OR I G I N A L AR T I C L E

Pollination structures plant and nectar-feeding birdcommunities in Cape fynbos, South Africa: Implications forthe conservation of plant–bird mutualisms

Sjirk Geerts1 | Anina Coetzee2 | Anthony G. Rebelo3 | Anton Pauw4

1Department Conservation and MarineSciences, Cape Peninsula University ofTechnology, Cape Town, South Africa2DST/NRF Centre of Excellence at theFitzPatrick Institute of AfricanOrnithology, University of Cape Town,Cape Town, South Africa3South African National BiodiversityInstitute, Kirstenbosch Research Centre,Claremont, South Africa4Department of Botany and Zoology,Stellenbosch University, Matieland,South Africa

CorrespondenceSjirk Geerts, Department Conservationand Marine Sciences, Cape PeninsulaUniversity of Technology, P.O. Box652, Cape Town 8000, South Africa.Email: geertss@cput.ac.za

Funding informationCPUT University Research Grant;South African National ResearchFoundation (NRF), Grant/AwardNumbers: 115093, 88553; BotanicalEducation Trust

Abstract

With the current global concerns about pollinators, relationships between spe-

cies 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 struc-

tured by resource abundance (Proteaceae nectar) or Proteaceae diversity at dif-

ferent 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, veg-

etation 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 com-

plementary 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 conser-

vation areas.

KEYWORD S

bird-pollination, nectar, pollination mutualisms, Promerops cafer, Proteaceae

1 | INTRODUCTION

The variation in plant richness can be explained—at leastpartially—by pollinators and vice versa, with a subse-quent positive correlation between pollinator andSjirk Geerts and Anina Coetzee contributed equally to this study.

Received: 10 April 2020 Revised: 22 April 2020 Accepted: 3 May 2020

DOI: 10.1111/1440-1703.12148

Ecological Research. 2020;1–19. wileyonlinelibrary.com/journal/ere © 2020 The Ecological Society of Japan 1

flowering plant species richness at a community level(Biesmeijer et al., 2006; Kleijn et al., 2004; Potts, 2003;Steffan-Dewenter & Tscharntke, 2001). In general, theseplant–pollinator networks have a robust structure(Fortuna & Bascompte, 2006; Memmott, Waser, &Price, 2004) and only under high disturbance pressures dothese networks reach a tipping point (Memmottet al., 2004; Potts et al., 2010). Globally pollinators areinfluenced by human activities in a variety of ways(Bond, 1994; Geerts & Pauw, 2011a; Geerts &Pauw, 2011b; Kearns, Inouye, & Waser, 1998; Lindberg &Olesen, 2001). Therefore, it is not surprising that one offthe main focus areas of plant–pollinator studies is tounderstand what determines and alters their communitycomposition (Cameron, 1999; Fleming & Muchhala, 2008;Fox & Hockey, 2007; Schmid et al., 2015).

The shift toward a more inclusive community-wideapproach (Pauw & Stanway, 2015; Sargent & Ackerly, 2008;Stanton, 2003)—rather than species specific pair-wiseinteractions—enables a better evaluation of environmentalchanges since more connections in the plant–pollinatorcommunity are considered. The dependence of individualspecies in pollinator communities will change with changesin particular components of the pollinator network. For pol-linators, impacts will be determined by nest site availability,predation, disease or territoriality (Burd, 1995; Skead, 1967).For plants, the impact will depend on the degree of depen-dence on pollinators for seed set, degree of pollinator speci-ficity and the degree of dependence on seeds for populationpersistence (Bond, 1994). The currency is nectar, whichplays an important role in plant–pollinator interactions(Heinrich, 1975; Heinrich & Raven, 1972). In particular,since foraging movements of pollinators—and more solarger pollinators such as birds—are influenced by the het-erogeneous spatial distribution of nectar (Ghazoul, 2005).Nectar-feeding bird pollinators occur mostly in the Neotrop-ics, Australasia and the Afrotropics (Pauw, 2019). In Africa,sunbirds and sugarbirds are the dominant vertebrate polli-nators (see, e.g., Fleming & Muchhala, 2008). Together withthis, a wealth of bird data is available in South Africa (theSouth African Bird Atlas Project). Despite this, the extent towhich nectarivorous bird communities are structured byresource abundance or resource composition at differentspatial scales in South Africa has received limited attention.Add to this the detailed dataset available for the huge diver-sity and abundance of nectar rich Proteaceae in the Capefynbos and it presents an ideal study system to addressthese questions (Rebelo, 2006).

Pollinators are thought to be important in the originand maintenance of the Cape's floral diversity, but thespecialist nectar-feeding bird community in the Cape Flo-ristic Region (CFR) is a relatively simple one with onlyfour nectar-feeding bird species that occur throughout

the CFR. They therefore play a disproportionally impor-tant role in maintaining the large number of bird-pollinated plant species at the Cape, which comprisesabout 4% of the total plant species (Rebelo, 1987). This sys-tem is thus highly asymmetrical, which is in contrast withbird-pollination systems in other parts of the world whichinvolve many more bird species. Despite this, the interac-tion specialization is similar between sunbird–flower andhummingbird–flower communities (Bond, 1994; Brown &Bowers, 1985; Feinsinger, 1978; Geerts & Pauw, 2009;Hockey, Dean, & Ryan, 2005; Zanata et al., 2017). Further-more, the CFR is a fire-adapted ecosystem and pollinatorcommunities are influenced by the successional stage ofplant communities and thus the frequency of fires (vanWilgen et al., 2010).

From a landscape scale perspective, the nectar-feedingbird community in the CFR is an ideal system, since exten-sive information is available in the form of bird atlas data.From the plant community perspective, the Proteaceae isan ideal study system since other than the extensive infor-mation available (Protea Atlas Project; Rebelo, 2006),Proteaceae are the dominant overstorey species in most fyn-bos communities (Vlok & Yeaton, 1999), contain manybird-pollinated species (Rebelo, 1987) and provide abundantnectar (Calf, Downs, & Cherry, 2003; Geerts, 2011).Although parts of the biome (southwestern Cape) and asubset of Proteaceae species (19) have been studied in rela-tion to nectar availability, here we present data on theentire biome and include all bird-pollinated Proteaceae(Nottebrock et al., 2017; Schmid et al., 2015, 2016).

