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FRES1IWATER SPONGES FR( )M A NEOTROPICAL SAND DUNE AREA CE< II IA V01 K\1I K-KII'.I IRQ, MARIA M F < 'ORRLIA. SLRC.IO I A, BR] MI \ WD MAIJR1CIOA. MINDONITA Xoikmer-Riheiro- (".. Correia, M.M.K. Brenha, S.L.A. & Mendonva, MA. I9« 06 30: FieshwalerspongesfromaNeotropical sanJdunearea MewoirxujtheQueenslandMuseum 44: 643-649. Brisbane, issn QQ?£&835. .!' .. freshwaterspon* , unjty fromasanddunebeltarea. I^EcoastofBrazil, is reported for the RtSI tittle. ('on'oheteromeycjiiaheteroselera was the only sponge livingin erystal clear seasonal ponds nestled among Lhe sand dunes. The sponge forms fan-shaped 'hsaroundthe leaves oi&eocham sp.(Cyperacoae) m tileshallow border ofponds, oi ive crusts on sporophytic plants of Eifuise/um sp.(Equisetaceac) in deeper parts of ponds. Towards the boundary, between sand dunes and savanna (cerrado), ponds ait I jeCt tO WJttd action, thus more stable and allowing the establishment of shrubby vegetation and palm trees. Accumulation ofdecaying vegetation produces brownish a watersinwhichsomeofthefivespongespecies live,all characteristicofthe savanna fauna; miaspnuihi, Corvpm&yeflia thwtti Dosifiapydanieli, RodlospottgiliaQmctzonensh and TrachoSpongiila variabilis. An association between twoofthe five savanna species with C he/enisa'cra was ob$erved in some ponds at the verge ofthe mobile sanddunes. This large to representthe 'patch concept' inthedj namicsDfttspondsandtheirspoi communities,i3 Porifera, freslnvater ephemera! habitats, sanddunes, savanna, eeatone. survival i 9!sjp< i . \L - ' ptafiftw- Cecilia lolkmer-Riheiru (email ebib(gpatnpffjche.br) Museu tcias Xaturais, l fJumiacao Z.H/bfitanica d<> Ri'j (jrandcd(j sul. (_\\ Posted U8S, 90.001-9 U :'• R;, andGraduateI ' utificia t'niversidade Catolieado Rio ( Sal. Dr. Postal 1429, 90.61*400, Porto Aieg'nc'- R.\ and helhm Researcher qf'CNPq, Brazil; Maria Marlueia Ferreira Corp tufS A. Bnnha A Muwicj,, drau/c MDcitauzio2n1c,a,65I.0t2e0p-a2r4t0a,wmStaaodLeuiBzio-IMoglTCLBrUanziivl:er1s0iaFaedberFueadreyraJl99d9o. Maranhua, h: GoflQll\ TheeasternpariofMaranhao State, Brazil, isa MATERIALS AND METHODS coastal sand dune field containing an amazing array of seasonal freshwater ponds, nestled 0|it SUTVey offreshwaterSponges ill thesand amongdunes, stretchingalonglhemunicipalities dunelenticsystem wasundertakenatthe Eand W niTut6ia,BarreirinhasandlhmibcrlodeCampos borders ofthe Len^ois Maranhenses, Maranhau and penelralinu 10-50ktn into the countryside State, Brazil {in proximity to the villages of where it borders with the Vcrrado1 (Brazilian Tutoia and Santo Amaro), with some sites inside savanna). The National Park of 'Ecncots the National Park, where sand dunes border with Maranhenscs' was created in 1^X1 to protect the the savanna (Fig I). In response to valuable western part of ibis area. Under Koeppcn's informationprovided by local residentsoncurrent classification thisregion isclassedasAWclimate, Water levels (since dr> and wet seasons do not with the Winy season between Deeembet-Mav, «*lff exactly at the same period each year), our and the annual mean air temperature between survey was conducted between 20-3(1 October 26,S-27.2c,C.(Padua. 1983). Prior to the present W5. At this time oi^ycar lhe largest ponds work we knew nothing about the freshwater (approximately 1500m) contained only about sWcpehroitncaahmelavfpapuweniaatrhosifnttohtihsbeelaNumeneoitsqreuoaepsiocinnaallthlReeengtwiicuotns.vistTaehnmed, c-»>*ounw%saitsd)elrlme]uldCS1la'n|«lol,€pktpetlot>riatluIhnwiea'1ttei5rm»ec™atpgoaecsaialm>«p,lw«eI«bneceh,hw«ia«. study is part of ongoing investigations of the gStnimues. Neotropical freshwater sponge habitats and Severalvariablesweremeasuredinsomeofthe communitiesundertaken bylheseniorauthorand ponds in the western area (piI. temperature and collaborators ( Volkmer-R ibeiro, 1992: salinity ). ThepiI wastaken in sttuwithMerckpll Voikmer-Ribciro & TavatesJ'W; Volkmer- paper. Salinity was also recorded in situ with a Ribeiroet al., 1983,199 salmometer. Samples of sediments were also 644 MEMOIRS OF THE QUEENSLAND MUSEUM !