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Benthos Research Vol.56,No.2:47-55(2001) BENTHOS RESEARCH

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Benthos Research Vol.56,No.2:47-55(2001) BENTHOS RESEARCH Benthos Research Vol.56,No.2:47-55(2001) BENTHOS RESEARCH The Japanese Association of Benthology Blood Osmoregulation and Ultrastructure of the Gas Windows(•eTympana•f)of Intertidal Ocypodid Crabs:Dotilla vs.Scopimera Masatoshi Matsumasa1),Susumu Kikuchi1),Satoshi Takeda2),Sombat Poovachiranon3) , oi-Sen Yong4)and Minoru Murai5) H 1) Department of Biology,School of Liberal Arts and Sciences,Iwate Medical•@ University, Honcho-dori3-16-1,Morioka020-0015,Japan 2)Marine Biological St ation,Faculty of Science,Tohoku University,Asamushi,Aomori039-3501,Japan Phuket Marine Biological Center,Phuket83000,Thailand3) 4)Department of Zool ogy,Faculty of Science,University of Malaya,59100,Kuala Lumpur,Malaysia 5)Sesoko Station ,Tropical Biosphere Research Center,University of the Ryukyus,3422 Sesoko,Motobu,Okinawa905-0227,Japan Abstract:Intertidal ocypodid crabs of the two genera Dotilla and Scopimera have unique membranous windows(•etympana•f)on their legs for aerial gas exchange,and the former also has them on its thoracic sterna.The osmoregulatory capabilities of Dotilla myctiroides and Scopimera pilura in dilute external media were compared,and microstructure of their tympana was examined to clarify whether they have an osmoregulatory function as well as a respiratory one,because respiratory surfaces are probable sites for osmoregulation or of water/ion loss.Although both D.myctiroides and S.pilura were hyper smoregulators,the former species was much the weaker in this respect.Histological results showed o that the tympana have simple,thin respiratory epithelia in both of these species as well as S.proxima,which indicates that the tympana are probably sites of water/ion loss .The thicker cuticle in Scopimera species than in D.myctiroides may be an adaptive characteristic for maintaining blood osmolality in dilute media,and this was confirmed by silver staining,which indicated that the loss of Cl-through tympana was smaller in Scopimera than in Dotilla.However,at the same time ,the longer blood/gas diffusion dis tance due to the thickened cuticle must result in lower efficiency of gas exchange.Hence ,a trade-off be tween respiratory efficiency and water/ion retention is involved in the development of tympana.From this iewpoint,the presence/absence of tympana among species of the subfamily Dotillinae,which includes v Dotilla and Scopimera,is reviewed with reference to some taxonomic and phylogenetic considerations. Key words:blood/gas diffusion distance,cuticle thickness,Dotilla ,ion/water permeability, osmoregulation,Scopimera,terrestrial adaptation,ultrastructure of tympanal epithelia Semi-terrestrial crabs of the family Ocypodidae pro Received April2,2001:Accepted July27,2001INTRODUCTION vide interesting perspectives for considering the adap tation of aquatic invertebrates to life on land(Powers &Bliss1983).These crabs mainly inhabit intertidal 47 Matsumasa et al. areas and exhibit a distinct zonation of genera and spe All members of the subfamily Dotillinae(Crus cies that reflects their differing degrees of terres tacea:Brachyura:Ocypodidae)except some species of triality.Reduced salinity due to freshwater inflows is Ilyoplax possess large membranous disks(•etympana•f) one of the major problems faced by such semi on the meral segment of the legs(Kemp1919).Species terrestrial crabs.Since variation in salinity increases of Dotilla and Scopimera that inhabit sandy shores with height on the shore as the moderating influence of have these tympana,and species of the former genus the tides diminishes,higher shore species have stronger also have tympana on their thoracic sterna.Maitland physiological mechanisms to protect against salinity (1986)carried out an excellent work on the function of reduction/fluctuation than lower shore inhabitants tympana and revealed that the surfaces are primarily (Macintosh1979). gas windows for aerial gas exchange.In the present To address this problem,comparative studies of study,we compare Dotilla myctiroides as a lower shore crustacean species,including semi-terrestrial crabs, inhabitant and Scopimera spp.as a higher shore dweller have focused largely on the characteristics of respira (see Kemp1919,Hartnoll1973)in terms of their tory organs(e.g.,surface area and morphology)in re osmoregulatory capabilities in dilute external media lation not only to osmoregulatory but also respiratory and the microstructures of their tympana,in order to functions.This is because respiratory surfaces,which clarify whether the gas window also has an require thin membranes for gas exchange,are likely to osmoregulatory function.In addition,we propose a be more permeable to water and ions than other body functional reason for the