Coleoptera: Carabidae) in Bt- (MON810) and in Isogenic Maize Stands

Activity density, diversity and seasonal dynamics of ground beetles (Coleoptera: Carabidae) in Bt- (MON810) and in isogenic maize stands

Dora Szekeres, Ferenc Kadar & Jozsef Kiss

Szekeres, D., Kadar, F. & Kiss, J. 2006: Activity density, diversity and seasonal dynamics of ground beetles (Coleoptera: Carabidae) in Bt— (MON810) and in isogenic maize stands. — Entomol. Fennica 17: 269—275.

To compare carabid assemblages from transgenic Bt— and isogenic maize in Hun- gary, we used pitfall traps in an experiment (30x30 m plots, arranged alternately in 6 replications), during the growing season of maize during 2001—2003. We captured altogether 44,103 individuals of 58 species. The most common species in our sampling were Calatlzus ambiguus, Doliclzus halensis, Harpalus distingu— endus, H rufipes, Poecilus sericeus and Treclius quadristriatus. The same species dominated both in the Bt— and in the isogenic maize plots. Under our test con- ditions (plot size and 3 years of sampling), no significant differences were found either in the structural characteristics (number of individuals, number of species and diversity), activity density or seasonal activity patterns ofthe dominant spe- Cies.

D. Szekeres andJ. Kiss, Department ofPlant Protection, SzentIstvan University, H—2100, Go'do'll, Pater Karoly utca 1, Hungary; E—mail.‘ szekeres.dora@mkk. szie.lzu F. Kadar, Plant Protection Institute, Hungarian Academy ofSciences, P. 0. Box 102, Budapest, H—I525, Hungary

