Comparative leaf anatomy of the nothospecies × Butyagrus nabonnandii (Arecaceae) with its parental species

Abstract

Anatomical studies of the leaf blade have been used to complement the morphological data and aid circumscription and identification in Arecaceae. The hybrid palm ×Butyagrus nabonnandii results from the natural cross between Butia odorata and Syagrus romanzoffiana. This study aimed to verify if the leaf anatomy can help identify the hybrid and differentiate it from the parental taxa. Samples from the middle portion of the pinnae were collected and subjected to the usual techniques for light microscopy. Three portions of the pinnae were sampled: margin, intermediate region, and midrib. The main characteristics considered were the arrangement of fibre and vascular bundles. Pinnae anatomy proved to be useful in the identification of ×B. nabonnandii, because it showed a distinctive pattern, highlighting the importance of leaf anatomy in differentiating the hybrid from parental taxa. The pinnae anatomy of the hybrid was a combination of parental taxa’s characters, similar to the external morphology.

Key words:
Butia; hybrid palm; plant anatomy; Syagrus; taxonomy

Resumo

Estudos anatômicos da lâmina foliar têm sido usados para complementar os dados morfológicos e ajudar na circunscrição taxonômica em Arecaceae. A palmeira híbrida ×Butyagrus nabonnandii é o resultado de cruzamento natural entre Butia odorata e Syagrus romanzoffiana. Objetivou-se verificar se a anatomia foliar pode ajudar na identificação do híbrido, bem como diferenciá-lo dos taxa parentais, ajudando em possíveis dúvidas sobre a identificação taxonômica envolvendo esses três taxa. Amostras da porção mediana de pinas foram coletadas e sujeitas a técnicas usuais para microscopia óptica. Três regiões da pina foram amostradas: margem, região intermediária e nervura mediana. O arranjo das fibras e feixes vasculares foram os principais caracteres considerados. A anatomia da pina provou ser útil na identificação de ×B. nabonnandii, porque mostrou um padrão distinto, demonstrando a importância da anatomia foliar na diferenciação do híbrido dos taxa parentais. A anatomia do híbrido revelou uma combinação de caracteres de ambos os parentais, da mesma maneira como é observado na morfologia externa.

Palavras-chave:
Butia; palmeira híbrida; anatomia vegetal; Syagrus; taxonomia

Introduction

In Brazil, there are 87 genera, 388 species and 18 natural hybrids of Arecaceae, the most of them from interspecific crosses (Lorenzi 2010; Noblick 2010a,b, 2017a; Soares et al. 2023). Although rare, natural hybrids from intergeneric crosses are also observed. The most common intergeneric hybrid among palms originate from Syagrus romanzoffiana (Cham.) Glassman and species belonging to the Butia genus, creating the nothogenus ×Butyagrus Vorster, with three nothospecies recorded to Brazil: ×B. nabonnandii (Prosch.) Vorster, ×B. alegretensis K. Soares, and ×B. paranaensis Engels, T.A. Meyer & K. Soares (Noblick 2010a; Soares et al. 2014a; Engels et al. 2021).

×Butyagrus nabonnandii is the result of a cross between B. odorata (Barb. Rodr.) Noblick and S. romanzoffiana, and it occur in far southern Brazil and in the southeastern region of Uruguay (Noblick 2010a, 2011; Rivas et al. 2017; Oliveira-Neves et al. 2022; Rosa et al. 2023). However, artificially bred specimens of this hybrid have been cultivated in Europe and in the USA since the end of the 19th century (Tournay 2009).

To date, plant morphology has been the only taxonomic tool used to identify Arecaceae hybrids in Brazil, indicated by the presence of intermediate characters of each parental species (Noblick 2012; Soares et al. 2014b; Soares & Assis 2015; Silveira et al. 2022). Regarding ×B. nabonnandii, the external morphology helps identify reproductive specimens, but this tool is not equally efficient for non-reproductive specimens. Furthermore, herbaria vouchers of ×B. nabonnandii are challenging to identify using solely morphology or based on incomplete labels. Such difficulty was also reported by Noblick (2013) for Syagrus, whose pressed and dried specimens appear similar but show characters in the field that are not well preserved on herbarium sheets or not recorded on the labels. However, leaf anatomy is well preserved after the pressing and drying process, even in older samples (see Fig. 3 in Firmo et al. 2021), allowing the differentiation of morphologically similar species not only on a herbarium sheet but also in the field.

