Sandrine Mariella Bayendi Loudit, René Noël Poligui, Auguste Ndoutoume, François Verheggen & Frédéric Francis

Abundance and diversity (taxon families) of entomofauna within vegetable crops of urban gardens (in July and August) in Libreville and Owendo (Gabon)

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Résumé

L'abondance et la diversité de l'entomofaune a été réalisée dans trois périmètres maraîchers du Gabon, à savoir les localités de l'aéroport de Libreville (ADL), PK8 et Owendo. Les piégeages avec des pièges jaunes des insectes et des observations visuelles sur les plants ont été réalisés de juillet à août, en 2012 et 2013. Les insectes collectées chaque semaine ont été identifiés au niveau taxonomique (famille) et classés en trois catégories: nuisibles, utiles et associés. Huit ordres et 84 familles d’insectes ont été échantillonnés avec 7910 et 3148 individus, respectivement en 2012 et 2013. L'abondance d'insectes sur l’oseille de guinée (Hibiscus sabdariffa L. 1753; Malvaceae) était significativement plus élevée à ADL qu’au PK8 et à Owendo, que sur l'amarante (Amaranthus hibridus L. 1753; Amaranthaceae), la tomate (Lycopersicon esculentum Mill. 1768; Solanaceae) et le chou (Brassica oleracea L. 1753; Brassicaceae) au PK8 et à Owendo. En 2012, 29,6 %, 31,4 % et 38,9 % des insectes ont été enregistrés respectivement à ADL, PK8 et Owendo. En 2013, seulement les sites de ADL et PK8 ont été échantillonnés, avec une abondance respective de 61,7 % et 38,3 % d'insectes respectivement. Pour les deux années, les abondances relatives totales ont été réparties entre 50,6 % (4002 individus) et 41,3 % (1300 individus) pour les ravageurs, 19,9 % (1577 individus) et 23,4 % (737 individus) pour les utiles et 29,5 % (2331 individus) et 35,3 % (1111 individus) pour les insectes associés. Les familles d'insectes prédominantes étaient, en 2012 et en 2013 respectivement, Aphididae (30,8 % et 21,3 %), Cecidomyiidae (4,9 % et 3,9 %) et Chrysomelidae (3,8 % et 0,3 %) pour les ravageurs, Dolichopodidae (5,3 % et 16,5 %), Staphylinidae (3,0 % et 1,5 %) et Coccinellidae (2,1 % et 0,6 %) pour les utiles, et Muscidae (6,5 % et 18,1 %), Psychodidae (7,7 % et 0,9 %) et Formicidae (4,9 % et 2,0 %) pour les insectes associés. Cette étude est l'une des rares à donner la diversité des insectes nuisibles et utiles dans les périmètres maraîchers de Libreville. Ces résultats permettraient de mettre en place des stratégies de contrôle durable des ravageurs rencontrés.

