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ECOSYSTEMS • An. Acad. Bras. Ciênc. 94 (3) • 2022 • https://doi.org/10.1590/0001-3765202220210100   copy

Comparative cypsela morphology in Campuloclinium DC. and contributions to Eupatorieae tribe (Asteraceae) systematics

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Cypselae anatomical studies have helped to understand the evolution and classification of some groups within Asteraceae. In Eupatorieae, there are many uncertainties about the Campuloclinium circumscription. There are currently two classifications for the genus, and still no consensus for their delimitation. Since structural studies have contributed to the delimitation of groups in Asteraceae, we studied the cypselae of Campuloclinium, searching how the pericarpial taxonomic features could enlighten the genus classification. We studied the fruits of eleven species of this genus through morphological and anatomical observation. Our results showed relevant features to the classification of Campuloclinium and its closely related groups. The stipitate cypsela together with other diagnostic characters are relevant to delimitation of this genus within of Eupatorieae. The trichomes present in cypselae have taxonomic proved to be a possible diagnostic character for the genus, and the six-celled trichomes are essential to distinguish C. campuloclinioides and C. hirsutum. The combination of phylogenetic and structural studies may lead to future research on the delimitation of Campuloclinium and its clades and understand how the stipitate cypselae and the phytomelanin layer evolve in Eupatorieae.

Key words
anatomy; fruit; Gyptidinae; pericarp; phytomelanin layer; stipitate cypsela

INTRODUCTION

Campuloclinium DC. is a genus in the Eupatorieae tribe within Asteraceae (King & Robinson 1972KING RM & ROBINSON H. 1972. Studies in the Eupatorieae (Asteraceae). XC. The genus, Campuloclinium. Phytologia 24: 170-172., 1987). It presents a Neotropical distribution and comprises 12 species, which occur in southeastern South America, especially in Brazil (Calvo & Roque 2018CALVO J & ROQUE N. 2018. Taxonomic Revision of the Neotropical Genus Campuloclinium (Eupatorieae, Compositae). Syst Bot 43(2): 602-627.).

The genus was described by Candolle (1836)CANDOLLE AP. 1836. Prodromus systematis naturalis regni vegetabilis. Vol. 5. Paris: Sumptibus Sociorum Treuttel et Würtz, 706 p., and since then, it has undergone several modifications in its generic classification. It has been recognized as a section within Eupatorium L. (Bentham 1873BENTHAM G. 1873. LXXXVIII. Compositae. In BENTHAM G & HOOKER JD (Eds), Genera Plantarum: Vol. 2(1), London: Lovell Reeve & Co., Williams & Norgate, London, England, p. 163-533., Baker 1876BAKER JG. 1876. Compositae. II. Eupatoriaceae. In: MARTIUS CFP & EICHLER AG Eds. Flora Brasiliensis: Vol. 6(2): 181-376, Monachii and Lipsiea: Frid. Fleischer in Comm., Monachii and Lipsiea, French and German, p. 181-398., Robinson 1918ROBINSON BL. 1918. A descriptive revision of the Colombian Eupatorium’s. P Am Ac Arts Sci 54: 264-330.), and at others as a separate genus (Candolle 1836CANDOLLE AP. 1836. Prodromus systematis naturalis regni vegetabilis. Vol. 5. Paris: Sumptibus Sociorum Treuttel et Würtz, 706 p., Gardner 1846GARDNER G. 1846. Contributions towards a Flora of Brazil, being the characters of several new species of Compositae, belonging to the tribe Eupatoriaceae. London J Bot 5: 455-491.). However, Campuloclinium is currently recognized at the generic level (King & Robinson 1972KING RM & ROBINSON H. 1972. Studies in the Eupatorieae (Asteraceae). XC. The genus, Campuloclinium. Phytologia 24: 170-172., 1987). According to King & Robinson (1972, 1987), the genus is characterized by its receptacle being hemispherical or conical, scrobiculate and glabrous, and by elongate cypsela with tapered base (stipitate).

Although King & Robinson (1987)KING RM & ROBINSON H. 1987. The genera of the Eupatorieae (Asteraceae). Monog Syst Botan 22: 1-581. allocated Campuloclinium within Gyptidinae, the genus position is still uncertain. Phylogenetic studies performed by Robinson et al. (2009) and Rivera et al. (2016a)RIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300. differ in the subtribal positioning of the genus. While Robinson et al. (2009) agreed that Campuloclinium belongs in the subtribe Gyptidinae, Rivera et al. (2016a)RIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300. postulated that this genus and its related genera should be circumscribed in a new subtribe.

As King & Robinson (1972, 1987) mentioned, reproductive structures have great importance to the classification of Campuloclinium. The fruits of Asteraceae, known as cypselae, arise from the inferior ovary (Marzinek et al. 2008MARZINEK J, DE-PAULA OC & OLIVEIRA DMT. 2008. Cypsela or achene? Refining terminology by considering anatomical and historical factors. Braz J Bot 31: 549-553.). The cypselae have a high classification value in different hierarchical levels in the family (Angulo et al. 2015ANGULO MB, SOSA MM & DEMATTEIS M. 2015. Systematic significance of cypsela morphology in Lessingianthus (Vernonieae, Asteraceae). Aust Syst Bot 28: 173-189., Freitas et al. 2015FREITAS FS, DE-PAULA OC, NAKAJIMA JN & MARZINEK J. 2015. Fruits of Heterocoma (Vernonieae-Lychnophorinae): Taxonomic significance and a new pattern of phytomelanin deposition in Asteraceae. Bot J Linn Soc 179: 255-265., Via do Pico et al. 2016VIA DO PICO GM, VEGA AJ & DEMATTEIS M. 2016. Systematic consideration of floral microcharacters of the South American genus Chrysolaena (Vernonieae, Asteraceae). Syst Biodivers 14: 224-243., Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107., Marques et al. 2018a, b, 2020, Bonifácio et al. 2019BONIFÁCIO SKV, MOURA LL, MARZINEK J & DE-PAULA OC. 2019. Comparative embryology of Stiffia and Wunderlichia and implications for its evolution in Asteraceae. Bot J Linn Soc 189(2): 169-185., Grossi et al. 2020GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.) and the anatomical studies of these structures have contributed to solving taxonomy problems (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., Freitas et al. 2015FREITAS FS, DE-PAULA OC, NAKAJIMA JN & MARZINEK J. 2015. Fruits of Heterocoma (Vernonieae-Lychnophorinae): Taxonomic significance and a new pattern of phytomelanin deposition in Asteraceae. Bot J Linn Soc 179: 255-265., Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107., Marques et al. 2018a, b, 2020, Bonifácio et al. 2019BONIFÁCIO SKV, MOURA LL, MARZINEK J & DE-PAULA OC. 2019. Comparative embryology of Stiffia and Wunderlichia and implications for its evolution in Asteraceae. Bot J Linn Soc 189(2): 169-185.).

