Spatiotemporal Distribution and Population Structure of Monokalliapseudes schubarti (Tanaidacea:...

Hindawi Publishing CorporationThe Scientific World JournalVolume 2013 Article ID 363187 9 pageshttpdxdoiorg1011552013363187

Research ArticleSpatiotemporal Distribution and Population Structure ofMonokalliapseudes schubarti (Tanaidacea Kalliapseudidae) inan Estuary in Southern Brazil

Felipe Freitas-Juacutenior1 Martin Lindsey Christoffersen2

Joafracircncio Pereira de Arauacutejo2 and Joaquim Olinto Branco1

1 Centro de Ciencias Tecnologicas da Terra e do Mar (CTTMar) Universidade Vale do Itajaı (UNIVALI)CP 360 88302-202 Itajaı SC Brazil

2 Departamento de Sistematica e Ecologia Universidade Federal da Paraıba (UFPB) 58059-900 Joao Pessoa PB Brazil

Correspondence should be addressed to Martin Lindsey Christoffersen mlchristdseufpbbr

Received 6 August 2013 Accepted 15 September 2013

Academic Editors X Pochon and W O Watanabe

Copyright copy 2013 Felipe Freitas-Junior et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Monokalliapseudes schubarti is an endemic tanaidacean microcrustacean from southeastern Brazil to Uruguay inhabiting lowenergy estuaries Saco da Fazenda is located in the estuary of the Itajaı-Acu River state of Santa Catarina Brazil It is exposed tostrong anthropic impact and receives intensive flows of domestic wastewater solid residues and drainage activities Specimens ofM schubartiwere collected monthly in the intertidal and subtidal regions of Saco da Fazenda in four stations defined as a functionof the physiography of the environment during the period of July 2003 to June 2004 Fecundity values were high with continuousreproductive activity during the whole period of study The greatest population densities were observed in the intertidal regionwhere they are nevertheless intensely consumed by birds swimming crabs and fish This species represents a fundamental link inthe food chain of Saco da Fazenda transferring energy from the detritus level to higher trophic levels Habitat disturbance and highorganic matter may represent factors controlling the distribution of populations of M schubarti For this reason the species maybe used to monitor anthropic effects in estuarine areas

1 Introduction

Monokalliapseudes schubarti [1] is a tanaidacean microcrus-tacean of no known economic importance but with a relevantecological role in estuarine environments

It is found in the region located between Cabo Frio Riode Janeiro and La Plata River Uruguay [2 3] It inhabits lowenergy estuaries where individuals construct ldquoU-rdquo shapedtubes reaching a depth of up to 15 cm [1 4 5] It has beenfrequently cited in the literature asKalliapseudes schubarti butis now included in the monotypic genus Monokalliapseudessince Gutu [6] elevated the subgenus to generic rank Thereare 39 species in the primarily circumtropical family Kalli-apseudidae [7] which was inferred to be monophyletic onthe basis of three molecular loci [8] Members of this familyin addition to being deposit feeding as other tanaidaceans are

thought to be filter feeders based on the rows of long plumosesetae on their chelipeds [9 10] F P P Leite and P E P Leite[11] provided evidence that Kalliapseudes gianucai describedby Bacescu [12] and known only from the type locality in thestate of Rio Grande do Sul Brazil represents a dimorphicmale stage and is thus a synonym ofM schubarti

Monokalliapseudes schubarti displays pronounced spatialand seasonal variations in population densities having a rapiddevelopment continuous reproductive activity high recruit-ment potential and mass mortalities being considered an 119903-strategist [5 13ndash17] This species is important in communitystructuring [18] having a relevant function in the feeding offish crustaceans and aquatic birds [4 13 19 20] It was foundto represent a dominant species in the faunal community ofLagoa dos Patos Rio Grande do Sul [21ndash24] Gamboa doPereque Parana [14] Paranagua Bay Parana [25 26] and

2 The Scientific World Journal

Atalaia BeachSaco daFazenda

Navegantes

Itajaiacute

ItajaiacuteIIIIV

I

II0 150 300 450

N

(km) acute

-Accedilu

Figure 1 Studied area indicating the collecting sites in Saco da Fazenda Santa Catarina Brazil (source modified of chart 1801 fromDiretoriade Hidrografia e NavegacaoDHN)

Araca beach Sao Paulo [13] Such abundant opportunisticcommunity structuring persistent and resilient species havebeen found to be excellent biotic indicators and have beenincreasingly used as such [18 20 27ndash29]

In south and southeastern Brazil M schubarti has beenstudied in tidal flats [26] fine-grained beaches of low slopeand high organic matter [13 15] estuaries [16] and coastallagoons [17]

In the state of Santa Catarina about halfway along its totalgeographic range M schubarti was found to be very abun-dant in the estuarine area of Saco da Fazenda [30]This paperreports the spatiotemporal distribution population structureand reproduction ofM schubarti in this environment

2 Material and Methods

21 Study Area Saco da Fazenda is located in the estuaryof the Itajaı-Acu River between 26∘5310158403310158401015840ndash26∘5510158400610158401015840 S and48∘3810158403010158401015840ndash48∘3910158401410158401015840W state of Santa Catarina Brazil It ischaracterized as a shallow artificial estuary [31] because of theconstruction of piers to rectify and stabilize the canal of theItajaı-Acu River These piers have isolated a previous affluentof this river [32] and water exchange became restricted Thetotal surface area of Saco da Fazenda is about 63 times 105m2[31] The substrate is siliceous argillic and maximum depthis 20m except in the river canals which attain 90m depthTidal variations are not higher than 14m Mean annualrainfalls range from 1250 to 1500mm [33]

The ecosystem of Saco da Fazenda despite its exposureto a strong anthropic impact and to an intensive dischargeof domestic wastewater solid residues [33] and drainageactivities [32] supports a high diversity of animals and serves

as a natural nursery for several species of crustaceans fishand birds which may useM schubarti as a source of food

