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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Effectiveness of native nectar-feeding birds and the introduced Apis mellifera as pollinators of the kangaroo paw, Anigozanthos manglesii (Haemodoraceae)

Bronwyn M. Ayre https://orcid.org/0000-0001-7553-3491 A B F , David G. Roberts B E , Ryan D. Phillips https://orcid.org/0000-0002-3777-9260 B C D , Stephen D. Hopper https://orcid.org/0000-0002-0364-2856 E and Siegfried L. Krauss https://orcid.org/0000-0002-7280-6324 A B
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Western Australia, 35 Stirling Highway, Crawely, WA 6009, Australia.

B Kings Park Science, Department of Biodiversity, Conservation and Attractions, 2 Kattidj Close, Kings Park, WA 6005, Australia.

C Department of Ecology, Environment and Evolution, La Trobe University, Melbourne, Vic. 3086, Australia.

D Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2600, Australia.

E Centre for Excellence in Natural Resource Management, School of Agriculture and Environment, University of Western Australia, 35 Stirling Terrace, Albany, WA 6330, Australia.

F Corresponding author. Email: bronwyn.ayre@research.uwa.edu.au

Australian Journal of Botany 68(1) 14-25 https://doi.org/10.1071/BT19097
Submitted: 21 May 2019  Accepted: 14 March 2020   Published: 5 May 2020

Abstract

Plants pollinated by vertebrates are often visited by native and exotic insects foraging for pollen and nectar. We compared flower visitation rates, foraging behaviour, and the contribution to reproduction of nectar-feeding birds and the introduced honeybee Apis mellifera in four populations of the bird-pollinated Anigozanthos manglesii (Haemodoraceae). The behaviour of floral visitors was quantified with direct observations and motion-triggered and hand-held cameras. Pollinator access to flowers was manipulated by enclosure in netting to either exclude all visitors or to exclude vertebrate visitors only. Apis mellifera was the only insect observed visiting flowers, and the most frequent flower visitor, but primarily acted as a pollen thief. Although birds visited A. manglesii plants only once per week on average, they were 3.5 times more likely to contact the anther or stigma as foraging honeybees. Exclusion of birds resulted in 67% fewer fruits and 81% fewer seeds than flowers left open and unmanipulated. Unnetted flowers that were open to bird and insect pollinators showed pollen-limitation and a large variation in reproductive output within and between sites. Although honeybees have been shown to pollinate other Australian plants, compared to birds, they are highly inefficient pollinators of A. manglesii.

Additional Keywords: bird pollination, honeybee, pollinator exclusion, pollen limitation, pollen-thief.


References

Abrahamczyk S, Souto-Vilaros D, Renner SS (2014) Escape from extreme specialization: passionflowers, bats and the sword-billed hummingbird. Proceedings of the Royal Society of London – B. Biological Sciences 281, 20140888
Escape from extreme specialization: passionflowers, bats and the sword-billed hummingbird.Crossref | GoogleScholarGoogle Scholar |

Abrol DP (2012) Non bee pollinators-plant interaction. In ‘Pollination Biology: Biodiversity Conservation and Agricultural Production’. pp. 265–310. (Springer Netherlands: Dordrecht, Netherlands)

Anderson SH, Kelly D, Ladley JJ, Molloy S, Terry J (2011) Cascading effects of bird functional extinction reduce pollination and plant density. Science 331, 1068–1071.
Cascading effects of bird functional extinction reduce pollination and plant density.Crossref | GoogleScholarGoogle Scholar | 21292938PubMed |

Anderson S, Kelly D, Robertson A, Ladley J (2016) Pollination by birds, a functional evaluation. In ‘Why Birds Matter: Avian Ecological Function and Ecosystem Services’. (Eds CH Sekercioglu, D Wenny, C Whelan) pp. 73–106. (University of Chicago Press: London, UK)

Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421.
Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences.Crossref | GoogleScholarGoogle Scholar |

Atlas of Living Australia (2018). Occurrence records download on 2018-09-07. Available at https://doi.ala.org.au/doi/7077fd45-e396-4dd3-9661-98057f647940 [Verified 19 February 2020]

