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World Primates, Callitrichidae M Measurement of faecal steroids for monitoring ovarian function in New World primates, Callitrichidae M. Heistermann, S. Tari and J. K. Hodges Department of Reproductive Biology, German Primate Centre, ¡(ellnenveg 4, 37077 Göttingen, Germany Measurement of immunoreactive progesterone, pregnanediol and oestradiol in faeces col- lected throughout ovarian cycles in three species of callitrichid primates is reported. Faecal hormone concentrations were compared with plasma progesterone profiles during PGF2\g=a\- controlled (n = 7) and natural (n = 8) cycles in Callithrix jacchus and Saguinus fuscicollis, respectively, and with urinary oestrone conjugates during five cycles in Saguinus oedipus. Unconjugated steroids, which predominated over enzyme hydrolysable conjugates in samples from all species, were used to generate cycle profiles. According to results from HPLC, oestrone and oestradiol accounted for virtually all oestrogen immunoreactivity, and oestradiol most often predominated, whereas large amounts of nonspecific immunoreactivity were detected by both progesterone and pregnanediol assays. Faecal progestins were excreted in a cyclic manner in all species; luteal phase values were on average five- to tenfold higher than corresponding follicular phase values. Significant increases in mean amounts of faecal progestins were seen within 48 h of the post-ovulatory rise in plasma progesterone. Although a similar trend was also seen for faecal oestradiol, a clear and consistent luteal phase increase was seen only in Callithrix jacchus and this generally occurred later than that of progestins. The results indicate that faecal progestin analysis provides a useful method for noninvasive reproductive assessment in callitrichid primates. In particular, measurement of immunoreactive pregnanediol enables a multispecies application of a single assay methodology for comparative studies on callitrichid reproductive function. Introduction Shideler et al, 1993). However, with the exception of yellow baboons (Wasser et al, 1991) and cynomolgus monkeys Over the last 10 years, noninvasive methods for determining (Shideler et al, 1993), there is no detailed information describ¬ reproductive status have been important in facilitating studies ing patterns of faecal steroid excretion throughout ovulatory which the measurements in a wide variety of disciplines including biomedicai research, cycles from reliability of faecal hormone behavioural ecology and conservation biology. The predomi¬ for determining ovarian function can be critically assessed. nant method for endocrine monitoring of reproductive status The present study was conducted to evaluate the use of for the has been (and still is) urinary hormone analysis, and measure¬ faecal hormone determinations monitoring ovarian cycle ment of steroid metabolites in urine has provided valuable in callitrichid primates. Apart from the importance of certain information on ovarian cyclicity and pregnancy in a wide species in biomedicai research, the family Callitrichidae is the variety of mammalian species (see Lasley, 1985; Hodges, 1992, subject both of interest with regard to social regulation of in press). female fertility (Abbott, 1984; Heistermann et al, 1989) and of More recently, however, there has been increasing interest in concern owing to the endangered status of several species in the wild these the application of faecal hormone analysis as an additional or (Mittermeier et al, 1988). As primates exhibit alternative approach to noninvasive endocrine assessment, pri¬ few, if any, clearly visible signs of reproductive status, the of endocrine methods has marily owing to the relative ease of sample collection from ani¬ application monitoring usually been hormone mals in group situations or in their natural habitat (Safar-Hermann necessary. Although urinary analysis has been invalu¬ et al, 1987; Wasser et al, 1988, 1991; Bamberg et al, 1984, able in this regard, species variation in the qualitative nature 1991; Lasley and Kirkpatrick, 1991 for review). A number of of urinary steroid metabolites (see, for example, Hodges and has limi¬ studies have shown the presence of measurable amounts of Eastman, 1984; Heger and Neubert, 1987) imposed reproductive steroids in faeces of primates (Risler et al, 1987; tations on the inter-species applicability of individual assays. Wasser et al, 1988; Perez et al, 1988; Ziegler et al, 1989; Information on the potential of faecal hormone analysis for Bamberg et al, 1991) and described improved methods for their monitoring reproductive status in Callitrichidae or indeed any extraction and immunological detection (Wasser et al, 1991; other New World primate is not available. The study described here was therefore carried out with the