Nectary structure is not related to pollination system in Trichocereeae cactus from Northwest Argentina

GONZÁLEZ, VALERIA V.; GOROSTIAGUE, PABLO; ORTEGA-BAES, PABLO; GALATI, BEATRIZ G.; FERRUCCI, MARÍA S.

doi:10.1590/0001-3765202120201401

VALERIA V. GONZÁLEZ

Universidad Nacional del Nordeste/CONICET, Instituto de Botánica del Nordeste (IBONE), Sargento Juan Bautista Cabral 2131, W3402BKG, Corrientes, Argentina

http://orcid.org/0000-0002-8405-9274

PABLO GOROSTIAGUE

Universidad Nacional de Salta/CONICET, Facultad de Ciencias Naturales, Laboratorio de Investigaciones Botánicas (LABIBO), Av. Bolivia 5150, A4400, Salta, Argentina

http://orcid.org/0000-0001-5131-5940

PABLO ORTEGA-BAES

Universidad Nacional de Salta/CONICET, Facultad de Ciencias Naturales, Laboratorio de Investigaciones Botánicas (LABIBO), Av. Bolivia 5150, A4400, Salta, Argentina

http://orcid.org/0000-0002-3436-6823

BEATRIZ G. GALATI

Universidad de Buenos Aires, Facultad de Agronomía, Depto. de Recursos Naturales y Ambiente, Cátedra de Botánica General, Av. San Martín 4453, C1417DSE, Buenos Aires, Argentina

http://orcid.org/0000-0001-7891-9429

MARÍA S. FERRUCCI

Universidad Nacional del Nordeste/CONICET, Instituto de Botánica del Nordeste (IBONE), Sargento Juan Bautista Cabral 2131, W3402BKG, Corrientes, Argentina

http://orcid.org/0000-0003-4917-1188

Correspondence to: Valeria V. González E-mail: valeriavanesagonzalez@gmail.com

AUTHOR CONTRIBUTIONS

VVG, PG and POB contributed to the study conception and design, and field work. VVG performed material preparation, data analysis, and wrote the manuscript. BG contributed to transmission electron microscopy analysis. MSF read the manuscript, revised and completed the information. All the authors commented on previous versions of the manuscript and approved the final version.

Figures (5)
Tables (1)

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Figure 1
a-d Ornitophilous flowers of cactus. a Cleistocactus baumannii, detail of sigmoid tubular flower. b C. hyalacanthus, detail of upper portion of stem with buds, flowers in anthesis and fruits. c C. smaragdiflorus, detail of tubular flower, note green tepals. d Denmoza rhodacantha, detail of buds and sigmoid tubular flowers at the apex of the stem. e-j Sphingophilous flowers. e Echinopsis albispinosa, plant and infundibuliform flower. f E. ancistrophora, plant and flower still open early in the morning. g E. atacamensis, detail of infundibuliform flower. h E. leucantha, detail of a set of flowers. i E. schickendantzii, detail of two flowers. j E. terscheckii, detail of flower. Photographs: V. González a-c, P. Gorostiague d-j.

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Figure 2
Floral nectary morph-anatomy in Cleistocactus species. a-d C. baumannii a Scanning Electron Microscope (SEM) of nectar chamber in longitudinal section, note at the upper portion the vault-roof structure (white arrowheads) formed by the fusion of the base of the internal stamens that begin to be released. b Cross section of floral nectary. c Detail of nectarostoma (black arrowhead) with remnants of crystallized secretion. d Detail of epidermis interrupted with traces of crystallized secretion. e-g C. hyalacanthus. e SEM of nectar chamber in longitudinal section, note the fused base of the filaments of the internal series (white stars) released in the upper portion of the chamber. f Cross section of floral nectary. g Longitudinal section of floral nectary. h-j C. smaragdiflorus. h SEM of nectar chamber in longitudinal section, white arrows indicate the bases of the fused filaments. i Cross section of floral nectary, with polarized light the starch grains show the figure of a Maltese cross. j Longitudinal section of nectar chamber. Abbreviations: (ep) epidermis; (f) filament; (nc) nectar chamber; (np) nectariferous parenchyma; (snp) sub-nectariferous parenchyma. Scale bars: a 2mm; b 100µm; c, i 20µm; d 30µm; e, h 1mm; f 50µm; g, k 200µm.

