Acta agriculturae Slovenica, 118/4, 1–8, Ljubljana 2022 doi:10.14720/aas.2022.118.4.2441 Original research article / izvirni znanstveni članek Diversity of hymenopteran families associated to quinoa crop in Algeria (case of Biskra province) Hasna SEGHIR 1, NacerTARAI 1 and Souad TAHAR-CHAOUCHE 2, 3 Received November 29, 2021; accepted November 06, 2022. Delo je prispelo 29. november 2021, sprejeto 6. november 2022 1 University of Biskra, Faculty of Exact and Natural Sciences, Department of Agronomy, Biskra, Algeria 2 Scientific and Technical Research Centre for Arid Areas (CRSTRA), Biskra, Algeria 3 Corresponding author, e-mail: souadhouda@gmail.com Diversity of hymenopteran families associated to quinoa crop in Algeria (case of Biskra province) Abstract: The quinoa (Chenopodium quinoaWilld.) crop is originated from Andean region (South America). Its nutri- tional values as well as its drought climate and water salinity tolerant character have motivated many countries such as Al- geria to adapt such a plant culture. This study aims to assess entomofauna from Hymenoptera order in terms of composi- tion and functional diversity. We aim also to evaluate the con- sequences of the expansion and uncommon crop on the hy- menopteran composition. For the first field trial, the survey was carried out in Biskra province during 2018-2019. The Shannon Wiener index and evenness indices were used to measure fam- ily’s diversity. The results revealed that 1737 specimens were identified into forty families and 166 species. Formicidae spe- cies were the most abundant with 68 % of total number of in- dividuals, followed by Braconidae with 7 % and Crabronidae with 5 %. As well, diversity collected with yellow pan traps was more important in winter and spring seasons. As the functional groups, results indicated the presence of three major groups; parasitoids, pollinators and predators. The parasitoid group is the richest one. Key words: quinoa crop; hymenoptera order; abundance; Shannon Wiener index; Biskra Raznolikost družin kožokrilcev v posevkih kvinoje v Alžiriji (primer province Biskra) Izvleček: Kvinoja ali perujski riž (Chenopodium quinoa Willd.) je poljščina, ki izvira iz območja Andov v Južni Ameri- ki. Njena velika hranilna vrednost kot tudi odpornost na sušo in slanost so motivirale številne države, med njimi tudi Alžirijo, da jo uvedejo v pridelovanje. Name te raziskave je bil oceniti favno žuželk iz reda kožokrilcev v posevkih te poljščine glede na sestavo in funkcionalno raznolikost. Namen raziskave je bil tudi ovrednotiti posledice razširjanja te nenavadne poljščine na sestavo favne kožokrilcev. Prvi poljski pregled je bil izveden v province Biskra, v rastni sezoni 2018-2019. Kot merili raznoli- kosti družin sta bila uporabljena Shannon Wienerjev indeks in indeks izenačenosti. Rezultati so pokazali, da je bilo določenih 1737 primerkov, ki so pripadali 40 družinam in 166 vrstam. Vrste iz družine Formicidae so bile najbolj pogoste, s 68 % de- ležem vseh osebkov. Tem so sledile Braconidae s 7 % in Cra- bronidae s 5 % deležem. Raznolikost, ki je temeljila na ulovu z rumenimi ploščami je bila bolj pomembna pozimi in spomladi. Rezultati so pokazali, da so bili med funkcionalnimi skupinami prisotni parazitoidi, opraševalci in plenilci kot glavne skupine, med njimi je bila skupina parazitoidov najbogatejša. Ključne besede: kvinoja; redovi kožokrilcev; pogostost; Shannon Wienerjev indeks; Biskra Acta agriculturae Slovenica, 118/4 – 20222 H. SEGHIR et al. 1 INTRODUCTION Insects represent the major component of terrestrial ecosystems (Weisser and Siemann, 2004).In trophic in- teractions (insect-plant), plants serve as resources for in- sects. They tend to interact with similar partners and they show a stronger conservatism levels for insect pollinators and herbivorous insects (FontaineandThébault , 2015). However, this relationship between insects and plants is not stable and in several cases, native insects