TY - JOUR
AU - Brabec,, Marek
AB - Abstract Harmonia axyridis (Pallas), an invasive non-native species in central Europe, can outcompete other aphidophagous species. The distribution and abundance of H. axyridis vary depending on different host plants, and its effects on native coccinellid communities may change accordingly. The distribution and abundance of coccinellids in central Europe (50°N, 14°E) were investigated from 2010 to 2016. Coccinellids were counted at regular intervals on cereals (Avena, Hordeum, and Triticum), herbaceous plants (Matricaria and Urtica) and trees (Acer, Betula, and Tilia). Additionally, the occurrence over time of each species on these plants was assessed and used as an index of persistence. Across all years, the adults and larvae of H. axyridis were the dominant species of coccinellid on trees. However, H. axyridis was less abundant on herbaceous plants and cereals than on trees. Populations of native coccinellids and H. axyridis co-occurred on trees and persisted for the same length of time, while native coccinellids persisted longer than H. axyridis on herbaceous plants and cereals. Compared to 1976–1986, in the 2010s, the abundance of native species decreased on all plants by 50–70%. The presence of H. axyridis could be considered as a factor driving changes in the assemblages of native coccinellids. invasive alien species, larva, cereal, herbaceous plant, trees Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), an invasive alien species in many regions of the world (Roy et al. 2016), was first recorded in central Europe (Czech Republic) in 2006 (Sprynar 2008). By 2009, it had become abundant, principally on trees but also on herbaceous plants and crops (Honek et al. 2014). This species can outcompete other aphidophagous species (Howe et al. 2016) and is an intraguild predator, principally consuming the immature stages of other aphidophagous species (Lucas 2005, Ware et al. 2008a, Ingels et al. 2013). Harmonia axyridis is considered not only a threat to biodiversity but also a pest to viticulture and a nuisance to humans because it forms large overwintering aggregations in buildings and occasionally bites humans, which can lead to allergic reactions (Nakazawa et al. 2007, Chakir et al. 2016). The general outline of its life cycle is well known (Honek et al. 2018). There are a number of important determinants of coccinellid occurrence, including host plant, prey abundance, and microclimate (Iperti 1999). Some species occur on a wide range of plant species (e.g., Propylea quatuordecimpunctata (L.)), while others are specialists on trees (e.g., Adalia decempunctata (L.)) or herbaceous plants (e.g., Hippodamia variegata (Goeze)) (Honek and Rejmanek 1982, Honek 1985). Studies in Western Europe have revealed that H. axyridis has a preference for trees (Adriaens et al. 2008; Brown et al. 2008, 2011; Panigaj et al. 2014; Roy et al. 2016; Brown and Roy 2018), particularly those growing in urban areas (Purse et al. 2015). In contrast, the abundance of H. axyridis is comparatively low on herbaceous vegetation and cereals (Adriaens et al. 2008, Jansen and Hautier 2008). The global distribution of H. axyridis is well documented (Roy et al. 2016), but detailed observations on particular hostplants (e.g., Gardiner et al. 2009) are still incomplete. Such studies would not only increase our understanding of the population dynamics of H. axyridis but also provide empirical data to underpin predictive models specifically assessing the effects of this alien species on coccinellid assemblages. We studied the variations in the abundance of H. axyridis and the community of native species of coccinellids. This is because H. axyridis is likely to affect many different mechanisms and native species (Bahlai et al. 2015, Diepenbrock and Finke 2013, Diepenbrock et al. 2016). The presence of invasive H. axyridis and native coccinellids was recorded on trees, herbaceous plants, and cereals from 2010 to 2016. For comparison, we used an existing dataset containing the abundance of coccinellids but spanning 1976 to 1986, before the arrival of H. axyridis. The temporal changes in the abundance of coccinellids, including in the later time period, and H. axyridis, on particular plants, provides the basis for exploring the hypothesis that long-term declines in the abundance of native coccinellids are correlated with the high abundance and wide distribution of H. axyridis. Materials and Methods Field Surveys Harmonia axyridis and native species of coccinellids were sampled in 2010–2016, in the western part of the Czech Republic in an 11 × 7 km area centered at 50.105°N and 14.264°E. Surveys focused on trees (Acer platanoides L., A. pseudoplatanus L., Betula pendula Roth, Tilia cordata Mill., and Tilia platyphyllos Scop.), herbaceous plants (Tripleurospermum inodorum (L.) Schultz-Bip. and Urtica dioica L.) and small-grain cereals (Avena sativa L., Hordeum vulgare L., and Triticum aestivum L.). These host plants were considered as three distinct types: trees, herbaceous plants, and cereal crops. The same locations were sampled over the years for the trees and U. dioica stands, whereas because of crop rotation, cereal stands and T. inodorum were sampled at different sites each year but all within close proximity. Each year surveys on trees started in April and terminated in November. On herbaceous plants and cereals, surveys started when the vegetation was ≥30 cm high and terminated when plants became senescent. At particular sites, surveys were repeated at 14-d intervals. Sampling was conducted on sunny and calm days, between 08:00 and 18:00 hours. On trees, coccinellids were sampled from the canopy below 3 m in height, on herbaceous plants and cereals, they were sampled from the upper 20–30 cm stratum of vegetation. Coccinellids were sampled by sweeping with a standard entomology net (35 