Behavioral Ecology Vol. 10 No. 1: 68-72
© 1999 International Society for Behavioral Ecology
Offspring sex ratio is related to male body size in the great tit (Parus major)
a Zoology Department, University of Bern, CH-3032 Hinterkappelen Switzerland b Netherlands Institute of Ecology, Boterhoeksestraat 22, PO Box 40, 6666 ZG Heteren The Netherlands
Address correspondence to M. Kölliker or H. Richner. E-mail: mathias.koelliker{at}esh.unibe.ch richner{at}esh.unibe.ch.
Received 12 March 1998; revised 30 June 1998; accepted 6 July 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Sex allocation theory predicts that the allocation of resources to male and female function should depend on potential fitness gain realized through investment in either sex. In the great tit (Parus major), a monogamous passerine bird, male resourceholding potential (RHP) and fertilization success both depend on male body size (e.g., tarsus length) and plumage traits (e.g., breast stripe size). It is predicted that the proportion of sons in a brood should increase both with male body size and plumage traits, assuming that these traits show a father—offspring correlation. This was confirmed in our study: the proportion of sons in the brood increased significantly with male tarsus length and also, though not significantly, with the size of the breast stripe. A sex ratio bias in relation to male tarsus length was already present in the eggs because (1) the bias was similar among broods with and without mortality before the nestlings' sex was determined, and (2) the bias remained significant when the proportion of sons in the clutch was conservatively estimated, assuming that differential mortality before sex determination caused the bias. The bias was still present among recruits. The assumption of a father—offspring correlation was confirmed for tarsus length. Given that both RHP and fertilization success of male great tits depend on body size, and size of father and offspring is correlated, the sex ratio bias may be adaptive.
Key words: body size, great tits, Parus major, resource holding potential, sex allocation, sexual selection..
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Natural selection favors offspring sex ratios that maximize fitness returns per unit parental investment. The allocation of resources to sons versus daughters should be sensitive to the potential fitness gains through either sex (Charnov, 1982)
. As an example, if
male reproductive success increases more steeply with body size than does
female reproductive success, a male-biased offspring sex ratio is predicted
for large parents (Trivers and Willard,
1973), assuming that body size of parent and offspring is
correlated.
In birds, evidence for sex allocation in relation to parental traits
includes the zebra finch (Taeniopygia guttata) in captivity
(Burley, 1981,
1986), and the blue tit (Parus
caeruleus; Svensson and Nilsson,
1996) and the collared flycatcher (Ficedula
albicollis; Ellegren et al.,
1996) in wild populations. As predicted by sex allocation theory
(Charnov, 1982), females mated to sexually
attractive and/or high-quality males produced relatively more sons.
Furthermore, female zebra finches bias the sex ratio toward daughters when
they are relatively more attractive than their male mate
(Burley, 1981,
1986). In the zebra finch the sex ratio
bias may mainly arise through differential mortality after hatching
(Burley, 1986; but see
Oddie, 1998), whereas in blue tits and
collared flycatchers, a sex ratio bias seems to occur before or at hatching
(Ellegren et al., 1996;
Svensson and Nilsson, 1996). Thus, both
the timing and the mechanism of sex ratio modification can probably vary
(Clutton-Brock, 1986;
Oddie, 1998).
The great tit (Parus major) is a monogamous passerine with weak
sexual size dimorphism (e.g., Perrins,
1979). Both parents feed their young at the nest. A manipulation
of brood sex ratio did not result in a significant change of parental effort
(Lessells et al., 1998), suggesting that
raising male and female offspring may require a similar effort. Male great
tits compete both for territories and mates (Drent,
1983; Gosler,
1993; Perrins, 1979).
Male body size, as estimated from tarsus length in field studies (e.g.,
Senar and Pascual, 1997), and plumage
traits have been shown to correlate with measures of resource holding
potential (RHP), such as priority for access to food (e.g., tarsus
length: Garnett, 1981;
Maynard Smith and Harper, 1988;
breast stripe size: Lemel and Wallin,
1993; Maynard Smith and Harper,
1988; but see Wilson,
1992) and success in obtaining a breeding territory (tarsus
length: Drent, 1983). Furthermore,
male tarsus length in the great and blue tit correlates with both within-pair
and extrapair fertilization success (Blakey,
1994; Kempenaers et al.,
1992; Verboven and Mateman,
1997), and there is evidence that males with large breast stripes
are preferred by females (Norris, 1990).