In Arecaceae, leaf anatomical studies have helped identify several species and infer systematic relationships within the family (Silva & Potiguara 2008; Sanín & Galeano 2011; Noraini et al. 2012; Martins et al. 2015; Defaveri et al. 2015; Kikuchi et al. 2016; Pinedo et al. 2016; Vianna 2017; Vianna et al. 2017; Silva & Lemos 2020). In Butia and Syagrus, several anatomical studies became prominent along with morphological data to identify and circumscribe species within these two genera (Glassman 1970; Tomlinson et al. 2011; Noblick 2013, 2014, 2017b, 2018; Sant’Anna-Santos et al. 2015, 2018, 2023a,b,c; Sant’Anna-Santos 2021; 2023; Firmo et al. 2021; Noblick & Sant’Anna-Santos 2021).

For instance, the Butia genus was first considered a section of Syagrus by Glassman (1970). Later, he performed a systematic survey of the leaf anatomy in Syagrus (Glassman 1972), which prompted him to reinstate Butia as a valid genus (Glassman 1979) - based on a distinctive pinna anatomy, in which the adaxial and abaxial leaf surfaces and mesophyll are alike (Horn et al. 2009). Therefore, disregarding the polarity of the vascular bundles, the pinna anatomy of Butia is about mirror-image equivalents on cross-sections (Horn et al. 2009). The so-called mirrored mesophyll in the literature is rather uncommon in Arecaceae but is the most striking pinna character to identify the Butia genus (Tomlinson et al. 2011; Noblick 2014; Sant’Anna-Santos et al. 2015; 2018; Noblick & Sant’Anna-Santos 2021; Sant’Anna-Santos 2021, 2023). In Syagrus, the mirrored mesophyll has never been observed (Noblick 2013, 2017a, 2018; Firmo et al. 2021; Sant’Anna-Santos et al. 2023a,b).

Therefore, this study aimed to evaluate whether the leaf anatomy in ×B. nabonnandii can be a valuable tool for identifying the hybrid and differentiating it from its parental species.

Materials and Methods

Specimens of ×B. nabonnandii, B. odorata and S. romanzoffiana were collected in five municipalities of Rio Grande do Sul state: Venâncio Aires, Porto Alegre, Cachoeira do Sul, Manoel Viana and São Vicente do Sul (Fig. 1). Vouchers were deposited in the Bruno Edgar Irgang Herbarium (HBEI) at the Universidade Federal do Pampa (UNIPAMPA). Complete voucher information is available as supplementary material (Tab. S1, available at <https://doi.org/10.6084/m9.figshare.25475860.v1>).

Leaf samples for anatomical analysis were collected from five specimens of B. odorata and S. romanzoffiana at each municipality and a total of 17 specimens of ×B. nabonnandii. The leaf of palms is pseudo-compound and dissected, and in the present work, we adopted the long-established term “pinna” to refer to each unit, following the terminology adopted by Dransfield et al. (2008). For the anatomical data, the pinnae were sampled from the middle of the leaves and sectioned into three portions: leaf margin, midrib portion, and the intermediate region between the former and the latter (Firmo et al. 2021). The previously collected dried samples were subjected to a herborisation reversion process adapted from Meira & Martins (2003), then softened according to Firmo et al. (2021). Next, they were dehydrated and stored in 70% ethyl alcohol. After that, the samples were freehand-sectioned with a disposable razor blade following Firmo et al. (2021). The microscopic features were measured and examined by bright-field microscopy using an Axio Imager A2 microscope (Carl Zeiss, Germany) equipped with Axiocam MRc (Carl Zeiss, Germany) and the ZEN 2 v 4.0 software. The distribution of the three sampled taxa was mapped using QGIS v.3.10.13 (QGIS.org 2020), and municipalities data were taken from IBGE (2018).

The qualitative anatomical characters examined in the present study follow Glassman (1972), Noblick (2013, 2017b), and Noblick & Sant’Anna-Santos (2021). For the pinnae margin and intermediate region, the following characteristics were analysed: (1) vascular bundles with exaggerated fibrous sheath; (2) vascular bundles arrangement and location in the mesophyll; and (3) location and size of non-vascular fibre bundles (henceforth fibre bundles). For the midrib, the following characteristics were analysed: (1) shape; (2) number of collateral bundles; (3) connection to the hypodermis, (4) abaxial projection of the fibrous ring (MFR); (5) accessory bundles partially or completely surrounding the MFR; and (6) expansion tissue. The terminology adopted here for leaf anatomical descriptions follows Noblick (2013, 2017b) for the margin and Glassman (1972), Sant’Anna-Santos et al. (2018) and Firmo et al. (2021) for midrib and intermediate regions. The midrib shapes in cross-section used for Butia and Syagrus - truncate, round and triangular - were here adopted to characterise the midrib of ×B. nabonnandii, B. odorata and S. romanzoffiana (see Glassman 1972; Sant’Anna-Santos et al. 2015, 2018; Firmo et al. 2021; Sant’Anna-Santos 2021, 2023).

