Research Article |
Corresponding author: Kristin Ludewig ( kristin.ludewig@uni-hamburg.de ) Academic editor: Sven Jelaska
© 2022 Kristin Ludewig, Yves P. Klinger, Tobias W. Donath, Lukas Bärmann, Carsten Eichberg, Jacob Gadegaad Thomsen, Eugen Görzen, Wiebke Hansen, Eliza M. Hasselquist, Thierry Helminger, Frida Kaiskog, Emma Karlsson, Torsten Kirchner, Carola Knudsen, Nikola Lenzewski, Sigrid Lindmo, Per Milberg, Daniel Pruchniewicz, Elisabeth Richter, Tobias M. Sandner, Judith M. Sarneel, Ralf Schmiede, Simone Schneider, Kathrin Schwarz, Åsa Tjäder, Barbara Tokarska-Guzik, Claudia Walczak, Odile Weber, Ludwik Żołnierz, Rolf Lutz Eckstein.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ludewig K, Klinger YP, Donath TW, Bärmann L, Eichberg C, Thomsen JG, Görzen E, Hansen W, Hasselquist EM, Helminger T, Kaiskog F, Karlsson E, Kirchner T, Knudsen C, Lenzewski N, Lindmo S, Milberg P, Pruchniewicz D, Richter E, Sandner TM, Sarneel JM, Schmiede R, Schneider S, Schwarz K, Tjäder Å, Tokarska-Guzik B, Walczak C, Weber O, Żołnierz L, Eckstein RL (2022) Phenology and morphology of the invasive legume Lupinus polyphyllus along a latitudinal gradient in Europe. NeoBiota 78: 185-206. https://doi.org/10.3897/neobiota.78.89673
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Plant phenology, i. e. the timing of life cycle events, is related to individual fitness and species distribution ranges. Temperature is one of the most important drivers of plant phenology together with day length. The adaptation of their phenology may be important for the success of invasive plant species. The present study aims at understanding how the performance and the phenology of the invasive legume Lupinus polyphyllus vary with latitude. We sampled data across a >2000 km latitudinal gradient from Central to Northern Europe. We quantified variation in phenology of flowering and fruiting of L. polyphyllus using >1600 digital photos of inflorescences from 220 individual plants observed weekly at 22 sites. The day of the year at which different phenological phases were reached, increased 1.3–1.8 days per degree latitude, whereas the growing degree days (gdd) required for these phenological phases decreased 5–16 gdd per degree latitude. However, this difference disappeared, when the day length of each day included in the calculation of gdd was considered. The day of the year of the earliest and the latest climatic zone to reach any of the three studied phenological phases differed by 23–30 days and temperature requirements to reach these stages differed between 62 and 236 gdd. Probably, the invasion of this species will further increase in the northern part of Europe over the next decades due to climate warming. For invasive species control, our results suggest that in countries with a large latitudinal extent, the mowing date should shift by ca. one week per 500 km at sites with similar elevations.
Flowering phenology, invasive plant, latitudinal gradient, legume, Lupinus polyphyllus, photoperiod
Plant phenology is the timing of seasonal events, such as budburst, greening, flowering, and fruit ripening (
The potential for adaptation of phenology may also be key to understanding the success of invasive plant species (
Latitudinal gradients provide the opportunity to study the effects of climate on plants in natural experiments (
Lupinus polyphyllus Lindl. (Fabaceae) is a perennial herbaceous hemicryptophyte originating from western North America that was introduced in Central Europe as an ornamental plant in the 19th century. From Central Europe and Scandinavia, the species spread very successfully to almost all parts of Europe, now ranging from the Pyrenees in the West to the Ural (and beyond) in the East (Eckstein et al., unpublished data). From North to South, L. polyphyllus is currently covering the full range of Europe, except for Mediterranean zones such as the Iberian Peninsula and Italy (
Our overall aim was to understand how the timing, temperature dependence of flowering and fruiting, and performance (canopy height, potential seed production and seed release height) of L. polyphyllus change along the latitudinal gradient from Central to Northern Europe. We tested differences between populations that were assigned to different climatic zones and quantified variation in phenology in relation to latitude. To our knowledge, the present study is the first attempt to quantify variation in phenology of an invasive plant across a large latitudinal gradient in the field. This information may help to develop more effective management schemes for this invasive plant. Generally, the species is managed by cutting at fixed calendar dates (
We wanted to test the following hypotheses:
We analysed Lupinus polyphyllus populations along a latitudinal gradient ranging > 2000 km from Luxembourg, in Central Europe, to Umeå, in northern Sweden (49°38' – 63°49', Fig.
