Você está na página 1de 10

BAAE-50467; No.

of Pages 10


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

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

Received 8 February 2010; accepted 1 November 2010

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.

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

Neuere Netzwerkanalysen zeigen eine stark ausgeprägte Komplementarität der Interaktionen zwischen Pflanzen.B.001 . emphasised in the terms ‘functional niche’ and ‘functional (niche) complementarity’ (Loreau et al. In extreme cases.baae. Petchey 2003. Keywords: Complementary specialisation. Nutrition. Effects of species complementarity should also be distinguished from a ‘sampling’ or ‘selection’ effect: does the density of a particular effective species. 2001. and communities). the quantitative reproductive fitness of a plant may be equally high no matter if pollinated by a single pollinator species A. 2001. & Klein. Blüthgen. Whereas the ecological niche concept includes various abiotic and biotic factors in multidimensional space. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx besser die Ansprüche der Bestäuberarten deckt. H2 . Levine & HilleRisLambers 2009).B. B or C or by all of them together – in this case A. B. Both complementarity and ecosystem functioning may occur at multiple scales. In addition. z. where n1 = number of individuals of species A.-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. 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. N. Aus der Sicht des Konsumenten können Unterschiede in der Phänologie oder Unterschiede in den Nährstoffressourcen der Blüten (z. Finke & Snyder 2008). The equation above not only represents an effect of niche complementarity. einer einzelnen Blüte. 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). Functional redundancy in a community implies that species are mutually substitutable in terms of an ecological function. we synthesise some general points about functional complementarity its importance in the biodiversity–functioning relationship. of Pages 10 2 ARTICLE IN PRESS N.und Bestäuberarten auf Gemeinschaftsniveau. f(A + B). redundancy can also occur if species are specialised on the same function (Fig. Functional consequences As a consequence of functional complementary. Ecosystem functioning. it also represents a prediction of ecological facilitation between A and B (examples for facilitation are given below). Elton 1958. Mutualism.-M. B. species. Functional complementarity suggests the opposite: A. All rights reserved. Published by Elsevier GmbH. Nektar. i. A. die Funktion einer einzigen Art. the overall functional performance f of two species A and B together. several niche dimensions represent important biotic processes and thus ecosystem functions. Before drawing attention to plant–pollinator interactions. Ecological networks. For instance. will the functional performance of this particular species alone suffice to explain the functional effect size? Hence. Hence. should be larger than the performance of each species in isolation. facilitating their co-existence (MacArthur 1955. eines Individuums oder sogar nur eines Teils eines Individuums. while high generalisation is associated with high niche overlap and thus redundancy. and explore its functional consequences on different scales (individuals. Pollination. Aus der Sicht der Pflanze können zeitliche oder wetterbedingte Aktivitätsunterschiede der Bestäuberarten zu komplementären Effekte bei der Bestäubung beitragen.11. the proposed overall functional effect is an example of synergism. Bis heute sind empirische Nachweise komplementärer Effekte und mechanistische Erklärungen für solche Effekte selten untersucht worden. f(n1 · A + 0 · B) = 0. Zukünftige vergleichende Untersuchungen zu Komplementaritätseffekten sollten verschiedene Skalen berücksichtigen. Specialisation and complementarity are related: complementarity requires a certain degree of specialisation of each species. No.g. A. so that f (A + B) > f (A) ∧ f (A + B) > f (B). Rosenfeld 2002). & Thomson 1997. Wir fassen unterschiedliche Mechanismen zusammen. Basic and Applied Ecology (2010). e. Solche Studien können zum Verständnis beitragen. Ecological niche. thus we will also highlight some important gaps in our understanding of complementarity. the participation of both species may be essential for an ecosystem function – when A is unable to perform the function without B being present. Pollen) eine komplementäre Rolle mehrerer Pflanzenarten erklären. die Komplementarität hervorbringen. Komplementarität kann bei unterschiedlichen Skalen ansetzen und die kollektive Funktion der Gemeinschaft beeinflussen. and C are redundant regarding this particular function. doi:10. a highly productive plant. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions.e. Loreau & Hector 2001)? When such effective species occurs in a density similar to that of all species together in a diverse community. Several mechanisms and effects are still speculative. Our paper will focus on complementarity between species in the context of species diversity.1016/j. ob und wie Artenvielfalt die Qualität und Quantität der funktionellen Beziehungen zwischen Blüten und Bestäubern fördert. interspecific competition is reduced.. 1). Lehman. from individuals via species to entire functional groups. increase with species richness (Tilman. © 2010 Gesellschaft für Ökologie.2010.BAAE-50467. 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. Außerdem können verschiedene Tierarten unterschiedlich räumlich verteilte Blüten eines Pflanzenindividuums bestäuben oder sich die Funktion innerhalb einer Blüte aufteilen.

