Thermal Requirements and Effect of Temperature and Prey on the Development of the Predator Harmonia Axyridis

PHYSIOLOGICAL ECOLOGY Thermal Requirements and Effect of Temperature and Prey on the Development of the Predator Harmonia axyridis

GEORGE J. STATHAS,1,2 DIMITRIOS C. KONTODIMAS,3 FILITSA KARAMAOUNA,3 1 AND STAVROS KAMPOURIS

Environ. Entomol. 40(6): 1541Ð1545 (2011); DOI: http://dx.doi.org/10.1603/EN10240 Downloaded from https://academic.oup.com/ee/article/40/6/1541/532414 by guest on 23 September 2021 ABSTRACT Thermal requirements (lower temperature threshold and thermal constant) for the development of each developmental stage of the predator Harmonia axyridis (Pallas) were studied on Aphis fabae Scopoli and Dysaphis crataegi (Kaltenbach) under controlled laboratory conditions. The effect of temperature (15, 20, 25, and 30ЊC) and prey species was examined on pre-imaginal developmental duration and life cycle (pre-oviposition period included) of the predator. Our results suggest comparable thermal requirements for the development of H. axyridis on the particular prey and when compared with other aphid species. The total preimaginal development of H. axyridis,at 15, 20, and 30ЊC, and its life cycle, at 15 and 30ЊC, are shorter on D. crataegi than on A. fabae.

KEY WORDS aphids, predator, pumpkin, rearing, thermal thresholds

The predator Harmonia axyridis (Pallas) (Coleoptera: posed, therefore the lower developmental threshold t Coccinellidae) was introduced into Greece from and the day-degree requirements for their develop- France for the control of aphids in central and south- ment (thermal constant K) may be useful indicators of ern Greece from 1994 to 1999, where it was released an insectÕs potential distribution (Messenger 1959). at various crop and ornamental plant production sites The relationship between the development rate and (Katsoyannos et al. 1997; Kontodimas et al. 2008a,b). temperature is usually curvilinear (Davidson 1944, Mass rearing of H. axyridis for the purpose of re- Sharpe and DeMichele 1977, Mills 1981). However, leases was performed on two aphid species, Aphis within the limits of a certain temperature range, this fabae Scopoli and Dysaphis crataegi (Kaltenbach) relationship is linear, allowing an estimate of the lower (Hemiptera: Aphididae) under controlled laboratory developmental threshold and thermal constant using conditions in the insectary of Benaki Phytopatholog- the linear model by Campbell et al. (1974). ical Institute, Athens (Kontodimas et al. 2008a,b). The inßuence of food quality and quantity on the Aphis fabae is one of the most abundant species, to- developmental rate of an aphidophagous predator gether with Aphis craccivora Koch, Myzus persicae (species and number of supplied aphids per day) is (Sulzer) and Toxoptera aurantii (Boyer de Fonsco- well documented (Hodek and Hone˘k 1996). Never- lombe) (all of them Hemiptera: Aphididae) in citrus theless, in the case of H. axyridis, both the species of and vegetables in Greece, including the areas of the aphid preyed upon and the host-plant the aphids de- predatorÕs release. Dysaphis crataegi also is a pest in velop on can affect its larval developmental time (Hu- vegetables, although of less importance compared kusima and Kamei 1970, Koch 2003, Reznik 2010). with A. fabae (Katsoyannos 1996, Katsoyannos et al. This project aims at estimating the thermal require- 1997, Tzanakakis and Katsoyannos 2003). ments for development (lower developmental thresh- Harmonia axyridis proved to be an important bio- old t and thermal constant K) of all immature stages of logical control agent during the release seasons, but the predator H. axyridis, which may give some insight follow-up surveys at the release sites during 1994Ð2007 into the reasons for the difÞculty of H. axyridis to indicated the inability of the predator to establish in overwinter successfully in Greece. Also, the effect of Greece, as reported in Portugal and Spain (Brown et temperature and different prey (two indicatory aphid al. 2008). Harmonia axyridis imposed no adverse ef- species, A. fabae and D. crataegi) on the development fects on the native coccinellid fauna in Greece (Kon- of the predator will be examined. todimas et al. 2008a,b). The developmental rate of insects depends on the Materials and Methods environmental temperature to which they are ex- Insect Rearing. Individuals of H. axyridis used in the 1 Technological Educational Institute of Kalamata, 24100-Anti- experiments originated from a colony imported from kalamos, Greece. France and established at Benaki Phytopathological 2 Corresponding author, e-mail: [email protected]. 3 Benaki Phytopathological Institute, 8 St. Delta str, 14561-KiÞssia, Institute in 1994 (Katsoyannos et al. 1997). Harmonia Greece. axyridis was reared on the aphids A. fabae and D.

