TAXON 56 (3) • August 2007: 729–736 Olesen & al. • Flower openness and number of visiting species

The openness of a flower and its number of flower-visitor species

Jens M. Olesen1, Yoko L. Dupont1, Bodil K. Ehlers1 & Dennis M. Hansen2

1 Department of Biological Sciences, University of Aarhus, Ny Munkegade B1540, 8000 Århus C, Denmark. [email protected] (author for correspondence) 2 Institute of Environmental Sciences, University of Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland

Using a sample of 1,403 flowering species, we tested the hypothesis that flower openness and flower-

visitor generalization level of a plant species correlate positively. The “flower-visitor generalization level” Ln of a species n, here defined as number of flower-visiting animal species attracted to the flowers of n in a given study site, varied enormously among plant species. Its frequency distribution was extremely skewed. Within a study site, L also increased with number of flower-visitor species A. In order to correct for this, we expressed L relatively, as the proportion of the total flower-visitor fauna in a study site that visited a given plant species (relative generalization level, L/A). We listed the top-10 most generalized species (both according to L and L/A) in the “world”, i.e., out of our sample of 1,403 plant species. Flower openness is defined as accessibility to the interior of the flower. We placed the blossom classes of Fægri & van der Pijl along a gradient, albeit not very well defined, of decreasing flower openness (dish-bowl, bell-funnel, head-brush, tube, gullet, flag) and tested for any relationship to their generalization level. The classes differed slightly but significantly in their level of L/A. Tube, bell-funnel, and dish-bowl had the highest generalization level and flag, gullet, and head-brush the lowest. Thus, flower openness and generalization level were not correlated. We discuss other factors influencing generalization level such as accessibility to pollen and nectar, morphology and behavior of visitor, and species diversity of the different functional types of visitors.

KEYWORDS: blossom class, ecomorphology, generalization level, pollination

the ecosystem. It will be an enormous task! … for total INTRODUCTION investigation of flower-pollinator interactions in only one Floral ecomorphology is the study of relationships ecosystem, complete dedication by the investigator will between the morphology of flowers and aspects of their be needed” (Baker, 1979: 437). ecology related to floral morphology, i.e., flower visitors, Here we address one important aspect of floral eco- and vice versa for the ecomorphology of flower visitors. morphology, viz. the relationship between flower open- Thus, flower and visitor together constitute an ecomor- ness of a plant species and its number of flower-visitor phological entity (Turner, 2002). A very closed flower, species. By openness we mean accessibility to the interior for example, may only interact with a single long-tongued of the flower and its rewards. We expect this relationship or physically strong visitor species. However, an entity to be significantly positive. It is so obvious an ecomor- may also encompass several highly interacting species, phological hypothesis in pollination biology that it has together constituting an interaction network compartment reached the status of truism. Nobody has, however, tested (Dicks & al., 2002). For example, plant species with an it on a large species sample. open flower morphology may attract a richer coterie of Flower openness. — Flower openness is a contin- flower-visitor species and together all species involved uous character, but for which no appropriate parameter make up a more complex entity. Consequently, floral is available. For this reason, we have to make do with ecomorphology has to take place on the level of the existing typological classification schemes. (sub-)community, i.e., we need data about the complete Carl von Linné, typologist par excellence, classified interaction environment of a set of flowering plant species according to their reproductive organs. Flower biol- sharing a visitor fauna in order to make valid statements ogists more fond of forms and colors of flowers and their about their ecomorphology (Jordano, 1987; Jordano & al., pollen, nectar, scent, and flower visitors went along other 2006). However, this is certainly a time-consuming task. roads of classification. Some dived into the diversity of Baker pleaded for a move towards ecosystem pollination flowers and inflorescences ignoring their visiting fauna, biology, but also noted that this was very laborious: “The whereas others focused upon characters assumed to be same sort of tallying, on a much more exact and quantified important to the attraction of animals. This debate about basis, needs to be done with all of the other species in choice of focus was imbedded in a broader typological-

