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Article

Adonis fucensis (A. sect. Adonanthe, Ranunculaceae), a New Species from the Central Apennines (Italy)

by
Fabio Conti
1,
Christoph Oberprieler
2,
Marco Dorfner
2,
Erik Schabel
2,
Roxana Nicoară
3 and
Fabrizio Bartolucci
1,*
1
Floristic Research Center of the Apennine, University of Camerino—Gran Sasso Laga National Park, San Colombo, 67021 Barisciano, Italy
2
Evolutionary and Systematic Botany Group, Institute of Plant Biology, University of Regensburg, Universitätsstr. 31, D-93053 Regensburg, Germany
3
Department of Taxonomy, Ecology and Nature Conservation, Institute of Biology Bucharest—Romanian Academy, Splaiul Independenței 296, District 6, 060031 Bucharest, Romania
*
Author to whom correspondence should be addressed.
Biology 2023, 12(1), 118; https://doi.org/10.3390/biology12010118
Submission received: 15 December 2022 / Revised: 9 January 2023 / Accepted: 9 January 2023 / Published: 11 January 2023
(This article belongs to the Special Issue Advances in Plant Taxonomy and Systematics)
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Versions Notes

Abstract

:

Simple Summary

Adonis sect. Adonanthe is characterized by species with strongly gibbous abaxial side of achenes, reticulate-venation on its surface, with short and recurved style and includes four series: ser. Amurenses, ser. Coeruleae, ser. Apenninae, ser. Vernales. In the Euro-Mediterranean area three species belonging to A. sect. Adonanthe are currently recognized: A. apennina (ser. Apenninae), A. volgensis (incl. A. transsilvanica; ser. Vernales), A. vernalis (ser. Vernales). In 2021 was discovered in the Central Apennines (Italy) a yellow-flowered Adonis population belonging to sect. Adonanthe similar to A. volgensis. Following an integrated taxonomic approach, we have shown that the newly discovered population should be regarded as a new species, named A. fucensis, endemic to Abruzzo (Central Apennines, Italy).

Abstract

Adonis fucensis is herein described as a new species based on morphological and molecular analyses. It is endemic to one locality of the Central Apennines between Amplero and Fucino plains within the NATURA 2000 network in the SAC IT7110205 (Central Italy). The only discovered population is composed of 65 individuals and is at risk of extinction. The conservation status assessment according to IUCN categories and criteria is proposed and discussed. The new species belongs to A. sect. Adonanthe and is morphologically similar to A. volgensis (incl. A. transsilvanica), a species distributed in Hungary, Romania, Bulgaria, and Turkey as well as eastward to SW Siberia and Central Asia. Adonis fucensis can be distinguished from A. volgensis by larger cauline leaves, pentagonal with lobes lanceolate, larger stipules with more lobes and teeth, and larger flowers. Finally, an analytical key to Adonis species belonging to sect. Adonanthe distributed in Europe is presented.

