Received: 10 April 2020 Revised: 22 April 2020 Accepted: 3 May 2020 DOI: 10.1111/1440-1703.12148

ORIGINAL ARTICLE

Pollination structures and nectar-feeding communities in Cape , : Implications for the conservation of plant–bird mutualisms

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

1Department Conservation and Marine Sciences, University of Abstract Technology, Cape Town, South Africa With the current global concerns about pollinators, relationships between spe- 2DST/NRF Centre of Excellence at the cies interactions and diversity are pivotal. If pollinator communities depend FitzPatrick Institute of African strongly on the diversity of flowering and vice versa, anthropogenic Ornithology, University of Cape Town, Cape Town, South Africa influences—whether positive or negative—on one partner will cause changes 3South African National Biodiversity in the other. Here we ask whether nectarivorous bird communities are struc- Institute, Kirstenbosch Research Centre, tured by resource abundance ( nectar) or Proteaceae diversity at dif- Claremont, South Africa ferent spatial scales in the Cape fynbos of South Africa. On a small spatial 4Department of Botany and Zoology, Stellenbosch University, Matieland, scale, we sampled 34 one-hectare plots across the (CFR) South Africa for flowering Proteaceae species, number of , nectar volume, veg- etation age, nectar-feeding bird abundance and species richness. At small Correspondence Sjirk Geerts, Department Conservation scale, nectar—rather than vegetation structure or plant community and Marine Sciences, Cape Peninsula composition—was the most strongly correlated to nectar-feeding bird diversity University of Technology, P.O. Box and abundance. On a landscape scale we investigated the spatio-temporal 652, Cape Town 8000, South Africa. Email: [email protected] flowering patterns of ornithophilous Proteaceae throughout the CFR. Similar flowering patterns—with a winter floral abundance peak—were found Funding information CPUT University Research Grant; throughout the region, but , and showed com- South African National Research plementary flowering periods. At large spatial scales ornithophilous Proteaceae Foundation (NRF), Grant/Award species richness is strongly correlated—more so than plant or floral Numbers: 115093, 88553; Botanical — Education Trust 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.

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

1 | INTRODUCTION

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

Ecological Research. 2020;1–19. wileyonlinelibrary.com/journal/ere © 2020 The Ecological Society of Japan 1 2 GEERTS ET AL. species richness at a community level the CFR. They therefore play a disproportionally impor- (Biesmeijer et al., 2006; Kleijn et al., 2004; Potts, 2003; tant role in maintaining the large number of bird- Steffan-Dewenter & Tscharntke, 2001). In general, these pollinated plant species at the Cape, which comprises plant–pollinator networks have a robust structure about 4% of the total plant species (Rebelo, 1987). This sys- (Fortuna & Bascompte, 2006; Memmott, Waser, & tem is thus highly asymmetrical, which is in contrast with Price, 2004) and only under high disturbance pressures do bird-pollination systems in other parts of the world which these networks reach a tipping point (Memmott involve many more bird species. Despite this, the interac- et al., 2004; Potts et al., 2010). Globally pollinators are tion specialization is similar between sunbird–flower and influenced by human activities in a variety of ways hummingbird–flower communities (Bond, 1994; Brown & (Bond, 1994; Geerts & Pauw, 2011a; Geerts & Bowers, 1985; Feinsinger, 1978; Geerts & Pauw, 2009; Pauw, 2011b; Kearns, Inouye, & Waser, 1998; Lindberg & Hockey, Dean, & Ryan, 2005; Zanata et al., 2017). Further- Olesen, 2001). Therefore, it is not surprising that one off more, the CFR is a fire-adapted ecosystem and pollinator the main focus areas of plant–pollinator studies is to communities are influenced by the successional stage of understand what determines and alters their community plant communities and thus the frequency of fires (van composition (Cameron, 1999; Fleming & Muchhala, 2008; Wilgen et al., 2010). Fox & Hockey, 2007; Schmid et al., 2015). From a landscape scale perspective, the nectar-feeding Theshifttowardamoreinclusivecommunity-wide bird community in the CFR is an ideal system, since exten- approach (Pauw & Stanway, 2015; Sargent & Ackerly, 2008; sive information is available in the form of bird atlas data. Stanton, 2003)—rather than species specific pair-wise From the plant community perspective, the Proteaceae is interactions—enables a better evaluation of environmental an ideal study system since other than the extensive infor- changes since more connections in the plant–pollinator mation available (Protea AtlasProject;Rebelo,2006), community are considered. The dependence of individual Proteaceae are the dominant overstorey species in most fyn- species in pollinator communities will change with changes bos communities (Vlok & Yeaton, 1999), contain many in particular components of the pollinator network. For pol- bird-pollinated species (Rebelo, 1987) and provide abundant linators, impacts will be determined by nest site availability, nectar (Calf, Downs, & Cherry, 2003; Geerts, 2011). predation, disease or territoriality (Burd, 1995; Skead, 1967). Although parts of the biome (southwestern Cape) and a Forplants,theimpactwilldependonthedegreeofdepen- subset of Proteaceae species (19) have been studied in rela- dence on pollinators for seed set, degree of pollinator speci- tion to nectar availability, here we present data on the ficity and the degree of dependence on seeds for population entire biome and include all bird-pollinated Proteaceae persistence (Bond, 1994). The currency is nectar, which (Nottebrock et al., 2017; Schmid et al., 2015, 2016). plays an important role in plant–pollinator interactions Of the 330 Proteaceae species occurring in the CFR, (Heinrich, 1975; Heinrich & Raven, 1972). In particular, approximately 25% are potentially pollinated by nectar- since foraging movements of pollinators—and more so feeding , with the Cape a particularly impor- larger pollinators such as birds—are influenced by the het- tant pollinator (Collins, 1983; Fraser, 1989; Fraser & erogeneous spatial distribution of nectar (Ghazoul, 2005). McMahon, 1992; Martin & Mortimer, 1991; Mostert, Sieg- Nectar-feeding bird pollinators occur mostly in the Neotrop- fried, & Louw, 1980; Pauw & Johnson, 2017; Skead, 1967). ics, Australasia and the Afrotropics (Pauw, 2019). In Africa, DespiteProteaceaebeingsuch an important component of sunbirds and are the dominant vertebrate polli- the CFR vegetation, relatively few comprehensive polli- nators (see, e.g., Fleming & Muchhala, 2008). Together with nation studies have been conducted on avian pollination this, a wealth of bird data is available in South Africa (the in this family (Collins, 1983; Collins & Rebelo, 1987; South African Bird Atlas Project). Despite this, the extent to Johnson, 2015; Schmid et al., 2015; Wright, Visser, which nectarivorous bird communities are structured by Coetzee, & Giliomee, 1991). About half of the resource abundance or resource composition at different ornithophilous Proteaceae are non-resprouting and spatial scales in South Africa has received limited attention. when adult plants are killed by fire the next generation Add to this the detailed dataset available for the huge diver- grows from seeds, resulting in stands of similar aged sity and abundance of nectar rich Proteaceae in the Cape plants. Proteaceae are relatively slow to mature and only fynbos and it presents an ideal study system to address start to flower abundantly 4–5 years after a fire these questions (Rebelo, 2006). (Cowling, 1992). Most South African Proteaceae—but Pollinators are thought to be important in the origin less so for Leucospermum—are dependent on pollen and maintenance of the Cape's floral diversity, but the vectors—since they are self-incompatible and set no via- specialist nectar-feeding bird community in the Cape Flo- ble seed when pollinators are excluded (Collins & ristic Region (CFR) is a relatively simple one with only Rebelo, 1987; Horn, 1962; Johnson, 2015; Schmid four nectar-feeding bird species that occur throughout et al., 2015). GEERTS ET AL. 3

