The Ferns of the Calilegua National Park: a look through their spores. Part I

Abstract

Calilegua National Park is located in the Southeast of the province of Jujuy, Argentina. It is comprised of different districts within the Yungas Biogeographic Province, where conditions are optimal for fern development. The palynological studies with light microscopy in this area are very limited. The aim of this work is to present the morphology of spores from 42 taxa belonging to 9 families of isosporate ferns that grow in this protected area. The study was carried out with herbarium material. The families studied are Anemiaceae, Aspleniaceae, Athyriaceae, Blechnaceae, Cyatheaceae, Cystopteridaceae, Dennstaedtiaceae, Dryopteridaceae, and Equisetaceae. According to the spore aperture type, 35 taxa are monolete, five trilete, and two alete. The spores are yellowish, light to dark brown or brown greenish. The largest spores belong to Anemia australis and the smallest to Asplenium argentinum. Equinate, folded, cristate, alate, reticulate, ridged, psilate, verrucate, and baculate spores were observed. For the first time, the spores of 27 species are illustrated under a light microscope. An identification key of the spores is also provided. The morphological characteristics of the spores allowed for the identification of 23 species, contributing to spore bank analysis, aeropalynological and paleopalynological studies, and taxonomic identifications.

Keywords:
Atlas; Calilegua National Park; Isosporate ferns; Palynology; Spores

Introduction

Calilegua National Park (CNP) is located in the Southeast of the province of Jujuy, Argentina, between 23°27' and 23°56' S latitude and between 64°33' and 65°02' W longitude (Torres et al. 2008). It was established in 1979 and has 76306 hectares that comprise different districts of the Yungas Biogeographic Province (Ganem et al. 2013a). According to Arana et al. (2021), there are 3 districts. The Transition Jungle (elevation: 350-600m) has an annual rainfall record of 700 mm. The Mountain Jungle (elevation: 500-1500m) corresponds to the lower part of the mountain slopes, with rainfall that reaches up to 3000mm per year, an addition to the humidity produced by mists. Lastly, the Montane Forest district (elevation: 1200-2500m) has an annual rainfall of 400mm that is limited to the summer season. The climate in CNP is subtropical mountain with a dry winter season. Average temperatures range from 28 ºC in summer to 17 ºC in winter; absolute maximum records of 40 ºC indicate hot summers (National Parks [Parque Nacional Calilegua], s.f.).

These environmental conditions are optimal for the development of ferns and lycophytes (Ponce et al. 2002) and given that up to 40-50% of the country's species diversity is confined to less than 2% of the Argentine national territory, these environments are of great importance in terms of biodiversity (Arana et al. 2021). Therefore, they have been included by UNESCO within the World Biosphere Reserves (Ganem et al. 2013a).

Given the disturbance of practically all known ecosystems, due to physiognomic changes in the landscape from human activity, Torres et al. (2008) affirm that it is very important to increase knowledge about biodiversity. As a result, it has become evident in recent years that it is necessary to carry out surveys in order to know what there is, with the purpose of implementing tasks for conservation. In this sense, some taxa that grow in the CNP and are endemic to the Yungas have been classified as threatened by Giudice et al. (2011), such as Alsophila odonelliana (Cyatheaceae), Asplenium argentinum (Aspleniaceae), Austroblechnum squamipes, Lomariocycas moritziana (=Lomariocycas yungensis) (Blechnaceae), Diplazium lilloi (Athyriaceae), and Elaphoglossum crassipes (Dryopteridaceae).

The following palynological atlases offer a great reference for paleopalynological, aeropalynological, and forensic studies, among others (Farfán-Santillán et al. 2016). For the Neotropics, the studies carried out by Heusser (1971) in Chile, Contreras-Duarte et al. (2006) in Colombia, Coelho and Esteves (2008) and Lebrão et al. (2014) in Brazil, and Gorrer et al. (2021) and Di Pasquo et al. (2016) for Argentina, are of importance.

According to Ganem et al. (2013a), there have been numerous floristic and survey studies carried out in CNP, although palynological studies are relatively limited. The studies that focus on the palynology of ferns from Northwest Argentina (NWA) focus on genera or families and were mostly performed using scanning electron microscopy (SEM) (Morbelli & Giudice 2005; Marquez et al. 2009; Ramos Giacosa et al. 2009; 2012; Ganem et al. 2013b). However, in these studies, the spores were not described nor illustrated using a light microscope (LM).

For Argentina, Zuloaga et al. (2019) cite 397 fern taxa, while for CNP, 100 taxa are cited (Ganem et al. 2013a; 2014; 2016; Arana et al. 2016; 2017; Jaimez & Martínez 2016). The spores of about 40 of these taxa have been illustrated using SEM in the previously mentioned works and only about 25 with LM (Contreras-Duarte et al. 2006; Coelho & Esteves 2008; Gómez-Noguez et al. 2013; Gorrer et al. 2021). Therefore, of the fern spores that inhabit CNP, approximately 60% and 75% have not yet been illustrated using SEM and LM, respectively.

The aim of this work is to provide the spore morphology of 42 taxa belonging to nine isosporate ferns families that grow in the CNP, mainly through LM analysis, as a contribution to aeropalynological, paleopalynological, and systematic studies of Neotropical ferns.

Materials and methods

The families studied are Anemiaceae, Aspleniaceae, Athyriaceae, Blechnaceae, Cyatheaceae, Cystopteridaceae, Dennstaedtiaceae, Dryopteridaceae and Equisetaceae.