22 Methods Specimens were collected monthly in theintertidal and subtidal regions of Saco da Fazenda in fourareas (Figure 1) between July 2003 and June 2004 In eacharea six samplings with a Van Veen grab (0075m2) wereconducted during high spring tides Three samples wereobtained in the intertidal region (40 cm depth) and threein the subtidal (140 cm depth) For the analyses the threesamples from each region were considered as a single sample(0225m2 per region)

The tanaidaceans were separated from the sediment witha 05mmmesh-size sieve fixed in 4 formalin and preservedin labelled bottles In the lab the residual sediment wasremoved and the total number of specimens per sample wasdetermined

To estimate the density of males females and juvenilesalong the year as well as the number of females in repro-ductive activity a subsample was established from the totalnumber of collected individuals To obtain this capturedanimals were put in a beaker of 250mL with water Thematerial was homogenized and three samples of 20mL wereextractedWe used themean value of individuals for the threesamples and calculated the total number of individuals persample for that collecting month

To characterize the structure of the population weobtained two new samples from the field during the summerand winter of 2005 Due to the low abundance of organ-isms captured in these samples the samples were pooledand 220 entire individuals were chosen for the classes ofmales females ovigerous females and juveniles which were

The Scientific World Journal 3

2003 2004

Winter Spring FallSummer3530

2025

1510

50

2018

1012

6420

8

1416

Salin

ity (

)

Tem

pera

ture

of w

ater

(∘C)

SalinityWater (∘C)

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

Figure 2 Mean temporal variation of salinity and temperature ofbottom water during the period from July 2003 to June 2004 (meanplusmn standard error)

measured from the tip of the rostrum to the tip of the telsonwith a micrometric ocular on a stereoscopic microscope[2] The eggs and mancae in the marsupium of each femalewere counted the largest diameter of these was obtained andthen classified by developmental stage [11] The relationshipbetween the length of females and the number of eggs andmancae was determined by simple regression analysis [34]utilizing 80 individuals of each stage selected randomlyamong those with intact marsupia

Temperature and salinity of the bottom water weremeasured monthly during the morning and afternoon fromJuly 2003 to June 2004 The salinity was recorded using arefractometer A sample of sediment was collected at eacharea every trimester (four replicates per zone) which wasused for granulometric analysis andmeasurement of calciumcarbonate content and organic matter Calcium carbonatewas determined using the gravimetricmethod from a sampleof 100 g which was dissolved in hydrochloric acid (HCL)at 50∘C To determine total organic matter the sampleswere burned in a muffle furnace at 800∘C for eight hoursand the content was determined by the difference betweeninitial and final weights For the granulometric and texturalcharacterization of the sediment samples were wet-sieved atintervals of 14 phi [35] and then weighed [36] To comparegranulometry calcium carbonate content and organicmatteramong stations between intertidal and subtidal regions weconducted a one-way ANOVA for each comparisonThe datawere transformed into the one-fourth root

To verify if abundance of M schubarti is correlated withtemperature and salinity the Pearson correlation was tested(with data transformed into the one-fourth root) To comparetotal abundance of M schubarti with the three studiedsediment parameters (granulometry calcium carbonate andorganic matter) we also used one-way ANOVA

The chi-square test (1205942) with Yates correction at level ofsignificance of 5 (119899 minus 1 degrees of freedom) was applied

to verify the possible differences among the sex ratio percollecting month and total number of adults

To evaluate the spatiotemporal variation of tanaidaceanswe applied a two-way ANOVA on data of total abundanceand number of individuals for each size class ofM schubarti(males females ovigerous females and juveniles) for thedifferent months of the year and regions (intertidal and sub-tidal) When the data did not fit these requirements we usedthe transformation in the fourth root Such transformationsantedated the use of ANOVA which was followed by Tukeyrsquostest (120572 = 005)

3 Results

31 Abiotic Parameters Themean bottom water temperatureshowed a typical seasonal pattern with significant differencesamong the studied months (119865 = 69212 df = 11 84 119875 lt0001) Highest mean values occurred in February (266∘C)and April 2004 (268∘C) and the smallest occured in May(173∘C) and June (178∘C) of this same year (Figure 2)

Salinity varied significantly among collecting months(119865 = 44043 df = 11 84 119875 lt 0001) Highest valuesweremeasured in September 2003 (161) andApril 2004 (159)and the smallest value was found in December 2003 (21)(Figure 2)

Grain size calcium carbonate content and organicmatterpresented significant differences among the intertidal andsubtidal regions (119865 = 41649 119875 lt 0001 119865 = 5028 119875 =0033 119865 = 30487 119875 lt 0001 resp df = 1 30 for allmeasurements) Mean grain size and mean values of calciumcarbonate and organic matter were higher in the subtidalregion (803 plusmn 023 phi 714 plusmn 058 1105 plusmn 044 resp)than in the intertidal region (554 plusmn 030 phi 544 plusmn 053666 plusmn 062 resp)

Calcium carbonate was significantly different when com-pared among seasons (119865 = 9653 df = 3 28 119875 lt0001) (Figure 3) Fall presented the smallest mean (139 plusmn024) while the largest mean was observed in spring (169plusmn078) Grain size and organic matter content did not varysignificantly among stations (119865 = 0108 119875 = 0955 and119865 = 0788 119875 = 0513 resp df = 3 24)

32 Spatiotemporal Distribution Total abundance of Mschubarti was not correlated to water temperature and salini-ties in the intertidal regions (119903

119904water ∘C = 008 119899 = 48 119875 = 06119903119904 salinity = minus018 119899 = 48 119875 = 02) nor in the subtidal regions(119903119904water ∘C = 005 119899 = 48 119875 = 07 119903

119904 salinity = minus009 119899 = 48119875 = 05)

