Visits of Caluromys lanatus (Didelphidae) to Flowers of Pseudobombax tomentosum (Bombacaceae): A Probable Case of Pollination by Marsupials in Central Brazil Author(s):

Rogerio Gribel Source: Biotropica, Vol. 20, No. 4 (Dec., 1988), pp. 344-347 Published by: The Association for Tropical Biology and Conservation Stable URL: http://www.jstor.org/stable/2388329 Accessed: 08/09/2010 09:57
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S., AND H. GELBAND. 1975. Nectar:its production and functions trumpet in creeper. Science 189: 289-291. L. E. 1975. Ecologicalconsequences a coevolvedmutualism of betweenbutterflies plants.In L. E. Gilbertand P. and H. Raven (Eds.). Coevolution animalsand plants,pp. 210-240. International of Congress Systematics Evolutionary of and Biology,Boulder,CO. GOTTSBERGER, G., J. SCHRAUWEN, AND H. F. LINSKENS. 1984. Amino acids and sugarsin nectar, and their putativeevolutionary significance. Plant Syst.Evol. 145: 55-77. GUERRANT, E. O., JR., AND P. L. FIEDLER. 1981. Flowerdefenses againstnectar pilferage ants. Biotropica(Suppl.): 25-33. by HARBORNE, J. B. 1982. Introduction ecological to biochemistry, edition.AcademicPress,New York. 2nd HORVITZ, C. C., AND D. W. SCHEMSKE. 1984. Effects ants and an ant-tended of herbivore seed production a neotropical on of herb.Ecology65: 1369-1378. INOUYE, D. W., AND R. S. INOUYE. 1980. The amino acids of extrafloral nectarfromHelianthellaquinquenervis (Asteraceae). Am. J. Bot. 67: 1394-1396. , AND G. D. WALLER. 1984. Responsesof honeybees (Apis mellifera) amino acid solutions to mimicking floral nectars. Ecology65: 618-625. LANZA, J., AND B. R. KRAUSS. 1984. Detection aminoacids in artificial of nectars twotropical by antsLeptothorax Monomorium. and Oecologia 63: 423-425. LONGINO, J. T. 1984. Shoots,parasitoids, and ants as forces the populationdynamics Heliconius in of hewitsoni. Ph.D. Thesis, of University Texas (Austin). McLAIN,D. K. 1983. Ants,extrafloral nectaries and herbivory the passionvine, Passiflora on incarnata.Am. Midl. Nat. 110: 433-439. RHOADES, D. F., AND J. C. BERGDAHL. 1981. Adaptivesignificance toxicnectar. of Am. Nat. 117: 798-803. RISCH, S. J., AND C. R. CARROLL. 1982. Effect a keystone of predaceousant, Solenopsis geminata, arthropods a tropical on in agroecosystem. Ecology63: 1979-1983. SCHEMSKE, D. W. 1980. The evolutionary of nectarproduction Costuswoodsonii significance extrafloral by (Zingiberaceae):an of experimental analysis ant protection. Ecol. 68: 959-967. J. SMILEY, J. T. 1985. Heliconius caterpillar mortality duringestablishment plantswithand withoutattending on ants.Ecology66: 845-849. at 1986. Ant constancy Passiflora extrafloral nectaries: effects caterpillar on survival. Ecology67: 516-521. SOUTHWICK, E. E. 1984. Photosynthate allocation floral to nectar: neglected a investment. energy Ecology65: 1775-1779. WATT,W. B., P. C. HOCH, AND S. G. MILLS. 1974. Nectar resource use by Colias butterflies: chemicaland visual aspects. Oecologia 14: 353-374. Janet Lanza BiologyDepartment SUNY at Fredonia Fredonia,New York 14063, U.S.A.

ELIAS, T. GILBERT,

Visitsof Caluromys lanatus(Didelphidae)to Flowersof Pseudobombax tomentosum (Bombacaceae): A Probable Case of Pollination Marsupialsin CentralBrazil by
Due to the greater numberof observations non-flying of mammalsvisiting flowers Old World plant species(see of in review Turner1983) it was considered, untilrecently, thispollination that system was rareor non-existent the in New World. This was explainedby competition with neotropical nectarivorous bats (Sussman & Raven 1978). However,morerecent observations (Lumer 1980; Prance1980; Jansonet al. 1981; Steiner1981, 1983; Torresde AssumpSao1981; Lumer& Schoer 1986) show thatmarsupials, and primates potential rodents, are pollinators of some neotropical plants. During threeconsecutive seasonsI made observations visitsby the marsupial(Caluromys lanatus flowering on (Olfers))to flowers Pseudobombax of tomentosum (Mart. & Zucc.) A. Robyns(Bombacaceae) in the FederalDistrict of CentralBrazil (15?45'S, 47?48'W). The studysiteis locatednearthe coreof the "cerrado"(Eiten 1972) and its was described Eiten (1984). Observations Caluromysvisiting vegetation by of of flowers Pseudobombax were made a during studyon plantspollinated bats (Gribel et al., unpubl. data). by Pseudobombax tomentosuma deciduoustreewhichis typically is foundalong the edges of galleryforest this in and has a markedly region It clumpeddistribution. has a horizontal and normally ends of the branching pattern the branches in contact are withthe canopyof the gallery forest. occursduringthe dryseason after Flowering leaf fall. The flowers alwayslocatedat theend ofthebranches areerect slightly are and or inclined. The flower large(diameter is 344 BIOTROPICA20(4): 344-347 1988

