Grana ISSN: 0017-3134 (Print) 1651-2049 (Online) Journal homepage: https://www.tandfonline.com/loi/sgra20 An extinct species of Basella: pollen evidence from sediments (~80 ka) in Kerala, India Anjum FarooquiANJUM FAROOQUI, Joseph G. RayJOSEPH G. RAY & Arti GargARTI GARG To cite this article: Anjum FarooquiANJUM FAROOQUI, Joseph G. RayJOSEPH G. RAY & Arti GargARTI GARG (2019): An extinct species of Basella: pollen evidence from sediments (~80 ka) in Kerala, India, Grana, DOI: 10.1080/00173134.2019.1630479 To link to this article: https://doi.org/10.1080/00173134.2019.1630479 Published online: 08 Aug 2019. Submit your article to this journal Article views: 6 View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=sgra20 Grana, 2019 https://doi.org/10.1080/00173134.2019.1630479 An extinct species of Basella: pollen evidence from sediments (~80 ka) in Kerala, India ANJUM FAROOQUI1, JOSEPH G. RAY2 & ARTI GARG3 1 Birbal Sahni Institute of Palaeosciences, Lucknow, India, 2School of Biosciences, Mahatma Gandhi University, Kottayam, India, 3Botanical Survey of India, Allahabad, India Abstract The genus Basella belongs to family Basellaceae and is comprised of five species. Out of these, Basella alba is pantropical in distribution, B. paniculata is endemic to south-eastern Africa and the other three species viz. B. excavata, B. leandriana and B. madagascariensis are endemic to Madagascar. The palynological study of an organic layer buried ~80 ka in Chaganacherry, Kerala revealed a rich diversity of rainforest pollen and estuarine/marine palynomorphs indicating warm and humid climate coupled with sea level high stand. The Basella pollen recorded from this sediment shows intermediate characters of two extant Basella species. While it resembles B. paniculata in being pantocolpate (20), it shows affinity with B. alba in sexine characters. The recovered pollen was therefore, ascertained to be a new species, named here as B. keralensis sp. nov. The age correlation of the studied sediment was carried out by fingerprinting (Rare Earth Elements) of Youngest Toba Tuff (YTT) (glass shards) which spread in the atmosphere through a volcanic eruption in Sumatra ~74 ka and also with marine palynomorph markers correlating the interglacial Marine Isotopic Stage 5a (~80 ka). It is inferred that earlier, the genus Basella comprised of six species out of which Basella keralensis sp. nov. became extinct and until now neither the fossil record nor the extant form of this is known in records from any part of the World. Keywords: Basella keralensis, southern-Western Ghats, Kerala, late Quaternary The tropical montane rainforest in southern Western Ghats, Kerala (Barboni et al. 2003) is a home to many endemic floras (Pascal 1982; Pascal et al. 1982). This flora is the legacy of the Paleogene/ Neogene time period (Ramanujam 1987) and has continued to exist during Pleistocene (Prasad et al. 2009; Farooqui et al. 2010, 2014) where species extinction and migration cannot be ruled out. The vegetation affirms the presence of a monsoon-like atmospheric circulation over southern Western Ghats in India since the Middle Miocene Climate Optimum (MMCO) (Ramanujam et al. 1991; Campanile et al. 2008). Scant records of rainforest pollen taxa during Quaternary glacial and interglacial cycles are available from Arabian Sea sediments (Van Campo et al. 1982; Caratini et al. 1994; Bentaleb et al. 1997; Prabhu et al. 2004) and from Kerala (Vasanthy 1988; Narayanan et al. 2002; Kumaran et al. 2008). At present southern Western Ghats montane vegetation occupies temperate habitats at tropical latitudes. The relics of an ecoclimatic and geologic past are preserved in its pristine form and have been described as fossil rainforest ecosystem. The palynological records on land from Palani and Annamalai Hills in southern Western Ghats showed prevalence of savanna grassland vegetation during the last glacial cycle of the Quaternary (Vishnu-Mittre & Gupta 1971; Blasco & Thanikaimoni 1974; Vasanthy 1988; Gupta & Bera 1996; Rajagopalan et al. 1997). This time period was extremely adverse and could not sustain many plant species. For example, the pollen of Ongokea gore (Hua) Pierre, now