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    Iowa ofthe Marne Bgl Asociaon of the Une Kg, page. © Mane loa Asc of he Uae Kington. 207 Eco-morphological consequences of the ‘rostral loss’ in the intertidal marine shrimp Hippolyte sapphica morphotypes ROMAN LIASKO', CHRYSSA ANASTASIADOU* AND ALEXANDROS NTAKIS" ‘Laboratory of Zoology, Department of Biological Applications & Technology, University of loannina, University Campus, Toannina, 45210, Greece, *Fsheries Research Institute, Nea Peramos, Kavala, Macedonia, 64007, Greece ‘The shrimp Hippolyte sapphica has a unique and sharp rostral dimorphism: morphotype A with a well-developed dentate rostrum, and morphotype B with a short, juvenile-like toothless rastrum. Previous research has shown that both morpho ‘ypesiforms belong tothe same species and co-oceur in the same habitat. Both forms occur in both soxes; however, forms B individuals have a higher tendency to Become males. Moreover, form A females are characterized by prolonged viability. ‘The present comparative morphometric study concentrate onthe changes induced bythe rostral dimorphism and interprets ‘hem in terms ofeco-morphologcal adaptations. Results showed that () the rostral length was the mast isometric among the studied morphometric variables (i) male of A and B forms were not significantly diffrent morphometrically ii) unexpet: ily, form A non-ovigerous females had more developed carapace, abdominal somites and appendage in comparzon with form B and, finaly (i), form B ovigerous females had higher tail and scaphocrite lengths, suggesting that they overcome higher turbulent force during the rapid backward movements and thatthe long rostrum improves hydrodynamic streamlining and stability. In conclusion, the previous finding that form B individuals tend to become male receives an adaptational ‘explanation. The gene(s) responsible forthe shor rostrum accumulate in males, where their micro-evolutionary disadvantage {s minimal or even absent. Keywords: adaptation, allometic growth, dimorphism, geometric morphometrcs, Hippoytiae, hydrodynamics, rostrum Submited a9 March 2017; accepted 9 May 2017 INTRODUCTION Rostra polymorphisms in shrimps are rather common phe- ‘omens, which can be observed in both marine (De Grave, 1999; Kapiris, 2005; Kapiris & Kavvadas, 2009) and freshwater species (Anasasiadou et a, 2004; Ocasio-Torres el, 20152). ‘They are usually related to sexual dimosphism (&'Udekem d'Acoz, 1996; Kapiris & Thessalou-Legaki, 2001), reproduct- jive age (Lozano-Alvarez et al., 2007), strategies for the avoid- ance of predation (Jugovic ef al, 2010; Ocasio-Torres etal, 2014, 20136) and other micro-evoltionary factors. However, only inthe species H. sapphica isthe variation of the rostrum structure so sharp and discontinuous. For the species of the genus Hippoyfe the long, well developed rostra, resembling that of morphotype A, seems to be the rule with only three exceptions (Ntakis et al, 2010). Moreover, the geographic distribution of H. sapphica ‘morphotypes shows that form A is widely distributed in the ‘Adriatic, lonian, Aegean and Black Seas, whereas form B has a restricted distribution in the Central Mediterranean (Amvrakikos Gulf and Venice Lagoon) (d’Udekem d’Acoz, 4999 and references herein; Koukouras & Anastasiadou, 2002). The above may suggest that form B could represent @ Serived character. \Corponding author, ma sheng Hippolyte sapphica (Caridea: Decapoda: Crustacea) 4'Udekem d’Acoz, 1993 is a small inshore shrimp, which is distibuted in the Central and Eastern Mediterrancan Seas (@'Udekem d’Acoz, 1993, 1996; Koukouras & Anastasiadou, 2002). The species is marked by a sharp rostal dimorphism (morphotype A and B), which occurs in both sexes: indivi- duals of morphotype A bear a long, robust, dentate rostrum, Whereas those of morphotype bear a short, toothless rostrum resembling thet of juvenile specimens, The two mor- ‘hotypes forms) become distinguishable soon after the com pletion of their Iaval development (megalopal stage), and before the sex ferentiation (fit immature stage) (Niakis et al, 2010). ‘The rostrum is @ prominent structure, which in mature individuals can exceed the carapace length. One could specu- late that the ‘loss’ or the ‘shortening’ of this anatomical feature (type B) must have some epigenetic compensatory effects on other morphological statutes and functional uniies of the ship's body. Moreover, in shrimps, the plastic phenotypical ‘morphological changes could be consistently stuhed, a they aay exceed variation due to genetic diferences (Sarda etal, 1998; Fernandes & Bichuette, 012). iratly, Makis eal. (2010) confirmed the conspecic status ofthe two forms and later Liasko eta. (2015) suggested that rostral length is genetically regulated by a simple locus, with Allele b (morphotype 1B) being dominant. Furthermore, has been shown that morphotype A specimens had high pro- Pensity to become female (A/B ratio in females ~1 : 0.63), Dowrade to npn cambridg argh Nagel on 4 042017 «122424 wat the Cambridg Coe tars of ue, lab tp canrdge rho Downloade er while the oppoite was true for morphotype B specimens (A/B ratio in males 049: ). Likewise, A-phenotype turned out to be superior, in terms of viability. for big ovigerous females (Ciasko et al, 2015) Despite the above advances, the functional value of the long, rostrum and how it contributes to viability is not entirely clea. ‘The defence from predators is a natural explanation and has been advocated by some researchers (Covich et al, 20095 Jugovie etal, 2010; Ocasio-Torres et aly, 2014, 20258, b). However, it is also argued that a long, robust rostrum diminishes the turbulent water flow behind the shrimp's body Goring a rapid escape backward movement (Burukovsky, 1972; Burukovsky & Romensky, 1972; Sard etal, 2005), and thus decreases the energy expenditure while swimming Based on the above hypothesis, and since the effects of ‘rostral loss! in H. sapphica have not been investigated 10 date, the present work aims to comparatively study the com: plete, detailed morphometry ofthe two forms (A and B). In this way, we attempt to benefit from this unique discontinuous rostral variability to draw eco-morphological conclusions about the adaptation of the species and its morphotypes. We expected that, since form A benefits females (Liasko et al, 2015), the females of form B must develop some com- pensatory traits, which would substitute for the lack of @ Jong rostrum. MATERIALS AND METHODS: Shrimp collection and laboratory observation ‘Shrimps were collected in June 2013 from Amvrakikos Gulf (39°13'961"N 20°4s’971"E, NW Greece), at depth 0.52 m using a zooplankton net (mesh size 200 um) in order to sample all the size classes ofthe species. Samples were fixed in situ with 4% formaldehyde solution. In the laboratory, samples were identified by sterco-microscopic inspection and by using a specialized Key (@'Udekem €’Acoz, 1996). In the next step, sex and morphotype identification was accom- plished by inspection of the second pleopod (appendix mascu- lina) and rostrum, respectively. For the present stady, only ‘mature individuals with well-developed secondary sex charac- ters (presence of appendix masculina) were measured and analysed, in order to avoid morphometric variation related to the developmental immature staging, The specimens and their appendages were photographed afterwards under a stereomicroscope and processed blindly by Zen 2012 image analysis software. Morphometrics ‘The morphometric measures reflected different aspects of its functional morphology (Sarda et al, 2005; Kapiris & Kavvadas, 2009), such as vision (eye), defence and streamlin- ing (rostrum), walking (pereiopod) and swimming ability (pleopod, til, telson, uropod), orientation and maintaining direction (caphocerite), metabolic (carapace) and reproduct- jive (abdomen) capacity. All the morphometric variables andmarks and distances), which were used in the present stady, are shown in Figure 3, For the morphological study of the carapace, both distances and geometric morphometrics ‘were used. For mobile structures, lke tal end appendages dis- tances (and not landmarks) were preferred. Statistics ‘The allometri pattern for all distances was neatly linear and was studied by means of the linear least squares regression (character + CL) for all groups pooled (except for the rostrum, for which the allometric patterns were calculated for the two forms separately). Allometric