Received 1 1 January 2006, accepted 22 May 2006

1. Introduction indicators for measuring ecological impacts because the family is rich in species, taxonomically Maize is one ofthe major crops in Hungary, cov- well known, they are very abundant in arable ering about 1.2 million ha (http://faostat.fao. crops and seem highly sensitive to habitat org/faostat/). Lepidopteran pests of maize, the changes (Lovei & Sunderland 1996, Rainio & European Corn Borer (Ostrinia nubilalis Hfibner; Niemela 2003). ECB) and the Cotton Bollworm (Helicoverpa One ofthe control options for managing ECB armigera Hfibner; CB) can cause yield losses in population level is using transgenic maize with maize though their actual damage varies largely cryIAb gene from Bacillus thuringiensis Berliner by location and year (Palfy 1983, Szeoke 1994). var. kurstaki that expresses CrylAb toxin (Bt Ground beetles are common predators in agricul- maize) which is effective against ECB larvae. tural fields playing an important role in reducing The coexistence potential of these two types of pest populations in many crop ecosystems (Lovei pest control needs careful assessment. & Sunderland 1996). Carabids are widely used The CrylAb toxin is effective against larvae 270 Szekeres et a]. ° ENTOMOL. FENNICA Vol. 17 ofLepidoptera, the predatory arthropods in maize 2. Material & Methods stands may be affected by the altered maize plant and through various trophic interactions. Many 2.1. Experimental area and sampling method species of carabids are generalist predators con- suming arthropods on foliage or on the ground, The three-year field experiment was carried out larvae and pupae ofLepidoptera on the plant or in in an isolated field surrounded by large peach and the soil (Thiele 1977). Therefore carabids may be apricot orchards near Budapest (47°25’ N, impacted by CrylAb toxin through preyed ar- 18°47’ E), Hungary. Plots (30 m X 30 m) with Bt- thropods. Carabids may also consume maize maize (DK 440 BTY-transformation event MON plant tissues or residues. The presence of Cry 810) and with its isogenic line (DK 440) were es- 1Ab toxin in seven carabid adults sampled from tablished on chernozem soil and arranged alter- fields with Br maize residues was recently dem- nately, with 6 replications (Fig. 1). An alley dis- onstrated by Zwahlen and Andow (2005). Larvae tance of 3 m was used between replications. A ofground beetles can also be exposed to CrylAb maize hybrid of similar maturity ground to the toxin in the soil by root exudates in the rhizo- test hybrid was planted in the retention zone (pol- sphere ofBt maize plants (Saxena et al. 2002). len capture crop surrounding the entire test field) Some laboratory experiments indicated that in accordance with the requirements of the re- Bt—toxin had negative impact on the development lease permit. of Chrysoperla carnea larvae as non-target pred- Maize was planted at a seed rate of 65,000 ator (Hilbeck et al. 1998, Dutton et al. 2002). seeds/ha reduced to 50,000 plants/ha after emer- Transgene products can adversely affect also gence. Planting was between late April and early ground beetles (Jorgensen & Lovei 1999, Meissle May, and maize was harvested between mid-Oc- et al. 2005). Field studies indicate that the sea- tober and early November, depending on the sonal activity in Europe of non-target arthropods year. Regulations did not allow replanting GM (Lozzia & Rigamonti 1998, Bourguet et al. 2002, plants in exactly the same place; hence the plots, Sehnal et al. 2004, Daly & Buntin 2005, De la even though close, were physically different fiom Poza et al. 2005) and among them that of carabid year to year: the maximum distance between two beetles (Manachini et al. 1999, Volkmar et al. areas was some meters. The previous crop was to- 1999, Sehnal et al. 2004) does not differ between mato for the first year and sunflower for the sec- the transgenic and isogenic maize. ond and third years. There was no insecticide ap- No studies have been performed on the poten- plication in the maize plots (except a soil applica- tial impact of GM maize in the Carpathian Basin, tion of diazinon at planting in the first year). which forms a special biogeographical area Carabid adults were collected using pitfall (Anon. 2004). In a three-year (200172003) study traps. Traps were made from two 300 ml plastic under the Bt—BioNoTa project “Effects and mechanism of Bt transgenes on biodiversity of non-target insects: pollinators, herbivores and their natural enemies” (No. QLK3-CT-2000- 00547), we have surveyed the carabid assemblages in Bt— and in isogenic maize plots. Our aim was to asses the possible impact of Bt—maize on carabid assemblages measured by their activity density, the structural characteristics and seasonal activity patterns of the carabid assemblages. Our hypothesis was that these parameters will reflect any adverse effect oftransgenes on carabid individuals either through direct or indirect way. Fig. 1. Aerial view of the experimental block design with plots of transgenic (Bt) and isogenic (lso) maize in 2001 in Séskl'it, Hungary. ENTOMOL. FENNICA V01. 17 ° Carabl'd assemblages in Bt— and isogenic maize 271

Table 1. Percentage of carabid individuals captured in 2001—2003, SOslit, Hungary (+ indicates <1%).

Species 2001 2002 2003

ISO 81‘ ISO 81‘ ISO 81‘

Amara ingenua (Duftschmid) —— 1.90 2.14 + + Anchomenus dorsa/is (Pontoppidan) + 2.07 — + + + Anisodactylus signatus (Panzer) + + + + 2.07 1.55 Brachinus exp/odens Duftschmid + — 6.20 5.95 + + Broscus cephalotes cephalotes (Linnaeus) 1.08 + + + + + Calathus ambiguus (Paykull) 13.05 8.78 6.14 4.45 2.31 1.73 Calathus melanocephalus (Linnaeus) 2.11 2.02 + + + + Dolichus halensis (Schaller) 5.04 5.77 6.58 6.86 2.99 2.12 Harpa/us distinguendus distinguendus (Duftschmid) 3.41 3.16 26.03 25.83 16.22 16.78 Poecilus sericeus Fischer von Waldheim 2.60 3.01 3.04 3.26 5.92 5.09 Pseudoophonus ca/ceatus (Duftschmid) 3.63 3.75 + + + + Pseudoophonus (Harpalus) rufipes (De Geer) 59.12 64.18 43.14 45.01 65.87 68.07 Trechus quadristriatus (Schrank) 5.85 3.95 2.70 2.08 2.65 2.80 Other species 3.47 2.61 3.00 3.04 + + Total number of species 27 25 47 46 33 34 Total number of individuals 2,027 1,847 7,109 7,372 12,758 12,990

