International Association for Ecology

Oviposition Choices by a Pre-Dispersal Seed Predator (Hylemya sp.). I. Correspondence with Hummingbird Pollinators, and the Role of Plant Size, Density and Floral Morphology Author(s): Alison K. Brody Source: Oecologia, Vol. 91, No. 1 (1992), pp. 56-62 Published by: Springer in cooperation with International Association for Ecology Stable URL: http://www.jstor.org/stable/4220031 . Accessed: 29/09/2011 14:38

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http://www.jstor.org Oecologia ( 1992) 91:56-62 ~ZZ-Z-?- Oecologia ? Springer-Verlag 1992

Oviposition choices by a pre-dispersal seed predator {Hylemya sp.)

I. Correspondence with hummingbird pollinators, and the role of plant size, density and floral morphology

Alison K. Brody

Department of Entomology University of California Davis, CA 95616, USA, and the Rocky Mountain Biological Laboratory, Crested Butte, CO 81224, USA

Received July 15, 1991 / Accepted in revised form February 21, 1992

Summary. Although the importance of pollinators has that may use floral traits in locating hosts and subse- most often been examined in the evolution of floral quently affect floral evolution. Pollinators and florivores characters, seed predators may also play a role in shaping are likely to interact in affecting floral evolution. In floral evolution. In this study, I examined the role of particular, the effects of seed predators that use floral interplant distance, plant size, and flower morphology on cues and ultimately consume potential offspring (i.e., Ipomopsis aggregata'^ (Polemoniaceae) attractiveness to seeds) and pollinators may interact in affecting floral a pre-dispersal seed predator, Hylemya sp. (Anthomyii- traits. To date this interaction has been little studied. In dae) and to hummingbird pollinators. The attractiveness comparison to hundreds, if not thousands, of references of /. aggregata individuals to Hylemya was nonlinearly on the interactions between pollinators and host plants related to interplant distance in experimental arrays. (for reviews see Faegri and van der Pijl 1978; Real 1983; Clumped and highly dispersed plants were preyed upon Jones and Little 1983), the interaction between seed more frequently than those at intermediate distances. I predators and pollinators in affecting floral evolution has found no relationship between interplant distance and received relatively little attention (Beattie et al. 1973; visitation rates by hummingbird pollinators in these ex- Zimmerman 1980a; Augsburger 1981 ; Hainsworth et al. perimental arrays. However, in natural populations stud- 1984; Campbell 1991). Pollination ecologists have ad- ied, clumped plants were more frequently approached by dressed the question of how plants attract pollinators, hummingbirds than those growing more widely disper- and have studied the variety and sequences of behaviors sed. Display size was unrelated to visitation by Hylemya that pollinators exhibit in searching for floral rewards on inflorescences I clipped and maintained as "large", (see Jones and Little 1983; Waser 1983 for reviews). We "small" and "control". Display size was also unrelated know much less about how seed predators locate hosts. to the total number of visits by hummingbird pollinators Host finding is certainly a multi-level process occur- to each of these experimental plants, however "large" ring at several spatial scales. The cues that govern host display plants were more likely to be visited first in any finding and utilization by both pollinators and seed given visitation sequence. Of various morphological predators can conveniently be broken down into those measurements, corolla length showed the strongest pos- that attract animals to a given patch, to an individual itive correlation with Hylemya egg presence. To the ex- plant, and to flowers on that individual. tent that plant spacing and morphology is correlated Host density, or interplant distances, may affect with pollinator visits and ultimate seed set, Hylemya movement rates to and within a local population (Evans could be choosing flowers optimally, and playing a role 1983; Karieva 1982, 1983, 1985; Bergelson and Karieva in the evolution of floral traits. 1987). The presence of neighboring conspecifics can af- fect arrival and tenure times within a patch of hosts - - Key words: Pre-dispersal seed pr?dation Pollination (Evans 1983; Bach 1980). One would predict that a - - Floral display Plant spacing Hylemya sp. denser host stand would attract more visitors (Moore 1978; Evans 1983) although this is not always the case (Moore 1978). Insects may respond primarily to within- plant (e.g., pod or flower production) characteristics, The evolution of floral traits conventionally has been and/or to local densities (Evans 1983). viewed as a function of plant attractiveness to pollina- Once in a patch, an animal must choose an individual tors. However, pollinators are not the only organisms plant. Large individuals may be most apparent, and thus Current address and address for offprint requests: The Rocky Moun- most attractive. The role of floral display size has been tain Biological Laboratory Crested Butte, CO 81224, USA addressed primarily in relation to pollinator attraction 57

