Research Article: A validation of 11 body-condition indices in a giant snake species that exhibits positive allometry

Date Published: July 19, 2017

Publisher: Public Library of Science

Author(s): Bryan G. Falk, Ray W. Snow, Robert N. Reed, Christopher M. Somers.

http://doi.org/10.1371/journal.pone.0180791

Abstract

Body condition is a gauge of the energy stores of an animal, and though it has important implications for fitness, survival, competition, and disease, it is difficult to measure directly. Instead, body condition is frequently estimated as a body condition index (BCI) using length and mass measurements. A desirable BCI should accurately reflect true body condition and be unbiased with respect to size (i.e., mean BCI estimates should not change across different length or mass ranges), and choosing the most-appropriate BCI is not straightforward. We evaluated 11 different BCIs in 248 Burmese pythons (Python bivittatus), organisms that, like other snakes, exhibit simple body plans well characterized by length and mass. We found that the length-mass relationship in Burmese pythons is positively allometric, where mass increases rapidly with respect to length, and this allowed us to explore the effects of allometry on BCI verification. We employed three alternative measures of ‘true’ body condition: percent fat, scaled fat, and residual fat. The latter two measures mostly accommodated allometry in true body condition, but percent fat did not. Our inferences of the best-performing BCIs depended heavily on our measure of true body condition, with most BCIs falling into one of two groups. The first group contained most BCIs based on ratios, and these were associated with percent fat and body length (i.e., were biased). The second group contained the scaled mass index and most of the BCIs based on linear regressions, and these were associated with both scaled and residual fat but not body length (i.e., were unbiased). Our results show that potential differences in measures of true body condition should be explored in BCI verification studies, particularly in organisms undergoing allometric growth. Furthermore, the caveats of each BCI and similarities to other BCIs are important to consider when determining which BCI is appropriate for any particular taxon.

Partial Text

As a measure of the relative energy stores of an animal [1], body condition has both theoretical and practical importance because of its strong associations with reproductive capacity [2, 3], survivorship [3–5], competition [6, 7], and disease [8–10]. Despite this importance, body condition is generally unfeasible to measure directly because direct measurement requires destruction of the whole specimen [11–14]. Instead, biologists frequently estimate body condition using a body condition index (BCI) calculated from mass and length variables obtained from non-invasive measurements (reviewed in [14]; see [15] for alternative means to estimate body condition).

We performed necropsies on Burmese pythons that were collected in southern Florida during 2004–2014 as part of ongoing invasive-species management activities. The snakes were humanely euthanized via captive bolt, kept on ice, and either necropsied within 24 hours of euthanasia or frozen and later thawed on ice for necropsy. No Institutional Animal Care and Use Committee approval was necessary because the invasive pythons were euthanized as part of management–and not research–activities, but methods of safe and humane euthanasia were developed in consultation with the National Park Service Wildlife Health Team. Similarly, these necropsies were not performed explicitly to evaluate BCIs, but we nonetheless collected the necessary data. We used measurements of total body mass (g) and snout-vent length (SVL; cm) as body-mass and length metrics for our BCIs. We used SVL instead of total length because SVL is more tightly associated with mass than is total length in snakes (because tail length varies; [37]). During necropsy we removed all visible fat from the coelomic cavity and weighed it (wet-fat mass; g). We recorded sex (male or female) and for a subset of individuals we recorded whether the snake was necropsied while fresh or frozen and later thawed. We excluded pythons that were not immediately put on ice or frozen after death (e.g., we excluded pythons found dead on roads). We performed all subsequent analyses in R v.3.3.3 [38] using the car [39], corrplot [40], cowplot [41], extrafont [42], fBasics [43], ggplot2 [44], lmodel2 [45], lmtest [46], moments [47], and smatr [48] packages.

We obtained records of total mass, wet-fat mass, SVL, and sex for 248 Burmese pythons that were immediately placed on ice or frozen after death. Of these, 137 were male and 109 were female, and males were usually smaller and had less fat than females (Table 2). We rejected the null hypothesis that differences in sex do not affect the relationship between wet-fat mass and SVL (p ≤ 0.05), and so we separated males and females in all downstream analyses. In contrast, we could not reject the null hypothesis that our specimen-handling procedures (i.e., whether the animals had been frozen prior to necropsy) do not affect the relationship between wet-fat mass and SVL (p = 0.28), so we ignored specimen-handling information in downstream analyses.

We evaluated 11 BCIs using percent fat, scaled fat, and residual fat as alternative measures of true body condition in Burmese pythons. In our dataset, females exhibit a more positive allometric relationship between mass and length and between fat mass and length than do males, and fat mass is strongly associated with length in both sexes. None of our three measures of true body condition completely removed this effect of size, though the effects of size were minor for scaled fat and residual fat. Our inferences of the best-performing BCIs heavily depended on our measure of true body condition. BCIs exhibiting strong associations with percent fat often exhibited even stronger relationships with SVL. These BCIs included most of the ratio indices (ratio index, Quételet index, relative condition index, log ratio index, and log relative condition index). Conversely, BCIs with strong associations with scaled fat and residual fat exhibited weak or no relationships with SVL. These BCIs included most of the regression indices (OLS residual index, MA residual index, and SMA residual index), the Fulton index, and the SMI.

 

Source:

http://doi.org/10.1371/journal.pone.0180791

 

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