In this study, we ask whether nectarivorous bird com- are pollinated by birds, but Protea angustata was excluded munities are structured by resource abundance or (Johnson, 2015; Rebelo, 2001; S. Steenhuisen, personal com- resource composition at (a) the plot and (b) landscape munication). In addition, all species that are specifically scale and (c) whether flowering phenology varies by mentioned to have a yeasty odor or pollinated by wasps region. were excluded (Rebelo, 2001). We also excluded all hybrids. Based on this, only the genera Mimetes, Leucospermum and Protea contain potentially bird-pollinated species. 2 | METHODS These include 35 Protea,23Leucospermum and 13 Mimetes species (Appendix B). 2.1 | Study area The four nectar specialist bird species resident in the CFR are the (Promerops cafer L.), We obtained Proteaceae ecological data and distribution Orange-breasted Sunbird (Anthobaphes violacea L.), Mal- data for the CFR from the Protea Atlas Project database achite Sunbird (Nectarinia famosa L.) and Southern and bird distribution and abundance data for the CFR Double-collared Sunbird (Cinnyris chalybeus L.). The first from the South African Bird Atlas Project 2 database. two species are endemic to the CFR and largely confined Data for the Cape fynbos were extracted by clipping the to Fynbos vegetation (Hockey et al., 2005). All four spe- datasets with the Cape boundary GIS layer derived from cies have long, curved bills adapted to drink from tubular the Cape Action for People and Environment project flowers (Skead, 1967). Proteaceae nectar is critical for— (CAPE). Spatial data were projected to the WGS 1984 and determines the site scale visitation of—nectar feed- geographic coordinate system. Spatial analyses were con- ing birds (Carlson & Holsinger, 2013; Nottebrock ducted in ArcMap 10.3 (ESRI ArcMap 2010). On a et al., 2017; Rebelo et al., 1984). In particular, since nec- smaller scale, 34 one-hectare plots were sampled across tar-feeding birds breed in winter, when nectar resources the southwestern Cape for nectar-feeding birds, nectar from Proteaceae are at a maximum (Skead, 1967). and vegetation characteristics (Appendix A).

