New records of ant species from Yunnan, China

Cong Liu; Benoit Guénard; Francisco Hita Garcia; Seiki Yamane; Benjamin Blanchard; Da-Rong Yang; Evan Economo

doi:10.3897/zookeys.477.8775

. 2015 Jan 26;(477):17–78. doi: 10.3897/zookeys.477.8775

New records of ant species from Yunnan, China

Cong Liu ¹, Benoit Guénard ^1,², Francisco Hita Garcia ¹, Seiki Yamane ³, Benjamin Blanchard ^1,⁴, Da-Rong Yang ⁵, Evan Economo ¹

PMCID: PMC4319057 PMID: 25685004

Abstract Abstract

As with many other regions of the world, significant collecting, curation, and taxonomic efforts will be needed to complete the inventory of China’s ant fauna. This is especially true for the highly diverse tropical regions in the south of the country, where moist tropical forests harbor high species richness typical of the Southeast Asian region. We inventoried ants in the Xingshuangbanna prefecture, Yunnan, in June 2013, using a variety of methods including Winkler extraction and hand collection to sample ant diversity. We identified 213 species/morphospecies of ants from 10 subfamilies and 61 genera. After identification of 148 valid species of the 213 total species collected, 40 species represent new records for Yunnan province and 17 species are newly recorded for China. This increases the total number of named ant species in Yunnan and China to 447 and 951 respectively. The most common species collected were Brachyponera luteipes and Vollenhovia emeryi. Only one confirmed exotic species Strumigenys membranifera, was collected, although several others were potentially introduced by humans. These results highlight the high biodiversity value of the region, but also underscore how much work remains to fully document the native myrmecofauna.

Keywords: China, Formicidae, new records, Xishuangbanna, Yunnan

Introduction

The understanding of regional and global patterns of insect diversity is limited by our incomplete accounting of Earth’s species, especially for tropical regions where species richness peaks in most taxonomic groups. This is also true for Formicidae, an ecologically dominant insect family comprising at least 15,000 described species (Bolton 2014). Despite the ubiquity and ecological importance of ants (Hölldobler and Wilson 1990), many tropical regions remain undersampled even at the generic level (Guénard and Dunn 2012). Compiling and curating complete and accurate species checklists for all regions of the world should be a priority in biodiversity research, especially for diverse insect groups.

Towards that end, here we present the results of an ant survey conducted during the summer of 2013 in the area of Xishuangbanna, Yunnan Province, in the south of China. In particular, our goal here is to document new records of ant species detected in Yunnan, and some new records for China as a whole. The geographic location of Yunnan (ranging from 21.15°N to 29.20°N of latitude) and its topography (elevation range from < 100m to 6740m) render it the most diverse province of China in terms of ant diversity (406 species) (Guénard and Dunn 2012). The same is true for other taxa, such as plants (Li and Walker 1986, Mutke and Barthlott 2005), tiger beetles (Wu and Shook 2007), butterflies (Xie et al. 2009), or amphibians (Chen and Bi 2007). Xishuangbanna prefecture is located in the tropical southwestern region of Yunnan province, bordering Laos and Myanmar, and has been identified as the most diverse region of Yunnan (Long 1995). The ant fauna of Xishuangbanna has been the subject of three studies (Xu 1998, 1999, 2002) and new species are regularly described from this prefecture (e.g. Guénard et al. 2013, Xu et al. 2014a, b). According to Xu’s survey (2002), the myrmecofauna of Xishuangbanna consists of approximately 262 species, which constitute about 65% of the total number of species recorded for Yunnan province.

While elements of China’s ant fauna may be undocumented due to a lack of sampling in certain geographic regions, there are many taxa likely hidden in areas that have been sampled historically. In particular, methods targeting specifically subterranean or leaf litter ants have been rarely used in China, which as a result might bias our detection of ant species from specific strata. One of the most successful sampling techniques for collecting leaf litter ants, Winkler extraction, which is now commonly used for ant fauna surveys all over the world (Olson 1991, Fisher 1999, Agosti et al. 2000, Martelli et al. 2004, Vasconcelos and Lopes 2008, Ivanov and Keiper 2009), has only been used once in China (Hong Kong in Fellowes 1996) to the best of our knowledge. In this study we used Winkler extraction as a standardized collection technique for the first time in order to survey the leaf litter ant fauna of Xishuangbanna. Based predominantly on this highly successful sampling technique, our diversity survey revealed 40 new species records for Yunnan including 17 new records for China. Here we present those new records, as well as their known global distributions by using data information aggregated by the Global Ant BioInformatics project (GABI, Guénard et al. in prep).

