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Why do female ball pythons (Python regius) coil so tightly around their eggs?

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Question: What benefits does brooding confer to offspring viability that outweigh its costs to the nest-attending female? Organisms: Thirty captive Python regius females and their clutches. Site: Vicinity of Lomé, Togo. Background: It has previously been shown that brooding enhances ball python hatching success by reducing desiccation of eggs. Methods: We captured wild, gravid females just before the time of egg-laying. Then we varied maternal attendance, allowing it to last 0, 15 or 60 days. Conclusions: Brooding weakly influenced incubation temperature but markedly decreased egg mass loss owing to water loss and associated yolk coagulation. Brooded eggs produced larger, more active, faster swimming and more rapidly developing neonates than did non-brooded eggs.
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Why do female ball pythons (Python regius)
coil so tightly around their eggs?
Fabien Aubret,1,3 Xavier Bonnet,1,2* Richard Shine2
and Stéphanie Maumelat1
1Centre d’Etudes Biologiques de Chizé – CNRS, 79360 Villiers en Bois, France,
2Biological Sciences, A08, University of Sydney, Sydney, NSW 2006, Australia and
3School of Animal Biology, M092, University of Western Australia, Crawley, WA 6009, Australia
Question: What benefits does brooding confer to offspring viability that outweigh its costs to
the nest-attending female?
Organisms: Thirty captive Python regius females and their clutches.
Site: Vicinity of Lomé, Togo.
Background: It has previously been shown that brooding enhances ball python hatching
success by reducing desiccation of eggs.
Methods: We captured wild, gravid females just before the time of egg-laying. Then we varied
maternal attendance, allowing it to last 0, 15 or 60 days.
Conclusions: Brooding weakly influenced incubation temperature but markedly decreased egg
mass loss owing to water loss and associated yolk coagulation. Brooded eggs produced larger,
more active, faster swimming and more rapidly developing neonates than did non-brooded
Keywords: brooding, incubation, parental care, phenotypic plasticity, Python regius.
Mathematical models suggest that whether or not a given life-history ‘tactic’ will evolve and
continue to be expressed is dependent on the relative magnitude of two opposing forces: the
costs and benefits that accrue from expression of that characteristic (e.g. Charnov and Krebs, 1974).
One example of a complex behavioural trait with high costs is parental care (Alckock, 1993;
Andersson, 1994). In many organisms, reproductive individuals experience substantial risks, and
spend considerable energy in the process of raising their offspring (Clutton-Brock, 1988, 1991).
Presumably, the compensating benefit in this case accrues to the offspring: higher parental
investment may increase the offspring’s probability of survival or its subsequent
reproductive success (Townsend, 1986; Clutton-Brock, 1988; Clutton-Brock and Godfray, 1991). In cases where
* Address all correspondence to Xavier Bonnet, Centre d’Etudes Biologiques de Chizé – CNRS, 79360 Villiers en
Bois, France. e-mail:
Consult the copyright statement on the inside front cover for non-commercial copying policies.
Evolutionary Ecology Research, 2005, 7: 743–758
© 2005 Xavier Bonnet
the parent provides direct protection against predators or nutritional input, the benefits to
offspring fitness are well known (Woodruff, 1977; Forester, 1979; Woodside et al., 1981; Gross and Sargent, 1985;
Wolf et al., 1988). However, the benefits of energetically expensive forms of parental care that do
not involve protection or nutrient transfer to the neonates are less obvious.
Although parental care of eggs is relatively rare among squamate reptiles, a distinctive
form of this behaviour appears to be ubiquitous in one lineage of snakes. Female pythons
remain tightly coiled around their eggs throughout incubation (Noble, 1935; Cogger and Holmes, 1960;
Hutchinson et al., 1966; Shine, 1985; Somma, 1990). In cool climates (where almost all studies have been
conducted), brooding females maintain high and constant temperatures within the clutch
by shivering thermogenesis (Vinegar et al., 1970), a behaviour that entails high energetic costs
(Vinegar et al., 1970; Harlow and Grigg, 1984; Slip and Shine, 1988). In addition, brooding females do not
feed during incubation (Ellis and Chappell, 1987). Given these high costs, what are the benefits?
The most likely benefits involve the effects of maternally controlled incubation regimes
on embryogenesis. Developmental trajectories in reptile embryos are highly sensitive to the
physical conditions encountered during incubation (Andrews, 2004; Deeming, 2004; Shine, 2004). Eggs
that experience conditions that are too dry or too wet, or too hot or too cold, either may die
before hatching or may hatch but produce inferior hatchlings with a lowered probability of
subsequent survival and growth (Fox, 1948; Taning, 1952; Licht and Moberly, 1965; Osgood, 1978; Muth, 1980;
Burger et al., 1987; Webb, 1987; Packard and Packard, 1988). This sensitivity has acted as a strong selective
force on maternal behaviour in reptiles from a diverse array of phylogenetic lineages, and
has favoured the evolution of careful nest-site selection in egg-laying species, and careful
thermoregulation by pregnant females of viviparous taxa (Beuchat, 1988; Shine, 2004). Plausibly,
the same kinds of selective forces have acted on maternal nest-attending behaviour (Shine et al.,
1997). That is, the benefit of maternal attendance might involve control over the physical
conditions experienced by incubating eggs, in ways that enhance egg survival and/or
hatchling phenotypes. The only obvious alternative hypothesis is that maternal attendance
functions to reduce predation on the eggs, but this could be achieved by the mother simply
remaining near the eggs rather than coiling around them and twitching. Indeed, this simpler
form of parental care is seen in many other squamate species (Shine, 1985; York and Burghardt, 1988;
Somma, 1990). Thus, attention focuses on two additional pathways by which maternal egg-
brooding might enhance offspring viability: through changes to the thermal and/or hydric
regimes experienced by the developing eggs.
The most detailed analysis of this question has come from research on water pythons
(Liasis fuscus) from tropical Australia (Shine et al., 1997; Madsen and Shine, 1999). Reproducing
females display facultative nest attendance, depending upon thermal regimes inside the
burrows where they lay their eggs (Madsen and Shine, 1999). Experimental incubation of eggs at a
variety of thermal regimes (but without maternal attendance) suggested that maternal
thermogenesis might substantially enhance offspring fitness, in some but not all natural nest
sites (Shine et al., 1997). This thermal effect was manifested both via increased hatching success
and via modifications to phenotypic traits of hatchlings (Shine et al., 1997). However, this study
was conducted on artificially incubated clutches only and was restricted to temperature
variations. Thus, Shine and colleagues (1997) study provided no information on the
determinants or consequences of hydric conditions during incubation, nor did it include
maternally brooded clutches.
We have addressed some of these missing elements with a study on ball pythons (Python
regius) at a field site in equatorial Africa (Aubret et al., 2003, 2005). This study is the third part
of an experiment that investigated: (a) the effects of brooding on the females energy
Aubret et al.744
expenditure (Aubret et al., 2005), (b) the influence of clutch size manipulation on hatching
success and hatchling traits (Aubret et al., 2003), and (c) the effects of brooding duration on
the phenotype of neonates (this study). The questions addressed in each of the three
constituents of the study diverge clearly: they focus respectively on the relationships
between parental care and costs of reproduction versus clutch size and reproductive
success versus brooding duration and offspring phenotype. Although complementary,
these issues were consequently considered separately. One part of the study showed that
brooding females spent very little energy over the 2 month incubation period, and that such
expenditure was independent of fecundity, challenging the notion that intensive parental
care necessarily entails major energy costs (Aubret et al., 2005). Experimental manipulation of
clutch size in fully attended clutches (i.e. ignoring brooding duration) strongly influenced
hatching success because females were unable to physically cover enlarged clutches, and
thus some eggs desiccated and died (Aubret et al., 2003). The current study focuses specifically
on the effects of the duration of maternal brooding on phenotypic traits of hatchling
snakes. Our current data thus bear directly on the effects of parental care duration on the
phenotypic traits of offspring.
