Research ArticleECOLOGY

Seasonal reproductive endothermy in tegu lizards

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Science Advances  22 Jan 2016:
Vol. 2, no. 1, e1500951
DOI: 10.1126/sciadv.1500951
  • Fig. 1 Life cycle and seasonal changes in the daily profile of body temperature variation in the tegu lizard, with concomitant changes in the outside and burrow temperatures.

    (A to C) The annual cycle (A) of tegu lizards is characterized by a reproductive season of mating and egg laying, a postreproductive season during the wet, warm summer months, a period of prolonged entrance into burrows during inclement weather, before a dormant period during the dry winter months. Averaged (±SEM; n = 4) monthly values (B) of tegu, burrow, and sunlight are shown plotted against hour of the day for the four periods of the year. The temperature difference (ΔT) between tegu and burrow temperature at the coldest time of the day (typically 4:00 a.m. to 6:00 a.m.) when tegus are inside their burrows is shown for the four different months (C). The temperature difference between tegu and burrow was greatest during the reproductive period in the month of October, as denoted by the asterisk (F3,9 = 43.2; P < 0.001).

  • Fig. 2 Infrared thermal images of tegu lizards following prolonged absence of solar heat gain.

    (A and B) A tegu lizard viewed before emerging from its burrow at first light in the morning (6:00 a.m.) during the reproductive season, demonstrating thermogenesis in an outside burrow (A). On a separate occasion, tegu lizards were imaged (10:00 a.m.) after extensive equilibration in a constant temperature environmental chamber, demonstrating cool skin temperature (B) whereas the core temperature, recovered from implanted data loggers, was much warmer.

  • Fig. 3 Body temperature–ambient temperature differences in outdoor burrows and under indoor conditions in male and female tegus.

    Temperature differentials (mean daily values from the coldest period of the day: 4:00 a.m.) for individual tegus held under seminatural outdoor conditions for 7 days (TbTburrow) and subsequently after transfer to constant temperature conditions indoors for 7 days (TbTchamber). The thermogenic response observed indoors shows strong correlations with the thermogenic response observed outdoors as well as with sex, but not with body mass (r2 = 0.352; outdoor P = 0.016; sex P = 0.037; mass P = 0.85), with males having an indoor ΔT 0.29°C cooler than females.

  • Fig. 4 Thermogenesis correlates with HRs in tegus in natural enclosures.

    (A) Average (±SEM; shaded area) daily ΔT values (TteguTburrow) obtained during the daily minimum body temperature period (between 4:00 a.m. and 6:00 a.m.) from tegu lizards (n = 4) free to behave within outdoor enclosures. (B) Continuous records of average HRs (± SEM; shaded area) from the same time period of each day are also shown. Discrete feeding events are marked by small vertical lines in (A). The elevation in ΔT shows a strong correspondence (r2 = 0.56) to the seasonal elevation in HR that cannot be explained strictly on the basis of biochemical Q10 effects alone (that is, HR from July to November increases from 3 to 18 beats/min, whereas body temperature itself only changes from 16° to 26°C; the estimated Q10 for this would be 6, which far exceeds normal biochemical Q10 values of 2 to 3). Inset figure shows ΔT correlation with HR [type II Wald χ2df = 1 = 129; P < 0.0001] for the fed (gray symbol) and unfed (open symbols) periods; neither feeding status [type II Wald χ2df = 1 = 1.93; P = 0.16] nor body mass [type II Wald χ2df = 1 = 1.74; P < 0.18] had effects on ΔT.

  • Fig. 5 Thermogenesis in tegu lizards depends on changes in metabolism and in whole-body thermal conductance.

    (A and B) Proposed model of seasonal endothermy in tegu lizards obtained from monthly averaged (early morning, predawn; n = 4 animals, two males and two females; 344 days of observations) HR values (A) and associated predicted metabolic rates (B) [from Piercy et al. (34)] from the postreproductive period (PR), entrance into dormancy period (EN), dormancy period (DR), and reproductive season (RS). Between the winter dormant period and the reproductive season, HR increases more than sixfold (despite body temperature changing by less than 10°C; see mean temperature ± SEM). (C) Graphical representation of the calculated relationship between thermal conductance and ΔT at different levels of metabolic rate for lizards. The thermal conductance for tegus (see fig. S6) is plotted against the ΔT values obtained for the nonreproductive tegus (solid circle; April) and reproductive tegus (open circle; October). Isopleths (gray lines) indicate the fold increase from the dormancy metabolic rate (of a tegu at Tb = 25°C) needed to produce the observed change in ΔT. The values calculated are consistent with those measured. Small changes in thermal conductance can have large effects on the ΔT. Squares represent conductance values (for comparison) from 300-g agamid lizards with ectothermic rates of metabolism, showing that a change from high air flow (filled) to low air flow (open) conditions in a burrow would have little effect on ΔT.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/2/1/e1500951/DC1

    Fig. S1. Temperature differentials for tegus (n = 11) held under constant temperature conditions (Ta = 18°C) indoors with and without a photoperiod plotted against days after transfer indoors (±SD, one direction, gray area).

    Fig. S2. Mean (±SD) temperature differences (A) between tegu (Tb), skin (Ts), and ambient (Ta) temperature in a seminatural burrow (B), indoor chamber with (C-P) and without (C-NP) a photoperiod.

    Fig. S3. Transient thermal changes in tegu lizards associated with photoperiod.

    Fig. S4. Trace from a tegu in a natural enclosure during 3 days in January when it did not emerge out of its burrow.

    Fig. S5. Average (±SEM) minimum daily HRs (that is, between 4:00 a.m. and 6:00 a.m.) as a function of body temperature in tegu lizards in seminatural outdoor enclosures.

    Fig. S6. Thermal equilibrium curves from tegus that had previously warmed in the sun and then transferred themselves to their lower temperature burrows.

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Temperature differentials for tegus (n = 11) held under constant temperature conditions (Ta = 18°C) indoors with and without a photoperiod plotted against days after transfer indoors (±SD, one direction, gray area).
    • Fig. S2. Mean (±SD) temperature differences (A) between tegu (Tb), skin (Ts), and ambient (Ta) temperature in a seminatural burrow (B), indoor chamber with (C-P) and without (C-NP) a photoperiod.
    • Fig. S3. Transient thermal changes in tegu lizards associated with photoperiod.
    • Fig. S4. Trace from a tegu in a natural enclosure during 3 days in January when it did not emerge out of its burrow.
    • Fig. S5. Average (±SEM) minimum daily HRs (that is, between 4:00 a.m. and 6:00 a.m.) as a function of body temperature in tegu lizards in seminatural outdoor enclosures.
    • Fig. S6. Thermal equilibrium curves from tegus that had previously warmed in the sun and then transferred themselves to their lower temperature burrows.

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