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. 2022 May 25;24(5):806–814. doi: 10.1111/plb.13433

A generalized bird pollination system in Schotia brachypetala (Fabaceae)

I Kiepiel 1,✉, M Brown 1, S D Johnson 1
Editor: A Dafni
PMCID: PMC10286656  PMID: 35500151

ABSTRACT

  • 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.

Keywords: Bird pollination, breeding system, opportunistic nectarivore, pollen transfer, self‐incompatibility, specialist nectarivore

The relatively open, cup‐shaped flowers of Schotia brachypetala are pollinated by both specialist and opportunistic nectarivorous birds; however, opportunistic birds are likely to contribute more to fecundity due to their greater abundance and per‐visit pollen deposition on stigmas.

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INTRODUCTION

The diverse morphology and nectar properties of bird‐pollinated flowers reflect various behavioural, morphological and physiological traits of flower‐visiting birds (Cronk & Ojeda, 2008; Pauw, 2019; McWhorter et al. 2021). A long‐standing distinction was made between hummingbird and passerine avian pollination systems (Baker & Baker, 1983; Martínez del Rio et al. 1989), but it has been suggested that this taxonomic framework be replaced by a more functionally based system which distinguishes flower feeding birds as either specialist or generalist nectar feeders (Johnson & Nicolson, 2008). This functional system better explains global trends of convergent evolution in the morphology and nectar properties of bird‐pollinated flowers (Johnson et al. 2006; Johnson & Nicolson, 2008; Nicolson et al. 2015). For example, a meta‐analysis showed that generalist adapted flowers are characterized by large volumes (40–100 µl) of dilute nectar (8–12%), containing little sucrose (0–5%), whilst those adapted to specialist nectarivores produce smaller volumes (10–30 µl) of more concentrated nectar (15–25%) with higher sucrose proportions (40–60%) (Johnson & Nicolson, 2008).

Bird pollination has evolved numerous times in diverse angiosperm lineages (Cronk & Ojeda, 2008; Krauss et al. 2017; Abrahamczyk, 2019; Janeček et al. 2020). The best‐known avian flower visitors are specialist nectarivores (obligate nectar feeders) such as hummingbirds (Trochilidae), sunbirds (Nectariniidae) and honey‐eaters (Meliphagidae); however, an estimated 50 bird families (Proctor et al. 1996) encompassing more than 1000 species have been identified in pollination mutualisms embracing several thousand plants (Krauss et al. 2017; Pauw 2019). Generalist avian nectarivores (opportunistic nectar feeders) are involved in the pollination of at least 70 plant genera spanning 36 families (Abrahamczyk, 2019). Southern Africa contains a large number of plant species which are seemingly adapted to generalist bird pollination (Oatley & Skead, 1972; Johnson et al. 2006; Botes et al. 2008; Brown et al. 2009; Arena et al. 2013; Craig, 2014; Nicolson et al. 2015; Diller et al. 2019; Payne et al. 2022). Corolla tubes of these species are typically more open and shorter than those of flowers adapted to sunbirds, the specialist avian nectarivores in the region. Nectar in generalist bird‐adapted flowers is therefore also available to sunbirds, but not always utilized, either because it is very dilute and thus not energetically profitable, or because it is laced with distasteful secondary compounds which function as a palatability filter (Johnson et al. 2006; Nicolson et al. 2015).

Because fruit is similar to nectar in terms of sugar constituents, many frugivorous birds such as bulbuls (Pycnonotidae) and white‐eyes (Zosteropidae) are preadapted to nectar feeding. Yet, even seed‐eating birds such as weavers (Ploceidae) are known to be opportunistic nectarivores (for review see Craig, 2014). Data on the pollination effectiveness of generalist birds are comparatively scarce (Ortega‐Olivencia et al. 2005, 2012; Ollerton et al. 2008; Fernandez de Castro et al. 2017), but one study demonstrates that generalist birds outperform specialist sunbirds in terms of pollen deposition on stigmas of an African aloe (Diller et al. 2019). Highly generalized bird pollination systems involving both specialist and opportunistic avian nectarivores are unusual (Botes et al. 2008; Brown et al. 2009; Symes et al. 2009; Etcheverry et al. 2012; Craig, 2014; Diller et al. 2019). These systems may reflect intermediate states during shifts from specialist to generalist pollination (or vice versa) or an evolutionary stable strategy of pollination system generalization (see de Brito et al. 2017 and references therein). In the South African lily Kniphofia linearifolia Baker (Asphodelaceae), there is evidence for geographically separated morphotypes pollinated by either generalist or by specialist avian nectarivores (Brown et al. 2011). Although trade‐offs in deployment of floral traits usually favour some degree of ecological specialization in pollination systems (Phillips et al. 2020; Ohashi et al. 2021), it is well‐known that some pollination systems can involve several functional pollinator groups (Waser, 1998). Whilst sunbirds have beaks which are much narrower than those of generalist birds, both groups have similar perching requirements and often have similar beak lengths (Diller et al. 2019), suggesting that relatively open flowers which are adapted for generalist bird pollination could also be effectively pollinated by sunbirds if the nectar in these flowers is energetically profitable and not distasteful to sunbirds because of the presence of secondary compounds.

