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Energyversusrisk:Costsofreproductionin
free-rangingpythonsintropicalAustralia
ArticleinAustralEcology·June2008
DOI:10.1111/j.1442-9993.2000.tb00073.x
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Austral Ecology (2000) 25, 670–675
Energy versus risk: costs of reproduction in free-ranging
pythons in tropical Australia
THOMAS MADSEN AND RICHARD SHINE*
School of Biological Sciences, University of Sydney, New South Wales 2006, Australia
(Email: [email protected])
Abstract Data from a 12-year field study have allowed us to quantify ‘costs of reproduction’ in a natural population of water pythons (Liasis fuscus) in tropical Australia. Both sexes of pythons cease feeding during the reproductive season. For males, this involves fasting for a 6 week period. Adult males lose weight rapidly over this period
(approximately 17% of their body mass) but regain condition in the following months, and do not experience
reduced survival. In contrast, reproductive adult females cease feeding for 3 months, lose an average of 44% of
their body mass over this period, and experience increased mortality. A causal link between reproductive output
and reduced female survival is supported by (i) a decrease in survival rates at female maturation; (ii) a correlation
between survival rates and frequency of reproduction, in a comparison among different size classes of adult pythons;
and (iii) a lowered survival rate for females that allocated more energy to reproduction. Hence, both sexes experience substantial energy costs of reproduction, but a relatively higher energy cost translates into a survival cost only
in females. Such non-linearities in the relationship between energy costs and survival costs may be widespread,
and challenge the value of simple energy-based measures of ‘reproductive effort’.
Key words: feeding, growth, Liasis fuscus, life-history, reproductive effort, reptile, snake, survival.
INTRODUCTION
When an organism reproduces, it may experience substantial ‘costs’ in terms of its energy balance and potentially, its probability of survival (Williams 1966; Bell
1980; Bell & Koufopanou 1986; Madsen & Shine
1993). Mathematical models suggest that the form and
magnitude of such costs, and their relationship to the
level of reproductive output, can influence the evolution of life-history traits such as age at maturation,
reproductive effort, and the relative allocation of
resources between growth, storage and reproduction
(Williams 1966; Hirschfield & Tinkle 1975; Bell
1980; Madsen & Shine 1994). Although the notion of
costs of reproduction is a simple and intuitively
reasonable one, such costs have been quantified under
natural conditions for relatively few types of organisms
(Reznik 1985; Schwarzkopf 1994). This dearth of
information reflects logistical difficulties in overcoming problems, such as the tendency of viability differences among individuals to generate positive rather
than negative correlations between reproductive output and associated costs (van Noordwijk & de Jong
1986). Also, the situation is complicated by the fact
that not only can reproductive costs accrue in two different currencies (i.e. mortality and/or energy), but that
organisms can modify their behaviour so as to change
*Corresponding author.
Accepted for publication March 2000.
the relative magnitude of these different cost components (Bauwens & Thoen 1981; Brodie 1989).
Some authors have argued that we need to estimate
costs by measuring the underlying genetic covariances
among traits, rather than simply measuring phenotypic
traits (Reznik 1985), but this approach is difficult to
apply to many natural systems. Ideally, measures of
reproductive costs should incorporate experimental
manipulation to decouple pre-existing correlations
between reproductive expenditure and costs (Bell &
Koufopanou 1986; van Noordwijk & de Jong 1986).
Although several authors have successfully manipulated
reproductive expenditure in the field and quantified the
consequences of that perturbation (Sinervo et al. 1992;
Gustafsson et al. 1995), such techniques are difficult
to apply to most field situations. For many kinds of
organisms, the only feasible approach would be to rely
on correlational evidence in order to document the
approximate form and magnitude of different types of
costs of reproduction. Current theoretical debates
about the evolution of reproductive effort identify such
information as crucial in choosing between alternative
models (Shine & Schwarzkopf 1992; Niewiarowski &
Dunham 1994). In particular, we need to understand
more about different currencies of reproductive cost,
and the relationship between them. For example, under
what conditions is high energy expenditure on reproduction associated with reduced survival? Our
long-term studies on tropical pythons provide an
opportunity to investigate questions such as these, in
a study system very different from any of those in which
these topics have previously been explored.