••(* 43"W W FIG. I.TheLencoisMaranhenses.ThevillagesofTutoiaandofSantoAmaro(arrows)areshown,attheEand areaoftheLencoisMaranhenses,respectively,aswellastheNational Parklimitsandthecontactareaswiththe savanna. collected from the top layer ofpond beds, stored of the dry specimens was deposited in the in small glass jars, for ponds in which sponges collection of Departamento de Biologia of were not conspicuous. This was undertaken in Universidade Federal do Maranhao. The other ordertodetermine,throughthepresenceofspicule patl was deposited in the Porifera Collection of sediments,whetherspongeshadeverbeenpresent Museu de Ciencias Naturais of Fundacao intheseponds(Volkmer-Ribeiro&Turcq, 1996). Zoobotanicado Rio Grande do Sul (MCN/POR) These sediment samples are also currently being with Catalog numbers listed in Tables 1 and 2. used by the senior author to study recent and paleo sediments. Entire or cross-sectioned dry RESULTS specimensofC. heteroscleraweregluedtoastub and gold-coated for scanning electron A succession of ponds with different spatial microscope (SEM) observations and areas (Fig. 2A-C) and water color was observed photographedonaMCNJEOL-5200microscope asoneprogressedfromthemobiledunestowards equipped with a Pentax SF7 35mm camera. Part the savanna boundary. Ponds situated among the TABLE 1. Identificationofthespongessampledatthepondsfromthe EareaofLencois Maranhenses, together with theirenvironmental characteristics and substrates. PondTsutsoaimapVlieldlaagreound Typeof sample Environment Substrate Watercolor Spongespecies CatMaCloNg/nPuOmRber LagoadoVidro specimens sanddunes Equisettmisp clear Corvoheteromevcnia 3829-3840 heterosclera ALrapgooaaddoarPontado specimens sanddunes Eteocharissp clear (\uvhoehteetreosrcolmeeryaenia 3830-3839 Radiospongilla amazonensis. I.agoadaPedraHume sediment sanddunes brownishclear Trochospongilla 3854-3856 variabilis, Con'oheteromeycnia heterosclera Radiospongilla LagoadaPontado amazonensis, Mangue bottomsediment oasis brownish Trochospongilla 3859 variabilis LagoadaCoceira sediment grassy field black Corvomeyeniaihumi, 3858 Metaniaspinata NEOTROPICAL SANDDUNE SPONGES 645 FIG. 2. Study area. A, Lagoa do Vidro, at the Eboundary ofthe Lenc6is Maranhenses. B,LagoadaPontado Arpoador,showingthestiffCyperaceanvegetationexposedtothesunasthepondbecomesfullydry.C, Lagoa doPico,atthewesternborderoftheLen^ois,withitssurroundingdunescoveredbybushyvegetationandpalm trees(photosC. VolkmerRibeiro). mobile dunes had crystal clear waters whereas Lagoa da Pedra Hume, Lagoa da Ponta do those approaching the savanna boundary had Mangue,Laguinho,LagoadoPico(Fig. 2C) and increasinglybrownishcolorandacidicpH(Tables Lagoada'Coceirarepresentasuccessionofponds 1-2). having brownish clear to black water, and distributed from the mobile sand dunes into the Lagoa do Vidro (Fig. 2A), Lagoada Pontado almost flat, fixed dunes, covered with grassy or Arpoador (Fig. 2B) and Lagoa do Cajueiro are bushyvegetation. LagoadaPonta do Mangue is clearwaterpondsamongstthemobiledunes.The anoasispondwithsurroundingpatchesorislands dominant plants in these ponds, as potential ofpalmtreesandcontainingshrubbyvegetation. sponge substrates, were Eleocharis sp. and Lagoa da Coceira was reduced to a fetid, tiny Equisetum sp. The former plant is a small but muddy pond with black water surrounded by very abundant Cyperaceae which inhabits