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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE (Open Access)

Improving weed management by targeting the seed ecology of blackberry (Rubus anglocandicans) in a biodiversity hotspot

Caroline Delaisse https://orcid.org/0000-0003-1306-5797 A B C , Paul B. Yeoh https://orcid.org/0000-0002-6233-5901 A , Raphael K. Didham https://orcid.org/0000-0001-6685-7005 A B , Wolfgang Lewandrowski https://orcid.org/0000-0002-7496-7690 B D , John K. Scott https://orcid.org/0000-0002-8303-9706 A B and Bruce L. Webber https://orcid.org/0000-0001-5934-6557 A B E *
+ Author Affiliations
- Author Affiliations

A CSIRO Health & Biosecurity, Private Bag 5, Wembley PO, Wembley, WA 6913, Australia.

B School of Biological Sciences, University of Western Australia, Crawley, WA 6009, Australia.

C CSIRO Health & Biosecurity, PO Box 1700, Canberra, ACT 2601, Australia.

D Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kattidj Close, Kings Park, WA 6009, Australia.

E Western Australian Biodiversity Science Institute, 133 St Georges Terrace, Perth, WA 6000, Australia.

* Correspondence to: bruce.webber@csiro.au

Handling Editor: Grant Wardell-Johnson

Australian Journal of Botany 71(1) 28-42 https://doi.org/10.1071/BT22041
Submitted: 26 April 2022  Accepted: 20 January 2023   Published: 20 February 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC)

Abstract

Context: Germination is a vulnerable life stage for plants, therefore understanding the dynamics of seed ecology is essential to guiding management recommendations for highly invasive weeds.

Aim: We addressed the knowledge gap for how seeds contribute to the invasion process for European blackberry (Rubus anglocandicans), a threatening weed across the riparian ecosystems of south-western Australia.

Methods: We performed mechanical, chemical and thermal treatments on seeds to test for changes in germination success and conducted seed-burial trials to monitor seed viability over time in the soil seedbank.

Key results: In germination trials, freshly picked and frugivore egested seeds failed to germinate with the endocarp intact. With the endocarp removed, germination remained lower at 4–6 months compared with 10–28 months after collection, indicating a significant after-ripening period. Seeds in intact endocarps survived water immersion for more than 2 months, indicating an ability to survive winter flooding. Acid immersion did not improve germination. The germination success of seeds with endocarp removed increased linearly above 11°C, was greatest at 30°C and thereafter declined rapidly (no survival at 40°C). In a 5-year seed-burial trial, germination varied from 7.6 to 48.4% and was significantly lower closer to a river, and in areas where ‘blackberry decline’ syndrome was present.

Conclusions: While germination of seed without its pyrene coat occurred over a range of controlled conditions, the natural processes needed to break the pyrene remain unknown.

Implications: High germination success and the long-term survival of seeds in soil clarifies that the management of blackberry remains a difficult challenge in Australia.

Keywords: after-ripening, bet hedging, dormancy, ecophysiology, frugivory, invasive species, riparian restoration, seedbank, seed germination, seed persistence.


References

Aghighi S, Hardy GESJ, Scott JK, Burgess TI (2012) Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia. European Journal of Plant Pathology 133, 841–855.
Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Aghighi S, Fontanini L, Yeoh PB, Hardy GESJ, Burgess TI, Scott JK (2014) A conceptual model to describe the decline of European blackberry (Rubus anglocandicans), a weed of national significance in Australia. Plant Disease 98, 580–589.
A conceptual model to describe the decline of European blackberry (Rubus anglocandicans), a weed of national significance in Australia.Crossref | GoogleScholarGoogle Scholar |

Amor RL (1974) Ecology and control of blackberry (Rubus fruticosus L. agg.). II. Reproduction. Weed Research 14, 231–238.
Ecology and control of blackberry (Rubus fruticosus L. agg.). II. Reproduction.Crossref | GoogleScholarGoogle Scholar |

Amor RL, Richardson RG, Pritchard GH, Bruzzese E (1998) Rubus fruticosus L. agg. In ‘The biology of Australian weeds’. Vol. 2. (Eds FD Panetta, RH Groves, RCH Shepherd) pp. 225–246. (RG and FJ Richardson: Melbourne, Vic., Australia)

