Rewilding in the Garden: are garden hybrid plants (cultivars) less resilient to the effects of hydrological extremes than their parent species? A case study with Primula

Primula species and cultivars are popular garden plants, being represented within mainstream bedding-plant taxa (i.e. those planted out in flower ‘beds’ en masse to provide extensive displays of colour), as well as commonly used as herbaceous perennials in borders and woodlands, with certain species also being well-adapted respectively, to bog gardens (e.g. Primula bulleyana) or to more drought-prone ‘alpine’ rockeries (e.g. Primula allionii). Primula vulgaris was selected for this research given that both the wild species and cultivated varieties are widely used as ornamentals across temperate parts of the globe (Hayta et al. 2016). The wild P. vulgaris is a spring flowering perennial (naturally distributed across Europe, south-west Asia and northern Africa), and is associated with a range of habitats, from woodlands and hedgerows to unsheltered grasslands and heaths (Jacquemyn et al. 2009). It has been extensive bred to provide new cultivars that improve the uniformity and seasonality of flowering, in addition to enhancing the flower size and colour (Karlsson 2001). Consequently, the majority of cultivars now in existence are similar in overall size to the wild species but generally offer more substantial floral displays in an extensive range of colours. As with many commercial ornamental plants, the ancestry of these cultivars is not well documented. Therefore, the degree of cultivation is discussed relative to the morphological divergence from the wild species (i.e. variations due to flower size and colour).

Primula vulgaris (pale yellow flowers, 20–30 mm dia.) was selected as the main model species and included in all experiments. Cultivated forms of P. vulgaris were compared for their resilience to wet and dry regimes. These included i. Primula F1 ‘Cottage Cream’ (P. ‘Cottage Cream’) which resembles the wild species but is marginally more compact and has a reputation for reliable, consistent flowering, with flowers 22–35 mm dia.; ii. Plants from the Primula F1 ‘Alaska’ strain, namely ‘Alaska – White with Orange Eye’ (P. ‘Alaska WOE’), P. ‘Alaska-Blue’, P. ‘Alaska-Orange’ and P. ‘Alaska-Rose’; all the Alaska strain cultivars have large flowers 35–50 mm dia.; iii. Primula ‘Forza’ – with pink/peach flowers 22–35 mm dia. In addition, two other native species of Primula, i.e. P. veris and P. elatior were included in one experiment. Primula veris has an intermediate UK distribution but is only associated with well-drained natural habitats and is notably absent from much of the west of the UK (with higher rainfall patterns) (Brys and Jacquemyn 2009). Finally, P. elatior has a much more restricted UK distribution, being naturally confined to wet sites typically in woodlands and meadows (Taylor and Woodell 2008). Despite the natural distribution patterns, both these species are also used relatively commonly as garden plants. For all taxa, seed-raised plug plants were purchased and transplanted into 90 mm pots using a 3:1 mix of Levington M3 compost (95% fine peat, 5% coir with 233 g N, 104 g P and 339 g K m⁻³, pH: 5.3–6.0: Scotts, Frimley, Surrey, UK) and perlite, and grown-on in a glasshouse (18-22 °C) at the University of Sheffield, UK. Batches of plants were potted on 28 Nov. 2014 (Exp. 1) 15 Jan. 2015 (Exp. 3) and 28 Sep. 2015 (Exp. 2) prior to experimentation (see below).

The aim of this experiment was to determine how cultivated taxa of Primula performed compared to their parent species (Primula vulgaris), when exposed to combinations of drought and waterlogging. Plants of four taxa (P. vulgaris, P. ‘Cottage Cream’, P. ‘Alaska WOE’ and P. ‘Forza’- Fig. 1) were re-potted into 130 mm pots on 28 Feb. 2015 and grown-on under glass (with a day/night regime of 12 h 24 °C/12 h 18 °C and supplementary lighting [Helle Lamps, IR 400 HPS, 400 W] to ensure a consistent photoperiod and photosynthetic photon flux density > 1000 μmol m⁻² s⁻¹). Irrigation treatments were initiated on 13 Apr. 2015 and included a double stress treatment where plants were exposed to either drought or waterlogging, followed by a recovery phase (3 wk) before a second stress period composed of the same stress again or the alternative stress factor. Thus treatments were; double drought (DD), drought/waterlogging (DW), waterlogging/drought (WD), double waterlogging (WW) or an un-stressed control group (CC) (Table 1). Additional plants were harvested after the initial stress period to determine impact on biomass at this stage.

