Why Do Most Tropical Animals Reproduce Seasonally?

Testing Hypotheses on an Australian

Snake
Author(s): G. P. Brown and R. Shine
Source: Ecology, Vol. 87, No. 1 (Jan., 2006), pp. 133-143
Published by: Ecological Society of America
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Ecology, 87(1), 2006, pp. 133-143

? 2006 by the Ecological Society of America

WHY DO MOST TROPICAL ANIMALS REPRODUCE SEASONALLY?

TESTING HYPOTHESES ON AN AUSTRALIAN SNAKE

Sciences

Biological

Abstract.

Most

year-round.
tive) reasons
all

although

South Wales

2006

Australia

reproduce

reptile

synchronizing
are
reptiles

on
of

but with a major peak inMay-June.

driven

food

for

reproduce
factors

biotic

by

or
hatchlings)
Keelback

conditions).
from
reproduce

Australia

However,

temperatures.
most
do not

constraint,
be
might

tropical
reptiles
or hatchlings,
or
eggs
moist
incubation
suitably

in tropical

Colubridae)

ambient

high

thermal

in

reproduction

mairii,

with

embryogenesis
from
freed
this

of pr?dation
(e.g.,
peak
periods
factors
seasonal
(e.g.,
availability
(Tropidonophis

of Sydney,

Shine1
New

reptiles
restriction

tropical
Seasonal

year-round.

University

R.

even
occurs
in the tropics where
seasonally,
activity
to clarify
ideal model
the ultimate
provide
organisms
(adap
to specific
of reproduction
times
of year. Females
of almost
or offspring
their eggs
in the warmest
time of
species
produce

species

Squamate
for the

temperate-zone
the year,
thereby

A08,

and

P. Brown

G.

snakes

to November,

April

Our field studies falsify hypotheses

abiotic

that invoke biotic

as explanations
for this pattern:
the timing
of nesting
not minimize
does
pr?dation
on eggs,
nor maximize
or survival
rates for hatchlings.
our data
food
Instead,
availability
soon
nest
most
abiotic
factors:
female
keelbacks
after
the
of
cessation
implicate
intensely
are moist
to sustain
monsoonal
rains when
soils
(wetter
enough
optimal
embryogenesis
factors

nests

produce

Key

that
hatchlings,
to eggs).
is lethal

larger
(which
as well

waterlogged
in tropical

words:

as

temperate-zone

Australia;
mairii.

Tropidonophis

climate;

are more

developmental

Introduction
Most

and
animals
do not
year
plants
reproduce
but
instead
in
seasonal
distinct
peaks
display
some
cases
In
this
reproductive
activity.
reproductive
is extraordinarily
all gametes
with
seasonality
precise,
round,

a few

within

produced

or even
hours
coral
days
(e.g.,
et al. 1994).
cases
In other
the re

Babcock

spawning;

is spread

out

productive
activity
but nonetheless
is clearly
seasonal
uous
temperate-zone
(e.g., most

Abts

Homo

weeks
rather

species;

1992, Bauer

1988, Aichinger

Even
2000).
a continuously

over

of

life-history
to clarify
both
the observed

2000,

the

sapiens,

reproduction
extensive

occurs

is a major
axis
research
has sought
reasons
ultimate
for

variation,

the proximate

and

in patterns

diversity
factors

in day
1985,

1970,

19926, Alkins-Koo

of

length

Kumar

Chandola-Saklani

bard and Brooks

that
such

(Murt?n and Westwood

and

Kumar
et al.

1991,
2004),

1987, Hart 2004),

13 December
received
Manuscript
accepted 21 July 2005. Corresponding
1
author. E-mail:
Corresponding

tim

reproductive
have
proved

ing. Proximate
generally
to study, with
amenable
robust
evidence
can be initiated
reproduction
by stimuli
Burns

contin

Fitch

of
archetypal
example
exhibits
breeding
species,
significant
in births
Because
the time
(Bronson
1995).

seasonality
at which
of year

ations

or months,
than

likely

abiotic
Thus,
animals.

more
seasonal
as

vari

1977,

Wikelski

et al.

temperature

(Ob

rainfall (Patterson

2004; revised 9 June 2005;

Editor: D. A. Spiller.
rics@bio.usyd.edu.au

to survive)
factors may

plasticity;

are unlikely
to become
seasonal
reproduction

but
favor

hydric;

oviposition;

pr?dation;

reptile;

1991, Lampo and Medialdea

1996, Madsen and Shine
19996, Christian et al. 2003), and food supply (Tinney
et al. 2001, Clouet 2003, Rubenstein and Wikelski
or

2003),

interactions

Johannes

1967,

et al. 2000,

Hau

2000,

1978,

between

these

factors

Kramer

1978,

Garrido

Hau

Pankhurst

2001,

(Janzen
et

al.

and Porter

2003).
more
to identify
cau
difficult
ultimate
proven
for reproductive
that is, the selec
seasonality,
tive advantages
and disadvantages
re
associated
with
at different
times
of year. Many
producing
hypotheses
It has

sations

have

been

tests

are

proposed
rare. For

mal

requirements
the highly
seasonal
ectothermic
animals

in this

reproductive
(which

to midsummer;

genesis

but

respect,

robust

authors

many
example,
for developing

empirical
invoke
ther

to explain
offspring
of cool-climate

cycles

restrict

typically

Fitch

1970,

Tauber

embryo
et al. 1986,

Vitt

1991, Olsson and Shine 1998). However, the near

ubiquity of this constraint makes it difficult to test the
in

cases

Mouton

and

hypothesis

except

Herselman

1994, Olsson and Shine 1998). Species with

special

(e.g.,

extended

but with
in the
clear peaks
seasons,
breeding
of breeding
within
that longer
offer
intensity
period,
better
for study
in this respect
et
(Sexton
opportunities

al. 1971, Smith and Iverson

Colli

et al.

cases

we

period,
as well

1997,

know
and
as

can
their

1993, Winemiller
et al.

