© 2006 The Authors Entomologia Experimentalis et Applicata 119: 207–211, 2006 207 Journal compilation © 2006 The Netherlands Entomological Society
Blackwell Publishing Ltd
Temperature effects on egg development of the rosy apple aphid and forecasting of egg hatch
B. Graf*, H.U. Höpli, H. Höhn & J. Samietz
Agroscope FAW, Swiss Federal Research Station for Horticulture, CH-8820 Wädenswil, Switzerland Accepted: 30 January 2006
Key words: Dysaphis plantaginea, Aphididae, Homoptera, phenology, modelling, control
Abstract The development of Dysaphis plantaginea (Pass.) (Homoptera: Aphididae) winter eggs was studied at six different constant temperatures ranging from 7.5 to 16.5 °C in order to improve the basis for phenological forecasts in early spring. The mortality was generally low at temperatures below 13.5 °C but increased considerably at 16.5 °C. The effect of temperature on development rates could be described with linear regression within the temperature range under study. The lower temperature threshold for development was estimated to be 4.0 °C and the thermal constant 140 day-degrees. A time-varying distributed delay approach was used to establish a temperature driven phenology model for winter egg hatch of D. plantaginea considering the intrinsic variability in development time. The model parameters such as temperature-dependent development times and corresponding variances were quantified based on the experimental data. When compared with independent observations on egg hatch under semifield conditions, the model gave satisfactory validation results. It can be used as forecasting tool for the optimal timing of monitoring and control measures for D. plantaginea in early spring.
Introduction
The rosy apple aphid, Dysaphis plantaginea (Pass.) (Homo- ptera: Aphididae), is one of the major insect pest species on apple in Europe (Hill, 1987). Even at low population densities, the economic damage can be considerable and treatments are recommended when only 1% of flower buds are infested in early spring (Graf et al., 1998, 1999). One to two aphicide applications are common in commercial apple orchards (Höhn et al., 1996). Due to improved efficacy, the first treatment is normally applied before bloom (Hull &
Starner, 1983). However, timing of monitoring and control measures is difficult at this time of the year. Moreover, the risk assessment based on visual counts is unreliable when done too early, as freshly hatched nymphs are hardly visible on newly opened buds. Furthermore, an early treatment may not give good results because most specific compounds are ineffective against winter eggs, and a late treatment may have a reduced efficacy because established colonies are partly protected in curled leaves. Therefore, monitoring and control measures need to be applied within the restricted time slot after the nymphs have hatched from winter eggs and before the first fundatrices begin to
reproduce. This period may last a couple of weeks or only a few days, depending on actual weather conditions.
The effect of temperature on the development of different mobile life stages of D. plantaginea has already been described on apple as its primary host (Graf et al., 1985) and on plantain as a secondary host (Blommers et al., 2004).
However, the development of winter eggs has not been investigated experimentally up to now. The objective of the present study was to develop a basis for a reliable, temperature-driven tool to forecast the phenology of D.
plantaginea in order to facilitate decision making of apple growers with respect to aphid control before bloom.
Materials and methods
Egg development and hatching were studied under six different temperature conditions, ranging from 7.5 to 16.5 °C.
The relationship between temperature and developmental rates was described by means of regression and used to assess the lower temperature threshold and the thermal constant for egg development. A phenology model for hatching of D. plantaginea winter eggs was developed using the time-varying distributed delay approach (Manetsch, 1976). The model parameters were quantified on the basis of the experimentally established relationship between
*Correspondence: E-mail: benno.graf@faw.admin.ch
208 Graf et al.
temperature and developmental rates. Observations on hatching of nymphs from winter eggs under semifield conditions from 2 years were used to validate model predictions.
Experiments to quantify temperature effects on egg development Apart from D. plantaginea, various other aphid species hibernate on apple, but the eggs of the different species cannot be differentiated with non-destructive methods.
This fact requires either the determination after hatching when eggs were collected in the field, or the production of winter eggs using a species-specific rearing system.
In a preliminary experiment (Series 1), twig samples with 2017 aphid eggs of a naturally occurring species mix- ture were enclosed in small plastic trays and kept humid with wet blotting paper. They were stored at 1 °C until the beginning of March and then exposed to 10 °C in a climate chamber. This temperature corresponds roughly to the long-term average field temperature in the apple produc- ing regions of central Switzerland during the time period of mid-March to mid-April. The eggs were examined daily and hatching nymphs were subsequently reared on apple seedlings until they could be determined according to literature descriptions (Baker & Turner, 1916; Rogerson, 1947; Bonnemaison, 1959; Stroyan, 1963).
