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BAAE-50467; No.

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ARTICLE IN PRESS

Basic and Applied Ecology xxx (2010) xxx–xxx

Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions
Nico Blüthgena,∗ , Alexandra-Maria Kleinb,c
a

Department of Animal Ecology and Tropical Biology, University of Würzburg, Biozentrum, Am Hubland, 97074 Würzburg, Germany Department of Crop Sciences, Section Agroecology, Georg-August University of Göttingen, Waldweg 26, 37073 Göttingen, Germany c Institute of Ecology, Section Ecosystem Functions, Leuphana University of Lüneburg, Scharnhorststraße 1, 21335 Lüneburg, Germany
b

Received 8 February 2010; accepted 1 November 2010

Abstract
Ecological niche breadth (specialisation) and niche differentiation (complementarity) play a key role for species coexistence and hence biodiversity. Some niche dimensions of a species represent ecosystem functions or services such as pollination (functional niche). When species differ in their contribution to some collective function (functional complementarity), this implies that functions from several species are required for a high overall functional performance level. Applied to plant–pollinator interactions, functional complementary suggests that a higher diversity of pollinators contributes to an increased pollination success of the plants or, in turn, that a higher diversity of flowers may better sustain the consumers’ requirements. Complementarity can affect functioning at different scales: the collective functioning of the target community, a single species, an individual or even a part of the individual, e.g. a single flower. Recent network analyses revealed that plant–pollinator interactions display a relatively high extent of complementary specialisation at the community scale. We propose several mechanisms that generate complementarity. From the consumers’ viewpoint, differences in flowering phenology and/or nutritional variation in floral resources (nectar, pollen) may explain a complementary role of different flower species. From the plant’s viewpoint, temporal or environmental variation in the pollinator species’ activities may contribute to complementary effects on pollination of plant communities. In addition, different species may also pollinate either more exposed or more sheltered flowers from the same plant individual, or vary in their functions within single flowers. So far, empirical evidence for complementary effects in general, and particularly mechanistic explanations of such effects are scant and will require comparative investigations at multiple scales in the future. Such studies will help us to understand if and how biodiversity maintains the quality and quantity of plant–pollinator functional relationships.

Zusammenfassung
Nischendifferenzierung (Komplementarität) und ökologische Nischenbreite (Spezialisierung) spielen eine Schlüsselrolle in der Koexistenz von Arten und demzufolge für die Biodiversität. Einige Nischendimensionen von Arten bilden Ökosystemfunktionen (funktionale Nische) wie z.B. Bestäubung. Wenn Arten sich in ihrem funktionellen Beitrag unterscheiden (funktionale Komplementarität), lässt das darauf schließen, dass artenreiche Gemeinschaften insgesamt leistungsfähiger als artenarme Gemeinschaften sind. Bezogen auf die Interaktionen von Blüten und Bestäubern impliziert funktionale Komplementarität, dass eine größere Artenvielfalt der Bestäuber zu einer besseren Bestäubung der Pflanzenarten beiträgt und umgekehrt eine größere Blütenvielfalt

∗ Corresponding

author. Tel.: +49 931 318 4370; fax: +49 931 318 4352. E-mail address: bluethgen@biozentrum.uni-wuerzburg.de (N. Blüthgen).

1439-1791/$ – see front matter © 2010 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.baae.2010.11.001

Please cite this article in press as: Blüthgen, N., & Klein, A.-M. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. Basic and Applied Ecology (2010), doi:10.1016/j.baae.2010.11.001