2.3 | Protea nectar quantification 2.2 | Study species The genus Protea frequently dominate the overstorey of We compiled a list of all Proteaceae species within the fynbos shrublands (Collins & Rebelo, 1987) and being CFR that conform to the bird-pollination syndrome. such an ecological important genus in the fynbos it is Proteaceae species that are visited by nectar-feeding birds thus well suited for studying plant–pollinator interactions have brush-type inflorescences with morphological adap- (Schurr, Esler, Slingsby, & Allsop, 2012). Leucospermum tations for bird-pollination described in detail in Rebelo, and also provide nectar sources for pollina- Siegfried, and Crowe (1984). We based our list on the tors but rarely co-flower with Protea (Collins & available Proteaceae pollination studies (Biccard & Rebelo, 1987) and no Leucospermum were flowering at Midgley, 2009; Coetzee & Giliomee, 1985; Collins, 1983; our study sites, while Erica produces insignificant Collins & Rebelo, 1987; Horn, 1962; Johnson, 2015; amounts of nectar compared to Protea (Heystek, Geerts, Lamont, 1985; Mostert et al., 1980; Pauw & Johnson, 2017; Barnard, & Pauw, 2014). To determine the effect of nectar Pauw & Stanway, 2015; Schmid et al., 2015; Seiler & availability on bird communities, nectar was sampled at Rebelo, 1987; Whitehead, Giliomee, & Rebelo, 1987; all study sites that contained bird-pollinated plant spe- Wiens et al., 1983; Wright, 1994; Wright et al., 1991) but cies. Inflorescences were collected early in the morning with a number of species not assessed for bird-pollination, and nectar was extracted in the laboratory using either a we subsequently selected species according to the follow- 5 μLora40μL capillary tube (Drummond Scientific ing morphological criteria that are likely to indicate bird Company, Broomall, PA). Nectar concentrations were pollination (Rebelo, 2001): For the genera Mimetes and determined with a 0–50% field handheld refractometer Protea, species that bore inflorescences >20 cm above gro- (Bellingham and Stanley, Tunbridge Wells, UK). und level and have flower styles longer than 25 mm. For In Protea inflorescences the outer ring of flowers Leucospermum we considered species that bore inflores- mature first and then the inner rows mature consecu- cences >20 cm above ground level and with styles longer tively. Nectar for a row of open flowers (n ≈ 14) across than 35 mm as these larger flower heads are typically bird- the middle of the (as seen from above) was pollinated (Rebelo, 2001). For the group of flat pincush- measured, which effectively samples flowers of all ages in ions (styles less than 35 mm), L. mundii (Meisn.) and the inflorescence. This largely controls for variation in L. oleifolium ((Bergius) R.Br.) were also included as they nectar volume between the different aged flowers in an 4 GEERTS ET AL. inflorescence, without measuring nectar for all the above, with the following addition: In open cup shaped 200–250 flowers. Protea species (e.g., ), nectar in the inter- The average standing crop of nectar volume and con- floral pool between the flowers was also measured. The centration per flower was then calculated and multiplied only other flowering bird-pollinated species were Erica by the total number of flowers in the inflorescence. spp.—which are closely associated with the Orange- Standing crop provides an accurate estimate of the nectar breasted Sunbird (Heystek et al., 2014)—in which nectar available to pollinators at a given time (collection was was measured from individual flowers. To obtain nectar done early morning when birds are most active) sugar per hectare the number of inflorescences (Protea) (Kearns & Inouye, 1993). In contrast, total nectar produc- or flowers (Erica) was counted in the study plot and mul- tion over the lifetime of a single flower or inflorescence is tiplied by the amount of nectar sugar. an important measurement from a plant's perspective, Ten-minute bird counts were conducted within the but is less relevant to pollinators. All nectar measure- 1-ha plots by standing on a ladder and recording all ments were transformed to milligrams (mg) of nectar nectar-feeding birds heard or seen within a 25 m radius sugar (sucrose equivalents). (Bibby, Burgress, Hill, & Mustoe, 2000; Dawson & Bull, 1975). During a pilot study, counts were conducted for 1 hr each at three sites. Nectar-feeding bird species 2.4 | Plant–pollinator communities at a richness and abundance was found to reach a plateau small scale after 10 min of observation. Although short, this was suf- ficient to detect nectar-feeding birds, since they are terri- Birds are well known to respond to vegetation structure. torial in winter, conspicuous and have a clearly Therefore, to test whether vegetation structure (post-fire distinguishable call. Before counts were conducted, a set- age and plant community composition) or nectar avail- tling period of 15 min was allowed. All sites were sam- ability best explains variation in bird species richness and pled once between May–July 2007. Bird counts were abundance, vegetation of different post-fire ages, known done early in the morning when nectar-feeding birds are as a chrono-sequence, was sampled (Foster & most active; rainy and very windy days were avoided Tilman, 2000). To determine the effect of nectar availabil- (Fry, 2000). ity in different plant communities, areas containing Proteaceae, Ericaceae and Restionaceae communities of different vegetation ages, were sampled. All bird- 2.5 | Plant–pollinator community pollinated plant species were sampled. To improve sam- patterns on a landscape scale ple size for statistical analysis, plant communities were divided into Protea-dominated (Proteoid Fynbos) and To test if nectarivorous bird communities are structured by non-Protea (mainly Restioid, Ericaceous and Asteraceous resourceabundanceorresourcecompositionatthebiome Fynbos) vegetation. This is justified as Protea contributed scale, nectar-feeding bird distribution data was overlaid almost all, or all nectar, since no flowering bulbs and with species richness and abundance of ornithophilous only a few Erica scrubs were present in the plots. For Proteaceae. Nectar-feeding bird distribution data were 34 one-hectare plots across the southwestern Cape we obtained from the second South African Bird Atlas Project recorded the following variables at each site within a sin- (SABAP2) database. Bird occurrences were recorded by vol- gle day: vegetation age, number of flowering bird- unteers since July 2007, and data collected until October pollinated Proteaceae species, number of Proteaceae indi- 19, 2017 were used in this study. Records of species occur- viduals and inflorescences, amount of nectar and nectar- rences were collected as checklists in grids with a pentad feeding bird richness and abundance (Appendix A). All resolution: 50 × 50 (approximately 8 × 8km).Weonlyused sites were sampled between May and July 2007. Post-fire grid cells with four or more checklists (n = 788 cells), which vegetation age was obtained from local experts or esti- produced a range of 5 to 1,134 (average 26) checklists per mated by counting the number of internodes (new inter- cell. Reporting rates (number of times a species was nodes form annually) on the tallest stem of five recorded in a grid cell as a proportion of the total checklists individuals of a non-sprouting Proteaceae species, with for the cell) from repeated visits to sites can be used as an the mode accepted as the true age (Lamont, 1985; van estimate of the abundance of a species at a location der Merwe, 1969). (Underhill, Oatley, & Harrison, 1991). For the calculation of nectar availability, all bird- Although the SABAP reporting rates are not always pollinated (i.e., Protea and other species) plants in the directly proportional to bird abundance (Harrison, Allan, 1-ha plots were identified. Nectar for Protea was deter- Underhill, et al., 1997), it has been evaluated previously, mined as described in the nectar quantification method and found to correspond well to other field data and GEERTS ET AL. 5 considered fit for use in general population studies flowering data for a species were combined and the cal- (Fairbanks, Kshatriya, van Jaarsveld, & Underhill, 2002). culation of floral abundance per month was extrapolated Factors that will influence the accuracy of SABAP data in to all the plants of a species, which assumes relative uni- our study are that mountaintops are not well sampled, formity of flowering patterns across the fynbos biome. grid cells with a small fraction of fynbos habitat might The proportional floral abundance per month was calcu- have biased reporting rates of fynbos specialist birds lated as a proportion of all records: (Huntley, Altwegg, Barnard, Collingham, & Hole, 2012), BUD OVER and females, juveniles and individuals in eclipse plumage 4 + PEAK + FLOWER + 2 can be more difficult to identify (Harrison et al., 1997). BUD + PEAK + FLOWER + OVER + CONE + NONE However, this study only compares abundances within species, which is appropriate for this type of data BUD was divided by four since about three quarters of (Underhill, Prys-Jones, Harrison, & Martinez, 2008). the plants have only very few plants actually in flower. The Protea Atlas Project (PAP) (http://protea. Likewise, when a population was classified as OVER, worldonline.co.za) collected distribution data on south- only half of the plants were bearing open flowers. In ern African Proteaceae in 500 m diameter plots during some cases, no flowers may have been recorded because 1991–2002 (Rebelo, 2006). Although the PAP and SABAP of a recent fire and plants were not mature enough to data were not collected during the same time period, flower yet. However, most data were collected in Proteaceae are long-lived plants, particularly resprouting mature veld. species, and their abundances and distribution at the land- The locational floral abundance of a species was cal- scape scale can remain constant for 30 years (Privett, culated by multiplying the proportional floral abundance Cowling, & Taylor, 2001), barring disturbances such as for a given month with the population abundance of the land-use change and fires, which would have affected given location. In order to compare the bird and plant birds similarly (Chalmandrier, Midgley, Barnard, & abundances, the Protea Atlas point data were converted Sirami, 2013). Furthermore, both surveys were done over to grid data of the same resolution as the SABAP2 data so 10 year periods and therefore captured the average dynam- that each grid cell represents the mean floral abundance ics that occur at each site. During PAP, ecological data of ornithophilous Proteaceae of all plots in the grid cell. was also collected, such as plant abundance and flowering Mean floral abundances and bird reporting rates are thus status, and we used the population codes recorded for esti- comparable estimates of abundances. For this analysis, mates of population abundances (Table S1). Distribution all phenological considerations were excluded and thus and flowering patterns of ornithophilous Proteaceae spe- the annual floral abundances per plot were used (the cies in the CFR were extracted from the database for a sum of the monthly abundances) and bird data were total of 101,047 plots. This includes accurate absence data pooled irrespective of the season of sampling. Species since 2,472 well-distributed fynbos plots contained no richness and mean plant abundance of all ornithophilous ornithophilous Proteaceae species at the time. Proteaceae (Protea, Leucospermum and Mimetes species) During PAP sampling, the flowering status of each were determined for each grid cell and combined. species in a plot was recorded based on the condition of the majority of inflorescences on all plants. Observers recorded the proportion of plants that fell into each of 2.6 | Floral spatio-temporal patterns on a the following six categories: In bud (BUD: majority of landscape scale flower heads in bud; a few may be open but fewer are over than are open), flowering (FLOWER: flower heads To explore whether Proteaceae flowering phenology varies either in bud or over predominate with some open; all by region we analyzed the floral spatio-temporal patterns three classes must be present), peak flowering (PEAK: of ornithophilous Proteaceae in the fynbos biome. For some flower heads in bud and over but with the majority each plot sampled, the total floral abundance was esti- open), over (OVER: majority of flower heads over; a few mated by adding up the floral abundance of all species in may be open, but fewer are in bud than are open), in the plot for a particular month. This is justified since spe- cone (CONE: all of the flower heads over with none open cies differed little in the number of inflorescences pro- or in bud and seed heads with seeds present on plant) duced per plant, since floral abundances and population and nothing (NONE: no flower heads visible either as in abundances are highly correlated (Spearman Rank correla- bud, open or over and seed heads absent or having tion: S =1,496,p < .0001). To investigate the spatial pat- released all their seeds; (Rebelo, 1991)). Since most plots terns, for this analysis only, the CFR was divided into were only sampled once, there is no complete phenologi- 29 subregions and the phenology pattern of each subre- cal data available for every location. Thus, all the gion was drawn. This division is based on the grouping of 6 GEERTS ET AL.