For the main experiment (Series 2), a pure culture of D. plantaginea winter eggs was produced in order to avoid posthatching determination. Beginning in late spring of the preceding year with adult virgins from infested apple trees, the whole development cycle including the host changes from apple to plantain and back was reproduced under protected field conditions (Figure 1). Oviposition took place on encaged potted apple trees, which were sub- sequently dissected. As in the first series, the twig samples with the eggs were enclosed in humidified plastic trays and stored at 1 °C. By the end of February, 139, 133, 111, 145, and 132 D. plantaginea eggs were exposed to temperatures of 7.5, 10.6, 11.6, 13.5, and 16.5 °C, respectively, in climate chambers. The thermal threshold for development was expected to be close to 7.5 °C, and 16.5 °C was near the upper range of temperature measured from mid-March to mid-April in the apple producing regions of central Swit- zerland. Day length was kept constant in all chambers at 12 h using white fluorescent lighting (approximately 5000 lux). In daily observations, the eggs were examined indi- vidually and hatching of nymphs and duration of egg development was recorded.
Observations for model validation
In the winters of 2000/01 and 2001/02, 141 and 283 D. plantaginea eggs, respectively, were exposed to field conditions, and hatching of nymphs was monitored. Air
temperature was recorded continuously with a Hotdog®
micrologger (Elpro-Buchs, Buchs, Switzerland). The resulting data on hatching of nymphs was subsequently used for independent model validation.
Statistics and model development
The individual values of egg developmental duration recorded in the climate chambers were transformed to developmental rates (reciprocal values). Linear regression statistics (SPSS® 13.0, SPSS Inc., Chicago, IL, USA) were then applied to describe the rate of egg development as a continuous function of temperature. The thermal constant (i.e., the reciprocal of the regression slope), the thermal threshold (i.e., the x-intercept of the regression), and the corresponding standard errors were computed for winter egg development of D. plantaginea according to Campbell et al. (1974).
The time-varying distributed delay approach (Manetsch, 1976; Severini et al., 1990; Gutierrez, 1996) was used as the Figure 1 Rearing procedure for winter eggs of rosy apple aphid, Dysaphis plantaginea.
core element of the phenology model. In this approach, an Erlang density function is applied to reproduce the observed frequency distribution of the individual developmental times. In a poikilothermic development process, the mean transit time in calendar time units and its variance vary depending on temperature. In order to account for this fact, developmental time and variance are not considered as constants but as variables that are updated for each simu- lation step on the basis of the regression described pre- viously. The ratio between the square of the mean transit time in physiological time units (i.e., the thermal constant in day-degrees) and its variance specifies the order (k) of the delay and hence the number of first order differential equations required to generate the observed variability.
Each of these k first order differential equations represents an age class within the winter egg stage and describes the daily changes in this age class as:
Qi(t) stands for the proportion of eggs in age class i at time t. The parameter r(t) is the transition rate from age class i to age class i + 1 and corresponds to the developmental rate that is quantified with the linear regression describing winter egg development as function of temperature.
Individuals leaving the last age class are hatching nymphs.
The model uses air temperature as the driving variable to generate values for the parameter r(t) and to update age structure of the aphid population on an hourly basis start- ing 1 January. The algorithm of the model was written in Pascal with Delphi™ 6 (Borland® Inc., Cupertino, CA and Atlanta, GA, USA).
Results
Effect of temperature on egg development
From the two experimental series, a total of approximately 700 D. plantaginea winter eggs were observed to study the effect of temperature on development. At temperatures below 15 °C, mortality was low, slightly increasing from
5% at 7.5 °C to 8% at 10.6 and 11.6 °C and to 12% at 13.5 °C.
At 16.5 °C, mortality was considerably higher at 37%
(Table 1). The duration of egg development decreased with increasing temperature. Winter egg development took on average 36.7 days at 7.5 °C and 11.1 days at 16.5 °C.
The standard deviations slightly varied between 14 and 20% of the mean at the different temperatures (Table 1).
The observed hatching curves from Series 2 are plotted in Figure 2. At 16.5 °C, the first nymphs emerged after 7 days and the last 11 days later. With decreasing temperature, the beginning of hatching was delayed and the hatching period extended. At 7.5 °C, hatching began 16 days later and lasted 13 days longer than at 16.5 °C.
