© 2018 The Mendel Society Cytologia 83(3): 223–228

Cytologia Focus:

Karyotype and Chromosome Behavior Analyses in Three Regions of the Indomalayan Realm

Shigeyuki Kawano*

Functional Biotechnology PJ, Future Center Initiative, The University of Tokyo, Wakashiba, Kashiwa, Chiba 277–0871, Japan

Received August 23, 2017; accepted September 6, 2018

Summary The Wada Memorial Award was created in 2011 to encourage the submission of high-quality papers to Cytologia. Coincidentally, the first to fourth holders of the award were experts in karyotype and chromosome analyses among the three regions of the Indomalayan . Most of Indomalaya was originally covered by tropical and subtropical moist broadleaf forests, with high biodiversity that is currently at risk due to various anthropogenic influences. Karyotype and chromosome analyses provide an essential foundation for main- taining biodiversity through conservation; therefore, in this paper, we focus recent their contributions of the early Wada Memorial Award winners to the three regions of Indomalayan

Key words Chromosome behavior, Endangered species, Endemic species, Indomalaya, Karyotype.

Biogeographic realms are large spatial regions within and R. C. Gupta at the Department of Botany of Punjabi which ecosystems share a broadly similar biological evo- University (Fig. 1A), have been studying the ploidy and lutionary history (Udvardy 1975). Eight terrestrial bio- meiosis of plants in North (Saggoo and Kaur 2016, geographic realms, corresponding roughly to continents, Gupta et al. 2017a). North India is located mainly on are typically recognized. Holt et al. (2013) recently continental India, north of peninsular India. Toward its proposed 11 biogeographic realms according to the dis- north are the , which define the boundary be- tribution of organisms and the phylogenic relationships tween the and the Tibetan plateau. among 21037 taxa of amphibians, birds, and mammals. To its west is the , shared between North In- The Indomalayan biogeographic realm extends across dia and , and the Aravalli Range, beyond which most of South and into the southern parts lies the Indian state of Gujarat. The Vindhya Mountains of (Fig. 1). Three distinctive characteristic are, in some interpretations, taken to be the southern areas within this realm have received particular attention boundary of North India. in Cytologia; these are North India, including Himalaya; The predominant geographical features of North India downstream of the Ganges and Brahmaputra (including Punjab) are the following three regions: the Rivers and around their delta; and , including Indo-Gangetic plain, which spans the states of Punjab, the Indochina Peninsula and the Northern Malay Penin- Haryana, Uttar Pradesh, and Bihar (Gupta et al. 2017a). sula. Research groups are actively performing karyotype The Himalayas, which span three states, , analysis of local plants and animals in these regions. Himachal Pradesh, and Jammu and Kashmir, contain Four professors (Dr. Sheikh Shamimul Alam† at Dhaka many endemic species: Impatiens devendrae Pusalkar University, Bangladesh; Dr. Alongklod Tanomtong at (Kumar and Singhal 2016b) and Meconopsis aculeata Khon Kaen University, Thailand; and Drs. Vijay Kumar Royle (Kumar et al. 2016) in Uttarakhand, some mem- Singhal and Raghbir Chand Gupta at Punjabi University, bers of subclass Gamopetalae (Gupta et al. 2016a), India) representing these research groups each won the Achillea millefolium L. (Kaur et al. 2017), Astragalus Wada Memorial Award for their achievements from rhizanthus Royle ex Benth. (Kumar and Singhal 2016a), 2011 to 2014. Sedum oreades (Decne) R. Hamet (Kumar and Singhal 2016b), species of the genus Clematis L. (Kumar et al. North India, including Himalaya 2017), Melica persica Kunth (Kumari and Saggoo Several research groups, led mainly by V. K. Singhal 2016), Eremurus himalaicus Baker (Kumari and Sag- goo), Angelica glauca Edgew (Rani et al. 2016), Pteris * Corresponding author, e-mail: [email protected] cretica L. (Saggoo and Kaur 2017a), Adiantum DOI: 10.1508/cytologia.83.223 lunulatum Burm (Saggoo and Kaur 2017b), †Professor Dr Sheikh Shamimul Alam of Botany Department at Dhaka University (DU) died at a hospital in on 18 De- Anthoxanthum odoratum L. (Singhal and Kumari 2017), cember 2017. He was 57. some dicots (Singhal et al. 2016b), and Neurobasis 224 S. Kawano Cytologia 83(3)

Fig. 1. Three regions (A, B, and C) within the Indomalayan biogeographic realm; these regions are further classified into five : green, ; dark ocher, tropical and subtropical dry broadleaf forests; yellow-green, tropical and subtropical coniferous forests; light ocher, deserts and xeric ; and pink, . chinensis L. (Walia et al. 2016) in Himachal Pradesh. germplasms. Various breeding procedures, such as hy- Species endemic to Jammu and Kashmir include bridization, mutation, and polyploidy breeding, are used Angelica glauca Edgew. (Rani et al. 2016), Lavatera to increase germplasm variability; these procedures rely cachemiriana Cambess (Saggoo et al. 2017), Heracleum on accurate quantification and qualification of genetic pinnatum C. B. Clarke (Singhal et al. 2016a), Tanacetum variability. Karyotype analysis provides preliminary artemisioides Sch. Bip. ex Hook. f. (Singhal et al. information about the genome of a specimen. It is stable 2016c), Physochlaina praealta (Decne) Miers (Singhal and specific to each individual. Probably due to the large et al. 2017). North India also encompasses the Thar number and small size of chromosomes, it was not possi- Desert, which lies mainly in the state of Rajasthan. ble to determine detailed karyotypes until recently. Endemic species of this desert include Abutilon indicum Conventional karyotype analysis alone remains unable (L.) Sweet (Gill and Kaur 2016), some members of the to express critical differences among species if they Agrostideae and Eragrosteae tribes (Gupta et al. 2017a, possess similar 2n chromosome numbers or other karyo- 2017b), and some members of the Paniceae tribe (Kaur type parameters. In such cases, a combination of modern and Gupta 2016). cytogenetic and molecular techniques is necessary to compare chromosomes between species. Professor Dr. Bangladesh downstream of the Ganges and Brahmapu- Sheikh Shamimul Alam† and his coworkers at the Bota- tra Rivers and around their delta ny Department at Dhaka University (Fig. 1B) have Bangladesh is located almost at the center of Indo- revealed the genetic diversity among Gossypium malaya. It is notable for its soil fertility, especially in the hirsutum L. germplasms and genotypes using chromo-

Ganges Delta, Sylhet Division, and the Chittagong Hill mycin A3 (CMA) and 4′,6-diamidino-2-phenylindole Tracts. Agriculture is the largest economic sector in this (DAPI) banding, random amplification of polymorphic region, employing about 45% of the workforce. Thus, DNA (RAPD), and simple sequence repeat (SSR) molec- the agricultural sector has a major impact on employ- ular markers (Sultana and Alam 2016a, b, Hossain et al. ment, poverty alleviation, human resources develop- 2017). ment, and food security. More Bangladeshis earn their Coccinia grandis L. has an active XX–XY sex deter- living from agriculture than from any other sector. The mination system with male heterogametic and morpho- country is among the top producers of rice (fourth), po- logically distinguishable sex chromosomes. Both male tatoes (seventh), tropical fruits (sixth), jute (second), and and female plants have equal medicinal importance; farmed fish (fifth) worldwide. Cotton (Gossypium spp.) therefore, this plant has long been used as traditional is the most important cash crop in Bangladesh after jute. medicine by the local people of Bangladesh. As a con- Cotton is a major natural fiber crop that provides edible sequence, C. grandis is now under threat. Scientists oil and seed by-products for livestock food. are working to conserve and to create awareness about A successful breeding program depends on a com- the proper use of this plant. The genetic information of plete knowledge and understanding of the genetic diver- a plant is essential to this type of conservation work. sity within and among the genetic resources of available Through a combination of cytogenetic and molecular 2018 Chromosome Studies in Three Regions of the Indomalayan Realm 225 analyses, male and female C. grandis from Bangladesh andamanensis (Supiwong et al. 2017b), Synchiropus were characterized for the first time (Hossain et al. ocellatus, S. picturatus (Kasiroek et al. 2017c), Axis axis 2016). These researchers also used the same combi- (Khongcharoensuk et al. 2017), Plectorhinchus pictus nation of analyses to obtain genetic information for (Jantarat et al. 2017a), Micronema cheveyi (Pinthong Cicer arietinum L. (Begum and Alam 2016), Gynura et al. 2017b), Scolopsis vosmeri (Patawang et al. 2017d), nepalensis DC. (Begum and Alam 2017), Ocimum spp. and Crassostrea iredalei (Chooseangjaew et al. 2018). (Dash et al. 2017), Oxalis L. spp. (Bonna et al. 2017), Professor Tanomtong won the second Wada Memorial and Asparagus L. spp. (Akter et al. 2017) within a short Award for this achievement. time span. The chickpea (C. arietinum L.) plays an Khon Kaen is a rural city in northern Thailand important role in human nutrition as a source of protein, (Trisurat et al. 2018). Covering an area of 513120 km2, energy, fiber, vitamins, and minerals for large popula- Thailand comprises several distinct geographic regions, tion sectors in the developing world and is considered a partly corresponding to its provinces. Northern Thai- healthy food in many developed countries. Breeders in land contains the mountainous Thai highlands. In the Bangladesh have been trying to develop better varieties northeast, the Isan region consists of the Khorat Plateau, of this important pulse crop in terms of both yield and which is bordered to the east by the Mekong River. The disease resistance. center of the country is dominated by the predominantly Dhaka is among the largest cities worldwide, with a flat Chao Phraya river valley, which runs into the Gulf population of 18.89 million people in the Greater Dhaka of Thailand. Southern Thailand consists of the narrow Area, making it the fourth most densely populated city Kra Isthmus, which widens into the . in the world. Increasing air and water pollution from Professor Tanomtong and his coworkers are currently traffic congestion and industrial waste are serious prob- analyzing karyotypes of several species in these re- lems affecting the public health and quality of life in gions, including Rhinolophus coelophyllus; R. pusillus Dhaka. Water bodies and around Dhaka are (Patawang et al. 2017c); Axis (Khongcharoensuk et al. facing destruction as they are filled during the construc- 2017); Varanus bengalensis (Patawang and Tanomtong tion of multi-storey buildings and other developments. 2017, Patawang et al. 2017a); Lipinia vittigera (Pa- Coupled with pollution, this erosion of natural habitats tawang, et al. 2017b); Microhylid spp. (Sangpakdee et al. threatens to destroy much of the regional biodiversity. 