pollination ecology of the cerrado species eschweilera nana (lecythidaceae subfam. lecythidoideae)

Pollination ecology of the Cerrado species Eschweilera nana(Lecythidaceae subfam. Lecythidoideae)

CAROLINA DE MORAES DE POTASCHEFF1, SCOTT A. MORI2, AND

JULIO ANTONIO LOMBARDI1

1Departamento de Botânica, Universidade Estadual Paulista (UNESP), Av. 24-A, 1515, Bela Vista,CEP 13056-900, Rio Claro, São Paulo, Brazil; e-mail: [email protected]

2 The New York Botanical Garden, Institute of Systematic Botany, 200th St. & Southern Blvd.,Bronx, NY 10458, USA; e-mail: [email protected]

Abstract. Eschweilera nana is pollinated by a guild of pollinators consisting ofmostly bees. Effective pollinators are large bees able to force their way into theclosed androecium to access nectar. The morphology of the flowers diminishes selfpollination and promotes cross-pollination. Although many pollinators make diurnalvisits to the flowers, fruit set was very low in comparison with the number of flowersproduced. Breeding system tests yielded only two fruits, one produced by xenogamyand another one in the control test. The results of this study are consistent with studiesof other Cerrado plants pollinated by guilds of insects and support the conclusion ofother pollination studies of Lecythidaceae that fruit set is low in comparison with thehigh numbers of flowers produced.

Key Words: Barra do Garças, bee pollination, Campsomeris, Parque Estadual daSerra Azul, pollination biology.

Resumo. Eschweilera nana é polinizada por uma guilda de polinizadores composta,principalmente, por abelhas. Os polinizadores são insetos grandes o suficiente paralevantar a estrutura floral que restringe o acesso ao néctar, o capuz estaminal. Amorfologia das estruturas reprodutivas diminui a polinização entre flores da mesmaárvore e promove a polinização cruzada. Apesar da grande quantidade de visitasdiárias às flores por polinizadores, a produção de frutos em relação ao número deflores produzidas por árvore é muito baixa. Os testes de sistema reprodutivo resulta-ram na formação de apenas dois frutos, um produzido por xenogamia e outro docontrole, sugerindo que a espécie seja exclusivamente xenógama. Os resultados dessetrabalho coincidem com de outras espécies do Cerrado, as quais são polinizadaspor uma guilda de polinizadores, com poucas relações específicas, e com de outrasLecythidaceae, as quais também apresentam baixa produção de frutos e acredita-seque sejam xenógamas.

Species of New World Lecythidaceaebelong to subfamily Lecythidoideae (Moriet al., 2007) of which none are native tothe Old World. The other subfamilies ofLecythidaceae (Barringtonioideae [previouslyerroneously called Planchonioideae [Mori etal., 2007] fide Thorne, 2000] and Foetidioideae)are native to the Old World, and the familiesNapoleonaeaceae and Scytopetalaceae are con-sidered by us to be separate families (Mori et al.,

2007) instead of subfamilies of a broaderLecythidaceae. In addition, Asteranthosbrasiliensis Desf., a native species to Amazo-nian Brazil and Venezuela, is now placed in theAfrican family Scytopetalaceae instead of in theNapoleonaeaceae (Appel, 2004).Species of the subfamily Lecythidoideae

are restricted to tropical regions in the NewWorld (Mori & Prance, 1990). In Brazil, thisgroup of trees has the most species in

Brittonia 66(2): 191–206 (2014), DOI 10.1007/s12228-013-9314-0ISSN: 0007-196X (print) ISSN: 1938-436X (electronic)© 2013, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

Published online: 6 September 2013

Amazônia, fewer species along the easterncoast of Brazil, and very few species in theCerrado of central Brazil, where this studywas carried out. Eschweilera nana (O. Berg)Miers is the only species with a widegeographic distribution in Cerrado where itis common in Bahia, Ceará, Goiás, MatoGrosso, Mato Grosso do Sul, Pará, Piauí,Tocantins (Silva Júnior, 2005), Rondônia, andPernambuco (Mori & Prance, 1990).Among the ten genera of New World

Lecythidaceae, there are three types ofandroecial symmetry (Huang et al., in manu-script; Mori et al., in manuscript) as followsin order of morphological complexity: I)Actinomorphic as found in Allantoma Miers,Grias L., and Gustavia L. (Fig. 1A–C); II)Zygomorphic resulting from a unilateralexpansion of a staminal tube as in onlyCariniana Casar. (Fig. 1D); and III) Zygo-morphic resulting from a unilateral expansionof a staminal ring as in Bertholletia Bonpl.,Corythophora R.Knuth, Couratari Aubl.,Couroupita Aubl., Eschweilera Mart. exDC, and Lecythis Loefl. (Fig. 1E–H).Eschweilera nana has the type III androe-

