Abstract
The plasticity of functional traits promotes invasiveness of a species. Biomass allocation, as one of these traits, is responsible for resource acquisition, and its plastic modifications can be of adaptive value in new environments before any genetic adaptations may occur. Our aim was to compare in situ biomass allocation in aboveground and belowground organs in an Antarctic and a Polish population of annual bluegrass (Poa annua), the only alien plant species successfully invading Antarctica. The Antarctic population was characterised by three times lower aboveground biomass, more compact plant growth habit and higher fraction of biomass allocated into belowground organs than in the Polish population. The differences between populations are probably a result of adaptation to local conditions. The modifications of the studied traits in the Antarctic population are most likely a response to extreme atmospheric and edaphic conditions and enable the species to survive and spread in this hostile environment. Our results are in accordance with the balanced growth hypothesis. At the same time, these trait values enhance species performance under Antarctic conditions making P. annua a potential threat to local plant communities under altering climate changes and growing human impact scenario.
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Introduction
Plastic resource allocation in plants is a response to varying growing conditions affecting dispersal, distribution, resilience, and speciation (Harper and Ogden 1970; Hickman 1975; Reekie and Bazzaz 1987; Dong and de Kroon 1994). Hence, it has a substantial effect on plant’s competitiveness (Berendse and Elberse 1990). Functional traits related to physiology, biomass allocation, growth rate, size, and fitness affect invasiveness (Alpert et al. 2000; van Kleunen et al. 2010; Espeland 2013; Colautti et al. 2017). Invasive species are often physiologically plastic, which allows them to take advantage of a variety of habitats and different ecological niches (Baker 1974; Meekins and McCarthy 2001; Richards et al. 2006). In consequence, a species can be well adapted to the conditions of the colonised area without genetic changes (Alpert et al. 2000; Chwedorzewska and Bednarek 2012). The plastic response enables the survival of a population even before any favourable genetic changes may take place. Therefore, species plasticity has been suggested as one of the key traits important for predicting species invasiveness (Rejmanek and Richardson 1996).
Many authors point to resource allocation as one of the traits important for species invasiveness. This is because plastic biomass allocation enables the control of resource absorption from the environment. Greater root biomass allows for better acquisition of nutrients and water from soil, and greater photosynthetically active biomass enables a more efficient collection of solar energy (Sultan 1995, 2000; Ryser and Eek 2000). Plastic biomass allocation is therefore an important parameter during species invasion, because it directly affects adaptation to the conditions prevailing in the new environment. This results in a broadening of the tolerance to environmental conditions, whereby species can survive in different ecological niches (Sexton et al. 2002; Richards et al. 2006; Geng et al. 2016).
Theoretically if the source and invaded habitats share similar environmental conditions, there is no need for plastic response of a species conquering new sites. Phenotypic plasticity of the invasive species is most evident and often necessary when conditions differ between the source and target habitats. In such a case, plasticity can be the main factor that determines establishing of the species in a new environment and further invasion success (Hulme 2007; Espeland 2013; Colautti et al. 2017). In particular, harsh conditions, differing from the majority of potential source habitats and being on the border of endurance for most vascular plant species, are met in Maritime Antarctica (e.g. Robinson et al. 2003; Galera et al. 2015).
The only invasive plant species successfully conquering the harsh Maritime Antarctic environment and establishing a self-sustaining population in the region is annual bluegrass (Poa annua L.), one of the most common grass species in the world. The species is of Eurasian origin with the centre of its range in temperate climates (Grime et al. 1988; Mitich 1998; Vargas and Turgeon 2003). It grows in a variety of climatic zones from the equator to the polar regions (Vargas and Turgeon 2003). The species has been noted for over 30 years in Point Thomas Oasis on King George Island, Maritime Antarctica (Galera et al. 2017). Due to harsh environmental factors, this Antarctic population exhibits specific morphological traits (Galera et al. 2015).
The aim of our work was to compare biomass allocation in aboveground and belowground organs of annual bluegrass in two populations of the species occurring under different environmental conditions in Maritime Antarctica and Poland. We were interested in finding out how these traits may vary to exploit the local environment and to what extent the biomass allocation of the studied species is shaped by different climatic and/or edaphic factors. This is an initial study of biomass allocation of the species in situ. This research reports differences in the studied populations under local conditions and precedes a common garden study in which climatic factors and soil properties will be controlled.