COS T S OF R EP ROD U CT I ON I N S N A KES
METHODS
Study species and area
Water pythons (Liasis fuscus) are large (up to 3 m and
5 kg) non-venomous snakes that occur over a wide area
of tropical Australia (Cogger 1992). They are very
abundant in our study area on the Adelaide River floodplain, 60 km east of Darwin in the Northern Territory.
Our previous papers on this system have described the
climate, topography and environment (Madsen &
Shine 1996a). The area is in the wet-dry tropics; it is
hot year-round but rainfall is concentrated in a 4 month
wet season (December to March), with resultant seasonal flooding.
The water pythons in this area feed primarily on the
dusky rat (Rattus colletti), a native rodent that exhibits
massive annual fluctuations in abundance depending
upon local rainfall patterns (Redhead 1979; Madsen
& Shine 1999a). Reproductive rates of the pythons vary
considerably among years, with rat abundance determining python feeding rates, body condition, and the
proportion of adult-size female snakes that reproduce
each year (Shine & Madsen 1997; Madsen & Shine
1999b). Despite their extensive seasonal migrations,
radiotelemetric monitoring shows that adult pythons
of both sexes are highly philopatric (Madsen & Shine
1996a). Indeed, during the dry-season, <1% of adult
snakes have been recorded moving among different
areas, separated by 2–4 km, even within our main study
site (Madsen & Shine 1998a).
Both male and female pythons reach sexual maturity at a snout–vent length (SVL) of approximately
140 cm (Madsen & Shine 1998a). Reproduction is
highly seasonal. Mating occurs in the middle of the dry
season (July to mid-August), and the eggs are laid about
a month later (Madsen & Shine 1996b; 1998c).
Females reproduce, on average, once every second year,
but with substantial variation due to body size, local
food availability, and nest-site location (Shine &
Madsen 1997; Madsen & Shine 1998c; 1999b).
Reproductive (pre-ovulatory, gravid or immediately
post-ovipositional) females are easily recognizable by
body shape during the months of July, August and
September (Madsen & Shine 1996b). Eggs are laid in
the burrows of varanid lizards, or in the root-boles of
paperbark trees (Shine et al. 1997; Madsen & Shine
1998c). Some but not all females attend their eggs
throughout the 2 month incubation period, and may
use shivering thermogenesis to maintain high constant
incubation temperatures (Shine et al. 1997).
METHODS
The pythons were caught at night by spotlighting (on
foot, or from a slowly moving vehicle), and released the
671
following day after they had been measured, weighed,
sexed and individually marked for later recognition.
Between 1987 and 1998, we collected and marked
5327 pythons. An additional 1224 hatchlings were
incubated in captivity and subsequently marked and
released. The feeding rates of pythons were determined
from faeces production; newly captured pythons enthusiastically provided faecal samples when handled.
Experience with captive snakes indicated that if a
python did not produce faeces, and none could be palpated from its lower gut, then it had not fed for a period
of at least 1 week. In 1991 and 1992, we retained 116
gravid females in captivity until they produced eggs.
The post-ovipositional females were then re-weighed
and released (Madsen & Shine 1996b). For these
females we examined the relationship between reproductive output and the probability of subsequent
recapture. To exclude short-term records, we treated
an animal as being recaptured only if the two capture
events were separated by >365 days.
RESULTS
Recapture rates
From 1987 to 1997 we captured and marked 2844
male pythons. From 1988 to 1998, 985 of these
animals (34.6%) were recaptured. During the same
period we captured and marked 2136 females, but only
519 (24.3%) of these animals were recaptured. The
recapture rate of male pythons was significantly higher
than that of females (x2 = 61.8, P = 0.0001, d.f. = 1).