FIGURE 1. Visit Caluromys of lanatus a flower Pseudobombax to of tomentosum.animal The introducingnoseinto funnel its the in the formed thestamens order reach nectar. by to

16-20 cm) with a predominantly whitecolor. The receptade, the perianth, and the base of the stamensforma All in The pistilis erectand the stigmais localized4 cm above the anthers. of chamber whichnectar accumulates. but flexible. as Anthesis the stamens, well as the pistil,are structurally strong beginsbetween1820 and 1840, and the wholeopeningprocess occurswithin to 30 min. The flowers functional one nightonly. 20 are for in Duringthree nights Juneof 1984, eleveninJuneand Julyof 1985, and two in May of 1986, I observed the of animalswhichvisited flowers nineindividuals P. tomentosum, the of locatedin three different of theCapetinga areas of gallery forest the Fazenda Agua Limpa (18 km south of the center Brasilia).A total of 62 hr of nocrumal on weremade. The observations 2100 and 2230. observations began at 1800 hr and ended between I observed totalof 178 flowers a during the 16 nights, and themaximum observed number open flowers of per lanatus visitedflowers and a totalof 169 visitswere treeper nightwas 18. Caluromys during14 of the 16 nights, The numberof visitsto a particular zero and five.I onlyobserved observed 134 flowers. to flower variedbetween flowers bat witha total of six visits.From its size and typeof one large-sized speciesvisiting duringthreenights, I flight, believethatthe bat was Artibeus lituratus, speciesI had observed the and captured previousoccasions on in of an tree visiting flowers Ochroma pyramidale, amazonian introduced urbanareasofBrasilia. Duringthese observations bats flowers P. tomentosum, of theseare themostfrequent visitors bat to no glossophagine wereseenvisiting although in flowers thisregion(Gribelet al., unpubl. data). lanatusvisitedP. tomentosum I the forest. three On occasions observed Caluromys through canopyof thegallery in two individualsforaging simultaneously the same tree,however, duringthe othernightsC. lanatus foraged I individually. During six nights observed movement individuals C. lanatus betweenflowers fourtrees the of of of in the same duster.During theirvisits,the animalsplaced theirfacesinto the flower, with theirnose and eyes whiledrinking nectar the covered the stamens of completely by (Fig. 1). The mean length timespentduringa visit for I was 173 sec (SD = 22, N = 5 forflowers visited the first timeduring night).On three the occasions observed whicharrived before beginning anthesis. the of an individual Duringthesetimestheindividual "opened" theflower, feet without the separating petalswithits front apparently the harming flowers speeding theanthesis and up process. cordatain thetropical lanatusis also citedbyJansonet al. (1981) as a visitor flowers Quararibea to of Caluromys as of also forests Peruand Equador.The twoother speciesof Caluromys apparently use nectar a foodsource.Caluromys L. courbaril French in flowers Inga thibaudiana, ingoides, Hymenaea of and Guiana (Charles-Dominique visits philander BIOTROPICA20(4) 1988 345