Methods
Data collection
For our study, we chose two locations where P. annua populations are found. One of the sampling sites was situated in the vicinity of the Polish Antarctic Station H. Arctowski (62°09′36″S, 58°28′16″W), King George Island, South Shetlands, Maritime Antarctica. The other sampling site was situated in the Botanic Garden of the Polish Academy of Sciences (52°06′19″N, 21°05′43″E), Warsaw, Poland—representing one of the core native range populations (Tutin 1952). The two locations differ in climatic characteristics (Table 1). The King George Island site has polar climate (Galera et al. 2015, 2018) with sub-zero temperatures even during the short Antarctic “summer” (annually 143 days with mean daily temperature above 0 °C, Kejna 1992). There is no growing season defined as a period with mean daily temperature above 5 °C (Table 1). The site is characterised by strong desiccating wind (Wierzbicki 2009), soil of initial type (Bölter et al. 1997; Nędzarek 2008; Łachacz et al. 2018), low competition, and no herbivory (Galera et al. 2018). Contrastingly the Warsaw site receives a temperate climate with sufficient rainfall and optimal temperature during the growing season (Galera et al. 2015) that lasts over 200 days a year (Table 1). In this site, the dry podzolic soil (Puchalski and Gawryś 2002) is relatively more fertile than in our Antarctic study site, but there is pressure from competitors as well as herbivores.
In each site, we sampled 60 randomly selected P. annua tussocks. The sampling was performed at the end of P. annua growth cycle in February/March 2015 in the Antarctic site and in October 2015 in the Warsaw site. We measured the height of each tussock (0.5 cm accuracy) and carefully dug them without disturb the roots. Our goal was to assess the differences in biomass of aboveground and belowground organs of annual bluegrass in both studied populations. During our study, we observed that tussocks from the Antarctic population were not large enough to measure the dry weight of their organs and failed to be detected by our scale. We therefore had to employ a procedure to extrapolate their mass from photographs of individuals (Fig. 1).
Tussocks were transported to the laboratory, washed to dispose of any remaining soil, separated into individuals in order to minimise the overlapping of leaves and photographed (Fig. 1). The images were used to calculate the area of the above- and belowground parts of the plant (0.01 cm2 accuracy) as a proxy of biomass, as well as to measure the maximum length of the root within the tussock (0.01 cm accuracy). The measurements were taken with ImageJ software (Rasband 1997–2018). All annual bluegrass individuals were subsequently fractioned into aboveground organs and roots and dried at 40 °C for 24 h. We weighed the aboveground and belowground organs of each tussock on a laboratory scale (0.0001 g accuracy). For the Arctowski population, we were able to collect biomass information for only 27 tussocks as the remaining 33 tussocks were too small to be detected by the scale.
Statistical analysis
Our dataset included a direct biomass measure of the aboveground and belowground organs, as well as an indirect biomass estimate based on photographs. We compared the assessment of biomass using these two methods by correlation analysis. We estimated Pearson correlation coefficients and least-squares linear regression coefficients between the biomass and organ area on the photographs. We compared the regression slopes between direct measurement of biomass and its estimate from photographs separately for aboveground and belowground organs between populations with pairwise comparisons of least-squares means using the Tukey method (Piepho 2004). As the regression coefficients differed between populations, we used them in subsequent analyses to estimate the biomass of organs based on the photographs according to the formula: B = A × R (B–biomass of plant organs, A—area of plant organs on photographs, R—regression coefficient). Based on our method comparison results, further analyses of biomass were performed not on the direct measurements of biomass, but on their regression-based estimate.
We compared the studied populations in regard to the number of individuals per tussock, tussock height, the length of the longest root in a tussock and aboveground, belowground and total tussock biomass. Furthermore, we calculated shoot-to-root length ratio per tussock and percentage of the belowground biomass in total biomass. The Shapiro–Wilk test showed that the distribution of the measured parameters deviated from the normal distribution; therefore, the Kruskal–Wallis test was used to compare data from analysed populations. All statistical analyses were carried out in the R program with the use of base (R Core Team 2018), lsmeans (Lenth 2016) and multcompView (Graves et al. 2015) packages.
