This art icle was downloaded by: [ 177.17.57.29] On: 14 Oct ober 2014, At : 11: 33 Publisher: Taylor & Francis I nform a Lt d Regist ered in England and Wales Regist ered Num ber: 1072954 Regist ered office: Mort im er House, 37- 41 Mort im er St reet , London W1T 3JH, UK Grana Publicat ion det ails, including inst ruct ions f or aut hors and subscript ion inf ormat ion: ht t p: / / www. t andf online. com/ loi/ sgra20 Pollen morphology and taxonomic implications in Jacquemontia Choisy (Convolvulaceae) a b c Maria Teresa Buril , Paulino Pereira Oliveira , Ricardo Rodrigues , Francisco de Assis b d Ribeiro Dos Sant os & Marccus Alves a Depart ament o de Biologia, Universidade Federal Rural de Pernambuco, Recif e, Brazil b Depart ament o de Ciências Biológicas, Universidade Est adual de Feira de Sant ana, Feira de Sant ana, Brazil c Depart ament o de Sist emát ica e Ecologia, Universidade Federal da Paraíba, João Pessoa, Brazil d Depart ament o de Bot ânica, Universidade Federal de Pernambuco, Recif e, Brazil Published online: 15 Sep 2014. To cite this article: Maria Teresa Buril, Paulino Pereira Oliveira, Ricardo Rodrigues, Francisco de Assis Ribeiro Dos Sant os & Marccus Alves (2014): Pollen morphology and t axonomic implicat ions in Jacquemont ia Choisy (Convolvulaceae), Grana, DOI: 10. 1080/ 00173134. 2014. 946961 To link to this article: ht t p: / / dx. doi. org/ 10. 1080/ 00173134. 2014. 946961 PLEASE SCROLL DOWN FOR ARTI CLE Taylor & Francis m akes every effort t o ensure t he accuracy of all t he inform at ion ( t he “ Cont ent ” ) cont ained in t he publicat ions on our plat form . However, Taylor & Francis, our agent s, and our licensors m ake no represent at ions or warrant ies what soever as t o t he accuracy, com plet eness, or suit abilit y for any purpose of t he Cont ent . Any opinions and views expressed in t his publicat ion are t he opinions and views of t he aut hors, and are not t he views of or endorsed by Taylor & Francis. The accuracy of t he Cont ent should not be relied upon and should be independent ly verified wit h prim ary sources of inform at ion. Taylor and Francis shall not be liable for any losses, act ions, claim s, proceedings, dem ands, cost s, expenses, dam ages, and ot her liabilit ies what soever or howsoever caused arising direct ly or indirect ly in connect ion wit h, in relat ion t o or arising out of t he use of t he Cont ent . This art icle m ay be used for research, t eaching, and privat e st udy purposes. Any subst ant ial or syst em at ic reproduct ion, redist ribut ion, reselling, loan, sub- licensing, syst em at ic supply, or dist ribut ion in any form t o anyone is expressly forbidden. Term s & Condit ions of access and use can be found at ht t p: / / www.t andfonline.com / page/ t erm s- and- condit ions Grana, 2014 http://dx.doi.org/10.1080/00173134.2014.946961 Pollen morphology and taxonomic implications in Jacquemontia Choisy (Convolvulaceae) MARIA TERESA BURIL1, PAULINO PEREIRA OLIVEIRA2, RICARDO RODRIGUES3, FRANCISCO DE ASSIS RIBEIRO DOS SANTOS2 & MARCCUS ALVES4 Downloaded by [177.17.57.29] at 11:33 14 October 2014 1 Departamento de Biologia, Universidade Federal Rural de Pernambuco, Recife, Brazil, 2Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Feira de Santana, Brazil, 3Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, João Pessoa, Brazil, 4Departamento de Botânica, Universidade Federal de Pernambuco, Recife, Brazil Abstract Jacquemontia is one of the larger genera in Convolvulaceae, with around 120 species, and is considered taxonomically difficult. The family is eurypalynous and pollen morphology has been considered as an important taxonomic character. Pollen morphology of 43 species, representing all morphological groups of Jacquemontia, was analysed with light microscopy and/or scanning electron microscopy. Three pollen types were characterised. These pollen types do not corroborate the current circumscription of sections in Jacquemontia, which is based on inflorescence structure. Conversely, however, some macro-morphological features are discussed that support groups defined on the basis of pollen analysis. Keywords: bireticulum, Brazil, palynology, palynotaxonomy, pollen classification Pollen morphology of Convolvulaceae, which was considered a eurypalynous family by Erdtman (1952), has traditionally been used as an important taxonomic character at generic level (Sengupta 1972). Hallier (1893) proposed a classification for the family based on the pollen surface characters. He divided Convolvulaceae into two unranked groups: Echinoconieae, comprising the genera with spiny pollen, and Psiloconiae, including the genera with smooth pollen grains. Together with other characters, the diversity of pollen morphology has been useful for the separation of several pairs (or trios) of genera such as Calystegia and Convolvulus (Lewis & Oliver 1965), Stylisma and Bonamia (Lewis 1971), Merremia and Operculina (Ferguson et al. 1977), Maripa, Dicranostyles and Lysiostyles (Austin 1973a, 1973b), Odonellia and Jacquemontia (Robertson 1982). At the interspecific level, pollen is also recognised as a taxonomically valuable character in a few cases, for example in Cuscuta (Welsh et al. 2010). Sengupta (1972) and Van Campo (1976) suggested an evolutionary hypothesis for the morning glory family based on the apertures, in