cm diameter, 140 cm handle). The same person (A.H.) carried out all the surveys and ensured similar sampling efficiency in sweeping. Sampling intensity was quantified by the number of sweeps per survey. In each survey, sampling coccinellid adults and larvae on a particular plant at a particular site, lasted 15–30 min. Adults and larvae of the third and fourth instars were identified to species, counted, and immediately released at the site. In total, there were 1,588 survey visits, with a mean of 129 ± 1.5 sweeps per survey (range 50–400 sweeps). Localities and dates of sampling are listed in Supp. Tables 1 and 2. To compensate for the different sampling intensities, in terms of number of sweeps, the numbers of individuals recorded during a particular survey were recalculated to numbers per 100 sweeps (further ‘n/100’) except for the GLM analyses where raw data were used. The duration of persistence of adults and larvae on particular plants was calculated as the difference (days) between the first and the last record in a particular year. The term ‘persistence’ for the native species means persistence at the community level. This term indicates the amount of time for which each taxon, H. axyridis and community of native species, was present on a given hostplant in a given year. This metric is useful for understanding differential use of the various plant habitats. To establish long-term changes in the abundance of native coccinellids, the recent data were compared with the data for 1976–1986 when the same surveys were used. In this period, there were 71 surveys of trees, 94 of herbaceous plants and 150 of cereals. Data Analysis Analyses only included surveys where ≥1 coccinellid was captured, i.e., one or more adults of any species in the analysis of adult populations, or one or more larvae of any species in the analysis of larval populations. For 2010–2016, the differences in the abundance of H. axyridis, and all native species among three plant types (trees, herbaceous plants, and cereals) were compared using generalized estimating equations (GEE). This method is an extension of GLM for correlated data (Yan and Fine 2004). As the sampling dates were nested within years, and an exchangeable correlation structure was used (Pekár and Brabec 2018). To correct for the different sampling intensity each year, the natural logarithm of the total number of sweeps per year was set as an offset in the model formula because we expected that the mean value of abundance would be proportional to the sampling intensity. Total abundance per year was used as a response variable. GEE with a Poisson error structure (GEE-p) was used due to the counting process and heteroscedasticity. The differences in the length of coccinellid occurrence (days between the first and the last record in a particular year) on particular plants were compared using GEE with a normal distribution of errors (GEE). Plant type and coccinellid species (H. axyridis and natives) were used as factors. Analyses of abundance and occurrence were performed separately for the adults and larvae. Differences in the abundance of native coccinellid communities among plant types and between two periods, 1976–1986 and 2010–2016, were also compared using GEE-p, with an offset of sampling effort and exchangeable correlation structure. Post-hoc tests with Tukey adjustment were used on pairwise comparisons of H. axyridis versus native species for all factor combinations. All analyses were performed in the R program (R Core Team 2015). Results The abundance of all coccinellids varied between host plants (Table 1). There was a significant interaction between plant type and the abundance of adult coccinellid species (GEE-p, χ22 = 361, P < 0.0001). Adults of H. axyridis were dominant on trees (Fig. 1). Indeed, the average abundance (17.8 ± 1.62 n/100) on trees was 7.5 times greater than on herbaceous plants (3.6 ± 2.25 n/100) and 89 times greater than on cereals (0.2 ± 0.06 n/100). The abundance of native coccinellids exhibited a markedly different pattern. The average abundance of native coccinellids on trees (5.2 ± 0.90 n/100) and cereals (9.1 ± 1.92 n/100) was lower compared to that on herbaceous plants (16.7 ± 2.38 n/100). The high abundance of native coccinellids on herbaceous plants and cereals was attributed to the occurrence of Coccinella septempunctata L., P. quatuordecimpunctata (L.) and, on herbaceous plants in some years, also Ceratomegilla undecimnotata (Schneider) and Hippodamia variegata (Goeze). There was also a significant interaction between plant type and larval coccinellid species (GEE-p, χ22 = 286.4, P < 0.0001). The larvae of H. axyridis were on the same host plants as the adults (Fig. 1). The average abundance of H. axyridis on trees (8.8 ± 2.38 n/100) was approximately three times greater than that on herbaceous plants (3.4 ± 1.26 n/100) and 44 times greater than that on cereals (0.2 ± 0.07 n/100). The abundance pattern of the larvae of native species (Fig. 1) also mirrored that of the adults. The mean abundance on herbaceous plants (17.4 ± 3.45 n/100) was nearly two times greater than that on cereals (9.3 ± 4.82 n/100) and 12 times greater than that on trees (1.4 ± 0.23 n/100). In summary, H. axyridis was dominant on trees, and native coccinellids prevailed on herbaceous plants and cereals. Table 1. The occurrence of adults and larvae of H. axyridis and native coccinellids on trees, low-growing herbaceous plants (Herbs) and small-grain cereals in 2010–2016 Total Harmonia axyridis Native species Samplesn SpeciesN Individualsn Abundancen/100 ± SE Persistence Individualsn Abundancen/100 ± SE Persistence Start End Lengthd Start End Lengthd Adults  Trees   2010 56 15 839 15.5 ± 2.70 08 Oct. 465 8.5 ± 1.02 08 Oct.   2011 120 15 2,643 17.0 ± 3.57 20 April 18 Oct. 181 1,049 7.3 ± 1.06 20 April 18 Oct. 181   2012 96 19 2,412 18.0 ± 2.84 