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First published online March 30, 2006
Journal of Experimental Biology 209, 1413-1420 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02138
Kidnapping of chicks in emperor penguins: a hormonal by-product?
1 Centre d'Etudes Biologiques de Chizé, Centre National de la
Recherche Scientifique, F-79360 Villiers en Bois, France
2 Office National de la Chasse et de la Faune Sauvage, F-79360 Villiers en
Bois, France
* Author for correspondence (e-mail: angelier{at}cebc.cnrs.fr)
Accepted 31 January 2006
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Key words: kidnapping, hormones, prolactin, non-cooperative breeding, seabird, emperor penguin, Aptenodytes forsteri
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;
Heinsohn, 1991). Why
individuals struggle, feed and provide care for unrelated offspring is not
clear (Riedman, 1982), and
such kidnapping appears to be inconsistent with evolutionary theory
(Riedman, 1982). However, some
ultimate factors have been proposed to explain this strange behaviour.
Firstly, kidnapping offspring could increase the kidnapper's breeding
experience and hence promote their future breeding success
(Riedman, 1982;
Komdeur, 1996;
Clutton-Brock, 2002).
Secondly, because of their apparent breeding success and thus high individual
quality, kidnappers could also enhance their probability of finding a mate for
the next breeding event (Clutton-Brock,
2002). Finally, kidnapping can even create an association with the
kidnapped offspring and thus enhance the probability of the kidnapper being
helped during the subsequent breeding event
(Heinsohn, 1991). Despite
these potential benefits, kidnapping behaviour could also be costly because
injuries could occur to the kidnapper if it tries to wrestle the offspring
from its parents. Additionally, kidnapping of a chick may lead to costly
parental behaviours because kidnappers might balance their need to satisfy
their own energy requirements with those of the kidnapped chick
(Stearns, 1992;
Heinsohn and Legge, 1999).
Thus, ultimate factors arguably do not explain the kidnapping or adopting
behaviour, except in some rare cases when the advantages outweigh
disadvantages (Heinsohn,
1991). Consequently, kidnapping and adoption have sometimes been
attributed to reproductive errors
(Riedman, 1982;
Birkhead and Nettleship, 1984;
Bustamante and Hiraldo, 1990) resulting from failure to recognise the
offspring.
Kidnapping behaviour could also be an artefact of proximate factors
selected to allow reproduction in particular environmental conditions
(Riedman, 1982). Among these
proximate factors, hormonal mechanisms deserve particular attention,
specifically prolactin (PRL), which is associated with parental physiology and
behaviour in males and females (review in
Buntin, 1996). PRL is also
known to be associated with parental care provided by helpers in cooperative
species (Vleck et al., 1991;
Schoech et al., 1996;
Brown and Vleck, 1998;
Khan et al., 2001). Kidnapping
of unrelated offspring could result from high residual hormone levels that are
involved in the drive to provide parental care
(Riedman, 1982;
Birkhead and Nettleship, 1984;
Jouventin et al., 1995).
Although kidnapping behaviour has been described in many species
(Riedman, 1982), to our
knowledge its proximate mechanism has never been experimentally studied.
In this study, we examined the physiological mechanism of kidnapping
behaviour. We tested specifically for the effect of artificially decreased PRL
levels on kidnapping behaviour in a non-cooperative species, the emperor
penguin Aptenodytes forsteri Gray, where the kidnapping of chicks by
failed breeders is commonly observed
(Jouventin et al., 1995). In
emperor penguins, ultimate factors could not explain kidnapping behaviour
because in most cases kidnappers neglect the chick only a few hours after the
kidnap (Jouventin et al.,
1995), so that there do not seem to be any obvious advantages for
kidnappers and kidnapped chicks. Emperor penguins thus constitute a promising
model to study the proximate factor triggering kidnapping behaviour. In
contrast to most bird species (Chastel and
Lormée, 2002), penguins that lose their eggs or their
chicks maintain high residual PRL levels throughout the whole breeding season
(Garcia et al., 1996;
Lormée et al., 1999;
Vleck et al., 2000). We
hypothesised that kidnapping behaviour is the result of these high levels of
PRL. Therefore, we predict that penguins with experimentally decreased PRL
levels would either stop kidnapping chicks or would kidnap them less
often.