Results
We recorded 233 individuals in 60 tussocks from Poland and 209 individuals in the same number of tussocks from Antarctica. The median tussock height was three times greater in the Polish population than in the Antarctic, but plant roots were shorter (Table 2). In both populations, shoot-to-root length ratio was lower than 1, indicating that roots were longer than shoots, but there were large differences between the populations (Table 2).
We found a strong linear correlation between the biomass and the area of the plant organs on photographs for tussock from both studied populations (Figs. 2, 3). Comparison of the regression slopes between biomass and plant organ area on photographs indicated two groups (Fig. 4). We did not find significant differences between linear regression slopes for biomass and area of photographed organs within each population, but the slopes differed between populations. The average regression coefficients were 0.0117 for the Antarctic and 0.0079 for the Polish population.
The total biomass of tussocks from Poland was about 2 times higher than from the Antarctic (Table 2). Aboveground tussock biomass was significantly higher in the Polish than in the Antarctic population. The only studied trait that is not significantly different between studied populations was root biomass (Table 2). Biomass allocation expressed as the percent of the belowground biomass in the biomass of the entire tussock also differed between populations with 26.6% for the Polish population and 60.1% for the Antarctic one (Table 2).
Discussion
Estimating biomass based on the photograph area of plant organs
Due to small size of the plants studied, especially from the Antarctic population we had to develop another means of assessing plant biomass. Therefore, we used linear regression to estimate the biomass of organs from photographs. The regression method is indirect, but gave satisfactory results. The interlacing of roots and leaves induces an error in the estimate, but the error is similar over all measured objects. Our results indicated strong correlation between photographed area and biomass, which may suggest that measuring the photographed area of plant organs is a good proxy of biomass for comparison purposes. This technique may be helpful in biomass allocation estimation, as it requires less time or resources to perform and can help measure specimens otherwise not eligible for examination.
Similar methods are used widely for difficult measurements, like large-area estimations of forest biomass (Brown et al. 1989), commonly using existing regression equations for this purpose. Generalised equations may cause significant errors and every usage of regression estimates should be thoroughly checked before being applied (Wang et al. 2002). We found significant differences in population-specific regression equations confirming their cross-inapplicability. Also extrapolating the regression line beyond the range of both measured variables can be questioned, but in our opinion it is a better estimate than not having any results at all, especially from unique sites, like Antarctica.
Factors shaping studied tussock traits
Environmental conditions considerably differ between South Shetlands and Poland (Table 1). This demands plastic changes from the invading plant species. Apart from such factors as temperature and soil properties, which may be studied under controlled environment, biomass allocation may be influenced by an interlacing complex of other factors, which are hard to simulate. One of them is water availability restricting plant growth in the Antarctic. Despite a large supply of water on King George Island in the form of glacial caps, it is periodically inaccessible to plants inducing physiological drought due to low temperature and salinity (Mahajan and Tuteja 2005). Very strong wind often exceeding 40 m/s is another important factor affecting plant growth in Maritime Antarctica (Kowalski 1985; Wierzbicki 2009). Wind acts both as a stressor, causing plant desiccation, and as disturbance factor (Berjak 1979; Gardiner et al. 2016). Differences in these environmental factors may induce multiple responses in plants, which determine the ultimate trait values, depending on their magnitude and potentially interactive effects (Bradshaw 1965).
Response of local populations to contrasting environmental conditions
Our results unequivocally indicate differences in tussock traits and biomass allocation in populations from the two study sites. In the Antarctic population, P. annua had lower aboveground biomass than in the Polish population. We did not detect differences in belowground biomass, but plants from the Antarctic had longer roots. Differences in biomass allocation detected by us between the study sites are in accordance with the balanced growth hypothesis (Shipley and Meziane 2002), which states that plant organs responsible for acquisition of the limiting resource should develop better than others. Under harsh conditions, pioneer plants exhibit a similar scheme of biomass allocation which is driven by abiotic factors (Jumpponen et al. 1999). Lower total biomass is often detected in plants growing in sites prone to drought (Enquist and Niklas 2002). In polar regions, members of the Poaceae (grass family) exhibit a xerophytic character, including a lower biomass of the aboveground organs, longer root system and higher root biomass (Giełwanowska et al. 2011).