have adapt- ed to the introduced crops(Morrill, 2004).Hymenoptera order is one of the largest orders (Gaston, 1993), it ranks the third after Coleoptera and Lepidoptera (Stork, 1997), important members of hymenopteran species belong to higher trophic levels, they are more sensitive to any change of their habitats. Three main groups, ants, bees and parasitoids play crucial role in preserving diversity (Rot et al., 2021).Quinoa ((L.)Willdenow) crop is a pseu- do-cereal with high nutritional value; it can be grown in dry climates and tolerates high levels of irrigation water- salinity. To improve food security, it was introduced in Algeria in 2014.It has been the subject of some field tri- als in arid regions. In Biskra province, quinoa crop was firstly sown in September 2015 on El-Outaya site. There are various reasons for studying diversity related to an exotic plant species.Firstly, know the taxonomy of local hymenoptera reservoir and understand the influence of quinoa crop on species behaviors.This study aims to car- ry out an exhaustive inventory of hymenopteran families associated with this introduced crop and to evaluate their diversity and abundance. 2 MATERIALS AND METHODS 2.1 STUDY REGION Fieldwork was conducted in El-Outayalocated in the north of Biskra province (34°55’58.27 ‘’ N, 5°39’34 41’’ E, altitude,207 m) (Figure1). This region is character- ized by an arid climate with mild winter and wet spring. Survey was done from February 2018 to February 2019 during plant life cycle. Collections were done every week to twice a month depending on the season. 2.2 SAMPLING METHODS Two trap types were chosen for this study: yellow pan traps and pitfall traps. They were known to be good in catching insects. First trap type is a yellow colored plastic rectangular pan with 30 cm of diameter and a height of 20 cm.The pitfall traps were a plastic jar with a diameter of 10 cm and a height of 10 cm-16 cm. Each trap was filled with an immersing medium composed with a mixture of half liter of clean water and some deter- gent drops. Three traps of each trap type were distribu- teover crop area of 250 m2 at a distance of about 2.5-5 m from each other. 2.3 IDENTIFICATION OF INSECTS Collected insects were preserved in Eppendorf tubes that contain 70  %ethanol and taken to Entomo- logical laboratory, Department of Agronomy, Biskra for identification. Several available keys of identification were used with reference to Delvare and Aberlenc, 1989; Goulet and Huber, 1993; Amiet et al., 2001; Amiet et al., 2004; Mikó et al., 2007, 2013; Farahani and Talebi, 2012; Paukkunen et al., 2015; Wu et al., 2016; Zi and Zaifu, 2016; Ghafouri Moghaddam et al., 2016; Farahani et al., 2016; Rousse and Villemant, 2012; Edmardashand et al., 2011; Schmid-Egger et al., 2017; Ferrer-Suay et al., 2015; Choi et al., 2012; Chen et al., 2017; Izadizadeh et al., 2015; Mokrousov, 2017; Aguirre et al., 2015; Yari et al., 2016; Zargaretal, 2019; Mikó et al., 2013; Prous et al., 2014, 2019. In order to justify insect trophic relation- ships, different plant species nearby the quinoa crop were sampled (Table1). 2.4 ANALYSIS To evaluate insect biodiversity, the common meas- ures were used, like species richness, Shannon-Wiener index and evenness measure. 2.4.1 Species richness (S) It is a simple measure of total number of species in each sample in a given area. Thismeasurement is strongly dependent on sampling efforts. 2.4.2 Shannon-Wiener index (H’) It takes into account the number of individuals of each species within the local community. H’ = -ΣPi log Pi Where: H’ = Shannon Wiener index Pi = proportion of “ith” species and is calculated as Acta agriculturae Slovenica, 118/4 – 2022 3 Diversity of hymenopteran families associated to quinoa crop in Algeria (case of Biskra province) “ni/N”, where, “ni” is the number of individuals in “ith” species and N is the total number of individuals in the sample. 