2017); Hoplobatrachus rugulosus (Tengjaroenkul et al. In one recent study (Hossen et al. 2016), plants 2017); the three-spot damselfish Dascyllus trimaculatus that commonly grow in urban areas of Dhaka, such (Getlekha et al. 2017); the tropical oyster Crassostera as Colocasia esculenta (L.) Schott (Nahar and Alam belcheri (Chooseangjaew et al. 2017); freshwater fish, 2016a) and Ipomoea aquatic (Nahar and Alam 2016b), such as Nile tilapia, Oreochromis niloticus (Sriuttha were used to observe the effects of effluents from the et al. 2017); freshwater perciforms Channa marulius and textile, pesticide, tannery, ceramic, and pharmaceuti- C. marulioides (Sarasan et al. 2018); the hihgfin barb cal industries on chromosomal and DNA levels. These fish, Cyclocheilichthys armatus (Chaiyasan et al. 2018); plants also included Tacca spp., which are used as folk and the black lancer, Bagrichthys majusculus (Supiwong medicines by different tribal peoples and are now under et al. 2018). severe threat in Bangladesh due to rapid industrializa- The (Elephas maximus) is Thailand’s tion, urbanization, deforestation, and misuse of land. Re- national symbol. Although there were 100000 domesti- searchers are working to conserve these plants; however, cated elephants in Thailand in 1850, the elephant popu- authentic identification of each species is essential to this lation has dropped to an estimated 2000. Poachers have process, and no ethnobotanical exploration of these spe- long hunted elephants for their ivory and hides, and now cies has yet been undertaken. they increasingly do so for meat. Young elephants are often captured for use as tourist attractions or work ani- Thailand, including the Indochina and Northern Malay mals, although their use has declined since the govern- Peninsulas ment banned logging in 1989. There are now more el- Professor Alongklod Tanomtong of the Department ephants in captivity than in the wild, and environmental of Biology at the Faculty of Science at Khon Kaen Uni- activists claim that captive elephants are often mistreat- versity (Fig. 1C) is among the most active researchers ed (Van de Water and Matteson 2018). Elephants are publishing in Cytologia. He and his coworkers have listed as endangered, and a continued decline of elephant published 92 articles, reporting the karyotypes of at populations is expected. Professor Tanomtong and his least 124 species in Cytologia since his first such work coworkers have presented the standardized karyotype, in 2005. At least 32 of these karyotypes were the first ideogram, and basic cytogenetic data that could serve to be reported worldwide, including those of Fibramia as a basis for future chromosome analyses of Asian ele- lateralis (Kasiroek et al. 2017a), Pterapogon kaud- phant populations and for cytogenetic studies comparing erni (Kasiroek et al. 2017b), Chaetodon decussatus, C. their chromosomes with those of other related species lineolatus (Supiwong et al. 2017a), C. triangulum, C. (Rattanayuvakorn et al. 2017). 226 S. Kawano Cytologia 83(3)

Poaching and mistreatment of protected species re- in nine varieties of Cicer arietinum L. Cytologia 81: 383–387. mains a major problem. Hunters have decimated popu- Begum, K. N. and Alam, S. S. 2017. Karyotype, RAPD and ISSR analysis of four specimens in Gynura nepalensis DC. Cytologia lations of , , and other large cats for their 82: 423–428. valuable pelts. Many animals, including tigers, bears, Bonna, I. J., Afroz, M., Sultana, S. S. and Alam, S. S. 2017. Com- crocodiles, and king cobras, are farmed or hunted for parative karyotype and RAPD analysis of four Oxalis L. species. their meat, which is considered a delicacy, and for their Cytologia 82: 527–533. supposed medicinal properties. The practice of keeping Chaiyasan, P., Supiwong, W., Saenjundaeng, P., Seetapan, K., Pin- mongkhonkul, S. and Tanomtong, A. 2018. A report on classical wild animals as pets threatens several species. Baby cytogenetics of hihgfin barb fish, Cyclocheilichthys armatus animals are