Abstract

The abundance and diversity of entomofauna was evaluated in three urban gardens of Gabon, i.e. the localities of Libreville’s airport (ADL), PK8 and Owendo. Insects were pan-trapped and visual observations were done on plants in July and August 2012 and 2013. Samples were collected weekly, insects were identified at the family level and classified into three categories: pests, beneficials and associated (i.e. other families). Eight orders and 84 families were recorded with 7910 and 3148 individuals of insects, were sampled in 2012 and 2013, respectively. Insect abundance on roselle (Hibiscus sabdariffa L. 1753; Malvaceae) was significantly higher in ADL than in PK8 and Owendo, while amaranth (Amaranthushybridus L. 1753; Amaranthaceae), tomato (Lycopersicon esculentum Mill. 1768; Solanaceae) and cabbage (Brassica oleracea L. 1753; Brassicaceae) showed similar insect abundance in PK8 and Owendo. In 2012, 29.6 %, 31.4 % and 38.9 % of insects were recorded in ADL, PK8 and Owendo respectively. In 2013, only ADL and PK8 were sampled, with respective abundance of 61.7 % and 38.3 % of insects respectively. For both years, the global relative abundances were distributed between 50.6 % (4002 individuals) and 41.3 % (1300 individuals) for pests, 19.9 % (1577 individuals) and 23.4 % (737 individuals) for beneficials, and 29.5 % (2331 individuals) and 35.3 % (1111 individuals) for associated insects. The predominant insect families were, in 2012 and 2013 respectively, Aphididae (30.8 % and 21.3 %), Cecidomyiidae (4.9 % and 3.9 %) and Chrysomelidae (3.8 % and 0.3 %) for pests, Dolichopodidae (5.3 % and 16.5 %), Staphylinidae (3.0 % and 1.5 %), and Coccinellidae (2.1 % and 0.6 %) for beneficials, and Muscidae (6.5 % and 18.1 %), Psychodidae (7.7 % and 0.9 %) and Formicidae (4.9 % and 2.0 %) for associated insects. This study is one the few exploring the composition of insects within Libreville’s urban gardens. The results provide knowledge to be used for developing pest management strategies and enhancing other ecosystem services in these localities of Gabon.

Table des matières

Introduction

1In Gabon, peoples living in urban areas represented 87 % of total population (FAO, 2017), and corresponding to food requirements that are mainly dependent on food imports (Organisation Mondiale du Commerce, 2013). Practicing urban and peri-urban agriculture was instigated by the Institut Gabonais d’Appui au Développement (IGAD) in the last twenty years. Many vegetable species (e.g. amaranth, tomato, lettuce, cabbage, roselle, okra, african nightshade) and aromatic plants (e.g. basil, persil, celery) are cultivated. However, pests and diseases cause significant damaged and losses. The control methods are based on systematic applications of chemical pesticides (Bayendi Loudit et al., 2017).

2Studies investigating insect pests occurring on crops are rare in Gabon, to our knowledge. Previous studies showed that many insect pests in Gabon belong to Chrysomelidae, Noctuidae, Pyralidae, Pluttelidae and Thripidae families (Bordat & Arvanitakis, 2004). On fruit trees and vegetable crops of home gardens of the Haut-Ogooué province, the major pests belong to Aphididae, Cecidomyiidae, Cicadellidae and Crambidae families (Poligui et al., 2014). A similar study performed on insect diversity (i.e. pests and natural enemies) was conducted in Yaoundé, Cameroon, in the main crops from nine plant families, namely Solanaceae, Malvaceae, Tiliaceae, Amaranthaceae, Fabaceae, Apiaceae, Lamiaceae, Asteraceae and Cucurbitaceae (Djiéto-Lordon et al., 2007).

3In Gabonese localities of Libreville and Owendo, vegetable crops grown are mainly amaranth (Amaranthus hybridus L. 1753; Amaranthaceae), lettuce (Lactuca sativa L. 1753; Asteraceae), roselle (Hibiscus sabdariffa L.1753; Malvaceae), african nightshade (Solanum nigrum L.1753; Solanaceae) and tomato (Lycopersicon esculentum L. 1768; Solanaceae) (Bayendi Loudit et al., 2017). The main insect pests occurring on these crops are aphids (Hemiptera: Aphididae) and chrysomelids (Coleoptera: Chrysomelidae), usually controlled by spraying conventional insecticides mainly lambda-cyhalothrine (Bayendi Loudit et al., 2017). However, knowledge about the diversity of the entomofauna occurring in these areas remains limited.

4This study aims to improve knowledge of entomofauna in these gabonese crops focusing on the assessment of abundance and diversity of insects from three urban gardens. This work was designed to classify the collected insects into pests, beneficials and associated. The understanding of insect pest and natural enemie occurrence and interactions would enable the setup of further integrated pest management in Libreville and Owendo.