In Eupatorieae, anatomical studies with the cypselae have contributed to the resolution of taxonomic issues at the subtribal (Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107.), generic (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291.), and specific levels (Franca et al. 2015FRANCA RO, DE-PAULA OC, CARMO-OLIVEIRA R & MARZINEK J. 2015. Embryology of Ageratum conyzoides L. and A. fastigiatum R. M. King & H. Rob. (Asteraceae). Acta Bot Bras 29: 8-15.). Moreover, these studies have reevaluated the morphological terms of cypselae that sometimes generate confusion (Marzinek et al. 2010MARZINEK J, DE-PAULA OC & OLIVEIRA DMT. 2010. The ribs of Eupatorieae (Asteraceae): of wide taxonomic value or reliable characters only among certain groups? Plant Sys Evol 285: 127-130.).

In this study, we evaluated the taxonomic value of cypselae for the classification of Campuloclinium. We compared the cypselae anatomy between species in the genus and then to other genera and subtribes within Eupatorieae to find features that would support some current classifications.

MATERIALS AND METHODS

The cypselae of 11 Campuloclinium species were studied using light microscopy and scanning electron microscopy (SEM). The material was obtained from herbaria of the Northeast Botany Institute (CTES, Argentina), the New York Botanical Garden Herbarium (NY), in NY, United States and the Federal Universities of Brasília (UB), Uberlândia (HUFU), and Bahia (ALCB), in Brazil. Details of the collection locations and the vouchers are available in Table I. For the SEM analysis, some samples were coated with gold and others were dehydrated in acetone and immersed in CO2 to a critical point before gold coating. After that, all the cypselae were examined and photographed using the scanning electron microscopes JEOL 5800 LV or Zeiss EVO MA 100.

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Table I
Voucher information for species of Campuloclinium used in present study. * samples submitted to critical point drying. ** samples not submitted to critical point drying.

For observation of microcharacters, cypselae were softened in boiling water with a drop detergent, mounted in Hoyer’s solution (Anderson 1954ANDERSON LE. 1954. Hoyer’s solution as a rapid permanent mounting medium for bryophytes. Bryologist 57: 242-244., King & Robinson 1970KING RM & ROBINSON H. 1970. The new synantherology. Taxon 19(1): 6-11.), and then analyzed under a Zeiss Axioplan light microscope.

For the anatomical analysis, fruits were rehydrated with a solution of 5M NaOH for half an hour (Anderson 1963ANDERSON LC. 1963. Studies on Petradoria (Compositae): Anatomy, cytology, taxonomy. Transactions of the Kansas Academy of Science 66: 632-684., modified), dehydrated in an ethanol series, and embedded in historesin (Leica Microsystems, Heidelberg, Germany). The samples were sectioned in a rotating microtome using 10µm thickness. The cuts were stained with 0.05% toluidine blue in acetate buffer, pH 4.7 (O’Brien et al. 1964O’BRIEN TP, FEDER N & MCCULLY ME. 1964. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59: 368-373., modified), and mounted with synthetic resin. The slides were analyzed under a light microscope and images from three regions of the cypsela (basal, median, and apical) were acquired under the microscope Olympus BX51.

For the distribution of trichomes, three cypselae of each specimen were analyzed. The term rare was used when the trichomes were present in up to 10% of the surface of the cypsela, the frequent term was used between 11% and 50% and the term abundant when the trichomes were present above 50% of the surface of the cypsela.

Trichome terminology was based on Metcalfe & Chalk (1950METCALFE CR & CHALK L. 1950. Anatomy of the Dicotyledons: Leaves, Stem, and Wood in Relation to Taxonomy with Notes on Economic Uses. Oxford: Clarendon Press, Oxford, Great Britain, 724 p., 1979METCALFE CR & CHALK L. 1979. Anatomy of the dicotyledons: volume 1. Systematic anatomy of lead and stem, with a brief history of the subject. Oxford: Clarendon Press, Oxford, Great Britain, 276 p.). The description of the pericarp and the trichome distribution were carried out in an ontogenetic way, as proposed by Marzinek & Oliveira (2010)MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291..

RESULTS

External morphology

All cypselae studied are stipitate and prismatic, with evident ribs and trichome throughout the pericarp (Fig. 1a-k, Table II). Biseriate tector trichomes are restricted to the ribs and are composed of four cells (Table II). In the apical and basal portion of cypsela of C. campuloclinioides (Fig. 2b) and C. hirsutum is found biseriate tector trichome with six cells (Table II). Glandular trichomes were observed in the interrib region, with four to six basal cells and a biseriate head with eight cells (Fig. 2c-d, Table II). In Table II, it is also possible to observe the distribution pattern of the trichomes which have been categorized as rare, frequent and abundant in all species.

