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 (,TRIBE ONAGREAE)IN MIESTERN TEXASxU.S.A.1

A 13$'1'RACrr

This analysisreports 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 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() 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 ,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 ; 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 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 . 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,, , 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- , 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 on limited observations)and proach simultaneouslyconsiders the patterns of may be autogamous.Future papers in this series pollinatorvisitation of severaltaxa of Onagreae,as will include analysesof other communitiesin the well as that of the majorco-blooming taxa in other AmericanSouthwest rich in representationof spe- plant familiesthat growwith them.This approach cies of Onagreae,especially Gaura and Calylophus, providesdata for an entire pollinationcommunity, leadingultimately to an evolutionarysynthesis for which in turnwill facilitatecomparison with other the pollinationbiology of these groups.Our primary communities,for ourpurposes especially those with focushere is to describeand quantifythe pollinator similarclusters of Onagreae. guilds for a plant communityin the Monahans This paperconsiders the commurlitypollination Sandhillsthat includes a varietyof species of On- biologyof four commorlarld two uncommonsym- agraceae,as a step towardanalyzing the evolution patricspecies of Onagreaeand threeimportant co- of pollinatiorlbiology in Onagraceaetribe Ona- 372 Annals of the Missouri Botanical Garden

Table1. Localitiesincluded in this study.All sites are in Texas,U.S.A., locality numbers coincide with numbers on Figure1 and are referencedin the text and Tables4-10. Plant species studiedat each localityare notedwith vouchers,where available (all specimensdeposited at MOexcept as noted). are in familyOnagraceae, except as noted.

1. BrewsterCo.: outskirts of Alpine,2 June 1964 Gauracoccinea Pursh: Raven & Gregory19182 (CAS) 2. BrewsterCo.: 16.2 km W Marathonon TX Hwy.90, 22-28 May2000 Calylophushartwegii (Benth.) P. H. Ravensubsp. filifolius (Eastw.) Towner & P. H. Raven:Clinebell 2086 Gauracoccinea: Clinebell 2085 3. CraneCo.: 20.8 km E Monahanson TX Hwy.1053; 18 June 1966 Gauravillosa Torr. subsp. villosa: Gregory s.n. (RSA) 4. EctorCo.: 22.4 km E Monahanson US Hwy.I-20 frontageroad, 1-2 June 1964 Gauracoccinea: Raven & Gregory19234 G. villosasubsp. villosa: Raven & Gregory19235 5. EctorCo.: 17.2 km E Monahanson US Hwy.I-20 frontageroad: 28 May2000 Gauracoccinea: Clinebell, no voucher 6. Jeff Davis Co.:9.3 km & 30.4 km S Toyahvale,16 May1959 Gauracoccinea: Gregory 108-163 (RSA) 7. MidlandCo.: W end of Midland,1 June 1964 Gauravillosa subsp. villosa: Raven & Gregory19224 (RSA) 8. WardCo.: 10.7 km S Monahans,2 June 1964 Calylophushartwegii subsp. filifolius: Raven & Gregory,no voucher Gauracoccinea: Raven & Gregory19231 (CAS) 9. WardCo.: 2-14 km E Monahanson US Hwy.I-20 frontageroad; 7-12 Juneand 30 Aug-l Sep. 1999, 20-29 May 2000, S13 May2001 Calylophusberlandieri Spach subsp. berlanslieri: Clinebell 2034, 2096 C. hartwegiisubsp. filifolius: Clinebell 2093, 3066 Gauravillosa subsp. villosa: Clinebell 2032, 2036 G. coccinea:Clinebell, no voucher Oenotheraengelmannii (Small) Munz: Clinebell 2040, 3063 O. rhombipetalaNutt. ex Torr.& A. Gray:Clinebell 2031, 2041 Asteraceae: Thelespermamegapotamicum (Spreng.) Kuntze: Clinebell 2033 Loasaceae: Mentzeliastrictissima (Wooton & Standl.)J. Darl.:Clinebell 2039 Papaveraceae: Argemonepolyanthemos (Fedde) G. B. Ownbey:Clinebell 2037 greae.As an additionalfocus, ouranalysis address- sphingidmoths, which are both activeprimarily at es the debateregarding generalized versus special- dusk. Subsequentobservations revealed the impor- ized pollination,using the communitypollination tance of otherpollinator grou^)s that are activedur- ecologyof the Monahanssite. ing other times of the day an(l night. In orderto renderthe analysisrandom or unbiasedwith regard MATERIALSAND METHODS to time of day, recent fiel(lworkhas emphasized these other times of pollinatoractivity, with rela- The datapresented here utilizepollinator collec- tions madeby D. Breedlove,D. Gregory,P. Raven, tively less samplingfrom 7:00 P.M. to midnight. and H. Townerin 1959-1966 throughoutNorth Relativeamounts of time devotedto pollinatorcap- Americaon Gaura(Raven & Gregory,1972a, b) ture by time of day are presentedin Table2. and in the early 1970s on Calylophus(Towner, Withinany time period,we tried to randomize 1977). Manyof those results were reportedanec- samplingof floralvisitors in recentfieldwork. The dotally in those monographs.One of us (RC) ex- insect-capturetechnique employedmultiple nets tended these studies on both genera startingin and killing jars, each dedicatedto one plant spe- 1998. We have combinedthese data sets into sev- cies. The collector(s)alternated among the different eral biogeographicallymeaningful units (Table1), net-jarcombinations, which enabled moreor less of which the data set presentedhere is the first. continuouscollecting, avoided delays while the in- Mostof the earlierdata were collectedbetween sects wereasphyxiated in the jars, keptthe samples 7:00 P.M. and midnight,resulting in specimencol- collectedon each plant species separated,and re- lections strongly weighted toward noctuid and sulted in more equal samplingtimes amongplant Volume 91, Number3 Clinebell et al. 373 2004 Pollination Ecology

Table2. Cumulativehours spent collectingpollinators at each plant species by time periodand averagenumber of insects caughtper hourof observation.In somecases, we collectedinsects from more than one plantspecies during the sametime period,as explainedin the text.

Average # insects 12 A.M. 4 A.M. 8 A.M. 12 P.M. 4 P.M. 8 P.M. Total caught/ TO TO TO TO TO TO observation observation 4 A.M. 8 A.M. 12 P.M 4 P.M. 8 P.M. 12 A.M. hours hour Gauravillosa 8 15 9 3 9 20 64 8.6 Calylophusberlandieri 8 15 8 6 10 12 59 4.3 Gauracoccinea 2 2 14 18 13.2 Calylophushartwegii 1 2 9 12 6.5 ThelespernianiegapotaniicunI 1 3 4 9 1 18 3.1 Mentzeliastrictissinia 4 6 6 7 23 1.8 Argenionepolyanthenios 4 6 6 7 23 3.1 Oenotherarhonibipetala 6 6 Oenotheraengelniannii 2 5 2 2 11

Totals 16 42 39 15 44 78 EE = 234 species. A primaryset of insect specimenvouchers In additionto determiningoverall pollen load on is maintainedat the MissouriBotanical Garden, individualinsects, we tried to note the patternof with duplicate sets deposited at the California pollen depositionand specificallywhere on the in- Academyof Science,the Enns Museumat the Uni- sect body the pollen was found. Coupledwith ob- versityof Missouri,the Field Museum,the Smith- servationof insect behaviorin the course of floral sonianInstitution, and the SnowEntomological Mu- foraging,this patternmay provideuseful data re- seum at the Universityof Kansas.Clinebell visited gardingthe efficacyof the insect as a pollinator.In the Field and Snowmuseums to consulttheir col- all cases we recordedtotal pollen presenton cap- lections. turedinsects. Pollenload analysisinvolved bathing the insects In listing Lepidoptera(moths and butterflies)in in ethanol,or removingpollen from corbicularor our tables, we have followedmost standardrefer- scopal provisioningloads, and makingpermanent ences on North Americanmoths (Covell, 1984; slides stainedwith basic fuchsin (Calberla'ssolu- Holland,1968), while acknowledgingthat the ac- tion; Clinebell & Bernhardt,1998). Pollen loads cepted higherclassification of somegroups such as were then identifiedwith the aid of a pollen refer- the Catocalinaehas been modifiedquite substan- ence library(at MO),consisting of similarlypre- tially (Poole, 1989). Accordingto Hepner's(1998) paredslides for each of the plantspecies blooming classificationof Lepidoptera,all of the moths we at the site. Pollen of Onagraceaeis highlydistinc- encounteredbelong to suborderGlossata, cohort tive due to its shape, "paracrystallinebeaded" ek- Myoglossata,division .Within this group, texine, and viscin threads(Raven, 1988; Hoch et all except the Pyralidae(sect. Tineina)belong to al., 1993), and even in mixedpollen loads we were sectionCossina, subsection Bombycina. McGinley's able to distinguishamong specific taxa of Calylo- (2003) recentmonograph of the halictidbee phusn Gaur^ and Oerlotherausing pollen size, Sphecodogasleraproved most useful for that group, shape, and aperturaloutline, as describedby Prag- as did Penny et al. (1997) for the Neuropterain lowski et al. (1987, 1988). In orderto simplifythe our sample.Determinations for most insect groups tablesand facilitate comparisons among individuals were providedor checked by authoritiesas listed and sites, we groupedpollen loads into five size in the acknowledgments. classes, with the largest being simply "> 500 The collectionprotocol, large samplesizes, and grains."In orderto calculatetotal amountsof pol- pollenload analysisare intendedto ensurethat our len carriedby species and overall, we used the methodswill include the majorpollen carriersfor mean of each size class (i.e., 1-10 grains-mean each species of plant studied.This in turnenables 5; 11-50-mean 30; 51-100-mean 75; 101- accuratedelimitation of both similaritiesand dif- 500-mean 300; and > 500-estimate 500), mul- ferencesin the pollinatorguilds servingeach plant tiplied times the numberof individualsin that species. When sufficientdata were available,we class. tested the statistical significance of pollinator 374 Annais of the Missouri Botanical Garden

Table3. Selectedfloral c,haracters relaited to pollinationbiology for species of Onagraceaein this analysisSmea- surements(mm) listed are the lnean of measurementslnade on five individualsfroln the primarystudy population. A/Ieasurementsin parentheses are from descriptions provided in revi,sionsfor CaZylophus(Towner, 1977) Gamra(Raven & Gregory,1972a) and Oenothera(Dietrich & Wagner,1988).

Floraltube Dlstance Lengthof frolnthroat Distance eylindrical Lengthof Diameter to longer fromthroat Tason part flaringapex at throat anthers to stigma Petal length CXalyloph7lsberlandieri 4.8 5.6 7.0 7.B 8.2 15.2 (3-11) (2-9) (3-14) (2-11) (4-10) (6-25) Cl(llylophushartwegii 19.2 11.6 5.5 7.6 12.8 12.6 (11-33) (5-17) (4914) (6-13) (8-12) (12-23) Ca7lrac0ce7irzea 5.0 N/A 2.3 5.0 7.0 5.0 (4-11) - (3-7) (S10) (3A3 Gauravillosa 2.4 N/A 2.0 6.9 8.1 4.3 (1.55) _ (4-11) (7-13) (7-13) Oenotherarhonibipetala 29.0 N/A 5.0 15.0 25.0 20.0 (30-45) - (13-23) (15-25) (15-35) ehoice using Chi-squaretest for independence gapotanicalnt?but due to their extremelyfast and (Conover,1980), wheresimilar pollinators seemed unpredictableflighte they are almostimpossible to to be choosingdifferent onagrads to visit in their catch in the act of foraging,and few were actually foragingactivities. The null hypothesispredicts eapturedon flowers.On severaloccasins, however that insect groups should visit different plants largenumbers of these beeflieswere cl)tured when equallyduring their respectivetimes of -vis- they landedon nets clothing?and skil apparently

. . . . lhng actlvlty. attractedby a concentrationof onagltltlsecondary Behavioralobservations are necessaryto sepa- compounds.Most of these insects carriedeither ratethose carriersof pollenthat might be expected Calylophusor Thelespernzapollen, a11(lwere as- to effectpollination from those that do not. In terms signedto these respectivespecies in the tables.The of logistics, it is difficultto collect and observesi- few beefliesthat lacked pollenloads }lavebeen as- multaneously.While our characterizationof the signed to Calylophusnsince they atTear to have pollinatorguilds is quantitativeSour behavioralob- been attractedby volatilesof that speeies. In gen- servationsare, by their nature qualitative.Behar- eral,it is ourassumption that baiting i*; a legitimate ioral observationsoften are sufficientto separate partof scientificsampling, especially fol document- pollinatorsfrom non-pollinators,but may not be ing relativeabundances of sucha divelsecommunity sufficientto evaluatethe relativeefficacies of var- of floralvisitors as reportedhere. (3) Whereasfive ious pollinators.We tried to combinecollection and species of antliorzswere capturedon (>aura1villos observationat all studysites. flowers,the only two malesof Brachyllemmra.shub- One challengein this studyis that all groupsof bardiwere collected at the car dome light. How- insect visitorsare not equallylikely to be captured. ever both carried Gamrapollen, so we included In three instances,our field activitiesunwittingly them in our analysis even though they were not baitedinsects that are includedin ourdata. (1) The caughtactually visiting flowers. (?nagrad(?ligolege Sphecodogastra noctiraga is largely nocturnalon CamraWIllosaS and because FLORAIj FEATURES AND PHENOLOGY these bees are small and hardto see at night?most were capturedsecondarily in net sweepsfor moths. Table3 summarizesfloral measurements of par- HcxweverGregory collected a large set of this spe- ticularrelevance to pollinationfor the taxa of On- cies (includingmany females carrying onagrad pol- agraceaein this analysis withmean measurements len) underthe dome light of his car while parked fromour study populations as well as overallranges at a GamrariZlosa colony in the MonahansSand- of measurementsfor the species. Five taxa (both hillseand we have includedthese datain our anal- species of GaUra? Calylophmsberlandieri? Argemone ysis. (2) Colorful orangeand black beeflies (Poe- polyanthemos? and Mentzeliastrictissima) were in cilanthraxeffrenms) are regulardiurnal visitors to full bloomfrom early May through early SeptemberS both Calylophmsberlandieri and Thelespermame- while only a few flowerswere present on Theles- - *:Ai*S -

