Thermoregulation

1. Thermoregulation Peter B. McEvoy Oregon State University Corvallis

2. Classifying Thermal Relationships Homeotherm Body Temperature Tb Poikilotherm Ambient Temperature Ta

3. Homeothermy in EctothermsHyles lineata (Lepidoptera: Sphingidae) • Occurs in Mojave desert of SW USA • Polyphagous on desert annuals • Abundant in April and May, dormant rest of year • Population size varies drastically yr to yr • Caterpillars regulate body temperature Tb through position and postural changes

4. Caterpillars Maintain Body Temperatures Above Ambient Tb = Ta Tb – Ta is greater for low T than for high

5. sun wind How Do Caterpillars Maintain Steady Tb Above Ta? • By exploiting thermal heterogeneity of it microhabitat through position and postural changes • As Ta increases mid-day, spends less time on ground and more on plant (can feed either on ground or plant) • On warm days, as temperature increases, spends more time in vertical position on stem

6. Shifts in Location and Posture With Changing T on Hot and Cold Days  Location  Posture Ground Vertical Hot Cold Time % on ground decreases, % vertical increases, with increasing Ta Ground Vertical Temp

7. Environmental Uncertainty and Evolution of Physiological Adaptations in Colias Butterflies • Variation in melanin on the underside of the hind wing, seasonal polyphenism • Allows insect to absorb solar energy and warm more quickly to 35-38oC required for flight • Intraspecific and interspecific variation

8. MALE (DORSAL) SUMMER FORM MALE (DORSAL) WINTER FORM Orange Sulphur (Colias eurytheme) http://www.dallasbutterflies.com/Butterflies/html/eurytheme.html

9. Adjusting Phenotype to Environmental Regime • If cues to thermal regime, two factors contribute to uncertainty • Noise in the signal • Magnitude (or strength) of the signal • If cues to photoperiod • Signal noise free • Free to respond to lack of accuracy with which signal predicts temperature

10. Seasonal, Inter-Generational Variation in Hindwing Underside Coloration in Colias eurytheme in relation to photoperiod Short day, low reflectance, high melanin Long day, high reflectance, low melanin

11. Predicting Thermal Regimes From Photoperiod Cycles Thermoperiod and photoperiod out of phase Slope (signal strength) and scatter (precision in prediction) Temperature

12. Dorsal view, male Polyphenism in butterflies and moths:the pipevine swallowtail Battus philenor (Nice and Fordyce 2006) Dorsal view, female Larvae are red in AZ to western TX Larvae are black in CA and SE USA • In South Texas, both forms occur • Each population, CA and Tx, has potential to produce either form • Color cued directly to temperature • Color can be changed at each larval molt Ventral view

13. Aristolochia host plantshttp://plants.usda.gov/java/profile?symbol=ARIST2 A. recta

14. Aristolochia serpentariaAristolochiaceae

15. Thermoregulation by an Ectotherm • Larvae of the pipevine swallowtail butterfly, Battus philenor, employ behavioral and phenotypic plasticity as thermoregulatory strategies • Two years of field observations in south Texas: • Behavior. Larvae were also observed to shift their microhabitats by climbing on non-host vegetation and avoided excessive heat in their feeding microhabitat • Phenotypic plasticity. Proportion of red larvae increases with increasing daily temperatures as the growing season progresses

16. Proportion of red larvae increases with increasing daily temperatures as the growing season progresses Fig. 2  Proportion of pipevine swallowtail larvae (Battus philenor) at the Freeman Ranch, TX field site observed exhibiting the red phenotype from April to June. Data from field surveys conducted in 2003 (open circle) and 2004 (open square) Color cued directly to temperature and not photoperiod Color can change at each molt depending on temperature experienced by larva Drop in proportion of red larvae late in the season allegedly due to unseasonably cold temperatures (no evidence given) Apr 10Jun 19

17. Experimental MethodsEffect of temperature on larval color and performance • Common garden experiment in temperature-controlled environments to assess the relative contributions of heritable variation and phenotypic plasticity to color variation • Origins of larvae: Ten half-sib (possibly full-sib given sperm precedence) families, 2 populations (CA and TX) • Treatments. Reared under conditions of constant temperature (24, 30, 36, 40 oC) and darkness (0L:25D) • Responses: Larval performance measured in two ways: time to pupation (days) and pupal mass (mg) • Analysis: Two mixed model ANOVAs used to test for effects of family, population (CA vs. TX), and temperature on time to pupation and pupal weight

18. Probability of red larval phenotype increases with max daily temperature over range 24-36 oC • Critical temperature (50% red) ~ 30-31 o C

