Mating strategies dictate the importance of insect visits to native plants in urban fragments
E. L. Eakin-Busher![https://orcid.org/0000-0001-8408-2055](/media/client/orcid_16x16.png)
![https://orcid.org/0000-0002-7730-9685](/media/client/orcid_16x16.png)
A Environmental and Conservation Sciences, Murdoch University, Murdoch, WA 6150, Australia.
B Corresponding author. Email: e.eakin-busher@murdoch.edu.au
Australian Journal of Botany 68(1) 26-36 https://doi.org/10.1071/BT19122
Submitted: 17 July 2019 Accepted: 17 March 2020 Published: 7 May 2020
Abstract
Plant species conservation relies on their reproductive success and likelihood of population persistence. Knowledge of plant mating systems, particularly the relationship between plants and their pollinators, is fundamental to inform conservation efforts. This knowledge could be critical for prioritising efforts in human-dominated fragmented landscapes such as the world’s biodiversity hotspots, where reproductive success can be compromised due to habitat loss, limited access to pollinators or other factors. Yet, fundamental data on plant mating systems are lacking for many Australian plants. Here we determined the mating systems of native plant species growing in native woodland fragments within Perth’s urban landscape in south-western Australia. We manipulated insect access to flowers and pollen transfer on five locally common native species, then observed floral visitors and examined reproductive success. Hemiandra pungens and Patersonia occidentalis had mixed mating systems with some ability to self-pollinate, whereas Dianella revoluta and Jacksonia sericea were reliant on insects for outcross pollination. The fruits and seeds produced by Tricoryne elatior were too low to draw conclusions about its mating system. The introduced honey bee (Apis mellifera) was the sole visitor to the mixed mating species, whereas native bees visited D. revoluta and J. sericea (one bee species each). Overall, our data suggest that D. revoluta and J. sericea are more vulnerable to fragmentation than H. pungens and P. occidentalis. Although insects contributed significantly to the reproductive output of the two former plant species, our observations suggested low frequency and richness of insect visitors to these urban fragments. More research is required to determine the generality of our findings. A comparative study in larger native woodland fragments would help estimate the effect of fragmentation on insect pollinators and consequences for the insect-reliant plant species.
Additional Keywords: floral visitors, mating systems, plant breeding systems, pollination ecology, pollinators, urban ecology.
References
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 |
Aguirre-Gutiérrez J, Biesmeijer JC, van Loon EE, Reemer M, WallisDeVries MF, Carvalheiro LG (2015) Susceptibility of pollinators to ongoing landscape changes depends on landscape history. Diversity & Distributions 21, 1129–1140.
| Susceptibility of pollinators to ongoing landscape changes depends on landscape history.Crossref | GoogleScholarGoogle Scholar |
Aizen MA, Feinsinger P (2003) Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. In ‘How Landscapes Change’. (Eds G Bradshaw, P Marquet) pp. 111–129. (Springer: Berlin, Germany)
Albrecht M, Schmid B, Hautier Y, Müller CB (2012) Diverse pollinator communities enhance plant reproductive success. Proceedings of the Royal Society of London – B. Biological Sciences 279, 4845–4852.
| Diverse pollinator communities enhance plant reproductive success.Crossref | GoogleScholarGoogle Scholar |
Andrieu E, Dornier A, Rouifed S, Schatz B, Cheptou PO (2009) The town Crepis and the country Crepis: how does fragmentation affect a plant-pollinator interaction? Acta Oecologica-International Journal of Ecology 35, 1–7.
| The town Crepis and the country Crepis: how does fragmentation affect a plant-pollinator interaction?Crossref | GoogleScholarGoogle Scholar |
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Bennett AB, Lovell S (2019) Landscape and local site variables differentially influence pollinators and pollination services in urban agricultural sites. PLoS One 14, e0212034
| Landscape and local site variables differentially influence pollinators and pollination services in urban agricultural sites.Crossref | GoogleScholarGoogle Scholar | 30759171PubMed |
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.
| Generalized linear mixed models: a practical guide for ecology and evolution.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2018) Climate statistics for Australian locations. Available at http://www.bom.gov.au/climate/dwo/IDCJDW6111.latest.shtml [Verified 31 March 2020]
Chappill JA, Wilkins CF, Crisp MD (2007) Taxonomic revision of Jacksonia (Leguminosae: Mirbelieae). Australian Systematic Botany 20, 473–623.
| Taxonomic revision of Jacksonia (Leguminosae: Mirbelieae).Crossref | GoogleScholarGoogle Scholar |
Charlesworth D (2006) Evolution of plant breeding systems. Current Biology 16, R726–R735.
| Evolution of plant breeding systems.Crossref | GoogleScholarGoogle Scholar | 16950099PubMed |
De Luca PA, Vallejo-Marín M (2013) What’s the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination. Current Opinion in Plant Biology 16, 429–435.
| What’s the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination.Crossref | GoogleScholarGoogle Scholar | 23751734PubMed |
Doull K (1973) Bees and their role in pollination. Australian Plants 7, 230–231.