1. Introduction

The genus Adonis L. (Ranunculaceae) comprises 38 accepted, annual and perennial, species and subspecies, distributed in the northern hemisphere and native to Asia, Europe, northern Africa, and Mediterranean region [1]. According to Wang [2,3], based on a morphological study, the genus Adonis should be divided into two subgenera, six sections, and six series: subg. Adonis (divided into three sections and two series) and subg. Adonanthe (Spach) W.T.Wang (divided into three sections and four series). Recent molecular studies [4,5] do not fully support the taxonomic treatment based on morphological features proposed by Wang [2,3], whereas a phylogenetic classification has not yet been established. In Italy, the genus Adonis is represented by 10 taxa (species and subspecies): the annual and red-flowered A. annua L., A. flammea Jacq. (with two subspecies), A. aestivalis L. (with two subspecies), A. microcarpa DC., and the perennial and yellow-flowered A. distorta Ten. and A. vernalis L. Adonis distorta is the only species of the genus endemic to Italy [6,7], growing in the alpine belt on limestone screes and less frequently on more stabilized rocky slopes between 1845 and 2675 m a.s.l. of the Central Apennines [8]. The Abruzzo administrative region, in Central Italy, hosts seven Adonis taxa, the highest number among the Italian administrative regions, including the rare endemic A. distorta, and the only Italian populations of the steppe species A. vernalis [9]. In recent years extensive field surveys have been carried out for floristic and vegetation research in the National Park of Abruzzo, Lazio, and Molise [10,11,12,13,14], thanks to which some plants typical of the Alpine continental valleys or even of the E-European steppes have been discovered (i.e., [15,16]), confirming that the inner basins of the Central Apennine mountains have a pronounced steppic character. In March 2021 a group of hikers, discovered within the buffer area of the National Park, a yellow-flowered Adonis population. After analyzing the photographic material sent to us by Marina Buschi, who discovered the plant, we immediately realized that we were dealing with a very interesting population of Adonis morphologically very different from the two yellow-flowered species that already occurred in Italy, which are A. vernalis and A. distorta. From March to June 2021, we performed field surveys in the discovery locality, close to Amplero in Collelongo municipality (L’Aquila, Abruzzo, Central Italy), to evaluate the numerical consistency of the population and look for new stations. According to the classification proposed by Wang [2,3], the new discovered Adonis population belongs to A. sect. Adonanthe W.T.Wang ser. Vernales Bobr. ex Poschk. The section is characterized by species with strongly gibbous abaxial side of achenes, reticulate-venation on its surface, with short and recurved style and includes four series [2,3]: ser. Amurenses Poschk. with petiolate lower cauline leaves, ovoid, triangular or elliptic, and yellow or white petals; ser. Coeruleae Poschk. with petiolate lower cauline leaves, oblong or ovoid-oblong, 3–4 pinnatisect, and white or purple petals; ser. Apenninae Bobr. ex Poschk. with sessile or sub-sessile cauline leaves, pinnately compound, segments 2–3 pinnatisect, and yellow petals; ser. Vernales with sessile cauline leaves, palmately compound, segments 3 pinnatisect, and yellow petals. In the Euro-Mediterranean area three species belonging to A. sect. Adonanthe are currently recognized [1,17]: A. apennina L. (ser. Apenninae), A. volgensis DC. (incl. A. transsilvanica Simonov.; ser. Vernales), and A. vernalis L. (ser. Vernales). All other currently accepted species [1] within A. sect. Adonanthe are distributed exclusively in Asia: A. amurensis Regel & Radde (ser. Amurenses), A. davidi Franch. (ser. Amurenses), A. multiflora Nishikawa & Koji Ito (ser. Amurenses), A. pseudoamurensis W.T.Wang (ser. Amurenses), A. ramosa Franch. (ser. Amurenses), A. shikokuensis Nishikawa & Koji Ito (ser. Amurenses), A. sutchuenensis Franch. (ser. Amurenses), A. coerulea Maxim. (ser. Coeruleae), A. bobroviana Simonov. (ser. Apenninae), A. mongolica Simonov. (ser. Apenninae), A. tianschanica (Adolf) Lipsch. (ser. Apenninae), A. turkestanica (Korsh.) Adolf (ser. Apenninae), and A. villosa Ledeb. (ser. Apenninae).
The closest species within A. sect. Adonanthe ser. Vernales based on morphology is A. volgensis, a typical plant of the E-European and Asiatic steppes, distributed in Hungary, Romania, Bulgaria, and Turkey, as well as eastward to SW Siberia and Central Asia [1,17,18]. The populations from Romania and Hungary were regarded by Wang [3] as a different species with the name A. transsilvanica Simonov. Instead, others authors have considered A. transsilvanica as synonym of A. volgensis (i.e., [1]), as a name ambiguous [19], or have not listed it at all [17,18].
An extensive morphological and molecular investigation has been carried out providing evidence about the differentiation between A. volgensis and the new discovered Apennines’ population. Our results, and the disjunct and isolated geographical distribution of the population occurring in the Central Apennines, allowed us to describe it as a species new to science, named A. fucensis.

2. Materials and Methods

2.1. Plant Material

This study is based on field surveys, an extensive analysis of the relevant literature, and examination of herbarium specimens (including the original material of A. volgensis and A. transsilvanica; Supplementary File S1) kept in APP, B, BP, BRNU, CL, G, K, LD, LE, MW, S, UPS, and US (acronyms follow [20]).
Morphological characters, recognized as taxonomically discriminant in Adonis [2,3,18,21] were scored in the herbarium specimens kept in APP, BP, CL, K, MW, UPS, and US. All morphological characters were observed and measured under a Leica MZ16 stereoscopic microscope, using a digital caliper with 0.1 mm precision. Digital images of herbarium specimens from online databases were measured with IC Measure version 2.0.0.245.
Regarding the new species, having found only one small population, we have not collected whole individuals, but only some parts, such as petals, sepals, leaves, etc., and then dried them. Only two individuals, without rhizomes, probably displaced by wild fauna, were collected. For the description of the new species some characters, i.e., length of the sepals and petals, were also scored in the field on fresh material.

2.2. Morphometric Analyses

A total of 18 morphological characters were selected and scored in 87 dried individuals belonging to A. volgensis (63) from Romania, Moldavia, Russia and to the new population from the Central Apennines (Italy), named A. fucensis (24). Two characters, i.e., height (H) and number of petals (NP), were scored for A. fucensis on the field. Among the morphological characters studied, 14 are quantitative, 1 is calculated ratio, and 3 are qualitative (Table 1). Samples with missing data were not included in the multivariate analysis (resulting dataset of 50 individuals × 18 variables). For each quantitative character an independent sample t-test was carried out with SPSS v25 software (IBM Corp., Armonk, NY, USA) [22]. A non-metric multidimensional scaling (NMDS) and Cluster Analysis (CA) using the average linkage method (UPGMA), were performed with PAST package v4.11 software (Natural History Museum, Oslo, Norway) [23]. The similarity matrix was calculated using the Gower coefficient, suitable for mixed data [24]. Furthermore, the variability of the analyzed morphological characters was described by standard statistical parameters (mean, standard deviation, minimum, maximum, and 25th and 75th percentiles). Boxplots were built through SPSS v25.

