Wild intersex roach (Rutilus rutilus) have reduced fertility.
Endocrine-disrupting chemicals, known to be present in the environment, have great potential for interfering with reproductive health in wildlife and humans. There is, however, little direct evidence that endocrine disruption has adversely affected fertility in any organism. In freshwater and estuarine fish species, for example, although a widespread incidence of intersex has been reported, it is not yet known if intersexuality influences reproductive success. The purpose of this study was, therefore, to determine gamete quality in wild intersex roach (Rutilus rutilus) by assessing sperm characteristics, fertilization success, and ability to produce viable offspring. The results clearly demonstrate that gamete production is reduced in intersex roach. A significantly lower proportion of moderately or severely feminized fish (17.4% and 33.3%, respectively) were able to release milt compared with normal male fish from contaminated rivers (in which 97.6% of the males were able to release milt), reference male fish (97.7%), or less severely feminized intersex fish (experiment 1: 85.8%, experiment 2: 97%). Intersex fish that did produce milt produced up to 50% less (in terms of volume per gram of testis weight) than did histologically normal male fish. Moreover, sperm motility (percentage of motile sperm and curvilinear velocity) and the ability of sperm to successfully fertilize eggs and produce viable offspring were all reduced in intersex fish compared with normal male fish. Male gamete quality (assessed using sperm motility, sperm density, and fertilization success) was negatively correlated with the degree of feminization in intersex fish (r = -0.603; P < 0.001) and was markedly reduced in severely feminized intersex fish by as much as 50% in terms of motility and 75% in terms of fertilization success when compared with either less severely feminized intersex fish or unaffected male fish. This is the first evidence documenting a relationship between the morphological effects (e.g., intersex) of endocrine disruption and the reproductive capabilities of any wild vertebrate. The results suggest that mixtures of endocrine-disrupting substances discharged into the aquatic environment could pose a threat to male reproductive health.
Department of Biological Sciences, Brunel University, Kingston Lane, Uxbridge, Middlesex UB8 3PH, UK. susan.jobling@brunel.ac.uk
Susan
S
Jobling
S
S
Coey
J G
JG
Whitmore
D E
DE
Kime
K J W
KJ
Van Look
B G
BG
McAllister
N
N
Beresford
A C
AC
Henshaw
G
G
Brighty
C R
CR
Tyler
J P
JP
Sumpter
D000818:Animals; D001835:Body Weight / Q000502:physiology; D003530:Cyprinidae / Q000502:physiology*; D045166:Estradiol Congeners / Q000633:toxicity*; D005260:Female; D005298:Fertility / Q000187:drug effects / Q000502:physiology*; D005306:Fertilization / Q000502:physiology; D005854:Germ Cells / Q000502:physiology; D008297:Male; D009929:Organ Size / Q000502:physiology; D010053:Ovary / Q000502:physiology; D012727:Sex Characteristics; D012733:Sex Differentiation / Q000502:physiology*; D012726:Sexual Behavior, Animal / Q000502:physiology; D013094:Spermatozoa / Q000502:physiology; D013737:Testis / Q000502:physiology; D014874:Water Pollutants, Chemical / Q000633:toxicity*; D015262:Xenobiotics / Q000633:toxicity*
D045166:Estradiol Congeners; D014874:Water Pollutants, Chemical; D015262:Xenobiotics