Identity of parasitoids and their potential for biocontrol of oilseed rape pests in Europe

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EPPO Workshop on integrated management of insect pests in oilseed rape, Berlin 2017-09-20/22 Identity of parasitoids and their potential for biocontrol of oilseed rape pests in Europe B. Ulber, University of Goettingen, Dept. of Crop Sciences, Agricultural Entomology, Grisebachstrasse 6, D-37077 Goettingen, bulber@gwdg.de T. fulvipes T. perfectus Photo: A. W. Ferguson, UK

Major factors affecting the population dynamics of pest insects on OSR Entomopathogenic fungi and nematodes Predators Parasitods Mortality at hibernation site Coincidence with susceptible crop stage Pest insect Abundance Reproduction Larval mortality - on the plant - on soil surface Adult mortality Climatic factors OSR plant phenology architecture crop density Tillage following OSR Insecticide application

Outline 1. Identity and status of hymenopterous parasitoids of OSR pests 2. Biology, phenology and behaviour of key parasitoids on OSR 3. Percentage parasitism and potential for conservation biocontrol of pests 4. Factors affecting parasitoid efficacy

Management Strategies for European Rape pests Integrated Pest Management Strategies Incorporating Bio-Control for European Oilseed Rape Pests (EU project QLK5-CT-2001-01447, 2001-2006) MASTER project partners: I.H. Williams, A.W. Ferguson (UK), A. Luik, E. Veroman (Estonia), B. Ulber, W. Büchs (Germany), H. Hokkanen, I. Menzler-Hokkanen (Finland), Z. Klukowski (Poland), C. Nilsson (Sweden) T. fulvipes T. perfectus

Key larval parasitoids of stem-mining pests and of pollen beetle on oilseed rape in Europe Target Pest Cabbage stem flea beetle, Psylliodes chrysocephala Rape stem weevil, Ceutorhynchus napi Cabbage stem weevil, Ceutorhynchus pallidactylus Pollen beetle, Meligethes aeneus (syn. Brassicogethes aeneus) Key Parasitoids Tersilochus microgaster (Szépligeti) Tersilochus fulvipes (Gravenhorst) Tersilochus obscurator Aubert Phradis interstitialis (Thomson) Phradis morionellus (Holmgren) Tersilochus heterocerus Thomson Diospilus capito (Nees)

Life history of parasitoids of stem-mining pests and pollen beetle T. obscurator P. interstitialis Photo: A. W. Ferguson, UK T. obscurator T. heterocerus Photo: A. W. Ferguson, UK Diospilus capito Ichneumonidae- Life history: Tersilochinae: univoltine T. microgaster solitary larval T. fulvipes T. obscurator (Hym.; Ichneumonidae-Tersilochinae) koinobiont P. interstitialis P. morionellus univoltine nearly host specific T. heterocerus Life history of Tersilochus spp. endoparasitoids and Phradis spp. Braconidae: solitary larval endoparasitoids koinobiont nearly host specific Diospilus capito Life history: multivoltine solitary larval endoparasitoid koinobiont host specific

Key larval parasitoids of seed weevil and pod midge on oilseed rape in Europe Target Pest Cabbage seed weevil, Ceutorhynchus assimilis (syn. C. obstrictus) Key Parasitoids Trichomalus perfectus (Walker) Stenomalina gracilis (Walker) C. assimilis Mesopolobus morys (Walker) Cabbage pod midge, Dasineura brassicae Platygaster subuliformis (Kieffer) Omphale clypealis (Thomson)

Life history of parasitoids of cabbage seed weevil and cabbage pod midge T. perfectus Photo: A. W. Ferguson, UK P. subuliformis Photo: A. W. Ferguson, UK O. clypealis Photo: A. W. Ferguson, UK Chalcidoidea: Pteromalidae Trichomalus perfectus Mesopolobus morys Stenomalina gracilis Platygastridae Platygaster subuliformis Eulophidae Omphale clypealis Life history larval ectoparasitoids of seed weevil solitary idiobiont multivoltine egg/larval endoparasitoid of pod midge solitary koinobiont multivoltine larval endoparasitoid of pod midge solitary koinobiont multivoltine?