Proteaceae species into centers of endemism, which cluster 33.5 mg (±39 SD) per inflorescence in to on either the mountain ranges or within lowland basins 852 mg (±307 SD) nectar sugar per inflorescence in (Rebelo & Siegfried, 1990). Temporal patterns were investi- P. coronata (Appendix C). Bird species richness and gated by comparing the mean floral abundance in each abundance was best correlated to the amount of sugar month across the whole biome. Patterns for the different available (Table 1; Figure 1). The second most supported genera were also investigated separately. For these ana- model explaining bird species richness contained vegeta- lyses the Fynbos was divided into eastern and western tion age (Table 1). Nectar sugar varies with vegetation CFR as these areas differ in rainfall (western CFR is age and a threshold age of 4–5 years appears to be strictly winter rainfall, eastern CFR less so) and fire season required to produce sufficient nectar for nectar-feeding importance for serotinous Proteaceae (Rebelo, Boucher, bird species richness and abundance to obtain optimal Helme, Mucina, & Rutherford, 2006; van Wilgen, 2009). levels (Figure S1), with sugarbirds only present when Protea vegetation is at least 4 years old (Figure S3).

2.7 | Statistical analyses 3.2 | Plant–pollinator community To determine which variables best explain the species rich- patterns on a landscape scale ness and abundance of nectar-feeding birds at small and landscape scales, models were compared with Akaike Infor- Nectar-feeding bird species richness and the abundance of mation Criterion (AIC) scores and Akaike weights Cape Sugarbird (R2 = .25), Orange-breasted Sunbird (Burnham, Anderson, & Huyvaert, 2011) using the MuMIn (R2 = .26) and Malachite Sunbird (R2 =.04)wasbestcorre- package in R (Barton, 2012). The effect of the predictor vari- lated to Proteaceae species richness (Table 2; Figure 2), with ables on bird species richness (count data) and abundance nectar-feeding bird species richness closely matching (at small scale) was tested with generalized linear models ornithophilous Proteaceae speciesrichnessacrosstheregion (GLM) with a Poisson-error distribution. For the 1-ha plot (Figure 3, R2 = .09). Of all bird species, the Cape Sugarbird scale analyses, the following variables were assessed: (a) log and Orange-breasted Sunbird show the strongest relation- − nectar sugar ha 1 (mg), (b) presence of ornithophilous Pro- ships with Proteaceae richness (Figure 2). The abundance tea, (c) vegetation age (years), (d) ornithophilous Protea of Southern Double-collared Sunbird was best correlated to species richness, (e) number of ornithophilous Protea indi- Proteaceae plant abundance, but it was a very weak rela- viduals and (f) number of inflorescences. For the landscape tionship (Table 2, R2 = .002, p =1). scale analyses, three predictor variables were assessed: plant abundance, floral abundance and plant species richness (normalized and, since they were correlated, they were not 3.3 | Floral spatio-temporal patterns on a included in the same models). The effect on bird abun- large scale dances (reporting rate, which is proportional data) was tested separately for each bird species using generalized lin- Annual floral abundance across all ornithophilous ear mixed-effect models with binomial error distribution Proteaceae species showed a unimodal peak in the winter and an observational level random factor to account for (July–August), while lowest abundance was at the end of over dispersion (Browne, Subramanian, Jones, & summer (February–March; Figure 4). This winter peak in Goldstein, 2005). Marginal pseudo-R2 values were calcu- floral abundance was largely due to the hyper-abundant lated with the delta method for the most supported models Protea genus, since the flowering of Leucospermum and (Nakagawa, Johnson, & Schielzeth, 2017). Mimetes species peaked later in the year (Figure 4). All analyses were conducted in R (R Development Leucospermum and Mimetes had relatively high floral Core Team, 2012). abundances in spring (September–November) and, partic- ularly Leucospermum, in mid-summer, when Protea floral abundances was at its lowest. For the spatio-temporal pat- 3 | RESULTS tern across the fynbos, all subregions showed the same phenological pattern with a peak in winter (Figure S2). 3.1 | Plant–pollinator communities at small scales and nectar volumes 4 | DISCUSSION Nectar sugar availability in Protea vegetation ranged from 4 g to 29.688 kg in the 1 ha plots. The total sugar content Here we show that fynbos nectar-feeding bird richness of nectar varied greatly between Protea species, from and abundance is correlated to resource abundance at GEERTS ET AL. 7

