NEW DATA ON THE DISTRIBUTION OF LIPARA MEIGEN, 1830 (DIPTERA: CHLOROPIDAE) AND ITS GALL-INQUILINE CHLOROPIDS IN THE IBERIAN PENINSULA

Víctor Moreno-González¹

¹Departamento de Biodiversidad y Gestión Ambiental – Área de Zoología, Universidad de León, León, Spain.

ORCID iD: http://orcid.org/0000-0003-0094-1559 E-mail: vmoreg00@estudiantes.unileon.es

IntroductionTOP

Grass-flies (Diptera: Chloropidae) are a widely distributed Diptera family occupying a vast range of habitats, although most species prefer open habitats such as grasslands and wetlands (Nartshuk & Andersson, 2013; Nartshuk, 2014) and most of them live on Poaceae and Cyperaceae (Nartshuk, 2014). There are many studies about this group in Europe, some of them focused on the Mediterranean region (Collin, 1946; De Bruyn, 1989; Nartshuk, 2004, 2011, 2012, 2013; Nartshuk & Andersson, 2013), although the knowledge of the chloropid fauna of the Iberian Peninsula remains incomplete (De Bruyn, 1999; De Bruyn & Báez, 2002; Nartshuk, 2004; Nartshuk et al., 2013; Ebejer & Andrade, 2015).

Among Chloropidae genera, Lipara Meigen, 1830 has attracted the attention of entomologists for its ability to induce cigar-like apical galls on Phragmites australis (Cav.) Trin. ex Steud., 1841 (Poaceae) (Chvála et al., 1974). There are four recognized species in Europe: L. lucens Meigen, 1830, L. pullitarsis Doskočil & Chvála, 1971, L. rufitarsis Loew, 1858 and L. similis Schiner, 1854. Their biology, taxonomy, ecology and distribution has been well studied in Europe (Mook, 1967; Chvála et al., 1974; De Bruyn, 1987; Grochowska, 2006, 2007, 2013; Nartshuk, 2013), although, up to now, there are few records in the Iberian Peninsula and the Balearic Islands. Thus, Nartshuk (2004) recorded for the first time the genus Lipara (L. similis) in the Province of Castellón (Spain). Later, Ebejer (2006) cited L. lucens, L. rufitarsis and L. similis in Mallorca (Balearic Islands, Spain) and finally, Ebejer & Andrade (2015) recorded L. lucens from the district of Aveiro (Portugal). Thereby, the knowledge of Lipara species distribution and biology in the Iberian Peninsula remains inadequate.

Its life cycle is well understood (Chvála et al., 1974), as well as the development of the gall (Vandevyvere & De Bruyn, 1998). All Lipara species are univoltine and lay the eggs on P. australis leaves. After hatching, the phytophagous first instar larvae climbs to the stem apex and installs itself in the upper rolled leaves of the stem. The larva feeds on the enrolled leaves, starting the gall induction. Thereby, the newly formed internodes are shortened and thickened (Figs. 2C-D). In the case of L. lucens and L. pullitarsis, once the gall is completely developed, the third-instar larvae gnaws through the shoot apical meristem and feeds on the hypertrophied parenchyma. On the other hand, L. rufitarsis and L. similis, remain in the upper rolled and hardened leaves and feed on the panicle. Finally, the larva goes into diapause inside the gall until next spring, when it pupariates and later the adult emerges.

The galls of Lipara, especially those of L. lucens, also serve as microhabitats and important refuges for other chloropids and other insects such as Hymenoptera, Coleoptera or Lepidoptera (De Bruyn, 1985; Nartshuk & Andersson, 2013; Heneberg et al., 2014; Bogusch et al., 2015, 2016; Astapenková et al., 2017).

Materials and MethodsTOP

As galls are the extended phenotype of the cecidogenic organism (Stone & Schönrogge, 2003), it is enough to sample galls induced by Lipara in P. australis in order to identify the species. In this way, it is also possible to find the associated chloropids living as inquilines in those galls. Between January and October of 2017, one-year-old galls were sampled in several localities throughout Spain (Table 1). They were kept individually in Petri dishes at room temperature until adult fly emergence. The galls were identified using the key of Chvála et al. (1974), and the chloropids inhabiting them were identified using keys of Grochowska (2007) and Nartshuk & Andersson (2013).

Additionally, the photography collection of the “Banco Taxonómico y Faunístico Digital de los Invertebrados Ibéricos” (BTFDII) (Biodiversidad Virtual, 2017) were reviewed in order to look for Lipara records from other Spanish localities (see Table 1).

