Lecture Notes - Florida International University

Lecture Notes
The Biology of Marine Mammals
Spring 2010
Dr. Mike Heithaus
Marine Sciences 361
Office Hours: Tue 1300-1630*
*by appointment; I am also available by appointment at other times
[email protected]
(305) 919-5234
www.fiu.edu/~heithaus
Goals for the course
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Gain an appreciation for the evolution and diversity of marine mammals
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Learn the theory relevant to these areas of biology, especially ecology and behavior
Gain a basic understanding of the physiology, population biology, ecology, and behavior of marine
mammals
Begin to explore the primary scientific literature and learn research techniques
Course structure
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Lectures: T,Th 0930
Grading
– 4 Exams
– Participation in Class Discussions
Succeeding in this class
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Read the assignments/papers that are assigned – you will be responsible for some material outside of
lecture notes!
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Don’t skip classes
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Come talk to me!
Take good notes, and ask questions!
Make sure you understand your notes
Get help if you don’t understand something
– Book, peers, me
Marine Mammal Diversity and Zoogeography
Marine Mammals
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Any mammal that takes to the sea for part of its life
Polyphyletic group of ~120 species
– Taking to the sea has evolved multiple times among mammals – at least 5-8 times
Marine Mammal Diversity
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Extant groups
– Ceataceans
– Sirineans
– Pinnipeds
– Sea Otter
– Polar Bear
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Extinct groups
– Desmostylians
– Kolponomos – bear-like, fed on marine invertebrates
– Thalassocnus – an aquatic sloth!!!
Challenges of the Marine Environment for Mammals
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Can’t exchange gases continuously
Increased rate of heat loss
Resistance to movement (viscosity)
Differences in sound characteristics
Generally low light/visibility
but, provides support (buoyancy)
Level of adaptation depends on proportion of life spent in the water
Some basic adaptations
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Polar bears (least derived)
– Mainly adapted for cold terrestrial environment
– Too buoyant for any real diving but strong swimmers
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Sea otters
– Well adapted for life in the ocean
– Spend much time rafting at surface but somewhat accomplished divers
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Pinnipeds (seals, sea lions, walrus)
– Amphibious but spend considerable time at sea
– Limbs provide propulsion on land and sea
– Dense fur and streamlined bodies
– Carnivore-like dentition (differentiated teeth)
– Sensory bristles (vibrissae)
– Rely on vision/touch
– Amazing diving capabilities
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Sirenians (dugongs and manatees)
– entire life at sea
– Herbivores
– Nostrils at dorsal tip of snout
– Use vision/touch
– Fat layer
– Heavy bones
– Modified tail for efficient propulsion
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Cetaceans (whales, dolphins, porpoises)
– Nostrils on dorsal surface of head (blowhole)
– Great breath-holding capacity
– Blubber and vascular heat-exchangers
– Very streamlined
– Horizontal flukes/efficient propulsion
– Sound producing systems (echolocation in odontocetes)
Extant Marine Mammal Families
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ORDER CARNIVORA
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Family Mustelidae (1 MM species)
– Sea otter (Enhydra lutris)
Family Ursidae (1 MM species)
– Polar Bear (Ursus maritimus)
Order Carnivora, Suborder Pinnipedia
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Not as diverse as cetaceans
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36 species, 3 families
– Otariidae (eared seals)
– Odobenidae (walrus)
– Phocidae (true seals)
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Family Odobenidae: walrus (1 sp)
– External tusks in both sexes
• Used for combat, display, anchorage/leverage, kill phocid prey
– Adapted to feed on clams
• Bristles detect prey then vacuum pump with tongue as piston to suck clams from shell
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Family Otariidae: Sea lions and Fur Seals (eared seals, 16 Sp)
– External ear flaps
– Large, mostly hairless foreflippers (fold under body)
– Long hind flippers (fold under body)
– Can “walk”
– Major Sexual dimorphism
– Fur seals have pointier snouts, dense underfur
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Family Phocidae: true seals (19 sp)
– No external ear flaps
– Short, haired foreflippers
– Non-rotateable rear flippers
– Hunch or wiggle on land
– Diverse coloration and body size
– Hooded and gray seal diverge from usual form
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Great size differences
– Blue whale (33m, 190,000kg)
– Vaquita (<1.7m, 60kg)
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Two major divisions: baleen whales (mysticetes) and toothed whales (odontocetes)
Size range not as extreme
– Lake seals (1.5m, 70 kg) – Male elephant seal (4m, 2.5t) (2.5 fold, 35 fold differences)
Order Cetacea
Don’t be confused by the names whale, dolphin, porpoise!
– e.g. Mellon-headed whale and killer whale!
Order Cetacea, Suborder Mysticeti
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14 Species
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Balaenopteridae: Rorqual whales (~8 sp)
– Have ventral grooves, gular pouch
– Gulp water then force back through baleen then use tongue to wipe prey off baleen
– Dislocatable jaws, disarticulate lower jaw
– Generally sleek, have dorsal fin
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Family Balaenidae: Right whales (3 sp)
– Rotund, slow, no dorsal fin
– Huge, arched mouth
– Very thick blubber
– Longest baleen (to 4m long)
– No throat grooves
– Skim feeders
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Paired Blowholes
Baleen plates (keratin) in upper jaw (no teeth)
– Semi rigid, grow continuously, inner edge has fringe of fibers to form strainer
– Water goes in through mouth and out through plates
– Fiber diameter matches prey size (finest in right whales)
Family Neobalaenidae: Pygmy right whale (1 sp)
– Has dorsal fin
– Smaller and sleeker than right whales but has arched jaw
Family Eschrichtiidae: Gray whale (1 sp)
– Intermediate between right whales and rorquals
– Arched jaw
– Short, course baleen
– Uses tongue as a piston to suck food into mouth along benthos
Order Cetacea, Suborder Odontoceti
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Toothed whales
– 10 Families, ~70 species
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Great diversity in size
– Vaquita to sperm whale (18.5m, 57 t)
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Great diversity in teeth
– Number, size, shape
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Raptorial predators
Single blowhole (left of center)
Family Physeteridae (1 sp)
– Sperm whale
– Largest odontocete
– Extreme sexual dimorphism
• Males 15m, 45t; Females 11m, 20 t
– Biggest head (oil storing organ)
– Slim mandible (lower jaw)
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Family Kogiidae
– Pygmy and dwarf sperm whales
– Upright dorsal fin
– Underslung, narrow mandible
– Small (3.3, 2.7m)
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Ziphidae (>20 sp)
– Beaked whales
– Medium-small
– Posterior-tending dorsal fin
– Extensive skull asymmetry
– Few functional teeth (some only erupt in males)
– Many have bizarre teeth erupting from lower jaw in males
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Family Platanistidae
– Ganges and Indus River dolphins
• Blind (loss of lens in eye)
• 120 long, interlocking teeth
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Family Iniidae
– Amazon river dolphin
• Only extant odontocete with differentiated teeth (cusps on posterior teeth)
• Can crush armored fish and turtles
• Very maneuverable (useful in flooded forest)
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Family Lipotidae (could be part of Iniidae)
– Yagtze river dolphin
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Family Pontoporiidae (could be part of Iniidae)
– Franciscana (not really in rivers)
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Family Monodontidae
– Beluga and Narwhal
– Arctic
– ~5m length
– No dorsal fin
– Eruptive tooth in upper left jaw of male narwhal
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Family Delphinidae (dolphins) 35 species
– Most diverse odontocete family
– Peglike teeth
– Subfamily Cephalorhynchinae
• Coastal dolphins of the S. Hemisphere
– Subfamily Stenoninae
• Humpback and roughtoothed dolphins
– Subfamily Delphininae
• Largest group of dolphins (e.g. bottlenose dolphins)
– Subfamily Lissodelphinae
• Right whale dolphins
– Subfamily Globicephalinae
• Killer whales and the “blackfish”
– Subfamily Orcaellinae
• Irrawaddy dolphin
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Family Phocoenidae: True porpoises (6 species)
– Small flippers
– No beak
– Five have small dorsal fins, one has none
– Laterally compressed spatulate teeth that form cutting edge
Order Sirenia
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Family Trichechidae: manatees (3 sp)
– More generalized than dugongs
– Slow, built for confined spaces
– “normal” mouth
– Feed throughout water column
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Family Dugongidae: Dugong and Stellar’s Sea Cow
– Fluke-like tail for acceleration
– Rostral disk oriented down (expanded upper lip)
– Male has protruding tusks
– Obligate bottom feeders
Zoogeography
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Study of the distribution of extant species
Water temperature critical for marine mammals
– Directly on animals physiology
– Indirectly on prey
– Species often occur in latitudinal bands
Shape of nearby land/shelf
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History is Critical
– When did lineages arise and diversify?
– Continental Drift and Climate Change
– The early and middle Miocene
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Polar
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Cosmopolitan
Basic Climatic Zones
Subpolar/Cold Temperate
Temperate
Subtropical
Tropical
Basic Types of Distribution
Pan Tropical
Temperate/Subpolar
Circumpolar
Anti-tropical
Regional (Endemic)
still unknown for many species
Horizontal Habitats
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Nearshore
– Lakes and Rivers
– Estuaries
– Freshwater and saltwater mix, high productivity and low visibility
– Bays
– Relatively protected waters
– Coastal
– Shallow waters, often high energy (wave action)
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Offshore
– Continental Shelf
• Relatively shallow but deeper than nearshore habitats
• Light usually penetrates to bottom over much of this habitat
– Continental Slope
• Depth changes rapidly, light penetration begins to diminish
• Often associated with high productivity
– Pelagic
• Extremely deep, no light at depth
• Generally low productivity except in areas of relief (seamounts, etc)
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Frontal dynamics and current features may be very important
Vertical Marine Habitats
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Vertical Distribution of Habitats
– Light, temperature, pressure, salinity, and water density change considerably as depth increases
– Deep-water habitats can be divided into photic and aphotic zones
– Depth where these start varies considerably with water visibility
Ice Habitats
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Many pinnipeds rely on ice as habitat
– Haul outs
– Breeding
Polar bears use the ice to stalk seals
Cetaceans must navigate the ice to access many polar habitats
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Fast ice
– Ice attached to shore that does not move
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Pack ice
– Ice that forms at sea and moves with currents
– Covers central Arctic, surrounds Antarctica
– Largely melts in summer, especially in Antarctica
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Ice floes
– Large pieces of sea ice broken by wind or waves
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Leads
– Open water formed when floes move apart
Current Distributions: Mysticetes
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Typified by seasonal shifts from high latitudes (feeding in summer) to low latitudes (breeding in winter)
Bowhead: arctic
Right whales: temperate
Gray whale: warm temperate
Rorquals: cosmopolitan
– B. edeni, B. brydei pantropical (<40°)
Current Distributions: Odontocetes
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Not limited by temperature in general
Sperm whales – pelagic, cosmopolitan
– 2 smaller species more tropical
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Narwhal and Beluga – coastal, arctic
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Beaked whales – pelagic, regional or antitropical
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– Move with sea ice
– In general, very poorly known
Delphinidae – coastal and pelagic forms; tropical, anti-tropical, cosmopolitan, regional all found
Porpoises – coastal, sometimes freshwater, regional/endemic
“River Dolphins” – large tropical river drainages; one coastal species in SA
– Indus, Ganges, Yangtze, Orinoco, Amazon
Current Distributions: Sirenians
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Tropical/Subtropical; Regional
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Dugongs: fully marine
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Manatees (Trichechids): tend towards freshwater sources
– Recently extinct Stellar’s Sea Cow was cold temperate
– Limited by marine plant distributions
– Prefer >18°C, <6m depth
– Amazon manatee: obligate fresh water
Current Distributions: Pinnipeds
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Cetaceans more successful in low latitudes, pinnipeds more successful at high latitudes
Odobenids
– disjunct circumpolar
Otariids
– cool temperate/subpolar (except N. Atlantic)
– lower latitudes where cold currents occur
– Arctopcephalus (fur seals) have 6 species only in southern ocean
– Distributions highly influenced by sealing
– Some species highly endemic, but others widespread
– Zalophus (sea lions) mainly in north with California sea lion most widespread
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Phocids
– Most widespread pinnipeds
– Northern group Phocinae
• Many give birth on ice or in ice lairs
• Temperate, Arctic, subarctic, some landlocked lake seals
– Monachinae
• Warm water seals, elephant seals, Antarctic ice seals
– Some ice seals can maintain holes (Ringed seal) in ice, others must stay near ice edge (Bearded seal)
– Monk seals only true warm water seals
Current Distributions: Sea otters and Polar Bear
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Sea Otter
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Polar Bear
– North Pacific
– Tied to shallow waters
– Poor dispersal ability
– Circumpolar
– Track seal distribution (mainly ringed seals)
Current and historical distributions
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May have been modified greatly by human activities both ancient and modern
Pinnipeds in central and northern California are a perfect example
Pinnipeds of central California
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Currently dominated by CA sea lions and N elephant seals with northern fur seals (NFS) rare and only
breeding in recent and small colonies on offshore islands
Most NFS breeding is in Alaska and may forage in pelagic waters as far south as Baja
A strange observation: remains of NFS extremely common in archeological sites in California.
Explanations of NFS abundance in ancient times
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Always had northern rookeries and foraged closer to shore where they were available or were hunted
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More abundant on offshore rookeries of California
Were historically more abundant and had mainland rookeries
Burton et al (2001)
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Used archeological data, stable isotopes to address these hypotheses: what did they find?
– Differences in hunting or foraging location did not explain remains
– NFS were mainland breeders in CA during mid-late Holocene
– NFS were extremely abundant historically compared to other pinnipeds and may have limited the
abundance of other pinnipeds
Evolution and Systematics
Convergence, Divergence and Parallel Evolution
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Distantly related taxa can come to resemble one another through the process of convergence
Closely related taxa may quickly develop very different morpholgies through divergence
Species may have diverged in the distant past can maintain similar morphologies through parallel
evolution
Adaptations
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An adaptation is a character or suite of characters that helps an organism cope with its environment
A preadaptation (or exaptation) is an adaptation that performs a function other than previously held
– e.g. the lower jaw of odontocetes is used to transmit high frequency sounds underwater but first
evolved to transmit low frequency sounds from the ground
Adaptive Radiation
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Rapid diversification of a lineage into many forms
Can obscure relationships due to rapid evolutionary change if in distant past
If recent, may be hard to detect differences: what is a species??
– Biological Species Concept
– Inability to interbreed
Studying evolutionary relationships
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Systematics – the study of defining evolutionary relationships among organisms both extinct and extant
A phylogeny is a hypothesis about evolutionary relationships
– Often shown on a tree
– Can never be “proven” only strongly supported!!!
Phylogenetic Trees(Cladograms)
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Tree representing best estimate of phylogenetic lineages
– Lines are clades or lineages (groups of related taxa from a common ancestor)
– Nodes = branch points = speciation events
Cladistics
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Organisms can be deemed related based on shared derived characters (synapomorphies)
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Character State
– Condition of the character
Characters
– any feature useful in phylogenetic analysis
– May be ancestral (primitive) or derived (apomorphy)
– Characters may be primitive or derived but taxa are not
• Taxa are all endpoints of evolution
Homology and Analogy
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Cladistics relies on finding synapomorphies
Homology
– Characters that arise from similar ancestry
– Bats’ wing bones and human fingers
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Analogy
– Similar characters that do not share evolutionary history
• Bird wing and bat wing
• Do analogies help in resolving evolutionary relationships?
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It is critical to determine which character states are ancestral and which derived
– Can use outgroups or closely related lineages; often use sister group – the most closely related
lineage
– Character states shared with outgroup likely are ancestral
Determining Character States
Types of groups on cladograms
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Monoplyletic
– includes hypothetical ancestor and all descendents
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Paraphyletic
– does not include all descendants of an ancestor
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Polyphyletic
– Collection of descendants from >1 ancestor not including all ancestors
Types of characters
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Behavioral
Physiological
Mophological
Molecular
Molecular vs Morphological Characters
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Molecular
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Morphological
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Use of both types of data best!
– Huge number of possible characters (down to each nucleotide)
– Can find parts of genome not under environmental selection
– Long time periods can obscure due to saturation (problems with parallel evolution)
– Time to saturation depends on rate of evolution at each locus
– Evolve more slowly (little saturation)
– Can include extinct taxa
– Can have problems with convergence
– Defining characters can be difficult
Fossil Taxa
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Contribute most when they help plug holes in long divergent lineages
Can complete morphological series, help determine homologies
Can help determine earliest occurences
Can’t Use many characters – results in poloytomy (unresolved nodes)
Constructing a Cladogram
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Select group, define all taxa
Select and define characters and character states
Create data matrix
Use outgroup comparison to determine ancestral and derived states
Construct all possible cladograms
Select best cladogram using parsimony
Principle of Parsimony – the best cladogram is the one involving the fewest evolutionary transitions
(steps)
Uses of phylogenies
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Character mapping
Pinniped Evolution and Systematics
The pinnipeds
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Monophyletic group with 3 monphyletic families
18 phocids, 14 otariids, walrus
Diversity was once much greater (13 species of walrus are extinct)
First pinnipeds arose in Oligocene (27-25mya)
Much speciation in last 2-5 million years
Poor fossil record generally
Major pinniped synapomorphies
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Large infraorbital foramen (hole below eye to allow vessel and nerve passage) (1)
Short, robust humerous (6)
Digit I on hand emphasized (7)
Digit I and V on foot emphasized (8)
Mono or diphyly?
Evidence for diphyly
– Biogeorgaphy and morphology
– Otarrids and odobenids close to bears; phocids close to mustelids
Evidence for monophyly: the best explanation
– Molecular, karyological, morphology
– All support close ties to ursids, mustelids, otters (sister group unclear)
– Diving behavior and breeding patterns suggest eared seals evolved first (Costa 1993)
• Phocids are most aquatically adapted (diving, breeding, body plan)
Early Pinnipeds
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Find describe in 2009 sheds new light on early evolution
Pujila darmwini was “walking seal” ~24 mya
Otter-like body, webbed feet, lived in freshwater lakes of Canadian Arctic
Suggests pinnipeds went through a freshwater phase
High productivity associated with cold water upwelling probably supported prey base early pinnipeds
exploited
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First found from cool waters and rocky coasts of eastern N. Pacific during late Oligocene
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Pinnipedimorpha clade
– Lateral and vertical movement of vertebral column possible
– Both sets of flippers modified for aquatic locomotion
– Still very capable on land, probably spent more time there than modern forms
Pinnipedimorpha clade
– Show ancestral, heterodont, dentition
– Many similarities to archaic bears
– Later forms show derived homodont dentition
Early Pinnipeds
Modern Pinnipeds: Otariidae
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Seal lions and fur seals
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Frontals extend anterior between nasals (9)
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Otariinae (sea lions) monophyletic, not Arctocephalinae (fur seals) which are still poorly resolved
Shallow divers often targeting fast-swimming fish
Monophyletic group first appeared late Miocene (11 mya) but all modern forms in last 2-3 my
Two subfamilies
– Otariinae (seal lions)
– Arctocephalinae (fur seals)
Some Otariid synapomorphies
Uniformly spaced pelage units
Trachea subdivides close to voicebox (13)
Secondary spine on scapula (11)
External ear flaps “pinnae”
Can turn hindflippers forward; use to walk
Otariid systematics
Hybridization and Introgression may cause problems
– aggressive sexual behavior of male sea lions directed at other species
Modern Pinnipeds: Odobenidae
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Current 2 subspecies relicts of once diverse group
– Modern walrus large-bodied, shallow diving mollusk feeder
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Monophyletic family, origin middle Miocene (16-9 mya) eastern North Pacific
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Five synapomorphies
Odobenid synapomorphies
Modern walrus distinguished by squirt-suction feeding
TUSKS ARE NOT A SYNAPOMORPHY
– They evolved in only one lineage leading to modern walrus
– Many ancient odobenids did not have tusks
Where do the odobenids fit?
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Molecular evidence points to otariids, but morphological data suggests a close association with phocids
– Middle earbone enlarged
– No pinnae
– Well-developed thick subcutaneous fat
– Abdominal testes
– Similarities in hair and venous system
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What gives?
– Still unclear where walrus fit in pinniped clade
– Odobenids probably branched off from basal pinnipeds very early leading to a long branch
– Subsequent long-branch attraction causes molecular similarities
Odobenid movements
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Origin in eastern North Pacific
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“True” seals, lack ear flaps
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Late Oligocene origin (29-23mya) in N. Atlantic
Invaded Atlantic through Carribean
600,000 ya modern walrus reinvades Pacific through Arctic and diverge into subspecies
Modern Pinnipeds: Phocidae
Generally larger than otariids
Some fantastic divers
– Weddell and elephant seals over 1000m
Monphyletic family with two subgroups
– monoachines and phocines
Some phocid synapomorphies
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Unable to turn hindflippers forward
Inflated entotympanic bone (21)
No supraorbital process (10)
Subspecies, hybridization and a misplaced genus
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Five subspecies of harbor seal recognized based on morphological, molecular, behavioral differences
– Eastern and western sides of Atlantic and Pacific, lakes of northern Quebec
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Harp seal Phagophilus groenlandicus x hooded seal Cystophora cristanta hybird – what does this mean
for biological species concept
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What is the status of the gray seal genus?
Phocid systematics
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Are traditional subgroups monophyletic?
Monk seals Monachus often considered most basal of phocids due to ancestral characters (some moreso
than fossil taxa)
Pinniped Evolution: Summary
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Morphologic and molecular data support monophyly
Derived from arctoid carnivores, probably close relatives of bears
Earliest appear 27-25mya in north Pacific
Modern lineages diverged quickly
Position of the walrus unclear
Cetacean Evolution and Systematics
Cetaceans
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Monophyletic group with 3 suborders
– Archaeoceti (extinct)
– Odontoceti (~76 species)
– Mysticeti (11 species)
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Earliest marine mammals (with sireneans) 53-54 mya
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Currently some questions about origins: several competing hypotheses
Cetacean Origins
Evolved from small primitive ungulate group
– Could be from mesonychid condylarths
– Could share common ancestor with hippos
– Could be sister group of other artiodactyls (even-toed; hippos, camels, antelope, pigs, giraffes, etc)
– Could be another ancestor not closely related to moder artiodactyls
Cetacean Origins: The old favorite
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1. Decendent of Order Condylartha, Family Mesonychidae
• Wolf-like with digitigrade stance (walk on toes), possibly hoofed
• Massive crushing dentition; early skulls suggest similarity
Cetacean Origins: close to hippos?
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2. Some molecular data points to close affinity with hippos; recent skull finds disagree – more like
mesonychids
Cetacean Origins
3. Sister group to clade including hippos and artiodatyls; not particularly close to mesonychids
– Works well with #2 if hippo ancestors were very different morphologically
– Probably all derived from mouse-deer like ancestor
Cetacean Origins: Indohyus brings us closer to an answer
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4. Sister group to cetaceans more primitive than other artiodactlys
– Recent finds in India suggest cetaceans closest ancestor is an ancient artiodactyl group (raoellids)
– Similarity to cetaceans based on morphology of inner ear, the arrangement of incisors, and
morphology of premolars
– Indohyus was an aquatic wader based on bone density and oxygen isotopes
– Carbon isotopes suggest feeding on terrestrial vegetation or omnivores on land but escaped to water
when in danger like modern African mouse deer
– Adaptation to aquatic habitats did not occur first in early cetaceans, but more basal species –
cetacean branch probably driven by switching to aquatic prey (unique dentition and oral skeleton)
– Early cetacean ancestors went through a hippo-like stage
– Study published in 2009 suggests that hippos are, in fact, closest living relatives of cetaceans.
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Paraphyletic group of ancient whales that gave rise to modern whales
– lack telescoped bones of the skull
– Elongate snout
– Narrow braincase
– Large temporal fossa
– Well defined sagital and lambdoidal crests
Archaeocete cetaceans
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Earliest from Early Eocene (>50 mya)
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Ambulocetids
– Found in middle Eocene rocks of India and Pakistan
– Most basal amphibious marine cetaceans
• Nearshore marine (estuaries and bays) but tied to freshwater for drinking
– Abulocetus natans and others close to size of male sea lion
– Show first signs of hearing adaptations
– Eyes above profile of skull
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Ambulocetids
– Likely slow on land
– Elongated hind feet and tail that would aid in locomotion
• Probably swam like modern otter swinging tail and feet
– Probably ambush hunter like modern crocodiles
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Remingtonocetidae
– Short-lived group from Middle Eocene of India and Pakistan
– Nearshore tidal environments, but more aquatic than ambulocetids
– Long narrow jaws
– Probably swam with tail like Amazonian giant otter
– Captured fast-swimming aquatic prey
Protocetids
– Globally distributed during the middle Eocene
• First group to leave South Asia
– Expanding niches inhabited including deep offshore waters but probably restricted to tropics
– Nasal openings more caudal than earlier species
• Could breath with much of head underwater
– No fluke
– Lifestyle probably very similar to modern pinnipeds
– Hindlimbs may not have been able to support weight in some species
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Extinct by end of Eocene
Pakecetoids are most ancient group (50 my)
– Pakecetus – earliest whale; India and Pakistan
– Ear morphology gives them away as cetaceans
– Lived in an arid environment with ephemeral streams and floodplains
• Always found in river deposits
• At best site, 60% of mammal remains are pakicetids!
– Quadropedal and probably mainly terrestrial but not swift runners (dense bones that may have
been for ballast)
– Long thin legs and short hands and feet suggest they were poor swimmers (quadropedal
paddling) and many deposits were rivers that were too shallow for swimming
– Teeth vary greatly – some hyena-like
• may have been scavengers or predators
• Probably ate freshwater aquatic organisms and land animals near water
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Basilosaurids
– Middle to late Eocene/early Oligocene
– large-bodied family with elongated vertebral bodies (Basilosaurinae)
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Very reduced hind limbs – fully aquatic
– Basilosaurus grew to 25m
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Throughout the tropics and subtropics
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Had fluke, but back undulations rather than the fluke provided propulsion
Piscivorous
Dorudontids
– Related to basilosaurids, sometimes put in the same family
– smaller-bodied with non-elongated vertebral bodies
– Throughout tropics and subtropics, often in deposits with basilosaurids
– Dolphin-like and more diverse than basilosaurids
– Had a fluke and swam like a modern cetacean
– Likely ancestors of odontocetes and mysticetes
Archaeocete trends
Rapid evolution (few million years) from
– Quadropedal to flukes (hindlimb reduction)
– Freshwater dringing to seawater drinking
– Land animal to not able to move on land and giving birth in water
– Movement of nostrils to the top of the head
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Extinction probably tied to changes in food supply driven by oceanographic change
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Diverged from Archaeocetes about 37 mya
Modern Cetaceans
Monophyletic clade derived from dorudontids
Split between mysticetes and odontocetes probably 35 mya
Synapomorphies
– Telescoping of skull: movement of blowholes to the top of skull
• Migration of premaxillary and maxillary bones forms a rostrum (beak)
– Fixed elbow joint not present in archaeocetes
Mysticetes (Baleen whales)
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Modern forms distinguished by baleen plates, but early mysticetes had teeth
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Early mysticetes were small 4-5 m
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Other trends include increased body and head size, shortening of the neck
Origin probably tied to Oligocene development of Circum-Antarctic current and generation of nutrientrich upwelling that led to huge zooplankton shoals
Major evolutionary transition is from raptorial predation (single prey item at a time) with teeth to batch
or filter feeding with no teeth (baleen present by Oligocene, but decomposes so record poor)
Mysticete Synapomorphies
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Maxilla extends posteriorly to form infraorbital process
Mandibular symphysis (lower jaw connection) unfused
Modern Mysticete Relationships
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Four extant families?
– Balaenopteridae,
– Balaenidae
– Eschrichtiidae
– Neobalaenidae
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Taxonomy not well-resolved
Cytochrome b suggests that Eschrichtiidae is not valid
Mysticetes: in order of divergence
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Balaenidae
– Right whales and Bowhead
– First appear in early Miocene (23 mya)
– Heavy body, cavernous mouth, no throat grooves
– Head 1/3 of length
– Long baleen plates
– Only mysticetes with 5 digits on forelimb
– Monopyletic
• Support for two separate genera poor
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Neoalaenidae
– Anatomical data places as separate family outside Balaenidae
– More anteriorally thrust occipital shield
– Shorter, wider mouth for shorter baleen
– Separate from balaenids due to presence of dorsal fin, throat furrows, different type of baleen,
relatively smaller heard, four digits on hand, shorter humerous
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Eschrichtiidae
– Current species has 100,000 year fossil record (only one for family)
– North Atlantic population extinct in 17th or 18th century
– Probably falls within the Balaenopterids, but further work needed
• No dorsal fin
• 2-4 throat grooves
• Baleen is thicker, fewer in # and whiter than rorquals
– Unique paired occipital tuberosities on skull for neck muscles
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Balaenopteridae
– Fossil record extends 10-12 mya from Americas, Europe, Asia, Australia
– Hybrids occur
– Dorsal fin
– 14-22 (humpback) to 56-100 (fin) throat grooves extend beyond gular region
– Short baleen
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Diverse array of toothed forms from freshwater rivers to deep-diving in pelagic habitats
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Monophyly well supported despite well-publicized argument against with early genetic data
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Most morphological characters argue that they are, but one of the supposed synapomorphies has come
been disputed: presence of a single blowhole
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Odontocete facial structure serves a number of functions
– Respiration cause of much skull rearrangement
– Sound production (echolocation) and detection another major force
– Buoyancy control, at least in sperm whales
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Some of the 20 Synapomorphies
– Concave facial plane
– Asymmetric cranial vertex
– Premaxillary foramen present
– Maxilla overlays supraorbital process (frontal bone)
Odontocetes
First appear in fossil record 28-29 mya
Major Miocene radiation of pelagic forms appears to be linked to changes in currents and thermal
gradients
Are odontocetes monophyletic?