19. No among-family or between-population variation in coloration detected, but there were effects of temperature on days to pupation and pupal mass Significant terms from ANOVAs A, Response: Time to pupation – Population – CA take longer than TX Temperature – shorter at higher T Family (Population) Family (Population) x Temperature (lines appear to be parallel) ?? B. Response: Pupal Mass Population – CA heavier at low T Temperature – lighter at high T Population x Temperature Family (Population) x Temperature Note: 40oC lethal maximum

20. Red larvae maintain lower body temperatures in full sunlight • Fig. 5  Effects of larval color on internal body temperatures in Battus philenor. Body temperatures (mean±SE) of 11 pairs of black (filled circle) and red (open diamonds) larvae exposed to sunlight for 17 min 6.85 oC > ambient 3.81 oC > ambient However, mean (± SE) body temperatures Black 44.91 ± 1.16 o C Red 41.87± 1.46 o C Appear to be above the lethal maximum of 40 o C - so we lack evidence to conclude ‘red phenotype… a mechanism to avoid internal temperatures above the lethal maximum’

21. Warming up by Basking

22. Morphology and Thermoregulation • Insulation – air sacs, scales, setae • Color – dark wing undersides • Stilts add Parasols – ground dwelling beetles on host sands of Namib Desert • Countercurrent and Alternating-Current Heat Exchanges as in Bumblebee

23. Stilts and ParasolsTenebrionidae of the Namib Desert The head-standing beetle (Onymacris unguicularis) creeps to the crest of a dune when fog is present, faces into the wind and stretches its back legs so that its body tilts forward, head down. As fog precipitates onto its body and runs down into its mouth the beetle drinks (Armstrong 1990).

24. Larvae of Australian sawfly Perga dorsaliscool evaporatively from back using rectal fluid

25. Apache cicada Sonoran desert Dicerooproctoa apache • Among the loudest insects on record • Sings when TA 40oC in shade • Keeps cool by evaporative cooling from fluid shed from dorsal pores • Extravagant water loss for desert insect made possible by xylem feeding

26. Warming Up by Shivering • Who does it?Found among large, active flyers across the insects • dragonflies (Odonata) • moths and butterflies (Lepidoptera) • katydids (Orthoptera) • cicadas (Clypeorrhyncha or Homoptera) • flies (Diptera) • beetles (Coleoptera) • wasps and bees (Hymenoptera) • How do they do it?Involves disengaging flight muscles form wings and synchronous contractions of muscles that normally alternate in flight • Who does it best?Honey bees and bumble bees represent the zenith of shivering response among any host-blooded animal (invertebrate and vertebrate)

27. Bumblebees out in the cold • Bumblebees occur throughout the temperature region and on cool mountaintops in the tropics • They can forage and fly at or near 0 o C after they are heated up (depending on body size and availability of fuel) Books by Bernd Heinrich • Bumblebee Economics • The hot-blooded insects: strategies and mechanisms of thermoregulation. • Insect Thermoregulation. Photo by John Ascher Bombus vosnesenskii female queen Note: Keys to species found at http://www.discoverlife.org/mp/20o?guide=Bumblebees

28. Regulation of body temperature in bumblebees (Ch 6 in Heinrich) • Pubescence – How can the contribution to thermoregulation be separated from alternative functions? • Body Mass – Small bees cool faster than larger bees, but both large and small bees maintain similar Tth. How? • Brood incubation – How is heat generated in the thorax transferred to abdomen and brood? • Ovary incubation – Arctic queens maintain higher Tabd than New England counterparts. Why? • Circulatory Anatomy – How do counter-current exchange and alternating current regulate body temperatures? • Evaporative cooling by regurgitation – How does regurgitation help regulate head temperature?

29. Thoracic and Abdominal Temperatures of bumblebee Bombus vosnesenskii Queen in continuous flight Tth is stabilized independently of ambient temperature

30. Countercurrent and Alternating Current • Countercurrent flow recovers heat from thorax by passing cold, incoming flow from abdomen by the warm, outgoing flow from the thorax  prevents excessive cooling • Alternating current removes heat from thorax by alternating warm outgoing and cool incoming flow  prevents excessive heating

31. High artic bumblebeeBombus polaris By incubating brood with abdomen, queen can produce a batch of workers in ~2 weeks http://pick4.pick.uga.edu/mp/20q

32. Summary • Insect performance depends on temperature • Thermoregulation allows some insects a measure of independence from variation in the thermal environment • Biochemical, physiological, behavioral, morphological mechanisms involved • Thermoregulation has consequences from individual insects to populations and communities