Geometric Morphometrics of Carapace of Macrobrachium Australe

Acta Zoologica (Stockholm) 93: 492–500 (October 2012) doi: 10.1111/j.1463-6395.2011.00524.x

Geometric morphometrics of carapace of Macrobrachium australe (Crustacea: Palaemonidae) from Reunion Island Gabrielle Zimmermann,1 Pierre Bosc,2 Pierre Valade,2 Raphae¨l Cornette,3 Nadia Ame´ziane1 and Vincent Debat3

Abstract 1Museúm National d’Histoire Naturelle, Zimmermann,G.,Bosc,P.,Valade,P.,Cornette,R.,Ame´ziane, N. and Debat, UMR CNRS 7208, De´partement Milieux V. 2012. Geometric morphometrics of carapace of Macrobrachium australe et Peuplements Aquatiques, 43 rue Cuvier, (Crustacea: Palaemonidae) from Reunion Island. — Acta Zoologica (Stockholm) 2 75005 Paris, France; Association Reúnion- 93: 492–500. naisepourleDe´veloppement de l’Aquacul- ture, Z.I. Les Sables – BP 16 – 97427 We investigated the structure of carapace shape variation in six populations of 3 Etang-Sale´,LaReúnion, France; Museúm Macrobrachium australe Gue´rin-Meńeville 1838 (Crustacea: Decapoda: Palae- National d’Histoire Naturelle, UMR CNRS monidae) from Reunion Island (Indian Ocean) freshwaters. The morphometric 7205, De´partement Syste´matique et Evolu- analysis revealed the occurrence of two morphotypes corresponding to two dif- tion, 45 rue Buffon, 75005 Paris, France ferent types of habitats. Individuals living in lotic habitats present a thick carapace armed with a short, robust and straight rostrum, while individuals from Keywords: lentic habitats have a slender carapace armed with a thin long rostrum orientated phenotypic plasticity, crustaceans, amphidromy, morphometrics, shape, carapace upward. This difference suggests an adaptation to lotic disturbances and is tenta- tively interpreted as adaptive phenotypic plasticity. In such amphidromous Accepted for publication: organisms regressing to freshwaters after a marine larval phase, selection for 11 July 2011 physiological and developmental flexibility might facilitate further adaptation and allows the colonisation of a wide panel of environmentally different and sometimes geographically distant insular streams. Vincent Debat, Museúm National d’Histoire Naturelle, UMR CNRS 7205, De´partement Syste´matique et Evolution, 45 rue Buffon, 75005 Paris, France. E-mail: [email protected]

(Atkinson 1977; Jalihal et al. 1993; Murphy and Austin 2004) Introduction and finally return to freshwaters after metamorphosis. This Freshwater prawns of the genus Macrobrachium Bate, 1868 larval marine phase allows an intense dispersion of the larvae (Crustacea: Palaemonidae) are a highly diverse group of deca- and the colonisation of new habitats sometimes very distant pod crustaceans (with 239 speciesdistributedintropical from the home river (McDowall 2007). regions across the world (De Grave et al. 2009)) and are often This extremely challenging strategy of dispersion requires considered as good aquaculture species (New and Singholka the adaptation to sharply contrasting salinity and the ability to 1985; Mariappan et al. 2002, 2003; Mariappan and Balasun- settle into a panel of habitats (McDowall 2007) often drasti- daram 2004). In particular, Macrobrachium australe Gue´rin- cally different in terms of hydrodynamic and physicochemical Meńeville 1838, also known as ‘chevrette’, is a widespread parameters. species in the Indo-West Pacific region. In Reunion Island Amphidromy has evolved several times independently in (Mascarenes Islands), it is commonly captured in traditional crustaceans, fish and molluscs (McDowall 2007). Phenotypic fisheries and is a potential candidate to regional farming plasticity might play a role in the adaptation to the new and activities. stressful environments amphidromous organisms face during Although commonly referred to as freshwater prawns, their life cycle. Natural selection is indeed expected to favour many Macrobrachium species are amphidromous (sensu Myers plasticity over local adaptation when environmental variation 1949); the adults live in freshwater habitats where they mate is recurrent and therefore predictable (e.g. Scheiner 1993; De- and lay eggs; then, the newly hatched larvae reach the estua- Witt and Scheiner 2004), and it is thus generally assumed that rine or marine environments to complete their larval life cycle organisms facing such environmental changes during their life

