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Hymenoptera: Megachilidae)

Hymenoptera: Megachilidae)

Proceedings of International Conference on Biodiversity: IBD2019 (2019); 94 - 101

Checklist of Latreille, 1802 in (: )

Nontawat Chatthanabun and Natapot Warrit* Department of Biology & Center of Excellence in Entomology, Faculty of Science, University, Pathum Wan District, , Thailand *Corresponding author e-mail: [email protected]

Abstract: A checklist of Thai megachilid is reported for the first time. Species names listed were recorded from specimens collected throughout Thailand and deposited at the Natural History Museum, Bangkok and through literature review. A total of 30 Thai Megachile species are listed with locality information and notes on floral records, diagnostic characters, and nesting habitats (when appropriate). Due to their abundance, we suggest that Megachile (Amegachile) bicolor, M. () disjuncta, M. (Creightonella) fraterna, and M. (Pseudomegachile) velutina are good candidates for being future crop .

Keywords: Diversity, Leafcutter bee, Pollination, , Resin bee.

Introduction

Megachile Latreille, 1802 (Hymenoptera; Megachilidae) is one of the most diverse bee genera that include leafcutter, resin, and . Megachile has a wide distribution and diverse habitats in most regions of the world (Michener, 2007; Gonzalez et al., 2012). Presently, over 1,500 species are already named and described (Michener, 2007; Ascher & Pickering, 2019). These bees include many important pollinators for natural ecosystems and agricultural areas, e.g. , a well-known alfalfa crop pollinator (Delaplane & Mayer, 2000; Michener, 2007). Historically, Southeast Asian megachilid bees are poorly known, underrepresented in collections, and inadequately explored (Engel & Gonzalez, 2011; Gonzalez & Engel, 2012). Therefore, megachilid bees in Thailand are not well recognized and protected from various anthropogenic threats such as habitat destruction and insecticide usages in agriculture areas. This work attempts to contribute to the basic knowledge of Thai megachilid bee fauna. The checklist comprises number of species and valid names, their distributions in Thailand, and notes on some species.

Materials and Methods

588 specimens (368♀, 220♂) collected throughout Thailand and deposited at the Chulalongkorn University Natural History Museum (CUNHM) since 1962 were examined (see in Table 1). In addition, literature on Thai Megachile taxonomic treatments were reviewed following Tadauchi and Tasen (2009), Engel and Gonzalez (2011), Gonzalez & Engel, 2012, Ascher et al., (2016) and the Discoverlife Bee Species Guide and World Checklist (Ascher and Pickering, 2019).

Result & Discussion

This checklist recorded 30 species of Megachile in Thailand through specimens examination and literature review. For generic and subgeneric classification we follow Michener (2007) and Trunz et al. (2016), whereas for species level identification, the specimens were verified with their original descriptions. In addition, notes on floral records, diagnostic character, and nesting habitats are provided below. Species and collecting localities names are alphabetically ordered. Family: Megachilidae Genus: Megachile Latreille, 1802 Subgenus: Aethomegachile Engel and Baker, 2006 Megachile (Aethomegachile) conjuncta Smith, 1853 Distribution: Chiang Mai. Note: There is a sexual dimorphism between male and female bees. Megachile (Aethomegachile) laticeps Smith, 1853 Distribution: Bangkok, Surat Thani. Note: Superficially resembling to M. (Callomegachile) umbripennis but it can be easily distinguished by mandible with an incomplete cutting edge in the second interspace and hidden cutting edge in the third interspace. Megachile (Aethomegachile) siamensis Cockerell, 1927 Distribution: Chiang Mai, Mae Hong Son. Note: Only male was described. Megachile (Aethomegachile) trichorhytisma Engel, 2006

Proceeding of International Conference on Biodiversity: IBD2019 on 22nd - 24th May 2019 94 at Centara Grand & Bangkok Convention Centre at CentralWorld, Bangkok, Thailand