We investigated the pollination system of Schotia brachypetala Sond. (Fabaceae), a tree known as the ‘weeping boer‐bean’ on account of its copious production of dilute nectar that often drips to the ground. Ornithologists have noted visits to flowers of this tree by at least 54 bird species, including both specialist and generalist nectarivores (Symes & Yoganand, 2013). The aims of this research were to: (i) document floral traits, including nectar properties and spectral reflectance; (ii) determine whether the species is genetically self‐incompatible; (iii) determine if seed production is pollen‐limited; (iv) determine the overall contributions of birds to seed production; and (v) establish the per‐visit pollen deposition effectiveness of generalist versus specialist avian nectarivores.

MATERIAL AND METHODS

Study species

Schotia Jacq. comprises four southern African endemic tree species closely allied with the thicket biome (Ross, 1997; Ramdhani et al. 2010). Schotia brachypetala has a widespread distribution in the eastern and north‐eastern parts of South Africa, as well as Mozambique, Eswatini and Zimbabwe (Codd, 1956; Ross, 1997; Symes & Yoganand, 2013). Flowering takes place from early to late in the Austral spring (August to November), occurring prior to leaf emergence in areas where frost occurs. The protogynous flowers are usually cauliflorous and are arranged in densely clustered panicles. The tubular floral cup (hypanthium) of the perianth forms the nectar chamber of the largely actinomorphic flowers.

Study sites and duration

During August to November 2020, we conducted pollinator observations, floral trait measurements, controlled hand‐pollinations and experimental bird exclusion in a population of ca. 50 trees at Fountainhill Nature Reserve (hereafter FHNR, 29°28′ S, 30°31′ E) outside of Wartburg, KZN, RSA. We observed trees in the Mpushini Valley (Ashburton, KZN, RSA) and also made numerous opportunistic observations in the Pietermaritzburg area (KZN, RSA). Single‐visit pollen deposition trials were conducted in 2009 using trees in the Botanical gardens of University of KwaZulu‐Natal (Pietermaritzburg Campus). Four camera traps (Bushnell® 14 Mp NatureView Cam HD) were also set at this site in October 2014 over a period of 4 days (total of 384 camera hours) for comparative purposes.

Floral visitor observations

Over a period of several days, we recorded the species, time of arrival and behaviour of floral visitors in trees at the FHNR site (30‐min observation periods). We also continued monitoring trees for the duration of the study period for any species we had missed during this time. Using footage from the camera traps, we recorded the date, time of day, number of probes per animal per flower, the duration of probing, the perch and head position of birds (either below or above the flowers) and the angle at which birds probed flowers (i.e. either from above the flower, through the anthers, or from the side of the flower, through the base of the stamens). From direct observations and video footage we also recorded anther and stigma contact and the location of pollen on the animals visiting S. brachypetala.

