Cent. Eur. J. Biol. • 7(3) • 2012 • 487-494 DOI: 10.2478/s11535-012-0034-3

Central European Journal of Biology

Biology and ecology of Appendiseta robiniae (: Aphidoidea) – an alien species in Europe

Research Article

Beata Borowiak-Sobkowiak1,*, Roma Durak2

1Poznań University of Life Sciences, Department of Entomology and Environmental Protection, 60-594 Poznań, Poland 2University of Rzeszów, Department of Invertebrate Zoology, 35-601 Rzeszów, Poland

Received 16 December 2011; Accepted 06 March 2012

Abstract: Elements of the biology and ecology of A. robiniae were studied in Poland during the period of 2008–2009. The term of spring hatching, number of generations per season, developmental time of particular generations, lifespan of specimens and fecundity of particular generations were all defined. The dynamics of the species’ occurrence on its host plant were also determined. The two-year study showed a maximum of 11 generations can develop on Robinia pseudoacacia. Females of the second and third generations were found to be the most fertile. These findings indicate that the species has adapted well in Poland and its biological predispositions have enabled it to rapidly increase in population.

Keywords: Robinia pseudoacacia • Bionomy • Development • Abundance dynamics © Versita Sp. z o.o.

1. Introduction on R. neomexicana var. albiflora Kusche or Sephora japonica L. [5,7,11]. In Europe, black locust is often Appendiseta robiniae (Gillette, 1907) is the only planted along streets and in parks, especially in large representative of the genus Appendiseta Richards, cities, because it tolerates pollution well. It is highly 1965. According to Heie and Wegierek [1] this valued as nectar bearing plant. species belongs to the family Drepanosiphidae, The current literature covering the biology of subfamily , tribe Panaphidini, subtribe A. robiniae includes no detailed data referring to its Panaphidina. specific biology. Adult morphs and development of larval A. robiniae is a Nearctic species commonly found instars have been described so far [6,12,13]; however, in some areas of North America [2,3] on black locust as of yet, other aspects of its biology have not been (Robinia pseudoacacia L) trees. Along with the plant, examined in detail. the species was carried to the Neotropics [4] and, most The aim of this study was to describe the unknown importantly, to the Western Palearctic [5,6], where elements of A. robiniae biology and establish whether favourable habitat conditions allowed the species to its adaptation to Poland’s climate would facilitate rapid flourish. This species has been found in central and population growth. This involved determining the term southern Europe [7]; however, in Poland, A. robiniae of spring hatching, as well as the number of generations has been recorded only twice, in central and western per season, developmental time, individual lifespan areas of the country [8,9]. and fecundity in particular generations. In addition to A. robiniae is described as an alien species in Europe observing in insectary conditions, a field study was [10]; a holocyclic, monoecious, monophagous species conducted in order to specify the term of species feeding on R. pseudoacacia, and only exceptionally occurrence and its dynamics on its host plant.

* E-mail: [email protected] 487 Biology and ecology of Appendiseta robiniae (Hemiptera: Aphidoidea) – an alien species in Europe

2. Experimental Procedures D is the developmental period from birth to the beginning of the first reproduction (pre-reproductive

2.1 reared in insectary conditions period) and Md is the number of nymphs produced by Studies on the biology of A. robiniae were conducted the adult in the first D days of reproduction after the adult in insectary conditions in the garden of the Chair of moult. The aphids were reared in a climate chamber Entomology, Poznań University of Life Sciences, Poland, (Sanyo) at a constant temperature of 20°C, 70% relative from 2008 to 2009. The aphids were isolated on the humidity and a 16:8 h L:D photoperiod. stems of R. pseudoacacia L. A single parthenogenetic female was placed under each isolator (gauze cage). 2.3 Abundance dynamics studies The first larvae they gave birth to would mark the In order to determine the abundance dynamics of beginning of a new generation. The female was then A. robiniae on R. pseudoacacia, samples of 10 leaves moved to a new isolator, where her fecundity was studied. from 10 trees were collected between May and October Parthenogenetic females of particular generations were in monthly intervals. Both adults and larvae were observed in terms of the length of pre-reproductive, included in the sample. reproductive and post-reproductive periods throughout their lifespan. The development of five females in each 2.4 Meteorological conditions generation was studied. Observations were conducted Meteorological data came from the Meteorological from April to the end of November. Station Poznań-Marcelin (Figures 1, 2), which is situated During autumn, sexuparae generation was observed 3 km from where the research was conducted. in the order of rearing amphigonic females and males. With this aim in mind, subsequent larvae were bred 2.5 Statistical analysis under separate isolators until they reached maturity. The statistical analysis, conducted using a Kruskal-Wallis In order to define a fecundity index for amphigonic test, examined the data on particular developmental females, a dissection of 30 mature females was stages of generations, the total lifespan and fecundity. performed. Differences in developmental stages: pre-reproductive, reproductive, post-reproductive, total lifespan and 2.2 Aphids reared in controlled conditions fecundity, between subsequent generations in vegetation

The intrinsic rate of increase (rm) was calculated with seasons were compared. The data was analyzed the Wyatt and White formula [14,15], which relates the separately for 2008 and 2009 and between years. To fecundity of an individual aphid to its development time: determine any relationship between developmental

rm=(lnMdx0,738)/D. stages and temperature, non-parametric correlations

Figure 1. Meteorological conditions in Poznań in 2008.

