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Anachronistic fruits and the ghosts who haunt them

Authors:

Abstract

BARLOW WRITES: "Arnoldia editor Peter del Tredici asked me to write this article, which focuses far more on the fruit characteristics and paleohistory of genus Torrreya than does the 2004 paper by Barlow and Martin, which is the most cited. The last section of this article, pages 19-21, present an exclusive focus on torreya." EXCERPTS: "... The proximate cause of Torreya taxifoha's imminent extinction, and thus the cause that gets all the attention, is disease. Some thirty pathogens are known to infest it, but no single disease seems to be the culprit.... The genus Torreya was once distributed throughout the Northern Hemisphere. Range fragmentation has created distinct species in eastern China, patches of the Coast Range and the Sierras of California, and the Apalachicola of Florida. During the coldest times of the Pleistocene, the Apalachicola, with its moderate climate and rich soils, was a refuge for the trees and forbs that now enrich the Cove Hardwood forest of Great Smoky Mountains National Park, 375 miles (600 km) to the north. After the ice retreated, most of the plants hitched rides from wind and animals and moved back north to their pre-glacial home. Torreya seems to have been left behind.... Global or regional extinction of an animal partner (or partners) may be the root cause of the tree's current distress. Torreya is probably not ideally suited for the warmth and humidity of today's Apalachicola region. It wants to head north, but it hasn’t found a vehicle....
Anachronistic
Fruits
and
the
Ghosts
Who
Haunt
Them
Connie
Barlow
hirteen
thousand
years
ago,
the
Age
of
Great
Mammals
came
crashing
to
a
close
in
the
Western
Hemi-
sphere.
Lost
were
the
giants
of
the
elephant
clan:
the
mammoths,
mastodons,
and
gomphotheres,
which
had
maintained
a
presence
in
North
America
for
twenty
mil-
lion
years.
The
native
horses,
a
tall
camel,
and
all
but
one
species
of
pronghorn-each
group
from
a
lineage
thought
to
have
originated
in
North
America-vanished
from
the
plains.
Gone,
too,
were
the
strange
beasts
that
had
evolved
in
South
America
during
millions
of
years
of
con-
tinental
isolation:
ground
sloths
as
massive
as
elephants,
hippo-like
toxodons,
and
lumbering,
spike-tailed
glyptodonts,
which
looked
uncan-
nily
like
the
ankylosaurs
that
had
shared
the
Cretaceous
landscape
with
T.
rex.
These
large
herbivores
(along
with
the
biggest
bear,
the
biggest
canid,
and
several
big
cats,
all
of
which
depended
upon
the
plant
eaters)
disap-
peared
in
a
geological
instant.
Evidence
is
mounting
that
newly
arrived
humans
with
for-
midable
stone-tipped
spears
of
Clovis
design
were
to
blame.’
This
"extinction
of
the
mas-
sive"
that
marks
the
end
of
the
Pleistocene
epoch
ravaged
the
megafauna.
What
happened
to
the
plants?
We
cannot
be
sure.
Leaves
and
flowers
and
seeds
are
not
preserved
as
readily
as
bone.
Plant
lineages
restricted
to
upland
habitats
may
come
and
go
without
a
trace.
Bogs
and
lakes,
of
course,
receive
a
shower
of
pollen,
often
from
vast
distances.
But
detectable
quantities
of
pol-
len
preserved
in
sediments
are
restricted
to
wind-pollinated
plants-notably,
grasses,
coni-
Reumted:
osage
orange
and
mastodon.
Shown
here
is
surely
the
first
time
m
thirteen
thousand
years
that
the
fruit
of
osage
orange,
Maclura
pomifera,
has
touched
a
molar
of
its
missmg
partner
in
evolutlon,
Mammut
amencanum.
fers,
and
many
deciduous
trees
of
our
temperate
forests. (And
of
these,
some
produce
pollen
that
can
be
distinguished
only
at
the
genus
or
even
family
level.)
Indeed,
fossil
pollen
from
strati-
fied
bog
and
lake
sediments
is
the
primary
evi-
dence
used
to
reconstruct
the
vegetational
shifts
that
accompanied
the
repeated
coolings
and
warmings
of
the
Pleistocene
epoch.
The
Pleistocene
pollen
record
shows
only
one
tree
extinction
(a
species
of
spruce)
in
North
America
near
the
end
of
the
epoch.z
Is
there
rea-
son
to
suspect
that
plants
pollinated
by
insects,
birds,
or
bats-that
is,
plants
with
little
or
no
pollen
record-might
have
been
more
vulner-
able
to
extinction?
The
answer
is
yes,
but
vulnerability
to
extinc-
tion
in
this
case
has
nothing
to
do
with
the
mode
of
pollination.
Many
plants
that
are
pollinated
by
animals
rather
than
by
wind
produce
fleshy
fruits
whose
seeds
are
dispersed
by
other, larger
ani-
mals.
Plants
dependent
on
megafauna
for
dis-
persal
would
indeed
have
been
vulnerable
to
range
reduction
or
even
outright
extinction
when
their
partners
in
evolution
and
ecology
vamshed.
15
s
Riddle
of
the
Rotting
Fruit
Ecologist
Dan
Janzen
speculates
that
although
fossil
evidence
is
lacking,
some
fruit-bearing
plants
probably
did
follow
the
megafauna
into
extinction.
These
plants
would
have
begun
to
decline
when
their
megafaunal
seed
dispersers
vanished.
Some
might
have
gone
extinct
rela-
tively
soon
after
losing
their
partners.
Others,
especially
the
long-lived
and
those
that
regener-
ate
clonally
from
their
roots
as
well
as
from
seed,
still
survive
but
may
ultimately
be
on
track
for
extinction.
Still
others
have
been
regenerated
as
domesticated
cultivars
by
humans
fond
of
their
fruit
or
other
botanical
qualities.
But
by
and
large
Janzen
thinks
that
those
that
are
still
here
today
suffered
signifi-
cant
reductions
in
range
when
important
mem-
bers
of
their
disperser
guilds
were
extinguished.
The
narrowly
restricted
ranges
of
some
of
today’s
big-fruited
plants
suggest
that
Janzen
may
be
right:
plant
extinctions
may,
in
fact,
have
stemmed
from
the
animal
extinc-
tions.
An
indicator
that
something
is
amiss
is
evident
in
the
case
of
trees
whose
fleshy
fruits
fall
and
rot
beneath
the
canopy
of
the
parent.
It
was
this
"riddle
of
the
rotting
fruit"
that
cap-
tured
Janzen’s
attention
twenty-five
years
ago
while
he
was
studying
the
ecology
of
Costa
Rican
plants.
It
made
no
sense
for
plants
to
waste
energy
by
building
pulp
that
attracted
few
if
any
dispersers.
Worse,
in
the
case
of
many
fleshy
fruits,
when
the
pulp
rots,
the
embedded
seeds
are
killed
as
well.
