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Pollination Structures Plant and Nectar‐Feeding Bird

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Pollination Structures Plant and Nectar‐Feeding Bird Received: 10 April 2020 Revised: 22 April 2020 Accepted: 3 May 2020 DOI: 10.1111/1440-1703.12148 ORIGINAL ARTICLE Pollination structures plant and nectar-feeding bird communities in Cape fynbos, South Africa: Implications for the conservation of plant–bird mutualisms Sjirk Geerts1 | Anina Coetzee2 | Anthony G. Rebelo3 | Anton Pauw4 1Department Conservation and Marine Sciences, Cape Peninsula 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 plants 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 (Proteaceae 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 Cape Floristic Region (CFR) South Africa for flowering Proteaceae species, number of inflorescences, 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 Protea, Leucospermum and Mimetes 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. flowering plant 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 birds, with the Cape Sugarbird 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 sugarbirds 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,
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