However. a linear increase of the overall level of functioning with biodiversity is expected (Fig. either when they are both generalised. and the overall functioning increases with biodiversity. 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. Basic and Applied Ecology (2010). but may apply only to a scenario where niche overlaps among all species are the same. 2) may be predicted by theory. see below) is the target functioning. obligate nectar consumers A and B may be specialised to be active at different times of the day. 2). doi:10. so that f (n1 · A + n2 · B) > f ((n1 + n2 ) · A) ∧ f (n1 · A + n2 · B) > f ((n1 + n2 ) · B).-M. Redundancy may improve the stability of a community. Because interspecific competition is usually lower than intraspecific competition. necessarily be inferred from nor be fully understood by a statistical correlation between species diversity and the total magnitude of a function. Such competitive avoidance would enhance the importance of complementarity for functioning. Blüthgen. Perfectti. which requires that niches are relatively narrow. or when it represents an average scenario for randomly adding or removing species along the biodiversity axis multiple times.1016/j. Is a single species sufficient. 2). Hence. species are completely redundant. Moreover. In the functional context. the functional niche itself often represents a limited resource among which animals or plants compete. Certain functional performances then depend on a certain species (species A or B) and the system may therefore be more vulnerable to species losses.-M. none of the species alone may reach a population density as high as their combined activity (n1 + n2 ). A. N. the niche → biodiversity relationship can be reversed to a biodiversity → (functional) niche hypothesis (Fig. No. Fernández. it likely underestimates the importance of biodiversity for functioning. 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. and adding more species would not necessarily improve the functionality (Fig. biodiversity. where n1 and n2 represent numbers of individuals or activity densities. Complementarity describes that species are functionally different. one is specialised on a subset of the other’s niche (‘nested’). and given their temporal niche constraints. & Steffan-Dewenter 2008). In a scenario of no complementarity. When species differ entirely in their functional niche (strongest complementarity). This effect of reduced interspecific competition is most evident when overall biomass production (e. plant productivity. and ecosystem stability. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx 3 Fig. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions.baae.BAAE-50467.11. A smooth saturating curve (like the one illustrated in Fig. the overall density n1 + n2 for two coexisting species A and B may reach a higher level than a single species. & Klein. Bosch. & Abdelaziz 2007). An intermediate level along the redundancy – complementarity continuum would predict a saturating relationship (Fig. Tscharntke.001 . 2B). For instance. of Pages 10 ARTICLE IN PRESS N. A. while this condition may be useful for detecting complementarity.. 2) (Gómez.2010. 1. It is important to test whether the increased functioning is not just due to confounding effects of overall higher density (Hoehn. However. The relationship between functional niche complementarity. or both are specialised on the same function.g. depending on the specific contribution of each species that Please cite this article in press as: Blüthgen. A higher overall density is likely to translate into a higher overall functional performance. 1). Tylianakis. but also enhance interspecific competition when the target function represents a limited resource. Species A and B are redundant if their functional niches overlap. 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. Specifically.