confined to Congo-adjoining areas and in more humid southeast Asia was reported from marine sediment, off Kerala during Marine Isotopic Stage 5a (MIS 5a) (Farooqui et al. 2014). The palynological record shows that the present day southern Western Ghats flora rejuvenated Correspondence: Anjum Farooqui, Birbal Sahni Institute of Palaeosciences, 53, University Road, Lucknow, India. E-mail: afarooqui_2000@yahoo.com (Received 27 October 2016; accepted 25 April 2019) © 2019 Collegium Palynologicum Scandinavicum 2 A. Farooqui et al. with the onset of warm and humid conditions during the Middle Holocene (Bera & Farooqui 2000). The two sedimentary profiles studied earlier from Chaganacherry (Farooqui et al. 2010) were restudied as it had great potential to explore pollen diversity during the interglacial cycle of Pleistocene epoch. The present work elucidates morphology of new fossil Basella pollen recovered in the sediment from Chaganacherry which is typical of the genus but differs in pollen grain morphology when compared to other five extant species which are distributed world over. Study site in the southern Western Ghats, India Vazhapally in Chaganacherry, district Kottayam is situated southeast of Vembanad Lake and Alleppey coastline (Figures 1, 2). Two laterite ridges dominate the Vazhapally area, which is ~25 km from the present shoreline in the southwest coast of the Indian peninsula. The slope gradient varies from low (300 m above sea level [a.s.l.]), medium (300–650 m a.s.l.) to highlands (> 650 m a.s.l.). The vegetation is mainly tropical moist evergreen or moist deciduous, receiving 2000–3500 mm of average rainfall from the southwest and northeast monsoons (Champion & Seth 1968; Bonnefille et al. 1999). The vegetation is adapted to temperatures not exceeding 35 °C in summers and mild winters at low altitudes but cooler/misty weather conditions at high altitudes, particularly in valleys harbouring a rich biodiversity. Many plants and animals are endemic to this region and the climate and vegetation gradient from low to high altitudes is well documented (Pascal 1988; Barboni et al. 2003). Classification, distribution and habitat of Basella species The family Basellaceae is classified under the suborder Portulacineae (Kubitzki et al. 1993). Total five extant species of the genus Basella are distributed world over. Basella alba/B. rubra is pantropical in distribution (Figure 1). It grows in warm and humid climate (Swati & Agarwal 2015) and is commonly found in India, China, Malaysia, Indonesia, Philippines, southern China, New Guinea, Africa, Central America and several adjoining oceanic islands. Basella excavata Elliot, B. leandriana H. Perrier and B. madagascariensis Boivin ex Perrier are endemic to Madagascar. Basella paniculata Volkens is endemic to Kenya, Tanzania, Mozambique, Transvaal and Kwazulu-Natal in East Africa (Stannard 1988; Eriksson 2007). All the species of Basella are perennial twining herbs (climbers) having glabrous stem and succulent leaves. The sepals are greenish white or pinkish purple. The petals are green as well as white to pink purple (Kubitzki et al. 1993). It is self-pollinated and entomophilous occurring at altitudes ranging from 20 to 1350 m. The fruits are berries/drupes that are dispersed by birds. Material and methods The sedimentary soil section in Vazhapally, Chaganacherry (Figures 2, 3) is located southeast of Vembanad Lake at 8° 350ʹ N and 76° 300ʹ E. A well was dug out Figure 1. Distribution map of extant Basella species and location of extinct Basella keralensis from the Indian subcontinent. Pollen of an extinct Basella keralensis, India 3 Figure 2. Vegetation pattern in the southern peninsular part of India and location map of Chaganacherry, Kerala, India and the extent of Youngest Toba Tuff (YTT) ash dispersal (redrawn from Pattan et al. 2001). manually (2 m in diameter) for the retrieval of groundwater in Vazhapally and samples were collected for palynological investigation from the exposed sediment section. The organic matter (OM, 3 min thickness) in the well section was used for palynological study (FigFigure 3). Other layers in the entire section did not yield any pollen/spores. Random