Organic matter and grain size presented a significantnegative correlation with the total abundance ofM schubarti(119903 = minus038 119899 = 32 119875 = 0034 119903 = minus052 119899 = 32119875 = 0003 resp) The calcium carbonate content did notshow a significant correlation with the total abundance ofMschubarti (119903 = minus015 119899 = 32 119875 = 0404)

Density M schubarti in the intertidal region (Figure 4)was significantly larger than that in the subtidal region (119865 =1723 df = 22 70 119875 = 0045) while abundances ofmales females ovigerous females and juveniles were also


150

135

175

170

165

160

145

140

155

Winter Spring Summer Fall

Calc

ium

carb

onat

e con

tent

()

Figure 3 Mean values of calcium carbonate of Saco da Fazendaduring the seasons of sampled period (mean plusmn standard error)

Winter Spring FallSummer

2003 2004

12

13

14

15

16

17

18

19

InfralittoralIntertidal

Nin

divi

dual

s0225

m2

Janu

ary

Febr

uary

Mar

ch

April

May

June

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

July

Figure 4 Monthly variation of the mean density of Monokalli-apseudes schubarti per 0225m2 (in this case transformed to thefourth root) in intertidal and subtidal of Saco da Fazenda duringthe period from July 2003 to June 2004 (mean plusmn standard error)

significantly correlated (119865 = 16199 119875 lt 0001 119865 = 23029119875 lt 0001 119865 = 16369 119875 lt 0001 119865 = 20822 119875 lt 0001resp df = 1 94 for all data)

The density of males and females varied monthly (119865 =4747 and 119865 = 3895 resp 119875 lt 0001 and df = 11 84 forboth data) with a peak in spring and another in summerfollowed by subsequent declines and remaining low duringfall (Figures 5(a) and 5(b))

Statistical differences were verified in the density ofovigerous females among months (119865 = 5908 df = 11 84119875 lt 0001) However this density varied only slightly alongthe year with the statistical differences being a reflection

of the strong peak occurring at the beginning of summer(Figure 5(c))

Juveniles varied monthly (119865 = 3919 df = 11 84 119875 lt0001) with a peak of density at the beginning of springdecreasing gradually along the following stations The lowestvalues occurred during fall (Figure 5(d))

33 Length Structure The sex ratio (females males) of thepopulation was 9 1 Females strongly predominate (1205942 =8 47032 119875 lt 0001)

The total length formales varied from52 to 135mmwiththe largest captures occurring in classes of 95 and 100mmand the mean total length being 98 plusmn 01mm (Figure 6(a))

In females total length ranged from 45 to 133mmpresenting a polymodal distribution with peaks in the classesof 50 60 and 85mm and with a mean length of 79 plusmn01mm (Figure 6(b)) For ovigerous females the lengthvaried from 82 to 139mm with modes in the classes of 95105 and 130mm and with a mean size of 106 plusmn 01mm(Figure 6(c))

In juveniles the range of variationwas from 20 to 45mmwith a peak in the class of 30mm and a median length of33 plusmn 00mm (Figure 6(d))

34 Reproductive Period and Fecundity Monokalliapseudesschubarti presented females in reproductive activity duringthe whole sampled period reinforcing the hypothesis ofcontinuous reproduction The largest density of ovigerousfemales was observed in January 2004 (19825 plusmn 6521) whilein April 2004 the smallest numbers were registered (963 plusmn336) (Figure 5(c))

Juveniles were encountered throughout the year Thelargest peak of recruitment was registered in October andNovember 2003 (141527 plusmn 47558 and 125378 plusmn 33292resp) and the smallest intensity occurred in May 2004 with10773 plusmn 2373 individuals (Figure 5(d))

In Table 1 we present the fecundities of M schubarti inrelation to their distinct stages and respective sizes

Analyzing the number of eggs and mancae stages relativeto the length of females we verified that fecundity showed aconsiderable tendency to increase with the size of the femaleThis correlation was corroborated with the determinationcoefficients found both for the eggs (1199032 = 031 119875 lt 0001)and for the mancae (1199032 = 057 119875 lt 0001) (Figures 7(a) and7(b) resp)

4 Discussion

The distribution of Monokalliapseudes schubarti is highlyaggregated with the greatest densities occurring in estuarineareas andmuddy depressions where they commonly becomethe dominant species of the macrofauna [4 14 21ndash23 37]

Several authors have tried to correlate the distributionof this tanaidacean with environmental parameters in par-ticular Bemvenuti [4] Leite [13] and Leite et al [15] Theyobserved great densities of this species in fine sedimentcontaining much organic matter and a low concentration ofcalcium According to them the organic matter contributes


2003 2004

Winter Spring Fall

100

200

50

150

0

250

SummerN

indi

vidu

als0225

m2

minus50

400350300

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(a)

2003 2004

Winter Spring Fall

1000

2000

500

3500

0

3000

Summer

Nin

divi

dual

s0225

m2

minus500

2500

1500

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(b)

2003 2004

100

200

50

250

0


150

Nin

divi

dual

s0225

m2

minus50

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(c)

2003 2004

400

1800

0

600800

Winter Spring FallSummerN

indi

vidu

als0225

m2

minus200

1600140012001000

200

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(d)

Figure 5 Monthly variation in the mean density of Monokalliapseudes schubarti per 0225m2 of Saco da Fazenda during the period fromJuly 2003 to June 2004 (a) males (b) females (c) ovigerous females (d) juveniles (mean plusmn standard error)

to the availability of food while the carbonates usuallyassociated with the presence of shells may interfere with theconstruction of tubes by the species

In Saco da Fazenda on the other hand the quantity oforganic matter was found to be inversely correlated withthe abundance of M schubarti Nucci et al [38] discusseda preference of M schubarti for high concentrations oforganic matter but their data obtained for beaches of the SaoSebastiao Channel Sao Paulo indicate higher densities of thisspecies in localities with low values of organic matter

