An avian bioassay for environmental estrogens: The growth response of zebra finch (Taeniopygia guttata) chick oviduct to oral estrogens

Abstract

The rat uterotrophic assay is a recommended tier 1 screening assay for environmental estrogens, but no comparable assay exists for altricial birds. We orally dosed zebra finch chicks daily during their linear growth phase (days 5-11) with estradiol benzoate (EB), genistein, methoxychlor, or octylphenol, all dissolved or suspended in canola oil, or canola oil alone, as a vehicle control. On day 12, oviducts were removed, weighed and examined histologically. All doses of EB (0.1-1,000 nmol/g body wt), genistein at 100 nmol/g. and methoxychlor and octylphenol at 1,000 nmol/g, markedly increased oviduct weight, with the highest dose of EB inducing a 60-fold increase over controls. Oviducts were differentiated in a dose-depedent manner to the point of having tubular glands and a pseudostratified, ciliated epithelium at the higher doses of EB. Our earlier results show that EB at 100 and 1,000 nmol/g impairs reproductive performance of zebra finches. Thus, the zebra finch oviduct bioassay measures estrogenicity over a wide dose range and, for EB exposure, can predict impairment in adult reproductive performance. The responsiveness of chick oviducts to estrogen stimulation may serve as a useful marker of estrogen exposure in wild populations of songbirds.

Dietary red clover (Trifolium pratense) induces oviduct growth and decreases ovary and testes growth in Japanese quail chicks

“…Uterotropic assays are commonly used in rodents to assess estrogenic activity [66,67]. Similarly, estrogen exposure induces oviduct growth in birds [68], and phytoestrogens have been shown to induce oviduct growth in rodents [67] and birds [13,14]. Previous studies in our laboratory have tested the oviduct-growth response of zebra finch chicks by orally exposing chicks to 0.1–1000 nmol estradiol benzoate per g bodyweight per day for a week.…”

“…Phytoestrogens are a subset of plant secondary compounds (SPCs, so-called because they have no function in the primary roles of growth and development in plants), and include several classes of chemicals [6]. While phytoestrogens have been shown to exert endocrine disrupting effects on many species of vertebrates, including livestock [7,8], rodents [9–11], fish [12], and birds [13,14], little is known about the evolutionary function of these chemicals in plants. It has been suggested, however, that phytoestrogens have evolved as a chemical defense against vertebrate herbivory [15–17], similar to the well-studied ecdysteroidal disruption that plants exert on certain insects [18].…”

“…Livestock grazing on red clover and other subterranean clovers can exhibit what is known as “clover disease” resulting in behavioral and physiological reproductive disruption in both males and females, leading to infertility [7,8,35]. Although the phytoestrogen genistein has been shown to act as an estrogen in zebra finch and chickens [13,36], few studies have considered the endocrine disruptive effects of whole estrogenic plants in birds (or, for that matter, any other vertebrate). Accordingly, here we describe studies directed toward determining whether drought-stress changes phytoestrogenic activity of red clover and whether red clover as a dietary component can influence growth and/or sexual development in Japanese quail.…”

Selecting the right bird model in experimental studies on endocrine disrupting chemicals

“…Songbirds that have been frequently used in laboratory ecotoxicological research are, for example, zebra finches (Taeniopygia guttata) and European starlings (Sturnus vulgaris). Millam et al (2002) have assessed the growth response of zebra finch chick oviducts to oral estrogens. They concluded that this measure can be used as a sensitive avian bioassay for environmental estrogens and is particularly relevant for passerine species, in which sexual differentiation may remain sensitive to estrogen perturbation after, as well as before, hatching (Millam et al, 2002).…”

“…Millam et al (2002) have assessed the growth response of zebra finch chick oviducts to oral estrogens. They concluded that this measure can be used as a sensitive avian bioassay for environmental estrogens and is particularly relevant for passerine species, in which sexual differentiation may remain sensitive to estrogen perturbation after, as well as before, hatching (Millam et al, 2002). The drawback of working with zebra finches is that they are small and thus a limited amount of sample can be obtained from each individual.…”