cium (Fig. 2A, B). In the early developmentof a type III androecium, a prolongationdevelops on the abaxial side of the androecialring, at least in other species that have beenstudied (Tsou & Mori, 2007). The fullydeveloped prolongation is called the ligule(Fig. 1E–H). In one species, Couroupitanicaraguarensis DC., the stamens andstaminodes extend from the staminal ring tothe end of the ligule (Fig. 1E) but in otherspecies with type III symmetry the stamens ofthe staminal ring are separated from thestaminodes and/or the vestigial stamens (=staminodes without anthers) located distallyon the ligule by a more or less appendage-free area (Fig. 1F–H). The androecia of thesespecies are, thus, divided into three parts: 1)the staminal ring, 2) the appendage-freeligule, and 3) the androecial hood.Species of New World Lecythidaceae that

have been studied possess one of three typesof pollinator reward: 1) Only fertile pollen,i.e., there are only fertile stamens in theflower and no nectar is produced, so the samekind of pollen effects fertilization and alsoserves as the pollinator reward (e.g., species

of Gustavia); 2) Sterile pollen (also calledfodder pollen) which is produced in theantherodes of the staminodes; thus, bothfertile stamens and staminodes are found inthe same flower—the pollen from the fertileanthers effects fertilization and pollen fromthe antherodes serves as the pollinator re-ward, the best example of this type isCouroupita guianensis Aubl. (Ormond et al.,1981; Yarsick et al., 1986); and 3) Nectarproduced in the androecial hood which servesas the pollinator reward. Sometimes thenectar originates in non-differentiated tissueof the androecial hood but in two genera,Couratari and Eschweilera (Fig. 1H), it isproduced in staminal derived appendagescalled vestigial stamen nectaries. A fewspecies (e.g., Lecythis corrugata Poit.) seemto possess both fodder pollen and a smallamount of nectar (Mori & Boom, 1987).Some species possess open and others closed

androecia. The open flowers, such as found inLecythis pisonis Cambess. (Fig. 1F), do notrestrict pollinators from entering flowers where-as the closed, such as found in Bertholletiaexcelsa Bonpl. (Fig. 1G), limit entry into theflower to only pollinators with the strength toenter the flower by pushing open the androecialhood. Petals pressed tightly against the androe-cium, such as those of Bertholletia excelsa, alsorestrict entry into the flowers. The presence ofyellow antherodes and yellow at the entranceinto nectar-producing flowers serve as a guidefor bees to find pollinator rewards becausefemale bees have an innate preference foryellow (Ushimaru et al., 2007; Kriebel, 2012).Finally, species with geniculate (Fig. 1G) orobliquely oriented styles promote outcrossingby increasing the chance that pollen fromdifferent flowers are rubbed onto the stigmawhen pollinators enter a flower and decreasesthe chance that pollen from the same flowertouches the stigma when pollinators departfrom flowers.Although bees are the most frequent floral

visitors (Mori & Boeke, 1987), bats havebeen recorded visiting the flowers of Lecythisbarnebyi S. A. Mori (Mori & Prance, 1990)and Lecythis poiteaui O. Berg (Mori et al.,1978), and beetles have been suggested aspossible pollinators of some species of Grias(Knudsen & Mori, 1996). In addition, it is not

192 BRITTONIA [VOL 66

FIG. 1. Androecial symmetry of New World Lecythidaceae, type I (A–C), type II (D), and type III (E–H). A.Gustavia B. Allantoma. C. Grias. D. Cariniana. Species of type II are zygomorphic because one side of the staminalring elongates to form a ligule that arches over the summit of the ovary. E. Couroupita nicaraguarensis and C.guianensis F. Lecythis pisonis. G. Bertholletia excelsa H. Eschweilera pedicellata. The drawings are not in scale. A,B, D from Prance & Mori (1979), C from Clark & Mori (2000), E–H from Mori & Prance (1990). Drawings A–C, E–F by B. Angell, D by B. Moyer.

193POTASCHEFF ET AL.: ESCHWEILERA POLLINATION2014]

surprising that many other insects visit theflowers of Lecythidaceae attracted by thefleshy petals and androecia as a place to find

food (Feinstein et al., 2007), lured to theflowers by the usually pleasant but sometimesmalodorous floral aromas, to gather both

FIG. 2. Morphological features of Eschweilera nana. A. Leaves and inflorescence. B. Medial section ofandroecium. Note the single coil with well-developed vestigial stamens on the inner side. C. Hypanthium with twosepals removed. Note the erect style. D. Cross section of an ovary. Note the 2 locules. E. Stamen from the staminalring. F. Fruit base and operculum. G. Seeds. Note the basal arils. A–E. Hatschbach 26025, NY, F–G, Irwin et al.31360, NY.


pollen and nectar without effecting pollina-tion (Jackson & Salas, 1965; Mori & Boeke,1987; Aguiar & Ganglianone, 2008), or as aplace to await concealed to prey upon otherfloral visitors (S. Mori, pers. obs.). Thus,careful observation is needed to examine thebehavior of floral visitors to determine if theytransfer pollen from the anthers of one flowerto the stigma of another flower on anotherplant with enough frequency to warrant beingcalled pollinators instead of visitors, or if theyare flower robbers that utilize floral resourceswithout effecting pollination.The goals of this paper are to describe the

pollination biology of Eschweilera nana,study its breeding system, document itspollinators, compare our results with what isknown about the pollination of other speciesof New World Lecythidaceae and with otherspecies of Cerrado plants, and make recom-mendations for future studies.

