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Article

Are There Resource Allocation Constraints to Floral Production in the Endangered Barbarea vulgaris subsp. lepuznica (Southern Carpathians, Romania)?

by
Dan Gafta
1,*,
Emilia Aczel
1,
Rahela Carpa
2,
Claudia Dănău
3 and
Irina Goia
1
1
Department of Taxonomy and Ecology, 3B Centre, Babeș-Bolyai University, 42 Republic Street, 400015 Cluj-Napoca, Romania
2
Department of Molecular Biology and Biotechnonolgy, 3B Centre, Babeș-Bolyai University, 1 M. Kogălniceanu Street, 400084 Cluj-Napoca, Romania
3
Retezat National Park Administration R.A.–NFA Romsilva, 284 Nucșoara, 337423 Sălașul de Sus, Romania
*
Author to whom correspondence should be addressed.
Conservation 2025, 5(4), 56; https://doi.org/10.3390/conservation5040056
Submission received: 24 July 2025 / Revised: 24 September 2025 / Accepted: 1 October 2025 / Published: 4 October 2025
(This article belongs to the Special Issue Conservation Biology, Management of Natural Resources, and Protected Areas Policies)
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Abstract

Given the endangered status and very limited distribution of Barbarea vulgaris R.Br. subsp. lepuznica (Nyár.) Soó in stressful, high-elevation habitats, where these plants must prioritise the resource acquisition and vegetative growth to sustain their survival and persistence, we aimed to reveal possible abiotic/biotic-driven constraints in biomass allocation for flower production. Three functional traits, i.e., the tallest shoot height, leaf mass area (LMA) and number of inflorescences (racemes), were measured in thirty plants in each of the three studied populations differing in altitude and sheep grazing intensity (P1—1700 m, grazed; P2—1900 m, ungrazed; P3—2100 m, ungrazed). The LMA and dominant shoot height were significantly higher and, respectively, lower in P3 compared with P1. Although the mean number of racemes in P1 was lower than in P2 and P3, the differences were not statistically significant. The tallest shoot height, followed by the LMA, displayed the highest contribution to differentiating the three populations. The raceme count decreased significantly with increasing height of the dominant shoot in P1 and P2, and also with increasing LMA in P3. The observed constraint in raceme production within all populations is very likely one facet of the trade-off between reproductive and vegetative allocation under harsh edapho-climatic conditions. The studied plants have adopted a conservative-tolerant strategy to cope with the abiotic stress at higher elevations, but an acquisitive-tolerant strategy in face of grazing. The subspecies lepuznica seems to be in a favourable conservation status, but a close monitoring in grazed areas is recommended.

1. Introduction

The analysis of intraspecific trait variation is a useful approach in functional ecology to figure out how conspecific plants respond through phenotypic plasticity to environmental stress and biotic interactions [1,2]. In particular, the patterns of biomass allocation for resource acquisition, vegetative growth and reproduction may reflect functional trade-offs and life history strategies that have evolved following different selection pressures and constraints [3,4]. Such whole-plant, economic trade-offs are more conspicuous in stressful habitats, where plants may be constrained to reduce their allocation to sexual reproduction, to the detriment of vegetative growth, to cope with the local unfavourable biotic/abiotic conditions and to maximise their fitness [5].
The harsh edapho-climatic conditions occurring at higher altitudes, such as low winter temperatures, short growing season, strong winds and shallow, skeletal soils, have long shaped the resource allocation strategies adopted by alpine plants [6]. As a general rule, in high-mountain habitats, the height of conspecific plants decreases with increasing elevation [7,8,9,10,11,12,13,14], which is very likely because smaller plants have lower resource requirements and are less exposed to strong winds. Also, the leaf mass area (LMA) usually increases within plant species with rising elevation [12,15,16], since tougher, high-density leaves are, among other features, more resistant to cold [17,18]. Besides, high LMA is closely associated with the resource-conservative strategy developed in harsh environments [15,19,20]. Plants growing at high altitudes usually allocate proportionally less resources to sexual reproduction than their conspecifics occurring at lower elevations [16,21,22]. Thus, a decrease in the number of distinct flowers or inflorescences with increasing elevation was reported in various species [7,8,9,10,14,23,24,25,26]. This relationship stems from an inexorable energetic trade-off between vegetative and reproductive investment under limited resources (e.g., soil nutrients) and harsh climate (e.g., unpredictable early/late frosts), since the alpine plants need to allocate a higher proportion of their resources for survival and persistence [21,27]. However, under similar abiotic and biotic conditions, there is a positive allometric relationship between plant size (e.g., height) and reproductive allocation [28].
Plants are also able to reallocate their resources among different organs in order to cope with herbivores. Generally, perennial plants that have developed under grazing regimes have shorter stature than those growing without grazing pressure [29,30,31,32]. This is part of the plant’s avoidance strategy aimed to avoid grazing [33,34]. Instead, the small, grazed plants can invest more in regrowth after defoliation if they have the ability of resprouting [35]. As a response to grazing, many plants usually allocate more resources to leaves following either the tolerance or avoidance mechanism [33,36] corresponding to the acquisitive and, respectively, conservative strategy [19]. Grazing-tolerant plants display low LMA after grazing by increasing their photosynthetic area, in order to maximise resource acquisition for recovery and/or regrowth [31,34,37,38]. On the contrary, plants that attempt to avoid grazing exhibit high LMA, as herbivores prefer tender rather than tough leaves [32,38,39,40,41,42]. Biomass allocation to sexual reproduction may also be constrained by grazing, given that a part of the available resources should be directed to building new leaves and shoots in order to compensate for the biomass loss. In fact, the number of flowers reaches higher values in perennial plants from ungrazed habitats compared with their conspecifics affected by grazing, which in turn are stimulated to regenerate vegetatively [43,44]. Moreover, grazing can reduce or even inhibit seed production in biennials and perennials [33,36].
The plastic, intraspecific variations in resource allocation to flowers (seeds) are good indicators of the reproductive effort and strategy adopted by plants to maximise their fitness in relation to their biotic/abiotic environment. Such indicators achieve particular relevance for the rare, endangered plant species that occur in harsh environments and are represented via a few small populations, whose viability is critical for their in situ conservation [45]. This is also the case for Barbarea vulgaris subsp. lepuznica, which, unlike the common and widespread subsp. vulgaris, is a taxon that is sub-endemic to the Southern Carpathians. To date, no studies of any kind have been performed on subsp. lepuznica.
Based on the current theories, we presumed that constraints in vegetative and/or reproductive resource allocation should be observed in B. vulgaris subsp. lepuznica individuals growing at higher elevations or under stronger grazing pressure. In particular, the aim of this study was to answer the following questions: (i) are there differences in resource investment in leaves, shoot growth and sexual reproduction between plants developing under contrasting conditions in terms of sheep grazing pressure and/or abiotic stress? (ii) Are there trade-offs in flower production with respect to leaf/shoot growth? (iii) If yes, are these constraints stronger under sheep grazing or under harsher environmental conditions? We were especially interested in the plant response in terms of investment in sexual reproduction, given the endangered status of subsp. lepuznica and its very limited distribution area. We expected to observe decreasing resource allocation to floral production for the benefit of shoot height growth and leaf mass area once the stress determined by high elevation conditions or grazing becomes stronger.