Figure 1
SEM of cypselae of Campuloclinium in the general view (a-k). a) C. alternifolium. b) C. burchellii. c) C. campuloclinioides. d) C. chlorolepis. e) C. hirsutum. f) C. irwinii. g) C. macrocephalum. h) C. megacephalum. i) C. parvulum. j) C. purpuracens. k) C. riedelii. ap: apex; ca: carpopodium; gt: glandular trichome; pa: pappus; tt: tector trichome; double arrowhead: ribs.
Figure 2
Microcharacters (a-d) and SEM (e-l) of Campuloclinium in detail. a-d. Detail of the trichomes. a-b. C. campuloclinioides. a) Note the biseriate trichomes is 4-celled. b) Note the biseriate tector trichome is 6-celled. c) Middle region of C. hirsutum, with 4-celled biseriate trichomes composed and glandular trichomes with 4–6 basal cells and 8-celled biseriate head. d) C. riedelli note glandular trichomes with 4–6 basal cells and 8-celled biseriate head. e-h) Annular carpopodium. e) C. burchelli. f) C. campuloclinioides. g) C. chlorolepis. h) C. hirsutum. i-l) Apex of the cypsela. Note the fused base of the pappus. i) C. campuloclinoides, j) C. irwinii, k) C. purpurascens, l) C. riedelli. ap: apex; ca: carpopodium; gt: glandular trichome; tt: tector trichome.
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Table II
Types and distribution of trichomes on the cypselae of the Campuloclinium (A: apex, M: middle region, B: base; - absent, +: rare, ++: frequent, +++: abundant).

In the basal region is located the carpopodium, which presented annular shape in all species (Fig. 2e-h). The apical region has a uniseriate pappus with bristles connate on the base (Fig. 2i-l).

Anatomy

Almost all species presented five evident ribs (Fig. 3a). However, in some specimens of C. chlorolepis, (Fig. 3b) the cypsela has six ribs and in specimens C. parvulum, the cypsela can present eight ribs (Fig. 3c).

Figure 3
Transversal sections of the Campuloclinium cypsela. a–b) General view. a) C. irwinnii with five ribs. b) C. chlorolepis with six ribs. c) C. parvulum with eight ribs. d-f) Pericarp detail. d) C. irwinnii. e) C. macrocephalum. f) C. purpuracens. g-i) Detail of the ribs. g) C. irwinnii. h) C. macrocephalum. i) C. purpuracens. Note the phytomelanin is a continuous layer internal to the vascular bundle. j) Carpopodium of C. burchelli. k) Lignified pappus of C. irwinnii. l) Apex in C. purpuracens. co: cotyledon; ex: exocarp; gt: glandular trichome; im: inner mesocarp; ir: interrib; ou: outer mesocarp; pe: pericarp; sc: sclereids; se: seed; tt: tector trichome; vb: vascular bundle; double arrowhead: ribs.

The exocarp is uniseriate with juxtaposed ordinary cells (Fig. 3d-f). The outer mesocarp is compound by the outer parenchymatic region; more internally by a schizogenous space filled with phytomelanin (Fig. 3d-f). The inner mesocarp is formed by a sclereid layer and a variable number of parenchymatic cells (Fig. 3d-f). This parenchymatic layer is found with five or six layers in C. parvulum; two to five in C. burchellii; one in C. alternifolium, C. campuloclinioides, C. irwinnii (Fig. 3d), C. macrocephalum (Fig. 3e), C. purpuracens (Fig. 3f), and absent in C. chlorolepis, C. hirsutum, C. megacephalum, and C. riedelii consumed during seed development. In the rib region, we observed a collateral vascular bundle involved by fibers (Fig. 3g-i). The distribution of phytomelanin is internal to the bundles (Fig. 3g-i). In all species, the endocarp is also consumed by seed development.

The carpopodium has a uniseriate exocarp and lignified, with cells slightly elongated in the periclinal sense (Fig. 3j); in C. purpuracens and C. hirsutum are observed glandular trichome. The mesocarp presents isodiametric to elongated cells, which can be parenchymatic or lignified (Fig. 3j). In the central region is observed vascular bundles (Fig. 3j).

The pappus presents one series of lignified bristles connate in the base in all species (Fig. 3k).

In the apical region of fruit, the exocarp presents cells with a primary wall, flattened in the periclinal sense (Fig. 3l). More internally lignified cells are found elongated in the periclinal sense (Fig. 3l).

DISCUSSION

External morphology

As King & Robinson (1987)KING RM & ROBINSON H. 1987. The genera of the Eupatorieae (Asteraceae). Monog Syst Botan 22: 1-581. mentioned, all these cypsela features are important to delimitate this genus once these traits and the receptacle shape are diagnostic to Campuloclinium. Our study is in agreement with these authors and, again, the detailed study of cypselae corroborated the importance of this reproductive organ for the classification of Asteraceae.