picking of 10 g sample from the unconsolidated OM layer between 13 and 13.5 m was taken for the palynological study as the maximum pollen yield was at this depth. The OM layer contained ash, carbonised seeds, plant twigs, abundant resinous matter and a strong odour of sulphur along with glass shards of Youngest Toba Tuff (YTT) (Farooqui et al. 2010). The radiocarbon age (carbon-14, 14C) of the organic carbon in bulk sediment was analysed in Birbal Sahni Institute of Palaeosciences (BSIP), Lucknow, India and calibrated following Stuiver et al. (1998). Since the radiocarbon (14C) age of the studied OM goes back to > 40 000 yr BP (Figure 3), which is beyond the limit of this methodology for dating, to ascertain the time period of the buried OM the fingerprinting of trace and rare earth elements (REE) in glass shards (Farooqui et al. 2010) was carried out using inductively coupled plasma mass spectrometry (ICP-MS) (Varian 820-MS). The REE results were in conformation with the earlier records of REE for the YTT ash that erupted ~74 ka (Rose & Chesner 1987; Chesner et al. 1991; Pattan et al. 2001). For palynology, about 10 g of sediment was treated with a warm 10% potassium hydroxide solution (in deionised water) and sieved through a 150 mesh (105 µm pore size). The filtrate was settled over- 4 A. Farooqui et al. keralensis pollen constituting 1.02% were recorded. It was observed that the morphology of the fossil pollen was intermediate, showing affinities with two extant species, i.e. B. alba/B. rubra and B. paniculata. Thus, the fossil pollen did not show resemblance with any of the five extant Basella species and therefore, it has been assigned to a status of new species. The systematic description and detailed pollen morphology is given here. Systematic palynology Family Basellaceae Genus Basella Basella keralensis sp. nov. (Figures 4A–F, 5) Etymology. — The specific epithet is derived from Kerala (India), the area of collection of the fossil sediments. Figure 3. Lithology, sediment texture and pollen percentage in the sedimentary section, Chaganacherry, Kerala, India. night and the supernatant drained. The residue was treated with 40% hydrofluoric acid and later acetolysed following Faegri and Iverson (1989). Subsequently, it was sieved through 650 mesh size (10 µm) and the residue was mounted on glass slides in glycerine jelly for palynological study under a high power light microscope (Olympus BX-51). Out of 320 total pollen counts, only four grains of Basella pollen were recovered (Figure 3). Pollen characteristics of five extant Basella species (Table I) were documented referring to Erdtman (1952), Kubitzki et al. (1993), Nowicke (1996), Punt et al. (2007), Halbritter (2015) and Halbritter et al. (2018). The reference pollen slide of B. alba L. housed in a pollen repository of the French Institute, Pondicherry (India) was also studied under a light microscope (Figure 4) for its comparison with the fossil pollen. Figures 4A–F, 5 show the light microscope images of a single fossil pollen grain of B. keralensis. A drop of homogenised maceral was mounted in glycerine medium and the identified pollen was rolled by ticking on coverslip in order to capture images in different orientation for the study of pollen morphology. Results Among all the pollen/spores recorded in the OM (Figure 3) only four grains of rare fossil Basella Holotype. — Pollen specimen BSIP Slide No. 15822. Coordinates: G 3 (Figure 4A). The slides are deposited in the museum of BSIP, Lucknow. Type locality and stratigraphic horizon. — The sediment was retrieved from a well section in Vazhapally, Chaganacherry (Figures 2, 3), Kottayam district at 8° 35ʹ N and 76° 300ʹ E, Alleppey coastline, Vembanad Lake, Kerala. Figure 3 shows the OM in which the pollen was recovered. The fingerprinting of REE of glass shards embedded in the OM layer revealed the remains of YTT indicating the deposition of sediment prior to or during this event and also coincided with the highest sea level stand on the basis of estuarine/marine palynomorph record of MIS 5a, i.e. ~80 ka (Farooqui et al. 2010; Fairbanks & Mathews 1978). Diagnostic characters. — The pollen grains of Basella