kg−1 treatment group was also significantly different from that in the 10 mg·kg−1 treatment group (P < 0.05) (Fig. 2).
Fig. 2

The body weight variation of Japanese quails at different time points (a, female; b, male). Same letter means not remarkable difference, and different letter means remarkable difference (P < 0.05)

For male quails, we did not observe significant differences in body weight between all groups before they were placed in the cage (P > 0.05), or at the beginning of egg production (P > 0.05). In contrast, at the end of the test, the body weight of male quails in 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups was significantly lower compared with the control group (P < 0.05). However, there was no difference between treatment groups (P > 0.05) (Fig. 2). Under the condition of no significant change in food intake, the body weight of treatment groups changed after a fairy long period of exposure, suggesting that 4-NP treatment could affect the growth of the quails.

Effect of 4-NP on egg production of C. japonica

Table 2 shows the total egg production in 8 weeks during the peak egg-laying period, exhibiting that 4-NP in the diet had no adverse effect on egg production of C. japonica.
Table 2

Reproduction performance of Japanese quails in different treatment groups

Group

Cage number

Egg production1

Total amount per group

Egg cracked

Average % ± SD

eggs cracked2

Egg set3

Viable embryos

Fertility %4

Average fertility % ± SD2

Number of the embryos that liberate themselves from the eggs

Hatchability %5

Hatchability % ± SD2

14-day-old survivors

14-day-old survivors % ± SD2

Female:male ratio

Control

1

78

212

9

15.7 ± 3.8a

54

49

94.4

91.4 ± 2.9a

46

85.2

85.1 ± 0.7a

46

98.0 ± 1.7a

1.009 ± 0.098a

2

74

14

45

40

91.1

38

84.4

37

3

60

10

35

31

88.6

30

85.7

29

10 mg·kg−1

4

60

207

10

18.8 ± 4.2a

35

32

88.6

86.5 ± 2.8b

31

88.6

82.7 ± 5.8a

28

91.1 ± 0.6b

1.062 ± 0.006a

5

75

12

48

40

83.3

37

77.1

33

6

72

17

40

36

87.5

33

82.5

31

20 mg·kg−1

7

76

211

15

16.0 ± 3.2a

46

41

86.9

85.4 ± 2.9b

38

82.6

79.3 ± 2.3ab

34

89.8 ± 3.2b

1.061 ± 0.056a

8

63

9

39

32

82.1

29

74.4

27

9

72

10

47

42

87.2

38

80.9

33

50 mg·kg−1

10

80

252

17

19.1 ± 2.0a

48

43

85.4

86.2 ± 0.9b

37

77.1

74.7 ± 3.8b

32

86.8 ± 4.8b

1.084 ± 0.114a

11

75

13

47

42

87.2

36

76.6

33

12

97

18

64

55

85.9

45

70.3

37

1Egg production refers to the total egg production during the egg-laying period, which normally includes 8 weeks of laying 2In this column, same letter means no significant difference (P > 0.05), and different letter means significant difference (P < 0.05) 3Egg set = egg production − egg cracked − egg for testing eggshell thickness (15 per cage) 4Fertility % = viable embryos/egg set × 100 5Hatchability % = number of the embryos that liberate themselves from the eggs/egg set × 100

Effect of 4-NP on egg quality

The eggshell thickness was measured five times during the 8-week-long peak egg production period. Moreover, the numbers of broken eggs were also counted during this period.

During the experiment, the eggshell of treatment groups was slightly thinner than that of the control group, but the differences were not significant (P > 0.05). Furthermore, there was no significant difference between the treatment groups (P > 0.05) (Fig. 3).
Fig. 3

Effect of 4-NP on eggshell thickness

The average broken egg rates were 15.7%, 18.8%, 16.0%, and 19.1% for the control group, 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups, respectively. The broken egg rates of the treatment groups were slightly higher compared with the control group, but with no statistical significance (P > 0.05) (Table 2). In conclusion, 4-NP did not affect the quality of eggs.

