The critical role of honeyeaters in the pollination of the catspaw Anigozanthos humilis (Haemodoraceae)
Tayla van der Kroft A B , David G. Roberts B C and Siegfried L. Krauss A B D
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, The University of Western Australia, Crawley, WA 6009, Australia.
B Kings Park Science, Botanic Gardens and Parks Authority, Department of Biodiversity, Conservation and Attractions, West Perth, WA 6005, Australia.
C Centre for Natural Resource Management, The University of Western Australia, Albany, WA 6330, Australia.
D Corresponding author. Email: siegy.krauss@dbca.wa.gov.au
Australian Journal of Botany 67(4) 281-289 https://doi.org/10.1071/BT18209
Submitted: 2 November 2018 Accepted: 1 April 2019 Published: 6 June 2019
Abstract
The pollination biology of Anigozanthos humilis (Haemodoraceae) was studied within a Banksia woodland reserve using a combination of field techniques and genetic analysis. Motion-triggered cameras were deployed on 25 flowering plants to identify visitors to flowers, quantify visitation rates and assess visitor behaviour. Entire A. humilis plants were caged to exclude potential floral visitors with six treatments: (i) bird and honey possum exclusion, allowing access by insects; (ii) bird and insect exclusion, allowing access by honey possums; (iii) total animal exclusion; (iv) open, allowing access by birds, insects and honey possums; (v) hand-pollination with cross-pollen; and (vi) hand-pollination with self-pollen. Open pollinated seed were genotyped to assess mating system parameters including outcrossing rate. From 23 424 h of surveillance with camera traps, 109 visits were recorded, 106 (97%) of which were western spinebills (Acanthorhynchus superciliosus), with three visits by brown honeyeaters (Lichmera indistincta). We recorded an average of 8 (±4) visits per plant, equivalent to one visit every eleven days over the 2016 flowering season (mean = 63 days). Mean seed set per fruit was negligible (0.2–0.3 seed per fruit) for all pollination treatments except open- and hand-pollination with cross pollen. Mean seed set per fruit for hand cross-pollinated flowers (37.1 seed per fruit) was 37 times that of open pollinated flowers (1.0 seed per fruit). Outcrossing rate estimates were not significantly different to one. Our results indicate that at least for the study population and season, A. humilis was largely dependent on western spinebills for delivery of outcross pollen and resulting seed set, but visitation rates were low and pollen limitation was severe. Given the known sensitivity of western spinebills to habitat fragmentation, our results suggest flow on effects that may negatively impact on reproduction, and means that A. humilis may be particularly vulnerable to environmental changes that impact on bird pollinators.
Additional keywords: banksia woodland, bird pollination, camera trap, conservation, mating system, pollination syndrome, pollinator.
References
ABBBS (2018) Australian bird and bat banding scheme. Available at: http://www.environment.gov.au/science/bird-and-bat-banding (accessed 5 May 2019)Anderson B, Cole WW, Barrett SCH (2005) Specialized bird perch aids in cross-pollination. Nature 435, 41–42.
| Specialized bird perch aids in cross-pollination.Crossref | GoogleScholarGoogle Scholar | 15875009PubMed |
Anderson SH, Kelly D, Robertson AW, Ladley JJ (2016) Pollination by birds, a functional analysis. In ‘Why birds matter: Avian ecological function and ecosystem services’. (Ed. CH Sekercioglu) pp. 73–106. (University of Chicago Press: Chicago, IL)
Anthony J, Allcock R, Krauss S (2016) Isolation and characterization of 13 microsatellites for the rare endemic shrub Tetratheca erubescens (Elaeocarpaceae). Applications in Plant Sciences 4, 1500102
| Isolation and characterization of 13 microsatellites for the rare endemic shrub Tetratheca erubescens (Elaeocarpaceae).Crossref | GoogleScholarGoogle Scholar | 26949577PubMed |
Armbruster WS (2017) Plant pollinator interactions from flower to landscape: the specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Functional Ecology 31, 88–100.
| Plant pollinator interactions from flower to landscape: the specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation.Crossref | GoogleScholarGoogle Scholar |
Armstrong JA (1979) Biotic pollination mechanisms in the Australian flora – a review. New Zealand Journal of Boany 17, 467–508.
