Bat and Hummingbird Pollination of an Autotetraploid Columnar , Weberbauerocereus weberbaueri (Cactaceae) Author(s): Catherine T. Sahley Source: American Journal of Botany, Vol. 83, No. 10 (Oct., 1996), pp. 1329-1336 Published by: Botanical Society of America Stable URL: http://www.jstor.org/stable/2446118 . Accessed: 03/12/2014 11:09

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This content downloaded from 192.135.179.249 on Wed, 3 Dec 2014 11:09:35 AM All use subject to JSTOR Terms and Conditions AmericanJournal of Botany 83(10): 1329-1336. 1996.

BAT AND HUMMINGBIRD POLLINATION OF AN AUTOTETRAPLOID COLUMNAR CACTUS, WEBERBA UEROCEREUS WEBERBA UERI (CACTACEAE)'

CATHERINE T. SAHLEY2

Departmentof Biology, Universityof Miami, Coral Gables, Florida 33124

I presentdata on flowermorphology, pollination, breeding system, and genetic diversityof the columnarcactus Weber- bauerocereus weberbaueriat 2500m elevation in southwesternPeru. Weberbauerocereusweberbaueri is a self-compatible columnarcactus thatis visited and pollinatedby one of rare endemic bat, Platalina genovensium,and two species of hummingbirds,Patagona gigas and Rhodopis vesper. W. weberbaueriexhibits pronounced interplant variation in floral color and size, and flowersexhibit traitscorresponding to both bat and hummingbirdpollination syndromes.Starch-gel electrophoresisof flowerbud tissue indicated that W. weberbaueri is an autotetraploidand that genetic diversity(Hep = 0.257) of the studypopulation was high relativeto diploid plantsbut similarto othertetraploid species. Initial fruitset from pollinatorexclusion experimentsconducted in 1991 and 1993, at the onset of and aftera droughtassociated with the El Ninioevent of 1991-1992, revealed thatbats were the most importantpollinators in 1991, but thathummingbirds and diurnal insects were most importantin 1993. In both years,however, autogamy and lepidopteranlarval infestationof fruitsreduced differencesin maturefruit production among pollinatorexclusion treatmentsso thatdifferences in maturefruit set were not statisticallysignificant. Reduced bat pollinationin 1993 is attributedto the reduced abundance of bats at the study site duringa droughtcaused by El Niiio. I hypothesizethat interaction among several factors,including tetraploidy, autogamy, larval infestationof developing fruits,and variationin pollinatorabundance, may not resultin strongselection for a bat vs. hummingbirdfloral morph, thus allowing the persistenceof floralvariation in this cactus.

Key words: Andean habitats;bats; Cactaceae; hummingbirds;Peru; pollination;polyploidy; Weberbauerocereus.

In arid habitats,a large proportionof plantsbelonging share several characteristics,evolutionary transitions be- to the Cactaceae and Agavaceae exhibitfloral adaptations tween these syndromeswithin a lineage may occur for bat and/orhummingbird pollination (Porsche, 1939; relativelyfrequently (Helverson, 1993). In fact, several Vogel, 1969). Several recentfield studies in Mexico, Cu- plantfamilies (including the Cactaceae), genera,and even ragao, and Venezuela have experimentallydemonstrated species, exhibitfloral traits corresponding to bothbat and the importanceof bats (Nassar, 1991; Petit, 1995; Flem- hummingbirdpollination syndromes(e.g., Barthlottand ing, Tuttle,and Horner,in press) and/orhummingbirds Hunt, 1993; Helverson, 1993; Kress and Stone, 1993; (Fleming, Tuttle,and Horner,in press) as pollinatorsof Sazima, Sazima, and Buzato, 1994) yet few studieshave columnar cacti. Traits associated with bat pollinationof compared the relativecontribution of these pollinatorsto cacti include large, funnelform,nocturnal, white, and fruitand seed set. pungent-smellingflowers that produce large amountsof The purpose of this study was to investigatethe im- pollen and nectar."Hummingbird" flowers, on the other portanceof bat and hummingbirdpollination in Weber- hand, tend to be tubular,red, diurnal,and odorless, but bauerocereus weberbaueri (tribe ), a co- may also produce copious nectar and large amounts of lumnarcactus occurringin southwesternPeru thatexhib- pollen (Faegri and van der Pijl, 1979; Helverson, 1993). its floraltraits associated withboth bat and hummingbird Perhaps because bat and hummingbirdfloral syndromes pollination.Several factorsmotivated this study:first, the arid regions of Peru contain the second richest cactus floraafter Mexico, with -44 genera and 249 species dis- i Manuscript received 28 June 1995; revision accepted 21 March tributedprimarily along the westernAndean slopes (We- 1996. diversity, The authorthanks M. Donnelly, T. Fleming, J. Hamrick,D. Janos, berbauer,1945; Hunt, 1992). Yet, despite the C. Horvitz, K. Lips, M. Nelson, K. Waddington,and membersof the abundance, and prominence of these , virtually plant-animal interactionsgraduate discussion group of the University nothingis known regardingtheir ecology and reproduc- of Miami for valuable discussion, assistance, and comments;L. Bar- tive biology. Second, habitatsoccurring along thewestern aybar forassistance in the fieldthroughout the durationof the study;J. slopes of the Andes are underrepresentedwithin Peru's Estefaneroand J. Ugarte for assistance at the outset of the study; P nationalreserve system,and have been rankedas deserv- Jimenez for importantlogistic advice; E. Linares for assistance with researchand conservation(Centro plant identification;P Baldizan for graciouslypermitting the authorto ing of high priorityfor conduct researchon his property,and J. Hamrick of the Universityof de Datos para la Conservacion, 1986). Third, the only Georgia for kindlyallowing me the opportunityto work in his labora- nectarivorousbat occurringat mid-to-highelevation sites tory.Funds for this researchwere provided by grantsfrom New York in southwesternPeru, Platalina genovensium,is an ex- Zoological Society-TheWildlife Conservation Society, a WorldWildlife tremelyrare and endemic bat for which no ecological Fund-Garden Club of America Scholarship in Tropical Botany, Bat informationexisted prior to this study.Finally, W. we- ConservationInternational, and a Maytag GraduateFellowship fromthe varia- College of Arts and Sciences, Universityof Miami. berbaueri exhibitsconsiderable within-population 2 Currentaddress: CONATURA, Apartado 688, Arequipa, Peru (Fax: tion in several floralmorphological characters including 5154 424372). size, shape, and color, althoughthis variationhad never 1329

