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Buzz-Pollination and Patterns in Sexual Traits in North European Pyrolaceae Author(S): Jette T

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Buzz-Pollination and Patterns in Sexual Traits in North European Pyrolaceae Author(S): Jette T Buzz-Pollination and Patterns in Sexual Traits in North European Pyrolaceae Author(s): Jette T. Knudsen and Jens Mogens Olesen Reviewed work(s): Source: American Journal of Botany, Vol. 80, No. 8 (Aug., 1993), pp. 900-913 Published by: Botanical Society of America Stable URL: http://www.jstor.org/stable/2445510 . Accessed: 08/08/2012 10:49 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Botanical Society of America is collaborating with JSTOR to digitize, preserve and extend access to American Journal of Botany. http://www.jstor.org American Journalof Botany 80(8): 900-913. 1993. BUZZ-POLLINATION AND PATTERNS IN SEXUAL TRAITS IN NORTH EUROPEAN PYROLACEAE1 JETTE T. KNUDSEN2 AND JENS MOGENS OLESEN Departmentof ChemicalEcology, University of G6teborg, Reutersgatan2C, S-413 20 G6teborg,Sweden; and Departmentof Ecology and Genetics,University of Aarhus, Ny Munkegade, Building550, DK-8000 Aarhus,Denmark Flowerbiology and pollinationof Moneses uniflora, Orthilia secunda, Pyrola minor, P. rotundifolia,P. chlorantha, and Chimaphilaumbellata are describedand discussedin relationto patternsin sexualtraits and possibleevolution of buzz- pollinationwithin the group. The largenumber of pollengrains are packedinto units of monadsin Orthilia,tetrads in Monesesand Pyrola,or polyadsin Chimaphila.Pollen is thesole rewardto visitinginsects except in thenectar-producing 0. secundaand C. umbellata.Correlations are presentbetween several sexual traits. Pollen: ovule ratiosare verylow, indicatingefficient pollen transfer. Use ofpolyads may reduce the number of siring males. This trend may be counteracted by largerstigmas as in C. umbellata.Increasing pollen unit size mayenhance relatedness of seeds,reduce abortion, and improveseed set.This mayexplain the evolution, within the Pyrolaceae and otherfamilies, of higher ovule numbers with largerpollen units. The plantsare mainlypollinated by bumblebees. Chimaphila umbellata is visitedby nectar-collectors; Monesesuniflora, Pyrola minor, P. rotundifolia,and P. chloranthaare visitedexclusively by pollen-buzzers; and Orthilia secundais visitedby both nectar-collectors and pollen-buzzers.Nectar secretion is suggestedto be an ancientattractant in thegroup with C. umbellatahaving the least specialized pollination system, and buzz-pollinationin M. unifloraand in the studiedPyrola species regarded as an advancedsystem. About 20,000 species in 72 familiesof floweringplants Moneses (one sp.) of perennialevergreen herbs and sub- have antherswith poricidal dehiscence, i.e., opening by shrubs.The familyoccurs mostlyin coniferforests in the apical pores, valves, or flaps(Buchmann, 1983). Many of northtemperate zone (Andersen, 1943). these species are presumedto be buzz-pollinatedby bees Some highertaxa, e.g., the Pyrolaceae,possess a variety (van der Pijl, 1954; Michener, 1962; sensu Buchmann, of what could be called evolutionarystable reprotypes, 1974). Using rapid contractionsof their indirect flight i.e., differentsets of sexual characterseach carried by a muscles, bees sonicate anthersand harvestpollen. These restrictedgroup of species, while others are extremely buzz-pollinated flowersshare a number of floraltraits. uniformin their expression. Species of the Pyrolaceae They are oftenopen bowl-shaped or withreflexed petals, displaya strikingvariation in floralform and traitsrelated small to average-sized,and oftenlack floralnectar (Buch- to theirpollination ecology. The inflorescencevaries among mann, 1983). Vaccinium,however, a largegenus of buzz- generain its structureand numberof flowers.The flower pollinated plant species, has urceolatecorolla and nectar. varies interspecificallyin its size, form,anther dehiscence, Anthersmay forma cone or brush,and pollen grainsare and stylecurvature (Dahlgren et al., 1980). In addition, of small to medium size with a nonoily,smooth surface thereis a largevariation in pollen formand development (Buchmann, 1983). However, the featureshared by most (Takahashi, 1986a, b, 1987). Several authors have pub- buzz-pollinatedflowers is antherdehiscence by small api- lished pollination ecological informationon the Pyrola- cal pores. Poricidal anthersand deep and narrowcorolla ceae (e.g., Muller, 1881; Ekstam, 1894; Warnstorf,1896; tubes concealing nectar are two parallel ways to reduce Knuth, 1905; Silen, 1906a, b; Andres, 1910; Lovell and therange ofpotential flower resource harvesters -to buzz- Lovell, 1936; Knaben, 1944; Hagerup, 