which tricolpate is the plesiomorphic condition and pantocolpate is apomorphic, from which the pantoporate type is derived. Tellería and Daners (2003) suggested that exine features could be more relevant than the aperture variation and divided the family in three groups: (1) tectate, punctate-microechinate-microgranulate, with columellae distally ramified; (2) tectate, punctatemicroechinate-perforate with microspines, with single columellae; and (3) semitectae, gemmate or echinatemicrogranulate-microechinate-microreticulate. Even though there are other modern and currently used tribal classifications (Staples & Brummitt 2007), pollen morphology is still considered as an important character to recognise tribes in the family. Correspondence: Maria Teresa Buril, Área de Botânica, Departamento de Biologia, Universidade Federal Rural de Pernambuco, R. Dom Manoel de Medeiros, s/n, Dois Irmãos, Recife, PE, Brazil. CEP: 52171–900. E-mail: mtburil@gmail.com (Received 26 December 2013; accepted 10 July 2014) © 2014 Collegium Palynologicum Scandinavicum Downloaded by [177.17.57.29] at 11:33 14 October 2014 2 M. T. Buril et al. Pollen characters are crucial to generic recognition of Convolvulaceae in many contemporary floras from all geographical regions: Malesia (Van Ooststroom & Hoogland 1953), China (Fang & Staples 1995), Thailand (Staples 2010), tropical East Africa (Verdcourt 1963), Cabo Verde (Gonçalves 1996), Panama (Austin 1975), Mexico (Austin & Pedraza 1983; McDonald 1993) and Ecuador (Austin 1982). Jacquemontia is one of the larger genera (c. 120 species) in the family and most of the species are Neotropical. The genus is characterised morphologically by the presence of stellate trichomes and an entire style, with two oval, flattened or cylindrical stigmatic lobes. Jacquemontia has been considered a taxonomically difficult genus, and many questions surround it (Robertson 1971; Buril 2013). Meisner (1869) and Van Ooststroom (1936) proposed four sections: Cymosae, Capitatae, Anomalae and Cephalanthae, based exclusively on inflorescence structure. However, these sections do not seem to correspond to any meaningful grouping of species when other morphological characters are considered (Buril & Alves 2011; Buril 2013). Phylogenetically, the genus had long been assigned to the tribe Convolvulae, based on morphological data (Austin 1998); more recently, molecular data placed the tribe Jacquemontiae (containing only the genus Jacquemontia) as sister to the clade Dicranostyloideae that comprises the genera with bifid styles (Stefanovic et al. 2003; Stefanovic & Olmstead 2004). The literature describes pollen aperture types in Jacquemontia in several different ways: 3-aggrecolpate by Austin (1973b) and Lewis (1971); 12-rugate by Ferguson et al. (1977); 12-pantocolpate by Manitz (1968); 3-zonocolpate by Vij and Sachdeva (1974); dodecacolpate by Sengupta (1972); and dodecaedricus by Hallier (1893). This diversity of descriptors may be partly due to multiple terms for a single pattern, and it surely reflects the different species sampled by various authors, but it also very likely indicates the presence of two aperture patterns in the genus. In fact, Tellería and Daners (2003) found two distinct aperture patterns: tricolpate and pantocolpate, with each pattern corroborated by the structure of the columellae: branched in the first and simple in the second. The surface ornamentation is referred to as perforate with microspines, without apparent variation among species (Vij & Sachdeva 1974; Tellería & Daners 2003; Vital et al. 2008). Considering the importance of pollen morphology to the classification of the family, as well as the variation reported heretofore in Jacquemontia, this study aims to provide new evidence for an assessment of infrageneric taxonomy, based on the diversity of pollen grains found in this genus. Material and methods Pollen morphology of 43 species (c. 40% of the genus), representing all morphological groups of Jacquemontia, was analysed with light microscopy (LM) and/or scanning electron microscopy (SEM). The anthers were collected from dried herbarium material or from living specimens in field trips in Brazil during the revision study of the Brazilian species of Jacquemontia (Buril 2013). For five species, information from the analysis of images on the Pollen Atlas of Convolvulaceae (Austin et al. 2008–2014) was also included. These species are J. acuminata, J. glaucescens, J. mexicana and J. polyantha, the samples of which are included in the present analysis provided only collapsed pollen grains, and J. tamnifolia, which is a widely distributed species, with the pollen morphology largely well described in the literature (Table 1). The anthers were acetolysed (Erdtman 1960), and permanent slides were mounted with glycerine jelly, and deposited in the pollen collection of the Universidade Estadual de Feira de Santana (PUEFS) collection. For SEM analysis, the samples were first treated with an alcoholic series (50%, 70%, 80%, 90% and 100% ethanol), and then subjected to a metallisation procedure. Pollen grain size, aperture size and exine thickness were measured under LM. For pollen size, the measurements were taken from 25 grains, while the exine thickness was measured from ten grains. The arithmetic mean, standard deviation and the maximum and minimum