What
was
going
on
here?
In
1982
Dan
Janzen,
with
paleoecolo-
gist
Paul
Martin,
published
a
paper
in
the
journal
Science
titled
"Neotropical
Anachronisms:
The
Fruits
the
Gomphotheres
Ate."’
Janzen
had
car-
ried
out
field
studies
in
Costa
Rica
to
learn
whether
introduced
livestock
(horses
and
cattle)
served
as
surrogate
Pleistocene
megafauna
for
the
bereft
plants.
The
result:
a
list
of
some
thirty
species
of
trees
and
vines
of
the
Costa
Rican
dry
forest
whose
fruits
bear
the
physical
and
ecological
characteristics
of
"ecological
anachronisms."’
These
plants
are
living
in
a
time
warp;
they
are
adapted
for
a
lost
world.
Their
missing
animal
partners
are
"the
ghosts
of
evolution."
Anachronisms
and
ghosts
caught
the
early
attention
of
Robert
E.
Cook,
who
is
the
director
of
the
Arnold
Arboretum.
Citing
Janzen
and
Martin,
Cook
published
an
essay
in
1982
in
Natural
History
that
described
the
avocado,
Persea
americana,
as
an
ecological
anachromsm
that
has
been
stunningly
successful
in
attract-
ing
a
replacement
dispersal
agent:
us.~
Within
the
past
few
hundred
years,
avocado
has
been
taken
from
the
New
World
tropics
to
orchards
in
Florida,
California,
northern
Mexico,
and
far
beyond
this
hemisphere.
Wild
elephants
who
raid
village
fruit
trees
in
Africa
are
now
"plant-
ing"
American
avocado
on
that
continent.’
In
their
landmark
paper,
Dan
Janzen
and
Paul
Martin
concentrated
on
Costa
Rican
plants.
But
in
the
final
paragraph
they
extrapolated
the
anachronism
concept
to
large-fruited
plants
of
Strategies
of
the
megafaunal
dispersal
syndrome.
Domesticated
vaneties
of
three
tropical
fruits
native
to
the
New
World
demonstrate
a
range
of
pulp
attractions
and
seed
defenses
Ripe
papaya
frmt,
Canca
papaya,
is
soft
enough
to
mash
rather
than
chew,
so
the
tmy
seeds
require
no
physical
protection
A
mammal
that
madvertently
crushes
a
papaya
seed
is,
however,
deterred
by
a
sharp,
peppery
flavor-and
thus
the
toxms
so
signaled.
Pmmate
fruit
thieves
(hke
us)
can
eat
around
and
discard
the
concentration
of
seeds,
thus
foiling
the
papaya’s
’s
mtent
Avocado,
Persea
americana,
produces
a
shppery
and
dense
seed,
whose
potent
toxms
taste
bitter
to
mammals
In
contrast,
the
seeds
of
the
camstel
tree,
Poutena
campechmana,
have
a
mild
flavor
and
are
protected
mstead
by
a
tough
coatmg.
All
but
the
biggest
frugmores
could
be
expected
to
eat
around
or
spit
the
seeds
of
avocado
and
camstel
16 6
Honey
locust
and
her
new
partner
m
evolution.
Strung
along
the
top
are
the
usual
number
of
seeds
m
a
honey
locust
pod,
such
as
the
one
restmg
on
the
author’s
arm.
The
most
anachromstic
legume
m
North
Amemca.
The
mpe
pod
of
kentucky
coffee
tree
is
toughened
byresms,
and
the
seeds
are
mvulnerable
to
msect
attack
The
green
pulp
is
sweet
but
reputedly
poisonous
to
humans
Early
colomsts
m
Kentucky
roasted
and
ground
the
seeds
to
make
a
coffeehke
brew.
The
ground
"cof fee"
shown
here
is
courtesy
of
Carl
Mehling.
the
eastern
and
central
United
States:
kentucky
coffee
tree
(Gymnocladus
dioicusJ,
honey
locust
(Gleditsia
triacanthos),
pawpaw
(Asimina
triloba),
persimmon
(Diospyros
virginiana),
and
osage
orange
(Maclura
pomi fera).
).
To
a
plant
lover,
the
notion
that
ghosts
may
be
haunting
some
of
the
most
magnificent
native
fruits
of
one’s
homeland
is
a
revelation.
It
was
quite
a
surprise,
therefore,
when
I
began
the
library
research
four
years
ago
for
my
book
The
Ghosts
of
Evolution
(2001)
to
discover
that
vir-
tually
no
effort
had
been
made
to
test
these
five
temperate
plants
or
to
identify
other
possible
anachronisms
in
the
forests
and
fields
of
North
America.
Indeed,
scientists
currently
breeding
honey
locust
trees
to
increase
the
fodder
value
of
their
pods,
and
those
developing
improved
pawpaw
cultivars
and
promoting
the
use
of
their
fruit,
have
been
doing
so
unaware
that
the
fruits
are
anachronistic.
Osage
Orange-An
Extreme
Anachronism
Recently,
I
spoke
with
an
archeologist,
Frank
Schambach,
who
felt
frustrated
because
nowhere
in
the
published
lit-
erature
could
he
find
the
information
he needed
to
solve
the
ecological
puzzle
of
osage
orange-information
crucial
for
validating
his thesis
that
before
set-
tlers
began
rearranging
the
landscape,
the
wood
of
this
tree, highly
valued
for
making
hunting
bows,
may
have
been
traded
far
and wide
in
North
America
under
the
complete
control
of
a
single
indigenous
tribe.8
Schambach
suspected
that
osage
orange
(also
known
as
bois
d’arc,
"wood
of
the
bow")
occupied
a
very
constricted
range
that
could
in
fact
be
claimed
by
a
single
tribe.
Osage
orange
would
more
appropri-
ately
have been
named
osage
breadfruit.
A
close
relative
to
Maclura,
of
America,
and
to
its
sister
genus
Cudrama,
of
eastern
Asia,
is
the
breadfruit
genus,
Artocarpus.
All
are
linked
through
the
mulberry
family,
a
largely
tropical
family
dominated
by
the
figs
and
striking
for
its
members’
compound
fruits
and
the
white
latex
some
exude
when
cut.
Osage
orange
was
named
after
the
Osage
Indians
of
Missouri,
who
first
introduced
white
traders
to
this
strange
fruit-the
color
of
a
glow-
green
tennis
ball
and
about
the
size
and
firm-
ness
of
a
softball.
Inhabitants
of
the
plains
and
prairie
states
know
this
fruit
by
another
name:
hedge
apple.
Until
the
invention
of
barbed
wire
in
1874,
there
was
no
more
effective
or
economical
way
to
fence
free-ranging
livestock
out
of
one’s
veg-
etable
garden
or
cornfield
than
to
plant
a
hedge
of
thorny
osage
orange
stems,
later
interweav-
17
7
An
elephant
fruit
m
a
land
without
elephants
The
bnght
green
fruit
of
osage
orange
was
shaped
by
the
now
extinct
megafauna
of
North
Amenca.
ing
the
abundant
root
suckers
that
the
trees
send
up
in
response
to
severe
pruning.