488 B. Borowiak-Sobkowiak, R. Durak

Figure 2. Meteorological conditions in Poznań in 2009.

(Spearman rank correlation) were used. Duration of June temperatures. The reproductive period lasted pre-reproduction, reproduction, and post-reproduction between 11 to 36 days on average (Table 1). The periods; longevity and average maximum temperature; longest average reproduction period in 2008 was average minimum temperature; and average daily noted for the fundatricae and females of the fourth and temperature in 2008 and 2009 were examined. The data seventh generations, whereas in 2009, the females of was statistically analysed using StatSoft, Inc. (2010), the eighth generation reared the longest (approximately STATISTICA, version 9.0, (www.statsoft.com). 36 days) followed by females in the second and ninth generations (Figure 3). The shortest reproductive stage was reported in the seventh and tenth generations in 3. Results 2009 (11 days on average). The post-reproductive period most frequently lasted Viviparous females in all generations were found to from 0 to 9 days (Figure 3). It lengthened in the last be winged, while in the sexual generation apterous three generations, lasting up to 20 days for the tenth oviparae and alate males occurred. The aphids infested generation of females in 2009 (Table 1). The second, leaves, feeding along ribs. The fundatricae hatched third and eighth generations took the longest to develop, from eggs at the end of April, during the stage when typically around 50 days (Table 1). the firstR. pseudoacacia leaves started to grow. Across The statistical analysis revealed significant the two study seasons, 10 (9 parthenogenetic and differences in the development of particular aphid 1 sexual) generations were noted in 2008 and 11 (10 generations in 2008. Significant differences in the length parthenogenetic and 1 sexual) in 2009 (Figure 3). The of development were observed in the pre-reproductive first stage of ontogenesis of parthenogenetic females, stage between generations 1 and 2, 2 and 3, 3 and namely the pre-reproductive stage, took 11 to 24 4, 2 and 5, and 3 and 8 (H=39.79; P≤0.05) (Table 1). days on average (Table 1). The longest average pre- Generations did not differ significantly in the length reproductive stage (about 20 days) was reported in 2008 of reproductive or post-reproductive stages or in their for females of the second and eighth generations, and in lifespan. 2009 for the third and tenth generations (Figure 3). The Significant statistical differences were observed shortest average pre-reproductive stage took 11 days between generations during the 2009 vegetation and occurred in the third generation of the 2008 season. season. The differences were mainly found in the This may have been caused by rather unusually high lengths of pre-reproductive stages between generations

489 Biology and ecology of Appendiseta robiniae (Hemiptera: Aphidoidea) – an alien species in Europe

Figure 3. The average length of developmental stages of parthenogenetic females of A. robiniae on Robinia pseudoacacia in insectary conditions in 2008-2009.

Average length of development stages in days Year Generation Overall longevity Prereproduction Reproduction Postreproduction

2008 1 13.2 (12-16) [2**] 30 (22-42) 0 43.2 (36-54)

2 20.4 (18-21)[1**, 3***, 5**] 26 (21-31) 0.4 (0-2) 46.8 (42-53)

3 11 [2***, 4**, 8***] 27 (19-41) 2 (0-6) 40 (30-56)

4 18.2 (18-19) [3***] 28.6 (21-37) 0 46.8 (39-55)

5 13.4 (13-15) [2**] 22.6 (10-39) 1.4 (0-4) 37.4 (27-55)

6 14 17.4 (14-22) 0 31.4 (28-36)

7 16 29.8 (22-40) 2.6 (0-5) 48.4 (42-56)

8 20 [3***] 25.4 (15-36) 3.6 (0-8) 49 (41-64)

9 16.4 (15-20) 26.4 (13-42) 4.4 (0-10) 47.2 (36-72)

2009 1 17.4 (11-22) 23.8 (8-32) 2.8 (0-7) 44 (22-60)

2 19.2 (17-22) 33 (29-37) [7*, 10*] 3.2 (0-6) 55.4 (52-60) [7*]

3 21 [4*] 26.8 (14-30) 1.2 (0-2) 48.6 (37-53)

4 14 [3*, 10***] 16 (10-28) 2.8 (0-4) 32.8 (28-45)

5 14.8 (14-16) [10**] 21.6 (14-39) 0.4 (0-2) 34.8 (28-43)