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Materials and methods |
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).
Emperor penguins breed during the Antarctic winter in dense colonies on sea
ice. Monogamous pairs form in May, and following a 65 day incubation shift
undertaken by the male alone, females come back to relieve their partner and
bring food to the newly hatched chick. Then, both parents take turns to feed
at sea and to stay with their offspring, until the chicks leave the colony
when the sea ice breaks up
(Prévost, 1961).
Kidnapping behaviour
Kidnapping behaviour is mostly exhibited by failed breeders, especially
females, which have lost an egg or a young chick
(Jouventin et al., 1995).
During kidnapping, the biological parent always tries to protect the chick by
fighting (pecking, stroke of flipper) the intruder
(Jouventin et al., 1995), but
kidnappers are sometimes able to displace the parent and to get the chick
(Prévost, 1961). It is
very rare that kidnapping episodes end in physical injury to the parent or to
the kidnapper (H. Lormée, personal communication). Kidnapped chicks can
sometimes benefit from being fed by the kidnapping parent, but in most cases
kidnappers neglect the chick only a few hours after it was kidnapped, and the
chick left unattended dies due to hypothermia or predation
(Jouventin et al., 1995).
`Readoptions' of chicks by their parents are rare and occur only when the
kidnapper rapidly abandons the chick, when the parent is still close to the
chick and when the abandoned chick calls its parent
(Jouventin et al., 1995).
Kidnapping mostly occurs during August and September. Failed breeders are very
active during the weeks that follow the hatching period, when the presence of
chicks may stimulate kidnapping behaviour
(Prévost, 1961).
Manipulation of prolactin levels and prolactin assay
In winter 1999, 47 failed breeders were captured, individually marked by a
number painted on their chest and 1 ml of blood was collected, prior to
treatment, from the marginal vein of the flipper into heparinized tubes and
then immediately centrifuged. Plasmas were stored at –20°C until
measured for PRL concentration by radioimmunoassay as described
(Lormée et al., 1999).
Plasma PRL levels were experimentally decreased by treating the penguin with
an intramuscular injection of bromocriptine (ParlodelR long-acting
form, Sandoz, Basel, Switzerland; 1.5 mg kg–1 body mass).
Bromocriptine is a dopamine agonist that inhibits PRL secretion in mammals
(Bridges and Ronsheim, 1990;
Roberts et al., 2001;
Ben-Jonathan and Hnasko, 2001),
and in birds (Jouventin and Mauget,
1996; Reddy et al.,
2002). One group (bromocriptine group, N=23 birds) was
treated with bromocriptine; the other (control group, N=24 birds) was
treated with a vehicle (10% ethanol solution). The penguins were then released
near the colony. We did not observe any adverse effect of bromocriptine on the
behaviour of treated penguins and the sighting probability was similar between
groups (no difference in sighting probability, see the Results section).
Moreover, all treated penguins were seen later (at the end of the breeding
season) in the colony.
To monitor the effect of bromocriptine treatment on PRL levels, we kept two
additional birds (one injected with bromocriptine and one injected with a
vehicle) in captivity and blood was sampled 3 days and 8 days after the
capture. Afterwards, they were released back to the colony. All procedures
used in this study were approved by the ethical institution of the French
Polar Institute (IPEV). PRL levels were determined by radioimmunoassay at the
Centre d'Etudes Biologiques de Chizé (France) following the procedure
previously validated for the emperor penguin and described in Lormée et
al. (Lormée et al.,
1999). Only one assay was performed and the intra-assay
coefficient of variation was 3.5% (N=4 duplicates).
Behavioural monitoring and statistical analysis
We followed the kidnapping behaviour of the birds from the bromocriptine
and control groups during a 3 h scan each day during the week following
treatment. Hence we were able to attribute for each day and each monitored
bird a categorical datum (sighted and non-kidnapped=non-kidnapping state;
sighted and kidnapped=kidnapping state; or not sighted). A bird was classified
as a kidnapper when he or she was in physical contact with the chick.