Ball pythons (Python regius; Pythonidae) are small (up to 170 cm snoutvent length and
4 kg in weight) nocturnally active, non-venomous constricting snakes. The species extends
over a vast area of Africa in terms of longitude, latitude and habitat types (Luiselli and Angelici,
1998; Chippaux, 2001). High-density populations occur from South Ghana to South Benin,
especially in disturbed areas where rodents [the main prey of these snakes (Luiselli and Angelici,
1998)] are abundant. Our study was conducted in the extreme south of Togo (Lomé; 67N,
113E), an equatorial area characterized by high and relatively stable temperatures all year
round (from 25 to 35C).
In the study area, females lay 314 eggs in tortoise or rodent burrows or abandoned
termite mounds, usually in early February (Aubret et al., 2003). Females coil tightly around their
clutches and adopt a defensive posture when disturbed (Fig. 1). Based on observations by
professional snake hunters (and personal observations), almost all clutches are attended by
females. However, some clutches are found without a female in attendance, suggesting
that brooding may be interrupted (perhaps for short periods) or may be facultative in this
species as it is in the water python (Shine et al., 1997).
Experimental procedure
As this study is the last part of a larger experiment, material (e.g. animals) and methods
overlap partly. However, all the current statistics are original. There is also a weak overlap
between previous mean values [e.g. maternal and offspring characteristics (size and mass) of
the control group, initial clutch sizes and initial maternal characteristics of the manipulated
groups remain unchanged] and those presented here. Such overlap was inevitable,
and necessary to provide links between the three studies. However, the current study
focuses on offspring phenotype, behaviour and growth rate as a result of incubation
regime; maternal and initial clutch characteristics are only provided to illustrate the
homogeneity of the procedure during the allocation of the mothers in the three treatment
Benefits of brooding to offspring viability 745
Snake hunters employed by the registered farm TOGANIM (SARL) captured 30 gravid
female pythons from the wild in the vicinity (<50 km) of Lomé at the beginning of the
laying season in January 2000. Each female was initially measured for total length (±0.5 cm)
and snoutvent length (±0.5 cm) with a flexible ruler, and body mass with an electronic scale
(resolution 1 g, precision ±0.2%). The snakes were maintained in small wooden cages
(50 ×50 ×30 cm) in a quiet, dark room. Water and food (pre-killed mice) were provided to
the snakes once a week. Although the females drank regularly, they refused to eat [as in
reproductive females of many snake species (Lourdais et al., 2002a)]. The 30 females produced
their clutches 1545 days after capture. The clutch was weighed less than 6 h after
oviposition. Abnormal eggs (i.e. undersized or with incomplete shell) were discarded to
avoid possible mould contamination to the entire clutch. The mass, maximum length and
width of the eggs were recorded at the beginning of the experimental period, and then every
15 days until hatching. Because python eggs are strongly adherent, it was not always pos-
sible to separate them without damaging the shell. In such cases, the mass of each egg was
inferred from the mass of the clutch divided by egg number instead of weighing the eggs
individually. An estimate of the volume of the eggs was obtained using the equation to
calculate the volume of an ellipsoid: 4/3πab2, where a=1/2 the length of the egg and b=1/2
the width of the egg (Mayhew, 1963). As soon as the females began to lay their eggs, they were
randomly allocated to one of the three treatment groups:
Fig. 1. Female ball python coiled around her clutch. The defensive posture adopted by the female
allows observation of the eggs that are normally completely hidden.
Aubret et al.746
1. Ten maternally brooded clutches were left with their mothers until hatching (i.e. control
2. Ten partly brooded clutches were left with the mother for the first 15 days after laying;
then the female was removed and the eggs left without maternal attendance.
3. Ten artificially incubated clutches were separated from the mother immediately after
The clutches left without maternal attendance were placed in boxes (50 ×50 ×20 cm)
filled with wood shavings. The eggs were placed in the middle of each box, close to the
surface, and were covered by a thin layer of shavings. Similar artificial incubators are used at
TOGANIM. However, the room we used was large and well ventilated, while local farmers
incubate the eggs in small and closed rooms. Despite the fact that the boxes we used were
watered once a week to keep the uppermost shavings damp, the humidity (not measured)
may have fallen below 100% at times. The high ambient temperatures in Lomé were buffered
in the incubators in a similar way as occurs in natural nests inside the burrows of tortoises
(see below). The clutches were inspected several times a week and any eggs affected by
mould were removed. Eggs that died during development were dissected, and we recorded
the body mass and body length of the embryo and the residual egg mass.
At the end of the experiment, all the females were apparently healthy and in good body
condition (Aubret et al., 2005). The females were released along with 10% of the neonates,
under regulations set down by local wildlife authorities. The rest of the neonates were
legally exported to the USA, Japan or Europe. None of the animals involved in our study
were mistreated, sick or injured. Our study was carried out under the ongoing legal activity
of TOGANIM. The IUCN recently undertook a survey on ball python populations of
Togo suggesting that this species adapts well to this legal trade (further information
is provided at the following IUCN site:
Temperature records
Incubation temperatures were recorded using two data loggers per treatment (Tinytag Ultra
40 to 85C; 1929 data for each recorder; delay between each record of 16 min and 30 s). We
attached the loggers (n=6) to the clutch. We placed two other temperature recorders in
potential natural nest sites: one in a termite mound and the other in a tortoise burrow. This
allowed us to compare potential natural incubation temperatures without maternal attend-
ance to those we monitored in our experiment. We also recorded the ambient temperature
of the room that housed the three sets of clutches. For analysis, we focused on the first
2 weeks of incubation, because early development is the period of highest sensitivity of the
embryos in squamates as well as many other vertebrates (Gerhart and Kirschner, 1997; Shine, 1999; Shine
and Elphick, 2001; Andrews, 2004). All our clutch data loggers recorded temperatures within a
narrow range [extremes were recorded in the natural nest site (25.9C) and ambient room
temperature (33.0C)], and with similar means (28.830.5C). Because the conditions were
further buffered in the cages and boxes, all the embryos experienced similar temperatures;
there were subtle differences among treatment groups, however. On average, mean temper-
atures of the maternally brooded or partly brooded clutches were slightly higher (1C) than
those of the artificially incubated clutches (30.5C in maternally or partly brooded clutches
versus 29.5C in artificial incubators; the extremes ranged from 26.3 to 32.2C). As expected
Benefits of brooding to offspring viability 747
with such a narrow range of temperatures, the variances were low (all standard deviations
lower than 1.3).
Incubation and hatchling characteristics
As soon as the neonatal snakes began to slit their eggshells, the eggs were removed from
the females or from the incubator and placed in individual containers. The time elapsing
between oviposition and egg-slitting was recorded (incubation time). The delay between
the first shell-slitting and the full emergence of the hatchling was also recorded. Most
hatchlings required more than 24 h to fully emerge from the egg (see Results), perhaps
because the snakes slit the shell before absorbing their residual yolk completely. On a few
occasions with unusually dry eggshells, the young snakes were unable to slit an opening
large enough to escape from the egg. After 1 day of unsuccessful attempts, we opened a
window (1 cm incision) with a scalpel. This reduced the total time necessary for emergence,
but prevented unnecessary mortality. Data on delay of emergence for these animals were
not used in our analyses.