Characteristics of the 22 study sites along the latitudinal gradient. For abbreviation of climatic zones, see Figure
Study site | Full site name | Coordinates (Latitude, Longitude) | Elevation (m a.s.l.) | Climatic zone | Weather station | Distance (km) | MAT (°C) | MAP (mm) |
---|---|---|---|---|---|---|---|---|
UMEA | Umeå | 63.82961°N, 20.33164°E | 38 | BOR | Umeå Flygplats 1 | 4.3 | 2.6 | 644 |
TRON | Trondheim | 63.41364°N, 10.40789°E | 41 | ATN | Trondheim-Voll Plu 2 | 2.3 | 4.7 | 925 |
RESE | Resele | 63.34757°N, 17.00437°E | 55 | BOR | Forse 1 | 22.4 | 2.5 | 536 |
RATT | Rättvik | 60.87959°N, 15.12866°E | 209 | BOR | Leksand 1 | 18.3 | 4.1 | 591 |
KARL | Karlstad | 59.40300°N, 13.62328°E | 78 | NEM | Karlstad Flygplats 1 | 17.0 | 5.7 | 635 |
KRIS | Kristinehamn | 59.33775°N, 14.19258°E | 139 | NEM | Kristinehamn 1 | 6.1 | 5.8 | 659 |
OREB | Örebro | 59.26483°N, 15.33968°E | 26 | NEM | Örebro Flygplats 1 | 17.3 | 5.8 | 586 |
LINK | Linköping | 58.17554°N, 15.71404°E | 99 | NEM | Malexander A 1 | 30.6 | 5.9 | 519 |
ODEN | Odense | 55.36990°N, 10.42298°E | 21 | CON | Odense Lufthavn 3 | 5.9 | 8.1 | 583 |
SCHL | Schleswig | 54.48772°N, 9.56911°E | 10 | ATN | Schleswig 4 | 4.0 | 8.0 | 926 |
KIEL | Kiel | 54.34886°N, 10.10497°E | 24 | ATN | Kiel-Holtenau 4 | 3.5 | 8.4 | 754 |
HAMB | Hamburg | 53.54843°N, 9.86951°E | 9 | ATN | Hamburg-Fuhlsbüttel 4 | 12.1 | 8.6 | 770 |
SWHA | Südwest-Harz | 51.66625°N, 10.60720°E | 508 | ALS | Braunlage 4 | 6.3 | 5.9 | 1263 |
WROC | Wrocław | 51.04966°N, 17.25088°E | 128 | CON | Wroclaw-Strachowice 5 | 25.3 | 8.4 | 588 |
ERZG | Erzgebirge | 50.93647°N, 13.71082°E | 432 | CON | Dresden-Klotzsche 4 | 20.2 | 8.9 | 667 |
MARB | Marburg | 50.80591°N, 8.80855°E | 332 | ATN | Cölbe, Kr. Marburg-Biedenkopf 4 | 5.6 | 8.9 | 756 |
RHON | Rhön | 50.46310°N, 10.04884°E | 767 | ALS | Wasserkuppe 4 | 8.4 | 4.8 | 1084 |
GIES | Gießen | 50.45559°N, 8.58841°E | 303 | CON | Giessen-Wettenberg 4 | 25.5 | 8.2 | 719 |
JAWO2 | Jaworzno | 50.23825°N, 19.22854°E | 273 | CON | Krakow -Balice 5 | 43.3 | 7.8 | 679 |
JAWO1 | Jaworzno | 50.23744°N, 19.22739°E | 275 | CON | Krakow 5 | 43.0 | 7.8 | 679 |
TRIE | Trier | 49.81556°N, 6.57417°E | 374 | ATC | Trier-Petrisberg 4 | 10.7 | 9.1 | 784 |
LUXE | Luxembourg | 49.63619°N, 6.17952°E | 365 | ATC | Luxembourg/Luxembourg 4 | 3.4 | 8.3 | 875 |
Position of the 22 study sites (for site abbreviations, see Table
Each participant in the study selected a population of L. polyphyllus along a road verge or in close vicinity to a road, in an open, sunny locality. For each population we documented geographic coordinates, elevation, and climatic parameters from the nearest weather station (Table
