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Cambria, CA, 16 November 2013
Hold your Breath and Stay Fat: Sleep Apnea as a Water and Energy-Saving
Strategy in Elephant Seals
Presented by Susanna B. BlackwellWednesday, November 20, 13
Cambria, CA, 16 November 2013
Wednesday, November 20, 13
Cambria, CA, 16 November 2013
Elephant seals are desert animals!
Wednesday, November 20, 13
Dehydration = problem for all mammals. Loss of 15-20% body
water is fatal to most species.
Options if living in a dry environment:
- get better at extracting water from the environment
- evolve ways
of reducing water loss
- develop the ability to withstand temporary imbalances
Desert animals generally use a combination of physiological and
behavioral adaptations
Wednesday, November 20, 13
Physiological adaptations
Efficient kidneys
Hopping mouse (25x body fluids)Kangaroo ratSand ratSpringbok antelope
Nasal heat exchanger Giraffe
Reduction in metabolic rate
Springbok antelopeElandOryxOstrich
Use body as a heat sink
Camel (6° => 5 liters)Eland OryxSpringbok antelopeGrant’s gazelle
Wednesday, November 20, 13
Physiological adaptations
Efficient kidneys
Hopping mouse (25x body fluids)Kangaroo ratSand ratSpringbok antelope
✓
Nasal heat exchanger Giraffe ✓
Reduction in metabolic rate
Springbok antelopeElandOryxOstrich
✓
Use body as a heat sink
Camel (6° => 5 liters)Eland OryxSpringbok antelopeGrant’s gazelle
E. seals
Wednesday, November 20, 13
Two-sentence summary of what I will tell you today?
Elephant seals have an
unusual breath-holding ability, likely
acquired for procuring prey at sea.
They use this breath-holding
ability during long fasts on land to
save both water and energy.
Wednesday, November 20, 13
Apnea (apnoea) = suspension of external breathing. No movement of respiratory muscles and no change in lung volume.
Eupnea (eupnoea) = “normal” breathing
Sleep apnea in humans is a disorder (includes obstructive and central sleep apnea)
Terrestrial sleep apnea in seals is “normal”!
Weddell seal
Southern elephant
seal
Northern elephant
seal
Gray seal
Harbor seal
Hawaiian monk seal
Wednesday, November 20, 13
OUTLINE
Wednesday, November 20, 13
http://www.racerocks.com/racerock/archives_08/vidslashsleep.htm
Wednesday, November 20, 13
While on land, elephant seals abstain from food and water ...
~ 100 days in breeding males, particularly top-ranking males
Mass loss: 7.1 kg / day(average, ad. ♂)
Over entire season:41% top ♂34% low- ranking ♂
Wednesday, November 20, 13
While on land, elephant seals abstain from food and water ...
~ 100 days in breeding males, particularly top-ranking males~ 30 days in adult females that are nursing a pup
Wednesday, November 20, 13
While on land, elephant seals abstain from food and water ...
~ 100 days in breeding males, particularly top-ranking males~ 30 days in adult females that are nursing a pup
Day: 1 21 Day: 1 21
88%
75 %
35 %
15 %
4.5 %
55 %
Human
Elephant seal
Water FatWednesday, November 20, 13
While on land, elephant seals abstain from food and water ...
~ 100 days in breeding males, particularly top-ranking males~ 30 days in adult females that are nursing a pup~ 70 days in weaned pups, before their first trip to sea
Wednesday, November 20, 13
No eating, no drinking => very small fecal and urinary water losses In addition, urine is concentrated Evaporation from the skin is minimal So what’s left?
Wednesday, November 20, 13
No eating, no drinking => very small fecal and urinary water losses In addition, urine is concentrated Evaporation from the skin is minimal So what’s left?
Respiratory water loss!
Wednesday, November 20, 13
Nasal turbinates = counter-current heat exchanger
Huntley et al. 1985
No eating, no drinking => very small fecal and urinary water losses In addition, urine is concentrated Evaporation from the skin is minimal So what’s left?
Respiratory water loss!