1954; Vogel, 1978; ers and long-tonguedsuckers, respectively.One of the Buchmann, 1983; Standley, Kim, and Hjersted, 1988). predominantlybuzz-pollinated families is thePyrolaceae. These authors have observed Hymenoptera (Bombus, The Pyrolaceae includes four genera, Pyrola (20-30 Halictidae), Diptera (Muscidae, Syrphidae), and Cole- spp.), Chimaphila(seven spp.), Orthilia(one sp.), and optera (e.g., Meligethes)as flowervisitors. A strikingfea- ture common to all these observations is the very low abundance of visitorsto species of the Pyrolaceae. Thus, ' Receivedfor publication 30 October1991; revisionaccepted 25 pollination by wind or selfinghas also been suggestedto March1993. play an importantrole in the reproductiveecology of the The authorsthank the reviewers, S. L. Buchmannand P. G. Kevan, Pyrolaceae (e.g., Knuth, 1905; Hagerup, 1954). formany helpful comments; U. Molau,P. N0rgaard,R. Olson,B. Ox- The aims of this studywere to describe and compare elman,and B. StAhlfor comments on earlierdrafts of the manuscript; L. Tollsten,G. Stenhagen,and H. Albomfor help with the nectar anal- the flowerbiology in relationto the pollinationsystem in yses;R. Erikssonfor help with UV-photographing; P. Johnsen, B. Ov- six NorthernEuropean species of Pyrolaceae,to describe ergaardNielsen, V. Mahler,and B. G. Svenssonfor assistence with and discuss patternsin theexpression of sexual characters, identificationof the insectvisitors; and E. Larssonfor permission to especially pollen unit size and pollination mechanism, campon his property.The studywas supportedfinancially by Marcus and to hypothesizeabout the origin of buzz-pollination LorentzenFoundation (JTK), Nordic Council (JTK), Uppsala Univer- withinthe group. However, since differentplant species sityEcological Research Station, Oland, Sweden (JTK), Danish Natural ScienceResearch Council (#1 1-9025-1, JMO), and CarlsbergFounda- may vary in total amount of resources available for re- tion(#88-0386, JMO). productionand in theirshared ancestry (comparative ob- 2 Authorfor correspondence. servationsare structuredby theircommon evolution[Fel- 900 August 1993] KNUDSEN AND OLESEN-SEXUAL PATTERNS AND POLLINATION 901 senstein,1985]), cross-taxontrends and patternsmust be petrumnigrum. One hundred floweringshoots were viewed with caution. In spite of that we are certainthat monitoredin July 1986. a comparative study of a closely related set of species LocalityB, 1,000 floweringshoots at the-LakeHomsjon obviously possessing a greatvariation in theirsexuality locality,Sweden. Sixtyflowering shoots were monitored might tell us how evolution has favored differentsuc- in July 1988. cessful solutions, i.e., reprotypes,within the ecological and phylogeneticconstraints of the species set. Flowerform - Inflorescenceand grossflower characters forall species were described and measured. MATERIALS AND METHODS Ultraviolet reflectancepatterns were revealed with a UV-transmittingKodak Wratten18A filter(Kevan et al., Plant species,study sites, and populations-Six taxa were 1973; Kevan, 1983). Spectralreflectance in the 300-700- studied: Moneses uniflora(L.) A. Gray, Orthiliasecunda nm rangeof innerand outerpetal surfaces,and of anthers (L.) House, Pyrola minor L., P. rotundifoliaL. ssp. ro- was obtained using a Unicam SP 8,000 recordingspec- tundifolia,P. chloranthaSwartz, and Chimaphilaum- trophotometerfitted with a SP 890 diffusereflectance unit. bellata (L.) W. Barton. To reveal the presenceof nectaries,serial cross sections Moneses uniflora:Locality A, 3,000 floweringshoots of paraffin-embeddedflowers were made. The sections in an area of 1,000 m2 in a forestdominated by Pinus were stained in safraninand fastgreen (Mattsson, 1968). sylvestris,Hasle Lystskov,Bornholm, Denmark (55?10'N, In 0. secunda,nectar productionwas measured with 14?42'E). The forestfloor was sparselycovered by herbs, 1- or 2-Almicropipettes on inflorescencesenclosed for3, especiallyDeschampsia flexuosa, Festuca rubra,Lotus 6, 9, 12, and 24 hr afterthey were depleted fornectar by corniculatus,0. secunda,P. minor,Sarothamnus sco- bumblebees. A seriesof flowers was testedfor nectar pres- parius, and Thymus serpyllum.One hundred and fifty- ence afterbumblebee visits and nothingor only minute eightflowers were monitoredin June-July1987. amounts were present,since nothingwas extractable.In Locality B, severalthousand flowering shoots in an area C. umbellata,standing crop of nectarwas measured with alongthe Northeastern shoreside of Lake Hornsjon,Oland, 1- or 2-idlmicropipettes after enclosure of flowersfor 24 Sweden (57013'N, 16?58'E). Dominant herbs were An- hr, the firstflowers were enclosed from06 to 06 hr and thyllisvulneraria,
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