T U R T L E S

1
TURTLES
Introduction, evolution, biodiversity, and
life-history.
2
Presentation Plan

• Two Wordy Slides on Life-History
  generalizations.
• (Further notes on life-history will be
  interwoven, and possible discussion questions
  will be indicated in red.)
• Evolutionary origins of turtles.
• Turtles shells.
• Respiration.
• Locomotion
• Terrestrial turtles.
• Marine turtles.
• Reproduction and demography.
• Phylogeny Family-by-Family review.

3
Boring Generalizations (mostly true!) about
Turtle Life Histories
All turtles reproduce sexually, and all lay
eggs. Typically, 1 clutch is laid per year, but
many species produce gt 1 clutch annually.
Species that multi-clutch often skip one or more
years between reproductive seasons. In most
species, gender is determined by incubation
temperatures (females are the hot gender), but
in a few it is determined genetically. Incubation
period varies greatly (lt 2mo - gt 1yr). A baby
turtle looks like a smaller adult, but underneath
its keratin scutes, its bony shell is not fully
developed. Hatchlings receive no care from their
parents though in 1-2 species a mother will guard
her nest of eggs. In some temperate species,
hatchlings over-winter in the nest. Compared to
most mammals, all baby turtles grow slowly in
some species sexual maturity is reached as early
as 2 years in others it may be delayed for gt 35.
Average may be 6-10 years.
4
More Generalizations
In all turtle species the young suffer heavy
mortality, and in all species adult mortality is
much lower (in some it is very, very much lower),
so all species produce some adults that live a
long time. In some species older turtles undergo
apparent senescence in other species they do not
in so far as we know). Maximum longevity in a
few species is known to exceed 100 years. Adult
turtles range in size from about 10cm (and lt
500g) to gt 2m (and gt 500kg). Some species eat
nothing but plants some eat nothing but animals
many are in between. In quite a few species the
diet changes with age, often becoming more nearly
vegetarian. In all species calcium is an
important nutrient, particularly for hatchlings
and for reproducing females. Turtles inhabit 6
of 7 continents and all warm oceans. The region
richest in species was S.E. Asia but is now S.E.
North America. Many turtle species are
endangered because their demographic patterns are
not conducive to sustained-yield exploitation by
people.
5
Evolutionary origins

• They appeared c. 230 million years before present
  (MYBP) as recognizable, fully-formed turtles.
• By 210 MYBP all major living ( many extinct)
  turtle lineages existed.
• Ancient turtles
• Some had teeth (no modern turtles do).
• None could fully withdraw head into shell.
• As we shall see (next slide), a debate about
  relationships persists
• Are turtles the earliest reptile (even earliest
  amniote) branch?
• Are they relatives of snakes and lizards?
• Or are they relatives of crocs and birds?

Earliest known turtle (Proganochelys) photo of
fossil artists rendition. (from
tolweb.org/tree)
6
Disputes about Evolutionary Connections(The
molecular dudes gonna save us all???)
Why do ideas on turtle phylogeny change so much?
7
Of course the shell makes the turtle!

• Shell is living tissue and therefore grows with
  turtle. (And most species have indeterminate
  growth.)
• To produce shell, a turtle needs much calcium,
  limited phosphorus, some Vitamin D, and plenty of
  sunlight.
• Topics for next shell-slides
• Positioning of girdles
• Embryological construction of the shell.
• Scute patterns.
• Further shell-based meditations.

Note how pectoral and pelvic girdles are within
the shell. Turtles are the only vertebrates that
can withdraw both head and legs into the shell.
8
Rib Vertebra

• Turtles are unique among vertebrates because
  their pectoral and pelvic girdles are within
  their rib cages.
• During embryological development the girdles do
  not move into the rib cage (though that's where
  their position ends up) instead, the developing
  ribs grow laterally to cover the girdles. (The
  next slide tells how.)

