Taxonomy of the tribe Ozophorini (Lygaeoidea: Rhyparochromidae) in Oriental region

UNIVERSITY OF PANNONIA GEORGIKON FACULTY KESZTHELY FESTETICS DOCTORAL SCHOOL Head of School: Dr. Anda Angéla D. Sc. Thesis of Doctoral (Ph.D ) Dissertation Taxonomy of the tribe Ozophorini (Lygaeoidea: Rhyparochromidae) in Oriental region Supervisor: Dr. Kondorosy Előd Associate Professor Written by Varga Katinka Keszthely 2016 1

1. Introduction and aims Currently there approximately 40.000 known species of true bugs. (SCHUH & SLATER 1995). They can be found almost anywhere on the planet, they populate water and land habitats alike. During our research, I studied specific groups of Lygaeoidea specimen in identified and unidentified museum collections with my advisor. The taxonomic position of some species is not clear and there are plenty undescribed. We did numeric and morphological studies along with genital studies. In my dissertation, I present the identified new species described by us in the tribe Ozophorini family Rhyparochromidae, but I did research in other groups as well. Research history During the latter half of 19 th and in the early 20 th century, several renowned lygaeid researchers were active like C. StaL, E. Bergorth, G. Breddin, W. L. Distant and W. E. China, who studied the oriental Lygaeoidea taxons as well. Géza Horváth, our world renowned true bug researcher also did excellent work on lygaeids (141 species described by him are still valid today), his monograph Magyarország bodobácsféléinek magánrajza ( The monograph of the Hungarian lygaeids ) he gives detailed morphological description of the group (HORVÁTH 1875). The Fauna Regni Hungariae mentions 115 Lygaeidae species in the present region of Hungary (HORVÁTH 1897). In the second half of the 20 th century, the interest in researching lygaeids had once again risen. This time J. A. Slater and G. G. E. Scudder started working with these insects. On many occasions, Slater worked together with other researchers like L. Y Zheng, P. D. Ashlock, J. E. O Donnell and M. H. Sweet. Slater broadened his research to almost every continent. 2

In 1964, A Catalogue of the Lygaeidae of the World was published by SLATER with all the known species and their bibliography, and later in 1995 he published a supplemental catalogue which contained new literature and was co-authored with O DONNELL. Slater did tremendous work related to taxonomical, morphological and bibliographical studies in the Lygaeoidea groups (SLATER & HURLBUTT 1957, SLATER & WOODWARD 1982). In 1997, a research published by HENRY revised the taxons in the Lygaeoidea superfamily, detailing their relationship connections. The result of this research was the elevation of some subfamilies to family level like the subfamily Rhyparochrominae. Since this publication is the latest review dealing with lygaeid taxonomy, in my dissertation description of the family Rhyparochromidae refers to the earlier Rhyparochrominae subfamily. The zoogeographical status of the family Rhyparochromidae (then Rhyparochrominae subfamily) is discussed by SLATER in his 1986 publication: A Synopsis of the Zoogeography of the Rhyparochrominae (Heteroptera: Lygaeidae). In 1999, PÉRICART published his three volume book about Lygaeidae (sub)families, which contained the morphology, description and distribution of European subfamilies and species. The subfamily Rhyparochromine was described by AMYOT & SERVILLE in 1843 (as Rhyparochromides). STÅL in 1872 wrote about the European lygaeids and in 1874 about the lygaeids of the world. In these publications he established the Myodochina (now Rhyparochromidae) subfamily with seven tribes, only partially matching today s contents. 3