The study was carried out with herbarium material from the following Argentine institutions: LP, JUA, LIL, MCNS, RCV and SI (Thiers 2022) (Table 1). When specimens from the CNP area were found to be infertile or with insufficient numbers of spores, herbarium specimens from other locations were selected. Material of only three species could not be obtained: Megalastrum ciliatum M. Kessler & A.R. Sm., Elaphoglossum lorentzii (Hieron.) H. Christ (Dryopteridaceae) and Diplazium divergens Rosenst. (Athyriaceae).

Table 1
Material studied. COL AND N. C.: collector and number collection; HERB.: herbaria.

FAMILY	TAXA	COL. AND N.C.	HERB.	ORIGIN
Anemiaceae	Anemia australis (Mickel) M. Kessler & A.R. Sm.	Larsen & Arana 134	SI	Jujuy, PN Calilegua, Descendiendo desde el Monolito hacia Mesada de las Colmenas, 23°40'58''S-64°54'04''W, 1720 snmn
Anemiaceae	Anemia herzogii Rosenst.	Ramos Giacosa et al. 36	LP	Jujuy, PN Calilegua, Sendero Tataupá
Anemiaceae	Anemia phyllitidis var. phyllitidis (L.) Sw.	Ramos Giacosa 117	LP	Jujuy, PN Calilegua, Mesada de las Colmenas, Sendero de la Cascada, 1100 msnm
Aspleniaceae	Asplenium argentinum Hieron.	Ramos Giacosa et al. 49	LP	Jujuy, PN Calilegua, Sendero Tataupá
Aspleniaceae	Asplenium auritum Sw.	Larsen & Arana 130	RCV	Jujuy, PN Calilegua, Sendero que une el camino principal con Arroyo El Negrito (Sendero 4), 23°44'20''S-64°51'14''W, 758 msnm
Aspleniaceae	Asplenium claussenii Hieron.	Ganem et al. 17	LP	Jujuy, PN Calilegua, Zona pozos de petróleo, yacimiento El Caimancito
Aspleniaceae	Asplenium cuspidatum Lam.	Ganem et al. 29	LP	Jujuy, PN Calilegua, Camino a Mesada de las Colmenas
Aspleniaceae	Asplenium gilliesii Hook.	Fabris 6968	LP	Jujuy, Valle Grande, Finca Pozuelos, a 6 km de Caspalá
Aspleniaceae	Asplenium harpeodes Kunze	Ganem 223	JUA	Jujuy, PN calilegua, Ledesma
Aspleniaceae	Asplenium inaequilaterale Willd.	Ramos Giacosa et al. 125	LP	Jujuy, PN Calilegua, Camino de Abra de las Cañas a Mesada de las Colmenas, 23°41'S-64°54'W, 1650 msnm
Aspleniaceae	Asplenium lorentzii Hieron.	Ganem et al. 32	LP	Jujuy, PN Calilegua, Camino a Mesada de las Colmenas
Aspleniaceae	Asplenium monanthes L.	Fabris, Crisci & Petriella 5933	LP	Jujuy, PN Calilegua, Serranía de Calilegua, Tolditos
Aspleniaceae	Asplenium serra Langsd. & Fisch.	Larsen & Arana 155	SI	Jujuy, PN Calilegua, Aguada de Tigre, 23°41'03''S-64°53'40''W, 1630 msnm
Aspleniaceae	Asplenium squamosum L.	Ganem et al. 31	LP	Jujuy, PN Calilegua, Camino a Mesada de las Colmenas
Athyriaceae	Diplazium cristatum (Desr.) Alston	Ahumada 7158 b	JUA	Jujuy, PN calilegua, Ledesma
Athyriaceae	Diplazium lilloi (Hicken) R.M. Tryon & A.F. Tryon	Ganem et al. 38	LP	Jujuy, PN Calilegua, Camino a Mesada de las Colmenas
Blechnaceae	Austroblechnum squamipes (Hieron.) Gasper & V.A.O. Dittrich	Ramos Giacosa et al. 37	LP	Jujuy, PN Calilegua, Aguada de Tigre
Blechnaceae	Blecnhum laevigatum Cav.	Zuloaga et al. 7548	LP	Jujuy, PN Calilegua, 1100 msnm
Blechnaceae	Blechnum occidentale L.	Ramos Giacosa 104	LP	Jujuy, PN Calilegua, Camino de Aguas Negras a Mesada de las Colmenas, 23°41'S-64°52'W, 1100 msnm
Blechnaceae	Cranfilia caudata (Baker) V.A.O. Dittrich & Gasper	Meyer 14034	LIL	Tucumán, Chicligasta, entre Puesto Las Pavas y Saladillo, 1000 m