9
Morphogenesis of a turtles shell

• Early on, cells of the carapacial ridge (or CR,
  an ectodermal structure analogous to apical
  ectodermal ridge of developing limbs) express
  messenger proteins, which attract migrating
  rib-precursor cells.
• Thus the ribs (which are endochondral bone) are
  directed laterally by the CR, and they will
  complete their development outside of the
  girdles.
• The ribs also become signaling centers that
  tell dermal cells between them to build bone
  (i.e., they secrete morphogenetic proteins that
  signal ossification).
• The cooptation of an existing (Wnt) signaling
  pathway allowed for rapid evolution of the
  carapace.

Above Cross-sections of turtle embryo from
Burke, Amer. Zool., 1991
Expanding edge of CR
10
Scutes the external covering
Names of scutes

• In most turtles the bony shell is covered with
  horn-like, keratinous epidermal scales called
  scutes. Typically a thin layer of skin lies
  between the bone and the scutes.
• The scutes have a different pattern from the bone
  segments that underlie them, and this non-overlap
  of sutures adds to the strength of turtles
  shells.
• Relative plastral scute suture-lengths can often
  be helpful in identifying a species
• Anal gt Abdominal gtGular gt Pectoral gtFemoral
  gt Humeral is the pattern on the plastron at
  left.

From theturtlepages.crosswinds.net
11
Further meditations on the shell

• Nothing else has a shell like a turtle!
• Because the shell is so bulky, there are some
  evolutionary pathways closed to turtles.
• But bulkiness does have advantages
• Size and herbivory
• Size and reproduction (more on reproduction
  later)
• Size and longevity
• Soon well discuss the shell and its relationship
  to turtle respiration. In our research well tie
  this in with thermoregulation.

12
Turtle respiration

• Gas exchange is mostly by lungs, but also
  consider
• blood-buffering against CO2
• myoglobin for additional oxygen storage
• tolerance of lactic acid
• reduction of metabolism
• (in a few species) non-lung surfaces of gas
  exchange
• Breathing per se (next slide)
• A turtle cant move its ribs or expand its chest
  cavity!
• Muscles and viscera act as a pump by pressing on
  lungs.
• Moving the pectoral girdle also pumps air.

13
Breathing

• Exhalation. Contraction of transverse abdominus
  draws posterior limiting membrane up forward
  while contraction of pectoralis draws pectoral
  girdle posteriorly. These actions press visceral
  mass against lungs, forcing air out.
• Inhalation. Contraction of abdominal oblique
  pulls posterior limiting membrane down and back
  contraction of serratus moves pectoral girdle
  forward. These actions (plus gravity) move
  visceral mass to increase lung volume air comes
  in.
• The exact arrangement of these structures varies
  from species to species.

14
Locomotion

• On land, turtles gait (next slide) is ponderous,
  but even terrestrial turtles can move a long way
  if you give them enough time.
• Marine turtles are the swiftest of all living
  reptiles (next slide plus one), and some make
  truly prodigious journeys. (See leatherback
  turtle slide, far below.)
• Turtle feet were once used extensively in turtle
  taxonomy. But feet are under heavy selective
  pressure from environment and are therefore
  liable to convergence.

15
Plodding Terrestrial Locomotion

• The red lines connect feet touching substrate.
• The blue blobs indicate the center of gravity.
  (In 3 7, the body is supported only by diagonal
  limbs as C.G. shifts.)
• Note the broad triangles of support.

16
Locomotion in marine turtles

• The hydrodynamic forces are shown as if they
  were acting on the center of the hydrofoil. The
  passage of the hydrofoil elicits a hydrodynamic
  reaction force (R), which can be resolved into a
  force acting in the direction opposite to the
  motion at that point, which is drag (D), and a
  force at right angles to D, which is lift (L).
  Lift is inclined forward, indicating that there
  is a forward propulsive component to its action.
  Pough et al., 2001

Cross-section of propulsive ( front!) limb.
Note that its more like flying than like
swimming.
17
Generalities of turtle reproduction

• All turtles lay eggs with
• 4 extra-embryonic membranes (reptiles, birds,
  mammals)
• Highly calcified shells (some are brittle, some
  leathery).
• Most (not all) turtle species have
  temperature-dependent sex determination.
• Some species can lay gt 1 clutch in a single
  season some species skip a year (or more)
  between clutches.
• Mortality is usually high among eggs and baby
  turtles.
• Most turtles mature quite slowlybut typically
  live a very long time if they reach adulthood.
  This general demographic pattern has important
  conservation implications! (See next slide.)