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350

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4- C 150

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0n 62 63 64 65 66 67 68 69 70 71 81 82 83 84 85 86 87 88 89 90 91 92 93 Year Fig. 1. Rainfall data for 1962-1971 and 1981-1993 forthe Characato weatherstation (2400 m above sea level). This stationis 15 km from the main studysite and occurs withinthe same life zone. El Nifnoevents occurredin 1963-1965, 1969, 1972-1973, 1976, 1982-1983, and 1991- 1992 (no rainfalldata was available for 1969 and 1972-1973 events). Rainfall data from1961 to 1976 fromONERN, 1974. previouslybeen quantified.Among-plant variation in flo- tus in the region around the city of Arequipa (Aragon, 1982; C. T ral color ranges frombright pink-red to white.This vari- Sahley, personal observation).Although the populationaround Arequi- ation in floral color, along with the presence of long, pa has been classifiedas threespecies by Ritter(1981), the continuous stout,funnelform-tubular corollas and both diurnal and variationamong plants in flowermorphology and color and the lack of nocturnalnectar production, suggests adaptationto both any diagnosticalleles among morphs,has led me to consider them as bat and hummingbirdpollination. Prior to this study, one highlyvariable species, W. weberbaueri,in accordance with Hunt however,the relativeimportance of bat and hummingbird (1992). pollination for fruitproduction in W. weberbaueri was Flowers of W. weberbaueri are hermaphroditic,begin opening be- unknown. tween 1500 and 1700, remainopen throughoutthe night,and generally To elucidate possible ecological and genetic mecha- close by 1100 the followingmorning. Nectar productionis continuous, but variable, while the floweris flower nisms contributingto the presence of floralmorphologi- open (Sahley, 1995). Although and fruitproduction peaks in Septemberand October,some flowerand cal variationin this cactus, I addressedthe followingfive fruitproduction occurs year-round(Sahley, 1995). Weberbauerocereus questions: (1) What is the morphologicaland geneticdi- weberbaueriis visitedby the rare and endemic nectar-feedingbat, Pla- versityof W. weberbaueri at the studysite? (2) What is talina genovensium(Phyllostomidae), two species of hummingbirds, the extentof outcrossingvs. selfingoccurring within the Patagona gigas and Rhodopis vesper (Trochilidae),small, unidentified studypopulation? (3) What is the relativeimportance of nocturnalmoths, diurnal flies, bees, and rarely,butterflies (C. T Sahley, bats, hummingbirds,and insects as pollinatorsof W. we- personal observation). berbaueri and is the importanceof pollinatorsconstant between years? (4) What factors,in additionto effective Flower and fruit morphology-My observationsindicated that vari- pollinationof flowers,influence successful development ation in floralmorphs was among, ratherthan withinplants, so I col- of maturingfruits? Finally, because this studycoincided lected one flowerfrom each of 97 cacti in 1991 and one flowerfrom with the occurrenceof the 1991-1992 El Nifnosouthern 22 additional cacti in 1993. Unfortunately,low flowerproduction per oscillation, (5) How did climatic fluctuationsassociated plant coupled with the necessityof using flowersfor exclusion experi- with El Nifio influencethe pollination biology of this mentshindered efforts to collect additionalflowers per plantduring the cactus? course of the study.However, long-term, repeated observations of plants confirmedthat basic floralattributes such as color, shape, and presence MATERIALS AND METHODS or absence of stigma exsertion were at least qualitativelyconsistent withinplants. I recorded outer corolla tube length,outer corolla tube Study site and study organisms-The main study site is located in width at both widest and narrowestpoints, petal length,stigma exser- the departmentof Arequipa, Peru, 25 km south of the city of Arequipa tion, and style length.The numberof stigma lobes, corolla tube color, (16.27? S, 71.300 W) on the westernslopes of the Andes, at -2500 m and petal color were also recorded.As the studyprogressed, additional elevation. The site correspondsto the subtropicallow-montane desert floralcharacters were measured. Thus, in 1993 I also recorded ovary scrub life zone according to the Holdridge system (ONERN, 1976). length,width, and innercorolla tube lengthand width.Petal color was Average annual rainfallfor this life zone is 222 mm/yr,but varies sub- scored in one of four categories: white,white tinged with varyingde- stantiallyamong years. Between 1990 and 1993, forinstance, a drought grees of reddishbrown, maroon, and brightpink-red. associated withan El Ninioevent resulted in a drasticdecrease in rainfall I collected one mature fruitfrom each of 115 plants. Fruits when at the site (Fig. 1). immaturewere green and took -2 mo to mature; when maturethey Weberbauerocereusweberbaueri is the most abundantcolumnar cac- usually changed color and soon afteropened to expose the fruitpulp

