research article sexual shape dimorphism of the mangrove...

Research ArticleSexual Shape Dimorphism of the MangroveCrab Ucides cordatus (Linnaeus 1763) (Decapoda Ucididae)Accessed through Geometric Morphometric

C E R D Alencar1 P A Lima-Filho2 W F Molina3 and F A M Freire1

1 Grupo de Estudos em Ecologia e Fisiologia de Animais Aquaticos (GEEFAA) Departamento de BiologiaEcologia e Zoologia Centro de Biociencias Universidade Federal do Rio Grande do Norte Campus Universitario Lagoa NovaCaixa Postal 1524 59078-970 Natal RN Brazil

2 Federal Institute of Science and Technology of Rio Grande do Norte 59500-000 Macau RN Brazil3 Centro de Biociencias Departamento de Biologia Celular e Genetica Universidade Federal do Rio Grande do Norte59078-970 Natal RN Brazil

Correspondence should be addressed to C E R D Alencar carlosce2002gmailcom

Received 11 April 2014 Revised 16 July 2014 Accepted 16 July 2014 Published 14 October 2014

Academic Editor M Antonio Todaro

Copyright copy 2014 C E R D Alencar 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

Sexual dimorphism is often observed in Crustaceans Considering the great diversity of this subphylum only few reports are foundin the literature and most are mainly based on traditional morphometryThe present study uses geometric morphometrics analysisto identify sexual dimorphism by shape variation in the overexploited semiterrestrial crabUcides cordatus species with great socialand economic importance in South America Comparative morphology analyses were performed by using the outer face of thepropodus of major cheliped dorsal and anterior region of carapace shape Significant differences in shape between sexes weredetected in these body areas The causes of dimorphism presented in this species are not clear but analogous to other possiblyassociated species it may be inferred that the causes are with adaptations to body ability of reproductive potential (females) andof reproductive behaviour and agonistics encounters (males) Additional analyses on courtship displays and other reproductiveaspects should provide better comprehension of functionality of this morphological differentiation

1 Introduction

Crustaceans comprise a profitable model for morphometricstudies due to the presence of a rigid exoskeleton that allowsaccurate biometric measurements [1 2] The applicationsof geometric morphometric in crustaceans are numeroussuch as using the body shape for taxonomic identificationsfishery stocks maturity instars ontogenetic stages or sexualdimorphism [3ndash14]

Body shape changes in crabs either in male or femalespecimens can have important ecological consequences andevolutionary trends [15] given that in adults crabs forinstance physiological processes of growth and reproductionhave different targeting energy expenditure for each genderdue to the different reproductive activities performed [16]

Hartnoll [16] states that adaptively female crabs can showfeeding restriction and less number of moults than malesduring reproductive process reduced feeding chances areassociated with cryptic habits to avoid predation and protectthe egg mass while less number of moults are related toavoiding the loss of the eggs during the incubation periodor on the other hand while making the moult the egg masswould be releasedwith the cast integument andwould die dueto the absence of parental care

Ucides cordatus (Linnaeus 1763) [17] a semiterrestrialcrab has great economic importance in Northeast Brazilwhere it is considered an overfished species [18] It inhabitsmangroves of the Atlantic coastndashfrom Florida USA to SantaCatarina Brazil [19]ndashand it is an efficient bioindicator ofenvironmental pollution [20ndash24] Curiously although this

Hindawi Publishing Corporatione Scientific World JournalVolume 2014 Article ID 206168 8 pageshttpdxdoiorg1011552014206168

2 The Scientific World Journal

123

4

5

6

7

8

9

10

(a)

12

3

45

67

8

9

10

(b)

12

3

4

5

6

7

8

9

10

(c)

Figure 1 Ucides cordatus (Linnaeus 1763) localization of landmarks in each anatomic area (a) Dorsal area of carapacemdashC (b) outer face ofmajor chelipedmdashMC and (c) anterior region of cephalothoraxmdashAR

species is being exploited during several hundreds of yearsmany aspects of its biology are scarcely known

Previous investigations using traditional morphometricmethods were performed on populations of U cordatus atSouth Atlantic coast [25ndash32] evaluating ontogenetic changesbetween juveniles and adults of each sex (seeHartnoll [33] fordetails) or by simply testing statistically difference on severalbody measurements between sexes

However despite the fact that analyses using geomet-ric morphometric techniques on U cordatus are relativelyunknown they have been used on several crabs generaon sexual dimorphism and evolutionary studies such asLiocarcinus (Linnaeus 1758) [34] some species ofUca (Leach1814) [35] and the shrimp Litopenaeus (Boone 1931) [4 1014 15 36] Thus the aim of this study is to investigatethe sexual shape dimorphism in three body areas (anteriorand dorsal region of carapace and major cheliped) on aU cordatus population from Northeast Brazil based ongeometric morphometric analyses