Floral traits

Using the method of Johnson & Andersson (2002), we measured floral spectral reflectance (300–700 nm, 6 flowers from 6 trees) using a fibre optic reflection probe (QR‐400‐7‐UV‐VIS; 400 µm) coupled with an Ocean Optics S2000 spectrophotometer (Ocean Optics, Dunedin, FL, USA). We measured the width of the broadest part of the flower (sepal to sepal), and floral length was recorded from the base of the receptacle to the furthermost projection of the flower (anther or stigma). The inside width of the nectary was recorded as a measure of the floral entrance. To measure the depth of the nectary, flowers were dissected in half and measurements taken from the bottom‐most part of the nectary along the principal axis, culminating at the base of the stamens. Herkogamy was measured as the distance from the stigma to the nearest anther. Nectar volume was measured using 100‐µl microcapillary tubes and concentration measured using a portable refractometer (Bellingham and Stanley; 0–50%). We measured nectar volume (at the time of anther dehiscence) and concentration in virgin bagged flowers (bagged prior to anthesis) as well as the standing nectar crop. Nectar composition was analysed using a Shimadzu high performance liquid chromatography (HPLC) instrument (12 flowers from 12 trees) according to the methods described in Steenhuisen & Johnson (2012).

Breeding system

Self‐incompatibility and the dependence of S. brachypetala on pollinators for seed set were determined using controlled hand‐pollination at the FHNR site (see figures for sample sizes). A total of 1326 flowers on 64 inflorescences (from 7 trees) were bagged at the bud stage using wire‐framed fine mesh nylon pollination bags. Bagged flowers were allocated to one of three treatments at anthesis: (i) unmanipulated (15 inflorescences) to test for autogamy; (ii) self‐pollination (23 inflorescences); (iii) cross‐pollination (26 inflorescences, where cross pollen was collected from trees at least 1 km distant). Flowers allocated to the unmanipulated treatment were bagged separately. Self‐ and cross‐pollination treatments were applied at least twice per flower prior to anther dehiscence.

Bird exclusion and supplemental hand‐pollination

To test whether birds contribute to seed production, we enclosed nine inflorescences with 545 flowers at bud stage in selective‐exclusion cages (mesh aperture: 15 × 10 mm) that permitted access by insects such as bees, but prevented visits by birds (Kiepiel & Johnson, 2014). Uncaged inflorescences (17) with 648 flowers were selected as controls. We also tested for pollen limitation of fecundity by performing supplemental cross‐pollination (pollen supplemented at least twice) on a third set of 29 inflorescences with 331 flowers. We compared natural fruit and seed set among flowers in the three treatment groups (treatments were on separate inflorescences). We scored fruit set, seeds per fruit and the number of aborted seeds per fruit for all treatment groups. Pollination bags were left on inflorescences for the duration of floral senescence or fruit development to prevent damage by fruit chafers (Scarabaeidae: Cetoniinae) and other fruit feeders.

Pollen deposition trials

Cage trials

Four village weavers (Ploceus cucullatus), four Cape white‐eyes (Zosterops virens) and two amethyst sunbirds (Chalcomitra amethystina) were captured in Pietermaritzburg (October 2009) using mist nets. Birds were housed in 300 × 450 × 900 mm cages at the University of KwaZulu‐Natal’s (Pietermaritzburg) Animal House and provided with food and water ad libitum (refreshed twice daily). Each trial (n = 96) involved a single bird which was placed into one section of an experimental cage. Each cage contained a perch (ca. 15‐mm diameter) running the breadth of the cage at a height of around 150 mm. A single pollen‐bearing flower was attached to the upper side of a perch, approximating the natural presentation of flowers on the trees. After this flower was visited by a bird and prior to any bill‐wiping activity, it was replaced by a single emasculated unpollinated flower. Birds typically probed the flowers multiple times (also observed in trees), which necessitated our designation of each feeding bout as a single visit rather than a single probe. After a single visit to the emasculated flower, stigmas were harvested and placed onto a glass microscope slide containing a small block of fuchsin gel which was melted prior to adding a coverslip. Pollen was counted using a light microscope at 40× magnification. After each trial, residual pollen was removed from birds using cotton swabs and birds were checked with a 10× magnification hand lens to ensure they were free from pollen prior to the next trial.

Field trials

Schotia brachypetala flowers (n = 90) were bagged and emasculated in the location and manner described above. Upon stigma receptivity, flowers were unbagged and allowed a single visit (feeding bout) from an individual bird. Immediately following feeding, stigmas were collected and mounted onto microscope slides as described above.