Distribution: Chiang Rai, Loei Note: Male can be easily recognized by the modification of its last flagellomere. Subgenus: Amegachile Friese, 1909 Megachile (Amegachile) bicolor (Fabricius, 1781) Distribution: Chiang Mai, Kanchanaburi, Mukdahan, Nakhon Nayok, Nakhon Pathom, Nong Khai, Phayao, Ratchaburi, Saraburi, Tak. Note: A widespread species in Oriental region, particularly India and southern China. This species is commonly found in sunhemp field (Crotalaria juncea L.) and its nesting biology was reported back from 1955 by Von Rudolf Altevogt. Subgenus: Callomegachile Michener, 1962 Megachile (Callomegachile) atratiformis (Meade-Waldo, 1914) Distribution: Uthai Thani. Note: Engel and Gonzalez (2011) reported the species was collected on Dipterocarpus obtusifolius Teijsman & Miquel. Megachile (Callomegachile) disjuncta (Fabricius, 1781) Distribution: Bangkok, Chiang Mai, Phayao, Surat Thani, Yala. Note: This species forages on numerous types of plants, especially in Fabaceae. In addition, Soh (2014) was first to report its nest construction using resins. Megachile (Callomegachile) faceta (Bingham, 1897) Distribution: No specific location provided. Megachile (Callomegachile) facetula (Cockerell, 1918) Distribution: No specific location provided. Note: This species is superficially similar to M. (Callomegachile) faceta though can be distinguished by the presence of dense fulvous hairs on the vertex of the former species. Megachile (Callomegachile) fulvipennis (Smith, 1879) Distribution: Surat Thani. Note: Soh (2014) reported the species using resin for nest construction and visited Peltophorum pterocarpum (Fabaceae) and Memecylon sp. (Melastomataceae). Megachile (Callomegachile) impressa (Friese, 1903) Distribution: No specific location provided. Note: Only male was described. Megachile (Callomegachile) monticola (Smith, 1858) Distribution: No specific location provided Note: This species has a wide distribution in south China. Megachile (Callomegachile) odontophora Engel, 2011 Distribution: Nakhon Ratchasima Note: Engel and Gonzalez (2011) reported the species was collected on Sindora siamensis Teijsman & Miquel (Fabaceae). Megachile (Callomegachile) ornata (Smith, 1853) Distribution: Chiang Mai Note: Tadauchi and Tasen (2009) identified only one specimen from a teak plantation. Megachile (Callomegachile) tuberculata (Smith, 1858) Distribution: No specific location provided Note: Ascher et al. (2016) reported the species was collected on Grammatophyllum speciosum Blume (Orchidaceae). Megachile (Callomegachile) umbripennis (Smith, 1853) Distribution: Bangkok, Phayao. Note: This species has a wide distribution range in Southeast Asia and was reported to be adventive in the US. Subgenus: Carinula Michener, McGinley, and Danforth, 1944 Megachile (Carinula) fruhstorferi Friese, 1903 Distribution: Saraburi. Note: This species is superficially similar to M. (Callomegachile) stulta though can be easily distinguished by the presence of yellow felted hairs on the metasomal terga. Subgenus: Chelostomoda Michener, 1962 Megachile (Chelostomoda) aureocincta Cockerell, 1927 Distribution: Nakhon Si Thammarat. Megachile (Chelostomoda) nematocera Cockerell, 1929 Distribution: Chiang Mai.

Proceedings of International Conference on Biodiversity: IBD2019 on 22nd - 24th May 2019 at Centara Grand & Bangkok Convention Centre at CentralWorld, Bangkok, Thailand 95