Material and methods

Ant specimens were collected from primary forest, secondary forest and rubber plantation habitats near Menglun town, Xishuangbanna Prefecture, Yunnan Province, China during a survey in June 2013. Ants from leaf litter of multiple sites were collected and extracted by mini Winkler extractors for 72 hours using the shuffling method as described in Guénard and Lucky (2011). Ants were also collected by hand on the ground, lower vegetation, and tree trunks.

Samples were first sorted to morphospecies in alcohol, and up to three representatives of each morphospecies per sample were point-mounted. Each mounted specimen was assigned a unique specimen code, in this case a CASENT number, and traditional locality and collection labels. All mounted and alcohol-preserved ant specimens are currently located in EPE’s lab at the Okinawa Institute of Science and Technology Graduate University. Extended depth of field specimen images were taken with an incorporated Leica DFC400 digital camera mounted on a Leica M205C stereomicroscope through the Leica Application Suite V4 software. All specimens were identified to genus using Bolton’s key (Bolton 1994), and then identified to species using available keys (see results section) as well as the digital resources on AntWeb (http://www.antweb.org). All the specimen data are freely available on AntWeb.

Species distributions presented in the following maps are based on records reported here at the country level, or for the larger countries (China, India, Japan), at the first administration level. For large islands (e.g. Borneo, Sumatra, New Guinea) that form natural biogeographic units, we used the island boundary instead of political boundaries similar to a previous study (Guénard and Dunn 2012).

Results

Over 20000 specimens from 61 genera and 213 valid species and morphospecies were collected during this ant diversity survey (Table 1). A total of 40 new species records are presented for Yunnan province. Seventeen of these are recorded for the first time from China. The newly detected species belong to 15 genera from eight subfamilies. It is beyond the scope of the current paper to perform a comprehensive review/revision of the ant fauna of Yunnan Province, which would require much more geographically comprehensive sampling. Here, we present species accounts for the described ant species found during our survey that were previously unknown to Yunnan, supplementing other recently published checklists of the myrmecofauna of the region (Guénard and Dunn 2012).

Table 1.

Ant species (Formicidae) collected from Xishuangbanna, Yunnan in 2013.

