TY - JOUR
AU1 - Gerald, Gary, W
AU2 - Wass, Emma, D
AB - Abstract Trade-offs among performance traits are often difficult to detect despite the physiological and morphological incompatibilities that underlie disparate traits being well understood. However, recent studies that have corrected for individual quality have found trade-offs in human athletes performing various performance tasks. Few studies have found trade-offs among multiple performance tasks after correcting for individual quality in non-human animals because of the difficulty in motivating many animals to perform biomechanically different tasks. We examined potential trade-offs in maximal speeds among ten locomotor conditions that involved the utilization of different locomotor modes in cornsnakes (Pantherophis guttatus). Snakes were assessed during terrestrial lateral undulation, swimming, concertina movements (small and large width) and six conditions of arboreal locomotion (combinations of three perch diameters and two inclines). We found no trade-offs among locomotor conditions when analysing uncorrected speeds or speeds corrected for body condition. However, we found several trade-offs among modes and treatments for speeds corrected for individual quality. Terrestrial lateral undulation speeds were negatively related to speeds of concertina and two of the arboreal locomotion conditions. A trade-off between speeds on large and small perch diameters on a 30° incline was also detected and probably reflects potential conflicts in traits that maximize lateral undulation and concertina. arboreal, concertina, lateral undulation, locomotor mode INTRODUCTION For most animals, movement is crucial in determining how successful individuals are at defending resources, escaping predation, and locating and obtaining food, potential mates and optimal habitats (Arnold, 1983; Irschick & Garland, 2001; Biewener, 2003). To successfully complete many of these tasks, many animals must negotiate and manoeuvre through various habitats and substrates (Börger et al., 2008). When performing different tasks or moving on different substrates, compromises in performance capabilities among tasks are commonly present (Vanhooydonck et al., 2001; Irschick & Higham, 2016). These compromises or trade-offs can occur when different performance tasks cannot be simultaneously maximized because of conflicting physiological or biochemical mechanisms that underlie different tasks (Garland et al., 1995; Wilson & James, 2004; Irschick & Higham, 2016). At the muscle level, trade-offs between power and endurance occur owing to differences in the composition of red and white muscle fibres resulting in a speed–endurance trade-off (Rome et al., 1988; Garland et al., 1995; Wilson et al., 2002, 2004; Wilson & James, 2004). The presence of trade-offs results in constraints on certain types of performance that hinder movements and behaviours in some habitats which can influence fitness. Previous studies have found that some individuals are superior or inferior at multiple performance tasks simultaneously, thereby suggesting that an individual’s quality, resulting from inter-individual variation in physical fitness, health, nutrition, etc., confounds studies of trade-offs and must be accounted for when comparing multiple performance tasks (Van Damme et al., 2002). After correcting for individual quality, trade-offs between endurance and power (speed) tasks and between maximal performance of one task (specialist) and average performance during all tasks (generalist) were detected in human soccer players (Wilson et al., 2014). Similar trade-offs between pairs of different events were found only following a correction for individual quality in human decathletes (Van Damme et al., 2002; Careau & Wilson, 2017). Studies assessing performance trade-offs in non-human animals that correct for individual quality are rare, probably owing to the difficulties in motivating animals to perform biomechanically different tasks under controlled conditions (Wilson et al., 2014). However, correcting for individual quality did permit trade-offs to be detected in running speeds on different diameter substrates (terrestrial and arboreal) in the lizard Anolis carolinensis (Sathe & Husak, 2015). More recently, functional trade-offs were found in an arboreal marsupial (Dasyurus hallucatus) between sets of traits related to motor control and strength, which were more closely related to differences in body size than individual quality (Charters et al., 2018). In snakes, it has been suggested that trade-offs in performance are likely among disparate modes of limbless movement that can be altered depending on the characteristics of the environment being traversed (see Gray, 1946; Gans, 1974; Cundall, 1987; Jayne, 1988a, b). For example, trade-offs might occur between the biomechanically similar modes of terrestrial lateral undulation and swimming due to the differences in muscle activity requirements related to moving on land vs. water (Cundall, 1987; Jayne, 1988a). Other trade-offs in performance have been proposed between lateral undulation and concertina (Gerald & Claussen, 2007) and among different branch diameters, textures and inclines during arboreal limbless locomotion, which is due to alterations in the challenges associated with maintaining speed while simultaneously balancing and gripping to prevent falling in different arboreal contexts (Astley & Jayne, 2007; Gerald et al., 2008; Jayne & Hermann, 2011; Byrnes & Jayne, 2014). However, as has been observed in other taxonomic groups, studies that have investigated trade-offs in performance have mostly found either positive or no relationships among multiple limbless locomotor modes (Finkler & Claussen, 1999; Shine & Shetty, 2001; Gerald & Claussen, 2007; Isaac & Gregory, 2007; Gerald, 2017). A recent investigation found that 42 of 45 intraspecific comparisons among the performance of five snake species during four locomotor modes (terrestrial lateral undulation, swimming, concertina and arboreal) showed either positive or no relationship (Gerald, 2017). The aim of this study was to assess potential trade-offs in performance among various modes of limbless locomotion after correcting for individual quality, defined as the scalar variable from performance of multiple modes that are presumed to have some influence on fitness (see Wilson & Nussey, 2010). We hypothesized that negative relationships among kinematically different modes (e.g. lateral undulation and concertina) and positive relationships among kinematically similar modes (e.g. lateral undulation and swimming) will