Effect of 4-NP on fertilization of C. japonica

The fertilization rates of the control group, 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups, were 91.4%, 86.5%, 85.4%, and 86.2%, respectively. The fertilization rates of the treatment groups were significantly lower compared with the control group (P < 0.05). However, there was no significant difference between treatment groups (P > 0.05) (Table 2). Therefore, 4-NP dietary exposure reduced the fertilization rate of C. japonica.

Effect of 4-NP on hatching of C. japonica

The hatching rates of the control group, 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups, were 85.1%, 82.7%, 79.3%, and 74.7%, respectively. The 50 mg·kg−1 treatment group had a significantly lower hatching rate than the control group (P < 0.05) and the 10 mg·kg−1 treatment group (P < 0.05), but the difference between other groups was not significant (P > 0.05) (Table 2). Therefore, long-term 4-NP dietary exposure could affect the hatching rate of the eggs.

Effect of 4-NP on survival of the newborn C. japonica

The 14-day survival rates of the newborn quails in the control group, 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups, were 98.0%, 91.1%, 89.8%, and 86.8%, respectively. There were significant differences between the treatment groups and the control group (P < 0.05) (Table 2), suggesting that 4-NP dietary exposure could reduce the offspring survival rate of C. japonica.

Effect of 4-NP on sex ratio of the newborn C. japonica

The female/male ratios were 1.009, 1.062, 1.061, and 1.084 in the control group, 10 mg·kg−1, 20 mg·kg−1, and 50 mg·kg−1 treatment groups, respectively. There was no significant difference between all the groups (P > 0.05) (Table 2), indicating that the sex ratio of the offspring was not affected by ingestion of 4-NP.

Effect of 4-NP on the gonadal tissue of C. japonica

Figures 4, 5, and 6 show the tissue pathology of male quail gonads at three time points: pre-exposure, post-exposure, and at the end of the experiment, respectively.
Fig. 4

Pathological observations on the testis of male Japanese quails before exposure to 4-NP. a Control (normal). b Diet 10 mg·kg−1 (normal). c Diet 20 mg·kg−1 (normal). d Diet 50 mg·kg−1 (normal). Black arrows indicate seminiferous tubule wall, and yellow star indicates lumen of the seminiferous tubule

Fig. 5

Pathological observations on the testis of male Japanese quails at the end of exposure to 4-NP. a Control (normal). b Diet 10 mg·kg−1 (black arrow indicates attenuation of the seminiferous tubule and slight reduction of spermatogenesis). c Diet 20 mg·kg−1 (black arrow notes slight reduction of spermatogenesis). d Diet 50 mg·kg−1 (slight reduction of spermatogenesis, and blue arrows note shed spermatogenic cells within the lumen)

Fig. 6

Pathological observations on the testis of male Japanese quails at the end of experiment. a Control (normal). b Diet 10 mg·kg−1 (black arrows note slight reduction of spermatogenesis, and blue arrows note shed spermatogenic cells within the lumen). c Diet 20 mg·kg−1 (black arrows note slight reduction of spermatogenesis). d Diet 50 mg·kg−1 (black arrows note slight reduction of spermatogenesis, and blue arrows note shed spermatogenic cells within the lumen)

Figures 7, 8, and 9 show the tissue pathology of female quail gonads at the above-mentioned time points. Prior to 4-NP treatment, testicle tissues of male quails were normal. However, after 4-NP treatment and at the end of the experiment, spermatogenesis in the seminiferous tubules was reduced in male quails. Germ cell shedding was observed in the lumen, suggesting that 4-NP affected spermatogenesis in the male testicle. However, no pathological lesions were found in the ovaries of female quails before 4-NP exposure, after 4-NP exposure, or at the end of the experiment.
Fig. 7