Ayre BM, Anthony JM, Roberts DG, Allcock RJN, Krauss SL (2017) Characterisation and transferability of microsatellites for the kangaroo paw, Anigozanthos manglesii (Haemodoraceae). Applications in Plant Sciences 5, 1700055
| Characterisation and transferability of microsatellites for the kangaroo paw, Anigozanthos manglesii (Haemodoraceae).Crossref | GoogleScholarGoogle Scholar | 28924516PubMed |
Brown EM, Burbidge AH, Dell J, Edinger D, Hopper SD, Wills RT (1997) ‘Pollination in Western Australia: a database of animals visiting flowers. Handbook no. 15.’ (WA Naturalists Club: Perth, WA)
Burton AC, Neilson E, Moreira D, Ladle A, Steenweg R, Fisher JT, Boutin S (2015) Wildlife camera trapping: a review and recommendations for linking surveys to ecological processes. Journal of Applied Ecology 52, 675–685.
Carlson JE, Tulsieram J, Glaubitz JC, Luk VMK, Kauffeldt LC, Rutledge R (1991) Segregation of random amplified DNA markers in F1 progeny of conifers. Theoretical and Applied Genetics 83, 194–200.
| Segregation of random amplified DNA markers in F1 progeny of conifers.Crossref | GoogleScholarGoogle Scholar | 24202358PubMed |
Carthew S (1993) An assessment of pollinator visitation to Banksia spinulosa. Austral Ecology 18, 257–268.
| An assessment of pollinator visitation to Banksia spinulosa.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. Australian Wildlife Research 9, 557–569.
| Seasonal variation of abundance and foraging of three species of Australian honeyeaters.Crossref | GoogleScholarGoogle Scholar |
Davis R, Gole C, Roberts D (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 |
Department of Environment and Energy (2016) Banksia woodlands of the Swan Coastal Plain. A nationally-protected ecological community. (Department of Environment and Energy, Commonwealth of Australia: Canberra, ACT)
Florabase (2017) Anigozanthos humilis Lindl. subsp. humilis. Perth, Western Australia. Available at: https://florabase.dpaw.wa.gov.au/browse/profile/11434 (accessed 24 May 2017)
Frick KM, Ritchie AL, Krauss SL (2014) Field of dreams: restitution of pollinator services in restored bird-pollinated plant populations. Restoration Ecology 22, 832–840.
| Field of dreams: restitution of pollinator services in restored bird-pollinated plant populations.Crossref | GoogleScholarGoogle Scholar |
Gioia P, Hopper SD (2017) A new phytogeographic map for the Southwestern Australian Floristic Region after an exceptional decade of collection and discovery. Botanical Journal of the Linnean Society 184, 1–15.
Gonzalez-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyörgyi H, Woyciechowski M, Vilà M (2013) Combined effects of global change pressures on animal-mediated pollination. Trends in Ecology & Evolution 28, 524–530.
| Combined effects of global change pressures on animal-mediated pollination.Crossref | GoogleScholarGoogle Scholar |
Groffen J, Rethus G, Pettigrew J (2016) Promiscuous pollination of Australia’s baobab, the boab, Adansonia gregorii. Australian Journal of Botany 64, 678–686.
Hobbhahn N, Steenhuisen SL, Olsen T, Midgely JJ, Johnson SD (2017) Pollination and breeding system of the enigmatic South African parasitic plant Mystropetalon thomii (Mystropetalaceae): rodents welcome, but not needed. Plant Biology 19, 775–786.