In the 1967 comprehensive publication of Sweet, he uses the current knowledge and nomenclature for the morphological attributes of the tribes, describes the Ozophorini and Udeocorini genera and provides keys to the genera. The research history of the Ozophorini tribe has gone a long way. For a long time it was included in the Myodochini tribe since it is rather similar to this tribe, so much so that for example SCUDDER (1957) incorrectly put the genus Vertomannus here (calling it Plociomerina at the time). The other genera in the present-day Ozophorini tribe are mentioned by him in the description of the Stygnocorini tribe, although he notes that the sperm reservoir is very similar to Rhyparochromini species (SCUDDER 1957). However, SWEET (1967) put these genera in their current place in the Ozophorini tribe. Slater and Zheng together revised the Prosomoeus, Primierus and Porta genera and also described the monotypic Gressittocoris genus SLATER & ZHENG 1985. Zheng during his work described many (30) species from China. From the Ozophorini tribe, the description of the monotypic Paraporta genus is attributed to him, as well as the addition of five new species to the once monotypic Vertomannus genus, also examined by me (ZHENG & ZOU 1981). The Ozophorini tribe can be found all around the world, and the most species are known from the tropical areas of America (SLATER 1964, SLATER & O DONNELL 1995). These American groups (especially the numerous Ozophora Uhler, 1871) are the most researched in this tribe (ASHLOCK & SLATER 1982, SLATER 1995, BRAILOVSKY & CERVANTES 2009). 4

The second most diverse habitat of these bugs is the Oriental and Pacific region, with 82 described species from 12 genera. The Papuan subregion is especially rich in species, we know 35 species from New-Guinea and the SolomonI Islands. In contrast, we know only of 5 species from the Philippines and only 11 from the Indo- Malayan region. There are 13 described species from China (ZHENG & ZOU 1981, LI & BU 2015). The Oriental and the Pacific regions are less studied regarding lygaeid habitats. During our research, we studied specimens collected from the Oriental region and we also studied material from different European museums. Our research focused on the undescribed Ozophorini tribe specimens. The morphological features of the family Rhyparochromidae: The body is usually dark in colour. The head is usually small compared to the body. Long trichobothria can be observed on the head. Their pronotum is well developed. The corium is sparsely punctate, the clavus has rows of punctures The numbers of the rows are different in each genera. Ventral trichobothria are aligned medially on the 3 rd and 4 th abdominal segments and laterally on the 5 th -6 th -7 th segments. Usually there are three trichobothria on each segment. The ovipositor spawns from the 7 th abdominal segment, dividing it into two parts. It is typical for the male reproductive organ to have a spiral projection (helical process) on the phallus. The suture between the 5 th and 6 th abdominal segments is curving anterial but does not reach the ventral abdominal margin (SLATER & WOODWARD 1982). 5

The morphological features of the tribe Ozophorini: The relation between the genera in this tribe are based on the developed venal structure on the second pair of wings, the location of the trichobothria and the spiracles, the structure of the phallus, the shape of the pronotum, and the suture on the head. My aims are the following: - revision of the already known genera, writing detailed description of the new species belonging to the genera (pygophore dissection, making photographs and drawings) - searching for new key features in the Ozophorini group - studying, documenting and photographing type specimens - clarification of the relation between the species of the genera from the old-world gene center. 2. Applied methods During our work, we strictly followed the guidelines of the International Code of Zoological Nomenclature (ICZN 1999). Beside the species description, we also commented on the features which separate them from the related species, we designated a type species for the new subgenus, we designated holo- and paratypes for the new species, and as for the already known old species where there were only syntypes available we designated lectotypes and paralectotypes. I did the majority of my research on the following microscopes: Stereomicroscope type: Olympus SZ 11, Alpha STO zoom, Light microscope type: Alpha SA 3300. I measured the animals with the help of an ocular micrometer. 6

During our research we examined specimens borrowed from European museums and type specimens in these museums. List of museums with examined specimens: BMNH Natural History Museum, London, United Kingdom; HNHM Hungarian Natural History Museum, Budapest, Hungary; IRSN Royal Belgian Institute of Natural Sciences, Brussels, Belgium; MFNB Natural History Museum, Berlin, Germany; MMBC Moravian Museum, Brno, Czech Republic; MNHN National Natural History Museum, Paris, France NHMW Natural History Museum, Vienna, Austria; NHRS Swedish Museum of Natural History, Stockholm, Sweden; NMWC National Museum of Wales, Cardiff, United Kingdom; RMNH National Museum of Natural History (Naturalis), Leiden, the Netherlands; TLMF Tirolese Regional Museum (Ferdinandeum), Innsbruck, Austria. ZMAN Zoological Museum, Amsterdam; A species or other taxa can be distinguished from another with the key features that are typical for that group. Key features are the attributes (present or absent) that separate two species. These key features can be rather different in species, genera and families. I established possible relationship connections, which I presented on a cladogram. To be absolutely sure about the position of a specimen, the knowledge of the key features is vital. There are many species which are almost impossible to distinguish based on outer key features. In these cases we can use the unique features of the genitals to separate them. 7