Volume 91, Number 3 Clinebell et al. 375 2004 Pollination Ecology

Figure2. Habitatin MonahansSandhills, Ward Co., Texas(site 9, Table1); typicaldune vegetation;1 Sep. 1999 (photoby D. Hardin). permamegapotamicum in late Augustthrough early Monahansdunefields throughabout 250 km of September.Both species of Oenotherawere in southeasternNew Mexico,and rangefrom 20 to 60 bloomon only one of the fourfield tripsto the site km across, from east to west. Their formationis made by Clinebell:Oenothera engelmannii was in associatedwith paleowindsfrom the northwestand full bloomin earlyMay 2001, and O. rhombipetala the arid conditionsthat accompaniedthe close of only in earlyJune 1999. the mostrecent ice age (Machenberg,1984). The preservationof a sectionof the sandhillsfor- STUDY AREAS mation stems from the publicationof Bedichek's All of our study sites are located in an area (1947) Adventureswith a TexasNaturalist, which boundedroughly by 30.2-32.1°N, 102-103.8°W,in inspiredlocal supportfor protectionbeginning in Brewster,Crane, Ector, Jeff Davis, Midland,and 1957. Today,1554 hectaresof the sandhillshave WardCounties of southwesternTexas, U.S.A. (Table been preservedas MonahansSandhills State Park 1; Fig. 1). Ourprimary sites occurwithin the Mon- (WardCo., Texas),which featuresboth active and ahansSandhills eco-geographic region (Fig. 2); the stabilizeddunes. This park,located about 8 km to other sites are located in the adjacentTranspecos the west of Monahansbordering U.S. Highway region(between the Pecos and Rio GrandeRivers). I-20, and its immediatesurroundings served as our Elevationsof these sites rangefrom about 800 to primarystudy site (site 9, 'rable1; Fig. 2). Because 1400 m. the parkis closed at nightwhen many onagrad pol- The MonahansSandhills are a youngfeature of linatorsare active, our study areas were adjacent the Pecos Plain (about16,000 years old; Machen- to the parkalong the frontageroads on both sides berg, 1984), borderingthe CaprockEscarpment of I-20. These areas contain many fine coppice alongthe westernborder of the LlanoEstacado, or dunes, which are stabilizedby the miniatureshin southernhigh plains of south-centralNorth Amer- oak (Quercushavardii Rydb.). Other woody plants ica. The sandhillsformation extends along this es- commonlyencountered include honey mesquite carpment,which trappedthe sand on its leeward (Prosopisglandulosa Torr.) and desertwillow (Chil- side, about50 to 100 km east of the Pecos River. opsis linearis(Cav.) Sweet). Major grasses include The dune formationsextend northwesterly from the xeric species of Andropogon,Calamovilfa, Eragros- 376 Annals of the Missouri Botanical Garden

tis, and Panicum;cacti and Yuccaare also abun- derwingsubfamily, Catocalinae). A collectionof 46 dant(Machenberg, 1984). Embeddedin this matrix pollinatorsmade at site 9 on 30 Aug.-l Sep. 1999 is a rich diversityof forbs, of which the species is combinedwith datafrom May to June,since the studied are the most abundantfrom late May to two data sets include comparablegroups of polli- early September.Nearby secondarystudy areas nators.We collectedadditional pollinators at site 9 (sites 3-5, 7-8) are similar. on S13 May 2001. Extremedrought marked the On a map,the dunalareas appear as islandson years 1999 and 2000, whereasthe winterof 2001 the Pecos plains. In the dunal areas themselves, was very wet, producingremarkable flowering dis- species of Onagraceaecommonly encountered in- plays throughoutwestern Texas. clude Calylophusberlandieria Gaura villosa, and As summarizedin Table4, we captureda total Oenotherarhombipetala. On interdunalsites, the of 562 insect visitorsbelonging to 45 species on commononagrads are Calylophushartwegii, Gaura Gauravillosa. In termsof individualvisits, the 27 coccinea,and G. villosa. species of Lepidopteraaccount for a majority(353 The sites in TranspecosTexas (sites 1, 2, 6 in visits; 63Woof the total)followed by the 6 species Brewsterand Jeff Davis Counties,about 100 km of Neuroptera(128; 23Wo),and the 7 speeies of Hy- southwestof the MonahansSandhills) include more menoptera(68; 12Wo);visits by Coleoptera(3 spe- arborescentelements of mesquitesavanna, and are cies) and Diptera(2 species),mostly without pollen, rich in Gauracoccinea and Calylophushartwegii. are negligible.The mostnumerous visitors by spe- Here,the onagradspecies typicalof the duneswere cies are the noctuid Bulia deducta (253; absent. Overall,the mosaiccharacter of the sand- 45Wo),the antlionScotoleon minusculus (104; 18Wo), hill belt is such that it is not unusualto find these the noctuidMelipotis indomita (46; 8Wo),and 2 spe- key onagradsin variousrandom subsets, depending cies of the halictid bee Sphecodogastr(l(each 27; upon local variationin substrates.Additional spe- 5Wo).We estimate that these 562 indivi(lualscarried cies of Onagreaeare present in southwesternTexas, some 32,705 pollen grains.In termsof pollen car- but we believethat the ones chosenfor this analysis ried, the importanceof the Lepidopterais dimin- representa majorityof the pollinationsyn(lromes ished relativeto the othertwo groups:Neuroptera of Onagreaethat occur in the Transpecosan(l Perm- account for gross pollen load of 20,045 grains ian Basin (areato the east of the Pecos River,and (61Wo),Hymenoptera for 8720 (27Wo),and Lepidop- of which the sandhillsare a part). tera for on]y 4035 (12Wo).The species that cumu- lativelycarry the largestpollen la(ls are the ant- RESIJLTS lion Scotoleonminusculus (18,160 grains;55Wo) the halictidbee Sphecodogastradanforthi (4345 grains; Insect visitorswere collected throughout the day 13Wo),the noctuid moth Bulia (Ze(lucta(2130 and night from nine species of plants in south- grains; 6Wo),the bee Sphecodogastr(lnoctivaga westernTexas, includingsix species of Onagreae (1755 grains;5Wo), and the introduce(lhoney bee (Tables1, 2). We presentdata on Onagraceaefirst, Apismellifera (1500 grains;5Wo). So althoughnoc- followedly otherfamilies, and withinOnagraceae tuid mothscollectively appear to be importantpol- list species in orderof decreasingsize of visitor linatorsof Gauravillosa, the antlionScotoleon and samples. the twospecies of Sphecodogastrabees are the ma- jor pollen carriersfor this species, responsiblefor GAlJRAVILLOSA TORR. SUBSP. VILLOSA nearlythree-quarters of the totalpollen load in this Gregorystudied this self-incompatibleperennial analysis. species in the sandhills region (sites 4 and 7 in The activityof these majorpollinators spans the June 1964 and site 3 in June 1966). His collec- entire time of day and night duringwhich Gaura tions, madebetween about 8:00 P.M.and midnight, villosa flowerswere open. In the 1960s, Gregory are included with Clinebell'sdata from site 9 in began collectingpollinators as early as 7:45 P.M. 1999-2001, whichwere recorded in additionaldis- and ceased sampling around midnight. In the crete time intervals.Almost every moth collected droughtyears of 1999 and2000, the flowersopened at site 4 on 2 June 1964 containedGaura pollen later,after 10:00 P.M. In May2000, we clockedthe on the proboscis,whereas a similar collectionof openingof the firstflowers at 10:35 P.M. The flow- mothsmade at site 7 on 1 June 1964 less than50 ers, which last only one day, then remainedopen km awaycontained almost no Gaurapollen; these for several hours after sunrise (a few as late as latter accountfor manyof the "no Gaurapollen" 10:00 A.M.). individualsof the twomost abundant noctuid moth Most of the insects collected from anthesisto foragers,Bulia deductaand indomita (un- midnightwere noctuidmoths in the subfamilyCa- Volume 91, Number 3 Clinebell et al. 2004 Pollination Ecology 377

tocalinae,especially Bulia deductaand Melipotis accountsfor almosthalf of the sampleof pollinators indomita.In the droughtyears, these were joined (Table5). In earlymorning, but continuingthrough- aroundmidnight by a varietyof wingedadult ant- out the day,pollen-eating beetles visit the flowers; lions, especiallyScotoleon minusculus (of bothsex- the most commonbeetles are the buprestidAch- es), but also includingfour other species of ant- maeoderamixta and the chrysomelidgenus Altica lions. In the non-droughtyear of 2001, Gaura (Alticasp. indet.). As the day progressed,beeflies villosa flowersopened about9:00 P.M., and moths in five generaof Bombylidae,especially Heterosty- and antlions were encounteredforaging together lum robustumand Poecilanthraxefenats, visited from9:30 P.M. until morning.Throughout the night, the flowers.Two large anthophorid bees, in the gen- onagradoligoleges in the sweat bee familyHalic- era Centrisand Diadasia, visited rarely; only a sin- tidae (Sphecodogastranoctivaga, both sexes) were gle individualof each was collected.In early May also collected, mostly in sweeps for moths. After 2001, the halictid bee Sphecodogastradanforthi sunrise,another halictid oligolege, Sphecodogastra was infrequent,and the majorearly morningpol- danforthi,actively foragedfor pollen on both the linator was the bombyliidbeefly Poecilognathus Gauraand nearby Calylophus berlandieri. This spe- scolopax. cies was collected at Gauraflowers in both May- Werecorded 252 individualsrepresenting 27 in- Juneand August-Septemberobservational periods, sect species visitingthe flowersof Calylophatsber- and sometimescarried mixed loads of Gauraand landieri,and carryinga total pollen load of 52,010 Calylophuspollen. Sphecodogastradanforthi re- grains (Table 5). In order, the most important mainedactive until about9:30 A.M. Anotherhal- groupsare as follows:Hymenoptera (7 species, 106 ictid bee and onagradoligolege, Evylaeus sp. 1, was individuals(42Wo), carrying 44,240 grains(85Wo)); also collectedin the morningon Gaura.While this Coleoptera(10 species, 80 individuals(32Wo), car- species is not abundantin this data set, it is well rying4650 grains(9Wo)); Diptera (5 species, 60 in- representedin anothercollection made at the Ki- dividuals(24Wo), carrying 2940 grains (6Wo));and owa NationalGrassland (Union County, New Mex- the Lepidopteraand Neuroptera,both of negligible ico, U.S.A.) in July 1999 (Clinebell,unpublished importanceas visitors and carriers.The halictid data),where Sphecodogastr(l d(leforthi was not col- bee S3heco(X0gastr(ldanforthi, which is also a sig- lected. nificantpollen carrierof Gauravillosfl (Table4), Linsleyand MacSwain(1962) reportedSpheco- accountsfor 40Wo of the individualvisits, butnearly dogastratexana and S. noctivag(las geographical 83Woof the cumulativepollen load of Calylophus replacements,with S. texan(loecurring largely to berlandieri.Several other species of beetles, bee- the east of the MonahansSan(lhills and S. nocti- flies, and largerbees are significantvisitors to this vaga to the west. Those authorsreported the two plant,but none of them carrymore than 5Woof the species as sympatricfrom the sandhillsalone, but total pollen load recorded.Because of the slight all specimensin ourcollection key to S. noctivaga. herkogamyof the flowersof this species, virtually Ecologically,these two species are similar and all floralvisitors are true pollinators,regardless of uniquewithin Sphecodogastra in that they are the whetherthey are visitingthe flowersfor pollen, for only knownnocturnal species in the genus, which nectar,or for both. Seasonalvariation in the polli- is otherwisecrepuscular or matinal;this includes natorguild appearsminimal in our data set. Town- S. danforthiin our analysis. er's (1977) list of floralvisitors in PotterCo., Texas, is a qualitativesubset of our collection. CALYLOPHUSBEALANDIERI SPACH SUBSP. BERLANDIERI GAURACOCCINEA PURSH Like Gauravillosa, this self-incompatibleona- gradtaxon has a long bloomingperiod from March Both Gregoryand Clinebellstudied this self-in- to Septemberthroughout Texas, western Oklahoma, compatiblespecies in boththe MonahansSandhills and adjacent regions (Towner,1977). Clinebell (sites 4 and 8 and sites 5 and 9, respectively)and studiedthis species in Juneand August-September in mesquitesavanna (sites 1 and 6 and site 2, re- 1999, May2000, and May2001 at the Monahans spectively)in TranspecosTexas (Table 1). In 1964 Sandhills(site 9, Table 1). All study populations and 1959, Gregorycommenced collecting moths at grewintermixed with Gaura villosa. Anthesis of this about 7:00 P.M., whereasin the droughtyear of species occurs shortly before sunrise (Towner, 2000 the flowersopened later, between9:00 and 1977) when the halictid bee Sphecodogastradan- 9:30 P.M. This patternof delayedanthesis is similar forthi begins to forage.This bee species remains to the patternreported above for Gauravillosa in active only fromsunrise until about9:30 A.M., but the droughtyears of 1999 and 2000. At sites 5 and 378 Annals of the Missouri Botanical Garden

Talgle4. Floralforagers on Gauravillosa subsp.villosa in the PermianBasin (Texas,U.S.A.: see Talgle1 for site data);pooled data from1-2 June 1964 (sites 4, 7); 18 June 1966 (site 3); 7-12 June, 30 Aug.-l Sep. 1999, 20-29 May2000, and 6-13 May2001 (site 9). Legend:F = female,M = male;W = worker;a = Argernonepolyanthernos; b = Mentzeliastrictissirna; c = Calylophusberlandieri; d = Asclepiassp. pollinia.