Hopper S (1980) 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 S (1993) ‘Kangaroo paws and catspaws: a natural history and field guide.’ (Department of Conservation and Land Management: Perth, WA)
Hopper S, Burbidge A (1978) Assortative pollination by red wattlebirds in a hybrid population of Anigozanthos Labill. (Haemodoraceae). Australian Journal of Botany 26, 335–350.
| Assortative pollination by red wattlebirds in a hybrid population of Anigozanthos Labill. (Haemodoraceae).Crossref | GoogleScholarGoogle Scholar |
Hort F, Hort J (2010) ‘Plant inventory: Ioppolo Nature Reserve, Chittering.’ (Department of Conservation and Environment Volunteers: Swan View, WA)
Johnson SD (2006) Pollinator-driven speciation in plants. In ‘Ecology and evolution of flowers’. (Eds LD Harder, SCH Barrett) pp. 295–310. (Oxford University Press: Oxford, UK)
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.
Karron JD, Mitchell RJ, Bell JM (2006) Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits. American Journal of Botany 93, 1306–1312.
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 |
Kelly D, Ladley J, Robertson A, Anderson S, Wotton D, Wiser S (2010) Mutualisms with the wreckage of an avifauna: the status of bird pollination and fruit-dispersal in New Zealand. New Zealand Journal of Ecology 34, 66–85.
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 R, Karron J, Johnson S, Roberts D, Hopper S (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 night time visitation by vertebrate pollinators. Ecology and Evolution.
| Effectiveness of camera traps for quantifying daytime and night time visitation by vertebrate pollinators.Crossref | GoogleScholarGoogle Scholar | 30377502PubMed |
Larson BM, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society. Linnean Society of London 69, 503–520.
| A comparative analysis of pollen limitation in flowering plants.Crossref | GoogleScholarGoogle Scholar |
Lombardi G, Peter C, Midgley JJ, Turner R (2013) Evidence for rodent-pollination in Erica lanuginosa (Ericaceae). South African Journal of Botany 86, 175–176.
Meek PD, Ballard GA, Vernes K, Fleming PJS (2015) The history of wildlife camera trapping as a survey tool in Australia. Australian Mammalogy 37, 1–12.
Melidonis C, Peter C (2015) Diurnal pollination, primarily by a single species of rodent, documented in Protea foliosa using modified camera traps. South African Journal of Botany 97, 9–15.
| Diurnal pollination, primarily by a single species of rodent, documented in Protea foliosa using modified camera traps.Crossref | GoogleScholarGoogle Scholar |
Menz MHM, et al. (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends in Plant Science 16, 4–12.
Newland C, Wooller R (1985) Seasonal changes in a honeyeater assemblage in Banksia woodland near Perth, Western Australia. New Zealand Journal of Zoology 12, 631–636.
| Seasonal changes in a honeyeater assemblage in Banksia woodland near Perth, Western Australia.Crossref | GoogleScholarGoogle Scholar |
O’Connell AF, Nichols JD, Karanth KU (2011) (Eds) ‘Camera traps in animal ecology: methods and analyses.’ (Springer: New York)
Ollerton J, Alarcon R, Waser NM, Price M, Watts S, Cranmer L, Hingston A, Peter C, Rottenberry J (2009) A global test of the pollination syndrome hypothesis. Annals of Botany 103, 1471–1480.
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120, 321–326.
| How many flowering plants are pollinated by animals?Crossref | GoogleScholarGoogle Scholar |
Phillips R, Hopper S, Dixon K (2010) Pollination ecology and the possible impacts of environmental change in the southwest Australian biodiversity hotspot. Philosophical Transactions of the Royal Society of London. Series 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 |
Potts S, Biesmeijer J, Kremen C, Neumann P, Schweiger O, Kunin W (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25, 345–353.