Species	Collection record¹
*Aenictinae*
Aenictus artipus Wilson, 1964	N*
Aenictus hodgsoni Forel, 1901	N
Aenictus maneerati Jaitrong & Yamane, 2013	N*
Aenictus paradentatus Jaitrong, Yamane & Tasen, 2012	N*
Aenictus thailandianus Terayama & Kubota, 1993	N
Aenictus clm01
Aenictus clm04
*Amblyoponinae*
Bannapone scrobiceps Guénard, Blanchard, Liu, Yang & Economo, 2013	N*
Mystrium camillae Emery, 1889
*Cerapachyinae*
Cerapachys clm01
Cerapachys sulcinodis Emery, 1889
Cerapachys typhlus (Roger, 1861)
*Dolichoderinae*
Chronoxenus wroughtonii (Forel, 1985)
Dolichoderus affinis Emery, 1889
Dolichoderus laotius Santschi, 1920	N*
Dolichoderus squamanodus Xu, 2001
Dolichoderus thoracicus (Smith, 1860)
Iridomyrmex anceps (Roger, 1863)
Tapinoma indicum Forel, 1895
Tapinoma melanocephalum (Fabricius, 1793)
Tapinoma clm04
Technomyrmex albipes (Smith, 1861)
Technomyrmex horni Forel, 1912
Technomyrmex pratensis (Smith, 1860)	N
*Ectatomminae*
Gnamptogenys costata (Emery, 1989)	N*
Gnamptogenys bicolor (Emery, 1989)
Gnamptogenys treta Lattke, 2004	N*
*Formicinae*
Acropyga nipponensis Terayama, 1985
Anoplolepis gracilipes (Smith, 1857)
Camponotus lasiselene Wang & Wu, 1994
Camponotus mitis (Smith, 1858)
Camponotus parius Emery, 1889
Camponotus singularis Smith, 1858
Camponotus clm02
Camponotus clm03
Camponotus clm04
Camponotus clm07
Camponotus clm08
Camponotus clm09
Echinopla cherapunjiensis Bharti & Gul, 2012	N
Gesomyrmex kalshoveni Wheeler, W.M. 1929	N*
Lepisiota opaca (Forel, 1892)
Lepisiota rothneyi (Forel, 1894)
Myrmoteras binghamii Forel, 1893
Myrmoteras cuneonodum Xu, 1998
Nylanderia clm01
Nylanderia clm02
Nylanderia clm03
Nylanderia clm04
Nylanderia clm05
Nylanderia clm06
Oecophylla smaragdina (Fabricius, 1775)
Paraparatrechina clm01
Paraparatrechina clm02
Paraparatrechina clm03
Paraparatrechina clm04
Plagiolepis clm01
Polyrhachis armata (Le Guillou, 1842)
Polyrhachis bicolor Mayr, 1862
Polyrhachis bihamata (Drury, 1773)
Polyrhachis furcata Emery, 1889
Polyrhachis halidayi Emery, 1889
Polyrhachis hippomanes Smith, 1861
Polyrhachis illaudata Walker, 1859
Polyrhachis illaudata pauperata Emery, 1889
Prenolepis naoroji Forel, 1902
Prenolepis sphingthoraxa Zhou & Zheng, 1998	N
Pseudolasius cibdelus Wu & Wang, 1992
Pseudolasius emeryi Forel, 1915
Pseudolasius silvestrii Wheeler, 1927
*Myrmicinae*
Acanthomyrmex luciolae Emery, 1893
Aphaenogaster beccarii Emery, 1887
Aphaenogaster feae Emery, 1889
Aphaenogaster clm05
Cardiocondyla wroughtonii (Forel, 1890)
Carebara affinis (Jerdon, 1851)
Carebara altinoda (Xu, 2003)
Carebara bruni (Forel, 1913)
Carebara diversa (Jerdon, 1851)
Carebara melasolena (Zhou & Zheng, 1997)	N
Carebara clm01
Carebara clm05
Carebara clm06
Carebara clm07
Carebara clm08
Carebara clm09
Carebara clm10
Carebara clm11
Carebara clm12
Carebara clm13
Cataulacus granulatus (Latreille, 1802)
Crematogaster dohrni Mayr, 1879
Crematogaster ferrarii Emery, 1888
Crematogaster millardi Forel, 1902
Crematogaster osakensis Forel, 1900
Crematogaster politula Forel, 1902
Crematogaster rothneyi Mayr, 1879
Crematogaster clm05
Crematogaster clm09
Crematogaster clm10
Crematogaster clm11
Dilobocondyla fouqueti Santschi, 1910
Kartidris ashima Xu & Zheng, 1995
Lophomyrmex quadrispinosus (Jerdon, 1851)
Lordomyrma idianale Taylor, 2012