Lemos-Espinal
that breeding
quantify

is possible
the conditions

consequences

133

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All use subject to JSTOR Terms and Conditions

for

1999).
over

the entire

at various

reproductive

1993,
In these

times
females

G.134 P. BROWN

their

and

Such

progeny.
from

predictions
sonally

then

be

to

used

about

hypotheses

test
sea

the

nest conditions,
(e.g., weather,
that might
restrict
repro
supply)
some
of
time within
the
subset

factors

varying

pr?dation
ductive

risk,

food

activity

to

broader

temporal

window

ically

can

data

alternative

AND

when

is phys

reproduction

offer

of
cycles
excellent

ma
In cool-climate
to investigate
these
topics.
species,
events
within
the
female
(ovu
cycle
jor
reproductive
are al
and parturition)
lation,
pregnancy,
oviposition,
most

(Fitch 1970, Ota

in warmer

down
ical

et al. 2003),

with
over

all year

sometimes

1991, Clerke

Schall

1994).

ous)

reproduction
climates
equatorial

female

by

and

(James

1985,

and

aseasonal

reptiles
Girons
and

(Saint

Shine

1993, Dearing

truly

al.

et al. 2003, Mojica

and Alford

Nonetheless,

et

(continu
is rare, even
Pfeffer

in

1971,

to
been
invoked
have
kinds
of hypotheses
major
in trop
the seasonality
of female
reproduction
explain
ical reptiles:
may
(1) Biotic
factors?egg
production
on eggs or nest
to periods
when
be restricted
pr?dation
that newly
such
is low, or timed
emerged
ing females
encounter

will

of

conditions

optimal

food

may

be

(e.g.,

same

The

later

kinds

of

to explain
seasonality
animals
(e.g., Wikelski

seasonally

sonality: (1) food availability (and thus, growth rates)

of hatchlings produced at different times of year; (2)
pr?dation

risk

produced

at different

optimal

we

and

that

Shine

found

season

whereas

of reproductive
the wet-dry
trop
sea
is highly

seasonal
species'
to the geographic
in the wet-dry
tives.
Species
to arid-zone
related
lineages

Critically,
was
linked

season,

whereas

habitats

were

(1985)
otic"

of

the variables

taxa
wet-season

interpreted
hypothesis

this

bred
species
in the wet
bred

of
timing
distribution
tropics
tended

to breed

to those

related

pattern
with
above,

as

from

support

lineages

mostly
season.

and
for

the

preadapted

but

not

flooded

identified

by

to see whether

these

hypoth
is indeed

there

in the putative
selective
condi
of optimal
timing
season
the observed
reproductive

variation

annual

with

the

population.

mesic

of

floodplain

the

year,
with

and

to

species

the onset

Shine

on

empoundment

the Ade

60 km east of Darwin,

The
tropics.
but is shallowly

wet-dry

19966;

of

seasonal
see

Plate

in the

is dry for
for up to

floodplain
inundated

rains

monsoonal
In contrast

1).

to

maximum
regime,
precipitation
mean
warm
remain
(monthly
year-round
temperatures
minima
lower
with
maxima
31-34?C)
during
although
mean
Brown
minima
15-24?C:
the dry season
(monthly
the

highly

seasonal

2001).

Keelbacks

are medium-sized

(to

length [SVL], 280 g) nonvenomous

Widely
much
throughout

"abi

and

is an artificial

Dam

Fogg

laide River

snakes.

Shine

area

Study

et al.

closely
in the dry

more

James

breeders.

our data

the keelback

(Madsen

reproduction
of its rela

that were

moist

(cool,

if so whether

five months

1991), and

some

others

hatchlings
rates

(3.) pr?dation

Methods

most

in the dry

conditions

examine

significant
and

a comparative
analysis
from
in
species
squamate
seasonality
Australia.
ics of northern
Precipitation

sonal in this area (McDonald andMcAlpine

for

rates)

of year;

times of year; and (4) availability

nest

each

For
eses,

Australian

James

times

1976, Wolda

advanced
have
been
explanations
in other
of reproduction
types of
et al. 2001).
et al. 2000,
Aung

with

survival

thus,

(and

on eggs at different
of

James and Shine (1985) attempted to test between these

hypotheses

we
to identify
the
paper,
attempt
to a series
of
with
respect
breeding
factors
that might
biotic
and abiotic
varying
sea
act as selective
for reproductive
forces

ality

1975,

spe

of

timing

coincides

1967, Barbault

in tropical

In this

1).

(Fig.

of

(Fitch and Fitch

1989).

snake

mairii)

an opportunity
to test among
alter
provide
on the possible
and dis
advantages
hypotheses
This
breeds
of seasonal
breeding.
species
advantages
a strong peak of
over most
of the year, but with
breeding
two months
in May-June;
the eggs hatch
about
activity

tions

precipitation

Tropidonophis

colubrid

native

hence,
reproduction
tropical
con
nest
to periods
when
optimal
are available
but not flooded
moist
soils)

year-round,
areas
and

other

by

reproductive

faunas,
squamate
to fall
along

1996).
on a small

studies

(the keelback,

force,

high

restricted

ditions

Simberloff

is sea

are

made

divergent

soils).

to pr?dation (Tinkle
availability or low vulnerability
et
and Pfeffer 1971,
Saint
al.
Girons
Tinkle
1970,
1967,
ambient
Fitch 1982); or (2) Abiotic factors?although
temperatures
in many
sonal

diversity

long-term

plausibly

Two

offspring

with

1991; see also Zim

the

and

Our

in

divergence
consistent

lines (Barbault 1976, Vitt

optimal

1991, Shine etal. 1998).