2 Material and Methods

Hundred and twenty specimens ofUcides cordatus 60 of eachgender were used for morphometric analysis Specimenswere obtained in the estuary of Potengi River (05∘481015840 S35∘151015840W) state of Rio Grande do Norte Northeast of Brazilthrough active collecting by only one researcher Immediatelyafter collecting the animals were placed inside a freezer atminus20∘C for cryoanesthesia Identification of specimens wasbased on Melo [19] and sex classification on the observa-tion of abdominal shape (narrow for males and wide forfemales) and pleopods number (two pairs in males and fourin females) In this study only specimens with completeappendages without any damage or punctual abnormalitieswere used In order to avoid ontogenetic allometry effects[37] only crabs from the same adult cohort (larger sizes fromthe sexual morphologic maturity sizemdashdata not shown) wereused Sizes of sexual morphology maturity were defined bythe literature review of previous investigations done in thesame geographic region [27]

Digitalized images were obtained by a Sony H10 digitalcamera (81 megapixels) using standardized position anddistance The body areas and structures analysed were the

anterior region of cephalothorax (AR) carapace dorsal area(C) and the outer face of major cheliped (MC) Major rightcheliped was always used when possible Image digitalizationof chelipeds was facilitated by removing them from the bodyThis process was carried out cutting them between propodusand carpus [38]

The software tpsUtil was used to ordinate the digitalizedimages in the same file under the TPS format In additionthe tpsDig2 software [39] was used to record ten landmark ineach structure (Figure 1 Table 1) Description of landmarksfor AR and C followed anatomical criterion defined byCrane [40] and Williams [41] Descriptions of landmarks forthe MC were based on Rosenberg [3] and Rosenberg [4]with some modifications Ucides cordatus shows a more ovaland smooth carapace without any ornamentation whichmakes landmarks establishment difficult differently fromother brachyurans [6 15]Thus the choice of such landmarkswas made using intersections of transverse commissures thatare strongly marked in this species

Landmarks coordinates were submitted to a GeneralizedProcrustes analysis (GPA) [42] in MorphoJ 102b [43] Gen-eralized Procrustes analysis is a procedure that fixes non-shape related variation due to the specimensrsquo position sizeand rotation [44]

In order to avoid static and ontogenetic allometry effectsan allometric correction was necessary to compare the bodyshapes of each gender according to the procedure proposedby Sidlauskas et al [45] Thereunto a pooled within-groupallometric regression using centroid size (Size) was per-formed on Procrustes coordinates (Shape) The statisticalsignificance of the allometric regressions was tested withpermutation tests against the null hypothesis of allometryindependence [46] Percentage of predicted allometry in eachbody area was also calculated as a percentage of total shapevariation that the regression model calculated computedfrom the Procrustes metric [47 48] From this residuals ofthe allometric regression were used for statistical analysis andinvestigation of shape variation [45] for each body part Thedefinition of static allometry used in this work followed Cock[37] that is referred to size allometry as a result of the varia-tion of individuals in the same population and age group Inall body area cases even with static allometry independence(119875 gt 005) the residuals of the regression were used to obtainfurther results of shape variation corrected for allometry

The Scientific World Journal 3

Table 1Ucides cordatus (Linaeus 1763) list of landmarks descriptions used in sexual dimorphism characterization Dorsal area of carapacemdashC Anterior region of cephalotoraxmdashAR and Outer face of major chelipedmdashMC

Landmarks DescriptionC

1 Middle point of frontal carapace outer margin2 Anterolateral margin carapace deviation3 Intersection of the anterolateral and supraorbital margin4 Intersection point of anterolateral and posterolateral carapace margin5 Middle point of posterior carapace margin6 Middle point of transversal commissure7 Deviation of anterolateral proportion of transversal commissure8 Intersection of lateral commissure between hepatic and gastric regions9 Intersection of lateral commissure between gastric and cardiac regions10 Posterolateral margin deviation with transversal commissure in intestinal area

AR1 Middle point of frontal carapace outer margin2 Antennula proximal point3 Antenna proximal point4 Lateral point of the epistomic margin of carapace5 Intersection of the lateral margin and supraorbital areas of carapace6 Distal point of suborbital carapace margin7 Intersection of supraorbital margin supraorbital carena and frontal ramification margin of the transversal commissure8 Intersection between the suborbital subhepatic and pterigostomic regions9 Superior middle point of the epistomial margin of carapace10 Inferior middle point of the epistomial margin of carapace

MC1 Distal point of the superior manus margin2 Intersection of the dactyly on superior margin3 Intersection between the inferior margin of the dactyly and the gap between the pollex and the dactyl4 Proximal point of the pollex5 Distal point of the pollex6 Inferior margin of chelae in rectilinear distance to the distal point of the superior margin7 Deviation of the inferior margin of the manus8 Inferior articulation point between the propodus and the carpus9 Superior articulation point between the propodus and the carpus10 Proximal deviation of the superior margin of the manus

effect (ontogenetic or static) Subsequent multivariate analy-sis of variance (MANOVA) was used in order to test shapedifference between sexes in each body part separately Adiscriminant function analysis (DFA) was used to verifywhich shape variations could reliably distinguish a genderfrom the other Finally Procrustes distance was inspectedto verify which body part showed greater strength in thedissimilarity between genders

