1 - Fruitteeltnieuws 12 - 12 juni 2015

Aphids and their parasitoids in fruit 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

Fruit tree orchards attract many kinds of insect pests that damage vegetation and fruit.

Aphids are among the most serious pests that attacking fruit trees in Belgium, of which they

are generating severe economic damage through direct feeding, honeydew producing and

virus spreading. These aphids have fortunately insect enemies of their own. Growers can

provide safe habitat for beneficial insects as part of an integrated pest management (IPM)

strategy that reduces the need for pesticides.

Problems related to honeydew production by aphids

- Encouraging the growth of black sooty mould.

- Attracting ants that play an important role in structuring aphid communities and

protecting them against natural enemies (reduce the efficiency of biological

control) and addition to helping in spreading disease in fruit tree orchard during

their movement from soil to the tree and between trees.

- Blocking out the light it needs affecting by the on the photosynthesis process in

leaves and the tree health in general.

Why this study?

The lack of information about diversity of parasitoid wasps associated with aphids in

fruit orchards in Belgium, in addition to the economic importance of fruit tree crops, lead us

to realize this study. Data obtained from this study could be used in developing and subsequently

evaluating integrated management strategies for aphid pests. Data availability on tritrophic

associations is considered as the key element when we want to develop biological control

strategy against aphids, as well as to provide the background information about their host

range patterns. Our field observations were weekly carried-out in apple, pear and cherry

orchards of Sint-Truiden region (pcfruit, Bernissem, Wilderen-Staain, Bevingen, Gingelom)

from June and October 2014. The potential importance of alternative habitats of aphid

parasitoids lead us also to monitor flora growing naturally in or adjacent of fruit tree crops.

mailto:ammar.alhmedi@pcfruit.bemailto:tim.belien@pcfruit.be

2 - Fruitteeltnieuws 12 - 12 juni 2015

What were aphid species observed attacking fruit trees?

In 2014 season, 11 aphid species belonging to different genera were observed on fruit

trees, presented mainly by the rosy apple aphid, Dysaphis plantaginea (Fig. 1A), woolly apple

aphid Eriosoma lanigerum (Fig. 1B), green apple aphid Aphis pomi (Fig. 1C), on apple, and

black cherry aphid Myzus cerasi (Fig. 1D) on cherry. Pear trees remarkably seemed to be less

vulnerable for aphid attacks and their relative damages. Those aphids were subject to attack

by a wide range of natural enemies, including parasitoid wasps, predators and pathogens. We

focused in the present study on the parasitoid fauna.

Figure 1. Aphids: A: Rosy apple aphid, B: Woolly apple aphid, C: Green apple aphid, D: Black

cherry aphid

Aphid parasitoids (parasitic wasps), which are considered as one of the most important

natural enemies against aphid pests in agricultural system, include aphelinid (Fig. 2a) and

braconid (Fig. 2b) wasps. Parasitoid female lays eggs (Fig. 2a, b) into aphids; the eggs hatch

into larvae that consume the internal contents. Eventually, the larva pupates and becomes an

adult, which chews out an emergence hole. Parasitized aphids are characteristically swollen,

brown, gray to black, and are called mummies (Fig. 2c). During the 2014 season, 15 aphid

parasitoids belonging to 8 genera were recorded attacking aphids (but not all aphid species)

A B

C D

3 - Fruitteeltnieuws 12 - 12 juni 2015

in apple, pear, and cherry trees (Table 1). Among the collected parasitoid species, 4 species

(Aphelinus mali, Ephedrus persicae, Ephedrus plagiator and Binodoxys angelicae) seemed to be

important biocontrol agents for fruit tree orchards on the basis of their abundance in our samples

and knowledge of their and biology. The rosy apple aphid D. plantaginea hosted more parasitoids

species (8 species) than other aphids observed on fruit tree crops. We, surprisingly for the first time,

detected D. plantaginea as a host aphid of Toxares deltiger in European orchards, this founding

related to vegi orchards of pcfruit.

Figure 2. Parasitic wasps on aphids

Potential solutions have to offer more for both your health and the health of your orchard

In optimal conditions, natural enemies can maintain aphid numbers below thresholds

for causing plant damage so that an insecticide application is not warranted. The use of

conventional insecticides to control aphids may not only kill their natural enemies but also

significantly impact those of other plant-feeding pests, such as two-spotted spider mites. As a

result, spider mites may become a bigger problem than the aphids. This type of phenomenon

is referred to as secondary pest outbreak.