For both tarsus length and breast stripe size, a parent—offspring
correlation has been demonstrated. The two traits are heritable as well as
sensitive to environmental conditions during growth
(Gebhardt-Henrich and van Noordwijk,
1991; Norris,
1993).
We investigated the relationship between the proportion of sons in a brood and parental phenotypes in the great tit. Given the importance of body size and plumage traits for male fitness, we evaluated the assumption that offspring body size correlates with male body size, and predicted that the proportion of sons is positively related to the male parent's tarsus length and/or breast stripe size.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The study was carried out in spring 1995 in a nest-box-breeding great tit population in the Bremgarten forest near Bern, Switzerland. The forest consists mainly of beech and pine trees with a few interspersed oaks and hornbeams. The habitat is of rather poor quality for breeding great tits, as indicated by a comparatively small average (mean ± SD) clutch size (7.74 ± 1.38, N = 91; cf. Oppliger et al., 1997
;
Smith et al., 1989). We visited
nest-boxes regularly to record laying date, clutch size, start of incubation,
hatching date, brood size, and fledging date. Nestlings were ringed 9 days
after hatching with numbered aluminum rings. Fourteen days after hatching, we
captured both parents, and for both nestlings and parents we recorded body
mass (to the nearest 0.1 g using a Sartorius balance), tarsus length (to the
nearest 0.1 mm using calipers), and wing length (to the nearest millimeter),
and took a blood sample from the brachial vein. Parents were aged according to
the color of the wing coverts as first-year or older birds (e.g.,
Gosler, 1993;
Perrins, 1979). We photographed the
ventral side of the males (holding the bird fully extended on its back and
using a reflex camera with a 105-mm macro lens), and later determined breast
stripe area from the slides projected onto a digitizing table. A reference
scale (graph paper) was photographed together with every bird to calibrate the
breast stripe measures of different birds. We measured the surface of the
ventral breast stripe to the nearest square millimeter including the area of
black feathers posterior to the edges of the white cheeks and anterior to the
legs. The mean of three measures of breast stripe size from the same slide was
used in the analysis. Photographing and measuring were each carried out by one
person (P.H. and I.W., respectively). As expected for a heritable trait
(Norris, 1993), breast stripe size was
significantly repeatable for male birds that were measured in more than 1 year
(r' =.412, F39,49 = 2.557, p
=.001; Lessells and Boag, 1987). In
the breeding seasons of 1996 and 1997, we recorded all the breeding birds to
assess local recruitment into the local breeding population and the sex of the
recruits.
For molecular sexing, blood was collected in capillary tubes (20 µl) and
transferred directly to an Eppendorf tube containing 100 µl EDTA buffer.
Samples were frozen the same day at -20°C. We extracted the DNA from a
subsample of the blood using a commercial kit (Puregene, Gentra Systems,
Minneapolis, Minnesota) following the manufacturer's protocol. Sexing was
carried out using RAPD (random amplified polymorphic DNA) markers
(Griffiths and Tiwari, 1993;
Lessells and Mateman, 1998). Random
primer sequences had previously been screened for their ability to amplify
femalespecific DNA fragments in great tits. Such a 10-mer primer was used for
polymerase chain reaction (PCR) with the extracted great tit DNA, and the
products were separated on an agarose gel. We identified females by the
presence of a 941 base-pair DNA fragment that does not occur in males (for
further details of laboratory procedures, see
Lessells et al., 1996;
Lessells and Mateman, 1998). In total, 48
out of 505 (=9.5%) eggs either failed to hatch or the chicks died before
blood samples were taken. Nestlings of 64 broods were sexed. To test the
accuracy of the molecular sexing method, the sexes of 69 individuals (31
females and 38 males) determined both at the nestling stage in 1995 (using
RAPD markers) and as breeding adults in 1996 or 97 (using breast stripe size
and the presence/absence of a brood patch;
Gosler, 1993;
Perrins, 1979) were compared. The
molecular and morphological sex determinations agreed in all 69 cases.
Statistical analysis of the proportion of sons in a brood was carried out
using logistic regression analysis with binomial errors and a logit link,
taking the number of sons in a brood as the dependent variable, and brood size
(number of sexed nestlings) as the binomial denominator. The statistical
significance of a sex ratio bias in relation to an independent variable was
assessed from the change in deviance (denoted as 
D) when that
variable was excluded first from (or included last into) the model
(Crawley 1993). The change in deviance is
asymptotically distributed as 
2 with corresponding degrees of
freedom (Crawley, 1993). Statistical
analysis of the proportion of sons in a brood was carried out using the
statistical package GLMStat (Beath, 1997).
