MELLIFERA 12-24:17-26 (2012) HARUM 17 RESEARCH ARTICLE

NOTES ON ALGIRUS PÉREZ, 1895 AND ROPHITES QUINQUESPINOSUS SPINOLA, 1808 OF MEDITERRANEAN TURKEY WITH AN UPDATED LIST OF SUBFAMILY (: ) OF TURKEY TÜRKIYE’DEKI ROPHITINAE (HYMENOPTERA: HALICTIDAE) ALTFAMILYASININ GÜNCEL LISTESI ILE TÜRKIYE’NIN AKDENIZ HAVZASINDAKI ROPHITES ALGIRUS PÉREZ, 1895 AND ROPHITES QUINQUESPINOSUS SPINOLA, 1808 ÜZERINE NOTLAR

Fatih DİKMEN* and Ahmet Murat AYTEKİN*

Summary: The study was conducted in the Mediterranean region of southern Turkey. Two Rophitinae (Halictidae: Hymenoptera) species, Rophites algirus Pérez, 1895 and Rophites quinquespinosus Spinola, 1808 were considered. Taxonomical identification keys, distribution maps and flower visits of these spe- cies were given. Detailed microscopic photos and drawings of some important morphological features were also revealed. Besides, the literature on the fauna of the subfamily Rophitinae was reviewed to es- tablish an updated species list of Turkey. As a result of this overview eight species seem possibly endemic for Turkey.

Key Words: Halictidae, Rophitinae, Fauna, Distribution, Turkey

Özet: Çalışma Türkiye’nin güneyindeki Akdeniz Bölgesi’nde gerçekleştirildi. İki Rophitinae (Halictidae: Hymenoptera) türü, Rophites algirus Pérez, 1895 and Rophites quinquespinosus Spinola, 1808 ele alındı. Bu türlere ait taksonomik tanı anahtarları, yayılım haritaları ve bitki ziyaretleri belirtildi. Bazı önemli morfolojik karakterlere ait fotoğraflar ve çizimler de ayrıca gösterildi. Bunların yanında, Türkiye’deki güncel tür listesinin elde edilebilesi için, Rophitinae altfamilyası faunası üzerine yapılmış olan literatür derlendi. Bu genel taslağın bir sonucu olarak, sekiz türün Türkiye için muhtemelen endemik olabilecek- leri görüldü.

Anahtar Kelimeler: Halictidae, Rophitinae, Fauna, Yayılım, Türkiye

*Hacettepe University Faculty of Science, Department of Biology, 06800 Beytepe, Ankara, Turkey Corresponding Author E-mail: [email protected] This study based on part of the PhD thesis of F. Dikmen submitted to Hacettepe University Institute of Science in 22.06.2012. MELLIFERA 18