Methods of study 1. Parasitoid activity, phenology and distribution: - emergence traps on previous OSR fields - YWT sampling on new crops of OSR 2. Percentage larval parasitism: - dissection of host larvae under a stereo micrscope - rearing of adult parasitoids from host larvae 3. Identification of parasitoid species: - rearing out of adult parasitoids from host larvae Parasitoid larva T. heterocerus egg Full-grown host larva transfer to soil Pupal cocoon of parasitoid emergence from soil Female parasitoid

Life cycle of pollen beetle Winter March / April May June July August Flight activity Overwintering in soil under leaf litter Invasion and feeding on buds Oviposition into buds; larval development in buds and flowers Pupation in soil Autumn-Winter diapause in litter Excerpt from CETIOM 1985

Life cycle of pollen beetle and its univoltine parasitoids winter March/April May June July Flight activity 20 C PB Pollen beetle: Parasitoid: Parasitoid Overwintering under litter Feeding on buds Emergence from previous year OSR field Oviposition into buds, feeding of larvae in buds/flowers Crop location and oviposition into PB eggs or larvae Full-grown larvae (nonparasitized and paras.) dropping to the ground In soil: parasitoid larva kills prepupa of PB, pupates in silken cocoon; adult wasp hibernates

18 Feb. 28 Feb. 10 March 20 March 30 March 10 April 20 April 30 April 10 May 20 May 30 May 10 June 20 June 30 June 10 July Phenology of tersilochine parasitoids on crops of oilseed rape in relation to the time of flowering 1) 2) 3) T. heterocerus ma T. heterocerus fe P. interstitialis ma P. interstitialis fe T. fulvipes ma T. fulvipes fe T. micro./obsc. ma T. microgaster fe T. obscurator fe ma males; fe - females Period of flowering (Nitzsche, 1998)

Parasitisation behaviour of T. obscurator (video by U. Wyss) Cabbage stem weevil larvae are mining in petioles and stems Tersilochus obscurator for parasitisation, females lay single eggs through the stem tissue into host larvae

Percentage parasitism of insect pests on oilseed rape (data collected from crops of OSR around Göttingen, 1993-2016) Pest Parasitoid Range of parasitism rate Rape stem weevil (Ceutorhynchus napi) Tersilochus fulvipes 0-21 % Cabbage stem weevil (Ceutorhynchus pallidactylus) Tersilochus obscurator 20 50 % Pollen beetle (Meligethes aeneus) Seed pod weevil (Ceutorhynchus assimilis) Phradis interstitialis Phradis morionellus Tersilochus heterocerus Mesopolobus morys Stenomalina gracilis Trichomalus perfectus 45-83 % 30 70 % Stem flea beetle (Psylliodes chrysocephala) Tersilochus microgaster up to 44 %

% parasitism Percentage larval parasitism of M. aeneus in IPM OSR plots in EU countries (2003 2005) 100 80 60 40 20 0 DE EE PL SE UK Levels of parasitism ranging between 4 26% in EE 18 46% in DE and PL 26 80% in SE and the UK (max. 97% in the UK) Data collected by Ulber/DE, Luik/EE, Klukowski/PL, Nilsson/SE, Williams/UK

Species composition of T. heterocerus and Phradis spp. in parasitized pollen beetle larvae collected from 4 regions in Northern Germany 1 2 3 4 1 2 3 4

Percent emergence* of new-generation pollen beetles * Number of emerging beetles as percentage of dropping larvae Level of larval parasitism: 2008: 39.1 42.3 % 2009: 42.2 46.3 % 2010: 70.8 77.3 % Kruskal-Wallis; p < 0.05; n = 4

Emerging new adults / m² Larvae / m² Effect of larval parasitization on the abundance of emerging new generation pollen beetles Conventional Conservation Direct drill Adult emergence rate: 10.5 % 8.0 % 4.8 % (larval parasitism 68-83%) (Ulber & Schierbaum-Schickler, 2005)

Emerging new adults / m² Larvae / m² Effect of larval parasitization on the abundance of emerging new generation pollen beetles Conventional Conservation Direct drill Adult emergence rate: 10.5 % 8.0 % 4.8 % (larval parasitism 68-83%): Adult emergence rate calculated 61.6 % 25.2 % 25.7 % - in absence of parasitism:

% parasitism Percentage larval parasitism of C. obstrictus in IPM OSR plots in EU countries (2003 2005) 100 80 60 40 20 Levels of parasitism ranging between 4 6% in PL 0 46% in EE and SE 57% in the UK (1 exp.) 87 % in DE (1 exp.) 0 DE EE PL SE UK Data collected by Ulber/DE, Luik/EE, Klukowski/PL, Nilsson/SE, Williams/UK

% parasitism Percentage larval parasitism of C. pallidactylus in IPM OSR plots in EU countries (2003 2005) 60 50 40 30 20 10 Levels of parasitism ranging between 5 37% in DE, PL, SE and in the UK up to 57% in SE 0 DE PL SE UK Data collected by Ulber/DE, Klukowski/PL, Nilsson/SE, Williams/UK