0046-225X/11/1541Ð1545$04.00/0 ᭧ 2011 Entomological Society of America 1542 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 6

Table 1. Developmental duration of Harmonia axyridis (mean ؎ SEM) on the prey Aphis fabae and Dysaphis crataegi at four constant temperatures (15, 20, 25, and 30°C)

15ЊC20ЊC Developmental stage A. fabae D. crataegi A. fabae D. crataegi

Egg 10.45 Ϯ 0.44a (n ϭ 25) ͓10Ð11͔ 9.25 Ϯ 0.26b (n ϭ 25) ͓9Ð9.5͔ 5.00 Ϯ 0.28a (n ϭ 25) ͓4.5Ð5.5͔ 4.74 Ϯ 0.25b (n ϭ 25) ͓4.5Ð5͔ L1 8.08 Ϯ 1.00a (n ϭ 23) ͓7Ð10͔ 5.14 Ϯ 0.74b (n ϭ 24) ͓4Ð6.5͔ 3.50 Ϯ 0.52a (n ϭ 24) ͓3Ð4͔ 3.00 Ϯ 0.14b (n ϭ 24) ͓2.5Ð3.5͔ L2 7.55 Ϯ 1.29a (n ϭ 22) ͓6Ð10͔ 5.29 Ϯ 0.67b (n ϭ 24) ͓4.5Ð7͔ 3.00 Ϯ 0.52a (n ϭ 24) ͓2Ð4͔ 2.35 Ϯ 0.49b (n ϭ 24) ͓2Ð3͔ L3 7.73 Ϯ 0.90a (n ϭ 21) ͓6Ð9͔ 6.33 Ϯ 0.87b (n ϭ 24) ͓5Ð8͔ 3.53 Ϯ 0.64a (n ϭ 24) ͓3Ð5͔ 3.05 Ϯ 0.21b (n ϭ 24) ͓3Ð4͔ L4 17.40 Ϯ 1.14a (n ϭ 22) ͓16Ð19͔ 14.78 Ϯ 1.30b (n ϭ 24) ͓13Ð17͔ 8.17 Ϯ 1.03a (n ϭ 24) ͓7Ð10͔ 6.95 Ϯ 0.58b (n ϭ 24) ͓6Ð8͔ Pupa 18.80 Ϯ 2.77a (n ϭ 22) ͓16Ð23͔ 14.56 Ϯ 0.82b (n ϭ 24) ͓13Ð16͔ 7.65 Ϯ 0.49a (n ϭ 23) ͓7Ð10͔ 7.78 Ϯ 0.42a (n ϭ 24) ͓7Ð8͔ Total pre-imaginal 70.20 Ϯ 2.14a (n ϭ 22) ͓69Ð74͔ 56.58 Ϯ 2.82b (n ϭ 24) ͓53.5Ð60.5͔ 28.43 Ϯ 1.13a (n ϭ 23) ͓27Ð30͔ 26.60 Ϯ 0.99b (n ϭ 24) ͓25.5Ð27.5͔ development Pre-oviposition period 20.13 Ϯ 1.64a (n ϭ 22) ͓18Ð23͔ 20.10 Ϯ 1.32a (n ϭ 24) ͓18Ð22͔ 10.43 Ϯ 1.40a (n ϭ 23) ͓9Ð12͔ 10.20 Ϯ 1.62a (n ϭ 24) ͓8Ð13͔ Total development 90.20 Ϯ 2.56a (n ϭ 22) ͓88Ð94͔ 76.67 Ϯ 2.58b (n ϭ 24) ͓73.5Ð80.5͔ 38.86 Ϯ 2.48a (n ϭ 23) ͓36Ð42͔ 36.80 Ϯ 1.89a (n ϭ 24) ͓34.5Ð40.5͔ (Life cycle) Downloaded from https://academic.oup.com/ee/article/40/6/1541/532414 by guest on 23 September 2021 ͓͔: maximum and minimum value, n: number of cohort adults, values of the same row followed by the same small letter are not signiÞcantly different, TukeyÐKramer HSD Test, a ϭ 0.05. crataegi. Aphis fabae was reared on seedlings of Vicia Values of standard errors (SE) for parameters t and faba L. (Leguminosae) at 22ЊC, 60 Ϯ 5% RH, and a ⌲ were calculated from equations of Campbell et al. photoperiod of 16:8 (L:D) h, whereas D. crataegi was (1974): reared on pumpkins Cucurbita moschata (Duchesne ex Lam.) (Cucurbitaceae) at 25ЊC, 60 Ϯ 5% RH, and y s2 S.E 2 S.E ϭ m ͱ ϩ ͩ bͪ ϭ b a photoperiod of 16:8 (L:D) h. S.Et and S.EK 2 b N ϫ ym2 b b Experiments for thermal requirements and temperature effect on developmental duration of all devel- where ym is the sample mean (mean value rate of opmental stages of H. axyridis started with eggs of development as derived from the linear equation y ϭ mated females, which were reared on either aphid aϩbT), b is the linear equation parameter, s2 is the species in cylindrical Plexiglas cages (30 cm in diam- residual mean square, ⌵ is the sample size (number of eter, 50 cm in length) (Iperti and Burn 1969) at four different temperatures used during study). constant temperatures (15ЊϮ0.5Њ,20ЊϮ0.5Њ,25ЊϮ Data on developmental duration of all immature 0.5Њ, and 30 ЊϮ 0.5ЊC), 60 Ϯ 5% RH, and a photoperiod stages and pre-oviposition period were subjected to of 16:8 (L:D) h. The developmental duration of