Statistical analysis

Data was analysed using generalized linear models executed in SPSS 27 (IBM). The proportion of flowers setting fruit were analysed using models with a binomial distribution and a logit link function, while data for the other count measures (number of seeds per fruit, number of seeds per flower, number of aborted seeds) and pollen deposition were analysed using negative binomial models with a log link function. We used generalized estimating equations (GEEs), which accounted for possible correlations between flowers on the same tree by considering each tree as a subject variable. Models incorporated an exchangeable correlation matrix and significance was assessed with Wald statistics. To adjust for multiple comparisons, we used the sequential Šidák method. Marginal means and asymmetrical standard errors were obtained through back‐transformation of values from the linear scale. Where GEEs failed to run due to a lack of variance (e.g. zero fruit set for self‐pollination treatment), we substituted a single value (e.g. a 0 replaced by a 1) to allow model convergence. Since this reduces differences among means it makes the test slightly more conservative.

RESULTS

Floral visitor observations

We recorded 23 bird species from ten families visiting S. brachypetala at the FHNR site (Table 1). Seven of these species were specialist nectarivorous sunbirds, while the remainder were opportunistic nectarivores (generalists). Cape white‐eyes (Fig. 1C,D) were the most common visitors recorded by camera traps in Pietermaritzburg, followed by bees (Apis mellifera scutellata, Apidae), amethyst sunbirds (Fig. 1F), village weavers (Fig. 1A), white‐bellied sunbirds and a single mousebird (Table 2). Weavers, Cape white‐eyes and mousebirds typically received and deposited pollen via the forehead feathers, base of the bill and, to a lesser extent, the bill itself (Table 2). Camera traps showed that amethyst and white‐bellied sunbirds mostly failed to make anther or stigma contact because they probed sideways through the stamen filaments rather than by feeding from above the flowers (Table 2). However, we did observe sunbirds occasionally contacting anthers and stigmas with bill and head feathers. Almost 90% of Cape white‐eyes and over two thirds of village weavers probed sideways, but unlike sunbirds, these birds often made anther and stigma contact (Table 2).

Table 1.

Specialist and opportunistic avian nectarivores observed feeding on Schotia brachypetala flowers at the FHNR site.

bird type family species common name n proportion of recorded visits
Specialist Nectariniidae Cinnyris afer Greater double‐collared Sunbird NR
Cinnyris chalybeus Southern double‐collared Sunbird NR
Cinnyris talatala White‐bellied Sunbird 36 0.20
Chalcomitra amethystina Amethyst Sunbird 52 0.29
Cyanomitra olivacea Eastern Olive Sunbird 1 0.01
Cyanomitra veroxii Grey Sunbird NR
Hedydipna collaris Collared Sunbird 1 0.01
Opportunist Cisticolidae Prinia subflava Tawny‐flanked Prinia 2 0.01
Coliidae Colius striatus Speckled Mousebird NR
Lybiidae Lybius torquatus Black‐collared Barbet 3 0.02
Oriolidae Oriolus larvatus Black‐headed Oriole NR
Phoeniculidae Phoeniculus purpureus Green Wood‐hoopoe 5 0.03
Ploceidae Amblyospiza albifrons Thick‐billed Weaver NR
Ploceus bicolor Dark‐backed Weaver NR
Ploceus cucullatus Village Weaver 9 0.05
Ploceus intermedius Lesser Masked Weaver 14 0.08
Ploceus ocularis Spectacled Weaver NR
Ploceus velatus Southern Masked Weaver NR
Pycnonotidae Pycnonotus tricolor Dark‐capped Bulbul 4 0.02
Sturnidae Lamprotornis corruscus Black‐bellied Starling NR
Onychognathus morio Red‐winged Starling 5 0.03
Lamprotornis nitens Cape Glossy Starling 6 0.03
Zosteropidae Zosterops virens Cape white‐eye 40 0.22
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NR = not recorded.

Fig. 1.

Fig. 1

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Examples of birds feeding on the nectar‐rich flowers of Schotia brachypetala in the Pietermaritzburg area. (A) Village weaver Ploceus cucullatus. (B) Spectacled weaver Ploceus ocularis. (C, D) Cape white‐eye Zosterops virens. (E) Olive sunbird Cyanomitra olivacea. (F) Amethyst Sunbird Chalcomitra amethystina. Scale bars 20 mm.

Table 2.

