The key to the Ephemeroptera (Insecta) larvae in running waters of the Eastern Black Sea Basin...

Review of Hydrobiology RESEARCH ARTICLEwww.reviewofhydrobiology.com6,1: 31-55 (2013)ISSN 1308-4119

31

The key to the Ephemeroptera (Insecta) larvae in running waters of the Eastern Black Sea Basin (Turkey)

with the new records

GENCER TÜRKMEN1* AND NİLGÜN KAZANCI1

1Hacettepe University, Science Faculty, Biology Department, Hydrobiology Section, Ankara, Turkey [*Corresponding Author: Gencer Türkmen, [email protected]]

ABSTRACT

1. In this study, a key was provided for the identification of Ephemeroptera larvae of the Eastern Black Sea Region of Turkey.

2. Total 12252 Ephemeroptera individuals were sampled. There were 30 species, belonging 7 families and 11 genera, were found. Eight of them were the new records for Turkey.

3. The Ephemeroptera fauna of Turkey consists of 14 families, 34 genera, 146 species and 5 sub-species now.

4. Furthermore, the importance of Ephemeroptera were emphasized in the applications of the Water Framework Directive in Turkey.

KEY WORDS: Eastern Black Sea Region, Ephemeroptera, identification key, Turkey, Water Framework Directive.

Review of Hydrobiology RESEARCH ARTICLEwww.reviewofhydrobiology.com6,1: 31-55 (2013)ISSN 1308-4119

32

Doğu Karadeniz Havzası’ndaki (Türkiye) akarsularda bulunan Ephemeroptera (Insecta) larvalarının

teşhis anahtarı ve yeni kayıtlar

GENCER TÜRKMEN1* VE NİLGÜN KAZANCI1

1Hacettepe Üniversitesi, Fen Fakültesi, Biyoloji Bölümü, Hidrobiyoloji Anabilim Dalı, Ankara, Türkiye[*İletişim: Gencer Türkmen, [email protected]]

ÖZ

1. Bu çalışmada Türkiye’nin Doğu Karadeniz Bölgesi’nin Ephemeroptera larvalarına ait teşhis anahtarı verilmiştir.

2. Toplam 12252 Ephemeroptera bireyi örneklenmiştir. Yedi familya ve 11 cinse ait 30 Ephemeroptera türü belirlenmiştir. Bunlardan sekiz tanesi Türkiye Ephemeroptera faunası için yeni kayıttır.

3. Türkiye Ephemeroptera faunası 14 familya, 34 cins, 146 tür ve 5 alttürden oluşmaktadır.

4. Ayrıca, Türkiye’deki Su Çerçeve Direktifi uygulamalarında Ephemeroptera’nın önemi belirtilmiştir.

ANAHTAR KELİMELER: Doğu Karadeniz Bölgesi, Ephemeroptera, Su Çerçeve Direktifi, teşhis anahtarı, Türkiye.

The key to the Ephemeroptera larvae in running waters of the Eastern Black Sea Basin with the new records

33

INTRODUCTION

Ephemeroptera is the most abundant and widespread insect order in the benthic macroinvertebrate communities in running water ecosystems. Ephemeroptera has also a great importance in the studies of determining habitat and water qualities of running waters. Many indicator taxa are included in Ephemeroptera, and their usage in biomonitoring of streams and rivers very common and effective (Rosenberg and Resh 1993, Kazancı et al. 1997).

Ephemeroptera researches in Turkey started with the study of Ulmer (1919). After this study, there have been many studies concerning about Ephemeroptera in Turkey (Verrier 1955, Demoulin 1963, 1965, Puthz 1972, 1973, 1978, Jacob 1977, Soldan and Landa 1977, Berker 1981, Braasch 1981, 1983, Kazancı 1981, 1984, 1985, 1986a,b, 1987a,b,c, 1990a,b, 1991, 1992, 1998, 2001a,b, 2009, 2011, Sowa et al. 1986, Kazancı and Braasch 1986, 1988, Kazancı and Thomas 1989, Tanatmış 1995, 1997, 2000, 2002, 2004a,b, 2005, 2007, Belfiore et al. 2000, Ertorun and Tanatmış 2004, Narin and Tanatmış 2004, Tanatmış and Ertorun 2006, 2008, Kazancı and Türkmen 2008a,b, 2011, 2012, Kazancı and Girgin 2008, Dalkıran 2009, Tanatmış and Haybach 2010, Özyurt and Tanatmış 2011, Türkmen and Özkan 2011, Türkmen 2008, 2013).