egg, Analysis of Variance with ␣ ϭ 0.05 and means were larval, and pupal stage as well as the pre-oviposition separated using the TukeyÐKramer honestly signiÞ- period was measured for individuals reared on A. fabae cant difference (HSD) Test (Sokal and Rohlf 1995) or D. crataegi in petri dishes (9 cm in diameter), at the using JMP. aforementioned temperatures. In total, 25 petri dishes with single individuals were used for each aphid spe- Results ciesÐtemperature combination. Measurements were recorded every 12 h. The duration of all developmental stages of H. axy- After measurement, individuals were supplied with ridis fed on A. fabae and D. crataegi at four constant up to 100 aphids per petri dish to secure food abun- temperatures (15Њ,20Њ,25Њ and 30ЊC) are presented at dance and avoid the effects of lack of food on the Table 1. Development of all immature stages of H. duration of development, as is reported for H. axyridis axyridis was signiÞcantly shorter on D. crataegi than (Hukusima and Ohwaki 1972) and other coccinellids on A. fabae prey at most temperatures. In the rest of in many studies (Hodek and Hone˘k 1996). The offered the cases, the development of the predator was rela- quantity of food in the current study (up to 100, per tively shorter when fed on D. crataegi, but these dif- individual, twice per day) is known to be the maxi- ferences were not proven to be statistically signiÞcant. mum daily prey consumption of larvae and adults by The mean total preimaginal developmental duration H. axyridis when fed on A. fabae and D. crataegi of H. axyridis on D. crataegi (12.6Ð56.6 d) was signif- (Stathas et al., 2011). icantly shorter than on A. fabae (13.7Ð70.2 d), at 15Њ, Statistical Analysis. Estimation of lower develop- 20Њ and 30ЊC (Table 1). The duration of pre-oviposi- mental threshold t and thermal constant K and their tion period of H. axyridis was 20.1, 10.4, 5.2 and 4.6 d standard errors was based on the linear model by on A. fabae and 20.1, 10.2, 7.9 and 4.1 d on D. crataegi Campbell et al. (1974) (y ϭ a ϩ bT, where y is the rate at 15Њ,20Њ,25Њ and 30ЊC, respectively and it was sig- of development at temperature T, and ␣ and b are niÞcantly longer on D. crataegi than on A. fabae at 25ЊC constants) using the statistical program JMP (Sall et al. (Table 1). The life cycle duration of the predator at 2001). The regression line was extrapolated and met 15ЊC and 30ЊC was shorter on D. crataegi (76.7 and abscissa at the developmental zero t, which was cal- 16.6 d, respectively) than on A. fabae (90.2 and 18.3 d, culated from t ϭ -a/b. The total quantity of thermal respectively) but it did not differ signiÞcantly be- energy required to complete development, the ther- tween the species at 20ЊC (36.8Ð38.9 d) or 25ЊC (24.0Ð mal constant K, was calculated from the reciprocal of 24.9 d) (Table 1). the slope of the regression line (1/b) (Wigglesworth Linear regression equations of developmental rate 1953, Campbell et al. 1974). of H. axyridis fed on the two aphid species, lower December 2011 STATHAS ET AL.: TEMPERATURE AND PREY EFFECT ON H. axyridis 1543