Andrewartha HG, Birch LC (1954) ‘The distribution and abundance of animals.’ (University of Chicago Press: Chicago, IL, USA)

Asante SK, Danthanarayana W, Heatwole H (1991) Bionomics and population-growth statistics of apterous virginoparae of woolly apple aphid (Eriosoma lanigerum) at constant temperatures. Entomologia Experimentalis et Applicata 60, 261–270.
Bionomics and population-growth statistics of apterous virginoparae of woolly apple aphid (Eriosoma lanigerum) at constant temperatures.Crossref | GoogleScholarGoogle Scholar |

Baskin CC, Baskin JM (1998) ‘Seeds ecology, biogeography, and evolution of dormancy and germination.’ (Academic Press: San Diego, CA, USA)

Baskin CC, Baskin JM (2014) ‘Seeds ecology, biogeography, and evolution of dormancy and germination.’ 2nd edn. (Academic Press: San Diego, CA, USA)

Bates D, Mächler 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 |

Bell DT (1994) Interaction of fire, temperature and light in the germination response of 16 species from the Eucalyptus marginata forest of south-western Western Australia. Australian Journal of Botany 42, 501–509.
Interaction of fire, temperature and light in the germination response of 16 species from the Eucalyptus marginata forest of south-western Western Australia.Crossref | GoogleScholarGoogle Scholar |

Bell DT, Rokich DP, McChesney CJ, Plummer JA (1995) Effects of temperature, light and gibberellic acid on the germination of seeds of 43 species native to Western Australia. Journal of Vegetation Science 6, 797–806.
Effects of temperature, light and gibberellic acid on the germination of seeds of 43 species native to Western Australia.Crossref | GoogleScholarGoogle Scholar |

Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) ‘Seeds physiology of development, germination and dormancy.’ 3rd edn. (Springer: New York, NY, USA)

Bradshaw CJA, Hoskins AJ, Haubrock PJ, et al. (2021) Detailed assessment of the reported economic costs of invasive species in Australia. NeoBiota 67, 511–550.
Detailed assessment of the reported economic costs of invasive species in Australia.Crossref | GoogleScholarGoogle Scholar |

Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9, 378–400.
glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling.Crossref | GoogleScholarGoogle Scholar |

Brunner H, Harris RV, Amor RL (1976) A note on the dispersal of seeds of blackberry (Rubus procerus P.J. Muell.) by foxes and emus. Weed Research 16, 171–173.
A note on the dispersal of seeds of blackberry (Rubus procerus P.J. Muell.) by foxes and emus.Crossref | GoogleScholarGoogle Scholar |

Buddenhagen CE, Tye A (2015) Lessons from successful plant eradications in Galapagos: commitment is crucial. Biological Invasions 17, 2893–2912.
Lessons from successful plant eradications in Galapagos: commitment is crucial.Crossref | GoogleScholarGoogle Scholar |

Burnham KP, Anderson DR (2002) ‘Model selection and inference: a practical information-theoretical approach.’ 2nd edn. (Springer-Verlag)

Choi GE, Ghimire B, Lee H, et al. (2016) Scarification and stratification protocols for breaking dormancy of Rubus (Rosaceae) species in Korea. Seed Science and Technology 44, 239–252.
Scarification and stratification protocols for breaking dormancy of Rubus (Rosaceae) species in Korea.Crossref | GoogleScholarGoogle Scholar |

Clark LV, Evans KJ, Jasieniuk M (2013) Origins and distribution of invasive Rubus fruticosus L. agg. (Rosaceae) clones in the Western United States. Biological Invasions 15, 1331–1342.
Origins and distribution of invasive Rubus fruticosus L. agg. (Rosaceae) clones in the Western United States.Crossref | GoogleScholarGoogle Scholar |

Davies SJJF (1978) Food of emus. Australian Journal of Ecology 3, 411–422.
Food of emus.Crossref | GoogleScholarGoogle Scholar |

Dixon KW, Merritt DJ, Flematti GR, Ghisalberti EL (2009) Karrikinolide – a phytoreactive compound derived from smoke with applications in horticulture, ecological restoration and agriculture. ISHS Acta Horticulturae 813, 155–170. https://doi.org/10.17660/ActaHortic.2009.813.20