6 14 (11-17) [10**] 16.8 (13-26) 0 30.8 (27-37)

7 16 11.8 (10-17) [2*] 1.8 (0-5) 29.6 (26-33) [2*]

8 16.6 (15-19) 35.8 (21-53) 2.8 (0-11) 55.2 (36-79)

9 15.6 (14-16) 32.2 (13-54) 4 (1-7) 51.8 (30-74)

10 24.2 (23-26)[4***, 5**, 6**] 11 [2*] 9 (3-20) 44.2 (34-54)

Table 1. Length of developmental stages of parthenogenetic females of A. robiniae in insectary conditions in 2008-2009 (mean (min–max); in square brackets – number of generation in which statistical differences occurred; significance levels * P≤0,05, ** P≤0,01, *** P≤0,001).

490 B. Borowiak-Sobkowiak, R. Durak

3 and 4, 4 and 10, 5 and 10, 6 and 10 (H=33.66; P≤0.05) fecundity of 12.7 eggs per female was found. Bred females (Table 1). Further significant statistical differences consistently laid their first eggs at the end of September. were observed in the 2009 data for the reproductive The intrinsic growth rate (rm) was calculated to stage length between generations 2 and 7, and determine the fitness of A. robiniae. Under constant

2 and 10 (H=28.03; P≤0.05) (Table 1). Generations 2 conditions, rm was 0.1843 ♀/♀ a day. and 7 differed significantly in their lifespan (H=27.01; In the field, the highest abundance of aphids on the P≤0.05). No significant differences were found in the host plant was recorded in June and July in both study post-reproductive stage. years. In other months the infestation level was low Differences were also found between particular (Figure 4). generations developing in 2008 and 2009: generation The meteorological variables were closely correlated 1 significantly differed in post-reproductive stage to pre-reproduction periods in 2008 and 2009. The length (H=5.58; P≤0.05) and fecundity (H=3.93; average maximum temperature (2008: R=-0.353, P≤0.05). Generation 2 showed significant differences in P≤0.01; 2009: R=-0.526, P≤0.001), average minimum reproductive stage length (H=4.84; P≤0.05) as well as temperature (2009: R=-0.564, P≤0.001) and average lifespan (H=4.84; P≤0.05). In generation 3, differences daily temperature (2009: R=-0.499, P≤0.001) were were found in pre-reproductive stage length (H=9.00; significantly negative-correlated with pre-reproduction P≤0.05), while in generation 4 significant differences of A. robiniae. were found within the pre-reproductive stage (H=8.33; P≤0.05), reproductive stage (H=4.41; P≤0.05), post-reproductive stage (H=5.62; P≤0.05) and 4. Discussion lifespan (H=5.44; P≤0.05). Generation 5 differed in the pre-reproductive stage length during consecutive seasons In Polish conditions, the first larvae of A. robiniae (H=4.33; P≤0.05). There were no significant differences hatched from wintering eggs at the end of April. The in the development of generation 6. Differences in exact timing depended on the weather conditions and generation 7 occurred in the reproductive stage (H=6.98; the R. pseudoacacia phenology. P≤0.05) and lifespan (H=6.94; P≤0.05). Generation 8 Across the two study seasons, a maximum of 11 was significantly different in pre-reproductive stage length generations of A. robiniae were found. The species has (H=8.03; P≤0.05), and finally, no significant statistical more generations than its relatives, such as Panaphis differences were found in generation 9. juglandis (Goetz.) [16] or fagi L. [17], which The highest fecundity was noted for the second were reported to have only 8 generations. generation of parthenogenetic females in 2008, with an average of 95.6 and a maximum of 136 larvae per female (Table 2). In the 2009 season, the highest fecundity Fecundity by virginoparae Generation was noted for the females of the third generation (82.2 2008 2009 larvae per female on average). The fecundity of females 1 77.6 (50-119) [9*] 44.6 (17-57) decreased noticeably in summer generations. Also, the sexual generation was characterized by low fecundity. 2 95.6 (63-136) [9**] 55.8 (32-104) Analysis revealed significant differences in the fecundity 3 63.4 (52-81) 82.2 (26-117) [10**] of particular aphid generations in 2008, between generations 1 and 9 and also 2 and 9 (H=24.73; P≤0.05) 4 68.4 (43-97) 72.4 (48-112) [10**] (Table 2). Female fecundity within generations in 2009 5 37.8 (16-81) 45.6 (11-86) was similar, with significant differences occurring only between generations 3 and 10, and 4 and 10 (H=20.74; 6 43 (30-65) 46.4 (21-72) P≤0.05) (Table 2). 7 50.2 (26-74) 34.2 (21-55) The sexuparae females that appeared at the end of 8 63.8 (46-83) 65.6 (31-117) August most frequently bred amphigonic generation females and then males. Females which bred only 9 23.2 (15-28) [1*, 2**] 65 (22-125) amphigonic generation females were also observed, as 10 9.8 (7-16) [3**, 4**] well as those which first bred males and then amphigonic generation females and parthenogenetic females. In late Table 2. Fecundity of parthenogenetic females of A. robiniae in autumn, specimens rearing only parthenogenetic females insectary conditions in 2008-2009 (mean (min–max); in were observed in the bred colonies. On the basis of square brackets – number of generation in which statistical differences occurred; significance levels * P≤0,05, ** dissection of 30 mature females, a mean oviparous female P≤0,01).

