New contributions to the Eulophidae fauna from Morocco (Hymenoptera, Chalcidoidea) with comparison in the North African region

New contributions to the Eulophidae fauna from Morocco (Hymenoptera, Chalcidoidea) with comparison in the North African region. We present an update of the Moroccan Eulophidae following samples collected in the Maâmora forest between 2012 and 2014, and completed with a thorough bibliographic study. We report seven genera for the first time in Morocco: Allocerastichus Masi, 1924; Euderomphale Girault, 1916; Eulophus Geoffroy, 1762; Euplectrus Westwood, 1832; Microlycus Thomson, 1878; Tamarixia Masi, 1924 and Trjapitzinichus Kostjukov & Kosheleva, 2006 and six species: Baryscapus impeditus (Nees, 1864); Ceranisus menes (Walker, 1839); Elachertus lateralis (Spinola, 1808); Elasmus atratus Howard, 1897; Microlycus biroi (Erdös, 1951) and Trjapitzinichus politus (Graham, 1991). A possible new species (Baryscapus n. sp.) and two unidentified species (Allocerastichus sp. and Euderomphale sp.) are included in the list of Moroccan Eulophidae. Data published through GBIF (Doi: 10.15470/wpyzuh) Keys word: Hymenoptera, Chalcidoidea, Eulophidae, Additions, Morocco Resumen Nuevas aportaciones a la fauna de Eulophidae de Marruecos (Hymenoptera, Chalcidoidea) y comparación con la de la región del norte de África. En este artículo se presenta una actualización de los Eulophidae de Marruecos tras un estudio de las muestras recolectadas en el bosque de Maâmora entre 2012 y 2014, completándose con una minuciosa revisión bibliográfica. Se han registrado por primera vez en Marruecos siete géneros: Allocerastichus Masi, 1924; Euderomphale Girault, 1916; Eulophus Geoffroy, 1762; Euplectrus Westwood, 1832; Microlycus Thomson, 1878; Tamarixia Masi, 1924 y Trjapitzinichus Kostjukov & Kosheleva, 2006 y seis especies: Baryscapus impeditus (Nees, 1864); Ceranisus menes (Walker, 1839); Elachertus lateralis (Spinola, 1808); Elasmus atratus Howard, 1897; Microlycus biroi (Erdös, 1951) y Trjapitzinichus politus (Graham, 1991). Se han incluido en la lista de Eulophidae de Marruecos una posible nueva especie (Baryscapus n. sp.) y dos especies no identificadas (Allocerastichus sp. and Euderomphale sp.). Datos publicados en GBIF (Doi: 10.15470/wpyzuh) New contributions to the Eulophidae fauna from Morocco (Hymenoptera, Chalcidoidea) with comparison in the North African region K. Kissayi, S. Benhalima, A. Benhoussa


Introduction
The family Eulophidae (Hymenoptera, Chalcidoidea) currently comprises 6,038 species belonging to five subfamilies (Noyes, 2019).Several phylogenetic studies have been carried out on this family (Gauthier et al., 2000;Burks et al., 2011;Munro et al., 2011;Heraty et al., 2013).Members of the Eulophidae family are recognized as parasitoids of many insects belonging to Coleoptera, Diptera, Hemiptera, Hymenoptera, and Lepidoptera (Noyes, 2019).They parasitize older larvae or nymphs of holometabolous insects and paralyze them or kill them by multiple bites of the laying female that feeds on the host's juices (Blanchot 1992).Thus, a large number of species in this group have been used in biological control against various crop pests (Cochereau, 1969;Lecoustre et al., 1980;Clair et al., 1987;Etienne and Dumbardon-Martial, 2013;Yefremova et al., 2015).
Another species, Chrysocharis pubicornis (Zetterstedt, 1838), was later cited by Jourdan and Rungs (1934).Two years after this, Rungs (1936) reported Tetrastichus inunctus (Nees, 1834) and Smirnoff (1950Smirnoff ( , 1956) ) cited Aprostocetus minutus (Howard, 1881).A few years later, Delucchi (1962) published a first monograph of the Eulophidae fauna in Morocco, composed of 12 species.At the end the 1990s, other researchers reported the presence of several further species such as Semielacher petiolatus (Girault, 1988) and Citrostichus phyllocnistoides (Narayanan, 1960) used in biological control in agricultural (Nia et al., 1997;Abbassi et al., 1999;Rizqi et al., 2003;Pintureau et al., 2003;Delvare et al., 2011;Smaili et al., 2013).Meantime, in the forest domain, Eulophidae species have been described by El Alaoui El Fels et al. (1999), Maatouf and Lumaret (2012) and Kissayi and Benhalima (2018).In summary, according to a recent study by Noyes ( 2019), 36 species of Eulophidae are known from Morocco, but 14 previously described species were not included in their study (2019).Therefore, we consider that before our study, a total of 50 species were known from Morocco.The aim of this study was to provide an updated annotated checklist of the Moroccan Eulophidae with new data, general distribution, and host preferences.

Collection method
The samples were collected once a week using Malaise traps during the following periods: from May 26th to October 8th in 2012, from May 24th to September 23rd in 2013, and from November 27th to June 14th in 2013.After sorting, the specimens were preserved in alcohol at 70º for identification.
The work of the determinations of this family was preceded by a thorough bibliographical study.