Materials and Methods

STUDY AREA

This study was carried out on a population ofEschweilera nana located in an area of cerradosensu stricto in the Parque Estadual da SerraAzul (15º 51’S, 52º 16’W), municipality ofBarra do Garças, state of Mato Grosso, Vale doRio Araguaia region. The park encompasses11,002 hectares at an average elevation of 562m and represents an important conservationunit in the eastern part of the state of MatoGrosso. It includes different physiognomies ofthe widespread Cerrado vegetation that domi-nates the landscapes of the central Brazilianplateau where much of it has been converted toagriculture (FEMA, 2000).According to the classification of Köppen

(1901), the dominant climate of the studyarea is type A (wet tropical), subtype AW(with dry winters and humid summers). Theaverage temperature is 22°C and rainfall isbetween 1200 and 1600 mm with the greatestprecipitation occurring from October to April.

METHODS

A voucher specimen, Potascheff 001,representing the population of Eschweileranana studied, is archived in the Herbário

Rioclarense (HRCB) of the UniversidadeEstadual Paulista Júlio de Mesquita Filho,Rio Claro, São Paulo, Brazil. A total of 30individuals from this population were studied.Insects collected are deposited in the ColeçãoEntomológica das Coleções Taxonômicasdo Instituto de Ciências Biológicas daUniversidade Federal de Minas Gerais.Floral morphology.—Flower morphology

was described based on dissections of flowers(n = 10) and then compared with otherspecies of Lecythidaceae. The morphologicalfeatures of Eschweilera nana were thenevaluated as possible adaptations for pollina-tion.Floral biology.—The duration of anthesis

was determined by observing over 30 markedflowers (n = 10) from the time the budsopened to when the petals and androecia fellfrom the ovary. Stigma receptivity wasstudied by recording morphological changesin the stigma (Dafni, 1992) of 60 flowers andby observing their reaction when 3% hydro-gen peroxide (H2O2) was applied to them(Dafni et al., 2005). In this method, therelease of bubbles from the stigmatic surfaceindicates that the stigma is receptive. Thetiming of anther dehiscence was determinedby direct observation of ten flowers beforeand during anthesis and pollen viability wastested by dying the grains with aceto-carmine(Radford et al., 1974). Flowers were coveredwith bags (n = 13) while still in bud toexclude pollen contamination by floral visi-tors carrying pollen from other flowers.Pollen was then removed throughout anthesisand observed with a compound microscope todetermine if the cytoplasm was uniformlystained thereby suggesting that it was viable.Because some species of Lecythidaceae havetwo pollen types, it was determined if E. nanapossesses two types of pollen by looking forcolor differences in the anthers (when twotypes of pollen are present in the same flowerfertile anthers are usually white and sterileanthers are yellow). Differences in anthercolor are not present in E. nana.Pollinator rewards.—In order to quantify

the amount of nectar produced, buds wereenclosed in sacks (n = 25) to exclude removalof nectar by floral visitors. About half waythrough anthesis the nectar was removed withHamilton micro syringes and the quantity of


nectar was recorded. In addition, the sugarconcentration was registered using an Atago®(0–32% sugar concentration) pocket refrac-tometer. It was not possible to collect nectarat regular intervals because extracting itdestroyed the flowers.Breeding systems/fruit set.—The breeding

system of Eschweilera nana was studied bymaking manual cross pollinations amongflowers of the same individual to test forgeitonogamy (n = 75), among flowers ofdifferent individuals to test for xenogamy(n = 75), within the same flowers to testfor self compatibility (n = 66), and byemasculating flowers to test for apomixis(n = 65) (Radford et al., 1974). Spontane-ous self pollination was tested by baggingflowers. A silk fabric with a mesh size ofless than 2 mm was used to bag theflowers to exclude flower visitors.To estimate fruit set flowers were left

exposed as a control to determine how manyfruits are produced under natural conditions.The number of flowers produced by sixindividuals was estimated by determiningthe average number of inflorescences perindividual and the average number of flowersper inflorescence.Floral visitors.—The number and type of

flower visitor was recorded for a total of 227hours (200 diurnal and 27 nocturnal observa-tions). No observations were made for 24consecutive hours. An effort was made todetermine 1) what animals visited the flowers;2) if visitors contacted the anthers and/or thestigmas; 3) what pollinator reward, if any,visitors collected; 3) the time and frequencyof visits; 4) the number of visits in each treestudied; 5) the movement of visitors amongflowers of the same tree and among differenttrees; and 6) record, when possible, thepresence or not of pollen grains found onthe visitor. An insect was considered a visitorwhen it landed on a flower in search of aresource but did not utilize it and did notconsistently touch the anthers or the stigmawhile in the flower; a robber when it removeda resource from a flower with little or nopossibility that the visit would promotepollination; and a pollinator when it movedpollen from one flower to another flower,either on the same individual or amongindividuals (Endress, 1994).