values were calculated using Excel for Windows™. Details on the surface were observed on a Jeol JEM 1230 SEM. Microspine density was determined within an area of 100 µm2. The descriptive terminology follows Punt et al. (2007). Results Based on LM and SEM observations, pollen grains are monads, apolar or isopolar, suboblate to spherical, medium to large; zonoaperturate or pantoaperturate, with 3, 6, 9, 15, c. 20 or c. 30 colpi, apertures often with a granulate membrane; columellae simple or bifid; exine tectate, sexine thicker than the nexine, with perforations and spinules, the spinules with constricted or straight base, and acute, simple to multi-tipped apex (Table I, II). Three types can be recognised. Type I. Zonocolpate, tricolpate Species in this group present mainly pollen grains with two-tipped spines. Species with straight spinule base: Jacquemontia bracteosa, J. diamantinensis, J. glaucescens, J. holosericea, J. martii, J. nodiflora, J. sphaerocephala, J. spicaeflora and J. tomentella. Pollen grains perforate tending to 3 Downloaded by [177.17.57.29] at 11:33 14 October 2014 Pollen morphology in Jacquemontia Figure 1. Pollen type I, pollen grains tricolpate. A, B. Jacquemontia bracteosa. A. Polar view. B. Detail of spinules. C. Jacquemontia diamantinensis, polar view. D. Jacquemontia holosericea, polar view. E. Jacquemontia martii, polar view. F, G. Jacquemontia nodiflora. F. Polar view. G. Surface detail. H, J. Jacquemontia sphaerocephala. H. Polar view. J. Equatorial view. K, L. Jacquemontia spicaeflora. K. Polar view. L. Surface detail. M. Jacquemontia tomentella. Scale bars – 10 µm (A, C–F, H–K), 1 µm (B, G, L, M). microreticulate, spinulose. Heterobrochate in J. holosericea, J. nodiflora and J. spicaeflora. In J. chrysanthera, the surface is wavy, with the spinules on the higher areas and perforations on the valleys. In both J. nodiflora and J. tomentella, the base of the spinules is constricted (Figure 1). Downloaded by [177.17.57.29] at 11:33 14 October 2014 4 M. T. Buril et al. Figure 2. Pollen type II, pollen grains with three, six or nine heteromorphic apertures. A, B. Jacquemontia fusca. A. Polar view. B. Two pollen grains with heteromorphic apertures. C. Jacquemontia chrysanthera, polar view. D, E. Jacquemontia staplesii. D. Overview. E. Spinules detail. F. Jacquemontia uleana, spinules detail. Scale bars – 10 µm (A, C, D), 20 µm (B), 1 µm (E, F). Type II. Zonocolpate to pantocolpate Pollen grains heteromorphic, with three, six or nine colpi. Species with spine apex one- or two-tipped: Jacquemontia blanchetii, J. chrysanthera, J. fusca, J. staplesii, J. uleana. Grains perforate, perforations with diameter heterogeneous. Jacquemontia uleana has microreticulate grains and the spinules are more than three-tipped (Figure 2). J. havanensis and J. heterantha. Both J. gracillima and J. serpyllifolia present 30 short colpi, surface irregular, with spinules on the higher areas and perforations in the valleys. Occasionally, the number of apertures can vary in J. ovalifolia with 12 and 15 colpi in pollen from the same flower (Figure 3). Type IIIB.—Pollen grains with 15 colpi, spines ≥ three-tipped, and perforations organised in circular areas, forming a bireticulum: Jacquemontia agrestis, J. decumbens, J. fruticulosa, J. guaranitica and J. sphaerostigma. Bireticulate, with spinules on the wall of suprareticulum (Figure 4). Type III. Pantocolpate Including species with usually 15, 20 or 30 colpi, distributed into connected pentagons, and usually with spines more than three-branched. Two subtypes are recognised. Type IIIA.—Pollen grains with 15, c. 20 or c. 30 colpi (rarely heteromorphic, with 12 and 15 colpi), spines two- or ≥ three-tipped, and perforations organised randomly: Jacquemontia acuminata, J. cayensis, J. corymbulosa, J. cumanensis, J. eastwoodiana, J. floribunda, J. gracillima, J. havanensis, J. heterantha, J. linarioides, J. mexicana, J. oaxacana, J. ovalifolia, J. paniculata, J. pentanthos, J. polyantha, J. pringlei, J. pycnocephala, J. selloi, J. serpyllifolia, J. smithii, J. solanifolia, J. tamnifolia. Perforate, usually tending to microreticulate, spinulose. Perforations tending to foveoles in J. cumanensis, Discussion The number of apertures in pollen grains of Convolvulaceae species has received extensive consideration. Similar to the pattern observed in other eudicots, the evolutionary sequence ‘successiformy’ (Van Campo 1976; Thanikaimoni 1986) is found. This model regards the tricolpate pollen type as plesiomorphic, while the pantocolpate and pantoporate grains are considered successively derived in the family (Manitz 1971; Sengupta 1972; Austin 1973a, 1973b, 1998; Tellería & Daners 2003). According to Furness and Rudall (2004), increasing the number of apertures might offer a selective advantage because of an improved fertilisation rate. This 5 Downloaded by [177.17.57.29] at 11:33 14 October 2014 Pollen morphology in Jacquemontia Figure 3. Pollen type IIIA, pollen grains with 15–20 colpi. A. Jacquemontia cumanensis, overview. B. Jacquemontia havanensis, overview. C. Jacquemontia heterantha, overview. D. Jacquemontia linarioides, overview. E. Jacquemontia oaxacana, overview. F. Jacquemontia ovalifolia, overview. G. Jacquemontia pentanthos, overview. H. Jacquemontia pringlei, overview. J. Jacquemontia pycnocephala, surface detail. K. Jacquemontia