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Antorbital notch present
Asymmetric skulls (except possibly most primitive)
Asymmetric soft tissues in modern forms due to enlargement on right side
Fatty melon in front of nasal passages for echolocation
Ziphiidae
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More than 20 species in 5-6 genera extant
– Found in Mocene and Pliocene, including one freshwater form; extant species mainly pelagic
– Trend towards loss of teeth with exception of 1-2 pairs anteriorly which become enlarged (only
Shepard’s beaked whale has full functional dentition)
• Possible sexual display/weapons
– Pair of throat grooves that converge anteriorly
– Phylogeny unclear; no rigorous cladistic review
Physeteridae
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Long fossil record (29-21 mya), once diverse but only one extant species
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Linked into a superfamily with sperm whales because of supercranial basin and spermaceti organ
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Once put into a single family, but similarities (reduced eyes, elongated snouts) are due to convergent
evolution
– freshwater/estuaries have been invaded at least 4 times
Platanistidae
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Asiatic river dolphins
– Ganges and Indus Rivers
– Reduced eyes in Ganges form
– Long narrow beak with numerous narrow pointed teeth
– Broad paddle-like flippers
– No known fossil record, time of freshwater invasion unknown
– Bony facial crest
Pontoporiidae
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Fransiscana
– Coastal waters of western S. Atlantic
– Long rostra, tiny teeth
– Close relative of Iniidae
Loss of one or both nasal bones
Deepest known divers
Have spermaceti organ
– not homologus to melon; “junk” below organ probably melon homolog
– in supracranial basin
– may occupy 30% of length and 20% of weight
– May control buoyancy but still unclear
Kogiidae
Lack both nasal bones
Have short rostrum and are much smaller than sperm whales (<4m; <2.7m)
Oldest known from late Miocene (8.8 mya)
“River Dolphins”
Iniidae
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Amazon river (botu)
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Reduced eyes
Extremely elongated rostrum and mandible
Conical front teeth, molariform rear teeth
Greatly reduced orbital region
Maxilla forms crest
Fossils from late Miocene originated in Amazonian basin
Lipotidae
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Yangtze Tiver (baiji)
– Narrow, upturned beak
– Triangular dorsal fin
– Broad round flippers
– Reduced eyes
– One fossil, one extant species from China
Delphinidae
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Most diverse cetacean family 36 sp, 17 gen
Open ocean to some into freshwater (Orcella brevirostris, Sotalia fluvatilis)
Most small to medium 1.5-4.5m, killer whale to 9.5m
Loss of posterior sac of nasal passage
Reduction of posterior end of left premaxilla: does not contact the nasal
Oldest from late Miocene (11 Ma)
Systematics are still a mess
– Some genera are not monophyletic
– Diversity likely to increase (e.g. Tursiops)
– Stenella is polyphyletic
Phocenidae
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Six small extant species
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Sister taxa of delphinids
Synapomorphies
– Raised rounded protuberances on premaxillae
– Premaxillae do not extend beyond anterior half of nares
– Spatualte (not conical) teeth
First appeared in late Miocene, eastern Pacific
Monodontidae
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Delphinoids with flat or convex facial planes in profile
Extant species in Arcitc
Miocene/Pliocene some species found in E. Pacific to Baja California
Sirenians, Sea otters, Polar Bears, and other marine mammals: Evolution
Sirenians
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Monophyletic group with two extant familes
– Trichechidae (manatees)
– Dugongidae (dugongs)
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Unique in strictly herbivorous diet
First appear in early Eocene (50 mya)
Sirenian Origins
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Monophyly strongly supported
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Closest living relatives are proboscideans (elephants)
– Teeth and skull morphology unite the groups
– Extinct Desmostylians form clade with sirenians and elephants (monophyletic “Tethytheria”)
– First arose in Old World, but quickly spread to New World 50 mya
Syapomorphies
– External nares retracted and enlarged reaching beyond the level of the anterior margin of the orbit
– Premaxilla contacts frontal
– Lacks sagital crest
– Bones dense and compact (for buoyancy regulation)
Ancient Sirenians
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Prorastomus (50mya) first (Jamaica)
– Had functional hindlimbs
– Dense bones, swollen ribs and presence in marine deposits suggest partially aquatic; riverine and
estuarine selective browser
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Protosiren (middle Eocene) (Egypt)
– Functional terrestrial locomotion but auditory, olfactory, and visual systems appear modified for
aquatic lifestyles
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Much of the spread of sirenians tied to the spread of seagrasses in the temperate Pacific
Modern Sirenians: Trichechidae
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Appear to be derived in late Eocene/early Oligocene, possibly from dugongids
Monophyletic, united by features of the skull and reduction of neural spines on vertebrae
Mainly freshwater/estuarine
Ability to produce new teeth as old ones are worn down
3 modern species
– West Indian manatee (Trichechus manatus)
• 2 subspecies: Antillean (T.m. manatus); Florida (T.m. latirostris)
– Amazon manatee (Trichechus inunguis); freshwater only
– West African manatee (Trichechus senegalensus)
Modern Sirenians: Dugongidae
Paraphyletic family with Caribbean/W. Atlantic origins spreading to Pacific
More marine than manatees
Two extinct subfamilies and one extant
– Hydrodamalinae (includes Steller’s sea cow) appears to have split from Dugonginae (dugong) in
late Eocene
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Includes Stellar’s sea cow (extant into historical times)
Some temperate species
Large body size
Loss of tusks
May have fed on kelp high in the water column
Steller’s sea cow
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Named after Georg Steller
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Extinct by 1768 (27 years after discovery)
– Mainly Russian hunting, but possibly exacerbated by aboriginal hunting
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7.6m long, 4-10 tons
Lacked teeth, had bark-like skin
Cold waters near islands of the Bering Sea
– Prehistorically from Japan to Baja California (to Montery 19,000 years ago)
Dugonginae
Currently one species, but once many genera
Tropical and subtropical
Once widespread; 15 mya from North and South America, Caribbean, Mediterranean, Indian Ocean,
North Pacific
Some extinct species used tusks to dig up seagrasses
Modern dugongs use tusks socially, not for feeding
Sirenian evolution in the Caribbean (Domning 2001)
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From Oligocene onwards, there was a great diversity of sirenians in the Caribbean, especially dugongids
Seagrass communities were similar to extant ones but were more diverse
Habitat could be partitioned along several axes
– Rhizome size
– Location of feeding in water column
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Morphology of sirenians reflects partitioning of seagrass resources
– Body size differences lead to differences in access to shallow waters and ability to consume more
fibrous seagrasses (bigger are better)
– Rostral deflection influences ability to feed on the bottom or on midwater or surface plants and
ability to dig
– Tusk size influences ability to dig out largest rhizomes
– Interaction of tusk size and defection can be complex
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Why so few species today?
Close of Central American Seaway about 3 mya led to major shifts in habitats
– Dugongids died out along with large rhizome seagrasses
– Manatees were able to disperse into open marine habitats to move into North America and to West
Africa
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Desmostylia: Sirenian Relatives
Only extinct Order of marine mammals
Confined to North Pacific (Japan through N. America)
Late Oligocene to Middle Miocene (33-10mya)
Hippo-like amphibious quadropeds
More closely related to elephants than sirenians
Probably fed on algae and seagrasses in subtropical and cool-temperate waters
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Locomotion probably like polar bears
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Thalassocnus
Aquatic ground sloth!
Pliocene marine rocks of Peru
Medium to giant sized herbivores
Aquatic or semi-aquatic grazer on seagrasses or seaweeds (well developed lip for grazing)
Probably swam with tail
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Kolponomos
Bear-like carnivore (early Miocene)
Massive skull, down-turned snout, broad crushing teeth
Coastal habitat feeding on marine invertebrates on rocks and crushed their shells
Sea otter only marine mammal that may be similar in habitat
Relationships problematic
– Appears to be closely related to basal ursids and forms leading to pinnipedimorphs
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Sea otter Enhydra lutris
Smallest marine mammal but largest mustelids
Three subspecies across northern Pacific
E. lutris arose in North Pacific early Pleistocene (1-3mya)
Several extinct species from Africa, Europe, and Eastern United States that appear to have
consumed extremely hard prey items like modern otters
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Polar Bear Ursus maritimus
Most recently derived marine mammals
Descended from lineage of brown bears during middle Pleistocene (300,000-400,000 ya)
Brown bears of southeast Alaskan islands closest relatives
Conservation and Management of Marine Mammals
Conservation
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The preservation of biological diversity which may include
– Species richness and diversity
– Evolutionarily significant units (ESU)
– Genetic variation
– Communities
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Does not rely on management of resources for human exploitation or not.
Many conservation and management decisions are extremely difficult and involve serious trade-offs
This lecture is a primer on conservation and management . . . Keep these themes in mind as we go
through the rest of the semester
What do you conserve?
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Resources are limited and many decisions are painful
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Taylor and Dizon: goal should be to maintain full historical range of a species including feeding and
breeding grounds
Sustainable Exploitation
Historically marine mammals have been conserved as exploitable resources
Theoretically animal populations can be exploited indefinitely as long as too many individuals are not
taken
Maximum Sustainable Yield
Precautionary Principle and the Burden of Proof
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In general, conserve species that are of low abundance, but invest in preserving large populations
– Small populations are vulnerable!
– What is a population?
• Geographic barriers
• Genetic and evolutionary techniques
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The precautionary principle states that decisions should error on the side of not having a major effect
(incorporate uncertainty and a buffer)
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Burden of Proof is currently for conservationists to prove there is an impact
– This is backwards!!! If you want to make sure resources are around for generations, exploiters
should have to prove that there is not going to be an impact
Risks for Marine Mammals: Direct effects
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Many species have been deliberately killed for profit, subsistence, or control
– Indigenous humans
– Commercial Whaling and Sealing
• Extinction of the Steller’s sea cow
– Competition (or perception of competition) leading to culls
• Pinnipeds particularly vulnerable
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Direct effects are not always targeted at killing marine mammals
– Loud Sounds in the Ocean
– Interactions with fishing gear
• Deliberate nets set or incidental entanglement
– Ship Strikes
– Toxins in the environment
• Oil spills
• Organochlorides
Risks for Marine Mammals: Indirect effects
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Reduction in prey resources
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Habitat Alterations
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Climate change
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– Competition with human fisheries
– Navy in particular
– The science is solid: human-caused climate change is happening
Aboriginal Exploitation
Aboriginal populations have exploited marine mammal populations for subsistence on all continents
except Antarctica
Pinnipeds at rookeries and haul outs most often exploited, but also nearshore cetaceans
Effects of aboriginal hunting pressure relatively localized compared to commercial hunting
Aboriginal hunting continues in many locations throughout the world
• Pinnipeds, polar bears, otters, cetaceans in the Arctic
• Cetaceans and sirenians in more tropical areas
Historical Exploitation
Can marine mammals be exploited in a sustainable manner?
– Some places make it look likely
• Long-finned pilot whales (Azores)
• South American fur seals (Uruguay)
• Belugas (Canada)
– Deliberate killing most often results in population decline or extinction
Commercial Hunting
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Commercial sealing, ottering, and whaling has drastically reduced many populations leading to many
current-day conservation problems
– Some populations reduced so much they can’t recover on their own
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Several species extinctions at least partly due to overexploitation
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Near-extinctions as well
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– Steller’s Sea Cow
– Extinct in 25 years of exploitation
– Caribbean monk seal
– Atlantic gray whale
– Northern right whale
– Manatee populations
Sea otters, all fur seals, hooded seals, elephant seals, walrus heavily exploited for skins and oil in early
19th century
California sea otter, N. elephant seal thought to be extinct by late 19th century
Several species of pinnipeds have rebounded well with end of exploitation
– Southern hemisphere fur seals, Baltic sea harbor seals
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Commercial Exploitation
By early 19th century New England whalers were hunting the Pacific and Indian Oceans
– Looking for slow-swimming whales easily harpooned by hand
• Sperm, bowhead, right, gray
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– By end of century, both right whales, bowhead, gray whales severely depleted
Cannon-fired harpoon invented in 1860 and steam-powered catcher boats allowed exploitation of
rorqual whales (faster)
Rorquals first exploited from land-stations
– First in Antarctica in 1904 (195 kills)
– 6 land stations, 21 floating factories in 1913 (10,760 kills)
1925: Stern slipway allows pelagic factory ships to pull whales in
– Catches up from 176 blues in 1910 to 37,000 whales (most blue) in 1931 with 41 factory
ships
Blue whale catches dropped to insignificance by 1950s; only 70 taken worldwide in 1966
With few blue whales, whalers switched to progressively smaller rorquals
Other cetaceans taken less often commercially, but some drive-fisheries for odontocetes continue
– Azores
– Asia
Commercial exploitation of seals still occurs in many places
Culling (Control Killing)
Mammalian predators in many habitats are killed because of killing of domestic animals or
competition for resources, marine mammals are no different
– Perceived and real competition for fish and invertebrates
– Damage to nets or lines
– Threat to humans (polar bears)
Pinnipeds often targeted
– Gray and harbor seals in Sweden USA and Canada had bounties put on them
– Sometimes governments directly organize culls
Belugas in St. Lawrence and small odontocetes in Japan also targeted
Other than belugas and odontocetes, these culls don’t appear to have had huge populationendangerment impacts
Bycatch
Many marine mammals (in addition to many other taxa) are captured in fishing operations even
though they are not the target of operations
– Passive gear (gillnets) is most dangerous
– Active gear (purse seines, trawls, longlines) also kill marine mammals; also may cause
culls when fisherman see catch stolen
– Anti-shark nets
– Discarded gear
For many species, bycatch mortality is a much greater threat than intentional killing
Bycatch rates may be non-sustainable
– Vaquita (Gulf of California), baiji (Yangtze) harbor porpoises (N Atlantic), striped
dolphins (Mediterranean), northern right whale dolphins (North Pacific)
Discarded gear may be responsible for declines of populations of Hawaiian monk seals and
northern fur seals
Dolphins and Tuna
Tuna purse seiners have long exploited the association between yellowfin (mainly) tuna and
dolphins (Stenella attenuata S. longirostris Delphinus delphis)
Site a school of dolphins and set around it
Hundreds of thousands of dolphins were killed in the nets every year
Marine Mammal Protection Act, sets on logs, and better methods for releasing dolphins from nets
have led to reduced catches
• Backdown procedure and Medina panels
Impact to dolphins may be underestimated
– calf separation from mothers not accounted for
– would increase kill of spinner dolphins 6-10% and spotted dolphins 10-15%
From an ecological standpoint, dolphin safe is not necessarily a better option
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Large bycatch of other species
Smaller tuna
Vessel collisions
Vessel collisions have become a major threat to several marine mammal species
First recognized for manatees
– Primary cause of anthropogenic mortality since 1974
– Ship collisions with right whales a major problem
• Are alarm signals the answer? (Nowacek et al.)
– Young cetaceans also at risk
Acute mortality events
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Viral infection
– 1987-88: 5-10k Baikal seals, 17K harbor seals in Europe (morbillivirus)
– Human links often a bit unclear but likely
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Oil spills
– Species with fur most vulnerable
– Exxon Valdez 1000s of otters, 300 harbor seals in Prince William Sound
Environmental Contaminants
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Many areas heavily polluted; organochlorides (especially PCBs) are especially bad
– may reduce immune function, increase chance of viral infection
– Interfere with embryo implantation in seals
– Subject to bioaccumulation (build up in fat)
– Transferred to young through milk
Geographic variation in organochloride loads
– St. Lawrence river belugas heavily polluted with heavy metals OCs, other pollutants and have high
rates of infection
– Killer whales (WA, BC), California Sea lions (N. Pac.), ringed and gray seals (Baltic) are
experiencing reproductive failures associated with contaminants
Indirect Effects
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Many threats to marine mammals may not result in the immediate death of individuals, but may be more
important through reductions in carrying capacity or impacts on reproductive or survival abilities
Habitat alteration
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Critical habitat: areas vital to the survival of marine species at some point in their life
– Location where density dependence occurs
– May include breeding and/or foraging habitats
– Can’t be considered in isolation from other species
– “ . . . must provide resources that determine the abundance of a species through density-dependent
or Allee effects” (Harwood 2001)
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Some habitats are increasing in area, like offshore islands for pinnipeds that people no longer populate
while others are being negatively impacted
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Changes in the physical structure of the environment or prey resources can lower K; not wellestablished, but likely widespread
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Stellar sea lions may be declining due to reductions in prey (also bycatch, culling by fishermen,
commercial hunting until 1972)
– Prey changes may be due to biomass reduction or prey type change (fatty herring to trashy pollock)
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Changes to the flow rate and course in rivers can modify available habitat
– Indus river dolphins may have lost ½ of habitat
– Damns and flood control may block migrations of manatees and river dolphins
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Ice habitats are being altered and in some cases reduced dramatically
– Early breakup of winter sea ice reduces bear foraging intake
– Less habitat for some ice-breeding seals (especially Caspian and Baikal seals that rely on stable
winter ice)
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Suitable beaches for Mediterranean monk seals being taken over by people
Climate Change
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Changes in currents and climates are likely to have huge effects on marine mammals
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Most drastic consequences likely in polar regions for species that rely on ice
– Changes in prey resources and primary productivity
– Changes in temperatures (many species in narrow temperature bands)
– Shutdown of upwelling during El Niño causes huge falls in otariid populations of S. America
– Phocid seals, polar bears, walrus
– May already have reduced ringed seal availability to polar bears leading to reduced reproductive
success
– Polar bears having hard time finding ice in some cases
– Shifts in currents in Pacific may have caused reduction in monk seal yoy survival
Disturbance
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Disturbance can lead to reduced foraging efficiency, reproductive disruption, and abandonment of
habitats
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Daily tours by two commercial sailing vessels in Shark Bay resulted in reduction in some dolphins
abandoning portions of their home range
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Impacts of boat traffic and other human disturbance still poorly known for most marine mammals
Strandings
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Single and group strandings have long been a curiosity
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Mass strandings are those with
Refers to live cetaceans and sirenians that intentionally swim onto shore or are unintentionally trapped
by waves or tides (not the same as “beached”)
> 3 individuals of the same species
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Pinnipeds along US West coast stranded or beached due to
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Algal biotoxins (red tide) often implicated for manatees and some cetaceans
– Gun shots, disease, predation/parasitism
Mass Strandings
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20 species of odontocetes, most common:
– Pilot whales, false killer whales, sperm whales
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Explanations
– Non-lethal infections
– Panic flight responses
– Social bonds (follow the sick individual)
– Nearshore disorientation (echolocation, magnetic fields)
– Loud sounds in the ocean
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Probably a mix; infections and bonds likely
Conservation Efforts
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All of the threats we have talked about are currently being addressed in at least some parts of the world,
but their effectiveness varies considerably and some species aren’t going to make it
Direct Killing: Things to Consider
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First step is to define goal
– Maximize profits or production
– Minimize extinction risk
– Optimize risk and human benefit
Management must account for uncertainty
Scale of agreement critical
– International often necessary
– Unilateral management of walrus (US, Russia) has led to wide fluctuations
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Management must be sensitive to history of local people (maintain populations and cultures)
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Commercial whaling banned for decades but “scientific whaling” continues
– However, traditional view often broken by profit possibilities
Keeping marine mammals safe
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Pingers can be attached to nets to keep some species away
– Harbor porpoises in the Gulf of Maine
International treaties to ban some gillnets, attempt to reduce discarded gear
Clean-up attempts
– Hawaiian monk seal
Reducing indirect impacts
Need to establish the effects of changes to habitat or prey
Currently not much is being done to work on these problems
– Especially climate change!
First step is probably gaining a functional understanding of species interactions
Supplementing Populations
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Translocations
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Captive breeding
– Not always a good idea, but sometimes useful for highly endangered populations
– Sea otters (CA), harbor seals (Europe), monk seals (Hawaii)
– Have not been used for marine mammals
– Thought about for baiji, but a failure (couldn’t capture enough individuals)
Habitat Protection
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Reserves need to be carefully planned
– Individual movements/migrations
– Source-sink dynamics
– Resource dynamics and movements
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Large IWC sanctuaries in the Indian Ocean and circumpolar Antarctic
– Only closed to commercial whaling, other threats remain
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Several pinniped rookeries are protected
– Año Nuevo for elephant seals
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Sanctuary for Hector’s dolphins in New Zealand (gillnet protection)
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Gray whale “nursery” lagoons in Mexico
Upper Gulf of California for the vaquita
While these reserves are nice, an ecosystem approach would be preferable
Just reducing anthropogenic disturbance and mortality is not enough
Ecosystem conservation preserves habitats and interacting species making long term survival more
likely
A better way to make money
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Ecotourism
– Whale watching and viewing of other marine mammals is growing rapidly and often allows local
human populations to benefit without killing individuals
– Whale watching especially growing rapidly
– Must be careful not to have negative impact
– Humpback cows and calves off Maui may have shifted habitats in response to boat traffic
– Gray whales may have shifted migratory paths
– Some locations allow swimming with wild dolphins, but largely discouraged
– Feeding of marine mammals outlawed in many places
– Monkey Mia: a unique spot
– 3-12 dolphins being provisioned since 1960s
– 100,000 visitors a year
– Problems with calf survival until new management practices brought in
Conservation Status
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Some species are rebounding well
– Gray whales and most other large baleen whales
– Northern elephant seals
– California sea otters
– Southern hemisphere fur seals
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Some aren’t
– Continued problems for Steller sea lions
• Down from 250,000 (1960) to 90,000 (1989)
– Vaquita still declining due to mortality in fishing nets
– Baiji and other Asian river dolphins in big trouble and may become extinct
– Northern right whale still at risk
Adaptations to the Marine Environment
Challenges of living in water
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Drag (physical forces that reduce forward movement)
– 60x more viscous than air and 800x denser
– But provides support – easy to generate propulsion
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Pressure change
– Additional 1 atm/10m; crushing at depth
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Heat loss
– 24x thermal conductivity of air
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Salt Balance
– High salinity challenges water and electrolyte balance
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No usable oxygen
– Must take oxygen from the surface
Adaptations involve
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Swimming and locomotion
Thermoregulation
Osmoregulation
Diving and breath holding
Structure and Locomotion
Major trends in marine mammals skeletal system
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Streamlining of the body
– Loss or reduction of much of the appendicular skeleton
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Enlarged propulsive appendages
Cetaceans typify trends
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Gradual reduction of limbs and streamlining
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There are costs associated with transitional forms!
Body shape and hydrodynamics
Drag can be calculated by
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Ambulocetus
– could walk on land
– in water, like sea otters
p = fluid density, V = swimming velocity, A = frontal area of body, Cd = drag coefficient (accounts for
flow characteristics of fluid around body)
Consequences of drag
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Swimming faster causes more drag fast
Larger frontal area increases drag
Poor flow increases drag
Four types of drag
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1. Frictional Drag
– Interaction of the animal’s surface with the water surrounding its body
– Cab be reduced by reducing SA/VOL ratio
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2. Pressure Drag
– Need to displace the amount of water equal to animals largest frontal area
Size and shape affect magnitude
Predominate when submerged
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3. Induced Drag
– Associated with flow around flippers, fins, etc
– Results from pressure difference between two surfaces of hydrofoil and formation of vortices at tips
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4. Wave Drag
– Energy that could be used for forward motion used to create waves
– Total drag 4-5x higher when moving near surface
– Becomes negligible 3 body diameter below surface
How to minimize drag
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Be streamlined
– Ideal shape is bluntly rounded at front, round cross section, and tapered toward rear
– Finess ratio (FR) helps to find optimum length/area
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Optimum FR for fast-swimming 3-7 (optimum 4.5)
Odontocetes, otariids, phocids 3.3-8.0
Balaenopteridae 4.8-8.1, Balaenidae 3.3-8.0
Weird ones: northern right whale dolphin (Lissodelphis borealis), minks, river otters 9-11
How to minimize drag
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Appendages with rounded leading edges that taper toward tail
– Similar morphology in very different lineages
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Don’t try to swim fast on the surface or minimize time at the surface
If you must come to the surface fast, reduce drag by porpoising or leaping while getting air
– Cross-over speed: speed at which leaping becomes cheaper energetically
– C-O speed 5 m/sec in spotted dolphins increases with body size until too costly at >10m
Locomotion Modes in Marine Mammals
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Several modes of locomotion found in marine mammals that reflect degree of aquatic specialization
We’ll look at structure and mode of locomotion for major taxa before returning to the implications for
energetic costs
Polar bear
Largest bear species, but smaller than recent ancestors
Large feet aid in swimming
Pulls through water with forelimbs, hindlimbs trail behind
Postscapular fossa allows attachment of subscapularis muscle
– Position aids in pulling heavy body for swimming (climbing in other bears)
Large paws distrubute body weight on land
Foot pads have small soft papillae that increase friction with ice
Usually walk with lateral, not diagonal, legs
Can reach 40 kph on land
Sea otter
Increased development of posterior areas
– Greater muscle mass
– Increased height of neural spines and transverse processes that provide attachment
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Pelvis is elevated to almost in line with spine
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Terrestrial locomotion slow and clumsy because of large hind feet
– Walk or bounce on land, can’t run (bounce to go fast)
– Use alternate limbs
Sea otter aquatic locomotion
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Pelvic paddling using hind limb propulsion and pelvic undulation of the vertebral column
Femur, tibia, fibula relatively short
Elongated toe bones
– Skin web between hinddigits
– Hind foot 2x as wide when digits spread
– 4th and 5th digits closely bound to add rigidity for propulsion
Giant extinct otter was forelimb paddler
Three swimming modes
– Ventral up swimming
– Ventral down swimming
– Alternate ventral up and down swimming
– Ventral up swimming
• Used during food consumption and initial escape
• Alternate or simultaneous strokes of hind feet
• Some lateral undulation of tail to maneuver
– Ventral down swimming
• During intermediate speed traveling and before high speed diving
• Alternate or simultaneous strokes of hind feet, no role of tail or forefoot
– Alternate ventral up and down swimming
• Use hindpaws
• During periods of grooming while traveling forward
Pinnipeds
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Front and hind limbs lie within body outline
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Hind flippers have elongated digits I and V
Otariids: Terrestrial locomotion
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Limb based, can use foreflippers to push up, but propulsion more from movements of head and neck
rather than hind limbs
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Walk and gallop gaits, depend on environment
– Sandy: limbs moved in alternative and independent sequence
– Rocky: bounding that displaces center of gravity vertically. Hind limbs in unison.
Phocids: Terrestrial locomotion
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Move through vertical undulations of the body trunk
– Arch lumbar region and bring pelvis forward while sternum take weight
– Extend anterior end of body while pelvis takes weight
– Forelimbs may help by lifting and thrusting anterior regions
– Can’t turn hind limbs forward; not used
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Phocids have eversion of the ilium for greater muscle attachment responsible for body movements in
swimming
Some ice-dwelling species use lateral undulations of the body
– Use backward strokes of forelimbs and lateral movement of posterior torso (hind limbs lifted)
– Can be very fast
– Seen in leopard, crabeater, ribbon, harp seals
Odobenids: Terrestrial locomotion
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Similar to otariids, can rotate hind limbs forward
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Pectoral oscillation (forelimb flapping)
– Produce thrust like birds in flight
– Move in unison, act as oscillatory hydrofoils
– Power, paddle, and recover phases
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Hind limbs provide maneuverability
Phocids: Aquatic locomotion
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Pelvic oscillation (hind limb swimming)
– Hind limbs used in lateral undulation of lumbosacral region
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Forelimbs steer
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Pelvic oscillation like phocids
Weight is supported by belly on ground rather than limbs!
Feet move in lateral sequence followed by lunge for propulsion
Otariids: Aquatic locomotion
Odobenids: Aquatic locomotion
Cetaceans: structure to aid locomotion
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Thoracic and lumbar vertebrae restrained by strong collagenous subdermal conntective tissue sheath
– Gives rigidity to thorax
– Provides enlarged surface for tail flexor and extensor muscles
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Ligaments between vertebrae in tension during extension and flexion of the tail
– Dolphin vertebral column can store elastic energy and dampen oscillations and control body
deformation during swimming
Cetacean locomotion
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Vertical oscillations of the tail
Caudal propulsion improves efficiency at higher sustained velocities
Thrust is generated by up- and downstrokes, but more from upstroke
Elastic rebound of connective tissues increases energy efficiency
Maneuverability: an odontocete problem
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Maresh et al. 2004 investigated the problem of how Tursiops truncatus is able to catch smaller, more
maneuverable prey
What did they discover?