We analyzed continuous dependent variables using the statistical package
Systat (Wilkinson, 1989).
Of the original 64 broods, the breast stripe size of 7 males could not be
measured either because the male had not been caught at the nest (3 cases) or
the photographic slide was missing (4 cases). Thus, all analyses in the
Results are based on a sample size of 57 broods. Experimental infestation of
some broods with fleas as part of a different experiment had no significant
influence on nestling sex ratio (p >.53), and the analysis was
therefore performed on the pooled data. Parametric tests were only applied to
continuous dependent variables with normal distributions. We used directed
statistical tests when the direction of the association between two variables
was specified by our hypothesis (Rice and Gaines,
1994). This is the case for the relationships between (1) the
proportion of sons in a brood and both male tarsus length and size of breast
stripe, (2) the proportion of sons among reproducing offspring and the
nestling sex ratio, and (3) the correlation between parent and offspring
tarsus length.
The proportion of male nestlings (age 14 days) in the local population was
51.9% (237 males and 220 females from 64 broods), and did not differ
significantly from unity (12 = 0.633, p
>.30). At the level of the brood, the observed distribution of the
proportion of male nestlings tended to deviate from the binomial distribution
[deviance in null model = 89.40 with 63 df; p (based on 1000
randomizations) =.07; see Westerdahl et al.,
1997].
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Proportion of sons among offspring
The proportion of sons in a brood was significantly and positively related to the male parent's tarsus length (Figure 1, Table 1), but not the female parent's tarsus length (Table 1). The proportion of sons also tended to be positively related to the size of male breast stripe (Table 1). In a model containing breast stripe size, the inclusion of male tarsus length led to a further significant reduction in deviance (
D = 13.30,
p <.001). Conversely, in a model containing male tarsus length,
the inclusion of breast stripe size led to no further significant reduction
(D = 1.11, p >.18). This difference may be partly
due to the observed correlation between breast stripe size and male tarsus
length (r =.27, n = 57, p =.042). The proportion of
sons was not significantly related to laying date (D = 1.65,
p >.19), male age (D = 0.17, p >.60),
female age (D = 0.16, p >.60), clutch size
(D = 0.39, p >.50), and brood size
(D = 0.30, p >.50). Brood size was not
significantly correlated with male tarsus length (Pearson's r = 0.21,
n = 57, p >.10). The absence of a significant correlation
between male and female tarsus length (r = -.03, n = 57,
p =.83) suggests that there was no size-assortative mating,
indicating that the sex ratio bias in relation to male tarsus length did not
arise indirectly via female tarsus length.
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The observed nestling sex ratio bias could arise both by variation in the
clutch sex ratio or differential mortality (e.g.,
Clutton-Brock, 1986). For 29 broods, all
the eggs laid could subsequently be sexed; in 28 broods, either not all
eggs hatched or nestling mortality occurred before blood sampling. The
relationship between the proportion of sons and male tarsus length was similar
in the two types of broods (Figure
1; interaction term: D = 0.001,
p >.95) and the proportion of sons did not differ between the two
groups Figure 1; D =
0.003, p >.95). These results suggest, but cannot firmly prove
(see Fiala, 1980), a sex ratio bias in
the eggs. A conservative test for a relationship between the proportion of
sons in the eggs and male tarsus length can be made by assuming that
differential mortality has caused the observed bias
(Ellegren et al., 1996). If chick
mortality before sex determination is taken as entirely son-biased in broods
with fathers having a smaller tarsus than the one predicting a 1:1
nestling sex ratio (as calculated from the logistic equation;
Figure 1), and entirely daughter-biased in
broods with larger fathers, the relationship between the estimated proportion
of sons in the eggs and male tarsus length remains positive and significant
(D = 5.76, p <.015). Thus an association between
sex ratio and male tarsus length was already present at egg laying.