Of the 330 Proteaceae species occurring in the CFR,approximately 25% are potentially pollinated by nectar-feeding birds, with the Cape Sugarbird a particularly impor-tant pollinator (Collins, 1983; Fraser, 1989; Fraser &McMahon, 1992; Martin & Mortimer, 1991; Mostert, Sieg-fried, & Louw, 1980; Pauw & Johnson, 2017; Skead, 1967).Despite Proteaceae being such an important component ofthe CFR vegetation, relatively few comprehensive polli-nation studies have been conducted on avian pollinationin this family (Collins, 1983; Collins & Rebelo, 1987;Johnson, 2015; Schmid et al., 2015; Wright, Visser,Coetzee, & Giliomee, 1991). About half of theornithophilous Proteaceae are non-resprouting andwhen adult plants are killed by fire the next generationgrows from seeds, resulting in stands of similar agedplants. Proteaceae are relatively slow to mature and onlystart to flower abundantly 4–5 years after a fire(Cowling, 1992). Most South African Proteaceae—butless so for Leucospermum—are dependent on pollenvectors—since they are self-incompatible and set no via-ble seed when pollinators are excluded (Collins &Rebelo, 1987; Horn, 1962; Johnson, 2015; Schmidet al., 2015).

2 GEERTS ET AL.

In this study, we ask whether nectarivorous bird com-munities are structured by resource abundance orresource composition at (a) the plot and (b) landscapescale and (c) whether flowering phenology varies byregion.

2 | METHODS

2.1 | Study area

We obtained Proteaceae ecological data and distributiondata for the CFR from the Protea Atlas Project databaseand bird distribution and abundance data for the CFRfrom the South African Bird Atlas Project 2 database.Data for the Cape fynbos were extracted by clipping thedatasets with the Cape boundary GIS layer derived fromthe Cape Action for People and Environment project(CAPE). Spatial data were projected to the WGS 1984geographic coordinate system. Spatial analyses were con-ducted in ArcMap 10.3 (ESRI ArcMap 2010). On asmaller scale, 34 one-hectare plots were sampled acrossthe southwestern Cape for nectar-feeding birds, nectarand vegetation characteristics (Appendix A).

2.2 | Study species

We compiled a list of all Proteaceae species within theCFR that conform to the bird-pollination syndrome.Proteaceae species that are visited by nectar-feeding birdshave brush-type inflorescences with morphological adap-tations for bird-pollination described in detail in Rebelo,Siegfried, and Crowe (1984). We based our list on theavailable 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) butwith a number of species not assessed for bird-pollination,we subsequently selected species according to the follow-ing morphological criteria that are likely to indicate birdpollination (Rebelo, 2001): For the genera Mimetes andProtea, species that bore inflorescences >20 cm above gro-und level and have flower styles longer than 25 mm. ForLeucospermum we considered species that bore inflores-cences >20 cm above ground level and with styles longerthan 35 mm as these larger flower heads are typically bird-pollinated (Rebelo, 2001). For the group of flat pincush-ions (styles less than 35 mm), L. mundii (Meisn.) andL. oleifolium ((Bergius) R.Br.) were also included as they

are pollinated by birds, but Protea angustata was excluded(Johnson, 2015; Rebelo, 2001; S. Steenhuisen, personal com-munication). In addition, all species that are specificallymentioned to have a yeasty odor or pollinated by waspswere excluded (Rebelo, 2001). We also excluded all hybrids.Based on this, only the genera Mimetes, Leucospermumand Protea contain potentially bird-pollinated species.These include 35 Protea, 23 Leucospermum and 13Mimetesspecies (Appendix B).

The four nectar specialist bird species resident in theCFR are the Cape Sugarbird (Promerops cafer L.),Orange-breasted Sunbird (Anthobaphes violacea L.), Mal-achite Sunbird (Nectarinia famosa L.) and SouthernDouble-collared Sunbird (Cinnyris chalybeus L.). The firsttwo species are endemic to the CFR and largely confinedto Fynbos vegetation (Hockey et al., 2005). All four spe-cies have long, curved bills adapted to drink from tubularflowers (Skead, 1967). Proteaceae nectar is critical for—and determines the site scale visitation of—nectar feed-ing birds (Carlson & Holsinger, 2013; Nottebrocket al., 2017; Rebelo et al., 1984). In particular, since nec-tar-feeding birds breed in winter, when nectar resourcesfrom Proteaceae are at a maximum (Skead, 1967).

2.3 | Protea nectar quantification

The genus Protea frequently dominate the overstorey offynbos shrublands (Collins & Rebelo, 1987) and beingsuch an ecological important genus in the fynbos it isthus well suited for studying plant–pollinator interactions(Schurr, Esler, Slingsby, & Allsop, 2012). Leucospermumand Erica also provide nectar sources for animal pollina-tors but rarely co-flower with Protea (Collins &Rebelo, 1987) and no Leucospermum were flowering atour study sites, while Erica produces insignificantamounts of nectar compared to Protea (Heystek, Geerts,Barnard, & Pauw, 2014). To determine the effect of nectaravailability on bird communities, nectar was sampled atall study sites that contained bird-pollinated plant spe-cies. Inflorescences were collected early in the morningand nectar was extracted in the laboratory using either a5 μL or a 40 μL capillary tube (Drummond ScientificCompany, Broomall, PA). Nectar concentrations weredetermined with a 0–50% field handheld refractometer(Bellingham and Stanley, Tunbridge Wells, UK).

In Protea inflorescences the outer ring of flowersmature first and then the inner rows mature consecu-tively. Nectar for a row of open flowers (n ≈ 14) acrossthe middle of the inflorescence (as seen from above) wasmeasured, which effectively samples flowers of all ages inthe inflorescence. This largely controls for variation innectar volume between the different aged flowers in an

GEERTS ET AL. 3

inflorescence, without measuring nectar for all the200–250 flowers.

The average standing crop of nectar volume and con-centration per flower was then calculated and multipliedby the total number of flowers in the inflorescence.Standing crop provides an accurate estimate of the nectaravailable to pollinators at a given time (collection wasdone early morning when birds are most active)(Kearns & Inouye, 1993). In contrast, total nectar produc-tion over the lifetime of a single flower or inflorescence isan important measurement from a plant's perspective,but is less relevant to pollinators. All nectar measure-ments were transformed to milligrams (mg) of nectarsugar (sucrose equivalents).

2.4 | Plant–pollinator communities at asmall scale

Birds are well known to respond to vegetation structure.Therefore, to test whether vegetation structure (post-fireage and plant community composition) or nectar avail-ability best explains variation in bird species richness andabundance, vegetation of different post-fire ages, knownas a chrono-sequence, was sampled (Foster &Tilman, 2000). To determine the effect of nectar availabil-ity in different plant communities, areas containingProteaceae, Ericaceae and Restionaceae communities ofdifferent vegetation ages, were sampled. All bird-pollinated plant species were sampled. To improve sam-ple size for statistical analysis, plant communities weredivided into Protea-dominated (Proteoid Fynbos) andnon-Protea (mainly Restioid, Ericaceous and AsteraceousFynbos) vegetation. This is justified as Protea contributedalmost all, or all nectar, since no flowering bulbs andonly a few Erica scrubs were present in the plots. For34 one-hectare plots across the southwestern Cape werecorded the following variables at each site within a sin-gle day: vegetation age, number of flowering bird-pollinated Proteaceae species, number of Proteaceae indi-viduals and inflorescences, amount of nectar and nectar-feeding bird richness and abundance (Appendix A). Allsites were sampled between May and July 2007. Post-firevegetation age was obtained from local experts or esti-mated by counting the number of internodes (new inter-nodes form annually) on the tallest stem of fiveindividuals of a non-sprouting Proteaceae species, withthe mode accepted as the true age (Lamont, 1985; vander Merwe, 1969).

