Community phylogenetic diversity drives flowering synchrony among coexisting plant species even under drought conditions

Abstract

Flowering time is a critical event in the lifetime of angiosperms, being particularly sensitive to environmental conditions, although the range of flowering response should be ultimately constrained by evolutionary history. We hypothesize that (1) phylogenetically diverse assemblages exhibit more segregated flowering peaks due to lineage-specific constraints, while closely related assemblages show synchronized flowering, and (2) under drought conditions, phenotypic plasticity most likely increase flowering overlap, though this response may depend on species’ phylogenetic relatedness in the assemblage. We designed assemblages with annual plants of semiarid systems of Spain, considering two contrasted levels of phylogenetic diversity (PD) and two water availability treatments in a common garden experiment, where we analysed the flowering segregation among species. High PD assemblages resulted in greater flowering overlap, while assemblages composed of close relatives segregated more their flowering peaks. Water stress triggered flowering synchronization both in high and low phylogenetic diversity assemblages. Our findings suggest that the high phylogenetic diversity characteristic of Iberian gypsophilous annual plant communities is compatible with substantial flowering overlap, which may, in turn, facilitate species coexistence and contribute to the remarkable species richness observed in these environmentally harsh habitats.

Introduction

Flowering time is a crucial event in the lifetime of angiosperms that has critical impacts on plant fitness. If flowering occurs too early in the growing season, late frosts could damage floral tissues, pollinators may not yet be abundant enough to ensure fertilization, or plant size may constrain total flower production. However, if flowering occurs too late, environmental conditions may not be favorable for seed maturation or dispersal or may leave the offspring in harsh conditions to survive^{1, 2–3}. Flowering time is determined by a trade-off between water availability⁴, temperature^5,6, photoperiod⁷, and the optimal moment of germination⁸. External environmental conditions are linked to a complex set of endogenous molecular pathways that trigger flowering time⁹. Closely related species are known to share similar gene regulatory pathways governing flowering¹⁰, and several studies have demonstrated that the genetic basis of flowering pathways is conserved—for instance, vernalization in Pooideae grasses¹¹, photoperiod pathway in perennial C4 grasses¹², indicating a phylogenetically conserved mechanism with species-specific variations. Consequently, closely related species are expected to respond similarly to environmental cues, whereas distantly related species may rely on different triggers to initiate flowering.

In arid and semiarid systems, where unpredictable droughts occur, soil water availability is known to be a critical driver of plant growth and plant community dynamics^{13, 14, 15, 16–17}. Low water availability has been linked to acceleration in flowering time, especially in annual plants^18,19, which has been interpreted as a drought escape response to complete phenology before the environment becomes too harsh for plant survival²⁰. Flowering time is associated with the period of maximum vegetative biomass^5,21,22, indicating high resource uptake. Indeed, several studies suggest that phenology can serve as a proxy for temporal resource use in plants^{23, 24–25}.

It is expected that species are more likely to coexist if their phenology is segregated because of a reduction of interspecific competition^26,27. Furthermore, phenological segregation has recently been demonstrated to be a plausible driver of community structure by enabling nitrogen transfer between plants in different phenological stages²⁵. In communities where coexisting species flower concurrently, species performance may benefit from overlapping flowering periods due to the attraction of a larger number and greater diversity of pollinators^{28, 29–30}. However, co-flowering species might also face increased competition for pollinators, potentially reducing the frequency of pollinator visits^{31, 32–33}, as well as competition for shared abiotic resources. Consequently, the aggregation versus segregation of flowering phenology can alter plant-plant interactions among coexisting species³⁴, ultimately influencing the species assembly process.

In the last two decades, community ecologists have focused their attention on phylogenetic patterns in order to unveil ecological processes underlying coexistence³⁵. Phylogenetic diversity (PD, hereinafter) measures the degree of evolutionary relatedness among species of a community (Faith, 1992). It provides a valuable measure of biodiversity because it integrates the evolutionary history of species with their ecological requirements^{36, 37, 38–39} and it can inform on the main ecological processes involved in the species assembly^35,40,41. Many authors have analyzed phylogenetic relatedness observed in local communities to infer ecological processes that can influence the community structure (i. e., phylogenetic response)^16,42,43. Phylogenetic convergence is usually related to habitat filtering processes³⁵ and to competitive exclusion processes when a phylogenetically conserved trait promoting survival is selected by environmental constraints⁴⁴. Phylogenetic overdispersion in assemblages (phylogenetic divergence) is usually associated with nurse-mediated facilitation⁴⁵, and competitive exclusion interactions between close relatives with the same niche-use^35,46. Phylogenetic divergence, however, also occurs when distantly related taxa converge on similar niche-use^{47, 48, 49–50}.

Integrating knowledge on how flowering time is influenced by community-level patterns, such as phylogenetic diversity, and how flowering time, in turn, affects species coexistence within the community, is crucial for understanding the assembly of plant communities and for predicting how they will respond to ongoing environmental change. From a community perspective, few studies have manipulated the phylogenetic diversity of experimental assemblages^51,52 and even fewer have done so to evaluate the causal effect of phylogenetic diversity of assemblages as driver of the assembly processes^53,54. We build on our previous study⁵³, that established that under drought conditions, phylogenetically diverse assemblages of Iberian gypsophilous annual plants resulted in higher plant survival and fitness than neighborhoods composed of closely related species, to explore potential mechanisms driven by plant phenology. The phylogenetic diversity of species assemblages appears to be a driving force in the assembly process, with niche complementarity among species being a central mechanism in community organization^35,53,55. However, a deeper understanding of the underlying mechanisms is necessary to enhance our predictions of how communities will respond to varying conditions.