18
Conservation implications of turtle
demography(or, in the old days most wildlife
managers were trained to be deer biologists)

• White-Tail Deer
• First-year survival probably c. 25-50.
• Sexual maturity is possible _at_ lt 1 year.
• So, about a quarter to half of all fauns mature.
• Longevity after maturity is typically 1-4 years.
• So each adult is not worth a whole lot,
  demographically.

• More or less typical turtle
• First-year survival can be lt 1 juvenile
  survival is generally low too.
• Sexual maturity is usually _at_ about 5-15 years
  (sometimes much later).
• So, typically, about 0.1 - 10 of hatchlings
  mature.
• Longevity after maturity is probably 10-75 years.
• So each adult is worth a whole lot,
  demographically!

19
Phylogeny of the turtles

• Turtles appear about 230MYBP w/developed shell
  thereafter undergo few other obvious changes.
• During the Triassic (before 210MYBP) turtles had
  split into 2 main branches, distinguished today
  by head-withdrawal mechanisms (see next slide)
• vertical-plane head withdrawal (hidden-neck)
  turtles today abundant on all warm continents
  except Australia (mechanism developed by
  200MYBP).
• horizontal-plane head withdrawal (side-neck)
  turtles today found in Africa, Madagascar, South
  America, and Australia (mechanism developed by
  about 135MYBP).

20
Head-withdrawal mechanisms

• Top neck bent in horizontal plane to withdraw
  head (Pleurodira, side-necks).
• 3 Families
• Africa, Madagascar, South America, and Australia
• Bottom neck bent in vertical plane to withdraw
  head. (Cryptodira hidden-necks).
• 10 Families
• All warm oceans and all warm continents (marginal
  in Australia).

http//research.amnh.org/esg/
21
Possible relationship of turtle families
22
SIDENECKS 1 Chelidae,The snake-neck Family

• 11 genera and about 40 species, in South America
  and Australia. (On anatomical grounds, South
  American and Australian species appear closely
  related, but some molecular data suggest
  otherwise.)
• The Family includes some species with moderately
  long necks and some with very long necks.
• Longnecks usually are ambush predators lying on
  shallow bottom, they raise heads for occasional
  breaths. And they snatch passing fish.
• Shorter-necked (still pretty long!) types are
  usually mobile predators and scavengers.
• Australian types have been well studied (South
  American types less so).

23
Chelidae (a snake-necked sideneck)

• Commonly called mata-mata.
• Carapace length to c. 50cm.
• Mata-matas inhabit the ponds and slow streams of
  South American tropics.
• A well camouflaged ambush predator, the mata-mata
  is an aquatic implosion feeder on small fish and
  invertebrates.
• Occasionally mata-matas are active foragers,
  sometimes herding fish into shallow water.

Chelus fimbriatus
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A more typical snakeneckof the very-long-neck
persuasion
Chelodina expansa

• Longnecks are Australian. Many types are
  drought-resistant, some surviving without water
  for gt 2 years. Most are ambush predators.

25
SIDENECKS 2 shortnecks

• Two Families
• Pelomedusidae (Africa and Madagascar)
• Podocnemidae (South America and Madagascar)
• Pelomedusids are small-to-medium, mud-turtle
  convergents. Brown to dark brown, they are oval
  and nondescript.
• Podocnemids are river turtles, often large. They
  resemble familiar pond turtles. Often
  podocnemids are heavily exploited and endangered.
  Some species are of great potential economic
  value.

26
Pelomedusidae

• 2 genera, about 18 species.
• These small to medium-sized turtles are
  omnivorous, but most prefer animal food.
• Crocodiles constrain the distribution of some
  species consider selective pressures to inhabit
  ephemeral waters (such as isolated ponds) or to
  evolve high-domed shells.
• Many of these turtles are adapted to a wet-dry
  seasonal environment and survive droughts well.