Subdividing the data shows that the difference between
sexes was restricted to adult life; recapture rates of
subadult males were similar to those of subadult
females (x2 = 2.51, P = 0.11, d.f. = 1) but differed significantly between adult males and adult females (x2 =
71.0, P = 0.0001, d.f. = 1; Table 1). Recapture rates of
males did not differ between subadults and adults
(x2 = 1.33, P = 0.25, d.f. = 1), but adult female pythons
were significantly less frequently recaptured compared
to subadult females (x2 = 33.03, P = 0.0001, d.f. = 1;
Table 1).
Table 1. Recapture rates of water pythons (Liasis fuscus) of
different sexes and body sizes. Both sexes mature at approximately 140 cm snout-vent length
Age
Males
Total Recapture (%)
Females
Total Recapture (%)
Subadult
Adult
959
1885
660
1476
36.1
33.9
Each animal appears only once in the table.
32.3
20.7
6 72
T. MADSEN AND R. SHINE
We calculated recapture probabilities for adult
pythons of both sexes known to have been alive (due
to subsequent recapture) for recapture intervals ranging from three to 11 years (Table 2). A contingency
table analysis indicated that males and females did not
differ significantly in overall catchability (x2 = 0.40,
P = 0.52, d.f. = 1). Thus, the overall sex difference in
frequency of recapture presumably reflects sex differences in survival rates rather than catchability.
The size range of adult female pythons was divided
into six 10 cm cohorts (140–149 cm to >190 cm SVL).
From each cohort we calculated the proportion of
snakes that were gravid and the proportion that were
recaptured. These proportions ranged from 10.7% and
26.5%, respectively (for snakes of 140–149 cm SVL)
to 58.3% and 15.9%, respectively (for snakes of
180–189 cm SVL). Cohorts with a higher proportion
of gravid females had lower recapture rates than did
cohorts with lower proportions of gravid females (r =
0.86, P = 0.03, d.f. = 5; Fig. 1). There was no significant correlation between recapture rates and average
body-size of snakes within the six cohorts (r = 0.66,
P = 0.15, d.f. = 5).
males initially captured in early July and then recaptured in mid August lost, on average, 16.7% (SE =
0.81) of their initial body mass. However, once the
males commenced feeding after the mating season they
regained condition rapidly, and soon attained the same
body mass they had displayed at the onset of the reproductive season (Fig. 3). The recapture rate was not
affected; indeed, males that lost relatively more mass
over this period (mean 17.4%, SE = 0.9) were slightly
more likely to be recaptured than those that lost less
(mean 14.6%, SE = 1.7). However, logistic regression
(with rate of mass loss as the independent variable and
‘recapture or not’ as the dependent variable) showed
that this difference was not statistically significant (loglikelihood ratio test, x2 = 2.40, 1 d.f., P = 0.13).
Because reproductive females ceased feeding over a
much longer period than did conspecific males, they
underwent a much greater reduction in body mass. For
seven reproductive females, initially captured in early
Feeding rates
Male pythons exhibited a reduced feeding rate during
the 6 week mating season (July to mid-August; Fig. 2).
Reproductive females did not feed during the entire
3 month reproductive period, from mating until oviposition (July to September; Fig. 2). Of the 564 capture
records of reproductive female pythons, only two provided faecal samples. Both females were captured in
early July, the onset of the mating season. The low feeding rate among reproductive pythons cannot be due to
a lack of prey, because non-reproductive animals had
often fed when captured during this period (Fig. 2).
Cessation of feeding by the snakes translated into a
precipitous decline in body condition. The 28 adult
Table 2. Proportion of adult male and female pythons that
were recaptured during an intervening period of 3–11 years
during which they were known to be alive (based on subsequent recaptures)
No.
years
Males
Total Recapture (%)
3
4
5
6
7
8
9
10
11
99
106
65
39
24
15
8
10
3
16.2
37.7
47.7
66.7
70.8
80.0
37.5
80.0
100.0
Fig. 1. Reproductive frequencies in female water pythons
(Liasis fuscus) compared to the rates at which female snakes
of those size classes were recaptured.