European Union Water Framework Directive (WFD) is an action plan in the field of water policy generated by the European Parliament in 23 October 2000 (Council of European Communities, 2000). According to this directive, member states of European Union guaranteed to improve all water bodies within their own borders to “good ecological status” by the end of 2015. It’s emphasized in WFD that water is not a commercial value, but it’s a vulnerable source which must be protected. The objects of WFD can be summarized briefly as (1) prevent the devastation of aquatic ecosystems, (2) rehabilitate the aquatic ecosystems and (3) protect the water resources in the long term (Wijk et al. 2003).

Turkey is in the process of candidacy, so there are some legislations to be reconciled and performed. One of the studies in the process is about to applications of WFD in Turkey. In this context, there are many studies carried out by the Ministry of Forestry and Water Affairs of Turkey. There are 26 river basins designated in Turkey. This study were performed in the Eastern Black Sea Basin.

The aim of the study is to determine the Ephemeroptera fauna of the Eastern Black Sea Basin and to create an identification key to Ephemeroptera larvae in this Basin. Another aim of the study is to provide conducive knowledge for the WFD studies in Turkey.

GENCER TÜRKMEN AND NİLGÜN KAZANCI

34

MATERIALS AND METHODS

Sampling was carried out from river and streams in Eastern Black Sea Region in

2008, 2009 and 2011. Ephemeroptera larvae were collected from 24 sites by standard pond

net. Samples were preserved in 80% ethyl alcohol (ethanol). Leica MZ75 stereomicroscope

and Olympus CX21FS1 binocular microscope were used for identifications.

This research is a part of PhD Thesis which is “Analysis of macrobenthic

community of reference sites in some running waters in the province of Bolu” (Türkmen

2013).

RESULTS

In this study, 30 species (belonging to 7 families and 11 genera) of Ephemeroptera

were identified. Total number of individuals were 12252. As a result of that, an identification

key to the Ephemeroptera species of the Eastern Black Sea region was prepared.

Among these species, 8 of them were the new records for the Ephemeroptera fauna

of Turkey. These were Epeorus znojkoi, Rhithrogena zelinkai, Rhithrogena germanica,

Rhithrogena puytoraci, Electrogena affinis, Electrogena quadrilineata, Ecdyonurus

macani and Ecdyonurus picteti. Kazancı (2001b) reported 14 families, 31 genera, 118

species and 1 subgenus in the first comprehensive faunal study of Ephemeroptera in

Turkey. After these new records, Ephemeroptera fauna of Turkey consists of 14 families,

34 genera, 146 species and 5 sub-species now.

The Key to the Ephemeroptera species of the Eastern Black Sea Region

1a. Gills single (Figure 2A) ...................................................................................... 2

1b. Gills two or more branches (Figure 27B, 29A) ................................................... 5

2a. Gills on abdominal segment 2 highly visible and operculate; the other gills hidden

under the operculate gills (Figure 27C) ............................................ CAENIDAE

2b. All gills visible .................................................................................................... 3


35

3a. Abdominal segments with 4 lamellate gills………………. .EPHEMERELLIDAE

3b. Abdominal segments with 7 lamellate gills ......................................................... 4

4a. Body dorso-ventrally flattened, leaf-like gills with tuft of filaments (Figure 19A,

20A) ………… .......................................................................HEPTAGENIIDAE

4b. Body fusiform, not flattened, leaf-like gills without tuft of filaments (Figure 2A)

..........................................................................................................BAETIDAE

5a. Gills dorsally held on the abdomen. Mandibles tusk-shaped (Figure 29)

..................................................................................................EPHEMERIDAE

5b. Gills laterally held on the abdomen. Mandibles normal-shaped .......................... 6

6a. Gill branches with numerous fine filaments (Figure 30) ....... POTAMANTHIDAE

6b. Gill branches without numerous fine filaments (Figure 27B)

.......................................................................................... LEPTOPHLEBIIDAE

Family: BAETIDAE Leach, 1815

1a. Spines on the posterior margins of terga triangular with pointed apex (Figure 1B).

