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Functional complementarity and specialisation: The role of biodiversity in plantpollinator interactions

Nico Blthgena, , Alexandra-Maria Kleinb,c
a

Department of Animal Ecology and Tropical Biology, University of Wrzburg, Biozentrum, Am Hubland, 97074 Wrzburg, Germany Department of Crop Sciences, Section Agroecology, Georg-August University of Gttingen, Waldweg 26, 37073 Gttingen, Germany c Institute of Ecology, Section Ecosystem Functions, Leuphana University of Lneburg, Scharnhorststrae 1, 21335 Lneburg, 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 plantpollinator 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 owers 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 ower. Recent network analyses revealed that plantpollinator 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 owering phenology and/or nutritional variation in oral resources (nectar, pollen) may explain a complementary role of different ower species. From the plants 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 owers from the same plant individual, or vary in their functions within single owers. 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 plantpollinator functional relationships.

Zusammenfassung
Nischendifferenzierung (Komplementaritt) und kologische Nischenbreite (Spezialisierung) spielen eine Schlsselrolle in der Koexistenz von Arten und demzufolge fr die Biodiversitt. Einige Nischendimensionen von Arten bilden kosystemfunktionen (funktionale Nische) wie z.B. Bestubung. Wenn Arten sich in ihrem funktionellen Beitrag unterscheiden (funktionale Komplementaritt), lsst das darauf schlieen, dass artenreiche Gemeinschaften insgesamt leistungsfhiger als artenarme Gemeinschaften sind. Bezogen auf die Interaktionen von Blten und Bestubern impliziert funktionale Komplementaritt, dass eine grere Artenvielfalt der Bestuber zu einer besseren Bestubung der Panzenarten beitrgt und umgekehrt eine grere Bltenvielfalt

Corresponding

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

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

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besser die Ansprche der Bestuberarten deckt. Komplementaritt kann bei unterschiedlichen Skalen ansetzen und die kollektive Funktion der Gemeinschaft beeinussen, die Funktion einer einzigen Art, eines Individuums oder sogar nur eines Teils eines Individuums, z.B. einer einzelnen Blte. Neuere Netzwerkanalysen zeigen eine stark ausgeprgte Komplementaritt der Interaktionen zwischen Panzen- und Bestuberarten auf Gemeinschaftsniveau. Wir fassen unterschiedliche Mechanismen zusammen, die Komplementaritt hervorbringen. Aus der Sicht des Konsumenten knnen Unterschiede in der Phnologie oder Unterschiede in den Nhrstoffressourcen der Blten (z.B. Nektar, Pollen) eine komplementre Rolle mehrerer Panzenarten erklren. Aus der Sicht der Panze knnen zeitliche oder wetterbedingte Aktivittsunterschiede der Bestuberarten zu komplementren Effekte bei der Bestubung beitragen. Auerdem knnen verschiedene Tierarten unterschiedlich rumlich verteilte Blten eines Panzenindividuums bestuben oder sich die Funktion innerhalb einer Blte aufteilen. Bis heute sind empirische Nachweise komplementrer Effekte und mechanistische Erklrungen fr solche Effekte selten untersucht worden. Zuknftige vergleichende Untersuchungen zu Komplementarittseffekten sollten verschiedene Skalen bercksichtigen. Solche Studien knnen zum Verstndnis beitragen, ob und wie Artenvielfalt die Qualitt und Quantitt der funktionellen Beziehungen zwischen Blten und Bestubern frdert. 2010 Gesellschaft fr kologie. Published by Elsevier GmbH. All rights reserved.
Keywords: Complementary specialisation; Ecological networks; Ecological niche; Ecosystem functioning; H2 ; Mutualism; Nutrition; Pollination; 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), interspecic competition is reduced, facilitating their co-existence (MacArthur 1955; Elton 1958; Levine & HilleRisLambers 2009). Whereas the ecological niche concept includes various abiotic and biotic factors in multidimensional space, several niche dimensions represent important biotic processes and thus ecosystem functions, emphasised in the terms functional niche and functional (niche) complementarity (Loreau et al. 2001; Rosenfeld 2002). Functional redundancy in a community implies that species are mutually substitutable in terms of an ecological function. For instance, the quantitative reproductive tness of a plant may be equally high no matter if pollinated by a single pollinator species A, B or C or by all of them together in this case A, B, and C are redundant regarding this particular function. Functional complementarity suggests the opposite: A, B, 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. 2001; Petchey 2003; Finke & Snyder 2008). Specialisation and complementarity are related: complementarity requires a certain degree of specialisation of each species, while high generalisation is associated with high niche overlap and thus redundancy. In addition, redundancy can also occur if species are specialised on the same function (Fig. 1). Both complementarity and ecosystem functioning may occur at multiple scales, from individuals via species to entire functional groups. Our paper will focus on complementarity between species in the context of species diversity, and explore its functional consequences on different scales (individuals, species, and communities). The aim of this paper is (a) to conceptualise various mechanisms of complementar-