Foraging behaviour of animals visiting Schotia brachypetala flowers, as determined using video footage from camera traps at the Botanical gardens site.

species n

probes per flower

mean ± SE

probe time (s)

mean ± SE

 perch below flower (%) head below flower (%) probe flower from side (%) anther contact (%) pollen location stigma contact (%)
Bee 17 1.0 ± 0.0 3.3 ± 0.7 N.A. N.A. 100 71 legs, body 35
Amethyst sunbird 10 1.0 ± 0.0 1.7 ± 0.2 60 80 100 0 – 0
Cape white‐eye 24 1.3 ± 0.2 2.7 ± 0.2 91 82 88 32 head 21
Speckled mousebird 1 1.0 ± 0.0 2.0 ± 0.0 100 0 0 100 head, bill 100
Village weaver 6 1.4 ± 0.2 2.8 ± 0.5 50 50 67 83 head, bill 67
White‐bellied sunbird 6 1.0 ± 0.0 2.5 ± 0.8 50 50 100 0 – 0
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Bees were very frequent and numerous visitors to S. brachypetala flowers. Bees began foraging early in the morning, with activity increasing throughout the day and ceasing in the late afternoon. Bees fed exclusively on S. brachypetala nectar at the FHNR site but were also recorded collecting pollen at the Botanical Gardens site, where over a third of bee visits resulted in stigma contact (Table 2).

The green‐banded swallowtail butterfly Papilio nireus lyaeus (Papilionidae) was observed feeding on the flowers on four occasions. Towards the end of the flowering season, many species of fly (Calliphoridae, Muscidae, Tabanidae) were observed attempting to feed from floral nectar in a similar fashion to bees.

Floral traits

The volume of nectar found in bagged flowers was double that of the standing crop, and nectar concentration was higher in bagged flowers compared to unbagged ones (Table S1). Nectar was dominated by monosaccharides (Table S1). Almost all parts of S. brachypetala flowers are a vivid red to humans and reflect only small amounts of other wavelengths, including UV (Fig. S1). Flowers exhibit protogyny, and herkogamy becomes more pronounced with time.

Breeding system

Bagged unmanipulated and self‐pollinated flowers yielded negligible fruit set, while approximately 57% of cross‐pollinated flowers set fruit (Fig. 2A). Control and self‐pollination treatments failed to produce any viable seeds, while cross‐pollinated flowers set large numbers of viable seeds, as well as some aborted seeds (Fig. 2C,E,G).

Fig. 2.

Fig. 2

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Schotia brachypetala fecundity among unmanipulated (bagged and open control), self, cross, bird exclusion (caged) and pollen supplementation treatments. Fecundity measures for treatment sets are the proportion of flowers that set fruit (A–B), seeds per fruit (C–D), seeds per flower (E–F) and aborted seeds per fruit (G–H). Values are mean (±SE), with number of flowers (and trees) given adjacent to mean symbols. Means that share a letter are not significantly different.

Bird exclusion and supplemental hand‐pollination

Exclusion of birds led to a significant reduction in fruit and seed set relative to the open‐pollinated control treatment (Fig. 2B,D,F). Pollen supplementation led to a significant increase in fruit and seed set (Fig. 2B,D,F), but did not influence the total number of aborted seeds (Fig. 2H).

Pollen deposition trials

Cage trials

There was a significant difference in per‐visit pollen deposition among the three bird species (Fig. 3). Village weavers deposited twice as much pollen on stigmas as was deposited by Cape white‐eyes, and seven times as much pollen as was deposited by amethyst sunbirds (Fig. 3).

Fig. 3.

Fig. 3

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(A) Schotia brachypetala stigmatic pollen deposition by three bird species during flight cage trails. Birds were allowed to feed once (feeding bout) from a single pollen‐bearing (dehiscent) virgin S. brachypetala flower, followed by a single emasculated virgin flower. Values represent mean (±SE) deposition of S. brachypetala pollen, with number of individual birds and number of flowers (in parentheses) given adjacent to mean symbols. (B) Schotia brachypetala stigmatic pollen deposition by five bird species during field trials. Birds were allowed to feed once (feeding bout) from a single emasculated virgin S. brachypetala flower. Values represent mean (±SE) deposition of S. brachypetala pollen, with number of individual birds/flowers given adjacent to mean symbols. Means that share letters are not significantly different.

Field trials

Per‐visit pollen deposition in the field also varied significantly among bird species, with the highest deposition being by red‐winged starlings and the lowest by amethyst sunbirds (Fig. 3B).