2011 The Authors 492 Acta Zoologica 2011 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 93: 492–500 (October 2012) Zimmermann et al. • Carapace shape variation in Macrobrachium cycletendtobemoreplasticthanthoselivinginmorestable pereiopods, very developed in the Macrobrachium genus and habitats [see Schlichting and Pigliucci (1998); Pigliucci commonly used in the systematic discrimination of species) (2001); West-Eberhard (2003) for comprehensive reviews]. has been discarded. In addition to its ability to detect subtle Macrobrachium species are known to combine a rather low size and shape differences and to allow groups discrimination, level of global shape differentiation across species with a rela- GM was chosen because of the possibility to reconstruct theo- tively high intra-specific variability that often makes the alpha retical landmarks configurations (i.e. extremes, averages) taxonomic work difficult (Koshy 1971; Short 2000; Mariap- making it possible to visually display morphological changes pan and Balasundaram 2004). and thereby facilitating biological interpretations. Focusing on the Australian endemic Macrobrachium australiense Holthuis, 1950, Dimmock et al. (2004) have shown that Materials and Methods morphological traits such as abdomen length and width can be strongly affected by environmental parameters such as Reunion Island (2512 km2) is a French overseas department water temperature, a result in agreement with previous sug- located in the Indian Ocean. With Mauritius and Rodrigues, gestions (e.g. Lee and Fielder 1981). it makes up the Mascarenes. La Reunion Island is located at Other environmental factors such as hydrodynamic param- approximately 21S, about 700 km from Madagascar and eters likely alter crustaceans’ morphology (Spaargaren 1999). 160 km from Mauritius. The island counts 13 perennial rivers This might be particularly true for sessile organisms; for exam- and several seasonal streams, among which water velocity ple, Neufeld and Palmer (2008) showed that penis size and appears to be contrasted at river mouth. On the basis of this shape in barnacles (Balanus glandula Darwin, 1854) vary observation, six rivers were chosen in the hydrographical net- among sites with different wave force regimes and suggested work (Fig. 1). The Gol gully, the Saint-Jean River and the that the differences observed should arise primarily owing to Roches River present lentic river mouths characterised by phenotypic plasticity. slow water current, while the Saint-Etienne River, the Saint- Mobile organisms might be affected by hydrodynamic fac- Gilles gully and the Langevin River have lotic river mouths tors as well. Evidence of ecophenotypic variation has been characterised by high-speed water current (see Fig. 2 for provided in various organisms (e.g. De Wolf et al. 2000; Tits- details). As diverse environmental parameters covary with cur- elaar 1998), particularly related to gradients of exposure to rent speed that might also affect morphology, we will hereafter wave action and tidal height (Coˆrte-Real, Hawkins and refer to ‘river type’ when contrasting lotic and lentic rivers. Thorpe 1992). Among crustaceans, river specimens of Aegli- dae crabs were shown to differ in shape from the lake speci- Sampling mens and to present much higher intra-populational variability (Giri and Loy 2008), presumably in relation to the M. australe prawn populations were sampled close to six river different water dynamics of both systems. mouths at a rate of 20–30 individuals per river from late In this study, we investigated the variation in size and shape August to early October 2007, leading to a total sample size of of the carapace among M. australe individuals from Reunion 159 individuals. The natural stocks of this vulnerable species Island sampled in six river mouths strongly differing in terms are much eroded, which limited sample size. of current speed. Derived from the fusion of the head and the In order to focus on a single troop of juveniles having trunk in crustacean decapods, the carapace is involved in passed the river mouth at the same time after their marine many functions (nutrition, sensing, locomotion), which makes phase and having spent the same 3-week-long period in the it a suitable structure to investigate adaptation to contrasted rivers, we decided to sample post-larvae and juvenile individu- environments. Landmark-based geometric morphometrics als of total length ranging from 30 to 40 mm. Sexual dimor- (GM) was used to investigate carapace variation. GM has phism does not affect the individuals of this size; the two sexes been successfully applied to the analysis of phenotypic plastic- are indeed virtually identical at that stage and cannot be ity in diverse organisms [ranging from Drosophila wings (e.g. discriminated on a morphological basis (Gue´rin-Meńeville Debat et al. 2003, 2009) to freshwater snails shell (e.g. Lan- 1838). This, therefore, allows to include in the dataset both gerhans and DeWitt 2002) or fish body shape (e.g. Walker males and females. 1997; Langerhans et al. 2003)], including crustaceans (e.g. Prospections were led in the known habitat preferendum of Giri and Loy 2008). The carapace being a one-piece rigid M. australe: near banks above river mouth, in areas rich in structure is particularly amenable to GM studies, allowing the aquatic plants (mostly periphyton, algae and microphytes) definition of homologous landmarks (Giri and Agustin-Col- (Keith et al. 2006). For each sampling point, the current lins 2004; Giri and Loy 2008). In body articulated organisms speed was recorded and box plots of the data per river were such as decapod crustaceans, the use of such one-piece body calculated (Fig. 2). feature is required for landmark-based analysis, in order for All prospections were carried out using the ‘electric fishing’ the landmarks relative position not to fluctuate because of method with a ‘Martin-peˆcheur’ power generator (Gosset body articulation. For this reason, the use of articulated body et al. 1971). Fishing was carried out walking upstream so that structures such as the chelipeds (the second pair of the water ahead remained clean and to ensure that the animals