2. Materials and Methods

2.1. Study Area

The study area is situated in the Southern Carpathians (Romania), specifically in the Retezat Mountains and within the boundaries of the Retezat National Park (Figure 1). The study sites are relatively homogeneous in relation to bedrock type, namely metamorphic rocks, such as micaceous schists and paragneisses [46]. The climate is cold-temperate (mean annual temperature between 0 and 2 °C and mean annual precipitation of about 1200 mm) but influenced by the convergence of Atlantic and Mediterranean air masses [47].

2.2. Study Taxon and Population Sites

Barbarea vulgaris R.Br. subsp. lepuznica (Nyár.) Soó is a short-lived, perennial forb that is distributed in wet, open habitats, along streamsides within the upper montane–subalpine belt of the Retezat Mountains. A doubtful, small, disjunct area of occurrence was reported in the Vršačke Hills (Serbia) at only 200–300 m a.s.l., mainly along the margins and glades of mixed deciduous forests, but also on degraded screes beside roads [48]. The subsp. lepuznica is considered critically endangered by different authors [49,50], although it has a contentious taxonomic status. Initially described as a new species by Nyárádi [51], several authors list it as a distinct subspecies based on the shape of the basal leaves, which are entire or divided by only one pair of laciniae [52,53,54]. Instead, the Euro + Med PlantBase [55] and EUNIS [56] databases consider it to be synonymous with subsp. vulgaris.
Among the few extant natural populations of B. vulgaris subsp. lepuznica, we selected three of them that encompassed the widest altitudinal range and intensity levels of sheep grazing. The selected populations are located along the valleys of two shallow streams: Population 1 (P1) in the Peleaga Valley, at around 1700 m a.s.l., and Populations 2 and 3 (P2 and P3) in the Mării Valley, at about 1900 m and, respectively, 2100 m a.s.l. (Figure 1). All three populations have developed on sunny slopes and similar bedrocks, whereas the soil depth/skeleton content is mainly determined by differences in terrain slope (Table 1). The plants from P1 have developed under moderate sheep grazing in summer. Population 2 might be subject to occasional grazing in late summer/early autumn, so we considered it essentially unaffected by the sheep flocks. Population 3 is established on a steeper, rocky slope covered by screes and is free from sheep grazing (Table 1).
The plant communities hosting the three studied populations can all be ascribed to the order Adenostyletalia alliariae Br.-Bl. 1930, which encompasses tall-herb, hygrophilous vegetation developed on fertile soils at high elevations. Nevertheless, the graminoid cover was much lower at P2 and P3 sites compared with their P1 counterpart where Deschampsia cespitosa was dominant.
One soil sample per population was collected at the depth of 5 cm and temporarily preserved in a paper bag. The pH (in distilled water) of each soil sample was subsequently measured in the lab using a Multi340i/SET (WTW GmbH, Weilheim, Germany).

2.3. Plant Sampling and Trait Data Collection

The field work was carried out in July 2023 based on a standardised protocol for plant sampling and measuring functional traits. Thirty plants, at least two metres apart, were randomly selected within each population, in order to prevent the sampling of genetically identical individuals. The height of the tallest shoot (excluding the inflorescence peduncles) and the number of racemes were recorded in each sampled plant. Three leaves were randomly collected from each individual, and subsequently, three discs with a diameter of 17 mm were cut out from each sampled leaf. All leaf discs were air-dried in a dark, ventilated room for two months before being weighed in the lab using a high-precision analytical balance (Kern & Sohn, Balingen, Germany). The leaf mass per area (LMA) was calculated by dividing the leaf dry mass by the fresh leaf area.
The tallest shoot height and LMA are considered relevant traits for estimating the intensity of two different functional processes, i.e., vegetative growth and, respectively, resource acquisition [57]. The number of inflorescences (racemes) per plant individual was employed as a proxy of reproductive investment.