in (Musaceae) and Couepia longipendul(Chrysobalanaceae) the of et al. 1981), and flowers Ravenala guyanensis derbianus amazon (R. Gribel,pers.obs.). Caluromys brazilian nearManaus, whichis in thecentral tropical rainforest and Kigeliapinnata Ochroma pyramidale, Trichanthera gigantea, visiting flowers Mabea occidentalis, of was recorded in CentralAmerica(Steiner1981). (Sussman of from mammalflowers non-flying havetried differentiate characteristicsbat flowers to the Some authors nonof about the existence a worldwide, & Raven 1978, Jansonet al. 1981), althoughthereis some controversy of bats (Turner1982, 1983; Wiens et al. 1983). The occurrence glossophagine syndrome flying mammalpollination mammals. this others withregardto the guild of pollinating in differentiates regionfrom exclusively the Neotropics in whereas other phyllostomid flight, bats are alwayssmall (less than 15 g) and visitflowers hovering Glossophagine therefore, are duringvisits.In the Neotropics, largerand land on flowers bats and neotropical marsupials generally thatsome selective on structures. is likely It exercise distinct pressures flower thesetwo groupsof mammalsprobably a comes to require certain once the processof pollination by plantsare used predominantly one groupor the other, & of (Wheelwright Orians1982, Janzen1983). VariousNeotropical interaction of degree specialization theplant-animal Quararibea(Bombacaceae) and Parkia (Leguminosae)are visited,and trees,such as species of Ceiba, Ochroma, mammals (Jansonet al. 1981, bats and/or by non-flying by apparently pollinated,especially non-glossophagine Hopkins 1984). positionof the flowers; largesize, and vertical tomentosum strong structure; the I believethatforPseudobombax by pollination mediumsize mammalssuchas Caluromys chamber;and theerect pistilfavor thedeep and wide nectar to is not becausethe erect bats. Glossophagine pollination probably important P. tomentosum and largephyllostomid visitsof glossophagine difficult impossible. or make typical of hovering and generalmorphology the flowers position This species is bat-pollinated. region, probably speciesin thisgenusin thecerrado another Pseudobombax longiflorum, in the form a are but position, stamens with flowers concurrently P. tomentosum its flowers predominately an inclined discolor bats and Phyllostomus and thepistilhangs.Glossophagine chamber narrow, is "ball," the accessto thenectar in (Gribelet al., unpubl.data; I. Sazima & M. Sazima pers.comm.). of visitflowers Pseudobombax longiflorumcerrado in of of visitor flowers P. tomentosum the area. The clumped distribution P. of lanatus is a regular Caluromys whichare determined severalenvironmental by tomentosum theirpositionalong the edge of the galleryforest, and The relatively small crosspollination. of facilitate movement C. ianatus betweentreesand consequently the factors, of from one treeto another. of per number flowers treeper nightcould also favorthe movement thismarsupial of flowers P. tomentosum. skin The an of On 12 June 1985 I collected individual C. ianatuswhileit was visiting of an of thisindividual, adult male weighing199 g, is depositedin the mammalcollection the Zoology Laboratory in were of and of theUniversity Brasilia.Voucherspecimens P. tomentosum P. longiflorum deposited theHerbarium of of RGO01 and RGO02 respectively). of the University Brasilia(numbers to I wishto thanktheFundaSaoUniversidade Brasiliaforpermission workin Fazenda Agua Limpa; Maristerra de the JohnD. Hay fortranslating manuscript; R. Lemes and JaimeT. FranSaforhelpingin the fieldobservations; the and Eliana Feldeberg helpingin developing photos. for comments Marc Hero formakinghelpful
A. M. CHARLES-DoMINIQUE, M. ATRAMENTOWICZ, CHARLES-DOMINIQUE, HLADIK, C. M. HLADIK, AND M. F. PREVOST. 1981. P.,

plants-animaux. Rev. Ecol. (Terreet d'une foret guyanaise: inter-relations arboricoles nocturnes Les mammiferes frugivores Vie) 35: 341-435. vegetation Brazil. Bot. Rev. 38: 201-341. EITEN, G. 1972. The cerrado of 12: of 1984. Vegetation Brasilia.Phytocoenologia 271-292. ecologyof the neotropical speciesof Parkia. J. of Ecology72: 1-23. HOPKINS, H. C. 1984. Floralbiologyand pollination agentsin the Amazon forest. mammals as pollinating JANSON,C. H., J. TERBORGH,AND L. H. EMMONS. 1981. Non-flying Reproductive Botany,suppl. to Biotropica13: 1-6. guts. In D. J. Futuymaand M. Slatkin(Eds.). Coevolution, pp. 232JANZEN,D. H. 1983. Dispersalof seeds by vertebrate 262. SinauerAss. Inc., Sunderland. in Brittonia 32: 512-517. of LUMER,C. 1980. Rodent pollination Blakea (Melastomataceae) a Costa Rican doud forest. and (Melastomataceae) small rodents by of , AND R. D. SCHOER. 1986. Pollination Blakea austin-smithii B. penduliflora in Costa Rica. Biotropica18: 363-364. of Biotropica12: 239. by PRANCE,G. T. 1980. A note on the probablepollination Combretum Cebusmonkeys. by marsupial.Ann. Mo. Bot. Gdn. 68: 505-513. and potential pollination a neotropical STEINER,K. E. 1981. Nectarivory of (Euphorbiaceae)in Panama. Syst.Bot. 8: 105-117. 1983. Pollination Mabea occidentalis system.Science by SUSSMANN, W., AND P. H. RAVEN. 1978. Pollination lemursand marsupials:an archaiccoevolutionary R. 200: 731-736. arachnoides of C. 1981. Cebusapella and Brachyteles pollinators Mabeafistulifera (Cebidae) as potential TORRESDE ASSUMPyAO, (Euphorbiaceae). Mamm. 62: 386-388. J. 346 BIOTROPICA 20(4) 1988-