Results

Individuals of the population of Eschweileranana studied are shrubs or small trees (Fig. 3A)that produce fruits when they are as small as 1.3m tall. The largest trees recorded in the studiedpopulation are 13 m tall. The inflorescences areracemes (Fig. 2A) or sometimes paniculatearrangements of racemes with an average of21 inflorescences per tree. An inflorescenceproduces a maximum of two flowers per day.Flower morphology.—The flowers are ap-

proximately 5 to 6 cm in largest diameter, andpossess white petals, fertile stamens only inthe staminal ring, vestigial stamens but notstaminodes, an androecial hood that is dis-tinctly yellow at the opening into the flower,yellow fertile anthers, yellow vestigial sta-mens, a closed androecial hood with a singlecoil, and much longer appendages on theinterior than on the exterior of the coil(Fig. 3B). The fruits are thick-walled capsules(Fig. 2F) with seeds that possess a small basalaril (Fig. 2G).Floral biology.—Anthesis begins with the

separation of the petals between 0800 and0900 h and the average duration of anthesis is37 hours. During the entire time of anthesis,but not consistently, two morphologicalchanges in the style were observed, theformation of globules at the basal part of thestyle and dark punctations along the length ofthe style. It was not, however, possible to usethese changes to determine the exact time ofreceptivity of the stigma. In addition, it wasnot possible with the hydrogen peroxide testto determine stigma receptivity because itreacts with damaged tissue as well as with thesmall black dots mentioned above. Antherdehiscence begins as soon as the flowersbegin to open and pollen viability, at ca.97.9%, is extremely high. This species doesnot posses fodder pollen.Pollinator rewards.—Nectar is produced at

the base of the vestigial stamens and isalready available in buds that have not yetopened. The quantity of nectar removed fromthe bagged flowers at half way throughanthesis averages 196.55 μl (maximum =388 μl, minimum = 38 μl) and has from27.4% to more than 32% sugar content.Fertile pollen is available from the onset ofanthesis.


FIG. 3. Habit, habitat, flowers, and pollinators of Eschweilera nana. A. Tree in cerrado habitat. B. Mediallongitudinal section of a flower showing the single coil and the well-developed vestigial stamens on the inner side ofthe coil. Nectar is produced at the bases of the vestigial stamens. C. A large, unknown bee taking nectar from theflower before the petals have completely opened. D. The bee Centris scopipes in a flower. Note that even with theopening to the androecium facing downward the bee is still able to enter the flower to take the nectar from the base ofthe vestigial stamens and that the dorsal surface of the bee is placed against the anthers of the staminal ring. E. Thebeetle Xylocopa frontalis taking nectar from a flower. In this case the opening to the androecium is horizontallyoriented and the androecial hood serves as a landing platform. F. The beetle Cyclocephala bicolor preying upon thevestigial stamens of the androecium hood. A–F based on Potascheff 001, HRCB.


Breeding system/fruit set.—Only two fruitswere formed from the 641 flowers tested, onefrom a flower bagged to test xenogamy andanother from flowers in the control group thatwas not preyed upon by Trigona branneri(Table I). Because individual trees variedconsiderably in size, the number of flowersproduced per tree ranged from 540 and 1890per individual over the flowering season. Thepercent of flowers that produced fruits variedfrom 0.5% to 1.33%. Some trees did notproduce any fruits.Floral visitors.—Many insects visited the

flowers of this population of Eschweileranana, including bees, wasps, beetles, butter-flies, ants, moths and grasshoppers. All ofthem are listed and classified as either visitor,robber, or pollinator in Table II. Nevertheless,the pollinators were all relatively large insectscapable of lifting the androecial hood therebymaking it possible for them to enter flowersto collect nectar or pollen and, at the sametime, touch the anthers and stamens.We observed 11 pollinator species: the bees

Bombus atratus, Centris collaris, Centrisdenudans, Centris dorsata, Centris longimana,Centris scopipes, Epicharis flava, Eufrieseaauriceps, Eulaema cingulata, Eulaema nigrita,Xylocopa frontalis, and the wasp Campsomerissp., Apis mellifera and Tetragona clavipeswereobserved a few times trying to access the nectarwithout success as well as collecting pollenfrom the marginal stamens of the staminal ring.The wasps Agelaia pallipes and Apoicaflavissima, the grasshopper, and the katydidate the androecial hood without touching thereproductive parts. The only insect classified as

visitor was an unidentified ant which wasfrequently observed at flowers.The number of pollinator visits made at

hour intervals is shown in Fig. 4. The mostfrequent visits were registered between 0900and 1300 h (Fig. 4) which coincided with thetime when the largest amount of pollen wasavailable. In addition, the largest bees enteredthe flowers to gather nectar even before thepetals opened (Fig. 3C).The smallest bee pollinator was Eufriesea

auriceps which had difficulty opening theandroecial hood. The most frequent pollina-tors were the bees Centris scopipes (Fig. 3D),Epicharis flava, Eufriesia auriceps, Eulaemacingulata, Eulaema nigrita, and Xylocopafrontalis (Fig. 3E). At each visit, the beesand the wasp Campsomeris sp. visited morethan two flowers per individual tree therebymaking geitonogamy possible. Nevertheless,there was a deal of movement of these beesamong individuals of Eschweilera nana andthe bees carried ample pollen on their bodies,both of which increased the probability ofxenogamy.The pollinating bees and Campsomeris sp.