Low aboveground biomass of plants in the polar regions was found to be driven by low temperature and strong wind (Giełwanowska et al. 2011). Lower biomass of the aboveground organs and lower tussock height detected by us in the Antarctic in comparison with the Polish population may be a result of the differences in temperature and wind conditions between the studied sites. Under suboptimal low temperature, plant growth may be much slower than under optimal climatic conditions. The temperature on the soil surface can be even 10 °C higher than temperature recorded by meteorological stations (Kellman-Sopyła and Giełwanowska 2015). In the Antarctic, a compact plant growth habit may allow aboveground organs to be confined to more favourable conditions present just above the soil surface as well as reduce transpiration caused by desiccating wind. Deschampsia antarctica Desv. (Antarctic hair grass) was shown to have a different growth habit depending on the wind speed, with more erect plants under lower wind speed and more procumbent plants under high wind (Parnikoza et al. 2015). In contrast, plants from a temperate climate may be taller to win competition for light (McCarthy and Enquist 2007).
Species more resistant to drought and harsh climatic conditions were found to have higher biomass allocation in roots (Fort et al. 2012). In comparison with plants cultivated under optimal conditions, the root system of plants experiencing harsh conditions was even twice as large (Gleeson and Tillman 1990). The impact of low nitrogen and phosphorus availability in soil was experimentally shown to impact biomass allocation in many species (Aerts et al. 1991; Müller et al. 2000). The study of nutrient deficiency on the development of Arabidopsis thaliana (L.) Hynh. (thale cress) indicated that increased root growth is a consequence of nitrogen and phosphorus deficiency, while other nutrient deficiency does not enhance root growth (Hermans et al. 2006). Although we did not find differences in root biomass between the Antarctic and Polish population, the roots in the Antarctic plants were significantly longer. The larger rhizosphere in the Antarctic population may aid in nutrient and water acquisition. A similar root biomass allocation pattern was found for annual bluegrass occurring in a sub-Antarctic site (Williams et al. 2018). Longer root system may also better anchor the plants against strong wind (Reubens et al. 2009; Gardiner et al. 2016).
The role of phenotypic plasticity in the invasion of P. annua
Our results confirm that P. annua is a highly plastic species. The differences in biomass allocation observed in this study between two populations of the same species, but from climatic zones highly differing in environment severity (Table 1), show the species high adjustment capability. Also, our previous findings regarding differences in morphological traits between individuals confirm the highly adaptive nature of this species. Modifications of morphological traits make the tussocks (this study) as well as individual specimens (Galera et al. 2015) more compact under harsh conditions, and differences in biomass allocation help with the acquisition of scarce resources. While individuals in the Antarctic population tended to be composed of more shoots (Galera et al. 2015), they still have lower aboveground biomass than individuals from the Polish population. Also their sexual organs are smaller, more compact enabling lower seed set under Antarctic conditions, despite the higher number of panicles per individual (Galera et al. 2015). This may indicate high influence of harsh conditions on plant performance. Nevertheless, these traits can be modified in such a way that although fecundity is lowered in comparison with optimal growing conditions, the species is able to adapt and set viable seeds in the Antarctic. Together these traits facilitate the ongoing invasion of the species in this hostile environment.
Annual bluegrass has also been reported to show plastic physiological response to different environmental conditions (Giełwanowska et al. 2011). High plasticity in all of these traits, rather than genetic diversity, makes the species highly invasive. This adaptability allows alien species to “set foot” in novel environments before any genetic adaptations may have time to take place (Frenot et al. 2005; Richards et al. 2006). The species has been reported as invasive in sub-Antarctic islands (e.g. Scott and Kirkpatrick 2005; Whinam 2009; Williams et al. 2016; Greve et al. 2017). The species successfully penetrated the Antarctic geographical barrier (Chwedorzewska et al. 2015; Hughes and Pertierra 2016) and established a breeding population on King George Island (Galera et al. 2017). This confirms the pivotal role of high phenotypic plasticity of this species in the invasion success in the broad Antarctic region.
Phenotypic plasticity has been observed to determine the ability of species to succeed in a broad range of habitats (Pigliucci 2001; Leger and Rice 2003; Richards et al. 2006). Modifications of developmental, physiological and life-history traits observed in natural populations exposed to novel environments can be driven by plastic response (Chevin et al. 2013). We found such response in our study species. Besides promoting species persistence, adaptive plasticity can facilitate the rapid spread of invasive species across diverse new habitats (breaking the survival barrier, Blackburn et al. 2011). The start of expansion of P. annua in Point Thomas Oasis (Wódkiewicz et al. 2018) may be an effect of this facilitation. The invasion of P. annua at Point Thomas Oasis, possible due to the species plasticity, is a most pronounced invasion in the region. It enabled us to study the invasion process in harsh environments and species traits facilitating this invasion. Nevertheless, we started the eradication process to protect this unique ecosystem (Galera et al. 2017). The plasticity of P. annua may pose a risk of local tundra communities under a changing climate scenario. Hopefully this invasion can be stopped with the use of proper eradication methods.