2.3. DNA Sequencing and AFLPseq Fingerprinting

Genomic DNA for both sequencing and genetic fingerprinting was extracted according to the CTAB DNA extraction protocol of Doyle and Dickson [25] and Doyle and Doyle [26]. Amplification of the two internal transcribed spacer regions (ITS1, ITS2) of the nuclear ribosomal repeat (nrDNA) was carried out with primers ITS-18SF [27] and ITS2 [28] for ITS1 and ITS-D [29] and ITS-SR [30] for ITS2, respectively. After purification of PCR amplicons with AmpliClean (Nimagen, Nijmegen, The Netherlands) magnetic beads, Sanger sequencing was carried out by a contract sequencing company (Macrogen Europe, Amsterdam, The Netherlands). Electropherograms were manually edited with CHROMAS v2.6.6 [31]; polymorphisms observed in accession A1251 were resolved manually and the two resulting sequences were independently included in the alignment together with sequences of other species of Adonis sect. Adonanthe and an outgroup sequence (from Trollius ranunculoides Hemsl.). We used PAUP* v4.0a169 [32] to calculate distances among the aligned sequences based on the Kimura-2-Parameter model and constructed a Neighbor-joining tree. A bootstrap analysis was performed with 1000 replicates.
The AFLPseq fingerprinting method has been proposed by [33] and combines the genome-complexity reducing AFLP approach [34] with the next-generation sequencing (NGS) of resulting AFLP bands using the Nanopore sequencer MinION from Oxford Nanopore Technologies (Oxford, UK). It provides sequence and single-nucleotide polymorphism (SNP) information for hundreds of anonymous loci from across the whole genome and could be used for both population genetic, phylogenetic, and species delimitation studies. It is suited for both well-preserved DNA from silica-gel dried leaf material and degraded DNA from herbarium specimens.
The present AFLPseq study comprised 12 Adonis accessions (Supplementary Table S1), either recently collected, silica-gel dried material (five accessions from Italy and Romania), or well-preserved herbarium material housed in the herbaria B and BRNO (seven accessions from Romania, the Russian Federation, and Kazakhstan). The accessions were selected (a) to cover large parts of the distribution range of A. volgensis and (b) to include only plant material in the fingerprinting procedure, for which extracts of unfragmented genomic DNA was expectable. The AFLPseq procedure followed the protocol given in [33] with the following modifications: in the restriction-ligation step, we used a double-digestion procedure with restriction enzymes MseI and EcoRI. After ligation of MseI and EcoRI adapters (MseI adapter: 5′-GACGATGAGTCCTGAG-3′ + 5′-TACTCAGGACTCAT-3′; EcoRI adapter: 5′-CTCGTAGACTGCGTACC-3′ + 5′-AATTGGTACGCAGTCTAC-3′), we continued with the AFLP genome-reduction protocol using primers with 1bp-overhangs (MseI-C: 5′-GATGAGTCCTGAGTAAC-3′; EcoRI-A: 5′-GACTGCGTACCAATTCA) in the pre-selective amplification step and in the selective amplification step with additional 1bp- (EcoRI side) or 2bp-overhangs (MseI side), respectively. The two primers used in the latter amplification step, however, were additionally tailored to include Nanopore barcode adapter sequences at the 5′ end of the primers (Mse_CTG_Nanopore_fw: 5′-TTTCTGTTGGTGCTGATATTGCGATGAGTCCTGAGTAACTG-3′; Eco_AA_Nanopore_rv: 5′-ACTTGCCTGTCGCTCTATCTTCGACTCCGTACCAATTCAA-3′), as suggested in the ′Ligation sequencing amplicons—PCR barcoding (SQK-LSK109 with EXP-PBC001)’ protocol by Oxford Nanopore Technologies, substituting a subsequent ligation of the Nanopore barcode adapter with an additional barcoding PCR. To ensure specific binding with long and tailed primers, a two-step variation of the selective PCR was conducted (94 °C for 2 min; followed by 30 cycles of 94 °C for 20 s and 72 °C for 2 min; and a final step at 72 °C for 2 min). To every 2 µL of 1:10 diluted preselective PCR product, 5 µL Taq DNA Polymerase Master Mix RED, 0.25 µL of each 10 µM tailed selective primer, and 2.5 µL H2O were added. After the selective PCR, the length of the fragments ranged from 200–500 bp. All subsequent steps (Nanopore barcode PCR, sample multiplexing, size selection, preparation of Nanopore sequencing library) followed [33]. The resulting library was sequenced with the MinION using a Flongle flow cell. Read data processing, de novo locus assembly, identification of orthologous loci, and reference-based SNP calling with the SLANG pipeline, and the final calculation of frequency-sensitive SNP-based Nei distances followed the protocol described by [33]. Based on these pairwise distances both a phylogenetic network reconstruction using the Neighbor-joining method in SPLITSTREE v4.16.1 [35] and a principal co-ordinate analysis (PCoA) with a custom R v4.0.5 script using the ‘phangorn‘ library to read the distance matrices and the ‘ape‘ package to calculate and plot the PCoA was carried out.

3. Results

3.1. Morphometric Analyses

The NMDS, performed with three dimensions, yielded an ordination with a stress value of 0.09224. The scatterplot shows on the first two axes a clear distinction between A. volgensis and A. fucensis, and no overlapping areas among individuals were found (Figure 1). The UPGMA dendrogram (Figure 2) yielded two well-defined clusters, one including all individuals of A. volgensis and the other all individuals of A. fucensis.
Comparisons of morphological characters between A. volgensis and A. fucensis (Figure 3) are summarized in Table 2. The states of 13 characters (H, MLL, MLW, NMLN, ATL, LMW, LWB, LMW/ LWB, SL, SW, NSL, CD, SLD, SWD, PLD, and PWD) show significant differences between the two species (p < 0.01). Boxplots of relevant characters are showed in Figure 4.