Duncan D (2003) Pollination of black-anther flax lily (Dianella revoluta) in fragmented New South Wales mallee. A report to the Australian Flora Foundation. School of Botany and Zoology, Australian National University, Canberra, ACT, Australia.
Duncan DH, Nicotra AB, Cunningham SA (2004) High self-pollen transfer and low fruit set in buzz-pollinated Dianella revoluta (Phormiaceae). Australian Journal of Botany 52, 185–193.
| High self-pollen transfer and low fruit set in buzz-pollinated Dianella revoluta (Phormiaceae).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 |
Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marín M, Winn AA (2010) Plant mating systems in a changing world. Trends in Ecology & Evolution 25, 35–43.
| Plant mating systems in a changing world.Crossref | GoogleScholarGoogle Scholar |
Grass I, Jauker B, Steffan-Dewenter I, Tscharntke T, Jauker F (2018) Past and potential future effects of habitat fragmentation on structure and stability of plant–pollinator and host–parasitoid networks. Nature Ecology & Evolution 2, 1408–1417.
| Past and potential future effects of habitat fragmentation on structure and stability of plant–pollinator and host–parasitoid networks.Crossref | GoogleScholarGoogle Scholar |
Gross CL (1990) The breeding systems of three cooccurring legumes: Dillwynia hispida, D. uncinata and Pultenaea densifolia (Leguminosae, Papilionoideae). Australian Journal of Botany 38, 207–215.
| The breeding systems of three cooccurring legumes: Dillwynia hispida, D. uncinata and Pultenaea densifolia (Leguminosae, Papilionoideae).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 |
Hall MA, Nimmo DG, Cunningham SA, Walker K, Bennett AF (2019) The response of wild bees to tree cover and rural land use is mediated by species’ traits. Biological Conservation 231, 1–12.
| The response of wild bees to tree cover and rural land use is mediated by species’ traits.Crossref | GoogleScholarGoogle Scholar |
Holsinger KE (1996) Pollination biology and the evolution of mating systems in flowering plants. Evolutionary Biology 29, 107–149.
Houston TF (2000) ‘Native Bees on Wildflowers in Western Australia: a Synopsis of Native Bee Visitation of Wildflowers in Western Australia Based on the Bee Collection of the Western Australian Museum.’ (Western Australian Insect Study Society: Perth, WA, Australia)
Houston T (2018) ‘A Guide to Native Bees of Australia.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Houston TF, Ladd PG (2002) Buzz pollination in the Epacridaceae. Australian Journal of Botany 50, 83–91.
| Buzz pollination in the Epacridaceae.Crossref | GoogleScholarGoogle Scholar |
Humphreys AM, Govaerts R, Ficinski SZ, Nic Lughadha E, Vorontsova MS (2019) Global dataset shows geography and life form predict modern plant extinction and rediscovery. Nature Ecology & Evolution 3, 1043–1047.
| Global dataset shows geography and life form predict modern plant extinction and rediscovery.Crossref | GoogleScholarGoogle Scholar |
Jauker F, Jauker B, Grass I, Steffan-Dewenter I, Wolters V (2019) Partitioning wild bee and hoverfly contributions to plant–pollinator network structure in fragmented habitats. Ecology 100,
| Partitioning wild bee and hoverfly contributions to plant–pollinator network structure in fragmented habitats.Crossref | GoogleScholarGoogle Scholar | 30506556PubMed |
Johanson LG, Hoffmann AA, Walker KL, Nash MA (2019) Bees of the Victorian Alps: Network structure and interactions of introduced species. Austral Ecology 44, 245–254.
| Bees of the Victorian Alps: Network structure and interactions of introduced species.Crossref | GoogleScholarGoogle Scholar |
Kearns CA, Inouye DW (1993) Mating systems: A. Field tests for the ability to self-pollinate. In ‘Techniques for Pollination Biologists’. pp. 217–222. (University Press of Colorado: Niwot, CO, USA)
King JR (1960) The peroxidase reaction as an indicator of pollen viability. Stain Technology 35, 225–227.
