And Pot Marigold (Calendula Officinalis) on Diamondback Moth (Plutella Xylostella L.) Population Density and It’S Parasitoid Complex

2010 vol. 73, 107-117 DOI: 10.2478/v10032-010-0023-x ______

EFFECT OF INTERCROPPING WHITE CABBAGE WITH FRENCH MARIGOLD (TAGETES PATULA NANA) AND POT MARIGOLD (CALENDULA OFFICINALIS) ON DIAMONDBACK MOTH (PLUTELLA XYLOSTELLA L.) POPULATION DENSITY AND IT’S PARASITOID COMPLEX

Beata JANKOWSKA University of Agriculture in Kraków Faculty of Horticulture, Department of Plant Protection 29 Listopada 54, 31-425 Kraków, Poland Received: May 12, 2010; Accepted: July 27, 2010

Summary The impact of intercropping white cabbage (‘Bently F1’) with French Mar- igold Tagetes patula nana ‘Kolombina’ and Pot Marigold Calendula officinalis ‘Promyk’ on the occurrence of diamondback moth (DBM) (Plutella xylostella L.) and its parasitoid complex was estimated in years 2003-2005. The number of DBM larvae and pupae was significantly lower on plots where cabbage was intercropped compared with the control variant (homogenous crop). The combination with Pot Marigold turned out to be the best in this respect. The DBM larvae parasitization level varied from year to year and its percentage oscillated from 65 to 88%. Eight beneficial insect species belonging to families: Ichneu- monidae (4 species), Braconidae (2 species), Pteromalidae (1 species) and Eu- lophidae (1 species) emerged from collected DBM pupae. Diadegma fenestralis Holmgr. was the most abundant species among all Plutella parasitoids every year of observations as it constitued 65% of all of the reared wasps. No significant differences were determined between the level of parasitization in relation to the type of cultivation. key words: Plutella xylostella, cabbage, intercropping, parasitoids

INTRODUCTION belonging to Brassicaceae family in Poland (Jankowska 2005, 2006) and The diamondback moth (DBM), have the potential to severely reduce Plutella xylostella (L.) (Lepidoptera: the marketable yield or to completely Plutellidae), remains one of the most destroy the crop. Overuse of broad- damaging insect pests of brassica spectrum insecticides for diamond- plants (Brassica sp.) worldwide. It is back moth control is a serious prob- particularly dangerous to vegetables lem and has obscured the contribu-

Corresponding author: e-mail: [email protected] © Copyright by RIVC

108 VEGETABLE CROPS RESEARCH BULLETIN 73 ______of indigenous parasitoids. The ab- ‘Bently F1’, cabbage intercropped with sence of effective natural enemies, Tagetes patula nana ‘Kolombina’ and especially parasitoids is belived to be cabbage intercropped with Calendula a major cause of the diamondback officinalis ‘Promyk’. Tagetes and Ca- moth’s pest status. Naturally occur- lendula were sown by hand on 22 ring parasites are important factors April in 2003-2004, and 24 April in regulating pest population densities 2005. Cabbage was transplanted in (Łagowska 1981, Wiech & Jankow- spacing of 67.5  40 cm between flow- ska 1999, Jankowska & Wiech 2006). er rows on 28 May in 2003-2004, and The biodiversification of the cultivat- 3 June in 2005. On experimental plots ed landscape has been a research trend no chemical treatments were applied in many countries worldwide. Moreo- and weeds were removed mechanical- ver there is an increased realization ly. Ten plants from each plot were over the world that development of selected and marked for inspections biological control including preserva- made on a weekly basis during which tion or augmentation of natural ene- both diamondback moth caterpillars mies is the base of management pro- and pupae were counted. The collected grammes (Talekar & Shelton 1993, pupae of the diamondback moth were Biever et al. 1994). Diversity of plants kept separately in glass vials at the la- in agrocenosis may be an important boratory until either parasitoid or moth factor that influences the presence of emerged. Results were statistically ana- pests as well as their natural enemies. lysed using analysis of variance. The Intercropping is one of the ways to significance of differences between diversify the species populations in particular combinations was counted the field. The aim of this work was to using Duncan test at the 5% level. determine the impact of intercropping white cabbage with Pot Marigold RESULTS AND DISCUSSION Calendula officinalis L. and French Marigold Tagetes patula nana of the The diamondback moth was ob- presence of diamondback moth and its served each year of the experiment parasitoid complex. and occurred in all combinations. The first instar larvae were leaf miners, MATERIAL AND METHODS but later instars fed on the leaf surface. Caterpillars did not feed on Observations on the occurrence veins and the sign of their presence of P. xylostella and its parasitoids were either windows or holes in were carried out in the Plant Protec- leaves. Feeding caterpillars were ob- tion Experimental Station in Mydlniki served both on the upper and lower near Krakow, on brown soil devel- leaf surface. The biggest DBM infes- oped on loess in 2003-2005. The ex- tation was observed in July (Fig.1). periment was designed as a random- Also in the previous research Jankow- ized block, in three replications on ska (2005) noted the biggest infesta- 10.8 m2 plots. The combinations of tion of different cabbage vegetables the experiment included three objects: by DBM larvae at the same time. The homogenous crop white cabbage crop occurrence period of caterpillars was