09 May 19 Oct. 163 994 7.2 ± 1.26 09 May 19 Oct. 163   2013 109 16 1,707 12.3 ± 2.34 04 May 16 Oct. 165 478 3.7 ± 0.85 04 May 16 Oct. 165   2014 160 20 3,716 14.6 ± 3.12 19 April 04 Nov. 199 756 3.1 ± 0.55 19 April 05 Nov. 200   2015 165 17 4,807 24.0 ± 3.07 22 April 03 Nov. 195 654 3.2 ± 0.41 22 April 03 Nov. 195   2016 198 17 4,070 23.0 ± 1.96 06 May 08 Nov. 186 678 3.3 ± 0.43 06 May 09 Nov. 187  Herbs   2010 25 11 23 1.5 ± 0.29 11 Aug. 611 26.2 ± 7.05 11 Aug.   2011 79 15 1,271 17.1 ± 3.54 19 May 23 Aug. 96 1,539 20.4 ± 2.82 19 May 23 Aug. 96   2012 67 12 90 1.5 ± 0.57 24 May 15 Oct. 144 1,416 16.9 ± 3.62 09 May 19 Oct. 163   2013 62 14 32 0.4 ± 0.13 20 May 04 Oct. 137 683 7.1 ± 1.69 15 May 04 Oct. 142   2014 64 17 101 0.9 ± 0.39 08 May 17 Sept. 132 1,043 10.2 ± 2.81 08 May 04 Nov. 180   2015 75 16 199 2.3 ± 0.78 18 May 26 Oct. 161 1,076 11.2 ± 3.38 05 May 26 Oct. 174   2016 47 11 91 1.7 ± 0.36 08 June 19 Aug. 72 1,173 25.0 ± 7.07 09 May 26 Sept. 140  Cereals   2010 19 8 3 0.1 ± 0.09 09 July 16 July 7 221 9.0 ± 1.02 22 July   2011 57 10 31 0.3 ± 0.16 29 June 03 Aug. 35 1,857 17.3 ± 1.06 10 May 03 Aug. 85   2012 37 8 7 0.1 ± 0.09 02 July 26 July 24 688 11.6 ± 1.26 09 May 26 July 78   2013 55 6 3 0.0 ± 0.03 20 June 17 July 27 342 3.1 ± 0.85 13 May 16 Aug. 95   2014 46 9 8 0.1 ± 0.08 17 June 01 Aug. 45 802 10.9 ± 0.55 06 May 06 Aug. 92   2015 19 7 2 0.1 ± 0.07 26 June 01 Aug 36 236 8.6 ± 0.41 02 Jun 01 Aug 60   2016 32 11 28 0.5 ± 0.28 30 May 23 July 54 138 2.7 ± 0.43 30 May 23 July 54 Larvae  Trees   2012 31 5 114 3.3 ± 0.77 21 May 09 Oct. 141 69 1.8 ± 0.80 09 May 27 July 79   2013 34 7 207 4.9 ± 1.64 19 June 08 Sept. 81 38 1.0 ± 0.33 17 June 15 Sept. 90   2014 64 7 953 8.6 ± 3.72 19 May 05 Nov. 170 80 0.8 ± 0.29 21 May 19 Oct. 151   2015 44 6 519 10.0 ± 3.01 18 May 23 July 66 113 2.3 ± 0.74 18 May 07 July 50   2016 89 7 1,303 17.0 ± 3.43 27 May 02 Nov. 159 106 1.1 ± 0.32 06 June 23 Sept. 109  Herbs   2012 15 7 26 1.8 ± 0.81 23 May 06 July 44 200 14.7 ± 4.85 23 May 15 Oct. 145   2013 18 7 8 0.3 ± 0.22 08 July 27 July 19 305 8.6 ± 4.70 28 June 24 Aug. 57   2014 17 7 204 8.4 ± 8.81 18 June 18 Aug. 61 297 11.2 ± 9.02 15 May 06 Aug. 83   2015 23 7 122 4.9 ± 2.08 11 June 16 July 35 697 21.0 ± 5.18 04 June 26 Aug. 83   2016 23 7 33 1.3 ± 0.50 16 June 27 June 11 860 31.5 ± 15.47 16 June 26 Sept. 102  Cereals   2012 15 3 6 0.3 ± 0.34 05 July 05 July 808 32.0 ± 15.27 29 May 11 July 43   2013 16 4 1 0.0 ± 0.06 17 July 17 July 100 3.1 ± 1.71 28 June 02 Aug. 35   2014 22 4 11 0.3 ± 0.21 02 July 17 July 15 78 1.9 ± 0.77 17 June 27 July 40   2015 9 3 0 0.0 ± 0.00 66 4.9 ± 1.55 03 July 17 July 14   2016 18 3 12 0.4 ± 0.31 23 June 13 July 20 188 4.8 ± 5.97 10 June 23 July 43 Total Harmonia axyridis Native species Samplesn SpeciesN Individualsn Abundancen/100 ± SE Persistence Individualsn Abundancen/100 ± SE Persistence Start End Lengthd Start End Lengthd Adults  Trees   2010 56 15 839 15.5 ± 2.70 08 Oct. 465 8.5 ± 1.02 08 Oct.   2011 120 15 2,643 17.0 ± 3.57 20 April 18 Oct. 181 1,049 7.3 ± 1.06 20 April 18 Oct. 181   2012 96 19 2,412 18.0 ± 2.84 09 May 19 Oct. 163 994 7.2 ± 1.26 09 May 19 Oct. 163   2013 109 16 1,707 12.3 ± 2.34 04 May 16 Oct. 165 478 3.7 ± 0.85 04 May 16 Oct. 165   2014 160 20 3,716 14.6 ± 3.12 19 April 04 Nov. 199 756 3.1 ± 0.55 19 April 05 Nov. 200   2015 165 17 4,807 24.0 ± 3.07 22 April 03 Nov. 195 654 3.2 ± 0.41 22 April 03 Nov. 195   2016 198 17 4,070 23.0 ± 1.96 06 May 08 Nov. 186 678 3.3 ± 0.43 06 May 09 Nov. 187  Herbs   2010 25 11 23 1.5 ± 0.29 11 Aug. 611 26.2 ± 7.05 11 Aug.   2011 79 15 1,271 17.1 ± 3.54 19 May 23 Aug. 96 1,539 20.4 ± 2.82 19 May 23 Aug. 96   2012 67 12 90 1.5 ± 0.57 24 May 15 Oct. 144 1,416 16.9 ± 3.62 09 May 19 Oct. 163   2013 62 14 32 0.4 ± 0.13 20 May 04 Oct. 137 683 7.1 ± 1.69 15 May 04 Oct. 142   2014 64 17 101 0.9 ± 0.39 08 May 17 Sept. 132 1,043 10.2 ± 2.81 08 May 04 Nov. 180   2015 75 16 199 2.3 ± 0.78 18 May 26 Oct. 161 1,076 11.2 ± 3.38 05 May 26 Oct. 174   2016 47 11 91 1.7 ± 0.36 08 June 19 Aug. 72 1,173 25.0 ± 7.07 09 May 26 Sept. 140  Cereals   2010 19 8 3 0.1 ± 0.09 09 July 16 July 7 221 9.0 ± 1.02 22 July   2011 57 10 31 0.3 ± 0.16 29 June 03 Aug. 35 1,857 17.3 ± 1.06 10 May 03 Aug. 85   2012 37 8 7 0.1 ± 0.09 02 July 26 July 24 688 11.6 ± 1.26 09 May 26 July 78   2013 55 6 3 0.0 ± 0.03 20 June 17 July 27 342 3.1 ± 0.85 13 May 16 Aug. 95   2014 46 9 8 0.1 ± 0.08 17 June 01 Aug. 45 802 10.9 ± 0.55 06 May 06 Aug. 92   2015 19 7 2 0.1 ± 0.07 26 June 01 Aug 36 236 8.6 ± 0.41 02 Jun 01 Aug 60   2016 32 11 28 0.5 ± 0.28 30 May 23 July 54 138 2.7 ± 0.43 30 May 23 July 54 Larvae  Trees   2012 31 5 114 3.3 ± 0.77 21 May 09 Oct. 141 69 1.8 ± 0.80 09 May 27 July 79   2013 34 7 207 4.9 ± 1.64 19 June 08 Sept. 81 38 1.0 ± 0.33 17 June 15 Sept. 90   2014 64 7 953 8.6 ± 3.72 19 May 05 Nov. 170 80 0.8 ± 0.29 21 May 19 Oct. 151   2015 44 6 519 10.0 ± 3.01 18 May 23 July 66 113 2.3 ± 0.74 18 May 07 July 50   2016 89 7 1,303 17.0 ± 3.43 27 May 02 Nov. 159 106 1.1 ± 0.32 06 June 23 Sept. 109  Herbs   2012 15 7 26 1.8 ± 0.81 23 May 06 July 44 200 14.7 ± 4.85 23 May 15 Oct. 145   2013 18 7 8 0.3 ± 0.22 08 July 27 July 19 305 8.6 ± 4.70 28 June 24 Aug. 57   2014 17 7 204 8.4 ± 8.81 18 June 18 Aug. 61 297 11.2 ± 9.02 15 May 06 Aug. 83   2015 23 7 122 4.9 ± 2.08 11 June 16 July 35 697 21.0 ± 5.18 04 June 26 Aug. 83   2016 23 7 33 1.3 ± 0.50 16 June 27 June 11 860 31.5 ± 15.47 16 June 26 Sept. 102  Cereals   2012 15 3 6 0.3 ± 0.34 05 July 05 July 808 32.0 ± 15.27 29 May 11 July 43   2013 16 4 1 0.0 ± 0.06 17 July 17 July 100 3.1 ± 1.71 28 June 02 Aug. 35   2014 22 4 11 0.3 ± 0.21 02 July 17 July 15 78 1.9 ± 0.77 17 June 27 July 40   2015 9 3 0 0.0 ± 0.00 66 4.9 ± 1.55 03 July 17 July 14   2016 18 3 12 0.4 ± 0.31 23 June 13 July 20 188 4.8 ± 5.97 10 June 23 July 43 For each plant and year, the table indicates number of samples and species collected; for H. axyridis