11 to 51 to 101 to No. 1 to 10 50 100 500 >500 Other Gaura Gaura Gaura Gaura Gaura Gaura pollen pollen grains grains grains grains grains carried Totals Coleoptera Cantharidae Chauliognathussp. 1 1 Chrysomelidae Alticasp. indet. 1 1 8 Diabroticaundecirnpunctata Mann. l 1 Diptera Bomlgyliidae Poecilanthraxeffrenus (Coquillett); M Tachinidaesp. indet. 1 l l Hymenoptera Andrenidae Perditasp. indet 1; F 1 1 Apidae Apisrnellifera L.; W 3 3 Halictidae Agaposternonangelicus Cockerell; F 1 Agaposternonsplendens (Lepel.)¢ F Evylaeussp. 1; F l 1 2 a(l), 1)(1) 5 Evylaeussp. 1; M 3 3 Sphecodogastranoctivaga (Linsley & MacSwain);F 13 1 5 2 2 23 Sphecodogastranoctivaga (Linsley & MacSwain);M 4 4 Sphecodogastradanforthi McGinley; F 5 2 2 1 4 6 b(1), c(l) 20 Sphecodogastradanforthi McGinleyX M 6 1 7 Lepidoptera Butterflies Pieridae Nathalisiole; M 2 2 Moths Arctiidaesp. indet. 1 1 Geometridae Serniothisapunctilineata (Packard) Geometridsp. indet. 1 l 1 2

. . Acontllnae Acontiaaprica (Hulgner) 2 2 Amphipyrinae Cosrniacalarni (Harvey) 1 1 Catocalinae Bulia deducta(Morr.) 155 54 37 6 d(3) 253 Caenurginaerechtea (Cram.) Melipotisindornita Wlk. 24 12 4 4 2 46 Melipotisjucunda Hulgner 2 1 Synedahowlandi Grote; M l Hadeninae Pseudaletiaunipunctata (Haw.) 1 I Volume 91, Number 3 Clinebell et al. 379 2004 Pollination Ecology

Talgle4. Continued.

11 to 51 to 101 to No. 1 to 10 50 100 500 >500 Other Gaura Gaura Gaura Gaura Gaura Gaura pollen pollen grains grains grains grains grains e arried Totals Helico1eerpazea (Boddie) 2 3 5 Schiniagaurae (J. E. Smith);M 1 1 2 lfoctuinae Agrotismalefida Guenee 6 1 1 8 Feltiavolubilis Harvey 1 Plusiinae Trichop67asiani (Hbn.) 1 noctuidsp. indet. 1 (small,white) moctuidsp. Indet.(12 mm,mottled brown) 2 noctuidsp. indet.(15 mm,mottled brown) 1 l noctuidsp. indet. (12 mm,light tan) 1 Pyralidae Achyrarantalis (Guenee) 8 2 10 Nomophilanearctica Monroe Sphingidae Hyleslineata L. 1 mothsp. indet. (lightbrown) 4 4 mothsp. indet. (small,cream) 1 mothsp. indet. (small,tan) 1 Neuroptera Chrysopiclae la(ewing sp. indet. 1 1 2 Myrmeleontidae Brachynemurushubl)(lr(Xi; M I 2 4

Brachyltemurus hublvar(li; ' 2 I I 5 Paranthaclisishageni; ' 3 3 2 8 Parcanth(lelisishageni; M l Scotoleoltminusculu.s N. Banks;F 1 4 8 7 61 10 3l_ Scotoleo71minusculus N. Banks;M 2 3 7 43 ll 10 Vellafallans; M (60 mm) 1 1 antlionsp. indet. 1; M (40 rrlm) 1 1

Totals 262 101 85 38 56 20 = 562

9, Clinebellcollected early morningbees on this pollen load. The noctuidmoth Bulia deductawas species that are similarat least at the familylevel marginallythe most importantspecies in termsof to those collected in the llanos of San Luis Potosi, individuals (57, 24%) and pollen carried (830 Mexico,by Breedlove(collections at the Missouri grains, 17%),but at least four othermoth species BotanicalGarden, analyzed by Clinebell),and dis- (Melipotisindomita, M. jucunda, Discestratrifolii, similarto morningbees collectedon G. villosaand and an undeterminedspecies) carried nearly as Calylophusberlandieri as discussedpreviously. much pollen (Table6). The 238 individualscollected on Gauracoccinea The noctuidmoths Bulia deductaand Melipotis represent34 species of insects (Table6), and they indomitaare majorfloral visitors to bothGaura coc- carrya cumulativepollen load of 4945 grains.A1- cinea and G. villosa,but G. coccineaalso attractsa thoughColeoptera, Diptera, and Hymenopterawere widerarray of othersmall noctuidsand geometers present, all were negligible in importancecom- in the first two hours after anthesis (Table6). We pared with the Lepidoptera,especially geometrid have not yet studiedGaura coccinea between mid- and noctuidmoths, which account cumulatively for night and sunrise, so we do not know if antlions 86t3toof the individualvisits and 99t3toof the gross play a role in its pollination.A numberof bees that - 252

380 Annals of the Missouri Botanical Garden

Table5. Floralforagers on Calylophusberlandieri subsp. berlandiereiin the MonahansSandhills (Texas, U.S.A.: site 9, Table1); pooleddata from 7-12 June, 30 Aug.-1 Sep. 1999, 2s29 May2000, and S13 May2001. Legend: F = female;M = male;a = Thelespermamegapotamicum; b = Mentzeliastrictissima, c = Mimosaquadrivalvis var. Occidentalis; d = Gauravillosa; e = Argemonepolyanthemos. Counts designated with an asterisk(8) are fromslides made to quantifyproportions of mixed loads of Calylophusand Gaurapollen. Specimensoften carriedmuch larger loads (> 1000 grains)of Calylophuspollen.

1 to 11 to 51 to 101 to lfo 10 50 100 500 >500 Other Caly. Caly. Caly. Caly. Caly. Caly. pollens pollen grainsgrains grainsgrains grains carried Totals Coleoptera Buprestidae Achmaeoderamixta 1 4 2 a(2) 13

Cantharidae 6 Chauliognathussp. indet. 1 Chrysomelidae Alticasp. indet. 1 15 12 4 3 b(2) 50 Cleridae 16 Trichodesoresterus Wolcott a(2) 2 Coccinellidae lady beetle sp. indet. 1 Meloidae Eupomphaviridis (Horn) 2 1 1 4 Scarabaeidae Anomalasp. indet. 1 Euphoriasp. indet. 1 (blackand yellow) 1 beetle sp. indet. 1 (black,4 mm) 2 4 6 beetle sp. indet.2 (orange-brown,5 mm) 1 Diptera Bombyliidae Anastoechussp indet.,M Exoprosopasp. indet. 3 a(2) 1 5 Heterostylumrobustum (Osten Sacken); F 3 3 Poecilanthraxegrenus (Coq.) 6 10 9 a(8) 9 Poecilognathusscolopax (Osten Sacken) 4 5 6 6 25 Hymenoptera 22 Anthophoridae Centriscaesalpiniae Clell.; F 1 b(l) Diadasiarinconis; M b(l) Apidae Bombuspennsylvanicus (DeGeer); W C(1) Halictidae 1 Evylaeussp. indet. 1 Sphecodogastradanforthi McGinley; F 95 Sphecodogastradanforthi McGinley; M 2 2 d(l3) 4 808 Sphecodogastralusoria (Cresson); F 2 4 108 2 rnllpnllclae 1 *- 1 Tiphias p. indet. 1; F b(l) Lepidoptera Danaidae Danausgilippus (Cramer); F Hesperiidae e(l) Lerodeaeufola (W. H. Edwards) l ll T . I Lyeaenldae lyeaenidsp. indet 1 Noctuidae Plusiinae Autographabiloba (Stephens) Pieridae Nathalisiole; M Neuroptera Myrmeleontidae ScotoleonminuXsculus N. Banks; F Totals 45 37 45 17 24 84 Volume 91, Number 3 Clinebell et al. 2004 Pollination Ecology 381

are otherwiserare in our data set visit this species like C. berlandierior C. tubicula(Towner, 1977), in the early morning,but most of these bees, in- presenceof honeybeesnegatively impacts the na- cluding the anthophoridMartinapis enteicornis tive bees. At a populationof C. tubiculain Brewster (bothsexes) and the halictidAgapostemon angeli- County,Texas, near Big Bend NationalPark? hon- cus (malesonly), carrylittle or no pollen. Consid- eybees were the majorvisitor and pollen carrier, ering the relativelyhigh numberof insect visitors competitivelyexcluding the native bees that are to this species, the total pollen load identifiedis presentand presumablyare the originalpollinators considerablysmaller than those for other species of (Clinebell, unpublished data; see also Towner, Onagraceaein this analysis.It is unclearif we have 1977). We interpretthe lack of noctuidmoth visi- missedone or moremajor pollen carriers,or if this tation on C. hartwegiiat Monahansto the abun- species relies moreheavily on insect visitorslike dance at the site of Gauravillosa, a preferrednoc- noctuidmoths or smallbees thatindividually carry tuid nectar resource.By contrast,at the Brewster small pollen loads but that are present in large Countysite, therewere few G. coccineaplants ver- numbers. sus many C. hartwegiiplants, renderingany re- sourcepartitioning between the noctuidand sphin- CALYLOPHUSHARTWEGII (HENTH.) P. tI. RAVEN SUBSP. gid mothsbioenergetically untenable.

FILIFOLIUS(EASTW.) TOWNER & P. H. RAVEN As summarizedin Table 7, 77 individualsrep- resenting13 species were capturedon Calylophus Just as we oftenencountered Calylophus berlan- hartwegii,carrying a total of 11,665 pollen grains. dieri and Gauravillosa togetheron the sandiest Lepidopteraaccount for mostof the individualsre- sites, we also notedan associationbetween C. hart- corded(50, 65%), comparedto Hymenoptera(23, wegii and G. coccineaon firmersubstrates. Gregory 30t3to),with Coleopteraand Neuropterapresent, but studiedthe self-incompatibleC. hartwegiiat site 8 of negligible significance.However, Hymenoptera in the Monahansarea; Clinebell studied it at both carry a majorityof the pollen load (7530 grains? Monahans(site 9) and in the Transpecosarea (site 65%), compared to Lepidoptera(4130 grains, 2). This species seems to be particularlynegatively 35t3to).The sphingidmoth Hyles is the mostcommon impactedby drought;at site 9 it bloomedabun- visitor (27 individuals,35%; with 3535 grains, dantlyin 2001, but was not even observedin the 30%), especially at Monahans(site 9), but overall droughtyears of 1999 and 2()()().At site 2 in the carries 1ess pollen than the introtlucedhoneybee droughtyear of 2000! it did bloom, but the first A,vis(18, 23%;with 5500 grains,47%), which oc- flowersdid not open until 8:00 l.M., at least a half c urs only at site 2. The next mostabundant visitors an hour later than the same plants in the mesic are noctuid mothsBulia (7 individuals,9%) and year of 2001. Meli/)otis(5, 6%) and the nativehalictid bee Sphe- Duringeach eveningof observation,anthesis in codogastradanforthi (5, 6%),but in termsof pollen Calylophushartwegii set off a "rush"of activityby loads, the latter carries significantlymore pollen sphinx moths.The first sphingidmoths (Hylesli- (2030 grains, 17%) than the noctuids (both 140 neata) appearedat 8:15 P.1\1.,and the last at 9:20 grains, 1%). In fact, the single individualof the P.1\1.We also collectedthe largenoctuid moths Bu- large sphingid moth (Manducaquinquemaculata) lia and Melipotishere, but they were notablyless encounteredcarried more pollen (300 grains,3%) abundanton Calylophusthan on (;auraat the same than all of the noctuidmoths combined. It appears sites. At site 2, abouta thirdof the 54 floralvisitors that all of the Hymenopterareported on C. hartwe- wereworker honeybees (Apis mellifera), which were gii are pollen robbersrather than pollinators,as otherwiseuncommon in the data set. By compari- they do not contactthe stigmasduring their forag- son, honeybees(and noctuidmoths) did not visit ing, whereasthe sphingidmoths always made con- this taxonat Monahans(site 9). This underscoresa tact. Similarlynthe noctuidsalso appearto be large- great problemfor studentsof southwesternpolli- ly nectar robbers.Thus, only the sphingidmoths nation biology:where feral honeybeesare abun- were effectivepollinators, due to the extremeher- dant,their presence may affect adversely the activ- kogamyof the flowers. ities of nativeinsects (Primack& Silander,1975). Most of the pollen of CalylophushartwegiiS a The presenceof honeybeesmay be less of a prob- self-incompatiblespecies, was movedby sphingid lem in the case of sphingidmoth-pollinated species moths (Hyles lineata) at Monahans,and at other like CalylophushartwegiiS where honeybees and sites by sphingids and honeybees, with smaller sphingidmoths co-forage in apparentharmony, pos- amountsof pollencarried by the noctuidmoths Bu- sibly by partitioningnectar versus pollen resources. lia deductaand Melipotisindomita (Table 7). Greg- However,in the case of diurnalbee-pollinated taxa ory (1964) also studied this taxon (as Oenothera 382 Annals of the MissouriBotanical Garden

Table6. Floralforagers on Gauracoccinea from sites in Texas,U.S.A. (see Table1 for site data);pooled data from 7 and 16 May 1959 (site 6); 1-2 June 1964 (sites 1, 4, 8); and 22-28 May2000 (site 9). Legend:a = Dalea sp.; b = Mimosaquadrivalvis var. occidentalis; c = Aselepiassp. pollinia.