Procedures for allometric correction and multivariateanalysis were performed in MorphoJ 102b [43] Moreoverstarting from comparative transformation grids (grids notshown) obtained from discriminant function drawing out-lines were incorporated to clearly indicate vector variationsof mean shape between each gender in each body areaOutline drawing is an alternative form of presentation of the

structure under study that makes it easy to interpret shapechanges However all information provided in this form ofrepresentation comes from landmarks Outline drawing wasgenerated by tpsDig2 [39] and exported to MorphoJ 102b[43]

3 Results

Landmarks displacements on the body areas (AR C andMC) revealed significant differences between sexes Staticallometry independence (119875 gt 005) was detected in AR(119875 = 014 predicted = 127) and C (119875 = 009 predicted =172) and allometry dependence was detected in MC (119875 lt001 predicted = 536) However as previously men-tioned for further comparison analysis only residuals of the


allometric regression were used Furthermore discriminantfunction analysis ascertains statistical differences in all threebody areas revealing major similarity between sexes for AR(Procrustes distance = 00145 119875 lt 001) and minor for MC(Procrustes distance = 00455 119875 lt 001) (Table 2) Correctassignments of the cross validation matrix were obtained forMC (9833 for correct assignment for each sex) C (8666for males and 8333 for females) and AR (7166 for malesand 7500 for females)

Females revealed a less convex profile in C plus a slightreduction of lateral points and in the anterior region ofcephalothorax On the other hand points of anterior marginrevealed a slight vector displacement on the opposite side Formales the posterolateral region of C was more rounded thanfemales Furthermore points above transversal commissuresshowed great vector displacement evidencing a slightly verti-cal elongation in females with amajor functionalmesogastricand gonad area Although males reveal variation in shapeevidencing major functional branchial gut and cardiac areas(Figure 2(a)) males presented reduction of the points relatedto hiatus distance of MC (landmarks 3 and 4) and a sturdycheliped manus evidenced by vector displacement of thelandmarks in the posterior and inferior margin of the MCMoreover the same pattern was observed on the landmarksof the intersection on the base of the dactylus and thearticulation between the propodus and carpus No vectordifference was observed on the fixed dactyl shapes (pollex)(Figure 2(b)) Changes in shape for the margin of orbitalcavity and its supraorbitalmarginweremeaningful Howeverfemales showed slight vector displacement in the connectedlandmarks with basis of ocular peduncle (Figure 2(c))

4 Discussion

The three analysed body areas of U cordatus displayedshape variation related to sexual dimorphism A less convexprofile and reduction for anterolateral points found for Cin females are probably related to the increase of bodyability and reproductive potential [49] This seems to be apattern for most brachyurans [6 11 15] During the gonadaldevelopment of U cordatus females this structure increasestheir volume sometimes reaching four times the initial sizeIn this condition upper and lower lobes became evident inthe interior of the cephalothorax occupying a great part ofthemidgut areaMoreover according to the same authors (seeabove) the ovarian lobes are connected by a transverse com-missure According to Santana and Silva [50] the transversecommissure displayed a macroscopic morphology which isvery similar to gonads forming a structure in the shape ofldquoHrdquo that can be visualized on the dorsal region ofU cordatus(indicated by landmarks 6ndash10 Figure 2(a)) In males a largercarapace can mean a larger size or even a more robust basisfor the insertion of muscles of pereiopods and chelipeds[15] essential in agonistic encounters in the competition forterritory or females [15 51ndash53]

Chelipeds of decapods are excellent model for morpho-logic studies due to their unique structure and the varietyof functions [54] For Uca pugnax (Smith 1870) [55] majorchelipeds are related to social behaviour and mating [3] On

Table 2 Ucides cordatus (Linaeus 1763) statistical results forcomparison of shape variation between males and females

Analysis ParametersMANOVAlowast SS df 119865 119875 Pillairsquos traceC 00252 16 704 lt001 061AR 00049 16 361 lt001 043MC 00727 16 2535 lt001 087DFA 119879

2

119879

2

119875 119875

lowastlowast

119863

2 Prc distC 18667 lt001 lt001 249 00304AR 8668 lt001 lt001 171 00145MC 26342 lt001 lt001 504 00455MANOVA multivariate analysis of variance DFA discriminant functionanalysis SS sum square df degrees of freedom 1198792 Hotellingrsquos 119905 test119863

