Local population density affects pollinator visitation in the endangered grassland daisy Rutidosis leptorhynchoides (Asteraceae)
Ben Courtice A C , Susan E. Hoebee A , Steve Sinclair B and John W. Morgan AA Department of Environment, Ecology and Evolution, La Trobe University, Bundoora, Vic. 3086, Australia.
B Arthur Rylah Institute for Environmental Research, Victorian State Government Department of Environment, Land, Water and Planning, 123 Brown Street, Heidelberg, Vic. 3084, Australia.
C Corresponding author. Email: bencourtice.bze@gmail.com
Australian Journal of Botany 67(8) 638-648 https://doi.org/10.1071/BT18243
Submitted: 21 December 2018 Accepted: 3 February 2020 Published: 2 March 2020
Abstract
The spatial arrangement of plants has implications for their pollination. Dense patches of flowering plants can result in increased pollinator attraction and, consequently, higher pollination and seed set per flower. We investigated this effect in the endangered, self-incompatible Australian daisy Rutidosis leptorhynchoides F.Muell. (Asteraceae) by quantifying the effect of plant density on pollinator visitation and seed set in a wild population. Pollinator activity was investigated by direct observation of insect behaviour, by examining the pollen carried on candidate insect species, by video monitoring of visitation, and by tracking the movement of dye as a pollen analogue. Two native Lasioglossum species (Hymenoptera: Halictidae) were identified as the most frequent pollen-carrying visitors to inflorescences. Their visitation was significantly higher where plants were dense, but no statistical correlation between seed set and plant density was found. Florivory was identified as potentially having a substantial negative influence on seed set, but without any clear relationship to plant density. Given that R. leptorhynchoides has declined substantially across its range, and previous reintroduction attempts have often failed, our findings provide key information pertaining to knowledge of pollinator and florivore behaviour in relation to plant density. To maximise success of future management strategies, these animal-plant interactions should be captured in species recovery designs.
Additional keywords: Allee effects, density dependence, endangered species, florivory, pollination, Rutidosis leptorrhynchoides.
References
ACT Government (2017). ‘Button wrinklewort.’ Threatened species action plans. Available at https://www.environment.act.gov.au/cpr/conservation_and_ecological_communities/threatened_species_action_plans [Verified 5 February 2020]Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9, 968–980.
| Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 16913941PubMed |
Akter A, Biella P, Klecka J (2017) Effects of small-scale clustering of flowers on pollinator foraging behaviour and flower visitation rate. PLoS One 12, e0187976
| Effects of small-scale clustering of flowers on pollinator foraging behaviour and flower visitation rate.Crossref | GoogleScholarGoogle Scholar | 29136042PubMed |
Ancheta L, Heard SB (2011) Impacts of insect herbivores on rare plant populations. Biological Conservation 144, 2395–2402.
| Impacts of insect herbivores on rare plant populations.Crossref | GoogleScholarGoogle Scholar |
Antos M, Williams NS (2015) The wildlife of our grassy landscapes. In ‘Land of sweeping plains: managing and restoring the native grasslands of south-eastern Australia’. (Eds NS Williams, A Marshall, JW Morgan) pp. 87–114. (CSIRO Publishing: Melbourne, Vic., Australia)
APSA Members (2007) ‘Australasian pollen and spore atlas V1.0.’ Australian National University. Available at http://apsa.anu.edu.au [Verified 5 February 2020]
Bateman AJ (1956) Cryptic self-incompatibility in the wallflower: Cheiranthus cheiri L. Heredity 10, 257–261.
| Cryptic self-incompatibility in the wallflower: Cheiranthus cheiri L.Crossref | GoogleScholarGoogle Scholar |
Bommarco R, Biesmeijer JC, Meyer B, Potts SG, Pöyry J, Roberts SP, Steffan-Dewenter I, Öckinger E (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proceedings of the Royal Society B 277, 2075–2082.