Sediment accumulation may interfere with the popula-tion of M schubarti from Saco da Fazenda According toSchettini [39] Saco da Fazenda represents a sedimentarybasin for sediments transported by the Itajaı-Acu River towhich it is connected by a single opening Leite et al [15]suggest that the density of M schubarti may be influencedby the quantity of silts and clays in the environment being

positive when the quantity is low or intermediate andbecoming negative when these sediments attain high valuesHigh concentrations of organic matter may interfere with thedevelopment of the species due to the reduction of oxygenresulting in low densities in these localities

Regarding temperature and salinity Leite [13] verifiedthat salinity does not interfere with the distribution of thespecies becauseM schubarti is commonly found in estuarineareas Brendolan and Soares-Gomes [40] found experimen-tally that M schubarti is very sensitive when exposed totemperatures above 25∘C which also correlates with thespecies being restricted to subtropical latitudes

In the ecosystem of Saco da Fazenda the highest densitiesoccurred in spring and summer Barreiros et al [41] observedthat in these seasons the abundance of the ichthyofaunawas lowest It thus seems possible that these correlations arefunctional According to Freitas-Junior [42] M schubarti is


35

30

15

25

20

5

10

0

()

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(a)

()

35

30

15

25

20

5

10

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(b)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(c)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(d)

Figure 6 Distribution of frequency by class of length ofMonokalliapseudes schubarti in Saco da Fazenda during the period from July 2003to June 2004 (a) males (b) femaleslowast (c) ovigerous femaleslowast (d) juveniles (119899 = 220 lowasttraces line = size of first mature stage according toFonseca and DrsquoIncao [16])

010

90

50

7080

60

40

2030

100

Neg

gs

10 1412 1311Length (mm)

6 987

(a)

10 1412 13110

10

60

30

50

40

20Nm

anca

e

6 987Length (mm)

(b)Figure 7 Relationship between the total size of ovigerous females of Monokalliapseudes schubarti and the number of (a) eggs (b) mancae(119873 = number)

the main food item of the bony fishes Centropomus parallelusandMicropogonias furnieri the dominant fish species in thisestuary FurthermoreM schubarti becomes a common fooditem not only to fish but also to crustaceans and birds [3 413 20 41 43 44]

The number of females (119899 = 12133) captured in thepresent study was larger than the number ofmales (119899 = 1419)over the whole sampled period resulting in the proportion9 1 Leite et al [15] found a proportion of 269 1 This pre-dominance of females may be attributed to the reproductive

behavior of the species Because fertilization occurs inside thetube of the female males must leave their tubes in search offemales becomingmore susceptible to predation desiccationand dispersal by currents resulting in a greater differentialmortality [15]

Bemvenuti [45] stresses thatM schubarti from the estuar-ine region of Lagoa dos Patos Rio Grande do Sul reproducesthe whole year round with peaks of reproductive activity inthe most favorable periods of food and temperature In Sacoda Fazenda this species presented females in reproductive


Table 1 Fecundity ofMonokalliapseudes schubarti using 80 females per developmental stage

Embryonic stage 119899 Length (mm)lt gt Mean plusmn SE lt gt Mean plusmn SE

Egg I 20 93 37 plusmn 181 030 056 045 plusmn 000Egg II 26 60 36 plusmn 132 049 082 060 plusmn 000Manca I 15 57 30 plusmn 194 070 136 107 plusmn 001Manca II 13 51 24 plusmn 179 123 212 163 plusmn 002119899 number lt minimum gt maximum SE standard error

activity during the whole sampled time span reinforcingthe hypothesis of continuous reproduction However weobserved a seasonal pattern of reproduction and recruitmentwith larger intensities in spring and summer and reducedfrequencies in fall and winter corroborating the results ofLana et al [14] Bemvenuti [5] Leite [13] Leite et al [15]Fonseca and DrsquoIncao [16] and Colling et al [46]

The length of the female ofM schubarti at sexualmaturityin Saco da Fazenda (119871

50= 82mm) was higher than that in

Lagoa de Itaipu (11987150= 59mm) [17] and the Araca region (119871

50

= 502mm) [15]Maranhao et al [47] andNicolau andOshiro[48] observed that environmental factors and differencesin the latitudinal gradient may interfere in the growth andmetabolism of individuals altering the body length at sexualmaturity Thus females at Saco da Fazenda may be under theinfluence of latitude

For Fonseca and DrsquoIncao [16] the size of the firstmature stage of the species in Lagoa dos Patos is attainedapproximately two months after leaving the marsupium (119871

50

= 66mm) indicating the high investment that precedes theprocess of reproduction According to these authors the highinvestment in somatic growth maximizes the reproductivepotential of females permitting that a larger number ofmancae stages may be brooded in the marsupium In Sacoda Fazenda we found a significant correlation between size offemales and number of eggs andmancaeThis differs from theresults in Leite et al [15] who attributed the weak correlationobtained in their study to the loss of eggs while processingspecies during collecting For Fonseca and DrsquoIncao [16] thenonsignificant correlation between female size and numberof eggs and mancae is a consequence of the nonsynchronicdevelopment of the progeny They found eggs embryos andmancae together in the same marsupium

The mean number of eggs and mancae observed in ourstudy (Table 1) was higher than that found by Leite et al [15](mean values of 118 eggs and 78 mancae)

In general M schubarti presented high values of fecun-dity with continuous reproductive activity during the wholestudied period Their greatest population densities wereobserved in the areas that border the ecosystem wherethey are intensely consumed by mixed bands of marineand freshwater birds [19] Furthermore they constitute animportant food item in the diet of swimming crabs of genusCallinectes [49] and of gobiid fish [50]Wemay consider thema fundamental link in the food chain of Saco da Fazendatransferring energy from the detritus level to the highertrophic levels

The predominance of M schubarti along the intertidalregion of the estuary may indicate preference for shallowtidal flats or difficulty in colonizing themore highly disturbedriver channels of the estuary On the other hand the deepersubtidal region where the smallest population densities ofM schubarti were found also accumulated the highest per-centages of organic matter according to our results If habitatdisturbance and high organic matter are factors controllingthe population distribution of M schubarti we would havetwo additional factors favoring the use of this species tomonitor anthropic effects in estuarine areas