selloi, overview. L. Jacquemontia smithii, spinules detail. M. Jacquemontia solanifolia, columellae detail. Scale bars – 10 µm (A–H, K), 1 µm (J, K, M). variation from tricolpate to pantocolpate can be found in several genera from Dicranostyloideae, to which Jacquemontia is related, and Convolvuloideae (Lewis 1971; Sengupta 1972; Austin 1973b; Robertson 1982; Tellería & Daners 2003; Welsh et al. 2010). Downloaded by [177.17.57.29] at 11:33 14 October 2014 6 M. T. Buril et al. Figure 4. A, B. Pollen type IIIA, pollen grains with c. 30 colpi; Jacquemontia gracillima. A. Overview. B. Spinules detail. C–F. Pollen type IIIB, pollen grains 15-colpate, with bireticulum. C. Jacquemontia agrestis, overview. D. Jacquemontia decumbens, overview. E. Jacquemontia fruticulosa, columellae detail. F. Jacquemontia sphaerostigma, surface detail. Scale bars – 10 µm (A, C, D), 1 µm (B, E, F). Apertural heteromorphism is common in angiosperms (Erdtman 1966), and is found in several genera of Convolvulaceae, for example in Bonamia, Cuscuta and Merremia (Lewis 1971; Leite et al. 2005; Welsh et al. 2010). This heteromorphic condition can result from the succession of events during meiotic cytokinesis (Blackmore & Crane 1998). Till-Bottraud et al. (1999) discussed heteromorphic pollen of Violaceae: the four-aperturate grains have more chances to germinate, while the three-aperturate grains have faster pollen tube growth and better survival. This could represent a good strategy to improve the success of pollen germination and consequent ovule fertilisation. Thanikaimoni (1986) discussed the events that can lead to the increase in number of apertures due to polyploidy. In Jacquemontia, heteromorphic pollen is found in a group of South American species (J. blanchetii, J. chrysanthera, J. fusca, J. staplesii, and J. uleana). Morphologically, this group is related to the species with 3-colpate pollen, which have coriaceous sepals, with few exceptions. Most shrubby species of the genus, a minority of species within a predominantly climbing genus, are also 3-colpate or heteromorphic. An occasional heteromorphism was found in Jacquemontia ovalifolia, with 12- and 15-colpate grains in the same sample. This same variation was found in species of Bonamia (Lewis 1971). Sengupta (1972) described the pollen of Jacquemontia as 3- or 12-colpate (designated by her as dodecacolpate). However, in the 12-colpate category, Sengupta (1972) analysed only J. violacea (=J. pentanthos), which in this study was found with 15 colpi. Jacquemontia pentanthos is an extremely variable and difficult to delimit species (Buril 2013). In that context this variation in pollen aperture numbers is understandable. Now that the diversity of pollen apertures is better understood in Jacquemontia, it is possible to settle a long running dispute about the correct generic placement for the widespread neotropical species J. nodiflora (or Convolvulus nodiflorus). Based on its 3-colpate pollen, this species was long assigned to Convolvulus (Lewis & Oliver 1965; Austin 1975, 1982) who understood Jacquemontia to have exclusively aggrecolpate pollen. Other authors (O’Donell 1960; McDonald 1993; Buril 2013) placed this species in Jacquemontia, based on its stellate trichomes and other morphological characters. However, molecular data (Carine et al. 2004) showed that this species is nested within Jacquemontia; the data presented here confirm that 3-colpate pollen is actually rather common in Jacquemontia and so the placement of J. nodiflora is confirmed by pollen evidence. The 15-colpate pollen type, and its variations (20and 30-colpate), was the most common. Most species presenting this pollen type belong to section Pollen morphology in Jacquemontia Cymosae. In general, the morphology of these species is characterised by the presence of umbelliform cymes, membranaceous and unequal sepals, with the middle sepal asymmetric at the base, for example in Jacquemontia pentanthos and the Paleotropical J. paniculata. The most widespread species of the genus, J. tamnifolia, also has 15-colpate pollen; it had been placed in the section Capitatae by Meisner (1869). The highest number of apertures (30 colpi) was found in Jacquemontia serpyllifolia, endemic to Cuba, 7 and in J. gracillima (section Anomalae), a species disjunctly distributed in Brazil, Venezuela and Panama (Robertson 1971). Jacquemontia serpyllifolia is morphologically most similar to the Central American species (in the section Cymosae), in which case the 30-colpate pollen could be independently derived. The average size of pollen in Jacquemontia is between 40 and 80 µm, comparable to what is found in most genera of Convolvulaceae with nonspiny pollen (Sengupta 1972; Tellería & Daners Table I. Species of Jacquemontia analysed and pollen morphometric values. Downloaded by [177.17.57.29] at 11:33 14 October 2014 Species J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. abutiloides acuminataa agrestis blanchetii bracteosa cayensis chrysanthera corymbulosa cumanensis decumbens diamantinensis eastwoodiana floribunda fruticulosa fusca glaucescensa gracillima guaranitica havanensis heterantha holosericea linarioides martii mexicanaa nodiflora oaxacana ovalifolia paniculataa pentanthos polyanthaa pringlei pycnocephala selloi serpyllifolia smithii solanifolia sphaerocephala sphaerostigma