Levine & HilleRisLambers 2009). Keywords: Complementary specialisation. of Pages 10 2 ARTICLE IN PRESS N. Bis heute sind empirische Nachweise komplementärer Effekte und mechanistische Erklärungen für solche Effekte selten untersucht worden. f(n1 · A + 0 · B) = 0. Lehman.baae. z. Mutualism. i. Loreau & Hector 2001)? When such effective species occurs in a density similar to that of all species together in a diverse community. Neuere Netzwerkanalysen zeigen eine stark ausgeprägte Komplementarität der Interaktionen zwischen Pflanzen. facilitating their co-existence (MacArthur 1955..-M. demonstrating a causal effect of complementarity on an ecosystem function may not be trivial and cannot Please cite this article in press as: Blüthgen.11. f(A + B).g. Whereas the ecological niche concept includes various abiotic and biotic factors in multidimensional space. Rosenfeld 2002). einer einzelnen Blüte. the quantitative reproductive fitness of a plant may be equally high no matter if pollinated by a single pollinator species A. Wir fassen unterschiedliche Mechanismen zusammen. A. and C together contribute more to the function than any of them alone – a direct and positive effect of biodiversity on ecosystem functioning (Loreau et al. and communities). Published by Elsevier GmbH. Zukünftige vergleichende Untersuchungen zu Komplementaritätseffekten sollten verschiedene Skalen berücksichtigen. several niche dimensions represent important biotic processes and thus ecosystem functions.B. we synthesise some general points about functional complementarity its importance in the biodiversity–functioning relationship. the participation of both species may be essential for an ecosystem function – when A is unable to perform the function without B being present. Functional complementarity suggests the opposite: A. In extreme cases. thus we will also highlight some important gaps in our understanding of complementarity. Basic and Applied Ecology (2010). B. No.B. doi:10.001 .BAAE-50467. Pollination. the proposed overall functional effect is an example of synergism. Petchey 2003. 1). and explore its functional consequences on different scales (individuals. Aus der Sicht des Konsumenten können Unterschiede in der Phänologie oder Unterschiede in den Nährstoffressourcen der Blüten (z. Finke & Snyder 2008). 2001. Nektar. will the functional performance of this particular species alone suffice to explain the functional effect size? Hence.und Bestäuberarten auf Gemeinschaftsniveau. H2 . Blüthgen. where n1 = number of individuals of species A. Elton 1958. the overall functional performance f of two species A and B together. Ecological niche. Effects of species complementarity should also be distinguished from a ‘sampling’ or ‘selection’ effect: does the density of a particular effective species.-M. Functional redundancy in a community implies that species are mutually substitutable in terms of an ecological function. ob und wie Artenvielfalt die Qualität und Quantität der funktionellen Beziehungen zwischen Blüten und Bestäubern fördert. The aim of this paper is (a) to conceptualise various mechanisms of complementar- ity in flower–pollinator relationships and (b) to briefly sketch the functional consequences. die Komplementarität hervorbringen. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. © 2010 Gesellschaft für Ökologie. A.e. species. Hence. while high generalisation is associated with high niche overlap and thus redundancy. The equation above not only represents an effect of niche complementarity. and C are redundant regarding this particular function. redundancy can also occur if species are specialised on the same function (Fig.2010. so that f (A + B) > f (A) ∧ f (A + B) > f (B). increase with species richness (Tilman. N. Ecosystem functioning. B. & Thomson 1997. Before drawing attention to plant–pollinator interactions. Pollen) eine komplementäre Rolle mehrerer Pflanzenarten erklären. Specialisation and complementarity are related: complementarity requires a certain degree of specialisation of each species. Both complementarity and ecosystem functioning may occur at multiple scales. from individuals via species to entire functional groups. & Klein. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx besser die Ansprüche der Bestäuberarten deckt. Außerdem können verschiedene Tierarten unterschiedlich räumlich verteilte Blüten eines Pflanzenindividuums bestäuben oder sich die Funktion innerhalb einer Blüte aufteilen. Nutrition. Ecological networks. a highly productive plant. Redundancy The concept of functional complementarity Differentiation of ecological niches is known to promote biodiversity: when multiple species are specialised and differ in their niche (niche complementarity). In addition. emphasised in the terms ‘functional niche’ and ‘functional (niche) complementarity’ (Loreau et al. Functional consequences As a consequence of functional complementary. B or C or by all of them together – in this case A. interspecific competition is reduced. it also represents a prediction of ecological facilitation between A and B (examples for facilitation are given below). e. Komplementarität kann bei unterschiedlichen Skalen ansetzen und die kollektive Funktion der Gemeinschaft beeinflussen. 2001.1016/j. die Funktion einer einzigen Art. Solche Studien können zum Verständnis beitragen. Our paper will focus on complementarity between species in the context of species diversity. All rights reserved. eines Individuums oder sogar nur eines Teils eines Individuums. should be larger than the performance of each species in isolation. For instance. Several mechanisms and effects are still speculative. Aus der Sicht der Pflanze können zeitliche oder wetterbedingte Aktivitätsunterschiede der Bestäuberarten zu komplementären Effekte bei der Bestäubung beitragen.