Atlas of Living Australia (2019). Occurrence records download on 2019-03-12. Available at https://doi.ala.org.au/doi/742e1132-609b-485f-b750-bc705be7fe04 [Verified 19 February 2020]

Ayre BM, Roberts DJ, Phillips RD, Hopper SD, Krauss SL (2019) Near-neighbour optimal outcrossing in the bird-pollinated Anigozanthos manglesii. Annals of Botany 124, 423–436.
Near-neighbour optimal outcrossing in the bird-pollinated Anigozanthos manglesii.Crossref | GoogleScholarGoogle Scholar | 31115446PubMed |

Bailey WJ, Lebel T (1998) The mating biology of Phasmodes ranatriformis (Orthoptera: Tettigoniidae: Phasmodinae), a mute genus of bushcricket from Western Australia. Journal of the Royal Society of Western Australia 81, 149–155.

Beattie AJ, Turnbull C, Knox RB, Williams EG (1984) Ant inhibition of pollen function: a possible reason why ant pollination is rare. American Journal of Botany 71, 421–426.
Ant inhibition of pollen function: a possible reason why ant pollination is rare.Crossref | GoogleScholarGoogle Scholar |

Breed MF, Christmas MJ, Lowe AJ (2014) Higher levels of multiple paternities increase seedling survival in the long-lived tree Eucalyptus gracilis. PLoS One 9, e90478
Higher levels of multiple paternities increase seedling survival in the long-lived tree Eucalyptus gracilis.Crossref | GoogleScholarGoogle Scholar | 25192006PubMed |

Brown E (1988) Pollination and seed production in two species of kangaroo paws, Anigozanthos pulcherrimus and Macropidia fuliginosa. MSc thesis, School of Molecular and Life Sciences, Curtin University of Technology, Perth, WA, Australia.

Brown B, Mitchell RJ (2001) Competition for pollination: effects of pollen of an invasive plant species on seed set of a native congener. Oecologia 129, 43–49.
Competition for pollination: effects of pollen of an invasive plant species on seed set of a native congener.Crossref | GoogleScholarGoogle Scholar | 28547066PubMed |

Brown E, Burbidge A, Dell J, Edinger D, Hopper SD, Wills RT (1997) ‘Pollination in Western Australia: a Data Base of Animals Visiting Flowers.’ (WA Naturalists’ Club: Perth, WA, Australia)

Burd M, Ashman T-L, Campbell DR, Dudash MR, Johnston MO, Knight TM, Mazer SJ, Mitchell RJ, Steets JA, Vamosi JC (2009) Ovule number per flower in a world of unpredictable pollination. American Journal of Botany 96, 1159–1167.
Ovule number per flower in a world of unpredictable pollination.Crossref | GoogleScholarGoogle Scholar | 21628266PubMed |

Carpenter FL (1976) Plant-pollinator interactions in Hawaii: pollination energetics of Metrosideros collina. Ecology 57, 1125–1144.
Plant-pollinator interactions in Hawaii: pollination energetics of Metrosideros collina.Crossref | GoogleScholarGoogle Scholar |

Castellanos MC, Wilison P, Thomson JD (2004) ‘Anti-bee’ and ‘pro-bird’ changes during the evolution of hummingbird pollination in Penstemon flowers. Journal of Evolutionary Biology 17, 876–885.
‘Anti-bee’ and ‘pro-bird’ changes during the evolution of hummingbird pollination in Penstemon flowers.Crossref | GoogleScholarGoogle Scholar | 15271088PubMed |

Celebrezze TM (2002) Effects of European honeybees (Apis mellifera) on the pollination ecology of bird-and insect-adapted Australian plants. PhD thesis, Department of Biological Sciences, University of Wollongong, Wollongong, NSW, Australia.