study of morpho- logical traits is the simplest way to reveal their functional Importance during different stages of the life history, ‘uncover sexual dimorphisms etc. (eg, Kapiris & Thessalou- Legaki, 2001; Kapiti, 2005) Furthermore, for distances, the general allometric trend (size effect) was removed according to the following formula (Lleonart etal, 2000): f= ¥(Cly/CLY, ‘where Ys the orginal measure, CLs carapace length and b is the slope oflinear regression of ¥ vs CI for al groups together. The remaining shape patter was investigated by a variety of statistical procedures, ‘Normality of distribution wes ascessed by applying the ‘Kolmogorov -Smimmov est. fects of sex and form on morpho- metric variables were studied by MANOVA and ANOVA techniques (Tukey pairwise comparisons) In order to reduce dimensionality and obtain an ilustrative representation of morphological differences, PCA with varimax rotation vas run oa orginal variables. Finally, geometric morphometrcs were applied for the study ofthe carapace shape and the landmarks shift was et- mated by MANOVA. All statistical analyses were done using SPSS.23 sofware. Geometric morphometrics were performed by Morpho} free software. RESULTS For the 347 shrimps individuals studied, the values of CL vated from 186 (0 3.18 mm in form A and from 1.90 to Suomm in form B (Table 1), The range corresponded to the mature stages of if history and was not biased for A or B for. Al the descriptive stasis (pooled) forthe distance tuowphonetrc characters sted are shown in Table 2. “Te allometic growth pater was isometric forthe rostral Jeng (RL) inform A and negtiveellometri fo he remain ing character. The slope (8) was found to havea wie vai ftion across the studied morphometric variables, ranging from oxo forthe eye's width (EyeW) to 1.02 for the rostral Jength (RL) in fom A (Figure 2). The coelfilentsb for Rl AbaL, Abd, Leg, TL, and to lesser extent for Se and CH vere eaivel love to lnometrie pattern, This nding suggests thatthe functional load (mechanical work and careying ap- aciy) ofthese morphologic tats remains important 2 the animal grows ‘Al departures ofthe morphometi varables from normal ity were elated to Kurta rther than to skewness, fact that allows the application of paremetic methods, which are robust for sich violations. MANOVA run on the distance tnorphometri characters reveled sgnfcant effects of Sex factor (Wilks L= 0120; F= 25. P<0.00%; patti 1 0063) and ofthe interaction Sex x Form (Wilk L=a79; Po nes; P—ooan; pata 70.12), but at of Form inelf Wik’ L= 092; F= 12%; P= 0273). The eis of spwncamrige rare Nal on 4 Dec 281 a 12224 abject the Cambie Coe ems of us arable ip cambMdge renee Faget ori sot vomnsotoaTe0oo Fgrdoorg ov PStosstse (1 ig. (A) Schematic representation ofthe whale body f Hipp sapphic. (8) The oat part of carapace. (C)Cerapce outing Morphomete characters (lances and lindas). Distances Abd abdomen Abd: somes length; CO carapace eight: Clearspace lengths Bye: ee lengthy Bye je ‘dt Lag 3 prio length: Pl ~ rope length of 3 plead; Rs rst lng: RW: rot wi (hig Se seaphoere gi TL: 4h 9 Sone lng Ts Tekon tase leg: Ti: teen length; TW ~ eth somite Baal we; Ur exopodte length of urood. Landmarks: the rearend of ‘tial mage postal tot: the dara most posterior pent of crac: « idl ofthe rear mst pint ofthe epic: the venta lowest oi ‘fearpace 6 plgocomian pin of crpac: 7: antennal ont of crspce ‘the factors on particular morphometric characters were difi- cult to assess by MANOVA due to many missing values, Which cases are excluded from the analysis listwise. ‘Therefore, for this purpose, ANOVA was run foreach charac- ter separately, since these analyses were independent from each other. “The results of multiple ANOVA revealed a strong influence ‘of sex onal distance morphometric characters (Table 3), In all, cases, the effect of form was not significant, but rather the interaction of form with sex (Table 3). More specifically the ale specimens of both forms did not demonstrate any sig- nificant diference for the characters stucied, which suggests ‘that rostrum loss has no serious impact on males. "Table 1. Sample ie, means and ranges of carapace length (CL. mn) Bren by sex and form foe theinvduals staid of H