and the community of native coccinellids, the number (n) of individuals, mean abundance (number of individuals × 100 sweeps−1 [n/100]) and the characteristics of temporal persistence, date of the first catch (Start), date of the last catch (End) and number of days (d) from the first to the last catch (Length) are indicated. Mean values of Abundance (Fig. 1) and Length (Fig. 2) are presented in graphs. Each sample represents a set of individuals collected on a particular date on a group of trees, a herb stand or in a field. View Large Table 1. The occurrence of adults and larvae of H. axyridis and native coccinellids on trees, low-growing herbaceous plants (Herbs) and small-grain cereals in 2010–2016 Total Harmonia axyridis Native species Samplesn SpeciesN Individualsn Abundancen/100 ± SE Persistence Individualsn Abundancen/100 ± SE Persistence Start End Lengthd Start End Lengthd Adults  Trees   2010 56 15 839 15.5 ± 2.70 08 Oct. 465 8.5 ± 1.02 08 Oct.   2011 120 15 2,643 17.0 ± 3.57 20 April 18 Oct. 181 1,049 7.3 ± 1.06 20 April 18 Oct. 181   2012 96 19 2,412 18.0 ± 2.84 09 May 19 Oct. 163 994 7.2 ± 1.26 09 May 19 Oct. 163   2013 109 16 1,707 12.3 ± 2.34 04 May 16 Oct. 165 478 3.7 ± 0.85 04 May 16 Oct. 165   2014 160 20 3,716 14.6 ± 3.12 19 April 04 Nov. 199 756 3.1 ± 0.55 19 April 05 Nov. 200   2015 165 17 4,807 24.0 ± 3.07 22 April 03 Nov. 195 654 3.2 ± 0.41 22 April 03 Nov. 195   2016 198 17 4,070 23.0 ± 1.96 06 May 08 Nov. 186 678 3.3 ± 0.43 06 May 09 Nov. 187  Herbs   2010 25 11 23 1.5 ± 0.29 11 Aug. 611 26.2 ± 7.05 11 Aug.   2011 79 15 1,271 17.1 ± 3.54 19 May 23 Aug. 96 1,539 20.4 ± 2.82 19 May 23 Aug. 96   2012 67 12 90 1.5 ± 0.57 24 May 15 Oct. 144 1,416 16.9 ± 3.62 09 May 19 Oct. 163   2013 62 14 32 0.4 ± 0.13 20 May 04 Oct. 137 683 7.1 ± 1.69 15 May 04 Oct. 142   2014 64 17 101 0.9 ± 0.39 08 May 17 Sept. 132 1,043 10.2 ± 2.81 08 May 04 Nov. 180   2015 75 16 199 2.3 ± 0.78 18 May 26 Oct. 161 1,076 11.2 ± 3.38 05 May 26 Oct. 174   2016 47 11 91 1.7 ± 0.36 08 June 19 Aug. 72 1,173 25.0 ± 7.07 09 May 26 Sept. 140  Cereals   2010 19 8 3 0.1 ± 0.09 09 July 16 July 7 221 9.0 ± 1.02 22 July   2011 57 10 31 0.3 ± 0.16 29 June 03 Aug. 35 1,857 17.3 ± 1.06 10 May 03 Aug. 85   2012 37 8 7 0.1 ± 0.09 02 July 26 July 24 688 11.6 ± 1.26 09 May 26 July 78   2013 55 6 3 0.0 ± 0.03 20 June 17 July 27 342 3.1 ± 0.85 13 May 16 Aug. 95   2014 46 9 8 0.1 ± 0.08 17 June 01 Aug. 45 802 10.9 ± 0.55 06 May 06 Aug. 92   2015 19 7 2 0.1 ± 0.07 26 June 01 Aug 36 236 8.6 ± 0.41 02 Jun 01 Aug 60   2016 32 11 28 0.5 ± 0.28 30 May 23 July 54 138 2.7 ± 0.43 30 May 23 July 54 Larvae  Trees   2012 31 5 114 3.3 ± 0.77 21 May 09 Oct. 141 69 1.8 ± 0.80 09 May 27 July 79   2013 34 7 207 4.9 ± 1.64 19 June 08 Sept. 81 38 1.0 ± 0.33 17 June 15 Sept. 90   2014 64 7 953 8.6 ± 3.72 19 May 05 Nov. 170 80 0.8 ± 0.29 21 May 19 Oct. 151   2015 44 6 519 10.0 ± 3.01 18 May 23 July 66 113 2.3 ± 0.74 18 May 07 July 50   2016 89 7 1,303 17.0 ± 3.43 27 May 02 Nov. 159 106 1.1 ± 0.32 06 June 23 Sept. 109  Herbs   2012 15 7 26 1.8 ± 0.81 23 May 06 July 44 200 14.7 ± 4.85 23 May 15 Oct. 145   2013 18 7 8 0.3 ± 0.22 08 July 27 July 19 305 8.6 ± 4.70 28 June 24 Aug. 57   2014 17 7 204 8.4 ± 8.81 18 June 18 Aug. 61 297 11.2 ± 9.02 15 May 06 Aug. 83   2015 23 7 122 4.9 ± 2.08 11 June 16 July 35 697 21.0 ± 5.18 04 June 26 Aug. 83   2016 23 7 33 1.3 ± 0.50 16 June 27 June 11 860 31.5 ± 15.47 16 June 26 Sept. 102  Cereals   2012 15 3 6 0.3 ± 0.34 05 July 05 July 808 32.0 ± 15.27 29 May 11 July 43   2013 16 4 1 0.0 ± 0.06 17 July 17 July 100 3.1 ± 1.71 28 June 02 Aug. 35   2014 22 4 11 0.3 ± 0.21 02 July 17 July 15 78 1.9 ± 0.77 17 June 27 July 40   2015 9 3 0 0.0 ± 0.00 66 4.9 ± 1.55 03 July 17 July 14   2016 18 3 12 0.4 ± 0.31 23 June 13 July 20 188 4.8 ± 5.97 10 June 23 July 43 Total Harmonia axyridis Native species Samplesn SpeciesN Individualsn Abundancen/100 ± SE Persistence Individualsn Abundancen/100 ± SE Persistence Start End Lengthd Start End Lengthd Adults  Trees   2010 56 15 839 15.5 ± 2.70 08 Oct. 465 8.5 ± 1.02 08 Oct.   2011 120 15 2,643 17.0 ± 3.57 20 April 18 Oct. 181 1,049 7.3 ± 1.06 20 April 18 Oct. 181   2012 96 19 2,412 18.0 ± 2.84 09 May 19 Oct. 163 994 7.2 ± 1.26 09 May 19 Oct. 163   2013 109 16 1,707 12.3 ± 2.34 04 May 16 Oct. 165 478 3.7 ± 0.85 04 May 16 Oct. 165   2014 160 20 3,716 14.6 ± 3.12 19 April 04 Nov. 199 756 3.1 ± 0.55 19 April 05 Nov. 200   2015 165 17 4,807 24.0 ± 3.07 22 April 03 Nov. 195 654 3.2 ± 0.41 22 April 03 Nov. 195   2016 198 17 4,070 23.0 ± 1.96 06 May 08 Nov. 186 678 3.3 ± 0.43 06 May 09 Nov. 187  Herbs   2010 25 11 23 1.5 ± 0.29 11 Aug. 611 26.2 ± 7.05 11 Aug.   2011 79 15 1,271 17.1 ± 3.54 19 May 23 Aug. 96 1,539 20.4 ± 2.82 19 May 23 Aug. 96   2012 67 12 90 1.5 ± 0.57 24 May 15 Oct. 144 1,416 16.9 ± 3.62 09 May 19 Oct. 163   2013 62 14 32 0.4 ± 0.13 20 May 04 Oct. 137 683 7.1 ± 1.69 15 May 04 Oct. 142   2014 64 17 101 0.9 ± 0.39 08 May 17 Sept. 132 1,043 10.2 ± 2.81 08 May 04 Nov. 180   2015 75 16 199 2.3 ± 0.78 18 May 26 Oct. 161 1,076 11.2 ± 3.38 05 May 26 Oct. 174   2016 47 11 91 1.7 ± 0.36 08 June 19 Aug. 72 1,173 25.0 ± 7.07 09 May 26 Sept. 140  Cereals   2010 19 8 3 0.1 ± 0.09 09 July 16 July 7 221 9.0 ± 1.02 22 July   2011 57 10 31 0.3 ± 0.16 29 June 03 Aug. 35 1,857 17.3 ± 1.06 10 May 03 Aug. 85   2012 37 8 7 0.1 ± 0.09 02 July 26 July 24 688 11.6 ± 1.26 09 May 26 July 78   2013 55 6 3 0.0 ± 0.03 20 June 17 July 27 342 3.1 ± 0.85 13 May 16 Aug. 95   2014 46 9 8 0.1 ± 0.08 17 June 01 Aug. 45 802 10.9 ± 0.55 06 May 06 Aug. 92   2015 19 7 2 0.1 ± 0.07 26 June 01 Aug 36 236 8.6 ± 0.41 02 Jun 01 Aug 60   2016 32 11 28 0.5 ± 0.28 30 May 23 July 54 138 2.7 ± 0.43 30 May 23 July 54 Larvae  Trees   2012 31 5 114 3.3 ± 0.77 21 May 09 Oct. 141 69 1.8 ± 0.80 09 May 27 July 79   2013 34 7 207 4.9 ± 1.64 19 June 08 Sept. 81 38 1.0 ± 0.33 17 June 15 Sept. 90   2014 64 7 953 8.6 ± 3.72 19 May 