Prosteca of right mandible reduced to two thick bristle with feathery margins

(Figure 1A) ............................................................................................Alainites

1b. Spines on the posterior margins of terga triangular with rounded apex or cracked

tooth-like (Figure 5D, 6B) or thick, robust with rounded apex (Figure 2B, 3C,

4C). Prosteca of right mandible not reduced, like left mandible ................. Baetis

Genus: Alainites Walts, McCafferty & Thomas, 1994

Alainites is represented by one species (A. muticus) in Turkey (Kazancı and Türkmen

2012).

A. muticus (Linnaeus, 1758): Prosteca of left mandible normal shaped with 7-8 teeth.

Prosteca of right mandible reduced to two thick bristle with feathery margins (Figure

1A). 8-12 robust bristle on posterior margin of femur with fine bristles (Figure 1C).

Spines on the posterior margins of terga triangular with pointed apex (Figure 1B).


36

0,1 mm

0.5 mm

0,1 mm 0,2 cm

A B C

Figure 1. Alainites muticus, A. Right mandible; B. Tergum 4; C. Leg 1

Genus: Baetis Leach, 1815

1a. Spines on posterior margins of terga thick, robust with rounded apex (Figure 2B, 3C, 4C) ............................................................................................................... 2

1b. Spines on posterior margins of terga thick, small triangular with cracked tooth (Figure 5D, 6B) .................................................................................................. 4

2a. Spines on outer margins of gills with long and thin bristles (Figure 3B, 4B) ...... 32b. Outer margins of gills smooth or serrated without spines (Figure

2A)……………. ............................................................ B. gemellus Eaton, 1885

3a. Behind the thick, robust spines on posterior margins of terga with pointed triangular spines (Figure 3C). Tarsal claws with 12-14 teeth (Figure 3D) ..................................................................................... B. rhodani (Pictet, 1843)

3b. Behind the thick, robust spines on posterior margins of terga without pointed triangular spines (Figure 4C). Tarsal claws with 9-12 teeth. (Figure 4D) ................................. ……………B. milani Godunko, Prokopov & Soldan, 2004

4a. Segment 3 of labial palp elongated to the tip and triangular shaped with blunt apex (Figure 5B) ...................................................... B. lutheri Müller-Liebenau, 1967

4b. Segment 3 of labial palp not elongated with rounded apex (Figure 6A) .. .............................................................................. B. fuscatus (Linnaeus, 1761)

.


37

0,5 mm

0,1 mm

0.5 mm

0,1 mm

A B

Figure 2. Baetis gemellus, A. Gill 4; B. Tergum 4

0.5 mm

0,1 mm

C

0,05 mm

0,5 mm

0,1 mm

0,2 mm

A B

D

Figure 3. Baetis rhodani, A. Maxillar palp; B. Gill 4; C. Tergum 4; D. Tarsal claw.


38

0,05 mm

0.5 mm

0,1 mm

0,2 mm

0,5 mm

0,1 mm

A B

C D

Figure 4. Baetis milani, A. Maxillar palp; B. Gill 4; C. Tergum 4; D. Tarsal claw.

0,05 mm

0.2 mm

0,2 mm

0.5 mm

0.05 mm

A B

C D

Figure 5. Baetis lutheri, A. Maxillar palp; B. Labial palp; C. Tarsal claw; D. Tergum 4.


39

0.2 mm

0.5 mm

0.05 mm

A B

Figure 6. Baetis fuscatus, A. Labial palp; B. Tergum 4.

Family: CAENIDAE Newman, 1853

Caenidae is represented by 2 genera (Caenis and Brachycercus) in Turkey (Kazancı and Türkmen 2012). In this study, only Caenis was found in the area.

Genus: Caenis Stephens, 1836Gill 2 operculate. Single or multiple microtrichia line on the ventral side of the operculate gill (Figure 7C, 8C, 9C). Distinct small process on middle of abdominal tergum 2 (Figure 7A, 8A, 9A).