New data of Lipara and other associated chloropids were displayed on a blank map of the Iberian Peninsula and the Balearic Islands (Instituto Geográfico Nacional, 2017) using ArcGis 10.5 (ESRI, 2016).

ResultsTOP

The recorded species are listed, indicating the source of the individuals or galls examined (see Table 1 for localities). In the case that Lipara spp. individuals emerged from the collected galls, this is indicated in square brackets, preceded by the total number of galls collected. If the collector was different from the author, this is indicated.

GALL-FORMING CHLOROPIDS

Lipara lucens Meigen, 1830 (Figs. 1A, 2A, 2C)

MATERIAL EXAMINED: 1 gall: [21], 23-VI-2007, David Molina, leg. (BTFDII: image 12288); 1♂, 1♀: [2], 12-V-2009, Jordi Clavell, leg. (BTFDII: image 76825); 1 adult: [6], 17-IV-2010, Arturo López Gallego, leg. (BTFDII: image 220119); 1 gall: [19], 17-VII-2010, David Molina, leg. (BTFDII: image 142504); 1 adult: [9], 5-V-2012, Matilde Martínez, leg. (BTFDII: image 335977); 1 adult: [8], 7-V-2012, Juan Manuel Casanova, leg. (BTFDII: image 337392); 1 adult: [12], 2-V-2014, Ferran Turmo, leg. (BTFDII: image 573233); 1 adult: [22], 6-V-2014, Constantino Escuer, leg. (BTFDII: images 574353, 574354 and 574355); 1 adult: [7], 26-IV-2015, Nacho Cabellos, leg. (BTFDII: image 699602); 4 galls: [16], 8-I-2017; 13 galls (1♂, 4♀♀): [14], 11-III-2017; 2 galls (1♂): [17], 11-IV-2017, Moreno-González & Cuesta-Segura, leg.; 3 galls (1♂): [11], 17-IV-2017; 3 galls (2♀♀): [5], 8-V-2017, Cuesta-Segura, leg.; 8 galls: [4], 11-VI-2017, Cuesta-Segura, leg.; 2 galls: [13], 19-VIII-2017, Oteo-Mijancos, leg.; 3 galls [1], 7-IX-2017; 1 gall [19], 22-X-2017.

The galls of this species were robust and cigar like, with 8 to 14 shortened internodes and showing a hairy layer in its upper zone (Fig. 2C). The larvae or pupae were found living inside the internodes, below the growing point. The adults (Fig. 2A) were about 6 to 8.5 mm.

DISTRIBUTION: widely distributed in Europe and in the Mediterranean region. Previously reported in the ibero-balearic region from Mallorca island (Spain) (Ebejer, 2006) and the district of Aveiro (Portugal) (Ebejer & Andrade, 2015).

BIOLOGY: The adults emerged from galls from April to early June. The photographs of BTFDII were taken from mid April to mid May.

Lipara similis Schiner, 1854 (Figs. 1B, 2B, 2D)

MATERIAL EXAMINED: 1 adult: [2], 22-V-2016, Jordi Clavell, leg. (BTFDII: image 800994); 4 galls: [14], 11-III-2017; 2 galls (1♂, 1♀): [17], 11-IV-2017, Moreno-González & Cuesta-Segura, leg.; 2 galls (1♂, 1♀) [20], 14-IV-2017; 3 galls: [11], 17-IV-2017; 2 galls (1♀): [14], 24-IV-2017; 1 gall (1♂) [15], 26-IV-2017; 1 gall: [10], 28-IV-2017, Oteo Mijancos, leg. 1 gall: [5], 8-V-2017, Cuesta-Segura, leg.; 1 gall: [4], 11-VI-2017, Cuesta-Segura, leg.; 2 galls [1], 7-IX-2017; 1 gall [19], 22-X-2017; 4 galls [18], 17-X-2017.

The galls of this species were thin and cigar like. They had 3 shortened internodes (4 in some cases), and the upper ones were shorter than the basal. They lacked a hairy layer on the internodes (Fig. 2D). The larvae or the pupae were found living between the enrolled and hardened upper leaves, above the growing point. The adults (Fig. 2B) were about 4 to 6 mm long

DISTRIBUTION: widely distributed species in Europe and in the Mediterranean region. Previously reported in the ibero-balearic region from the province of Castellón (Nartshuk, 2004) and Mallorca Island (Ebejer, 2006) (Spain).

BIOLOGY: The adults emerged from galls from late April to early May. The photograph of BTFDII was taken in mid May.