11 to 51 to 101 to No 1 to 10 50 100 500 >500 Other Gaura Gaura Caura Gczura Gaura Gczura pollens pollen pollen pollen pollen pollen pollen carried Totals Coleoptera Buprestidae Achmaeoderamixta 1 a 1 Chrysomelidae Alticasp. indet. 1 7 4 (Cleridae ll 'I'richodesoresteres Wolcott 1 1 Diptera Bombyliidae Poecilognathalsscolopax (Osten Saeken) 4 4 Hymelloptera Anthophoridae Martinapisenteicornis (Clell.); F 1 1 Martinapisenteicornis (Clell.); M 2 3 1 a(5), b(l) 6 Halictidae Agapostemonangelicus Cockerell; M 7 3 10 Lepidoptera Moths Geometridae Semiothisasp. indet. 1 (small,tan) 14 19 9 5 47 Scotograrnmainfuscata Smith 1 1 geometridsp. indet. 1 (18 mm,brown) 1 1 1 3 Noctuidae Acontiinae Acontiaaprica (Hubner) 1 Acontiasp. indet. 1 (5 mmSbrown) 6 1 Acontiasp. indet.2 (8 mm,black 2 & tan) Cobubathaorthozona (Hampton) 1 1 Catocalinae Bulia deducta(Morr.) 29 13 13 1 1 c(2) 57 Matigrammarubrosuffzusa Grote 2 2 Melipotisindomita Wlk. 3 22 16 Melipotisjucunda Hubner 1 1 1 9 Hadeninae 6 DiscestratrifolEi (Hufnagel) 1 Leucaniasp. indet. 1 1 1 2 hadeninidsp. indet.(15 mm,with 1 brownreticulations) Heliothinae Helicoverpazea (Boddie) 2 4 4 2 12 Schiniacitrinella 1 1 2 Noctuinae Agrotismalef da Guenee l noctuinidsp. indet. 1 Plusiinae Rachiplusiaou (Guenee) 1 1 mothsp. indet. 1 (small,tan) 1 1 2 mothsp. indet.2 (small,brown) 1 1 mothsp. indet.3 (small,tan with brown 7 4 2 1 2 16 markings) Volume 91, Number 3 Clinebell et al. 383 2004 Pollination Ecology

Table6. Continued.

11 to 51 to 101 to No 1 to 10 50 100 500 >500 Other Gaura Gaura Gaura Gaura Gaura Gaura pollens pollen pollen pollen pollen pollen pollen carried Totals mothsp. indet. 4 (13 mm,dark brown) 1 1 2 Pyralidae Pyraustinae Pyraustinaesp. indet. 1 1 1 Diatsictisfracturalis (Zeller) 3 3 Epipagishuronalis (Guenee) 2 1 1 4 pyralidsp. indet. 1 (13 mm,reddish) 1 1 Sphingidae Hyleslineata L. 1 1

Totals 94 64 60 15 4 1 EE = 238

hartwegii)in the Monahansarea. He describedvis- abundantly.In the course of several hours of ob- itationby large bees in Melissodes(Anthophoridae) servationin early morningand early evening,few and Megachile(Megachilidae) in the hour before insects visited its flowers.Additional fieldwork is sunset, and anecdotallyascribed to bees the ma- needed for this species. jority of the pollen transfer.We did not observe In additionto the six onagradsjust discussed, these bees visiting C. hartwegiiin our studies in Clinebellcollected floral visitors on threetaxa that the same general region.Instead, we found these bloomedat the same time in these communities: large bees on Argemonevolyanthemos (Table 10), Theles)ermamegapotamicum (Asteraceae), Mentze- and in no c ases did they carryany onagradpollen. lia strictissima(Loasac eae), and Argemone,volyan- We inelude here observationsof two additional themos(Papaveraceae; Table 1). We include them species of Onagraceaetribe Onagreae that oe curred in the analysisas partof a (ommunity-ecologyap- sporadicallyat the Monahanssite 9 (Table1). How- proachto the study of Onagra(eaepollination, in ever, these species were not present in sufficient orderto identifyflower-visiting insects sharedwith numbersto allowus to analyzetheir pollination bi- the onagradtaxa as well as those that do not ( ome ologycompletely. to the onagrads.These three non-onagradspecies co-occurredwith Calylo)hu.sberlandieri and (;aura OF,NOTHEIVAKHOMAII'ETAIS N UTrJ'. EX T()llR. & villosa in the stabilizeddune areasof site 9 (Table A. GRAY 1; Fig. 2). Clinebellstudied this species in June 1999 at Monahans(site 9) with Calylophusberlandieri and THELESPEKMAMEGAPOTAMlUlJM (SPRENC.) KUNTZE (;aura villosa on stabilized dunes, but blooming Commonlyknown as Navajotea, this species of plantswere absent in the severedrought year 2000. Asteraceaewas abundant in the stabilizeddunes and Duringa fairly short observationalperiod of six attractednumerous beeflies and scoliidwasps. A to- hours(Table 2) in 1999, he collectedthree sphingid tal of 56 insectsin 22 species carrieda cumulative moths (Hyleslineata), three noctuidmoths (Meli- load of 10,950 pollen grains(Table 8). The colorful potis indomita),and a beetle (Eupomphaviridis orangeand black beeflyPoecilanthrax effrenus was Horn).This anecdotalinformation suggests that O. the mostcommon visitor (15 individuals,27Wo) and rhombipetala,with long corolla tubes (2.5-3 cm carriedmuch of the pollen moved (3390 grains, long), is pollinatedprimarily by sphingidmoths, 31%). This beeflydivided its time betweenNavajo muchlike C. hartwegii,which also possesses long tea and the onagradCalylophus berlandieri. The sin- corollatubes. gle individualencountered of the large beefly,An- thraxsp. indet.(at 15 mm long, as largeas a small OENOTHERAENGELMANNII (SMALL) MUNZ bumblebee),also carrieda largeload of Thelesperma Clinebellobserved this species at Monahansin pollen. The next most abundantpollen carrierwas 1999 and2000, butthe plantswere never in bloom. anotherbeefly, Exoprosopasp. 1 (11 individuals, In May 2001, however,O. engelmanniibloomed 20g0), which carried760 pollen grains (7@o).The 384 Annals of the Missouri Botanical Garden

Table7. Floralforagers on Calylophushartwegii subsp. flifiolius in the PermianBasin and Transpecos region (Texas, U.S.A.:see Table 1 for site data);pooled data from2 June 1964 (site 8); 22-28 May2000 (site 2); and 6-13 May 2001 (site 9). Legend:F = female;M = male;W = worker;a = Dalea sp.; b = Gauravillosa; c = Solanaceaeor Nyetaginaceae;asterisks (*) referto sightrecords, pollen load unknown.

11 to 51 to 101 to No 1 to 10 50 100 500 >500 Other Caly. Caly. Caly. Caly. Caly. Caly. pollens pollen grains grains grains grains grains carried Totals Coleoptera Chrysomelidae Alticasp. indet. 1 2 1 3 Hymelloptera Apidae Apismellifera L.; W 7* 11 a(2), b(l) 18 Halictidae Sphecodogastradanforthi McGinley; F 1 4 5 Lepidoptera Moths Noctuidae Acontiinae acontiinidsp. indet.1 (brown,7 mm) 3 Catocalinae Bulia deducta(Morr.) 2 1 Drasteriapallescens (Grote & Robin- l son) Matigrammarubrosugosa Grote Melipotisindomita Wlk. 2 5 Heliothinae Shiniacitrinella (Grote & Robinson) 1 4 Pyralidue Diastictisfracturalis (Zeller) 1 Sphingidae Hyleslineata L. 7* 2 5 5 5 3 c(l) 27 Manducaquinquemaculata (Haworth) C 1 Neuroptera Myrmeleontidae Scotoleonminusculus (N. Banks);M 1

Totals 28 8 10 7 6 18 = 77

third most commonpollen carrier,which was en- collectedat site 9 in Juneand Aug.-Sep.1999 (Ta- counterednowhere else in this data set, was the ble 1), shows no significantoverlaps between this small orange-yellowscoliid wasp Trielis octomacu- species of Loasaceaeand any co-bloomingona- lata (4 individuals,7%), carrying the secondlargest grads(Table 9). Bees accountedfor mostof the vis- amountof pollen (2000 grains,18%). Two individ- itors (35 individuals,83%) and carriedmost of the uals of an undeterminedwasp carried the thirdlarg- pollen (16,025 grains,95%); only one beefly(Dip- est cumulativepollen load (1000 grains,9%). At tera;2% pollencarried), one skipper(Hesperiidae; least 11 differentinsect species carriedsignificant Lepidoptera),and five beetles (Coleoptera;2% pol- loadsof Thelespermapollen (> 100 grains),many of them representedin the data set by only a single len carried)were collected on Mentzelia. The co- specimen(such as the beeflyAnthrax). dominantvisitors to M. strictissimaare worker bum- blebees (Bombuspennsylvanicus) and females of the MENTZE,LIASTSCTISSIMA (WOOTON & STANDL.) J. DARL. green halictid bee Agapostemon splendens, each A sampleof 42 floralvisitors in 11 species, car- with 10 individuals(24%) that carrycumulatively ryinga cumulativepollen load of 16,790 grainsand 5000 grains(30%) each. Bothspecies arerare else- Volume 91, Number 3 Clinebell et al. 385 2004 Pollination Ecology

Table8. Floralforagers on ThelespernianiegapotaniicunI (Asteraceae) in the Monahanssandhills (Texasa U.S.A.: site 9, Table]); Ecooleddata from7-12 June, 30 Aug.-l SeE. 1999, 28 May2000, and 6 May2001. Legend:F = fetnale;M = male;a = Miniosaquadrivalvis var. oceidentalis; b = Argemonepolyanthenws; c = Calylophusberlandieri.

11 to 51 to 101 to No 1 to 10 50 100 500 >500 Other Thele. Thele. Thele. Thele. The>. Thele. pollens pollen grains grains grains grains grains carried Totals Coleoptera Cleridae Thrichodesoresterus Wolcott 1 1 Chrysomelidae Diabroticaundecin7pmncta;a Mann 1 coleopteransp. indet. 1 (gray) Diptera Bombyliidae Anthraxsp indet. 1 1 Chrysanthraxedititims (Say) 1 1 2 Exoprosopasp. indet. 1 1 5 2 1 2 ll lYxoprosopasp. indet.2 I 1 Poecilanthraxeffrenus (Coquillett); M 2 4 Poecilanthraxeffrerzms (Coquillett); F 1 Poecilanthraxeffrenus (Coquillett) M+F 3 3 2 2 10 Bombyliidsp. indet. 1 1 1 Fiyrphidae Eristalissp. indet. 1 1 Tachinidaesp. indet. I 1 2 3 Hymenoptera Halic [ielaP Agalsostemnangelicufls Cot kerell; M 2 2 hecofl(sgastra dtlXrthi M (JiXIIPYF I Tchneumonidae ichneumonid sp. in(let. I I Scoliidae Trielisoctornaculata texensis (S. ss.); M I 1 Trielisoctoniaculata tensensis (S. ss.); F 3 3 a(2)7 b(l) Sphecidae hens sp. indet. 1; F 1 1 Vespidae Eumeninaesp. indet. I; M waspsp. indet. 1; M 2 a(l) 2 Lepidoptera Lyeaenidae lyeaenidsp. indet. 1 (small7blue) 1 1 Nymphalidae W7eptoietaclaudia (Cramer) 2 1 c(1) 3 Pieridae

Coliasphilodice philodice Godart; F 1 1 Nathalisiole Bois. F 1 Totals 4 10 10 8 10 14 ES - 56

where in our data sets. Perdita kiowi, a small ARGEMONE POLEANTHEMOS (FEDDE) G. B. OWNBEY cream-coloredandrenid bee that is active at twi- light and well-camouflagedon the Mentzelza This species intergradesconsiderably with Ar- blooms,is foundnowhere else in our collections. gemone albiq(loraHornem. subsp. te.xana G. B. 386 Annals of the Missouri Botanical Garden

Table9. Floralforagers on Mentzeliastrictissima (Loasaceae) in the Monahanssandhills (Texas, U.S.A.: site 9, Table1); Ecooleddata from 7-12 June 1999 and 30 Aug.-l Sep. 1999. Legend:F = female;M = male;W = worker; a = Argemonepolyanthemos.