2.4. Statistical Analyses

To test the significance of differences in trait values between the three populations, a nested ANOVA was separately employed for each trait, while accounting for between-plant variability within populations and, if the case, between-leaf variability within plants. Unlike the fixed effect of population, the ‘Leaf’ and ‘Plant’ were considered random factors. When the null hypothesis of equal means was rejected, all possible post hoc, pairwise comparisons of population means were performed through the Tukey-Kramer procedure.
The assignment of each sampled plant to one of the three populations, as well as the relative contribution (importance) of each trait to the distinction of the three populations, was predicted via the Bootstrap Forest model. The prediction accuracy of the bootstrap forest model was assessed via the entropy R-square and the misclassification rate.
Either multiple linear or simple non-linear regression analysis was employed to reveal—within each population—the expected trade-offs between the number of racemes (as the response variable) and the tallest shoot height and/or leaf mass area (as predictors). The interaction term between the two mentioned predictors was also tested but it resulted always non-significant; therefore, it was not considered in the final models of multiple linear regression. For complying with the assumptions of the parametric tests and reducing the heteroscedasticity, all variables involved were log-transformed prior to analyses.
All numerical analyses were conducted in JMP Pro v18.1 (JMP Statistical Discovery LLC, Cary, NC, USA).

3. Results

The fixed effect of ‘Population’ on both LMA and maximum height was statistically significant (Table 2 and Table 3). The lower proportion of variance explained in shoot maximum height compared with LMA (as shown by the R-square values) was mostly determined by the larger noise variance associated with the random effects. The plants from P1 displayed a significantly lower mean LMA than those from P3, whereas their counterparts from P2 was indistinguishable in this respect from the other two (Figure 2a). The plants from P3 were on average significantly shorter than their counterparts from P1 and P2, whereas the latter two did not differ significantly in terms of maximum height (Figure 2b). Although the mean number of racemes in P1 was lower than in the other two populations, the differences were not statistically significant, given the large with-population variance and the very low R-square value (Table 4, Figure 2c).
The Bootstrap Forest model showed a fairly good accuracy (misclassification rate = 0.178) in predicting the plant membership based on the three traits considered. The maximum height, followed by the LMA, displayed the highest contribution to differentiating the three populations (Figure 3).
The number of racemes per plant decreased significantly with increasing height of the tallest shoot in all populations (Figure 4), but the strength of this relationship was stronger, and the regression slope was obviously steeper in P3 (Figure 4c). While the shapes of the regression curves associated with P1 and P2 were quite similar, the latter curve positioned slightly above its P1 counterpart, as indicated by their apparent intercepts when the log of shoot height equals 3 cm (Figure 4a,b).
When both the dominant shoot height and LMA were used as linear predictors of the raceme count, no significant effects were detected in P1 and P2 (Table 5). Instead, significant negative effects were revealed in P3, in which the number of racemes declined sharply with increasing both LMA and maximum shoot height (Table 5). The effect size of the latter was about 50% larger than that of the former.

4. Discussion

4.1. Trait Response to Increasing Elevation

The plants growing at the highest altitude (P3) displayed the strongest response in terms of shoot growth and leaf mass area, namely by reducing and, respectively, increasing the resource allocation. These are typical conservative adaptations to the more severe edapho-climatic conditions in the upper subalpine belt, where strong winds and frequent frosts promote shorter statures and tougher, high-density leaves [6,17,18]. Similar trait adjustments were documented in many alpine plant species throughout Europe [8,13,14,15] and eastern Asia [9,10,12,16].
Contrary to our expectations, the number of racemes per plant did not decrease toward higher elevations. One possible explanation is that the altitudinal range of distribution of the studied plant taxon is not wide enough (only 400 m) to detect perceptible variations, although this is not always the case [58]. Yet, another explanation could be given by the possible decline in the number/biomass of flowers composing the racemes with increasing elevation. This result is, however, not out of the norm, as similar outcomes [13,15] or even increasing reproductive investment with altitude [11,12] were reported in certain montane plant taxa. Such inconsistent results suggest that the pattern of reproductive allocation along the altitudinal gradient might be conditioned by the specific gene pool, governed by interactions between genetic background and local environmental conditions, or susceptible to third-party processes (e.g., interspecific facilitation).

4.2. Trait Response to Grazing

Grazing had no effect on plant stature, probably because sheep prefer to browse the leaves instead of the tougher and thicker shoots. However, grazing seems to have induced a weak response of plants from P1 consisting in reduced leaf mass per area and raceme production.
Building tender leaves (i.e., with low LMA) is a typical response of grazing-tolerant plants to defoliation that could potentially counterbalance the loss of photosynthetic area and allow fast recovery/regrowth [34,35,37,38,40,41]. This was actually observed in sprouting shoots of B. vulgaris subsp. vulgaris emerging from adventitious root buds after experimental biomass removal [59].
Contrary to the expected negative relationship between altitude and floral production, there was a mild increase trend in number of racemes toward higher elevations, which suggests a possible weak effect from grazing. Despite the non-significant differences, the slightly lower mean number of racemes produced by the plants growing at the lowest elevation under grazing regime may be a consequence of resource re-allocation to the new leaves and shoots to be built following the defoliation by sheep. Such a constraint in resource investment to flower production is triggered by the browsed plants being stimulated to regenerate vegetatively [43,44]. Under the scenario of a further increase in sheep grazing intensity within Population 1, the success rate of generative reproduction might be affected, as suggested by an experiment showing a decrease in whole-life seed production in damaged plants of B. vulgaris subsp. vulgaris [60].