491 Biology and ecology of Appendiseta robiniae (Hemiptera: Aphidoidea) – an alien species in Europe

Figure 4. Number of A. robiniae on Robinia pseudoacacia in field conditions in 2008-2009.

The pre-reproductive stage for parthenogenetic generations. Similar observations were reported by females took from 11 to 26 days, and fluctuations in Prabucki [17] when studying the development of P. fagi. temperature during the season resulted in shortening or In Poland, most of the studies of aphid biology have lengthening of the period. been conducted on the family . It was shown Higher temperatures stimulated faster aphid that in species such as Rhopalosiphum insertum (Walk.) development; however, temperatures above 30oC impaired [18], Hyalopterus pruni (Geoff.) [19], Myzus cerasi (F.) it. Statistical analyses corroborate our observations and [20], Hyperomyzus pallidus HRL [21], Phorodon humuli biological experiments, clearly indicating the impact of Schr. [22], Aphis idaei v.d. Goot [23], or Amphorophora temperature on the length of pre-reproductive stages idaei (Börn) [24], it was the fundatrices that were of subsequent aphid generations. Obvious differences characterised by the highest fecundity. This finding was were found between those generations developing in not confirmed for A. robiniae. optimal temperatures for aphids - about 20oC - and the The average lifespan of the species appears to be generations at the end of the vegetation season, when relatively long. The females of the studied generations the temperatures were lower. lived for 43 days in 2008 and 42 days in 2009. It is worth The species reproductive stage length remained noting that lifespan is influenced mainly by the fluctuating comparatively stable, at 24 days for most generations. length of the pre-reproductive stage between generations. Temperature had a significant effect on the length Temperature and short photoperiod are important of developmental time of aphids: our study showed factors in the induction of sexual morphs. Sexual temperature influence mainly in pre-reproduction. No morphs are produced at shorter day lengths and at demonstrated effect of temperature was observed on lower temperatures, resulting in sexuals being produced the reproduction and post-reproduction periods, except earlier in the year when autumn is cool [15]. This study in individual generations. High temperatures of around established that, besides the sexuparae generation, 30oC represented a critical point for the aphids. It follows the development cycle also includes a generation prereproduction is the most dependent on the weather of parthenogenetic females of virgino-sexuparae conditions among development stages. character. Larvae born by that generation developed Significant differences were found in the female into oviparae females, males or parthenogenetic fecundity of spring and autumn generations. females. Similar observations were made for Aphis Our study confirmed the highest fecundity of female idaei and Amphorophora idaei [23,24] as well as aphids developing in the initial months of vegetation Betulaphis helvetica H.R.L. [25]. Karwańska [25] claims season and a drop in fecundity in subsequent that this indicates that B. helvetica may develop in an

492 B. Borowiak-Sobkowiak, R. Durak

anholocyclic manner. This suggests that A. robiniae In Poland, the species was only recorded relatively could continue the development of parthenogenetic recently, and was found to be most abundant on the host females in favourable temperatures below the critical plant in June and July. The dynamics of its occurrence temperature level. The character of the order of breeding are typical of many tree-infesting species. The results by sexuparae – first amphigonic females, then males, or of our research indicate that the species has adapted first males, and then females, or only females or males, very well in Poland (in western Poland two more sites ensures that the species are subject to considerable of A. robiniae have been found; unpublished data). Its gender mixing. Genetic diversity enhances adapting biological predispositions enable it to expand quickly, abilities, which makes the species dynamic and as is corroborated by the data from Croatia, where the expansive in different conditions. species has occurred as a result of active dispersion. In The oviposition period for A. robiniae, which in Poland Croatia, A. robiniae is now reaching the dominant status falls at the end of September, corresponds with the among the species caught in Rothamsted suction traps relevant data of another species of the same subfamily, (RST) [27].

Panaphis juglandis [16]. The intrinsic growth rate (rm) of the studied species was comparatively high and comparable with the species considered to be damaging Acknowledgements pests, such as Aphis idaei [23], Amphorophora idaei, [24] or Aphis gossypii Gloger, developing on sweet We would like to express our gratitude to Ms Katarzyna pepper [26]. Sztukowska for the help in aphid rearing.

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