Introduction ondly the scattered literature data were evaluated to Halictidae (Apiformes: Apoidea: Hymenoptera) is one figure out the updated faunistic list of the subfamily of the largest families of all bees (Pesenko et al. 2000; for Turkey. Michener 2007). It contains four subfamily (Rophi- tinae, Nomiinae, Nomioidinae, Halictinae) according Materials and Methods to Michener (2007) and nearly 3500 species (Pesenko The study was conducted at Mediterranean Region of 2007) in the world. From these, Rophitinae is one the Southern Turkey. Field studies were performed during most interesting one because of their unique morpholo- the spring and summer seasons of 2008 and 2009. Ran- gy and biological features. Rophitinae members can be dom sampling protocol was used and vegetation bound- easily separated from other groups by such brief char- aries were followed in collecting bees. Bee specimens acters; antennal sockets placed on lower half of face were collected via hand nets and aspirators. Mean- and clypeus shorter than labrum (Pesenko et al. 2000). while, the plants that have been visited by bees were Apart from these, they exhibit solitary life and they are also recorded or collected for diagnosis. Captured bee mostly oligolectic unlike the other Halictidae members samples and collected plants were properly prepared (Pesenko et al. 2000). Patiny and Michez (2006) report- for collections. All of these specimens were depos- ed that spp. are the most typical ones that ited in the Department of Biology, Faculty of Science, show narrow plant choice and especially oligoleg on Hacettepe University, Ankara (Turkey). GPS coordi- Convovulus L. spp. (Convolvulaceae). Moreover, Pat- nates were taken by Garmin Etrex H®. Materials were iny et al. (2007) suggested that there should be an evo- examined with stereoscopic microscopes for diagnosis. lutionary tendency for Rophitinae species to specialize Identification of the bee specimens were made accord- on the members of certain plant groups. ing to Warncke (1980), Ebmer and Schwammberger (1986) and Niu et al. (2005). Identification of plant This subfamily contains nearly 200 species in the specimens were made by Demet Töre (Department of world and half of them are distributed in Palaearctic Biology, Faculty of Science, Hacettepe University) and region (Pesenko et al. 2000). Generally in West Pa- The International Plant Names Index (IPNI 2008) were laearctic Region and also locally in Turkey it is repre- followed for the author names of the plant taxa. Taxo- sented by four genera: Lepeletier, Morawit- nomical identification key for two species were pre- zia Friese, Rophites Spinola, and Systropha Illiger pared. Some important morphological features includ- (Michener 2007). Among them, the most diverse ge- ing the dorsal view of genitalia of these species were nus is Dufourea and it has generally Holoarctic dis- also photographed. Ebmer and Schwammberger (1986) tribution. Whereas members of the genera Systropha, was followed for genitalia inspection. Morawitzia and Rophites show more likely restricted distributions (Pesenko et al. 2000; Michener 2007). Ecoregion map (fig.1) was prepared with CFF 2.0 (Car- On the other hand there are many tasks had to be done to Fauna-Flora; Barbier and Rasmont 2000) and modi- for exact evolutionary explanations. Especially there fied with Adobe Photoshop© v7.0 for a better visualiza- are still no sufficient and up to date knowledge on the tion. We followed the explanation of borders of West distributions of Rophitinae groups for Turkey. The Palaearctic Region proposed by Patiny et al (2009). leading studies which also include scrappy data on the Distribution maps (fig. 4) for the Rophites algirus and Rophitinae fauna of Turkey are Ebmer (1987; 1988; R. quinquespinosus was also prepared with CFF 2.0 1993) and Schwammberger (1976). Moreover the in- (Barbier and Rasmont 2000: Carto Fauna-Flora). Spe- formation about the members of the genus Rophites cies lists for regions and subregions were prepared ac- Spinola of Turkey is very scanty. cording to Schwammberger (1976), Ebmer (1987; 1988; 1993), Baker (1996); Pesenko (1998); Pesenko et al. For these reasons, this study aimed to make contri- (2000), Patiny (2003; 2004), Niu et al. (2005), Patiny butions on the Rophitinae fauna of Turkey. Rophites and Michez (2006), Pesenko and Astafurova (2006), algirus Pérez, 1895 and Rophites quinquespinosus Ascher et al. (2009). The species are listed in tables are Spinola, 1808 were considered taxonomically. Sec- in the alphabetical order (tab.1 and tab.3). 19

Results As a result of our literature research we can suppose Species identification key for female that 29 of them (13 from Dufourea; 11 from Rophites; 1. Frons with thick spines medially, with 7 – 8 spines three from Morawitzia; and two from Systropha) are under median ocel and 8 – 10 spines laterally (fig. 2a) recorded from Turkey (tab.1). These numbers also con- ……………………………………… R. algirus Pérez stitute nearly 30% of Palaearctic fauna and also close 1’. Frons with thick spines medially, with 4 – 5 spines with the richness of the fauna of Europe mainland under median ocel and 4 – 5 spines laterally (fig. 2b) (tab.2). Moreover, eight of them are possibly endemic ……………………….. R. quinquespinosus Spinola for Turkey (tab.1). In addition to these data, twelve Ro- phitinae spp. were also listed according to their close Species identification key for male distribution within adjacent boundaries (tab.3). 1. S6 with a slight thin process longitudinally; distal lobe of S8 thin; gonostylus narrower and more cylin- Discussion drical (fig. 2c, 2e, 3a) ………………R. algirus Pérez During our field studies in Mediterranean Region of 1’. S6 with thick and obvious process longitudinally; Turkey only two species belong to Rophites spp. were distal lobe of S8 thick; gonostylus broader and determined. However it was interesting that all speci- more foliate like (fig. 2d, 2f, 3b) ……. R. quin- mens were captured at high elevation (between 1200- quespinosus Spinola 2200 meters). Secondly it is important that Rophites algirus and R. quinquespinosus are captured just only Rophites algirus Pérez, 1895 on Lamiaceae members. This may be counted as a kind Distribution: Turkey, Caucasus (Pesenko et al. 2000); of clue about their oligolectic feeding behavior which Bulgaria, Morocco, France, Iran, Italy, Tunisia, was also mentioned in Pesenko et al. (2000). However Ukraine (Ascher et al. 2009). because of the low sampling size it is difficult to make Inspected Material: 18-VII-2008, 37°16’70”N, inference about the flower preferences and distributions 30°07’27”E, 1963 m, Söbüce Yayla, Antalya, 1♀; 22- of the Rophites species within Mediterranean Turkey. VII-2008, 36°20’53”N, 32°35’22”E, 2225 m, Anamur - Ermenek road Gazipaşa cross, Anamur, Mersin, 1♂; The biogeographical results showed that Turkey is one 07-VI-2009, 36°21’59”N, 33°13’63”E, 1241 m, Gülnar of the important reserves for the members of Mora- - Ermenek road, 5 km to Akova, Mersin, 2♂♂; 23- witzia, Rophites and Dufourea. On the other hand VII-2009, 36°26’84”N, 32°47’30”E, 1752 m, Anamur Systropha members have Palaeatrctic and African - Ermenek road, Gazipaşa cross, Ermenek, Karaman, distribution and they are hardly represented within 1♀ (fig. 4a). Turkey (tab.2). The members of Morawitzia are gener- Visited Flowers: Phlomis armeniaca Willd., P. mono- ally endemic to Anatolian part of Turkey and Caucasia cephala P.H.Davis, P. sieheana, Stachys byzantina C. (Georgia and Armenia) and do not distributed in any koch. (Lamiaceae). other parts of the world. The endemism (nearly 20% of Palaearctic fauna) and the species richness (nearly Rophites quinquespinosus Spinola, 1808 60% of the Palaearctic fauna) of the genus Rophites Distribution: Europe, China, Western Russia, Caucasus, are also high in Turkey (Table.2). These findings gen- Kazakhstan, Kirgizstan, Turkey (Ascher et al. 2009). erally supports that Turkey is one of the most impor- Inspected Material: 23-VII-2009, 36°26’84”N, tant biogeographical zones for bees with considerably 32°47’30”E, 1752 m, Anamur - Ermenek road diversified fauna. The data presented here might ex- Gazipaşa cross, Ermenek, Karaman, 2♀♀ (fig. 4b). hibit a good ground base for bee conservation studies Visited Flowers: Ballota saxatilis Sieber ex C.Presl. in Turkey and also would be helpful in such taxonomi- (Lamiaceae). cal studies focusing on the subfamily Rophitinae.