be detected only after correcting for individual quality. We also hypothesized that trade-offs among modes result from the underlying trade-off between maximizing speed (i.e. propulsion-based movements) and precision, where slower movements are needed to prevent mistakes in gripping and balance. For example, some modes (e.g. concertina and arboreal) require better precision for gripping and balance to optimize force production while reducing slipping. We predicted that trade-offs in speed will be present during arboreal movements among perch diameters and inclines that require different proportions of propulsion-based (i.e. undulatory) and precision-based (i.e. gripping and balance) movements. Travelling on smaller diameter and on inclined perches probably requires more motor skills for gripping because slipping and falling off arboreal perches is more likely (Byrnes & Jayne, 2014). Thus, we expect to observe trade-offs among diameters and inclined perches. MATERIAL AND METHODS Study species and husbandry Thirteen, unrelated subadult cornsnakes (Pantherophis guttatus, Linnaeus, 1766), relatively similar in size [snout–vent length (SVL): mean = 32.8 cm, range = 29.1–36.8 cm; mass: mean = 25.5 g, range = 16.3–35.1 g] and age, were acquired from Backwater Reptiles (Sacramento, CA, USA). Snakes were housed individually at room temperature (25 ± 0.5 °C) in 54 × 21 × 9-cm plastic trays within a custom-made rack system. Each tray contained newspaper bedding, water ad libitum, and heat tape below to provide a thermal gradient for thermoregulation. Snakes were fed pre-killed mice (Mus musculus) of the appropriate size once per week. Snakes were fasted at least 1 week prior to performance trials. Locomotor performance All locomotor trials were conducted at room temperature (25 ± 0.5 °C). Attempts were made to measure maximal speeds in all individual snakes during movement in each of ten locomotor conditions, which included terrestrial lateral undulation, aquatic lateral undulation (i.e. swimming), two conditions for concertina (small and large track widths), and six conditions for arboreal locomotion (three diameter and two incline perch combinations). For all locomotor treatments, snakes were videotaped to 60 frames s−1 (Casio Elixim Pro EX-F1) while being encouraged to move at maximal speed using either a painter’s brush or finger. Maximal speed was determined to be the fastest run of three successive trials of non-stop movement over a 75-cm segment of substrate. All individual snakes were assessed on all ten locomotor treatments. Order of treatments for each individual was randomized and at least 24 h was given for each snake between successive treatments. Terrestrial lateral undulation was assessed using a 3.0 × 0.75-m track containing terrarium carpet (Trafficmaster Pet Turf) that contained small projections (c. 0.1–0.5 mm high) needed for force generation characteristic of this mode (Jayne, 1986; Gerald, 2017). A linear trough (220 × 20 × 15 cm) filled the aged water equilibrated to room temperature (an aquatic heater was used to keep water at 25 °C) and marked at 25-cm intervals was used to quantify swimming speeds (Gerald, 2017). Concertina speeds were measured using the same track previously described to measure lateral undulation, but with the track width reduced to either 2.5× (small width) or 4.0× (large width) maximum body width. The use of body width-relative diameters was necessary because snakes used in the study varied in body size and because tunnel width relative to body width can influence concertina speeds (Gerald & Claussen, 2007). Instead of terrarium carpet, a smooth Plexiglas substrate was used to encourage the use of side-walls to generate the forces characteristic of concertina locomotion. Maximal arboreal speeds were ascertained on two horizontal, artificial cylindrical perches, of circular cross-section, positioned end-to-end (thereby producing a 2-m-long perch), and tightly wrapped in burlap-textured material to provide push-off points c. 0.5–1.4 mm high (Gerald et al., 2008; Gerald, 2017). Combinations of three perch diameters (3, 6 and 10 cm) and two incline treatments (0° and 30° uphill) were used as the six arboreal conditions. Arboreal locomotion involves a combination of undulatory and concertina-like movements that vary in proportions depending on the perch characteristics (Astley & Jayne, 2007; Jayne et al., 2015). We defined lateral undulation as non-stop movement as the entire body travels down the path determined by the push-off points in the texture of the perch. Concertina was determined by periodic stopping and gripping the perch with some parts of the body while other portions were pushed or pulled forward down the perch. Similar to the findings of Jayne et al. (2015), we observed that concertina movements were used more often as perch diameter decreased and on inclined perches. Statistical analyses The raw values of all speeds were standardized to produce a mean = 0 and standard deviation = 1 for each locomotor condition by subtracting the mean of all individuals from each observed value and dividing by the standard deviation (see Wilson et al., 2014), and hence referred to as standardized speeds. A principal component analysis (PCA) was performed on standardized speeds of all ten locomotor conditions. Scores from the first principal component (PC1) explained 41.4% of the variation in speeds and was therefore considered a measure of individual quality because all vectors loaded positively (Table 1); this indicates that some individuals were faster across most of the experimental locomotor treatments relative to other individuals that performed more poorly across treatments. The lack of significant correlations found between both mass and SVL and absolute speeds (P > 0.05) reduces the likelihood of body size influencing PC1. To correct for the influence of individual quality on speeds of each locomotor condition, residuals were calculated from regressions of standardized speeds and individual quality score (PC1) (Wilson et al., 2014). Positive and negative residuals represent higher and lower speeds relative to individual quality and are referred to as quality-corrected speeds. Thus, quality-corrected speeds can be defined as a measure of performance in P. guttatus that accounts for most variation in factors that can influence locomotor speeds (genetics, health, motivation, physiology, etc.) so that differences or similarities in speeds among locomotor treatments are due primarily to incompatibilities or similarities among locomotor modes. We also corrected standardized