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and seeds. I recorded width and lengthof all fruitsand externalfruit TABLE 1. Pollinatorexclusion treatmentsperformed in 1991 and 1993 color of 69 fruits.Seeds were counted from 14 open-pollinatedfruits, for Weberbauerocereusweberbaueri. and individual seed masses were recorded for five seeds per fruitfor Treat- 26 fruits. ment num- Pollination Descriptionof Flower visitors ber treatment flowertreatment allowed Genetic diversityand matingsystem-To sample geneticdiversity in the studypopulation, flower bud tissue was collected from25 adults in 1 Open No treatment Insects,bats, 1993. Bud tissue was crushedwith liquid nitrogenprior to additionof hummingbirds 2 Total exclusion Bridal veil during None phosphate-polyvinylpyrrolidone(PVP) extractionbuffer. For themating entiretime flower system one mature analysis, fruitwas collected fromeach of 31 plants. open Seeds were germinatedon moist filterpaper in petri dishes inside 3 Diurnal exclusion Bridal veil netting Bats, nocturnal growthchambers. Germination usually occurredwithin 10-14 d. Six to duringday insects 24 seedlingsat the cotyledonstage (-3 wk old; mean numberseedlings 4 Nocturnalexclusion Bridal veil netting Hummingbirds, per fruit= 14) per fruitwere preparedfor electrophoresisby crushing duringnight diurnalinsects with a PVP extractionbuffer (see Mittonet al., 1979). 5 Diurnal and bat Bridal veil netting Nocturnalinsects Starch gel electrophoresiswas performedon preparedtissues using exclusion duringday and buffersystems and stainingrecipes of Soltis et al. (1983). Eightenzyme wire mesh during night systemswith 15 loci were assayed for the bud tissues. Of these, one 6 Nocturnaland Bridal veil netting Diurnal insects probablemonomorphic (Pgm- 1) and two polymorphicloci (Fe-2, Aat-1) hummingbird duringnight and were not consistentlyscoreable and were not used in analyses. The exclusion wire mesh during enzyme systems and loci used were: phosphoglucoisomerase(Pgi- 1, day Pgi-2), alcohol dehydrogenase(Adh), phosphoglucomutase(Pgm-2), mannose reductase (Mnr-1), fluorescentesterase (Fe- 1), triose-phos- phate isomerase (Tpi-1, Tpi-2, Tpi-3), leucine-aminopeptidase (Lap), flowersbut excluded nocturnalvisitors; (5) bat and diurnalexclusion, 6-phosphogluconatedehydrogenase (6PGD), and aspartateamino trans- which permittedaccess to nocturnalinsects only; and (6) hummingbird ferase (Aat-2). Buffersystem 8- was used forFe, Mnr, and Aat, system and nocturnalexclusion, which permittedaccess to diurnalinsects only 11 for Pgm and 6PGD, and system 34 for Tpi, Adh, and Lap. Adult (Table 1). Materials used to exclude potentialpollinators consisted of genotypeswere scored forall of the above loci. Only Adh-1, Lap, Tpi-3, either2.54 cm (1 inch) hexagonal wire mesh (used to exclude verte- Aat-1, Mnr, and 6PGD were used in matingsystem analyses. Maternal brates,but not insects) or bridal veil netting(used to exclude all visi- genotypeswere inferredfrom the genotypesof the seedlings. tors). For treatment(1), no excluderswere used, while fortreatment (2) Electrophoreticdata from flower bud tissue collected from adult (total exclusion) bridal veil nettingwas placed over the flowerprior to plants were used to calculate the following genetic parametersas in opening and removed afterthe flowerclosed the following day. The Hamrick and Godt (1990): percentagepolymorphic loci, mean number diurnalexclusion treatmentconsisted of puttingbridal veil nettingover of alleles per locus, and genetic diversity.Genetic diversity(Hep) was the flowerin the late afternoonprior to opening,removing the netting calculated for each locus as Hep = 1 - Jp,2, wherepi is the frequency at sunset (between 1740 and 1800), and replacing it again just before of the ith allele. An overall mean Hep was obtained