Evans KJ, Weber HE (2003) Rubus anglocandicans (Rosaceae) is the most widespread taxon of European blackberry in Australia. Australian Systematic Botany 16, 527–537.
Rubus anglocandicans (Rosaceae) is the most widespread taxon of European blackberry in Australia.Crossref | GoogleScholarGoogle Scholar |

Evans KJ, Symon DE, Whalen MA, Hosking JR, Barker RM, Oliver JA (2007) Systematics of the Rubus fruticosus aggregate (Rosaceae) and other exotic Rubus taxa in Australia. Australian Systematic Botany 20, 187–251.
Systematics of the Rubus fruticosus aggregate (Rosaceae) and other exotic Rubus taxa in Australia.Crossref | GoogleScholarGoogle Scholar |

Fedriani JM, Delibes M (2009) Functional diversity in fruit-frugivore interactions: a field experiment with Mediterranean mammals. Ecography 32, 983–992.
Functional diversity in fruit-frugivore interactions: a field experiment with Mediterranean mammals.Crossref | GoogleScholarGoogle Scholar |

Gallagher RS (2000) ‘Seeds: the ecology of regeneration in plant communities.’ 3rd edn. (CAB International: Wallingford, UK)

García-Rodriguez A, Albrecht J, Szczutkowska S, Valido A, Farwig N, Selva N (2021) The role of the brown bear Ursus arctos as a legitimate megafaunal seed disperser. Scientific Reports 11, 1282
The role of the brown bear Ursus arctos as a legitimate megafaunal seed disperser.Crossref | GoogleScholarGoogle Scholar |

Greet J, Webb JA, Cousens RD (2015) Floods reduce the prevalence of exotic plant species within the riparian zone: evidence from natural floods. Applied Vegetation Science 18, 503–512.
Floods reduce the prevalence of exotic plant species within the riparian zone: evidence from natural floods.Crossref | GoogleScholarGoogle Scholar |

Hancock CN, Ladd PG, Froend RH (1996) Biodiversity and management of riparian vegetation in Western Australia. Forest Ecology and Management 85, 239–250.
Biodiversity and management of riparian vegetation in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Herd RM (1985) Anatomy and histology of the gut of the emu Dromaius novaehollandiae. Emu – Austral Ornithology 85, 43–46.
Anatomy and histology of the gut of the emu Dromaius novaehollandiae.Crossref | GoogleScholarGoogle Scholar |

Herd RM, Dawson TJ (1984) Fiber digestion in the emu, Dromaius novaehollandiae, a large bird with a simple gut and high-rates of passage. Physiological Zoology 57, 70–84.
Fiber digestion in the emu, Dromaius novaehollandiae, a large bird with a simple gut and high-rates of passage.Crossref | GoogleScholarGoogle Scholar |

Hope P, Abbs D, Bhend J, Chiew F, Church J, Ekström M, Kirono D, Lenton A, Lucas C, McInnes K, Moise A, Monselesan D, Mpelasoka F, Timbal B, Webb L, Whetton P (2015) ‘Southern and south-western flatlands cluster report. Climate change in Australia. Projections for Australia’s NRM regions.’ (Eds M Ekström, P Whetton, C Gerbing, M Grose, L Webb, J Risbey) (CSIRO and Bureau of Meteorology: Canberra, ACT, Australia) Available at https://www.climatechangeinaustralia.gov.au/media/ccia/2.2/cms_page_media/168/SSWFLATLANDS_CLUSTER_REPORT.pdf

Hoyle GL, Daws MI, Steadman KJ, Adkins SW (2008) Mimicking a semi-arid tropical environment achieves dormancy alleviation for seeds of Australian native Goodeniaceae and Asteraceae. Annals of Botany 101, 701–708.
Mimicking a semi-arid tropical environment achieves dormancy alleviation for seeds of Australian native Goodeniaceae and Asteraceae.Crossref | GoogleScholarGoogle Scholar |

Jacobs B, Donoghue MJ, Bouman F, Huysmans S, Smets E (2008) Evolution and phylogenetic importance of endocarp and seed characters in Viburnum (Adoxaceae). International Journal of Plant Sciences 169, 409–431.
Evolution and phylogenetic importance of endocarp and seed characters in Viburnum (Adoxaceae).Crossref | GoogleScholarGoogle Scholar |

Keith D (1996) Fire-driven extinction of plant populations: a synthesis of theory and review of evidence from Australian vegetation. Proceedings of the Linnean Society of New South Wales 116, 37–78.