1 to 11 to 51 to 101 to No 10 50 100 500 >500 Other Ment. Ment. Ment. Ment. Ment. Ment. Ecollens Ecollengrains grains grains grains grains carried Totals Coleoptera coleoEnteransp. indet. 1 (11 mm,gray) 1 3 1 5 Diptera Bombyliidae Poecilognathusscopulax (Osten Sacken); F 1 1 Hymenoptera Andrenidae Perditakiowi Griswold; M 2 2 Perditakiowi Griswold; F 1 1 2 Apidae Apismellifera L.; W 4 4 Bombuspennsylvanicus (DeGeer); W 10 a(2) 10 Halictidae Agapostemonangelicus Cockerell; F 1 1 Agapostemonsplendens (Lepel.); F 10 10 Agapostemonsplendens (Lepel.); M 3 3 Augochloropsissumptuosa (Smith); F 1 a(l) 1 Dialictussp. indet. 1; F 1 1 Evylaeussp. indet. 1; F 1 1 Lepidoptera Hesperiidae Atalopedescampestris huron W. H. Edwards;M 1 1

Totals 1 3 4 3 31 E = 42

Ownbey(Papaveraceae) in centralTexas, and al- vaga) carrying significantpollen loads (> 300 thoughthe two are consideredto be distinct spe- grains each) also were unique in the data set, as cies, these whiteprickly poppies are oftennot eas- were two other species of Megachile.The halictid ily separable(Diggs et al., 1999). We have treated bee Augochloropsissumptuosa was otherwisefound the specimensfrom the MonahansSandhills (site only on Mentzelia.We collected four individuals 9) as A. polyanthemos.Most of the 72 floralvisitors (6%)of Evylaeussp. 1, anotherhalictid bee com- in this sample, belongingto 18 species and cu- monly encounteredon species of Onagraceae;no- mulativelycarrying 27,140 pollen grains (Table tably,one of the specimenscaptured on Argemone 10), show no overlapwith the insects sampledon had a pollen load with 90WoGaura pollen. The an- Onagraceae.Hymenoptera account for mostvisitors thophoridand megachilidbees were mostly col- (56, 78%)and most pollen carried(23,895 grains, lected in early morning,sleeping in the flowersin 88Wo),with Coleoptera(10, 14%;2405 grains,9Wo) the crevicebetween the stamencluster and the pet- and Diptera(5, 7%;930 grains,3%) also present. als, oftenin groups.Since the stigmaof this species Femalesof the anthophoridbee Diadasia rinconis is locatedat the centerof the ball of stamens,these are uniqueto Argemonein the dataset, thoughone bees wouldhave to crawlto the top of the stamen also carriedsome Mentzelia pollen. Both males (20 ball beforeflying off in orderto effect pollination, individuals,28%) and females (11, 15%) of this and this was not observed.However, this spatial cactusbee werethe mostcommon Argemone pollen arrangementof stigmaand stamensapplies to all carriers; altogether, Diadasia rinconis carried floral visitors, and we have no observationsthat 13,100 grains (48%). One male and two female wouldsingle out one groupof visitorsas beingmore long-tonguedmegachilid bees (Megachilemonti- or less effectiveas pollinators. E 72

Volume 91, Number3 Clinebell et al. 387 2004 Pollination Ecology

Table10. Floralforagers on Argemonepolyanthemos (Papaveraceae) in the MonahansSandhills (TexasX U.S.A.: site 9 Table1); pooleddata frorll 7-11 June 1999 and 6-8 May2001. Legend:M-male; F = female;a = Onagraceae; b = Calylophatsberlandieri; c = Menl;zeliastrictissima d = Gauru.uillosa.

1 to 11 to 51 to 101 to No 10 50 100 500 >500 C)ther Arge. Arge. Arge. Arge. Arge. Arge. pollens pollen grainsgrains grains grains grains carried Totals Coleoptera Chrysomelidae Alt;icasp. 1 Diabroticaalndecimpunctata Mann. 1 1 Coccinellidae coccinellid sp. indet. 1 1 a Meloidae Eupomphaviridis (Horn) 1 5 coleopteran sp. indet. 1 (red thorax) 2 2 Diptera Bombyliidae Poecilognathzzsscopulax (C)sten Sacken) 1 b l bombyliid sp. indet. 1 (tiny, wings c,lear) 1 ryrpo a1C. ae Eupeodesvolucris C)sten Sacken; F 2 2 E7lpeodesvolucris C)sten Sacken; M 1 1 Hymelloptera Anthophoridae Centristripes Moes.; M Diadasiaaff. diminuta(Cr.); F 3 4 Dilidtlsiarinconis Clell.; F 3 7 c,(1) ll Didasia ritlconitsClell. M 5 1t$ 20 Halicti(lae Augochloropsissumptuosu (Smith); F 2 2 F,vylaezzssp. inclet. 1; F 1 d(l) c(l) kSphecodogastra(lantorthi McGinley; 1#' 1 Megachilidae Megachilecf. IauritaXF 1 4 5 Megachilemontivaga Cresson; F 2 Megachilemontivaga Cresson, M 1 l Megachilemucurosa Clell.; F 1 Megachilemucurosa Clell.; M 2 2 Lepideptera Noctuidae Plusiinae Autographabiloba (Stephens) I r fc)tals 3 2 23 40

SUMMARY OF MAJOR POLLEN CARR1ERS significantabsence of overlapamong the majorpol- len carriersin termsof the plants}ecies they visit. Forthis analysis7we definemajor pollen carriers as insects carryingmore than 50 pollen grainsof a These are unexpectedresults that argue for the given ?lantspeciesS Table 11 lists those majorcar- need to conduct more field studies in pollination riersfor each of the seven plant species for which biology at the communitylevel. Althoughit has we have enoughdata. For convenience,Table 12 been difficultto get insect deterulinationsacross pools majcyrpollen carriersby plant species and this data set and tedious to quantifythe pollen showsthat there is greatspecificity in each pollen loadsSwe feel that these data demonstratea higher guild. Whatis remarkableabout these tablesis the level of pollinatorspecialization in these commu- ... 7* f 1 * ,

388 Annals of the Missouri Botanical Garden

Table 11 Majorpollen caITiers by plantspecies, definedas arlyinsect carryingmore than 50 pollengrains of that plant species. Insecttaxa represented in the data set by a single specimen("singleton') are markedwith an asterisk (*) and includedin the closest inclusivetaxon in whichthey can be deterrnined.

Thele- sperma MentzeliaArgemone (;amra Calylophms Gaura Calylophalsmesopo- stric- poly- villosa herlandieri coccinea hartwegii tamicurn tissima anthemos Coleoptera 1* Buprestidae Achmaeoderamixta 7 tlerleaerr . ] 18 Chrysomelidae 1* Alticas p. indet. 1 7 Meloidae Ellpomphauiridis 5 Scarabaeidae 1* Coleopterasp. indet. 1 2 Diptera Bombylndae 3* :Egxoprosopasp. indet. 1 3 Heterostylu.mrobustunt G PoeciZ.rzthraxeffrenus 12 Poecilognathusscopulax 7 1 1 Syrphidae 18 Eupeodesvollleris 2 Tachinidae indet. 1 3 Hymenoptera Apidae Apismellilera 3 11 4 BombuspennsylvaniGus 1 10 Andrenidae

rerAlta tIOWI 4 Anthophoridae 28 1* Diadasiaaff. diminuta 4 D. rinconensis 30 Halictidae 1* Agopostemonangelieus 1 1 A, splendens 13 Augochloropsissumptmosa 1 2 Evylaealssp. indet. 1 2 1. 4 Sphecodogastradar2forthi 11 94 4 1 t.f) noctivaga 4 Megachilidae Megachilemontivaga 3 M. mucurosa 5 1R cf. Iallrita 5 ncolllelae Trielisoctom,aculata 4 Sphecidae 18 Vespidae 18 wasp indet. 2 Lepidoptera 18 Geometridae Semiothisasp. indet. 5 Volume 91, Number 3 Clinebell et al. 389 2004 Pollination Ecology

Table11. Continued.

Thele- sperma MentzeliaArgemone Gaura Calylophus Gaura Calylophusmesopo- stric- poly- villosa berlandieri coccinea hartwegii tamicum tissima anthemos Noetuidae 4* 5* Bulia deducta 7 2 1 Helicoverpazea 2 Melipotisindomita 6 3 1 noctuidsp. indet.3 3 Sphingidae 1* Hyleslineata 13 Neuroptera Myrmeleontidae 1* Brachynemurushubbardi 3 Paranthaclisishageni 3 Scotoleonminusculus 69 Total:singletons 5 3 5 1 7 3 2 Total:all majorpollen carriers 114 125 20 31 32 3t3 65 nities than expected,based on currentdebate re- (the overall"community efficiency" is 33.3%),sug- gardingspecialized versus generalizedpollination gestingconsiderable variability among species. niches (Waseret al., 1996). In summarizingpolli- At the other extreme,many rare insect species natoractivity (Table13), we found that the guild also appearin this large data set. Whetherit is the fidelityof the seven mainplant spec ies rangesfrom large scarabflower beetle Euphori(lon C(llylophus 75.0% to 99.2%, with a mean of 91.2%. Pollen berlandieri,the large antlionVell(lfell(lx on G(lur transportefficiency ranged from 8.4% to 90.5% in villos(l,or the large beeflyAnthr(lx on Thelesperm the seven taxa, with a mean of 50.9% efficiency meg(lpotamicum,these insect raritiesrepresent an

Table 12. Pollinationguilds of majorpollen carriersfor each of the primaryplant species in this analysis,as detailedin Table11. Insecttaxa (including singletons) are assigned to the guildof the plantwhose pollen they primarily carry(i.e., serve as modalpollen c arrier); individual insects that are majorpollen carriers for other(non-modal) plant species appearunder those species. The halictid bee Agopostemonangelicus (only one individualeach on Gauravillosa andMentzelia strictissima) is assignedto Guild6 (of Mentzelia)because that individual carried a largerload and Guild 6 also includesA. splendens.

Thele- sperma MentzeliaArgemone Gaura Calylophus Gaura Calylophusmegapo- stric- poly- villosa berlandiericoccinea hartwegii tamicum tissima anthemos Guild 1 97 5 2 (Gauravillosa) Guild 2 11 124 4 1 1 1 (Calylophusberlandieri) Guild 3 15 (Gauracoccinea) Guild 4 3 25 4 (Calylophushartwegii) Guild 5 31 (Thelespermamegapotamicum) Guild 6 1 1 31 (Mentzeliastrictissima) Guild 7 2 2 64 (Argemonepolyanthemos) 390 Annals of the MissouriBotanical Garden

Table 13 Communitysummary statistics. The o+rerallcommunity pollen transportefficiency (marked t) is an averagefor all insect visits observed,this figureis biased by the unequalpollinator sample stzes amongthe plant species. The mean guild pollen transportefficiency (marked **), the averageof the efficiencyfigures for each of the seven guilds,is not biasedby unequalsample sizes.

