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Effects of Floral Display Size and Plant Density on Pollinator Visitation Rate

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Effects of Floral Display Size and Plant Density on Pollinator Visitation Rate Functional Blackwell Publishing, Ltd. Ecology 2005 Effects of floral display size and plant density on pollinator 19, 383–390 visitation rate in a natural population of Digitalis purpurea J. M. GRINDELAND,* N. SLETVOLD†‡ and R. A. IMS§ Department of Biology, University of Oslo, PO Box 1066 Blindern, N-0316 Oslo, Norway Summary 1. Pollinator visitation patterns in relation to variation in floral display size may be modified both quantitatively and qualitatively by local plant density. In this study four measures of pollinator response by Bombus spp. (plant visitation rate, bout length, proportion of flowers visited, flower visitation rate) were investigated under two or three different plant densities in two consecutive years in a natural population of Digitalis purpurea L. 2. Plant visitation rate increased with floral display size in both years, and was higher in dense patches compared with sparse ones in 1999. Bout lengths increased with dis- play size in 1999, and bouts were longer in sparse patches. However, the actual rate of increase with display size was independent of plant density for both response measures. 3. The proportion of flowers visited decreased with floral display size in both years, and in 1999 the decline was faster in high-density patches. As a result, the proportion visited was higher in dense patches for the smallest display sizes, and higher in sparse patches for larger display sizes. 4. Flower visitation rate decreased with floral display size in both years. This is incon- sistent with the idea that bees achieve an ideal free distribution across flowers. There was no significant effect of plant density. 5. These results demonstrate that local plant density variation may modify the functional relationship between floral display size and pollinator visitation rate, and potentially influence plant mating patterns. Key-words: Bombus, flower visitation rate, plant density effects, plant–pollinator interactions, pollinator foraging behaviour Functional Ecology (2005) 19, 383–390 doi: 10.1111/j.1365-2435.2005.00988.x An increase in bout lengths on larger plants is pre- Introduction dicted in optimality models of insect foraging (Pyke Animal-pollinated plants are expected to evolve strat- 1979). From the plant’s point of view this may not be egies that maximize the efficiency of pollen transfer of any selective advantage, since it will result in geito- to and from the plant. One such strategy may be to nogamous pollination (de Jong, Waser & Klinkhamer develop large floral displays that attract more pollina- 1993) and possible inbreeding depression in self- tors. There is usually considerable within-population compatible species (Darwin 1876; Charlesworth & variation in the number of open flowers presented on Charlesworth 1987), or pollen discounting (Ritland a plant, and several studies have reported a positive 1991) and stigma clogging in self-incompatible ones relationship between floral display size and the fre- (Robertson & Macnair 1995). Empirical evidence sup- quency of pollinator visits at the individual plant level port that bout lengths usually increase with plant size, (i.e. plant visitation rate) (e.g. 15 out of 17 studies but this is often accompanied by a decrease in the pro- reviewed by Ohashi & Yahara 1999). portion of open flowers probed (references in Mitchell et al. 2004). As a result, per flower visitation rate has †Author to whom correspondence should be addressed. been found to increase (Klinkhamer, de Jong & de Bruyn E-mail: [email protected] 1989; Andersson 1991), decrease (Andersson 1988; *Present address: Sør-Trøndelag University College, Rotvoll Klinkhamer & de Jong 1990) or show a constant relation Allé 1, N-7004 Trondheim, Norway. with floral display size (e.g. Robertson & Macnair 1995; ‡Present address: Natural History Museum, University of Oslo, PO Box 1172 Blindern, N-0318 Oslo, Norway. Vaughton & Ramsey 1998; Ohashi & Yahara 2002). © 2005 British §Present address: Department of Biology, University of How pollinators respond to differences in display Ecological Society Tromsø, N-9037 Tromsø, Norway. size may be modified by ecological factors, especially 383 384 plant density (Charnov 1976). Optimal foraging theory Materials and methods J. M. Grindeland predicts plant visitation rate to be higher in dense et al. patches, but more flowers to be probed per plant visit in isolated plants (Pyke 1979, 1982). Some studies have documented a positive relationship between plant Foxglove, Digitalis purpurea L., is a facultative biennial visitation rate and plant density (e.g. Klinkhamer & de herb that grows on naturally disturbed soil. The plant Jong 1990; Kunin 1997; Nielsen & Ims 2000), while produces one or a few inflorescences, usually 1–2 m in others have not (e.g. Aizen 1997; Bosch & Waser 2001), height, and normally with 20–100 flowers. The self- and there is at least one report of a decrease in visita- compatible flowers (Darwin 1876) produce nectar and tion