4.3. Allocation Trade-Offs Between Reproductive and Vegetative Traits

The negative relationship between the raceme count and maximum shoot height, which was observed in all studied populations, reflects very likely a trade-off in resource allocation that is probably determined by the limited soil nutrients available in the upper montane–subalpine belt. Such a hypothesis is supported by the opposite, widely observed pattern (i.e., positive allometric relationship between plant size and reproductive allocation) that has been documented in many different plant populations occurring in benign habitats [28,61,62,63], including populations of Barbarea vulgaris subsp. vulgaris growing in old fields [64]. Although the shape of this allometric relationship was very similar between Population 1 and 2, the number of racemes borne by plants of the same height was slightly higher in the latter population, suggesting a somewhat stronger trade-off under grazing pressure.
The additional negative relationship between raceme count and leaf mass area, exclusively observed in Population 3, suggests a further constraint in resource allocation to inflorescence formation due to extreme soil rockiness (i.e., steeper slope cover with scree) and harsher climatic conditions above 2000 m altitude. Similar allocation constraints to sexual reproduction with respect to vegetative growth were also observed in other plant species populations distributed at high elevations [21,25,65,66]. Given the higher cost of sexual reproduction [67], many high-mountain plants are constrained to allocate a higher proportion of their resources first to survival and storage reserves [25].

4.4. Synthesis, Limitations and Implications for Conservation

Overall, the indirect effects of altitudinal differences (expressed through variation in edaphic–climatic factors) on the mean trait values measured in plants of B. vulgaris subsp. lepuznica were stronger and more conspicuous compared to the effects induced by the differences in grazing pressure. Increasing elevation had the strongest effect on the patterns of resource allocation within the studied plants, which were constrained to invest more to building tough leaves at the expense of vegetative growth. The moderate, extensive grazing displayed only weak, negative effects on resource allocation to leaves and inflorescences. The present findings show that the individuals of B. vulgaris subsp. lepuznica have adopted a resource-conservative strategy to cope with the abiotic stress at higher elevations, but a resource-acquisitive, tolerant strategy in the face of grazing at lower elevations.
The present study has an inexorable limitation that could not be overcome. Thus, the effects of elevation and grazing on the leaf mass area could not be clearly separated, since there was no ungrazed population of subsp. lepuznica at the lower altitudinal limit of its distribution range. Nevertheless, the results obtained herein bring some evidence of trade-offs in the resource investment to sexual reproduction and vegetative growth, which translate in increasing allocation constraints to floral production toward higher elevations.
Until the presumed inhibitory effects on sexual reproduction success become visible and of concern, sheep grazing may be maintained at current intensity levels. At the time of this investigation, Barbarea vulgaris subsp. lepuznica seems to be in a favourable conservation status, but a close monitoring of its few populations that occur in grazed areas is recommended.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/conservation5040056/s1, Table S1: Original trait data associated with 90 plants of Barbarea vulgaris subsp. lepuznica sampled in the three studied populations.

Author Contributions

Conceptualization, D.G. and I.G.; data curation, I.G.; formal analysis, D.G.; investigation, E.A., R.C. and C.D.; methodology, D.G. and I.G.; project administration, I.G.; resources, E.A., R.C., C.D. and I.G.; supervision, D.G.; visualisation, D.G.; writing—original draft, D.G.; writing—review and editing, D.G., E.A., R.C., C.D. and I.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The dataset of plant traits analysed in this study is included in the Supplementary Materials.