B. JANKOWSKA – EFFECT OF INTERCROPPING WHITE CABBAGE ... 109 ______similar on all combinations, but statis- 209 studies involving 287 pest spe- tically significant differences were cies. Compared with monocultures, found between infestation in accord- the population of pest insects was ance to the type of cultivation. On lower in 52% of the studies (149 spe- plots where cabbage was intercropped cies). Meny studies reported lower the number of DBM larvae and pupae abundance of P. xylostella in inter- was significantly lower compared cropping system with labiate herbs with control variant (homogenous (Dover 1986), clover and french bean crop) (Table 1). The combination with (Wiech & Wnuk 1991), subterranean Pot Marigold turned out to be the best clover (Finch & Kienegger 1997), in this respect. Vegetational diversity stravbery clover (Theunissen & Schel- in the form of intercropping can result ling 1996), white clover (Dover 1986, in reduced pest densities and increases Wiech 1993), red clover (Åsman et al. the resistance of the environment 2001), tomatoes, garlic, dill, or clover (Wiech & Kałmuk 2005, Jankowska (Buranday & Raros 1975, Dover et al. 2009). Andow (1991) analysed 1986).

Table 1. Occurrence of the diamondback moth (Plutella xylostella L.) larvae and pupae on the cabbage according to the type of cultivation (2003-2005)

Mean number larvae and pupae/30 plants Type of cultivation 2003 2004 2005 Cabbage (homogenous crop) 13 b 4.8 b 5.3 b Cabbage with Tagetes patula 9.3 b 1.0 a 0.8 a Cabbage with Calendula officinalis 3.5 a 0.2 a 0.2 a Values followed by the same letter do not differ significantly at 5% level

Phytophagous insects locate a host may mask the scent of host plants for oviposition on the basis of plant which hampers its finding (Per- scent and visual stimuli. Characteris- rin & Philips 1978). tic plant odours (volatile chemicals) During 2003-2005 315 pupae of are credited with the major role of DBM were collected, but only 98 guiding phytophagous insects to their moths (31%) were recovered from the host plants. Biologically active com- cocoons. The most important factor pounds called glucosinolates are feed- decreasing the number of DBM was ing and oviposition stimulants for such parasitization (69%). The highest a crucifer specialist. According to numbers of parasitoids were recorded many authors (Gupta & Thorsteinson in 2003 (Table 2, 3) when DBM was 1960, Srinivisan & Moorthy 1991, the most abundant. Result of rearing Pawar & Lawande 1995, Mitchel et al. pupae of this pest are presented in 1997, Pivnick et al. 1990), Plutella Table 2. Total parasitization of DBM xylostella is stimulated to oviposition by all the parasitoids varied between on cabbage leaves by the secondary the years and oscillated from 65 to plant compound - allyl isothiocyanate. 88% in the three years (Table 2). The The proximity of plants which are not dynamics of parasitizing was similar

110 VEGETABLE CROPS RESEARCH BULLETIN 73 ______irrespective of the way of cropping recorded throughout the whole period (Fig. 2). High rates of parasitism were of infestation by the DBM (Fig. 2).

30 2003 25

number larvae and pupae / 30 plants 30 / pupae and larvae number 0 11.06 17.06 25.06 2.07 08.07 16.07 21.07 29.07 06.08 13.08 A B C 30 2004 25

number larvae and pupae / 30 plants 0 25.06 28.06 02.07 08.07 14.07 22.07 30.07 04.08 11.08 17.08 A B C 30 2005 25

number larvae and pupae / 30 plants 30 / pupae and larvae number 0 22.06 25.06 29.06 06.07 09.07 15.07 20.07 27.07 03.08 10.08 A B C

A - cabbage in homogenous crop B - cabbage intercropped with French Marigold (Tagetes patula nana) C - cabbage intercropped with Pot Marigold (Calendula officinalis) Fig. 1. Comparison of diamondback moth (Plutella xylostella L.) dynamics in relation to the cultivation method (2003-2005)

