Ctenocallis Israelica – First Record in Central Europe, with a Note on the Genus Ctenocallis

Turkish Journal of Zoology Turk J Zool (2014) 38: 35-41 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1301-29

Ctenocallis israelica – first record in Central Europe, with a note on the genus Ctenocallis

1 2, Roman HAŁAJ , Barbara OSIADACZ * 1 The Upper Silesian Nature Society, Katowice, Poland 2 Department of Entomology and Environmental Protection, Poznań University of Life Sciences, Poznań, Poland

Received: 22.01.2013 Accepted: 12.07.2013 Published Online: 01.01.2014 Printed: 15.01.2013

Abstract: This paper presents a new locality for a rare aphid species from Panaphidini (Aphidoidea: Drepanosiphidae, Calaphidinae), Ctenocallis israelica Hille Ris Lambers, 1954, which was recorded for the first time in Hungary and also for the first time in Central Europe. The genus Ctenocallis Klodnitsky, 1924 has been briefly described. The main morphological diagnostic features of apterous viviparous females have been presented, which allow the distinguishing of separate species of the genus. Their current range and the possibility of its broadening have been discussed on the basis of present information on the occurrence of these aphid species. Furthermore, the history of the Ctenocallis genus name has been presented.

Key words: Aphidoidea, Drepanosiphidae, Ctenocallis, Cytisus, Europe, biodiversity, zoogeography

1. Introduction 2. Materials and methods Ctenocallis [= Gentnera Essig, 1952; = Oniscomyzus While browsing through a section of the aphid collection Börner, 1942 (Nieto Nafría et al., 2011b)], a genus from the Museum and Institute of Zoology of the Polish described by Klodnitsky (1924), belongs to Panaphidini Academy of Sciences (which was created by the late Oestlund, 1923 from Calaphidinae Oestlund, 1919, Professor Henryk Szelegiewicz, and which is currently which has been included in Drepanosiphidae Herrich- located in the Department of Zoology at the University Schaeffer, 1857 according to the latest aphid classification of Silesia), we found a microscopic slide (No. 2279: 4 (Heie and Wegierek, 2009). The genus consists of only 3 apterous viviparous females). It contains Drepanosiphidae species: C. dobrovljanskyi Klodnitsky, 1924; C. israelica specimens. They were collected on 21 June 1964 by H. Hille Ris Lambers, 1954; and C. setosa (Kaltenbach, Szelegiewicz near Sas-hegy in Hungary, and they were 1846) (Eastop and Hille Ris Lambers, 1976; Remaudière initially identified as Ctenocallis dobrovljanskyi Klodnitsky, 1924. However, after more detailed identification of these and Remaudière, 1997; Quednau, 2003). These occur in aphid specimens, it turned out that they belong to the Europe and the Middle East (Bodenheimer and Swirski, species C. israelica Hille Ris Lambers, 1954. 1957; Nieto Nafría et al., 2011a), but C. setosa has also been The Sas-hegy is a small nature reserve (it extends for introduced to North America (Maw et al., 2000; Blackman approximately 30 ha with a maximal height of 254 m above and Eastop, 2006). The host plants from these aphids sea level) in the center of Budapest, protected due to its are species of the genus Cytisus Desf. s. lato [sections: relic flora and special fauna. It is on a dolomite hill with Cytisus s. str., Calycotome (Link) DC., Lembotropis steep slopes covered by xerothermic habitats. (Griseb.) Benth., Spartopsis Dumort., Tubocytisus DC. (Cristofolini and Troìa, 2006)] belonging to Fabaceae, and 3. Results less frequently species of the genus Genista L. (Table). All The feature that distinguishes aphids of Ctenocallis from species from the genus Ctenocallis are monoecious and other genera of Panaphidini is the long marginal body holocyclic; they feed on leaves (on the lower parts of the finger-shaped processes (Figure 1), the apices of which have blades, and less frequently on the upper parts) or on green with short setae. Another common feature of the genus shoots (Szelegiewicz, 1968; Stroyan, 1977; Heie, 1982b; is the siphunculi. They resemble trunks in shape and are Halperin et al., 1988; Nieto Nafría and Mier Durante, not too high (not higher than the diameter of the aperture 1998; Blackman and Eastop, 2006). itself), and they are situated at the bottom of the marginal * Correspondence: [email protected] 35 HAŁAJ and OSIADACZ / Turk J Zool

Table. Ctenocallis Klodnitsky, 1924 spp. host plant and distribution.