Beneficial fauna is however actually threatened by human-induced habitat alteration, e.g. the

agricultural intensification and the pesticide application. Therefore, in the context of natural aphid

control, to have an efficient and sustainable management for aphids, a diversification through

habitat manipulation can be useful to create an appropriate ecological infrastructure offering

suitable foods for aphid natural enemies, alternative prey or hosts, and shelter from adverse

conditions. Growers can help in this context by providing safe habitat, borders or stripes

occupied by beneficial weeds, shrubs and trees, for beneficial insects, as part of IPM strategy

that reduces the need for pesticides.

Certain weeds are in fact already known as important components in the agro-

ecosystems because they positively affect the biology and dynamics of beneficial insects (e.g.,

a b c

4 - Fruitteeltnieuws 12 - 12 juni 2015

Miliczky and Horton 2005, Alhmedi et al. 2011, Alignier et al. 2014). Based on the above-

mentioned facts, we observed the distribution and relative abundance of aphids and their

parasitoids on the associated flora (weeds, shrubs and trees) naturally grown in or adjacent to

fruit orchards, in order to evaluate their potential role for enhancing biological control against

orchard aphids. On 29 non-crop plants, associated with aphids and parasitoids, growing

naturally in or adjacent to orchards, 23 aphid species associated with 24 parasitoid species

were sampled, from which 7 parasitoid species share aphid hosts from orchard trees and associated

uncultivated plants (Table 2, Fig. 3). Among the common collected parasitoid species, 4 species

(Ephedrus plagiator, Aphidius matricariae, Aphidius ervi and Praon abjectum) seemed to be

important biocontrol agents for fruit tree orchards on the basis of their abundance in our samples.

Capsella bursa-pastoris, Bellis perennis, Sonchus asper and Senecio vulagris were potentially

seemed to be important as banker for parasitoids, such as Ephedrus persicae, Ephedrus

plagiator, Praon abjectum and Aphidius matricariae, which can attack aphid pests on fruit tree

crops.

Table 1. Association of aphids and their parasitoids on fruit tree crops (apple, pear and cherry)

Host Plants / Aphids Parasitoid wasps

Malus domestica

Eriosoma lanigerum Aphelinus mali Dysaphis plantaginea Ephedrus persicae, Ephedrus plagiator, Binodoxys angelicae,

Praon abjectum, Toxares deltiger, Lipolexis gracilis, Diaeretiella rapae, Aphidius ervi

Aphis pomi Ephedrus persicae, Ephedrus plagiator Healthy aphids : Aphis spiraecola, Macrosiphum euphorbiae, Dysaphis devecta, Rhopalosiphum insertum

Prunus avium

Myzus cerasi Ephedrus persicae , Aphidius matricariae, Binodoxys angelicae

Healthy aphids : Myzus lythri

Pyrus communis

Macrosiphum euphorbiae Praon volucre Healthy aphids : Macrosiphum rosae, Aphis spiraecola, Aphis pomi, Melanahpis pyraria Rhopalosiphum insertum

5 - Fruitteeltnieuws 12 - 12 juni 2015

Table 2. Association of aphids and their parasitoids on non-crop flora grown naturally in or adjacent

to fruit orchards (apple, pear and cherry)

Host Plants / Aphids Parasitoid wasps

Artimisia vulgaris

Macrosiphoniella oblonga Aphidius absinthii, Aphidius phalangomyzi

Bellis perennis

Macrosiphum euphorbiae Aphidius matricariae, Aphidius ervi

Myzus persicae Aphidius matricariae

Aulacorthum solani Aphidius matricariae

Capsella bursa-pastoris

Lipaphis erysimi Ephedrus plagiator

Myzus persicae Aphidius matricariae, Ephedrus plagiator

Chenopodium album

Macrosiphum euphorbiae Praon volucre, Aphidius ervi

Cirsium arvense

Aphis fabae Lysiphlebus fabarum, Aphelinus sp.

Uroleucon cirsii Aphidius funebris

Capitophorus horni Aphidius matricariae

Crataegus monogyna

Aphis pomi Binodoxys angelicae

Eupatrium cannabinum

Macrosiphum euphorbiae Aphidius ervi

Galinosa quadriradiata

Aphis fabae Lysiphlebus fabarum

Tripleurospermum inodorum Brachycaudus cardui Lysiphlebus brachycaudi, Aphidius matricariae, Ephedrus plagiator

Myzus persicae Aphidius matricariae, Ephedrus plagiator

Medicago lupulina

Acyrthosiphon pisum Aphidius ervi

Phalaris arundinacea

Hyalopterus pruni Ephedrus plagtiator, Praon volucre, Praon abjectum

Plantago lanceolata

Aulacorhtum solani Aphidius ervi

Dysaphis plantaginea Aphidius ervi

Poa annua Sitobion avenae Aphidius rhopalosiphi, Aphidius uzbekistanicus, Aphidius avenae,

Aphidius ervi, Ephedrus plagiator Ribes rubrum

Cryptomyzus ribis Aphidius ribis

Rosa canina

Macrosiphum rosae Aphidius rosae

Rumex obtusifolius

Aphis rumicis Aphidius uzbekistanicus

Rubus idaeus

Amphorophora idaei Aphidius urticae

6 - Fruitteeltnieuws 12 - 12 juni 2015

Table 2. Continued.