by averagingover sunrise (between 0445 and 0515). The nocturnalexclusion treatment all loci. consisted of placing bridal veil nettingover flowersafter opening at To determinethe degree of outcrossingvs. selfingin the population, sunset and removingthe nettingthe following morningjust prior to genotypicdata from416 seedlings of 31 open-pollinatedfruits were sunrise.Treatment (5), the bat and diurnalexclusion, involved placing analyzed using the multiallelicversion of the TETRAT programwritten bridal veil over flowersprior to opening and replacing the bridal veil by Ritland (1990), which is fullydescribed in Murawski et al. (1993). nettingwith wire mesh at sunset. Before sunrise,the wire mesh was The programinferred maternal genotypes from their progeny arrays by again replaced withbridal veil netting,which was removedthe follow- calculatingprobabilities of progenyderived fromselfing and outcross- ing day afterflowers had closed. Treatment(6), the hummingbirdand ing and then calculated population-levelmultilocus and single-locus nocturnalexclusion, involved placing wire mesh excludersover flowers estimates of outcrossingrates. The programalso calculated standard priorto opening and replacingthe wire mesh excluderswith bridal veil errorsof the estimatesusing the bootstrapmethod. Fifty among-family nettingat sunset. Before sunrise,the bridal veil nettingwas replaced (i.e., fruit)bootstraps were used forpopulation estimates. with wire mesh, which was removed later that day afterflowers had closed. Pollinator exclusion experiments-Pollinatorexclusion experiments All cacti used in the pollinatorexclusion experimentswere tagged were conductedfrom September to November in 1991 and 1993. Rep- and numbered.Each experimentalflower was also individuallytagged lication of experimentsin 1992 was not feasible due to the extremely and numberedusing soft aluminumtags insertedinto the cactus 2 cm low floweringfrequency of W. weberbauerithat year. Flowers from48 below the flower.Each flowerwas censused once a week untilthe fruits plants in 1991 and 51 plants in 1993 were subjected to six pollination matured.I recordedwhether flowers and fruitswere on or offthe plant, treatmentsin a randomizedblock design, so thatwhen possible, each whetherfruit development had initiated(indicated by swelling of ova- plant underwentall six treatments.Because daily floweringfrequency ries 1 wk aftertreatment; this was used as an indicationof effective is low in W. weberbaueri,generally only one treatmentper nightper pollination),and presence or absence of lepidopteranlarval infestation. plant was applied; exclusion experimentsthus took several weeks to Afterfruits began to develop, 0.635 X 0.635 cm (1/4inch) wire mesh complete. In a few instances,more than one treatmentper nightwas was placed over themto preventfruit predation by vertebrates.In 1991 applied to a plant. This occurred when it appeared that not enough all undamaged, mature experimentalfruits were collected and their flowerswould be available in the futureto complete the experiment. seeds were storedin labeled envelopes. Seeds from14 open-pollinated The pollinatorexclusion treatmentsapplied in 1991 and 1993 were: (1) fruitswere countedand weighed,and all seeds fromthe other treatments open control,which allowed access to all flowervisitors; (2) total ex- were weighed. In 1993 fruitset was recorded,but fruitswere not col- clusion, which prohibitedaccess to all visitors; (3) diurnal exclusion, lected. which permittedbats and nocturnalinsects access to flowers,but ex- cluded diurnalvisitors such as hummingbirdsand insects; (4) nocturnal Statisticalanalyses-Data fromthe pollinatorexclusion experiments exclusion, which permittedhummingbirds and diurnalinsects access to were analyzed using SYSTAT version 5.3 (Wilkinson,1991) and SAS