Results and Discussion

Intermediate region

Two patterns of arrangement of fibre bundles and vascular bundles were observed in ×B. nabonnandii . The most common is pattern 1, characterised by fibre bundles attached to the adaxial hypodermis, tertiary vascular bundles attached to both surfaces (adaxial and abaxial) and rare minute fibre bundles (Fig. 2a). The pattern 2 is characterised solely by tertiary vascular bundles attached to both surfaces (Fig. 2b), and this pattern was observed only in the population from Venâncio Aires municipality.

Figure 1
Localization of the municipalities where the specimens of ×Butyagrus nabonnandii, Butia odorata and Syagrus romanzoffiana were collected in Rio Grande do Sul state, Brazil.

Figure 2
a-b, e-f. Pinnae anatomy of ×Butyagrus nabonnandii. c, g. Butia odorata. d, h. Syagrus romanzoffiana under light microscopy (cross sections). a-d. intermediate region. e-h. margin. a-b. pattern 1 and 2 of fibre and vascular bundles arrangement, respectively. c. mirrored anatomy. d. non mirrored anatomy. e, g-h. quadrangular shape. f. deltoid shape. (white arrows = tertiary vascular bundles; black arrows = fibre bundles on the adaxial surface; white arrowheads = minute vascular bundles; black circles = fibres on the abaxial surface; black arrowheads = vascular bundle with an exaggerated fibrous sheath in the leaf margin; Fi = fibres; PVB = primary vascular bundle; SVB = secondary vascular bundle; TVB = tertiary vascular bundle). Scale bars = 200 µm.

Currently, 11 species of Syagrus possess different patterns in the pinnae anatomy of intermediate region (Noblick et al . 2014; Noblick 2017b; Sant’Anna-Santos et al . 2023a,b). It could indicate intra-specific variation within a single species or even a complex of several closely related unresolved species (Noblick 2017b).

The vascular arrangement in B. odorata is clearly mirrored because the vascular bundles on the adaxial side are more or less reflected on the abaxial side (Fig. 2c), as shown by Sant’Anna-Santos et al . (2015, 2018) and also observed in other Butia species (Noblick 2014). In specimens of B. odorata studied here, the abaxial surface possesses, near the primary vascular bundles, smaller tertiary vascular bundles, which are not attached to the hypodermis (Fig. 2c), corroborating previous descriptions (see Sant’Anna-Santos et al . 2015, 2018; Noblick & Sant’Anna-Santos 2021).

In Syagrus , the presence and relative abundance of fibre bundles on adaxial and abaxial surfaces were some of the criteria used by Glassman (1972) to separate groups within Syagrus . For example, S. romanzoffiana is characterised by the presence of fibre bundles attached only to the adaxial hypodermis (Glassman 1972; Noblick 2013, 2017b) (Fig. 2d). On the abaxial surface, minute fibre bundles and tertiary vascular bundles are observed in S. romanzoffiana (Fig. 2d) and ×B. nabonnandii also presented the same pattern (Fig. 2a). OtherSyagrus species also presented the same fibre and vascular bundles arrangement on the abaxial surface (Glassman 1972; Noblick 2013, 2017b, 2018; Firmo et al . 2021; Sant’Anna-Santos et al . 2023a,b).

The fibre and vascular bundles arrangement of ×B. nabonnandii in the intermediate region is easily distinguishable from the parental taxa , considering that the two patterns presented by the hybrid are not observed in S. romanzoffiana and neither B. odorata .

Margin

In ×B. nabonnandii , it was observed only one tertiary vascular bundle with exaggerated fibrous sheath in the margin (Fig. 2e-f) and variation in the shape of the margin on cross-sections: quadrangular (Fig. 2e) and deltoid (Fig. 2f).