typically captured and sold, which often (Cypriniformes, Cyprinidae). Cytologia 83: 149–154. requires killing the mother. Once in captivity and out of Chooseangjaew, S., Tanyaros, S., Jumrusthanasan, S., Getlekha, N. their natural habitat, many pets die or fail to reproduce. and Tanomtong, A. 2018. Karyological analysis and nucleolar Thailand is a tropical country with high biodiversity organizer region of tropical oyster, Crassostrea iredalei (Ostre- due to its climate and environment; the diversity of oida, Ostreidae) in Thailand. Cytologia 83: 129–132. Chooseangjaew, S., Tanyaros, S., Maneechot, N., Buasriyot, P., Getle- wild animals should be maintained for their ecological kha, N. and Tanomtong, A. 2017. Chromosomal characteristics importance and impact on the food chain. Deforestation of the tropical oyster, Crassostrea belcheri Sowerby, 1871 (Os- also causes wild animal extinction or risk of extinction, treoida, Ostreidae) by conventional and Ag-NOR banding tech- as in the family Hylobatidae, which contains four Thai niques. Cytologia 82: 3–8. species: the white-handed (Hylobates lar), pile- Dash, C. K., Afroz, M., Sultana, S. S. and Alam, S. S. 2017. Con- ventional and fluorescent karyotype analysis of Ocimum spp. ated (H. pileatus), and dark-handed gibbon (H. agilis) Cytologia 82: 429–434. are endangered (EN) (i.e., have a high risk of extinc- Getlekha, N., Supiwong, W., Yeesin, P., Pengseng, P., Kasiroek, tion in the wild). The white-cheeked gibbon (Nomascus W. and Tanomtong, A. 2017. Chromosomal characteristics of leucogenys) is critically endangered (CR), (i.e., has an the three-spot damselfish, Dascyllus trimaculatus (Perciformes, extremely high risk of extinction in the wild). Profes- Pomacentridae) in Thailand. Cytologia 82: 51–57. Gill, P. A. and Kaur, R. 2016. Meiotic studies on Abutilon indicum sor Tanomtong and his coworkers have analyzed the (L.) Sweet from North Indian Plains. Cytologia 81: 379–382. standardized karyotypes of these Thai gibbon species Gupta, R. C., Gupta, A. and Kaur, A. 2017a. Meiotic studies in some (Supanuam et al. 2012), recommending the designation members of tribe Andropogoneae (Poaceae) from a semi-desert of 1 CR, 11 EN, and 12 vulnerable (VU) species (having area of North India. Cytologia 82: 105–113. a high risk of endangerment in the wild), and 7 near- Gupta, R. C., Gupta, A. and Kaur, N. 2017b. Cytological diversity in some members of tribe Agrostideae and Eragrosteae (Poaceae) threatened (NT) species (likely to become endangered in from Haryana and adjoining Shiwalik Hills. Cytologia 82: the near future). The NT category includes the Sumatra 501–505. serow, Capricornis sumatraensis (Jantarat et al. 2017b), Gupta, R. C., Kumari, K., Kaur, K. and Singh, V. 2016. Anomalous and Indian hog deer, Hyelaphus porcinus (Pinthong chromosomal behaviour and chromosomal data in some mem- et al. 2017a). Most of these publications were the first re- bers of subclass Gamopetalae from district Hamirpur (H. P.), India. Cytologia 81: 25–34. ports of standardized karyotype and idiogram measure- Holt, B. G., Lessard, J.-P., Borregaard, M. K., Fritz, S. A., Araújo, ments conducted using Giemsa (GTG), high-resolution, M. B., Dimitrov, D., Fabre, P.-H., Graham, C. H., Graves, G. R., and Ag-NOR banding techniques. These findings repre- Jønsson, K. A., Nogués-Bravo, D., Wang, Z., Whittaker, R. J., sent new, basic knowledge that will be useful to future Fjeldså, J. and Rahbek, C. 2013. An update of Wallace’s zoogeo- research on and applications in the fields of genetic di- graphic regions of the world. Science 339: 74–78. versity, taxonomy, conservation, and evolution. Hossain, A., Afroz, M., Sultana, S. S. and Alam, S. S. 2017. Karyo- type and RAPD diversity in four varieties of Gossypium hirsu- tum L. Cytologia 82: 