speeds to determine if trade-offs are revealed when accounting for variation related to body condition only. A body condition residual score was calculated using the residuals from an ordinary least squares regression of log body mass and log SVL (Cox & Calsbeek, 2015), which was significant (r2 = 0.69; N = 13; P < 0.001). Residuals of the regressions of standardized speeds and body condition residual score were calculated and are referred to as condition-corrected speeds. A repeated-measures ANOVA with Bonferroni corrections for pairwise comparisons was used to test for differences in speeds (non-standardized; non-corrected) among locomotor conditions. Pearson correlations were performed on standardized speeds, quality-corrected speeds and condition-corrected speeds for all ten locomotor conditions. All statistical analyses were conducted using XLSTAT software (Addinsoft, 2018). Table 1. Principal components analysis matrix showing percentage variance and the factor loadings of each of ten locomotor conditions PC1 PC2 PC3 % Variance 41.4 17.6 15.1 Arb sm 0° 0.70 0.22 0.31 Arb sm 30° 0.60 −0.45 −0.48 Arb med 0° 0.87 0.24 −0.23 Arb med 30° 0.82 −0.19 0.45 Arb lg 0° 0.30 −0.71 −0.36 Arb lg 30° 0.74 −0.15 0.39 Conc sm 0.69 0.37 −0.17 Conc lg 0.22 0.73 −0.24 LU 0.04 −0.56 0.24 Swim 0.05 0.05 0.78 PC1 PC2 PC3 % Variance 41.4 17.6 15.1 Arb sm 0° 0.70 0.22 0.31 Arb sm 30° 0.60 −0.45 −0.48 Arb med 0° 0.87 0.24 −0.23 Arb med 30° 0.82 −0.19 0.45 Arb lg 0° 0.30 −0.71 −0.36 Arb lg 30° 0.74 −0.15 0.39 Conc sm 0.69 0.37 −0.17 Conc lg 0.22 0.73 −0.24 LU 0.04 −0.56 0.24 Swim 0.05 0.05 0.78 Arb = arboreal; Conc = concertina; LU – terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large Table 1. Principal components analysis matrix showing percentage variance and the factor loadings of each of ten locomotor conditions PC1 PC2 PC3 % Variance 41.4 17.6 15.1 Arb sm 0° 0.70 0.22 0.31 Arb sm 30° 0.60 −0.45 −0.48 Arb med 0° 0.87 0.24 −0.23 Arb med 30° 0.82 −0.19 0.45 Arb lg 0° 0.30 −0.71 −0.36 Arb lg 30° 0.74 −0.15 0.39 Conc sm 0.69 0.37 −0.17 Conc lg 0.22 0.73 −0.24 LU 0.04 −0.56 0.24 Swim 0.05 0.05 0.78 PC1 PC2 PC3 % Variance 41.4 17.6 15.1 Arb sm 0° 0.70 0.22 0.31 Arb sm 30° 0.60 −0.45 −0.48 Arb med 0° 0.87 0.24 −0.23 Arb med 30° 0.82 −0.19 0.45 Arb lg 0° 0.30 −0.71 −0.36 Arb lg 30° 0.74 −0.15 0.39 Conc sm 0.69 0.37 −0.17 Conc lg 0.22 0.73 −0.24 LU 0.04 −0.56 0.24 Swim 0.05 0.05 0.78 Arb = arboreal; Conc = concertina; LU – terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large RESULTS Relationships among locomotor modes Non-standardized maximal speeds differed among locomotor modes, with the fastest speeds attained during aquatic and terrestrial lateral undulation, followed by concertina and arboreal, respectively (P < 0.001; Fig. 1). During arboreal movements, snakes were able to achieve faster speeds on smaller diameter perches (Fig. 1). When comparing standardized speeds among modes, we found no significant relationships among any locomotor mode and conditions (Table 2). After correcting for body condition, a positive relationship was found between terrestrial lateral undulation and swimming (r = 0.70; P < 0.05; Table 3). Table 2. Matrix of Pearson product moment correlations of the standardized speeds (not corrected for individual quality) of the ten locomotor conditions tested in 13 cornsnakes (Pantherophis guttatus). No significant correlations were detected Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.03 Arb med 0° 0.24 0.11 Arb med 30° 0.11 −0.14 0.16 Arb lg 0° 0.34 0.11 0.10 0.15 Arb lg 30° −0.15 −0.23 0.02 0.04 0.23 Conc sm 0.20 0.07 0.08 0.31 0.17 −0.05 Conc lg 0.05 0.33 −0.03 −0.05 0.03 0.15 0.34 LU 0.27 −0.38 −0.26 0.28 0.06 0.10 0.08 −0.17 Swim 0.12 −0.10 0.17 0.12 0.17 −0.22 0.25 0.13 0.41 Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.03 Arb med 0° 0.24 0.11 Arb med 30° 0.11 −0.14 0.16 Arb lg 0° 0.34 0.11 0.10 0.15 Arb lg 30° −0.15 −0.23 0.02 0.04 0.23 Conc sm 0.20 0.07 0.08 0.31 0.17 −0.05 Conc lg 0.05 0.33 −0.03 −0.05 0.03 0.15 0.34 LU 0.27 −0.38 −0.26 0.28 0.06 0.10 0.08 −0.17 Swim 0.12 −0.10 0.17 0.12 0.17 −0.22 0.25 0.13 0.41 Arb = arboreal; Conc = concertina; LU = terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large Table 2. Matrix of Pearson product moment correlations of the standardized speeds (not corrected for individual quality) of the ten locomotor conditions tested in 13 cornsnakes (Pantherophis guttatus). No significant correlations were detected Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.03 Arb med 0° 0.24 0.11 Arb med 30° 0.11 −0.14 0.16 Arb lg 0° 0.34 0.11 0.10 0.15 Arb lg 30° −0.15 −0.23 0.02 0.04 0.23 Conc sm 0.20 0.07 0.08 0.31 0.17 −0.05 Conc lg 0.05 0.33 −0.03 −0.05 0.03 0.15 0.34 LU 0.27 −0.38 −0.26 0.28 0.06 0.10 0.08 −0.17 Swim 0.12 −0.10 0.17 0.12 0.17 −0.22 0.25 0.13 0.41 Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.03 Arb med 0° 0.24 0.11 Arb med 30° 0.11 −0.14 0.16 Arb lg 0° 0.34 0.11 0.10 0.15 Arb lg 30° −0.15 −0.23 0.02 0.04 0.23 Conc sm 0.20 0.07 0.08 0.31 0.17 −0.05 Conc lg 0.05 0.33 −0.03 −0.05 0.03 0.15 0.34 LU 0.27 −0.38 −0.26 0.28 0.06 0.10 0.08 −0.17 Swim 0.12 −0.10 0.17 0.12 0.17 −0.22 0.25 0.13 0.41 Arb = arboreal; Conc = concertina; LU = terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large Table 3. Matrix of Pearson product moment correlations of the body condition-corrected standardized speeds of the ten locomotor conditions tested in 13 cornsnakes (Pantherophis guttatus). Significant correlations (0.05 level) are shown in bold type Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° 0.25 Arb med 0° −0.07 0.12 Arb med 30° 0.18 −0.35 0.13 Arb lg 0° 0.30 −0.03 0.04 0.31 Arb lg 30° −0.24 0.17 0.16 0.40 −0.18 Conc sm −0.29 0.08 −0.05 0.25 0.22 −0.21 Conc lg 0.10 0.16 0.35 0.07 0.30 −0.15 −0.16 LU −0.05 −0.25 −0.31 −0.34 0.34 −0.38 −0.24 −0.32 Swim −0.15 −0.29 −0.18 −0.27 0.11 −0.30 0.08 −0.20 0.70 Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° 0.25 Arb med 0° −0.07 0.12 Arb med 30° 0.18 −0.35 0.13 Arb lg 0° 0.30 −0.03 0.04 0.31 Arb lg 30° −0.24 0.17 0.16 0.40 −0.18 Conc sm −0.29 0.08 −0.05 0.25 0.22 −0.21 Conc lg 0.10 0.16 0.35 0.07 0.30 −0.15 −0.16 LU −0.05 −0.25 −0.31 −0.34 0.34 −0.38 −0.24 −0.32 Swim −0.15 −0.29 −0.18 −0.27 0.11 −0.30 0.08 −0.20 0.70 Arb = arboreal; Conc = concertina; LU = terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large Table 3. Matrix of Pearson product moment correlations of the body condition-corrected standardized speeds of the ten locomotor conditions tested in 13 cornsnakes (Pantherophis guttatus). Significant correlations (0.05 level) are shown in bold type Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° 0.25 Arb med 0° −0.07 0.12 Arb med 30° 0.18 −0.35 0.13 Arb lg 0° 0.30 −0.03 0.04 0.31 Arb lg 30° −0.24 0.17 0.16 0.40 −0.18 Conc sm −0.29 0.08 −0.05 0.25 0.22 −0.21 Conc lg 0.10 0.16 0.35 0.07 0.30 −0.15 −0.16 LU −0.05 −0.25 −0.31 −0.34 0.34 −0.38 −0.24 −0.32 Swim −0.15 −0.29 −0.18 −0.27 0.11 −0.30 0.08 −0.20 0.70 Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° 0.25 Arb med 0° −0.07 0.12 Arb med 30° 0.18 −0.35 0.13 Arb lg 0° 0.30 −0.03 0.04 0.31 Arb lg 30° −0.24 0.17 0.16 0.40 −0.18 Conc sm −0.29 0.08 −0.05 0.25 0.22 −0.21 Conc lg 0.10 0.16 0.35 0.07 0.30 −0.15 −0.16 LU −0.05 −0.25 −0.31 −0.34 0.34 −0.38 −0.24 −0.32 Swim −0.15 −0.29 −0.18 −0.27 0.11 −0.30 0.08 −0.20 0.70 Arb = arboreal; Conc = concertina; LU = terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large Figure 1. View largeDownload slide Differences in average maximal (non-standardized) speeds (cm s−1) among ten locomotor treatments consisting of three locomotor modes (lateral undulation, concertina and arboreal) measured in 13 cornsnakes (Pantherophis guttatus) (F9,108 = 17.3; P < 0.001). Swim = swimming; Terr = terrestrial; Sm width = small track width (2.5× maximum body width); Lg width = large track width (4.0× maximum body width); Small 0 = small experimental diameter perch with 0 incline; Small 30 = small experimental diameter perch on 30° uphill incline; Med 0 = intermediate experimental diameter perch with 0 incline; Med 30 = intermediate experimental diameter perch on 30° uphill incline; Lg 0 = largest experimental diameter perch with 0 incline; Lg 30 = largest experimental diameter perch on 30° uphill incline. Letters denote pairwise significant differences at the 0.05 level. Figure 1. View largeDownload slide Differences in average maximal (non-standardized) speeds (cm s−1) among ten locomotor treatments consisting of three locomotor modes (lateral undulation, concertina and arboreal) measured in 13 cornsnakes (Pantherophis guttatus) (F9,108 = 17.3; P < 0.001). Swim = swimming; Terr = terrestrial; Sm width = small track width (2.5× maximum body width); Lg width = large track width (4.0× maximum body width); Small 0 = small experimental diameter perch with 0 incline; Small 30 = small experimental diameter perch on 30° uphill incline; Med 0 = intermediate experimental diameter perch with 0 incline; Med 30 = intermediate experimental diameter perch on 30° uphill incline; Lg 0 = largest experimental diameter perch with 0 incline; Lg 30 = largest experimental diameter perch on 30° uphill incline. Letters denote pairwise significant differences at the 0.05 level. A number of trade-offs and positive associations were observed after correcting for individual quality (Table 4). Terrestrial lateral undulation was found to be positively related to swimming (r = 0.58; P < 0.05; Fig. 2) and negatively related to arboreal performance on the small-diameter perch at a 30° incline (r = −0.57; P < 0.05), arboreal performance on the intermediate-diameter perch with no incline (r = −0.71; P < 0.05), and concertina performance on the large track width (r = −0.62; P < 0.05; Fig. 2) when examining quality-corrected speeds (Table 4). Additionally, quality-corrected speeds of concertina (small width) were negatively related to those measured on the largest arboreal perch at 30° (r = −0.66; P < 0.05), whereas corrected concertina speeds on the largest width were positively related to those on the smallest arboreal perch at 30° (r = 0.65; P < 0.05; Table 4). Table 4. Matrix of Pearson product moment correlations of the individual quality-corrected standardized speeds of the ten locomotor conditions tested in 13 cornsnakes (Pantherophis guttatus). Significant correlations (0.05 level) are shown in bold type Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.49 Arb med 0° −0.16 −0.32 Arb med 30° −0.23 −0.14 −0.39 Arb lg 0° −0.12 −0.46 0.39 −0.18 Arb lg 30° 0.21 −0.77 −0.44 0.50 −0.43 Conc sm −0.09 0.22 0.18 −0.18 −0.15 −0.66 Conc lg −0.16 0.65 0.46 −0.22 −0.27 −0.31 0.33 LU −0.14 −0.57 −0.71 0.47 −0.04 0.25 −0.14 −0.62 Swim 0.11 −0.25 −0.08 0.59 0.10 0.12 −0.24 0.05 0.58 Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.49 Arb med 0° −0.16 −0.32 Arb med 30° −0.23 −0.14 −0.39 Arb lg 0° −0.12 −0.46 0.39 −0.18 Arb lg 30° 0.21 −0.77 −0.44 0.50 −0.43 Conc sm −0.09 0.22 0.18 −0.18 −0.15 −0.66 Conc lg −0.16 0.65 0.46 −0.22 −0.27 −0.31 0.33 LU −0.14 −0.57 −0.71 0.47 −0.04 0.25 −0.14 −0.62 Swim 0.11 −0.25 −0.08 0.59 0.10 0.12 −0.24 0.05 0.58 Arb = arboreal; Conc = concertina; LU = terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large Table 4. Matrix of Pearson product moment correlations of the individual quality-corrected standardized speeds of the ten locomotor conditions tested in 13 cornsnakes (Pantherophis guttatus). Significant correlations (0.05 level) are shown in bold type Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.49 Arb med 0° −0.16 −0.32 Arb med 30° −0.23 −0.14 −0.39 Arb lg 0° −0.12 −0.46 0.39 −0.18 Arb lg 30° 0.21 −0.77 −0.44 0.50 −0.43 Conc sm −0.09 0.22 0.18 −0.18 −0.15 −0.66 Conc lg −0.16 0.65 0.46 −0.22 −0.27 −0.31 0.33 LU −0.14 −0.57 −0.71 0.47 −0.04 0.25 −0.14 −0.62 Swim 0.11 −0.25 −0.08 0.59 0.10 0.12 −0.24 0.05 0.58 Arb sm 0° Arb sm 30° Arb med 0° Arb med 30° Arb lg 0° Arb lg 30° Conc sm Conc lg LU Arb sm 30° −0.49 Arb med 0° −0.16 −0.32 Arb med 30° −0.23 −0.14 −0.39 Arb lg 0° −0.12 −0.46 0.39 −0.18 Arb lg 30° 0.21 −0.77 −0.44 0.50 −0.43 Conc sm −0.09 0.22 0.18 −0.18 −0.15 −0.66 Conc lg −0.16 0.65 0.46 −0.22 −0.27 −0.31 0.33 LU −0.14 −0.57 −0.71 0.47 −0.04 0.25 −0.14 −0.62 Swim 0.11 −0.25 −0.08 0.59 0.10 0.12 −0.24 0.05 0.58 Arb = arboreal; Conc = concertina; LU = terrestrial lateral undulation; Swim = swimming; 0° = horizontal orientation (i.e. no incline); 30° = 30° uphill incline; sm = small diameter (Arb) or track width (Conc); med = intermediate diameter; lg = large diameter (Arb) or track width (conc). View Large Figure 2. View largeDownload slide Relationships between terrestrial lateral undulation and swimming speeds (A, B) and between terrestrial lateral undulation and concertina performed in the larger track width (4.0× maximum body width) (C, D) in cornsnakes (Pantherophis guttatus). No significant relationships were detected (P > 0.05) when comparing the standardized raw data (A: r = 0.41; C: r = −0.17). Significant positive (B) and negative (D) relationships were observed (P < 0.05) when comparing the standardized data corrected for individual quality between modes (B: r = 0.58; D: r = −0.62). Figure 2. View largeDownload slide Relationships between terrestrial