Journal of Entomology and Zoology Studies 2017; 5(4): 966-971

E-ISSN: 2320-7078 P-ISSN: 2349-6800 Some (: Collembola) of JEZS 2017; 5(4): 966-971 © 2017 JEZS Northeastern Algeria Received: 03-05-2017 Accepted: 04-06-2017 Brahim Bounab H, Bendjaballah M and Hamra Kroua S Brahim Bounab H Laboratoire de Biosystématique et Ecologie des Arthropodes. Abstract Faculté des Sciences de la Nature The present study is part of the biodiversity component. It is a commented checklist of the species of the et de la Vie, Département de three subfamilies of (, and ), and of Biologie Animale, Université des . Twenty six collembolan species were collected, including 7 Frieseinae, 5 Frères Mentouri Constantine, Neanurinae, 6 Pseudachorutinae, 6 Odontellidae and 2 Brachystomellidae. Frieseinae were particularly Algérie. diverse with seven species of the , two among them were endemics in North-East of Algeria. The Neanurinae were represented by five species, one of them was a new genus and two were Bendjaballah M endemics. The Odontellidae were represented by six species new for Algeria and the whole North Laboratoire de Biosystématique African region one of them was an endemic. Firstly interesting character of this fauna was the importance et Ecologie des Arthropodes. of endemisme: Friesea laouina, Friesea major, Edoughnura rara, zana and Superodontella Faculté des Sciences de la Nature tayaensis. Secondly the collembolan fauna of this present study showed affinities with that of the et de la Vie, Département de Mediterranean area. Biologie Animale, Université des

Frères Mentouri Constantine, Keywords: Collembola, Checklist, Frieseinae, Neanurinae, Pseudachorutinae, Odontellidae, Algérie. Brachystomellidae, Northeastern Algeria

Hamra Kroua S Laboratoire de Biosystématique 1. Introduction et Ecologie des Arthropodes. Knowledge of the biological diversity of the invertebrates of Algeria has made considerable Faculté des Sciences de la Nature progress in recent years. One of the most important groups, Collembola, was the object of et de la Vie, Département de several taxonomic studies with description of several species and genera. The very first are Biologie Animale, Université des realized in the end of the 19th century [1, 2]. At the beginning of the 20th century other works Frères Mentouri Constantine, including those of [3-7]. These works and those of [8, 9] and those of [10] give a new knowledge of Algérie. [11] algerian fauna. In the second half of the last century, we find the works of in the area of Bône (Annaba), [12, 13] and the bibliographic synthesis of [14]. More recently, several taxonomic papers were published, describing or listing additional species [15-23]. The present study is a commented checklist of the species of the three subfamilies of Neanuridae (Frieseinae, Neanurinae and Pseudachorutinae), Odontellidae and of

Brachystomellidae. It is based on a compilation of faunistic data covering all species recorded so far in the literature for northeastern Algeria, and on field works carried out recently in five sites of Northeastern Algeria. The study sites belong to different bioclimatic zones: Edough (Annaba), Azzaba and Ouled Habeba (Skikda), Taya (Guelma), Beni Haroun (Mila).

2. Materiels and Methods

The study sites; Edough (Annaba), Azzaba and Ouled Habeba (Skikda), Taya (Guelma), Beni Haroun (Mila) have been explored from 2009 to 2013 (Fig.1). Several hundred samples were collected in different habitats: forest litter of Quercus faginea, Quercus suber, Pistacia lentiscus and Ceratonia silliqua, moss on soil and moss on rock. The fauna was extracted on simple Berlèze funnels in the laboratory of "Biosystematique et Ecologie des Arthropodes", University Mentouri Constantine.

Edough is a part of the East Coast chain which rises to 1008 m (36 ° 90 'North, 07 ° 65' East). The region belongs to the Mediterranean climate zone. The vegetation is dense and diverse; Correspondence there is the Quercus coccifera, Quercus suber and Quercus faginea ssp. Mirbeckii, (Aouadi, Brahim Bounab H 1989) [24]. Laboratoire de Biosystématique et Ecologie des Arthropodes. Ouled Habeba belongs to the bioclimatic sub-humid mild to sub-humid wet (36 ° 48 'North, Faculté des Sciences de la Nature 06 ° 97' East) at an altitude of 932 m. We took in a thicket of Quercus suber and Pistacia et de la Vie, Département de lentiscus. The region of Azzaba belongs to the eastern part of the Numidian chain at an altitude Biologie Animale, Université des not exceeding 200 m (36°90' North, 07°65' East), belongs to the bioclimatic sub-humid mild to Frères Mentouri Constantine, sub-humid wet. The present work was done within a thicket of cork oak (Quercus suber), moss Algérie. and litter on ground mastic. ~ 966 ~ Journal of Entomology and Zoology Studies