How did they address this problem?
Sirenian Locomotion
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Caudal oscillation for propulsion
– Body changes pitch (degree changes with power of stroke)
– Tail can be used to bank, steer and roll
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Slow swimmers, unable to sustain or reach high speeds (usually 0.6-0.8 m/s)
– Slow speeds allows greater maneuverability
– Can reach 22 kpm (6 m/s) during flight sprints
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Flippers primarily for maneuvering, but may use to slowly paddle (juveniles may use a lot)
– manatee shoulder muscles reflect habitats that require greater maneuvering than dugongs
– Manatees use mainly for left-right turns
– Dugongs also use to maintain balance
Evolution of Sirenian Locomotion
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Three stages
– Quadropedal: trusts with alternate limbs
– Dorsovenral spinal undulation and thrusts of hindlimbs
– Tail swimming only
Cost of Transport (COT)
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Swimming and diving are major energy sinks
– Can account for 82% of daytime activity budget (Tursiops)
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COT useful for comparing locomotor efficiencies
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Where P Is Power required to move body mass (M) at a given velocity (V)
Power curve is usually U shaped – lowest transport cost at intermediate velocities
COT varies with body size
Swimming is least costly (body supported)
Cetaceans reduce COT by wave-riding
COT of dolphins lower than pinnipeds
COT is higher than predicted for fishes of their size (due to high metabolic rate, warm blooded)
Swimming and migration speeds (2m/s) very close to predicted optimum for minimizing COT
Swimming speeds
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Cruising swimming speeds not very different based on swimming modes and body sizes
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Sprint speeds can be much higher
– Amazingly narrow range 1.3-3.6 m/s
Adaptations: Thermoregulation and Osmoregulation
Two major challenges in water
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Staying warm
– Waters are cooler than internal body temperatures of mammals; many marine mammals live in polar
climates
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– Water is a good heat conductor
– Transfers heat 24x faster than air
– Body heat is lost rapidly
– Typical mammalian hair isn’t the greatest insulator when wet
– Many solutions to staying warm
Maintaining salt balance
– Steep gradient between solute concentrations in blood and that in saltwater
– Trick is maintaining electrolyte balance in body fluids: keep the water from flowing out of the body
Staying warm: methods
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Change body shape (be round)
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Have external insulation (be furry)
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Have internal insulation (be fat)
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Generate your own heat (be a furnace)
– Low SA/VOL ratio reduces rate of heat loss
– Fur can help to insulate the body and trap body heat
– Fat and blubber stores are great insulators and can be burned to produce heat
– Increase activity
– Shiver
– Process food
– Metabolize fat (non shivering heat production)
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Don’t waste heat (be a heat conserver)
– Countercurrent heat exchangers
– Peripheral vasoconstriction
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Choose the right place to warm (cool)
– Behavioral thermoregulation
Which of these are long-term and which are short term?
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Change body shape (be round)
Have external insulation (be furry)
Have internal insulation (be fat)
Generate your own heat (be a furnace)
Don’t waste heat (be a heat conserver)
Choose the right place to warm (cool)
Being round
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SA/VOL ratios must be optimized with streamlining
Marine mammals have, on average 23% lower SA than similar sized terrestrial mammals
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Many species in cold climates are very stocky
External insulation: Fur
Polar bears, sea otters, and pinnipeds covered by fur, but fur differs among species
Consists of two layers
– Guard hairs (outer protective layer)
– Underfur hairs (soft inner layer)
Polar bear hair once thought to direct light to skin to warm animal is incorrect
Sea otter fur
Most dense fur of any mammal
2
– 125,000 hairs/cm (twice fur seal)
– Greatly reduces heat loss
Guard hairs sparse
– Protect underhair integrity when wet
– Trap air when emerge from water
Underhairs are wavy
– Trap and maintain air when submerged
Lack arrector pili muscles that erect hair
– May help in streamlining by letting hair lay flat during submersion
Only source of insulation yet almost never leave water
– Cost: 12% of day spent grooming to maintain water repellency and insulative value
Pinniped pelage
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Monk and elephant seals and walrus lack underfur
Otarrid fur is uniformly arranged, phocid and walrus fur clumped
Lack arrector pili muscles that erect hair
Ntal coat differs from adult coat
– Monk and elephant seal pups are black
– Phocines, walrus white or gray
– Otarrids dark brown to black
– Lanugo is longer than adult pelage and helps conserve heat on land, but is not a good insulator in the
water
– White hair focuses heat and long hairs trap heat near body
Moulting
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Phocids, sea otters, and beluga whale molt annually
Otariids renew pelt gradually throughout year and many cetaceans lose skin continuously
Phocids must molt on shore to keep skin warm enough
– For pinnipeds, opportunity to renew and repair pelt and epidermis
– Occurs in summer and autumn in S. hemisphere
– More variable timing in N. hemisphere usually in spring
– Begins around face then abdomen and back
– Speed variable (25d elephant seal; 10-170d harbor seal
– Usually involves hairs lost individually, but monk and elephant seals shed attached to sheets of
epidermis
Natal Moulting
– Usually lost in few days to few months
– Hooded and harbor seals lose in utero
– Likely because natal coat evolved for ice breeding, loss is secondary adaptation to land breeding
– Unlikely since hooded seal on ice
– More likely adaptation for being inundated by water at early age (natal coat poor when wet)
Coloration of Coverings
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Coloration of marine mammals can serve a variety of functions
– Camouflage
– Communication
– Species ID
– Sexual display
– Foraging aid
Phocid coloration
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Only pinnipeds that aren’t fairly uniform
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Many color patters help seals blend in
Pagophilic (ice breeding) species have disruptive coloration of contrasting light and dark
– Harp and ribbon seal patterns develop with age and vary by gender (most extreme in males)
Cetacean coloration
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Three types
– Uniform (e.g. beluga)
– Spotted or striped with sharp colored areas on head side, belly, flukes (e.g. killer whale)
– Saddled or countershaded (e.g. most dolphins)
• Helps to blend in when seen from above or below
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Presence of “capes” can provide information about rotation to other group members
Internal insulation: blubber, the choice insulation
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Many marine mammals make use of blubber (hypodermis) to stay warm
– Loose connective tissue composed of fat cells interlayered with collagen bundles
– Loosely connected to underlying muscle
– Thickness and lipid content vary with species, age, sex, location, and season
• Bottlenose dolphins may vary up to 2mm/month
Blubber
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Otariids rely on fur and underlying blubber
Phocids, sirenians, and cetaceans rely solely on a think blubber layer
Blubber thinnest in sirenians and sea otters, thickest in blue whales (ave 23 cm, max 50 cm depth)
Blubber thermal conductivity
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Thermal conductivity is inverse of insulative value
– Depends on thickness and peripheral blood flow
– Thermal conductivity largely influenced by lipid content
• Higher lipid content and greater thickness at higher latitudes
• Harbor porpoise blubber (81% lipid) has 4x insulative value of spotted dolphin (55% lipid)
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Pinniped blubber better insulator than cetacean blubber because little fibrous material
Insulation value depends on distribution
– if distributed around body core, lose heat more slowly
Pinniped distribution+blubber thickness
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High latitude distribution of some pinnipeds may be limited by insulation layer
– Cold air temperatures may be limiting during breeding season through effects on pups that are
fasting after weaning
– Thinner blubber layer and lower metabolic rate to conserve blubber for entering water
– Appears to be case for gray seals, but generality unclear
Other uses of blubber
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Used in metabolic heat production as well as insulation
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Possible anti-predator function in cetaceans
Distributed to optimize streamlining
Serves as energy store
– Most of energy stores for some species
– Appears to be thicker than needed in some locations
Heat conservation: Heat exchangers
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Rete mirabilia (miraculous network)
– Massive contorted spiral of blood vessels (primarily arteries with some thin-walled veins)
– Form blocks of tissue on inner dorsal wall of thoracic cavity and extremities or periphery of the
body
– Found in many other taxa
• Sharks, tuna, billfish, wading birds, anteaters, lemurs, sloths
Countercurrent heat exchangers
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Retia work as Countercurrent heat exchangers
– Works through transfer of heat by setting up heat differential between opposing blood flow
– Cools down warm blood as it flows to periphery
– Warms cool blood moving back to body
– Found in flippers, fins, flukes
– Conserve body temperature
– Baleen whales have CCHE in mouths to reduce loss of heat when feeding in cold water
– Sirenian CCHE best developed in tail, but found throughout body
Countercurrent heat exchangers and staying cool
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CCHE associated with reproductive tracts
Phocids and dolphins use to cool testes or fetus
– Phocids run from extreme hindflippers (6-7°C lower temp @ testes than body core)
– Dolphins run from flukes and dorsal fin
Countercurrent heat exchangers and staying cool (Elsner et al. 2004)
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Bowhead whales have CCE and arteriovenous anatosomes (AVAs)
To stay warm, blood is shunted into CCE and away from AVAs
To cool, blood is shunted to AVAs
Peripheral vasoconstriction
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Helps in diving, but also reduces amount of heat lost
– Less blood cooled
Heat production
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Variety of mechanisms
– High metabolic rate
– Appear to be relatively high for many MM
– Sirenians are an exception: 25-30% of expected for terrestrial mammal
– Increase activity
– May be necessary for many species to stay warm (e.g. Tursiops truncatus, Stenella longirostris)
– Process food
– Shivering
– Non-shivering thermogenesis (fat burning)
Sea otter heat production
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Have high basal metabolic rate (2.4x expected for terrestrial mammal)
Increase activity level as water temperature drops
Use heat produced during digestion to increase core body temperature
Relative use of these in other marine mammals poorly known
Behavioral thermoregulation
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Environment differs in temperature, and marine mammals can make use of this to warm up or stay cool
– Warm surface waters for deep divers
– Basking for pinnipeds
– Will also rest in water with flippers sticking up into air
– Seasonal migrations
– Manatees and power plants
Thermoregulation in pinniped pups
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Lack blubber at birth
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Adaptations to heat conservation when in the water may lead to difficulties staying cool on land for
pinnipeds
– Some have hypothesized that pinniped distribution toward low latitudes is limited by high
temperatures on land and difficulties in staying cool
– In warmer areas, pinnipeds need to move into the water to cool off occasionally
– Elephant seals flip sand on their backs to stay cool by digging up cool sand
– Monk seals dig holes to cool layers or rest on damp sand
– Northern fur seals pant
Osmoregulation
Possess brown fat (also found in hibernating mammals and human babies)
– Keeps pups warm through nonshivering thermogenesis: metabolizing fat to produce heat
– Converted into blubber in a few days
Thermoregulation on land
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Refers to maintaining salt (electrolytes) and water balance in internal environment
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Marine mammals are hypoosmotic
– Body fluids have lower salt concentration than surrounding water
– In danger of losing water through osmosis
Balancing salt and water
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Feeding and water ingestion alter osmoregulatory balance
– Most (or all) water ingestion from food intake
Reestablished by urine, feces, evaporation; Kidneys are organ responsible for balance
Kidneys of marine mammals
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Many species have large kidneys, but not all (e.g. elephant seals)
– Kidney:body mass ratios
• 0.44-1.0% cetaceans; 0.3-0.4% terrestrial mammals
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Pinnipeds, cetaceans, polar bear and sea otter have reniculate kidney
– Many small lobes (reniculi)
– Each lobe functions as mini-kidney
– Cetaceans have 100s to 3000 reniculi in kidney
– Number of reniculi depends on salinity of diet
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Sirenian kidneys are not reniculate
Dugong kidneys are elongate, smooth, and have some characteristics of ungulate kidneys
Dugongs are physiologically independent of freshwater
Manatees must have access to fresh or brackish water to maintain osmotic balance for prolonged periods
Drinking and water sources
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Marine mammals will drink freshwater when it is available
– Some pinnipeds in polar areas eat ice
– Is it needed? Not really
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Water sources
– Drinking
– Water in food
• Fish/invertebrates 60-80% water
– Water from own stores (catabolism)
• 1.07 g water/g fat; 0.4 g water/ g protein
• Used extensively during fasting
Drinking saltwater
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Allows high rate of urea production to get rid of more wastes
Associated with high protein diet
– Need to get rid of more nitrogen
Sea otters drink lots of seawater
Cetaceans and pinnipeds will drink seawater (especially adult male otariids that have prolonged fasting)
Reducing water loss
Few salt glands present in pinnipeds and none in cetaceans
Reduced urine output
Countercurrent moisture exchangers in respiratory tract
Maintaining water balance
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Water loss from exhalation can be extreme (especially on land)
– Some pinnipeds (elephant and gray seals) conserve water during breathing
– Countercurrent blood flow in the nose sets up temperature gradients
– Increased surface area in nasal passages
– Moisture in exhalation condenses on epithelium then humidifies inhaled air on way to the lungs
Adaptations: Sensory Systems
Marine mammal sensory abilities
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Life underwater presents unique challenges in trying to navigate, find food, avoid predators, and interact
with conspecifics due to low light and visibility conditions
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Most species rely heavily on numerous sensory systems working in concert
Many marine mammal systems highly modified from terrestrial mammals
In this lecture, we’ll look at all but sound production and echolocation
Mechanoreception
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Includes:
– Touch
– Hydrodynamic reception
– Sensing vibration and water disturbance
– Audition
– Sensing sound waves
Touch
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Other than whiskers, receptor units are distributed across entire body
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Most specialized mechanoreceptors are vibrissae (whiskers or sinus hairs)
– Specialized sensory hairs
– Diameter and structure reflect does not reflect importance but adaptation to signals received and
transmitted (sensitivity and function)
– Used for tactile information but may also detect vibrations
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Occur only on face
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Three types of vibrissae
– Rhinal
• 1 or 2/side just posterior to nostril (phocids only)
– Supraorbital
• Above eye, mostly immobile
– Mystacial
• Upper lip, mobile
• Most prominent and numerous
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Walruses have most (600-700)
Head area most sensitive for tactile information
– Skin sensitivity in dolphins may be used to help with drag reduction, but most interest in other
species focuses on whiskers
Pinniped Vibrissae
Differ from terrestrial mammals
– Enlargement of whiskers and site of innervation different in pinnipeds
– Stiffer hair in pinnipeds
– Follicles surrounded by 3 (not 2) blood sinuses
Pinniped vibrissae structure
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Number of nerve fibers (1000-1600) passing through capsule in Phoca hispida is 10x greater than
terrestrial species with sensitive whiskers
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Mechanoreception is decreased when skin is cold, so how do pinnipeds manage to use vibrissae in such
cold conditions?
– No vasoconstriction to vibrissal pads (selective heating)
– Highlights importance of this sensory mode
Pinniped Vibrissae
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Extremely sensitive
– Baltic seal vibrissae have 10x nerve fibers of terrestrial mammals
– Size discrimination abilities of harbor seals and CA sea lions are similar to primate hands and close
to visual capabilities of the seal which shows the importance of this sensory system (Denhardt and
Kaminski 1995)
– Move head side to side when object is small but don’t need to for large objects (touch multiple
vibrissae simultaneously)
Pinniped Vibrissae function
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Tactile receptors
– Mystacial vibrissae used for discrimination of textured surfaces (location, shape, size, surface
texture)
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Navigation
– Can help navigation in total darkness and low visibility conditions
– Use as speedometer, sense direction changes
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Prey detection and capture
– Even blind seals found to be well-fed in wild
– Often used to scan for benthic prey
Cetacean Vibrissae
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Only on head along margins of upper and lower jaws
Structure and innervation suggest sensory role
Mysticetes have ~100 very thin (0.3 mm dia) immobile vibrissae on upper and lower jaw
Most odontocetes lose hair postnatally; 2-10 follicles on either side of upper jaw
– Exception are river dolphins which possess many well developed immobile vibrissae on both jaws,
but not yet shown if they are true vibrissae
Sirenian Vibrissae
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Entire muzzle covered with flexible bristle-like hairs
– Used for discrimination of textured surfaces
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Also have perioral bristles on the upper lip, oral cavity and lower jaw that are very rigid and moveable
– Manipulation of objects, further exploration once grasped
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Manatees can control facial vibrissae which may have role in feeding
Sinus hairs also lightly scattered over body
The Sirenian mouth
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Combination of muscular lips and different types of facial vibrissae form a unique system
Manatees can use this “haptic” system in a prehensile fashion to investigate objects and manipulate food
into mouth
Sea otter and polar bear vibrissae
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Sea otters have all three types of vibrissae
– Mystacial whiskers most numerous
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Few vibrissae in polar bears
Hydrodynamic Reception
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Can vibrissae of pinnipeds detect pelagic fish through water disturbances? (Denhardt et al. 1998)
– Vibrissae respond to vibrations, but took an experiment to show that this worked for water
disturbances
– Vibrissae are tuned to frequency range of fish-generated water movements
– Fish leave trails of disturbance that last minutes
– Harbor seals can detect and tract trails up to 40m long (based on blind-folded seal following
minisub)
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Sensory abilities of vibrissae help explain success of pinnipeds in dark and murky water
Audition (hearing)
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Some changes in marine mammals
– Closing mechanisms to protect the ear from penetrating water under pressure at depth
– Loss or reduction of external ear flaps to increase streamlining
– No real tradeoff for underwater hearing since external ear tissue is acoustically transparent
underwater
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A major problem is how to transmit sounds to the inner ear and localize sources
Sound localization
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In horizontal plane, determined by interaural time and intensity differences
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Tursiops is equally good at sound localization in vertical plane, but we don’t know how!
Sound travels 4.5x faster in water so information processing must be better
– Tursiops has best discrimination ability for both types of information of any mammal tested
– can localize sounds other than echolocation separated by 2-3°
How do marine mammals localize sounds?
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Terrestrial mammals underwater can’t localize sounds
– Bone conducts sound to both ears almost simultaneously
Auditory organs of odontocetes are largely isolated from the skull to avoid bone conduction (less so in
other MM)
– How does sound reach the inner ear in odontocetes?
Sound reception in odontocetes
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Two pathways
– Ear canal functions to detect low frequency sounds
– Mandible (lower jaw) can detect high frequency sounds
– Fat channels in lower jaw have impedance close to water and channel sound over pan bone to
petrotympanic bullae
Sound reception in other MM
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Mysticetes still unknown, but conventional pathway of terrestrial mammals is functional
– Distance between ears makes localization less problematic with bone conduction
Manatees have lipid-filled zygomatic process which appears to transmit sound to squamosal-periotic
complex (mechanism similar to odontocetes)
Sound reception in pinnipeds
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Appear to use conventional pathway
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Ear functional in air sensitivity depends on species
– California sea lion: best in air
– Common seal: equal
– Northern elephant seal: better underwater
Bone conduction probably most important for sound transmission
– Should limit directional sensitivity with sound through skull
– good sound-localization in some sp (Phoca vitulina)
– Poor and variable in others (Zalophus califonianus)
Hearing ranges and discrimination
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Odontocetes have widest hearing range
– Tursiops best hearing 12-75 kHz but up to 150 kHz detected
– Can discriminate frequency difference of 0.2-0.8% from 2 kHz-130 kHz
Frequency discrimination is less precise and operates over a lower frequency range in pinnipeds and
sirenians
Weeding out background noise
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Marine mammals superior to terrestrial mammals in detecting signals in noise
However, this is often not enough and vocalizations may be used to reduce masking effects
Vision
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Electromagnetic radiation changes intensity and composition as it moves deeper in water
– Becomes more monochromatic and spectrum shifts to shorter wavelengths as depth increases due to
scattering and absorption
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Eyes of marine mammals adapted to see in water and in air
Habitat and vision
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Spectral sensitivity of visual pigments should correspond to the habitat where vision is most important
– Deep-sea fishes have blue-sensitive pigments
– Shallow water fishes are green-sensitive
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Generally fits for marine mammals
– Shallow diving species green or blue-green
• E.g. spotted seal, manatee, gray whale
– Deep-diving species tend to have blue
• E.g. elephant seal, Baird’s beaked whale
– Reflects habitats as well (e.g. open ocean is bluer; arctic is greener, Weddell Seal)
Marine Mammal Eyes
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Generally resemble nocturnal mammals
– Dilatable pupil maximizes light collection
– Choroid located between retina and outer coating of eye with tapetum lucidum (light reflecting
layer)
– Retina dominated by rod-like receptors but cone-like receptors (or second type or receptor) strongly
suggested or verified
•
Two types of cones in mammals
– S: short wavelength sensitive
– M/L: medium to long wavelength sensitive
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Absence of S cones associated with nocturnal habits
Cetaceans and pinnipeds lack S cones, which appears to be adaptation for redder coastal waters
– Loss may have occurred early in evolution or should see S-cones in pelagic species (we don’t)
Do marine mammals see in color?
•
Mixed results from psychophysical methods
•
Color discrimination and adaptive nature of vision is still unclear
– Demonstrated in spotted seals, California sea lions, manatees
– Failed in bottlenose dolphins
– Fur seals can discriminate blue and green but not red and yellow from grey shades
Adaptations to seeing in water
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–
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Cornea and encased fluids have about the same refractive index as saltwater; optically inefficient
–
Trade-off: when cornea regains power in air, results in extreme near-sightedness
Refractive power restricted to lens when submerged
Most pinnipeds and cetaceans have a large almost spherical lens with high refractive power allowing
normal vision underwater
River dolphin eyes
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Most river habitats extremely murky
Sensing light and dark for orienting to surface is all that is important
Platanista indi and P. gangetica have lost the lens of the eye and are essentially blind
Visual Acuity
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Perception of fine detail at various distances
Visual acuity degrades faster in air than in water
Acuity underwater is poorer than in-air acuity of many primates, but better than many terrestrial
mammals with good vision
– e.g. elephants, antelope
Chemoreception: Olfaction
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•
Relatively little attention in marine mammals
Relative to terrestrial mammals, marine mammal olfactory systems
– Somewhat reduced in pinnipeds and sirenians
– Very reduced in baleen whales
– Absent in odontocetes
Olfaction in pinnipeds
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Olfactory systems well-developed
Have vomeronasal organ
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– Can detect scents of food in mouth
Olfaction may function in mother-pup recognition
More research needed to understand role of olfaction in pinnipeds
Chemoreception: Gustation
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Taste buds in oral cavity provide information about dissolved substances
•
More taste buds present in sirenians
Taste appears to be limited in pinnipeds and small odontocetes
– Fewer taste buds that terrestrial mammals
– They can discriminate some chemicals in sea water and can detect the four primary tastes (sour,
bitter, salty, sweet) but for most of them, detection thresholds are much higher (especially salty)
Taste in pinnipeds and other marine mammals
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Use of taste in marine mammals poorly known
May be highly specialized for detecting salinity differences at high (marine) salinities
– Harbor seals shown to be very good at this
– Could be used for finding vertical layers
– For navigation to/along oceanic fronts?
Adaptations: Sound Production and Acoustic Communication
Sound and marine mammals
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The acoustic properties of water favor sound as a sensory mode for navigating, locating prey, and
communicating
– Reaches peak in odontocetes that use echolocation to visualize marine environment
•
Nature of signals used for communication depend on their function and spatial scale
– e.g. alarm calls vs display calls vs contact calls
•
We’ll focus on vocalizations made by marine mammals both in air and underwater
Sound underwater: basics
–
Frequency (f) (a measure of time)
– Vibrations (cycles) per second
– If each cycle takes t seconds, f = 1/t
– Measured in hertz (Hz)
– 1000 Hz = 1 kilohertz (kHz)
–
Wavelength (λ) (a measure of distance)
– Distance between peeks of cycles (m)
–
Bandwidth
– frequency range of sounds that are not pure tones
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Speed of sound (c) is much greater in water (1500 m/s) than air (340 m/s)
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Sounds that marine mammals use extend both above and below range detected by human ears
C = λf
Wavelength and frequency closely related
Does wavelength increase or decrease with increasing frequency?
Decrease!
Sound basics
Infrasonic sounds are < 18 Hz
Ultrasonic sounds are >20 kHz
Sound intensity and pressure
•
Intensity (volume) (I) is the energy per unit time flowing through an area and is related to acoustic
pressure (P) by
where ρ is water density; ρc is the specific acoustic resistance
•
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In water, measurements tend to be in sound pressure levels rather than intensity
Sound pressure level differences can be measured in decibels (dB) using the equation
Where Pref is a reference pressure (1 micropascal (µPa) underwater)
Measuring sounds
•
Frequency, duration, and energy of sounds can be shown on a sonogram and frequency power spectrum
Vocal and non-vocal sounds
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For marine mammals, vocal sounds are those produced by passing air through specialized soundproducing structures
– Not restricted to those produced in the larynx
– e.g. snorts produced in pinniped are considered “vocal”
Non-vocal sounds are those produced by striking or rubbing body parts on each other or external objects
Vocal sound production: larynx
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Like terrestrial mammals, marine mammals are capable of producing sounds in the larynx
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Vocal mechanisms are poorly studies
Larynx of mysticetes has diverticulum that may act as a resonator
Unclear whether odontocetes produce sounds in the larynx
– Complex with powerful musculature and vocal folds
– Also have complex upper respiratory tract and physiological evidence support sound production
here
Pinniped vocal specializations
Sounds sources may be complex and show considerable interspecific variation
California seal lions can produce barks in the larynx but may also bark underwater without releasing
bubbles, suggesting alternative mechanisms
Interspecifc variation in otariid barks
•
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South American sea lions (breeding)
– Bark produced when lower jaw depressed
– Tongue extended and flattened
– Nostrils closed
– Suggests oral exhalation (larynx)
Australian sea lion
– Vibrating the posterior part of the tongue against soft palate
Walrus vocal complexity
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Especially during mating season, walrus show amazing array of air-borne and underwater sounds
Probably most diverse manners of sound production in pinnipeds
– Whistles through lips
– Pharyngeal sacs to produce gong-like sounds
– Highly mobile tongue allows great call diversity
Other pinniped sound production
•
Anterior tracheal membrane vibrations from air moving between trachea and larynx may allow
vocalizations in Weddell and Ross seals underwater (not vocal folds)
•
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Vibration of dorsal tracheal membrane produces songs of male bearded seals
Large tracheal air sac in male ribbon seals likely used in production of sounds but mechanism unknown
Nose sac (nasal septum) of male hooded seals used in acoustic and visual displays
Inflation and deflation of the sac produces
bloops, pings, and wooshes
Mysticete sound production
•
Despite considerable research on cetacean acoustics, sound production is poorly understood
•
In mysticetes, air must move from lungs through a valve and nasal and laryngeal sac act as resonators of
the sound
– Actual location of vibration is not critical in this model, the key is the resonation in rigin passages
and the diverticulum
•
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Odontocetes produce great diversity of sounds
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Parts of the frequency spectrum can be reinforced by resonant properties of the vocal tract (formants)
–
–
There has been much debate about the location of production, but now general agreement
–
Supported by motion x-rays that show air movement into nasal passage; no movement of the larynx
during sound production
•
The phonic lips are part of a complex called the monkey lips/dorsal bursa (MLDB) complex
– Two bilaterally placed MLDB except Physter
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As air is shunted through the lips, the MLDB vibrates
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The melon of dolphins contains fats that act as an acoustic lens to help create a focused directional beam
Odontocete sound production
Two basic types
– Bust-pulse sounds
• Includes echolocation
– Whistles
Vocal complexity
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May result in non-linear dynamics of sound
– Subharmonics
– Biphonation
– Chaos
Odontocete sound production
Cranford (2000) showed that each click produced by Tursiops was synchronized with opening of phonic
lips (“monkey lips”) an explosion of released air, and closure of the lips
Clicks generated by periodic closing of lips
Sound production in sperm whales and other odontocetes homologous
– Spermaceti organ is likely homologous to right posterior bursa
– Mellon is homologous to junk
Skull may be most important in determining directionality of sounds
– Interaction of reflection off of air sacs, skull, soft tissue
Sound production in sperm whales
Phonic lips produce clicks (dominant sound in sperm whales, called codas)
Invariant interpulse interval suggests reverberation in spermaceti organ may control inverval
– Supported by IPI-body size correlation
Clicks reflect through spermaceti organ between anterior and posterior air sacs (reflectors)
Echolocation
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Production of sound bursts and listening for echoes reflected off objects in the environment (20% of
mammals)
•
Arisen at least 5 times in mammals
– Bats, Shrews, Golden hamsters, Flying lemurs, Odontocetes
•
May occur in more species, but need captive experiments to conclusively document
•
High frequency sounds are generally thought to be used, but low frequencies may be used as well – not
well documented
Odontocete echolocation
•
Best studied in bottlenose dolphins
– High-pressure clicks (>220 dB at 1 m) over shor duration (midcroseconds)
– Short duration (50-80 µs)
– High frequency (usually centered >100 kHz)
– Bandwidth of 30-40 kHz
– May be repeated up to 600 times per sec
Echolocation detection power
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Targets with a circumference > λ reflect sound energy efficiently
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Dolphins have been shown to have good detection abilities – 2.5 cm object 72m away
Since c = λf and c = 1500 m/sec
For frequency of 100 kHz,
– 1500= λ x 100,000 or λ = 0.015m
Detection ability depends of target strength
– Varies with prey type (e.g. cephalopods vs teleosts)
Echolocation processing
•
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Odontocete brains have a large portion of their mass dedicated to sound processing
•
Some species can process pulse series together, rather than singly
Brain processes results of incoming echo before producing another click in Tursiops
– Distance from object will determine ICI
– ICI = RT+LT; round trip click travel time and Lag time for signal processing (19-45 ms for targets
at 20-120m )
Measuring echolocation in the field
•
What are the two major problems of measuring echolocation in the field?