(Willson et al. 1979; Pyke 1981; Zimmerman 1980b; color (Elam and Linhart 1988), flare of the corolla, and level of Thomson 1988; Schemske 1980). Hummingbirds stigma exsertion; the latter may determine a flower's relative invest- ment in male and female function 1989b; and preferentially visit many-flowered inflorescences of Ipo- (Campbell Campbell Waser 1989). The primary pollinators of /. aggregata are broad- mopsis aggregata (Pyke 1981) and birds may skip over tailed hummingbirds {Selasphorus platycercus Swainson) and ru- small in favor of to the next plants flying large plant fous hummingbirds {Selasphorous rufus Gmelin) (Waser 1978) al- (Campbell and Waser 1989). Inflorescence size may also though small insects play some role in pollinating this species as well affect movements between and within individuals. Al- (Waser 1978; Brody unpub. data). though more flowers may be visited on a many- versus In the vicinity of the Rocky Mountain Biological Laboratory, where this was /. is at few-flowered inflorescence, per-flower visitation rates study undertaken, aggregata pollen-limited, least in some parts of the flowering season and/or in some years may be similar (Schmid-Hempel and Speiser 1988). (Hainsworth et al. 1985; Campbell 1991). Pollen limitation is im- inflorescences be favored an increase Large may through portant in assessing the effects of choices made by seed predators in male reproductive effort through pollen export (e.g., for the following reason. If plants are not pollen limited, and all are Queller 1985), but may show little or no relationship to likely to attract sufficient numbers of pollinators to ensure a full pollen donation (Geber 1985; Schmid-Hempel and complement of seeds, then selection will not act through female function on the characters most attractive to Speiser 1988; Campbell 1989a). With notable exceptions pollinators. Thus, there would be no reason for seed predators to be "choosy" if all (Willson and Rathcke 1974; Queller 1985; Schmid- flowers have an equal probability of producing seeds. Hempel and Speiser 1988; Thomson 1988), the conse- Ipomopsis aggregata is preyed upon by an anthomyiid fly of size for and seed quences display pollination pr?dation {Hylemya sp.) which lays its eggs under the sepals and whose larvae have only rarely been experimentally tested. burrow into the ovary and eat the developing ovules. Normally, a Flower morphology may affect movement of animals single egg is laid on each flower, however clutches of two eggs are foraging among individuals; pollinators preferred large sometimes laid under the same sepal. A single larva normally con- sumes all of the seeds in a given fruit, a larva flowers of Raphanus sativus (Stanton and Preston 1988) although occasionally will emerge from a fruit before consuming all seeds. The larvae exit and Polemonium viscosum (Galen and Stanton, 1989), through the ovary wall and drop to the ground, where they pupate. and with flowers were over-visited in com- plants large Adult females do not pollinate the flowers. parison to those with smaller flowers (Galen and Stanton 1989). After arrival on a host, the role of variation in flower morphology within a plant on pollinator or preda- Interplant distance (density) and display size tor behavior has received much less attention. Using an artificial array of plants, I manipulated interplant distance The of this was to examine cues used purpose study to simulate clumps of different densities. In addition, I manipulated by a predispersal seed predator (Hylemya sp. Antho- flower number on plants within the density (distance) treatments. myiidae) in its selection of oviposition sites on Ipomopsis Plants were potted after bolting but before initiation of flowering in mid-June. were into the and held there aggregata, and to determine if there is concordance bet- They brought greenhouse until being placed in the field in 10 cm Prior to ween visitation patterns of predators and pollinators. I pots. placing plants in the field, I cleared a 28 m ? 12 m area of all naturally growing that the same cues may be used by both hypothesized /. aggregata. I grouped plants into triplets and randomly assigned of in and hosts. I ex- groups organisms finding visiting each triplet to one of three densities - 0.25 meters between plants, perimentally tested the effects of plant distance and flow- 0.75 meters, or 1.5 meters. I chose these distances because they er number on visitation patterns by a pre-dispersal seed represent the range of normal interplant distances observed in /. while each was to predator {Hylemya sp., Anthomyiidae) and by hum- aggregata (AKB, unpub. data), distinct enough find a treatment effect if one existed. Each distance treatment was mingbird pollinators (Selasphorus platycercus Swainson replicated 6 times in a latin square design, for a total of 18 triplets, and S. rufus) of Ipomopsis aggregata. In addition, I ex- and separated from all adjacent triplicates by 4 meters. I rotated the amined the role of flower in morphology egg deposition rows of the array every six days to control for any possible position patterns of Hylemya sp. Specifically, I asked the follow- bias. ing questions: 1) What effect does host plant density Within each triplet of plants, individuals were originally match- ed overall size and In (nearest-neighbor distances) have on the location of by flowering phenology. addition to assigning the triplet to a distance treatment, I randomly each mem- hosts by Hylemya sp.? 2) How does display size (mea- assigned ber of the triplet to one of three display size treatments - "large", sured by the number of flowers open at a given time) affect "small" and "control". I removed flowers of "small" plants every rates of if oviposition by Hylemya sp.? 3) What, any, third day by clipping them at the base of the pedicel to maintain morphological flower traits correlate with Hylemya their flower number at a level half that of the "large" member of choice? 4) How does natural plant density, measured by the triplet. Some flowers and elongated buds of the "large" plants nearest-neighbor distances, affect rates of visitation by were removed as well to avoid introducing a bias due to damaging the The "control" were left to assess wheth- pollinators and seed predators? plants. plants undipped er Hylemya avoided ovipositing on damaged plants. Because con- trol plants were randomly chosen at onset of experiment, they varied in flower number and some had as few flowers as experimen- Materials and methods tally small plants while others had as many as the large treatment plants. Ipomopsis aggregata (Pursh) V. Grant (Polemoniaceae) is a long- I censused each plant every 2-3 days, at which time I recorded lived monocarpic perennial that occurs commonly along roadsides the total number of flowers and elongated buds and the number of and on dry, often disturbed hillsides. It produces many red, tubular flowers and buds with Hylemya eggs. I marked the sepals of flowers flowers on a determinate inflorescence (Waser 1978). The flowers on which I found Hylemya eggs using a small dot of indelible ink. are