Abstract
The Gaoligong Mountains accommodate diverse ecosystems and biological resources. Beauveria species diversity is inventoried in seven vegetation types of the Gaoligong Mountains along an elevation gradient from 600 to 3800 m. Strains were isolated from soil by using Tenebrio molitor larvae as baits and from naturally occurring insect cadavers carrying anamorphic or teleomorphic fruiting structures of Beauveria spp. The 231 isolated Beauveria strains were identified based on molecular phylogenetic analyses inferred from Bloc, nrSSU, nrLSU, TEF, RPB1, and RPB2 sequences. Eleven species were identified as Beauveria asiatica, B. bassiana, B. brongniartii, B. caledonica, B. medogensis, B. pseudobassiana, and B. sinensis, previously recorded in other Chinese environments, and B. baoshanensis sp. nov., B. malawiensis, B. rudraprayagi, and B. yunnanensis sp. nov., encountered in China for the first time. Species phylogenies are presented and morphological characters of the new species are described. Most isolates were identified as B. bassiana and B. pseudobassiana (86.1%), while the other nine species were isolated rarely. Beauveria was widely distributed in six vegetation types, but not in the vegetation type of the highest altitude. More than four species were encountered in vegetation types with moderate elevation, and these environments also showed highest diversity of plants and insects.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-019-01497-z/MediaObjects/11557_2019_1497_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-019-01497-z/MediaObjects/11557_2019_1497_Fig2_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-019-01497-z/MediaObjects/11557_2019_1497_Fig3_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-019-01497-z/MediaObjects/11557_2019_1497_Fig4_HTML.jpg)
Similar content being viewed by others
References
Agrawal Y, Mual P, Shenoy BD (2014) Multi-gene genealogies reveal cryptic species Beauveria rudraprayagi sp. nov. from India. Mycosphere 5(6):719–736. https://doi.org/10.5943/mycosphere/5/6/3
Ariyawansa HA, Hyde KD, Jayasiri SC, Buyck B, Chethana KWT, Dai DQ, Dai YC, Daranagama DA, Jayawardena RS, Lücking R, Ghobad-Nejhad M, Niskanen T, Thambugala KM, Voigt K, Zhao RL, Li GJ, Doilom M, Boonmee S, Yang ZL, Cai Q, Cui YY, Bahkali AH, Chen J, Cui BK, Chen JJ, Dayarathne M, Dissanayake AJ, Ekanayaka AH, Hashimoto A, Hongsanan S, Jones EBG, Larsson E, Li WJ, Li QR, Liu JK, Luo ZL, Maharachchikumbura SS N, Mapook A, McKenzie EHC, Norphanphoun C, Konta S, Pang KL, Perera RH, Phookamsak R, Phukhamsakda C, Pinruan U, Randrianjohany E, Singtripop C, Tanaka K, Tian CM, Tibpromma S, Abdel-Wahab MA, Wanasinghe DN, Wijayawardene NN, Zhang JF, Zhang H, Abdel-Aziz FA, Wedin M, Westberg M, Ammirati JF, Bulgakov TS, Lima DX, Callaghan TM, Callac P, Chang CH, Coca LF, Dal-Forno M, Dollhofer V, Fliegerová K, Greiner K, Griffith GW, Ho HM, Hofstetter V, Jeewon R, Kang JC, Wen TC, Kirk PM, Kytövuori I, Lawrey JD, **ng J, Li H, Liu ZY, Liu XZ, Liimatainen K, Lumbsch HT, Matsumura M, Moncada B, Nuankaew S, Parnmen S, de Azevedo Santiago ALCM, Sommai S, Song Yu, de Souza CAF, de Souza-Motta CM, Su HY, Suetrong S, Wang Y, Wei SF, Wen TC, Yuan HS, Zhou LW, Réblov M, Fournier J, Camporesi E, Luangsa-ard JJ, Tasanathai K, Khonsanit A, Thanakitpipattana D, Somrithipol S, Diederich P, Millanes AM, Common RS, Stadler M, Yan JY, Li XH, Lee HW, Nguyen TTT, Lee HB, Battistin E, Marsico O, Vizzini A, Vila J, Ercole E, Eberhardt U, Simonini G, Wen Hua-An, Chen XH, Miettinen O, Spirin V, Hernawati (2015) Fungal diversity notes 111–252–taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 75 (1): 27–274.doi: https://doi.org/10.1007/s13225-015-0346-5
