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Pollination Ecology of Gaura and Calylophus

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Pollination Ecology of Gaura and Calylophus Volume 91 Annals 8 Number 3 of the 2004 Missouri Botanical Garden POLLINATIONECOLOGY OF Richard R. Cli77ebellII 2 A77gelaCrowe 3 GAURAAND CALYLOPHUS 0at3id P. Gregory,4and Peter C. HochS (ONAGRACEAE,TRIBE ONAGREAE)IN MIESTERN TEXASxU.S.A.1 A 13$'1'RACrr This analysisreports insect ViSitf3rs7 with pollen loatl(1atae for the majorfltwering spee ies of a planttommunity at the Mt)nahaneiSandllills an(l nearly sites in the Transpe(os regil)n(f westernlexas U.S.A. with( oncentrationon four speeies (f ()nagraceaeStril)e Onagreae. We (hara(terizethe pllinatrs of tw) spe(ies of Gelzlra(C. coceineaand C. villv3a) andtW(I species of Calylvphzs(C. berl(lzzdieriand G Alrfusegli),as well as threemajor co-blooming non-(nagrad speeies (Thelespermamegfluatamiemm (Astera(eae) Men.t.zeliast.rict.issim.(l (IJoastaeeae), and Argemonepolyflnthemos (Papasxerafeav)).Partial data wele tollectefl on two a(lditionalspeties of ()rlagreae,Oenotfiaera ertgelmarti.i and 0. rhombi.petalfl.Insect collections were ma(leduring repeate( visits to the planttommunily, with samplingthroughout the floweringseason and a 24-hourperiod. Nearly 1tS0() insects were captured on the nine targetplant taxa, with more than l(K)insett species carryingpollen. The primaryspecies of Onagraceaestu(lied had diverseinsect visitors,and differentinsents served as primarypollen carriersfor differentspecies. Gauravillosa showedthe greatestdiversity, with at least 32 insect species carryingpollen, the majort arriersbeing the antlionXcotoleon 2 species of noctuid moths,and 2 halictidbees in $hecodogastra.By contrast,the pollencarriers of G.cocci7Iea were noctuid and geometrid moths,of Calylophs berlandzerione of the samespevies of Sphecodogastranseveral chrysomelid and buprestidbeetles ' The authorsare gratefulto Peter H. Ravenand Dennis Breedlovefor the opportunityto studyand analyzetheir earliercolleetions of onagradpollinators for illelusionin this paperand to the NationalGeographic Society and the MissollriBotanical Garden for fieldworksupport. We also gratefullyacknowledge prior support for Ravenfrom the U.S. NationalScience Foundation. We are gratefallto the Field Museumfor fundingresearch at the Museumby Clinebell and for permissionto workwith their collections.We thankthe followingtaxonomic specialists for help with insect identifications:Ted MacRae(Monsanto Company) and Philip Parrillo(Field Museum)for Coleoptera;Neil E+ranhuis (BishopMuseum) and DavidPollock (Bishop) for Diptera;Mike Arduser (Missouri Department of Conservation)and Ron McGinley(Illinois Natural History Survey) for Hymenoptera;Paul Goldstein(Field), Phil Koenig(no affiliation) and RichardHeitzman (no affiliation) for Lepidoptera; and Norm Penny (California Academy of Sciences)for Neuroptera. RobertRaguso (USCH), Warren Wagner (US), and GeorgeYatskievych (MO) provided help with plantidentifications. Don Hardin(Washington University) provided assistance in the field, preparationof tables, and photographicdocu- rnentation.Richard Keating (M0) helpedin the preparationof photomicrographs.We are gratefulto the librarystaff of the MissouriBotanical Garden for theirgenerous help in locatingand borrowingnecessary entomological publications. We also thankRaguso, the editor,and an anonymousreviewer for commentsthat improvedthis paper. 2 MissouriBotanical Garden, P.0. Box 299, St. Louis, Missouri63166-0299, U.S.A. [email protected]; peter. hoc h@m{>bot. org. 3 FontbonneCollege, St. Louis,Missouri. 4 24 BaldwinCOUI1, Fitzwilliam, New Hampshire034477 U.S.A. ANN.MISSOURI BOT. GARD. 91* 369400. 2004* 370 Annals of the Missouri Botanical Garden (Coleoptera),and severalbeeflies (Diptera);and of C. hartwegiia combinationof the sphingidmoth Hyles lineata, severalnoctuid moths, the honeybeeApis niellifera, and the samespecies of Sphe{rodogastraThe 3 co-bloomingspecies also had a diversityof insectvisitors, but therewas essentiallyno overlapin majorpollen carriers between the species of Onagraceaeancl the non-onagrads.This reportof pollinationby antlionsis the firstunambiguous such reportfor any memberof the orderNeuroptera. At least 5 species of antlionsvisit the flowersof Gaurasillosa, and Scotoleon minusculusis the most importantpollen-carrying species for this taxon. All visits by antlionsoccurred between :00 P.M. and 5:00 A.M., whichmay explain why this phenomenonhas not been reportedbefore. Keywords: antlions,Calylophus, Gaura, Onagraceae, pollination, Sphe{rodogastra. The plant familyOnagraceae provides an excel- between Caura and Stenosiphon7the latter clade lent model in which to studythe evolutionof pol- also supportedby Hoggardet al. (2004). However, linationsystems. Due largelyto the effortsof Raven Calylophusnow appearsto be moreclosely