Effects of Exposure to WwTW Effluents over Two Generations on

Oct 6, 2015 - Exposure to environmental estrogens in wastewater treatment works (WwTW) effluents induces feminized responses in male fish, including t...
0 downloads 15 Views 724KB Size
Subscriber access provided by University of Otago Library

Article

Effects of Exposure to WwTW Effluents over Two Generations on Sexual Development and Breeding in Roach Rutilus rutilus Patrick Birungi Hamilton, Anke Lange, Elizabeth Nicol, Lisa K Bickley, Eliane De-Bastos, Susan Jobling, and Charles Tyler Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b03777 • Publication Date (Web): 06 Oct 2015 Downloaded from http://pubs.acs.org on October 10, 2015

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 32

Environmental Science & Technology

1

Effects of Exposure to WwTW Effluents over

2

Two Generations on Sexual Development and

3

Breeding in Roach Rutilus rutilus

4 5

Patrick B. Hamilton,* † Anke Lange,† Elizabeth Nicol,‡ Lisa K. Bickley,† Eliane SR De-

6

Bastos,† Susan Jobling. ‡ Charles R. Tyler†

7 8



University of Exeter, Biosciences, College of Life and Environmental Sciences, Exeter,

9 10

EX4 4QD, UK ‡

Institute of Environment, Health and Societies, Brunel University, Uxbridge, Middlesex,

11

UB8 3PH, UK

12 13 14 15 16

Word count: currently 5462 + 1200 (2 figures at 300 word equivalents and 1 figure at 600 word equivalents each) = 6662

17

1 ACS Paragon Plus Environment

Environmental Science & Technology

18

ABSTRACT

19 20

Exposure to environmental estrogens in wastewater treatment works (WwTW) effluents

21

induces feminized responses in male fish, including the development of eggs in male

22

testes. However, the impacts on the offspring of exposed fish are not well understood. In

23

this study we examined whether roach (Rutilus rutilus) from mothers that had been

24

exposed to an undiluted WwTW effluent from early life to sexual maturity had altered

25

susceptibility to gonadal feminization and an impaired capacity to reproduce. For males

26

from both WwTW effluent exposed mothers and dilution water exposed mothers, effluent

27

exposure for up to three years and nine months induced feminized male gonads, although

28

the intersex condition was relatively mild. There was no difference in the severity of

29

gonadal feminization in roach derived from either WwTW effluent exposed or dilution

30

water exposed mothers. Furthermore, a breeding study revealed that roach with effluent-

31

exposed mothers reproduced with an equal success as roach with mothers exposed to

32

clean water. Roach exposed to the effluent for three years in this study were able to

33

reproduce successfully. Our findings provide no evidence for impacts of WwTW effluent

34

exposure on reproduction or gonadal disruption in roach down the female germ line and

35

add to existing evidence that male roach with a mild intersex condition are able to breed

36

competitively.

37

38 39

INTRODUCTION

2 ACS Paragon Plus Environment

Page 2 of 32

Page 3 of 32

Environmental Science & Technology

40

Wastewater treatment work (WwTW) effluents contain tens of thousands of chemicals,

41

including natural and pharmaceutical steroid estrogens. There is substantial evidence that

42

exposure of male fish to WwTW effluents causes feminization, and that severely

43

feminized male gonads impair breeding success of those individuals.1-3 Feminized male

44

phenotypes include the production of the female yolk protein precursor vitellogenin,4

45

feminized reproductive ducts and the presence of both male and female germ cells in the

46

male gonad.5

47 48

The estrogenic activity of WwTW effluents predominantly results from the presence of

49

steroid estrogens emanating from human excretion. These include estradiol (E2), its

50

breakdown product, estrone (E1) and the pharmaceutical estrogen 17α-ethinylestradiol

51

(EE2), a component of the female contraceptive pill.6 Other substances detected in

52

effluents shown to be estrogenic include the pharmaceutical metformin,7 alkylphenoxy

53

polyethoxylates (APEOs) and their breakdown products,8 and plasticizers (e.g. bisphenol

54

A9). These chemicals may also contribute to the feminization of male fish in some rivers

55

receiving high level industry discharges. Natural plant estrogens occur widely in effluent

56

discharges,10 but they are relatively weak in potency compared with steroidal estrogens.11

57

There is also some evidence supporting the involvement of chemicals that can act as

58

antiandrogens contribute to the feminization of fish in some rivers.6, 12-18

59

In the United Kingdom, concern regarding the impacts of estrogenic effluents on fish

60

health and fish populations led to a £40M investment to evaluate the ability of various

61

secondary and tertiary treatment processes to remove estrogens from effluents

62

more recently a £100M chemical investigation programme. From this work it has been

3 ACS Paragon Plus Environment

19, 20

and

Environmental Science & Technology

Page 4 of 32

63

established that although some tertiary processes, such as activated carbon are highly

64

effective, they are expensive and incur a greater carbon footprint than more widely

65

adopted secondary treatment processes.19, 21

66 67

Much of the current knowledge on the impacts of treated estrogenic effluents is derived

68

from studies on the cyprinid fish roach (Rutilus rutilus), which commonly occurs in

69

sewage-contaminated rivers in the United Kingdom. Endocrine disruption in fish was

70

first reported when a low (5%) incidence of intersex was found in wild roach populations

71

living just downstream of a WwTW effluent discharge into the River Lee in the UK.22

72

Later surveys found roach with feminized gonads at 86% of UK river locations

73

surveyed.23, 24. All feminized phenotypes seen in wild roach have been induced through

74

controlled exposures to WwTW discharges

75

female germ cells in an otherwise male gonad requiring persistent exposure during the

76

period of gonadal differentiation.

19, 25, 26

and to EE2,27,

28

with induction of

77 78

A major concern is whether WwTW effluents impact on fish populations by affecting

79

reproductive output. Several experimental exposures to EE2, at concentrations that have

80

been measured occasionally in WwTW effluents and encompassing the period of sexual

81

development, have found that exposure can result in complete feminization and/or

82

reproductive failure.28-32 Notably, exposure of an entire lake in Canada for three years to

83

4-6 ng EE2/L resulted in the collapse of the fathead minnow (Pimephales promelas)

84

population residing in this lake.31 These exposures, however, exceed typical river

85

concentrations of estrogens.33 Nevertheless EE2 exposures at concentrations