2.4.3 Measure of evenness (E: Equitability) It can be calculated by using species richness (S) and Shannon Wiener index (H’).It represents an important component of the diversity indices. It indicates how indi- viduals are distributed among the different species. E = H’ / log(S) 3 RESULTS During this study, 1737 specimens were collected from quinoa crop. They were identified into 40 fami- lies and 166 species (Table2). Values of different indices calculated over all the seasons were: Shannon-Wiener index, H’ = 3.72bits, Evenness (E) = 0.50. In the collec- tion, 32 families were collected withpitfall traps and 29 families with yellow pan traps. Among these 1737speci- mens, 1377 were collected with thepitfall traps and rep- resented 95 species, most of 1377 individuals belonged Plant species Cultivated Spontaneous Atriplex halimusL. - + Casuarina equisetifolia L. + - Chenopodium vulvaria L. - + Cupressus sempervirens L. + - Diplotaxis harra (Forssk.) Boiss. - + Hordeum vulgare L. + - Malva parviflora L. - + Medicago sativa L. + - Moricandia arvensis DC. - + Moringa oleifera Lam. + - Olea europaea L. + - Pinus halepensis Moulin + - Salsola vermiculata L. - + Sesbania aculeata (Willd.) Poir. + - Sonchus asper L. - + Suaeda mollis Delile - + Tamarix gallica L. - + Vitis vinifera L. + - Zea mays L. + - Table 1: Cultivated and spontaneous plants collected infield- work Figure 1: Situation of study site: Map of Algeria (A) showing the study province (B) and the study region Acta agriculturae Slovenica, 118/4 – 20224 H. SEGHIR et al. to Formicidae family with 1088 specimens. The rest 360 specimens were collected with the yellow pan traps. In this trap type, 126 species were recorded. 40 species were found in all trap types. The dominant family was For- micidae with 1175 specimens, followed by Braconidae with 124, Crabronidae with 80, Ichneumonidae with 55, Diapriidae 43 and Andrenidae with 35, whereas 17 families were represented with less number of specimens and 11 families with only one specimen (Figure 2). Dur- ing autumn (17/10-22/12) 136 specimens were collected while 261 insects were collected inwinter (23/12-22/3) and 1340 in spring (23/3-17/5). The calculate values of various indices were presented in Table 3. In autumn, in yellow pan traps two most abundant families were Ichneumonidae with 37  % and Vespidae with 20 %, but in pitfall traps, the Formicidae is the most abundant family with 58 %. In winter, the Diaprii- dae family was the most abundant with 21 % in yellow pan traps and the Braconidae family with 25 % in pitfall traps. In spring, in yellow pan traps; three families were the most abundant Formicidae with 40 %, Crabronidae with 20 % and Braconidae with 10 % but in pitfall traps, there was an almost total dominance of Formicidae fam- ily with 83 %. Values of Shannon-Wiener index (H’) and Evenness (E) indices presented in Table 4 and Table 5 indicate that yellow pan traps were more efficient.Spring and winter remain the best seasons of insect activity in study site. About the functional groups, results indicated the presence of three big groups; parasitoids, pollinators and predators Table 2. The parasitoid group is richer in all seasons. In collected data Crabronidae was the most abundant family of predator. Pollinator families showed no differences in abundance. However, various parasitoid species numbers were observed in all season (Figure3). 