Proportion of sons among local recruits
Thirty-six breeding pairs recruited at least one offspring into the local
breeding population the following years. The proportion of sons among these
recruits was, as expected, significantly related to the brood sex ratio at the
nestling stage (null model: D = 50.46; df = 35;
D = 15.41, p <.001). In a model containing
nestling sex ratio, the inclusion of male tarsus length (D =
0.43, p >.50), male breast stripe size (D = 0.07,
p >.70), or female tarsus length (D < 0.001,
p >.95) led to no further significant reduction in deviance. As
expected from the relationships between male tarsus and nestling sex ratio and
nestling and recruit sex ratios, the proportion of sons among recruits tended
to increase with male tarsus length (D = 2.83, p
=.058). The total number of recruits of a pair was not related to male tarsus
length (Spearman's rs =.05, p >.70).
Parent—offspring correlation of tarsus length
In a stepwise linear regression including both brood size and laying date,
mean offspring tarsus length was significantly related to the male but not to
the female parent's tarsus length (Figure
2, Table 2). This pattern was
similar for male and female offspring when analyzed separately (analyses not
shown).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Our results indicate that random segregation of sex chromosomes during meiosis is not the only mechanism determining the sex ratio of offspring (Charnov, 1982
;
Krackow, 1995;
Williams, 1979) in the great tit. As
predicted for the great tit, in which male RHP and fertilization success
correlate positively with tarsus length and size of breast stripe (see
Introduction), the proportion of sons in the brood was significantly related
to the male parent's tarsus length and tended to increase with the size of its
breast stripe. The relationship with male tarsus length remained significant
when breast stripe size was statistically controlled for, but the reverse was
not the case. This result may partly be due to the positive correlation
between breast stripe size and male tarsus length. The finding that the
relationship between the proportion of sons and breast stripe size was weaker
than tarsus length does not, however, necessarily indicate that breast stripe
size is of no biological importance. Tarsus length is measurable with greater
precision than breast stripe size and thus will show, due to lower measurement
error, a higher correlation coefficient. It may also be noted that the
proportion of deviance in brood sex ratio explained by breast stripe size
(5.4%; Table 1) is in the
range of the proportion explained by the white forehead patch in collared
flycatchers (8.3%), another example of a sexually selected plumage trait
(Ellegren et al., 1996).
Our findings suggest that the covariation between the proportion of sons
and male tarsus length was already present at egg laying and cannot be
explained purely by differential mortality (e.g.,
Dhondt, 1970), and that this sex ratio
bias may be adaptive: offspring tarsus length was significantly
correlated with the male parent's tarsus length, and the sex ratio at the
nestling stage was a significant predictor of the proportion of sons among
reproducing offspring in the local population. Thus, pairs with large males
produce both relatively more and larger sons which, due to their large body
size, may have a higher RHP and mating success than the relatively smaller
sons of pairs with small males (see Introduction). Daughters may therefore
yield higher fitness returns than sons to pairs with small males.
Three hypotheses could potentially explain the sex ratio bias in relation
to male tarsus length in great tits. Under the first hypothesis, local
resource or mate competition (see Gowaty,
1993) causes the observed sex ratio bias. In the Seychelles
warbler (Acrocephalus sechellensis) daughters stay as helpers in the
parental territory. In poor territories they compete with parents for
resources and thus become costlier for parents than sons. Consequently,
parents inhabiting poor habitats skew sex ratio in favor of sons
(Komdeur et al., 1997). In great tits
males disperse less after fledging than females
(Gosler, 1993;
Gowaty, 1993). To explain our result, the
overall nestling sex ratio should be female biased
(Gowaty, 1993), which was not the case.
In addition, a positive relationship between offspring body size and postnatal
dispersal distance would be require (i.e., small males disperse less than
large males). This is unlikely in a species where RHP (e.g., territory
acquisition) depends on body size. As expected, there is no such trend in our
data (sons: rs =.02, n = 28, p
>.50). Also, natal dispersal distance of sons was not significantly
correlated with the male parent tarsus length (rs = -.283,
n = 25, p >.15).
Under a second hypothesis, females may adjust the sex ratio of offspring in
the eggs to territory quality rather than to the quality of their male mate
per se, and large males, due to their superiority in competition over
territories (Drent, 1983), acquire and
defend higher quality territories (Richner,
1993). In a good territory, parents may be more able to raise
large offspring (Gebhardt-Henrich,
1990; Richner, 1989,
1992) and should therefore also produce a
larger proportion of sons. The hypothesis implies that the
parent—offspring correlation in tarsus length arises mainly through a
correlation between territory quality and male tarsus length
(Alatalo et al., 1986). The hypothesis
predicts a stronger relationship between the proportion of sons produced and
male tarsus length in poorquality habitats holding a limited number of good
territories. There competition is intense and male RHP may play an important
role in the settlement of breeding pairs. Indeed, in a great tit population in
the Netherlands where, contrary to our study population, food and thus
probably good territories are plentiful, no significant relationship between
hatchling sex ratio and measures of male body size was found (wing length and
body mass: Lessells et al.,
1996; tarsus length: Lessells CM, unpublished data).