535–541. Acknowledgements Hossain, M. U., Islam, M., Afroz, M., Sultana, S. S. and Alam, S. S. 2016. Karyotype and RAPD analysis of male and female Coc- The late Professor Dr. Sheikh Shamimul Alam cinia grandis L. from Bangladesh. Cytologia 81: 349–355. of the Botany Department at Dhaka University (DU) Hossen, R., Sultana, S. S. and Alam, S. S. 2016. Cyto-molecular char- acterization of three Tacca species from Bangladesh. Cytologia published 50 articles in Cytologia over the course of his 81: 371–377. lifetime. We greatly appreciate his substantial contribu- Jantarat, S., Supiwong, W., Phintong, K., Sonsrin, K., Kong-ngarm, tions to Cytologia. The Wada Memorial Award, of which N. and Tanomtong, A. 2017a. First analysis on the cytogenetics he was the first recipient, is a prize awarded by the Japan of painted sweetlip, Plectorhinchus pictus (Heamulidae: Perci- Mendel Society. formes) from Thailand. Cytologia 82: 145–150. Jantarat, S., Tanomtong, A., Patawang, I., Chaiphech, S., Rattanayu- vakorn, S. and Phintong, K. 2017b. Cytogenetics study and char- References acterization of Sumatra serow, Capricornis sumatraensis (Ar- tiodactyla, Bovidae) by classical and FISH techniques. Cytologia Akter, S., Begum, K. N., Sultana, S. S. and Alam, S. S. 2017. Karyo- 82: 127–135. type diversity in three Asparagus L. species. Cytologia 82: Kasiroek, W., Indananda, C., Luangoon, N., Pinthong, K., Supiwong, 551–557. W. and Tanomtong, A. 2017a. First chromosome analysis of the Begum, K. N. and Alam, S. S. 2016. Differential fluorescent banding humpback cardinalfish, Fibramia lateralis (Perciformes, Apogo- 2018 Chromosome Studies in Three Regions of the Indomalayan Realm 227

nidae). Cytologia 82: 9–15. Rhinolophidae). Cytologia 82: 471–480. Kasiroek, W., Indananda, C., Pinthong, K., Supiwong, W., Pengseng, Patawang, I., Tengjaroenkul, B., Supanuam, P., Kakampuy, W., Khun- P. and Tanomtong, A. 2017b. NOR polymorphism and chromo- sook, S. and Tanomtong, A. 2017d. First cytogenetic study of some analysis of Banggai cardinalfish, Pterapogon kauderni the whitecheek monocle bream, Scolopsis vosmeri (Perciformes, (Perciformes, Apogonidae). Cytologia 82: 17–23. Nemipteridae) from Thailand. Cytologia 82: 481–484. Kasiroek, W., Luangoon, N., Supiwong, W., Tengjaroenkul, B., Pinthong, K., Supiwong, W., Simporn, B., Chooseangjaew, S., Pinthong, K. and Tanomtong, A. 2017c. First report of chromo- Kakampuy, W. and Tanomtong, A. 2017b. A first chromo- some analysis of two dragonets (Perciformes, Callionymidae). somal and nucleolar organizer regions (NORs) analyses of Cytologia 82: 59–65. Chevey’s sheetfish, Micronema cheveyi (Siluriformes, Siluridae). Kaur, M., Himshikha. and Singhal, V. K. 2017. Occurrence of syn- Cytologia 82: 435–441. cytes: A possible mechanism owing to the origin of polyploid Pinthong, K., Tanomtong, A., Khongcharoensuk, H., Chaiphech, S., cytotypes in Achillea millefolium L. within Indian Himalayas. Rattanayuvakorn, S. and Supanuam, P. 2017a. Karyotype and Cytologia 82: 375–384. idiogram of Indian hog deer (Hyelaphus porcinus) by conven- Kaur, N. and Gupta, R. C. 2016. Cytological study in some members tional staining, GTG-, high-resolution and Ag-NOR banding of tribe Paniceae (Poaceae) from Rajasthan. Cytologia 81: 13–17. techniques. Cytologia 82: 227–233. Khongcharoensuk, H., Tanomtong, A., Patawang, I., Supanuam, P., Rani, S., Chahota, R. K. and Sharma, T. R. 2016. Cytomixis and Sornnok, S. and Pinthong, K. 2017. Karyotype and idiogram associated meiotic abnormalities during male meiosis in An- of the axis deer (Axia axis, Cervidae) by conventional staining, gelica glauca Edgew. (Apiaceae) from Northwestern Himalayas. GTG-, high-resolution GTG-, and Ag-NOR-banding techniques. Cytologia 81: 161–168. Cytologia 82: 91–98. Rattanayuvakorn, S., Tanomtong, A., Phimphan, S., Sangpakdee, Kumar, P. and Singhal, V. K. 2016a. Morphological and ecological ad- W., Pinmongkhonkul, S. and Phintong, K. 2017. Karyological aptations, and cytological studies in Astragalus rhizanthus Royle study of tusker and tuskless male Asian elephant (Elephas maxi- ex Benth. (Papilionaceae), an endemic to Himalayas. Cytologia mus) by conventional, GTG-, and Ag-NOR banding techniques. 