Conclusions
Biomass allocation is an important adaptive trait, and its variation can be a response to variable environmental factors like wind speed, availability of nutrients and water conditions. The Antarctic population of P. annua in comparison with the Polish one shows significant differences in biomass allocation. The plasticity of this trait as well as other morphological, developmental and physiological traits may greatly facilitate the species invasibility in polar regions. Higher biomass allocation in the belowground organs in the Antarctic population may allow plants to better exploit nutrients and water resources, as well as more efficiently anchor the plant to the ground. Smaller and compact aboveground organs restrict transpiration and reduce surface resistance, making plants less vulnerable to the adverse influence of wind abrasion. Plants are therefore better adapted to survive and set seed under local Antarctic conditions. To what extent these differences are population specific or remain flexible to changing environmental conditions will be a focus of our further studies involving transplant experiments under simulated environmental conditions.
References
Aerts R, Boot RGA, van der Aart PJM (1991) The relation between above- and belowground biomass allocation patterns and competitive ability. Oecologia 87:551–559. https://doi.org/10.1007/BF00320419
Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect Plant Ecol Evol Syst 3:52–66. https://doi.org/10.1078/1433-8319-00004
Baker HG (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24. https://doi.org/10.1146/annurev.es.05.110174.000245
Berendse F, Elberse WT (1990) Competition and nutrient availability in heathland and grass ecosystems. In: Grace JB, Tilman D (eds) Perspectives on plant ecology. Academic Press, San Diego, New York, Berkeley, Boston, London, Sydney, Tokyo, Toronto, pp 93–116
Berjak P (1979) The Marion Island Flora—leaf structure in Poa cookii (Hook f.). 9:67-68. Proc Electron Microsc Soc S Afr 9:67–68
Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. https://doi.org/10.1016/j.tree.2011.03.023
Bölter H, Blume H-P, Schneider D, Beyer L (1997) Soil properties and distributions of invertebrates and bacteria from King George Island (Arctowski Station), maritime Antarctic. Polar Biol 18:295–304. https://doi.org/10.1007/s003000050191
Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155. https://doi.org/10.1016/S0065-2660(08)60048-6
Brown S, Gillespie AJR, Lugo AE (1989) Biomass estimation methods for tropical forests with applications to forest inventory data. For Sci 34:881–902
Chevin L-M, Collins S, Lefevre F (2013) Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Funct Ecol 27:967–979. https://doi.org/10.1111/j.1365-2435.2012.02043.x
Chwedorzewska KJ, Bednarek PT (2012) Genetic and epigenetic variation in a cosmopolitan grass Poa annua from Antarctic and Polish populations. Pol Polar Res 33:63–80. https://doi.org/10.2478/v10183-012-0004-5
Chwedorzewska KJ, Giełwanowska I, Olech M, Molina-Montenegro MA, Wódkiewcz M, Galera H (2015) Poa annua L. in the maritime Antarctic: an overview. Polar Rec 51:637–643. https://doi.org/10.1017/S0032247414000916
Colautti RI, Alexander JM, Dlugosch KM, Keller SR, Sultan SE (2017) Invasions and extinctions through the looking glass of evolutionary ecology. Philos Trans R Soc B 372:20160031. https://doi.org/10.1098/rstb.2016.0031
Czernecki B, Miętus M (2017) The thermal seasons variability in Poland, 1951–2010. Theor Appl Climatol 127:481–493. https://doi.org/10.1007/s00704-015-1647-z
Dong M, de Kroon H (1994) Plasticity in morphology and biomass allocation in Cynodon dactylon, a grass species forming stolons and rhizomes. Oikos 70:99–106. https://doi.org/10.2307/3545704
Enquist BJ, Niklas KJ (2002) Global allocation rules for patterns of biomass partitioning in seed plants. Science 295:1517–1520. https://doi.org/10.1126/science.1066360
