First report of Lioponera longitarsus Mayr, 1879 (: Formicidae) in Algeria: an exotic or a rare native species from North Africa?

G. Barech1*, M. Khaldi1 & X. Espadaler2 1Département des Sciences Agronomiques, Faculté des Sciences, Université Mohamed Boudiaf de M’sila 28000, Algeria 2Ecology Unit and CREAF, Autonomous University of Barcelona, 08193 Bellaterra, Spain

Myrmecological investigations were conducted in an olive grove agro-ecosystem. Among the taxa we report the presence of the cryptic ant species Lioponera longitarsus, subfamily , for the first time in Algeria. Standard morphological measurements are presented for worker and queen. The discovery of this for the fourth time in North Africa in different habitats within a semi-arid climate suggests that the populations of Lioponera may be native but it is not possible to exclude them having been transported by humans. Key words: Dorylinae, Lioponera longitarsus, new record, North Africa, semi-arid.

INTRODUCTION

In terms of their numerical abundance, size and (2016) placed Cerapachys and Lioponera within the species richness, are a prominent taxonomic subfamily Dorylinae. group in many terrestrial ecosystems (Majer 1983). The ant genus Lioponera in North Africa was The ant community is an important contributor recorded in three countries: with Lioponera to the of many habitats and can also noctambula from Tunisia (Santschi 1910); Lioponera profoundly influence distribution and abundance cooperi (Donisthorpe, 1939) renamed as Cerapachys of other invertebrates (Majer 1976). aegyptiacus by Brown (1975), Lioponera alfierii The myrmecofauna of Algeria is poorly known. Donisthorpe, 1939, and Lioponera collingwoodi (as In particular, there is scant knowledge of exotic or Cerapachys collingwoodi Sharaf, 2007, in Fadl et al. tramp species with only seven species reported in 2007) from Egypt; and a Lioponera sp. as Cerapachys old references. These are Monomorium destructor group longitarsus by Guillem et al. (2012), from (Jerdon, 1851), Monomorium pharaonis (Linnaeus, Morocco. Taylor & Sharaf (2015) suggested that 1758), Linepithema humile (Mayr, 1868), Paratrechina the males recorded as Cerapachys collingwoodi and longicornis (Latreille, 1802), Pheidole megacephala Cerapachys noctambulus may be synonymous with (Fabricius, 1793), Tetramorium bicarinatum (Nylander, L. longitarsus. 1846) and Tetramoriumsimillimum (Fr.Smith, 1851). In North Africa, only a few, mostly male, speci- An eighth exotic species, Tetramorium lanuginosum mens were found, which characterises members Mayr,1870, was recorded in Algeria by Barech et al. of the genus as cryptic and rare in the region. (2011) in an irrigated green within the installations According to Gaston (1994) rare species are regarded of the Institut National Agronomique at Algiers. as those having low abundance and/or small Linepithema humile was rediscovered by Barech ranges. Likewise Flather & Sieg (2007) defined that et al. (2015) at Melbou (Bejaïa). species are considered rare if their area of occu- Here we report a further species, Lioponera pancy or their numbers are small compared to the longitarsus Mayr, 1879, for the first time in Algeria. other species that are taxonomically or ecologi- Brown (1975) considered Lioponera as subgenus cally comparable. of the genus Cerapachys but Brady et al. (2014) In the classification of ant communities done by suggested that Cerapachys (Lioponera) is a group Andersen (1995, 1997), the ant genus Cerapachys molecularly distinct enough to deserve reversion (Lioponera) appears within both the functional to Mayr’s original genus status under the name group of specialist predator and cryptic species. Lioponera. This was supported by Borowiec (2016) Here we provide the first report and standard and is accepted by us. In a further change, Borowiec morphological measurements of this rare ant in *Author for correspondence. E-mail: [email protected] Algeria, and we briefly discuss if Lioponera longi-

ISSN 1021-3589 [Print]; 2224-8854 [Online] African Entomology 25(2): 428–434 (2017) DOI: http://dx.doi.org/10.4001/003.025.0428 ©Entomological Society of Southern Africa Barech et al.: First report of Lioponera longitarsus (Formicidae) in Algeria 429