To model the kidnapping behaviour, daily resighting data obtained for each
individual were analysed using multistate probabilistic models (MARK software,
White and Burnham, 1999).
These models include three kinds of parameters: sighting probability, survival
probability and transition probabilities from one state to another
(Nichols et al., 1994). We
used two states in our study: (1) birds present but not seen kidnapping, and
(2) birds seen kidnapping (Fig.
1). Contrary to classical statistical tests, this modelling
approach permits independent estimates of kidnapping and resighting
probabilities, hence providing a better estimate of the treatment effect on
the kidnapping behaviour of emperor penguins
(Lebreton et al., 1992) by
taking into account the probability of sighting of the bird. We focused mainly
on the probability of transition (
) from the non-kidnapping state to the
kidnapping state over one post-treatment day (t) to the next
(t+1). This allowed us to estimate the kidnapping probability of
failed breeders, and to test for an effect of bromocriptine treatment on the
kidnapping behaviour of these birds. In our study, the apparent survival
probability (S) represents the probability that an individual
survived and stayed on the colony from one post-treatment day (t) to
the next (t+1). Note that because all birds survived (they were seen
later in the breeding season), S did not measure the survival
probability per se. (1–S) represents the probability
that a penguin left the colony from one post-treatment day (t) to the
next (t+1) and did not come back before the end of the behavioural
monitoring period (Fig. 1).
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An effect of treatment on survival probability means that bromocriptine-treated and vehicle-treated penguins have not the same probability to stay on the colony from one day (t) to the next (t+1). An effect of state (kidnapping or non kidnapping) on survival probability means that kidnapping and non-kidnapping birds during the post-treatment day (t) differ in the probability of staying on the colony from this day (t) to the next (t+1). The sighting probability (P) represents the probability that an individual was seen during the daily 3 h scan of the post-treatment day (t), given that it is alive and present on the colony during this post-treatment day (t). (1–P) represents the probability that an individual was not seen during the daily 3 h scan of the post-treatment day (t) given that it is alive and present on the colony during this post-treatment day (t). An effect of treatment on sighting probability means that bromocriptine-treated and vehicle-treated penguins differ in the probability of being seen during a post-treatment day (t), given that they are alive and present on the colony during this day (t). An effect of state (kidnapping or non kidnapping) on capture probability means that kidnapping and non-kidnapping penguins have not the same probability of being seen on the colony during the post-treatment day (t), given that they are alive and present on the colony during this day (t).
The sighting probability is calculated by considering penguins not seen
during the post-treatment day (t) but seen later during the
behavioural monitoring period, for example during the post-treatment day
(t+1). Because these penguins were seen during the day
(t+1), they had not left the colony. They were therefore present but
not seen in the colony during the post-treatment day (t), allowing a
sighting probability P to be calculated. Concerning survival
probability, a bird seen in the colony during the day (t) would be
scored as staying on the colony from this post-treatment day (t) to
the next (t+1) if (1) it was seen during the day (t+1), (2)
it was not seen in the colony during the day (t+1) but was seen later
during the behavioural monitoring period; more details about the probabilistic
framework are given by Lebreton et al.
(Lebreton et al., 1992).
Because time since treatment could have an effect on kidnapping behaviour,
we tested the likelihood of a model allowing differences in kidnapping
probability between the first day of behavioural monitoring and the six
following days. Moreover, to check for an effect of bromocriptine treatment on
the first day of behavioural monitoring, we compared the likelihood of two
nested models: (1) a model with an effect of treatment, (2) a model with no
effect of treatment on the transition probability from the non-kidnapping to
the kidnapping state during the first day of behavioural monitoring. To test
for an effect of initial PRL level (individual covariate) on probabilities of
transition, we used a logit link function:
logit()=A+B(covariate), where A was the
intercept and B the slope. The logit link function permits constraint
of a parameter (i.e. probability of transition) to be a function of a
covariate (i.e. initial PRL level) by linking it to a linear formula
(Lebreton et al., 1992).