the grass. Laguinho was arelatively deep pond, and shallowmarginalareaofponds,andisthefirstto together with Lagoa da Ponta do Mangue, is a emerge fromthe water(Fig. 2B) as ponds begin popularfishing site. to dry up. The second species is also relatively Taxonomic identification of the sponges W abundant in deeper parts ofponds, close to the sampledintheEand duneareasarepresented leeward face ofthe barchan dunes (Fig. 2A). inTables 1 and2,respectively,togetherwiththeir 646 MEMOIRS OF THE QUEENSLAND MUSEUM TABLE2. IdentificationofthespongessampledatthepondsfromtheWareaofLencoisMaranhenses,together withtheirenvironmental characteristics and substrates. PSaonntdosAsmamaprloedVialrloaguend Typeofsample Environment Substrate Watercolor Spongespecies CatMaCloNg/nPuOmRber sLpaealrgianotiautrydeo12%8C,.a5jwu°aeCtierartot(IeOpmaH-m6); Spseecdiimmeenntss& sanddunes Eleocharissp clear Corvhoehteetreosrcolmeeryaenia 3853 Laguinho Specimens sanddunes stones brownishclear Dosiliapydanieti 3857 submersed Metctniaspinata. slaalginoiatyd0o.P5i%c,ow<aptUer5.t5e;m- Specimens& witshanbdusdhuynevseg- bpraarnicahnebsuosfhersi- brownish C'oTrrvoocmheoysepnoinagiliilmami. 3089 perature32"Cat0.10pm) sediments etation {Ciysobalantis Radvairoisapbiolnigs,Ula icaco) amazonensis environmental characteristics and substrates. the accelerated production ofgemmules during Ponds in which only sediments were reported this time of the year. Living specimens of indicate that living samples ofsponges were not C.heterosclera had a light green color, probably found. These tables indicate that due to its association with a microscopic green Corvoheteromeyeniaheteroscleraand M. spinata algae, and this green color could be seen around were abundant, as were gemmules, particularly in thepond marginswherespongeshadbeenburied the two extremes ofthe 'pond succession' (i.e. and were decaying in the sand. very clear ones and the brownish colored ones), confirming that the sampling period was well The sponge community towards the savanna chosenandourprediction thatthishuge seasonal boundary included one or more ofthe following lentic system contained such a fauna. species, but never all live of them: Metania spinata (Carter, 1881), Corvomeyenia thitmi The pond sponge communities also revealed (Traxler, 1895), Dosilia pydanielli Volkmer- interestingdistributionpatterns.Theonlyspecies Ribeiro, 1992, Trochospongilla variabilis found in clear-water sand dune ponds was C. Bonetto & Ezcurra de Drago, 1973, and heterosclera (Ezcurra de Drago, 1974), with RadiospongillaamazonensisVolkmer-Ribeiro& fan-shaped growths on the leaves of the Maciel, 1983. However, leaving this area and Cyperaceae Eleocharis sp. (Fig. 3A) at the pond heading towards the clear-water ponds we margins (Fig. 2B), or thick irregular growths on observed associations ofC. heterosclera withR, the sporophitic plants ofEquisetum sp.(Fig. 3B) amazonensis and T. variabilis. in deeper parts ofthe pond close to the leeward dune face (Fig. 2A). Sponges on both substrates TAXONOMIC REMARKS. Ezcurra de Drago were fullydevelopedandfull ofgemmules. Many (1979) erected Corvoheteromeyenia for specimens were seen dried out, not far from the CorvomeyeniaaustralisBonetto& Ezcurra, 1966, pond margin, their gemmules continually swept and C. heterosclera Ezcurra de Drago,1974. The away by the wind. On the other hand specimens holotype ofthe first species comes from Laguna still submergedatthepondmargins werealready Setubal, nexttothetown ofSantaFe, Argentina, halfburied by sand blown in from the dune, the whereas the holotype of the second species same way as were specimens encrusting comes from NE Brazil, with no precise locality Equisetum located close to the dune inner wall. data.Thedistinctionbetweenthetwospecieswas