Acknowledgments

Special thanks go to the National Forest Administration-Romsilva, Zoran Acimov (director of the Retezat National Park) for granting a free pass, and to rangers Ioan Dăjulesc and Bogdan Danciu for their assistance in the field.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. de Bello, F.; Lepš, J.; Sebastià, M.T. Predictive value of plant traits to grazing along a climatic gradient in the Mediterranean. J. Appl. Ecol. 2005, 42, 824–833. [Google Scholar] [CrossRef]
  2. Laliberté, E.; Shipley, B.; Norton, D.A.; Scott, D. Which plant traits determine abundance under long-term shifts in soil resource availability and grazing intensity? J. Ecol. 2012, 100, 662–677. [Google Scholar] [CrossRef]
  3. Bazzaz, F.A.; Grace, J. Plant Resource Allocation; Academic Press: New York, NY, USA, 1997. [Google Scholar]
  4. Weiner, J. Allocation, plasticity and allometry in plants. Perspect. Plant Ecol. Evol. Syst. 2004, 6, 207–215. [Google Scholar] [CrossRef]
  5. Bazzaz, F.A.; Ackerly, D.D.; Reekie, E.G. Reproductive Allocation in Plants. In Seeds: The Ecology of Regeneration in Plant Communities; Fenner, M., Ed.; CABI Publishing: Wallingford, UK, 2000; pp. 1–29. [Google Scholar]
  6. Körner, C. Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems, 3rd ed.; Springer: Cham, Switzerland, 2021. [Google Scholar]
  7. Fabbro, T.; Körner, C. Altitudinal differences in flower traits and reproductive allocation. Flora 2004, 199, 70–81. [Google Scholar] [CrossRef]
  8. Gabel, E.R.; Sattler, J.; Reisch, C. Genetic variation and performance of the alpine plant species Dianthus callizonus differ in two elevational zones of the Carpathians. Alp. Bot. 2017, 127, 65–74. [Google Scholar] [CrossRef]
  9. He, J.D.; Xue, J.Y.; Gao, J.; Wang, J.; Wu, Y. Adaptations of the floral characteristics and biomass allocation patterns of Gentiana hexaphylla to the altitudinal gradient of the eastern Qinghai-Tibet Plateau. J Mt. Sci. 2017, 14, 1563–1576. [Google Scholar] [CrossRef]
  10. Takahashi, K.; Matsuki, S. Morphological variations of the Solidago virgaurea L. complex along an elevational gradient on Mt Norikura, central Japan. Plant Species Biol. 2017, 32, 238–246. [Google Scholar] [CrossRef]
  11. Paudel, B.R.; Dyer, A.G.; Garcia, J.E.; Shresta, M. The effect of elevational gradient on alpine gingers (Roscoea alpina and R. Purpurea) in the Himalayas. PeerJ 2019, 7, e7503. [Google Scholar] [CrossRef]
  12. Xu, B.; Wang, J.; Shi, F. Impacts of ontogenetic and altitudinal changes on morphological traits and biomass allocation patterns of Fritillaria unibracteata. J. Mt. Sci. 2020, 17, 83–94. [Google Scholar] [CrossRef]
  13. Kiełtyk, P. Intraspecific morphological variation of Bellidiastrum michelii (Asteraceae) along a 1,155 m elevation gradient in the Tatra Mountains. PeerJ 2021, 9, e11286. [Google Scholar] [CrossRef]
  14. Kiełtyk, P. Patterns of floral allocation along an elevation gradient: Variation in Senecio subalpinus growing in the Tatra Mountains. Alp. Bot. 2021, 131, 117–124. [Google Scholar] [CrossRef]
  15. Milla, R.; Gimenez-Benavides, L.; Escudero, A.; Reich, P.B. Intra- and interspecific performance in growth and reproduction increase with altitude: A case study with two Saxifraga species from northern Spain. Funct. Ecol. 2009, 23, 111–118. [Google Scholar] [CrossRef]
  16. Ma, W.; Shi, P.; Li, W.; He, Y.; Zhang, X.; Shen, Z.; Chai, S. Changes in individual plant traits and biomass allocation in alpine meadow with elevation variation on the Qinghai-Tibetan Plateau. Sci. China Life Sci. 2010, 53, 1142–1151. [Google Scholar] [CrossRef]
  17. Poorter, H.; Niinemets, Ü.; Poorter, L.; Wright, I.J.; Villar, R. Causes and consequences of variation in leaf mass per area (LMA): A meta-analysis. New Phytol. 2009, 182, 565–588. [Google Scholar] [CrossRef]
  18. Gonzalez-Zurdo, P.; Escudero, A.; Babiano, J.; Garcia-Ciudad, A.; Mediavilla, S. Costs of leaf reinforcement in response to winter cold in evergreen species. Tree Physiol. 2016, 36, 273–286. [Google Scholar] [CrossRef]
  19. Díaz, S.; Hodgson, J.G.; Thompson, K.; Cabido, M.; Cornelissen, J.H.; Jalili, A.; Montserrat-Martí, G.; Grime, J.P.; Zarrinkamar, F.; Asri, Y.; et al. The plant traits that drive ecosystems: Evidence from three continents. J. Veg. Sci. 2004, 15, 295–304. [Google Scholar] [CrossRef]
  20. Tecco, P.A.; Díaz, S.; Cabido, M.; Urcelay, C. Functional traits of alien plants across contrasting climatic and land-use regimes: Do aliens join the locals or try harder than them? J. Ecol. 2010, 98, 17–27. [Google Scholar] [CrossRef]
  21. Johnston, F.M.; Pickering, C.M. Effect of altitude on resource allocation in the weed Achillea millefolium (yarrow, Asteraceae) in the Australian Alps. Aust. J. Bot. 2004, 52, 639–646. [Google Scholar] [CrossRef]
  22. Guo, H.; Weiner, J.; Mazer, S.J.; Zhao, Z.G.; Du, G.Z.; Li, B. Reproductive allometry in Pedicularis species changes with elevation. J. Ecol. 2012, 100, 452–458. [Google Scholar] [CrossRef]