Wednesday, November 20, 13
Nasal turbinates = counter-current heat exchanger
Adult ♂
Wednesday, November 20, 13
Nasal turbinate: how it works
Air
OUTSIDE
---->
---->
---->
---->
LUNGS
Bone
Vascularized flesh (w / mucous)
NASAL TURBINATE
- Estimated surface area of 3140 cm2 in adult males- Allows 92% respiratory water recovery (sheep: 24%)
Wednesday, November 20, 13
Elephant seals do long fasts
They have a well-developed adaptation (the nasal turbinates) to cut down on their biggest water loss (respiratory water loss)
All their water is obtained from burning fat
Saving (water) would be a good idea, because you then also loose less weight!
Wednesday, November 20, 13
Elephant seals do long fasts
They have a well-developed adaptation (the nasal turbinates) to cut down on their biggest water loss (respiratory water loss)
All their water is obtained from burning fat
Saving (water) would be a good idea, because you then also loose less weight!
Sleep apnea = suspected of playing a role
Do all age groups use it?
Is it an ability that gets developed with age?
What difference does it end up making over days and weeks?
Wednesday, November 20, 13
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:5.5 min
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:3.2 min
Terrestrial neonates: more resistant to asphyxiation
than adults; this tolerance to asphyxia disappears early in development.
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:8.2 min
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:12.4 min
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:16.4 min
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:23.1 min
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:21.2 min
Wednesday, November 20, 13
N SP Yg W Old W J Sa M Ad F Ad M0
2
4
6
8
10
12
14M
ea
n A
pn
ea
Du
ratio
n (
min
)20
21
34
18
11
2020
19
N = neonates (1-4 d)SP = suckling pups (5-28 d)Yg W = young weanlings (25-60 d)Old W = old weanlings (61-100 d)J = juveniles (1-2 y)Sa M = subadult males (5-7 y)Ad F = adult females (3-10 y) Ad M = adult males (8-14 y)
Longest apnea:14.3 min
Wednesday, November 20, 13
What have we learned?
All age and sex categories of
elephant seals breathe apneustically.
Most of the development of this
behavior takes place during the post-
weaning fast.
==> therefore focus, in second part, on the period from weaning to the return to land after the first trip to sea
Wednesday, November 20, 13
Goal: to prove that sleep apnea makes a difference
How to do that: compare water loss between
Wednesday, November 20, 13
Goal: to prove that sleep apnea makes a difference
How to do that: compare water loss between
CharlieUses sleep apnea
HugoDoes not use sleep apnea
Wednesday, November 20, 13
Goal: to prove that sleep apnea makes a difference
How to do that: compare water loss between
CharlieUses sleep apnea
HugoDoes not use sleep apnea
How many breaths per
day
How much water lost per breath
+ ==>Water loss for Charlie
Water loss for HugoΔ
(diff.)
Remember: breathing is the biggest avenue of water loss during the fast
Wednesday, November 20, 13
Goal: to prove that sleep apnea makes a difference
How much time in
terrestrial apnea
How much time in aquatic apnea
+ ==> Total amount of time per day in eupnea
Wednesday, November 20, 13
Goal: to prove that sleep apnea makes a difference
How much time in
terrestrial apnea
How much time in aquatic apnea
+ ==> Total amount of time per day in eupnea
x
Breathing rate
==>Total number of breaths per day
Wednesday, November 20, 13
Goal: to prove that sleep apnea makes a difference
How much time in
terrestrial apnea
How much time in aquatic apnea
+ ==> Total amount of time per day in eupnea
x
Breathing rate
==>Total number of breaths per day
Temperature and relative humidity
==>Water loss per breath
Wednesday, November 20, 13
Goal: to prove that sleep apnea makes a difference
How much time in
terrestrial apnea
How much time in aquatic apnea
+ ==> Total amount of time per day in eupnea
x
Breathing rate
==>Total number of breaths per day
+
Temperature and relative humidity
==>Water loss per breath
==>
Water loss for CharlieWater loss for Hugo
Wednesday, November 20, 13
Problem: how to record apneas day and night
Wednesday, November 20, 13
Problem: how to record apneas day and night
Hea
rt R
ate
(BP
M)
Time (min)
We’re in luck: there is a relationship between heart rate and breathing!