4 DISCUSSIONS Available literature provides less information about entomofauna diversity of quinoa agro-ecosystem in na- tive regions (Valoy et al., 2015). In Algeria, Biskra prov- ince is one of few production areas of quinoa and the only inventory done by Deghiche et al. (2021) in 2015- 2016 at El-Outaya field may not reflect the true diversity at regional level. Deghiche et al. (2021) reported 5 hyme- nopteran families, 6 species and 174 specimens. As the second entomofauna listing on quinoa crop at the same site, present study showed a total of 40 hymenopteran families, 166 species and 1737 specimens. Among the collected families, the highest frequency was obtained for Formicidae (68  %). General calculate diversity indices (H’=3, 72 bits and E = 0.50) according to literature range indicated high rich hymenopteran families diversity and moderate distribution throughout the site study. In an ecosystem, various vegetation and favorable climatic con- ditions also maintain a high diversity of insect (Rasheed and Buhroo, 2018). At the trial site, different vegetation strata and types were present.Our results suggest that this agro-ecosystem harboured an important hymenopteran fauna. Comparison of the diversity indices between yel- low pan traps and pitfall traps revealed that hymenop- teran fauna composition collected by yellow pan is more important and evenly distributed (in terms of specimen abundance) than collected by pitfall traps. An analysis of the composition of hymenopteran families indicated that 77.77 % of the total specimen abundance is formed by 28 hymenopteran families but in the case of the pitfall traps, we found that 83.07 % of the total specimen abundance is formed by a single family (Formicidae). The winter and spring season results could be explained, in part, due to the key role of temperature as environmental factor inin- sect’s live cycle and in other part to high plant diversity nearby quinoa crop. Nonetheless, similar diversity could be not found in autumn, when all crop and spontane-Figure 3: Hymenoptera species abundances of different func- tional groups Figure 2: Population pie chart of abundant families given in relative abundance (percent) Acta agriculturae Slovenica, 118/4 – 2022 5 Diversity of hymenopteran families associated to quinoa crop in Algeria (case of Biskra province) Order Super-family Families Species Number Specimen effectif Diets Hymenoptera Pamphilioidea Cameron, 1890 Megalodontesidae Konow, 1897 1 4 phytophagous Tenthredinoidea Latreille 1803 Tenthredinidae Latreille, 1802 1 2 phytophagous Chrysidoidea Latreille, 1802 Chrysididae Latreille, 1802 7 7 Parasitoids Dryinidae, Haliday, 1833 1 1 Parasitoids Bethylidae, Forster, 1856 1 1 Parasitoids Scolioidea Latreille, 1802  Scoliidae, Latreille,1802‏ 6 7 Parasitoids Vespoidea Latreille, 1802 Vespidae, Latreille, 1802 5 30 Predators Mutillidae, Latreille, 1802 1 1 Parasitoids Formicidae Latreille, 1809 8 1175 Variable diets Pompilidae, Harris, 1987 2 2 Parasitoids Apoidea Latreille, 1802 Crabronidae, Latreille, 1802 3 80 Predators Sphecidae, Latreille, 1802 10 1 Parasitoids Andrenidae, Latreille, 1802 3 35 Pollinators Apidae, Latreille, 1802 9 32 Pollinators Megachilidae, Latreille, 1802 6 7 Pollinators Melittidae, Michener, 2000 2 9 Pollinators Halictidae, Thomson, 1869, 5 32 Pollinators Colletidae, Lepeletier, 1841 1 6 Pollinator Ichneumonoidea Latreille, 1802 Braconidae, Latreille, 1829 21 124 Parasitoids Ichneumonidae, Latreille, 1802 29 55 Parasitoids Cynipoidea Latreille, 1802 Figitidae,Thomson, 1862 1 1 Parasitoid Diaproidea Halliday, 1833 Diapriidae, Haliday, 1833 3 43 Parasitoids Proctotrupoidea Latreille, 1802 Proctotrupidae, Latreille, 1802 2 6 Parasitoids Platygastroidea Haliday, 1833 Platygastridae, Haliday, 1833 5 12 Parasitoids Scelioninae, Haliday, 1839 5 6 Parasitoids Ceraphronoidea Haliday, 1833 Megaspilidae, Ashmead, 1893 2 23 Parasitoids Ceraphronidae, Haliday, 1833 3 5 Parasitoids Mymarommatoidea Debauche, 1948 Mymarommatidae, Debauche, 1948 2 2 Parasitoids Continued on next page Table 2: Total number of species and specimens of Hymenoptera by families and their diets collected from Biskra province. No- menclature of all hymenoptera families is follows that orders in Fauna Europaea (2021) Acta agriculturae Slovenica, 118/4 – 20226 H. SEGHIR et al. Hymenoptera Chalcidoidea Latreille, 1817 Aphelinidae, Thomson, 1876 1 2 Parasitoid Chalcididae, Latreille, 1817 1 1 Parasitoid Elasminae (Eulophidae) 1 1 Parasitoid Encyrtidae, Walker, 1837 2 2 Parasitoids