05 Nov. 170 80 0.8 ± 0.29 21 May 19 Oct. 151   2015 44 6 519 10.0 ± 3.01 18 May 23 July 66 113 2.3 ± 0.74 18 May 07 July 50   2016 89 7 1,303 17.0 ± 3.43 27 May 02 Nov. 159 106 1.1 ± 0.32 06 June 23 Sept. 109  Herbs   2012 15 7 26 1.8 ± 0.81 23 May 06 July 44 200 14.7 ± 4.85 23 May 15 Oct. 145   2013 18 7 8 0.3 ± 0.22 08 July 27 July 19 305 8.6 ± 4.70 28 June 24 Aug. 57   2014 17 7 204 8.4 ± 8.81 18 June 18 Aug. 61 297 11.2 ± 9.02 15 May 06 Aug. 83   2015 23 7 122 4.9 ± 2.08 11 June 16 July 35 697 21.0 ± 5.18 04 June 26 Aug. 83   2016 23 7 33 1.3 ± 0.50 16 June 27 June 11 860 31.5 ± 15.47 16 June 26 Sept. 102  Cereals   2012 15 3 6 0.3 ± 0.34 05 July 05 July 808 32.0 ± 15.27 29 May 11 July 43   2013 16 4 1 0.0 ± 0.06 17 July 17 July 100 3.1 ± 1.71 28 June 02 Aug. 35   2014 22 4 11 0.3 ± 0.21 02 July 17 July 15 78 1.9 ± 0.77 17 June 27 July 40   2015 9 3 0 0.0 ± 0.00 66 4.9 ± 1.55 03 July 17 July 14   2016 18 3 12 0.4 ± 0.31 23 June 13 July 20 188 4.8 ± 5.97 10 June 23 July 43 For each plant and year, the table indicates number of samples and species collected; for H. axyridis and the community of native coccinellids, the number (n) of individuals, mean abundance (number of individuals × 100 sweeps−1 [n/100]) and the characteristics of temporal persistence, date of the first catch (Start), date of the last catch (End) and number of days (d) from the first to the last catch (Length) are indicated. Mean values of Abundance (Fig. 1) and Length (Fig. 2) are presented in graphs. Each sample represents a set of individuals collected on a particular date on a group of trees, a herb stand or in a field. View Large Fig. 1. View largeDownload slide Comparison of the abundance of adults and larvae of H. axyridis and native coccinellids on trees, low-growing herbaceous plants (Herbs) and cereals. Statistically significant differences (Tukey post-hoc tests, P < 0.05) between H. axyridis and Native species within each plant type evaluated separately for adults and larvae are indicated by different letters. Bars are means (±SE). Fig. 1. View largeDownload slide Comparison of the abundance of adults and larvae of H. axyridis and native coccinellids on trees, low-growing herbaceous plants (Herbs) and cereals. Statistically significant differences (Tukey post-hoc tests, P < 0.05) between H. axyridis and Native species within each plant type evaluated separately for adults and larvae are indicated by different letters. Bars are means (±SE). The persistence of coccinellid species on particular plants (Table 1) varied. There was a significant interaction between plant type and coccinellid species for adults (GEE, χ22 = 74, P < 0.0001, Fig. 2). Native species persisted longer than H. axyridis, particularly on herbs and cereals. On trees, the adults of native species were present for nearly the same period of time (182 ± 5.8 d) as those of H. axyridis (179 ± 5.7 d). The difference was greater on herbaceous plants where the adults of native species were present for 118 ± 12.5 d and those of H. axyridis for 149 ± 11.6 d, and on cereals, where adult native species and H. axyridis were present for 77 ± 6.2 d and 33 ± 5.8 d, respectively. There was also a significant interaction between the plant type and the larvae of coccinellid species (GEE, χ22 = 63.9, P < 0.0001). The persistence of larvae was significantly shorter than that of adults (GEE, χ22 = 47.5, P < 0.0001). On trees, the larvae of H. axyridis persisted for 123 ± 21.0 d, which is longer than that for the larvae of native coccinellids at 96 ± 16.8 d. On herbaceous plants, H. axyridis larvae were present for 34 ± 8.9 d and native coccinellids for 94 ± 14.6 d, and on cereals, H. axyridis and native coccinellids were present for 17.5 ± 2.5 and 35 ± 5.5 d, respectively. Fig. 2. View largeDownload slide Duration of persistence of coccinelllid populations (the number of days that elapsed from the date of capture of the first individual to the day of capture of the last individual) of adults and larvae of H. axyridis and native coccinellids on particular plants, trees, low-growing herbaceous plants (Herbs) and cereals. Statistically significant differences (Tukey post-hoc tests, P < 0.05) between H. axyridis and Native species within each plant type evaluated separately for adults and larvae are indicated by different letters. Bars are means (±SE). Fig. 2. View largeDownload slide Duration of persistence of coccinelllid populations (the number of days that elapsed from the date of capture of the first individual to the day of capture of the last individual) of adults and larvae of H. axyridis and native coccinellids on particular plants, trees, low-growing herbaceous plants (Herbs) and cereals. Statistically significant differences (Tukey post-hoc tests, P < 0.05) between H. axyridis and Native species within each plant type evaluated separately for adults and larvae are indicated by different letters. Bars are means (±SE). We found a significant effect of plant type (GEE-p, χ22 = 40, P < 0.0001) and time period (1976–1986 [early] or 2010–2016 [late]) on the abundance of adults (GEE-p, χ12 = 56.8, P < 0.0001). In the early time period, the average abundance of native coccinellid adults (31.9 ± 1.48 n/100) was 3.1 times greater than in 2010–2016 (9.9 ± 0.71 n/100) (Fig. 3). In both periods, coccinellids were most abundant on wild herbaceous plants. The native coccinellids decreased in abundance mostly on trees between the two time periods; the abundance in the early period was 4.4 times greater than that in the late period, and the abundance was less (3.4 times) on herbaceous plants and least (2.1 times) on cereals. The difference was mainly due to a decline in the abundance of the previously dominant species (Table 2) A. bipunctata (abundance decreased 22 times on trees and 84 times on herbaceous plants), C. septempunctata (abundance decreased 2–13 times) and