3. Results Genus Tachytatus was described by BERGROTH in 1918 with one species (Tachytatus prolixicornis) from the Philippines. After further studies, additional specimens were discovered from Malaysia and North-Sumatra. During our research, we described three new species, so the revision of the genus was timely. The suggested relationship connections were displayed on a cladogram (Fig. 1.). The specific features of the new species are the following: Tachytatus redeii Perhaps this is the most similar species to the T. prolixicornis but has a larger stature. Its membrane is darker than T. prolixicornis and the spot before the apex of the corium is larger. Distribution: Siberut Island. Tachytatus celebensis The most decorative species from the genus. It can easily be separated by the contrasting colouration. Its special feature is the sickle shaped spot on the edge of the membrane, which is curved contrary to the other species of this genus. Distribution: Celebes (Sulawesi Utara). Tachytatus longirostris This species is the easiest to identify in the genus since it is the only one with yellow and light brown colouration in contrast with other species which have dark brown base tone. Its labium is long, it can reach the 5 th abdominal segment. Distribution: Celebes (Sulawesi Utara). 8

Figure 1: The cladogram of the genus Tachytatus The genus Vertomannus was described by Distant in 1903 (V. capitatus). Since then several researchers described additional 7 species: V. crassus, V. validus, V. brevicollum, V. emeia, V. ophiocephalus, V. parvus, V. tibetanus. The species in this genus can be easily recognized by their elongated neck. As a result of our research, we added two new species to this genus. One of the new species is from Borneo, which is a new distribution area for the genus. The other species is rather different from the species ofhis genus, so we decided to establish a new subgenus (Elongatomannus). In Figure 2, the potential relationship of the species is presented on a cladogram. The new species and their special features are the following: Vertomannus (Elongatomannus) flavus The only species in this genus which has yellow colouration, its head is not rounded but elongated, reaching forward. Distribution: Vietnam, Laos. 9

Vertomannus borneensis Head rounded, shining, body dark brown. It is one of the smaller species in this genus. Labium does not reach the procoxa. Distribution: Borneo. Figure 2: Cladogram of the genus Vertomannus The genus Porta was described by Distant in 1903 (P. gracilis). In 1985 SLATER & ZHENG published P. illustris and P. longipes species. After we examined the available specimens, we added a new species to this genus. The species usually have dark colouration and have a pair of spines on their pronotum. The relationships in this genus are presented in Figure 3. Porta longirostris This species has the longest labium in the genus. Distribution: Middle Borneo. 10

Figure 3: Cladogram of the genus Porta, based on my own examination and Slater & Zheng 1985 The genus Primierus was described by Distant in 1901 with two species. Later Slater, Zheng & Zou expanded the genus. As a result of the work of these researchers, today we know seven described species from this genus. After studying the museum specimens we described four new species and made the potential raltionship cladogram of the genus (Fig. 4.). Primierus zetteli Similar to P. indicus, but its legs and scutellum is not red but light brown. The fore femora are not thickened on the new species and its labium does not reach the mid coxae. Distribution: South China (Jünnan). Primierus tenuis Similar to the previous species, but has a longer body, it is more slender, its labium is reaching the mid coxae. The head is long before compound eyes. Body colouration is more homogeneous, the spot on the apex of the corium is not explicit. Distribution: Northeast India (Meghalaya, Assam, Nagaland) 11