3.2. nrDNA Sequence Variation

The Neighbor-joining tree based on Kimura-2-parameter distances among nrDNA ITS sequences of 15 Adonis accessions is shown in Figure 5. The central Italian Adonis fucensis accession (A1252) is found being closely related with A. volgensis and A. vernalis in the monophyletic group of A. sect. Adonanthe ser. Vernales. As also found by a more comprehensive phylogenetic analysis of section Adonanthe performed by [4], series Amurenses did not form a monophyletic group.

3.3. AFLPseq Fingerprinting

In total, 731,698 reads and 243.72 Mbp were sequenced for the 12 Adonis accessions. After read preprocessing, 592,432 reads with lengths between 10 bp and 614 bp passed the Q5 quality filter. With the SLANG pipeline (cluster thresholds optimized to values of 0.85 and 0.95 for the first and second cluster step, respectively), 486 orthologous loci were inferred, containing 2944 SNPs. After calculation of pairwise Nei distances, the resulting Neighbor-joining tree (Supplementary File S2) and the PCoA plot were received (Figure 6). While in the first, the Adonis accession from the Central Apennines (A1252) is connected with the remaining A. volgensis representatives without any exceptionally longer branch than the other accessions, the PCoA plot demonstrates the clear separation between the two taxa; with accessions of the latter on the left and accession A1252 on the right side of principal co-ordinate PCo axis 1, which account for 20.8% of the total variation in the data set. Additionally, PCo axis 2 (accounting for additional 15.0% of the total variation) shows a clear geographical separation within A. volgensis, with accessions of this species from Romania (sometimes considered as being an independent species, A. transsilvanica) on the positive and accessions from Russia and Kazakhstan on the negative side of the axis.
An additional result of the analysis is worth mentioning in methodological respects: accessions A1251, A1273, and A1274 are very similar to each other in spite of the fact that the three probes come from the same locality (Romania, Constanta, Cotu Văii), but were recently collected as silica-gel dried leaf material (the latter two) or as an herbarium specimen (A1251) twenty years ago. This observation adds to the trustworthiness of the AFLPseq protocol and the comparability of differently preserved DNAs in terms of sequence information retrieved through this process.

4. Discussion

Morphological and molecular analyses provide evidence that A. fucensis should be regarded as a new species, endemic to Abruzzo (Central Apennines, Italy). It is similar to A. volgensis, a typical plant of the E-European and Asiatic steppes, distributed in Hungary, Romania, Bulgaria, and Turkey, as well as eastward to SW Siberia and Central Asia, but it can be distinguished by several quantitative and qualitative morphological characters, as shown in Table 2. The new species lives in shrub-steppe habitat in contact environments between bushes dominated by Prunus spinosa L. subsp. spinosa and steppe grasslands with the presence of Festuca valesiaca Schleich. ex Gaudin subsp. valesiaca. Abruzzo is the Italian administrative region with the highest number of taxa belonging to the genus Adonis, and also hosts the only Italian populations of the extremely rare steppe species A. vernalis.
The dry sub-continental climate of internal basins of the Central Italy, together with wild herbivore disturbance and prehistoric anthropogenic fires [36], may have reduced the post-glacial reforestation. Subsequently sheep grazing and the practice of transhumance, dating back to the 6th century BC or earlier in Abruzzo and widely practiced until the 1950s [37,38], has probably favored the spread of grasslands [39]. Around Amplero, close to the locality of A. fucensis, lies an archaeological site inhabited since the VI century B.C. The area hosted, from the Bronze age until Medieval times and beyond, important shepherd settlements and was located on transhumance routes [40]. These causes explain the persistence of steppe species in the internal areas of the Central Apennines.
In the internal basins of Abruzzo such as the Fucino and the L’Aquila plains, there is a consistent number of grassland taxa featuring a disjunction with E-European steppes, giving these areas a pronounced steppic character: Alyssum desertorum Stapf., Androsace maxima L., Astragalus danicus Retz., A. exscapus L. subsp. exscapus, A. onobrychis L., A. vesicarius L. subsp. vesicarius, Ceratocephala falcata (L.) Cramer, Crocus variegatus Hoppe & Hornsch, Falcaria vulgaris Bernh., Festuca valesiaca Schleich. ex Gaudin subsp. valesiaca, Pulsatilla montana (Hoppe) Rchb. subsp. montana, Poa perconcinna J.R.Edm., Salvia aethiopis L., and Stipa capillata L. [12,15,16]. In addition, some Italian endemics living in the same area should be considered of steppic origin such as Goniolimon tataricum (L.) Boiss. subsp. italicum (Tammaro, Pignatti & Frizzi) Buzurović [41,42], and Astragalus aquilanus Anzal. [43]. The presence of these plants in the central Apennines is due to different migrations from east to west. Plants with similar morphological features, with respect to the Northern and Eastern populations, e.g., A. exscapus subsp. exscapus, or F. valesiaca subsp. valesiaca, probably arrived in the Central Apennines during late-Pleistocene [15]. An initial wave of steppic plants probably occurred during the Messinian Salinity Crisis, such as the spread of an ancient G. tataricum lineage throughout south-eastern Europe [37]. This could be a hypothesis on the origin of the presence of A. fucensis in the Central Apennines.
Alternatively, a recent study on the phylogeography of the closely related A. vernalis [5] revealed that this plant species expanded its range from SE Europe into the Euro-Siberian steppe, with a Spanish population of the species being the earliest-diverging lineage. Whether members of our present study group parallel this migration pattern and A. fucensis constitutes the earliest-diverging remnant of an eastwards expanding A. volgensis could be hypothesized here but must await a much denser sampling of the latter species. Due to the restricted number of accessions analyzed in the present contribution, the biogeographical history of A. fucensis and A. volgensis remain unresolved.
Adonis fucensis is a very rare species, consisting of a very small population of 65 individuals, assessed here as critically endangered. In the two years (2021–2022) in which we were able to study the population we observed that although plants have a large number of flowers, they produce few fruits (we have observed many abortive achenes), and its survival is probably related to vegetative reproduction with consequent loss of genetic diversity. It will be absolutely necessary to undertake a dialogue with the National Park of Abruzzo, Lazio, and Molise to plan correct in situ and ex situ conservation strategies, to try to save this new species from extinction.

