Indirect competition in aphid community and biological control: Towards a new approach of aphid management in apple orchards

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1 1 - Fruitteeltnieuws juni 2016 Indirect competition in aphid community and biological control: Towards a new approach of aphid management in apple orchards Ammar Alhmedi & Tim Beliën Pcfruit vzw, Department of Zoology, Fruittuinweg 1, 3800 Sint-Truiden, Belgium For more info contact: ammar.alhmedi@pcfruit.be or tim.belien@pcfruit.be In conventional biological aphid control in its simplest form only direct interactions between the control agent and the aphid are considered. There is however increasing more than ever of evidences amassed by Ecologists for the structural importance of indirect interactions in insect communities. Hence, aphid communities could be structured by this type of interaction called also "apparent competition" where the species interact through shared natural enemies. Indirect impacts among aphids are the effects of one species on another mediated by at least one intermediate common natural enemy. Promising prospect for apple aphid management Aphids have many natural enemies, called also beneficials, including parasitic wasps, predators and entomopathogens. Beneficial complex which is a natural boon to growers can be disrupted by insecticides applied against other pests. Efficient natural enemy management well help us to control aphids and provide safe food products. Benefit from the indirect competition among aphids that share common natural enemies could be promising approach for aphid management strategies in apple orchard (Alhmedi et al. 2011). In fact, two species of aphids that feed different resources and that do not interact directly can still influence each other's population growth rates if they share natural enemies such as predators or parasitoids or others. If one species increases in abundance, the density of the shared natural enemy may also increase in density and in consequence the second species will suffer higher mortality. Two types of apparent competition may influence herbivore population densities. The first is a short-term apparent competition which occurs when the asymmetric interaction is prevalent, whereas the long-term type occurs when the result of such competition between species is highly symmetric. Aphid community structure and quantitative food web In apple orchards, aphids are common and more 50 species are already recorded worldwide, 9 species were detected in the present work, mainly Eriosoma lanigerum, Dysaphis plantaginea

2 2 - Fruitteeltnieuws juni 2016 and Aphis pomi (Figure 1). Apple aphids are implicated in a suite of problems ranging from feeding on all tree parts, secreting honeydew to acting as virus vectors, hence reducing crop yield that have significant economic consequences. We illustrated in the present work the construction of a quantitative food web and apparent competition using our work data on aphid and parasitoid communities collected in apple orchards including the associated flora of Sint-Truiden region (Limburg, Belgium) during growing seasons. The associated flora involved woody and herbaceous plants and other fruit trees grown in or adjacent to apple orchards. We discuss how apple aphids may be structured by indirect effects of associated flora aphids. In drawing quantitative food webs (Figure 1, 2) we used the same conventions as in the work of Müller et al. (1999). Parasitoids and aphid hosts are arranged as a series of bars; the width of each bar proportional to the cumulative abundance over the study period. Parasitoids and aphids are linked by triangular wedges; the relative width of each represents the relative strength of the plant-aphid-parasitoid interaction. The code numbers for the included species are listed in Table 1. Parasitoid density (scale : host x 59) Aphis pomi Dysaphis plantaginea Total host aphids per 10 plant units : Eriosoma lanigerum Figure 1. Summary quantitative apple aphid-parasitoid food web. In the top, white bars represent the predominant parasitoid abundance and black bars represent other parasitoids attacked apple aphids; in the bottom, bars represent main apple aphid abundance. The lengths of the edges in links between aphid-parasitoid species illustrate the relative strengths of the interactions between each trophic association