81: 155–160. Cytologia 82: 349–354. Kumar, P., Singhal, V. K. and Srivastava, S. K. 2016b. Meiotic stud- Saggoo, M. I. S. and Kaur, M. 2016. Irregular meiotic behavior in ies and B-chromosomes in Sedum oreades (Decne.) R. Hamet maidenhair fern Adiantum capillus-veneris L. from Northwest (Crassulaceae) from alpine regions of Northwest Indian Hima- India. Cytologia 81: 77–82. laya. Cytologia 81: 275–278. Saggoo, M. I. S. and Kaur, M. 2017a. Chromosomal aberrations and Kumar, R., Rana, P. K. and Singhal, V. K. 2016a. Chromatin sticki- apomictic behavior in two cytotypes of Pteris cretica L. from ness and abnormal spindle resulting in meiotic irregularities and Western Himalayas. Cytologia 82: 161–166. pollen sterility in Meconopsis aculeata Royle from the North- Saggoo, M. I. S. and Kaur, M. 2017b. Adiantum lunulatum Burm. west Himalayas. Cytologia 81: 83–87. naturalized triploid apomicts from Kangra Valley of Himachal Kumar, R. and Singhal, V. K. 2016b. Occurrence of univalents and Pradesh. Cytologia 82: 507–512. abnormal spindle activity in the meiocytes in Impatiens deven- Saggoo, M. I. S., Nawchoo, I. A. and Akhter, A. 2017. Meiotic ir- drae Pusalkar from Western Himalayas. Cytologia 81: 389–394. regularities in Lavatera cachemiriana, an endemic, endangered Kumar, S., Kumari, S., Gupta, R. C. and Sharma, V. K. 2017. Cyto- and ethnomedicinal herb of Kashmir Himalaya. Cytologia 82: genetic studies of genus Clematis L. (Ranunculaceae) from the 235–239. Western Himalayas, India. Cytologia 82: 355–361. Sangpakdee, W., Phimphan, S., Tengjaroenkul, B., Pinthong, K., Kumari, K. and Saggoo, M. I. S. 2016a. Male meiosis in two morphot- Neeratanaphan, L. and Tanomtong, A. 2017. Cytogenetic study ypes of Melica persica Kunth (Poaceae) from Himachal Pradesh, of three Microhylid species (Anura, Microhylidae) from Thai- India. Cytologia 81: 403–408. land. Cytologia 82: 67–74. Kumari, K. and Saggoo, M. I. S. 2016b. Analysis of meiotic behavior Sarasan, T., Jantarat, S., Supiwong, W., Yeesin, P., Srisamoot, N. and in Eremurus himalaicus Baker (Liliaceae): a rare endemic pe- Tanomtong, A. 2018. Chromosomal analysis of two snakehead rennial from Kinnaur, Himachal Pradesh, India. Cytologia 81: fishes, Channa marulius (Hamilton, 1822) and C. marulioides 447–453. (Bleeker, 1851) (Perciformes: Channidae) in Thailand. Cytologia Nahar, K. K. and Alam, S. S. 2016a. Effects of industrial effluents on 83: 115–121. chromosomes of Colocasia esculenta (L.) Schott collected from Singhal, V. K., Khan, N. A. and Gupta, R. C. 2016a. Syncyte and five different affected areas. Cytologia 81: 169–174. ‘2n’ pollen grain formation in Heracleum pinnatum: A possible Nahar, K. K. and Alam, S. S. 2016b. Karyotype and RAPD analysis mechanism for the origin of intraspecific polyploids. Cytologia of Ipomoea aquatica samples collected from different industrial 81: 335–339. effluent affected areas. Cytologia 81: 285–290. Singhal, V. K. and Kumari, V. 2017. Structural heterozygosity for Patawang, I. and Tanomtong, A. 2017. Constitutive heterochromatin reciprocal translocations affecting chiasma frequency and pol- observed on metaphase chromosome of Varanus bengalensis by len fertility of a natural tetraploid of Anthoxanthum odoratum L. C-banding and DAPI methods. Cytologia 82: 1–2. from Northwest Himalayas. Cytologia 82: 151–155. Patawang, I., Tanomtong, A., Getlekha, N., Phimphan, S., Pinthong, Singhal, V. K., Singh, J., Kaur, S. and