Totalmodal Totalrson-modal Guildpollen major rSotalfloral majorpollen Guild transport pollencarriers arisitors carriers fidelity(Wo) efficiency (%) A B C A/(A+C) (A+C)/B G(lur(lvillosa 97 562 17 85.1 20.3 C:(llylophusberlandieri 124 252 1L 99.2 49.6

6elllra coccinea 15 238 S 75.0 8.4 C:ulyll)phushartwegii 25 77 6 80.6 40.3 Thele.spermamegapotamicum 31 56 1 96.9 57.1 Mentzeliastrictissima 31 42 7 81.6 90.5 Argemonepolyanthemos 64 72 1 98.5 90.3

ES = 394 SE = 1299 SE, = 38 91.2 33.3* lWeanguild pollentrarlsport efficiency: 50.988

- importantsecondary outcome to the randomized . FORAGING BEEJAVIOROF MAJOR POLLINATING field collectionof a sufficientlylarge sample of the GROUPS commonpollen carriersto enable statisticalanal- ysis of the data. These data also highlightthe im- We discuss these in a diurnalsequence begin- ning at sunrise. We note especially those cases portanceof settingaside largeareas of naturalref- . . . . . waere a glven lnsect 1s a true po lnatorln one uges for the sake of rare s^)eciesthat exist at species of onagradbut not of otherspecies. relativelylow populationdensities, yet play impor- tant roles in the pollinationbiology and ecologyof naturalcommunities. Hailictidbees fHymenoptera) that are onagrad oligoleges

DI SCUSSION At least three species of Sphecodogastraand Ev- ylaeusvisit onagradspecies in the MonahansSand- We divide the discussioninto two parts:(1) for- hills. Sphecodogastranoctivaga: the largest(12 mm aging behaviorof majorpollinating insect groups, long)halictid, visits only GauravililosaS mostly from and comparisonwith other pollinationstudies of midnightto 6 A.M., but occasionallyuntil 8 A.M. Onagreae,and (2) analysis of mixed pollen loads Bothsexes of this species are uniqueamong insect carriedby foraginginsects. Withinthese areas of visitorsto C. villosain thatthey spentthe evenings on the inflorescences,crawling about and resting. discussion,we examineand comparethree inter- They are highly attractedto lights, and were col- related themes:(1) geograpllicreplacement of re- lected by both Gregoryand Clinebellat car lights latedpollinators across the rangeof a plantspecies, adjacentto colonies of G. villosa. Males did not (2) the effect of the presence or absence of large appearto carryany pollen, and femalesoften car- numbersof honeybeesat a particularsite; and (3) ried smallpollen loads,however, females occasion- the importanceof the ecological integrityof the ally carriedlarge amountsof pollen in a full rear community.The first two themes were highlighted femoralscopal load for the provisioningof young. in the Results sectionto underscoretheir high im- The efficaczzof S. noctivagaas a pollinatoris not portance,and the thirdtheme underpins this entire knownbecause we were unable to observe their analysis. The communitiesstudied here represent behavioron flowersdue to darkness.All bees col- the most ecologicallyintact study areasthat could lected of this species carryonly Scluravillosa pol- be. located for these plant species, and represent len. relicts of the original (i.e., pre-Europeansettle- Wecollected Sphecodogastra danforthi on Gaura ment)vegetation. Pollination studies conductedin villosa and Calylophusberlandieri (both Onagra- degradedareas may well yield differentresults than ceae). These halictid bees forage on C. villosa:, those reportedhere. where they were found almost exclusivelyin the . . 1 . . . . l , . ,

Volume 91, Number 3 Clinebell et al. 391 2004 Pollination Ecology

morning,from sunrise until about9:30 A.M. Sphe- requirean even larger sample size than reported codogastradanforthi was also infrequentlycaptured here, as is also the case for other rare species in at duskon both species of Calylophus.This species the data set. is muchmore prevalent on C. berlandieri,account- We tested the null hypothesisthat Sphecodogas- ing for about40% of individuals(and 83Wo of pol- tra danforthiand S. noctivagarandomly visited len carried)of the pollinatordata set for that spe- flowersof Calylophusberlandieri and Gauravillosa cies, than on Gaura,where it accountsfor about using the Chi-squaretest for independence(Con- 5Woof visitors (and 13% of pollen carried).This over, 1980). While most individualfloral visitors halictidbee is an effectivepollinator of Calylophus were females, the test was calculatedfirst using berlandieri,frequently climbing over the stigma both male and female bees. The Chi-squaretest while travelingfrom stamen to stamen.It appears statisticwas 61.31 (P < 0.01), indicatingsignifi- to be less effectiveon Gauravillosa, however, due cant non-random(selective) flower visitation. The to the more pronouncedherkogamy in the latter test statisticfor females only was 60.69 (P << 0.01), species,where the stamens(6.5-13.5 mmand clus- agaln lndlcatlngslgnlhcant devlatlon trom expec- teredin the lowerquarter of the zygomorphicflow- tation.These tests scoredthe bees accordingto the er) are notablyseparated from the stigma(atop the plant species on which they were collected. Be- style 10-18.5 mm;Raven & Gregory,1972a). Nev- cause 17 of the female Sphecodogastradanforthi ertheless,we observedfemales using the stigmaas collectedon Calylophuscarried mixed loads of Ca- a landingplatform several times, and so pollination lylophusand GaurapollenS a test was runassigning mightbe effectedoccasionally. Of 135 individuals half of these mixed-loadbees to Gaura.The re- of Sphecodogastradanforthi in the overalldata set, sulting test statistic, 46.83 (P << 0.01), was still 18 carriedno onagradpollen, but only 2 werecap- highlysignificant. Thile collectingefforts began at turedon non-onagradtaxa, 1 each onArgemone and 7:00 A.M., after which time few Sphecodogastra Thelesperma,carrying pollen of thosespecies. Four- danforthiwere collectedon Gaura,there obviously teen individualscarried mixed loads of Calylo)hus was an earlierperiod of activitythat included floral and Gaurapollen, 13 of which were capturedon visitationto Gaura.Whether or not this includeda Calylophusflowers. Thus, the 2 Sphecodogastra significantnumber of femalesthat visited only Gau- halicti(lbees, 1 nocturnaland 1 matinal,exhibit an ra an(l had ceased foragingbefore 7:00 A.M. iS un- overwhelmingpreference for foragingon species;of known.A conservativeinterpretation of these data Onagraceae. suggests that Sphecoflogastr(lnoctivaga does not Evylaellssp. 1 is not as commonin the dataset visit Calylo,l)husat all, that females of Sphecodo- as S)hecodogastra,but females do carryonagrad gastradanforthi visit bothplant taxa, and that these pollen loads. Evylaeus lacks the hooked scopal data may be biased in termsof under-representing hairs of Sphecodogastra(a synapomorphyfor the visits to Gauraby Sphecodogastradanforthi, if in- genus; McGinley,2003) that presumablyprovide deed these femalebees aremore likely to visit Gau- betterpollen adherencefor that genus. Mostof the ra than Calylophusprior to 7:00 A.M. specimens were capturedon Gauravillosa from Gregorycollected mostindividuals of Sphecodo- 6:30 to 8:30 A.M., and these foragedwith S)heco- gastra noctivaga in this data set in June 1964 dogastradanforthi. It is doubtfulthat Evylaeus is a aroundthe dome light of a car parked beside a reliablepollinator for G. villosa for the same rea- populationof Gauravillosa, and most of these fe- sons stated above for Sphecodogastra.Of 13 indi- males carriedeither no Gaurapollen or sparsepol- viduals collected in this study, 4 were found on len loads. However,in August2001, we collected Argemone,and so this halictidbee is not as closely ca. 30 femaleS. noctivagabees on G. villosain the associatedwith Onagraceaeas are the 2 species of CimarronNational Grassland (Morton Co., Kansas, Sphecodogastra. U.S.A.),all carryinglarge Gaurapollen loads (un- To summarize,females of Sphecodogastranocti- published).These are the onlyactive nocturnal pol- vaga appear to be majoreffective pollinatorsof len foragerson G. villosa at both sites. (The other Gauravillosa (pendingverification by ethological nocturnalfloral visitors, noctuid moths and ant- observations);Sphecodogastra danforthi is an effec- lions, actively harvest only nectar, but passively tive pollinatorof Calylophusberlandieri, but prob- transportpollen as a byproductof nectarforaging.) ably not of G. villosa;and Evylaeussp. 1 may not By contrast,S. noctivagaappears from our data to be an effectivepollinator of eitheronagrad species be less abundantat the MonahansSandhills in Tex- and does not even visit Calylophusflowers. Evy- asvand it is likely that S. danforthivisits bothon- laeus is uncommonin this data set, and under- agradtaxa in the presence of low densities of S. standingits role at the MonahansSandhills may noctivagaand for whateverreasons, visits Gaura 392 Annals of the Missouri Botanical Garden

before Calylophus.Clinebell collected a large set genionepolyanthenios and one on Mentzeliastrictis- of male S. noctivagaon 22 July 1999 from1:30 to sin7a.All of these bees werecollected between sun- 3:30 A.M. on the KiowaNational Grassland, Union rise and 10:00 A.M. County,New Mexico.Here, the males carriedvir- tually no pollen, and appearedto be searchingfor Otherbees and wasps(Hynienoptera) females on Gaura inflorescences.We emphasize We collectedbees in a diversityof families,in- that G. villosa was in bloomin this data set from cluding AndrenidaevAnthophoridae, Apidae, and earliestMay to earlySeptember, and thatwhile the Megachilidae,most often on plantsother than On- insect groups collected at Cimarron,Kiowa, and agraceae.Martinapis enteicornis (family Anthophor- Monahanswere the same fromsite to sitevthe rel- idae) was collectedexclusively on Gauracoccinea, ative abundancesof these groupsvaried according but carriedlittle pollen(Table 6). A singleDiadasia to site and season.The mostdramatic seasonal shift rinconis(Anthophoridae) male carriedCalylophus observedwas the rarityof Sphecodogastradanforthi berlandieripollen (Tahle 5), whereas 11 females in early May 2001 at Monahanson flowersof C. and 20 males were collected on Argen7onepolyan- berlandieri.Thile pollinatoractivity always oc- thenios,all but one femaleladen with pollen(Table curredin earlymorning, the majorpollinator in the 10). These femaleD. rinconiswere observedto be absence of S. danforthiwas the small beefly,Poe- sleepinginside the poppiesshortly after sunrise. A cilognathusscolopax. single female of Centriscaesalpiniae (Anthophori- Clearly,pollen load analysishas been essential dae) was collectedon Calylophusberlandieri, car- forelucidating the complexitiesof pollinatorforaging rying a heavy load of pollen (Table5). A single choice, especiallywhen the pollengrains of related Bonibuspennsylvanicus (Apidae) worker was col- onagradgenera can be distinguished(Praglowski et lected on C. berlandieri(Table 5), but ten were en- al., 1988). Withoutsuch analysis,we might have counteredon Mentzeliastrictissinia (Table 9), all concluded(erroneously) that Sphecodogastra danfor- carryinglarge pollen loads of the plantsvisited, and thi does not visit flowersof Gauravillosa when in mostly collected between sunrise and 10:00 A.M. fact it does, but only priorto 7:00 A.M. All are putativelyreliable pollinators of the plants A single femaleof Sphecodogastradanforthi was visited, thoughtheir densities are low in this eco- collectedon Thelesperniaand carrieda full load of system.Apis niellifera (Apidae) was a commonpol- its pollen.Four females of Evylaeussp. 1 werecol- len forager on Calylophushartwegii for several lected on Argenione,half of which were also car- hoursafter anthesis at a degradedsite in Brewster ryingGaura pollen. Otherwise,all pollen foundon County(site 2), but not at MonahansSandhills (site these halictid bee genera was from Onagraceae 9), and the honeybeeworkers were not observedto flowers. makecontact with the stigmaswhile col]ecting pol- len. They were not observedattempting to collect Halictidbees (Hyrnenoptera) that are not onagrad nectar, which normallyis quickly harvestedby oligoleges sphinxmoths (Hyles lineata) that appear just at the time of anthesis. Threegreen halictid bee species includedin this Five species of wasps,each in a differentfamily data set were not majoronagrad pollen carriersat (Ichneumonidae,Scoliidae, Sphecidae,Tiphiidae, the MonahansSandhills in Texas. Agaposternon and Vespidae)were collected on Thelasperrname- splendens(both males and females)occurred pri- gapotarnicllrnat the MonahansSandhills (site 9) in marilyon Mentzeliastrictissirna, comprising about westernTexas. Almost all of these was)s (8 out of one-thirdof the 42 insect visitorscollected on that 9) carriedmajor pollen loads (> 50 grains),so in- species. All carriedsubstantial loads of Mentzelia dividuallyall exceptthe undeterminedichneumon- pollen. Malesof Agaposternonangelicus were com- id wasp appearto be effectivepollinators, albeit at ulon on flowersof Gauracoccinea in earlymorning low densitiesin the population. at Monahans,but carriedlittle or no pollen. Sin- gleton females of A. angelicuswere collected on Beefies (Diptera) Gauravillosa and Mentzeliastrictissinia, each car- ryinglarge pollen loads, and twowere collected on Ten species of Bombyliidaewere flowervisitors ThelespernianiegapotanicunI, but cauied less than at our study sites, belongingto at least six genera. ten pollen grains.Thus, we do not yet knowwhat Manybeeflies visit Calylophusberlandieri, mostly the femalesof this species are doingat Monahans. carryingsmall to moderate(< 100 grains)pollen Finally,three femalesof Augochloropsissumptuosa loads (Table5); manyof the numerousbeeflies on were collectedwith heavypollen loads two on Ar- Thelesperniacarry somewhatlarger pollen loads Clinebell et al. Volume 91, Number 3 393 2004 Pollination Ecology