– Beam is narrow, signals distorted if not measured on axis
– Need to know range of animal to determine power
•
What is a solution?
– Multi-hydrophone arrays to measure axis and distance to whale
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What determines the strength of an echolocation signal hitting a salmon?
– Angle, distance, noise in the environment
•
What determines the strength of an echo at the whale
– EL = SL(source level) -TL (transmission loss)+TS(target strength)
– Noise level of environment can be added
Salmon-eating killer whales and echolocation (Au et al. 2004)
•
Killer whale clicks measured when echolocating on array
•
Determined target strength of salmon based on length-weight relationships and air bladder size
•
– What are the pros and cons of this technique?
– Odontocetes can adjust SL to target range in the wild!
What did Au et al. find?
– Echolocation lower frequency and longer duration than smaller species
– Clicks are Broadband
– Whales can probably detect salmon at distances much greater than 100m (based on hearing
threshold of 48 db)
•
How could whales deal with noise in the environment that was not considered in the model?
Killer whales and echolocation
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Salmon can’t detect echolocation signals of killer whales, but some prey can
How should prey respond to echolocation if they can hear it?
How should killer whales change their behavior?
How would you test your hypothesis?
Echolocation variation
•
Porpoises and Cephalorhynchus pulses compared to Tursiops
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Must not use Tursiops as a model for all odontocete echolocation!
– 5-10x longer (150-600 µs)
– ½ bandwidth (10-20 kHz)
– Much weaker (150-170 dB; remember log scale)
– Peak frequency higher (always >100 kHz)
Echolocation variation in the wild
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False killer whales and Risso’s dolphins were studied by Madsen et al. (2004)
– Why would these two species be chosen for such a study?
– Was this a good choice?
Echolocation signals were similar but highly variable within each species
– Adjust SL to distance from target
– Can change centroid frequency
• Higher frequency gives a more directional beam
Are sperm whale codas echolocation?
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–
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Consist of 3-30 pulses over 1-2 s
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Clicks often start about 300m from surface, but no experimental evidence from captivity
– ICI decreases as distance to bottom decreases supports ability to use for navigation
– May be able to use echolocation to detect prey, but it isn’t clear
– Clicks are lower frequency and less directional than those of dolphins but may be more directional
than previously thought
May be used in individual identification
Some codas shared by groups, so other functions likely as well
– Group codas persist over years
Echolocation Abilities
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Actual frequencies used can be constantly adjusted to avoid background noise
Captive dolphins can discriminate diameter ratios of 1:1.25 for metal targets the same size, shape
Target discrimination for Tursiops good up to 100m; sperm whales probably further
Likely means odontocetes can easily discriminate prey species
The big bang hypothesis
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Norris and Mohl (1983) suggested that odontocetes could stun prey with sound
Currently no experimental support for hypothesis but unlikely
– Total energy low
– Disorientation of fish in schools more likely due to reduced oxygen level
– Why chase a fish if you can just stun it?
Information parasites
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Experiments in captivity suggest that bottlenose dolphins can gather information from the echolocation
clicks made by other individuals raising the possibility of echolocation parasitism in the wild which in
known from bats
Do mysticetes use low frequency sounds to echolocate?
Numerous authors have suggested that whales may be able to use low frequency sounds and echoes to
navigate
Reasonable evidence that bowhead whales could use low frequency calls to detect deep ice during
migration
Calls by blue whales and gray whales unclear function
Would represent 6th independent evolution of echolocation
Do pinnipeds echolocate?
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Papers in the 60s and 70s claimed that pinnipeds could echolocate
•
Recent work (including some by our Vice President) has pointed out the methods were seriously flawed
and there is no current evidence in support
– Clicks have been recorded from some phocids
Communication
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Sharing of information from any source
•
Ritualized displays may evolve if the sender benefits from signaling a receiver
– May be deliberate or incidental
– May involve signals other than sound
– Coloration, posture, etc
– Harp seals slapping the water when alarmed
– Male hooded seals inflating nose sack
Ritualized displays may come from simple sounds
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Walrus show high degree of similarity in rutting vocalizations among individuals and years
Communication
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Cues may be used by receivers, but unlike displays, they do not necessarily benefit the sender
•
Receivers may benefit greatly by being able to assess condition, size, or location of sender
– Sounds related to movement through environment, feeding sounds
– e.g. body size of potential rival
Cue-display continuum
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Specialized displays and inadvertent cues form the ends of a continuum of animal communication
– Sometimes it is difficult to determine whether a signal is a cue or a display
– Displays often evolve from cues, and evolution can occur rapidly so transitional states may be found
– Elephant seals moving over the ground
Some obvious marine mammal displays
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Observers often notice what appear to be visual displays in cetaceans
•
In many cases, these probably send mostly acoustic signals
– Breaching, lobtailing, flipper slapping, bubble blowing
– Sound levels of breaches higher than vocalizations and may be heard kilometers away
Vocal communication
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Different sounds and calls must be described and linked with behaviors to gain functional understanding
– How many types of vocalization are there?
– What is their function/meaning?
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Quantitative analyses are critical for understanding function of sounds
– Too much work has been anecdotal
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Even determining number of calls from acoustic structure can be difficult and is highly dependant on
resolution of study
– When is a call different???
Quantifying calls
–
Multivariate methods including cluster analysis may help to distinguish number of calls
– Depends on acoustic variable included in analysis so results still somewhat subjective
– Presence, number, or distribution of harmonic structures
– Frequency or amplitude modulation
– Presence of broadband noise
– Biphonation or subharmonics
– Vocalization rate
–
Call are often composed of subunits, but when is it a subunit and when is it a new call?
Call function
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Also difficult to determine call function
– Behavioral observations can be difficult
– Meaning of a single call may have context-dependant (multiple functions)
Dolphin pulsed social sounds
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Bottlenose dolphins engaged in intense social behavior emit a great diversity of sounds including
whistles and many pulsed sounds often described as buzzes, brays, barks, screams and squeals
Functions of sounds difficult to tell but many appear to be aggressive sounds
Dolphin social sounds
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Male Tursiops aduncus in Shark Bay, Western Australia emit a “pop” vocalization when consorting
females (more of this later in the semester)
Vocalization can be heard in air and underwater
Appears to be a threat meant to induce the female to approach
Dolphin whistles
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Whistles are narrow band frequency modulated calls that often have harmonics
– Frequency between 7-15kHz
– Usually less than 1 sec
•
Once thought to form a language where each whistle corresponded to a word, but this is not the case
Signature whistles
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One function of whistles is individual identification
•
Harmonics and variations on theme possible
– Stereotyped features may include individual identity and variable features may convey other
information
•
Used by mothers and calves during separations and as contact calls for groups that are spread out
In bottlenose dolphins, each individual produces an individual whistle that can be identified by its
sonogram and is stable over years
Whistles
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Mimicry of whistles is well documented in Tursiops
– Captive individuals mimic each other
– Young dolphins may mimic sounds in environment like a trainer’s whistle
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Male T. aduncus in stable alliances will converge on a shared alliance whistle
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Common dolphin whistles do not seem to be individual or context specific
– Functions are still unclear
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Much work needs to be done to determine functions of whistles in the wild beyond work done on
Tursiops
Some whistles appear to be shared among many individuals in certain situations
– Simple whistles of calves
– Whistles in social situations
Killer whale dialects
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Groups of killer whales share calls that are fairly stable over time (last decades) and are considered
dialects
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Each group has a small repertoire of about 10 calls
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No calls are shared by groups of separate clans
Help to make communication within pods more efficient
In British Columbia, some groups share some calls but not others and the groups can be divided into
clans
Suggests pattern of new group formation
Mysticete vocalizations
–
Calls are usually very loud and very low frequency
– Blue whales 15-20 Hz (mostly below human hearing)
– Fin whales 20-30 Hz
–
Function not well known
– Social sounds or long-distance communication
• Blue whales make calls more often when in consortships
– Echolocation of very large features (e.g. islands)
• Wavelength too large to resolve anything else
Humpback whale sounds
•
Use sounds in more obvious ways than other mysticetes
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Small group of whales in SE Alaska make loud sounds used in foraging
– Calls are individually distinctive
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Most famous humpback calls are songs on mating grounds
•
Songs change over time
– Usually during winter breeding
– Changes in frequency
– Changes in duration of units
– Deletion and insertion of phrases or themes
– Sequence and composition of themes
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All whales change the song at the same time –actively learn changes
All whales on breeding ground share the same song, but differ among breeding areas
Songs are long (10-15 min) and complex
– Include repeated themes, phrases, subphrases
– Subphrases are generally a few seconds and <1.5kHz
Songs are a male display – only males sing
May function like songs of male birds
– Communicate sex, location readiness to mate
– May mark underwater territory
– May be honest signal of male size and stamina (quality)
– Innovation may be attractive to females
Pinniped underwater vocalizations
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Most vocalizations appear to be related to mating and social interactions
•
Leopard seals (more solitary) have less aggressive vocalizations and appear to advertise location and
readiness to mate
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Harbor seal vocalizations may function in male-male competition and display to females
•
Many pinnipeds have individually identifiable vocalizations stable over years
•
Occur within range of human hearing
– Grunts, snorts, barks
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Multiple functions
– Threat calls and display calls of males
– Pup attraction calls
– Identification calls of pups
•
Most produced in larynx but also clacking of teeth
– Male walrus strike inflated throat pouches to produce gong-like sounds
– Hood of hooded seal produces sound
•
Air-borne sound production varies with age, sex, and season
– Female harbor seals vocalize when they have pups
– Almost continuous barking at otariid haul outs
Weddell seals use vocalizations in territorial defense: use chirps, trills, buzzes
Bearded seals have complex underwater songs that may also be produced by females
– Male songs may change progressively
Male walrus produce a variety of knocking sounds in air and underwater both in and outside the
breeding season
Air-borne sounds: Pinnipeds
•
Two main uses
– Breeding males (threats and strutting)
– Mom/pup recognition
• Stay in contact in crowded conditions (many phocids)
• Find each other after a foraging trip (otariids)
Air-borne sounds
•
Polar bears only produce airborne sounds, but complexity low relative to other terrestrial mammals
•
Sea otters may produce mother/pup recognition calls that travel almost 1 km
– Grunts may function in mother/cub recognition
– Graded signals that may function in individual recognition
Sirenian vocalizations
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Manatees (2-8 kHz) and dugongs (3-18 kHz) produce chirps and squeaks
Some manatee vocalizations may function in keeping mothers and calves together
Dugong vocalizations appear to be used by males for advertisement to females and possibly to advertise
their location to other males on mating territories
Vocal learning
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Both pinnipeds and odontocetes appear to learn vocalizations
– Often imitate man-made sounds
– One harbor seal started imitating words with a Maine accent!
– Humpback songs
Noise and cetacean conservation
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Loud sounds can cause harm
– Naval exercises, ATOC, mining
– Beaked whale eardrums
Acoustic masking
The impacts of sound may vary with depth and be channeled
The SOFAR channel (SOund Fixing and Ranging)
– Speed of sound in influenced by water temperature
– Speed of sound in influenced by pressure
–When considered together they create a complex relationship between water depth and sound speed
– Sounds bounce off layers moving at different speeds, causing a channel where loud sounds can
travel great distances
– Expected to influence deep-diving species the most
Adaptations: Diving Physiology
Diving
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A prominent feature of marine mammal life
– Foraging
– Traveling
– Reproduction
– Social Behavior
Diving abilities of marine mammals vary greatly
Spending large amounts of time underwater involves changes in how oxygen is delivered, stored and
used by the body
Anatomical structures intended for use on land must accommodate needs of a diving animal
Oxygen Pathways
–
Components of terrestrial and marine mammal oxygen delivery systems are similar, but function of
individual components varies
–
Fixed Open System
– Terrestrial animals and marine mammals at the surface
– Oxygen constantly available
– Air → Lungs (alveoli) → Capillaries → Skeletal Muscles → Mitochondria
•
Closed system
– Marine mammals underwater
– Must perform multiple roles
– Respiratory and cardiovascular systems are relatively less important than open system while cellular
level is more important
Aerobic and Anaerobic Respiration
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Lack of oxygen during submergence leads to worsening physiological conditions
Aerobic respiration involves activity that does not result in the build-up of lactate in the blood
Anaerobic respiration occurs once oxygen runs out resulting in . . .
As oxygen runs out . . .
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CO2 and lactic acid buildup
Blood serum and cell fluid becomes more acidic
Organs like the brain and heart cannot survive long periods of hypoxia
Other organs and skeletal muscle can function during anaerobic conditions or be starved of oxygen
when it runs out
As pressure builds . . .
For every 10m of water depth, there is an additional atmosphere (atm) of pressure
Squeezes air-filled spaces
– may collapse or distort
Pressure and air can be trouble
– Oxygen toxic at high concentration
– Nitrogen can cause sleepiness (narcosis)
– Air bubbles in tissues and blood can cause problems as they expand on ascent
Respiratory system
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Many taxa show re-arrangement of the position of nares to allow easy access to the surface
•
Formed from a number of sources
– Water collected on blowhole
– Condensed vapor
– Fine oil droplets from cells lining sinuses
– Mucus from tracheal glands
– Surfacants: lipoproteins from lung that facilitate easy inflation
•
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Size, shape and direction can allow identification of whales
•
Pinnipeds
– No valve on nares; two throat cartilages and powerful larynx muscles keep water out of trachea
– Male elephant seals and hooded seals have some serious modifications!
Cetaceans
– Blowhole (nares) migrated to high on head except sperm whale – anterior to head
– Nasal passage closed by nasal plugs that open through muscle contraction, then close passively
(connective tissue)
A cetacean’s blow
Sirenians
– Manatees: two-valve nostrils at tip of rostrum
– Dugongs nostrils are closer together and allow less of the body to be brought out of water
– Nostrils closed by anteriorally-hinged valves
A diver’s lung
–
Volume is dictated by body size, not lifestyle
– Some exceptions above and below the norm
– Sea otters may use for O2 or buoyancy
– Volume probably not terribly important for most taxa; cetaceans dive with full lungs, pinnipeds
usually dive with relatively empty lungs
–
Lungs can also be used for buoyancy
– Sea otters (how much taken in); dugongs (contract muscles to reduce air volume)
•
Most collapse at depth
– Alters buoyancy
– Can’t be used for storing O2
•
•
Very fast and efficient at exchanging air
– Blue whale can vent and refill 1500L of air in under 2s
– Small dolphins can vent and refill in under 0.1s!
– Tursiops and Trichechids renew ~90% of air
– Humans exchange about 10%
Very fast and efficient at removing O2 from air
– Up to 90% removal for Tursiops
– Only about 20% for terrestrial mammals
Collapsing lungs
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–
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In cetacens bronchi, trachea, and alveoli all collapse
Collapse starts at alveoli then larger airways
Complete collapse of lungs by:
– 25-50m in Weddell seals
– 70m Tursiops
– Probably 50-100m in most marine mammals
–
Deep divers have cartilaginous reinforcement of airways to protect them from pressure
Benefit of collapsing lungs
•
•
Don’t need rigid structures to withstand pressure
Collapsing lung avoids buildup of Nitrogen
– Air in lungs is moved to upper airways by collapse so it doesn’t contact blood (N doesn’t enter
blood)
– Avoids nitrogen narcosis and decompression sickness (bends)
Oxygen Stores
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Despite closed O2 system during high activity, most marine mammals stay aerobic
Diving limitations set by the ability to balance oxygen conservation and use while submerged
Can be stored in lungs, blood (hemoglobin), muscles (myoglobin)
– Hemoglobin is found in red blood cells
Stores of marine mammals 2-3x terrestrial
Primary storage in skeletal muscles blood (87% in deep divers)
Myoglobin is the primary O2 carrier in mammals
– 3-7 x higher myoglobin level in marine mammals
• Terrestrial mammals: 1.0 g myoglobin/ 100 g wet muscle
• Sea otters, otariids ~3 g
• Phocids 4-5 g
• Odontocetes 2g (bottlenose dolphin) - 8g (n right whale dolphin)
• Mysticetes 0.9 g (sei) – 3.5 g (bowhead)
– In pinnipeds, more myoglobin associated with longer dives; no clear relationship in cetaceans
Enhancing Oxygen Storage
•
•
Increase blood volume
– 2-3 times higher in diving mammals than nondiving
– Stored in retia mirabilia or enlarged blood vessels
– For example (Ridgway and Johnson 1966)
• Best diver (Dall’s porpoise): 143 ml/kg mass
• Intermediate (Pac. White-sided dolphin): 108 ml/kg
• Worst (Bottlenose dolphin): 71 ml/kg
Increase hemoglobin concentration
– Important component of oxygen-carrying capacity
– Higher hemoglobin levels are associated with greater diving ability
– Shallow divers: 14-17 g / 100ml blood
– Deeper divers: 21-25 g / 100 ml blood
•
Increase # circulating red blood cells, RBC
– Haematocrit – volume of RBC/blood volume
– Phocid seals use this throughout the course of a dive
•
Weddell seals: hematocrit rises as dive progresses then drops at surfacing
– Amount of increase depends on dive duration
– Large spleen of Weddell seals serves as large blood reservoir: contracts during dives, injects RBC
leading to 60% increase in [hemoglogin]
•
Phocids have oxygen reserves 21-79% higher than dolphins
Breath holding = dive time
–
The key to effective diving
– Allows longer dives leading to less energy wasted and more chance to find prey/engage in
subsurface behaviors
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Not well correlated to body size of families
Phocids generally best (better than most cetaceans)
Within taxa (e.g. phocids) body size effects dive time
Maximum Dive Times
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Phocids
– 11 min Crabeater seal (250 kg)
– 120 min southern elephant seal (600 kg)
Otariids: 6-16 min
Walrus: 13 min
Manatee: 16 min
Odontocetes: 2-138 min
Mysticetes: 15-50 min
Why aren’t all species supreme breath holders?
•
Good question . . .
•
A trade-off within pinnipeds
– Surely involves trade-offs
– Phocids have longer dive times and physiology geared for energy conservation but they are slow
– Otariids are swift predators but they are not particularly good divers
Divers and Surfacers
•
The differences in diving abilities led Ian Boyd (1997) to suggest there are two major types of
underwater foragers
– “Divers” with most of the time spent at the surface with short dives
– “Surfacers” spend most time underwater and come to the surface for short periods
– Elephant seals dive continuously at sea for traveling and resting (take advantage of reduced
metabolic rate while diving)
Aerobic Dive Limits
– Aerobic Dive Limit (ADL) – maximum dive time before anaerobic metabolism starts
– Kooyman (1985): longest dive that an animal can make without increase in blood lactate
–
–
concentration during the dive
Diving within ADL means an animal can dive again as soon as oxygen stores are replenished
Diving above the ADL leads to increased recovery time as lactate is metabolized
ADL and Marine Mammals
•
Most dives are well within the ADL
•
•
– Weddell seals ~85% within calculated ADL
ADL is positively related to body size
Costs of going over ADL depend on duration of dive
– Seals may sleep for hours if the go way over the ADL (e.g. 60 min + dives for 20 min ADL)
•
Early work found that marine mammals dove much longer than their ADL as predicted by traditional
understanding of mammal breath-holding
•
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Research showed that long dive times were actually within ADL
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Breath holding (apnea)
Why the mismatch between predicted and actual ADL?
– Ability to modify physiology to use O2 efficiently
Diving response: how to maximize your ADL
•
Bradycardia: decrease in heart rate
Peripheral vasoconstriction (blood distribution changes)
Lungs may collapse at depth
Change in O2 delivery to skeletal muscle
Open system → closed system → open
Response levels depend on:
•
Degree of aquatic specialization
– “Mammalian Dive Reflex” is not a reflex of all mammals, response a better word as bradycardia is
under voluntary control!
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Dive duration
Behavior and type of dive
Voluntary vs forced dives
– Most extreme responses when dives are forced
Bradycardia: decreased heart rate
•
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Rapid response at onset of dive
– Anticipates diving
Trachycardia (heart rate increase) occurs on surfacing
– Anticipates surfacing
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Bradycardia increases with stress of dive
– HR during forced dives may be 2-10x slower than natural ones
•
Longer dives results in slower heart rate
– Elephant seals drop from 112 bpm (surface) to 20-50 bpm (10-17 min dive)
– Gray seals may drop from 119bpm to 4bpm on dives over 15 minutes!
– Tursiops ~105 bpm to ~35 bmp on 1-4 min dive
– Amazonian manatee 50 bpm to only 30-40 bpm typically when startlesd to 5-6 bpm
Peripheral vasoconstriction: blood redistribution
–
Dive times can be increased if oxygenated blood is delivered to places that cannot handle hypoxic
conditions by reducing flow to places that can
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Weddell seals
– Blood is restricted to all areas of the body except the brain
– Kidneys and liver still maintain reasonable flow, but during long dives kidney function is reduced
– Flow to skeletal muscles is generally maintained except during involuntary or extremely long dives
• Helps maintain exercise underwater
• If blood to restricted, buildup of lactic acid and prolonged recovery times
–
Boyd (2000) found that blood flow to the skin is highly variable during dives by Arctopechalus gazella
ADL and the dive response
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ADL may not be fixed for each species and may vary within an individual!
•
N. elephant seals adjust heart rate throughout a dive and may represent change in metabolic rate through
dive
– Would change oxygen demand
Evidence for metabolic rate adjustment
– Postmolt S. elephant seal females exceeded calculated ADL in 44% of dives but showed no
extended surface times
– Gray seals did not show extended surface intervals after unusually long dives
– 92% of N. fur seal dives exceeded calculated ADL, too high to really be using anaerobic respiration
– Lab studies of elephant seals
The exercise paradox
•
Heart rate usually increases with activity rate, but in marine mammals heart rates are slowing when
activity increases
•
Dive time, not exertion, determines heart rate and breathing
•
Why the difference between marine mammals and others?
•
•
– Not true of semi-aquatic hippos and birds
Underwater exercisers
In marine mammals, higher physiological rates occur during surface intervals, not underwater even if
they are resting after a dive rather than during exercise
High physiological rates on surfacing increase oxygen loading and reduce surface interval
Exercising with low oxygen
•
Several adaptation for skeletal muscles to work under hypoxia
•
These are also adaptations for endurance
– high myoglobin levels (more oxygen storage)
– elevated mitochondrial density (more energy production)
– enhanced aerobic enzyme capacities in swimming muscles
Studies of diving in the wild
•
Time-depth recorders (TDRs) have given us amazing insights into the dive times and depth of marine
mammals
•
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Attachment methods vary
Animal-borne video and data recorders add even more information
– Stroke rates, behavior, etc
Predators and Predation Risk
Predators and Predation
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Predation is the consumption of another organism, killing it in the process
•
Predation and the risk of predation can be critical in shaping behavior, population dynamics, community
structure, and evolution
•
Few marine mammals are not subject to predation risk at some point in their lives
Some animals make a living by gouging mouthfuls of flesh from other animals
– “Ectoparasites”
Predators of Sirenians
–
Relatively few predators for most populations but killer whales, large sharks, large crocodiles and
jaguars are reported predators
–
Predation risk appears to be very low on manatees
– Large body size, freshwater habitats
–
Dugongs appear to be more susceptible
– Risk varies with location
– Many tiger sharks have dugong remains in their stomachs in Shark Bay, Australia
–
Sirenians are not defenseless
– Thick skin, roundness, surprisingly fast, maneuverability
Predators of Sea Otters
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–
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Sharks, killer whales, birds, terrestrial carnivores
•
White sharks
– May account for 8-15% of mortality in CA
– Otters may rarely be eaten after being killed but data are scarce (few stomach contents)
– Other sharks rarely are predators but possibly sevengill sharks
•
Killer whales
– Not preferred prey of whales
– Documented attacks have increased but data aren’t great
– Unclear what the success rate of attacks really is
•
Almost all species are at risk at some stage of life except possibly some freshwater species
Coyotes take young sea otters in CA and brown bears take hauled out otters in Russia
Bald eagles in AK take pups off water
– 28% of prey remains @ nests are otters in some locations
– Young otters can’t dive easily to escape (too buoyant)
– Individual eagles may be otter specialists
Predators of Pinnipeds
Terrestrial Predation
•
Common in polar and subpolar northern hemisphere but not in southern hemisphere polar regions
•
In north pinnipeds flee to the water but in the south they flee to land
– Polar bears, Arctic foxes
Terrestrial predation on pups
–
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Golden jackals taken Mediterranean monk seal pups
In Lake Baikal and Caspian Sea wolves and eagles taken pups and sometimes adult seals
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Freshwater populations of ringed seals: pups taken by red foxes, ravens, wolves, dogs, wolverines
16% of harbor seal pup mortality in Puget Sound from coyotes
Mountain lions, bears take northern elephant seal pups in California
Mountain lions take southern sea lion pups
South African fur seals killed by brown hyenas and black-backed jackals
Terrestrial predators of ringed seals
Foxes enter ~15% of birth lairs in Beaufort Sea
Predation rate by foxes ~26%, but may be up to 58% in some years
Also attacked by red foxes, wolverines, wolves, dogs, several birds, and polar bears
Terrestrial predation and breeding
•
Terrestrial predation generally thought to limit many pinnipeds’ ability to breed in mainland sites
•
However, recent data suggest that this may be overrated as a limiting factor other than human predation
– Northern fur seals
– Pinnipeds can be seriously dangerous to terrestrial predators
Terrestrial predation and haul out selection
•
Harbor seals off the coast of Vancouver Island (Nordstrom 2002)
– What were the effects of
– Distance to foraging water depths
– Distance to mainland
– Addition of a bear model and tire model
– How were these results interpreted?
– What do you think?
Polar bear predation on pinnipeds
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Pinnipeds are primary prey throughout range
•
Also take bearded, harp, hooded seals, walrus
– Stampede walrus which often leads to injuries
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In some areas, pinnipeds are most important predators
Predation on pups is heaviest
Use many tactics: sit and wait, stalking, pursuit
Pinnipeds usually detect stalking bears but often caught by bears at breathing holes
Ringed seals most commonly taken
– In AK, mostly older seals (>6 yo)
– In Canada 1-2 yo most common
– Concentrate on pups in lairs when available
Pinniped predation on pinnipeds
Leopard seal and walrus most common
Male sea lions sometimes specialize on predation on pinnipeds
– Young male Steller sea lions attack harbor seals and Northern fur seals (4-8% of pup mortality at St.
George Island, AK)
– Male southern sea lions kill up to 10% of South American fur seal pups in Peru during breeding
season
– Single New Zealand sea lion responsible for 43% of fur seal pup mortality at Macquarie Island in
one year!