001 . Meriguet. Basic and Applied Ecology (2010). such positive biodiversity relationships would be expected only for functional associations with high complementarity (Fig. of Pages 10 4 ARTICLE IN PRESS N. Again. for example only X will be pollinated. The overall productivity of a plant community increases with the diversity of plants in grasslands. or if the maintenance of biodiversity is a part of the functional target (e. 2001. differentiation in other niche dimensions). redundancy under certain environmental conditions may not hold for other circumstances or under variable regimes and environmental impacts. the diversity of the receiver may increase with a higher diversity of the transmitter of the function. Dunne. A. Such community-scale views are particularly common in studies of nutrient cycling. suggesting some extent of niche complementarity among the species involved (Hector et al. and A in the same density as A. the functional target needs to be carefully defined. corresponding functions to the lower trophic levels include protection against enemies. Fontaine. & Scheu 2005). When a monoculture of X occurs in the same density as a polyculture comprising X. Valone & Barber 2008) implies hidden long-term complementarity behind an apparent redundancy: when pollinator A becomes unreliable (e. 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. leaf litter degradation (Hättenschwiler. Y. & Martinez 2007). (A) Niche complementarity in multispecies interactions. & Kremen 2005). the community-wide seed set per area may be similar in the monoculture of X with A than in the polyculture. When each of three pollinator species A. 2C). if only A is present. Pollination success may then be lower for communities with a reduced set of pollinator species. e. whereas a study that covered both pollination and dung decomposition found evidence for accelerating rather than saturating functions with higher biodiversity (Larsen. the shape of an empirical biodiversity–functioning relationship may vary. species B may compensate for the loss of functions performed by A. herbivore. displayed as a matrix with pollinator species as rows. and C is fundamentally specialised on a different plant species X. Williams.-M. other niche dimensions) differ between A and B. total functioning in polycultures is higher than in monocultures. due to population declines following unfavourable weather conditions). 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. pollination or seed dispersal. (B) The shape of the biodiversity–functioning relationship depends on the extent of functional complementarity (redundant. 2006). This is adequately described by the term ‘response diversity’ (Elmqvist Please cite this article in press as: Blüthgen. Dajoz.e. more hosts a higher diversity of parasitoids (Tylianakis. 2008). Weisser. herbivory. doi:10. Moreover. No. Y. Rosenfeld 2002). measures of plant productivity have served as the most intensively studied community example for community functioning. Schumacher.1016/j. & Klein 2006).g. Ecosystem functions provided to higher trophic levels include nutrition for parasitoid. 2001. 1999). and C together.g. reproductive success of as many species as possible. Here.BAAE-50467. it is important to consider that redundancy in one niche dimension may be associated with complementarity in another (Loreau et al. Y and Z. 2006). and more flowering plant species a higher diversity of flower visitors (Ebeling. Loreau et al. In fact.11. B. and Z. Blüthgen. one trophic level may have a functional contribution to another trophic level.baae. and more flower species are required to nourish a higher diversity of consumers. Tscharntke. more food plant species together harbour a higher diversity of herbivores (Novotny et al. Some studies suggest a higher robustness of ecosystem functioning to biodiversity losses (Srinivasan.. and Z) may be highest when all pollinator species are present. & Loreau 2006).-M. & Tscharntke. N. In this case. the insurance hypothesis (Yachi & Loreau 1999. Broadening the perspective from a single functional niche dimension to multidimensional niche space.g. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. In this way. is added or lost (extinction order). respectively. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx Fig. Due to species complementarity. the overall pollination function for the plant community (comprising X. (C) Parallel to an improved functioning on the community scale.2010. 2. A. this implies a positive feedback between biodiversity of both parties: more pollinator species are required to effectively pollinate the entire plant community. & Klein. Moreover. Harte. intermediate or complementary). Klein. plant species as columns and realised interactions as grey cells. Tiunov. B. flower visitor or frugivore guilds. Complementary specialisation increases from left to right.g. the degree of interaction partitioning between species (see next section) will be a predictor of the biodiversity–functioning relationship. Such compensatory effects may be particularly pronounced when responses to stress and environmental changes (i. Various ecosystem functions performed by one guild represent a limited resource for another guild. if polycultures have a higher performance for other reasons (e. However. For obligate mutualisms.