The region of Taya in Guelma (36°50' North, 07°09' East). Friesea espunaensis (Arbea et Jordana, 1993): So far The highest altitude reaches 1260 m. It belongs to the endemic to Spain [27]. This species is new to Algeria and bioclimatic sub-humid to cold winter and hot and dry North Africa. It was collected in moss on soil and forest litter summer. We took in a thicket of Quercus suber and Quercus of Quercus faginea in Edough. faginea and moss on soil. The region of Beni Haroun (Mila) belongs to the sub-humid bioclimatic zone at an altitude of Friesea oligorhopala (Caroli, 1914): Was collected in moss 139 m (36°36 'North, 06°16' East). Our work was carried out on rock in Azzaba. Mediterranean species, described in Libya in a thicket of Ceratonia silliqua, Quercus suber and litter of by [28]. In Algeria this species was harvest on first time in the Lentiscus sp. ruins of Hippone in Annaba by [11]. Reported for the first time in Morocco by [14] 3. Results and Discussion Only citations to the species level are given in the Table I: 3.1.2 The sub-family Neanurinae is represented by four The complete list of species harvested in different localities: genus and five species. three sub families of Neanuridae (Frieseinae, Neanurinae and aurantiaca (Caroli, 1912): A hémiédaphic species Pseudachorutinae), Odontellidae and Brachystomellidae. found in all localities in different types of forest litter, lentisk Among the five prospected localities was the massif of vegetation, in litter of Carob (Ceratonia silliqua) in all Edough from where the most of the total species (25) localities. Known for Algeria [8] and [11]. Reported by [26] in collected. The locality of Azzaba with 15 species had an several stations in Morocco, in Sidi Bourhaba Lake, Marmora average diversity. Guelma, Ouled Habeba and Beni Haroun Forest; Imlil (high Atlas); Mischliffen (middle Atlas). regions with respectively 5, 5 and 3 species were Reported for the first time in a cave in Morocco by [14]. characterized by a reduced diversity (Fig.2). Deutonura zana [22]: Species endemic to Algeria, encountered 3.1 Family Neanuridea in Edough in litter of Quercus faginea. 3.1.1 The sub-family Frieseinae is represented by only one genus with seven species. Edoughnura rara [17]: Endemic to Edough massif of Annaba - Friesea albida (Arbea et Jordana, 1993): A hémiédaphic (Algeria). Specie was found in moss on soil. species extracted from moss on soil in the forest of Quercus faginea of Edough, and in Quercus suber litter from Oum Protanura monticelli (Caroli, 1912): All the specimens were Laouina (Azzaba). Species known in Europe and the collected in Azzaba and Edough massif. Mediterranean region, described for the first time in Spain by [25], cited in Algeria by [16, 21]. Protanura pseudomuscorum (Börner, 1903): Hémiédaphic species was collected in all localities in different types of - Friesea ladeiroi (Gama, 1959): A hémiédaphic species forest litter. Cited for the first time in Algeria by [5] and [11] encountered in moss on soil, in forest litter of Quercus faginea and moss on rock in Edough. In Oum Laouina 3.1.3 The sub-family Pseudachorutinae: is represented by (Azzaba) and Ouled Habeba in litter of Quercus suber and five genus and six species. lentisk vegetation. In Beni Haroun the species was collected Pseudachorutella asigillata (Börner, 1901): A hémiédaphic for the first time in the litter of Pistacia lentiscus. Already species encountered in Edough in moss on trunk of Quercus reported in Algeria by [16] as a new species for the country in faginea and in Beni Haroun. Reported to Libya by [28], in Edough. Morocco by [26] in Mouyougou, and in the forest of Jaaba (Ifrane). Reported to Morocco by [14] in the litter cedar at the Friesea laouina (Deharveng & Hamra Kroua, 2004): The summit in Djebel Tazzeka (Taza). first species of the afurcata-ladeiroi group with reduced eyes (4 + 4). A hémiédaphique species found in different types of subcrassus (Tullberg, 1871): Hémiédaphic forest litter in all localities except Beni Haroun. Endemic to species encountered in Edough and Azzaba, new for Algeria Algeria, described as a new species for science by [15], found and North Africa. Species Widespread in Europe, the in the first time in Zen oak litter. Mediterranean region, Caribbean and Asian center.