TABLE 1 Variables that explain Model KL AICc ΔAICc wi the species richness and abundance of nectar-feeding birds at small scale (1 ha, Bird species richness n = 32) in the southwestern section of Nectar sugar/ ha log (mg) 2 −38.86 82.14 0.000 0.970 the Cape Floristic Region of South Vegetation age 2 −43.05 90.51 8.371 0.015 Africa 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 of parameters (K), log likelihood (L), Akaike Information Criterion (AICc), difference in AICc from the best model and the Akaike weight (wi) is presented.

the community scale and by resource diversity at a biome scale. This implies that these resources contribute to structuring nectar-feeding bird communities. We show that at an 1 ha scale the underlying mechanism linking nectar-feeding bird communities to ornithophilous Proteaceae communities is nectar abundance—rather than structural changes in vegetation height associated with large Proteaceae (Table 1). Bird numbers showed a rapid increase with an increase in vegetation age (Figure S1). This further highlight that there is not a gradual increase in vegetation height and structure that links bird and Proteaceae communities, but rather a sud- den availability of nectar when ornithophilous Proteaceae start flowering. Geerts, Malherbe, and Pauw (2012) showed that vegetation age is important for nectar-feeding birds and that even in recently burned vegetation where bird-pollinated bulbs are flowering, nectar-feeding bird numbers are low. Here we show that the underlying reason is sugar availability and although there is a correlation between vegetation age and nectar sugar, 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 enhanced FIGURE 1 The relationship between nectar sugar availability because there were no bird-pollinated bulbs flowering in in protea vegetation and nectar-feeding bird species richness (a) the study plots that would have flowered and attracted and abundance (b) at an 1 ha plot scale in the southwestern nectar-feeding birds. Also in our results, Erica species section of the Cape Floristic Region, South Africa only add an insignificant amount of nectar, with plots 8 GEERTS ET AL.

TABLE 2 Results of model Model KL AICc Δ AICc wi selection to determine whether Bird species richness Proteaceae species richness, floral Species richness 2 −1,531.07 3,066.16 0.000 1 abundance or plant abundance best Floral abundance 2 −1,560.44 3,124.89 58.727 0 explain the species richness and abundances of nectar-feeding birds in Plant abundance 2 −1,567.76 3,139.52 73.362 0 the Cape Floristic Region, of South − Null model 1 1,588.26 3,178.53 112.369 0 Africa 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 was used. For each model, the number of parameters (K), log likelihood (L), Akaike Information

Criterion (AICc), difference in AICc from the best model and the Akaike weight (wi)is presented. having few Erica bushes, and an Erica flower producing vegetation structure for nest sites or prey items (Siegfried & between 0.02 to 0.49 mg of nectar sugar per flower versus Crowe, 1983). Here we show that even if vegetation is 39–852 mg of sugar for a Protea inflorescence mature, without nectar sugar, most nectar-feeding birds will (Appendix C). However, Erica species are a particularly be absent. Similarly, when invasive alien plant species add critical nectar source for the Orange-breasted Sunbirds in structure, but lack nectar, nectar-feeding birds are absent areas with few Proteaceae and outside of the main (Mangachena & Geerts, 2017), while if invasive alien plant flowering time (i.e., winter and early spring) of bird- species add nectar to the landscape—but no structure—nec- pollinated Proteaceae (Rebelo et al., 1984). tar-feeding birds are common (Le Roux et al., 2020; Le Nectar-feeding birds are known to be more dependent Roux,Geerts,Ivey,etal.,2010).Nottebrocketal.(2017)did on ornithophilous Proteaceae than other avian guilds not consider vegetation structure per se, but also found that (De Swardt, 1993) and are some of the most abundant avian pollinator visitation strongly depends on site scale nectar fauna in mature Proteaceae vegetation. Other avian species sugar, which in turn influenced seed production. Interest- like the seed-eating Cape Turtle Dove (Streptopelia capicola ingly, at such small scales high nectar sugar can decrease Sundevall), and predators like the Common Fiscal (Lanius per-plant visitation rates due to oversupply and the collaris L.), also occur in high abundance in Proteaceae veg- resulting competition for pollinators (Schmid et al., 2015). etation (Winterbottom, 1964). But in contrast to nectar- On a larger scale, the abundance of three of the four feeders, these species are not dependent on nectar but on nectar-feeding species was best correlated with Proteaceae GEERTS ET AL. 9