1991, Vitt and Blackburn

sympatric

been

prey

"biotic"

Australia

year

1975,

Ramirez-Bautista

1999,

et al. 2002, Aldridge

Shine

Colli

and Hooker

within

that be

espe
taxo

merman

trop

each

months

several

documented

less

they
oc

of

the

predators,
not
similarity

have

when
reverse

argued
kinds

to similar

87, No.

appears

seasonality
when

cies

They
similar

used

predict
was
and hence,
timing
comments
have
Similar

that

nomic

taxa

would

cially

year

animals.

curring
cause
of these
many
and were
vulnerable

breaks

of many

females

1974, Fleming

Griffiths

1992,

2000, Luiselli

of

times

1994). This rigid seasonality

reproducing

species

the warmest

climates,

(Gorman and Licht

Rocha

to

restricted

entirely

that preference
retaining
arid habitat,
and the

a seasonally
for mesic-habitat

studies

systems

Vol.

Ecology,

incubation

dry-soil
invaded

reproductive
their data.

(lizards
reptiles
with which

squamate
model

SHINE

hypothesis

possible.

Reproductive
and snakes)

R.

in

distributed
of

tropical

and

0.8

snout-vent

natricine colubrid

near-coastal
subtropical

habitats
Australia

(Cogger 1992), these snakes feed primarily on frogs

(Shine 1991). Female keelbacks
produce multiple

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January 2006

SEASONAL REPRODUCTION IN THE TROPICS 135

all hatchlings
marked

prior

and individually

measured,

weighed,
to release

at their mother's

site of capture.

In total, we collected 2317 individual keelbacks over

the study period (2839 captures), and released 3523
marked hatchlings. Beginning
inMarch 1999 we also
conducted nightly surveys of frog abundance at Fogg
Dam.
each
along

Ten

established
grids were
2 X 3 m sections
of

survey

encompassing
the dam wall.

Each

100 m
the road

we

evening,

apart,
surface
the

recorded

numbers and species of frogs in each grid (Brown and

Shine 20026).
air

Shaded

temperature
over
the
hourly

measured

gers

located ~1

values

were

and

relative
period

study

were

humidity
using

datalog

km from Fogg Dam. Daily

recorded

using

a rain

located

gauge

rainfall
2 km

from Fogg Dam. Beginning in July 2001 we collected

monthly soil samples in potential nesting sites along
the dam

wall.

These

were

weighed,

then

dried

and

re

Plate
1. Seasonal
over
shifts
in habitat
characteristics
season for keelback
the course of the extended
snakes.
nesting
The upper photograph
shows
the Adelaide
River
floodplain
below
the wet season
when
Fogg Dam during
(early March)
the area is inundated
and vegetation-covered,
whereas
the
lower photo
shows
the same location
late in the dry season
after a wildfire
most
has removed
and
(October)
vegetation
left bare, deeply
cracked
soil. Photo
credit: G. P. Brown.

clutches

a single

within

season,

breeding

sition from April

through November

and

6;

Shine

2002a,

see

1). Two

Fig.

with

ovipo

each year (Brown

at

nests

natural

Fogg Dam were 10-20 cm beneath the soil surface

(Webb et al. 2001). Thermal and hydric conditions dur
ing incubation strongly influence the phenotypic traits
of hatchling keelbacks, including body size, shape, and
muscular strength (Webb et al. 2001, Brown and Shine
Incubation
under
cool moist
conditions
2004).
ates larger hatchlings,
in turn have a higher
which

gener
prob

ability of survival through the first year of life (Brown

and Shine 20026, 2004).
Field methods
A
Data

in

the

present

were

paper

over

gathered

the

period May 1998 to December 2003. We surveyed the

1.3 km long dam wall for snakes on 1851 nights during
this

on

period,

an

average

of

27.2

nights

per

month

(range 4-31). We attempted to catch all keelbacks

we

encountered

then measured
at

their

palpated

on
and

site

capture
prior

the dam wall;

to

these

individuals

to release
marked
individually
prior
were
the following
Snakes
day.
to obtain

release

fecal

order to quantify feeding frequencies,

to identify
the
sumed.
Gravid
1-28

that
were

nature
females

later
(mean
days
their eggs were
release;

samples,

in

and if possible

con
the prey
that had been
were
until oviposition
retained
= 6.5
sd = 3.4)
before
days,
in the laboratory
incubated
and

of

JAS

Month
Fig.
1. Seasonality
of reproduction
in female keelbacks,
at Fogg Dam
in tropical Australia.
The
mairii,
Tropidonophis
the mean percentage
of adult female keel
upper graph shows
= 809
backs
shelled
oviductal
(total N
eggs
containing
over 5.5 years. Error bars rep
each month
snakes)
during
errors. The
resent
standard
lower graph
the dis
represents
tribution
of expected
hatch dates
of the mean
of
number
clutches
each month,
based on a two-month
incu
produced
com
bation period. Note
that the two graphs do not coincide
of monthly
because
variation
in the numbers
of fe
pletely,
males
For example,
hatch in Jan
v?ry few clutches
captured.
a reasonably
of gravid
females
uary despite
high percentage
two months
earlier (in November),
overall were captured
in November
in the year.
earlier
captured

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because
compared

very few females

to the numbers

G.136P. BROWN

to determine

weighed
Brown

2002).

monthly

data
and

analyses
values

calculated
of

index
of

Thus,
for

the

are

figures
over

moisture

presented

those

interpolated
from
the

(1991).