mostly landed near the opening of theandroecium, forced open the hood, andgathered nectar from around the bases of thevestigial stamens on the interior side of thehood. At this time, their ventral surface wastoward the inside of the hood and their dorsalsurface rubbed against the fertile anthers ofthe staminal ring (Fig. 3D, E). When they leftthe flower pollen was carried on their backand head. Upon entering another flower,either on the same tree (geitonogamy) or onanother tree (xenogamy), the pollen wasrubbed off onto the stigma which is situatedslightly above the level of the anthers andobliquely oriented toward the opening of theflower.The beetle Cyclocephala bicolor was ob-

served two times inside flowers feeding onthe vestigial stamens of the androecial hood(Fig. 3F). In spite of it touching the anthersand stigma, this beetle is not considered apollinator because it was not observed tomove from one flower to another, even on thesame tree. The small bee Trigona branneriwas frequently observed robbing the flowersof Eschweilera nana by eating the petals,stamens of the staminal ring and tissue of the

TABLE INUMBER OF FRUITS PRODUCED FOR EACH TYPE OF CROSSING

EXPERIMENT.

Treatment% of fruitsformed

Xenogamy 1.33% (1/75)Geitonogamy 0 (0/75)Spontaneous self pollination 0 (0/60)Manual self pollination 0 (0/66)Apomixy 0 (0/65)Control (with predation by Trigonabranneri)

0.5% (1/200)

Control (without pedation by T.branneri)

0 (0/100)


androecial hood, especially where nectar hadaccumulated. These bees exhibit territorialbehavior by attacking and driving away largerbees that attempted to enter the flowers uponwhich the individuals of Trigona were feed-ing. Flowers damaged by individuals of T.branneri were less commonly visited bypollinators.Although the flowers of Eschweilera nana

remain open overnight, our observations didnot record visits by bats, big moths, ornocturnal bees. We observed only small mothsthat could access the nectar through the holes inthe androecial hood made by the trigonid bees,but without touching the anthers or the stigma.In addition, there were no claw marks on thepetals and androecial hood indicating that batsare possible pollinators.

Discussion

Eschweilera nana possesses flowers with azygomorphic androecium, petals that are nottightly pressed against the androecium and,

thus, do not restrict entry into the flower as dosome other zygomorphic Lecythidaceae (e.g.,Bertholletia excelsa), a single coiledandroecial hood that presses against thestaminal ring, yellow coloration at the en-trance into the androecium that serves as anectar guide, and a stigma located just abovethe fertile anthers that inclines slightly towardthe opening into the flower. Some of thesefeatures are most likely related to pollination:for example, the yellow color attracts bees(Ushimaru et al., 2007; Kriebel, 2012), theclosed androecium keeps most flower rob-bers, especially trigonids, from stealing nec-tar, and the inclined style increases the chanceof pollen from other flowers being depositedonto the stigma when a bee enters the flowerbut not rubbed of onto the stigma when itexits.This species flowers abundantly from Jan-

uary to August (Pirani et al., 2009) andproduces enough nectar to attract numerousvisits by insects. We observed that this

TABLE IILIST OF INSECTS OBSERVED VISITING FLOWERS OF ESCHWEILERA NANA. (* = POLLINATOR, ** = ROBBER, `` = VISITOR) AND WHAT

RESOURCE WAS EXPLOITED BY THEM (PF = PIECES OF FLOWERS, N = NECTAR, P = POLLEN, SH = SHELTER).

ORDER FAMILY SPECIESPOLLINATORREWARD

Coleoptera Scarabaeidae Cyclocephala bicolor ** pfHymenoptera Apidae Apis mellifera ** p

Bombus (Fervidobombus) atratus * nCentris (Melacentris) collaris * nCentris (Ptilotopus) denudans * nCentris (Melacentris) dorsata * nCentris (Trachina) longimana * nCentris (Ptilotopus) scopipes * nEpicharis (Epicharana) flava * nEufriesea auriceps * n, pEulaema (Apeulaema) cingulata * nEulaema (Apeulaema) nigrita * nTetragona clavipes ** pTrigona branneri ** n, p, pfXylocopa (Neoxylocopa) frontalis * n

Formicidae sp 1 ´´ pfScoliidae Campsomeris sp * nVespidae Agelaia pallipes ** pf

Apoica flavissima van der Vecht ** pfLepidoptera sp 1 (moth) ** n

sp 2 (moth) ** nsp 3 (moth) ** nsp 4 (moth) ** nsp 5 (moth) ** n

Orthoptera sp 1 (grasshopper) ** pfsp 2 (katydid) ** pf


species, like some other species of NewWorld Lecythidaceae that have been theobject of pollination study, attracts relativelylarge numbers of insects that exploit thefleshy tissue of the flowers, the pollen, orthe nectar. Many of these insects are simplyflower visitors while others are legitimatepollinators. In this study, we classified 11species of bees and one wasp as possiblelegitimate pollinators.Other species of zygomorphic-flowered

