Surveys were carried out in the 3 palm groves belonging to the oasis ecosystem of the Biskra region during the 3 years of sampling (2014, 2015, and 2016) revealed the presence of 18 species of primary parasitoids collected from the mummies of 22 species of aphids collected from 29 plant species, belonging to 13 botanical families. A number of 83 plant-aphid-parasitoid tri-trophic associations were obtained in the study area. The species Aphidius matricariae (Hal.) was the most abundant species by 16 tri-trophic associations. As well, the species L. testaceipes formed 14 associations.
Distribution
About 37 species of the aphid parasitoids have been recorded in Algeria before (Laamari et al. 2011, 2012; Aroun 2015; Ghelamallah et al. 2018). In this study, 18 species of the primary aphid parasitoids recorded belong to the 2 subfamilies; Aphidiinae (Hymenoptera: Ichneumonoidea, Braconidae), represented by 17 species and 6 genera (Aphidius, Diaeretiella, Ephedrus, Lysiphlebus, Praon, and Binodoxys) and the subfamily Aphelininae (Hymenoptera: Chalcidoidea, Aphelinidae) represented by only one species of the genus Aphelinus.
Most of the species mentioned in this study (Aphelinus mali, Aphidius colemani, A. ervi, A. funebris, A. matricariae, A. sonchi, Binodoxys angelicae, Diaeretiella rapae, Ephedrus niger, Lysiphlebus confusus, L. fabarum, L. testaceipes, Praon volucre, and P. yomenae) have been already reported in Algeria (Laamari et al. 2011, 2012). They have not been found only in the countries of the Great Maghreb (Stary and Sekkat 1987; Ben Halima and Ben Hamouda 2005; Laamari et al. 2011, 2012; Boukhris-Bouhachem 2011; Ayadi et al. 2017) but also been found in the eastern Mediterranean region (Kavallieratos et al. 2004). According to Laamari et al. (2012), the parasitoid fauna of Algeria reveals a clear resemblance to that of southern Europe.
Based on the number of species identified up to the present study, and given the great taxonomic, eco-systemic and landscape diversity in Algeria, it could be, fairly, stated that further expended surveys of aphid parasitoids of the country will undoubtedly enrich the present list.
Tri-trophic relationships: parasitoids-aphids-plants
All Aphidiinae species having a high degree of specialization against aphids and important capacity to control these pests. This strong specialization is an advantage for biological control. For the effective use of these organisms in biological control, it is important to know the trophic relationships between parasitoid species, aphid species, and host plants. According to Navasse (2016), the study of plant-aphid-parasitoid food webs enables us to define locally the width of the host/parasitoid spectrum, the dynamics of temporal exploitation of hosts and the distribution of generalist and specialist species in the different habitats over time.
In the present study, the 2 species A. matricariae and L. testaceipes were the most abundant species among aphid parasitoids in terms of trophic relationships. The same observations were reported by Tahar Chaouche and Laamari (2015) in the natural environment of the same region, and by Laamari et al. (2011, 2012) in Eastern Algeria.
The species A. matricariae had 16 associations, parasitizing 10 species of aphids infest 10 plant species (Table 1). According to the present work and the works carried out by Tahar Chaouche and Laamari (2015) in the natural environment, by Hemidi et al. (2013) in the urban environment of the Biskra region, and Laamari et al. (2011, 2012), it could be stated that this parasitoid species has a broad spectrum of hosts in this region. It was found associated with 25 species of aphids. In the Eastern part of the country, it was recorded on 23 aphid species (Laamari et al. 2011), while in the North, it was found associated with 36 species (Aroun 2015). It was, also, reported as the dominant species in the western part (Ghelamallah et al. 2018).