Espeland EK (2013) Predicting the dynamics of local adaptation in invasive species. J Arid Land 5:268–274. https://doi.org/10.1007/s40333-013-0163-1
Fort F, Jouany C, Cruz P (2012) Root and leaf functional trait relations in Poaceae species: implications of differing resource-acquisition strategies. J Plant Ecol 6:211–219. https://doi.org/10.1093/jpe/rts034
Frenot Y, Chown SI, Whinam J, Selkirk PM, Convey P, Skotnicki M, Bergstrom DM (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biol Rev 80:45–72. https://doi.org/10.1017/S1464793104006542
Frich P, Alexander LV, Della-Marta P, Gleason B, Haylock M, Klein Tank AMG, Peterson T (2002) Observed coherent changes in climatic extremes during the second half of the twentieth century. Clim Res 19:193–212. https://doi.org/10.3354/cr019193
Galera H, Chwedorzewska KJ, Wódkiewicz M (2015) Response of Poa annua to extreme conditions: comparison of morphological traits between populations from cold and temperate climate conditions. Polar Biol 38:1657–1666. https://doi.org/10.1007/s00300-015-1731-y
Galera H, Wódkiewicz M, Czyż E, Łapiński S, Kowalska ME, Pasik M, Rajner M, Bylina P, Chwedorzewska KJ (2017) First step to eradication of Poa annua L. from Point Thomas Oasis (King George Island, South Shetlands, Antarctica). Polar Biol 40:939–945. https://doi.org/10.1007/s00300-016-2006-y
Galera H, Chwedorzewska KJ, Korczak-Abshire M, Wódkiewicz M (2018) What affects the probability of biological invasions in Antarctica? Using an expanded conceptual framework to anticipate the risk of alien species expansion. Biodivers Conserv 27:1789–1809. https://doi.org/10.1007/s10531-018-1547-5
Gardiner B, Barry P, Moulia B (2016) Review: wind impacts on plant growth, mechanics and damage. Plant Sci 245:94–118. https://doi.org/10.1016/j.plantsci.2016.01.006
Geng Y, van Klinken RD, Sosa A, Li B, Chen J, Xu C-Y (2016) The relative importance of genetic diversity and phenotypic plasticity in determining invasion success of a clonal weed in the USA and China. Front Plant Sci 7:213. https://doi.org/10.3389/fpls.2016.00213
Giełwanowska I, Pastorczyk M, Kellmann-Sopyła W (2011) Influence of environmental changes on physiology and development of polar vascular plants. Pap Glob Change 18:53–62. https://doi.org/10.2478/v10190-010-0004-7
Gleeson SK, Tilman D (1990) Allocation and the transient dynamics of succession on poor soils. Ecol 71:1144–1155. https://doi.org/10.2307/1937382
Graves S, Piepho HP, Selzer L, Dorai-Raj S (2015) multcompView: visualizations of paired comparisons. R package version 0.1-7. https://CRAN.Rproject.org/package=multcompView. Accessed 7 August 2018
Greve M, Mathakutha R, Steyn C, Chown SL (2017) Terrestrial invasions on sub-Antarctic Marion and Prince Edward Islands. Bothalia 47:2143. https://doi.org/10.4102/abc.v47i2.2143
Grime JP, Hodgdon JG, Hunt R (1988) Comparative plant ecology: a functional approach to common British Species. Unwin Hyman, London. https://doi.org/10.1007/978-94-017-1094-7
Harper JL, Ogden J (1970) The reproductive strategy of higher plants: I. The concept of strategy with special reference to Senecio Vulgaris L. J Ecol 58:681–698. https://doi.org/10.2307/2258529
Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617. https://doi.org/10.1016/j.tplants.2006.10.007
Hickman JC (1975) Environmental unpredictability and plastic energy allocation strategies in the annual Polygonum Cascadense (Polygonaceae). J Ecol 63:689–701. https://doi.org/10.2307/2258745
Hughes KA, Pertierra LR (2016) Evaluation of non-native species policy development and implementation within the Antarctic Treaty area. Biol Conserv 200:149–159. https://doi.org/10.1016/j.biocon.2016.03.011
Hulme PE (2007) Phenotypic plasticity and plant invasions: is it all Jack? Funct Ecol 22:3–7. https://doi.org/10.1111/j.1365-2435.2007.01369.x