Thus
osage
orange
gained
a
replacement
dispersal
agent,
and
its
range
expanded
rapidly.
Maclura
pomlfera,
a
wind-pollinated
tree,
is
known
from
pollen
samples
to
have
been
wide
rangmg
in
North
America
during
earlier
ice-free
phases
of
Cenozoic
history.
But
by
the
time
of
European
contact,
its
range
had
shrunk
consid-
erably : just
before
its
transformation
into
a
com-
mon
hedge
plant,
it
inhabited
only
a
small
stretch
of
the
Red
River
watershed
near
the
junction
of
Texas,
Oklahoma,
and
Arkansas.
Frank
Schambach
suspects
that
at
its
nadir
the
range
was
even
more
restricted-possibly
limited
to
the
Bois
d’Arc
tributary
of
the
Red
River
in
Texas
and
nearby
creeks
of
the
adjacent
Blackland
Prairie.
Such
isolation
would
explam
how
a
single
tribe-the
Spiroans
of
Mississipian
culture-could
have
controlled
the
entire
bow
wood
trade.
And
this,
in
turn,
would
explain
the
archeological
evidence
of
extraordinary
wealth
accumulated
by
this
people
in
the
centuries
prior
to
European
contact.
What
ecological
information
did
Schambach
need
to
solve
his
archeological
puzzle?
He
wanted
to
know
whether
horses
spread
osage
orange-that
is,
do
horses
eat
the
fruit
and
defecate
viable
seeds?
If
so,
then
by
the
time
naturalists
got
around
to
documentmg
the
geo-
graphic
reach
of
osage
orange,
its
renaissance
had
already
been
initiated
by
horses,
which
had
been
reintroduced
into
North
America
in
the
sixteenth
century.
Surely
ama-
teur
naturalists
and
people
living
wher-
ever
osage
orange
and
ranch
horses
co-exist
know
the
answer
to
the
ques-
tion-it
seems
to
be
yes.
But
the
matter
isn’t
discussed
in
the
published
litera-
ture.
Thus
a
core
contention
in
Schambach’s
"Spiroan
trader"
theory
rests
on
what
he
has
been
able
to
glean
from
Red
River
ranchers
and
his
own
casual
observations.
The
search
continues.
A
year
after
publication
of
his
"Spiroan
trader"
theory,
Schambach
obtained
crucial
anecdotal
information:
"A
volunteer
at
my
dig
this
summer
lives
on
a
ranch
on
the
Blackland
Prairie
in
east
Texas,"
Schambach
wrote
me.
"She
has
a
small
herd
of
horses
which,
she
assures
me,
routinely
eat
osage
orange
fruits
on
their
own.
Furthermore,
she
knows
for
a
fact
that
horses
spread
the
tree
via
their
manure
because
when
she
and
her
hus-
band
acquired
their
property
there
was
no
osage
orange
growing
on
the
upland
(prairie)
parts
of
it,
only
in
the
bottomlands
along
the
creeks.
But
soon
after
they
began
pasturing
horses
on
the
land,
the
osage
orange
began
to
migrate
out
of
the
bottoms,
and
it
is
now
growing
all
over
their
prairie
areas,
to
their
dismay."
"
Here’s
another
intriguing
story
that
came
my
way
while
I
was
writing
this
article-this
one
from
Robert
M.
Timm,
professor
of
ecology
and
evolutionary
biology
at
the
Umversity
of
Kan-
sas.
Timm
has
horses
and
one
mule
on
his
farm
in
Kansas.
They
all "love
the
fruits"
of
osage
orange,
he
wrote
me.
"The
mule
is
the
best
at
locating
them,
but
if
you
are
experienced
with
mules
that
wouldn’t
be
a
surprise.
They
are
always
much
more
curious
and
more
explor-
atory
than
horses.
I’d
say
of
all
the
natural
foods
around
here,
osage
orange
fruits
are
the
mule’s
favorite.
He
seems
to
remember
them
from
one
year
to
the
next,
but
that
too
is
typical
of
mules.
I
have
no
doubt
that
Pleistocene
horses
would
have
long-term
memory
of
favorite
trees
to
feed
at
every
fall."
II
Timm
is
very
familiar
with
Dan
Janzen’s
anachronism
theory
and
has
been
casually
observing
mice,
rabbits,
and
tree
squirrels
feed-
18
8
ing
on
the
pulp
and
seeds.
"They
don’t
cache
osage
orange,"
he
observes,
"they
eat
it
on
the
spot."
Most
intriguing
is
his
discovery
of
large
quantities
of
shredded, freshly
fallen
fruit
in
the
stomachs
of
deer.
All
these
mammals
great
and
small
are
indeed
eating
the
fruit,
but
are
they
dispersing
the
seed?
Timm
concludes
no.
Timm
acquires
buckets
of
osage
orange
fruits
from
neighbors
and
spreads
them
on
the
unpastured
sections
of
his
own
property
as
supplemental
feed
for
wildlife.
Nevertheless,
he
has
encountered
no
seedling
trees.
"I
picked
up
another
five
gallon
bucket
of
fruits
this
morn-
ing,"
Timm
wrote
me
as
this
article
went
to
press,
"and
I’ll
check
here
in
a
few
weeks
to
see
if
the
seeds
make
it
intact
through
a
mule’s
digestive
tract.
I’ll
pull
the
mule
and
horses
off
the
pasture
later
this
month
and
keep
them
in
a
paddock
for
the
winter
and
give
the
mule
fruits
where
it
will
be
easy
for
me
to
retrieve
the
seeds."
Overall,
anachronism
theory
seems
to
be
anecdotally
well
supported
for
horses
as
dis-
persal
agents
of
osage
orange.
Are
there
any
other
plausible
ghosts
to
pair
with
this
native
fruit
besides
Pleistocene
horses?
Paul
Martin
and
I
had
a
chance
to
test
osage
orange
vicariously
on
a
much
bigger
Pleistocene
surrogate:
African
elephants
at
the
Brookfield
Zoo
in
Chicago.
Almost
surely
this
was
the
first
time
since
the Pleistocene
that
the
fruit of
An
extreme
anachromsm.
Osage
orange
is
one
of
North
America’s
most
anachromstic
frmts.
Freshly
sliced
fruit
oozes
a
white
latex,
which
has been
wiped
clean
from
the
slice
on
the
left.
Honey
locust
seed (1
cm)
for
scale
Maclura
pomifera
had
met
the
molar
of
a
pro-
boscidean.
I
sent
a
box
of
freshly
fallen
fruit
to
Martin,
which
he
in
turn
forwarded
to
the
Brookfield
Zoo.
After
a
search
of
the
literature,
zoo
staff
decided
that
there
was
no
danger
in
offering
the
elephants
a
few
fruits.