P. quatuordecimpunctata (abundance decreased 2–7 times). The order of dominance of the species in the communities on particular plants changed over time. Among the most abundant species on trees were Adalia bipunctata (L.) and Adalia decempunctata (L.), followed by P. quatuordecimpunctata in the early period and C. septempunctata in the late period. On herbaceous plants, C. septempunctata and H. variegata were dominant, followed by A. bipunctata in the early period and P. quatuordecimpunctata in the late period. On cereals, C. septempunctata and P. quatuordecimpunctata were dominant, followed by Coccinella quinquepunctata L. in the early period and H. variegata in the late period. Table 2. Composition of native coccinellid communities sampled in the early (1976–1986) and late (2010–2016) periods on trees, low-growing herbaceous plants (Herbs) and cereals (for list of species see methods) 1976–1986 2010–2016 Trees Herbs Cereals Trees Herbs Cereals n n/100 n n/100 n n/100 n n/100 n n/100 n n/100 Adalia bipunctata 585 (9.81) 1,290 (26.77) 10 (0.04) 416 (0.45) 130 (0.32) Adalia conglomerata (L.) 1 (0.00) Adalia decempunctata 209 (3.33) 11 (0.15) 2 (0.01) 1,150 (0.98) 16 (0.04) 1 (0.00) Anatis ocellata (L.) 7 (0.09) 1 (0.00) 8 (0.01) 1 (0.00) Aphidecta obliterata (L.) 4 (0.04) 83 (0.07) 1 (0.00) Calvia decemguttata (L.) 9 (0.22) 443 (0.44) 2 (0.01) 1 (0.00) Calvia quatuordecimguttata 19 (0.35) 11 (0.24) 287 (0.28) 38 (0.09) 5 (0.01) Ceratomegilla undecimnotata 251 (0.72) 2 (0.00) Chilocorus bipustulatus (L.) 38 (0.03) 1 (0.00) Coccidula rufa (Hbst.) 6 (0.13) Coccinella quinquepunctata 54 (1.76) 58 (1.00) 295 (1.39) 29 (0.02) 425 (0.69) 57 (0.13) Coccinella septempunctata 105 (1.32) 593 (12.27) 3,603 (13.46) 1,151 (0.99) 3,617 (7.30) 2,715 (5.87) Coccinella undecimpunctata 1 (0.02) 164 (3.49) 19 (0.08) Coccinulla quatuordecimpustulata (L.) 3 (0.01) Exochomus quadripustulatus (L.) 2 (0.03) 1 (0.02) 269 (0.26) 2 (0.00) Halyzia sedecimguttata (L.) 138 (0.15) 5 (0.01) Harmonia quadripunctata (Pontoppidan) 24 (0.02) Hippodamia septemmaculata (DeGeer) 2 (0.01) 1 (0.00) Hippodamia variegata 3 (0.02) 207 (4.34) 8 (0.03) 4 (0.00) 1,657 (3.20) 105 (0.26) Oenopia conglobata (L.) 34 (0.56) 16 (0.34) 358 (0.32) 3 (0.01) Propylea quatuordecimpunctata 259 (2.93) 192 (3.67) 1,398 (5.09) 462 (0.42) 549 (1.14) 1,264 (2.92) Psyllobora vigintiduopunctata (L.) 2 (0.01) 117 (0.11) 391 (0.90) 10 (0.02) Rhyzobius litura (F.) 5 (0.01) 2 (0.00) Scymnus sp. 1 (0.02) 18 (0.02) 10 (0.02) 2 (0.00) Subcoccinella vigintiquatuorpunctata (L.) 48 (0.03) 47 (0.11) 15 (0.04) Tytthaspis sedecimpunctata (L.) 2 (0.00) 383 (0.97) 103 (0.22) 1976–1986 2010–2016 Trees Herbs Cereals Trees Herbs Cereals n n/100 n n/100 n n/100 n n/100 n n/100 n n/100 Adalia bipunctata 585 (9.81) 1,290 (26.77) 10 (0.04) 416 (0.45) 130 (0.32) Adalia conglomerata (L.) 1 (0.00) Adalia decempunctata 209 (3.33) 11 (0.15) 2 (0.01) 1,150 (0.98) 16 (0.04) 1 (0.00) Anatis ocellata (L.) 7 (0.09) 1 (0.00) 8 (0.01) 1 (0.00) Aphidecta obliterata (L.) 4 (0.04) 83 (0.07) 1 (0.00) Calvia decemguttata (L.) 9 (0.22) 443 (0.44) 2 (0.01) 1 (0.00) Calvia quatuordecimguttata 19 (0.35) 11 (0.24) 287 (0.28) 38 (0.09) 5 (0.01) Ceratomegilla undecimnotata 251 (0.72) 2 (0.00) Chilocorus bipustulatus (L.) 38 (0.03) 1 (0.00) Coccidula rufa (Hbst.) 6 (0.13) Coccinella quinquepunctata 54 (1.76) 58 (1.00) 295 (1.39) 29 (0.02) 425 (0.69) 57 (0.13) Coccinella septempunctata 105 (1.32) 593 (12.27) 3,603 (13.46) 1,151 (0.99) 3,617 (7.30) 2,715 (5.87) Coccinella undecimpunctata 1 (0.02) 164 (3.49) 19 (0.08) Coccinulla quatuordecimpustulata (L.) 3 (0.01) Exochomus quadripustulatus (L.) 2 (0.03) 1 (0.02) 269 (0.26) 2 (0.00) Halyzia sedecimguttata (L.) 138 (0.15) 5 (0.01) Harmonia quadripunctata (Pontoppidan) 24 (0.02) Hippodamia septemmaculata (DeGeer) 2 (0.01) 1 (0.00) Hippodamia variegata 3 (0.02) 207 (4.34) 8 (0.03) 4 (0.00) 1,657 (3.20) 105 (0.26) Oenopia conglobata (L.) 34 (0.56) 16 (0.34) 358 (0.32) 3 (0.01) Propylea quatuordecimpunctata 259 (2.93) 192 (3.67) 1,398 (5.09) 462 (0.42) 549 (1.14) 1,264 (2.92) Psyllobora vigintiduopunctata (L.) 2 (0.01) 117 (0.11) 391 (0.90) 10 (0.02) Rhyzobius litura (F.) 5 (0.01) 2 (0.00) Scymnus sp. 1 (0.02) 18 (0.02) 10 (0.02) 2 (0.00) Subcoccinella vigintiquatuorpunctata (L.) 48 (0.03) 47 (0.11) 15 (0.04) Tytthaspis sedecimpunctata (L.) 2 (0.00) 383 (0.97) 103 (0.22) Total number of adults (n) and average abundance (n individuals × 100 sweeps−1, n/100) in brackets, bold figures indicate dominant species in terms of abundance. View Large Table 2. Composition of native coccinellid communities sampled in the early (1976–1986) and late (2010–2016) periods on trees, low-growing herbaceous plants (Herbs) and cereals (for list of species see methods) 1976–1986 2010–2016 Trees Herbs Cereals Trees Herbs Cereals n n/100 n n/100 n n/100 n n/100 n n/100 n n/100 Adalia bipunctata 585 (9.81) 1,290 (26.77) 10 (0.04) 416 (0.45) 130 (0.32) Adalia conglomerata (L.) 1 (0.00) Adalia decempunctata 209 (3.33) 11 (0.15) 2 (0.01) 1,150 (0.98) 16 (0.04) 1 (0.00) Anatis ocellata (L.) 7 (0.09) 1 (0.00) 8 (0.01) 1 (0.00) Aphidecta obliterata (L.) 4 (0.04) 83 (0.07) 1 (0.00) Calvia decemguttata (L.) 9 (0.22) 443 (0.44) 2 (0.01) 1 (0.00) Calvia quatuordecimguttata 19 (0.35) 11 (0.24) 287 (0.28) 38 (0.09) 5 (0.01) Ceratomegilla undecimnotata 251 (0.72) 2 (0.00) Chilocorus bipustulatus (L.) 38 (0.03) 1 (0.00) Coccidula rufa (Hbst.) 6 (0.13) Coccinella quinquepunctata 54 (1.76) 58 (1.00) 295 (1.39) 29 (0.02) 425 (0.69) 57 (0.13) Coccinella septempunctata 105 (1.32) 593 (12.27) 3,603 (13.46) 1,151 (0.99) 3,617 (7.30) 2,715 (5.87) Coccinella undecimpunctata 1 (0.02) 164 (3.49) 19 (0.08) Coccinulla quatuordecimpustulata (L.) 3 (0.01) Exochomus quadripustulatus (L.) 2 (0.03) 1 (0.02) 269 (0.26) 2 (0.00) Halyzia sedecimguttata (L.) 138 (0.15) 5 (0.01) Harmonia quadripunctata (Pontoppidan) 