B. JANKOWSKA – EFFECT OF INTERCROPPING WHITE CABBAGE ... 111 ______

25 A 20

0 11.06 17.06 25.06 2.07 08.07 16.07 21.07 29.07 06.08 13.08 25 B 20

0 11.06 17.06 25.06 2.07 08.07 16.07 21.07 29.07 06.08 13.08

25 C 20

0 11.06 17.06 25.06 2.07 08.07 16.07 21.07 29.07 06.08 13.08

P. xylostella Diadegma fenestralis Diadegma semiclausum Diadromus collaris Cotesia fuliginosus Cotesia longipalpis Mesochorus spp. Habrocytus sp. Oomyzus sokolowskii

A - cabbage in homogenous crop B - cabbage intercropped with French Marigold (Tagetes patula nana) C - cabbage intercropped with Pot Marigold (Calendula officinalis) Fig. 2. Number of parasitoid adults and diamondback moths obtained from the collected cocoons according to the type of cultivation on the example of year 2003

112 VEGETABLE CROPS RESEARCH BULLETIN 73 ______

217 specimens of parasitic wasps only species (Table 3) parasitizing belonging to 8 species from families: 88% (Table 2) of larvae. In Poland, in Ichneumonidae (4 species), Braco- research of Łagowska (1981) D. fe- nidae (2 species), Pteromalidae (1 nestralis was the dominant species species) and Eulophidae (1 species) reducing 40-90% of pest population. emerged from the collected DBM pu- Also observations of the dominant pae. Species composition and numbers parasitoid species D. fenestralis were of parasitoids are presented in Table 3. made by Wiech and Jankowska In each year of observations the (1999), Wiech and Kałmuk (2002, most abundant species among the 2003), Jankowska and Wiech (2006). Plutella parasitoids was Diadegma This species was introduced from fenestralis Holmgr. as it constitued Europe to India where it became a 65% of all of the reared wasps (Table natural enemy of P. xylostella (Devi 3). In the 2004 D. fenestralis was the & Raj 1995; Usha et al. 1997).

Table 2. Effect of rearing pupae of diamondback moth (Plutella xylostella L.) collected from cabbage crops

2003 2004 2005 Total Effect Num- Num- Num- Num- of rearing % % % % ber ber ber ber Plutella xylostella L. 79 34.8 5 12 14 30.5 98 31 Parasitoids 148 65.2 37 88 32 69.5 217 69 Total 227 100 42 100 46 100 315 100

The other numerous parasitoids Another ichneumonid species of P. xylostella caterpillars were: Di- emerging from P. xylostella larvae adromus collaris Holmgr. and Cotesia were D. semiclausum and C. fuligi- longicauda. Both of these species par- nosus (Table 3). Also three species of asitized about 11.5% of DBM larvae hyperparasitoids were reared: Meso- (Table 3). D. collaris has been record- chorus spp., Habrocytus sp. and ed in many parts of the world as an Oomyzus sokolowskii. The action of important parasitoid of the diamond- the secondary parasitoids limits the back moth and introduced to Asia efficiency of the primary parasitoids (Talekar 1996) and to New Zealand in controlling DBM populations. (Beck & Cameron 1990). In Poland it However, their presence is negligible was reported by Łagowska (1981) and and has no significant economic im- Miczulski (1996). D. collaris was de- pact. scribed as larval-pupal (Avci & Ozbek The attractiveness of flowers is 1990) or pupal (Okada 1991) parasi- an important characteristic that should toid. Braconids belonging to genus be taken into account for the selection Cotesia are considered as the most of flowering plants and tailoring nec- important representatives of this fami- tar supply to the requirements of para- ly reducing the number of DBM larvae sitoids holds potential to increase their (Łagowska 1981, Rice & Hahr 1994, effectiveness as biological control Talekar 1996). agents (Bianchi & Wäckers 2008).

B. JANKOWSKA – EFFECT OF INTERCROPPING WHITE CABBAGE ... 113 ______

Also Winkler et al. (2006) stress the and the percentages of predatory Syr- importance of providing suitable nec- phidae to prey were more favorable tar sources as an integral part of bio- than on homogenous crop. However, logical control programmes. Nawroc- studies conducted there were no sig- ka (2006) noted that the number of nificantly different between level of entomophagous species (parasitoids parasitization in relation to the culti- and predators) were always higher on vation method (Table 4). Also Wiech intercropped cabbage plants. Jankow- and Jankowska (1999) found no dif- ska (2007) noted that on plots where ferences between the level of parasit- cabbage was intercropped with Pot ism of the DBM larvae collected from Marigold and French Marigold cab- the cabbage in homogenous crop and bage aphid parasitization by Diae- those intercropped with white clover. retiella rapae M’Intosh was greater

Table 3. Species composition and quantities of parasitoid emerged from pupae of the diamondback moth (Plutella xylostella L.)