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Figure 3
Floral nectary morph-anatomy of Denmoza rhodacantha. a-b Longitudinal sections. a Basal portion of flower, note the nectar chamber surrounding the base of the style, with a “plug” of curled trichomes (white arrowheads). b SEM of portion of nectar chamber. c Detail of staminodes born in the upper portion of the nectar chamber, note differences in the bases of the curled trichomes (black starts and white starts). d Light micrographs of non-vascularized staminodes, note the morphological differences in the bases (black starts and white start). e and f transversal section of staminodes. g Longitudinal section of floral nectary wall. h Detail of nectary wall showing traces of xylem and phloem penetrating and branching deeply into the nectariferous parenchyma (arrows). i Cross section of nectar chamber, observe the pattern of peaks and valleys of the wall. j Detail of nectarostoma (arrowhead), with conspicuous sub-stomatic chamber. Abbreviations: filaments (f), nectar chamber (nc), nectariferous parenchyma (np), sub-nectariferous parenchyma (snp), style (S), vascular bundles (vb). Scales: b 500 µm; c, e, g 200 µm; f 20 µm; d, h 50 µm.

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Figure 4
Floral nectary morpho-anatomy of Echinopsis. a-c E. albispinosa. a-b SEM. a Superficial view of nectar chamber wall, note nectarostomata (white arrowheads). b Detail of nectarostoma. c Light micrographs of cross section of floral nectary. d-e E. ancistrophora. d Superficial view of nectar chamber wall, note nectar secretion (white stars). e Light micrographs of cross section of floral nectary. f-j E. atacamensis. f Nectar chamber in longitudinal section, note free filaments of the internal series at the top. g Transversal section of the flower above the nectar chamber, note the barrier formed by the filaments surrounding the style. h, k-m Light micrographs of transversal sections of floral nectary. i Floral nectary with polarized light, note druses and starch grains in nectariferous parenchyma. j Detail of nectarostoma with possible secretion remains (arrowhead), observe unicellular trichomes inclined towards the opening. k E. leucantha. l E. schickendantzii. m E. terscheckii. Abbreviations: (f) filament; (nc) nectar chamber; (np) nectariferous parenchyma, (S) style, (snp) sub-nectariferous parenchyma, (vb) vascular bundles. Scales: a, d, h-i, k-m 50µm; b 5µm; c 10µm; e, j 20 µm; f 3mm, g 5mm.

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Figure 5
Transmission Electron Microscope (TEM) of floral nectary of E. terscheckii. a-f Pre-anthesis. (a) Proximal portion of an epidermal trichome, showing a large nucleus and a prominent nucleolus, white arrow indicates a small vacuole fusing with the cell membrane; note cell walls flared towards the base of the trichome. (b) Detail of dense granular cytoplasm of the trichome, note abundant mitochondria, vacuoles of small dimensions, abundant compound amyloplasts and few lipid globules. (c) Connection between two epidermal trichomes, showing portions of the nuclei of both cells, occupying a basal position; the white arrow indicates a vacuole fusing with the cell membrane. (d) Connection between epidermal trichome (upper position) and nectariferous parenchyma (lower position), observe cell walls of different thicknesses, and the absence of plasmodesmata between both cells. (e) Detail of dense cytoplasm of a parenchymal nectariferous cell, showing plastids with several grains of starch, small vacuoles, rough endoplasmic reticulum; note the intercellular space. (f) Detail of connection between two cells of the nectariferous parenchyma, white arrowheads indicate plasmodesmata that communicate the cytoplasm of secretory tissue cells. (g-l) Anthesis. (g) Portion of epidermal trichome, observe the cytoplasm less electrodense than in pre-anthesis, with larger vacuoles. (h) Detail of epidermal trichome cytoplasm, plastids with partially degraded starch grains; note the accumulation of rough endoplasmic reticulum in the cytoplasm. (i) Detail of the apical portion of the epidermal trichome with secretion released by rupture of the cuticle (white arrow). (j) Connection between two epidermal trichomes and an underlying nectariferous parenchyma cell; in both tissues, large vacuoles relegate the cytoplasm to the periphery of the cells. (k) Detail of nectariferous tissue cells, observe less dense cytoplasm and mitochondria in apparent degeneration. l Detail of intercellular space in the nectariferous tissue, with homogeneous electrodense material, suggests that sugary secretion accumulates in these spaces; note partially degraded amyloplasts, and plasmodesmata connecting cytoplasms (white arrowhead). Abbreviations: (am) amyloplast; (d) dictyosome; (ecs) extracellular space; (ics) intercellular space; (lg) lipid globule; (m) mitochondria; (N) nucleus; (nu) nucleolus; (w) cellular wall; (np) nectariferous parenchyma; (rr) rough endoplasmic reticulum; (et) epidermal trichome; (v) vacuole. Scale: a-c, j, l 1μm; d-i, k 500nm.