The presence of stipitate cypsela is important for generic delimitation in the two current possible phylogenetic relationships of this genus, one proposed by Robinson et al. (2009)ROBINSON H. 2009. An introduction to micro-characters of Compositae. In: FUNK VA ET AL. (Eds), Systematics, Evolution and Biogeography of Compositae, Vienna: International Association for Plant Taxonomy, Vienna, Austria, p. 89-100. and the second by Rivera et al. (2016a)RIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300.. In the first classification, Campuloclinium is closely related to Trichogonia (DC.) Gardner, with both genera sharing the presence of stipitate cypsela (Robinson et al. 2009ROBINSON H, SCHILLING E & PANERO JL. 2009. Eupatorieae. In: FUNK VA ET AL. (Eds), Systematics, Evolution and Biogeography of Compositae, Vienna: International Association for Plant Taxonomy, Vienna, Austria, p. 731-744., Roque et al. 2012ROQUE N, BAUTISTA HP & MOTA AC. 2012. Taxonomic Revision of Trichogonia (Eupatorieae, Asteraceae): A South American Genus. Syst Bot 37(2): 525-553.). On the other hand, in the studies performed by Rivera et al. (2016a)RIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300., Campuloclinium appears phylogenetically related to Macropodina R.M.King & H.Rob., which most species presents stipitate cypsela (Nakajima et al. 2017NAKAJIMA JN, FERREIRA SC, FERNANDES AC, RIVERA VL, HATTORI EKO, QUARESMA AS, RITTER MR & Grossi MA. 2017. Tribo Eupatorieae Cass. In: ROQUE N ET AL. (Eds), A família Asteraceae no Brasil classificação e diversidade, Salvador, EDFBA, Salvador, Brasil, p. 209-230.). In Eupatorieae, this cypsela type is found in some genera and species of the different subtribes (Grossi et al. 2020GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.), but it is commonly found in genera in the Gyptidinae subtribe (Funk et al. 2009FUNK VA, SUSANNA A, STUESSY TF & BAYER RJ. 2009. Systematics, Evolution, and Biogeography of Compositae. Vienna: International Association for Plant Taxonomy, 965 p., Robinson et al. 2009) and some others Eupatorieae genera, as Trichogoniopis R.M.King & H.Rob., Platypodanthera R.M.King & H.Rob., Trichogonia, Campuloclinium and Macropodina (Hind & Robinson 2007HIND DJN & ROBINSON H. 2007. Eupatorieae. In: KADEIRET JW & JEFFREY C (Eds), The Families and Genera of Vascular Plants, Vol. 8: Flowering Plants, Eudicots, Asterales, Berlin: Springer-Verlag, Berlin, German, p. 510-574., Ferreira 2010, Nakajima et al. 2017NAKAJIMA JN, FERREIRA SC, FERNANDES AC, RIVERA VL, HATTORI EKO, QUARESMA AS, RITTER MR & Grossi MA. 2017. Tribo Eupatorieae Cass. In: ROQUE N ET AL. (Eds), A família Asteraceae no Brasil classificação e diversidade, Salvador, EDFBA, Salvador, Brasil, p. 209-230., Grossi et al. 2020GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.). Based on molecular data, Rivera et al. (2016b)RIVERA VL, PANERO JL, SCHILLING EE, CROZIER BS & MORAES MD. 2016a. Origins and recent radiation of Brazilian Eupatorieae (Asteraceae) in the eastern Cerrado and Atlantic Forest. Mol Phylogenet Evol 97: 90-100. describe a new subtribe, named Trichogoniinae, including the genera Platypodanthera, Trichogonia, and Trichogoniopsis. According to Rivera et al. (2016b)RIVERA VL, PANERO JL, SCHILLING EE, CROZIER BS & MORAES MD. 2016a. Origins and recent radiation of Brazilian Eupatorieae (Asteraceae) in the eastern Cerrado and Atlantic Forest. Mol Phylogenet Evol 97: 90-100., in addition to the molecular data, the presence of a subplumose to plumose pappus and stipitate cypsela supports the classification of these genera into this new subtribe. In both analyses by Rivera et al. (2016a, b), a clade formed by Campuloclinium, Macropodina, and other genera in the Ayapaninae subtribe emerge as a sister group of a clade that contains Trichogoniinae and others subtribes. So, given these new phylogenetic analyses, is relevant to emphasize the importance of stipitate cypsela in the classification of Campuloclinium and possible related groups. Nevertheless, further research involving phylogenetic and ontogenetic studies is still necessary for understanding the evolution of the stipitate cypsela within these groups, once the delimitation of Campuloclinium within Eupatorieae is yet unclear.

