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unctional complementarity and specialisation: The role of biodiversityn plant–pollinator interactions

ico Blüthgena,∗, Alexandra-Maria Kleinb,c

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

eceived 8 February 2010; accepted 1 November 2010

bstract

Ecological niche breadth (specialisation) and niche differentiation (complementarity) play a key role for species coexistencend hence biodiversity. Some niche dimensions of a species represent ecosystem functions or services such as pollination (func-ional niche). When species differ in their contribution to some collective function (functional complementarity), this implieshat functions from several species are required for a high overall functional performance level. Applied to plant–pollinatornteractions, functional complementary suggests that a higher diversity of pollinators contributes to an increased pollinationuccess of the plants or, in turn, that a higher diversity of flowers may better sustain the consumers’ requirements. Complemen-arity can affect functioning at different scales: the collective functioning of the target community, a single species, an individualr 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 special-sation at the community scale. We propose several mechanisms that generate complementarity. From the consumers’ viewpoint,ifferences in flowering phenology and/or nutritional variation in floral resources (nectar, pollen) may explain a complemen-ary role of different flower species. From the plant’s viewpoint, temporal or environmental variation in the pollinator species’ctivities may contribute to complementary effects on pollination of plant communities. In addition, different species maylso pollinate either more exposed or more sheltered flowers from the same plant individual, or vary in their functions withiningle flowers. So far, empirical evidence for complementary effects in general, and particularly mechanistic explanations ofuch effects are scant and will require comparative investigations at multiple scales in the future. Such studies will help us tonderstand if and how biodiversity maintains the quality and quantity of plant–pollinator functional relationships.

usammenfassung

Nischendifferenzierung (Komplementarität) und ökologische Nischenbreite (Spezialisierung) spielen eine Schlüsselrollen der Koexistenz von Arten und demzufolge für die Biodiversität. Einige Nischendimensionen von Arten bilden Ökosys-emfunktionen (funktionale Nische) wie z.B. Bestäubung. Wenn Arten sich in ihrem funktionellen Beitrag unterscheiden

dass artenreiche Gemeinschaften insgesamt leistungsfähiger als
funktionale Komplementarität), lässt das darauf schließen,
Please cite this article in press as: Blüthgen, N., & Klein, A.-M. Functional complementarity and specialisation: The role of biodiversityin plant–pollinator interactions. Basic and Applied Ecology (2010), doi:10.1016/j.baae.2010.11.001

rtenarme Gemeinschaften sind.Bezogen auf die Interaktionen von Blüten und Bestäubern impliziert funktionale Komplementarität, dass eine größere

rtenvielfalt 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: [email protected] (N. Blüthgen).

439-1791/$ – see front matter © 2010 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.oi:10.1016/j.baae.2010.11.001

dx.doi.org/10.1016/j.baae.2010.11.001

dx.doi.org/10.1016/j.baae.2010.11.001

mailto:[email protected]

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esser die Ansprüche der Bestäuberarten deckt. Komplementarität kann bei unterschiedlichen Skalen ansetzen und die kollektiveunktion der Gemeinschaft beeinflussen, die Funktion einer einzigen Art, eines Individuums oder sogar nur eines Teils einesndividuums, z.B. einer einzelnen Blüte.

Neuere Netzwerkanalysen zeigen eine stark ausgeprägte Komplementarität der Interaktionen zwischen Pflanzen- und Bestäu-erarten auf Gemeinschaftsniveau. Wir fassen unterschiedliche Mechanismen zusammen, die Komplementarität hervorbringen.us der Sicht des Konsumenten können Unterschiede in der Phänologie oder Unterschiede in den Nährstoffressourcen derlüten (z.B. Nektar, Pollen) eine komplementäre Rolle mehrerer Pflanzenarten erklären. Aus der Sicht der Pflanze könneneitliche oder wetterbedingte Aktivitätsunterschiede der Bestäuberarten zu komplementären Effekte bei der Bestäubung beitra-en. Außerdem können verschiedene Tierarten unterschiedlich räumlich verteilte Blüten eines Pflanzenindividuums bestäubender sich die Funktion innerhalb einer Blüte aufteilen.