% parasitism Percentage larval parasitism of P. chrysocephala in IPM OSR plots in EU countries (2003 2005) 60 50 40 30 20 10 Levels of parasitism ranging between 0 57 % in DE and SE 11 % in the UK (in 1 exp.) 0 DE SE UK Data collected by Ulber/DE, Nilsson/SE, Williams/UK

% of parasitised larvae Superparasitism of P. chrysocephala by T. microgaster Total number of host larvae = 352 (Goettingen, 15 April 2002) 30 20 Encapsulated eggs of T. microgaster 10 * 0 1+0* 1+1 1+2 1+3 1+4 0+1 0+2 0+3 0+4 >0+4 * non-encapsulated parasitoid eggs and larvae + encapsulated parasitoids

4. Some factors affecting parasitoid efficacy Spatio-temporal synchronisation between insect pests and their parasitoids (e.g. Ferguson et al., 2003, 2004; Johnen et al., 2010) Plant species and plant phenology (e.g. Veromann et al. 2006; Kaasik et al., 2014) Crop management: Insecticide application (e.g. Ulber et al., 2010; Jansen & San Martin y Gomez, 2014) Post-harvest soil tillage (e.g. Nitzsche 1998; Nilsson, 2010) Plant density / Plant architecture (e.g. Ulber et al., 2010) Field margins / banker plants (e.g. Barari et al., 2004) Landscape effects (e.g. Thies & Tscharntke, 2010; Zaller et al., 2009; Rusch et al., 2010; 2011)

18 Feb. 28 Feb. 10 March 20 March 30 March 10 April 20 April 30 April 10 May 20 May 30 May 10 June 20 June 30 June 10 July Activity period of tersilochine parasitoids on crops of oilseed rape in relation to insecticide treatment (1997) 1) 2) 3) T. heterocerus ma T. heterocerus fe P. interstitialis ma P. interstitialis fe T. fulvipes ma T. fulvipes fe T. micro./obsc. ma T. microgaster fe T. obscurator fe Period of flowering common dates of insecticide spray

18 Feb. 28 Feb. 10 March 20 March 30 March 10 April 20 April 30 April 10 May 20 May 30 May 10 June 20 June 30 June 10 July Activity period of tersilochine parasitoids on crops of oilseed rape in relation to insecticide treatment (1996) 1) 2) 3) T. heterocerus ma T. heterocerus fe P. interstitialis ma P. interstitialis fe T. fulvipes ma T. fulvipes fe T. micro./obsc. ma T. microgaster fe T. obscurator fe Period of flowering common dates of insecticide spray

Post-harvest tillage effects on adult parasitoids emerging from soil in spring (Ind./m²) Conventional tillage Conservation tillage Direct drilling GÖ-Reinshof 1996 P. interstitialis 2 c 7 b 14 a T. heterocerus 1 c 7 b 11 a GÖ-Weende 1997 P. interstitialis 38 c 88 b 113 a T. heterocerus 17 c 49 b 55 b (Nitzsche, 1998) Non-inversion tillage applied following harvest of oilseed rape increases the survival of parasitoids, thus contributing to IPM

% parasitism of larvae (+ S.E.) No. of larvae/ petiole (+ S.E.) Mean number of P. chrysocephala larvae (A) and larval parasitism (B) in petioles of small (<5mm) and large (>5mm) diameter. May 2003

Potential of parasitoids for biocontrol of oilseed rape pests in Europe Percent parasitism of pests in STN/ICM experiments Collaborative field experiments on a farm-scale to compare two OSR crop management systems: Standard European OSR cropping system (STN) Integrated Pest Management system (IPM) in Germany (DE), Estonia (EE), Poland (PL), Sweden (SE), and (UK) in 2002/03, 2003/04, 2004/05

% parasitism (+ SE) Mean percent larval parasitism of OSR pests in conventional STN and IPM plots MASTER IPM Strategies experiments in EE, DE, PL, SE, UK 2003-2005 50 45 p = 0.047 40 35 30 p = 0.037 25 20 ns 15 10 5 0 STN IPM STN IPM STN IPM M. aeneus (14 experiments) C. assimilis (9 experiments) C. pallidactylus (10 experiments) Data collected by Ulber/DE, Luik/EE, Klukowski/PL, Nilsson/SE, Williams/UK

Conclusions Twelve key parasitoids are sufficiently widespread and abundant across Europe to be of potential economic importance for biocontrol of pests. They occure in almost all EU countries where their host species are present Percentage parasitism of pest larvae varies between EU countries and years; levels frequently exceed 30%, indicating their impact on populations of new-generation adults Mean parasitism of M. aeneus and C. assimilis was increased by an Integrated Pest Management system, compared to a Standard Management system Strategies for conservation and enhancement of parasitoid efficacy need to be improved in further studies

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