2011 The Authors Acta Zoologica 2011 The Royal Swedish Academy of Sciences 493 Carapace shape variation in Macrobrachium • Zimmermann et al. Acta Zoologica (Stockholm) 93: 492–500 (October 2012)

15 km Saint-Jean river * Sampling on 13/09/2007 27

Roches river * Sampling on 11/09/2007 S 21° Saint-Gilles gully * 26 Sampling on 26/09/2007 30

Leeward coast

Bras de Cilaos

Bras de la plaine Windward coast 25 Gol gully Sampling on 31/08/2007 * 23 * Saint-Etienne river Sampling on 02/10/2007 Sampling station 28 River with lentic mouth * River with lotic mouth Langevin river Sampling on 28/09/2007 27 Number of specimen sampled E 55°30’ E 56°

Fig. 1—Map of the perennial rivers of Reunion Island and summary of the location data for the six sampling stations. The star indicates river with lotic mouth, and the circle indicates river with lentic mouth. paralysed by electric shock drifted with the current into the configurations to a common size; the configurations are then landing net (Lamarque 1975). translated so that their centre of gravity would match; finally, the configurations are rotated so that to minimise the distance among corresponding landmarks (maximise the superimposi- Images acquisition, landmarks definition tion). In order to avoid problems related to the loss of dimen- A digital image of the carapace of each specimen was obtained sions owing to the superimposition, a principal component using an Olympus SZ61 dissection microscope connected to a analysis (PCA) was applied to the Procrustes coordinates (i.e. computer by means of a camera (Olympus camedia C5050 the coordinates after superimposition) and the PC scores were zoom). The alignment of the two eyes with the optical axis used as shape variables in all subsequent shape analyses. Log was used as criteria for standardising the specimens position- of the centroid size was used as a size variable. ing under the dissection microscope. TheimageswereacquiredinthetpsDig1.40program Measurement error analysis (Rohlf 2004), and 10 landmarks were digitised on each indi- vidual carapace (Fig. 3). When possible, landmarks were Imaging error could not be estimated as only one picture was defined at intersection of different tissues or at very conspicu- available. Digitizing error was assessed as follows: the land- ous and singular locations [Type 1 landmarks (Bookstein marks were acquired three times on a single picture of each of 1991); LM # 1, 2 and 10], but curvature maxima (Type 2 20 specimens. PCA plots were visually inspected, and a landmarks) were used in most cases (all other landmarks). MANOVA (multivariate analysis of variance) using individu- Generalised least-squares Procrustes superimposition was alsasthemainfactorwasappliedtothePCscores.Asignifi- used to extract shape variation from the landmark data (see cant effect would indicate that shape variation among for example Dryden and Mardia 1998). This superimposition individuals is higher than that attributing to digitizing error. is an iterative process that comprises three steps (Rohlf and Slice 1990): first the raw landmark coordinates of each config- Statistical analysis uration are divided by the corresponding centroid size (i.e. the square root of the sum of the squared distances from each Analysis of size. Variation of carapace mean size across rivers landmark to the centroid of the configuration) to scale all and ‘river types’ (i.e. lotic versus lentic) was investigated using