Blechnaceae	Lomariocycas moritziana (Klotzsch) Gabriel y Galán & Vicent	Ramos Giacosa et al. 60	LP	Jujuy, PN Calilegua, Camino hacia Abra de las Cañas
Blechnaceae	Parablechnum cordatum (Desv.) Gasper & Salino	Ramos Giacosa et al. 45	LP	Jujuy, PN Calilegua, Camino hacia Abra de las Cañas
Cyatheaceae	Alsophila odonelliana (Alston) Lehnert	Vervoorst 440	LIL	Salta, Orán, A° El Negrito, afluente de Río Santa María, 846 msnm
Cystopteridaceae	Cystopteris diaphana (Bory) Blasdell	Larsen & Arana 142	RCV	Jujuy, PN Calilegua, Camino desde Monolito hacia Mesada de las Colmenas, 23°40'58''S-64°54'04''W, 1720 msnm
Dennstaedtiaceae	Mucura globulifera (Poir.) L.A. Triana & Sundue	Ganem et al. 14	LP	Jujuy, PN Calilegua, Zona pozos de petróleo, yacimiento El Caimancito
Dennstaedtiaceae	Hypolepis poeppigii (Kunze) R. Rodr.	Larsen & Arana 147	SI	Jujuy, PN Calilegua, Camino desde Monolito hacia Mesada de las Colmenas, 23°41'08''S-64°53'47''W, 1616 msnm
Dryopteridaceae	Bolbitis serratifolia (Mert. ex Kaulf.) Schott	Ramos Giacosa et al. 18	LP	Jujuy, PN Calilegua, Sendero Guaraní
Dryopteridaceae	Ctenitis submarginalis (Langsd. & Fisch.) Ching	Capurro 229	LIL	Jujuy, PN Calilegua
Dryopteridaceae	Dryopteris patula (Sw.) Underw.	Larsen & Arana 146	RCV	Jujuy, PN Calilegua,Camino desde Monolito hacia Mesada de las Colmenas, 23°41'08''S-64°53'47''W, 1616 msnm
Dryopteridaceae	Dryopteris wallichiana (Spreng.) Hyl.	Ganem et al. 36	LP	Jujuy, PN Calilegua, Camino desde Monolito hacia Mesada de las Colmenas
Dryopteridaceae	Elaphoglossum crassipes (Hieron.) Diels	Ramos Giacosa et al. 67	LP	Jujuy, PN Calilegua,Aguada de Tigre
Dryopteridaceae	Elaphoglossum gayanum (Fée) T. Moore	Legname y Cuezzo 5932 c	LIL	Jujuy, Ledesma, RP n°3 camino a Valle Grande (10 km antes del Río Jordán)
Dryopteridaceae	Elaphoglossum hybridum (Bory) Brack.	Larsen & Arana 149	SI	Jujuy, PN Calilegua, Camino desde Monolito hacia Mesada de las Colmenas, 23°41'08''S-64°53'47''W, 1616 msnm
Dryopteridaceae	Elaphoglossum sellowianum (Klotzsch ex Kuhn) T. Moore	Ganem et al. 43	LP	Jujuy, PN Calilegua, Aguada de Tigre
Dryopteridaceae	Elaphoglossum spathulatum (Bory) T. Moore	Ganem et al. 38	LP	Jujuy, PN Calilegua, Camino a Mesada de las Colmenas
Dryopteridaceae	Elaphoglossum yungense de la Sota	Guantay 8	LIL	Tucumán, Chicligasta, La Banderita
Dryopteridaceae	Megalastrum adenopteris (C. Chr.) A.R. Sm. & R.C. Moran	Tolaba, Arentsen, Juárez & Acuña 5005	JUA	Jujuy, PN Calilegua, Área afectada a Yacimiento petrolífero Caimancito, próximo a Serranías de Socabón, 15-20 km NW Caimancito, 589 m, 23°38'28,3'' S 64°36'48,9'' W
Dryopteridaceae	Megalastrum fugaceum R.C. Moran, J. Prado & Sundue	Sleumer 2097	MCNS	Jujuy, PN Calilegua, Aguada de Tigre, RP83, 1600 msnm
Dryopteridaceae	Polystichum montevidense (Spreng.) Rosenst.	Ganem et al. 37	LP	Jujuy, PN Calilegua, Camino a Mesada de las Colmenas
Dryopteridaceae	Polystichum platyphyllum var. platyphyllum (Willd.) C. Presl	Ramos Giacosa et al. 43	LP	Jujuy, PN Calilegua, Sendero El Negrito
Equisetaceae	Equisetum bogotense Kunth	Rotman 727	JUA	Jujuy, PN calilegua, Ledesma
Equisetaceae	Equisetum giganteum L.	Filipovich 340	LIL	Salta, Rosario de Lerma, Campo Quijano, 1588 msnm