5. Taxonomic Treatment

Adonis subg. Adonanthe (Spach) W.T.Wang, Bull. Bot. Res., Harbin 14(1): 22 (1994) ≡ Adonanthe Spach, Hist. Nat. Vég. 7: 227 (1838).
Type: A. vernalis L. [Lectotype, Herb. Linn. No. 714.4, LINN [digital photo!]); image of the lectotype is available at https://linnean-online.org (accessed on 28 November 2022)].
Adonis sect. Adonanthe W.T.Wang, Bull. Bot. Res., Harbin 14(1): 26 (1994).
Type: A. vernalis L.
Adonis ser. Vernales Bobr. ex Poschk., Novosti Sist. Vyssh. Rast. 14: 83 (1977).
Type: A. vernalis L.
Adonis volgensis DC., Syst. Nat. [Candolle] 1: 545 (1817) ≡ Adonanthe volgensis (DC.) Chrtek & Slavíková, Preslia 50(1): 24 (1978).
Holotype: Ad Volgam, 1817, Steven s.n. [G barcode G00144834 [digital photo!]; image of the holotype is available at http://www.ville-ge.ch/musinfo/bd/cjb/chg (accessed on 28 November 2022)].
= Adonis transsilvanica Simonovich, Dokl. Akad. Nauk Belorusski. S.S.R., IX(6): 396 (1965).
Holotype: Hungaria. Transsilvania. In collibus herbidis ad “Szénafü” prope “Kolozsvár”, May and June 1910, A. Richter 5201 [LE barcode LE00012366 [digital photo!], isotypes LD No. 2196730 [digital photo!], S No. 7488 [digital photo!]; image of the holotype is available at https://en.herbariumle.ru (accessed on 28 November 2022)].
Adonis fucensis F.Conti & Bartolucci, sp. nov. (Figure 7).
Type: ITALY. Abruzzo, Valle Lupara alla base del Monte Annamunna (Collelongo, L’Aquila; WGS84 33T 41°55′21″ N, 13°38′8″ E), radura, margini e cespuglieti a Prunus spinosa L. subsp. spinosa, 1038 m, 9 April 2021, F. Conti s.n. (holotype APP No. 66211).
Diagnosis: it is similar to A. volgensis but can be distinguished by larger cauline leaves, leaf blade pentagonal vs. triangular-ovate, lobes lanceolate vs. linear to narrowly lanceolate, larger stipules more divided, and larger sepals and petals.
Description: Herbs perennial. Rhizomatous. Roots numerous, fibrous. Stems erect, branched, pubescent, (8)10.25–13.75(16) cm tall. Scales membranous, alternate at lower parts of stem. Leaves stipulate, alternate, palmately compound with segments 3-pinnatifid, sessile, pentagonal, (56.7)65.75–86.22(96.06) mm long, (45.16)57.01–75.06(79.30) mm wide, green, hairy, n. of lobes and teeth (84)123–187(280), terminal lobes lanceolate, dentate, mucronate to acute at apex with angle (31.73)43.36–54.32(74.4)°, subterminal lobes (3.3)3.5–5.7(6.7) mm long, (1.14)1.41–1.91(2.83) mm max wide, (0.90)1.08–1.49(2.29) mm wide at base; stipules pinnatifid, (14.13)19.83–25.23(31.00) mm long, (9.59)16.40–23.24(32.87) mm wide, n. of stipules lobes and teeth (7)10–21(–28). Flower solitary, (40)44.75–60(66) mm in diameter in vivo, yellow. Sepals 5–8, ovate, obovate to elliptic, rarely truncate or dentate, (17)19–27.8(33) mm long (fresh), (11)12.25–23.63(27) mm long (dry), (9)10.1–14.9(18) mm wide (fresh), (7.5)9.63–12(14) mm wide (dry), olive-green, yellowish, brownish, purplish abaxially, hairy. Petals (9)12–14(18), yellow, obovate to narrowly obovate, (19)21–32(33) mm long (fresh), (11)21.75–27(30) mm long (dry), (7–)8–12.9(–14) mm wide (fresh), (6)8–10.50(13) mm wide (dry), obtuse, entire or rarely with rounded notches at apex, glabrous. Stamens numerous, basifixed; anther 2-loculed, oblong, 2–2.2 mm long, 0.5–0.7 mm wide; filaments filiform ca. 6 mm. Pistil numerous, ovary ovate, puberulous; styles 0.9–1.5 mm long, recurved. Aggregated fruit subglobular to ellipsoidal, 9–11 mm long, 8–10 mm wide. Receptacle elliptical pubescent. Achenes numerous, obovoid to ellipsoidal, 3.5–4.3 mm long, 2.5–3.2 mm wide, pubescent; style 0.9–1.5 mm long, recurved at base, ± appressed.
Etymology: Adonis fucensis is named after Fucino Plain located nearby to the north and affected by the presence of the third largest Italian lake drained in 1878.
Habitat: The species grows in the contact zone between bushes dominated by Prunus spinosa subsp. spinosa and steppic grasslands with Festuca valesiaca subsp. valesiaca, Achillea setacea Waldst. & Kit., Koeleria splendens C.Presl, Centaurea jacea L. subsp. gaudinii (Boiss. & Reut.) Gremli, and Galium verum L. subsp. verum.
Phenology: Flowering from March to April; fruiting from May to June.
Distribution: Endemic to one locality of Abruzzo (Central Italy) within the SAC IT7110205 “Parco Nazionale d’Abruzzo”. The species grows in a small flat clearing on the slopes of Mt. Annamunna, between Amplero and Fucino plains (Supplementary File S1).
Conservation status: Adonis fucensis is known only by one location (locus classicus) where, during 2021, we counted only 65 individuals (genets). It is located within the NATURA 2000 network in the SAC IT7110205 “Parco Nazionale d’Abruzzo”. The area of occupancy (AOO) is 4 km2 (cell grid 2 × 2 km), calculated with GeoCAT (Geospatial Conservation Assessment Tool) software (http://www.plantsoftheworldonline.org/ (accessed on 10 October 2022)) [44]. We observed pressure due to the grazing of wild animals (especially wild boars that dig up single plants). Observing the aerial photos of the 1980s it is evident how in the A. fucensis habitat the shrub and tree vegetation increased by reducing the surface of the pastures probably due to a decrease in grazing by livestock. The natural succession of vegetation is a pressure and a threat for the population of A. fucensis. It is not possible to be certain of the decline of the species even if it is reasonable to assume that it was more common in the past. According to IUCN criterion B2ab(iii) [45], the species is assessed as Critically Endangered (CR).