Lecythidaceae that have been the subject ofpollination studies are 1) Bertholletia excelsapollinated by species belonging to the fol-lowing genera of large-bodied bees: Bombus,Centris, Epicharis, Eulaema, and Xylocopa(Mori et al., 2010); 2) Corythophoraamapaensis S. A. Mori & Prance pollinatedby species of Epicharis, Euglossa, Eufriesea,and Xylocopa with Euglossa mixta the mostcommon pollinator (Mori & Boeke, 1987); 3)Couratari tenuicarpa A. C. Sm. pollinated bytwo large-bodied bees, Eulaema mocsaryiand Xylocopa frontalis with the latter speciesentering many more flowers than the former(Nelson et al., 1985); 4) Eschweileradecolorans Sandwith pollinated by at leastfive species of large-bodied bees (Mori &Boeke, 1987); 5) the large-flowered (4.5–6cm diam.) Eschweilera grandiflora (Aubl.)Sandwith pollinated by four species of large-bodied bees, the most common being

Eulaema peruviana and Eufriesea ornata(Mori & Boeke, 1987); 6) Eschweileraintegrifolia (Ruiz & Pav. ex Miers) R. Knuth(syn. = E. garagarae Woodson) pollinated bythe large-bodied Eufriesea ornata (Prance etal., 1983); 7) the relatively small-flowered (2–2.5 cm diam.) Eschweilera apiculata (Miers)A. C. Sm. pol l ina ted by Eulaemabombiformis and Eulaema peruviana (Mori& Boeke, 1987); 8) the medium-flowered(exact size not known) Eschweilerabogotensis R. Knuth principally pollinatedby Epicharis rustica (Gamboa-Gaitán, 1997);9) the large-flowered (3.5–5 cm diam.)Eschweilera pedicellata (Rich.) S. A. Moripollinated by Eulaema peruviana (Mori &Boeke, 1987); 10) Lecythis lurida (Miers)S.A. Mori pollinated by 13 species of mostlylarge-bodied bees (Aguiar & Ganglianone,2008); 11) Lecythis minor Jacq. (treated as L.elliptica, Jackson & Salas, 1965) visited bymany i n s e c t s bu t on l y Xy l o copabrasilianorum was considered an efficientpollinator; 12) the open androecial hoodedLecythis pisonis pollinated by Xylocopafrontalis (Mori & Orchard, 1979) and; 13)the open androecial-hooded species Lecythispoiteaui, and Lecythis barnebyi (Mori et al.,1978; Mori & Prance, 1990) pollinated bybats.There are several examples of wasp polli-

nation represented by numerous papers in the

FIG. 4. Graph showing the number of visits in hourly intervals throughout the day. Based on observations madeduring 227 and 27 hourly intervals from dawn to dusk and from dusk to dawn, respectively.


published literature, e.g., the relationshipbetween fig wasps (Agaonidae) and figs(Ficus L. spp.) and the interaction betweenpollinating wasps and the orchid genusOphrys L. (Proctor et al., 1996). In neotrop-ical Lecythidaceae, only Couroupitasubsessilis Pilg. has been reported to have awasp among potential pollinators (Prance,1976). We conclude that any wasp thatgathers pollen and nectar from flowers shouldbe considered potential pollinators of theplants they visit (Gess & Gess, 2010).Based on their studies of pollination of

Cerrado plants, Saraiva et al. (1988) reportthat wasps pollinate species of Styrax L.(Styracaceae), but observed that their visitsare few in comparison to those of bees. Somewasps, including Campsomeris sp., wereobserved by Barros (1992) collecting pollenfrom three species of Byrsonima Rich. exJuss. (Malpighiaceae), all of which werejudged by them to be capable of pollination;Barros (1998) considered wasps to be theprincipal pollinators of three species ofErythroxylum P.Browne (Erythroxylaceae).Although one of the visitors was a speciesof Campsomeris, for unexplained reasonsthey did not consider it to be a pollinator.Finally, Barbosa (1997) reported that twospecies of Zornia J. F. Gmel. (Fabaceae) arepollinated exclusively by species of waspsand that species of Asteraceae, Burseraceae,Celastraceae, Erythroxylaceae, Euphorbiace-ae, Lamiaceae, Oxalidaceae, Rubiaceae,Verbenaceae, and Vitaceae are pollinated bywasps but not exclusively by them.We conclude that the Campsomeris sp. we

observed in the flowers of Eschweilera nanais a legitimate but probably minor pollinatorof this species because of its infrequent visitsto this species. In addition, Campsomeris sp.is an omnivore and does not rely solely onnectar and pollen for its sustenance therebymaking it less dependent on visiting E. nanafor nectar and pollen.The behavior of the insect pollinators of

Eschweilera nana is the same as reported forother species of Lecythidaceae with zygomor-phic androecia that produce nectar (Jackson &Salas, 1965; Prance, 1976; Mori et al., 1978;Mori & Orchard, 1979; Prance et al., 1983;Nelson et al., 1985; Mori & Boeke, 1987;Gamboa-Gaitán, 1997; Mauès, 2002; Aguiar &