Control plants were watered weekly. In contrast, drought treatments comprised withholding irrigation for 3 wks, whereas waterlogging constituted placing a plant in a water bath, so the growing media was flooded to the surface, and kept saturated for 1 wk. Preliminary studies (data not shown) demonstrated that physiological effects of drought occurred 12–14 d after irrigation ceased, whereas equivalent responses occurred after only 2–3 d of waterlogging, as such the period water was withheld (3 wks), was not equal to the period of waterlogging (1 wk) (Table 1). Each treatment was represented by 8 replicate plants per taxa, randomly distributed across the glasshouse bench. Plants were recorded for quality every 3–4 d and destructive harvests implemented on 30 Jul. 2015. Data is presented for key phases only – before stress, after 1st stress, during recovery phase 1, after 2nd stress and during recovery phase 2, relating to 0, 22 40, 64 and 77 d of the experiment respectively.

Treatments were implemented to consider the impacts of seasonally redistributed rainfall on plant performance. As such, plants experienced either a ‘control’ or alternatively a ‘wet’ winter (Dec. 2015- Mar. 2016), followed by a ‘control’, ‘wet’ or ‘dry’ spring/summer (Apr. 2016-Aug. 2016). Control treatments were based on the seasonal average rainfall calculated from the 1981–2010 Sheffield Central data set. Wet treatments then received a 40% increase whilst dry treatments received a 40% reduction relative to the seasonal mean calculated from the historical data (Table 2).

The study was conducted outdoors at the University of Sheffield, South Yorkshire, UK. A single plant from each taxon (P. vulgaris, P. elatior, P. veris, P. ‘Cottage Cream’, P. ‘Alaska WOE’ and P. ‘Forza’) was randomly located within small experimental plots (trays 600 × 400 × 200 mm). Forty-eight experimental plots were used and distributed between the 6 irrigation treatments placed within 3 open-ended ‘rain-shelter’ polytunnels. Polytunnels were covered in translucent PVC to excluded natural rainfall but facilitate a PPFD of between 460 and 1450 μmol m⁻² s⁻¹. Controlled volumes of water were then supplied evenly across the plots using 6 drippers per plot. Plants were monitored weekly with final quality assessments terminated 16 Aug. 2016.

A final experiment determined how cultivated Primula taxa performed in an in vivo garden situation, when exposed to naturally varying hydrological regimes. Three hybrids of Primula from the Alaska strain (P. ‘Alaska Blue’, P. ‘Alaska Orange’ and P. ‘Alaska Rose’) were compared with P. vulgaris; ideally specimens of P. ‘Alaska WOE’ would also have been included, but these were undersized at time of planting. A garden in Skelton, East Yorkshire, UK. (53°42′46.10”N; 0°50′12.16”W) was chosen due to its heavy clay-loam floodplain soil, where a naturally-high ground water table could cause surface flooding on occasions, but also where the soil could desiccate, shrink and crack after prolonged dry periods. To escalate the potential stress plants may experience, control plots at ground level (2.5 × 2.5 m, l x b) were augmented with raised plots (300 mm above) and sunken plots (300 mm below) ground level. It was anticipated that the raised plots would improve drainage in the winter, but enhance risk of moisture deficits in summer, and conversely, sunken plots may predispose plants to winter waterlogging, but have greater moisture availability in summer. All plots comprised the parent clay soil without supplementary fertilizer, cultivated to a ‘crumb structure’ before planting. Each plot treatment (height) was represented by 2 plots each, and each taxon represented by 5 replicate plants per plot. Plants were planted 450 mm apart in a randomised manner on 24 Feb. 2015 and watered until established - 30 May 2015. Soil moisture status was monitored weekly (ML3 ThetaProbe Soil Moisture Sensor and HH2 Moisture Meter, Delta-T, Devices, Cambridge, UK) with data meaned from three samples per plot. The presence of any standing surface water was also noted. Plants were monitored for survival, growth and flower numbers present on a monthly basis and the experiment terminated on 24 Jun. 2016.