Friesea mirabilis (Tullberg, 1871): This specie differs from Pseudachorutes parvulus (Börner, 1901): Was found in litter F. mirabilis by a reduced chaetotaxy of tibiotarsus (tibiotarsi of Quercus suber in Edough. Holarctic species cited for the I, II and III with 17, 17 and 16 chaetae instead of 18, 18 and first time in Morocco by [14] in Azrou, the species was 17), 8+8 eyes, three anal spines without papillae and claw extracted from the humus of Quercus sp. untoothed. F. cf. mirabilis is widespread; found under moss in the forest of Quercus faginea in Edough, in litter of Quercus Pseudachorudina meridionalis (Bonet, 1929): Reported suber in Azzaba and in litter of Ceratonia silliqua in Beni from the Mediterranean region and Europe, it is a Haroun. It is a hémiédaphique species. A widespread species, hémiédaphic species found in Edough massif, Azzaba and cited for the first time in several stations in Morocco by [26], Guelma. Reported in Morocco by [26] in Ifrane under the name reported by [14] in several stations in Morocco in the litter of of Pseudachorudina bougisi. Also cited in Morocco by [14] in cedar and cork oak. Known for Algeria cited by [16] and [21]. Souk el Arba, road Bin el Ouidane Afourer.

Friesea major [19]: Hémiédaphic specie, endemic to Algeria. Pratanurida boerneri (Schött, 1902): Euro-Mediterranean Collected in litter of Quercus faginea in Edough (Annaba), in specie. Reported as new species from Algeria and North litters of Quercus suber and Lentiscus litter in Oum Laouina Africa by [16]. Was found in wood of Quercus suber in (Azzaba), at Djebel Taya (Guelma) and Ouled Habeba Edough massif, also in Guelma and Ouled Habeba. (Skikda).

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Micranurida pygmaea (Börner, 1901): We have found this Edough, and in Djebel Bouarbid (Ouled Habeba). Widespread specie in forest litter of Quercus faginea in Edough massif in Specie in Europe, in America and Australia, reported in Annaba. Species has wide distribution cited for the first time Morocco by [14] under the name of lamellifera in in Morocco in Imlil (high Atlas), Ain Kerzouza, Mouyougou, Djebel Musa near Ceuta; Mount Lexchab. forest of Jaaba (middle Atlas). Also cited by [14] at the cascades of Ain Leuh (Bab Berred), Azrou in a green oak Axenyllodes bayeri (Kseneman, 1935): rara and termophyl forest. specie. It was collected in forest litter of Quercus suber in Edough and Azzaba. Reported in Morocco by [26] in Mikdane 3.2. Family Odontellidae (high Atlas). Superodontella vallvidrerensis subalpina (Arbea 1990) and Superodontella vallvidrerensis vallvidrerensis (Selga 1966): Xenyllodes armatus (Axelson, 1903): Specie was found in Sub-species described in Spain in the Vallvidrera locality forest litter of Quercus faginea in Edough, and in forest litter (Barcelona). S. vallvidrerensis subalpina is endemic in the of Quercus suber in Azzaba. Specie widespread in Europe north of Navarre region [27] are new for Algeria and North cited in Algeria and the whole North Africa as new specie by Africa. The two subspecies were found in forest litter of [16]. Quercus faginea in Edough, in moss on soil near to spring water for S. v. subalpina. S. v. vallvidrerensis were found in 3.3. Family Brachystomellidae moss on rocks near to spring water. curvula (Gisin, 1948): Specie prefers the litter of Cistus, Rosmarinus officinalis and Halimium Superodontella tayaensis [20]: A specie new to science halimifolium. Collected in litter of Quercus faginea in recently described by [20] endemic to Taya massif of Guelma. Edough. It is morphologically closest to S. subalpina [29], with three subequal dental chaetae. They differ in the number of (Schäffer, 1816): We have found tibiotarsal chaetae and the sensilar chaetotaxy of Ant IV. It is this specie in only one locality in Edough massif (Annaba) in hémiédaphic specie. All the specimens were collected in moss moss on soil and litter of Quercus suber. Cited for the first on soil in Taya massif of Guelma. time in Algeria by [30], in Morocco by [26] in Asni (high Atlas), Ifrane, Oued Zad, Jaaba forest (middle Atlas), also reported Superodontella lamellifera (Axelson, 1903): A hémiédaphic by [14] in Azrou in cedar litter Mamora forest (Rabat) in sandy specie. It was collected in forest litter of Quercus faginea in soil.