DISCUSSION

Our results indicate that S. brachypetala is pollinated almost exclusively by birds, employing a pollination system that is highly generalized in terms of avian diversity. This diversity of visitors may reflect that the flowers are relatively open, with nectar volumes large enough to entice generalist birds, but also concentrated enough to be energetically attractive to sunbirds. We found that both opportunistic and specialist nectarivores are capable of transferring pollen of this species, but opportunistic nectarivores are likely more important pollinators based on their visitation frequency (Tables 1, 2; Symes & Yoganand, 2013), foraging behaviour (Table 2) and greater per‐visit pollen deposition compared to sunbirds (Fig. 3A,B). This study corroborates earlier work (Symes & Yoganand 2013) indicating that S. brachypetala is visited by a diverse assemblage of generalist and specialist avian nectarivores (Table 1). Specialist sunbirds made up ca. 30% of the 23 bird species recorded in our study (Table 1), whereas they made up ca. 20% of the 54 species recorded by Symes & Yoganand (2013). This likely reflects spatiotemporal variation in diversity and abundance bird community assemblages.

Controlled hand‐pollination experiments indicate that S. brachypetala is self‐incompatible (Fig. 2) and consequently reliant on pollinators. Strong self‐incompatibility systems are common in long‐lived plants and large trees, where the risks of geitonogamy are significantly greater than for those species with fewer flowers (Gibbs & Bianchi, 1999). Schotia brachypetala trees display substantial pollen limitation, as evidenced by significant enhancement of fruit and seed set by pollen supplementation treatment (Fig. 2B,D,F). This could be limitation of either pollen quantity or quality, or both. The increased number of aborted seeds in cross‐pollinated flowers compared to self‐pollinated flowers (Fig. 2G) may reflect local resource limitation in the fruits of well‐pollinated flowers.

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 bird‐adapted 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; Johnson et al. 2014; 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). In a study involving the bird‐pollinated southern African Aloe maculata All., experimental increases of bee abundance in plant populations resulted in the reduction of both female and male fitness (Hargreaves et al. 2010). Self‐incompatibility (Fig. 2), herkogamy (Table S1) and protogyny (see Hargreaves et al. 2009) in S. brachypetala restrict the ability of bees to act as pollinators (Fig. 2B,D,F) and effectively mean that pollen collection by these insects amounts to pollen theft. As is the case of a number of South African Aloes (Hoffman, 1988; Botes et al. 2009a), bees are blocked from entering the corolla by the tubular cage‐like stamen arrangement, and nectar theft is thus partially mitigated by floral architecture.

Lower levels of S. brachypetala pollen deposition by sunbirds compared to generalist birds is probably related to their tendency to probe for nectar through the anther filaments with their long slender bills (e.g. Table 2), thus avoiding stigma and anther contact (Fig. 1E). Although little evidence exists for bird‐mediated selection pressure on floral width (Nattero & Cocucci, 2007; Brown et al. 2011; García et al. 2020), experiments with hummingbirds suggest that pollen removal increases as floral width increases (Campbell et al. 1996). Conversely, pollen transfer by sunbirds has been shown to be less effective when flowers are wide‐mouthed (Hargreaves et al. 2019) and, consistent with our results, a recent study of a South African Aloe reveals that generalist birds with their broad bills can be more effective pollinators of wide‐mouthed flowers than specialist nectarivores (Diller et al. 2019).

Schotia brachypetala nectar has a sugar concentration of ca. 15%, which is within the lower range of sunbird‐pollinated plants (Table S1; Nicolson, 2002), and at the upper end of the sugar concentrations of nectar in flowers pollinated by opportunistic birds (Johnson & Nicolson 2008). However, the very large volumes and dominance of monosaccharides in the nectar are more consistent with pollination by generalist birds (Table S1; Symes & Yoganand, 2013). Furthermore, given that S. brachypetala nectar contains only trace amounts of sucrose, sturnids are not excluded from the pollination assemblage as they would be if the nectar contained a significant proportion of sucrose, which is toxic to these birds (Martínez del Rio et al. 1992). Schotia brachypetala flowers at a time when food for birds is comparatively scarce. Since few other plants are flowering or fruiting, and insect abundance is comparatively low, the flowers form an important energy resource for sunbirds and occasional nectarivores, such as frugivores and granivores. These species likely track the trees when they commence flowering at the end of the dry season (Craig & Hulley, 1994; Symes et al. 2001; Symes & Nicolson, 2008; Kuiper et al. 2015). Spatiotemporal seasonal nectar tracking has been documented in a number of South African bird species (Skead, 1967; Oatley & Skead, 1972; Frost & Frost, 1980; Symes & Nicolson, 2008; Kuiper et al. 2015), and South African nectarivorous bird communities are known to be shaped at a small scale by resource abundance, and by resource diversity at larger scales (Geerts et al. 2020). However, in some years entire populations of S. brachypetala can go without flowering, making the extent of bird seasonal reliance on local trees unclear.