Ganglianone, 2008). Mori et al. (1978) sug-gested that the more complex the androecium,the fewer the number of species of animals thatare capable of pollination. Nevertheless, therewas a high number of species of pollinators ofE. nana which formed a guild of insectpollinators defined by their relatively large sizeand behavior that allows them to open theandroecial hood to obtain nectar while theirhead and dorsal surfaces touch the anthers andthe stigma of the flowers visited. Aguiar andGanglianone (2008) observed 13 species ofbees they considered to be potential pollinatorsof Lecythis lurida, a species with floral mor-phology similar to E. nana in the MataAtlântica of eastern Brazil. In their study,species of bees of Xylocopa and Epicharisexhibited the same behavior in the way thatthey opened the flowers of L. lurida as weobserved for the bees in our study of E. nana.Eschweilera nana possesses a single coil

and nectar is produced from non-differentiat-ed tissue in the androecial hood that is easilyaccessible once a bee opens the hood. Incontrast, access to the vestigial stamen nectariesof species of Couratari and Eschweilera arelimited by the tightly pressed androecial hoodand their location in a nectar chamber at the endof two or more coils. We agree with, but cannotprove, the hypothesis that the more complex aspecies becomes the more limited are thenumber of pollinators that can open theandroecial hood and reach the nectar. Incontrast, smaller flowered species can even bevisited by large bees with long tongues; forexample, the 2–2.5 cm diam. flowers ofEschweilera apiculata are most efficientlypollinated by Eulaema bombiformis andEulaema peruviana but the latter large bee alsopollinates the 4.5–6 cm diam. flowers ofEschweilera grandiflora.The territorial behavior of species of

Trigona recorded in this study has also beenobserved in papers studying the pollination ofother Cerrado species (Barros, 1992, 2001;Barbosa, 1999) and with other species ofLecythidaceae outside of this vegetation type(Mori & Boeke, 1987; Mauès, 2002). In spiteof the observations that species of Trigonafrequently rob pollen (e.g., of Gustaviaaugusta L.) and nectar by perforating holesin the androecial hood (Mori & Boeke, 1987),they may be legitimate pollinators of some


Lecythidaceae (e.g., pollination of the relativelysmall-flowered Corythophora rimosaW.A.Rodrigues subsp. rubra S.A.Mori and therelatively large Trigona capitata, Mori &Boeke, 1987) and other species of Cerradoplants (Barros, 1992, 1996; Barbosa, 1997,1999; Freitas & Oliveira, 2002). Nevertheless,for the most part species of Trigona are robbersof floral resources of species of other plantfamilies as they are of species of Lecythidaceae(Mori & Boeke, 1987; Oliveira & Sazima,1990; Oliveira et al., 1992; Barbosa, 1997;Gamboa-Gaitán, 1997; Oliveira & Gibbs, 2000;Maués, 2002; Carvalho & Oliveira, 2003;Jacobi & del Sarto, 2007; Montoro & Santos,2007; Guimarães et al., 2008). The aggressiverobbery and defense of floral resources byspecies of Trigona may cause the movementof pollen among individuals of species they robby driving legitimate pollinators to other indi-viduals after the pollinators have entered a fewflowers on a plant, a behavior that reduces selfand promotes cross pollination (Gottsberger,1986; Barros, 2001). In this study, we observedthat legitimate pollinators were driven from theflowers of Eschweilera nana to flowers on otherconspecific trees by the aggressive floral re-source robber Trigona branneri.Our studies of the reproductive biology of

Eschweilera nana suggest that it is exclusive-ly xenogamous because fruits were onlyformed from crosses made between flowerson different trees; however, only one fruitwas set from 75 cross pollinations andanother fruit resulted from the 200 controlflowers. Because of the difficulty in makingcrosses among individuals of the same spe-cies of tropical tree there are few studiesbased on crossing experiments; neverthelessstudies of Bertholletia excelsa (Moritz, 1984),Couratari multiflora (J. E. Sm.) Eyma(Lepsch-Cunha & Mori, 1999), Eschweileraovata (Gusson et al., 2006), and Gustaviasuperba (Kunth) O. Berg (Mori & Kallunki,1976) support the conclusion that species ofLecythidaceae are self-incompatible and,thus, rely on cross pollination for fruit set.Mori and Prance (1990) reported that trees

of Couroupita guianensis growing in isola-tion do not set fruit, but when pollen fromother trees was used to pollinate those treesfruits were produced thereby adding furthersupport to the hypothesis that species of

Lecythidaceae are self-incompatible. Maués(2002) found a high ratio of pollen grains perovule (Cruden, 1977) in Lecythis pisonis andBertholletia excelsa which suggests that these,and perhaps other species of Lecythidaceae, arexenogamous. Other species, however, mayhave some self-compatibility; for exampleOrmond et al. (1981) demonstrated self com-patibility in Couroupita guianensis and Moritz(1984) noted that there is a low percentage offruit set derived from self pollination. Notenough is known about the genetics ofLecythidaceae to know the role this factormay play in self-incompatibility.Studies of Cerrado plants have demonstrated