In this study, we aimed to evaluate if differences in flowering time of coexisting species could be a key driver of niche complementarity in the communities of annual plants growing in gypsum soils. To pursue this aim, we monitored the flowering phenology of plants in a common garden experiment, where the initial phylogenetic diversity of species assemblages together with water availability were manipulated. We hypothesize that, both phylogenetic constraints and phenotypic plasticity influence flowering phenology; however, their relative importance varies with the phylogenetic diversity of the species assemblage and prevailing drought conditions. Specifically, we expect that (1) in phylogenetically diverse assemblages, lineage-specific constraints will lead to more segregated flowering peaks, whereas in closely related assemblages, flowering schedules will be more synchronized and (2) under drought conditions, we anticipate a shift toward increased flowering overlap driven by phenotypic plasticity; specifically, we hypothesize that this response may be modulated by the phylogenetic relatedness among coexisting species within the assemblage.

Materials and methods

The target annual plant community of this study grows on gypsum soils in the Tagus valley, central Spain. The climate in the area is semiarid Mediterranean with mean annual temperatures around 14.5 °C and mean annual precipitation of 400 mm, especially distributed in the late autumn and early spring (Aranjuez weather station, 40° 4′ 2′′ N; 3° 32′ 46′′ W, 540 m). The habitat comprises a gypsum steppe, where gypsophilous dwarf shrubs (e.g., Lepidium subulatum L. -Brassicaceae-, Centaurea hyssopifolia Vahl -Asteraceae-, Gypsophila struthium L. -Caryophyllaceae-, Helianthemum squamatum (L.) Dum. Cours. -Cistaceae-, Thymus lacaitae Pau -Lamiaceae-, Herniaria fruticosa L. -Caryophyllaceae-, and Frankenia thymifolia Desf.) -Frankeniaceae- are patchily scattered along with Macrochloa tenacissima (L.) Kunth -Poaceae-grass tussocks on a matrix of bare soil with a well-developed biological crust dominated by lichens (e.g., Diploschistes diacapsis (Ach.) Lumbsch, Squamarina lentigera (G.H. Weber) Poelt, Fulgensia subbracteata (Nyl.) Poelt, and Psora decipiens (Hedw.) Hoffm). From October to July a seasonally dynamic, rich community of annual plants proliferates. They remain in seed form the rest of the year by accumulating dense and well-structured seed banks in the soil^{56, 57–58}. The regional species pool is composed of nearly 120 species⁵⁹ with up to 38 plant species/0.25 m² in rainy years^15,60. Relevant examples are Campanula fastigiata Dufour ex A. DC. – Campanulaceae-, Chaenorhinum reyesii (C. Vicioso & Pau) Benedí – Plantaginaceae-, Asterolinon linum-stellatum (L.) Duby in DC. – Primulaceae-, Campanula erinus L. – Campanulaceae-, Galium parisiense L. -Rubiaceae-, Helianthemum salicifolium (L.) Miller. -Cistaceae-, Micropyrum tenellum (L.) Link -Poaceae-, Bromus rubens L. -Poaceae-, Lomelosia stellata (L.) Raf. -Caprifoliaceae- and Pistorinia hispanica (L.) DC. -Crassulaceae.

We used data collected from the experiment described in⁵³ in which we manipulated the initial phylogenetic diversity of experimental assemblages in a common garden approach in the greenhouse. We aimed to evaluate the causal effect of phylogenetic diversity on flowering phenology of annual plant assemblages. This approach has rarely been attempted with vascular plants (but see 51, 52). To determine the initial levels of phylogenetic diversity of each assemblage, we prepared a phylogenetic tree (see 53) using phylo.maker function of “V.Phylomaker” package⁶¹, and to calculate indices we used the packages “ape”⁶² and “picante”⁶³ in software R (http://www.R-project.org). We calculated the phylogenetic species variability (PSV) index⁶⁴ and the standardized effect size of mean pairwise distances in communities index (SES.MPD). The PSV index, bounded between 0 and 1, indicates the degree of relatedness among different species in a community. Values close to zero imply very low PD, while values close to one represent maximum PD. The SES.MPD index measures the mean phylogenetic distance between pairs of species and contrasts it to 1000 null species assemblages from the phylogenetic community tree. High positive values imply larger mean phylogenetic distance than the null model, thus phylogenetic diversity, while high negative values indicate lower mean phylogenetic distance than the null model, thus phylogenetic convergence.