After full emergence, hatchlings were measured for body length, snoutvent length and
body mass (±0.1 g with an electronic scale). We counted the number of ventral scales,
recorded scale abnormalities, and determined sex by eversion of hemipenes. The size and
the shape of the head were measured with callipers as follows: (1) jaw length (from the tip of
the snout to the quadrato-articular projection); (2) skull length (from the tip of the snout to
the base of the skull); and (3) head width (maximal width above the eyes, from the external
margins of the supraoculars). The remaining egg mass was weighed [shell plus remaining
yolk (Deeming 1989)]. Water was provided to the neonates immediately after completion of the
first measurements.
Locomotor performance and behaviour of hatchlings
Locomotor performances of 1-week-old neonates were assessed by several tests, similar to
those previously used to quantify phenotypic quality in neonate reptiles (Van Damme et al., 1992;
Shine et al., 1997; Aubret et al., 2003). Swimming ability was recorded in a circular pool (1 m in
external diameter; 0.9 m in internal diameter; water temperature 28C). Dropped from 5 cm
above the water, the hatchlings usually started swimming after a few seconds. During a
3 min trial, we recorded the total number of laps swum and the total time spent swimming
(disregarding the time during which the hatchling was immobile, or was trying to escape).
Hatchling swimming speed (distance covered in centimetres per minute) and the percentage
of time spent swimming per trial were calculated.
The crawling aptitude of the hatchlings was assessed in an open area of sand, a common
natural substrate for ball pythons in South Togo. The experimenter sat 3 m from the snake
to minimize disturbance. Over 2 min, the distance travelled from the departure point to the
final position was recorded, as well as the total number of tongue flicks (using a manual
counter). Scores on this test may reflect a combination of variables such as the vigour with
which the animal attempted to sample cues (tongue licking) and to escape (crawling speed)
from a potentially dangerous open area.
The defensive behaviour of the hatchlings was also recorded. Their propensity to strike
defensively at a small object (a pen moved at 10 cm from the snout) was assessed. The first
strike started the test, and then we counted the total number of strikes during the next 30 s.
Aubret et al.748
If the snake refused to strike after 3 min of harassment, or had adopted a passive defensive
position such as curling itself into a compact ball by that time, we scored the trial as null.
We also measured growth rates of the hatchling snakes from birth to 10 days after
emergence. Water was available, but the snakes were not fed during that period, so
variations in body mass or body size must reflect utilization of energy stores originally
present in the egg, including yolk conversion into new tissues and the associated water
intake. Notably, residual yolk can provide enough materials to sustain growth in body size
(Congdon et al., 1982; Ji and Sun, 2000). Finally, we recorded the age when the snakes first shed their
Statistical analyses
It was not possible to allocate the eggs randomly among treatments because they were often
strongly adherent to each other. Consequently, to control for the variance due to a possible
maternal effect, we used mixed-model analyses of variance (or analyses of covariance) with
maternal identity as a random factor, experimental treatment as a fixed factor, and morpho-
logical traits of the eggs or of the hatchlings as the dependent variables. We also used
mixed-model analyses of variance to assess physiological performances post hatching.
Snake body condition (mass relative to length) was analysed using analyses of covariance
with body mass as the dependent variable and snoutvent length as the covariate
(Garcia-Berthou, 2001). Because the neonates used in the behavioural tests were chosen randomly
within different clutches and equally distributed among groups, it was not necessary to
control for maternal (i.e. clutch) identity. Indeed, the mean number of neonates per mother
included in the behavioural analyses was 1.14 (range 12), removing a potential maternal
(pseudo-replication) effect. Growth trajectories were analysed using multivariate analysis of
variance with repeated measures of snoutvent length and body mass over time; maternal
identity was included as a random factor [multivariate analysis of variance (OBrien and Kaiser,
1985)]. For all behavioural tests, several variances were not homogeneous (even after log
transformation), so we used non-parametric Kruskal-Wallis analyses of variance for these
tests. Null scores (i.e. no strike during the defensive behaviour test) were taken into account
in the analysis to avoid comparing behavioural measurements that may emerge from
different decisions taken by the snakes (facing versus escaping the danger). All statistical
tests were performed with Statistica 6.1.
Maternal and clutch characteristics
The mean characteristics of the females and of their clutches allocated to the three
treatment groups are given in Table 1. We did not find any significant differences among
the three batches in the mean body lengths of the mothers (ANOVA with treatment as the
factor: F2,27 =0.47, P=0.63), their body masses (F2,27 =0.71, P=0.50), their body condition
(same design ANCOVA with maternal size as a covariate: F2,26 =0.31, P=0.74), their clutch
sizes (same design ANOVA: F2,27 =0.68, P=0.51), clutch masses (same design ANOVA:
F2,28 =0.19, P=0.82), or laying dates (same design ANOVA: F2,27 =0.59, P=0.56; P>0.50
in all post-hoc tests for these five analyses of variance). Similarly, egg mass at oviposition
(mixed-model ANOVA with maternal identity as a random factor and treatment as the
Benefits of brooding to offspring viability 749
main factor: F2,9 =0.02, P=0.98) and egg volume at laying (same design mixed-model
ANOVA: F2,26 =1.36, P=0.28) did not differ among the three groups. Therefore, any
difference in relevant traits among our treatment groups should reflect the influence of
incubation regimes on incubation periods and on the phenotypes of hatchlings.
Incubation regime, incubation period and morphology of the hatchlings
Incubation periods averaged 2 months and did not differ significantly among the three
treatment groups (Table 2). However, many traits we measured were affected by the
incubation regime (Table 2). Maternally incubated neonates were larger, heavier and had
longer jaws than neonates in the other two groups (all P<0.001). The artificially incubated
hatchlings were small and in poor body condition. However, our experimental treatments
did not induce any significant difference in many other traits, such as length or width of the
heads, or scale counts (total number of ventral scales, number of abnormal scales). Import-
antly, the mass of the material remaining after hatching (yolk +shell) was significantly
lower in the maternally brooded group, intermediate in the partly brooded group and higher
in the artificially incubated group. This pattern suggests that maternal brooding allowed
hatchlings to incorporate their available yolk material into the body cavity before leaving
the egg. As expected, the mass of the remaining material was negatively correlated with the
body mass of the hatchlings (n=79, r=−0.40, P=0.0002).
Due to a net loss of water (Wangensteen et al., 1970; Rahn and Ar, 1974; Packard, 1991), the eggs lost mass
from laying to hatching in all three groups. However, the amount of water lost differed
significantly among the treatments (repeated measures of mass over time: Wilks λ=0.53,
F2,19 =6.34, P<0.008). Maternally brooded eggs lost, on average, 16% of their initial mass,
partly brooded eggs lost 37% of their initial mass, while the artificially incubated eggs lost
51% of their initial mass. This result clearly suggests that the presence of the mother limited
desiccation of the eggs.
Considering only maternally brooded hatchlings, greater hatchling mass was associated
with longer incubation (n=21, r=0.54, P<0.01) [Fig. 2; mean values per clutch plotted
in these analyses we also used supplementary data from a parallel experiment in which
females were allowed to completely brood their clutches (Aubret et al., 2003)]. Also, larger eggs
gave rise to larger hatchlings (n=18, r=0.47, P<0.04).
