Structure of Ladybird (Coleoptera: Coccinellidae) Assemblages in Apple: Changes through Developmental Stages GABOR L. LOVEI,' MIKLOS SAROSPATAKI, ANDZEINAB A. RADWAN Laboratory of Functional Ecology, Department of Zoology, Plant Protection Institute, Hungarian Academy of Sciences, P.O. Box 102, Budapest, 1525 Hungary Environ.Entomol.20(5): 1301-1308 (1991) ABSTRACT Larvae, pupae, and adults of ladybird beetles were observed in an insecticide- free and an insecticide-treated block in an apple orchard near Budapest, Hungary during 1980-1982. Speciesnumbers and densities in all developmental stageswere higher and species turnover was lower in the insecticide-free block. Diversity and similarity indices showed more diverse and constant assemblages in the insecticide-free block. The adult assemblage was the most rich in species, with 19 species in the insecticide-free and 12 species in the treated block. The most common species overall were Coccinella septempunctata, Adonia variegata, Adalia bipunctata, and Exochomus quadripustulatus. The larval assemblage included nine and eight species for the untreated and treated blocks respectively, whereas the pupal assemblage had eight species in both blocks. Immature stages of II species were found in at least 1 yr and 10 of these was able to complete development in the orchard. The rate of successwas higher in the insecticide-free block for most species. Only A. btpunctata reproduced successfully in both blocks in all three years but A. decempunctata and C. septempunctata were often successful. KEY WORDS Insecta, Coccinellidae, apple, species assemblage COCCINELLIDSare probably the best studied nat- perimental Farm of the Plant Protection Institute ural enemies of aphids (Hodek 1973, Niemczyk & near Budapest, Hungary. The natural vegetation Dixon 1988). The coccinellid fauna of cultivated of this hilly aI:ea is composed of oak-hornbeam areas has received considerable interest, especially forests and dry meadows, cleared and cultivated in crops on which aphids and coccids are important in the valleys and hillsides. The cultivated areas pests. Apple trees support several species of ho- consist of orchards and fields of small grains, leg- mopteran pests and consequently, the ladybird fau- umes, and forage crops. na of apple orchards is well studied in Europe The experimental orchard, established in 1967, (Hodek 1973) and elsewhere (Niemczyk & Dixon was sprayed 4-6 times a year until 1976, when a 1988). However, only a few of these studies include treated and an untreated block of equal size was developmental stages other than adults (Skanland established. Both blocks had three apple varieties, 1981, Radwan & L6vei 1982, Carroll & Hoyt 1984, 'Jonathan', 'Starking', and 'Red Delicious', in equal Lovei & Radwan 1988). Even these typically con- proportions. The 'insecticide-free' block received sider larvae or pupae as a group and do not distin- no insecticide sprays since 1976 but was sprayed guish species within them. with fungicides, herbicides, or both. Weeds were In the current paper we report on the compo- controlled by mowing and spraying with herbicides sition of all coccinellid developmental stages on (three sprays in 1980 and 1982, five in 1981). The apple trees in an orchard in central Hungary. We 'treated' block received the same management but describe the structure of the assemblage of larvae, was also sprayed with insecticides. There were three pupae, and adults and show that although 20 la- insecticide applications in 1980 (28 April, with dybird species were present as adults and ten spe- Novenda 2.0% (AI) dinitrophenol; 23 June and 5 cies laid eggs, subsequent developmental stages of August, with Ditrifon 50, 0.2% [AI] ditrifon), three these species were not found in all years. in 1981 (the methylparathion Wofatox SPP, 0.4% on 31 March and 29 June, Ditrifon 50 on 16 May) and two in 1982 (Wofatox SPP on 7 May and 16 Materials & Methods August). Study Orchard. The study site was a 5.8-ha ex- Observation Methods. Ladybirds were visually perimental apple orchard at the Juliannamajor Ex- observed weekly from early spring (March) until late autumn (October) in 1980-1982, 32 wk/yr. Fifty branches (five randomly selected major 'Currentaddressand addressfor reprints:The Agroecology branches of each on ten trees) per block were cen- Group,Ministryof Agricultureand Fisheries,HorticulturalRe- sused. Half of these trees were selected randomly searchCentre,KimberleyRoad,PrivateBag,Levin,NewZealand. at the first census and were 'constant' afterwards; 0046-225Xj91j1301-1308$02.00jO © 1991 EntomologicalSocietyof America 1302 ENVIRONMENTAL ENTOMOLOGY Vol. 20, no. 5 Table I. Composition and characteristics of the larvnl assemhlages in the apple