Celebrezze T, Paton DC (2004) Do introduced honeybees (Apis mellifera, Hymenoptera) provide full pollination service to bird-adapted Australian plants with small flowers? An experimental study of Brachyloma ericoides (Epacridaceae). Austral Ecology 29, 129–136.
Do introduced honeybees (Apis mellifera, Hymenoptera) provide full pollination service to bird-adapted Australian plants with small flowers? An experimental study of Brachyloma ericoides (Epacridaceae).Crossref | GoogleScholarGoogle Scholar |

Collins BG (1985) Energetics of foraging and resource selection by honeyeaters in forest and woodland habitats of Western Australia. New Zealand Journal of Zoology 12, 577–587.
Energetics of foraging and resource selection by honeyeaters in forest and woodland habitats of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Collins BG, Briffa P (1982) Seasonal variation of abundance and foraging of three species of Australian honeyeaters. Wildlife Research 9, 557–569.
Seasonal variation of abundance and foraging of three species of Australian honeyeaters.Crossref | GoogleScholarGoogle Scholar |

Cronk Q, Ojeda I (2008) Bird-pollinated flowers in an evolutionary and molecular context. Journal of Experimental Botany 59, 715–727.
Bird-pollinated flowers in an evolutionary and molecular context.Crossref | GoogleScholarGoogle Scholar | 18326865PubMed |

Davis RA, Wilcox JA (2013) Adapting to suburbia: bird ecology on an urban-bushland interface in Perth, Western Australia. Pacific Conservation Biology 19, 110–120.
Adapting to suburbia: bird ecology on an urban-bushland interface in Perth, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Davis RA, Gole C, Roberts JD (2013) Impacts of urbanisation on the native avifauna of Perth, Western Australia. Urban Ecosystems 16, 427–452.
Impacts of urbanisation on the native avifauna of Perth, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Eakin-Busher EL, Fontaine JB, Ladd PG (2016) The bees don’t know and the flowers don’t care: the effect of heterospecific pollen on reproduction in co-occurring Thysanotus species (Asparagaceae) with similar flowers. Botanical Journal of the Linnean Society 181, 640–650.
The bees don’t know and the flowers don’t care: the effect of heterospecific pollen on reproduction in co-occurring Thysanotus species (Asparagaceae) with similar flowers.Crossref | GoogleScholarGoogle Scholar |

Evans KL, Newson SE, Gaston KJ (2009) Habitat influences on urban avian assemblages. The Ibis 151, 19–39.
Habitat influences on urban avian assemblages.Crossref | GoogleScholarGoogle Scholar |

Fernández-Juricic E (2000) Bird community composition patterns in urban parks of Madrid: the role of age, size and isolation. Ecological Research 15, 373–383.
Bird community composition patterns in urban parks of Madrid: the role of age, size and isolation.Crossref | GoogleScholarGoogle Scholar |

Gagliardi B, Marcos-Filho J (2011) Relationship between germination and bell pepper seed structure assessed by the X-ray test. Scientia Agrícola 68, 411–416.
Relationship between germination and bell pepper seed structure assessed by the X-ray test.Crossref | GoogleScholarGoogle Scholar |

Garavanta C (1997) A mark-recapture study of the social organisation of the honey possum Tarsipes rostratus in the Fitzgerald River National Park, Western Australia. PhD thesis, School of Biological Sciences, Murdoch University, Perth, WA, Australia.

Gilpin A-M, Collette JC, Denham AJ, Ooi MKJ, Ayre DJ (2016) Do introduced honeybees affect seed set and seed quality in a plant adapted for bird pollination? Journal of Plant Ecology 10, 721–729.
Do introduced honeybees affect seed set and seed quality in a plant adapted for bird pollination?Crossref | GoogleScholarGoogle Scholar |

Goldingay RL (1990) The foraging behaviour of a nectar feeding marsupial, Petaurus australis. Oecologia 85, 191–199.
The foraging behaviour of a nectar feeding marsupial, Petaurus australis.Crossref | GoogleScholarGoogle Scholar | 28312555PubMed |

Grab H, Blitzer EJ, Danforth B, Loeb G, Poveda K (2017) Temporally dependent pollinator competition and facilitation with mass flowering crops affects yield in co-blooming crops. Scientific Reports 7, 45296
Temporally dependent pollinator competition and facilitation with mass flowering crops affects yield in co-blooming crops.Crossref | GoogleScholarGoogle Scholar | 28345653PubMed |

Gross C (2001) The effect of introduced honeybees on native bee visitation and fruit-set in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem. Biological Conservation 102, 89–95.
The effect of introduced honeybees on native bee visitation and fruit-set in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem.Crossref | GoogleScholarGoogle Scholar |