2011 The Authors 494 Acta Zoologica 2011 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 93: 492–500 (October 2012) Zimmermann et al. • Carapace shape variation in Macrobrachium

v (cm/s) Lentic/Lotic threshold = 30 cm/s (Malavoi & Souchon, 2002) 180 Min and Max outliers 160

140

120

100

Current speed Current 60

0 Gol Roc Stj Stg Ste Lgv

Fig. 2—Box plots of water current data at river mouth (in cm ⁄ s) for the six rivers chosen in the study, with mention of the lentic ⁄ lotic threshold suggestedbyMalavoiandSouchon(2002).Gol,Golgully;Roc,RochesRiver;Stj,Saint-JeanRiver;Stg,Saint-Gillesgully;Ste,Saint-Etienne River; Lgv, Langevin River. Box plots display the median (horizontal bar); the boxes hinges are for the quartiles; whiskers extrema indicate the deciles.

Fig. 3—Side view of the carapace and position of the 10 landmarks used. a nested ANOVA on centroid size with river as a random communiation) running with the R version 2.6.2 (R Develop- effect nested into river type. Multiple pairwise t-tests were run ment CoreTeam 2008). to detect the statistically significant differences among couples of rivers, using the correction proposed by Benjamini and Results Yekutieli (2001) to avoid false positives. Measurement error Analysis of shape. Shape data were first examined using a principal component analysis (PCA) applied to the Procrustes The results of the MANOVA on shape variables are shown in coordinates. Table 1. The variation among individuals is higher than that We then tested whether individuals from the six rivers induced by the digitizing procedure. Although this procedure morphologically differ from each other applying a MANO- likely underestimates the actual measurement error (the imag- VA to the PC scores. In order to better display the rela- ing error is not assessed), these results nevertheless suggest tionship among groups, canonical analyses (CA) were that the data are indicative of real biological differences. performed using either river or river type as classifying parameters. Differences in size Changes in conformation along each multivariate axis were reconstructed using multivariate regressions, and the corre- Results are shown on Fig. 4 and Table 2. Statistically signifi- sponding deformations were visualised. cant difference in size was detected among rivers, but not All morphometric and statistical analyses were performed among river types. The individuals of the Saint-Gilles are the using R-morph library (Michel Baylac, 2007 personal largest, slightly larger than the ones from Saint-Jean river

2011 The Authors Acta Zoologica 2011 The Royal Swedish Academy of Sciences 495 Carapace shape variation in Macrobrachium • Zimmermann et al. Acta Zoologica (Stockholm) 93: 492–500 (October 2012)

Table 1 Measurement error analysis of shape environments (group 1) from those caught in lotic ones (group 2). The mapping of other environmental parameters Effect df Pillai Approx. F Numerator df Denominator df P-value provided extremely similar results, as expected from the strong correspondence between the river flow and vegetation, Individuals 19 13.49 11.29 304 640 <000.1 granulometryandsubstrate.Thisresultisconfirmedbya Residuals 40 canonical variates analysis (CVA) using ‘river type’ as a group- df, degrees of freedom; SS, sums of squares; MS, mean squares. ing factor (i.e. lentic versus lotic) (Fig. 6). The corresponding shape differences were reconstructed using a multivariate regression. The lentic and the lotic populations mainly differ (adjusted pairwise t-test P = 0.0021); individuals from the in the relative length and orientation of the rostrum and in the Gol gully and the Roches river stations have a similar, interme- general thickness of the carapace, which differences are mac- diatesize(adjustedpairwiset-test P = 1 ns). Individuals from roscopically visible (Fig. 7). the Saint-Etienne and Langevin rivers stations are similar in The analysis of the residuals of a multivariate regression of size (adjusted pairwise t-test P = 1 ns) and are the smallest. the shape variables on the river mouth flow shows that statistically significant differences exist between rivers within each of the two morphotypes (Table 2). Differences in shape Statistically significant differences in shape were detected Discussion among rivers and river types as shown in Table 2. This is clearly illustrated by the first PC plan (Fig. 5): two morpho- The structure of M. australe carapace shape variation logical groups are discriminated on the first axis (accounting recorded in this study is dominated by the opposition of two for 66.8% of the total variance). The group 1 is defined for types of morphology (Figs 6 and 7): a first morphotype char- the negative values of PC1 and made up by the Gol gully, the acterised by a thick carapace armed with a short, robust and Roches and Saint-Jean rivers stations; the group 2 is defined straight rostrum and a second morphotype characterised by a for the positive values of PC1 and made up by the Saint- slender carapace armed with a thin long rostrum orientated Etienne, Saint-Gilles and Langevin rivers stations. upward. The mapping of environmental data on the first PC plan As the tip of the rostrum is strongly affected by this effect, (Fig. 5) clearly contrasts the samples caught in lentic we investigated whether removing LM1 would impact on the