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Table I
Voucher information, comparison of floral characters and reproductive biology of the studied species of Trichocereeae.

Figure 5 Transmission Electron Microscope (TEM) of floral nectary of E. terscheckii. a-f Pre-anthesis. (a) Proximal portion of an epidermal trichome, showing a large nucleus and a prominent nucleolus, white arrow indicates a small vacuole fusing with the cell membrane; note cell walls flared towards the base of the trichome. (b) Detail of dense granular cytoplasm of the trichome, note abundant mitochondria, vacuoles of small dimensions, abundant compound amyloplasts and few lipid globules. (c) Connection between two epidermal trichomes, showing portions of the nuclei of both cells, occupying a basal position; the white arrow indicates a vacuole fusing with the cell membrane. (d) Connection between epidermal trichome (upper position) and nectariferous parenchyma (lower position), observe cell walls of different thicknesses, and the absence of plasmodesmata between both cells. (e) Detail of dense cytoplasm of a parenchymal nectariferous cell, showing plastids with several grains of starch, small vacuoles, rough endoplasmic reticulum; note the intercellular space. (f) Detail of connection between two cells of the nectariferous parenchyma, white arrowheads indicate plasmodesmata that communicate the cytoplasm of secretory tissue cells. (g-l) Anthesis. (g) Portion of epidermal trichome, observe the cytoplasm less electrodense than in pre-anthesis, with larger vacuoles. (h) Detail of epidermal trichome cytoplasm, plastids with partially degraded starch grains; note the accumulation of rough endoplasmic reticulum in the cytoplasm. (i) Detail of the apical portion of the epidermal trichome with secretion released by rupture of the cuticle (white arrow). (j) Connection between two epidermal trichomes and an underlying nectariferous parenchyma cell; in both tissues, large vacuoles relegate the cytoplasm to the periphery of the cells. (k) Detail of nectariferous tissue cells, observe less dense cytoplasm and mitochondria in apparent degeneration. l Detail of intercellular space in the nectariferous tissue, with homogeneous electrodense material, suggests that sugary secretion accumulates in these spaces; note partially degraded amyloplasts, and plasmodesmata connecting cytoplasms (white arrowhead). Abbreviations: (am) amyloplast; (d) dictyosome; (ecs) extracellular space; (ics) intercellular space; (lg) lipid globule; (m) mitochondria; (N) nucleus; (nu) nucleolus; (w) cellular wall; (np) nectariferous parenchyma; (rr) rough endoplasmic reticulum; (et) epidermal trichome; (v) vacuole. Scale: a-c, j, l 1μm; d-i, k 500nm.