The
results
were
inconclusive.
At
first,
the
youngest
two
elephants
didn’t
want
to
even
touch
the
fruits
offered
by
their
keepers.
Finally,
each
curled
a
trunk
around
a
sphere
and
hurled
the
offensive
object
out
of
their
habitat.
The
matriarch,
however,
chose
to
sample
the
first
fruit
offered,
chewing
and
swallowing.
But
she
would
then
accept
no
more.
Herbivores
are
known
to
be
wary
of
novel
foods.
Cultural
knowledge
of
gastronomic
pos-
sibilities,
passed
from
one
generation
to
the
next
in
social
animals,
would
not
be
available
to
zoo
elephants.
Then
too,
well-fed
captive
am-
mals
will
often
turn
up
their
noses
at
foods
that
their
wild
counterparts
would
happily
consume.
The
case
is
therefore
still
to
be
made
that
Pleis-
tocene
mastodons
and
mammoths
would
have
joined
horses
in
dispersing
osage
orange
fruits
in
North
America.
But
it
will
be
a
most
interesting
hypothesis
to
pursue-for
anyone
excited
by
the
theory
and
who
has
access
to
elephants!
Powers
of
Persistence
It
is
perhaps
no
coincidence
that
the
five
species
of
temperate
American
trees
judged
anachronis-
tic
by
Dan
Janzen
and
Paul
Martin
are
all
prodigious
cloners.
Vegetative
means
of
reproduction
would
have
helped
these
trees
persist
for
the
thir-
teen
thousand
years
that
sexual
repro-
duction
has
been
disrupted
for
want
of
adequate
seed
dispersal.
Kentucky
coffee
tree,
honey
locust,
pawpaw,
persimmon,
and
osage
orange
all
send
up
root
suckers-prolifically
so
when
the
main
stem
is
pruned
or
other-
wise
damaged.
Kentucky
coffee
and
pawpaw
are
extraordinarily
skilled
in
growing
lateral
root
runners
that
sprout
new
stems
many
meters
from
the
elder
stem,
supported
by
photosynthates
sup-
plied
by
the
parent.
Indeed,
a
few
years
ago
when
a
pawpaw
tree
"died"
of
old
age
in
the
Arnold
Arboretum,
more
19
than
a
hundred
fresh
stems
popped
up
almost
immediately
from
a
vast
network
of
root
run-
ners.
And
although
the
Arboretum
isolates
its
mature
kentucky
coffee
specimens
by
encir-
cling
the
trees
with
a
wide
buffer
of
mowed
lawn,
grounds
staff
must
periodically
rid
neigh-
boring
beds
of
the
vigorous
fresh
stems
emanat-
mg
from
hidden
root
runners.
As
the
ice
retreated
from
its
last
southward
advance,
which
peaked
about
twenty
thousand
years
ago,
four
of
the
five
above-mentioned
anachronistic
trees
of
eastern
and
central
North
America
would
have been
helped
to
reclaim
former
territory
by
newly
arriving
humans.
Pawpaw
and
persimmon
fruits
would
have
been
carried
back
to
camp,
their
seeds
removed
or
spit
out
at
the
time
of
eating.
Honey
locust
pods
would
have
been
opened
and
licked
for
their
sweet
matrix,
the
hard
seeds
discarded.
Ken-
tucky
coffee
trees
were
valued
not
for
their
fruit
but
for
their
large,
nearly
spherical
seeds,
which
took
a
lovely
polish
and
were
used
for
gaming
tokens.
Although
the
wood
of
osage
orange
was
highly
prized
and
known
to
have
been
traded
across
great
distances
in
the
time
just
prior
to
European
contact,
the
fruits
held
little
if
any
value.
Does
this
perhaps
explain
why
the
range
of
osage
orange
became
so
constricted?
Is
the
Endangered
Torreya
Tree
Anachronistic?
Coming
to
terms
with
the
likelihood
that
native
horses
almost
certainly
and
elephants
probably
were
effective
seed
dispersers
of
osage
orange
during
the
Pleistocene
and
for
several
tens
of
millions
of
years
before
that
provides
fresh
insights
into
how
to
rescue
from
extinction
a
severely
endangered
American
tree,
Torreya
taxifolia
(florida
torreya).
Torreya
is
a
conifer
of
the
plum
yew
family,
Cephalotaxaceae,
and
thus
bears
no
fruit
as
botanically
defined.
Nevertheless,
the
fleshy
design
of its
diaspore-
ecologically
a
fruit-is
an
obvious
lure
for
am-
mals.
Like
a
yew
or
a
gmkgo,
torreya
produces
single
large
seeds
enveloped
in
what
ought
to
be
viewed
as
fruits
by
vertebrate
dispersers.
The
proximate
cause
of
Torreya
taxifoha’s
imminent
extinction,
and
thus
the
cause
that
gets
all
the
attention,
is
disease.
Some
thirty
pathogens
are
known
to
infest
it,
but
no
single
disease
seems
to
be
the
culprit.9
Once
common
in
the
rich
soils
of
the
Apalachicola
River
of
northern
Florida,
adult
specimens
growing
in
the
wild
suddenly
began
to
die
in
the
1950s,
and
none
remam
today.
Like
the
American
chestnut
that
was
destroyed
by
(an
imported)
blight
dur-
ing
the
early
years
of
the
twentieth
century,
torreya
survives
only
because
new
stems
keep
sprouting
from
the
same
rootstock.
Sadly,
each
fresh
sprout
of
torreya
is
doomed
to
die
before
it
is
old
enough
to
produce
pollen
or
ova.
Energy
stored
in
the
roots
will
eventually
give
out,
since
new
starts
in
the
shady
forest
may
con-
sume
more
photosynthate
than
they
can
return
to
the
roots
before
their
demise.
The
genus
Torreya
was
once
distributed
throughout
the
Northern
Hemisphere.
Range
fragmentation
has
created
distinct
species
in
eastern
China,
patches
of
the
Coast
Range
and
the
Sierras
of
California,
and
the
Apalachicola
of
Florida.
The
geographic
range
of
the
Florida
species
is
today
restncted
to
the
cool
ravines
along
the
east
side-only
the
east
side-of
a
22-
mile
(35-km)
stretch
of
the
Apalachicola
River
in
northern
Florida.
During
the
coldest
times
of
the
Pleistocene,
the
Apalachicola,
with
its
moderate
climate
and
rich
soils,
was
a
refuge
for
the
trees
and
forbs
that
now
enrich
the
Cove
Hardwood
forest
of
Great
Smoky
Mountains
National
Park,
375
miles
(600
km)
to
the
north.
After
the
ice
retreated,
most
of
the
plants
hitched
rides
from
wind
and
animals
and
moved
back
north
to
their
pre-glacial
home.
Torreya
seems
to
have
been
left
behind.