Material and Methods

Study area and sites

5The study was conducted in market gardens during two successive years in July and August 2012 and 2013. In Libreville, the first location was at proximity of Libreville’s airport (ADL) (0°27'30.46" N; 9°25'6.30" E; E: 10 m above sea level) and the second was PK8 (0°24'39.89"N; 9°29'26.23"E; E: 20 m above sea level). The third location was situated at Owendo (0°18'26.86" N; 9°29'40.83" E; E: 10 m above sea level). The vegetable farmers from these sites benefit from a technical advices of IGAD.

Sampling data

6Yellow pan traps (Flora®, 27 cm diameter and 10 cm depth) were placed in each vegetable species per sites according to the topography and availability of the crops grown by farmers. Each trap contains water with few drops of liquid soap (weekly changed) and fixed on a cane. Three traps were installed within each crop plot, and visited during five weeks, ensuring weekly trapping during this period. Visual observations were conducted in addition on three (3) plants per plots weekly on the same day of the week, to have a better vision of insects diversity. In 2012, four plots were investigated per site for amaranth and roselle, corresponding to 12 traps per crops. In same year, tomato plots were similarly visited at Owendo while five plots at PK8 were followed as for cabbage (five plots in PK8). In 2013, every crop was observed from three plots within all sites. The difference in number of plot replicates depended on the crop availability set by farmers.

7All insects were then transferred into 70 % ethanol, according to the method previously described by Duviard & Roth (1973). The insects (collected by traps) were counted and systematically classified on the basis of exterior morphology, until the family taxon (Hutcheson & Jones, 1999). Insect families were identified using keys (Delvare & Aberlenc, 1989; Chinery, 1993, 2007; Picker et al., 2002). At laboratory, identifications were performed by using a stereomicroscopic magnifying glass (euromex nexius zoom). Insects were tidied up by categories: crop pests, beneficials for agriculture and associated ones.

Statistical analysis

8For all analyses, the total of insect (trapped and observed) per culture, per site and per year were used. Data analyses were performed with R 3.3.1 software (R Core Team, 2016). Comparisons of insect families per crop and locality were assessed using two-way analysis of variance (ANOVA, P < 0.05). In addition, Tukey test was conducted for comparing insect families per locality. Before this parametric test, residual deviance was checked (P > 0.05).

9Abundance and diversity of the major pests from traps were compared following method used Shannon index (1) and its related Evenness Index (2) were calculated as (Magurran, 2004):

(1) (2) with pi= ni/N ; ni= the abundance of the ith species; S = the total number of species and N = the total abundance.

Results

Crop species

10The monitoring of the three urban gardens allowed to record 22 species of current crops (Table 1). The most important crops were amaranth, lettuce, roselle,cabbage and tomato.

11Among these various plant species, only four were selected as main crops for monitoring insects, namely amaranth, cabbage, roselle and tomato, according to the growing duration and area importance.

Insect abundance

12Global insect abundances per site and year

13In 2012, insect abundances were relatively similar between ADL (2344 individuals) and PK8 (2484 individuals), while it was higher in Owendo (3082 individuals). In 2013, insect abundance was the highest in ADL (1942 individuals) compared to PK8 (1206 individuals). The results indicate that insect abundance varied according to sites and years.

14Both 2012 and 2013 years provided respective global insect abundances of 7910 and 3148 individuals, with rates of 50.6 % to 41.3 %, 19.9 % to 23.4 % and 29.5 % to 35.3 % for pests, beneficials and associated entomofauna respectively (Figure 1).

15Insect abundances according to major families

16The entomofauna monitoring revealed 84 families within the three main categories, namely pests (31 families), beneficials (26 families) and associated insects (27 families) (Table 2).

17Table 1: Plant diversity in garden markets of Libreville’s airport, PK8 and Owendo.