In the cypsela, the biseriate tector trichome (twin hairs) are common in most Asteraceae genera (Hess 1938HESS R. 1938. Vergleichende Untersuchungen iiber die Zwillingshaare der Kompositen. Bot Jahrb Syst 68: 435-496., Robinson 2009), but glandular trichomes can also be found (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., Angulo et al. 2015ANGULO MB, SOSA MM & DEMATTEIS M. 2015. Systematic significance of cypsela morphology in Lessingianthus (Vernonieae, Asteraceae). Aust Syst Bot 28: 173-189., Via do Pico et al. 2016VIA DO PICO GM, VEGA AJ & DEMATTEIS M. 2016. Systematic consideration of floral microcharacters of the South American genus Chrysolaena (Vernonieae, Asteraceae). Syst Biodivers 14: 224-243., Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107., Marques et al. 2018aMARQUES D, ANGULO MB, NAKAJIMA JN & DEMATTEIS M. 2018b. The taxonomic utility of micromorphology in Lepidaploa (Vernonieae: Asteraceae). Nord J Bot 36: 1-17., bMARQUES D, FRANCA RO, ANGULO MB, VIA DO PICO GM, DEMATTEIS M & MARZINEK J. 2020. Comparative Anatomy of Cypselae in the Complex Group Chrysolaena, Echinocoryne, Lepidaploa, and Lessingianthus: Contributions to the Systematics of Vernonieae (Compositae). Syst Bot 45: 668-680., 2020MARQUES D, FRANCA RO, DEMATTEIS M & MARZINEK J. 2018a. Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): Anatomy and taxonomic implications. Acta Bot Bras 32: 642-655., Grossi et al. 2020GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.). The presence or absence of tector and glandular trichomes has successfully been used for the delimitation of genera and species in several groups within Asteraceae, including Eupatorieae (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., Angulo et al. 2015ANGULO MB, SOSA MM & DEMATTEIS M. 2015. Systematic significance of cypsela morphology in Lessingianthus (Vernonieae, Asteraceae). Aust Syst Bot 28: 173-189., Freitas et al. 2015FREITAS FS, DE-PAULA OC, NAKAJIMA JN & MARZINEK J. 2015. Fruits of Heterocoma (Vernonieae-Lychnophorinae): Taxonomic significance and a new pattern of phytomelanin deposition in Asteraceae. Bot J Linn Soc 179: 255-265., Via do Pico et al. 2016VIA DO PICO GM, VEGA AJ & DEMATTEIS M. 2016. Systematic consideration of floral microcharacters of the South American genus Chrysolaena (Vernonieae, Asteraceae). Syst Biodivers 14: 224-243., Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107., Marques et al. 2018a, b, 2020, Grossi et al. 2020GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.). In Campuloclinium, all species present tector trichomes in ribs and glandular trichomes in interribs. Marzinek & Oliveira (2010)MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291. had already reported the trichome distribution pattern in Campuloclinium macrocephalum. This distribution pattern in Campuloclinium cypsela in conjunction with other characteristics can assist in genera identification at a specific level, type of trichomes and its distribution is very important to identification of species. The tector trichome with six cells is unique to C. campuloclinoides and C. hirsutum, and it can be used to differentiate both species within the genus. Distribution and trichome type are very important in Campuloclinium to species delimitation. The tector trichome with six cells is unique to C. burchelli, C. campuloclinoides and C. hirsutum, and this type of trichome could be a synapomorphy for these last two species taking into account the phylogeny performed by Rivera et al. (2016a)RIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300.. However, C. hirsutum is unique species with six cells tector trichome presents in the interrib region. Campuloclinium riedelii is a unique species that has cypsela with only glandular trichomes, while C. macrocephalum has only tector trichome, such characteristics differentiate both species from the others of the genus. Finally, C. hirsutum and C. purpuracens are the only species of the genus that present glandular trichome in the carpopodium.

The carpopodium is an abscission zone between the cypsela and the receptacle (Roque et al. 2009ROQUE N, KEIL DJ & SUSANNA A. 2009. Illustrated glossary of Compositae. In: FUNK VA ET AL. (Eds), Systematics, Evolution and Biogeography of Compositae, Vienna: International Association for Plant Taxonomy, p. 781-806.). According to Haque & Godward (1984)HAQUE MZ & GODWARD MBE. 1984. New records of the carpopodium in Compositae and its taxonomic use. Bot J Linn Soc 89(4): 321-340., this region can delimitate genera in Asteraceae. The carpopodium symmetry is of great taxonomic value to some tribes (Freitas et al. 2015FREITAS FS, DE-PAULA OC, NAKAJIMA JN & MARZINEK J. 2015. Fruits of Heterocoma (Vernonieae-Lychnophorinae): Taxonomic significance and a new pattern of phytomelanin deposition in Asteraceae. Bot J Linn Soc 179: 255-265., Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107., Grossi et al. 2020GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.). In Eupatorieae, studies performed by Silva et al. (2018)SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107. demonstrated that all species within of Disynaphiinae have a symmetric carpopodium, except Disynaphia praeficta (B.L.Rob.) R.M.King & H.Rob. In these studies, the assymetric carpopodium and other cypsela characteristic found in D. praeficta supported the exclusion this species from the subtribe, as well as had been demonstrated by molecular data (Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107.). The carpopodium in Eupatorieae, in general, is conspicuous, but in some species this structure can be undistinguishable, as presented in recent studies performed by Silva et al. (2018)SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107. and Grossi et al. (2020)GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.. However, in Campuloclinium, the carpopodium is present and conspicuous in all species, therefore it is a structure with no taxonomic value for species delimitation.

Anatomy

Most of the analyzed species of Campuloclinium presented five ribs. This result agrees with those of Grossi et al. (2020)GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566., who reported that having five ribs is a feature present in most Eupatorieae. However, according to Marzinek et al. (2010)MARZINEK J, DE-PAULA OC & OLIVEIRA DMT. 2010. The ribs of Eupatorieae (Asteraceae): of wide taxonomic value or reliable characters only among certain groups? Plant Sys Evol 285: 127-130., species with broader capitula had cypselae with a more uniform number of ribs while species of narrower capitula caused greater pressure between the cypselae, changing their shape. In our studies, we corroborate the hypothesis of Marzinek et al. (2010)MARZINEK J, DE-PAULA OC & OLIVEIRA DMT. 2010. The ribs of Eupatorieae (Asteraceae): of wide taxonomic value or reliable characters only among certain groups? Plant Sys Evol 285: 127-130., because the cypselae of C. chlorolepis and C. parvulum as previously reported by Calvo & Roque (2018)CALVO J & ROQUE N. 2018. Taxonomic Revision of the Neotropical Genus Campuloclinium (Eupatorieae, Compositae). Syst Bot 43(2): 602-627. they are narrower, and in our results these fruits have a variable number of ribs.