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evolutionary controversy and has been ongoing since the species); (4) gullet (pollen is placed dorsally on pollinators; days of the flower biologist Delpino (1868–1874) (Olesen, e.g., Salvia and Acanthus species); (5) flag (pollen is most 2000; Waser, 2006). Delpino and other, much later, writers, often placed ventrally on pollinators; e.g., Fabaceae and in particular Vogel (e.g., 1954), van der Pijl (e.g., 1961), Corydalis species); and (6) tube blossoms (e.g., Primula and Fægri & van der Pijl (1971), discussed pollinator types species) (Fig. 1). Combinations are also often found, e.g., or classes, and pollination syndromes, illustrating and an open dish-shaped capitulum of a composite, where each listing important character states. Pollination syndromes flower is tube-shaped. In this study, 1–3 were regarded as were defined as suites of states expected to be adaptive open types and 4–6 as closed. to various classes of pollinators. The wind blew from complete rejection of any notion about classification to heralding its importance (van der Pijl, 1961). Classes of natural entities are commonly taken too MATERIAL AND METHODS literally by scientific and public readerships, which most Thirty-seven pollination networks extracted from 22 often was not the intention of their inventors. These sci- published and 7 unpublished studies were collated and con- entists, all being skilled naturalists, of course knew the stituted our network database. A pollination network depicts exceptions to their classificatory schemes. For example, graphically all flowering plant and flower-visitor species van der Pijl (1961) stressed that a plant can be more or less within an area and all their interactions. We included all adapted to a certain kind of pollinator. He says: I will try to “total” networks to which we had access. “Total” does not, revive interest in the classes according to the pollinators, of course, indicate that networks are completely sampled classes with bad boundaries, but with a clear centre, foci with respect to species and links, which no networks are of differentiation in different substrata, but leading to and never will be. It only refers to sampling width, i.e., convergence, a style [p. 44], and he goes on: The [earlier] all species involved in flower visitation are included irre- interest in demarcation and classification shall here be spective of taxonomic and functional affinity (Olesen & replaced by more positive elements [p. 48]. Jordano, 2002). All networks are also “temporarily cumu- Blossom classes. — The blossom classes of Fægri lative” (sensu Schoenly & Cohen, 1991), i.e., data originate & van der Pijl (1971) are characterized by a set of floral from one site only, but are, in general, sampled over an states, some of which may be adaptations to pollinators extensive period, most often one season. All networks or other flower visitors. They may be pooled into broader are described in detail in their individual references and classes of flower openness (Fig. 1) (à la Ramírez, 2003). their most important descriptors are tabulated in Olesen The former authors define a blossom as the pollination & Jordano (2002), Bascompte & al. (2003, 2006), Jordano unit. In most species flower and blossom are the same, & al. (2003, 2006), and Olesen & al. (2006). The networks but, for example, in the Asteraceae the blossom is both the originate from highly disparate sites all over the world. capitulum and the individual flower, whereas in others it However, lowland rainforest sites are unfortunately missing. is only a part of the flower such as in Iris, where it is one Sampling effort of flower-visitor species varied a lot in the third of the flower. Fægri & van der Pijl (1971) base their different network studies. Sorting of species according to classification of blossom classes upon what is termed “the their blossom types was based on information from floras, functional structure with regard to the … processes of pol- monographs, the World Wide Web, etc. In some plant spe- lination” (p. 99). They operate with three main categories: cies, scoring of blossom type was ambiguous. Asteraceae open (most angiosperm flowers); closed blossoms, e.g., species got a score of ½ in the dish category and ½ in the the flowers of Trollius europaeus (Hagerup & Petersson, tube category, and Apiaceae species got a score of ½ in the 1956), Linaria vulgaris (Newman & Thompson, 2005), dish category and ½ in the head/brush category. Informa- some Annonaceae species (Silberbauer-Gottsberger & al., tion on flower-visitor generalization level L was retrieved 2003; Gottsberger & Silberbauer-Gottsberger, 2006); and from the network database. L is generalization level and traps, e.g., the inflorescence of Arum (Knoll, 1926) and is measured as total number of flower-visitor species to a the flower of Ceropegia (Vogel, 1961). Here, we exclude plant species during the entire study period. In the dataset traps because of a shortage of data. The open blossoms a few plant species have several entries because they appear consist of inconspicuous (abiotically pollinated blossoms in more than one network. All these species entries are as in Zostera and Urtica [Fægri & van der Pijl, 1971]) kept separate in the analysis because they are members and conspicuous blossoms. Inconspicuous blossoms are of different networks varying in size. Plant species were also excluded from this analysis. Conspicuous and closed treated as independent data points. blossoms are sorted into six categories. (1) Dish- to bowl- According to the database almost all flower-visitor shaped (examples are the flowers of Rosa and Saxifraga species are insects, which may vary a lot in their floral species); (2) bell to funnel (e.g., and Convolv- behavior, e.g., pollination, florivory, rendezvous mating, ulus species); (3) head to brush (e.g., Salix and Myrtaceae egg-laying, perfume-collecting, floral resource robbery