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TABLE 2. Morphological measurementsfor flowersof Weberbauerocereusweberbaueri. Coefficients of variationare in parentheses.

Outer corolla Outer corolla Outer corolla tube width tube width Petal Style Stigma Numberof Ovary Ovary tube length (widest) (narrowest) length length exsertion stigma length width (cm) (cm) (cm) (cm) (cm) (mm) lobes (mm) (mm) Mean 7.57 2.20 1.45 2.08 7.49 7.2 11.49 7.02 7.4 (0.11) (0.12) (0.11) (0.15) (0.15) (0.79) (0.12) (0.32) (0.13) N= 96 N= 71 N= 69 N= 95 N= 92 N= 92 N= 51 N= 21 N= 22 Minimum 5.2 1.5 1.0 1.2 3.5 0 8 3.7 5.8 Maximum 10.3 2.9 1.9 2.9 10.5 2.5 15 14.9 9.1

(SAS, 1989). Differencesamong treatmentsin the frequencyof fruit mained open until late morning (between 0900 and initiationand fruitmaturation were analyzed using an experimentwise 1100). likelihoodratio x2 statistic(G statistic;Sokal and Rohlf, 1981) foreach Mature fruits(N = 69) rangedin color frombright red year and forboth years combined. Individual treatment G statisticswere (23%), to orange-red(29%), orange (23%), orange-yel- also calculated for each year and both years combined followingthe low (4%), yellow (4%), and green (15%). Seed number procedure in Sokal and Rohlf (1981). Chi-square tests were used to and seed mass in W. weberbaueri were more variable conductpairwise comparisonsbetween the diurnaland diurnalplus bat than fruitlength and width (Table 3). The number of exclusion treatments,as well as between the nocturnaland nocturnal seeds per fruitranged from 181 to 1 533; individualseeds plus hummingbirdexclusion treatments.The G statisticwas also used on average weighed slightlyless than 0.001 g. to analyze differencesin fruitinitiation frequencies and the proportion of maturefruit set between years as well as between-yeardifferences in frequencyof larval infestationand fruitmortality due to larval in- Genetic diversityand mating system-Banding pat- festation. terns obtained from assays of all polymorphicenzyme Seeds frommature fruits collected in 1991 were weighed to the near- systemsin all individualsindicated that W. weberbaueri est 0.0001 g. A Pearson product-momentcorrelation coefficient was is an autotetraploid.Both balanced and unbalanced het- calculated to determinethe relationshipbetween total seed mass and erozygote banding patterns,corresponding to equal and seed numberper fruitfor the 14 open-pollinatedfruits. A one-wayanal- unequal combinationsof alleles, were present in adult ysis of variance was performedto analyze differencesin totalseed mass and offspringtissues. Fixed heterozygotes,which would per fruitamong treatments.Because treatments(5) and (6) did notdiffer be expected to occur in allotetraploids,were never ob- significantlyfrom the total exclusion treatmentfor both fruitinitiation served for any enzyme system. and mature fruitset in eitheryear or in both years combined, seeds Of the 12 resolvable loci assayed, eight (66.6%) were fromthese treatmentswere pooled withthe total exclusion treatmentin polymorphic.The number of alleles in adult heterozy- orderto increase sample size. gotes ranged fromtwo to four per locus per individual plant (Table 4); the mean numberof alleles per locus was RESULTS Flower and fruit morphology-W. weberbaueriflow- ers were tubularto slightlyfunnelform in shape; flowers TABLE 4. Allele frequenciesof eightpolymorphic loci foradult plants were long, rangingfrom 5.2 cm to 10.3 cm, and corolla at the main study site. Tpi-1, Tpi-2, Pgi-1, Pgi-2 were monomor- tube widthwas narrow,especially just above the nectary phic.

(Table 2). The most variable floralmorphological char- Allele Allele Genetic diversity Locus designation acters were petal length,ovary length,style length,and frequency (He,) lengthof stigmaexsertion (Table 2). Despite variationin FE- I 1 0.408 0.704 style and stigma exsertion length,most flowers (82%) 3 0.276 exhibited some degree of exsertion.The most common 4 0.197 petal color (N = 117) was white tinged with varying 5 0.118 degrees of reddish-brown(42%) followed by white MNR 2 0.927 0.135 3 0.073 (38%), maroon (14%), and pink-red(6%) Within-plant PGM-2 2 0.307 0.425 flowercolor was constantand did not exhibitseasonal or 3 0.693 annual variation.All flowersregardless of shape or color, 6P-2 2 0.546 0.516 opened between 1500 and 1700 (priorto sunset) and re- 3 0.432 4 0.023 AAT-2 3 0.875 0.219 4 0.125 TABLE 3. Fruitmorphology of Weberbauerocereusweberbaueri. Co- TPI-3 3 0.890 0.196 efficientsof variationare in parentheses. 4 0.110 ADH 1 0.060 0.267 Fruitlength Fruitwidth Seed number Individual 3 0.850 (mm) (mm) per fruit seed mass (g) 4 0.080 Mean 27.0 30.6 1067 0.0009 5 0.010 (0.15) (0.14) (0.39) (0.31) LAP 2 0.227 0.625 N= 115 N= 113 N= 14 N= 133 3 0.546 Minimum 15.7 18.4 181 0.0004 4 0.113 Maximum 37.5 41.5 1533 0.0020 5 0.114

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TABLE 5. Proportioninitiated and maturefruits for Weberbauerocereusweberbaueri accordingto pollinatorexclusion treatment.G statisticsare in parentheses.

1991 1993 1991-1993 Combined Initiated Mature Initiated Mature Initiated Mature Treatment N fruits fruits N fruits fruits N fruits fruits Open 51 0.55 0.35 44 0.64 0.25 95 0.59 0.30 Total exclusion 40 0.40 0.28 40 0.48 0.25 80 0.44 0.26 (5.1099)* Diurnal exclusion 40 0.70 0.48 43 0.60 0.16 83 0.65 0.32 (5.534)* Nocturnalexclusion 41 0.56 0.37 46 0.76 0.35 87 0.67 0.35 (4.927)* (3.8610)* Bat and diurnalexclusion 32 0.38 0.31 39 0.54 0.26 71 0.46 0.28 Hummingbirdand nocturnalexclusion 30 0.47 0.20 42 0.60 0.26 72 0.54 0.23 ExperimentwiseG statistics 234 11.177* 7.003 254 8.671 4.128 488 14.769* 3.127 * P < 0.05 (likelihood ratio x2 to test hypothesisof equal proportionsamong treatments).