To create species assemblages, during the springs of 2016 and 2017, we collected seeds from more than 40 random individuals of each annual plant species that naturally co-occur in open areas in the field in two nearby locations (Aranjuez (40° 02′ 11.7″ N, 3° 32′ 59.5″ W; 591 m) and Ciempozuelos (40° 08′ 36.9″ N, 3° 37′ 00.0″ W; 585 m), which can be considered part of the same genetic species pool. Seeds were cleaned and stored in paper envelopes in dry conditions. Prior to sowing, seeds were placed in an oven at 50 °C for fifteen days in order to simulate summer conditions and break seed dormancy⁵³. Annual plant communities from Mediterranean gypsum soils provide a useful model system to conduct manipulative experiments to determine mechanisms involved in the assembly of communities, because they comprise a rich regional species pool (over 120 taxa) of ephemeral, small-sized species, with short and highly synchronized life cycles (October-early June), which overall allow to perform, handle, and complete common garden experiments in small spaces and short time lapses (see^{14,15,17,53,58, 59–60}. Experimental assemblages were formed by four combinations of seven different species (Fig. 1, Appendix 1): two combinations with low PD and two with high PD. Two taxonomic scenarios with high phylogenetic diversity were composed of Poaceae, Crassulaceae, Apiaceae and Caryophylaceae families (PSV = 0.82 and 0.85; SES.MPD = 0.53 and 0.17) and two taxonomic scenarios with low PD, one composed of Asteraceae species (PSV = 0.24; SES.MPD =  − 9.6; p < 0.001) and another one made up of Brassicales and Malvales (PSV = 0.64; SES.MPD =  − 2.5; p < 0.05). Replication of taxonomic scenarios allows to control for the effects of taxonomic identity.

[See PDF for image]

Fig. 1

(A) Schematic representation of the implemented phylogenetic diversity (PD) scenarios: Two levels of phylogenetic diversity—high and low—were established, each encompassing two distinct taxonomic compositions (see Appendix 1 for details). Both average and drought watering treatments were applied across these scenarios. Each treatment was replicated more than twelve times, resulting in a total of 110 experimental pots (see Appendix 2 for details). (B) Study site and experimental setup: Seeds used in the experiment were collected from gypsum ecosystems located in two nearby sites within the Tagus Valley, southeastern Madrid (Spain). The experimental setup was conducted in a greenhouse at Rey Juan Carlos University. Each pot (30 cm diameter) contained a community of seven annual species, with ten individuals per species. C) Expected trends in flowering phenology: Anticipated patterns in flowering phenology were proposed for both high and low PD scenarios, in combination with the average and drought irrigation treatments.

Two irrigation treatments were applied, differing in the amount of water applied. We calculated the average monthly precipitation recorded between 1981 and 2010 in the area of our study system (Getafe weather station, 40° 18.0′ N, 3° 43.2′ W, 620 masl) and we applied it to pots manually, distributing the corresponding amount twice a week, being this the average irrigation treatment. To simulate an intense drought, the amount of water applied per irrigation event in the Drought treatment was reduced to 33% of that used in the Average treatment, while maintaining the same watering frequency. We established a fully crossed factorial design with two phylogenetic diversity levels × two taxonomic combinations of species × two water availability treatments (eight experimental scenarios). Each experimental scenario was replicated in 10 to 16 units, thereby resulting in 110 experimental assemblages (pots) (Appendix 2).

The experiment was set up in October 2017, thus synchronized with the natural life cycle of annual plants, at the Rey Juan Carlos University greenhouse (https://urjc-cultive.webnode.es; Móstoles, Madrid, Spain: 40° 20′ 2′′ N, 3° 52′ 00′′ W, 650 masl). We filled round plastic pots with a diameter of 30 cm and depth of 10 cm with 5 kg of seed-free gypsum soil from a gypsum quarry near the natural habitat of the study species. This substrate originates from the deeper layers of the quarry, which ensures the absence of viable seeds. Seventy seeds per species were sown in each pot and excess seedlings were removed until we obtained 10 established individuals per each of the seven species per pot. Plants persisted as seedlings during all winter, as naturally occurs in the field, and in February, the experimental irrigation and periodic monitoring of plants started. Between February and June (the natural growing season for annual plants in gypsum systems;^15,60). We monitored the number of flowering plants per species and pot weekly. Flowering range was defined as the number of days between the date on which the first flower opened and the date on which the last flower opened for each species and pot. Flowering intensity was quantified as the number of flowering individuals per species and pot recorded at each sampling time. We calculated the time of flowering peak for each species in each pot by assigning the ordinal number of the week in which we censed the highest number of flowering plants of that species in that pot.

We evaluated the floral phenology at the community level based on the flowering segregation index per pot. Each pot was characterized by a single value of the flowering segregation index. This index consists of the mean pairwise distances of the flowering peaks between every species in each pot (measured in number of days). Flowering segregation informs on the degree of flowering overlap among species in each species assemblage⁶⁵. High values of segregation imply large temporal differences in flowering peaks among co-occurring species in each pot and low values imply synchronized or aggregated flowering peaks among coexisting species.

Statistical analyses

We performed a nested linear model to analyze whether the flowering segregation index (dependent variable), was influenced by the experimentally manipulated initial phylogenetic diversity (two levels, high and low PD), taxonomic composition (two taxonomic compositions per level of PD) and water irrigation (two levels, Average and Drought treatments) (explanatory variables). The variable taxonomic composition was nested within the phylogenetic diversity treatment to control differences associated with species identities. Specifically, we followed the recommendations of⁶⁶, which suggest that a factor should only be considered random if it includes at least five levels to ensure representativeness. Since our design included only two levels of taxonomic composition per treatment, we considered it more appropriate to treat this factor as fixed. We used the lm function in the “stats” package in R (4.0.3 version)⁶⁷.