Ten randomly selected adult individuals, representative for each population, were marked early in the season in 2019. We focussed on the first developed central inflorescence of each of these marked individuals. Starting when the inflorescences were visible (mid-end April), we made digital photos of the inflorescence of each marked individual against a scale bar, usually a meter stick. We used photos for consistent measurements across sites and stored them for future analysis. The photos were sent to the project coordinator (RLE), who analysed all photos together with a student assistant. Additionally, all participants measured the maximum height from the ground to the top of the basal leaves (canopy height) and to the top of the inflorescence (seed release height) of the 10 marked individuals per measuring event on site. Usually, the photos and direct measurements were taken once per week until the first pods of the inflorescences were ripe. We obtained between five and twelve observations per site, resulting in 180 site × date combinations. Depending on the site location, observations ranged from 29 April to 4 August, with the majority of observations (160 site × date combinations) made between 6 May and 8 July.
In total, 1633 photos from 22 sites were analysed using the software ImageJ 1.52a (
Variable | Usage* | Description | Formula/Remarks |
---|---|---|---|
Canopy height | R | Maximum height from the ground to the top of the basal leaves (cm) | Measured in the field (usually weekly) |
Seed release height | R | Maximum height from the ground to the top of the inflorescence (cm) | Measured in the field (usually weekly) |
Total length of inflorescence | R | Length of inflorescence (cm) from the lowermost flower bud, flower or flower scar to the top (A–C in Fig. |
Determined via photos |
Length of the inflorescence with open flowers | A | Length from the lowermost flower/flower scar to the uppermost open flower (A–B in Fig. |
Determined via photographs; open flowers were defined as flowers with unfolded standard, visible keel, and elongated pedicel |
RLF | A | Relative length of the inflorescence with open flowers at each measuring event (tx) | |
doy | A/E/R | Day of the year | Day number (1st of January = day 1) |
gdd | A/E/R | Number of growing degree days using a base temperature of 5 °C | GDD=(Tmax – Tmin)/2 – TBase, if TMean > TBase |
gdh | E | Cumulated day length: growing degree day length (hours), called growing day hours | GDH=GDD*Day length of each day included in calculation of GDD |
Flow.half | R | Day of the year (doy.flow.half) or number of growing degree days (gdd.flow.half) when half of the actual length of the inflorescence carried open flowers | Estimated per site via RLF using logistic regressions |
First.flow | R | Day of the year (doy.first.flow) or number of growing degree days (gdd.first.flow) when the first flower was formed | Determined via photographs |
First.ripe | R | Day of the year (doy.first.ripe) or number of growing degree days (gdd.first.ripe) when the first black pod was formed | Determined via photographs |
Measurements taken along the inflorescence of Lupinus polyphyllus (a): A – C: total length of inflorescence; A – B: length of inflorescence with open flowers; an example photo showing the flower development taken at the population KARL, on the 7th of June 2019 by Lutz Eckstein (b) and example photos showing the different stages first.flow, on 24th of May (c), flow.half, on 31st of May (d), and first.ripe, on 5th of July (e). White arrows show an open flower and a ripe pod, in (c) and (e), respectively.