Table 1. Maternal and clutch characteristics of the three brooding treatment groups of ball pythons
(n=10 females in each group)
Variable Maternally brooded Partially brooded Not brooded
Snoutvent length (cm) 112.5 ±2.2 114.5 ±1.6 115.3 ±2.6
Body mass (g) 1844.2 ±98.5 1933.3 ±91.2 2032.3 ±139.2
Pre-laying body condition (g) 1910.2 ±71.3 1917.7 ±70.6 1981.9 ±71.0
Clutch size 7.3 ±1.2 7.4 ±1.1 8.0 ±1.9
Egg masses at laying (g) 86.9 ±1.9 88.7 ±1.1 87.9 ±2.8
Egg volume at laying (cm3) 80.0 ±1.0 86.0 ±1.2 84.8 ±1.7
Note: Pre-laying maternal body condition represents maternal body mass adjusted by size. Sample sizes for egg
mass (n=12, 4, 12) and individual egg size at laying (n=62, 64, 65) for the maternally brooded, partially
brooded and the artificially incubated group, respectively. Egg volume =volume of an ellipsoid (4/3πab2, where
a=1/2 the length of the egg and b=1/2 the width of the egg). Mean values are given with standard errors.
Aubret et al.750
Locomotor performance and behaviour of hatchlings
Incubation regimes affected several aspects of hatchling performance. First, maternally
brooded hatchlings emerged more rapidly from their eggs than did the partly brooded
snakes, which in turn emerged more rapidly than did the artificially incubated hatchlings
(Table 2). Larger neonates emerged from the egg more rapidly than smaller snakes, as
indicated by a negative correlation between body size and the duration to escape from
the egg (snoutvent length: n=66, r=−0.39, P<0.001; body mass: n=66, r=−0.47,
P<0.001). Thus, maternally brooded snakes were not only larger, but they also emerged
Table 2. Effects of incubation regime on incubation period, remaining egg mass and hatchling traits
(mean ±standard error) in the ball python, Python regius
brooded Not brooded d.f. F/H P
Incubation period (days) * 60.73 ±0.15 60.55 ±0.35 61.83 ±0.83 2,19 0.74 0.49
Emergence duration (days) 1.51 ±0.08 2.07 ±0.15 2.60 ±0.60 2,16 5.43 <0.01
Remaining egg mass (g) 5.50 ±0.43 13.14 ±2.00 17.18 ±3.58 2,19 11.31 <0.001
Morphology at hatching
Body mass (g) 55.05 ±0.91 44.31 ±3.23 38.35 ±2.96 2,19 9.00 0.001
Snoutvent length (cm) 39.26 ±0.28 35.01 ±0.81 35.83 ±0.95 2,19 15.66 <0.001
Body condition index 48.38 ±1.22 47.65 ±1.54 40.68 ±2.80 2,19 1.51 0.24
Jaw length (mm) ** 26.95 ±0.14 25.25 ±0.19 25.67 ±0.37 2,19 21.09 <0.001
Skull length (mm) *** 9.65 ±0.07 9.51 ±0.09 9.45 ±1.16 2,19 0.75 0.48
Head width (mm) ** 4.76 ±0.04 4.61 ±0.06 4.80 ±0.11 2,19 2.23 0.13
Number of ventral scales 207.04 ±0.48 205.82 ±0.65 205.33 ±1.09 2,19 0.82 0.45
Abnormal ventral scales (n) 2.37 ±0.26 3.55 ±1.10 3.00 ±0.68 2,19 1.32 0.28
Behavioural traits
Distance swum (m) 6.62 ±0.56 3.52 ±0.74 3.31 ±0.14 2,63 11.04 <0.005
Swimming speed (m ·min1) 3.07 ±0.27 2.45 ±0.34 1.49 ±0.64 2,63 8.17 <0.02
Percentage of activity 67.95 ±4.34 47.62 ±5.69 56.18 ±10.64 2,63 7.86 <0.02
Distance covered on ground (m) 1.12 ±0.14 0.70 ±0.18 0.62 ±0.34 2,63 3.32 0.19
Number of strikes elicited 5.57 ±0.98 6.08 ±1.18 9.00 ±1.91 2,37 0.99 0.61
Number of strikes elicited 2.94 ±0.73 3.76 ±0.96 7.50 ±1.79 2,63 3.18 <0.02
Number of tongue flicks 112.11 ±7.67 95.05 ±10.03 103.83 ±18.76 2,63 2.73 0.26
Physiological performance
Delay to first slough (days) 10.47 ±0.16 12.25 ±0.62 12.50 ±0.96 2,10 9.21 <0.01
BM (g) (10 days old) 58.18 ±1.13 52.31 ±2.64 40.50 ±3.28 2,12 8.12 <0.01
SVL (g) (10 days old) 44.31 ±0.30 42.44 ±0.73 40.10 ±1.05 2,12 5.43 <0.02
Increase in BM (g) **** 1.90 ±0.72 3.62 ±0.78 0.59 ±1.51 2,12 0.96 0.41
Increase in SVL (cm) *** 5.83 ±0.29 6.22 ±0.34 4.08 ±0.62 2,12 2.05 0.17
Note: All comparisons among the three treatments were performed using mixed-model analyses of variance with
maternal identity as a random factor, except for behavioural traits where Kruskal-Wallis analyses of variance were
used (see text for details). BM =body mass; SVL =snoutvent length.
Maternally brooded =clutch left with their mother until hatching (n=51 neonates); partially brooded =clutch
left with their mother during the first 2 weeks, then placed into an artificial incubator (n=22 hatchlings); artificially
incubated =clutch placed into an artificial incubator throughout incubation (n=6 hatchlings); * mean value per
clutch; ** relative to skull length; *** relative to initial snoutvent length; **** relative to initial body mass;
number of strikes including null scores.
Benefits of brooding to offspring viability 751
from the egg more quickly. However, this latter effect may have been a consequence of the
former: when the effect of neonate size was taken into account, statistical significance was
lost using an analysis of covariance with clutch identity nested within incubation treatment
as factors, hatchling mass as covariate and escape time as the dependent variable
(F2,47 =2.96, P<0.061), but not with snoutvent length as covariate (F2,47 =4.95, P<0.011).
Maternally brooded hatchlings swam faster and over a longer distance than did young
snakes from the other treatments. We found a positive influence of snoutvent length on
locomotor ability. However, when significant, this relationship was always very weak
(n=63; 0.02 <r2<0.08, 0.25 <P<0.03 in all correlations between locomotor perform-
ances and snoutvent length), and including snoutvent length as a covariate in the analyses
did not affect the results. Consequently, the better swimming performance of maternally
incubated hatchlings was mostly attributable to the effect of maternal attendance per se
rather than a by-product of size. The maternally incubated hatchlings were also more active
(see Table 2). Our results suggest that on average maternally brooded hatchlings tended to
travel greater distances over the ground and explored their environment more intensively by
tongue flicking. However, the results for tongue-flicking rates and distance travelled over the
ground did not reach statistical significance, perhaps due to high variability for these traits.
The maternally incubated hatchlings did not display more intense defensive behaviour when
harassed during experimentation. In fact, the reverse trend was observed, and this effect was
significant when null scores were included. The proportion of snakes that struck the pen or
adopted a defensive passive posture differed, although not significantly so (due to the small
sample size of several cells in the contingency table), between treatments: 53% of the mater-
nally brooded snakes decided to strike, versus 62% for the partially brooded and 83% for the
non-brooded neonates (χ2=2.11, d.f. =2, P=0.34).