Eulophidae, Westwood, 1829 2 6 Parasitoids Eupelmidae, Walker, 1833 1 1 Parasitoid Pteromalidae, Dalman, 1820 4 4 Parasitoids Tanaostigmatidae, Howard, 1890 1 1 Parasitoid Trichogrammatidae Haliday & Walker, 1851 1 1 Parasitoid Eurytomidae, Walker, 1832 3 3 Parasitoids Mymaridae, Haliday, 1833 3 5 Parasitoids Tetracampidae, Förster, 1856 1 1 Parasitoid Indices of Hymenopterafamilies diversity Name Autumn Winter Spring All Season Richness S 19 28 27 40 Individuals 136 261 1340 1737 Shannon H (bits) 3.04 3.86 1.28 3.72 Evenness E 0.71 0.80 0.26 0.50 Table 3: Indices values of Hymenoptera families’ diversity Indices of yellow pan collected Hymenoptera families Name Autumn Winter Spring All Season Richness S 12 20 22 29 Individuals 51 113 196 360 Shannon H (bits) 2.75 3.48 3.01 3.72 Evenness E 0.76 0.80 0.67 0.76 Table 4: Indices values of hymenoptera families collected by yellow pan in study seasons Indices of pitfall traps collected Hymenoptera families Name Autumn Winter Spring All Sea- son Richness (S) 15 21 21 32 Individuals 85 148 1144 1377 Shannon (H) (bits) 2.45 3.55 0.80 1.47 Evenness (E) 0.62 0.80 0.18 0.29 Table 5: Indices values of hymenoptera families collected by pitfall traps in study seasons ous plants were in the early stages of their growth. In El-Outayasite, the average monthly temperatures during study in winter ranged from 12.1 to16.7 (with maximum of 27.1 ⁰C) and the difference between the maximum and minimum temperature did not exceed 8 ⁰C.Some obser- vations were recorded in spring with mean monthly tem- peratures oscillated between 17.5 and 25 (with maximum of 30 ⁰C). With the exception of spring data collected by pit- fall traps, various diversity indices calculated in all sea- son (Tables 4 and 5) showed that great hymenopteran diversity were recorded and the detected families were evenly distributed throughout areas trial. At the quinoa field, scares infestation were observed. Moth was found on leaves in early stages, but the presence of aphid spe- cies and thrips were later. In the quinoa native region (Andes), aphids and thrips are considered occasional pests (Cruces et al., 2021).In trial field, quinoa harbours important hymenopteran diversity with different diets. The natural enemy complex formed by parasitoids and predatorsplays an essential role in plant protection. This crop-system proved very favorable for pollinator because they need good foraging resources.Surrounded by low use of pesticides and a variety of crops and herbs, the quinoa crop allows insects to have food and refuge Bur- gioet al. (2006).The results may also explain the greater diversity of entomophagous hymenopteran families. Par- asitoids were the dominate group (Table 2).According to Rasmussen et al. (2003) in Andean region, up 45  % of quinoa pests were naturally controlled by parasitoids and predators. Apparently, our results were relatively similar to those in Cruces et al. (2020 a, 2020b); the introduced Acta agriculturae Slovenica, 118/4 – 2022 7 Diversity of hymenopteran families associated to quinoa crop in Algeria (case of Biskra province) quinoa crop appears with positive impact on local in- sects’ diversity. 5 CONCLUSIONS This study is the first research to emphasize the di- versity of hymenopteran families present in the Biskra province. It has been shown the presence of 40 hymenop- teran families and 166 species. Thus, the found richness may give more information about herbivore identity and entomophagous guilds function in relation to local plant diversity and introduced crops us quinoa at locality scale. It may be important to survey the component of each family. This data can be used as example for integrate pest management of quinoa cultivation in the future. 6 REFERENCES Aguirre, H., D’Almeida, L.P., Shaw, S.R., & Sarmiento, C.E. (2015). An illustrated key to Neotropical species of the ge- nus MeteorusHaliday (Braconidae, Euphorinae). 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