Delayed implantation in giant pandas: the first comprehensive empirical evidence

Abstract

Successful conservation of an endangered species relies on a good understanding of its reproductive biology, but there are large knowledge gaps. For example, many questions remain unanswered with regard to gestation and fetal development in the giant panda. We take advantage of a sample size that is unprecedented for this species (nZ13) to explore patterns in reproductive development across individuals at the China Conservation and Research Center for the Giant Panda. We use ultrasound techniques on multiple giant pandas for the first time to empirically confirm what has long been suspected that pandas exhibit delayed implantation of the embryo. We also show that the duration of postfetal detection period is remarkably similar across individuals (16.85G1.34 days). Detection of fetus by ultrasound was strongly correlated to the peak in urinary progesterone (rZ0.96, tZ8.48, d.f.Z8, PZ0.0001) and swelling in the mammary glands (rZ0.79, tZ3.61, d.f.Z8, PZ0.007) and vulva (rZ0.91, tZ6.40, d.f.Z8, PZ0.0002) of adult females. When controlling for both the duration of the total gestation period and the postfetal detection period, infant birth weight was only significantly predicted by the latter (bZ11.25, S.E.M.Z4.98, tZ2.26, PZ0.05), suggesting that delayed implantation increases flexibility in the timing of birth but is not important in dictating infant growth. This study informs reproductive biology by exploring the little-studied phenomenon of delayed implantation in relationship to physiological changes in pregnant giant panda females.

Giant Panda Maternal Care: A Test of the Experience Constraint Hypothesis

“…Captive giant pandas sometimes fail to care for their offspring3135. For instance, some mothers respond fearfully to their neonate immediately after giving birth and fail to pick the cub up (R. Snyder, personal observation), particularly first time mothers36.…”

“…Moreover, because female giant pandas experience little weight change during pregnancy and their fetuses are extremely small (90–130 g) at birth2631, primiparous and multiparous females would not be expected to experience significant changes in body condition during pregnancy. Accordingly, by studying captive giant pandas that are consistently provisioned with high quality food and are subject to regular health checks, the effect of body condition on primiparous and multiparous mothers is mostly controlled, and it is possible to provide clear support for or against the experience constraint hypothesis in this species.…”

Mammalian Reproduction Overview

“…An alternative approach to the temporal uncoupling of mating and fetal development, known as delayed implantation (Fenelon et al, 2014;Lopes et al, 2004) has been adopted by at least 130 eutherian mammals. In species such as the seal (Pomeroy, 2011), badger (Yamaguchi et al, 2006), Giant panda (Zhang et al, 2009), armadillo and stoat (reviewed by Mead, 1993), the embryos do not develop for some weeks or even months, before the diapause ends and the pregnancy resumes. Sixteen species of mustelids exhibit long gestations ranging from 172 to 365 days, with embryonic development being arrested for most of this period (Mead, 1993).…”

Estimation of the growth curve and heritability of the growth rate for giant panda (Ailuropoda melanoleuca) cubs

“…Lineage-specific biological traits, such as difficult reproduction, a restricted diet, and a low cub survival rate during the newborn and early growth stages also contribute to the high risk of extinction (Zhu et al, 2001;Czekala et al, 2003;Liao et al, 2003;Sutherland-Smith et al, 2004;Zhang et al, 2009). The giant panda has a relatively high birth rate of twins (~45%) (Huang et al, 2002).…”