INQUILINE CHLOROPIDS

Calamoncosis minima (Strobl, 1893) (Fig. 1C)

MATERIAL EXAMINED: 3♂♂, 2♀♀: [6], 8-V-2017, Cuesta-Segura, leg.

All individuals live and pupate on the rolled upper leaves of the Lipara lucens galls. The adults were about 3 mm long.

DISTRIBUTION: widely distributed Palearctic species. Previously reported in the ibero-balearic region from Mallorca Island (Spain) (Ebejer, 2006) and the districts of Aveiro, Braga, Leiria, Lisboa and Porto (Portugal) (Ebejer & Andrade, 2015).

BIOLOGY: Living in the rolled upper leaves of Lipara lucens galls, feeding on the inner part of the leave. The adults emerged during mid June.

Cryptonevra flavitarsis (Meigen, 1830) (Fig. 1D)

MATERIAL EXAMINED: 12♂♂, 6♀♀: [15], 11-III-2017; 1♀: [19], 11-IV-2017, Moreno-González & Cuesta-Segura, leg.; 2♂♂, 1♀: [12], 17-IV-2017; 2♀♀: [5], 8-V-2017, Cuesta-Segura, leg.; 2♀♀: [4], 6-VI-2017, Cuesta-Segura.

All individuals live and pupate in the rolled upper leaves of the Lipara lucens galls. The adults were 2 to 2.5 mm long.

DISTRIBUTION: widely distributed Palearctic species. Previously reported in the ibero-balearic region from Mallorca Island (Spain) (Ebejer, 2006) and the districts of Aveiro, Braga, Coimbra, Leiria, Lisboa and Porto (Portugal) (Ebejer & Andrade, 2015).

BIOLOGY: Lives in the rolled upper leaves of Lipara lucens galls, feeding on the inner part of the leaves. The adults emerged from early April to early June.

DiscussionTOP

Chloropids are poorly studied in many areas (De Bruyn, 1999) and thereby, their knowledge is still poor. In this work, the knowledge on the distribution of Lipara and other gall-inquiline chloropids is extended. Thus, L. lucens, Cr. flavitarsis and C. minima are recorded for the first time from the Spanish mainland. They seem to be widespread in the ibero-balearic region, since they have been found from Portugal (Ebejer & Andrade, 2015) to the Balearic Islands (Ebejer, 2006) and in many provinces of Spain (Nartshuk, 2004). Furthermore, most of the Iberian Peninsula has a Mediterranean bioclimate (Rivas-Martínez et al., 2004) and freshwater habitats are characterized by seasonal flood and dry periods (Gasith & Resh, 1999). These features are suitable for Lipara species, since they prefer Phragmites growing in temporary flooded sites (Mook, 1967; Chvála et al., 1974; De Bruyn, 1987).

Many of the inquiline chloropids that can inhabit Lipara galls (Nartshuk & Andersson, 2013) have already been documented in the Iberian Peninsula, although they have not always been recorded inhabiting galls: Calamoncosis minima, C. duiensis, Cryptonevra flavitarsis, Cr. nigritarsis, Elachiptera cornuta, Eribolus hungaricus and Incertella zuercheri (De Bruyn & Báez, 2002; Ebejer, 2006; Ebejer & Andrade, 2015). However, in this study, only two of them (C. minima and Cr. flavitarisis) have been recorded associated with Lipara lucens galls. Thus, Cr. flavitarsis seems to be a common inquiline of L. lucens galls in the study area, living in the rolled leaves of the upper part of the gall (Nartshuk & Andersson 2013). On the other hand, based on the results, C. minima is more difficult to find living in Lipara galls.

It can be pointed out that the information available on the Internet turned out to be a useful source in the taxonomic (Zeegers & Álvarez Fidalgo, 2016), biogeographic (Pérez Hidalgo et al., 2009; García-Barros et al., 2011) and ethological studies (Olivero & Robillar, 2017). Nevertheless, such information should be up-to-date, reliable and comprehensive (Carling & Harrison, 1996). In this study, the records of BTFDII were useful to refine the distribution of Lipara spp. in the Iberian Peninsula. Nevertheless, further studies are necessary in order to improve the knowledge of the biology, distribution and associated fauna of Lipara spp.

AcknowledgementsTOP

The author wish to acknowledge Amonio David Cuesta-Segura, Fernando Ortega-Alcalde and Juan Carlos Oteo-Mijancos for their valuable records of the chloropids. Also to Antonio Encina-García for the grammatical review of the manuscript. Finally, to Biodiversidad Virtual team, especially to Piluca Álvarez, who allowed me to use their data base, and the persons who altruistically have photographed galls or adults of Lipara.

ReferencesTOP