228 Population Biology Uca

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POPULATION BIOLOGY OFUCA THAYERIRATHBUN, 1900(BRACHYURA, OCYPODIDAE) IN A SUBTROPICAL SOUTH AMERICAN

MANGROVE AREA: RESULTS FROM TRANSECT ANDCATCH-PER-UNIT-EFFORT TECHNIQUES

BY

TNIA MARCIA COSTA1,2/and MARIA LUCIA NEGREIROS-FRANSOZO 1,2/

1/ NEBECC (Group of Studies on Crustacean Biology, Ecology and Culture)2/ Instituto de Biocincias, Departamento de Zoologia, Campus de Botucatu,

Universidade Estadual Paulista (UNESP), C.P. 510, CEP-18618-000 Botucatu, SP, Brazil

ABSTRACT

The population biology ofUca thayeriwas studied in a subtropical mangrove in Ubatuba, State

of So Paulo, Brazil. Two sampling techniques were used: transect sampling and catch-per-unit-effort. Size frequency distribution, sex-ratio, and reproductive period were analysed. For juvenilecrabs (CW < 4.6 mm), the transect procedure was most efcient, while ovigerous females weremost collected during the capture effort. Males were most numerous in the transect technique, whilein the catch-per-unit-effort there was no difference between sexes. The species showed a differentsize frequency distribution for each sampling procedure. The reproduction ofU.thayeri is seasonal,being more pronounced in the warmer months of the year. However, juveniles occurred all overthe year, although more numerous in the colder months. The success of the species in reproductiveactivity and the constant colonizationof the area can be attributedto the availabilityof foodresources

and differential occupation of the habitat by ovigerous females.

RESUMEN

Se ha estudiado la biologa poblacional de Uca thayerien un manglar subtropical de Ubatuba,Estado de So Paulo, Brasil. Se emplearon dos mtodos de muestreo: transectos y capturas porunidad de esfuerzo. Se analiz la distribucin de frecuencias de tallas, proporcin de sexos yperiodo reproductivo. Para los ejemplares juveniles y machos adultos (CW


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1202 TNIA M. COSTA & MARIA L. NEGREIROS-FRANSOZO

INTRODUCTION

Fiddler crabs live in the intertidal zone of mud-sandy sediments in estuarineand sheltered areas from tropical to warm-temperate regions. These crabs build

complex burrows in the substratum and display particular behaviour associatedwith burrow utilization. Both activities follow a tidal rhythm (Crane, 1975;Barnwell & Thurman, 1984; Macintosh, 1988).

The characterization of natural populations is considered to be of importancefor an understanding of their ecological stability. Seasonal variations of populationstructure, density, sex ratio, juvenile recruitment, and breeding intensity, togetherwith estimates of migration, birth, and mortality rates are the most frequentlystudied aspects regarding population biology (for crabs see, e.g., Pillay & Nair,1971; Hutchinson, 1981; Jones & Simons, 1983; Santos et al., 1995).

Fiddler crab populations are usually characterized by a high density comparedto other brachyurans, including other semiterrestrial crabs (Teal, 1958). Severaltechniques have been used to estimate the abundance of burrowing crabs, but onlya few are appropriate to be used in mangroves due to the complex structure ofthis habitat. Thus, one should be cautious when comparing different species orpopulations, or reports from different authors (Nobbs & McGuinnes, 1999).

Mangrove crab populations have been characterized by means of examiningsize frequency distributions (Genoni, 1985). These populations usually undergowide reproductive periods, during which females spawn several egg masses a year.Consequently, the modal classes change over time as a result of both reproductionand quick juvenile recruitment (Thurman, 1985; Macintosh, 1988).