Females
Total Recapture (%)
57
36
30
29
20
11
0
2
0
10.5
36.1
43.3
65.5
60.0
72.7
0
100.0
0
Fig. 2. Feeding rates of adult water pythons (Liasis
fuscus) July–September as a function of sex and reproductive
status (>99% of the gravid females were captured during
this period). Numbers denote sample sizes for each group.
j, Gravid females; , non-gravid adult females; h, adult
males.
COS T S OF R EP ROD U CT I ON I N S N A KES
3.
Fig. 3. Rates of change in body mass (and associated SE)
of adult male water pythons (Liasis fuscus) relative to their
mass at the onset of the mating season. Numbers denote
sample sizes for each group.
to mid-July and then recaptured shortly before oviposition in mid-September, mass loss averaged 10.6% of
their initial body mass (SE = 1.46). However, this
figure underestimates actual mass loss, because the
oviductal eggs would have increased substantially in
mass (due to water uptake; Naulleau & Bonnet 1996)
over the same period. Of the 116 females retained in
captivity, 57 were captured in mid-to late September.
The mass of these females fell considerably at oviposition. The average mass loss at this time (mass loss
divided by prepartum mass) for these females was
33.2% (SE = 0.4). Hence, the total mass loss of reproductive females (the sum of these two components)
averaged 10.6 + 33.2 = 43.8%. That is, female pythons
lost almost half of their body mass during reproduction. In contrast to male pythons, a logistic regression
revealed a link between reproductive expenditure and
probability of recapture. Females that were never recaptured after they reproduced (and hence, may not have
survived) had higher average mass loss at oviposition
(34.2%, SE = 0.5) than those females that were later
recaptured (mean mass loss 31.6%, SE = 0.3; loglikelihood ratio test, x2 = 16.4, P = 0.0001, d.f. = 1,
with recaptured versus not recaptured as the dependent
variable and proportional body mass reduction at
oviposition as the independent variable).
DISCUSSION
We suggest that the high mortality rates of adult female
pythons reflect a higher cost of reproduction in females
than in conspecific males. This hypothesis makes a
series of predictions that we can test with our data.
1. Male and female pythons should display similar
recapture rates prior to maturation, but different
rates after maturation.
2. Recapture rates of males should not differ between
juvenile and adult life, whereas adult females
should be recaptured less frequently than juvenile
females.
673
Because the frequency of reproduction shifts
among size-classes of adult female pythons
(Madsen & Shine 1996b), we expect that recapture
rates should be lower for size-classes with higher
reproductive frequencies.
Our data support all of these predictions (Table 1;
Fig. 1). Potentially, reproduction might reduce the
probability of survival of a snake for several reasons.
Starvation and predation, or a combination of these two
factors, would seem to be the most likely. In support
of this hypothesis, we recorded the deaths of five reproductive females during our study. Three of the snakes
apparently died of starvation as no overt injuries were
visible on their emaciated bodies. Varanid lizards killed
two other female pythons when they were basking outside their nesting holes in the later stages of brooding.
Both of these snakes were also in extremely poor
condition (Madsen & Shine 1999b). Survival rates of
juvenile pythons are also linked to food supply; cohorts
that hatch in years with low prey availability experience
very high mortality (Madsen & Shine 1998b).