Fig 1: Sampled areas in the Northeastern Algeria

Friesea laouina [15] Friesea major [19]

Edoughnura rara [17] Protanura pseudomuscorum [9] ~ 968 ~ Journal of Entomology and Zoology Studies

Deutonura zana [22] Deutonura deficiens meridionalis [16]

Bilobella aurantiaca [31] Pseudachorutes parvulus [31]

Superodontella tayaensis [20] Brachystomella parvula [31]

Fig 2: Photos of some collembolan species

Table 1: Neanuridae, Odontellidae and Brachystomellidae species from Algeria (Ed-Edough, Az-Azzaba, Gu-Guelma, O.H.-Ouled Habeba, B.H.-Beni Haroun, OTHER-other localities in Algeria).

Species Ed Az Gu O.H. B.H. OTHER I-Family Neanuridae Börner, 1901 a-Sub family Frieseinae Massoud, 1967 Friesea albida Arbea & Jordana, 1993 0,8 0 8 Friesea espunaensis Arbea & Jordana, 1993 0 Friesea ladeiroi Gama, 1959 0,8 0 0 0 Friesea laouina Deharveng & Hamra Kroua, 2004 0,7,8 0 0 0 Friesea major Hamra Kroua & al, 2009 0,8,11 0 0,12 0 Friesea mirabilis Tullberg, 1971 0,8 0 0 Friesea oligorhopala Caroli, 1914 8 8 b-Sub family Neanurinae Börner, 1901 Bilobella aurantiaca Caroli, 1912 8, 9 8 12 2, 5, 6, 8 Deutonura zana Deharveng et al. 2015 13 13 13 Edoughnura rara Deharveng, Hamra Kroua & Bedos, 2007 9 Protanura monticelli Caroli, 1912 8,9 Protanura pseudomuscorum Börner, 1903 8,9 1, 5, 6, 8 c-Sub-family Pseudachorutinae Börner, 1906 Pseudachorutella asigillata Börner, 1901 0,8 8 0 11 Pseudachorutes parvulus Börner, 1901 8 5,6 Pseudachorutes subcrassus Tullberg, 1871 0,8 0 Pseudachorudina meridionalis Bonet, 1929 8 0 0,12 4,6 pygmaea Börner, 1901 8 Pratanurida boerneri Schött, 1902 0,8 0 0 II-Family Odontellidae Massoud, 1967 Axenyllodes bayeri Kseneman, 1935 8 8 8 Superodontella lamellifera Axelson, 1903 0,8 0 0 4,6 Superodontella vallvidrerensis subalpina Arbea 1990 8 Superodontella vallvidrerensis vallvidrerensis Selga 1966 8 Superodontella tayaensis (1) Arbea et al, 2013 0,8 0,12 Xenyllodes armatus Axelson, 1903 8 8 III- Family Brachystomellidae Stach, 1949 Brachystomella curvula Gisin, 1948 8 Brachystomella parvula Schäffer, 1816 8 3,6,9,10 ~ 969 ~ Journal of Entomology and Zoology Studies