18The relative abundances were represented according to previous four main crops (amaranth, roselle, tomato and cabbage). Pest predominant families, in 2012 and 2013 respectively, were Aphididae (2436 and 707 individuals), Cecidomyiidae (391 and 123 individuals), Chrysomelidae (300 in 2012 only), Cicadellidae respectively, predominant families were Dolichopodidae (with 417 and 520 individuals), Staphylinidae (234 and 48 individuals), Coccinellidae (166 and 18 individuals), and Pteromalidae (160 and 29 insects). Associated five major families, in 2012 and 2013 respectively, were Muscidae (512 and 570 individuals),

19Psychodidae (612 and 28 insects), Formicidaewinged insect only (384 and 64 insects), Calliphoridae (60 and 254 insects) and Anthomyiidae (314 and 36 insects). In addition to these major families, there were 54 other and minor families, respectively 21 for pests, 17 for beneficials and 16 for associated.

20Figure 1:Total insect prevalence according to their categories in 2012 and 2013

Table 2: Main insect families and their relate abundance per location and selected crop species.Main families related to abundances

21The most abundant pest families in 2012 and 2013 were Aphididae (30.8 % and 21.3 %), Cecidomyiidae (4.9 % and 3.9 %), Chrysomelidae (3.8 % and 0.3 %), Cicadellidae (1.7 % and 2.5 %) and Delphacidae (1.8 %). The most abundant beneficial families in both years were Dolichopodidae (5.3 % and 16.5 %), Staphylinidae (3.0 % and 1.5 %), Coccinellidae (2.1 % and 0.6 %) and Pteromalidae (2.0 % and 0.9 %). The predominant associated families in both years were Muscidae (6.5 % and 18.1 %), Psychodidae (7.7 % and 0.9 %), Formicidae (4.9 % and 2.0 %), Calliphoridae (0.8 % and 8.1 %) and Anthomyiidae (4.0 % and 1.1 %).

22Insect abundance per crops and alimentary categories

23Insect abundance on roselle (H. sabdariffa) was significantly higher in ADL site than in PK8 and Owendo sites, while amaranth, tomato (L. esculentum) and cabbage (B. oleracea) showed close (p  0.05) insect abundance in PK8 and Owendo (Figure 2). Excepted for ADL where pests were only dominant on roselle, in PK8 and Owendo, pests were dominant on all crops, followed by associated insects.

24Figure 2:Insect categories abundance per crops (means ±SE) and year according to sites.

25Table 3:Distribution of insect diversity (expressed in family number) according to crops and localities.

Entomofauna diversity

26Insect diversity (taxon family) according to crops and sites

27Insect family abundances differed significantly between localities (χ² = 18.1961, P < 0.05). There was a highly significant difference between the insect families in Owendo and ADL (P < 0.001) and a significant difference between PK8 and ADL (P < 0.05). There was no significant difference of insect families within crops (P > 0.05) during both years. Nevertheless, comparing sampling years, 2012 allowed to record a higher number of families (77) than 2013 (60) (Table 3).

28Insect family occurrence per crop during both years

29Only ADL and PK8 sites were sampled for both years 2012 and 2013. Monitoring in Owendo was performed in 2012, Common families were more numerous on amaranth (26) and roselle (30) in ADL site

30(Figure 3). In PK8, tomato and amaranth provided a lower number of common families (23). Comparing both years, there was a higher number of insect families in 2012 than in 2013, respectively on amaranth in ADL (17 in 2012 against 6 in 2013) and PK8 (26 in 2012 against 10 in 2013) (Figure 3). On roselle, the insect family number appears to be lower in 2012 (9 against 15 for 2013). On tomato, there was the same number of families (24) for common as for insect families caught in 2012, while only 11 exclusive families were caught in 2013 (Figure 3).

31Figure 3:Insect diversity occurrence within sampled sites and crops.