Walrus predation on pinnipeds
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•
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Kill bearded, ringed, spotted, harp seals and young walrus
•
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Usually kill young seals, but sometimes adults
Usually adult and subadult males, but sometimes females
Some individuals are regular predators
– Have massive chest and shoulder muscles
– Tusks stained amber from diet
Impale other pinnipeds on tusks
Selectively consume hide and blubber
Leopard seal predation on pinnipeds
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•
Use of pinnipeds varies spatially
Take variety of species, but young crabeater most commonly attacked
– 78% of 85 crabeater seals had scars in one study
– May be more important prey then penguins and krill in some locations
Shark predators of pinnipeds
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Most important commonly in tropics and temperate waters
All species but those in freshwater at some risk
Probably influence many aspects of pinniped biology
– Tiger shark attacks on Galapagos fur seals may be reason for 3 year period of maternal investment
White shark predation on pinnipeds
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Pinniped specialists in some areas
Generally cold-water areas (cool temperate)
Many species recorded in diet
– Elephant seals, Steller sea lion, harbor seal, gray seal, CA sea lion, fur seals and sea lions of
Southern Africa, Australia, New Zealand, South America, Galapagos
– Can kill elephant seals up to 2200 kg, 3.5m
•
Best-studied in California
– Usually attack at or near the surface within several km of shore
– Ambush from below and behind
– Hold onto elephant seals after capture but release sea lions to bleed
– Females that survive usually lose current pup and fail to copulate (e. seals and sea lions)
– Decisions how to leave and return to haul out sites driven largely by risk of predation from white
sharks
•
More studies starting in South Africa
– Sharks appear to focus on foraging where young seals are concentrated
–
Tiger shark, Galeocerdo cuvier
– More tropical, take Hawaiian monk seals
–
Galapagos shark, Carcharhinus galapagensis
Other shark predators of pinnipeds
– Tropical, take Hawaiian monk seal juveniles and weaners
– Possible cause of population decline at FFS
–
Sevengill shark, Notorynchus cepidianus
– Observed hunting South African fur seals
– Will hunt even adult males in groups
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Greenland shark, Somniosus microcephalus
– Have high proportion of pinnipeds in stomachs
– Possibly scavenging, but ma also hunt below holes or lairs
– Take harbor seals, young gray seals off of Sable Island, Canada
• May be increasing in numbers
–
Sixgill shark, Hexanchus griseus
– May take pinnipeds at depth
– Pinniped remains very common in sharks off of South Africa
–
Sleeper shark, Somniosus pacificus
– Appear to be major predators of harbor seals in AK
Sharks and Pinnipeds
•
Sable Island, North Atlantic
– Shark numbers appear to have increased with changes in water temperature
– Gray seal populations have exploded
– Harbor seals virtually extinct on island
– At least 50% of decline may be due to sharks
•
Sharks responsible for much of the mortality of juvenile monk seals on French Frigate Shoals
•
•
Only taken by mammal eating form, 14-24 pinniped sp
•
•
Most common in polar to cold temperate areas
Killer whale predation on pinnipeds
Some populations rely heavily on pinnipeds
– 62% of diet in BC and WA is harbor seals
Attack at many locations
– Offshore, near haulouts, on beach (pups most commonly attacked and taken)
Predation on Cetaceans
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River dolphins and killer whales are probably the only species with minimal risk
Mammal-eating killer whales may be a risk for fish eating forms
Bull sharks may attack river dolphins
Predators include cetaceans, sharks, and humans
“Blackfish” predation on cetaceans
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False and pygmy killer whales, short-finned pilot whales
•
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PKW attacks all of dolphins in ETP fishery
FKW attack small pelagic dolphins
– May go after humpback and sperm whales
– Observations of most attacks on dolphins released from ETP tuna nets
SFPW rarely take cetaceans
– Occasionally harass dolphins during fishing operations
– Seen harassing sperm whales and were treated as a threat
Shark predation on cetaceans
•
•
Risk mostly to smaller species but white sharks can kill mysticete calves
•
Classify whether sharks are predators based on
– Frequency of occurrence in stomach contents
– Flukes and vertebrae method
– Direct observations of predation events
– Scars on living animals
– Sometimes difficult to classify
Shark predation on cetaceans: Regular predators
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White sharks, Carcharodon carcharius
– Large individuals shift to largely MM diet including cetaceans
– Major predator of harbor porpoises along N. American coasts
– Off Natal, SA dolphins may be the major MM prey item
– 44% of white shark stomachs off South Australia contained bottlenose dolphin remains
– May take humpback calves
– Most common in cold temperate waters, but risk may occur in warmer areas (e.g. Moreton Bay,
Australia)
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Bull sharks, Carcharhinus leucas
– Occur in warm coastal waters including river mouths and even 100s-1000s of km inland
– One of few sharks that attack prey bigger than their own body size
– Dolphins found in stomachs of bull sharks in South Africa more often than in any other shark
species in the area (tiger, white, dusky)
– Often scavenge whale carcasses
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Tiger shark, Galeocerdo cuvier
– Generally warm waters but reach higher latitudes in summer
– Large sharks bigger risk to cetaceans
– Well adapted to taking large prey (terminal mouth, curved and serrated teeth, broad jaw)
– Dolphins observed being killed or in stomachs in Hawaii, Western Australia, Florida, and South
Africa (1.9% had flukes and vertebrae)
Considerable variation in risk from sharks and likelihood of attack success
– More likely to kill small species
– Risk to cetaceans tends to be higher further offshore and in warmer waters
•
Sixgill shark, Hexanchus griseus
•
Sevengill shark, Notorynchus cepidianus
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Dusky shark, Carcharhinus obscurus
– Deep-water sharks that reach lengths >5m
– Dominant predators of continental slope
– Dolphins occurred in 18.2% of sharks >2m off South Africa
– Take other swift prey like fur seals and swordfish
– Cool temperate waters, prefer turbid habitats
– 12.5% of sharks from the Eastern Cape of South Africa contained dolphins
– High degree of geographic variation in diet
– 17% of stomachs in South America had franciscana (Pontoporia blainvillei) remains
Shark predation on cetaceans: Occassional predators
– Known to attack living dolphins
– 0.2% (1 of 50) sharks had flukes or vertebrae in stomach in South Africa
– Other studies shown no marine mammal remains
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Oceanic whitetip shark, Carcharhinus longimanus
– Common scavengers of whale carcasses
– May take calves straying too far from dolphin schools in pelagic waters
– Have been seen killing dolphins in purse seines
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Greenland shark, Somniosus microcephalus
– Arctic shark
– Scavenge beluga and narwhal in nets and harbor porpoises found in stomach contents
•
Pacific sleeper shark, Somniosus pacificus
– Arctic and cold-water distribution (or very deep)
– Southern right whale dolphin found inside one that probably wasn’t scavenged
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Mako shark, Isurus oxyrinchus
– Remains rare in stomachs but bites found on live-stranded animal (was highly parasitized)
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Almost nothing known about consequences of predation
Shark predation on cetaceans: Suspected predators
Shark predation pressure on odontocete populations
Intensity of predation often estimated using frequency of population with scars (relationship between
successful and unsuccessful attacks)
– Differences in death rate vary with size and species of shark attacking, body size of attacked
odontocete, and habitat (e.g. pelagic vs coastal)
Scars on odontocetes
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Few in pelagic waters compared to coastal areas
•
Most known from Tursiops
•
Humpback dolphins in South Africa
•
Sex-differences in scar frequencies have been noted with males seeming to take more risks than females
– Probably because of high probability of death if attacked in pelagic waters
– T. aduncus
– 36.6% in Moreton Bay (tiger and white)
– >74% in Shark Bay (tiger) some individuals with >9 attacks
– South Africa 10-19% scars, estimated 2.2% of population taken every year
– T. truncatus
– No scars in Adriatic
– 31% in Sarasota Bay, FL
– Higher wound rate than T. aduncus at 28%
Tiger shark attacks on T. aduncus in Shark Bay
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Very large population of tiger sharks
How were wound frequencies and attack rates calculated?
Were all sex classes attacked equally?
Did shark size matter?
•
What data would you like to gather to complete the picture?
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Hunt and kill belugas and narwhals
Polar bear predation on cetaceans
Attempt to catch from ice edge (younger cetaceans), but most common at iceholes
Also take belugas that move into extremely shallow water and partially strand
Even try to swim after belugas or narwhals but very low probability of success
Often kill more than they need to eat
Killer whale predation on cetaceans
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No cetaceans within range are safe
–
Often kill much more than needed to consume or don’t consume whole carcasses
– Have been recorded killing or fatally wounding entire sperm whale groups
– Eat only tongue/lips of gray whales
– Often eat only blubber
– Very different from terrestrial predators that tend to eat everything
–
Attacks on large whales usually target smaller individuals
– Drive/exhaust them before drowning
– Separate calves from mothers, but calves do occasionally escape
Social foraging allows them to take even blue whales with dozens of individuals involved in attack
Can’t be outrun – not even Dall’s porpoise
Kill through drowning, ramming, smashing, biting
Geographic variation in diet
– 50% Dall’s porpoise in AK, rarely eat porpoise in BC
Antipredator tactics
•
Can be divided into tactics that reduce probability of encounter with a predator or increase the
probability of detection and responses to a predator encounter or attack
•
•
While sea otters seem primarily to use the former, most species under threat use both tactics
•
Dolphins have been shown to readily discriminate sharks that are potential predators from those that are
not a risk
Avoiding attack
Hide from predators
– Birth lairs of ringed seals, up to 1.5m deep, and Baikal seals offer protection
– Each mother may have many lairs, so not all are occupied at any one time
– May allow for longer lactation period than is possible when breeding on the ice exposed to
predators (but confounded by being fast ice rather than pack ice breeders)
Group Formation
•
Predation hypothesized as factor leading to evolution of group living in odontocetes
– Group sizes are much larger in open ocean habitats than nearshore
– In many species, group size may change with activity (fission-fusion societies)
•
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Harbor seals show vigilance reduction as group size increases
Mixed-species odontocete groups found in both coastal and pelagic areas may serve to reduce predation
risk
– Why not form larger groups of conspecifics?
Change activity patterns
•
Very few Galapagos fur seals forage at night when there is a full moon
– Similar to bats facing owl predation?
•
Hawaiian spinner dolphins enter sand-bottom bays and form large, compact groups to rest during the
day (increased visual detection)
•
Tursiops aduncus in Shark Bay form larger groups and move to deeper waters where there are fewer
tiger sharks when they rest
Leaving and arriving at a haul out
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Particularly dangerous time for pinnipeds
Appear to modify their swimming behavior in response to risk
– Wait outside the danger zone then swim in fast along the bottom to avoid being seen at the surface
or porpoise rapidly through this area in groups
– Similar behaviors seen in elephant seals, CA sea lions, Cape fur seals
Once a predator is detected
•
Flight
– Pinnipeds faced with terrestrial predators flee into water while those threatened from water flee to
land
– Most odontocetes that encounter predators flee at high speed even when there is no attack
– Gray whales deviate paths when they are presented with recording of killer whale sounds
•
Mobbing and predator inspection
•
Concealment and Confusion
– Rare in pinnipeds
– Cape fur seals will follow white sharks
– Galapagos fur seals seen mobbing sharks
– Several records from cetaceans
– Humpback dolphins chasing white shark
– Common dolphins herding sharks away from rest of school that sheltered near research vessel
– Beluga whales chased a polar bear out of the water
– Pygmy and dwarf sperm whales can expel large clouds of red-brown feces and spread them with
their flukes when they face a threat
•
Active Defense
– Stories of dolphins ramming sharks are overblown, and only recorded defense of calves in small
odontocetes occurs when sharks are not a risk to the adults
•
– Gray whales thrust their flukes at predators attacking their calves
Sperm whale defense
– Attacks by killer whales appear to be relatively common, and can be successful
– Widespread groups of sperm whale tend to coalesce when killer whales are in the vicinity
– Don’t appear to use diving as primary escape tactic
– Form “rosette” or line abreast formations
– Individuals may assist others that are injured or are vulnerable
Cookie-cutter sharks: a special case
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Gouge mouthfuls of flesh from many pinnipeds and cetaceans, especially deep-diving species
Impact of bites unclear
•
Several other sharks may use this “ectoparasitic” tactic on marine mammals
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Killer whales and bottlenose dolphins have been killed by stingray spines
Stingrays: not predators, but a possible mortality agent
Killer whales in NZ feed on rays and likely get stung fairly often
Tursiops doesn’t feed on rays often, but encounters are common in shallow foraging areas
Marine Mammal Feeding Mechanisms and Diet
Feeding behavior and ecology
•
Shaped at a variety of levels
– Evolutionary: shape feeding apparatus, determine what types of prey are possible
– May involve coevolution with prey and be shaped by forces like competition
– Ecological: determine general feeding locations and prey, includes short-term responses to
competition
•
– Behavioral: selection of specific feeding locations and tactics
Evolution shapes foraging at all levels!
Evolution and Foraging
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All aspects of foraging are shaped by evolution since foraging success influences the probability of
survival, mating access and success and therefore fitness
Trade-offs are a key concept
– Time allocation
– How energy and resources are spent
– Opportunity costs (selection and rejection of prey)
Marine Mammal Foraging
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•
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Marine mammals have evolved to exploit a wide variety of prey from some of the smallest zooplankton
(not phytoplankton or smallest zooplankton) to the largest whales
Many specialized morphologies (within constraints of living in aquatic environment) have evolved to
exploit specific prey
Forage on many different temporal and spatial scales
Marine Mammal Foraging Research
•
For a variety of reasons, we still know relatively little about the foraging behavior and ecology of
marine mammals
•
New technologies in the field and the lab are providing new ways to study marine mammal foraging and
diets
Major ways to feed
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Batch (filter) feeding
•
Scavenging (facultative in marine mammals)
Grazing (herbivory)
Raptorial feeding
– Suction feeding
Why so few feeding modes?
•
Similarities in challenges and biomechanics of capturing prey (and moving through) a dense, viscous
medium lead to convergence and parallel evolution within and among clades
– Have strong musculature to prevent water entering trachea and lungs
– Must accommodate suckling by neonates
Messing with mammalian tooth standards
•
Either greatly exceed or fall far short of typical mammal tooth numbers (42 in either jaw usually max
for mammals)
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Reduced heterodonty (differentiation) and complexity is the rule
Some have incisor or canine tusks
Few marine mammals chew, the mouth is for food acquisition not processing
Batch (filter) feeding
•
•
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Capture of multiple prey items simultaneously
Can limit prey types available (mysticetes especially)
Requires dense aggregations of prey for successful foraging
In general, allows feeding near base of food chain
– Allowed high abundance and wide distributions pre-exploitation
– 10% transfer efficiency
– Most MM filter feeders are ~ TL3
Three types of batch feeding in MM
•
Gulping (ram filter feeding)
– Forward motion used to engulf mouthfuls of water
– Balaenopterids, most pinniped batch feeders
•
Suction filter feeding
– Water drawn into mouth through rapid buccal expansion
– Gray whale
•
Skimming (continuous ram filter feeding)
– Water continuously flows into mouth
– Balaenidae
Baleen
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Keretinaceaous integumentary product
– Not ossified or mineralized
– NOT TEETH
–
–
–
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Suspended from maxillae in laminae or plates
Each side of mouth may have 100-400 triangular plates
50-500cm long
Hypotenuse of plate frayed, “hairs” form fibrous mat
Baleen and prey size
•
Number of plates and fringes (filter porosity) correlated with prey type
–
Continuous filter feeders consume tiny zooplankton; have 250-350 narrow finely fringed plates up
to 4-5m long and may have 35-70 bristles/cm2
– Rorquals and grays have shorter (0.5-1m) wider baleen with coarser fringes
• Sei whale consumes smallest prey has finest baleen
• Prey of balaenids would pass through most rorqual baleen
Skimming (CRFF)
•
Bowhead, right whales, pygmy right whale
– Mouth is like a net with baleen covering entire side of mouth when it is fully open
– Baleen is of primary importance in prey capture – can’t feed without it
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–
–
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Head may be up to ½ body length
Strongly curved jaw
Feed at ~ 5km/hr
Only mysticetes with a large gap between left and right baleen racks
Water flows into cleft, through mouth, over baleen and out of gutter-like structure at rear of lower
lip
Flow draws water in center of mouth outward
Up to 5m long tongue sweeps laterally to deflect water to racks and to sweep food from baleen
Feeding occurs throughout water column including surface midwater and bottom
Gulping (RFF)
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Rorquals are most specialized mysticetes
– Slimmer and faster than balaenids
– Can use gulps and lunges to draw in mouthfuls of prey
– Baleen of secondary importance in prey capture: 1) catch prey in mouth, 2) strain it from the water
– Generally forage alone
– Can forage throughout water column
•
Gulps involve:
– Inward folding of tongue into ventral space
– Massive gular expansion: pouch extends to umbilicus
– Volume increase >600% in blue whales taking in t least 60m3 and 70 tons of water, maybe much
more
The rorqual jaw
•
Jaw unlocks, adductor muscle relaxes, allowing 30-90º opening
– Water rapidly fills mouth because of high swimming speed, but is passively enveloped (smaller
species may use some suction)
– Timing of opening critical – too soon and bow wave pushes prey away
•
•
•
Front of jaw disarticulates
Lower jaw disarticulates
Pouch deflation
– Adductor muscles close jaw
– Elastic rebound helps close jaw and pull pouch in
– Gravity aids in closing and deflation for surface lunges
– Water dumped from back corners of mouth as it is pushed out by piston-like tongue
Batch suction feeding
•
Gray whale often suction feeds on bottom
– Stiff, short, coarse baleen filter fine sediment out and retain mollusks and amphipods
– Most individuals prefer to feed on right side!
• Baleen on this side shorter scratched and worn
– May also skim feed
Prey removal hypotheses
•
Mechanism for removing prey from baleen not well-known
– Scrape with tongue
– May miss a lot of prey
– Shake head to dislodge
– Backwash through baleen to get prey to the middle of the mouth
Filter feeding pinnipeds
–
Crabeater seals consume krill, probably using suction rather than locomotion based RFF
– Cheek teeth with comb-like cusps interlock to trap prey while allowing water out
– Swim with mouth open through dense krill swarms
– Probably suck krill selectively then swallow when they have a mouthful
– Normal meal is 8 kg (each krill is 1 g)
– Worlds most abundant seal (63 million tons krill/yr)
–
–
Leopard seals also filter feed krill
Ringed seals, Antarctic fur seals to a lesser extent
Raptorial suction feeding
•
Ingest and transport prey using negative pressure
– Generated with oral and pharyngeal expansion
– Water expelled before swallowing
– Allows capture of relatively large and rapid prey
– Wide variety of prey taken; most commonly mesopelagic cephalopods, then bivalves and benthic
invertebrates
– Requires substantial modification of skull jaws, and associated skeleton
• Many suction feeders highly derived (walrus and narwhal most highly derived)
– Found in at least 5 odontocete families
–
• Monodontids, phocenids, physterids, delphinids, ziphiids)
None of these taxa are exclusively made up of suction feeders – multiple evolutionary origins!
Dynamics of suction feeding
•
Rapid piston-like retraction of flat tongue
•
Water and prey drawn into mouth
– Creates negative pressure
Suction feeding allows for bizarre morphologies
•
•
•
Sperm whales with distorted jaws survive and apparently feed as well as normal individuals
•
•
Suction-feeding odonotocetes tend to have blunt heads
Beaked whale teeth that limit gape (strap-toothed whale)
Loss of teeth in some taxa
– Narwhal only has the tusk and a gape that would limit grasping prey
– Reduced dentition in walrus and elephant seal
What about sperm whale with very long jaw?
– No oral cavity!
– Prey go straight down throat without being transported through mouth
Evolution of suction feeding
–
Odontocetes with long snouts had to move prey from the jaws to the back of the throat
– Can’t use tongue, can’t use gravity (like crocs)
– Use small amount of suction for prey transport
– Some taxa eventually lose grasping step
Pinniped suction feeders
•
Ross, bearded, cape fur, elephant seals all likely suction feeders
•
Walrus most proficient pinniped sucker
– Powerful suction dislodges prey (soft and hard-bodied) from bottom, but may also squirt water jets
to excavate and stir bottom
– Can use suction for processing: remove siphons and feet of bivalves and clams
• Shells held in lips during suction then discarded
• Can process at least 6 clams/minute and up to 6000 per meal
– Amazing convergence with an extinct cetacean, Odobenocetops, of the S. Hemisphere
Raptorial feeding (grasping)
•
•
Sometimes called raptorial ram feeding
•
•
Seizure of prey with jaws
•
•
Smaller species tend to pursue prey head-on with bursts of speed
•
Often have many slender, pointed teeth
Primitive marine mammal foraging mechanism (except sirenians); similar to terrestrial mammals in
many ways
Specialized forms have elongated jaws (odontocetes)
– River dolphins, some extinct forms extreme cases
Larger species strike with neck swinging
– Sea lions
– Leopard seal carries its neck coiled
Herbivory
•
•
Sirenians only extant MM herbivores
•
Dugongs forage on offshore and intertidal seagrasses
– Dislodge plants (rooting) or crop
– Often form feeding trails when eating rhizomes
•
•
Skull shapes reflect dietary differences
•
•
Manatees eat blades, leaves, and stems of aquatic plants
– Seagrasses, sedges, forbs, herbs, mangrove, water hyacinth
– Prefer submerged plants
Hind gut fermentors (like horses, rabbits)
– Long intestines
– Bacterial microflora to digest cellulose
– Defecation and flatulence almost constant
Sirenian Dentition
– Manatees continuously replace cheek teeth from the rear, fall out from the front
– 5-8 functional teeth at one time
– Few teeth in dugongs, far back in the jaw, grinding plates on palate used in chewing
Oral disks
– Dugongs have down-turned disk for benthic feeding; Lips rotate outwards during feeding which
pushes sediment away from the mouth
– Manatees have bilobed lips for grasping (rotate inwards) plants throughout water column
Prey choice and diet
•
Efficient foraging requires
– Ability to recognize food requirements and where to feed
– Ability to choose best food
– Ability to locate, capture, and ingest food
– Ability to assimilate food
•
All of the above may be influenced by age, sex, experience, reproductive status, competition (inter and
intraspecific), prey characteristics (size, quality, behavior, abundance and distribution, handling time),
predation risk
Diet choice depends on many factors
•
Energy content of prey
– Fish and zooplankton 4-10 kJ/g
– Squid 3-3.5 kJ/g
– Marine mammal blubber – jackpot!
•
Prey digestibility
– Fish protein easier than crustaceans
•
Cost of prey capture
– Energy and time expended in capture and handling
•
Probability of prey capture
– Rapid-swimmers vs slow (or non) swimmers
•
•
•
Prey relative abundance
Body condition of predator
– Predators in good condition or with full guts should be selective for better prey
Needs for specific nutrients
Diet
•
•
•
•
The end result of all the foraging decisions that are made (which we will talk about next lecture) and
anti-predator behavior of prey, but . . . morphology matters!
MacLeod et al. (2006) looked into the influence of morphology on the basic diets of odontocetes
What is most important measure to consider when quantifying the the diet of a species or population?
• Number of individuals that eat a type of prey
• Number of prey items eaten
• Biomass of prey taken
• Some combination of these (Index of Relative Importance
Back up a step – how do you even figure out what marine mammals are eating?
Measuring diet
–
–
Direct observations of prey capture are rare and biased to certain types of prey
Food remains in scats, vomit, or lavage of living animals and stomachs and intestines of dead animals
– Relies heavily on hard parts like squid beaks and otoliths (ear stones)
– The size of these hard parts correlates with size of prey
– Advantages
• Low cost
• Can get information from carcasses in advanced state of decomposition
• Large samples often possible
• Can reconstruct prey size classes
• Can give an idea of prey that are hard for humans to sample
– Disadvantages
• Underrepresent prey that have no hard parts or with hard parts that quickly pass through gut or
digest quickly (otoliths digested more quickly than squid beaks)
• dead animals may not represent feeding habits of healthy animals
• Not always possible to access a “hard part library”
•
Stable Isotope Analysis
– Heavier vs lighter isotopes of carbon, nitrogen, in predators can be traced to their prey in general
– Good at detecting some dietary shifts
– Different tissues look at different time scales
– Carbon can be traced spatially to primary producers while nitrogen can help determine trophic level
• Requires good calibration to system
– Can be used in historical reconstructions
– Drawbacks: high cost, reference libraries of prey signatures and basal species not always available
–
Fatty acid analysis
– Fatty composition of prey is species-specific and is reflected in fatty tissues of predators
– Can reconstruct diets in space and time
– Can look at population differences in diet
– Tissue collection can be non-invasive
– Must sample entire blubber layer or results may be misleading
– Expensive, and need prey library
Trophic level
•
Marine mammals found at almost all trophic levels
– Sirenians TL 2
– Mysticetes ~TL 3
– Other marine mammals generally above TL 3 and many are top predators
– Why are high trophic-level species (killer whales) rare?
Pinniped diet
•
Prey taken varies greatly with general foraging habitat but fish and cephalopods are the most commonly
taken prey
•
Generally thought of as generalists, but are they?
– 100 taxa of crustaceans, cephalopods and teleosts found in ~6500 harp seals
– 40 taxa of fish and invertebrates in grey seals of Eastern Canada
•
However
•
– 80% of grey seal prey biomass are from 2-4 taxa
– 5 of 52 prey species of CA sea lions mage up 80% of prey (% N)
– Crabeater seals and lactating Australian fur seals eat almost exclusively krill, Euphausua superba
– Walrus eat primarily clams
Most pinnipeds show amazing flexibility in prey choice, but will switch among prey items based on
availability and quality
– Harp seals always prefer capelin, only take Arctic cod in nearshore waters
– harbor seals off Scotland feed on most abundant prey but prefer fish 10-16cm
Mysticete diet
•
•
Most species relatively specialized on particular prey, especially those with very fine baleen
Some flexibility
– Gray whales will skim feed during migration
– Fin whales will take krill, fish and cephalopods depending on the location
– Other rorquals will also take krill, fish, and cephalopods in various locations
Odontocete diet
•
•
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Wide variety of prey species taken, but in many cases a small number make up the bulk of prey
Delphinidae
– 45% of species have diets of >75% cephalopods
– 24 % of species have diets of 50-75% cephalopods
– Prefer muscular squid over soft-bodied ones
Phocenidae
– 3 species have >75% cephalopods
– 3 sp 50-75% cephalopods
– Often include economically important species in diet like octopus, cuttlefish, muscular squid,
herring, etc
•
Ziphiidae
– More than half of species eat >50% cephalopods
•
“Sperm whales”
– Primarily squid eaters
•
“River dolphins”
– Primarily fish eaters
•
•
Monodontidae
– Fish, cephalopods, benthic invertebrates
Like pinnipeds, even species that appear to have broad diets, may focus on a small number of prey
species
– T. truncatus in Sarasota FL showed 43 taxa from 76 stomachs, but 70% of diet was pinfish
– Over 160 taxa reported
– Much variation among individuals, with each specializing in 1-3 species of prey
– Prey preferences appear to be life-long and may be maternally inherited suggesting that learning
foraging tactics is important to foraging success
Diet specialization and speciation
•
Throughout most of their range, killer whales can be divided into two forms
– Fish-eaters (“residents” in the Eastern N Pacific)
– Mammal-eaters (“transients”)
–Elasmobranch (shark/ray) eaters in New Zealand
– Genetic, morphological, and behavioral data all can be used to distinguish these forms and
differences could warrant species-distinction
– Dietary differences and different foraging needs likely have led to the reproductive isolation of these
forms and differences in social structure
– Fish-eating killer whales may occur in large groups and use echolocation to hunt
– Mammal-eating whales cannot use echolocation and need to forage in smaller groups to maximize
energy intake rate
– Occurrence of both forms in one group would lead to foraging interference!
Marine Mammal Diets
•
Sea otters
•
Polar bears
•
Sirenians
– Benthic invertebrates (urchins, bivalves, gastropods)
– Some slow-swimming fishes and occasionally birds
– Ice seals, primarily ringed seals with occasional whale or bird
– Marine and aquatic vegetation with the occasional invertebrate (sea squirt or polychete)
Marine mammal diets are flexible
•
Many species will switch prey to more profitable ones or will show strong preferences for profitable
sizes
– CA sea lions prefer 2-4 year old Pacific hake
– Sea otters prefer larger urchins and mussels
– Resident killer whales prefer coho salmon in Alaska but prefer chinook (energy rich but scarce) off
BC
•
Many species will switch prey to more profitable ones or will show strong preferences for profitable
sizes
– Harbor seals in Scotland shift to foraging offshore on clupeids when they are abundant
– Sea otters will switch to smooth lumpsuckers when they move into coastal areas
– Otter %time foraging and foraging bout length decrease
– Average body condition increases
– Juvenile mortality decreases
Foraging Strategies and Tactics
Strategies and Tactics: not the same thing
•
Strategies are genetically based decision rules (or sets of rules) that results in the use of particular tactics
(Gross 1996)
•
Tactics are used to pursue strategies
•
Few strategies show in animals, most are tactics
– fixed or flexible
– may be condition or frequency dependant and vary with environment
Some possible marine mammal foraging strategies
•
Several strategies have been proposed, including
– Maximize overall energy intake rate
– Maximize net energy gain
– Maximize energy intake efficiency (energy gain/energy expenditure)
– Minimize intake variability (adequate mean)
– Maximize mean rate of delivery to offspring
– Costa (1993) proposed that otariids maximize intake rate and phocids maximize efficiency
Steps in a predator-prey interaction
•
Marine mammals can increase the probability of successful foraging at many
stages that generally fall into
– finding prey
– capturing, subduing and consuming prey
•
We will start by focusing on the later
Studying marine mammal foraging behavior
•
•
Limited by access to foraging areas of most species
•
Some major methods include
Recent technological advances have lead to rapid increase in our ability to assess tactics and foraging
success
– Direct observations/focal follows
– Unless study designed properly these tend to be biased towards surface-oriented or spectacular
events
– Time-depth recorders
– Used to infer foraging behavior, but subject to misinterpretations of diving profiles
–Multiple behaviors for the same dive type
–The same behavior for multiple dive types
– Addition of stomach temperature pills has helped to determine foraging success, but still not
fully calibrated
– Animal-borne video and environmental data (AVED) systems
• Have video (or still camera), TDR, 3-D acceleromentry
• Runs 2-9 hours of continuous video that can also be cycled
• Early applications limited by relatively large sizes but shrinking rapidly as battery technology
improves
• Deployed on a variety of marine animals and other species
• Limited by video data analysis, sample sizes (costly, deployment and retrieval difficulties)
– D-tag (WHOI)
•
•
•
•
•
Multi-sensor tag that focuses on sound
Has TDR, 3-D accelerometer
Records sounds on multiple channels
Can hear sounds, record echolocation and returning sounds from echolocation (what
odontocetes “see” with sound)
Can determine individual fluke strokes
Prey capture tactics
•
•
Approaching prey is a critical first step in being a successful predator
1. Pursuit
– speedy marine mammals simply chase down their prey
– otariids tend to use mobile neck to dart out and capture prey once they are close
– seals will chase after shoals of fish, picking off stragglers
1. Pursuit
– Dolphins tend to set up prey to one side and spin in a “pinwheel”to capture the prey
– lateral specialization apparent
– Dolphins pursuing fish at the surface, often chase belly up for improved vision and ability to catch
jumping fish in the air
– Killer whales will chase Dall’s porpoises for hours
2. Stalking and ambush
•
Close approach to prey without being detected often critical for successful predation, especially for
swift-moving prey
•
•
Stalking predators try to closely approach prey without being seen then make a final fast charge
Ambush (lie-in-wait) predators conceal themselves and wait, motionless, for prey to approach close
enough for an attack
Marine Mammal stalking and ambush
•
Polar bears use both
– stalk forward on ice, using chunks for cover
• not very successful
– aquatic stalking of hauled-out pinnipeds
– ambush seals at ice holes
• most energy efficient and most commonly used
•
Leopard seals use both
•
Leopard seals, Stellar sea lions, Sea otters, Weddell seals stalk prey from below often using silhouettes
•
– stalk penguins through ice, then break through
– stalk fur seal pups on beaches from water
– ambush penguins returning to colonies by hiding between ice flows
– take birds, fur seals, penguins, fish in this manner
– may be more common tactic than currently desctribed
Killer whales
– strand feeding would be an example of ambush
• males often swim on their sides close to the beach to conceal fin
–
• dangerous feeding tactic; full stranding possible
• requires learning
• also used by Stellar sea lions, leopard seals
reduce use of echolocation and breathe quietly around harbor seal haul outs
3. Prey herding and manipulation
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•
•
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Manipulation behavior of prey can greatly increase foraging success
–
In coastal areas, dolphins, porpoises, pinnipeds will herd prey against shorelines and barriers to reduce
escape routes
– results in extreme shallow water foraging in some areas
• humpback dolphins in Mozambique and Indian Ocean bottlenose dolphins in Shark Bay
•
Many offshore marine mammals herd prey into dense schools and trap them against the surface
– done individually and in groups that swim around the perimeter of fish schools and below to prevent
escape
– manipulate prey in many ways to keep them together
Take advantage of natural schooling and flight responses of prey
Used to flush prey from hiding, lure prey, increase prey density, tire prey
Common tactic, especially in pelagic areas
Why does it work?