Differences in the number of surviving plants in the drought treatments could affect the flowering segregation index. Thus, in order to statistically control for the differences in the number of surviving individuals, we conducted a bootstrap procedure to standardize the number of species used to calculate this index in each pot. Specifically, we randomly selected four of the coexisting species since most pots had at least four species during the flowering peak even in drought conditions (n = 107) and bootstrapped 100 times to calculate the average value for the flowering segregation index for each specific pot. The average value obtained by this bootstrap procedure was analyzed with the same nested linear model explained above.

Results

In high phylogenetic diversity experimental scenarios, the peak flowering time averaged among coexisting species occurred at 8.9 weeks (± 0.18 SE) under average water availability and at 7.6 weeks (± 0.22 SE) under drought conditions. In low PD scenarios, the peak flowering time was observed at 7.7 weeks (± 0.3 SE) with average water availability and at 5.95 weeks (± 0.29 SE) under drought conditions (Fig. 2; Appendix 3). Overall, drought conditions accelerated the flowering time in high and low phylogenetic diversity experimental scenarios. The initial phylogenetic diversity of species assemblages significantly influenced flowering segregation in pots, irrespective of irrigation treatment (Table 1, Fig. 3). Specifically, flowering phenology was more segregated in assemblages with low phylogenetic diversity compared to those with high phylogenetic diversity. Conversely, assemblages composed of phylogenetically distant species tended to have overlapping flowering peaks. Additionally, drought treatment increased flowering overlap, regardless of the initial phylogenetic diversity of the assemblage. Similar results were obtained when the number of species per pot was standardized using the bootstrap procedure. In this case, we found that the initial phylogenetic diversity was significant 100% of the time, irrigation was significant 95% of the time, and the interaction between them was not significant 92% of the time.

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Fig. 2

Average flowering phenology by species and treatment. Each line represents the average flowering density of a single species. Similar colors indicate closely related species. High PD refers to scenarios with initially high phylogenetic diversity (taxonomic compositions A and C), while Low PD corresponds to scenarios with initially low phylogenetic diversity (taxonomic compositions E and F).

Table 1. Linear models (LMs) for the analyses of flowering segregation among coexisting species per pot.

	df	Sum sq	F value
Phylogenetic diversity (PD)	1	41.9	137.5***
Irrigation (I)	1	14.8	48.7***
PD × Taxonomic composition (TC)	2	63.4	103.9***
PD × I	1	1.1	3.6
PD × TC × I	2	5.6	9.2***
Residuals	102	31.1

Taxonomic composition (TC) nested within phylogenetic diversity (PD), irrigation treatment (I) and their interaction were included as fixed factors. Note that each level of taxonomic composition is specific to a given phylogenetic diversity treatment, with no overlap across treatments (see Appendix 1). This nested structure precludes the estimation of a main effect for taxonomic composition, as its levels are not comparable across the different levels of phylogenetic diversity. Sum of squares and F values are presented. df: degrees of freedom. *: p < 0.05; **: p < 0.01; ***: p < 0.001.

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Fig. 3

Mean flowering segregation (weeks) in high vs. low phylogenetic diversity (PD) of the plant neighborhood under two irrigation treatments (average vs. drought). Vertical bars represent standard errors.

Discussion

Contrary to our expectations, this study found that flowering was more temporally overlapped in phylogenetically more diverse assemblages than in less diverse ones. This finding is particularly noteworthy for two reasons: (1) We anticipated that flowering would be more temporally segregated in phylogenetically diverse assemblages and more synchronized in those composed of closely related species, given the phylogenetic conservatism of flowering phenology^{68, 69, 70–71}; (2) Flowering segregation among coexisting species is often considered a proxy for temporal segregation in soil resource uptake^{23, 24–25}. Based on the findings of⁵³, who used the same experimental setup and demonstrated that assemblages with higher phylogenetic diversity were structured by niche complementarity, we would have expected these assemblages to also exhibit greater flowering segregation, reflecting temporal segregation of resource use. Instead, the community assembly is more likely driven by differences in other functional strategies and mechanisms rather than flowering time. Phylogenetically distant species may exhibit differences in functional traits related, for instance, to water use efficiency, photosynthetic efficiency, or resistance to desiccation^35,37,50. In our experimental setup, species with contrasting strategies to withstand water restriction successfully coexisted in phylogenetically diverse assemblages (e.g., the water accumulator Pistorinia hispanica, Crassulaceae, and the almost leafless Echinaria capitata, Poaceae) (Appendix 1). Therefore, species in phylogenetically diverse assemblages may attenuate interspecific competition by means of differences in functional traits, allowing them to allocate resources to flower production during the optimal period (in terms of temperature, soil moisture, photoperiod, etc.;⁹, that resulted in the overlap of species flowering peaks and presumably of their maximum development and resource uptake periods⁵.