24 (0.02) Hippodamia septemmaculata (DeGeer) 2 (0.01) 1 (0.00) Hippodamia variegata 3 (0.02) 207 (4.34) 8 (0.03) 4 (0.00) 1,657 (3.20) 105 (0.26) Oenopia conglobata (L.) 34 (0.56) 16 (0.34) 358 (0.32) 3 (0.01) Propylea quatuordecimpunctata 259 (2.93) 192 (3.67) 1,398 (5.09) 462 (0.42) 549 (1.14) 1,264 (2.92) Psyllobora vigintiduopunctata (L.) 2 (0.01) 117 (0.11) 391 (0.90) 10 (0.02) Rhyzobius litura (F.) 5 (0.01) 2 (0.00) Scymnus sp. 1 (0.02) 18 (0.02) 10 (0.02) 2 (0.00) Subcoccinella vigintiquatuorpunctata (L.) 48 (0.03) 47 (0.11) 15 (0.04) Tytthaspis sedecimpunctata (L.) 2 (0.00) 383 (0.97) 103 (0.22) 1976–1986 2010–2016 Trees Herbs Cereals Trees Herbs Cereals n n/100 n n/100 n n/100 n n/100 n n/100 n n/100 Adalia bipunctata 585 (9.81) 1,290 (26.77) 10 (0.04) 416 (0.45) 130 (0.32) Adalia conglomerata (L.) 1 (0.00) Adalia decempunctata 209 (3.33) 11 (0.15) 2 (0.01) 1,150 (0.98) 16 (0.04) 1 (0.00) Anatis ocellata (L.) 7 (0.09) 1 (0.00) 8 (0.01) 1 (0.00) Aphidecta obliterata (L.) 4 (0.04) 83 (0.07) 1 (0.00) Calvia decemguttata (L.) 9 (0.22) 443 (0.44) 2 (0.01) 1 (0.00) Calvia quatuordecimguttata 19 (0.35) 11 (0.24) 287 (0.28) 38 (0.09) 5 (0.01) Ceratomegilla undecimnotata 251 (0.72) 2 (0.00) Chilocorus bipustulatus (L.) 38 (0.03) 1 (0.00) Coccidula rufa (Hbst.) 6 (0.13) Coccinella quinquepunctata 54 (1.76) 58 (1.00) 295 (1.39) 29 (0.02) 425 (0.69) 57 (0.13) Coccinella septempunctata 105 (1.32) 593 (12.27) 3,603 (13.46) 1,151 (0.99) 3,617 (7.30) 2,715 (5.87) Coccinella undecimpunctata 1 (0.02) 164 (3.49) 19 (0.08) Coccinulla quatuordecimpustulata (L.) 3 (0.01) Exochomus quadripustulatus (L.) 2 (0.03) 1 (0.02) 269 (0.26) 2 (0.00) Halyzia sedecimguttata (L.) 138 (0.15) 5 (0.01) Harmonia quadripunctata (Pontoppidan) 24 (0.02) Hippodamia septemmaculata (DeGeer) 2 (0.01) 1 (0.00) Hippodamia variegata 3 (0.02) 207 (4.34) 8 (0.03) 4 (0.00) 1,657 (3.20) 105 (0.26) Oenopia conglobata (L.) 34 (0.56) 16 (0.34) 358 (0.32) 3 (0.01) Propylea quatuordecimpunctata 259 (2.93) 192 (3.67) 1,398 (5.09) 462 (0.42) 549 (1.14) 1,264 (2.92) Psyllobora vigintiduopunctata (L.) 2 (0.01) 117 (0.11) 391 (0.90) 10 (0.02) Rhyzobius litura (F.) 5 (0.01) 2 (0.00) Scymnus sp. 1 (0.02) 18 (0.02) 10 (0.02) 2 (0.00) Subcoccinella vigintiquatuorpunctata (L.) 48 (0.03) 47 (0.11) 15 (0.04) Tytthaspis sedecimpunctata (L.) 2 (0.00) 383 (0.97) 103 (0.22) Total number of adults (n) and average abundance (n individuals × 100 sweeps−1, n/100) in brackets, bold figures indicate dominant species in terms of abundance. View Large Fig. 3. View largeDownload slide Abundance of adults of native coccinellids on trees, low-growing herbaceous plants (Herbs) and cereals in two periods, 1976–1986 and 2010–2016. Statistically significant differences between plants within periods (Tukey post-hoc tests, P < 0.05) are indicated by different letters. Differences between the periods for particular plants are all significant. Bars are means (±SE). Fig. 3. View largeDownload slide Abundance of adults of native coccinellids on trees, low-growing herbaceous plants (Herbs) and cereals in two periods, 1976–1986 and 2010–2016. Statistically significant differences between plants within periods (Tukey post-hoc tests, P < 0.05) are indicated by different letters. Differences between the periods for particular plants are all significant. Bars are means (±SE). Discussion Harmonia axyridis was the most abundant coccinellid on trees, but it only occurred at low abundance (only a few individuals) on herbaceous plant and cereals. Other studies across Europe that considered the abundance patterns of coccinellids on different host plants are consistent with the findings from our study in the Czech Republic, with a high frequency of H. axyridis on trees (Vandereycken et al. 2012) and Urtica (Alhmedi et al. 2007) and a low abundance on most other herbaceous plants and field crops except maize (Vandereycken et al. 2013a,b). However, this scenario is not the case further afield. In North America, H. axyridis is abundant on cotton (Conway and Kring 2010), maize (Musser and Shelton 2003, Hesler and Kieckhefer 2008), potato (Alyokhin and Sewell 2004), soybean (Hesler 2014), and wheat (Nault and Kennedy 2003) while in Chile it occurs nearly exclusively on alfalfa (Grez et al. 2014, 2016). The variation in host plant preference globally may be a consequence of the global genetic diversification of the populations (Lombaert et al. 2010), variations in flight capacity (Lombaert et al. 2014), and opportunistic preferences for anthropogenic habitats (Sloggett 2017). Within the native range of H. axyridis, there is also a considerable variability in host plant associations, with a low relative abundance on field crops in eastern Siberia (Kuznetsov and Pinsker 1973, Arefin and Ivliev 1988) but a high abundance on crops in Japan (Komai and Hosino 1951) and China (Liu et al. 2012). In contrast, the occurrence of H. axyridis on trees is consistently high across its native range (Kuznetsov 1972, Osawa 2011, Dong et al. 2015) and in areas it has recently colonized (Brown 2002, Michaud 2002, Frechette et al. 2008, Milleo et al. 2008, Johnson and Giliomee 2012, Torres-Acosta and Sanchez-Pena 2015). In North and South America, recently arrived H. axyridis apparently outcompetes native species on crops (Diepenbrock and Finke 2013, Diepenbrock et al. 2016, Grez et al. 2016). One reason for this scenario could be the larger body size of H. axyridis compared to that of the native species. A larger body size is advantageous in both competitive interactions and intraguild predation. Crop habitats are populated by small native species (e.g., Hippodamia convergens Guerin, H. quinquesignata (Kirby), and H. sinuata Mulsant in North America). The large non-native species, C. septempunctata and H. axyridis, largely replace the small native species, which may survive and coexist only if they are