Acknowledgments

The authors thank Carolina Nunes Liberal and VirgıniaFarias P de Araujo for help with the statistical treatmentof data Martin Lindsey Christoffersen and Joaquim OlintoBranco wish to thank Conselho Nacional de Desenvolvi-mento Cientıfico e TecnologicoCNPq for the productivitygrants received during the writing of this paper

References

[1] F Mane-Garzon ldquoUn nuevo Tanaidaceo ciego de sud AmericaKalliapseudes schubartii nov sprdquo Comunicaciones Zoologicasdel Museo de Historia Natural de Montevideo vol 52 pp 1ndash61949

[2] K Lang ldquoTanaidacea aus BrasilienrdquoKielerMeeresforschung vol12 no 2 pp 249ndash260 1956

[3] J S Rosa-Filho and C E Bemvenuti ldquoO sedimento comofator limitante para a distribuicao de Kalliapseudes schubartiiMane-Garzon 1949 (Crustacea Tanaidacea) em fundos molesestuarinosrdquo Nauplius vol 6 pp 119ndash127 1998

[4] C E Bemvenuti ldquoPredation effects on a benthic community inestuarine soft sedimentsrdquo Atlantica vol 9 no 1 pp 5ndash32 1987

[5] C E Bemvenuti Interacoes Biologicas daMacrofauna Bentonicanuma enseada Estuarina da Lagoa dos Patos RS Brasil Tese deDoutorado Universidade de Sao Paulo Sao Paulo Brazil 1992

[6] M Gutu New Apseudomorph Taxa of the World Ocean Crus-tacea Tanaidacea Curtea Veche Romania 2006

[7] D T Drumm Systematic revision of the Kalliapseudidae (Crus-tacea Peracarida Tanaidacea) and the population genetic struc-ture and phylogeography of a species along the southeasternand Gulf coasts of North America [MS thesis] University ofSouthern Mississipi Ocean Springs Mississippi 2010

[8] D T Drumm ldquoPhylogenetic relationships of Tanaidacea(Eumalacostraca Peracarida) inferred from three molecularLocirdquo Journal of Crustacean Biology vol 30 no 4 pp 692ndash6982010


[9] D T Drumm ldquoComparison of feeding mechanisms respira-tion and cleaning behavior in two kalliapseudidsKalliapseudesmacsweenyi and Psammokalliapseudes granulosus (PeracaridaTanaidacea)rdquo Journal of Crustacean Biology vol 25 no 2 pp203ndash211 2005

[10] D B Fonseca and F DrsquoIncao ldquoMortality of Kalliapseudesschubartii in unvegetated soft bottoms of the estuarine regionof the Lagoa dos Patosrdquo Brazilian Archives of Biology andTechnology vol 49 no 2 pp 257ndash261 2006

[11] F P P Leite and P E P Leite ldquoDesenvolvimento morfologicoe dos ovarios de Kalliapseudes schubarti Mane-Garzon (Crus-tacea Tanaidacea) do canal de Sao Sebastiao Sao Paulo BrasilrdquoRevista Brasileira de Zoologia vol 14 no 3 pp 675ndash683 1997

[12] M Bacescu ldquoKalliapseudes gianucai a newTanaidacea from theBrazilian watersrdquo Revue Roumaine de Biologie vol 24 no 1 pp3ndash8 1979

[13] F P P Leite ldquoDistribuicao temporal e espacial de Kalli-apseudes schubartiMane-Garzon 1949 (Crustacea Tanaidacea)na regiao do Araca Sao Sebastiao (SP)rdquo Arquivos de Biologia eTecnologia vol 38 no 2 pp 605ndash618 1995

[14] P C Lana M V O Almeida C A F Freitas et al ldquoEstruturaespacial de associacoes macrobenticas sublitorais da gamboaPereque (Pontal do Sul Parana)rdquo Nerıtica vol 4 no 12 pp119ndash136 1989

[15] F P P Leite A Turra and E C Souza ldquoPopulation biologyand distribution of the tanaid Kalliapseudes schubarti Mane-Garzon 1949 in an intertidal flat in southeastern BrazilrdquoBrazilian Journal of Biology vol 63 no 3 pp 469ndash479 2003

[16] D B Fonseca and F DrsquoIncao ldquoGrowth and reproductiveparameters of Kalliapseudes schubartii in the estuarine regionof the Lagoa dos Patos (southern Brazil)rdquo Journal of the MarineBiological Association of the United Kingdom vol 83 no 5 pp931ndash935 2003

[17] S Pennafirme and A Soares-Gomes ldquoPopulation biology andreproduction of Kalliapseudes schubartii Mane-Garzon 1949(Peracarida Tanaidacea) in a tropical coastal lagoon Itaipusoutheastern Brazilrdquo Crustaceana vol 82 no 12 pp 1509ndash15262009

[18] S Pennafirme andA Soares-Gomes ldquoO estudo da biologia pop-ulacional de Kalliapseudes schubartii (Tanaidacea Crustacea)como subsıdio para testes ecotoxicologios de sedimentos mar-inhosrdquo in 3o Congresso Brasileiro de Pesquisa e Desenvolvimentoem Petroleo e Gas pp 1ndash4 Salvador 2005

[19] W L S Ferreira C E Bemvenuti and L C Rosa ldquoEffects of theshorebirds predation on the estuarine macrofauna of the PatosLagoon south BrazilrdquoThalassas vol 21 no 2 pp 77ndash82 2005

[20] W Montagnolli A Zamboni R Luvizotto-Santos and J SYunes ldquoAcute Effects of Microcystis aeruginosa from the PatosLagoon Estuary Southern Brazil on the MicrocrustaceanKalliapseudes schubartii (Crustacea Tanaidacea)rdquo Archives ofEnvironmental Contamination and Toxicology vol 46 no 4 pp463ndash469 2004