sapphic Morpbonpeorm Sx ON GL Gam) Man Range ™ M6 a= 300 NOP a2 160-308 OF (Saas penne 4 2 M 190 as-ag0 NOP 2 aay mga oF ss 3n0 376-383 ‘Toul 7 1 numberof kndividuals Me Male; NOF Noo-ovgeous female: OF ‘Overs females. “The non-ovigerous females of form A had significantly higher relative values of the abdomen length, eye length, third pereiopod length, exopodite length of the and pleopod. scaphocerite length, telson base length, telson length, and cexopodite length of uropod (ANOVA, pairwise comparisons). ‘We may thus conclude that these traits develop faster in A ‘females, than in their B counterparts. ‘Table 2, Descriptive statis of the studied morphometric characters (Gr all groups pole). SD: Standard Deviation, ‘Morphometric daracter Mean (mum) SD Range (an—max) ‘oat ua or 078370 ‘Aba, 297 064 488-4800 cH 3596 ‘0409 a5c0-2500, a 238 605 o8sa—432 Bre. seas 2136 0965-1459 Ew os 083 0488-1282 Leg 385 ayn 10te-s6a7 a 0875 203 0366-2008 RL (form A) 2909 700 0797-4257 RL (form 8) 0565 307 0236-1305 RW (orm A) 104 ec0-0754 se aya east-3st th 8835 1019-$07, 1B ugg oa8tonsi2 Ta 0388 0211-2360 w asa oayi-uam ur 0336 0703-3699 ey oreo Mage on 0820173122624 sutjetthe Cambridge Core tems of use. allt p/m carpe croenerns 3 4 Exponent b vs CL CPP PR HPS ARETE Fig 2 Almich tern of diferent characters in Happ Bats ‘The morphologial differences between the ovigerous females of form A and B were detected mosty in the relative total length of abdominal 4th to 6th somites (TL P< 0.05) and in scaphocerit length (Se, P < 0.001), characters which are responsible for driving force and stcering respectively and which were more developed in individuals of form B, Finally, an important sexual dimorphic character was the rostral width (RW) in form A. The RW was found to signifi cantly increase in the row males ~ non-ovigerous ~ ovigerous females (ANOVA, P < 0.001). Principal component analysis (PCA), using the morpho- logical distances as original variables, revealed two PCs (PC. Land PC Il, explaining the 65.3% of the total variance, Figure 3). PC incorporated many morphological characters related to the bodys lengths as wells tothe shrimp’sappen- ages, whereas the PC II was positively correlated with Leg, TL, AbdL and, to a lesser extent, with Sc and Ur (walking-swimming machinery). The mean values of the PCs along with the 95% of confidence intervals forthe differ- ent sex/form groups are shown in Figure 4. In this concise representation, tis shown thatthe males of both forms have higher values of PC Il, which is expected, since males are usually more active and tobi. Morphology ‘of males. of both forms was not significantly different (MANOVA, P= 0.43). Only the non-ovigerous females of form A had significantly higher values for both PCs (P-< 0.001), whereas the ovigerous females of form B had @ ‘higher mean value for PCI, without reaching statistical sig- nificance (P = 01082) because only TL and Se were signifi cantly diferent for those sex groups ‘The geometric morphometric analysis did not reveal any diferences in the carapace shape between A and B males. In rnon-ovigerous females, the carapace height (CH) was signifi- cantly higher in form A (Figure 5), whereas in ovigerous females this difference disappeared, DISCUSSION All the morphometric characters studied showed negative allomettic growth, except the rostral length (RL) in form A ‘able 3. ANOVA rests for the sted morphometric characters given by ser and form factors. Morphological Factors ——-Model—-Sigaificance Model uncer F 7 an Tom maa or on Sex oto Form x ex oa30 ‘Aba fom 95 0963 os sex 000 orm x sex ons cH Form 8 oop ow se 000 Form x sex e073 Bt Form sa ors ons see 200 Form x sex ov Ep Foem 7 bus 0x0 See oto Form x se ous Le Form waa oass ow Sex 000 orm x sex oon I Form re) ose Sex 2000 orm x sex 001, se Form ss on out Ser 2200 Form x sex 2000 ™ Fo 78 osy6 oan sex 000 Form xser oss 1 Fo ey one oat Sex ne Form x x 004 TH Form, rr) oy sex 08 Form x sex 000 Ww orm yes oar on Sex 000 orm sex sss ur Eom mom eas Sex 000 Form see 000 individuals, whichis characterized by isometry, in accordance with relevant literature (Kapiris, 2005). The strict isometry of the rostrum in H. sapphica indicates that this morphological character, like