ity in owerpollinator relationships and (b) to briey sketch the functional consequences. Several mechanisms and effects are still speculative, thus we will also highlight some important gaps in our understanding of complementarity. Before drawing attention to plantpollinator interactions, we synthesise some general points about functional complementarity its importance in the biodiversityfunctioning relationship.

Functional consequences
As a consequence of functional complementary, the overall functional performance f of two species A and B together, f(A + B), should be larger than the performance of each species in isolation, so that f (A + B) > f (A) f (A + B) > f (B). Hence, the proposed overall functional effect is an example of synergism. In extreme cases, the participation of both species may be essential for an ecosystem function when A is unable to perform the function without B being present, i.e. f(n1 A + 0 B) = 0, where n1 = number of individuals of species A. The equation above not only represents an effect of niche complementarity, it also represents a prediction of ecological facilitation between A and B (examples for facilitation are given below). Effects of species complementarity should also be distinguished from a sampling or selection effect: does the density of a particular effective species, e.g. a highly productive plant, increase with species richness (Tilman, Lehman, & Thomson 1997; Loreau & Hector 2001)? When such effective species occurs in a density similar to that of all species together in a diverse community, will the functional performance of this particular species alone sufce to explain the functional effect size? Hence, demonstrating a causal effect of complementarity on an ecosystem function may not be trivial and cannot

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Fig. 1. The relationship between functional niche complementarity, biodiversity, and ecosystem stability. Species A and B are redundant if their functional niches overlap, either when they are both generalised, one is specialised on a subset of the others niche (nested), or both are specialised on the same function. Redundancy may improve the stability of a community, but also enhance interspecic competition when the target function represents a limited resource. Complementarity describes that species are functionally different, which requires that niches are relatively narrow. Certain functional performances then depend on a certain species (species A or B) and the system may therefore be more vulnerable to species losses, and the overall functioning increases with biodiversity.

necessarily be inferred from nor be fully understood by a statistical correlation between species diversity and the total magnitude of a function. It is important to test whether the increased functioning is not just due to confounding effects of overall higher density (Hoehn, Tscharntke, Tylianakis, & Steffan-Dewenter 2008). Hence, we can ask whether there is a signicant benet from the activity of different species that exceeds the effect of just adding more individuals of the same species. Specically, 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, so that f (n1 A + n2 B) > f ((n1 + n2 ) A) f (n1 A + n2 B) > f ((n1 + n2 ) B), where n1 and n2 represent numbers of individuals or activity densities. However, while this condition may be useful for detecting complementarity, it likely underestimates the importance of biodiversity for functioning. Because interspecic competition is usually lower than intraspecic competition, the overall density n1 + n2 for two coexisting species A and B may reach a higher level than a single species. A higher overall density is likely to translate into a higher overall functional performance. Moreover, the functional niche itself often represents a limited resource among which animals or plants compete. For instance, obligate nectar consumers A and B may be specialised to be active at different times of

