An integrative morphological and molecular approach to identification of three Australian cucurbitaceous invasive weeds: Citrullus colocynthis, C. lanatus and Cucumis myriocarpusRazia S. Shaik A E , Brendan J. Lepschi D , David Gopurenko B E , Nigel A. R. Urwin C , Geoffrey E. Burrows A E and Leslie A. Weston E
A School of Agricultural and Wine Sciences, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia.
B New South Wales Department of Primary Industries, Wagga Wagga Agricultural Institute, PMB, Wagga Wagga, NSW 2650, Australia.
C Faculty of Science, Charles Sturt University, Port Macquarie, NSW 2444, Australia.
D Australian National Herbarium, Centre for Australian National Biodiversity Research, GPO Box 1600, Canberra ACT 2601, Australia.
E Corresponding author. Present address: Graham Centre for Agricultural Innovation, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia. Email: email@example.com
Australian Systematic Botany 29(5) 247-264 https://doi.org/10.1071/SB16027
Submitted: 21 June 2016 Accepted: 16 September 2016 Published: 22 December 2016
Camel melon (Citrullus lanatus), colocynth (Citrullus colocynthis) and prickly paddy melon (Cucumis myriocarpus) are summer-growing invasive weeds distributed throughout Australia. We used DNA-sequence information from samples collected across Australia and morphological data from glasshouse-grown plants to determine diagnostic features of these species, and to determine the infraspecific identity of Australian Citrullus lanatus and Cucumis myriocarpus. All species possessed distinct genotypes and haplotypes at nuclear G3pdh and chloroplast ycf6–psbM gene regions and could be easily identified on the basis of molecular phylogenetic analysis. A combination of vegetative, floral, fruit and seed characters also allowed for species identification at all developmental stages. On the basis of our morphological and molecular analyses, Australian camel melon and prickly paddy melon populations were identified as Citrullus lanatus var. citroides and Cucumis myriocarpus subsp. myriocarpus respectively.
Additional keywords: G3pdh, infraspecific taxonomic identification, integrative taxonomy, key morphological characteristics, phylogenetic analysis, species identification, ycf6–psbM.
ReferencesAbd El-Ghani M, Abo El-Kheir M, Abdel-Dayem M, Abd El-Hamid M (2011) Vegetation analysis and soil characteristics of five common desert climbing plants in Egypt. Turkish Journal of Botany 35, 561–580.
Bailey FM (1900) ‘The Queensland Flora, Part 2.’ (Diddams HJ and Co.: Brisbane, Qld, Australia)
Baldwin BG, Goldman DH, Keil DJ, Patterson R, Rosatti TJ (2012) ‘The Digital Jepson Manual: Vascular Plants of California.’ (University of California Press: Berkeley, CA, USA)
Barker HM (1964) ‘Camels and the Outback.’ (Sir Isaac Pitman & Sons: Melbourne, Vic., Australia)
Barrett CF, Freudenstein JV (2011) An integrative approach to delimiting species in a rare but widespread mycoheterotrophic orchid. Molecular Ecology 20, 2771–2786.
| An integrative approach to delimiting species in a rare but widespread mycoheterotrophic orchid.CrossRef |
Bentham G (1867‘Flora Australiensis’, vol. 3. (Lovell Reeve and Co.: London))
Bryson CT, DeFelice MS (2009) ‘Weeds of the South.’ (University of Georgia Press: Athens, GA, USA)
Burrows GE, Shaik RS (2014) Comparative developmental anatomy of the taproot of the cucurbitaceous vines Citrullus colocynthis (perennial), Citrullus lanatus (annual) and Cucumis myriocarpus (annual). Australian Journal of Botany 62, 537–545.
| Comparative developmental anatomy of the taproot of the cucurbitaceous vines Citrullus colocynthis (perennial), Citrullus lanatus (annual) and Cucumis myriocarpus (annual).CrossRef |
Chomicki G, Renner SS (2015) Watermelon origin solved with molecular phylogenetics including Linnaean material: another example of museomics. New Phytologist 205, 526–532.
| Watermelon origin solved with molecular phylogenetics including Linnaean material: another example of museomics.CrossRef |
Dane F, Liu J (2007) Diversity and origin of cultivated and citron type watermelon (Citrullus lanatus). Genetic Resources and Crop Evolution 54, 1255–1265.