rate with plant density (Stout, Allen & Goulson are mainly visited by bumble-bees (Best & Bierzychudek 1998). The longer visitation sequences predicted in 1982). The basal flowers mature first (acropetal flower- isolated plants have been confirmed by several workers ing). There is little spatial separation of the sexes within (Cibula & Zimmerman 1984; Klinkhamer & de Jong flowers, but temporal separation (protandry) is pro- 1990; Cresswell 1997; Bosch & Waser 1999). How these nounced. The combination of acropetal flowering and density effects combine into resulting visitation rates protandry results in inflorescences where the sexes are to individual flowers has received much less attention, spatially separated: the lowest flowers are female, usu- and no clear pattern has emerged from the results so ally followed by neuter flowers, male flowers and, at the far. Sih & Baltus (1987) found the relationship between top open, prefertile flowers. Nectar reward increases density (i.e. patch size) and average flower visitation during flower life (Percival & Morgan 1965) and rate in the perennial Nepeta cataria to depend on visitor consequently induces bumble-bees to visit the lowest type; for honey-bees and bumble-bees it was positive, flowers first. for solitary bees it was negative. No effect of density on flower visitation rate was found either in the facultative biennial Echium vulgare (Klinkhamer & de Jong 1990), or in the perennial Cirsium purpuratum (Ohashi & Field work was conducted during the summers of 1998 Yahara 2002), while Kunin (1997) found a positive and 1999 in a population on established pasture land effect in the annual Brassica kaber. in Ulvik (Hordaland County) in SW Norway (60°34′ N, In addition to the effects density may have on mean 6°54′ E). An area of approximately 200 m by 100 m on pollinator response to variation in floral display size, the south-facing slopes towards the Hardangerfjord it may also change the actual shape of the response was used (10–50 m above sea level). The population curve. Ohashi & Yahara (2002) compared pollinator consisted of a mosaic of areas with varying plant behaviour in two populations of differing density of density, and focal plants were chosen within patches of Cirsium purpuratum, and showed that plant visitation uniform local density. rate in relation to display size increased at a higher rate In 1998 patches of three plant density categories were in the high-density stand. As far as we are aware this is used: four dense patches with plants less than 0·5 m the only study to address whether density affects the apart, four intermediate patches with plants approxi- functional relationship between floral display size and mately 1 m apart, and four sparse patches with plants pollinator visitation patterns. If pollinators alter their approximately 2 m apart. Ten neighbouring plants behaviour according to density variation at a smaller were haphazardly selected in each patch, yielding a spatial scale (i.e. within populations), this may have large total of 120 focal individuals. Approximately 900 impact on size-dependent pollen flow and plant mating flowering plants were present in the population. Insect patterns in populations with varying local plant density. activity was monitored in each patch for 10 min on Studies that address the effects of combined varia- each of 3 days: 11, 12 and 14 July 1998 (i.e. each patch and tion in floral display size and plant density at the level plant was observed for 30 min in total). The sequence of the individual flower are still few, and very little is of patch observations were changed at random known about how local density-variation may affect between days to avoid observing the same patch at the the shape of pollinator response curves. In this paper same time each day. Total observation time was 6 h. we report the results of an observational study on pol- The relatively low visitation frequency observed in linator visitation patterns in patches of varying spatial 1998 made us increase total observation time in the density in a natural population of Digitalis purpurea L. 1999 season, and the fact that fewer flowering plants (Scrophulariaceae). Two main questions are presently were present (c. 450) made it necessary to reduce the addressed: number of patch density levels. Two density categories were used: seven dense patches with plants less than 1. Is there a positive relationship between four meas- 0·5 m apart, and seven sparse patches with plants more ures of pollinator response (plant visitation rate, than 1 m apart. Neighbouring focal plants were bout length, proportion of flowers visited, flower haphazardly selected in each patch according to the © 2005 British Ecological Society, visitation rate) and floral display size? number available. In dense patches plant number Functional Ecology, 2. How are these relationships affected by plant varied from 6 to 14 with a total of 65, and in sparse 19, 383–390 density? patches from 8 to 11 with a total of 68. Insect visitation 385 was monitored for 15 min on 5 days between 29 June tively small integer counts) were analysed by log-linear Floral display size and 8 July 1999 (i.e.
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