| Global pollinator declines: trends, impacts and drivers.Crossref | GoogleScholarGoogle Scholar |
Proctor M, Yeo P, Lack A (1996) ‘The natural history of pollination.’ (Timber Press: Portland, OR, USA)
Ramsay M (1989) The seasonal abundance and foraging behaviour of honeyeaters and their potential role in the pollination of Banksia menziesii. Australian Journal of Ecology 14, 33–40.
| The seasonal abundance and foraging behaviour of honeyeaters and their potential role in the pollination of Banksia menziesii.Crossref | GoogleScholarGoogle Scholar |
Ramsey M, Vaughton G (1991) Self-incompatibility, protandry, pollen production and pollen longevity in Banksia menziesii. Australian Journal of Botany 39, 497–504.
| Self-incompatibility, protandry, pollen production and pollen longevity in Banksia menziesii.Crossref | GoogleScholarGoogle Scholar |
Ratto F, Simmons BI, Spake R, Zamora-Gutierrez V, MacDonald MA, Merriman JC, Tremlett CJ, Poppy GM, Peh KS-H, Dicks LV (2018) Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis. Frontiers in Ecology and the Environment.
| Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Ritchie AL, Krauss SL (2012) A genetic assessment of ecological restoration success in Banksia attenuata. Restoration Ecology 20, 441–449.
| A genetic assessment of ecological restoration success in Banksia attenuata.Crossref | GoogleScholarGoogle Scholar |
Ritland K (2002) Extensions of models for the estimation of mating systems using independent loci. Heredity 88, 221–228.
| Extensions of models for the estimation of mating systems using independent loci.Crossref | GoogleScholarGoogle Scholar | 11920127PubMed |
Rosas-Guerrero V, Aguilar R, Marten-Rodriguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecology Letters 17, 388–400.
Rovero F, Zimmermann F, Berzi D, Meek P (2013) “Which camera trap type and how many do I need?” A review of camera features and study designs for a range of wildlife research applications. Hystrix, the Italian Journal of Mammalogy 24, 148–156.
Srestha M, Dyer AG, Boyd-Gerny S, Wong BBM, Burd M (2013) Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision. New Phytologist 198, 301–310.
| Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision.Crossref | GoogleScholarGoogle Scholar |
Steenweg R, Hebblewhite M, Kays R, et al. (2017) Scaling-up camera traps: monitoring the planet’s biodiversity with networks of remote sensors. Frontiers in Ecology and the Environment 15, 26–34.
van der Niet T, Cozien R, Johnson S (2015) Experimental evidence for specialized bird pollination in the endangered South African orchid Satyrium rhodanthumand analysis of associated floral traits. Botanical Journal of the Linnean Society 177, 141–150.
| Experimental evidence for specialized bird pollination in the endangered South African orchid Satyrium rhodanthumand analysis of associated floral traits.Crossref | GoogleScholarGoogle Scholar |
Waser NM, Ollerton J (2006) ‘Plant–pollinator interactions: from specialization to generalization.’ (University of Chicago Press: Chicago, IL, USA)
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77, 1043–1060.
| Generalization in pollination systems, and why it matters.Crossref | GoogleScholarGoogle Scholar |
Wiens D, Rourke JP, Casper BB, Rickart EA, LaPine TR, Peterson CJ, Channing A (1983) Nonflying mammal pollination of southern African proteas: a non-coevolved system. Annals of the Missouri Botanical Garden 70, 1–31.
| Nonflying mammal pollination of southern African proteas: a non-coevolved system.Crossref | GoogleScholarGoogle Scholar |
Wooller R, Wooller S (2013) ‘Sugar and sand: the world of the honey possum.’ (Swanbrae Press: Perth, WA)
Zoeller K, Steenhuisen S, Johnson S, Midgley J (2016) New evidence for mammal pollination of Protea species (Proteaceae) based on remote-camera analysis. Australian Journal of Botany 64, 1–7.
| New evidence for mammal pollination of Protea species (Proteaceae) based on remote-camera analysis.Crossref | GoogleScholarGoogle Scholar |
