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
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
Ground
on ground decreases, vertical increases,
with increasing Ta
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
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
Polyphenism in butterflies and moths the
pipevine swallowtail Battus philenor (Nice and
Fordyce 2006)
Dorsal view, male
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/ja
va/profile?symbolARIST2

• 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
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 10 Jun 19

• 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)

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
  (0L25D)
• 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
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

• Fig. 5  Effects of larval color on internal body
  temperatures in Battus philenor. Body
  temperatures (meanSE) of 11 pairs of black
  (filled circle) and red (open diamonds) larvae
  exposed to sunlight for 17 min

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)

Photo by John Ascher
Bombus vosnesenskii female queen Note Keys to
species found at
http//www.discoverlife.org/mp/20o?guideBumblebee
s

• Books by Bernd Heinrich
• Bumblebee Economics
• The hot-blooded insects strategies and
  mechanisms of thermoregulation.
• Insect Thermoregulation.

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