DIVING PHYSIOLOGY, OSMOREGULATION & HEALTH

Simone Baumann-Pickering May 9, 2013 sbaumann@ucsd.edu (858) 534-7280

Marine Mammal Biology

LITERATURE

•  Perrin WF, Wuersig B, Thewissen JGM (2009) Encyclopedia of Marine Mammals, 2nd ed, Academic Press *  Diving Physiology *  Diving Behavior *  Osmoregulation

•  Berta A, Sumich JL, Kovacs KM (2006) Marine Mammals: Evolutionary Biology, 2nd 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: *  Dynamic Apnea 273 m *  Static Apnea 11 min 35 sec

DIVING PHYSIOLOGY – DURATION

2 min

30 min

DIVING PHYSIOLOGY – DEPTH

DIVING PHYSIOLOGY

NEW MAMMALIAN DIVE RECORD August 6, 2010, NW of San Clemente, nearby ship using mid-frequency active sonar •  Cuvier’s beaked whale *  3000 m depth *  137 minutes *  Followed by 7 hours of shallow dives

DEEP / PROLONGED DIVES

•  Conflicting, physiological conditions during apneic conditions *  Oxygen stores deplete *  CO2 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

DEEP / PROLONGED DIVES

•  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

•  Cold, dark water •  High pressure environment •  Rich food sources

•  Adaptations *  External body shape *  Internal structures *  Sensory system

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 O2/kg body mass •  Elephant seal: 100 ml 02/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

OXYGEN STORES / DISTRIBUTION

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 * 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

•  Blood reservoirs to increase oxygen stores

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): O2 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 O2

and N2 partial pressure in blood)

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)

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 6O2 + C6H12O6 = 6H20 + 6CO2

*  1g Fat = 1.07 g H20 *  1g Protein = 0.56 g H20 *  1g Carbohydrate = 0.39 g H20

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

HEALTH

ADAPTATIONS TO LIFE AT SEA

•  Taxonomically distant groups evolved similar biological mechanisms to cope with marine existence *  Biological and behavioral strategies for controlling •  Body temperature •  Diving •  Maintaining salt and water balance •  Promoting reproductive success

•  Adaptations vital to health and survival

POSSIBLE PROBLEMS

•  Impairment in one body system can disturb equilibrium -> secondary problems threating health *  E.g. blubber: hydrodynamic shield + source of energy,

insulation, water reserves, buoyancy *  Food scarce -> blubber depletion

•  Less able to rest at surface, maintain body heat, forage, escape predators, keep up with group -> stress

•  Possible disease, further weakening •  Stress poorly understood *  Can disrupt thyroid + adrenal gland function, water and

electrolyte balance, metabolism, reproduction, weaken immune response

HEALTH RISKS

•  Reproductive failure/death of newborn •  Starvation •  Direct environmental effects •  Trauma •  Predation •  Parasites •  Microorganisms •  Metabolic disorders •  Tumors •  Biotoxins •  Strandings •  Habitat alteration and disturbance

REPRODUCTIVE FAILURE/NEWBORN DEATH

•  Weakness or disruption at any point can lead to failure – abortion, stillbirth, premature birth, weakness or death of newborn

•  Health and nutritional condition of mother affects the fetus *  Environmental disruption *  Epidemic disease * Reduced prey stocks * High levels of anthropogenic contaminants

STARVATION

•  Starvation when food is plentiful: dependent young, sick, old

•  Survival duration without food dependent on: *  Age, fat reserves, metabolic rate, energy demands, general

health *  Baleen whales: feed little over 6-8 months *  Sea otters: 2 days (can die from complications)

•  Major cause for death in pinniped and sea otter pups *  Dependency on health of mother and food supply *  Newly independent juvenile sea otters: high need for food,

inexperience of gathering •  Starvation when food sources are low (overgrazing,

overfishing, climatic or oceanographic fluctuation)

DIRECT ENVIRONMENTAL EFFECTS

•  Intensely cold winters (e.g. killed up to 2% of Florida manatee population, mostly juveniles)

•  Storms hitting pinniped rookery during breeding -> hypothermic pups, injuries, drowning, etc.

•  Unexpected frozen water surfaces: sea otters trapped outside; cetaceans trapped in ice

•  Unseasonable warm weather: *  fractured ice: crush breeding seals and pups * melting ice: walrus mothers abandon calves

TRAUMA

•  Natural source of injury: storms, predators, aggressive encounters

•  Anthropogentic source: fishery operations, shipping, (recreational) boating * Historically: whaling; today more accidents *  Leading: interaction with fisheries •  Direct during fishing activities •  Indirect during entanglement of lost gear

*  Vessel collisions * Noise impacts

PREDATION

•  Easiest target: small, inexperienced animals, found in particular place on schedule

•  Predators: Arctic fox, polar bears, killer whales, sharks

•  Predation consequence on female may effect current pup and possible future pup (recovery period without pregnancy)

PARASITES

•  Parasitic infestation unproblematic condition *  Amphipods / copepods (eat whale skin) *  Seal lice (small numbers, seal blood) *  Gastrointestinal helminths

•  Harmful for individual *  Heartworm, lungworm, hookworm *  Nematodes (mammary glands, cranial sinuses, kidneys) *  Trematodes (Nasitrema spp.: cranial sinuses; Campula spp.:

liver and pancreas) *  Wrong host for parasite (e.g. protozoan Toxoplasma gondi

from cat; may lead in sea otters to encephalitis, heart disease, abnormal behavior)

MICROORGANISMS

•  Bacteria, fungi, viruses * Many organisms are considered normal *  Few are pathogenic (= cause infectious disease),

some more threatening than others •  Degree of infectious disease depends on *  Aggressiveness of organism *  Susceptibility of host (condition of immune system) *  Age of individual (very young or old more likely to

get infected)

BIOTOXINS

•  Thousands of species of marine phytoplankton *  40 can produce toxins harmful to top predators

•  Examples *  Ciguatoxin: (dinoflagellate) 1978, 50 Hawaiian monk

seals -> emaciated, parasitic infections, died *  Saxitoxin in mackerel (neurotoxin): 14 humpback

whales died from respiratory paralysis, Cape Cod 1987 *  Brevetoxin (neurotoxin in dinoflagellate Karenia brevis

(red tide)): danger to bottlenose dolphin, manatees (Florida, Gulf of Mexico)

*  Domoic acid (neurotoxin in diatom Pseudonitzschia sp): CA sea lions along central California -> convulsions, loss of coordination, vomiting

OTHER

•  Strandings •  Habitat alteration and disturbance *  Contaminants * Oil spills *  Ingesting debris *  Prey depletion * Nutrient enrichment (toxic algal blooms) *  Anthropogenic noise …