Wednesday, November 20, 13
Tattletale Lite Data Logger- Heart rate (modified Polar jogger’s system)- Activity (motion switch)- Temperature (thermistor)- Presence in and out of the water (salt switch)
Wednesday, November 20, 13
Yearling JET2
Wednesday, November 20, 13
Example records: yearling 1 on the beach
Time (minutes)Hea
rt R
ate
(BP
M) a
nd T
empe
ratu
re (°
C)
Wednesday, November 20, 13
Example records: yearling 2 on the beach
Time (minutes)Hea
rt R
ate
(BP
M) a
nd T
empe
ratu
re (°
C)
Wednesday, November 20, 13
Example records: weaner coming out of the water
Time (minutes)Hea
rt R
ate
(BP
M) a
nd T
empe
ratu
re (°
C)
Wednesday, November 20, 13
Percentage time spent in terrestrial apnea vs time-of-dayM
ean
% o
f eac
h H
our S
pent
in T
erre
stria
l Apn
ea
Time of Day (hrs)
Time of Day (hrs)Wednesday, November 20, 13
Percentage time spent in the water vs time-of-dayM
ean
% o
f eac
h H
our S
pent
in th
e W
ater
Time of Day (hrs)
Time of Day (hrs)Wednesday, November 20, 13
Percentage time spent in terrestrial apnea vs age
Age (days)
Mea
n %
of e
ach
Day
Spe
nt in
Ter
r. A
pnea
Wednesday, November 20, 13
Percentage time spent in the water vs ageM
ean
% o
f eac
h D
ay S
pent
in th
e W
ater
Age (days)Wednesday, November 20, 13
Total percentage time spent in apnea vs ageM
ean
% o
f eac
h D
ay S
pent
in A
pnea
Age (days)Wednesday, November 20, 13
OUTLINE So does sleep apnea make a difference?
We still need:- water loss per breath- breathing rates
Then we can compare daily respiratory water loss between
CharlieUses sleep apnea
HugoDoes not use sleep apnea
&
Wednesday, November 20, 13
Eupneic breathing rateB
reat
hing
Rat
e (b
reat
hs /
min
)
Age (days)Wednesday, November 20, 13
Eupneic breathing rateB
reat
hing
Rat
e (b
reat
hs /
min
)
Age (days)
Humans?
Wednesday, November 20, 13
Breaths / day
AgeAge Br / day apnea Br / day no apnea Increase (%)
W 50 days 9630 12,850 33
65 days 7860 10,260 31
80 days 6410 8670 35
95 days 5240 7850 50
Y ~290 days 6640 11,680 76
Wednesday, November 20, 13
Water loss / breath- Varies with temperature and humidity
Hours of the Day
Tem
p. (°
C)
Rel
. Hum
. (%
)
- Where weanlings spend 80% of their time:50 mg H2O / breath (26-80 mg / breath)
Wednesday, November 20, 13
Respiratory water loss for Charlie and Hugo (“average weaners”, 131 kg, 68 days old)
Hours of the Day
Gra
ms
H2O
lost
/ hr
Wednesday, November 20, 13
Respiratory water loss for Charlie and Hugo (“average weaners”, 131 kg, 68 days old)
Hours of the Day
Gra
ms
H2O
lost
/ hr
CharlieUses sleep apnea
HugoDoes not use sleep apnea
378 g
529 g121%87%
As a % of the H2O available for respiratory water loss:
Wednesday, November 20, 13
AcknowledgmentsFor the use of pictures I thank the Pinniped Cognition and Sensory Systems Laboratory (UCSC), in particular Colleen Reichmuth and Caroline Casey, as well as my former advisor Burney Le Boeuf. Images obtained with authorization from NMFS. Do not use or post this material without permission from the author.
Wednesday, November 20, 13