restriction of this unique res surfaces(Greenaway1988;Lockwood&Bolt1989). piratory organ to only some semi-terrestrial crabs, Some previous studies have revealed that the gill,a namely,members of the Dotillinae,referring to previ major respiratory organ of crustaceans,has ion ous taxonomic studies(Kemp1919;Serene&Lundoer transporting as well as respiratory functions in a vari 1974)and a recent phylogenetic analysis(Kitaura et al. ety of crustacean groups that encounter reduced salin 1998)of this subfamily. ity(Barra et al.1983;Dickson et al.1991;Farrelly& Greenaway1992;Kikuchi&Matsumasa1993a,b; Takeda et al.1996a;Matsumasa et al.1998;Tsubokura MATERIALS AND METHODS et al.1998).However,little work has been done on other types of respiratory organs,although respiratory Animals were collected from sand flats at Port Dickson surfaces other than gills are seen in a variety of crusta (Pantai),Negeri Sembilan,Malaysia,and in Phuket, ceans(McLusky1968;Bliss1979;Maitland1986; Thailand.At Port Dickson,Dotilla myctiroides and Maitland&Maitland1992;Kikuchi&Matsumasa Scopimera pilura were sympatrically distributed.The 1993a,1995,1997). former species inhabited a bare sand substratum on the 一A:・ 穿… 燕 一 刷.㌧ ∠ ・..ヨ.嵐藁 霧.毒 一 …・繭叫 ・ 灘犠 繍 灘 樋 蔽 謙∴-謬 ジ 『猿墓;繍.翻瞳1… .一 ・ 「 ㌧ ・ も '1'』 曹 ヒ ..'竃 ・..・ ・ 一 ∴ ご ∵讐 ・7ご.ぞ:㌶1レξ 読 鵜1・_...詞 鱗., β 窯".齢 賦 羅....齢 、 齢 ・継 ・ rqr'●ば ∵ 灘 閣F●P 1蓑融1繋 鷺鰻 輝懸ii麟 、,降. Fig.1. The Port Dickson site,Malaysia(2•‹30'N;101•‹51'E).Dotilla myctiroides inhabited the lower part of the shore (A).Many individuals of the species often left their burrows,wandered down to the shoreline,and fed in groups there . This behavior,referred to as•edroving•for•eherding•f ,is characteristic for some ocypodid crabs including this species(B). Scopimera pilura was an upper-shore inhabitant,and its habitat was associated with sparse mangroves in this site(C) . These photographs were taken in November,1994. 48 Osmoregulation and gas windows of crab legs lower part of the shore,and the latter,a sand area with analyzed by using a Hitachi H-600A scanning sparse mangrove vegetation higher up(Fig.1;see also transmission electron microscope equipped - with a Takeda et al.1996b).Dotilla myctiroides was also sam Kevex8000X-ray detector. pled at Ao Nam Bor and Ao Tang Khen,and S.pilura For morphological study,meral segments of the and S.proxima at Ban Pa Khloh and Sa Pan Hin,re second and third ambulatory legs of the three species spectively,in Phuket.As on the Malaysian beach,D. and sterna(for Dotilla only)were fixed in a mixed so myctiroides was observed in the lower parts of the tidal lution of2.5%glutaraldehyde and2%formaldehyde flats(see Matsumasa et al.1992,Takeda et al.1996a). buffered with0.2M phosphate at pH7.4.They were Scopimera pilura and S.proxima inhabited the higher rinsed several times in0.2M phosphate buffer and then part of the sandy beaches,although these areas were post-fixed for1hr at room temperature in2%osmium not associated with mangroves. tetroxide in the same buffer solution.After dehydra Adult males of D.myctiroides(mean•}SD of cara tion in an ascending ethanol series,the specimens were pace length:8.15•}0.376mm;n=20)and S.pilura embedded in an epoxy resin(Spurr).Ultrathin sections (mean•}SD of carapace length:5.83•}0.470mm;n= double-stained with uranylacetate and lead citrate were 20)from the Port Dickson site were used in an experi examined for five individuals of each of the three spe ment to determine their blood osmoregulatory charac cies with a JEOL JEM-100B transmission electron mi teristics.Four individuals of each species of crab were croscope.Epithelial and cuticle thicknesses were meas placed in containers with20,30,60,95,and100% ured using a ruler at ten haphazardly selected places on seawater from Port Dickson.The depth of water was photographs of the cross sections(magnification:1•~ just1cm,so the crabs were able to lift their bodies up 104)for each individual;their sum was referred to as into the air.After18hrs(room temperature:22.5•}1 the'total blood/gas diffusion distances'across the tym ),blood samples(ca.100,ƒÊl)were •Ž removed with a sy pana.Because a Bartlett test indicated heterogeneities ringe from the arthrodial membrane at the base of the in variances for the cuticle thickness and the blood/gas fourth ambulatory leg of each crab and allowed to clot. diffusion distance,log(x+1)-transformed data were Osmolality of the serum and external water samples examined by ANOVA using SYSTAT(Wilkinson1992). were determined using a freezing point micro Bonferroni tests were done for multiple comparisons osmometer(Hermann Roebling,Type13DR). among means. Permeable areas on the body surfaces were deter Energy-dispersive X-ray analysis was also used to mined for D.myctiroides,S.pilura,and S.proxima compare the relative abundance of Ca as an index of cu from Phuket by a modified silver staining
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