Campuloclinium species present the phytomelanin layer positioned internally to the vascular bundles, the same position found in most Eupatorieae subtribes (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., Franca et al. 2015FRANCA RO, DE-PAULA OC, CARMO-OLIVEIRA R & MARZINEK J. 2015. Embryology of Ageratum conyzoides L. and A. fastigiatum R. M. King & H. Rob. (Asteraceae). Acta Bot Bras 29: 8-15., T.D.G. Silva, unpublished data). This position of phytomelanin is also found in Ageratum conyzoides L., Ageratum fastigiatum R.M.King & H.Rob. (Ageratinae subtribe) (Franca et al. 2015FRANCA RO, DE-PAULA OC, CARMO-OLIVEIRA R & MARZINEK J. 2015. Embryology of Ageratum conyzoides L. and A. fastigiatum R. M. King & H. Rob. (Asteraceae). Acta Bot Bras 29: 8-15.), Mikania micrantha H.B.K (Mikaniinae subtribe) (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291.), Vittetia orbiculata (DC.) R.M.King & H.Rob. (Gyptidinae subtribe), and in the Praxelinae subtribe (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., T.D.G. Silva, unpublished data). However, in Disynaphiinae, the phytomelanin layer is positioned externally to the vascular bundles (Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107.). Until now, all anatomical studies with Eupatorieae cypsela (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., Franca et al. 2015FRANCA RO, DE-PAULA OC, CARMO-OLIVEIRA R & MARZINEK J. 2015. Embryology of Ageratum conyzoides L. and A. fastigiatum R. M. King & H. Rob. (Asteraceae). Acta Bot Bras 29: 8-15., T.D.G. Silva, unpublished data, Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107., present work), has been corroborated that the phytomelanin layer observed externally to the vascular bundles is a synapomorphy to Disynaphiinae, as already mentioned by Silva et al. (2018)SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107..

The position of Campuloclinium remains uncertain within Eupatorieae. King & Robinson (1987)KING RM & ROBINSON H. 1987. The genera of the Eupatorieae (Asteraceae). Monog Syst Botan 22: 1-581. placed Campuloclinium in Gyptidinae, and Robinson et al. (2009) later elucidated the relations between Campuloclinium and other genera. According to Robinson et al. (2009), Campuloclinium closely relates to Trichogonia (DC.) Gardner (Gyptidinae) and Acritopappus R.M.King & H.Rob. (Ageratinae subtribe). On the other hand, Rivera et al. (2016a)RIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300. in their studies they expand the sampling of Brazilian species of Eupatorieae suggest that Campuloclinium is closely related to Macropodina, Heterocondylus R.M.King & H.Rob., Alomiella R.M.King & H.Rob., Monogereion G.M.Barroso & R.M.King, and Ayapanopsis R.M.King & H.Rob. Indeed, the classification of several Eupatorieae subtribes is uncertain, with eight of them not monophyletic, including Gyptidinae and its genera (Rivera et al. 2016aRIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300.). The uniformity of the pericarp structure (exocarp, outer mesocarp, middle mesocarp, inner mesocarp, and position of phytomelanin in respect to vascular bundles) of Campuloclinium and other genera within Eupatorieae demonstrated that several subtribes have the same pericarp pattern. Therefore, there is a need for further evolutionary studies to understand the infratribal classification of Eupatorieae. As Grossi et al. (2020)GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566. pointed out that Eupatorieae has several tribes and genera whose circumscriptions need reevaluation. In Vernonieae, studies on anatomical cypsela performed by Marques et al. (2018a, 2020) display that the genera Chrysolaena H.Rob, Echinocoryne H.Rob, Lepidaploa (Cass.) Cass and Lessingianthus H.Rob. also have similar pericarps. In the same way, as raised for Eupatorieae by Grossi et al. (2020)GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566., Marques et al. (2018a, 2020) reinforce the importance of more morphological and phylogenetic studies, as the current circumscription of these genera should be revised (Marques et al. 2020MARQUES D, FRANCA RO, ANGULO MB, VIA DO PICO GM, DEMATTEIS M & MARZINEK J. 2020. Comparative Anatomy of Cypselae in the Complex Group Chrysolaena, Echinocoryne, Lepidaploa, and Lessingianthus: Contributions to the Systematics of Vernonieae (Compositae). Syst Bot 45: 668-680.).

A lignified pappus has been found in Eupatorieae (Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107.), Vernonieae (Marques et al. 2018a, 2020), Tageteae, and Millerieae (Frangiote-Pallone & Souza 2014FRANGIOTE-PALLONE S & SOUZA LA. 2014. Ontogenia del papus y cipsela en Asteraceae: las consideraciones structurales de la categoría tribal. Rev Mex Biodivers 85: 62-77.). In Campuloclinium, all species present lignified pappus and this feature is not relevant to its taxonomy. In general, the cypsela apex varies little in Asteraceae (Pandey & Singh 1980PANDEY AK & SINGH RP. 1980. Development and structure of seeds and fruits in tribe Vernonieae – some Vernonia and Elephantopus species. Flora 169: 443-452., Galastri & Oliveira 2010GALASTRI NA & OLIVEIRA DMT. 2010. Morfoanatomia e ontogênese do fruto e semente de Vernonia platensis (Spreng.) Less. (Asteraeceae). Acta Bot Bras 24: 73-83., Marzinek & Oliveira 2010MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291., Silva et al. 2018SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107., Marques et al. 2020MARQUES D, FRANCA RO, ANGULO MB, VIA DO PICO GM, DEMATTEIS M & MARZINEK J. 2020. Comparative Anatomy of Cypselae in the Complex Group Chrysolaena, Echinocoryne, Lepidaploa, and Lessingianthus: Contributions to the Systematics of Vernonieae (Compositae). Syst Bot 45: 668-680.), with no difference found between the apex of Campuloclinium species.

Until now, the carpopodium anatomy has shown little variation within Asteraceae (Marques et al. 2020MARQUES D, FRANCA RO, ANGULO MB, VIA DO PICO GM, DEMATTEIS M & MARZINEK J. 2020. Comparative Anatomy of Cypselae in the Complex Group Chrysolaena, Echinocoryne, Lepidaploa, and Lessingianthus: Contributions to the Systematics of Vernonieae (Compositae). Syst Bot 45: 668-680.). In some cases, as reported by Silva et al. (2018)SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107. and Marques et al. (2018a, 2020), the carpopodium exocarp lignification can be useful for species separation, but in Campuloclinium this character does not present taxonomic value because it occurs in all species.