The species L. testaceipes ranked the second, with 14 associations. It was collected from the mummies of 10 aphid species infested 12 plant species (Table 1). Currently, the host spectrum of this species is 13 species of aphids (Hemidi et al. 2013; Tahar Chaouche and Laamari 2015). It is reported in different types of habitats (natural, cultivated, and urban) and on different host plant species (spontaneous, cultivated, and ornamental plants). According to Laamari et al. (2011), this parasitoid was recorded parasitizing 20 aphid species.
This parasitoid originally from the Nearctic realm (Tomanović et al. 2018) introduced into France, and later became the most dominant parasitoid in the Mediterranean region (Žikic et al. 2015). The same authors mentioned that this parasitoid was recently classified as an invasive species, and its presence may be responsible for a partial change in the structure of the native parasitoid fauna in the form of a decrease in their relative abundance. On the other hand, L. testaceipes, often, parasitizes populations of common and often even exotic pest species such as Toxoptera aurantii (Boyer de Fonscolombe) and Aphis spiraecola (Patch) (Žikic et al. 2015). In Algeria, L. testaceipes is considered promising as a naturalized biocontrol agent against the newly invasive pest in the Mediterranean; Aphis illinoisensis (Shimer) (Laamari et al. 2016).
The two species Aphidius funebris and A. ervi were also among the most abundant parasitoid species in the study area, with relatively a quite number of associations and host spectrums.
The parasitoid Aphidius funebris was the most dominant in the site of Foughala than in the other two sites dominated by A. matricariae and L. testaceipes. It was reported on 7 species of aphids, but it showed a preference to parasitize the aphid species of the genus Uroleucon. The same remarks were mentioned by Talebi et al. (2009) and Aggoun et al. (2016).
Aphidius ervi, the parasitoid of alfalfa aphids, is a Palearctic oligophagous species associated mainly with macrosiphinin aphids, such as Acyrthosiphon pisum on legumes and, in a lesser measure, with Macrosiphum euphorbiae Thomas and Aulacorthum solanii (Kaltenbach) (Kos et al. 2009). In the present study, this species was reported by 10 associations, especially on Uroleucon ambrosiae and U. sonchi (Table 1). This oligophagous parasitoid is used as a biological control agent for many species of aphids, especially against large aphid species (Kos et al. 2009).
The presence of parasitoid species with an intermediate number of associations and the host spectrum can be described as intermediate, such as the cases of Aphidius colemani, Diaeretiella rapae, L. fabarum, P. volucre, P. yomenae, and B. angelicae.
The species A. colemani was found associated much more with aphids of fruit trees (Aphis punicae and Hyalopterus pruni). It is also considered among the most dominant species on ornamental plants in the urban environment of Biskra (Hemidi et al. 2013), and in the oasis in the Ghardaïa region (Chehma and Laamari 2014).
In the Mediterranean basin, A. colemani was isolated from mummies of Melanaphis donacis (Passerini) and H. pruni in Morocco, Italy, and France (Stary and Sekkat 1987). It was also reported in Tunisia on H. pruni (Ben Halima and Ben Hamouda 2005) and on Aphis gossypii (Boukhris-Bouhachem 2011). In the Southern parts of Western Europe, this species is naturally absent (Laamari et al. 2012).
Diaeretiella rapae was found mainly associated with barley aphids, Rhopalosiphum maidis and Metopolophium dirhodum and on Myzus persicae infesting Lepidium draba (Brassicaceae) (Table 1). This association was also mentioned in other regions in Algeria (Chehma and Laamari 2014; Tahar Chaouche and Laamari 2015; and Laamari et al. 2016). Laamari et al. (2016) noted that this species was found at several locations in all cereal crops, and it was considered as the most important parasitoid of the Russian wheat aphid Diuraphis noxia (Kurdjumov).
An overall analysis of the data in the study area showed the habitat preferences of Lysiphlebus fabarum, as well as its specific activity on general aphids, belong to the genus Aphis. It parasitized the aphids that appeared on plant species belonging to 4 botanical families: Asteraceae, Fabaceae, Poaceae, and Amaranthaceae.