For the calculation of nectar availability, all bird-pollinated (i.e., Protea and other species) plants in the1-ha plots were identified. Nectar for Protea was deter-mined as described in the nectar quantification method

above, with the following addition: In open cup shapedProtea species (e.g., Protea repens), nectar in the inter-floral pool between the flowers was also measured. Theonly other flowering bird-pollinated species were Ericaspp.—which are closely associated with the Orange-breasted Sunbird (Heystek et al., 2014)—in which nectarwas measured from individual flowers. To obtain nectarsugar per hectare the number of inflorescences (Protea)or flowers (Erica) was counted in the study plot and mul-tiplied by the amount of nectar sugar.

Ten-minute bird counts were conducted within the1-ha plots by standing on a ladder and recording allnectar-feeding birds heard or seen within a 25 m radius(Bibby, Burgress, Hill, & Mustoe, 2000; Dawson &Bull, 1975). During a pilot study, counts were conductedfor 1 hr each at three sites. Nectar-feeding bird speciesrichness and abundance was found to reach a plateauafter 10 min of observation. Although short, this was suf-ficient to detect nectar-feeding birds, since they are terri-torial in winter, conspicuous and have a clearlydistinguishable call. Before counts were conducted, a set-tling period of 15 min was allowed. All sites were sam-pled once between May–July 2007. Bird counts weredone early in the morning when nectar-feeding birds aremost active; rainy and very windy days were avoided(Fry, 2000).

2.5 | Plant–pollinator communitypatterns on a landscape scale

To test if nectarivorous bird communities are structured byresource abundance or resource composition at the biomescale, nectar-feeding bird distribution data was overlaidwith species richness and abundance of ornithophilousProteaceae. Nectar-feeding bird distribution data wereobtained from the second South African Bird Atlas Project(SABAP2) database. Bird occurrences were recorded by vol-unteers since July 2007, and data collected until October19, 2017 were used in this study. Records of species occur-rences were collected as checklists in grids with a pentadresolution: 50 × 50 (approximately 8 × 8 km). We only usedgrid cells with four or more checklists (n = 788 cells), whichproduced a range of 5 to 1,134 (average 26) checklists percell. Reporting rates (number of times a species wasrecorded in a grid cell as a proportion of the total checklistsfor the cell) from repeated visits to sites can be used as anestimate of the abundance of a species at a location(Underhill, Oatley, & Harrison, 1991).

Although the SABAP reporting rates are not alwaysdirectly proportional to bird abundance (Harrison, Allan,Underhill, et al., 1997), it has been evaluated previously,and found to correspond well to other field data and

4 GEERTS ET AL.

considered fit for use in general population studies(Fairbanks, Kshatriya, van Jaarsveld, & Underhill, 2002).Factors that will influence the accuracy of SABAP data inour study are that mountaintops are not well sampled,grid cells with a small fraction of fynbos habitat mighthave biased reporting rates of fynbos specialist birds(Huntley, Altwegg, Barnard, Collingham, & Hole, 2012),and females, juveniles and individuals in eclipse plumagecan be more difficult to identify (Harrison et al., 1997).However, this study only compares abundances withinspecies, which is appropriate for this type of data(Underhill, Prys-Jones, Harrison, & Martinez, 2008).

The Protea Atlas Project (PAP) (http://protea.worldonline.co.za) collected distribution data on south-ern African Proteaceae in 500 m diameter plots during1991–2002 (Rebelo, 2006). Although the PAP and SABAPdata were not collected during the same time period,Proteaceae are long-lived plants, particularly resproutingspecies, and their abundances and distribution at the land-scape scale can remain constant for 30 years (Privett,Cowling, & Taylor, 2001), barring disturbances such asland-use change and fires, which would have affectedbirds similarly (Chalmandrier, Midgley, Barnard, &Sirami, 2013). Furthermore, both surveys were done over10 year periods and therefore captured the average dynam-ics that occur at each site. During PAP, ecological datawas also collected, such as plant abundance and floweringstatus, and we used the population codes recorded for esti-mates of population abundances (Table S1). Distributionand flowering patterns of ornithophilous Proteaceae spe-cies in the CFR were extracted from the database for atotal of 101,047 plots. This includes accurate absence datasince 2,472 well-distributed fynbos plots contained noornithophilous Proteaceae species at the time.

During PAP sampling, the flowering status of eachspecies in a plot was recorded based on the condition ofthe majority of inflorescences on all plants. Observersrecorded the proportion of plants that fell into each ofthe following six categories: In bud (BUD: majority offlower heads in bud; a few may be open but fewer areover than are open), flowering (FLOWER: flower headseither in bud or over predominate with some open; allthree classes must be present), peak flowering (PEAK:some flower heads in bud and over but with the majorityopen), over (OVER: majority of flower heads over; a fewmay be open, but fewer are in bud than are open), incone (CONE: all of the flower heads over with none openor in bud and seed heads with seeds present on plant)and nothing (NONE: no flower heads visible either as inbud, open or over and seed heads absent or havingreleased all their seeds; (Rebelo, 1991)). Since most plotswere only sampled once, there is no complete phenologi-cal data available for every location. Thus, all the

flowering data for a species were combined and the cal-culation of floral abundance per month was extrapolatedto all the plants of a species, which assumes relative uni-formity of flowering patterns across the fynbos biome.The proportional floral abundance per month was calcu-lated as a proportion of all records:

BUD4 +PEAK+FLOWER+ OVER

2

BUD+PEAK+FLOWER+OVER+CONE+NONE

BUD was divided by four since about three quarters ofthe plants have only very few plants actually in flower.Likewise, when a population was classified as OVER,only half of the plants were bearing open flowers. Insome cases, no flowers may have been recorded becauseof a recent fire and plants were not mature enough toflower yet. However, most data were collected inmature veld.

The locational floral abundance of a species was cal-culated by multiplying the proportional floral abundancefor a given month with the population abundance of thegiven location. In order to compare the bird and plantabundances, the Protea Atlas point data were convertedto grid data of the same resolution as the SABAP2 data sothat each grid cell represents the mean floral abundanceof ornithophilous Proteaceae of all plots in the grid cell.Mean floral abundances and bird reporting rates are thuscomparable estimates of abundances. For this analysis,all phenological considerations were excluded and thusthe annual floral abundances per plot were used (thesum of the monthly abundances) and bird data werepooled irrespective of the season of sampling. Speciesrichness and mean plant abundance of all ornithophilousProteaceae (Protea, Leucospermum and Mimetes species)were determined for each grid cell and combined.