Jumpponen A, Väre H, Mattson KG, Ohtonen R, Trappe JM (1999) Characterization of “safe sites” for pioneers in primary succession on recently deglaciated terrain. J Ecol 87:98–105. https://doi.org/10.1046/j.1365-2745.1999.00328.x
Kejna M (1992) Próba wydzielenia termicznych pór roku w Stacji H. Arctowskiego (Szetlandy Pd) w latach 1978-1989 [An attempt to asses thermal seasons at H. Arctowski Station (South Shetlands) in the years 1978–1989—in Polish]. Probl Klimatol Polar 34:21–29
Kellman-Sopyła W, Giełwanowska I (2015) Germination capacity of five polar Caryophyllaceae and Poaceae species under different temperature conditions. Polar Biol 38:1753–1765. https://doi.org/10.1007/s00300-015-1740-x
Kowalski D (1985) Wind structure at Arctowski Station. Pol Pol Res 6:391–403
Łachacz A, Kalisz B, Giełwanowska I, Olech M, Chwedorzewska KJ, Kellmann-Sopyła W (2018) Nutrient abundance and variability from Antarctic soils in the coastal of King George Island. J Soil Sci Plant Nutr 18:294–311. https://doi.org/10.4067/S0718-95162018005001101
Leger EA, Rice KJ (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol Lett 6:257–264. https://doi.org/10.1046/j.1461-0248.2003.00423.x
Lenth RV (2016) Least-squares means: the R Package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158. https://doi.org/10.1016/j.abb.2005.10.018
McCarthy MC, Enquist BJ (2007) Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Funct Ecol 21:713–720. https://doi.org/10.1111/j.1365-2435.2007.01276.x
Meekins JF, McCarthy BC (2001) Effect of environmental variation on the invasive success of a nonindigenous forest herb. Ecol Appl 11:1336–1348. https://doi.org/10.1890/1051-0761(2001)011%5b1336:EOEVOT%5d2.0.CO;2
Mitich LW (1998) Annual Bluegrass (Poa annua L.). Weed Technol 12:414–416. https://doi.org/10.1017/S0890037X00044031
Müller I, Schmid B, Weiner J (2000) The effect of nutrient availability on biomass allocation patterns in 27 species of herbaceous plants. Perspect Plant Ecol Evol Syst 3:115–127. https://doi.org/10.1078/1433-8319-00007
Nędzarek A (2008) Sources, diversity and circulation of biogenic compounds in Admiralty Bay, King George Island, Antarctica. Antarct Sci 20:135–145. https://doi.org/10.1017/S0954102007000909
Parnikoza I, Miryuta N, Ozheredova I, Kozeretska I, Smykła J, Kunakh V, Convey P (2015) Comparative analysis of Deschampsia antarctica Desv. population adaptability in the natural environment of the Admiralty Bay region (King George Island, maritime Antarctic). Polar Biol 38:1401–1411. https://doi.org/10.1007/s00300-015-1704-1
Piepho H-P (2004) An algorithm for a letter-based representation of all pairwise comparisons. J Comput Gr Stat 13:456–466. https://doi.org/10.1198/1061860043515
Pigliucci M (2001) Phenotypic plasticity, beyond nature and nurture. The Johns Hopkins University Press, Baltimore, London
Puchalski J, Gawryś W (2002) Ogród Botaniczny—Centrum Zachowania Różnorodności Biologicznej Polskiej Akademii Nauk w Warszawie [Botanic Garden—Center for Biological Diversity Conservation of the Polish Academy of Sciences—in Polish]. In: Łukasiewicz A, Puchalski J (eds) Ogrody botaniczne w Polsce. ARW Arkadiusz Grzegorczyk, Fundacja Homo et Planta, Warszawa, pp 103–122
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 7 August 2018
Rasband WS (1997–2018) ImageJ. U. S. National Institutes of Health, Bethesda. http://imagej.nih.gov/ij/. Accessed 7 August 2018
Reekie EG, Bazzaz FA (1987) Competition and patterns of resource use among seedlings of five tropical trees grown at ambient and elevated CO2. Oecologia 79:212–222. https://doi.org/10.1007/BF00388481
Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661. https://doi.org/10.2307/2265768
Reubens B, Pannemans B, Danjon F, De Proft M, De Baets S, De Baerdemaeker J, Poesen J, Muys B (2009) The effect of mechanical stimulation on root and shoot development of young containerised Quercus robur and Robinia pseudoacacia trees. Trees 23:1213–1228. https://doi.org/10.1007/s00468-009-0360-x