2.25. Mean genetic diversity(Hep) of adults in the study ed in 1993 were not significant(G = 8.671, df = 5, P population was 0.257. > 0.05). Examination of the contributionsof individual Analysis of the matingsystem of open-pollinatedseed- treatmentsto the overall G statisticindicates that in 1993, lings from 1991 indicated that population outcrossing only hummingbird-and diurnal-insect-visitedflowers levels were high based on both multilocus(tm = 0.937, (nocturnal exclusion) resulted in a significantlyhigher SE = 0.042) and single locus (ts = 0.869, SE = 0.047) proportion(76%) of fruitsinitiated (G = 4.927, df = 1, estimates. P < 0.05) relativeto expected values. Pairwise compar- ison to the hummingbirdand nocturnalexclusion treat- Pollinator exclusion experiments-Fruit initiation mentdid notreveal a significantdifference (X2 = 0.086, frequencies-Data on fruitinitiation frequencies indicat- P = 0.768), indicatingthat in additionto hummingbirds, ed thatbats, hummingbirds,and diurnalinsects effective- diurnalinsects may have played a role in pollination.As ly pollinate W. weberbaueriflowers but thatflowers also in 1991, a relativelyhigh proportionof flowers (48%) produce fruitsin the absence of flowervisitors (Table 5). developed fruitsin the absence of flowervisitors. In 1991, fruitinitiation frequencies among pollinatorex- When data from1991 and 1993 are combined,differ- clusion treatmentsdiffered significantly (G = 11.177, df ences among treatmentswere significant,with the noc- = 5, P < 0.05). The diurnalexclusion treatment(bat plus turnalexclusion treatment(hummingbird and diurnalin- nocturnalinsect pollination)accounted for a significantly sect pollination) contributinga significantlygreater pro- higherproportion of fruitsinitiated (70%; G = 5.534, df portionof developing fruits(G = 3.861, df = 1, P < = 1, P < 0.05) than the otherfive treatments.Pairwise 0.05) and the totalexclusion treatmentcontributing a sig- comparisonbetween the diurnalexclusion treatmentand nificantlysmaller proportion of fruits(G = 5.1099, df the bat and diurnal exclusion treatmentrevealed a sig- 1, P < 0.05). nificantdifference, (X2 = 6.34, P = 0.01), indicatingthat the high fruitinitiation frequency for the diurnalexclu- Maturefruit set-In 1991, the diurnalexclusion treat- sion treatmentwas due to bat, not nocturnalinsect pol- ment (bat pollination) resultedin the largestproportion lination.Remaining treatments were not significantlydif- of maturefruits (48%), while in 1993, the nocturnalex- ferentfrom the hypothesisof equal proportionsamong clusion treatment(hummingbird and diurnal insect pol- treatments.Forty percent of flowersfrom which all flow- lination) yielded the largestproportion (35%) of mature er visitorswere excluded initiatedfruit development, in- fruits(Table 5). However, differencesin maturefruit set dicatingthe presence of self-compatibilityand autogamy among treatmentsin both 1991 and 1993 were not sig- in W. weberbaueri. Because flowers in this treatment nificantat the experimentwiseor individual level, nor were not emasculated, however,the possibilityof apo- were theysignificant when data for 1991 and 1993 were mixis having occurredcannot be ruled out. combined. In contrastto 1991, differencesin fruitinitiation fre- Total seed mass per fruitwas highly correlatedwith quencies among pollinatorexclusion treatmentsconduct- the total numberof seeds (r = 0.915, P < 0.001). How- ever, differencesin total seed mass for mature experi- mental fruits collected in 1991 were not significant TABLE 6. Total seed mass per fruitby pollinatorexclusion treatment among treatments(one-way ANOVA, F = 0.727, P = in 1991. Data fromthe total exclusion treatmentwere pooled with 0.539; Table 6). bat and hummingbirdexclusion treatments. Between-year comparisons-In 1993, fruitinitiation Mean total seed No. of mass per frequencies were significantlyhigher for the nocturnal Pollinatorexclusion treatment fruits fruit(g) SD exclusion treatmentthan in 1991 (G = 3.920; df = 1, P Open 22 0.838 0.460 < 0.05; Table 7). However, differencesin mature fruit Total exclusion 23 0.842 0.550 set between years for the nocturnalexclusion treatment Diurnal exclusion 28 1.00 0.406 were not significant.The most marked differencebe- Nocturnalexclusion 15 0.789 0.292 tween years was the decrease in maturefruit set by bat-