Table 1. Continued

25ЊC30ЊC A. fabae D. crataegi A. fabae D. crataegi 3.00 Ϯ 0.14a (n ϭ 25) ͓2.5Ð3.5͔ 2.85 Ϯ 0.47a (n ϭ 25) ͓2.5Ð4͔ 2.50 Ϯ 0.21a (n ϭ 25) ͓2Ð3͔ 2.00 Ϯ 0.19b (n ϭ 25) ͓1.5Ð2.5͔ 2.73 Ϯ 0.34a (n ϭ 24) ͓2.5Ð3.5͔ 2.27 Ϯ 0.47b (n ϭ 24) ͓2Ð3͔ 1.76 Ϯ 0.31a (n ϭ 24) ͓1Ð2͔ 1.60 Ϯ 0.21a (n ϭ 24) ͓1.5Ð2͔ 1.84 Ϯ 0.29a (n ϭ 24) ͓1Ð2͔ 1.36 Ϯ 0.50b (n ϭ 24) ͓1Ð2͔ 1.38 Ϯ 0.38a (n ϭ 24) ͓1Ð2͔ 1.35 Ϯ 0.38a (n ϭ 24) ͓1Ð2͔ 2.17 Ϯ 0.24a (n ϭ 24) ͓2Ð2.5͔ 2.20 Ϯ 0.79a (n ϭ 24) ͓1Ð4͔ 1.61 Ϯ 0.36a (n ϭ 23) ͓1Ð2͔ 1.21 Ϯ 0.26b (n ϭ 24) ͓1Ð1.5͔ 4.37 Ϯ 0.44a (n ϭ 24) ͓4Ð5.5͔ 5.00 Ϯ 0.93a (n ϭ 24) ͓4Ð7͔ 3.67 Ϯ 0.45a (n ϭ 23) ͓3Ð4.5͔ 3.17 Ϯ 0.25b (n ϭ 24) ͓3Ð3.5͔ 4.85 Ϯ 0.29a (n ϭ 24) ͓4.5Ð5.5͔ 4.11 Ϯ 0.33b (n ϭ 24) ͓4Ð5͔ 3.47 Ϯ 0.13a (n ϭ 23) ͓3Ð3.5͔ 3.54 Ϯ 0.33a (n ϭ 24) ͓3Ð4͔ 18.75 Ϯ 0.29a (n ϭ 24) ͓18.5Ð19͔ 17.56 Ϯ 1.27a (n ϭ 24) ͓15.5Ð19͔ 13.75 Ϯ 0.27a (n ϭ 23) ͓13.5Ð14͔ 12.56 Ϯ 0.46b (n ϭ 24) ͓12Ð13͔