2) (Gómez.-M. Tylianakis. Complementarity describes that species are functionally different. Basic and Applied Ecology (2010). but also enhance interspecific competition when the target function represents a limited resource. Certain functional performances then depend on a certain species (species A or B) and the system may therefore be more vulnerable to species losses. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. Fernández. a linear increase of the overall level of functioning with biodiversity is expected (Fig. In a scenario of no complementarity. see below) is the target functioning. Because interspecific competition is usually lower than intraspecific competition. the functional niche itself often represents a limited resource among which animals or plants compete. necessarily be inferred from nor be fully understood by a statistical correlation between species diversity and the total magnitude of a function. the overall density n1 + n2 for two coexisting species A and B may reach a higher level than a single species.11.1016/j. or are multiple species necessary to sustain the functional performance associated with a certain niche dimension? Overall functioning increases with the number of contributing species when their complementarity is pronounced (Fig. so that f (n1 · A + n2 · B) > f ((n1 + n2 ) · A) ∧ f (n1 · A + n2 · B) > f ((n1 + n2 ) · B). Redundancy may improve the stability of a community. obligate nectar consumers A and B may be specialised to be active at different times of the day. 2) may be predicted by theory. In the functional context. 2B). and adding more species would not necessarily improve the functionality (Fig. & Steffan-Dewenter 2008). Blüthgen. A smooth saturating curve (like the one illustrated in Fig. which requires that niches are relatively narrow. we can ask whether there is a significant benefit from the activity of different species that exceeds the effect of just adding more individuals of the same species. functional complementary may require that the overall functional performance f of two species A and B together is larger than those of each of the species alone at the same density. where n1 and n2 represent numbers of individuals or activity densities. However. A. When species differ entirely in their functional niche (strongest complementarity). No. 2). and ecosystem stability. and the overall functioning increases with biodiversity.g. 1. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx 3 Fig.001 . the niche → biodiversity relationship can be reversed to a biodiversity → (functional) niche hypothesis (Fig. Tscharntke. It is important to test whether the increased functioning is not just due to confounding effects of overall higher density (Hoehn. or both are specialised on the same function. 1). The relationship between functional niche complementarity.-M. while this condition may be useful for detecting complementarity. Species A and B are redundant if their functional niches overlap. N. of Pages 10 ARTICLE IN PRESS N. it likely underestimates the importance of biodiversity for functioning. A higher overall density is likely to translate into a higher overall functional performance. depending on the specific contribution of each species that Please cite this article in press as: Blüthgen. or when it represents an average scenario for randomly adding or removing species along the biodiversity axis multiple times. Moreover. but may apply only to a scenario where niche overlaps among all species are the same. none of the species alone may reach a population density as high as their combined activity (n1 + n2 ). either when they are both generalised. However.. & Klein.BAAE-50467. Hence. Bosch.baae. For instance. 2). This effect of reduced interspecific competition is most evident when overall biomass production (e. & Abdelaziz 2007). species are completely redundant. Is a single species sufficient.2010. Specifically. A. doi:10. one is specialised on a subset of the other’s niche (‘nested’). Such competitive avoidance would enhance the importance of complementarity for functioning. plant productivity. and given their temporal niche constraints. An intermediate level along the redundancy – complementarity continuum would predict a saturating relationship (Fig. biodiversity. Perfectti.