Some
experts
confirm
that
the
tree’s
troubles
may
have
begun
for
want
of
a
disperser. 10
Glo-
bal
or
regional
extinction
of
an
animal
partner
(or
partners)
may
be
the
root
cause
of
the
tree’s
current
distress.
Torreya
is
probably
not
ideally
suited
for
the
warmth
and
humidity
of
today’s
Apalachicola
region.
It
wants
to
head
north,
but
it
hasn’t
found
a
vehicle.
That
florida
torreya
may
be
haunted
by
the
ghosts
of
extinct
dispersers
is
suggested
by
a
host
of clues.
First,
the
diaspore
of
all
species
of
Torreya
is
distasteful
or
toxic
to
many
(possibly
all)
mammals
who
normally
consume
fruits.
The
pulp
has
a
high
terpene
content
and
it
leaves
a
sticky
residue
on
one’s
skin.
Squirrels
treat
the
fruit
as
they
treat
gmkgo
fruit
m
New
20
A
florida
torreya
photographed
well
north
of
its
"native"
grounds,
near
Philadelphia,
Pennsylvama,
at
the
Henry
Botamc
Garden,
near
Gladwyne.
York
City’s
parks:
they
discard
the
flesh
and
steal
the
seeds.
Squirrels
that
fed
on
torreya
seeds
on
the
east
side
of
the
river
would
be
unable
to
carry
them
across
water
to
the
west
side,
and
if
the
rich
soils
of
the
Apalachicola
are
isolated
from
rich
soils
to
the
north
by
a
barrier
of
sandy
soils,
then
the
squirrels
would
also
be
unable
to
disperse
the
seeds
farther
north.
Squir-
rels
may
thus
be
a
disperser,
but
they
apparently
are
not
the
right
disperser
for
helping
this
tree
reclaim
its
pre-glacial
range.
This
explanation
would
account
for
the
seemingly
paradoxical
fact
that
until
the
1950s,
florida
torreya
was
the
seventh
most
abundant
tree
species
in
an
aston-
ishingly
small
patch
of
"native"
habitat.
Perhaps
the
best
evidence
that
florida
torreya
may
be
suffering
from
an
mabil-
ity
to
track
climate
change
is
that
before
the
blight
took
hold,
this
tree
was
planted
hundreds
of
miles
north
of
its
Florida
habitat
in
the
mountains
of
North
Carolina,
near
Asheville.
There,
on
the
Biltmore
Estate,
the
torreyas
are
thriving,
and
the
females
produce
abun-
dant
seeds.
"Flower
beds
often
abound
with
seedlings
’planted’
by
squirrels,"
reports
Bill
Alexander,
landscape
histo-
rian
at
the
Biltmore.
During
his
23
years
there,
Alexander
has
watched
the
torreyas
stand
up
well
to
a
five-year
drought.
And
in
the
winter
of
1985
the
thermometer
plunged
to
minus-20
degrees
Fahrenheit,
yet
"our
trees
smiled
right
through,"
he
told
me.
For
a
number
of
years,
Alexander
had
been
thinking
that
"florida"
torreya
really
belonged
back
in
North
Carolina.
So
he
was
delighted
to
hear
of
the
lost-
disperser
theory.
A
megafaunal
ghost?
If
so,
the
ghost
may
well
be
a large
extinct
tortoise,
I
suggested,
as
reptiles
are
far
more
tolerant
of
plant
terpenes
than
are
mammals,
and
as
the
thin
"shell"
protecting
the
large
single
seed
of
this
conifer
offers
scant
protection
against
molars.
One
must
not,
however,
ponder
the
plight
of
the
florida
torreya
in
isolation
from
its
sister
species.
In
contrast
to
Torreya
taxifolia,
California’s
torreya
(Torreya
californica)
is
maintaining
its
popula-
tion,
as
are
the
several
Asian
species
of
Torreya-all
of
which
bear
nearly
identical
propagules.
Nevertheless,
all
occupy
restricted
geographic
ranges.
What
if
the
entire
genus
lost
its
key
dispersers
and
now
depends
on
the
local
activities
of
squirrels?
Bill
Alexander
and
I
easily
came
up
with
two
plausible
explanations
for
the
differences
in
endangerment,
based
strictly
on
geographic
differences.
In
eastern
North
America,
the
cli-
matic
effects
of
the
Ice
Sheet
reached
much
farther
south
than
was
the
case
in
either
west-
ern
North
America
or
eastern
Asia,
forcing
the
Appalachian
species
to
take
refuge
at
a
lower
21
latitude.
Perhaps
even
more
significant
is
that
latitudinal
migration
was
the
only
option
for
florida
torreya
as
the
climate
warmed.
In
contrast,
torreya
species
in
California
and
in
Asia
could
head
upslope.
These
torreyas
are
native
to
mountainous
regions,
where
altitudi-
nal
gain
facilitated
by
nothing
more
than
squir-
rels
could
help
the
trees
keep
pace
with
a
warming
climate.
Such
unsubstantiated
and
untested
leaps
of
speculation
are
normally
not
well
received
within
the
scientific
commumty-but
these
are
not
normal
times.
Without
some
drastic
break-
through
in
the
management
of
Florida’s
wild
population
of
torreya
trees,
Torreya
taxlfolia
will,
within
fifty
years,
almost
surely
be
extinct
outside
of
botanical
gardens.
Perhaps
it
is
time
to
help
this
torreya
gain
rootholds
of
wild
popu-
lations
in
the
mountams
of
North
Carolina.
Such
is
not,
alas,
how
things
are
done
with
endangered
species-the
exception
being
the
recent
return
of
the
california
condor
to
its
Pleistocene
home
near
the
Grand
Canyon.
Native
territory
is
regarded
as
the
last
best
place
to
be.
But
what
is
"native"?
How
far
might
we
justifiably
reach
back
in
time
for
a
benchmark?
In
a
study
of
endangered
species
published
in
2000,
Rob
Channell
and
Mark
Lomolino
con-
cluded
that
"most
species
examined
persist
in
the
periphery
of
their historical
geographic
ranges.""
If
habitat
at
the
periphery
of histori-
cal
range
is
adequate
but
not
ideal,
then
the
last
place
a
troubled
species
is
found
may
not,
in
fact,
be
the best
place
to
assist
its
recovery.
Transplantation
across
great
distances
is
an
uncommon
and
controversial
technique
for
biodiversity
conservation
today.
But
as
the
greenhouse
effect
ratchets
up
temperatures
and
reroutes
ramfall,
and
as
botanical
preserves
become
even
more
isolated
islands
in
a
sea
of
human
development,
long-distance
trans-
plantation
will
become
the
norm.
If
gardening
a
few
local
patches
of
endangered
plants
is
tough
today,
it’s
gomg
to
get
a
lot
tougher
when,
like
it
or
not,
we
become
gardeners
of
the
planet.l2
Helping
plants
track
climate
change
from
one
patch
of
habitat
to
another
will
be
a
routine
tactic
for
conserving
biodiversity
decades
hence.