Subgenus: Creightonella Cockerell, 1908 Megachile (Creightonella) fraterna Smith, 1853 Distribution: Ayutthaya, Chiang Mai, Kanchanaburi, Petchabun, Phayao, Ratchaburi, Saraburi, Thonburi. Note: This species usually forages on sunhemp flower (Crotalaria juncea L.) and constructs its nest underground in the sun hemp field. Megachile (Creightonella) atrata Smith, 1853 Distribution: Chumphon, Surat Thani, Yala. Note: This species only occur in south Thailand. The bee forages on sunhemp flower (Crotalaria juncea L.) and constructs its nests underground in the sun hemp field. Subgenus: Eutricharaea Thomson, 1872 Megachile (Eutricharaea) gathela Cameron, 1908 Distribution: No specific location provided. Megachile (Eutricharaea) griseopicta Radoszkowski, 1882 Distribution: Chiang Mai. Note: This species is superficially similar to M. (Callomegachile) faceta though can be easily distinguished by the presence of the hidden cutting in the third interspace of the mandible. Megachile (Eutricharaea) hera Bingham, 1897 Distribution: Kamphaeng Phet, Mae Hong Son, Nakhon Pathom, Petchabun, Phetchaburi, Phang Nga, Phayao, Sakon Nakhon, Samut Sakorn, Ubon Ratchathani, Udon Thani. Note: This species has a wide distribution and commonly found in Thailand. Subgenus: Lophanthedon Gonzalez and Engel, 2011 Megachile (Lophanthedon) amputata Smith, 1857 Distribution: No specific location provided. Note: This species is superficially similar to M. (Aethomegachile) laticeps though can be easily distinguished by the presence of the outer ridge on the mandible. Megachile (Lophanthedon) dimidiata Smith, 1853 Distribution: Lumpang. Note: This species is superficially similar to M. (Pseudomegachile) velutina though can be easily distinguished by the presence of the outer ridge on the mandible and absence of dense long hairs on the inner adductor interspace of the mandible. Megachile (Lophanthedon) erythropoda Cameron, 1901 Distribution: Songkhla. Megachile (Lophanthedon) ferruginea Friese, 1903 Distribution: Nong Bua Lam Phu. Note: This species is superficially similar to M. (Lophanthedon) dimidiata though can be easily distinguished by the presence of fulvous hairs on the apical margin of the metasomal terga. Subgenus: Pseudomegachile Friese, 1898 Megachile (Pseudomegachile) lanata (Fabricius, 1775) Distribution: No specific location provided. Note: A common species found in India. Megachile (Pseudomegachile) velutina Smith, 1853 Distribution: Lumpang, Nakhon Si Thammarat, Pattani. Note: Commonly found in sunhemp field (Crotalaria juncea L.). This report listed 30 Megachile species recorded in Thailand, which consist of 18 species of mason and resin bees from 4 subgenera: Callomegachile, Carinula, Lophanthedon, and Pseudomegachile. Leafcutter bees are represented for 12 species from 5 subgenera: Aethomegachile, Amegachile, Chelostomoda, Creightonella, and Eutricharaea. Callomegachile has the highest number of species for Thai megachilid bees, whereas others are infrequently reported. Despite Megachile wide distribution in Thailand, historical records are sporadic and rare. Here, we documented 27 provinces in Thailand for the occurrence of Megachile. Of these 8 provinces are new records for Thailand: Ayutthaya, Chumphon, Kanchanaburi, Mukdahan, Nakhon Pathom, Nong Khai, Petchabun, and Thonburi. Remarkably, three of the most abundance in agricultural areas, the leafcutter bees Megachile (Amegachile) bicolor (Figure 1a), Megachile (Creightonella) fraterna (Figure 2a) and mason bee Megachile (Pseudomegachile) velutina (Figure 2e), live and nest in sunhemp field. According to above, we suggest that these bees are potential candidates for future pollination study. Another candidate is Megachile (Callomegachile) disjuncta (Figure 1e), usually foraging on fabaceae and easy adoption human artifacts.

Proceeding of International Conference on Biodiversity: IBD2019 on 22nd - 24th May 2019 96 at Centara Grand & Bangkok Convention Centre at CentralWorld, Bangkok, Thailand

Two close species of Thai Megachile, which have fulvous hairs on prosoma and mesosoma with the yellow wings: the female of Megachile (Lophanthedon) dimidiata and Megachile (Pseudomegachile) velutina. These bees have similar appearance, but differ in outer ridge on mandible, which are reaching to mandible base and reaching only three-fourth mandible respectively. Female of Megachile (Aethomegachile) conjuncta and Megachile (Callomegachile) disjuncta, which are black with white hairs on propodeum and first metasomal tergite, closely resemble and they are sympatric species, but differ in scopal color, orange-red and black respectively. The male of Megachile (Aethomegachile) conjuncta and Megachile (Aethomegachile) laticeps, black covered with fulvous hairs, are very similar but differ in apical of gonostylus. Anonther interesting case is the Müllerian mimicry that occurs to Megachile (Callomegachile) fulvipennis and Megachile (Callomegachile) tuberculata (Ascher et al., 2016). Of the 5 species of Thai Megachile, include, Megachile (Aethomegachile) siamensis, Megachile (Aethomegachile) trichorhytisma, Megachile (Callomegachile) monticola, Megachile (Callomegachile) tuberculata and Megachile (Lophanthedon) dimidiate, are collected since past decades and there is no any recent appearance. For this reason, we suggest that these bees may be extinct from Thailand. Nevertheless, these list may be not completely verifiable because unclear distribution pattern, poor records and observations are difficult to determine and remain questionable. In addition, anthropogenic activities such as deforestation, expansion of urban areas, and irresponsible tourism are cause of habitat destruction and reduction of pollinators (Kjøhl et al., 2011).