[21] C E Bemvenuti R R Capitoli and N M Gianuca ldquoEstu-dos de ecologia bentonica na regiao estuarial da Lagoa dosPatos II-Distribuicao quantitativa domacrobentos infralitoralrdquoAtlantica vol 3 pp 23ndash32 1978

[22] C E Bemvenuti S Cattaneo and S A Netto ldquoCaracterısticasestruturais da macrofauna bentonica em dois pontos da regiaoestuarial da Lagoa dos Patos RS Brasilrdquo Atlantica vol 14 pp5ndash28 1992

[23] R R Capitoli C E Bemvenuti andNM Gianuca ldquoEstudos deecologia bentonica na regiao estuarial da Lagoa dos Patos I-Ascomunidades bentonicasrdquoAtlantica vol 3 no 1 pp 5ndash22 1978

[24] L C Rosa and C E Bemvenuti ldquoTemporal variability of theestuarine macrofauna of the Patos Lagoon Brazilrdquo Revista deBiologia Marina y Oceanografia vol 41 no 1 pp 1ndash9 2006

[25] E C G Couto M V O Almeida and P C Lana ldquoDiversidadee distribuicao da macrofauna bentica do Saco do Limoeiro-Ilha do Mel Paranamdashoutono de 1990rdquo Publicacao Especial doInstituto Oceanografico vol 11 pp 239ndash247 1995

[26] P C Lana and C Guiss ldquoInfluence of Spartina alterniflora onstructure and temporal variability of macrobenthic associationsin a tidal flat of Paranagua Bay (southeastern Brazil)rdquo MarineEcology Progress Series vol 73 no 2-3 pp 231ndash244 1991

[27] A C Z Amaral A E Migotto A Turra and Y Schaeffer-Novelli ldquoAraca biodiversity impacts and threatsrdquo BiotaNeotropica vol 10 no 1 pp 219ndash264 2010

[28] L G Angonesi Dinamica de Curto Prazo da MacrofaunaBentonica emumaEnseadaEstuarina da Lagoa dos Patos EfeitosAntropicos e mecanismos de persistencia e resiliencia Tese deDoutorado FundacaoUniversidade Federal doRioGrande RioGrande RS Brasil 2005

[29] R A Brendolan Utilizacao do Crustaceo Tanaidaceo Kalli-apseudes schubarti Mane-Garzon 1949 em Testes de Ecotoxi-cologia Dissertacao de Mestrado Universidade Federal Flumi-nense Rio de Janeiro RJ Brasil 2004

[30] J O Branco and F Freitas Junior ldquoAnalise quali-quantitativados crustaceos no ecossistema Saco da Fazenda Itajaı SCrdquoin Estuario do Rio Itajaı-Acu Santa Catarina CaracterizacaoAmbiental e alteracoes Antropicas M J Lunardon-Branco andV R Belloto Eds pp 180ndash206 UNIVALI Itajaı SC 2009

[31] C A F Schettini ldquoHidrologia do Saco da Fazenda Itajaı SCrdquoBrazilian Journal of Aquatic Science and Technology vol 12 no1 pp 49ndash58 2008

[32] J G N Abreu J O Branco F L Diehl M T Rosa andD Shumacher Monitoramento Ambiental Plano Executivo deDragagemUtilizacao de Bota-Foras eAtividades compensatoriaspara o Saco da Fazenda (SC) UNIVALI-CTTMar Itajaı SCBrasil 1999

[33] J O Branco ldquoAvifauna associated to the estuary of Saco daFazenda Itajaı Santa Catarina Brazilrdquo Revista Brasileira deZoologia vol 17 no 2 pp 387ndash394 2000

[34] J H Zar Biostatistical Analysis Prentice hall New Jersey NJUSA 1999

[35] W C Krumbein ldquoSize frequency distributions of sedimentsrdquoJournal of Sedimentary Research vol 4 no 2 pp 65ndash77 1934

[36] F P Shepard ldquoNomenclature based on sand-silt-clay ratiosrdquoJournal of Sedimentary Petrology vol 24 no 3 pp 151ndash158 1954

[37] I R Martins J A Villwock L R Martins and C EBemvenuti ldquoThe Lagoa dos Patos estuarine ecosystem (RSBrazil)rdquo Pesquisas vol 22 pp 5ndash44 1989

[38] P R Nucci A Turra and E H Morgado ldquoDiversity anddistribution of crustaceans from 13 sheltered sandy beachesalong Sao Sebastiao channel south-eastern Brazilrdquo Journal ofthe Marine Biological Association of the United Kingdom vol 81no 3 pp 475ndash484 2001

[39] CA F Schettini ldquoCaracterizacao fısica do estuario do rio Itajaı-acu SCrdquo Revista Brasileira de Recursos Hıdricos vol 7 no 1 pp123ndash142 2002

[40] R A Brendolan and A Soares-Gomes ldquoResposta aguda domicrocrustaceo Kallipseudes schubartii Mane-Garzon 1949


(Tanaidacea) ao zinco duodecil sulfato de sodio e petroleobruto em ensaios ecotoxicologicosrdquo Revista Cubana de Inves-tigaciones Pesqueras vol 24 no 1 pp 85ndash90

[41] J P Barreiros J O Branco F Freitas Junior L MachadoM Hostim-Silva and J R Verani ldquoSpace-time distribution ofthe ichthyofauna from Saco da Fazenda Estuary Itajaı SantaCatarina Brazilrdquo Journal of Coastal Research vol 25 no 5 pp1114ndash1121 2009

[42] F Freitas-Junior Ictiofauna do Estuario do Saco da FazendaItajaı SC Trabalho de Conclusao de Curso Universidade doVale do Itajaı Itajaı SC Brasil 2005