Han F, Wallberg A, Webster MT (2012) From where did the western honeybee (Apis mellifera) originate? Ecology and Evolution 2, 1949–1957.
From where did the western honeybee (Apis mellifera) originate?Crossref | GoogleScholarGoogle Scholar | 22957195PubMed |

Hargreaves AL, Harder LD, Johnson SD (2009) Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biological Reviews of the Cambridge Philosophical Society 84, 259–276.
Consumptive emasculation: the ecological and evolutionary consequences of pollen theft.Crossref | GoogleScholarGoogle Scholar | 19382932PubMed |

Hargreaves AL, Harder LD, Johnson SD (2012) Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees. Annals of Botany 109, 761–772.
Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees.Crossref | GoogleScholarGoogle Scholar | 22278414PubMed |

Higham RK, McQuillan PB (2000) Cyathodes divaricata (Epacridaceae) the first record of a bird-pollinated dioecious plant in the Australian flora. Australian Journal of Botany 48, 93–99.
Cyathodes divaricata (Epacridaceae) the first record of a bird-pollinated dioecious plant in the Australian flora.Crossref | GoogleScholarGoogle Scholar |

Holzschuh A, Steffan-Dewenter I, Kleign D, Tscharntke T (2007) Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context. Journal of Applied Ecology 44, 41–49.
Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context.Crossref | GoogleScholarGoogle Scholar |

Hopper SD (1980a) Pollen and nectar feeding by purple-crowned lorikeets on Eucalyptus occidentalis. Emu 80, 239–240.
Pollen and nectar feeding by purple-crowned lorikeets on Eucalyptus occidentalis.Crossref | GoogleScholarGoogle Scholar |

Hopper SD (1980b) A biosystematic study of the kangaroo paws, Anigozanthos and Macropidia (Haemodoraceae). Australian Journal of Botany 28, 659–680.
A biosystematic study of the kangaroo paws, Anigozanthos and Macropidia (Haemodoraceae).Crossref | GoogleScholarGoogle Scholar |

Hopper SD (1993) ‘Kangaroo Paws and Catspaws: a Natural History and Field Guide.’ (Department of Conservation and Land Management: Perth, WA, Australia)

Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil 322, 49–86.
OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes.Crossref | GoogleScholarGoogle Scholar |

Hopper SD, Burbidge N (1978) Assortative pollination by red wattlebirds in hybrid populations of Anigozanthos Labill. (Haemodoraceae). Australian Journal of Botany 26, 335–350.
Assortative pollination by red wattlebirds in hybrid populations of Anigozanthos Labill. (Haemodoraceae).Crossref | GoogleScholarGoogle Scholar |

Hopper SD, Gioia P (2004) The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology, Evolution, and Systematics 35, 623–650.
The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity.Crossref | GoogleScholarGoogle Scholar |

Hopper SD, Silveira FAO, Fiedler PL (2016) Biodiversity hotspots and Ocbil theory. Plant and Soil 403, 167–216.
Biodiversity hotspots and Ocbil theory.Crossref | GoogleScholarGoogle Scholar |

How RA, Dell J (2000) Ground vertebrate fauna of Perth’s vegetation remnants: impact of 170 years of urbanization. Pacific Conservation Biology 6, 198–217.
Ground vertebrate fauna of Perth’s vegetation remnants: impact of 170 years of urbanization.Crossref | GoogleScholarGoogle Scholar |

Jha S, Vandermeer JH (2009) Contrasting bee foraging in response to resource scale and local habitat management. Oikos 118, 1174–1180.
Contrasting bee foraging in response to resource scale and local habitat management.Crossref | GoogleScholarGoogle Scholar |

Johnson SD (2010) The pollination niche and its role in the diversification and maintenance of the southern African flora. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 365, 499–516.
The pollination niche and its role in the diversification and maintenance of the southern African flora.Crossref | GoogleScholarGoogle Scholar | 20047876PubMed |

Johnson SD, Wester P (2017) Stefan Vogel’s analysis of floral syndromes in the South African flora: an appraisal based on 60 years of pollination studies. Flora 232, 200–206.
Stefan Vogel’s analysis of floral syndromes in the South African flora: an appraisal based on 60 years of pollination studies.Crossref | GoogleScholarGoogle Scholar |

Kamra SK (1964) Determination of germinability of cumber with X-ray contrast method. Proceedings of the International Seed Testing Association 29, 519–534.