– Rare enemy or still better than being alone
Marine Mammal prey manipulation
•
Splashing, leaping, and tail slaps commonly used around fish schools
– dusky dolphins
•
Blazing involves flashing light-colored portions of the body at prey to scare them
– killer whales flash bellies
– humpback whales flash flippers
•
Not really herding, but humpback whales will “flick-feed” to concentrate euphasids
•
•
Fish show strong aversion to crossing bubble barriers and swim away from bubbles - many marine
mammals take full advantage
– Atlantic spotted dolphins separate individual fish from the school
– Weddell seals use bubbles to flush icefish
– Killer whales flush rays from sediment
– Killer whales concentrate herring and pelagic dolphins use bubbles to concentrate fish schools
Humpback whales most prodigious bubble-users
– many bubble structures deployed during individual and group foraging
• curtains, clouds, nets, columns
• formation depends on prey type
•
Sound can be used to manipulate prey
•
Lures
– “Kerplunking” by 2 bottlenose dolphin species foraging in shallow seagrass areas
– makes loud low-frequency sound that elicits startle response in hiding fish
– Humpback whales in southeast Alaska use feeding calls to startle herring
– not well known in marine mammals, but white coloration near sperm whale jaw may lure squid
Humpback whales of southeast Alaska: masters of prey manipulation
–
Group foraging to capture prey relies on using many anti-predator behaviors of herring against them
– Most individuals dive deep and use bodies to scare herring toward surface
– One individual blows a bubble net to trap herring (they come in but don’t go out)
– Use loud feeding calls to further scare herring to trap them against surface
– Blaze with pectoral fins
– Emit bubble cloud just before lunge
–
–
–
Core community members use this tactic predominantly
Krill feeders sometimes join groups
Preferential associations among fish-eaters, but not relatives
4. Prey debilitation
•
•
Can be energetically cheaper and safer
– Killer whales exhaust then drown mysticetes
– Killer whales and bottlenose dolphins smack fish with their tails to kill or stun them
– Walrus use tusks to stun or kill pinniped prey
– Humpback whale bubble clouds may debilitate euphasids
– Packing fish into dense schools can debilitate them due to greatly lowered oxygen levels
Norris and Mohl (1983) suggested that odontocetes can use sound to debilitate their prey
– most of the evidence they gave could be explained by adaptations for suction feeding or results of
depleted oxygen within fish schools
– why chase a fish if you can zap it?
– interesting but untested hypothesis
5. Tool use
•
•
•
•
“ . . . External employment of an unattached environmental object to alter more efficiently the form,
position, or condition of another object, another organism, or the user itself when the user holds or
carries the tool during or just prior to use and is responsible for the proper and efficient orientation of
the tool (Beck 1990).”
Sea otters are serious tool users
– rocks held on chest and used as anvil for crushing mussels, crabs, urchins, etc
– used as hammer to knock abalone off rocks
– often retained between dives and reused
Bubbles are employed as tools
Killer whales use bow waves to knock seals off ice floes and sea otters off shoals
Tursiops truncatus uses a wave to wash small fish onto mud banks
•
Tursiops aduncus in Shark Bay: tool culture
•
– carry sponges on snouts and use as protection during benthic foraging
– predominantly carried by females within matrilines
– individual variation in types of sponges used and relative use of sponges vs other tactics
6. Benthic foraging: three tactics
•
Collecting
– sea otters collect epibenthic inverts in forepaws
– usually with gather with right paw and carry them under left paw while more prey items are
collected
– Always eat at surface
•
•
Engulfing (gray whales)
Extracting
– sea otters dig for clams with forepaws
– harbor seals dig with foreflippers or snouts
– narwhals, belugas, walrus use water jets to dislodge buried bivalves
– crater feeding in Tursiops truncatus
7. Kleptoparasitism and 8. Ectoparasitism
•
No concrete evidence of ectoparasitism
•
Food stealing only reported in sea otters and polar bears
– killer whales sometimes fit when attacking large whales and not killing them
– pilot whales may harass sperm whales to get them to regurgitate
9. Scavenging
•
•
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Remarkably rare in marine mammals
Important for polar bears
Some pinnipeds may use occasionally
Feeding from fisheries/humans might fit
– dolphins of Monkey Mia
– dolphins feed behind trawlers in Gulf of Mexico and other areas like eastern Australia
– Killer whales and sperm whales take fish from long lines in Alaska (up to complete loss!)
– Pinnipeds happy to steal fish in many areas
Prey Preparation and Consumption
–
–
–
Some prey require extensive handling
–
•
Odontocetes must break large prey apart since they cannot chew
•
Partial consumption of carcasses common tactic to maximize energy intake
– Killer whales may only eat tongue of mysticetes
– Polar bears and walrus prefer hide, blubber, then muscle but all better than internal organs when
eating pinnipeds or narwhal
Sea otters remove heads from birds and strip meat from breast, neck and legs
Sea lions and dolphins discard heads from large fish and may strip flesh from spiny fish
– spines implicated in dolphin deaths
Killer whales often handle mammalian prey extensively after capture
– breach upon and tail slap pinnipeds
– tenderizing or teaching aid?
Group Foraging
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•
•
Extremely common in marine mammals
•
What is cooperative?
– Killer whales reduce echolocation rates as group size increases, but is it information sharing or
avoiding info parasitism?
May represent aggregations and mutual attraction to prey or be highly coordinated and even cooperative
Group foraging may be common because of selection for group formation by factors other than
foraging; may have no choice
Cooperative Foraging
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•
•
•
Often assumed in marine mammal group foraging, but rarely validated
Cooperation: an “outcome that - despite individual costs - is ‘good’ in some appropriate sense for the
members of the group . . . And whose achievement requires collective action” (Mesterson-Gibbons and
Dugatkin 1992).
By-product mutualism
Individual acts selfishly, to benefit itself, but has actions incidentally benefit others
Often mechanism that leads to cooperation, but not all by-product mutualisms are cooperative
– Bowhead whales skim feed in formation
– May aid in whale prey capture by using adjacent whales to trap prey or catch “spillover” from other
whales
– groups appear coordinated (change direction and leadership)
– individuals probably being selfish but benefits others
Three requirements to show cooperation
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•
•
•
•
1. Short-term cost
– having to divide resource
– opportunity costs (restraint from attacking)
2. Energy intake rate must be higher with cooperation than without
3. Collective action required to be successful
Not all individuals necessarily get equal benefit and not all individuals have to cooperate in cooperative
groups
Marine Mammal cooperative foraging
Most anecdotal accounts and don’t provide enough data to satisfy all three criteria
– Dolphins spread out across a large front when foraging and when one subgroup finds fish, all groups
converge
•
•
– How many criteria have been met?
Fish herding in dolphins and pinnipeds
How many criteria have been met?
– Cost: waiting to attack until prey herded to surface
– Energy intake rate higher with collective action?
– Larger dusky dolphin groups feed for longer than small ones, but does this really mean intake
rate is higher? Increased foraging interference? Larger fish schools?
•
•
•
•
– More studies needed
Humpback whale groups?
– Cost: temporary restraint, lost opportunities to be feeding on more abundant krill
– Higher energy intake rates with groups?
• Don’t seem to do well alone on herring, but info on intake rates is taking forever!
– Collective action required?
• Yes: groups that don’t coordinate well don’t do well
Deliberate food sharing provides strong evidence of cooperation
– be careful: could it be kleptoparasitism?
Leopard seals seen foraging in tandem on penguins, sometimes sharing prey
Killer whales are great example
•
– large groups needed to capture large prey
– highly coordinated hunts that may include labor division like lions
– prey are shared among group members
Preen (1995) suggested cultivation grazing in dugongs
– dugong grazing changes seagrass community composition towards more profitable species
– however, for cultivation to occur, the individual that invests in the cultivation must receive the
benefit which is unlikely due to large numbers of dugongs and wide ranging movements
– traplining is more likely explanation with groups rotating to most profitable meadows
Optimal group size
•
•
Why do we see groups of particular size?
•
•
Do any marine mammals hit optimal group size?
Some authors suggest that they are the ones that maximize energy intake rate (optimal group size), but
this is unlikely in most circumstances
– difficult (or not worth it) to exclude joining individuals in most situations so group size should
increase until intake rates of group members are the same as solitary individuals (stable groups size)
– other benefits to grouping also increase likelihood that optimal group size for foraging will not be
seen
Transient killer whales
– may be able to exclude joiners and live in closed family-groups
– don’t form groups for protection
– observed modal group size (n=3) of foraging whales is group size that maximizes energy intake
Marine mammal group foraging
•
Groups may form for reasons other than foraging
– Individuals must forage in groups even if they would do better on their own (e.g. lions)
•
When foraging, groups often split into subgroups and travel in echelon formation
– May improve detection of prey or reduce competition at small patches
Competition
•
Most marine mammals found in groups are subject to intraspecific competition through either
interference or scramble competition
•
There is evidence for interspecific competition
– Competitive release with loss of N fur seals along California?
– Grey seals may be excluding harbor seals from around Sable Island
•
In South African waters, odontocetes show significant dietary overlap with several species of sharks
Variation in foraging strategies and tactics
•
•
•
•
Both strategies and tactics may vary
– among species populations, age/sex classes, individuals
– within individuals
– in response to environmental variation or energetic demands (Bailleul et al. 2005)
Variation occurs at all levels of the foraging process
Most obvious variations are those in response to differences in prey and habitats occupied
Body size has a major influence on strategies and tactics
– Influences oxygen storage and use and therefore dive depth and duration
– Affects foraging options available
– Affects fasting ability and energy storage (mass-specific metabolism decreases with increasing body
size while fat storage increases)
– Affect temporal and spatial scale of foraging and foraging ability during reproduction
Modifying foraging strategies
•
•
When predators are an issue, many species will adopt a strategy that balances risk and energy intake
– µ/G
– Attain minimum energy requirement while maximizing safety
Condition changes the tactics that marine mammals will use in the face of predators
– animals in poor condition will place more value on food than safety compared to those in good
condition or with large stored reproductive assets
– Asset protection principle (Clark 1994)
Tursiops foraging tactics
–
Both T. aduncus and T. truncatus show amazing variation in foraging tactics within and among
individuals
–
In Shark Bay, Western Australia
– Deep water tail-out/peduncle diving
– Belly-up foraging on small near-surface fish
– Shallow water grubbing in seagrass
– Kerplunking
– Sponge carrying
– Tail-whacking
– Extreme shallow water foraging
– Beg from tourists
– Several others
Trade-offs are a major source of tactical variation
•
One common foraging strategy is to maximize lifetime net energy intake
– requires individuals to change tactics based on prey and predators (or disease)
– may cause variation among individuals depending on condition
– those in poor condition are more likely to take risks to gain large rewards
Shark Bay dugongs
Shift more to edges of banks as sharks become more abundant
•
– Closer to safer deep waters
Change foraging tactics as well
– Excavation vs cropping
Trade-offs in polar bears
•
Female polar bears with cubs will select habitats with lower food to avoid adult males that might kill
cubs
Ontogenetic variation in foraging
•
Differences with age may relate to changes in physiological or foraging abilities, differences in learning,
or differences in relative importance of food and survival
•
•
•
Young pinniped foraging constrained by diving abilities, but other variation as well
– make shorter and shallower dives than adults
– elephant seals make transition from short shallow dives to adult-type during first trip to sea
• change related to changes in physiology
Larger yearling Weddell seals dive shallower and forage on benthic prey while smaller yearlings dive
deeper to forage on energy-rich prey
– likely differences in strategy being pursued
Young T. aduncus need lots of practice chasing and catching fish
– early in life spend most time pursuing small fish
Interindividual variation
•
Individuals may use different foraging tactics
– During lactation, Northern fur seals use one of two tactics or a mix
– Shallow dives <75m that become shallower at night to catch vertically migrating prey beyond
continental shelf
•
– Deep dives with no diel variation to catch non-migrating prey at or near the shelf break
– Net energy gain of two tactics appears to be similar – what would happen if they were not?
Individuals may use different foraging tactics
– In odontocetes, some variation appears to be traditional with offspring inheriting or learning their
mother’s tactics
– Sponge carrying in Shark Bay T. aduncus (primarily females)
– Extreme shallow water foraging
– Strand feeding in killer whales
Foraging in Space and Time: Movements and Habitat Use
Habitat use and movements
–
Habitat use is important because the habitat provides all of the resources needed for survival and
reproduction
–
–
Choosing where to forage is one of the most important steps in successful foraging
–
Habitat use patterns and movements/search patterns are adaptations to
– deal with the patchy nature (distribution and abundance) of prey
– reduce the probability of being killed by predators
– Maximize reproduction
–
In general, animals should only move as mush as they have to in order to meet their needs including
having a buffer
– “needs” often vary by age and sex
Marine mammals forage in many marine habitats and prey are often patchy is space and time
– Scale of patchiness highly variable
– Patchiness may vary predictably at various scales or be unpredictable
– Patches usually vary in quality
– Predictably good patches tend to be found at shelf breaks, other high-relief features
– Open ocean frontal systems are productive but often unpredictably located
Home range
•
•
•
•
Stable area over which an individual conducts its activities
May shift seasonally
Optimal home range size is smallest possible
Female home range is usually set by foraging needs, males by reproductive ones
– In species with distinct breeding season males may be driven more by foraging concerns
Home range and movements of marine mammals
•
Home range size and movement distances vary greatly
•
•
Some movements are huge and involve long periods of fasting (migrations)
– Body size scales with home range size
Others are restricted and involve choices of discrete habitat patches
Spatial and temporal scales of marine mammal foraging
–
–
Scale is a critical issue in foraging ecology
–
Ability to store energy serves as a further buffer
Large bodies and long lives allow individuals to deal with variability in resources over large spatial and
temporal scales
Scale and sperm whale feeding success
–
–
–
–
–
–
Whitehead used defecation rates is indicator of success for whales of Galapagos Is
Scales of 5h – 4yr and 100-5000 km2 (individuals potential range)
Warm water leads to lower success
Variation at scale of ~100km and2 several months is about 60% of mean success
Variation of 2-4 yrs >500km2 130% of long-term mean
Sperm whales can live off stores for ~ 3mo and environmental variables don’t coincide at scales of
500km
–
They should move when faced with prey shortage since trips of ~500km should only take about 5-6
days
–
–
Such trips have been observed
Adaptive behavior allows survival in a patchy and unpredictable environment
Determining Movements
•
Indirect Methods
– Inferences from distributions
– Whaling/sealing records
– Ship based and aerial surveys
– Strandings
– Seasonal and annual changes in distribution can help infer-large scale movements but not
smaller scale
•
•
– Tracking with acoustics
– Acoustic surveys
– Navy anti-submarine listening network
Indirect Methods
– Population characteristics
• Parasite infections, morphology, genetics, contaminants, vocalizations, stable isotope ratios,
diet, fatty acids can all give clues as to where animals might be moving
• Like other indirect methods, these are macro-scale movements only
Direct Methods
– Individual identification is critical
– Tagging
– Fin/flipper tags, freeze branding, and dyes
– Provides information on resightings
– Large samples are possible but large gaps also possible
– Natural markings (Photoidentification)
– Scar patters (sirenians, cetaceans)
– Pigmentation patterns (tails, bodies)
– Dorsal fin scarring/nicks
– Callosities
– Both tagging and natural markings are quite useful for determining fine-scale movements and
habitat use of species with restricted home ranges but are of more limited use for wide-ranging
species
– Low resighting rates
– However, there can be useful long-distance resightings (e.g. humpbacks between Hawaii and SE
Alaska)
•
Direct Methods: Surveys
– May be conducted from boats, airplanes, helicopters
– It is critical to determine sighting biases
• Species-specific
• Weather-specific
• Distance from platform
Tracking movements
•
Direct methods: Telemetry
– Radio (vhf), acoustic, satellite, and cell phone
– Satellite-linked time depth recorders
– GPS-tags
– Stomach temperature probes
– Techniques are useful in different circumstances
– Appropriate attachment to animals is critical (collars, glue, suction cups, tail harness, barbs)
– Locations determined by following the animal or passive listening/satellite-linked data
collection
Studying movements of marine mammals
•
•
Understanding the distribution and abundance of food resources is critical
Prey surveys are very important
– Remote sensing (primary productivity)
– Trawls/ship-based sampling
– Towed acoustic arrays
– Fish trapping
– Video surveys
Central place foraging
•
•
When a species makes foraging trips from a location to which they must return
•
Much theory has investigated how to allocate time and effort
– In general, stay at the foraging patch longer when you have to swim farther
– Usually supported in marine mammals
Pinnipeds that must haul out are the most obvious marine mammal CPFs but diving can be considered a
second type of CPF
Body size, sex and CPF
•
Size dimorphism and sex influences trip duration and distance
– In Moray Firth, Scotland male harbor seals make trips of 61 hours and 25.5 km while the smaller
females make trips that are about 30 hours and 14 km
– Antarctic fur seal females forage within 350km of breeding sites while males range to 900 km
Foraging costs and CPF
•
•
Foraging costs influence foraging decisions
Boyd et al (1997) glued 250g wood blocks to lactating Antarctic fur seals, and these seals
– Increased trip duration (stayed at sea longer)
– Pups grew at same rate as untreated fur seals suggesting successful compensation
– What were the costs of longer trips?
Environmental variability and CPF
•
When prey availability drops
– Antarctic fur seals increase time at sea and foraging activity
– More dives (same % time underwater and dives/hr)
– 33-50% greater effort, but still lower pup growth and higher pup mortality
– Northern fur seals keep time at sea constant but work harder
– Field metabolic rate increased, probably indicative of different foraging tactics
Foraging effort in non-CPF
•
Varies with prey abundance or population status
– Sea otter populations near K spend more than 50% of time foraging
– New colonies or growing colonies spend less than 20% of time foraging
Habitat use
•
Densities generally higher at features that concentrate prey
– Banks, canyons, shelf edges, estuaries, oceanic fronts, core rings
– Individuals often return to productive areas annually if they are not year-round residents
– Humpback whales, polar bears
•
Ideal free distribution suggests that there should be a mathematical match between prey abundance and
predator abundance
– Let’s draw some graphs of
– 1. Predicted densities in two habitats
– 2. Predicted densities relative to food
•
Some marine mammals don’t conform
– Humpback and common minke whales show a threshold response, only using a patch when prey
density is high enough
Scale habitat use
•
Antarctic fur seals appear to maximize energy intake rate, and best match with krill abundance is at
scale of 10-100 km
– Do not match as well at very small spatial scale
– Why wouldn’t they match at all spatial scales?
Boto habitat use (Martin and da Silva 2004)
–
Habitats available to dolphins varies throughout year
– Main channel
– Várzea channel (seasonally flooded next to main channels
– Igapó (dense forest inside várzea flooded to 7m)
– Chavascal (temporary and permanent shallow lakes within várzea)
– Ressacas (shallow bays next to rivers with reduced flow)
–
Used boat surveys and VHF telemetry
•
How did densities change relative to water level?
•
Did all botos show the same habitat use patterns?
– Females used flooded channels and shallow lakes more than males which used main channels
•
What were the explanations for this pattern?
– Food, avoiding harassment, current avoidance
Foraging-Safety Tradeoffs
•
•
•
Often the most productive places to forage are also the most dangerous
•
Two major habitat types
– Shallow (<4m, seagrass covered)
Animals must trade-off foraging in a safe spot with getting enough food to eat
Since most marine mammals are both predators and prey, this type of trade-off is probably quite
common but has rarely been investigated
Habitat use by Tursiops aduncus in Shark Bay, Australia (Heithaus and Dill 2006)
– Deep (>6m, sand covered)
Shark Bay dolphins summary
•
•
Match food distribution at scale of habitat patches and microhabitats when sharks are absent
Largely abandon high-prey but dangerous areas when sharks move in
– but some individuals remain in shallows
– juvenile males tend to keep foraging in dangerous but now more productive habitats
Search Patterns
•
•
Once a general region is selected, must locate and remain in high quality prey patches
Marginal Value Theorem: stay in a patch until harvest rate in patch is equal to environmental average
– Need to have good info of environmental average
– Traplining – moving among a series of resource locations to sample prey density
– Humpback whales?
– Dugongs?
•
A general movement tactic
Area Restricted Search: Move in a straight line when foraging is poor, but make frequent turns, and
increase angle when doing well
– Right whales and sperm whales fit
– Elephant seals probably
– No data on foraging success
Movement tactics of grey seals
–
Austin et al. (2004) studied grey seal movements after departing Sable Island and stressed the
importance of individual differences in foraging tactics
– Satellite tags of 52 individuals
–
What were the findings of this study
– Three movement tactics used: directed movers, residents, and CRW movers
– Directed movers more likely to be males
– Residents more likely to be females
–
What is a major problem with tracking data?
– Autocorrelation of points
–
How can this be overcome
– Individual is a sampling unit
– Use features of the original track
Variation in foraging movements
•
•
Tides can influence habitat use and foraging behavior
– Dolphins in tidal creeks of SE US only come to strand feed during certain tides
– Humpback dolphins move inshore with risking tides into mangrove habitats then offshore with
falling tide
– Rising tides can make certain habitats available like shallow banks for bottlenose dolphins or
dugongs or beaches for killer whales to strand feed
At night, many organisms in pelagic waters move from very deep to 100-200m from the surface,
becoming more readily available
– Striped dolphins in the Mediterranean and spinner dolphins in Hawaii move from resting during the
day to foraging at night
– Antarctic fur seals sometimes modify diving tactics to take advantage
Habitat partitioning
•
Habitats may be partitioned at small spatial scales
– Harbor seals at different haul outs in Prince William sound forage in different locations even though
they could reach the entire sound
•
– Reduce killer whale predation in transit?
– Benefit of local knowledge?
Individuals may specialize in foraging in particular habitats
– Tursiops aduncus in Shark Bay show preferences for particular habitat types
– Swift-current channels
– Deep water foraging
– Shallow water feeding
– Use of specialized tactics may drive this pattern (e.g. sponge carrying)
Seasonal movements
–
Some are associated with predictable shifts in prey distribution
– Harbor seals move from NS, ME in summer to MA, NH in winter
– Hector’s dolphins move inshore/offshore seasonally
– T truncatus off east coast of US make seasonal shifts N and S (portions of pop’ns)
– Tucuxi and botu use flooded forests seasonally
–
Some shifts are unpredictable
– Humpback, fin, right, sei whales of NE US coast shift in response to abundance of copepods,
herring, and sand lance
– Harp seals in Barents Sea moved in response to collapse in capelin
Migrations
–
Fat stores and large bodies allow seasonally available or distant prey and patchy resources to be
exploited
–
Northern Elephant seals
– Males 5 times the size of females
– Make two migrations yearly (CA to N Pacific)
– Use California current as a corridor but males and females segregate on foraging grounds
– Females stay south of 50º in subarctic current
– Males are further north in Alaska Stream
– Both areas are frontal regions with high productivity and cephalopod aggregations
•
•
•
Predictable movements made between widely separated habitats
–
–
Most obvious and long distance migrations involve transits between feeding and breeding areas
–
Large size contributes to migratory ability through lower size-specific metabolism and storage
capacities
Cetacean migration
•
Most cetaceans do not show migrations to traditional breeding and feeding sites, but those that do
involve N/S movements
•
Mysticetes are well-known for their migrations, unlike odontocetes
Some made in relation to food resources
Temperature may also be a driving factor
– North/south movements of manatees and dugongs (19ºC may be a threshold)
– Cetaceans and most pinnipeds can’t stay in areas where ice cover is complete and those that don’t
find leads may be trapped
Fasting occurs during many mysticete migrations, but not others
– Gray whales also feed on northward migration
•
Reason for baleen whale migration is still debated: why travel so far from your food to give birth?
– Calves could survive the cold climates, but they grow faster in warmer waters
– Could have evolved to avoid high predation risk from killer whales in higher latitudes
•
Humpback whales follow traditional routes, but some dispersal/interannual movement between
breeding areas occurs
– Hawaii may be a recent colonization event
• Up to 8300 km from South America to Antarctica
• Only 1200 km North Pacific to CA/MX
– Not all individuals migrate each year
•
Gray whales move about 9000 km from the Bering Sea to Baja California
– Females and calves stay closer to shore and follow contours of coast and immatures are closer than
adults – probably to avoid killer whales
–
Sperm whale males migrate from as far as the ice edge in summer to the Equator (6500 km) in winter
– Females stay within tropics/temperate areas
–
–
Northern right whale males stay in northern waters while females and calves move north/south
Sei whales don’t appear to migrate to breed, and other species movements are still poorly known
Migration Routes: Pinnipeds
•
•
Elephant seals travel up to almost 4000 km from North Pacific to breeding/molting areas in California
Harp seals move up to 4000 km from 70ºN feeding grounds to 40N breeding areas
Sexual segregation in foraging
–
Beluga whales
– Males move to deep water trenches in summer to feed (larger size allows deeper dives??)
– Females stay in shallower water
–
Elephant seals (northern and southern)
– Males tend to stay over the continental shelf
– Females are in open deeper waters
– Occurs even in juveniles
Optimal Diving Behavior: Theory and Practice
Diving
•
•
•
A key choice that all marine mammal
s must make: how to allocate time between the surface and the bottom
Huge impact on energy balance
– may also influence other decisions like habitat use
Diving bouts
•
•
Groups of individual dives made almost continuously
•
•
In general, few individuals are studied, but each contributes a huge number of dives
•
Most studies treat these as the same with each dive as an independent point – this is statistically wrong
Bouts are generally separated by periods of inactivity (e.g. haul out or very slow, shallow dives)
A general problem with studies of diving in marine mammals
Which is better or are they the same?
– 3 individuals with 1000 dives (3000 total)
– 30 individuals with 100 dives (3000 dives total)
Marginal Value Theorem
•
Charnov (1976)
– Broadly applicable to optimality questions
– Can be used to determine behavior that optimizes rates (e.g. number of flowers visited during a
foraging trip)
– Kramer (1988) first to apply it to diving behavior
Optimal Diving: The first model
•
•
Keys:
– Oxygen uptake occurs at a decelerating rate
– Energy intake determined by bottom time
Prediction
– As travel time increases, so should the corresponding surface interval and time spent submerged
– There is an optimal surface time s* for every depth to maximize oxygen delivery
Optimal Diving and Marine Mammals
•
Do marine mammals conform to theory?
– Increasing dive times with increasing depth (travel time) found in many species
• Northern fur seals
• Antarctica fur seals
• Humpback whales
•
When would this theory not hold?
– Single prey loaders
– Not trying to maximize bottom time
– Any others?
Dive Types
•
•
Looking at a TDR profile, simple theory might predict one type of dive – flat bottomed
Dive shape can be used to infer foraging, but be careful!
Thompson and Fedak (2001)
•
TDR studies show that many marine mammals make numerous dives that are much shorter in duration
than expected by simple theory
•
Modeled diving decisions when foragers face patchy prey resources and can assess the quality of
patches throughout the dive
– Divers should abort dives early if encounter rates are low (use a simple giving up rule)
– Shallow divers should conform to this prediction more tightly than deep divers (fewer dives close to
ADL
– Support for predictions, but how were the sample sizes?