The length of the breeding period can be inuenced by interacting biotic andabiotic environmental factors. Temperature has been identied as a main factorinuencing the reproductive process by promoting an increase of the metabolic rate

(in case of decapod crustaceans see Jones & Simons, 1983; Negreiros-Fransozo& Fransozo, 1992). Other authors emphasized the importance of the availabilityof food as a primary factor affecting growth rate and egg production in naturalpopulations (Pillay & Nair, 1971; Wenner et al., 1974; Seiple, 1979; Sastry, 1983).Reproductive periodicity can also be controlled by a combination of factors,including latitude and intertidal zonation (Thorson, 1950; Jones & Simons, 1983;Sastry, 1983; Emmerson, 1994).

According to Crane (1975), ddler crabs can be separated into two groups by themorphology of their carapace front. Wide-front crabs include Central, South, andNorth American species, while narrow-front crabs are found in the Indo-Pacic.Christy & Salmon (1984) have demonstrated that differences between wide andnarrow fronts are a consequence of variations of ecological pressures that promotealternatives, but with similarly adaptative strategies. However,U.thayeridoes nott in either group, as it presents an intermediate front-orbital distance.


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POPULATION BIOLOGY OFUCA THAYERI 1203

The crabs of the genus Uca have been the subject of a wide range of studiesrelated to reproduction and behaviour (Christy & Salmon, 1984; Thurman, 1985;Zucker, 1986; Caravello & Cameron, 1987; Mouton & Felder, 1995; Backwell &

Passmore, 1996; Yamaguchi, 1998; Backwell et al., 1999; Backwell et al., 2000).Nevertheless, U. thayeri has been seldomly studied. Salmon (1987) analysedits reproductive behaviour, Thurman (1987) and Costa & Negreiros-Fransozo(2001) addressed the relationship between the morphology of their mouthpartsand their ecological distribution, and Negreiros-Fransozo et al. (in press) reporton allometric relationships.

The ddler crab,Uca thayeriRathbun, 1900 is one of the most abundant speciesinhabiting mud ats within estuarine mangrove areas on the northern coast of thestate of So Paulo.

In this paper, we characterize the population structure and breeding season ofU. thayeri in an estuarine mangrove from a subtropical region of Brazil. Twosampling techniques were used and compared.

MATERIAL AND METHODS

The study site is located at the conuence of the rivers Comprido and Escuro(23290S 45090W), which ow onto Praia Dura. This mangrove area is situated inFortaleza Bay, Ubatuba, So Paulo state, Brazil (g. 1).

According to Negreiros-Fransozo et al. (2000), the mangrove vegetation at thestudy area is mostly composed of Laguncularia racemosa (L.) Grtn. (91.3%),but Avicennia shaweriana Stapf. & Leech. ex Mold. and Rhizophora mangleL.

are also present. Average tree height is 9.6 m, and mean density approximates3.12 trees/ha. Temperature varied from 21:6 3:0C during winter to 26:1 0:4Cin summer. Relative air humidity was 84:7 11:7% during winter and 93:6 5:7%in spring. Sediments are mostly composed of very ne sand and selectivity is veryhigh.

Crabs were collected each month by hand during low-tide periods by digging thesediment around the burrows with a garden shovel or a divers knife. All capturedcrabs were put into labelled plastic bags.

Two sampling techniques were used:1. Transect sampling (from January to December 1997). Nine sites were

delimited according to habitat features, namely the presence of mangrove trees,the predominance of sediments of different grain size, and distance from the rivermargin. The sites were established parallel to the river margin, with stratiedsamplings, following the humidity gradient.


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Fig. 1. Map of the study area, indicating the mangrove site in the Ubatuba region.

At each site, samplings were carried out monthly. Each sampling was com-pounded by a transect (5 m 0.40 m) in the same site, thus totalling 9 transects a

month.2. Catch per unit effort (CPUE) (performed monthly from July 1999 to June2000). Two experienced people scanned the sediment for U. thayeri specimensduring 15 minutes, within a sampling area of approximately 600 m2 along bothmargins of the Comprido River. Such a sampling area was delimited based onprevious scanning in the same mangrove, searching for U.thayerispecimens of amaximum size range.