Moreover, the logit link function has the advantage of keeping estimates of
probabilities within the interval (0,1). The model selection was performed
following the parsimony principle (Burnham
and Anderson, 1998), based on Akaike's information criterion
corrected for small sample size (AICc). This measure combines the
goodness-of-fit of a model to data and the number of estimated model
parameters and therefore reflects model parsimony
(Burnham and Anderson, 1998).
We started our model selection from the most general model with an effect of
treatment and behavioural state on survival (S), sighting
(P) probabilities and an effect of treatment on transition
probabilities () from one behavioural state to another, and subsequent
models were constrained in a step-down approach
(Lebreton et al., 1992).
Differences between AICc values for two different nested models can be used to
determine which provides the most adequate description of the data based on
the fewest model parameters (
AICc=AICc of the starting model –
AICc of the constrained model). The model with the lowest AICc was considered
the best fit that describes the relationship. AICc values >2 are a
good indicator that the constrained model is preferable. AICc values
<2 and >–2 indicate that models are fairly similar in their
ability to describe the data, and the simplest model including the fewest
model parameters was then selected by following the parsimony principle
(Burnham and Anderson, 1998).
AICc values <–2 indicate that the starting model is
preferable. We tested whether the global model provided an adequate
description of our data, using the goodness-of-fit (GOF) test for multistate
models implemented in U-CARE software [R. Choquet, A. M. Reboulet, R. Pradel,
O. Gimenez and J. D. Lebreton (2003); U-Care User's Guide, Version
2.0. Mimeographed document, CEFE/CNRS, Montpellier
(ftp://ftp.cefe.cnrs-mop.fr/biom/Soft-CR/)].
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Results |
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Kidnapping behaviour and model selection
A total of 28 chick kidnappings were observed during the behavioural
monitoring. 30.4% of the penguins treated with bromocriptine and 54.2% of the
penguins treated with vehicle were sighted at least once with a chick. At
capture both groups were almost identical in body mass (bromocriptine,
27.53±0.38 kg; control, 27.08±0.72 kg; t-test:
t=0.6, P=0.55), sex ratio (
2=0.1,
d.f.=1, P=0.95), date of treatment (bromocriptine:
260.71±0.73 Julian days; control: 261.52±0.84 Julian days;
Mann–Whitney test: U=308, P=0.47) and PRL levels
(bromocriptine: 27.66±1.73 ng ml–1; control:
26.36±1.50 ng ml–1; t=0.65,
P=0.52).
The overall GOF test revealed that the global model fitted the data
satisfactorily (2=8.81, d.f.=11, P=0.64). Starting
with the general model (Fig. 2,
model 1; model with an effect of treatment and behavioural state on survival
(S) and sighting (P) probabilities and an effect of
treatment on transition probabilities () from one behavioural state to
another), we found that survival probability did not depend on treatment
(Fig. 2, models 1 and 2,
AICc=4.72). There was also no effect of behavioural state (kidnapping
or not kidnapping) on survival probability
(Fig. 2, models 2 and 3,
AICc=1.80). Sighting probability did not depend on treatment
(Fig. 2, models 3 and 4,
AICc=2.12), but on behavioural state
(Fig. 2, models 4 and 5,
AICc=–6.40). Although there was no effect of treatment on the
transition probability from the kidnapping state to the non-kidnapping state
(Fig. 2, models 4 and 6,
AICc=3.77), our model selection demonstrated a strong effect of
treatment on transition probability from the non-kidnapping state to the
kidnapping state (Fig. 2,
models 6 and 7, AICc=–12.70). There was no effect of time since
treatment on transition probabilities for the control group
(Fig. 2, models 6 and 8,
AICc=0.20) and for the bromocriptine group
(Fig. 2, models 6 and 9,
AICc=–0.94). Moreover, the model allowing an effect of treatment
on the transition probability from the non-kidnapping state to the kidnapping
state during the first day of behavioural monitoring had a lower AICc than the
simpler model (Fig. 2, models A
and B, AICc=–7.57). We also observed no effect of plasma PRL
levels measured prior to the injection of bromocriptine or vehicle on this
transition probability for the control group
(Fig. 2, models 6 and 10,
AICc=–0.34). This effect was, however, strong in the
bromocriptine group (Fig. 2,
model 6 and 11, AICc=5.88).