  23. Kelly, C.A. Effects of variable life history and insect herbivores on reproduction in Solidago macrophylla (Asteraceae) on an elevational gradient. Am. Midl. Nat. 1998, 139, 243–254. [Google Scholar] [CrossRef]
  24. Kudo, G.; Molau, U. Variations in reproductive traits at inflorescence and flower levels of an arctic legume, Astragalus alpinus L.: Comparisons between a subalpine and an alpine population. Plant Species Biol. 1999, 14, 181–191. [Google Scholar] [CrossRef]
  25. Hautier, Y.; Randin, C.F.; Stöcklin, J.; Guisan, A. Changes in reproductive investment with altitude in an alpine plant. J. Plant Ecol. 2009, 2, 125–134. [Google Scholar] [CrossRef]
  26. Maad, J.; Armbruster, W.S.; Fenster, C.B. Floral size variation in Campanula rotundifolia (Campanulaceae) along altitudinal gradients: Patterns and possible selective mechanisms. Nor. J. Bot. 2013, 31, 361–371. [Google Scholar] [CrossRef]
  27. Bliss, L.C. Arctic and alpine plant life cycles. Annu. Rev. Ecol. Syst. 1971, 2, 405–438. [Google Scholar] [CrossRef]
  28. Weiner, J.; Campbell, L.G.; Pino, J.; Echarte, L. The allometry of reproduction within plant populations. J. Ecol. 2009, 97, 1220–1233. [Google Scholar] [CrossRef]
  29. Cingolani, A.M.; Posse, G.; Collantes, M.B. Plant functional traits, herbivore selectivity and response to sheep grazing in Patagonian steppe grasslands. J. Appl. Ecol. 2005, 42, 50–59. [Google Scholar] [CrossRef]
  30. Whitworth-Hulse, J.I.; Cingolani, A.M.; Zeballos, S.R.; Poca, M.; Gurvich, D.E. Does grazing induce intraspecific trait variation in plants from a sub-humid mountain ecosystem? Austral Ecol. 2016, 41, 745–755. [Google Scholar] [CrossRef]
  31. Wang, Z.; Zhang, J.; Li, Z.; Liu, H.; Wang, L.; Wang, W.; Wang, Y.; Liang, C. Single grazing is more detrimental to grasslands than mixed grazing: Evidence from the response of functional traits of dominant plants to grazing systems. Front. Ecol. Evol. 2021, 9, 682289. [Google Scholar] [CrossRef]
  32. Jiang, S.; Zhang, J.; Tang, Y.; Li, Z.; Liu, H.; Wang, L.; Wu, Y.; Liang, C. Plant functional traits and biodiversity can reveal the response of ecosystem functions to grazing. Sci. Total Environ. 2023, 899, 165636. [Google Scholar] [CrossRef] [PubMed]
  33. Briske, D.D. Strategies of plant survival in grazed systems: A functional interpretation. In The Ecology and Management of Grazing Systems; Hodgson, J., Illius, A.W., Eds.; CABI International: Wallingford, UK, 1996; pp. 37–67. [Google Scholar]
  34. Díaz, S.; Noy-Meir, I.; Cabido, M. Can grazing response of herbaceous plants be predicted from simple vegetative traits? J. Appl. Ecol. 2001, 38, 497–508. [Google Scholar] [CrossRef]
  35. Cayssials, V.; Rodríguez, C. The adaptive value of grass traits in response to grazing. J. Plant Ecol. 2018, 11, 248–255. [Google Scholar] [CrossRef]
  36. Hendrickson, J.; Olson, B. Understanding plant response to grazing. In Targeted Grazing: A Natural Approach to Vegetation Management and Landscape Enhancement; Launchbaugh, K., Walker, J.W., Eds.; American Sheep Industry Association: Englewood, CO, USA, 2006; pp. 32–39. [Google Scholar]
  37. Strauss, S.Y.; Agrawal, A.A. The ecology and evolution of plant tolerance to herbivory. Trends Ecol. Evol. 1999, 14, 179–185. [Google Scholar] [CrossRef]
  38. Pérez-Harguindeguy, N.; Diaz, S.; Vendramini, F.; Cornelissen, J.H.C.; Gurvich, D.E.; Cabido, M. Leaf traits and herbivore selection in the field and in cafeteria experiments. Austral Ecol. 2003, 28, 642–650. [Google Scholar] [CrossRef]
  39. Adler, P.; Raff, D.; Lauenroth, W. The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 2001, 128, 465–479. [Google Scholar] [CrossRef]
  40. Louault, F.; Pillar, V.D.; Aufrère, J.; Garnier, E.; Soussana, J.F. Plant traits and functional types in response to reduced disturbance in a semi-natural grassland. J. Veg. Sci. 2005, 16, 151–160. [Google Scholar] [CrossRef]
  41. Díaz, S.; Lavorel, S.; McIntyre, S.U.; Falczuk, V.; Casanoves, F.; Milchunas, D.G.; Skarpe, C.; Rusch, G.; Sternberg, M.; Noy-Meir, I.; et al. Plant trait responses to grazing—A global synthesis. Glob. Change Biol. 2007, 13, 313–341. [Google Scholar] [CrossRef]
  42. Hanley, M.E.; Lamont, B.B.; Fairbanks, M.M.; Rafferty, C.M. Plant structural traits and their role in anti-herbivore defence. Perspect. Plant Ecol. Evol. Syst. 2007, 8, 157–178. [Google Scholar] [CrossRef]
  43. Kostrakiewicz-Gierałt, K.; Kozak, M.; Kozłowska-Kozak, K. The impact of extensive sheep grazing on the population and individual traits of Trollius altissimus Crantz. Pol. J. Ecol. 2015, 63, 523–533. [Google Scholar] [CrossRef]
  44. Wentao, M.; Shiming, T.; Le, Q.; Weibo, R.; Fry, E.L.; De Long, J.R.; Margerison, R.C.; Yuan, C.; Xiaomin, L. Grazing reduces plant sexual reproduction but increases asexual reproduction: A global meta-analysis. Sci. Total Environ. 2023, 879, 162850. [Google Scholar] [CrossRef]
  45. Menges, E.S. Applications of population viability analyses in plant conservation. Ecol. Bull. 2000, 48, 73–84. [Google Scholar]
  46. Comitetul de Stat al Geologiei. Harta Geologică 1:200000, Foaia L-34-XXIV; Institutul Geologic: București, Romania, 1968. [Google Scholar]