2.6 | Floral spatio-temporal patterns on alandscape scale

To explore whether Proteaceae flowering phenology variesby region we analyzed the floral spatio-temporal patternsof ornithophilous Proteaceae in the fynbos biome. Foreach plot sampled, the total floral abundance was esti-mated by adding up the floral abundance of all species inthe plot for a particular month. This is justified since spe-cies differed little in the number of inflorescences pro-duced per plant, since floral abundances and populationabundances are highly correlated (Spearman Rank correla-tion: S = 1,496, p < .0001). To investigate the spatial pat-terns, for this analysis only, the CFR was divided into29 subregions and the phenology pattern of each subre-gion was drawn. This division is based on the grouping of

GEERTS ET AL. 5

Proteaceae species into centers of endemism, which clusteron either the mountain ranges or within lowland basins(Rebelo & Siegfried, 1990). Temporal patterns were investi-gated by comparing the mean floral abundance in eachmonth across the whole biome. Patterns for the differentgenera were also investigated separately. For these ana-lyses the Fynbos was divided into eastern and westernCFR as these areas differ in rainfall (western CFR isstrictly winter rainfall, eastern CFR less so) and fire seasonimportance for serotinous Proteaceae (Rebelo, Boucher,Helme, Mucina, & Rutherford, 2006; van Wilgen, 2009).

2.7 | Statistical analyses

To determine which variables best explain the species rich-ness and abundance of nectar-feeding birds at small andlandscape scales, models were compared with Akaike Infor-mation Criterion (AIC) scores and Akaike weights(Burnham, Anderson, & Huyvaert, 2011) using the MuMInpackage in R (Barton, 2012). The effect of the predictor vari-ables on bird species richness (count data) and abundance(at small scale) was tested with generalized linear models(GLM) with a Poisson-error distribution. For the 1-ha plotscale analyses, the following variables were assessed: (a) lognectar sugar ha−1 (mg), (b) presence of ornithophilous Pro-tea, (c) vegetation age (years), (d) ornithophilous Proteaspecies richness, (e) number of ornithophilous Protea indi-viduals and (f) number of inflorescences. For the landscapescale analyses, three predictor variables were assessed: plantabundance, floral abundance and plant species richness(normalized and, since they were correlated, they were notincluded in the same models). The effect on bird abun-dances (reporting rate, which is proportional data) wastested separately for each bird species using generalized lin-ear mixed-effect models with binomial error distributionand an observational level random factor to account forover dispersion (Browne, Subramanian, Jones, &Goldstein, 2005). Marginal pseudo-R2 values were calcu-lated with the delta method for the most supported models(Nakagawa, Johnson, & Schielzeth, 2017).

All analyses were conducted in R (R DevelopmentCore Team, 2012).

3 | RESULTS

3.1 | Plant–pollinator communities atsmall scales and nectar volumes

Nectar sugar availability in Protea vegetation ranged from4 g to 29.688 kg in the 1 ha plots. The total sugar contentof nectar varied greatly between Protea species, from

33.5 mg (±39 SD) per inflorescence in Protea nitida to852 mg (±307 SD) nectar sugar per inflorescence inP. coronata (Appendix C). Bird species richness andabundance was best correlated to the amount of sugaravailable (Table 1; Figure 1). The second most supportedmodel explaining bird species richness contained vegeta-tion age (Table 1). Nectar sugar varies with vegetationage and a threshold age of 4–5 years appears to berequired to produce sufficient nectar for nectar-feedingbird species richness and abundance to obtain optimallevels (Figure S1), with sugarbirds only present whenProtea vegetation is at least 4 years old (Figure S3).

3.2 | Plant–pollinator communitypatterns on a landscape scale

Nectar-feeding bird species richness and the abundance ofCape Sugarbird (R2 = .25), Orange-breasted Sunbird(R2 = .26) and Malachite Sunbird (R2 = .04) was best corre-lated to Proteaceae species richness (Table 2; Figure 2), withnectar-feeding bird species richness closely matchingornithophilous Proteaceae species richness across the region(Figure 3, R2 = .09). Of all bird species, the Cape Sugarbirdand Orange-breasted Sunbird show the strongest relation-ships with Proteaceae richness (Figure 2). The abundanceof Southern Double-collared Sunbird was best correlated toProteaceae plant abundance, but it was a very weak rela-tionship (Table 2, R2 = .002, p = 1).

3.3 | Floral spatio-temporal patterns on alarge scale

Annual floral abundance across all ornithophilousProteaceae species showed a unimodal peak in the winter(July–August), while lowest abundance was at the end ofsummer (February–March; Figure 4). This winter peak infloral abundance was largely due to the hyper-abundantProtea genus, since the flowering of Leucospermum andMimetes species peaked later in the year (Figure 4).Leucospermum and Mimetes had relatively high floralabundances in spring (September–November) and, partic-ularly Leucospermum, in mid-summer, when Protea floralabundances was at its lowest. For the spatio-temporal pat-tern across the fynbos, all subregions showed the samephenological pattern with a peak in winter (Figure S2).

4 | DISCUSSION

Here we show that fynbos nectar-feeding bird richnessand abundance is correlated to resource abundance at

6 GEERTS ET AL.

the community scale and by resource diversity at a biomescale. This implies that these resources contribute tostructuring nectar-feeding bird communities. We showthat at an 1 ha scale the underlying mechanism linkingnectar-feeding bird communities to ornithophilousProteaceae communities is nectar abundance—ratherthan structural changes in vegetation height associatedwith large Proteaceae shrubs (Table 1). Bird numbersshowed a rapid increase with an increase in vegetationage (Figure S1). This further highlight that there is not agradual increase in vegetation height and structure thatlinks bird and Proteaceae communities, but rather a sud-den availability of nectar when ornithophilousProteaceae start flowering. Geerts, Malherbe, andPauw (2012) showed that vegetation age is important fornectar-feeding birds and that even in recently burnedvegetation where bird-pollinated bulbs are flowering,nectar-feeding bird numbers are low. Here we show thatthe underlying reason is sugar availability and althoughthere is a correlation between vegetation age and nectarsugar, vegetation age is a crude measure of sugar avail-ability. In fact, if nectar sugar is included in our analyses,vegetation age adds no additional explanatory power(Table 1). In our case, this effect is probably enhancedbecause there were no bird-pollinated bulbs flowering inthe study plots that would have flowered and attractednectar-feeding birds. Also in our results, Erica speciesonly add an insignificant amount of nectar, with plots