Soil

moisture

rainfall

and

of moisture

1.0

averages

calculated
and

to plants

0.5-1

from

estimates

the
and

(McDonald

assess

of keelback
ability
occur
in water
(as might
we
rain),
eggs
placed
heavy
stages

opmental
the end

of

varying
to moist
whether

or

1 to 30

dictions

not

lation
is

to reduce

relations,

hence

of

In

total,

and

pre

approach

correlations,

c) Body

by

the

limiting
=
of N

hatchling
authors

Many
plain

invoked

seasonality

reproductive

Saint Girons and Pfeffer

idea,

we

conservative

of

size

sample

OH

-0.1

12.

sonally,
condition

study
and

area.

First,

second,

of hatchling

such

of

to ex
(e.g.,

year

Although

mean
the onset
in frog

do

frog abundances
rates
the feeding
influenced
snakes
by

are

abundance
frog
season
of the wet

numbers

among

(Table
tistically
significant
were
cm SVL)
backs
(<35
and few were
captured
July
tober,
dition

increased

offer

sea

vary
and
frog

body
abun

in 10 survey
Fig. 2.
of frogs seen per month
(a) Number
over 1465 nights over five years; (b) monthly
grids monitored
cm SVL) keelback
rates of 458 small
snakes
(<35
feeding
over five years;
condition
from general
(c) body
(residuals
vs. ln(snout-vent
linear regression
of ln(body mass)
length)
of 458 small (<35 cm SVL) keelback
snakes over five years.
? se.
are shown as mean
in all three panels
Values

1). Because

no

captured
between

during

small

keel
or

June
and

Oc

con
body
condition

to length,

relative

(mass

linear

general

regression

residual
using
vs.
of Inmass

scores

from

In SVL)

of

the
small

(<35 cm SVL) keelbacks also did not vary among

months, but tended to be lowest during the early dry
season

twofold

(Fig. 2a), overall

was
not sta
months

August
rates
and
data on feeding
pooled
over
the August-October
Body
period.

we

A-0

for hatchling keelbacks

dance?

following
variation

Month
thus,

this hypothesis
in tropical
reptiles
times

that
(and

availability
is maximized

which

the best feeding opportunities

at our

is timed

1971, Fitch 1982). To test the

to establish

need

of small keelbacks

growth)
have

condition

-0.2

1. Oviposition
when
emerge
food

hatchlings

0.1

cor

of

A-0

0.2-,

Results
Hypothesis

rates of small keelbacks

an
used
1998). We
to adjust
the sample
overall
calculating

Peterman

means
and thereby
monthly
to a maximum
correlations

A-0

recorded

size

sample
more

them

making
and

such

time

exposure.

assumptions

"effective"

1995,
(Bence
Pyper
even more
conservative
sizes

near

of

auto
positive
I error
in corre
of Type
of compensating
for this

means

returned

we

and

the

risk

the

the

b) Feeding

hypotheses.
data exhibit

time-series

inflating
One
analyses.

0.7 -,

devel
and

lengths
were
then

eggs

to address

alternative

our

of

Some

different

for

incubation,

survived

they
us

allow

from

for

correlation,

risk

h. The

vermiculite

data

these

in water

incubation)

from

of

laid, mid-incubation,

(newly

to withstand
eggs
if a nest was flood

the

immersion
by

~~i-1?
F
J

1991).

were
over
at Fogg
Dam
recorded
temperatures
a 12-month
thermal
buried
0,
using
period
dataloggers
at two locations.
the soil surface
10, and 30 cm under

ed

a) Frog abundance

1.5

Soil

To

and McAlpine

rates,

available

87, No.

values

monthly

was

storage
evaporation

Vol.

Ecology,

2.0-1

statistical

60-year

15 of McDonald

2.5

of monthly
an additional

As

periods.

SHINE

of

years

our

on means

based

storage"

weekly
amount

Mc Alpine

five

R.

and

(Shine

to

variables;

we

in Fig.

content
two

have

above

soil moisture,

"soil

water

their
we

AND

be
but

like

rate

did

during
frog
not

vary

1). Correlation
show
surveys
young

2c).
Fig.
the dry season
and
abundance

(April-May;

lower

that

the

were
keelbacks

not

body

significantly

analyses
numbers

using
of frogs

correlated
=
10,
(N

Spearman

to

tended
(Fig.

condition,

among
mean

with

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All use subject to JSTOR Terms and Conditions

rates

Feeding
May-October

months

monthly
on our
seen

2b),

feeding
(Table
values

nightly
condition
of
body
r = -0.01,
P =

137

SEASONAL REPRODUCTION IN THE TROPICS

2006

January

Table

to examine
and biotic

1.

Results
of statistical
(ANOVA)
analysis
of keelback
and in abiotic
snakes,
activity
in this
of nesting
consequences
seasonality

nesting
fitness

variation
among
factors
that might

Variable

0.99),
P

0.20,

or their feeding
=
0.59).

These
a

be

df

frogs
months,
may
will

10,

r =

Spearman

that prey
young

availability
keelbacks.

to be more

not

may

prey

In fact,

vember.

few

1). This

(Fig.
falsifies

hatching

(December-January)
of nests
laid
are

clutches

mismatch

we

at

between

this

time

2. Oviposition
is timed
that
such
when
risk (and
thus,
pr?dation
is minimized
hatchling
mortality)

Hypothesis
hatchlings

Neonate

are

keelbacks

3.8 g) and nonvenomous

and thus,
en by a wide
of predators
waterbirds,
variety
including
and varanid
lizards.
the most
snakes,
Hence,
important
of the optimal
determinant
of oviposition
timing
might
to produce
be
snakes
young

provide
at different

snakes

hatching

(7-mo)

emergence
we have

ple sizes
between
(Fig.