Fig. 4—Log of the mean centroid size for each sampled river. The star indicates river with lotic mouth, and the circle indicates river with lentic mouth.

2011 The Authors 496 Acta Zoologica 2011 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 93: 492–500 (October 2012) Zimmermann et al. • Carapace shape variation in Macrobrachium

Table 2 Effects of river and river type on size (ANOVA) and on The most striking pattern of this analysis is the strong con- shape(MANOVA).Thetestontherivereffectonshapeisrunonthe gruence between water flow environment and morphology; residuals from a multivariate regression of current speed on shape the robust carapace characterises lotic habitats while the slen- (i.e. after the effect of current speed was removed) der carapace occurs in lentic habitats. Although the hypothesis of genetic adaptation to these con- Effect df SS MS FP-value trasted habitats cannot be apriorirejected (neither at the very Size extreme, the occurrence of two slightly differentiated species River type 1 1.18 1.18 0.5 0.52 each specialised on a type of river) – a genetic analysis of the River 4 9.5 2.38 82.76 <0.0001 Reunion Island samples is necessary to test it – the occurrence (nested in of adaptive phenotypic plasticity, which is an important fea- river type) ture of the genus [e.g. Dimmock et al. (2004)], seems a plau- Residual 312 8.95 0.03 sible scenario. Evolution of plasticity is indeed particularly likely in amphidromous organisms, where regular switches Approx. Numerator Denominator from freshwater to sea are experienced. Besides, the marine df Pillai F df df P-value larval stages are highly dispersive and their further return to Shape freshwater is likely to occur in any stream of the area of disper- River type 1 0.7 43.74 16 301 <000.1 sion. In other words, the juveniles might return to rivers other Residuals 316 River 5 2.05 13.03 80 1505 <000.1 than those inhabited by their parents and thus encounter dif- Residuals 312 ferent environmental conditions, impeding adaptation across generations and likely inducing a strong genetic mixing. This, df, degrees of freedom; SS, sums of squares; MS, mean squares. together with the lack of evidence from other commonly used traits in alpha taxonomy (e.g. chelipeds, position of cephalo- thorax spines), also makes the presence of two morphologically very close species unlikely. As previously mentioned, diverse environmental parameters covary with current speed, potentially jointly influencing carapace shape. For example, different predation regimes related to different vegetation covers might stimulate different development of the rostrum. It is also conceivable that carapace shape may vary as a plastic response to differences in oxygen levels in still versus moving water. The observed shape change is nevertheless particularly consistent with biomechan- ical predictions; the flexibility of cephalothoracic and rostral structure influences the mechanical behaviour of the prawn body while standing or moving in the water current. Accord- ing to Statzner and Holm (1989), the steepest velocity gradients close to lotic macro-invertebrates are found near areas of their bodies protruding furthest into the flow, such as the rostrum for the genus Macrobrachium. The beam theory (Vogel 2003) thus predicts that shorter and stouter morphological features should better resist to the forces experienced in the Fig. 5—Scatter plot of shape configurations projected into the first fast water currents of a lotic habitat. two principal components. Symbols for specimens are plotted Such a shape plasticity in relation to water velocity has according to sample. indeed been documented in several crustacean groups [e.g. barnacles (Neufeld and Palmer 2008); Aeglidae crabs (Giri and Loy 2008)]. Therefore, although other environmental occurrence of the two groups. Landmarks showing large devi- effects might occur, it seems reasonable that current speed, ation from general pattern might indeed bias interpretations through its hydrodynamical implications, should have a major by artificially inflating variation at other landmarks owing to influence on Macrobrachium carapace shape. the least-squares criterion used in the superimposition proce- Finally, it is conceivable that the high developmental and dure [the ‘Pinocchio effect’ (Chapman 1990; Zelditch et al. physiological flexibility imposed by selection for amphidromy 2004)]. We thus removed LM1 and conducted the analyses might in turn facilitate the colonisation of diverse and fluctuat- anew. Centroid size differences detected among rivers were ing habitats. This ecological strategy might thus provide not affected, and neither was the overall structure of shape organisms with a higher adaptability to new environments via variation, suggesting that there is no Pinocchio effect. plasticity (West-Eberhard 2003).