Lasheen AM, Blackhurst HT (1956) Biochemical changes associated with dormancy and after-ripening of blackberry seed. Proceedings of the American Society for Horticultural Science 67, 331–340.

Long RL, Gorecki MJ, Renton M, et al. (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biological Reviews 90, 31–59.
The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise.Crossref | GoogleScholarGoogle Scholar |

Lüdecke D, Ben-Shachar MS, Patil I, Waggoner P, Makowsk D (2021) performance: an R package for assessment, comparison and testing of statistical models. Journal of Open Source Software 6, 3139
performance: an R package for assessment, comparison and testing of statistical models.Crossref | GoogleScholarGoogle Scholar |

Mian MAR, Skirvin RM, Norton MA, Otterbacher AG (1995) Drying interferes with germination of blackberry (Rubus sp.) seeds in vitro. HortScience 30, 124–126.
Drying interferes with germination of blackberry (Rubus sp.) seeds in vitro.Crossref | GoogleScholarGoogle Scholar |

Molefe KL, Tedder MJ, Thabethe V, Rushworth I, Downs CT (2020) Role of native avian frugivores in germination facilitation and potential dispersal of invasive American bramble (Rubus cuneifolius) in South Africa. Biological Invasions 22, 1109–1120.
Role of native avian frugivores in germination facilitation and potential dispersal of invasive American bramble (Rubus cuneifolius) in South Africa.Crossref | GoogleScholarGoogle Scholar |

Moore JN, Brown GR, Lundergan C (1974) Effect of duration of acid scarification on endocarp thickness and seedling emergence of blackberries. HortScience 9, 204–205.
Effect of duration of acid scarification on endocarp thickness and seedling emergence of blackberries.Crossref | GoogleScholarGoogle Scholar |

Morin L, Evans KJ (2012) Rubus fruticosus L. aggregate – European blackberry. In ‘Biological control of weeds in Australia’. (Eds M Julien, R McFadyen, J Cullen) pp. 499–509. (CSIRO Publishing: Melbourne, Vic., Australia)

Muggeo VMR (2008) segmented: an R package to fit regression models with broken-line relationships. R News 8, 20–25.

Muggeo VMR (2017) Interval estimation for the breakpoint in segmented regression: a smoothed score-based approach. Australian & New Zealand Journal of Statistics 59, 311–322.
Interval estimation for the breakpoint in segmented regression: a smoothed score-based approach.Crossref | GoogleScholarGoogle Scholar |

Nesme X (1985) Respective effects of endocarp, testa and endosperm, and embryo on the germination of raspberry (Rubus idaeus L.) seeds. Canadian Journal of Plant Science 65, 125–130.
Respective effects of endocarp, testa and endosperm, and embryo on the germination of raspberry (Rubus idaeus L.) seeds.Crossref | GoogleScholarGoogle Scholar |

Nybom H (1980) Germination in Swedish blackberries (Rubus L. subgenus Rubus). Botaniska Notiser 133, 619–631.

Nybom H (1987) A demographic study of the apomictic blackberry, Rubus nessensis (Rosaceae). Nordic Journal of Botany 7, 365–372.
A demographic study of the apomictic blackberry, Rubus nessensis (Rosaceae).Crossref | GoogleScholarGoogle Scholar |

Packer JG, Delean S, Kueffer C, Prider J, Abley K, Facelli JM, Carthew SM (2016) Native faunal communities depend on habitat from non-native plants in novel but not in natural ecosystems. Biodiversity and Conservation 25, 503–523.
Native faunal communities depend on habitat from non-native plants in novel but not in natural ecosystems.Crossref | GoogleScholarGoogle Scholar |