Aphid species Host plants Distribution/Reference

Hungary: Szelegiewicz (1977), Quednau (2003) Italy: Roberti (1993), Quednau (2003) Cytisus Desf. s. str. spp. France: Leclant (1978) Russia: Blackman and Eastop (2006) Cytisus (sect. Tubocytisus) spp. Belarus: Buga (2001) Cytisus (Tubocytisus) borysthenicus (Grun.) Ukraine: Bozhko (1976) Klásková C. (T.) heuffelii (Wierzb.) Rothm. Serbia: Petrović (1998) Ctenocallis dobrovljanskyi Klodnitsky, 1924 C. (T.) ratisbonensis Schaeff. (=C. biflorus Ukraine: Klodnitsky (1924), Mamontova (1955), L’Hér.) Quednau (2003) Belarus: Buga (2001) Czech Republic: Pintera (1955) Hungary: Pintera and Szalay-Marzsó (1962) C. (sect. Lembotropis) nigricans (L.) Griseb. Italy: Barbagallo and Patti (1994) Romania: Holman and Pintera (1981) Ukraine: Mamontova-Solucha (1963) Genista pilosa L. Austria: Börner (1942, 1949), Börner and Franz (1956)

Spain (León, Malaga): Nieto Nafría (1975), Nieto Nafría Cytisus (sect. Calycotome) spp. et al. (1984), Nieto Nafría and Mier Durante (1998)

France (Antibes): Leclant (1978), Quednau (2003) C. (Calycotome) spinosus (L.) Lam. Italy (SE Italy, Sardinia): Barbagallo and Patti (1993), Ctenocallis israelica Hille Ris Roberti (1993) Lambers, 1954 Israel (Rehovot): Hille Ris Lambers (1954), Bodenheimer and Swirski (1957), Halperin et al. (1988), Quednau Cytisus lanigerus (Desf.) DC. [= Calycotome (2003) villosa (Poir.) Link = Spartium villosum Poir.] Italy (Sicily, Sardinia): Barbagallo and Stroyan (1982), Roberti (1993) Cytisus sp.? Hungary (Budapest): leg. H. Szelegiewicz Denmark: Heie (1982a, 1982b) France: Leclant (1968, 1978), Heie (1982b) Germany: Börner (1952), Heie, (1982b) The Netherlands: Börner (1952) C. (sect. Spartopsis) scoparius (L.) Link Poland: Huculak (1967), Achremowicz (1975), Heie Ctenocallis setosa (1982b), Osiadacz and Hałaj (2009), (2010) (Kaltenbach, 1846) Spain: Nieto Nafría and Mier Durante (1998) Great Britain: Stroyan (1957, 1977), Heie (1982b)

Italy: Barbagallo and Stroyan (1982), Roberti (1993) Greece: Tsitsipis et al. (2007) C. (Cytisus) villosus Pourr. Note: species recorded also from North America: Heie (1982b), Maw et al. (2000), Blackman and Eastop (2006) processes on abdominal tergite VI. Consequently, it may presence and size are the basis on which specific species seem that the whole structure is a siphunculus imitating of Ctenocallis genus can be distinguished. In the case of the rest of the processes. Additionally, on particular C. setosa they are long, similar to the marginal processes. abdominal tergites (especially I–IV and VI) in the spinal However, in the case of C. israelica they are very short, part, processes that have a similar shape may or may not often transparent, and, as a result, poorly visible. In the occur. In the case of apterous viviparous females, their case of C. dobrovljanskyi, the spinal surface of the dorsum

36 HAŁAJ and OSIADACZ / Turk J Zool

C. setosa C. dobrovljansky

s phuncul

0.2 mm marg nal processes A

sp nal processes

0.2 mm C. srael ca

Figure 1. Morphology of abdomen of Ctenocallis spp.: A– C. setosa (drawing from Nieto Nafría and Mier Durante, 1998, modified), C. dobrovljanskyi (drawing from Quednau, 2003, modified); B– C. israelica (original photograph). does not have such processes. Quednau (2003) found that He classified the genus to the Callipterea tribe in the aptera spinal body, setae are sometimes placed on [currently Panaphidini (Quednau, 1999)]. In addition, he flat elevations that are hardly raised above the surface. left a short note on the genus, in which he stated, among Ctenocallis Klodnitsky, 1924 other things, that “it can be distinguished from other Ctenocallis: Grossheim 1920 (manuscript name): genera by specific processes on its head and setae situated Klodnitsky 1924: 61. on (and directed to) the bottom of its body on the sides Type species: Ctenocallis dobrovljanskyi, by original of sections”. designation (Nieto Nafría et al., 2011b, pp. 182–183). Unfortunately, Grossheim’s paper has never been Etymology: Cortés Gabaudan et al. (2011), p. 431. published (it remained in manuscript form), and after the Note: as Klodnitsky (1924) describes: war period it was probably lost. Thus, the first research “Ctenocallis genus has been established by N. scientist who used the “Ctenocallis” name in published Grossheim who in 1920 discovered one species from the materials was II Klodnitsky in 1924, and he should be genus on the leaves of Spirea sp. in the area of Kiev and considered as the author of the name according to the named it C. spirea”. International Code of Zoological Nomenclature.