Ladd PG, Yates CJ, Dillon R, Palmer R (2019) Pollination ecology of Tetratheca species from isolated, arid habitats (Banded Iron Formations) in Western Australia. Australian Journal of Botany 67, 248–255.
| Pollination ecology of Tetratheca species from isolated, arid habitats (Banded Iron Formations) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Larson BMH, 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 |
Lentini PE, Martin TG, Gibbons P, Fischer J, Cunningham SA (2012) Supporting wild pollinators in a temperate agricultural landscape: maintaining mosaics of natural features and production. Biological Conservation 149, 84–92.
| Supporting wild pollinators in a temperate agricultural landscape: maintaining mosaics of natural features and production.Crossref | GoogleScholarGoogle Scholar |
Lomov B, Keith DA, Hochuli DF (2010) Pollination and plant reproductive success in restored urban landscapes dominated by a pervasive exotic pollinator. Landscape and Urban Planning 96, 232–239.
| Pollination and plant reproductive success in restored urban landscapes dominated by a pervasive exotic pollinator.Crossref | GoogleScholarGoogle Scholar |
Loy X, Wainwright CE, Mayfield MM (2015) Asteraceae invaders have limited impacts on the pollination of common native annual species in SW Western Australia’s open woodland wildflower communities. Plant Ecology 216, 1103–1115.
| Asteraceae invaders have limited impacts on the pollination of common native annual species in SW Western Australia’s open woodland wildflower communities.Crossref | GoogleScholarGoogle Scholar |
Newman BJ, Ladd P, Brundrett M, Dixon KW (2013) Effects of habitat fragmentation on plant reproductive success and population viability at the landscape and habitat scale. Biological Conservation 159, 16–23.
| Effects of habitat fragmentation on plant reproductive success and population viability at the landscape and habitat scale.Crossref | GoogleScholarGoogle Scholar |
O’Connell LM, Mosseler A, Rajora OP (2006) Impacts of forest fragmentation on the mating system and genetic diversity of white spruce (Picea glauca) at the landscape level. Heredity 97, 418–426.
| Impacts of forest fragmentation on the mating system and genetic diversity of white spruce (Picea glauca) at the landscape level.Crossref | GoogleScholarGoogle Scholar | 16912700PubMed |
Plein M, Morris WK, Moir ML, Vesk PA (2017) Identifying species at coextinction risk when detection is imperfect: Model evaluation and case study. PLoS One 12, e0183351
| Identifying species at coextinction risk when detection is imperfect: Model evaluation and case study.Crossref | GoogleScholarGoogle Scholar | 28846734PubMed |
Popic T (2013) Pollination networks: dynamic responses to rain-driven resource pulses. PhD thesis, School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia.
Popic TJ, Wardle GM, Davila YC (2013) Flower-visitor networks only partially predict the function of pollen transport by bees. Austral Ecology 38, 76–86.
| Flower-visitor networks only partially predict the function of pollen transport by bees.Crossref | GoogleScholarGoogle Scholar |
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (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 |
Roda F, Hopkins R (2019) Correlated evolution of self and interspecific incompatibility across the range of a Texas wildflower. New Phytologist 221, 553–564.
| Correlated evolution of self and interspecific incompatibility across the range of a Texas wildflower.Crossref | GoogleScholarGoogle Scholar | 29992588PubMed |
Stephenson AG, Good SV, Vogler DW (2000) Interrelationships among inbreeding depression, plasticity in the self-incompatibility system, and the breeding system of Campanula rapunculoides L. (Campanulaceae). Annals of Botany 85, 211–219.
| Interrelationships among inbreeding depression, plasticity in the self-incompatibility system, and the breeding system of Campanula rapunculoides L. (Campanulaceae).Crossref | GoogleScholarGoogle Scholar |
Teixido AL, Aizen MA (2019) Reproductive assurance weakens pollinator-mediated selection on flower size in an annual mixed-mating species. Annals of Botany 123, 1067–1077.
| Reproductive assurance weakens pollinator-mediated selection on flower size in an annual mixed-mating species.Crossref | GoogleScholarGoogle Scholar | 30778517PubMed |
Toon A, Cook LG, Crisp MD (2014) Evolutionary consequences of shifts to bird-pollination in the Australian pea-flowered legumes (Mirbelieae and Bossiaeeae). BMC Evolutionary Biology 14, 43
| Evolutionary consequences of shifts to bird-pollination in the Australian pea-flowered legumes (Mirbelieae and Bossiaeeae).Crossref | GoogleScholarGoogle Scholar | 24602227PubMed |
Wade MR, Zalucki MP, Franzmann BA (2005) Influence of observer presence on Pacific damsel bug behavior: who is watching whom? Journal of Insect Behavior 18,
| Influence of observer presence on Pacific damsel bug behavior: who is watching whom?Crossref | GoogleScholarGoogle Scholar |
Yates CJ, Hopper SD, Taplin RH (2005) Native insect flower visitor 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.
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) ‘Mixed Effects Models and Extensions in Ecology with R.’ (Springer Science+Business Media: New York City, NY, USA)