2 Mahalanobis distance Prc dist Procrustes distance dorsal area ofcarapace C outer face of the major cheliped MC and anterior region ofcephalothorax ARlowastRepresented only shape resultslowastlowastSignificance value to permutation tests under Procrustes distance amonggroups

the other hand minor chelipeds are adaptively associatedwith feeding function As verified forMunida rugosa (Fabri-cius 1775) (Galatheidae) [56] chelipeds with higher volumeconsequently major finger closing muscle show markedmechanic advantage [8] Same conditions are observed formales of U cordatus considering territorialistic behaviour ofthis species [49] In some U cordatus males some punctualdamage or abnormalities beyond several traceswere observedconfirming the utilization of chelipeds for attack and defencePrevious traditional morphometric allometric studies withjuveniles and adults of U cordatus evidenced a higher ratioof growth for the adult malesrsquo chelae than the femalesrsquocorroborating a potential use in reproductive behaviouraldisplay [29]

Based on the aforementioned different uses of che-lipeds and knowing that U cordatus males exhibit agonisticbehaviour with other males it may be assumed that becauseof the shape variation in chelipeds of U cordatus the largerhiatus found in chelipeds of females could demonstrateadaptations of its utilization in feeding while males withsmaller hiatus could probably represent major efficiency ofthe increasing of the prehensile ability that is very importantto grab female during themating and also causemore damagein fights against other males However more studies shouldbe realized to confirm this assumptionMorphological differ-entiations for chelipeds between genders are conspicuouslyevidenced in size frequency distribution of the discriminantfunction and the value of the Procrustes distance This lastone pointed it as the major parameter in the differentiationbetween genders when compared to the other body partsanalysed in the present study

Foraging behaviour reproduction and agonisticbehaviour constitute a triad of selective pressures that driveevolutionary responses proper for each sex in Brachyuracrustaceans [54] The role of the complex morphologicstructures which are evolved in the sexual selection processbegins with the shape variation analysis


Frequency

Discriminant

0

2

4

6

10

8

minus6 minus3 0 3 6 9minus9 12minus12

(a)

Frequency

0

2

4

6

8

Discriminantminus20 minus10 0 10 20 30minus30

(b)

Frequency

Discriminant

0

2

4

6

8


(c)

Figure 2 Ucides cordatus (Linnaeus 1763) comparison of body shape from outline drawing obtained frequencies from Discriminantfunction analysis Deviation between male and female correspondent landmarks in each structure represents the vector displacement(deformation grid) (a) Dorsal area of carapacemdashC (b) outer face of major chelipedmdashMC and (c) anterior region of cephalothoraxmdashARgray = female and black = male

Some Brachyurans can show behavioural changes thatcan be associated with certain body parts Crabs of thegenus Uca are a good example for this phenomenon asmales use their hypertrophied cheliped during courtship[40] Moreover several evidences indicate the role of suchappendage as visual stimulus in conspecific partner choice[57 58] Descriptions of mating behavior of U cordatusare still officially unpublished information However infor-mation from dissertations as well as information obtainedduring field observations by these authors indicates that

U cordatus presents courtship and mating behaviour It isbelieved that visual stimulus as coloration and heterochely inmales may be decisive for femalesrsquo acceptation or rejection(personal communication)

5 Conclusions

Mapping differences of body shape reveal different func-tions for the same body structures in male and female


of the mangrove crab Ucides cordatus These differencesare more evident in body parts related with reproductiveaspects In fact secondary sexual morphologic differencesbetween males and females reveal a sexual dimorphismevolving distinct morphologic aspects of these crabs Inthis sense the present results sustain the hypothesis thatmorphologic differences found between genders have animportant role in sexual selection in this species Furtherstudies on behavioural aspects could contribute to a betterunderstanding of adaptive functions related with the bodystructures of this species

Conflict of Interests

The authors declare that they have no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors (Carlos E R D Alencar and Paulo A deLima-Filho) would like to thank the ldquoCoordenacao deAperfeicoamento de Pessoal de nıvel Superiorrdquo (CAPES) forthe provided fellowship They thank the ldquoInstituto Brasileirodo Meio Ambienterdquo (IBAMA) for sampling license (number28314-1) and Maria Lucia Negreiros-Fransozo for her criti-cism and suggestions in the draft of the paper The authorsalso thank A Cardini and other anonymous reviewers for thehelpful comments in this work

References

[1] R G Hartnoll ldquoThe determination of relative growth inCrustaceardquo Crustaceana vol 34 pp 281ndash293 1978

[2] D A Somerton ldquoA computer technique for estimating the sizeof sexual maturity in crabsrdquo Canadian Journal of Fisheries andAquatic Science vol 37 pp 1488ndash1494 1980

[3] M S Rosenberg ldquoEvolution of shape differences betweenthe major and minor chelipeds of Uca pugnax (DecapodaOcypodidae)rdquo Journal of Crustacean Biology vol 17 no 1 pp52ndash59 1997