whereas a study that covered both pollination and dung decomposition found evidence for accelerating rather than saturating functions with higher biodiversity (Larsen. Klein. 2006). pollination or seed dispersal. Rosenfeld 2002). herbivory. suggesting some extent of niche complementarity among the species involved (Hector et al. A. the diversity of the receiver may increase with a higher diversity of the transmitter of the function. Moreover. due to population declines following unfavourable weather conditions). Some studies suggest a higher robustness of ecosystem functioning to biodiversity losses (Srinivasan. reproductive success of as many species as possible. intermediate or complementary). Moreover. measures of plant productivity have served as the most intensively studied community example for community functioning. 2. it is important to consider that redundancy in one niche dimension may be associated with complementarity in another (Loreau et al. This is adequately described by the term ‘response diversity’ (Elmqvist Please cite this article in press as: Blüthgen. and C together. No. Broadening the perspective from a single functional niche dimension to multidimensional niche space. & Scheu 2005). (A) Niche complementarity in multispecies interactions. and Z) may be highest when all pollinator species are present. Ecosystem functions provided to higher trophic levels include nutrition for parasitoid. the functional target needs to be carefully defined. the shape of an empirical biodiversity–functioning relationship may vary. Various ecosystem functions performed by one guild represent a limited resource for another guild.-M. more food plant species together harbour a higher diversity of herbivores (Novotny et al. Y and Z. and C is fundamentally specialised on a different plant species X. Loreau et al. if polycultures have a higher performance for other reasons (e. for example only X will be pollinated. In this way. e.2010. the overall pollination function for the plant community (comprising X. 2006). is added or lost (extinction order). Community-scale functioning Ecosystem functioning is often defined as the collective performance of an entire community and not only the effect on a single target species. 2008). 2C). N. flower visitor or frugivore guilds. leaf litter degradation (Hättenschwiler. Tscharntke. Here. Y. Due to species complementarity. this implies a positive feedback between biodiversity of both parties: more pollinator species are required to effectively pollinate the entire plant community. one trophic level may have a functional contribution to another trophic level. In fact. Again. B. Dajoz. Basic and Applied Ecology (2010). and more flower species are required to nourish a higher diversity of consumers. species B may compensate for the loss of functions performed by A. When each of three pollinator species A. (C) Parallel to an improved functioning on the community scale. redundancy under certain environmental conditions may not hold for other circumstances or under variable regimes and environmental impacts. the community-wide seed set per area may be similar in the monoculture of X with A than in the polyculture. displayed as a matrix with pollinator species as rows. of Pages 10 4 ARTICLE IN PRESS N. Complementary specialisation increases from left to right. It has been confirmed that the combined activity of different pollinator species increases the overall success of a small experimental plant community (Fontaine et al. such positive biodiversity relationships would be expected only for functional associations with high complementarity (Fig.baae. Fontaine. Blüthgen.-M. if only A is present.001 . When a monoculture of X occurs in the same density as a polyculture comprising X. Meriguet.g. Valone & Barber 2008) implies hidden long-term complementarity behind an apparent redundancy: when pollinator A becomes unreliable (e. Williams.g. & Klein. Schumacher.e. (B) The shape of the biodiversity–functioning relationship depends on the extent of functional complementarity (redundant. However. doi:10. 2001.BAAE-50467. differentiation in other niche dimensions). total functioning in polycultures is higher than in monocultures. Such community-scale views are particularly common in studies of nutrient cycling. Weisser. Dunne. & Tscharntke. Tiunov. and A in the same density as A. Harte. other niche dimensions) differ between A and B. & Loreau 2006). & Klein 2006). the degree of interaction partitioning between species (see next section) will be a predictor of the biodiversity–functioning relationship. For obligate mutualisms. respectively. 1999).11. Y.g. and Z. Such compensatory effects may be particularly pronounced when responses to stress and environmental changes (i. B.g. herbivore. 2001.1016/j. and more flowering plant species a higher diversity of flower visitors (Ebeling. Pollination success may then be lower for communities with a reduced set of pollinator species. In this case. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. or if the maintenance of biodiversity is a part of the functional target (e. A. plant species as columns and realised interactions as grey cells. & Martinez 2007). more hosts a higher diversity of parasitoids (Tylianakis. corresponding functions to the lower trophic levels include protection against enemies. the insurance hypothesis (Yachi & Loreau 1999. & Kremen 2005).. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx Fig. The overall productivity of a plant community increases with the diversity of plants in grasslands.