Received 5 January 1993. following specific objectives: (i) to establish and validate Downloaded from Bioscientifica.com at 09/27/2021 03:01:27AM via free access methods for the extraction and determination of reproductive polypropylene tube and a total of 10 000 c.p.m. [3H]progester- steroids in faeces of callitrichid primates and (ii) to provide one (Amersham Buchler, Braunschweig) was added to monitor comparative data on the pattern of faecal steroid excretion extraction efficiency. [3H]progesterone was used routinely as throughout ovarian cycles in three species, namely the common recovery tracer irrespective of which hormone was to be assayed, marmoset, Callithrix jacchus, the saddle-back tamarin, Saguinus as initial studies showed extraction efficiencies to be similar fuscicollis and the cotton-top tamarin, Saguinus oedipus. for all unconjugated steroids tested (progesterone: 82-94%; pregnanediol: 86-95%; oestradiol: 82-95%). Recovery values between species were not different and the overall mean recov¬ Materials and Methods ery value for all samples extracted was 89.1 + 1.0% (x + SEM, = 418). Animals Steroids were extracted from the faeces according to a modification of the method described by Wasser et al. (1991). Adult female Callithrix jacchus {n = 4) and Saguinus fuscicollis Ethanol:acetone (5 ml; 4:1 v:v) was added to the sample; the = were the the German (n 3) housed in Primate facilities of mixture was vortexed for 15 min and after centrifugation h Primate Centre under a 12 light:12 h dark lighting regimen, in (2600 g for 15 min), the supernatant was decanted into a 15 ml rooms maintained within a temperature and humidity range of glass tube. The faecal pellet was re-extracted by vortexing for 25 + 1°C and 60 + 5%, respectively. Animals received pri¬ 5 min with 2 ml 80% ethanol, recentrifuged and the supernatants mate pellets (variously supplemented with fruit, vegetables and were combined. The volume of the mixture was reduced under and mineral once a a vitamin mix) day and water ad libitum. nitrogen to approximately 3 ml; 1 ml distilled water was added Saguinus oedipus (n = 2) were maintained in the primate colony and the solution vortexed and further reduced in volume to the conditions described at University of Bielefeld under by approximately 1 ml (step 1). Unconjugated steroids were then Heistermann et al. (1989). Callithrix jacchus females were housed extracted into 5 ml diethylether and after evaporation to dry- with intact males and cyclic ovarian function was maintained by ness, steroids were reconstituted in 1 ml absolute methanol the a application of luteolytic dose of PGF2a during the mid- (step 2). The radioactivity of a 50 pi portion of the extract was luteal phase (Summers et al, 1985). Saguinus fuscicollis females measured to determine extraction efficiency; the remaining males and were kept with vasectomized female Saguinus oedipus methanolic extract was stored at 20°C until assayed. Initial — were maintained in family groups without a breeding male. studies on the effect of quenching on counting efficiency deter¬ mined by counting different volumes of extract (25-200 pi) in Sample collection 3 ml scintillation fluid showed that quenching was not observed in volumes of less than 100 pi. A volume of 50 pi was therefore Faecal samples were collected 5-7 days a week for at least chosen to determine recovery. one but not more than three ovarian cycles for an individual The relative abundance of steroids present in faeces as conju¬ animal. In total, samples were collected from seven, eight and gates was assessed by extracting selected samples from the fol¬ five cycles from Callithrix jacchus, Saguinus fuscicollis and Saguinus licular and luteal phase in each species, and taking both organic oedipus, respectively. Samples were collected between 07:00 and and residual aqueous phases (step 2, see above) for further 08:00 h by separating females from their partner or family mem¬ analysis. The aqueous residue was adjusted to pH 5 with bers and keeping them in isolation in the home cage until they 0.1 mol HC1 H and incubated for 18-20 h at 37°C with defaecated (usually less than 40 min). Faeces were collected on 50 pi ß-glucuronidase/sulfatase (Type H-5, No. G-1512; plastic sheets positioned under the cage and constructed in a Sigma Chemicals, Deisenhofen; containing 2500 Fishman U ß- way to minimize contamination with urine. A 5-10 g faecal glucuronidase and 200 U sulfatase activity per 50 pi). sample was transferred to a plastic tube and stored at 20°C After hydrolysis the free steroids were extracted with 5 ml — until analysed. diethylether, the ether evaporated to dryness and the extract In addition, blood samples (0.2 ml) taken from the femoral reconstituted in 1 ml methanol. Extraction and hydrolysis vein
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