that the majority of plants studied are obligatoryxenogamous (Oliveira & Gibbs, 2000, 2002),but other studies have established that somespecies are self compatible (Sazima et al., 1982;Oliveira & Sazima, 1990; Gribel & Hay, 1993;Saraiva et al., 1996; Barros, 1998; Barbosa,1999; Oliveira et al., 2007). In addition, somedevelop fruits through apomixes, for example,Eriotheca pubescens (Mart. & Zucc.) Schott &Endl. (Oliveira et. al., 1992), and some speciesof Melastomataceae (Saraiva et al., 1996;Goldenberg & Shepherd, 1998).Low fruit production in relation to the

numbers of flowers produced in this specieshas also been observed in the fruit set docu-mented for other Lecythidaceae (Mori et al.,1980; Ormond et al., 1981; Nelson et al., 1985;Gamboa-Gaitán, 1997; Aguiar & Ganglianone,2008). In these and other studies, low fruitproduction was attributed to 1) low numbers ofpollinators in the study area perhaps becausethe trees were growing in disturbed habitats(only 0.02% of the flowers of Lecythis pisonisproduced by five trees yielded fruits, Mori etal., 1980); 2) the inability of trees to supportmany large fruits (Ormond et al., 1981;Gamboa-Gaitán, 1997); 3) poor soil (Nelsonet al., 1985); and 4) intense herbivory of bark(Mori & Becker, 1991), wood (Berkov &Tavakilian, 1999), leaves (Haugaasen, 2009),flowers (Mori & Boeke, 1987; Aguiar &Ganglianone, 2008; this paper), and fruits andseeds (Prance & Mori, 1978; Peres, 1991;Haugaasen, 2009; Haugaasen et al., 2010; S.A. Mori, pers. obs.).The low production of fruits in relation to

the number of flowers produced has also beenobserved for species of plants from Cerrado,


for example, Eriotheca pubescens (Oliveira etal. 1992), two species of Styrax (Saraiva etal., 1988), and two species of TabebuiaGomez (Barros, 2001). In the last two papers,the authors relate the low number of fruitsthat develop to maturity with the low avail-ability of the nutrients needed for theirdevelopment. Barros (2001) also suggestedthat the high production of flowers ensuresthat fruits that do develop are those well-adapted to the Cerrado environment. Inaddition, Oliveira et al. (1992) attributed thelow fruit set of Eriotheca pubescens topredation of immature fruits by Trigonaspinipes.Even the economically important Brazil

nut (Bertholletia excelsa) produces only 63 to216 fruits per tree (Miller, pers. comm.; Malu& Peres, 2005), and it is commonly believedthat production drops significantly after ayear of good production. On the other hand,the second author of this paper has observedvery large fruit crops of Lecythidaceae,especially on trees of species of Carinianaand Couratari and the fruit production ofEschweilera tetrapetala S.A. Mori is some-times so high that its fruits are used to“pave” wet sections of roads (see the speciespage at Mori et al., 2010). We conclude thatthere is a relationship between fruit size andthe number of fruits produced per tree suchthat species with very large, thick-walledfruits (e.g., the Brazil nut [Bertholletiaexcelsa] and the sapucaia tree [Lecythispisonis]), usually produce relatively fewfruits per year in comparison to the smaller,thin-walled fruits of species of Carinianaand Couratari. There are of course excep-tions to this such as the large fruit cropsproduced by the medium-sized, thick-walledfruited E. tetrapetala.

Conclusions

This study confirms that zygomorphic-flowered New World Lecythidaceae withclosed androecial hoods are most efficientlypollinated by a guild of large bee pollinators.Eschweilera nana possesses an androeciumintermediate in complexity when compared toother species of the family in the New World:their closed androecium is more limiting topollinators than is found in species with open

androecia and the single androecial coil isless complex than species with two or moreandroecial coils.We recommend more detailed studies on

the pollination of New World Lecythidaceaethat would encompass all flower types,including those with act inomorphicandroecia, and employs phylogenetic meth-odology to help understand the complexmorphology of the Brazil nut family’s flowersand how that relates to the morphology andnutritional needs of its pollinators. In addi-tion, genetic studies are needed to determinewhy fruit set is so low and to establish ifEschweilera nana and other species ofLecythidaceae are self incompatible. Pollina-tion of Lecythidaceae is a fascinating co-evolutionary story that needs to be studied inmore detail before it is fully understood.

Acknowledgments

We are grateful to Bobbi Angell fordrawing the illustrations used to make theplates in this paper. The senior and thirdauthors are grateful to CNPq (ConselhoNacional de Desenvolvimento Científico eTecnológico) for financial support of thisproject; Fernando Amaral da Silveira(Universidade Federal de Minas Gerais),Rogério Botion Lopes (Universidade Federalde Minas Gerais), and Juares Fuhrmann(Museu de Zoologia da Universidade de SãoPaulo) for insect identification; the Secretariado Meio Ambiente for providing the permitsneeded to carry out research in the ParqueNacional da Serra Azul; and MarylandSanchez and Fernando Pedroni for facilitatingfield work. The second author thanks theNational Science Foundation for the financialsupport provided by a National ScienceFoundation-Opportunities for Promoting Un-derstanding through Synthesis program(NSF-DEB-1119712) grant.

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pollination ecology of the cerrado species eschweilera nana (lecythidaceae subfam. lecythidoideae)

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