Corvoheteromeyeniaheteroscleraappearstobea based particularly on their respective species fully adapted to such an environment. gemmoscleres, which are composed of two SEM studyofcross sectionsofEleocharis leaves categories differing in size and shape in the first encrusted with this species (Fig. 3C) disclosed a species, and one category in the second species. skeletal staicture ofvery slim fibers producing a Specimens from the Lencois Maranhenses agree very open and irregular network enclosing sand with the second species in spiculation and grains ofvariable sizes. The presence ofoscular geographical origin. Corvoheteromeyenia sieves(Fig. 3D)isanotherdeviceusedtoprevent heterosclera has also been collected from other oseula being clogged with sand. Gemmoscleres sand dune or paleo sand dune areas in S Brazil were also seen to take part in skeletal fibers, (Volkmer-Ribeiro, unpublished data), and its togetherwith megascleres and two categories of spicularremainsmaybeusefulindicatorsofsuch microscleres (Fig. 3E-F), which might be due to environments. NEOTROPICAL SAND DUNE SPONGES 647 M $U*$Jm*~ FIG. 3. Freshwater sponges. A, Fan-shaped specimens ofCorvoheteromeyenia heterosclera full ofgemmules growing onEleocharis sp. B, Specimens ofCorvoheteromeyenia heteroscleragrowing on Equisetum sp. C, Skeleton of Corvoheteromeyenia heterosclera with an open network where sand grains are enclosed side-by-sidewiththegemmules.D,CrosssectionofaleafofEleocharissp.(arrow,upperleft)encrustedbythe skeletonofCorvoheteromeyeniaheterosclera, showingan irregulardistributionofthethin skeletal fibersand (arrow,upperright)thepresenceofanoscularsieve.E,SkeletonofCorvoheteromeyenia,heterosclerawithtwo gemmulesintheprocessofcompletionatthebottomaswellasabundantfreegemmoscleres(arrow).F,Skeletal fiberofCorvoheteromeyeniaheterosclera(seearrow in Fig. 3E)showingthe reduced amountofsponginand thepresenceofthetwocategoriesofmicroscleres(O, microspinedoxea; M,microanfidiscs)and several large anfidisc gemmoscleres (A) around the megascleres (MG). 648 MEMOIRS OF THE QUEENSLAND MUSEUM ^ - ~ ^piillv^ , hind -* / /:-:-:vK-:v/-:mX-v-v iMmmm 4 q f ' :x-:::^>^^^^/-:v:-y-:-:-:/--- FIG.4.Schematicdrawingofthewind-drivendynamicsthatseasonalpondsaroundthemovingdunesofLencois Maranhenses are subjected to, together with the vegetation and sponges they contain. E= Eleocharis, Eq= Equisetum, DISCUSSION movingdune when again they will be setagainst the inner side of a barchan dune, protected Recent literature dealing with the study of against drought and ready to again form the Neotropical freshwater sponge communities has Equisetum/Corvoheteromeyenia association shown that the five species recorded in the (Fig. 4). present study, found in the ponds close to the The region extending between the areas savanna boundary, generally thrive in seasonal occupied by these two faunas thus biologically ponds N to S throughout the Brazilian savanna and physically defines a savanna/sand dune (Volkmer-Ribeiro, 1992; Volkmer-Ribeiro et al., ecotone. This particular ecotone best fits the 1998). Thus, two characteristic faunal dynamic 'patchconcept' (White&Picket, 1985), assemblages are present: one in the savanna driven by constant disturbance through dune ponds with five species, and one which is mono- movement. The Lencois Maranhenses is an specific and lives in the sand dune ponds. outstandingexampleofthepatchconceptwithits Observations made here on the characteristics pond system, spatial and temporal relationships of C, heterosclera match well with our present todunemovement,anddynamicspongefauna. It understanding of the processes associated with alsoillustratestheremarkableabilityoffreshwater constant disturbances imposed by