Pelomedusa subrufa
27
Podocnemidae

• This Family was formerly lumped with the
  Pelomedusidae.
• Podocnemids include 3 genera and 8 species.
• The Malagasy species are not well known.

Podocnemisunifilis
28
Podocnemis expansa An important South American
turtle

• Very large females can weigh almost 100kg. (An
  extinct relative, Stupendemys, approached 3.5m
  long it might have weighed 2000kg and was
  probably the largest turtle ever.)
• Colonial nester (48 million eggs were taken from
  one Amazonian beach during one year in the early
  20th century).
• P. expansa is legally protected, but it plays
  important cultural roles in South American
  society, so many are still eaten.
• If conserved, this species could be a renewable
  source of protein in a hungry world. (Should the
  eggs or the adults be exploited?)

29
Sea Turtles Cheloniidae

• 5 genera, 6-7 species.
• All warm oceans, w/1 species often extending into
  temperate zone.
• The front legs are the primary swimming
  structures.
• Females return to their natal beaches to nest.
• All except green turtle (Chelonia mydas, left)
  are animal eaters.
• Green turtle demographics
• Prob(egg?adult) ? 0.0005
• Prob(adult lives another year) ? 0.8
• Lays c. 300 eggs, 1 out of 2-3yrs.
• These are the published figures can you do the
  math to see if all can be correct?

Chelonia mydas
30
More on green turtles(and see next slide for
even more)

• Green turtle females return from distant foraging
  areas to particular nesting beaches.
• Hatchlings become pelagic and remain at sea until
  they are about 20-30cm.
• Then as juveniles they return to shallower
  waters, where they feed on sea-grass beds.
• Maturation time is not well understood and may
  vary enormously.

Older juvenile foraging in shallow water
31
Sea turtles oceanic navigation

• Most sea turtles apparently have sun-compasses
  that interface with time-keeping mechanisms.
  (Displacement experiment Turtles orient, at
  least initially, as if they were in their
  original area.)
• Most sea turtles apparently have magnetic
  compasses. (Magnetic-field reversal experiment
  Turtles at least initially reverse direction of
  movement.)
• But eventually at least some sea turtles can
  navigate successfully when either system fails to
  function. (See below for results of an
  experiment that involved disruption of magnetic
  compass).

32
Life-cycle of green turtles (Chelonia mydas)
Big questions coming turtles and longevity?
33
How can some turtles live such a long time?

• Of course turtles often die quite young.
• And adults succumb to
• Depredation, accidents, disease
• External, erosive, wearing-out
• Senescence (internal wearing out) in some
  species.
• Still, large adults of some turtle varieties can
  live a very, very long time.
• As we think about why, lets consider 3 (not
  mutually exclusive) forms of senescence
• An internal decay of genetic instructions so that
  when some older cells divide they lose constraint
  (cancers, etc)
• An accumulation over evolutionary time of
  mutations that adversely impact older adults
• Selective pressures for genes that favor survival
  of young but reduce survival probabilities of
  older individuals (antagonistic pleiotrophy).

In many cultures turtles are symbols of longevity.
34
Chromosome stability and telomere length
Contrasting mammals vs. long-lived reptiles
Why?????
35
Senescence as failure to purge genes that have
deleterious effects in later life
Lineage commitments to life-history strategies
affect selective pressures.

• Assume that
• Mastomys natalensis has physiological capacity to
  live 8yrs.
• M. natalensis matures at 4mo., and 99.99 die of
  extrinsic causes before 6yrs.
• Mutation O reduces maximum longevity by 25.
• Selective pressure to purge a population of
  Mutation O would be minimal!

• Assume that
• Gopherus polyphemus has physiological capacity to
  live 60yrs.
• G. polyphemus matures at 15yrs., and annual
  survival thereafter is gt 95.
• Mutation ? reduces maximum longevity by 25.
• Selective pressure to purge a population of
  Mutation ? would be substantial.

36
Selection genes that work antagonistically with
age

• Lets invent a turtle-gene that substantially
  increases the rates of calcium uptake and
  deposition.
• Juveniles would grow shells faster, avoid
  predators better, and reach reproductive maturity
  sooner.
• Older adults would experience earlier
  calcification of connective tissue in artery
  walls and die younger.
• What sorts of turtles (with what sorts of life
  histories under what ecological conditions) would
  you expect to express such a gene?

