Ontogenetic shifts and spatial associations in organ positions for snakes

Abstract

Snakes possess an elongated body form and serial placement of organs which provides the opportunity to explore historic and adaptive mechanisms of organ position. We examined the influence of body size and sex on the position of, and spatial associations between, the heart, liver, small intestine, and right kidney for ten phylogenetically diverse species of snakes that vary in body shape and habitat. Snake snout-vent length explained much of the variation in the position of these four organs. For all ten species, the position of the heart and liver relative to snout-vent length decreased as a function of size. As body size increased from neonate to adult, these two organs shifted anteriorly an average of 4.7% and 5.7% of snout-vent length, respectively. Similarly, the small intestine and right kidney shifted anteriorly with an increase in snout-vent length for seven and five of the species, respectively. The absolute and relative positioning of these organs did not differ between male and female Burmese pythons (Python molurus). However, for diamondback water snakes (Nerodia rhombifer), the liver and small intestine were more anteriorly positioned in females as compared to males, whereas the right kidney was positioned more anteriorly for males. Correlations of residuals of organ position (deviation from predicted position) demonstrated significant spatial associations between organs for nine of the ten species. For seven species, individuals with hearts more anterior (or posterior) than predicted also tended to possess livers that were similarly anteriorly (or posteriorly) placed. Positive associations between liver and small intestine positions and between small intestine and right kidney positions were observed for six species, while spatial associations between the heart and small intestine, heart and right kidney, and liver and right kidney were observed in three or four species. This study demonstrates that size, sex, and spatial associations may have potential interacting effects when testing evolutionary scenarios for the position of snake organs.

Ontogenetic shifts of heart position in snakes

“…In a recent analysis reported by Anderson and Secor (2015), neither absolute nor relative heart position was different between males and females of Nerodia rhombifer, the species for which the sample of individuals was largest (n 5 434). Similarly, we did not find a significant difference between sexes for relative heart position in Agkistrodon conanti (t-test, p 5 .0723).…”

“…The independent regression variables were functions of body length. There is no problem using ratios in regressions, as has been shown in great detail by Firebaugh and Gibbs (1985) as well as numerous other articles (see also Anderson & Secor, 2015). Our analyses of data reported herein demonstrate that for all snakes the residuals from regressions of the form $y_i=b{x}_i+c{x}_i^2+{\epsilon }_i$ (where ε is an error term) have a clear pattern of increasing variance with increasing x (see Supporting Information).…”

“…The relative extent of heart displacement during ontogeny, representing just a few percent of total body length (Table 1; Figures 2 and 4; see also Anderson & Secor, 2015, 2016), is small compared with the difference of mean heart position between species (e.g., 32%TL vs. 17%TL in Agkistrodon and Pantherophis , respectively). It seems clear there is selection for heart position related to gravity and postural behaviors in Pantherophis but not in Agkistrodon , and this is an interspecific phenomenon (Lillywhite, 1985, 2005; Lillywhite & Donald, 1994; Lillywhite & Gallagher, 1985; Lillywhite & Smits, 1992).…”

“…Data germane to this question were published recently by Anderson and Secor (2015), who documented anterior shifts of the heart as body size increased from neonate to adult in ten species of snakes. These authors also demonstrated (2016) that internal organs in Diamondback water snakes ( Nerodia rhombifer ) did not exhibit any size-dependent changes in their alignment to body segments, and they concluded that observed anterior shifts in relative organ positions (including the heart) are the result of regional differences in the growth of body segments.…”

“…These are representative of the extreme end of the environmental spectrum with respect to gravity stress, which is essentially absent for snakes having long evolutionary association with completely aquatic habitats (Lillywhite & Pough, 1983; Lillywhite, 1987, 1996). Fully aquatic species were not included in the recently published studies of Anderson and Secor (2015, 2016). We test the hypothesis that ontogenetic changes in heart position in aquatic snakes are more similar to that of ground-dwelling cottonmouths than to scansorial rat snakes.…”