Plants were monitored for survival (%) and visual quality. Plants were assessed visually following Zollinger et al. (2006), where they were scored separately on degree of wilting, chlorosis and senescence based on a ranking 0–5 in each case. Scores across the three scales were combined to give each plant a total score out of 15. Flowers were also recorded for number per plant (flower score) or as biomass.

Chlorophyll florescence was used to determine levels of stress imposed in the first two experiments. The maximum quantum efficiency of PSII photochemistry (F_v/fm) was measured twice weekly (Handy PEA -Plant Efficiency Analyser, Hansatech Instruments, Kings Lynn, UK) on three randomly selected dark-adapted (30 min.) leaves per plant. The three measurements were meaned to obtain a single F_v/fm for each plant. Lower values occur when a plant is exposed to stress and indicate inactivation of PSII (photoinhibition) (Björkman and Demmig 1987; Murchie and Lawson 2013).

At the end of experimental periods (Exp. 1 and 2), plants were harvested and assessed for final biomass. Roots were washed and separated from above-ground material (top-growth). Dead leaves and stems were removed and biomass was dried (80 °C for 72 h), before dry weights were recorded. In some experiments top-growth was also assessed non-destructively by estimating the area of ground the plant covered. The longest leaf was identified and length from the centre of the plant measured (radius 1). A leaf at 90^o around from this was also measured (radius 2) and a mean radius value calculated. The surface area was then estimated from A = πr².

Analysis of visual assessments for quality, chlorophyll florescence, flower scores and plant coverage were analysed using ANOVA, with significant levels between means compared via Tukey post-hoc tests. Where variance in data was insufficient or the design unbalanced ANOVA was not applied (NA) and mean values only are presented. Percentage survival was calculated using visual quality scores, where 0 was taken to mean plant death. The dry weight of roots and shoots, and change in biomass between the treatments were analysed using the Welsh Test as assumptions of homogeneity of variance were violated, with subsequent treatment differences identified by Games-Howell tests. Analyses were conducted through ‘R’ version 3.3.1. For large data sets, data and analysis was restricted to a single taxon for ease of presentation (e.g. Exp. 1) otherwise comparisons across taxa were included where appropriate (e.g. Exp. 3). Data are depicted in tables/figures as mean values, with significant differences between treatments denoted by letters.

In P. vulgaris, exposure to drought during the first stress phase significantly reduced visual plant quality (DD and DW) and Fv/fm values (DW only), but scores improved again during the first recovery phase (Table 3). During the second stress, exposure to waterlogging or drought reduced visual scores compared to controls, but there was no effect on Fv/fm. On recovery, plants generally improved in visual quality, except for those previously exposed to WW (10.9) where quality remained significantly lower than controls (13.7, Table 3). Notably, all plants of P. vulgaris survived, irrespective of the stress combinations imposed (Table 3).

Drought also had a significant effect in P. ‘Cottage Cream’ during the first stress phase, but visual values did not always recover to that of controls during the first recovery phase, (i.e. 11.9 for DD, Table 4). A second drought episode reduced visual quality further (7.6 for DD) and caused some plant fatalities in DD (Table 4). Visual quality scores for DD, however, were not significantly different to those of the controls at the second recovery phase. In contrast, quality was significantly reduced in plants first waterlogged then exposed to drought (WD) when compared to controls (i.e. 10.0 vs 13.3, Table 4). Stress events reduced Fv/fm values, but these were rarely significantly different. Overall survival rate was high in P. ‘Cottage Cream’ with fatalities only associated with DD.

Exposure to the first stress reduced plant quality in P. ‘Alaska WOE’, irrespective of whether it was waterlogging or drought (Table 5). Most plants recovered, the exception being some of the specimens exposed to waterlogging (e.g. 9.7 for WW). A second period of stress generally reduced quality again, but only significantly so for the WW treatment (8.0), with visual values remaining low even during the second recovery period (Table 5). The WW treatment was associated with reductions in Fv/fm, and although some plants recovered, approximately 30% of P. ‘Alaska WOE’ specimens eventually died. Some fatalities (14%) were also noted in DD.