the day, and given their temporal niche constraints, none of the species alone may reach a population density as high as their combined activity (n1 + n2 ). Such competitive avoidance would enhance the importance of complementarity for functioning. This effect of reduced interspecic competition is most evident when overall biomass production (e.g. plant productivity, see below) is the target functioning. In the functional context, the niche biodiversity relationship can be reversed to a biodiversity (functional) niche hypothesis (Fig. 1). Is a single species sufcient, 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. 2). When species differ entirely in their functional niche (strongest complementarity), a linear increase of the overall level of functioning with biodiversity is expected (Fig. 2B). In a scenario of no complementarity, species are completely redundant, and adding more species would not necessarily improve the functionality (Fig. 2). An intermediate level along the redundancy complementarity continuum would predict a saturating relationship (Fig. 2) (Gmez, Bosch, Perfectti, Fernndez, & Abdelaziz 2007). A smooth saturating curve (like the one illustrated in Fig. 2) may be predicted by theory, but may apply only to a scenario where niche overlaps among all species are the same, or when it represents an average scenario for randomly adding or removing species along the biodiversity axis multiple times. However, depending on the specic contribution of each species that

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Fig. 2. (A) Niche complementarity in multispecies interactions, displayed as a matrix with pollinator species as rows, plant species as columns and realised interactions as grey cells. Complementary specialisation increases from left to right. (B) The shape of the biodiversityfunctioning relationship depends on the extent of functional complementarity (redundant, intermediate or complementary). (C) Parallel to an improved functioning on the community scale, the diversity of the receiver may increase with a higher diversity of the transmitter of the function.

is added or lost (extinction order), the shape of an empirical biodiversityfunctioning relationship may vary. Some studies suggest a higher robustness of ecosystem functioning to biodiversity losses (Srinivasan, Dunne, Harte, & Martinez 2007), whereas a study that covered both pollination and dung decomposition found evidence for accelerating rather than saturating functions with higher biodiversity (Larsen, Williams, & Kremen 2005).

Community-scale functioning
Ecosystem functioning is often dened as the collective performance of an entire community and not only the effect on a single target species. When each of three pollinator species A, B, and C is fundamentally specialised on a different plant species X, Y, and Z, respectively, the overall pollination function for the plant community (comprising X, Y, and Z) may be highest when all pollinator species are present. Pollination success may then be lower for communities with a reduced set of pollinator species, for example only X will be pollinated, if only A is present. Here, the functional target needs to be carefully dened. When a monoculture of X occurs in the same density as a polyculture comprising X, Y and Z, and A in the same density as A, B, and C together, the community-wide seed set per area may be similar in the monoculture of X with A than in the polyculture. However, if polycultures have a higher performance for other reasons (e.g. differentiation in other niche

dimensions), or if the maintenance of biodiversity is a part of the functional target (e.g. reproductive success of as many species as possible; Fontaine, Dajoz, Meriguet, & Loreau 2006), total functioning in polycultures is higher than in monocultures. In this case, the degree of interaction partitioning between species (see next section) will be a predictor of the biodiversityfunctioning relationship. Such community-scale views are particularly common in studies of nutrient cycling, e.g. leaf litter degradation (Httenschwiler, Tiunov, & Scheu 2005). Moreover, measures of plant productivity have served as the most intensively studied community example for community functioning. The overall productivity of a plant community increases with the diversity of plants in grasslands, suggesting some extent of niche complementarity among the species involved (Hector et al. 1999). Various ecosystem functions performed by one guild represent a limited resource for another guild. In this way, one trophic level may have a functional contribution to another trophic level. Ecosystem functions provided to higher trophic levels include nutrition for parasitoid, herbivore, ower visitor or frugivore guilds; corresponding functions to the lower trophic levels include protection against enemies, herbivory, pollination or seed dispersal. Due to species complementarity, more food plant species together harbour a higher diversity of herbivores (Novotny et al. 2006), more hosts a higher diversity of parasitoids (Tylianakis, Tscharntke, & Klein 2006), and more owering plant species a higher diversity of ower visitors (Ebeling, Klein, Schumacher, Weisser, & Tscharntke, 2008). For obligate mutualisms, this implies a positive feedback between biodiversity of both parties: more pollinator species are required to effectively pollinate the entire plant community, and more ower species are required to nourish a higher diversity of consumers. It has been conrmed that the combined activity of different pollinator species increases the overall success of a small experimental plant community (Fontaine et al. 2006). Again, such positive biodiversity relationships would be expected only for functional associations with high complementarity (Fig. 2C). Broadening the perspective from a single functional niche dimension to multidimensional niche space, it is important to consider that redundancy in one niche dimension may be associated with complementarity in another (Loreau et al. 2001; Rosenfeld 2002). Moreover, redundancy under certain environmental conditions may not hold for other circumstances or under variable regimes and environmental impacts. In fact, the insurance hypothesis (Yachi & Loreau 1999; Loreau et al. 2001; Valone & Barber 2008) implies hidden long-term complementarity behind an apparent redundancy: when pollinator A becomes unreliable (e.g. due to population declines following unfavourable weather conditions), species B may compensate for the loss of functions performed by A. Such compensatory effects may be particularly pronounced when responses to stress and environmental changes (i.e. other niche dimensions) differ between A and B. This is adequately described by the term response diversity (Elmqvist