CONCLUSION

The studies presented here have shown that the morphology and anatomy of cypselae can bring new perspectives to the cypselae evolution in Eupatorieae, as well as to the subtribal and generic classifications of this tribe. The morphological studies presented here corroborate the importance of the stipitate form of the cypsela together with other diagnostic characters (such as, hemispherical or conical, scrobiculate and glabrous receptacle) to delimit Campuloclinium within Eupatorieae, that is, stipitate cypsela, such as this feature could have evolved independently within the Trichogoniinae and Campuloclinium + Macropodina. However, phylogenetic studies with a larger sampling of Campuloclinium species must be carried out to understand their relation to these other clades. A new possible diagnostic trait presented to Campuloclinium is the trichome distribution in the cypsela, which is characterized by tector trichomes in the ribs and glandular trichomes in the interribs. The external position of the phytomelanin layer regarding the vascular bundles is also important for understanding the subtribal classification in Eupatorieae. So far, all studied subtribes have the phytomelanin layer internal to the vascular bundles, except for Disynaphiinae. The position of this layer in Campuloclinium, which is a group close to Disynaphiinae. Finally, the finding of six-celled biseriate trichomes only in C. campuloclinoides and C. hirsutum reinforces the importance of the cypselae features at a specific level.

ACKNOWLEDGMENTS

The first author would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/MEC) and the Fundação Cearense de Apoio ao Desenvolvimento Científico e tecnológico (FUNCAP) for the scholarship granted (proc. 301734/2020-8). We are grateful to the curators: Dr. Massimiliano Demmateis (CTES), Dr. Barbara Thiers (NY), Dr. Regina Célia de Oliveira (UB), Dr. Rosana Romero (HUFU) and Dr. Nádia Roque (ALCB) for providing the necessary material for the analyses. We also thank for the Laboratório Multiusuário de Microscopia Eletrônica of the Faculdade de Engenharia Química (UFU) for technical support with the SEM.