| Dispersal capacity and diet breadth modify the response of wild bees to habitat loss.Crossref | GoogleScholarGoogle Scholar | 20219735PubMed |
Bosch M, Waser NM (1999) Effects of local density on pollination and reproduction in Delphinium nuttallianum and Aconitum columbianum (Ranunculaceae). American Journal of Botany 86, 871–879.
| Effects of local density on pollination and reproduction in Delphinium nuttallianum and Aconitum columbianum (Ranunculaceae).Crossref | GoogleScholarGoogle Scholar | 10371728PubMed |
Bosch M, Waser NM (2001) Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126, 76–83.
| Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs.Crossref | GoogleScholarGoogle Scholar | 28547440PubMed |
Bureau of Meteorology (2018) ‘087031 Laverton RAAF VIC’. Climate Data Online. Available at http://www.bom.gov.au/climate/data/ [Verified 23 April 2018]
Byers DL, Meagher TR (1992) Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68, 353–359.
| Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility.Crossref | GoogleScholarGoogle Scholar |
Chu C-J, Maestre FT, Xiao S, Weiner J, Wang Y-S, Duan Z-H, Wang G (2008) Balance between facilitation and resource competition determines biomass-density relations in plant populations. Ecology Letters 11, 1189–1197.
| Balance between facilitation and resource competition determines biomass-density relations in plant populations.Crossref | GoogleScholarGoogle Scholar | 18684118PubMed |
Commander LE, Coates DJ, Broadhurst L, Offord C, Makinson RO, Matthes M (2018) ‘Guidelines for the translocation of threatened plants in Australia.’ (3rd edn) (Australian Network for Plant Conservation: Canberra, ACT, Australia)
de Jong TJ, Klinkhamer PGL (1989) Limiting factors for seed production in Cynoglossum officinale. Oecologia 80, 167–172.
| Limiting factors for seed production in Cynoglossum officinale.Crossref | GoogleScholarGoogle Scholar | 28313102PubMed |
de Waal C, Anderson B, Ellis AG (2015) Relative density and dispersion pattern of two southern African Asteraceae affect fecundity through heterospecific interference and mate availability, not pollinator visitation rate. Journal of Ecology 103, 513–525.
| Relative density and dispersion pattern of two southern African Asteraceae affect fecundity through heterospecific interference and mate availability, not pollinator visitation rate.Crossref | GoogleScholarGoogle Scholar |
Department of Agriculture, Water and the Environment (2019) ‘EPBC Act list of threatened flora’. Australian Government, Species Profile and Threats Database. Available at http://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl?wanted=flora [Verified 13 February 2020]
Dixon KW (2009) Pollination and restoration. Science 325, 571–573.
| Pollination and restoration.Crossref | GoogleScholarGoogle Scholar | 19644110PubMed |
Feldman TS (2006) Pollinator aggregative and functional responses to flower density: does pollinator response to patches of plants accelerate at low-densities? Oikos 115, 128–140.
| Pollinator aggregative and functional responses to flower density: does pollinator response to patches of plants accelerate at low-densities?Crossref | GoogleScholarGoogle Scholar |
Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biological Reviews of the Cambridge Philosophical Society 80, 413–443.
| Pollen and seed dispersal among dispersed plants.Crossref | GoogleScholarGoogle Scholar | 16094807PubMed |
Goulson D, Stout JC, Kells AR (2002) Do exotic bumblebees and honeybees compete with native flower-visiting insects in Tasmania? Journal of Insect Conservation 6, 179–189.
| Do exotic bumblebees and honeybees compete with native flower-visiting insects in Tasmania?Crossref | GoogleScholarGoogle Scholar |
Gross CL (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 |
Hobbs RJ, Yates CJ (2003) Impacts of ecosystem fragmentation on plant populations: generalising the idiosyncratic. Australian Journal of Botany 51, 471–488.
| Impacts of ecosystem fragmentation on plant populations: generalising the idiosyncratic.Crossref | GoogleScholarGoogle Scholar |
Hoebee SE, Thrall PH, Young AG (2008) Integrating population demography, genetics and self-incompatibility in a viability assessment of the Wee Jasper Grevillea (Grevillea iaspicula McGill., Proteaceae). Conservation Genetics 9, 515–529.