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Fig. 1. Blossom classes each showing an example of a flower visitor. A, gullet: Lobelia stricta and the hummingbird Cyanophaia bicolor from the Island of Dominica; B, dish-bowl: Opuntia dillenii flower and the lizard Gallotia galloti from La Palma, the Canary Islands; C, bell-funnel: Wercklea tulipiflora and the bat Monophyllus plethodon from the Island of Dominica; D, brush-head: Echium nervosum and the lizard Podarcis dougesii on the Island of Madeira; E, flag: Chadzia irondoensis and the sunbird Nectarinia notata in Madagascar; F, tube: a Kniphofia hybrid and nectar-drinking blue-tit Parus caeruleus in a Danish garden (photos Jens M. Olesen).

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or just tourism. Non-pollinating florivores may be very Table 1. Frequency of blossom types (N = 1,403 common in flowers (Frame, 2003). However, we do not species). know how common. In generalist flowers, the number Blossom type % of sample of florivores may even be higher than the number of Open Dish-bowl 42.0 61.3 principal pollinators and these flowers may thus play an Bell-funnel 16.0 important role to the conservation of the biodiversity of Head-brush 3.2 flower-visiting insects in general (Frame, 2003). Closed Gullet 7.1 38.7 During the last couple of decades, the relative impor- Flag 7.6 tance of generalists and specialists in pollination networks Tube 24.0 has been intensely debated (Jordano, 1987; Herrera, 1996; Waser & al., 1996; Johnson & Steiner, 2000; Olesen & Jordano, 2002; Jordano & al., 2003, 2006; Fenster & al., 2004; Thompson, 2005; and chapters in Waser & Ollerton, 2006). Generalists are common, not just in pollination, but overall in ecological webs (Polis & Strong, 1996; Zamora, 2000). However, when one consults the many published link frequency distributions (e.g., Elberling & Olesen, 1999), generalist species make up a minority, although the bulk of links in any pollination network is between generalist species. In this paper we define a generalist as a taxon, which uses a broader piece of a given resource util- ization axis than most other taxa, belonging to the same functional group. Thus, a species is always a generalist— or a specialist—with respect to a particular resource axis and with respect to the other members of its community. In order to make valid comparisons, this definition also implies that one defines an operative taxonomical level and spatial scale (Fox, 1981).

RESULTS Fig. 2. Frequency distribution of generalization level or The sample of pollination networks included a total of number of flower-visitor links per plant species, L (sample 1,403 plant species and their 5,003 flower-visitor species. size is 1,403 plant species, but four species with an L > 100 Sixty-one percent of all plant species had an open blossom [104, 109, 124, 188] were excluded). (i.e., dish-bowl + bell-funnel + head-brush) and 39% had a closed blossom (i.e., flag + gullet + tube) (Table 1). Table 2. Frequency distribution of Average generalization level L was 9.7 ± 13.8 links generalization level or number of per plant species (median = 5, mode = 1). The frequency flower-visitor species links per plant distribution of L was extremely skewed (Fig. 2, Table 2). species, L (sample size is 1,403 plant Twenty-percent of all plant species were only visited by species). one flower-visitor species, and about half (52%) by ≤ 5 L No. plant species % visitor species. The top-10 most generalized plant species ≥10 443 32 ranked according to their L are listed in Table 3. Six (60%) 5–9 316 23 of these had a dish-bowl-shaped flower compared to 42% 4 101 7 3 111 8 in the total sample (Table 1). L was influenced by the size 2 156 11 of the flower-visitor community, A (Fig. 3). For this reason, 1 276 20 we redid the analysis using relative generalization level L/A. This is known to correct for most of the influence of A on L (Dupont & al., 2003). in Table 4. Eighty-five (85%) of these had a dish-bowl- Average L/A was 0.067 ± 0.094 links per plant per shaped flower. However, L/A and blossom type were not animal species. The frequency distribution of L/A was associated (Gadj = 0.75, df = 2, P < 0.76; Table 5). This list extremely skewed (Fig. 4). The top-10 most generalized was completely different from the L-list because of the plant species ranked according to their L/A are listed correction for variation in A.