Keighery GJ (1980) Bird pollination in South Western Australia: a checklist. Plant Systematics and Evolution 135, 171–176.
Bird pollination in South Western Australia: a checklist.Crossref | GoogleScholarGoogle Scholar |

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36, 467–497.
Pollen limitation of plant reproduction: pattern and process.Crossref | GoogleScholarGoogle Scholar |

Krauss SL, Phillips RD, Karron JD, Johnson SD, Roberts DG, Hopper SD (2017) Novel consequences of bird pollination for plant mating. Trends in Plant Science 22, 395–410.
Novel consequences of bird pollination for plant mating.Crossref | GoogleScholarGoogle Scholar | 28412035PubMed |

Krauss SL, Roberts DG, Phillips RD, Edwards C (2018) Effectiveness of camera traps for quantifying daytime and nighttime visitation by vertebrate pollinators. Ecology and Evolution 8, 9304–9314.
Effectiveness of camera traps for quantifying daytime and nighttime visitation by vertebrate pollinators.Crossref | GoogleScholarGoogle Scholar | 30377502PubMed |

Le Roux JJ, Geerts S, Ivey P, Krauss S, Richardson DM, Suda J, Wilson JRU (2010) Molecular systematics and ecology of invasive kangaroo paws in South Africa: management implications for a horticulturally important genus. Biological Invasions 12, 3989–4002.
Molecular systematics and ecology of invasive kangaroo paws in South Africa: management implications for a horticulturally important genus.Crossref | GoogleScholarGoogle Scholar |

Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81, 2651–2661.
Are nectar robbers cheaters or mutualists?Crossref | GoogleScholarGoogle Scholar |

Menz MHM, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD, Dixon KW (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends in Plant Science 16, 4–12.
Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms.Crossref | GoogleScholarGoogle Scholar |

Micheneau C, Fournel J, Warren BH, Hugel S, Gauvin-Bialecki A, Pailler T, Strasberg D, Chase MW (2010) Orthoptera, a new order of pollinator. Annals of Botany 105, 355–364.
Orthoptera, a new order of pollinator.Crossref | GoogleScholarGoogle Scholar | 20067913PubMed |

Newland C (1982). The effect of changes in nectar availability on an assemblage of honeyeaters in a banksia woodland, near Perth. BSc(Hons) thesis, School of Veterinary and Life Sciences, Murdoch University, Perth, WA, Australia.

Ollerton J, Johnson SD, Hingston AB (2006) Geographical variation in diversity and specificity of pollination systems. In ‘Plant–Pollinator Interactions from Specialization to Generalization’. (Eds NM Waser, JM Olesen) pp. 283–308. (University of Chicago Press: Chicago, IL, USA)

Paini DR (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: a review. Austral Ecology 29, 399–407.
Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: a review.Crossref | GoogleScholarGoogle Scholar |

Paton DC (1993) Honeybees in the Australian environment. Does Apis mellifera disrupt or benefit the native biota? Bioscience 43, 95–103.
Honeybees in the Australian environment. Does Apis mellifera disrupt or benefit the native biota?Crossref | GoogleScholarGoogle Scholar |

Paton DC (1996) ‘Overview of the Impacts of Feral and Managed Honeybees in Australia: Distribution, Abundance, Extent of Interactions with Native Biota, Evidence of Impacts and Future Research.’ (Australian Nature Conservation Agency: Canberra, ACT, Australia)

Paton DC, Turner V (1985) Pollination of Banksia ericifolia Smith: birds, mammals and insects as pollen vectors. Australian Journal of Botany 33, 271–286.
Pollination of Banksia ericifolia Smith: birds, mammals and insects as pollen vectors.Crossref | GoogleScholarGoogle Scholar |

Phillips RD, Hopper SD, Dixon KW (2010) Pollination ecology and the possible impacts of environmental change in the Southwest Australian Biodiversity Hotspot. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 365, 517–528.
Pollination ecology and the possible impacts of environmental change in the Southwest Australian Biodiversity Hotspot.Crossref | GoogleScholarGoogle Scholar | 20047877PubMed |