| Integrating population demography, genetics and self-incompatibility in a viability assessment of the Wee Jasper Grevillea (Grevillea iaspicula McGill., Proteaceae).Crossref | GoogleScholarGoogle Scholar |
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant–pollinator interactions. Annual Review of Ecology and Systematics 29, 83–112.
| Endangered mutualisms: the conservation of plant–pollinator interactions.Crossref | GoogleScholarGoogle Scholar |
Kim TN, Underwood N (2015) Plant neighborhood effects on herbivory: damage is both density and frequency dependent. Ecology 96, 1431–1437.
| Plant neighborhood effects on herbivory: damage is both density and frequency dependent.Crossref | GoogleScholarGoogle Scholar | 26236855PubMed |
Kirchner F, Luijten SH, Imbert E, Riba M, Mayol M, González-Martínez SC, Mignot A, Colas B (2005) Effects of local density on insect visitation and fertilization success in the narrow-endemic Centaurea corymbosa (Asteraceae). Oikos 111, 130–142.
| Effects of local density on insect visitation and fertilization success in the narrow-endemic Centaurea corymbosa (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Kunin WE (1993) Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 74, 2145–2160.
| Sex and the single mustard: population density and pollinator behavior effects on seed-set.Crossref | GoogleScholarGoogle Scholar |
Kunin WE (1997) Population biology and rarity: on the complexity of density dependence in insect–plant interactions. In ‘The biology of rarity’. (Eds WE Kunin, KJ Gaston) pp. 150–173. (Springer: Dordrecht, The Netherlands)
Kwak MM, Velterop O, Andel J (1998) Pollen and gene flow in fragmented habitats. Applied Vegetation Science 1, 37–54.
| Pollen and gene flow in fragmented habitats.Crossref | GoogleScholarGoogle Scholar |
Levin DA, Kelley CD, Sarkar S (2009) Enhancement of Allee effects in plants due to self-incompatibility alleles. Journal of Ecology 97, 518–527.
| Enhancement of Allee effects in plants due to self-incompatibility alleles.Crossref | GoogleScholarGoogle Scholar |
McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecology Letters 9, 1351–1365.
| Florivory: the intersection of pollination and herbivory.Crossref | GoogleScholarGoogle Scholar | 17118009PubMed |
McDougall K, Kirkpatrick JB (1994) ‘Conservation of lowland native grasslands in south-eastern Australia.’ (World Wide Fund for Nature: Sydney, NSW, Australia)
Morgan JW (1995) Ecological studies of the endangered Rutidosis leptorrhynchoides. I. Seed production, soil seed bank dynamics, population density and their effects on recruitment. Australian Journal of Botany 43, 1–11.
| Ecological studies of the endangered Rutidosis leptorrhynchoides. I. Seed production, soil seed bank dynamics, population density and their effects on recruitment.Crossref | GoogleScholarGoogle Scholar |
Morgan JW (1997) The effect of grassland gap size on establishment, growth and flowering of the endangered Rutidosis leptorrhynchoides (Asteraceae). Journal of Applied Ecology 34, 566–576.
| The effect of grassland gap size on establishment, growth and flowering of the endangered Rutidosis leptorrhynchoides (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Morgan JW (1998) Importance of canopy gaps for recruitment of some forbs in Themeda triandra-dominated grasslands in south-eastern Australia. Australian Journal of Botany 46, 609–627.
| Importance of canopy gaps for recruitment of some forbs in Themeda triandra-dominated grasslands in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Morgan JW (1999a) Effects of population size on seed production and germinability in an endangered, fragmented grassland plant. Conservation Biology 13, 266–273.
| Effects of population size on seed production and germinability in an endangered, fragmented grassland plant.Crossref | GoogleScholarGoogle Scholar |
Morgan JW (1999b) Have tubestock plantings successfully established populations of rare grassland species into reintroduction sites in western Victoria? Biological Conservation 89, 235–243.
