Simone Baumann-Pickering May 13, 2015 sbaumann@ucsd.edu (858) 534-7280 Marine Mammal Biology DIVING PHYSIOLOGY & OSMOREGULATION
LITERATURE Perrin WF, Wuersig B, Thewissen JGM (2009) Encyclopedia of Marine Mammals, 2 nd ed, Academic Press * Diving Physiology * Diving Behavior * Osmoregulation Berta A, Sumich JL, Kovacs KM (2006) Marine Mammals: Evolutionary Biology, 2 nd ed, Academic Press * Chapter 10
REASONS FOR DIVING Forage for food Increase swimming efficiency (low drag) Save energy (low metabolic costs) Sleep while minimizing risk of predation Human dive record (AIDA): * Dynamic apnea with fins distance 288 m (2014) * No-limits apnea depth 214 m (2007) * Variable weight apnea with fins depth 145 m (2013) * Static apnea time 11 min 35 sec (2009)
DIVING PHYSIOLOGY DURATION 30 min 2 min
DIVING PHYSIOLOGY DEPTH
DIVING PHYSIOLOGY NEW MAMMALIAN DIVE RECORD Cuvier s beaked whale * 2992 m depth * 137.5 minutes (HOWEVER: Watkins et al. 1985, Cetology 49, 1-15; Sperm whale longest dive: 138 minutes)
ADAPTATIONS Cold, dark water High pressure environment Rich food sources Adaptations * External body shape * Internal structures * Sensory system
DEEP / PROLONGED DIVES Conflicting, physiological conditions during apneic conditions * Oxygen stores deplete * CO 2 and lactate increase in blood and muscle tissue (acidic blood serum and cell fluid) Period of hypoxia: muscle activity maintained anaerobically (low efficiency) * Anaerobic glycolysis + creatine phosphate catabolism * Greater accumulation of lactate longer subsequent recovery Large brains in marine mammals * human brain has permanent damage when oxygen supply is interrupted for >3 min
OXYGEN STORES Storage in 3 compartments * Respiratory system Lung volume Concentration of oxygen in lung at start of breath hold * Blood Blood volume Concentration of oxygen binding protein - hemoglobin * Body musculature Muscle mass Concentration of oxygen binding protein myoglobin * MYOGLOBIN most characteristic for deep divers!
OXYGEN STORES / DISTRIBUTION Increased blood volume (2-3 x 70 ml/kg human value) -> increased blood oxygen stores Greater blood volume in more active, and longer diving species Largest blood volumes (200-260 ml/kg) in some of best divers: elephant seals, Weddell seals, sperm whales
BLOOD VOLUME
OXYGEN STORE Humans: 20 ml O 2 /kg body mass Elephant seal: 100 ml 0 2 /kg body mass * (human comparison) * 3x blood volume * 1.5x hemoglobin concentration * 10x myoglobin concentration -> most of its oxygen in blood and muscles (exhale before diving; lung collapsed during dive)
OXYGEN STORES / DISTRIBUTION L = Lung; B = Blood; M = Muscle
MECHANISM OF THE HEART
ORIGIN AND CONDUCTION OF HEART BEAT
BLOOD PRESSURE
MECHANISM OF THE HEART
OXYGEN STORES / ADAPTATIONS Pinnipeds: ascending aorta with increased diameter (30-40%) -> aortic bulb (aortic arch) * Size of the bulb correlated to diving habits Cetaceans: some species bulbous expansion of aortic arch * Volumetric expansion * Differences in mechanical properties of walls (thickness, organization of elastic tissues)
RETIA MIRABILIA (WONDERFUL NETS) Extensive contorted spirals of blood vessels (mainly arteries but with thin-walled veins) Inner dorsal wall of thoracic cavity, extremities or periphery of body Sperm whale: most extensive
CARDIOVASCULAR RESPONSE 2 categories of dives * Routine duration * Extended dive Measurements of cardiovascular and metabolic response are limited, most measurements from seals Arrhythmic breathers, pauses between series of breaths * Resting maintenance heart rate = respiratory pause or apnea * Heart rates during dive are lower than rate of resting apneusis * Heart rate even lower during extended dive
CARDIOVASCULAR RESPONSE Gastric, renal, hepatic functions reduced; 50% of resting metabolism (extrapolation from indirect measures) Muscle (probably) relies on internal store of oxygen bound to myoglobin for aerobic metabolic needs Extended dives (3-5 x routine dives) uncommon * Urgent need (e.g., search for new hole under ice; escape from predator) * Limitation of blood flow to obligate aerobic tissue (e.g., brain), additionally Slow heart rate Lowest blood flow to muscle (myoglobin, glycogen)
AEROBIC DIVING LIMIT Lactate accumulates in muscle as muscle oxygen is depleted After surfacing: increased blood flow to muscle, lactate is flushed into circulation, disappears over several minutes Aerobic Diving Limit (ADL): diving duration beyond which there is net increase in lactate production Calculated ADL (cadl): O 2 store / metabolic rate * Prediction of basic information about foraging * Clarification of physiological responses * Models to breath holding (e.g., elephant seal exceeds cadl, how?)