  47. Fărcaș, I.; Scorocovschi, V. Clima Munților Retezat. In Parcul Național Retezat—Studii Ecologice; Popovici, I., Ed.; West Side Computers: Brașov, Romania, 1992; pp. 13–20. [Google Scholar]
  48. Diklić, N.; Lakušić, D. Barbarea vulgaris R. Br subsp. lepuznica (E.I. Nyárády) Soó. In The Red Data Book of Flora of Serbia I: Extinct and Critically Endangered Taxa; Stevanović, V., Ed.; Institute for Protection of Nature of the Republic of Serbia: Belgrade, Serbia, 1999; pp. 221–222. [Google Scholar]
  49. Dihoru, G.; Negrean, G. Cartea Roșie a Plantelor Vasculare din România; Editura Academiei Române: București, Romania, 2009. [Google Scholar]
  50. Bilz, M.; Kell, S.P.; Maxted, N.; Lansdown, R.V. European Red List of Vascular Plants; Publications Office of the European Union: Luxembourg, 2011. [Google Scholar]
  51. Nyárády, E.I. Adnotațiuni la Flora României, vol. IX. Bul. Grad. Bot. Muz. Bot. Cluj 1934, 14, 3–4. [Google Scholar]
  52. Ciocârlan, V. Flora Ilustrată a României: Pteridophyta et Spermatophyta; Editura Ceres: București, Romania, 2009. [Google Scholar]
  53. Sârbu, I.; Ștefan, N.; Oprea, A. Plante vasculare din Romania: Determinator Ilustrat de Teren; Editura Victor B Victor: București, Romania, 2013. [Google Scholar]
  54. Kliment, J.; Turis, P.; Janišová, M. Taxa of vascular plants endemic to the Carpathian Mts. Preslia 2016, 88, 19–76. [Google Scholar]
  55. Euro+Med PlantBase. 2025. Available online: https://europlusmed.org (accessed on 2 April 2025).
  56. EUNIS. 2025. Available online: https://eunis.eea.europa.eu/species/163785 (accessed on 2 April 2025).
  57. Díaz, S.; Kattge, J.; Cornelissen, J.H.C.; Wright, I.J.; Lavorel, S.; Dray, S.; Reu, B.; Kleyer, M.; Wirth, C.; Prentice, I.C.; et al. The global spectrum of plant form and function. Nature 2016, 529, 167–171. [Google Scholar] [CrossRef]
  58. Hikosaka, K.; Kurokawa, H.; Arai, T.; Takayanagi, S.; Tanaka, H.O.; Nagano, S.; Nakashizuka, T. Intraspecific variations in leaf traits, productivity and resource use efficiencies in the dominant species of subalpine evergreen coniferous and deciduous broadleaved forests along the altitudinal gradient. J. Ecol. 2021, 109, 1804–1818. [Google Scholar] [CrossRef]
  59. Martínková, J.; Hájek, T.; Adamec, L.; Klimešová, J. Growth, root respiration and photosynthesis of a root-sprouting short-lived herb after severe biomass removal. Flora 2021, 284, 151915. [Google Scholar] [CrossRef]
  60. Martínková, J.; Šmilauer, P.; Mihulka, S.; Latzel, V.; Klimešová, J. The effect of injury on whole-plant senescence: An experiment with two root-sprouting Barbarea species. Ann. Bot. 2016, 117, 667–679. [Google Scholar] [CrossRef]
  61. Samson, D.A.; Werk, K.S. Size-dependent effects in the analysis of reproductive effort in plants. Am. Nat. 1986, 127, 667–680. [Google Scholar] [CrossRef]
  62. Stoecklin, J.; Favre, P. Effects of plant size and morphological constraints on variation in reproductive components in two related species of Epilobium. J. Ecol. 1994, 82, 735–746. [Google Scholar] [CrossRef]
  63. Pluess, A.; Stoecklin, J. The importance of population origin and environment on clonal and sexual reproduction in the alpine plant Geum reptans. Funct. Ecol. 2005, 19, 228–237. [Google Scholar] [CrossRef]
  64. Aarssen, L.W.; Taylor, D.R. Fecundity allocation in herbaceous plants. Oikos 1992, 65, 225–232. [Google Scholar] [CrossRef]
  65. Laiolo, P.; Obeso, J.R. Life-history responses to the altitudinal gradient. In High Mountain Conservation in a Changing World; Catalan, J., Ninot, J.M., Aniz, M.M., Eds.; Springer: Cham, Switzerland, 2017; Volume 62, pp. 253–283. [Google Scholar]
  66. Dai, W.; Gao, R.; He, M.; Yang, Y.; Li, F.; Mu, J. Linkages among the functional traits, insect visitation rate and seed set of Gentiana taxa on the Tibetan Plateau. J. Mt. Sci. 2022, 19, 2312–2321. [Google Scholar] [CrossRef]
  67. Harper, J.L. Population Biology of Plants; Academic Press: London, UK, 1977. [Google Scholar]
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Figure 1. Geographic position of the study area within the Southern Carpathians (inset map) and location of the three studied populations of Barbarea vulgaris subsp. lepuznica in the Retezat Mountains.
Figure 1. Geographic position of the study area within the Southern Carpathians (inset map) and location of the three studied populations of Barbarea vulgaris subsp. lepuznica in the Retezat Mountains.
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Figure 2. Multiple comparisons of means of the leaf mass area (a), tallest shoot height (b) and raceme count (c) by population. Means not sharing any letter are significantly different at 5% alpha probability level.
Figure 2. Multiple comparisons of means of the leaf mass area (a), tallest shoot height (b) and raceme count (c) by population. Means not sharing any letter are significantly different at 5% alpha probability level.
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Figure 3. Relative contribution of plant traits to the predictive assignment of individuals to the three study populations via Bootstrap Forest (entropy R-square = 0.459; misclassification rate = 0.178).