TABLE 1 Variables that explain

the species richness and abundance of

nectar-feeding birds at small scale (1 ha,

n = 32) in the southwestern section of

the Cape Floristic Region of South

Africa

Model K L AICc ΔAICc wi

Bird species richness

Nectar sugar/ ha log (mg) 2 −38.86 82.14 0.000 0.970

Vegetation age 2 −43.05 90.51 8.371 0.015

Protea species richness 2 −44.22 92.85 10.711 0.005

Protea plant abundance 2 −44.53 93.48 11.342 0.003

Protea (absent/present) 2 −44.55 93.51 11.369 0.003

Null model 1 −45.80 93.74 11.603 0.003

Protea inflorescence abundance 2 −45.65 95.71 13.569 0.001

Bird abundance

Nectar sugar/ ha log (mg) 2 −48.80 102.02 0.000 1

Protea (absent/present) 2 −64.76 133.93 31.911 0

Protea species richness 2 −65.44 135.29 33.264 0

Protea plant abundance 2 −65.70 135.80 33.781 0

Vegetation age 2 −66.43 137.28 35.256 0

Protea inflorescence abundance 2 −67.08 138.57 36.546 0

Null model 1 −69.00 140.13 38.110 0

Note: All the Protea variables refer to ornithophilous Protea. For each model, the number ofparameters (K), log likelihood (L), Akaike Information Criterion (AICc), difference in AICcfrom the best model and the Akaike weight (wi) is presented.

FIGURE 1 The relationship between nectar sugar availability

in protea vegetation and nectar-feeding bird species richness (a)

and abundance (b) at an 1 ha plot scale in the southwestern

section of the Cape Floristic Region, South Africa

GEERTS ET AL. 7

having few Erica bushes, and an Erica flower producingbetween 0.02 to 0.49 mg of nectar sugar per flower versus39–852 mg of sugar for a Protea inflorescence(Appendix C). However, Erica species are a particularlycritical nectar source for the Orange-breasted Sunbirds inareas with few Proteaceae and outside of the mainflowering time (i.e., winter and early spring) of bird-pollinated Proteaceae (Rebelo et al., 1984).

Nectar-feeding birds are known to be more dependenton ornithophilous Proteaceae than other avian guilds(De Swardt, 1993) and are some of the most abundant avianfauna in mature Proteaceae vegetation. Other avian specieslike the seed-eating Cape Turtle Dove (Streptopelia capicolaSundevall), and predators like the Common Fiscal (Laniuscollaris L.), also occur in high abundance in Proteaceae veg-etation (Winterbottom, 1964). But in contrast to nectar-feeders, these species are not dependent on nectar but on

vegetation structure for nest sites or prey items (Siegfried &Crowe, 1983). Here we show that even if vegetation ismature, without nectar sugar, most nectar-feeding birds willbe absent. Similarly, when invasive alien plant species addstructure, but lack nectar, nectar-feeding birds are absent(Mangachena & Geerts, 2017), while if invasive alien plantspecies add nectar to the landscape—but no structure—nec-tar-feeding birds are common (Le Roux et al., 2020; LeRoux, Geerts, Ivey, et al., 2010). Nottebrock et al. (2017) didnot consider vegetation structure per se, but also found thatpollinator visitation strongly depends on site scale nectarsugar, which in turn influenced seed production. Interest-ingly, at such small scales high nectar sugar can decreaseper-plant visitation rates due to oversupply and theresulting competition for pollinators (Schmid et al., 2015).

On a larger scale, the abundance of three of the fournectar-feeding species was best correlated with Proteaceae

TABLE 2 Results of model

selection to determine whether

Proteaceae species richness, floral

abundance or plant abundance best

explain the species richness and

abundances of nectar-feeding birds in

the Cape Floristic Region, of South

Africa

Model K L AICc Δ AICc wi

Bird species richness

Species richness 2 −1,531.07 3,066.16 0.000 1

Floral abundance 2 −1,560.44 3,124.89 58.727 0

Plant abundance 2 −1,567.76 3,139.52 73.362 0

Null model 1 −1,588.26 3,178.53 112.369 0

Cape Sugarbird abundance

Species richness 3 −1,697.19 3,400.41 0.000 1

Floral abundance 3 −1,821.88 3,649.78 249.371 0

Plant abundance 3 −1,855.00 3,716.03 315.612 0

Null model 2 −1,947.61 3,899.24 498.827 0

Orange-breasted Sunbird abundance

Species richness 3 −1,355.15 2,716.32 0.000 1

Floral abundance 3 −1,521.21 3,048.45 332.131 0

Plant abundance 3 −1,541.94 3,089.90 373.582 0

Null model 2 −1,595.61 3,195.24 478.924 0

Malachite Sunbird abundance

Species richness 3 −2,590.63 5,187.28 0.000 1

Floral abundance 3 −2,633.00 5,272.02 84.734 0

Plant abundance 3 −2,638.03 5,282.08 94.795 0

Null model 2 −2,656.32 5,316.66 129.379 0

Southern Double-collared Sunbird abundance

Plant abundance 3 −2,718.86 5,443.74 0.000 0.765

Species richness 3 −2,720.87 5,447.76 4.012 0.103

Null model 2 −2,722.12 5,448.25 4.502 0.081

Floral abundance 3 −2,721.56 5,449.15 5.408 0.051

Note: Data are at a spatial resolution of 50 × 50 (n = 788). Mean annual floral abundance wasused. For each model, the number of parameters (K), log likelihood (L), Akaike InformationCriterion (AICc), difference in AICc from the best model and the Akaike weight (wi) ispresented.

8 GEERTS ET AL.

species richness, more so than to floral or plant abundance(Table 2). This differs from hummingbird assemblages inthe Bolivian lowlands that are structured by floral abun-dances, rather than diversity, at local (1.5 km transect)and large scales (�700 km) (see, e.g., Abrahamczyk &Kessler, 2010). The patterns observed in landscape levelcorrelations are generally influenced by spatial autocorre-lation, and the same is likely to apply here. However, herewe show several distinct and widely separated areas ofnectar and bird dearth (Figure 3). These, at least, representindependent observations, and certainly have very few, ifany, Proteaceae species in common. Proteaceae specieshave unusually small geographical ranges such that adja-cent cells will often have a different community composi-tion, contributing to the independence of observations.The SABAP data was collected later than the PAP dataand since Proteaceae community composition is more con-sistent over time than floral abundance, this may havecontributed to the stronger correlation between birds and

species richness. Nonetheless, both data sets were collectedover multiple years and therefore represent averages. Theexplanatory power of these models was relatively low,likely because of the influence of abiotic factors—otherthan mutualistic interactions—that will also affect speciesrichness. For example, it is well known that Orange-breasted Sunbirds are uncommon in lowland areas andprefer higher altitudes (Pauw & Louw, 2012). This, whilesugar water feeders and indigenous garden plants canincrease nectar-feeding bird resources in an urban context(Coetzee, Barnard, & Pauw, 2018). Other abiotic factors,such as temperature and rainfall also influence speciesrichness, with fewer ornithophilous Proteaceae in the drierand warmer west coast regions of the fynbos biome(Rebelo, 2006).