spicaeflora staplesii tamnifoliaa tomentella uleana PD (µm) 54.8 ± 58.0 59.8 ± 65.9 ± 60.4 ± 63.6 ± 49.7 ± 60.0 ± 75.0 ± 62.2 ± 49.7 ± 56.6 ± 65.9 ± 63.05 ± 54.55 ± 60.0 63.6 ± 49.3 ± 55.7 ± 59.1 ± 61.6 ± 64.3 ± 45.2 ± 45.0 63.8 ± 71.5 ± 50.5 ± 60.0 66.0 ± 45.0 61.0 ± 54.7 ± 70.55 ± 64.9 ± 50.8 ± 66.5 ± 56.2 ± 64.75 ± 57.3 ± 52.6 ± 55.0 32.75b 78.1 ± 0.56 0.52 0.63 0.96 0.65 0.71 0.46 0.88 0.58 0.71 0.65 1.37 0.94 0.87 0.52 0.34 0.51 1.05 0.86 0.67 0.54 0.97 0.91 0.54 0.64 0.65 0.44 0.64 0.79 0.49 0.61 0.63 0.68 1.38 0.60 0.78 ED (µm) — — — — 82.0 ± — 65.8 ± — — — 65.8 ± — — — 61.40 ± n.o. — — — — 73.6 ± — 56.3 ± — 76.9 ± — — — — — — — — — — — 65.0 ± — 66.5 ± — — 47.25b — 1.19 0.50 0.50 0.71 0.98 0.46 1.15 0.76 1.20 EDp (µm) — — — — 80.6 ± — 65.1 ± — — — 65.1 ± — — — 61.65 ± n.o. — — — — 74.5 ± — 56.5 ± — 79.1 ± — — — — — — — — — — — 65.4 ± — 70.8 ± — — 48.9 ± — 1.45 0.70 0.70 0.46 1.05 0.54 0.85 0.55 1.50 0.46 Exine (µm) DS Sections 4.15 n.o. 5.0 5.6 5.5 5.0 5.0 4.5 6.0 4.6 5.1 4.0 5.0 4.7 5.4 n.o. 5.1 4.1 5.0 4.2 5.3 5.8 5.0 40 62 41 64 185 29 98 25 20 38 30 38 39 119 37 57 34 135 22 55 18 53 73 32 14 36 39 19 30 42 77 30 28 79 42 150 44 44 74 90 45 37 21 CY CY AN CY CA CY CY CY AN AN CY CY CY AN CA CY AN AN AN AN CY AN CY CY CY CY AN CY CY CY CY CY CY AN AN CY CA CY CA CP CA CY CY 7.7 5.6 4.1 n.o. n.o. n.o. 5.2 4.0 4.65 5.2 4.1 5.4 5.3 4.8 7.0 4.2 5.5 5.9 Note: PD, polar diameter; ED, equatorial diameter; EDp, equatorial diameter in polar view; DS, density of spines; AN, Anomalae; CY, Cymosae; CA, Capitatae; CP, Capituliflorae; n.o., not observed. a Data according to images posted on Austin et al. (2008–2014). b Measurements made from ten pollen grains. 8 M. T. Buril et al. 2003). Welsh et al. (2010) indicated that the pollen size in Cuscuta may be associated with chromosome size, ploidy level and nuclear genome size. However, this connection remains unexplored in Jacquemontia. Regarding the shape, the grains in Jacquemontia are polymorphic. Tricolpate pollen grains are usually prolate or oblate; as the number of apertures increases the grains become spheroidal, a derived condition according to Austin (1998). In general, the tectum in the pollen grains of the studied species is characterised as perforate and with spinules. However, the perforate tectum in several species tends toward a foveolate or microreticulate pattern. This transition from perforate to reticulate is Table II. Characterisation of ornamentation and number of apertures in pollen grains of Jacquemontia species. Downloaded by [177.17.57.29] at 11:33 14 October 2014 Species J. J. J. J. J. J. J. abutiloides acuminataa agrestis blanchetii bracteosa cayensis chrysanthera J. J. J. J. J. J. J. J. J. J. corymbulosa cumanensis decumbens diamantinensis eastwoodiana floribunda fruticulosa fusca glaucescensa gracillima Number of apertures Ornamentation 15 15 15 3, 6, 9 3 15 3, 6 Perforate, spinulose Perforate, spinulose Bireticulate, with spinules on the walls of the suprareticulum Perforate, spinulose Perforate tending to microreticulate, spinulose Perforate, spinulose Perforate tending to microreticulate, spinulose the surface is wavy, with the spinules on the higher areas and perforations on the valleys Perforate, perforations with heterogeneous diameters, spinulose Perforate, tending to foveolate, spinulose Bireticulate, with spinules on the walls of the suprareticulum Perforate tending to microreticulate, spinulose Perforate, spinulose Perforate, spinulose, perforations with different sizes Bireticulate Perforate, tending to microreticulate, spinulose Perforate tending to microreticulate, spinulose Perforate, tending to foveolate, spinules on the higher areas and perforations on the valleys Bireticulate Perforate, tending to foveolate, spinules on the higher areas and perforations on the valleys Perforate, tending to foveolate, spinules on the higher areas and perforations on the valleys Bireticulate Perforate tending to microreticulate, heterobrochate, spinulose Perforate, spinulose Perforate tending to foveolate, spinulose Perforate, spinulose Perforate, tending to microreticulate, heterobrochat; spinules with different diameters Perforate, perforations with heterogeneous diameters Perforate, spinulose; perforations with heterogeneous diameters; base of the spinules with heterogeneous diameters Perforate, perforations with heterogeneous diameters, spinulose Perforate, perforations with heterogeneous diameters, spinulose Perforate, perforations with heterogeneous diameters, spinulose Microreticulate, spinulose Perforate, spinulose Perforate, spinulose Perforate, spinulose Perforate, spinulose Perforate, spinulose Perforate tending to microreticulate, spinulose Bireticulate Perforate tending to microreticulate, heterobrochate, spinulose Perforate, perforations with heterogeneous diameters, spinulose Perforate, perforations with heterogeneous diameters, spinulose Microreticulate, spinulose Microreticulate, spinulose 15 15 15 3 c. 20 15 15 3 3 c. 30 J. guaranitica J. havanensis 15 15 J. heterantha 15 J. J. J. J. J. J. 15 3 15 3 15 3 heterotricha holosericea linarioides martii mexicanaa nodiflora J. oaxacana J. ovalifolia J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. J. a paniculataa pentanthos polyanthaa pringlei pycnocephala selloi serpyllifolia smithii solanifolia sphaerocephala sphaerostigma