The spores were studied with LM and after the analysis with LM five species were selected as representative for the study with SEM.

For the analysis with LM, the material was acetolized according to the method of Erdtman (1960). For the study with SEM, the spores without treatment were placed into stubs with adhesive double-faced tape and coated with gold.

The observations were made with a Leica DM500 with Leica ICC50 digital camera incorporated from Laboratorio de Palinología, Facultad de Ciencias Agrarias, Universidad Nacional de Jujuy and with SUPRA 55VP SEM from Centro Integral de Microscopía Electrónica (CONICET- UNT).

The characteristics analyzed were: color, shape, equatorial and polar diameters, laesura length and ornamentation. The measurements of the spores were estimated on 20 spores in each sample.

The terminology proposed by Punt et al. (2007) and Tryon and Lugardon (1991) was used for the descriptions of the spores.

Results

Measurements of the spores are given in Table 2.

Table 2
Spore measurements. Dimensions in µm. MAED: Major Equatorial Diameter; MIED: Minor Equatorial Diameter; PD: Polar Diameter; LL: Laesura Length.

TAXA	MAED	MIED	PD	LL
Alsophila odonelliana	38 - 48	40 - 47	30 - 36	16 - 25
Anemia australis	76 - 91	70 - 91	65 - 77	28 - 42
Anemia herzogii	53 - 67	53 - 70	49 - 57	14 - 26
Anemia phyllitidis var. phyllitidis	54 - 74	56 - 70	49 - 65	17 - 28
Asplenium argentinum	28 - 35	21 - 29	23 - 33	11 - 21
Asplenium auritum	39 - 56	26 - 35	26 - 35	14 - 33
Asplenium claussenii	35 - 46	21 - 35	25 - 35	14 - 35
Asplenium cuspidatum	37 - 53	25 - 39	28 - 35	25 - 28
Asplenium gilliesii	31 - 42	25 - 33	25 - 32	17 - 34
Asplenium harpeodes	29 - 41	25 - 32	22 - 32	15 - 24
Asplenium inaequilaterale	32 - 46	23 - 35	23 - 35	18 - 35
Asplenium lorentzii	28 - 35	25 - 32	23 - 32	11- 25
Asplenium monanthes	37 - 53	33 - 42	28 - 42	21 - 32
Asplenium serra	28 - 49	28 - 35	28 - 42	12 - 18
Asplenium squamosum	39 - 53	32 - 48	26 - 46	21 - 35
Austroblechnum squamipes	35 - 42	28 - 35	30 - 36	21 - 35
Blechnum laevigatum	35 - 42	23 - 30	25 - 31	21 - 32
Blechnum occidentale	35 - 49	25 - 32	25 - 33	18 - 32
Bolbitis serratifolia	30 - 46	25 - 39	22 - 35	23 - 28
Cranfilia caudata	33 - 42	24 - 32	24 - 31	25 - 34
Ctenitis submarginalis	28 - 49	24 - 43	21 - 44	11 - 43
Cystopteris diaphana	39 - 49	25 - 35	28 - 35	14 - 25
Diplazium cristatum	43 - 54	33 - 47	27 - 43	20 - 35
Diplazium lilloi	49 - 74	39 - 61	40 - 53	23 - 42
Dryopteris patula	40 - 54	28 - 40	30 - 40	18 - 32
Dryopteris wallichiana	39 - 57	27 - 37	29 - 39	22 - 36
Elaphoglossum crassipes	35 - 47	35 - 39	30 - 39	18 - 35
Elaphoglossum gayanum	43 - 58	33 - 44	32 - 43	24 - 34
Elaphoglossum hybridum	35 - 40	27 - 35	23 - 32	18 - 26
Elaphoglossum sellowianum	35 - 46	30 - 39	27 - 34	25 - 34
Elaphoglossum spathulatum	42 - 63	35 - 49	35 - 49	21 - 35
Elaphoglossum yungense	37 - 52	32 - 42	24 - 41	25 - 35
Equisetum bogotense	26 - 38
Equisetum giganteum	45 - 53
Hypolepis poeppigii	44 - 52	26 - 33	28 - 35	14 - 28
Lomariocycas moritziana	49 - 70	35 - 49	37 - 56	32 - 46
Megalastrum adenopteris	45 - 64	26 - 43	29 - 40	25 - 45
Megalastrum fugaceum	27 - 34	20 - 25	22 - 27	12 - 20
Mucura globulifera	32 - 40	32 - 42	21 - 28	11 - 14
Parablechnum cordatum	30 - 41	21 - 36	21 - 30	21 - 33
Polystichum montevidense	34 - 48	25 - 38	26 - 38	14 - 30
Polystichum platyphyllum var. platyphyllum	28 - 46	26 - 35	27 - 38	16 - 24

Descriptions of the spores

ANEMIACEAE

Anemia australis: Fig. 1A-C

Figure 1
A-C: Anemia australis. Ridged with echinulate surface. D-F: Anemia herzogii. Ridged with baculae. G-I: Anemia phyllitidis var. phyllitidis. Ridged with baculae. J-L: Asplenium argentinum. Alate-folded with short folds and echinulate margin. M-O: Asplenium auritum. Alate-folded with long folds and smooth margin. P-R: Asplenium claussenii. Alate-folded with long folds and echinulate margin. S-U: Asplenium cuspidatum. Alate-folded with long folds and smooth margin. V-X: Asplenium gilliesii. Alate-folded with short folds and echinulate margin. Scale bar: 10 µm.

Aperture: trilete; Color: brown; Shape in equatorial view: Convex/hemisferic; Amb: Triangular, convex sides and prominent angles; Ornamentation: Parallel ridges separated by narrow grooves, echinulate surface.

Anemia herzogii: Fig. 1D-F

Aperture: trilete; Color: Light brown; Shape in equatorial view: Plane-convex/convex; Amb: Subglobose to triangular, convex sides and and rounded angles; Ornamentation: Parallel and narrow ridges with high bacula, separated by wide grooves.

Anemia phyllitidis var. phyllitidis: Fig. 1G-I

Aperture: trilete; Color: Light brown; Shape in equatorial view: Plane-convex/convex; Amb: Subglobose to triangular, convex sides and and rounded angles; Ornamentation: Parallel and narrow ridges with high bacula, separated by wide grooves.

ASPLENIACEAE

Asplenium argentinum: Fig. 1J-L

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal/subcircular; Ornamentation: Alate-folded, short folds, echinulate margin, surface perforated between and on folds.

Asplenium auritum: Fig. 1M-O

Aperture: monolete; Color: dark brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Alate-folded, long folds, smooth margin, surface perforated between folds.

Asplenium claussenii: Fig. 1P-R

Aperture: monolete; Color: light brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Alate-folded, long folds, echinulate margin, surface perforated between folds.

Asplenium cuspidatum: Fig. 1S-U

Aperture: monolete; Color: dark brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Alate-folded, long folds, smooth margin, surface perforated between folds.