Is
it
too
early
to
begin
now
with
florida
torreya?
Notes
1 In
the
June
8,
2001,
issue
of
Science,
two
papers
confirmed
the
"overkill
hypothesis"
of
end-
Pleistocene
extinctions,
one
for
Australia
and
the
other
for
North
America.
The
North
American
paper
is
John
Alroy,
2001,
"A
multispecies
overkill
simulation
of
the
end-Pleistocene
megafaunal
mass
extinction,"
292
1893-1896.
A
news
report
by
Leigh
Dayton
pubhshed
in
the
same
issue
(p.
1819),
"Mass
extinctions
pmned
on
ice
age
hunters,"
suggests
that
this
view
is
now
the
majority
position.
2 Stephen
T.
Jackson
and
Chengyu
Weng,
1999,
"Late
Quaternary
extinction
of
a
tree
species
in
eastern
North
America,"
Proceedings
of
the
National
Academy
of
Scsence
96.
13847-14852.
3 Dan
Janzen’s
suggestion
that
fleshy-fruited
plants
may
have
gone
extinct
smce
the
end
of
the
Pleistocene
is
m
Connie
Barlow,
2001,
The
Ghosts
of
Evolution
(New
York:
Basic
Books~,
88
4
D
H.
Janzen
and
P.
S
Martin,
1982,
"Neotropical
anachromsms:
The
fruits
the
gomphotheres
ate,"
Science
215:
19-27.
5 For
the
story
of
how
Janzen
and
Martin
developed
their ideas
and
conducted
their
fieldwork,
see
chapters
1-3
of
the
author’s
Ghosts
of
Evoluuon,
op
cit.
6 Robert
E.
Cook,
1982,
"Attractions
of
the
flesh,"
Natural
History
91 / 1
20-24.
~ Martrn
N.
Tchamba
and
Prosper
M.
Seme,
1993,
"Diet
and
feedmg
behavior
of
the
forest
elephant
m
the
Santchou
Reserve,
Cameroon,"
Afncan
Journal
of
Ecology 31:
165-171.
8 The
theory
that
osage
orange,
prior
to
European
colonization,
occupied
a
very
restricted
range
is
presented
in
Frank
F.
Schambach,
2000,
"Spiroan
traders,
the
Sanders
Site,
and
the
Plams
Interaction
Sphere,"
Plains
Anthropologist
45
7-33.
9
Mark
W
Schwartz,
Sharon
M.
Hermann,
and
Philip
J.
Van
Mantgem,
1999,
"Population
persistence
in
Florida
Torreya,"
Conservation
Biology
14.
1023-1033.
lo
See
p.
229
of
The
Ghosts
of
Evolution.
l Rob
Channell
and
Mark
V.
Lomolino,
2000,
"Dynamic
biogeography
and
conservation
of
endangered
species,"
Nature
403:
84-86
’z D.
H.
Janzen,
1998,
"Gardemfication
of
wrldland
nature
and
the
human
footprint,"
Science
279:
1312-
1313.
Acknowledgments
I
wish
to
thank
Dan
Janzen,
Paul
Martm,
Bill
Alexander,
Robert
Timm,
and
Frank
Schambach
for
helpful
critiques,
comments,
and
anecdotes.
Connie
Barlow
is
a
science
writer
and
author
of
The
Ghosts
of
Evolution
Nonsensical
Frmts,
Missing
Partners,
and
Other
Ecological
Anachromsms,
published
in
2001
by
Basic
Books.
... Plants that are categorized as anachronistic usually produce large, edible fruits that apparently evolved to attract a now extinct, seed dispersing frugivore. The large size of many of these fruits has led authors to conclude the megafaunal mammals were the main seed dispersers for these species (Janzen and Martin, 1982;Barlow, 2001), as is often the case where megafauna survive to the present ( Sekar and Sukumar, 2015). Several authors have proposed these plants are well represented in North America, a region that suffered particularly high mammal extinction rates during the end of the Pleistocene (Janzen, 1982;Janzen and Martin, 1982;Barlow, 2000;Kistler et al., 2015). ...
... The large size of many of these fruits has led authors to conclude the megafaunal mammals were the main seed dispersers for these species (Janzen and Martin, 1982;Barlow, 2001), as is often the case where megafauna survive to the present ( Sekar and Sukumar, 2015). Several authors have proposed these plants are well represented in North America, a region that suffered particularly high mammal extinction rates during the end of the Pleistocene (Janzen, 1982;Janzen and Martin, 1982;Barlow, 2000;Kistler et al., 2015). ...
... One hypothesized anachronistic plant is the Osage orange (Moraceae: Maclura pomifera), which produces an unusually large fruit (up to 15 cm in diameter and 1 kg in weight) and which appears to have no extant seed disperser. At the time of European settlement, the realized range of M. pomifera was much smaller than its potential range (Smith and Perino, 1981;Burton, 1990;Barlow, 2000), suggesting it lacked an effective seed dispersal mechanism. Today, M. pomifera has a much larger range due to active human dispersal (Burton, 1990). ...
Article
Full-text available
The Osage orange (Maclura pomifera) is considered anachronistic because it has no known seed disperser. However, anecdotal observations suggest squirrels (Sciurus spp.) may act as dispersers as they move fruits away from parent plants and through the prolonged handling time required to access the seeds. Our aim was to determine if squirrels potentially disperse Osage orange seeds in this manner by presenting Osage orange seeds and fruits in the presence and absence of sunflower seeds (whole and shelled), which squirrels are known to consume readily. We found, although squirrels preferred sunflower seeds, they readily consumed the Osage orange seeds and moved the fruits when multiple food sources were available. However, when fruits were presented alone, we found a small number of fruits were moved and these were moved only a short distance. Our results suggest that while squirrels occasionally show interest in Osage orange fruits, they do not typically disperse M. pomifera seeds via fruit handling. We therefore conclude anecdotal observations of squirrels feeding on seeds represent uncommon events, supporting the hypothesis that M. pomifera is anachronistic.
... An analysis of modern M. pomifera populations found high local genetic structure (Schnabel et al., 1991) which is consistent with the lack of fruit dispersal. For these reasons, Osage oranges have been proposed as a megafauna-dispersed fruit, with speculation that it may be adapted to extinct dispersers such as North American horses, mastodons, or giant ground sloths (Barlow, 2001;Brounaugh, 2010). Although M. pomifera is climatically adapted to much of North America, and fossils have been found as far north as Ontario (Penhallow, 1907), by the time of European settlement its range appears to have dwindled to a portion of Texas and Oklahoma, allowing a single tribe to control the trade for its wood, valued for bows (Barlow, 2000). ...
... Experimental efforts to identify the extinct dispersers have been elusive. Although there is anecdotal evidence that domesticated horses sometimes eat the syncarps (Barlow, 2001), passage of M. pomifera seeds through modern elephant or domesticated horse guts has not been shown to improve germination (Boone et al., 2015). With a ca. ...