Conclusion

30 species of Thai Megachile are recorded in 27 provinces. Here, we note some informations of Thai Megachile such as diagnostic characters, food plants or nesting biology. Due to their high abundance and commonly found in crop fields in Thailand, we suggest that M. (Amegachile) bicolor, M. (Callomegachile) disjuncta, M. (Creightonella) fraterna, and M. (Pseudomegachile) velutina may be potential candidates for future pollination studies in Thailand for food crops. In Addition, threats to the decline of Megachile species in Thailand should be of great concern since they can be affected through anthropogenic activities.

Acknowledgement

The authors would like to thank the following institutions and persons as follow: Chawakorn Kunsete, Pakorn Nalinrachatakan, Patsavee Utaipanon, Puttita Pasukdee, Sirat Lertjintanakit and Varat Sivayyapram, CU Bee and Spider Research Lab, Chulalongkorn University, Thailand. We would like to express their gratitude towards to The Scholarship from the Graduate School, Chulalongkorn University to commemorate the 72nd anniversary of his Majesty King Bhumibol Adulyadej is gratefully acknowledged and The 90th Anniversary Chulalongkorn University Fund (Ratchadaphiseksomphot Endowment Fund) (GCUGR1125604070M).

Referenes

Altevogt, R. 1955. Zur Technik der Blattschneidebienen F. und M. maritime Schck. Beitrage zur Entomologie 5: 152–165. Ascher, J. S. and Pickering, J. 2019. Discover Life bee species guide and world checklist (Hymenoptera: : Anthophila). [Online]. Available from: http://www.discoverlife.org/mp/20q?guide=Apoidea_species [20 February 2019]. Ascher, J. S., Risch, S., Soh, Z. W. W., Lee J. X. Q., and Soh, E. J. Y. 2016. Megachile leaf-cutter and resin bees of Singapore (Hymenoptera: Apoidea: Megachilidae). Raffles bulletin of zoology Supplement 32: 33-55. Bingham, C. T. 1897. The fauna of British India, including Ceylon and Burma. Hymenoptera. Vol. I. wasps and bees, Taylor & Francis, London, xxix+579 pp. Cameron, P. 1908. A contribution to the Aculeate Hymenoptera of the Bombay presidency. The journal of the Bombay Natural History Society 18: 649–659. Cockerell, T. D. A. 1918. Descriptions and Records of Bees-LXXX. The annals and magazine of natural history, including zoology, botany, and geology 2: 380–394. Cockerell, T. D. A. 1927. Some bees, principally from Formosa and China. American Museum Novitates 274: 1–16. Delaplane, K. S., and Mayer, D. F. 2000. Crop Pollination by Bees. CABI Publishing, New York, 322 pp. Engel, M. S. and Gonzalez, V. H. 2011. Alocanthedon, a new subgenus of from Southeast Asia (Hymenoptera, Megachilidae). ZooKeys 101: 51–80. Fabricius, J. C. 1775. Systema Entomologiae, Sistens Insectorum Classes, Ordines, Genera, Species, Adiectis Synonymis, Locis, Descriptionibus, Observationibus, Flensburgi et Lipsiae, Korte, xxviii + 832 pp. Fabricius, J. C. 1781. Species Insectorvm Exhibentes eorvn differentias specificas, synonyma avctorvm, loca natalia, metamorphosin adiectis observationibvs, descriptionibvs, Hamburgi et Kilonii:Impensis Carol. Ernest, Bohnii, viii+552 pp.