spicaeflora staplesii tamnifolia tomentella uleana 15 12 15 15 15 15 15 15 c. 30 15 15 3 15 3, 6, 9 3, 6, 9 15 3 3, 6, 9 Data according to images posted on Austin et al. (2008–2014). Downloaded by [177.17.57.29] at 11:33 14 October 2014 Pollen morphology in Jacquemontia an evolutionary trend in angiosperms in general (Doyle 2005) and was also observed within Convolvulaceae (Sengupta 1972). The variation found in Jacquemontia, cannot be associated with other characters, neither palynological nor morphological. The presence of a bireticulum in Jacquemontia agrestis, J. decumbens, J. fruticulosa and J. sphaerostigma represents an apparent synapomorphy (Elsam 2008). Due to the inflorescence morphology of J. sphaerostigma, it was placed in a distinct section (sect. Cymosae) from the other three species (sect. Anomalae). However, if other morphological characters are analysed, e.g. the presence of glandular trichomes, the relationship of J. sphaerostigma with J. agrestis, J. decumbens and J. fruticulosa is comprehensible (Austin 1982). Even though it was not possible to analyse the columellae of all species studied, the correlation found by Tellería and Daners (2003), between single columellae and the pantocolpate grains, is not supported in Jacquemontia. In fact, while most species present single and stout columellae, J. ovalifolia (12–15 colpi) presents both single and ramified. The morphology of spines was described by Sengupta (1972) to distinguish the species in the ‘echinate group’ (e.g. tribe Ipomoeae). Tellería and Daners (2003) stated that the spine shape of Ipomoea pollen is difficult to describe because of intraspecific variation observed in several species. In Jacquemontia differences were observed in the shape and ramification of spinules. However, we do not suggest that spinule morphology is a taxonomically valuable character because there may be infraspecific variation in spinules similar to that observed in Ipomoea by Tellería and Daners (2003) and, furthermore, the spinule morphology can only be observed under very high magnification under SEM. Ferguson et al. (1977) examined the pollen grains of Operculina and Merremia species and concluded that there is no correlation between pollen morphology and subgeneric classification. Welsh et al. (2010), studying the pollen evidence for Cuscuta phylogeny, concluded that although pollen alone is not enough to reconstruct the history of this genus, it is a useful character for species level recognition. Pollen type itself might not be enough to propose an infrageneric classification in Jacquemontia. However, considering other morphological characters (Buril 2013) in addition to pollen features, it is clear that the sections based only on inflorescence morphology do not correspond to any meaningful groups of species. Conclusion Pollen in Jacquemontia is diverse, varying from the presumed plesiomorphic condition in Convolulaceae 9 (the 3-colpate grain), through successively higher numbers of apertures, to the apomorphic (pantocolpate) type. The existing sectional classification, based on inflorescence structure, is not correlated with palynological characters. However, pollen characters such as the presence of a bireticulum do correlate with macromorphological features (bract characters, presence of glandular trichomes), which suggests that an expanded character analysis could lead to a much improved infrageneric classification in future. Acknowledgements MTB is indebted to Fundação de Apoio à Ciência e Tecnologia do estado de Pernambuco (FACEPE), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and International Association for Plant Taxonomy (IAPT) for funding her PhD project; and to Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, for the use of the scanning electron microscope; to Daniel Austin and an anonymous reviewer that made valuable suggestions to this work; to George Staples for critically reviewing and improving the text. Specimens investigated Jacquemontia abutiloides Benth. México: Baja California. Carter A, 14 March 1961. NY 4782 (NY). Jacquemontia acuminata Rusby. Bolivia: Espirito Santo. A. M. Bang 1263, November 1983 (M). Jacquemontia agrestis (Mart. ex Choisy) Meissn. Brazil: Paraíba, São João do Cariri. M. T. Buril 358, 14 February 2010 (UFP). Jacquemontia blanchetii Moric. Bolivia. Mroginskie 754, March 1877 (P). Jacquemontia bracteosa Meisn. Brazil: Bahia, Feira de Santana. J. R. Noblick 2064, 8 October 1982 (HUEFS). Jacquemontia cayensis Britton. Bahamas: Grand Bahama. D. S. Correll 51309, 10 May 1980 (NY). Jacquemontia chrysanthera Buril. Brazil: Bahia, Abaíra. M. T. Buril 224, February 2009 (UFP). Jacquemontia corymbulosa Benth. Brazil: Pernambuco, Buíque. M. T. Buril 394, 18 May 2009 (UFP). Jacquemontia cumanensis Kuntze. United States: St John. N. L. Britton 289, February 1913 (MO). Jacquemontia decumbens O’Donell. Argentina. G. J. Schwarz 5553, 1934 (NY). Jacquemontia diamantinensis Buril. Brazil: Bahia, Igatu. M. T. Buril 227, 24 June 2009 (UFP). Jacquemontia eastwoodiana I.M.Johnst. Mexico: Baja California, Sierra de La Giganta. A. Carter 4782, 18 October 1964 (NY). Jacquemontia floribunda (Kunth.) Hallier f. Peru. T. Plowman 14220, 1962 (P). Jacquemontia fruticulosa Hallier f. Paraguai: Missiones. H. S. Irwin 31906, March 1965 (SP). Jacquemontia fusca Hallier. Brazil: Goiás, Luziania. 