protandrous ; each flower is open for a 3-5 day interval about I also recorded the number of flowers marked on the previous half of which is spent as a male (Campbell 1989b). Individuals show census date as having eggs. Hylemya usually lays eggs singly (pers. a good deal of morphological variation in such characters as flower observ.). An oviposition-deterring pheromone is deposited on Pole- 58 moniumfoliosissimum, the only other known host of Hylemya (Zim- presence was directly related to the depauperacy of visits to these merman 1982). Although Zimmerman concluded that Hylemya plants. However, I normally censused these plants between 0900 does not deposit an oviposition deterrent on /. aggregata, in the and 1400 - times which do not correspond to the peak time of populations I've studied eggs are more highly dispersed than in hummingbird feeding activity. This could account for, or contribute those of Zimmerman's (1982) work. Therefore, I believe that to, the relative scarcity of visits observed to the artificial arrays. Hylemya may avoid flowers on which eggs were previously laid. Because the area in which the arrays were placed is a site where Thus flowers with eggs cannot be considered potential oviposition /. aggregata typically grows and, in fact, was surrounded by natu- sites, but could function in attracting the fly to the plant. rally occurring /. aggregata, I am confident that hummingbirds The arrays were maintained in the field from 29 June through visit this site regularly. 5 August, 1990. Plants were replaced if they died or ceased flowering For each of the seven bird-visits I observed, I recorded the using others that I had potted in mid-June and kept in the green- sequence of visitation from the time the bird arrived until it left the house. The experiment was terminated on 6 August, by which time experimental array. I recorded, in order, each triplet the bird visited, most plants had stopped producing new flowers. each plant within the triplet and the number of flowers probed I analyzed the results of this experiment with a two-way, re- within each plant. On three occasions I observed a bird visit a triplet peated measures ANOVA. Density and display size were fixed but could not determine which plant the bird visited; for these effects, and census date the repeated measure. I included only every I recorded the triplet's distance treatment but could not include third census to avoid counting flowers that could have been present these visits in assessing the relative attractiveness to plants of the on consecutive dates (/. aggregata flowers rarely last more than 3-5 three display size treatments. days). The percentage of flowers and elongated buds with eggs, and the percentage of available flowers (i.e., those not previously mark- ed as having eggs) were analyzed separately as response variables. Results All percentage data were arcsin (square-root) transformed prior to analysis. The design became unbalanced because not all triplets Hylemya visitation, plant density and display size flowered for the same length of time, nor were all represented on each census date because plants died or quit flowering during the There was an effect of interplant distance in the artificial experiment and had to be replaced. patches on the percentage of flowers attacked by Hylem- = = ya (F 5.42, df=2,45, P 0.008; Table 1). The percent- Morphological flower traits age of flowers that Hylemya laid eggs on was not dif- ferent for plants at distances of 0.25 m and 1.5 m, how- To study the relationship between flower morphology and egg ever these plants received more Hylemya eggs than those deposition by Hylemya, I used three populations north of the at the intermediate distance of 0.75 meter. I found no RMBL located ca. 1/8 mile from Avery Campground, Gunnison significant relationship between display size (number of National Forest. Eighty-nine plants in these populations had been marked a with the number on flowers open at any given time) and the percentage of by placing yellow flag nearby plant's = it, and were currently under investigation by R. Mitchell. I haphaz- flowers with eggs (F 0.093, df= 2,45, ?=0.912), nor did ardly chose two flowers on each plant with eggs and two flowers on I find a significant interaction between interplant dis- each plant without eggs and measured corolla length, corolla width, tance and display size (F= 1.652, df=4,45, ?>=0.178; width and If two flowers were not sepal length, sepal carpel length. Table 1). There was a significant effect of time (census available in each category (with and without eggs) I measured only date) within a plant, but no significant interactions be- two flowers on that plant, one of each category. I then asked tween time and either distance or size treatments whether the group of flowers with eggs was statistically different display from the group without eggs using discriminant function analysis (Table 1). (SPSS/PC+ , procedure DSCRIMINANT). All data were nor- malized each observation from the mean for by subtracting plant Table 1. A repeated-measures ANOVA of the effect of plant density that trait. of the marked 89 had Seventy-five originally plants and flower number on the proportion of /. aggregata flowers par- flowers both with and without eggs and were thus used in the asitized by Hylemya. The proportion of flowers with eggs was arcsin analysis. root) transformed. Census date was used as the In I (square repeated addition, measured the distance to the nearest three neigh- measure bors of each of the 89 plants used for morphological measurements. Each population was observed for over 7 hours during peak feeding ANOVA activity of hummingbirds (ca. 1830-2000) over a period of one week. The mean number of hummingbird approaches to each plant SOURCE SS DF MS F ? and average number of flowers probed on each plant were recorded and then correlated with the mean distance to the three nearest Between subjects neighbors. On 21 and 24 July, all flowers of all 89 plants were Density 3888.228 2 1944.114 5.420 0.008 censused for Hylemya eggs. I used the percentage of flowers with size 66.479 2 33.240 0.093 0.912 as an of visitation to individual eggs index rates by Hylemya plants. Density I then correlated the percent of flowers with eggs and the average ?size 2369.921 4 592.480 1.652 0.178 number of approaches and flowers probed to examine whether there Error 16142.163 45 358.715 was concordance between hummingbird and Hylemya visitation individual rates to plants. Within subjects Trial 5969.051 4 1492.263 5.632 0.000 (Census date) Effects of plant density on pollinators Trial * density 1412.338 8 176.542 0.666 0.721 In 60 hours of observation of artificial arrays while censusing plants Trial ?size 1858.619 8 232.327 0.877 0.537 for eggs, I observed only 7 hummingbirds visits to the arrays. I have Trial ?size 1437.512 16 89.845 0.339 0.992 * frequently had birds visit plants very close to where I was working density in the field, often approaching me directly to investigate a bit of Error 47690.079 180 264.945 bright clothing I was wearing. Therefore, I do not believe that my 59