Host Plants / Aphids Parasitoid wasps

Senecio vulgaris Brachycaudus cardui Lysiphlebus brachycaudi, Lysiphlebus fabarum, Ephedrus plagiator,

Aphidius smithi, Aphidius matricariae, Aphidius sp., Ephedrus persicae

Myzus persicae Aphidius matricariae, Ephedrus plagiator, Lysiphlebus fabarum, Ephedrus persicae

Macrosiphum euphorbiae Praon volucre, Praon gallicum

Solanum nigrum

Aulacorthum solani Praon volucre

Sonchus arvensis

Uroleucon sonchi Aphidius sonchi

Hypermyzus lactucae Praon abjectum

Sonchus asper

Uroleucon sonchi Aphidius sonchi, Aphidius funebris, Praon yomenae

Hypermyzus lactucae Praon abjectum, Aphidius sonchi

Aphis fabae Praon abjectum

Sonchus oleraceus

Uroleucon sonchi Aphidius funebris

Hypermyzus lactucae Aphidius funebris

Tanacetum vulgare Macrosiphoniella millefolii Aphidius urticae

Aphidius ervi

Trifolium pratense

Acyrthosiphon pisum Aphidius urticae

Trifolium repens

Acyrthosiphon pisum Aphidius ervi, Aphidius eadyi

Macrosiphum euphorbiae Aphidius ervi

Myzus persicae Lysiphlebus fabarum

Urtica dioica Microlophium carnosum Aphidius microlophii, Aphidius ervi, Aphidius urticae, Aphidius

funebris Urtica urens

Microlophium carnosum Aphidius microlophii

Vicia hirsute Acyrthosiphon pisum Aphidius ervi

Vaccinium corymbosum Macrosiphum euphorbiae Praon voulcre

7 - Fruitteeltnieuws 12 - 12 juni 2015

Figure 3. Diagrams of common parasitoids and host aphids occurred on fruit tree crops and associated flora.

Aphelinus mali

Eriosoma lanigerum

Malus domestica

Ephedrus persicae

Dysaphis plantaginea

Malus domestica

Aphis pomi Myzus cerasi

Prunus avium

Brachycaudus cardui

Senecio vulgaris

Myzus persicae

Ephedrus plagiator

Dysaphis plantaginea

Malus domestica

Aphis pomi

Hyalopterus pruni

Phalaris arundinacea

Sitobion avenae

Poa annua

Myzus persicae

Lipaphis erysimi

Capsella bursa-pastoris

Brachycaudus cardui

Senecio vulgaris

Myzus persicae

Matricariae maritima

8 - Fruitteeltnieuws 12 - 12 juni 2015

Conclusion

There are in fact several advantages to encouraging beneficial insects to inhabit our

orchards. Less time and money are spent controlling pests because the beneficials are doing

the work for you. You don’t need to worry about pesticide resistance or environmental

pollution. It is unrealistic and unwise to strive for a weed-free and insect-free orchard. The

presence of natural enemies provides free aphid control, so before spraying with an

insecticide, check to be sure that existing natural enemies are not already taking care of

business. The results of the present study improve our knowledge about aphids and their

parasitoids in apple, pear and cherry orchards including the associated flora in orchards.

Further studies on the relationships between aphids and their parasitoids according to

landscape management are needed to improve biological control strategies against aphid

pests. Further work on preferential behaviour and chemical ecology of biocontrol candidates is also

needed to achieve efficient program of control against aphids.

Acknowledgments

This research is part of the BIOCOMES project in which pcfruit (Department of Zoology)

cooperates with the partners Viridaxis and the Zoological Institute of the University of Belgrade

(Serbia), and has received funding from the European project BIOCOMES (WP10, Grant

Agreement number: 612713).

References

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, 103–112.

Alignier A, Raymond L, Deconchat M, Menozzi P, Monteil C, Sarthou J-P, Vialatte A, Ouin A (2014) The effect of semi-natural habitats on aphids and their natural enemies across spatial and temporal scales. Biological control, 77, 76–82.

Miliczky ER, Horton DR (2005) Densities of beneficial arthropods within pear and apple orchards affected by distance from adjacent native habitat and association of natural enemies with extra-orchard host plants. Biological Control, 33, 249–259.