6 April 1991; E. Melo 567 (HUEFS). Jacquemontia glaucescens Choisy. Brazil: Bahia. Blanchet 3164, 1859 (P). Jacquemontia gracillima (Choisy) Hallier f. Brazil: Pernambuco, Salgueiro. M. T. Buril 290, 15 April 2009 (UFP). Downloaded by [177.17.57.29] at 11:33 14 October 2014 10 M. T. Buril et al. Jacquemontia guaranitica Hassl. Paraguay: Missiones. D. R. Kunth 5814, February 1945 (G). Jacquemontia havanensis (Jacq.) Urb. Cuba. Bucher 153, December 1939 (NY). Jacquemontia heterantha (Nees et Mart.) Hallier f. Brazil: Bahia, Manoel Vitorino. E. Melo 6118, 21 September 2009 (HUEFS). Jacquemontia holosericea (Weinm.) O’Donell. Brazil: Rio de Janeiro. G. Lott 02, 7 December 1975 (RB). Jacquemontia linarioides Meisn. Brazil: Bahia. A. Krapovickas 45051, June 1970 (SP). Jacquemontia martii Meisn. Brazil: Alagoas, Quebrangulo. M. T. Buril 387, October 2011 (UFP). Jacquemontia mexicana (Loes.) Standl. et Steyerm. Mexico: Oaxaca. E. Narvaez 1253, 25 February 1982 (NY). Jacquemontia nodiflora (Desr.) G.Don. Brazil: Bahia, Jacobina. M. T. Buril 376, 15 April 2009 (UFP). Jacquemontia oaxacana (Meisn.) Hallier f. México: Vera Cruz. H. Ross 610, October 1966 (MO). Jacquemontia ovalifolia (Choisy) Hallier f. Porto Rico. Britton 9451, 25 December 1929 (NY). Jacquemontia paniculata (Brum. f.) Hallier f. China: Hainan. Cuming 645 (MO). Jacquemontia pentanthos (Jacq.) G.Don. Brazil: Ceará: Milagres. M. T. Buril 316, 14 May 2009 (UFP). Jacquemontia polyantha Hallier f. Mexico: Sinaloa. Y. Mexia 912, 14 October 1926 (NY). Jacquemontia pringlei A.Gray. United States: Arizona. C. G. Pringle 1970, 1884 (NY). Jacquemontia pycnocephala Benth. Mexico. G. B. Hinton 12604, 18 November 1938 (NY). Jacquemontia selloi Hallier f. Brazil: Rio Grande do Sul. G. Hatschbach 32958, 20 November 1968 (SP). Jacquemontia serpyllifolia Urb. Cuba: Havana. P. Wilson 11634, 4 January 1912 (NY). Jacquemontia smithii B.L.Rob. et Greenm. Mexico: Puebla. H. D. Hipley 14717, 17 November 1966 (NY). Jacquemontia solanifolia (L.) Hallier f. Puerto Rico. H. Alain & O. Liogier 29854, 28 October 1994 (BM). Jacquemontia sphaerocephala Meisn. Brazil: Minas Gerais, Lagamar. M. Brandão 23465, 12 December 1992 (SP). Jacquemontia sphaerostigma (Cav.) Rusby. Brazil: Minas Gerais, Joaquim Felício. E. B. Souza 1060, 30 March 2005 (HUEFS). Jacquemontia spicaeflora Hallier f. Brazil: Goiás, Caldas Novas. E. P. Heringer 16677, 6 January 1977 (UB). Jacquemontia staplesii Buril. Brazil: Bahia, Abaíra. W. Ganev 3295, 2 June 1994 (HUEFS). Jacquemontia tamnifolia (L.) Benth. United States: Alabama. S. R. Hill 21888, 26 August 1966 (NY). Jacquemontia tomentella (Miq.) Hallier f. Sumatra: Djambi. Posthumus 1017, March 1928 (SING). Jacquemontia uleana Hallier f. Brazil: Bahia, Barra do Mendes. M. L. Guedes 8177, 27 January 2001 (HUEFS). References Austin DF. 1973a. The American Erycibeae (Convolvulaceae). Maripa, Dicranostyles, and Lysiostyles I. Systematics. Annals of the Missouri Botanical Garden 60: 306–412. doi:10.2307/ 2395089. Austin DF. 1973b. The American Erycibeae (Convolvulaceae). Maripa, Dicranostyles and Lysiostyles. II. Palynology. Pollen et Spores 15: 203–226. Austin DF. 1975. Convolvulaceae. In: Woodson RE, Schery RW, eds. Flora of Panama. Annals of the Missouri Botanical Garden 62: 157–224. Austin DF. 1982. Convolvulaceae. In: Harling G, Sparre B, eds. Flora of Ecuador, 15. Göteborg: Opera Botanica. Austin DF. 1998. Parallel and convergent evolution in the Convolvulaceae. In: Mathews P, Sivadasan M, eds. Biodiversity and taxonomy of tropical flowering plants, 201–234. Calicut: Mentor Books. Austin DF, Pedraza RA. 1983. Los generos de Convolvulaceae en Mexico. Boletín de la Sociedad Botanica de Mexico 44: 3–16. Austin DF, Staples G, Carine M. 2008–2014. Convolvulaceae pollen atlas. http://cals.arizona.edu/herbarium/sites/cals.arizo na.edu.herbarium/files/old_site/assoc/projects/convolv/Conv olvulaceae_Pollen_Atlas.htm; accessed 27 June 2014. Blackmore S, Crane PR. 1998. The evolution of apertures in the spores and pollen grains of embryophytes. In: Owens SJ, Rudall PJ, eds. Reproductive biology, 159–182. Kew: Royal Botanic Gardens. Buril MT. 2013. Sistemática e filogenia de Jacquemontia Choisy (Convolvulaceae). PhD Thesis, Universidade Federal de Pernambuco, Recife, Brazil. Buril MT, Alves M. 2011. A new species of Jacquemontia (Convolvulaceae) from north-eastern Brazil. Brittonia 63: 436–441. doi:10.1007/s12228-011-9188-y. Carine M, Russell SJ, Santos-Guerra A, Francisco-Ortega J. 2004. Relationships of the Macaronesian and Mediterranean floras: Molecular evidence for multiple colonizations into Macaronesia and back-colonization of the continent in Convolvulus (Convolvulaceae). American Journal of Botany 91: 1070–1085. doi:10.3732/ajb.91.7.1070. Doyle JA. 2005. Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana 44: 227–251. doi:10.1080/00173130500424557. Elsam JE. 2008. Reassessment of the tribal and generic delimitation of Convolvuleae (Convolvulaceae) based on ITS and trnH-psbA sequences, and on morphological characters. PhD thesis, Imperial College, London, UK. Erdtman G. 1952. Pollen morphology and plant taxonomy. Angiosperms. Stockholm: Almqvist and Wiksell. Erdtman G. 1960. The acetolysis method. A revised description. Svensk Botanisk Tidskrift 39: 561–564. Erdtman G. 1966. Sporoderm morphology and morphogenesis. A collocation of data and suppositions. Grana Palynologica 6: 317–323. doi:10.1080/00173136609430030. Fang RC, Staples G. 1995. Convolvulaceae. In: Raven P, Wu CY, eds. Flora of China, 16, 271–325. Beijing: Science Press. Ferguson IK, Verdcourt B, Poole MM. 1977. Pollen morphology in the genera Merremia and Operculina (Convolvulaceae) and its taxonomic significance. Kew Bulletin 31: 763–773. doi:10.2307/4109548. Furness CA, Rudall PJ. 2004. Pollen aperture evolution – a crucial factor for eudicot success? Trends in Plant Science 9: 154–158. doi:10.1016/j.tplants.2004.01.001. Gonçalves ML. 1996. Convolvulaceae. In: Paiva J, ed. Flora de Cabo Verde: Plantas vasculares. Lisboa: Instituto de Investigaçã o Científica Tropical. Hallier H. 1893. Versuch einer natürlichen Gliederung der Convolvulaceen auf morphologischer und anatomischer Grundlage. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 16: 453–591. Leite K, Simão-Bianchini R, Santos F. 2005. Morfologia polínica de espécies do gênero Merremia Dennst. (Convolvulaceae) ocorrentes no estado da Bahia, Brasil. Acta Botanica Brasilica 19: 313–321. doi:10.1590/S0102-33062005000200014. Lewis WH. 1971. Pollen differences between Stylisma and Bonamia (Convolvulaceae). Brittonia 23: 331–334. doi:10.2307/2805701. Lewis WH, Oliver RL. 1965. Realignment of Calystegia and Convolvulus (Convolvulaceae) in Taiwan. Annals of the Missouri Botanical Garden 52: 217–222. doi:10.2307/2394871. Downloaded by [177.17.57.29] at 11:33 14 October 2014 Pollen morphology in Jacquemontia Manitz H. 1968. Beiträge zur Pollenmorphologie der Convolvulaceae s.l. Wissenschaftliche Zeitschrift der FriedrichSchiller Universität Jena/Thüringen. Mathematisch-naturwissenschaftliche Reihe 17: 387–390. Manitz H. 2008. Beiträge zur Pollenmorphologie und Systematik der Convolvulaceen-Gattungen Maripa und Mouroucoa. Feddes Repertorium 82: 167–181. doi:10.1002/fedr.19710820205. McDonald JA. 1993. Convolulaceae I. In: Sosa V, ed. Flora de Veracruz, 73, 1–99. Xalapa: Instituto de Ecología. Meisner CF. 1869. Convolvulaceae. In: Martius CFP, Eichler AG, eds. Flora Brasiliensis, 7, 199–370. Leipzig: Fleischer. O’Donell CA. 1960. The Peruvian species of Jacquemontia. Lilloa 89: 71–105. Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A. 2007. Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143: 1–81. doi:10.1016/j. revpalbo.2006.06.008. Robertson KR. 1971. A revision of the genus Jacquemontia (Convolvulaceae) in North and Central America and the West Indies. PhD Thesis, Washington University, Saint Louis, United States of America. Robertson KR. 1982. Odonellia, a new genus of Convolvulaceae from tropical America. Brittonia 34: 417–423. doi:10.2307/ 2806498. Sengupta S. 1972. On the pollen morphology of Convolvulaceae with special reference to taxonomy. Review of Palaeobotany and Palynology 13: 157–212. doi:10.1016/0034-6667(72)90030-9. Staples GW. 2010. Convolvulaceae. In: Santisuk T, Larsen K, eds. Flora of Thailand, 330–468. Bangkok: Royal Forest Department. Staples GW, Brummitt RK. 2007. Convolvulaceae. In: Heywood VH, Brummitt RK, Culham A, Seberg O, eds. Flowering plant families of the world, 108–110. Kew: Royal Botanic Gardens. Stefanovic S, Austin DF, Olmstead RG. 2003. Classification of Convolvulaceae: A phylogenetic approach. Systematic Botany 28: 791–806. Stefanovic S, Olmstead RG. 2004. Testing the phylogenetic position of a parasitic plant (Cuscuta, Convolvulaceae, Asteridae): 11 Bayesian inference and the parametric bootstrap on data drawn from three genomes. Systematic Biology 53: 384–399. doi:10.1080/10635150490445896. Tellería MC, Daners G. 2003. Pollen types in southern New World Convolvulaceae and their taxonomic significance. Plant Systematics and Evolution 243: 99–118. doi:10.1007/ s00606-003-0069-z. Thanikaimoni G. 1986. Pollen apertures: Form and function. In: Blackmore S, Ferguson IK, eds. Pollen and spores: Form and functions, 119–136. London: Academic Press. Till-Bottraud I, Vincent M, Dajoz I, Mignot A. 1999. Pollen aperture heteromorphism. Variation in pollen-type proportions along altitudinal transects in Viola calcarata. Comptes Rendus de l’Académie des Sciences - Series III - Sciences de la vie 322: 579–589. doi:10.1016/S0764-4469(00)88528-5. Van Campo M. 1976. Patterns of pollen morphological variation within taxa. In: Ferguson IK, Muller J, eds. The evolutionary significance of the exine, 125–135. London: Academic. Van Ooststroom SJ. 1936. Beiträge zur Kenntnis der südamerikanischen Convolvulaceen. Recueil des Travaux Botaniques Néerlandais 33: 211–221. Van Ooststroom SJ, Van Hoogland RD. 1953. Convolvulaceae. In: Van Steenis CGGJ, ed. Flora Malesiana, 1, 388–512. Jakarta: Noordhoff-Kolff. Verdcourt B. 1963. Convolvulaceae. In: Hubbard CE, Redhead RM, eds. Flora of Tropical East Africa, London: Crowns Agent. Vij SP, Sachdeva VP. 1974. Pollen grain studies in some Indian Convolvulaceae. Journal of Palynology 10: 132–344. Vital MTAB, Santos FAR, Alves M. 2008. Diversidade palinológica das Convolvulaceae do Parque Nacional do Catimbau, Buíque, PE, Brasil. Acta Botanica Brasilica 22: 1163–1171. doi:10.1590/S0102-33062008000400027. Welsh M, Stefanović S, Costea M. 2010. Pollen evolution and its taxonomic significance in Cuscuta (dodders, Convolvulaceae). Plant Systematics and Evolution 285: 83–101. doi:10.1007/ s00606-009-0259-4.