5.25 Ϯ 0.87a (n ϭ 24) ͓4.5Ð6.5͔ 7.92 Ϯ 1.62b (n ϭ 24) ͓6Ð11͔ 4.58 Ϯ 0.66a (n ϭ 23) ͓3.5Ð5.5͔ 4.06 Ϯ 0.17a (n ϭ 24) ͓4.0Ð4.5͔ 24.00 Ϯ 0.71a (n ϭ 24) ͓23.5Ð25͔ 24.94 Ϯ 1.64a (n ϭ 24) ͓22.5Ð27.5͔ 18.33 Ϯ 0.75a (n ϭ 23) ͓17.5Ð19.5͔ 16.61 Ϯ 0.55b (n ϭ 23) ͓16Ð17.5͔ Downloaded from https://academic.oup.com/ee/article/40/6/1541/532414 by guest on 23 September 2021

developmental thresholds t and thermal constants K This Þnding coincides with data on other aphidopha- (degree-days) of each developmental stage are pre- gous coccinellid species (Hodek and Hone˘k 1996). sented in Table 2. CoefÞcient of determination (R2) The differences between the temperature require- for the development of H. axyridis fed on A. fabae ments of the developmental stages of H. axyridis could ranged between 0.9677 (pre-oviposition period) and be attributed to differences in the effect of tempera- 0.9999 (pupa) whereas the development of the pred- ture on their metabolism. Acar et al. (2004) showed ator fed on D. crataegi ranged between 0.9041 (L2) that adults and second instar larvae of H. axyridis and 0.9987 (total preimaginal development). These exposed to temperatures from 0 to 40ЊC, at 5ЊC inter- high rates of R2 indicate that the linear model de- vals, were stressed at 35ЊC (increase of metabolic heat scribed well the developmental rate of H. axyridis on and CO2 production rates) and experienced high mor- both aphids within the temperature regime of the tality at 40ЊC, but all the other developmental stages study (15Ð30ЊC). (third and fourth instar larvae, pupae) tolerated these The lower developmental threshold of H. axyridis temperatures. ranged between 10.2ЊC (egg) and 11.9ЊC (pupa), Pre-oviposition period of H. axyridis decreased with when fed on A. fabae, and between 8.2ЊC (L1) and increasing temperature on both prey species (also 12.1ЊC (L3), when fed on D. crataegi. The lower de- shown by Stathas et al. 2001) whereas at 25ЊCitwas velopmental threshold t of total preimaginal develop- longer when the prey was D. crataegi (7.9 d) compared ment and life cycle duration of H. axyridis was found with A. fabae (4.6 d). Pre-oviposition period of H. relatively lower (10.8 and 11.0ЊC, respectively) on D. axyridis lasted 7.2 d when fed on A. fabae at 25ЊC and crataegi than on A. fabae prey (11.2 and 11.8ЊC, re- 4.6 d at 30ЊC, 65 Ϯ 1% RH, and a photoperiod of 16:8 spectively). Accordingly, the thermal constant K of (L:D) h, according to Stathas et al. (2001); it lasted total preimaginal development and life cycle duration 8Ð10 d when reared on eggs of the Mediterranean of H. axyridis was lower (243.6 and 333.2 DD, respec- ßour moth Ephestia kuehniella (Zeller) (Lepidoptera: tively) on prey D. crataegi than on A. fabae (258.2 and Pyralidae) (Brun 1993) and7donartiÞcial diet at 30ЊC 357.1 DD, respectively). (Hong and Park 1996). Thermal constant K of total pre-imaginal development of H. axyridis was lower (243.6 above lower Discussion developmental threshold of 10.8ЊC) on D. crataegi The life cycle duration of H. axyridis was compa- prey than on A. fabae (258.2 DD above lower devel- rable on either prey, D. crataegi or A. fabae, at 25ЊC opmental threshold of 11.2ЊC). In comparison with our (24.0 and 24.9 d, respectively), but it was shorter when results, pre-imaginal development of an Oregon pop- the predator fed on D. crataegi (16.6 d) than on A. ulation of H. axyridis was shown to require 267.3 DD fabae (18.3 d) at 30ЊC. Consequently, on the grounds above a lower developmental threshold of 11.2ЊC (La- of shorter development, D. crataegi should be a better Mana and Miller 1998), whereas a French population diet for H. axyridis compared with A. fabae at high required 231.3 DD above a lower developmental temperatures in the Þeld as well as for mass rearing of threshold of 10.5ЊC (Schanderl et al. 1985). Differ- the predator; the effect of temperature on other bio- ences in thermal requirements for development (t, K) logical parameters of the predator, such as fecundity, of H. axyridis between the prey species could be re- also should be considered. lated with food quality (prey), whereas discrepancies Developmental rate of H. axyridis increased with between studies could also associate with different temperature in a linear trend on either aphid prey (D. experimental conditions (i.e., relative humidity) (Hu- crataegi or A. fabae) within the temperature regime of kusima and Ohwaki 1972, Stathas 2000). Smith the study (15Ð30ЊC) for each developmental stage and (1965a,b,c) and Obrycki and Orr (1990) investigated overall the preimaginal development. However, the the effect of two aphid prey species [A. pisum and temperature requirements for development varied Rhopalosiphum maidis (Fitch) (Hemiptera: Aphidi- among stages of H. axyridis fed on either aphid species. dae] on the development of seven coccinellid species 1544 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 6