related (1979, 1988) and associates,detailed modern tax- to certainsections of Oenothera7and the Gaura+ onomicrevisions are availableor in preparationfor Stenosiphonclade to other sections of Oenothera. virtuallyall species of the family,as are detailed Additionalstudy is in progress,using additional comparativestudies of the morphologyand anatomy nuclearDNA sequencesand moreextensive sam- of pollen, stigmas,flowers, seeds, and otherrepro- pling within the tribe, since these initial findings ductivecharacters (reviewed in Raven,1979; fIoch challenge the classificationof the tribe that has et al., 1993). At least preliminarypollination data been in place for some 40 years (Raven, 1964, have been publishedfor many groups,especially 1979, 1988). Oenothera(Gregory, 1963, 1964, includingCaly- Caura(21 species; Raven& Gregory,1972a, b) lophus;Linsley et al., 1964), Camissonia(Linsley and Calylophus(6 species;Towner, 1977) bothoc- et al., 1963a, b, 1973; Raven, 1969), and (Clarkia cur primarilyin the southernplasns of the United (MacSwainet al., 1973) in the tribeOnagreae, and Statesand adjacentMexico, with tollcentrationsof Raven(1979) presenteda lucid overallsynthesis of taxa in westernTexas. Morphologi(al (Carr et al., the reproductivebiology of the family.Recent work 1990) and molecular(tIoggard et aI., 2004) phy- by Raguso and associates (Raguso& Pichersky, logeniesfor Gauraare available;those for Calylo- 1995; Raguso& Willis,2002; Levinet al., 2003a) phus are in progress.Both genera ale eharacterized has begunto documentadaptive changes in nectar, by a diversityof pollinationsysterlls. Five species floral morphology,visual display, and floral fra- of Cauraare reportedto be self-T)ollinating,and of grance associated with hawkmothpollination in the 16 outcrossingspecies, 13 ale pollinatedby Onagraceaeand otherfamilies, building in parton small moths,1 by hawkmoths,and 2 by bees, but- earlierstudies by Gregory(1963, 1964). terflies,and flies (Raven& Gregory,1972a; Raven, An understandingof relationshipswithin Ona- 1979). One species of Calylophu.sis reportedto be graceae (8 tribes, 17 genera,and about650 spe- autogamous?and of the five outcrossingspecies, cies; Raven, 1988; Levin et al., 2003b), which is three are visited by hawkmoths(one of these also essential to a comparativestudy of pollinationbi- by variousbees), andthe othertwo by bees, beetles, ology,is beginningto emerge,based on both mor- butterflies, and occasional hawkmoths(Towner, phological(Hoch et al., 1993) and molecularphy- 1977; Raven, 1979). The diversityof pollination logenetics (Crisci et al., 1990; Bult & Zimmer, syndromesfound in these generaprovides testable 1993; Contiet al., 1993;Levin et al., 2003b,2004). hypothesesregarding the evolutionof the species Of particularimportance to the presentstudy is the and their reproductivebiology. strong supportfor a terminalclade that includes Even in this comparativelywell-known tribe On- tribes Onagreae(8 genera)and Epilobieae(2 gen- agreae,much of the informationon pollinationsys- era;Conti et al., 1993; Levinet al., 2003b). Raven tems is descriptiveor anecdotaland oftenrests on (1964) suggestedthat Cauraand Calylophus7two insect pollinatorcollections from only one or a few generaof Onagreae,were closely relatedbased on short periods of observation.Few previousstud- similarities in stigma and anther morphology,a ies in this or most other groups have docu- view supportedby embryologicalstudies (Tobe& mented insect visitors to a plant species through Raven,1985). Recentphylogenetic analysis of On- the entire daily and seasonal cycles (Robertson, agreaebased on chloroplastand nuclearDNA se- 1928) nor have many tested the efficacyof those quences (Levinet al., 2003b, 2004) stronglysup- visitors as pollen vectors (Schemske& fIorvitz, portsa clade of Calylophus+ Oenothera7' Caurcl 1984). + Stenosiphon,and a close sister-taxonrelationship Our study exploits three featuresof Gauraand Volume 91, Number3 Clinebell et al. 371 2004 Pollination Ecology Figure1. Mapof southwesternTexas, U.S.A., with adja(ent se(tions of New Mexi(oand Mexi(o(Chihuahua and Coahuila),numbers 1-9 on maprefer to studysite lovalitiesdetailed in Table1. Calylophus the existence of a diversityof major bloomingspecies in Asteraceae,Loasaceae, and pollinators,the availabilityof sound taxonomies Papaveraceae,in the MonahansSandhills and sur- and testablephylogenetic hypotheses, and the oc- roundingareas in westernTexas (Fig. 1; Table 1, currenceof severalrelated plant taxa in a relatively withvoucher information). Two other species of On- restrictedgeographical area to facilitatethe gath- agreae, Oenotheraengelmannii and O. rhombipe- ering of comparativepollination data and the eco- tala, were presentat the site, but attractedfew in- evolutionaryinterpretation of these data. Our ap- sect visitors (based
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