Panetta FD (2004) Seed banks: the bane of the weed eradicator. In ‘Proceedings of the 14th Australian Weeds Conference’, 6–9 September 2004, Wagga Wagga, NSW, Australia. (Eds BM Sindel, SB Johnson) pp. 523–526. (Weed Society of New South Wales)

Renteria JL, Gardener MR, Panetta FD, Crawley MJ (2012) Management of the Invasive Hill Raspberry (Rubus niveus) on Santiago Island, Galapagos: eradication or indefinite control? Invasive Plant Science and Management 5, 37–46.
Management of the Invasive Hill Raspberry (Rubus niveus) on Santiago Island, Galapagos: eradication or indefinite control?Crossref | GoogleScholarGoogle Scholar |

Rose RC (1919) After-ripening and germination of seeds of Tilia, Sambuchus, and Rubus. Botanical Gazette 67, 281–308.
After-ripening and germination of seeds of Tilia, Sambuchus, and Rubus.Crossref | GoogleScholarGoogle Scholar |

Sperber K, Steinbrecher T, Graeber K, et al. (2017) Fruit fracture biomechanics and the release of Lepidium didymum pericarp-imposed mechanical dormancy by fungi. Nature Communications 8, 1868
Fruit fracture biomechanics and the release of Lepidium didymum pericarp-imposed mechanical dormancy by fungi.Crossref | GoogleScholarGoogle Scholar |

Strik BC, Mann J, Finn CE (1996) Percent druplet set varies between blackberry genotypes. Journal of the American Society for Horticultural Science 121, 371–373.
Percent druplet set varies between blackberry genotypes.Crossref | GoogleScholarGoogle Scholar |

Thorp JR, Lynch R (2000) ‘The determination of Weeds of National Significance.’ (National Weeds Strategy Executive Committee: Launceston, Tas., Australia)

Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives in Plant Ecology, Evolution and Systematics 1, 151–190.
Effect of seed passage through vertebrate frugivores’ guts on germination: a review.Crossref | GoogleScholarGoogle Scholar |

van Staden J, Campbell PL (1984) A complex dormancy mechanism in seeds of the weed Rubus cuneifolius. South African Journal of Plant and Soil 1, 48–50.
A complex dormancy mechanism in seeds of the weed Rubus cuneifolius.Crossref | GoogleScholarGoogle Scholar |

Wada S, Reed BM (2010) Seed coat morphology differentiates blackberry cultivars. Journal of the American Pomological Society 64, 152–161.

Wada S, Reed BM (2011a) Optimized scarification protocols improve germination of diverse Rubus germplasm. Scientia Horticulturae 130, 660–664.
Optimized scarification protocols improve germination of diverse Rubus germplasm.Crossref | GoogleScholarGoogle Scholar |

Wada S, Reed BM (2011b) Standardizing germination protocols for diverse raspberry and blackberry species. Scientia Horticulturae 132, 42–49.
Standardizing germination protocols for diverse raspberry and blackberry species.Crossref | GoogleScholarGoogle Scholar |

Wada S, Kennedy JA, Reed BM (2011) Seed-coat anatomy and proanthocyanidins contribute to the dormancy of Rubus seed. Scientia Horticulturae 130, 762–768.
Seed-coat anatomy and proanthocyanidins contribute to the dormancy of Rubus seed.Crossref | GoogleScholarGoogle Scholar |

White HA, Scott JK, Didham RK (2021) Evidence of range shifts in riparian plant assemblages in response to multidecadal streamflow declines. Frontiers in Ecology and Evolution 9, 605951
Evidence of range shifts in riparian plant assemblages in response to multidecadal streamflow declines.Crossref | GoogleScholarGoogle Scholar |

Wilson JR, Panetta FD, Lindgren C (2017) ‘Detecting and responding to alien plant incursions.’ (Cambridge University Press: Cambridge, UK)

Yeoh PB, Fontanini L, Carley JA, Russell AT, Dawson KE, Scott JK, Delaisse CYM, Webber BL (2016) Landscape transformations following blackberry decline in the south-west of Western Australia: successful restoration or back to blackberry? In ‘Proceedings of the 20th Australasian Weeds Conference’, 11–15 September 2016, Perth, WA, Australia. (Eds R Randall, S Lloyd, C Borger) pp. 146–151. (WA Weeds Society)