dune sponges to manage constant disturbance via movement on populations. The living barchan asexual reproduction when gemmules produced dunes,whichmove inthedirectionofthewindin by these sponges are especially selected coastal areas, is awell known geomorphological mechanisms to withstand drought and to phenomenon (Termier & Termier, 1963). The passively disperse via the wind, enabling all six Lencois Maranhenses is, however, unique in its species to opportunistically colonise new pond situation being in a tropical area with a marked systems as they develop. rainy season, resulting in temporary accumulation of water in ponds on the leeward ACKNOWLEDGEMENTS sides of moving dunes, with the ponds subsequently displaced next season. The wind, The authors acknowledge the kind assistance which was seen to blowthe sand into the ponds, of Dr. Marcio F.Costa Vaz dos Santos of the was also seen to blow ahead the gemmules from Biology Dept., Universidade Federal do dry, exposed sponges growing on Eleocharis at Maranhao, Sao Luiz, for identification ofplant the perimeter of ponds. Moreover, the erect specimens. The authors are indebted to two position of plant leaves together with the fan- anonymousreviewersas well astothe editor, for shaped moq^hology of the sponges appears to valuablecommentsonthemanuscript. Thanksto facilitate gemmule dispersal via wind action. Rejane Rosa and M.Sc. Laura Maria G. Tavares These are the pioneers of new sponge (MCN)for,respectively,preparationofFigs1and populations, opportunistically waiting in place 1 1, and operation ofthe SEM. A grant from the where the new border of the pond with National Council for the Scientific and Eleochariswillbesituatednextseason.Thesame Technological Development ofBrazil (CNPq.)- process applies to sponges encrusting on RHAE Program to the senior author funded her Equisetum, which will be passed over by the travelling and field expenses.. NEOTROPICAL SAND DUNE SPONGES 649 LITERATURE CITED extreme South ofBrazil. Iheringia, Zoologia 63: 3-10. EZCURRA DE DRAGO, I. 1979. Un nuevo genera VOLKMER-RIBEIRO, C, MANSUR, M.C.D., sudamericano de esponjas: Corvoheteromeyenia MERA, PA.S. & ROSS, S.M. 1998. Biological gen. nov. (Porifera: Spongillidae). Neotropica. indicators ofthe quality ofwateronthe island of 25(74): 109- 118. Maraca, Roraima, Brazil. Pp. 403-414. In PADUA, M.T.J. 1983. Osparquesnacionaisereservas Miliken, W. & Ratter, J. (eds) MARACA: The biologicas do Brasil. (Instituto Brasileiro de biodiversity and Environment ofan Amazonian Desenvolvimento Florestal: Brasilia). Rainforest.(JohnWiley&SonsLtd:Chichester). TERMIER, H. & TERMIER, G. 1963. Erosion and VOLKMER-RIBEIRO, C. & TURCQ, B. 1996. SEM Sedimentation. (D. Van Nostrand: London). analysis of siliceous spicules of a freshwater VOLKMER-R1BEIRO, C. 1992. The freshwater sponge indicate paleoenvironmental changes. sponges in some Peat-bog ponds in Brazil. Acta Microscopica 5(B): 186-187. Amazoniana. 121(2): 317-335. VOLKMER-RIBEIRO, C. & TAVARES, M.C.M. VOLKMER-RIBEIRO, C. & De ROSA-BARBOSA, 1993. Sponges from theflooded sandbeachesof R. 1972. OnAcallerecurvata(Bowerbank,1863) two amazonian clear water rivers (Porifera). and an associated fauna of other freshwater Iheringia,Zoologia75: 187-188. sponges. Revista Brasileira de Biologia 32(3): WHITE, P.S. & PICKET, S.T.A. 1985. Natural 303-317. disturbance and Patch Dynamics: An VOLKMER-RIBEIRO, C, DeROSA-BARBOSA, R. Introduction.Pp. 3-13.InPicket, S.T.A.& White, &MELLO,J.F. 1983.Theunexpectedoccurrence P.S. (eds) The Ecology ofNatural Disturbances of Drulia browni (Bowerbank, 1863) and Patch Dynamics. (Academic Press: Orlando, (Porifera:Spongillidae) in an oxbow lake at the Florida).

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