Remarkably, even under severe drought conditions, temporal flowering synchronization was greater in high phylogenetic diversity assemblages, which nevertheless showed higher reproductive success than low phylogenetic diversity ones (see fitness data in⁵³). This finding aligns with⁷², who observed that flowering time acceleration did not penalize reproductive performance. Unexpectedly, temporal flowering segregation was observed in assemblages of closely related species. Flowering segregation has been extensively studied in coflowering species that share pollinators^{28,73, 74–75}, potentially explaining the coexistence of shrub species within the same genus due to reduced deposition of heterospecific pollen⁶⁵. We propose two non-mutually exclusive mechanisms to account for these findings in the experimental species assemblages: (1) Flowering segregation among closely related species may have evolved over several plant generations as a mechanism to reduce competition for shared pollinators, and it is possible that our experimental setup is capturing evidence of this adaptive response. The predominantly insect-pollinated nature of our study species supports the plausibility of such a mechanism operating within our system. Nevertheless, a longer-term longitudinal study would be necessary to substantiate this hypothesis. (2) Flowering segregation among coexisting, phylogenetically related species may result from ecological processes driven by plant–plant interactions. Specifically, closely related species are expected to experience more intense competition for resources, which could lead to a sequential pattern in the timing of full plant development—and consequently, flowering—based on their relative capacities for resource acquisition. This dynamic may give rise to the hierarchical flowering pattern observed in our experiment, reflecting flowering segregation. Shifts in flowering time are a well-documented evolutionary strategy that plants adopt to maximize reproductive success under stressful conditions^76,77. Furthermore, Montesinos-Navarro²⁵ demonstrated that phenologically dissimilar species are more likely to coexist due to enhanced nitrogen uptake and reduced nitrogen losses through leaching. Taken together, our results suggest that selective pressure for high plasticity in flowering phenology is particularly important in gypsum annual plant communities in semiarid ecosystems.

In conclusion, this study evidences that when coexisting species undergo niche segregation mediated by non-phenological traits, their flowering periods can overlap, enabling them to flower at the time of optimal environmental conditions. This observation aligns with the significant overlap in flowering times reported in other Mediterranean dry grasslands⁷⁵. Conversely, when coexisting related species compete for resources, temporal segregation of flowering times may emerge as an adaptive strategy to mitigate stressful conditions. Moreover, the significant plasticity in flowering time observed in our target community suggests that it may adapt more successfully to future climate change, which will be particularly severe in the Iberian gypsum drylands, compared to systems with lower levels of phenotypic plasticity⁵, provided that environmental conditions remain within certain thresholds that permit this response.

Acknowledgements

We thank Carlos Díaz and José Margalet for experiment assistance. Roberto López Rubio for his help with the experimental setup. We thank the Spanish Meteorological Agency (AEMET) for providing climatic data and Yesos Ibéricos-Algiss for providing gypsum soil. Financial support was provided by the PHYLOFUNKEY project (PID2023-149999NB-I00—Spanish Government) and NITOFLOW project (CNS2023-144743, Consolidacion investigadora, Ministerio de Ciencia, Innovación y Universidades – Spanish Government).

Author contributions

ALL conceived the idea; ALL, RC and PF collected seeds for the experimental set-up; ALL and RC designed methodology; RC collected the data; AMN and RC analysed the data; ALL led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Data availability

Dryad. https://doi.org/10.5061/dryad.98sf7m0tq Data could be also provided by Arantzazu L. Luzuriaga (corresponding author): [email protected].

Declarations

Competing interests

The authors declare no competing interests.

Ethical statement

Authors assure that legislation on seed collection has been accomplished. Permission obtained from responsible authority to collect seeds.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

1. Bernal, M; Estiarte, M; Peñuelas, J. Drought advances spring growth phenology of the Mediterranean shrub Erica multiflora. Plant Biol.; 2011; 13, pp. 252-257.1:STN:280:DC%2BC3M7otlyisw%3D%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21309971]

2. Montesinos-Navarro, A; Wig, J; Xavier Pico, F; Tonsor, SJ. Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytol.; 2011; 189, pp. 282-294. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20880224]

3. Bucher, SF; Römermann, C. Flowering patterns change along elevational gradients and relate to life-history strategies in 29 herbaceous species. Alp. Bot.; 2020; 130, pp. 41-58.

4. Shavrukov, Y; Kurishbayev, A; Jatayev, S; Shvidchenko, V; Zotova, L; Koekemoer, F; de Groot, S; Soole, K; Langridge, P. Early flowering as a drought escape mechanism in plants: How can it aid wheat production?. Front. Plant Sci.; 2017; 8, 1950. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29204147][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5698779]

5. Cleland, EE; Chiariello, NR; Loarie, SR; Mooney, HA; Field, CB. Diverse responses of phenology to global changes in a grassland ecosystem. Proc. Natl. Acad. Sci.; 2006; 103, pp. 13740-13744.2006PNAS.10313740C1:CAS:528:DC%2BD28XpvFSmtbw%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16954189][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1560087]

6. Jagadish, SVK; Bahuguna, RN; Djanaguiraman, M; Gamuyao, R; Prasad, PVV; Craufurd, PQ. Implications of high temperature and elevated CO₂ on flowering time in plants. Front. Plant Sci.; 2016; 7, 913. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27446143][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4921480]

7. Johansson, M; Staiger, D. Time to flower: Interplay between photoperiod and the circadian clock. J. Exp. Bot.; 2014; 66, pp. 719-730. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25371508]

8. Rathcke, B; Lacey, EP. Phenological patterns of terrestrial plants. Annu. Rev. Ecol. Syst.; 1985; 16, pp. 179-214.

9. Lee, Z; Kim, S; Choi, SJ; Joung, E; Kwon, M; Park, HJ; Shim, JS. Regulation of flowering time by environmental factors in plants. Plants; 2023; 12, 3680.1:CAS:528:DC%2BB3sXitlymsbnN [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37960036][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10649094]