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TABLE 7. Fruitinitiation and maturefruit set comparedbetween years never demonstratedany formof damage due to flower for Weberbauerocereusweberbaueri. Numbers indicate G statis- visitors. Preliminaryobservations indicate that because tics. open-pollinatedflowers were never covered withnetting, 1991 vs. 1993 theymay have been exposed to a higherdegree of larval Initiated Mature infestationthan the other treatments.This may have Treatment Flowers fruits fruits caused the slightlylower fruitinitiation frequencies, but Open 95 0.747 1.190 since I did not want to unintentionallydamage flowers Total exclusion 80 0.457 0.065 by checkingthem for larvae, this possibilityneeds to be Diurnal exclusion 83 0.832 9.243** exploredfurther. Nocturnal insect visitation to flowersdid Nocturnalexclusion 87 3.920* 0.010 not significantlycontribute to eitherfruit initiation or ma- Bat and diurnalexclusion 71 1.236 0.273 turefruit set in eitheryear, while diurnalinsect visitation Hummingbirdand nocturnalexclusion 72 1.166 0.077 contributedto fruitinitiation in 1993 only. Differencesin * P < 0.05; ** P < 0.01 (likelihood ratio x2 fordeviation of expected mature fruitset among pollination treatmentswithin a ratio of 1:1 for each pollinationtreatment). year were statisticallyundetectable, as were differences in seed production.The importanceof bats as pollinators varied between years withthe proportionof bat-pollinat- visited flowers (diurnal exclusion) in 1993 relative to - ed flowersbeing greaterin 1991 than in 1993. In 1993, 1991 (G 9.243, P < 0.001). Despite the variabilityin hummingbirdsand diurnalinsects were the most impor- bat and hummingbirdpollination effectiveness, both fruit tantpollinators. Lepidopteran larval infestationand sub- initiationfrequencies and maturefruit set for open-pol- sequent fruitmortality were greaterin 1993 thanin 1991. linated flowersdid not differsignificantly between years. Despite variabilityin pollinatoreffectiveness as measured The proportionof both autogamous initiatedand mature by fruitinitiation frequencies, mature fruit set of open- fruitswas also constantfrom year to year. pollinated flowers did not differsignificantly between 1991 and 1993. Larval infestationof developingfruits-Infestation of developing fruitsby unidentifiedlepidopteran larvae oc- curredin both 1991 and 1993 and had a pronouncedef- Genetic and morphological diversity-Polyploidy is fect on fruitsurvivorship. Fruit mortalityin developing, frequent(35-47% of species) in angiosperms (Grant, open-pollinatedfruits ranged from36% in 1991 to 61% 1971; Stebbins, 1971), and the Cactaceae are no excep- in 1993; of these, 11% and 39%, respectively,were pos- tion.Pinkava et al. (1985) foundthat 27.9% of 551 cactus itively identifiedas being due to larval infestation.This taxa analyzed were polyploid. Polyploidy has been hy- differencein fruitmortality due to larval infestationbe- pothesized as having several advantages and/orconse- tween years was statisticallysignificant (G = 7.74, df = quences. For example, polyploidyenhances the capacity 1, P = 0.005). Differencesin fruitmortality among pol- of individuals and populations to "store" genetic varia- linatorexclusion treatmentswere not significantlydiffer- tion (Briggs and Walters,1990). Several theoreticaland ent in 1991 or in 1993 (G = 5.051, df = 5, P = 0.410; empirical studies have shown that autotetraploidshave G 3.689, df = 5, P = 0.595, respectively). higher heterozygosityrelative to diploids (Ness, Soltis, and Soltis, 1989; Soltis and Soltis, 1989; Wolf, Soltis, DISCUSSION and Soltis, 1990; Moody, Mueller,and Soltis, 1993). Ge- netic diversityof W. weberbauerocereus in the study Flower shape, color, and nectarproduction of W. we- populationis highcompared to diploid plantswith similar berbaueri at the study site are consistentwith bat and mating systems,but is similar to estimatesin otherau- hummingbirdpollination syndromes. Results of this totetraploidplants (Table 8). study indicate that bats, hummingbirds,and diurnal in- A second advantage to polyploidyis the release of ge- sects visit and pollinate flowersof W. weberbaueri.Nev- netic variation and a consequent increase in ecological ertheless,a large proportion(26%) of flowersfrom which amplitude and geographical distributionrelative to dip- all visitors were excluded set fruit,indicating the pres- loids (Briggs and Walters,1990; Brochmannand Elven, ence of self-compatibilityand autogamy(or possiblyapo- 1992). Previous authors(Backeberg, 1976; Ritter1981) mixis) in this cactus. Mating systemanalysis, however, have noted the morphological variation present within suggests thatif flowersare visited,they are highlyout- and among populations belonging to the Weber- crossed. bauerocereus but have assumed that this variationwas Interestingly,in neitheryear was the open pollination due to interspecificdifferences. This studysuggests that treatmentthe most successful. Open-pollinatedflowers only one species is presentin the vicinityof Arequipa

TABLE 8. Levels of heterozygosityin W. weberbaueriand otherautotetraploid and animal-outcrossingdiploid plants.

Plant species Heterozygosity Source Weberbauerocereusweberbaueri (Cactaceae) 0.257 (Autotetraploid) This study Pachycereuspringlei (Cactaceae) 0.209 (Autotetraploid) J. Hamrick (Universityof Georgia) and T. Flem- ing (Universityof Miami, unpublisheddata) Heuchera grossularifolia(Saxifragaceae) 0.159 (Autotetraploid) Wolf, Soltis, and Soltis (1990) Tolmiea menziesii(Saxifragaceae) 0.237 (Autotetraploid) Soltis and Soltis (1989) Mixed-animal outcrossing(mean value, N = 85) 0.120 (SD = 0.015) (Diploid species) Hamrick and Godt (1990)