Key to Adonis Species Belonging to sect. Adonanthe Distributed in Europe

  • 1. Leaves pinnately compound …………………………………………………... A. apennina
  • 1. Leaves palmately compound …………………………………………………….………… 2
  • 2. Leaves glabrous, with narrowly linear, entire lobes, rarely few-dentate ........ A. vernalis
  • 2. Leaves pubescent, rarely glabrescent, with linear-lanceolate to lanceolate, dentate lobes …………………………………………………………………………………………………….. 3
  • 3. Middle cauline leaves triangular-ovate, rarely pentagonal, (24.12)38.70–58.35(109.66) mm long × (10.00)27.00–42.60(81.30) mm wide, with (12)32–85(176) lobes and teeth linear to narrowly lanceolate; stipule (4.64)9.31–15.88(22.00) mm long, with (2–)3–6(–12) lobes and teeth; sepal (6.40)9.26–14.51(21.07) mm long × (2.50)3.57–6.05(9.46) mm wide, petal (7.61)12.12–20.69(29.28) mm long × (2.85)3.95–6.83(11.68) mm wide ………………….………………………………………………………..………..…. A. volgensis
  • 3. Middle cauline leaves pentagonal, (56.70)65.75–86.22(96.06) mm long × (45.16)57.01–75.06(79.30) mm wide, with (84)123–187(280) lobes and teeth lanceolate; stipule (14.13)19.83–25.23(31.00) with 10–22.4(–26) lobes and teeth; sepal (11.00)12.25–23.63(27.00) mm long × (7.50)9.63–12.00(14.00) mm wide, petal (11.00)21.75–27.00(30.00) mm long × (6.00)8.00–10.50(13.00) mm wide …………………………………………………… A. fucensis

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/biology12010118/s1, File S1: List of the herbarium specimens examined; distribution map of Adonis fucensis. File S2: Neighbor-joining tree of accessions of Adonis fucensis and A. volgensis. Table S1: Adonis populations sampled for the present study with information on localities, voucher specimens, and GenBank accession numbers for nrDNA ITS.

Author Contributions

Conceptualization and methodology, F.C., F.B. and C.O.; field investigations, F.C., F.B. and R.N.; morphological measurements, F.C.; morphological analyses, F.B.; molecular analyses, C.O., M.D. and E.S.; writing—original draft preparation, F.C., F.B. and C.O.; writing—review and editing, F.C., F.B., C.O. and R.N.; supervision, F.C. and F.B.; funding acquisition, F.C. and F.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Abruzzo, Lazio, and Molise National Park (grant number BVI400031).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in the current study are available within the article and Supplementary Materials.