October

3). This

significantly

were

these

for hatchlings
when
numbers

larged

periods

comparison.
did not differ

(Table

1). Neonates

3. Oviposition
rates
of

the

higher

reproduction

rates

of

to produce

their nesting activity

recapture.
hatchlings

If females
during

timed
this

is timed
egg

such

that
are

pr?dation

eggs

are

low

drive
reproductive
to oviposit
at times
risk from predators.

to a range

vulnerable

at

teeth

bladelike

the

rear

I/

g
B
?? 4*^ 3- T

of mammals

of

the maxilla

that

1\
\

I
\ 1

2
1
Jul

their

Fig.
backs

period,

should peak in July (allowing

year

fluctuations

snake
cucullatus.
slatey-grey
Stegonotus
at Fogg
to a phy
this species
Dam,
belongs
in which
is frequent,
and S.
lineage
oophagy
such as en
possesses
adaptations
egg-eating

released during September had slightly but nonsignif

icantly

are

abundant

seasonal

unlikely.

when

nests

impor
(wading

8-1

low

and

are

thus

our

varanid
G. P.
bandicoots,
lizards;
reptiles
(e.g.,
Brown
and R. Shine,
but the most
data),
unpublished
an oophagous
be
colubrid
may
important
predator

for

periods

(5.2%)

are

pressure

the most

and

released
were

and

site,

therefore
with

keelbacks

rates of egg pr?dation

High
might
with
females
favored
seasonality,
are at less
of year when
their eggs

the prolonged
sam
acceptable

data

low

among

within

To maintain

January,
four time

leaves

rates

Recapture

times

period.
combined
and

study

at times
of year when
the
to survive.
Our mark
likely
rates
estimates
of survival
of

hatchlings
are most

data

recapture

snakes,

Keelback

and

case,

inconsistent

hypothesis
with
this conclusion,

at our

logenetic
cucullatus

(9.5-17.0

the
as

round

Abundant

cm SVL,
0.8
are eat
presumably

small

is not

This

birds,

snake,

emerge

of freedom

(degrees

of hatchling
predators
and varanid
lizards)

laid

and
prediction
seasonal
of
timing
food
availability

<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
0.31
0.001
0.02
0.42
0.18
0.96
0.69
0.49
0.38

the

reject
In keeping

data.

Hypothesis

of

years

incubation).
can

would

in October-No

laid

the hypothesis
that the
to maximize
has evolved

oviposition
for hatchlings.

2-mo

in predator

the year. Ad
throughout
was
to coincide
timed

frequently

0.4

eggs

tant potential

Although
the wetter

abundant
during
common
Thus,
they
year-round.
frogs
remain
abundant
that young
keelbacks
sufficiently

if keelback
ditionally,
with
abundance
frog
to see a majority
expect

data

were

encounter

year

(N

1, 51
1, 42
42
42
56
19
19
19
1, 46
1, 56
1, 46
7, 29
7, 29
3, 14

were gathered
over periods
of 2-5
for which
data were obtained).

we

suggest
factor
for

analyses
limiting
tended

rates

in
the

species.

of females
11.2
Proportion
gravid
5.6
air temperature
Daily maximum
air temperature
9.7
Daily minimum
air temperature
17.7
Daily mean
Rainfall
19.2
Maximum
1.3
soil moisture
Minimum
5.0
soil moisture
Mean
soil moisture
2.8
Abundance
of frogs
1.1
Abundance
of slatey-grey
snakes
1.4
snakes eating keelback-sized
of slatey-grey
Proportion
keelbacks
condition
of hatchling
0.7
Body
of hatchling
keelbacks
with food 1.0
Proportion
keelbacks
1.1
of hatchling
Proportion
recaptured
Note:
Data on these variables
are based on number
of months

months
affect

3523

3.

hatchlings

rates

Sep
?

Oct-Jan

(mean
se) of marked
baby keel
calculated
from 183 recaptures
of
period,
over five years.
released

Recapture

by hatching

-1-1-1-1
Aug

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All use subject to JSTOR Terms and Conditions

138 P. BROWN
G.

AND

22

did

snake abundance

a) Slatey-grey

R.

SHINE

not

vary

(Fig. 4b),
in on keelback
are

eggs
of

16

keelback

dation.
14
12

are

10H

potential

M
0.6 -,

seasonality

in occurrence
data).

rates of slatey-grey

snakes

thermal

case

but

hatching,

type of the young

size,

only

also

many

2004).

Brown

significant
that air
whereas
mer
numbers
of slatey-grey
snakes
(Ste
(a) Monthly
= 756 over five
(b)
(N
cucullatus)
gonotus
caught
years);
of slatey-grey
snake fecal samples
(from
monthly
proportion
=
a total TV
All
keelback-sized
246)
eggshells.
containing
? se.
are shown as mean
values

soil

that

the

to penetrate

function

eggs
in our

P. Brown

(Shine
1991).
leathery
eggshells
iden
of all prey
items
>20%
comprise
at Fogg
Dam
studies
of S. cucullatus
(G.

and

R.

Shine,

some

of

ards,

the vast majority

these

unpublished
small
and

are

eggs

feces

unambiguously
The most
plausible

that

times

of year

(1)

than
of

numbers
did

not

eggs

would

shifts

at others.

wall

ble

1), but (2) numbers

significantly

in

variation
be

in habitat

keelback

Contrary
snakes

slatey-grey

dam

vary

seasonal

if slatey
use or diet

eggs

some

at

to this prediction,
on the
encountered
among

months

tended to be highest

(Ta

during

period
snake

to the keelback
nesting
corresponding
of
the
The
4a).
slatey-grey
proportion
(Fig.
on
of keelback
diet
(as based
eggs
composed

shells

in the feces

May-September,

of

recently

captured

specimens).also

studies

have

are optimal
thus,

(and

the

Hence,
be

might

restrict

the year

could
be
(or both)
mean
values
reveal

5b).