[43] R F Contente M F Stefanoni and H L Spach ldquoSize-related changes in diet of the slipper sole Trinectes paulistanus(Actinopterygii Achiridae) juveniles in a subtropical Brazilianestuaryrdquo Pan-American Journal of Aquatic Sciences vol 4 no 1pp 63ndash69 2009

[44] R F Contente M F Stefanoni and H L Spach ldquoFeedingecology of the American freshwater goby Ctenogobius shufeldti(Gobiidae Perciformes) in a sub-tropical estuaryrdquo Journal ofFish Biology vol 80 no 6 pp 2357ndash2373 2012

[45] C E Bemvenuti Efeitos da predacao sobre as caracterısticasEstruturais de uma comunidade Macrozoobentonica numaenseada Estuarina da Lagoa dos Patos RS Brasil Dissertacaode Mestrado Fundacao Universidade Federal de Rio GrandeRio Grande RS Brasil 1983

[46] L A Colling C E Bemvenuti and M S Gandra ldquoSeasonalvariability on the structure of sublittoralmacrozoobenthic asso-ciation in the Patos Lagoon estuary southern Brazilrdquo Iheringiavol 97 no 3 pp 257ndash262 2007

[47] P Maranhao N Bengala M Pardal and J C Marques ldquoTheinfluence of environmental factors on the population dynamicsreproductive biology and productivity of Echinogammarusmarinus Leach (Amphipoda Gammaridae) in the Mondegoestuary (Portugal)rdquo Acta Oecologica vol 22 no 3 pp 139ndash1522001

[48] C F Nicolau and L M Y Oshiro ldquoAspectos reprodutivosdo caranguejo Aratus pisonii (H Milne Edwards) (CrustaceaDecapoda Grapsidae) do manguezal de Itacuruca Rio deJaneiro Brasilrdquo Revista Brasileira de Zoologia Curitiba vol 192 pp 167ndash173 2002

[49] S C Kapusta and C E Bemvenuti ldquoAtividade nictemeral dealimentacao de juvenis de Callinectes sapidus Rathbun 1895(Decapoda Portunidae) numa pradaria de Ruppia maritima Le num plano nao vegetado numa enseada estuarina da Lagoados Patos RS Brasilrdquo Nauplius vol 6 pp 41ndash52 1998

[50] R F Contente Particao Inter-Especıfica e Efeitos SazonaisEspaciais e ontogeneticos no Uso de recursos Troficos por seisTeleostei em um sistema Estuarino Sub-Tropical Dissertacao deMestrado Universidade Federal do Parana Curitiba PR Brasil2008

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


Atalaia BeachSaco daFazenda

Navegantes

Itajaiacute

ItajaiacuteIIIIV

I

II0 150 300 450

N

(km) acute

-Accedilu

Figure 1 Studied area indicating the collecting sites in Saco da Fazenda Santa Catarina Brazil (source modified of chart 1801 fromDiretoriade Hidrografia e NavegacaoDHN)

Araca beach Sao Paulo [13] Such abundant opportunisticcommunity structuring persistent and resilient species havebeen found to be excellent biotic indicators and have beenincreasingly used as such [18 20 27ndash29]

In south and southeastern Brazil M schubarti has beenstudied in tidal flats [26] fine-grained beaches of low slopeand high organic matter [13 15] estuaries [16] and coastallagoons [17]

In the state of Santa Catarina about halfway along its totalgeographic range M schubarti was found to be very abun-dant in the estuarine area of Saco da Fazenda [30]This paperreports the spatiotemporal distribution population structureand reproduction ofM schubarti in this environment

2 Material and Methods

21 Study Area Saco da Fazenda is located in the estuaryof the Itajaı-Acu River between 26∘5310158403310158401015840ndash26∘5510158400610158401015840 S and48∘3810158403010158401015840ndash48∘3910158401410158401015840W state of Santa Catarina Brazil It ischaracterized as a shallow artificial estuary [31] because of theconstruction of piers to rectify and stabilize the canal of theItajaı-Acu River These piers have isolated a previous affluentof this river [32] and water exchange became restricted Thetotal surface area of Saco da Fazenda is about 63 times 105m2[31] The substrate is siliceous argillic and maximum depthis 20m except in the river canals which attain 90m depthTidal variations are not higher than 14m Mean annualrainfalls range from 1250 to 1500mm [33]

The ecosystem of Saco da Fazenda despite its exposureto a strong anthropic impact and to an intensive dischargeof domestic wastewater solid residues [33] and drainageactivities [32] supports a high diversity of animals and serves

as a natural nursery for several species of crustaceans fishand birds which may useM schubarti as a source of food

22 Methods Specimens were collected monthly in theintertidal and subtidal regions of Saco da Fazenda in fourareas (Figure 1) between July 2003 and June 2004 In eacharea six samplings with a Van Veen grab (0075m2) wereconducted during high spring tides Three samples wereobtained in the intertidal region (40 cm depth) and threein the subtidal (140 cm depth) For the analyses the threesamples from each region were considered as a single sample(0225m2 per region)

The tanaidaceans were separated from the sediment witha 05mmmesh-size sieve fixed in 4 formalin and preservedin labelled bottles In the lab the residual sediment wasremoved and the total number of specimens per sample wasdetermined

To estimate the density of males females and juvenilesalong the year as well as the number of females in repro-ductive activity a subsample was established from the totalnumber of collected individuals To obtain this capturedanimals were put in a beaker of 250mL with water Thematerial was homogenized and three samples of 20mL wereextractedWe used themean value of individuals for the threesamples and calculated the total number of individuals persample for that collecting month

To characterize the structure of the population weobtained two new samples from the field during the summerand winter of 2005 Due to the low abundance of organ-isms captured in these samples the samples were pooledand 220 entire individuals were chosen for the classes ofmales females ovigerous females and juveniles which were


2003 2004


2025

1510

50

2018

1012

6420

8

1416

Salin

ity (

)

Tem

pera

ture

of w

ater

(∘C)


Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r








3 Results







119904 salinity = minus009 119899 = 48119875 = 05)