lateral undulation and swimming speeds (A, B) and between terrestrial lateral undulation and concertina performed in the larger track width (4.0× maximum body width) (C, D) in cornsnakes (Pantherophis guttatus). No significant relationships were detected (P > 0.05) when comparing the standardized raw data (A: r = 0.41; C: r = −0.17). Significant positive (B) and negative (D) relationships were observed (P < 0.05) when comparing the standardized data corrected for individual quality between modes (B: r = 0.58; D: r = −0.62). Relationships among arboreal conditions Among the experimental arboreal locomotor conditions, no trade-offs were detected when examining non-corrected standardized speeds (Table 2). We also did not detect significant relationships when assessing condition-corrected speeds (Table 3). We found one negative correlation for quality-corrected data among the arboreal conditions. We found a trade-off in speeds between the small- and large-diameter perch for uphill (30°) movement (r = −0.77; P < 0.05; Table 4; Fig. 3). Figure 3. View largeDownload slide Relationship between arboreal performance during the largest and smallest experimental perch diameter on uphill (30°) speeds in cornsnakes (Pantherophis guttatus). This relationship was not statistically significant (P > 0.05) when comparing uncorrected standardized speeds (A: r = -0.23), but a significant correlation (P < 0.05) was found when comparing standardized speeds corrected for individual quality (B: r = −0.77). Figure 3. View largeDownload slide Relationship between arboreal performance during the largest and smallest experimental perch diameter on uphill (30°) speeds in cornsnakes (Pantherophis guttatus). This relationship was not statistically significant (P > 0.05) when comparing uncorrected standardized speeds (A: r = -0.23), but a significant correlation (P < 0.05) was found when comparing standardized speeds corrected for individual quality (B: r = −0.77). DISCUSSION Compromises in performance abilities (i.e. trade-offs) occur because the multiple performance traits many animals must utilize in nature cannot be simultaneously maximized (see Garland et al., 1995; Wilson et al., 2002; Irschick & Higham, 2016). However, many studies have failed to show trade-offs between multiple performance traits owing to the large amount of inter-individual variation often observed (e.g. Garland & Else, 1987; Jayne & Bennett, 1990; Herrel & Bonneaud, 2012; Gerald, 2017). We also found no trade-offs among locomotor modes and conditions in P. guttatus when analysing non-corrected standardized speeds. When correcting for individual quality, which results from differences in genetics, health, physical fitness, nutrition, etc., previous studies have detected trade-offs when examining multiple performance tasks in humans, thereby suggesting that individual quality is the primary cause of the inter-individual variation that often conceals trade-offs (Van Damme et al., 2002; Wilson et al., 2014; Careau & Wilson, 2017). Ours is the first study to show that variation in individual quality is the main factor obscuring trade-offs among multiple performance traits in a non-human animal. Although a recent study examining eight performance measures in northern quolls (Dasyurus hallucatus) showed trade-offs between pairs of performance traits that were mediated by body size, individual quality did not explain the variation across multiple performance tasks (Charters et al., 2018). The influence of variation in individual quality on various phenotypic traits is difficult to ascertain because of how individual quality has been defined and applied in various contexts (discussed in Moyes et al., 2009; Wilson & Nussey, 2010; Lailvaux & Kasumovic, 2011). Our study utilized Wilson & Nussey’s (2010) definition of individual quality as a scalar variable determined from the measurement of multiple traits and quantified as the first dimension of a PCA of variation among performance across biomechanically disparate modes of limbless locomotion. Note that we cannot discount the possibility that the loadings for PC1 result from variation in some factor other than individual quality. For example, it is possible that PC1 loadings are mostly a reflection of differences in body condition. However, our findings of only one positive relationship among all comparisons for condition-corrected speeds (Table 3) suggests that PC1 loadings result from factors beyond body condition, such as variation in genetics, motivation and physiology that we refer to as individual quality. Moreover, there is potential that PC1 loadings are due to differences in previous experience utilizing certain locomotor modes more than others (Gerald, 2017). However, individuals did not differ in the amount of time modes were used following acquisition and prior to the beginning of this study. We hypothesize that individual quality, which incorporates multiple factors, reasonably reflects the PC scores and can be used to assess hypothesized trade-offs in this context. Previous studies that have used this method of correcting for individual quality have uncovered functional trade-offs among multiple performance traits in human athletes (Wilson et al., 2014) and found trade-offs between investment in current and future reproduction in female mountain goats (Oreamnos americanus) (Hamel et al., 2009). At present, it is unclear how quality-corrected speeds among modes relate to individual fitness. We hypothesize that quality-corrected speeds represent speeds of each locomotor condition and mode minus the influence of individual variation in other traits that determine a snake’s individual quality. In nature, these quality-related traits combine with biomechanical demands to define locomotor performance that is ecologically relevant and can affect fitness. After correcting for both body condition and individual quality, we found a positive relationship between terrestrial lateral undulation speeds and swimming speeds. Terrestrial lateral undulation involves lateral bending that conforms to irregularities in the substrate to produce a path the body travels down while muscular activity propagates posteriorly as the snake moves forward (Gans, 1974; Jayne, 1988a). Moreover, the ventral scales possess a directional coefficient of friction that permits terrestrial lateral undulation on smooth substrates while lifting some portions of the body (Hu et al., 2009). Our finding that the performance of lateral undulation on land and in water are correlated (after correcting for quality) is similar to the findings of previous studies