these

Reflecting

(Fig. 5c)
nest
sites

soil water

also

vary

1). Correlation

(Table

climatic

and

pat
content
the

through

reveal

analyses

relative

not

ilar

snakes.

for

fewer

contain

they

Although
to liz
belong
in Stegonotus

of eggshells
to keelback

belong
reason

on keelback
rates
pr?dation
show
snakes
seasonal
grey
such

data).
likely
found

body
2001,

of nesting
1)
intensity
activity
(Fig.
to either
related
maximum
air tem
monthly
=
r = -0.20,
or
P = 0.53)
12, Spearman
(N
perature
=
mean
to monthly
air temperature
12, Spearman
(N
r = -0.46,
P = 0.14).
relative
of
However,
intensity
was
re
(and
nesting
activity
significantly
inversely)
=
to monthly
lated
minimum
air temperature
12,
(N
=
=
r
P
and to monthly
rain
-0.83,
0.001)
Spearman
=
r = -0.94,
P < 0.0001).
fall (N
Sim
12, Spearman

was

Reptile
tified

(Fig.

temperatures
in potential

5d)
(Fig.
course
of

et al.

5a),
mid-year
(Fig.
concentrated
in the midsum

is highly

season

wet

suc

of

availability.

rainfall

terns,

the
species,
a
keel
by

larger

reproduction

are

eggs

its overall

hatchlings.

or moisture
temperature
in this respect.
Monthly
are
lowest
temperatures

Either

4.

2004)

Shine,

the pheno

Webb

generating

Shine

of keelback

peak period
ed by nest

Fig.

and

of

aspects

Experimental
moist
conditions

that relatively
cool,
keelback
incubation,

fitter;

the

optimal

reptile

strength;

R.

that

are

snake (including

Shine

and

experienced
its probability

not

shown
for

pr?
of

the
support
Varanid
lizards

such

other

and muscular

shape,
and

Brown

is timed

conditions

hydric
can
affect

egg

cessful

egg

to

fail

conditions

for many

and

back

also

(G. P. Brown

4. Oviposition
incubation

the

timing

of

abundance

hypothesis.

when

is

on

predators

unpublished

As
b) Feeding

are

Hypothesis
laid

rates

reduce

but especially
year-round,
of keelback
(the peak period
nesting).
seen
no clear
in the area, with
rarely

season

in the dry
Bandicoots

6H

not

egg pr?dation"
on the dam wall

active

the observed

1). Thus,

observations

Qualitative

other
only
"seasonal

months
but peaked
in
snakes
slatey-grey
key
most
time when
keelback

the

(Fig.
does

nesting

that

suggesting
at
eggs

incubating

87, No.

among

significantly

June

20

Vol.

Ecology,

correlation

strong

soil
temperature
P = 0.004)
but no

monthly
-0.76,

and

activity
=
-0.22,
Thus,

lowest
Figs.

soil
=

is scarce
relation

for
analyses
between
nesting

link

water

soil

(N

parameters

activity
=
12,

relationship
=
content
(N

and

showed
minimum

r =
Spearman
between
nesting
12,

Spearman

0.50).

occurs
when
rainfall
by keelbacks
are
cor
low.
The
temperatures
relatively
are
is less than perfect,
however:
temperatures

peak
and

nesting

in July

but

1 vs.

5a),

but
September
of
the
part
dry

is rare at that time

nesting
(compare
and rainfall
is low from May
through
in the earliest
is concentrated
nesting

season

(May-June;

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All use subject to JSTOR Terms and Conditions

compare

Figs.

1 vs.

139

SEASONAL REPRODUCTION IN THE TROPICS

2006

January

Month

Month

in thermal and hydric

at Fogg Dam:
variation
conditions
air temper
and maximum
(a) daily minimum
Monthly
were
and (d) soil water
content.
Data
for soil temperature
available
for only one
(b) rainfall;
(c) soil temperatures;
? se. In (d) the soil moisture
are shown
as mean
was
values
year, but for all other variables,
percentage
(open circles)
measured
from monthly
the soil moisture
soil samples
from Fogg Dam;
index (solid circles) was taken from McDonald
and
(1991: Fig.
15).
McAlpine
Fig.

5.

atures;

water

Soil

5b).

content

is higher

latter

pattern

ation: flooding.
experience

logged
To assess
inundation

rain

different
each

the

additional

wet

and
that

of

ability

two mid-incubation,
eggs
rates were

near

two
1 and

survived
50%

after

8.5

4 h

are likely to

5b,d),
(Fig.
in water
drown

keelback

the

(two

end

h; 67%

1-30

h.
laid,

newly

of

incubation).

but mortality
12, 17.5, and 21

immersion,
after

h; and 100% after 25 and 30 h. The egg's stage of

development did not affect its probability of survival;
a multiple

logistic
variable

pendent

significantly
(X2

8.57,

regression
showed
that

affected
1 df, P

did not
development
=
teraction
0.83,
x2

possibly
until

nesting
and 5b,d).

the

as

survival

the duration

the probability

of

explaining
cessation

for more
keelbacks
why
of monsoonal

the

de

immersion

in

eggs

are

do

not

(Figs.

from

these

that

invoke

ductive

and disadvantages
of reproduction.

egg

analyses
biotic

pr?dation

abiotic

prey
at

factors

cies,

and

keelback

forces

availability,

and

with

inconsistent

as

ideal

our
nesting

field

coincides

factors
Instead,

in keelbacks.

nesting

incubation
data

as

such
survival

predic
as causal
our

from the hypothesis

imental studies identify cool, moist

sites

Results

paradigms
for repro

Factors

times

constrain

year.

reptiles.

these
hypotheses
invoking
on reproductive
cyclicity.