keralensis sp. nov. are dice shaped (in one view), heteropolar with one axis longer, medium sized (~26 µm), pantocolpate, amb varying from rectangular/octangular to circular having ridges and grooves, colpi located on ridges, crassisexinous with perforated tectum. It is close to B. paniculata in having more number of colpate apertures, spinulose and punctate tectum (Nowicke & Skvarla 1979). It shows affinities with B. alba in apertural shape and exine pattern. It is also close to B. excavata in terms of pollen size. Detailed description of Basella keralensis (Figure 4A–F). — Grains pantocolpate, brevicolpate, colpi Table I. A comparative account of pollen morphology and morphometry of fossil grain Basella keralensis and five extant species of Basella (after Woodehouse 1935; Erdtman 1952; Nowicke & Skvarla 1979; Nowicke 1996; Halbritter et al. 2018). Pollen Characters B. alba B. paniculata (B. keralensis sp. nov. present work) Aperture number, position and character (NPC) Colpus character Hexacolpate, brevicolpate with one colpus arranged diagonally in each of the six faces of the cube. 9 – (–12) Pantocolpate, colpi very short straight, scattered on surface cutting off many ridges. Very short, sometimes irregular – 4 μm (4–5). Pantocolpate (20), colpi very short, scattered on surface cutting off many ridges. Short, narrow to slit-like, 6 μm (5–6). Very short – 4 μm (4–4.5) long, 2–2.5 μm broad. Tectum reticulate and deeply punctate, muri with or without spinules. Tectum spinulose and punctate. Complete, almost as thick as foot layer, sparsely channelled. Tectum spinulose and punctate, complete, almost as thick as foot layer. Sexine (= ectoexine) Exceedingly thick walled, rather opaque. Thick walled, twice thicker than endoexine, columella of variable size. Thick walled, twice thicker than endoexine, columella of variable size. Nexine (= Endoexine) Apertural endexine a thin layer of granules, nonapertural absent to finely granular. Uniformely thin. Surface pattern in Apertural field Large thin walled, each with one colpus. Surface psilate or minutely spinulose. almost straight. Apertural and non-apertural are similar in form of a layer of very fine granules. Not well demarcated. Exine of Apertural field Thin walled, short. Thick at ridges with elongated columellae. Thick walled, columellae variable, progressively elongated on ridges to form dome shaped buldges. Large lumen Punctae Rods or columella Occasionally with a free columellae. More circular than angular. Variable in length, short to elongate within a grain. Ending in muri; some are free; rarely projecting beyond to form spinule. Elongated along ridges, shortened nearer the apertural fields and colpus. Thin. Not fused. Thick walled, columellae variable, not of uniform length both short and long present (around the aperture). Free columellae absent. More angular than circular. Projects out of muri at places. Uniform in length. As thick as long as the thickness of foot layer. Surfaces slightly granular. Uniform, well developed, as thick or slightly thicker than tectum. Foot layer Reticuloid. Free columellae absent. More angular than circular. End in muri sometimes projecting to form spinules. Variable in length. Elongated to double length in all ridges, shortened nearer to apertural fields and colpus. Uniform, well developed, almost as thick as tectum, not fused. Hexacolpate. One colpus in each of the six faces of cube. B. leandriana 5 (5–6) B. excavata 4 (range 3–4) B. madagascariensis 5 (5–6) slit like. Psilate and deeply punctuate or more rarely with larger perforations, without spinules. Thick walled, thicker than endoexine. columella partially fused. Foot layer uniform. — Narrow, thin walled, granular or minutely spinulose, almost straight. Thin walled, granular or minutely spinulose. — — Short to elongate within a grain. — Pollen of an extinct Basella keralensis, India Surface ornamentation (tectum character) B excavata, B. leandriana and B. madagascariensis (Continued ) 5 Mostly spheroidal grains with one axis longer. The shape is a modified form of cube. Perfect cuboidal. Pollen shape Mostly spheroidal, one axis longer than the other. B. excavata 28 (range 26–31) B. leandriana 51 (43–59) B. madagascariensis 46 (43–48). Cuboidal to subcuboidal rarely almost spheroidal. Longest axis × shortest axis: 27.5 × 22 μm (range 22–28 × 21–27 μm). 