In the laboratory, all crabs were identied and U. thayeri specimens wereselected and preserved in alcohol (70%).

The size (maximum carapace width, CW) of smaller crabs up to 10 mm CWwas measured using a dissecting microscope provided with a ocular micrometre,while larger specimens were measured using digital callipers (0.05 mm).

Both relative size of chelipeds and pleopod morphology were used for sex deter-mination. Smaller crabs (CW


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could be recognized, were categorized as non-sexable (ns). The presence of oviger-ous females was also recorded.

Population structureCrabs were classied according to the following demographic categories: adultmales, juvenile males, adult females, juvenile females, ovigerous females, and non-sexable juveniles. Size at sexual maturity was determined for the same populationby using the allometric technique (Negreiros-Fransozo et al., submitted), renderingan estimate of 12.5 mm CW for males and 12.9 mm CW for females.

Crab size estimates for samples obtained using the transect and CPUE methodswere compared by using the Mann-Whitney test ( D 5%) (Sokal & Rohlf,

1995). Such comparisons were made within the same demographic categorybetween crabs obtained by different sampling techniques. Specimens were groupedinto nine 3-mm size classes (starting at 2 mm CW). The normality of the sizefrequency distribution for the whole sample in each method was tested using theKolmogorov-Smirnov procedure ( D 5%; Zar, 1996).

Sex-ratio

A chi-square test for goodness of t ( D 5%) was performed to verify if thesex-ratio in the population sampled signicantly departed from 1 : 1 (Sokal &Rohlf, 1995).

Reproductive period and recruitmentBreeding intensity was analysed by relating the number of ovigerous females to

that of the total of adult females obtained by both sampling techniques. This ratio

was compared among months by means of the multinomial proportion comparisoncomplemented by Tukeys test (Goodman, 1964, 1965) ( D 5%).Monthly estimates of the proportion of juveniles, non-sexable crabs, and sex-

ratio were tested for a correlation with air temperature ( D 5%) (Zar, 1996).Average air temperature values were obtained at the Oceanographic InstituteStation (Ubatuba, SP) of the University of So Paulo.

RESULTS

A total of 690 specimens of Uca thayeri were obtained using the transectmethod, and 1,099 crabs using the CPUE technique. Descriptive statistics of eachdemographic category are shown in table I.

The largest male (CW D 25.2 mm) and ovigerous female (CW D 23.9 mm) wereobtained using the CPUE method, while the largest female (CW D 28.4 mm) was


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Fig. 2.Uca thayeri Rathbun, 1900. Total size frequency distribution(CW in mm) for each of the twosampling techniques employed.

obtained during transect sampling. With the exception of juveniles, transect andCPUE methods rendered different median size values of crabs in the remainingdemographic categories (Mann-Whitney, P < 0:05). Crabs collected using theCPUE technique were always larger.

Normality was rejected for overall size frequency distributions obtained us-ing both techniques (Kolmogorov-Smirnov test, g. 2). Monthly size frequency

distributions of U. thayeri obtained in each sampling technique are shown ings. 3 and 4. Ovigerous females occurred from January to March 1997 (transectsampling), and from August to October 1999 and December 1999 to May 2000(CPUE). Juveniles were recorded all year-round in both techniques, but in highernumbers using the transect method.

The presence of ns individuals was considered to evaluate seasonal recruit-ment trends. Since higher numbers of early juveniles were obtained by transect

sampling, only juveniles thereby obtained were used for analyses. Juvenile recruit-ment was found to occur during autumn and winter (from April to August, 1997).Estimates of overall sex-ratio differed according to sampling method. While

data from transect sampling suggested a male-biased proportion (1 : 0.7; 2 test,P 0:05). Fig. 6 shows the proportion of malesin each size class for both sampling techniques. For the transect technique, males


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Fig. 3.Uca thayeriRathbun, 1900. Monthly size frequency distributions for the transect technique.Upper and lower part of each histogram represent females and males, respectively. White bars Dadultcrabs;blackbars D ovigerous females; gray bars Djuveniles; cross-hatched bars D non-sexable

crabs.