Kind of 2003 2004 2005 Total Family /Species parasitiza- No. % No. % No. % No. % tion Family: Ichneumonidae parasite of Diadeg- 3 2 0 0 0 0 3 1.4 DBM larvae ma semiclausum Hellen Diadegma fenes- parasite of 84 56,8 37 100 20 62.5 141 65 tralis Holmgr. DBM larvae Diadromus collaris parasite of 18 12.2 0 0 7 21.9 25 11.5 Holmgr. DBM pupae hyperparasi- Mesochorus spp. 5 3.4 0 0 0 0 5 2.3 toid Family: Braconidae parasite of Cotesia longicauda 20 13.5 0 0 5 15.6 25 11.5 DBM larvae Wesm. Cotesia fuliginosus parasite of 12 8.1 0 0 0 0 12 5.5 Wesm. DBM larvae Family: Pteromalidae hyperparasi- 2 1.3 0 0 0 0 2 1 Habrocytus sp. toid Family Eulophidae hyperparasi- Oomyzus sokolowskii 4 2.7 0 0 0 0 4 1.8 toid Kurd. Total 148 100 37 100 32 100 217 100

114 VEGETABLE CROPS RESEARCH BULLETIN 73 ______

Table 4. Comparison of the occurrence of parasitoids of diamondback moth (Plutella xylostella L.) in relation to the cultivation method (2003-2005)

Cabbage with Species of Cabbage (ho- Cabbage with Calendula parasitoids mogenous crop) Tagetes patula officinalis 2003 Diadegma semiclausum Hellen 1 1 1 Diadegma fenestralis Holmgr 43 30 11 Diadromus collaris Holmgr. 9 7 2 Mesochorus spp. 2 2 1 Cotesia fuliginosus Wesm. 5 5 2 Cotesia longicauda Wesm. 9 10 1 Habrocytus sp. 0 1 1 Oomyzus sokolowskii Kurd. 1 2 1 Total 70 58 20 Parasitization % 67 a 63 a 65 a 2004 Diadegma fenestralis Holmgr 28 7 2 Parasitization % 74 90 100 2005 Diadegma fenestralis Holmgr. 17 2 1 Diadromus collaris Holmgr. 6 1 0 Cotesia longipalpis Reinhard 3 1 1 Total 26 4 2 Parasitization % 54 54 100

CONCLUSIONS (1 species) emerged from the collected DBM pupae. In each year 1. On plots where cabbage was in- of observations the most abundant tercropped the number of DBM species among Plutella parasi- larvae and pupae was significant- toids was Diadegma fenestralis ly lower compared with control Holmgr. as it constitued 65% of variant (homogenous crop). The all of reared wasps. combination with Pot Marigold 4. No differences were determined turned out to be the best in this re- between the level of parasitization spect. in relation to the cultivation 2. The parasitization of DBM larvae method. varied between the years and oscillated from 65 to 88% and was a REFERENCES very important factor reducing the number of emerging diamondback Andow D.A. 1991. Vegetational diversity moths. and arthropod population response. 3. Eight species belonging to fami- Annual Review of Entomology 36: 561-568. lies: Ichneumonidae (4 species), Åsman K., Ekbom B., Rämert B. 2001. Braconidae (2 species), Pteroma- Effect of intercropping on oviposi- lidae (1 species) and Eulophidae tion and emigration behavior of the

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WPŁYW WSPÓŁRZĘDNEJ UPRAWY KAPUSTY BIAŁEJ Z NAGIETKIEM KARŁOWYM (CALENDULA OFFICINALIS L.) I AKSAMITKĄ NISKĄ PEŁNĄ (TAGETES PATULA NANA) NA WYSTĘPOWANIE TANTNISIA KRZYŻOWIACZKA PLUTELLA XYLOSTELLA L. I JEGO PARAZYTOIDÓW

Streszczenie W latach 2003-2005 badano wpływ współrzędnej uprawy kapusty białej z nagietkiem karłowym (Calendula officinalis L.) ‘Promyk’ i aksamitką niską pełną (Tagetes patula nana) ’Kolombina’ na występowanie tantnisia krzyżowiaczka Plutella xylostella L. oraz związanych z nim parazytoidów. Na poletkach, gdzie kapusta była uprawiana współrzędnie, stwierdzono istotnie mniej gąsienic i poczwarek tantnisia. Najlepsza pod tym względem okazała się kombinacja z nagietkiem. Spasożytowanie wahało się w poszczególnych latach od 65 do 85%. Nie stwierdzono istotnych różnic w spasożyto- waniu w zależności od sposobu uprawy. Z zebranych poczwarek wyhodowano 8 gatun- ków parazytoidów z rodzin Ichneumonidae (4 gatunki), Braconidae (2 gatunki), Ptero- malidae (1 gatunek) i Eulophidae (1 gatunek). We wszystkich latach gatunkiem domi- nującym był Diadegma fenestralis Holmgr.