The Praon genus is represented in the present study by 2 species; P. volucre and P. yomenae. Those showed a preference for Macrosiphini aphids, especially Uroleucon species. The same results were found in other regions of Algeria by Laamari et al. (2011, 2012).
In general, species of the genus Binodoxys are specialized in parasitism of aphids found on herbaceous plants (Lazarević et al. 2017), but in the area of this study, the parasitoid Binodoxys angelicae was found associated with Aphis rumicis infesting Rumex sp. It was found to parasitize Aphis punicae installed on pomegranate.
Monophagous or specific parasitoid species attacking one or two aphidian species are also present. That was found in cases of Aphelinus mali, Aphidius sonchi, Binodoxys sp, Ephedrus niger, and Lysiphlebus confusus.
The parasitoid Aphelinus mali emerged from a single host species of aphids, Hyperomyzus lactucae on Sonchus oleraceus. The presence of this parasitoid was noted only twice in Algeria: on Eriosoma lanigerum associated with Malus communis; in Northern and Eastern Algeria (Laamari et al. 2011; Aroun 2015).
The species Aphidius sonchi has been well developed on the aphidian species Capitophorus inulae associated with Dittrichia viscosa. It has been reported only once in Eastern Algeria on Hyperomyzus lactucae associated with Sonchus oleraceus (Laamari et al. 2012). In the present study, it was also collected from H. lactucae associated with Sonchus oleraceus.
Binodoxys sp., was recorded for the first time in Algeria parasitizing Hyadaphis foeniculi (Passerini) on Rubia tinctorum (Rubiaceae).
Ephedrus niger was reported only once in Algeria by Laamari et al. (2011) who collected it from Brachycaudus helichrysi on an ornamental plant Myoporum laetum. In the present study, this species was collected only from the region of Branis, which represents the mountain oasis system from Capitophorus inulae Passerini and Ovatus inulae Walker, two specific aphids on the viscous Inula, Dittrichia viscosa (Asteraceae). The same behavior was found in the parasitoid, Lysiphlebus confuses, that found only on the Aphis fabae associated with Solanum nigrum in the same region.
An analysis of the tri-trophic associations constituted in the different oasis ecosystems of the Biskra region allowed to find out primordial results, which constitute a very important source of ecological information on the aphid parasitoids as biocontrol agents.
Given the number of associations formed during this study, it is noted that some parasitoids had a large dispersal capacity, in particular, the species belonging to the genera Aphidius and Lysiphlebus.
The parasitoids identified in the present study showed a specialization gradient, ranging from a group of species with a high degree of specialization (as in cases of Binodoxys sp, Ephedrus niger, and Lysiphlebus confusus) to a high degree of generalist (as in cases of A. matricariae and L. testaceipes) with many intermediate statuses. Some generalists’ parasitoid species showed a preference towards some host species (e.g., Aphidius funebris). Some aphid parasitoid species had preferences towards the habitat, the host plant, the botanical family. etc., all these parameters had an impact on the trophic associations formed. Generally, generalists were the most abundant. Navasse (2016) reported that the existence of generalist parasitoids is strongly questioned because with the dominance of specialists, there is a risk of limiting the possibilities of exchanges between cultivated and wild resources of agroecosystems. So, generalists may prove as an important resource for biological control programs in the future.
It has been, also, observed that the host (aphids) include both economic and non-economic species, and some species of aphid parasitoids did attack both types of hosts, so these non-economic species may play a potential role as alternative hosts of parasitoid species in case of absence of their main hosts.
This study assessed the potential of non-crop areas as reservoirs for parasitoids available for crop protection.
Finally, the oasis ecosystems of this region have an appreciable richness of parasitoids than the other surveys carried out in the same region. This can be explained by the complexity and heterogeneity of these environments, which offer a favorable and relatively stable environment for the conservation of these natural enemies.
