Comparative skull analysis suggests species-specific captivity-related malformation in lions (Panthera leo)

Lion (Panthera leo) populations have dramatically decreased worldwide with a surviving population estimated at 32,000 across the African savannah. Lions have been kept in captivity for centuries and, although they reproduce well, high rates of stillbirths as well as morbidity and mortality of neonate and young lions are reported. Many of these cases are associated with bone malformations, including foramen magnum (FM) stenosis and thickened tentorium cerebelli. The precise causes of these malformations and whether they are unique to captive lions remain unclear. To test whether captivity is associated with FM stenosis, we evaluated 575 lion skulls of wild (N = 512) and captive (N = 63) origin. Tiger skulls (N = 276; 56 captive, 220 wild) were measured for comparison. While no differences were found between males and females or between subadults and adults in FM height (FMH), FMH of captive lions (17.36±3.20 mm) was significantly smaller and with greater variability when compared to that in wild lions (19.77±2.11 mm). There was no difference between wild (18.47±1.26 mm) and captive (18.56±1.64 mm) tigers in FMH. Birth origin (wild vs. captive) as a factor for FMH remained significant in lions even after controlling for age and sex. Whereas only 20/473 wild lions (4.2%) had FMH equal to or smaller than the 5th percentile of the wild population (16.60 mm), this was evident in 40.4% (23/57) of captive lion skulls. Similar comparison for tigers found no differences between the captive and wild populations. Lions with FMH equal to or smaller than the 5th percentile had wider skulls with smaller cranial volume. Cranial volume remained smaller in both male and female captive lions when controlled for skull size. These findings suggest species- and captivity-related predisposition for the pathology in lions.Scopu

Two captive lion skull specimens.

<p><b>A</b>– A skull of an adult lion with a normal opening of the foramen magnum. <b>B</b> - Abnormal bone growth protruding down from the roof of the foramen magnum (asterisk) in a young adult lion. (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094527#pone-0094527-g002" target="_blank">Figure 2A</a> courtesy of Mr. Tom Kouris).</p

Measurements of lion skulls with FM stenosis (FMH< = 16.60 mm) and those with larger FM opening, comparing males and females separately.

<p>Significantly different values in the same raw and within the same sex are marked with a superscript asterisk.</p><p>FMH  =  foramen magnum height, BT  =  basilar thickness</p><p>All comparisons were done using <i>T</i>-test:</p><p>a t = 2.284, <i>DF</i> = 159, <i>P</i> = 0.024</p><p>b t = 3.630, <i>DF</i> = 120, <i>P</i><0.001</p><p>c t = 1.339, <i>DF</i> = 72, <i>P</i> = 0.185</p><p>d t = 1.468, <i>DF</i> = 61, <i>P</i> = 0.147</p><p>e t = 3.283, <i>DF</i> = 265, <i>P</i> = 0.001</p><p>f t = 2.229, <i>DF</i> = 205, <i>P</i> = 0.027</p><p>g t = 1.826, <i>DF</i> = 192, <i>P</i> = 0.069</p><p>h t = 0.826, <i>DF</i> = 145, <i>P</i> = 0.410</p

The mean foramen magnum height (FMH) in captive lions is significantly lower than that of lion skulls from wild populations (17.36±3.20 and 19.77±2.11 respectively; <i>T</i>-test: t = 5.543, <i>DF</i> = 61.969, <i>P</i><0.001).

<p>No statistically significant difference was noted between the captive and wild tiger populations. Asterisks represent outliers.</p

Pearson Correlations between FMH and SL and between SL and SW in lions and tigers.

<p>FMH  =  foramen magnum height, SL  =  skull length, SW  =  skull width.</p

A - The distance between the posthion and the inion - skull length (SL) - black arrow.

<p>The distance between the left and right zygomatic arches - skull width (SW) - white arrow. <b>B</b> - The distance between the top of the basilar part of the occipital bone and the bottom of the occipital bone - foramen magnum height (FMH) – white arrow. The distance between the bottom and the top of the basilar part of the occipital bone at its most caudal aspect - basilar thickness (BT) – black arrow.</p