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Table 3. The top-10 most generalized plant species ranked according to their generalization level L. Species Family Dish-Bowl Bell-Funnel Gullet Tube L Reference Anthriscus aemula Apiaceae 1 188 Kato & al., 1990 Thymus capitatus Lamiaceae 1 124 Petanidou, 1991 Angelica pubescens Apiaceae 1 119 Inoue & al., 1990 Persicaria thunbergii Polygonaceae 1 104 Inoue & al., 1990 Castanopsis sieboldii Fagaceae 1 101 Kato, 2000 Daphne gnidium Thymelaeaceae 1 86 Herrera, 1988 Rubus crataegifolius Rosaceae 1 84 Inoue & al., 1990 Reynoutria japonica Polygonaceae 1 78 Inoue & al., 1990 Deutzia crenata Hydrangeaceae 1 76 Inoue & al., 1990 Hydrangea paniculata Hydrangeaceae 1 75 Kato & al., 1990

Fig. 3. Relationship between generalization level L of plant Fig. 4. Frequency distribution of relative generalization level species and size of flower-visitor community A, i.e., num- per plant species, L/A (sample size is 1,403 plant species). ber of flower-visitor species in the network (sample size is 1,403 plant species; lnL = 0.27lnA + 0.22, F = 113, R2 = 0.07, P ≤ 0.0001).

Table 4. The top-10 most generalized plant species ranked according to their relative generalization level L/A. Species Family Dish-Bowl Bell-Funnel Tube L/A Reference Claytonia virginica Portulacaceae 1 0.70 Schemske & al., 1978 Cirsium arvense Asteraceae 0.5 0.5 0.68 Bundgaard, 2003 Azorina vidalii 1 0.67 Olesen & al., 2002 Dryas integrifolia Rosaceae 1 0.66 Kevan, 1970 Gastonia mauritiana Araliaceae 1 0.62 Olesen & al., 2002 Angelica archangelica Apiaceae 1 0.61 Bundgaard, 2003 Isopyrum biternatum Ranunculaceae 1 0.61 Schemske & al., 1978 Epilobium hirsutum Onagraceae 1 0.57 Bundgaard, 2003 Anthriscus sylvestris Apiaceae 1 0.57 Bundgaard, 2003 Angelica sylvestris Apiaceae 1 0.52 Bundgaard, 2003