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Fig. 4. Uca thayeriRathbun, 1900. Monthly size frequency distributions for the CPUE technique.Upper and lower part of each histogram represent females and males, respectively. White bars Dadultcrabs;blackbars D ovigerous females; gray bars Djuveniles; cross-hatched bars D non-sexable

crabs.


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Fig. 5.Uca thayeri Rathbun, 1900. Sex-ratio as a function of crab size (carapace width in mm).

prevailed in the rst three classes (from 2 to 8 mm CW). For the samples obtained

by the CPUE method, males outnumbered females in the size range from 5 to11 mm CW, while females prevailed from 17 to 20 mm CW.

The frequency of ovigerous females along the sampling period is shown forboth sampling methods in g. 7. For the transect technique (g. 7a), there were nosignicant differences among ovigerous ratio estimates over the year (P >0:05),while in the capture effort there was a signicant temporal variation (P < 0:05;g. 7b). In the latter, highest proportions of ovigerous females were found fromFebruary to March, which did not, however, differ signicantly from the ovigerousratio estimated in September, November, and January.

The Pearson linear correlation analyses performed on the results of eachsampling technique is based on the data presented in g. 8. For both techniques,the proportion of ovigerous females within the sampled population was found tobe positively correlated with mean air temperature (r D 0:62; P


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Fig. 6. Uca thayeriRathbun, 1900. Proportion and numbers (inside squares or ellipses) of males

for each size class for both sampling techniques. Asterisks indicate statistical differences from thefrequency of females in the same size class (2; P 0:05).

DISCUSSION

Difculties in sampling ddler crabs are often related to burrowing behaviourand to the complexity of the mangrove habitat. Most contributions on samplingmethods in mangrove areas aim to describe techniques to estimate the density ofmangrove crabs. A common technique consists on visual counts of either burrowsor active crabs over the bottom surface using quadrat sampling, thus minimizinghabitat disturbance (Macintosh, 1988; Nobbs & McGuinness, 1999; Macia et al.,2001). Nevertheless, this technique is not suitable when there is a need to obtain

information on size, age, and sex of the crabs.In this study, the median size of collected crabs differed signicantly in sam-ples obtained using different methods. Thus, the suitability of a given samplingprotocol depends on the objectives to be achieved. It is likely that more than onesampling method should be employed if one needs to cover different demographiccategories. For example, non-sexed individuals of Uca thayeri were mostly ob-tained by transect sampling in this study.


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Fig. 7. Uca thayeriRathbun, 1900. Temporal variation of the ovigerous female ratio in the twosampling techniques.Lower case letters indicate statistical comparisons of the ovigerousratio amongsampled months. Bars sharing the same letter represent no statistical differences (P >0:05). Black

bars D ovigerous females; white bars D adult non-ovigerousfemales.

Sex ratio in crabs of the genus Ucais frequently different from the 1 : 1 ratio,

males usually being more abundant (Genoni, 1985). In U. thayeri, males appearto outnumber females as evidenced by transect sampling. Such a difference can beattributed to several factors favouring a biased sex-ratio (Wenner, 1972).

Various studies have estimated similar male-biased populations in other ddlercrab species. ForU.pugnax(Smith, 1870), males encompass 59% of all sampledcrabs in Massachusetts (Valiela et al., 1974) and 53% in Georgia (Wolf et al.,1975). Similar results were reported for U. panacea Novak & Salmon, 1974 in

southern Texas (63%) and for U. rapax(Smith, 1870) (52%) (cf. Powers, 1975),for Venezuela populations ofU. rapaxandU. cumulantaCrane, 1943 (59 and 52%,respectively; Ahmed, 1976) andU.uruguayensisNobili, 1901 in Argentina (65%;Spivak et al., 1991).