Phillips RD, Steinmeyer F, Menz MHM, Erickson TE, Dixon KW (2014) Changes in the composition and behaviour of a pollinator guild with plant population size and the consequences for plant fecundity. Functional Ecology 28, 846–856.
Changes in the composition and behaviour of a pollinator guild with plant population size and the consequences for plant fecundity.Crossref | GoogleScholarGoogle Scholar |

Pyke G (1999) The introduced Honeybee Apis mellifera and the precautionary principle: reducing the conflict. Australian Zoologist 31, 181–186.
The introduced Honeybee Apis mellifera and the precautionary principle: reducing the conflict.Crossref | GoogleScholarGoogle Scholar |

Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. The Quarterly Review of Biology 52, 137–154.
Optimal foraging: a selective review of theory and tests.Crossref | GoogleScholarGoogle Scholar |

Ramsey MW (1988) Differences in pollinator effectiveness of birds and insects visiting Banksia menziesii (Proteaceae). Oecologia 76, 119–124.
Differences in pollinator effectiveness of birds and insects visiting Banksia menziesii (Proteaceae).Crossref | GoogleScholarGoogle Scholar | 28312388PubMed |

Rathcke BJ (2000) Hurricane causes resource and pollination limitation of fruit set in a bird-pollinated shrub. Ecology 81, 1951–1958.
Hurricane causes resource and pollination limitation of fruit set in a bird-pollinated shrub.Crossref | GoogleScholarGoogle Scholar |

Ratto F, Simmons BI, Spake R, Zamora-Gutierrez V, MacDonald MA, Merriman JC, Tremlett CJ, Poppy GM, Peh KSH, Dicks LV (2018) Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis. Frontiers in Ecology and the Environment 16, 82–90.
Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Recher HF (1997) Impact of wildfire on the avifauna of Kings Park, Perth, Western Australia. Wildlife Research 24, 745–761.
Impact of wildfire on the avifauna of Kings Park, Perth, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Recher HF, Servety DL (1991) Long term changes in the relative abundances of birds in Kings Park, Perth, Western Australia. Conservation Biology 5, 90–102.
Long term changes in the relative abundances of birds in Kings Park, Perth, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Regan EC, Santini L, Ingwall-King L, Hoffmann M, Rondinini C, Symes A, Taylor J, Butchart SHM (2015) Global trends in the status of bird and mammal pollinators. Conservation Letters 8, 397–403.
Global trends in the status of bird and mammal pollinators.Crossref | GoogleScholarGoogle Scholar |

Ritchie AL, Dyer RJ, Nevill PG, Sinclair EA, Krauss SL (2019) Wide outcrossing provides functional connectivity for new and old Banksia populations within a fragmented landscape. Oecologia
Wide outcrossing provides functional connectivity for new and old Banksia populations within a fragmented landscape.Crossref | GoogleScholarGoogle Scholar | 30919107PubMed |

Saffer VM, Brown EM, Hopper SD, Dell J, Wills RT, Burbidge AH, Majer JD (2000) Pollination and revegetation in the south west of Western Australia. Western Australian Naturalist 22, 221–279.

Sakai AK, Wagner WL, Mehrhoff LA (2002) Patterns of endangerment in the Hawaiian flora. Systematic Biology 51, 276–302.
Patterns of endangerment in the Hawaiian flora.Crossref | GoogleScholarGoogle Scholar | 12028733PubMed |

Sánchez-Lafuente AM (2002) Floral variation in the generalist perennial herb Paeonia broteroi (Paeoniaceae): differences between regions with different pollinators and herbivores. American Journal of Botany 89, 1260–1269.
Floral variation in the generalist perennial herb Paeonia broteroi (Paeoniaceae): differences between regions with different pollinators and herbivores.Crossref | GoogleScholarGoogle Scholar | 21665727PubMed |

Schmid B, Nottebrock H, Esler KJ, Pagel J, Pauw A, Böhning-Gaese K, Schurr FM, Schleuning M (2016) Responses of nectar-feeding birds to floral resources at multiple spatial scales. Ecography 39, 619–629.
Responses of nectar-feeding birds to floral resources at multiple spatial scales.Crossref | GoogleScholarGoogle Scholar |