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Table 5. L/A and blossom type (N = 1,403 plant species). the way for further, more detailed and much more inter- Types with different letters are significantly different in esting ecomorphological analyses. Dish- and bell-funnel- their relative generalization level (1-ANOVA: F = 2.38, P ≤ shaped flowers allow most flower-visiting animals access. 0.04). However, tubular flowers have an exclusive visitor fauna Blossom type Differences L/A of long-tongued animals. Hence, their high generalization Tube A 0.033 level may be explained by a high diversity of long-tongued Bell-funnel A 0.033 animals, such as lepidopterans and bees. Some flower Dish-bowl AB 0.030 Gullet ABC 0.025 types might have spurred a richer evolution among their Flag BC 0.024 visitors than other types (that is to say, certain bauplans Head-brush C 0.018 might have greater potential to influence the expansion of specific animal phyletic lines). Harvesting nectar and pollen from flag blossoms may require both specialized L/A varied significantly among blossom classes, but pollinator behavior and a critical body size, restricting it was not correlated with flower openness (Table 5). the visitor fauna to mainly large bees and birds. Brush The most generalized group was tube, bell, dish, and blossoms may pose problems to visiting animals too. gullet. Their L/A did not differ from each other. Thus, The density, length, and stiffness of stamens and styles the ecomorphological hypothesis did not pass our test: of many brush blossoms make nectar harvesting difficult openness did not correlate with generalization level. The for larger animals. Head-brush blossoms were here classi- closed type “tube” and the open type “bell” were more fied as open blossoms, but should maybe be regarded as a generalized than the closed type “flag” and the open type closed, specialized type. Thus, the generalization level of “head-brush”. a flower is influenced by accessibility to pollen and nec- tar, morphology and behavior of visitor, species diversity of the different functional types of visitors, etc. Other studies also relate flower morphology to pol- DISCUSSION linator diversity. Using Robertson’s (1928) dataset and The extensive database used in this analysis was far functional groups (long-tongued bees, short-tongued bees, from perfect. Its limitations have been discussed in Olesen other hymenopterans, Diptera, Coleoptera, Lepidoptera, & Jordano (2002). In particular, sampling effort varied, Hemiptera, Neuroptera, hummingbirds), Fenster & al. which, of course, influenced generalization level (Her- (2004) found that 52% of all open flowers were visited rera, 2005). Researchers spend very different amounts of by one functional group only, whereas this figure was 61% time observing pollinators to a plant species. However, in closed flowers. From this they concluded that increased the relation between sampling effort and L/A, is not obvi- floral complexity increases pollination specialization. ous and may follow various non-linear trajectories. Our McCall & Primack (1992) showed that visitation rate classification of flower and inflorescence into blossom (number of visits by all visitor species per flower per 100 type was doubtless too gross, possibly even inaccurate. minutes) to open flowers was 2.8 times higher than to Mother Nature does not make jumps and many blossoms tubular flowers. The visitor spectrum to the two flower may be intermediates between our restricted set of cat- types was quite similar, although flies and beetles were egories. The database did not include any information more common visitors of open flowers, whereas butterflies from lowland rainforests. Generalization level may vary were more common visitors of tubular flowers. In three between conspecifics within a population and number of Spanish localities, species having dish-shaped flowers or flower visits may be a better indicator of generalization tubular flowers were visited by the same number of insect level than number of visitor species (Gómez & Zamora, orders (ca. 2.7 orders per plant species, sample size was 83 1999). Generalization level is also dependent upon the plant species; Herrera, 1996). This is in accordance with size and taxonomic composition of the local visitor fauna our results, using number of species instead of number (Olesen, 2000). However, in this analysis we assumed that of visitor orders. However, 58 insect-pollinated, tubular- generalization level was a species property. The strength flowered species having a very long corolla tube ( > 20 of the database was, of course, its size and geographic mm) were only visited by 1–11 insect species, whereas range. short-corolla species ( < 10 mm) were visited by < 90 Using the database, we found that open blossoms insect species (from various sources and summarized by (dish-bowl, bell-funnel, head-brush) were twice as fre- Herrera, 1996). Thus, if a positive trend is present between quent as closed. Tubular, bell-funnel, and dish-shaped blossom openness and high L/A, it may especially stand blossoms were more generalized than especially flag and out in a within-blossom class comparison. head-brush blossoms. Thus, generalization level did not Pollinators may be sorted into broad pollinator agent simply follow level of flower openness. This result paves classes (sensu Ramírez, 2003), such as wind, beetles,