Kumar, R. 2016b. Chromo- K. and Neeratanaphan, L. 2017a. Standardized karyotype and some counts through male meiosis in some dicots from the Hills idiogram of Bengal monitor lizard, Varanus bengalensis (Squa- around Shimla, Himachal Pradesh. Cytologia 81: 183–188. mata, Varanidae). Cytologia 82: 75–82. Singhal, V. K., Tantray, Y. R. and Gupta, R. C. 2016c. Structural het- Patawang, I., Tanomtong, A., Jumrusthanasan, S., Khongcharoensuk, erozygosity for reciprocal translocation in Tanacetum artemisi- H., Kaewsri, S. and Pinthong, K. 2017b. Cytogenetic of skink oides Sch. Bip. ex Hook. f. from Ladakh division of Jammu and (Reptilia, Scincidae) from Thailand: II: Chromosome analyses of Kashmir. Cytologia 81: 319–322. stripe tree skink (Lipinia vittigera). Cytologia 82: 83–90. Singhal, V. K., Tantray, Y. R., Kaur, D. and Gupta, R. C. 2017. First Patawang, I., Tengjaroenkul, B., Supanuam, P., Kakampuy, W., Khun- report of intraspecific polyploidy (2x, 4x) in Physochlaina sook, S. and Tanomtong, A. 2017c. Chromosome analysis and praealta (Decne.) Miers. (Family: Solanaceae). Cytologia 82: morphometric of croslet horseshoe bat, Rhinolophus coelophyl- 245–250. lus and least horseshoe bat, Rhinolophus pusillus (Chiroptera, Sriuttha, M., Khammanichanh, A., Patawang, I., Tanomtong, A., 228 S. Kawano Cytologia 83(3)

Tengjaroenkul, B. and Neeratanaphan, L. 2017. Cytotoxic as- Supiwong, W., Getlakha, N., Chaiphech, S., Pinthong, K., Phimphan, sessment of Nile tilapia (Oreochromis niloticus) from a domestic S. and Tanomtong, A. 2018. Nucleolar organizer regions poly- wastewater canal with heavy metal contamination. Cytologia 82: morphism and karyological analysis of black lancer, Bagrichthys 41–50. majusculus (Siluriformes, Bagridae) in Thailand. Cytologia 83: Sultana, S. S. and Alam, S. S. 2016a. Differential fluorescent band- 193–199. ing in 11 varieties of Gossypium hirsutum L. from Bangladesh. Tengjaroenkul, B., Intamat, S., Sriuttha, M., Tanomtong, A. and Cytologia 81: 111–117. Neeratanaphan, L. 2017. Cytotoxicity evaluation of the East Sultana, S. S. and Alam, S. S. 2016b. SSR and RAPD-based genetic Asian bullfrog (Hoplobatrachus rugulosus) in an agricultural diversity in cotton germplasms. Cytologia 81: 257–262. area affected by Chlorpyrifos. Cytologia 82: 175–181. Supanuam, P., Tanomtong, A., Khunsook, S., Sangpakdee, W., Pin- Trisurat, Y., Kanchanasaka, B. and Kreft, H. 2014. Assessing poten- thong, K., Sanoamuang, L. and Keawsri, S. 2012. Localization tial effects of land use and climate change on mammal distribu- of nucleolar organizer regions (NORs) of 4 gibbon species in tions in northern Thailand. Wildl. Res. 41: 522–536. Thailand by Ag-NOR banding technique. Cytologia 77: 141–148. Udvardy, M. D. F. 1975. A Classification of the Biogeographical Supiwong, W., Boonsuk, J., Jantarat, S., Suvarnaraksha, A., Pengseng, Provinces of the World. IUCN Occasional Paper No. 18. IUCN, P. and Tanomtong, A. 2017b. The first chromosomal charac- Morges. teristics of nucleolar organizer regions and karyological analy- Van de Water, A. and Matteson, K. 2018. Human–elephant conflict in sis of two chaetodontid fishes (Perciformes, Chaetodontidae). western Thailand: Socio–economic drivers and potential mitiga- Cytologia 82: 33–39. tion strategies. PLoS ONE 13: e0194736. Supiwong, W., Boonsuk, J., Jumrusthanasan, S., Pinthong, K., Suvar- Walia, G. K., Gill, J. K. and Hallan, H. K. 2016. C-banding and Ag- naraksha, A. and Tanomtong, A. 2017a. First report of chromo- NOR staining on Neurobasis chinensis (Linnaeus) of family some analysis of two Chaetodontid fishes (Perciformes, Chae- Calopterygidae from Himachal Pradesh, India (Odonata: Zygop- todontidae). Cytologia 82: 25–31. tera). Cytologia 81: 175–178.