Post-hatching growth rates
Despite the absence of food, all young pythons increased their snoutvent length and body
mass from hatching to the age of 10 days (Table 2). Importantly, water was available ad
libitum over this period. This early growth undoubtedly was sustained by abdominal yolk or
other body reserves (Ji et al., 1997; Ji and Sun, 2000). Hatchlings from all groups showed similar
increases in size and mass (Table 2), but maternally brooded snakes maintained a significant
Fig. 2. Relationship between the duration of incubation and the body mass of hatchlings in the ball
python. These two parameters are plotted as means per clutch.
Aubret et al.752
advantage in terms of body size and body mass after 10 days (Table 2). Partially brooded
snakes were also larger and heavier than the artificially brooded offspring. Snakes with the
highest body condition index at the time of hatching, and hence with greater body reserves,
exhibited a higher post-natal growth rate (growth rate after hatching was positively
correlated with initial body condition: n=54, r=0.64, P<0.0001) (Fig. 3).
Maternally brooded hatchlings also sloughed their skins earlier than did other hatchlings.
The delay from birth to the first slough was significantly correlated with the initial body
mass of hatchlings (n=46, r=0.52, P<0.0002). When this effect of body size was controlled
through an analysis of covariance (with body mass as the covariate), the influence of
treatment on sloughing delay was not statistically significant (F2,34 =1.25, P=0.30). Thus,
incubation treatment influenced sloughing mainly via its effect on the size of neonates;
small neonates tended to delay their first slough until they had attained a larger size.
Overall, our data suggest that maternally brooded hatchlings were in better condition
(larger, faster, more active, faster-developing) than those that were partly brooded. The
hatchlings that were artificially incubated were in the poorest condition.
Our data show that for ball pythons, parental care over a prolonged period strongly affected
not only hatching success of the eggs (Aubret et al., 2005), but also the phenotypic traits
of hatchlings that emerged from the viable eggs (this study). The variety of traits that
we measured support the inference that maternally incubated eggs gave rise to better
hatchlings. That is, not only was hatching success much higher from maternally incubated
clutches, but the hatchlings that emerged were larger, more active, swam faster and
for longer, and developed more rapidly post hatching than did offspring from artificially
incubated clutches.
Why did maternal brooding enhance hatching success and generate superior hatchling
phenotypes in our experiment? Previous discussions of the benefits of maternal brooding
for offspring fitness have generally focused on thermal regimes (Vinegar et al., 1970; Vinegar, 1973;
Harlow and Grigg, 1984; Shine et al., 1997). Notably, in pythons, enhanced embryonic survival and
development has been attributed to the maintenance of high stable temperatures via
shivering thermogenesis. More generally, many studies on squamate reptiles have concluded
Fig. 3. Relationship between body condition index at hatching and growth in snoutvent length until
the age of 10 days in neonate ball pythons.
Benefits of brooding to offspring viability 753
that hatchling phenotype temperatures are more sensitive to thermal than to hydric con-
ditions during incubation (Van Damme et al., 1992; Shine et al., 1997; Flatt et al., 2001; Shine and Elphick, 2001).
However, several studies have reported strong hydric effects (e.g. Warner and Andrews, 2002; Brown
and Shine, 2004). Our results support this latter conclusion. Although we acknowledge that our
experimental design did not separate out thermal and hydric effects, the consequences of
maternal brooding for hatching success and offspring phenotypes are more likely to reflect
hydric than thermal factors. We base this conclusion on four observations:
1. Maternally brooded eggs lost less water than eggs in the other treatments, and the partly
brooded clutches lost less water than the non-attended ones [see also Aubret et al. (2003,
2005) for the difficulties faced by the mother in covering an artificially enlarged clutch
during incubation].
2. The low hatching success of artificially incubated eggs was due to yolk desiccation:
many of these hatchlings left substantial solidified yolk behind in the egg, rather than
incorporating it into their bodies before hatching (note the negative correlation between
hatchling mass and residual egg mass; and the heavier residual mass of non-brooded
eggs). Yolk in artificially incubated eggs began to solidify, especially on the desiccation-
prone upper surface. The solid mass of yolk may have directly impaired the hatching
3. Mean hatching dates did not differ among treatments. In reptiles, incubation period and
gestation length are strongly influenced by mean temperatures during development
(Blanchard and Blanchard, 1941; Naulleau, 1986; Lourdais et al., 2002b), so the similarity in incubation
periods infers a similarity in mean temperature.
4. We did not find any difference in the number of ventral scales or in the occurrence of
scale anomalies among the three groups. These traits are also sensitive to incubation
temperatures (Fox, 1948; Osgood, 1978; Lourdais et al., 2004). Overall, the differences in temperature
experienced by the embryos generated by our experiment were probably too small
( 1C) to induce any major effects.
How can the mothers presence modify the hydric balance of her clutch? Female ball
pythons coil so tightly around the clutch that the eggs are completely hidden (Fig. 1;
personal observation). This bell surrounding the clutch could create a saturated micro-
climate around the eggs, substantially reducing evaporation (O. Lourdais and D. DeNardo,
personal communication). Thus, our results differ from those of most previous research by
advocating an important hydric rather than thermal benefit for parental care in pythons. If
optimal incubation conditions generate optimal hatchling phenotypes, there will be strong
selection for maternal behaviours that expose embryos to such conditions [for example,
temperature-dependent sex determination processes (Shine, 1999); nest-site selection, shivering
thermogenesis (Shine et al., 1997)]. In such cases, natural selection can act at two levels: on genes
that code for maternal influence on the clutch (e.g. thermal criteria for nest-site selection or
the intensity of shivering thermogenesis), and on genes involved in norms of reaction
during embryogenesis.
The mechanism that generated phenotypic variation among our hatchling pythons is one
that has not attracted previous interest yolk coagulation due to egg desiccation that
reduces the amount of resources available to the embryos (Sinervo, 1990). We note that the
relative importance of hydric control on fitness versus that of thermic control remains an
open question in wild-brooding pythons. However, the eggs of many species that are not
Aubret et al.754
maternally incubated (reptiles, insects) often suffer from desiccation; hydric control may
allow pythons to incubate their eggs in areas where the clutch would potentially desiccate if
left alone (Snell and Tracy, 1986; Tracy and Snell, 1986).
A plausible scenario for the evolution of parental care in pythons involves an initial step
whereby the females presence benefited offspring survival by discouraging egg predators
(Shine, 1985). The subsequent change to the females posture (coiling tightly around her eggs)
may have been favoured because of the resultant substantial reduction in water loss from
the clutch at a very low additional cost (Aubret et al., 2005). Lastly, advantages associated
with high and more stable incubation temperatures may have resulted in the evolution of
shivering thermogenesis. Our results suggest that even a brief initial period (2 weeks) of
maternal brooding enhances hatching success and improves phenotypes compared with
artificially incubated eggs. If offspring fitness is enhanced even by brief parental attendance,
it is easy to imagine the evolution of obligate brooding through a series of intermediate
stages that involved a gradual increase in the duration of this behaviour (Mell, 1929; Shine, 1985;
Farmer, 2000, 2003). Any such adaptationist scenario is speculative, and relies upon data from
present-day taxa to extrapolate back to the ancestral condition. We may be misled by
adaptive changes that have occurred subsequent to the evolution of brooding. For example,
if maternal brooding maintains high constant humidity around the clutch, eggs may evolve
a lowered resistance to desiccation (because they are never exposed to this problem):
the sensitivity to desiccation might be secondary, notably to allow embryonic respiration
(Wangensteen et al., 1970). In keeping with this possibility, the eggs of ball pythons are more
vulnerable to desiccation than are the eggs of most other squamate reptiles (Alberts et al.,
1997). Comparative data on desiccation rates of eggs from brooding species and their
non-brooding relatives could clarify the validity of this hypothesis.