| Diversity and origin of cultivated and citron type watermelon (Citrullus lanatus).CrossRef | 1:CAS:528:DC%2BD2sXhtVKks7bL&md5=a2383de1d74b076ac005ce91d2cfa7edCAS |
Dane F, Liu J, Zhang C (2007) Phylogeography of the bitter apple, Citrullus colocynthis. Genetic Resources and Crop Evolution 54, 327–336.
| Phylogeography of the bitter apple, Citrullus colocynthis.CrossRef |
Dayrat B (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
| Towards integrative taxonomy.CrossRef |
Deakin JR, Bohn GW, Whitaker TW (1971) Interspecific hybridization in Cucumis. Economic Botany 25, 195–211.
| Interspecific hybridization in Cucumis.CrossRef |
DiTomaso JM, Healy EA (2007) Weeds of California and other western states. Publication 3488. University of California, Division of Agriculture and Natural Resources, Oakland, CA, USA.
Eichler H (1965) ‘Supplement to J. M. Black’s Flora of South Australia (second edition, 1943–1957).’ (Government Printer: Adelaide, SA, Australia)
Fursa TB (1972) K sistematike roda Citrullus Schrad. [On the taxonomy of genus Citrullus Schrad.] Botanicheskii Zhurnal 57, 31–41.
Fursa TB (1981) Intraspecific classification of water-melon under cultivation. Die Kulturpflanze 29, 297–300.
| Intraspecific classification of water-melon under cultivation.CrossRef |
GBIF (2011a) Species: Citrullus colocynthis (L.) Schrader. (Global Biodiversity Information Facility) Available at http://gbif.org/species/2874622/ [Verified 18 October 2016]
GBIF (2011b) Species: Citrullus lanatus (Thunb.) Matsum. & Nakai. (Global Biodiversity Information Facility) Available at http://gbif.org/species/2874621/ [Verified 18 October 2016]
GBIF (2011c) Species: Cucumis myriocarpus E.Mey. ex Naudin. (Global Biodiversity Information Facility) Available at http://gbif.org/species/2874575/ [Verified 18 October 2016]
Gopurenko D, Bellis G, Yanase T, Wardhana A, Thepparat A, Wang J, Cai D, Mitchell A (2015) Integrative taxonomy to investigate species boundaries within Culicoides (Diptera: Ceratopogonidae): a case study using subgenus Avaritia from Australasia and eastern Asia. Veterinaria Italiana 51, 345–378.
Grubben GJH, Denton OA (Eds) (2004) ‘Plant Resources of Tropical Africa 2: Vegetables.’ (PROTA Foundation: Wageningen, Netherlands)
Harden GJ (1990) ‘Flora of New South Wales.’ (New South Wales University Press: Sydney, NSW, Australia)
Harden GJ (2000) Cucurbitaceae. ‘Flora of New South Wales 1’, rev. edn. (Ed. GJ Harden) pp. 228–229. (New South University Press: Sydney, NSW, Australia)
Hollingsworth PM, Forrest LL, Spouge JL, Hajibabaei M, Ratnasingham S, van der Bank M, Chase MW, Cowan RS, Erickson DL, Fazekas AJ, Graham SW, James KE, Kim K-J, Kress WJ, Schneider H, van AlphenStahl J, Barrett SCH, van den Berg C, Bogarin D, Burgess KS, Cameron KM, Carine M, Chacón J, Clark A, Clarkson JJ, Conrad F, Devey DS, Ford CS, Hedderson TAJ, Hollingsworth ML, Husband BC, Kelly LJ, Kesanakurti PR, Sung Kim J, Kim Y-D, Lahaye R, Lee H-L, Long DG, Madriñán S, Maurin O, Meusnier I, Newmaster SG, Park C-W, Percy DM, Petersen G, Richardson JE, Salazar GA, Savolainen V, Seberg O, Wilkinson MJ, Yi D-K, Little DP (2009) A DNA barcode for land plants. Proceedings of the National Academy of Sciences 106, 12794–12797.
| A DNA barcode for land plants.CrossRef | 1:CAS:528:DC%2BD1MXhtVKlt77J&md5=83415b1865ab852fe2d3f44bc521e254CAS |
Jacobs SW, Pickard J (1981) ‘Plants of New South Wales: a census of the cycads, conifers and angiosperms.’ (National Herbarium of New South Wales: Sydney, NSW, Australia)
Jeffrey C (2001) ‘Cucurbitaceae (Citrullus).’ (Ed. P Hanelt) (Springer: New York)
Johnson SB, Hazlewood S (2002) Weed species lists. In ‘WEEDpak, a guide for integrated management of weeds in cotton’. (Eds SB Johnson, GW Charles, GN Roberts, IN Taylor) pp. J3.1–8. (Australian Cotton CRC: Narrabri, NSW, Australia)
Kay SH, Hoyle ST (2001) Mail order, the internet, and invasive aquatic weeds. Journal of Aquatic Plant Management 39, 88–91.