Article
Background and aims: Maclura (ca. 12 spp., Moraceae) is a widespread genus of trees and woody climbers found on five continents. Maclura pomifera, the Osage orange, is considered a classic example of an anachronistic fruit. Native to the central USA, the grapefruit-sized Osage oranges are unpalatable and have no known extant native dispersers, leading to speculation that the fruits were adapted to extinct megafauna. Our aim was to reconstruct the phylogeny, estimate divergence dates, and infer ancestral ranges of Maclura in order to test the monophyly of subgeneric classifications and to understand evolution and dispersal patterns in this globally distributed group. Methods: Employing Bayesian and maximum-likelihood methods, we reconstructed the Maclura phylogeny using two nuclear and five chloroplast loci from all Maclura species and outgroups representing all Moraceae tribes. We reconstructed ancestral ranges and syncarp sizes using a family level dated tree, and used Ornstein-Uhlenbeck models to test for significant changes in syncarp size in the Osage orange lineage. Key results: Our analyses support a monophyletic Maclura with a Paleocene crown. Subgeneric sections were monophyletic except for the geographically-disjunct Cardiogyne. There was strong support for current species delineations except in the widespread M. cochinchinensis. South America was reconstructed as the ancestral range for Maclura with subsequent colonization of Africa and the northern hemisphere. The clade containing M. pomifera likely diverged in the Oligocene, closely coinciding with crown divergence dates of the mammoth/mastodon and sloth clades that contain possible extinct dispersers. The best fitting model for syncarp size evolution indicated an increase in both syncarp size and the rate of syncarp size evolution in the Osage orange lineage. Conclusions: We conclude that our findings are consistent with the hypothesis that M. pomifera was adapted to dispersal by extinct megafauna. In addition, we consider dispersal rather than vicariance to be most likely responsible for the present distribution of Maclura, as crown divergence post-dated the separation of Africa and South America. We propose revised sectional delimitations based on the phylogeny. This study represents a complete phylogenetic and biogeographic analysis of this globally distributed genus and provides a basis for future work, including a taxonomic revision.
... Such low seed-dispersal effectiveness has been documented for Florida torreya (T. taxifolia) (Barlow, 2001). Therefore, we speculate that the species was most probably contained in glacial refugia even during the interglacial periods. ...
Article
Both palaeoclimatic change and anthropogenic habitat destruction can have adverse effects on species demography and, in turn, may lead a species towards being endangered and rare. Understanding the relative importance of these natural and anthropogenic factors driving species endangerment and rarity is thus crucial for effective conservation planning but remains elusive. Here, we examine the phylogeography and demographic history of an endangered conifer species in China, Torreya jackii, and assess the relative importance of natural and anthropogenic factors that might have put the species in its endangered state. We collected tissue samples from all the 13 extant wild populations, and analyzed the genetic variation using eight nuclear microsatellites and 4 chloroplast and 1 mitochondrial DNA fragments. We found low genetic and nucleotide diversities, which could explain the absence of spatial and phylogeographic structure. Using a hierarchical approximate Bayesian computation technique, we identified the demographic scenario that best fits the genetic data and found that effective population size was low at least 200,000 years ago but expanded after the Last Glacial Maximum (LGM). The palaeoclimatic niche model revealed a profound effect of precipitation on the distribution of T. jackii and predicted that the current distribution areas were suitable during the LGM. Despite the post‐LGM expansion, the best‐supported scenario showed a dramatic population collapse during the past three centuries, when anthropogenic disturbances also increased dramatically. Overall, our study sheds light on how historical factors and human impacts jointly threaten the persistence of a species, and these aspects should be duly considered in species conservation planning. This article is protected by copyright. All rights reserved.
... America supported a megafauna assemblage as diverse as modern Africa (Koch & Barnosky 2006), which contained numerous animals proposed to disperse the now-anachronistic fruits (Janzen & Martin 1982;Barlow 2000Barlow , 2002. Among these species, the most notable frugivore dispersers were proboscideans (elephants and their relatives, especially fruit-eating mastodons), xenarthans (ground sloths, which have no extant species), and equids (horses and their relatives) (Barlow 2000;Boone et al. 2015;Gardner et al. 2017). ...
Article
Understanding the degree to which species distributions are controlled by climate is crucial for forecasting biodiversity responses to climate change. Climatic equilibrium, when species are found in all places which are climatically suitable, is a fundamental assumption of species distribution models, but there is evidence in support of climate disequilibria in species ranges. Long-lived, sessile organisms such as trees may be especially vulnerable to being outpaced by climate change, and thus prone to disequilibrium. In this dissertation, I tested the degree to which North American trees are in equilibrium with their potential climatic ranges using the ‘range filling’ metric, which is calculated by taking the proportion of modeled potential climatic range which is realized. In Chapter I, I demonstrated that most species are missing from the majority of their potential ranges (mean range filling 48%). Range filling was strongly positively correlated with realized range size. I found that small-ranged species have underfilled climatic ranges relative to a spatially randomized ecological null model, suggesting that climate is a poor predictor of their distributions. I further show small-ranged species tend to have range shapes more indicative of dispersal limitations than climatic filling. In Chapter II, I found that range filling correlates with species’ functional differences; I found low range filling among species with traits correlated with pioneer plant strategies, while “climax” species showed high range filling. An analysis of range filling through time from pollen-derived distributions (Chapter III) revealed that while range filling decreased during post-glacial climatic change events, much of the contemporary disequillibrium is the result of decreases in the last 5000 years. Megafauna-adapted species which are proposed to have dispersal limitations due relying on now-extinct Pleistocene megafauna mostly do not show the hypothesized consequences, possibly due to compensatory dispersers. Overall, these findings suggest that nonclimatic factors and dispersal limitations drive climatic disequlibrium in North American trees. Considering this in light of human induced landscape fragmentation and climate change which exacerbate dispersal potential and increase equilibrium, attention should be given towards transplanting narrowly distributed tree species.
... This last concept, described for the first time several decades ago by Janzen and Martin (1982), is defined in a context of frugivory as "extant interactions between animal frugivores and plants involving traits that show striking unfit patterns to an extant fauna" (Guimarães et al., 2008, p. 2). Typical examples are fruits with huge seeds which are dispersed inefficiently by the contemporary frugivore assemblages, like avocado (Persea americana) (Cook, 1982), osage orange (Maclura pomifera) (Janzen and Martin, 1982), or Florida torreya (Torreya taxifolia) (Barlow, 2001). Anachronisms can also show up through antagonisms, such as the presence of spines or other plant defenses against large herbivores that no longer exist (e.g., Bond et al., 2004). ...