| Have tubestock plantings successfully established populations of rare grassland species into reintroduction sites in western Victoria?Crossref | GoogleScholarGoogle Scholar |
Morgan JW, Scacco PJ (2006) Planting designs in ecological restoration: insights from the button wrinklewort. Ecological Management & Restoration 7, 51–54.
| Planting designs in ecological restoration: insights from the button wrinklewort.Crossref | GoogleScholarGoogle Scholar |
Morgan JW, Meyer MJ, Young AG (2013) Severe habitat fragmentation leads to declines in genetic variation, mate availability, and reproductive success in small populations of a once-common Australian grassland daisy. International Journal of Plant Sciences 174, 1209–1218.
| Severe habitat fragmentation leads to declines in genetic variation, mate availability, and reproductive success in small populations of a once-common Australian grassland daisy.Crossref | GoogleScholarGoogle Scholar |
Neal PR (1998) Pollinator restoration. Trends in Ecology & Evolution 13, 132–133.
| Pollinator restoration.Crossref | GoogleScholarGoogle Scholar |
Orford KA, Vaughan IP, Memmott J (2015) The forgotten flies: the importance of non-syrphid Diptera as pollinators. Proceedings. Biological Sciences 282, 20142934
| The forgotten flies: the importance of non-syrphid Diptera as pollinators.Crossref | GoogleScholarGoogle Scholar | 25808886PubMed |
Osborne JL, Williams IH (2001) Site constancy of bumble bees in an experimentally patchy habitat. Agriculture, Ecosystems & Environment 83, 129–141.
| Site constancy of bumble bees in an experimentally patchy habitat.Crossref | GoogleScholarGoogle Scholar |
PaDIL (2018) ‘Australian pollinators’. PaDIL. Available at http://www.padil.gov.au/pollinators [Verified 5 February 2020]
Prober SM, Spindler LH, Brown AH (1998) Conservation of the grassy white box woodlands: effects of remnant population size on genetic diversity in the allotetraploid herb Microseris lanceolata. Conservation Biology 12, 1279–1290.
| Conservation of the grassy white box woodlands: effects of remnant population size on genetic diversity in the allotetraploid herb Microseris lanceolata.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2016) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/ [Verified 5 February 2020]
Richards AJ (1997) ‘Plant breeding systems.’ (Garland Science: New York, NY, USA)
Roll J, Mitchell RJ, Cabin RJ, Marshall DL (1997) Reproductive success increases with local density of conspecifics in a desert mustard (Lesquerella fendleri). Conservation Biology 11, 738–746.
| Reproductive success increases with local density of conspecifics in a desert mustard (Lesquerella fendleri).Crossref | GoogleScholarGoogle Scholar |
Scarlett NH, Parsons RF (1990) Conservation biology of the southern Australian daisy Rutidosis leptorrhynchoides. In ‘Management and conservation of small populations’. (Eds TW Clark, JH Seebeck) pp. 195–205. (Chicago Zoological Society: Chicago, IL, USA)
Schmidt-Lebuhn AN, Marshall DJ, Dreis B, Young AG (2018) Genetic rescue in a plant polyploid complex: case study on the importance of genetic and trait data for conservation management. Ecology and Evolution 8, 5153–5163.
| Genetic rescue in a plant polyploid complex: case study on the importance of genetic and trait data for conservation management.Crossref | GoogleScholarGoogle Scholar | 29876089PubMed |
Steffan-Dewenter I, Klein A, Gaebele V, Alfert T, Tscharntke T (2006) Bee diversity and plant-pollinator interactions in fragmented landscapes. In ‘Plant–pollinator interactions’. (Eds NM Waser, J Ollerton) pp. 387–407. (University of Chicago Press: Chicago, IL, USA)
Steven JC, Rooney TP, Boyle OD, Waller DM (2003) Density-dependent pollinator visitation and self-incompatibility in upper Great Lakes populations of Trillium grandiflorum. The Journal of the Torrey Botanical Society 130, 23–29.
| Density-dependent pollinator visitation and self-incompatibility in upper Great Lakes populations of Trillium grandiflorum.Crossref | GoogleScholarGoogle Scholar |
Stuwe J, Parsons RF (1977) Themeda australis grasslands on the Basalt Plains, Victoria: floristics and management effects. Australian Journal of Ecology 2, 467–476.