Primierus decoratus Its body is larger and darker than the other new species. It has a bright spots on the corium which the other species lack. Its membrane is light brown, with light brown spots while the other species contrary to this have brown membrane with light-yellow spots. Labium reaches the mid coxae. Distribution: East Borneo (Kalimantan), West Java. Primierus javanus The colouration of the body lighter, apical corial spot visible. At ¼ of the 4 th antennal segment there is a white ring. Distribution: West Java. Figure 4: Cladogram of the genus Primierus based on own examination 12

The genus Salaciola, which is endemic in Africa, was described by BERGROTH in 1906. As a result of the work of Linnavuori and Slater, today we know 21 described species belonging to this taxon. Salaciola goellnerae S. goellnerae is a bigger, more robust species, with uniform brown antennal segments and the pattern of the corium is different from the other species in this genus. There are no big spots on the membrane, the anterior pronotal lobe is not swollen and the fore femora is unarmed. Meschia and Heissothignus genus The genus Meschia was described by DISTANT in 1910, while the genus Heissothignus was described by SLATER & BRAILOVSKY in 2006. Based on all the studied features, these genera have the attributes of the Heterogastridae family, so we think they should be put in this family. The specimens of the two genera have stocky bodies in contrast to the species belonging to the family Heterogastridae. The antennae are widely separated from the eyes, unlike on the other species, roughly as far as the diameter of the compound eye, the mandibular plates are elongated in an edge (on the other Heterogastridae species it slicks to the clypeus). Their heads are broad, eyes usually stalked, which is especially observable on the Heissothignus genus. All these differences separate them from the other Heterogastrinae species, and we decided to establish a new subfamily, which would have been named Meschiinae, but in the meantime unfortunately Malipatil described it as a family in 13

2014. He did not work on the genus Heissothignus, so this result is a new discovery. 4. Thesis points 1. Revision of the genus Tachytatus. Designation of the lectotype of T. prolixicornis and the expansion of its distribution area, also the description of three new species: Tachytatus celebensis Varga et Kondorosy, 2014, Tachytatus redeii Varga et Kondorosy, 2014, Tachytatus longirostris Varga et Kondorosy, 2014. 2. Revision of the genus Vertomannus, establishing of a new subgenus (Elongatomannus Varga et Kondorosy 2013), expansion of the distribution area of the species, described two new species: Vertomannus flavus Varga et Kondorosy, 2013, Vertomannus borneensis Varga et Kondorosy, 2013. 3. Addition of a new species in the genus Porta: Porta longirostris Kondorosy, Varga et Zsalakovics, 2012 4. Addition of 4 new species to genus Primierus: P. zetteli sp. nov., P. tenuis sp. nov., P. decoratus sp. nov., P. javanus sp. nov. 5. We made the first key to the Oriental and Pacific Ozophorini genera, with taking the possible relationships into account without detailed phylogenetic examination. We separated the genera with the help of the theoretical relationships and I established the possible phylogenetic tree of the genera. 14

6. New key feature: I used the new key feature, the colouration of the hemelytral membrane successfully, which is important on my opinion, since the researchers who studied this genera did not mention this in previous works, even though it is an important feature. I suggest taking this key feature into consideration in the future. - During the study of the Drymini tribe I determined the following new scientific results: 7. Expansion of the genus Salaciola with the addition of a new species: S. goellnerae, Kondorosy et Varga, 2012. - During the study of the genera Meschia and Heissothignus, I determined the following new scientific results: 8. We determined that these genera are related and belong to an individual subfamily inside the family Heterogastridae since then Malipatil elevated the Meschia genus to family level. The classification of the genus Heissothignus into this family and the discovery of several new species are one of our unpublished results. 15

