Research Article |
Corresponding author: Francisco Javier Zamora-Camacho ( zamcam@ugr.es ) Academic editor: Günter Gollmann
© 2019 Francisco Javier Zamora-Camacho, Pedro Aragón.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Zamora-Camacho FJ, Aragón P (2019) Hindlimb abnormality reduces locomotor performance in Pelobates cultripes metamorphs but is not predicted by larval morphometrics. Herpetozoa 32: 125-131. https://doi.org/10.3897/herpetozoa.32.e35654
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Locomotor performance is a fundamental feature commonly related to many animals’ fitness. In most cases, locomotor performance is closely related to morphology of the structures responsible for it, which is therefore under strong selective pressure. Hence, limb abnormality could hinder locomotion and, for that reason, be eradicated by selection, which could explain its overall low prevalence that makes proper research difficult. Here, we took advantage of the moderately high prevalence of hindlimb abnormality in a sample of Iberian spadefoot (Pelobates cultripes) metamorphs developed from tadpoles captured and transferred to the laboratory before selection could act against metamorph abnormality. We tested the hypothesis that limb abnormality impairs locomotor performance. Moreover, we measured several larval and metamorph morphometrics, and checked for differences between normal and abnormal-limbed individuals. We also assessed correlations between hindlimb ratio (hindlimb length/SVL) and jumping performance in normal and abnormal-limbed metamorphs. Larval traits measured could not predict hindlimb abnormality. In metamorphs, only hindlimb ratio differed between normal and abnormal-limbed individuals, being shorter in the latter. Abnormal-limbed metamorphs jumped considerably shorter distances than normal-limbed conspecifics. Therefore, selection against reduced locomotor performance could eliminate limb abnormality from populations. Hindlimb ratio was included in the model as a covariable, and thus controlled for. Consequently, other factors besides shorter hindlimbs, probably hindlimb abnormality itself, could play a role in worse jumping capability of abnormal-limbed individuals. Hindlimb ratio was positively related to jumping distance in both groups, although the relationship was weaker in abnormal-limbed metamorphs.
anomaly, anuran, jumping distance, morphology, spadefoot
Locomotor performance is key to most animals’ fitness (
In most vertebrates, locomotor performance is closely related to morphology of the appendages responsible for locomotion, such as fins in fish (
However, anurans are increasingly susceptible to limb abnormality (
In this paper, we took advantage of a cohort of metamorphs of Iberian spadefoot toads (Pelobates cultripes Cuvier, 1829) resulting from tadpoles captured from a wild population and transferred to the laboratory before selection could act against metamorph abnormality. This procedure enabled us to obtain a prevalence higher than in nature and hence to perform analyses with an appropriate sample size. Among those metamorphs, an abnormality in hindlimb morphology, consisting of misshaped limbs (see below), was present in a sufficiently high number of metamorphs to study its effect on locomotion. We predict that locomotion will be impaired in abnormal-limbed metamorphs as compared to normal-limbed conspecifics. Abnormal morphology of amphibian metamorphs could reflect a deficient larval development (
Pelobates cultripes is a medium-to-large sized toad widely distributed throughout most of the Iberian Peninsula and in Southern France (
Animal collection took place in Pinares de Cartaya (SW Spain, 37°20'N, 7°09'W), a sandy stone pine (Pinus pinea) grove. In March 2017, we captured 71 recently hatched larvae in a small pond (a suboptimal habitat for these tadpoles;
where Wi and Li are, respectively, body mass and total length of each tadpole, L0 is the arithmetic mean of total length in the sample, as a valid value to which the individual values can be standardised, and bSMA is the slope of a standardised major axis regression, calculated here as the result of dividing the slope from the ordinary least squares regression of body mass on total length by the Pearson’s correlation coefficient, r (
In total, 23 out of 71 metamorphs showed abnormal hindlimbs. Abnormality consisted of a malformation in the angle of insertion of the hindlimbs in the pelvis, both inserted with an angle of approximately 270° with respect to each other (Fig.
Within 12 hours of metamorphosis having completed, metamorphs were tested for jumping distance. Metamorphs were not fed prior to the trials, which reduces variability due to nutritional status. In the laboratory, metamorphs were transferred to a box of expanded polystyrene (50×50×20 cm) for the trials. To that end, they were individually released next to a corner of the box, with a drawing pin stuck in the polystyrene immediately behind the urostyle. Then, we gently prodded their hindquarters to stimulate jumping, and stuck a new drawing pin immediately behind the urostyle in the spot where metamorphs touched down. We stimulated five successive jumps, and stuck a drawing pin as described each time. Finally, we measured the distance between drawing pins consecutively stuck, corresponding with the distance of each jump. This way, we could calculate maximum jumping distance as that of the longest jump of each individual. Trials were performed at 22 °C room temperature, because body temperature can affect locomotor performance in anurans (
We conducted parametric statistics after the appropriate transformations (maximum jumping distance needed to be log-transformed, in order to meet those criteria) to accomplish homoscedasticity and residual normality (
Sample sizes were 48 normal- and 23 abnormal-limbed individuals. The MANOVA analysis for morphological variables was significant (F8, 62 = 5.200; P < 0.001). When the separate effects on each variable within the model were checked, only that on hindlimb ratio was significant (F1, 69 = 34.111; P < 0.001; Fig.
According to our prediction, abnormal-limbed metamorphs jumped considerably shorter distances. Reduced jumping capacity in abnormal-limbed metamorphs could severely compromise their survival, because of their reduced capacity to flee from predators (
Morphological variables measured in tadpoles were not able to predict hindlimb abnormality in metamorphs. This coincides with findings by
Limb length is typically related to locomotor performance in anurans (
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Animal capture and management was conducted according to permits issued to the authors by CSIC bioethics committee (reference 695/2018) and “Junta de Andalucía” Government (reference AWG/mgd GB-509-17). FJZ-C was supported by a “Juan de la Cierva-Formación” postdoctoral grant by the Spanish “Ministerio de Economía, Industria y Competitividad” (MINECO). PA was supported by a “Ramón y Cajal” contract (RYC-2011-07670, MINECO). This study was partly funded by the project CGL2014-56416-P (MINECO). Comments by Günter Gollmann and two anonymous reviewers improved the manuscript.