cups containing 4% formaldehyde solution as 3. Results killing agent and preservative. Two pitfall traps were placed in the middle (15th) row ofthe plot, at A total of44, 103 individuals of 58 ground beetle 10m distance from each other and from the border species were collected in maize plots during the of the plot. Samplings lasted from late July in three sampling periods (Table 1). Harpalus 2001 and from late May in 2002 and 2003 until rufipes De Geer, 1774, Harpalus distinguendus harvest. Traps were emptied weekly. The content Duftschmid, 1812, Poecz'lus sericeus Fischer von oftraps was taken to the laboratory for identifica- Waldheim, 1823, Dolichus halensis Schaller, tion of carabid adults to species level, using keys 1783, Calathus ambiguus Paykull, 1790, and by Hfirka (1996). Trechus quadristriatus Schrank, 1781 (in order of decreasing catch) were the most common species. These six species made up 93% of the total 2.2. Statistical analyses number of individuals captured. The same species dominated both in Bt— and in isogenic maize The structural characteristics ofthe assemblages: plots. the number of species, Shannon diversity index No significant differences were found in (Magurran 2003) and the activity density ofdom— structural characteristics in terms of ground bee- inant species on Bt— and isogenic plots were com- tles captured between the two treatments in the pared using Kruskal—Wallis test and ANOVA given year, using Kruskal—Wallis test (Table 2). with repeated measures, respectively (Sokal & For the mean number ofspecies/trap, the H values Rohlf 1995). The level of significance was set at were(1) in 20012H1’24 =0.223; (2) in 2002: 1’24: p=0.05. The Rényi diversity (Tothmérész 1995) 0.986; and (3) in 2003: H1,24 = 1.055. Likewise, was used for comparing the diversity of assem- for the mean number of individuals/trap, the val- blages in Bt— vs. isogenic plots. Analyses were ues were (1) in 2001: H1,24 = 3.102; (2) in 2002: made using STATISTICA (Statsoft 2000) and H1,24 = 0.213; and (3) in 2003: H1,24 = 0.013. The the DivOrd (Tothmérész 1993) program pack- mean diversity/trap did not show significant dif- ages. ferences either; the H values were as follows: (1) 272 SzekereS et al. ° ENTOMOL. FENNICA Vol. 17

Table 2. Structural characteristics of carabid assemblages in Bt— and in isogenic maize plots (2001, 2002 and 2003, Séslit, Hungary). Values are means $ SE. None of the comparisons within year were significantly different (Kruskal-Wallis test).

2001 2002 2003

Characteristic 81‘ ISO 81‘ ISO 81‘ ISO

Total no. species 25 27 47 46 33 34 No. species/trap 12.33$0.43 12.92$0.54 21 .25$0.97 22.67$0.93 15.0$0.66 16.08$0.67 Total no. individuals 2,027 1,847 7,109 7,372 12,758 12,990 No. indiv/trap. 168.92$7.55 153.92 592.42$43.8 614.33$39.6 1,063.17 1,082.5 $13.04 $71.95 $34.67 Shannon diversity 1.36$0.05 1.47$0.04 1.64$0.04 1.72$0.05 1.13$0.04 1.2$0.03

Table 3. Mean activity density of the most common carabid species/trap in Bt— and in isogenic maize plots (2001, 2002 and 2003, Séslit, Hungary). Values are means $ SE. None of the comparisons within year were significantly different (Kruskal-Wallis test).

2001 2002 2003

Treatment 81‘ ISO 81‘ ISO 81‘ ISO

C. ambiguus 14.83$1.72 20.08$3.81 26.33$5.15 37.75$6.54 18.42$2.58 25.0$2.93 D. ha/ensis 9.75$1.34 7.75$2.1 40.67$7.14 40.42$3.56 22.5$2.34 32.33$6.32 H. distinguendus 5.33$0.87 5.25$0.91 153.0$19.63 159.92$15.73 178.42$15.53 175.58$11.77 H. rufipes 108.42$5.49 91.0$7.18 266.67$16.45 265.0$29.89 723.67$58.36 713.0$31.57 P. sericeus 5.08$0.92 4.0$0.84 19.33$2.55 18.67$3.07 54.17$5.37 64.08$8.69 T. quadristriatus 6.67$1.7 9.0$1.4 12.33$1.34 16.58$2.61 29.75$5.24 28.67$4.88