Butia odorata specimens here analysed showed a quadrangular margin with two tertiary bundles; the abaxial bundle has an exaggerated fibrous sheath compared to the adaxial bundle (Fig. 2g). These results are similar to those found by Sant’Anna-Santos et al . (2018) for B. odorata specimens collected in Tapes municipality (Rio Grande do Sul state, Brazil). Despite this congruence in B. odorata, the margin shape must be used cautiously since Sant’Anna-Santos et al. (2018) demonstrated that it is not a reliable character to distinguish some species of Butia.

Pinnae margin has identified Syagrus species effectively, showing variations in anatomical patterns of some species (Noblick 2013, 2017b; Noblick et al . 2014). Noblick (2013) developed an identification key based solely on anatomical characters of the pinnae margin for acaulescent Syagrus species because morphology alone could not identify certain species complexes. Noblick (2017b) discussed this variation in taxa of wide geographic distribution, such as Syagrus glazioviana Becc., and hypothesised that these differences could either represent intraspecific variation or mean that the species is, in fact, a complex of several closely related unresolved species. However, as shown by Sant’Anna-Santos et al . (2023a, b) in Syagrus cabraliensis (Noblick & Lorenzi) Sant’Anna-Santos and Syagrus carvalhoi B.F. Sant’Anna-Santos, narrow endemics could also show this variation.

In Syagrus romanzoffiana , for example, two margin patterns were observed by Noblick (2017b): the first in specimens collected in Brazil and the second in specimens collected in Paraguay. The S. romanzoffiana specimens studied here are similar to the specimens from Paraguay studied by Noblick (2017b), where the margin has a quadrangular shape and has only a single tertiary bundle with exaggerated fibrous sheath (Fig. 2h). This might be explained by the greater proximity of the collection areas of the present study to the territory of Paraguay. Syagrus romanzoffiana is one of the most widely distributed species in South America and is known to be polymorphic in response to differences in soil and altitude, which has been widely discussed in the literature (for a comprehensive review of this issue, see Noblick 2017a).

Midrib

In ×B. nabonnandii , the midrib is truncate because of the two tips that project outwards (sensu Sant’Anna-Santos et al . 2018), ranging from less (Fig. 3a) to more vertically elongated (Fig. 3b). The main vascular system is composed of 4 to 10 collateral bundles (Fig. 3a-b) and is surrounded by a continuous fibrous ring, projected abaxially and not connected to the abaxial hypodermis. Moreover, accessory vascular bundles around the fibrous ring are present, surrounding it completely (Fig. 3a) or not (Fig. 3b), and at least one has an exaggerated fibrous sheath. Accessory vascular bundles are miniveins, which partially or completely surround the fibrous ring in the midrib (Noblick & Sant’Anna-Santos 2021). In addition, fibre bundles surround the fibrous ring, and they can also be present within the expansion tissue (not shown), as previously shown in Syagrus (see Fig. 4 in Firmo et al . 2021). In Butia , fibre bundles within the expansion tissue have not yet been observed (see Sant’Anna-Santos et al. 2015, 2018; Sant’Anna-Santos 2021, 2023). The expansion tissue is interrupted and is formed by three (Fig. 3a) to four (Fig. 3b) layers of expansion cells.

Butia odorata and S. romanzoffiana midribs present some similarities when compared to ×B. nabonnandii. The main similarities are observed in the midrib: the number of collateral bundles (more than three), continuous fibrous ring and an interrupted expansion tissue (Fig. 3c-d).

Figure 3
a-h. Cross sections of midrib region under light microscopy a-b, e-f. ×Butyagrus nabonnandii. c. Butia odorata. d, g-h. Syagrus romanzoffiana. a-c. accessory bundles around the fibrous ring (white arrowheads); vascular bundles with sheath reiforcement (black arrowheads). a-b, d. nonvascular fibers around the fibrous ring and in the expansion tissue (ET) (black circles). a-d. expansion tissue interrupted (dotted white line); collateral bundles in the main vascular system (white circles). e. Detail of b: nonvascular fiber bundle (fi) and accessory bundle (ab) near the adaxial surface. f. detail of b: fibre bundles (fi) near the expansion tissue. g. detail of d: fibre bundles (fi) near the adaxial surface. h. detail of d: fibre bundles (fi) in the expansion tissue. Scale bars = 100 µm.

Several midrib characteristics have been useful for Butia and Syagrus taxonomy, such as size, shape, expansion tissue and fibrous ring characteristics, vascular bundles around the fibrous ring, and the number of vascular bundles in the main vascular system (see Glassman 1972; Sant’Anna-Santos et al . 2015, 2018, 2023a, b; Firmo et al . 2021; Noblick & Sant’Anna-Santos 2021; Sant’Anna-Santos 2021, 2023). For example, the presence of accessory bundles that completely surround the midrib fibrous ring is one of the main characters distinguishing Butia odorata from Butia capitata (Mart.) Becc. (Sant’Anna-Santos et al. 2015).