5. References 1. AMYOT, C. J. B., SERVILLE, A. (1843) Histoire naturelle des insectes Hemipteres. Librairie Encyclopedique de Roret, Paris, p. 675. 2. ASHLOCK, P. D., SLATER J. A. (1982): A review of the Genera of Western Hemisphere Ozophorini with two new genera from Central America (Hemiptera-Heteroptera: Lygaeidae). Journal of the Kansas Entomological Society, 55 (4): 737 750. 3. BERGROTH, E. (1906): Neue Hemiptera aus Madagascar. Wiener Entomologische Zeitung 25 (1): 17-19. 4. BERGROTH, E. (1918): Studies in Philippine Heteroptera. I.Philippine Journal of Science, 13 (3): 75-77. 5. BRAILOVSKY, H., CERVANTES-PEREDO, L. (2009): New genus and three new species of leaf-litter-inhabiting Ozophorini (Hemiptera: Heteroptera: Lygaeoidea: Rhyparochromidae: Rhyparochromidae). Annals of the Entomological Society of America, 102 (6): 959 963. 6. DISTANT, W. L. (1901): In: Rhynchotal notes. XI. Heteroptera: Family Lygaeidae. Annals and Magazine of Natural History, 8: 464-486 7. DISTANT, W. L. (1903): Contributions to a knowledge of the Rhynchota. Annales de la Société Entomologique de Belgique 89: 44 46. 8. DISTANT, W. L. (1910): In Heteroptera: Appendix. V. Rynchota. The fauna of British India, Ceylon and Burma. p. 362. 9. HENRY, T. J. (1997): Phylogenetic analysis of family groups within the infraorder Pentatomomorpha (Hemiptera: Heteroptera) with Emphasis on Lygaeoidea. Annals of the Entomological Society of America 90 (3): 275-301. 10. HORVÁTH G. (1875): Lygaeidarum Hungariae, Magyarország bodobácsféléinek magánrajza. Kir. Magyar Természettudományi Társulat, p. 130. 16

11. HORVÁTH G. (1897): Fauna Regni Hungariae, A Magyar Birodalom Állatvilága. Kir. Magyar Természettudományi Társulat. p.72. 12. LI, J.-L., BU, W-J. (2015): Review of the genus Vertomannus Distant (Hemiptera: Heteroptera: Lygaeoidea: Rhyparochromidae: Ozophorini), with description of two new species. Zootaxa 3972 (4): 581 588. 13. MALIPATIL, M. B. (2014): Meschiidae, a new family of Lygaeoidea (Hemiptera: Heteroptera) from India and Australia, with descriptions of a new genus and two new species. Zootaxa, 3815 (2): 233-248. 14. PÉRICART, J. (1999): Faune de France I-III., Hémiptéres Lygaeidae Euro- Mediterranéens, Fédération Française des Sociétés de Sciences Naturelles- Paris. 84-A, 84-B, 84-C 15. SCHUH, R. T., SLATER, J. A. (1995): True Bugs of The World (Hemiptera: Heteroptera). Cornell University Press, New York. p. 1-41., 246-266. 16. SLATER, J. A. (1964): A Catalogue of the Lygaeidae of the World I-II. University of Connecticut Storrs, New York, p.1668 17. SLATER, J. A. (1986): A synopsis of the zoogeography of the Rhyparochrominae (Heteroptera: Lygaeidae) Contributions on Heteroptera. Journal of the New York Entomological Society, 94 (2): 262-280 18. SLATER, J. A., BRAILOVSKY, H. (2006): A new genus and three new species of Lygaeoidea from New Guinea (Heteroptera, Lygaeoidea). In: Rabitsch, W. (ed.): Hug the bug for love of true bugs. Denisia 19, zugleich Kataloge der Oberösterreichischen Landesmuseen, 647-652. 19. SLATER, J. A., HURLBUTT, H. W. (1957): A comparative study of the metathoratic wing in the family Lygaeidae (Hemiptera, Heteroptera). Entomological Society, Washigton, 59 (2): 67-77. 17