| Themeda australis grasslands on the Basalt Plains, Victoria: floristics and management effects.Crossref | GoogleScholarGoogle Scholar |
Thomson JD (1981) Spatial and temporal components of resource assessment by flower-feeding insects. Journal of Animal Ecology 50, 49–59.
| Spatial and temporal components of resource assessment by flower-feeding insects.Crossref | GoogleScholarGoogle Scholar |
Thomson JD, Price MV, Waser NM, Stratton DA (1986) Comparative studies of pollen and fluorescent dye transport by bumble bees visiting Erythronium grandiflorum. Oecologia 69, 561–566.
| Comparative studies of pollen and fluorescent dye transport by bumble bees visiting Erythronium grandiflorum.Crossref | GoogleScholarGoogle Scholar | 28311616PubMed |
Threlfall CG, Walker K, Williams NS, Hahs AK, Mata L, Stork N, Livesley SJ (2015) The conservation value of urban green space habitats for Australian native bee communities. Biological Conservation 187, 240–248.
| The conservation value of urban green space habitats for Australian native bee communities.Crossref | GoogleScholarGoogle Scholar |
Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Annual Review of Entomology 49, 405–430.
| Plant-insect interactions in fragmented landscapes.Crossref | GoogleScholarGoogle Scholar | 14651470PubMed |
Wahren CHA, Papst WA, Williams RJ (1994) Long-term vegetation change in relation to cattle grazing in subalpine grassland and heathland on the Bogong High Plains: an analysis of vegetation records from 1945 to 1994. Australian Journal of Botany 42, 607–639.
| Long-term vegetation change in relation to cattle grazing in subalpine grassland and heathland on the Bogong High Plains: an analysis of vegetation records from 1945 to 1994.Crossref | GoogleScholarGoogle Scholar |
Waser NM, Real LA (1979) Effective mutualism between sequentially flowering plant species. Nature 281, 670–672.
| Effective mutualism between sequentially flowering plant species.Crossref | GoogleScholarGoogle Scholar |
Wells GP, Young AG (2002) Effects of seed dispersal on spatial genetic structure in populations of Rutidosis leptorrhychoides with different levels of correlated paternity. Genetical Research 79, 219–226.
| Effects of seed dispersal on spatial genetic structure in populations of Rutidosis leptorrhychoides with different levels of correlated paternity.Crossref | GoogleScholarGoogle Scholar | 12220129PubMed |
Williams NS, McDonnell MJ, Seager EJ (2005) Factors influencing the loss of an endangered ecosystem in an urbanising landscape: a case study of native grasslands from Melbourne, Australia. Landscape and Urban Planning 71, 35–49.
| Factors influencing the loss of an endangered ecosystem in an urbanising landscape: a case study of native grasslands from Melbourne, Australia.Crossref | GoogleScholarGoogle Scholar |
Young AG, Pickup M (2010) Low S-allele numbers limit mate availability, reduce seed set and skew fitness in small populations of a self-incompatible plant. Journal of Applied Ecology 47, 541–548.
| Low S-allele numbers limit mate availability, reduce seed set and skew fitness in small populations of a self-incompatible plant.Crossref | GoogleScholarGoogle Scholar |
Young AG, Brown AHD, Murray AG, Thrall PH, Miller CH (2000) Genetic erosion, restricted mating, and reduced viability in the endangered grassland herb Rutidosis leptorrhynchoides. In ‘Genetics, demography and viability of fragmented populations’. (Eds AG Young, GM Clarke, G Cowlishaw) pp. 335–359. (Cambridge University Press: Cambridge, UK)
Zeeman BJ, McDonnell MJ, Kendal D, Morgan JW (2017) Biotic homogenization in an increasingly urbanized temperate grassland ecosystem. Journal of Vegetation Science 28, 550–561.
| Biotic homogenization in an increasingly urbanized temperate grassland ecosystem.Crossref | GoogleScholarGoogle Scholar |