Fecal estrogen, progestagen and glucocorticoid metabolites during the estrous cycle and pregnancy in the giant anteater (Myrmecophaga tridactyla): evidence for delayed implantation

Abstract

BackgroundDeclining numbers of wild giant anteaters highlight the importance of sustainable captive populations. Unfortunately, captive reproductive management is limited by the lack of external physical indicators of female reproductive status and the aggressive behavior of males. We examined the endocrinology of the estrous cycle and pregnancy, and whether delayed implantation is a gestational strategy for giant anteaters as described for other xenarthrans.MethodsFeces were collected from seven captive females 3–5 times weekly and mating was recorded. Concentrations of estrogen (estrone–glucuronide, E1, and estradiol–17β, E2), progestagen (20–oxo–progestagens, P4), and glucocorticoid (GC) metabolites were examined in fecal extracts by enzyme immunoassay.ResultsEstrous cycles for nulliparous females (6 cycles, n = 2) compared to the multiparous female (6 cycles, n = 1) were shorter (47.3 +/− 4.3 days versus 62.5 +/− 2.6 days) with relatively lower luteal phase concentrations of P4 (49.4 +/− 2.9 ng/g versus 136.8 +/− 1.8 ng/g). The four remaining females had unclear ovarian activity: two females exhibited apparent luteal activity but unclear fluctuations in estrogens, while the other two females had parallel fecal P4 and estrogens concentrations. Pregnancy ranged 171–183 days with females returning to estrus post–partum as early as 60 days (n = 3, 1.8-4 years of age at mating). Delayed implantation was indicated by a biphasic elevation in fecal P4 metabolites: the initial 4–fold increase occurred for 81–105 days and was followed by a 26–fold secondary rise in P4 metabolites lasting 66–94 days prior to parturition. Fecal GC was correlated with fecal estrogens and greatest during estrus, late pregnancy, and six days prior to parturition (estrous cycle GC, 14.4-62.8 ng/g; pregnancy GC, 13.6-232.7 ng/g).ConclusionsEstrous cycles of giant anteaters occurred year–round, but were shorter and more intermittent in younger nulliparous animals compared to a multiparous female. A pronounced elevation in fecal P4, estrogen, and GC occurred during late gestation after an initial post-mating delay providing evidence for delayed implantation. Adrenocorticoid activity indicated impending parturition. Differences in estrous cycle characteristics with age and the protracted but variable gestation length must be considered to improve reproductive success and neonatal survival in giant anteaters.

Embryonic diapause: development on hold

“…However, the precise mechanisms by which the uterus exerts its influence on the embryo are still not clearly understood. (Selwood, 1980, Renfree, 1981, Gilbert, 1984, Nelson and Goldstone, 1986, Hodara et al, 1989, Sandell, 1990, Huang et al, 1993, Atkinson, 1997, Newkirk et al, 1997, Smith, 1998, Fisher, 1999, Johnson and Delean, 1999, Crocker et al, 2001, Johnson and Delean, 2002, Courtenay and Friend, 2004, Thom et al, 2004, Delean, 2007, Knott et al, 2013 an increased understanding of the embryo-uterine dialogue has implications not only for women with recurrent miscarriages but also in improving the success rate of embryo transfers resulting from assisted reproductive technologies.…”

In‐house monitoring of steroid hormone metabolites in urine informs breeding management of a giant anteater (Myrmechophaga tridactyla)

“…Non‐invasive hormone monitoring from animal excreta has been long established as an irreplaceable tool for physiologists hoping to gauge internal processes without handling dangerous species or resorting to surgical procedures (Schwarzenberger, ; Schwarzenberger & Brown, ). Previously, estrous cycle and pregnancy in giant anteaters has been described using fecal hormone metabolite concentrations, revealing a ∼51 day estrous cycle and gestation length of 171–184 days (Knott et al, ; Patzl, Schwarzenberger, Osmann, Bamberg, & Bartmann, ). Females also exhibit a pronounced progestogen increase in the second half of pregnancy, reaching the highest concentrations about a week before parturition (Knott et al, ; Patzl et al, ).…”

“…Previously, estrous cycle and pregnancy in giant anteaters has been described using fecal hormone metabolite concentrations, revealing a ∼51 day estrous cycle and gestation length of 171–184 days (Knott et al, ; Patzl, Schwarzenberger, Osmann, Bamberg, & Bartmann, ). Females also exhibit a pronounced progestogen increase in the second half of pregnancy, reaching the highest concentrations about a week before parturition (Knott et al, ; Patzl et al, ). In this report, we use hormone monitoring alongside management to repeatedly achieve successful introduction and breeding in a pair of giant anteaters ( M. tridactyla ) housed at the Cleveland Metroparks Zoo, a facility which had never before successfully bred this species.…”

“…Progestogen (P) and estrogen (E) metabolite concentrations in urine samples were determined using enzyme immunoassays routinely applied in our laboratory, utilizing a mouse monoclonal antibody specific for progesterone (CL425, C. Munro, University of California, Davis, CA), and a rabbit polyclonal antibody specific for estrone‐3‐glucuronide (R522‐2, C. Munro, University of California). Both antibodies were used previously to monitor excreted hormones in giant anteater feces (Knott et al, ). In brief, these assays used a double antibody system with a secondary goat‐anti mouse (P) or rabbit (E) IgG antibody (A008 and A009, respectively; Arbor Assays, Ann Arbor, MI).…”

“…Reproductive cycle phases were determined as previously described (Knott et al, ; Patzl et al, ). Estrous cycle length was measured as days between E peaks, the sampling day containing the highest E concentration during estrus was labeled Day 0.…”