We thank TOGANIM SARL, and the snake hunters who helped us in Togo: Kodjo, Edmond,
Bélémé, Tamer, Enchorte and Apouale. Rex Cambag built the boxes and analysed the temperature
data. Radikale Menvotre helped with the English. Manuscript preparation was supported by
the Australian Research Council and the Conseil Général des Deux-Sèvres, Niort 79, France. All
experiments complied with the current laws in Togo.
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Aubret et al.758
... For example, mass loss during the egg-caring period is observable for post-ovipositional female Eutropis (formerly Mabuya) longicaudata, but it can be balanced after a subsequent foraging period (Huang 2007). The energy cost caused by egg-caring could be trivial even during the actual egg-caring period in some snake species, such as Python regius (less than 6% mass loss in egg-caring females, Aubret et al. 2005b). Certainly, other aspects of maternal costs (e.g., increased parasite load, and reduced future survival and reproductive output) may be entailed by egg-caring behavior (Huang 2007;Stahlschmidt et al. 2012). ...
... However, only a very limited number of studies focused on reptilian species show some inconsistencies. For example, eggs cared for by post-ovipositional females produce larger and betterperforming (faster swimming and developing) hatchlings in the ball python, Py. regius (Aubret et al. 2005b), but produce smaller and poorer-performing hatchlings in the children's python, A. childreni (Stahlschmidt & DeNardo 2009b). Smaller and poor performing hatchlings were produced because coiling tightly around the eggs by females created a hypoxic incubation environment for developing embryos (Stahlschmidt & DeNardo 2008, 2009a. ...
Maternal egg-caring behavior can often be observed in oviparous scincid lizards. The expression of such behavior is predictably affected by the trade-off between its resultant costs and benefits for mothers and/or offspring, which has been investigated in only a few scincid species. Here, post-ovipositional Plestiodon chinensis females were treated to care for their egg clutches without interference, under simulated predation pressure, or to be care-deprived. Potential maternal costs and offspring benefits associated with egg-caring behavior were then evaluated by measuring changes in maternal body condition, egg mortality, and hatchling performance. Egg-caring behavior caused post-ovipositional females to participate less in outside-nest activity, eat less food, and show relatively poorer body conditions at egg hatching. By contrast, compared with care-deprived females, egg-caring females gained mass slightly faster, and achieved a similar body condition within a few months of hatching. Eggs that were cared for by their mothers were more likely to hatch and produced larger, faster-running and better-growing hatchlings with higher survival than uncared-for eggs. Simulated exposure to a potential predator had no distinct impact on maternal egg-caring behavior expression and offspring performance. These results indicated that marked benefits of offspring viability but minor maternal energy costs might play a decisive role in the occurrence of maternal egg-caring behavior in P. chinensis. This article is protected by copyright. All rights reserved
... Guided by environmental and social clues (e.g. empty shells of previous hatchlings, Brown & Shine, 2005a;Meek, 2017) and using their spatial memory, gravid females search underground tunnels or cavities for localities with stable ambient temperatures of around 30 -35 °C and high moisture levels, which produce optimal conditions for embryo development (Shine et al., 1997;Aubret et al., 2005;Brown & Shine, 2005b;Löwenborg et al., 2010Löwenborg et al., , 2011Ramesh & Bhupathy, 2010;Stahlschmidt et al., 2011;Meek, 2017). Such conditions can be represented by large partly rotting logs, hollow trees, thick leaf litters, underground insect nests or the burrows of various animals (Carman- Blazquez & Villafuerte, 1990;Madsen & Shine, 1999;Pearson et al., 2003;Velásquez-Múnera et al., 2008;Ramesh & Bhupathy, 2010;Nagy et al., 2017;Meek, 2017;Alexander, 2018). ...
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Published by the British Herpetological Society. Oviparous snakes deposit their egg clutches in sites sheltered from predation and from strong thermal and hydric fluctuations. Appropriate laying sites with optimum thermal and hydric conditions are generally scarce and are not necessarily localised in the home range. Thus, many gravid females undertake extensive trips for oviposition, and many may converge at the best egg laying sites. Dispersal mortality of neonates post-hatchling is also a critical factor. Assessing the parameters involved in this intergenerational trade-off is difficult however, and no study has succeeded in embracing all of them. Here we report data indicating that gravid females of the highly mobile European whip snake, Hierophis viridiflavus exhibit nest site fidelity whereby they repeatedly deposit their eggs in cavities under sealed roads over many decades. These anthropogenic structures provide benefits of relative safety and suitable incubation conditions (due to the protective asphalted layer?), but they expose both females and neonates to high risk of road mortality. Artificial laying sites constructed at appropriate distances from busy roads, along with artificial continuous well protected pathways (e.g. dense hedges) that connect risky laying sites to safer areas, should be constructed.
... For example, it has been demonstrated that crocodilian embryos produce vocalisations and also respond to those of their nest-mates (Vergne & Mathevon, 2008 predation risk, such as demonstrated in yellow-legged gull Larus michahellis embryos (Noguera & Velando, 2019), or optimal hatching conditions, as is the case in pig-nosed turtles Carettochelys insculpta (Doody et al., 2012). In taxa where parents brood or incubate the eggs [chiefly birds, but also pythons (Aubret et al., 2005), monotreme mammals (Beard & Grigg, 2000), and several amphibian species (Stebbins & Cohen, 1995)], embryos may also gain considerable information from parental behaviours. For example, parental vocalisations produced while on the nest have been suggested to influence nestling phenotype in zebra finches Taeniopygia guttata (Mariette & Buchanan, 2016), although whether or not such vocalisations are indeed adaptive is still debated (McDiarmid, Naguib & Griffith, 2018Mariette & Buchanan, 2019). ...
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Maternal effects, or the influence of maternal environment and phenotype on offspring phenotype, may allow mothers to fine‐tune their offspring's developmental trajectory and resulting phenotype sometimes long after the offspring has reached independence. However, maternal effects on offspring phenotype do not evolve in isolation, but rather within the context of a family unit, where the separate and often conflicting evolutionary interests of mothers, fathers and offspring are all at play. While intrafamilial conflicts are routinely invoked to explain other components of reproductive strategy, remarkably little is known about how intrafamilial conflicts influence maternal effects. We argue that much of the considerable variation in the relationship between maternally derived hormones, nutrients and other compounds and the resulting offspring phenotype might be explained by the presence of conflicting selection pressures on different family members. In this review, we examine the existing literature on maternal hormone allocation as a case study for maternal effects more broadly, and explore new hypotheses that arise when we consider current findings within a framework that explicitly incorporates the different evolutionary interests of the mother, her offspring and other family members. Specifically, we hypothesise that the relationship between maternal hormone allocation and offspring phenotype depends on a mother's ability to manipulate the signals she sends to offspring, the ability of family members to be plastic in their response to those signals and the capacity for the phenotypes and strategies of various family members to interact and influence one another on both behavioural and evolutionary timescales. We also provide suggestions for experimental, comparative and theoretical work that may be instrumental in testing these hypotheses. In particular, we highlight that manipulating the level of information available to different family members may reveal important insights into when and to what extent maternal hormones influence offspring development. We conclude that the evolution of maternal hormone allocation is likely to be shaped by the conflicting fitness optima of mothers, fathers and offspring, and that the outcome of this conflict depends on the relative balance of power between family members. Extending our hypotheses to incorporate interactions between family members, as well as more complex social groups and a wider range of taxa, may provide exciting new developments in the fields of endocrinology and maternal effects.