Cape Sugarbirds and Orange-breasted Sunbirds showthe strongest relationships with Proteaceae richness(Figure 2). We suggest that this is not because resourcequantity is unimportant (Nottebrock et al., 2017), but

FIGURE 2 The abundance (reporting rate) of (a) Cape Sugarbird, (b) Orange-breasted Sunbird and (c) Malachite Sunbird and (d) the

species richness of nectar-feeding birds (each line at a data point represents an additional observation) in relation to species richness of bird-

pollinated Proteaceae per grid cell (50 × 50 spatial resolution, n = 788 grid cells) in the Cape Floristic Region, South Africa. Data from SABAP

GEERTS ET AL. 9

rather a result of the combination of the uniform spatio-temporal flowering patterns across the biome and com-plementary flowering of different genera for most of theyear. The differences in floral traits (such as rewardquantity and accessibility) between Proteaceae speciesmay also contribute to this pattern. Data on geographicalvariation of phenology patterns within species were notanalyzed in this study as the focus here was landscapescale. In particular, since most of the studied Proteaceaespecies have small distribution ranges, it is unlikely thatphenology patterns of populations would differ at thecoarse scale we used (i.e., monthly abundances). As forthe wide-spread species, their floral abundances are likelyoverestimated (e.g., a species flowering in different sea-sons in the east and west of the region will appear to havea long flowering period since we combined all records)and yet we still see a clear pattern of low floral abun-dances in summer across the biome. Similar to Rebeloet al. (1984), we found a weaker relationship betweenproteas and Malachite Sunbirds compared to Orange-breasted Sunbirds, potentially due to Malachite Sunbirds'use of other plant species (Geerts & Pauw, 2009). South-ern Double-collared Sunbirds were not strongly related toProteaceae species richness or floral abundance (Table 2).This species generally occurs in lower numbers in

mountain fynbos, being present in only 2 out of the 34study plots—this despite most of the lowland fynbosbeing transformed—probably being less of a fynbos spe-cialist, more adaptable to land use change and able to uti-lize habitats such as urban, riparian and agriculturalareas (Hockey et al., 2005; Mangachena & Geerts, 2019;Pauw & Louw, 2012).

Broadly, similar phenological patterns in Proteaceaeflowering are found throughout the biome at the coursescale sampled: a floral abundance peak in winter. Sincefloral abundances are generally low in all subregions atthe same time of year, this points to the possibility that itmay not be profitable for birds to migrate in search fornectar resources. A similar study on the flowering phenol-ogy of bird-visited Eucalyptus species in Australia proposethat reliable and concordant flowering (flowering at thesame time across sites and species) makes movementsbetween sites by nectarivorous birds unlikely (Keatley &Hudson, 2007). In contrast, swift parrot migration inAustralia might be linked to flowering of specific speciessuch as Acacia pycnantha (Mac Nally & Horrocks, 2000;Saunders & Heinsohn, 2008). Furthermore, some hum-mingbirds seem to track floral abundances (Cotton, 2007).

The overall temporal floral abundance patterns ofProteaceae are mainly due to the patterns of the speciesrich and abundant Protea genus. Leucospermum andMimetes species contribute less to total abundances,except in the dry summer months when Protea floweringis at its lowest. Thus, a diversity of Proteaceae may sus-tain nectar-feeding bird populations throughout the yearwithin mountain ranges, particularly if birds are unableto escape the summer nectar scarcity by moving acrossmountain ranges because they show synchronous pat-terns. In Costa Rica, sequential flowering of the domi-nant bird-visited plant species, Hamelia, Inga and Lobeliaprovides abundant nectar for hummingbirds throughoutthe year in one mountain range (Feinsinger, 1976;Waser & Real, 1979). Likewise, the Australasian honey-eaters rely on a diversity of plant species for nectarthroughout the year (Collins & Briffa, 1982). The CFRnectar-feeding birds may be foraging from plants of otherplant families (Feinsinger & Swarm, 1982) during thenectar scarcity at the end of summer, but at this stagethere is too little data to provide insight into this.

The flowering of Leucospermum and Mimetes speciesduring times of low Protea floral abundance suggeststhat the conservation of their diversity is important forthe persistence of nectar-feeding birds and other polli-nators in the landscape. These genera are importantresources, and already under greater threat than Proteaspecies. Of the 35 ornithophilous Protea species studiedhere, 16 (46%) have a Red List status of conservationconcern, whereas 8 of the 13 (62%) Mimetes species and

FIGURE 3 Species richness of (a) nectar-feeding birds, and

(b) bird-pollinated Proteaceae in the Cape Floristic Region (50 × 50

spatial resolution, n = 788 grid cells). The location of the Cape

Floristic Region (enlarged maps) in South Africa is shown in grey

in the inset map

10 GEERTS ET AL.

16 of the 23 (70%) Leucospermum species are of conser-vation concern, that is, near threatened, threatened,endangered, or critically endangered (Appendix B;www.redlist.sanbi.org).

Many Proteaceae species are predicted to face rangecontractions with a change in climate (Bomhardet al., 2005). However, at least some species are known tobe able to successfully grow outside their native range andcould thus potentially move with climate change (Latimer,Silander, Rebelo, & Midgley, 2009). More importantly, fre-quency of fire, which is likely to increase with climatechange (IPCC, 2001), will reduce the extent of mature veg-etation and the nectar available to the bird community(Bond, Midgley, & Woodward, 2003; Geerts et al., 2012).Within the nectar-feeding bird community, species differin their nectar requirements, with the large-bodied CapeSugarbird needing substantial amounts (Collins, 1983)which can only be supplied by Proteaceae vegetation of atleast 4 years in age (Figure S3). The probability of extinc-tion depends on the strength of the pollinator–plant mutu-alism (Geerts, 2016; Geerts & Pauw, 2009). Since thenectar-feeding bird community plays an important role inshaping the plant community, a change in range of a

particular nectar-feeding bird species could elicit changesin bird-dependent plant communities. Protea reproductionand bird pollinators are most likely linked through nectarabundance (this study) and not floral signaling and acces-sibility traits (Schmid et al., 2015).

In conclusion, resource abundance contributes toshaping nectar-feeding bird communities at a small scale,while resource diversity—driven by different floweringtimes for Protea, Mimetes and Leucospermum—are bettercorrelatives at the landscape scale. This study thus high-lights the importance of community-wide conservation topreserve mutualistic relationships. From a restoration per-spective, and to bring birds back into small conservationareas, providing high volumes of nectar sugar throughoutthe year is key. Many other plant families in the fynbosprovide additional nectar resources for birds, but their rel-ative importance in sustaining birds requires attention.