Asplenium gilliesii:Fig. 1V-X

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal/subcircular; Ornamentation: Alate-folded, short folds, echinulate margin, surface perforated between and on folds.

Asplenium harpeodes: Fig. 2A-C

Figure 2
A-C: Asplenium harpeodes. Alate-folded with short folds and echinulate margin. D-F: Asplenium inaequilaterale. Alate-folded with long folds and echinulate margin. G-I: Asplenium lorentzii. Alate-folded with short folds and echinulate margin. J-L: Asplenium monanthes. Alate-folded with long folds and echinulate margin. M-O: Asplenium serra. Reticulate mesh supported by spines or baculae. P-R: Asplenium squamosum. Alate-folded with long folds and echinulate margin. S-U: Diplazium cristatum. Alate-folded. V-X: Diplazium lilloi. Alate-folded. Scale bar: 10 µm.

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal/subcircular; Ornamentation: Alate-folded, short folds, echinulate margin, surface perforated between and on folds.

Asplenium inaequilaterale: Fig. 2D-F

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Alate-folded, long folds, echinulate margin, surface perforated between folds.

Asplenium lorentzii: Fig. 2G-I; 7A-C

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal/subcircular; Ornamentation: Alate-folded, short folds, echinulate margin, surface perforated between and on folds.

Asplenium monanthes: Fig. 2J-L

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Alate-folded, long folds, echinulate margin, surface perforated between folds.

Asplenium serra: Fig. 2M-O

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Reticulate mesh supported by spines or bacula.

Asplenium squamosum: Fig. 2P-R

Aperture: monolete; Color: light brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal/subcircular; Ornamentation: Alate-folded, long folds, echinulate margin, surface perforated between folds.

ATHYRIACEAE

Diplazium cristatum: Fig. 2S-U; 7D-E

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal/subcircular; Ornamentation: Alate-folded.

Diplazium lilloi: Fig. 2V-X

Aperture: monolete; Color: light brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal/subcircular; Ornamentation: Alate-folded.

BLECHNACEAE

Austroblechnum squamipes:Fig. 3A-C

Figure 3
A-C: Austroblechnum squamipes. Psilate. D-F: Blechnum laevigatum. Psilate. G-I: Blechnum occidentale. Psilate. J-L: Cranfillia caudata. Folded. M-O: Lomariocycas moritziana. Folded, with narrow and low folds. P-R: Parablechnum cordatum. Folded. S-U: Alsophila odonelliana. Cristate. V-X: Cystopteris diaphana. Echinate. Scale bar: 10 µm.

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal; Ornamentation: psilate.

Blechnum laevigatum: Fig. 3D-F

Aperture: monolete; Color: Light brown; Shape in equatorial view: Concave/convex; Amb: Oblong to ellipsoidal; Ornamentation: psilate.

Blechnum occidentale: Fig. 3G-I

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsiodal; Ornamentation: psilate.

Cranfillia caudata: Fig. 3J-L

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: folded.

Lomariocycas moritziana: Fig. 3M-O

Aperture: monolete; Color: light brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: folded, narrow and low folds.

Parablechnum cordatum: Fig. 3P-R

Aperture: monolete; Color: brown/dark brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: folded.

CYATHEACEAE

Alsophilla odonelliana: Fig. 3S-U

Aperture: trilete; Color: yellow; Shape in equatorial view: Conic-convex/convex; Amb: Triangular, concave to straight sides and rounded angles; Ornamentation: cristate.

CYSTOPTERIDACEAE

Cystopteris diaphana: Fig. 3V-X

Aperture: monolete; Color: dark brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: echinate.

DENNSTAEDTIACEAE

Mucura globulifera: Fig. 4A-C

Figure 4
A-C: Mucura globulifera. Verrucate-reticulate. D-F: Hypolepis poeppigii. Baculate-cristate. G-I: Bolbitis serratifolia. Folded. J-L: Ctenitis submarginalis. Folded, with short and subglobose folds. M-O: Dryopteris patula. Folded, coarse folds fusionated partially. P-R: Dryopteris wallichiana. Folded, narrow folds fusionated partially. S-U: Elaphoglossum crassipes. Folded, narrow folds fusionated partially. V-X: Elaphoglossum gayanum. Folded, narrow echinulate surface. Scale bar: 10 µm.

Aperture: trilete; Color: brown; Shape in equatorial view: plane/convex; Amb: Triangular, concave sides and rounded angles; Ornamentation: Verrucate-reticulate.

Hypolepis poeppigii: Fig. 4D-F; 7I-K

Aperture: monolete; Color: yellowish; Shape in equatorial view: plane/convex; Amb: ellipsoidal; Ornamentation: Baculate-cristate.

DRYOPTERIDACEAE

Bolbitis serratifolia: Fig. 4G-I

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/hemisferic; Amb: globose; Ornamentation: folded.

Ctenitis submarginalis: Fig. 4J-L

Aperture: monolete; Color: light brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: folded, short and subglobose folds.

Dryopteris patula: Fig. 4M-O

Aperture: monolete; Color: dark brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal; Ornamentation: Folded, coarse folds fusionated partially.

Dryopteris wallichiana: Fig. 4P-R

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal; Ornamentation: Folded, narrow folds fusionated partially.

Elaphoglossum crassipes: Fig. 4S-U

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal; Ornamentation: Folded, narrow folds fusionated partially.

Elaphoglossum gayanum: Fig. 4V-X

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal; Ornamentation: Folded, narrow echinulate surface.