and found that the total developmental duration increased when the food was unsuitable. The preima- 2.1882 4.1704 6.5436 8.5646 6.1575 11.9695 27.8764 2.6974 5.8600 ginal development of the predator was shorter by 4.6 d SEM Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ

Ϯ when larvae fed on the green peach aphid M. persicae

K than when fed on eggs of the Angoumois grain moth Sitotroga cerealella (Olivier) (Lepidoptera: Gelechii- dae) at 20ЊC (Reznik 2010). Overall, our results suggest similar thermal requirements for the development of H. axyridis on A. fabae 0.7164 38.0060 2.09401.32561.7095 23.4631 0.3275 62.5383 2.6570 66.1459 243.5823 1.0702 80.9398 333.2435 1.15463.3223 35.7516 25.4469 SEM Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ and D. crataegi prey and also are in agreement with Ϯ

t data on other aphid species (LaMana and Miller 1998,

8.2582 9.2002 Schanderl et al. 1985). As H. axyridis seems to meet 11.3837 12.1298 11.1336 10.5424 10.8165 11.9695 11.0449

these thermal requirements for development in Downloaded from https://academic.oup.com/ee/article/40/6/1541/532414 by guest on 23 September 2021 Greece and it is known to be able to survive very low temperatures during winter (lower lethal temperature 2 0.9934 0.9887 0,9041 0.9406 0.9786 0.676 0.9987 0.9088 0.9860 was estimated at Ϫ16ЊC in Japan by Watanabe 2002) ϭ ϭ ϭ ϭ ϭ ϭ ϭ ϭ ϭ 2 2 2 2 2 2 2 2 2 and to migrate to overwintering sites in Asia and Ohio (Liu and Qin 1989, Sakurai et al. 1993, Kidd et al. 1995, LaMana and Miller 1996), further investigation is needed to explore the environmental reasons for the 0.3615 R 0.29950.2310 R 0.5170 R 0.17800.1594 R 0.0444 R 0.1479 R 0.0331 R R R difÞculties of this predator to establish in Greece. ϫϪ ϫϪ ϫϪ ϫϪ ϫϪ ϫϪ ϫϪ ϫϪ ϫϪ

at four constant temperatures (15, 20, 25, and 30°C) References Cited 0.0263 0.0280 0.03930 0.0426 0.0160 0.0151 0.0041 0.0124 0.0030

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Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ aphids. Infos (Paris). 94: 41Ð42. SEM)

Ϯ Campbell, A., B. D. Frazer, N. Gilbert, A. P. Gutierrez, and t M. Mackauer. 1974. Temperature requirements of some on the prey thermal constant (degree days). 10.2055 10.6993 11.6414 11.3393 11.0135 11.8750 11.1703 10.8333 11.7856 aphids and their parasites. J. Appl. Ecol. 11: 431Ð438. K: Davidson, J. 1944. On the relationship between tempera- C),

Aphis fabaeture and rate of Dysaphis crataegi development of insects at constant tem- o

2 peratures. J. Appl. Ecol. 13: 26Ð38. 0.9854 0.9768 0.9991 0.9987 0.9709 0.9999 0.9993 0.9677 0.9800

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