Conclusions

Opportunistic bird pollination systems may involve only a few bird species (Arena et al. 2013), but more frequently comprise a large and diverse number of taxa (Johnson et al. 2006; Johnson & Nicolson, 2008). Some systems include dozens of species (Botes et al. 2008; Symes & Yoganand, 2013) encompassing a significant proportion of local avian communities (Symes & Nicolson, 2008), and a number of these systems involve visitation by both opportunistic and specialist bird nectarivores (Botes et al. 2008; Symes et al. 2008; Brown et al. 2009; Symes & Yoganand, 2013; Payne et al. 2022). Few studies have determined the contribution to pollination by either functional group (Brown et al. 2009; Diller et al. 2019). This work demonstrates that both specialist and opportunistic birds can contribute to plant fecundity in a generalized bird pollination system. The relatively open flowers of S. brachypetala with their large volumes of moderately concentrated hexose‐dominated nectar are attractive to a wide range of birds and can be pollinated by birds of varying morphology and size. Schotia brachypetala flowers could be considered as adapted mainly to opportunistic avian nectarivores given that opportunistic birds deposited more pollen than specialist sunbirds. Yet, despite being visited by large numbers of birds, trees showed clear evidence of pollen limitation to fecundity. A key challenge is to determine whether pollen limitation is due to high levels of geitonogamy (i.e. stigma clogging with self‐pollen interfering with seed production) or failure of some flowers to receive any cross pollen. Measuring fruit and seed set following single visits would also prove valuable in determining the contributions that generalist and specialist birds make to S. brachypetala fecundity (e.g. Geerts 2016).

Supporting information

Fig. S1. Spectral reflectance of Schotia brachypetala flowers. Spectra represent mean reflectance (n = 6 flowers, from 6 trees).

Click here for additional data file. (211.4KB, EPS)

Fig. S2. Deposition of foreign pollen grains on Schotia brachypetala stigmas by five bird species during field trials. Birds were allowed to feed once (feeding bout) from a single emasculated virgin S. brachypetala flower. Values represent mean (±SE) deposition of foreign pollen, with number of individual birds/flowers given adjacent to mean symbols. Means that share letters are not significantly different.

Click here for additional data file. (184.6KB, EPS)

Table S1. Floral traits of Schotia brachypetala flowers at the FHNR site. Values are grand means (mm ± SE) with sample size in parentheses (number of flowers, number of trees).

Click here for additional data file. (13.7KB, docx)

Acknowledgements

Thanks to Fountainhill Estate and Ed Gevers for assistance and for permission to work in Fountainhill Nature Reserve. Thanks to Daniella Egli, Julian Z. Kiepiel, S. Anne Kiepiel and Cande Rodríguez for assistance with fieldwork. Thanks to five reviewers for valuable comments on the manuscript. This study was funded by the National Research Foundation (grant 46372 to SDJ).

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Fig. S1. Spectral reflectance of Schotia brachypetala flowers. Spectra represent mean reflectance (n = 6 flowers, from 6 trees).

Click here for additional data file. (211.4KB, EPS)

Fig. S2. Deposition of foreign pollen grains on Schotia brachypetala stigmas by five bird species during field trials. Birds were allowed to feed once (feeding bout) from a single emasculated virgin S. brachypetala flower. Values represent mean (±SE) deposition of foreign pollen, with number of individual birds/flowers given adjacent to mean symbols. Means that share letters are not significantly different.

Click here for additional data file. (184.6KB, EPS)

Table S1. Floral traits of Schotia brachypetala flowers at the FHNR site. Values are grand means (mm ± SE) with sample size in parentheses (number of flowers, number of trees).

Click here for additional data file. (13.7KB, docx)

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