support predictions

nest

of

enhances
associated

either did not vary through

for hatchlings

or peaked

from

costs

selective

in tropical
rates,

further

conventional

challenge
as
factors

seasonality

broadly

ideal

hypotheses
associated
with

schedules

over five years)

hatchlings,
produced
our
or
to
detect
any benefits
ability
at
with
different
times
reproduction

influences

begin

an

offer

In partic
a clear
of nesting
dates
but with
range
us to compare
the fate of hatchlings
1) allows
peak
(Fig.
at different
from
clutches
times
of year. Our
produced
set (809
data
clutches
3523
unusually
large
totaling

tions

of

stage
0.15;

snakes
alternative

the broad

the year,

than about eight

rains

seasonal

probabilities

of egg mortality

but that an egg's

0.003)
=
2 df, P =
3.87,
(x2
=
2 df, P
Thus,
0.66).

likely to die if submerged

hours,

with

keelback
respects,
to test
with which

system
the advantages

study
about

ular,

of

eggs

submerged
in water
for

eggs

several

different

to withstand

eggs

we

In

consider

substrate

varying
periods,
of development
stages
we used
time period
six

All

abiotic

they might

for

Discussion

(Fig. 5d). The

period

laid prior to May

Eggs

heavy
the possibility
nests.

raising

At

an

suggests

season

the wet

during

than during the peak breeding

with

This content downloaded from 200.18.33.232 on Thu, 20 Mar 2014 12:09:05 PM

All use subject to JSTOR Terms and Conditions

that

that

Exper

(but not flooded)

environments

show

data

the

for
peak

the availability

this

spe

of
timing
of such

140 P. BROWN
G.

conditions.

That

when

the

when

soil

soil

but

about

hypotheses

failed

the

For
seasonality.
that reproductive

heavy

are

temperatures
we
have

Inevitably,

nest

is, keelbacks
is moist

AND

the period
during
rain is unlikely,
and

low.
relatively
to consider

other

output

concentrated

both
in time and space because
of benefits
to predator
satiation
Barbault
1967,
(Janzen
are most
to survive
That
is, hatchlings
likely

related
1975).

in a

hatch

they

even

escape

if

Unlike

hatching.

so

group,

large
there
the

reviewed

hypotheses

both

occurring
R. Shine,

Contrary
site are not

entire

sea

synchrony
weeks
and months

wall

(G. P. Brown

a temporal
to generate

On

satiation

predator
at a scale

instead

concentrated,

spatially
dam

data).

unpublished

expect

might

the

along

the

above,
predict
selection

that
will
only
and spatial
concentration
of nest
to this prediction,
nests
keelback

temporal

ing activity.
at our study

not

does

if

inevitably
soon
after

pressure

satiation"
"predator
hypothesis
sonal
of reproduction,
timing
favor

that many

is predator

scale,

hours

seen

How
reptile
erable
ality

are

general
species

this

(Fig.

looks

phenomenon

determinants

with

this
However,
seasonality.
in theory,
in a way
least
are
There
testing.
empirical

to further

why
sympatric
even
if in all
times,
that

conditions

(incubation)

inconsistent

at

reasons

three

at different

duce

to be

(either biotic or abiotic) for the

of reproductive
resolved

is easily
paradox
that is amenable
least

there

restrict

taxa might
repro
cases
it is abiotic
their

incubation

fer

and

among
species,
in incubation

gence
In an

area

with

ture content

and

embryonic

can

generate

dif

physiology

diver
significant
Badham
1971).
(e.g.,
in soil mois
variation

requirements
seasonal

strong

taxa with
Fogg Dam),
differing
hydric
at different
to breed
would
be
forced

(like

requirements
times
of year.
respect
careous

involves

(Bauer

1992a,

the
in

shell

most

The

dramatic

evolution

some

of

of
lineages
and Russell

to

reduce

Shine

can

hold

desiccation

pythons

Thompson

1999).

et

al.

so
5a),
Fig.
water
allows

1996:

secure

locations

from

flooding

(G.

P. Brown

and

R.

Shine,

data).
unpublished
selection
2) Nest-site
that

slatey-grey
tree snakes

con
can modify
the physical
nest.
For
in
the
eggs
example,
experience
and golden
snakes
cucullatus)
(Stegonotus

at Fogg
punctulatus)
(Dendrelaphis
season
nest
rather
than the dry season
in the wet
and R. Shine,
1991; G. P. Brown
unpublished

Dam

1996?,
the

that

condi

1999a).

Attend

off

a flooded

eggs

from
parental
protection
to exploit
optimally
of their eggs.

vs. oviparity)
pro
(viviparity
conditions
experienced
by
an tgg
Inside
the maternal
uterus,
developing
embryos.
to relatively
is exposed
constant
water
and high
po
tential
of seasonal
in soil water
variations
independent
mode

Reproductive
modifies
foundly

content

the abiotic

et al.

(Packard

Maternal

The

ectothermy)
environmental

optimize)

to a sub

to

embryo

1993),

(and

regulate
of

temperatures

their

rather

viviparous

er

abiotic

also

can

risks

than

taxa
et al.

(Bolton

than

aseasonal

(Shine
1982),

influence
as

such

of

the causal

en

likely

especially
reflects
biotic

rath

as

such

parental
Adaptations
to
the offspring's
vulnerability
and
starvation
(via pa
pr?dation

and

conditions

in

reproduction

1986),

factors.

protection

that

can
biology
a developing
conditions.

of reproductive
adaptations
the vulnerability
buffer
of
variable
incubation
seasonally

tropical
dotherms

hydric

can

mammals)

developmental

seasonal

rental

al.