Using the photo measurements, we calculated the relative length of the inflorescence with open flowers (RLF) for each plant individual per measuring event (Table
We obtained temperature measurements from meteorological stations located closest to the field sites (distances between 2.3 and 43.3 km from the studied sites (Table
Since light is an important driver of phenology alongside temperature, and day length increases with latitude, we aimed at incorporating differences in day length in our analyses by creating a variable (growing degree day length, in accumulated hours: gdh) that combines growing degree days and day length. For each population and day of the year, the day length was calculated using the ‘geosphere’ package in R (
For all variables, we used mean values from the ten measured individuals per site. We analysed the data in two different ways. Firstly, we calculated linear regressions of doy.first.flow, doy.flow.half, doy.first.ripe, gdd.first.flow, gdd.flow.half, and gdd.first.ripe against latitude (decimal degrees north) to quantify the rate of change in flowering, seed ripening, and seed shedding phenology with latitude. In these analyses, we excluded the two sites of the Alpine south climatic zone (SWHA, RHON), since these populations potentially experience much higher temperature selection due to a cold montane climate as compared to other sites at similar latitudes and would lead to confounding latitude and elevation. Secondly, we did one-way ANOVAs of all six dependent variables with the climatic zones according to
The maximum canopy height varied by a factor of 2.5 between sites (min: HAMB – 34.9 cm; max: JAWO2 – 88.0 cm). Averaged across sites of the same climatic zone (Fig.
a canopy height (cm) b seed release height (cm) c length of the inflorescence (cm) during the time of biomass maximum for sites grouped according to climatic zones according to
The doy at which the inflorescences of L. polyphyllus reached first.flow, flow.half, and first.ripe increased with decreasing mean annual temperatures of the climatic zones (Fig.
Day of year (doy), at which a the first open flower was observed (first.flow) b half of the length of the inflorescence bears open flowers (flow.half) c the first ripe (black) pods were observed (first.ripe) for each climatic zone (
The gdd at which the inflorescences reached first.flow did not differ between the climatic zones (F5,16 = 0.96, p = 0.468). For the next phenological phase, flow.half, the gdd tended to be affected by the climatic zone (F5,16 = 2.48, p = 0.076). Finally, the effects of climatic zone on gdd were significant for first.ripe (F5,13 = 5.96, p = 0.0047). More specific, the gdd at which the inflorescences reached flow.half and first.ripe tended to be lower for the zones NEM, ALS and BOR than for ATC, CON and ATN (data not shown). While these patterns were found for growing degree days (gdd), they disappeared when the day length was taken into account as growing day hours (gdh, Fig.
Growing day hours (gdh), at which a the first open flower was observed (first.flow) b half of the length of the inflorescence bears open flowers (flow.half) c the first ripe (black) pods were observed (first.ripe) for each climatic zone (
Our regression analyses showed that the day of the year, on which the first open flower was observed (first.flow), half of the inflorescence’s length at each site had open flowers (flow.half), and the first ripe pod (first.ripe) was observed increased significantly (p < 0.001) with latitude (Appendix
The accumulated growing degree days (gdd) until the inflorescence at each site reaches first.flow, flow.half, and first.ripe, decreased significantly (all p-values < 0.05) with latitude (Appendix
The data supporting the findings of this study are openly available in the repository dryad at https://doi.org/10.5061/dryad.stqjq2c3t (
According to our findings, canopy height and the length of the inflorescence of Lupinus polyphyllus does not vary significantly among climatic zones. Seed release height shows significant variation among climatic zones but there is no consistent pattern with latitude. Consequently, we found no evidence for our first hypothesis that the latitudinal gradient affects these measures of performance of the invasive L. polyphyllus. Plant height and seed mass usually decrease with decreasing temperatures along latitudinal gradients (
The day of year (doy) at which the first open flower was found, half of the length of the inflorescence had open flowers and the doy at which the first black, ripe pod was found, increased significantly with northern latitude. Populations in zones with a colder climate reach these phenological phases significantly later than populations in climatic zones with higher annual temperatures. Therefore, and as stated in our second hypothesis, the phenology of flowering and seed ripening is delayed in populations of L. polyphyllus in the northern part of the gradient. More specifically, all measured phenological parameters were delayed under colder climate conditions, i.e., at higher latitudes or elevations (boreal and alpine south zone). This is in contrast to studies, in which plant material from latitudinal gradients was collected and grown in common garden experiments (
While the accumulated growing degree days (gdd) required to reach the different phenological phases decrease with latitude, suggesting that energy requirements for flowering and fruit ripening are lower at higher latitudes, this effect disappeared when day length was considered. This finding shows that longer day lengths may compensate for the fewer growing degree days at northern latitudes. As a result, the energy demands of L. polyphyllus to reach the studied phenological phases, measured as growing day hours (gdh), do not differ significantly along the latitudinal gradient. The first finding is in line with
Longer day length during summer allows L. polyphyllus to fulfil its life cycle relatively quickly in the investigated northern latitudes. Therefore, populations in the northern part of the gradient have probably not changed their climatic niche (
For invasive species control, our results suggest that in countries with a large latitudinal extent, the timing of management (e.g. mowing date) should shift by ca. one week every 500 km, at least for sites at lower elevations. For example, in Germany (ca. 900 km south-north extent) or Sweden (ca. 1600 km south-north extent), the southernmost populations should be managed ca. 12 and 22 days earlier, respectively, than the northernmost populations. The variable flow.half may represent a good indicator for the optimal time for management since no viable seeds are present at this stage. In our study year, flow.half was reached in the southernmost populations in Germany and Sweden at the end of May and beginning of June, respectively. With later mowing the possibility of seed shedding increases and the potential to limit the spread of L. polyphyllus decreases. The practical planning of phenology-based control of invasive plants (
We thank Denis Lafage for help with an app for photo submission and Tobias Knieps and Muriel Fauth for help with analysis of photos, data input and acquisition of climate data. We thank Adrian Wächtershäuser (site GIE) and Katrin Eichberg for help in the field (site TRIE). We thank Nina Sajna and one anonymous referee for valuable comments on the manuscript.