Kholia BS, Fraser-Jenkins CR (2011) Misidentification makes scientific publications worthless: save our taxonomy and taxonomists. Current Science 100, 458–461.
Kilian R, Hanelt P (2001) Cucurbitaceae. In ‘Mansfeld’s Encyclopedia of Agricultural and Horticultural Crops (except ornamentals)’. pp. 1533–1536. (Springer Science and Business Media: Berlin, Germany)
Kirkbride JH (1993) ‘Biosystematic Monograph of the Genus Cucumis (Cucurbitaceae): Botanical Identification of Cucumbers and Melons.’ (Parkway Publishers, Inc.: Boone, NC, USA)
Kristkova E, Lebeda A, Vinter V, Blahousek O (2003) Genetic resources of the genus Cucumis and their morphological description (English–Czech version). Horticultural Science-UZPI 30, 14–42.
Llewellyn R, Ronning D, Clarke M, Mayfield A, Walker S, Ouzman J (2016) Impact of weeds in Australian grain production. Grains Research and Development Corporation, Canberra, ACT, Australia.
McNeill J (1982) Problems of weed taxonomy. In ‘Biology and Ecology of Weeds’. (Eds W Holzner, M Numata) Vol. 2. pp. 35–45. (Springer: Dordrecht, Netherlands)
Michael PJ, Borger CP, MacLeod WJ, Payne PL (2010) Occurrence of summer fallow weeds within the grain belt region of southwestern Australia. Weed Technology 24, 562–568.
| Occurrence of summer fallow weeds within the grain belt region of southwestern Australia.CrossRef |
Moody ML, Les D, DiTomaso J (2008) The role of plant systematics in invasive aquatic plant management. Journal of Aquatic Plant Management 46, 7–15.
Parsons WT, Cuthbertson EG (2001) ‘Noxious Weeds of Australia.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Post AR, Ali R, Krings A, Xiang J, Sosinski BR, Neal JC (2011) On the identity of the weedy bittercresses (Cardamine: Brassicaceae) in United States nurseries: evidence from molecules and morphology. Weed Science 59, 123–135.
| On the identity of the weedy bittercresses (Cardamine: Brassicaceae) in United States nurseries: evidence from molecules and morphology.CrossRef | 1:CAS:528:DC%2BC3MXhsF2qtL8%3D&md5=9baac9f863b7b397267eb937a092b92eCAS |
Pyšek P, Hulme PE, Meyerson LA, Smith GF, Boatwright JS, Crouch NR, Figueiredo E, Foxcroft LC, Jarošík V, Richardson DM, Suda J, Wilson JRU (2013) Hitting the right target: taxonomic challenges for, and of, plant invasions. AoB Plants 5, plt042
| Hitting the right target: taxonomic challenges for, and of, plant invasions.CrossRef |
Renner SS, Chomicki G, Greuter W (2014) (2313) Proposal to conserve the name Momordica lanata (Citrullus lanatus) (watermelon, Cucurbitaceae), with a conserved type, against Citrullus battich. Taxon 63, 941–942.
| (2313) Proposal to conserve the name Momordica lanata (Citrullus lanatus) (watermelon, Cucurbitaceae), with a conserved type, against Citrullus battich.CrossRef |
Royal Horticultural Society (2007) ‘RHS Colour Chart’, 5th edn. (The Royal Horticultural Society: London, UK)
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
Schaefer H, Carine MA, Rumsey FJ (2011) From European priority species to invasive weed: Marsilea azorica (Marsileaceae) is a misidentified alien. Systematic Botany 36, 845–853.