Elaphoglossum hybridum: Fig. 5A-C

Figure 5
A-C: Elaphoglossum hybridum. Folded, narrow folds fusionated partially. D-F: Elaphoglossum sellowianum. Folded, narrow folds fusionated partially. G-I: Elaphoglossum spathulatum. Folded, narrow folds echinulate surface. J-L: Elaphoglossum yungense. Folded, narrow folds fusionated partially. Scale bar: 10 µm.

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal; Ornamentation: Folded, narrow folds fusionated partially.

Elaphoglossum sellowianum:Fig. 5D-F; 7F-H

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal; Ornamentation: Folded, narrow folds fusionated partially.

Elaphoglossum spathulatum: Fig. 5G-I

Aperture: monolete; Color: dark brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal/subcircular; Ornamentation: Folded, narrow echinulate surface.

Elaphoglossum yungense: Fig. 5J-L

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: Ellipsoidal/subcircular; Ornamentation: Folded, narrow folds fusionated partially.

Megalastrum adenopteris: Fig. 6A-C; 7L-N

Figure 6
A-C: Megalastrum adenopteris. Folded, reticulate surface. D-F: Megalastrum fugaceum. Echinate. G-I: Polystichum montevidense. Alate-folded, echinulate surface. J-L: Polystichum platyphyllum var. platyphyllum. Folded, short and subglobose folds. M-N: Equisetum bogotense. Psilate with elaters. O-P: Equisetum giganteum. Psilate with elaters. Scale bar: 10 µm.

Figure 7
A-C: Asplenium lorentzii. A) Proximal view. B) Ecuatorial view. C) Perispore surface. The arrowheads show echinulae and the arrows the perforations. D-E: Diplazium cristatum. D) Equatorial view. E) Perispore surface. The arrowheads show echinulae. F-H: Elaphoglossum sellowianum. F) Distal view. G) Proximal view. H) Perispore surface. The arrows show echinulae. I-K: Hypolepis poeppigii. I) Equatorial view. J) Proximal view. K) Perispore surface. The arrowead show bacula. The baculae is formed by threads (arrows). The ellipse shows crest. L-N: Megalastrum adenopteris. L) Equatorial view. M) Proximal view. N) Perispore surface. Perforation-like opening formed by the dense reticulum (arrows).Scale bar: A-B, D, F-G, I-J, L-M: 10 µm; E, H, K, N: 2 µm; C: 0.2 µm.

Aperture: monolete; Color: brown; Shape in equatorial view: Plane-concave/convex; Amb: ellipsoidal; Ornamentation: Folded, reticulate surface.

Megalastrum fugaceum: Fig. 6D-F

Aperture: monolete; Color: light brown; Shape in equatorial view: Plane/convex; Amb: Oblong; Ornamentation: echinate.

Polystichum montevidense: Fig. 6G-I

Aperture: monolete; Color: dark brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Alate-folded, echinulate surface.

Polystichum platyphyllum var. Platyphyllum: Fig. 6J-L

Aperture: monolete; Color: brown; Shape in equatorial view: Plane/convex; Amb: ellipsoidal; Ornamentation: Folded, short and subglobose folds.

EQUISETACEAE

Equisetum bogotense: Fig. 6M-N

Aperture: alete; Color: brown greenish; Shape in equatorial view: globose; Amb: globose; Ornamentation: Psilate with elaters.

Equisetum giganteum: Fig. 6O-P

Aperture: alete; Color: brown greenish; Shape in equatorial view: globose; Amb: globose; Ornamentation: Psilate with elaters.

Spore identification key

1. Alete spores, with elaters …………………. 2

1’. Monolete or trilete spores, without elaters …………………. 3

2. Spores smaller than 40 µm …………………. Equisetum bogotense

2’. Spores larger than 40 µm …………………. Equisetum giganteum

3. Trilete spores …………………. 4

3’. Monolete spores …………………. 7

4. Parallel and wide ridges separated by narrow grooves …………………. 5

4’. Verrucae or narrow cristae …………………. 6

5. Ridges with echinulate surface, without baculae …………………. Anemia australis

5’. Parallel and narrow ridges with high baculae …………………. Anemia herzogii/Anemia phyllitidis

6. Cristate and yellowish spores …………………. Alsophila odonelliana

6’. Verrucate and brownish spores …………………. Mucura globulifera

7. Echinate, baculate or psilate spores …………………. 8

7’. Folded or reticulate spores …………………. 12

8. Psilate ornamentation …………………. 9

8’. Echinate or baculate ornamentation …………………. 10

9. Light brown spores …………………. Blechnum laevigatum

9’. Dark brown spores …………………. Austroblechnum squamipes/Blechnum occidentale

10. Ornamentation formed by baculae that can fuse and form short ridges, spores yellowish …………………. Hypolepis poeppigii

10’. Ornamentation formed by echinae that cannot fuse, spores brown …………………. 11

11. Light brown spores, MAED up to 34 µm …………………. Megalastrum fugaceum

11’. Dark brown spores, MAED greater than 39 µm …………………. Cystopteris diaphana

12. Reticulate mesh supported by spines or bacula, spores brown …………………. Asplenium serra

12’. Folded ornamentation …………………. 13

13. Short, subglobose and inflated folds …………………. 14

13’. Alate or narrow folds, never inflated or subglobose folds …………………. 15

14. Light brown spores …………………. Ctenitis submarginalis

14’. Brown to dark brown spores …………………. Polystichum platyphyllum var. platyphyllum