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Key to the European Ctenocallis spp. based on the of Macaronesia through Europe (except Scandinavia) to apterous morph: Southwest Asia, with the most frequent occurrence around 1. Spinal processes on abdominal tergites absent; the Mediterranean Sea (Cristofolini and Troìa, 2006). A if present, they are shaped like tiny projections of a more or less similar range (southwestern Palearctic) is height equal at the most to ½–¾ their diameter at the also seen for the genus Ctenocallis. However, for particular base...... C. dobrovljanskyi Klodnitsky (Figure 1A) species, it is not a continuous but rather an interrupted –. Spinal processes on abdominal tergites always disjunct type of aphid species distribution (restricted present ...... 2. to host-plant distribution, climate and microclimate 2. The length of the spinal processes on abdominal conditions, and K-survival population strategy). tergites is nearly equal to marginal processes on those tergi According to the present state of knowledge, Ctenocallis tes...... C. setosa (Kaltenbach) (Figure 1A) species are not connected with specific plant species or –. The length of the spinal processes on abdominal even sections of the genus Cytisus (Table). Therefore, they tergites (especially I–IV) never exceeds half the length of may be considered as narrow oligophagous rather than marginal processes on those tergites and is never smaller typical monophagous species. It is possible that one of the than their diameter at the base ...... reasons for such disjunction is habitat, and the specific ...... C. israelica Hille Ris Lambers (Figure 1B) microclimate that is connected with it and that is preferred by particular Ctenocallis species and not just the availability 4. Discussion of host plants. C. israelica has so far been spotted in Israel Aphids of the genus Ctenocallis feed mainly on plants (where it was described for the first time), southern Italy currently classified in the genusCytisus , in the broad (including Sicily and Sardinia), southern France, and sense (Holman, 2009). The genus consists of about 60 southern Spain (Malaga). Its sites near León (Spain) and species which, according to the latest research (including near Budapest (Hungary) seem to be beyond the compact genetics), are grouped into 13 sections (Cristofolini and range of plants from Cytisus (section Calycotome), Troìa, 2006). Particular sections of the genus Cytisus create on which it has so far been observed (Figure 2). C. relatively compact ranges within their whole (i.e. generic) dobrovljanskyi, connected to plant species from the section area of occurrence. This includes the area from the islands Cytisus (and from sections Lembotropis and Tubocytisus),

Figure 2. Localities of Ctenocallis israelica: on sections Cytisus (1) and Calycotome (2).

38 HAŁAJ and OSIADACZ / Turk J Zool has also been spotted in the south of Europe (Italy, Serbia); C. dobrovljanskyi and C. setosa in the Mediterranean Sea however, its center of occurrence is in Central Europe (the basin area. Czech Republic, Romania, Hungary) and East Europe However, regardless of which element will be ascribed (Ukraine) (Figure 3). In southern Europe (Italy, Greece), to a particular species, it is beyond doubt that all of them a third species of the genus Ctenocallis (C. setosa) occurs are relatively rare on a global scale. The reasons for this on plants of the sections Cytisus and Spartopsis. In the may vary. Apart from such prosaic ones as abandonment case of this species, the center of distribution is in West of typical faunistic research, a more important reason, and (Great Britain, Denmark, Germany, and the Netherlands) possibly the main reason, could be the constant decrease in and Central Europe (Poland). Taking into account the the number of natural sites of host plants, especially steppe above information, it may be claimed that there are 3 or xerothermic grass (All.: Festucetalia valesiaceae) and zoogeographic elements, Mediterranean (C. israelica), thermophilic undergrowth and forests (All.: Quercetalia Pannonian (C. dobrovljanskyi), and Atlantic (Atlantic– pubescenti-petraeae). In spite of this, it seems possible to Central European), in the case of C. setosa. However, since find another site for aphids from the genus Ctenocallis on all species of the genus Ctenocallis have been observed on the borders of ranges. It is probable that such a border for plants of the section Cytisus s. str., and mainly on C. villosus geographic vicariants C. dobrovljanskyi and C. setosa (as (a species that occurs in natural sites only on the periphery the present results of research seem to indicate) may be of the Mediterranean Sea), one may draw the conclusion located in Poland and in the Czech Republic. This is all the that all of them have a Mediterranean origin. The reverse more so probable since host species for C. dobrovljanskyi is also possible, however: since C. villosus turned out from sections Tubocytisus and Lembotropis occur in to be a very attractive plant as far as food is taken into Poland, and host species for C. setosa from section account, perhaps it has become a secondary host plant for Spartopsis also occur in the Czech Republic.

123

Figure 3. Range of Ctenocallis spp.: 1– C. israelica; 2– C. dobrovljanskyi; 3– C. setosa.

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