A python can be in poor energy balance after reproducing, either because it has expended a great deal of
energy directly on reproduction (as measured by relative clutch mass), and/or because it has failed to gather
sufficient energy (due to decreased rates of feeding during the reproductive season). Because many snakes do
not feed during reproduction (Shine 1980; Madsen &
Shine 1993), this ‘opportunity cost’ component might
be important for both males and females. The rapid
decrease in body mass of pythons during the nonfeeding period suggests that this opportunity cost is
considerable. In male pythons this cost reflects both
direct expenditure (due to increased mate-searching
movements) and underlying maintenance costs over the
same period (17% over 6 weeks). The preoviposition
mass loss of females (11% over 8 weeks) reflects movements over this period (to egg-laying sites), but is complicated by the change in water content of oviductal
eggs (Naulleau & Bonnet 1996). Nonetheless, our data
suggest that the maintenance requirements of pythons
over the non-feeding period constitute a significant
component of the overall energy-based costs of reproduction in both sexes.
Although the total energy costs of reproduction (i.e.
opportunity costs plus direct investment) are thus high
in both sexes, intriguingly they influence survival only
in females. Male pythons ceased feeding for six weeks,
and lost 17% of their body mass during this period,
but then rapidly regained their previous body condition (Fig. 3) and their survival was not affected. In contrast, the much longer fast of reproductive female
pythons, combined with the direct investment into the
clutch, resulted in an increased risk of mortality. The
most parsimonious interpretation is that pythons of
both sexes can tolerate a mass decrease of approximately 20% without incurring an increased mortality
6 74
T. MADSEN AND R. SHINE
risk, but cannot tolerate a 45% decrease in body mass
without survival consequences. In keeping with this
interpretation, females that expended more energy in
clutch production also suffered from increased mortality. Also, females that deserted their eggs soon after
laying (and thereby reduced the duration of their nonfeeding period) were more likely to survive than were
females that remained with the clutch throughout the
2 month incubation period (Madsen & Shine 1998c).
Energy-allocation measures offer operationally convenient indices of the total resources devoted to reproduction, but may bear little relationship to the actual
costs experienced by the reproducing organism. For
example, traditional measures of reproductive effort
(such as relative clutch mass or proportional energy
allocation to reproduction) in our water python population would be only weakly correlated with reproductive costs for at least three reasons.
1. Direct investment in the clutch is only one component of the energy costs of reproduction. The
prolonged period without feeding, together with
other costs associated with maternal attendance of
the clutch, constitute a substantial fraction of the
overall impact of reproduction on the energy budget of a female python. This ‘opportunity cost’ is
ignored in measures based upon the mass or
energy content of the clutch. Indeed, the magnitude of such ‘opportunity costs’ may sometimes
bear little relationship to the magnitude of the direct
energy expenditure of a female on reproduction
(Bull & Shine 1979).
2. Even if the opportunity cost is incorporated into
an overall energy-based measure of reproductive
effort, the resulting variable does not translate in
any straightforward way into a consequent survival
cost. As the sex difference in survival rates indicates,
survival may be impaired only when energy costs
exceed some threshold value.
3. Costs accruing from a given level of reproductive
allocation vary through time, depending upon
local prey availability. In years when prey is abundant, female pythons are more likely to reproduce,
are in better body condition after they have done
so, and thus are more likely to survive (Shine &
Madsen 1997; Madsen & Shine 1998c). However,
in years when prey are scarce, female pythons actually decrease the level of body reserves necessary to
initiate reproduction; thus, they are extremely
emaciated after oviposition (Madsen & Shine
1999b). Such emaciated females are more likely to
die, in water pythons as in other snake species (e.g.
Madsen & Shine 1993; Luiselli 1995; Luiselli et al.
1996).Given these complexities, the link between
energy costs and survival costs may be so weak that
one cannot be used to infer the other. Energy allocation measures are of great interest in their own
right, but we need to measure survival rates in order
to quantify costs of reproduction.
ACKNOWLEDGEMENTS
We thank G. Bedford, B. Cantle, E. Cox, P. Fisher,
P. Harlow, P. Osterkamp, J. Osterkamp and G. ‘King’
Brown for field assistance, and K. Levy for logistical
support. The study was funded by the Australian
Research Council.
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