Diving and prey abundance in wild pinnipeds
•
•
Antarctic fur seals foraging on krill had longer diving bouts with increased prey encounter rates
Galapagos fur seals largely cease diving during full moons when DSL organisms are too deep to capture
efficiently
Testing Thompson and Fedak
•
•
•
Cornick and Horning (2003) conducted captive trials to test
– There is a density of prey under which seals should never forage
– Dive duration should increase with increasing prey abundance above this threshold
– There should be a peak in foraging efficiency at a some encounter rate over which there is no gain
Trials with Stellar sea lions
– A problem: only 3 individuals!
Trials with Stellar sea lions
– Dive duration, foraging time and efficiency increased with increasing encounter rate
– Were extrapolations to wild pinnipeds convincing?
Another diving question
•
•
When prey density varies vertically, how deep should you dive
– To the shallowest prey available?
– To the highest prey density?
Theoretical models predict that dives should generally be deeper than the shallowest prey, but not to the
maximum prey density
– Some preliminary support from harbor seals
Vertical movements by prey
•
The deep scattering layer organisms change their availability throughout the day and many marine
mammals take advantage
– Forage mainly at night (e.g. spinner dolphins) or decrease dive depths during the night (e.g.
Antarctic fur seals)
Anticipatory and Compensatory Diving
•
•
Some debate as to whether an animal should have an optimal surface interval for a dive based on the
preceding (anticipatory) or following (compensatory) surface interval
Work on Weddell seals suggests anticipatory diving, but this may vary by species and circumstance
– e.g.
Prolonged dives in pursuit of prey
Diving under the risk of predation
•
LeBoef and Crocker 1996
– Elephant seals spend little time at the surface when on the continental shelf, often swim near bottom
when moving to or from rookeries
– Interpreted as avoidance of white sharks in NES and killer whales in SES
Heithaus and Frid (2003)
•
A graphical model of diving under the risk of predation
– Suggests that surface time should decrease!
–What happens when divers are at risk for prolonged time periods?
–Risk may vary with time spent at the surface in several ways
–Increase linearly, accelerate to a point, decelerate to a point
–Influences how a diver should modify their surface interval
–If risk is level or increases with time at the surface divers should make more, shorter
dives
–If risk decreases with time at the surface they should make fewer, longer dives
Harbor seal diving: fish, sharks and killer whales (Frid)
•
•
Prince William Sound, Alaska
•
–
–
Many of the fish that they eat are at high densities at depth where risk from sharks may be high
–
Results
– Sharks appear to be the biggest threat (where food is highest – down deep)
– Diving behavior modified to reduce risk
– Body condition matters
Diving decisions should vary with condition
•
Harbor seals must maintain adequate body condition to breed while avoiding killer whale predation in
surface waters and sleeper shark predation at depth
Used indirect estimates of shark and killer whale threat
TDRs on harbor seals to monitor diving
– While being tracked with simultaneous measures of prey density using acoustic surveys
– Left attached long-term to monitor diving changes throughout season
Individuals in poor condition should be willing to forage for lesser returns or take more risks
– Largely unexplored in marine mammals, but Alejandro Frid has found that:
– Harbor seals in poor condition spend more time diving deep, where risk of sharks is high, than
seals in good condition
– Prey shortage (more seals in poor condition) can lead to increased predation rates due to greater
risk-taking
Swimming costs and diving
•
•
Swimming costs influence foraging decisions
Boyd et al (1997) glued 250g wood blocks to lactating Antarctic fur seals, and these seals
– Made shorter, shallower dives
– Dive and steeper angles to compensate for slower swimming speeds
– Adjusted maximum bottom time
Minimizing energy expenditure
•
During diving, marine mammals try to keep energy expenditures to a minimum
•
Most marine mammals that have been studied only swim actively to the point where they are negatively
buoyant, then glide as the descend
Energetics
Evolutionary Energetics
•
•
•
•
•
How is energy used to maximize fitness?
Energetics includes processes that change chemical energy to heat and work
For energy, type of use, efficiency of use, and storage ability are critical to fitness and thus should be
optimized by selection
Energetics are critical at many levels of organization
– Individuals
– Populations
– Ecosystem energy flux
We’ll focus on individuals since energy is a good fitness currency and thus aids our understanding of
both ecology and life history
Energy allocation
•
•
Once food is captured and processed, what do you do with it?
Decisions are not simple
– Counterintuitive results are possible.
For example, being lean may be better than being fat if
foraging is reliable and it helps you escape predators
•
Three uses for energy
– Metabolism (including activity)
– Growth
• Length or weight (can be a tradeoff)
• Storage is part of growth
– Reproduction
•
Metabolism and Growth occur over many time scales from minutes to months
– e.g. seasonal changes in resources for cetacean fasting
•
Reproductive investment and Growth can be observed over period of years
Allocation to Reproduction
•
Depends of age, expectations of current and future reproduction, body condition, environmental factors
and variability
•
•
Body mass is often more important than age in pinnipeds
What should happen to allocation if food availability were to increase markedly?
Energetics of life in cold water
•
•
Energetics driven by difficulties of staying warm
Distribution may be influenced by metabolic demands of staying warm
– Sirenians and cetaceans tend to give birth in tropics since young are born in the water
– Pinnipeds give birth on land, allowing high latitude reproduction
Metabolic rate
•
•
•
•
Rate of energy use
– Measured in Watts (Joules/sec)
Calories (heat): energy to raise 1 ml water 1ºK
Heat is a measure of energy in a body and 1 J = 4.185 calories
Metabolic rates sometimes measured as ml O2/sec
– Close surrogate of metabolic rate
– VO2 = oxygen consumption/body mass (kg)
Some methods to measure metabolic rate
•
Calorimetry
– Direct measurement of heat production
– Only truly direct method
•
Oxygen respiromemtry
– Measurement of oxygen consumption and sometimes carbon dioxide production
– Most common technique in the laboratory
•
Doubly labeled water
– Indirect respirometry that measures water and carbon dioxide flux
– Often used in field studies
Metabolic fuels
•
Fat, protein, carbohydrates used as fuels
•
Harbor seals use lipids for 87% of resting energy and 95% of exercising energy
– Generally a mix of fat and protein with little carbohydrate
– Mix burned usually close to diet proportions
– Probably due to high fat diet
– May burn more protein and carbohydrate just after feeding
Metabolic rates
•
•
MR (metabolic rate)
BMR (basal metabolic rate)
– measured for a sexually mature, resting, thermoneutral, non-growing, non-digesting individual
– Should be lowest stable measurement possible
•
RMR (resting metabolic rate)
•
AMR (active metabolic rate)
•
ADMR (average daily metabolic rate)
•
FMR (field metabolic rate)
– individual is at rest, but doesn’t fit all BMR criteria
– measured during an activity
– AMR expressed on a daily basis
– Measured in a free-ranging animal
Metabolic rates of marine mammals
–
Huge range of body size
– 28 kg Galapagos fur seal – 120,000 kg blue whale
–
–
Problems of heat management very different at these sizes
BMR predicted to increase at a rate of 3.39 M0.75 for terrestrial mammals
– However, only 5 of 76 studies conformed to BMR measures
– Difficult to know relationship holds due to statistical and experimental difficulties
– BMR of cetaceans and pinnipeds appears to be 1.4-2.1x predicted for terrestrial mammals
– Not particularly helpful for marine mammals – need FMR
Blubber and metabolic rate
•
Blubber uses little energy but can account for more than 40% of body weight and can be reduced
quickly (>50% in weeks)
– BMR on a body mass basis may fluctuate widely
– Makes comparisons in MR within and among species difficult
– Should fat be excluded from comparisons?
– Still unclear
Field metabolic rate
•
•
•
•
Often expressed as multiples of BMR or predicted BMR for body size
Needed to examine links to ecology
Less sensitive to mass increases than other measures
FMR per kg decreases with increasing body size
Surface area and metabolic rate
•
Convergence of terrestrial and marine mammal MR at large body size suggests marine mammals don’t
need elevated MR to stay warm
– Also aided by not needing to fight gravity
•
•
SA scales to VOL at power of 0.64-0.68 except on flippers (0.49)
–
Mass-specific FMR decreases with body size, but fat storage capacity increases in proportion to body
mass
– Northern elephant seal 46% fat
– Harbor seal 31% fat
–
Takes longer to exhaust fat as size increases
– Can survive on fat alone
– Could be days to more than 2 years!
– Mysticetes take full advantage
FMR-mass relationship scales at the rate of flipper SA:VOL so flipper SA may be important
determinant of FMR
Fat stores, FMR, and body size
What determines energetic strategies and tactics?
•
Costa suggested a difference in foraging strategies between otariids and phocids
•
Given what we have learned, this relationship is more likely due to body size and not phylogeny
•
– otariids maximize intake rate and phocids maximize efficiency
– Can this be tested?
Maximum MR
Generally much higher than FMR
– Juvenile harbor seals 5.8-7.3x predicted BMR
– Juvenile California sea lions 6.2x
– Tursiops 6.6-9.9x
•
•
•
•
•
•
These measurements are at the high end of what is possible under aerobic metabolism
FMRs of 5-7x predicted BMR have been measured in small marine mammals
– May be too high – validity of doubly labeled water technique in marine mammals needs to be tested
MR, activity, and control
BMR lowest mean metabolic rate
Other expenditure on activates
– Movement, growth, digestion
MR appears to be under high degree of control in marine mammals
BMR may not be constant
– Reduced to conserve energy during fasting
– Reduced to conserve oxygen during diving
Energetics of locomotion
–
Cost increases as speed increases
– Drag and increased power needs (power increases as cube of speed)
–
–
Basal locomotion costs lower than terrestrial mammals due to buoyancy
As size increases frontal area relative to mass decreases
– Frontal area most important in cost of transport
– Swimming costs decrease as portion of FMR as size increases
Locomotion costs
•
•
Theory predicts locomotion costs of 40-60% of overall energy expenditure in southern elephant seals
Field results are mixed
– MR of standard swimming speeds of Tursiops not significantly different from resting (higher if
faster)
– Antarctic fur seals: no relationship between speed and MR
– May be due to switching swimming tactics (e.g. porpoise)
•
Cost of transport is lowest at intermediate swimming speeds (1.5-2.2 m/sec)
– Supported by field studies of pinnipeds and cetaceans
•
Minimum COT speed increases as temperature drops
– Heat generated by increased MR at high speeds used in thermoregulation so metabolism not needed
to generate heat
– Travel speeds higher in winter for Tursiops aduncus in Shark Bay
•
COT per stroke increases with mass
Energetics of Thermoregulation
•
•
Q10 – change in MR with change of 10ºC
Antarctic fur seal adults
– 8.1ºC in air MR = 2.6 W/kg
– 6.8ºC in water MR = 6.1 W/kg
– Extra energy may come from non-shivering thermogenesis
Critical temperature
•
Temperature below which MR must be increased to maintain core body temperature
– 10ºC for harbor seals in water
– <-10ºC for harbor seals in air
– Harbor seals Q10 = 1 from -2.3ºC – 25.1ºC but Q10 2 outside this range
Feeding can elevate MR
•
Heat increment of feeding or specific dynamic action (SDA) is the increase in metabolic rate over
fasting (food processing tax)
– Up to 46% increase in harbor seal MR
– Stellar sea lion 10-12%
– Sea otters 54%; otters rest after feeding since they don’t need activity to stay warm
•
If costs are too high, may need to cease swimming to avoid overshooting max MR
Foraging costs (Williams et al 2004)
•
Studied 9 Weddell seals diving at isolated hole covered with a dome using animal-borne video and data
loggers
•
Determined cost of each flipper stroke and cost of feeding
– HIF 44% over AMR (non foraging dives) and may last for up to 5 hr after meal
– Strokes (0.044 ml O2 kg-1 stroke-1) accounted for elevating MR more than duration of dives (due to
gliding) and is lower than stride costs of terrestrial sp
– Swimming resulted in 1.3-3.5x increase from RMR
– Suggests that the cost of diving may be predicted by sum of individual stroke costs
Metabolic rate and diving
•
Aerobic dive limits are influenced by MR
– Higher MR can greatly reduce the time that can be spent submerged using aerobic respiration
–Dive depths can influence the metabolic rate during a dive (Hastie et al. 2006)
–Deeper dives in Stellar sea lions led to lower oxygen consumption rates (3.4 L/min @ 10m vs
1.4 L/min @ 300m)
–Probably because more time spent gliding due to negative buoyancy at depth
–Energetic demand higher at shallow depths (~18.9 kg/day) than deep ones (~8 kg/day)
–How would changes in vertical distribution of prey influence sea lions and their populations?
Foraging costs in blue and fin whales
–
Often perform numerous foraging lunges while at depth
– Blue whales lunge by rolling upside down, creating unique depth profile
–
•
•
Exhibit short dive times relative to predicted ADL (blue: 31 vs 8 min; fin 28 vs 6 min) – why?
•
Costs of lunge probably associated with need to accelerate
Recovery times greater for same submerged time when whales make multiple lunges
Appears to be due to energetic costs of lunge feeding (3.15 fold increase in blue whales, 3.6x for fin
whales)
MR and foraging in spinner dolphins
•
•
•
Benoit-Bird (2004)
Spinner dolphins feed on boundary layer organisms that are only available for limited time
Used MR of captive striped dolphin to assess energetic need and measured energy content of possible
spinner dolphin prey
•
•
Tried to determine how many prey must be captured and what prey are best to catch
•
Stomach contents of published reports and one stranded dolphin suggest that the model is reasonable
– Squid lengths 8-11 cm, fish ~7.7 cm; 985 prey items in stranded animal that were likely from one
night of foraging
•
Suggest that spinner dolphin population is limited by foraging time not prey availability
– What do you think about this hypothesis?
Number of prey required per night depends greatly on energetic content of prey (size) and costs
associated with catching it
Energy budgets
•
•
Must be balanced, but time scale varies
– Small species must be balanced over periods of days or weeks
– Larger body sizes have longer time scales, on the order of a year for large mysticetes
Reproductive strategies of pinnipeds are heavily influenced by the time scale of energy budgets and how
they scale to body size
Energetics and management
•
Understanding individual energy demand (across age-sex classes) can help build a population energy
budget
•
•
Tied to diet, these budgets can estimate mortality inflicted on prey
Can help trace energy flow through ecosystems and vulnerability to changes in food availability
Community Ecology of Marine Mammals
Community Ecology
•
•
Communities are collections of potentially interacting populations
Many types of interactions may occur within communities
– Predation (+,-)
– Parasitism (+,-)
– Competition (+,-)
– Mutualisms (+,+)
– Comensalisms (+,0)
The role of predators in communities
•
A large question in community ecology is whether predators limit populations of their prey or if
population sizes are driving by food availability
•
•
•
•
Bottom-up: consumers limited by food availability at lower trophic levels
Top-down: consumers control diversity and abundance at lower trophic levels
Both occur – it isn’t one or the other
Marine mammals likely to exert top-down effects
Beyond the body count: risk effects
•
Most of ecology has focused on direct predation and consumptive effects
– How many prey are killed by predators
– How much food is taken by competitors
•
•
Behavioral effects (“risk effects” or “non-consumptive effects”) are not as well appreciated by most
marine mammalogists
– Anti-predator behavior
– Predator-prey games
– Dominance interactions and interference
Risk effects can reduce population sizes and modify community dynamics
The complete role of predators
•
Predators affect their prey through direct predation, risk effects, and the interaction of both
– For ecample, prey may give up feeding opportunities to stay safe but then have to take risks when
they near starvation and become an easier meal
•
•
Direct predation and risk effects can impact the wider community alone or together
Predators can also influence communities by moving nutrients and disturbing the habitat
Direct and Indirect Effects
•
•
When two species effect one another through intimate interaction it is a direct effect (e.g. Species A eats
Species B)
Direct effects may be transmitted through an environment so that a species may effect another without a
direct interaction by affecting the other species’ competitors, predators, prey, etc
Indirect Effects
•
•
Killer whales in the northeast Pacific (Baird et al 1992)
•
Keystone Species
– Species that has an impact on the structure of a community that is out of proportion to their relative
abundance (high impact, low abundance)
– Sea otters are a keystone species through predation on urchins
• If kelp lost, sets off a cascade that influences invertebrates, fishes, birds, other marine mammals
Trophic Cascade
– Indirect effects may cascade through an ecosystem such that a change in one species may have a
large effect on the rest of the community
Marine Mammal roles in their communities
•
Marine mammals assumed to play large role in regulating populations of their prey
– High metabolic rates and large size mean that they can consume a large biomass of prey
•
•
Need to know if this rate of predation impacts prey populations or if it is compensatory
(predators eat individuals that would have died anyway) . . . In other words, studies of prey are
critical
Feed at high trophic levels – means that they may have wide-ranging impacts on communities
– Top predators require high primary productivity to support their populations because ~90% of
energy lost at each trophic transfer
The role of marine mammals
•
•
•
How would the removal of marine mammals affect marine ecosystems?
Hard to determine for marine mammals due to inability to conduct manipulative experiments
Cetaceans (or even sperm whales alone) may consume more prey than all human fisheries, but
consumption levels alone do not necessarily mean that predators play an important role in marine
ecosystems
Consumptive effects of Marine Mammals
•
•
Sea otters reduce urchin populations
•
Dugong grazing may remove 65-95% of shoots, 31-71% of above ground biomass and 73-96% of
below ground biomass
– Exclosure experiments show that dugong grazing modifies seagrass species composition
Gray whales may remove 8-18% of amphipod productivity annually, but bioturbation may improve
productivity by sediments trapped in pits providing nutrients for early success ional species
Interspecific competition
•
Marine mammals are often engaged in direct competitive interactions with other marine mammals or
other taxa
– Significant dietary overlap between several dolphin species and sharks in South Africa, including
some that would eat them (intraguild predation)
– Killer whales and white sharks
– Krill feeders in Antarctica
Competition in Antarctica
•
•
•
Removal of cetacean biomass (45 million tons to 9 million tons) released ~ 150 million tons of krill
Led to huge increase in crabeater and Antarctic fur seals as well as penguins and possibly minke whales
Competitive release is a likely mechanism
Competition and apparent competition
•
Gray and harbor seals exhibit apparent competition because they share large sharks as predators with
the disproportionate effect on harbor seals (Bowen et al. 2004)
•
There is also competition for food resources (e.g. sand lance)
Risk effects of marine mammals
•
Because most marine mammals target mobile prey, MM certainly induce risk effects
– E.g. sea lions cause herbivorous fishes to reduce foraging rates
•
Studies of responses of prey to marine mammals are few, but we have already talked about some in the
prey manipulation sections
The role of sea otters
•
•
Sea otters have many direct and indirect effects, and even facilitate their own population growth to some
extent (more fishes)
Importance of herbivores depends on number of trophic levels
– May explain lack of chemical defenses in Northern hemisphere
– Add a sea otter predator and see what happens!
Other roles of marine mammals
–
In Arctic ecosystems, benthic foraging by walrus and gray whales may increase productivity of benthic
habitats through bioturbation (benefits early succession species)
– Gray whales may turn over 9-27% of northern Bering sea substrate annually
–Ray et al. (2006) suggest that thousands of square kilometers of bottom are turned over by walrus
–How would changes in sea ice influence the ecosystem via walrus?
The role of marine mammals
•
Harbor seals in Lower Seal Lake of Quebec appear to influence
– Fish species composition (brook trout dominate rather than lake trout)
– Life history characteristics of trout (generally smaller, younger, grow more rapidly, mature earlier)
•
•
Based on differences in lakes with and without seals, not on experimental data
Dugongs can have a large impact on the community composition and biomass of seagrasses
– Consume 8-15% of body weight each day
– Can reduce above-ground biomass 70-95% and below-ground biomass 30-70%
– Heavy grazing favors fast-growing nitrogen-rich species over slower growing ones (reverses
competitive interactions in seagrasses
– Likely has impact on invertebrate and fish communities that rely on seagrasses
Community ecology and management
•
•
The belief that marine mammals can have a large impact on prey species abundance is at the root of
arguments that they compete with fisheries
Good data on effects of marine mammals on prey populations are critical for making management
decisions, but their position at the highest trophic levels (e.g. Lesage et al. 2001) makes them good
candidates for having an effect
Fisheries and TMII
•
Collapse of Atlantic cod was largely unforeseen, perhaps because of cod behavior and their responses to
seals
•
As cod collapsed, may have formed bigger schools to stay safe from predators like harp seals
Reproductive cycles and energetics
Life in the slowish lane
•
Marine mammals tend to have relatively long gestation periods and all but polar bears have a single
offspring at a time
•
•
•
Interbirth intervals are long
Investment in each offspring fairly high
Marine mammals reproduce slowly!
Reproductive Cycles
–
Normal minimum time for all stages of reproduction in females from ovulation through birth, lactation,
and rest
–
Reproductive (interbirth) interval may be extended based on internal, social, or environmental
conditions
–
Estrus is the period of receptivity in females
Sea otter reproductive cycles
–
–
–
Not well known in general
–
–
–
–
Males appear to be reproductive year-round
–
Pups dependent for 6 months
Do not need to come ashore to give birth
Largely aseasonal reproduction but there may be peaks that occur at different times in different
locations
Exhibit delayed implantation but duration unknown and may be variable
Gestation of 6-8 months, but fetal growth probably 4.5-5.5
Annual reproduction possible, but likely to exhibit longer cycles due to prolonged lactation (4-8
months)
Polar bear reproductive cycles
–
–
Reproductive cycle dominated by cycle of sea ice
–
–
–
–
–
Delay implantation 4-5 months until females enter dens
Mating Mar-May while females have 1 or 2 yo cubs
– Ovulation induced by presence of male
3-4 month period of fetal growth
Mean litter size ~2
IBI 3.1-3.6 years
Reproduction linked closely to food availability and maternal condition
Pinniped reproductive cycles
•
•
Pattern appears to be fairly similar among species
Distinctive features
– Delayed implantation in all species
– Allows uncoupling of time of mating and parturition
– Highly seasonal and synchronized reproductive cycles in most species
– Single offspring during each attempt
– Birth on land or ice
•
Cycle is usually annual and synchronous, but there are exceptions
– Australian sea lion (18 month cycle),
– Walrus (2 year cycle)
– Galapagos fur seals (lactation >1 yr)
– Hawaiian monk seal birth period: 8 months
– Galapagos fur seals: 4 months
–
Phases of female reproductive cycles
– Estrus, delayed implantation, fetal growth
– 15 month gestation in odobenids
– Lengths of phases are consistent within families
– Differences in estrus period lead to differences in period of implantation delay
– Period of fetal growth is not affected by body size
–
Males are also reproductive seasonally and show cycles, but they are reproductive longer (several
months)
•
•
Pregnancy rates vary in annual pinnipeds generally from 0.5-0.9
May be linked to changes in population density and food availability but results vary
– Harp seals appear to show density-dependent regulation (0.81-0.99)
– Not evident in northern elephant seals (>0.9) or Weddell seals (0.46-0.89)
Reproductive seasonality
•
In marine carnivores (pinnipeds, polar bears, sea otters), synchronicity and seasonality of breeding is
probably related to environmental factors
– Ability to exploit seasonal changes in prey are likely the cause of synchronicity in pinnipeds and
polar bear and lack of changes in prey the reason for aseasonality in sea otters
– Predation risk can select for synchronizing breeding, but this possibility not well studied for this
group
•
In Antarctic fur seals, the mean birth date fluctuated based on the availability of prey in the previous
year
•
Pregnancy rate was also tied to food available
Pinniped lactation
–
Otariid and phocids show contrasting lactation patterns
– Otariids stay ashore for a few hours to several days to nurse their pup then go to see for up to 8 days
– Otariids nurse pups for 4 months to over a year
– Most phocids don’t leave the pup during lactation or if they do for periods of hours
– Phocids nurse pups for 4-60 days
• Hooded seals (4 days) and harp seals (9-12 days) are the shortest
–
Odobenids have another pattern
– Calf accompanies mother when they leave the ice to feed
– Calf can nurse at sea
– Maternal care may last 2-3 years but sole dependence on milk is probably only 5 months
Sirenian Reproductive Cycle
•
Mating and calving occur throughout year
– Some seasonality in West Indian manatees and dugongs
•
•
Gestation 12-14 months in manatees and ~14 months in dugongs
•
Interbirth intervals vary greatly
Generally give birth to single offspring but low incidence of twins in Florida manatees (~1.5% of
nursing young; 4% for fetuses)
– 2.5-5 years in manatees
– 3-7 years in dugongs
–
–
Lactation ~ 1 yr in manatee and >1.5 yr for dugongs and accompany for at least second year
•
•
Tend to have highly seasonal birthing and mating times
•
Brydes whales are an exception in some ways: there is no major seasonality to mating or births in
almost all locations they have been studied
Reproduction may be delayed in environmental conditions are poor
– Amazonian manatees during prolonged drought conditions must fast for up to 7 months and lose
body condition
– For dugongs, reductions in food abundance lead to lower proportion of females pregnant, proportion
of population that are claves, and incidence of testicular activity
Mysticete reproductive cycles
Length of cycles vary somewhat
– Fin, blue, humpback, sei, and gray whales tend to follow a two year cycle with ~11-12 month
gestation and 6-10 month lactation
– Minke whales may reproduce annually
– Balaenid whales reproduce every 3-4 years despite gestation and lactation periods similar to other
mysticetes
Odontocete reproductive cycles
•
•
•
Reproduction is seasonal in many species but not as highly synchronized as baleen whales
Gestation periods generally around a year or less, but sperm whales (15-16 mo) and killer whales (17)
are exceptions
Lactation is variable and can be extremely prolonged (we’ll discuss this later)
Sperm whale reproduction
•
•
•
Breeding occurs in the spring (Oct-Dec in SH; Apr-June NH)
•
Reproduction uses a great deal of energy
– Lactation is generally more demanding than gestation
– Pregnancy costs usually spread over much longer time periods
– Fetal mass at birth can be used to estimate cost of gestation, but there are not many differences in
relative birth rates – due to low cost of fetus production
•
Pods of female ovulate synchronously which may be induced by arrival of male
Lactation is important for calves for about 2 years, but suckling may last for 7-8 years in females and 13
years in males
Energetics of reproduction
Lactation lengths and investment vary greatly
– Phocids and mysticetes show relatively short lactation periods
– Shorter lactation periods are compensated by greater offspring growth rate
– Offspring weaned quickly are still dependant on maternally-derived resources for a period of time
while those with longer periods of dependency are not very reliant on stores generated during
lactation
– Offspring begin feeding before weaning in many species with prolonged lactation
Phocids and Otariids
•
Northern elephant seals
– Pups born at 7.5% maternal mass, after 28 days are weaned at 26% of maternal mass
– Pups fast on beach for 2.5 months post-weaning
– Lose 30% of weaning mass before going to sea (18% of maternal mass at 3.5 months of age)
•
Northern fur seals
– Pups nurse for 4 months and are weaned at 35% of maternal mass
– Begin feeding at or near weaning and are nutritionally independent
Hanging around after weaning
•
Many phocids have pups that must remain on the beach for days to months after being weaned while
lipid stores are converted to lean body mass
Phocids and Otariids
•
Phocids are able to store more energy than otariids
•
Phocids have lower metabolic overhead than otariids
– 24.5% (harbor) - 47%(harp) fat in phocids
– 8.3% (California sea lion) – 26% (Galapagos fur seal)
Phocid lactation
•
•
Shortest lactation and fastest pup growth rates in pack ice habitats (4 days in hooded seals)
Longest lactation and slowest pup growth in fast ice habitats (6-7 weeks in Weddell seals)
– Species with long lactation periods and nearby food resources may forage for short periods during
lactation (Weddell, harbor)
Body size and maternal resources
•
Ability to fast during lactation is a unique component of marine mammal reproduction
– Can separate feeding and breeding temporally and spatially
•
Energetic overhead is the energy a female must spend on herself while suckling and fasting
•
–
Large body size can reduce energetic overhead because of the way metabolism and fat storage ability
scale to mass
– Energy reserves increase faster than MR
Short lactation periods allow female to divert greater proportion of stores to milk production
Trip duration and energy investment
•
Females making shorter trips provide less milk energy to their pups at each shore visit
– Consistent with CPF theory
–
Stellar sea lions (36 hrs) provide 0.8 MJ/kg0.75
–
N. fur seals (7 days) provide 4.6 MJ/kg0.75
Food intake during lactation
•
•
Lactating northern fur seals consume 80% more food than nonlactating females
– Requires high-productivity waters
– Lack of warm-water otariids may be linked to lower productivity available in tropical waters
Lactating northern elephant seals would only have to increase daily intake by 12% for the long foraging
period before they migrate to the rookery to give birth
Concentrating energy for offspring
–
Milk composition somewhat reflects diet composition, but the mother enriches the lipid content so milk
is very rich
–
Fat content of milk is related to lactation duration but protein is not (65% lipid in hooded seals)
•
•
•
•
Offspring growth rate is related to fat content of milk
Energetics of ice breeding seals
Lydersen and Kovacs (1999)
There is substantial variation in breeding strategies of ice breeding seals
Energy allocation during lactation influenced by
– Stability of pupping platform
– Water access
– Risk of Predation
– Local food availability
–
Two basic nursing strategies: Strategy 1
– Short lactation period with large amount of energy transferred through very energy rich milk
– Mothers rarely or never feed during lactation
– Pups largely inactive, don’t enter water, and able to allocate high proportion of delivered energy to
reserves (blubber)
– Unstable pupping platforms and low predation risk
– Harp, hooded, grey seals
–
Two basic nursing strategies: Strategy 2
– Longer lactation period with delivery of lower energy milk
– Pups are active and learn to swim and dive during nursing
– Weaned with body compositions similar to adults
– Mothers feed during lactation and weaning is gradual
– Associated with high predation risk habitats
– Bearded and ringed seals
Period of dependency
•
Sirenians
– About 70% of Florida manatees only seen with mother over one winter, the rest in two
– Calves of younger females more likely to be dependant for two winters
– Poorly known in dugongs, but may last at least 1.5 years even though young dugongs start eating
seagrass early
•
Cetaceans
– Highly variable
– 6-7 months in mysticetes with no effect of body size on duration
– 8-24 months in odontocetes and possibly 3-6 years in Tursiops aduncus
– Records of 13 year old sperm whale suckling
– Variable within populations of odontocetes
– Mysticete weaning appears to be abrupt and not overlap with calf feeding very much, and milk is
relatively high in fat (30-53%) - like phocids
– Odontocete weaning is gradual and calves may start catching some food for themselves months (or
years) before being weaned, and milk is relatively low in fat (10-30%) – like otariids
– Important when prey capture difficult
– Duration of lactation should depend on relative benefit of continued nursing for offspring fitness
and costs to future reproduction by the female
– May lead to sex-biased investment in offspring
Female reproduction in Shark Bay bottlenose dolphins
•
Mann et al. (2000)
– Used group surveys and focal follows
– Births are somewhat seasonal
– Females exhibit interbirth intervals of about 4 years
– Mortality rate high (44% by year 3)
– Mothers may enter estrus quickly after loss of calf, but depends on time of loss
– Calves weaned after 2.7-8.0 years with most weaned by 4 (67%)
– Females wean mid-pregnancy
– Female reproductive success was higher for females that were found in shallower water
– What reasons were suggested for this pattern?