10. Wang, R; Farrona, S; Vincent, C et al. PEP1 regulates perennial flowering in Arabis alpina. Nature; 2009; 459, pp. 423-427.2009Natur.459.423W1:CAS:528:DC%2BD1MXksFemu78%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19369938][DOI: https://dx.doi.org/10.1038/nature07988]

11. McKeown, M; Schubert, M; Marcussen, T; Fjellheim, S; Preston, JC. Evidence for an early origin of vernalization responsiveness in temperate pooideae grasses. Plant Physiol.; 2016; 172, pp. 416-426.1:CAS:528:DC%2BC28XitVWjsrjO [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27474116][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5074605][DOI: https://dx.doi.org/10.1104/pp.16.01023]

12. Nuñez, FDB; Yamada, T. Molecular regulation of flowering time in grasses. Agronomy; 2017; 7, 17.1:CAS:528:DC%2BC1cXhsFaltbfO [DOI: https://dx.doi.org/10.3390/agronomy7010017]

13. Peñuelas, J; Filella, I; Zhang, X; Llorens, L; Ogaya, R; Lloret, F; Comas, P; Estiarte, M; Terradas, J. Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol.; 2004; 161, pp. 837-846. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33873715]

14. Peralta, AM; Sánchez, AM; Luzuriaga, AL; de Bello, F; Escudero, A. Evidence of functional species sorting by rainfall and biotic interactions: A community monolith experimental approach. J. Ecol.; 2019; 107, pp. 2772-2788.1:CAS:528:DC%2BC1MXhvFOis7%2FK

15. Luzuriaga, AL; Sánchez, AM; Maestre, FT; Escudero, A. Assemblage of a semi-arid annual plant community: Abiotic and biotic filters act hierarchically. PLoS ONE; 2012; 7, pp. 1-9.

16. Luzuriaga, AL; Ferrandis, P; Flores, J; Escudero, A. Effect of aridity on species assembly in gypsum drylands: A response mediated by the soil affinity of species. AoB Plants; 2020; 12, pp. 1-8.

17. Sánchez, AM; Peralta, AM; Luzuriaga, AL; Prieto, M; Escudero, A. Climate change and biocrust disturbance synergistically decreased taxonomic, functional and phylogenetic diversity in annual communities on gypsiferous soils. Oikos; 2022; 3, e08809.

18. Fitter, AH; Fitter, RSR. Rapid changes in flowering time in British plants. Science; 2002; 296, pp. 1689-1691.2002Sci..296.1689F1:CAS:528:DC%2BD38XktlCgsrs%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12040195]

19. Kigel, J; Konsens, I; Rosen, N; Rotem, G; Kon, A; Fragman-Sapir, O. Relationships between flowering time and rainfall gradients across Mediterranean-desert transects. Isr. J. Ecol. Evol.; 2011; 57, pp. 91-109.

20. Franks, SJ. Plasticity and evolution in drought avoidance and escape in the annual plant Brassica rapa. New Phytol.; 2011; 190, pp. 249-257. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21210818]

21. Mooney, HA; Hobbs, RJ; Gorham, J; Williams, K. Biomass accumulation and resource utilization in co-occurring grassland annuals. Oecologia; 1986; 70, pp. 555-558.1986Oecol.70.555M1:STN:280:DC%2BC1czotVSjtQ%3D%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28311498]

22. Sun, S; Frelich, LE. Flowering phenology and height growth pattern are associated with maximum plant height, relative growth rate and stem tissue mass density in herbaceous grassland species. J. Ecol.; 2011; 99, pp. 991-1000.

23. Davis, CC; Willis, CG; Primack, RB; Miller-Rushing, AJ. The importance of phylogeny to the study of phenological response to global climate change. Philos. Trans. Roy. Soc. B Biol. Sci.; 2010; 365, pp. 3201-3213.

24. Craine, JM; Wolkovich, EM; Gene Towne, E; Kembel, SW. Flowering phenology as a functional trait in a tallgrass prairie. New Phytol.; 2012; 193, pp. 673-682. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22074383]

25. Montesinos-Navarro, A. Nitrogen transfer between plant species with different temporal N-demand. Ecol. Lett.; 2023; 26, pp. 1676-1686.1:STN:280:DC%2BB2szovFaktQ%3D%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37340907]

26. Chase, J; Laibold, M. Ecological Niches: Linking Classical and Contemporary Approaches; 2003; University of Chicago Press:

27. Chesson, P; Gebauer, RL; Schwinning, S; Huntly, N; Wiegand, K; Ernest, MS; Weltzin, JF. Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia; 2004; 14, pp. 236-253.2004Oecol.141.236C

28. Moeller, DA. Facilitative interactions among plants via shared pollinators. Ecology; 2004; 85, pp. 3289-3301.

29. Ricketts, TH; Regetz, J; Steffan-Dewenter, I; Cunningham, SA; Kremen, C; Bogdanski, A; Gemmill-Herren, B; Greenleaf, SS; Klein, AM; Mayfield, MM; Morandin, LA; Ochieng, A; Viana, BF. Landscape effects on crop pollination services: Are there general patterns?. Ecol. Lett.; 2008; 11, pp. 499-515. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18294214]