assessing relationships between these two modes of lateral undulation (Finkler & Claussen, 1999; Shine & Shetty, 2001; Shine et al., 2003; Gerald & Claussen, 2007; Gerald, 2017). This suggests that the kinematic similarities of lateral undulation on land vs. water have a larger impact on performance than the differences in the compliance of the media snakes are travelling through, which affects force generation and thrust. The trade-offs we found between speeds of terrestrial lateral undulation and those of concertina and two arboreal experimental conditions suggest that underlying physiological and morphological traits that enhance the performance of terrestrial lateral undulation may not completely align with those that improve movement through environments that require the utilization of concertina or arboreal locomotion. Concertina, which results from snakes moving through narrow tunnels or climbing up an inclined cylinder requiring alternating lateral bends to anchor the body while other portions of the body are moved forward before producing other static contact points, is an energetically expensive, stop-and-go mode of locomotion (Gans, 1974; Jayne, 1986; Walton et al., 1990; Jayne & Davis, 1991). Although most previous studies have failed to find correlations between the speeds of terrestrial lateral undulation and concertina (Gerald & Claussen, 2007; Gerald, 2017), a recent study found a negative relationship in one of five snake species studied, the bullsnake (Pituophis catenifer) (Gerald, 2017). Our results suggest that differences in individual quality do mask the detection of a performance trade-off owing to the potentially contradictory traits that enhance the kinematics of lateral undulation and concertina. Despite the known differences in kinematics between terrestrial lateral undulation and concertina (see Jayne, 1986), it is unclear which underlying traits are capable of producing an increase in performance during one mode at the expense of performance during the other. Our study revealed an arboreal trade-off between the largest and smallest perch diameter when moving up a 30° incline (Fig. 3B). Limbless arboreal locomotion usually consists of undulatory or concertina movements and is heavily influenced by differences in perch diameter, incline, compliance and surface roughness, and by the presence and characteristics of discontinuous gaps and adjacent branches or vegetation that can impede or facilitate movement (Astley & Jayne, 2007; Pizzatto et al., 2007; Gerald et al., 2008; Byrnes & Jayne, 2010, 2014; Jayne et al., 2015). Moreover, the need for balance and gripping while simultaneously generating force to produce forward momentum presents a unique kinematic challenge for snakes traversing a three-dimensional arboreal environment. Our findings suggest an interaction between perch diameter and incline that affects the proportion of balance and gripping vs. the need to use either a stop-and-go, concertina-like mode of forward progression or one that resembles lateral undulation. On smaller diameter perches, snakes stopped forward momentum more frequently to grip the perch by producing alternating left and right bends to maintain their centre of mass (COM) over the top of the perch to prevent toppling, thereby necessitating the utilization of concertina-like movements (Astley & Jayne, 2007). At larger perch diameters, snakes were able to utilize lateral undulation more easily by pushing off the small projections and using the ventral scales to push against the perch (Hu et al., 2009) while alternating left and right coils for balance to keep their COM on top of the perch. Snakes were able to maintain speeds without stopping to grip for balance more often on the larger perch diameters. We found more periodic stopping and gripping the perch to maintain balance, along with more concertina movements, during inclined movement on all diameters. Therefore, a slow form of lateral undulation is used more often when the perch is more horizontal and the diameter (relative to the snake’s length and width) is sufficient to keep the COM above the perch. Our findings agree with previous work that has shown that kinematic strategies related to locomotor mode and gripping are influenced by incline, diameter and surface roughness of the perch (Astley & Jayne, 2007; Gerald et al., 2008; Byrnes & Jayne, 2010, 2014; Jayne & Herrmann, 2011; Jayne et al., 2013, 2015). It is likely that the trade-off we observed among arboreal perch diameters is due mostly to the incompatible traits related to enhancing lateral undulation vs. concertina along with the associated gripping and balancing. This is further supported by our data that show that inclined arboreal speeds on the smallest perch diameter were negatively related to terrestrial lateral undulation speeds. Detailed kinematic and electromyographic studies would be needed to tease apart the mechanisms underlying these potential trade-offs. It has been suggested that a trade-off will exist between maximal speed and motor skill because increasing the power and rapidity of a movement should decrease the ability to produce more fined-tuned, accurate movements requiring more precision (Wilson et al., 2014; Wheatley et al., 2015; Nasir et al., 2017). When traversing arboreal substrates, animals typically must utilize a higher proportion of motor control compared to most terrestrial movements because of the increased importance of balance requiring more precise movements. Therefore, comparing locomotor performance on arboreal perches to that on terrestrial substrates in snakes is a good model to test this hypothesis, especially because the kinematics of arboreal locomotion in snakes is a derivative of modes used in many terrestrial situations (Gans, 1974; Jayne & Herrmann, 2011). The only trade-offs we found among the 18 comparisons of arboreal speeds to terrestrial speeds using quality-corrected data were that lateral undulation speed was negatively related to two of the arboreal conditions (Table 4). Although these relationships suggest a trade-off between power-based and precision-based movements in snakes, it is difficult to distinguish between the possibility that the negative correlations were due to conflicts between maximizing both lateral undulation and concertina. Correcting for individual quality has been shown to be successful in statistically detecting trade-offs among multiple performance tasks in human athletes (Van Damme et al., 2002; Wilson et al., 2014). Although our finding of six significant trade-offs among 45 comparisons following a correction for