Departures from the 1 : 1 sex-ratio can be a result of different processes.There might be sex-related capabilities to cope with environmental adversities,differential spatial or temporal utilization of habitat resources (Giesel, 1972),


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Fig. 8. Uca thayeriRathbun, 1900. Temporal variationof ovigerous females, juvenilesand ns crabsfor both sampling techniques. Temperature trend also shown.

contrasting mortality rates (Wolf et al., 1975; Genoni, 1985), or migration patterns(Montague, 1980; Murai et al., 1983). In the present study, the predominanceof males suggested by transect sampling may reect different patterns of spatialdistribution between sexes, since CPUE estimates did not differ signicantly fromthe 1 : 1 ratio.

Montague (1980) found males to be more abundant than females in speciesof the genus Uca, and suggested that this may be due to the sampling methodsemployed. Males spend more time on the surface than females, performingdefensive and mate-attracting behaviour as well as feeding for longer periods tocompensate for having only one chela and would thus be more readily caught(Valiela et al., 1974; Emmerson, 1994). Variability of the male behaviour mayhave been responsible for the results obtained in the CPUE method, rendering nostatistical basis to reject the hypothesis of equal proportions of males and females.


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The population structures of ddler crabs have been reported for some speciesand they were found to be closely related to each species life cycle and habits.A bimodal size frequency distribution has been veried for U. pugilator (Bosc,1802) in the U.S.A. by Colby & Fonseca (1984), U. subcylindrica (Stimpson,1859) in Mexico (Thurman, 1985) and U. uruguayensis in Argentina (Spivak etal., 1991). Such fact indicates a seasonal reproduction with at least two mainevents a year, which is a pattern commonly found in brachyurans from higherlatitudes (Seiple, 1979; Spivak et al., 1991). A unimodal frequency distributionwas reported for ddler crabs from temperate and tropical areas suggesting thatbreeding is continuous year-round (Thurman, 1985; Colpo, 2001).

Reproductive intensity in brachyurans can be measured by quantifying the

relative frequency of ovigerous females. According to Sastry (1983), the beginningand the duration of the reproductive period are dependent on the occurrence offavourable environmental conditions. The major controlling factors appear to belatitude, temperature, larval food availability, and intertidal zonation (Thorson,1950; Sastry, 1983).

In a warm-temperate area, species inhabiting the middle-high shore show amarkedly seasonal reproduction (often limited to a few months of the year),

while species living on the low shore breed continuously (Emmerson, 1994). Suchdifference can be related to seasonal changes in temperature, photoperiod, and theavailability of food resources, which are more variable in terrestrial than in aquatichabitats (Pillay & Ono, 1978).

In the present study, both sampling techniques showed that ovigerous femaleswere more abundant during March, while none had been recorded in June and July.According to Salmon (1987), ovigerous females occupy burrows with a chimneyshape near river margins, as observed by us during sampling. Since chimney-type

burrow entrances are more conspicuous, the density of ovigerous females may wellbe overestimated using the CPUE method.

The breeding period becomes longer going from cool to warm subtropicallocalities (Emmerson, 1994). Since most studies were conducted in temperateregions, seasonal breeding is well reported in the literature (table II). Yet, themajority of tropical crabs breed continuously, i.e., throughout the year, or haveprolonged breeding seasons compared to species at higher latitudes (Sastry, 1983).