| From European priority species to invasive weed: Marsilea azorica (Marsileaceae) is a misidentified alien.CrossRef |
Shaik RS, Weston LA, Burrows GE, Gopurenko D (2011) A comparative phenological and genetic diversity analysis of two invasive weeds, camel melon (Citrullus lanatus (Thunb.) Matsum. and Nakai var. lanatus) and prickly paddy melon (Cucumis myriocarpus L.), in inland Australia. In ‘Proceedings of the 23rd Asia–Pacific Weed Science Society Conference’, 26–29 September 2011, Cairns, Qld, Australia. (Ed. S Adkins) pp. 510–518. (Asian Pacific Weed Science Society)
Shaik RS, Gopurenko D, Burrows GE, Urwin NAR, Lepschi BJ, Hildebrand SM, Weston LAV (2012) Identification of the invasive weeds, camel melon, prickly paddy melon and colocynth in Australia: a morphological and molecular approach. In ‘Eighteenth Australasian Weeds Conference’, 8–11 October, 2012, Melbourne, Vic., Australia. (Ed. V Eldershaw) pp. 73–77. (Weed Science Society of Victoria Inc.: Melbourne, Vic., Australia) Available at http://www.caws.org.au/awc/2012/awc201210731.pdf [Verified 17 October 2016]
Shaik RS, Gopurenko D, Urwin NAR, Burrows GE, Lepschi BJ, Weston LA (2015) Population genetics of invasive Citrullus lanatus, Citrullus colocynthis and Cucumis myriocarpus (Cucurbitaceae) in Australia: inferences based on chloroplast and nuclear gene sequencing. Biological Invasions 17, 2475–2490.
| Population genetics of invasive Citrullus lanatus, Citrullus colocynthis and Cucumis myriocarpus (Cucurbitaceae) in Australia: inferences based on chloroplast and nuclear gene sequencing.CrossRef |
Shaik RS, Zhu X, Clements DR, Weston LA (2016) Understanding invasion history and predicting invasive niches using genetic sequencing technology in Australia: case studies from Cucurbitaceae and Boraginaceae. Conservation Physiology 4, cow030
| Understanding invasion history and predicting invasive niches using genetic sequencing technology in Australia: case studies from Cucurbitaceae and Boraginaceae.CrossRef |
Smirnov AV, Nassonova ES, Cavalier-Smith T (2008) Correct identification of species makes the amoebozoan rRNA tree congruent with morphology for the order Leptomyxida Page 1987; with description of Acramoeba dendroida n.g., n.sp., originally misidentified as ‘Gephyramoeba sp.’ European Journal of Protistology 44, 35–44.
| Correct identification of species makes the amoebozoan rRNA tree congruent with morphology for the order Leptomyxida Page 1987; with description of Acramoeba dendroida n.g., n.sp., originally misidentified as ‘Gephyramoeba sp.’CrossRef |
Solmaz I, Sari N (2009) Characterization of watermelon (Citrullus lanatus) accessions collected from Turkey for morphological traits. Genetic Resources and Crop Evolution 56, 173–188.
| Characterization of watermelon (Citrullus lanatus) accessions collected from Turkey for morphological traits.CrossRef |
Steele PR, Friar LM, Gilbert LE, Jansen RK (2010) Molecular systematics of the neotropical genus Psiguria (Cucurbitaceae): implications for phylogeny and species identification. American Journal of Botany 97, 156–173.
| Molecular systematics of the neotropical genus Psiguria (Cucurbitaceae): implications for phylogeny and species identification.CrossRef | 1:CAS:528:DC%2BC3cXhs12qsbg%3D&md5=7c4e2b75090388163155a300a53e80e9CAS |
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.CrossRef | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=f96b9a6ff756fc575d7627d1961f5101CAS |
Telford IRH (1982) Cucurbitaceae. In ‘Flora of Australia’. (Ed. AS George.) Vol. 8, pp. 158–198. (Australian Government Publishing Service: Canberra, ACT, Australia)
Tiébré M-S, Bizoux J-P, Hardy OJ, Bailey JP, Mahy G (2007) Hybridization and morphogenetic variation in the invasive alien Fallopia (Polygonaceae) complex in Belgium. American Journal of Botany 94, 1900–1910.
| Hybridization and morphogenetic variation in the invasive alien Fallopia (Polygonaceae) complex in Belgium.CrossRef |
van der Veen M (2011) Consumption, trade and innovation. In ‘Exploring the Botanical Remains from the Roman and Islamic Ports at Quseir al-Qadim, Egypt’. (Eds P Brewnig, K Neumann) p. 106. (Africa Magna Verlag: Frankfurt, Germany)
White CT, Francis WD (1926) Contributions to the Queensland flora, no. 3. Proceedings of the Royal Society of Queensland 37, 152–167.
Will KW, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology 54, 844–851.
| The perils of DNA barcoding and the need for integrative taxonomy.CrossRef |