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et al. 2003; Lalibert et al. 2010). Consequently, systems with functional redundancy plus response diversity may be more resilient against population uctuations of associated species for months or years, or even longer time periods following local extinction.

Detecting complementarity patterns in ecological networks

Several quantitative niche overlap metrics (Krebs 1999) may be suited to characterise the degree of complementarity between species. In addition, species interaction networks represent functional links between species and may be used for inference about species complementarity. Each link in a network represents all of the interactions between a pair of species, e.g. between pollinator species A and plant species X. Fig. 2A displays networks in a matrix format. Links are often weighted by the number of interactions recorded. However, drawing inferences on specialisation and complementarity from raw data of a network can be problematic given that number of observations per species is unequal (Blthgen 2010). Using a method that accounts for unequal observations in a network, complementary specialisation can be characterised by the metrics di for each species and H2 for the entire network (Blthgen, Frnd, Vzquez, & Menzel 2008). Each di and the overall H2 increase (in the same way as the matrices illustrated in Fig. 2A) from 0.0 (highest redundancy) to 1.0 (highest complementarity possible). As stated above, high complementarity presupposes high specialisation (see Finke & Snyder 2008); thus di and H2 also express specialisation, but are conservative for cases where species are specialised on a commonly utilised niche (see Blthgen 2010). When these indices are applied to different systems, large variation in the extent of complementarity is found. Plantpollinator interactions often show a high level of complementarity, while plant-seed disperser associations have a signicantly lower H2 (Blthgen, Menzel, Hovestadt, Fiala, & Blthgen 2007). Complementarity (H2 ) of ower visits even on a single day is pronounced and relatively consistent across meadows irrespective of their management (Weiner, Werner, Linsenmair, & Blthgen 2011). High complementarity suggests that plant biodiversity may be important to sustain the ower visitor diversity and vice versa. This may explain both why biodiversity of both trophic levels showed a parallel decline over the last decades (Biesmeijer et al. 2006), and that diversity of pollinators increases with ower diversity (Frnd, Linsenmair, & Blthgen 2010). The increase in pollinator abundance and richness in habitats with higher ower diversity is particularly pronounced in those taxa that exhibit a high degree of specialisation (bees, butteries), whereas less specialised taxa (dipterans) poorly respond to ower diversity (Weiner et al. 2011). Correspondingly, in desert habitats where interactions between plants

and bees show a high complementarity (H2 ), bee species abundance and richness showed a stronger response to ower species richness than in garden habitats where H2 was lower (Gotlieb, Hollender, & Mandelik submitted for publication). However, before inferring functional complementarity from network data, several precautions should be considered. (1) Observed links may not always reect the function under consideration, as in the case of unrewarding ower visits or visits that do not result in a pollination event. Different links vary in quantitative functional importance. Whereas the interaction frequency of pollinators often reects their contribution to pollination of a plant (Vzquez, Morris, & Jordano 2005), this may not hold for every context, every plant species, and every link. (2) An interaction network summarises the observed interactions in the community contextrelated to the realised niche rather than fundamental niche. A single network may therefore underestimate the potential redundancy and dynamics of the system, but also fail to depict more subtle complementarity at the link scale, e.g. when different resources are involved in different links. Progress in understanding owerpollinator networks thus depends on linking the visitation patterns to functional variation between links and their spatio-temporal dynamics. (3) Since sampling effort is always limited in empirical datasets, the full range of plant species visited by a pollinator (and vice versa) may simply be undetected. Consequently, specialisation may be overestimated and complementarity erroneously inferred when using uncorrected metrics (Blthgen 2010). Below we will highlight some possible mechanisms that may explain complementary effects of different partner species on the population of a target species, separately for consumers (Fig. 3B and C) and plants (Fig. 3DF) as targets.