1a. Regular bristle line present on the anterior middle of the fore femur (Figure 7B). Sternum 9 with “V” shaped notch on the center of its posterior margin (figure 7D). Microtrichias on the ventral side of the second gill long with narrow basal part (Figure 7C) ........................................................... C. luctuosa (Burmeister, 1839)

1b. Irregular bristle line present on the anterior middle of the fore femur (Figure 8B). Sternum 9 with “U” shaped notch on the center of its posterior margin (figure 8D). Microtrichias on the ventral side of the second gill short with thick basal part (Figure 8C) ......................................................................................................... 2

2a. Dorsal projection on abdominal tergum 2 prominently long and rounded apically (Figure 9A) .................................................................. C. martae Belfiore, 1984

2b. Dorsal projection on abdominal tergum 2 short and pointed apically (Figure 8A).. ......................................................................... C. macrura Stephens, 1836


40

0,2 mm 0,2 mm

0,5 mm

0,05 mm

0,2 mm

A B

C D

Figure 7. Caenis luctuosa, A. Abdominal tergum 2; B. Femur 1; C. Operculate gill (Gill 2) and microtrichia; D. Abdominal sternum 9.

0,2 mm

0,2 mm

0,5 mm

0,05 mm

0,2 mm

A B

C D

Figure 8. Caenis macrura, A. Abdominal tergum 2; B. Femur 1; C. Operculate gill (Gill 2) and microtrichia; D. Abdominal sternum 9.


41

0,2 mm0,2 mm

0,5 mm

0,05 mm

0,2 mm

A B

C D

Figure 9. Caenis martae, A. Abdominal tergum 2; B. Femur 1; C. Operculate gill (Gill 2) and microtrichia; D. Abdominal sternum 9.

Family: HEPTAGENIIDAE Needham, 1901

1a. Gill 1 enlarged and connected to the abdomen ventrally .....................................21b. Gill 1 not enlarged and connected to the abdomen laterally ................................3

2a. Two cerci and one terminal filament at the end of the abdomen. Gill fragile and their margins sometimes crenulated ................................................. Rhithrogena

2b. Two cerci but no terminal filament at the end of the abdomen. Gill robust and their margins not crenulated ............................................................................Epeorus

3a. Postero-lateral edge of pronotum elongated .......................................Ecdyonurus3b. Postero-lateral edge of pronotum not elongated .................................Electrogena

Genus: Rhithrogena Eaton, 18811a. Margin of the gill 7 smooth .................................................................................21b. Margin of the gill 7 cranulated (Figure 10D) ... R. zelinkai Sowa & Soldan, 1984

2a. Gill 1 with plica (Figure 10A, 12B, 12B, 14B, 15B) ...........................................32b. Gill 1 without plica (Figure 11B) ....R. beskidensis Alba-Tercedor & Sowa, 1987


42

3a. Plica pointed or with finger-like projection (Figure 12B, 13B) ...........................43b. Plica rounded and without any projection (Figure 14B, 15B) .............................5

4a. Gills 2 and 3 quadrangular with rounded edges (Figure 12C) ............................... .............................................................................. R.semicolorata (Curtis, 1834)

4b. Gills 2 and 3 rectangular with rounded edges (Figure 13C) .................................. .................................................................................... R. germanica Eaton, 1885

5a. Spines on the dorsal surface of hind femur spatular shape (Figure 14D) ............... .................................................................. R. puytoraci Sowa & Degrange, 1987

5b. Spines on the dorsal surface of hind femur rectangular (Figure 15D) ................... ...................................................................................R. iridina (Kolenati, 1859)

0,05 mm

1 mm

0,1 mm

0,5 mm

A B C D

Figure 10. Rhithrogena zelinkai, A. Comb-shaped bristle on maxilla; B. Gill 1 and plica; C. Tarsal claw; D. Gill 7.

A B C

0,05 mm

1 mm

0,1 mm

Figure 11. Rhithrogena beskidensis, A. Comb-shaped bristle on maxilla; B. Gill 1; C. Tarsal claw.


43

A B C D

0,05 mm

1 mm

0,5 mm

0,1 mm

Figure 12. Rhithrogena semicolorata, A. Comb-shaped bristle on maxilla; B. Gill 1 and plica; C. Gill 2; D. Tarsal claw.

0,05 mm 1 mm

0,5 mm

0,1 mm

A B C D

Figure 13. Rhithrogena germanica, A. Comb-shaped bristle on maxilla; B. Gill 1 and plica; C. Gill 2; D. Tarsal claw.