32Insect diversity index within sites and years

33The Shannon index calculation showed that the diversity level depended on the insect categories, on their sites and the trapping year (Figure 4). Pests, beneficials and associated insects recorded lower rates of diversity in 2012 in ADL site. However, diversity rate was relatively similar between insect pests from ADL (in 2013) and PK8 (in 2012 and 2013). Owendo recorded the highest level of insect pest diversity (2012). Shannon evenness of pests was weak in ADL and PK8, but high in Owendo. Then, there was a balance of insect pest family distribution within both sites and years. In Owendo, the evenness is high because there was predominance occurrence of three families, namely Aphididae, Cecidomyiidae and Chrysomelidae. The Evenness was high for both beneficial and associated insects during both years, indicating a balance between the few families occurring in these sites.

34Insect diversity within crops

35Regarding crops, similar diversity level was found on amaranth between sites, with the highest levels in 2012. On cabbage, a similar diversity level was also observed between PK8 and Owendo. On roselle, higher diversity was obtained from Owendo while it was the low at ADL.

36Globally, in both 2012 and 2013, the Evenness corresponding to the highest diversity rate varied from 0.65 and 0.83, indicating that there was a group of dominant insect families occurring in these sites.

Discussion

37Our study gave preliminary results of insect diversity in vegetables produced in peri-urban area in Libreville and Owendo. In the two towns, about 22 plant families are cultivated within the peri-urban area. Most of crop families cultivated like Malvaceae, Amaranthaceae, Basellaceae and Tiliaceae are described as African indigenous vegetables (Shackleton et al., 2009). In our knowledge no previous inventories about insect pests were known for each of these crops in Gabon. This research was done with the farmer conditions, meaning that we did not manage the plant sowing but only used existing plots for visual observations and insect trapping in the fields. Then, our results depends on the crop accessibility/availability in the investigated areas. During the two years, the most important crops were amaranth, tomato, cabbage and roselle.

38In 2013, the insects collected were 2.5 times more abundant than the ones counted in 2012. The difference between insect abundance in the two years was due to the closure of the Owendo site and the number of traps. That site was closed for political reasons in relation to terrestrial management. In addition, some farmers thought that our presence on the sites was due to a governmental control and used pesticides to protect crops.

39Whatever the considered site or crop, the pests were more important than associated and beneficial insects. The result of the present study showed that the most important pest were aphids that are polyphagous and caused many damages on plants. Most of this pest are vectors of phytoviruses (Blackman & the late Eastop, 2017). This results confirmed Djiéto-Lordon et al., (2007) study where aphids were also the most abundant pests on Solanaceae, Malvaceae, Amaranthaceae, Fabaceae, Lamiaceae and Curcurbitaceae cultures. Although Chrysomelidae insects were not very abundant, several damages (holes on the leaves) were observed essentially on roselle crop.

40For beneficial insects Dolichopodidae was the most important for both years. For these insects, adult and larval stages are predatory. Nevertheless, the preys used by both stages are notably different : the adults are predatory on small, soft-bodied insects and mites, and the larvae are probably all carnivorous (Hagen et al., 1999). Also, Coccinellidae and Ichneumonidae were found both in Gamba (Gabon) forest and gardens (Basset et al., 2008).

41This work constituted a first inventory of crop and insect family diversities in the garden market in Libreville and Owendo. Further study should be performed to determine more accurately the different insect species and their importance in agriculture.

42Figure 4:Comparison of Shannon Index diversity and Eveness within sampled sites and crops.

43ACKNOWLEDGMENTS

44We thank farmers of Institut Gabonais d’Appui au Développement (IGAD) for access in the fields, the personal of IGAD (Nzegho Charles, Edou Edou Germain, Edzang Jean Jacques), the staff of Institut de Recherches Agronomiques et Forestières (IRAF) especially Andeime Eyene Myrianne Flore, Abaga Obiang Ernest, Mbeng Hendrix, Koudaou Gervais for experiment help and Fabre Anguilet Edgard for statistical analyses help. We also thank Severin Hatt (Entomologie fonctionnelle et évolutive) for reading manuscript.

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