Discussion
This work has enriched the family of Eulophidae in Morocco by adding one new species (scientific description underway), two unidentified species, seven genera, and 20 species, 14 of which have not been listed previously and six are newly identified in addition to the 36 species previously cataloged.Thus, the new number of Eulophidae species in the Kingdom is currently 59.This is a relatively low number and represents only about 1% of this family worldwide according to the catalog of Noyes (2019).Moreover, the majority of genera and species identified in this study belong to the subfamily Eulophinae (14 genera / 27 species), followed by Tetrastichinae (10 genera/19 species), Entedoninae (8 genera/11 species) and finally Opheliminae and Entiinae (recently identified) (1 genus/1 species).
Concerning the Great Maghreb, the Eulophidae currently has 52 genera and 132 binomial species.In addition, some genera have been newly found in Morocco and will be published soon.All these species are included in the annex 1.Moreover, the figures reveal that the entomofauna of the southern shore of the Mediterranean is generally little represented compared to Eulophidae of countries on the north shore, which have many more, such as in France (411 species), Italy (355 species), Spain (232 species), Croatia (165 species), Greece (101 species) and Montenegro (99 species), according to Noyes (2019).This suggests that the entomofauna of the North African region is still poorly known.
The comparison of Moroccan Eulophids with those of the Maghreb countries reveals that Morocco has a relatively rich diversity of this family (59 species is 33 %), almost equitable to Egypt (55 species or 32 %).Egyptian wildlife has been enriched with 15 species thanks to the work of Gadallah et al. (2015).Paradoxically, in Algeria, Tunisia, Libya and Mauritania, the number of species mentioned is respectively 33 (19 %), 16 (9 %) [knowing that Leptocybe invasa is not catalogued (Dhahri et al., 2010)], 9 (5 %) and 3 (2 %) species.It is likely that these figures do not reflect reality because no studies or revisions are currently available in these countries.
The comparative study of Eulophids based on available bibliographic data on fauna of North African indicates a clear difference in faunistic composition.Most of the species have a restricted distribution in North Africa; few are found in more than three or four countries.In fact, of the 132 species mentioned from the total group of Maghreb countries only two species (Baryscapus servadeii (Domenichini) and Necremnus tutae Ribes and Bernardo) are common to four of the six countries in the region.
In addition, Mauritania has the lowest biodiversity of this family, with only three species belonging to three genera: Meruacesa Koçak and Kemal, Trichospilus Ferrière and Tamarixia Mercet.This last genus has recently been identified in Morocco (Benyahia, 2016).
Four genera, Allocerastichus Masi, Ceranisus Walker, Microlycus Thomson, and Trjapitzinichus Kostjukov and Kosheleva are mentioned for the first time in North Africa (Morocco), each represented by a single species.
On the other hand, Aprostocetus Westwood is the most diversified genus of this family, not only in the Maghreb (11 species) in general but also in Morocco (5 species).It is a widespread Mediterranean genus, being known on European shores in Spain and France (Askew et al., 2013), Italy (Conti et al., 2000), Greece (Graham, 1987), Montenegro (Bouček, 1977), and Cyprus (Thompson, 1955), and on Asian shores in Turkey (Fry, 1989), Lebanon (Domenichini, 1966) Syria, and Israel (Japoshvili et al., 2015).It is also known on the African east shore in Algeria (Kostjukov, 1989), in the west in Tunisia (Lo Verde et al., 2010) and east in Egypt (Doğanlar and Elsayed, 2013).This genus is also reported in Eastern Europe in Slovenia (Graham, 1987) and Croatia (Bouček, 1977).Some rather diverse genera in the Maghreb, such as Cirrospilus Westwood and Baryscapus Förster (8 species), Chrysocharis Förster and Entedon Dalman (6 species), occupy a region that goes from Morocco to Egypt, passing through at least two of the following countries: Algeria, Tunisia, and/or Libya.These genera have shown the ability to adapt and settle in these diversified places along a horizontal trajectory.They were also widely represented in several European Mediterranean countries as far as Turkey, Israel and Syria for the genus Baryscapus.
Other genera, such as Diglyphus Walker, Elasmus Westwood and Tetrastichus Haliday (four species), are better represented in the countries of the northern shore of the Mediterranean (France, Spain, Italy, Croatia, Turkey and Israel) and less diversified in the southern shore Neochrysocharis Kurdjumov (two species) and Sigmophora Rondani (one species) are  reported in the west of Morocco and Egypt in the east while they are absent from Algeria, Tunisia and Libya.This gap in space cannot be explained for the moment, but it probably due to a lack of research and only partial knowledge of this entomofauna in these Maghreb countries.The genus Neochrysocharis is most highly represented in Spain, Italy, Croatia, Greece, Montenegro and Turkey, unlike Sigmophora that is represented in the Mediterranean countries only by two species, S. brevicornis (Panzer) and S. italica (Domenichini) (fig.2).
Being located in the West-Palaearctic region, Morocco is known for its rich and diverse ecosystems and habitats, and should in principle therefore shelter a greater number of species.Knowledge of the Moroccan heritage should be improved by carrying out research programmes on this Hymenoptera group in several regions of Morocco in order to discover and enrich our knowledge of this fauna.The same applies to all the countries of the Great Maghreb which should be part of this research logic since they are among the biodiversity hotspots.Trjapitzin, V. A., 1978. Hymenoptera II. Chalcidoidea 13. Eulophidae (excl. Tetrastichinae).

Fig. 2 .
Fig. 2. Geographical distribution of most of the genera compared in countries of the Mediterranean Sea.