individual quality could result from the large number of correlations performed, the significant negative relationships we found all suggest trade-offs between lateral undulation and concertina. This is the first study to show that individual quality, defined as a collection of traits (e.g. genetics, health, motivation and physiology) that result in individuals performing better or worse across all performance tasks, is the main source of variation that masks trade-offs among multiple performance types in non-human animals. These trade-offs probably introduce constraints on some performance tasks that can impact habitat preferences and other important behaviours (finding food, avoiding predators, etc.) that affect fitness. Because of their ability to move in a variety of biomechanically distinct ways disparate from quadrupeds, snakes can be an excellent model to investigate the influence of habitat specialization, training and muscle plasticity on trade-offs among different performance tasks. ACKNOWLEDGMENTS This study was approved by the Nebraska Wesleyan University Institutional Animal Care and Use Committee (IACUC protocol 01-002255). This work was supported by grants from the National Center for Research Resources (5P20RR016469) and the National Institute for General Medical Science (NIGMS) (5P20GM103427), a component of the National Institutes of Health (NIH) awarded to G.W.G. We thank three anonymous reviewers who provided comments that improved the manuscript. We also thank Alyssa Marian and Amanda Schumacher for assistance with husbandry and conducting locomotor trials. REFERENCES Addinsoft . 2018 . XLSTAT v 2. Data Analysis and Statistics Software for Microsoft Excel. Available at: https://www.xlstat.com/en/ Arnold SJ . 1983 . Morphology, performance and fitness . American Zoologist 23 : 347 – 361 . Google Scholar Crossref Search ADS WorldCat Astley HC , Jayne BC . 2007 . Effects of perch diameter and incline on the kinematics, performance and modes of arboreal locomotion of corn snakes (Elaphe guttata) . The Journal of Experimental Biology 210 : 3862 – 3872 . Google Scholar Crossref Search ADS PubMed WorldCat Biewener AA . 2003 . Animal locomotion. Oxford : Oxford University Press . Google Preview WorldCat Börger L , Daiziel BD , Fryzell JM . 2008 . Are there general mechanisms of animal home range behavior? A review and prospects for future research . Ecology Letters 11 : 637 – 650 . Google Scholar Crossref Search ADS PubMed WorldCat Byrnes G , Jayne BC . 2010 . Substrate diameter and compliance affect the gripping strategies and locomotor mode of climbing boa constrictors . The Journal of Experimental Biology 213 : 4249 – 4256 . Google Scholar Crossref Search ADS PubMed WorldCat Byrnes G , Jayne BC . 2014 . Gripping during climbing of arboreal snakes may be safe but not economical . Biology Letters 10 : 20140434 . Google Scholar Crossref Search ADS PubMed WorldCat Careau V , Wilson RS . 2017 . Performance trade-offs and ageing in the ‘world’s greatest athletes’ . Proceedings of the Royal Society B 284 : 20171048 . Google Scholar Crossref Search ADS PubMed WorldCat Charters JE , Heiniger J , Clemente CJ , Cameron SF , Amir Abdul Nasir AF , Niehaus AC , Wilson RS . 2018 . Multidimensional analyses of physical performance reveal a size-dependent trade-off between suites of traits . Functional Ecology 32 : 1541 – 1553 . Google Scholar Crossref Search ADS WorldCat Cox RM , Calsbeek R . 2015 . Survival of the fattest? Indices of body condition do not predict viability in the brown anole (Anolis sagrei). Functional Ecology 29 : 404 – 413 . Google Scholar Crossref Search ADS WorldCat Cundall D . 1987 . Functional morphology . In: Siegel RA , Collins JT , Novak SS , eds. Snakes: ecology and evolutionary biology. Caldwell : The Blackburn Press , 106 – 142 . Google Preview WorldCat Finkler MS , Claussen DL . 1999 . Influence of temperature, body size, and inter-individual variation on forced and voluntary swimming and crawling speeds in Nerodia sipedon and Regina septemvittata . Journal of Herpetology 33 : 62 – 71 . Google Scholar Crossref Search ADS WorldCat Gans C . 1974 . Biomechanics. An approach to vertebrate biology. Ann Arbor : University of Michigan Press . Google Preview WorldCat Garland T Jr , Else PL . 1987 . Seasonal, sexual, and individual variation in endurance and activity metabolism in lizards . The American Journal of Physiology 252 : R439 – R449 . Google Scholar PubMed WorldCat Garland T Jr , Gleeson TT , Aronovitz BA , Richardson CS , Dohm MR . 1995 . Maximal sprint speeds and muscle fiber composition of wild and laboratory house mice . Physiology & Behavior 58 : 869 – 876 . Google Scholar Crossref Search ADS PubMed WorldCat Gerald GW . 2017 . Effects of morphology, substrate use, and potential trade-offs on locomotor performance during multiple modes of snake locomotion . Evolutionary Ecology Research 18 : 1 – 20 . WorldCat Gerald GW , Claussen DL . 2007 . Thermal dependencies of different modes of locomotion in neonate brown snakes, Storeria dekayi . Copeia 2007 : 577 – 585 . Google Scholar Crossref Search ADS WorldCat Gerald GW , Mackey MJ , Claussen DL . 2008 . Effects of temperature and perch diameter on arboreal locomotion in the snake Elaphe guttata . Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology 309 : 147 – 156 . Google Scholar Crossref Search ADS PubMed WorldCat Gray J . 1946 . The mechanism of locomotion in snakes . The Journal of Experimental Biology 23 : 101 – 120 . Google Scholar PubMed WorldCat Hamel S , Côté SD , Gaillard JM , Festa-Bianchet M . 2009 . Individual variation in reproductive costs of reproduction: high-quality females always do better . The Journal of Animal Ecology 78 : 143 – 151 . Google Scholar Crossref Search ADS PubMed WorldCat Herrel A , Bonneaud C . 2012 . Trade-offs between burst performance and maximal exertion capacity in a wild amphibian, Xenopus tropicalis . The Journal of Experimental Biology 215 : 3106 – 3111 . Google Scholar Crossref Search ADS PubMed WorldCat Hu DL , Nirody J , Scott T , Shelley MJ . 2009 . The mechanics of slithering locomotion . Proceedings of the National Academy of Sciences USA 106 : 10081 – 10085 . Google Scholar Crossref Search ADS WorldCat Irschick DJ , Garland T Jr . 2001 . Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system . Annual Review of Ecology and Systematics 32 : 367 – 396 . Google Scholar Crossref Search ADS WorldCat Irschick DJ , Higham TE . 2016 . Animal athletes: an ecological and evolutionary approach. Oxford : Oxford University Press . Google Preview WorldCat Isaac LA , Gregory PT . 