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. 3B). When their activity period exceeds the blooming period of a plant species, the availability of other plant species could become essential to bridge the temporal gaps in nourishment of the animals population (Baker 1963). If this species is a crucial pollinator, this scenario would represent a case of facilitation among plants, as the late owering plant species would benet from the presence of an earlier owering species and vice versa (Heinrich & Raven 1972; Waser & Real 1979; Moeller 2004). This effect may be widespread, since blooming periods of plant species are often relatively limited, and seasonality pronounced, while social bees and many other pollinators are active for several months (e.g. Olesen, Bascompte, Elberling, & Jordano 2008). Temporal partitioning in owering may even occur in the course of the

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Fig. 3. Complementarity conceptualized at different scales and mechanisms of plantpollinator interactions, including the partitioning of interactions in the community, effects on the pollinator species, and effects on the plant species. The partitioning of apical versus basal stigmata pollination within a strawberry ower (F) between larger and smaller bee species was shown by Chagnon et al. (1993).

day (Stone, Willmer, & Nee 1996), which might also affect the nourishment of a pollinator species on a short time scale.

Nutritional complementarity
Several ower-visiting species consume both pollen and nectar (Fig. 3C). Whereas nectar is mainly composed of a carbohydrate solution and contains relatively low amounts of amino acids among some other nutrients (Baker & Baker 1983), pollen is much richer in proteins, and also contains free amino acids, lipids, starch, sterols, and vitamins (Roulston & Cane 2000). However, surprisingly little is known about minerals and other trace elements in pollen and nectar. In bees, nectar is primarily used as an energy source for adults, whereas pollen is provisioned for growing larvae as their major protein source. Hence, bees and many other animals need to forage for both nectar and pollen. Both resources may be sometimes obtained from the same ower, 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. Like phenological complemen-

tarity, when plant species X and Y provide complementary resources such as pollen versus nectar, X may facilitate pollination of Y and vice versa (Ghazoul 2006). This facilitative mechanisms, based on complementary ower traits, may thus add to a more commonly predicted effect based on overlapping traits: different plant species enhance the overall oral display and generalist pollinator attraction, which seems likely for plant species with visually similar owers (Schemske 1981; Moeller 2004; Ghazoul 2006). Since pollen from different plants varies in nutrient composition as well as nectar sources, a dietary mix containing different plant species could be more nutritious than pollen or nectar from a single plant species. Some generalist herbivores may obtain a more balanced diet by feeding on different plant species (Behmer 2009). It has been rarely studied in generalised pollinators, and is best known for honeybees: while honeybee larvae grow well on a mixed diet of different pollen species, pure dandelion pollen is insufcient (see Roulston & Cane 2000). The addition of tryptophane which is missing or occurs in minute quantities in this pollen solves this problem (Roulston & Cane 2000), so the deciency in this essential amino acid is a case where complementary nutrition is required. In several pollen species, tryptophane and methionine occur in small quantities (Weiner, Hilpert, Werner, Linsenmair, & Blthgen 2010). Such decient resources are possible candidates where complementary nutrition may enhance the nutrient balance for the consumer. Moreover, diet mixing may help to avoid high concentrations of toxic compounds in herbivores (Singer, Bernays, & Carriere 2002), which is plausible but has not yet been demonstrated for ower visitors. Feeding bee larvae with mixed pollen diets indirectly suggests that toxin dilution may occur (Williams 2003), but mechanisms are yet to be shown. Toxins occur in pollen (Roulston & Cane 2000) as well as nectar (Adler 2000). Hence, positive effects of mixed pollen and/or nectar diets may provide indirect evidence for either nutritional complementarity or toxin dilution. In addition, mixed pollen diets were recently shown to have positive effects on the immunocompetence of honeybees compared to monospecic diets (Alaux, Ducloz, Crauser, & Le Conte 2010), although mechanisms are unresolved and require further investigations.