Biogeographical results Acknowledgements The subfamily Rophitinae is represented by 95 species This study partly supported by Hacettepe University in Palaearctic region (Pesenko and Astafurova 2006). Research Foundation Project No: 0701601016. 8

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Fig. 1: SubregionsFig. 1: Subregions of West Palaearctic of West Region Pal andaearctic Asia. BA: Region Balkans; and CA: Asia. Central BA: Asia; Balkans; CAU: Caucasia; CA: Central EA: Eastern Asia; Asia; ME: Middle East; MED: Mediterranean Basin; NA: Northern Asia; SA: Southern Asia; WP: West Palaearctic Region (includingCAU: BA, CAU, Caucasia; MED, and EA: ME regions). Eastern Asia; ME: Middle East; MED: Mediterranean Basin; NA: Northern Asia; SA: Southern Asia; WP: West Palaearctic Region (including BA, CAU, MED, and ME regions).

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Fig. 2: a-b: Female head and the spines on frons; a: Rophites algirus and b: R. quinquespinosus; c-d: Sterna VI (S6) of male; c: Rophites algirus and d: R. quinquespinosus; Sterna VIII (S8) of male; e: Rophites algirus and f: R. quinquespi- nosus.

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Fig. 2: a-b: Female head and the spines on frons; a: Rophites algirus and b: R. quinquespinosus; c-d: Sterna VI (S6) of male; c: Rophites algirus and d: R. quinquespinosus; MELLIFERA 22 Sterna VIII (S8) of male; e: Rophites algirus and f: R. quinquespinosus.

Fig. 3: Male genitalia drawing and detailed microscopic photograph: a: Rophites algirus and b: R. quinquespinosus. gb: gonobase; gc: gonocoxite; gs; gonostylus; pv: penis valve; vs: volsella; S8: Sterna VIII. Fig. 3: Male genitalia drawing and detailed microscopic photograph: a: Rophites algirus and b: R. quinquespinosus. gb: gonobase; gc: gonocoxite; gs; gonostylus; pv: penis valve; vs: volsella; S8: Sterna VIII.

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Fig. Fig.4: Mediterranean 4: Mediterranean distributions distributions of a: Rophites of a: algirus Rophites and algirusb: R. quinquespinosus. and b: R. quinquespinosus.

Table.1: The list of the Rophitinae Species of Turkey. 1: Ascher et al. (2009); 2: Ebmer (1987); 3: Pesenko (1998); 4: Ebmer (1988); 5: Ebmer (1993); 6: Schwammberger (1976); 7: Pesenko et al. (2000); 8: Baker (1996); Ref: References.

Species Subgenus Ref. Distribution

Dufourea armenia Ebmer, 1987 Cyprirophites 1; 2 Caucasia

Dufourea atrata (Warncke, 1979) Dufourea 1, 3 Endemic - Caucasia

Dufourea caelestis Ebmer, 1987 Dufourea 1; 2 Endemic

Dufourea cypria Mavromoustakis, 1952 Dufourea 1 East Mediterranean

Dufourea graeca Ebmer, 1976 Halictoides 1; 2 Caucasia, Balkan

Dufourea longicornis (Warncke, 1979) Cyprirophites 1 East Mediterranean, Middle East, West Part of

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Table 1: The list of the Rophitinae Species of Turkey. 1: Ascher et al. (2009); 2: Ebmer (1987); 3: Pesenko (1998); 4: Ebmer (1988); 5: Ebmer (1993); 6: Schwammberger (1976); 7: Pesenko et al. (2000); 8: Baker (1996); Ref: References.