In Syagrus , e.g. , Firmo et al . (2021) suggested the existence of a new species from a very isolated mountain in Brazil, based on its geographical isolation associated with morphological and exclusive anatomical characters of the midrib (uniseriate adaxial hypodermis and a fibrous ring reaching the abaxial hypodermis). Recently, this new species was formally described as Syagrus aristeae B.F. Sant’Anna-Santos (Sant’Anna-Santos et al . 2023c).

In B. odorata , fibre bundles around the fibrous ring and within the expansion tissue were absent (Fig. 3c), corroborating with the previously showed by Sant’Anna-Santos et al. (2018). Only accessory bundles surrounding completely the fibrous ring were observed, with two of them showing sclerenchymatic sheath reinforcement in the adaxial surface (Fig. 3c). This last character is an important taxonomic character for Butia as shown by Sant’Anna-Santos et al . (2018). In general, the presence of fibre bundles in the midrib region was not observed in Butia (Sant’Anna-Santos et al . 2015, 2018; Noblick & Sant’Anna-Santos 2021), except in B. buenopolensis B. F. Sant’Anna-Santos (Sant’Anna-Santos 2021).

Regarding S. romanzoffiana , all specimens analysed here presented truncate midrib, and were observed only fibre bundles surrounding completely the fibrous ring and within the expansion tissue (Fig. 3d, 3g-h). In several species of Syagrus , the presence of fibre bundles in the midrib and within the expansion tissue are commonly observed (see Glassman 1972; Firmo et al . 2021; Sant’Anna-Santos 2023a, b, c). However, to our knowledge, this is the first report to S. romanzoffiana with images.

The presence of fibre and accessory vascular bundles in the midrib region of ×B. nabonnandii (Fig. 3e-f), characteristics observed in all specimens sampled, becomes this pinnae region more useful in identifying the hybrid, in comparison with margin and intermediate region.

The comparative description of the anatomical characters from the intermediate region, margin, and midrib of S. romanzoffiana , B. odorata and ×B. nabonnandii are shown in Table 1.

Table 1
Pinnae anatomy differences among ×Butyagrus nabonnandii, Butia odorata and Syagrus romanzoffiana.

Characters	×B. nabonnandii	B. odorata	S. romanzoffiana
Intermediate region
Tertiary vascular bundles on the adaxial surface	Present	Present	Absent
Nonvascular bundles on the adaxial surface	Absent/Present	Absent	Present
Leaf margin
Shape	Deltoid/Quadrangular	Quadrangular	Quadrangular
Number tertiary vascular bundles	1	2	1
Midrib
Accessory vascular bundles completely surrunding the main vascular system	Absent/Present	Present	Absent
Number of accessory bundles with exaggerated fibrous sheath	1-2	2	0
Expansion tissue (ET) estratification	3-4	4	4
Fibers in the hypodermis and ET	Absent/Present	Absent	Present

Pinnae anatomy proved useful in the identification of the hybrid ×Butyagrus nabonnandii and also differentiated it from both parental taxa . In addition to the morphological aspects, the recognition of a hybrid individual in areas where Butia and Syagrus are sympatric, and even specimens deposited in herbaria, can be done using an easy and fast method of leaf anatomy analysis. The pinnae anatomy of the hybrid revealed a combination of characters of both parental taxa, as observed in the external morphology.

Acknowledgements

The authors are thankful to Pró-Reitoria de Pesquisa, Pós-graduação e Inovação (PROPPI, UNIPAMPA), for scientific support; the Laboratório de Anatomia e Biomecânica Vegetal from the Universidade Federal do Paraná (LABV-UFPR); the Núcleo de Estudos da Vegetação Antártica (NEVA-UNIPAMPA), for light microscopy analyses; Luiz Fernando Lima Carvalho from Programa de Pós-graduação em Botânica from UFPR, for support with anatomical techniques; and Matheus Teixeira Martins, for producing the distribution map. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001.

Data availability statement

In accordance with Open Science communication practices, the authors inform that all data are available within the manuscript.

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Edited by

Area Editor:

Dr. João Paulo Basso-Alves

Publication Dates

• Publication in this collection
  29 Apr 2024
• Date of issue
  2024

History

• Received
  12 July 2023
• Accepted
  29 Jan 2024