Meranoplus laeviventris Emery, 1889
Monomorium chinense Santschi, 1925
Monomorium pharaonis (Linnaeus, 1758)
Monomorium clm01
Monomorium clm02
Monomorium clm05
Monomorium clm06
Myrmecina curvispina Zhou, Huang & Ma L., 2008	N
Myrmecina guangxiensis Zhou, 2001	N
Pheidole hongkongensis Wheeler, 1928	N
Pheidole noda Smith, 1874
Pheidole pieli Santschi, 1925
Pheidole plagiaria Smith, 1860	N
Pheidole planifrons Santschi, 1920	N
Pheidole roberti Forel, 1902
Pheidole rugithorax Eguchi, 2008	N
Pheidole sagei Forel, 1902
Pheidole smythiesii Forel, 1902	N
Pheidole tumida Eguchi, 2008	N
Pheidole vieti Eguchi, 2008	N*
Pheidole zoceana Santschi, 1925	N
Pheidole clm03
Pheidole clm04
Pheidole clm07
Pheidole clm12
Pheidole clm13
Pheidole clm16
Pheidole clm18
Pheidole clm22
Pheidole clm13
Pristomyrmex brevispinosus Emery, 1887
Pristomyrmex hamatus Xu & Zhang, 2002
Pristomyrmex punctatus (Smith, 1860)
Recurvidris recurvispinosa (Forel, 1890)
Recurvidris kemneri (Wheeler & Wheeler, 1954)	N*
Solenopsis jacoti Wheeler, 1923
Strumigenys ailaoshana (Xu & Zhou, 2004)
Strumigenys dyschima (Bolton, 2000)	N*
Strumigenys exilirhina Bolton, 2000
Strumigenys feae Emery, 1895
Strumigenys kichijo (Terayama, Lin & Wu, 1996)	N
Strumigenys lyroessa (Roger, 1862)
Strumigenys membranifera Emery, 1869
Strumigenys mitis (Brown, 2000)	N
Strumigenys mutica (Brown, 1949)
Strumigenys nanzanensis Lin & Wu, 1996
Strumigenys nepalensis Baroni Urbani & De Andrade, 1994	N*
Strumigenys rallarhina Bolton, 2000	N
Strumigenys sauteri (Forel, 1912)	N
Tetramorium aptum Bolton, 1977
Tetramorium ciliatum Bolton, 1977
Tetramorium difficile Bolton, 1977	N*
Tetramorium flavipes Emery, 1893	N*
Tetramorium kheperra (Bolton, 1976)
Tetramorium kraepelini Forel, 1905
Tetramorium nipponense Wheeler, 1928
Tetramorium parvispinum (Emery, 1893)	N
Tetramorium polymorphum Yamane & Jaitrong, 2011	N*
Tetramorium tonganum Mayr, 1870	N
Tetramorium clm03
Tetramorium clm10
Tetramorium clm18
Tetramorium clm19
Vollenhovia emeryi Wheeler, 1906
*Ponerinae*
Anochetus graeffei Mayr, 1870
Anochetus mixtus Radchenko, 1993
Anochetus myops Emery, 1893
Anochetus clm04
Brachyponera luteipes (Mayr, 1862)
Diacamma clm01
Ectomomyrmex astutus (Smith, 1858)
Ectomomyrmex leeuwenhoeki (Forel, 1886)
Ectomomyrmex lobocarenus (Xu, 1995)
Ectomomyrmex clm01
Ectomomyrmex clm02
Ectomomyrmex clm03
Ectomomyrmex clm04
Emeryopone melaina Xu, 1998
Hypoponera clm01
Hypoponera clm02
Hypoponera clm03
Hypoponera clm04
Hypoponera clm05
Hypoponera clm06
Hypoponera clm07
Leptogenys birmana Forel, 1900
Leptogenys chinensis (Mayr, 1870)
Leptogenys crassicornis Emery, 1895
Leptogenys diminuta (Smith, 1857)
Leptogenys lucidula Emery, 1895
Leptogenys mengzii Xu, 2000
Leptogenys clm01
Leptogenys clm02
Leptogenys clm09
Myopias hania Xu & Liu, 2011
Odontomachus clm01
Odontoponera denticulata (Smith, 1858)	N
Platythyrea parallela (Smith, 1859)
Pseudoneoponera rufipes (Forel, 1911)
*Proceratinae*
Discothyrea clavicornis Emery, 1897	N*
Discothyrea kamiteta Kubota & Terayama, 1999	N
Probolomyrmex longiscapus Xu & Zeng, 2000
Proceratium deelemani Perrault, 1981	N*
*Pseudomyrmecinae*
Tetraponera amargina Xu & Chai, 2004
Tetraponera allaborans (Walker, 1859)
Tetraponera attenuata Smith, 1877
Tetraponera concava Xu & Chai, 2004