A single network may therefore underestimate the potential redundancy and dynamics of the system. the availability of other plant species could become essential to “bridge” the temporal gaps in nourishment of the animal’s population (Baker 1963). separately for consumers (Fig. 2A displays networks in a matrix format. This may explain both why biodiversity of both trophic levels showed a parallel decline over the last decades (Biesmeijer et al. Linsenmair. Fig. 2010). Waser & Real 1979. Plant–pollinator interactions often show a high level of complementarity. & Blüthgen 2011). 3B and C) and plants (Fig.-M. 3D–F) as targets. Fründ. Using a method that accounts for unequal observations in a network. As stated above. 2006). but also fail to depict more subtle complementarity at the link scale. Linsenmair. Menzel. Vázquez. Detecting complementarity patterns in ecological networks Several quantitative niche overlap metrics (Krebs 1999) may be suited to characterise the degree of complementarity between species. Each di and the overall H2 increase (in the same way as the matrices illustrated in Fig. Elberling.1016/j. This effect may be widespread. thus di and H2 also express specialisation. Progress in understanding flower–pollinator networks thus depends on linking the visitation patterns to functional variation between links and their spatio-temporal dynamics. Temporal partitioning in flowering may even occur in the course of the Please cite this article in press as: Blüthgen. or even longer time periods following local extinction. 3B). Laliberté et al. Correspondingly. Bascompte.11. Basic and Applied Ecology (2010). drawing inferences on specialisation and complementarity from raw data of a network can be problematic given that number of observations per species is unequal (Blüthgen 2010).0 (highest redundancy) to 1.2010. Each ‘link’ in a network represents all of the interactions between a pair of species. Complementarity (H2 ) of flower visits even on a single day is pronounced and relatively consistent across meadows irrespective of their management (Weiner. whereas less specialised taxa (dipterans) poorly respond to flower diversity (Weiner et al. high complementarity presupposes high specialisation (see Finke & Snyder 2008). Links are often weighted by the number of interactions recorded. High complementarity suggests that plant biodiversity may be important to sustain the flower visitor diversity and vice versa. Morris. in desert habitats where interactions between plants and bees show a high complementarity (H2 ). & Klein. Mechanisms at the animal species scale: the consumers’ viewpoint Phenological complementarity Flower-visiting species often utilise different plant species during the season or at different times of the day (Fig. 2A) from 0. this may not hold for every context. and every link. However. In addition. When their activity period exceeds the blooming period of a plant species. Olesen. while social bees and many other pollinators are active for several months (e. between pollinator species A and plant species X. & Blüthgen 2010).. 2003. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx 5 et al. complementary specialisation can be characterised by the metrics di for each species and H2 for the entire network (Blüthgen. several precautions should be considered. Consequently. before inferring functional complementarity from network data. Consequently. the full range of plant species visited by a pollinator (and vice versa) may simply be undetected.g. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. (2) An interaction network summarises the observed interactions in the community context–related to the realised niche rather than fundamental niche. and seasonality pronounced. & Jordano 2005). Hollender.g. as the late flowering plant species would benefit from the presence of an earlier flowering species and vice versa (Heinrich & Raven 1972. & Menzel 2008). (3) Since sampling effort is always limited in empirical datasets. Whereas the interaction frequency of pollinators often reflects their contribution to pollination of a plant (Vázquez. when different resources are involved in different links. Different links vary in quantitative functional importance. e. No. e. while plant-seed disperser associations have a significantly lower H2 (Blüthgen.0 (highest complementarity possible). large variation in the extent of complementarity is found. & Jordano 2008). Fiala. Hovestadt. species interaction networks represent functional links between species and may be used for inference about species complementarity. 2011). and that diversity of pollinators increases with flower diversity (Fründ. of Pages 10 ARTICLE IN PRESS N. butterflies). However.BAAE-50467. N. systems with functional redundancy plus response diversity may be more resilient against population fluctuations of associated species for months or years. If this species is a crucial pollinator. & Blüthgen 2007). specialisation may be overestimated and complementarity erroneously inferred when using uncorrected metrics (Blüthgen 2010). A. The increase in pollinator abundance and richness in habitats with higher flower diversity is particularly pronounced in those taxa that exhibit a high degree of specialisation (bees.-M. (1) Observed links may not always reflect the function under consideration. Blüthgen. but are conservative for cases where species are specialised on a commonly utilised niche (see Blüthgen 2010). every plant species. When these indices are applied to different systems.001 . as in the case of unrewarding flower visits or visits that do not result in a pollination event. bee species abundance and richness showed a stronger response to flower species richness than in garden habitats where H2 was lower (Gotlieb. & Mandelik submitted for publication). this scenario would represent a case of facilitation among plants. since blooming periods of plant species are often relatively limited.g. A. doi:10. Werner. Moeller 2004). Below we will highlight some possible mechanisms that may explain complementary effects of different partner species on the population of a target species.baae.