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

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

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

B.. M.. N. Weisser. Fiala. Biesmeijer. Specialization. & van der Meijden 2009). U.. 139. a phenomenon that is widespread in several systems (Loreau et al. (1983). I. & Tscharntke. H.BAAE-50467.. & T. et al. The biology of nectaries (pp.. (2006). C. overall ecosystem functioning thus increases with biodiversity. Current Biology. D. C.. N. Hooper. (2010).2010. Folke. the first ones acting as “drivers”. References Adler. Klein. F. 488–494.. (2000). & Valiente.-S. In addition. ecosystem change. S. Basic and Applied Ecology... H. (2009). 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. & Menzel. A... J. 69–86.. 86. Insect herbivore nutrient regulation. in a short-term study) may be no longer redundant over longer time spans and a wider range of conditions (Chapin et al. P. 277. Peeters. What do interaction network metrics tell us about specialization and biological traits? Ecology. In general. and resilience. Sala. C. Ecology Letters. M. (2006). Evolutionary mechanisms in pollination biology.. 2006). Diurnal and nocturnal pollination of Marginatocereus marginatus (Pachycereeae: Cactaceae) in central Mexico. those of AMK by the Alexander von Humboldt Foundation and DFG Biodiversity Exploratories KL 1849/3-1. 97. Lawton. SFB 554 and BL 960/1-1). (2007). Menzel. James Cresswell. (1958). P. Basic and Applied Ecology (2010). Ecological Monographs.. Vázquez. S. Science.. A. (1997). 11. P. The ecological significance of toxic nectar.. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. more subtle complementarity effects and less obvious traits on the species or individual scale are much less understood. London. H... (2006). Raffaelli. D. Bengtsson. species that appear similar in their ecosystem effects under particular conditions (e. F. Peterson. & Klein. and conflicting interests in mutualistic networks.. Responsible mechanisms for the high degree of species partitioning include flower morphology. e. Walker. R. Balvanera. Compared to effects on the community scale. the latter as “passengers” of an ecosystem (Walker 1992). Pfisterer. 89. W.-M. Klinkhamer. 416–420. Ohlemüller. J. Methuen and Co. while functionally redundant species could be of lower importance. KL 1849/4-1 and of the Jena Experiment Please cite this article in press as: Blüthgen. Hobbs.. 126–152). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. 185–195.11.-M. Crauser. A. Sara Leonhardt and an anonymous reviewer provided helpful comments on an earlier draft. Schumacher. 562–565. E. J. Response diversity. Ducloz. et al. & Baker. S. Bentley.. 6. 313. Arizmendi. doi:10. (2008). & Blüthgen. A. J.. 1997).. constraints.1016/j. Müller.. Dar.. 423–427. He. Chapin.. Klein. A. J. S.. when they differ in responses to disturbance or other changes in environmental conditions. 500–504.g. 877–883. 91. Due to functional complementarity. T. et al. F. S.. Elmqvist. 2008. Subalpine meadow flowering phenology responses to climate change: Integrating experimental and gradient methods. Nyström. Behmer.. 17. Harte. narrow tubes that are inaccessible to visitors that are too large or have a short proboscis) are particularly important in this regard (Stang. F. Blüthgen. Pollinators differ in their abilities to access a flower. N. Science. Dunne.. D.. New York: Columbia University Press. No. Y. Hovestadt. B. Annual Review of Entomology. different pollinator species may complement each other due to differences in temporal activities (temporal complementarity). (1993). Blüthgen.. The ecology of invasions by animals and plants. Annals of Botany. J. D. Frontiers in Ecology and the Environment. Blüthgen.... T. C. Journal of Economic Entomology. The concept of environmental complementarity outlined above includes such complementary roles of otherwise functionally similar species. It has thus been suggested that conservation should prioritise species with complementary functions. different species may serve different flowers or parts of a flower of a plant individual (spatial complementarity). & Kremen 2009). et al. and temporal variation among other factors. Science. KL 1849/5-1. A. Elton. & Le Conte. J. (1963). UK: T. T. T. 1808–1815. Stang. Edwards. Biology Letters. Ebeling. Ingras. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx This has been confirmed by quantitative network analyses. B. J.baae. (2010). Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. A brief historical review of the chemistry of floral nectar.. N. L. Reemer. (2008). D. Baker. R. J. different plant species may provide food at different times (phenological complementarity) or different nutrients (resource complementarity). H. Roberts. Effect of honey bee (Hymenoptera: Apidae) visits on the pollination rate of strawberries. Balvanera et al. Blüthgen. 2010). N. Hoehn. Understanding the mechanisms and consequences of complementarity and redundancy is thus crucial to predict impacts of biodiversity on functioning in changing environmental conditions.. How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos. K. 54. 73.. T. Fründ. Nakashizuka. G.g. & Taylor. In B.. and interactions among species may facilitate the overall functioning (Hoehn et al. 117. 351–354.. G. 1. 409–420. 1146–1156.. Oikos. Baker. 2001. & de Oliveira. M. 2006) and across functions (Scherber et al... O. 165–187.. N. (2003). M. For a flower visitor population.001 . Waser. 3387–3399. J. For a plant population. M. T. 9. Diet effects on honeybee immunocompetence. W. Acknowledgements Research projects of NB are funded by the Deutsche Forschungsgemeinschaft (DFG: Biodiversity Exploratories. 341–346. Chagnon.-M. B. of Pages 10 8 ARTICLE IN PRESS N. A. S. J. Alaux. Floral morphological barriers (long. visual and olfactory signals. Walker. Elias (Eds. Biotic control over the functioning of ecosystems.. (2003). C. Why network analysis is often disconnected from community ecology: A critique and an ecologist’s guide. G.). However.. Buchmann. this would neglect the potential stabilising role of redundant species.