15. Alate folds with perforations between and on folds …………………. 16

15’. Other type of folds without perforations …………………. 19

16. Short folds with echinulate margin …………………. Asplenium argentinum/ Asplenium gilliesii/ Asplenium harpeodes/ Asplenium lorentzii

16’. Long folds, with echinulate or smooth margin …………………. 17

17. Echinulate margin …………………. 18

17’. Smooth margin, MAED can exceed 50 µm …………………. Asplenium auritum/Asplenium cuspidatum

18. Light brown spores …………………. Asplenium inaequilaterale/ Asplenium claussenii/ Asplenium squamosum

18’. Brown to dark brown spores …………………. Asplenium monanthes

19. Folds with echinulate surface …………………. 20

19’. Folds without echinulate surface …………………. 22

20. Light brown spores …………………. Elaphoglossum gayanum/ Diplazium cristatum

20’. Dark brown spores …………………. 21

21. High and narrow folds, alated type, with MAED 34-48 µm …………………. Polystichum montevidense

21’. Low and narrow folds, not alated type, with MAED 42-63 µm …………………. Elaphoglossum spathulatum

22. Folds full fused to form complete reticles …………………. 23

22’. Folds partially fused without forming complete reticles …………………. 24

23. Heterobrochate reticles, with small brochi or lumina of different sizes …………………. Megalastrum adenopteris

23’. Homobrochate reticles, with big brochi or lumina of similar sizes …………………. Parablechnum cordatum

24. Coarse and wide folds, dark brown spores …………………. Dryopteris patula

24’. Folds never coarse and wide, brown to light brown spores …………………. 25

25. High and compressed folds, notoriously alate type, up to 10 µm high …………………. Diplazium lilloi

25’. Narrow and low folds, if high they never exceed 7 µm …………………. Bolbitis serratifolia/ Cranfillia caudata/ Dryopteris wallichiana/ Elaphoglossum crassipes/ Elaphoglossum hybridum/ Elaphoglossum sellowianum/ Elaphoglossum yungense/ Lomariocycas moritziana

Discussion

ANEMIACEAE

The ornamentation observed here for the genus Anemia is the same that Ramos Giacosa et al. (2012) observed. These authors analyzed the same three species that we analyzed here but they did not illustrate them with LM. The only difference found is in the longer size of equatorial diameter of A. phyllitidis var. phyllitidis (42-55 vs. 54-74µm). The authors cited material from Jujuy (Yungas Biogeographic Province) but also from Misiones (Paranaense Biogeographic Province), so the difference could be due to this geographical disjunction.

ASPLENIACEAE

Ganem (2018) and Ganem et al. (2013b; 2014) analyzed and illustrated with SEM the spores of Asplenium from Argentina. They recognized a folded perispore with variability in the density of perforations and the margin of the folds that may be smooth, jagged, or echinulate. We agree with the authors that the spores of the genus present a folded perispore and that the folds are alate type, except A. serra wich has a reticulate perispore. However, regarding the margin of the folds, we did not make a difference between jagged or echinulate, since the LM magnification (1000x) did not allow us to differentiate between teeth and echinulae.

Regarding the relationship between the perispore and the size of the plants, in this study it is observed that the epiphytic species present particular spores, dark brown in color with long folds and a smooth margin (A. auritum and A. cuspidatum) or reticulated mesh (A. serra), which agrees with Ganem (2018).

ATHYRIACEAE

Spores of Diplazium species growing in Argentina have not been illustrated with LM or SEM until now. Other American species have been analyzed with SEM by Tryon and Lugardon (1991) and those analyzed by these authors presented a minimum size of the MAED 16 µm smaller than those analized here. However, the ornamentation of D. lilloi and D. cristatum described here coincides with what was mentioned by these authors, in which they have prominent wing-like folds.

BLECHNACEAE

Melo da Silva et al. (2019) illustrated A. squamipes from Brazil with LM and SEM. They describe it with psilate ornamentation, just as we have observed it here.

L. moritziana from Jujuy was illustrated with SEM and LM by Ramos Giacosa (2019). He affirms that the spores of this species present a folded ornamentation, and the folds partially merge, forming an incomplete reticle. Here we observe that the spores present low and narrow rugulate folds, which can fuse patially, as mentioned this author. An even more noticeable difference with the spores analyzed by Ramos Giacosa (2019) is that ours presented a MAED up to 25 µm lower (49-70 vs. 82-95µm). This variation could be due to hybridization and polyploidy issues, which are very recurrent throughout the family, and do not provide a useful tool to differentiate subfamilies or genera, much less at a specific level (Melo da Silva et al. 2021).

According to Melo da Silva et al. (2019) the Brazilian specimens of Cranfillia caudata have narrow and smooth ridges that form thin reticles. Passarelli et al. (2010) described Argentinian specimens of C. caudata (= Blechnum sprucei) with a folded perispore. Here it has been observed that have very low rugulae, even almost imperceptible, but there are no ridges or folds that could form reticles. The closest thing to what we observed is what Ramos Giacosa et al. (2009), where with SEM they illustrate spores that have a few folds and a smoothly rugulate surface.

Parablechnum cordatum (= Blechnum cordatum) was illustrated by Ramos Giacosa et al. (2009) with SEM and by Melo da Silva et al. (2019) with SEM and LM. The spores analyzed here do not agree with the description mentioned by these authors, probably due to a failure in the acetolysis. Spores of various colors were found with the same degree of maturation and without evidence of folds, but of very low rugulas, barely perceptible. Although in the equatorial view a supralesural fold can be seen, as affirm Contreras-Duarte et al. (2006).