The surprising lack of an association between the proportion of sons and
female tarsus length in the present study might indicate that male body size
is more important than female body size in determining the quality of the
breeding territory (Drent, 1983).
Under a third hypothesis, the correlation between the proportion of sons in
a brood and male parent tarsus length could arise by a female mate preference
for male genetic attractiveness (as predicted for the Fisher process) or
quality (as predicted for the good genes process) (see
Andersson, 1994). Both these processes
imply that the parent—offspring correlation in tarsus length is mainly
genetic and, in our case, would require a correlation between body size and
genetic attractiveness or quality. Offspring of large males would inherit the
large body size from their father, and these parents should therefore produce
a higher proportion of sons. The result that the proportion of sons only
increases with male but not female tarsus length would require that tarsus
length (or the correlated sexually selected trait) is inherited from parents
to offspring nonadditively (sensu Falconer and
Mackay, 1996), e.g., through paternal genomic imprinting
(Haig, 1997). Tarsus length is known to
be heritable in the great tit (e.g., Gebhardt-Henrich
and van Noordwijk, 1991), and it has also been shown that mate
preference is related to male tarsus length for both great and blue tits
(Blakey, 1994;
Kempenaers et al., 1992;
Verboven and Mateman, 1997). Thus the
potential for one or both these processes to operate may also exist. In this
context it may also be noted that breast stripe size may be an indicator of
male genetic quality (Norris, 1993).
We cannot disentangle, based on our data, whether the sex ratio bias arises
as a response to body-size—related territory quality, genetic quality,
or both. Offspring sex ratios should be measured in studies where the effects
of territory quality and parental phenotype have been separated experimentally
(e.g., Alatalo et al., 1986).
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Martin Brinkhof for help with logistic regression analysis and two anonymous referees for comments. We gratefully acknowledge financial support by the Swiss National Science Foundation, grant no. 31-43570.95 (to H.R.).
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P. Korsten, C. M. Lessells, A. C. Mateman, M. van der Velde, and J. Komdeur Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits Behav. Ecol., July 1, 2006; 17(4): 539 - 546. [Abstract] [Full Text] [PDF]
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A. Dreiss, M. Richard, F. Moyen, J. White, A.P. Moller, and E. Danchin Sex ratio and male sexual characters in a population of blue tits, Parus caeruleus Behav. Ecol., January 1, 2006; 17(1): 13 - 19. [Abstract] [Full Text] [PDF]
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A.N. Rutstein, H.E. Gorman, K.E. Arnold, L. Gilbert, K.J. Orr, A. Adam, R. Nager, and J.A. Graves Sex allocation in response to paternal attractiveness in the zebra finch Behav. Ecol., July 1, 2005; 16(4): 763 - 769. [Abstract] [Full Text] [PDF]
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M. K. Rathburn and R. Montgomerie Offspring sex ratios correlate with pair-male condition in a cooperatively breeding fairy-wren Behav. Ecol., January 1, 2005; 16(1): 41 - 47. [Abstract] [Full Text] [PDF]
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T. L. F. Martins Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment Behav. Ecol., January 1, 2004; 15(1): 174 - 180. [Abstract] [Full Text] [PDF]
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K. R. Oddie and C. Reim Egg sex ratio and paternal traits: using within-individual comparisons Behav. Ecol., July 1, 2002; 13(4): 503 - 510. [Abstract] [Full Text] [PDF]
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D. I. Leech, I. R. Hartley, I. R. K. Stewart, S. C. Griffith, and T. Burke No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus) Behav. Ecol., November 1, 2001; 12(6): 674 - 680. [Abstract] [Full Text] [PDF]
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A. N. Radford and J. K. Blakey Is variation in brood sex ratios adaptive in the great tit (Parus major)? Behav. Ecol., May 1, 2000; 11(3): 294 - 298. [Abstract] [Full Text] [PDF]
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