37
The evolutionary choice that constrains the
life-history strategy of many turtles

• The basic turtle plan is to accept all
  demographic developmental costs of producing a
  very long-lived adult biotype.
• This semester we want you to think about
• What macro-evolutionary event is most closely
  associated with this life-history strategy? Why?
• How does this event elicit a cascade of
  life-history consequences?
• How does this tie in with thermoregulation and
  ecology? (I.e., why are there no truly
  turtle-like mammals?)

38
(But wait Turtles are more wonderful than
theories!)Dermochelyidae (leatherback)

• Maximum size gt 2m (1000kg) usually 1.5m.
• Operates 22.6m down in water columnand in cold
  water (TB25.5 _at_ TE 7.5).
• What about temperature?
• Mammal-type metabolism?
• Inhabits an eco-niche that is unavailable to
  other marine turtles the leatherbacks major
  food is jellyfish.
• How does it get enough?
• How does it deal with the salt (jellyfish are
  approximately iso-osmotic to seawater, which has
  3X osmo-concentration of turtles somatic
  tissue)?
• Can it avoid plastic bags?
• Physiological ecology of this animal needs study.

39
More on leatherbacks

• Large size, dark color, counter-current exchange,
  insulation, enormous food intake, blood-shunting,
  constant activity Scaled for size, leatherback
  metabolism is intermediate between reptile
  mammal. (Convergent w/ Scombroidei.)
• Growth rate is mammalian Leatherbacks can
  approach maturity in 2 yrs (10-20k size
  increase!).

40

• Leatherbacks (Dermochelys coriacea) make
  enormously long oceanic circuits.
• Probably much transport is by riding currents,
  but these turtles swim almost constantly and
  sometimes progress sub-surface.
• Movement patterns resemble those of whales
  subsisting on similar foods.

41
Carettochelyidae New Guinea Pig-Nosed Turtle (1
genus, 1 species)

• Length to 70cm.
• Front limbs are hydrofoils. Note convergence
  with sea turtles.
• Beneath the soft, pitted skin, the bony shell is
  heavy and complete. This is unlike the
  softshells, so does the leathery covering reflect
  shared evolutionary lineage or convergence?

42
Carettochelyidae (Carettochelys insculpta)

• Adults are largely vegetarian young eat more
  animal food.
• Fully developed embryos remain dormant in shells
  until nest floods (at least in Australia).
• 40MYBP the Family included far more species and
  was distributed across all the northern
  continents.
• Note snorkel-type snout and think about softshell
  turtles (next slides) again, does this reflect
  convergence or relationship?

43
Trionychidae (softshells)

• About 14 genera, about 25 species.
• Reduced-bone shells are covered with leathery
  skin, which allows significant gas-exchange.
• Softshells have long necks, snorkel snouts, and
  fleshy lips.
• Trionychids are fast, streamlined swimmers, but
  their webbed limbs are paddles, not hydrofoils.

Pictures are Pelodiscus sinensis.
44
Softshells(Trionyx spinifera is shown below.)

• Large number of eggs (gt 200/yr for big Florida
  softshells) gender determination is genetic.
• Eat any available animal of right size snails
  are often a favorite.
• Florida populations heavily exploited for Asian
  meat trade.
• Females are much bigger than males maximum sizes
  and longevity are poorly known.

45
Dermatemydidae(Central American mud or river
turtle)

• 1 genus, 1 species (though this is an ancient
  Family, once widely spread).
• Entirely aquatic, Dermatemys inhabits sluggish
  waters in southern Mexico and Central America.
• While underwater, most gas exchange is through
  the lining of mouth. (In lab conditions, these
  turtles constantly take water in through the
  mouth and expel it through the nostrils.)

46
Dermatemydidae(Dermatemys mawii)

• Large (to c. 75cm).
• Babies eat mostly animals adults eat mostly
  plants. (This is a common pattern among aquatic
  turtles.)
• Adults rarely leave water except to lay eggs.
• Throughout their range, these large river turtles
  are heavily exploited for food.