Mechanisms at the plant species scale: the plants viewpoint

Temporal or environmental complementarity
Whereas variation in phenology between plant species could affect ower visitors, see above (Fig. 3B), temporal complementarity of pollinators may be important for plants (Fig. 3D). Seasonal complementarity can play a role for plants that ower over longer periods, and inter-annual variation for perennial plants when pollinators uctuate between

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years. Complementarity may occur when different pollinator species of a target plant forage at different times of the day (Hoehn et al. 2008) or due to the distinction between diurnal and nocturnal pollinators (Dar, Arizmendi, & Valiente 2006; Muschala, Caiza, Vizuete & Thomson 2008). For example, a study of columnar cacti (Fleming, Sahley, Holland, Nason, & Hamrick 2001) compared the reproductive success of plant individuals that were either (O) continuously open to any pollinator, (D) only open to diurnal pollinators, or (N) open only to nocturnal pollinators, based on a temporal exclusion experiment. In one of four species studied, the authors demonstrated a signicant temporal complementarity, dened as a higher fruit set in control cacti [fruit set (O) > fruit set (D) + fruit set (N)]. The authors also predicted that pollinator complementarity may be more pronounced in plant species whose reproductive success is pollen limited, while redundancy may be common in resource limited plant species. It is expected that systems with strong temporal complementarity are vulnerable to climate warming when phenologies are changed, but changes differ between owers and their visitors, causing phenological mismatches (Memmott, Craze, Waser, & Price 2007Hegland, Nielsen, Lzaro, Bjerknes, & Totland 2009). Although ower phenology has been examined under different climatic conditions (e.g. Dunne, Harte, & Taylor 2003), studies that examined the functional role of interactions between pollinator and plant species in changing climatic conditions are missing (Hegland et al. 2009). Temporal complementarity (seasonal, daytime) is often regular and predictable, with pollinators being adapted to specic foraging activity periods (e.g. Stone et al. 1999). Related to such temporal niche differentiation is the idea that pollinators may vary in their response to site-specic weather conditions (Torres-Diaz, Cavieres, Munoz-Ramirez, & K. Arroyo 2007), particularly thermal constraints (Willmer 1983). Fluctuations in environmental conditions such as changes in temperature, moisture or wind velocity can disturb some species in their foraging activity, but not others which continue to forage. Hence, a complementarity based on variable pollinator responses to climatic conditions might represent a potential buffer against climate change for generalised plants (Hegland et al. 2009). Variation in responses to environmental conditions of otherwise functionally redundant species is the conceptual basis of response diversity (Elmqvist et al. 2003, see Community-scale functioning above) and represents an environmental complementarity (Fig. 3D) in the context of our paper.