Table 2. of visits Frequency hummingbird Density Floral display size to experimental arrays at 0.25 m, 0.75 m and 1.5 m, and to large', 'small' and 0.25 m 0.75 m .5 m 'control' plants. Mean numbers of flowers open ( 4- one standard deviation) for each treatment are given at the bottom of the All visits 6 6 5 2 0 1 5 1 1 table 1st in sequence 3 1 1 2 0 0 5 0 0 Ave. display 20.6 11.2 11.6 14.2 9.7 15.3 16.3 9.5 11.4 Std. dev. 8.8 6.5 6.9 7.5 6.4 7.9 9.4 5.8 7.0

Given that females do not usually oviposit on flowers erage number of approaches to each plant and the num- that already have eggs, one might expect the percentage ber of flowers probed by hummingbirds (Fig. 1, Table 3). of available flowers (total number of flowers minus those I did not find a significant correlation between the per- that already had eggs) on a plant to be a more important centage of flowers with Hylemya eggs and the number of predictor of subsequent oviposition than the total num- approaches or flowers probed by hummingbirds (Table 4). ber of flowers. I did not find this to be the case. Using Nor did I find the percentage of flowers with eggs to be the percentage flowers available to a newly arrived correlated with nearest-neighbor distances. female as the dependent variable yielded results similar to those obtained using the total number of flowers. Table 3. Correlation analysis of nearest-neighbor distances and the visitation rates by hummingbirds to /. aggregata in 1990. Bonfer- roni are in parentheses. TV= 89. Hummingbird visita- Pollinator and size probabilities visitation, plant density display tion data from R. Mitchell

