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Outcrossing and Pollinator Limitation of Fruit Set: Breeding Systems of Neotropical Inga Trees (Fabaceae: Mimosoideae)

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Outcrossing and Pollinator Limitation of Fruit Set: Breeding Systems of Neotropical Inga Trees (Fabaceae: Mimosoideae) Evolution, 38(5), 1984, pp. 1130-1143 OUTCROSSING AND POLLINATOR LIMITATION OF FRUIT SET: BREEDING SYSTEMS OF NEOTROPICAL INGA TREES (FABACEAE: MIMOSOIDEAE) SUZANNE KOPTURI Department ofBotany, University ofCalifornia, Berkeley, California 94720 Received October 17, 1983. Revised January 25, 1984 Many hermaphroditic flowering plants flowers on a plant are visited, and pol­ produce many more flowers than fruit. linated with pollen appropriate for fer­ Low fruit set from a large number ofpo­ tilization, the plant may be unable to ma­ tential fruit may result from a variety of ture every fruit because of resource, factors. In animal-pollinated species, a spatial, or physical restrictions. Resource large floral display may be advantageous limitation may cause abortion of some in attracting pollinators (Gentry, 1974; developing ovules or ovaries (Stephen­ Willson and Rathcke, 1974; Schaffer and son, 1981), and can provide a logistical Schaffer, 1979; Stephenson, 1979; Aug­ basis for mate choice in plants (Janzen, spurger, 1980; Udovic, 1981), especially 1977; Willson, 1979) and sibling com­ if the density of plants is low, the dura­ petition between developing embryos tion ofbloom ofthe species is short, and/ (Kress, 1981). or there are many other species blooming Inga is a large genus ofneotropicalle­ simultaneously. If pollinators visit only gume trees that have alternate, parapin­ some of the flowers, not all flowers will nately compound leaves (often with fo­ receive pollen, and fruit set without fer­ liar nectaries: Leon, 1966; Bentley, 1977; tilization will not take place in plants that Koptur, 1984) and large floral displays are non-agamospermous and without au­ (Croat, 1978; Koptur, 1983). The showy tomatic selfing; in this way the plants can white inflorescences are composed of be pollinator-limited, by virtue of low many flowers that have reduced perianth visitation (Bierzychudek, 1981). Incom­ parts and many white stamens; the sta­ patibility systems can cause pollinator­ mens are basally connate, forming a tube limitation ofa more complex nature: the within which nectar accumulates. The fruit set ofa self-incompatible species will open flowers are visited by a wide array be limited by the kinds of visitors, and ofvisitors ofwhich bats, hummingbirds, the kinds ofvisits (intraplant movements hawkmoths, butterflies, and settling resulting in intrafloral selfing or geito­ moths are pollinators (Snow and Snow, nogamy versus interplant movements 1972; Salas, 1974; Toledo, 1975; Fein­ resulting in xenogamy) (Arroyo, 1976). singer, 1976, 1978; Koptur, 1983). Inga Interspecific pollinator movements can pollen grains are clustered into globular result in stigma-clogging, with foreign polyads of 16 to 32 grains; the po1yad is pollen impairing the adherence and ger­ dispersed as a unit. Most Inga produce mination ofpollen ofthe correct species few fruit in relation to the number of (Levin and Anderson, 1970; Wissel, 1977; flowers they bear (Leon, 1966; pers. ob­ Waser, 1978). Allelopathic effects offor­ serv.). The focus of this study is the fac­ eign pollen may also depress fecundity of tors influencing fruit set in some Costa some species (Sukada and Jayachandra, Rican species ofInga. The floral biology, 1980; Thompson et al., 1981). Even ifall flowering and fruiting phenology ofthese Inga species is described by Koptur (1983). The breeding systems of these I Present address: Department of Biological Sci­ ences, Florida International University, Miami, trees are elucidated here as a basis for Florida 33199. understanding patterns offlowering, and 1130 BREEDING SYSTEMS OF NEOTROPICAL TREES 1131 interpreting pollinator movements in po1yads were mounted in polyvinyl lac­ terms of potential fertilization of Inga tophenol cotton blue, and the pollen flowers. The opposing evolutionary con­ grains were separated by applying pres­ straints of massive flowering to attract sure on the cover slip. The number of pollinators and the resulting excessive pollen grains per polyad was counted un­ self-pollination are conflicts common to der a compound microscope. Twenty many tropical trees (Bawa, 1983). In this five-30 polyads from 2-5 individuals per study I consider the importance of pol­ species were counted. Ovules were dis­ lination phenomena in limiting fruit set sected from ovaries and counted under a in Inga and possibly many other species. dissecting microscope. Twenty five-40 ovaries from 2-5 individuals per species MATERIALS AND METHODS were dissected. The pollen ovule ratio (P/ The study area is in Puntarenas Prov­ 0) for each species was calculated using ince, Costa Rica, situated between 1,320 the formula shown in Table 1. m and 1,600 m elevation, and includes Activity of visitors was observed at two forest types and the transition zone flowers of selected Inga brenesii and I. between. The lower areas consist largely punctata individuals for 10 min every 30 offorest remnants bordering cleared pas­ min over 8-h