Acknowledgments

The authors wish to thank Directors and Curators of B, BP, CL, K, MW, UPS, and US for providing us digital images herbarium specimens. We sincerely thank our friend Marina Buschi, who was the first to discover this new species during a CAI (Club Alpino Italiano) excursion, as well as Valeria Giacanelli and Biagio Sucapane for accompanying us during field investigations. Maximilian Schall is thankfully acknowledged for his technical help in the molecular systematic laboratory of C.O. (Regensburg University). Finally, we would like to thank the President, the Director and the Staff at Abruzzo, Lazio and Molise National Park Agency for encouraging and supporting this research. This work was supported by the “Progetto di Ricerca di Rilevante Interesse Nazionale” (PRIN) “PLAN.T.S. 2.0—towards a Renaissance of PLANt Taxonomy and Systematics” led by the University of Pisa, under grant number 2017JW4HZK.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Non-metric multidimensional scaling scatterplot showing the first two dimensions of the analysis.
Figure 1. Non-metric multidimensional scaling scatterplot showing the first two dimensions of the analysis.
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Figure 2. Hierarchical clustering of individuals of A. volgensis and A. fucensis using paired group algorithm (UPGMA) and Gower Similarity Index. Cophenetic correlation coefficient is 0.8566.
Figure 2. Hierarchical clustering of individuals of A. volgensis and A. fucensis using paired group algorithm (UPGMA) and Gower Similarity Index. Cophenetic correlation coefficient is 0.8566.
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Figure 3. Comparison of A. fucensis and A. volgensis: (A) A. fucensis from Mt. Annamunna locality (Italy, Abruzzo, photo by F. Bartolucci); (B) A. volgensis from Murfatlar locality (Romania, Constanța County, photo by R. Nicoară); (C) dry cauline leaf of A. fucensis, pentagonal leaf blade; (D) dry cauline leaf of A. volgensis, triangular-ovate leaf blade. Scale bar 1 cm.
Figure 3. Comparison of A. fucensis and A. volgensis: (A) A. fucensis from Mt. Annamunna locality (Italy, Abruzzo, photo by F. Bartolucci); (B) A. volgensis from Murfatlar locality (Romania, Constanța County, photo by R. Nicoară); (C) dry cauline leaf of A. fucensis, pentagonal leaf blade; (D) dry cauline leaf of A. volgensis, triangular-ovate leaf blade. Scale bar 1 cm.
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Figure 4. Boxplots expressing morphological variation between A. fucensis (FUC) and A. volgensis (VOL). Outlined central box depicts middle 50% of data, extending from 25th and 75th percentiles, and horizontal bar is the median. Ends of vertical lines (or “whiskers”) indicate minimum and maximum data values, unless outliers are present, in which case whiskers extend to a maximum of 1.5 times inter-quartile range. Circles indicate outliers.
Figure 4. Boxplots expressing morphological variation between A. fucensis (FUC) and A. volgensis (VOL). Outlined central box depicts middle 50% of data, extending from 25th and 75th percentiles, and horizontal bar is the median. Ends of vertical lines (or “whiskers”) indicate minimum and maximum data values, unless outliers are present, in which case whiskers extend to a maximum of 1.5 times inter-quartile range. Circles indicate outliers.
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Figure 5. Neighbor-joining tree of 15 accessions of Adonis sect. Adonanthe based on nrDNA ITS sequence variation and Kimura-2-parameter distances. GenBank accession numbers and probe numbers of the present study (A. fucensis, A. volgensis) are given in brackets. Numbers above branches are bootstrap values based on 1000 replicates.
Figure 5. Neighbor-joining tree of 15 accessions of Adonis sect. Adonanthe based on nrDNA ITS sequence variation and Kimura-2-parameter distances. GenBank accession numbers and probe numbers of the present study (A. fucensis, A. volgensis) are given in brackets. Numbers above branches are bootstrap values based on 1000 replicates.
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Figure 6. Ordination of accessions of A. fucensis (black) and A. volgensis (blue: Romania; red: Russia; green: Kazakhstan) based on pairwise Nei distances from 2944 single-nucleotide polymorphisms (SNPs) from 486 AFLPseq loci in a Principal Co-ordinate Analysis (PCoA), with axis 1 explaining 20.8% and axis 2 explaining 15.0% of the total variance, respectively.
Figure 6. Ordination of accessions of A. fucensis (black) and A. volgensis (blue: Romania; red: Russia; green: Kazakhstan) based on pairwise Nei distances from 2944 single-nucleotide polymorphisms (SNPs) from 486 AFLPseq loci in a Principal Co-ordinate Analysis (PCoA), with axis 1 explaining 20.8% and axis 2 explaining 15.0% of the total variance, respectively.