This content downloaded from 192.135.179.249 on Wed, 3 Dec 2014 11:09:35 AM All use subject to JSTOR Terms and Conditions October 1996] SAHLEY-BAT AND HUMMINGBIRD POLLINATION 1335 and thatmuch of the intrapopulationalvariation may be genovensiumindicates that in Arequipa, it specializes on because of high heterozygositycaused in part by auto- cactus flowersand fruit,and no other species of cactus tetraploidy. produced flowersor fruitduring the drought,it is prob- able that bats emigratedfrom the studyarea duringthe Mating system-Analysis of the matingsystem of W. drought (Sahley, 1995). While I did not census hum- weberbaueri based on fruitscollected in 1991 indicated mingbirdssystematically, one of two species, Rhodopis that most seedlings were outcrossed (tmn= 0.937); this vesper, was consistentlyobserved throughoutthe entire was probablybecause both bats and hummingbirdswere study.Because of the small size of this bird (-4.5 g), its presentthat year and high visitationrates resulted in high total energeticrequirements are lower than those of P. levels of outcrossing.Unfortunately I did not estimate genovensium (average mass = 19 g; Sahley, 1995). outcrossingrates in 1993, when the proportionof bat pol- Therefore,in addition to being able to subsist on fewer lination was low. Because the increase in homozygosity flowersthan P. genovensiumduring times of low flower due to selfingis farless fora tetraploidthan for a diploid abundance, R. vesper was also able to feed fromplants (Moody, Mueller,and Soltis, 1993), facultativeautogamy that produced small flowersthat would have been un- and self-compatibilityin W. weberbaueri may be an ef- available to bats (C. T. Sahley, personal observation).If, fectivestrategy in years when importantpollinators such as the data suggest,flower, fruit, and bat abundance de- as bats are absent. crease near Arequipa duringdrought conditions, then in The high degree of stigmaexsertion exhibited by most some years bats are the most importantpollinators, but flowerslikely decreased the possibilityof self-pollination in otheryears hummingbirdsand diurnalinsects may be duringvisits by bats or hummingbirdsin 1991. Motten more important. and Antonovics(1992) examinedoutcrossing rates in Da- Dramatic shiftsin rainfallavailability at the studysite tura stramoniumand found thatthe most importantde- associated withEl Nifnoevents (Fig. 1) have implications terminantof outcrossingrate was the degree of stigma not only for the pollinationof columnarcacti, but likely exsertionexhibited by flowers.Flowers with stigmaspo- have a large influenceon variationin larval infestation sitioned above the anthershad higher outcrossingrates frequencyas well. Larval infestationand fruitmortality than did those withoverlapping stigmas and anthers.Re- varied between years in this study,probably as a result sults obtained for the bat-pollinatedMexican columnar of differencesin lepidopteranabundance duringand after cactus P. pringlei show thatopen-pollinated hermaphro- the drought.After rains resumed in 1993 insects, es- dite flowerswere found to have a low outcrossingrate pecially moths and butterflies,were observed more fre- (tm= 0.301) even thoughhigh flowervisitation rates were quentlythan theyhad been in late 1991 and 1992 (C. T observed (Murawski et al., 1993; Fleming et al., 1994). Sahley, personal observation).Thus, El Niiio events,by Murawski et al. (1993) hypothesizedthat the high degree influencingrainfall, plant phenology, and pollinatorabun- of selfing in the presence of flower visits was due to dance, may play an importantrole in thispollination mu- absence of stigma exsertionin flowersof P. pringlei. tualism.

Variationin pollinator effectivenessand larval infes- Maintenance of variationin W. weberbaueri-An im- tation among years: the role of El Niuo-As in the rest portantresult of this study was that although bat and of westernPeru, the arid westernslopes of the Peruvian hummingbird/diurnalinsect pollinationtreatments result- Andes are subjectto dramaticclimatic changes associated ed in significantlyhigher fruit initiation frequencies than with the El Ninio southernoscillation (Rasmusson and the otherfour treatments,differences in maturefruit set Wallace, 1983). Changes in sea level and temperature among treatmentswithin a year were not significant.In duringthis time cause considerablereduction in primary additionto the small differencesin maturefruit set among productivityof upwelling areas offthe coast of Peru that treatments,it is likely thatautogamy or apomixis limited result in the elevation of mortalityrates and disruption differencesamong treatments.Also, as fruitsmatured, of breeding schedules in seabirds, and marinemammals many were subject to larval infestationand subsequent (Barber and Chavez, 1983; Schreiber and Schreiber, fruitdeath. This furtherreduced differencesamong treat- 1984; Castro, 1986), while having a beneficialeffect on ments. These resultssuggest thateven if bats and hum- Andean condor populations(Wallace and Temple, 1988). mingbirdswere to preferdifferent flower types and col- However,the effectsthat such interyearvariability in cli- ors, in any given year selectionfor a bat vs. hummingbird mate have on terrestrialecological interactionsin Peru flowermorph would be weak. have previouslyreceived littleattention. I propose that interactionamong several factors,in- A major findingof this study was that mature fruit cluding variationin pollinatorimportance among years, productionattributable to bat pollination decreased sig- low within-yeardifferences in pollinatorimportance, and nificantlyin 1993 relativeto 1991 because of a decrease high levels of genetic variationin part due to autotetra- in bat populations near the study area. The 1991-1992 ploidy, may have led to weak and/orshifting selection El Niinoevent led to 3 yr of low rainfallat the studysite pressurefor any one flowermorph and have allowed the and a rainlessperiod thatspanned 17 mo. Phenologydata persistenceof morphologicalvariation in the population obtained over the course of this studyindicate thatfruit of W. weberbaueri that I studied. El Nifio events may and flowerproduction of W. weberbaueri dropped con- play an importantrole in influencingthe pollinationbi- siderably during this time, while census data obtained ology of this cactus by causing droughtconditions and from 1990 to 1993 for Platalina genovensiumdemon- reducingthe abundance of importantpollinators such as strateda substantialdecrease in bat abundance in 1992 nectar-feedingbats. Longer termstudies thatinclude ob- and 1993 (Sahley, 1995). Because data on the diet of P. servational data as well as experimentsspecifically de-

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