temporally (Kajita et al. 2000, Kajita and Evans 2010) or spatially segregated (Evans 2004). In contrast, European coccinellid communities on cereals are dominated by the large C. septempunctata (Honek and Rejmanek 1982, Nedved 1999), which has endured the competition from H. axyridis and remained the dominant species in crops and most herbaceous stands even after the arrival of H. axyridis. Similarly, in the Eastern Palearctic, these two species can coexist because of spatial niche segregation: H. axyridis occupies trees and C. septempunctata herbaceous plant stands (Takahashi 1987). In contrast to the large differences in abundance, there was little difference in the duration of persistence of H. axyridis and native coccinellids. Adults were present when the plant foliage was lush and infested with prey. On trees, coccinellids persisted from leaf appearance in late April–early May until leaf fall in late October–early November. Over the course of a growing season, stands of herbaceous plants may be regenerated by cutting (Urtica), or the development of plants may occur at different times during the vegetative season (Tripleurospermum), and coccinellids can persist on such vegetation for long periods. Native coccinellids, particularly C. septempunctata, move readily from patch to patch throughout the vegetative season (Honek 1989), while H. axyridis only occupies low-growing patches of vegetation when aphids are abundant on these plants, i.e., in late May to early July (Honek et al. 2015). Consequently, native coccinellids remain longer in patches of wild herbaceous plants than H. axyridis. On cereals, the abundance of prey depends to a large extent on the stage of development of the crop. Coccinellids arrive following aphid immigration (May) and leave when the crop matures (July). Evaluating the effect of invasive alien species on native species is critical for biodiversity conservation. Several mechanisms can explain the common persistence of native species and H. axyridis: temporal and spatial segregation of native coccinellid and H. axyridis populations and physical resistance of native species to intraguild predation or competitive exploitation. On trees, Adalia decempunctata (L.) and Calvia quatuordecimguttata (L.) were able to persist following the arrival of H. axyridis, but their abundance was reduced (Honek et al. 2016). The survival of A. decempunctata populations may be an example of temporal segregation. It appears to be facilitated by alternating temporal presence of both species on trees where A. decempunctata dominates coccinellid communities until early June and is then replaced by H. axyridis (Honek et al. 2015). An example of physical resistance may be Ca. quatuordecimguttata. This species may have thrived because the large and mobile larvae may resist intraguild predation by H. axyridis (Ware and Majerus 2008); this endurance is further supported by the chemical protection of its eggs (Ware et al. 2008b). An example of spatial segregation was already addressed: C. septempunctata and P. quatuordecimpunctata successfully resist competition of H. axyridis because their breeding takes place mostly on crops and herbs (Honek and Rejmanek 1982, Honek 1985) where the latter species is not abundant. Native coccinellid communities were 2–4 times more abundant in the 1980s than in the 2010s (Fig. 2). The large decrease in the abundance of native species was apparent on all plants, regardless of the abundance of H. axyridis. However, the change in abundance was most pronounced on trees where H. axyridis was abundant and least on cereals where its presence was sporadic. These differences again show the importance of the overall negative effect of H. axyridis on the abundance of native coccinellids. In summary, the data from 2010 to 2016 provide quantitative evidence of the abundance and persistence of adult and larval coccinellids on different plants. While H. axyridis occurs mainly on trees, native coccinellids were most abundant (in terms of individuals) on herbaceous plants, followed by cereals and trees. A comparison with data from 1976 to 1986 revealed a general decrease in the abundance of native coccinellids but with variation in the extent of the decrease on particular plants, which is inversely correlated with the abundance of H. axyridis. It is clear that coccinellids and other insects are undergoing rapid large-scale changes in distribution and abundance (Hickling et al. 2006) as well as small-scale changes within habitats and on particular plants. Such changes are likely to be due to a number of interacting factors. The spread of invasive alien species is one such threat. However, the decrease in the overall abundance of native coccinellids, as outlined here, is unlikely to be due solely to the presence of H. axyridis. The decline in the abundance of A. bipunctata on planted (Honek et al. 2016) and forest trees (Nedved 2014) and of C. septempunctata on herbaceous plants and cereals (Honek and Martinkova 2005, Bianchi et al. 2007, Honek et al. 2016) was apparent before the arrival of H. axyridis. Other changes in native coccinellid communities are also not explained by the arrival of H. axyridis, e.g., the extinction of Coccinella undecimpunctata L. in the area of this study, the general decline in the abundance of Coccinella quinquepunctata L. or, in contrast, the increased abundance of the thermophilous Ce. undecimnotata and H. variegata. (Honek et al. 2014). 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TI - Differences in the Phenology of Harmonia axyridis (Coleoptera: Coccinellidae) and Native Coccinellids in Central Europe
JF - Environmental Entomology
DO - 10.1093/ee/nvy173
DA - 2019-02-13
UR - https://www.deepdyve.com/lp/oxford-university-press/differences-in-the-phenology-of-harmonia-axyridis-coleoptera-rXJIUZ3Pw3
SP - 80
VL - 48
IS - 1
DP - DeepDyve
ER -