(Table8). These twoplant species accountfor most and otherflower parts and regularlycontacted the beefly visitationin our analysis,but all plant spe- stigmas.They also fly betweenplants and are prob- cies except Calylophushartwegii had at least one ably effectivepollinators. The beetlesAltica sp. in- beeflyvisitor. Beeflies tend to be mostactive in the det. (Chrysomelidae)and Achniaeoderaniixta (Bu- hot middayperiod and are veryhard to catch,even prestidae)together accounted for 25% (63 of 252) with a runningstart with the sweep net. We unin- of all insects collectedon flowersof C. berlandieri, tentionallybaited individualsof Poecilanthraxef- but carriedless than 8% of the cumulativepollen frenus at two separatepopulations of Calylophus load (Table5). At least somebeetles werecollected berlandieriat site 9 (Table1). Althoughthe beeflies on all plantspecies in our dataset, and in all three apparentlywere attractedto onagradfloral chemi- non-Onagraceaespecies (Tables8-10), at least one cals on clothingand nets, we assignedthem to ei- beetle carrieda largepollen load. However,beetles ther C. berlandierior Thelespermadepending on did not cumulativelyconstitute a majorclass of each individual'spollen load. flowervisitors or of pollen carriersfor any plant Twoadditional species of beeflies,Heterostylum species otherthan C. berlandieri.Primack and Sil- robustunIand Poecilognathusscolopax (Bombyli- ander(1975) reportedbeetles as effectivepollina- idae), also visitedflowers of Calylophusberlandieri tors of the day-floweringOenothera fruticosa L. (Table5). Weobserved H. robustum,a hirsute,gold- (Onagraceae)in NorthCarolina, although they were en-coloredbeefly that hovered over the flowerscol- secondaryin importanceto introducedhoneybees lecting nectaronly at midday;most specimens car- as pollinators.We did not observe beetle larvae ried heavy pollen loads. On the other hand, feedingon any plantsat our study site. Poecilognathusscolopax, a cream-coloredand less hairy beefly than Heterostylum,foraged mostly in Mothsand butterfies(Lepidoptera) early morning,landing on the flowerand pushing about halfwayinto the floral tube, presumablyto Butterflieswere rare at the MonahansSandhills reach the nectar.Despite the scarcityof hairs and site in westernTexas in 1999 and 2000, possibly theirnectar-gathering habits, most individuals of P. due to prolongeddrought conditions. Scattere(l in- scolop(lxcarrie(l some Calylophuspollen, though divi(lualsof five butterflyfamilies visited plantsin only one carrie(lmore than 100 grains (Table5). our stu(lycommunities, but in only two instances Both species are effectivepollinatorsv since many werethey carryingany pollen.Three indivi(luals of indivi(lualsactively forage among y)lants an(l con- Eulstoit(lcl(lu(li(l (Nymphali(lae)e arrie(l small tact stamensan(l stigmasduring flower visits. amountsof Theles)er7r7>(lpollen, an(l a single male Poecilanthr(lxeffirenus (Bombyliidae) is a medi- sachemskipper (At(llol)edes c(lrnpestris huron; Hes- um-size(l,orange and black beeflythat divi(le(lits perii(lae)c arrie(l a majorloa(l (> 50 grains) of time between the onagra(lCalylo)hu.s berlan(lieri Mentzeli(lpollen, each of them foragingduring the (Table5) and the compositeThelewerrna (Table 8) noonto 4 l'.M. period. duringthe warmestparts of the day. In fact, of all Moths,on the otherhand, were the mostcommon the beeflies in this analysis collected with pollen groupof insects in our analysis. Four families of loads, 76 of 78 individuals(97%) visited one of moths (Geometridae,Noctuidae, Pyralidae, and these two planttaxa; only one individualof Poecil- Sphingidae)are representedin this data set, and ognathusscolopax was collectedeach on Mentzelia all limitedtheir flower visitations to species of On- (Table9) and Argernone(Table 10). In conclusion, agraceae,although a few carriedpollinia of an un- it appearsthat the beeflies of the MonahansSand- knownand unseen species of Asclepi(ls(Apocyna- hills are eitheronagrad foraging specialists or com- ceae, Asclepiadoideae)on the tips of their legs. posite foragingspecialists, or in the case of one Even thoughthese four mothfamilies account col- species, generalizedenough to visit onagrads,com- lectivelyfor 622 of the 1299 totalinsects collected posites, and othertaxa. (48%),they generallycarry small pollen loads; only 59 of these 622 individuals(9%) carry more than Beetles(Coleoptera) 50 pollen grains,our pollen-loadthreshold for ma- jor pollinators.This majordiscrepancy between the Like beeflies, flower-visitingbeetles were most visitorfrequency and pollen load in mothsmay be abundantin the hottestparts of the day, although a collectingartifact (i.e., pollen is lost frommoths we collectedsome beetles at othertimes. They are in the captureprocess more easily thanfrom other mostsignificant as floralvisitors of Calylophusber- insects), but morelikely has a structuralexplana- landieri(80 individualsof 10 species, 60 of which tion. carrysome pollen;Table 5), wherethey ate pollen The patternof pollen depositionon the bodiesof 394 Annals of the MissouriBotanical Garden

moths found during pollen load analysis differs Sphingidae fromthe patternobserved on mostother insect vis- itors. On manyinsects, especiallythose that forage Commencingat twilight,there is a surge in ac- primarilyfor pollen ratherthan nectar,we found tivityof the sphingidmoth Hyles lineata on flowers mostor all pollenon the ventralsurface of the body. of Calylophushartwegiip and to a lesser degree, Hymenopterafrequently carried massive pollen Oenotherarhornbipetala. Difficult light conditions loads, concentratedin and aroundspecific pollen- and the speed with whichthese mothsmove made gatheringstructures such as corbiculaeor scopae. catchingthem a particularchallenge. Like other Mostindividuals of ColeopteravDiptera, and Neu- moths, Sphingidaecarry pollen on the proboscis, ropteraalso carrymost or all of their pollen loads but unlike othermoths, they also carrysubstantial on their ventralsurfaces. Some pollen grainsalso pollen on their ventral surfaces. Nonnenmacher werefound on the head and aroundthe mouthparts (1999)observed ventral pollen deposition on sphin- of many insect visitors.However, in all groupsof gid mothsvisiting Oenotheraniacrocarpa (Onagra- mothsin our sample except the Sphingidae,most ceae) on the Konza Prairie (Riley Co., Kansas, or all of the pollenwas foundon the proboscis,with U.S.A.).This species is rathersimilar in floralmor- relativelyless on the ventralthorax, abdomen, and phologyto Calylophushartwegii, and elicits similar legs. This is true even on freshlycolleeted speci- behaviorby the sphingidmoth visitors. mens handledcarefully to avoid pollen loss. This relativeabsence of pollen on the ventralsurfaces Geornetridae of mothsmay be due to a generallack of hairsand Whereaslarge sphingid moths forage on onagrad otherepidermal features that mighttrap pollen on taxa with long corollatubes at twilight,small geo- those bodyparts, and also to the presenceof scales metridmoths (as well as somewhatlarger noctuids on Lepidoptera,which may impede pollen adher- and pyralids)actively visit freshlyopened flowers ence. It is unclearwhether pollen on the mothpro- of Gauracoccinea. Gregory collected moths on this boscises effects pollinationas well as that on the species from7:00 P.M. until midnight,in both the ventralsurfaces, but we recordedtotal pollen pre- Monahans(sites 4 and 8; Table 1) and the Trans- sent (proboscisand ventralbody) for all lepidop- pecos (sites 1 and 6) in westernTexas. In bothcas- . . teranvlsltors. es, small mothswere most abundant until about9: For the non-sphingidmoths in our sample,most 30 P.M., afterwhich largernoctuids predominated. of the pollen load (ca. 85%)adheres to the probos- Mostof the geometridmoths are an undetermined cis, with much smalleramounts on the legs (less species of Seniiothisa,which accounts for 47 of 238 than 10So)and ventralthorax and abdomen(less insects (20%)caught on G. coccineaflowers. Even than5%). We observed a similardistribution of pol- thoughmost carrysmall pollen loads, they maybe len on museum specimens of noctuids and geo- effective pollinatorsof G. coccinea as they fly metridsexamined at the Field Museum.fSecause amongplants and land on flowersto foragenectar. most moths land on the staminalfilaments while extendingtheir proboscisesto gathernectar, with Noctuidcle the ventralthorax and abdomenpressed against lhe anthersand stigma,this lack of ventralpollen is Raven and Gregory(1972a, also Raven, 1979) puzzling.If pollen falls off or even is ;;dusted"off suggestedthat noctuidmoths are the primarypol- duringhandling of the specimens,one mightexpect linatorsof mostspecies of Gaura,and ourdata sup- comparablepollen loss on other types of insects, portthis contentionat least in part.The mostnu- and perhapssimilar loss of pollen frommoth pro- merouspollinators of G. coccineaare four species boscises, but this is not observed.Ventral deposi- of noctuid moths and one geometrid,of the nine tion of pollen on mothssurely must occur but per- majorpollinators of G. villosa,two species of noc- haps adherenceof pollen to moth scales is weak, tuid moths,Bulia deductcland Melipotisindomitcl, at least relativeto adherenceon insects with hairy accountfor 53Woof totalvisitors but less than 10% or scabrousventral surfaces. If so, the pollenloads of the total pollen load (the othermajor pollinators countedfor moths in our analysis may underesti- are antlionsand bees, Table11). If, as we discussed mate the actual pollen carriedby the moths,and above,the small pollenloads on these noctuidtaxa underestimatetheir efficacyas pollinators.A com- are an artifactof collectingand/or curating moth parativeexperimental analysis of pollenadherence specimens,then the importanceof noctuidmoths to insect bodieswould be necessaryto resolvethis as pollinatorsof these Gauraspecies may be un- question,and wouldbe very useful for determina- derestimatedin ouranalysis. However, even if noc- tion of pollinatoreffectiveness. tuid mothscarry only smallpollen loads,the sheer Clinebell et al. Volume 91, Number 3 395 2004 Pollination Ecology

numberof these insects activelymoving that pollen A.M.), carriedhardly any pollen.Like severalof the amongplants clearly marks them as importantand smaller noctuid moths, these pyralidmoths were effectivepollinators. shorterthan the length of the stamen filaments. Bulia deductaand Melipotisindomita (Noctui- Thus, they could land near the throatof the floral dae, subfamilyCatocalinae) were active throughout tube and touchneither the anthersnor the stigmas. the night,with an activitypeak between10:00 P.M. These infrequentvisitors may be nectar robbers, and 2:00 A.M. Both of these species exhibitedin- but in any event are not effectivepollinators. terestingbehaviors. At site 9 in Aug. 1999, indi- vidualsof M. indomitacame to the vicinityof Oen- Antlions(Neuroptera) otherarhornbipetala plants an hourbefore sundown when the flowersopen and alightedon the sandy The firstantlion of this studywas recoveredtak- ground,where they were perfectly camouflaged. ing nectarfrom a populationof Gauravillos(l just This behaviorenabled them to visit the flowersas south of the Kiowa National Grassland(Carrizo soon as they burstabruptly into bloomat twilight, Creekpatch, Union County,New Mexico,23 July in competitionwith a dramaticinflux of sphingid 1999, 2:00-4:00 A.M.). This femaleScotoleon min- moths.It may in fact be essentialfor Melipotisto usculus(Neuroptera, Myrmeliontidae) carried about forage at newly opened flowersbefore the larger 20 pollen grainsof Gaur(lon its legs and ventral sphingidmoths, with their longer proboscises, take surfaces.Insofar as we know,this specimenappears too much nectarfrom the long floraltubes of the to providethe first unambiguousdocumentation of Oenothera(20-30 mm;Munz, 1965). Melipotis also pollen transportand pollinationby any memberof co-foragedwith sphingidsduring the twilightan- family Myrmeleontidae.There are several reports thesis period in BrewsterCounty (site 2 in May in the literatureof floralvisitation (nectar and pol- 2000) on Calylophushartuvegiin which also has rel- len foragingwithout clear pollination)involving ativelylong floraltubes (19.2 mm;Table 3), but we other Neuroptera,especially Sialis (alderfly)and were unable to observe if they clustered around Hemerolius(brown la(ewing) on Apiaceae(Muller, plants priorto anthesis.We di(l not observeeither 1883, Proetor& Yeo, 1973, Proctoret a1., 1996), (lusteringor co-foragingbehavior in 1k1.indomit but in no ( ases are they reportedas anythingother when it visited flowersof either species of G(lur(l than rare and minorfloral visitors. Muller (1883) (floraltubes 2.4-5 mm long; Table 3), whieh are reportedthat only 13 of 5231 (0.2Wo)pollinator vis- sel(lomvisited by sphingidmoths. its he observe(linvolve(l Neuroptera, and manyof Buli(l deduct(lexhibited two foragingstrategies those involve(lPanorl(l, now consi(leredin the or- on Gaur(lvillos(l. Commonly,this noctuid moth der Mecoptera(s(orpionflies). This stu(lyprovides alightedupon the staminalfilaments and style, and (lear evi(len(e that antlionsare majorpollinators restedits wingswhile feeding on nectar.On several of G(lur(lvillos(l. occasions,however, a mothwould land on the floral Additionalspecimens of Scotoleonminusculus tube and ovary,below the petals and stamens,and (both males and females)were collected at site 9 reachits proboscisbetween the petals and into the in the MonahansSandhills on G(lur(lvillos(l flowers floraltube without contacting the stamensor stigma in Aug.-Sep. 1999. Seven specimenswere recov- and thereforenot effectingpollination. This behav- ered from5:30 to 7:00 A.M., while it was still dark, ior was observedat site 9 in May2000, when one and observedto hoverover and land on the flowers. of the largestantlions, Paranthaclisis hageni, was All seven carriedGaura pollen, and fourhad more present.In May2001, this antlionspecies was par- than 100 grains,mostly on the faceSlegs, and ven- ticularlyabundant in the largepopulation of G.vil- tral thorax,with a few on the wings (Fig. 3). Six losa at MonahansSandhills (site 9), and no moths more antlions were collected from 2:30 to 4:30 were present,a mostunusual situation for this sys- A.M., with five carryingmore than 100 grainsand tem. Abundantmoth scales on the bodies of these two up to 1000 grains.Among this late-nightsam- antlionssuggest they may be preyingon mothsat ple was a male of Wellafallax,the largestantlion the same time as they foragefor nectar. (60 mmlong) in NorthAmerica. This largeantlion, carryingfewer than 10 Gaura pollen grains but Pyralidae well-dustedwith moth scales, was observedon a flower in contact with stamens and stigma, sug- The gardenwebworm (Achrya rantalis) was the gesting that it may be an effective pollinator,but primarypyralid moth encountered.This species, also that it may prey on moths.The specimenalso collected on Gaura villosa both after midnight exuded several dropletsof clear liquid (nectar?) (2:30-4:30 A.M.) and before sunrise (5:30-7:00 fromthe mouthduring the pinningprocess. 396 Annals of the Missouri Botanical Garden

Figure3. Femaleadult antlion, Scotoleon minusculus, showing pollen of Gauravillosa on ventralsurface of thorax collectedat MonahansSandhills, Ward Co., Texas(site 9, Table1); 1 Sep. 1999 (photoby R. Keating).