ACKNOWLEDGMENTSWe would like to thank the Animal Demography Unit,University of Cape Town, especially Michael Brooks andRene Navarro, for use of the SABAP data in this studyand Willem Augustyn for assistance with nectar

FIGURE 4 Mean species floral abundance per month for (a) the western and (b) the eastern Cape Floristic Region, from the Protea

Atlas Project (n = 98,575 plots). Floral abundances are shown for all bird-visited Proteaceae species together (n = 71 species; n = 77 taxa), as

well as for each genus separately (Protea, Leucospermum and Mimetes have 35, 23, and 13 species, respectively; Appendix B). Error bars

indicate the standard error

GEERTS ET AL. 11

measurements. We thank Protea Atlassers for the plantdata. A. C. was funded by the Botanical Education Trustand the South African National Research Foundation(NRF) grant 88553. S. G. was funded by the NRF (grant115093) and a CPUT University Research Grant. TheNRF accepts no liability for opinions, findings and con-clusions or recommendations expressed in thispublication.

AUTHOR CONTRIBUTIONSSjirk Geerts, Anina Coetzee, Tony Rebelo, and AntonPauw conceived and designed the experiments. SjirkGeerts and Anina Coetzee performed the experiments.Sjirk Geerts, Anina Coetzee, and Anton Pauw analyzedthe data. Sjirk Geerts and Anina Coetzee wrote the man-uscript; other authors provided editorial advice.

ORCIDSjirk Geerts https://orcid.org/0000-0003-0149-2783Anina Coetzee https://orcid.org/0000-0002-1646-557X

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SUPPORTING INFORMATIONAdditional supporting information may be found onlinein the Supporting Information section at the end of thisarticle.

How to cite this article: Geerts S, Coetzee A,Rebelo AG, Pauw A. Pollination structures plantand nectar-feeding bird communities in Capefynbos, South Africa: Implications for theconservation of plant–bird mutualisms. EcologicalResearch. 2020;1–19. https://doi.org/10.1111/1440-1703.12148

GEERTS ET AL. 15

APPENDIX A

A list of all 1 ha plot field sites where the following datawas collected in the south west of the Cape Floristic

Region, South Africa. All sites were sampled duringMay–July 2007. This only includes bird-pollinated speciesin the genus Protea. For the non-Protea plots there wereno bird-pollinated Protea species flowering during the

Site

Vegetationwith orwithoutfloweringbird-pollinatedProteaceae

Vegetationage (years)

Number ofnectar-feedingbird speciesobserved

Nectar-feeding birdabundance

CapeSugarbirdpresence

Totalsugar (g)hectare GPS coordinates

Kogelberg 1 Protea 20 3 5 Yes 9,616.30 34�20062.000S 18�55090.700E

Kogelberg 2 Protea 7.5 2 3 Yes 753.82 34�20071.700S 18�55058.000E

Buffelslaagte Protea 1 0 0 No 0 34�18083.700S 18�49068.000E

Helderberg nature reserve 1 Protea 12 2 5 Yes 29,687.83 34�02069.300S 18�52026.900E

Helderberg nature reserve 2 Protea 2 0 0 No 0 34�02074.200S 18�52008.000E

Table mountain pipe track Protea 1 0 0 No 0 33�57010.800S 18�3063.700E

Table mountain cable car Protea 1 1 2 No 0 33�57013.900S 18�24084.000E

Kogelberg Harold Porter 1 Protea 8 2 4 Yes 99.27 34�20071.700S 18�55058.000E

Paarl mountain, monument Protea 12 3 5 Yes 1,793.41 33�45056.500S 18�56075.200E

Cape point Protea 11 2 3 Yes 3,295.81 34�15071.000S 18�27042.500E

Redhill 1 Protea 11 3 6 Yes 3,085.44 34�13012.900S 18�24082.500E

Du Toitskloof pass 1 Protea 9 2 4 Yes 2,693.20 33�44087.800S 19�04019.800E

Du Toitskloof pass 2 Protea 3 1 2 No 0 33�44086.400S 19�04019.400E

Du Toitskloof pass 3 Protea 5 2 3 Yes 1,314.91 33�43002.200S 19�05003.600E

Franschoek Villiersdorp road Protea 1.5 0 0 No 0 33�55074.300S 19�09060.100E

Jonkershoek fire break Protea 2 1 1 No 5.08 33�59016.700S 18�57007.700E

Jonkershoek Swartboskloof Protea 6 3 8 Yes 3,434.03 33�59015.400S 18�57011.100E

Jonkershoek Panorama trail Protea 4.5 2 6 Yes 4,808.13 33�59032.500S 18�58036.300E

East of Kleinmond Protea 6 3 7 Yes 2,332.34 34�19045.900S 19�01085.900E

Paarl mountain Protea 12 1 2 No 4.21 33�44017.900S 18�57019.200E

Theewaterskloof dam 1 Protea 15 2 3 Yes 361.21 –

Theewaterskloof dam 2 Protea 20 2 2 Yes 125.64 –

Jonkershoek 1 Protea 12 3 3 Yes 502.55 –

Redhill 2 Non-protea 2 1 1 No 0 34�11029.700S 18�23065.200E

Redhill 3 Non-protea 3 2 2 No 0 34�11022.900S 18�23076.000E

Redhill 4 Non-protea 5 1 1 No 0 34�11008.700S 18�23086.200E

Scarborough Non-protea 3 1 3 No 4.47 34�11084.300S 18�22083.600E

Kogelberg Harold porter 2 Non-protea 8 1 6 No 32.77 34�20062.000S 18�55090.700E

Kogelberg Harold porter 3 Non-protea 8 1 2 No 3.62 34�20080.600S 18�55077.400E

West of Kleinmond Non-protea 5 1 3 No 16.35 34�20023.600S 18�59075.600E

Cape Point road Restio Non-protea 11 1 1 No 0 34�14031.400S 18�25023.200E

Cape Point road Leucadendron Non-protea 11 1 1 No 0 34�14022.700S 18�25017.900E

Helshoogte Non-protea 12 1 1 No 0 33� 55040.200S 18�54065.900E

Jonkershoek 2 Non-protea 8 0 0 No 0 –

16 GEERTS ET AL.

study period; veld either too young, bird-pollinated Pro-tea species absent or not flowering. The sugar values fromnon-Protea vegetation are from Erica species. GPS coordi-nates were not recorded for all sites.

APPENDIX B

List of Proteaceae species classified as bird pollinated(or at least partly bird pollinated) and their Red Liststatus.