Schuett EM, Vamosi JC (2010) Phylogenetic community context influences pollen delivery to Allium cernuum. Evolutionary Biology 37, 19–28.
Phylogenetic community context influences pollen delivery to Allium cernuum.Crossref | GoogleScholarGoogle Scholar |

Sekercioglu CH (2006) Increasing awareness of avian ecological function. Trends in Ecology & Evolution 21, 464–471.
Increasing awareness of avian ecological function.Crossref | GoogleScholarGoogle Scholar |

Shrestha M, Dyer AG, Burd M (2013) Evaluating the spectral discrimination capabilities of different pollinators and their effect on the evolution of flower colors. Communicative & Integrative Biology 6, e24000
Evaluating the spectral discrimination capabilities of different pollinators and their effect on the evolution of flower colors.Crossref | GoogleScholarGoogle Scholar |

Stang M, Klinkhamer PGL, Waser NM, Stang I, van der Meijden E (2009) Size-specific interaction patterns and size matching in a plant–pollinator interaction web. Annals of Botany 103, 1459–1469.
Size-specific interaction patterns and size matching in a plant–pollinator interaction web.Crossref | GoogleScholarGoogle Scholar | 19228701PubMed |

Stenhouse RN (2004) Fragmentation and internal disturbance of native vegetation reserves in the Perth metropolitan area, Western Australia. Landscape and Urban Planning 68, 389–401.
Fragmentation and internal disturbance of native vegetation reserves in the Perth metropolitan area, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Stiles FG (1975) Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia species. Ecology 56, 285–301.
Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia species.Crossref | GoogleScholarGoogle Scholar |

Taylor G, Whelan RJ (1988) Can honeybees pollinate Grevillea? Australian Zoologist 24, 193–196.
Can honeybees pollinate Grevillea?Crossref | GoogleScholarGoogle Scholar |

Temeles EJ, Kress WJ (2010) Mate choice and mate competition by a tropical hummingbird at a floral resource. Proceedings of the Royal Society of London – B. Biological Sciences 277, 1607–1613.
Mate choice and mate competition by a tropical hummingbird at a floral resource.Crossref | GoogleScholarGoogle Scholar |

Tieu A, Dixon KW, Meney KA, Sivasithamparam K, Barrett RL (2001) Spatial and developmental variation in seed dormancy characteristics in the fire-responsive species Anigozanthos manglesii (Haemodoraceae) from Western Australia. Annals of Botany 88, 19–26.
Spatial and developmental variation in seed dormancy characteristics in the fire-responsive species Anigozanthos manglesii (Haemodoraceae) from Western Australia.Crossref | GoogleScholarGoogle Scholar |

Vaughton G (1992) Effectiveness of nectarivorous birds and honeybees as pollinators of Banksia spinulosa (Proteaceae). Australian Journal of Ecology 17, 43–50.
Effectiveness of nectarivorous birds and honeybees as pollinators of Banksia spinulosa (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Vaughton G (1996) Pollination disruption by European honeybees in the Australian bird-pollinated shrub Grevillea barklyana (Proteaceae). Plant Systematics and Evolution 200, 89–100.
Pollination disruption by European honeybees in the Australian bird-pollinated shrub Grevillea barklyana (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Veddeler D, Klein A-M, Tscharntke T (2006) Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos 112, 594–601.
Contrasting responses of bee communities to coffee flowering at different spatial scales.Crossref | GoogleScholarGoogle Scholar |

Wardhaugh CW (2015) How many species of arthropods visit flowers? Arthropod–Plant Interactions 9, 547–565.
How many species of arthropods visit flowers?Crossref | GoogleScholarGoogle Scholar |

Whelan CJ, Şekercioğlu ÇH, Wenny DG (2015) Why birds matter: from economic ornithology to ecosystem services. Journal of Ornithology 156, 227–238.
Why birds matter: from economic ornithology to ecosystem services.Crossref | GoogleScholarGoogle Scholar |

Yates CJ, Hopper SD, Taplin RH (2005) Native insect flower diversity and feral honeybees on jarrah (Eucalyptus marginata) in Kings Park, an urban bushland remnant. Journal of the Royal Society of Western Australia 88, 147–153.