– Based on your knowledge of the Shark Bay ecosystem from previous lectures, what is your
hypothesis for this pattern?
Life history and Mating Systems
Major life history traits
•
Marine mammals are relatively large and exhibit traits typical of large body size
– Long lives
– Slow growth
– Delayed sexual maturity
– Produce few offspring per bout
– Invest heavily in each offspring
•
•
Traits relate to trade-offs of costs of growth, maintenance, and reproduction
Traits fine-tuned by ecological variables like food availability and risk
•
Number of offspring
•
Gestation length
– Typically one, except polar bears (2)
– 7 to 17 months
– Long periods probably associated with harsh environments and need for well developed young
(polar bear cubs born small and fast, relatively, but much growth occurs in den)
•
Age at sexual maturity
– Age of being able to fertilize or be fertilized
– Delayed in all species due to tradeoff between growth and reproduction
– Reproduce too small and young less likely to survive or future reproduction compromised
– Sirenians
– Male (2-11 manatee; 9-15 dugong)
– Female (2.5-6 manatee; 9-17 dugong)
– Sea otters
– Male 5-6
– Female 2-5
– Pinnipeds
– Earlier maturation than cetaceans
– Generally 3-7 years
– Cetaceans
– Generally over 7 years, maybe 15-20 (bowhead whales)
– Odontocetes 2-20 years
– Age at maturity generally follows trend of later maturation for larger species, but some notable
exceptions (e.g. balaenopterids – humpback whales at 5)
– Males and females do not necessarily mature at same age
Social vs physiological maturation
•
In many pinniped and cetacean species males do not compete for matings even though they are capable
of fertilization
– Occurs when there is extreme competition among males and smaller males can’t compete
– Sperm whales
Major life history traits: lifespan
•
•
Sirenians
– Dugongs: 73 years
– Manatees: 59 years
– No evidence of post-reproductive lifespan
Cetaceans
– Some social species (e.g. pilot whales, killer whales) appear to live well after their reproductive
lifespan is over which may help them increase inclusive fitness
– Fin whale 94 years
– Minke whale 60 years
– Bowhead appears to be >100 years
– Bottlenose dolphins: 50 years (though usually much less, and shorter lifespan for males)
– Smaller species like harbor porpoise: 15- 25 years
Reproductive senescence
•
At older ages, most mammals show a decline in fertility but few show termination of reproduction well
before expected time of death
•
Short-finned pilot whales definitely show this pattern and there is a strong possibility that it occurs in
killer whales
– Pilot whales stop reproducing at 36 but expect to live to 50
– Most resident killer whales have last calf by 39 but mortality is low for an additional 20 years
•
•
Some evidence for bottlenose dolphins, false killer whales, sperm whales but none for mysticetes
Function not well known but may be due to heavy investment in last offspring at cost of future
reproduction or the “grandmother” effect and investment in their adult offspring and grandoffspring
(inclusive fitness)
Foraging and Life History
•
•
Two types of breeding
•
Income breeders
– Few nutrient and energy reserves, feed during breeding
– Sea otters, most odontocetes, otariid females, small phocids
– Variation in how much income is needed and how frequently foraging trips are made
• E.g. sea otters almost all income
•
•
•
•
Individual animals act to maximize their lifetime fitness
Capital Breeding
– Rely on fat stores, don’t forage during breeding
– Large baleen whales, polar bears, larger phocids, male otariids
Reproductive Strategies and Tactics
May involve tradeoffs between current and future reproduction
Females and males may have different agendas
Strategies and tactics of males and females result in mating systems
Mating systems
•
Monogamy
•
Polygamous
– One partner for both sexes
– Polygyny: many mates for males, one for females
•
– Polyandry: many mates for females, one for males
Promiscuous
– Multiple mates for both genders
•
•
Mating systems are influenced by a number of ecological and social factors
•
Male mating potential, and often distribution, is determined by temporal and spatial distribution of
females
•
Female distributions are often set by resource distribution, predation risk, and costs and benefits of
grouping
Males and females usually have different interests
– Females in rearing offspring
– Males in acquiring mates
Mating tactics
•
Male contests may include
– Contest competition
– Endurance competition
– Scramble competition (locate more efficiently)
– Display competition
– Sperm competition
•
Basic male mating tactics (or are they strategies)
– Resource defense
– Female defense (harems, multi- and single- male groups)
– Search for receptive females (scramble competition)
– Sequential defense of females
– Lekking (aggregate and attract)
Territorial defense vs female defense
•
Juan Fernandez fur seals and grey seals demonstrate difference
Mating tactics
•
Female mating tactics
– Accept males attempting to mate
– Investigate and choose males based on direct or indirect benefits
– Mate promiscuously and use sperm competition
– Incite male-male aggression and mate with the winner
•
Ability to mate with many females is highest when there is high clumping of females and receptivity is
slightly asynchronous . . . why?
– Pinnipeds highly synchronous, but not so much to keep males from monopolizing mating
opportunities (high skew)
– Sirenians most asynchronous
– Odontocetes: there are usually some females available throughout the year
– Mysticetes: seasonal breeding, but season is several months long
•
Where should we see highest degree of monopolization?
Interbirth internals and male competition
•
When there is a high IBI, a smaller proportion of females are going to reproduce in any one year
– What should this do to male-male competition?
Pinniped mating patterns
–
–
–
–
–
•
•
Most intensively studied aspect of pinniped behavior
•
Female phocids are less clumped, especially when receptive and entering water
Polygynous mating seems to be the rule, but degree is highly variable and tactics are also variable
Males do not participate in rearing and invest in acquiring mates
Otariids mate on land
Phocids may mate on land (3) or in the water (15)
Female otariids are highly clumped even when there is plenty of beach habitat available
Several possible reasons for this
– Marginal males
• Poor quality males might fertilize females on periphery
– Male harassment
• Less likely to be target of male if in big group
– Southern sea lions, grey seal, elephant seal
– Selfish herd (and other anti-predator factors)
• Reduce probability of being target of predator
– Thermoregulation
• Cluster near places to stay cool
Pinniped mating systems
•
•
Five basic types of polygamous mating
Phocids use, or may use, all five but most data are from the minority land-maters
– Resource defense
• Possible in a number of species but no concrete evidence
– Female defense
• Elephant seals and grey seal
– Lekking
• Harbor seals of Sable Island: most fertilizations are by males not adjacent to where the female
was on the beach
• May be common in aquatically mating species – conditions are perfect – no resources to defend,
females difficult to defend when receptive, hot spot
– Scramble competition
• Possible in hooded seals and other species but no concrete evidence
– Sequential female defense
• Hawaiian monk seals a possibility – males follow females after they wean their pup
•
Otariids
•
Odobenids
– Resource defense
– Demonstrated in 6 otariids and suggested in 6 others
– Defend thermoregulatory or parturition sites
– Female defense
– May occur in 3 species but methods poor except for one study
– Lekking
– Possibly in 3 species, but still unclear
– Do not use scramble competition to our knowledge
– Atlantic walrus males may defend small groups of females
– Possibility of lekking in Pacific walrus with males displaying and acting aggressively with one
another near female groups
•
Many of the questions about mating strategies and tactics require genetic studies of paternity, especially
for aquatically mating species
–
Multiple mating tactics may occur within a population and likely depend on condition
– Some elephant and grey seal males defend female groups
– Other males stay near periphery of territories and at the water’s edge and attempt matings (forced
copulations) with departing females
– Some evidence of female mimics
Otariid territoriality
–
–
Males usually arrive at traditional breeding sites before females
–
Females choose locations on the beaches based on several factors
– Shade or proximity to water (males don’t seem to be able to predict this)
– Select groups of females to reduce male harassment
•
•
Females will leave their pup before mating occurs, often to thermoregulate
Territories tend to get smaller as breeding season progresses and more males show up
– Antarctic fur seals: 60m2 at beginning 22m2 at peak
Some male Juan Fernandez fur seals defend aquatic territories in areas that females rest
– Have same mating success as those with terrestrial territories
Phocid territoriality
–
Elephant seal males arrive before females and establish dominance hierarchies through fights then
maintain the through vocal and visual threats
– Fight outcomes not predictable based on body size comparisons, but larger males remain in the
hierarchy longer
– Dominant males maintain nearly exclusive access and have higher RS than subordinates but must
expend large amount of energy to maintain position
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–
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Females form large groups and compete for central positions which confer higher reproductive success
–
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Promiscuous mating system, often scramble competition
–
Male dugongs can be more physical than manatees and may gash with tusks
– Mating pairs sometimes seen alone
–
Male mating herds may last weeks for a manatee female, but usually < 1 day for dugong
Gray seal males and females arrive simultaneously
Females do not cluster as tightly as elephant seals but loosely clustered
Male dominance not easily arranged but some males better at holding positions while others roam
Visual threat displays more important than fighting
Not as site-attached; males move to stay near receptive females that often move 5-10m
Length of tenure key for male RS and correlates with body size
Sirenian Mating
Solitary for much of the year (large feeding herds may form) but female manatees in estrus can attract
many males (up to 22 observed) that compete for copulations
Female mating strategies
•
•
Probably limited by maternal care needs
Female choice cannot be resolved currently but may occur in all families
– Females may choose indirectly by inciting competition among males (gray, N elephant) by noisily
resisting attempted copulations
– Multiple matings may allow for sperm competition
– Multiple matings (2-3) common in land-breeding phocids but frequency unknown in otariids
– In several otariid species, females may change locations from year to year to stay with same male
Pup recognition
•
In dense breeding aggregations, especially where mothers leave temporarily, there is strong selection for
mother-pup recognition
– Otariid mothers will strongly reject pups that try to nurse if they are not theirs
– Reunions based on vocalizations, returning to area left before foraging, and scent
– Vocalizations less important in phocids and walrus – individual recognition may be less strong
•
Otariids rarely nurse other’s pups but it does occur in phocids
– Reasons for this behavior in phocids unclear
Sirenian Mating
•
In Shark Bay, male dugongs may display a lek mating tactic (indicates geographic variation in mating
system)
– Males patrol small territories in a bay with little seagrass
– Seem to display (vocal, “sit-ups”)
– Female was seen with single male, but no mating observed
Sea otter mating
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–
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Polygynous mating system with aquatic mating
–
Males establish breeding territories of ~ 1km of coastline during spring breeding season
within female areas
– Resource defense (feeding territories)
– Strong relationship between resources in territory and male mating success
–
Success of non-territorial adult males unknown
Female estrus lasts 3-4 days only when male is swimming with female
Outside breeding season sexes are segregated with males forming large rafting groups and exhibiting
ranges on the periphery of females’
Polar bear mating
•
Polygynous
– Males travel extensively in spring searching for receptive females
– Females may release pheromones in urine or footpad secretions
• Males can track for up to 100 km
– Male scramble competition for females and will fight for access
– Mate multiple times over several days
•
Habitat use of females with cubs influenced by distribution of potentially infanticidal males
Cetacean Mating
•
•
Mating systems of most species unknown
•
•
Monogamy not described for any species
•
Resource defense is unlikely due to nature of resources
Sexual behavior is important in social behavior and for some species there are many non-reproductive
copulations
Polygyny appears to be most likely mating system for most mysticetes, but form not well known and
promiscuity also likely
•
Scramble competition described in some species (e.g. humpback whales) and sperm competition may be
important
•
Right, bowhead, and gray whales have bigger testes than predicted for body size suggesting sperm
competition
Humpback male tactics
•
•
Escort (accompany) females with calves
•
Singers may be a “floating lek”
Fight for access to females
– Males will wound one another, and there is a report of one killed in a “competitive group”
– Suggestion that males may cooperate to gain access to females
Mysticete Mating
•
Female mysticetes may exhibit choice in several ways
– Female southern right whales and bowheads may invert at the surface, increasing the difficulty for
males
– Humpback whale females have shown aggression towards attending males and may also be able to
choose based on song displays of males
Odontocete Mating
•
Sperm whales are different from other species that are well known
– Males move from high latitude feeding grounds to low latitude ranges of females during breeding
season
– Males rove among groups of females and swim with them for ~8 hrs and 2-4 large males may
accompany a female group over a period of days
– This “roving” strategy is expected based on probabilities of finding female groups and the duration
of estrus
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–
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Many species are probably promiscuous and sperm- or male-male competition are common features
Roving looking for receptive female probably most common tactic
Male-male competition suggested by sexual dimorphism and tooth rakes
– Many narwhal have scars from tusks or broken tips
– Eruptive teeth and scars in beaked whales
– Male sperm whales appear to delay reproduction substantially until they are big enough to compete
– Male coalitions may form (more later)
Female choice and false estrus
•
•
Role of female choice in cetacean mating still relatively unclear
•
•
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Females may successfully avoid males
Female bottlenose dolphins in Shark Bay exhibit multiple attractive periods that do not result in
copulations
– Function is apparently to obscure paternity to prevent infanticide
Unknown if female odontocetes test males abilities or incite competition
Promiscuity and sperm competition likely in numerous species
Social Structure and Behavior
Group living
•
Evolution of social behavior has been shaped by a number of factors
– Where they give birth
– Where they forage
– What they eat
– Predation risk
•
Level of sociality in marine mammals varies considerably among taxa and may vary with season as well
•
Benefits
– Reduced risk of predation through a variety of mechanisms
– Reduced risk of non-socially transmitted parasites (remember the cookie cutter shark)
– Cooperative foraging
– Increased access to food or space
– Reduced male harassment (e.g. southern sea lions)
•
Costs
– Parasite transmission
– Increased competition for limiting resources
Costs and benefits of groups
Marine mammal groups
•
Geographic vs Social Philopatry
– Unlike many mammals, both male and female marine mammals, especially odontocetes, may
remain in locations where their mothers are
– In male bottlenose dolphins, philopatry is geographic – they rarely interact with mothers
– Male killer whales exhibit both – the remain in natal areas and stay with natal group for life
– Land-breeding pinnipeds may show strong breeding-site fidelity but not necessarily family-based
interactions
Social relationships
•
Based on pattern of interactions between individuals over time
– Individuals have relationships with other individuals; the network of relationships results in a social
structure
•
Even “solitary” species have relationships
– Maybe aggressive interactions with individuals in adjacent territories
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Social bonds are relationships that include consistent affiliative component
– Bonds are a social tool for increasing reproductive success
– Bonds may vary with ecological conditions, age, sex, social position, and tactics of other individuals
•
•
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Multiple methods for determining how strong relationships are among individuals
Calculating Social relationships
Most based on the amount of time that individuals spend together versus the time they are seen apart
Half weight index is the most common
– Based on group surveys with individual identification
– Varies from 0 (never together) to 1 (always together)
– HWI+ 2*(# times individuals A and B seen together)/(# times indiv A seen + # times individual B
seen)
Affiliative behaviors
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Used to strengthen bonds, repair damaged ones, or reduce tension, or obtain needed service
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“Greeting ceremonies” when killer whale pods unite
Dolphins in Shark Bay (and other odontocetes)
– Petting, fin overlaps, rubbing
– Synchronous surfacing events
Affiliative behaviors reported in species without bonds
– Nuzzling in male manatees
– California sea lion males maintaining physical contact or prolonged side-by-side swimming
Aggression and agonistic displays
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•
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Wide variety of vocal and physical threats including growling, opening mouth, jerking heads, lunging,
and charging
Male California sea lions shake heads side to side vigorously while Steller’s males shake up and down
Pop vocalizations of male dolphins in Shark Bay
Jaw claps, bubble blowing also common
•
•
•
May escalate into physical conflicts of biting and ramming
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Non-conceptive sexual behavior common in birds and mammals
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T. aduncus in Shark Bay
– Many combinations observed, most common in immature individuals
– In adult males, may involve affiliate behaviors or dominance interactions depending on context
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Bonding in females related to calf protection and resource access
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Male odontocetes are rovers
– Should they rove alone or in groups?
• Varies with species from alone to roving with other males or their natal kin
Tusks and modified teeth (e.g. beaked whales) for combat
In many species, blows to the body are more lethal and fatalities occur with no external injuries
Sociosexual behavior
Reported from northern fur seals, manatees, right whales, and many odontocetes
– Some delphinids may rival bonobos
Odontocete bonding
Male bonding based on access to receptive females
Males should rove if the receptive period of females exceeds the time it takes for males to travel
between groups
Females bonded, males rove alone
•
Sperm whales
– Stable matrilineal groups of ~10 related individuals
– Matrilineal groups may be found with other groups for short periods of time
– Groups may split on temporal scale of 5-10 years
– Female bonds based on cooperative care of offspring that are poor divers and at high risk of
predation at the surface
– Dives staggered when calves present in group
– Can’t defend resource territories
– Males disperse to bachelor groups and become increasingly solitary as they get larger and roam to
high latitudes
• Need greater feeding opportunities to support mass
– Adult males may form loose associations without bonds while on breeding grounds
– Individuals rove between groups of females
– Social structure of sperm whales remarkably like that of elephants
Weaker female bonds, roving male alliances
•
Bottlenose dolphins (T. aduncus, T. truncatus)
– Fission-fusion society – individuals form small groups that change in size and composition
frequently
• Changes occur relative to behavior, location, and individuals present in a group
– Strong male-male bonds in Shark Bay and Sarasota
• Some male-male bonds as strong as mother-calf bonds
– Female bonds usually much weaker and variable
– Males in Shark Bay form pairs and trios (alliances) that cooperate to form consortships with females
that are often maintained with aggressive herding
– Some alliances may last over a decade while other alliances are very liable
• Second-order alliances occur among stable alliances that have more variable interactions
– Super-alliances in Shark Bay
• Stable at higher orders but less so in pair and trio formation
• Alliance stability within super-alliance correlated to female access
– In Sarasota, pairs occur but never trios
– In Moray Firth, Scotland there are no strong male bonds (very large body size)
– Female bonds in Shark Bay and Sarasota contain some individuals with moderately strong bonds
with several individuals – other females largely solitary
– Females maintain more of a social network with moderate and weak bonds than do males
– Social females in Sarasota form bands that may be female relatives or unrelated matrilines
– Associations among females may be related to reproductive state
– Juvenile dolphins tend to associate in groups
•
Bottlenose whales (Gowans et al. 2001)
– Ecological factors, body size, and feeding behavior would suggest similar social structure to sperm
whales
– Society is a fission-fusion society like bottlenose dolphins with longer-term male bonds and short
associations between females without preferential bonds apparent
– Deep-diving does not necessarily lead to strong female bonds and communal care of young
– Function of male bonds remains unclear – no observations of cooperation in mate acquisition
Roving with natal kin
•
Resident killer whales
– Individuals associate in pods and pods only associate with other pods of “community” despite range
overlaps of communities
– Within-pod units are matrilineal of 2-9 individuals and up to 4 generations that rarely spend more
than hours apart
– E.g. grandmother, adult son, adult daughter, offspring of daughter
– 1-11 units associate in sub-pods that temporarily travel apart from pods made of 103 sub-pods
– Social structure may be quite different from transients, but male transients may stay with mother
– Why do males stay with natal groups
– Male benefits to offspring of related females
–Assistance in hunting and teaching
–Cooperative foraging reported in fish-eaters in Norway and many mammal-eating populations but less
important in other populations of fish eaters
– Mother assistance to adult sons in reproduction
–Older mothers and adult sons noted traveling independent of other pod members
•
Long-finned pilot whales
– Genetic analyses of individuals captured in drive fisheries show that males don’t mate within natal
pods and also do not disperse
– Unclear if pilot whales in drive fisheries more like killer whale pods or communities
Ecological factors and bonding
•
Low cost of locomotion in odontocetes may be the reason for philopatry of both sexes which is rare in
terrestrial mammals
– Can pursue widely scattered resources over large ranges
– Day ranges much larger than terrestrial species
– Allows range to overlap ranges of many unrelated females
Bonding in other marine mammals
•
•
Generally not well known
Mysticetes generally thought of as solitary or with few social bonds beyond mothers and calves
– Groups of herring feeding humpback whales in SE Alaska appear to have strong bonds on feeding
grounds while krill-feeders do not
– Most humpbacks on feeding grounds show fission-fusion dynamics with small unstable groups
Culture
“Information acquired from members of the same species through some form of social learning which
causes similarities in behavior among members of a population or subpopulation” (Rendell and
Whitehead 2001)
Cetacean culture
•
Complex social systems (e.g. second-order alliances) and advanced cognitive abilities make cetaceans
strong candidates to exhibit culture
•
Within generation cultural exchange
– Male songs of humpback whales
– Lobtail feeding in humpback whales (slam flukes onto water before diving to use bubble clouds)
•
Mother-offspring similarity
– Strongly suggested when mother and offspring have similar, but characteristic patterns of complex
feeding behavior
– Sponge carrying in T. aduncus
– Feeding from humans by T. aduncus in Shark Bay
– Migratory routes of beluga and humpbacks
– Intentional stranding by killer whales
•
Group-specific behavior
– Must show that different groups face the same ecological conditions and traits are not genetically
inherited rather than learned
– Resident killer whale dialects
– Foraging tactics of killer whale groups
– Choice of rubbing locations by killer whales
– Sperm whale codas
– Sperm whale defense tactics???????
• Correlation between group and scarring rate on tail
– Dolphin cooperation with fishermen during foraging
Culture and conservation
•
Cultural transmission within generations may help animals deal with anthropogenic changes or even
exploit it (e.g. taking fish from longlines)
•
Cultures that are transmitted vertically between generations may have the opposite effect and impede
adaptation
– Reduce range recovery, confound reintroductions
– May lead to maladaptive behavior (cultural imperative to remain with a group may lead to
strandings)
•
Important in determining Evolutionarily significant units when culture divides populations into
subpopulations
Population Biology and Genetics
Abundance
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Understanding abundance of marine mammals key to understanding ecology
–
•
Pinnipeds (especially commercially exploited ones) best known
•
•
Taxa vary widely in abundances
Good estimates of abundance only available for a few species and usually only for a small number of
populations
Current estimates of most species are poor indicators of historical population levels and some are
increasing
High latitude pinnipeds tend to be more abundant (especially phocids) possibly due to productivity of
the systems
Estimating abundance
•
A census is a total count of the population at a particular time and place
– Rarely possible for marine mammals
– Pinnipeds during breeding (e.g. Sable Island)
– Resident killer whales off BC and WA
•
•
A sample is a count of a subset of the population
•
Catch-effort analysis
– Uncommon today but used during commercial hunting (CPUE)
•
Mark-recapture models
– Uses known (or marked individuals) and the proportion of later sightings (captures) that are marked
– Used for pinnipeds and cetaceans
– Particularly useful for populations where individuals return to the same area annually
– Hampered by tag loss or unreported (unobserved) individuals that return
•
A index estimates some statistic that is correlated with population size at a particular point in time
– e.g. gray whale numbers counted migrating up CA coast is thought to be a fixed portion of the
population
Methods to estimate abundance
Transect surveys
– Strip transects of fixed width
– No difference in sighting probability with distance from transect
– Line transects of theoretically infinite width
– Use frequency distribution of sighting probability with distance from transect
– Move along transect line on ship or by air, estimate distance to all individuals observed
Population structure
•
Most marine mammal species have multiple populations
– Interbreeding group of conspecifics that occur within a particular geographic area
•
Genetic exchange may occur among populations but probability of mating within population is much
higher
– There will be genetic differentiation among populations
•
•
Population structure influenced by
– Patterns of movement
– Distribution of suitable habitat
– History of exploitation
Methods to study population structure
Most common methods are tagging studies and analysis of morphological and genetic data
– Movements of individuals and presence of morphological or genetic differences help to define
extent of populations
– DNA analyses have been used to show differentiation not observed with other techniques
(morphology, enzymes)
Examples of how genetic data are used
– Differentiation of Atlantic walrus
– Differentiation of sea otter populations
– Genetic data show differences in humpback whales of the Atlantic and Pacific as well as structure in
the Pacific populations
•
Natoli et al (2004)
– Two forms of bottlenose dolphin – offshore and coastal
– Coastal forms have lower genetic variation and appear to be derived from coastal populations
– There may be a third Tursiops species in South Africa
Population dynamics
•
•
How and why do populations vary in abundance
•
Marine mammals generally k-selected making them vulnerable to exploitation and slow to rebound
– r = 0.01/year for sperm whales; 0.03 for AK bowheads; 0.031-0.144 for other mysticetes
– Pinnipeds may have r = 0.13-0.15 (Sable Island gray seals 0.13 from 1976-1990)
– Dugongs estimated to have max r = 0.063 and adult survivorship is most critical factor
– Note: doubling times of populations are 34.6 years for r = 0.02 and 4.6 for r = 0.15!
•
Estimating equilibrium population sizes and the factors that might influence them for marine mammals
has been difficult
•
•
•
K is likely to vary annually depending on the resources that are available
Knowing the age of animals is critical, but difficult in marine mammals
– Can count growth layer groups (GLGs) in teeth in many species and other ossified structures in
others
Understanding population dynamics
Many populations assumed or thought to be food-limited
Influence of predators and predation risk largely overlooked
– Even if predators don’t kill many individuals they may have an impact on population size – this may
occur for bottlenose dolphins in Shark Bay
•
Estimating historical abundance and current carrying capacity can be difficult and there is much
uncertainty in parameter estimates and catch statistics (unreported catches, whales killed but not
recovered)
Population genetics of impacted populations
•
Many marine mammals have experienced severe population depletion
– Recovery is limited by long generation times, low reproductive rates
– Often leads to genetic bottlenecks (loss of genetic diversity)
– Not all species have lost variation in face of population reduction
– Guadalupe fur seal, Juan Fernandez fur seal, sea otter
Bottleneck in northern elephant seals
•
•
•
In ~1829, only 10-30 individuals, but population has recovered to over 150,000
Low variation in mtDNA, allozymes, MHC, micro and minisatellite DNA
Based on genetic data, there were probably <20 individuals for 1 year or 20-30 individuals for 20 years
Bottleneck in Hawaiian monk seals
•
•
•
Almost extinct in 1890s, up to 3000 before 50% reduction in 1950s-1970s
Great loss of genetic diversity, but population appears to be recovering again
Possibly through inbreeding depression
Juan Fernandez Fur seals
•
•
•
•
Late 1600s: 4 million thought to be extinct in late 1800s
•
•
Less well known than pinnipeds
•
Vaquita has most restricted range and is depleted. There is almost no variation
– Founder effect or chronic low effective pop size?
•
Species with matriarchal societies tend to have reduced variation, but mechanism unclear
– Cultural selection, low effective pop size, etc
200 individuals found in 1965, now at 6000 and increasing at 15-20%/year
Genetic variation high
Possibly due to refuges on rock ledges and cliff edges so populations may not have been reduced as
much as once thought
Cetacean bottlenecks
Northern right whales probably <100 individuals and genetic variation reduced relative to other baleen
whales
Historical cetacean populations
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–
Amount of genetic variation in a small population can be used to estimate historical population size
Roman and Palumbi (2003) showed that whale populations in the North Atlantic were probably 3-10
times larger before exploitation than previously thought
– More genetic data could help to resolve exactly how much larger