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Robinson SA, Wasley J, Tobin AK (2003) Living on the edge—plants and global change in continental and maritime Antarctica. Glob Change Biol 9:1681–1717. https://doi.org/10.1046/j.1365-2486.2003.00693.x
Ryser P, Eek L (2000) Consequences of phenotypic plasticity vs. interspecific differences in leaf and root traits for acquisition of aboveground and belowground resources. Am J Bot 87:402–411. https://doi.org/10.2307/2656636
Scott JJ, Kirkpatrick JB (2005) Changes in Subantarctic Heard Island Vegetation at Sites Occupied by Poa annua, 1987–2000. Arct Antarct Alp Res 37:366–371. https://doi.org/10.1657/1523-0430(2005)037%5b0366:CISHIV%5d2.0.CO;2
Sexton JP, McKay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climates in north America. Ecol Appl 12:1652–1660. https://doi.org/10.1890/1051-0761(2002)012%5B1652:PAGDMA%5D2.0.CO;2
Shipley B, Meziane D (2002) The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Funct Ecol 16:326–331. https://doi.org/10.1046/j.1365-2435.2002.00626.x
Sultan SE (1995) Phenotypic plasticity and plant adaptation. Acta Bot Neerl 44:363–383. https://doi.org/10.1111/j.1438-8677.1995.tb00793.x
Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542
Tutin TG (1952) Origin of Poa annua L. Nature 169:160
van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. https://doi.org/10.1111/j.1461-0248.2009.01418.x
Vargas JM, Turgeon AJ (2003) Poa annua: physiology, culture, and control of annual bluegrass. John Wiley and Sons, Hoboken
Wang JR, Zhong AL, Kimmins JP (2002) Biomass estimation errors associated with the use of published regression equations of paper birch and trembling aspen. North J Appl For 19:128–136
WeatherOnline (2016). http://www.weatheronline.co.uk/. Accessed 14 March 2016
Whinam J (2009) Aliens in the sub-Antarctic—biosecurity and climate change. Pap Proc R Soc Tasman 143:45–51
Wierzbicki G (2009) Wiatry huraganowe w 2008 roku w Zatoce Admiralicji, Wyspa Króla Jerzego, Antarktyda Zachodnia [Hurricane winds during 2008 year in Admiralty Bay, King George Island, West Antarctica—in Polish with English summary]. Przegląd Naukowy. Inż Kształt Środowiska 18:47–55
Williams LK, Kristiansen P, Sindel BM, Wilson SC, Shaw JD (2016) Quantifying the seed bank of an invasive grass in the sub-Antarctic: seed density, depth, persistence and viability. Biol Invasions 18:2093–2106. https://doi.org/10.1007/s10530-016-1154-x
Williams LK, Shawn JD, Sindel BM, Wilson SC, Kristiansen P (2018) Longevity, growth and community ecology of invasive Poa annua across environmental gradients in the subantarctic. Basic Appl Ecol 29:23–31. https://doi.org/10.1016/j.baae.2018.02.003
Wódkiewicz M, Chwedorzewska KJ, Bednarek PT, Znój A, Androsiuk P, Galera H (2018) How much of the invader’s genetic variability can slip between our fingers? A case study of secondary dispersal of Poa annua on King George Island (Antarctica). Ecol Evol 8:592–600. https://doi.org/10.1002/ece3.3675
Acknowledgements
We thank two anonymous reviewers and the editor for remarks and discussion which helped us refine our ideas and improve the manuscript. This research was supported by The National Science Centre, Grant No 218361 (2013/09/B/NZ8/03293). Part of this study was carried out at the Biological and Chemical Research Centre, University of Warsaw, established within a project co-financed by the EU European Regional Development Fund under the Innovative Economy Operational Program, 2007–2013. Part of the plant material used in this research was collected at Henryk Arctowski Polish Antarctic Station.
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Rudak, A., Wódkiewicz, M., Znój, A. et al. Plastic biomass allocation as a trait increasing the invasiveness of annual bluegrass (Poa annua L.) in Antarctica. Polar Biol 42, 149–157 (2019). https://doi.org/10.1007/s00300-018-2409-z
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DOI: https://doi.org/10.1007/s00300-018-2409-z