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N = New to Yunnan province; N* = New to China.

Tetramorium polymorphum has been collected from leaf litter in secondary forest, and is known to be an exotic species in China (Guenard and Dunn 2012). Despite its wide distribution and tramping ability, there is very little information about its biology. In addition to Bolton (1977), Sarnat and Economo (2012) also confirm that Tetramorium tonganum is able to establish populations outside its native range without damaging or significantly altering ecological or agricultural systems in its introduced habitats. They also report that Tetramorium tonganum is mostly found on vegetation in disturbed or edge habitats.

Discussion

The total number of named ant species in China is 939, but the true species richness is expected to be significantly higher, perhaps as high as 1200 to 1600 species (Guénard and Dunn 2012). The collection of these 40 new ant records for Yunnan and 17 for China through Winkler extraction, combined with the discovery of the extremely rare ant species Bannapone scrobiceps (Guenard et al. 2013), should encourage myrmecologists to consider leaf litter extraction as one of the primary methods to collect leaf litter ants, especially for places where this method has not previously been used. Nevertheless, further sampling methods that specifically target different strata will very likely yield additional species, which is especially true for hypogaeic and arboreal ant communities.

Based on our collections, many newly recorded species, such as Discothyrea clavicornis, Myrmecina curvispina, and Odontoponera denticulata are relatively common. The reason why those species were never reported from Yunnan before may be due to different collection techniques and/or misidentifications. For example, Odontoponera denticulata has long been misidentified as Odontoponera transversa (Yamane 2009). Another reason may be that some of the newly recorded species have been described only recently outside of Yunnan and/or China, such as Myrmecina curvispina and Pheidole tumida (Zhou et al. 2008, Eguchi 2008).

Many new species records in our collection such as Aenictus artipus, Aenictus maneerati, Aenictus paradentatus, Discothyrea clavicornis, Dolichoderus laotius, Gesomyrmex kalshoveni, Gnamptogenys treta, Pheidole plagiaria, Pheidole planifrons, Pheidole rugithorax, Pheidole tumida, Pheidole vieti, Recurvidris kemneri, Strumigenys dyschima, Strumigenys mitis, Tetramorium difficile, Tetramorium flavipes, Tetramorium parvispinum, and Tetramorium tonganum, are at the northern limit of their known distribution in Yunnan. Interestingly, the occurrence of several species in Yunnan, such as Discothyrea clavicornis, Gesomyrmex kalshoveni, Gnamptogenys treta, Recurvidris kemneri, and Strumigenys dyschima constitutes a disjunction from the rest of their known distribution in the Malay Peninsula. At present, it is unclear if these represent sampling artifacts and the ranges are actually continuous in the region, if these species ranges represent true biogeographic disjunctions, or if they are actually different species. Only future diversity inventories and taxonomic treatments, of which this paper represents one modest contribution, can answer these questions and further resolve the biodiversity map for ants and other organisms.

Despite the comparatively short collecting time we invested in the inventory of the myrmecofauna, we were able to identify 145 species, of which over 30% represent new records. This increases the list of known species for Yunnan by 10%, and there are still more than 60 species that we tentatively consider undescribed. This shows how little was previously known about the ant fauna of the region, and we are convinced that more intensive sampling in different habitats and microhabitats will likely reveal the presence of even more species or help improve the current taxonomic resolution. In this context, we think that Yunnan should be considered an area of high biodiversity value and deserving of attention of both biologists and conservationists. Regrettably, this interesting biota is being degraded at an alarming speed, particularly due to the rapid expansion of rubber plantations in the area (Li et al. 2007).