Ghazoul 2006). and also contains free amino acids. A. temporal complementarity of pollinators may be important for plants (Fig. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx Fig. when plant species X and Y provide complementary resources such as pollen versus nectar.-M.-M. which might also affect the nourishment of a pollinator species on a short time scale. However. positive effects of mixed pollen and/or nectar diets may provide indirect evidence for either nutritional complementarity or toxin dilution. doi:10. The addition of tryptophane which is missing or occurs in minute quantities in this pollen solves this problem (Roulston & Cane 2000). starch. so the deficiency in this essential amino acid is a case where complementary nutrition is required. tryptophane and methionine occur in small quantities (Weiner. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. pure dandelion pollen is insufficient (see Roulston & Cane 2000). In bees. based on complementary flower traits. Such deficient resources are possible candidates where complementary nutrition may enhance the nutrient balance for the consumer. but mechanisms are yet to be shown. which is plausible but has not yet been demonstrated for flower visitors. nectar is primarily used as an energy source for adults. Seasonal complementarity can play a role for plants that flower over longer periods.1016/j. & Carriere 2002). N.2010. Blüthgen. Moeller 2004. and is best known for honeybees: while honeybee larvae grow well on a mixed diet of different pollen species. Crauser. No. see above (Fig. Mechanisms at the plant species scale: the plants’ viewpoint Temporal or environmental complementarity Whereas variation in phenology between plant species could affect flower visitors. A. Since pollen from different plants varies in nutrient composition as well as nectar sources. whereas pollen is provisioned for growing larvae as their major protein source. diet mixing may help to avoid high concentrations of toxic compounds in herbivores (Singer. Basic and Applied Ecology (2010). lipids. In several pollen species. & Nee 1996). Willmer. but often need to be collected from two or more different plant species offering either nectar or pollen as the main reward – a case of complementary nutrition.001 . effects on the pollinator species. Bernays. surprisingly little is known about minerals and other trace elements in pollen and nectar. Linsenmair. 3C). The partitioning of apical versus basal stigmata pollination within a strawberry flower (F) between larger and smaller bee species was shown by Chagnon et al. 3B). Werner. 3.. and effects on the plant species. 3D). Moreover. Like phenological complemen- tarity. Feeding bee larvae with mixed pollen diets indirectly suggests that toxin dilution may occur (Williams 2003). bees and many other animals need to forage for both nectar and pollen. including the partitioning of interactions in the community. & Klein. This facilitative mechanisms. Toxins occur in pollen (Roulston & Cane 2000) as well as nectar (Adler 2000). Nutritional complementarity Several flower-visiting species consume both pollen and nectar (Fig. which seems likely for plant species with visually similar flowers (Schemske 1981. and vitamins (Roulston & Cane 2000). Both resources may be sometimes obtained from the same flower. of Pages 10 6 ARTICLE IN PRESS N. In addition. Some generalist herbivores may obtain a more balanced diet by feeding on different plant species (Behmer 2009).11. (1993). may thus add to a more commonly predicted effect based on overlapping traits: different plant species enhance the overall floral display and generalist pollinator attraction. Hilpert.baae. sterols. day (Stone. pollen is much richer in proteins. and inter-annual variation for perennial plants when pollinators fluctuate between Please cite this article in press as: Blüthgen. & Blüthgen 2010). mixed pollen diets were recently shown to have positive effects on the immunocompetence of honeybees compared to monospecific diets (Alaux. Complementarity conceptualized at different scales and mechanisms of plant–pollinator interactions. X may facilitate pollination of Y and vice versa (Ghazoul 2006). although mechanisms are unresolved and require further investigations. It has been rarely studied in generalised pollinators.BAAE-50467. Ducloz. a dietary mix containing different plant species could be more nutritious than pollen or nectar from a single plant species. Whereas nectar is mainly composed of a carbohydrate solution and contains relatively low amounts of amino acids among some other nutrients (Baker & Baker 1983). Hence. Hence. & Le Conte 2010).