Bis heute sind empirische Nachweise komplementärer Effekte und mechanistische Erklärungen für solche Effekte sel-en untersucht worden. Zukünftige vergleichende Untersuchungen zu Komplementaritätseffekten sollten verschiedene Skalenerücksichtigen. Solche Studien können zum Verständnis beitragen, ob und wie Artenvielfalt die Qualität und Quantität derunktionellen Beziehungen zwischen Blüten und Bestäubern fördert.

2010 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

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eywords: Complementary specialisation; Ecological networks;ollination; Redundancy

he concept of functional complementarity

Differentiation of ecological niches is known to pro-ote biodiversity: when multiple species are specialised

nd differ in their niche (niche complementarity), interspe-ific competition is reduced, facilitating their co-existenceMacArthur 1955; Elton 1958; Levine & HilleRisLambers009). Whereas the ecological niche concept includes var-ous abiotic and biotic factors in multidimensional space,everal niche dimensions represent important biotic pro-esses and thus ecosystem functions, emphasised in the termsfunctional niche’ and ‘functional (niche) complementarity’Loreau et al. 2001; Rosenfeld 2002). Functional redundancyn a community implies that species are mutually substi-utable in terms of an ecological function. For instance, theuantitative reproductive fitness of a plant may be equallyigh no matter if pollinated by a single pollinator species A,or C or by all of them together – in this case A, B, and C

re redundant regarding this particular function. Functionalomplementarity suggests the opposite: A, B, and C togetherontribute more to the function than any of them alone – airect and positive effect of biodiversity on ecosystem func-ioning (Loreau et al. 2001; Petchey 2003; Finke & Snyder008). Specialisation and complementarity are related: com-lementarity requires a certain degree of specialisation ofach species, while high generalisation is associated withigh niche overlap and thus redundancy. In addition, redun-ancy can also occur if species are specialised on the sameunction (Fig. 1).

Both complementarity and ecosystem functioning mayccur at multiple scales, from individuals via species to entireunctional groups. Our paper will focus on complementar-

Please cite this article in press as: Blüthgen, N., & Klein, A.-M. Functioin plant–pollinator interactions. Basic and Applied Ecology (2010), doi:

ty between species in the context of species diversity, andxplore its functional consequences on different scales (indi-iduals, species, and communities). The aim of this paper isa) to conceptualise various mechanisms of complementar-

ts

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gical niche; Ecosystem functioning; H2′; Mutualism; Nutrition;

ty in flower–pollinator relationships and (b) to briefly sketchhe functional consequences. Several mechanisms and effectsre still speculative, thus we will also highlight some impor-ant gaps in our understanding of complementarity. Beforerawing attention to plant–pollinator interactions, we synthe-ise some general points about functional complementarityts importance in the biodiversity–functioning relationship.

unctional consequences

As a consequence of functional complementary, the over-ll functional performance f of two species A and B together,(A + B), should be larger than the performance of eachpecies in isolation, so that

(A + B) > f (A) ∧ f (A + B) > f (B).

Hence, the proposed overall functional effect is an exam-le of synergism. In extreme cases, the participation of bothpecies may be essential for an ecosystem function – when

is unable to perform the function without B being present,.e. f(n1 · A + 0 · B) = 0, where n1 = number of individuals ofpecies A. The equation above not only represents an effectf niche complementarity, it also represents a prediction ofcological facilitation between A and B (examples for facil-tation are given below). Effects of species complementarityhould also be distinguished from a ‘sampling’ or ‘selec-ion’ effect: does the density of a particular effective species,.g. a highly productive plant, increase with species rich-ess (Tilman, Lehman, & Thomson 1997; Loreau & Hector001)? When such effective species occurs in a density simi-ar to that of all species together in a diverse community, will

nal complementarity and specialisation: The role of biodiversity10.1016/j.baae.2010.11.001

he functional performance of this particular species aloneuffice to explain the functional effect size?

Hence, demonstrating a causal effect of complementar-ty 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 iftheir functional niches overlap, either when they are both generalised, one is specialised on a subset of the other’s niche (‘nested’), or both arespecialised on the same function. Redundancy may improve the stability of a community, but also enhance interspecific competition when thetarget function represents a limited resource. Complementarity describes that species are functionally different, which requires that niches arer a certav ith bio

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elatively narrow. Certain functional performances then depend onulnerable to species losses, and the overall functioning increases w

ecessarily be inferred from nor be fully understood by atatistical correlation between species diversity and the totalagnitude of a function. It is important to test whether the

ncreased functioning is not just due to confounding effectsf overall higher density (Hoehn, Tscharntke, Tylianakis, &teffan-Dewenter 2008). Hence, we can ask whether there issignificant benefit from the activity of different species thatxceeds the effect of just adding more individuals of the samepecies. Specifically, functional complementary may requirehat the overall functional performance f of two species A and

together is larger than those of each of the species alone athe same density, so that

(n1 · A + n2 · B) > f ((n1 + n2) · A) ∧ f (n1 · A + n2 · B)

> f ((n1 + n2) · B),

here n1 and n2 represent numbers of individuals or activityensities.

However, while this condition may be useful for detect-ng complementarity, it likely underestimates the importancef biodiversity for functioning. Because interspecific com-etition is usually lower than intraspecific competition, theverall density n1 + n2 for two coexisting species A and Bay reach a higher level than a single species. A higher

verall density is likely to translate into a higher overall


unctional performance. Moreover, the functional niche itselfften represents a limited resource among which animals orlants compete. For instance, obligate nectar consumers And B may be specialised to be active at different times of

ossd

in species (species A or B) and the system may therefore be morediversity.

he day, and given their temporal niche constraints, none ofhe species alone may reach a population density as high asheir combined activity (n1 + n2). Such competitive avoid-nce would enhance the importance of complementarity forunctioning. This effect of reduced interspecific competitions most evident when overall biomass production (e.g. plantroductivity, see below) is the target functioning.

In the functional context, the niche → biodiversity rela-ionship can be reversed to a biodiversity → (functional)iche hypothesis (Fig. 1). Is a single species sufficient, orre multiple species necessary to sustain the functional per-ormance associated with a certain niche dimension? Overallunctioning increases with the number of contributing specieshen their complementarity is pronounced (Fig. 2). When

pecies differ entirely in their functional niche (strongestomplementarity), a linear increase of the overall level ofunctioning with biodiversity is expected (Fig. 2B). In acenario of no complementarity, species are completelyedundant, and adding more species would not necessar-ly improve the functionality (Fig. 2). An intermediate levellong the redundancy – complementarity continuum wouldredict a saturating relationship (Fig. 2) (Gómez, Bosch,erfectti, Fernández, & Abdelaziz 2007). A smooth saturat-

ng curve (like the one illustrated in Fig. 2) may be predictedy theory, but may apply only to a scenario where niche


verlaps among all species are the same, or when it repre-ents an average scenario for randomly adding or removingpecies along the biodiversity axis multiple times. However,epending on the specific contribution of each species that

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Fig. 2. (A) Niche complementarity in multispecies interactions, dis-played as a matrix with pollinator species as rows, plant speciesas columns and realised interactions as grey cells. Complemen-tary specialisation increases from left to right. (B) The shape ofthe biodiversity–functioning relationship depends on the extent offunctional complementarity (redundant, intermediate or comple-mentary). (C) Parallel to an improved functioning on the communityss

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cale, the diversity of the receiver may increase with a higher diver-ity of the transmitter of the function.

s added or lost (extinction order), the shape of an empiricaliodiversity–functioning relationship may vary. Some stud-es suggest a higher robustness of ecosystem functioning toiodiversity losses (Srinivasan, Dunne, Harte, & Martinez007), whereas a study that covered both pollination andung decomposition found evidence for accelerating ratherhan saturating functions with higher biodiversity (Larsen,

illiams, & Kremen 2005).

ommunity-scale functioning

Ecosystem functioning is often defined as the collectiveerformance of an entire community and not only the effectn a single target species. When each of three pollinatorpecies A, B, and C is fundamentally specialised on a dif-erent plant species X, Y, and Z, respectively, the overallollination function for the plant community (comprising X,, and Z) may be highest when all pollinator species areresent. Pollination success may then be lower for commu-ities with a reduced set of pollinator species, for examplenly X will be pollinated, if only A is present. Here, theunctional target needs to be carefully defined. When a mono-ulture of X occurs in the same density as a polycultureomprising X, Y and Z, and A in the same density as A,


, and C together, the community-wide seed set per areaay be similar in the monoculture of X with A than in the

olyculture. However, if polycultures have a higher perfor-ance for other reasons (e.g. differentiation in other niche

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PRESSlied Ecology xxx (2010) xxx–xxx

imensions), or if the maintenance of biodiversity is a partf the functional target (e.g. reproductive success of as manypecies as possible; Fontaine, Dajoz, Meriguet, & Loreau006), total functioning in polycultures is higher than inonocultures. In this case, the degree of interaction parti-

ioning between species (see next section) will be a predictorf the biodiversity–functioning relationship.

Such community-scale views are particularly commonn studies of nutrient cycling, e.g. leaf litter degradationHättenschwiler, Tiunov, & Scheu 2005). Moreover, mea-ures of plant productivity have served as the most intensivelytudied community example for community functioning. Theverall productivity of a plant community increases with theiversity of plants in grasslands, suggesting some extent ofiche complementarity among the species involved (Hectort al. 1999). Various ecosystem functions performed byne guild represent a limited resource for another guild. Inhis way, one trophic level may have a functional contribu-ion to another trophic level. Ecosystem functions providedo higher trophic levels include nutrition for parasitoid,erbivore, flower visitor or frugivore guilds; correspond-ng functions to the lower trophic levels include protectiongainst enemies, herbivory, pollination or seed dispersal.ue to species complementarity, more food plant species

ogether harbour a higher diversity of herbivores (Novotnyt al. 2006), more hosts a higher diversity of parasitoidsTylianakis, Tscharntke, & Klein 2006), and more floweringlant species a higher diversity of flower visitors (Ebeling,lein, Schumacher, Weisser, & Tscharntke, 2008). For obli-ate mutualisms, this implies a positive feedback betweeniodiversity of both parties: more pollinator species areequired to effectively pollinate the entire plant community,nd more flower species are required to nourish a higher diver-ity of consumers. It has been confirmed that the combinedctivity of different pollinator species increases the overalluccess of a small experimental plant community (Fontainet al. 2006). Again, such positive biodiversity relationshipsould be expected only for functional associations with high

omplementarity (Fig. 2C).Broadening the perspective from a single functional niche

imension to multidimensional niche space, it is importanto consider that redundancy in one niche dimension may bessociated with complementarity in another (Loreau et al.001; Rosenfeld 2002). Moreover, redundancy under certainnvironmental conditions may not hold for other circum-tances or under variable regimes and environmental impacts.n fact, the insurance hypothesis (Yachi & Loreau 1999;oreau et al. 2001; Valone & Barber 2008) implies hidden

ong-term complementarity behind an apparent redundancy:hen pollinator A becomes unreliable (e.g. due to populationeclines following unfavourable weather conditions), speciesmay compensate for the loss of functions performed by A.


uch compensatory effects may be particularly pronouncedhen responses to stress and environmental changes (i.e.ther niche dimensions) differ between A and B. This is ade-uately described by the term ‘response diversity’ (Elmqvist

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t al. 2003; Laliberté et al. 2010). Consequently, systems withunctional redundancy plus response diversity may be moreesilient against population fluctuations of associated speciesor months or years, or even longer time periods followingocal extinction.

etecting complementarity patterns incological networks

Several quantitative niche overlap metrics (Krebs 1999)ay be suited to characterise the degree of complementarity

etween species. In addition, species interaction networksepresent functional links between species and may be usedor inference about species complementarity. Each ‘link’ innetwork represents all of the interactions between a pair of

pecies, e.g. between pollinator species A and plant species X.ig. 2A displays networks in a matrix format. Links are ofteneighted by the number of interactions recorded. However,rawing inferences on specialisation and complementarityrom raw data of a network can be problematic given thatumber of observations per species is unequal (Blüthgen010). Using a method that accounts for unequal observationsn a network, complementary specialisation can be charac-erised by the metrics di

′ for each species and H2′ for the

ntire network (Blüthgen, Fründ, Vázquez, & Menzel 2008).ach di

′ and the overall H2′ increase (in the same way as

he matrices illustrated in Fig. 2A) from 0.0 (highest redun-ancy) to 1.0 (highest complementarity possible). As statedbove, high complementarity presupposes high specialisa-ion (see Finke & Snyder 2008); thus di

′ and H2′ also express

pecialisation, but are conservative for cases where speciesre specialised on a commonly utilised niche (see Blüthgen010).

When these indices are applied to different systems,arge variation in the extent of complementarity is found.lant–pollinator interactions often show a high level of com-lementarity, while plant-seed disperser associations have aignificantly lower H2

′ (Blüthgen, Menzel, Hovestadt, Fiala,Blüthgen 2007). Complementarity (H2

′) of flower visitsven on a single day is pronounced and relatively consistentcross meadows irrespective of their management (Weiner,erner, Linsenmair, & Blüthgen 2011). High complemen-

arity suggests that plant biodiversity may be important toustain the flower visitor diversity and vice versa. Thisay explain both why biodiversity of both trophic levels

howed a parallel decline over the last decades (Biesmeijert al. 2006), and that diversity of pollinators increases withower diversity (Fründ, Linsenmair, & Blüthgen 2010). The

ncrease in pollinator abundance and richness in habitatsith higher flower diversity is particularly pronounced in


hose taxa that exhibit a high degree of specialisation (bees,utterflies), whereas less specialised taxa (dipterans) poorlyespond to flower diversity (Weiner et al. 2011). Correspond-ngly, in desert habitats where interactions between plants

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PRESSlied Ecology xxx (2010) xxx–xxx 5

nd bees show a high complementarity (H2′), bee species

bundance and richness showed a stronger response to flowerpecies richness than in garden habitats where H2

′ was lowerGotlieb, Hollender, & Mandelik submitted for publication).

However, before inferring functional complementarityrom network data, several precautions should be consid-red. (1) Observed links may not always reflect the functionnder consideration, as in the case of unrewarding flowerisits or visits that do not result in a pollination event. Differ-nt links vary in quantitative functional importance. Whereashe interaction frequency of pollinators often reflects theirontribution to pollination of a plant (Vázquez, Morris, &ordano 2005), this may not hold for every context, everylant species, and every link. (2) An interaction networkummarises the observed interactions in the communityontext–related to the realised niche rather than fundamen-al niche. A single network may therefore underestimate theotential redundancy and dynamics of the system, but alsoail to depict more subtle complementarity at the link scale,.g. when different resources are involved in different links.rogress in understanding flower–pollinator networks thusepends on linking the visitation patterns to functional vari-tion between links and their spatio-temporal dynamics. (3)ince sampling effort is always limited in empirical datasets,

he full range of plant species visited by a pollinator (and viceersa) may simply be undetected. Consequently, specialisa-ion may be overestimated and complementarity erroneouslynferred when using uncorrected metrics (Blüthgen 2010).

Below we will highlight some possible mechanisms thatay explain complementary effects of different partner

pecies on the population of a target species, separately foronsumers (Fig. 3B and C) and plants (Fig. 3D–F) as targets.

echanisms at the animal species scale: theonsumers’ viewpoint

henological complementarity

Flower-visiting species often utilise different plant speciesuring the season or at different times of the day (Fig. 3B).hen their activity period exceeds the blooming period of a

lant species, the availability of other plant species couldecome essential to “bridge” the temporal gaps in nour-shment of the animal’s population (Baker 1963). If thispecies is a crucial pollinator, this scenario would represent aase of facilitation among plants, as the late flowering plantpecies would benefit from the presence of an earlier flower-ng species and vice versa (Heinrich & Raven 1972; Waser

Real 1979; Moeller 2004). This effect may be widespread,ince blooming periods of plant species are often relatively


imited, and seasonality pronounced, while social bees andany other pollinators are active for several months (e.g.lesen, Bascompte, Elberling, & Jordano 2008). Temporalartitioning in flowering may even occur in the course of the

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Fig. 3. Complementarity conceptualized at different scales andmechanisms of plant–pollinator interactions, including the parti-tioning of interactions in the community, effects on the pollinatorspecies, and effects on the plant species. The partitioning of api-cb(

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al versus basal stigmata pollination within a strawberry flower (F)etween larger and smaller bee species was shown by Chagnon et al.1993).

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

utritional complementarity

Several flower-visiting species consume both pollen andectar (Fig. 3C). Whereas nectar is mainly composed of aarbohydrate solution and contains relatively low amountsf amino acids among some other nutrients (Baker & Baker983), pollen is much richer in proteins, and also contains freemino acids, lipids, starch, sterols, and vitamins (Roulston

Cane 2000). However, surprisingly little is known aboutinerals and other trace elements in pollen and nectar. In

ees, nectar is primarily used as an energy source for adults,hereas pollen is provisioned for growing larvae as theirajor protein source. Hence, bees and many other animals

eed to forage for both nectar and pollen. Both resources


ay be sometimes obtained from the same flower, but ofteneed to be collected from two or more different plant speciesffering either nectar or pollen as the main reward – a casef complementary nutrition. Like phenological complemen-

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arity, when plant species X and Y provide complementaryesources such as pollen versus nectar, X may facilitateollination of Y and vice versa (Ghazoul 2006). This facil-tative mechanisms, based on complementary flower traits,

ay thus add to a more commonly predicted effect based onverlapping traits: different plant species enhance the over-ll floral display and generalist pollinator attraction, whicheems likely for plant species with visually similar flowersSchemske 1981; Moeller 2004; Ghazoul 2006).

Since pollen from different plants varies in nutrient com-osition as well as nectar sources, a dietary mix containingifferent plant species could be more nutritious than pollenr nectar from a single plant species. Some generalist her-ivores may obtain a more balanced diet by feeding onifferent plant species (Behmer 2009). It has been rarelytudied in generalised pollinators, and is best known foroneybees: while honeybee larvae grow well on a mixediet of different pollen species, pure dandelion pollen isnsufficient (see Roulston & Cane 2000). The addition ofryptophane which is missing or occurs in minute quanti-ies in this pollen solves this problem (Roulston & Cane000), so the deficiency in this essential amino acid is a casehere complementary nutrition is required. In several pollen

pecies, tryptophane and methionine occur in small quanti-ies (Weiner, Hilpert, Werner, Linsenmair, & Blüthgen 2010).uch deficient resources are possible candidates where com-lementary nutrition may enhance the nutrient balance forhe consumer. Moreover, diet mixing may help to avoid highoncentrations of toxic compounds in herbivores (Singer,ernays, & Carriere 2002), which is plausible but has notet been demonstrated for flower visitors. Feeding bee larvaeith mixed pollen diets indirectly suggests that toxin dilu-

ion may occur (Williams 2003), but mechanisms are yet toe shown. Toxins occur in pollen (Roulston & Cane 2000) asell as nectar (Adler 2000). Hence, positive effects of mixedollen and/or nectar diets may provide indirect evidence forither nutritional complementarity or toxin dilution. In addi-ion, mixed pollen diets were recently shown to have positiveffects on the immunocompetence of honeybees comparedo monospecific diets (Alaux, Ducloz, Crauser, & Le Conte010), although mechanisms are unresolved and require fur-her investigations.

echanisms at the plant species scale: thelants’ viewpoint

emporal or environmental complementarity

Whereas variation in phenology between plant speciesould affect flower visitors, see above (Fig. 3B), temporal


omplementarity of pollinators may be important for plantsFig. 3D). Seasonal complementarity can play a role forlants that flower over longer periods, and inter-annual vari-tion for perennial plants when pollinators fluctuate between

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ears. Complementarity may occur when different pollinatorpecies of a target plant forage at different times of the dayHoehn et al. 2008) or due to the distinction between diurnalnd nocturnal pollinators (Dar, Arizmendi, & Valiente 2006;uschala, Caiza, Vizuete & Thomson 2008). For exam-

le, a study of columnar cacti (Fleming, Sahley, Holland,ason, & Hamrick 2001) compared the reproductive suc-

ess of plant individuals that were either (O) continuouslypen to any pollinator, (D) only open to diurnal pollinators,r (N) open only to nocturnal pollinators, based on a tem-oral exclusion experiment. In one of four species studied,he authors demonstrated a significant temporal complemen-arity, defined as a higher fruit set in control cacti [fruit setO) > fruit set (D) + fruit set (N)]. The authors also predictedhat pollinator complementarity may be more pronounced inlant species whose reproductive success is pollen limited,hile redundancy may be common in resource limited plant

pecies.It is expected that systems with strong temporal com-

lementarity are vulnerable to climate warming whenhenologies are changed, but changes differ between flow-rs and their visitors, causing phenological mismatchesMemmott, Craze, Waser, & Price 2007Hegland, Nielsen,ázaro, Bjerknes, & Totland 2009). Although flower phenol-gy has been examined under different climatic conditionse.g. Dunne, Harte, & Taylor 2003), studies that examined theunctional role of interactions between pollinator and plantpecies in changing climatic conditions are missing (Heglandt al. 2009).

Temporal complementarity (seasonal, daytime) is oftenegular and predictable, with pollinators being adapted topecific foraging activity periods (e.g. Stone et al. 1999).elated to such temporal niche differentiation is the idea

hat pollinators may vary in their response to site-specificeather conditions (Torres-Diaz, Cavieres, Munoz-Ramirez,K. Arroyo 2007), particularly thermal constraints (Willmer

983). Fluctuations in environmental conditions such ashanges in temperature, moisture or wind velocity can dis-urb some species in their foraging activity, but not othershich continue to forage. Hence, a complementarity basedn variable pollinator responses to climatic conditions mightepresent a potential buffer against climate change for gener-lised plants (Hegland et al. 2009). Variation in responses tonvironmental conditions of otherwise functionally ‘redun-ant’ species is the conceptual basis of ‘response diversity’Elmqvist et al. 2003, see Community-scale functioningbove) and represents an ‘environmental complementarity’Fig. 3D) in the context of our paper.

rchitectural complementarity


Complementary effects may also occur within plant indi-iduals or even within a single flower. Hoehn et al. (2008)ecently showed that certain bee species tend to forage atround flowers, whereas other bee species preferred higher

ap


owers on climbing pumpkin plant individuals. Such species-pecific preferences for flowers at single plant individualsepresent a response to different micro-climatic conditions,or example, when lower flowers are more shaded than highernd more exposed flowers. Similarly, the pollinator commu-ity might be distinct at inner and outer regions of a treeanopy. In addition, the flower location on a plant may bessociated with differences in flower shape or nectar con-entration. Bumblebees, for example, respond to differencesn flower shape (artificial flowers; Yoshioka et al. 2007) andectar concentrations (zucchini flowers, where it translatesnto seed set; Roldan-Serrano & Guerra-Sanz 2005).

Architectural complementarity within plant individualsFig. 3E) thus represents a promising topic for future research,otentially explaining why pollinator diversity enhancesollination of certain plants. The different scales of comple-entarity could be linked: for plant individuals with extended

looming periods, temporal complementarity of differentollinators may also affect reproductive success at the plantndividual scale, which may also be important for individualowers if they are long-lived.Complementarity among flower visitors to promote polli-

ation within a single flower (Fig. 3F) was described in anggregate strawberry fruit (Chagnon, Ingras, & de Oliveira993). Here, small bees mainly pollinated the basal stigmas,hereas larger bees such as honeybees pollinated the apical

tigmas of a flower. Pollination success was optimal onlyhen strawberry flowers were pollinated by both groups.similar pattern was observed in pumpkin flowers (Hoehn

t al. 2008). Again, small bees of the family Halictidae andndrenidae foraged mainly at the base of a single, large

tigma, whereas honeybees often foraged at the apical partr at the whole stigma. The behavioural differences in visita-ion at the flower scale remain to be studied. The relevance forlant species with an aggregate fruit such as the strawberrys clear: only when many stigmas per flower get pollinated,he fruit will be well shaped. For plant species with a sin-le stigma per flower, such as pumpkin, the relevance is lesslear, but possible mechanisms for a biodiversity-functioningelationship may include that (1) one flower-visiting speciesA) transfers pollen to a flower, whereas another species (B)s needed to place the pollen at the right place on the stigma or2) that A is only an effective pollinator when B is present, forxample, because the activity of B forces A to switch moreften between plant individuals to facilitate cross pollinationGreenleaf & Kremen 2006). Functional complementarityay explain why the seed set of coffee increases with the

iversity of pollinator species (Klein, Cunningham, Bos, &teffan-Dewenter 2008).

onclusions


Complementary specialisation of plant–pollinator inter-ctions is pronounced at the community scale: differentollinator species utilise and pollinate different plant species.

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ptfiattictgunonii

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his has been confirmed by quantitative network analyses.esponsible mechanisms for the high degree of species par-

itioning include flower morphology, visual and olfactoryignals, and temporal variation among other factors. Floralorphological barriers (long, narrow tubes that are inacces-

ible to visitors that are too large or have a short proboscis)re particularly important in this regard (Stang, Klinkhamer,aser, Stang, & van der Meijden 2009). Pollinators dif-

er in their abilities to access a flower, which provides anxplanation for the experimental evidence that bumblebeeslus syrphids together contribute to a higher reproductiveuccess of a plant community than either of the pollinatoraxa alone (Fontaine et al. 2006). Due to functional com-lementarity, overall ecosystem functioning thus increasesith biodiversity, a phenomenon that is widespread in sev-

ral systems (Loreau et al. 2001; Balvanera et al. 2006)nd across functions (Scherber et al. 2010). Compared toffects on the community scale, more subtle complementar-ty effects and less obvious traits on the species or individualcale are much less understood. For a flower visitor popu-ation, different plant species may provide food at differentimes (phenological complementarity) or different nutrientsresource complementarity). For a plant population, differ-nt pollinator species may complement each other due toifferences in temporal activities (temporal complementar-ty). In addition, different species may serve different flowersr parts of a flower of a plant individual (spatial comple-entarity), and interactions among species may facilitate the

verall functioning (Hoehn et al. 2008; Klein, Müller, Hoehn,Kremen 2009).It has thus been suggested that conservation should

rioritise species with complementary functions, while func-ionally redundant species could be of lower importance, therst ones acting as “drivers”, the latter as “passengers” ofn ecosystem (Walker 1992). However, this would neglecthe potential stabilising role of redundant species, e.g. whenhey differ in responses to disturbance or other changesn environmental conditions. The concept of environmentalomplementarity outlined above includes such complemen-ary roles of otherwise functionally similar species. Ineneral, species that appear similar in their ecosystem effectsnder particular conditions (e.g. in a short-term study) may beo longer redundant over longer time spans and a wider rangef conditions (Chapin et al. 1997). Understanding the mecha-isms and consequences of complementarity and redundancys thus crucial to predict impacts of biodiversity on function-ng in changing environmental conditions.

cknowledgements

Research projects of NB are funded by the Deutsche


orschungsgemeinschaft (DFG: Biodiversity Exploratories,FB 554 and BL 960/1-1), those of AMK by the Alexanderon Humboldt Foundation and DFG Biodiversity Explorato-ies KL 1849/3-1, KL 1849/4-1 and of the Jena Experiment

E


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

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