Augustyniuk-Kram A, Kram KJ (2012) Entomopathogenic fungi as an important natural regulator of insect outbreaks in forests (review). In: Forest ecosystems-more than just trees. (Eds.: Blanco JA, Lo YH). Rijeka: in tech pp. 265–294.doi: https://doi.org/10.5772/30596
Bischoff JF, Rehner SA, Humber RA (2006) Metarhizium frigidum sp. nov.: a cryptic species of M. anisopliae and a member of the M. flavoviride complex. Mycologia 98(5):737–745. https://doi.org/10.1080/15572536.2006.11832645
Cai Y, Pu SC, Nie Y, Rehner SA, Huang B (2013) Discrimination of Chinese Beauveria strains by DGGE genoty** and taxonomic identification by sequence analysis of the Bloc nuclear intergenic region. Applied Entomology and Zoology 48(3):255–263. https://doi.org/10.1007/s13355-013-0179-1
Chen MJ, Huang B, Li ZZ, Spatafora JW (2013) Morphological and genetic characterisation of Beauveria sinensis sp. nov. from China. Mycotaxon 124:301–308. https://doi.org/10.5248/124.301
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Huang B, Chen MJ, Wang SB, Li ZZ, Fan MZ (2007) A new record of Beauveria isolated from Scolytidae in China. Mycosystema 26(1):139–142 (in Chinese)
Huang GQ, Zhang ZS, Liu YH (2017) Review of the comb-tailed spider genus Hahnia C.L. Koch 1841 (Hahniidae) from Gaoligong Mountains in Yunnan, China. Zootaxa. 4344(3): 444–464. https://doi.org/10.11646/zootaxa.4344.3.2
Imoulan A, Wu HJ, Lu WL, Li Y, Li BB, Yang RH, Wang WJ, Wang XL, Kirk PM, Yao YJ (2016) Beauveria medogensis sp. nov., a new fungus of the entomopathogenic genus from China. J Invertebr Pathol 139:74–81. https://doi.org/10.1016/j.jip.2016.07.006
Kavanaugh DH, Hieke F, Liang H, Dong D (2014) Inventory of the carabid beetle fauna of the Gaoligong Mountains, western Yunnan Province, China: species of the tribe Zabrini (Coleoptera, Carabidae). Zookeys 8(407):55–119. https://doi.org/10.3897/zookeys.407.7353
Kepler RM, Luangsa-Ard JJ, Hywel-Jones NL, Quandt CA, Sung GH, Rehner SA, Aime MC, Henkel TW, Sanjuan T, Zare R, Chen M, Li Z, Rossman AY, Spatafora JW, Shrestha B (2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus 8(2):335–353. https://doi.org/10.5598/imafungus.2017.08.02.08
Keyser CA, Licht HHDF, Steinwender BM, Meyling NV (2015) Diversity within the entomopathogenic fungal species Metarhizium flavoviride associated with agricultural crops in Denmark. BMC Microbiol 15(1):1–11. https://doi.org/10.1186/s12866-015-0589-z
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701.https://doi.org/10.1093/molbev/mss020
Li R, Dao ZL, Li H (2011) Seed plant species diversity and conservation in the northern Gaoligong Mountains in western Yunnan, China. Mountain Research and Development 31(2):160–165 jstor.org/stable/mounresedeve.31.2.160
Ma C, Huang ZP, Zhao XF, Zhang LX, Sun WM, Matthew BS, Wang XW, Cui LW, **ao W (2014) Distribution and conservation status of Rhinopithecus strykeri in China. Primates 55(3):377–382. https://doi.org/10.1007/s10329-014-0425-3
Ormond EL, Thomas AP, Pugh PJ, Pell JK, Roy HE (2010) A fungal pathogen in time and space: the population dynamics of Beauveria bassiana in a conifer forest. Fems Micriobiol Ecol 74(1):146–154. https://doi.org/10.1111/j.1574-6941.2010.00939.x
Pendland JC, Boucias DG (2008) Beauveria. In: Encyclopedia of Entomology. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6359-6_253
Rehner SA, Muro MAD, Bischoff JF (2006) Description and phylogenetic placement of Beauveria malawiensis sp. nov. (Clavidpitaceae, Hypocreales). Mycotaxon 98(7):137–145. https://doi.org/10.1046/j.1365-313X.1999.00542.x
Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97(1):84–98. https://doi.org/10.3852/mycologia.97.1.84
Rehner SA, Minnis AM, Sung GH, Luangsaard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073. https://doi.org/10.3852/10-302
Robène-Soustrade I, Jouen E, Pastou D, Payet-Hoarau M, Goble T, Linderme D, Lefeuvre P, Calmès C, Reynaud B, Nibouche S, Costet L (2015) Description and phylogenetic placement of Beauveria hoplocheli sp. nov. used in the biological control of the sugarcane white grub, Hoplochelus marginalis, on Reunion Island. Mycologia 107:1221–1232. https://doi.org/10.3852/14-344
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Sάnchez-Peña SR, Lara JSJ, Medina RF (2011) Occurrence of entomopathogenic fungi from agricultural and natural ecosystems in Saltillo, México, and their virulence towards thrips and whiteflies. J Insect Sci 11(1):1. https://doi.org/10.1673/031.011.0101
Sanjuan T, Tabima J, Restrepo S, Læssøe T, Spatafora JW, Franco-Molano AE (2014) Entomopathogens of Amazonian stick insects and locusts are members of the Beauveria species complex (Cordyceps sensu stricto). Mycologia 106(2):260–275. https://doi.org/10.3852/106.2.260
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 75:758–771. https://doi.org/10.1080/10635150802429642
Tamura K, Stecher G, Peterson D, Filipski A, Nei M, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Vega FE, Posada F, Aime MC, Pava-Ripoli M, Infante F, Rehner SA (2008) Entomopathogenic fungal endophytes. Biol Control 46(11):72–82. https://doi.org/10.1016/j.biocontrol.2008.01.008
Vuillemim P (1912) Beauveria, nonveau genera de Verticillacees. Bull Soc Bot Franc 59:34–40
Wang YB, Yu H, Dai YD, Wu CK, Zeng WB, Yuan F, Liang ZQ (2015) Polycephalomyces agaricus, a new hyperparasite of Ophiocordyceps sp. infecting melolonthid larvae in southwestern China. Mycol Prog 14:70. https://doi.org/10.1007/s11557-015-1090-7
Wang ZH, Chen AP, Pu SL, Fang JY (2004) Pattern of species richness along an altitudinal gradient on Gaoligong mountains, southwest China. Biodivers Sci 12(1):82–88. https://doi.org/10.3321/j.issn:1005-0094.2004.01.010 (In Chinese)
Yu XD, Lü L, Luo TH, Zhou HZ (2013) Elevational gradient in species richness pattern of epigaeic beetles and underlying mechanisms at east slope of Balang mountain in southwestern China. PLoS One 8(7):e69177. https://doi.org/10.1371/journal.pone.0069177
Zhang SL, He LM, Chen X, Huang B (2012) Beauveria lii sp. nov. isolated from Henosepilachna vigintioctopunctata. Mycotaxon 121:199–206. 10.5248.121.199 https://doi.org/10.1093/molbev/mss020
Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol SciTechno l17:553–596. https://doi.org/10.1080/09583150701309006
Acknowledgments
The authors thank Dr. Qin Liu (College of Resources and Environment, Baoshan University) for his assistance in identifying host insects.
Funding
This work was financially supported by the National Natural Science Area Fund Projects of China (31460153), Key Project of Universities Joint Foundation in Yunnan Province (2017FH001-126), and Surface Project of Universities Joint Foundation in Yunnan Province (2017FH001-029).
Author information
Authors and Affiliations
Corresponding author
Additional information
Section Editor: Hans-Josef Schroers
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chen, ZH., Chen, K., Dai, YD. et al. Beauveria species diversity in the Gaoligong Mountains of China. Mycol Progress 18, 933–943 (2019). https://doi.org/10.1007/s11557-019-01497-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-019-01497-z