3 3 - Fruitteeltnieuws juni 2016 Aphelinus mali Parasitoid density (scal : host x 189) Binodoxys angelicae Ephedrus persicae Ephedrus plagiator Praon volucre Total aphid density / 10 plant units : Host plant distribution scale : common (large bars), medium (medium bars), low (thin bars) Figure 2. Summary quantitative aphid-parasitoid food web (apple orchard and associated flora). The three series of bars represent host plants (bottom), aphid abundance (middle), and parasitoid abundance (top), drawn at different scales. In the middle bars : green bars represent promising aphids, red bars represent apple aphid pests, black bars represents other aphids less promising than green ones. The lengths of the edges in links between both plant-aphid and aphid-parasitoid species illustrate the relative strengths of the interactions between each trophic association. Aphid community structure and apparent competition In fact we will try to simplify how apple aphids can be managed when they are other no-pest aphids present in the apple orchard and share common parasitoids. We observed in our work many no-pest aphids occur on herbaceous and woody plants grown in or adjacent to apple orchard and many of them share common parasitoids (Figure 2), in addition to other beneficials, with apple aphids. Hence, they can potentially contribute in increasing the local density of apple aphid parasitoids and consequently enhancing the biological aphid control in apple orchard. To evaluate the potential benefit from this type of competition in aphid control, the population dynamic of aphids and their parasitoids in association with host plants should be studied. Regarding apple tree crop, the quantitative data analysis of our weekly monitoring

4 4 - Fruitteeltnieuws juni 2016 effectuated during 2014 and 2015 allowed us to better understanding the indirect interaction between friendly and pest aphids mediated by parasitoids. Hence, the potential for indirect effects among those aphids in apple orchards was evaluated. The potential of indirect effects resulting from aphid competition mediated by parasitoids was assessed by quantitative overlap diagrams (Figure 3) and quantitative measure. Different host aphid species are linked using the quantitative measure (apparent competition) d ij, representing the probability that a parasitoid attacking aphid species i develops on aphid species j. The quantitative index d ij for each pair of aphid species was overall calculated as :, where α ik is the absolute density of the trophic link between aphid i and parasitoid k (and, hence, the summations in k and l are over all parasitoids and in m over all aphid hosts). This measure ranges from 0 to 1 and reaches the maximum 1 when all parasitoid individuals fed on the same aphid species. The woolly apple aphid Eriosoma lanigerum This problematic aphid hasn t shared any parasitoids with other aphids; its populations were only attacked by the specific parasitoid Aphelinus mali. Consequently the apparent competition extent mediated by parasitoids between E. lanigerum and other aphids is 0 (Figure 3). The rosy apple aphid Dysaphis plantaginea Many aphids occurring on both herbaceous plants and fruit trees have shared efficient parasitoids, Aphidius ervi, Binodoxys angelicae, Ephedrus persicae, E. plagiator with the rosy apple aphid D. plantaginea (Table 2, Figure 1), specially the black bean aphid Aphis fabae, the leaf-curling plum aphid Brachycaudus helichrysi and the black cherry aphid Myzus cerasi (Table 2, Figure 3). Regarding the value of apparent competition (Table 2) and the seasonal occurrence in the orchard, B. helichrysi and M. cerasi can potentially provide promising approach for managing the population of the rosy apple aphid in apple orchard.

5 5 - Fruitteeltnieuws juni 2016 Brachycaudus cardui (7) Aulacorthum solani (6) Aphis sp. (5) Aphis pomi (4) Aphis grossulariae (3) Brachycaudus helichrysi (8) Aphis fabae (2) Dysaphis plantaginea (9) Aphis epilobiaria (1) Eriosoma lanigerum (10) Hyalopterus pruni (11) Macrosiphum rosae (12) Myzus cerasi (13) Rhopalosiuphum padi (16) Rhopalosiphum insertum (15) Phorodon humuli (14) Figure 3. Quantitative parasitoid overlap diagram. The vertices represent aphid species; white circle sizes indicate the relative size of aphid species population; black circle sizes indicate the contribution of the aphid species as a source of its own parasitoids. Polygons between aphid species denote shared parasitoid interaction strength, where the width of the link to each species represents the potential effect derived from another aphid species as a source of parasitoids. The green apple aphid Aphis pomi This is aphid was widely distributed in apple orchards mainly in 2015 growing season. Six parasitoids attacked green apple aphid were identified, mainly Ephedrus persicae, Binodoxys angelicae and Praon volucre. As the same in the rosy apple aphid case, there many aphids occurring in or adjacent to apple orchard can potentially provide apple orchard parasitoids of A. pomi, mainly A. fabae, B. helichrysi, Hyalopterus pruni and M. cerasi and Aphis epilobiaria (Table 2, Figure 3).