Interestingly, the various Uca species occurring in the Transkei region follow atropical regime (Crane, 1975), but do not breed continuously (Emmerson, 1994).The reproduction of U. thayeri is also markedly seasonal, with a pronouncedreproductive activity from January to March, and an apparent resting period in Juneand July, when no ovigerous females were recorded. This could be attributed to thehigher availability of food resources during warmer months, when conditions forplanktonic development of larvae are thought to be optimal. Beyond this, the more


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TABLEIIComparative data for reproductive periods of ddler crabs

Species Study Reproductive Referencessite period

U.annulipes* India Winter Pillay & Nair, 1971(H. Milne Edwards, 1837)

U.subcylindrica U.S.A. / Summer Thurman, 1985(Stimpson, 1859) Mexico

U.lactea Japan Summer Murai et al., 1987(De Haan, 1835)

U.uruguayensis Argentina Summer Spivak et al., 1991Nobili, 1901

U.lactea annulipes* Africa Autumn Emmerson, 1994(H. Milne Edwards, 1837)

U.chlorophthalmus Africa Summer Emmerson, 1994(H. Milne Edwards, 1852)

U.urvillei Africa Summer Emmerson, 1994(H. Milne Edwards, 1852)

U.vocator hesperiae Africa Summer / Emmerson, 1994Crane, 1975 Autumn

U.longisignalis Mexico Summer Mouton & Felder, 1995Salmon & Ataides, 1968

U.spinicarpa Mexico Autumn Mouton & Felder, 1995Rathbun, 1900

U.vocator Brazil Summer Colpo, 2001(Herbst, 1804)

U.thayeri Brazil Summer Present studyRathbun, 1900

* (Variously cited as a species or as a subspecies.)

pronounced reproductive intensity for U. thayeri occurs in the warmer monthsof the year, also coinciding with a higher feeding activity of ovigerous females(Salmon, 1987).

With respect to the relative frequency of early recruits, data obtained using bothmethods agree in that the ingress of juveniles into the adult grounds is highest dur-

ing the colder months when reproductive activity is decreasing. Thorson (1950)suggested that timing, not temperature, was the ultimate factor affecting breed-ing patterns, allowing larvae to encounter adequate food supplies for development.Breeding in summer, when temperatures are higher and phytoplankton more abun-dant, would shorten development time and reduce larval predation (Emmerson,1994).


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: 315-341.MONTAGUE , C. L., 1980. A natural history of temperate western Atlantic ddler crabs (genus Uca)with reference of their impact on the salt marsh. Contr. mar. Sci.,23: 25-55.

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PILLAY, K. K. & N. B. NAIR , 1971. The annual reproductive cycles ofUca annulipes, Portunuspelagicusand Metapenaeus afnis(Decapoda: Crustacea) from the south-west coast of India.Mar. Biol., Berlin, 11: 152-166.

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POWERS

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SANTOS, S., M. L. NEGREIROS-FRANSOZO& A. FRANSOZO, 1995. Morphometric relationshipsand maturation in Portunus spinimanusLatreille, 1819 (Crustacea, Brachyura, Portunidae).Rev. Brasileira Biol.,55(4): 545-553.

SASTRY, A. N., 1983. Ecological aspects of reproduction.In: W. B. V ERNBERG(ed.), The biologyof Crustacea, 8, Environmental adaptations: 179-270. (Academic Press, New York).

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http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0160-8347^28^2918:3L.469[aid=4793778]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0101-1944^28^2917L.31[aid=3011992]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0025-3162^28^2976L.159[aid=4793779]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0003-3472^28^2935L.1334[aid=29568]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0160-8347^28^2918:3L.469[aid=4793778]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0018-8158^28^29449L.213[aid=4793775]


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to court. Bull. mar. Sci.,38(2): 384-388.

First received 8 January 2002.Final version accepted 6 November 2002.
http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0011-216X^28^2929L.79[aid=4710315]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0003-0147^28^29106L.321[aid=3011996]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0011-216X^28^2953:1L.94[aid=4793793]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0011-216X^28^2971L.565[aid=1161013]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0008-4301^28^2952:9L.1095[aid=4793791]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0003-0147^28^29106L.321[aid=3011996]http://fernando.ingentaselect.com/nw=1/rpsv/cgi-bin/linker?ext=a&reqidx=/0006-3185^28^29169L.215[aid=4793789]

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