Fig. 1. A, Geographical location for Nouara (M’Sila, NE Algeria) (image Google Earth); B, perspective of the olive grove (image Google Earth); C, some constituent olive trees. tarsus is to be considered a native or exotic ant in comparison with www.antweb.org resources. The North Africa. worker is in the entomological collection of G.B. (University of M’Sila, Algeria). The queen is in the MATERIAL AND METHODS personal collection of X.E. The study site was a plantation of olive trees We conducted a pitfall trap collecting programme (Fig. 1) located at Nouara (M’sila, NE Algeria; (from 11–14 April 2013; leg. G. Barech) in an olive 35°43’22”N 4°33’34”E at 490 m altitude. The local grove (Nouara, M’sila) in Algeria (Fig. 1). Lioponera climate is classified as lower arid with a cold winter. longitarsus specimens were identified using Precipitation is variable, with a mean of 207.5 mm Brown (1975), Bharti & Akbar (2013), and visual and ranging between 105 and 348 mm/year. Annual 430 African Entomology Vol. 25, No. 2, 2017 mean temperatures are 19.43 °C (ranging between margins. Bicoloured, with the head and meso- 8.73 °C to 31.63 °C). The dry period can last 11 soma reddish brown and gaster blackish months. Worker biometry. HW 0.63; HL 0.72; SL 0.40; PW The 60-year-old olive grove covered an area of 0.43; WL 0.91; PetW 0.44; IIIAW 0.53; IIIAL 0.43; 6 ha and consisted of 500 olive trees (Olea europaea IVAW 0.64; IVAL 0.56; Femur III 0.51; Tibia III 0.41; var. Chemlal). The olive grove complied with all Basitarsus III 0.39. TL 3.3. organic agriculture standards, i.e. no pesticides, Ergatoid queen biometry. HW 0.72; HL 0.76; SL fungicides or herbicides were applied. Trees were 0.44; PW 0.51; WL 1.08; PetW 0.53; IIIAW 0.67; regularly watered during dry periods by furrow IIIAL 0.52; IVAW 0.81; IVAL 0.65; Femur III 0.56; irrigation (surface irrigation). Tibia III 0.47; Basitarsus III 0.44. Spurs of middle In association with olive trees diverse adventive and hind tibia (Bolton 2003, p. 274): 1p, 1p. Both plants (17 species) were recorded, for example: legs have a single pectinated spur. TL 3.7. The Asteraceae (Dittrichia viscosa (L.) Greuter, Launaea ergatoid queen morphology fits exactly the speci- nudicaulis (L.) Hook. f., Pallenis spinosa (L.) Cass., men shown at ANTWEB1008626. This poorly Echinops spinosus L., Phagnalon saxatile (L.) Cass., differentiated caste was already noted in the origi- Sonchus sp.), Poaceae (Oryzopsis miliacea (L.) Asch. nal description as Lioponera longitarsus Mayr, 1879, et Schweinf., Cynodon dactylon (L.) Pers. and and subsequently by Bingham (1903) and Brown Apiaceae (Eryngium campestre L.). The vegetation (1975). Its bigger size and presence of ocelli sepa- cover was estimated at 69 %. The most dominant rates it from the worker. Winged queens, in addi- species was Oryzopsis miliacea. tion to ergatoid queens, are also indicated for this Measurements (mm) were taken using a Nikon species (Bharti & Akbar 2013), as with several other SMZ-U stereomicroscope at ×75 magnification formerly Cerapachys species, now in Cerapachys with an ocular micrometer. HW: Head width (C. sulcinodis Emery), Parasyscia (P. seema Bharti & across eyes; HL: maximum head length; SL: scape Akbar) or Ooceraea (O. biroi Forel) (Borowiec 2016). length, excluding neck and basal condyle; PW: The nest was not detected, so we have no data on pronotum width, dorsal view; WL: Weber’s nest population size. Further dedicated searches length; PetW: petiole width, dorsal view; IIIAW: failed to find more specimens (e.g. baits at night third abdominal segment width, dorsal view; composed by dead ants, in deadwood, other pit- IIIAL: third abdominal segment length, dorsal fall traps and hand sampling). view; IVAW: fourth abdominal segment width; But for the widely distributed Tetramorium IVAL: fourth abdominal segment length; Femur sericeiventre Emery, 1877, other species within the III: hind femur length; Tibia III: hind tibia length; same habitat (Table 1) indicate a native, strongly Basitarsus III: hind basitarsus length; TL: total anthropophilous fauna. Monomorium salomonis body length. (Linnaeus, 1758) and Cataglyphis bicolor (Fabricius, Two legs of each specimen were destructively 1793) are the most abundant species in the olive sampled for molecular analysis. Unfortunately grove of Nouara. two attempts at DNA extraction failed. Lioponera longitarsus is a new addition to Algerian myrmecofauna. The species is noted as probably RESULTS AND DISCUSSION twig-nesting (Brown 1975) and possibly as predators of other ants. Some formerly Cerapachys species are One worker (Fig. 2) and one ergatoid queen mainly myrmecophagous and conduct group (Fig. 3) of Lioponera longitarsus were recovered (11 raids on other ant nests (Wilson 1958; General & April 2013) from a single pitfall trap set at an olive Alpert 2012). In nests prey larvae can be stored for grove in Nouara (M’sila, Algeria). several weeks without showing any sign of decay General morphology. Both specimens (worker, (Hölldobler 1982). The nesting behaviour of these ergatoid queen) have 12-segmented antennae. ants may have facilitated their dispersal (Framenau Ocelli absent in the worker; ocelli present in the & Thomas 2008). It is widespread in the Indo- ergatoid queen. Post-ocular carinae absent. Sculp- Australasian region and China (Brown 1975; ture predominantly punctuate on a smooth or Terayama et al. 1988; Shattuck 2000; Guénard & finely sculptured background. Dorsum of pro- Dunn 2012). Populations from the Middle East notum and propodeum rounding into the sides. (Collingwood 1985; Collingwood & Van Harten Petiole with strong overhanging dorsolateral 2001; Sharaf et al. 2013; Vonshack & Ionescu- Barech et al.: First report of Lioponera longitarsus (Formicidae) in Algeria 431