For the seven bird-visits I observed to the experimental Pearson correlation matrix I found no differences in the to visit array, propensity Approach Ave. distance Probes triplets with different interplant distances. Numbers of to nearest visits summed across all birds were, respectively, 8,4 and neighbor 5 to triplets with spacings of 0.25, 0.75 and 1.5 meters. Approach 1.000 I also found no significant pattern in bird visits based on (0.000) plant display size. "Large display" plants were visited Ave. distance to -0.250 1.000 13 times, while "small display" and "control display" nearest neighbor (0.055) (0.000) plants were visited 7 and 6 times respectively. However, Probes 0.832 -0.274 1.000 if I examine visitation sequence, "large" plants were (0.000) (0.028) (0.000) visited first in a sequence on 10 occasions, while "small" and "control" plants were visited first only once each (Table 2). Table 4. Correlation analysis between visitation rates by humming- For the 89 plants measured and observed in natural birds and oviposition by Hylemya on /. aggregata in 1990. N~ 54 I found significant negative correlations populations, Bonferroni probabilities are in parentheses between average nearest-neighbor distance and the av- Pearson correlation matrix Approach Percent of Probes 1.00 flowers with Hylemya eggs 0.60 + + Approach 1.000 + + + Percent of flowers 0.154 1.000 0.60 with Hylemya eggs (0.266) Probes 0.817 0.171 1.000 ? 0.40 (0.000) (0.217) ++ ++ + + + + +

0.20 Table 5. Pooled-within-groups correlations between discriminating variables and canonical discriminant functions. Variables are ' 0.00 ordered by strength of correlation within the function 32 64 96 128 160 0.83156 Ave. Nearest-neighbordistance (cm) Corolla Length Carpel Length 0.36164 to Fig. 1. The average number of approaches by hummingbirds Sepal Length 0.34250 the distance of Ipompsis aggregata plants as a function of average Sepal Width 0.29848 plants to their three nearest neighbors. Hummingbird visitation Corolla Width -0.08974 data from R. Mitchell 60

Table 6. Results of discriminant function analysis of morphological each group were excluded from analysis. Data were normalized by traits of flowers grouped by presence/absence of Hylemya eggs. subtracting each observation from the plant mean. (L = length; Plants that did not have a balanced number of observations for in W-width) Within Group Means (std deviations)