The mean developmental rates with the corresponding standard deviations are plotted against the six experimen- tal temperatures in Figure 3. Within the temperature range under study, the relationship is fairly linear and can be described with simple regression. From this regression a thermal threshold of 4.0 °C and a thermal constant of 140 day-degrees were calculated for winter egg develop- ment. Based on the ratio between the square of the thermal constant and its variance, the winter egg stage was divided into 30 age classes (30th order delay) in the model in order to reproduce the observed variability of egg hatching.
Table 1 Effect of temperature on duration of egg development and survival of rosy apple aphid, Dysaphis plantaginea
Series no.
Temperature (°C)
Eggs exposed (no.)
Nymphs hatched (no.)
Survival rate (%)
Duration ± SD (days)
2 7.5 139 132 95 36.7 ± 5.2
1 10.0 — 40 — 24.5 ± 3.6
2 10.6 133 122 92 22.9 ± 4.1
2 11.6 111 102 92 19.3 ± 3.7
2 13.5 145 128 88 14.5 ± 2.5
2 16.5 132 83 63 11.1 ± 2.2
dQ (t)
dti =r(t) ×[Qi−1( ) t −Q (t)i ].
Figure 2 Cumulative egg hatch of rosy apple aphid, Dysaphis plantaginea, at five different constant temperatures (Series 2).
210 Graf et al.
Validating the phenology model for winter egg hatching
For validation, the model was run with hourly average outdoor temperature data recorded in the winters of 2000/
01 and 2001/02, and the output was compared with the corresponding observations on hatching of nymphs in field cages (Figure 4). Despite the very different weather conditions, the model was able to capture the general hatching pattern of D. plantaginea in both years. In 2001, the first nymphs emerged on 16 March while in 2002 hatching started between 1 and 7 March. In 2001, 50% of the overwintering population became nymphs until 23 March while at the same date in 2002 hatching was roughly terminated. In both years, but particularly in 2002, cool periods caused a slowdown or even a break of hatching effects, which were well reproduced by the model. The deviation of the model predictions from observations was generally within the range of ± 1 day. The forecasting error was only larger (3 – 4 days) at the end of the hatching period in 2001 and the beginning in 2002.
Discussion
According to our observations, winter egg mortality of D. plantaginea seems to be strongly affected by increasing temperatures. Survival was more than 90% at temperatures below 11.6 °C, but decreased drastically above 13.5 °C.
Graf et al. (1985) observed a similar pattern for nymphs of the first generation where mortality rates were less than 10% at 11 °C but reached 30 – 40% at temperatures above 15 °C. This indicates that the early development stages of D. plantaginea have a rather low temperature optimum, and high temperatures in early spring may significantly reduce population growth.
The mean duration of egg development and the length of the hatching period decreased inversely proportional with increasing temperature. At 7.5 °C, egg development took on average 36.7 days and the hatching period lasted 24 days. At 16.5 °C, mean duration of egg development was just 11.1 days and the last egg hatched 11 days after the first. Bonnemaison (1959) reported a hatching period of 10 –12 days at 20 °C. Extrapolating from our data, we would expect a shorter hatching period. However, considering the fact that 20 °C may be above the optimum temperature, as Figure 3 Temperature effect on developmental rates of rosy apple
aphid winter eggs. Mean rates (± SE) under constant temperatures in Series 1 (white symbol) and Series 2 (black symbols), and linear regression (line) describing developmental rates as a function of temperature (slope ± SE = 0.00713 ± 0.00015; intercept ± SE = −0.0287 ± 0.0018; r2 = 0.80; lower temperature threshold ± SE = 4.02 ± 0.06 °C; thermal constant
± SE = 140 ± 3 day-degrees).
Figure 4 Validation of the phenology model for rosy apple aphid egg hatch – predicted (Sim) and observed (Obs) egg hatch under field conditions in 2001 and 2002.
the mortality data suggest, our results may well agree with his observations.
With 4.0 °C, the thermal threshold for D. plantaginea winter egg, development is just slightly lower than the thermal threshold for the following nymphal stages, which was found to be 4.5 °C (Graf et al., 1985). It is also in the range of the threshold for juvenile development on the summer host plantain, which was reported to be 5.1 °C (Blommers et al., 2004). As it is also very close to 4.4 °C, the developmental threshold of apple (Baumgärtner et al., 1983), rosy apple aphid seems to be well adapted to the phenology of its winter host plant in early spring.
The thermal constant for egg development is 140 day- degrees above the lower thermal threshold of 4.0 °C. This corresponds with the empirically approximated mean duration of egg development of 143 day-degrees reported in an earlier study, which was based on field observations on hatching of winter eggs (Graf, 1984).