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Friese, J. H. 1903. Neue Megachile-Arten des Sunda-Archipels. Zeitschrift für systematische Hymenopterologie and Dipterologie 3: 349–359. Gonzalez, V. H., and Engel, M. S., 2012. African and Southeast Asian Chalicodoma (Hymenoptera: Megachilidae): new subgenus, new species, and notes on the composition of Pseudomegachile and Largella. Annales Zoologici 62: 599–617. Gonzalez, V. H., Griswold, T., Praz C. J., and Danforth, B. 2012. Phylogeny of the bee family Megachilidae (Hymenoptera: Apoidea) based on adult morphology. Systematic Entomology 37: 261–286. Kjøhl, M., Nielsen, A. and Stenseth, N. C. 2011. Potential effects of climate change on crop pollination. FAO, Rome, 38 pp. Meade-Waldo, M. A. G. 1914. Note on the Hymenoptera in the Collection of the British Museum, with Descriptions of new Species. The annals and magazine of natural history, including zoology, botany, and geology 14: 450–464. Michener, C. D. 2007. The Bees of the World [2nd Edition]. Johns Hopkins University Press, Baltimore, MD, xvi+[i]+953 pp. Radoszkowski, O. 1882. Opisanie nowych gatunków błonkoskrzydłych (Hymenoptera). Wiadomości z Nauk Przyrodzonych (Warszawa) 2: 72–81. Smith, F. 1853. Catalogue of Hymenopterous in the collection of the British Museum. Taylor and Francis, London, [i]+197 pp. Smith, F. 1858. Catalogue of the Hymenopterous Insects collected at Sarawak, Borneo; Mount Ophir, Malacca; and at Singapore, by A. R. Wallace. Journal of the proceeding of the Linnean Society 2: 42–52. Smith, F. 1879. Descriptions of new species of Hymenoptera in the collection of the British Museum. Taylor and Francis, London, xxi+240 pp. Soh, E. J. Y. 2014. Nesting of two species of resin bees (genus Megachile) in a wooden bench. Singapore Biodiversity Records 2014: 280–282. Tadauchi, O., and Tasen, W. 2009. Bees of natural forests, teak plantations and agricultural fields in Thailand. Esakia 49: 7–13. Trunz, V., Packer, L., Vieu, J., Arrigo, N., and Praz, C. J. 2016. Comprehensive phylogeny, biogeography and new classification of the diverse bee tribe : Can we use DNA barcodes in phylogenies of large genera?. Molecular Phylogenetics and Evolution 103(2016): 245–259.

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Figure 1. Pictures of candidates for future pollination studies (a–d) Megachile (Amegachile) bicolor (a) dorsal view (b) lateral view (c) frontal view of mandible (d) lateral view of (e–h) Megachile (Callomegachile) disjuncta (e) dorsal view (f) lateral view (g) frontal view of mandible (h) lateral view of scopa.

Proceedings of International Conference on Biodiversity: IBD2019 on 22nd - 24th May 2019 at Centara Grand & Bangkok Convention Centre at CentralWorld, Bangkok, Thailand 99

Figure 2. Pictures of candidates for future pollination studies (a–d) Megachile (Creightonella) fraterna (a) dorsal view (b) lateral view (c) frontal view of mandible (d) lateral view of scopa (e–h) Megachile (Pseudomegachile) velutina (e) dorsal view (f) lateral view (g) frontal view of mandible (h) lateral view of scopa.

Proceeding of International Conference on Biodiversity: IBD2019 on 22nd - 24th May 2019 100 at Centara Grand & Bangkok Convention Centre at CentralWorld, Bangkok, Thailand

Table 1. Examined specimens. sex Subgenus locality female male Aethomegachile 55 43 Bangkok, Chiang Mai, Chiang Rai, Loei, Mae Hong Son, Surat Thani Amegachile 72 20 Chiang Mai, Kanchanaburi, Mukdahan, Nakhon Nayok, Nakhon Pathom, Nong Khai, Phayao, Ratchaburi, Saraburi, Tak Callomegachile 120 62 Bangkok, Chiang Mai, Nakhon Ratchasima, Phayao, Surat Thani, Uthai Thani, Yala Creightonella 56 18 Ayutthaya, Chiang Mai, Chumphon Kanchanaburi, Petchabun, Phayao, Ratchaburi, Saraburi, Thonburi. Eutricharaea 24 70 Chiang Mai, Kamphaeng Phet, Mae Hong Son, Nakhon Pathom, Petchabun, Phetchaburi, Phang Nga, Phayao, Sakon Nakhon, Samut Sakorn, Ubon Ratchathani, Udon Thani. Lophanthedon 1 - Lumpang Pseudomegachile 40 7 Lumpang, Nakhon Si Thammarat, Pattani

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