0,05 mm

1 mm

0,1 mm

0,02 mm

A B C D

Figure 14. Rhithrogena puytoraci, A. Comb-shaped bristle on maxilla; B. Gill 1 and plica; C. Tarsal claw; D. Spine on the surface of femur


44

0,05 mm

1 mm

0,1 mm 0,02 mm

A B C D

Figure 15. Rhithrogena iridina, A. Comb-shaped bristle on maxilla; B. Gill 1 and plica; C. Tarsal claw; D. Spine on the surface of femur

Genus: Epeorus Eaton, 18811a. Gill 1 enlarged, kidney-shaped (Figure 17A). Postero-lateral edges of abdominal

sternum not elongated ........................................................................................ 21b. Gill 1 enlarged, but not kidney-shaped (Figure 16A). Postero-lateral edges of

abdominal sternum elongated forming pointed spine (Figure 16B) .....................………………… ........................................................E. zaitzevi Tshernova, 1981

2a. Anterior margin of gills 2-7 with distinct median projection (Figure 19A, 20A) . 32b. Anterior margin of gills 2-7 without median projection ………………………… .

...................................................................................... E. alpicola (Eaton, 1871)

3a. Interior margins of gill 1 touched to each other on ventral side ........................... 43b. Interior margins of gill 1 not touched to each other on ventral side…… ...............

...................................................................................... E.sylvicola (Pictet, 1865)

4a. Gills 2 and 3 with at least 15 filaments (Figure 19A) ........................................... .......................................................................... E. caucasicus (Tshernova, 1938)

4b. Gills 2 and 3 with more than 30 filaments (Figure 20A) ....................................... ................................................................................ E. znojkoi (Tshernova, 1938)


45

0,5 mm2 mm

A B

Figure 16. Epeorus zaitzevi, A. Gill 1; B. Lateral spines on sterna.

0,5 mm

0,2 mm

0,1 mm

A B C

Figure 17. Epeorus alpicola, A. Gill 1; B. Gill 4; C. Tarsal claw.

0,5 mm

0,1 mm

A B

Figure 18. Epeorus sylvicola, A. Gill 1; B. Tarsal claw.


46

0,5 mm

0,1 mm

A B

Figure 19. Epeorus caucasicus, A. Gill 2; B. Tarsal claw.

2 mm

0,1 mm

A B

Figure 20. Epeorus znojkoi, A. Gill 2; B. Tarsal claw.

Genus: Ecdyonurus Eaton, 18681a. Lateral tips of superlingua of hypopharynx with long and fine bristles (Figure 23C,

24C). ..................................................................................................................21b. Lateral tips of superlingua of hypopharynx without long and fine bristles (Figure

21A, 22A) ..........................................................................................................3

2a. Spines on the surface of femur long and rectangular (Figure 21B) .……………… .............................................................E. starmachi Sowa, 1971

2b. Spines on the surface of femur short and rectangular (Figure 22B) ………………… ...................................... …..E. macani Thomas & Sowa, 1970

3a. Postero-lateral edge of the pronotum pointed (Figure 23A). Gill 1 long and slim tongue-shaped with pointed apical part (Figure 23B) .......................................... .................................................................................... E. helveticus Eaton, 1883

3b. Postero-lateral edge of the pronotum bluntly pointed (Figure 24A). Gill 1 long and thick tongue-shaped with blunt apical part (Figure 24B) …………………………………………………...….E. picteti (Meyer-Dür, 1864)


47

0,5 mm0,05 mm

A B

Figure 21. Ecdyonurus starmachi, A. Hypopharynx; B. Spine on the surface of femur.

0,5 mm0,05 mm

A B

Figure 22. Ecdyonurus macani, A. Hypopharynx; B. Spine on the surface of femur.

1 mm

0,5 mm

0,5 mm

A B C

Figure 23. Ecdyonurus helveticus, A. Pronotum; B. Gill 1; C. Hypopharynx.


48

1 mm

A B C

0,5 mm

0,5 mm

Figure 24. Ecdyonurus picteti, A. Pronotum; B. Gill 1; C. Hypopharynx.

