Ballistic tongue projection in chameleons maintains high performance at low temperature

Abstract

Environmental temperature impacts the physical activity and ecology of ectothermic animals through its effects on muscle contractile physiology. Sprinting, swimming, and jumping performance of ectotherms decreases by at least 33% over a 10 degrees C drop, accompanied by a similar decline in muscle power. We propose that ballistic movements that are powered by recoil of elastic tissues are less thermally dependent than movements that rely on direct muscular power. We found that an elastically powered movement, ballistic tongue projection in chameleons, maintains high performance over a 20 degrees C range. Peak velocity and power decline by only 10%-19% with a 10 degrees C drop, compared to >42% for nonelastic, muscle-powered tongue retraction. These results indicate that the elastic recoil mechanism circumvents the constraints that low temperature imposes on muscle rate properties and thereby reduces the thermal dependence of tongue projection. We propose that organisms that use elastic recoil mechanisms for ecologically important movements such as feeding and locomotion may benefit from an expanded thermal niche.

Fig. 1.

Mean temperature coefficients (Q₁₀) with SE bars for tongue projection (green) and retraction (gold), indicating the factor by which each performance parameter changes over 10 °C. Note the consistently lower values for projection versus retraction. Q₁₀ was calculated as the average of each individual's Q₁₀ value for that parameter; individual Q₁₀ values were calculated from interpolated performance values at an average projection distance of 12.5 cm (from performance values regressed against projection distance).

Fig. 2.

Performance parameters (mean ± SE) as a percent of maximum for tongue projection and retraction, showing low thermal dependence of projection (green) compared with retraction (gold). Absolute values of means are shown in native units. Values were calculated as the average of each individual's value for that parameter; individual values were interpolated at an average projection distance of 12.5 cm (from performance values regressed against projection distance).

Fig. 3.

Kinematic and dynamic profiles from two representative feedings of similar projection distance showing similar peak values for projection at 15 °C and 35 °C, compared with dissimilar values for retraction at the two temperatures. Retraction is analyzed only until the tongue reaches the entoglossal process. Profiles are overlaid at the time of maximum projection distance (dashed line). Power values are not corrected for muscle mass (2× for projection and 4× for retraction).