Primula ‘Forza’ was susceptible to loss of quality (and viability) to both drought and waterlogging. Unlike other taxa, both visual and Fv/fm values tended to continue to decrease during the first recovery phase (Table 6), corresponding to a number of fatalities at this stage. Exposure to a second round of stress reduced quality across all treatments, with lowest scores and highest fatalities associated with the DD and WD treatments, where only 14% of plants survived (Table 6).

After the initial stress event, there was no significant effect on biomass in any taxa (data not shown). After the second stress period, there was no effect on shoot biomass in P. vulgaris or P. ‘Cottage Cream’ but in the former, root biomass was reduced in DW compared to WD (Table 7). In P. ‘Alaska WOE’, shoot and root biomass was reduced in all treatments compared to controls except WD (shoots only). In P. ‘Forza’, both shoot and root biomass loss was greatest in treatments associated with the initial waterlogging (WD and WW). Flowers contributed a relatively small proportion of biomass, with the exception of P. ‘Forza’, which was relatively floriferous (Table 7).

Of the four taxa evaluated, P. vulgaris showed the most resilience, closely followed by P. ‘Cottage Cream’. Primula ‘Alaska WOE’ showed some intermediate levels of tolerance, although it was most susceptible to a double waterlogging treatment. In contrast, P. ‘Forza’ showed limited tolerance to waterlogging or drought and overall was the least resilient taxon.

Primula ‘Forza’ was the most damaged cultivar, showing some fatalities and loss of quality after a wet winter (W/C) (Fig. 2), but also intolerance to either a dry or wet spring-summer, especially after a previous wet winter i.e. (W/D and W/W) (Fig. 2). Treatments had no effect on P. vulgaris, and by the end of the experiment all plants demonstrating similar quality scores (Fig. 3) and 100% survival. Primula veris on the other hand, lost quality in the wet winter/wet spring-summer scenario (W/W), with 50% fatalities; whereas P. elatior had marginal non-significant quality reductions associated with control winter/dry spring-summer (C/D).

Above ground biomass tended to be greatest with P. vulgaris, but there were no significant differences due to treatment in any of the taxa (data not shown). Of the plants that survived though, specimens tended to have smaller canopies in P. veris W/D; P. ‘Cottage Cream’ W/W; P. ‘Alaska WOE’ C/D, C/W, W/D, W/W and P. ‘Forza’ W/W (Table 8).

Moisture levels in garden soils ranged between 0.35–0.46 m³ m⁻³ during winter, but no significant differences overall were noted between treatments (i.e. based on plot level). Values were less in summer, decreasing to 0.27 m³ m⁻³ during Aug. 2015 in one raised plot, but there was no evidence of plant injury at this point. Surface water (puddling) was noted in the ground level and sunken plots on 12–14 Dec. 2015 and 7 Feb. 2016, with additional surface water also apparent for the sunken plots on 27–29 Dec 2015, 15–17 Feb, 26–29 Mar. and 12 Apr. 2016. No surface water was noted on the raised plots. During these wet periods the crown of individual plants could be submersed in water for up to 48 h.

There was no evidence of treatment effects during the first spring (2015), but plant development the following year showed strong effects of both treatment and taxa (quality data for May 2016 is presented, Fig. 4). As before, P. vulgaris outperformed the cultivated forms (significantly so in the case of P. ‘Alaska Orange’ and P. ‘Alaska Rose’) with no loss of quality or size associated with any of the plot levels (Fig. 4, Table 9). In contrast, loss of quality in P. ‘Alaska Blue’ was greater with plants in sunken compared to raised plots. Primula ‘Alaska Blue’ in raised plots also performed significantly better than P. ‘Alaska Rose’ in any treatment (Fig. 4). Primula ‘Alaska Orange’ tended to be intermediate in its tolerance levels between the other two cultivars (differences NS). Flower score supported the other metrics of quality, with significantly higher numbers of flowers associated with P. vulgaris and lowest with P. ‘Alaska Rose’ (Fig. 5). By the end of the experiment (Jun. 2016) plant deaths were in the order of; Sunken plots P. ‘Alaska Rose’ = 60%, P. ‘Alaska Blue’ = 10% and P. ‘Alaska Orange’ = 10% and in the raised plots P. ‘Alaska Rose’ = 50%.