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

species richness, more so than to floral or plant abundance species richness. Nonetheless, both data sets were collected (Table 2). This differs from hummingbird assemblages in over multiple years and therefore represent averages. The the Bolivian lowlands that are structured by floral abun- explanatory power of these models was relatively low, dances, rather than diversity, at local (1.5 km transect) likely because of the influence of abiotic factors—other and large scales (700 km) (see, e.g., Abrahamczyk & than mutualistic interactions—that will also affect species Kessler, 2010). The patterns observed in landscape level richness. For example, it is well known that Orange- correlations are generally influenced by spatial autocorre- breasted Sunbirds are uncommon in lowland areas and lation, and the same is likely to apply here. However, here prefer higher altitudes (Pauw & Louw, 2012). This, while we show several distinct and widely separated areas of sugar water feeders and indigenous garden plants can nectar and bird dearth (Figure 3). These, at least, represent increase nectar-feeding bird resources in an urban context independent observations, and certainly have very few, if (Coetzee, Barnard, & Pauw, 2018). Other abiotic factors, any, Proteaceae species in common. Proteaceae species such as temperature and rainfall also influence species have unusually small geographical ranges such that adja- richness, with fewer ornithophilous Proteaceae in the drier cent cells will often have a different community composi- and warmer west coast regions of the fynbos biome tion, contributing to the independence of observations. (Rebelo, 2006). The SABAP data was collected later than the PAP data Cape Sugarbirds and Orange-breasted Sunbirds show and since Proteaceae community composition is more con- the strongest relationships with Proteaceae richness sistent over time than floral abundance, this may have (Figure 2). We suggest that this is not because resource contributed to the stronger correlation between birds and quantity is unimportant (Nottebrock et al., 2017), but 10 GEERTS ET AL.

mountain fynbos, being present in only 2 out of the 34 study plots—this despite most of the lowland fynbos being 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 agricultural areas (Hockey et al., 2005; Mangachena & Geerts, 2019; Pauw & Louw, 2012). Broadly, similar phenological patterns in Proteaceae flowering are found throughout the biome at the course scale sampled: a floral abundance peak in winter. Since floral abundances are generally low in all subregions at the same time of year, this points to the possibility that it may not be profitable for birds to migrate in search for nectar resources. A similar study on the flowering phenol- ogy of bird-visited Eucalyptus species in Australia propose that reliable and concordant flowering (flowering at the same time across sites and species) makes movements between sites by nectarivorous birds unlikely (Keatley & Hudson, 2007). In contrast, swift parrot migration in Australia might be linked to flowering of specific species such as Acacia pycnantha (Mac Nally & Horrocks, 2000; Saunders & Heinsohn, 2008). Furthermore, some hum- FIGURE 3 Species richness of (a) nectar-feeding birds, and mingbirds seem to track floral abundances (Cotton, 2007). 0 × 0 (b) bird-pollinated Proteaceae in the Cape Floristic Region (5 5 The overall temporal floral abundance patterns of spatial resolution, n = 788 grid cells). The location of the Cape Proteaceae are mainly due to the patterns of the species Floristic Region (enlarged maps) in South Africa is shown in grey rich and abundant Protea genus. Leucospermum and in the inset map Mimetes species contribute less to total abundances, except in the dry summer months when Protea flowering rather a result of the combination of the uniform spatio- is at its lowest. Thus, a diversity of Proteaceae may sus- temporal flowering patterns across the biome and com- tain nectar-feeding bird populations throughout the year plementary flowering of different genera for most of the within mountain ranges, particularly if birds are unable year. The differences in floral traits (such as reward to escape the summer nectar scarcity by moving across quantity and accessibility) between Proteaceae species mountain ranges because they show synchronous pat- may also contribute to this pattern. Data on geographical terns. In Costa Rica, sequential flowering of the domi- variation of phenology patterns within species were not nant bird-visited plant species, Hamelia, Inga and Lobelia analyzed in this study as the focus here was landscape provides abundant nectar for hummingbirds throughout scale. In particular, since most of the studied Proteaceae the year in one mountain range (Feinsinger, 1976; species have small distribution ranges, it is unlikely that Waser & Real, 1979). Likewise, the Australasian honey- phenology patterns of populations would differ at the eaters rely on a diversity of plant species for nectar coarse scale we used (i.e., monthly abundances). As for throughout the year (Collins & Briffa, 1982). The CFR the wide-spread species, their floral abundances are likely nectar-feeding birds may be foraging from plants of other overestimated (e.g., a species flowering in different sea- plant families (Feinsinger & Swarm, 1982) during the sons in the east and west of the region will appear to have nectar scarcity at the end of summer, but at this stage a long flowering period since we combined all records) there is too little data to provide insight into this. and yet we still see a clear pattern of low floral abun- The flowering of Leucospermum and Mimetes species dances in summer across the biome. Similar to Rebelo during times of low Protea floral abundance suggests et al. (1984), we found a weaker relationship between that the conservation of their diversity is important for and Malachite Sunbirds compared to Orange- the persistence of nectar-feeding birds and other polli- breasted Sunbirds, potentially due to Malachite Sunbirds' nators in the landscape. These genera are important use of other plant species (Geerts & Pauw, 2009). South- resources, and already under greater threat than Protea ern Double-collared Sunbirds were not strongly related to species. Of the 35 ornithophilous Protea species studied Proteaceae species richness or floral abundance (Table 2). here, 16 (46%) have a Red List status of conservation This species generally occurs in lower numbers in concern, whereas 8 of the 13 (62%) Mimetes species and GEERTS ET AL. 11