20. SLATER, J. A., WOODWARD, T. E. (1982): Lilliputocorini, a new tribe with six new species of Lilliputocoris, and cladistic analysis of the Rhyparochrominae (Hemiptera, Lygaeidae). American Museum Novitates, 2754: 1-23. 21. SLATER, J. A., ZHENG L.Y. (1985): Revision of the lygaeid genera Porta and Primierus (Hemiptera: Heteroptera), with the description of a new genus of Ozophorini from Papua New Guinea (Heteroptera). Systematic Entomology, 10: 453-469. 22. SLATER, J. A., O DONNELL, J. E. (1995): A catalogue of the Lygaeidae of the world (1960-1994). New York Entomological Society, New York, p. 410. 23. STÅL, C. (1872) Genera Lygaeidarum Europae disposuit. Öfversigt af Kongl. Vetenskaps-Akademiens Förhandlingar, 29: 37-62. 24. STÅL, C. (1874): Enumeratio Lygaeidarum Extraeuropaearum. In: Enumeratio Hemipterorum Vol. IV. Kongl. Svenska Vetenskaps-Akademiens Handlingar, 12 (1): 98-170. 25. SWEET, M. H. (1967): The tribal classification of the Rhyparochrominae (Heteroptera, Lygaeidae).Entomological Society of America pp. 208-226. 26. ZHENG, L., ZOU, H. G. (1981) Lygaeidae. In: Hsiao TY (Ed) A handbook for the determination of the Chinese Hemiptera- Heteroptera vol. 2.. Science Press, Beijing, 1 215, plates 1 26. [in Chinese, English summary], pp: 589-612. 18

6. Publications Scientific presentations in the topic of the dissertation: 1. VARGA K., KONDOROSY E. (2011): Új bodobács alcsalád a láthatáron?(taxonómiai kutatások Délkelet-Ázsiában). XVII. Ifjúsági Tudományos Fórum 2011. 04. 21. ISBN: 978-963- 9639-42-3 2. VARGA K., KONDOROSY E. (2011): Revision of genus Tachytatus (Heteroptera, Pentatomomorpha, Lygaeoidea, Rhyparochromidae). Young Systematists Forum, Flett Theatre, Natural History Museum, London, UK, 2011. 12.01., Abstracts: 27./ 23. p. 3. VARGA K., KONDOROSY E. (2012): Zsiráfnyakú bodobácsok Ázsiából. XVIII. Ifjúsági Tudományos Fórum 2012. 04. 19. ISBN: 978-963-9639-45-4 4. VARGA K., KONDOROSY E. (2012): Studies on the genus Vertomannus (Heteroptera: Rhyparochromidae: Ozophorini). Sixth European Hemiptera Congress, Bulgária, Blagoevgrad 2012. 06. 25-29. Abstracts: 107. p 5. VARGA K., KONDOROSY E. (2012): Betekintés a bodobácsok óvilági csoportjainak taxonómiájába. ELTE- Környezettudományi DI Konferenciája 2012. 08. 30-31. ISBN: 978-963-284-242-4 19

6. VARGA K., KONDOROSY E. (2012): Preliminary key for the Oriental genera of Ozophorini (Insecta, Heteroptera, Rhyparochromidae), XIV. Young Systematists Forum Flett Theatre, Natural History Museum, London, UK 2012. 11. 29. Abstracts: 14./17.p. 7. VARGA K., KONDOROSY E. (2013): Tanulmányok egy délkelet-ázsiai bodobács (Rhyparochromidae) genuszon. II. Interdiszciplináris Doktorandusz Konferencia 2013. 05. 15-17. ISBN 978-963-642-598-2 Scientific publications in the topic of the dissertation: 1. KONDOROSY E., VARGA K. (2012): A new species of Salaciola Bergroth, 1906 from Africa (Heteroptera: Rhyparochromidae). Entomologische Zeitschrift Stuttgart 122 (3): 117-118. 2. KONDOROSY E., VARGA K., ZSALAKOVICS L. (2012): A new species of Porta Distant 1903 (Hemiptera: Heteroptera: Rhyparochromidae: Ozophorini). Zootaxa 3413:64-68, IF= 0,927 3. VARGA K., KONDOROSY E. (2013): Two new species of Vertomannus Distant, 1903 (Heteroptera, Rhyparochromidae, Ozophorini), with proposal of a new subgenus. ZooKeys 319: 325 331. IF= 0,933 4. VARGA K., KONDOROSY E. (2014): Revision of the genus Tachytatus (Heteroptera: Lygaoidea: Rhyparochromidae). Acta Entomologica Musei Nationalis Pragae 2014. 04. 30. 54 (1): 99-108 IF= 0,659 20