orchard, Juliannamajor, 1980- 1982 Treated block Insecticide-free block Species 1980 1981 1982 Total 1980 1981 1982 Total Adalia bipunctata 0 10 217 227 84 126 147 357 A. decempunctata 0 2 26 28 16 36 1 53 Anatis ocellata 0 0 0 0 0 1 0 1 Calma quatu01'dee/mguttata 0 0 16 16 43 65 16 124 Coce/nella septempunctata 0 2 39 41 1 47 46 94 Exochomus quadripustulatus 2 6 3 11 21 21 20 62 Propylea quatuordee/mpunctata 0 9 4 13 0 0 1 1 Scymnus subvillosus 0 0 0 0 0 0 7 7 Semiadalia undee/mnotata 0 0 1 1 0 1 0 1 Stet horus punctillum 0 49 1 50 0 0 0 0 Identified, total 2 78 307 387 165 297 238 700 Unidentified 0 7 259 266 392 279 170 850 Species number 1 6 8 8 5 7 7 9 Dominance 0.63 0.71 0.51 0.42 0.62 Q diversity 1.86 U56 1.09 1.31 1.39 Numbers are yearly totals (32 weekly samples) observed on 50 branches. the other five were randomly selected before every As a measure of stability of species composition, census. This design was recommended throughout we calculated species turnover, the sum of the the Agroecology Project as a result of spatial anal- number of species 'acquired' and 'lost' in a given ysis of apple arthropods (Szentkinilyi, unpub- year, compared to the previous one: lished). All coccinellid developmental stages were Species turnover for year n = number of species counted and identified if possible. To ascertain the present in year n but not in year n-l number validity of observations on reproduction, eclosion + of species not present in year n but present in year events and the presence of teneral adults was noted. n-l. (4) Samples of unidentified larvae and pupae were taken to the laboratory for rearing and confirma- tion as necessary. This was difficult with smalilar- Results vae and consequently, many of these were not iden- tified to species. Densities are given as the totals Larval Assemblages. The number of larvae ob- observed on 50 branches for each year. served in the insecticide-free block (1,550 in 3 yr) Analysis. The species rank-abundances were fit- was twice that in the treated block (653). About ted to the logarithmic distribution using the linear half of these, mainly newly hatched larvae, were regression subroutine of the BIOM package (Rohlf not identified to species. More species and more 1987) on log-transformed data. To compare the individuals in the insecticide-free block than in the diversity of the assemblages, we used the domi- treated block were observed in 1980 and 1981 but nance index (Southwood 1978) and the midrange not in 1982 (Table 1). Species turnover was higher diversity (Kempton & Taylor 1976), both of which in the treated block (3.5 species/yr versus 2.67 spe- are superior for comparisons than the more popular cies/yr in the insecticide-free block). Densities Shannon-Wiener index of diversity (Kempton & among years varied widely in the treated block Wedderburn 1978). The dominance index, d, is (1980-1981, 39 x increase; 1981-1982, 3.9 x), less so in the insecticide-free block (1980-1981, 1.8 x; = NJN,ota'. (1) d 1981-1982, 0.8 x). where N, is the number of individuals of the most In the insecticide-free block, 5 the 9 species were common species, N,"••) is the number of individuals present in all 3 yr; all others were found in 1 yr in the sample, and d is the relative abundance of only. These five species made up 98.6% of all the the most common species. The midrange or Q- individuals identified. diversity was calculated as: Larvae of eight species were observed in the treated block over the 3 yr studied. Only Exocho- Q = 0.371 S/u, (2) mus quadripustulatus (L.) was found in all 3 yr. where S is the number of species and u is the stan- Five of the remaining seven species were present dard deviation of the natural logarithm of the in both remaining years; Calvia quatuordecim- abundances (Kempton & Taylor 1976). guttata (F.) and Semiadalia undecimnotata The similarities were evaluated by Renkonen's (Schneider) were observed in 1982 only. The con- percentage similarity (Renkonen 1938): stant six species found in two or more years ac- counted for 95.6% of all identified larvae. PS = ~ min (PH' P2i), (3) Most species present in the treated block in a where Pj; = njJNj, the proportion of species i in given year were also present in the insecticide-free sample j. block. Exceptions to this were: Stethorus punctil- October 1991 LOVEI ET AL.: COCCINELLID ASSEMBLAGES IN ApPLE 1303 Table 2. Renkonen similarities of the larval assem- secticide-free block. Contrary to this, the Q index blages in the apple orchard, 1980-1982 indicated a higher than average diversity in the treated block in 1982, a medium value in the in- TR 1982 IF 1980 IF 1981 IF 1982 secticide-free block in 1980-1981 and a low one in TR 1981 0.205 0.237 0.250 0.239 the treated block in 1981.