Species IUCN category

Totalnumberof species

Leucospermum catherinaeCompton

Endangered

L. conocarpodendronconocarpodendron (L.)Buek

Endangered

L. conocarpodendronviridum Rourke

Near threatened

L. cordifolium (Salisb. ExKnight) Rourke

Near threatened

L. cuneiforme (Burm.f)Rourke

Least concern

L. erubescens Rourke Rare

L. formosum (Andrews)Sweet

Endangered

L. fulgens Rourke Critically endangered

L. glabrum Phill. Endangered

L. grandiflorum (Salisb.) R.Br.

Endangered

L. gueinzii Meisn. Endangered

L. lineare R.Br. Subsplineare

Vulnerable

L. mundii Meisn. Rare

L. oleifolium (Bergius) R.Br. Least concern

L. patersonii Phill. Vulnerable

L. pluridens Rourke Near threatened

L. praecox Rourke Vulnerable

L. praemorsum (Meisn.)Phill.

Vulnerable

L. profugum Rourke Endangered

L. reflexum Rourke Near threatened

L. spathulatum R.Br.Cedarberg form

Near threatened

L. spathulatum R.Br.Keerom form

Near threatened

(Continues)

Species IUCN category

Totalnumberof species

L. truncatum (Buek. exMeisn.) Rourke

Least concern

L. tottum var. glabrum Critically endangered

L. tottum (L.) R.Br var.tottum

Near threatened

L. vestitum (Lam.) Rourke Near threatened 23 (26 taxa)

Mimetes arboreus Rourke Endangered

M. argenteus Salisb. ex Kn. Endangered

M. capitulatus R.Br. Endangered

M. chrysanthus Rourke Vulnerable

M. cucullatus (L.) R.Br. Least concern

M. fimbriifolius Salisb. ex Kn. Rare

M. hirtus (L.) Salisb. ex Kn. Vulnerable

M. hottentoticus Phill &Hutch.

Critically endangered

M. palustris Salisb. ex Kn. Critically endangered

M. pauciflorus R.Br. Vulnerable

M. saxatilis Phill. Endangered

M. splendidus Salisb. ex Kn. Endangered

M. stokoei Phill. & Hutch. Critically endangered 13 (13 taxa)

Protea aristata Phill. Vulnerable

P. aurea aurea (Burm.f)Rourke

Least concern

P. aurea potbergensisRourke

Near threatened

P. burchellii Stapf Vulnerable

P. convexa Phill. Critically endangered

P. compacta R.Br. Near threatened

P. coronata Lam. Near threatened

P. cynaroides (L.) L. Least concern

P. denticulata Rourke Rare

P. eximia (Salisb. ex Kn.)Four.

Least concern

P. glabra Thunb. Least concern

P. grandiceps Tratt. Near threatened

P. holosericea (Salisb. exKn.) Rourke

Endangered

P. inopina Rourke Vulnerable

P. lacticolor Salisb. Endangered

P. lanceolata Meyer exMeisn.

Least concern

P. laurifolia Thunb. Least concern

P. lepidocarpodendron (L.)L.

Near threatened

(Continues)

GEERTS ET AL. 17

APPENDIX C

Location and nectar amount for Protea and Erica specieswithin the 1 ha plots in the southwestern Cape FloristicRegion, South Africa.

Species IUCN category

Totalnumberof species

P. longifolia Andrews Vulnerable

P. longifolia minor Not assessed

P. lorea R.Br. Near threatened

P. lorifolia (Salisb. ex Kn.)Fourc.

Least concern

P. magnifica Link Least concern

P. mundii Klotzsch Least concern

P. neriifolia R.Br. Least concern

P. nitida Miller Least concern

P. nitida dwarf Miller Not assessed

P. obtusifolia Buek exMeisn.

Near threatened

P. pendula R.Br. Least concern

P. pityphylla Phill. Near threatened

P. pudens Rourke Endangered

P. repens (L.) L. Least concern

P. rupicola Mund ex Meisn. Endangered

P. speciosa L. Least concern

P. stokoei Phill. Endangered

P. susannae Phill. Near threatened

P. venusta Compton Endangered

P. witzenbergiana Phill. Least concern 35 (38 taxa)

Site Plant species

Nectar sugar mgper flower (Erica)or perinflorescence(Protea) (SD)

Nectar volume(μl) perflower (Erica)or perinflorescence(Protea) (SD)

Nectar concentration(Brix% sucroseequivalent)per flower (Erica)or perinflorescence(Protea) (SD)

Inflorescencessampled(total numberof flowers)

Kogelberg HaroldPorter 2 and 3

Erica coccinea 0.02 (0.06) 0.05 (0.16) 35 – (10)

Scarborough E. abietina 0.08 (0.18) 0.52 (1.07) 15.5 (0.7) – (10)

West of Kleinmond E. perspicua 0.49 (0.15) 1 (0.5) 28.67 (7.6) – (7)

Scarborough E. plukenetii 0.05 (0.13) 0.62 (1.34) 7.5 (3.5) – (10)

Paarl mountainmonument

Protea burchelli 113.25 (–) 387 (–) 25.7 (2.8) 1 (10)

East of Kleinmond P. compacta 388.72 (192) 1,474 (728) 11.6 (3.4) 2 (19)

18 GEERTS ET AL.

Site Plant species

Nectar sugar mgper flower (Erica)or perinflorescence(Protea) (SD)

Nectar volume(μl) perflower (Erica)or perinflorescence(Protea) (SD)

Nectar concentration(Brix% sucroseequivalent)per flower (Erica)or perinflorescence(Protea) (SD)

Inflorescencessampled(total numberof flowers)

Helderberg naturereserve

P. coronata 852.90 (307) 3,041 (1,043) 25.1 (1.4) 2 (24)

Paarl mountain P. laurifolia 146.72 (99) 572 (461) 23.2(6.9) 2 (27)

Du Toitskloof 1 and 3 P. laurifolia 282.54 (99) 937 (308) 24.6 (8.1) 18 (238)

KogelbergHarold Porter 1

P. lepidocarpodendron 49.64 (6) 196 (29) 22.4 (3.9) 2 (20)

Cape Point P. lepidocarpodendron 175.31 (80) 684 (109) 23.3(5.2) 3 (30)

Kogelberg 1 P. mundii 39.28 (–) 131 (–) 26.50 (2.1) 1 (10)

Scarborough Mimetes fimbriifolius 0 Traces – 3 (15)

Du Toitskloof pass 1 P. repens 314.09 (93) 2,296 (797)a 11.9 (6.0)a 5 (41)

Jonkershoek Swartboskloof P. neriifolia 801.35 (476) 2,739 (1,632) 26.8 (3.9) 23 (291)

Jonkershoek fire break P. nitida 33.44 (39) 122 (116) 29.3 (14.5) 4 (40)

aNectar in-between flowers (pool nectar) included.

GEERTS ET AL. 19