... Parental and maternal care of eggs is observed in a wide range of taxa (Royle et al., 2012) and improves the survival of offspring by protection against predators (Evans, 1998;Croshaw & Scott, 2005;Requena et al., 2009), by grooming and incubation (Aubret et al., 2005;Mungu ıa-Steyer et al., 2008;Boos et al., 2014). However, prey individuals that take care of their eggs may themselves be more susceptible to attack by predators than those that do not exhibit such behavior (Reguera & Gomendio, 1999;Li & Jackson, 2003;Suzuki & Futami, 2018). ...
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Predators frequently compete with other species for prey but can also interact by preying on each other’s vulnerable stages. Because eggs and juveniles are more vulnerable to this intraguild predation than adults, their survival will depend on maternal strategies to reduce predation risk. Recently, we reported that adult female predatory mites Gynaeseius liturivorus Ehara (Acari: Phytoseiidae) reduce intraguild predation on their eggs by remaining at oviposition sites, thus deterring the egg predators. In addition, they avoid oviposition close to eggs laid by conspecific females. We therefore expected that adult female G. liturivorus protect their own eggs better against these egg predators than eggs of other females. This was tested using juveniles of the predatory mite Neoseiulus californicus McGregor (Acari: Phytoseiidae) as egg predators and the western flower thrips, Frankliniella occidentalis Pergande (Thysanoptera: Thripidae), as the shared prey. When G. liturivorus eggs were kept with their mothers, the presence of juvenile egg predators did not affect the survival of eggs. However, when G. liturivorus eggs were kept with females that were not their mothers, the mortality of eggs in the presence of juvenile egg predators increased. When adult female G. liturivorus were guarding their eggs, they killed a similar number of juvenile egg predators as females that were not kept with their eggs. Hence, adult female G. liturivorus protect their eggs by remaining close to their eggs. Predators frequently compete with other species for prey but can also interact by preying on each other’s vulnerable stages. Previously, we showed that adult female predatory mites remain at oviposition sites, thus deterring juveniles of another predatory mite species, resulting in reduced intraguild predation on their eggs. We now show that this guarding behavior is more effective when adult females guard their own eggs than when guarding eggs of other females.
... Further, while eggs incubated at LE tended to gain mass during incubation, eggs incubated at EHE maintained their mass over the same period (Fig. 2a), suggesting a low efficiency of water or carbon dioxide diffusion (Cunningham & Hurwitz 1936). Excessive water loss in snake eggs may gradually increase yolk viscosity and impede absorption by the developing embryo (Cunningham & Hurwitz 1936;Aubret et al. 2005b). Eggs exposed to EHE, by losing excessive water, may have exposed the embryo to a similar constraint, leading to lesser yolk intake (and higher amounts of residual yolk post-hatching) and consequently smaller body size at hatching (Table 2). ...
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Climate change is generating range shifts in many organisms, notably along the elevational gradient in mountainous environments. However, moving up in elevation exposes organisms to lower oxygen availability, which may reduce the successful reproduction and development of oviparous organisms. To test this possibility in an upward‐colonizing species, we artificially incubated developing embryos of the viperine snake (Natrix maura , Linnaeus 1758), using a split‐clutch design, in conditions of extreme high elevation (hypoxia at 2877 m above sea level; 72% sea‐level equivalent O2 availability) or low elevation (control group; i.e. normoxia at 436 m above sea level). Hatching success did not differ between the two treatments. Embryos developing at extreme high elevation had higher heart rates and hatched earlier, resulting in hatchlings that were smaller in body size and slower swimmers compared to their siblings incubated at lower elevation. Furthermore, post‐hatching reciprocal transplant of juveniles showed that snakes which developed at extreme high elevation, when transferred back to low elevation, did not recover full performance compared to their siblings from the low elevation incubation treatment. These results suggest that incubation at extreme high elevation, including the effects of hypoxia, will not prevent oviparous ectotherms from producing viable young, but may pose significant physiological challenges on developing offspring in ovo . These early‐life performance limitations imposed by extreme high elevation could have negative consequences on adult phenotypes, including on fitness‐related traits. This article is protected by copyright. All rights reserved
... 70%) captured a maximum of five ball pythons per trip (n = 40), and fewer than six or seven eggs per trip (n = 35 and 40, respectively) (most likely a single clutch of eggs). Most ball python clutches comprise five to eight eggs (Aubret et al. 2003), and the eggs are strongly adherent so it is not possible to separate them without damaging the shell (Aubret et al. 2005). ...
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The ball python ( Python regius ) is the single most exported live CITES-listed species from Africa, with a large proportion of snakes being sourced from Togo, West Africa, officially via a system reported nationally as “ranching”. This study represents the first in-depth review of ball python hunting being carried out by rural communities in Togo for nearly 15 years. Our approach, focused at the bottom of the trade chain, permitted extensive detailed data to be collected from hunters, and provides a unique insight into the practices, drivers and impacts associated with this type of large-scale commercial wildlife trade activity. We show that ball python hunting remains an economically valuable endeavour for these rural hunters. However, it also highlights a number of potential legal, conservation and animal welfare issues associated with the current hunting practices being carried out in Togo (and neighbouring range States) to supply the snake farms and ultimately the international exotic pet trade. Our findings suggest that the methods applied on the ground do not accurately reflect those being reported to national authorities and international regulatory mechanisms such as CITES. This irregular, if not illegal, trade may also be unsustainable, as suggested by hunters reporting that there are fewer ball pythons in the wild than there were five years previously. We recommend that additional scientific investigation (focusing on the size and status of the wild population), better management, and enforcement of regulations, are required to ensure that ball python populations are managed in a sustainable, legal and traceable way.
... Independent of the absence of kin bias, our results confirm that maternal presence is crucial to maximize hatching success in earwigs (Boos et al. 2014). Across species and taxa, the presence of mothers with eggs often mitigates the costs of external stressors acting during egg development, such as predation (Swennen et al. 1993;Machado and Oliveira 2002;Requena et al. 2009;Miller et al. 2011), pathogen infection (Grindstaff et al. 2003;Herzner and Strohm 2007;Kudo et al. 2011;Trumbo 2012;Boos et al. 2014), desiccation (Aubret et al. 2005;Poo and Bickford 2013), and other environmental changes (Green and McCormick 2004;Smiseth et al. 2012). Given the standard laboratory conditions used in the present study, our findings suggest that maternal presence buffers the otherwise lethal effects of small variation in the nesting environment, for example, humidity and/or the development of nonpathogenic microbes such as mold (see also Boos et al. 2014). ...