— in 2001: H42 =3.630; (2)1n 2002: H42 —1.333; 0.141;p>0.05 in all cases). and (3)in 20203: H1 24— 1921;p>0.051n all cases) The Rényi diversity profiles ran very close to The evenness of the assemblages was not differ- each other (Fig. 2), and while the profile from the ent either (Table 2). Bt plots usually indicates a lower diversity, the There were no significant differences in the difference was minimal. mean total activity density of carabids/year/trap Within-season comparisons of activity den- between the Bt— and isogenic maize plots regard- sitys showed generally no significant differences ing all carabids for three years (Kruskal-Wallis either in total activity density (Fig. 3; GLM, in test; 2001: H42 —3.— 102; 2002: H424—— 0.213; 2002: F= 0.56 and in 2003: F= 0.58; d.f. =16,p 2003: =0.04'13 051n all or >0.05 in all cases, in see or in H4 24 ,p>0. cases) among except 2001; later) the dominant species (Table 3 Kruskal-Wallis the activity density of the most common species test; (1) C. ambiguuS, in 2001: H42 =0.482 in (H rufipeS in 2003, Fig. 4; GLM, C. ambiguus: in 2002' H424= 2. 343, in 2003' H424=23.234; (2)D. 2001: F= 0.94, d.f. = 6; in 2002: F= 0.98, d.f. = 4, halenSl'S, in 2001: =1.4,80 in 2002: D. halenSis: in 2001: F= 1.79, d.f. = 4; in 2002: F H424 H424

— <0.001, in 2003: H424 —1. 849; (3) H. distingu— = 1.08, d.f. = 5; in 2003: F= 0.43, d.f. = 6, H — in 2001: —0. in 2002: in 2001: F = d.f. = in enduS, H42 014, H424 distinguenduS: 0.004, 2;

— <0.001, in 2003: H424— 0.021; (4) H. rufipeS, in 2002: F= 1.71, d.f. = 13; in 2003: F= 0.57, d.f. = — — 2001' H424 —3.635, in 2002: H424— 06,08 in 15, H rufipes: in 2002: F = 0.22, d.f. = 13; in 2003: H 24=0.053; SericeuS, in 2001: H 2003: F= 0.51, d.f. =12, P. SericeuS: in 2001: F= 124 (5)P. 1,24 — —1. 159, in 2002: H =0303, in 2003: 0.46, d.f. = 4; in 2002: F = 0.91, d.f. = 8, T. 1,24 H424= 0.5;22 (6) T. quadristriatuS, in 2001: H42 = quadristriatuS: in 2001: F = 0.69, d.f. = 4; in

— 18,64 in 2002: H424 —12,89 in 2003: H424 = 2003: F= 0.25, d.f. = 1;p>0.05, in all cases; ex- TCA V01. 17 w Cambid assemblages in Brm and isagenic maize 273

4.0 " 2001 October W

(%) A sem- J

2 .0 '- isegenic 00-"- July indiv.

‘i .0 - n0. 40-"

0 Cumuiative 20"

4 . O

0 2'0 40 do so Cumulative no. indiv. Bi: (%)

Fig. 3. A comparison of the seasonal activity pattern of N C3 diversity adult carabids in Btu- and in captured by pitfall traps Renyi isogenic maize plots in 2003. at Sésknfiit, Hungary. The two activity curves did not deviate from each other F m 0.58. dsi. m ’16. ,0 >005).