Fig. 2. Worker of Lioponera longitarsus collected in the olive grove of Nouara (Algeria). A, Lateral view; B, dorsal view of propodeum, petiole and postpetiole. Scale bars = 0.5 mm.

Hirsch 2009) and North Africa (Santschi 1910; Table 1. List of ant species collected in the olive grove of Donisthorpe 1939; Guillem et al. 2012) are perhaps Nouara (April 2013). exotic in those regions. Lioponera is part of a well- supported Old World clade where the inter- Subfamilies Species generic relationships are known (Brady et al. 2014). A phylogeny of the relatively few species of Dolichoderinae Tapinoma nigerrimum (Nylander, 1856) Lioponera that have been sequenced suggests that Myrmicinae Monomorium subopacum (Smith, 1858) the genus may have originated in Africa and later Monomorium salomonis (Linnaeus, 1758) spread to the Indomalayan and Australasian Messor barbarus (Linnaeus, 1767) regions (Borowiec 2016). Cardiocondyla mauritanica Forel, 1890 Lioponera longitarsus was sampled at different Tetramorium semilaeve André, 1883 altitudes from 25 m below sea level in Egypt by Tetramorium sericeiventre Emery, 1877 Donisthorpe (1939) to 1000 m in the Himalaya Solenopsis sp. Mountains by Bharti et al. (2013). Formicinae Cataglyphis bicolor (Fabricius, 1793) In North Africa Lioponera longitarsus is recorded Cataglyphis albicans Roger, 1859 in different habitats within a semi-arid climate. Lepisiota frauenfeldi s.l. Mayr, 1855 The first report of this species is mentioned by Camponotus thoracicus (Fabricius, 1804) Donisthorpe (1939) at two localities (Siwa Oasis, as 432 African Entomology Vol. 25, No. 2, 2017

Fig. 3. Ergatoid queen of Lioponera longitarsus collected in the olive grove of Nouara (Algeria). A, Lateral view; B, close up lateral view of mesosoma, petiole and postpetiole; C, head, frontal view. Scale bars = 0.5 mm.

Lioponera cooperi, and Wadi Digla, as Lioponera olive and palm trees. This species is relatively rare alfierii) from Egypt. Both are characterised by a and the worker caste is less abundant (Fadl et al. desertic climate. Siwa Oasis is a fertile basin, sitting 2007). In Morocco the habitat was a dry oued about 25 m below sea level and brimming with surrounded by stony, desert steppe of Hammada Barech et al.: First report of Lioponera longitarsus (Formicidae) in Algeria 433 scoparia (Pomel) Iljin (Amaranthaceae) with scat- biogeographic realm are more likely to have similar tered Ziziphus lotus (L.) (Guillem et al. 2012). climates and habitats which might increase the The other species of Lioponera, L. noctambulus was odds of the success of introduced species. Here, found by Santschi (1910) on the plain of Kairouan we cannot determine with certainty whether the where a steppe climate is present with low rainfall. population of Lioponera longitarsus is native or The unique report of L. collingwoodi was in Port exotic to Algeria. Said which has a hot desert climate but only one male was collected from leaf litter inhabited by ACKNOWLEDGEMENTS many groups of terrestrial invertebrates (Fadl et al. 2007). We acknowledge the useful comments of B. Taylor Collectively the varied L. longitarsus habitats on a previous version of this paper. K. Mimoun suggest the species is native to North Africa because and S.Yaakoubi from the University of M’sila are exotic species tend to establish in regions with thanked for their help in the field. All the authors similar climatic conditions to their region of origin thank R. Vila and S. Schär (Ph.D. student) from the (Williamson 1996). According to Miravete et al. IBE of Barcelona for their contribution in the (2013) regions in similar latitudes or in the same molecular tools.

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Accepted 6 March 2017