Species Subgenus Ref. Distribution

Dufourea armenia Ebmer, 1987 Cyprirophites 1; 2 Caucasia

Dufourea atrata (Warncke, 1979) Dufourea 1, 3 Endemic - Caucasia

Dufourea caelestis Ebmer, 1987 Dufourea 1; 2 Endemic

Dufourea cypria Mavromoustakis, 1952 Dufourea 1 East Mediterranean

Dufourea graeca Ebmer, 1976 Halictoides 1; 2 Caucasia, Balkans

East Mediterranean, Middle East, West Dufourea longicornis (Warncke, 1979) Cyprirophites 1 Part of East Asia

Dufourea pontica (Warncke, 1979) Halictoides 1; 2 Caucasia

Dufourea quadridentata (Warncke, 1979) Dufourea 1 Endemic

Dufourea salviae Ebmer, 2008 Cyprirophites 1 Endemic

Dufourea schmiedeknechtii (Kohl, 1905) Halictoides 1; 2; 3 North Asia; Caucasia; Europe

Dufourea wolfi Ebmer, 1989 Dufourea 1 Balkans

Morawitzia fuscescens Friese, 1902 Morawitzia 1 Endemic

Morawitzia mandibularis Alfken, 1935 Morawitzia 1 Caucasia

Morawitzia panurgoides Friese, 1902 Morawitzia 1 Caucasia

Rophites algirus Pérez, 1895 Rophites 1; 4 West Palaearctic

Rophites anatolicus (Schwammberger, 1975) Rophitoides 1 Endemic

Rophites canus Eversmann, 1852 Rophitoides 1; 4 Trans-Palaearctic

Rophites caucasicus Morawitz, 1875 Rophites 1; 5 Caucasia

Rophites clypealis Schwammberger, 1976 Rophites 1; 6 Pontic

Rophites foveolatus Friese, 1900 Rophites 1; 5 Caucasia, South Europe

Rophites gusenleitneri Schwammberger, 1971 Rophites 1; 5 Endemic

Rophites hartmanni Friese, 1902 Rophites 1; 4 East Europe, East Mediterranean

Rophites heinrichi Schwammberger, 1976 Rophites 1, 6 Endemic

Rophites leclercqi Schwammberger, 1971 Rophites 1, 7 Balkans

Rophites nigripes Friese, 1902 Rophites 1; 5 East Mediterranean

Rophites quinquespinosus Spinola, 1808 Rophites 1 WP, Middle East

Rophites transitorius Ebmer, 1993 Rophites 1; 5 Endemic

Systropha curvicornis (Scopoli, 1770) Systropha 1; 4 West Palaearctic and East Asia

Systropha planidens Giraud, 1861 Systropha 1; 4; 8 Europe and Middle East 25

Table 2: Comparison of the Rophitinae fauna of Palaearctic Region, Europe and Turkey.

Palaearctic Turkey Europe Genus General Distribution (Number of Species) (Number of Species) (Number of Species)

Dufourea Holarctic 54 11 (3 endemic) 17

Rophites Palaearctic 21 13 (4 endemic) 10

Mainly Palaearctic Systropha 17 2 (no endemism) 2 and Africa

Morawitzia Caucasia 3 3 (1 endemic) -

Table 3: The list of the Rophitinae species of adjacent boundaries. 1: Ascher et al. (2009); 2: Ebmer (1987).

Species Reference Distribution

Dufourea alpina Morawitz, 1865 1 Mediterranean (South Europe)

Dufourea bytinskii Ebmer, 1999 1 East Mediterranean

Dufourea dentiventris (Nylander, 1848) 1 Europe, East Asia

Dufourea goeleti Ebmer, 1999 1 East Mediterranean

Dufourea halictula (Nylander, 1852) 1 Europe, Caucasia

Dufourea inermis (Nylander, 1848) 1 Europe, Northeastern and East Asia

Dufourea iris Ebmer, 1987 1; 2 Balkans

Dufourea minuta Lepeletier, 1841 1 Europe, East Asia

Dufourea paradoxa (Morawitz, 1867) 1 West Europe, Central Asia, East Asia

Dufourea similis Friese, 1898 1 North Africa, East Mediterranean

Dufourea trigonellae Ebmer, 1999 1 East Mediterranean

Rophites schoenitzeri Dubitzky, 2005 1 Caucasia MELLIFERA 26

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