150

135

175

170

165

160

145

140

155


Calc

ium

carb

onat

e con

tent

()



2003 2004

12

13

14

15

16

17

18

19


Nin

divi

dual

s0225

m2

Janu

ary

Febr

uary

Mar

ch

April

May

June

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

July















4 Discussion




2003 2004

Winter Spring Fall

100

200

50

150

0

250

SummerN

indi

vidu

als0225

m2

minus50

400350300

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(a)

2003 2004

Winter Spring Fall

1000

2000

500

3500

0

3000

Summer

Nin

divi

dual

s0225

m2

minus500

2500

1500

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(b)

2003 2004

100

200

50

250

0


150

Nin

divi

dual

s0225

m2

minus50

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(c)

2003 2004

400

1800

0

600800


indi

vidu

als0225

m2

minus200

1600140012001000

200

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(d)









35

30

15

25

20

5

10

0

()

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(a)

()

35

30

15

25

20

5

10

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(b)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(c)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(d)


010

90

50

7080

60

40

2030

100

Neg

gs

10 1412 1311Length (mm)

6 987

(a)

10 1412 13110

10

60

30

50

40

20Nm

anca

e

6 987Length (mm)














50



50





Acknowledgments


References





























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


2003 2004


2025

1510

50

2018

1012

6420

8

1416

Salin

ity (

)

Tem

pera

ture

of w

ater

(∘C)


Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r








3 Results







119904 salinity = minus009 119899 = 48119875 = 05)




150

135

175

170

165

160

145

140

155


Calc

ium

carb

onat

e con

tent

()



2003 2004

12

13

14

15

16

17

18

19


Nin

divi

dual

s0225

m2

Janu

ary

Febr

uary

Mar

ch

April

May

June

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

July















4 Discussion




2003 2004

Winter Spring Fall

100

200

50

150

0

250

SummerN

indi

vidu

als0225

m2

minus50

400350300

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(a)

2003 2004

Winter Spring Fall

1000

2000

500

3500

0

3000

Summer

Nin

divi

dual

s0225

m2

minus500

2500

1500

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(b)

2003 2004

100

200

50

250

0


150

Nin

divi

dual

s0225

m2

minus50

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(c)

2003 2004

400

1800

0

600800


indi

vidu

als0225

m2

minus200

1600140012001000

200

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(d)









35

30

15

25

20

5

10

0

()

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(a)

()

35

30

15

25

20

5

10

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(b)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(c)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(d)


010

90

50

7080

60

40

2030

100

Neg

gs

10 1412 1311Length (mm)

6 987

(a)

10 1412 13110

10

60

30

50

40

20Nm

anca

e

6 987Length (mm)














50



50





Acknowledgments


References





























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


150

135

175

170

165

160

145

140

155


Calc

ium

carb

onat

e con

tent

()



2003 2004

12

13

14

15

16

17

18

19


Nin

divi

dual

s0225

m2

Janu

ary

Febr

uary

Mar

ch

April

May

June

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

July















4 Discussion




2003 2004

Winter Spring Fall

100

200

50

150

0

250

SummerN

indi

vidu

als0225

m2

minus50

400350300

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(a)

2003 2004

Winter Spring Fall

1000

2000

500

3500

0

3000

Summer

Nin

divi

dual

s0225

m2

minus500

2500

1500

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(b)

2003 2004

100

200

50

250

0


150

Nin

divi

dual

s0225

m2

minus50

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(c)

2003 2004

400

1800

0

600800


indi

vidu

als0225

m2

minus200

1600140012001000

200

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(d)









35

30

15

25

20

5

10

0

()

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(a)

()

35

30

15

25

20

5

10

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(b)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(c)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(d)


010

90

50

7080

60

40

2030

100

Neg

gs

10 1412 1311Length (mm)

6 987

(a)

10 1412 13110

10

60

30

50

40

20Nm

anca

e

6 987Length (mm)














50



50





Acknowledgments


References





























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


2003 2004

Winter Spring Fall

100

200

50

150

0

250

SummerN

indi

vidu

als0225

m2

minus50

400350300

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(a)

2003 2004

Winter Spring Fall

1000

2000

500

3500

0

3000

Summer

Nin

divi

dual

s0225

m2

minus500

2500

1500

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(b)

2003 2004

100

200

50

250

0


150

Nin

divi

dual

s0225

m2

minus50

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(c)

2003 2004

400

1800

0

600800


indi

vidu

als0225

m2

minus200

1600140012001000

200

Janu

ary

Febr

uary

Mar

ch

April

May

JuneJuly

Augu

st

Sept

embe

r

Oct

ober

Nov

embe

r

Dec

embe

r

(d)









35

30

15

25

20

5

10

0

()

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(a)

()

35

30

15

25

20

5

10

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(b)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(c)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(d)


010

90

50

7080

60

40

2030

100

Neg

gs

10 1412 1311Length (mm)

6 987

(a)

10 1412 13110

10

60

30

50

40

20Nm

anca

e

6 987Length (mm)














50



50





Acknowledgments


References





























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


35

30

15

25

20

5

10

0

()

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(a)

()

35

30

15

25

20

5

10

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(b)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(c)

()

3530

15

2520

510

0

25

20

30

35

40

45

50

55

60

65

70

75

80

85

90

95

100

105

110

115

120

125

130

135

140

Length (mm)

(d)


010

90

50

7080

60

40

2030

100

Neg

gs

10 1412 1311Length (mm)

6 987

(a)

10 1412 13110

10

60

30

50

40

20Nm

anca

e

6 987Length (mm)














50



50





Acknowledgments


References





























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology









50



50





Acknowledgments


References





























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology





















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Spatiotemporal Distribution and Population Structure of Monokalliapseudes schubarti (Tanaidacea:...

Documents

Transcript of Spatiotemporal Distribution and Population Structure of Monokalliapseudes schubarti (Tanaidacea:...