Article
Full-text available
Megafauna extinctions often lead to the disruption of plant-animal interactions, such as the seed-disperser mutualisms, which might entail severe consequences for plant populations and entire communities. Interestingly, the contemporary persistence of anachronistic plant species might be possible thanks to surrogate dispersers or seed dispersal "rescuers". We know very little on how these relevant functional replacements are contributing to the performance of present-day plant-frugivore networks. The dwarf palm Chamaerops humilis L. is a Mediterranean endemism with fleshy fruits and typically dispersed by mammals. Despite its ecological importance and wide distribution in some of the Mediterranean islands, no information exists about its seed dispersal on these depauperated-fauna systems. In this study, we aim at identifying and quantifying the relative importance of introduced frugivores on the island of Mallorca (Balearic Islands), where no native terrestrial mammals exist. Specifically, we assess for the first time the seed dispersal effectiveness (SDE) for C. humilis on islands; we evaluate the quantitative component by fecal and regurgitation sampling surveys, and the qualitative component by means of seed germination experiments and seedling growth measures. Introduced goats (Capra hircus L.) and pine martens (Martes martes L.) were the local mammal fruit consumers of C. humilis identified in our study sites. Results suggest that goats are much more important quantitatively than pine martens, due to the high number of fruits handled in each foraging bout and their extremely high abundance on the island. However, pine marten-ingested seeds showed the highest final seedling emergence success and seedling growth, thus its qualitative contribution on C. humilis seed dispersal is higher than that of goats. Overall, SDE was almost 9-fold higher for goats than for pine Muñoz-Gallego et al. Chamaerops Humilis Seed-Dispersal Rescuers martens. We conclude that these two non-native mammal species are effective seed dispersers of C. humilis in this and probably other Mediterranean islands, where humans led to the extinction of its native seed dispersers, as it was probably the case of the goat-like Myotragus balearicus in the Balearic Islands.
... There has been extensive discussion of ecological anachronisms in the ecology literature (Janzen & Martin, 1982;Guimarães et al., 2008;Johnson, 2009;Gill, 2014). Popular natural history writing (Barlow, 2000(Barlow, , 2001Bronaugh, 2010) has paid attention to some species native to temperate North America that may once have been dispersed by megaherbivores such as mammoths, mastodons, or ground sloths. A particularly striking example is Maclura pomifera (Raf.) ...
Article
In organismic biology, the formation of ecological and evolutionary hypotheses on the basis of observable morphologies is a central element of research, and by extension of teaching and learning. Often it is necessary to take account of complex combinations of factors, some of which may be far from obvious. In the work described here, hypothesis formation and testing was exercised and studied in a learner-centered and object-based manner using an anachronistic, seemingly "nonsensical" plant, Maclura pomifera (Moraceae), in which the link between structure and function only becomes clear when considering past faunistic environments. The element of the unexpected and the allure of the large animals is thought to add to epistemic curiosity and student motivation to engage in the study of plants.
... Both large fruits and large thorns are believed to be adaptations to the former presence of large herbivores, namely of the late Pleistocene. The species is therefore thought to be shaped by past evolutionary forces and fit for a biological environment that no longer exists (Barlow, 2001(Barlow, , 2002Bronaugh, 2010). ...
Article
Object-based learning is an approach that aims to foster observational skills and sensory awareness. Paradoxical plant objects that do not lend themselves to all-too-easy explanations and interpretations can be used to practice the search for ecological explanations and the formation of evolutionary hypotheses. They can be the basis of particularly fruitful and rewarding learning experiences. Gleditsia triacanthos, the honey locust, is a commonly planted ornamental tree. It exhibits striking structures of defense against – and fruit that point to a mutualism with – large animals. These structures, possibly developed in coevolution with Pleistocene faunas, invite a discussion of the complex, neither fully antagonistic nor fully mutualistic, relationships between plants and animals. © 2019 National Association of Biology Teachers. All rights reserved.
... For example, Janzen & Martin [11] proposed that extinct Central American megafauna had a central role in the dispersal and evolution of several large angiosperm seeds. Their argument was supported by the existence of dispersal anachronisms-plant species with seed traits (such as size) that appear maladapted for dispersal by the contemporary fauna, haunted by the 'ghosts of past mutualisms' [12]. As well as being large seeded, these putatively anachronistic plants had fruits that dropped to the ground when ripe (early abscission), where the terrestrial megafauna could access them; were unattractive to arboreal or volant frugivores; showed low contemporary dispersal rates; and had seeds that were protected by a thick, woody, endocarp [11]. ...
Article
Full-text available
Often the mutualistic roles of extinct species are inferred based on plausible assumptions, but sometimes palaeoecological evidence can overturn such inferences. We present an example from New Zealand, where it has been widely assumed that some of the largest-seeded plants were dispersed by the giant extinct herbivorous moa (Dinornithiformes). The presence of large seeds in preserved moa gizzard contents supported this hypothesis, and five slow-germinating plant species (Elaeocarpus dentatus, E. hookerianus, Prumnopitys ferruginea, P. taxifolia, Vitex lucens) with thick seedcoats prompted speculation about whether these plants were adapted for moa dispersal. However, we demonstrate that all these assumptions are incorrect. While large seeds were present in 48% of moa gizzards analysed, analysis of 152 moa coprolites (subfossil faeces) revealed a very fine-grained consistency unparalleled in extant herbivores, with no intact seeds larger than 3.3 mm diameter. Secondly, prolonged experimental mechanical scarification of E. dentatus and P. ferruginea seeds did not reduce time to germination, providing no experimental support for the hypothesis that present-day slow germination results from the loss of scarification in moa guts. Paradoxically, although moa were New Zealand's largest native herbivores, the only seeds to survive moa gut passage intact were those of small-seeded herbs and shrubs.
... Moreover, we modeled the spatial distribution of immature motacú palms potentially generated as a result of the seeds dispersed by macaws and cattle, which resulted the main dispersers of this species. Our results challenge the seed dispersal anachronism 12,27 by showing that macaws are currently the main dispersers of the motacú palm, thus contributing to shaping the landscape structure and function of this Amazonian biome. ...
Article
Full-text available
Seed dispersal is one of the most studied plant–animal mutualisms. It has been proposed that the dispersal of many large-seeded plants from Neotropical forests was primarily conducted by extinct megafauna, and currently by livestock. Parrots can transport large fruits using their beaks, but have been overlooked as seed dispersers. We demonstrate that three macaws (Ara ararauna, A. glaucogularis and A. severus) are the main dispersers of the large-seeded motacú palm Attalea princeps, which is the biomass-dominant tree in the Bolivian Amazonian savannas. Macaws dispersed fruits at high rates (75–100% of fruits) to distant (up to 1200 m) perching trees, where they consumed the pulp and discarded entire seeds, contributing to forest regeneration and connectivity between distant forests islands. The spatial distribution of immature palms was positively associated to the proximity to macaws’ perching trees and negatively to the proximity to cattle paths. The disperser role of livestock, presumably a substitute for extinct megafauna, had little effect due to soil compaction, trampling and herbivory. Our results underscore the importance of macaws as legitimate, primary dispersers of large-seeded plants at long distances and, specifically, their key role in shaping the landscape structure and functioning of this Amazonian biome.