2011 The Authors Acta Zoologica 2011 The Royal Swedish Academy of Sciences 497 Carapace shape variation in Macrobrachium • Zimmermann et al. Acta Zoologica (Stockholm) 93: 492–500 (October 2012)

Fig. 6—Canonical variates analysis using ‘river type’ as a grouping factor (i.e. lentic versus lotic) with shapes reconstructed using multivariate regression of shape coordinates over CV scores. The frequencies are shown on the Y-axis.

Fig. 7—Drawing of Macrobrachium australe sampled in Reunion Island showing the two morphotypes revealed in this study. The scale is the same for both images. —A.Prawn B ﬁshed in Roches River, showing the ‘lentic’ morphotype characterised by a slender carapace armed with a thin and long rostrum orientated upward; —B.Prawnﬁshedin Langevin River, showing the ‘lotic’ morphotype characterised by a thick carapace armed with a short, robust and straight rostrum.

These results that emphasise the potential impact of Thomas Chancerel for their precious help during the sam- environmental parameters on morphology, therefore, sug- pling and laboratory work. gest that the rostral features classically used in the alpha taxonomy of the Macrobrachium prawns and for the species References description should be considered cautiously, as previously suggested by Short (2004). Atkinson, J. M. 1977. Larval development of a freshwater prawn, Additional data are needed and particularly at the genetic Macrobrachium lar (Decapoda, Palaemonidae), reared in the labora- level to better understand the processes involved in shaping tory. –Crustaceana33: 119–132. Benjamini, Y. and Yekutieli, D. 2001. The control of the false discov- Macrobrachium morphological diversity. ery rate in multiple testing under dependency. – Annals of Statistics 29: 1165–1188. Acknowledgements Bookstein, F. L. 1991. Morphometric Tools for Landmark Data: Geome- try and Biology. Cambridge University Press, Cambridge. Samples were collected and photographed during the annual Chapman, R. 1990. Conventional Procrustes approaches. In: Rohlf, survey of the freshwater species of La Reunion, led by the F.J.andBookstein,F.L.(Eds):Proceedings of the Michigan Morpho- Association Reúnionnaise pour le De´veloppement de l’Aqua- metrics Workshop (Special publication No. 2), pp. 251–267. Univer- sity of Michigan Museum of Zoology, Ann Arbor. culture (ARDA). We especially thank Henri Grondin. This Coˆrte-Real,H.B.S.M.,Hawkins,S.J.andThorpe,J.P.1992. research was supported by the MNHN PPF ‘Structure et Genetic confirmation that intertidal and subtidal morphs of Patella Evolution des ećosyste`mes’ and ‘Etat et structure phylogeńe´- ulyssiponensis aspera Roding (Mollusca: Gastropoda: Patellidae) tiquedelabiodiversite´ actuelle et fossile’. We are grateful to are conspecific. Arquipe´lago 10: 55–66. the members of the MNHN Plateforme morphome´trie and DeGrave,S.,Pentcheff,N.D.,Ahyong,S.T.,Chan,T.-Y.,Cran- especially to Michel Baylac. We particularly thank Gerard dall,K.A.,Dworschak,P.C.,et al. 2009. A classification of living and fossil genera of decapod crustaceans. – The Raffles Bulletin of Marquet, Marc Eleáume, Philippe Keith and Danielle Defaye Zoology, Supplement Series 21: 1–109. for their valuable advises, and Marine Richardson and

2011 The Authors 498 Acta Zoologica 2011 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 93: 492–500 (October 2012) Zimmermann et al. • Carapace shape variation in Macrobrachium

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2011 The Authors 500 Acta Zoologica 2011 The Royal Swedish Academy of Sciences