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AICc=–12.70). Within the bromocriptine group,
kidnapping behaviour was not totally suppressed and the transition probability
from the non-kidnapping to the kidnapping state (12) was
positively correlated to the plasma PRL level measured before injection of
bromocriptine [logit (12)=A+B(PRL level before
injection), B=1.42±0.64 (mean ± s.e.m.), [0.16, 2.68]
95% CI]. Similarly, this relationship was selected because the model with an
effect of plasma PRL level measured before injection on this transition
probability within the bromocriptine group had a lower AICc than the model
without this effect (Fig. 2,
models 6 and 11, AICc=5.88). Within the bromocriptine group, kidnappers
had higher PRL levels prior to the bromocriptine treatment than non-kidnappers
(t-test: t=–3.45, P=0.005,
Fig. 4) whereas this was not
observed in the control group (t-test: t=–0.99,
P=0.33).
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).
Moreover, bromocriptine is particularly well known as a suppressant of PRL
secretion in penguins. Jouventin and Mauget injected 30 king penguins
Aptenodytes patagonicus with the same bromocriptine dose as in the
present study, resulting in a 78% decrease in PRL levels
(Jouventin and Mauget, 1996).
King penguins and emperor penguins have the same endogenous mode of secretion
of PRL (Garcia et al., 1996;
Lormée et al., 1999)
and the decrease observed in king penguins was similar to the decrease that we
observed in our bromocriptine treated penguin (i.e. 75%), which confirms the
efficiency of bromocriptine treatment in our study.
When penguins were injected with bromocriptine, the probability that they
kidnapped a chick was on average 4.5 times lower than that of penguins
injected with a vehicle. Although bromocriptine, as a dopamine agonist, might
have reduced the probability of kidnapping by other mechanisms that its
prolactin-inhibiting properties
(Ben-Jonathan and Hnasko,
2001), this result is consistent with the hypothesis that
kidnapping of chicks by failed breeders is the result of high residual level
of PRL.
Survival probability (S) did not vary with treatment or
behavioural state, suggesting that the probability to leave the colony did not
depend on treatment (i.e. PRL levels). Within the control group, failed
breeders had a high probability of transition from the non-kidnapping to the
kidnapping state (0.77±0.10). This result illustrates the high
frequency of kidnapping in emperor penguins. Our results suggest that this
behaviour is probably more common than previously thought in the emperor
penguins; Jouventin et al. had found that only 28.7% of penguins kidnapped
during the rearing period (Jouventin et
al., 1995).
Although kidnapping behaviour was reduced by an injection of bromocriptine, it was not totally suppressed. This could be due to a temporary absence of effect of bromocriptine on PRL levels. It may have taken several days before bromocriptine had its full effect on PRL levels and bromocriptine-treated penguins could have therefore been more likely to engage in the kidnapping behaviour for the first day and less likely to engage in this behaviour later. We found no effect of time since treatment on transition probabilities, however. Moreover, the probability of kidnapping was affected by treatment since the first day of behavioural monitoring. These results demonstrate that bromocriptine had an effect on kidnapping probability since the day following the treatment.
Within the bromocriptine group, the model selection showed that the probability of kidnapping a chick increased with increasing plasma PRL levels measured prior to bromocriptine treatment. Kidnappers had higher PRL levels prior to bromocriptine treatment than non-kidnappers within this group. As these relationships were not observed within the control group, it raises the question of the physiological mechanism linking PRL and kidnapping behaviour. Our results suggest that kidnapping behaviour might depend on a threshold level of PRL. Bromocriptine administration could have failed to diminish the PRL level below this threshold in penguins with the highest PRL levels prior to the treatment, which could explain why these birds still kidnapped chicks during the study whereas birds with low PRL levels prior to bromocriptine treatment did not. As a consequence, high PRL level would be necessary to promote kidnapping behaviour. Future studies should now determine what PRL level represents a threshold for kidnapping to occur by sampling blood from bromocriptine-treated penguins at the exact time they are engaged in kidnapping behaviour.