Egg TRT Sepal L Sepal W Corolla L Corolla W Carpel L

No egg -0.062 (0.63) -0.017 (0.20) 0.249 (1.21) 0.007 (0.27) -0.044 (0.45) egg 0.062 (0.62) 0.017 (0.19) 0.249 (0.84) 0.007 (0.24) 0.044 (0.38)

Function Eigenvalue Canonical Wilks' Chi-square DF Correlation Lambda

0.0845 0.2791 0.9221 11.801 0.038

Table 7. Classification results of discriminant function analysis ing these ecological consequences can still be of heuristic based on morphological measurements of flowers with and without value in determining means by which seed predators eggs locate hosts, and important for studies in plant popula- tion dynamics. Actual No. of Predicted group membership The Group cases non-linear relationship between interplant dis- 1 2 tance and seed pr?dation I found in this study is intrigu- ing. One explanation for such a finding might be that 1 75 45 30 Group plants that are either clumped, or widely dispersed from 60.0% 40.0% other individuals, may be more apparent to visually- Group 2 75 29 46 38.7% 61.3% oriented insects. The resource concentration hypothesis championed by Root (1973) predicts that herbivores are Percent of "grouped" cases correctly classified: 60.67% more likely to find hosts occurring in dense stands. Con- trary to this hypothesis, Euphydryas editha butterflies alight more often on large, isolated plants than would be traits Morphological expected (Rausher et al. 1981). A second explanation for my finding that isolated and clumped plants had higher Flowers with eggs tended to be larger than flowers with- rates of oviposition than intermediately dispersed in- out eggs. The most important characters in discriminat- dividuals could be as follows: If one views finding host- ing these two groups were corolla length, carpel length, plants as a two-step process, the first step being that of sepal length and sepal width, respectively (Table 5). encountering an initial host, the second that of encoun- I found significant correlations between characters only tering a subsequent host, then one might predict plants for sepal length and corolla width, and sepal width and at low and high densities to be encountered more fre- sepal length. Both correlations were positive. Wi thin- quently than those at intermediate densities. Imagine an group (where groups distinguish flowers with and with- insect flying into a patch. If plants are widely spaced, the out eggs) means, expressed as the difference from the probability of encounter with one of those plants is grand mean, were positive for corolla length, carpel greater than if plants are clumped. Having left a plant, length, sepal length and sepal width, while that for the probability of encounter with an adjacent host will corolla width was Discri- very weakly negative (Table 6). be a function its distance from the first. As a result of minant function analysis classified sixty-percent of the these two separate mechanisms (initial and subsequent flowers without eggs correctly, and sixtyone percent = host encounters), plants that are widely spaced and those of those with eggs correctly (Chi-square 6.83, 1 df, that are clumped might be found more often than those P<0.01;Table7). at intermediate densities. Further work is needed to as- sess which of these (or other) mechanisms is responsible Discussion for the pattern I obtained. The effects on the fitness of seed predators choosing Seeds of /. aggregata have no known dispersal agents large plants, or plants in dense stands, may be mediated (Waser and Price 1983). Given the preponderance of by pollinators' response to plant display size and/or stochastic events leading to seeds' initial dispersal from density. If pollinators preferentially visit clumped plants, a parental plant, location in an adequate microhabitat, plants living in aggregations may have higher relative germination and ultimate reproductive success, the fruit set and thus provide greater resources for larvae heritabilities of traits important to seed dispersal and feeding on seeds. In the natural populations of /. ag- seedling establishment are probably quite low for /. ag- gregata, I found a significant negative correlation be- gregata. Therefore, local plant density may have ecolog- tween nearest-neighbor distances and hummingbird vis- ically interesting consequences but not respond to selec- itation rates, indicating again that clumped plants receive tion by either pollinators or seed predators. Understand- more visits by these pollinators. 61