REFERENCES

  • ANDERSON LE. 1954. Hoyer’s solution as a rapid permanent mounting medium for bryophytes. Bryologist 57: 242-244.
  • ANDERSON LC. 1963. Studies on Petradoria (Compositae): Anatomy, cytology, taxonomy. Transactions of the Kansas Academy of Science 66: 632-684.
  • ANGULO MB, SOSA MM & DEMATTEIS M. 2015. Systematic significance of cypsela morphology in Lessingianthus (Vernonieae, Asteraceae). Aust Syst Bot 28: 173-189.
  • BAKER JG. 1876. Compositae. II. Eupatoriaceae. In: MARTIUS CFP & EICHLER AG Eds. Flora Brasiliensis: Vol. 6(2): 181-376, Monachii and Lipsiea: Frid. Fleischer in Comm., Monachii and Lipsiea, French and German, p. 181-398.
  • BENTHAM G. 1873. LXXXVIII. Compositae. In BENTHAM G & HOOKER JD (Eds), Genera Plantarum: Vol. 2(1), London: Lovell Reeve & Co., Williams & Norgate, London, England, p. 163-533.
  • BONIFÁCIO SKV, MOURA LL, MARZINEK J & DE-PAULA OC. 2019. Comparative embryology of Stiffia and Wunderlichia and implications for its evolution in Asteraceae. Bot J Linn Soc 189(2): 169-185.
  • CALVO J & ROQUE N. 2018. Taxonomic Revision of the Neotropical Genus Campuloclinium (Eupatorieae, Compositae). Syst Bot 43(2): 602-627.
  • CANDOLLE AP. 1836. Prodromus systematis naturalis regni vegetabilis. Vol. 5. Paris: Sumptibus Sociorum Treuttel et Würtz, 706 p.
  • FRANCA RO, DE-PAULA OC, CARMO-OLIVEIRA R & MARZINEK J. 2015. Embryology of Ageratum conyzoides L. and A. fastigiatum R. M. King & H. Rob. (Asteraceae). Acta Bot Bras 29: 8-15.
  • FRANGIOTE-PALLONE S & SOUZA LA. 2014. Ontogenia del papus y cipsela en Asteraceae: las consideraciones structurales de la categoría tribal. Rev Mex Biodivers 85: 62-77.
  • FREITAS FS, DE-PAULA OC, NAKAJIMA JN & MARZINEK J. 2015. Fruits of Heterocoma (Vernonieae-Lychnophorinae): Taxonomic significance and a new pattern of phytomelanin deposition in Asteraceae. Bot J Linn Soc 179: 255-265.
  • FUNK VA, SUSANNA A, STUESSY TF & BAYER RJ. 2009. Systematics, Evolution, and Biogeography of Compositae. Vienna: International Association for Plant Taxonomy, 965 p.
  • GALASTRI NA & OLIVEIRA DMT. 2010. Morfoanatomia e ontogênese do fruto e semente de Vernonia platensis (Spreng.) Less. (Asteraeceae). Acta Bot Bras 24: 73-83.
  • GARDNER G. 1846. Contributions towards a Flora of Brazil, being the characters of several new species of Compositae, belonging to the tribe Eupatoriaceae. London J Bot 5: 455-491.
  • GROSSI MA, BARRETO JNV, PLOS A, RODRÍGUEZ-CRAVERO JF, FORTE NB, GUTIÉRREZ DG & SANCHO G. 2020. Providing tools for the reassessment of Eupatorieae (Asteraceae): Comparative and statistical analysis of reproductive characters in South American taxa. Perspect Plant Ecol 46: 125566.
  • HAQUE MZ & GODWARD MBE. 1984. New records of the carpopodium in Compositae and its taxonomic use. Bot J Linn Soc 89(4): 321-340.
  • HESS R. 1938. Vergleichende Untersuchungen iiber die Zwillingshaare der Kompositen. Bot Jahrb Syst 68: 435-496.
  • HIND DJN & ROBINSON H. 2007. Eupatorieae. In: KADEIRET JW & JEFFREY C (Eds), The Families and Genera of Vascular Plants, Vol. 8: Flowering Plants, Eudicots, Asterales, Berlin: Springer-Verlag, Berlin, German, p. 510-574.
  • KING RM & ROBINSON H. 1970. The new synantherology. Taxon 19(1): 6-11.
  • KING RM & ROBINSON H. 1972. Studies in the Eupatorieae (Asteraceae). XC. The genus, Campuloclinium. Phytologia 24: 170-172.
  • KING RM & ROBINSON H. 1987. The genera of the Eupatorieae (Asteraceae). Monog Syst Botan 22: 1-581.
  • MARQUES D, ANGULO MB, NAKAJIMA JN & DEMATTEIS M. 2018b. The taxonomic utility of micromorphology in Lepidaploa (Vernonieae: Asteraceae). Nord J Bot 36: 1-17.
  • MARQUES D, FRANCA RO, ANGULO MB, VIA DO PICO GM, DEMATTEIS M & MARZINEK J. 2020. Comparative Anatomy of Cypselae in the Complex Group Chrysolaena, Echinocoryne, Lepidaploa, and Lessingianthus: Contributions to the Systematics of Vernonieae (Compositae). Syst Bot 45: 668-680.
  • MARQUES D, FRANCA RO, DEMATTEIS M & MARZINEK J. 2018a. Fruit of Lepidaploa (Cass.) Cass. (Vernonieae, Asteraceae): Anatomy and taxonomic implications. Acta Bot Bras 32: 642-655.
  • MARZINEK J, DE-PAULA OC & OLIVEIRA DMT. 2008. Cypsela or achene? Refining terminology by considering anatomical and historical factors. Braz J Bot 31: 549-553.
  • MARZINEK J, DE-PAULA OC & OLIVEIRA DMT. 2010. The ribs of Eupatorieae (Asteraceae): of wide taxonomic value or reliable characters only among certain groups? Plant Sys Evol 285: 127-130.
  • MARZINEK J & OLIVEIRA DMT. 2010. Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82: 279-291.
  • METCALFE CR & CHALK L. 1950. Anatomy of the Dicotyledons: Leaves, Stem, and Wood in Relation to Taxonomy with Notes on Economic Uses. Oxford: Clarendon Press, Oxford, Great Britain, 724 p.
  • METCALFE CR & CHALK L. 1979. Anatomy of the dicotyledons: volume 1. Systematic anatomy of lead and stem, with a brief history of the subject. Oxford: Clarendon Press, Oxford, Great Britain, 276 p.
  • NAKAJIMA JN, FERREIRA SC, FERNANDES AC, RIVERA VL, HATTORI EKO, QUARESMA AS, RITTER MR & Grossi MA. 2017. Tribo Eupatorieae Cass. In: ROQUE N ET AL. (Eds), A família Asteraceae no Brasil classificação e diversidade, Salvador, EDFBA, Salvador, Brasil, p. 209-230.
  • O’BRIEN TP, FEDER N & MCCULLY ME. 1964. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59: 368-373.
  • PANDEY AK & SINGH RP. 1980. Development and structure of seeds and fruits in tribe Vernonieae – some Vernonia and Elephantopus species. Flora 169: 443-452.
  • RIVERA VL, FERREIRA SC & PANERO JL. 2016b. Trichogoniinae, a new subtribe of Eupatorieae (Asteraceae). Phytotaxa 260: 296-300.
  • RIVERA VL, PANERO JL, SCHILLING EE, CROZIER BS & MORAES MD. 2016a. Origins and recent radiation of Brazilian Eupatorieae (Asteraceae) in the eastern Cerrado and Atlantic Forest. Mol Phylogenet Evol 97: 90-100.
  • ROBINSON BL. 1918. A descriptive revision of the Colombian Eupatorium’s. P Am Ac Arts Sci 54: 264-330.
  • ROBINSON H. 2009. An introduction to micro-characters of Compositae. In: FUNK VA ET AL. (Eds), Systematics, Evolution and Biogeography of Compositae, Vienna: International Association for Plant Taxonomy, Vienna, Austria, p. 89-100.
  • ROBINSON H, SCHILLING E & PANERO JL. 2009. Eupatorieae. In: FUNK VA ET AL. (Eds), Systematics, Evolution and Biogeography of Compositae, Vienna: International Association for Plant Taxonomy, Vienna, Austria, p. 731-744.
  • ROQUE N, BAUTISTA HP & MOTA AC. 2012. Taxonomic Revision of Trichogonia (Eupatorieae, Asteraceae): A South American Genus. Syst Bot 37(2): 525-553.
  • ROQUE N, KEIL DJ & SUSANNA A. 2009. Illustrated glossary of Compositae. In: FUNK VA ET AL. (Eds), Systematics, Evolution and Biogeography of Compositae, Vienna: International Association for Plant Taxonomy, p. 781-806.
  • SILVA TDG, MARZINEK J, HATTORI EKO, NAKAJIMA JN & DE-PAULA OC. 2018. Comparative cypsela morphology in Disynaphiinae and implications for their systematics and evolution (Eupatorieae: Asteraceae). Biol J Linn Soc 186: 89-107.
  • VIA DO PICO GM, VEGA AJ & DEMATTEIS M. 2016. Systematic consideration of floral microcharacters of the South American genus Chrysolaena (Vernonieae, Asteraceae). Syst Biodivers 14: 224-243.

Publication Dates

  • Publication in this collection
    27 June 2022
  • Date of issue
    2022

History

  • Received
    28 Jan 2021
  • Accepted
    4 Nov 2021
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