2007 . Aquatic versus terrestrial locomotion: comparative performance of two ecologically contrasting species of European natricine snakes . Journal of Zoology 273 : 56 – 62 . Google Scholar Crossref Search ADS WorldCat Jayne BC . 1986 . Kinematics of terrestrial snake locomotion . Copeia 1986 : 915 – 927 . Google Scholar Crossref Search ADS WorldCat Jayne BC . 1988a . Muscular mechanisms of snake locomotion: an electromyographic study of lateral undulation of the Florida banded water snake (Nerodia fasciata) and the yellow rat snake (Elaphe obsoleta) . Journal of Morphology 197 : 159 – 181 . Google Scholar Crossref Search ADS WorldCat Jayne BC . 1988b . Muscular mechanisms of snake locomotion: an electromyographic study of the sidewinding and concertina modes of Crotalus cerastes, Nerodia fasciata and Elaphe obsoleta . The Journal of Experimental Biology 140 : 1 – 33 . WorldCat Jayne BC , Baum JT , Byrnes G . 2013 . Incline and peg spacing have interactive effects on the arboreal locomotor performance and kinematics of brown tree snakes, Boiga irregularis . The Journal of Experimental Biology 216 : 3321 – 3331 . Google Scholar Crossref Search ADS PubMed WorldCat Jayne BC , Bennett AF . 1990 . Selection on locomotor performance capacity in a natural population of garter snakes . Evolution 44 : 1204 – 1229 . Google Scholar Crossref Search ADS PubMed WorldCat Jayne BC , Davis JD . 1991 . Kinematics and performance capacity for the concertina locomotion of a snake (Coluber constrictor) . Journal of Experimental Biology 156 : 539 – 556 . WorldCat Jayne BC , Herrmann MP . 2011 . Perch size and structure have species-dependent effects on the arboreal locomotion of rat snakes and boa constrictors . The Journal of Experimental Biology 214 : 2189 – 2201 . Google Scholar Crossref Search ADS PubMed WorldCat Jayne BC , Newman SJ , Zentkovich MM , Berns HM . 2015 . Why arboreal snakes should not be cylindrical: body shape, incline and surface roughness have interactive effects on locomotion . The Journal of Experimental Biology 218 : 3978 – 3986 . Google Scholar Crossref Search ADS PubMed WorldCat Lailvaux SP , Kasumovic MM . 2011 . Defining individual quality over lifetimes and selective contexts . Proceedings of the Royal Society B 278 : 321 – 328 . Google Scholar Crossref Search ADS PubMed WorldCat Moyes K , Morgan BJ , Morris A , Morris SJ , Clutton-Brock TH , Coulson T . 2009 . Exploring individual quality in a wild population of red deer . The Journal of Animal Ecology 78 : 406 – 413 . Google Scholar Crossref Search ADS PubMed WorldCat Nasir AFAA , Clemente C , Wynn M , Wilson RS . 2017 . Optimal running speeds when there is a trade-off between speed and the probability of mistakes . Functional Ecology 31 : 1941 – 1949 . Google Scholar Crossref Search ADS WorldCat Pizzatto L , Almeida-Santos SM , Shine R . 2007 . Life-history adaptations to arboreality in snakes . Ecology 88 : 359 – 366 . Google Scholar Crossref Search ADS PubMed WorldCat Rome LC , Funke RP , Alexander RM , Lutz G , Aldridge H , Scott F , Freadman M . 1988 . Why animals have different muscle fibre types . Nature 335 : 824 – 827 . Google Scholar Crossref Search ADS PubMed WorldCat Sathe EA , Husak JF . 2015 . Sprint sensitivity and locomotor trade-offs in green anole (Anolis carolinensis) lizards . The Journal of Experimental Biology 218 : 2174 – 2179 . Google Scholar Crossref Search ADS PubMed WorldCat Shine R , Cogger HG , Reed RR , Shetty S , Bonnet X . 2003 . Aquatic and terrestrial locomotor speeds of amphibious sea-snakes (Serpentes, Laticaudidae) . Journal of Zoology 259 : 261 – 268 . Google Scholar Crossref Search ADS WorldCat Shine R , Shetty S . 2001 . Moving in two worlds: aquatic and terrestrial locomotion in sea snakes (Laticauda colubrina, Laticaudidae) . Journal of Evolutionary Biology 14 : 338 – 346 . Google Scholar Crossref Search ADS WorldCat Van Damme R , Wilson RS , Vanhooydonck B , Aerts P . 2002 . Performance constraints in decathletes . Nature 415 : 755 – 756 . Google Scholar Crossref Search ADS PubMed WorldCat Vanhooydonck B , Van Damme R , Aerts P . 2001 . Speed and stamina trade-off in lacertid lizards . Evolution 55 : 1040 – 1048 . Google Scholar Crossref Search ADS PubMed WorldCat Walton M , Jayne BC , Bennet AF . 1990 . The energetic cost of limbless locomotion . Science 249 : 524 – 527 . Google Scholar Crossref Search ADS PubMed WorldCat Wheatley R , Angilletta Jr MJ , Niehaus AC , Wilson RS . 2015 . How fast should an animal run when escaping? An optimality model based on the trade-off between speed and accuracy . Integrative and Comparative Biology 55 : 1166 – 1175 . Google Scholar PubMed WorldCat Wilson RS , David GK , Murphy SC , Angilletta Jr MJ , Niehaus AC , Hunter AH , Smith MD . 2017 . Skill not athleticism predicts individual variation in match performance of soccer players . Proceedings of the Royal Society B 284 : 2017095 . WorldCat Wilson RS , James RS . 2004 . Constraints on muscular performance: trade-offs between power output and fatigue resistance . Proceedings of the Royal Society B 271 : S222 – S225 . Google Scholar PubMed WorldCat Wilson RS , James RS , Kohlsdorf T , Cox VM . 2004 . Interindividual variation of isolated muscle performance and fibre-type composition in the toad Bufo viridus . Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 174 : 453 – 459 . Google Scholar PubMed WorldCat Wilson RS , James RS , Van Damme R . 2002 . Trade-offs between speed and endurance in the frog Xenopus laevis: a multi-level approach . The Journal of Experimental Biology 205 : 1145 – 1152 . Google Scholar PubMed WorldCat Wilson RS , Niehaus AC , David G , Hunter A , Smith M . 2014 . Does individual quality mask the detection of performance trade-offs? A test using analyses of human physical performance . The Journal of Experimental Biology 217 : 545 – 551 . Google Scholar Crossref Search ADS PubMed WorldCat Wilson AJ , Nussey DH . 2010 . What is individual quality? An evolutionary perspective . Trends in Ecology & Evolution 25 : 207 – 214 . Google Scholar Crossref Search ADS PubMed WorldCat © 2019 The Linnean Society of London, Biological Journal of the Linnean Society This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Correcting for individual quality reveals trade-offs in performance among multiple modes of limbless locomotion in snakes
JF - Biological Journal of the Linnean Society
DO - 10.1093/biolinnean/blz086
DA - 2007-06-20
UR - https://www.deepdyve.com/lp/oxford-university-press/correcting-for-individual-quality-reveals-trade-offs-in-performance-0u36vB7ujR
SP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -