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a: Non-flowering L. conocarpodendron (left) and M. fimbriifolius (right) are difficult to distinguish even when growing side-by-side, as they do here on Red Hill, Cape Peninsula. b: L. conocarpodendron inflorescence. c: M. fimbriifolius inflorescence.
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Interactions among plant species via pollinators vary from competitive to mutualistic and can influence the probability of stable coexistence of plant species. We aimed to determine the nature of the interaction via flower visitors between Leucospermum conocarpodendron and Mimetes fimbriifolius , two shrubs in the Proteaceae that share many ecologi...
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... this background in mind, we studied the pollination biology of two very similar Proteaceae shrub species that typically co-occur in Fynbos communities on the Cape Penin- sula, South Africa (Fig. 1). Leucospermum conocarpodendron and Mimetes fimbriifolius share many vegetative features, mode of seed dispersal and fire regeneration strategy, but their polli- nation biology has not previously been studied ( Midgley et al. 1998). We combined nectar analysis, differential pollinator exclusion experiments, pollinator observations and ...
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... and have small ranges, with M. fimbriifolius confined to the Cape Peninsula and L. conocar- podendron extending slightly beyond. An earlier study of these two prominent species exemplified them as ecological equivalents (Midgley et al. 1998). They occur interspersed and are so similar that they are difficult to distinguish when not flowering (Fig. 1). Their leaves are broad, sclerophyllous, hairy and tipped with extra-floral nectaries (Zachariades & Midgley 1999). Both are unusual in that their aboveground parts generally survive fires and sprout new growth from buds protected under thick bark ( Midgley et al. 1998). This strategy gives them the height advantage over the other ...
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... flowers of the two species share many traits, such as large size, but there are also key differences. L. conocarpo- dendron inflorescences possess ~60 flowers with bright yel- low, incurved styles that act as pollen presenters (Fig. 1b). M. fimbriifolius inflorescences (alternatively, conflorescences) are composed of separate headlets in multiple whorls. Each headlet consists of four to seven flowers with long, straight pollen presenters and enclosed in a tube formed by bracts (Fig. 1c). The adaxial bract is pink and typically extends beyond the pollen presenters to ...
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... possess ~60 flowers with bright yel- low, incurved styles that act as pollen presenters (Fig. 1b). M. fimbriifolius inflorescences (alternatively, conflorescences) are composed of separate headlets in multiple whorls. Each headlet consists of four to seven flowers with long, straight pollen presenters and enclosed in a tube formed by bracts (Fig. 1c). The adaxial bract is pink and typically extends beyond the pollen presenters to form a hood. Although flowering overlaps broadly, M. fimbriifolius peaks earlier (September) than L. conocarpodendron (October), and M. fimbriifolius has a longer flowering window (May- February) than L. conocarpodendron (July-January; A. G. Rebelo, ...
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... number of pollinating Cape Sugarbird visits to L. conocarpodendron increased significantly with conspecific density, but the rate of increase was greatest at high densities of co-occurring M. fimbriifolius (significant positive interaction term; Table 3, Fig. 2a, Fig. S1). Similarly, Cape Sugarbird visits to M. fimbriifolius increased steeply with increasing conspecific density only in the presence of high densities of L. conocarpo- dendron (significant positive interaction term; Table 3, Fig. 2b, Fig. S2). Thus, for both plant species the number of visits by pollinating Cape Sugarbird is positively ...
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... In the Cape Floristic Region (CFR) of South Africa, nectar-feeding birds are important pollinators of flowering plants, especially for Proteaceae (Geerts, 2011). This dependence is highly asymmetric, with only six nectar-feeding bird species existing in this region, but approximately 70 species of Proteaceae, dependent on these nectar-feeding birds for reproduction (Geerts et al., 2020;Pauw & Johnson, 2018). Of the six nectar feeding birds in this region, four occur throughout, and of these, the Cape sugarbird Promerops cafer and orange-breasted sunbird Anthobaphes violaceae are endemic to this region. ...
Aim: Climate change influences species distribution in space and time, but predicting
the overlap in the range of interacting species under different climate scenarios
remains a challenge. Here, we explore how climate change influences shifts in species
ranges among mutualists.
Location: Cape Floristic Region (CFR), South Africa.
Taxon: Proteaceae and Passeriformes.
Methods: We used machine-learning
algorithms (random forest and boosted-regression
trees) and regression model (generalized additive models) to predict range
shifts of 11 bird-pollinated
Proteaceae species, combined occurrence prediction of
71 bird-pollinated
Proteaceae and their two most important, endemic, pollinator
bird species. We determined the degree of overlap in geographical ranges of nectar-feeding
birds and Proteaceae under different climate scenarios. Species ranges were
projected to the years 2050 and 2070 using representative concentration pathways
(RCP) 4.5 and 8.5 and three global climate models.
Results: The majority of Proteaceae species in our model are predicted to experience
range contractions, which ranged from 1% under 2050 RCP 4.5 CCSM4 to 79% under
2070 RCP 8.5 CNRM-CM5
climate scenarios, leading to 55% and 62% range loss for
Cape sugarbird and orange-breasted
sunbird, respectively, under extreme climate
scenarios. Proteaceae species are predicted to experience least overlap with nectar-feeding
birds in the northern and eastern range under future climate scenarios.
Main Conclusion: Climate change threatens species occupying the mountain range of
the northern limit and other regions of the CFR. Reduced range overlap of mutualists
may have significant implications for the reproduction and persistence of Proteaceae.
We suggest active monitoring of Proteaceae populations in regions where species are
predicted to lose their range, particularly so for threatened species with small ranges.
... Moreover, individual birds are able to carry a substantially greater load of conspecific pollen than insects (Collins & Rebelo, 1987). Accordingly, many Protea species have specialized in bird pollination in this biome (Hargreaves et al., 2004;Pauw & Johnson, 2018). ...
Combined studies of the communities and interaction networks of bird and insect pollinators are rare, especially along environmental gradients. Here, we determined how disturbance by fire and variation in sugar resources shape pollinator communities and interactions between plants and their pollinating insects and birds. We recorded insect and bird visits to 21 Protea species across 21 study sites and for 2 years in Fynbos ecosystems in the Western Cape, South Africa. We recorded morphological traits of all pollinator species (41 insect and nine bird species). For each site, we obtained estimates of the time since the last fire (range: 2-25 calendar years) and the Protea nectar sugar amount per hectare (range: 74-62 000 g/ha). We tested how post-fire age and sugar amount influence the total interaction frequency, species richness and functional diversity of pollinator communities, as well as pollinator specialization (the effective number of plant partners) and potential pollination services (pollination service index) of insects and birds. We found little variation in the total interaction frequency, species richness and functional diversity of insect and bird pollinator communities, but insect species richness increased with post-fire age. Pollinator specialization and potential pollination services of insects and birds varied differently along the environmental gradients. Bird pollinators visited fewer Protea species at sites with high sugar amount, while there was no such trend for insects. Potential pollination services of insect pollinators to Protea species decreased with increasing post-fire age and resource amounts, whereas potential pollination services of birds remained constant along the environmental gradients. Despite little changes in pollinator communities, our analyses reveal that insect and bird pollinators differ in their specialization on Protea species and show distinct responses to disturbance and resource gradients. Our comparative study of bird and insect pollinators demonstrates that birds may be able to provide more stable pollination services than insects. K E Y W O R D S Cape Floristic Region, community composition, plant-animal interactions, pollination networks, pollinator specialization 2 | NEU et al.
... Bees were frequent and numerous flower visitors yet contributed very little to S. brachypetala pollination, as evidenced by very low fruit and seed set in treatments in which birds but not bees were excluded (Fig. 2B,D,F). Some southern African birdadapted plants show an absence of seed production (Stokes & Yeaton, 1995) or reductions in fecundity following similar bird exclusion (Botes et al. 2009a;Hargreaves et al. 2010;Kiepiel & Johnson, 2014;Schmid et al. 2015;Pauw & Johnson, 2018); however, in other apparently bird-adapted species, bird exclusion has no impact on fecundity, indicating that bees contribute significantly to pollination (Hargreaves et al. 2008;Botes et al. 2009b;Wilson et al. 2009;Patrick et al. 2018). Bees likely negatively impact S. brachypetala fecundity through theft of floral resources (Wills et al. 1990;Horskins & Turner, 1999;Hargreaves et al. 2009;Wilson et al. 2009). ...
Bird pollination systems are diverse, ranging from narrow‐tubed flowers pollinated by specialist nectarivores such as hummingbirds and sunbirds, to relatively open flowers pollinated by opportunistic ( i.e . generalist) nectarivores. The role of opportunistic avian nectarivores as pollinators has historically been under‐appreciated. A key aspect to understanding the importance of opportunistic birds as pollinators is to investigate how efficiently they transfer pollen among flowers. Here, we document the pollination and breeding systems of Schotia brachypetala , a southern African tree known as the ‘weeping boer‐bean’ on account of its prolific production of dilute hexose‐dominated nectar. The cup‐shaped flowers of this tree attract a large number of bird species, including both opportunistic and specialist nectarivores.
We identified floral visitors using observations and camera traps and quantified the floral traits responsible for animal attraction. We documented the breeding system, used selective pollinator exclusion to test the contribution of birds to fecundity, and performed supplemental pollination to test for pollen limitation. Single‐visit pollen deposition trials were undertaken to determine the efficacy of bird pollinators.
Controlled hand‐pollination experiments showed that S . brachypetala is genetically self‐incompatible and therefore dependent on pollinators for seed production. Supplemental hand‐pollination experiments showed that natural fecundity is limited by either the amount and/or the quality of pollen on stigmas. Flowers from which birds but not insects were experimentally excluded set fewer seeds than open control flowers. Opportunistic birds deposited more pollen per visit than did specialist sunbirds.
We conclude that S . brachypetala has a generalized bird pollination system that mainly involves opportunistic nectarivores.
... To facilitate the interaction, bird-pollinated plants have evolved large, reddish flowers that secrete copious, dilute nectar, while nectar-feeding birds have evolved long, thin beaks and brush-tipped or tubular tongues for nectar extraction (Pauw, 2019). The interacting partners are linked in a positive feedback loop: when the abundance of nectar-producing plants increases, the abundance of nectar-feeding birds increases, which leads to enhanced seeds set and a further increase in plant abundance (Montgomerie and Gass, 1981;Anderson et al., 2011;Schmid et al., 2016b;Pauw and Johnson, 2018). The positive correlation between the abundances of these partners implies that by restoring the one, we might restore the other (Schmid et al., 2016a;Geerts et al., 2020). ...
... Pollinator exclusion experiments have shown that several species are strongly dependent on birds for seed production (e.g. Pauw, 1998; Schmid et al., 2015;Pauw and Johnson, 2018), and seeds are very important for population persistence because, in the majority of species, the adults are killed during a fire and cannot resprout (le Maitre and Midgley, 1992). The potential climate change related decrease in the inter-fire period (Batllori et al., 2013) enhances this dependence on seeds, and hence birds, because plants have less time to make the seeds needed to replace the adult population. ...
Pollinators are among the first to be lost when natural habitat is reduced to small patches and this can have cascading effects on multiple plant species. Simultaneously, the loss of natural habitat cuts people off from nature and, when people are out of touch with nature they do not care for biodiversity, resulting in further losses. Theoretically, the effects of habitat loss and fragmentation on pollinators can be mitigated by reconnecting isolated conservation areas with stepping stones and, if these are located in an urban matrix, they offer opportunities for people to reconnect with nature. Here we assess the effect of creating stepping stone habitats for nectar-feeding birds across Cape Town, South Africa. With the help of pupils, we planted gardens of indigenous, bird-pollinated plants at eight schools in the urbanized matrix between two conservation areas. To test for change in the bird community on school grounds we conducted 398 bird observation sessions over a seven-year period. Changes in attitudes and knowledge were assessed with questionnaires distributed to 176 pupils. We found that, as gardens matured, nectar availability increased and the probability of observing a Southern Double-collared Sunbird (Cinnyris chalybeus) on school grounds during a 30 min period increased from 10% to 50%. Bird species richness increased from ~5 to ~7 species. Questionnaire scores increased by 30% in participating pupils versus 8% in non-participating pupils. Although effects were small, the results suggest that it is possible to restore the bird-pollination mutualism in cities and in the process reconnect people with nature.
... among co-flowering communities) shifts in the density and diversity of co-flowering species may affect the direction of pollinator mediated plant-plant interactions (facilitation or competition). For instance, pollinator-mediated facilitation can be expected to be prevalent during dry seasons, where the number of species and/or flower densities are typically lower and thus pollinator attraction may be enhanced by the increase in the amount of floral resources that are simultaneously available to pollinators (Ghazoul, 2006;Moeller, 2004;Pauw & Johnson, 2018;Rathcke, 1983). However, the dominant interaction may switch from facilitative to competitive as the number of flowering species and/or floral density increases during the rainy season, as plants will start to compete for a limited pollinator pool (Fontaine, Collin, & Dajoz, 2008;Rathcke, 1983). ...
... It is also known that high floral trait similarity can enhance pollinator attraction leading to facilitative interactions in pollinator limited communities (e.g. Pauw & Johnson, 2018). ...
... Our findings are also consistent with studies of density-dependent pollinatormediated effects between plant species pairs, where the sign of the interaction depends on the abundance of the other species present (e.g. Ghazoul, 2006;McEwen & Vamosi, 2010;Pauw & Johnson, 2018;Rathcke, 1983Rathcke, , 1988. ...
Species' floral traits and flowering times are known to be the major drivers of pollinator‐mediated plant–plant interactions in diverse co‐flowering communities. However, their simultaneous role in mediating plant community assembly and plant–pollinator interactions is still poorly understood. Since not all species flower at the same time, inference of facilitative and competitive interactions based on floral trait distribution patterns should account for fine phenological structure (intensity of flowering overlap) within co‐flowering communities. Such an approach may also help reveal the simultaneous action of competitive and facilitative interactions in structuring co‐flowering communities.
Here we used modularity within a co‐flowering network context, as a novel approach to detect convergent and/or over‐dispersed patterns in floral trait distribution and pollinator sharing. Specifically, we evaluate differences in floral trait and pollinator distribution patterns within (high temporal flowering overlap) and among co‐flowering modules (low temporal flowering overlap). We further evaluate the consistency of observed floral trait and pollinator sharing distribution patterns across space (three geographical regions) and time (dry and rainy seasons).
We found that floral trait similarity was significantly higher in plant species within co‐flowering modules than in species among them. This suggests pollinator facilitation may lead to floral trait convergence, but only within co‐flowering modules. However, our results also revealed seasonal and spatial shifts in the underlying interactions (facilitation or competition) driving co‐flowering assembly, suggesting that the prevalent dominant interactions are not static.
Synthesis. Overall, we provide strong evidence showing that the use of flowering time and floral trait distribution alone may be insufficient to fully uncover the role of pollinator‐mediated interactions in community assembly. Integrating this information along with patterns of pollinator sharing will greatly help reveal the simultaneous action of facilitative and competitive pollinator‐mediated interactions in co‐flowering communities. The spatial and temporal variation in flowering and trait distribution patterns observed further emphasize the importance of adopting a more dynamic view of community assembly processes.
... Of the 330 Proteaceae species occurring in the CFR, approximately 25% are potentially pollinated by nectarfeeding birds, with the Cape Sugarbird a particularly important pollinator (Collins, 1983;Fraser, 1989;Fraser & McMahon, 1992;Martin & Mortimer, 1991;Mostert, Siegfried, & Louw, 1980;Pauw & Johnson, 2017;Skead, 1967). Despite Proteaceae being such an important component of the CFR vegetation, relatively few comprehensive pollination studies have been conducted on avian pollination in this family (Collins, 1983;Collins & Rebelo, 1987;Johnson, 2015;Schmid et al., 2015;Wright, Visser, Coetzee, & Giliomee, 1991). ...
... Proteaceae species that are visited by nectar-feeding birds have brush-type inflorescences with morphological adaptations for bird-pollination described in detail in Rebelo, Siegfried, and Crowe (1984). We based our list on the available Proteaceae pollination studies (Biccard & Midgley, 2009;Coetzee & Giliomee, 1985;Collins, 1983;Collins & Rebelo, 1987;Horn, 1962;Johnson, 2015;Lamont, 1985;Mostert et al., 1980;Pauw & Johnson, 2017;Pauw & Stanway, 2015;Schmid et al., 2015;Seiler & Rebelo, 1987;Whitehead, Giliomee, & Rebelo, 1987;Wiens et al., 1983;Wright, 1994;Wright et al., 1991) but with a number of species not assessed for bird-pollination, we subsequently selected species according to the following morphological criteria that are likely to indicate bird pollination (Rebelo, 2001): For the genera Mimetes and Protea, species that bore inflorescences >20 cm above ground level and have flower styles longer than 25 mm. For Leucospermum we considered species that bore inflorescences >20 cm above ground level and with styles longer than 35 mm as these larger flower heads are typically birdpollinated (Rebelo, 2001). ...
With the current global concerns about pollinators, relationships between species interactions and diversity are pivotal. If pollinator communities depend strongly on the diversity of flowering plants and vice versa, anthropogenic influences—whether positive or negative—on one partner will cause changes in the other. Here we ask whether nectarivorous bird communities are structured by resource abundance (Proteaceae nectar) or Proteaceae diversity at different spatial scales in the Cape fynbos of South Africa. On a small spatial scale, we sampled 34 one‐hectare plots across the Cape Floristic Region (CFR) for flowering Proteaceae species, number of inflorescences, nectar volume, vegetation age, nectar‐feeding bird abundance and species richness. At small scale, nectar—rather than vegetation structure or plant community composition—was the most strongly correlated to nectar‐feeding bird diversity and abundance. On a landscape scale we investigated the spatio‐temporal flowering patterns of ornithophilous Proteaceae throughout the CFR. Similar flowering patterns—with a winter floral abundance peak—were found throughout the region, but Protea , Leucospermum and Mimetes showed complementary flowering periods. At large spatial scales ornithophilous Proteaceae species richness is strongly correlated—more so than plant or floral abundance—to the nectar‐feeding bird community. At large spatial scales resource diversity—and at a smaller scale resource abundance, shapes nectar‐feeding bird communities. Providing high volumes of nectar sugar throughout the year is key to restore the nectar‐feeding bird communities in small conservation areas.
... Interestingly, pollinator-mediated facilitative interactions resulting from an increase in the number of co-flowering species have been observed when plant species share similar floral characteristics (e.g. Moeller 2004;Pauw & Johnson, 2018). However, the effects of an increase in floral trait diversity on aspects of the pollinator environment (i.e. ...
... For instance, facilitative effects on visitation rate have been commonly observed in studies of congeneric species that show ample similarity in floral traits (colour and/or morphology; e.g. Johnson et al., 2003;Moeller, 2004;Pauw & Johnson, 2018). In contrast, adverse effects have been observed in studies that have considered co-flowering communities with a much wider diversity of floral traits (e.g. ...
The number of co‐flowering species, floral density and floral trait diversity can be major determinants of pollinator‐mediated plant–plant interactions in a community. However, evaluation of how each one of these co‐flowering components affects the pollination success of a single focal plant species, and how these effects vary at different spatial scales, is lacking.
Here, we evaluated the effects of functional diversity (flower morphology and colour), taxonomic diversity (reflecting potential sampling effects) and flower density (conspecific and heterospecific), on the pollinator environment (i.e. visitation rate and pollinator diversity) and pollination success (i.e. pollen load size and number of pollen tubes per style) of Cakile edentula (Brassicaceae). We applied structural equation models (SEMs) at the floral‐neighbourhood (plot level) and community‐wide scales to uncover the factors that mediate co‐flowering community effects on C. edentula pollination success.
We found that co‐flowering community effects at the community level are more important than fine‐scale floral‐neighbourhood differences in mediating plant pollination success in our study species. Increasing plant functional diversity decreased pollinator visitation rate but increased the diversity of pollinator functional groups visiting C. edentula flowers. Taxonomic diversity negatively affected pollinator diversity suggesting that other unmeasured floral traits may be relevant or that single‐species effects (sampling effects) may be important. Overall, our results suggest that functional floral trait diversity in a community may be the most important factor influencing pollination success of species in a community. We also found evidence for intra‐ and interspecific pollinator competition mediated by flower density, but none of these effects seemed to have a significant impact on pollination success.
This study is an important step towards understanding the complexity of co‐flowering community effects on the pollination success of individual plant species at multiple spatial scales. This study further reveals the potential importance of plant functional diversity in a community in helping predict competitive and facilitative interactions in co‐flowering communities.
Synthesis. Floral density and taxonomic and functional co‐flowering diversity are important drivers of pollination success in flowering plants. The effects of the co‐flowering diversity on the pollination success of plant species can largely depend on the spatial scale being studied. Only evaluating the outcomes of pollinator‐mediated plant–plant interactions at multiple stages of the pollination process can lead to a complete understanding of their ecological consequences in nature.
... Such effect may be particularly likely if plants offer complementary rewards (e.g. nectar and pollen), or if differentiation occurs with respect to flowering time (Waser & Real 1979) or pollen placement site (Pauw & Johnson 2017). It is interesting that Fantinato et al. found no evidence for positive interactions in their system. ...
The role of competition in structuring plant communities has recently entered a new phase by considering interactions with pollinators. In this issue of Journal of Vegetation Science, Fantinato et al. show that co-occurring grassland plants tend to use different pollinators or diverge in anther morphology. The study opens the door for investigation of the ecological and evolutionary processes that generate this pattern.