et al. Grime. T. & Abdelaziz. Land use intensification reduces functional redundancy and response diversity in plant communities. Science.. 1115–1118. L. V. (2005). (1955). E. Schmid.. T. Ø. N.. P. 153. O. Ecology Letters. L. Proceedings of The Royal Society B – Biological Sciences. & Kremen. Voigt.. Waser. L. Willmer.. Evolution and Systematics. 935–943. Perfectti. 195–208). J. (1999).. T. & Kremen. Basic and Applied Ecology. & Loreau. Global warming and the disruption of plant–pollinator interactions. H. Why are there so many species of herbivorous insects in tropical rainforests? Science.. C. Rosenfeld. Klein. (2009). S. Pollen nutritional content and digestibility for animals. (1999). 103. The interplay between nutrient balancing and toxin dilution in foraging by a generalist insect herbivore. P. 629–643. Menlo Park. 511–530. Klinkhamer. M. Linsenmair.... & Cane. Beierkuhnlein. J. 1459–1469. 597–602. D. Perrings (Eds. S... Dajoz. Nature. Weisser. H. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. 71. M. Fluctuation of animal populations and a measure of community stability. Hector. 323–330.. Energetics and pollination ecology... T. S. Annals of Botany. Bosch... J. Proceedings Of The Royal Society B-Biological Sciences. Oxford University Press. M... Hector. Petchey. The importance of niches for the maintenance of species diversity. Oikos. Daily partitioning of pollinators in an African Acacia community. Laliberté. e1. U. Stone. (2009). (2010). Klein / Basic and Applied Ecology xxx (2010) xxx–xxx 9 Finke. S. & Snyder. & Hamrick. G. J. & Jordano. (2008). C. C. 98. birds and Aphelandra acanthus.. J. T. C. A.. Size-specific interaction patterns and size matching in a plant–pollinator interaction web.. 13890–13895. 103. J. (2005). J. J. Bunker. Ecology. Klein. et al. Hättenschwiler. S. M. Niche partitioning increases resource exploitation by diverse communities. C. L. Plant Systematics and Evolution. M. E. Williams. Olesen. Tscharntke. Wells. 597–605. Y. (2003). Y. C.. & Steffan-Dewenter. Y. Functional group diversity of bee pollinators increases crop yield.. Greenleaf. Ecology Letters. 103. F. G. N.-M. Schmid.. S. 89. D. S. Fründ. E.. 275. Loreau. A. 461. Oikos. Metcalfe. (2009).. P..001 . Gómez. Tiunov.. (2001). Gardening in the desert changes bee communities and pollination network characteristics.. 62. (2008). R.. Harte. Bjerknes. I.... D. 222.. D. and human wellbeing – An ecological and economic perspective (pp. Naeem. W.. Integrating methods that investigate how complementarity influences ecosystem functioning. J. W. J. Inchausti. (2007). B. A. Floral convergence and pollinator sharing in two bee-pollinated tropical herbs.. M. C. Hollender. S. 1389–1393. E. (2008). Moeller.. Bascompte. & Zalat. Diemer.. & Scheu. Roldan-Serrano. Dunne. 191– 218. J. 76–86.. (2007). J. 440 doi:10. 313. Functional redundancy in ecology and conservation. Loreau. 64. P. N. Schemske.. Lázaro. Hegland. Janda. J. European Journal of Horticultural Science. Elberling. M.. A. 36. 321.. Advances in pollination ecology from tropical plantation crops. (2009). E. Basic and Applied Ecology (2010). M. 412. (2008). (2004). G. Floral diversity and the facilitation of pollination. Drozd. Levine. Nason. M. MacArthur. M. Science. Bengtsson.. Dimitrakopoulos. 263. Willmer. F. M. J. Windows of opportunity and the temporal structuring of foraging activity in a desert solitary bee. J. M. Pollinator diversity and specialization in relation to flower diversity. Biodiversity. & C. 184–195.. H. Loreau.. Nielsen. A... C. (2010). 1488–1490. C. (2002).. Meriguet. (2000). Sahley. et al. Pollinator diversity affects plant reproduction and recruitment: The tradeoffs of generalization.. Gilbert. Tylianakis. Plant diversity and productivity experiments in European grasslands.. G.. V... Muschala. S. D. J.. Potts.. 1481–1487. & van der Meijden.-M. Ecological Monographs. Biodiversity and litter decomposition in terrestrial ecosystems.. Basset. Annual Review of Ecology. Müller. A. (2006). 710–717. Caiza. (1996). Reward attractions of zucchini flowers (Cucurbita pepo L. S. 94. Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. 8. Stang. Catterall. No. Ecology Letters. B. 24. I. Scherber. E... P. Miller. & Raven. Ecology. Cunningham. H. A. A. P. (2007). & Thomson. doi:10. K. A.2010. Semida. Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. T.. Srinivasan. A. 208–221.. B. 804–808.. 671–682. Oecologia. Caldeira. 101. M. F. & Hector. Fernández.BAAE-50467. 254–257.baae.. 187–209. & Carriere. Ecology. Please cite this article in press as: Blüthgen. & Kremen. Oikos.. In S.. Novotny. 2283–2291. (2008).) to bumblebees (Bombus terrestris L. Science. M. A generalized pollination system in the tropics: Bats. A. 1123–1127. & Guerra-Sanz. M. 119. 10. A. J. A. Animal Behaviour. M. Memmott. 13. Craze. E. Extinction order and altered community structure rapidly disrupt ecosystem functioning. M. & HilleRisLambers.. & Mandelik. & Totland. C. How does climate warming affect plant–pollinator interactions? Ecology Letters. (2006). H. (1999). N. 4. 538–547. & Price. N.1016/j. Facilitative interactions among plants via shared pollinators. N. Stang. Stone. Hector. Hoehn. Ecological methodology. J. P. Roulston. Ecology. Sonoran Desert columnar cacti and the evolution of generalized pollination systems.. P. Hoehn. W. submitted for publication. J. & Blüthgen.-L. G... et al. J... Naeem. M. Bernays. PLoS Biology. W. Eisenhauer.). 3289–3301. 295–304. Holland.. 36. (2006). (2005). Krebs.. I.. H. 294. 88.. 286. Y. M.. D. 89.. (2002). A. Fleming. (2001). P.. Fontaine. N.. M. 1581–1590. A. A. (1981)... 85. Wild bees enhance honey bees’ pollination of hybrid sunflower. P. & Nee. 70. S.. 533–536. Science. Annals of Botany.). Larsen.. Waser. S. Nature. W. (1972). & Klein. J. (2010). Partitioning selection and complementarity in biodiversity experiments. 12. J. P. J. N. M. A. J. Understanding the role of species richness for crop pollination services. DeClerck. (2006). Heinrich. M.. A... 72–76.. Fischer.1038/nature09492 Singer. Gotlieb.. N. Blüthgen. J. (2001). ecosystem functioning. A. & Steffan-Dewenter. C. Kulfan. Journal of Ecology. Nature. 176. S. Ecology. J. California: Benjamin Cummings.. et al. M. Queiroz. Vizuete. Ecological Entomolology. N. D. Proceedings of the National Academy of Sciences of the United States of America. & Martinez.. H. Response of complex food webs to realistic extinction sequences. J.. J. M. C.. P.11. Temporal dynamics of a pollination network. of Pages 10 ARTICLE IN PRESS N.. 946–954. C. V. S. Ghazoul. 1573–1582. 156–162. Ecology. D. Bos. Biodiversity and ecosystem functioning: Current knowledge and future challenges. 23–28. I... P. F.