the fruit will be well shaped. & Hamrick 2001) compared the reproductive success of plant individuals that were either (O) continuously open to any pollinator. Similarly. a complementarity based on variable pollinator responses to climatic conditions might represent a potential buffer against climate change for generalised plants (Hegland et al. Munoz-Ramirez. For plant species with a single stigma per flower. Waser. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. Craze. Basic and Applied Ecology (2010). Ingras. Holland.-M. Cavieres. large stigma. Sahley. 3D) in the context of our paper. Although flower phenology has been examined under different climatic conditions (e. Complementarity among flower visitors to promote pollination within a single flower (Fig. with pollinators being adapted to specific foraging activity periods (e. Please cite this article in press as: Blüthgen.11.g. Variation in responses to environmental conditions of otherwise functionally ‘redundant’ species is the conceptual basis of ‘response diversity’ (Elmqvist et al. the authors demonstrated a significant temporal complementarity.. whereas other bee species preferred higher Complementary specialisation of plant–pollinator interactions is pronounced at the community scale: different pollinator species utilise and pollinate different plant species. temporal complementarity of different pollinators may also affect reproductive success at the plant individual scale.1016/j. & Steffan-Dewenter 2008).001 . when lower flowers are more shaded than higher and more exposed flowers. based on a temporal exclusion experiment. Vizuete & Thomson 2008). It is expected that systems with strong temporal complementarity are vulnerable to climate warming when phenologies are changed. for example. studies that examined the functional role of interactions between pollinator and plant species in changing climatic conditions are missing (Hegland et al. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx 7 years. the pollinator community might be distinct at inner and outer regions of a tree canopy. of Pages 10 ARTICLE IN PRESS N. Roldan-Serrano & Guerra-Sanz 2005).2010. because the activity of B forces A to switch more often between plant individuals to facilitate cross pollination (Greenleaf & Kremen 2006). small bees of the family Halictidae and Andrenidae foraged mainly at the base of a single. daytime) is often regular and predictable. Pollination success was optimal only when strawberry flowers were pollinated by both groups. but changes differ between flowers and their visitors. 2007) and nectar concentrations (zucchini flowers. (2008) recently showed that certain bee species tend to forage at ground flowers. In one of four species studied. 3E) thus represents a promising topic for future research. 2003. A. whereas larger bees such as honeybees pollinated the apical stigmas of a flower. doi:10. & K. causing phenological mismatches (Memmott. Again. Functional complementarity may explain why the seed set of coffee increases with the diversity of pollinator species (Klein. Hoehn et al. respond to differences in flower shape (artificial flowers. for example.baae. the flower location on a plant may be associated with differences in flower shape or nectar concentration. No. Temporal complementarity (seasonal. Complementarity may occur when different pollinator species of a target plant forage at different times of the day (Hoehn et al. Such speciesspecific preferences for flowers at single plant individuals represent a response to different micro-climatic conditions. Fluctuations in environmental conditions such as changes in temperature. The authors also predicted that pollinator complementarity may be more pronounced in plant species whose reproductive success is pollen limited. N. Dunne. particularly thermal constraints (Willmer 1983). & Price 2007Hegland. A. for example. A similar pattern was observed in pumpkin flowers (Hoehn et al. Architectural complementarity within plant individuals (Fig.BAAE-50467. Harte. 1999). 2008) or due to the distinction between diurnal and nocturnal pollinators (Dar. 2008). Lázaro. small bees mainly pollinated the basal stigmas. Cunningham. Nielsen. while redundancy may be common in resource limited plant species. whereas honeybees often foraged at the apical part or at the whole stigma. 2009). Stone et al. Blüthgen. Caiza. (D) only open to diurnal pollinators. & Taylor 2003). potentially explaining why pollinator diversity enhances pollination of certain plants. defined as a higher fruit set in control cacti [fruit set (O) > fruit set (D) + fruit set (N)]. Architectural complementarity Conclusions Complementary effects may also occur within plant individuals or even within a single flower. 3F) was described in an aggregate strawberry fruit (Chagnon. or (N) open only to nocturnal pollinators. The different scales of complementarity could be linked: for plant individuals with extended blooming periods. For example. see Community-scale functioning above) and represents an ‘environmental complementarity’ (Fig. Yoshioka et al. a study of columnar cacti (Fleming. & de Oliveira 1993). & Totland 2009). which may also be important for individual flowers if they are long-lived.-M. Hence. Arizmendi. but not others which continue to forage. 2009). where it translates into seed set.g. & Valiente 2006. Arroyo 2007). the relevance is less clear. Bos. In addition. Bjerknes. flowers on climbing pumpkin plant individuals. Muschala. Bumblebees. Nason. but possible mechanisms for a biodiversity-functioning relationship may include that (1) one flower-visiting species (A) transfers pollen to a flower. Related to such temporal niche differentiation is the idea that pollinators may vary in their response to site-specific weather conditions (Torres-Diaz. such as pumpkin. moisture or wind velocity can disturb some species in their foraging activity. & Klein. The behavioural differences in visitation at the flower scale remain to be studied. whereas another species (B) is needed to place the pollen at the right place on the stigma or (2) that A is only an effective pollinator when B is present. Here. The relevance for plant species with an aggregate fruit such as the strawberry is clear: only when many stigmas per flower get pollinated.

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