Figure 3. Relative contribution of plant traits to the predictive assignment of individuals to the three study populations via Bootstrap Forest (entropy R-square = 0.459; misclassification rate = 0.178).
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Figure 4. Michaelis–Menten curve fitting of the number of racemes by the tallest shoot height in Populations 1 (a), 2 (b) and 3 (c). All regression coefficients are significantly different from zero at 5% alpha probability level.
Figure 4. Michaelis–Menten curve fitting of the number of racemes by the tallest shoot height in Populations 1 (a), 2 (b) and 3 (c). All regression coefficients are significantly different from zero at 5% alpha probability level.
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Table 1. Geo-topographic conditions and soil acidity associated with the sites corresponding to the three studied populations (P1—P3) of B. vulgaris subsp. lepuznica.
Table 1. Geo-topographic conditions and soil acidity associated with the sites corresponding to the three studied populations (P1—P3) of B. vulgaris subsp. lepuznica.
FeatureP1 SiteP2 SiteP3 Site
Latitude north (degrees)45.34471745.34071045.343711
Longitude east (degrees)22.90687322.92700622.923895
Mean elevation (m)170019002100
Mean slope (degrees)41925
Slope aspectSWSESE
Soil pH (at 5 cm depth)6.66.47.1
Sheep grazing intensityModerateVery lowAbsent
Table 2. Significance tests of the Leaf’, ‘Plant’ and ‘Population effects estimated via nested ANOVA on the leaf mass area (whole model R-square = 0.586).
Table 2. Significance tests of the Leaf’, ‘Plant’ and ‘Population effects estimated via nested ANOVA on the leaf mass area (whole model R-square = 0.586).
Fixed EffectF RatioProb > F
Population4.1510.0190
Random EffectsVariance ComponentWald p-Value
Plant [within Population]0.0298<0.0001
Leaf [within Population and Plant]0.0271<0.0001
Table 3. Significance tests of the ‘Plant and ‘Population effects estimated via nested ANOVA on the tallest shoot height (whole model R-square = 0.431).
Table 3. Significance tests of the ‘Plant and ‘Population effects estimated via nested ANOVA on the tallest shoot height (whole model R-square = 0.431).
Fixed EffectF RatioProb > F
Population32.964<0.0001
Random EffectVariance ComponentWald p-Value
Plant [within Population]0.0878<0.0001
Table 4. Significance tests of the ‘Plant and ‘Population effects estimated via nested ANOVA on the number of racemes per plant (whole model R-square = 0.034).
Table 4. Significance tests of the ‘Plant and ‘Population effects estimated via nested ANOVA on the number of racemes per plant (whole model R-square = 0.034).
Fixed EffectF RatioProb > F
Population1.5300.2223
Random EffectVariance ComponentWald p-Value
Plant [within Population]0.2267<0.0001
Table 5. Estimated raw and standardised coefficients (effect relative size) along with their significance tests corresponding to the multiple linear regression of the raceme count by the tallest shoot height and leaf mass area (LMA) in the three studied populations.
Table 5. Estimated raw and standardised coefficients (effect relative size) along with their significance tests corresponding to the multiple linear regression of the raceme count by the tallest shoot height and leaf mass area (LMA) in the three studied populations.
TermRaw EstimateStandardised Estimatet RatioProb > |t|R-Square
Population 1
Intercept3.23901.790.0851
LMA0.1410.0760.410.68390.081
Height−0.435−0.266−1.440.1626
Population 2
Intercept3.09900.740.4682
LMA0.3730.0890.450.65420.095
Height−0.611−0.263−1.330.1943
Population 3
Intercept6.71905.69<0.0001
LMA−0.668−0.352−2.420.02260.428
Height−0.519−0.534−3.660.0011
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Gafta, D.; Aczel, E.; Carpa, R.; Dănău, C.; Goia, I. Are There Resource Allocation Constraints to Floral Production in the Endangered Barbarea vulgaris subsp. lepuznica (Southern Carpathians, Romania)? Conservation 2025, 5, 56. https://doi.org/10.3390/conservation5040056

AMA Style

Gafta D, Aczel E, Carpa R, Dănău C, Goia I. Are There Resource Allocation Constraints to Floral Production in the Endangered Barbarea vulgaris subsp. lepuznica (Southern Carpathians, Romania)? Conservation. 2025; 5(4):56. https://doi.org/10.3390/conservation5040056

Chicago/Turabian Style

Gafta, Dan, Emilia Aczel, Rahela Carpa, Claudia Dănău, and Irina Goia. 2025. "Are There Resource Allocation Constraints to Floral Production in the Endangered Barbarea vulgaris subsp. lepuznica (Southern Carpathians, Romania)?" Conservation 5, no. 4: 56. https://doi.org/10.3390/conservation5040056

APA Style

Gafta, D., Aczel, E., Carpa, R., Dănău, C., & Goia, I. (2025). Are There Resource Allocation Constraints to Floral Production in the Endangered Barbarea vulgaris subsp. lepuznica (Southern Carpathians, Romania)? Conservation, 5(4), 56. https://doi.org/10.3390/conservation5040056

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