periods on several different tures in the communities of Santa Elena days. Visitor frequency and the number and Monteverde. The transition area is of flowers visited in each foraging bout included in a large tract of privately were noted where possible, and in some owned forest contiguous with the Mon­ cases it was possible to watch where the teverde Cloud Forest Biological Reserve, visitors went after they left the individual a large area of pristine forest, which in­ tree under observation. cludes the uppermost locations. The sites The amount ofpollination in the field have been described in detail (Buskirk was measured by looking for polyads on and Buskirk, 1976; Feinsinger, 1976; stigmas of randomly collected flowers Powell, 1979; Lawton and Dryer, 1980; (both fresh and recently wilted) from 3­ Hartshorn, 1983). 5 individuals ofall the species. The flow­ Seven species of Inga were studied: ers were preserved in ETOH or FAA and Inga brenesii StandI., I. densiflora Benth., not examined until later, so that some I. longispica StandI., I. mortoniana J. polyads may have fallen off if not ger­ Leon, I. oerstediana Benth. ex. Seem., 1. minated. The measure is therefore a con­ punctata Willd., and 1. quaternata Poep­ servative estimate on two counts: fresh pig. Voucher specimens are in the her­ flowers may have had additional polli­ baria of the University of California, nation opportunities prior to wilting, and Berkeley (UC), the Missouri Botanical ungerminated polyads may have been Garden (MO), and the Museo Nacional disturbed prior to counting. de Costa Rica (CR). All these species are Crossing experiments to investigate the canopy or subcanopy trees. Trees used in breeding systems ofsix species were per­ the study were growing at the forest's edge, formed on inflorescences bagged with along trails, or in open pastureland, as Pollen-Tector heavy paper bags (Carpen­ the flowers ofthese individuals were ac­ ter Paper Co., Des Moines, IA). Inflo­ cessible. Flowers were reached by climb­ rescences were bagged the day before the ing trees, using a ladder, or occasionally opening offlowers to be hand-pollinated. from the ground. There are biases that Flowers that were open previously were may have arisen by working on semi­ removed at the time ofbagging. Approx­ isolated trees (altered pollinator activity, imately equal numbers were used for each resource availability) resulting in false treatment on each tree. Flowers were first (perhaps) estimates of actual fruit num­ emasculated, andpolyads from eitherdif­ bers in nature. ferent flowers on the same tree (self-pol­ To determine pollen/ovule ratios, lination) or from flowers on two or three 1132 SUZANNE KOPTUR other trees (cross-pollination) were ap­ Interspecific cross-pollinations were plied to the receptive stigmas. All flowers performed between simultaneously pollinated on an inflorescence received blooming Inga species: I. brenesii x I. the same kind ofpollen; only 1-4 flowers oerstediana; I. brenesii x I. punctata; I. were pollinated per inflorescence, as it punctata x I. densiflora; I. brenesii x I. was found (see below, maximum fruit set mortoniana. 20-30 crosses were per­ capacity) that maximum fruit set did not formed on at least two individuals ofeach exceed 4-6 fruit per inflorescence. Pollen species in all cases. was collected from flowers that had In all experiments, inflorescences were opened inside bags; stamens were re­ re-bagged for 3-5 days after pollination, moved with clean forceps and put in glas­ until the non-fertilized flowers began fall­ sine envelopes. Polyads were visible on ing. Inflorescences with flowers remain­ the hairs of fine paint brushes that were ing (presumably fertilized) were tagged used to place polyads on stigmas. Care and labeled, and subsequent fruit devel­ was always taken to apply at least three opment was monitored on a monthly ba­ polyads to a stigma. On other bagged in­ sis. When fruits appeared fully mature, florescences on the same trees, newly­ they were removed and opened to see if opened flowers were left untouched to they had mature seeds; only then was a test for autogamy (automatic selfing). An flower counted as successful in producing additional group of unbagged inflores­ a fruit. All seeds germinated after sowing cences on the same trees were unobtru­ unless they had been damaged in the pod sively tagged and left untouched for mon­ by insect larvae. itoring fruit set on "open pollinated" In order to examine more closely the flowers, in order to estimate the actual nature ofthe incompatibility system, the amount ofsuccessful fertilization that oc­ styles of I. brenesii flowers pollinated ac­ curs under natural conditions. cording to the preceding regime (401 The fertilization effectiveness ofpollen treatment) were fixed in lactophenol at from different distances away from stig­ 2-h intervals from the time ofpollination matic parent was investigated for Inga (2 h, 4, 6, 8, 12, and 24 h). These styles brenesii and I. punctata. Pollen was col­ were cleared and stained with aniline blue lected from three sources (Self, Near­ using the method of C. Johnson and D. Cross, and Far-Cross-2 or 3 individuals Mulcahy (adapted from Ramming et aI., at each distance) from flowers newly 1973, Stain Tech.
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