(Farmer 2000, 2003).

significantly

Hence,

thermal

(en
regulation
buffer
embryos
endothermic
Thus,

variation.

birds,

(pythons,

1977).

the

body-temperature
can further

vs.

against
parents
hence

of

mode

dothermy

pect

buffer

experienced
by developing
embryos
et
Peterson
1987,
(Peterson
degree
not entirely
et al. 2004).
(Lourdais

albeit
5)

and Gibbons
can

also

thermor?gulation

regimes
stantial

Tinkle

1977,

but

feeding)

likely will be less buffered

the

nest-site

pythons
incubation

for

temperatures

4)

biotic

Presum

punctulatus
also.

of the clutch
in dry
conditions
in water
Embryonic
development
more
in relatively
hot
effectively
season
of
the
late
(Shine
typical
dry

2003).

proceeds
as are

conditions,

cal

con
from
substratum
hydric
independence
seasons
a
wider
of
allow
range
egg-laying
might
are laid in elevated
if the eggs
in such
taxa, especially

ably,
ditions

ditions

and

pythons

et al.

(Aubret

care

lizards

gekkonid

them

substratum (Barker and Barker 1996) and/or coil tightly

this

in

divergence
a water-resistant

for

modify

(Madsen

In summary,
structure,

of D.

true

be
can

behavior

female

ing

timing:
1) Eggshell

habits

will

ameliorate

offspring

reproductive

arboreal
same

constraints.
For
climate-imposed
water
at
nest
Liasis
Dam
example,
pythons
fuscus
Fogg
season
late
in the dry
and fe
(September-October),
males
remain
with
their
clutch
generally
throughout
tions,

high

most

Although

and

87, No.

of S. cucullatus
suggests
monitoring
nest
in the hollows
of standing
trees,
risk of flooding
et al.
any
(Brown

the

Parental

3)

we

tropical
is consid
seasonally,
season
in reproductive
diversity
a single
area (Barbault
1976). At first

any single hypothesis

at

results?

reproduce

interspecific
even within

sight,

our

that

desiccation

1).

females

suggest

Vol.

Ecology,

eliminating
The
highly

and

hatching
than the

or days
rather
at Fogg Dam
in keelbacks

of

that most

2005).

that modify
reproductive
authors
have
many
suggested
a population
within
be
may

SHINE

Radiotelemetric

thus
some

factors

example,

R.

incubation.

biotic

overall,

than will

factors

the thermal and

we

Hence,

might

ex
sea

factors

generating
reproductive
to
in tropical
will
differ
sonality
organisms
according
of
features
outlined
above.
the kinds
reproductive

Many
(probably
with
ectotherms
care,
ations

(Shine

gimes)
seasonal

data).

as

and

for

in hydric
be
may

most)

tropical

eggs
water-permeable
taxa we
that
such
expect
conditions
the most

of egg
timing
calcareous
eggshells,

are oviparous
no parental

organisms

(and
important

production.
parental

This content downloaded from 200.18.33.232 on Thu, 20 Mar 2014 12:09:05 PM

All use subject to JSTOR Terms and Conditions

and

seasonal

thermal
perhaps
on
constraints
However,
care,

traits

viviparity,

vari
re
the
such
and

SEASONAL REPRODUCTION IN THE TROPICS 141

January2006

less
organisms
increasingly
in ambient
environmental
variations

will

endothermy
vulnerable

render

to such

This
shift to a great
potentials.
rather
than abiotic
factors
may
For
features.
endo
example,

and water

temperatures
er importance
be reinforced

of biotic
other

by

an animal's
thermy
compromises
term
of
(because
energy
storage

for

capacity
extensive

et al.
Bonnet
thermor?gulation;
physiological
cannot
the sea
endotherms
dissociate

impede

Hence,

1998).

of feeding
from
the sea
intake)
(energy
as
of reproduction
timing
(energy
expenditure)
as
can
et
In
ectotherms
al.
this
(Bonnet
1998).
readily
to act as "income
endotherms
be forced
situation,
may
sonal

timing

sonal

such

breeders",

that

their

seasonal

of offspring
timing
seasonal
of
by
availability
or her
the reproducing
female

is constrained
production
resources
food
for either
offspring

et al.

Bolton

(e.g.,

1982,

and Millar

Duquette

1995).
are

there

sumably

of tropical
diversity
reptiles,
for which
species
reproductive

immense

is the result

sonality
see

(e.g.,

of biotic

constraints
phylogenetic
ductive
in some
timing

are

a broad
taxa.

of

in

groups

of

expected

a priori.
constraint

portant

taxa,

physical

Thermal

at

true

for

to hold

temperate-z?ne
season

similar

than

in most

these

two

would

be

a more

are

conditions

than moisture

rel

for

driving
reproductive
of habitats,
in
and

be more

may

the

breed
reptiles
conditions

appears
likely
as well
as
tropical

the processes
two
these
types

Similarly,
in repro

variation

that

im

cool-climate

and the high

in such
of viviparity
systems,
frequency
areas
removes
(Shine
2002)
any significant
presumably
role for ambient
conditions.
None
regulatory
hydric
even

theless,
itats,
may

especially
be a major

in relatively
cool and highly
seasonal
hab
in the arid zone,
of rainfall
seasonality
on

influence

seasonal

patterns

of reptile
there may

1988,
Thus,
(Andrews
1991).
reproduction
be strong
between
the forces
parallels
driving
ductive
in tropical,
and
arid-zone,
seasonality
ate-zone

reptile

of embryonic

species.

emphasizes

requirements
the intimate

bryogenesis

on

incubation

In

the

turn,

the

central

repro
influence

reproductive
of
dependence
conditions

seasonality
em
reptilian
available

for

(Deeming 2004).

their

thank E. Cox
continued

ideas, assistance,
by the Australian

Hill Farm for

of Beatrice
and C. Shilton
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SEASONAL REPRODUCTION IN THE TROPICS 143

January2006
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