6 6 - Fruitteeltnieuws juni 2016 Table 1. Identity of species in the food webs. Code Plant hosts Code Plant hosts (continue) Code Aphid hosts (continue) 1 Achillea millefolium 24 Rosa canina 9 Dysaphis plantaginea 2 Arctium lappa 25 Rosa sp. 10 Eriosoma lanigerum 3 Beta vulgaris 26 Rubus fruticosus 11 Hyalopterus pruni 4 Capsella bursa-pastoris 27 Rumex obtusifolius 12 Macrosiphum rosae 5 Carduus crispus 28 Senecio inaequidens 13 Myzus cerasi 6 Chenopodium album 29 Senecio vulgaris 14 Phorodon humuli 7 Cirsium arvense 30 Sinapis alba 15 Rhopalosiphum insertum 8 Cirsium vulgare 31 Sonchus asper 16 Rhopalosiphum padi 9 Digitalis purpurea 32 Tanacetum parthenium 10 Epilobium hirsutum 33 Tanacetum vulgare 11 Euonymus europaeus 34 Tripleurosperum maritimum Code Parasitoids 12 Galium aparine 35 Vicia faba 1 Aphelinus mali 13 Helianthus annus 2 Aphidius ervi 14 Leucanthemum vulgare 3 Aphidius urticae 15 Malus domestica Code Aphid hosts 4 Binodoxys angelicae 16 Myosotis arvensis 1 Aphis epilobiaria 5 Diaeretiella rapae 17 Phalaris arundinacea 2 Aphis fabae 6 Ephedrus persicae 18 Phragmites australis 3 Aphis grossulariae 7 Ephedrus plagiator 19 Prunus avium 4 Aphis pomi 8 Lipolexis gracilis 20 Prunus domestica 5 Aphis sp. 9 Lysiphlebus fabarum 21 Prunus padus 6 Aulacorthum solani 10 Praon abjectum 22 Prunus spinosa 7 Brachycaudus cardui 11 Praon volucre 23 Ribes rubrum 8 Brachycaudus helichrysi 12 Toxares deltiger Table 2. Apparent competition extent among apple aphids, A. pomi and D. plantaginea, and other aphids occurring on the associated flora and share common parasitoids. A. pomi D. plantaginea A. pomi D. plantaginea A. epilobiaria A. fabae A. grossulariae A. pomi Aphis sp. A. solani B. cardui B. helichrysi D. plantaginea E. lanigerum H. pruni M. rosae M. cerasi P. humuli R. insertum R. padi

7 7 - Fruitteeltnieuws juni 2016 Conclusion The main motivation behind this study was to compare the potential for apparent competition mediated by aphid parasitoids. The majority of aphids present in our community cannot compete directly because they feed on different host plants. Based to our data analysis, a likely route is that aphid species on different host plants interact through shared parasitoids. Our quantitative analysis of population dynamic offer promise for future studies on the management of apple aphids via the specific orchard management taking in consideration the promising plant-aphid associations as source of efficient natural enemies of aphids. Further semi-field and field approaches aimed to highlight the potential of seasonal benefits of apparent competition on the management of apple aphids Acknowledgments This research is part of the BIOCOMES project and has received funding from the European project BIOCOMES (WP10, Grant Agreement number: ). References Muller CB, Adriaanse ICT, Belshaw R, Godfray HCJ (1999) The structure of an aphid parasitoid community. Journal of Animal Ecology 68, Alhmedi A, Haubruge E, D Hoedt S, Francis F (2011) Quantitative food webs of herbivore and related beneficial community in non crop and crop habitats. Biological Control 58,