Species	Voucher information	Floral nectary				Floral length (mm)	Floral diameter (mm)	Floral cycle	Floral phenotype	Pollinators/ visitors	Reference
Species	Voucher information	Type	Vascularization	Epidermis	Secretion mode	Floral length (mm)	Floral diameter (mm)	Floral cycle	Floral phenotype	Pollinators/ visitors	Reference
Cleistocactus baumanii	Argentina. Salta, González, V.V. et al. 5 (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Smooth	Stomata Holocrine	50.20 ± 9.53	7.19 ± 1.68	Diurnal, more than 48 h open	Ornithophilous	Hummingbirds	Gorostiague & Ortega Baes 2016
C. hyalacanthus	Argentina. Salta, González, V.V. et al. s.n. (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Smooth	Stomata	c. 35-40	-	Diurnal	Ornithophilous	No available information	Hunt 2006HUNT D. 2006. The new cactus lexicon. Milborne Port: DH Books, UK, p. 373-526.
C. smaragdiflorus	Argentina. Salta, González, V.V. et al. 4 (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Smooth	Stomata	44.71 ± 4.09	6.97 ± 1.89	Diurnal, more than 48 h open	Ornithophilous	Bees Hummingbirds	Gorostiague & Ortega Baes 2016
Denmoza rhodancantha	Argentina. Salta, González, V.V. et al. 17 (CTES)	Closed chamber	Xylem and phloem penetrate the nectariferous parenchyma	Papillose	Stomata	49.1 ± 7.9	9.9 ± 2.4	Diurnal, more than 48 h open	Ornithophilous	Bees Hummingbirds (Oreotrochilus leucopleurus)	Eggli & Giorgetta 2015EGGLI U & GIORGETTA M. 2015. Flowering phenology and observations on the pollination biology of South American cacti. 1. Denmoza rhodacantha. Haseltonia 20: 3-12., Gorostiague 2017GOROSTIAGUE P. 2017. Las cactáceas y sus polinizadores en el Noroeste de Argentina: distribución geográfica, cambio climático y conservación. Doctoral Dissertation. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata (Unpublished).
Echinopsis albispinosa	Argentina. Salta, González, V.V. et al. 9 (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Unicellular trichomes	Stomata	128.6 ± 18.6	78.7 ± 13.6	nocturnal, extended to the following morning	Sphingophilous	Bees Moths	Gorostiague 2017GOROSTIAGUE P. 2017. Las cactáceas y sus polinizadores en el Noroeste de Argentina: distribución geográfica, cambio climático y conservación. Doctoral Dissertation. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata (Unpublished).
E. ancistrophora	Argentina. Salta, González, V.V. et al. 20 (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Unicellular trichomes	Stomata	111.7 ± 17.4	80.0 ± 14.1	nocturnal, extended to the following morning	Sphingophilous	Bees Moths	Schlumpberger et al. 2009SCHLUMPBERGER BO, COCUCCI AA, MORÉ M, SÉRSIC AN & RAGUSO RA. 2009. Extreme variation in floral characters and its consequences for pollinator attraction among populations of an Andean cactus. Ann Bot 103: 1489-1500.
E. atacamensis	Argentina. Salta, González, V.V. et al. 14 (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Unicellular trichomes	Stomata	124 ± 2	96 ± 3	nocturnal, extended to the following morning	Sphingophilous	Bees Giant hummingbird (Patagona gigas) Moths Wasps	De Viana et al. 2001DE VIANA ML, ORTEGA-BAES P, SARAVIA M, BADANO EI & SCHLUMPBERGER B. 2001. Biología floral y polinizadores de Trichocereus pasacana (Cactaceae) en el Parque Nacional Los Cardones, Argentina. Rev Biol Trop 49: 279-285., Schlumpberger & Badano 2005SCHLUMPBERGER BO & BADANO EI. 2005. Diversity of floral visitors to Echinopsis atacamensis subsp. pasacana (Cactaceae). Haseltonia 11: 18-26.
E. leucantha	Argentina. Salta, González, V.V. et al. s.n. (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Unicellular trichomes	Trichomes	198.17 ± 13.20	113.62 ± 21.74	nocturnal, extended to the following morning	Sphingophilous	Bees Passerine birds (Phrygilus gayi)	Gorostiague & Ortega-Baes 2017GOROSTIAGUE P & ORTEGA-BAES P. 2017. Pollination biology of Echinopsis leucantha (Cactaceae): passerine birds and exotic bees as effective pollinators. Botany 95: 53-59.
E. schickendantzii	Argentina. Salta, González, V.V. et al. 18 (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Unicellular trichomes	Stomata	118.8 ± 2.3	105 - 140	nocturnal, extended to the following morning	Sphingophilous	Bees Moths	Alonso- Pedano & Ortega-Baes 2012
E. terscheckii	Argentina. Salta, González, V.V. et al. 10 (CTES)	Semi-closed chamber	Xylem and phloem delimit the nectariferous parenchyma	Unicellular trichomes	Stomata Trichomes	177.7 ± 16.0	163.8 ± 21.7	nocturnal, extended to the following morning	Sphingophilous	Bees Moths Beetles Hummingbirds Passerine birds	Ortega-Baes et al. 2011ORTEGA-BAES P, SARAVIA M, SÜHRING S, GODÍNEZ-ALVAREZ H & ZAMAR M. 2011. Reproductive biology of Echinopsis terscheckii (Cactaceae): the role of nocturnal and diurnal pollinators. Plant Biol 13: 33-40.

[1] Correspondence to: Valeria V. González E-mail: valeriavanesagonzalez@gmail.com

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Nectary structure is not related to pollination system in Trichocereeae cactus from Northwest Argentina

Abstract