the carapace length, may perfectly serve es {growth and/or age marker of the species. The nearly isomet ‘growth exhibited by the abdomen length and width, the 3rd ppereiopod and the length of the 4th, sth and 6th somites ‘points out the great importance of the abdomen parts, and ofthe ‘walking/swimming machinery’ of the shrimp. ‘The present data show that the morphology of H. sapphica was highly influenced by sex. Sexual dimorphic characters hhave been widely studied across the crustacean species and ‘may concern the rostrum (d'Udekem dAcoz, 1997; Kapiris| & Thessalou-Legaki, 2001) as well as the size and other body structures (Bertin et al, 2002; Accioly et al, 2033). In ‘our study, males had relatively moze developed AbdL, TL, Leg, Sc and Us, as PCI reveals. These characters all are related to the capacity of the escape movement and swim- sing, This is expected, since males are smaller, more mobile and active in many species (Correa & Thiel, 2003) including Dowroaed om ttm cane argon Nagra on 4 Dec 20174122424, ajc te Camberg Ceasers fue wae at pw campeon Fegeidsargotorecozntea coo io a5 30 05 wo Pci ig. 5. Pcp component ans dig fer he gal morphometric andes, H. sapphica, As the body size increases in females (which are heavier than males), these characters seem to become func ‘nally less important, ie. the moving ability of the shrimp decreases. Itcan be observed, that in morphotype A, morpho- logical differences have a clear pattern: high values of PCI in males, intermediate position of non-ovigerous females, and high values of PCI in females. This pattern, however, is significantly blurred in B-morphotype, mainly because of female specimens. ‘An interesting and unexpected finding was the clear differ- cence between the non-ovigerous females of forms A and B. ‘More specifically, the non-ovigerous females of form A demonstrated a more developed carapace, abdomen and appendages. This could suggest that form A females develop ‘more rapidly than their B counterparts and, therefore, may reach the reproductive age earlier. The underlying mechan- ims of this diference are sill unknown. Pcl 05 00 Por Fig 4 Meas vals of the PCs along with 9 cndence intra (C1) for ‘Seret sex groups AM: forma A modes BMC form B malen AF orm A son ovigerous feral BF. fm B non oigeoat females; AOV: form A Cnigetou female; BOV: form 8 origras eal, os (10 Fig. 5. Mean carapace shaper (ect magnitied two fd) forthe non- ‘ongeou fale ar the geometric merphomets analysis, Doted ne form A contnseas lie form 8 The Beer show sats sgcant Aplcenent. Differences between form A and B non-ovigeous females concerning the carapace height (CH) did not reach statistical significance when analysed by distance measurements (P= (0079), but could be revealed by geometric morphometric ana- Iysis (MANOVA, P < oo; Figure 5). The majority ofthe carapace landmarks were of ype Il (Le defined geometrically, Bookstein, 1993), but this should not affect the validity of our reals, since the focus of our research was not to study strict homologies but the pure geometric form of the carapace. In such cases, all types of landmarks may be useful (Hingst- Zaher & de Moraes, 2003). Therefore, our rents suggest that when solid structures are under investigation, geometric ‘morphometric means should be preferred against distance sncasurement alysis Finally, for the ovigerous female individual, form B was characterized by relatively greater seaphoceite (Se) and 4th to 6th somites’ lengths (TL). Tail is the structure that ensures rapid movements, whereas scaphocerte serves princi- pally in storing (Sard etal, 1995) It seems reasonable to suppose that the over-development of these characters is related to the swimming needs ofthe form B specimens. A short rostrum, like inform B individuals results in more tur- bulent water flow behind the shrimp during fast backward movements, which needs to he overcome (Burukovsky, 1973 Burukovaky & Romensky, 1972). The observed clon, ation of TL and Se morphometric characters in form B of HL. sapphiea may be explained in this way. Moreover, in form A individuals, the rostral width (RW) was significantly increased in the ascending order. RW (males)

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