" 4.0 2003 September

‘f 3.0" (%) 80-"- isogenic 2.0- 60-“- indiv. no. 1.0" 40--

20'“- 2 Cumulative Scale parameter Juneid May Fig. 2. Rényi diversity profiles of the ground beetle as“ I I I 0 20 40 60 80 100 in Btu and in maize "for 200’! sembiages isogenic plots Cumulative no. indiv. Bi (%) (up). 2002 (middle) and 2003 (bottom); Séskrfiit. Hun“ Fig. 4-. A comparison of seasonal activity patterns of gary. Harpaius rufipes adults captured by pitfall traps in Bi:- and isogenic in maize plots in 2003, at Séskm. Hun-— The curves were not different from each oth- cept for given species; see beicw) in the Brm and. in gary. ers ; F m 0.51. dxi. m ’12. p >005). isogenic maize in any year. The activity peaks of adult carabids varied from year to year (in 2001, late Juiy; in 2002, quadrisrriams (GL F 3 0.02, d.f. : 4, p 2 miduJuiy; and, in 2003, early July) both in the Bru- 0.021) in 2002 and P. sericeus F E 2.09, and the iscgenic plots. Several species showed bin d.f. Z 11,,p 3 0.025) in 2003. The activity density modal activity (cg, H. dislinguendus: ay and values offhese three species alternated in. time ei- October, TI quadrisrriams: um and Octo- ther for Btu or for isogenic plots Without any con:- ber), while other species showed unimodai activ- stant difference between treatments. ity (eg, D. halensis: Juiy, H mfipes: early Juiy). N0 significant differences were found in the sea»- scnal activity patterns ofabove species in Br“ and in isogenic picts with the exception for total spew Cies in 2001(GLMgF: 2.57, df. E 11,p E 0.006), We found a speciesmrich carabid assembiage with due to the different activity pattern ofH. mfipes high individual numbers both in the Bra (Cry 1 Ab) (GLM; F: 2.53,d.f.:11,p : 0.009) in 2001, C. and in the iscgenic maize plots. The number of ambiguus F x 3.5, d.f. : 7, p x 0.003), T collected species (58) exceeded the one found in 274 Szekeres et al. ° ENTOMOL. FENNICA Vol. 17 maize stands in various regions in Central Europe between the two peaks observed by Sekulic (Sekulic 1976, Andriescu et al. 1984, Lovei (1976). D. halensz's is common in August in Cen- 1984). A possible reason for this is the immigra- tral Hungary (Gergely & Lovei 1987) while we tion of some species from the neighbouring or- found a longer activity period. T. quadristriatus chard to the maize plots. The most common spe- showed a similar activity pattern to that described cies in our sampling are typical in agricultural by Desender and Pollet (1987). These patterns fields in Europe (Thiele 1977, Lovei & Saros- were probably caused by their reproductive peri- pataki 1990). ods and the appearance of teneral specimens. The relatively small plot size (30 m X 30 m) In conclusion, we did not detect drastic differ- raises the question of the validity of our data and ences between carabid assemblages of Bt— and the potential to draw conclusions regarding larger isogenic maize plots, considering activity den- fields. This was a logistical constraint as the re- sity, and seasonal activity density at our plot size. lease permit did not allow larger plots sizes. Bare The impact of planting Bt—maize on larger field ground between plots probably decreased the and over a longer period should be tested. movement of carabid adults between plots (Frampton et al. 1995, Garcia et al. 2000). Field Acknowledgements. A European Union Framework-5 re- X search project, (No.: QLK3—CT—2000—00547) and the tests on even smaller plots [10 m 25 m; Car- Hungarian National Scientific Research Foundation (No. camo & Spence (1994)] showed that carabid as- OTKA T048434) supported this research. The authors use in to semblages adjust habitat relation varia- would like to thank M. Perczel and Soskut Fruct Kft. for tion at this spatial scale. their technical support. We acknowledge the valuable and During our three-year field investigation, we critical comments of the reviewers. found no difference in assemblage characteristics in Bt— vs. non-Bt to other studies maize, similarly References (Manachini et al. 1999, Lozzia 1999, Manachini 2000, Dively & Rose 2002, Sehnal et al. 2004, Andriescu, I., Varvara, M. & Moglan, I. 1984: The dynam- & Buntin De la Poza et al. Daly 2005, 2005, ics of carabids (Coleoptera, Carabidae) in the maize Lopez et al. 2005). Our results showed that the experimental crops (Zea mais L.) treated with insecti- activity patterns of the most common species cides. 7 In: Kaszab, Z. (ed.), Verhandlungen X. Inter— nat. Symp. Entomofaunistik Mitteleuropas (SIEEC): were also mostly similar in Bt— and in isogenic 1437145. 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