30. Lázaro, A; Lundgren, R; Totland, Ø. Co-flowering neighbors influence the diversity and identity of pollinator groups visiting plant species. Oikos; 2009; 118, pp. 691-702.2009Oikos.118.691L

31. Elzinga, JA; Atlan, A; Biere, A; Gigord, L; Weis, AE; Bernasconi, G. Time after time: Flowering phenology and biotic interactions. Trends Ecol. Evol.; 2007; 22, pp. 432-439. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17573151]

32. Mitchell, RJ; Flanagan, RJ; Brown, BJ; Waser, NM; Karron, JD. New frontiers in competition for pollination. Ann. Bot.; 2009; 103, pp. 1403-1413. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19304814][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2701753]

33. Pauw, A. Can pollination niches facilitate plant coexistence?. Trends Ecol. Evol.; 2013; 28, pp. 30-37. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22951227]

34. Strauss, SY; Truszczinski, AM; Anacker, BL. Do habitat shifts alter flowering phenology overlap in close relatives? Implications for local coexistence. Madroño; 2021; 68, pp. 406-415.

35. Webb, CO; Ackerly, DD; McPeek, MA; Donoghue, MJ. Phylogenies and community ecology. Annu. Rev. Ecol. Syst.; 2002; 33, pp. 475-505.

36. Ackerly, DD. Community assembly, niche conservatism, and adaptive evolution in changing environments. Int. J. Plant Sci.; 2003; 164, pp. 165-184.

37. Cavender-Bares, J; Kozak, KH; Fine, PV; Kembel, SW. The merging of community ecology and phylogenetic biology. Ecol. Lett.; 2009; 12, pp. 693-715. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19473217]

38. Srivastava, DS; Cadotte, MW; MacDonald, AAM; Marushia, RG; Mirotchnick, N. Phylogenetic diversity and the functioning of ecosystems. Ecol. Lett.; 2012; 15, pp. 637-648. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22583836]

39. Gerhold, P; Cahill, JF, Jr; Winter, M; Bartish, IV; Prinzing, A. Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). Funct. Ecol.; 2015; 29, pp. 600-614.

40. Emerson, BC; Gillespie, RG. Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol. Evol.; 2008; 23, pp. 619-630. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18823678]

41. Lemos-Costa, P; Miller, ZR; Allesina, S. Phylogeny structures species’ interactions in experimental ecological communities. Ecol. Lett.; 2024; 27, [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/39152685]e14490.

42. Godoy, O; Kraft, NJ; Levine, JM. Phylogenetic relatedness and the determinants of competitive outcomes. Ecol. Lett.; 2014; 17, pp. 836-844. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24766326]

43. López-Angulo, J; Swenson, NG; Cavieres, LA; Escudero, A. Interactions between abiotic gradients determine functional and phylogenetic diversity patterns in Mediterranean-type climate mountains in the Andes. J. Veg. Sci.; 2018; 29, pp. 245-254.

44. Mayfield, MM; Levine, JM. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol. Lett.; 2010; 13, pp. 1085-1093. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20576030]

45. Valiente-Banuet, A; Verdú, M. Facilitation can increase the phylogenetic diversity of plant communities. Ecol. Lett.; 2007; 10, pp. 1029-1036. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17714492]

46. Slingsby, JA; Verboom, GA. Phylogenetic relatedness limits co-occurrence at fine spatial scales: Evidence from the schoenoid sedges (Cyperaceae: Schoeneae) of the Cape Floristic Region, South Africa. Am. Naturalist; 2006; 168, pp. 14-27.

47. Cavender-Bares, J; Ackerly, DD; Baum, DA; Bazzaz, FA. Phylogenetic overdispersion in Floridian oak communities. Am. Nat.; 2004; 163, pp. 823-843.1:STN:280:DC%2BD2czmtFOnsQ%3D%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15266381]

48. Kembel, SW; Hubbell, SP. The phylogenetic structure of a neotropical forest tree community. Ecology; 2006; 87, pp. S86-S99. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16922305]

49. Swenson, NG; Enquist, BJ; Pither, J; Thompson, J; Zimmerman, JK. The problem and promise of scale dependency in community phylogenetics. Ecology; 2006; 87, pp. 2418-2424. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17089650]

50. Kraft, NJB; Cornwell, WK; Webb, CO; Ackerly, D. Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am. Nat.; 2007; 170, pp. 271-283. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17874377]

51. Feng, Y; Fouqueray, TD; van Kleunen, M. Linking Darwin’s naturalisation hypothesis and Elton’s diversity–invasibility hypothesis in experimental grassland communities. J. Ecol.; 2019; 107, pp. 794-805.

52. Galland, T; Adeux, G; Dvořáková, H et al. Colonization resistance and establishment success along gradients of functional and phylogenetic diversity in experimental plant communities. J. Ecol.; 2019; 107, pp. 2090-2104.

53. Chaves, R; Ferrandis, P; Escudero, A; Luzuriaga, AL. Diverse phylogenetic neighborhoods enhance community resistance to drought in experimental assemblages. Sci. Rep.; 2021; 11, pp. 1-12.

