Adverse temporal trends in human semen quality and cryptorchidism in infants have been associated with exposure to environmental chemicals (ECs) during development. Here we report that a population of breeding dogs exhibit a 26 year (1988–2014) decline in sperm quality and a concurrent increased incidence of cryptorchidism in male offspring (1995–2014). A decline in the number of males born relative to the number of females was also observed. ECs, including diethylhexyl phthalate (DEHP) and polychlorinated bisphenol 153 (PCB153), were detected in adult dog testes and commercial dog foods at concentrations reported to perturb reproductive function in other species. Testicular concentrations of DEHP and PCB153 perturbed sperm viability, motility and DNA integrity in vitro but did not affect LH stimulated testosterone secretion from adult testis explants. The direct effects of chemicals on sperm may therefore contribute to the decline in canine semen quality that parallels that reported in the human.

A temporal decline in human and dog sperm quality is thought to reflect a common environmental aetiology. This may reflect direct effects of seminal chemicals on sperm function and quality. Here we report the effects of diethylhexyl phthalate (DEHP) and polychlorinated biphenyl 153 (PCB153) on DNA fragmentation and motility in human and dog sperm. Human and dog semen was collected from registered donors (n = 9) and from stud dogs (n = 11) and incubated with PCB153 and DEHP, independently and combined, at 0x, 2x, 10x and 100x dog testis concentrations. A total of 16 treatments reflected a 4 × 4 factorial experimental design. Although exposure to DEHP and/or PCB153 alone increased DNA fragmentation and decreased motility, the scale of dose-related effects varied with the presence and relative concentrations of each chemical (DEHP.PCB interaction for: DNA fragmentation; human p < 0.001, dog p < 0.001; Motility; human p < 0.001, dog p < 0.05). In both human and dog sperm, progressive motility negatively correlated with DNA fragmentation regardless of chemical presence (Human: P < 0.0001, r = −0.36; dog P < 0.0001, r = −0.29). We conclude that DEHP and PCB153, at known tissue concentrations, induce similar effects on human and dog sperm supporting the contention of the dog as a sentinel species for human exposure.

Despite the vast body of evidence that environmental toxicants adversely affect reproductive development and function across species, demonstrating true cause and effect in the human remains a challenge. Human meta-analytical data, showing a temporal decline in male sperm quality, are paralleled by a single laboratory study showing a similar 26-year decline in the dog, which shares the same environment. These data are indicative of a common cause. Environmental chemicals (ECs) detected in reproductive tissues and fluids induce similar, short term, adverse effects on human and dog sperm. Both pre- and post-natal stages of early life development are sensitive to chemical exposures and such changes could potentially cause long term effects in the adult. The environmental ‘pollutome’ (mixtures of ECs) is determined by industrialisation, atmospheric deposition and bioaccumulation and characterises real-life exposure. In Arctic ecosystems, dietary and non-dietary chemical contaminants are detectable in biological tissues and linked with adverse health effects in both dogs and their handlers. In the female, such exposure could contribute to disorders such as ovarian insufficiency, dysregulated follicle development, ovarian cancer, and polycystic ovarian syndrome. In the dog, ovarian chemical concentrations are greater in the testis. In addition, preliminary studies indicate that dietary exposures may influence the sex ratio in the offspring in favour of females. Within this article, we review current knowledge on chemical effects on human reproduction and suggest that the dog, as a sentinel species for such effects, is an essential tool for addressing critical data gaps in this field.

In humans and dogs, a temporal decline in semen quality and increased incidence of testicular cancer is hypothesised to be associated with exposure to anthropogenic chemicals, particularly during fetal development. Human studies suggest that differential exposures to environmental chemicals may be associated with geographical differences in male reproductive health. Here we investigate testicular chemical profiles and pathologies in dogs residing in the UK [West Midlands (WM), East Midlands (EM), South East (SE)], Denmark (Copenhagen) and Finland (Vantaa). Testes, surplus from routine castrations, contained region specific differences in relative concentrations of diethylhexyl phthalate (DEHP), polybrominated diphenyl ethers (PBDE) and polychlorinated biphenyls (PCB). Relative to UK regions, testes from dogs living in Finland and Denmark had higher concentrations of PBDE and lower concentrations of DEHP and PCBs. Regional differences in the UK in PCB concentrations were also observed. Dog testes from Finland had fewer pathologies, reduced testicular area stained for Sertoli and germ cells and evidence of reduced cellular proliferation. Since the geographical differences in testis pathologies in dogs parallel reports of regional differences in human testicular cancer, we postulate that this may reflect chemical effects within the testis and that this may be related to environmental influences on male reproductive function.