Although PRL is involved in both parental and kidnapping behaviour
(Lormée et al., 1999;
this study), there are some important differences between the care provided by
kidnappers and parents. Kidnappers abandon the chick after few hours,
suggesting that there are differences in the mechanisms underlying the
expression of care between parents and kidnappers. Emperor penguin parents are
able to recognize their chick by voice and they reject all solicitation for
food apart from those of their own young
(Jouventin et al., 1979).
Therefore, kidnappers might abandon the kidnapped chick after few hours,
because they have never heard its voice before and do not recognize it.
Elevated PRL levels are necessary to initiate kidnapping behaviour, but they
do not seem sufficient to maintain care during a long period.
In contrast to most bird species where the loss of eggs or chicks lead PRL
to return rapidly to basal levels (Buntin,
1996; Chastel and
Lormée, 2002), PRL secretion in several penguin species is
poorly influenced by egg or chick stimuli and stays elevated for weeks and
even months after failure (Garcia et al.,
1996; Lormée et al.,
1999; Vleck et al.,
2000). This unusual pattern of PRL secretion has been interpreted
as an adaptation to maintain parental care despite long absences at sea to
forage (Garcia et al., 1996;
Lormée et al., 1999).
During breeding, emperor penguins have to undertake long foraging trips on
distant ice-free areas (Ancel et al.,
1992) and female emperor penguins undergo a 2 month foraging trip
just after laying, coming back at the expected time of hatching to relieve
their mate (Prévost,
1961). At this time, these birds will return to the colony with
elevated PRL levels and not know if their mate has lost the egg or the newly
hatched chick (Lormée et al.,
1999). Consequently, penguins that lose their egg or their chick
during a foraging trip still maintain high residual PRL levels over a long
period (Garcia et al., 1996;
Lormée et al., 1999;
Vleck et al., 2000). This,
combined with colonial breeding and the absence of a nest and territory,
probably facilitates kidnapping. Previous studies reported that failed
breeders become kidnappers through some process of social stimulation
(Prévost, 1961;
Jouventin et al., 1995), and
kidnapping behaviour often occurs when a failed breeder perceives stimuli from
a chick asking for food to its parents
(Jouventin et al., 1995). It
suggests that both elevated prolactin levels and environmental stimuli are
necessary for the display of kidnapping behaviour.
Ultimately, kidnapping behaviour does not seem to be costly for failed
breeder emperor penguins. Failed breeders probably do not support the cost of
raising unrelated young since in most cases kidnapping and adoption only last
for a few hours (Jouventin et al.,
1995). On the other hand, the benefits of kidnapping for emperor
penguins are not obvious. Kidnapped chicks are seldom fed and sometimes die
during the struggle for kidnapping
(Jouventin et al., 1995).
Young failed breeders may benefit from being kidnappers by gaining breeding
experience (Riedman, 1982;
Jouventin et al., 1995;
Komdeur, 1996;
Clutton-Brock, 2002). This is
unlikely, however, since most kidnappers are known to have already bred
successfully in previous years (Jouventin
et al., 1995). Kin selection hypothesis
(Hamilton, 1964) is also
unlikely to be supported here, as kidnapping does not seem to be directed
towards selected chicks. Moreover, a recent study showed that kin selection
did not promote fostering behaviour among Antarctic fur seals
Arctocephalus gazella, which have a comparable breeding system to
emperor penguins with long absences at sea and breeding occurring in densely
populated colonies (Hoffman and Amos,
2005). Hence, emperor penguins would have no direct fitness
interest in kidnapping chicks.
Conclusion
In cooperative species there is increasing empirical evidence that group
augmentation by kidnapping increases the fitness of group members
(Clutton-Brock, 2002). In
contrast, our experimental study suggests that kidnapping in the
non-cooperative breeding emperor penguin may be due to the hormonal byproduct
of a reproductive adaptation to extreme conditions, such as long foraging
trips during the Antarctic winter. As kidnapping in emperor penguins offers no
obvious benefits and does not seem to entail significant costs, this behaviour
might be considered as neutral, and not subject to selection pressures.
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Acknowledgments |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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