Duringa later trip to Monahans(site 9) in May single plant, approachingand retreatingbefore fi- 2000, we capturedmore individualsof Scotoleon nally landingon a flower. minusculuson Gauravillosa, as well as specimens A possible reason for this apparentreluttance of three additionalspecies of antlions,and were by the antlionsto landbecame clear when we found able to observetheir foragingbehavior more care- and collected an antlionon a Gauraflower in the fully. Most antlionswere capturedafter midnight, clutchesof an unidentifiedwhite crab spider(fam. when their clear wings and slender black bodies Thomisidae).We observedcrab spiderson several renderedthem almostinvisible. Typically, S. min- occasionshiding beneath the petalsand ambushing usculus and Brachynemurushubbardi spent long insectsthat landed on the flower,which is a typical periodshovering around the plants, at a distance and well-documentedbehavior for this family of of up to one meter,approaching a flowerand then spiders.We collected an additionalcrab spider and suddenlywithdrawing backward in a straightor el- observedone additionalantlion capture by a spider liptical pattern,but alwaysfacing the Gauraplant. at site 9 on 20-21 May2000 in the courseof col- The antlionslanded on the Gauraflower much like lecting 26 antlions.This suggeststhat predationof noctuidmoths, by graspingthe filamentsand style antlions(and other pollinators)by crab spidersis with their legs and crawlingup the filamentsuntil not an isolated occurrencein these communities, they couldbury their faces in the throatof the floral and mayinfluence the foragingbehavior of the ant- tube. They sometimesremained in this positionfor lions. Ourobservations also suggestthat nectar for- severalminutes. In this process,the ventralsurface aging is importantenough to antlionsto risk pos- of the insect became coveredwith pollen, which sible predationduring flower visitation. was absent only fromthe posteriorhalf of the ab- Paranthaclisishageni, the most abundantof the domenon the mostpollen-laden specimens. We ob- three large (> 40 mm in length) antlion species, servedas manyas six individualantlions around a also foragesfor nectar and lands on the Gauraflow- Clinebell et al. Volume 91, Number 3 397 2004 Pollination Ecology

ers just as do the smallerantlions. However, indi- and Thelespermaare borne at about 20-30 dm viduals of P. hageni are so heavy that they bend height,much lower than those of otherco-blooming the entireinflorescence downward when they land. taxa exceptfor Gauracoccinea, which does not oc- Thisantlion also is less likely to carryGaura pollen cur in the immediatevicinity of most populations and whenit does, the pollenload is smaller(Table of these two plants. By contrast,flowers of Gaura 4). villosaSMentzeliaS and Argemone are borneat about 60-120 dm height.This suggeststhat the beeflies 2. ANALYSIS OF MIXED POLLEN LOADS may preferto forage amongshorter vegetation at Monahans. Mixed pollen loads are relativelyrare in this analysis,at least comparedto othersimilar recent Othermixed pollen loads studies (Clinebell, 1998; Clinebell & Bernhardt, 1998; Nonnenmacher,1999). This is despite the The only othermixed load encounteredon more fact that all of the taxa studiedhere commonlyoc- than two individualsof any insect species was a curredtogether in mixedspecies stands,with meta- mixedpollen load of Gauracoccinea and Dalea sp. populationsof each plant species usually 50 to indet., foundon five of six male anthophoridbees 1000 individuals.Here we discuss these mixed (Martinapisenteicornis) collected on G. coccineaat loads by sharedplant species pairs. site 5 in the Monahansregion. Again, these flowers are held at a height of about20-30 dm, and may Calylophus-Caurapollen loads representa foragingheight preference. The verylow relativeabundance of mixedpollen The only insect visitors carryingthese mixed loads in this large sample of insect visitors was loadswere females of Sphecodogastradanforthi. We unexpectedand surprising.A possibleexplanation collected this species on both Gauravillosa and may derive from the fact that the data set is so Calylophusberlandieri at the MonahansSandhills heavily loaded with onagradoligoleges namely, (site 9) in August1999, May2000, and May2001. all the antlions,most of the moths and bees (es- Of the 94 females collected with pollen on Caly- peciallyin Sphecodogastraand Evylaeus), and some lophusS13 carriedGaura pollen, of which 12 car- beeflies. This paucityof mixed pollen loads is in ried morethan 50 Gauragrains out of 200 total spite of carefulexamination of pollen wash slides grainscounted, or > 25% (Table5). Of the 20 fe- for virtuallyevery individual insect for whicha po- males collectedon Gaura,one carriedabout equal tentialfor a mixedload existed. amountsof Calylophusand Gaurapollen (Table4). The grainsof C. berlansXieriare smaller,with prom- C()NCIUSl()NS inent basal constrictionsof the aperturalprotru- sions (see Praglowskiet al., 1988, fig. 1G), com- Our primarystudy site at the MonahansSand- pared with the larger grains of G. villosa hills in westernTexas representsa fairly simple (Praglowskiet al., 1988, fig. 2F). plantcommunity that supportsa diversityof insect Littlepollen of any otherplant was recoveredon pollen and nectar foragers.Because this is a hot other individualsof Sphecodogastradanforthi, in- semi-desert community,many insects avoid the dicatingthat this bee is a strongoligolege for On- heat of the day by foragingfrom early eveningto agraceae(McCinley, 2003). Morningsampling of earlymorning, with only a few insect groupsactive both onagradswas roughlyequal, suggestingthat between 10:00 A.M. and 5:00 P.M. Several plant these halictidsprefer Calylophus over Gaura;this species experienceintense and predictableperiods is supportedby the fact that we observedthe bees of visitationby specific insects, usuallycoinciding foragingfor nectar on the Calylophus,whose flowers with the onset of anthesis.An obviousconclusion open in the morning.By contrast,Gaura villosa of this study is that floralvisitation and effective opens in the eveningand its nectaris collectedall pollination-can take place throughoutthe diurnal nightlong by mothsand antlions. cycle, and that some visitorsare activeonly during the night.Another conclusion is that althougheach Calylophus-Thelespermapollen loads plant species has one or a few predominantpollen carrier(s),all species have a diversityof majorpol- Twospecies of beefliesat Monahans(site 9) car- len carriers(> 50 grains),including more than one ried this particularmixed pollen load. Eight of 25 orderof insects in all species except Gauracocci- individuals(32No) of Poecilanthraxcollected on C. nea. berlandiericarried such mixedloads, as did two of Tables11 and 12 indicatethat the majorpollen three Exoprosopasp. 1. Flowersof C. berlandieri carriers(all insects carryingmore than 50 pollen 398 Annals of the Missouri Botanical Garden

- grainsof the plantspecies in questioll)in the Mon- servations (1) Analysisof pollinationguilds is ob- ahans ecosystem are largely non-overlapping scuredwhen a studyarea is overwhelmedby large amongthe seven primaryplant species we studied. populationsof the EuropeanhoneybeeS Apis melli- In part,this may reflectthe floralmorphology and fera (see also Primack& Silander,1975). The gen- time of floweringin the species of Onagraceae.In eral scarcityof honeybeesin ourprimary study site the night-bloomingspecies thosewith shorter (1.5- in the sandhillsof WardCo., Te>;as(site 9) dem- 11 mm) corollatubes (Gauraspp.) attracLmostly onstratesthat the site is relativelypristine7 with its noctuidmoths (Raven& GregoryX1972a) and, in nativepollination guild intact. At our site in Brew- the surprisingcase of G. sillosa>antlions whereas ster Co. (site 2) however the invasive honeybee onagradswith longer(1S50 mm)floral tllbes (Ca- appears as a majorpollen earrierof Calyloph7l3 lylophmshartwegii) attract more sphingid moths harttsegiina species with apparentspecializations (Towner,1977). The day-floweringC. berlar2dieriat- for hawkmothpollination. (2) Disturbedand de- tracts day-flyingbees and other insects, but not graded assembla;es of plant species rnaygive a moths.Even in the day-floweringnon-onagrad spe- similarlydistorted picture of the pollinationguildS cies, there also is little overlapatnong pollen car- comparedwith an undisturbedsite. Ouranalysis of riers. Few comparablestudies that examirlefloral this relativelyintact community shows both a high visitationrates and pollenload throughdillrnal and degreeof pollinatorspecialization and the presence seasonalcycles are available,so it remainsto be of a diversityof relativelyrare insect visitorsas seen if this high degreeof pollinatorspecificity is pollinators. the exceptionor the rule. This reportis the firstin The richnessof the data that can be harvested a series of analysesof NorthAmerican plant com- when studies in pollinati(necology span a variety munitiesthat include Gamra7 Calylo?hzSS and other of co-bloomingdominant plants in differentplant species of Onagraceaein which we intend to ex- familiesis muchmore interesting, it appearsto us, amine the evolutionof pollinationbiology in this than studies that focus on a single speciesagenusS group,and to comparethe communitypollination or family (see also ClinelxellS199&¢ 2004i. Such biologyof these differentassemblages of taxa. communily-levelstudies give an overviewof the Evenwith our relatively large sample sizes, some role a given insect species plays in the overalldy- membersof the eommunitypollinator guikl remain namicof the community,and the degreeof fidelity rarein our dataset. This is particularlytrue for the enjoyedby a given plant st)eciesin the ecosystems largestspecies in variousinsect groups,mThere we These comparisonsallow the use of statisticalanal- collected only single specimensof two large ant- ysis and thus elevate stu(liesof pollinationbiology lionssan underwingnoetuid moth, a beefly,an an- fromthe status of descrilive naturalhistory into thophoridbee, and a Emphoriaflower beetle, each the realmof hypothesis-drivenquantitati+te ecolo;y, the largesttaxon in their group.This may simply as uTellas the identificati(nof probablecoe+tolu- indicatethat these large pollinatorsare less com- tionaryrelationships between plants and insects mon,but it also suggeststhat ollr description of this guild may be incomplete. LiteratureCitecl An apparentlyunavoidable cost in the census of species is the collectionof Bedichek R. A 1947. Advenlureswith a TexasNatllral- these rare po11inating ist. tJniv.Texas Press, Austin. largenumbers of the commonerspeeies in tlle com- BultaC. J. & Et A. Zimmer.199:3. Sllelear ribosortlal RNA munity.However, understandin$ the biology and sequeneesfor interringtrihal relatiotlships within Orl- behaviorof these raretasa and the role(S)they play agraccae.Systt Bot. 18: 48-63. in naturalcommunities may be critical to under- CarrSB. L. J. At.Crisci 8z P (2. Hech. 1990. A clacllstic analysisof the genus&amru (Onagraccae). Sysl. Bot. 15 standingthose c-ommunities.Some of the taxa that 454 Ibl. are rare in OU14 analysismay be more commonat ClinebellIIv R. R. 19943.The PollitlationBiology of thc othertimes forexample, mThen the communitiesare Genlls Penstemon(Scrophulariaceae) in the Tallgrass not experiencing droughtcontlitions. Pettersson Prairiet 3PhI). DlssertatiorlaSaint Louis University. (1991) found strong yearto-yearvariation in the [llniversityMicrofiltns.] . SQ04.toraging ecology of selectedprairle wild- abundanceof pollinatingmoths on Silerlev7l1garis flowers(EchinaceaS Liatris7 Monard and Ybronicasv in Sweden.We suggestthat sustailledand detailed tram)in Missouripraitie remnants and restorations Pp. studiesthat inelude a moderateamount of repeated 194212 irzS. Fore (editor) Proceedirzgsof the 18th collecting o+rerseveral years ate essential to elu- NorthAtnerican Prairie Conference. KirksvilleS Missou- ri. cidatingthe roles of rarespecies. & P Bernhardtt1998. The polliratlonecology of In terms of comtmlnitypollination ecology in five species of Penstemo7X.in the tallgra$sprairie. Ann. westernNorth America ourresults prortlpt two ob- MissouriBot. Gard.85: 126136. Volume 91, Number 3 Clinebell et al. 399 2004 Pollination Ecology

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