[4] M S Rosenberg ldquoFiddler crab claw shape variation a geo-metric morphometric analysis across the genusUca (CrustaceaBrachyura Ocypodidae)rdquo Biological Journal of the LinneanSociety vol 75 no 2 pp 147ndash162 2002

[5] A Bertin B David F Cezilly and P Alibert ldquoQuantification ofsexual dimorphism in Asellus aquaticus (Crustacea Isopoda)using outline approachesrdquo Biological Journal of the LinneanSociety vol 77 no 4 pp 523ndash533 2002

[6] MM Rufino P Abello andA B Yule ldquoGeographic and gendershape differences in the carapace of Liocarcinus depurator(Brachyura Portunidae) using geometric morphometrics andthe influence of a digitizing methodrdquo Journal of Zoology vol269 no 4 pp 458ndash465 2006

[7] S Iepure T Namiotko and D L Danielopol ldquoEvolutionaryand taxonomic aspects within the species group Pseudocandonaeremita (Vejdovsky) (Ostracoda Candonidae)rdquo Hydrobiologiavol 585 no 1 pp 159ndash180 2007

[8] T Claverie and I P Smith ldquoFunctional significance of anunusual chela dimorphism in a marine decapod specialization

as a weaponrdquo Proceedings of the Royal Society B BiologicalSciences vol 274 no 1628 pp 3033ndash3038 2007

[9] I C Silva S J Hawkins and J Paula ldquoA comparison of popu-lation differentiation in two shore crab species with contrastingdistribution along the Portuguese coast using two morpholog-ical methodologiesrdquo Marine and Freshwater Research vol 60no 8 pp 833ndash844 2009

[10] M J Hopkins and C L Thurman ldquoThe geographic structureof morphological variation in eight species of fiddler crabs(Ocypodidae genus Uca) from the eastern United States andMexicordquo Biological Journal of the Linnean Society vol 100 no 1pp 248ndash270 2010

[11] F M Ledesma S van der Molen and P J Baron ldquoSex identifi-cation of Carcinus maenas by analysis of carapace geometricalmorphometryrdquo Journal of Sea Research vol 63 no 3-4 pp 213ndash216 2010

[12] I C Silva N Mesquita and J Paula ldquoGenetic and morpholog-ical differentiation of the mangrove crab Perisesarma guttatum(Brachyura Sesarmidae) along an East African latitudinalgradientrdquo Biological Journal of the Linnean Society vol 99 no 1pp 28ndash46 2010

[13] I C Silva M J Alves J Paula and S J Hawkins ldquoPopulationdifferentiation of the shore crab Carcinus maenas (BrachyuraPortunidae) on the southwest English coast based on geneticand morphometric analysesrdquo Scientia Marina vol 74 no 3 pp435ndash444 2010

[14] I V Accioly P A Lima-Filho T L Santos et al ldquoSexualdimorphism in Litopenaeus vannamei (Decapoda) identified bygeometric morphometricsrdquo Pan-American Journal of AquaticSciences vol 8 pp 276ndash281 2013

[15] M Rufino P Abello and A B Yule ldquoMale and femalecarapace shape differences in Liocarcinus depurator (DecapodaBrachyura) an application of geometric morphometric analysisto crustaceansrdquo Italian Journal of Zoology vol 71 no 1 pp 79ndash83 2004

[16] R GHartnoll ldquoReproductive investment in BrachyurardquoHydro-biologia vol 557 no 1 pp 31ndash40 2006

[17] C Linnaeus ldquoCenturia insectorumrdquo Amoenitates Academicaeligvol 6 pp 384ndash415 1763

[18] Brasil ldquoProposta do Plano Nacional de Gestao para o UsoSustentavel do caranguejo-uca do guaiamum e do siri-azulrdquoInstituto Brasileiro do Meio Ambiente e dos Recursos NaturaisRenovaveis (IBAMA) Brasılia Brazil 2011

[19] G A SMeloManual de Identificacao dos Brachyura (carangue-jos e siris) do Litoral Brasileiro Pleidade Sao Paulo Brazil 1996

[20] TM TavaresM Beretta andM C Costa ldquoRatio of DDTDDEin the All Saints Bay Brazil and its use in environmentalmanagementrdquo Chemosphere vol 38 no 6 pp 1445ndash1452 1999

[21] R R Harris and M C F Santos ldquoHeavy metal contaminationand physiological variability in the Brazilian mangrove crabsUcides cordatus and Callinectes danae (Crustacea Decapoda)rdquoMarine Biology vol 137 no 4 pp 691ndash703 2000

[22] M doCarmo Fernandes Santos ldquoDrinking and osmoregulationin the mangrove crab Ucides cordatus following exposure tobenzenerdquo Comparative Biochemistry and Physiology A vol 133no 1 pp 29ndash42 2002

