Hold your Breath and Stay Fat: Sleep Apnea as a Water and Energy-Saving Strategy in Elephant Seals

Hold your Breath and Stay Fat: Sleep Apnea as a Water and Energy-Saving Strategy in Elephant Seals Cambria, CA, 16 November 2013 Presented by Susanna B. Blackwell

Cambria, CA, 16 November 2013

Elephant seals are desert animals! Cambria, CA, 16 November 2013

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

Physiological adaptations Efficient kidneys Nasal heat exchanger Reduction in metabolic rate Use body as a heat sink Hopping mouse (25x body fluids) Kangaroo rat Sand rat Springbok antelope Giraffe Springbok antelope Eland Oryx Ostrich Camel (6 => 5 liters) Eland Oryx Springbok antelope Grant s gazelle

Physiological adaptations E. seals Efficient kidneys Hopping mouse (25x body fluids) Kangaroo rat Sand rat Springbok antelope Nasal heat exchanger Giraffe Reduction in metabolic rate Use body as a heat sink Springbok antelope Eland Oryx Ostrich Camel (6 => 5 liters) Eland Oryx Springbok antelope Grant s gazelle

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.

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 Harbor seal Northern elephant seal Gray seal Hawaiian monk seal

OUTLINE

http://www.racerocks.com/racerock/archives_08/vidslashsleep.htm

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% lowranking

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

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 Human 88% 75 % 35 % Elephant seal 15 % 4.5 % 55 % Day: 1 21 Day: 1 21 Water Fat

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

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?

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!

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! Nasal turbinates = counter-current heat exchanger Huntley et al. 1985

Nasal turbinates = counter-current heat exchanger Adult

Nasal turbinate: how it works - Estimated surface area of 3140 cm 2 in adult males - Allows 92% respiratory water recovery (sheep: 24%) OUTSIDE Bone Vascularized flesh (w / mucous) Air ----> ----> ----> ----> LUNGS NASAL TURBINATE

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?

Mean Apnea Duration (min) 14 12 10 8 6 4 2 11 18 34 21 20 20 20 19 Longest apnea: 5.5 min 0 N SP Yg W Old W J Sa M Ad F Ad M 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)

Mean Apnea Duration (min) 14 12 10 8 6 4 2 0 20 20 20 21 19 34 11 18 N SP Yg W Old W J Sa M Ad F Ad M Longest apnea: 3.2 min Terrestrial neonates: more resistant to asphyxiation than adults; this tolerance to asphyxia disappears early in development. 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)

Mean Apnea Duration (min) 14 12 10 8 6 4 2 11 18 34 21 20 20 20 19 Longest apnea: 8.2 min 0 N SP Yg W Old W J Sa M Ad F Ad M 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)

Mean Apnea Duration (min) 14 12 10 8 6 4 2 11 18 34 21 20 20 20 19 Longest apnea: 12.4 min 0 N SP Yg W Old W J Sa M Ad F Ad M 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)

Mean Apnea Duration (min) 14 12 10 8 6 4 2 11 18 34 21 20 20 20 19 Longest apnea: 16.4 min 0 N SP Yg W Old W J Sa M Ad F Ad M 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)

Mean Apnea Duration (min) 14 12 10 8 6 4 2 11 18 34 21 20 20 20 19 Longest apnea: 23.1 min 0 N SP Yg W Old W J Sa M Ad F Ad M 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)

Mean Apnea Duration (min) 14 12 10 8 6 4 2 11 18 34 21 20 20 20 19 Longest apnea: 21.2 min 0 N SP Yg W Old W J Sa M Ad F Ad M 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)

Mean Apnea Duration (min) 14 12 10 8 6 4 2 11 18 34 21 20 20 20 19 Longest apnea: 14.3 min 0 N SP Yg W Old W J Sa M Ad F Ad M 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)

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 postweaning fast. ==> therefore focus, in second part, on the period from weaning to the return to land after the first trip to sea

Goal: to prove that sleep apnea makes a difference How to do that: compare water loss between

Goal: to prove that sleep apnea makes a difference How to do that: compare water loss between Hugo Does not use sleep apnea Charlie Uses sleep apnea

Goal: to prove that sleep apnea makes a difference How to do that: compare water loss between Hugo Does not use sleep apnea Charlie Uses sleep apnea Remember: breathing is the biggest avenue of water loss during the fast How many breaths per day How much water lost per breath + ==> Water loss for Charlie Water loss for Hugo Δ (diff.)

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

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 Total number of breaths per day ==> Breathing rate

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 Water loss for Charlie Water loss for Hugo ==> Total number of breaths per day + Water loss per breath ==> ==> Breathing rate Temperature and relative humidity

Problem: how to record apneas day and night

Problem: how to record apneas day and night We re in luck: there is a relationship between heart rate and breathing! Heart Rate (BPM) Time (min)

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)

Yearling JET2

Example records: yearling 1 on the beach Heart Rate (BPM) and Temperature ( C) Time (minutes)

Example records: yearling 2 on the beach Heart Rate (BPM) and Temperature ( C) Time (minutes)

Example records: weaner coming out of the water Heart Rate (BPM) and Temperature ( C) Time (minutes)

Percentage time spent in terrestrial apnea vs time-of-day Mean % of each Hour Spent in Terrestrial Apnea Time of Day (hrs) Time of Day (hrs)

Percentage time spent in the water vs time-of-day Mean % of each Hour Spent in the Water Time of Day (hrs) Time of Day (hrs)

Percentage time spent in terrestrial apnea vs age Mean % of each Day Spent in Terr. Apnea Age (days)

Percentage time spent in the water vs age Mean % of each Day Spent in the Water Age (days)

Total percentage time spent in apnea vs age Mean % of each Day Spent in Apnea Age (days)

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 Charlie Uses sleep apnea & Hugo Does not use sleep apnea

Eupneic breathing rate Breathing Rate (breaths / min) Age (days)

Eupneic breathing rate Humans? Breathing Rate (breaths / min) Age (days)

Breaths / day Age 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

Water loss / breath - Varies with temperature and humidity Temp. ( C) Rel. Hum. (%) Hours of the Day - Where weanlings spend 80% of their time: 50 mg H2O / breath (26-80 mg / breath)

Respiratory water loss for Charlie and Hugo ( average weaners, 131 kg, 68 days old) Grams H2O lost / hr Hours of the Day

Respiratory water loss for Charlie and Hugo ( average weaners, 131 kg, 68 days old) Grams H2O lost / hr As a % of the H2O available for respiratory water loss: 121% 87% 529 g 378 g Charlie Uses sleep apnea Hugo Does not use sleep apnea Hours of the Day

Acknowledgments For 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.