4. Conclusion de Belgique. 1974; 50:1-46. The region of Guelma was characterized by the presence in 13. Stomp N. Collemboles cavernicoles d’Afrique du nord. I addition to species recently described (Superodontella (Insecta). Annales de Spéléologie. 1974; 29(1):109-120. tayaensis). The Collembola of Northeast Algeria cited in this 14. Thibaud JM, Massoud Z. Etude des Collemboles de paper were all known to the country. However, the Northeast certains milieux du Maroc et considérations region biodiversity remains still poorly known regarding biogéographiques sur la faune du Maghreb. Revue Suisse Poduromorpha. First, the survey was limited to a few stations. Zoologie. 1980; 87(2):513-548. Then, the forest habitats sampled represent only a small part 15. Deharveng L, Hamra Kroua S. Une nouvelle espèce de of existing habitats. Friesea Dalla Torre, 1895, du massif de l’Edough, Nord- Finally, several of the cited taxa have been collected in only Constantinois, Algérie (Collembola, Neanuridae). one station and as a few specimens. Such a high proportion of Bulletin de la Société Entomologique de France. 2004; rare species suggests that we can expect new discoveries in 109(2):141-143. exploring other habitats and different types of soils. 16. Hamra Kroua S. Les Collemboles (Hexapoda, Six of the 27 species cited in this paper are new for North Arthropoda) du Nord-Est algérien: Taxonomie, Africa: Friesea laouina; Friesea major, Friesea espunaensis; Biogéographie et Ecologie. Thèse de Doctorat d'état Edoughnura rara; Deutonura zana; Superodontella tayaensis. N°221. Université Mentouri Constantine. 2005; Hence that Northeastern Algeria has a very different fauna 221(248):24, l. from that of its neighboring countries in the Mediterranean 17. Deharveng L, HamraKroua S, Bedos A. Edoughnura rara region. n.gen., n.sp., an enigmatic genus of Neanurinae Collembola from Edough Massif (Algeria). Zootaxa. 5. Acknowledgments 2007; 1652:57-61. Author wish to express their gratitude to: Louis Deharveng 18. Hamra Kroua S, Cancela da Fonseca JP. Dynamique MNHN Institut Systematique, Evolution, Biodiversité. CP 50, saisonnière du peuplement de Collemboles d’un sol 45 rue Buffon, 75005 Paris (France) and Javier I. Arbea,C/ agricole de la ferme pilote d’El-Baaraouia (Wilaya de Ría de Solía 3, Ch. 39, 39610 El Astillero: for their Constantine, Algérie). Bulletin de l’Institut Scientifique, identification, of the most species and for their suggestions Rabat, section Sciences de la Vie. 2009; 31(1):33-43. and corrections to the present manuscript. 19. Hamra Kroua S, Jordana R, Deharveng L. A new Friesea of the mirabilis-group from Algeria (Collembola: 6. Références Neanuridae: Frieseinae). Zootaxa. 2009; 2074:65-68. 1. Lucas H. Aperçu des espèces nouvelles d'insectes qui se 20. Arbea JI, Brahim Bounab H, Hamra Kroua S. Collembola trouvent dans nos possessions francaises du Nord de Poduromorpha from Guelma Province (Northeastern l'Afrique. Revue de Zoologie. 1846; 9:252- 256. Algeria), with description of a new Superodontella 2. Lucas H. Thysanoures de l'Algerie. Exlpor. Sc. Alg. species (Collembola: Odontellidae). Zootaxa. 2013; 1849; 1:371-376. 3709(2):177-184. 3. Absolon K. Ube reine neue subterrane Collembole 21. Brahim Bounab H. Les Collemboles (Hexapoda, Acherontiella onychiuriformis n.g. n.sp. aus den Höhlen Collembola) de quelques localités du Nord-Est algérien: Algiers. Archives de Zoologie Expérimentale et Taxonomie et Appartenance Biogéographique. Thèse de Générale. (Notes et Revues). 1913; 51:1-7. Doctorat 3éme Cycle. Université Mentouri Constantine. 4. Denis JR. Sur deux Collemboles de l'Afrique du Nord. 2016, 200. Bulletin de la Société Entomologique de France. 1922, 22. Deharveng L, Zoughailech A, Hamra Kroua S, Porco D. 284-285. A new species of Deutonura (Collembola: Neanuridae: 5. Denis JR. Sur les Collemboles de l'Afrique du Nord Neanurinae) from north-eastern Algeria, and (3°note). Bulletin de la Société d’Histoire Naturelle characterisation of two intraspecific lineages by their d’Afrique du Nord. 1925; 16:254-256. barcodes. Zootaxa. 2015; 3920(2):281-290p. 6. Denis JR. Sur les Collemboles de l'Afrique du Nord 23. Zoughailech A, Hamra Kroua S, Deharveng L. New (2°note). Bulletin de la Société Entomologique de France. species of Pseudachorutes (Collembola: Neanuridae) 1935; 16:230-233. from Northeastern Algeria. Zootaxa. 2016; (4):557-568. 7. Denis JR. Sur les Collemboles de l'Afrique du Nord 24. Aouadi H. La végétation de l'Algerie Nord orientale. (4°note), Bulletin de la Société d’Histoire Naturelle Histoire des influences anthropiques et cartographie a d’Afrique du Nord. 1937; 28:85-87. 1/200.000. Thèse de Doctorat, Université de Joseph 8. 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Annua. R. Mus. Zool. R. Univ. Napoli IV. 1914, 1-10. 29. Arbea JI. Nuevas especies de Odontella (Superodontella) (Collembola, Odontellidae) de Navarra (N. de la Península Ibérica). Misc. Zool. 1988, 1990; 12:109-119. 30. Handschin E, Über die von H. Gauthier in den Sümpfen Algeriens gesammelten Collembolen. Archiv für Naturgeschichte. 1928; 92(4-7):1-18. 31. Bellinger PF, Christiansen KA, Janssens F. Checklist of the Collembola of the World. http://www.collembola.org, (1996-2014).

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