Using the above-mentioned parameters, the simple temperature-driven phenology model presented here is able to reproduce the observed hatching pattern of rosy apple aphid winter eggs in a reasonable manner. Model predictions corresponded largely with independent obser- vations made in 2 years with distinct weather conditions.
Provided air temperature recordings and corresponding temperature forecasts are available, the model allows to predict the beginning, progression, and end of egg hatch- ing in various locations. In combination with the nymphal developmental parameters established by Graf et al. (1985), the current model can be used to determine the optimal time window for monitoring and control measures for rosy apple aphid.
References
Baker AC & Turner WF (1916) Rosy apple aphis. Journal of Agricultural Research 7: 321–356.
Baumgärtner J, Stoll K & Pfammatter W (1983) Studium tempera- turabhängiger Phänologiemodelle zur Beschreibung der Golden- Delicious-Entwicklung in schweizerischen Apfelanlagen.
Schweizerische Landwirtschaftliche Forschung 22: 247–252.
Blommers LHM, Helsen HHM & Vaal FWNM (2004) Life history data of rosy apple aphid Dysaphis plantaginea (Pass.) (Homopt., Aphididae) on plantain and as migrant to apple.
Journal of Pest Science 77: 155 –163.
Bonnemaison L (1959) Le puceron cendré du pommier (Dysaphis plantaginea Pass.) – Morphologie et biologie – Méthodes de lutte. Annales des Épiphyties 10: 257–320.
Campbell A, Frazer BD, Gilbert N, Gutierrez AP & Mackauer M (1974) Temperature requirements of some aphids and their parasites. Journal of Applied Ecology 11: 431– 438.
Graf B (1984) Analyse der Populationsdynamik von Dysaphis plantaginea (Pass.), Rhopalosiphum insertum (Walk.) und Aphis pomi (De Geer). (Homoptera: Aphididae) auf dem Apfelbaum in einer ostschweizerischen Obstanlage. Diss. ETH no. 7670, ETH, Zürich, Switzerland.
Graf B, Baumgärtner J & Delucchi V (1985) Life table statistics of three apple aphids, Dysaphis plantaginea, Rhopalosiphum insertum and Aphis pomi (Homoptera, Aphididae), at constant temperatures. Journal of Applied Entomology 99: 285 –294.
Graf B, Höhn H & Höpli HU (1998) Sind Sommerbehandlungen gegen die Mehlige Apfelblattlaus gerechtfertigt? Ansatz für eine zeitbezogene Schadenschwelle Schweizerische Zeitschrift für Obst- und Weinbau 134: 277–279.
Graf B, Höhn H & Höpli HU (1999) Optimising the control of rosy apple aphid Dysaphis plantaginea (Pass.) (Homoptera:
Aphididae). IOBC Wprs Bulletin 22(7): 71–76.
Gutierrez AP (1996) Applied Population Ecology: A Supply- Demand Approach. John Wiley & Sons, New York, NY, USA.
Hill DS (1987) Agricultural Insect Pests of Temperate Regions and Their Control. Cambridge University Press, Cambridge, UK.
Höhn H, Höpli HU & Graf B (1996) Mehlige Apfelblattlaus:
Befallsentwicklung und Bekämpfung. Schweizerische Zeitschrift für Obst- und Weinbau 132: 60 – 62.
Hull LA & Starner VR (1983) Effectiveness of insecticide applica- tions timed to correspond with the development of rosy apple aphid (Homoptera, Aphididae) on apple. Journal of Economic Entomology 76: 594 –598.
Manetsch TJ (1976) Time-varying distributed delays and their use in aggregative models of large systems. IEEE Transactions on Systems, Man, and Cybernetics 6: 547–553.
Rogerson JP (1947) The oat bird-cherry aphis, Rhopalosiphum padi L., and comparison with R. crataegellum Theo. (Hemiptera, Aphididae). Bulletin of Entomological Research 38: 157–176.
Severini M, Baumgärtner J & Ricci M (1990) Theory and practice of parameter estimation of distributed delay models for insect and plant phenologies. Meteorology and Environmental Sciences (ed. by R Guzzi, A Navarra & J Shukla), pp. 676 –719.
World Scientific Publishing, Singapore.
Stroyan HLG (1963) A Revision of the British Species of Dysaphis Börner. Part II: The Subgenus Dysaphis Sensu Stricto. Ministry of Agriculture, Fisheries and Food, London, UK.