54. Ortiz, L; Luzuriaga, AL; Ferrandis, P. Functional diversity of experimental annual plant assemblages drives plant responses to biological soil crusts in gypsum systems. Funct. Ecol.; 2023; 37, pp. 488-503.1:CAS:528:DC%2BB38XjtVWntLbI

55. Pausas, JG; Verdú, M. The jungle of methods for evaluating phenotypic and phylogenetic structure of communities. Bioscience; 2010; 60, pp. 614-625.

56. Caballero, I; Olano, JM; Escudero, A; Loidi, J. Seed bank spatial structure in semi-arid environments: Beyond the patch-bare area dichotomy. Plant Ecol.; 2008; 195, pp. 215-223.

57. Martínez-Duro, E; Luzuriaga, AL; Ferrandis, P; Escudero, A; Herranz, JM. Does aboveground vegetation composition resemble soil seed bank during succession in specialized vegetation on gypsum soil?. Ecol. Res.; 2012; 27, pp. 43-51.

58. Peralta, AML; Sánchez, AM; Luzuriaga, AL; Escudero, A. Factors driving species assemblage in Mediterranean soil seed banks: From the large to the fine scale. Ann. Bot.; 2016; 117, pp. 1221-1228. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27085181][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4904168]

59. Luzuriaga, AL; Sánchez, AM; López-Angulo, J; Escudero, A. Habitat fragmentation determines diversity of annual plant communities at landscape and fine spatial scales. Basic Appl. Ecol.; 2018; 29, pp. 12-19.

60. Luzuriaga, AL; González, JM; Escudero, A. Annual plant community assembly in edaphically heterogeneous environments. J. Veg. Sci.; 2015; 26, pp. 866-875.

61. Jin, Y; Qian, HV. PhyloMaker: An R package that can generate very large phylogenies for vascular plants. Ecography; 2019; 42, pp. 1353-1359.2019Ecogr.42.1353J

62. Paradis, E; Schliep, K. ape 50: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics; 2018; 35, pp. 526-528.

63. Kembel, SW; Cowan, PD; Helmus, MR; Cornwell, WK; Morlon, H; Ackerly, DD; Blomber, SP; Webb, CO. Picante: R tools for integrating phylogenies and ecology. Bioinformatics; 2010; 26, pp. 1463-1464.1:CAS:528:DC%2BC3cXmsVGnsbw%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20395285]

64. Helmus, MR; Bland, TJ; Williams, CK; Ives, AR. Phylogenetic measures of biodiversity. Am. Nat.; 2007; 169, pp. 68-83.

65. de Avila Jr, RS; Pinheiro, M. Flowering segregation and pollinator distinctiveness contribute to coexistence in an extremely generalist plant group. Plant Ecol. Divers; 2021; 14, pp. 245-253.

66. Zuur, AF; Ieno, EN; Meesters, EH. A Beginner’s Guide to R; 2009; Springer:

67. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/ (2020).

68. Swenson, NG; Enquist, BJ. Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation. Am. J. Bot.; 2007; 94, pp. 451-459. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21636415]

69. Willis, CG; Ruhfel, B; Primack, RB; Miller-Rushing, AJ; Davis, CC. Phylogenetic patterns of species loss in Thoreau’s woods are driven by climate change. Proc. Natl. Acad. Sci.; 2008; 105, pp. 17029-17033.2008PNAS.10517029W1:CAS:528:DC%2BD1cXhtlKmu7fL [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18955707][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2573948]

70. Kraft, NJ; Ackerly, DD. Functional trait and phylogenetic tests of community assembly across spatial scales in an Amazonian forest. Ecol. Monogr.; 2010; 80, pp. 401-422.

71. Simon, AD; Marx, HE; Starzomski, BM. Phylogenetic restriction of plant invasion in drought-stressed environments: Implications for insect-pollinated plant communities in water-limited ecosystems. Ecol. Evol.; 2021; 11, pp. 10042-10053. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34367557][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8328464]

72. Ferguson, JN; Meyer, RC; Edwards, KD; Humphry, M; Brendel, O; Bechtold, U. Accelerated flowering time reduces lifetime water use without penalizing reproductive performance in Arabidopsis. Plant Cell Environ.; 2019; 42, pp. 1847-1867.1:CAS:528:DC%2BC1MXpvVCntLc%3D [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30707443][PubMedCentral: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6563486]

73. Cozzolino, S; Schiestl, FP; Müller, A; De Castro, O; Nardella, AM; Widmer, A. Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: Absence of premating barriers?. Proc. Roy. Soc. B Biol. Sci.; 2005; 272, pp. 1271-1278.

74. Aizen, MA; Vázquez, DP. Flowering phenologies of hummingbird plants from the temperate forest of southern South America: Is there evidence of competitive displacement?. Ecography; 2006; 29, pp. 357-366.2006Ecogr.29.357A

75. Fantinato, E; Del Vecchio, S; Giovanetti, M; Acosta, ATR; Buffa, G. New insights into plants co-existence in species-rich communities: The pollination interaction perspective. J. Veg. Sci.; 2018; 29, pp. 6-14.

76. Kazan, K; Lyons, R. The link between flowering time and stress tolerance. J. Exp. Bot.; 2016; 67, pp. 47-60.1:CAS:528:DC%2BC28Xhtlahu73N [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26428061]

77. Gaudinier, A; Blackman, BK. Evolutionary processes from the perspective of flowering time diversity. New Phytol.; 2020; 225, pp. 1883-1898. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31536639]