Supplementary Material

XML Treatment for Aenictus artipus

zookeys.477.8775-treatment1.xml^{(6.4KB, xml)}

XML Treatment for Aenictus hodgsoni

zookeys.477.8775-treatment2.xml^{(6.2KB, xml)}

XML Treatment for Aenictus maneerati

zookeys.477.8775-treatment3.xml^{(5.9KB, xml)}

XML Treatment for Aenictus paradentatus

zookeys.477.8775-treatment4.xml^{(6KB, xml)}

XML Treatment for Aenictus thailandianus

zookeys.477.8775-treatment5.xml^{(6.2KB, xml)}

XML Treatment for Bannapone scrobiceps

zookeys.477.8775-treatment6.xml^{(5.4KB, xml)}

XML Treatment for Carebara melasolena

zookeys.477.8775-treatment7.xml^{(5KB, xml)}

XML Treatment for Discothyrea clavicornis

zookeys.477.8775-treatment8.xml^{(8.4KB, xml)}

XML Treatment for Discothyrea kamiteta

zookeys.477.8775-treatment9.xml^{(5.8KB, xml)}

XML Treatment for Dolichoderus laotius

zookeys.477.8775-treatment10.xml^{(4.7KB, xml)}

XML Treatment for Echinopla cherapunjiensis

zookeys.477.8775-treatment11.xml^{(5.1KB, xml)}

XML Treatment for Gesomyrmex kalshoveni

zookeys.477.8775-treatment12.xml^{(5.5KB, xml)}

XML Treatment for Gnamptogenys costata

zookeys.477.8775-treatment13.xml^{(5.1KB, xml)}

XML Treatment for Gnamptogenys treta

zookeys.477.8775-treatment14.xml^{(6.4KB, xml)}

XML Treatment for Myrmecina curvispina

zookeys.477.8775-treatment15.xml^{(9.1KB, xml)}

XML Treatment for Myrmecina guangxiensis

zookeys.477.8775-treatment16.xml^{(6KB, xml)}

XML Treatment for Odontoponera denticulata

zookeys.477.8775-treatment17.xml^{(11.7KB, xml)}

XML Treatment for Pheidole hongkongensis

zookeys.477.8775-treatment18.xml^{(8.2KB, xml)}

XML Treatment for Pheidole plagiaria

zookeys.477.8775-treatment19.xml^{(6KB, xml)}

XML Treatment for Pheidole planifrons

zookeys.477.8775-treatment20.xml^{(9.6KB, xml)}

XML Treatment for Pheidole rugithorax

zookeys.477.8775-treatment21.xml^{(5.9KB, xml)}

XML Treatment for Pheidole smythiesii

zookeys.477.8775-treatment22.xml^{(6.3KB, xml)}

XML Treatment for Pheidole tumida

zookeys.477.8775-treatment23.xml^{(10.9KB, xml)}

XML Treatment for Pheidole vieti

zookeys.477.8775-treatment24.xml^{(5.7KB, xml)}

XML Treatment for Pheidole zoceana

zookeys.477.8775-treatment25.xml^{(10KB, xml)}

XML Treatment for Prenolepis sphingthoraxa

zookeys.477.8775-treatment26.xml^{(4.9KB, xml)}

XML Treatment for Proceratium deelemani

zookeys.477.8775-treatment27.xml^{(5.2KB, xml)}

XML Treatment for Recurvidris kemneri

zookeys.477.8775-treatment28.xml^{(6.3KB, xml)}

XML Treatment for Strumigenys dyschima

zookeys.477.8775-treatment29.xml^{(5KB, xml)}

XML Treatment for Strumigenys kichijo

zookeys.477.8775-treatment30.xml^{(5KB, xml)}

XML Treatment for Strumigenys mitis

zookeys.477.8775-treatment31.xml^{(10.6KB, xml)}

XML Treatment for Strumigenys nepalensis

zookeys.477.8775-treatment32.xml^{(10KB, xml)}

XML Treatment for Strumigenys rallarhina

zookeys.477.8775-treatment33.xml^{(6.9KB, xml)}

XML Treatment for Strumigenys sauteri

zookeys.477.8775-treatment34.xml^{(5.5KB, xml)}

XML Treatment for Technomyrmex pratensis

zookeys.477.8775-treatment35.xml^{(5.4KB, xml)}

XML Treatment for Tetramorium difficile

zookeys.477.8775-treatment36.xml^{(6.2KB, xml)}

XML Treatment for Tetramorium flavipes

zookeys.477.8775-treatment37.xml^{(6.7KB, xml)}

XML Treatment for Tetramorium parvispinum

zookeys.477.8775-treatment38.xml^{(7KB, xml)}

XML Treatment for Tetramorium polymorphum

zookeys.477.8775-treatment39.xml^{(10.2KB, xml)}

XML Treatment for Tetramorium tonganum

zookeys.477.8775-treatment40.xml^{(8KB, xml)}

Acknowledgments

We would like to thank Yan-Qiong Peng, and Jia-jia Liu for their assistance and advice on conducting this ant diversity survey. We also thank B. Bolton, P.S. Ward, G. Fischer, and M. Yoshimura for their help in ant identification. The authors acknowledge the support of OIST and an NSF grant to EPE (NSF DEB-1145989).

Citation

Liu C, Guénard B, Garcia FH, Yamane S, Blanchard B, Yang D-R, Economo E (2015) New records of ant species from Yunnan, China. ZooKeys 477: 17–78. doi: 10.3897/zookeys.477.8775

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