42 (36–46). 31 × 31 μm (range 29–33). Pollen size Pollen Characters B. alba B. paniculata (B. keralensis sp. nov. present work) B excavata, B. leandriana and B. madagascariensis A. Farooqui et al. Table I. (Continued ). 6 Figure 4. Light microscope images of Basella keralensis (A–F, different views of a single pollen). A–D. Basella keralensis, pollen monad, medium-sized, heteropolar, pantoaperturate pollen with a dice-shaped appearance. C. Shows measurements of a single dice view and the columellae length at the ridge. E, F. Spherical shape in polar view showing about 20 pantocolpate apertures marked with ridges/bulges due to longer columellae. F. (inset) Schematic representation of four to five dices overlapping at varied angle perhaps shows the ridges of the pollen in this manner; X – spinules; Y –length of short colpi/rugae. G, H. The exine morphology and size dimensions of Basella alba (courtesy of the French Institute, Pondicherry) showing exine morphology and dice shaped grain which is typical of the genus. H. Shows measurements of the dice along with the length of the columellae at the ridge in B. alba. Scale bars – 10 µm. is 4–4.5 µm × 2–2.5 µm, up to 20 in number, sparsely and evenly distributed across the surface of the grains, arranged in four corners of the dice-shaped (Figure 4D) Pollen of an extinct Basella keralensis, India 7 Discussion Figure 5. Light microscope images of Basella keralensis. A–F. Basella keralensis: different views of the grain showing amb which exhibits much variability from quadrangular/octangular/ polygonal/circular outline in different polar views with prominent ridges corresponding to aperture number. In all the image views a reticulate, free-standing columellae is observed, near the rugae the sexine consists of low elements giving reticulate/spinulose appearance. However at a greater distance from the rugae (colpi) at the corners of the dice, very long columellae appear and the tectum gives angular perforated reticuloid pattern. At places the muri is either free or spinulated. Scale bars – 10 µm. grains as shown in different views, typical of the genus Basella. Exine crassisexinous (sexine twice as thick as the nexine), exceptionally thicker on ridges forming dome shaped bulges (ridges), very long sexinous rods appear near the ridges forming a spinulose-reticuloid surface (Figure 5A–F) at the ridge margins; columellae 2.5–2.6 µm long at ridges, reducing to 1–1.5 µm all over the grain, at ridges it is longer than two times. Tectum not continuous, angular perforations and reticulate pattern observed with muri with or without spinules at some places. Foot layer does not appear fused, intine is uniformly thin all over the grain and the pollen measures 22 µm × 26 µm. A comparative account of the five extant Basella species and the recovered fossil pollen with respect to pollen size, aperture and exine features differentiated it into a new Basella species preserved in Pleistocene sediments from Kerala, India. The pollen size in B. alba is relatively smaller and almost similar to B. excavata (26– 31 µm) followed by B. paniculata (36–46 µm) and the larger size are of B. madagascariensis (43–48 µm) and B. leandriana (43–59) as documented by Nowicke (1996). Thus, the pollen size of B. keralensis is very close to B. alba and B. excavata. The shape is perfect cuboidal in B. alba but sub-cuboidal in B. excavata, B. leandriana and B. madagascariensis, however, it is spheroidal in B. paniculata. Basella paniculata pollen is characterised by 12– 15 colpi having spinulose and punctate tectum (Nowicke & Skvarla 1979; Nowicke 1996). Except for B. paniculata, all the other four extant species have similar number of pollen apertures, i.e. six colpi (Erdtman 1952). The grains are brevicolpate and each colpi measures 4.5–6 µm long in B. paniculata. However, in B. keralensis the length of each colpi is relatively shorter (4– 4.5 µm) perhaps due to the increased number of colpi and smaller grain size as compared to B. paniculata. The surface