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flies, bees, etc. When this was done, Ramírez (2003) in a coevolutionary networks facilitate biodiversity mainte- large study found that number of pollinator agent classes nance. Science 312: 431–433. differed between blossom types. His ranking of blossom Bundgaard, M. 2003. Tidslig og Rumlig Variation i et Plante- types according to number of pollinating agent classes Bestøvernetværk. [Temporal and spatial variation in a plant-pollinator network]. MS thesis. Univ. Aarhus, Aar- was very similar to ours: bell, tube, dish, brush, gullet, hus. and flag with decreasing generalization level measured Dicks, L.V., Corbet, S.A. & Pywell, R.F. 2002. Compart- as number of pollinator agent classes (compare to Table mentalization in plant-insect flower webs. J. Anim. Ecol. 5). Flag and gullet blossoms were visited by 1.1–1.2 agent 71: 32–43. classes, and dish, bell, brush, and tube by 1.6–2.0. Polli- Dupont, Y.L., Hansen, D.M. & Olesen, J.M. 2003. Structure nators also preferred different blossom types (Ramírez, of a plant-flower visitor network in the high-altitude sub- 2003). Dish blossoms were visited by bees, flies and alpine desert of Tenerife, Canary Islands. Ecography 26: 301–310. wasps; tubes by butterflies, moths and birds, flags and Elberling, H. & Olesen, J.M. 1999. The structure of a high gullets by bees. Thus, from the studies of Ramírez (2003) latitude plant-pollinator system: the dominance of flies. and ours, we conclude that tubular-, bell-, and dish-shaped Ecography 22: 314–323. flowers are more generalized than flag-, gullet- and head/ Fægri, K. & van der Pijl, L. 1971. The Principles of Pollina- brush-shaped flowers. tion Ecology. Pergamon Press, Oxford. One point brought out by our sample is how efficient Fenster, C.B. 1991. Selection on floral morphology by hum- mingbirds. Biotropica 23: 98–101. temperate Apiaceae species are in attracting large num- Fenster, C.B., Armbruster, W.S., Wilson, P., Dudash, M.R. bers of flower visitors. Many of these visitor species only & Thomson, J.D. 2004. Pollination syndromes and floral visit Apiaceae species. Thus, Apiaceae are very important specialization. Annual Rev. Ecol. Syst. 35: 375–403. to local insect diversity. If these hub species disappear, Fox, L.R. & Morrow, P.A. 1981. Specialization: species prop- we may anticipate that many local flower visitors may erty or local phenomenon? Science 211: 887–893. disappear as well. In the bee-rich European Mediterra- Frame, D. 2003. Generalist flowers, biodiversity and florivory: nean, Thymus and maybe other Lamiaceae species, are implications for angiosperm origins. Taxon 52: 681–685. Gómez, J.M. & Zamora, R. 1999. Generalization vs. spe- important to bee diversity. If we had made a top-L list for cialization in the pollination system of Hormathophyllum the flower visitors, the most generalized species would be spinosa (Crucifera). Ecology 80: 796–805. species of Apis (honey bees) and Bombus (bumble bees) Gottsberger, G. & Silberbauer-Gottsberger, I. 2006. Life in (data not shown). the Cerrado: a South American Tropical Seasonal Ecosys- In our analysis, we ignored phylogenetical constraints. tem, vol. 2. Pollination and Seed Dispersal. Reta, Ulm. Therefore, future study directions might be analyses of Hagerup, O. & Petersson, V. 1956. Botanisk Atlas, vol. 1. Munksgaard, Copenhagen. specific systematic, evolutionary or ecological groups, Herrera, C.M. 1996. Floral traits and plant adaptation to in- such as the penstemons (Wilson & al., 2004), co-occurring sect pollinators: a devil’s advocate approach. Pp. 65–87 hummingbird-pollinated plant species (Snow & Snow, in: Lloyd, D.G. & Barrett, S.C.H. (eds.), Floral Biology. 1972; Fenster, 1991), or regional (Herrera, 1996; Fenster Chapman & Hall, New York. & al., 2004) and local floras. Herrera, C.M. 2005. Plant generalization on pollinators: species property or local phenomenon? Amer. J. Bot. 92: 13–20. Herrera, J. 1988. Pollination relationships in Southern Spanish ACKNOWLEDGEMENTS Mediterranean shrublands. J. Ecol. 76: 274–287. Inoue, T., Kato, M., Kakutani, T., Suka, T. & Itino, T. 1990. We thank Dawn Frame and Gerhard Gottsberger for their Insect-flower relationship in the temperate deciduous forest invitation to participate in the symposium about generalized of Kibune, Kyoto: an overview of the flowering phenology flowers at IBC 2005. Dawn Frame is thanked cordially for many and the seasonal pattern of insect visits. Contr. Biol. Lab. comments on the manuscript. The study was financed by a Kyoto Univ. 27: 377–463. Johnson, S.D. & Steiner, K.E. 2000. 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