The rejection of foreign individuals is considered a central parameter in the evolution of social life. Within family units, parents are typically thought to reject foreign offspring to ensure that their investment into care is directed towards their own descendants. Whereas selection for such kin bias is expected to be high when parental care is extended and involves numerous and energetically costly behaviors, it can be reduced when the acceptance of foreigners provide subsequent benefits to offspring and when alternative parental strategies limit the risk of clutch parasitism. In this study, we investigated the outcome of these conflicting selection pressures in the European earwig. Our results overall demonstrate that mothers do not eliminate foreign eggs, provide the same level of care to both foreign and own eggs (egg grooming, egg defense, and maternal return) and pay the same costs of care in terms of weight loss and immunity when tending each type of eggs. We also show that foreign and own eggs exhibit similar development time, hatching success and lead to comparable juvenile quality. Interestingly, our results reveal that tending eggs (of any origin) reduces mothers' weight loss during this long period, possibly due to egg cannibalism. Hence, these findings emphasize the difficulty to predict the occurrence of kin bias, and stress the need to broaden our knowledge on the net benefits of egg rejection for parents to better understand the general importance of kin bias in the evolution of pre-hatching parental care.
... Producing clusters of eggs is an effective way of facilitating the care of offspring 1 3 (Kudô et al. 1989;Buzatto et al. 2007;Poo and Bickford 2013;Giffney and Kemp 2016). Specific behaviors to take care of eggs, such as grooming, was not observed in G. liturivorus although it has been reported for other animals (Aubret et al. 2005;Munguía-Steyer et al. 2008;Boos et al. 2014). Thus, the aim of producing clusters of eggs by G. liturivorus mothers would not be for taking care of own eggs. ...
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Animals often select oviposition sites to minimize the predation risk for eggs and juveniles, which are more vulnerable to predation than adults. When females produce eggs in clusters, the eggs and juveniles are likely to suffer from cannibalism. Although cannibalism among siblings is known to be lower than among non-siblings, there have been few investigations into the possibility that females select oviposition sites that reduce the risk of cannibalism for the offspring. To test this possibility, we examined oviposition preference by adult females of the predatory mite Gynaeseius liturivorus in response to the presence of her own eggs and to eggs of other females, offering plastic discs as oviposition substrates. Although females did not clearly show a preference for plastic discs on which they had oviposited, they avoided plastic discs on which other females had oviposited. When eggs of other females were artificially placed on clean plastic discs, adult female mites avoided these discs, suggesting that the eggs were used as cues for oviposition preference. Cannibalism among juvenile siblings was lower than among non-siblings. These observations show that adult females and juveniles of G. liturivorus discriminate kin relationships among conspecific individuals. Therefore, oviposition preference by adult female G. liturivorus may lead to the reduced risk of cannibalism among offspring.
... From the perspective of the offspring, egg mass in squamates is typically positively correlated with offspring size [53,54]. Additionally, the egg mass difference we report probably reflects reduced water allocation, and lower egg watercontent reduces embryonic yolk absorption, resulting in smaller size and reduced offspring performance [55,56]. ...
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The use of fat to support the energy needs of reproduction (i.e. capital breeding) has been studied in a diversity of taxa. However, despite reproductive output (i.e. young or eggs) being approximately 70% water, little is known about the availability of internal resources to accommodate the hydric demands of reproduction. Recent research suggests that dehydration increases the catabolism of muscle as a means of maintaining water balance. Accordingly, we investigated the interactive effects of reproductive investment and water deprivation on catabolism and reproductive output in female Children's pythons (Antaresia childreni). Both reproductive and non-reproductive females were either provided water ad libitum or were water-deprived for three weeks at the time when reproductive females were gravid. We found that water-deprived reproductive females had, in general, greater body mass loss, epaxial muscle loss, plasma osmolality and plasma uric acid concentrations relative to the other groups. Furthermore , water-deprived females had similar clutch sizes compared with females with access to water, but produced lighter eggs and lower total clutch masses. Our results provide the first evidence that selective protein catabolism can be used to support water demands during reproduction, and, as a result, these findings extend the capital breeding concept to non-energetic resources.
... Adult female G. liturivorus spent most of their time on the plastic discs with their own eggs during the experiments, regardless of the presence of juvenile N. californicus; therefore, the behaviour of adult female G. liturivorus was not a response to IGpredators. Previous studies reported that parents or mothers of some species can increase the hatching rate by egg grooming and incubation (Aubret, Bonnet, Shine, & Maumelat, 2005;Boos, Meunier, Pichon, & K€ olliker, 2014;Munguía-Steyer, Favila, & Macías-Ord oñez, 2008). However, we did not observe any specific behaviour in which adult female G. liturivorus had active contact with the eggs. ...
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Intraguild (IG)-prey prefer to oviposit at sites with a low IG-predation risk of their offspring. However, IG-predators sometimes show oviposition preferences similar to those of IG-prey. In such cases, IG-prey eggs might need protection against IG-predators to survive. We tested this possibility using a system that consisted of an IG-prey, the predatory mite Gynaeseius liturivorus, and an IG-predator, the predatory mite Neoseiulus californicus. Both mite species feed on larvae of the western flower thrips, Frankliniella occidentalis, as a shared food source. When offered plastic discs as substrates for oviposition, both mite species preferred to lay eggs on the discs, regardless of the presence of heterospecifics. Subsequently, we examined G. liturivorus egg survival in the presence of only conspecific mothers or N. californicus, and the presence and absence of both mite species. The survival of G. liturivorus eggs was significantly reduced when kept with only N. californicus, but this reduction was not found in the presence of both G. liturivorus and N. californicus. These results indicate that G. liturivorus mothers improved the survival of the eggs in the presence of N. californicus. Behavioural observation revealed that adult female G. liturivorus mostly remained on the plastic discs with their own eggs during experiments. Furthermore, the presence of G. liturivorus mothers reduced the residence time of N. californicus on plastic discs with G. liturivorus eggs, whereas the residence time of G. liturivorus mothers was not affected by the presence of N. californicus. We conclude that mothers of G. liturivorus are able to increase the survival of their eggs by deterring IG-predators.
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Embryos incubated at 32 and 35°C hatch c10 days before those of 28°C and over 5 wk before those of 24°C. Hatching success was high at 24°C and 28°C but much lower at higher temperatures (32 and 35°C). Neonates incubated at low temperatures had larger snout-vent lengths and body masses, grew faster, and had higher sprint speeds than hatchlings incubated at higher temperatures. Hence, incubation temperatures that accelerate embryo development (32-35°C) did not maximize embryo survival and hatchling characteristics. An incubation temperature of 28°C provided the best balance between developmental rate, hatching success, and posthatch performances. -from Authors
This paper reports data on the mobilization of some yolk and eggshell nutrients and their incorporation into hatchlings and post-hatching yolk in an oviparous colubrid snake, Elaphe carinata. The incubation time at 30±0.3°C averaged 50.5 days. During incubation, pliable-shelled E. carinata eggs increased in wet mass. Dried shells from freshly laid eggs averaged 8.1% of the entire egg dry mass. Freshly laid eggs had significantly heavier shells than did hatched eggs with the same wet mass at oviposition. Dry mass conversion from egg contents of the freshly laid egg to hatchling averaged 81.1%. During incubation, approximately 63.7% of non-polar lipids and 72.1% of energy in egg contents of the freshly laid egg were transferred to the hatchling, with 36.3% of non-polar lipids and 27.9% of energy used for embryogenesis. Shells from freshly laid eggs had a higher level of calcium but a lower level of magnesium than did shells from hatched eggs. Fully developed embryos could obtain all magnesium from yolk but withdrew approximately 30.5% of their total calcium requirements from sources other than yolk. A few days after hatching, a decrease in post-hatching yolk dry mass was accompanied by an increase in carcass dry mass. This confirms that post-hatching yolk could be used to support early growth of hatchlings.