Pathological observations on the ovary of female Japanese quails before exposure to 4-NP. a Control (normal). b Diet 10 mg·kg−1 (normal). c Diet 20 mg·kg−1 (normal). d Diet 50 mg·kg−1 (normal)

Fig. 8

Pathological observations on the ovary of female Japanese quails at the end of exposure to 4-NP. a Control (normal). b Diet 10 mg·kg−1 (normal). c Diet 20 mg·kg−1 (normal). d Diet 50 mg·kg−1 (normal)

Fig. 9

Pathological observations on the ovary of female Japanese quails at the end of experiment. a Control (normal). b Diet 10 mg·kg−1 (normal). c Diet 20 mg·kg−1 (normal). d Diet 50 mg·kg−1 (normal)

Discussion

For test quality control, OECD 206 (1984) provides some standards that need to be met in the untreated control group. In this study, each measurement was in line with the requirements of the OECD quality control test, suggesting valid and reliable test results.

Nishijima et al. (2003) found that continuing incubation of the broken egg embryos after direct exposure to 4-NP results in impaired development and reduced body weight. Body weight losing of the test quails after exposure to 4-NP was also observed in the present study. Roig et al. (2014) injected 0.1–50 μg·egg−1 of 4-NP, which is equivalent to environmental concentrations, into the yolks of chicken embryos. They found that at doses less than 10 μg·egg−1, the intraluminal seminiferous surface area is reduced by 64.1%. Oshima A et al. (2012) injected 0.2, 2, 20, and 200 μg·egg−1 of 4-NP into the egg white of quails. After incubation for 16 days, they dissected all the embryos and found that the male quails showed feminization with their left testicles turning into ovaries. Nishijima et al. (2003) also found that male embryos showed enlarged gonads and feminization, evidenced by an increase in female-specific enzymes. Cheng et al. (2017) investigated the effect of 4-NP on reproduction ability of Japanese quail by administrating 4-NP in drinking water, and found gonad impairment of male quails. Although feminization was not observed in our study, spermatogenesis was affected in male quails, confirming that as a chemical with estrogenic activity, 4-NP could induce impairment in gonads of male quails when using either unrealistic exposure method, injection, or realistic exposure conditions, drinking water or dietary exposure. In our study, 4-NP dietary exposure for 18 weeks caused weight loss and reduced fertilization rate, hatching rate, and 14-day newborn quail survival rate, adding more evidence on the reproduction toxicity effects of 4-NP on birds. As to the mechanism, Ishihara et al. (2003) studied the effect of endocrine-disrupting chemicals, including medical, industrial, and agricultural chemicals, on triiodothyronine (T3) binding to purified transthyretin (qTTR) and the thyroid hormone receptor β ligand binding domain (qTR LBD) of Japanese quails. Their results indicated that 4-NP effectively blocks the binding of T3 and qTTR. In Roig’s study (2014), an impairment of liver development with an abnormal bile spillage was observed at a higher concentration of 4-NP (50 μg·egg−1) and a heterogeneous organization of the renal tubules occurred. In many other studies, thymus, kidneys, and other organs of the quails were found to be damaged by nonylphenol exposure (Hanafy et al. 2007; Razia et al. 2005; Sakimura et al. 2002). As the effects of 4-NP on birds are complex, the underlying mechanism should be explored by further investigation.

Conclusions

In the present study, we investigated the reproductive toxicity of 4-NP to C. japonica after 4-NP dietary exposure for 18 weeks. The results showed that 4-NP could induce damaged spermatogenesis in male quails, cause weight loss and reduced fertilization rate, hatching rate, and 14-day newborn quail survival rate.

Notes

Funding

This work was supported by the Special Fund for Environmental Scientific Research in the Public Interest (grant no. 2013467026).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Not applicable.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Life SciencesNanjing UniversityNanjingChina
  2. 2.Nanjing Institute of Environmental ScienceMEPNanjingChina

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