ornamentation of pantropical B. alba pollen is similar to B. excavata, B. leandriana and B. madagascariensis but differs with B. paniculata and B. keralensis in having spinulose tectum. The length of columellae at ridges varies within all five species. In B. alba and B. keralensis the columellae at ridges are twice longer than all over the grain. In B. alba (Figure 4G, H) the columellae are 4.5 µm at the ridges and tapers to 2.5–2.6 µm in mesocolpium. In B. keralensis, the columellae at ridges are 2.5–2.6 µm, tapering to about 1.2– 1.4 µm (Figure 4C). Hence, in terms of exine characters B. keralensis is closer to B. alba. In the rest of the four extant species there is only a slight variation in the length of columellae at the aperture (Nowicke 1996) and therefore, ridges are not prominent, particularly in the B. paniculata pollen. Tectum is uniformly perforate in all species. Volkens (1907) first described B. paniculata to be comparable with B. alba; mainly because B. paniculata is described as having tectum typical of the order, punctae more angular and at places spinulate or without spinulate conditions but varied in the length of columellae at ridges. The collumellae, both at ridges near colpi and mesocolpium are relatively longer in B. alba than B. keralensis. However, the ratio of collumellae length at ridges and non-ridge area is similar in B. alba and B. keralensis as well. Based on several relevant plant morphological characters, both B. paniculata and B. alba are considered congeneric (Baker & Wright 1913; Nowicke 1996). However, the flowers of B. paniculata are very different from B. alba (Stannard 1988) and also vary in the pollen morphology. It is observed 8 A. Farooqui et al. that pollen morphological affinity of B. keralensis is with B. paniculata in respect to number of apertures which is the primary character (NPC, number position character) to classify a taxon (Woodehouse 1935; VishnuMittre 1964; Nair 1965, 1970; Walker & Doyle 1975; Perveen 2000) and with B. alba/B. rubra with respect to exine structure which is secondary in character for identification. Hence, B. keralensis exhibits intermediate character and shows closer lineage with two extant Basella species, i.e. B. paniculata and B. alba/B. rubra. It is concluded that B. keralensis occurred in India, around 80 ka perhaps when the climate was warmer and more humid than present during the interglacial cycle (MIS 5a, Shackleton [2000]) of Quaternary period. The present study therefore, confirms the existence of six species of Basella in the past, of which B. keralensis is considered as extinct until any reports of this pollen/ plant is reported in future from any part of the world. Conclusions The thin organic layer at 13–13.5 m deep sediment buried ~80 ka in a sedimentary sequence from a wellsection in Chaganacherry, Kerala, India, yielded Basella pollen of family Basellaceae. Out of the five extant species of Basella, the recovered fossil pollen shows affinity with B. paniculata in primary characters of pollen, namely number of apertures (~20 sunken, pantocolpate) but resembled B. alba in secondary characters viz. exine morphology and columellar morphometry. The fossil pollen was ascribed to a new species, B. keralensis as it was recovered from Kerala state in India and shows intermediate characters of B. paniculata and B. alba. To date, this is the first record of B. keralensis, in the geological time period and it grew until ~74 ka in the Indian sub-continent. As it has been not found elsewhere either in fossil records or as extant species it is considered as an extinct species. Thus, a total of six species of Basella occurred in the past out of which only five are living. Acknowledgements The authors thank the Director, Birbal Sahni Institute of Palaeosciences (BSIP) for granting permission to this collaborative work. The authors sincerely thank S Prasad, French Institute, Pondicherry for sparing the time to study the reference slides and provide valuable suggestions. Thanks are also due to MS Chauhan, ex-scientist, BSIP and to Director, Botanical Survey of India, Allahabad for encouragement. 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