[23] A H Nudi A de Luca Rebello Wagener E Francioni Ade Lemos Scofield C B Sette and A Veiga ldquoValidation ofUcides cordatus as a bioindicator of oil contamination andbioavailability in mangroves by evaluating sediment and crabPAH recordsrdquo Environment International vol 33 no 3 pp 315ndash327 2007


[24] M A A Pinheiro P P G E Silva L F D A Duarte AA Almeida and F P Zanotto ldquoAccumulation of six metalsin the mangrove crab Ucides cordatus (Crustacea Ucididae)and its food source the red mangrove Rhizophora mangle(Angiosperma Rhizophoraceae)rdquo Ecotoxicology and Environ-mental Safety vol 81 pp 114ndash121 2012

[25] E R O Botelho A F Dias and C T C Ivo ldquoEstudo sobrea biologia do caranguejo-uca Ucides cordatus cordatus (Lin-naeus 1763) capturado nos estuarios dos Rios Formoso (RioFormoso) e ilhotas (Tamandare) no estado de PernambucordquoBoletim Tecnico Cientıfico do CEPENE vol 7 no 1 pp 117ndash1451999

[26] C T C Ivo A F Dias and R I Mota ldquoEstudo sobre a biologiado caranguejo-uca Ucides cordatus cordatus (Linnaeus 1763)capturado no Delta do Rio Parnaıba Estado do Piauırdquo BoletimTecnico-cientıfico do CEPENE vol 7 no 1 pp 53ndash84 1999

[27] EM S Vasconcelos J A Vasconcelos andC T C Ivo ldquoEstudosobre a biologia do caranguejo-uca Ucides cordatus (Linnaeus1763) capturado no estuario do rio Curimatau (Canguaretama)no Estado do Rio Grande do Norterdquo Boletim Tecnico Cientıficodo CEPENE vol 7 pp 85ndash116 1999

[28] M M L Leite A A Fonteles-Filho J R F Silva and N SCardoso ldquoAnalise do crescimento alometrico no caranguejo-uca Ucides cordatus (Decapoda Ocypodidae) no estuario dorio Coreau Camocim CearardquoArquivos de Ciencias doMar vol39 pp 93ndash98 2006

[29] M A A Pinheiro and G Y Hattori ldquoRelative growth of themangrove crab Ucides cordatus (Linnaeus 1763) (CrustaceaBrachyura Ocypodidae) at Iguape Sao Paulo Brazilrdquo BrazilianArchives of Biology and Technology vol 49 no 5 pp 813ndash8232006

[30] M S L C Araujo and T C S Calado ldquoBioecologia docaranguejo-UcaUcides cordatus (Linnaeus) no Complexo Estu-arino LagunarMundauManguaba (CELMM) Alagoas BrasilrdquoRevista da Gestao Costeira Integrada vol 8 pp 169ndash181 2008

[31] A C L Castro M M F Correia A R Nascimento et alldquoAspectos bioecologicos do caranguejo-uca (Ucides cordatuscordatus L 1763) (Decapoda Brachyura) nos manguezais dailha de Sao Luıs e litoral oriental do Estado do MaranhaoBrasilrdquo Amazonia Ciencia e Desenvolvimento vol 3 no 6 pp17ndash33 2008

[32] P Goes J O Branco M A A Pinheiro E Barbieri DCosta and L L Fernandes ldquoBioecology of the uca-crab Ucidescordatus (Linnaeus 1763) in Vitoria bay Espırito Santo StateBrazilrdquoBrazilian Journal of Oceanography vol 58 no 2 pp 153ndash163 2010

[33] R G Hartnoll ldquoGrowth sexual maturity and reproductiveoutputrdquo in Factors in Adult Growth A MWenner Ed pp 101ndash128 A A Balkema Rotterdam The Netherlands 1985

[34] C Linnaeus Systema Naturaelig vol 1 10th edition 1758[35] W E Leach ldquoCrustaceologyrdquoThe Edinburgh Encyclopaeligdia vol

7 pp 383ndash437 1814[36] L Boone ldquoA collection of anomuran and macruran crustacea

from the bay of panama and the fresh waters of the Canal ZonerdquoBulletin of the AmericanMuseum of Natural History vol 63 pp137ndash189 1931

[37] A G Cock ldquoGenetical aspects of metrical growth and form inanimalsrdquoQuarterly Review of Biology vol 41 no 2 pp 131ndash1901966

[38] I C Silva and J Paula ldquoIs there a better chela to use forgeometric morphometric differentiation in brachyuran crabs

A case study using Pachygrapsus marmoratus and Carcinusmaenasrdquo Journal of the Marine Biological Association of theUnited Kingdom vol 88 no 5 pp 941ndash953 2008

[39] F J Rohlf ldquotpsDig version 210rdquo Ecology and Evolution SUNYat Stony Brook 2006 httplifebiosunysbedumorph

[40] J Crane Fiddler Crabs of the World Princeton University PressPrinceton NJ USA 1975