Genus: Electrogena Zurwerra & Tomka, 19851a. Setae on inner margin of glossa distinct and small (Figure 25A). Bristles on the

surface of femur rectangular shape (Figure 25B) ................................................. ........................................................................... E. quadrilineata (Landa, 1969)

1b. No setae on inner margin of glossa (Figure 26A). Bristles on the surface of femur thick and pointed (Figure 26B) ..................................... E. affinis (Eaton, 1887)

0,5 mm 0,02 mm

A B

Figure 25. Electrogena quadrilineata, A. Labium; B. Spine on the surface of femur.

0,5 mm0,02 mm

A B

Figure 26. Electrogena affinis, A. Labium; B. Spine on the surface of femur.


49

Family: LEPTOPHLEBIIDAE Banks, 1900

Leptophlebiidae is represented by 6 genera (Choroterpes, Euthraulus, Thraulus, Paraleptophlebia, Habrophlebia and Habroleptoides) in Turkey (Kazancı 2001b, Kazancı and Türkmen 2012). In this study, only Habroleptoides was found in the area.

Genus: Habroleptoides Schoenemund, 1929Abdomen dorso-ventrally flattened. Lateral tips of superlingua of hypopharynx elongated (Figure 27A). Femur broad, tarsal claws large and curved slightly.

Habroleptoides is represented by 4 species (H. modesta, H. caucasica, H. umbratilis and H. kavron) in Turkey (Kazancı and Türkmen 2012). In this study, only H. modesta was found in the area.

H. modesta (Hagen, 1864): Gills with two branches (Figure 27B). Lateral tips of superlingua of hypopharynx elongated (Figure 27A).

0,2 mm0,2 mm

A B

Figure 27. Habroleptoides modesta, A. Hypopharynx; B. Gill 5.

Family: EPHEMERELLIDAE Klapálek, 1909

Ephemerellidae is represented by 5 genera (Ephemerella, Serratella, Quatica, Teloganopsis and Torleya) in Turkey (Kazancı and Türkmen 2012). In this study, only Serratella was found in the area.

Genus: Serratella Edmunds, 1959Abdominal terga with a pair of tubercules (Figure 28C). Thin and long spine ring on the apex of the segments of caudal filaments and no long and dense bristles between segments (Figure 28D).


50

Serratella is represented by 2 species (S. ignita and S. karia) in Turkey (Kazancı and Türkmen 2012). In this study, only S. ignita was found in the area.

S. ignita (Poda, 1761): Apex of the last segment of labial palp rounded (Figure 28A). Abdominal terga with two distinct tubercules (Figure 28C). Outer edge of the posterior-lateral side of the gills elongated (Figure 28B). Thin and long spine ring on the apex of the segments of caudal filaments, no long and dense bristles between segments (Figure 28D).

0,2 mm0,2 mm

0,5 mm

0,1 mm

A B C D

Figure 28. Serratella ignita, A. Labium; B. Gill 5; C. Terga 4-5; D. Cerci.

Family: EPHEMERIDAE Latreille, 1810

Ephemeridae is represented by 1 genus (Ephemera) in the World.

Genus: Ephemera Linnaeus, 1758Ephemera is represented by 5 species (E. danica, E. glaucops, E. lineata, E. vulgata, and E. zettana) in Turkey (Kazancı 2001b, Kazancı and Türkmen, 2012). In this study, only E. danica was found in the area.

E. danica Müller, 1764: Mandibular tusk well developed (Figure 29B). Gill 1 small, other gills two-branched with deep cleft bearing dense fringe (Figure 29A).

2 mm 2 mm

A B

Figure 29. Ephemera danica, A. Gill; B. Mandibular tusk.


51

Family: POTAMANTHIDAE Albarda, 1888

Potamanthidae is represented by 1 genus (Potamanthus) and 1 species (P. luteus) in the World.

P. luteus (Linnaeus, 1767): Gill 1 tube-shaped and two segmented. Gills 2-7 fork-shaped with deep cleft bearing fringes on ventral sides (Figure 30).

1 mm

Figure 30. Potamanthus luteus, Gill 2.

ACKNOWLEDGMENT

We thank to Hacettepe University Scientific Research Projects Coordination Unit for their financial support.

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The key to the Ephemeroptera (Insecta) larvae in running waters of the Eastern Black Sea Basin...

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