V. 1982. Marsupials pollinators Australia. J. A. Armstrong, M. Powell,and A. J. Richards(Eds.). Pollination in as In J. and Evolution, pp. 55-66. Royal BotanicGarden,Sydney. 1983. Non-flying mammal pollination: opportunity Australia.In E. G. Williams,R. B. Knox, J. H. Gilbert, in an and P. Bernhardt (Eds.). Pollination '82, pp. 110-122. MelbourneUniversity Press,Melbourne. WEINS, D., J. P. ROURKE, B. B. CASPER, E. A. RHICKART, T. R. LAPINE, C. J. PETERSON, AND A. CHANNING. 1983. Nonflying mammalpollination Southern of African Proteas: a non-coevolved system. Ann. Mo. Bot. Gdn. 70: 1-31. WHEELWRIGHT, N. T., AND G. H. ORIANS. 1982. Seed dispersal animals: with by contrasts pollendispersal, problems terminology, of on Am. Nat. 119: 402-413. and constraints coevolution.
TURNER,

Rogerio Gribel1 Departamentode Biologia Vegetal FundagAoUniversidadede Brasilia 70910 Brasilia-DF Brasil Presentaddress:Departamentode Ecologia, InstitutoNacional de Pesquisas da Amaz6nia-INPA, Caixa Postal 478, 69.000 Manaus-AM, Brasil

a The Shape of Birdand Bat-Generated Seed Shadows Around Tropical Fruiting Tree
Considering how important shape of the seed shadowsgenerated different the by frugivores to the reproductive is on and of successof animal-dispersed plants,selection fruit characteristics, the spatialpatterning plant communities, few data are available concerning seed shadows generated any frugivores. the Janzen surprisingly quantitative by and directionality batof (1978a, b), Janzenet al. (1976), and Flemingand Heithaus(1981) described density the Smith(1975) and McDonnell and Stiles(1983), data forbirdsappearsto seed shadows,but, excepting generated of timesand movements Janzen1983 fora comprehensive to be limited descriptions visitation (see review).No data are availableto permit comparison seed shadowsgenerated thesetwo groups. the of by In thisstudywe comparedthe shape of the seed shadowsgenerated birdsand phyllostomid by fruit bats around in We did not attempt identify detailthesuiteof avian and to a singlefruiting Muntingiacalabura (Eleocarpaceae). individual contributions the totalfruit to we bat frugivores the removal.Rather, asked visiting M. calabura northeir "Do avian and bat frugivores the tree?"Fleming thequestion, generate same shape of seed shadowarounda fruiting of et al. (1985) present excellent an M. description the natural history and birdand bat speciesvisiting, calabura of, in the same regionas our study. at This studywas conducted Hacienda La Pacifica, Guanacaste,Costa Rica during July1986. The M. calabura forest was locatedat the tip of a narrow band of riparian projecting m intosavanna.The treewas surrounded 15 by grazedsavannaon three sides,whilethe fourth side facedriparian forest m distant. 15 When theM. calabura began seed collectors underthe canopy(6 collectors) and at 5 and 15 m ripening fruit, placed a seriesof 1 m2 screen we Twelve of theselatter from tree(20 collectors). the seed collectors werelocatedon the savannaside of the distances We checkedtheseseed collectors removed and tree(eightat 5 m, 4 at 15 m distances). dailyat dawn and dusk any seeds.Sinceno collectors other thanthosedirectly underthecanopywerepositioned feces undervegetation, containing to we considered seed-bearing fecesthatappearedat the dusk survey be frombirdsand at the dawn survey be to from bats. over 23 sample days (Table 1). Of these,39.1 percent fecal specimens We collected335 seed-bearing were weredepositedby bats. A 2 x 2 contingency comparing numbers test the of deposited birds,while60.9 percent by "undercanopy"and "away" by birdsand batsshowedthatbirdsdeposited significantly a feces seed-bearing deposited of = greater proportion theirseed loads underthe canopythan did bats (X2 4.83, df = 1, P < 0.05). Considering of differed betweenthe birdonlyseeds thatweremoved away fromthe canopy,the directionality seed deposition seed shadows(2 x 2 contingency x2 = 27.4, df = 1, P < 0.05). The bird-generated and bat-generated seed test, the the shadowwas strongly skewedtowards open savanna,whereas bat-generated shadowhad a strong skew in the direction the forest of edge. of fecesdepositedunderthe treecanopyby birdssuggests The higher proportion seed-bearing that,on avetage, of within treeand so deposited to the theyspenta greater proportion the timefromfruit ingestion seed elimination BIOTROPICA20(4): 347-348 1988 347