Results of the global Moran´s I test for spatial autocorrelation in the statistical models.
Dependent | Independent | Figure | Moran’s I standard deviate | p-value |
---|---|---|---|---|
Canopy height | Climatic zone | 3a | 0.08931 | 0.4644 |
Seed release height | Climatic zone | 3b | -0.12235 | 0.5487 |
Length infl. | Climatic zone | 3c | -0.11074 | 0.5441 |
First.flow(doy) | Climatic zone | 4a | -0.21516 | 0.5852 |
Flow.half(doy) | Climatic zone | 4b | -0.11702 | 0.5466 |
First.ripe(doy) | Climatic zone | 4c | -0.57733 | 0.7181 |
First.flow(gdh) | Climatic zone | 5a | -0.93938 | 0.8262 |
Flow.half(gdh) | Climatic zone | 5b | 0.26693 | 0.3948 |
First.ripe(gdh) | Climatic zone | 5c | 2.1708 | 0.01497 |
First.flow(doy) | Northern latitude | A1a | 0.045778 | 0.4817 |
Flow.half(doy) | Northern latitude | A1b | 0.34373 | 0.3655 |
First.ripe(doy) | Northern latitude | A1c | 0.21317 | 0.4156 |
First.flow(gdd) | Northern latitude | A2a | 0.87796 | 0.1900 |
Flow.half(gdd) | Northern latitude | A2b | -0.36804 | 0.6436 |
First.ripe(gdd) | Northern latitude | A2c | -0.78436 | 0.7836 |
First.flow(gdh) | Northern latitude | A2d | -0.0080847 | 0.5032 |
Flow.half(gdh) | Northern latitude | A2e | -0.0091361 | 0.5036 |
First.ripe(gdh) | Northern latitude | A2f | 2.2439 | 0.01242 |
Linear regressions of the day of year (doy) for each site, at which a the first open flower was observed (first.flow) b half of the inflorescence’s length bears open flowers (flow.half) c the first ripe (black) pods was observed (first.ripe), against latitude (°N). Only the sites in black were included into the model. White symbols are sites of the high altitude, alpine south climatic zone (RHON, SWHA) that were omitted from this analysis and only shown for comparison. Grey areas depict 95% confidence intervals.
Linear regressions of the accumulated growing degree days (gdd; from January 1, base temperature: 5 °C from weather stations) for each site, until a the first open flower was observed (first.flow) b half of the inflorescence’s length bears open flowers (flow.half) c the first ripe (black) pods were observed (first.ripe), against latitude (°N). Furthermore, linear regressions of the accumulated growing day hours (gdh) for each site, until d the first open flower was observed (first.flow) e half of the inflorescence´s length bears open flowers (flow.half) f the first ripe pod was observed (first.ripe) against latitude (°N). Only the sites in black were included into the model. White symbols are sites of the high altitude, alpine south climatic zone (RHON, SWHA) that were omitted from this analysis and only shown for comparison. Grey areas depict 95% confidence intervals.