owers on climbing pumpkin plant individuals. Such speciesspecic preferences for owers at single plant individuals represent a response to different micro-climatic conditions, for example, when lower owers are more shaded than higher and more exposed owers. Similarly, the pollinator community might be distinct at inner and outer regions of a tree canopy. In addition, the ower location on a plant may be associated with differences in ower shape or nectar concentration. Bumblebees, for example, respond to differences in ower shape (articial owers; Yoshioka et al. 2007) and nectar concentrations (zucchini owers, where it translates into seed set; Roldan-Serrano & Guerra-Sanz 2005). Architectural complementarity within plant individuals (Fig. 3E) thus represents a promising topic for future research, potentially explaining why pollinator diversity enhances pollination of certain plants. The different scales of complementarity could be linked: for plant individuals with extended blooming periods, temporal complementarity of different pollinators may also affect reproductive success at the plant individual scale, which may also be important for individual owers if they are long-lived. Complementarity among ower visitors to promote pollination within a single ower (Fig. 3F) was described in an aggregate strawberry fruit (Chagnon, Ingras, & de Oliveira 1993). Here, small bees mainly pollinated the basal stigmas, whereas larger bees such as honeybees pollinated the apical stigmas of a ower. Pollination success was optimal only when strawberry owers were pollinated by both groups. A similar pattern was observed in pumpkin owers (Hoehn et al. 2008). Again, small bees of the family Halictidae and Andrenidae foraged mainly at the base of a single, large stigma, whereas honeybees often foraged at the apical part or at the whole stigma. The behavioural differences in visitation at the ower scale remain to be studied. The relevance for plant species with an aggregate fruit such as the strawberry is clear: only when many stigmas per ower get pollinated, the fruit will be well shaped. For plant species with a single stigma per ower, such as pumpkin, the relevance is less clear, but possible mechanisms for a biodiversity-functioning relationship may include that (1) one ower-visiting species (A) transfers pollen to a ower, 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, for example, because the activity of B forces A to switch more often between plant individuals to facilitate cross pollination (Greenleaf & Kremen 2006). Functional complementarity may explain why the seed set of coffee increases with the diversity of pollinator species (Klein, Cunningham, Bos, & Steffan-Dewenter 2008).

Architectural complementarity

Conclusions
Complementary effects may also occur within plant individuals or even within a single ower. Hoehn et al. (2008) recently showed that certain bee species tend to forage at ground owers, whereas other bee species preferred higher Complementary specialisation of plantpollinator interactions is pronounced at the community scale: different pollinator species utilise and pollinate different plant species.

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This has been conrmed by quantitative network analyses. Responsible mechanisms for the high degree of species partitioning include ower morphology, visual and olfactory signals, and temporal variation among other factors. Floral morphological barriers (long, narrow tubes that are inaccessible to visitors that are too large or have a short proboscis) are particularly important in this regard (Stang, Klinkhamer, Waser, Stang, & van der Meijden 2009). Pollinators differ in their abilities to access a ower, which provides an explanation for the experimental evidence that bumblebees plus syrphids together contribute to a higher reproductive success of a plant community than either of the pollinator taxa alone (Fontaine et al. 2006). Due to functional complementarity, overall ecosystem functioning thus increases with biodiversity, a phenomenon that is widespread in several systems (Loreau et al. 2001; Balvanera et al. 2006) and across functions (Scherber et al. 2010). Compared to effects on the community scale, more subtle complementarity effects and less obvious traits on the species or individual scale are much less understood. For a ower visitor population, different plant species may provide food at different times (phenological complementarity) or different nutrients (resource complementarity). For a plant population, different pollinator species may complement each other due to differences in temporal activities (temporal complementarity). In addition, different species may serve different owers or parts of a ower of a plant individual (spatial complementarity), and interactions among species may facilitate the overall functioning (Hoehn et al. 2008; Klein, Mller, Hoehn, & Kremen 2009). It has thus been suggested that conservation should prioritise species with complementary functions, while functionally redundant species could be of lower importance, the rst ones acting as drivers, the latter as passengers of an ecosystem (Walker 1992). However, this would neglect the potential stabilising role of redundant species, e.g. when they differ in responses to disturbance or other changes in environmental conditions. The concept of environmental complementarity outlined above includes such complementary roles of otherwise functionally similar species. In general, species that appear similar in their ecosystem effects under particular conditions (e.g. in a short-term study) may be no longer redundant over longer time spans and a wider range of conditions (Chapin et al. 1997). Understanding the mechanisms and consequences of complementarity and redundancy is thus crucial to predict impacts of biodiversity on functioning in changing environmental conditions.

KL 1849/5-1. James Cresswell, Sara Leonhardt and an anonymous reviewer provided helpful comments on an earlier draft.

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Acknowledgements
Research projects of NB are funded by the Deutsche Forschungsgemeinschaft (DFG: Biodiversity Exploratories, SFB 554 and BL 960/1-1), those of AMK by the Alexander von Humboldt Foundation and DFG Biodiversity Exploratories KL 1849/3-1, KL 1849/4-1 and of the Jena Experiment

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