BLOOD LACTATE WEDDELL SEAL Red: no net production of lactate Blue: net production Inflection: Aerobic Diving Limit (ADL) or Diving Lactate Threshold (DLT)
ADAPTATIONS TO PRESSURE Increase in water pressure (1 atm for each 10 m) * Compression of air-filled spaces -> distortion or collapse * Absorption of gases from air at high pressure Toxicity of oxygen at high concentrations Narcotic effect of nitrogen on central nervous system Damaging bubbles in tissues and blood during ascent * Sensitivity of nervous system to high pressure Terrestrial animals: over stimulation, uncoordinated nerve conduction and dysfunction
ADAPTATIONS TO PRESSURE 3 major airspaces within most mammals * Facial sinuses absent in marine mammals * Middle ear rigid structure, no compressibility Complex vascular sinus lining of the wall Blood sinus volume increases as pressure reduces gas volume -> close match between ambient and blood pressure, transferred from one fluid to another (hydraulic compression) * Lung (largest airspace) modifications that make alveoli collapse first, squeeze gases into upper airway spaces Gas exchange ceases in upper airway spaces (important for O 2 and N 2 partial pressure in blood)
LUNG MODIFICATION Phocidae (True seals) Otariidae (Eared seals) Odobenidae (Walrus)
BREATHING Breathing cycle * Rapid exhalation (blow) * Slightly longer inhalation Extremely high flow rates over breathing cycle * Flexible chest walls * Cartilage reinforcement of smallest terminal air passages (prevent collapse) 0.1 s for dolphins; 2 s for blue whales (1500 l) * Human avg. male 6 l Flow rate breathing grey whale calf
BREATHING Inspiration: extensive elastic tissue in lungs and diaphragm stretched by diaphragm and intercostal musculature Expiration: fibers recoil rapidly -> nearly completely empty lungs Rapid uptake of oxygen, ~90% per breath (humans, terrestrial mammals: 20 %) Lung collapse ~(25) 50-100 m
OSMOREGULATION
OSMOREGULATION MAJOR FLUXES Goal: maintain homeostasis
OSMOREGULATION SEAWATER No freshwater Different electrolyte concentrations * Seawater (1000 mosm L-1) * Body water (300 mosm L-1) Prey * Hypotonic (fish) with seawater * Isotonic/hypertonic (invertebrates)
OSMOREGULATION SALT GLANDS
DRINKING SEAWATER Must be able to concentrate urine Dolphin: gains water from drinking seawater Human: loss in water
OSMOREGULATION WATER
OSMOREGULATION Preformed water * Food: 60-80% water content * Seawater Metabolism 6O 2 + C 6 H 12 O 6 = 6H 2 0 + 6CO 2 * 1g Fat = 1.07 g H 2 0 * 1g Protein = 0.56 g H 2 0 * 1g Carbohydrate = 0.39 g H 2 0
OSMOREGULATION ELECTROLYTES
OSMOREGULATION KIDNEY STRUCTURE
OSMOREGULATION KIDNEY STRUCTURE
OSMOREGULATION KIDNEY STRUCTURE
OSMOREGULATION Larger kidneys in marine mammals High concentrating ability * Mysticetes -> hypertonic invertebrate prey -> thousands of kidney lobes * Odontocetes -> hypotonic prey -> hundreds of kidney lobes * Additional reading: Ortiz 2001 Osmoregulation in marine mammals, J Exp Biol 204:1831-1844