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

16 of the 23 (70%) Leucospermum species are of conser- particular nectar-feeding bird species could elicit changes vation concern, that is, near threatened, threatened, in bird-dependent plant communities. Protea reproduction endangered, or critically endangered (Appendix B; and bird pollinators are most likely linked through nectar www.redlist.sanbi.org). abundance (this study) and not floral signaling and acces- Many Proteaceae species are predicted to face range sibility traits (Schmid et al., 2015). contractions with a change in climate (Bomhard In conclusion, resource abundance contributes to et al., 2005). However, at least some species are known to shaping nectar-feeding bird communities at a small scale, be able to successfully grow outside their native range and while resource diversity—driven by different flowering could thus potentially move with climate change (Latimer, times for Protea, Mimetes and Leucospermum—are better Silander, Rebelo, & Midgley, 2009). More importantly, fre- correlatives at the landscape scale. This study thus high- quency of fire, which is likely to increase with climate lights the importance of community-wide conservation to change (IPCC, 2001), will reduce the extent of mature veg- preserve mutualistic relationships. From a restoration per- etation and the nectar available to the bird community spective, and to bring birds back into small conservation (Bond, Midgley, & Woodward, 2003; Geerts et al., 2012). areas, providing high volumes of nectar sugar throughout Within the nectar-feeding bird community, species differ the year is key. Many other plant families in the fynbos in their nectar requirements, with the large-bodied Cape provide additional nectar resources for birds, but their rel- Sugarbird needing substantial amounts (Collins, 1983) ative importance in sustaining birds requires attention. which can only be supplied by Proteaceae vegetation of at least 4 years in age (Figure S3). The probability of extinc- ACKNOWLEDGMENTS tion depends on the strength of the pollinator–plant mutu- We would like to thank the Animal Demography Unit, alism (Geerts, 2016; Geerts & Pauw, 2009). Since the University of Cape Town, especially Michael Brooks and nectar-feeding bird community plays an important role in Rene Navarro, for use of the SABAP data in this study shaping the plant community, a change in range of a and Willem Augustyn for assistance with nectar 12 GEERTS ET AL. measurements. We thank Protea Atlassers for the plant Burd, M. (1995). Pollinator behavioral-responses to reward size in data. A. C. was funded by the Botanical Education Trust Lobelia deckenii—No escape from pollen limitation of seed set. – and the South African National Research Foundation Journal of Ecology, 83(5), 865 872. Burnham, K. P., Anderson, D. R., & Huyvaert, K. P. (2011). AIC (NRF) grant 88553. S. G. was funded by the NRF (grant model selection and multimodel inference in behavioral ecol- 115093) and a CPUT University Research Grant. The ogy: Some background, observations, and comparisons. Behav- NRF accepts no liability for opinions, findings and con- ioral Ecology and Sociobiology, 65,23–35. clusions or recommendations expressed in this Calf, K. M., Downs, C. T., & Cherry, M. I. (2003). Foraging and ter- publication. ritorial behaviour of male Cape and Gurney's sugarbirds (Prom- erops cafer and P. gurneyi). African Zoology, 38, 297–304. AUTHOR CONTRIBUTIONS Cameron, A. (1999). The effects of fragmentation of vege- Sjirk Geerts, Anina Coetzee, Tony Rebelo, and Anton tation on bird community composition (M.Sc. mini-thesis). Uni- versity of Cape Town, Cape Town. Pauw conceived and designed the experiments. Sjirk Carlson, J. E., & Holsinger, K. E. (2013). Direct and indirect selec- Geerts and Anina Coetzee performed the experiments. tion on floral pigmentation by pollinators and seed predators in Sjirk Geerts, Anina Coetzee, and Anton Pauw analyzed a color polymorphic South African . Oecologia, 171, the data. Sjirk Geerts and Anina Coetzee wrote the man- 905–919. uscript; other authors provided editorial advice. Chalmandrier, L., Midgley, G. F., Barnard, P., & Sirami, C. (2013). Effects of time since fire on birds in a plant diversity hotspot. – ORCID Acta Oecologia, 49,99 106. Sjirk Geerts https://orcid.org/0000-0003-0149-2783 Coetzee, A., Barnard, P., & Pauw, A. (2018). Urban nectarivorous bird communities in Cape Town, South Africa, are structured Anina Coetzee https://orcid.org/0000-0002-1646-557X by ecological generalisation and resource distribution. Journal of Avian Biology, 49, e01526. REFERENCES Coetzee, J. H., & Giliomee, J. H. (1985). Insects in association with Abrahamczyk, S., & Kessler, M. (2010). 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APPENDIX A Region, South Africa. All sites were sampled during May–July 2007. This only includes bird-pollinated species A list of all 1 ha plot field sites where the following data in the genus Protea. For the non-Protea plots there were was collected in the south west of the Cape Floristic no bird-pollinated Protea species flowering during the

Vegetation with or without Number of flowering nectar- bird- feeding Nectar- Cape Total pollinated Vegetation bird species feeding bird Sugarbird sugar (g) Site Proteaceae age (years) observed abundance presence hectare GPS coordinates Kogelberg 1 Protea 20 3 5 Yes 9,616.30 3420062.000S1855090.700E Kogelberg 2 Protea 7.5 2 3 Yes 753.82 3420071.700S1855058.000E Buffelslaagte Protea 1 0 0 No 0 3418083.700S1849068.000E Helderberg nature reserve 1 Protea 12 2 5 Yes 29,687.83 3402069.300S1852026.900E Helderberg nature reserve 2 Protea 2 0 0 No 0 3402074.200S1852008.000E Table mountain pipe track Protea 1 0 0 No 0 3357010.800S183063.700E Table mountain cable car Protea 1 1 2 No 0 3357013.900S1824084.000E Kogelberg Harold Porter 1 Protea 8 2 4 Yes 99.27 3420071.700S1855058.000E Paarl mountain, monument Protea 12 3 5 Yes 1,793.41 3345056.500S1856075.200E Cape point Protea 11 2 3 Yes 3,295.81 3415071.000S1827042.500E Redhill 1 Protea 11 3 6 Yes 3,085.44 3413012.900S1824082.500E Du Toitskloof pass 1 Protea 9 2 4 Yes 2,693.20 3344087.800S1904019.800E Du Toitskloof pass 2 Protea 3 1 2 No 0 3344086.400S1904019.400E Du Toitskloof pass 3 Protea 5 2 3 Yes 1,314.91 3343002.200S1905003.600E Franschoek Villiersdorp road Protea 1.5 0 0 No 0 3355074.300S1909060.100E Jonkershoek fire break Protea 2 1 1 No 5.08 3359016.700S1857007.700E Jonkershoek Swartboskloof Protea 6 3 8 Yes 3,434.03 3359015.400S1857011.100E Jonkershoek Panorama trail Protea 4.5 2 6 Yes 4,808.13 3359032.500S1858036.300E East of Protea 6 3 7 Yes 2,332.34 3419045.900S1901085.900E Paarl mountain Protea 12 1 2 No 4.21 3344017.900S1857019.200E 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 3411029.700S1823065.200E Redhill 3 Non-protea 3 2 2 No 0 3411022.900S1823076.000E Redhill 4 Non-protea 5 1 1 No 0 3411008.700S1823086.200E Scarborough Non-protea 3 1 3 No 4.47 3411084.300S1822083.600E Kogelberg Harold porter 2 Non-protea 8 1 6 No 32.77 3420062.000S1855090.700E Kogelberg Harold porter 3 Non-protea 8 1 2 No 3.62 3420080.600S1855077.400E West of Kleinmond Non-protea 5 1 3 No 16.35 3420023.600S1859075.600E Cape Point road Restio Non-protea 11 1 1 No 0 3414031.400S1825023.200E Cape Point road Non-protea 11 1 1 No 0 3414022.700S1825017.900E Helshoogte Non-protea 12 1 1 No 0 33 55040.200S1854065.900E Jonkershoek 2 Non-protea 8 0 0 No 0 – GEERTS ET AL. 17

