Response Of The Reproductive Function In Male Tree Sparrow To Environmental Heavy Metal Pollution

Heavy metals are known to easily accumulate in food chain,have long biological half-lives and hard to be degraded,which could enter the body of animals via many routes including inhalation,ingestion and skin contact,then cause serious health problems.Studies have revealed that heavy metals could affect male reproductive function,one of the determinants of reproductive success,through impairing reproductive organs,disturbing reproductive hormone levels or directly affecting sperm quality.Birds are valued elements of the natural world,whose declining populations partly caused by environmental pollution.Anyway,little research attention has been paid to the response of reproductive function in wild male birds to environmental heavy metals.In the present study,tree sparrow(Passer montanus),a resident bird species in northwest China,was selected as the study object.Two plots,Baiyin(BY)and Liujiaxia(LJX),with absolutely different heavy metal pollution were selected as the sampling sites.BY was an experimental area mainly polluted by copper(Cu),zinc(Zn),lead(Pb)and cadmium(Cd),while LJX was a relatively unpolluted plot.During breeding season of tree sparrows,alterations of reproductive function in males were investigated systematically considering their body condition,testicular structure and function,reproductive hormones levels and sperm quality under environmental heavy metal pollution.The results would provide reference for exploring changes in reproductive output of wild birds exposed to environmental heavy metals.The results were shown as follows:1.Enrichment levels of environmental heavy metals in male tree sparrows.The results showed that Cd concentrations in liver,muscle,primary feather,breast feather and testes,Cu and Pb concentrations in primary feather,as well as Pb concentrations in breast feather of male tree sparrows from BY were significantly higher than those from LJX(P < 0.05).These results suggested that Cd,Cu and Pb significantly accumulated in male tree sparrows under environmental heavy metal pollution.2.Effect of environmental heavy metal pollution on body condition of male tree sparrows.The results showed: body size of male tree sparrows from BY was significantly smaller than those from LJX(P = 0.002);coefficients of heart,kidney or lung in male tree sparrows from BY were not significantly different compared to those from LJX(P > 0.05),while liver coefficient was higher for males from BY(P < 0.001).These results indicated that body size of male tree sparrows exposed to environmental heavy metal pollution decreased and their liver coefficient increased,suggesting the liver of male tree sparrows was more sensitive to environmental heavy metal exposure.3.Effect of environmental heavy metal pollution on testicular structure and function of tree sparrows.The results showed: there was no significant difference in testis size,testis histological structure or activity of marker enzymes of testicular function between the two study sites(P > 0.05);however,superoxide dismutase(SOD)activity and malondialdehyde(MDA)level in testes of tree sparrows from BY were significantly lower than those from LJX(SOD,P = 0.019;MDA,P = 0.004),while the total antioxidant capacity(T-AOC)and apoptosis level in testes were higher compared to the LJX population(T-AOC,P = 0.012;apoptosis level,P = 0.001).These results suggested that the development and metabolism of testes in tree sparrows were not evidently affected under environmental heavy metal pollution,however,lipid peroxidation level in testes decreased,and antioxidant defense and apoptosis level in testes elevated.4.Effect of environmental heavy metal pollution on reproductive hormones levels in male tree sparrows.The results showed that male tree sparrows from BY had higher plasma levels of estrogen,luteinizing hormone(LH)and follicle-stimulating hormone(P < 0.001),and no significant difference was observed in plasma level of testosterone(P = 0.917).These results suggested that reproductive hormones levels were increased in male tree sparrows under environmental heavy metal pollution.5.Effect of environmental heavy metal pollution on sperm quality of tree sparrows.The results showed: no difference was observed in sperm quantity or sperm ATP concentration between the twp populations(P > 0.05);compared to the LJX population,tree sparrows from BY produced longer sperm with longer flagella(P < 0.05),in addition to sperm with smaller head/flagellum ratios,and their among-male coefficient of variation in total sperm length and percentage of the abnormal sperm or the sperm with abnormal head were lower(P < 0.05);sperm velocity,percentage of progressive sperm,as well as sperm linearity,wobble and straightness of tree sparrows from BY were significantly higher than those from LJX(P < 0.05),and the percentage of immotile sperm was lower than the LJX population(P = 0.016);sperm velocity was negatively correlated with sperm head length and head/flagellum ratio in the BY population(P < 0.05),but no significant relationship was observed between sperm velocity and total sperm length or sperm flagellum length in both the populations(P > 0.05).In addition,a negative relationship was found between sperm flagellum length and ATP concentration in the BY population(P = 0.040),and similar relationship was observed between sperm ATP concentration and sperm velocity in both the LJX and the BY populations(LJX,P = 0.008;BY,P < 0.001).These results suggested that sperm morphology and sperm swimming ability of tree sparrows showed positive variations under environmental heavy metal pollution,and males increase sperm flagellum length to decrease head/flagellum ratio to achieve higher sperm velocity.6.Relationship between heavy metal concentrations in testes of male tree sparrows and their reproductive function.The results showed: a significant relationship was observed between testis size and Cu or Cd concentration in testes of tree sparrows(P < 0.05),and testis coefficient and volume decreased with the increase of heavy metal levels;Pb level in testes significantly inhibited SOD activity in testes(P = 0.043);a negative relationship was observed between Zn concentration in testes and plasma level of estrogen(P = 0.046);percentages of the abnormal sperm and the sperm with abnormal head decreased with increase of Cu level in testes of tree sparrows(P < 0.05),and sperm nucleus length increased with Pb level in testes(P = 0.046)and decreased with Cd level(P = 0.035).These results suggested that heavy metals accumulated in testes of tree sparrows had negative effect on testis size,SOD activity in testes and plasma levels of estrogen,which could also interact directly with sperm and affect sperm morphology traits.7.Relationship between testis parametes,reproductive hormones levels and the sperm quality in tree sparrows.The results showed: a significant relationship was observed between sperm movement characteristics and testis volume in tree sparrows(P = 0.029),and sperm swimming ability improved with increased testis volume;sperm movement characteristics of tree sparrows were also affected by SOD activity in testes and plasma level of LH,though the effects were only marginally significant(SOD,P = 0.058;LH,P = 0.077),where sperm swimming ability decreased with increase in SOD activity,and similar trend was observed between percentage of immotile sperm and LH level.These results suggested that testis size,SOD activity in testes and plasma level of LH were some of vital factors determining sperm movement performance under environmental heavy metal pollution.In conclusion,heavy metals significantly enriched in male tree sparrows,resulting in smaller body size and higher liver coefficient under environmental heavy metal pollution.Heavy metals accumulated in testes of tree sparrows had significantly adverse influence on indicators related to male reproductive function,while their testicular function,reproductive hormone levels and sperm quality responded positively to the environmental heavy metal stress.The positive response included strengthening antioxidant defense to protect testes from oxidative damage,enhancing testes quality control by increased apoptosis levels in testes,promoting secretion of reproductive hormones and improving sperm quality.In addition,increased reproductive investment in regulation of testicular function and reproductive hormone levels was the main factor for the better sperm quality of tree sparrows exposed to environmental heavy metals.This study provides reference and foundation for exploring the mechanism of environmental pollution affecting reproductive function of birds and evaluating trends in bird population dynamics in polluted areas.