47
Kinosternidae (Mud and musk turtles)

• About 4 genera and perhaps 30 species, mostly
  Mexican (but into U.S. South America).
• All forage mostly by bottom-walking, but
• Kinosternon moves a lot on land, from water to
  water.
• Sternotherus seldom ventures onto land.
• The highly aquatic Central American Claudius
  Saurotypus are sometimes listed as a separate
  Family.

48
Musk Mud Turtles(Kinosternidae)

• The non-descript mud and musk turtles are
  typically small, oval, and light to dark brown.
• Most species tend to be omnivorous.
• Kinosternids usually lay few eggs at a time and
  produce multiple clutches.
• Adults live several years but do display
  senescence.
• The plastron is reduced and/or hinged.
• This allows for larger heads that can take larger
  prey.
• And keeping your mouth open while your head is in
  the shell makes for better defense.

49
Platysternidae (big-headed turtle)

• 1 species s. China n. S.E. Asia into southern
  Myanmar.
• Its relationship to snappers is unclear, and the
  big-headed turtle is often included in the
  Chelydridae.
• 15-18cm carapace.
• Long tail very large head.

50
Platysternidae(Platysternon megacephalum)

• This species inhabits rocky, cool (12o -17oC),
  mountain streams.
• It is active at night buried in stream gravel by
  day.
• Big-headed turtles eat animals, mostly snails but
  also other invertebrates and some vertebrates.
• The species may hunt on land as well as in water.
• Platysternon climbs well (for a turtle).

51
Chelydridae (snapping turtles)

• 2 genera and 2 species (Family once more
  widespread).
• Big head, reduced plastron opens mouth w/ head
  withdrawn.
• Snappers are in part implosion-feeders.
• Carapace scutes overlap.
• These animals tend to walk the bottom (as opposed
  to swimming).

52
Chelydridae (snappers)

• Common snapper is an active forager any
  freshwater habitat to c. 25kg.
• Alligator snapper (see left) is a luring ambush
  predator (can stalk) deep rivers weight can
  exceed 125kg.
• Both kinds eat almost any animal they can catch,
  but some recent research suggests that they eat a
  good bit of vegetable matter too.

53
Emydidae (Euro-American pond turtles)

• C. 12 genera and 40 species.
• These are the best-known American turtles.
• Small to medium large (12-60cm), mostly aquatic.
• Young are mostly carnivorous adults largely
  herbivorous.
• Aquatic emydids have stereotypical courtship.
• Demography not in general well known, but many
  live for a very long time.
• Many taxonomic issues remain unresolved.

Trachemys scripta
54
Bataguridae (Asian pond turtles)

• About 23 genera and 65 species.
• Relationships entangled w/ emydids (which they
  resemble ecologically) w/ testudinids (which
  are relatives).
• Mostly S.E. Asian but also south Asian spotty
  elsewhere (e.g., Rhinoclemmys in Central America).

Pyxidea mouhotii
55
Bataguridae (Example below is Heosemys silvatica
of s.w. India)

• Most species herbivorous or omnivorous (except
  probably babies).
• Most life histories very poorly known (but all
  probably live long).
• Severe conservation crisis in Southeast Asia is
  worth extensive discussion.
• Human population increase and ecological
  destruction in Southeast Asia
• Economic development of China.

56
Testudinidae (tortoises)

• Terrestrial elephantine hind feet mostly
  high-domed mostly lightened shells. (Pancake
  tortoises are flat, thin, and flexible.)
• Distributional epicenters are Africa
  Madagascar.
• Tortoises are the most vocal of all turtles.
• Many types very slow to mature adults may live
  very long conservation problems.

57
Burmese mountain tortoise

• This is probably the most primitive of all
  tortoises.
• Unique among turtles, it builds and guards an
  above-ground nest.
• Its conservation status is representative of
  S.E.A. turtles plight.
• This concludes our turtles PPT. But keep
  tortoises in mind! They are advanced herbivores,
  and the difficult job of plant-eating is a major
  concern of ecology, a sub-discipline of biology
  that will underlie all our semesters topics.