[41] A BWilliams Shrimps Lobsters andCrabs of theAtlantic Coastof the Eastern United States Maine to Florida SmithsonianInstitution Press Washington DC USA 1984

[42] I L Dryden and K V Mardia Statistical Shape Analysis WileyChichester UK 1998

[43] C P Klingenberg ldquoMorphoJ an integrated software package forgeometricmorphometricsrdquoMolecular Ecology Resources vol 11no 2 pp 353ndash357 2011

[44] F J Rohlf and D E Slice ldquoExtensions of the procrustes methodfor the optimal superimposition of landmarksrdquo SystematicZoology vol 39 pp 40ndash59 1990

[45] B L Sidlauskas J H Mol and R P Vari ldquoDealing withallometry in linear and geometric morphometrics a taxonomiccase study in the Leporinus cylindriformis group (Characi-formes Anostomidae) with description of a new species fromSurinamerdquo Zoological Journal of the Linnean Society vol 162no 1 pp 103ndash130 2011

[46] P Good Permutation Tests A Practical Guide to ResamplingMethods for Testing Hypotheses Springer New York NY USA2000

[47] C R Goodall ldquoProcrustes methods in the statistical analysis ofshaperdquo Journal of the Royal Statistical Society B vol 53 no 2 pp285ndash339 1991

[48] C P Klingenberg and G S Mcintyre ldquoGeometric morpho-metrics of developmental instability analyzing patterns offluctuating asymmetry with procrustes methodsrdquo Evolutionvol 52 no 5 pp 1363ndash1375 1998

[49] R G Hartnoll ldquoGrowthrdquo in The Biology of Crustacea Embry-ology Morphology and Genetics D E Bliss Ed pp 11ndash196Academic Press New York NY USA 1982

[50] G X Santana and J F R Silva ldquoMaturacao gonadal em femeasdo caranguejo-uca Ucides cordatus Linnaeus 1763 (DecapodaBrachyura Ocypodidae) no mangue do Rio Ceara Caucaia-CErdquo Revista da Gestao Costeira Integrada vol 2 2010

[51] G F Warner ldquoThe occurrence and distribution of crabs in aJamaican mangrove swamprdquo Journal of Animal Ecology vol 38pp 379ndash389 1969

[52] J O Branco ldquoAspectos ecologicos do caranguejo Ucides cor-datus (Linnaeus 1763) (Crustacea Decapoda) do manguezaldo Itacorubi Santa Catarina Brasilrdquo Arquivos de Biologia eTecnologia vol 36 pp 133ndash148 1993

[53] I Nordhaus K Diele and M Wolff ldquoActivity patterns feedingand burrowing behaviour of the crabUcides cordatus (Ucididae)in a high intertidal mangrove forest in North Brazilrdquo Journal ofExperimental Marine Biology and Ecology vol 374 no 2 pp104ndash112 2009

[54] S Y Lee ldquoCheliped size and structure the evolution of a multi-functional decapod organrdquo Journal of Experimental MarineBiology and Ecology vol 193 no 1-2 pp 161ndash176 1995

[55] P K L Ng D Guinot and P J F Davie ldquoSystema Brachyuro-rum part I An annotated checklist of extant brachyuran crabsof the worldrdquo Raffles Bulletin of Zoology supplement 17 pp 1ndash296 2008


[56] J C Fabricius ldquoSystema entomologiae sistens insectorvmclasses ordines genera species adiectis synonymis locisdescriptionibvs observationibvsrdquo pp 1ndash31 Flensbvrgi 1775

[57] M Salmon G W Hyatt K Mccarthy and J D Costlow ldquoDis-play specificity and reproductive isolation in the fiddler crabsUca panacea and U pugilatorrdquo Zeitschrift fur Tierpsychologievol 48 pp 251ndash276 1978

[58] T Detto P R Y Backwell J M Hemmi and J Zeil ldquoVisuallymediated species and neighbour recognition in fiddler crabs(Uca mjoebergi and Uca capricornis)rdquo Proceedings of the RoyalSociety B Biological Sciences vol 273 no 1594 pp 1661ndash16662006

Submit your manuscripts athttpwwwhindawicom

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123

4

5

6

7

8

9

10

(a)

12

3

45

67

8

9

10

(b)

12

3

4

5

6

7

8

9

10

(c)

Figure 1 Ucides cordatus (Linnaeus 1763) localization of landmarks in each anatomic area (a) Dorsal area of carapacemdashC (b) outer face ofmajor chelipedmdashMC and (c) anterior region of cephalothoraxmdashAR

species is being exploited during several hundreds of yearsmany aspects of its biology are scarcely known

Previous investigations using traditional morphometricmethods were performed on populations of U cordatus atSouth Atlantic coast [25ndash32] evaluating ontogenetic changesbetween juveniles and adults of each sex (seeHartnoll [33] fordetails) or by simply testing statistically difference on severalbody measurements between sexes