To the extent that they are genetically based, alloca- apparently chooses /. aggregata flowers in a similar tion patterns to reproduction may respond directly to fashion. selection from herbivores, seed predators, and pollina- Emerging from these studies is an unequivocal need tors (Augsburger 1980, 1981; Beattie et al. 1973; De to further test experimentally the hypotheses erected to Steven 1983; Janzen 1971a, b; Taylor and Inouye 1985). explain patterns of floral display based on attractiveness However, I found no evidence that seed predators re- to pollinators and avoidance of pr?dation. To fully un- sponded to floral display size in my artificially manipu- derstand the evolution of floral traits, one must examine lated plants. The response of seed predators to in- the effects of all organisms affecting plant fitness. florescence size in other studies is equivocal. For exam- Acknowledgements. Randy Mitchell generously provided humming- ple, predispersal seed pr?dation in Bartsia alpina was bird visitation data. Rick Karban, Maureen Stanton and Nick significantly higher for large than for small inflorescences Waser offered many helpful comments and suggestions on both (Molau et al. 1989). However, infructescence size had no experimental design and earlier versions of this manuscript. Mary Price statistical advice. lent apparent effect on the percentage of Crotalaria seed pods provided Gary Entsminger support wherever and whenever needed. To all of these people I offer thanks attacked by chewing insects (Moore 1978), or flowers and gratitude. This research was supported in part Snyder in this Results of by preyed upon by Hylemya study. my Foundation grants from the RMBL, and Jastro-Shields Research - /. other studies corroborate this finding aggregata Scholarship awards from the University of California, Davis. plants with larger inflorescences received more eggs but not proportionally more (Brody 1991). References In my study, display size also did not have a signifi- cant effect on the total number of visits by pollinators, Augsburger CK (1980) Mass-flowering of a tropical shrub : influence on attraction and but large display plants were the first to be visited. (Hybanthus prunifolius) pollinator movement. Evolution 34:475-488 Honeybees appear to exhibit the same pattern while Augsburger CK (1981) Reproductive synchrony of a tropical shrub: foraging on sativa ; individuals Raphanus large-flowered experimental studies on effects of pollinators and seed predators are the first to be visited and are in often over-visited on Hybanthus prunifolius (Violaceae). Ecology 62:775-788 comparison to small-flowered plants (Young and Stan- Bach CE (1980) Effect of plant diversity and time of colonization ton 1990). Since hummingbirds (and other foragers) must on an herbivore-plant interaction. Oecologia 44:319-326 Beattie Breedlove Ehrlich PR The of the leave patches, and do so after varying numbers of visits, AJ, DE, (1973) ecology pollinators and predators of Frasera speciosa. Ecology 54:81-91 if large plants are consistently visited first then they will Bergelson J, Karieva ? (1987) Barriers to movement and the re- receive more visits than smaller In ultimately plants. sponse of herbivores to alternative cropping patterns. Oecologia addition, first-visited individuals will be more likely to 71:457^160 receive pollen from greater distances than those visited Brody AK (1991) Pre-dispersal seed pr?dation by Hylemya (Delia) sequentially later. sp. (Diptera: Anthomyiidae): Mechanisms and consequences of choice. PhD dissertation Univ of Davis Since nearest-neighbors tend to be more closely re- oviposition California, Campbell DR (1989a) Inflorescence size: test of the male function lated than distant individuals, and there is evidence for hypothesis. Am J Bot 76:730-738 in /. and Price inbreeding depression aggregata (Waser Campbell DR (1989b) Measurements of selection in a herma- I 1989), the positive correlation found between nearest- phroditic plant: variation in male and female pollination suc- neighbor distances in natural populations and pollinator cess. Evolution 43:318-334 visits may translate into a less-than optimal donation and Campbell DR (1991) Effects of floral traits on sequential com- of fitness in Am Nat 137:713-737 receipt of pollen. However, this must be superimposed ponents Ipomopsis aggregata. Campbell DR, Waser ? M (1989) Variation in pollen flow within upon visitation sequences; as mentioned above, first- and among populations of Ipomopsis aggregata. Evolution visited individuals have a higher probability of receiving 43:1444-1455 pollen from longer distances. De Steven D (1983) Reproductive consequences of insect seed The effects of flower morphology on pollinator or seed pr?dation in Hamamelis virginiana. Ecology 64:89-98 predator foraging have been less studied and are more Elam DR, Linhart ? ? (1988) Pollination and seed production in differences and within flower color difficult to measure. Here, I found a positive relationship Ipomopsis aggregata: among morphs. 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