study period; veld either too young, bird-pollinated Pro- Total tea species absent or not flowering. The sugar values from number non-Protea vegetation are from Erica species. GPS coordi- Species IUCN category of species nates were not recorded for all sites. L. truncatum (Buek. ex Least concern Meisn.) Rourke L. tottum var. glabrum Critically endangered APPENDIX B L. tottum (L.) R.Br var. Near threatened tottum List of Proteaceae species classified as bird pollinated L. vestitum (Lam.) Rourke Near threatened 23 (26 taxa) (or at least partly bird pollinated) and their Red List status. Mimetes arboreus Rourke Endangered M. argenteus Salisb. ex Kn. Endangered M. capitulatus R.Br. Endangered Total M. chrysanthus Rourke Vulnerable number M. cucullatus (L.) R.Br. Least concern Species IUCN category of species M. fimbriifolius Salisb. ex Kn. Rare Leucospermum catherinae Endangered Compton M. hirtus (L.) Salisb. ex Kn. Vulnerable L. conocarpodendron Endangered M. hottentoticus Phill & Critically endangered conocarpodendron (L.) Hutch. Buek M. palustris Salisb. ex Kn. Critically endangered L. conocarpodendron Near threatened M. pauciflorus R.Br. Vulnerable viridum Rourke M. saxatilis Phill. Endangered L. cordifolium (Salisb. Ex Near threatened M. splendidus Salisb. ex Kn. Endangered Knight) Rourke M. stokoei Phill. & Hutch. Critically endangered 13 (13 taxa) L. cuneiforme (Burm.f) Least concern Rourke Protea aristata Phill. Vulnerable L. erubescens Rourke Rare P. aurea aurea (Burm.f) Least concern Rourke L. formosum (Andrews) Endangered Sweet P. aurea potbergensis Near threatened Rourke L. fulgens Rourke Critically endangered P. burchellii Stapf Vulnerable L. glabrum Phill. Endangered P. convexa Phill. Critically endangered L. grandiflorum (Salisb.) R. Endangered Br. P. compacta R.Br. Near threatened L. gueinzii Meisn. Endangered P. coronata Lam. Near threatened L. lineare R.Br. Subsp Vulnerable P. cynaroides (L.) L. Least concern lineare P. denticulata Rourke Rare L. mundii Meisn. Rare P. eximia (Salisb. ex Kn.) Least concern L. oleifolium (Bergius) R.Br. Least concern Four. L. patersonii Phill. Vulnerable P. glabra Thunb. Least concern L. pluridens Rourke Near threatened P. grandiceps Tratt. Near threatened L. praecox Rourke Vulnerable P. holosericea (Salisb. ex Endangered Kn.) Rourke L. praemorsum (Meisn.) Vulnerable Phill. P. inopina Rourke Vulnerable L. profugum Rourke Endangered P. lacticolor Salisb. Endangered L. reflexum Rourke Near threatened P. lanceolata Meyer ex Least concern Meisn. L. spathulatum R.Br. Near threatened Cedarberg form P. laurifolia Thunb. Least concern L. spathulatum R.Br. Near threatened P. lepidocarpodendron (L.) Near threatened Keerom form L. (Continues) (Continues) 18 GEERTS ET AL.

Total number Species IUCN category of species P. longifolia Andrews Vulnerable P. longifolia minor Not assessed P. lorea R.Br. Near threatened P. lorifolia (Salisb. ex Kn.) Least concern Fourc. 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 ex Near threatened Meisn. 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)

APPENDIX C

Location and nectar amount for Protea and Erica species within the 1 ha plots in the southwestern Cape Floristic Region, South Africa.

Nectar concentration Nectar volume (Brix% sucrose Nectar sugar mg (μl) per equivalent) per flower (Erica) flower (Erica) per flower (Erica) Inflorescences or per or per or per sampled inflorescence inflorescence inflorescence (total number Site Plant species (Protea)(SD) (Protea)(SD) (Protea)(SD) of flowers) Kogelberg Harold Erica coccinea 0.02 (0.06) 0.05 (0.16) 35 – (10) Porter 2 and 3 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 mountain Protea burchelli 113.25 (–) 387 (–) 25.7 (2.8) 1 (10) monument East of Kleinmond P. compacta 388.72 (192) 1,474 (728) 11.6 (3.4) 2 (19) GEERTS ET AL. 19

Nectar concentration Nectar volume (Brix% sucrose Nectar sugar mg (μl) per equivalent) per flower (Erica) flower (Erica) per flower (Erica) Inflorescences or per or per or per sampled inflorescence inflorescence inflorescence (total number Site Plant species (Protea)(SD) (Protea)(SD) (Protea)(SD) of flowers) Helderberg nature P. coronata 852.90 (307) 3,041 (1,043) 25.1 (1.4) 2 (24) reserve 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) Kogelberg P. lepidocarpodendron 49.64 (6) 196 (29) 22.4 (3.9) 2 (20) Harold Porter 1 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.