However despite the fact that analyses using geomet-ric morphometric techniques on U cordatus are relativelyunknown they have been used on several crabs generaon sexual dimorphism and evolutionary studies such asLiocarcinus (Linnaeus 1758) [34] some species ofUca (Leach1814) [35] and the shrimp Litopenaeus (Boone 1931) [4 1014 15 36] Thus the aim of this study is to investigatethe sexual shape dimorphism in three body areas (anteriorand dorsal region of carapace and major cheliped) on aU cordatus population from Northeast Brazil based ongeometric morphometric analyses

2 Material and Methods

Hundred and twenty specimens ofUcides cordatus 60 of eachgender were used for morphometric analysis Specimenswere obtained in the estuary of Potengi River (05∘481015840 S35∘151015840W) state of Rio Grande do Norte Northeast of Brazilthrough active collecting by only one researcher Immediatelyafter collecting the animals were placed inside a freezer atminus20∘C for cryoanesthesia Identification of specimens wasbased on Melo [19] and sex classification on the observa-tion of abdominal shape (narrow for males and wide forfemales) and pleopods number (two pairs in males and fourin females) In this study only specimens with completeappendages without any damage or punctual abnormalitieswere used In order to avoid ontogenetic allometry effects[37] only crabs from the same adult cohort (larger sizes fromthe sexual morphologic maturity sizemdashdata not shown) wereused Sizes of sexual morphology maturity were defined bythe literature review of previous investigations done in thesame geographic region [27]

Digitalized images were obtained by a Sony H10 digitalcamera (81 megapixels) using standardized position anddistance The body areas and structures analysed were the

anterior region of cephalothorax (AR) carapace dorsal area(C) and the outer face of major cheliped (MC) Major rightcheliped was always used when possible Image digitalizationof chelipeds was facilitated by removing them from the bodyThis process was carried out cutting them between propodusand carpus [38]

The software tpsUtil was used to ordinate the digitalizedimages in the same file under the TPS format In additionthe tpsDig2 software [39] was used to record ten landmark ineach structure (Figure 1 Table 1) Description of landmarksfor AR and C followed anatomical criterion defined byCrane [40] and Williams [41] Descriptions of landmarks forthe MC were based on Rosenberg [3] and Rosenberg [4]with some modifications Ucides cordatus shows a more ovaland smooth carapace without any ornamentation whichmakes landmarks establishment difficult differently fromother brachyurans [6 15]Thus the choice of such landmarkswas made using intersections of transverse commissures thatare strongly marked in this species

Landmarks coordinates were submitted to a GeneralizedProcrustes analysis (GPA) [42] in MorphoJ 102b [43] Gen-eralized Procrustes analysis is a procedure that fixes non-shape related variation due to the specimensrsquo position sizeand rotation [44]

In order to avoid static and ontogenetic allometry effectsan allometric correction was necessary to compare the bodyshapes of each gender according to the procedure proposedby Sidlauskas et al [45] Thereunto a pooled within-groupallometric regression using centroid size (Size) was per-formed on Procrustes coordinates (Shape) The statisticalsignificance of the allometric regressions was tested withpermutation tests against the null hypothesis of allometryindependence [46] Percentage of predicted allometry in eachbody area was also calculated as a percentage of total shapevariation that the regression model calculated computedfrom the Procrustes metric [47 48] From this residuals ofthe allometric regression were used for statistical analysis andinvestigation of shape variation [45] for each body part Thedefinition of static allometry used in this work followed Cock[37] that is referred to size allometry as a result of the varia-tion of individuals in the same population and age group Inall body area cases even with static allometry independence(119875 gt 005) the residuals of the regression were used to obtainfurther results of shape variation corrected for allometry










3 Results





4 Discussion





2

119879

2

119875 119875

lowastlowast

119863







Frequency

Discriminant

0

2

4

6

10

8


(a)

Frequency

0

2

4

6

8


(b)

Frequency

Discriminant

0

2

4

6

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(c)




5 Conclusions






Acknowledgments


References






































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology










3 Results





4 Discussion





2

119879

2

119875 119875

lowastlowast

119863







Frequency

Discriminant

0

2

4

6

10

8


(a)

Frequency

0

2

4

6

8


(b)

Frequency

Discriminant

0

2

4

6

8


(c)




5 Conclusions






Acknowledgments


References






































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




4 Discussion





2

119879

2

119875 119875

lowastlowast

119863







Frequency

Discriminant

0

2

4

6

10

8


(a)

Frequency

0

2

4

6

8


(b)

Frequency

Discriminant

0

2

4

6

8


(c)




5 Conclusions






Acknowledgments


References






































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Frequency

Discriminant

0

2

4

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10

8


(a)

Frequency

0

2

4

6

8


(b)

Frequency

Discriminant

0

2

4

6

8


(c)




5 Conclusions






Acknowledgments


References






































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology





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

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