134.. R.. Morris.2010. Werner. N. N. (2003). Ohashi. Linsenmair. Weiner. B. K.-M.. A. M..08. Ability of bumblebees to discriminate differences in the shape of artificial flowers of Primula sieboldii (Primulaceae). Proceedings of the National Academy of Sciences of the United States of America.2010. Blüthgen. T. Tylianakis. P. Munoz-Ramirez. Waser. 522–531. C. N. (2006). (2005). W. (2007). Willmer.baae. & Jordano. (2007). Proceedings of the National Academy of Sciences of the United States of America. & K. (1983). A. & Real. L. ecosystem function. Annals of Botany. 1175–1182. doi:10. 670–672. Consequences of microclimate variation on insect pollinator visitation in two species of Chaetanthera (Asteraceae) in the central Chilean Andes.. & Ninomiya. G. H.11.. Oecologia.baae.. Vázquez. M. E. A. A. & Klein. Valone.-M. 8.-M. J. K. 89. T.006. 3047–3057. Pollen amino acids and flower specialisation in solitary bees. K. (2010). L. F. A. (2011). L.. (1999). T. Werner.BAAE-50467. S. Hilpert. 99.. A. Revista Chilena de Historia Natural. 476–487. (1979). 18–23. & Thomson.. 228–237. S.1016/j. Basic and Applied Ecology (2010).. Y. of Pages 10 10 ARTICLE IN PRESS N.. 455–468. N. Ecology Letters. Diversity. H. Land use intensity in grasslands: Changes in biodiversity. Thermal constraints on activity patterns in nectar-feeding insects. Linsenmair. C.. Science. Torres-Diaz. Ecology. Ecological Entomology. this issue. Klein / Basic and Applied Ecology xxx (2010) xxx–xxx Tilman. and stability of parasitoid–host interactions across a tropical habitat gradient.1016/j. M. Please cite this article in press as: Blüthgen. Plant diversity and ecosystem productivity: Theoretical considerations. Ohsawa.. P. & Barber.. Williams. Apidologie. doi:10. 455– 469. Biodiversity and ecological redundancy.. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. species composition and specialisation in flower-visitor networks. 80. D.001 . Ecology. Use of novel pollen species by specialist and generalist solitary bees (Hymenoptera: Megachilidae). M. 1088–1094. No. Arroyo. A. Interaction frequency as a surrogate for the total effect of animal mutualists on plants. C. Weiner. Yoshioka. E. 8. Konuma. 8. 94. Basic and Applied Ecology. D. & Blüthgen.. N. Walker. An empirical evaluation of the insurance hypothesis in diversity–stability models... M. Effective mutualism between sequentially flowering plant species. & Klein. & Loreau. A. (2008).. Lehman. T. N. (1992). C. C. 87. Yachi. 41. (1997). P. K.. 1857–1861.. Biological Conservation. & Blüthgen. M. 1463–1468.. N.. J.. Cavieres. M. 96. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. 281. N. Iwata. Tscharntke.