CYATHEACEAE

The type of ornamentation and the measurements of A. odonelliana found here are similar to those described by Marquez et al. (2009), with large and parallel ridges. In addition, these authors affirm that the edges of the crests are echinulate. We could not observe the latter, since we used LM and they used SEM.

CYSTOPTERIDACEAE

Arana and Mynssen (2015) illustrated with SEM the spores of C. diaphana with material from Brazil. In agreement with the authors, the spores analyzed here, with Argentine material, the sculpture and the color are the same, echinate and dark brown.

DENNSTAEDTIACEAE

Martínez et al. (2014) illustrated with SEM the spores of Hypolepis poeppigii and Mucura globulifera. They say that the spores of first species have echinae that are partially fused; while the second has verrucae. Yañez (2015) observed that the spores of M. globulifera seen with LM present verrucae that partially merge. These fused verrucae give a darker appearance compared to verrucae that are not fused. The same characteristic has been observed in the photos illustrated by us. The small differences in size (between 5-11μm) could be due to a geographical disjunction since the measurements were taken based on samples from different phytogeographic provinces.

As for the spores of H. poeppigii observed here, they present baculae that can fuse laterally forming short ridges, unlike what was observed by Martínez et al. (2014). In our SEM illustrations, the baculae are formed by cords that branch and merge with each other and that these cords, in turn, are formed by globose structures, such as spherules. A similar ornamentation was described by Yañez (2015) for other species of the genus Hypolepis for northeastern Argentina.

DRYOPTERIDACEAE

Chambi et al. (2013) illustrated the spores of Polystichum motevidense with SEM, where it can be seen that they present inflated folds, with an equinulate surface, as has been observed here. Likewise, we observed that the echinulate surface and the dark brown color of the spores of this species easily distinguish it from the other species (P. platypyllum var. platypyllum) that inhabit the CNP (with a surface without equinules and brown color).

The spores of the Argentine species of Dryopteris and Ctenitis were illustrated with SEM and LM by Gorrer et al. (2020; 2022), respectively. The authors mention that D. patula spores may present a foveolate surface, seen only with SEM, but this surface has not been observed here with LM. While the spores of the two remaining species of both genera present an ornamentation and color similar to what was said by them.

When Lavalle and Rodríguez (2014) analyzed with SEM six of the seven Elaphoglossum species that inhabit in Nortwest Argentina., they described the spore ornamentation of E. yungense with reticles and spines. Nevertheless, in the present paper we observed a folded perispore.

Regarding the remaining species analyzed here, we were able to observe that the spore color in E. spathulatum is a very important character to differentiate it from the other species.

The spores of the Argentine species of Megalastrum have not been illustrated either with SEM or with LM, until now. Arana et al. (2016) affirm that the spores of M. adenopteris and M. fugaceum are equinated. We agree with the ornamentation mentioned by these authors for M. fugaceum, but the spores of M. adenopteris observed and illustrated here with LM and SEM are folded and have a reticulated surface. EQUISETACEAE

In Argentina, the family has a genus with only two species, Equisetum bogotense and E. giganteum. The spores of these species have been analyzed with LM and SEM by Piñeiro and Morbelli (2014). Our observations are agree with those of the authors in that the spores of both species are spheroidal, greenish and have two elater ribbons with spatulate ends, located helically around the spore. We noted similarities in the measurements, where E. bogotense has smaller spores than those of E. giganteum. However, here we could not appreciate with LM the circular apertural mentioned by the authors, so we continue to consider them alete. Also Di Pasquo et al. (2016) and Gorrer et al. (2021) analyzed the spores of E. giganteum with LM from the center-east of Argentina, showing characteristics consistent with those found here.

Conclusion

For the first time, the spores of 27 species are illustrated under a light microscope. Of these 27 species, the spores of five were also illustrated using a scanning electron microscope.

The morphological characteristics of the spores allowed for the identification of 23 species.

The most demanding genera to identify at a specific level are Asplenium and Elaphoglossum, with some species that are difficult to differentiate by the qualitative or quantitative characteristics of their spores.

The Equisetaceae is the only family that had two species with alete and green (chlorophyllous) spores, but they are differentiated by size, with E. giganteum almost 20 µm larger than E. bogotense.

In the Dennstaedtiaceae family, both species are differentiated by aperture type, color, and ornamentation, where H. poeppigii is monolete, yellowish, and baculate-cristate and D. globulifera is trilete, brown, and verrucate.

Only two species are echinate. They belong to two distinct families and are differentiated by color and size. C. diaphana (Cystoperidaceae) is dark brown and more than 10µm larger than M. ciliatum (Dryopteridaceae), which is brown.

Studying the morphological characteristics of spores allows for the creation of a reference point for paleoenvironmental reconstructions in the Yungas of Northwestern Argentina, particularly in the province of Jujuy. The data set provided here contributes to spore bank analysis, aeropalynological and paleopalynological studies, and taxonomic identifications.

Acknowledgements

The authors are grateful to the herbaria that supplied the studied material. This work was supported by grants from Universidad Nacional de La Plata (N940), PICT 02227, and P-UE 22920170100027CO.

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Publication Dates

• Publication in this collection
  20 Oct 2023
• Date of issue
  2023

History

• Received
  30 Mar 2023
• Accepted
  06 Aug 2023