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Figure 7. Adonis fucensis F.Conti & Bartolucci [Italy, Abruzzo, Mt. Annamunna, photo by F. Conti (A–E,G) and (F). Bartolucci (F)]. (A) Habitat and flowering plants of A. fucensis; (B) whole plants; (C) flowering plants; (D) cauline leaf; (E) flower, dorsal view; (F) flower, front view; (G) not mature aggregate fruit.
Figure 7. Adonis fucensis F.Conti & Bartolucci [Italy, Abruzzo, Mt. Annamunna, photo by F. Conti (A–E,G) and (F). Bartolucci (F)]. (A) Habitat and flowering plants of A. fucensis; (B) whole plants; (C) flowering plants; (D) cauline leaf; (E) flower, dorsal view; (F) flower, front view; (G) not mature aggregate fruit.
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Table
Table 1. Morphological characters studied.
Table 1. Morphological characters studied.
AbbreviationDescription of the CharacterType
HHeight (cm)quantitative continuous
MLLMiddle leaf length (mm)quantitative continuous
MLWMiddle leaf width (mm)quantitative continuous
SMLShape of middle leaf
(0: pentagonal; 1: triangular-ovate)		qualitative
NLMLNumber of lobes and teeth of the middle leafquantitative discrete
STLShape of terminal lobe
(0: lanceolate; 1: narrowly lanceolate; 2: linear)		qualitative
ATLAngle of terminal apex lobe (°)quantitative continuous
LMWSubterminal lobe max width (mm)quantitative continuous
LWBSubterminal lobe width at base (mm)quantitative continuous
LMW/LWBRatio lobe max width/lobe width at basecalculated ratio
SLStipule length (mm)quantitative continuous
SWStipule width (mm)quantitative continuous
NSLNumber stipule lobes and teethquantitative discrete
SLDSepal length (mm)quantitative continuous
SWDSepal width (mm)quantitative continuous
PLDPetal length (mm)quantitative continuous
PWDPetal width (mm)quantitative continuous
NPNumber of petalsquantitative discrete
Table
Table 2. Morphological comparison of A. volgensis and A. fucensis. Quantitative continuous characters are expressed in mm and are reported as mean ± standard deviation and 25–75 percentiles (extreme values in brackets). For quantitative discrete cardinal characters, 25–75 percentiles are given (extreme values in brackets). Significantly different character states are shown in bold (p < 0.01).
Table 2. Morphological comparison of A. volgensis and A. fucensis. Quantitative continuous characters are expressed in mm and are reported as mean ± standard deviation and 25–75 percentiles (extreme values in brackets). For quantitative discrete cardinal characters, 25–75 percentiles are given (extreme values in brackets). Significantly different character states are shown in bold (p < 0.01).
Adonis volgensisAdonis fucensis
Height (cm)22.80 ± 7.21(10.49)17.42–27.39(39.61)12.06 ± 2.46(8)10.25–13.75(16)
Middle leaf length (mm)50.36 ± 16.86(24.12)38.70–58.35(109.66)74.28 ± 12.39(56.70)65.75–86.22(96.06)
Middle leaf width (mm)35.01 ± 13.75(10.00)27.00–42.60(81.30)64.31 ± 10.83(45.16)57.01–75.06(79.30)
Shape of middle leaf triangular-ovate, rarely pentagonal pentagonal
Number of lobes and teeth of the middle leaf (12)32–85(176) (84)123–187(280)
Shape of terminal lobe linear to narrowly lanceolate lanceolate
Angle of terminal apex lobe (°)31.95 ± 11.21(15.04)23.73–37.55(64.96)50.45 ± 11.76(31.73)43.36–54.32(74.4)
Subterminal lobe max width (mm)1.13 ± 0.39(0.53)0.84–1.34(2.39)1.76 ± 0.48(1.14)1.41–1.91(2.83)
Subterminal lobe width at base (mm)0.94 ± 0.28(0.51)0.70–1.10(1.75)1.36 ± 0.38(0.90)1.08–1.49(2.29)
Ratio lobe max width/lobe width at base1.21 ± 0.27(0.91)1.02–1.32(2.52)1.29 ± 0.11(1.13)1.21–1.37(1.57)
Stipule length (mm)12.63 ± 4.36(4.64)9.31–15.88(22.00)22.41 ± 4.53(14.13)19.83–25.23(31.00)
Stipule width (mm)8.45 ± 4.82(1.69)4.85–10.60(24.63)22.06 ± 5.56(9.59)16.40–23.24(32.87)
Number of stipule lobes and teeth (2–)3–6(–12) (7)10–21(–28)
Sepal length (mm)12.23 ± 3.67(6.40)9.26–14.51(21.07)18.81 ± 5.80(11.00)12.25–23.63(27.00)
Sepal width (mm)4.98 ± 1.71(2.50)3.57–6.05(9.46)10.61 ± 1.82(7.50)9.63–12.00(14.00)
Petal length (mm)17.2 ± 6.04(7.61)12.12–20.69(29.28)23.48 ± 5.54(11.00)21.75–27.00(30.00)
Petal width (mm)5.59 ± 2.15(2.85)3.95–6.83(11.68)9.37 ± 1.96(6.00)8.00–10.50(13.00)
Number of petals (10)12–13(16) (9)12–14(18)
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Conti, F.; Oberprieler, C.; Dorfner, M.; Schabel, E.; Nicoară, R.; Bartolucci, F. Adonis fucensis (A. sect. Adonanthe, Ranunculaceae), a New Species from the Central Apennines (Italy). Biology 2023, 12, 118. https://doi.org/10.3390/biology12010118

AMA Style

Conti F, Oberprieler C, Dorfner M, Schabel E, Nicoară R, Bartolucci F. Adonis fucensis (A. sect. Adonanthe, Ranunculaceae), a New Species from the Central Apennines (Italy). Biology. 2023; 12(1):118. https://doi.org/10.3390/biology12010118

Chicago/Turabian Style

Conti, Fabio, Christoph Oberprieler, Marco Dorfner, Erik Schabel, Roxana Nicoară, and Fabrizio Bartolucci. 2023. "Adonis fucensis (A. sect. Adonanthe, Ranunculaceae), a New Species from the Central Apennines (Italy)" Biology 12, no. 1: 118. https://doi.org/10.3390/biology12010118

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